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Soil-Transmitted Helminthiasis in indigenous communities of the southern border of Amazonian Ecuador: Is
chemoprophylaxis enough?
Journal: BMJ Open
Manuscript ID bmjopen-2016-013626
Article Type: Research
Date Submitted by the Author: 28-Jul-2016
Complete List of Authors: Romero-Sandoval, Natalia; Universidad Internacional del Ecuador, Facultad de Ciencias Médicas de la Salud y de la Vida; Grups de Reserca d'Amèrica i Africa LLatines, Ortiz Rico, Claudia; Universidad Autonoma de Barcelona, Unidad de Bioestadística; Grups de Recerca d’Amèrica i Àfrica Llatines – GRAAL Sánchez-Pérez, Hector; El Colegio de la Frontera Sur - ECOSUR; Grups de Recerca d’Amèrica i Àfrica Llatines – GRAAL Valdivieso, Daniel; Universidad Internacional del Ecuador, Facultad de Ciencias Médicas de la Salud y de la Vida Sandoval, Carlos; Fundación Ecuatoriana para la Investigación en Salud - FEPIS, Parasitología Pástor, Jacob; Instituto Geografico Militar Martin Mateo, Miguel; Universidad Autónoma de Barcelona, Departamento de Bioestadística; Grups de Recerca d’Amèrica i Àfrica Llatines – GRAAL
<b>Primary Subject Heading</b>:
Public health
Secondary Subject Heading: Epidemiology, Infectious diseases, General practice / Family practice
Keywords: Epidemiology < TROPICAL MEDICINE, helminths, indigenous population, chemoprophylaxis, Ecuador
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Soil-Transmitted Helminthiasis in indigenous communities of the southern border of
Amazonian Ecuador: Is chemoprophylaxis enough?
Natalia Romero-Sandoval PhD1,2* Claudia Ortiz-Rico MPH2,3 Héctor Javier Sánchez-
Pérez PhD2,4 Daniel Valdivieso1 Carlos Sandoval5 Jacob Pástor6 Miguel Martín PhD2,3
1Facultad de Ciencias Médicas, de la Salud y la Vida, Universidad Internacional del
Ecuador, Quito, Ecuador
2 Grups de Recerca d’Amèrica i Àfrica Llatines – GRAAL, Barcelona, España
3 Unidad de Bioestadística y Epidemiología, Universidad Autónoma de Barcelona,
Barcelona, España
4 El Colegio de la Frontera Sur – ECOSUR, San Cristóbal de Las Casas, Chiapas,
México
5 Fundación Ecuatoriana para la Investigación en Salud - FEPIS, Quinindé, Ecuador
6Instituto Geográfico Militar, Quito, Ecuador
* Corresponding author
Facultad de Ciencias Médicas, de la Salud y la Vida, Universidad Internacional del
Ecuador, Quito, Ecuador
Av. Jorge Fernandez and Simon Bolivar, Quito, Ecuador. Zip Code: EC170113
E-mail: [email protected]
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Telephone number: + 593 2 2 985600
Keywords: helminths, rural population, indigenous population, chemoprophylaxis,
Ecuador
Word count: 2856
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Abstract
Background: Rural communities on the Amazonian southern border of Ecuador have
been the object of governmental social programs during the past nine years, addressing
diseases associated with poverty, such as soil-transmitted helminth infection. The aim of
this study was to explore the prevalence of geo-helminth infection and factors
associated with it –including having received chemoprophylaxis in the last month- in
those communities.
Methods: Cross sectional study, in two indigenous communities of the Amazonian
southern border of Ecuador. The data were analyzed at both household level and
individual level.
Results: At individual level, the prevalence found was 46.9% (95% CI 39.5-54.2), with
no differences in terms of gender, age, temporary migration movements, or previous
chemoprophylaxis. In 72.9% of households, one or more members were infected.
Receiving subsidies and overcrowding were associated to presence of helminths.
Conclusion: The prevalence found of soil-helminth infection remained high in spite of
recent chemoprophylaxis. Our study suggests that it is necessary to conduct studies
focusing on communities, and not simply on captive groups such as school-children,
with the object of proposing more suitable and effective strategies to control this
problem.
Strengths and limitations of this study
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• A cross-sectional study carried out in indigenous communities of extreme
poverty, during a community visit, shows the situation of geo helminths.
• Applied strategy called for 80% of the inhabitants and only one of every three
homes not found helminths.
• This study was conceived as an exercise in community participation, conceived
as a mechanism for more democracy and transformation of the health sector.
• This study is limited by the low participation rate of men of working age.
• This study is limited by the collection of a single stool sample and prevalence
could be underestimated.
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INTRODUCTION
Soil-transmitted helminthiasis is a neglected tropical disease, which particularly
affects low and medium-low income population groups. The social and health
consequences become evident through academic performance, nutritional status,
economic development and chronic infection.[1] Both Ascaris lumbricoides and
whipworm (Trichuris trichiura), are transmitted through food and water contaminated
by feces of infected individuals, while Ancylostoma duodenale (hookworm) is
transmitted by walking barefoot on contaminated soil, or by ingestion of larva. The
situation is particularly serious in populations with high rates of migration and mobility
within and between rural and urban communities, and hence these infections constitute
a serious public health problem in these kinds of communities.[2]
Since the announcement in 2001[3] of a commitment to eradicate soil-
transmitted helminthiasis in low transmission areas, and reduce morbidity in high
transmission areas, reports from various places around the world indicate that these
goals are not being met, despite the established chemoprophylactic models.[4]
Ecuador, a multi-ethnic, medium-low income country, initiated a process of
social and economic reform in 2007, which has been reflected, for example, in a rise of
122% in public health spending and in the proportion of the gross domestic product
during the period 2000-2011.[5]
Among the various social policies, we may cite the antipoverty conditional cash
transfer programs (human development subsidies, subsidies for school books, and for
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school uniforms), aimed to assist people in extreme poverty.[6] On the other hand,
Ecuador has had one of the highest rates of internal and external migration, including
inhabitants of the Amazonian area.[7]
In the Amazonian southern border area, object of the present study, 34% of
homes are considered to be of poor quality (bare earth floor, gaps in house walls, roof of
metal or palm leaves), 55% use water from a well, river or rainwater collection system,
only 22% are connected to a sewage network.[8] These communities, located some 45
km from the nearest urban area and nearest communication center, until five years ago
were only accessible via unpaved road, and residents could only get to health facilities
and administrative municipal offices via narrow tracks through the jungle.
In Ecuador there are no data on soil-transmitted helminthiasis prevalence, nor on
systematic coverage of prophylactic treatment or epidemiological surveillance;
however, according to official figures covering the whole country, all children aged
under five years ought to have received chemoprophylaxis in 2014.[9]
Seeking to increase visibility of health problems in population areas which are
so small that classical studies tend to conceal them, the GRAAL research group (“Grups
de Recerca d’Amèrica i Âfrica Llatines”) conducts studies on infectious/contagious
diseases focusing on vulnerable, and often high-risk, population groups, often invisible
in national level epidemiological analyses. This approach has been termed patchwork
studies.[10]
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In the present study in two indigenous communities of the Amazonian southern
border of Ecuador, we aimed to quantify the prevalence of soil-transmitted
helminthiasis at both household and individual levels, as well as its relationship with
chemotherapy received in the last month, among other variables of interest.
METHODS
In June 2015, a cross-sectional study was performed in two communities, once
agreement and consent of local authorities had been obtained, based on criteria of
convenience in a community assembly where local political and health personnel were
represented. Although no censuses were available for these communities, they are
estimated to have about 240 inhabitants, according to their leaders. Both communities
can be reached by road, and are situated around 10 hours travelling (540 km) from the
capital of Ecuador.
Figure 1 shows the rate of joint distribution of the proportion of households self-
identified as indigenous poverty measured by unsatisfied basic needs index in Ecuador.
The studied communities are located in the Amazon border and one of the two
Ecuadorian areas with more poverty among the indigenous population.[11]
Following the patchwork methodological scheme, which has been applied by
our research team to analyze health problems such as pulmonary tuberculosis and
sylvatic rabies,[12,13] we applied a questionnaire that was administered face-to-face to
identify dwellings and obtain household characteristics, including whether they boiled
the water used, overcrowding, whether they received any unconditional cash transfers
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(subsidy), functionally illiterate person and transportation system to the nearest health
unit. At individual level we recorded self-perceived presence of geohelminths in the last
month, whether they had received preventive chemotherapy (also in the last month,
since the communities had recently been visited by local health teams), and temporary
migratory movements. Age was categorized into three categories (2-5, 6-19, ≥20 years).
For children aged under eight years, the questions were answered by the mother or
guardian.
One fecal sample was collected from each participant. All samples (192) were
examined using direct observation, 178 samples by Kato-Katz technique, and 184 by
formol-ether concentration; in both the latter cases, missing data corresponds to samples
that were insufficient to permit their being assessed. A positive sample was defined by
the presence of at least one egg or larva being detected by any one of the three methods.
Direct observation and the Kato-Katz method were used to assess samples on the same
day on site, in the communities, with a mobile parasitological analysis laboratory
installed there. Kato-Katz technique was performed with a template of 41.7 mg, as
recommended by the WHO.[14] Samples were preserved in formol-ether and an
analysis of this concentrate was performed at a base laboratory.
In the cases of the Kato-Katz method and formol-ether concentrate analyses, the
result recorded was the highest value obtained after examining two aliquots. Eggs per
gram of feces (epg) were calculated using the helminths eggs counted for each parasite
species obtained from the Kato-Katz technique multiplied by a factor of 24, as
recommended by WHO for the template used. Egg counts as epg were utilized to
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classify the intensity of infection as slight, moderate or high respectively, as follows: for
A. lumbricoides 1-4999 epg, 5000 – 49999 epg, and >= 50000 epg; for T. trichuria 1-
999 epg, 1000 – 9999 epg, and >= 10000 epg.[15] We used frequencies, percentages;
mean, standard desviation, median and percentile for continuous variables. We estimate
global and stratified prevalence and 95% confidence intervals. In the case of cross
tabulations we used prevalence ratio (PR) and 95% confidence intervals, likelihood
ratio (LR) and p value ≤ 0.05. We calculated a linear association between age and
perception of parasites, and having received preventive chemotherapy.
RESULTS
The study included 59 households, and a total of 320 individual members. The
number of members per household ranged from 2 to 13 (average 5.4, median 5). At
least one functionally illiterate person was identified in 33.3% of the households
studied; 15.4% of the households had to travel by walking to get to the nearest health
facility, the remainder used ground-based public transport; 72.4% of households
reported that at least one member had expelled geohelminths in the last month. Fifty
nine households provided fecal samples (average number of members providing a
sample: 3.1; median, 3).
In 16 (27.1%) of the households which provided fecal samples, no geohelminths
were observed; in another 30 (50.8%) one or more members were infected, and in 13
(22.0%; 95% CI 12.1-32.8) all fecal samples were positive.
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Sanitary and/or socioeconomic deficiencies were observed in 49.2% of
households (bare earth floor, windows not covered, no wastewater disposal system, no
electricity, did not have their own supply of drinking water), and in 79.3% (23/29) of
these, at least one member was infected by geohelminths; in contrast, among
households with better conditions, 66.7% (20/30) presented one or more infected
members (PR 1.19; 95% CI 0.86-1.67).
Forty four (74.6%) households reported receiving one or more state subsidies.
Of them, 81.8% had infected members, compared to 46.7% (7/15) among households
not receiving any subsidies (PR 1.75; 95% CI 1.09-3.97).
