research article intestinal parasites of owned dogs and cats...
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Research ArticleIntestinal Parasites of Owned Dogs and Cats from Metropolitanand Micropolitan Areas Prevalence Zoonotic Risks and PetOwner Awareness in Northern Italy
Sergio Aurelio Zanzani1 Alessia Libera Gazzonis1 Paola Scarpa1 Federica Berrilli2 andMaria Teresa Manfredi1
1 Department of Veterinary Science and Public Health Universita degli Studi di Milano 20133 Milan Italy2 Department of Public Health Universita di Tor Vergata 00133 Rome Italy
Correspondence should be addressed to Maria Teresa Manfredi mariateresamanfrediunimiit
Received 28 February 2014 Accepted 3 April 2014 Published 28 April 2014
Academic Editor Stefano DrsquoAmelio
Copyright copy 2014 Sergio Aurelio Zanzani et al This is an open access article distributed under the Creative Commons AttributionLicense which permits unrestricted use distribution and reproduction in any medium provided the original work is properlycited
Intestinal parasites of dogs and cats are cosmopolitan pathogens with zoonotic potential for humans Our investigation consideredtheir diffusion in dogs and cats from northern Italy areas specifically the metropolitan area of Milan and twomicropolitan areas ofneighboring provinces It included the study of the level of awareness in pet owners of the zoonotic potential from these parasitesA total of 409 fresh fecal samples were collected from household dogs and cats for copromicroscopic analysis and detection ofGiardia duodenalis coproantigens The assemblages of Giardia were also identified A questionnaire about intestinal parasitesbiology and zoonotic potential was submitted to 185 pet ownersThe overall prevalence of intestinal parasites resulted higher in cats(4737minus6042) and dogs (5741minus4302) from micropolitan areas than that from the metropolis of Milan (dogs 119875 = 2816cats 119875 = 3258 ) The zoonotic parasites infecting pets under investigation were T canis and T cati T vulpis Ancylostomatidaeand G duodenalis assemblage A Only 4919 of pet owners showed to be aware of the risks for human health from canine andfeline intestinal parasites Parasitological results in pets and awareness determination in their owners clearly highlight how the roleof veterinarians is important in indicating correct and widespread behaviors to reduce risks of infection for pets and humans inurban areas
1 Introduction
Intestinal parasites of dogs and cats are diffused worldwideThough some differences can be noticed between stray andshelter dogs and even in pets in general veterinarian concernfor these parasites is still living matter due to their zoonoticpotential and their significant pathogen effects on carnivorehosts [1] The overall prevalence of intestinal parasites inpet dogs and cats varies considerably In fact recent studiesrevealed percentages from 125 to 344 in dogs and from101 to 228 in cats High variability also relates to singlespecies or taxon [2ndash6] Giardia duodenalis appeared to be themost frequent parasite with prevalence values varying from13 to 2478 (dogs) and from 0 to 2031 (cats) [5 7ndash10] As regards helminthic infections hookworms ascarids
andwhipwormswere themost frequent intestinal parasites indogs [2 3 5 6 8 10ndash12] In cats Toxocara cati was the mostcommon helminth with prevalence values ranging from 15to 10 [7 8 10 13]
Several causes might have affected observed variabilityin intestinal parasite infections such as host individualfeatures management heartworm prophylactic treatmentsand diagnostic techniques [2 5ndash7 9 11 14 15] Furthercanine and feline helminths are susceptible to the effectsof environmental condition and to climate change due totheir developmental stages and their survival periods in theenvironment [1 16 17]
To date domestic carnivores still represent an importantsource of zoonotic helminths among which the most com-mon Toxocara species are far-back well known as regards
Hindawi Publishing CorporationBioMed Research InternationalVolume 2014 Article ID 696508 10 pageshttpdxdoiorg1011552014696508
2 BioMed Research International
their impact on human health [1 18ndash21] As to Giardiaseveral surveys showed that carnivore pets host-specific (CD F) or zoonotic assemblages (A and B) of G duodenaliswhose prevalence values strongly depend on the diagnostictechniques used for example PCR and antigen detectionseemed more sensitive than copromicroscopic analysis [1022ndash24]
Lombardy is the region of northwestern Italy withthe largest population of companion animals representingabout 15 of their overall presence in Italy (data fromNational CompanionRegistry httpwwwsalutegovitanag-caninapublic newAdapterHTTP) Nevertheless only fewdata are available on the occurrence of intestinal parasitesin companion animals in this area Moreover they are notupdated or just limited to stray cats [25 26] Major aim of thissurvey was to determine the prevalence of intestinal parasitesin three groups of dogs and cats from the metropolitanarea of Milan and two micropolitan areas at the boundariesof two neighboring provinces where pets can have accessor live outdoor more easily than those in Milan Influenceon prevalence of individual pet features (age gender sizeand presenceabsence of clinical signs) and management(householdoutdoor husbandry and heartworm effectivetreatment) were also considered Furthermore owner aware-ness mainly about zoonotic potential of intestinal parasitesaffecting their pets was investigated by a specifically designedquestionnaire
2 Materials and Methods
21 Study Area and Sampling The survey was carried outin the northwestern Italian region of Lombardy (latitude45∘401015840N longitude 9∘301015840E) Climate is mainly continentalexcept above 1500m asl where the typical features of alpineareas are recognized Consequently temperatures show highvariability with a maximumminimum annual mean of350∘C (even less in the Alpine areas) The mean annualrainfall is 600ndash700mm in the southern planes and 2000mmin the Alpine or Prealpine areas
The study included dogs and cats from three majorprovinces of Lombardy Milan (latitude 45∘301015840N longitude9∘301015840E) Bergamo (latitude 45∘501015840N longitude 09∘481015840E)and Brescia (latitude 45∘551015840N longitude 10∘151015840E) A total of202 and 207 fecal samples were collected from owned pets inthe metropolitan area of Milan (MT) and in the micropolitanareas of Bergamo (MC 1) and Brescia (MC 2) respectivelyIn the latter areas cities with 10000 to 50000 residents wereincluded (MC 1 23 MC 2 15) From January 2010 to October2011 a total of 409 fresh fecal samples were collected byowners or veterinarians from household dogs (119899 = 253)and cats (119899 = 156) that underwent clinical examinationin two different veterinary clinics located in the namedareas At clinical examination data about individual features(age sex breed and presenceabsence of clinical signs) andmanagement (indooroutdoor housing cohabitation withother dogs andor cats and effective prophylaxis againstDirofilaria immitis in dogs and in cats older than 12 months)of animals were recorded by clinicians Further data (gender
age education level and number of family components)about 207 owners were obtained
22 Fecal Examination Feces were stored at +4∘C and exam-ined within 48 hours Macroscopic examination was firstlyperformed for the detection of proglottids of cestodes Sub-sequently each fecal sample was divided into two aliquotsIn order to detect parasite eggs and oocysts one aliquot wassubjected to microscopic analysis by centrifugation-flotationtechnique with sucrose and sodium nitrate solution (specificgravity 1360)The parasite eggs were differentiated accordingto their morphologic characteristics Quantitative measure-ment of helminth infection (EPG) was not implementedThe second aliquot was used to detect coproantigens of Gduodenalis by a commercially available immunochromato-graphic test (RIDA QUICK Giardia cassette R-BiopharmAG Germany)
23 PCRAssay A group of selectedGiardia-positive sampleswere processed by a commercial kit (QIAamp DNA StoolMini Kit QIAGEN Valencia CA USA) for DNA extractionA nested PCR protocol was applied to amplify a fragment ofthe small subunit ribosomal RNA (SSUrRNA) Giardia geneFor external PCR the forward primer RH11 (51015840-CATCCG-GTCGATCCTGCC-31015840) and the reverse primer RH4 (51015840-AGTCGAACCCTGATTCTCCGCCCAGG-31015840) designedby Hopkins et al [27] were used the internal primers(GIAR-F forward 31015840-GACGCTCTCCCCAAGGAC-51015840 andGIAR-R reverse 51015840-CTGCGTCACGCTCG-31015840-) designedby Read et al [28] were used Amplification productswere run on 2 ethidium bromide agarose gels and visu-alized under ultraviolet light Bands were excised fromagarose gels and purified using a QIAquick Gel Extrac-tion Kit (QIAGEN Valencia CA USA) Amplificationproducts were sent to an external laboratory for sequenc-ing BLAST analysis of the GeneBank database was per-formed to identify G duodenalis assemblages from obtainedsequences
24 Questionnaire Survey A questionnaire designed to knowowner general information on canine and feline intestinalparasites together with their awareness of risks for animal andhuman health from these parasites was submitted A total of185 questionnaires were answered namely by 125 dog ownersand 60 cat owners
25 Statistical Analysis We defined prevalence after Bush etal [29] Prevalence of each parasite within categories of theconsidered variables was compared using a Chi-Square testand results were retained significant when the null hypothesishad a probability less than 119875 lt 001 or 119875 lt 005 Since preva-lence of single taxon was too low for a risk factor analysisdata on infection with helminths andor Giardia were alsocombined to the purpose Labelling an animal as positive iftested positive for at least one species of parasite preliminaryunivariate logistic regression was performed considering thefollowing independent variables gender age (le12 monthsold gt12 months old) habitation (metropolitan area and
BioMed Research International 3
micropolitan areas 1 and 2) management (outdoor or house-hold) breed size (small medium or large) and cohabitationwith other animals Variables showing a 119875 value lt 020were included in the multivariate regression model Back-ward elimination was used to determine which variablesentered the final model setting at 005 the level of signifi-cance to be included in the model The association betweeninfection and gastrointestinal symptoms was analyzed byChi-Square test Further the owner features (gender ageeducational qualification family components and presenceof young lt15 years old) were compared for ldquoinfectedrdquo or ldquonotinfectedrdquo pets by Chi-Square test All statistical analysis wasperformed using SPSS v190 (IBMCorp ArmonkNYUSA)
3 Results
31 Parasitological Analysis Theoverall prevalence of intesti-nal parasites resulted higher in dogs and cats from microp-olitan areas (dogs 119875 = 5741 and 119875 = 4302 respcats 119875 = 4737 and 119875 = 6042 resp) than those fromthe metropolitan area of Milan (dogs 119875 = 2816 cats119875 = 3258) In general a scarce parasitofauna was detectedin most cases of dogs and cats They were frequently infestedby one parasite species (dogs 119875 = 7794 cats 119875 = 7368)or by two parasite species (dogs 119875 = 2206 cats 2632)In both dogs and cats G duodenalis was the most prevalentspecies detected Itsprevalence values accounted as followsdogs 2037 (MC 1) and 2558 (MC 2) 1605 (MT) cats3684 (MC 1) 2500 (MC 2) and 247 (MT) T canisresulted to be the most common helminth in dogs from MC1 (119875 = 2222) with a lower prevalence in those from MC 2(119875 = 930) and MT (119875 = 448) T cati showed its highestprevalence values in cats fromMC 2 (119875 = 2239) and lowervalues in those from MC 1 (526) and MT (119875 = 562)(Table 1)
Considering the univariate logistic regression analysisin dogs pet age was the strongest predictor of intestinalparasite infection the odds of a dog being infected were044 smaller in animals gt12 months old (Table 2) Dogsfrom the metropolitan area of Milan were significantly lesssusceptible to intestinal parasites than dogs from MC 2 (OR= 1947) or MC 1 (OR = 3476) (Table 2) Besides husbandrymanagement (single or multiple animals in the same house)had impressive effect on the infection multiple dogs showedhigher infection risk than single dogs (OR = 2059) Genderbreed size and housingmanagement (household or outdoor)had no impressive effect on the infection In cats thepredominant predictors of intestinal parasite infection werehabitation age and housing Specifically older cats were lesslikely infected than younger ones (OR = 0347) and cats fromthe metropolitan area of Milan showed less susceptibility toinfections than cats from the micropolitan areas (OR = 2100and OR = 3561) (Table 2) The age and husbandry variablesfor dogs and habitation and age for cats entered in the finalmultivariable model (Table 3)
Subsequently data of each taxon was analyzed dogslt12 months old showed significantly a higher prevalence ofinfection byT canis (119875 = 2065)Cystoisospora (870) and
byGiardia duodenalis (119875 = 2717) than older ones (Table 4)Cystoisospora was more commonly found in household dogsthan in dogs living outdoor Dogs with multiple husbandrieswere frequently infected by Ancylostomatidae and T vulpis(Table 4)
In cats T cati and T leonina infection prevalence resultedsignificantly higher in young animals than in adult ones Tleonina was more commonly found in cats living outdoorthan in household cats (Table 4)
The dogs and cats in this study were presented to twoVeterinary Clinics for routine control or vaccination clinicalfindings were absent in most cases except for 2071 ofdogs and 1343 of cats with gastrointestinal signs suchas diarrhea vomiting nausea or lack of appetite Out ofthem 4483 of dogs and 4444 of cats had intestinalparasites (Table 5) A large percentage of the sampled dogsreceived regular prophylaxis againstD immitis (119875 = 7042)with selamectin in spot-on formulation (5417) ivermectin(3958) per os or moxidectin (625) in injectable formu-lation Thus only a few dogs were infected by helminthsIn particular dogs under selamectin treatment were infectedwithT vulpis (119899 = 4) Ancylostomatidae (119899 = 2) T canis (119899 =1) and Toxascaris leonina (119899 = 1) dogs under ivermectintreatment were infected with T canis (119899 = 2) and T vulpis(119899 = 1) one dog under moxidectin treatment was infectedwith T canis
Only 2 adult cats received proper prophylaxis againstheartwormswith a spot-on formulation containing selamect-in one of them were infected by Dipylidium caninum
32 Genotyping of Giardia Duodenalis Fifty-four Giardia-positive samples (37 dogs and 17 cats) were processed for thenested PCR protocol In dogs prevalence of G duodenalisassemblages obtained from 1137 dogs showed the occur-rence of C and D assemblages precisely with percentagesof 545 (C) and 4545 (D) In cats A and D assemblageswere detected with percentages of 833 (A) and 166(D)
33 Survey on Health Risk Awareness in Pet Owners Aspecifically designed questionnaire on health risk awarenesswas handed out among owners whose pets were underour investigation Results from filled-in forms showed that7189of them correctly identified the common transmissionroute of intestinal parasites that is fecal contamination offood or of other ingested materials While 973 of themthought that direct contact between healthy and infectedanimal triggers infection 1838 totally ignored the wayof transmission of intestinal parasites 6090 of ownersidentifying in fecal contamination the route of infection fordogs and cats retained that parasite eggs could stay infectivefor long About the possibility of transmission of intestinalparasites to puppieskittens by bitchesqueens only 4811 ofowners answered affirmatively while 1567 of them had noanswer When asked about human health risks due to canineand feline intestinal parasites 4919 showed awareness ofthe occurrence 3567 answered that no risk is given and
4 BioMed Research International
Table 1 Prevalence () and confidence interval (CI) of intestinal parasites in 253 owned dogs and 156 owned cats in northern Italy
Parasites Metropolitan area Micropolitan area 1 Micropolitan area 2 (CI) (CI) (CI)
Dogs
Toxocara canis 448 2222 930(209ndash1086) (1077ndash3668) (304ndash1557)
Toxascaris leonina 0 370 0(0-0) (0ndash891) (0-0)
Ancylostomatidae 097 556 349(017ndash529) (0ndash1187) (0ndash745)
Trichuris vulpis 608 1111 581(333ndash1337) (245ndash1977) (077ndash1086)
Strongyloides stercoralis 194 0 0(053ndash68) (0-0) (0-0)
Eucoleus aerophilus 097 0 0(017ndash529) (0-0) (0-0)
Dipylidium caninum 0 286 0(0) (010ndash562) (0-0)
Cystoisospora sp 097 370 698(017ndash529) (0ndash891) (148ndash1247)
Giardia duodenalis 1605 2037 2558(1056ndash2485) (927ndash3147) (1617ndash3499)
Overall prevalence 2816 5741 4302(2038ndash3751) (4378ndash7103) (3235ndash5370)
Cats
Toxocara cati 562 526 2239(242ndash1249) (0ndash1632) (1241ndash3237)
Toxascaris leonina 0 526 896(0-0) (0ndash1632) (212ndash1580)
Ancylostomatidae 112 0 208(002ndash609) (0-0) (0ndash627)
Trichuris vulpis 0 0 208(0-0) (0-0) (0ndash627)
Dipylidium caninum 0 286 448(0-0) (010ndash562) (0ndash943)
Spirometra 112 0 0(002ndash609) (0-0) (0-0)
Cystoisospora sp 112 526 417(002ndash609) (0ndash1632) (0ndash1003)
Toxoplasma-like 112 0 0(002ndash609) (0-0) (0-0)
Giardia duodenalis 2247 3684 2500(1504ndash3218) (1296ndash6073) (1229ndash3771)
Overall prevalence 3258 4737 6042(2374ndash4286) (2264ndash7209) (4607ndash7477)
1514 declared they had even never considered such prob-ability Of the ninety owners aware of zoonoses risk 7252of them thought that the most common source of infectionis contaminated food 23 answered that transmission ofparasites to humans is caused by direct contact with petswhile 440 had no idea Gender age and education level ofpet owners as well as their family size and possible presence
of young members do not seem to affect animal occurrenceof intestinal parasite infections (Table 6)
4 Discussion
The intestinal parasites in this survey are consistent with thetypical parasite spectrum of domestic carnivores worldwide
BioMed Research International 5
Table 2 Univariate analysis of risk factors for intestinal parasites in dogs and cats presenting at two veterinary practices in northern Italy
Variable Risk factor OR 95 CI 119875 valueDogs
HabitationMetropolitan 100 0006
Micropolitan area 1 3476 1632ndash7403 0001Micropolitan area 2 1947 0986ndash3845 0055
Age le12 months 100 NAgt12 months 0362 0205ndash0639 0000
Gender Male 100 NAFemales 0756 0433ndash1320 0325
SizeSmall 1 0917
Medium 0937 0451ndash1946 0861Large 1165 0439ndash3092 0760
Housing Household 1 NAOutdoor 0827 0364ndash1880 0651
Husbandry Single-dog-household 1 NAMultiple-dog-household 2059 1047ndash4051 0036
Cats
HabitationMetropolitan 100 0008
Micropolitan area 1 2100 0730ndash6039 0169Micropolitan area 2 3561 1601ndash7924 0002
Age le12 months 100 NAgt12 months 0347 0168ndash0716 0004
Gender Males 100 NAFemale 0809 0401ndash1631 0553
Housing Outdoorhousehold 1 NAHousehold 0526 0195ndash1424 0006
Husbandry Single-cat-household 1 NAMultiple-cat-household 1153 0437ndash3039 0774
OR odds ratio(CI) 95 confidence interval
Table 3 Final multivariate analysis of risks factors associated with intestinal parasites in dogs and cats presenting at two veterinary practicesin northern Italy
Variable Risk factor OR 95 CI 119875 valueDogs
Age gt12 months 100 NAle12 months 0445 0222ndash0894 0023
Husbandry Single-dog-household 1 NAMultiple-dog-household 2240 1115ndash4498 0023
Cats
HabitationMetropolitan area 100 0011Micropolitan area 1 2279 0762ndash6814 0141Micropolitan area 2 3510 1536ndash8020 0003
Age gt12 months 100 NAle12 months 0348 0163ndash0742 0006
OR odds ratio(CI) 95 confidence interval
6 BioMed Research InternationalTa
ble4Prevalence
()a
nd95CI
(minndashm
ax)o
fintestin
alparasites
indo
gsandcatsby
individu
alfeatures
andmanagem
ent
Parasites
Gender
Age
Hou
sing
Husband
ryMale
Female
le12
mon
ths
gt12
mon
ths
Hou
seho
ldOutdo
orSing
leMultip
leDogs
(119899=116)
(119899=92)
(119899=92)
(119899=116)
(119899=56)
(119899=84)
(119899=74)
(119899=66)
Toxocara
canis
1379
761
2065lowastlowast
345lowastlowast
1071
1667
1081
1818
(752ndash2007)
(219
ndash1303)
(1238ndash2892)
(013
ndash677)
(261ndash1881)
(870ndash
2464)
(374
ndash178
8)(888ndash2748)
Toxascarisleo
nina
086
109
109
086
0238
135
152
(0ndash254)
(0ndash321)
(0ndash321)
(0ndash254)
mdash(0ndash564)
(0ndash398)
(0ndash4
47)
Ancylostomatidae
345
326
326
345
179
595
0lowastlowast
909lowastlowast
(013
ndash677)
(0ndash6
89)
(0ndash6
89)
(013
ndash677)
(0ndash526)
(089ndash
1101)
mdash(215
ndash1603)
Trich
urisvulpis
517
870
326
948
536
952
270lowast
1364lowast
(114
ndash920)
(294ndash
1445)
(0ndash6
89)
(415
ndash1481)
(0ndash112
6)(324ndash
1580)
(0ndash6
39)
(536ndash
2192)
Eucoleu
saerophilus
010
90
086
00
00
mdash(0ndash321)
mdash(0ndash254)
mdashmdash
mdashmdash
Dipylidium
caninu
m17
2217
217
172
536
119
270
303
(0ndash4
09)
(0ndash515
)(0ndash515
)(0ndash4
09)
(0ndash112
6)(0ndash351)
(0ndash6
39)
(0ndash717
)
Cysto
isosporasp
345
543
870lowastlowast
086lowastlowast
1071lowast
238lowast
541
606
(013
ndash677)
(080ndash
1007)
(294ndash
1445)
(0ndash254)
(261ndash1881)
(0ndash564)
(026ndash
1056)
(030ndash
1182)
Giardiadu
odenalis
2155
1848
2717lowast
1466lowast
2679
2143
2297
2424
(1407ndash2903)
(1055ndash2641)
(1808ndash3626)
(822ndash2109)
(1519ndash3839)
(1265ndash3021)
(1339ndash3255)
(1390ndash3458)
Overallprevalence
4483
3804
5543lowastlowast
2931lowastlowast
5044
83
4054lowast
5758lowast
(3578ndash5388)
(2812ndash4
796)
(4528ndash6
559)
(210
3ndash3759)
(3690ndash6
315)
(2558ndash6
408)
(293
5ndash5173)
(4566ndash6
950)
Cats
(119899=62)
(119899=65)
(119899=61)
(119899=66)
(119899=38)
(119899=29)
(119899=31)
(119899=36)
Toxocara
cati
1290
1231
1967lowast
606lowast
2368
2069
1935
2500
(456ndash
2125)
(432
ndash2029)
(970ndash
2965)
(030ndash
1182)
(1016ndash372
0)(595ndash3543)
(544ndash
3326)
(1085ndash391
5)
Toxascarisleo
nina
323
615
984lowastlowast
0lowastlowast
263lowast
1724lowast
968
833
(0ndash762)
(031ndash1200)
(236ndash
1731)
mdash(0ndash772)
(349ndash
3099)
(0ndash2009)
(0ndash173
6)
Ancylostomatidae
161
016
40
263
00
278
(0ndash4
75)
mdash(0ndash4
83)
mdash(0ndash772)
mdashmdash
(0ndash815
)
Trich
urisvulpis
161
00
152
0345
0278
(0ndash4
75)
mdashmdash
(0ndash4
46)
mdash(0ndash1009)
mdash(0ndash815
)
Dipylidium
caninu
m323
154
0455
789
0323
556
(0ndash762)
(0ndash4
53)
(0ndash957)
(0ndash1646
)mdash
(0ndash945)
(0ndash1305)
Spiro
metra
sp
161
016
40
00
00
(0ndash4
75)
mdash(0ndash4
83)
mdashmdash
mdashmdash
mdash
Cysto
isosporasp
161
462
492
152
263
690
0833
(0ndash4
75)
(0ndash972)
(0ndash1034)
(0ndash4
46)
(0ndash772)
(0ndash1612)
mdash(0ndash173
6)
Toxoplasma-lik
e0
154
015
20
00
0mdash
(0ndash4
53)
mdash(0ndash4
46)
mdashmdash
mdashmdash
Giardiadu
odenalis
2903
2615
3279
2273
2368
3448
3548
2222
(177
3ndash40
33)
(1547ndash3684)
(210
1ndash44
57)
(1262ndash3284)
(1016ndash372
0)(1718ndash5178)
(1864
ndash5232)
(864ndash
3580)
Overallprevalence
4677
4154
5738lowastlowast
3182lowastlowast
506552
5484
5833
(3435ndash591
9)(295
6ndash5352
)(4497ndash6
979)
(2058ndash4
306)
(3410ndash6
590)
(4822ndash8282)
(3732ndash7236)
(4222ndash7444
)(C
I)95con
fidence
intervalof
thep
revalence
lowastlowast
Chi-S
quaretest119875valuelt
001
lowast
Chi-S
quaretest119875valuelt
005
BioMed Research International 7
Table 5 Frequency of pets (dogs or cats) infected or not infectedby intestinal parasites in northern Italy according to gastrointestinalsymptoms (presence or absence)
Infection No infection 119875 valuelowast
DogsSymptomatic 21 23 085Asymptomatic 48 48
CatSymptomatic 10 13 0128Asymptomatic 28 16
lowastFisherrsquos exact 119875 value
Table 6 Frequency of pets (dogs or cats) infected by intestinalparasites in northwestern Italy by features of their owners (number207)
Owner features Frequency of pets119875 valuelowast
Positive 119899 () Negative 119899 ()Gender
Female 75 (3694) 66 (3251) 024Male 29 (1428) 33 (1625)
Agele40 years old 65 (3202) 66 (3251) 031gt40 years old 39 (1921) 33 (1625)
Educationalqualification
Secondary schoolcertificate 38 (1871) 33 (1625) 037Intermediate schoolcertificateacademicdegree
66 (3251) 66 (3251)
Family componentsle2 42 (2058) 47 (2303) 020gt2 62 (3039) 53 (2598)
Presence of young lt15years old
Not 66 (3235) 68 (3333) 029Yes 38 (1862) 32 (1568)
lowastFisherrsquos exact 119875 value
Among the recovered helminthic species T canis and Tcati which accountedthe most frequent are consideredof great public health significance in their causing themost widespread and economically important zoonoses [30]Other parasites diffusing zoonoses ofminor importance werefound such as T vulpis Ancylostomatidae and Dypilid-ium canimum Finally molecular analysis on fecal samplesdemonstrated the presence of G duodenalis AssemblageA considered to have zoonotic potential [31] The overallprevalence of intestinal parasites both in dogs and in catsin northern Italy was higher than expected (119875 = 2816ndash5741 in dogs 119875 = 3258ndash6042 in cats) The currentlyreported prevalence rates of dog parasites are slightly differentconsidering the different origin of sampled dogs Particularlydogs from the large metropolitan area of Milan showed
lower prevalence than dogs from themicropolitan territoriesSeveral factors can justify these differences In fact most dogsfromMilan were rarely taken to large playgrounds limited intheir walks and regularly treated against heartworm diseaseFurther no colonies of stray dogs exist and proper disposalof dog waste from public soil is coming into common useamong urban pet owners On the other hand dogs frommicropolitan areas are usually at high risk of infection beingfrequently outdoors in their gardens or in large green areasIn addition transhumance being still practiced in Lombardythey might reasonably be infected by sheepdogs guardingtranshumant sheep flocks In fact they are moved fromAlpine pastures to lowlands twice yearly along the mainroutes (north to south) throughBergamo andBrescia towardsthe Po Plain areas whose fields may be contaminated by fecesof untreated sheepdog thus passing infection
In dogs as regards helminths only currently reportedprevalences significantly differ from what was previouslyobserved in Lombardy In 1974 in a coprological surveyconducted in some micropolitan areas located north andsouth of Milan helminths were recorded in 7579ndash853 ofexamined dogs [25] Further development in diagnosis andtreatment may account for the substantial differences foundwith our present survey together with a more widespreadprophylaxis against D immitis in the area of Milan whichmight have reasonably contributed to control canine intesti-nal parasites In 2007 helminth eggs were recovered in 7of dog feces collected from public places including parksof Milan [32] indicating a lower prevalence than in ourlatest survey (119875 = 141) This could be due to thekind of fecal samples collected from city soil that mainlyincluded droppings voided by old dogs typically showinglower infection values than young ones On the other handour findings are consistent with results from a recent surveyon pets from central Italy sampled in veterinary clinics wherehelminth infections were present in 241 of owned dogsand in 319 of owned cats [33] In the same year helminthinfections were recorded in 501 of stray cats from coloniespertaining to the metropolitan area of Milan [26]
Consistent with data obtained in several countriesascarids especially Toxocara spp were the most prevalentcanine and feline parasites [7 10 12ndash14 33 34] In contrastwith other surveys a low prevalence of Ancylostomatidaeinfection was recorded in our sampled dogs except thosefrom the micropolitan areas 1 and 2 A low presence ofhunting sporting or guard dogs in our samples as well asepidemiology and life cycle of Ancylostomatidae nematodescan account for this discrepancy [2 3 8 11 35]
As regardsG duodenalis it was themost prevalent canineand feline parasite according to other surveys [5 8ndash10 12]Such findings are not consistent with low prevalence valuesrecorded in the same species in other Italian studies whoseanalytical methods were different [32 36ndash39]
In this survey consistent with previous studies [31 40 41]G duodenalis assemblages C and D were isolated in dogsThey are considered host-adapted genotypes and a speciesname Giardia canis was proposed to label them As regardscats in our study the host-adapted F genotype was notfound however G duodenalis infections sustained also by
8 BioMed Research International
assemblages A B C and D have been previously describedin cats [40 42] In owned cats we observed a high prevalenceof G duodenalis infection by assemblage A whose possiblezoonotic potential must not be underestimated [31] FinallyG duodenalis assemblage D was recovered less frequentlythough [42 43]
Risk factors for dogs frommetropolitan andmicropolitanareas were being younger than 12 months or sharing thesame house with other dogs Compared to dogs from thelarge metropolitan area of Milan the odds for dogs from themicropolitan area 1 were 3476 times higher and the oddsfor dogs from MC 2 were 1947 times higher but with lowersignificance (119875 = 0001 versus 119875 = 0055) Further comparedto dogs le12 months old the odds of a dog gt12 months beingparasitized were 0362 times smaller Compared to single-household dogs the odds for multiple- household dogs were2059 times higher which means that cohabitation is oneof the most important risk factors associated to endopara-sitism In accordance with Katagiri andOliveira-Sequeira [2]who also found higher prevalence in multihousehold dogssignificant differences were found for Ancylostomatidae andT vulpis infections It might be that in the presence ofmultiple pets environmental contamination with infectivestages of these taxa occurs dogs become more susceptible toinfections and environmental contamination itself is higherand better maintained In cats the presence of endoparasiteswas associated only with their age housing and with the areathey lived in These findings are consistent with other studiesconsidering parasitism as of primarily concern for youngerdogs or cats [4 5 7 14] According to the univariate analysisthe overall prevalence of intestinal parasites in household catsshows statistically significant differences with cats that livedoutsidewith access to a garden (119875 = 50 in household versus119875 = 6552 in outdoor) Living outdoors or having accessto a garden seems to be a risk factor for T leonina infectionin cats as similarly described by Nareaho et al [15] It couldbe partially due to the source of infection for this parasitethat in addition to larvated eggs is represented by paratenichosts that harbour somatic third-stage larvae [44] As aconsequence of their predatory behavior domestic felinescould bemore susceptible to infections due to paratenic hostswhen they have outdoor access
Dogs and cats presenting gastrointestinal signs showed aprevalence of intestinal parasites close to 45 which urgesto differential diagnosis and periodic coprological exami-nation Prophylaxis against D immitis showed ineffectivein protecting dogs against gastrointestinal nematodes Forthem registered dosage of macrocyclic lactones used againstheartworms must be too low and seasonal administration ofthe treatment to all sampled adults dogs proved insufficientto cover their exposition to other risk factors all over theyear The answers to our questionnaire specifically designedto understand ownerrsquos awareness and information aboutcanine and feline gastrointestinal parasites showed thatthey knew but few aspects of the parasite biology In factmore than 7189 of them indicated that fecal contamina-tion can cause gastrointestinal parasite infection and thusthey were probably aware of the importance of reducingenvironmental fecal voiding Nonetheless 3910 of them
