PRACTICAL THERAPEUTICS

Common Intestinal ParasitesCORRY lEB KUCIK. LT, MC, USN, GARY L. MARTIN, LCDR, MC. USN,and BRETT \'. SORTOR, LCDR, MC, USN, Naval Hospital Jacksonville, Jacksonville, Florida

Intestinal parasites cause significant morbidity and mortality. Diseases caused by Entero-bius vermicularis, Giardia lamblia, Ar^cylostoma duodenale, Necator americanus, andEntamoeba histolytica occur in the United States. E. vermicularis, or pinworm, causes irri-tation and sleep disturbances. Diagnosis can be made using the "cellophane tape test."Treatment includes mebendazole and household sanitation. Giardia causes nausea, vom-iting, malabsorption, diarrhea, and weight loss. Stool ova and parasite studies are diag-nostic. Treatment includes metronidazole. Sewage treatment, proper handwashing, andconsumption of bottled water can be preventive. A. duodenale and N. americanus arehookworms that cause blood loss, anemia, pica, and wasting. Finding eggs in the feces isdiagnostic. Treatments include albendazole, mebendazole, pyrante! pamoate, iron sup-plementation, and blood transfusion. Preventive measures include wearing shoes andtreating sewage. E. histolytica can cause intestinal ulcerations, bloody diarrhea, weightloss, fever, gastrointestinal obstruction, and peritonitis. Amebas can cause abscesses inthe liver that may rupture into the pleural space, peritoneum, or pericardium. Stool andserologic assays, biopsy, barium studies, and liver imaging have diagnostic merit. Therapyincludes luminal and tissue amebicides to attack both life-cycle stages. Metronidazole,chloroquine, and aspiration are treatments for liver abscess. Careful sanitation and use ofpeeled foods and bottled water are preventive. (Am Fam Physician 2004:69:1161-8. Copy-right© 2004 American Academy of Family Physicians)

Members of variousfamily practice depart-ments develop articlesfor "Practical Therapeu-tics. " This article is or}ein a series coordinatedby the Departmerit ofFamily Medicine atNaval Hospital Jack-sonville, Jacksonville,Fla. Guest editor ofthe series is Anthor)y J.Viera, LCDR, MC, U5NR.

Intestinal parasites cause significantmorbidity and mortality throughoutthe world, particularly in undevelopedcountries and in persons with comor-bidities. Intestinal parasites that

remain prevalent in the United States includeEnterobius vermicularis, Giardia lamblia,Ancyhstoma duodenale, Necator americanus,and Entamoeba histolytica.

E. vermicularis

E. vermicularis, commonly referred to as thepinworm or seatworm, is a nematode, orroundworm, with the largest geographicrange of any helminth.' It is the most preva-lent nematode in the United States. Humansare the only known host, and about 209 mil-lion persons worldwide are infected. Morethan 30 percent of children worldwide areinfected.-

Pinworm infection should be suspected in children who

exhibit pehanal pruritus and nocturnal restlessness.

Adult worms are quite small; the malesmeasure 2 to 5 mm, and the females measure8 to 13 mm. The worms live primarily in thececum of the large intestine, from which thegravid female migrates at night to lay up to15,000 eggs on the perineum. The eggs can bespread by the fecal-oral route to the originalhost and nev hosts. Eggs on the host's per-ineum can spread to other persons in thehouse, possibly resulting in an entire familybecoming infected.

Ingested eggs hatch in the duodenum, andlarvae mature during their migration to thelarge intestine. Fortunately, most eggs desic-cate within 72 hours. In the absence of hostautoinfection, infestation usually lasts onlyfour to six weeks.

Disease secondary to E. vermicularis is rela-tively innocuous, with egg deposition causingperineal, perianal, and vaginal irritation.' Thepatient's constant itching in an attempt to re-lieve irritation can lead to potentially debili-tating sleep disturbance. Rarely, more seriousdisease can result, including weight loss, uri-nary tract infection, and appendicitis.'''

