Abstract
Angiostrongyliasis is a food-borne parasitic disease induced by the nematode Angiostrongylus cantonensis, and has been recognized as the main cause leading to human eosinophilic meningitis. Humans usually acquire infection by digestion of infected Pomacea canaliculata and Achatina fulica, the most predominant intermediate hosts found in China. This meta-analysis was aimed to assess the prevalence of A. cantonensis infection among these two snails in China in the past 10 years. Data were systematically collected in electronic databases such as PubMed, Web of Science, ScienceDirect, CNKI, SinoMed, VIP, CSCD, and Wanfang from 2005 to 2015. Thirty-eight studies with a total of 41,299 P. canaliculata and 21,138 Ac. fulica were included in the present study. The overall infection rate of A. cantonensis in China was estimated to be 7.6 % (95 % confidential interval (CI) = 0.063 to 0.090) in P. canaliculata and 21.5 % in Ac. fulica (95 % CI = 0.184 to 0.245), respectively. No significant difference was observed in prevalence rates among publication year and sample size for both snails. Also, it was found that the prevalence in Ac. fulica is significantly higher than that in P. canaliculata (odds ratio (OR) = 3.946, 95 % CI = 3.070 to 5.073). The present study reveals that snail infection with A. cantonensis is clearly prevalent in China. Further studies are required to improve strategies for control of infections of snails, particularly those of Ac. fulica, and to detect further factors and conditions such as geographic region, temperatures, and diagnosis method.
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References
Alirol E, Getaz L, Stoll B, Chappuis F, Loutan L (2011) Urbanisation and infectious diseases in a globalised world. Lancet Infect Dis 11:131–141
Cao CL, Guo JG (2011) Schistosome infection and control of migrant population. Chin J Schisto Control 22(4):388–390. doi:10.3969/j.issn.1005-6661.2010.04.025
Chen BJ, Yang WJ, Wu WZ et al (2008) Investigation on the host density and seasonal changes of infection rate of Angiostrongylus cantonensis in Nanan City, Fujian Province. J Pathogen Bio 3(3):218–220
Chen DX, Zhang Y, Shen HX, Wei YF, Huang D, Tan QM, Lan XQ, Li QL, Chen ZC, Li ZT, Ou L, Suen HB, Ding X, Luo XD, Li XM, Zhan XM (2011) Epidemiological survey of Angiostrongylus cantonensis in the west-central region of Guangdong Province, China. Parasitol Res 109:305–314
Chen CX, He HF, Yin Z, Zhou JH, Li SQ, Li FH, Chen JM, Zhu WJ, Zhong XM, Yang KY, Liu GP, Jia X, Chen WT, Li XM, Chen YC, Luo XD, Chen DX, Shen HX (2012a) The survey of Pomacea canaliculata and Achatina fulica infected Angiostrongylus cantonensis in Guangdong Panyu district. Chin J Schisto Control 24(3):336–338
Chen PH, Zhong XG, Zhang ZW (2012b) The investigation of the epidemic focus of Angiostrongylus cantonensis in Dongguan. China Trop Med 12(7):874–893
Chiu YW, Wu JP, Hsieh TC, Liang SH, Chen CM, Huang DJ (2014) Alterations of biochemical indicators in hepatopancreas of the golden apple snail, Ampullaria gigas, from paddy fields in Taiwan. J Environ Biol 35(4):667–673
Deng ZH, Zhang QM, Lin RX et al (2008) Survey on the natural focus of angiostrongyliasis in Guangdong Province. South China J Prev Med 24(4):42–45
Deng ZH, Zhang QM, Lin RX, Huang SY, Zhang Y, Lv S, Liu HX, Hu L, Pei FQ, Wang JL, Ruan CW (2010) The survey of epidemic focus of Angiostrongylus cantonensis in Guangdong. Chin J Parasitol Parasit Dis 28(1):12–16
Deng ZH, Lv S, Lin JY, Lin RX, Pei FQ (2011) An outbreak of angiostrongyliasis in Guanging, People’s Republic of China: migrants vulnerable to an emerging disease. Southeast Asian J Trop Med Public Health 42(5):1047–53
