KEYNOTE ADDRESS ON EMERGING PROBLEMS IN FOOD-BORNE PARASITIC ZOONOSIS: IMPACT ON AGRICULTURE AND PUBLIC HEALTH

Chirasak Khamboonruang

Department of Parasitology, Faculty of Medicine and ResearchInstitute for Health Science, Chiang Mai University, Chiang Mai, Thailand,

INTRODUCTION of hygiene in the food processing industry; and finally the appropriate application of food science Food-borne diseases can cause both direct and and technology iri food manufacture and process- indirect 'economic losses. The provision of 'clean ing' as well as in agricultural practices. food through enforceable food safety requirements In this overview, the public health aspects of afl'ects'many areas of human economic and social food-borne parasitic zoonoses, especially in Thai- activity . including agriculture, food manufacturing land, willbe reviewed.These parasitoses will have aDdprocessing,anirnal husbandry and the practice many feat'uteJ ~fscientific interestIorthosefrorn of veterinary medicine, (Waites and Arbuthnott, other countries. 1990). Unsafe 'and unclean 'foods may have to be withdrawn "frQIJl"sale and destroyed, baying a di.r,'~cteconqrnicimPllct on the food industry. FOOD-BORNE PARASITIC ZOONOnC Iadirecreconornic, distress occurs through a DISEASES IN THAILAND reductio.n or.Joss.of'income by those suffering These diseases can be categorized by their from a food-borne, illness. etiolegieal agents into four main'greups, namely, At-present; the emphasis <>0food-borne diseases protozoan, , trematode, and cestode is mainly confined to foods contaminated with infections. microbial organisms ,or their, toxins, but there has, been little .emphasis on food-borne p~r!l8itic PROTOZOAN INFECTIONS zionpSespr diseases acquired tbrOUib, the .elltm of ~wmats w~ch~arbol' these 'p~rasite~' Nqrt~~m' ToxoplasnrOsJs Thailand is highly endernic area for a l~ge number of animal parasitic infections that can be' trans- Northern Thais are fond of eating raw meat, mitted to man. Except for a fe,w. the clinical such as "lahb" and "nahm" - raw ~rk(jt ~f; aspects and treatment of these diseases have not however, toxoplasmc:>.sis.i$,rarely, .reported, Al- bteri' weD doeumentef4.6% by indirect hem~g- Be~vwr oLi:omnnmities in endemic .areas, in glutinationtest(IHA) and 1.2"/0 by indirect fluor- JW1i<:ular tl1eir.awal'eness of the disease,their escent antibOdy test (IF A), while in pregnant ~UQg, habit&;an4, changes in .diet are criticijl woman, 2.8% were positive by IHA (Morakote er fa~9r!h\ The imp~t .Qf parasitic zoonosis on al, 1984).,<\ survey of 60 cats in Chiang Mai apwul~ ,isi<>f, ~rn,. inoluc;Jinginarlcqllllte yielded l8A"AiPQsitive by the Sabin-Feldman ,dye inJpec.tio~ofJJlC$i;theneed for tougher standards test :(Mal!)eW<>nget(11, 1984). FOOD - BORNE PARASITIC ZOONOSIS

Intestinal sarcosporidiosis forage in the open, and in wild boar. The larvae A stool survey ,conducted in Nakhon Nayok, are rarely found in domestic pigs (Khamboonruang Phitsanulok andKalasin, representing thecentral, et ai, 1978). The parasite appears to be Trichinella northern, and northeastern regions of Thailand, spiralis rather than- other species (Pozioand yielded a prevalence of Sarcocystis hominis sporo- Khamboonruang, 1989). cysts of 3.76%, 1.1% and 2.97%, respectively, CapiUariasis (Ektasaeng et al, 1987). Six patients, four from the northeast and two from the north were admitted Human intestinal (Capillaria to Ramathibodhi Hospital in Bangkok with a philippinensis) causing chromic has been diagnosis of acute enteritis. Histopathological reported from several regions of Thailand. Man diagnosis was reported as either segmental eosino- acquires the infection from eating a raw fish dish philic enteritis or segmental necrotizing enteritis. called "koi-pla". Fresh-water fish were experi- Merozoite, microgamete, macrogamete, sporocyst mentally infected with the larvae (Bhaibulaya et and oocyst of Sarcocystis species were observed in ai, 1979). tissue sections. Because of the presence of Sarco- cystis cysts in the local beet and the habit of eating meat raw, it was postulated that the causative Human gnathostomiasis caused by agent was Sarcocystis bovihominis (Bunyaratvej et spinigerum is commonly reported in Thailand. ai, 1982). Third-stage larvae of the worm are commonly It another study, 99% of cardiac muscle of found in freshwater fishes; frogs and eels. Con- cattle from markets in Chiang Mai contained sumption of undercooked or raw flesh of second- Sarcocystis cysts of unknown species. (S Pan-In, intermediate hosts and paratenic hosts is the 1989, personal communication). major mode of transmission to humans.