gave a negative answer or no answer at all As to possiblelasting environmental contamination due to infected petfecalization 5622 of total owners were not aware of it andmost of them probably did not consider preventing contactwith intermediateparatenic hosts as a possible prophylaxisagainst intestinal parasites infections A higher number ofowners (4811) correctly answered affirmatively when askedabout the possibility of transmission of intestinal parasitesto puppieskittens by infective milk of bitchesqueens Theymay be more stressed by clinicians on the importance ofintestinal parasite infections in puppies and kittens than inadult dogs and cats Concerning their awareness of risks forhuman health from canine and feline intestinal parasites5081 declared that intestinal parasites of dogs and cats donot represent any kind of risk for human health or that theydid not know about the issue Further 2637 out of 90owners informed about human health risks stated that theycould not name possible diseases thus confirming that theydid not know what proper behavior is necessary to reducezoonotic risks
Overall these results indicated that owners needed moreand clear information about zoonotic potential of intestinalparasites and that the veterinarians can be of extremeimportance in this process
5 Conclusion
Results of this survey showed that intestinal parasites are stilla common finding in owned dogs and cats not to be underes-timated in both metropolitan and micropolitan areas even ifthe latter indicated higher pet infection prevalence Furtherwhen a dog or a cat is presented to clinical examination onaccount of gastrointestinal signs intestinal parasite infectionshould be considered as a possible differential diagnosisThis condition can be asymptomatic and can even affectanimals under proper prophylaxis against D immitis thuseven apparently fit and healthy pets should be submitted toannual or biannual fecal examination Clinicians should alsoconsider that younger patients that live in micropolitan areasare the most susceptible to parasite infections The zoonoticparasites T canis and T cati T vulpis Ancylostomatidae andG duodenalis assemblage A resulted to be the most commonspecies in owned pets In any case veterinaries clearly play akey role in increasing awareness and knowledge of pet ownersabout canine and feline gastrointestinal parasites as to theirinfection routes proper monitoring and correct behavior toavoid potential zoonotic risks
Conflict of Interests
The authors declare that there is no conflict of interestsregarding the publication of this paper
References
[1] A C Y Lee PM Schantz K R Kazacos S PMontgomery andD D Bowman ldquoEpidemiologic and zoonotic aspects of ascaridinfections in dogs and catsrdquo Trends in Parasitology vol 26 no4 pp 155ndash161 2010
BioMed Research International 9
[2] S Katagiri and T C G Oliveira-Sequeira ldquoPrevalence of dogintestinal parasites and risk perception of zoonotic infectionby dog owners in Sao Paulo State Brazilrdquo Zoonoses and PublicHealth vol 55 no 8ndash10 pp 406ndash413 2008
[3] S E Little E M Johnson D Lewis et al ldquoPrevalence ofintestinal parasites in pet dogs in the United Statesrdquo VeterinaryParasitology vol 166 no 1-2 pp 144ndash152 2009
[4] D Barutzki andR Schaper ldquoResults of parasitological examina-tions of faecal samples from cats and dogs in Germany between2003 and 2010rdquo Parasitology Research vol 109 no 1 pp S45ndashS60 2011
[5] N Itoh H Ikegami M Takagi et al ldquoPrevalence of intestinalparasites in private-household cats in Japanrdquo Journal of FelineMedical Surgery vol 14 no 6 pp 436ndash439 2012
[6] M C Gates and T J Nolan ldquoEfficacy of heartworm pre-ventatives against ascarids and hookworms in client-owneddogs a retrospective case control studyrdquo Journal of VeterinaryPharmacology andTherapeutics vol 34 no 2 pp 116ndash119 2011
[7] M C Gates and T J Nolan ldquoEndoparasite prevalence andrecurrence across different age groups of dogs and catsrdquoVeterinary Parasitology vol 166 no 1-2 pp 153ndash158 2009
[8] F S Ferreira P Pereira-Baltasar R Parreira et al ldquoIntestinalparasites in dogs and cats from the district of Evora PortugalrdquoVeterinary Parasitology vol 179 no 1ndash3 pp 242ndash245 2011
[9] C Epe G Rehkter T Schnieder L Lorentzen and L Kreien-brock ldquoGiardia in symptomatic dogs and cats in Europe-Resultsof a European studyrdquo Veterinary Parasitology vol 173 no 1-2pp 32ndash38 2010
[10] D Joffe D van Niekerk F Gagne J Gilleard S Kutz and RLobingier ldquoThe prevalence of intestinal parasites in dogs andcats in Calgary ABrdquo Canadian Veterinary Journal vol 52 no12 pp 1323ndash1328 2011
[11] T M Savilla J E Joy J D May and C C SomervilleldquoPrevalence of dog intestinal nematode parasites in southcentral West Virginia USArdquo Veterinary Parasitology vol 178no 1-2 pp 115ndash120 2011
[12] E Claerebout S Casaert A-C Dalemans et al ldquoGiardiaand other intestinal parasites in different dog populations inNorthern BelgiumrdquoVeterinary Parasitology vol 161 no 1-2 pp41ndash46 2009
[13] P A M Overgaauw L van Zutphen D Hoek et al ldquoZoonoticparasites in fecal samples and fur from dogs and cats in TheNetherlandsrdquo Veterinary Parasitology vol 163 no 1-2 pp 115ndash122 2009
[14] M C Gates and T J Nolan ldquoRisk factors for endoparasitismin dogs retrospective case-control study of 6578 veterinaryteaching hospital casesrdquo Journal of Small Animal Practice vol50 no 12 pp 636ndash640 2009
[15] A Nareaho J Puomio K Saarinen P Jokelainen T Juseliusand A Sukura ldquoFeline intestinal parasites in Finland preva-lence risk factors and anthelmintic treatment practicesrdquo Journalof Feline Medicine and Surgery vol 14 no 6 pp 378ndash383 2012
[16] L Polley and R C A Thompson ldquoParasite zoonoses and cli-mate change molecular tools for tracking shifting boundariesrdquoTrends in Parasitology vol 25 no 6 pp 285ndash291 2009
[17] E J Jenkins J M Schurer and K M Gesy ldquoOld problems on anew playing field helminth zoonoses transmitted among dogswildlife and people in a changing northern climaterdquoVeterinaryParasitology vol 182 no 1 pp 54ndash69 2011
[18] P N Acha and B Szyfres Zoonoses et Maladies TransmissiblesCommunes a lrsquohomme et Aux animaux Office International desEpizooties Paris France 1989
[19] M Fisher ldquoToxocara cati an underestimated zoonotic agentrdquoTrends in Parasitology vol 19 no 4 pp 167ndash170 2003
[20] Y Masuda T Kishimoto H Ito and M Tsuji ldquoVisceral larvamigrans caused by Trichuris vulpis presenting as a pulmonarymassrdquoThorax vol 42 no 12 pp 990ndash991 1987
[21] J J Dunn S T Columbus W E Aldeen M Davis and K CCarroll ldquoTrichuris vulpis recovered from a patient with chronicdiarrhea and five dogsrdquo Journal of Clinical Microbiology vol 40no 7 pp 2703ndash2704 2002
[22] M Papazahariadou A Founta E Papadopoulos SChliounakis K Antoniadou-Sotiriadou and Y TheodoridesldquoGastrointestinal parasites of shepherd and hunting dogs in theSerres Prefecture Northern Greecerdquo Veterinary Parasitologyvol 148 no 2 pp 170ndash173 2007
[23] C Martınez-Carrasco E Berriatua M Garijo J Martınez FD Alonso and R Ruiz De Ybanez ldquoEpidemiological study ofnon-systemic parasitism in dogs in southeast MediterraneanSpain assessed by coprological and post-mortem examinationrdquoZoonoses and Public Health vol 54 no 5 pp 195ndash203 2007
[24] S Leonhard K Pfister P Beelitz C Wielinga and R C AThompson ldquoThe molecular characterisation of Giardia fromdogs in southern Germanyrdquo Veterinary Parasitology vol 150no 1-2 pp 33ndash38 2007
[25] C Genchi G Gili and R Maraschin ldquoIndagine sullrsquoincidenzadelle elmintiasi intestinali del cane in alcune zone della Lom-bardiardquo La Clinica Veterinaria vol 97 no 6 pp 178ndash186 1974
[26] E Spada D Proverbio A Della Pepa et al ldquoPrevalence offaecal-borne parasites in colony stray cats in northern ItalyrdquoJournal of Feline Medicine and Surgery vol 15 no 8 pp 672ndash677 2013
[27] R M Hopkins B P Meloni D M Groth J D WetherallJ A Reynoldson and R C A Thompson ldquoRibosomal RNAsequencing reveals differences between the genotypes of Giar-dia isolates recovered from humans and dogs living in the samelocalityrdquo Journal of Parasitology vol 83 no 1 pp 44ndash51 1997
[28] C Read J Walters I D Robertson and R C A ThompsonldquoCorrelation between genotype of Giardia duodenalis anddiarrhoeardquo International Journal for Parasitology vol 32 no 2pp 229ndash231 2002
[29] A O Bush K D Lafferty J M Lotz and A W ShostakldquoParasitology meets ecology on its own terms Margolis et alrevisitedrdquo Journal of Parasitology vol 83 no 4 pp 575ndash5831997
[30] C N L Macpherson ldquoThe epidemiology and public healthimportance of toxocariasis a zoonosis of global importancerdquoInternational Journal for Parasitology vol 43 pp 999ndash10082013
[31] U Ryan and S M Caccio ldquoZoonotic potential of GiardiardquoInternational Journal For Parasitology vol 43 pp 943ndash9562013
[32] M Genchi E Ferroglio G Traldi S Passera G MezzanoandCGenchi ldquoFecalizzazione ambientale e rischio parassitarionelle citta di Milano e Torinordquo Professione Veterinaria vol 41pp 15ndash17 2007
[33] F Riggio R Mannella G Ariti and S Perrucci ldquoIntestinaland lung parasites in owned dogs and cats from central ItalyrdquoVeterinary Parasitology vol 193 no 1ndash3 pp 78ndash84 2013
[34] LMugnaini R Papini G Gorini A Passantino VMerildi andF Mancianti ldquoPattern and predictive factors of endoparasitismin cats in central Italyrdquo Revue de Medecine Veterinaire vol 163no 2 pp 85ndash88 2012
10 BioMed Research International
[35] D Traversa ldquoPet roundworms and hookworms a continuingneed for global wormingrdquo Parasite amp Vectors vol 5 no 1 p 912012
[36] F Berrilli D di Cave C de Liberato A Franco PScaramozzino and P Orecchia ldquoGenotype characterisation ofGiardia duodenalis isolates from domestic and farm animals bySSU-rRNA gene sequencingrdquo Veterinary Parasitology vol 122no 3 pp 193ndash199 2004
[37] P Bianciardi R Papini G Giuliani andG Cardini ldquoPrevalenceof Giardia antigen in stool samples from dogs and catsrdquo Revuede Medecine Veterinaire vol 155 no 8-9 pp 417ndash421 2004
[38] G Capelli A Frangipane di Regalbono R Iorio M PietrobelliB Paoletti and A Giangaspero ldquoGiardia species and otherintestinal parasites in dogs in north-east and central ItalyrdquoVeterinary Record vol 159 no 13 pp 422ndash424 2006
[39] L Rinaldi M P Maurelli V Musella et al ldquoGiardia andCryptosporidium in canine faecal samples contaminating anurban areardquo Research in Veterinary Science vol 84 no 3 pp413ndash415 2008
[40] A V Scorza L R Ballweber S Tangtrongsup C Panuska andM R Lappin ldquoComparisons of mammalianGiardia duodenalisassemblages based on the 120573-giardin glutamate dehydrogenaseand triose phosphate isomerase genesrdquo Veterinary Parasitologyvol 189 no 2ndash4 pp 182ndash188 2012
[41] F D Uehlinger S J Greenwood J T McClure G B ConboyR OrsquoHandley and H W Barkema ldquoZoonotic potential ofGiardia duodenalis and Cryptosporidium spp and prevalenceof intestinal parasites in young dogs from different populationson Prince Edward Island Canadardquo Veterinary Parasitology vol196 no 3-4 pp 509ndash514 2013
[42] L R Ballweber L Xiao D D Bowman G Kahn and V ACama ldquoGiardiasis in dogs and cats update on epidemiology andpublic health significancerdquo Trends in Parasitology vol 26 no 4pp 180ndash189 2010
[43] D Jaros W Zygner S Jaros and HWedrychowicz ldquoDetectionof Giardia intestinalis assemblages A B and D in domestic catsfrom Warsaw Polandrdquo Polish Journal of Microbiology vol 60no 3 pp 259ndash263 2011
[44] R C AndersonNematode Parasites of Vertebrates Their Devel-opment and Transmission Cabi Publishing Wallingford UK2nd edition 2000
Submit your manuscripts athttpwwwhindawicom
Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014
Anatomy Research International
PeptidesInternational Journal of
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International Journal of
Volume 2014
Zoology
Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014
Molecular Biology International
GenomicsInternational Journal of
Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014
The Scientific World JournalHindawi Publishing Corporation httpwwwhindawicom Volume 2014
Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014
BioinformaticsAdvances in
Marine BiologyJournal of
Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014
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Signal TransductionJournal of
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BioMed Research International
Evolutionary BiologyInternational Journal of
Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014
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Biochemistry Research International
ArchaeaHindawi Publishing Corporationhttpwwwhindawicom Volume 2014
Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014
Genetics Research International
Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014
Advances in
Virolog y
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International Journal of
Microbiology
2 BioMed Research International
their impact on human health [1 18ndash21] As to Giardiaseveral surveys showed that carnivore pets host-specific (CD F) or zoonotic assemblages (A and B) of G duodenaliswhose prevalence values strongly depend on the diagnostictechniques used for example PCR and antigen detectionseemed more sensitive than copromicroscopic analysis [1022ndash24]
Lombardy is the region of northwestern Italy withthe largest population of companion animals representingabout 15 of their overall presence in Italy (data fromNational CompanionRegistry httpwwwsalutegovitanag-caninapublic newAdapterHTTP) Nevertheless only fewdata are available on the occurrence of intestinal parasitesin companion animals in this area Moreover they are notupdated or just limited to stray cats [25 26] Major aim of thissurvey was to determine the prevalence of intestinal parasitesin three groups of dogs and cats from the metropolitanarea of Milan and two micropolitan areas at the boundariesof two neighboring provinces where pets can have accessor live outdoor more easily than those in Milan Influenceon prevalence of individual pet features (age gender sizeand presenceabsence of clinical signs) and management(householdoutdoor husbandry and heartworm effectivetreatment) were also considered Furthermore owner aware-ness mainly about zoonotic potential of intestinal parasitesaffecting their pets was investigated by a specifically designedquestionnaire
2 Materials and Methods
21 Study Area and Sampling The survey was carried outin the northwestern Italian region of Lombardy (latitude45∘401015840N longitude 9∘301015840E) Climate is mainly continentalexcept above 1500m asl where the typical features of alpineareas are recognized Consequently temperatures show highvariability with a maximumminimum annual mean of350∘C (even less in the Alpine areas) The mean annualrainfall is 600ndash700mm in the southern planes and 2000mmin the Alpine or Prealpine areas
The study included dogs and cats from three majorprovinces of Lombardy Milan (latitude 45∘301015840N longitude9∘301015840E) Bergamo (latitude 45∘501015840N longitude 09∘481015840E)and Brescia (latitude 45∘551015840N longitude 10∘151015840E) A total of202 and 207 fecal samples were collected from owned pets inthe metropolitan area of Milan (MT) and in the micropolitanareas of Bergamo (MC 1) and Brescia (MC 2) respectivelyIn the latter areas cities with 10000 to 50000 residents wereincluded (MC 1 23 MC 2 15) From January 2010 to October2011 a total of 409 fresh fecal samples were collected byowners or veterinarians from household dogs (119899 = 253)and cats (119899 = 156) that underwent clinical examinationin two different veterinary clinics located in the namedareas At clinical examination data about individual features(age sex breed and presenceabsence of clinical signs) andmanagement (indooroutdoor housing cohabitation withother dogs andor cats and effective prophylaxis againstDirofilaria immitis in dogs and in cats older than 12 months)of animals were recorded by clinicians Further data (gender
age education level and number of family components)about 207 owners were obtained
22 Fecal Examination Feces were stored at +4∘C and exam-ined within 48 hours Macroscopic examination was firstlyperformed for the detection of proglottids of cestodes Sub-sequently each fecal sample was divided into two aliquotsIn order to detect parasite eggs and oocysts one aliquot wassubjected to microscopic analysis by centrifugation-flotationtechnique with sucrose and sodium nitrate solution (specificgravity 1360)The parasite eggs were differentiated accordingto their morphologic characteristics Quantitative measure-ment of helminth infection (EPG) was not implementedThe second aliquot was used to detect coproantigens of Gduodenalis by a commercially available immunochromato-graphic test (RIDA QUICK Giardia cassette R-BiopharmAG Germany)
23 PCRAssay A group of selectedGiardia-positive sampleswere processed by a commercial kit (QIAamp DNA StoolMini Kit QIAGEN Valencia CA USA) for DNA extractionA nested PCR protocol was applied to amplify a fragment ofthe small subunit ribosomal RNA (SSUrRNA) Giardia geneFor external PCR the forward primer RH11 (51015840-CATCCG-GTCGATCCTGCC-31015840) and the reverse primer RH4 (51015840-AGTCGAACCCTGATTCTCCGCCCAGG-31015840) designedby Hopkins et al [27] were used the internal primers(GIAR-F forward 31015840-GACGCTCTCCCCAAGGAC-51015840 andGIAR-R reverse 51015840-CTGCGTCACGCTCG-31015840-) designedby Read et al [28] were used Amplification productswere run on 2 ethidium bromide agarose gels and visu-alized under ultraviolet light Bands were excised fromagarose gels and purified using a QIAquick Gel Extrac-tion Kit (QIAGEN Valencia CA USA) Amplificationproducts were sent to an external laboratory for sequenc-ing BLAST analysis of the GeneBank database was per-formed to identify G duodenalis assemblages from obtainedsequences
24 Questionnaire Survey A questionnaire designed to knowowner general information on canine and feline intestinalparasites together with their awareness of risks for animal andhuman health from these parasites was submitted A total of185 questionnaires were answered namely by 125 dog ownersand 60 cat owners
25 Statistical Analysis We defined prevalence after Bush etal [29] Prevalence of each parasite within categories of theconsidered variables was compared using a Chi-Square testand results were retained significant when the null hypothesishad a probability less than 119875 lt 001 or 119875 lt 005 Since preva-lence of single taxon was too low for a risk factor analysisdata on infection with helminths andor Giardia were alsocombined to the purpose Labelling an animal as positive iftested positive for at least one species of parasite preliminaryunivariate logistic regression was performed considering thefollowing independent variables gender age (le12 monthsold gt12 months old) habitation (metropolitan area and
BioMed Research International 3
micropolitan areas 1 and 2) management (outdoor or house-hold) breed size (small medium or large) and cohabitationwith other animals Variables showing a 119875 value lt 020were included in the multivariate regression model Back-ward elimination was used to determine which variablesentered the final model setting at 005 the level of signifi-cance to be included in the model The association betweeninfection and gastrointestinal symptoms was analyzed byChi-Square test Further the owner features (gender ageeducational qualification family components and presenceof young lt15 years old) were compared for ldquoinfectedrdquo or ldquonotinfectedrdquo pets by Chi-Square test All statistical analysis wasperformed using SPSS v190 (IBMCorp ArmonkNYUSA)
3 Results
31 Parasitological Analysis Theoverall prevalence of intesti-nal parasites resulted higher in dogs and cats from microp-olitan areas (dogs 119875 = 5741 and 119875 = 4302 respcats 119875 = 4737 and 119875 = 6042 resp) than those fromthe metropolitan area of Milan (dogs 119875 = 2816 cats119875 = 3258) In general a scarce parasitofauna was detectedin most cases of dogs and cats They were frequently infestedby one parasite species (dogs 119875 = 7794 cats 119875 = 7368)or by two parasite species (dogs 119875 = 2206 cats 2632)In both dogs and cats G duodenalis was the most prevalentspecies detected Itsprevalence values accounted as followsdogs 2037 (MC 1) and 2558 (MC 2) 1605 (MT) cats3684 (MC 1) 2500 (MC 2) and 247 (MT) T canisresulted to be the most common helminth in dogs from MC1 (119875 = 2222) with a lower prevalence in those from MC 2(119875 = 930) and MT (119875 = 448) T cati showed its highestprevalence values in cats fromMC 2 (119875 = 2239) and lowervalues in those from MC 1 (526) and MT (119875 = 562)(Table 1)
Considering the univariate logistic regression analysisin dogs pet age was the strongest predictor of intestinalparasite infection the odds of a dog being infected were044 smaller in animals gt12 months old (Table 2) Dogsfrom the metropolitan area of Milan were significantly lesssusceptible to intestinal parasites than dogs from MC 2 (OR= 1947) or MC 1 (OR = 3476) (Table 2) Besides husbandrymanagement (single or multiple animals in the same house)had impressive effect on the infection multiple dogs showedhigher infection risk than single dogs (OR = 2059) Genderbreed size and housingmanagement (household or outdoor)had no impressive effect on the infection In cats thepredominant predictors of intestinal parasite infection werehabitation age and housing Specifically older cats were lesslikely infected than younger ones (OR = 0347) and cats fromthe metropolitan area of Milan showed less susceptibility toinfections than cats from the micropolitan areas (OR = 2100and OR = 3561) (Table 2) The age and husbandry variablesfor dogs and habitation and age for cats entered in the finalmultivariable model (Table 3)
Subsequently data of each taxon was analyzed dogslt12 months old showed significantly a higher prevalence ofinfection byT canis (119875 = 2065)Cystoisospora (870) and
byGiardia duodenalis (119875 = 2717) than older ones (Table 4)Cystoisospora was more commonly found in household dogsthan in dogs living outdoor Dogs with multiple husbandrieswere frequently infected by Ancylostomatidae and T vulpis(Table 4)
In cats T cati and T leonina infection prevalence resultedsignificantly higher in young animals than in adult ones Tleonina was more commonly found in cats living outdoorthan in household cats (Table 4)
The dogs and cats in this study were presented to twoVeterinary Clinics for routine control or vaccination clinicalfindings were absent in most cases except for 2071 ofdogs and 1343 of cats with gastrointestinal signs suchas diarrhea vomiting nausea or lack of appetite Out ofthem 4483 of dogs and 4444 of cats had intestinalparasites (Table 5) A large percentage of the sampled dogsreceived regular prophylaxis againstD immitis (119875 = 7042)with selamectin in spot-on formulation (5417) ivermectin(3958) per os or moxidectin (625) in injectable formu-lation Thus only a few dogs were infected by helminthsIn particular dogs under selamectin treatment were infectedwithT vulpis (119899 = 4) Ancylostomatidae (119899 = 2) T canis (119899 =1) and Toxascaris leonina (119899 = 1) dogs under ivermectintreatment were infected with T canis (119899 = 2) and T vulpis(119899 = 1) one dog under moxidectin treatment was infectedwith T canis
Only 2 adult cats received proper prophylaxis againstheartwormswith a spot-on formulation containing selamect-in one of them were infected by Dipylidium caninum
32 Genotyping of Giardia Duodenalis Fifty-four Giardia-positive samples (37 dogs and 17 cats) were processed for thenested PCR protocol In dogs prevalence of G duodenalisassemblages obtained from 1137 dogs showed the occur-rence of C and D assemblages precisely with percentagesof 545 (C) and 4545 (D) In cats A and D assemblageswere detected with percentages of 833 (A) and 166(D)
33 Survey on Health Risk Awareness in Pet Owners Aspecifically designed questionnaire on health risk awarenesswas handed out among owners whose pets were underour investigation Results from filled-in forms showed that7189of them correctly identified the common transmissionroute of intestinal parasites that is fecal contamination offood or of other ingested materials While 973 of themthought that direct contact between healthy and infectedanimal triggers infection 1838 totally ignored the wayof transmission of intestinal parasites 6090 of ownersidentifying in fecal contamination the route of infection fordogs and cats retained that parasite eggs could stay infectivefor long About the possibility of transmission of intestinalparasites to puppieskittens by bitchesqueens only 4811 ofowners answered affirmatively while 1567 of them had noanswer When asked about human health risks due to canineand feline intestinal parasites 4919 showed awareness ofthe occurrence 3567 answered that no risk is given and
4 BioMed Research International
Table 1 Prevalence () and confidence interval (CI) of intestinal parasites in 253 owned dogs and 156 owned cats in northern Italy
Parasites Metropolitan area Micropolitan area 1 Micropolitan area 2 (CI) (CI) (CI)
Dogs
Toxocara canis 448 2222 930(209ndash1086) (1077ndash3668) (304ndash1557)
Toxascaris leonina 0 370 0(0-0) (0ndash891) (0-0)
Ancylostomatidae 097 556 349(017ndash529) (0ndash1187) (0ndash745)
Trichuris vulpis 608 1111 581(333ndash1337) (245ndash1977) (077ndash1086)
Strongyloides stercoralis 194 0 0(053ndash68) (0-0) (0-0)
Eucoleus aerophilus 097 0 0(017ndash529) (0-0) (0-0)
Dipylidium caninum 0 286 0(0) (010ndash562) (0-0)
Cystoisospora sp 097 370 698(017ndash529) (0ndash891) (148ndash1247)
Giardia duodenalis 1605 2037 2558(1056ndash2485) (927ndash3147) (1617ndash3499)
Overall prevalence 2816 5741 4302(2038ndash3751) (4378ndash7103) (3235ndash5370)
Cats
Toxocara cati 562 526 2239(242ndash1249) (0ndash1632) (1241ndash3237)
Toxascaris leonina 0 526 896(0-0) (0ndash1632) (212ndash1580)
Ancylostomatidae 112 0 208(002ndash609) (0-0) (0ndash627)
Trichuris vulpis 0 0 208(0-0) (0-0) (0ndash627)
Dipylidium caninum 0 286 448(0-0) (010ndash562) (0ndash943)
Spirometra 112 0 0(002ndash609) (0-0) (0-0)
Cystoisospora sp 112 526 417(002ndash609) (0ndash1632) (0ndash1003)
Toxoplasma-like 112 0 0(002ndash609) (0-0) (0-0)
Giardia duodenalis 2247 3684 2500(1504ndash3218) (1296ndash6073) (1229ndash3771)
Overall prevalence 3258 4737 6042(2374ndash4286) (2264ndash7209) (4607ndash7477)
1514 declared they had even never considered such prob-ability Of the ninety owners aware of zoonoses risk 7252of them thought that the most common source of infectionis contaminated food 23 answered that transmission ofparasites to humans is caused by direct contact with petswhile 440 had no idea Gender age and education level ofpet owners as well as their family size and possible presence
of young members do not seem to affect animal occurrenceof intestinal parasite infections (Table 6)
4 Discussion
The intestinal parasites in this survey are consistent with thetypical parasite spectrum of domestic carnivores worldwide
BioMed Research International 5
Table 2 Univariate analysis of risk factors for intestinal parasites in dogs and cats presenting at two veterinary practices in northern Italy
Variable Risk factor OR 95 CI 119875 valueDogs
HabitationMetropolitan 100 0006
Micropolitan area 1 3476 1632ndash7403 0001Micropolitan area 2 1947 0986ndash3845 0055
Age le12 months 100 NAgt12 months 0362 0205ndash0639 0000
Gender Male 100 NAFemales 0756 0433ndash1320 0325
SizeSmall 1 0917
Medium 0937 0451ndash1946 0861Large 1165 0439ndash3092 0760
Housing Household 1 NAOutdoor 0827 0364ndash1880 0651
Husbandry Single-dog-household 1 NAMultiple-dog-household 2059 1047ndash4051 0036
Cats
HabitationMetropolitan 100 0008
Micropolitan area 1 2100 0730ndash6039 0169Micropolitan area 2 3561 1601ndash7924 0002
Age le12 months 100 NAgt12 months 0347 0168ndash0716 0004
Gender Males 100 NAFemale 0809 0401ndash1631 0553
Housing Outdoorhousehold 1 NAHousehold 0526 0195ndash1424 0006
Husbandry Single-cat-household 1 NAMultiple-cat-household 1153 0437ndash3039 0774
OR odds ratio(CI) 95 confidence interval
Table 3 Final multivariate analysis of risks factors associated with intestinal parasites in dogs and cats presenting at two veterinary practicesin northern Italy
Variable Risk factor OR 95 CI 119875 valueDogs
Age gt12 months 100 NAle12 months 0445 0222ndash0894 0023
Husbandry Single-dog-household 1 NAMultiple-dog-household 2240 1115ndash4498 0023
Cats
HabitationMetropolitan area 100 0011Micropolitan area 1 2279 0762ndash6814 0141Micropolitan area 2 3510 1536ndash8020 0003
Age gt12 months 100 NAle12 months 0348 0163ndash0742 0006
OR odds ratio(CI) 95 confidence interval
6 BioMed Research InternationalTa
ble4Prevalence
()a
nd95CI
(minndashm
ax)o
fintestin
alparasites
indo
gsandcatsby
individu
alfeatures
andmanagem
ent
Parasites
Gender
Age
Hou
sing
Husband
ryMale
Female
le12
mon
ths
gt12
mon
ths
Hou
seho
ldOutdo
orSing
leMultip
leDogs
(119899=116)
(119899=92)
(119899=92)
(119899=116)
(119899=56)
(119899=84)
(119899=74)
(119899=66)
Toxocara
canis
1379
761
2065lowastlowast
345lowastlowast
1071
1667
1081
1818
(752ndash2007)
(219
ndash1303)
(1238ndash2892)
(013
ndash677)
(261ndash1881)
(870ndash
2464)
(374
ndash178
8)(888ndash2748)
Toxascarisleo
nina
086
109
109
086
0238
135
152
(0ndash254)
(0ndash321)
(0ndash321)
(0ndash254)
mdash(0ndash564)
(0ndash398)
(0ndash4
47)
Ancylostomatidae
345
326
326
345
179
595
0lowastlowast
909lowastlowast
(013
ndash677)
(0ndash6
89)
(0ndash6
89)
(013
ndash677)
(0ndash526)
(089ndash
1101)
mdash(215
ndash1603)
Trich
urisvulpis
517
870
326
948
536
952
270lowast
1364lowast
(114
ndash920)
(294ndash
1445)
(0ndash6
89)
(415
ndash1481)
(0ndash112
6)(324ndash
1580)
(0ndash6
39)
(536ndash
2192)
Eucoleu
saerophilus
010
90
086
00
00
mdash(0ndash321)
mdash(0ndash254)
mdashmdash
mdashmdash
Dipylidium
caninu
m17
2217
217
172
536
119
270
303
(0ndash4
09)
(0ndash515
)(0ndash515
)(0ndash4
09)
(0ndash112
6)(0ndash351)
(0ndash6
39)
(0ndash717
)
Cysto
isosporasp
345
543
870lowastlowast
086lowastlowast
1071lowast
238lowast
541
606
(013
ndash677)
(080ndash
1007)
(294ndash
1445)
(0ndash254)
(261ndash1881)
(0ndash564)
(026ndash
1056)
(030ndash
1182)
Giardiadu
odenalis
2155
1848
2717lowast
1466lowast
2679
2143
2297
2424
(1407ndash2903)
(1055ndash2641)
(1808ndash3626)
(822ndash2109)
(1519ndash3839)
(1265ndash3021)
(1339ndash3255)
(1390ndash3458)
Overallprevalence
4483
3804
5543lowastlowast
2931lowastlowast
5044
83
4054lowast
5758lowast
(3578ndash5388)
(2812ndash4
796)
(4528ndash6
559)
(210
3ndash3759)
(3690ndash6
315)
(2558ndash6
408)
(293
5ndash5173)
(4566ndash6
950)
Cats
(119899=62)
(119899=65)
(119899=61)
(119899=66)
(119899=38)
(119899=29)
(119899=31)
(119899=36)
Toxocara
cati
1290
1231
1967lowast
606lowast
2368
2069
1935
2500
(456ndash
2125)
(432
ndash2029)
(970ndash
2965)
(030ndash
1182)
(1016ndash372
0)(595ndash3543)
(544ndash
3326)
(1085ndash391
5)
Toxascarisleo
nina
323
615
984lowastlowast
0lowastlowast
263lowast
1724lowast
968
833
(0ndash762)
(031ndash1200)
(236ndash
1731)
mdash(0ndash772)
(349ndash
3099)
(0ndash2009)
(0ndash173
6)
Ancylostomatidae
161
016
40
263
00
278
(0ndash4
75)
mdash(0ndash4
83)
mdash(0ndash772)
mdashmdash
(0ndash815
)
Trich
urisvulpis
161
00
152
0345
0278
(0ndash4
75)
mdashmdash
(0ndash4
46)
mdash(0ndash1009)
mdash(0ndash815
)
Dipylidium
caninu
m323
154
0455
789
0323
556
(0ndash762)
(0ndash4
53)
(0ndash957)
(0ndash1646
)mdash
(0ndash945)
(0ndash1305)
Spiro
metra
sp
161
016
40
00
00
(0ndash4
75)
mdash(0ndash4
83)
mdashmdash
mdashmdash
mdash
Cysto
isosporasp
161
462
492
152
263
690
0833
(0ndash4
75)
(0ndash972)
(0ndash1034)
(0ndash4
46)
(0ndash772)
(0ndash1612)
mdash(0ndash173
6)
Toxoplasma-lik
e0
154
015
20
00
0mdash
(0ndash4
53)
mdash(0ndash4
46)
mdashmdash
mdashmdash
Giardiadu
odenalis
2903
2615
3279
2273
2368
3448
3548
2222
(177
3ndash40
33)
(1547ndash3684)
(210
1ndash44
57)
(1262ndash3284)
(1016ndash372
0)(1718ndash5178)
(1864
ndash5232)
(864ndash
3580)
Overallprevalence
4677
4154
5738lowastlowast
3182lowastlowast
506552
5484
5833
(3435ndash591
9)(295
6ndash5352
)(4497ndash6
979)
(2058ndash4
