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Published in: BMC Infectious Diseases 1/2019

Open Access 01-12-2019 | Helminths | Research article

Prevalence of intestinal helminth infections in Jiangsu Province, eastern China; a cross-sectional survey conducted in 2015

Authors: Yang Dai, Xiangzhen Xu, Jianfeng Liu, Xiaolin Jin, Mingxue Shen, Xiaoting Wang, Jun Cao, Haitao Yang

Published in: BMC Infectious Diseases | Issue 1/2019

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Abstract

Background

Intestinal helminth infections are a serious public health problem in developing countries. Jiangsu, an eastern coastal province of China, has an environment conducive to the transmission of intestinal parasites, and suffered human infection rates of 71.75% in 1990. Due to comprehensive anti-transmission measures undertaken throughout the province in the 1990s, the prevalence had decreased to 9.28% in 2002. In order to assess the current epidemic situation for intestinal parasitic infections in Jiangsu province, a province-wide cross-sectional survey was carried out in 2015.

Methods

Surveys were conducted in two main settings; rural (for soil-transmitted parasites) and urban (for Clonorchis sinensis), selected through stratified random sampling. Human infection rates were evaluated through the detection of helminth eggs or cysts (oocysts or trophozoites) of intestinal protozoa in fecal samples by microscopy. Secondary intermediate and reservoir hosts were surveyed for C. sinensis infection. Questionnaires were completed by each participant to evaluate knowledge, attitude and practice of soil-transmitted parasite and C. sinensis avoidance.

Results

115 out of 30153 participants (0.38%) had intestinal helminths or protozoa. There were eight species of helminth detected and the most common parasite was the hookworm Ancylostoma duodenale. In rural settings, there were significant differences in infection rates between participants of differing economic status. In urban settings, only four cases of C. sinensis infection were detected. However, secondary intermediate and reservoir hosts were found to harbor parasites. The questionnaire survey revealed that 38.42% participants were not aware of how humans become infected by hookworms. Knowledge and awareness of C. sinensis was similarly low, with 53.22% participants combining the use of chopping boards for raw and cooked food items when preparing meals.