Pinworm infection should be suspected in

MARCH 1,2004 / VOLUME 69, NUMBER 5 www.aafp.org/afp AMERICAN FAMILY PHYSICTAN 1161

FIGURE 1. "Cellophane tape test." (Top) Affixthe end of the tape near one end of the slide.Loop the rest of the tape over the end of theslide so the adhesive surface is exposed. (Cen-ter) Touch the adhesive surface to the perianalregion several times. (Bottom) Smooth downthe tape across the surface of the slide.

children who exhibit perianal pruritus andnocturnal restlessness. Direct visualization ofthe adult worm or microscopic detection ofeggs confirms the diagnosis, but only 5 per-cent uf infected persons have eggs in theirstool. The "cellophane tape test" (Figure I) canserve as a quick way to clinch the diagnosis."'

FIGURE 2. Giardia lamblia cyst.

Reprinted from Centers for Disease Control and Pre-vention. Accessed November 15, 2003, at http://phil.cdc.gov.

This test consists of touching tape to the peri-anal area several times, removing it, andexamining the tape under direct microscopyfor eggs. The test should be conducted rightafter awakening on at least three consecutivedays. This technique can increase the test'ssensitivity to rouglily 90 percent.

6. lamhiiaG. lamblia is a pear-shaped, flagellated pro-

tozoan (Figure 2) that causes a wide variety ofgastrointestinal complaints. Giardia is arg-uably the most common parasite infection ofhumans worldwide, and the second mostcommon in the United States after pin-worm."-" Between 1992 and 1997, the Centersfor Disease Control and Prevention (CDC)estimated that more than 2.5 million cases ofgiardiasis occur annually."'

Because giardiasis is spread by fecal-oralcontamination, the prevalence is higher inpopulations with poor sanitation, close con-tact, and oral-anal sexual practices. The dis-ease is commonly water-borne because Giar-dia is resistant to the chlorine levels in normaltap water and survives well in cold mountainstreams. Because giardiasis frequently infectspersons who spend a lot of time camping,backpacking, or hunting, it has gained thenicknames of "backpacker's diarrhea" and"beaver fever.""

1162 AMERICAN FAMILY PHYSICIAN wvw.aafp.org/afp VoujME 69, NUMBER 5 / MARCH 1,2004

Intestinal Parasites

Food-borne transmission is rare but canoccur with ingestion of raw or undercookedfoods. Giardiasis is a zoonosis, and cross-infectivity among beaver, cattle, dogs, ro-dents, and bighorn sheep ensures a constantreservoir.''

The life cycle of Giardia consists of twostages: the fecal-orally transmitted cyst andthe disease-causing trophozoite. Cysts arepassed in a host's feces, remaining viable in amoist environment for months. Ingestion ofat least 10 to 25 cysts can cause infection inhumans."' When a new host consumes a cyst,the host's acidic stomach environment stimu-lates excystation. Each cyst produces twotrophozoites. These trophozoites migrate tothe duodenum and proximal jejunum, wherethey attach to the mucosal wall by means of aventral adhesive disk and replicate by binaryfission.

Giardia growth in the small intestine isstimulated by bile, carbohydrates, and lowoxygen tension.^ It can cause dyspepsia, mal-absorption, and diarrhea. A recent theory sug-gests that the symptoms are the result of abrush border enzyme deficiency rather thaninvasion of the intestinal wall.'' Some tropho-zoites transform to cysts and pass in the feces.

Clinical presentations of giardiasis varygreatly. After an incubation period of one totwo weeks, symptoms of gastrointestinal dis-tress may develop, including nausea, vomit-ing, malaise, flatulence, cramping, diarrhea,steatorrhea, and weight loss. A history of gra-dual onset of a mild diarrhea helps differenti-ate giardiasis or other parasite infections frombacterial etiologies. Symptoms lasting two tofour weeks and significant weight loss are keyfindings that indicate giardiasis.

Chronic giardiasis may follow an acute syn-drome or present without severe antecedentsymptoms. Chronic signs and symptoms suchas loose stool, steatorrhea, a 10 to 20 percentloss in weight, malabsorption, malaise, fat-igue, and depression may wax and wane overmany months if the condition is not treated.

Rarely, patients with giardiasis also present

Antigen assays for Giardia have excellent sensitivity and

specificity, but direct microscopy can detect concomitant

parasite infections.

with reactive arthritis or asymmetric synovi-tis, usually of the lower extremities." Rashesand urticaria may be present as part of ahypersensitivity reaction.