306)
(3410ndash6
590)
(4822ndash8282)
(3732ndash7236)
(4222ndash7444
)(C
I)95con
fidence
intervalof
thep
revalence
lowastlowast
Chi-S
quaretest119875valuelt
001
lowast
Chi-S
quaretest119875valuelt
005
BioMed Research International 7
Table 5 Frequency of pets (dogs or cats) infected or not infectedby intestinal parasites in northern Italy according to gastrointestinalsymptoms (presence or absence)
Infection No infection 119875 valuelowast
DogsSymptomatic 21 23 085Asymptomatic 48 48
CatSymptomatic 10 13 0128Asymptomatic 28 16
lowastFisherrsquos exact 119875 value
Table 6 Frequency of pets (dogs or cats) infected by intestinalparasites in northwestern Italy by features of their owners (number207)
Owner features Frequency of pets119875 valuelowast
Positive 119899 () Negative 119899 ()Gender
Female 75 (3694) 66 (3251) 024Male 29 (1428) 33 (1625)
Agele40 years old 65 (3202) 66 (3251) 031gt40 years old 39 (1921) 33 (1625)
Educationalqualification
Secondary schoolcertificate 38 (1871) 33 (1625) 037Intermediate schoolcertificateacademicdegree
66 (3251) 66 (3251)
Family componentsle2 42 (2058) 47 (2303) 020gt2 62 (3039) 53 (2598)
Presence of young lt15years old
Not 66 (3235) 68 (3333) 029Yes 38 (1862) 32 (1568)
lowastFisherrsquos exact 119875 value
Among the recovered helminthic species T canis and Tcati which accountedthe most frequent are consideredof great public health significance in their causing themost widespread and economically important zoonoses [30]Other parasites diffusing zoonoses ofminor importance werefound such as T vulpis Ancylostomatidae and Dypilid-ium canimum Finally molecular analysis on fecal samplesdemonstrated the presence of G duodenalis AssemblageA considered to have zoonotic potential [31] The overallprevalence of intestinal parasites both in dogs and in catsin northern Italy was higher than expected (119875 = 2816ndash5741 in dogs 119875 = 3258ndash6042 in cats) The currentlyreported prevalence rates of dog parasites are slightly differentconsidering the different origin of sampled dogs Particularlydogs from the large metropolitan area of Milan showed
lower prevalence than dogs from themicropolitan territoriesSeveral factors can justify these differences In fact most dogsfromMilan were rarely taken to large playgrounds limited intheir walks and regularly treated against heartworm diseaseFurther no colonies of stray dogs exist and proper disposalof dog waste from public soil is coming into common useamong urban pet owners On the other hand dogs frommicropolitan areas are usually at high risk of infection beingfrequently outdoors in their gardens or in large green areasIn addition transhumance being still practiced in Lombardythey might reasonably be infected by sheepdogs guardingtranshumant sheep flocks In fact they are moved fromAlpine pastures to lowlands twice yearly along the mainroutes (north to south) throughBergamo andBrescia towardsthe Po Plain areas whose fields may be contaminated by fecesof untreated sheepdog thus passing infection
In dogs as regards helminths only currently reportedprevalences significantly differ from what was previouslyobserved in Lombardy In 1974 in a coprological surveyconducted in some micropolitan areas located north andsouth of Milan helminths were recorded in 7579ndash853 ofexamined dogs [25] Further development in diagnosis andtreatment may account for the substantial differences foundwith our present survey together with a more widespreadprophylaxis against D immitis in the area of Milan whichmight have reasonably contributed to control canine intesti-nal parasites In 2007 helminth eggs were recovered in 7of dog feces collected from public places including parksof Milan [32] indicating a lower prevalence than in ourlatest survey (119875 = 141) This could be due to thekind of fecal samples collected from city soil that mainlyincluded droppings voided by old dogs typically showinglower infection values than young ones On the other handour findings are consistent with results from a recent surveyon pets from central Italy sampled in veterinary clinics wherehelminth infections were present in 241 of owned dogsand in 319 of owned cats [33] In the same year helminthinfections were recorded in 501 of stray cats from coloniespertaining to the metropolitan area of Milan [26]
Consistent with data obtained in several countriesascarids especially Toxocara spp were the most prevalentcanine and feline parasites [7 10 12ndash14 33 34] In contrastwith other surveys a low prevalence of Ancylostomatidaeinfection was recorded in our sampled dogs except thosefrom the micropolitan areas 1 and 2 A low presence ofhunting sporting or guard dogs in our samples as well asepidemiology and life cycle of Ancylostomatidae nematodescan account for this discrepancy [2 3 8 11 35]
As regardsG duodenalis it was themost prevalent canineand feline parasite according to other surveys [5 8ndash10 12]Such findings are not consistent with low prevalence valuesrecorded in the same species in other Italian studies whoseanalytical methods were different [32 36ndash39]
In this survey consistent with previous studies [31 40 41]G duodenalis assemblages C and D were isolated in dogsThey are considered host-adapted genotypes and a speciesname Giardia canis was proposed to label them As regardscats in our study the host-adapted F genotype was notfound however G duodenalis infections sustained also by
8 BioMed Research International
assemblages A B C and D have been previously describedin cats [40 42] In owned cats we observed a high prevalenceof G duodenalis infection by assemblage A whose possiblezoonotic potential must not be underestimated [31] FinallyG duodenalis assemblage D was recovered less frequentlythough [42 43]
Risk factors for dogs frommetropolitan andmicropolitanareas were being younger than 12 months or sharing thesame house with other dogs Compared to dogs from thelarge metropolitan area of Milan the odds for dogs from themicropolitan area 1 were 3476 times higher and the oddsfor dogs from MC 2 were 1947 times higher but with lowersignificance (119875 = 0001 versus 119875 = 0055) Further comparedto dogs le12 months old the odds of a dog gt12 months beingparasitized were 0362 times smaller Compared to single-household dogs the odds for multiple- household dogs were2059 times higher which means that cohabitation is oneof the most important risk factors associated to endopara-sitism In accordance with Katagiri andOliveira-Sequeira [2]who also found higher prevalence in multihousehold dogssignificant differences were found for Ancylostomatidae andT vulpis infections It might be that in the presence ofmultiple pets environmental contamination with infectivestages of these taxa occurs dogs become more susceptible toinfections and environmental contamination itself is higherand better maintained In cats the presence of endoparasiteswas associated only with their age housing and with the areathey lived in These findings are consistent with other studiesconsidering parasitism as of primarily concern for youngerdogs or cats [4 5 7 14] According to the univariate analysisthe overall prevalence of intestinal parasites in household catsshows statistically significant differences with cats that livedoutsidewith access to a garden (119875 = 50 in household versus119875 = 6552 in outdoor) Living outdoors or having accessto a garden seems to be a risk factor for T leonina infectionin cats as similarly described by Nareaho et al [15] It couldbe partially due to the source of infection for this parasitethat in addition to larvated eggs is represented by paratenichosts that harbour somatic third-stage larvae [44] As aconsequence of their predatory behavior domestic felinescould bemore susceptible to infections due to paratenic hostswhen they have outdoor access
Dogs and cats presenting gastrointestinal signs showed aprevalence of intestinal parasites close to 45 which urgesto differential diagnosis and periodic coprological exami-nation Prophylaxis against D immitis showed ineffectivein protecting dogs against gastrointestinal nematodes Forthem registered dosage of macrocyclic lactones used againstheartworms must be too low and seasonal administration ofthe treatment to all sampled adults dogs proved insufficientto cover their exposition to other risk factors all over theyear The answers to our questionnaire specifically designedto understand ownerrsquos awareness and information aboutcanine and feline gastrointestinal parasites showed thatthey knew but few aspects of the parasite biology In factmore than 7189 of them indicated that fecal contamina-tion can cause gastrointestinal parasite infection and thusthey were probably aware of the importance of reducingenvironmental fecal voiding Nonetheless 3910 of them
gave a negative answer or no answer at all As to possiblelasting environmental contamination due to infected petfecalization 5622 of total owners were not aware of it andmost of them probably did not consider preventing contactwith intermediateparatenic hosts as a possible prophylaxisagainst intestinal parasites infections A higher number ofowners (4811) correctly answered affirmatively when askedabout the possibility of transmission of intestinal parasitesto puppieskittens by infective milk of bitchesqueens Theymay be more stressed by clinicians on the importance ofintestinal parasite infections in puppies and kittens than inadult dogs and cats Concerning their awareness of risks forhuman health from canine and feline intestinal parasites5081 declared that intestinal parasites of dogs and cats donot represent any kind of risk for human health or that theydid not know about the issue Further 2637 out of 90owners informed about human health risks stated that theycould not name possible diseases thus confirming that theydid not know what proper behavior is necessary to reducezoonotic risks
Overall these results indicated that owners needed moreand clear information about zoonotic potential of intestinalparasites and that the veterinarians can be of extremeimportance in this process
5 Conclusion
Results of this survey showed that intestinal parasites are stilla common finding in owned dogs and cats not to be underes-timated in both metropolitan and micropolitan areas even ifthe latter indicated higher pet infection prevalence Furtherwhen a dog or a cat is presented to clinical examination onaccount of gastrointestinal signs intestinal parasite infectionshould be considered as a possible differential diagnosisThis condition can be asymptomatic and can even affectanimals under proper prophylaxis against D immitis thuseven apparently fit and healthy pets should be submitted toannual or biannual fecal examination Clinicians should alsoconsider that younger patients that live in micropolitan areasare the most susceptible to parasite infections The zoonoticparasites T canis and T cati T vulpis Ancylostomatidae andG duodenalis assemblage A resulted to be the most commonspecies in owned pets In any case veterinaries clearly play akey role in increasing awareness and knowledge of pet ownersabout canine and feline gastrointestinal parasites as to theirinfection routes proper monitoring and correct behavior toavoid potential zoonotic risks
Conflict of Interests
The authors declare that there is no conflict of interestsregarding the publication of this paper
References
[1] A C Y Lee PM Schantz K R Kazacos S PMontgomery andD D Bowman ldquoEpidemiologic and zoonotic aspects of ascaridinfections in dogs and catsrdquo Trends in Parasitology vol 26 no4 pp 155ndash161 2010
BioMed Research International 9
[2] S Katagiri and T C G Oliveira-Sequeira ldquoPrevalence of dogintestinal parasites and risk perception of zoonotic infectionby dog owners in Sao Paulo State Brazilrdquo Zoonoses and PublicHealth vol 55 no 8ndash10 pp 406ndash413 2008
[3] S E Little E M Johnson D Lewis et al ldquoPrevalence ofintestinal parasites in pet dogs in the United Statesrdquo VeterinaryParasitology vol 166 no 1-2 pp 144ndash152 2009
[4] D Barutzki andR Schaper ldquoResults of parasitological examina-tions of faecal samples from cats and dogs in Germany between2003 and 2010rdquo Parasitology Research vol 109 no 1 pp S45ndashS60 2011
[5] N Itoh H Ikegami M Takagi et al ldquoPrevalence of intestinalparasites in private-household cats in Japanrdquo Journal of FelineMedical Surgery vol 14 no 6 pp 436ndash439 2012
[6] M C Gates and T J Nolan ldquoEfficacy of heartworm pre-ventatives against ascarids and hookworms in client-owneddogs a retrospective case control studyrdquo Journal of VeterinaryPharmacology andTherapeutics vol 34 no 2 pp 116ndash119 2011
[7] M C Gates and T J Nolan ldquoEndoparasite prevalence andrecurrence across different age groups of dogs and catsrdquoVeterinary Parasitology vol 166 no 1-2 pp 153ndash158 2009
[8] F S Ferreira P Pereira-Baltasar R Parreira et al ldquoIntestinalparasites in dogs and cats from the district of Evora PortugalrdquoVeterinary Parasitology vol 179 no 1ndash3 pp 242ndash245 2011
[9] C Epe G Rehkter T Schnieder L Lorentzen and L Kreien-brock ldquoGiardia in symptomatic dogs and cats in Europe-Resultsof a European studyrdquo Veterinary Parasitology vol 173 no 1-2pp 32ndash38 2010
[10] D Joffe D van Niekerk F Gagne J Gilleard S Kutz and RLobingier ldquoThe prevalence of intestinal parasites in dogs andcats in Calgary ABrdquo Canadian Veterinary Journal vol 52 no12 pp 1323ndash1328 2011
[11] T M Savilla J E Joy J D May and C C SomervilleldquoPrevalence of dog intestinal nematode parasites in southcentral West Virginia USArdquo Veterinary Parasitology vol 178no 1-2 pp 115ndash120 2011
[12] E Claerebout S Casaert A-C Dalemans et al ldquoGiardiaand other intestinal parasites in different dog populations inNorthern BelgiumrdquoVeterinary Parasitology vol 161 no 1-2 pp41ndash46 2009
[13] P A M Overgaauw L van Zutphen D Hoek et al ldquoZoonoticparasites in fecal samples and fur from dogs and cats in TheNetherlandsrdquo Veterinary Parasitology vol 163 no 1-2 pp 115ndash122 2009
[14] M C Gates and T J Nolan ldquoRisk factors for endoparasitismin dogs retrospective case-control study of 6578 veterinaryteaching hospital casesrdquo Journal of Small Animal Practice vol50 no 12 pp 636ndash640 2009
[15] A Nareaho J Puomio K Saarinen P Jokelainen T Juseliusand A Sukura ldquoFeline intestinal parasites in Finland preva-lence risk factors and anthelmintic treatment practicesrdquo Journalof Feline Medicine and Surgery vol 14 no 6 pp 378ndash383 2012
[16] L Polley and R C A Thompson ldquoParasite zoonoses and cli-mate change molecular tools for tracking shifting boundariesrdquoTrends in Parasitology vol 25 no 6 pp 285ndash291 2009
[17] E J Jenkins J M Schurer and K M Gesy ldquoOld problems on anew playing field helminth zoonoses transmitted among dogswildlife and people in a changing northern climaterdquoVeterinaryParasitology vol 182 no 1 pp 54ndash69 2011
[18] P N Acha and B Szyfres Zoonoses et Maladies TransmissiblesCommunes a lrsquohomme et Aux animaux Office International desEpizooties Paris France 1989
[19] M Fisher ldquoToxocara cati an underestimated zoonotic agentrdquoTrends in Parasitology vol 19 no 4 pp 167ndash170 2003
[20] Y Masuda T Kishimoto H Ito and M Tsuji ldquoVisceral larvamigrans caused by Trichuris vulpis presenting as a pulmonarymassrdquoThorax vol 42 no 12 pp 990ndash991 1987
[21] J J Dunn S T Columbus W E Aldeen M Davis and K CCarroll ldquoTrichuris vulpis recovered from a patient with chronicdiarrhea and five dogsrdquo Journal of Clinical Microbiology vol 40no 7 pp 2703ndash2704 2002
[22] M Papazahariadou A Founta E Papadopoulos SChliounakis K Antoniadou-Sotiriadou and Y TheodoridesldquoGastrointestinal parasites of shepherd and hunting dogs in theSerres Prefecture Northern Greecerdquo Veterinary Parasitologyvol 148 no 2 pp 170ndash173 2007
[23] C Martınez-Carrasco E Berriatua M Garijo J Martınez FD Alonso and R Ruiz De Ybanez ldquoEpidemiological study ofnon-systemic parasitism in dogs in southeast MediterraneanSpain assessed by coprological and post-mortem examinationrdquoZoonoses and Public Health vol 54 no 5 pp 195ndash203 2007
[24] S Leonhard K Pfister P Beelitz C Wielinga and R C AThompson ldquoThe molecular characterisation of Giardia fromdogs in southern Germanyrdquo Veterinary Parasitology vol 150no 1-2 pp 33ndash38 2007
[25] C Genchi G Gili and R Maraschin ldquoIndagine sullrsquoincidenzadelle elmintiasi intestinali del cane in alcune zone della Lom-bardiardquo La Clinica Veterinaria vol 97 no 6 pp 178ndash186 1974
[26] E Spada D Proverbio A Della Pepa et al ldquoPrevalence offaecal-borne parasites in colony stray cats in northern ItalyrdquoJournal of Feline Medicine and Surgery vol 15 no 8 pp 672ndash677 2013
[27] R M Hopkins B P Meloni D M Groth J D WetherallJ A Reynoldson and R C A Thompson ldquoRibosomal RNAsequencing reveals differences between the genotypes of Giar-dia isolates recovered from humans and dogs living in the samelocalityrdquo Journal of Parasitology vol 83 no 1 pp 44ndash51 1997
[28] C Read J Walters I D Robertson and R C A ThompsonldquoCorrelation between genotype of Giardia duodenalis anddiarrhoeardquo International Journal for Parasitology vol 32 no 2pp 229ndash231 2002
[29] A O Bush K D Lafferty J M Lotz and A W ShostakldquoParasitology meets ecology on its own terms Margolis et alrevisitedrdquo Journal of Parasitology vol 83 no 4 pp 575ndash5831997
[30] C N L Macpherson ldquoThe epidemiology and public healthimportance of toxocariasis a zoonosis of global importancerdquoInternational Journal for Parasitology vol 43 pp 999ndash10082013
[31] U Ryan and S M Caccio ldquoZoonotic potential of GiardiardquoInternational Journal For Parasitology vol 43 pp 943ndash9562013
[32] M Genchi E Ferroglio G Traldi S Passera G MezzanoandCGenchi ldquoFecalizzazione ambientale e rischio parassitarionelle citta di Milano e Torinordquo Professione Veterinaria vol 41pp 15ndash17 2007
[33] F Riggio R Mannella G Ariti and S Perrucci ldquoIntestinaland lung parasites in owned dogs and cats from central ItalyrdquoVeterinary Parasitology vol 193 no 1ndash3 pp 78ndash84 2013
[34] LMugnaini R Papini G Gorini A Passantino VMerildi andF Mancianti ldquoPattern and predictive factors of endoparasitismin cats in central Italyrdquo Revue de Medecine Veterinaire vol 163no 2 pp 85ndash88 2012
10 BioMed Research International
[35] D Traversa ldquoPet roundworms and hookworms a continuingneed for global wormingrdquo Parasite amp Vectors vol 5 no 1 p 912012
[36] F Berrilli D di Cave C de Liberato A Franco PScaramozzino and P Orecchia ldquoGenotype characterisation ofGiardia duodenalis isolates from domestic and farm animals bySSU-rRNA gene sequencingrdquo Veterinary Parasitology vol 122no 3 pp 193ndash199 2004
[37] P Bianciardi R Papini G Giuliani andG Cardini ldquoPrevalenceof Giardia antigen in stool samples from dogs and catsrdquo Revuede Medecine Veterinaire vol 155 no 8-9 pp 417ndash421 2004
[38] G Capelli A Frangipane di Regalbono R Iorio M PietrobelliB Paoletti and A Giangaspero ldquoGiardia species and otherintestinal parasites in dogs in north-east and central ItalyrdquoVeterinary Record vol 159 no 13 pp 422ndash424 2006
[39] L Rinaldi M P Maurelli V Musella et al ldquoGiardia andCryptosporidium in canine faecal samples contaminating anurban areardquo Research in Veterinary Science vol 84 no 3 pp413ndash415 2008
[40] A V Scorza L R Ballweber S Tangtrongsup C Panuska andM R Lappin ldquoComparisons of mammalianGiardia duodenalisassemblages based on the 120573-giardin glutamate dehydrogenaseand triose phosphate isomerase genesrdquo Veterinary Parasitologyvol 189 no 2ndash4 pp 182ndash188 2012
[41] F D Uehlinger S J Greenwood J T McClure G B ConboyR OrsquoHandley and H W Barkema ldquoZoonotic potential ofGiardia duodenalis and Cryptosporidium spp and prevalenceof intestinal parasites in young dogs from different populationson Prince Edward Island Canadardquo Veterinary Parasitology vol196 no 3-4 pp 509ndash514 2013
[42] L R Ballweber L Xiao D D Bowman G Kahn and V ACama ldquoGiardiasis in dogs and cats update on epidemiology andpublic health significancerdquo Trends in Parasitology vol 26 no 4pp 180ndash189 2010
[43] D Jaros W Zygner S Jaros and HWedrychowicz ldquoDetectionof Giardia intestinalis assemblages A B and D in domestic catsfrom Warsaw Polandrdquo Polish Journal of Microbiology vol 60no 3 pp 259ndash263 2011
[44] R C AndersonNematode Parasites of Vertebrates Their Devel-opment and Transmission Cabi Publishing Wallingford UK2nd edition 2000
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BioMed Research International 3
micropolitan areas 1 and 2) management (outdoor or house-hold) breed size (small medium or large) and cohabitationwith other animals Variables showing a 119875 value lt 020were included in the multivariate regression model Back-ward elimination was used to determine which variablesentered the final model setting at 005 the level of signifi-cance to be included in the model The association betweeninfection and gastrointestinal symptoms was analyzed byChi-Square test Further the owner features (gender ageeducational qualification family components and presenceof young lt15 years old) were compared for ldquoinfectedrdquo or ldquonotinfectedrdquo pets by Chi-Square test All statistical analysis wasperformed using SPSS v190 (IBMCorp ArmonkNYUSA)
3 Results
31 Parasitological Analysis Theoverall prevalence of intesti-nal parasites resulted higher in dogs and cats from microp-olitan areas (dogs 119875 = 5741 and 119875 = 4302 respcats 119875 = 4737 and 119875 = 6042 resp) than those fromthe metropolitan area of Milan (dogs 119875 = 2816 cats119875 = 3258) In general a scarce parasitofauna was detectedin most cases of dogs and cats They were frequently infestedby one parasite species (dogs 119875 = 7794 cats 119875 = 7368)or by two parasite species (dogs 119875 = 2206 cats 2632)In both dogs and cats G duodenalis was the most prevalentspecies detected Itsprevalence values accounted as followsdogs 2037 (MC 1) and 2558 (MC 2) 1605 (MT) cats3684 (MC 1) 2500 (MC 2) and 247 (MT) T canisresulted to be the most common helminth in dogs from MC1 (119875 = 2222) with a lower prevalence in those from MC 2(119875 = 930) and MT (119875 = 448) T cati showed its highestprevalence values in cats fromMC 2 (119875 = 2239) and lowervalues in those from MC 1 (526) and MT (119875 = 562)(Table 1)
Considering the univariate logistic regression analysisin dogs pet age was the strongest predictor of intestinalparasite infection the odds of a dog being infected were044 smaller in animals gt12 months old (Table 2) Dogsfrom the metropolitan area of Milan were significantly lesssusceptible to intestinal parasites than dogs from MC 2 (OR= 1947) or MC 1 (OR = 3476) (Table 2) Besides husbandrymanagement (single or multiple animals in the same house)had impressive effect on the infection multiple dogs showedhigher infection risk than single dogs (OR = 2059) Genderbreed size and housingmanagement (household or outdoor)had no impressive effect on the infection In cats thepredominant predictors of intestinal parasite infection werehabitation age and housing Specifically older cats were lesslikely infected than younger ones (OR = 0347) and cats fromthe metropolitan area of Milan showed less susceptibility toinfections than cats from the micropolitan areas (OR = 2100and OR = 3561) (Table 2) The age and husbandry variablesfor dogs and habitation and age for cats entered in the finalmultivariable model (Table 3)
Subsequently data of each taxon was analyzed dogslt12 months old showed significantly a higher prevalence ofinfection byT canis (119875 = 2065)Cystoisospora (870) and
byGiardia duodenalis (119875 = 2717) than older ones (Table 4)Cystoisospora was more commonly found in household dogsthan in dogs living outdoor Dogs with multiple husbandrieswere frequently infected by Ancylostomatidae and T vulpis(Table 4)
In cats T cati and T leonina infection prevalence resultedsignificantly higher in young animals than in adult ones Tleonina was more commonly found in cats living outdoorthan in household cats (Table 4)
The dogs and cats in this study were presented to twoVeterinary Clinics for routine control or vaccination clinicalfindings were absent in most cases except for 2071 ofdogs and 1343 of cats with gastrointestinal signs suchas diarrhea vomiting nausea or lack of appetite Out ofthem 4483 of dogs and 4444 of cats had intestinalparasites (Table 5) A large percentage of the sampled dogsreceived regular prophylaxis againstD immitis (119875 = 7042)with selamectin in spot-on formulation (5417) ivermectin(3958) per os or moxidectin (625) in injectable formu-lation Thus only a few dogs were infected by helminthsIn particular dogs under selamectin treatment were infectedwithT vulpis (119899 = 4) Ancylostomatidae (119899 = 2) T canis (119899 =1) and Toxascaris leonina (119899 = 1) dogs under ivermectintreatment were infected with T canis (119899 = 2) and T vulpis(119899 = 1) one dog under moxidectin treatment was infectedwith T canis
Only 2 adult cats received proper prophylaxis againstheartwormswith a spot-on formulation containing selamect-in one of them were infected by Dipylidium caninum
32 Genotyping of Giardia Duodenalis Fifty-four Giardia-positive samples (37 dogs and 17 cats) were processed for thenested PCR protocol In dogs prevalence of G duodenalisassemblages obtained from 1137 dogs showed the occur-rence of C and D assemblages precisely with percentagesof 545 (C) and 4545 (D) In cats A and D assemblageswere detected with percentages of 833 (A) and 166(D)
33 Survey on Health Risk Awareness in Pet Owners Aspecifically designed questionnaire on health risk awarenesswas handed out among owners whose pets were underour investigation Results from filled-in forms showed that7189of them correctly identified the common transmissionroute of intestinal parasites that is fecal contamination offood or of other ingested materials While 973 of themthought that direct contact between healthy and infectedanimal triggers infection 1838 totally ignored the wayof transmission of intestinal parasites 6090 of ownersidentifying in fecal contamination the route of infection fordogs and cats retained that parasite eggs could stay infectivefor long About the possibility of transmission of intestinalparasites to puppieskittens by bitchesqueens only 4811 ofowners answered affirmatively while 1567 of them had noanswer When asked about human health risks due to canineand feline intestinal parasites 4919 showed awareness ofthe occurrence 3567 answered that no risk is given and
4 BioMed Research International
Table 1 Prevalence () and confidence interval (CI) of intestinal parasites in 253 owned dogs and 156 owned cats in northern Italy
Parasites Metropolitan area Micropolitan area 1 Micropolitan area 2 (CI) (CI) (CI)
Dogs
Toxocara canis 448 2222 930(209ndash1086) (1077ndash3668) (304ndash1557)
Toxascaris leonina 0 370 0(0-0) (0ndash891) (0-0)
Ancylostomatidae 097 556 349(017ndash529) (0ndash1187) (0ndash745)
Trichuris vulpis 608 1111 581(333ndash1337) (245ndash1977) (077ndash1086)
Strongyloides stercoralis 194 0 0(053ndash68) (0-0) (0-0)
Eucoleus aerophilus 097 0 0(017ndash529) (0-0) (0-0)
Dipylidium caninum 0 286 0(0) (010ndash562) (0-0)
Cystoisospora sp 097 370 698(017ndash529) (0ndash891) (148ndash1247)
Giardia duodenalis 1605 2037 2558(1056ndash2485) (927ndash3147) (1617ndash3499)
Overall prevalence 2816 5741 4302(2038ndash3751) (4378ndash7103) (3235ndash5370)
Cats
Toxocara cati 562 526 2239(242ndash1249) (0ndash1632) (1241ndash3237)
Toxascaris leonina 0 526 896(0-0) (0ndash1632) (212ndash1580)
Ancylostomatidae 112 0 208(002ndash609) (0-0) (0ndash627)
Trichuris vulpis 0 0 208(0-0) (0-0) (0ndash627)
Dipylidium caninum 0 286 448(0-0) (010ndash562) (0ndash943)
Spirometra 112 0 0(002ndash609) (0-0) (0-0)
Cystoisospora sp 112 526 417(002ndash609) (0ndash1632) (0ndash1003)
Toxoplasma-like 112 0 0(002ndash609) (0-0) (0-0)
Giardia duodenalis 2247 3684 2500(1504ndash3218) (1296ndash6073) (1229ndash3771)
Overall prevalence 3258 4737 6042(2374ndash4286) (2264ndash7209) (4607ndash7477)
1514 declared they had even never considered such prob-ability Of the ninety owners aware of zoonoses risk 7252of them thought that the most common source of infectionis contaminated food 23 answered that transmission ofparasites to humans is caused by direct contact with petswhile 440 had no idea Gender age and education level ofpet owners as well as their family size and possible presence
of young members do not seem to affect animal occurrenceof intestinal parasite infections (Table 6)
4 Discussion
The intestinal parasites in this survey are consistent with thetypical parasite spectrum of domestic carnivores worldwide
BioMed Research International 5
Table 2 Univariate analysis of risk factors for intestinal parasites in dogs and cats presenting at two veterinary practices in northern Italy
Variable Risk factor OR 95 CI 119875 valueDogs
HabitationMetropolitan 100 0006
Micropolitan area 1 3476 1632ndash7403 0001Micropolitan area 2 1947 0986ndash3845 0055
Age le12 months 100 NAgt12 months 0362 0205ndash0639 0000
Gender Male 100 NAFemales 0756 0433ndash1320 0325
SizeSmall 1 0917
Medium 0937 0451ndash1946 0861Large 1165 0439ndash3092 0760
Housing Household 1 NAOutdoor 0827 0364ndash1880 0651
Husbandry Single-dog-household 1 NAMultiple-dog-household 2059 1047ndash4051 0036
Cats
HabitationMetropolitan 100 0008
Micropolitan area 1 2100 0730ndash6039 0169Micropolitan area 2 3561 1601ndash7924 0002
Age le12 months 100 NAgt12 months 0347 0168ndash0716 0004
Gender Males 100 NAFemale 0809 0401ndash1631 0553
Housing Outdoorhousehold 1 NAHousehold 0526 0195ndash1424 0006
Husbandry Single-cat-household 1 NAMultiple-cat-household 1153 0437ndash3039 0774
OR odds ratio(CI) 95 confidence interval
Table 3 Final multivariate analysis of risks factors associated with intestinal parasites in dogs and cats presenting at two veterinary practicesin northern Italy
Variable Risk factor OR 95 CI 119875 valueDogs
Age gt12 months 100 NAle12 months 0445 0222ndash0894 0023
Husbandry Single-dog-household 1 NAMultiple-dog-household 2240 1115ndash4498 0023
Cats
HabitationMetropolitan area 100 0011Micropolitan area 1 2279 0762ndash6814 0141Micropolitan area 2 3510 1536ndash8020 0003
Age gt12 months 100 NAle12 months 0348 0163ndash0742 0006
OR odds ratio(CI) 95 confidence interval
6 BioMed Research InternationalTa
ble4Prevalence
()a
nd95CI
(minndashm
ax)o
fintestin
alparasites
indo
gsandcatsby
individu
alfeatures
andmanagem
ent
Parasites
Gender
Age
Hou
sing
Husband
ryMale
Female
le12
mon
ths
gt12
mon
ths
Hou
seho
ldOutdo
orSing
leMultip
leDogs
(119899=116)
(119899=92)
(119899=92)
(119899=116)
(119899=56)
(119899=84)
(119899=74)
(119899=66)
Toxocara
canis
1379
761
2065lowastlowast
345lowastlowast
1071
1667
1081
1818
(752ndash2007)
(219
ndash1303)
(1238ndash2892)
(013
ndash677)
(261ndash1881)
(870ndash
2464)
(374
ndash178
8)(888ndash2748)
Toxascarisleo
nina
086
109
109
086
0238
135
152
(0ndash254)
(0ndash321)
(0ndash321)
(0ndash254)
mdash(0ndash564)
(0ndash398)
(0ndash4
47)
Ancylostomatidae
345
326
326
345
179
595
0lowastlowast
909lowastlowast
(013
ndash677)
(0ndash6
89)
(0ndash6
89)
(013
ndash677)
(0ndash526)
(089ndash
1101)
mdash(215
ndash1603)
Trich
urisvulpis
517
870
326
948
536
952
270lowast
1364lowast
(114
ndash920)
(294ndash
1445)
(0ndash6
89)
(415
ndash1481)
(0ndash112
6)(324ndash
1580)
(0ndash6
39)
(536ndash
2192)
Eucoleu
saerophilus
010
90
086
00
00
mdash(0ndash321)
mdash(0ndash254)
mdashmdash
mdashmdash
Dipylidium
caninu
m17
2217
217
172
536
119
270
303
(0ndash4
09)
(0ndash515
)(0ndash515
)(0ndash4
09)
(0ndash112
6)(0ndash351)
(0ndash6
39)
(0ndash717
)
Cysto
isosporasp
345
543
870lowastlowast
086lowastlowast
1071lowast
238lowast
541
606
(013
ndash677)
(080ndash
1007)
(294ndash
1445)
(0ndash254)
(261ndash1881)
(0ndash564)
(026ndash
1056)
(030ndash
1182)
Giardiadu
odenalis
2155
1848
2717lowast
1466lowast
2679
2143
2297
2424
(1407ndash2903)
(1055ndash2641)
(1808ndash3626)
(822ndash2109)
(1519ndash3839)
(1265ndash3021)
(1339ndash3255)
(1390ndash3458)
Overallprevalence
4483
3804
5543lowastlowast
2931lowastlowast
5044
83
4054lowast
5758lowast
