Hostname: page-component-586b7cd67f-r5fsc Total loading time: 0 Render date: 2024-11-26T08:13:59.813Z Has data issue: false hasContentIssue false
  • English
  • Français

Familial aggregation of human helminth infection in the Poyang lake area of China with a focus on genetic susceptibility to schistosomiasis japonica and associated markers of disease

Published online by Cambridge University Press:  02 June 2009

M. K. ELLIS  and
D. P. McMANUS
M. K. ELLIS*
Affiliation:
Molecular Parasitology Laboratory, Australian Centre for International and Tropical Health and Nutrition, The Queensland Institute of Medical Research 300, Herston Road, Herston, Brisbane, Queensland 4029, Australia
D. P. McMANUS
Affiliation:
Molecular Parasitology Laboratory, Australian Centre for International and Tropical Health and Nutrition, The Queensland Institute of Medical Research 300, Herston Road, Herston, Brisbane, Queensland 4029, Australia
*
*Corresponding author. Tel: +61 7 33620401. Fax: +61 7 33620405. E-mail: [email protected]
Get access Rights & Permissions [Opens in a new window]

Summary

Human helminthiases are common in China, especially in rural areas where sanitation conditions are poor. Soil-transmitted helminths (STHs) are predominantly found in the southern provinces. Schistosoma japonicum is also endemic to southern China. Here we review the prevalence of helminth infections and polyparasitism in China, and discuss the interactions between helminth parasites in the co-infected host. It is clear that STHs are more prevalent in rural China than previously suggested emphasizing the need for systematic control of STHs. Further, the need for improved sanitation and hygiene conditions to prevent parasite transmission is highlighted. We provide supporting evidence for human genetic susceptibility to both single helminth infection and polyparasitism, and suggest that susceptibility to helminths infections may not be independent of one or the other. We demonstrate an association between single nucleotide polymorphism (SNP) variants in IL-5 and symptomatic S. japonicum infection and discuss the potential role of IL-5 in other helminth infections. Fundamental to disease and morbidity control is adequate and effective diagnosis and surveillance of disease. We discuss the role of sICAM-1 and TNFR-I and -II as candidate markers for schistosome-induced hepatomegaly and fibrosis, and their potential for assessing disease stage and progression in schistosomiasis.

Keywords

Schistosoma japonicumAscaris lumbricoidesTrichuris trichiuragenetic susceptibilityhepatic inflammationChina
Type
Review Article
Information
Parasitology , Volume 136 , Issue 7 , June 2009 , pp. 699 - 712
Copyright
Copyright © Cambridge University Press 2009

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

REFERENCES

Abdalla, A., Sheesha, A. A., Shokeir, M., El-Agrody, O., El-Regal, M. E., Abdel-Khalik, M. K., Freeman, K., Boneberg, A. and Hh, A. K. (2002). Serum intercellular adhesion molecule-I in children with chronic liver disease: relationship to disease activity. Digestive Diseases and Sciences 47, 1206–1208.CrossRefGoogle ScholarPubMed
Abel, L., Demenais, F., Prata, A., Souza, A. E. and Dessein, A. (1991). Evidence for the segregation of a major gene in human susceptibility/resistance to infection by Schistosoma mansoni. American Journal of Human Genetics 48, 959–970.Google Scholar
Akgun, Y. (1996). Intestinal obstruction caused by Ascaris lumbricoides. Diseases of the Colon & Rectum 39, 1159–1163.CrossRefGoogle ScholarPubMed