Cryptosporidiosis Subcutaneous migratory swelling is the most common clinical feature, with worms also recovered Reports of the cryptosporidiosis in the past from the mucous membranes, conjunctiva, soft have been rare, but with the global spread of HIV palate, respiratory tract, eyeball, intra-abdominal (human immunodeficiency virus) infection, cases organs, and the central nervous system. Fatal are now reported. A prevalence of 9.26% was gnathostomiasis occurs when worms invade the reported among orphans from the "Home for central nervous system (Daengsvang, \.980). Boys" in Chiang Mai who were suffering from diarrhea (Morakote et al, 1990). Diagnosis. of gnathostomiasis is based on clinical signs, peripheral eosinophilia, and immu- nological tests. More sensitive and specific serolo- NEMA TODE INFECTIONS gical tests for diagnosis are needed. Specific drugs for treatment are also heeded. Trichinellosis Angiosttongyliasis Trichinellosis is widespread in northern Thai- or eosinophilic meningitis land. The first outbreak of the infection was is widely distributed in Thailand. Between 1965- recorded in Mae Sariang district in June 1962 1968,484 cases were reported (Punyaguptaet ai, (Boonthanom and Nawarat, 1963). To date, there 1970). The disease occurs in all age groups. with a have been 118 outbreaks, affecting some 5400 higher prevalence in the second and third decades. patients, 95 of whom have died (Chumkasian, Male farmers are at greatest risk. Infection occurs 1990). Patients usually acquire the infection by by eating raw or partially cooked Pi/a spp.snails. eating raw pork dishes called "lahb" and "nahm", Pi/a are usually eaten by people of lower socioeco- which are frequently served at traditional celebra- nomic levels, since it is an inexpensive source of tions. protein. They are also eaten while drinking The transmission cycle of alcoholic beverages. Twenty percent of Pi/a snails appears to be of the sylvatic type with larvae often in an endemic area were found infeCted with third- found in hill tribe pigs, which are allowed to stage larvae of Angiostrongylus ctmtonensis.

