intestinal capillariasis · for adult and larval stages of the parasite. the ilocano populations...

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CLINICAL MICROBIOLOGY REVIEWS, Apr. 1992, p. 120-129 0893-8512/92/020120-10$02.00/0 Copyright ©O 1992, American Society for Microbiology Intestinal Capillariasis JOHN H. CROSSt U.S. Naval Medical Research Unit No. 2, Manila, Philippines INTRODUCTION .......................... DESCRIPTION OF THE PARASITE. HISTORY .................................... LIFE CYCLE OF THE PARASITE... CLINICAL PICTURE..................... symptoms ... Pathology ...................... 124 Diagnosis ..................... 125 Treatment ..................... 126 EPIDEMIOLOGY ..................... 127 Distribution and Prevalence...................... 127 Transmission ...................... 128 Control .129 REFERENCES. INTRODUCTION Although more than 250 Capillaria species have been found in fish, amphibians, reptiles, birds, and mammals, only 4 species have been found in humans: Capillaria hepatica, C. aerophila (Eucoleus aerophilus), C. plica, and C. philippinensis. Reports of human infections with C. hepatica, C. aerophila, and C. plica are rare, but reports of C. philippinensis infections are increasing and appear to be spreading geographically. C. philippinensis has been in- volved in epidemics and has been responsible for the death of people in the Philippine Islands and Thailand. DESCRIPTION OF THE PARASITE Capillarids are closely related to Trichuris and Trichinella species; all are members of the superfamily Trichinelloidea. The group is characterized by having a filamentous thin anterior end and a slightly thicker, and sometimes shorter, posterior end. The esophagus consists of a short muscular portion surrounded by rows of secretory cells called sti- chocytes. The entire esophageal structure is called a sticho- some. The male worms may or may not have a single sheathed spicule. In the female, the vulva is located at the junction of the anterior and posterior ends. Chitwood et al. (6) described C. philippinensis in speci- mens collected at autopsy from the first person known to have the infection and in material obtained from several subsequent autopsies. Additional specimens were examined by other investigators, and the initial findings were con- firmed. The parasite is very small: males range in length from 1.5 to 3.9 mm and in width from 3 to 5 ,um at the head, 23 to 28 ,um at the stichosome, and 18 ,um at the cloaca. The male spicule is 230 to 300 ,um long, and the unspined spicular sheath may extend to 440 p.m. The anus is subterminal, and the tail has ventrolateral expansions containing two pairs of papillae. Females are much longer than males, 2.3 to 5.3 mm, with widths of 5 to 8 p.m at the head, 25 p.m at the t Present address: Department of Preventive Medicine and Bio- metrics, Uniformed Services University of the Health Sciences, 4301 Jones Bridge Road, Bethesda, MD 20814-4799. widest part of the stichosome, 28 to 36 p.m at the vulva, and 29 to 47 pum postvulva. The vulva is located behind the esophagus, is salient, and is without a flap. The anus is subterminal. Figures 1 and 2 illustrate male and female worms, respectively, showing some of the features men- tioned above. The female uterus contains numerous thick- shelled eggs (Fig. 2), thin-shelled eggs with or without embryos (Fig. 2), or larvae (Fig. 3). Eggs found in feces are peanut shaped with a striated shell and inconspicuous flat- tened bipolar plugs, and they measure 36 to 45 by 20 pum (Fig. 4). HISTORY Although a number of Capillaria species are known to inhabit the intestinal tract of lower animals, human intestinal capillariasis was unknown until Chitwood et al. presented the initial case report at the First International Congress of Parasitology in Rome in 1964. The patient was a 29-year-old male schoolteacher from Northern Luzon in the Philippines. He had an intractable diarrhea for 3 weeks prior to admission to the Philippine General Hospital, Manila. He suffered from chronic alcoholism, recurrent ascites, emaciation, and cachexia and died a week after hospitalization. At autopsy, a large number of worms were recovered from the intestines, but the parasite was not identified to species at the time. In late 1966, a Catholic missionary priest in Tagudin Ilocos Sur, Central Luzon, notified authorities of an unusually large number of deaths due to a chronic gastroenteritis that had been occurring since 1965 in a village called Pudoc West. This village is approximately 150 km south of the area where the first case was seen. Upon investigation the Philippine Department of Health established that C. philippinensis was responsible for the illnesses. The parasitosis soon spread to other villages and towns, and by the end of 1967, more than 1,000 people had become infected and 77 had died. The people in the village of Pudoc West were superstitious and believed that they were all destined to die of the mysterious disease because of a curse placed on them by a mystical river god. Against the advice of the public health authorities now working in the area, they hired two witch doctors to exorcise the village. The witch doctors were 120 Vol. 5, No. 2 .120 .121 1IA 129 on November 27, 2020 by guest http://cmr.asm.org/ Downloaded from