Cyst excretion occurs intermittently inboth formed and loose stools, while tropho-zoites are almost only found in diarrhea.Stool studies for ova and parasites (O&P)continue to be a mainstay of diagnosis despiteonly low to moderate sensitivity. Examinationof a single stool specimen has a sensitivity of50 to 70 percent; the sensitivity increases to85 to 90 percent with three serial speci-mens."'" Because Giardia is not invasive,eosinophilia, and peripheral or fecal leukocy-tosis do not occur.

Antigen assays use enzyme-linked im-munosorbent assay (ELISA) or immunofluo-rescence to detect antibodies to trophozoitesor cysts. Sensitivities range from 90 to 99 per-cent, with specificities of 95 to 100 percentcompared with stool O&P. Despite the highyield of these studies, direct microscopy isstill important, because multiple diarrhea-causing infectious etiologies can be presentsimultaneously.

Duodenal aspirates and biopsies give ahigher yield than stool studies but are invasiveand usually not necessary for diagnosis. Serol-ogy and stool cultures are generally unneces-sary. Polymerase chain reaction (PCR) analy-sis, while only experimental, may be effectivefor screening water supplies."

A. duodenale and N. americanus

Two species of hookworm, A. duodenale andN. americanus, are found exclusively inhumans. A. duodenale, or "Old World" hook-worm, is found in Europe, Africa, China, Japan,India, and the Pacific islands. N. americanus.

MARCH 1,2004 / VOLUME 69, NUMBER 5 www.aafp.org/afp AMERICAN FAMILY PHYSICIAN 1163

the "New World" hookworm, is found in theAmericas and the Caribbean, and has recentlybeen reported in Aft ica, Asia, and the Pacific.

Until the early 1900s, JV. americanus infesta-tion was endemic in the southern UnitedStates and was only controlled after the wide-spread use of modern plutnbing and footwear.Even though the prevalence of these parasiteshas drastically decreased in the general popu-lation, tlie CDC reports that in the UnitedStates, hookworm infection is the secondmost common helminthic infection identifiedin stool studies.'"

N. americamts ranges from 10 to 12 mm inlength for females and 6 to 8 mm for males. Itis distinguished from its slightly larger Euro-pean cousin by its semilunar dorsal and ventralcutting plates at the buccal cavity comparedwith A. iiuodenale's two pairs of ventraJ cuttingteeth (Figure 3). The e^s of both worms are 60to 70 |jm in length and bounded by an ovoidtransparent hyaline membrane; they containtwo to eight cell divisions (Figure 4).

Both species share a common life cycle.Eggs hatch into rhabditiform larvae, feed onbacteria in soil, and molt into the infectivefilariform larvae. Enabled by moist climatesand poor hygiene, filariform larvae enter theirhosts through pores, hair follicles, and evenintact sldn. Maturing larvae travel through thecirculation system until they reach alveolarcapillaries. Breaking into lung parenchyma,

FIGURE 3, Electron micrograph of teeth and cutting plate differencesbetween (left) Ar^cylostoma duodenale and (right) Necator americanus.

Reprinted from Centers for Disease Control and Prevention and Dr. Mae Melvin.Accessed November 75, 2003. at http.ilphil.cdcgov.

FIGURE 4. Hookworm egg.

Reprinted from Centers for Disease Control and Pre-vention. Accessed November 15, 2003, at http://phil.cdc.gov.

the larvae climb the bronchial tree and areswallowed with secretions. Six weeks after theinitial infection, mature worms have attachedto the wall of t!ie small intestine to feed, andegg production begins.

While larvae occasionally cause prurilicerythema or pulmonary symptoms duringtheir migration to the gut,'^ hookworm infec-tion rarely i.s symptomatic until a significantintestinal worm burden Is established. A tran-sient gastroenteritis-like syndrome can occurbecause mature worms attach to the intestinalmucosa.

The greatest concern from infection isblood loss. Aided by an organic anticoagulant,a hookworm consumes about 0.25 mL of hostblood per day. The blood loss caused by hook-worms can produce a microcytic hypo-chromic anemia."^ Compensatory volumeexpansion contributes to hypoproteinemia,edema, pica, and wasting. The infection mayresult in physical and mental retardation inchildren. Eosinophilia has been noted in 30 to60 percent of infected patients.