Deng ZH, Zhang QM, Huang SY, Jones JL (2012) First provincial survey of Angiostrongylus cantonensis in Guangdong Province, China. Trop Med Int Health 17(1):119–122
Eamsobhana P (2014) Eosinophilic meningitis caused by Angiostrongylus cantonensis—a neglected disease with escalating importance. Trop Biomed 31(4):569–578
Estebenet AL, Martín PR (2002) Ampullaria gigas (Gastropoda: Ampullariidae): life-history traits and their plasticity. Biocell 26(1):83–89
Guo YH, Lv S, Gu WB, Liu HX, Wu Y, Zhang Y (2014) Investigation on the species distribution and infection status of host snails of Angiostrongylus cantonensis in Shanghai. Chin J Parasitol Parasit Dis 32(6):455–458
Higgins JP, Thompson SG (2002) Quantifying heterogeneity in a meta-analysis. Stat Med 21:1539–1558
Hu XM, Tong CJ, Liu J, Wang SQ (2007) The survey of natural infectious foci of Angiostrongylus cantonensis in Hainan Province. China Trop Med 7(11):1995–1996
Hu XM, Du JW, Tong CJ, Wang SQ, Liu J, Li YC, He CH (2011) Epidemic status of Angiostrongylus cantonensis in Hainan island, China. Asian Pac J Trop Med 4(4):275–277
Huang D, Song JQ, Ye J, Cai ZW, Liu SJ, Qian LY, Xue JF, Chen MJ, Chen F, Wang TJ, Chen DX, Li XM, Zhan XM (2007) The survey of Pomacea canaliculata and Achatina fulica infected Angiostrongylus cantonensis in Jiangmen, Guangdong. Prev Med Trib 13(11):966–968
Huang SC, Su XM, Zhou YY, Lv SS, Tan MK, Lu QW, Chen DX, Zhang B, Zhan XM (2009) Dynamic observation of Angiostrongylus cantonensis as infection in the snail Achatina fulica from Jiangmen City of Guangdong Province. Practical Prev Med 16(5):1355–1356
Huang SY, Deng ZH, Zhang QM (2010) Analysis on the infection of Angiostrongylus cantonensis in water system of Pearl River Delta and coastal areas of Guangdong. Modern Prev Med 18:3529–3531
Huang K, Liang CH, Yang X, Zhan XM, Zhang DJ, Liu X, Chen J, Li ZY (2012) The survey of the infection status of the intermediate host of Angiostrongylus cantonensis in Guangzhou. Chin J Zoonoses 28(2):175–178
Huo XX, Chen WS, Gu WZ, Yang L (2012) Investigation of the infection rate of screw to Angiostrongylus cantonensis in different ecological environments. Practical Prev Med 19(7):1010–1012
Kim JR, Hayes KA, Yeung NW, Cowie RH (2014) Diverse gastropod hosts of Angiostrongylus cantonensis, the rat lungworm, globally and with a focus on the Hawaiian Islands. PLoS One 9(5), e94969
Li QL, Chen HY, Chen GJ et al (2007) A survey of snails Achatina fulica and Ampullaria gigas infection with Angiostrongylus cantonensis in Lianjiang of Guangdong Province China. Chin J Dis Control Prev 11(4):376–378
Li FH, Zhou XM, Li YZ, Tao H (2010) Investigation on epidemic focus of Angiostrongyliasis cantonensis in Yunnan Province, China. J Pathogen Bio 3(1):53–57
Li AM, Huang YT, Ye HB, Lin GC, Xv JJ (2015) The investigation of the infection status of Angiostrongylus cantonensis in winkle from 9 cities in Guizhou Province. Chin J Endemiol 34(4):300–302
Lin RX, Deng ZH, Wen XM, Ruan CW, Xie PJ, Chen YM (2008) The survey of epidemic focus of Angiostrongylus cantonensis in Luoding, Guangdong. China Trop Med 1(8):61–63
Lin YF, Yang PX, Xu GH, Liu XM, Lin FT, Qu ZY, Zhan XM, He A (2010) Investigation of the infection of Angiostrongylus cantonensis in Qingyuan City. J Trop Med 10(3):327–329
Liu HX, Zhang Y, Lv S et al (2007a) A comparative study of three methods in detecting Angiostrongylus cantonensis larvae in lung tissue of Pomacea canaliculata. Chin J Parasitol Parasit Dis 25(1):53–56
Liu J, Hu XM, Wang SQ, Luo D, Fu CQ, Chen H (2007b) The survey of natural infectious foci of Angiostrongylus cantonensis in Dingan County, Hainan. China Trop Med 7(3):408–409