2 KEYNOTE ADDRESS

Twelve percent of rats were reported infected with viverrini (Changbumrung et al, 1989). In Thailand, adult worms. Sensitive and specific serological appears to have an immense tests are needed to support the clinical diag- public health and social and economic impact on nosis. the population. Fascioliasis In Thailand, fascioliasis is caused by Fasciola TREMATODE INFECTIONS gigantica and is enzootic in ruminants, eg, cattle infections and water buffaloes; the prevalence is about 80% (Bhodhi-ngoen, 1982).Nine human cases, involving Opisthorchiasis and F. gigantica have been Thailand is now recognized as having the reported (Kachintorn et al, 1988). Infections highest prevalence of human liver fluke infections reported from man are mostly found as ectopic in the world. In the northeastern Thailand the fascioliasis, ie, breast abscess. Man acquires the in- overall prevalence rate is about 35%, involving fection by eating metacercariae-infected water- about 7 million persons (Preukraj, 1984). The cress and water hyacinth. habit of eating raw fish, called "koi-pla", and salted fish called "pla-ra", is the source of infec- Lung Fluke Infections tion. The infection is found in young people and increases with age. Immigration of infected people from northeast to the north impacts on prevalences. There are at least six species of Paragonimus in In Chiang Mai Province, the prevalence was Thailand: ., P. hetero- reported' to be as high as 37% (Yamaguchi et al, tremus, P. siamensis, P. bangkokensis, P .. harina- 1982). The northerners acquirethe infection from sutai, and P. macrorchis. The natural hosts are eating raw-fish dishes call "lahb-pla" and "pla- felines and rats. Seven adult mature Paragonimus som". heterotremus were recovered from a 40 year old Thai farmer from Nakhon Nayok Province, central Snails-of the genus Bithynia are the major first- Thailand, who coughed up the worm after treat- intermediate host of . These ment with praziquantel (Vanijanonta et ai, snails are found predominantly in rice fields in the 1981). north and the northeast. Many species of cyprinoid fishes serve as second-intermediate hosts. In some Human is prevalent in central, endemic localities, fish were found to have infec- northern and northeastern parts of Thailand. Two tion rates of 94% to~%. Dogs and cats are the endemic 'areas are in the central region, Saraburi major reservoir hosts. Province (Vajrasthiraet al, 1958) and Nakhon Nayok Province (Sirisumpun, 1963). In the north, The clinical picture of opisthorchiasis varies. there was one small focal area in Chiang Rai, the The mild cases have symptoms of dull abdominal northernmost province. However, sporadic cases pain and abdominal discomfort, eg, anorexia and have been recorded scattered throughout the flatulence. Liver and gallbladder enlargement is north and mostly from mountainous villages(C infrequently found. Hematological parameters Khamboonruang, unpublished data). Recently, and clinical chemistry are within normal limits, one endemic area has been reported from the except that some persons show peripheral eosino- north in Phitsanulok Province (Phanarunothai et philia(WykofT et al, 1966). Severe disease, with 01; 1988).Man usually acquires the infection from symptoms and' signs of obstructive cholangitis, is eating raw mountain stream crabs (Potamon and rare.Cholangiocarcinoma associated with. O. Parathelphusa spp.) containing metacercariae, in a viserrini infection has been reported. In the Udon favorite ethnic dish called "pla-poo". Thani.Provincial Hospital in an endemic area, 8 out of 11 cases of opisthorchiasis found in an autopsy had coexistent, cholangiocarcinoma Intestinal Fluke Infections (Sonakul et al, 1978). Serum bile acidsvalpha- fetoproteins, etc, are tumor markers for the early " Intestinal flukes are one of the most important detection .of cholangiocarcinoma caused by O. food-borne parasitic zoonoses found in the north,

3 FOOD - BORNE PARASITIC ZOONOSIS northeast and central parts of Thailand. Fourteen differentiate. Four species,' Haplorchis taichut, H. species'have been reported. The distribution yokogawai (Manning et al, 1971), H.pu~ilio depends on the presence of the first and the second (Rodomyos et al, 1984) and Stellanthchasmus intermediate hosts and eating habits of the local falcatus (Klicks and Tantachamrun, 1974). have people. been recovered from Thais. Man acquires the infection from eating raw fresh-water fishes, especially cyprinoids. No definite clinical symptoms The endemic area is restricted to central and signs have been described. Thaillinll, where, approximately 10,000 people are Lecithodendriasis ' infectedwith buski. Pigs appear to be the only reservoir host, Planorbidsnails the first- Lecithodendrid flukes (Phaneropsolus bonnei ' intermediate host, and five species of water plants and Prosthodendrium molenkampi} were recovered are important second-intermediate hosts. The from Thais in the northeastern part of the country water plants are caltrops (Trapabicornis), lotus (Manninger ai, 1971). Man acquires the infection (Nymphaea lotus); watercress (Neptunia oleracea], from eating infected naiads of the dragonfly morning glory (Ipomeoae aquatica), and hyacinth mixed in chilipaste. Rice field' crabs are also (Eichhornia speciosa) (Manning et al, 1969). second-intermediate hosts. ', Man acquires the infection from eating metacer- cariae-laden nuts and vegetables. CESTODE INFECTIONS , . Light infection causes diarrheawith a foul smelling feces,' ano'he!lVY infection may result in malabsorption andintestinal obstruction. Meta- , the beef tapeworm infection bolic productsofthe WOmlS can cause intoxication is prevalent throughout the counw. It is predom- and death (Daengsvang and Mangalasmaya, 1941). inantly found in .thenorthand.northeast of Thailand where the people are fond of eating raw Echinostomiasis meat. In contrast, infection due to , Human echinostcmiasishas been sporadically the pork tapeworm, is seldom foul'ld. InChiang recorded in Thailand, with infections caused by Mal Province, the incidence of taeniasis by stool Echinostoma malayanum, Hypoderaeum conoideum examination was about 3% (Yamaguchi 'et ai, (Bhaibulayaet ai, 1964), Erevolutum; Ellocanum 1982). The reported prevalence is low possibly (Radomyos et al, 1982, .t984), and Epis,thmium due to an inappropriate technique used to deter- cartinum '(Radomyoset al. 1985), Ducks •.rats. and mine the' infection. Flatulence and a gurgling dogs .are natural hosts. Planorbid snails serve as sound in the bowe1are major complaints. major first" and second-intermediate hosts. Man acquires the infection from consumption of raw snails, tadpoles and fish containing the meta- ,Cysticercus bovis in cattle is frequently found cercariae. The disease is asymptomatic. in slaughterhouses. Cysticercus cellulosae ~in pigs, on the other hand, is not as common as it was in Plagiorcbiasis the past. This may be due to ,the large number Four cases of plagiorchiasis have been found of commercially-raised grain-fed pigs being in northeastern Thailand but the species identifi- slaugbtered. However,c. cellulosae is sporadical- cation has not been made. In Thailand, Plagiorchis ly found in domestically raised pigs, illegally siamensis has been recovered from a rat (Yama- slaughtered in rural communities in the north, shita, 1967). The infection may be acquired by Cysticercosis is common in man in Thailand. eating raw snails. No typical clinical picture has The cyst is frequently located in' subcutaneous been described. tissue as asmallfirm nodule: Symptoms and signs Heterophyiasis of cysticercosis depend on the affected organ. However, neurocysticercosis is a major cause of The prevalence of heterophyid fluke infection epileptic convulsions, and increased intracranial in Thailand is masked by.opisthorchiasis viverrini pressure, severe headache, nausea, and vomiting. because the eggs of the flukes are difficult' to Surgical removal of the cyst is an appropriate