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Page 1: Intestinal Capillariasis · for adult and larval stages of the parasite. The Ilocano populations ofNorthern Luzonhave unique dietary habits, unlike those of other Filipino populations

CLINICAL MICROBIOLOGY REVIEWS, Apr. 1992, p. 120-1290893-8512/92/020120-10$02.00/0Copyright ©O 1992, American Society for Microbiology

Intestinal CapillariasisJOHN H. CROSSt

U.S. Naval Medical Research Unit No. 2, Manila, Philippines

INTRODUCTION ..........................DESCRIPTION OF THE PARASITE.HISTORY ....................................LIFE CYCLE OF THE PARASITE...CLINICAL PICTURE.....................symptoms...Pathology...................... 124Diagnosis..................... 125Treatment..................... 126

EPIDEMIOLOGY..................... 127Distribution and Prevalence...................... 127Transmission...................... 128Control.129

REFERENCES.

INTRODUCTION

Although more than 250 Capillaria species have beenfound in fish, amphibians, reptiles, birds, and mammals,only 4 species have been found in humans: Capillariahepatica, C. aerophila (Eucoleus aerophilus), C. plica, andC. philippinensis. Reports of human infections with C.hepatica, C. aerophila, and C. plica are rare, but reports ofC. philippinensis infections are increasing and appear to bespreading geographically. C. philippinensis has been in-volved in epidemics and has been responsible for the deathof people in the Philippine Islands and Thailand.

DESCRIPTION OF THE PARASITECapillarids are closely related to Trichuris and Trichinella

species; all are members of the superfamily Trichinelloidea.The group is characterized by having a filamentous thinanterior end and a slightly thicker, and sometimes shorter,posterior end. The esophagus consists of a short muscularportion surrounded by rows of secretory cells called sti-chocytes. The entire esophageal structure is called a sticho-some. The male worms may or may not have a singlesheathed spicule. In the female, the vulva is located at thejunction of the anterior and posterior ends.

Chitwood et al. (6) described C. philippinensis in speci-mens collected at autopsy from the first person known tohave the infection and in material obtained from severalsubsequent autopsies. Additional specimens were examinedby other investigators, and the initial findings were con-firmed. The parasite is very small: males range in length from1.5 to 3.9 mm and in width from 3 to 5 ,um at the head, 23 to28 ,um at the stichosome, and 18 ,um at the cloaca. The malespicule is 230 to 300 ,um long, and the unspined spicularsheath may extend to 440 p.m. The anus is subterminal, andthe tail has ventrolateral expansions containing two pairs ofpapillae. Females are much longer than males, 2.3 to 5.3mm, with widths of 5 to 8 p.m at the head, 25 p.m at the

t Present address: Department of Preventive Medicine and Bio-metrics, Uniformed Services University of the Health Sciences,4301 Jones Bridge Road, Bethesda, MD 20814-4799.

widest part of the stichosome, 28 to 36 p.m at the vulva, and29 to 47 pum postvulva. The vulva is located behind theesophagus, is salient, and is without a flap. The anus issubterminal. Figures 1 and 2 illustrate male and femaleworms, respectively, showing some of the features men-tioned above. The female uterus contains numerous thick-shelled eggs (Fig. 2), thin-shelled eggs with or withoutembryos (Fig. 2), or larvae (Fig. 3). Eggs found in feces are

peanut shaped with a striated shell and inconspicuous flat-tened bipolar plugs, and they measure 36 to 45 by 20 pum(Fig. 4).

HISTORY

Although a number of Capillaria species are known toinhabit the intestinal tract of lower animals, human intestinalcapillariasis was unknown until Chitwood et al. presentedthe initial case report at the First International Congress ofParasitology in Rome in 1964. The patient was a 29-year-oldmale schoolteacher from Northern Luzon in the Philippines.He had an intractable diarrhea for 3 weeks prior to admissionto the Philippine General Hospital, Manila. He suffered fromchronic alcoholism, recurrent ascites, emaciation, andcachexia and died a week after hospitalization. At autopsy,a large number ofworms were recovered from the intestines,but the parasite was not identified to species at the time.