Al-Sherbiny, M., Osman, A., Barakat, R., El Morshedy, H., Bergquist, R. and Olds, R. (2003). In vitro cellular and humoral responses to Schistosoma mansoni vaccine candidate antigens. Acta Tropica 88, 117–130.CrossRefGoogle ScholarPubMed
Anderson, R. M. and Gordon, D. M. (1982). Processes influencing the distribution of parasite numbers within host populations with special emphasis on parasite-induced host mortalities. Parasitology 85, 373–398.CrossRefGoogle ScholarPubMed
Asaolu, S. O. and Ofoezie, I. E. (2003). The role of health education and sanitation in the control of helminth infections. Acta Tropica 86, 283–294.CrossRefGoogle ScholarPubMed
Barnes, K. C., Grant, A. V. and Gao, P. (2005). A review of the genetic epidemiology of resistance to parasitic disease and atopic asthma: common variants for common phenotypes? Current Opinion in Allergy and Clinical Immunology 5, 379–385.CrossRefGoogle ScholarPubMed
Belizario, V. Y. Jr., De Leon, W. U., Lumampao, Y. F., Anastacio, M. B. and Tai, C. M. (2009). Sentinel surveillance of soil-transmitted helminthiasis in selected local government units in the Philippines. Asia-Pacific Journal of Public Health 21, 26–42.CrossRefGoogle ScholarPubMed
Bethony, J., Brooker, S., Albonico, M., Geiger, S. M., Loukas, A., Diemert, D. and Hotez, P. J. (2006). Soil-transmitted helminth infections: ascariasis, trichuriasis, and hookworm. Lancet 367, 1521–1532.CrossRefGoogle ScholarPubMed
Bethony, J., Gazzinelli, A., Lopes, A., Pereira, W., Alves-Oliveira, L., Willams-Blangero, S., Blangero, J., Loverde, P. and Correa-Oliveira, R. (2001). Genetic epidemiology of fecal egg excretion during Schistosoma mansoni infection in an endemic area in Minas Gerais, Brazil. Memorias do Instituto Oswaldo Cruz 96 (Suppl.), 49–55.CrossRefGoogle Scholar
Bethony, J., Williams, J. T., Blangero, J., Kloos, H., Gazzinelli, A., Soares-Filho, B., Coelho, L., Alves-Fraga, L., Williams-Blangero, S., Loverde, P. T. and Correa-Oliveira, R. (2002). Additive host genetic factors influence fecal egg excretion rates during Schistosoma mansoni infection in a rural area in Brazil. American Journal of Tropical Medicine and Hygiene 67, 336–343.CrossRefGoogle Scholar
Bierman, W. F., Wetsteyn, J. C. and Van Gool, T. (2005). Presentation and diagnosis of imported schistosomiasis: relevance of eosinophilia, microscopy for ova, and serology. Journal of Travel Medicine 12, 9–13.CrossRefGoogle ScholarPubMed
Bonnard, P., Remoue, F., Schacht, A. M., Pialoux, G. and Riveau, G. (2006). Association between serum cytokine profiles and schistosomiasis-related hepatic fibrosis: infection by Schistosoma japonicum versus S. mansoni. Journal of Infectious Diseases 193, 748–749; author reply 749–750.CrossRefGoogle ScholarPubMed
Booth, M., Guyatt, H. L., Li, Y. and Tanner, M. (1996). The morbidity attributable to Schistosoma japonicum infection in 3 villages in Dongting Lake region, Hunan province, PR China. Tropical Medicine & International Health 1, 646–654.CrossRefGoogle ScholarPubMed
Booth, M., Mwatha, J. K., Joseph, S., Jones, F. M., Kadzo, H., Ireri, E., Kazibwe, F., Kemijumbi, J., Kariuki, C., Kimani, G., Ouma, J. H., Kabatereine, N. B., Vennervald, B. J. and Dunne, D. W. (2004). Periportal fibrosis in human Schistosoma mansoni infection is associated with low IL-10, low IFN-gamma, high TNF-alpha, or low RANTES, depending on age and gender. Journal of Immunology 172, 1295–1303.CrossRefGoogle ScholarPubMed