4 KEYNOTE ADDRESS treatment. Praziquantel has been used for the and Loahaphan, 1986). Man may acquire the treatment of neurocysticercosis with steroids infection from eating raw snake meat. administered concomitantly (Kanchanapongkul, 1989). Neurocysticercosis can also be diagnosed CONCLUSION by computerized tomography (CT scan), and sensitive and specific serological tests. Thais are exposed to a variety of animal parasites through the eating of animals and animal It is reported that Taenia in Thailand may be by-products. Despite the availability of methods similar to Taenia from Taiwan, Korea, and for prevention and control, deeply rooted socio- Indonesia, but different from T. saginata and cultural practices and traditions often defy any T. solium (Fan et al, 1990). change; even one aimed at improving health and wellbeing. Lack of adequate information on epidemiology, The common Pseudophillidian tapeworm in diagnosis, treatment and prevention and control Thailand is Spirometra mansoni. Definitive hosts are important in the control of food-borne para- are dogs and cats, with the pleurocercoid found sitic zoonoses. During the days ahead, we will mostly in water snakes, fishes and frogs. In human discuss and share our common problems with the sparganosis, the larvae are almost always found in purpose to formulate a series of recommendations subcutaneous tissue or in tissues around the eye for research aimed at solving the problems in the (Jenchitu et al. 1989). A case of sparganosis, in food-borne parasitic zoonosis. Our ultimate goal, which the worm was found free in the peritoneal consistent with the WHO recommendation of cavity beneath the appendicial fossa, was reported "Health for all by the Year 2000", will be to by a medical student in Chiang Mai (Khamboon- create communities that enjoy a better quality of ruang et al. 1974). life. Man is believed to acquire the infection from eating raw fish and frogs. Snake meat is commonly REFERENCES used as a poultice in traditional treatment of subcutaneous abscesses and skin ulcers and other Bhaibulaya M, Indra-Ngarm S, Anunthaprutti M. wounds. Another possible source of transmjssion Fresh water fishes of Thailand as experimental is drinking water containing copepods infected intermediatehost for Capillaria philippinensis. Int J with procercoids. Parasitol 1979; 9 : tos-s. BhaibulayaM, Chareonlarp P, Harinasuta C. Report of Acanthocephala infection· casesof Echinostoma malayanum and Hypodereaum Three cases of Macracanthorhynchus hirudi- conoideum in Thailand. J Med Assoc Thai 1964; 47 naceus, a thorny-headed worm of pigs, were : 720. reported from Thailand (Tesana et al. 1982). Bhodi-ngoen S. Veterinary helminthology. Bangkok: All patients were from the northeast. Chulalongkom UniversityPress, 1982 : 32. Various adult dung beetles and grubs serve BoonthanomP, Nawarat A. The outbreak of at Mae Sarieng.Bull Public Health (Thailand)1963; as an intermediate host. Man acquires the infection 33 : 301-8. by eating beetles containing the infective stage orcystacanth which have not been thoroughly Boonyaratve] S, Bunyawongwiroj P, Nitiyanant P. cooked. The thorny-head of the worm becomes Human intestinal sarcosporidiosis: Report of six cases. Am J Trop Med Hyg 1982; 31 : 36-41. embedded in the intestinal wall, producing local inflammation with eosinophilic infiltration and Changbumrung S, Migasena P, Tungtrongchitr R, necrosis. Perforation of the gut at the site of Prayurahong B. Biochemical parameters in attachment is common. opisthorchiasisand cholangiocarcinoma.Proceed- ings of the workshop on development of early Pentastomiasis diagnosisand managementof cholangiocarcinoma associated with opisthorchiasis.Faculty of Tropi- Six cases of human pentastomiasis have been cal Medicine,Mahidol University,Bangkok,Thai- reported from Thailand. The nymphs were re- land, January 9-11, 1989. Sommani S and Bunnag covered during intra-abdominal surgery (Tesiareon T, eds. pp: 75-102.