Conclusions

The prevalence of intestinal parasitic infections in Jiangsu Province in eastern China has decreased from 71.57% in 1990 to 0.38% in 2015. Control measures should now focus on parasitic infections in the elderly and in children, health promotion and the development of alternative detection methods.
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Literature
1.
go back to reference Ojha SC, Jaide C, Jinawath N, Rotjanapan P, Baral P. Geohelminths: public health significance. J Infect Dev Ctries. 2014;8(1):5–16.CrossRef Ojha SC, Jaide C, Jinawath N, Rotjanapan P, Baral P. Geohelminths: public health significance. J Infect Dev Ctries. 2014;8(1):5–16.CrossRef
2.
go back to reference Hotez PJ, Bundy DAP, Beegle K, Brooker S, Drake L, de Silva N, Montresor A, Engels D, Jukes M, Chitsulo L et al. Helminth Infections: Soil-transmitted Helminth Infections and Schistosomiasis (Chapter 24). Disease Control Priorities in Developing Countries. In: Jamison DT, Breman JG, Measham AR, Alleyne G, Claeson M, Evans DB, Jha P, Mills A, Musgrove P. Editors. Washington (DC): The International Bank of Reconstruction and Development/The World Bank. New York: Oxford University Press; 2006. Hotez PJ, Bundy DAP, Beegle K, Brooker S, Drake L, de Silva N, Montresor A, Engels D, Jukes M, Chitsulo L et al. Helminth Infections: Soil-transmitted Helminth Infections and Schistosomiasis (Chapter 24). Disease Control Priorities in Developing Countries. In: Jamison DT, Breman JG, Measham AR, Alleyne G, Claeson M, Evans DB, Jha P, Mills A, Musgrove P. Editors. Washington (DC): The International Bank of Reconstruction and Development/The World Bank. New York: Oxford University Press; 2006.
3.
go back to reference Pullan RL, Brooker SJ. The global limits and population at risk of soil-transmitted helminth infections in 2010. Parasit Vectors. 2012;5:81.CrossRef Pullan RL, Brooker SJ. The global limits and population at risk of soil-transmitted helminth infections in 2010. Parasit Vectors. 2012;5:81.CrossRef
4.
go back to reference Pullan RL, Smith JL, Jasrasaria R, Brooker SJ. Global numbers of infection and disease burden of soil transmitted helminth infections in 2010. Parasit Vectors. 2014;7:37.CrossRef Pullan RL, Smith JL, Jasrasaria R, Brooker SJ. Global numbers of infection and disease burden of soil transmitted helminth infections in 2010. Parasit Vectors. 2014;7:37.CrossRef
5.
go back to reference Yang GJ, Liu L, Zhu HR, Griffiths SM, Tanner M, Bergquist R, Utzinger J, Zhou XN. China's sustained drive to eliminate neglected tropical diseases. Lancet Infect Dis. 2014;14(9):881–92.CrossRef Yang GJ, Liu L, Zhu HR, Griffiths SM, Tanner M, Bergquist R, Utzinger J, Zhou XN. China's sustained drive to eliminate neglected tropical diseases. Lancet Infect Dis. 2014;14(9):881–92.CrossRef
6.
go back to reference Coordinating Office of the National Survey on the Important Human Parasitic D. A national survey on current status of the important parasitic diseases in human population. Zhongguo ji sheng chong xue yu ji sheng chong bing za zhi = Chinese journal of parasitology & parasitic diseases. 2005;23(5 Suppl):332–40. Coordinating Office of the National Survey on the Important Human Parasitic D. A national survey on current status of the important parasitic diseases in human population. Zhongguo ji sheng chong xue yu ji sheng chong bing za zhi = Chinese journal of parasitology & parasitic diseases. 2005;23(5 Suppl):332–40.
7.
go back to reference Furst T, Keiser J, Utzinger J. Global burden of human food-borne trematodiasis: a systematic review and meta-analysis. Lancet Infect Dis. 2012;12(3):210–21.CrossRef Furst T, Keiser J, Utzinger J. Global burden of human food-borne trematodiasis: a systematic review and meta-analysis. Lancet Infect Dis. 2012;12(3):210–21.CrossRef