In late 1966, a Catholic missionary priest in Tagudin IlocosSur, Central Luzon, notified authorities of an unusually largenumber of deaths due to a chronic gastroenteritis that hadbeen occurring since 1965 in a village called Pudoc West.This village is approximately 150 km south of the area wherethe first case was seen. Upon investigation the PhilippineDepartment of Health established that C. philippinensis wasresponsible for the illnesses. The parasitosis soon spread toother villages and towns, and by the end of 1967, more than1,000 people had become infected and 77 had died.The people in the village of Pudoc West were superstitious

and believed that they were all destined to die of themysterious disease because of a curse placed on them by a

mystical river god. Against the advice of the public healthauthorities now working in the area, they hired two witchdoctors to exorcise the village. The witch doctors were

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INTESTINAL CAPILLARIASIS 121

SC

Sp

FIG. 1. Adult male C. philippinensis indicating spicule (Sp), extended spicular sheath (Ss), and stichocyte (Sc). Magnification, x32.

retained until one of them died of intestinal capillariasis.Other beliefs and superstitions emerged during the epidemicuntil a cure and means of transmission were established (15).A few years after the Pudoc West outbreak, it was

determined that during 1963 to 1965 a number of people haddied of a chronic gastroenteritis in the area of NorthernLuzon where the first patient lived. In 1965, the diseasebegan to be seen in Pudoc West, and in the ensuing yearsinfections were found in villages along the western andnorthern coasts of Central and Northern Luzon.

LIFE CYCLE OF THE PARASITE

Since C. philippinensis was a new human parasite, it wasessential to obtain knowledge about every aspect of the

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parasitosis. Clinical management and treatment regimenswere established, pathophysiologic studies were done, andepidemiologic information was gathered. One of the mostcomplex challenges, however, was to determine the meansof transmission of the parasite and its life cycle. First,attempts were made to determine possible reservoir hostsfor adult and larval stages of the parasite. The Ilocanopopulations of Northern Luzon have unique dietary habits,unlike those of other Filipino populations. These eatinghabits were considered when searching for a source ofinfection. More than 150,000 specimens of animal life wereexamined, and although adult Capillana worms were found,none were C. philippinensis. Capillaria larvae were alsofound, but species determination was not possible (15).

FIG. 2. Adult female C. philippinensis indicating stichocyte (Sc), salient vulva (Vu), uterus (Ut), eggs (Eg) in the uterus, and thin-shelledeggs with larvae (Lv). Magnification, x32.

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CLIN. MICROBIOL. REV.

Lv

Vu

FIG. 3. Adult female C. philippinensis indicating salient vulva (Vu) and uterus filled with larvae (Lv). Magnification, x 160.

Massive stool surveys were undertaken to detect asymp-tomatic infections and to determine whether a relationshipexisted between C. philippinensis and other intestinal para-sites. More than 7,000 stool samples from 23 village popu-lations were examined, but there was no correlation betweenC. philippinensis infection and other parasitic infections.Most people (94%) had 1 and, more often, 2 to as many as 10different parasites by a single stool examination. Only 2%were passing C. philippinensis eggs, compared with 83%passing Trichuris trichiura eggs (12).While the above studies were under way, investigations

were conducted to establish the life cycle in the laboratory.At that time the life histories of only a few Capillaria specieswere known. Some species had a direct egg-to-egg cyclewhereas others had indirect cycles involving an intermediatehost. Eggs isolated from patients were found to embryonateat ambient temperatures in 5 to 10 days. The eggs were givenorally to all types of animals, even human volunteers, but didnot hatch (9). The experiments continued, and eventuallyeggs were found to hatch in the intestines of freshwater andbrackish-water fish from the lagoons in the endemic area.The eggs hatched within a few hours after ingestion, and thelarvae increased in size from 130-150 ,um to 250-300 ,um

after 3 weeks (Fig. 5). Several species of fish in the Philip-pines (8, 10) and other species in Thailand (4) were found tobe susceptible to infection. In further studies, one species offish (Hypseleotris bipartita) was found naturally infectedwith the larval stage of the parasite, which was recoveredfrom the intestine.Larvae from fish were subsequently fed to monkeys

(Macaca spp.), and patent infections developed (8). Mon-keys tolerated the infections well and never manifestedsymptoms. A few of these infections remained patent for aslong as 14 months. Three to four months after being given 30to 50 larvae from fish, some monkeys were killed and 10,000to 30,000 worms were recovered from their intestines. Thisconfirmed the suspicion that autoinfection was part of thelife cycle because large numbers of worms in all stages ofdevelopment were found at autopsy. In addition, femaleworms are larviparous.Many other laboratory and wild animals were experimen-

tally infected with larvae from fish. Some wild rats (Rattusspp.) and multimammate rats (Mastomys natalensis) devel-oped transient infections, but Mongolian gerbils (Merionesunguiculatus) developed patent infections and died of over-whelming infections after 6 to 7 weeks. A series of experi-

FIG. 4. Two eggs of C. philippinensis, two-cell stage. Note the flattened bipolar plugs and striations in the eggshell; they measure 36 to45 by 20 p.m. Magnification, x 160.