Bradley, D. J. and May, R. M. (1978). Consequences of helminth aggregation for the dynamics of schistosomiasis. Tranactions of the Royal Society Tropical Medicine and Hygiene 72, 262–273.CrossRefGoogle ScholarPubMed
Breitling, L. P., Wilson, A. J., Raiko, A., Lagog, M., Siba, P., Shaw, M. A. and Quinnell, R. J. (2008). Heritability of human hookworm infection in Papua New Guinea. Parasitology 135, 1407–1415.CrossRefGoogle ScholarPubMed
Broide, D. H., Hoffman, H. and Sriramarao, P. (1999). Genes that regulate eosinophilic inflammation. American Journal of Human Genetics 65, 302–307.CrossRefGoogle ScholarPubMed
Bundy, D. A., Cooper, E. S., Thompson, D. E., Didier, J. M., Anderson, R. M. and Simmons, I. (1987). Predisposition to Trichuris trichiura infection in humans. Epidemiology and Infection 98, 65–71.CrossRefGoogle ScholarPubMed
Bundy, D. A. and Cooper, E. S. (1989). Trichuris and trichuriasis in humans. Advances in Parasitology 28, 107–173.CrossRefGoogle ScholarPubMed
Burchard, G. D., Guisse-Sow, F., Diop, M., Ly, A., Lanuit, R., Gryseels, B. and Gressner, A. M. (1998). Schistosoma mansoni infection in a recently exposed community in Senegal: lack of correlation between liver morphology in ultrasound and connective tissue metabolites in serum. Tropical Medicine & International Health 3, 234–241.CrossRefGoogle Scholar
Burke, M. L., Jones, M. K., Gobert, G. N., Li, Y. S., Ellis, M. K. and McManus, D. P. (2009). Immunopathogenesis in human schistosomiasis. Parasite Immunology 31, 163–176.CrossRefGoogle ScholarPubMed
Campino, S., Kwiatkowski, D. and Dessein, A. (2006). Mendelian and complex genetics of susceptibility and resistance to parasitic infections. Seminars in Immunology 18, 411–422.CrossRefGoogle ScholarPubMed
Chan, L., Bundy, D. A. and Kan, S. P. (1994). Aggregation and predisposition to Ascaris lumbricoides and Trichuris trichiura at the familial level. Transactions of the Royal Society of Tropical Medicine and Hygiene 88, 46–48.CrossRefGoogle ScholarPubMed
Chen, Y. D., Tang, L. H. and Xu, L. Q. (2008). Current status of soil-transmitted nematode infection in China. Biomedical and Environmental Sciences 21, 173–179.CrossRefGoogle ScholarPubMed
Cooper, P. J., Chico, M. E., Sandoval, C., Espinel, I., Guevara, A., Kennedy, M. W., Urban, J. F. Jr., Griffin, G. E. and Nutman, T. B. (2000). Human infection with Ascaris lumbricoides is associated with a polarized cytokine response. Journal of Infectious Diseases 182, 1207–1213.CrossRefGoogle ScholarPubMed
Coutinho, H. M., Mcgarvey, S. T., Acosta, L. P., Manalo, D. L., Langdon, G. C., Leenstra, T., Kanzaria, H. K., Solomon, J., Wu, H., Olveda, R. M., Kurtis, J. D. and Friedman, J. F. (2005). Nutritional status and serum cytokine profiles in children, adolescents, and young adults with Schistosoma japonicum-associated hepatic fibrosis, in Leyte, Philippines. Journal of Infectious Diseases 192, 528–536.CrossRefGoogle Scholar
De Jesus, A. R., Silva, A., Santana, L. B., Magalhaes, A., De Jesus, A. A., De Almeida, R. P., Rego, M. A., Burattini, M. N., Pearce, E. J. and Carvalho, E. M. (2002). Clinical and immunologic evaluation of 31 patients with acute schistosomiasis mansoni. Journal of Infectious Diseases 185, 98–105.CrossRefGoogle ScholarPubMed
Dessein, A., Kouriba, B., Eboumbou, C., Dessein, H., Argiro, L., Marquet, S., Elwali, N. E., Rodrigues, V., Li, Y., Doumbo, O. and Chevillard, C. (2004). Interleukin-13 in the skin and interferon-gamma in the liver are key players in immune protection in human schistosomiasis. Immunological Reviews 201, 180–190.CrossRefGoogle ScholarPubMed