Twenty nine (49.2%) of the households reported overcrowding (more than three
inhabitants per bedroom), of which 86.2% had infected members (PR 1.44; 95% CI
1.04-1.99) versus 60.0% (18/30). Among the 36 households declaring they did not boil
the water, 28 (77.8%; 95% CI 64.2-91.4) had geohelminths infection, whereas the
corresponding figure among households reporting they do boil water was 63.6% (95%
CI 53.3-73.8) (PR 1.22; 95% CI 0.88-1.88).
Of the 192 participants who provided fecal samples, 106 (55.2%) were females.
The mean age was 22.8 (SD 19.4) years, while P25 corresponded to 8 years, P50 to 14
years, and P75 to 38 years (range 76). The median ages for males and females were 10
and 18 years, respectively (p<0.05).
Positivity to the presence of soil-transmitted helminths was detected in 28.6% of
the 192 samples analyzed by direct observation; 39.9% by the Kato-Katz method, and
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31.5% by the formol-ether concentrate. It was possible to analyze 178 cases by both
direct observation and the Kato-Katz method, of which 105 were negative to both
(59%); 20 were negative according to direct observation but positive to Kato-Katz; two
were positive according to direct observation but negative to Kato-Katz, and 51 were
positive to both (28.9%). Determinations obtained by both direct observation and by
analysis of the formol-ether concentrate coincided in 184 cases: 119 were negative
(64.7%) and 45 (24.5%) positive to both; 13 were negative according to direct
observation but positive according to the formol-ether method, and 7 were positive by
direct observation but negative according to the formol-ether method.
A positive result in at least one of the three tests for soil-transmitted
helminthiasis was observed in 83 of the 177 samples where it was possible to perform
such determinations (46.9%; 95% CI 39.5-54.2). Among females the prevalence was
52.6%; (51/97; 95% CI 42.7-62.5) and among males was 40.0% (32/80; 95%CI 29.3-
50.7); prevalence ratio 1.31 (95% CI 0.9-1.8). In the 60/177 participants who declared
temporarily going away from their communities, geohelminthiasis was found in 51.7%
(95% CI 44.1-59.3), whereas among those who did not go away, the corresponding
figure was 44.4% (95% CI 37.3-52.0).
One hundred and twelve participants (58.3%; 95% CI 51.0-65.1) –without
significant differences by sex– declared the self-perceived presence of geohelminths in
the last month. Table 1 shows the distributions of the presence, both measured and self-
perceived, of soil-transmitted helminthiasis, by age groups. In the case of the measured
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presence of soil-transmitted helminthiasis, no differences were found in terms of age
groups (LR 1.53; p=0.47) (Table 1). In contrast, for the perceived presence of parasites,
differences were significant (LR 9.75; p<0.05), a linear association being found
between perception of parasites and age, with higher ages reporting a lower perception
(80.0% to 48.1%) (p<0.05).
Table 1. Measured and perceived prevalence of geohelminthiasis
Age group (years)
Presence of geohelminthiasis (measured)
Presence of geohelminthiasis in the last month (perceived )
n (%)
95% CI n
(%) 95% CI
2-5 15/29 24/30 51.7 34.5-69.0 80.0 63.3-93.3
6-19 39/80 51/85 48.8 37.5-58.8 60.0 49.4-70.6
≥20 40/68 37/77 58.8 47.1-70.6 48.1 36.4-59.7
In the group aged 2 to 5 years, having received preventive chemotherapy in the
last month was declared by 25/30 participants (83.3%); 56/85 (65.9%) in the group aged
6 to 19 years, and 30/77 (39.0%) in the group aged 20 years and over (LR 22.37
p<0.05). This association was also linear (p<0.05).
Of the 104 participants who declared having received preventive chemotherapy
in the last month and in whom the coproparasite assessment was performed, 46 (49.2%)
were positive to the presence of helminths, while this happened for 37/73 (50.7%) of
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those who had not received it (LR 0.72; p=>0.05); there were no differences by either
sex or age group.
The parasitic load of A. lumbricoides varied from 24 to 18792 epg, 50% having
408 epg or over. In the group aged 2-5 years the median intensity was 600 epg, in those
aged 6-19 it was 348, and in those aged 20 and over it was 384.
The intensity of infection among individuals aged 2-5 years was slight, among
those aged 6-19 years it was slight in 90% and moderate in 10%, while in those aged 20
or over it was slight in 86.4% and moderate in 13.6%. The parasitic load of T. trichuria
ranged from 24 to 1080 epg, with median 72 and levels by age group of 48, 72 and 60,
respectively. The most common level of intensity of infection, in all age groups, was
slight, with moderate levels being found in 2% of those aged 6 to 19 years.
DISCUSSION
Even though members of the two communities analyzed had received preventive
chemoprophylaxis one month before the study, 72.9% of households had at least one
person infected by soil-transmitted helminthiasis, and in 13% all members were
infected. Also we found a higher prevalence among households stating they did not boil
water, or presented overcrowding, as well as families receiving any kind of state
subsidy, thus indicating their worse sanitary conditions. This is an important aspect to
consider because our results show that preventive community health campaigns simply
aiming to reduce or avoid soil-transmitted helminthiasis, are not sufficient, and must be
accompanied by changes in sanitary conditions and poverty. In this sense, the lack of
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good water supplies and the inadequate basic sanitation observed during the fieldwork,
as well as a low participation of the communities themselves in basic sanitation
activities, could both be factors that impede the control of soil-transmitted helminth
infections.[16–18]
Additionally, the fact that receiving any kind of state subsidy or presenting
overcrowding were both associated to prevalence of infection at household level seems
to confirm that it is not enough to treat this problem as merely a medical one, and that it
is necessary improve the socioeconomic and sanitary conditions of population. At
individual level, the high prevalence found was not differentiated by gender, age group,
temporary migratory movement, nor by whether they had received chemoprophylaxis or
not.
With respect to the results obtained in this community-based study (global
prevalence of 46.9% in samples where it was possible to perform the three
determinations –direct observation, Kato-Katz method and analysis of the formol-ether
concentrate), there are few references with which we can compare, since the majority of
studies are conducted in “captive” populations, such as school-children.[19-21]
The prevalence found in this study is much higher than figures reported by four articles
available in the scientific literature that deal with the Ecuadorian situation –with an
average of 18.9%[22,23] –, which formed part of a meta-analysis based on all
publications related to prevalence of soil-transmitted helminth infection in South
American countries. Nevertheless, our overall prevalence figure is lower than that
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reported by a previous study carried out in groups of Shuar people (prevalence rate of
65%), using Kato-Katz method but without the antecedent of having received
chemoprophylaxis.[24]
We found a large discrepancy between the measured and perceived prevalence
of geohelminthiasis, particularly for children under 5 years of age, since in nearly 8 of
every ten, the mother or guardian who responded perceived the presence of parasites,
whereas our determinations halve this figure. This discrepancy could be explained by
the fact that the national program of preventive chemotherapy acted in these
communities four weeks before this study. On the other hand, the prevalence in those
aged over 19 years, who were also the least treated group, leads us to reflect that in
these communities, the adult population could constitute a reservoir for infection and re-
infection.[24]
In Ecuador, the epidemiological surveillance of soil-transmitted helminth
infections has not been considered either explicitly, nor as part of the group of neglected
infectious diseases, and the estimated prevalence of infection might be high,[25] but
currently the data are scarce or non-existent. However, the Ecuadorian state publishes
reports of its successful health campaigns for the control of neglected diseases such as
brucellosis, Chagas disease, urban rabies, Onchocerciasis, and publicizes the important
increase in the budget for the control of neglected tropical diseases.[26] Nevertheless,
the official figures themselves are indicative of the poor housing conditions, the high
proportion of indigenous population with limited access to health services and poor
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sanitation, all aspects that facilitate the continuance of these parasitic infections,
especially in rural areas.
The transmission rate of soil-helminths remains high in regions such as the
Amazonian southern border of Ecuador, in spite of the fact that in recent years Pan
American Health Organization member countries have celebrated regional conventions
addressing the intensification of control of these poverty-related diseases.[27] On the
other hand, the World Health Organization recommends that school-based deworming
programs include health hygiene education as a complementary measure, although the
sustainability and the long-term impact of such education in hygiene does not appear to
show encouraging results.[28]
These limitations in the control and epidemiological surveillance of helminthic
infections could be solved with a long-term, intersectoral multidisciplinary
program.[29]
Finally, two limitations should be taking into account when interpreting our
results. Given the age distribution of participants, the participation rate among working-
age males was very low, something which could be attributable to two aspects: to their
absence from the community due to work, and a tendency of people in this group to
refuse to provide fecal samples. The other limitation is that the collection of a single
stool sample probably means prevalence has been underestimated. Given the
environmental conditions and geographical isolation, as well as a lack of resources, it
was not possible to obtain more fecal samples.
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CONCLUSIONS
All inhabitants of the two participating communities may consider themselves to be at
risk of soil-transmitted helminth infection, despite their reporting having been
administered preventive chemotherapy during the month prior to the study. For this
reason, it is necessary to conduct holistic studies focusing on communities, and not
simply on captive groups such as school-children, with the object of proposing more
suitable and effective strategies to control such infections.
ACKNOWLEDGMENTS The authors gratefully acknowledge the contributions of
Lino Arisqueta, Lizeth Cifuentes, Nicole Mora-Bowen, Gabriela León and Paola Lecaro
to the field work of the study.
CONTRIBUTORS NRS, COR, MM wrote the statistical analysis plan, cleaned and
analyzed the data, and drafted and revised the paper. NRS, MM, CS JP and HSP
provided guidance on the data handling, contributed to the design of the analysis,
provided interpretation of data and revised the paper. COR, DV, CS, JP contributed to
interpretation of the data and revised the paper. NRS, JP, MM and HSP provided
guidance on the conception of the work, interpretation of the data and revised the paper
for content. All members have approved the final version of the manuscript.
FUNDING This work was supported by Universidad Internacional del Ecuador
Research Programme grant number I-EO-01-2014.
COMPETING INTERESTS None.
ETHICS APPROVAL The study protocol was approved by the Ethical Committee of
the Universidad Central del Ecuador, and by the Ecuador Ministry of Public Health.
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Each study participant gave their written informed consent, and in the case of children,
signed by their parents.
DATA SHARING STATEMENT No additional data available.
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22 Pullan RL, Smith JL, Jasrasaria R, Brooker SJ. Global numbers of infection and
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23 Cepon-Robins TJ, Liebert MA, Gildner TE, Urlacher SS, Colehour AM,
Snodgrass JJ, et al. Soil-transmitted helminth prevalence and infection intensity
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24 Nikolay B, Mwandawiro CS, Kihara JH, Okoyo C, Cano J, Mwanje MT, et al.
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Tropical Neglected Diseases in Ecuador in the Last 20 Years. PloS One.
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development. BMC Public Health. 2007;7(1):6.
