Asian Pacific Journal of Tropical Medicine (2011)275-277 275

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Document heading doi: Epidemic status of Angiostrongylus cantonensis in island, China Ximin Hu﹡, Jianwei Du﹡, Chongjin Tong, Shanqing Wang, Jian Liu, Yuchun Li, Changhua He

Hainan Provincial Center for Diseases Control and Prevention, 570203, Hainan, People’s Republic of China

ARTICLE INFO ABSTRACT

Article history: Objective: Angiostrongylus cantonensis To understand the current epidemiological status of Received 25 October 2010 in Hainan island and provide the scientific evidences for prevention and control of the Received in revised form 27 November 2010 Methods: Accepted 15 February 2011 disease. AngiostrongylusThe investigation cantonensis on nature infection condition of intermediate hosts and Available online 20 April 2011 final hosts of were carried out in five counties, Hainan Province, (ELISA) Angiostrongylusand enzyme linked cantonensis immunosorbent assayResults: was employed to detect antibodies of in human hosts. A total of 1 612 molluscs were examined, Keywords: Angiostrongylus cantonensis 21.3% of which harbored L3 of . Among them, the infection rates Angiostrongylus cantonensis Pomacea canaliculata, Achatina fulica, Cepaea Phlegm bilineatus of and were 12.36%(64/518), Epidemic focus 22.66%(121/534), 20.93%(9/43) 28.24%(146/517) 118 13 Rattus norvegicus , and Angiostrongylus, respectively. Ofcantonensis the rats trapped, Survey were found to be infected with . A total of 459 Angiostrongylus cantonensis serum samples were collected and tested. 92 serum samples were Conclusions: Angiostrongylus antibody-positive. The survey revealed a wide distribution of cantonensis Pomacea canaliculata Achatina fulica in Hainan island. and are main intermediate Angiostrongylus cantonensis. Rattus novegicus hosts of is a nature definitive host, indicating that a considerable number of people are at risk of angiostrongyliasis. Health education, rigorous food inspection and surveillance are all needed to prevent angiostrongyliasis outbreaks in future.

general public and physicians[4]. 1. Introduction Hainan° ′ °island′ is located in the° southern′ ° ′end of China, 18 10 -20 10 N latitude and 108 37 -111 03 E longitude, a Angiostrongylus cantonensis(A. The nematode worm tropical zone. The climate is warm with plentiful rainfalls, cantonensis) was discovered in the pulmonary arteries and proper humidity, and it is quite suitable for survival and A. cantonensis hearts of domestic rats in Guangzhou (Canton), China, by transmission of . Hainan island as one of a A. cantonensis Chen in 1935[1]. is a zoonotic pathogen, which province in China including 18 cities and counties, Xisha occasionally causes human angiostrongyliasis with the mainfi archipelago, Zhongsha archipelago and Nansha archipelago clinical manifestation of eosinophilic meningitis. The rst with a population of 8.28 million and total areas of 35 400 human infection case of angiostrongyliasis was reported square kilometers. To understand the distribution, A. cantonensis in Taiwan in 1945[2]. Since then, several outbreaks of the infectious status of and its hosts in the disease in human beings have been reported in the Pacific geographic region, a survey on the distribution, infectious A. cantonensis islands[3]. In the past 10 years, several major outbreaks status of and its intermediate hosts in Hainan of the disease have been reported in endemic regions, island was carried out from 2007 to 2009. Here we reported especially in China, causing great concern for both the significant findings.

*Corresponding author: Ximin Hu, Hainan’ Provincial Center for Diseases Control and 2. Materials and methods Prevention, 570203, Haikou Hainan, People s Republic of China. Jianwei Du, Hainan Provincial’ Center for Diseases Control and Prevention, 570203,Haikou Hainan,People s Republic of China. 2.1. Survey sites selection Tel: 86-898-65340342 Fax:86-898-65333245 E-mail: [email protected], [email protected] Foundation project: This work was supported by grants from Hainan Provincial According to different geographic locations with the Natural Science Foundation (No. 808226). Ximin Hu et al./Asian Pacific Journal of Tropical Medicine (2011)275-277 276 fulica P. canaliculata A. distribution of water systems, five counties or cites in was 28.43%(29/102). Infected and fulica Hainan island were selected as the survey sites. The five were found in four and one counties, respectively. counties or cites are Haikou, , , , Additionally, one native freshwater snail species, Cipangopaludina chinensis Qiongzhong, respectively. In each survey sites, one village was commonly found sale in was randomly selected for subsequent field work. many markets and none of them were checked positive. 2.2. Host etiology examination 3.3. Serological test results

