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    Schematic map of northeast Thailand showing 24 sampling localities in 8 provinces.

  • 1

    Crook JR, Fulton SE, Supanwong K, 1968. Ecological studies on the intermediate and definitive hosts of Angiostrongylus cantonensis (Chen, 1935) in Thailand. Ann Trop Med Parasitol 62 :27–43.

    • Search Google Scholar
    • Export Citation
  • 2

    Namue C, Wongsawad C, 1997. A survey of helminth infection in rats (Rattus spp.) from Chiang Mai Moat. Southeast Asian J Trop Med Public Health 28 (Suppl 1):179–183.

    • Search Google Scholar
    • Export Citation
  • 3

    Pipitgool V, Sithithaworn P, Pongmuttasaya P, Hinz E, 1997. Angiostrongylus infections in rats and snails in northeast Thailand. Southeast Asian J Trop Med Public Health 28 (Suppl 1):190–193.

    • Search Google Scholar
    • Export Citation
  • 4

    Lv S, Zhang Y, Steinmann P, Zhou XN, 2008. Emerging angiostrongyliasis in Mainland China. Emerg Infect Dis 14 :161–164.

  • 5

    Dissanaike AS, Ihalamulla RL, Naotunne TS, Senarathna T, Withana DS, 2001. Third report of ocular parastrongyliasis (angiostrongyliasis) from Sri Lanka. Parassitologia 43 :95–97.

    • Search Google Scholar
    • Export Citation
  • 6

    Campbell BG, Little MD, 1988. The finding of Angiostrongylus cantonensis in rats in New Orleans. Am J Trop Med Hyg 38 :568–573.

  • 7

    Bartschi E, Bordmann G, Blum J, Rothen M, 2004. Eosinophilic meningitis due to Angiostrongylus cantonensis in Switzerland. Infection 32 :116–118.

    • Search Google Scholar
    • Export Citation
  • 8

    Bronstein JA, Thevenot J, Tourneux M, 1978. Eosinophilic meningitis in Tahiti: clinical study of 54 patients. N Z Med J 88 :491–493.

  • 9

    Oku Y, Katakura K, Kamiya M, 1980. Tadpole of the clawed frog, Xenopus laevis, as an experimental transmission host of Angiostrongylus cantonensis. Am J Trop Med Hyg 29 :316–318.

    • Search Google Scholar
    • Export Citation
  • 10

    Radomyos P, Tungtrongchitr A, Praewanich R, Khewwatchan P, Kantangkul T, Junlananto P, Ayudhya SI, 1994. Occurrence of the infective stage of Angiostrongylus cantonensis in the yellow tree monitor (Varanus bengalensis) in five Provinces of Thailand. Southeast Asian J Trop Med Public Health 25 :498–500.

    • Search Google Scholar
    • Export Citation
  • 11

    Lai CH, Yen CM, Chin C, Chung HC, Kuo HC, Lin HH, 2007. Eosinophilic meningitis caused by Angiostrongylus cantonensis after ingestion of raw frogs. Am J Trop Med Hyg 76 :399–402.

    • Search Google Scholar
    • Export Citation
  • 12

    Bhaibulaya M, 1979. Geographical distribution of Angiostrongylus and Angiostrongyliasis in Thailand, Indo-China and Australia. Cross JH, ed. Studies on Angiostrongyliasis in Eastern Asia and Australia. A special publication of the U.S. Naval Medical Research Unit No. 2 Taipei, Taiwan NAMRU-2-SP-44. Taipei: L-C Publishing Company, 49–52.

  • 13

    Scrimgeour EM, 1984. Distribution of Angiostrongylus cantonensis in Papua New Guinea. Trans R Soc Trop Med Hyg 78 :776–779.

  • 14

    Ibrahim MM, 2007. Prevalence and intensity of Angiostrongylus cantonensis in freshwater snails in relation to some ecological and biological factors. Parasite 14 :61–70.

    • Search Google Scholar
    • Export Citation
  • 15

    Punyagupta S, Juttijudata P, Bunnag T, 1975. Eosinophilic meningitis in Thailand. Clinical studies of 484 typical cases probably caused by Angiostrongylus cantonensis. Am J Trop Med Hyg 24 :921–931.