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Figure 1. Poverty, indigenus and study area
297x210mm (299 x 299 DPI)
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STROBE Statement—checklist of items that should be included in reports of observational studies
Item
No
Recommendation Pg
Title and abstract 1 (a) Indicate the study’s design with a commonly used term in the title or the
abstract
3
(b) Provide in the abstract an informative and balanced summary of what was
done and what was found
3
Introduction
Background/rationale 2 Explain the scientific background and rationale for the investigation being
reported
5
Objectives 3 State specific objectives, including any prespecified hypotheses 7
Methods
Study design 4 Present key elements of study design early in the paper 7
Setting 5 Describe the setting, locations, and relevant dates, including periods of
recruitment, exposure, follow-up, and data collection
7
Participants 6 (a) Cohort study—Give the eligibility criteria, and the sources and methods of
selection of participants. Describe methods of follow-up
Case-control study—Give the eligibility criteria, and the sources and methods
of case ascertainment and control selection. Give the rationale for the choice
of cases and controls
Cross-sectional study—Give the eligibility criteria, and the sources and
methods of selection of participants
7
(b) Cohort study—For matched studies, give matching criteria and number of
exposed and unexposed
Case-control study—For matched studies, give matching criteria and the
number of controls per case
-
Variables 7 Clearly define all outcomes, exposures, predictors, potential confounders, and
effect modifiers. Give diagnostic criteria, if applicable
8
Data sources/
measurement
8* For each variable of interest, give sources of data and details of methods of
assessment (measurement). Describe comparability of assessment methods if
there is more than one group
8
Bias 9 Describe any efforts to address potential sources of bias 7
Study size 10 Explain how the study size was arrived at 7
Quantitative variables 11 Explain how quantitative variables were handled in the analyses. If applicable,
describe which groupings were chosen and why
7-8
Statistical methods 12 (a) Describe all statistical methods, including those used to control for
confounding
9
(b) Describe any methods used to examine subgroups and interactions 9
(c) Explain how missing data were addressed 9-
10
(d) Cohort study—If applicable, explain how loss to follow-up was addressed
Case-control study—If applicable, explain how matching of cases and
controls was addressed
Cross-sectional study—If applicable, describe analytical methods taking
account of sampling strategy
-
(e) Describe any sensitivity analyses -
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Results Pg
Participants 13* (a) Report numbers of individuals at each stage of study—eg numbers potentially
eligible, examined for eligibility, confirmed eligible, included in the study, completing
follow-up, and analysed
-
(b) Give reasons for non-participation at each stage -
(c) Consider use of a flow diagram -
Descriptive
data
14* (a) Give characteristics of study participants (eg demographic, clinical, social) and
information on exposures and potential confounders
9-10
(b) Indicate number of participants with missing data for each variable of interest 9-10
(c) Cohort study—Summarise follow-up time (eg, average and total amount) -
Outcome data 15* Cohort study—Report numbers of outcome events or summary measures over time -
Case-control study—Report numbers in each exposure category, or summary
measures of exposure
-
Cross-sectional study—Report numbers of outcome events or summary measures 9-10
Main results 16 (a) Give unadjusted estimates and, if applicable, confounder-adjusted estimates and
their precision (eg, 95% confidence interval). Make clear which confounders were
adjusted for and why they were included
9-12
(b) Report category boundaries when continuous variables were categorized 8
(c) If relevant, consider translating estimates of relative risk into absolute risk for a
meaningful time period
-
Other analyses 17 Report other analyses done—eg analyses of subgroups and interactions, and
sensitivity analyses
-
Discussion
Key results 18 Summarise key results with reference to study objectives 13
Limitations 19 Discuss limitations of the study, taking into account sources of potential bias or
imprecision. Discuss both direction and magnitude of any potential bias
14,16
Interpretation 20 Give a cautious overall interpretation of results considering objectives, limitations,
multiplicity of analyses, results from similar studies, and other relevant evidence
13-
16
Generalisability 21 Discuss the generalisability (external validity) of the study results 15
Other information
Funding 22 Give the source of funding and the role of the funders for the present study and, if
applicable, for the original study on which the present article is based
17
*Give information separately for cases and controls in case-control studies and, if applicable, for exposed and
unexposed groups in cohort and cross-sectional studies.
Note: An Explanation and Elaboration article discusses each checklist item and gives methodological background and
published examples of transparent reporting. The STROBE checklist is best used in conjunction with this article (freely
available on the Web sites of PLoS Medicine at http://www.plosmedicine.org/, Annals of Internal Medicine at
http://www.annals.org/, and Epidemiology at http://www.epidem.com/). Information on the STROBE Initiative is
available at www.strobe-statement.org.
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Soil-Transmitted Helminthiasis in indigenous groups. A community cross-sectional study in the southern border of
Amazonian Ecuador
Journal: BMJ Open
Manuscript ID bmjopen-2016-013626.R1
Article Type: Research
Date Submitted by the Author: 03-Nov-2016
Complete List of Authors: Romero-Sandoval, Natalia; Universidad Internacional del Ecuador, Facultad de Ciencias Médicas de la Salud y de la Vida; Grups de Reserca d'Amèrica i Africa LLatines, Ortiz Rico, Claudia; Universidad Autonoma de Barcelona, Unidad de Bioestadística; Grups de Recerca d’Amèrica i Àfrica Llatines – GRAAL Sánchez-Pérez, Hector; El Colegio de la Frontera Sur - ECOSUR; Grups de Recerca d’Amèrica i Àfrica Llatines – GRAAL Valdivieso, Daniel; Universidad Internacional del Ecuador, Facultad de Ciencias Médicas de la Salud y de la Vida Sandoval, Carlos; Fundación Ecuatoriana para la Investigación en Salud - FEPIS, Parasitología Pástor, Jacob; Instituto Geografico Militar Martin Mateo, Miguel; Universidad Autónoma de Barcelona, Departamento de Bioestadística; Grups de Recerca d’Amèrica i Àfrica Llatines – GRAAL
<b>Primary Subject Heading</b>:
Public health
Secondary Subject Heading: Epidemiology, Infectious diseases, General practice / Family practice
Keywords: Epidemiology < TROPICAL MEDICINE, helminths, indigenous population, chemoprophylaxis, Ecuador
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Soil-Transmitted Helminthiasis in indigenous groups. A community cross-sectional
study in the southern border of Amazonian Ecuador.
Natalia Romero-Sandoval PhD1,2* Claudia Ortiz-Rico MPH2,3 Héctor Javier Sánchez-
Pérez PhD2,4 Daniel Valdivieso1 Carlos Sandoval5 Jacob Pástor6 Miguel Martín PhD2,3
1Facultad de Ciencias Médicas, de la Salud y la Vida, Universidad Internacional del
Ecuador, Quito, Ecuador
2 Grups de Recerca d’Amèrica i Àfrica Llatines – GRAAL, Barcelona, España
3 Unidad de Bioestadística y Epidemiología, Universidad Autónoma de Barcelona,
Barcelona, España
4 El Colegio de la Frontera Sur – ECOSUR, San Cristóbal de Las Casas, Chiapas,
México
5 Fundación Ecuatoriana para la Investigación en Salud - FEPIS, Quinindé, Ecuador
6Instituto Geográfico Militar, Quito, Ecuador
* Corresponding author
Facultad de Ciencias Médicas, de la Salud y la Vida, Universidad Internacional del
Ecuador, Quito, Ecuador
Av. Jorge Fernandez and Simon Bolivar, Quito, Ecuador. Zip Code: EC170113
E-mail: [email protected]
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Telephone number: + 593 2 2 985600
Keywords: helminths, rural population, indigenous population, chemoprophylaxis,
Ecuador
Word count: 2935
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Abstract
Background: Rural communities in the Amazonian southern border of Ecuador have
benefited from governmental social programs during the past nine years, which have
been addressing diseases associated with poverty, such as soil-transmitted helminth
infection. The aim of this study was to explore the prevalence of geo-helminth infection
and several factors associated with it in those communities.
Methods: Cross sectional study in two indigenous communities of the Amazonian
southern border of Ecuador. The data were analyzed at both household and individual
level.
Results: At individual level, the prevalence of geo-helminthes reached a 46.9% (95% CI
39.5-54.2), with no differences in terms of gender, age, temporary migration
movements, or previous chemoprophylaxis. In 72.9% of the households, one or more
members were infected. Receiving subsidies and overcrowding were associated to
presence of helminths.
Conclusion: The prevalence found of soil-helminth infection remained high. Our study
suggests that it is necessary to conduct studies focusing on communities, and not simply
on captive groups such as school-children, with the object of proposing more suitable
and effective strategies to control this problem.
Strengths and limitations of this study
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• A cross-sectional study carried out in indigenous communities of extreme
poverty, shows the situation of geo helminths.
• Applied strategy called for 80% of the inhabitants and only one of every three
homes not found helminths.
• This study constituted an exercise in community participation, conceived as a
mechanism for achieving greater democracy.
• This study is limited by the low participation rate of men of working age.
• This study is constrained by the collection of a single stool sample and
prevalence could be underestimated.
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INTRODUCTION
Soil-transmitted helminthiasis is a neglected tropical disease, which particularly
affects low and medium-low income population groups. The social and health
consequences become evident through academic performance, nutritional status,
economic development and chronic infection.[1] Both Ascaris lumbricoides and
whipworm (Trichuris trichiura), are transmitted through food and water contaminated
by feces of infected individuals, while Ancylostoma duodenale (hookworm) is
transmitted by walking barefoot on contaminated soil, or by ingestion of larva.[2]
The situation is particularly serious in populations with high rates of migration
and mobility within and between rural and urban communities, and hence these
infections and hence these infections continue transmitting and spreading.[3]
Since the announcement in 2001[4] of a commitment to eliminate soil-
transmitted helminthiasis in low transmission areas, and reduce morbidity in high
transmission areas, reports from various places around the world indicate that these
goals are not being met, despite the established chemoprophylactic models.[5]
Ecuador, a multi-ethnic, medium-low income country, initiated a process of
social and economic reform in 2007, which has been reflected, for example, in a rise of
122% in public health spending and in the proportion of the gross domestic product
during the period 2000-2011.[6]
Among the various social policies, we may cite the antipoverty conditional cash
transfer programs (“human development subsidies”, for instance, subsidies for school
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books, and for school uniforms), aimed to assist people in extreme poverty.[7] On the
other hand, Ecuador has had one of the highest rates of internal and external migration,
including inhabitants of the Amazonian region.[8]
In the Amazonian southern border area, object of the present study, 34% of
dwellings are considered to be of poor quality (bare earth floor, gaps in house walls,
roof of metal or palm leaves), 55% use water from a well, river or rainwater collection
system, only 22% are connected to a sewage network.[9] These communities, located
approximately 45 km from the nearest urban area and nearest communication center,
until five years ago were only accessible via unpaved roads, and residents could only
get to health facilities and administrative municipal offices via narrow tracks through
the jungle.
In Ecuador there are no data on soil-transmitted helminthiasis prevalence, nor on
systematic coverage of prophylactic treatment or epidemiological surveillance;
however, according to official figures covering the whole country, all children aged
from two to five years ought to have received chemoprophylaxis in 2014.[10]
In an effort seeking to increase visibility of health problems in population areas
which are so small that classical studies tend to conceal them, the GRAAL research
group (“Grups de Recerca d’Amèrica i Âfrica Llatines”) conducts studies on
infectious/contagious diseases focusing on vulnerable, and often high-risk, population
groups, often invisible in national level epidemiological analyses. This approach has
been termed patchwork studies.[11]
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In the present study in two indigenous communities of the Amazonian southern
border of Ecuador, we aimed to quantify the prevalence of soil-transmitted
helminthiasis at both household and individual levels, as well as its relationship with
several variables of interest.
METHODS
In June 2015, a cross-sectional study was performed in two communities, once
agreement and consent of local authorities had been obtained, based on criteria of
convenience in a community assembly where local political and health personnel were
represented. Although no censuses were available for these communities, they are
estimated to have about 240 inhabitants, according to their leaders. Both communities
can be reached by road, and are situated around 10 hours journey (540 km) from the
capital of Ecuador, Quito.