(3578ndash5388)
(2812ndash4
796)
(4528ndash6
559)
(210
3ndash3759)
(3690ndash6
315)
(2558ndash6
408)
(293
5ndash5173)
(4566ndash6
950)
Cats
(119899=62)
(119899=65)
(119899=61)
(119899=66)
(119899=38)
(119899=29)
(119899=31)
(119899=36)
Toxocara
cati
1290
1231
1967lowast
606lowast
2368
2069
1935
2500
(456ndash
2125)
(432
ndash2029)
(970ndash
2965)
(030ndash
1182)
(1016ndash372
0)(595ndash3543)
(544ndash
3326)
(1085ndash391
5)
Toxascarisleo
nina
323
615
984lowastlowast
0lowastlowast
263lowast
1724lowast
968
833
(0ndash762)
(031ndash1200)
(236ndash
1731)
mdash(0ndash772)
(349ndash
3099)
(0ndash2009)
(0ndash173
6)
Ancylostomatidae
161
016
40
263
00
278
(0ndash4
75)
mdash(0ndash4
83)
mdash(0ndash772)
mdashmdash
(0ndash815
)
Trich
urisvulpis
161
00
152
0345
0278
(0ndash4
75)
mdashmdash
(0ndash4
46)
mdash(0ndash1009)
mdash(0ndash815
)
Dipylidium
caninu
m323
154
0455
789
0323
556
(0ndash762)
(0ndash4
53)
(0ndash957)
(0ndash1646
)mdash
(0ndash945)
(0ndash1305)
Spiro
metra
sp
161
016
40
00
00
(0ndash4
75)
mdash(0ndash4
83)
mdashmdash
mdashmdash
mdash
Cysto
isosporasp
161
462
492
152
263
690
0833
(0ndash4
75)
(0ndash972)
(0ndash1034)
(0ndash4
46)
(0ndash772)
(0ndash1612)
mdash(0ndash173
6)
Toxoplasma-lik
e0
154
015
20
00
0mdash
(0ndash4
53)
mdash(0ndash4
46)
mdashmdash
mdashmdash
Giardiadu
odenalis
2903
2615
3279
2273
2368
3448
3548
2222
(177
3ndash40
33)
(1547ndash3684)
(210
1ndash44
57)
(1262ndash3284)
(1016ndash372
0)(1718ndash5178)
(1864
ndash5232)
(864ndash
3580)
Overallprevalence
4677
4154
5738lowastlowast
3182lowastlowast
506552
5484
5833
(3435ndash591
9)(295
6ndash5352
)(4497ndash6
979)
(2058ndash4
306)
(3410ndash6
590)
(4822ndash8282)
(3732ndash7236)
(4222ndash7444
)(C
I)95con
fidence
intervalof
thep
revalence
lowastlowast
Chi-S
quaretest119875valuelt
001
lowast
Chi-S
quaretest119875valuelt
005
BioMed Research International 7
Table 5 Frequency of pets (dogs or cats) infected or not infectedby intestinal parasites in northern Italy according to gastrointestinalsymptoms (presence or absence)
Infection No infection 119875 valuelowast
DogsSymptomatic 21 23 085Asymptomatic 48 48
CatSymptomatic 10 13 0128Asymptomatic 28 16
lowastFisherrsquos exact 119875 value
Table 6 Frequency of pets (dogs or cats) infected by intestinalparasites in northwestern Italy by features of their owners (number207)
Owner features Frequency of pets119875 valuelowast
Positive 119899 () Negative 119899 ()Gender
Female 75 (3694) 66 (3251) 024Male 29 (1428) 33 (1625)
Agele40 years old 65 (3202) 66 (3251) 031gt40 years old 39 (1921) 33 (1625)
Educationalqualification
Secondary schoolcertificate 38 (1871) 33 (1625) 037Intermediate schoolcertificateacademicdegree
66 (3251) 66 (3251)
Family componentsle2 42 (2058) 47 (2303) 020gt2 62 (3039) 53 (2598)
Presence of young lt15years old
Not 66 (3235) 68 (3333) 029Yes 38 (1862) 32 (1568)
lowastFisherrsquos exact 119875 value
Among the recovered helminthic species T canis and Tcati which accountedthe most frequent are consideredof great public health significance in their causing themost widespread and economically important zoonoses [30]Other parasites diffusing zoonoses ofminor importance werefound such as T vulpis Ancylostomatidae and Dypilid-ium canimum Finally molecular analysis on fecal samplesdemonstrated the presence of G duodenalis AssemblageA considered to have zoonotic potential [31] The overallprevalence of intestinal parasites both in dogs and in catsin northern Italy was higher than expected (119875 = 2816ndash5741 in dogs 119875 = 3258ndash6042 in cats) The currentlyreported prevalence rates of dog parasites are slightly differentconsidering the different origin of sampled dogs Particularlydogs from the large metropolitan area of Milan showed
lower prevalence than dogs from themicropolitan territoriesSeveral factors can justify these differences In fact most dogsfromMilan were rarely taken to large playgrounds limited intheir walks and regularly treated against heartworm diseaseFurther no colonies of stray dogs exist and proper disposalof dog waste from public soil is coming into common useamong urban pet owners On the other hand dogs frommicropolitan areas are usually at high risk of infection beingfrequently outdoors in their gardens or in large green areasIn addition transhumance being still practiced in Lombardythey might reasonably be infected by sheepdogs guardingtranshumant sheep flocks In fact they are moved fromAlpine pastures to lowlands twice yearly along the mainroutes (north to south) throughBergamo andBrescia towardsthe Po Plain areas whose fields may be contaminated by fecesof untreated sheepdog thus passing infection
In dogs as regards helminths only currently reportedprevalences significantly differ from what was previouslyobserved in Lombardy In 1974 in a coprological surveyconducted in some micropolitan areas located north andsouth of Milan helminths were recorded in 7579ndash853 ofexamined dogs [25] Further development in diagnosis andtreatment may account for the substantial differences foundwith our present survey together with a more widespreadprophylaxis against D immitis in the area of Milan whichmight have reasonably contributed to control canine intesti-nal parasites In 2007 helminth eggs were recovered in 7of dog feces collected from public places including parksof Milan [32] indicating a lower prevalence than in ourlatest survey (119875 = 141) This could be due to thekind of fecal samples collected from city soil that mainlyincluded droppings voided by old dogs typically showinglower infection values than young ones On the other handour findings are consistent with results from a recent surveyon pets from central Italy sampled in veterinary clinics wherehelminth infections were present in 241 of owned dogsand in 319 of owned cats [33] In the same year helminthinfections were recorded in 501 of stray cats from coloniespertaining to the metropolitan area of Milan [26]
Consistent with data obtained in several countriesascarids especially Toxocara spp were the most prevalentcanine and feline parasites [7 10 12ndash14 33 34] In contrastwith other surveys a low prevalence of Ancylostomatidaeinfection was recorded in our sampled dogs except thosefrom the micropolitan areas 1 and 2 A low presence ofhunting sporting or guard dogs in our samples as well asepidemiology and life cycle of Ancylostomatidae nematodescan account for this discrepancy [2 3 8 11 35]
As regardsG duodenalis it was themost prevalent canineand feline parasite according to other surveys [5 8ndash10 12]Such findings are not consistent with low prevalence valuesrecorded in the same species in other Italian studies whoseanalytical methods were different [32 36ndash39]
In this survey consistent with previous studies [31 40 41]G duodenalis assemblages C and D were isolated in dogsThey are considered host-adapted genotypes and a speciesname Giardia canis was proposed to label them As regardscats in our study the host-adapted F genotype was notfound however G duodenalis infections sustained also by
8 BioMed Research International
assemblages A B C and D have been previously describedin cats [40 42] In owned cats we observed a high prevalenceof G duodenalis infection by assemblage A whose possiblezoonotic potential must not be underestimated [31] FinallyG duodenalis assemblage D was recovered less frequentlythough [42 43]
Risk factors for dogs frommetropolitan andmicropolitanareas were being younger than 12 months or sharing thesame house with other dogs Compared to dogs from thelarge metropolitan area of Milan the odds for dogs from themicropolitan area 1 were 3476 times higher and the oddsfor dogs from MC 2 were 1947 times higher but with lowersignificance (119875 = 0001 versus 119875 = 0055) Further comparedto dogs le12 months old the odds of a dog gt12 months beingparasitized were 0362 times smaller Compared to single-household dogs the odds for multiple- household dogs were2059 times higher which means that cohabitation is oneof the most important risk factors associated to endopara-sitism In accordance with Katagiri andOliveira-Sequeira [2]who also found higher prevalence in multihousehold dogssignificant differences were found for Ancylostomatidae andT vulpis infections It might be that in the presence ofmultiple pets environmental contamination with infectivestages of these taxa occurs dogs become more susceptible toinfections and environmental contamination itself is higherand better maintained In cats the presence of endoparasiteswas associated only with their age housing and with the areathey lived in These findings are consistent with other studiesconsidering parasitism as of primarily concern for youngerdogs or cats [4 5 7 14] According to the univariate analysisthe overall prevalence of intestinal parasites in household catsshows statistically significant differences with cats that livedoutsidewith access to a garden (119875 = 50 in household versus119875 = 6552 in outdoor) Living outdoors or having accessto a garden seems to be a risk factor for T leonina infectionin cats as similarly described by Nareaho et al [15] It couldbe partially due to the source of infection for this parasitethat in addition to larvated eggs is represented by paratenichosts that harbour somatic third-stage larvae [44] As aconsequence of their predatory behavior domestic felinescould bemore susceptible to infections due to paratenic hostswhen they have outdoor access
Dogs and cats presenting gastrointestinal signs showed aprevalence of intestinal parasites close to 45 which urgesto differential diagnosis and periodic coprological exami-nation Prophylaxis against D immitis showed ineffectivein protecting dogs against gastrointestinal nematodes Forthem registered dosage of macrocyclic lactones used againstheartworms must be too low and seasonal administration ofthe treatment to all sampled adults dogs proved insufficientto cover their exposition to other risk factors all over theyear The answers to our questionnaire specifically designedto understand ownerrsquos awareness and information aboutcanine and feline gastrointestinal parasites showed thatthey knew but few aspects of the parasite biology In factmore than 7189 of them indicated that fecal contamina-tion can cause gastrointestinal parasite infection and thusthey were probably aware of the importance of reducingenvironmental fecal voiding Nonetheless 3910 of them
gave a negative answer or no answer at all As to possiblelasting environmental contamination due to infected petfecalization 5622 of total owners were not aware of it andmost of them probably did not consider preventing contactwith intermediateparatenic hosts as a possible prophylaxisagainst intestinal parasites infections A higher number ofowners (4811) correctly answered affirmatively when askedabout the possibility of transmission of intestinal parasitesto puppieskittens by infective milk of bitchesqueens Theymay be more stressed by clinicians on the importance ofintestinal parasite infections in puppies and kittens than inadult dogs and cats Concerning their awareness of risks forhuman health from canine and feline intestinal parasites5081 declared that intestinal parasites of dogs and cats donot represent any kind of risk for human health or that theydid not know about the issue Further 2637 out of 90owners informed about human health risks stated that theycould not name possible diseases thus confirming that theydid not know what proper behavior is necessary to reducezoonotic risks
Overall these results indicated that owners needed moreand clear information about zoonotic potential of intestinalparasites and that the veterinarians can be of extremeimportance in this process
5 Conclusion
Results of this survey showed that intestinal parasites are stilla common finding in owned dogs and cats not to be underes-timated in both metropolitan and micropolitan areas even ifthe latter indicated higher pet infection prevalence Furtherwhen a dog or a cat is presented to clinical examination onaccount of gastrointestinal signs intestinal parasite infectionshould be considered as a possible differential diagnosisThis condition can be asymptomatic and can even affectanimals under proper prophylaxis against D immitis thuseven apparently fit and healthy pets should be submitted toannual or biannual fecal examination Clinicians should alsoconsider that younger patients that live in micropolitan areasare the most susceptible to parasite infections The zoonoticparasites T canis and T cati T vulpis Ancylostomatidae andG duodenalis assemblage A resulted to be the most commonspecies in owned pets In any case veterinaries clearly play akey role in increasing awareness and knowledge of pet ownersabout canine and feline gastrointestinal parasites as to theirinfection routes proper monitoring and correct behavior toavoid potential zoonotic risks
Conflict of Interests
The authors declare that there is no conflict of interestsregarding the publication of this paper
References
[1] A C Y Lee PM Schantz K R Kazacos S PMontgomery andD D Bowman ldquoEpidemiologic and zoonotic aspects of ascaridinfections in dogs and catsrdquo Trends in Parasitology vol 26 no4 pp 155ndash161 2010
BioMed Research International 9
[2] S Katagiri and T C G Oliveira-Sequeira ldquoPrevalence of dogintestinal parasites and risk perception of zoonotic infectionby dog owners in Sao Paulo State Brazilrdquo Zoonoses and PublicHealth vol 55 no 8ndash10 pp 406ndash413 2008
[3] S E Little E M Johnson D Lewis et al ldquoPrevalence ofintestinal parasites in pet dogs in the United Statesrdquo VeterinaryParasitology vol 166 no 1-2 pp 144ndash152 2009
[4] D Barutzki andR Schaper ldquoResults of parasitological examina-tions of faecal samples from cats and dogs in Germany between2003 and 2010rdquo Parasitology Research vol 109 no 1 pp S45ndashS60 2011
[5] N Itoh H Ikegami M Takagi et al ldquoPrevalence of intestinalparasites in private-household cats in Japanrdquo Journal of FelineMedical Surgery vol 14 no 6 pp 436ndash439 2012
[6] M C Gates and T J Nolan ldquoEfficacy of heartworm pre-ventatives against ascarids and hookworms in client-owneddogs a retrospective case control studyrdquo Journal of VeterinaryPharmacology andTherapeutics vol 34 no 2 pp 116ndash119 2011
[7] M C Gates and T J Nolan ldquoEndoparasite prevalence andrecurrence across different age groups of dogs and catsrdquoVeterinary Parasitology vol 166 no 1-2 pp 153ndash158 2009
[8] F S Ferreira P Pereira-Baltasar R Parreira et al ldquoIntestinalparasites in dogs and cats from the district of Evora PortugalrdquoVeterinary Parasitology vol 179 no 1ndash3 pp 242ndash245 2011
[9] C Epe G Rehkter T Schnieder L Lorentzen and L Kreien-brock ldquoGiardia in symptomatic dogs and cats in Europe-Resultsof a European studyrdquo Veterinary Parasitology vol 173 no 1-2pp 32ndash38 2010
[10] D Joffe D van Niekerk F Gagne J Gilleard S Kutz and RLobingier ldquoThe prevalence of intestinal parasites in dogs andcats in Calgary ABrdquo Canadian Veterinary Journal vol 52 no12 pp 1323ndash1328 2011
[11] T M Savilla J E Joy J D May and C C SomervilleldquoPrevalence of dog intestinal nematode parasites in southcentral West Virginia USArdquo Veterinary Parasitology vol 178no 1-2 pp 115ndash120 2011
[12] E Claerebout S Casaert A-C Dalemans et al ldquoGiardiaand other intestinal parasites in different dog populations inNorthern BelgiumrdquoVeterinary Parasitology vol 161 no 1-2 pp41ndash46 2009
[13] P A M Overgaauw L van Zutphen D Hoek et al ldquoZoonoticparasites in fecal samples and fur from dogs and cats in TheNetherlandsrdquo Veterinary Parasitology vol 163 no 1-2 pp 115ndash122 2009
[14] M C Gates and T J Nolan ldquoRisk factors for endoparasitismin dogs retrospective case-control study of 6578 veterinaryteaching hospital casesrdquo Journal of Small Animal Practice vol50 no 12 pp 636ndash640 2009
[15] A Nareaho J Puomio K Saarinen P Jokelainen T Juseliusand A Sukura ldquoFeline intestinal parasites in Finland preva-lence risk factors and anthelmintic treatment practicesrdquo Journalof Feline Medicine and Surgery vol 14 no 6 pp 378ndash383 2012
[16] L Polley and R C A Thompson ldquoParasite zoonoses and cli-mate change molecular tools for tracking shifting boundariesrdquoTrends in Parasitology vol 25 no 6 pp 285ndash291 2009
[17] E J Jenkins J M Schurer and K M Gesy ldquoOld problems on anew playing field helminth zoonoses transmitted among dogswildlife and people in a changing northern climaterdquoVeterinaryParasitology vol 182 no 1 pp 54ndash69 2011
[18] P N Acha and B Szyfres Zoonoses et Maladies TransmissiblesCommunes a lrsquohomme et Aux animaux Office International desEpizooties Paris France 1989
[19] M Fisher ldquoToxocara cati an underestimated zoonotic agentrdquoTrends in Parasitology vol 19 no 4 pp 167ndash170 2003
[20] Y Masuda T Kishimoto H Ito and M Tsuji ldquoVisceral larvamigrans caused by Trichuris vulpis presenting as a pulmonarymassrdquoThorax vol 42 no 12 pp 990ndash991 1987
[21] J J Dunn S T Columbus W E Aldeen M Davis and K CCarroll ldquoTrichuris vulpis recovered from a patient with chronicdiarrhea and five dogsrdquo Journal of Clinical Microbiology vol 40no 7 pp 2703ndash2704 2002
[22] M Papazahariadou A Founta E Papadopoulos SChliounakis K Antoniadou-Sotiriadou and Y TheodoridesldquoGastrointestinal parasites of shepherd and hunting dogs in theSerres Prefecture Northern Greecerdquo Veterinary Parasitologyvol 148 no 2 pp 170ndash173 2007
[23] C Martınez-Carrasco E Berriatua M Garijo J Martınez FD Alonso and R Ruiz De Ybanez ldquoEpidemiological study ofnon-systemic parasitism in dogs in southeast MediterraneanSpain assessed by coprological and post-mortem examinationrdquoZoonoses and Public Health vol 54 no 5 pp 195ndash203 2007
[24] S Leonhard K Pfister P Beelitz C Wielinga and R C AThompson ldquoThe molecular characterisation of Giardia fromdogs in southern Germanyrdquo Veterinary Parasitology vol 150no 1-2 pp 33ndash38 2007
[25] C Genchi G Gili and R Maraschin ldquoIndagine sullrsquoincidenzadelle elmintiasi intestinali del cane in alcune zone della Lom-bardiardquo La Clinica Veterinaria vol 97 no 6 pp 178ndash186 1974
[26] E Spada D Proverbio A Della Pepa et al ldquoPrevalence offaecal-borne parasites in colony stray cats in northern ItalyrdquoJournal of Feline Medicine and Surgery vol 15 no 8 pp 672ndash677 2013
[27] R M Hopkins B P Meloni D M Groth J D WetherallJ A Reynoldson and R C A Thompson ldquoRibosomal RNAsequencing reveals differences between the genotypes of Giar-dia isolates recovered from humans and dogs living in the samelocalityrdquo Journal of Parasitology vol 83 no 1 pp 44ndash51 1997
[28] C Read J Walters I D Robertson and R C A ThompsonldquoCorrelation between genotype of Giardia duodenalis anddiarrhoeardquo International Journal for Parasitology vol 32 no 2pp 229ndash231 2002
[29] A O Bush K D Lafferty J M Lotz and A W ShostakldquoParasitology meets ecology on its own terms Margolis et alrevisitedrdquo Journal of Parasitology vol 83 no 4 pp 575ndash5831997
[30] C N L Macpherson ldquoThe epidemiology and public healthimportance of toxocariasis a zoonosis of global importancerdquoInternational Journal for Parasitology vol 43 pp 999ndash10082013
[31] U Ryan and S M Caccio ldquoZoonotic potential of GiardiardquoInternational Journal For Parasitology vol 43 pp 943ndash9562013
[32] M Genchi E Ferroglio G Traldi S Passera G MezzanoandCGenchi ldquoFecalizzazione ambientale e rischio parassitarionelle citta di Milano e Torinordquo Professione Veterinaria vol 41pp 15ndash17 2007
[33] F Riggio R Mannella G Ariti and S Perrucci ldquoIntestinaland lung parasites in owned dogs and cats from central ItalyrdquoVeterinary Parasitology vol 193 no 1ndash3 pp 78ndash84 2013
[34] LMugnaini R Papini G Gorini A Passantino VMerildi andF Mancianti ldquoPattern and predictive factors of endoparasitismin cats in central Italyrdquo Revue de Medecine Veterinaire vol 163no 2 pp 85ndash88 2012
10 BioMed Research International
[35] D Traversa ldquoPet roundworms and hookworms a continuingneed for global wormingrdquo Parasite amp Vectors vol 5 no 1 p 912012
[36] F Berrilli D di Cave C de Liberato A Franco PScaramozzino and P Orecchia ldquoGenotype characterisation ofGiardia duodenalis isolates from domestic and farm animals bySSU-rRNA gene sequencingrdquo Veterinary Parasitology vol 122no 3 pp 193ndash199 2004
[37] P Bianciardi R Papini G Giuliani andG Cardini ldquoPrevalenceof Giardia antigen in stool samples from dogs and catsrdquo Revuede Medecine Veterinaire vol 155 no 8-9 pp 417ndash421 2004
[38] G Capelli A Frangipane di Regalbono R Iorio M PietrobelliB Paoletti and A Giangaspero ldquoGiardia species and otherintestinal parasites in dogs in north-east and central ItalyrdquoVeterinary Record vol 159 no 13 pp 422ndash424 2006
[39] L Rinaldi M P Maurelli V Musella et al ldquoGiardia andCryptosporidium in canine faecal samples contaminating anurban areardquo Research in Veterinary Science vol 84 no 3 pp413ndash415 2008
[40] A V Scorza L R Ballweber S Tangtrongsup C Panuska andM R Lappin ldquoComparisons of mammalianGiardia duodenalisassemblages based on the 120573-giardin glutamate dehydrogenaseand triose phosphate isomerase genesrdquo Veterinary Parasitologyvol 189 no 2ndash4 pp 182ndash188 2012
[41] F D Uehlinger S J Greenwood J T McClure G B ConboyR OrsquoHandley and H W Barkema ldquoZoonotic potential ofGiardia duodenalis and Cryptosporidium spp and prevalenceof intestinal parasites in young dogs from different populationson Prince Edward Island Canadardquo Veterinary Parasitology vol196 no 3-4 pp 509ndash514 2013
[42] L R Ballweber L Xiao D D Bowman G Kahn and V ACama ldquoGiardiasis in dogs and cats update on epidemiology andpublic health significancerdquo Trends in Parasitology vol 26 no 4pp 180ndash189 2010
[43] D Jaros W Zygner S Jaros and HWedrychowicz ldquoDetectionof Giardia intestinalis assemblages A B and D in domestic catsfrom Warsaw Polandrdquo Polish Journal of Microbiology vol 60no 3 pp 259ndash263 2011
[44] R C AndersonNematode Parasites of Vertebrates Their Devel-opment and Transmission Cabi Publishing Wallingford UK2nd edition 2000
Submit your manuscripts athttpwwwhindawicom
Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014
Anatomy Research International
PeptidesInternational Journal of
Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014
Hindawi Publishing Corporation httpwwwhindawicom
International Journal of
Volume 2014
Zoology
Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014
Molecular Biology International
GenomicsInternational Journal of
Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014
The Scientific World JournalHindawi Publishing Corporation httpwwwhindawicom Volume 2014
Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014
BioinformaticsAdvances in
Marine BiologyJournal of
Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014
Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014
Signal TransductionJournal of
Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014
BioMed Research International
Evolutionary BiologyInternational Journal of
Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014
Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014
Biochemistry Research International
ArchaeaHindawi Publishing Corporationhttpwwwhindawicom Volume 2014
Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014
Genetics Research International
Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014
Advances in
Virolog y
Hindawi Publishing Corporationhttpwwwhindawicom
Nucleic AcidsJournal of
Volume 2014
Stem CellsInternational
Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014
Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014
Enzyme Research
Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014
International Journal of
Microbiology
4 BioMed Research International
Table 1 Prevalence () and confidence interval (CI) of intestinal parasites in 253 owned dogs and 156 owned cats in northern Italy
Parasites Metropolitan area Micropolitan area 1 Micropolitan area 2 (CI) (CI) (CI)
Dogs
Toxocara canis 448 2222 930(209ndash1086) (1077ndash3668) (304ndash1557)
Toxascaris leonina 0 370 0(0-0) (0ndash891) (0-0)
Ancylostomatidae 097 556 349(017ndash529) (0ndash1187) (0ndash745)
Trichuris vulpis 608 1111 581(333ndash1337) (245ndash1977) (077ndash1086)
Strongyloides stercoralis 194 0 0(053ndash68) (0-0) (0-0)
Eucoleus aerophilus 097 0 0(017ndash529) (0-0) (0-0)
Dipylidium caninum 0 286 0(0) (010ndash562) (0-0)
Cystoisospora sp 097 370 698(017ndash529) (0ndash891) (148ndash1247)
Giardia duodenalis 1605 2037 2558(1056ndash2485) (927ndash3147) (1617ndash3499)
Overall prevalence 2816 5741 4302(2038ndash3751) (4378ndash7103) (3235ndash5370)
Cats
Toxocara cati 562 526 2239(242ndash1249) (0ndash1632) (1241ndash3237)
Toxascaris leonina 0 526 896(0-0) (0ndash1632) (212ndash1580)
Ancylostomatidae 112 0 208(002ndash609) (0-0) (0ndash627)
Trichuris vulpis 0 0 208(0-0) (0-0) (0ndash627)
Dipylidium caninum 0 286 448(0-0) (010ndash562) (0ndash943)
Spirometra 112 0 0(002ndash609) (0-0) (0-0)
Cystoisospora sp 112 526 417(002ndash609) (0ndash1632) (0ndash1003)
Toxoplasma-like 112 0 0(002ndash609) (0-0) (0-0)
Giardia duodenalis 2247 3684 2500(1504ndash3218) (1296ndash6073) (1229ndash3771)
Overall prevalence 3258 4737 6042(2374ndash4286) (2264ndash7209) (4607ndash7477)
1514 declared they had even never considered such prob-ability Of the ninety owners aware of zoonoses risk 7252of them thought that the most common source of infectionis contaminated food 23 answered that transmission ofparasites to humans is caused by direct contact with petswhile 440 had no idea Gender age and education level ofpet owners as well as their family size and possible presence
of young members do not seem to affect animal occurrenceof intestinal parasite infections (Table 6)
4 Discussion
The intestinal parasites in this survey are consistent with thetypical parasite spectrum of domestic carnivores worldwide
BioMed Research International 5
Table 2 Univariate analysis of risk factors for intestinal parasites in dogs and cats presenting at two veterinary practices in northern Italy
Variable Risk factor OR 95 CI 119875 valueDogs
HabitationMetropolitan 100 0006
Micropolitan area 1 3476 1632ndash7403 0001Micropolitan area 2 1947 0986ndash3845 0055
Age le12 months 100 NAgt12 months 0362 0205ndash0639 0000
Gender Male 100 NAFemales 0756 0433ndash1320 0325
SizeSmall 1 0917
Medium 0937 0451ndash1946 0861Large 1165 0439ndash3092 0760
Housing Household 1 NAOutdoor 0827 0364ndash1880 0651
Husbandry Single-dog-household 1 NAMultiple-dog-household 2059 1047ndash4051 0036
Cats
HabitationMetropolitan 100 0008
Micropolitan area 1 2100 0730ndash6039 0169Micropolitan area 2 3561 1601ndash7924 0002
Age le12 months 100 NAgt12 months 0347 0168ndash0716 0004
Gender Males 100 NAFemale 0809 0401ndash1631 0553
Housing Outdoorhousehold 1 NAHousehold 0526 0195ndash1424 0006
Husbandry Single-cat-household 1 NAMultiple-cat-household 1153 0437ndash3039 0774
OR odds ratio(CI) 95 confidence interval
Table 3 Final multivariate analysis of risks factors associated with intestinal parasites in dogs and cats presenting at two veterinary practicesin northern Italy
Variable Risk factor OR 95 CI 119875 valueDogs
Age gt12 months 100 NAle12 months 0445 0222ndash0894 0023
Husbandry Single-dog-household 1 NAMultiple-dog-household 2240 1115ndash4498 0023
Cats
HabitationMetropolitan area 100 0011Micropolitan area 1 2279 0762ndash6814 0141Micropolitan area 2 3510 1536ndash8020 0003
Age gt12 months 100 NAle12 months 0348 0163ndash0742 0006
OR odds ratio(CI) 95 confidence interval
6 BioMed Research InternationalTa
ble4Prevalence
()a
nd95CI
(minndashm
ax)o
fintestin
alparasites
indo
gsandcatsby
individu
alfeatures
andmanagem
ent
Parasites
Gender
Age
Hou
sing
Husband
ryMale
Female
le12
mon
ths
gt12
mon
ths
Hou
seho
ldOutdo
orSing
leMultip
leDogs
(119899=116)
(119899=92)
(119899=92)
(119899=116)
(119899=56)
(119899=84)
(119899=74)
(119899=66)
Toxocara
canis
1379
761
2065lowastlowast
345lowastlowast
1071
1667
1081
1818
(752ndash2007)
(219
ndash1303)
(1238ndash2892)
(013
ndash677)
(261ndash1881)
(870ndash
2464)
(374
ndash178
8)(888ndash2748)
Toxascarisleo
nina
086
109
109
086
0238
135
152
(0ndash254)
(0ndash321)
(0ndash321)
(0ndash254)
mdash(0ndash564)
(0ndash398)
(0ndash4
47)
Ancylostomatidae
345
326
326
345
179
595
0lowastlowast
909lowastlowast
(013
ndash677)
(0ndash6
89)
(0ndash6
89)
(013
ndash677)
(0ndash526)
(089ndash
1101)
mdash(215
ndash1603)
Trich
urisvulpis
517
870
326
948
536
952
270lowast
1364lowast
(114
ndash920)
(294ndash
1445)
(0ndash6
89)
(415
ndash1481)
(0ndash112
6)(324ndash
1580)
(0ndash6
39)
(536ndash
2192)
Eucoleu
saerophilus
010
90
086
00
00
mdash(0ndash321)
mdash(0ndash254)
mdashmdash
mdashmdash
Dipylidium
caninu
m17
2217
217
172
536
119
270
303
(0ndash4
09)
(0ndash515
)(0ndash515
)(0ndash4
09)
(0ndash112
6)(0ndash351)
(0ndash6
39)
(0ndash717
)
Cysto
isosporasp
345
543
870lowastlowast
086lowastlowast
1071lowast
238lowast
541
606
(013
ndash677)
(080ndash
1007)
(294ndash
1445)
(0ndash254)
(261ndash1881)
(0ndash564)
(026ndash
1056)
(030ndash
1182)
Giardiadu
odenalis
2155
1848
2717lowast
1466lowast
2679
2143
2297
2424
(1407ndash2903)
(1055ndash2641)
(1808ndash3626)
(822ndash2109)
(1519ndash3839)
(1265ndash3021)
(1339ndash3255)
(1390ndash3458)
Overallprevalence
4483
3804
5543lowastlowast
2931lowastlowast
5044
83
4054lowast
5758lowast
(3578ndash5388)
(2812ndash4
796)
(4528ndash6
559)
(210
3ndash3759)
(3690ndash6
315)
(2558ndash6
408)
(293
5ndash5173)
(4566ndash6
950)
Cats
(119899=62)
(119899=65)
(119899=61)
(119899=66)
(119899=38)
(119899=29)
(119899=31)
(119899=36)
Toxocara
cati
1290
1231
1967lowast
606lowast
2368
2069
1935
2500
(456ndash
2125)
(432
ndash2029)
(970ndash
2965)
(030ndash
1182)
(1016ndash372
0)(595ndash3543)
(544ndash
3326)
(1085ndash391
5)
Toxascarisleo
nina
323
615
984lowastlowast
0lowastlowast
263lowast
1724lowast
968
833
(0ndash762)
(031ndash1200)
(236ndash
1731)
mdash(0ndash772)
(349ndash
3099)
(0ndash2009)
(0ndash173
6)
Ancylostomatidae
161
016
40
263
00
278
(0ndash4
75)
mdash(0ndash4
83)
mdash(0ndash772)
mdashmdash
(0ndash815
)
Trich
urisvulpis
161
00
152
0345
0278
(0ndash4
75)
mdashmdash
(0ndash4
46)
mdash(0ndash1009)
mdash(0ndash815
)
Dipylidium
caninu
m323
154
0455
789
0323
556
(0ndash762)
(0ndash4
53)
(0ndash957)
(0ndash1646
)mdash
(0ndash945)
(0ndash1305)
Spiro
metra
sp
161
016
40
00
00
(0ndash4
75)
mdash(0ndash4
83)
mdashmdash
mdashmdash
mdash
Cysto
isosporasp
161
462
492
152
263
690
0833
(0ndash4
75)
(0ndash972)
(0ndash1034)
(0ndash4
46)
(0ndash772)
(0ndash1612)
mdash(0ndash173
6)
Toxoplasma-lik
e0
154
015
20
00
0mdash
(0ndash4
53)
mdash(0ndash4
46)
mdashmdash
mdashmdash
Giardiadu
odenalis
2903
2615
3279
2273
2368
3448
3548
2222
(177
3ndash40
33)
(1547ndash3684)
(210
1ndash44
57)
(1262ndash3284)
(1016ndash372
0)(1718ndash5178)
(1864
ndash5232)
(864ndash
3580)
Overallprevalence
4677
4154
5738lowastlowast
3182lowastlowast
506552
5484
5833
(3435ndash591
9)(295
6ndash5352
)(4497ndash6
979)
(2058ndash4
306)
(3410ndash6
590)
(4822ndash8282)
(3732ndash7236)
(4222ndash7444
)(C
I)95con
fidence
intervalof
thep
revalence
lowastlowast
Chi-S
quaretest119875valuelt
001
lowast
Chi-S
quaretest119875valuelt
005
BioMed Research International 7
Table 5 Frequency of pets (dogs or cats) infected or not infectedby intestinal parasites in northern Italy according to gastrointestinalsymptoms (presence or absence)
Infection No infection 119875 valuelowast
DogsSymptomatic 21 23 085Asymptomatic 48 48
CatSymptomatic 10 13 0128Asymptomatic 28 16
lowastFisherrsquos exact 119875 value
Table 6 Frequency of pets (dogs or cats) infected by intestinalparasites in northwestern Italy by features of their owners (number207)
Owner features Frequency of pets119875 valuelowast
Positive 119899 () Negative 119899 ()Gender
Female 75 (3694) 66 (3251) 024Male 29 (1428) 33 (1625)
Agele40 years old 65 (3202) 66 (3251) 031gt40 years old 39 (1921) 33 (1625)
Educationalqualification
Secondary schoolcertificate 38 (1871) 33 (1625) 037Intermediate schoolcertificateacademicdegree
66 (3251) 66 (3251)
Family componentsle2 42 (2058) 47 (2303) 020gt2 62 (3039) 53 (2598)
Presence of young lt15years old