8.
go back to reference Evans AC, Stephenson LS. Not by drugs alone: the fight against parasitic helminths. World Health Forum. 1995;16(3):258–61.PubMed Evans AC, Stephenson LS. Not by drugs alone: the fight against parasitic helminths. World Health Forum. 1995;16(3):258–61.PubMed
9.
go back to reference Actor JK, Shirai M, Kullberg MC, Buller RM, Sher A, Berzofsky JA. Helminth infection results in decreased virus-specific CD8+ cytotoxic T-cell and Th1 cytokine responses as well as delayed virus clearance. Proc Natl Acad Sci U S A. 1993;90(3):948–52.CrossRef Actor JK, Shirai M, Kullberg MC, Buller RM, Sher A, Berzofsky JA. Helminth infection results in decreased virus-specific CD8+ cytotoxic T-cell and Th1 cytokine responses as well as delayed virus clearance. Proc Natl Acad Sci U S A. 1993;90(3):948–52.CrossRef
10.
go back to reference Bentwich Z, Kalinkovich A, Weisman Z. Immune activation is a dominant factor in the pathogenesis of African AIDS. Immunol Today. 1995;16(4):187–91.CrossRef Bentwich Z, Kalinkovich A, Weisman Z. Immune activation is a dominant factor in the pathogenesis of African AIDS. Immunol Today. 1995;16(4):187–91.CrossRef
11.
go back to reference Nacher M, Singhasivanon P, Gay F, Phumratanaprapin W, Silachamroon U, Looareesuwan S. Association of helminth infection with decreased reticulocyte counts and hemoglobin concentration in Thai falciparum malaria. Am J Trop Med Hyg. 2001;65(4):335–7.CrossRef Nacher M, Singhasivanon P, Gay F, Phumratanaprapin W, Silachamroon U, Looareesuwan S. Association of helminth infection with decreased reticulocyte counts and hemoglobin concentration in Thai falciparum malaria. Am J Trop Med Hyg. 2001;65(4):335–7.CrossRef
12.
go back to reference Lun ZR, Gasser RB, Lai DH, Li AX, Zhu XQ, Yu XB, Fang YY. Clonorchiasis: a key foodborne zoonosis in China. Lancet Infect Dis. 2005;5(1):31–41.CrossRef Lun ZR, Gasser RB, Lai DH, Li AX, Zhu XQ, Yu XB, Fang YY. Clonorchiasis: a key foodborne zoonosis in China. Lancet Infect Dis. 2005;5(1):31–41.CrossRef
13.
go back to reference Qian MB, Utzinger J, Keiser J, Zhou XN. Clonorchiasis. Lancet. 2016;387(10020):800–10.CrossRef Qian MB, Utzinger J, Keiser J, Zhou XN. Clonorchiasis. Lancet. 2016;387(10020):800–10.CrossRef
14.
go back to reference Campbell SJ, Nery SV, McCarthy JS, Gray DJ, Soares Magalhaes RJ, Clements ACA. A critical appraisal of control strategies for soil-transmitted helminths. Trends Parasitol. 2016;32(2):97–107.CrossRef Campbell SJ, Nery SV, McCarthy JS, Gray DJ, Soares Magalhaes RJ, Clements ACA. A critical appraisal of control strategies for soil-transmitted helminths. Trends Parasitol. 2016;32(2):97–107.CrossRef
15.
go back to reference Zheng Q, Chen Y, Zhang HB, Chen JX, Zhou XN. The control of hookworm infection in China. Parasit Vectors. 2009;2(1):44.CrossRef Zheng Q, Chen Y, Zhang HB, Chen JX, Zhou XN. The control of hookworm infection in China. Parasit Vectors. 2009;2(1):44.CrossRef
16.
go back to reference Gass K, Addiss DG, Freeman MC. Exploring the relationship between access to water, sanitation and hygiene and soil-transmitted helminth infection: a demonstration of two recursive partitioning tools. PLoS Negl Trop Dis. 2014;8(6):e2945.CrossRef Gass K, Addiss DG, Freeman MC. Exploring the relationship between access to water, sanitation and hygiene and soil-transmitted helminth infection: a demonstration of two recursive partitioning tools. PLoS Negl Trop Dis. 2014;8(6):e2945.CrossRef
17.