While clinical history, hygiene status, andrecent travel to endemic areas can give impor-tant clues, definitive diagnosis rests on micro-scopic visualization of eggs in the stool.

f. histolyticaAniebiasis is caused by E. histolytica, a pro-

tozoan that is 10 to 60 \jLxn in length and moves

1164 AMERICAN FAMILY PHYSICIAN www.aafp.org/afp VOLUME 69, NUMBER 5 / MARCH 1,2004

Intestinal Parasites

through the extension of finger-like pseudo-pods.' Spreading occurs via the fecal-oralroute, usually by poor hygiene during foodpreparation or by the use of "night soil" (cropfertilization with human waste), as well as byoral-anal sexual practices. Spreading is fre-quent in persons who have a deficient im-mune system. Crowding and poor sanitationcontribute to its prevalence in Asia, Africa,and Latin America. Approximately 10 percentof the world's population is infected, yet90 percent of infected persons are asympto-matic.'' Of the roughly 50 million symptom-atic cases occurring each year, up to 100,000are fatal.'* The stable reservoir of infectivecases complicates eradication. After malaria, itis likely that E. histolytica is the world's sec-ond leading protozoan cause of death.''

Much like Giardia, the two stages in the E.histolytica life cycle are cysts and trophozoites(Figure 5). Infective cysts are spheres of ahout12 \xm in diameter that have one to fournuclei and can be spread via the fecal-oralroute by contaminated food and water ororal-anal sexual practices. The pseudopodaltrophozoite is about 25 \im across, has a sin-gle nucleus, and may contain red blood cellsof the host in various stages of digestion.Ingested cysts hatch into trophozoites in thesmall intestine and continue moving downthe digestive tract to the colon. Also like Giar-dia, some ameba trophozoites become cyststhat are passed in the stool and can survive forweeks in a moist environment. However,trophozoites can invade the intestinal mucosaand spread in the bloodstream to the liver,lung, and brain.

Amebiasis can cause both intraluminal anddisseminated disease. In the intestinal lumen,£. histolytica can disrupt the protective mucuslayer overlying the colonic mucosa. Theresulting epithelial ulcerations can bleed andcause colitis,- " usually two to six weeks afterinitial infection. Acute progression to malaise,weight loss, severe abdominal pain, profusebloody diarrhea, and fever can occur, oftenleading to a misdiagnosis of appendicitis, es-

Hookworm infection can cause microcytic hypochromic

anemia, hypoproteinemia, edema, pica, and wasting.

pecially in children. In chronic smoldering ca-ses, inflammatory bowel disease can be misdi-agnosed, and treatment with steroids only ex-acerbates the infection.

Rarely, a reactive collection of edematousgranulation and fibrous tissue called an ame-boma can grow into the lumen, causing pain,obstruction and, possibly, intussusception.Toxic megacolon, pneumatosis coli (intra-mural air), and peritonitis also may occur.''"

FIGURE 5. (Top) Entamoeba histolytica cyst and(bottom) trophozoite.

Reprinted from Centers for Disease Control and Pre-vention and Drs. LLA. Moore, Jr, and Mae Melvin.Accessed November 15, 2003, at http://phil.cdc.gov.

MARCH 1,2004 / VOLUME 69, NUMBER 5 www.aafp.org/afp AMERICAN FAMILY PHYSICIAN 1165

Tissue penetration and dissemination arepossible. Trophozoites that penetrate theintestinal wall spread through the body via theportal circulation. Amebas are chcmotactic,attracting neutrophils Ln the circulation. Anie-bic liver abscesses form because of toxinrelease and hepatocyte damage, and usuallydevelop within five months after infection.Symptoms of a developing abscess includefever, dull pleuritic right upper quadrant painradiating to the right shoulder, and pleuraleffusions. Diarrhea i.s present in only one ofthree patients v ith abscess. Fever is the pre-senting symptom in 10 to 15 percent of pa-tients, and therefore amebic abscess should beconsidered in patients with a lever of un-known origin. Abscesses may rupture into thepleural space, peritoneum, or pericardium,requiring emergency drainage.