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INTESTINAL CAPILLARIASIS 123

FIG. 5. Larva of C philippinensis from the intestines of a fish.Note the formation of stichocytes in the anterior end. Magnification,xlOO.

ments were subsequently carried out with the gerbil, and theunique life cycle of C. philippinensis was determined.When larvae from fish were administered by stomach tube

to gerbils, the larvae developed into adult males and femalesin 10 to 11 days and female worms started to releasefirst-stage larvae in 13 to 14 days. These larvae developedinto adult males and females in 22 to 24 days, and thesecond-generation females began to release thick-shelledunembryonated eggs, which passed in the feces in 25 to 35days postinfection. Most female worms at this time wereoviparous, but a few female worms always produced larvae,an event that led to autoinfections and hyperinfections. Inother studies only two larvae from fish were fed to gerbils,and on two occasions 2,520 and 5,353 worms in all stageswere recovered from gerbils that died after 46 and 47 days.Other studies were done by administering three larvae fromfish, and 852 to 5,253 worms were recovered (10). It was alsoestablished that female worms could switch from oviparousto larviparous reproduction when transferred from anecropsied infected gerbil to a clean gerbil. The larvaedeveloped into adults and produced eggs that passed in thefeces.

In studies in Thailand (3) and Taiwan (11), fish-eating birdswere infected with larvae from fish or were fed infected fish.It is now believed that fish-eating birds are natural hosts andthat the cycle is a fish-bird life cycle. However, humans canbecome infected when they eat the tiny fish that are usuallyconsumed by birds. One bird has been found naturallyinfected with the parasite in the Philippines. The proposedlife cycle is presented in Fig. 6.

CLINICAL PICTURE

Few intestinal nematode infections actually cause diseasethat leads to death in their host. Most parasites live unmo-lested in the gut and at the same time do little to disturb theirenvironment and the gracious host. C. philippinensis, how-ever, is different; it always causes illness as far as we know,and, if the infection remains untreated, it leads to death. Onnumerous occasions we detected individuals passing eggs intheir stools during surveys. Most were asymptomatic andwould not report to the hospital for recommended treatmentwhen told of their infections. Invariably, they developedsymptoms as the worm population built up, and they thenreported for treatment (17).

4

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3 weeks 4

FIG. 6. Proposed life cycle of C. philippinensis based on exper-imental infection in Mongolian gerbils. Reprinted from reference 14with permission of the publisher.

Symptoms

The first patients seen in the endemic area with intestinalcapillariasis had been suffering from abdominal pain, agurgling stomach (borborygmus), and intermittent diarrheafor several weeks. They eventually had 8 to 10 voluminousstools daily and lost a considerable amount of body weight.Some suffered from malaise, anorexia, and vomiting. Studiesby Whalen et al. (25) reported physical findings of musclewasting and weakness, borborygmus, distant heart sounds,hypotension, gallop rhythm, pulsus alterans, abdominal dis-tention and tenderness, edema, and hyporeflexia. There wasno hepatosplenomegaly or jaundice. Laboratory findingsshowed severe protein-losing enteropathy, malabsorption offats and sugars, decreased excretion of xylose, and lowlevels of potassium, sodium, calcium, carotene, and totalprotein in serum. There were usually high levels of immu-noglobulin E (IgE) and diminished levels IgG, IgM, and IgA;several months after treatment, however, all immunoglobu-lin levels returned to normal (21). Patients ill for more thanseveral months without treatment usually died either of theirreversible effects of the electrolyte loss resulting in heartfailure or of septicemia due to a secondary bacterial infec-tion.

Patients seen in the endemic areas at present usually havemild symptoms of borborygmus, abdominal pain, diarrhea,and edema. After treatment, the symptoms disappear in afew days to a week and eggs and other stages of the parasiteare no longer present in the stools. It is important thatsymptoms are recognized early and treatment initiated. Oneof the last patients to die of the infection had been misdiag-

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CLIN. MICROBIOL. REV.

FIG. 7. Human intestinal tissue at autopsy showing multiple histologic sections of C. philippinensis. Female worms with eggs in the uterusare visible. Magnification, x63.

nosed at several hospitals as simply having gastroenteritis.By the time the correct diagnosis was made, it was too lateto alter the course of his infection.