go back to reference Strunz EC, Addiss DG, Stocks ME, Ogden S, Utzinger J, Freeman MC. Water, sanitation, hygiene, and soil-transmitted helminth infection: a systematic review and meta-analysis. PLoS Med. 2014;11(3):e1001620.CrossRef Strunz EC, Addiss DG, Stocks ME, Ogden S, Utzinger J, Freeman MC. Water, sanitation, hygiene, and soil-transmitted helminth infection: a systematic review and meta-analysis. PLoS Med. 2014;11(3):e1001620.CrossRef
18.
go back to reference Mahmud MA, Spigt M, Bezabih AM, Pavon IL, Dinant GJ, Velasco RB. Efficacy of Handwashing with Soap and Nail Clipping on Intestinal Parasitic Infections in School-Aged Children: A Factorial Cluster Randomized Controlled Trial. PLoS medicine. 2015;12(6):e1001837 discussion e1001837.CrossRef Mahmud MA, Spigt M, Bezabih AM, Pavon IL, Dinant GJ, Velasco RB. Efficacy of Handwashing with Soap and Nail Clipping on Intestinal Parasitic Infections in School-Aged Children: A Factorial Cluster Randomized Controlled Trial. PLoS medicine. 2015;12(6):e1001837 discussion e1001837.CrossRef
19.
go back to reference Bethony J, Chen J, Lin S, Xiao S, Zhan B, Li S, Xue H, Xing F, Humphries D, Yan W, et al. Emerging patterns of hookworm infection: influence of aging on the intensity of Necator infection in Hainan Province, People's Republic of China. Clin Infect Dis. 2002;35(11):1336–44.CrossRef Bethony J, Chen J, Lin S, Xiao S, Zhan B, Li S, Xue H, Xing F, Humphries D, Yan W, et al. Emerging patterns of hookworm infection: influence of aging on the intensity of Necator infection in Hainan Province, People's Republic of China. Clin Infect Dis. 2002;35(11):1336–44.CrossRef
20.
go back to reference McHardy IH, Wu M, Shimizu-Cohen R, Couturier MR, Humphries RM. Detection of intestinal protozoa in the clinical laboratory. J Clin Microbiol. 2014;52(3):712–20.CrossRef McHardy IH, Wu M, Shimizu-Cohen R, Couturier MR, Humphries RM. Detection of intestinal protozoa in the clinical laboratory. J Clin Microbiol. 2014;52(3):712–20.CrossRef
21.
go back to reference Amiri SA, Rahimi MT, Mahdavi SA, Moosazadeh M, Ramzani O, Koshk AF, Rosbehan R, Siyadatpanah SA. Prevalence of Enterobius vermicularis infection among preschool children, Babol, North of Iran. J Parasit Dis. 2016;40(4):1558–62.CrossRef Amiri SA, Rahimi MT, Mahdavi SA, Moosazadeh M, Ramzani O, Koshk AF, Rosbehan R, Siyadatpanah SA. Prevalence of Enterobius vermicularis infection among preschool children, Babol, North of Iran. J Parasit Dis. 2016;40(4):1558–62.CrossRef
22.
go back to reference Liu XG, Liu G, Zhang WW. Infection status of wild freshwater fish with Metacercariae of Clonorchis sinensis in west Liaoning. Zhongguo ji sheng chong xue yu ji sheng chong bing za zhi = Chinese journal of parasitology & parasitic diseases. 2011;29(2):157–8. Liu XG, Liu G, Zhang WW. Infection status of wild freshwater fish with Metacercariae of Clonorchis sinensis in west Liaoning. Zhongguo ji sheng chong xue yu ji sheng chong bing za zhi = Chinese journal of parasitology & parasitic diseases. 2011;29(2):157–8.
23.
go back to reference Montresor A, Compton DWT, Hall A, Bundy DAP, Savioli L. Guidelines for the Evaluation of Soil-Transmitted Helminthiasis and Schistosomiasis at Community Level. Geneva: World Health Organization; 1998. Montresor A, Compton DWT, Hall A, Bundy DAP, Savioli L. Guidelines for the Evaluation of Soil-Transmitted Helminthiasis and Schistosomiasis at Community Level. Geneva: World Health Organization; 1998.
24.
go back to reference Nematian J, Nematian E, Gholamrezanezhad A, Asgari AA. Prevalence of intestinal parasitic infections and their relation with socio-economic factors and hygienic habits in Tehran primary school students. Acta Trop. 2004;92(3):179–86.CrossRef Nematian J, Nematian E, Gholamrezanezhad A, Asgari AA. Prevalence of intestinal parasitic infections and their relation with socio-economic factors and hygienic habits in Tehran primary school students. Acta Trop. 2004;92(3):179–86.CrossRef