Not 66 (3235) 68 (3333) 029Yes 38 (1862) 32 (1568)
lowastFisherrsquos exact 119875 value
Among the recovered helminthic species T canis and Tcati which accountedthe most frequent are consideredof great public health significance in their causing themost widespread and economically important zoonoses [30]Other parasites diffusing zoonoses ofminor importance werefound such as T vulpis Ancylostomatidae and Dypilid-ium canimum Finally molecular analysis on fecal samplesdemonstrated the presence of G duodenalis AssemblageA considered to have zoonotic potential [31] The overallprevalence of intestinal parasites both in dogs and in catsin northern Italy was higher than expected (119875 = 2816ndash5741 in dogs 119875 = 3258ndash6042 in cats) The currentlyreported prevalence rates of dog parasites are slightly differentconsidering the different origin of sampled dogs Particularlydogs from the large metropolitan area of Milan showed
lower prevalence than dogs from themicropolitan territoriesSeveral factors can justify these differences In fact most dogsfromMilan were rarely taken to large playgrounds limited intheir walks and regularly treated against heartworm diseaseFurther no colonies of stray dogs exist and proper disposalof dog waste from public soil is coming into common useamong urban pet owners On the other hand dogs frommicropolitan areas are usually at high risk of infection beingfrequently outdoors in their gardens or in large green areasIn addition transhumance being still practiced in Lombardythey might reasonably be infected by sheepdogs guardingtranshumant sheep flocks In fact they are moved fromAlpine pastures to lowlands twice yearly along the mainroutes (north to south) throughBergamo andBrescia towardsthe Po Plain areas whose fields may be contaminated by fecesof untreated sheepdog thus passing infection
In dogs as regards helminths only currently reportedprevalences significantly differ from what was previouslyobserved in Lombardy In 1974 in a coprological surveyconducted in some micropolitan areas located north andsouth of Milan helminths were recorded in 7579ndash853 ofexamined dogs [25] Further development in diagnosis andtreatment may account for the substantial differences foundwith our present survey together with a more widespreadprophylaxis against D immitis in the area of Milan whichmight have reasonably contributed to control canine intesti-nal parasites In 2007 helminth eggs were recovered in 7of dog feces collected from public places including parksof Milan [32] indicating a lower prevalence than in ourlatest survey (119875 = 141) This could be due to thekind of fecal samples collected from city soil that mainlyincluded droppings voided by old dogs typically showinglower infection values than young ones On the other handour findings are consistent with results from a recent surveyon pets from central Italy sampled in veterinary clinics wherehelminth infections were present in 241 of owned dogsand in 319 of owned cats [33] In the same year helminthinfections were recorded in 501 of stray cats from coloniespertaining to the metropolitan area of Milan [26]
Consistent with data obtained in several countriesascarids especially Toxocara spp were the most prevalentcanine and feline parasites [7 10 12ndash14 33 34] In contrastwith other surveys a low prevalence of Ancylostomatidaeinfection was recorded in our sampled dogs except thosefrom the micropolitan areas 1 and 2 A low presence ofhunting sporting or guard dogs in our samples as well asepidemiology and life cycle of Ancylostomatidae nematodescan account for this discrepancy [2 3 8 11 35]
As regardsG duodenalis it was themost prevalent canineand feline parasite according to other surveys [5 8ndash10 12]Such findings are not consistent with low prevalence valuesrecorded in the same species in other Italian studies whoseanalytical methods were different [32 36ndash39]
In this survey consistent with previous studies [31 40 41]G duodenalis assemblages C and D were isolated in dogsThey are considered host-adapted genotypes and a speciesname Giardia canis was proposed to label them As regardscats in our study the host-adapted F genotype was notfound however G duodenalis infections sustained also by
8 BioMed Research International
assemblages A B C and D have been previously describedin cats [40 42] In owned cats we observed a high prevalenceof G duodenalis infection by assemblage A whose possiblezoonotic potential must not be underestimated [31] FinallyG duodenalis assemblage D was recovered less frequentlythough [42 43]
Risk factors for dogs frommetropolitan andmicropolitanareas were being younger than 12 months or sharing thesame house with other dogs Compared to dogs from thelarge metropolitan area of Milan the odds for dogs from themicropolitan area 1 were 3476 times higher and the oddsfor dogs from MC 2 were 1947 times higher but with lowersignificance (119875 = 0001 versus 119875 = 0055) Further comparedto dogs le12 months old the odds of a dog gt12 months beingparasitized were 0362 times smaller Compared to single-household dogs the odds for multiple- household dogs were2059 times higher which means that cohabitation is oneof the most important risk factors associated to endopara-sitism In accordance with Katagiri andOliveira-Sequeira [2]who also found higher prevalence in multihousehold dogssignificant differences were found for Ancylostomatidae andT vulpis infections It might be that in the presence ofmultiple pets environmental contamination with infectivestages of these taxa occurs dogs become more susceptible toinfections and environmental contamination itself is higherand better maintained In cats the presence of endoparasiteswas associated only with their age housing and with the areathey lived in These findings are consistent with other studiesconsidering parasitism as of primarily concern for youngerdogs or cats [4 5 7 14] According to the univariate analysisthe overall prevalence of intestinal parasites in household catsshows statistically significant differences with cats that livedoutsidewith access to a garden (119875 = 50 in household versus119875 = 6552 in outdoor) Living outdoors or having accessto a garden seems to be a risk factor for T leonina infectionin cats as similarly described by Nareaho et al [15] It couldbe partially due to the source of infection for this parasitethat in addition to larvated eggs is represented by paratenichosts that harbour somatic third-stage larvae [44] As aconsequence of their predatory behavior domestic felinescould bemore susceptible to infections due to paratenic hostswhen they have outdoor access
Dogs and cats presenting gastrointestinal signs showed aprevalence of intestinal parasites close to 45 which urgesto differential diagnosis and periodic coprological exami-nation Prophylaxis against D immitis showed ineffectivein protecting dogs against gastrointestinal nematodes Forthem registered dosage of macrocyclic lactones used againstheartworms must be too low and seasonal administration ofthe treatment to all sampled adults dogs proved insufficientto cover their exposition to other risk factors all over theyear The answers to our questionnaire specifically designedto understand ownerrsquos awareness and information aboutcanine and feline gastrointestinal parasites showed thatthey knew but few aspects of the parasite biology In factmore than 7189 of them indicated that fecal contamina-tion can cause gastrointestinal parasite infection and thusthey were probably aware of the importance of reducingenvironmental fecal voiding Nonetheless 3910 of them
gave a negative answer or no answer at all As to possiblelasting environmental contamination due to infected petfecalization 5622 of total owners were not aware of it andmost of them probably did not consider preventing contactwith intermediateparatenic hosts as a possible prophylaxisagainst intestinal parasites infections A higher number ofowners (4811) correctly answered affirmatively when askedabout the possibility of transmission of intestinal parasitesto puppieskittens by infective milk of bitchesqueens Theymay be more stressed by clinicians on the importance ofintestinal parasite infections in puppies and kittens than inadult dogs and cats Concerning their awareness of risks forhuman health from canine and feline intestinal parasites5081 declared that intestinal parasites of dogs and cats donot represent any kind of risk for human health or that theydid not know about the issue Further 2637 out of 90owners informed about human health risks stated that theycould not name possible diseases thus confirming that theydid not know what proper behavior is necessary to reducezoonotic risks
Overall these results indicated that owners needed moreand clear information about zoonotic potential of intestinalparasites and that the veterinarians can be of extremeimportance in this process
5 Conclusion
Results of this survey showed that intestinal parasites are stilla common finding in owned dogs and cats not to be underes-timated in both metropolitan and micropolitan areas even ifthe latter indicated higher pet infection prevalence Furtherwhen a dog or a cat is presented to clinical examination onaccount of gastrointestinal signs intestinal parasite infectionshould be considered as a possible differential diagnosisThis condition can be asymptomatic and can even affectanimals under proper prophylaxis against D immitis thuseven apparently fit and healthy pets should be submitted toannual or biannual fecal examination Clinicians should alsoconsider that younger patients that live in micropolitan areasare the most susceptible to parasite infections The zoonoticparasites T canis and T cati T vulpis Ancylostomatidae andG duodenalis assemblage A resulted to be the most commonspecies in owned pets In any case veterinaries clearly play akey role in increasing awareness and knowledge of pet ownersabout canine and feline gastrointestinal parasites as to theirinfection routes proper monitoring and correct behavior toavoid potential zoonotic risks
Conflict of Interests
The authors declare that there is no conflict of interestsregarding the publication of this paper
References
[1] A C Y Lee PM Schantz K R Kazacos S PMontgomery andD D Bowman ldquoEpidemiologic and zoonotic aspects of ascaridinfections in dogs and catsrdquo Trends in Parasitology vol 26 no4 pp 155ndash161 2010
BioMed Research International 9
[2] S Katagiri and T C G Oliveira-Sequeira ldquoPrevalence of dogintestinal parasites and risk perception of zoonotic infectionby dog owners in Sao Paulo State Brazilrdquo Zoonoses and PublicHealth vol 55 no 8ndash10 pp 406ndash413 2008
[3] S E Little E M Johnson D Lewis et al ldquoPrevalence ofintestinal parasites in pet dogs in the United Statesrdquo VeterinaryParasitology vol 166 no 1-2 pp 144ndash152 2009
[4] D Barutzki andR Schaper ldquoResults of parasitological examina-tions of faecal samples from cats and dogs in Germany between2003 and 2010rdquo Parasitology Research vol 109 no 1 pp S45ndashS60 2011
[5] N Itoh H Ikegami M Takagi et al ldquoPrevalence of intestinalparasites in private-household cats in Japanrdquo Journal of FelineMedical Surgery vol 14 no 6 pp 436ndash439 2012
[6] M C Gates and T J Nolan ldquoEfficacy of heartworm pre-ventatives against ascarids and hookworms in client-owneddogs a retrospective case control studyrdquo Journal of VeterinaryPharmacology andTherapeutics vol 34 no 2 pp 116ndash119 2011
[7] M C Gates and T J Nolan ldquoEndoparasite prevalence andrecurrence across different age groups of dogs and catsrdquoVeterinary Parasitology vol 166 no 1-2 pp 153ndash158 2009
[8] F S Ferreira P Pereira-Baltasar R Parreira et al ldquoIntestinalparasites in dogs and cats from the district of Evora PortugalrdquoVeterinary Parasitology vol 179 no 1ndash3 pp 242ndash245 2011
[9] C Epe G Rehkter T Schnieder L Lorentzen and L Kreien-brock ldquoGiardia in symptomatic dogs and cats in Europe-Resultsof a European studyrdquo Veterinary Parasitology vol 173 no 1-2pp 32ndash38 2010
[10] D Joffe D van Niekerk F Gagne J Gilleard S Kutz and RLobingier ldquoThe prevalence of intestinal parasites in dogs andcats in Calgary ABrdquo Canadian Veterinary Journal vol 52 no12 pp 1323ndash1328 2011
[11] T M Savilla J E Joy J D May and C C SomervilleldquoPrevalence of dog intestinal nematode parasites in southcentral West Virginia USArdquo Veterinary Parasitology vol 178no 1-2 pp 115ndash120 2011
[12] E Claerebout S Casaert A-C Dalemans et al ldquoGiardiaand other intestinal parasites in different dog populations inNorthern BelgiumrdquoVeterinary Parasitology vol 161 no 1-2 pp41ndash46 2009
[13] P A M Overgaauw L van Zutphen D Hoek et al ldquoZoonoticparasites in fecal samples and fur from dogs and cats in TheNetherlandsrdquo Veterinary Parasitology vol 163 no 1-2 pp 115ndash122 2009
[14] M C Gates and T J Nolan ldquoRisk factors for endoparasitismin dogs retrospective case-control study of 6578 veterinaryteaching hospital casesrdquo Journal of Small Animal Practice vol50 no 12 pp 636ndash640 2009
[15] A Nareaho J Puomio K Saarinen P Jokelainen T Juseliusand A Sukura ldquoFeline intestinal parasites in Finland preva-lence risk factors and anthelmintic treatment practicesrdquo Journalof Feline Medicine and Surgery vol 14 no 6 pp 378ndash383 2012
[16] L Polley and R C A Thompson ldquoParasite zoonoses and cli-mate change molecular tools for tracking shifting boundariesrdquoTrends in Parasitology vol 25 no 6 pp 285ndash291 2009
[17] E J Jenkins J M Schurer and K M Gesy ldquoOld problems on anew playing field helminth zoonoses transmitted among dogswildlife and people in a changing northern climaterdquoVeterinaryParasitology vol 182 no 1 pp 54ndash69 2011
[18] P N Acha and B Szyfres Zoonoses et Maladies TransmissiblesCommunes a lrsquohomme et Aux animaux Office International desEpizooties Paris France 1989
[19] M Fisher ldquoToxocara cati an underestimated zoonotic agentrdquoTrends in Parasitology vol 19 no 4 pp 167ndash170 2003
[20] Y Masuda T Kishimoto H Ito and M Tsuji ldquoVisceral larvamigrans caused by Trichuris vulpis presenting as a pulmonarymassrdquoThorax vol 42 no 12 pp 990ndash991 1987
[21] J J Dunn S T Columbus W E Aldeen M Davis and K CCarroll ldquoTrichuris vulpis recovered from a patient with chronicdiarrhea and five dogsrdquo Journal of Clinical Microbiology vol 40no 7 pp 2703ndash2704 2002
[22] M Papazahariadou A Founta E Papadopoulos SChliounakis K Antoniadou-Sotiriadou and Y TheodoridesldquoGastrointestinal parasites of shepherd and hunting dogs in theSerres Prefecture Northern Greecerdquo Veterinary Parasitologyvol 148 no 2 pp 170ndash173 2007
[23] C Martınez-Carrasco E Berriatua M Garijo J Martınez FD Alonso and R Ruiz De Ybanez ldquoEpidemiological study ofnon-systemic parasitism in dogs in southeast MediterraneanSpain assessed by coprological and post-mortem examinationrdquoZoonoses and Public Health vol 54 no 5 pp 195ndash203 2007
[24] S Leonhard K Pfister P Beelitz C Wielinga and R C AThompson ldquoThe molecular characterisation of Giardia fromdogs in southern Germanyrdquo Veterinary Parasitology vol 150no 1-2 pp 33ndash38 2007
[25] C Genchi G Gili and R Maraschin ldquoIndagine sullrsquoincidenzadelle elmintiasi intestinali del cane in alcune zone della Lom-bardiardquo La Clinica Veterinaria vol 97 no 6 pp 178ndash186 1974
[26] E Spada D Proverbio A Della Pepa et al ldquoPrevalence offaecal-borne parasites in colony stray cats in northern ItalyrdquoJournal of Feline Medicine and Surgery vol 15 no 8 pp 672ndash677 2013
[27] R M Hopkins B P Meloni D M Groth J D WetherallJ A Reynoldson and R C A Thompson ldquoRibosomal RNAsequencing reveals differences between the genotypes of Giar-dia isolates recovered from humans and dogs living in the samelocalityrdquo Journal of Parasitology vol 83 no 1 pp 44ndash51 1997
[28] C Read J Walters I D Robertson and R C A ThompsonldquoCorrelation between genotype of Giardia duodenalis anddiarrhoeardquo International Journal for Parasitology vol 32 no 2pp 229ndash231 2002
[29] A O Bush K D Lafferty J M Lotz and A W ShostakldquoParasitology meets ecology on its own terms Margolis et alrevisitedrdquo Journal of Parasitology vol 83 no 4 pp 575ndash5831997
[30] C N L Macpherson ldquoThe epidemiology and public healthimportance of toxocariasis a zoonosis of global importancerdquoInternational Journal for Parasitology vol 43 pp 999ndash10082013
[31] U Ryan and S M Caccio ldquoZoonotic potential of GiardiardquoInternational Journal For Parasitology vol 43 pp 943ndash9562013
[32] M Genchi E Ferroglio G Traldi S Passera G MezzanoandCGenchi ldquoFecalizzazione ambientale e rischio parassitarionelle citta di Milano e Torinordquo Professione Veterinaria vol 41pp 15ndash17 2007
[33] F Riggio R Mannella G Ariti and S Perrucci ldquoIntestinaland lung parasites in owned dogs and cats from central ItalyrdquoVeterinary Parasitology vol 193 no 1ndash3 pp 78ndash84 2013
[34] LMugnaini R Papini G Gorini A Passantino VMerildi andF Mancianti ldquoPattern and predictive factors of endoparasitismin cats in central Italyrdquo Revue de Medecine Veterinaire vol 163no 2 pp 85ndash88 2012
10 BioMed Research International
[35] D Traversa ldquoPet roundworms and hookworms a continuingneed for global wormingrdquo Parasite amp Vectors vol 5 no 1 p 912012
[36] F Berrilli D di Cave C de Liberato A Franco PScaramozzino and P Orecchia ldquoGenotype characterisation ofGiardia duodenalis isolates from domestic and farm animals bySSU-rRNA gene sequencingrdquo Veterinary Parasitology vol 122no 3 pp 193ndash199 2004
[37] P Bianciardi R Papini G Giuliani andG Cardini ldquoPrevalenceof Giardia antigen in stool samples from dogs and catsrdquo Revuede Medecine Veterinaire vol 155 no 8-9 pp 417ndash421 2004
[38] G Capelli A Frangipane di Regalbono R Iorio M PietrobelliB Paoletti and A Giangaspero ldquoGiardia species and otherintestinal parasites in dogs in north-east and central ItalyrdquoVeterinary Record vol 159 no 13 pp 422ndash424 2006
[39] L Rinaldi M P Maurelli V Musella et al ldquoGiardia andCryptosporidium in canine faecal samples contaminating anurban areardquo Research in Veterinary Science vol 84 no 3 pp413ndash415 2008
[40] A V Scorza L R Ballweber S Tangtrongsup C Panuska andM R Lappin ldquoComparisons of mammalianGiardia duodenalisassemblages based on the 120573-giardin glutamate dehydrogenaseand triose phosphate isomerase genesrdquo Veterinary Parasitologyvol 189 no 2ndash4 pp 182ndash188 2012
[41] F D Uehlinger S J Greenwood J T McClure G B ConboyR OrsquoHandley and H W Barkema ldquoZoonotic potential ofGiardia duodenalis and Cryptosporidium spp and prevalenceof intestinal parasites in young dogs from different populationson Prince Edward Island Canadardquo Veterinary Parasitology vol196 no 3-4 pp 509ndash514 2013
[42] L R Ballweber L Xiao D D Bowman G Kahn and V ACama ldquoGiardiasis in dogs and cats update on epidemiology andpublic health significancerdquo Trends in Parasitology vol 26 no 4pp 180ndash189 2010
[43] D Jaros W Zygner S Jaros and HWedrychowicz ldquoDetectionof Giardia intestinalis assemblages A B and D in domestic catsfrom Warsaw Polandrdquo Polish Journal of Microbiology vol 60no 3 pp 259ndash263 2011
[44] R C AndersonNematode Parasites of Vertebrates Their Devel-opment and Transmission Cabi Publishing Wallingford UK2nd edition 2000
Submit your manuscripts athttpwwwhindawicom
Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014
Anatomy Research International
PeptidesInternational Journal of
Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014
Hindawi Publishing Corporation httpwwwhindawicom
International Journal of
Volume 2014
Zoology
Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014
Molecular Biology International
GenomicsInternational Journal of
Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014
The Scientific World JournalHindawi Publishing Corporation httpwwwhindawicom Volume 2014
Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014
BioinformaticsAdvances in
Marine BiologyJournal of
Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014
Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014
Signal TransductionJournal of
Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014
BioMed Research International
Evolutionary BiologyInternational Journal of
Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014
Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014
Biochemistry Research International
ArchaeaHindawi Publishing Corporationhttpwwwhindawicom Volume 2014
Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014
Genetics Research International
Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014
Advances in
Virolog y
Hindawi Publishing Corporationhttpwwwhindawicom
Nucleic AcidsJournal of
Volume 2014
Stem CellsInternational
Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014
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Enzyme Research
Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014
International Journal of
Microbiology
BioMed Research International 5
Table 2 Univariate analysis of risk factors for intestinal parasites in dogs and cats presenting at two veterinary practices in northern Italy
Variable Risk factor OR 95 CI 119875 valueDogs
HabitationMetropolitan 100 0006
Micropolitan area 1 3476 1632ndash7403 0001Micropolitan area 2 1947 0986ndash3845 0055
Age le12 months 100 NAgt12 months 0362 0205ndash0639 0000
Gender Male 100 NAFemales 0756 0433ndash1320 0325
SizeSmall 1 0917
Medium 0937 0451ndash1946 0861Large 1165 0439ndash3092 0760
Housing Household 1 NAOutdoor 0827 0364ndash1880 0651
Husbandry Single-dog-household 1 NAMultiple-dog-household 2059 1047ndash4051 0036
Cats
HabitationMetropolitan 100 0008
Micropolitan area 1 2100 0730ndash6039 0169Micropolitan area 2 3561 1601ndash7924 0002
Age le12 months 100 NAgt12 months 0347 0168ndash0716 0004
Gender Males 100 NAFemale 0809 0401ndash1631 0553
Housing Outdoorhousehold 1 NAHousehold 0526 0195ndash1424 0006
Husbandry Single-cat-household 1 NAMultiple-cat-household 1153 0437ndash3039 0774
OR odds ratio(CI) 95 confidence interval
Table 3 Final multivariate analysis of risks factors associated with intestinal parasites in dogs and cats presenting at two veterinary practicesin northern Italy
Variable Risk factor OR 95 CI 119875 valueDogs
Age gt12 months 100 NAle12 months 0445 0222ndash0894 0023
Husbandry Single-dog-household 1 NAMultiple-dog-household 2240 1115ndash4498 0023
Cats
HabitationMetropolitan area 100 0011Micropolitan area 1 2279 0762ndash6814 0141Micropolitan area 2 3510 1536ndash8020 0003
Age gt12 months 100 NAle12 months 0348 0163ndash0742 0006
OR odds ratio(CI) 95 confidence interval
6 BioMed Research InternationalTa
ble4Prevalence
()a
nd95CI
(minndashm
ax)o
fintestin
alparasites
indo
gsandcatsby
individu
alfeatures
andmanagem
ent
Parasites
Gender
Age
Hou
sing
Husband
ryMale
Female
le12
mon
ths
gt12
mon
ths
Hou
seho
ldOutdo
orSing
leMultip
leDogs
(119899=116)
(119899=92)
(119899=92)
(119899=116)
(119899=56)
(119899=84)
(119899=74)
(119899=66)
Toxocara
canis
1379
761
2065lowastlowast
345lowastlowast
1071
1667
1081
1818
(752ndash2007)
(219
ndash1303)
(1238ndash2892)
(013
ndash677)
(261ndash1881)
(870ndash
2464)
(374
ndash178
8)(888ndash2748)
Toxascarisleo
nina
086
109
109
086
0238
135
152
(0ndash254)
(0ndash321)
(0ndash321)
(0ndash254)
mdash(0ndash564)
(0ndash398)
(0ndash4
47)
Ancylostomatidae
345
326
326
345
179
595
0lowastlowast
909lowastlowast
(013
ndash677)
(0ndash6
89)
(0ndash6
89)
(013
ndash677)
(0ndash526)
(089ndash
1101)
mdash(215
ndash1603)
Trich
urisvulpis
517
870
326
948
536
952
270lowast
1364lowast
(114
ndash920)
(294ndash
1445)
(0ndash6
89)
(415
ndash1481)
(0ndash112
6)(324ndash
1580)
(0ndash6
39)
(536ndash
2192)
Eucoleu
saerophilus
010
90
086
00
00
mdash(0ndash321)
mdash(0ndash254)
mdashmdash
mdashmdash
Dipylidium
caninu
m17
2217
217
172
536
119
270
303
(0ndash4
09)
(0ndash515
)(0ndash515
)(0ndash4
09)
(0ndash112
6)(0ndash351)
(0ndash6
39)
(0ndash717
)
Cysto
isosporasp
345
543
870lowastlowast
086lowastlowast
1071lowast
238lowast
541
606
(013
ndash677)
(080ndash
1007)
(294ndash
1445)
(0ndash254)
(261ndash1881)
(0ndash564)
(026ndash
1056)
(030ndash
1182)
Giardiadu
odenalis
2155
1848
2717lowast
1466lowast
2679
2143
2297
2424
(1407ndash2903)
(1055ndash2641)
(1808ndash3626)
(822ndash2109)
(1519ndash3839)
(1265ndash3021)
(1339ndash3255)
(1390ndash3458)
Overallprevalence
4483
3804
5543lowastlowast
2931lowastlowast
5044
83
4054lowast
5758lowast
(3578ndash5388)
(2812ndash4
796)
(4528ndash6
559)
(210
3ndash3759)
(3690ndash6
315)
(2558ndash6
408)
(293
5ndash5173)
(4566ndash6
950)
Cats
(119899=62)
(119899=65)
(119899=61)
(119899=66)
(119899=38)
(119899=29)
(119899=31)
(119899=36)
Toxocara
cati
1290
1231
1967lowast
606lowast
2368
2069
1935
2500
(456ndash
2125)
(432
ndash2029)
(970ndash
2965)
(030ndash
1182)
(1016ndash372
0)(595ndash3543)
(544ndash
3326)
(1085ndash391
5)
Toxascarisleo
nina
323
615
984lowastlowast
0lowastlowast
263lowast
1724lowast
968
833
(0ndash762)
(031ndash1200)
(236ndash
1731)
mdash(0ndash772)
(349ndash
3099)
(0ndash2009)
(0ndash173
6)
Ancylostomatidae
161
016
40
263
00
278
(0ndash4
75)
mdash(0ndash4
83)
mdash(0ndash772)
mdashmdash
(0ndash815
)
Trich
urisvulpis
161
00
152
0345
0278
(0ndash4
75)
mdashmdash
(0ndash4
46)
mdash(0ndash1009)
mdash(0ndash815
)
Dipylidium
caninu
m323
154
0455
789
0323
556
(0ndash762)
(0ndash4
53)
(0ndash957)
(0ndash1646
)mdash
(0ndash945)
(0ndash1305)
Spiro
metra
sp
161
016
40
00
00
(0ndash4
75)
mdash(0ndash4
83)
mdashmdash
mdashmdash
mdash
Cysto
isosporasp
161
462
492
152
263
690
0833
(0ndash4
75)
(0ndash972)
(0ndash1034)
(0ndash4
46)
(0ndash772)
(0ndash1612)
mdash(0ndash173
6)
Toxoplasma-lik
e0
154
015
20
00
0mdash
(0ndash4
53)
mdash(0ndash4
46)
mdashmdash
mdashmdash
Giardiadu
odenalis
2903
2615
3279
2273
2368
3448
3548
2222
(177
3ndash40
33)
(1547ndash3684)
(210
1ndash44
57)
(1262ndash3284)
(1016ndash372
0)(1718ndash5178)
(1864
ndash5232)
(864ndash
3580)
Overallprevalence
4677
4154
5738lowastlowast
3182lowastlowast
506552
5484
5833
(3435ndash591
9)(295
6ndash5352
)(4497ndash6
979)
(2058ndash4
306)
(3410ndash6
590)
(4822ndash8282)
(3732ndash7236)
(4222ndash7444
)(C
I)95con
fidence
intervalof
thep
revalence
lowastlowast
Chi-S
quaretest119875valuelt
001
lowast
Chi-S
quaretest119875valuelt
005
BioMed Research International 7
Table 5 Frequency of pets (dogs or cats) infected or not infectedby intestinal parasites in northern Italy according to gastrointestinalsymptoms (presence or absence)
Infection No infection 119875 valuelowast
DogsSymptomatic 21 23 085Asymptomatic 48 48
CatSymptomatic 10 13 0128Asymptomatic 28 16
lowastFisherrsquos exact 119875 value
Table 6 Frequency of pets (dogs or cats) infected by intestinalparasites in northwestern Italy by features of their owners (number207)
Owner features Frequency of pets119875 valuelowast
Positive 119899 () Negative 119899 ()Gender
Female 75 (3694) 66 (3251) 024Male 29 (1428) 33 (1625)
Agele40 years old 65 (3202) 66 (3251) 031gt40 years old 39 (1921) 33 (1625)
Educationalqualification
Secondary schoolcertificate 38 (1871) 33 (1625) 037Intermediate schoolcertificateacademicdegree
66 (3251) 66 (3251)
Family componentsle2 42 (2058) 47 (2303) 020gt2 62 (3039) 53 (2598)
Presence of young lt15years old
Not 66 (3235) 68 (3333) 029Yes 38 (1862) 32 (1568)
lowastFisherrsquos exact 119875 value
Among the recovered helminthic species T canis and Tcati which accountedthe most frequent are consideredof great public health significance in their causing themost widespread and economically important zoonoses [30]Other parasites diffusing zoonoses ofminor importance werefound such as T vulpis Ancylostomatidae and Dypilid-ium canimum Finally molecular analysis on fecal samplesdemonstrated the presence of G duodenalis AssemblageA considered to have zoonotic potential [31] The overallprevalence of intestinal parasites both in dogs and in catsin northern Italy was higher than expected (119875 = 2816ndash5741 in dogs 119875 = 3258ndash6042 in cats) The currentlyreported prevalence rates of dog parasites are slightly differentconsidering the different origin of sampled dogs Particularlydogs from the large metropolitan area of Milan showed
lower prevalence than dogs from themicropolitan territoriesSeveral factors can justify these differences In fact most dogsfromMilan were rarely taken to large playgrounds limited intheir walks and regularly treated against heartworm diseaseFurther no colonies of stray dogs exist and proper disposalof dog waste from public soil is coming into common useamong urban pet owners On the other hand dogs frommicropolitan areas are usually at high risk of infection beingfrequently outdoors in their gardens or in large green areasIn addition transhumance being still practiced in Lombardythey might reasonably be infected by sheepdogs guardingtranshumant sheep flocks In fact they are moved fromAlpine pastures to lowlands twice yearly along the mainroutes (north to south) throughBergamo andBrescia towardsthe Po Plain areas whose fields may be contaminated by fecesof untreated sheepdog thus passing infection
In dogs as regards helminths only currently reportedprevalences significantly differ from what was previouslyobserved in Lombardy In 1974 in a coprological surveyconducted in some micropolitan areas located north andsouth of Milan helminths were recorded in 7579ndash853 ofexamined dogs [25] Further development in diagnosis andtreatment may account for the substantial differences foundwith our present survey together with a more widespreadprophylaxis against D immitis in the area of Milan whichmight have reasonably contributed to control canine intesti-nal parasites In 2007 helminth eggs were recovered in 7of dog feces collected from public places including parksof Milan [32] indicating a lower prevalence than in ourlatest survey (119875 = 141) This could be due to thekind of fecal samples collected from city soil that mainlyincluded droppings voided by old dogs typically showinglower infection values than young ones On the other handour findings are consistent with results from a recent surveyon pets from central Italy sampled in veterinary clinics wherehelminth infections were present in 241 of owned dogsand in 319 of owned cats [33] In the same year helminthinfections were recorded in 501 of stray cats from coloniespertaining to the metropolitan area of Milan [26]
Consistent with data obtained in several countriesascarids especially Toxocara spp were the most prevalentcanine and feline parasites [7 10 12ndash14 33 34] In contrastwith other surveys a low prevalence of Ancylostomatidaeinfection was recorded in our sampled dogs except thosefrom the micropolitan areas 1 and 2 A low presence ofhunting sporting or guard dogs in our samples as well asepidemiology and life cycle of Ancylostomatidae nematodescan account for this discrepancy [2 3 8 11 35]
As regardsG duodenalis it was themost prevalent canineand feline parasite according to other surveys [5 8ndash10 12]Such findings are not consistent with low prevalence valuesrecorded in the same species in other Italian studies whoseanalytical methods were different [32 36ndash39]
In this survey consistent with previous studies [31 40 41]G duodenalis assemblages C and D were isolated in dogsThey are considered host-adapted genotypes and a speciesname Giardia canis was proposed to label them As regardscats in our study the host-adapted F genotype was notfound however G duodenalis infections sustained also by
8 BioMed Research International
assemblages A B C and D have been previously describedin cats [40 42] In owned cats we observed a high prevalenceof G duodenalis infection by assemblage A whose possiblezoonotic potential must not be underestimated [31] FinallyG duodenalis assemblage D was recovered less frequentlythough [42 43]