PathologyFewer than 15 autopsies have been done on Filipinos who

died of intestinal capillariasis (5, 18). Their bodies wereemaciated, dehydrated, and pale. Serous fluid was found inthe peritoneal and pleural cavities. The heart weights werewithin normal limits with minimal pericardial fat. The lungswere congested. Bacteria (Micrococcus pyogenes [sincerenamed Streptococcus pyogenes] and Klebsiella pneumo-niae) were cultured from the lungs of two patients. Thesplenic white pulp was conspicuous because of prominentmalpighian corpuscles, and the livers were yellowish. Thekidneys were reduced in weight, and there was cerebralvascular congestion.

Most pathologic changes were found in the small intestine,especially the jejunum. Numerous C. philippinensis wormsin all stages were found in the lumen (Fig. 7 through 9) andin the intestinal mucosa (Fig. 10 and 11). In 1 liter of bowelfluid from one autopsy an estimated 200,000 worms wererecovered. Although most worms are found in the jejunum,some are found throughout the digestive tract, probably as aresult of postmortem migration. The parasite was found oncein extraintestinal tissue, in a section of liver (18).

Histologic findings were fatty metamorphosis of the liverand vacuolization of the cytoplasm of renal proximal convo-luted tubular lining cells. Hemoglobin pigments were alsofound in the tubules of some patients. Vacuolization ofmyocardial cells and concentrations of lipochrome pigmentin the myocardium were also seen. In the intestines, thecrypts of Lieberkuhn were atrophied and often containedparasites (Fig. 10 and 11) and cellular debris. The intestine

FIG. 8. First-stage larva of C. philippinensis recovered from the human intestine at autopsy. Magnification, x 160.

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INTESTINAL CAPILLARIASIS 125

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W.hFIG. 9. Third-stage larva of C. philippinensis recovered from the human intestine at autopsy. Magnification, x63.

also showed flattened denuded villi and dilated mucosalglands, and the lamina propria was infiltrated with plasmacells, lymphocytes, macrophages, and neutrophils.

Electron micrographs of biopsied jejunal tissue showedloss of adhesion specialization and widespread separation ofepithelial cells. In gerbil tissue taken at necropsy and studiedby electron microscopy, the following changes were seen: (i)microulcers in the epithelium (Fig. 12), (ii) compressivedegeneration and mechanical compression of cells, and (iii)homogeneous material at the anterior end of the worm (Fig.13). These ulcerative and degenerative lesions in the intes-

FIG. 10. FemaleMagnification, x63.

tinal mucosa may account in part for the malabsorption withloss of fluids, protein, and electrolytes (23).

Diagnosis

Patients presenting with borborygmus, abdominal pain,diarrhea, and weight loss are usually passing eggs (Fig. 4),larvae (Fig. 8 and 9), and/or adult worms (Fig. 1 through 3)in their feces. Larvae found in the feces are in all stages ofdevelopment and are difficult to identify as C. philippinensis(Fig. 8 and 9), but adult males and females have character-

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C. philippinensis (Cp) in crypts (Cr) of human intestinal tissue at autopsy. Note the larva (Lv) in the uterus.

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CLIN. MICROBIOL. REV.

t) 4

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FIG. 11. Sections of C philippinensis (Cp) in human intestinal tissue at autopsy. Magnification, x 160.

istic features (Fig. 1 through 3). An inexperienced observermay confuse the eggs with those of T. trichiura, which arelarger (50 to 54 by 22 to 23 ,um) and barrel shaped, withprominent mucoid bipolar plugs. Figure 14 shows C. philip-pinensis and T. tnichiura eggs for comparison. Multiplestools may have to be examined in some patients. Theparasite may also be found in material obtained by small-intestinal aspiration or biopsy. If intestinal capillariasis issuspected but not parasitologically confirmed, the patientshould be given an anthelminthic agent. The parasite usuallypasses in the feces for a few days following treatment.Serologic tests have been evaluated but are considered

unreliable (2, 16) and not necessary since eggs and wormsare usually found in stool specimens.

Treatment

In the early days of the Philippine epidemic, all availableanthelminthic agents were given to infected persons; how-ever, thiabendazole in dosages of 25 mg/kg/day or 1 g/day for30 days eventually became the drug of choice. Most patientsresponded well, but there were side effects and many re-lapses. In the second and third years of the epidemic, therewere more relapse cases than new infections (22). One

FIG. 12. Electron-microscopic view of a cross-section of C. philippinensis obtained from gerbil jejunum. Note the cuticular pore (CP) ofthe worm and dissolution of the plasma membrane and cytoplasmic organelles of the epithelial cell (arrow) opposite the cuticular pore.Magnification, x 12,500. Reprinted from reference 23 with permission of the publisher.