25.
go back to reference Quihui L, Valencia ME, Crompton DW, Phillips S, Hagan P, Morales G, Diaz-Camacho SP. Role of the employment status and education of mothers in the prevalence of intestinal parasitic infections in Mexican rural schoolchildren. BMC Public Health. 2006;6:225.CrossRef Quihui L, Valencia ME, Crompton DW, Phillips S, Hagan P, Morales G, Diaz-Camacho SP. Role of the employment status and education of mothers in the prevalence of intestinal parasitic infections in Mexican rural schoolchildren. BMC Public Health. 2006;6:225.CrossRef
26.
go back to reference Tarafder MR, Carabin H, Joseph L, Balolong E Jr, Olveda R, McGarvey ST. Estimating the sensitivity and specificity of Kato-Katz stool examination technique for detection of hookworms, Ascaris lumbricoides and Trichuris trichiura infections in humans in the absence of a 'gold standard'. Int J Parasitol. 2010;40(4):399–404.CrossRef Tarafder MR, Carabin H, Joseph L, Balolong E Jr, Olveda R, McGarvey ST. Estimating the sensitivity and specificity of Kato-Katz stool examination technique for detection of hookworms, Ascaris lumbricoides and Trichuris trichiura infections in humans in the absence of a 'gold standard'. Int J Parasitol. 2010;40(4):399–404.CrossRef
27.
go back to reference Habtamu K, Degarege A, Ye-Ebiyo Y, Erko B. Comparison of the Kato-Katz and FLOTAC techniques for the diagnosis of soil-transmitted helminth infections. Parasitol Int. 2011;60(4):398–402.CrossRef Habtamu K, Degarege A, Ye-Ebiyo Y, Erko B. Comparison of the Kato-Katz and FLOTAC techniques for the diagnosis of soil-transmitted helminth infections. Parasitol Int. 2011;60(4):398–402.CrossRef
28.
go back to reference de Boer RF, Ott A, Kesztyus B, Kooistra-Smid AM. Improved detection of five major gastrointestinal pathogens by use of a molecular screening approach. J Clin Microbiol. 2010;48(11):4140–6.CrossRef de Boer RF, Ott A, Kesztyus B, Kooistra-Smid AM. Improved detection of five major gastrointestinal pathogens by use of a molecular screening approach. J Clin Microbiol. 2010;48(11):4140–6.CrossRef
29.
go back to reference Mengelle C, Mansuy JM, Prere MF, Grouteau E, Claudet I, Kamar N, Huynh A, Plat G, Benard M, Marty N, et al. Simultaneous detection of gastrointestinal pathogens with a multiplex Luminex-based molecular assay in stool samples from diarrhoeic patients. Clin Microbiol Infect. 2013;19(10):E458–65.CrossRef Mengelle C, Mansuy JM, Prere MF, Grouteau E, Claudet I, Kamar N, Huynh A, Plat G, Benard M, Marty N, et al. Simultaneous detection of gastrointestinal pathogens with a multiplex Luminex-based molecular assay in stool samples from diarrhoeic patients. Clin Microbiol Infect. 2013;19(10):E458–65.CrossRef
30.
go back to reference Verweij JJ, Stensvold CR. Molecular testing for clinical diagnosis and epidemiological investigations of intestinal parasitic infections. Clin Microbiol Rev. 2014;27(2):371–418.CrossRef Verweij JJ, Stensvold CR. Molecular testing for clinical diagnosis and epidemiological investigations of intestinal parasitic infections. Clin Microbiol Rev. 2014;27(2):371–418.CrossRef
Metadata
Title
Prevalence of intestinal helminth infections in Jiangsu Province, eastern China; a cross-sectional survey conducted in 2015
Authors
Yang Dai
Xiangzhen Xu
Jianfeng Liu
Xiaolin Jin
Mingxue Shen
Xiaoting Wang
Jun Cao
Haitao Yang
Publication date
01-12-2019
Publisher
BioMed Central
Published in
BMC Infectious Diseases / Issue 1/2019
Electronic ISSN: 1471-2334
DOI
https://doi.org/10.1186/s12879-019-4264-0

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