    • Search Google Scholar
    • Export Citation
  • 16

    Kuberski T, Wallace GD, 1979. Clinical manifestations of eosinophilic meningitis due to Angiostrongylus cantonensis. Neurology 29 :1566–1570.

    • Search Google Scholar
    • Export Citation
  • 17

    Alto W, 2001. Human infections with Angiostrongylus cantonensis. Pac Health Dialog 8 :176–182.

  • 18

    Tsai HC, Liu YC, Kunin CM, Lee SS, Chen YS, Lin HH, Tsai TH, Lin WR, Huang CK, Yen MY, Yen CM, 2001. Eosinophilic meningitis caused by Angiostrongylus cantonensis: report of 17 cases. Am J Med 111 :109–114.

    • Search Google Scholar
    • Export Citation
  • 19

    Kliks MM, Kroenke K, Hardman JM, 1982. Eosinophilic radiculo-myeloencephalitis: an angiostrongyliasis outbreak in American Samoa related to ingestion of Achatina fulica snails. Am J Trop Med Hyg 31 :1114–1122.

    • Search Google Scholar
    • Export Citation
  • 20

    Chotmongkol V, Sawanyawisuth K, 2002. Clinical manifestations and outcome of patients with severe eosinophilic meningoencephalitis presumably caused by Angiostrongylus cantonensis. Southeast Asian J Trop Med Public Health 33 :231–234.

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    • Export Citation
  • 21

    Brandt RAM, 1974. The non-marine aquatic Mollusca of Thailand. Arch Molluskenkd 105 :1–423.

  • 22

    Upatham ES, Sornmani S, Kitikoon V, Lohachit C, Burch JB, 1983. Identification key for the fresh- and brackish-water snails of Thailand. Malacol Rev 16 :107–132.

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  • 23

    Chitramvong YP, 1992. The Bithyniidae (Gastropoda: Prosobranchia) of Thailand: comparative external morphology. Malacol Rev 25 :21–38.

  • 24

    Bhaibulaya M, 1979. Morphology and taxonomy of major Angiostrongylus species of Eastern Asia and Australia. Cross JH, ed. Studies on Angiostrongyliasis in Eastern Asia and Australia. A special publication of the U.S. Naval Medical Research Unit No. 2 Taipei, Taiwan NAMRU-2-SP-44. Taipei: L-C Publishing Company, 4–13.

  • 25

    Rambo PR, Agostini AA, Graeff-Teixeira C, 1997. Abdominal angiostrongylosis in Southern Brazil prevalence and parasitic burden in mollusc intermediate hosts from eighteen endemic foci. Mem Inst Oswaldo Cruz, Rio de Janeiro 92 :9–14.

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  • 26

    Tesana S, Srisawangwong T, Sithithaworn P, Laha T, 2008. Angiostrongylus cantonensis: experimental study on the susceptibility of apple snails, Pomacea canaliculata compared to Pila polita. Exp Parasitol 118 :531–535.

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  • 27

    Liu HX, Zhang Y, Lv S, Zhu D, Ang XH, Hu L, Zhou XN, 2007. A comparative study of three methods in detecting Angiostrongylus cantonensis larvae in lung tissue of Pomacea canaliculata. Zhongguo Ji Sheng Chong Xue Yu Ji Sheng Chong Bing Za Zhi 25 :53–56.

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  • 28

    Brockelman CR, Chusatayanond W, Baidikul V, 1976. Growth and localization of Angiostrongylus cantonensis in the molluscan host, Achatina fulica. Southeast Asian J Trop Med Public Health 7 :30–37.

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  • 29

    Graeff-Teixeira C, 2007. Expansion of Achatina fulica in Brazil and potential increased risk for angiostrongyliasis. Trans R Soc Trop Med Hyg 101 :743–744.

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  • 30

    Hochberg NS, Park SY, Blackburn BG, Sejvar JJ, Gaynor K, Chung H, Leniek K, Herwaldt BL, Effler PV, 2007. Distribution of eosinophilic meningitis cases attributable to Angiostrongylus cantonensis, Hawaii. Emerg Infect Dis 13 :1675–1680.

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    • Export Citation
  • 31

    Lv S, Zhou XN, Zhang Y, Liu HX, Zhu D, Yin WG, Steinmann P, Wang XH, Jia TW, 2006. The effect of temperature on the development of Angiostrongylus cantonensis (Chen 1935) in Pomacea canaliculata (Lamarck 1822). Parasitol Res 99 :583–587.