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INTESTINAL CAPILLARIASIS 127

FIG. 13. Electron-microscopic view of the penetrating site of theparasite (P) in gerbil jejunal epithelium. Note the electron-densehomogeneous material (arrow) at the anterior end of the parasite inconnection with two large vesicles (V) at both sides of the worm.The basal lamina (BL) below the oral tip of the nematode appearsdeteriorated. Epithelial cells (EC) at the right side are compressedwith increased compactness of the cytoplasmic organelles. A lym-phocyte (L) is seen between the cells. Magnification, x 7,500.Reprinted from reference 23 with permission of the publisher.

patient had 15 relapses in a 12-year period (1). Patients withsevere disease are given electrolyte replacement therapy, anantidiarrheal agent, and a high-protein diet.Mebendazole at 400 mg/day in two divided doses for 20

days soon replaced thiabendazole. In patients with relapsesthe drug was given for 30 days and there were few subse-quent relapses. Albendazole is presently the drug of choicein a dose similar to that for mebendazole, but is administeredonly for 10 days. Treatment for less than 10 days has resultedin relapses in some patients. It is believed that relapses resultfrom the inability of thiabendazole and mebendazole toaffect the larval stages. The adults are affected, and as thelarvae mature, they are susceptible to the drugs. Albenda-zole, on the other hand, appears to act on the larvae as wellas the adults. After therapy with most drugs the parasites arenot found in the feces after 4 days. If treatment stops at thistime, the parasite and eggs will reappear after 20 to 30 days.

EPIDEMIOLOGY

Distribution and PrevalenceFrom 1967 to the end of 1990, 1,884 confirmed cases of

intestinal capillariasis were documented and 110 people died(Fig. 15). Through the years, twice as many males, mostlymiddle-aged, as females have become infected (Fig. 16). Afew infections were reported elsewhere, and in the early1980s a new endemic area was identified in Southern Leyte

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FIG. 14. Eggs of C. philippinensis (Cp) compared with an egg of T. trichiura (Tt). Magnification, x 160.

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CLIN. MICROBIOL. REV.

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YEARFIG. 15. Intestinal capillariasis cases (total, 1,884) and deaths (total, 110) recorded in Northern Luzon in the Philippines from 1967 through

1990.

in the Central Philippines. In a preliminary stool survey, 14%of 362 specimens contained C. philippinensis eggs, larvae,and adults (13).As far as we know, intestinal capillariasis was first re-

ported from Bacarra, Ilocos Norte, in the Philippines. Thefirst epidemic occurred in Pudoc West in Ilocos Sur, andinfections were subsequently seen in persons from provincesup and down the Philippine coast along the South China Sea.A focus of infection was found near a U.S. Naval Base inZambalas (24), and the subsequent epidemic occurred inSouthern Leyte. Only sporadic cases are seen today inNorthern Luzon.

Capillariasis philippinensis was first recognized in Thai-land in 1973 (20), and additional cases were reported there-after. The disease seems to be widespread in Thailand, withcases being seen at many medical centers in the north andnorthwest and around Bangkok. No effort is being made todocument the infections, however. An epidemic is known tohave occurred in 1981; more than 100 persons acquired thedisease and 9 died of the parasitosis (15).

C. philippinensis infections are now being seen in Japan,with three cases reported, followed recently by a fourth (la).

350- 18% Northem Luzon, PhilippinesFebruary 1967 - December 1990

X 300-LU 14% U 1334 Males (70%)250-| E 550 Females (30%)C°) = LLL .11%

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FIG. 16. Intestinal capillariasis cases (1,884) reported in North-ern Luzon in the Philippines by age and sex from 1967 through 1990.

Iran and Taiwan have each had one case (7), and Egyptianworkers have documented two cases (19).

Transmission

The eating habits of people are responsible for the trans-mission of human C. philippinensis. Populations in thePhilippines where intestinal capillariasis occurs have uniqueeating habits in that they prefer to eat a variety of foodsuncooked. The Ilocanos of Northern Luzon relish rawanimal organs, and intestinal juices from animals are used toseason rice and other foodstuffs. They also eat raw crabs,snails, clams, shrimp, squid, goat, and water buffalo meatand a variety of small freshwater and brackish-water fishabundant in lagoons along the coast. The fish are too small toeviscerate and so are eaten whole. The people especially liketo eat female bagsit (Hypseleotris bipartita) (Fig. 17) whenfilled with roe. Thai populations also enjoy eating smallfreshwater fish and crabs uncooked. In other countriesreporting the infections, consumption of raw fish has beenassociated with most infections.

