INVITED REVIEWS

Prevalence of waterborne intestinal protozoosis and control strategies in China

  • Yu-juan SHEN ,
  • Yan-yan JIANG ,
  • Jian-ping CAO
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  • National Institute of Parasitic Diseases, Chinese Center for Disease Control and Prevention; Chinese Center for Tropical Diseases Research; WHO Collaborating Centre for Tropical Diseases; National Center for International Research on Tropical Diseases, Ministry of Science and Technology; Key Laboratory of Parasite and Vector Biology, Ministry of Health, Shanghai 200025, China

Received date: 2020-08-10

  Revised date: 2020-10-12

  Online published: 2021-03-10

Supported by

National Major Science and Technology Projects of China(2018ZX10713001-004);National Natural Science Foundation of China(82072307);Chinese Special Program for Scientific Research of Public Health(201502021);Fifth Round of Three?Year Public Health Action Plan of Shanghai, China(GWV-10.1-XK13)

Abstract

Intestinal protozoosis such as cryptosporidiosis, giardiasis, and cyclosporosis can be transmitted through water, and represents an important waterborne parasitic disease. Most intestinal parasites are characterized by the zoonotic nature and having multiple animal hosts, making it difficult to prevent and control. In addition, some of the intestinal protozoosis are emerging infectious diseases, with no available baseline data concerning human infection. This review focuses on the prevalence and detection techniques of the waterborne intestinal protozoosis in China, and discusses challenges for the disease prevention and control, in order to provide reference for establishment of an efficient disease surveillance network and an early-warning system, for carrying out risk assessments, and for proposing effective prevention and control measures.

Cite this article

Yu-juan SHEN , Yan-yan JIANG , Jian-ping CAO . Prevalence of waterborne intestinal protozoosis and control strategies in China[J]. CHINESE JOURNAL OF PARASITOLOGY AND PARASITIC DISEASES, 2021 , 39(1) : 8 -12 . DOI: 10.12140/j.issn.1000-7423.2021.01.002