Devaney, E. (2005). The end of the line for hookworm? An update on vaccine development. PLoS Med 2, e327.CrossRefGoogle ScholarPubMed
Ellis, M. K., Li, Y., Hou, X., Chen, H. and McManus, D. P. (2008). sTNFR-II and sICAM-1 are associated with acute disease and hepatic inflammation in schistosomiasis japonica. International Journal for Parasitology 38, 717–723.CrossRefGoogle ScholarPubMed
Ellis, M. K., Li, Y., Rong, Z., Chen, H. and McManus, D. P. (2006). Familial aggregation of human infection with Schistosoma japonicum in the Poyang Lake region, China. International Journal for Parasitology 36, 71–77.CrossRefGoogle ScholarPubMed
Ellis, M. K., Raso, G., Li, Y. S., Rong, Z., Chen, H. G. and McManus, D. P. (2007 a). Familial aggregation of human susceptibility to co- and multiple helminth infections in a population from the Poyang Lake region, China. International Journal for Parasitology 37, 1153–1161.CrossRefGoogle Scholar
Ellis, M. K., Zhao, Z. Z., Chen, H. G., Montgomery, G. W., Li, Y. S. and McManus, D. P. (2007 b). Analysis of the 5q31 33 locus shows an association between single nucleotide polymorphism variants in the IL-5 gene and symptomatic infection with the human blood fluke, Schistosoma japonicum. Journal of Immunology 179, 8366–8371.Google ScholarPubMed
Esrey, S. A., Potash, J. B., Roberts, L. and Shiff, C. (1991). Effects of improved water supply and sanitation on ascariasis, diarrhoea, dracunculiasis, hookworm infection, schistosomiasis, and trachoma. Bulletin of the World Health Organization 69, 609–621.Google ScholarPubMed
Esterre, P., Raobelison, A., Ramarokoto, C. E., Ravaoalimalala, V. E., Boisier, P. and Roux, J. (1998). Serum concentrations of sICAM-1, sE-, sP- and sL-selectins in patients with Schistosoma mansoni infection and association with disease severity. Parasite Immunology 20, 369–376.CrossRefGoogle ScholarPubMed
Finkelman, F. D., Shea-Donohue, T., Goldhill, J., Sullivan, C. A., Morris, S. C., Madden, K. B., Gause, W. C. and Urban, J. F. Jr. (1997). Cytokine regulation of host defense against parasitic gastrointestinal nematodes: lessons from studies with rodent models. Annual Review of Immunology 15, 505–533.CrossRefGoogle ScholarPubMed
Fleming, F. M., Brooker, S., Geiger, S. M., Caldas, I. R., Correa-Oliveira, R., Hotez, P. J. and Bethony, J. M. (2006). Synergistic associations between hookworm and other helminth species in a rural community in Brazil. Tropical Medicine & International Health 11, 56–64.CrossRefGoogle Scholar
Forbes, E., Hulett, M., Ahrens, R., Wagner, N., Smart, V., Matthaei, K. I., Brandt, E. B., Dent, L. A., Rothenberg, M. E., Tang, M., Foster, P. S. and Hogan, S. P. (2006). ICAM-1-dependent pathways regulate colonic eosinophilic inflammation. Journal of Leukocyte Biology 80, 330–341.CrossRefGoogle ScholarPubMed
Gandhi, N. S., Jizhang, C., Khoshnood, K., Fuying, X., Shanwen, L., Yaoruo, L., Bin, Z., Haechou, X., Chongjin, T., Yan, W., Wensen, W., Dungxing, H., Chong, C., Shuhua, X., Hawdon, J. M. and Hotez, P. J. (2001). Epidemiology of Necator americanus hookworm infections in Xiulongkan Village, Hainan Province, China: high prevalence and intensity among middle-aged and elderly residents. Journal of Parasitology 87, 739–743.CrossRefGoogle ScholarPubMed
Ganley-Leal, L. M., Mwinzi, P. N., Cetre-Sossah, C. B., Andove, J., Hightower, A. W., Karanja, D. M., Colley, D. G. and Secor, W. E. (2006). Correlation between eosinophils and protection against reinfection with Schistosoma mansoni and the effect of human immunodeficiency virus type 1 coinfection in humans. Infection and Immunity 74, 2169–2176.CrossRefGoogle ScholarPubMed