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(5):583–587
Lv S, Zhang Y, Steinmann P, Zhou XN (2008) Emerging angiostrongyliasis in mainland China. Emerg Infect Dis 14(1):161–164
Lv S, Zhang Y, Chen SR et al (2009a) Human angiostrongyliasis outbreak in Dali, China. PLoS Negl Trop Dis 3(9), e520
Lv S, Zhang Y, Liu HX, Hu L, Yang K, Steinmann P, Chen Z, Wang LY, Utzinger J, Zhou XN (2009b) Invasive snails and an emerging infectious disease: results from the first national survey on Angiostrongylus cantonensis in China. PLoS Negl Trop Dis 3(2), e368
Ou L, Cai T, Li L, Chen ZP, Huang YY, Xu J, Mo WY, Chen DX, Zhang Z, Li XM, Zhan XM (2008) The survey of Pomacea canaliculata and Achatina fulica infected Angiostrongylus cantonensis in Luoding, Guangdong. China Trop Med 12:2083–2084
Park SY, Fox LM (2013) Angiostrongylus cantonensis: epidemiology in the continental United States and Hawaii. Hawaii J Med Public Health 72:34
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(6 Pt 1):921–931
Rosen L, Loison G, Laigret J et al (1967) Studies on eosinophilic meningitis. 3. Epidemiologic and clinical observations on Pacific islands and the possible etiologic role of Angiostrongylus cantonensis. Am J Epidemiol 85:17–44
Shen HX, Chen K, Pan SH, Huang LT, Wang C, Lu YY, Ma CL, Chen DX, Chen XY (2012) Investigation on spread and hazards of human parasites in Qushui Village, Suixi County, Zhanjiang City. Chin J Schisto Control 24(4):461–463
Simoes RO, Monteiro FA, Sanchez E et al (2011) Endemic angiostrongyliasis, Rio de Janeiro, Brazil. Emerg Infect Dis 17:1331–1333
Slom TJ, Cortese MM, Gerber SI et al (2002) An outbreak of eosinophilic meningitis caused by Angiostrongylus cantonensis in travelers returning from the Caribbean. N Engl J Med 346:668–675
Sun HB, Liang ZZ, Zhong YL, Chen FZ, Huang JD, Huang ZH, Lin C, Liang ZQ, Yu JB, Zhou JM, Chen DX, Li XM, Zhan XM (2008) The survey of Pomacea canaliculata and Achatina fulica infected Angiostrongylus cantonensis in Zhaoqing, Guangdong. Parasitosis and Infectious Dis 01:18–20
Tang LN, Li AM, Lu LD, Xv LN, Lin GC, Wang SH, Zhang XS (2008) Survey of infections status of Angiostrongylus cantonensis in intermediate host in Guiyang city. Chin J Vector Bio & Control 19(4):342–344
Tong CJ, Hu XM, Wang SQ, Qu L, Cui LD, Wu QX (2008) The survey of natural infectious foci of Angiostrongylus cantonensis in coastal areas of Hainan Province. J Pathogen Bio 3(1):63–64
Tong CJ, Hu XM, Li KJ, Wang SQ, Liu J (2009) The survey of natural infectious foci of Angiostrongylus cantonensis in midwestern areas of Hainan Province. Chin J Zoonoses 25(3):292–293
Tong CJ, Wang SQ, Liu J, Li CY, Wu S, He CH, Li KJ, Zhuo KR, Hu XM (2011) Investigation on intermediate host and definitive host infection of Angiostrongylus cantonensis in Hainan Province. Modern Prev Med 38(19):4009–4011
Tsai HC, Liu YC, Kunin CM, Lee SS, Chen YS, Lin HH, Tsai TH, Lin WR, Huang CK, Yen MY, Yen (2001) Eosinophilic meningitis caused by Angiostrongylus cantonensis: report of 17 cases. Am J Med 111(2):109–14
Tseng YT, Tsai HC, Sy CL, Lee SS, Wann SR, Wang YH, Chen JK, Wu KS, Chen YS (2011) Clinical manifestations of eosinophilic meningitis caused by Angiostrongylus cantonensis: 18 years’ experience in a medical center in southern Taiwan. J Microbiol Immunol Infect 44(5):382–389
Wang LB, Du ZW, Jiang JY, Wu FW (2010) Investigation on epidemic focus of Angiostrongyliasis cantonensis in Yunnan Province, China. Chin J Vector Bio & Control 21(5):496–497