Figure 1 shows the participating communities and its geographical location, as
well as the joint distribution of the proportion of households self-identified as
indigenous and categorized as poor based on a measured called unsatisfied basic needs
index. These communities are located in the Amazon border and one of the two
Ecuadorian areas with more poverty among the indigenous population.[12]
Following the patchwork methodological scheme, which has been applied by
our research team to analyze health problems such as pulmonary tuberculosis and
sylvatic rabies,[13,14] we applied a questionnaire that was administered face-to-face to
identify dwellings and obtain household characteristics, including presence or absence
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of water supply and sanitary toilets, whether households boil water for consumption,
overcrowding, whether they received any subsidy. At individual level we recorded
temporary migratory movements, self-perceived presence of geohelminths in the last
month and whether they had received preventive chemotherapy – something which
could only be ascertained for the last month, due to problems in the register of the
information about administration of chemoprophylaxis in the studied communities. The
medication (Albendazol 400 mg one dose) was provided by Ecuador Ministry of Public
Health. For children aged under eight years, the questions were answered by the mother
or guardian.
One direct fecal sample was collected from each participant. All samples (192)
were examined using direct observation, 178 samples by Kato-Katz technique, and 184
by formol-ether concentration; in both the latter cases, missing data corresponds to
samples that were insufficient to permit their being assessed. A positive sample was
defined by the presence of at least one egg or larva being detected by any one of the
three methods. Direct observation and the Kato-Katz method were used to assess
samples on the same day on site, in the communities, with a mobile parasitological
analysis laboratory installed there. Kato-Katz technique was performed with a template
of 41.7 mg, as recommended by the WHO.[15] Samples were preserved in formol-ether
and an analysis of this concentrate was performed at a base laboratory. All three
techniques have been used by other studies in Ecuador.[16,17]
In the cases of the Kato-Katz method and formol-ether concentrate analyses, the
result recorded was the highest value obtained after examining two aliquots. Eggs per
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gram of feces (epg) were calculated using the helminths eggs counted for each parasite
species obtained from the Kato-Katz technique multiplied by a factor of 24, as
recommended by WHO for the template used. Egg counts as epg were utilized to
classify the intensity of infection as slight, moderate or high respectively, as follows: for
A. lumbricoides 1-4999 epg, 5000 – 49999 epg, and >= 50000 epg; for T. trichuria 1-
999 epg, 1000 – 9999 epg, and >= 10000 epg.[18]
RESULTS
The study included 59 households, and a total of 320 individual members. The
number of members per household ranged from 2 to 13 (average 5.4, median 5). At
least one functionally illiterate person was identified in 33.3% of the households
studied; 15.4% of the households had to travel by walking to get to the nearest health
facility, the remainder used ground-based public transport; 72.4% of households
reported that at least one member had expelled geohelminths in the last month. Fifty
nine households provided fecal samples (average number of members providing a
sample: 3.1; median, 3).
In 16 (27.1%) of the households which provided fecal samples, no geohelminths
were observed; in another 30 (50.8%) one or more members were infected, and in 13
(22.0%; 95% CI 12.1-32.8) all fecal samples were positive.
All inhabitants use natural spring-water, which is piped to community tanks
without any type of treatment; nobody had toilets. Other sanitary and/or socioeconomic
deficiencies were observed in 49.2% of households (bare earth floor, windows not
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covered, no wastewater disposal system, no electricity, absence of own drinking water
supply), and in 79.3% (23/29) of these, at least one member was infected by
geohelminths; in a similar fashion, among households with better conditions, 66.7%
(20/30) presented one or more infected members (PR 1.19; 95% CI 0.86-1.67).
Forty four (74.6%) households reported receiving one or more state subsidies.
Of them, 81.8% had infected members, compared to 46.7% (7/15) among households
not receiving any subsidies (PR 1.75; 95% CI 1.09-3.97).
Twenty nine (49.2%) of the households reported overcrowding (more than three
inhabitants per bedroom), of which 86.2% had infected members (PR 1.44; 95% CI
1.04-1.99) versus 60.0% (18/30). Among the 36 households declaring they did not boil
the water, 28 (77.8%; 95% CI 64.2-91.4) had geohelminths infection, whereas the
corresponding figure among households reporting they do boil water was 63.6% (95%
CI 53.3-73.8) (PR 1.22; 95% CI 0.88-1.88).
Of the 192 participants who provided fecal samples, 106 (55.2%) were females.
The mean age was 22.8 (SD 19.4) years, while percentile 25 corresponded to 8 years,
percentile 50 to 14 years, and percentile 75 to 38 years (range 76). The median ages for
males and females were 10 and 18 years, respectively (p<0.05); 37% of working-age
men reported having to migrate for work-related reasons (hunting, agriculture, mine-
work), tending to be away for 8 to 15 days, or even more.
Positivity to the presence of soil-transmitted helminths was detected in 28.6% of
the 192 samples analyzed by direct observation; 39.9% by the Kato-Katz method, and
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31.5% by the formol-ether concentrate. It was possible to analyze 178 cases by both
direct observation and the Kato-Katz method, of which 105 were negative to both
(59%); 20 were negative according to direct observation but positive to Kato-Katz; two
were positive according to direct observation but negative to Kato-Katz, and 51 were
positive to both (28.9%). Determinations obtained by both direct observation and by
analysis of the formol-ether concentrate coincided in 184 cases: 119 were negative
(64.7%) and 45 (24.5%) positive to both; 13 were negative according to direct
observation but positive according to the formol-ether method, and 7 were positive by
direct observation but negative according to the formol-ether method.
A positive result in at least one of the three tests for soil-transmitted
helminthiasis was observed in 83 of the 177 samples where it was possible to perform
such determinations (46.9%; 95% CI 39.5-54.2). Among females the prevalence was
52.6%; (51/97; 95% CI 42.7-62.5) and among males was 40.0% (32/80; 95%CI 29.3-
50.7); prevalence ratio 1.31 (95% CI 0.9-1.8). In the 60/177 participants who declared
temporarily going away from their communities, geohelmintiasis was found in 51.7%
(95% CI 44.1-59.3), whereas among those who did not go away, the corresponding
figure was 44.4% (95% CI 37.3-52.0).
One hundred and twelve participants (58.3%; 95% CI 51.0-65.1) –without
significant differences by sex– declared the self-perceived presence of geohelminths in
the last month. Table 1 shows the distributions of the presence, both measured and self-
perceived, of soil-transmitted helminthiasis, by age groups. In the case of the measured
presence of soil-transmitted helminthiasis, no differences were found in terms of age
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groups (LR 1.53; p=0.47) (Table 1). In contrast, for the perceived presence of parasites,
differences were significant (LR 9.75; p<0.05), a linear association being found
between perception of parasites and age, with higher ages reporting a lower perception
(80.0% to 48.1%) (p<0.05).
Table 1. Measured and perceived prevalence of geohelminthiasis
Age group (years)
Presence of geohelminthiasis (measured)
Presence of geohelminthiasis in the last month (perceived )
n (%)
95% CI n (%)
95% CI
2-5 15/29 24/30 51.7 34.5-69.0 80.0 63.3-93.3
6-19 39/80 51/85 48.8 37.5-58.8 60.0 49.4-70.6
≥20 40/68 37/77 58.8 47.1-70.6 48.1 36.4-59.7
In the last month 57.8% reported having received preventive chemotherapy; in
the group aged 2 to 5 years, having received preventive chemotherapy in the last month
was declared by 25/30 participants (83.3%); 56/85 (65.9%) in the group aged 6 to 19
years, and 30/77 (39.0%) in the group aged 20 years and over (LR 22.37 p<0.05). This
association was also linear (p<0.05).
Of the 104 participants who declared having received preventive chemotherapy
in the last month and in whom the coproparasite assessment was performed, 46 (49.2%)
were positive to the presence of helminths, while this happened for 37/73 (50.7%) of
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those who had not received it (LR 0.72; p=>0.05); there were no differences by either
sex or age group.
The parasitic load of A. lumbricoides varied from 24 to 18792 epg, 50% having
408 epg or over. In the group aged 2-5 years the median intensity was 600 epg, in those
aged 6-19 it was 348, and in those aged 20 and over it was 384.
The intensity of infection among individuals aged 2-5 years was slight, among
those aged 6-19 years it was slight in 90% and moderate in 10%, while in those aged 20
or over it was slight in 86.4% and moderate in 13.6%. The parasitic load of T. trichuria
ranged from 24 to 1080 epg, with median 72 and levels by age group of 48, 72 and 60,
respectively. The most common level of intensity of infection, in all age groups, was
slight, with moderate levels being found in 2% of those aged 6 to 19 years.
DISCUSSION
In this study we found that 72.9% of households had at least one person infected
by soil-transmitted helminthiasis, and in 13% all members were infected. Also we found
a higher prevalence among households stating they did not boil water; or presented
overcrowding, as well as families receiving any kind of state subsidy, thus suggesting
their worse sanitary conditions and greater poverty.
In marginalized populations, lacking sanitary conditions, one form of treating
water for human consumption, in the home, is by boiling it, thus preventing its
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contamination through contact with unwashed hands, dust rising from the bare earth
floor, etc., even though the effectiveness of boiling may be questionable.[19]
This is an important aspect to consider because our results show that community
de-worming campaigns (57.8% received chemoprophylaxis in the last month) aiming to
reduce or avoid soil-transmitted helminthiasis, without health education, are not
sufficient, and must be accompanied by changes in sanitary conditions and poverty
reduction policies and actions. In this sense, the lack of good water supplies and the
inadequate basic sanitation observed during the fieldwork, as well as a low participation
of the communities themselves in basic sanitation activities, could both be factors that
impede the control of soil-transmitted helminth infections.[20–22]
Additionally, the fact that receiving any kind of state subsidy or presenting
overcrowding were both associated to prevalence of infection at household level seems
to confirm that it is not enough to treat this problem merely as a medical, and that it is
necessary to improve the socioeconomic and sanitary conditions of the population. At
individual level, the high prevalence found was not differentiated by gender, age group,
temporary migratory movement, nor by whether they had received chemoprophylaxis or
not, this latter aspect being seen as a reflection of the community's situation, and not
necessarily as an assessment of the efficacy of the chemoprophylaxis program of Public
Health Ministry.
With respect to the results obtained in this community-based study (global
prevalence of 46.9% in samples where it was possible to perform the three
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determinations –direct observation, Kato-Katz method and analysis of the formol-ether
concentrate), there are few references with which we can compare against, since the
majority of studies are conducted in “captive” populations, such as school-children.[23-
25]
The prevalence found in this study is much higher than figures reported by several
articles available in the scientific literature that deal with the Ecuadorian situation –with
an average prevalence of 18.9%[26,27], which formed part of a meta-analysis based on
all publications related to prevalence of soil-transmitted helminth infection in South
American countries. Nevertheless, our overall prevalence figure is lower than that
reported by a previous study carried out in groups of Shuar people (prevalence rate of
65%), using Kato-Katz method but without the antecedent of having received
chemoprophylaxis.[28]
We found a large discrepancy between the measured and perceived prevalence
of geohelminthiasis, particularly for children under 5 years of age, since nearly 8 of
every ten, the mother or guardian who responded perceived the presence of parasites,
whereas our findings halve this figure. This discrepancy could be explained by the fact
that the national program of preventive chemotherapy acted in these communities four
weeks before this study. On the other hand, the prevalence in those aged over 19 years,
who were also the least treated group, leads us to reflect that in these communities, the
adult population could constitute a reservoir for infection and re-infection.