Gause, W. C., Urban, J. F. Jr. and Stadecker, M. J. (2003). The immune response to parasitic helminths: insights from murine models. Trends in Immunology 24, 269–277.CrossRefGoogle ScholarPubMed
Gilman, R. H., Chong, Y. H., Davis, C., Greenberg, B., Virik, H. K. and Dixon, H. B. (1983). The adverse consequences of heavy Trichuris infection. Transactions of the Royal Society of Tropical Medicine and Hygiene 77, 432–438.CrossRefGoogle ScholarPubMed
Haseeb, M. A., Shirazian, D. J. and Preis, J. (2001). Elevated serum levels of TNF-alpha, sTNF-RI and sTNF-RII in murine schistosomiasis correlate with schistosome oviposition and circumoval granuloma formation. Cytokine 15, 266–269.CrossRefGoogle ScholarPubMed
Henri, S., Chevillard, C., Mergani, A., Paris, P., Gaudart, J., Camilla, C., Dessein, H., Montero, F., Elwali, N. E., Saeed, O. K., Magzoub, M. and Dessein, A. J. (2002). Cytokine regulation of periportal fibrosis in humans infected with Schistosoma mansoni: IFN-gamma is associated with protection against fibrosis and TNF-alpha with aggravation of disease. Journal of Immunology 169, 929–936.CrossRefGoogle ScholarPubMed
Hong, S. T., Chai, J. Y., Choi, M. H., Huh, S., Rim, H. J. and Lee, S. H. (2006). A successful experience of soil-transmitted helminth control in the Republic of Korea. Korean Journal of Parasitology 44, 177–185.CrossRefGoogle ScholarPubMed
Hotez, P. J., Zheng, F., Long-Qi, X., Ming-Gang, C., Shu-Hua, X., Shu-Xian, L., Blair, D., Mcmanus, D. P. and Davis, G. M. (1997). Emerging and reemerging helminthiases and the public health of China. Emerging Infectious Diseases 3, 303–310.CrossRefGoogle ScholarPubMed
Hotez, P. J., Brindley, P. J., Bethony, J. M., King, C. H., Pearce, E. J. and Jacobson, J. (2008). Helminth infections: the great neglected tropical diseases. Journal of Clinical Investigation 118, 1311–1321.CrossRefGoogle ScholarPubMed
Jackson, J. A., Turner, J. D., Rentoul, L., Faulkner, H., Behnke, J. M., Hoyle, M., Grencis, R. K., Else, K. J., Kamgno, J., Boussinesq, M. and Bradley, J. E. (2004 a). T helper cell type 2 responsiveness predicts future susceptibility to gastrointestinal nematodes in humans. Journal of Infectious Diseases 190, 1804–1811.CrossRefGoogle ScholarPubMed
Jackson, J. A., Turner, J. D., Rentoul, L., Faulkner, H., Behnke, J. M., Hoyle, M., Grencis, R. K., Else, K. J., Kamgno, J., Bradley, J. E. and Boussinesq, M. (2004 b). Cytokine response profiles predict species-specific infection patterns in human GI nematodes. International Journal for Parasitology 34, 1237–1244.CrossRefGoogle ScholarPubMed
Jacobs, W. and Van Marck, E. (1998). Adhesion and co-stimulatory molecules in the pathogenesis of hepatic and intestinal schistosomiasis mansoni. Memorias do Instituto Oswaldo Cruz 93, 523–529.CrossRefGoogle ScholarPubMed
Kardorff, R., Mugashe, C., Gabone, R. M., Mahlert, C. and Doehring, E. (1999). Diagnostic value of connective tissue metabolites in Schistosoma mansoni related liver disease. Acta Tropica 73, 153–164.CrossRefGoogle ScholarPubMed
Katz, N., Chaves, A. and Pellegrino, J. (1972). A simple device for quantitative stool thick-smear technique in Schistosomiasis mansoni. Revista do Instituto de Medicina Tropical de São Paulo 14, 397–400.Google ScholarPubMed