5 FOOD - BORNE PARASrtIC ZOONOSIS

Chumkilsian P. Record of outbreaks oftrlcirinel1osis in Manning OS, Sukhawat K;' Viyanant V, Subhakiii M, Thailand from J962 - May 1990. -Statistieal Report, -.Lertprasert P. Fascio{o'pSiS buski in Thailand;wiih Division of Epidemiology, Department of Com- comment on other intestinal' parasites;' J' Med municable Di~< Control, Ministty of Public A3S0C Thai 1969; 52 :90>.-14 .. Health, Thailand, 1990. •Manrii~g GS, Lertprasert P, Watan~~;.mkit J{ ~~d :Pa,enpv~qg ~. t\ m~n~,gr.~ph91ltQegepWi,Gnqt~Q;toma Chamroen C. A' description of newly-discovered ,"<''and~athoStomiasis' in Thailand. Tokyo: SE-t\MIC, inte~tinalparasit~sepde!l1ic to.Northeastern '.~ '-r980.,r' .<' . ·I.·_.~- ," ';' .. ThaiJand. J Me4AssQC Thai 1971; 54 :,464-74.

,Il~ngsvang S•.MangalasmaYII M. A record, of SOme : ". - -.-' , - ,.-, .' Morakote N, Thamasontbi W. CharuchindaK •.Kham- . , .. ~ of human. i~fQStation with Fasciolopsis bll-f/{i boonruang C. Prevalen~ of Toxoplasma ~ntlbodies occurring in Thailand, Ann TrQP Me4 Pa,r(J{JitQI Southeast ,4$i(1n 1941; 35 : 43. in Chiang Mai population. l[rpp Med Public Health 1984; 15: 80-5. , , .: Ektasllen~IU:'B~ail>ulaya~,Suwankul S, KoeWIDanee Morakote N, JuiltraprasCiifJ;Srikaew S, Wongsa~asdii "S; B'halldhuprap,as Incidence of intestinal ,Po L.Crj>ptosPQridium'atld Giardia infectionsattiorig parasific'in(ec'tions'i'o'some provinces 'in the orphans in the Home for Boys; ChiallgMai; Chittng northeast,' central and north of Thailand: (Thai Mar Med Bull 1990;'29 : 41-4. with Engab$tr). J 'Parasit Trap Med A,y$Oc .Thai 1987; 10: '15'-27. PhanarunothaiS, Sukmuong U, Tiloklert ' M',' 'et al. Endemic area of paragonimiasis at Amphur FanPC,Chung' W~,Lin CY,'Wu Cc. Experimental Nernmaprang, Pitsanlllok Province. ReglDn6·Med infection of"ThailaridTaenia (Chiengmai strain) 'in J(Ministry of Public Health of ThaiJand) 1988; 2< domestic animals. hii J Paraiit()i'i990; 20':121-3. 1~8; . '. - Jenchitu W. Chaijukool S, Ying-Yuad r. Ocular Pozio E, Khamboonruang C. 'Trichinellosis-in Thailand: sparganosis in Lampang, Thai J OpiuhalmQ/1989; Epidemiology and. biochemical identification of 3 (I) : 21-5. the etiological agent. Trop Med Parasitol 1989; 40: 73"4.'" ' . Kachintom U. Atisook K. Tesjaroen S, Lertakyamanee N, Plengvanit V, Fasciola gtgantica: The second Preukraj S.. ~blicl;J.ealth .aspects ~f. opisthorchis in case of human infection in Thailand. J Med ASSQC in Thailand. Arzneim-Forch Drug Res 1984; Thai 1988; 71 : 451-4: ' 34:1Ir'9. . . .'