Since a number of species of freshwater fish have beenexperimentally infected with C. philippinensis and some fishin the Philippines were found naturally infected with larvalforms of the parasite (15), it is believed that the means of

MpII-,

FIG. 17. Bagsit (H. bipartita), a fish often eaten uncooked,especially when gravid, by Ilocano populations of Northern Luzonin the Philippines. The fish is usually only 2 to 3 in. (5.1 to 7.6 cm)in length. This species was found naturally infected. When these fishwere fed to Mongolian gerbils, patent infections developed and thegerbils died.

1037 Northern Luzon, Philippines

February 1967 - December 1990

291 F11 Cases

| Deaths

7465 6556

41 3

10 121968LI L[HUH WII 96 26

AGE GROUP 1-9 10-19 20.29 30.39 40.49 50-59 60.69 70-79 80-89COMBINED 7%o 14% 23% 19% 17% 12%h 6% 1% 1%

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INTESTINAL CAPILLARIASIS 129

transmission of capillariasis philippinensis is by eating un-cooked fish. The parasite has not been found in any areawhere the populations do not eat raw fish.

Several species of fish-eating birds have now been exper-imentally infected with the parasite (3, 11), and one bird(Ixobrychus spp.) has been found naturally infected in thePhilippines. Birds, especially migratory fish-eating birds, areconsidered potential natural hosts, and their migratory hab-its are considered responsible for dissemination of the par-asite to widely separated parts of the world (7). Bird drop-pings along the flyways could easily disperse the eggs intowater bodies, where fish become infected. Birds, as well ashumans, eating such fish would subsequently become in-fected.

Control

Sanitation in rural areas of the Philippines and Thailand isconsidered poor. There is indiscriminate defecation, andalthough indoor toilet facilities may be available, they maynot be fully used. During the epidemic in Pudoc West in thePhilippines, bed sheets soiled with feces from patients wereusually washed in the lagoons, thus depositing eggs into thewater and exposing the fish to infection. This practice maybe the reason for more than 200 cases of intestinal capillar-iasis occurring in the village. Drinking water comes fromwells and other natural sources and is rarely boiled orchemically treated. The people like to eat animals raw, andwhen asked why they do it, they explain that their ancestorsdid it, that it is a habit, and that in their opinion raw food ismore nutritious.

Control of this parasitosis is simple; it consists of noteating raw fish. This habit is difficult to end when it has beenpracticed for generations. Educational programs warning ofthe dangers associated with eating raw fish have been of littlehelp. Cooking the fish for a short time would be sufficient tokill larvae in the intestines, but most people prefer the fishraw. Early diagnosis and treatment are recommended toprevent serious disease and death. Early treatment withmebendazole or albendazole has been very effective, anddeaths are now rare.

Infections continue to be reported sporadically in thePhilippines and Thailand, and in the future the disease willvery probably continue to be reported from Japan and Egyptand possibly other areas of the world.

REFERENCES1. Alcantara, A. K., C. V. Uylangco, and J. H. Cross. 1985. An

obstinate case of intestinal capillariasis. Southeast Asian J.Trop. Med. Public Health 16:410-413.

la.Ando, K. 1991. Personal communication.2. Banzon, T. C., R. M. Lewert, and M. G. Yogore. 1975. Serology

of Capillaria philippinensis infection: reactivity of human serato antigens prepared from Capillaria obsignata and other hel-minths. Am. J. Trop. Med. Hyg. 24:256-263.

3. Bhaibulaya, M., and S. Indra-Ngarm. 1979. Amaurornis phoen-icurus and Ardeola bacchus as experimental definitive hosts forCapillaria philippinensis in Thailand. Int. J. Parasitol. 9:321-322.

4. Bhaibulaya, M., S. Indra-Ngarm, and M. Anathapruit. 1979.Freshwater fishes of Thailand as experimental intermediate hostfor Capillaria philippinensis. Int. J. Parasitol. 9:105-108.

5. Canlas, B. C., B. D. Cabrera, and U. Davis. 1967. Human

intestinal capillariasis. II. Pathological features. Acta Med.Philipp. 4:84-91.

6. Chitwood, M. B., C. Valasquez, and N. G. Salazar. 1968.Capillaria philippinensis sp. n. (Nematoda: Trichinellida) fromintestine of man in the Philippines. J. Parasitol. 54:368-371.