Risk factors for dogs frommetropolitan andmicropolitanareas were being younger than 12 months or sharing thesame house with other dogs Compared to dogs from thelarge metropolitan area of Milan the odds for dogs from themicropolitan area 1 were 3476 times higher and the oddsfor dogs from MC 2 were 1947 times higher but with lowersignificance (119875 = 0001 versus 119875 = 0055) Further comparedto dogs le12 months old the odds of a dog gt12 months beingparasitized were 0362 times smaller Compared to single-household dogs the odds for multiple- household dogs were2059 times higher which means that cohabitation is oneof the most important risk factors associated to endopara-sitism In accordance with Katagiri andOliveira-Sequeira [2]who also found higher prevalence in multihousehold dogssignificant differences were found for Ancylostomatidae andT vulpis infections It might be that in the presence ofmultiple pets environmental contamination with infectivestages of these taxa occurs dogs become more susceptible toinfections and environmental contamination itself is higherand better maintained In cats the presence of endoparasiteswas associated only with their age housing and with the areathey lived in These findings are consistent with other studiesconsidering parasitism as of primarily concern for youngerdogs or cats [4 5 7 14] According to the univariate analysisthe overall prevalence of intestinal parasites in household catsshows statistically significant differences with cats that livedoutsidewith access to a garden (119875 = 50 in household versus119875 = 6552 in outdoor) Living outdoors or having accessto a garden seems to be a risk factor for T leonina infectionin cats as similarly described by Nareaho et al [15] It couldbe partially due to the source of infection for this parasitethat in addition to larvated eggs is represented by paratenichosts that harbour somatic third-stage larvae [44] As aconsequence of their predatory behavior domestic felinescould bemore susceptible to infections due to paratenic hostswhen they have outdoor access
Dogs and cats presenting gastrointestinal signs showed aprevalence of intestinal parasites close to 45 which urgesto differential diagnosis and periodic coprological exami-nation Prophylaxis against D immitis showed ineffectivein protecting dogs against gastrointestinal nematodes Forthem registered dosage of macrocyclic lactones used againstheartworms must be too low and seasonal administration ofthe treatment to all sampled adults dogs proved insufficientto cover their exposition to other risk factors all over theyear The answers to our questionnaire specifically designedto understand ownerrsquos awareness and information aboutcanine and feline gastrointestinal parasites showed thatthey knew but few aspects of the parasite biology In factmore than 7189 of them indicated that fecal contamina-tion can cause gastrointestinal parasite infection and thusthey were probably aware of the importance of reducingenvironmental fecal voiding Nonetheless 3910 of them
gave a negative answer or no answer at all As to possiblelasting environmental contamination due to infected petfecalization 5622 of total owners were not aware of it andmost of them probably did not consider preventing contactwith intermediateparatenic hosts as a possible prophylaxisagainst intestinal parasites infections A higher number ofowners (4811) correctly answered affirmatively when askedabout the possibility of transmission of intestinal parasitesto puppieskittens by infective milk of bitchesqueens Theymay be more stressed by clinicians on the importance ofintestinal parasite infections in puppies and kittens than inadult dogs and cats Concerning their awareness of risks forhuman health from canine and feline intestinal parasites5081 declared that intestinal parasites of dogs and cats donot represent any kind of risk for human health or that theydid not know about the issue Further 2637 out of 90owners informed about human health risks stated that theycould not name possible diseases thus confirming that theydid not know what proper behavior is necessary to reducezoonotic risks
Overall these results indicated that owners needed moreand clear information about zoonotic potential of intestinalparasites and that the veterinarians can be of extremeimportance in this process
5 Conclusion
Results of this survey showed that intestinal parasites are stilla common finding in owned dogs and cats not to be underes-timated in both metropolitan and micropolitan areas even ifthe latter indicated higher pet infection prevalence Furtherwhen a dog or a cat is presented to clinical examination onaccount of gastrointestinal signs intestinal parasite infectionshould be considered as a possible differential diagnosisThis condition can be asymptomatic and can even affectanimals under proper prophylaxis against D immitis thuseven apparently fit and healthy pets should be submitted toannual or biannual fecal examination Clinicians should alsoconsider that younger patients that live in micropolitan areasare the most susceptible to parasite infections The zoonoticparasites T canis and T cati T vulpis Ancylostomatidae andG duodenalis assemblage A resulted to be the most commonspecies in owned pets In any case veterinaries clearly play akey role in increasing awareness and knowledge of pet ownersabout canine and feline gastrointestinal parasites as to theirinfection routes proper monitoring and correct behavior toavoid potential zoonotic risks
Conflict of Interests
The authors declare that there is no conflict of interestsregarding the publication of this paper
References
[1] A C Y Lee PM Schantz K R Kazacos S PMontgomery andD D Bowman ldquoEpidemiologic and zoonotic aspects of ascaridinfections in dogs and catsrdquo Trends in Parasitology vol 26 no4 pp 155ndash161 2010
BioMed Research International 9
[2] S Katagiri and T C G Oliveira-Sequeira ldquoPrevalence of dogintestinal parasites and risk perception of zoonotic infectionby dog owners in Sao Paulo State Brazilrdquo Zoonoses and PublicHealth vol 55 no 8ndash10 pp 406ndash413 2008
[3] S E Little E M Johnson D Lewis et al ldquoPrevalence ofintestinal parasites in pet dogs in the United Statesrdquo VeterinaryParasitology vol 166 no 1-2 pp 144ndash152 2009
[4] D Barutzki andR Schaper ldquoResults of parasitological examina-tions of faecal samples from cats and dogs in Germany between2003 and 2010rdquo Parasitology Research vol 109 no 1 pp S45ndashS60 2011
[5] N Itoh H Ikegami M Takagi et al ldquoPrevalence of intestinalparasites in private-household cats in Japanrdquo Journal of FelineMedical Surgery vol 14 no 6 pp 436ndash439 2012
[6] M C Gates and T J Nolan ldquoEfficacy of heartworm pre-ventatives against ascarids and hookworms in client-owneddogs a retrospective case control studyrdquo Journal of VeterinaryPharmacology andTherapeutics vol 34 no 2 pp 116ndash119 2011
[7] M C Gates and T J Nolan ldquoEndoparasite prevalence andrecurrence across different age groups of dogs and catsrdquoVeterinary Parasitology vol 166 no 1-2 pp 153ndash158 2009
[8] F S Ferreira P Pereira-Baltasar R Parreira et al ldquoIntestinalparasites in dogs and cats from the district of Evora PortugalrdquoVeterinary Parasitology vol 179 no 1ndash3 pp 242ndash245 2011
[9] C Epe G Rehkter T Schnieder L Lorentzen and L Kreien-brock ldquoGiardia in symptomatic dogs and cats in Europe-Resultsof a European studyrdquo Veterinary Parasitology vol 173 no 1-2pp 32ndash38 2010
[10] D Joffe D van Niekerk F Gagne J Gilleard S Kutz and RLobingier ldquoThe prevalence of intestinal parasites in dogs andcats in Calgary ABrdquo Canadian Veterinary Journal vol 52 no12 pp 1323ndash1328 2011
[11] T M Savilla J E Joy J D May and C C SomervilleldquoPrevalence of dog intestinal nematode parasites in southcentral West Virginia USArdquo Veterinary Parasitology vol 178no 1-2 pp 115ndash120 2011
[12] E Claerebout S Casaert A-C Dalemans et al ldquoGiardiaand other intestinal parasites in different dog populations inNorthern BelgiumrdquoVeterinary Parasitology vol 161 no 1-2 pp41ndash46 2009
[13] P A M Overgaauw L van Zutphen D Hoek et al ldquoZoonoticparasites in fecal samples and fur from dogs and cats in TheNetherlandsrdquo Veterinary Parasitology vol 163 no 1-2 pp 115ndash122 2009
[14] M C Gates and T J Nolan ldquoRisk factors for endoparasitismin dogs retrospective case-control study of 6578 veterinaryteaching hospital casesrdquo Journal of Small Animal Practice vol50 no 12 pp 636ndash640 2009
[15] A Nareaho J Puomio K Saarinen P Jokelainen T Juseliusand A Sukura ldquoFeline intestinal parasites in Finland preva-lence risk factors and anthelmintic treatment practicesrdquo Journalof Feline Medicine and Surgery vol 14 no 6 pp 378ndash383 2012
[16] L Polley and R C A Thompson ldquoParasite zoonoses and cli-mate change molecular tools for tracking shifting boundariesrdquoTrends in Parasitology vol 25 no 6 pp 285ndash291 2009
[17] E J Jenkins J M Schurer and K M Gesy ldquoOld problems on anew playing field helminth zoonoses transmitted among dogswildlife and people in a changing northern climaterdquoVeterinaryParasitology vol 182 no 1 pp 54ndash69 2011
[18] P N Acha and B Szyfres Zoonoses et Maladies TransmissiblesCommunes a lrsquohomme et Aux animaux Office International desEpizooties Paris France 1989
[19] M Fisher ldquoToxocara cati an underestimated zoonotic agentrdquoTrends in Parasitology vol 19 no 4 pp 167ndash170 2003
[20] Y Masuda T Kishimoto H Ito and M Tsuji ldquoVisceral larvamigrans caused by Trichuris vulpis presenting as a pulmonarymassrdquoThorax vol 42 no 12 pp 990ndash991 1987
[21] J J Dunn S T Columbus W E Aldeen M Davis and K CCarroll ldquoTrichuris vulpis recovered from a patient with chronicdiarrhea and five dogsrdquo Journal of Clinical Microbiology vol 40no 7 pp 2703ndash2704 2002
[22] M Papazahariadou A Founta E Papadopoulos SChliounakis K Antoniadou-Sotiriadou and Y TheodoridesldquoGastrointestinal parasites of shepherd and hunting dogs in theSerres Prefecture Northern Greecerdquo Veterinary Parasitologyvol 148 no 2 pp 170ndash173 2007
[23] C Martınez-Carrasco E Berriatua M Garijo J Martınez FD Alonso and R Ruiz De Ybanez ldquoEpidemiological study ofnon-systemic parasitism in dogs in southeast MediterraneanSpain assessed by coprological and post-mortem examinationrdquoZoonoses and Public Health vol 54 no 5 pp 195ndash203 2007
[24] S Leonhard K Pfister P Beelitz C Wielinga and R C AThompson ldquoThe molecular characterisation of Giardia fromdogs in southern Germanyrdquo Veterinary Parasitology vol 150no 1-2 pp 33ndash38 2007
[25] C Genchi G Gili and R Maraschin ldquoIndagine sullrsquoincidenzadelle elmintiasi intestinali del cane in alcune zone della Lom-bardiardquo La Clinica Veterinaria vol 97 no 6 pp 178ndash186 1974
[26] E Spada D Proverbio A Della Pepa et al ldquoPrevalence offaecal-borne parasites in colony stray cats in northern ItalyrdquoJournal of Feline Medicine and Surgery vol 15 no 8 pp 672ndash677 2013
[27] R M Hopkins B P Meloni D M Groth J D WetherallJ A Reynoldson and R C A Thompson ldquoRibosomal RNAsequencing reveals differences between the genotypes of Giar-dia isolates recovered from humans and dogs living in the samelocalityrdquo Journal of Parasitology vol 83 no 1 pp 44ndash51 1997
[28] C Read J Walters I D Robertson and R C A ThompsonldquoCorrelation between genotype of Giardia duodenalis anddiarrhoeardquo International Journal for Parasitology vol 32 no 2pp 229ndash231 2002
[29] A O Bush K D Lafferty J M Lotz and A W ShostakldquoParasitology meets ecology on its own terms Margolis et alrevisitedrdquo Journal of Parasitology vol 83 no 4 pp 575ndash5831997
[30] C N L Macpherson ldquoThe epidemiology and public healthimportance of toxocariasis a zoonosis of global importancerdquoInternational Journal for Parasitology vol 43 pp 999ndash10082013
[31] U Ryan and S M Caccio ldquoZoonotic potential of GiardiardquoInternational Journal For Parasitology vol 43 pp 943ndash9562013
[32] M Genchi E Ferroglio G Traldi S Passera G MezzanoandCGenchi ldquoFecalizzazione ambientale e rischio parassitarionelle citta di Milano e Torinordquo Professione Veterinaria vol 41pp 15ndash17 2007
[33] F Riggio R Mannella G Ariti and S Perrucci ldquoIntestinaland lung parasites in owned dogs and cats from central ItalyrdquoVeterinary Parasitology vol 193 no 1ndash3 pp 78ndash84 2013
[34] LMugnaini R Papini G Gorini A Passantino VMerildi andF Mancianti ldquoPattern and predictive factors of endoparasitismin cats in central Italyrdquo Revue de Medecine Veterinaire vol 163no 2 pp 85ndash88 2012
10 BioMed Research International
[35] D Traversa ldquoPet roundworms and hookworms a continuingneed for global wormingrdquo Parasite amp Vectors vol 5 no 1 p 912012
[36] F Berrilli D di Cave C de Liberato A Franco PScaramozzino and P Orecchia ldquoGenotype characterisation ofGiardia duodenalis isolates from domestic and farm animals bySSU-rRNA gene sequencingrdquo Veterinary Parasitology vol 122no 3 pp 193ndash199 2004
[37] P Bianciardi R Papini G Giuliani andG Cardini ldquoPrevalenceof Giardia antigen in stool samples from dogs and catsrdquo Revuede Medecine Veterinaire vol 155 no 8-9 pp 417ndash421 2004
[38] G Capelli A Frangipane di Regalbono R Iorio M PietrobelliB Paoletti and A Giangaspero ldquoGiardia species and otherintestinal parasites in dogs in north-east and central ItalyrdquoVeterinary Record vol 159 no 13 pp 422ndash424 2006
[39] L Rinaldi M P Maurelli V Musella et al ldquoGiardia andCryptosporidium in canine faecal samples contaminating anurban areardquo Research in Veterinary Science vol 84 no 3 pp413ndash415 2008
[40] A V Scorza L R Ballweber S Tangtrongsup C Panuska andM R Lappin ldquoComparisons of mammalianGiardia duodenalisassemblages based on the 120573-giardin glutamate dehydrogenaseand triose phosphate isomerase genesrdquo Veterinary Parasitologyvol 189 no 2ndash4 pp 182ndash188 2012
[41] F D Uehlinger S J Greenwood J T McClure G B ConboyR OrsquoHandley and H W Barkema ldquoZoonotic potential ofGiardia duodenalis and Cryptosporidium spp and prevalenceof intestinal parasites in young dogs from different populationson Prince Edward Island Canadardquo Veterinary Parasitology vol196 no 3-4 pp 509ndash514 2013
[42] L R Ballweber L Xiao D D Bowman G Kahn and V ACama ldquoGiardiasis in dogs and cats update on epidemiology andpublic health significancerdquo Trends in Parasitology vol 26 no 4pp 180ndash189 2010
[43] D Jaros W Zygner S Jaros and HWedrychowicz ldquoDetectionof Giardia intestinalis assemblages A B and D in domestic catsfrom Warsaw Polandrdquo Polish Journal of Microbiology vol 60no 3 pp 259ndash263 2011
[44] R C AndersonNematode Parasites of Vertebrates Their Devel-opment and Transmission Cabi Publishing Wallingford UK2nd edition 2000
Submit your manuscripts athttpwwwhindawicom
Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014
Anatomy Research International
PeptidesInternational Journal of
Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014
Hindawi Publishing Corporation httpwwwhindawicom
International Journal of
Volume 2014
Zoology
Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014
Molecular Biology International
GenomicsInternational Journal of
Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014
The Scientific World JournalHindawi Publishing Corporation httpwwwhindawicom Volume 2014
Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014
BioinformaticsAdvances in
Marine BiologyJournal of
Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014
Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014
Signal TransductionJournal of
Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014
BioMed Research International
Evolutionary BiologyInternational Journal of
Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014
Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014
Biochemistry Research International
ArchaeaHindawi Publishing Corporationhttpwwwhindawicom Volume 2014
Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014
Genetics Research International
Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014
Advances in
Virolog y
Hindawi Publishing Corporationhttpwwwhindawicom
Nucleic AcidsJournal of
Volume 2014
Stem CellsInternational
Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014
Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014
Enzyme Research
Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014
International Journal of
Microbiology
6 BioMed Research InternationalTa
ble4Prevalence
()a
nd95CI
(minndashm
ax)o
fintestin
alparasites
indo
gsandcatsby
individu
alfeatures
andmanagem
ent
Parasites
Gender
Age
Hou
sing
Husband
ryMale
Female
le12
mon
ths
gt12
mon
ths
Hou
seho
ldOutdo
orSing
leMultip
leDogs
(119899=116)
(119899=92)
(119899=92)
(119899=116)
(119899=56)
(119899=84)
(119899=74)
(119899=66)
Toxocara
canis
1379
761
2065lowastlowast
345lowastlowast
1071
1667
1081
1818
(752ndash2007)
(219
ndash1303)
(1238ndash2892)
(013
ndash677)
(261ndash1881)
(870ndash
2464)
(374
ndash178
8)(888ndash2748)
Toxascarisleo
nina
086
109
109
086
0238
135
152
(0ndash254)
(0ndash321)
(0ndash321)
(0ndash254)
mdash(0ndash564)
(0ndash398)
(0ndash4
47)
Ancylostomatidae
345
326
326
345
179
595
0lowastlowast
909lowastlowast
(013
ndash677)
(0ndash6
89)
(0ndash6
89)
(013
ndash677)
(0ndash526)
(089ndash
1101)
mdash(215
ndash1603)
Trich
urisvulpis
517
870
326
948
536
952
270lowast
1364lowast
(114
ndash920)
(294ndash
1445)
(0ndash6
89)
(415
ndash1481)
(0ndash112
6)(324ndash
1580)
(0ndash6
39)
(536ndash
2192)
Eucoleu
saerophilus
010
90
086
00
00
mdash(0ndash321)
mdash(0ndash254)
mdashmdash
mdashmdash
Dipylidium
caninu
m17
2217
217
172
536
119
270
303
(0ndash4
09)
(0ndash515
)(0ndash515
)(0ndash4
09)
(0ndash112
6)(0ndash351)
(0ndash6
39)
(0ndash717
)
Cysto
isosporasp
345
543
870lowastlowast
086lowastlowast
1071lowast
238lowast
541
606
(013
ndash677)
(080ndash
1007)
(294ndash
1445)
(0ndash254)
(261ndash1881)
(0ndash564)
(026ndash
1056)
(030ndash
1182)
Giardiadu
odenalis
2155
1848
2717lowast
1466lowast
2679
2143
2297
2424
(1407ndash2903)
(1055ndash2641)
(1808ndash3626)
(822ndash2109)
(1519ndash3839)
(1265ndash3021)
(1339ndash3255)
(1390ndash3458)
Overallprevalence
4483
3804
5543lowastlowast
2931lowastlowast
5044
83
4054lowast
5758lowast
(3578ndash5388)
(2812ndash4
796)
(4528ndash6
559)
(210
3ndash3759)
(3690ndash6
315)
(2558ndash6
408)
(293
5ndash5173)
(4566ndash6
950)
Cats
(119899=62)
(119899=65)
(119899=61)
(119899=66)
(119899=38)
(119899=29)
(119899=31)
(119899=36)
Toxocara
cati
1290
1231
1967lowast
606lowast
2368
2069
1935
2500
(456ndash
2125)
(432
ndash2029)
(970ndash
2965)
(030ndash
1182)
(1016ndash372
0)(595ndash3543)
(544ndash
3326)
(1085ndash391
5)
Toxascarisleo
nina
323
615
984lowastlowast
0lowastlowast
263lowast
1724lowast
968
833
(0ndash762)
(031ndash1200)
(236ndash
1731)
mdash(0ndash772)
(349ndash
3099)
(0ndash2009)
(0ndash173
6)
Ancylostomatidae
161
016
40
263
00
278
(0ndash4
75)
mdash(0ndash4
83)
mdash(0ndash772)
mdashmdash
(0ndash815
)
Trich
urisvulpis
161
00
152
0345
0278
(0ndash4
75)
mdashmdash
(0ndash4
46)
mdash(0ndash1009)
mdash(0ndash815
)
Dipylidium
caninu
m323
154
0455
789
0323
556
(0ndash762)
(0ndash4
53)
(0ndash957)
(0ndash1646
)mdash
(0ndash945)
(0ndash1305)
Spiro
metra
sp
161
016
40
00
00
(0ndash4
75)
mdash(0ndash4
83)
mdashmdash
mdashmdash
mdash
Cysto
isosporasp
161
462
492
152
263
690
0833
(0ndash4
75)
(0ndash972)
(0ndash1034)
(0ndash4
46)
(0ndash772)
(0ndash1612)
mdash(0ndash173
6)
Toxoplasma-lik
e0
154
015
20
00
0mdash
(0ndash4
53)
mdash(0ndash4
46)
mdashmdash
mdashmdash
Giardiadu
odenalis
2903
2615
3279
2273
2368
3448
3548
2222
(177
3ndash40
33)
(1547ndash3684)
(210
1ndash44
57)
(1262ndash3284)
(1016ndash372
0)(1718ndash5178)
(1864
ndash5232)
(864ndash
3580)
Overallprevalence
4677
4154
5738lowastlowast
3182lowastlowast
506552
5484
5833
(3435ndash591
9)(295
6ndash5352
)(4497ndash6
979)
(2058ndash4
306)
(3410ndash6
590)
(4822ndash8282)
(3732ndash7236)
(4222ndash7444
)(C
I)95con
fidence
intervalof
thep
revalence
lowastlowast
Chi-S
quaretest119875valuelt
001
lowast
Chi-S
quaretest119875valuelt
005
BioMed Research International 7
Table 5 Frequency of pets (dogs or cats) infected or not infectedby intestinal parasites in northern Italy according to gastrointestinalsymptoms (presence or absence)
Infection No infection 119875 valuelowast
DogsSymptomatic 21 23 085Asymptomatic 48 48
CatSymptomatic 10 13 0128Asymptomatic 28 16
lowastFisherrsquos exact 119875 value
Table 6 Frequency of pets (dogs or cats) infected by intestinalparasites in northwestern Italy by features of their owners (number207)
Owner features Frequency of pets119875 valuelowast
Positive 119899 () Negative 119899 ()Gender
Female 75 (3694) 66 (3251) 024Male 29 (1428) 33 (1625)
Agele40 years old 65 (3202) 66 (3251) 031gt40 years old 39 (1921) 33 (1625)
Educationalqualification
Secondary schoolcertificate 38 (1871) 33 (1625) 037Intermediate schoolcertificateacademicdegree
66 (3251) 66 (3251)
Family componentsle2 42 (2058) 47 (2303) 020gt2 62 (3039) 53 (2598)
Presence of young lt15years old
Not 66 (3235) 68 (3333) 029Yes 38 (1862) 32 (1568)
lowastFisherrsquos exact 119875 value
Among the recovered helminthic species T canis and Tcati which accountedthe most frequent are consideredof great public health significance in their causing themost widespread and economically important zoonoses [30]Other parasites diffusing zoonoses ofminor importance werefound such as T vulpis Ancylostomatidae and Dypilid-ium canimum Finally molecular analysis on fecal samplesdemonstrated the presence of G duodenalis AssemblageA considered to have zoonotic potential [31] The overallprevalence of intestinal parasites both in dogs and in catsin northern Italy was higher than expected (119875 = 2816ndash5741 in dogs 119875 = 3258ndash6042 in cats) The currentlyreported prevalence rates of dog parasites are slightly differentconsidering the different origin of sampled dogs Particularlydogs from the large metropolitan area of Milan showed
lower prevalence than dogs from themicropolitan territoriesSeveral factors can justify these differences In fact most dogsfromMilan were rarely taken to large playgrounds limited intheir walks and regularly treated against heartworm diseaseFurther no colonies of stray dogs exist and proper disposalof dog waste from public soil is coming into common useamong urban pet owners On the other hand dogs frommicropolitan areas are usually at high risk of infection beingfrequently outdoors in their gardens or in large green areasIn addition transhumance being still practiced in Lombardythey might reasonably be infected by sheepdogs guardingtranshumant sheep flocks In fact they are moved fromAlpine pastures to lowlands twice yearly along the mainroutes (north to south) throughBergamo andBrescia towardsthe Po Plain areas whose fields may be contaminated by fecesof untreated sheepdog thus passing infection
In dogs as regards helminths only currently reportedprevalences significantly differ from what was previouslyobserved in Lombardy In 1974 in a coprological surveyconducted in some micropolitan areas located north andsouth of Milan helminths were recorded in 7579ndash853 ofexamined dogs [25] Further development in diagnosis andtreatment may account for the substantial differences foundwith our present survey together with a more widespreadprophylaxis against D immitis in the area of Milan whichmight have reasonably contributed to control canine intesti-nal parasites In 2007 helminth eggs were recovered in 7of dog feces collected from public places including parksof Milan [32] indicating a lower prevalence than in ourlatest survey (119875 = 141) This could be due to thekind of fecal samples collected from city soil that mainlyincluded droppings voided by old dogs typically showinglower infection values than young ones On the other handour findings are consistent with results from a recent surveyon pets from central Italy sampled in veterinary clinics wherehelminth infections were present in 241 of owned dogsand in 319 of owned cats [33] In the same year helminthinfections were recorded in 501 of stray cats from coloniespertaining to the metropolitan area of Milan [26]
Consistent with data obtained in several countriesascarids especially Toxocara spp were the most prevalentcanine and feline parasites [7 10 12ndash14 33 34] In contrastwith other surveys a low prevalence of Ancylostomatidaeinfection was recorded in our sampled dogs except thosefrom the micropolitan areas 1 and 2 A low presence ofhunting sporting or guard dogs in our samples as well asepidemiology and life cycle of Ancylostomatidae nematodescan account for this discrepancy [2 3 8 11 35]
As regardsG duodenalis it was themost prevalent canineand feline parasite according to other surveys [5 8ndash10 12]Such findings are not consistent with low prevalence valuesrecorded in the same species in other Italian studies whoseanalytical methods were different [32 36ndash39]
In this survey consistent with previous studies [31 40 41]G duodenalis assemblages C and D were isolated in dogsThey are considered host-adapted genotypes and a speciesname Giardia canis was proposed to label them As regardscats in our study the host-adapted F genotype was notfound however G duodenalis infections sustained also by
8 BioMed Research International
assemblages A B C and D have been previously describedin cats [40 42] In owned cats we observed a high prevalenceof G duodenalis infection by assemblage A whose possiblezoonotic potential must not be underestimated [31] FinallyG duodenalis assemblage D was recovered less frequentlythough [42 43]
Risk factors for dogs frommetropolitan andmicropolitanareas were being younger than 12 months or sharing thesame house with other dogs Compared to dogs from thelarge metropolitan area of Milan the odds for dogs from themicropolitan area 1 were 3476 times higher and the oddsfor dogs from MC 2 were 1947 times higher but with lowersignificance (119875 = 0001 versus 119875 = 0055) Further comparedto dogs le12 months old the odds of a dog gt12 months beingparasitized were 0362 times smaller Compared to single-household dogs the odds for multiple- household dogs were2059 times higher which means that cohabitation is oneof the most important risk factors associated to endopara-sitism In accordance with Katagiri andOliveira-Sequeira [2]who also found higher prevalence in multihousehold dogssignificant differences were found for Ancylostomatidae andT vulpis infections It might be that in the presence ofmultiple pets environmental contamination with infectivestages of these taxa occurs dogs become more susceptible toinfections and environmental contamination itself is higherand better maintained In cats the presence of endoparasiteswas associated only with their age housing and with the areathey lived in These findings are consistent with other studiesconsidering parasitism as of primarily concern for youngerdogs or cats [4 5 7 14] According to the univariate analysisthe overall prevalence of intestinal parasites in household catsshows statistically significant differences with cats that livedoutsidewith access to a garden (119875 = 50 in household versus119875 = 6552 in outdoor) Living outdoors or having accessto a garden seems to be a risk factor for T leonina infectionin cats as similarly described by Nareaho et al [15] It couldbe partially due to the source of infection for this parasitethat in addition to larvated eggs is represented by paratenichosts that harbour somatic third-stage larvae [44] As aconsequence of their predatory behavior domestic felinescould bemore susceptible to infections due to paratenic hostswhen they have outdoor access
Dogs and cats presenting gastrointestinal signs showed aprevalence of intestinal parasites close to 45 which urgesto differential diagnosis and periodic coprological exami-nation Prophylaxis against D immitis showed ineffectivein protecting dogs against gastrointestinal nematodes Forthem registered dosage of macrocyclic lactones used againstheartworms must be too low and seasonal administration ofthe treatment to all sampled adults dogs proved insufficientto cover their exposition to other risk factors all over theyear The answers to our questionnaire specifically designedto understand ownerrsquos awareness and information aboutcanine and feline gastrointestinal parasites showed thatthey knew but few aspects of the parasite biology In factmore than 7189 of them indicated that fecal contamina-tion can cause gastrointestinal parasite infection and thusthey were probably aware of the importance of reducingenvironmental fecal voiding Nonetheless 3910 of them
gave a negative answer or no answer at all As to possiblelasting environmental contamination due to infected petfecalization 5622 of total owners were not aware of it andmost of them probably did not consider preventing contactwith intermediateparatenic hosts as a possible prophylaxisagainst intestinal parasites infections A higher number ofowners (4811) correctly answered affirmatively when askedabout the possibility of transmission of intestinal parasitesto puppieskittens by infective milk of bitchesqueens Theymay be more stressed by clinicians on the importance ofintestinal parasite infections in puppies and kittens than inadult dogs and cats Concerning their awareness of risks forhuman health from canine and feline intestinal parasites5081 declared that intestinal parasites of dogs and cats donot represent any kind of risk for human health or that theydid not know about the issue Further 2637 out of 90owners informed about human health risks stated that theycould not name possible diseases thus confirming that theydid not know what proper behavior is necessary to reducezoonotic risks
Overall these results indicated that owners needed moreand clear information about zoonotic potential of intestinalparasites and that the veterinarians can be of extremeimportance in this process
5 Conclusion
Results of this survey showed that intestinal parasites are stilla common finding in owned dogs and cats not to be underes-timated in both metropolitan and micropolitan areas even ifthe latter indicated higher pet infection prevalence Furtherwhen a dog or a cat is presented to clinical examination onaccount of gastrointestinal signs intestinal parasite infectionshould be considered as a possible differential diagnosisThis condition can be asymptomatic and can even affectanimals under proper prophylaxis against D immitis thuseven apparently fit and healthy pets should be submitted toannual or biannual fecal examination Clinicians should alsoconsider that younger patients that live in micropolitan areasare the most susceptible to parasite infections The zoonoticparasites T canis and T cati T vulpis Ancylostomatidae andG duodenalis assemblage A resulted to be the most commonspecies in owned pets In any case veterinaries clearly play akey role in increasing awareness and knowledge of pet ownersabout canine and feline gastrointestinal parasites as to theirinfection routes proper monitoring and correct behavior toavoid potential zoonotic risks
Conflict of Interests
The authors declare that there is no conflict of interestsregarding the publication of this paper
References
[1] A C Y Lee PM Schantz K R Kazacos S PMontgomery andD D Bowman ldquoEpidemiologic and zoonotic aspects of ascaridinfections in dogs and catsrdquo Trends in Parasitology vol 26 no4 pp 155ndash161 2010
BioMed Research International 9
[2] S Katagiri and T C G Oliveira-Sequeira ldquoPrevalence of dogintestinal parasites and risk perception of zoonotic infectionby dog owners in Sao Paulo State Brazilrdquo Zoonoses and PublicHealth vol 55 no 8ndash10 pp 406ndash413 2008
[3] S E Little E M Johnson D Lewis et al ldquoPrevalence ofintestinal parasites in pet dogs in the United Statesrdquo VeterinaryParasitology vol 166 no 1-2 pp 144ndash152 2009
[4] D Barutzki andR Schaper ldquoResults of parasitological examina-tions of faecal samples from cats and dogs in Germany between2003 and 2010rdquo Parasitology Research vol 109 no 1 pp S45ndashS60 2011
[5] N Itoh H Ikegami M Takagi et al ldquoPrevalence of intestinalparasites in private-household cats in Japanrdquo Journal of FelineMedical Surgery vol 14 no 6 pp 436ndash439 2012
[6] M C Gates and T J Nolan ldquoEfficacy of heartworm pre-ventatives against ascarids and hookworms in client-owneddogs a retrospective case control studyrdquo Journal of VeterinaryPharmacology andTherapeutics vol 34 no 2 pp 116ndash119 2011
[7] M C Gates and T J Nolan ldquoEndoparasite prevalence andrecurrence across different age groups of dogs and catsrdquoVeterinary Parasitology vol 166 no 1-2 pp 153ndash158 2009