’ ， Rats were trapped in fields and in residents houses. A total of 459 serum samples were collected and tested A. cantonensis All captured animals were euthanized and dissected to and 92 serum samples were antibody- A. cantonensis determine the presence of adult in their positive. Overall antibody positive rate was 20.04%, hearts and lung arteries. Freshwater snails, terrestrial Antibody-positive rate in males and female were 18.62% snails and certain terrestrial slugs were collected from the (35/188) and 20.36% (57/280), respectively, without 2 P surroundings of the study villages, and from restaurants significant gender differences (氈 = 0.22, >0. 05). Antibody and markets in the capital town of the counties, which were positive rate of people under the age of 14 (including 14 A. cantonensis 29 23 19 65 14 examined for the presence of larvae. Up to years of age) was . % ( / ), and over the age of2 was 100 specimens of each species were collected at each study 18.53% (73/394), with significant age difference (氈 = 3.99, P site. The intermediate hosts were artificially digested using <0.05) . routine procedures[5]. Additionally, for the examination Pomacea canaliculata(P. canaliculata) of , a recently 4. Discussion developed method relying on specific lung tissue features of this species was employed[5,6]. In brief, the lungs were A. cantonensis separated from the snail body and opened for checking the Eosinophilic meningitis caused by is A. cantonensis parasites. The nodules containing larvae endemic in , Australia, the Pacific islands were then directly observed under a microscope. Paratenic and the Caribbean. To date, more than 2 800 human hosts were also collected from markets and restaurants for cases have been reported. It had been suggested that the examination of L3 using an artificial digestion method. parasite was dispersed from East Asia to other regions in i.e A. fulica two important hosts, ., rats (definitive host) and 2.3. Seroepidemiological survey (intermediate host) especially during World War II[7]. Today, the parasite is still expanding and the associated disease Collecting serum from permanent residents in five survey is emerging in some regions, particularly in China. Hainan sites, ELISA was employed to detect the antibodies IgG Province is located in the southern end of China, a tropical A. cantonensis against in serum (Test kit producer: Shenzhen zone. The climate is warm with plentiful rainfalls and proper A. Bombined Biotech Co. Ltd, China ). humidity, and it is quite suitable for the transmission of cantonensis . As early as in 1984, a small-scale survey on the A. cantonensis infectious status of intermediate hosts of had 3. Results been carried out in County, Hainan Province[8]. A. The survey results showed that the infection rates of 3.1. A. cantonensis hosts and their infection status fulica were 33.3% (10/30). The results of the first provincial A. cantonensis survey on the distribution of and its hosts in Rattus A. cantonensis Of the 118 rats trapped during the field surveys, 13 Hainan Province indicate that the -endemic norvegicus A. cantonensis P. were found infected with . The area is very broad, covering all the counties surveyed. canaliculata A. fulica infection rate was 11.02%. A total of 1 612 molluscs were and are the primary intermediate A. cantonensis Rattus norvegicus examined, 21.3% of which harbored L3 of . hosts, is the major definitive host in P. canaliculata, Among them, the infection rates of Hainan Province. However, no angiostrongyliasis cases have Achatina fulica (A. fulica), Cepaea and Phlegm bilineatus been observed thus far in Hainan Province. The important were 12.36%(64/518), 22.66%(121/534), 20.93%(9/43), indicators might have been neglected or misdiagnosis due 28.24%(146/517), respectively. to low levels of awareness about angiostrongyliasis among medical staff. Many cases could have gone with unreported 3.2. Intermediate host snails from markets and restaurants or unrecognized during the past decades. It remains to be further investigated. Hospital-based surveillance might be A total of 680 snails collected from