References

[1] Karanis P, Kourenti C, Smith H. Waterborne transmission of protozoan parasites: a worldwide review of outbreaks and lessons learnt[J]. J Water Heal, 2007,5(1):1-38.
[2] Baldursson S, Karanis P. Waterborne transmission of protozoan parasites: review of worldwide outbreaks-an update 2004—2010[J]. Water Res, 2011,45(20):6603-6614.
[3] Efstratiou A, Ongerth JE, Karanis P. Waterborne transmission of protozoan parasites: review of worldwide outbreaks-an update 2011—2016[J]. Water Res, 2017,114:14-22.
[4] Nime FA, Burek JD, Page DL, et al. Acute enterocolitis in a human being infected with the protozoan Cryptosporidium[J]. Gastroenterology, 1976,704(4):592-598.
[5] Holubová N, T?mová L, Sak B, et al. Description of Cryptosporidium ornithophilus n. sp. (Apicomplexa : Cryptosporidiidae) in farmed ostriches [J]. Parasites Vectors, 2020,13:340.
[6] Han F, Tan WX, Zhou XL. Report of two cases of human cryptosporidiosis in Nanjing area[J]. Jiangsu Med J, 1987,13(12):692-703. (in Chinese)
[6] ( 韩范, 谭渭仙, 周性兰. 南京地区人体隐孢子虫病2例报告[J]. 江苏医药, 1987,13(12):692-703.)
[7] Zhang YJ, Luo P, Gao R. Survey on cryptosporidiosis among children with diarrhae in Chengdu[J]. J Pract Parasit Dis, 2001,9(2):72-73. (in Chinese)
[7] ( 章亚惊, 罗萍, 高蓉. 成都市某儿童医院腹泻儿童中隐孢子虫感染调查[J]. 实用寄生虫病杂志, 2001,9(2):72-73.)
[8] Su YQ. HIV-infected patients with chronic diarrhea stool specimens detection of pathogenic microorganisms[J]. Chin Heal Ind, 2014,11(6):24-25. (in Chinese)
[8] ( 苏映琼. HIV感染合并慢性腹泻患者粪便标本的病原微生物检测分析[J]. 中国卫生产业, 2014,11(6):24-25.)
[9] Yang Y, Zhou YB, Xiao PL, et al. Prevalence of and risk factors associated with Cryptosporidium infection in an underdeveloped rural community of southwest China[J]. Infect Dis Poverty, 2017,6:1-10.
[10] Yang Y, Zhou YB, Cheng WT, et al. Prevalence and determinants of Cryptosporidium infection in an underdeveloped rural region of southwestern China[J]. Am J Trop Med Hyg, 2017,96(3):595-601.
[11] Hung CC, Tsaihong JC, Lee YT, et al. Prevalence of intestinal infection due to Cryptosporidium species among Taiwanese patients with human immunodeficiency virus infection[J]. J Formos Med Assoc, 2007,106(1):31-35.
[12] Liu A, Gong B, Liu X, et al. A retrospective epidemiological analysis of human Cryptosporidium infection in China during the past three decades (1987—2018)[J]. PLoS Negl Trop Dis, 2020,14(3):e0008146.
[13] Peng MM, Matos O, Gatei W, et al. A comparison of Cryptosporidium subgenotypes from several geographic regions[J]. J Eukaryot Microbiol, 2001, Suppl: 28S-31S.
[14] Wang RJ, Zhang XS, Zhu HL, et al. Genetic characterizations of Cryptosporidium spp. and Giardia duodenalis in humans in Henan, China[J]. Exp Parasitol, 2011,127(1):42-45.
[15] Zhu HL, Zhao JF, Wang RJ, et al. Molecular identification of a rare subtype of Cryptosporidium hominis in infants in China[J]. PLoS One, 2012,7(8):e43682.
[16] Feng YY, Wang L, Duan LP, et al. Extended outbreak of cryptosporidiosis in a pediatric hospital, China[J]. Emerg Infect Dis, 2012,18(2):312-314.
[17] Wang L, Zhang HW, Zhao XD, et al. Zoonotic Cryptosporidium species and Enterocytozoon bieneusi genotypes in HIV-positive patients on antiretroviral therapy[J]. J Clin Microbiol, 2013,51(2):557-563.
[18] Liu H, Shen YJ, Yin JH, et al. Prevalence and genetic characterization of Cryptosporidium, Enterocytozoon, Giardia and Cyclospora in diarrheal outpatients in China[J]. BMC Infect Dis, 2014,14:25.
[19] Jiang Y, Ren J, Yuan Z, et al. Cryptosporidium andersoni as a novel predominant Cryptosporidium species in outpatients with diarrhea in Jiangsu Province, China[J]. BMC Infect Dis, 2014,14:555.