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  • 32

    Haswell-Elkins MR, Elkins DB, Sithithaworn P, Treesarawat P, Kaewkes S, 1991. Distribution patterns of Opisthorchis viverrini within a human community. Parasitology 103 :97–101.

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  • 33

    Sithithaworn P, Tesana S, Pipitgool V, Kaewkes S, Thaiklar K, Pairojkul C, Sripa B, Paupairoj A, Sanpitak P, Aranyanat C, 1991. Quantitative post-mortem study of Opisthorchis viverrini in man in north-east Thailand. Trans R Soc Trop Med Hyg 85 :765–768.

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    • Export Citation

 

 

 

 

Prevalence and Intensity of Infection with Third Stage Larvae of Angiostrongylus cantonensis in Mollusks from Northeast Thailand

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  • 1 Food-Borne Parasite Research Group, Department of Parasitology, Faculty of Medicine, Khon Kaen University, Khon Kaen Province, Thailand; Pharmacy and Medical Sciences, The University of South Australia, South Australia, Australia

Prevalences and intensity of infection with Angiostrongylus cantonensis third stage larvae were examined in mollusks to determine whether they are potential intermediate hosts in eight provinces, northeast Thailand. Mollusk samples were collected from 24 reservoirs (3 reservoirs/province) in close to human cases during the previous year. Six out of 24 localities and 9 (3 new record species) out of 27 species were found with the infection. The highest intensity in infected species was found to be only one or two snails, whereas the majority had very low or no infection. The highest density was found in Pila pesmei and the lowest in Pila polita. The edible snails, P. polita, P. pesmei, and Hemiplecta distincta have the potential to transmit A. cantonensis to man. The varying density levels of larvae in infected snails may reflect observed variation in symptoms of people who traditionally eat a raw snail dish.

INTRODUCTION

Angiostrongylus cantonensis is a rodent nematode, the adult worms living inside pulmonary arteries. Humans may become infected and migrating larvae and young adults may produce lesions mainly in the central nervous system. The natural definitive hosts are rodents, namely species of Rattus rattus, Rattus exulans, Rattus norvegicus, Bandicota indica, and Bandicota bengalensis.14 This parasite is distributed in Southeast and Far East Asia, including the Pacific and Indian Ocean islands.5 It is also found in South and North America continents,6 and there are many reported cases from Caribbean countries.7 The infective third stage larvae infests tissues of both fresh water and land snails, including slugs. Paratenic hosts include the reptile yellow tree monitor (Varanus bengalensis), prawns, the clawed frog (Xenopus laevis) and its tadpoles.811 It is possible that wide ranging species of snails could serve as intermediate host. Natural infection in fresh water snails was reported in Pila ampullacea turbines, Pila polita, Pila gracilis, Pila scutata, Pila pesmei, Pomacea canaliculata, Lanistes carinatus, Cleopatra bulimoides, Cleopatra cyclostomoides, Biomphalaria alexandrina, Lymnaea natalensis, and Melanoides tuberculata. Infection in slugs and land snails has been detected in Achatina fulica, Hemiplecta distincta, Hemiplecta siamensis, Veronicella siamensis, and Sarika resplendens.1,4,1114 Humans have acquired the infection by eating raw or improperly cooked snails, prawns, slugs, tadpoles, frogs, and yellow tree monitors.811 The most common symptom of infected patients was headache, in some cases they occasionally presented with a stiff neck, paresthesia, low-grade fever, nausea and/or vomiting. 1518 Many cases of ocular angiostrongyliasis resulted in visual disturbance and pain. 19,20 Inflammatory reaction in nervous tissues and cerebrospinal fluid is characterized by intense infiltration by eosinophils.

In the endemic areas in northeast Thailand, the infection in patients usually occurs in communities that eat a raw or undercooked dish of Pila snails while drinking alcohol. There is a possibility that severity of clinical disease is related to larvae burden. The aims of the present study are to describe the intermediate hosts for A. cantonensis in an endemic area in Thailand and to research the role of infected species for completion of the life cycle and transmission to humans.

MATERIALS AND METHODS

Preliminary survey.