7. Cross, J. H. 1990. Intestinal capillariasis. Parasitol. Today6:26-28.

8. Cross, J. H., T. C. Banzon, M. D. Clarke, V. Basaca-Sevilla,R. H. Watten, and J. J. Dizon. 1972. Studies on the experimentaltransmission of Capillaria philippinensis in monkeys. Trans. R.Soc. Trop. Med. Hyg. 66:819-827.

9. Cross, J. H., T. C. Banzon, K. D. Murrell, R. H. Watten, andJ. H. Dizon. 1970. A new epidemic diarrheal disease caused by thenematode, Capillariaphilippinensis. Ind. Trop. Health 7:124-131.

10. Cross, J. H., T. C. Banzon, and C. M. Singson. 1978. Furtherstudies on Capillaniaphilippinensis: development of the parasitein the Mongolian gerbil. J. Parasitol. 64:208-213.

11. Cross, J. H., and V. Basaca-Sevilla. 1983. Experimental trans-mission of Capillania philippinensis to birds. Trans. R. Soc.Trop. Med. Hyg. 77:511-514.

12. Cross, J. H., and V. Basaca-Sevilla. 1984. Biomedical surveys inthe Philippines. NAMRU-2 SP47:1-117.

13. Cross, J. H., and V. Basaca-Sevilla. 1986. Intestinal capillaria-sis-current concepts, laboratory diagnosis and treatment.Asian J. Clin. Sci. 7:63-67.

14. Cross, J. H., and V. Basaca-Sevilla. 1989. Intestinal capillariasis.Prog. Clin. Parasitol. 1:105-119.

15. Cross, J. H., and M. Bhaibulaya. 1983. Intestinal capillariasis inthe Philippines and Thailand, pp. 103-136. In N. Croll and J. H.Cross (ed.), Human ecology and infectious diseases. AcademicPress, Inc., New York.

16. Cross, J. H., and J. C. H. Chi. 1978. The ELISA test in thedetection of antibodies to some parasitic diseases in Asia, p.178-182. In Current concepts in the diagnosis and treatment ofparasitic and other tropical diseases in Southeast Asia. Proc.18th SEAMEO TROPMED Semin., Kuala Lumpur, 2 to 5August 1977.

17. Detels, R., L. Gutman, J. Jaramillo, E. Zerrudo, T. Banzon, J.Valera, K. D. Murrell, J. H. Cross, and J. J. Dizon. 1969. Anepidemic of human intestinal capillariasis: a study in a barrio inNorth Luzon. Am. J. Trop. Med. Hyg. 18:676-682.

18. Fresh, J. W., J. H. Cross, V. Reyes, G. E. Whalen, C. V.Uylangco, and J. J. Dizon. 1972. Necropsy findings in intestinalcapillariasis. Am. J. Trop. Med. Hyg. 21:169-173.

19. Mansour, N. S., M. H. Anis, and E. M. Mikhail. 1990. Humanintestinal capillariasis in Egypt. Trans. R. Soc. Med. Hyg.84:114.

20. Pradatsundarasar, A., K. Pecharanond, C. Chintanawongs, and P.Ungthavorn. 1973. The first case of intestinal capillariasis inThailand. Southeast Asian J. Trop. Med. Public Health 4:131-134.

21. Rosenberg, E. B., G. E. Whalen, H. Bennich, and S. G. 0.Johansson. 1970. Increased circulating IgE in a new parasiticdisease-human intestinal capillariasis. N. Engl. J. Med. 283:1148-1149.

22. Singson, C. N. 1974. Recurrences in human intestinal capillari-asis. Philipp. J. Microbiol. Infect. Dis. 3:7-13.

23. Sun, S. C., J. H. Cross, H. S. Berg, S. L. Kau, C. Singson, T.Banzon, and R. H. Watten. 1974. Ultrastructural studies ofintestinal capillariasis Capillana philippinensis in human andgerbil hosts. Southeast Asian J. Trop. Med. Public Health5:524-533.

24. Tidball, J. S., J. P. Aguas, and J. W. Aldis. 1978. A newconcentration of human intestinal capillariasis on western Lu-zon. Southeast Asian J. Trop. Med. Public Health 9:33-40.

25. Whalen, G. E., E. B. Rosenberg, G. T. Strickland, R. A.Gutman, J. H. Cross, R. N. Watten, C. Uylangco, and J. J.Dizon. 1969. Intestinal capillariasis-a new disease in man.Lancet i:13-16.

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