In Ecuador, the epidemiological surveillance of soil-transmitted helminth
infections has not been considered either explicitly, nor as part of the group of neglected
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infectious diseases, and the estimated prevalence of infection might be high,[16] but
currently the data are scarce. On the other hand, the Ecuadorian state publishes reports
of its successful health campaigns for the control of neglected diseases such as
brucellosis, Chagas disease, urban rabies, Onchocerciasis, and publicizes the important
increase in the budget for the control of neglected tropical diseases.[29]
The transmission rate of soil-helminths remains high in regions such as the
Amazonian southern border of Ecuador, in spite of the fact that in recent years member
countries of the Pan American Health Organization have celebrated regional
conventions to address the intensification of control of these poverty-related
diseases.[30]
As a part of intensification of control, the World Health Organization
recommends that school-based deworming programs include health hygiene education
as a complementary measure, although the sustainability and the long-term impact of
such education in hygiene does not appear to show encouraging results. These
limitations in the control and epidemiological surveillance of helminthic infections
could be solved with a long-term, intersectoral multidisciplinary program.[31-32]
Finally, two limitations should be taken into account when interpreting our
results. Given the age distribution of participants, the participation rate among working-
age males was very low, something which could be attributable to two aspects: to their
absence from the community due to work, and a tendency of people in this group to
refuse to provide fecal samples. The other limitation is that the collection of a single
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stool sample probably means prevalence has been underestimated. Given the
environmental conditions and geographical isolation, as well as a lack of resources, it
was not possible to obtain more fecal samples.
CONCLUSIONS
All inhabitants of the two participating communities may consider themselves to be at
risk of soil-transmitted helminth infection, despite having reported being subjected to
the administration of preventive chemotherapy during the month prior to the study. For
this reason, it is necessary to conduct holistic studies focusing on communities, and not
simply on captive groups such as school-children, with the object of proposing more
suitable and effective strategies to control such infections.
ACKNOWLEDGMENTS The authors gratefully acknowledge the contributions of
Lino Arisqueta, Lizeth Cifuentes, Nicole Mora-Bowen, Gabriela León and Paola Lecaro
to the field work of the study.
CONTRIBUTORS NRS, COR, MM wrote the statistical analysis plan, cleaned and
analyzed the data, and drafted and revised the paper. NRS, MM, CS JP and HSP
provided guidance on the data handling, contributed to the design of the analysis,
provided interpretation of data and revised the paper. COR, DV, CS, JP contributed to
interpretation of the data and revised the paper. NRS, JP, MM and HSP provided
guidance on the conception of the work, interpretation of the data and revised the paper
for content. All members have approved the final version of the manuscript.
FUNDING This work was supported by Universidad Internacional del Ecuador
Research Programme (I-EO-01-2014).
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COMPETING INTERESTS None.
ETHICS APPROVAL The study protocol was approved by the Ethical Committee of
the Universidad Central del Ecuador, and by the Ecuador Ministry of Public Health.
Each study participant gave their written informed consent, and in the case of children,
signed by their parents.
DATA SHARING STATEMENT No additional data available.
REFERENCES
1. Addiss DG. Soil-transmitted helminthiasis: back to the original point. Lancet Infect Dis. 2015 Aug;15(8):871–2.
2. Ojha SC, Jaide C, Jinawath N, Rotjanapan P, Baral P. Geohelminths: public health significance. J Infect Dev Ctries. 2014 Jan;8(1):5–16.
3. Norman FF, Monge-Maillo B, Martínez-Pérez Á, Perez-Molina JA, López-Vélez R. Parasitic infections in travelers and immigrants: part II helminths and ectoparasites. Future Microbiol. 2015;10(1):87–99.
4. Prichard RK, Basáñez M-G, Boatin BA, McCarthy JS, García HH, Yang G-J, et al. A Research Agenda for Helminth Diseases of Humans: Intervention for Control and Elimination. Brooker S, editor. PLoS Negl Trop Dis. 2012 Apr 24;6(4):e1549.
5. Mehta RS, Rodriguez A, Chico M, Guadalupe I, Broncano N, Sandoval C, et al. Maternal geohelminth infections are associated with an increased susceptibility to geohelminth infection in children: a case-control study. PLoS Negl Trop Dis. 2012;6(7):e1753.
6. Malo-Serrano M, Malo-Corral N. Reforma de salud en Ecuador: nunca más el derecho a la salud como un privilegio. Rev Peru Med Exp Salud Publica. 2014 Oct;31(4):754–61.
7. García B, Junior V. Conditional cash transfer a mechanism for social inclusion in Ecuador: An Assessment of Bono de Desarrollo Humano / Programas de transferencias monetarias condicionadas, un mecanismo para la inclusión social en Ecuador: una evaluación del Bono de Desarrollo Humano. 2014 Sep 1 [cited 2016
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8. Mosquera GH. Repensar el cuidado a través de la migración internacional: mercado laboral, Estado y familias transnacionales en Ecuador*/Rethinking care through international migration: labour market, State and transnational families in Ecuador. Cuad Relac Laborales. 2012;30(1):139.
9. Instituto Nacional de Estadísticas y Censo. Censo de Población y Vivienda 2010 [Internet]. Available from: http://www.inec.gob.ec/cpv/
10. WHO | PCT databank [Internet]. [cited 2015 Nov 6]. Available from: http://www.who.int/neglected_diseases/preventive_chemotherapy/sth/en/
11. Sánchez-Pérez HJ, Horna–Campos O, Romero-Sandoval N, Consiglio E, Mateo MM. Pulmonary Tuberculosis in Latin America: Patchwork Studies Reveal Inequalities in Its Control–The Cases of Chiapas (Mexico), Chine (Ecuador) and Lima (Peru). 2013 [cited 2013 Sep 6]; Available from: http://cdn.intechopen.com/pdfs/43737/InTech-Pulmonary_tuberculosis_in_latin_america_patchwork_studies_reveal_inequalities_in_its_control_the_cases_of_chiapas_mexico_chine_ecuador_and_lima_peru_.pdf
12. Encuesta de Condiciones de Vida, Ecuador, 2014. Instituto Nacional de Estadísticas y Censo, Ecuador. [cited 2016 Jun 2]. Available from: http://www.ecuadorencifras.gob.ec/documentos/web-inec/ECV/ECV_2015/
13. Romero-Sandoval N, Escobar N, Utzet M, Feijoo-Cid M, Martin M. Sylvatic rabies and the perception of vampire bat activity in communities in the Ecuadorian Amazon. Cad Saúde Pública. 2014 Mar;30(3):669–74.
14. Ortiz-Rico C, Aldaz C, Sánchez HJ, Martin M, Romero-Sandoval N. Conformance contrast testing between rates of pulmonary tuberculosis in Ecuadorian border areas. Salud Publica Mex. 57(6).
15. Committee WE, others. Prevention and control of schistosomiasis and soil-transmitted helminthiasis. World Health Organ Tech Rep Ser. 2002;912:i.
16. Menzies SK, Rodriguez A, Chico M, Sandoval C, Broncano N, Guadalupe I, et al. Risk factors for soil-transmitted helminth infections during the first 3 years of life in the tropics; findings from a birth cohort. PLoS Negl Trop Dis. 2014 Feb;8(2):e2718.
17. Moncayo A-L, Vaca M, Oviedo G, Workman LJ, Chico ME, Platts-Mills T a. E, et al. Effects of geohelminth infection and age on the associations between allergen-
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specific IgE, skin test reactivity and wheeze: a case-control study. Clin Exp Allergy J Br Soc Allergy Clin Immunol. 2013 Jan;43(1):60–72.
18. Speich B, Ali SM, Ame SM, Albonico M, Utzinger J, Keiser J. Quality control in the diagnosis of Trichuris trichiura and Ascaris lumbricoides using the Kato-Katz technique: experience from three randomised controlled trials. Parasit Vectors. 2015;8:82.
19. Strunz EC, Addiss DG, Stocks ME, Ogden S, Utzinger J, Freeman MC. Water, sanitation, hygiene, and soil-transmitted helminth infection: a systematic review and meta-analysis. PLoS Med. 2014 Mar;11(3):e1001620.
20. Bain R, Cronk R, Wright J, Yang H, Slaymaker T, Bartram J. Fecal contamination of drinking-water in low- and middle-income countries: a systematic review and meta-analysis. PLoS Med. 2014 May;11(5):e1001644.
21. Gyorkos TW, Maheu-Giroux M, Blouin B, Casapia M. Impact of health education on soil-transmitted helminth infections in schoolchildren of the Peruvian Amazon: a cluster-randomized controlled trial. PLoS Negl Trop Dis. 2013;7(9):e2397.
22. Lo NC, Bogoch II, Blackburn BG, Raso G, N’Goran EK, Coulibaly JT, et al. Comparison of community-wide, integrated mass drug administration strategies for schistosomiasis and soil-transmitted helminthiasis: a cost-effectiveness modelling study. Lancet Glob Health. 2015;3(10):e629–e638.
23. Dana D, Mekonnen Z, Emana D, Ayana M, Getachew M, Workneh N, et al. Prevalence and intensity of soil-transmitted helminth infections among pre-school age children in 12 kindergartens in Jimma Town, southwest Ethiopia. Trans R Soc Trop Med Hyg. 2015 Mar;109(3):225–7.
24. Macchioni F, Segundo H, Gabrielli S, Totino V, Gonzales PR, Salazar E, et al. Dramatic decrease in prevalence of soil-transmitted helminths and new insights into intestinal protozoa in children living in the Chaco region, Bolivia. Am J Trop Med Hyg. 2015 Apr;92(4):794–6.
25. Chammartin F, Scholte RGC, Guimarães LH, Tanner M, Utzinger J, Vounatsou P. Soil-transmitted helminth infection in South America: a systematic review and geostatistical meta-analysis. Lancet Infect Dis. 2013 Jun;13(6):507–18.
26. Pullan RL, Smith JL, Jasrasaria R, Brooker SJ. Global numbers of infection and disease burden of soil transmitted helminth infections in 2010. Parasit Vectors. 2014;7:37.
27. Cepon-Robins TJ, Liebert MA, Gildner TE, Urlacher SS, Colehour AM, Snodgrass JJ, et al. Soil-transmitted helminth prevalence and infection intensity
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among geographically and economically distinct Shuar communities in the Ecuadorian Amazon. J Parasitol. 2014 Oct;100(5):598–607.
28. Nikolay B, Mwandawiro CS, Kihara JH, Okoyo C, Cano J, Mwanje MT, et al. Understanding Heterogeneity in the Impact of National Neglected Tropical Disease Control Programmes: Evidence from School-Based Deworming in Kenya. PLoS Negl Trop Dis. 2015 Sep;9(9):e0004108.
29. Cartelle Gestal M, Holban AM, Escalante S, Cevallos M. Epidemiology of Tropical Neglected Diseases in Ecuador in the Last 20 Years. PloS One. 2015;10(9):e0138311.
30. Thériault FL, Blouin B, Casapía M, Gyorkos TW. Sustaining a hygiene education intervention to prevent and control geohelminth infections at schools in the Peruvian Amazon. 2015 [cited 2016 Jun 15]; Available from: http://iris.paho.org/xmlui/handle/123456789/18385
31. Panic G, Duthaler U, Speich B, Keiser J. Repurposing drugs for the treatment and control of helminth infections. Int J Parasitol Drugs Drug Resist. 2014 Dec;4(3):185–200.
32. Gabrie, J. A., Rueda, M. M., Canales, M., Gyorkos, T. W., & Sanchez, A. L. School hygiene and deworming are key protective factors for reduced transmission of soil-transmitted helminths among schoolchildren in Honduras. Parasites & vectors. 2014;7(1):354.
Figure 1 Distribution of the proportion of households self-identified as indigenous and categorized as poor based on unsatisfied basic needs index* and communities participants.