A cross-sectional mollusk survey was carried out during May–December 2002 in northeast Thailand where there was a high incidence of human A. cantonensis infection based on the records of Department of Prevention and Control of Diseases, Ministry of Public Health (Annual Epidemiological Surveillance Report, 2001). A high incidence of infection was found in 12 provinces of northeast Thailand in areas under the supervision of 5th and 6th Offices of Prevention and Control Diseases. Three water reservoirs in each province (8 out of 12 provinces, 24 water reservoirs in total) with histories as the sources of infection reported in previous years were selected for mollusk sampling (Figure 1). The sampling method for mollusks collection was done by manual collection, scooping five times at the reservoir edge, and an Ekman dredge twice in deep water. Scoop collection (5 drags/station) was used in the station where there was a high density of water plants and manual collection (two persons for 5 minutes each station) was performed at the station when sand, soil, or rock areas were predominant. In each water reservoir, mollusks sampling was conducted at 8–11 sites depending on the size of each reservoir. Each site was sampled at two stations (8–22 stations in total), at the edge and deep water (1–4 meters). If the water level at that site was too shallow only one station was done. Land snails were collected by villagers living nearby the selected water reservoirs. The mollusk samples were identified to the species level by following Brandt, 21 Upatham and others, 22 and Chitramvong, 23 using characters of shell morphology and radular patterns. Each species of mollusk in the same station was processed as one sample to determine whether there was any A. cantonensis infection in each reservoir. This study has been reviewed and approved by the Animal Ethics Committee of Khon Kaen University, based on the Ethic of Animal Experimentation of the National Research Council of Thailand.

Density and intensity of larval infection.

At the reservoirs where mollusks were found to be positive for A. cantonensis larva, sampling was repeated as outlined previously. Once samples were identified to species of each individual, the shell was removed and the soft tissue of each snail was digested in a test tube or a beaker. The larvae were collected and the total number was recorded from each individual snail.

Digestion and collection of larvae.

Soft tissues of each snail were minced and digested with 0.25% pepsin A (BDH, England) in acid condition (pH 2.2) for 1 hour at 37°C in shaking water bath. The soft tissues almost completely digested for liberation of free larvae then digested solution was collected by the Baermann apparatus method and searched for larvae under a dissecting microscope (at 40×). Individual larvae were collected by fine tip Pasteur pipette and identified as A. cantonensis third stage larvae following Bhaibulaya. 24 Fifty larvae were used to infect white Wistar rats to confirm A. cantonensis species at the adult stage. After 1 month the infected rats were anaesthesized by diethyl ether then killed and the pulmonary artery was dissected and examined for adult worms.

RESULTS

Following preliminary sampling, snails were found to be positive for A. cantonensis third stage larvae in 6 out of 24 reservoirs, which were subsequently resampled at 8–22 stations depending on size and ecology of those reservoirs. In positive reservoirs, infected snails were only detected in 1 or 2 stations, in shallow rather than deep water stations. From preliminary and second surveys of 24 water reservoirs, 27 species were identified (sample size in parenthesis): Pomacea canaliculata (1,134), P. polita (1,014), P. ampullacea (29), P. pesmei (476), Lymnaea (Radix) auricularia rubiginosa (324), Lymnaea swinhoei (9), Indoplanorbis exustus (94), Adameitta housei (303), Chrysallida eppersoni (11), Cipangopaludina annandalei (5), Idiopoma dissimilis (51), Melanoides tuberculata (312), Trochotaia trochoides (257), Clea helena (1,633), Bithynia siamensis goniomphalos (3,334), Filopaludina martensi martensi (2,839), Filopaludina sumartrensis polygramma (557), Filopaludina sumartrensis speciosa (299), Filopaludina martensi munensis (143), Filopaludina cambodjensis (15), Filopaludina doliaris (59), Eyriesia eyriesi (99), Wattebledia crosseana (266), Scabies crispata (6), Pilsbryoncha lemeslei (5), A. fulica (53) and H. distincta (10).