[20] Liu XJ, Mao TB, Wu P, et al. Molecular epidemiology of Cryptosporidium infection in infants with diarrhea in Wuhan City[J]. Chin J Schisto Control, 2017,29(2):188-191, 205. (in Chinese)
[20] ( 刘晓洁, 毛铁波, 吴鹏, 等. 武汉市腹泻婴幼儿隐孢子虫感染的分子流行病学调查[J]. 中国血吸虫病防治杂志, 2017,29(2):188-191, 205.)
[21] Wang T, Fan YY, Koehler AV, et al. First survey of Cryptosporidium, Giardia and Enterocytozoon in diarrhoeic children from Wuhan, China[J]. Infect Genet Evol, 2017,51:127-131.
[22] Xu N, Liu H, Jiang Y, et al. First report of Cryptosporidium viatorum and Cryptosporidium occultus in humans in China, and of the unique novel C. viatorum subtype XVaA3h[J]. BMC Infect Dis, 2020,20(1):16.
[23] Qi M, Feng C, Lv C, et al. Epidemiological status of zoonotic giardiasis[J]. Heilongjiang Animal Sci Vet Med, 2009(10):83-85. (in Chinese)
[23] ( 齐萌, 冯超, 吕超超, 等. 人畜贾第虫病流行概况[J]. 黑龙江畜牧兽医, 2009(10):83-85.)
[24] Jiang ZX, Xu LQ, Yu SH, et al. Epidemiological status of Giardia in China[J]. Chin Public Health, 1997,13(7):407-408. (in Chinese)
[24] ( 蒋则孝, 许隆祺, 余森海, 等. 中国贾第虫感染流行病学现况[J]. 中国公共卫生, 1997,13(7):407-408.)
[25] Tang LH, Xu LQ, Chen YD. Parasitic disease control and research in China[M]. Beijing: Beijing Science Technology Press, 2012. ( in Chinese)
[25] ( 汤林华, 许隆祺, 陈颖丹. 中国寄生虫病防治与研究[M]. 北京: 北京科学技术出版社, 2012.)
[26] Zhou XN. Report on the national survey of important human parasitic disease in China (2015)[M]. Beijing: People’s Medical Publishing House, 2018. ( in Chinese)
[26] ( 周晓农. 2015年全国人体重点寄生虫病现状调查报告. 北京: 人民卫生出版社, 2018.)
[27] Li YB, Ge FT, Yang MZ, et al. First investigation and research on distribution of human parasites in Hebei Province[J]. Chin J Parasitol Parasit Dis, 1994,12(S1):226. (in Chinese)
[27] ( 李远壁, 葛凤台, 杨满占, 等. 河北省首次人体寄生虫分布的调查与研究[J]. 中国寄生虫学与寄生虫病杂志, 1994,12(S1):226.)
[28] He DL, Wu XH, Guo ZX. Analysis on epidemiological characteristics of Giardia lamblia in Qinghai[J]. Endem Dis Bull, 1997,12(4):35-36. (in Chinese)
[28] ( 何多龙, 吴献洪, 郭再宣. 青海省人体蓝氏贾第鞭毛虫流行病学调查分析[J]. 地方病通报, 1997,12(4):35-36.)
[29] Li ZY. Giardia lamblia infection in Huaying City, Sichuan[J]. Parasit Infect Dis, 2003,1(1):34-35. (in Chinese)
[29] ( 李治有. 四川省华蓥市蓝氏贾第鞭毛虫感染情况的调查[J]. 寄生虫病与感染性疾病, 2003,1(1):34-35.)
[30] Wan GQ, Zhang DB, Liu X, et al. Infection status and impact factors of Giardia lamblia in children in rural areas of Shandong[J]. Chin Gen Pract, 1999,2(1):49-50. (in Chinese)
[30] ( 万功群, 张佃波, 刘新, 等. 山东省农村儿童蓝氏贾第鞭毛虫感染状况及流行因素调查[J]. 中国全科医学, 1999,2(1):49-50.)
[31] Fu M, Sun Q, Su L. Investigation on Giardia bamblia infection among students in Huainan[J]. Chin J Sch Dr, 2004,18(2):167-168. (in Chinese)
[31] ( 付敏, 孙群, 苏玲. 某地区在校学生贾第虫感染情况的调查[J]. 中国校医, 2004,18(2):167-168.)
[32] Wang L, Xiao LH, Duan LP, et al. Concurrent infections of Giardia duodenalis, Enterocytozoon bieneusi, and Clostridium difficile in children during a cryptosporidiosis outbreak in a pediatric hospital in China[J]. PLoS Negl Trop Dis, 2013,7(9):e2437.
[33] Liu H, Xu N, Shen YJ, et al. Infection and genotype of Giardia lamblia among HIV/AIDS patients in Guangxi[J]. Chin J Parasitol Parasit Dis, 2019,37(3):321-325. (in Chinese)
[33] ( 刘华, 徐宁, 沈玉娟, 等. 广西地区艾滋病病毒感染/艾滋病患者蓝氏贾第鞭毛虫感染情况及基因型分析[J]. 中国寄生虫学与寄生虫病杂志, 2019,37(3):321-325.)
[34] Brunkard JM, Ailes E, Roberts VA, et al. CDC surveillance for waterborne disease outbreaks associated with drinking water-United States, 2007—2008[J]. Surveill Summ, 2011,60(12):38-68.
[35] Centers for Disease Control and Prevention (CDC). Outbreaks of cyclosporiasis: United States, June-August 2013[J]. Morb Mortal Wkly Rep, 2013,62(43):862.
[36] Casillas SM, Bennett C, Straily A. Notes from the field: multiple cyclosporiasis outbreaks-United States, 2018[J]. Morb Mortal Wkly Rep, 2018,67(39):1101-1102.