*Unsatisfied basic needs index: Percentage of poor households self-identified as indigenous. That is, the number of households whose basic needs are either not accessible, or of poor quality. The UBN include quality of dwelling materials, access to electricity, kids attendance to school, among others.
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Figure 1 Distribution of the proportion of households self-identified as indigenous and categorized as poor based on unsatisfied basic needs* index and communities participants.
*Unsatisfied basic needs index: Percentage of poor households self-identified as indigenous. That is, the number of households whose basic needs are either not accessible, or of poor quality. The UBN include
quality of dwelling materials, access to electricity, kids attendance to school, among others.
297x210mm (299 x 299 DPI)
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STROBE Statement—checklist of items that should be included in reports of observational studies
Item
No
Recommendation Pg
Title and abstract 1 (a) Indicate the study’s design with a commonly used term in the title or the
abstract
3
(b) Provide in the abstract an informative and balanced summary of what was
done and what was found
3
Introduction
Background/rationale 2 Explain the scientific background and rationale for the investigation being
reported
5
Objectives 3 State specific objectives, including any prespecified hypotheses 7
Methods
Study design 4 Present key elements of study design early in the paper 7
Setting 5 Describe the setting, locations, and relevant dates, including periods of
recruitment, exposure, follow-up, and data collection
7
Participants 6 (a) Cohort study—Give the eligibility criteria, and the sources and methods of
selection of participants. Describe methods of follow-up
Case-control study—Give the eligibility criteria, and the sources and methods
of case ascertainment and control selection. Give the rationale for the choice
of cases and controls
Cross-sectional study—Give the eligibility criteria, and the sources and
methods of selection of participants
7
(b) Cohort study—For matched studies, give matching criteria and number of
exposed and unexposed
Case-control study—For matched studies, give matching criteria and the
number of controls per case
-
Variables 7 Clearly define all outcomes, exposures, predictors, potential confounders, and
effect modifiers. Give diagnostic criteria, if applicable
8
Data sources/
measurement
8* For each variable of interest, give sources of data and details of methods of
assessment (measurement). Describe comparability of assessment methods if
there is more than one group
8
Bias 9 Describe any efforts to address potential sources of bias 7
Study size 10 Explain how the study size was arrived at 7
Quantitative variables 11 Explain how quantitative variables were handled in the analyses. If applicable,
describe which groupings were chosen and why
7-8
Statistical methods 12 (a) Describe all statistical methods, including those used to control for
confounding
9
(b) Describe any methods used to examine subgroups and interactions 9
(c) Explain how missing data were addressed 9-
10
(d) Cohort study—If applicable, explain how loss to follow-up was addressed
Case-control study—If applicable, explain how matching of cases and
controls was addressed
Cross-sectional study—If applicable, describe analytical methods taking
account of sampling strategy
-
(e) Describe any sensitivity analyses -
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Results Pg
Participants 13* (a) Report numbers of individuals at each stage of study—eg numbers potentially
eligible, examined for eligibility, confirmed eligible, included in the study, completing
follow-up, and analysed
-
(b) Give reasons for non-participation at each stage -
(c) Consider use of a flow diagram -
Descriptive
data
14* (a) Give characteristics of study participants (eg demographic, clinical, social) and
information on exposures and potential confounders
9-10
(b) Indicate number of participants with missing data for each variable of interest 9-10
(c) Cohort study—Summarise follow-up time (eg, average and total amount) -
Outcome data 15* Cohort study—Report numbers of outcome events or summary measures over time -
Case-control study—Report numbers in each exposure category, or summary
measures of exposure
-
Cross-sectional study—Report numbers of outcome events or summary measures 9-10
Main results 16 (a) Give unadjusted estimates and, if applicable, confounder-adjusted estimates and
their precision (eg, 95% confidence interval). Make clear which confounders were
adjusted for and why they were included
9-12
(b) Report category boundaries when continuous variables were categorized 8
(c) If relevant, consider translating estimates of relative risk into absolute risk for a
meaningful time period
-
Other analyses 17 Report other analyses done—eg analyses of subgroups and interactions, and
sensitivity analyses
-
Discussion
Key results 18 Summarise key results with reference to study objectives 13
Limitations 19 Discuss limitations of the study, taking into account sources of potential bias or
imprecision. Discuss both direction and magnitude of any potential bias
14,16
Interpretation 20 Give a cautious overall interpretation of results considering objectives, limitations,
multiplicity of analyses, results from similar studies, and other relevant evidence
13-
16
Generalisability 21 Discuss the generalisability (external validity) of the study results 15
Other information
Funding 22 Give the source of funding and the role of the funders for the present study and, if
applicable, for the original study on which the present article is based
17
*Give information separately for cases and controls in case-control studies and, if applicable, for exposed and
unexposed groups in cohort and cross-sectional studies.
Note: An Explanation and Elaboration article discusses each checklist item and gives methodological background and
published examples of transparent reporting. The STROBE checklist is best used in conjunction with this article (freely
available on the Web sites of PLoS Medicine at http://www.plosmedicine.org/, Annals of Internal Medicine at
http://www.annals.org/, and Epidemiology at http://www.epidem.com/). Information on the STROBE Initiative is
available at www.strobe-statement.org.
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Soil-Transmitted Helminthiasis in indigenous groups. A community cross-sectional study in the Amazonian southern
border region of Ecuador
Journal: BMJ Open
Manuscript ID bmjopen-2016-013626.R2
Article Type: Research
Date Submitted by the Author: 30-Jan-2017
Complete List of Authors: Romero-Sandoval, Natalia; Universidad Internacional del Ecuador, Facultad de Ciencias Médicas de la Salud y de la Vida; Grups de Reserca d'Amèrica i Africa LLatines, GRAAL Ortiz Rico, Claudia; Universidad Autonoma de Barcelona, Unidad de Bioestadística; Grups de Recerca d’Amèrica i Àfrica Llatines – GRAAL Sánchez-Pérez, Hector; El Colegio de la Frontera Sur - ECOSUR; Grups de Recerca d’Amèrica i Àfrica Llatines – GRAAL Valdivieso, Daniel; Universidad Internacional del Ecuador, Facultad de Ciencias Médicas de la Salud y de la Vida Sandoval, Carlos; Fundación Ecuatoriana para la Investigación en Salud - FEPIS, Parasitología Pástor, Jacob; Instituto Geografico Militar Martin Mateo, Miguel; Universidad Autónoma de Barcelona, Departamento de Bioestadística; Grups de Recerca d’Amèrica i Àfrica Llatines – GRAAL
<b>Primary Subject Heading</b>:
Public health
Secondary Subject Heading: Epidemiology, Infectious diseases, General practice / Family practice
Keywords: Epidemiology < TROPICAL MEDICINE, helminths, indigenous population, chemoprophylaxis, Ecuador
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Soil-Transmitted Helminthiasis in indigenous groups. A community cross-sectional
study in the Amazonian southern border region of Ecuador.
Natalia Romero-Sandoval PhD1,2* Claudia Ortiz-Rico MPH2,3 Héctor Javier Sánchez-
Pérez PhD2,4 Daniel Valdivieso1 Carlos Sandoval5 Jacob Pástor6 Miguel Martín PhD2,3
1Facultad de Ciencias Médicas, de la Salud y la Vida, Universidad Internacional del
Ecuador, Quito, Ecuador
2 Grups de Recerca d’Amèrica i Àfrica Llatines – GRAAL, Barcelona, España
3 Unidad de Bioestadística y Epidemiología, Universidad Autónoma de Barcelona,
Barcelona, España
4 El Colegio de la Frontera Sur – ECOSUR, San Cristóbal de Las Casas, Chiapas,
México
5 Fundación Ecuatoriana para la Investigación en Salud - FEPIS, Quinindé, Ecuador
6Instituto Geográfico Militar, Quito, Ecuador
* Corresponding author
Facultad de Ciencias Médicas, de la Salud y la Vida, Universidad Internacional del
Ecuador, Quito, Ecuador
Av. Jorge Fernandez and Simon Bolivar, Quito, Ecuador. Zip Code: EC170113
E-mail: [email protected]
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Telephone number: + 593 2 2 985600
Keywords: helminths, rural population, indigenous population, chemoprophylaxis,
Ecuador
Word count: 2935
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Abstract
Background: Rural communities in the Amazonian southern border of Ecuador have
benefited from governmental social programs during the past nine years, which have
addressed, among others, diseases associated with poverty, such as soil-transmitted
helminth infection. The aim of this study was to explore the prevalence of geo-helminth
infection and several factors associated with it in those communities.
Methods: Cross sectional study in two indigenous communities of the Amazonian
southern border of Ecuador. The data were analyzed at both household and individual
levels.
Results: At individual level, the prevalence of geo-helminth infection reached 46.9%
(95% CI 39.5-54.2), with no differences in terms of gender, age, temporary migration
movements, or previous chemoprophylaxis. In 72.9% of the households, one or more
members were infected. Receiving subsidies and overcrowding were associated to
presence of helminths.
Conclusion: The prevalence found of geo-helminth infection was high. Our study
suggests that it is necessary to conduct studies focusing on communities, and not simply
on captive groups such as school-children, with the object of proposing more suitable
and effective strategies to control this problem.
Strengths and limitations of this study
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• A cross-sectional study carried out in indigenous communities of extreme
poverty, shows the situation of geo-helminth infection
• The strategy used involved 80% of the inhabitants and only one of every three
homes were free of geo-helminth infection.
• This study constituted an exercise in community participation, conceived as a
mechanism for achieving greater democracy.
• This study is limited by the low participation rate of men of working age.
• Collection of a single stool sample may mean that prevalence was
underestimated.
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INTRODUCTION
Soil-transmitted helminthiasis is a neglected tropical disease, which particularly
affects low and medium-low income population groups. The social and health
consequences become evident through academic performance, nutritional status,
economic development and chronic infection.[1] Both Ascaris lumbricoides and
whipworm (Trichuris trichiura), are transmitted through food and water contaminated
by feces of infected individuals, while Ancylostoma duodenale (hookworm) is
transmitted by walking barefoot on contaminated soil, or by ingestion of larva. [2]
The situation is particularly serious in populations with high rates of migration
and mobility within and between rural and urban communities, and hence these
infections continue to spread.[3]
Since the announcement in 2001[4] of a commitment to eliminate soil-
transmitted helminthiasis in low transmission areas, and reduce morbidity in high
transmission areas, reports from various places around the world indicate that these
goals are not being met, despite the established chemoprophylactic models.[5]
Ecuador, a multi-ethnic, medium-low income country, initiated a process of
social and economic reform in 2007, which has been reflected, for example, in a rise of
122% in public health spending and in the proportion of the gross domestic product
during the period 2000-2011.[6]
Among the various social policies, we may cite the antipoverty conditional cash
transfer programs (“human development subsidies”, for instance, subsidies for school
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books, and for school uniforms), aimed to assist people in extreme poverty.[7] On the
other hand, Ecuador has had one of the highest rates of internal and external migration,
including inhabitants of the Amazonian region.[8]
In the Amazonian southern border area, object of the present study, 34% of
dwellings are considered to be of poor quality (bare earth floor, gaps in house walls,
roof of metal or palm leaves), 55% use water from a well, river or rainwater collection
system, only 22% are connected to a sewage network.[9] These communities, located
approximately 45 km from the nearest urban area and nearest communication center,
until five years ago were only accessible via unpaved roads, and residents could only
get to health facilities and administrative municipal offices via narrow tracks through
the jungle.