Eight out of the 27 species of mollusks were positive for A. cantonensis. Of the species of mollusks, which were positive for larvae, all of them were snails (class Gastropoda) and no positive infections were found in clams. Infected snails were from the species of F. martensi martensi, F. sumartrensis polygramma, P. pesmei, P. polita, C. helena, B. siamensis goniomphalos, A. fulica, and H. distincta and the percentage of infection (from the total sample mollusks) was 0.41, 0.89, 2.42, 4.97, 0.49, 0.36, 7.55, and 20.00, respectively (Table 1). New records of positive infections were found in the following snails, F. sumartrensis polygramma, B. siamensis goniomphalos, and C. helena. In the preliminary survey P. canaliculata was found to be infected in Nong Boa Daeng district, Chaiyaphum province but no infections were detected in resampling. Prevalences ranged from 0.58% to 7.37% with highest values for P. polita (7.37%) and A. fulica (7.02%) and also found a large number of worm burden individually both in Wangyai, Khon Kaen (Table 2).

The intensity of larval infection was directly associated with the size of snails for P. polita, whereas the inverse was found for P. pesmei (Table 3). Remaining snails had a small worm load. Most of the snails were non-infected or had a low larvae burden, whereas from a few snails high numbers of larvae were recovered, such as the 3,113 (91.59%) larvae found in one A. fulica specimen (Tables 2 and 4).

The highest density of larvae in the positive species of snail was found in P. pesmei, 148.6 larvae/g with the lowest density in P. polita, 0.02 larva/g. The highest average density of larvae was found in A. fulica, 25.96 larvae/g and the lowest was F. m. martensi, 0.57 larvae/g. The infected snails varied in range from small to large snails; however, the infection depended on the size and species of snails (Table 5).

All of the adult worms obtained from the pulmonary artery of white Wistar rats experimentally infected with a sample of the larvae recovered from snails were identified as A. cantonensis.

DISCUSSION

Data from provincial CDC records showed all of the patients with eosinophilic meningoencephalitis shared the histories of raw Pila sp., consumption while drinking alcoholic beverages. The severity of clinical manifestations varies from case to case and may be related to the number of infective larvae ingested with the snails. The severity of symptoms of the severe cases may be related to the large number of larvae infecting just a few snails, which were prepared in the dish, hence each individual could be infected with different numbers of larvae. There was a wide variation of density and larvae burden in individual snails with the highest numbers found in a few specimens. Similar data were reported for A. costaricensis and their terrestrial intermediate hosts. 25 The higher frequency of low larvae burdens may lead to many patients with mild clinical manifestations or even asymptomatic infections.

Infected snails were distributed in 1–2 stations in each reservoir and were found only in the stations on the edge of the reservoir. Transmission of the parasite, therefore, occurred close to the edge of the reservoirs where infected rodents went to drink water and seek food and dropped fecal pellets directly into the water. Alternatively, rodent feces may be flushed by rain water into the reservoir. Our results show that parasite larvae did not disperse throughout the reservoir and infected rats seem to have a restricted home range.

Naturally infected snails were found over a wide range of snails including small-sized snails. We report the first recordings of A. cantonensis infection in B. siamensis goniomphalos and C. helena, including the large-sized snail F. sumartrensis polygramma. The low susceptibility to infection 26 in P. canaliculata could explain why that infection was not found in these snails in the subsequent second stage of sampling. The snails Pila ampullacea, P. polita, and Filopuludina sp. were found to be infected and confirm previous studies. The size of the snail did not relate to the intensity of infection, for instance a P. pesmei small-sized snail was also found to be infected and high intensity of infection did not occur by accumulation of larvae in a large-sized snail. The high intensity of larvae in that snail could be associated by chance with eating a large number of larvae in rat fecal pellets, which implies that infection may be via the oral route. 26

The digestion method for collection of A. cantonensis third stage larvae was found to be the best method compared with lung microscopy or tissue homogenate. 27 Snail tissues almost completely digested to liberate larvae and all of the larvae were very active to migrate down to the bottom by Baermann apparatus. A high density of larvae was found in P. pesmei (148.6 larvae/g) and the average size of the adult of this species of snail was smaller than P. polita (0.02 larva/g), which people preferred to eat. Infected persons who ate raw snails (Pila sp.) usually take the head-foot portion for the preparation of snail dishes. The distribution of larvae in snail organs of this species was highest in the mantle. 26 In the land snail, A. fulica, it has been documented that head-foot portion had low worm recovery. The mantle, which was the highest intensity, 28 may have been still attached to the head-foot portion, which could result in contradictory results.