Traditional O&P stool testing for amebiasisshould use at least three fresh samples toincrease sensitivity. However, tbis test hasrecently fallen out of favor'** because an£ histolytica stool antigen test with a sensitiv-ity of 87 percent and a specificity of more than90 percent has become available.'^ Stool cul-ture and PCR testing modalities used inresearch are not yet sufficiendy widespread tobe clinically useful. Positive stool samples arelikely lo be heme positive and to have low neu-trophils but may contain Charcot-Leyden

The AuthorsCORRY JEB KUCIK, LT, MC. USN, currently serves as flight surgeon for Marine FighterAttack Squadron 251, Marine Corps Air Station, Beaufort, S,C. He received his med-tcal degree from the Uniformed Services University of the Health Sciences, Bethesda,Md., and completed an internship in family medicine at Naval Hospital Jacksonville,Jacksonville, Fla.

GARY L. MARTIN, LCDR. MC, USN, serves as 27th Group Surgeon, 2d Marine AirWing, al the Marine Corps Air Station, Cherry Point, N.C. He received his medicaldegree from the Uniformed Sen/ices University of the Health Sciences and completeda residency in family medicine at Naval Hospital Jacksonville,

BRETT V. SORTOR, LCDR, MC, USN, is a senior resident in the family medicine resi-dency program at Naval Hospital Jacksonville. He received his medical degree from theMedicai University of South Carolina, Charleston.

Address correspondence to Corry J. Kucik, LT, MC, USN. 1210 Brookwood Circle. Ope-ilka, AL 36801. Reprints are not available from the authors.

FIGURE 6. Computed tomographic scan show-ing liver abscess.

Reprinted with permission from Medscape. AccessedNovember 15, 2003. at http://www.med scape.com/content/2002/00/44/12/441223/art'iim441223.

crystals, indicating tbe presence of eosino-phils. Biopsy of colonic ulcer edges may yieldintramural trophozoites but carries with it therisk of perforation.

Serologic tests such as ELISA and agar geldiffusion are more than 90 percent sensitive,but these tests often become negative within ayear of initial infection. Approximately 75 per-cent of infected patients have Ieukocytosis, butmucosal invasion does not cause eosinophilia.Liver function tests usually are normal but mayshow minimal elevation of alkaline phos-phatase, even in the presence of large abscesses.To avoid misdiagnosis, patients with suspectedulcerative colitis must be tested for £. histolyt-ka antibodies before starting steroid therapy.'^

Intestinal barium studies may be useful inidentifying possible amebomas, but biopsy isrequired to confirm the diagnosis and rule outneoplasia. Liver imaging studies, such as Liltra-sonography, computed tomography (Figure 6),magnetic resonance imaging, and nuclearmedicine scans, can reveal abscesses as ovalor round hypoechoic cysts, usually in the rightlobe of the liver.-'

Risk of complications increases with cysts of

1166 AMERICAN FAMILY PKYSICIAN wv^w.aafp.org/afp VOLUME 69, NUMBER 5 / MARCH 1,2004

TABLE 1

Treatment and Prevention of Parasite Infections

Parasite Treatment Preverition

Enterobius Primary; Mebendazole (Vermox), 100 mg orally oncevermicularis Secondary: Pyranlel pamoate (Pin-Rid), 11 mg per kg

(maximum of 1 g) orally once;oralbendazole (Valbazen). 400 mg orally once

If persistent, repeat treatment in two weeks.Do not give to children younger than two years,

Giardia Adults: Metronidazole (Flagyl), 250 mg orally three times daily forIarr)bli3 five to seven days

Pregnant women with miid symptoms: consider defen-ing treatmentuntil after delivery.

Pregnant women with severe symptoms: paromomycin (Humatin),500 mg oraliy four times daily for seven to 10 days; metronidazoleis acceptable.

Children: albendazole, 400 mg orally for five daysAsymptomatic carriers in developed countries: treat using regimen

for adults or children.Asymptomatic carriers in developing countries: not cost-effective

to treat because of high reinfection rate.