In Ecuador there are no data on soil-transmitted helminthiasis prevalence, nor on
systematic coverage of prophylactic treatment or epidemiological surveillance;
however, according to official figures covering the whole country, all children aged
from two to five years ought to have received chemoprophylaxis in 2014.[10]
In an effort to increase visibility of health problems in population areas which
are so small that classical studies tend to conceal them, the GRAAL research group
(“Grups de Recerca d’Amèrica i Âfrica Llatines”) conducts studies on
infectious/contagious diseases focusing on vulnerable, and often high-risk, population
groups, often invisible in national level epidemiological analyses. This approach has
been termed patchwork studies.[11]
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In the present study in two indigenous communities of the Amazonian southern
border of Ecuador, we aimed to quantify the prevalence of soil-transmitted
helminthiasis at both household and individual levels, as well as its relationship with
several variables of interest.
METHODS
In June 2015, a cross-sectional study was performed in two communities, once
agreement and consent of local authorities had been obtained, based on criteria of
convenience in a community assembly where local political and health personnel were
represented. Although no censuses were available for these communities, they are
estimated to have about 240 inhabitants, according to their leaders. Both communities
can be reached by road, and are situated around 540 km (10 hours travelling time) from
the capital of Ecuador, Quito.
Figure 1 shows the participating communities and their geographical location, as
well as the joint distribution of the proportion of households self-identified as
indigenous and categorized as poor based on a measure known as the unsatisfied basic
needs index. These communities are located in the Amazon border which is one of the
two Ecuadorian areas with more poverty among the indigenous population.[12]
Following the patchwork methodological scheme, which has been applied by
our research team to analyze health problems such as pulmonary tuberculosis and
sylvatic rabies,[13,14] we administered a questionnaire (face-to-face) to identify
dwellings and obtain household characteristics, including presence or absence of water
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supply and sanitary toilets, whether households boil water for consumption,
overcrowding, whether they received any subsidy. At individual level we recorded
temporary migratory movements, self-perceived presence of geohelminths in the last
month and whether they had received preventive chemotherapy – something which
could only be ascertained for the last month, due to problems in the recording of
information about administration of chemoprophylaxis in the studied communities. The
medication (Albendazol 400 mg one dose) was provided by the Ecuador Ministry of
Public Health. For children aged under eight years, the questions were answered by the
mother or guardian.
One direct fecal sample was collected from each participant. All samples (192)
were examined using direct observation, 178 samples by Kato-Katz technique, and 184
by formol-ether concentration; in both the latter cases, missing data corresponds to
samples that were insufficient to permit their being assessed. A positive sample was
defined by the presence of at least one egg or larva being detected by any one of the
three methods. Direct observation and the Kato-Katz method were used to assess
samples on the same day on site, in the communities, with a mobile parasitological
analysis laboratory installed there. Kato-Katz technique was performed with a template
of 41.7 mg, as recommended by the WHO.[15] Samples were preserved in formol-ether
and an analysis of this concentrate was performed at a base laboratory. All three
techniques have been used by other studies in Ecuador.[16,17]
In the cases of the Kato-Katz method and formol-ether concentrate analyses, the
result recorded was the highest value obtained after examining two aliquots. Eggs per
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gram of feces (epg) were calculated using the helminths eggs counted for each parasite
species obtained from the Kato-Katz technique multiplied by a factor of 24, as
recommended by WHO for the template used. Egg counts as epg were utilized to
classify the intensity of infection as slight, moderate or high respectively, as follows: for
A. lumbricoides 1-4999 epg, 5000 – 49999 epg, and >= 50000 epg; for T. trichuria 1-
999 epg, 1000 – 9999 epg, and >= 10000 epg.[18]
RESULTS
The study included 59 households, and a total of 320 individual members. The
number of members per household ranged from 2 to 13 (average 5.4, median 5). At
least one functionally illiterate person was identified in 33.3% of the households
studied; 15.4% of the households had to travel by walking to get to the nearest health
facility, the remainder used ground-based public transport; 72.4% of households
reported that at least one member had expelled geohelminths in the last month. Fifty
nine households provided fecal samples (average number of members providing a
sample: 3.1; median, 3).
In 16 (27.1%) of the households which provided fecal samples, no geohelminths
were observed; in another 30 (50.8%) one or more members were infected, and in 13
(22.0%; 95% CI 12.1-32.8) all fecal samples were positive.
All inhabitants use natural spring-water, which is piped to community tanks
without any type of treatment; nobody had toilets. Other sanitary and/or socioeconomic
deficiencies were observed in 49.2% of households (bare earth floor, windows not
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covered, no wastewater disposal system, no electricity, absence of own drinking water
supply), and in 79.3% (23/29) of these, at least one member was infected by
geohelminths; in a similar fashion, among households with better conditions, 66.7%
(20/30) presented one or more infected members (PR 1.19; 95% CI 0.86-1.67).
Forty four (74.6%) households reported receiving one or more state subsidies.
Of them, 81.8% had infected members, compared to 46.7% (7/15) among households
not receiving any subsidies (PR 1.75; 95% CI 1.09-3.97).
Twenty nine (49.2%) of the households reported overcrowding (more than three
inhabitants per bedroom), of which 86.2% had infected members (PR 1.44; 95% CI
1.04-1.99) versus 60.0% (18/30). Among the 36 households declaring they did not boil
the water, 28 (77.8%; 95% CI 64.2-91.4) had geohelminths infection, whereas the
corresponding figure among households reporting they do boil water was 63.6% (95%
CI 53.3-73.8) (PR 1.22; 95% CI 0.88-1.88).
Of the 192 participants who provided fecal samples, 106 (55.2%) were females.
The mean age was 22.8 (SD 19.4) years, while percentile 25 corresponded to 8 years,
percentile 50 to 14 years, and percentile 75 to 38 years (range 76). The median ages for
males and females were 10 and 18 years, respectively (p<0.05); 37% of working-age
men reported having to migrate for work-related reasons (hunting, agriculture, mine-
work), tending to be away for 8 to 15 days, or even more.
Positivity to the presence of soil-transmitted helminths was detected in 28.6% of
the 192 samples analyzed by direct observation; 39.9% by the Kato-Katz method, and
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31.5% by the formol-ether concentrate. It was possible to analyze 178 cases by both
direct observation and the Kato-Katz method, of which 105 were negative to both
(59%); 20 were negative according to direct observation but positive to Kato-Katz; two
were positive according to direct observation but negative to Kato-Katz, and 51 were
positive to both (28.9%). Determinations obtained by both direct observation and by
analysis of the formol-ether concentrate coincided in 184 cases: 119 were negative
(64.7%) and 45 (24.5%) positive to both; 13 were negative according to direct
observation but positive according to the formol-ether method, and 7 were positive by
direct observation but negative according to the formol-ether method.
A positive result in at least one of the three tests for soil-transmitted
helminthiasis was observed in 83 of the 177 samples where it was possible to perform
such determinations (46.9%; 95% CI 39.5-54.2). Among females the prevalence was
52.6%; (51/97; 95% CI 42.7-62.5) and among males was 40.0% (32/80; 95%CI 29.3-
50.7); prevalence ratio 1.31 (95% CI 0.9-1.8). In the 60/177 participants who declared
temporarily going away from their communities, geohelminthiasis was found in 51.7%
(95% CI 44.1-59.3), whereas among those who did not go away, the corresponding
figure was 44.4% (95% CI 37.3-52.0).
One hundred and twelve participants (58.3%; 95% CI 51.0-65.1) –without
significant differences by sex– declared the self-perceived presence of geohelminths in
the last month. Table 1 shows the distributions of the presence, both measured and self-
perceived, of soil-transmitted helminthiasis, by age groups. In the case of the measured
presence of soil-transmitted helminthiasis, no differences were found in terms of age
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groups (LR 1.53; p=0.47) (Table 1). In contrast, for the perceived presence of parasites,
differences were significant (LR 9.75; p<0.05), a linear association being found
between perception of parasites and age, with older ages reporting a lower perception
(80.0% to 48.1%) (p<0.05).
Table 1. Measured and perceived prevalence of geohelminthiasis
Age group (years)
Presence of geohelminthiasis (measured)
Presence of geohelminthiasis in the last month (perceived )
N (%)
95% CI n (%)
95% CI
2-5 15/29 24/30 51.7 34.5-69.0 80.0 63.3-93.3 6-19 39/80 51/85 48.8 37.5-58.8 60.0 49.4-70.6 ≥20 40/68 37/77 58.8 47.1-70.6 48.1 36.4-59.7
In the last month 57.8% of the participants reported having received preventive
chemotherapy; in the group aged 2 to 5 years, having received preventive chemotherapy
in the last month was declared by 25/30 participants (83.3%); 56/85 (65.9%) in the
group aged 6 to 19 years, and 30/77 (39.0%) in the group aged 20 years and over (LR
22.37 p<0.05). This association was also linear (p<0.05).
Of the 104 participants who declared having received preventive chemotherapy
in the last month and in whom the coproparasite assessment was performed, 46 (49.2%)
were positive to the presence of helminths, while this happened for 37/73 (50.7%) of
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those who had not received it (LR 0.72; p=>0.05); there were no differences by either
sex or age group.
The parasitic load of A. lumbricoides varied from 24 to 18792 epg, 50% having
408 epg or over. In the group aged 2-5 years the median intensity was 600 epg, in those
aged 6-19 it was 348, and in those aged 20 and over it was 384.
The intensity of infection among individuals aged 2-5 years was slight, among
those aged 6-19 years it was slight in 90% and moderate in 10%, while in those aged 20
or over it was slight in 86.4% and moderate in 13.6%. The parasitic load of T. trichuria
ranged from 24 to 1080 epg, with median 72 and levels by age group of 48, 72 and 60,
respectively. The most common level of intensity of infection, in all age groups, was
slight, with moderate levels being found in 2% of those aged 6 to 19 years.
DISCUSSION
In this study we found that 72.9% of households had at least one person infected
by soil-transmitted helminthiasis, and in 13% all members were infected. Also we found
a higher prevalence among households stating they did not boil water; or presented
overcrowding, as well as families receiving any kind of state subsidy, thus suggesting
their worse sanitary conditions and greater poverty.
In marginalized populations, lacking sanitary conditions, one form of treating
water for human consumption, in the home, is by boiling it, thus preventing its
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contamination through contact with unwashed hands, dust rising from the bare earth
floor, etc., even though the effectiveness of boiling may be questionable.[19]
This is an important aspect to consider because our results show that community
de-worming campaigns (57.8% received chemoprophylaxis in the last month) aiming to
reduce or avoid soil-transmitted helminthiasis, without health education, are not
sufficient, and must be accompanied by changes in sanitary conditions and poverty
reduction policies and actions. In this sense, the lack of good water supplies and the
inadequate basic sanitation observed during the fieldwork, as well as a low participation
of the communities themselves in basic sanitation activities, could both be factors that
impede the control of soil-transmitted helminth infections.[20–22]
Additionally, the fact that receiving any kind of state subsidy or presenting
overcrowding were both associated to prevalence of infection at household level seems
to confirm that it is not enough to treat this problem merely as a medical condition, and
that it is necessary to improve the socioeconomic and sanitary conditions of the
population. At individual level, the high prevalence found was not differentiated by
gender, age group, temporary migratory movement, nor by whether they had received
chemoprophylaxis or not, this latter aspect being seen as a reflection of the community's
situation, and not necessarily as an assessment of the efficacy of the chemoprophylaxis
program of the Public Health Ministry.