Prevalence of A. cantonensis infection in P. polita in the same part of the country was 0.9% but negative in P. ampullacea.3 In this study the prevalence of A. cantonensis infection in P. polita varied from place to place, 1.18–50%. The prevalence of infection might relate to the ecology of a specific reservoir and the presence of infected rats. In our study, we found that the highest intensity and density occurred in the land snail A. fulica (3,113 larvae or 91.59% in one snail from total larvae in the same species). It is possible that the distribution of larvae from feces of definitive rodent hosts is still present in intact fecal pellets when it was eaten directly by land snails. When fecal pellets are dropped into water, larvae can disperse after the pellet has dissolved and result in a subsequent low intensity to infect freshwater snails. The land snails, A. fulica and H. distincta, have been shown to be the causative agent of dispersal of this parasitic disease by their migration and eating by rats.29 The incidence of eosinophilic meningitis in the state of Hawaii has increased considerably from 2001 to 2005 30 and may be a result of global warming as Lv and others 31 have discussed.

We found that the average intensity of A. cantonensis third stage larvae in A. fulica was 13.6 per snail (1 to 441). The distribution of parasites in hosts have usually been found to be of a high intensity of worms in a few individual hosts and low intensity or non-infection in the majority of the population as in many kinds of worms, such as Opisthorchis viverrini, in both second intermediate hosts and human hosts. 32,33

Table 1

The prevalence of Angiostrongylus cantonensis infection of each species from total snail sample

Table 1
Table 2

The prevalence of Angiostrongylus cantonensis infection in each species of snails from each locality and showing absolute number of worm burden individually

Table 2
Table 3

The intensity of Angiostrongylus cantonensis larvae in each size group of Pila polita (Wangyai district), Pila pesmei (Pimai district), and Achatina fulica (Wangyai district)

Table 3
Table 4

Angiostrongylus cantonensis larvae recovery in Pila polita (Wangyai district), Pila pesmei (Pimai district), and Achatina fulica (Wangyai district)

Table 4
Table 5

Density of Angiostrongylus cantonensis larvae/gram in each species of positive snails

Table 5
Figure 1.
Figure 1.

Schematic map of northeast Thailand showing 24 sampling localities in 8 provinces.

Citation: The American Journal of Tropical Medicine and Hygiene Am J Trop Med Hyg 80, 6; 10.4269/ajtmh.2009.80.983

*

Address correspondence to Smarn Tesana, Food-Borne Parasite Research Group, Department of Parasitology, Faculty of Medicine, Khon Kaen University, Khon Kaen Province 40002, Thailand. E-mail: smarn_te@kku.ac.th

Authors’ addresses: Smarn Tesana, Tuanchai Srisawangwong, Paiboon Sithithaworn, and Thewarach Laha, Food-Borne Parasite Research Group, Department of Parasitology, Faculty of Medicine, Khon Kaen University, Khon Kaen Province 40002, Thailand, Tel: +66-43-348387, Fax: +66-43-202475, E-mail: smarn_te@kku.ac.th. Ross Andrews, Pharmacy and Medical Sciences, The University of South Australia, South Australia, Australia 5001.

Acknowledgments: We thank the Ministry of Public Health, Department of Communicable Diseases Control who funded this study and all of the public health personnel who helped in survey.

REFERENCES

  • 1

    Crook JR, Fulton SE, Supanwong K, 1968. Ecological studies on the intermediate and definitive hosts of Angiostrongylus cantonensis (Chen, 1935) in Thailand. Ann Trop Med Parasitol 62 :27–43.

    • Search Google Scholar
    • Export Citation
  • 2

    Namue C, Wongsawad C, 1997. A survey of helminth infection in rats (Rattus spp.) from Chiang Mai Moat. Southeast Asian J Trop Med Public Health 28 (Suppl 1):179–183.

    • Search Google Scholar
    • Export Citation
  • 3

    Pipitgool V, Sithithaworn P, Pongmuttasaya P, Hinz E, 1997. Angiostrongylus infections in rats and snails in northeast Thailand. Southeast Asian J Trop Med Public Health 28 (Suppl 1):190–193.

    • Search Google Scholar
    • Export Citation
  • 4

    Lv S, Zhang Y, Steinmann P, Zhou XN, 2008. Emerging angiostrongyliasis in Mainland China. Emerg Infect Dis 14 :161–164.