Kanchanapongkul C. Cysticercus cellulosae=ui the Punyagupta S, Bunnag T, Juttijudata P,. Rosen L. central nervous system (In Thai). Clinic 1989; 5 : Eosinophilic meningitis in Thailand. Epidemiolo- 29-34. gical studies of 484 typical cases and' the etiologic role of Angiostrongylus cantonensis: Am J. Trop Khamboonruang C; Thitasut P, Pan-In S. The rcles of Med Hyg 1970; 19: 950-8. pigs and rats in transmission of trichinellosis in northern Thailand. Proceeding of the Fourth Radomyos P, Bunnag D, Harinasuta T. Report of International Conference on Trichinellosis. August Episthmium caninum (Verma, 1935) Yamaguti 1958 26-28,1976, Poznan.Poland. Kim CW, Pawlowski (Digenea: Echinostomatidae) in man. Southeast ZS, eds. New England: University Press 1978, pp Asian J TrQP Med Public Health 1985; 16 : 545-50. 508-11. Khamboonruang C, Premasathian 0, Little MD. A Radomyos P, Bunnag D, Harinasuta. T.EchinQstQmt1 case of. intra-abdominal sparganosis in Chiang ilocanum (Garrison, 1908) Odhner, 1911. .infeetion Mai, Thailand. Am' J TrQP MedHyg 1974; 23 : in man in Thailand .. Southeast AsianJ Trop Med 538-9. Public Health 1982; 13 : 265'-9.

Klicks M, Tantachamrun T. Heterophyid () Radomyos P, Bunnag D, Harinasuta T:WoimS recovered 'parasites. of cats in north Thailand. with note on a in stool following praziquantel treatment. Arzneiml human case found at necropsy, Southeast Asian J Forch Drug Res 1984; 34 : 1215. Tmp Med P~/ic Health 1974; 5 :547-55. Radomyos P, Bunnag 0, Harinasuta T. Haplorchis Maleewong W, Pan-In S, Morakote N. Availability of pumilio (Looss) infection in man in Northeast Thailand. Southeast Asian J TrQP Med Public . accessary factor for Sabin-Feldmandye test and Health 1983; 4 : 2.23-6. seroprevalenee of ariti-toxoplasmaantibodies in Chiang Mai cats. Bull Chiang Ma; AssQC Med Sci Sirisumpan .P. Pulmonary paragonimiasis in Thailand. 1984; 17 : 103-12. J Med AssQC Thai 1963; 46 : 201-11.

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Sonakul S, Koompairochana C, Chinda K, Stitnimakam Pulmonary paragonimiasis with expectoration of T. Hepatic carcinoma with opisthorchiasis. South- worm: A case report. Southeast Asian J Trop Med east Asian J Trop Med Public Health 1978;9: 215-9. Public Health 1981; 12: IQ4.{). Tesana S, Mitrchai J, Chunsuttwat S. Acute abdominal Waites WM, Arbuthnott JP. Food-borne illness: An pain due to Macracanthorhynchus hirudinaceus overview. Lancet 1990; I : 722-4. infection: A case report. Southeast Asian J Trop Wykoff DE, Chittayasothom K, Winn MM. Clinical Med Public Health 1982; 13 : 262-4. manifestation of Opisthorchis viverrini infection Tesjaroen S, Loahaptan T. Pentastomida: the 5th report in Thailand. Am J Trop Med Hyg 1966; IS : case of porocephaliasis from Thailand. Med Counc 914-8. Bull Thai 1986; 15: 209-19. Yamaguchi T, Khamboonruang C, Inaba T et al. Vajrasthira S, Harinasuta C, Maiphoom C. Study on Studies on intestinal parasitic infection in Chiang helminthic infection in Thailand: the incidence of Mai Province, north Thailand. Jpn J Parasit 1982; paragonimiasis in the first recognized endemic 31 : 447-59. area. Jpn J Exp Med 1958; 29 : 159-66. Yamachita J. On Plagiorchis found in Thailand. Jpn J Vanijanonta S, Radomyos P,Bunnag D, Harinasuta T. Parasit 1967; 16 : 597.

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