Ancylostoma Albendazole, 400 mg orally onceduodenale, Mebendazole, 100 mg orally twice daily for three daysNecator Pyrantel pamoate, 11 mg per kg (maximum of 1 g) onceamericanus Iron supplementation is beneficial even before diagnosis or

treatment initiation-Packed red blood cells (as needed) can minimize risk of volume

overload in severely hypoproteinemic patients.Confirm eradication with follow-up stool examination two weeks

after discontinuation of treatment,

Entamoeba Intestinal disease: use both luminal amebicide (for cysts) and tissuehistolytica amebicide (for trophozoites}

Luminal:lodoquinol (Yodoxin), 650 mg orally three times daily for 20 days

orParomomycin, 500 mg orally three times daily for seven days

orDiloxanide furoate (Furamide), 500 mg orally three times daily

for 10 days (available from CDC)Tissue:

Metronidazole, 750 mg orally three times daily for 10 daysLiver abscess:

Metronidazole, 750 mg orally three times daily for five days, thenparomomycin, 500 mg three times daily for seven daysor

Chloroquine (Aralen), 600 mg orally per day for two days, then200 mg orally per day for two to three weeks (higher relapse rates)

Aspirate if:Pyogenic abscess is ruled out; there is no response to treatment in

three to five days; rupture is imminent; pericardial spread is imminent

Treat household contacts.Clean bedrooms, bedding.

Use proper sewage disposal and watertreatment (flocculation, sedimentation,filtration, and chlorination).

Consume only bottled water in endemic areas.Water treatment options:

Boil water for one minuteHeat water to 7O''C (158''F) for 10 minutesPortable camping filterIodine purification tablets for eight hours

Daycare centers:Proper disposal of diapersProper and frequent handwashmg

Use proper and continued shoe wear.Use proper sewage disposal.

Use proper sanitation to eradicate cyst carriage.Avoid eating unpeeled fruits and vegetables.Drink bottled water.Use iodine disinfeaion of nonbottied water.

CDC - Centers for Disease Control and Prevention.

Information from references 1, 2, 5, 7, 9, \7, 19, and22.

more than 10 cm, multiple cysts, superior rightlobe involvement, or any left lobe involvement.Repeat studies may be confusing by showinglarger abscesses in improving patients.Although two thirds of abscesses resolvewithin six months, approximately 10 percentof abscesses persist for more than a year.'''

Treatment and PreventionTreatment and prevention strategies

for parasite infections are summarized inTable //- 'S' ' -i'-'y" Amebicidal agents avail-able in the United States are compared inTable 2.'^

MARCH 1,2004 / VOLUME 69, NUMBER 5 www.aafp.org/afp AMERrcAN FAMILY PHYSICIAN 1167

TABLE 2

Advantages and Disadvantages of Amebicidal Agents

Amebicidal agent Advantages Disadvantages

Lumina! amebicides

Paromomycin

(Humatin)

lodoquinol (Yodoxin)

Diloxanide furoate(Furamide)

Seven-day treatment course; maybe useful during pregnancy

Inexpensive and effective

Alternative to paromomycin ifunable to tolerate

For invasive intestinal disease only

Tetracycline, Alternative to metrontdazoleerythromycin (flagyl) if unable to tolerate

For invaswe intestinal and extraintestinal amebiasisMetronidazole Drug of choice for amebic colitis

and liver abscessChloroquine (Aralen) Useful oniy for amebic liver

abscess

Frequent Gl disturbances; rare ototoxicity and nephrotoxicity; expensive

20-day treatment course; contains iodine; rare optic neuritis and atrophywith prolonged use

Available in United States only from the CDC; frequent Gl disturbances;rare diplopia; contraindicated in pregnant women

Not active for liver abscesses, frequent Gl disturbances; tetracycline should not beadministered to children or pregnant women: must be used with luminal agent

Anorexia, nausea, vomiting, and metallic taste in nearly one third of patientsat dosages used, disutfiram-like reaction with alcohol; rare seizures

Occasional headache, pruritus, nausea, alopecia, and myalgias; rare heart blockand irreversible retinal injury

Gl = gastrointestinal; CDC = Centers for Disease Control and Prevention.

Adapted with permission from Huston CD, Petri WA. Amebiasis. In: Rakel R. ed. Conn's Current therapy 2001. Philadelphia: Saunders, 2001:64-5.

The opinions and assertions contained herein are

the private views of the authors and are not to be

construed as official or as reflecting the views of

the U.S. Navy Medical Corps or the U.S. Navy at

large.

The authors thank Anthony j. Viera, LCDR. MC, USNR,for constructive feedback and encouragement.