  • 5

    Dissanaike AS, Ihalamulla RL, Naotunne TS, Senarathna T, Withana DS, 2001. Third report of ocular parastrongyliasis (angiostrongyliasis) from Sri Lanka. Parassitologia 43 :95–97.

    • Search Google Scholar
    • Export Citation
  • 6

    Campbell BG, Little MD, 1988. The finding of Angiostrongylus cantonensis in rats in New Orleans. Am J Trop Med Hyg 38 :568–573.

  • 7

    Bartschi E, Bordmann G, Blum J, Rothen M, 2004. Eosinophilic meningitis due to Angiostrongylus cantonensis in Switzerland. Infection 32 :116–118.

    • Search Google Scholar
    • Export Citation
  • 8

    Bronstein JA, Thevenot J, Tourneux M, 1978. Eosinophilic meningitis in Tahiti: clinical study of 54 patients. N Z Med J 88 :491–493.

  • 9

    Oku Y, Katakura K, Kamiya M, 1980. Tadpole of the clawed frog, Xenopus laevis, as an experimental transmission host of Angiostrongylus cantonensis. Am J Trop Med Hyg 29 :316–318.

    • Search Google Scholar
    • Export Citation
  • 10

    Radomyos P, Tungtrongchitr A, Praewanich R, Khewwatchan P, Kantangkul T, Junlananto P, Ayudhya SI, 1994. Occurrence of the infective stage of Angiostrongylus cantonensis in the yellow tree monitor (Varanus bengalensis) in five Provinces of Thailand. Southeast Asian J Trop Med Public Health 25 :498–500.

    • Search Google Scholar
    • Export Citation
  • 11

    Lai CH, Yen CM, Chin C, Chung HC, Kuo HC, Lin HH, 2007. Eosinophilic meningitis caused by Angiostrongylus cantonensis after ingestion of raw frogs. Am J Trop Med Hyg 76 :399–402.

    • Search Google Scholar
    • Export Citation
  • 12

    Bhaibulaya M, 1979. Geographical distribution of Angiostrongylus and Angiostrongyliasis in Thailand, Indo-China and Australia. Cross JH, ed. Studies on Angiostrongyliasis in Eastern Asia and Australia. A special publication of the U.S. Naval Medical Research Unit No. 2 Taipei, Taiwan NAMRU-2-SP-44. Taipei: L-C Publishing Company, 49–52.

  • 13

    Scrimgeour EM, 1984. Distribution of Angiostrongylus cantonensis in Papua New Guinea. Trans R Soc Trop Med Hyg 78 :776–779.

  • 14

    Ibrahim MM, 2007. Prevalence and intensity of Angiostrongylus cantonensis in freshwater snails in relation to some ecological and biological factors. Parasite 14 :61–70.

    • Search Google Scholar
    • Export Citation
  • 15

    Punyagupta S, Juttijudata P, Bunnag T, 1975. Eosinophilic meningitis in Thailand. Clinical studies of 484 typical cases probably caused by Angiostrongylus cantonensis. Am J Trop Med Hyg 24 :921–931.

    • Search Google Scholar
    • Export Citation
  • 16

    Kuberski T, Wallace GD, 1979. Clinical manifestations of eosinophilic meningitis due to Angiostrongylus cantonensis. Neurology 29 :1566–1570.

    • Search Google Scholar
    • Export Citation
  • 17

    Alto W, 2001. Human infections with Angiostrongylus cantonensis. Pac Health Dialog 8 :176–182.

  • 18

    Tsai HC, Liu YC, Kunin CM, Lee SS, Chen YS, Lin HH, Tsai TH, Lin WR, Huang CK, Yen MY, Yen CM, 2001. Eosinophilic meningitis caused by Angiostrongylus cantonensis: report of 17 cases. Am J Med 111 :109–114.

    • Search Google Scholar
    • Export Citation
  • 19

    Kliks MM, Kroenke K, Hardman JM, 1982. Eosinophilic radiculo-myeloencephalitis: an angiostrongyliasis outbreak in American Samoa related to ingestion of Achatina fulica snails. Am J Trop Med Hyg 31 :1114–1122.

    • Search Google Scholar
    • Export Citation
  • 20

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