[37] Su QP, Lin QJ, Chen JL. The first report of the cyclosporosis in China[J]. Chin J Zoonoses, 1995,11(5):6. (in Chinese)
[37] ( 苏庆平, 林秋君, 陈景龙. 我国圆孢子虫病首例报告[J]. 中国人兽共患病杂志, 1995,11(5):6.)
[38] Hou YS, Li JQ. First discovery of Cyclospore cayetanensis and its infectious status in Sshanxi Province[J]. Novel J Gastroenterology, 1997(12):785-786. (in Chinese)
[38] ( 侯云圣, 李景琦. 陕西省首次发现圆孢子虫感染情况调查[J]. 新消化病学杂志, 1997(12):785-786.)
[39] Dai JD, Ge JJ. Allicin in treatment of 48 cases of infants cyclosporidiosis[J]. Jiangsu Tradit Chin Med, 1997,29(6):16. (in Chinese)
[39] ( 戴君道, 戈建军. 大蒜素治疗婴幼儿圆孢子虫病48例[J]. 江苏中医, 1997,29(6):16.)
[40] Zhang BX, Yu H, Zhang LL, et al. Prevalence survey on Cyclospora cayetanensis and Cryptosporidium ssp. in diarrhea cases in Yunnan Province[J]. Chin J Parasitol Parasit Dis, 2002,20(2):106-108. (in Chinese)
[40] ( 张炳翔, 俞慧, 张莉莉, 等. 云南省腹泻患者圆孢子虫和隐孢子虫感染情况调查分析[J]. 中国寄生虫学与寄生虫病杂志, 2002,20(2):106-108.)
[41] Xing WL, Wu KW, Lin XY, , et al. Investigation on cyclosporidia infection in diarrhea patients in Wenzhou[J]. Chin J Parasit Dis Control, 2002, 15(5): 320, I001. (in Chinese)
[41] ( 邢文鸾, 吴康为, 林秀英, 等. 温州地区腹泻患者圆孢子虫感染情况调查[J]. 中国寄生虫病防治杂志, 2002, 15(5): 320, I001.)
[42] Wang KX, Li ZP, Wang J, et al. Preliminary investigation for Cyclospora cayetanensis infection in different populations in parts of Anhui Province[J]. Chin J Epidemiol, 2003,24(2):93. (in Chinese)
[42] ( 王克霞, 李朝品, 王健, 等. 安徽省部分地区不同人群中圆孢子虫感染的初步调查[J]. 中华流行病学杂志, 2003,24(2):93.)
[43] Chen XY, Xu LF. Infection of Cyclospora cayetanensis in children with diarrhea in a city[J]. Chin J Sch Heal, 2006,27(9):817-818. (in Chinese)
[43] ( 陈晓宇, 许礼发. 某市幼儿腹泻患者圆孢子虫感染情况[J]. 中国学校卫生, 2006,27(9):817-818.)
[44] Zhou Y, Lv B, Wang Q, et al. Prevalence and molecular characterization of Cyclospora cayetanensis, Henan, China[J]. Emerg Infect Dis, 2011,17(10):1887-1890.
[45] Tsang OT, Wong RW, Lam BH, et al. Cyclospora infection in a young woman with human immunodeficiency virus in Hong Kong: a case report[J]. BMC Res Notes, 2013,6:521.
[46] Jiang YY, Yuan ZY, Zang GQ, et al. Cyclospora cayetanensis infections among diarrheal outpatients in Shanghai: a retrospective case study[J]. Front Med, 2018,12(1):98-103.
[47] Li J, Chang Y, Shi KE, et al. Multilocus sequence typing and clonal population genetic structure of Cyclospora cayetanensis in humans[J]. Parasitology, 2017,144(14):1890-1897.
[48] Ni BX, Wu XM, Liu YH, et al. Establishment and evaluation of the detection method of Cryptosporidium specific DNA fragment by recombinase aided isothermal amplification[J]. Chin J Schisto Control, 2019,31(4):388-392, 399. (in Chinese)
[48] ( 倪碧娴, 吴小珉, 刘燕红, 等. 重组酶介导的隐孢子虫属特异性等温核酸扩增方法的建立及评价[J]. 中国血吸虫病防治杂志, 2019,31(4):388-392, 399.)
[49] Zhao S, Li T, Yang K, et al. Establishment of a recombinase-aided isothermal amplification technique to detect Schistosoma japonicum specific gene fragments[J]. Chin J Schisto Control, 2018,30(3):273-277, 306. (in Chinese)
[49] ( 赵松, 李婷, 杨坤, 等. 重组酶介导的日本血吸虫特异性基因片段核酸等温扩增检测方法的建立[J]. 中国血吸虫病防治杂志, 2018,30(3):273-277, 306.)
[50] Zhang Q, Ding X, Wu XM, et al. Establishment and preliminary evaluation of recombinase aided isothermal amplification(RAA) assay for specific nucleic acid detection of Clonorchis sinensis[J]. Chin J Schisto Control, 2019,31(5):468-473. (in Chinese)
[50] ( 张强, 丁昕, 吴小珉, 等. 重组酶介导的华支睾吸虫特异性核酸等温扩增方法的建立及初步评价[J]. 中国血吸虫病防治杂志, 2019,31(5):468-473.)
[51] Crannell Z, Castellanos-Gonzalez A, Nair G, et al. Multiplexed recombinase polymerase amplification assay to detect intestinal protozoa[J]. Anal Chem, 2016,88(3):1610-1616.