The authors indicate that they do not have any con-

flicts of interest Sources of funding: none reported.

REFERENCES ^ _ ^

1. Neva FA, Brown HW. Basic clinical parasitology. 6thed, NonA'alk, Conn : Appleton & Lange, 1994.

2. Goldmann DA, Wilson CM. Pinworm infestations.In: Hoekelman RA, Pnmary pediatnc care. 3d ed.St. louis: Mosby, 1997:1519.

3. MacPherson OW. Intestinal parasites in returnedtravelers Med Clin North Am 1999;83:1053-75

4. Saxena AK, Springer A, Tsokas J, Willital GH. Lap-aroscopic appendectomy in children with Entero-bius vermicularis. Surg Laparosc Endosc PercutanTech 2001:11:284-6.

5. Dickson R, Awasthi S, Demellweek C, Williamson P.Anthelmintic drugs for treating worms in children:effects on growth and cognitive performance.Cochrane Database Syst Rev 2003,(2): CD000371.

6. Parija SC, Sheeladevi C, Shivaprakash MR, Biswal N-Evaiuation of lactophenol cotton biue stain fordetection of eggs of Enterobius vermicularis in peri-anal surface samples. Trop Doct 2001;31(4):214-5.

7. Procop GW. Gastrointestinal infections. Infect DisCtin North Am 2001:15:1073-108.

8. Katz DF, Taylor DN. Parasitic infections of the gas-trointestinal traa, Gastroenterol Clin North Am2001:30:795-815.

9. Leder K, Welier P Giardiasis, In: Rose BD, ed. Infec-tious disease, Wellesley. Mass.: UpToDate, 2002,

10. Furness BW, Beach MJ, Roberts JM, Giardiasis sur-

veillance—United States, 1992-1997, MMWR CDCSurveiii Summ 2O00:49(7):1-13,

11. DuPont HL, Backer HD. Infectious diarrhea fromwilderness and foreign travel. In: Auerback PS, ed.Wilderness medicine: management of wildernessand environmental emergencies. 3d ed. St. Louis:Mosby, 1995:1028-59.

12. Giaser C, Lewis P, Wong S, Pet-, animal- and vec-tor-borne infeaions. Pediatr Rev 2000:21:219-32

13. Steiger U, Weber M, Ungewbhnliche ursache vonerythema nodosum. pleuraerguss und reaktiverarthritis: giardia lamblia. [Unusual etiology of ery-thema nodosum, pleural effusion and reactivearthritis: Giardia iamblia.] Schweiz Rundsch MedPrax2002;91:1091-2.

14. Centers for Disease Control and Prevention. Publi-cation of CDC surveillance summaries. MMWRMorb Mortal Wkiy Rep 1992:41 (8): 145-6,

15. Kitchen LW. Case studies in international medicine.Am Fam Physician 1999;59:3040-4.

15. Ali-Ahmad N, Bathija M, Abuhammour W. Index ofsuspicion. Case #2. Diagnosis: anemia from hook-worm infestation, Pediatr Rev 2OOO;21:354-7.

17 Reed SL. Amebiasis and infection with free-livingamebas. In: Harrison TR, Fauci AS. Braunwald E, etal., eds. Harrison's Principles of internal medicine.15th ed, NewYork: McGraw-Hill, 2001:1199-202.

18. Walsh JA. Problems in recognition and diagnosis ofamebiasis: estimation of the global magnitude ofmorbidity and mortality. Rev Infect Dis 1986;8;228-38,

19. Petri WA Jr, Singh U. Diagnosis and managementof amebiasis. Clin infect Dis 1999:29:1117-25.

20. Stanley SJ. Pathophysiology of amoebiasis. TrendsParasitol 2001:17:280-5.

21. Kimura K. Stoopen M. Reeder MM, Moncada R,Amebiasis: modern diagnostic imaging with patho-logical and clinical correlation. Semin Roentgenol1997:32:250-75.

22. Huston CD, Petri WA. Amebiasis. In: Rakel R, ed.Conn's Current therapy 2001. Philadelphia: Saun-ders. 2001:64-5.

1168 AMERICAN FAMILY PHYSICIAN www,aafp.org/afp VOLUME 69, NUMBER 5 / MARCH 1,2004