With respect to the results obtained in this community-based study (global
prevalence of 46.9% in samples where it was possible to perform the three
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determinations –direct observation, Kato-Katz method and analysis of the formol-ether
concentrate), there are few references with which we can compare our findings, since
the majority of studies are conducted in “captive” populations, such as school-
children.[23-25]
The prevalence found in this study is much higher than figures reported by several
articles available in the scientific literature that deal with the Ecuadorian situation –with
an average prevalence of 18.9%[26,27], which formed part of a meta-analysis based on
all publications related to prevalence of soil-transmitted helminth infection in South
American countries. Nevertheless, our overall prevalence figure is lower than that
reported by a previous study carried out in groups of Shuar people (prevalence rate of
65%), using Kato-Katz method but without the antecedent of having received
chemoprophylaxis.[28]
We found a large discrepancy between the measured and perceived prevalence
of geohelminthiasis, particularly for children under 5 years of age, since in nearly 8 of
every ten cases, the mother or guardian who responded perceived the presence of
parasites, whereas our findings halve this figure. This discrepancy could be explained
by the fact that the national program of preventive chemotherapy acted in these
communities four weeks before this study. On the other hand, the prevalence in those
aged over 19 years, who were also the least treated group, leads us to reflect that in
these communities, the adult population could constitute a reservoir for infection and re-
infection.
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In Ecuador, epidemiological surveillance of soil-transmitted helminth infections
has not been considered either explicitly, nor as part of the group of neglected infectious
diseases, and although the estimated prevalence of infection is high,[16] currently the
data are scarce. On the other hand, the Ecuadorian state publishes reports of its
successful health campaigns for the control of neglected diseases such as brucellosis,
Chagas disease, urban rabies, Onchocerciasis, and publicizes the important increase in
the budget for the control of neglected tropical diseases.[29]
The transmission rate of soil-helminths remains high in regions such as the
Amazonian southern border of Ecuador, in spite of the fact that in recent years member
countries of the Pan American Health Organization have celebrated regional
conventions to address the intensification of control of these poverty-related
diseases.[30]
As part of this intensification of control, the World Health Organization
recommends that school-based deworming programs include health hygiene education
as a complementary measure, although the sustainability and the long-term impact of
such education in hygiene does not appear to show encouraging results. These
limitations in the control and epidemiological surveillance of helminthic infections
could be solved with a long-term, intersectoral multidisciplinary program.[31-32]
Finally, two limitations should be taken into account when interpreting our
results. Given the age distribution of participants, the participation rate among working-
age males was very low, something which could be attributable to two aspects: to their
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absence from the community due to work, and a tendency of people in this group to
refuse to provide fecal samples. The other limitation is that the collection of a single
stool sample probably means prevalence has been underestimated. Given the
environmental conditions and geographical isolation, as well as a lack of resources, it
was not possible to obtain more fecal samples.
CONCLUSIONS
All inhabitants of the two participating communities may consider themselves to be at
risk of soil-transmitted helminth infection, despite having reported receiving preventive
chemotherapy during the month prior to the study. For this reason, it is necessary to
conduct holistic studies focusing on communities, and not simply on captive groups
such as school-children, with the object of proposing more suitable and effective
strategies to control such infections.
ACKNOWLEDGMENTS The authors gratefully acknowledge the contributions of
Lino Arisqueta, Lizeth Cifuentes, Nicole Mora-Bowen, Gabriela León and Paola Lecaro
to the field work of the study. Our thanks to Dave Macfarlane for help in developing the
english language version of this article.
CONTRIBUTORS NRS, COR, MM wrote the statistical analysis plan, cleaned and
analyzed the data, and drafted and revised the paper. NRS, MM, CS, JP and HSP
provided guidance on the data handling, contributed to the design of the analysis,
provided interpretation of data and reviewed the paper. COR, DV, CS, and JP
contributed to interpretation of the data and reviewed the paper. NRS, JP, MM and HSP
provided guidance on the conception of the work, interpretation of the data and
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reviewed the paper for content. All members have approved the final version of the
manuscript.
FUNDING This work was supported by Universidad Internacional del Ecuador
Research Programme (I-EO-01-2014).
COMPETING INTERESTS None.
ETHICS APPROVAL The study protocol was approved by the Ethical Committee of
the Universidad Central del Ecuador, and by the Ecuador Ministry of Public Health.
Each study participant gave their written informed consent, and in the case of children,
signed by their parents.
DATA SHARING STATEMENT No additional data available.
REFERENCES
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25. Chammartin F, Scholte RGC, Guimarães LH, Tanner M, Utzinger J, Vounatsou P. Soil-transmitted helminth infection in South America: a systematic review and geostatistical meta-analysis. Lancet Infect Dis. 2013 Jun;13(6):507–18.
26. Pullan RL, Smith JL, Jasrasaria R, Brooker SJ. Global numbers of infection and disease burden of soil transmitted helminth infections in 2010. Parasit Vectors. 2014;7:37.
27. Cepon-Robins TJ, Liebert MA, Gildner TE, Urlacher SS, Colehour AM, Snodgrass JJ, et al. Soil-transmitted helminth prevalence and infection intensity among geographically and economically distinct Shuar communities in the Ecuadorian Amazon. J Parasitol. 2014 Oct;100(5):598–607.
28. Nikolay B, Mwandawiro CS, Kihara JH, Okoyo C, Cano J, Mwanje MT, et al. Understanding Heterogeneity in the Impact of National Neglected Tropical Disease Control Programmes: Evidence from School-Based Deworming in Kenya. PLoS Negl Trop Dis. 2015 Sep;9(9):e0004108.
29. Cartelle Gestal M, Holban AM, Escalante S, Cevallos M. Epidemiology of Tropical Neglected Diseases in Ecuador in the Last 20 Years. PloS One. 2015;10(9):e0138311.
30. Thériault FL, Blouin B, Casapía M, Gyorkos TW. Sustaining a hygiene education intervention to prevent and control geohelminth infections at schools in the Peruvian Amazon. 2015 [cited 2016 Jun 15]; Available from: http://iris.paho.org/xmlui/handle/123456789/18385
31. Panic G, Duthaler U, Speich B, Keiser J. Repurposing drugs for the treatment and control of helminth infections. Int J Parasitol Drugs Drug Resist. 2014 Dec;4(3):185–200.
32. Gabrie, J. A., Rueda, M. M., Canales, M., Gyorkos, T. W., & Sanchez, A. L. School hygiene and deworming are key protective factors for reduced transmission of soil-transmitted helminths among schoolchildren in Honduras. Parasites & vectors. 2014;7(1):354.
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Figure 1 Distribution of the proportion of households self-identified as indigenous and categorized as poor based on unsatisfied basic needs* index and communities participants.
*Unsatisfied basic needs index: Percentage of poor households self-identified as indigenous. That is, the number of households whose basic needs are either not accessible, or of poor quality. The UBN include quality of dwelling materials, access to electricity, kids attendance to school, among others.
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Figure 1 Distribution of the proportion of households self-identified as indigenous and categorized as poor based on unsatisfied basic needs* index and communities participants.
*Unsatisfied basic needs index: Percentage of poor households self-identified as indigenous. That is, the number of households whose basic needs are either not accessible, or of poor quality. The UBN include
quality of dwelling materials, access to electricity, kids attendance to school, among others.
210x148mm (300 x 300 DPI)
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1
STROBE Statement—checklist of items that should be included in reports of observational studies
Item
No
Recommendation Pg
Title and abstract 1 (a) Indicate the study’s design with a commonly used term in the title or the
abstract
3
(b) Provide in the abstract an informative and balanced summary of what was
done and what was found
3
Introduction
Background/rationale 2 Explain the scientific background and rationale for the investigation being
reported
5
Objectives 3 State specific objectives, including any prespecified hypotheses 7
Methods
Study design 4 Present key elements of study design early in the paper 7
Setting 5 Describe the setting, locations, and relevant dates, including periods of
recruitment, exposure, follow-up, and data collection
7
Participants 6 (a) Cohort study—Give the eligibility criteria, and the sources and methods of
selection of participants. Describe methods of follow-up
Case-control study—Give the eligibility criteria, and the sources and methods
of case ascertainment and control selection. Give the rationale for the choice
of cases and controls
Cross-sectional study—Give the eligibility criteria, and the sources and
methods of selection of participants
7
(b) Cohort study—For matched studies, give matching criteria and number of
exposed and unexposed
Case-control study—For matched studies, give matching criteria and the
number of controls per case
-
Variables 7 Clearly define all outcomes, exposures, predictors, potential confounders, and
effect modifiers. Give diagnostic criteria, if applicable
8
Data sources/
measurement
8* For each variable of interest, give sources of data and details of methods of
assessment (measurement). Describe comparability of assessment methods if
there is more than one group
8
Bias 9 Describe any efforts to address potential sources of bias 7
Study size 10 Explain how the study size was arrived at 7
Quantitative variables 11 Explain how quantitative variables were handled in the analyses. If applicable,
describe which groupings were chosen and why
7-8
Statistical methods 12 (a) Describe all statistical methods, including those used to control for
confounding
9
(b) Describe any methods used to examine subgroups and interactions 9
(c) Explain how missing data were addressed 9-
10
(d) Cohort study—If applicable, explain how loss to follow-up was addressed
Case-control study—If applicable, explain how matching of cases and
controls was addressed
Cross-sectional study—If applicable, describe analytical methods taking
account of sampling strategy
-
(e) Describe any sensitivity analyses -
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Results Pg
Participants 13* (a) Report numbers of individuals at each stage of study—eg numbers potentially
eligible, examined for eligibility, confirmed eligible, included in the study, completing
follow-up, and analysed
-
(b) Give reasons for non-participation at each stage -
(c) Consider use of a flow diagram -
Descriptive
data
14* (a) Give characteristics of study participants (eg demographic, clinical, social) and
information on exposures and potential confounders
9-10
(b) Indicate number of participants with missing data for each variable of interest 9-10
(c) Cohort study—Summarise follow-up time (eg, average and total amount) -
Outcome data 15* Cohort study—Report numbers of outcome events or summary measures over time -
Case-control study—Report numbers in each exposure category, or summary
measures of exposure
-
Cross-sectional study—Report numbers of outcome events or summary measures 9-10
Main results 16 (a) Give unadjusted estimates and, if applicable, confounder-adjusted estimates and
their precision (eg, 95% confidence interval). Make clear which confounders were
adjusted for and why they were included
9-12
(b) Report category boundaries when continuous variables were categorized 8
(c) If relevant, consider translating estimates of relative risk into absolute risk for a
meaningful time period
-
Other analyses 17 Report other analyses done—eg analyses of subgroups and interactions, and
sensitivity analyses
-
Discussion
Key results 18 Summarise key results with reference to study objectives 13
Limitations 19 Discuss limitations of the study, taking into account sources of potential bias or
imprecision. Discuss both direction and magnitude of any potential bias
14,16
Interpretation 20 Give a cautious overall interpretation of results considering objectives, limitations,
multiplicity of analyses, results from similar studies, and other relevant evidence
13-
16
Generalisability 21 Discuss the generalisability (external validity) of the study results 15
Other information
Funding 22 Give the source of funding and the role of the funders for the present study and, if
applicable, for the original study on which the present article is based
17
*Give information separately for cases and controls in case-control studies and, if applicable, for exposed and
unexposed groups in cohort and cross-sectional studies.
Note: An Explanation and Elaboration article discusses each checklist item and gives methodological background and
published examples of transparent reporting. The STROBE checklist is best used in conjunction with this article (freely
available on the Web sites of PLoS Medicine at http://www.plosmedicine.org/, Annals of Internal Medicine at
http://www.annals.org/, and Epidemiology at http://www.epidem.com/). Information on the STROBE Initiative is
available at www.strobe-statement.org.
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