markets and/or an effective approach to reveal unfolding angiostrongyliasis P. canaliculata restaurants in five survey sites were examined. The overall epidemics in areas where snails, particularly A. fulica infection rate was 10.29% (41/680). Among them, the and , are popular. P. canaliculata A. A. fulica infection rates of was 9.67%(41/424) and was recorded for the first time in Ximin Hu et al./Asian Pacific Journal of Tropical Medicine (2011)275-277 277 A. fulica in 1931[9]. It has been suggested that eggs of were rigorous food inspection, and hospital-based surveillance accidentally imported from with shipments are needed to prevent from potential angiostrongyliasis of plants, and that an initial snail population became outbreaks in Hainan island. established in Xiamen (Amoy)[10]. These terrestrial snails are nocturnal and become active under high-humidity Conflict of interest statement conditions. The snails feed on plants and deposit their eggs in the soil nearby. Subsequently, the snail was farmed in most southern provinces with commercial aims[11], It is We declare that we have no conflict of interest. conceivable that the dense river networks in Hainan island A. cantonensis contributed to the dispersal of this snail. A. References infection is mediated not only by ingestion of the cantonensis -carrier intermediate or paratenic hosts but also Pulmonema [1] Chen HT. A new pulmonary nematode of rats, through the ingestion of vegetables, drinking water, and by cantonensis Ann Parasito 13 contact with fingers that are contaminated by the infective ng, nsp from Canton. l 1935; : 312- A. cantonensis. larvae of Small planarians could represent 317. [2] Rosen L, Laigret J, Boils PL. Observation on an outbreak of a very important but overlooked source of human infection Am J Trop eosinophilic meningitis on Tahiti, French Polynesia. when they are consumed together with contaminated Med Hyg 12 uncooked vegetables. 1961; : 613-615. The results of the survey also suggest that people are at [3] Kliks MM, Kroenke K, Hardman JM. Eosinophilic risk of angiostrongyliasis through consumption of raw or radiculomyeloencephalitis: an angiostrongyliasis outbreak in A. cantonensis Achatina fulica Am American Samoa related to ingestion of snails. undercooked snails infected with in some J Trop Med Hyg 31 markets and restaurants. It is important to enhance the 1982; : 1114-1122. [4] Lv S, Zhang Y, Steinmann P, Zhou XN. Emerging understanding of angiostrongyliasis epidemiology, increase Emerg Infect Dis 14 public awareness about the risks associated with eating raw angiostrongyliasis in mainland China. 2008; : food, and enhance food safety measures. Food safety and 161-164. [5] Lv S, Zhou XN, Zhang Y, Liu HX, Zhu D, Yin WG, et al. The transportation must be improved to avoid human infections Angiostrongylus effect of temperature on the development of and the further spread of intermediate host snails to areas in cantonensis Pomacea canaliculata (Chen 1935) in (Lamarck which the disease is not endemic. Collection and marketing Parasitol Res 99 of wild snails should be limited. Hygiene and food 1822). 2006; : 583-587. [6] Liu HX, Zhang Y, Lv S, Zhu D, Ang XH, Hu L, et al. A preparation techniques in restaurants should be improved Angiostrongylus comparative study of three methods in detecting to prevent from cross-contamination of other food items. cantonensis Pomacea canaliculata Chin J larvae in lung tissue of . These efforts should be accompanied by sound information Parasitol Parasit Dis 25 in communication and education campaigns to raise 2007; : 53-56. public awareness. The basic message, that consumption [7] Kliks MM, Palumbo NE. Eosinophilic meningitis beyond the Pacific Basin: the global dispersal of a peridomestic zoonosis of raw or undercooked snails is a key risk factor for the Angiostrongylus cantonensis caused by , the nematode lungworm of transmission of a serious disease, can be easily conveyed Soc Sci Med 34 and is readily understood by the public. Awareness of rats. 1992; : 199-212. [8] He LY, Zhong HL, Gao PZ, Li HH, Huang SY. 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