[8] F S Ferreira P Pereira-Baltasar R Parreira et al ldquoIntestinalparasites in dogs and cats from the district of Evora PortugalrdquoVeterinary Parasitology vol 179 no 1ndash3 pp 242ndash245 2011
[9] C Epe G Rehkter T Schnieder L Lorentzen and L Kreien-brock ldquoGiardia in symptomatic dogs and cats in Europe-Resultsof a European studyrdquo Veterinary Parasitology vol 173 no 1-2pp 32ndash38 2010
[10] D Joffe D van Niekerk F Gagne J Gilleard S Kutz and RLobingier ldquoThe prevalence of intestinal parasites in dogs andcats in Calgary ABrdquo Canadian Veterinary Journal vol 52 no12 pp 1323ndash1328 2011
[11] T M Savilla J E Joy J D May and C C SomervilleldquoPrevalence of dog intestinal nematode parasites in southcentral West Virginia USArdquo Veterinary Parasitology vol 178no 1-2 pp 115ndash120 2011
[12] E Claerebout S Casaert A-C Dalemans et al ldquoGiardiaand other intestinal parasites in different dog populations inNorthern BelgiumrdquoVeterinary Parasitology vol 161 no 1-2 pp41ndash46 2009
[13] P A M Overgaauw L van Zutphen D Hoek et al ldquoZoonoticparasites in fecal samples and fur from dogs and cats in TheNetherlandsrdquo Veterinary Parasitology vol 163 no 1-2 pp 115ndash122 2009
[14] M C Gates and T J Nolan ldquoRisk factors for endoparasitismin dogs retrospective case-control study of 6578 veterinaryteaching hospital casesrdquo Journal of Small Animal Practice vol50 no 12 pp 636ndash640 2009
[15] A Nareaho J Puomio K Saarinen P Jokelainen T Juseliusand A Sukura ldquoFeline intestinal parasites in Finland preva-lence risk factors and anthelmintic treatment practicesrdquo Journalof Feline Medicine and Surgery vol 14 no 6 pp 378ndash383 2012
[16] L Polley and R C A Thompson ldquoParasite zoonoses and cli-mate change molecular tools for tracking shifting boundariesrdquoTrends in Parasitology vol 25 no 6 pp 285ndash291 2009
[17] E J Jenkins J M Schurer and K M Gesy ldquoOld problems on anew playing field helminth zoonoses transmitted among dogswildlife and people in a changing northern climaterdquoVeterinaryParasitology vol 182 no 1 pp 54ndash69 2011
[18] P N Acha and B Szyfres Zoonoses et Maladies TransmissiblesCommunes a lrsquohomme et Aux animaux Office International desEpizooties Paris France 1989
[19] M Fisher ldquoToxocara cati an underestimated zoonotic agentrdquoTrends in Parasitology vol 19 no 4 pp 167ndash170 2003
[20] Y Masuda T Kishimoto H Ito and M Tsuji ldquoVisceral larvamigrans caused by Trichuris vulpis presenting as a pulmonarymassrdquoThorax vol 42 no 12 pp 990ndash991 1987
[21] J J Dunn S T Columbus W E Aldeen M Davis and K CCarroll ldquoTrichuris vulpis recovered from a patient with chronicdiarrhea and five dogsrdquo Journal of Clinical Microbiology vol 40no 7 pp 2703ndash2704 2002
[22] M Papazahariadou A Founta E Papadopoulos SChliounakis K Antoniadou-Sotiriadou and Y TheodoridesldquoGastrointestinal parasites of shepherd and hunting dogs in theSerres Prefecture Northern Greecerdquo Veterinary Parasitologyvol 148 no 2 pp 170ndash173 2007
[23] C Martınez-Carrasco E Berriatua M Garijo J Martınez FD Alonso and R Ruiz De Ybanez ldquoEpidemiological study ofnon-systemic parasitism in dogs in southeast MediterraneanSpain assessed by coprological and post-mortem examinationrdquoZoonoses and Public Health vol 54 no 5 pp 195ndash203 2007
[24] S Leonhard K Pfister P Beelitz C Wielinga and R C AThompson ldquoThe molecular characterisation of Giardia fromdogs in southern Germanyrdquo Veterinary Parasitology vol 150no 1-2 pp 33ndash38 2007
[25] C Genchi G Gili and R Maraschin ldquoIndagine sullrsquoincidenzadelle elmintiasi intestinali del cane in alcune zone della Lom-bardiardquo La Clinica Veterinaria vol 97 no 6 pp 178ndash186 1974
[26] E Spada D Proverbio A Della Pepa et al ldquoPrevalence offaecal-borne parasites in colony stray cats in northern ItalyrdquoJournal of Feline Medicine and Surgery vol 15 no 8 pp 672ndash677 2013
[27] R M Hopkins B P Meloni D M Groth J D WetherallJ A Reynoldson and R C A Thompson ldquoRibosomal RNAsequencing reveals differences between the genotypes of Giar-dia isolates recovered from humans and dogs living in the samelocalityrdquo Journal of Parasitology vol 83 no 1 pp 44ndash51 1997
[28] C Read J Walters I D Robertson and R C A ThompsonldquoCorrelation between genotype of Giardia duodenalis anddiarrhoeardquo International Journal for Parasitology vol 32 no 2pp 229ndash231 2002
[29] A O Bush K D Lafferty J M Lotz and A W ShostakldquoParasitology meets ecology on its own terms Margolis et alrevisitedrdquo Journal of Parasitology vol 83 no 4 pp 575ndash5831997
[30] C N L Macpherson ldquoThe epidemiology and public healthimportance of toxocariasis a zoonosis of global importancerdquoInternational Journal for Parasitology vol 43 pp 999ndash10082013
[31] U Ryan and S M Caccio ldquoZoonotic potential of GiardiardquoInternational Journal For Parasitology vol 43 pp 943ndash9562013
[32] M Genchi E Ferroglio G Traldi S Passera G MezzanoandCGenchi ldquoFecalizzazione ambientale e rischio parassitarionelle citta di Milano e Torinordquo Professione Veterinaria vol 41pp 15ndash17 2007
[33] F Riggio R Mannella G Ariti and S Perrucci ldquoIntestinaland lung parasites in owned dogs and cats from central ItalyrdquoVeterinary Parasitology vol 193 no 1ndash3 pp 78ndash84 2013
[34] LMugnaini R Papini G Gorini A Passantino VMerildi andF Mancianti ldquoPattern and predictive factors of endoparasitismin cats in central Italyrdquo Revue de Medecine Veterinaire vol 163no 2 pp 85ndash88 2012
10 BioMed Research International
[35] D Traversa ldquoPet roundworms and hookworms a continuingneed for global wormingrdquo Parasite amp Vectors vol 5 no 1 p 912012
[36] F Berrilli D di Cave C de Liberato A Franco PScaramozzino and P Orecchia ldquoGenotype characterisation ofGiardia duodenalis isolates from domestic and farm animals bySSU-rRNA gene sequencingrdquo Veterinary Parasitology vol 122no 3 pp 193ndash199 2004
[37] P Bianciardi R Papini G Giuliani andG Cardini ldquoPrevalenceof Giardia antigen in stool samples from dogs and catsrdquo Revuede Medecine Veterinaire vol 155 no 8-9 pp 417ndash421 2004
[38] G Capelli A Frangipane di Regalbono R Iorio M PietrobelliB Paoletti and A Giangaspero ldquoGiardia species and otherintestinal parasites in dogs in north-east and central ItalyrdquoVeterinary Record vol 159 no 13 pp 422ndash424 2006
[39] L Rinaldi M P Maurelli V Musella et al ldquoGiardia andCryptosporidium in canine faecal samples contaminating anurban areardquo Research in Veterinary Science vol 84 no 3 pp413ndash415 2008
[40] A V Scorza L R Ballweber S Tangtrongsup C Panuska andM R Lappin ldquoComparisons of mammalianGiardia duodenalisassemblages based on the 120573-giardin glutamate dehydrogenaseand triose phosphate isomerase genesrdquo Veterinary Parasitologyvol 189 no 2ndash4 pp 182ndash188 2012
[41] F D Uehlinger S J Greenwood J T McClure G B ConboyR OrsquoHandley and H W Barkema ldquoZoonotic potential ofGiardia duodenalis and Cryptosporidium spp and prevalenceof intestinal parasites in young dogs from different populationson Prince Edward Island Canadardquo Veterinary Parasitology vol196 no 3-4 pp 509ndash514 2013
[42] L R Ballweber L Xiao D D Bowman G Kahn and V ACama ldquoGiardiasis in dogs and cats update on epidemiology andpublic health significancerdquo Trends in Parasitology vol 26 no 4pp 180ndash189 2010
[43] D Jaros W Zygner S Jaros and HWedrychowicz ldquoDetectionof Giardia intestinalis assemblages A B and D in domestic catsfrom Warsaw Polandrdquo Polish Journal of Microbiology vol 60no 3 pp 259ndash263 2011
[44] R C AndersonNematode Parasites of Vertebrates Their Devel-opment and Transmission Cabi Publishing Wallingford UK2nd edition 2000
Submit your manuscripts athttpwwwhindawicom
Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014
Anatomy Research International
PeptidesInternational Journal of
Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014
Hindawi Publishing Corporation httpwwwhindawicom
International Journal of
Volume 2014
Zoology
Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014
Molecular Biology International
GenomicsInternational Journal of
Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014
The Scientific World JournalHindawi Publishing Corporation httpwwwhindawicom Volume 2014
Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014
BioinformaticsAdvances in
Marine BiologyJournal of
Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014
Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014
Signal TransductionJournal of
Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014
BioMed Research International
Evolutionary BiologyInternational Journal of
Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014
Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014
Biochemistry Research International
ArchaeaHindawi Publishing Corporationhttpwwwhindawicom Volume 2014
Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014
Genetics Research International
Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014
Advances in
Virolog y
Hindawi Publishing Corporationhttpwwwhindawicom
Nucleic AcidsJournal of
Volume 2014
Stem CellsInternational
Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014
Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014
Enzyme Research
Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014
International Journal of
Microbiology
BioMed Research International 7
Table 5 Frequency of pets (dogs or cats) infected or not infectedby intestinal parasites in northern Italy according to gastrointestinalsymptoms (presence or absence)
Infection No infection 119875 valuelowast
DogsSymptomatic 21 23 085Asymptomatic 48 48
CatSymptomatic 10 13 0128Asymptomatic 28 16
lowastFisherrsquos exact 119875 value
Table 6 Frequency of pets (dogs or cats) infected by intestinalparasites in northwestern Italy by features of their owners (number207)
Owner features Frequency of pets119875 valuelowast
Positive 119899 () Negative 119899 ()Gender
Female 75 (3694) 66 (3251) 024Male 29 (1428) 33 (1625)
Agele40 years old 65 (3202) 66 (3251) 031gt40 years old 39 (1921) 33 (1625)
Educationalqualification
Secondary schoolcertificate 38 (1871) 33 (1625) 037Intermediate schoolcertificateacademicdegree
66 (3251) 66 (3251)
Family componentsle2 42 (2058) 47 (2303) 020gt2 62 (3039) 53 (2598)
Presence of young lt15years old
Not 66 (3235) 68 (3333) 029Yes 38 (1862) 32 (1568)
lowastFisherrsquos exact 119875 value
Among the recovered helminthic species T canis and Tcati which accountedthe most frequent are consideredof great public health significance in their causing themost widespread and economically important zoonoses [30]Other parasites diffusing zoonoses ofminor importance werefound such as T vulpis Ancylostomatidae and Dypilid-ium canimum Finally molecular analysis on fecal samplesdemonstrated the presence of G duodenalis AssemblageA considered to have zoonotic potential [31] The overallprevalence of intestinal parasites both in dogs and in catsin northern Italy was higher than expected (119875 = 2816ndash5741 in dogs 119875 = 3258ndash6042 in cats) The currentlyreported prevalence rates of dog parasites are slightly differentconsidering the different origin of sampled dogs Particularlydogs from the large metropolitan area of Milan showed
lower prevalence than dogs from themicropolitan territoriesSeveral factors can justify these differences In fact most dogsfromMilan were rarely taken to large playgrounds limited intheir walks and regularly treated against heartworm diseaseFurther no colonies of stray dogs exist and proper disposalof dog waste from public soil is coming into common useamong urban pet owners On the other hand dogs frommicropolitan areas are usually at high risk of infection beingfrequently outdoors in their gardens or in large green areasIn addition transhumance being still practiced in Lombardythey might reasonably be infected by sheepdogs guardingtranshumant sheep flocks In fact they are moved fromAlpine pastures to lowlands twice yearly along the mainroutes (north to south) throughBergamo andBrescia towardsthe Po Plain areas whose fields may be contaminated by fecesof untreated sheepdog thus passing infection
In dogs as regards helminths only currently reportedprevalences significantly differ from what was previouslyobserved in Lombardy In 1974 in a coprological surveyconducted in some micropolitan areas located north andsouth of Milan helminths were recorded in 7579ndash853 ofexamined dogs [25] Further development in diagnosis andtreatment may account for the substantial differences foundwith our present survey together with a more widespreadprophylaxis against D immitis in the area of Milan whichmight have reasonably contributed to control canine intesti-nal parasites In 2007 helminth eggs were recovered in 7of dog feces collected from public places including parksof Milan [32] indicating a lower prevalence than in ourlatest survey (119875 = 141) This could be due to thekind of fecal samples collected from city soil that mainlyincluded droppings voided by old dogs typically showinglower infection values than young ones On the other handour findings are consistent with results from a recent surveyon pets from central Italy sampled in veterinary clinics wherehelminth infections were present in 241 of owned dogsand in 319 of owned cats [33] In the same year helminthinfections were recorded in 501 of stray cats from coloniespertaining to the metropolitan area of Milan [26]
Consistent with data obtained in several countriesascarids especially Toxocara spp were the most prevalentcanine and feline parasites [7 10 12ndash14 33 34] In contrastwith other surveys a low prevalence of Ancylostomatidaeinfection was recorded in our sampled dogs except thosefrom the micropolitan areas 1 and 2 A low presence ofhunting sporting or guard dogs in our samples as well asepidemiology and life cycle of Ancylostomatidae nematodescan account for this discrepancy [2 3 8 11 35]
As regardsG duodenalis it was themost prevalent canineand feline parasite according to other surveys [5 8ndash10 12]Such findings are not consistent with low prevalence valuesrecorded in the same species in other Italian studies whoseanalytical methods were different [32 36ndash39]
In this survey consistent with previous studies [31 40 41]G duodenalis assemblages C and D were isolated in dogsThey are considered host-adapted genotypes and a speciesname Giardia canis was proposed to label them As regardscats in our study the host-adapted F genotype was notfound however G duodenalis infections sustained also by
8 BioMed Research International
assemblages A B C and D have been previously describedin cats [40 42] In owned cats we observed a high prevalenceof G duodenalis infection by assemblage A whose possiblezoonotic potential must not be underestimated [31] FinallyG duodenalis assemblage D was recovered less frequentlythough [42 43]
Risk factors for dogs frommetropolitan andmicropolitanareas were being younger than 12 months or sharing thesame house with other dogs Compared to dogs from thelarge metropolitan area of Milan the odds for dogs from themicropolitan area 1 were 3476 times higher and the oddsfor dogs from MC 2 were 1947 times higher but with lowersignificance (119875 = 0001 versus 119875 = 0055) Further comparedto dogs le12 months old the odds of a dog gt12 months beingparasitized were 0362 times smaller Compared to single-household dogs the odds for multiple- household dogs were2059 times higher which means that cohabitation is oneof the most important risk factors associated to endopara-sitism In accordance with Katagiri andOliveira-Sequeira [2]who also found higher prevalence in multihousehold dogssignificant differences were found for Ancylostomatidae andT vulpis infections It might be that in the presence ofmultiple pets environmental contamination with infectivestages of these taxa occurs dogs become more susceptible toinfections and environmental contamination itself is higherand better maintained In cats the presence of endoparasiteswas associated only with their age housing and with the areathey lived in These findings are consistent with other studiesconsidering parasitism as of primarily concern for youngerdogs or cats [4 5 7 14] According to the univariate analysisthe overall prevalence of intestinal parasites in household catsshows statistically significant differences with cats that livedoutsidewith access to a garden (119875 = 50 in household versus119875 = 6552 in outdoor) Living outdoors or having accessto a garden seems to be a risk factor for T leonina infectionin cats as similarly described by Nareaho et al [15] It couldbe partially due to the source of infection for this parasitethat in addition to larvated eggs is represented by paratenichosts that harbour somatic third-stage larvae [44] As aconsequence of their predatory behavior domestic felinescould bemore susceptible to infections due to paratenic hostswhen they have outdoor access
Dogs and cats presenting gastrointestinal signs showed aprevalence of intestinal parasites close to 45 which urgesto differential diagnosis and periodic coprological exami-nation Prophylaxis against D immitis showed ineffectivein protecting dogs against gastrointestinal nematodes Forthem registered dosage of macrocyclic lactones used againstheartworms must be too low and seasonal administration ofthe treatment to all sampled adults dogs proved insufficientto cover their exposition to other risk factors all over theyear The answers to our questionnaire specifically designedto understand ownerrsquos awareness and information aboutcanine and feline gastrointestinal parasites showed thatthey knew but few aspects of the parasite biology In factmore than 7189 of them indicated that fecal contamina-tion can cause gastrointestinal parasite infection and thusthey were probably aware of the importance of reducingenvironmental fecal voiding Nonetheless 3910 of them
gave a negative answer or no answer at all As to possiblelasting environmental contamination due to infected petfecalization 5622 of total owners were not aware of it andmost of them probably did not consider preventing contactwith intermediateparatenic hosts as a possible prophylaxisagainst intestinal parasites infections A higher number ofowners (4811) correctly answered affirmatively when askedabout the possibility of transmission of intestinal parasitesto puppieskittens by infective milk of bitchesqueens Theymay be more stressed by clinicians on the importance ofintestinal parasite infections in puppies and kittens than inadult dogs and cats Concerning their awareness of risks forhuman health from canine and feline intestinal parasites5081 declared that intestinal parasites of dogs and cats donot represent any kind of risk for human health or that theydid not know about the issue Further 2637 out of 90owners informed about human health risks stated that theycould not name possible diseases thus confirming that theydid not know what proper behavior is necessary to reducezoonotic risks
Overall these results indicated that owners needed moreand clear information about zoonotic potential of intestinalparasites and that the veterinarians can be of extremeimportance in this process
5 Conclusion
Results of this survey showed that intestinal parasites are stilla common finding in owned dogs and cats not to be underes-timated in both metropolitan and micropolitan areas even ifthe latter indicated higher pet infection prevalence Furtherwhen a dog or a cat is presented to clinical examination onaccount of gastrointestinal signs intestinal parasite infectionshould be considered as a possible differential diagnosisThis condition can be asymptomatic and can even affectanimals under proper prophylaxis against D immitis thuseven apparently fit and healthy pets should be submitted toannual or biannual fecal examination Clinicians should alsoconsider that younger patients that live in micropolitan areasare the most susceptible to parasite infections The zoonoticparasites T canis and T cati T vulpis Ancylostomatidae andG duodenalis assemblage A resulted to be the most commonspecies in owned pets In any case veterinaries clearly play akey role in increasing awareness and knowledge of pet ownersabout canine and feline gastrointestinal parasites as to theirinfection routes proper monitoring and correct behavior toavoid potential zoonotic risks
Conflict of Interests
The authors declare that there is no conflict of interestsregarding the publication of this paper
References
[1] A C Y Lee PM Schantz K R Kazacos S PMontgomery andD D Bowman ldquoEpidemiologic and zoonotic aspects of ascaridinfections in dogs and catsrdquo Trends in Parasitology vol 26 no4 pp 155ndash161 2010
BioMed Research International 9
[2] S Katagiri and T C G Oliveira-Sequeira ldquoPrevalence of dogintestinal parasites and risk perception of zoonotic infectionby dog owners in Sao Paulo State Brazilrdquo Zoonoses and PublicHealth vol 55 no 8ndash10 pp 406ndash413 2008
[3] S E Little E M Johnson D Lewis et al ldquoPrevalence ofintestinal parasites in pet dogs in the United Statesrdquo VeterinaryParasitology vol 166 no 1-2 pp 144ndash152 2009
[4] D Barutzki andR Schaper ldquoResults of parasitological examina-tions of faecal samples from cats and dogs in Germany between2003 and 2010rdquo Parasitology Research vol 109 no 1 pp S45ndashS60 2011
[5] N Itoh H Ikegami M Takagi et al ldquoPrevalence of intestinalparasites in private-household cats in Japanrdquo Journal of FelineMedical Surgery vol 14 no 6 pp 436ndash439 2012
[6] M C Gates and T J Nolan ldquoEfficacy of heartworm pre-ventatives against ascarids and hookworms in client-owneddogs a retrospective case control studyrdquo Journal of VeterinaryPharmacology andTherapeutics vol 34 no 2 pp 116ndash119 2011
[7] M C Gates and T J Nolan ldquoEndoparasite prevalence andrecurrence across different age groups of dogs and catsrdquoVeterinary Parasitology vol 166 no 1-2 pp 153ndash158 2009
[8] F S Ferreira P Pereira-Baltasar R Parreira et al ldquoIntestinalparasites in dogs and cats from the district of Evora PortugalrdquoVeterinary Parasitology vol 179 no 1ndash3 pp 242ndash245 2011
[9] C Epe G Rehkter T Schnieder L Lorentzen and L Kreien-brock ldquoGiardia in symptomatic dogs and cats in Europe-Resultsof a European studyrdquo Veterinary Parasitology vol 173 no 1-2pp 32ndash38 2010
[10] D Joffe D van Niekerk F Gagne J Gilleard S Kutz and RLobingier ldquoThe prevalence of intestinal parasites in dogs andcats in Calgary ABrdquo Canadian Veterinary Journal vol 52 no12 pp 1323ndash1328 2011
[11] T M Savilla J E Joy J D May and C C SomervilleldquoPrevalence of dog intestinal nematode parasites in southcentral West Virginia USArdquo Veterinary Parasitology vol 178no 1-2 pp 115ndash120 2011
[12] E Claerebout S Casaert A-C Dalemans et al ldquoGiardiaand other intestinal parasites in different dog populations inNorthern BelgiumrdquoVeterinary Parasitology vol 161 no 1-2 pp41ndash46 2009
[13] P A M Overgaauw L van Zutphen D Hoek et al ldquoZoonoticparasites in fecal samples and fur from dogs and cats in TheNetherlandsrdquo Veterinary Parasitology vol 163 no 1-2 pp 115ndash122 2009
[14] M C Gates and T J Nolan ldquoRisk factors for endoparasitismin dogs retrospective case-control study of 6578 veterinaryteaching hospital casesrdquo Journal of Small Animal Practice vol50 no 12 pp 636ndash640 2009
[15] A Nareaho J Puomio K Saarinen P Jokelainen T Juseliusand A Sukura ldquoFeline intestinal parasites in Finland preva-lence risk factors and anthelmintic treatment practicesrdquo Journalof Feline Medicine and Surgery vol 14 no 6 pp 378ndash383 2012
[16] L Polley and R C A Thompson ldquoParasite zoonoses and cli-mate change molecular tools for tracking shifting boundariesrdquoTrends in Parasitology vol 25 no 6 pp 285ndash291 2009
[17] E J Jenkins J M Schurer and K M Gesy ldquoOld problems on anew playing field helminth zoonoses transmitted among dogswildlife and people in a changing northern climaterdquoVeterinaryParasitology vol 182 no 1 pp 54ndash69 2011
[18] P N Acha and B Szyfres Zoonoses et Maladies TransmissiblesCommunes a lrsquohomme et Aux animaux Office International desEpizooties Paris France 1989
[19] M Fisher ldquoToxocara cati an underestimated zoonotic agentrdquoTrends in Parasitology vol 19 no 4 pp 167ndash170 2003
[20] Y Masuda T Kishimoto H Ito and M Tsuji ldquoVisceral larvamigrans caused by Trichuris vulpis presenting as a pulmonarymassrdquoThorax vol 42 no 12 pp 990ndash991 1987
[21] J J Dunn S T Columbus W E Aldeen M Davis and K CCarroll ldquoTrichuris vulpis recovered from a patient with chronicdiarrhea and five dogsrdquo Journal of Clinical Microbiology vol 40no 7 pp 2703ndash2704 2002
[22] M Papazahariadou A Founta E Papadopoulos SChliounakis K Antoniadou-Sotiriadou and Y TheodoridesldquoGastrointestinal parasites of shepherd and hunting dogs in theSerres Prefecture Northern Greecerdquo Veterinary Parasitologyvol 148 no 2 pp 170ndash173 2007
[23] C Martınez-Carrasco E Berriatua M Garijo J Martınez FD Alonso and R Ruiz De Ybanez ldquoEpidemiological study ofnon-systemic parasitism in dogs in southeast MediterraneanSpain assessed by coprological and post-mortem examinationrdquoZoonoses and Public Health vol 54 no 5 pp 195ndash203 2007
[24] S Leonhard K Pfister P Beelitz C Wielinga and R C AThompson ldquoThe molecular characterisation of Giardia fromdogs in southern Germanyrdquo Veterinary Parasitology vol 150no 1-2 pp 33ndash38 2007
[25] C Genchi G Gili and R Maraschin ldquoIndagine sullrsquoincidenzadelle elmintiasi intestinali del cane in alcune zone della Lom-bardiardquo La Clinica Veterinaria vol 97 no 6 pp 178ndash186 1974
[26] E Spada D Proverbio A Della Pepa et al ldquoPrevalence offaecal-borne parasites in colony stray cats in northern ItalyrdquoJournal of Feline Medicine and Surgery vol 15 no 8 pp 672ndash677 2013
[27] R M Hopkins B P Meloni D M Groth J D WetherallJ A Reynoldson and R C A Thompson ldquoRibosomal RNAsequencing reveals differences between the genotypes of Giar-dia isolates recovered from humans and dogs living in the samelocalityrdquo Journal of Parasitology vol 83 no 1 pp 44ndash51 1997
[28] C Read J Walters I D Robertson and R C A ThompsonldquoCorrelation between genotype of Giardia duodenalis anddiarrhoeardquo International Journal for Parasitology vol 32 no 2pp 229ndash231 2002
[29] A O Bush K D Lafferty J M Lotz and A W ShostakldquoParasitology meets ecology on its own terms Margolis et alrevisitedrdquo Journal of Parasitology vol 83 no 4 pp 575ndash5831997
[30] C N L Macpherson ldquoThe epidemiology and public healthimportance of toxocariasis a zoonosis of global importancerdquoInternational Journal for Parasitology vol 43 pp 999ndash10082013
[31] U Ryan and S M Caccio ldquoZoonotic potential of GiardiardquoInternational Journal For Parasitology vol 43 pp 943ndash9562013
[32] M Genchi E Ferroglio G Traldi S Passera G MezzanoandCGenchi ldquoFecalizzazione ambientale e rischio parassitarionelle citta di Milano e Torinordquo Professione Veterinaria vol 41pp 15ndash17 2007
[33] F Riggio R Mannella G Ariti and S Perrucci ldquoIntestinaland lung parasites in owned dogs and cats from central ItalyrdquoVeterinary Parasitology vol 193 no 1ndash3 pp 78ndash84 2013
[34] LMugnaini R Papini G Gorini A Passantino VMerildi andF Mancianti ldquoPattern and predictive factors of endoparasitismin cats in central Italyrdquo Revue de Medecine Veterinaire vol 163no 2 pp 85ndash88 2012
10 BioMed Research International
[35] D Traversa ldquoPet roundworms and hookworms a continuingneed for global wormingrdquo Parasite amp Vectors vol 5 no 1 p 912012
[36] F Berrilli D di Cave C de Liberato A Franco PScaramozzino and P Orecchia ldquoGenotype characterisation ofGiardia duodenalis isolates from domestic and farm animals bySSU-rRNA gene sequencingrdquo Veterinary Parasitology vol 122no 3 pp 193ndash199 2004
[37] P Bianciardi R Papini G Giuliani andG Cardini ldquoPrevalenceof Giardia antigen in stool samples from dogs and catsrdquo Revuede Medecine Veterinaire vol 155 no 8-9 pp 417ndash421 2004
[38] G Capelli A Frangipane di Regalbono R Iorio M PietrobelliB Paoletti and A Giangaspero ldquoGiardia species and otherintestinal parasites in dogs in north-east and central ItalyrdquoVeterinary Record vol 159 no 13 pp 422ndash424 2006
[39] L Rinaldi M P Maurelli V Musella et al ldquoGiardia andCryptosporidium in canine faecal samples contaminating anurban areardquo Research in Veterinary Science vol 84 no 3 pp413ndash415 2008
[40] A V Scorza L R Ballweber S Tangtrongsup C Panuska andM R Lappin ldquoComparisons of mammalianGiardia duodenalisassemblages based on the 120573-giardin glutamate dehydrogenaseand triose phosphate isomerase genesrdquo Veterinary Parasitologyvol 189 no 2ndash4 pp 182ndash188 2012
[41] F D Uehlinger S J Greenwood J T McClure G B ConboyR OrsquoHandley and H W Barkema ldquoZoonotic potential ofGiardia duodenalis and Cryptosporidium spp and prevalenceof intestinal parasites in young dogs from different populationson Prince Edward Island Canadardquo Veterinary Parasitology vol196 no 3-4 pp 509ndash514 2013
[42] L R Ballweber L Xiao D D Bowman G Kahn and V ACama ldquoGiardiasis in dogs and cats update on epidemiology andpublic health significancerdquo Trends in Parasitology vol 26 no 4pp 180ndash189 2010
[43] D Jaros W Zygner S Jaros and HWedrychowicz ldquoDetectionof Giardia intestinalis assemblages A B and D in domestic catsfrom Warsaw Polandrdquo Polish Journal of Microbiology vol 60no 3 pp 259ndash263 2011
[44] R C AndersonNematode Parasites of Vertebrates Their Devel-opment and Transmission Cabi Publishing Wallingford UK2nd edition 2000
Submit your manuscripts athttpwwwhindawicom
Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014
Anatomy Research International
PeptidesInternational Journal of
Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014
Hindawi Publishing Corporation httpwwwhindawicom
International Journal of
Volume 2014
Zoology
Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014
Molecular Biology International
GenomicsInternational Journal of
Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014
The Scientific World JournalHindawi Publishing Corporation httpwwwhindawicom Volume 2014
Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014
BioinformaticsAdvances in
Marine BiologyJournal of
Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014
Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014
Signal TransductionJournal of
Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014
BioMed Research International
Evolutionary BiologyInternational Journal of
Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014
Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014
Biochemistry Research International
ArchaeaHindawi Publishing Corporationhttpwwwhindawicom Volume 2014
Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014
Genetics Research International
Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014
Advances in
Virolog y
Hindawi Publishing Corporationhttpwwwhindawicom
Nucleic AcidsJournal of
Volume 2014
Stem CellsInternational
Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014
Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014
Enzyme Research
Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014
International Journal of
Microbiology
8 BioMed Research International
assemblages A B C and D have been previously describedin cats [40 42] In owned cats we observed a high prevalenceof G duodenalis infection by assemblage A whose possiblezoonotic potential must not be underestimated [31] FinallyG duodenalis assemblage D was recovered less frequentlythough [42 43]