[52] Wu YD, Zhou DH, Zhang LX, et al. Recombinase polymerase amplification (RPA) combined with lateral flow (LF) strip for equipment-free detection of Cryptosporidium spp. oocysts in dairy cattle feces[J]. Parasitol Res, 2016,115(9):3551-3555.
[53] Yuan ZY, Shen YJ, Cao JP, et al. Detection of cattle-origin Cryptosporidium bovis by loop-mediated isothermal amplification[J]. Int J Med Parasit Dis, 2009,36(3):144-146. (in Chinese)
[53] ( 袁忠英, 沈玉娟, 曹建平, 等. 环介导等温扩增技术检测牛源隐孢子虫的研究[J]. 国际医学寄生虫病杂志, 2009,36(3):144-146.)
[54] Lu WY, Yuan ZY, Shen YJ, et al. Detection of Giardia lamblia by loop-mediated isothermal amplification[J]. Int J Med Parasit Dis, 2010,37(3):145-147. (in Chinese)
[54] ( 卢潍媛, 袁忠英, 沈玉娟, 等. 环介导等温扩增技术检测蓝氏贾第鞭毛虫[J]. 国际医学寄生虫病杂志, 2010,37(3):145-147.)
[55] Yang RC, Paparini A, Monis P, et al. Comparison of next-generation droplet digital PCR (ddPCR) with quantitative PCR (qPCR) for enumeration of Cryptosporidium oocysts in faecal samples[J]. Int J Parasitol, 2014,44(14):1105-1113.
[56] Sanders R, Huggett JF, Bushell CA, et al. Evaluation of digital PCR for absolute DNA quantification[J]. Anal Chem, 2011,83(17):6474-6484.
[57] Narayanan Unni H, Hartono D, Yue Lanry Yung L, et al. Characterization and separation of Cryptosporidium and Giardia cells using on-chip dielectrophoresis[J]. Biomicrofluidics, 2012,6(1):12805-12819.
[58] Mero S, Kirveskari J, Antikainen J, et al. Multiplex PCR detection of Cryptosporidium sp., Giardia lamblia and Entamoeba histolytica directly from dried stool samples from Guinea-Bissauan children with diarrhoea[J]. Infect Dis, 2017,49(9):655-663.
[59] Won EJ, Kim SH, Kee SJ, et al. Multiplex real-time PCR assay targeting eight parasites customized to the Korean population: potential use for detection in diarrheal stool samples from gastroenteritis patients[J]. PLoS One, 2016,11(11):e0166957.
[60] Mengelle C, Mansuy JM, Prere MF, et al. Simultaneous detection of gastrointestinal pathogens with a multiplex Luminex-based molecular assay in stool samples from diarrhoeic patients[J]. Clin Microbiol Infect, 2013,19(10):E458-E465.
[61] Zahedi A, Gofton AW, Greay T, et al. Profiling the diversity of Cryptosporidium species and genotypes in wastewater treatment plants in Australia using next generation sequencing[J]. Sci Total Environ, 2018,644:635-648.
[62] Zahedi A, Greay TL, Paparini A, et al. Identification of eukaryotic microorganisms with 18S rRNA next-generation sequencing in wastewater treatment plants, with a more targeted NGS approach required for Cryptosporidium detection[J]. Water Res, 2019,158:301-312.
[63] Zhou XN. Potential impacts of climate change on human health[J]. Adv Clim Chang Res, 2010,6(4):235-240. (in Chinese)
[63] ( 周晓农. 气候变化与人体健康[J]. 气候变化研究进展, 2010,6(4):235-240.)
[64] Ahmed SA, Guerrero Flórez M, Karanis P. The impact of water crises and climate changes on the transmission of protozoan parasites in Africa[J]. Pathog Glob Health, 2018,112(6):281-293.
[65] Adegoke AA, Amoah ID, Stenstr?m TA, et al. Epidemiological evidence and health risks associated with agricultural reuse of partially treated and untreated wastewater: a review[J]. Front Public Health, 2018,6:337.
[66] Li N, Xiao LH, Wang L, et al. Molecular surveillance of Cryptosporidium spp., Giardia duodenalis, and Enterocytozoon bieneusi by genotyping and subtyping parasites in wastewater[J]. PLoS Negl Trop Dis, 2012,6(9):e1809.
[67] Hu Y, Feng Y, Huang C, et al. Occurrence, source, and human infection potential of Cryptosporidium and Enterocytozoon bieneusi in drinking source water in Shanghai, China, during a pig carcass disposal incident[J]. Environ Sci Technol, 2014,48(24):14219-14227.
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