Wang QP, Wu ZD, Wei J, Owen RL, Lun ZR (2012) Human Angiostrongyliasis cantonensis: an update. Eur J Clin Microbiol Infect Dis 31:389–295
Wilkins PP, Qvarnstrom Y, Whelen AC, Saucier C, da Silva AJ, Eamsobhana P (2013) The current status of laboratory diagnosis of Angiostrongylus cantonensis infections in humans using serologic and molecular methods. Hawaii J Med Public Health 72(6 Suppl 2):55–57
Xie P, Wu DR (2013) The survey of epidemic focus of Angiostrongylus cantonensis in Beihai, Guangxi. Int J Parasit Dis 40(2):67–70
Yang X, Qu ZY, He HL, Zheng XY, He A, Wu Y, Liu Q, Zhang DJ, Wu ZD, Li ZY, Zhan XM (2012) Enzootic angiostrongyliasis in Guangzhou, China, 2008–2010. Am J Trop Med Hyg 86(5):846–849
Ye DG, Luo B, Liu BD, Zhen P (2008) The epidemiology investigation of Angiostrongylus cantonensis in Fu Zhou. J Trop Med 8(9):938–957
Zeng QX, Sun ZJ, Zhang B et al (2011) Susceptibility for different varieties of Pomacea canaliculata to Angiostrongylus cantonensis in South China. Chin J Zoonoses 27(7):625–628
Zhang B (2009) Epidemiological investigation of Angiostrongylus cantonensis in western part of Guangdong Province. Dissertation, Guangzhou Medical College, 32–37
Zhang HM, Tan YG, Li XM, Ruan TQ, Zhou XN, Zhang Y, Huang FM, Jiang H, Ou YY (2007a) Survey of epidemic focus of Angiostrongylus cantonensis in Guangxi. J Trop Dis Parasitol 5(2):79–84
Zhang WC, She SS, Chen DN, Lin J, Guo YH, Chen SL (2007b) Description on the intermediate hosts of Angiostrongylus cantonensis. Chin J Zoonoses 23(4):401–408
Zhang B, Huang D, Tan QM, Chen DX, Zhan XM (2008a) The epidemiology investigation of Angiostrongylus cantonensis in Jiangmen, Guangdong. Chin J Parasitol Parasit Dis 26(5):370–373
Zhang LH, Chen JL, Dong WR (2008b) The investigation of the infection rate of Pomacea canaliculata, Achatina fulica, Cipangopaludina cathayensis and Bellamya sp. to Angiostrongylus cantonensis in Foshan. Guangdong Med J 29(11):1898–1899
Zhang ZQ, Su XM, Sun W, Li BH, Lin SX, Li MJ, Chen ZC, Deng GY, Ye J, Li XY, Liu GH, Zhang GY, Zhu JH (2008c) The survey of Pomacea canaliculata and Achatina fulica infected Angiostrongylus cantonensis in Maoming, Guangdong. Chin J Vector Bio & Control 19(3):241–243
Zhang B, Huang Ding X, Chen DX, Zhan XM (2009a) The epidemiology investigation of Angiostrongylus cantonensis in Yangchun, Guangdong. Chin J Zoonoses 25(1):87–89
Zhang Y, Lv S, Yang K et al (2009b) The first national survey on natural nidi of Angiostrongylus cantonensis in China. Chin J Parasitol Parasit Dis 27(6):508–512
Zhou WC, She SS, Chen DN, Lin J, Guo YH, Chen SL (2007) Description on the intermediate hosts of Angiostrongylus cantonensi. Chin J Zoonoses 23(4):401–408
Acknowledgments
This study was funded by the grants from the National Natural Science Foundation of China (grant nos. 81271855, 81371836, 81261160324, and 81572023), the Laboratory of Parasite and Vector Biology, MOPH (grant no. WSBKTKT201401), the National Basic Research Program of China (grant no. 2010CB530004), Guangdong Natural Science Foundation (grant no. 2014A030313134), the 111 Project (grant no. B12003), and the Research Foundation for Students of Sun Yat-sen University (2012, 2014).
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Langui Song, Xiaowen Wang and Zi Yang contributed equally to this work.
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Song, L., Wang, X., Yang, Z. et al. Angiostrongylus cantonensis in the vector snails Pomacea canaliculata and Achatina fulica in China: a meta-analysis. Parasitol Res 115, 913–923 (2016). https://doi.org/10.1007/s00436-015-4849-5
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DOI: https://doi.org/10.1007/s00436-015-4849-5