Risk factors for dogs frommetropolitan andmicropolitanareas were being younger than 12 months or sharing thesame house with other dogs Compared to dogs from thelarge metropolitan area of Milan the odds for dogs from themicropolitan area 1 were 3476 times higher and the oddsfor dogs from MC 2 were 1947 times higher but with lowersignificance (119875 = 0001 versus 119875 = 0055) Further comparedto dogs le12 months old the odds of a dog gt12 months beingparasitized were 0362 times smaller Compared to single-household dogs the odds for multiple- household dogs were2059 times higher which means that cohabitation is oneof the most important risk factors associated to endopara-sitism In accordance with Katagiri andOliveira-Sequeira [2]who also found higher prevalence in multihousehold dogssignificant differences were found for Ancylostomatidae andT vulpis infections It might be that in the presence ofmultiple pets environmental contamination with infectivestages of these taxa occurs dogs become more susceptible toinfections and environmental contamination itself is higherand better maintained In cats the presence of endoparasiteswas associated only with their age housing and with the areathey lived in These findings are consistent with other studiesconsidering parasitism as of primarily concern for youngerdogs or cats [4 5 7 14] According to the univariate analysisthe overall prevalence of intestinal parasites in household catsshows statistically significant differences with cats that livedoutsidewith access to a garden (119875 = 50 in household versus119875 = 6552 in outdoor) Living outdoors or having accessto a garden seems to be a risk factor for T leonina infectionin cats as similarly described by Nareaho et al [15] It couldbe partially due to the source of infection for this parasitethat in addition to larvated eggs is represented by paratenichosts that harbour somatic third-stage larvae [44] As aconsequence of their predatory behavior domestic felinescould bemore susceptible to infections due to paratenic hostswhen they have outdoor access
Dogs and cats presenting gastrointestinal signs showed aprevalence of intestinal parasites close to 45 which urgesto differential diagnosis and periodic coprological exami-nation Prophylaxis against D immitis showed ineffectivein protecting dogs against gastrointestinal nematodes Forthem registered dosage of macrocyclic lactones used againstheartworms must be too low and seasonal administration ofthe treatment to all sampled adults dogs proved insufficientto cover their exposition to other risk factors all over theyear The answers to our questionnaire specifically designedto understand ownerrsquos awareness and information aboutcanine and feline gastrointestinal parasites showed thatthey knew but few aspects of the parasite biology In factmore than 7189 of them indicated that fecal contamina-tion can cause gastrointestinal parasite infection and thusthey were probably aware of the importance of reducingenvironmental fecal voiding Nonetheless 3910 of them
gave a negative answer or no answer at all As to possiblelasting environmental contamination due to infected petfecalization 5622 of total owners were not aware of it andmost of them probably did not consider preventing contactwith intermediateparatenic hosts as a possible prophylaxisagainst intestinal parasites infections A higher number ofowners (4811) correctly answered affirmatively when askedabout the possibility of transmission of intestinal parasitesto puppieskittens by infective milk of bitchesqueens Theymay be more stressed by clinicians on the importance ofintestinal parasite infections in puppies and kittens than inadult dogs and cats Concerning their awareness of risks forhuman health from canine and feline intestinal parasites5081 declared that intestinal parasites of dogs and cats donot represent any kind of risk for human health or that theydid not know about the issue Further 2637 out of 90owners informed about human health risks stated that theycould not name possible diseases thus confirming that theydid not know what proper behavior is necessary to reducezoonotic risks
Overall these results indicated that owners needed moreand clear information about zoonotic potential of intestinalparasites and that the veterinarians can be of extremeimportance in this process
5 Conclusion
Results of this survey showed that intestinal parasites are stilla common finding in owned dogs and cats not to be underes-timated in both metropolitan and micropolitan areas even ifthe latter indicated higher pet infection prevalence Furtherwhen a dog or a cat is presented to clinical examination onaccount of gastrointestinal signs intestinal parasite infectionshould be considered as a possible differential diagnosisThis condition can be asymptomatic and can even affectanimals under proper prophylaxis against D immitis thuseven apparently fit and healthy pets should be submitted toannual or biannual fecal examination Clinicians should alsoconsider that younger patients that live in micropolitan areasare the most susceptible to parasite infections The zoonoticparasites T canis and T cati T vulpis Ancylostomatidae andG duodenalis assemblage A resulted to be the most commonspecies in owned pets In any case veterinaries clearly play akey role in increasing awareness and knowledge of pet ownersabout canine and feline gastrointestinal parasites as to theirinfection routes proper monitoring and correct behavior toavoid potential zoonotic risks
Conflict of Interests
The authors declare that there is no conflict of interestsregarding the publication of this paper
References
[1] A C Y Lee PM Schantz K R Kazacos S PMontgomery andD D Bowman ldquoEpidemiologic and zoonotic aspects of ascaridinfections in dogs and catsrdquo Trends in Parasitology vol 26 no4 pp 155ndash161 2010
BioMed Research International 9
[2] S Katagiri and T C G Oliveira-Sequeira ldquoPrevalence of dogintestinal parasites and risk perception of zoonotic infectionby dog owners in Sao Paulo State Brazilrdquo Zoonoses and PublicHealth vol 55 no 8ndash10 pp 406ndash413 2008
[3] S E Little E M Johnson D Lewis et al ldquoPrevalence ofintestinal parasites in pet dogs in the United Statesrdquo VeterinaryParasitology vol 166 no 1-2 pp 144ndash152 2009
[4] D Barutzki andR Schaper ldquoResults of parasitological examina-tions of faecal samples from cats and dogs in Germany between2003 and 2010rdquo Parasitology Research vol 109 no 1 pp S45ndashS60 2011
[5] N Itoh H Ikegami M Takagi et al ldquoPrevalence of intestinalparasites in private-household cats in Japanrdquo Journal of FelineMedical Surgery vol 14 no 6 pp 436ndash439 2012
[6] M C Gates and T J Nolan ldquoEfficacy of heartworm pre-ventatives against ascarids and hookworms in client-owneddogs a retrospective case control studyrdquo Journal of VeterinaryPharmacology andTherapeutics vol 34 no 2 pp 116ndash119 2011
[7] M C Gates and T J Nolan ldquoEndoparasite prevalence andrecurrence across different age groups of dogs and catsrdquoVeterinary Parasitology vol 166 no 1-2 pp 153ndash158 2009
[8] F S Ferreira P Pereira-Baltasar R Parreira et al ldquoIntestinalparasites in dogs and cats from the district of Evora PortugalrdquoVeterinary Parasitology vol 179 no 1ndash3 pp 242ndash245 2011
[9] C Epe G Rehkter T Schnieder L Lorentzen and L Kreien-brock ldquoGiardia in symptomatic dogs and cats in Europe-Resultsof a European studyrdquo Veterinary Parasitology vol 173 no 1-2pp 32ndash38 2010
[10] D Joffe D van Niekerk F Gagne J Gilleard S Kutz and RLobingier ldquoThe prevalence of intestinal parasites in dogs andcats in Calgary ABrdquo Canadian Veterinary Journal vol 52 no12 pp 1323ndash1328 2011
[11] T M Savilla J E Joy J D May and C C SomervilleldquoPrevalence of dog intestinal nematode parasites in southcentral West Virginia USArdquo Veterinary Parasitology vol 178no 1-2 pp 115ndash120 2011
[12] E Claerebout S Casaert A-C Dalemans et al ldquoGiardiaand other intestinal parasites in different dog populations inNorthern BelgiumrdquoVeterinary Parasitology vol 161 no 1-2 pp41ndash46 2009
[13] P A M Overgaauw L van Zutphen D Hoek et al ldquoZoonoticparasites in fecal samples and fur from dogs and cats in TheNetherlandsrdquo Veterinary Parasitology vol 163 no 1-2 pp 115ndash122 2009
[14] M C Gates and T J Nolan ldquoRisk factors for endoparasitismin dogs retrospective case-control study of 6578 veterinaryteaching hospital casesrdquo Journal of Small Animal Practice vol50 no 12 pp 636ndash640 2009
[15] A Nareaho J Puomio K Saarinen P Jokelainen T Juseliusand A Sukura ldquoFeline intestinal parasites in Finland preva-lence risk factors and anthelmintic treatment practicesrdquo Journalof Feline Medicine and Surgery vol 14 no 6 pp 378ndash383 2012
[16] L Polley and R C A Thompson ldquoParasite zoonoses and cli-mate change molecular tools for tracking shifting boundariesrdquoTrends in Parasitology vol 25 no 6 pp 285ndash291 2009
[17] E J Jenkins J M Schurer and K M Gesy ldquoOld problems on anew playing field helminth zoonoses transmitted among dogswildlife and people in a changing northern climaterdquoVeterinaryParasitology vol 182 no 1 pp 54ndash69 2011
[18] P N Acha and B Szyfres Zoonoses et Maladies TransmissiblesCommunes a lrsquohomme et Aux animaux Office International desEpizooties Paris France 1989
[19] M Fisher ldquoToxocara cati an underestimated zoonotic agentrdquoTrends in Parasitology vol 19 no 4 pp 167ndash170 2003
[20] Y Masuda T Kishimoto H Ito and M Tsuji ldquoVisceral larvamigrans caused by Trichuris vulpis presenting as a pulmonarymassrdquoThorax vol 42 no 12 pp 990ndash991 1987
[21] J J Dunn S T Columbus W E Aldeen M Davis and K CCarroll ldquoTrichuris vulpis recovered from a patient with chronicdiarrhea and five dogsrdquo Journal of Clinical Microbiology vol 40no 7 pp 2703ndash2704 2002
[22] M Papazahariadou A Founta E Papadopoulos SChliounakis K Antoniadou-Sotiriadou and Y TheodoridesldquoGastrointestinal parasites of shepherd and hunting dogs in theSerres Prefecture Northern Greecerdquo Veterinary Parasitologyvol 148 no 2 pp 170ndash173 2007
[23] C Martınez-Carrasco E Berriatua M Garijo J Martınez FD Alonso and R Ruiz De Ybanez ldquoEpidemiological study ofnon-systemic parasitism in dogs in southeast MediterraneanSpain assessed by coprological and post-mortem examinationrdquoZoonoses and Public Health vol 54 no 5 pp 195ndash203 2007
[24] S Leonhard K Pfister P Beelitz C Wielinga and R C AThompson ldquoThe molecular characterisation of Giardia fromdogs in southern Germanyrdquo Veterinary Parasitology vol 150no 1-2 pp 33ndash38 2007
[25] C Genchi G Gili and R Maraschin ldquoIndagine sullrsquoincidenzadelle elmintiasi intestinali del cane in alcune zone della Lom-bardiardquo La Clinica Veterinaria vol 97 no 6 pp 178ndash186 1974
[26] E Spada D Proverbio A Della Pepa et al ldquoPrevalence offaecal-borne parasites in colony stray cats in northern ItalyrdquoJournal of Feline Medicine and Surgery vol 15 no 8 pp 672ndash677 2013
[27] R M Hopkins B P Meloni D M Groth J D WetherallJ A Reynoldson and R C A Thompson ldquoRibosomal RNAsequencing reveals differences between the genotypes of Giar-dia isolates recovered from humans and dogs living in the samelocalityrdquo Journal of Parasitology vol 83 no 1 pp 44ndash51 1997
[28] C Read J Walters I D Robertson and R C A ThompsonldquoCorrelation between genotype of Giardia duodenalis anddiarrhoeardquo International Journal for Parasitology vol 32 no 2pp 229ndash231 2002
[29] A O Bush K D Lafferty J M Lotz and A W ShostakldquoParasitology meets ecology on its own terms Margolis et alrevisitedrdquo Journal of Parasitology vol 83 no 4 pp 575ndash5831997
[30] C N L Macpherson ldquoThe epidemiology and public healthimportance of toxocariasis a zoonosis of global importancerdquoInternational Journal for Parasitology vol 43 pp 999ndash10082013
[31] U Ryan and S M Caccio ldquoZoonotic potential of GiardiardquoInternational Journal For Parasitology vol 43 pp 943ndash9562013
[32] M Genchi E Ferroglio G Traldi S Passera G MezzanoandCGenchi ldquoFecalizzazione ambientale e rischio parassitarionelle citta di Milano e Torinordquo Professione Veterinaria vol 41pp 15ndash17 2007
[33] F Riggio R Mannella G Ariti and S Perrucci ldquoIntestinaland lung parasites in owned dogs and cats from central ItalyrdquoVeterinary Parasitology vol 193 no 1ndash3 pp 78ndash84 2013
[34] LMugnaini R Papini G Gorini A Passantino VMerildi andF Mancianti ldquoPattern and predictive factors of endoparasitismin cats in central Italyrdquo Revue de Medecine Veterinaire vol 163no 2 pp 85ndash88 2012
10 BioMed Research International
[35] D Traversa ldquoPet roundworms and hookworms a continuingneed for global wormingrdquo Parasite amp Vectors vol 5 no 1 p 912012
[36] F Berrilli D di Cave C de Liberato A Franco PScaramozzino and P Orecchia ldquoGenotype characterisation ofGiardia duodenalis isolates from domestic and farm animals bySSU-rRNA gene sequencingrdquo Veterinary Parasitology vol 122no 3 pp 193ndash199 2004
[37] P Bianciardi R Papini G Giuliani andG Cardini ldquoPrevalenceof Giardia antigen in stool samples from dogs and catsrdquo Revuede Medecine Veterinaire vol 155 no 8-9 pp 417ndash421 2004
[38] G Capelli A Frangipane di Regalbono R Iorio M PietrobelliB Paoletti and A Giangaspero ldquoGiardia species and otherintestinal parasites in dogs in north-east and central ItalyrdquoVeterinary Record vol 159 no 13 pp 422ndash424 2006
[39] L Rinaldi M P Maurelli V Musella et al ldquoGiardia andCryptosporidium in canine faecal samples contaminating anurban areardquo Research in Veterinary Science vol 84 no 3 pp413ndash415 2008
[40] A V Scorza L R Ballweber S Tangtrongsup C Panuska andM R Lappin ldquoComparisons of mammalianGiardia duodenalisassemblages based on the 120573-giardin glutamate dehydrogenaseand triose phosphate isomerase genesrdquo Veterinary Parasitologyvol 189 no 2ndash4 pp 182ndash188 2012
[41] F D Uehlinger S J Greenwood J T McClure G B ConboyR OrsquoHandley and H W Barkema ldquoZoonotic potential ofGiardia duodenalis and Cryptosporidium spp and prevalenceof intestinal parasites in young dogs from different populationson Prince Edward Island Canadardquo Veterinary Parasitology vol196 no 3-4 pp 509ndash514 2013
[42] L R Ballweber L Xiao D D Bowman G Kahn and V ACama ldquoGiardiasis in dogs and cats update on epidemiology andpublic health significancerdquo Trends in Parasitology vol 26 no 4pp 180ndash189 2010
[43] D Jaros W Zygner S Jaros and HWedrychowicz ldquoDetectionof Giardia intestinalis assemblages A B and D in domestic catsfrom Warsaw Polandrdquo Polish Journal of Microbiology vol 60no 3 pp 259ndash263 2011
[44] R C AndersonNematode Parasites of Vertebrates Their Devel-opment and Transmission Cabi Publishing Wallingford UK2nd edition 2000
Submit your manuscripts athttpwwwhindawicom
Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014
Anatomy Research International
PeptidesInternational Journal of
Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014
Hindawi Publishing Corporation httpwwwhindawicom
International Journal of
Volume 2014
Zoology
Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014
Molecular Biology International
GenomicsInternational Journal of
Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014
The Scientific World JournalHindawi Publishing Corporation httpwwwhindawicom Volume 2014
Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014
BioinformaticsAdvances in
Marine BiologyJournal of
Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014
Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014
Signal TransductionJournal of
Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014
BioMed Research International
Evolutionary BiologyInternational Journal of
Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014
Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014
Biochemistry Research International
ArchaeaHindawi Publishing Corporationhttpwwwhindawicom Volume 2014
Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014
Genetics Research International
Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014
Advances in
Virolog y
Hindawi Publishing Corporationhttpwwwhindawicom
Nucleic AcidsJournal of
Volume 2014
Stem CellsInternational
Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014
Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014
Enzyme Research
Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014
International Journal of
Microbiology
BioMed Research International 9
[2] S Katagiri and T C G Oliveira-Sequeira ldquoPrevalence of dogintestinal parasites and risk perception of zoonotic infectionby dog owners in Sao Paulo State Brazilrdquo Zoonoses and PublicHealth vol 55 no 8ndash10 pp 406ndash413 2008
[3] S E Little E M Johnson D Lewis et al ldquoPrevalence ofintestinal parasites in pet dogs in the United Statesrdquo VeterinaryParasitology vol 166 no 1-2 pp 144ndash152 2009
[4] D Barutzki andR Schaper ldquoResults of parasitological examina-tions of faecal samples from cats and dogs in Germany between2003 and 2010rdquo Parasitology Research vol 109 no 1 pp S45ndashS60 2011
[5] N Itoh H Ikegami M Takagi et al ldquoPrevalence of intestinalparasites in private-household cats in Japanrdquo Journal of FelineMedical Surgery vol 14 no 6 pp 436ndash439 2012
[6] M C Gates and T J Nolan ldquoEfficacy of heartworm pre-ventatives against ascarids and hookworms in client-owneddogs a retrospective case control studyrdquo Journal of VeterinaryPharmacology andTherapeutics vol 34 no 2 pp 116ndash119 2011
[7] M C Gates and T J Nolan ldquoEndoparasite prevalence andrecurrence across different age groups of dogs and catsrdquoVeterinary Parasitology vol 166 no 1-2 pp 153ndash158 2009
[8] F S Ferreira P Pereira-Baltasar R Parreira et al ldquoIntestinalparasites in dogs and cats from the district of Evora PortugalrdquoVeterinary Parasitology vol 179 no 1ndash3 pp 242ndash245 2011
[9] C Epe G Rehkter T Schnieder L Lorentzen and L Kreien-brock ldquoGiardia in symptomatic dogs and cats in Europe-Resultsof a European studyrdquo Veterinary Parasitology vol 173 no 1-2pp 32ndash38 2010
[10] D Joffe D van Niekerk F Gagne J Gilleard S Kutz and RLobingier ldquoThe prevalence of intestinal parasites in dogs andcats in Calgary ABrdquo Canadian Veterinary Journal vol 52 no12 pp 1323ndash1328 2011
[11] T M Savilla J E Joy J D May and C C SomervilleldquoPrevalence of dog intestinal nematode parasites in southcentral West Virginia USArdquo Veterinary Parasitology vol 178no 1-2 pp 115ndash120 2011
[12] E Claerebout S Casaert A-C Dalemans et al ldquoGiardiaand other intestinal parasites in different dog populations inNorthern BelgiumrdquoVeterinary Parasitology vol 161 no 1-2 pp41ndash46 2009
[13] P A M Overgaauw L van Zutphen D Hoek et al ldquoZoonoticparasites in fecal samples and fur from dogs and cats in TheNetherlandsrdquo Veterinary Parasitology vol 163 no 1-2 pp 115ndash122 2009
[14] M C Gates and T J Nolan ldquoRisk factors for endoparasitismin dogs retrospective case-control study of 6578 veterinaryteaching hospital casesrdquo Journal of Small Animal Practice vol50 no 12 pp 636ndash640 2009
[15] A Nareaho J Puomio K Saarinen P Jokelainen T Juseliusand A Sukura ldquoFeline intestinal parasites in Finland preva-lence risk factors and anthelmintic treatment practicesrdquo Journalof Feline Medicine and Surgery vol 14 no 6 pp 378ndash383 2012
[16] L Polley and R C A Thompson ldquoParasite zoonoses and cli-mate change molecular tools for tracking shifting boundariesrdquoTrends in Parasitology vol 25 no 6 pp 285ndash291 2009
[17] E J Jenkins J M Schurer and K M Gesy ldquoOld problems on anew playing field helminth zoonoses transmitted among dogswildlife and people in a changing northern climaterdquoVeterinaryParasitology vol 182 no 1 pp 54ndash69 2011
[18] P N Acha and B Szyfres Zoonoses et Maladies TransmissiblesCommunes a lrsquohomme et Aux animaux Office International desEpizooties Paris France 1989
[19] M Fisher ldquoToxocara cati an underestimated zoonotic agentrdquoTrends in Parasitology vol 19 no 4 pp 167ndash170 2003
[20] Y Masuda T Kishimoto H Ito and M Tsuji ldquoVisceral larvamigrans caused by Trichuris vulpis presenting as a pulmonarymassrdquoThorax vol 42 no 12 pp 990ndash991 1987
[21] J J Dunn S T Columbus W E Aldeen M Davis and K CCarroll ldquoTrichuris vulpis recovered from a patient with chronicdiarrhea and five dogsrdquo Journal of Clinical Microbiology vol 40no 7 pp 2703ndash2704 2002
[22] M Papazahariadou A Founta E Papadopoulos SChliounakis K Antoniadou-Sotiriadou and Y TheodoridesldquoGastrointestinal parasites of shepherd and hunting dogs in theSerres Prefecture Northern Greecerdquo Veterinary Parasitologyvol 148 no 2 pp 170ndash173 2007
[23] C Martınez-Carrasco E Berriatua M Garijo J Martınez FD Alonso and R Ruiz De Ybanez ldquoEpidemiological study ofnon-systemic parasitism in dogs in southeast MediterraneanSpain assessed by coprological and post-mortem examinationrdquoZoonoses and Public Health vol 54 no 5 pp 195ndash203 2007
[24] S Leonhard K Pfister P Beelitz C Wielinga and R C AThompson ldquoThe molecular characterisation of Giardia fromdogs in southern Germanyrdquo Veterinary Parasitology vol 150no 1-2 pp 33ndash38 2007
[25] C Genchi G Gili and R Maraschin ldquoIndagine sullrsquoincidenzadelle elmintiasi intestinali del cane in alcune zone della Lom-bardiardquo La Clinica Veterinaria vol 97 no 6 pp 178ndash186 1974
[26] E Spada D Proverbio A Della Pepa et al ldquoPrevalence offaecal-borne parasites in colony stray cats in northern ItalyrdquoJournal of Feline Medicine and Surgery vol 15 no 8 pp 672ndash677 2013
[27] R M Hopkins B P Meloni D M Groth J D WetherallJ A Reynoldson and R C A Thompson ldquoRibosomal RNAsequencing reveals differences between the genotypes of Giar-dia isolates recovered from humans and dogs living in the samelocalityrdquo Journal of Parasitology vol 83 no 1 pp 44ndash51 1997
[28] C Read J Walters I D Robertson and R C A ThompsonldquoCorrelation between genotype of Giardia duodenalis anddiarrhoeardquo International Journal for Parasitology vol 32 no 2pp 229ndash231 2002
[29] A O Bush K D Lafferty J M Lotz and A W ShostakldquoParasitology meets ecology on its own terms Margolis et alrevisitedrdquo Journal of Parasitology vol 83 no 4 pp 575ndash5831997
[30] C N L Macpherson ldquoThe epidemiology and public healthimportance of toxocariasis a zoonosis of global importancerdquoInternational Journal for Parasitology vol 43 pp 999ndash10082013
[31] U Ryan and S M Caccio ldquoZoonotic potential of GiardiardquoInternational Journal For Parasitology vol 43 pp 943ndash9562013
[32] M Genchi E Ferroglio G Traldi S Passera G MezzanoandCGenchi ldquoFecalizzazione ambientale e rischio parassitarionelle citta di Milano e Torinordquo Professione Veterinaria vol 41pp 15ndash17 2007
[33] F Riggio R Mannella G Ariti and S Perrucci ldquoIntestinaland lung parasites in owned dogs and cats from central ItalyrdquoVeterinary Parasitology vol 193 no 1ndash3 pp 78ndash84 2013
[34] LMugnaini R Papini G Gorini A Passantino VMerildi andF Mancianti ldquoPattern and predictive factors of endoparasitismin cats in central Italyrdquo Revue de Medecine Veterinaire vol 163no 2 pp 85ndash88 2012
10 BioMed Research International
[35] D Traversa ldquoPet roundworms and hookworms a continuingneed for global wormingrdquo Parasite amp Vectors vol 5 no 1 p 912012
[36] F Berrilli D di Cave C de Liberato A Franco PScaramozzino and P Orecchia ldquoGenotype characterisation ofGiardia duodenalis isolates from domestic and farm animals bySSU-rRNA gene sequencingrdquo Veterinary Parasitology vol 122no 3 pp 193ndash199 2004
[37] P Bianciardi R Papini G Giuliani andG Cardini ldquoPrevalenceof Giardia antigen in stool samples from dogs and catsrdquo Revuede Medecine Veterinaire vol 155 no 8-9 pp 417ndash421 2004
[38] G Capelli A Frangipane di Regalbono R Iorio M PietrobelliB Paoletti and A Giangaspero ldquoGiardia species and otherintestinal parasites in dogs in north-east and central ItalyrdquoVeterinary Record vol 159 no 13 pp 422ndash424 2006
[39] L Rinaldi M P Maurelli V Musella et al ldquoGiardia andCryptosporidium in canine faecal samples contaminating anurban areardquo Research in Veterinary Science vol 84 no 3 pp413ndash415 2008
[40] A V Scorza L R Ballweber S Tangtrongsup C Panuska andM R Lappin ldquoComparisons of mammalianGiardia duodenalisassemblages based on the 120573-giardin glutamate dehydrogenaseand triose phosphate isomerase genesrdquo Veterinary Parasitologyvol 189 no 2ndash4 pp 182ndash188 2012
[41] F D Uehlinger S J Greenwood J T McClure G B ConboyR OrsquoHandley and H W Barkema ldquoZoonotic potential ofGiardia duodenalis and Cryptosporidium spp and prevalenceof intestinal parasites in young dogs from different populationson Prince Edward Island Canadardquo Veterinary Parasitology vol196 no 3-4 pp 509ndash514 2013
[42] L R Ballweber L Xiao D D Bowman G Kahn and V ACama ldquoGiardiasis in dogs and cats update on epidemiology andpublic health significancerdquo Trends in Parasitology vol 26 no 4pp 180ndash189 2010
[43] D Jaros W Zygner S Jaros and HWedrychowicz ldquoDetectionof Giardia intestinalis assemblages A B and D in domestic catsfrom Warsaw Polandrdquo Polish Journal of Microbiology vol 60no 3 pp 259ndash263 2011
[44] R C AndersonNematode Parasites of Vertebrates Their Devel-opment and Transmission Cabi Publishing Wallingford UK2nd edition 2000
Submit your manuscripts athttpwwwhindawicom
Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014
Anatomy Research International
PeptidesInternational Journal of
Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014
Hindawi Publishing Corporation httpwwwhindawicom
International Journal of
Volume 2014
Zoology
Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014
Molecular Biology International
GenomicsInternational Journal of
Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014
The Scientific World JournalHindawi Publishing Corporation httpwwwhindawicom Volume 2014
Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014
BioinformaticsAdvances in
Marine BiologyJournal of
Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014
Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014
Signal TransductionJournal of
Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014
BioMed Research International
Evolutionary BiologyInternational Journal of
Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014
Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014
Biochemistry Research International
ArchaeaHindawi Publishing Corporationhttpwwwhindawicom Volume 2014
Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014
Genetics Research International
Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014
Advances in
Virolog y
Hindawi Publishing Corporationhttpwwwhindawicom
Nucleic AcidsJournal of
Volume 2014
Stem CellsInternational
Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014
Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014
Enzyme Research
Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014
International Journal of
Microbiology
10 BioMed Research International
[35] D Traversa ldquoPet roundworms and hookworms a continuingneed for global wormingrdquo Parasite amp Vectors vol 5 no 1 p 912012
[36] F Berrilli D di Cave C de Liberato A Franco PScaramozzino and P Orecchia ldquoGenotype characterisation ofGiardia duodenalis isolates from domestic and farm animals bySSU-rRNA gene sequencingrdquo Veterinary Parasitology vol 122no 3 pp 193ndash199 2004
[37] P Bianciardi R Papini G Giuliani andG Cardini ldquoPrevalenceof Giardia antigen in stool samples from dogs and catsrdquo Revuede Medecine Veterinaire vol 155 no 8-9 pp 417ndash421 2004
[38] G Capelli A Frangipane di Regalbono R Iorio M PietrobelliB Paoletti and A Giangaspero ldquoGiardia species and otherintestinal parasites in dogs in north-east and central ItalyrdquoVeterinary Record vol 159 no 13 pp 422ndash424 2006
[39] L Rinaldi M P Maurelli V Musella et al ldquoGiardia andCryptosporidium in canine faecal samples contaminating anurban areardquo Research in Veterinary Science vol 84 no 3 pp413ndash415 2008
[40] A V Scorza L R Ballweber S Tangtrongsup C Panuska andM R Lappin ldquoComparisons of mammalianGiardia duodenalisassemblages based on the 120573-giardin glutamate dehydrogenaseand triose phosphate isomerase genesrdquo Veterinary Parasitologyvol 189 no 2ndash4 pp 182ndash188 2012
[41] F D Uehlinger S J Greenwood J T McClure G B ConboyR OrsquoHandley and H W Barkema ldquoZoonotic potential ofGiardia duodenalis and Cryptosporidium spp and prevalenceof intestinal parasites in young dogs from different populationson Prince Edward Island Canadardquo Veterinary Parasitology vol196 no 3-4 pp 509ndash514 2013
[42] L R Ballweber L Xiao D D Bowman G Kahn and V ACama ldquoGiardiasis in dogs and cats update on epidemiology andpublic health significancerdquo Trends in Parasitology vol 26 no 4pp 180ndash189 2010
[43] D Jaros W Zygner S Jaros and HWedrychowicz ldquoDetectionof Giardia intestinalis assemblages A B and D in domestic catsfrom Warsaw Polandrdquo Polish Journal of Microbiology vol 60no 3 pp 259ndash263 2011
[44] R C AndersonNematode Parasites of Vertebrates Their Devel-opment and Transmission Cabi Publishing Wallingford UK2nd edition 2000
Submit your manuscripts athttpwwwhindawicom
Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014
Anatomy Research International
PeptidesInternational Journal of
Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014
Hindawi Publishing Corporation httpwwwhindawicom
International Journal of
Volume 2014
Zoology
Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014
Molecular Biology International
GenomicsInternational Journal of
Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014
The Scientific World JournalHindawi Publishing Corporation httpwwwhindawicom Volume 2014
Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014
BioinformaticsAdvances in
Marine BiologyJournal of
Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014
Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014
Signal TransductionJournal of
Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014
BioMed Research International
Evolutionary BiologyInternational Journal of
Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014
Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014
Biochemistry Research International
ArchaeaHindawi Publishing Corporationhttpwwwhindawicom Volume 2014
Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014
Genetics Research International
Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014
Advances in
Virolog y
Hindawi Publishing Corporationhttpwwwhindawicom
Nucleic AcidsJournal of
Volume 2014
Stem CellsInternational
Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014
Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014
Enzyme Research
Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014
International Journal of
Microbiology
Submit your manuscripts athttpwwwhindawicom
Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014
Anatomy Research International
PeptidesInternational Journal of
Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014
Hindawi Publishing Corporation httpwwwhindawicom
International Journal of
Volume 2014
Zoology
Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014
Molecular Biology International
GenomicsInternational Journal of
Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014
The Scientific World JournalHindawi Publishing Corporation httpwwwhindawicom Volume 2014
Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014
BioinformaticsAdvances in
Marine BiologyJournal of
Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014
Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014
Signal TransductionJournal of
Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014
BioMed Research International
Evolutionary BiologyInternational Journal of
Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014
Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014
Biochemistry Research International
ArchaeaHindawi Publishing Corporationhttpwwwhindawicom Volume 2014
Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014
Genetics Research International
Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014
Advances in
Virolog y
Hindawi Publishing Corporationhttpwwwhindawicom
Nucleic AcidsJournal of
Volume 2014
Stem CellsInternational
Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014
Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014
Enzyme Research
Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014
International Journal of
Microbiology