Keiser, J., N'goran, E. K., Traore, M., Lohourignon, K. L., Singer, B. H., Lengeler, C., Tanner, M. and Utzinger, J. (2002). Polyparasitism with Schistosoma mansoni, geohelminths, and intestinal protozoa in rural Cote d'Ivoire. Journal for Parasitology 88, 461–466.Google ScholarPubMed
Khuroo, M. S. (1996). Ascariasis. Gastroenterology Clinics of North America 25, 553–577.CrossRefGoogle ScholarPubMed
Kouriba, B., Chevillard, C., Bream, J. H., Argiro, L., Dessein, H., Arnaud, V., Sangare, L., Dabo, A., Beavogui, A. H., Arama, C., Traore, H. A., Doumbo, O. and Dessein, A. (2005). Analysis of the 5q31-q33 locus shows an association between IL13-1055C/T IL-13-591A/G polymorphisms and Schistosoma haematobium infections. Journal of Immunology 174, 6274–6281.CrossRefGoogle ScholarPubMed
Leenstra, T., Acosta, L. P., Langdon, G. C., Manalo, D. L., Su, L., Olveda, R. M., Mcgarvey, S. T., Kurtis, J. D. and Friedman, J. F. (2006). Schistosomiasis japonica, anemia, and iron status in children, adolescents, and young adults in Leyte, Philippines 1. American Journal of Clinical Nutrition 83, 371–379.CrossRefGoogle Scholar
Li, Y. S., Chen, H. G., He, H. B., Hou, X. Y., Ellis, M. and McManus, D. P. (2005). A double-blind field trial on the effects of artemether on Schistosoma japonicum infection in a highly endemic focus in southern China. Acta Tropica 96, 184–190.CrossRefGoogle Scholar
Li, Y. S., Sleigh, A. C., Ross, A. G., Li, Y., Williams, G. M., Forsyth, S. J., Tanner, M. and McManus, D. P. (1999). A 2-year prospective study in China provides epidemiological evidence for resistance in humans to re-infection with Schistosoma japonicum. Annals of Tropical Medicine and Parasitology 93, 629–642.CrossRefGoogle Scholar
Liang, S., Yang, C., Zhong, B. and Qiu, D. (2006). Re-emerging schistosomiasis in hilly and mountainous areas of Sichuan, China. Bulletin of the World Health Organization 84, 139–144.CrossRefGoogle ScholarPubMed
Lin, S. Y., Wang, Y. Y. and Sheu, W. H. (2002). Increased serum leptin concentrations correlate with soluble tumour necrosis factor receptor levels in patients with cirrhosis. Clinical Endocrinology 57, 805–811.CrossRefGoogle ScholarPubMed
Manzella, A., Ohtomo, K., Monzawa, S. and Lim, J. H. (2008). Schistosomiasis of the liver. Abdom Imaging, [Epub ahead of print].CrossRefGoogle ScholarPubMed
Marquet, S., Abel, L., Hillaire, D. and Dessein, A. (1999). Full results of the genome-wide scan which localises a locus controlling the intensity of infection by Schistosoma mansoni on chromosome 5q31-q33. European Journal of Human Genetics 7, 88–97.CrossRefGoogle ScholarPubMed
Marquet, S., Abel, L., Hillaire, D., Dessein, H., Kalil, J., Feingold, J., Weissenbach, J. and Dessein, A. J. (1996). Genetic localization of a locus controlling the intensity of infection by Schistosoma mansoni on chromosome 5q31-q33. Nature Genetics 14, 181–184.CrossRefGoogle ScholarPubMed
Massara, C. L., Peixoto, S. V., Enk, M. J., Da Silva Barros, H., Dos Santos Carvalho, O., Sakurai, E. and Schall, V. (2006). Evaluation of an improved approach using residences of schistosomiasis-positive school children to identify carriers in an area of low endemicity. American Journal of Tropical Medicine and Hygiene 74, 495–499.CrossRefGoogle Scholar
Medeiros, I. M., Reed, S., Castelo, A. and Salomao, R. (2000). Circulating levels of sTNFR and discrepancy between cytotoxicity and immunoreactivity of TNF-alpha in patients with visceral leishmaniasis. Clinical Microbiology and Infection 6, 34–37.CrossRefGoogle ScholarPubMed
Montresor, A. (2007). Arithmetic or geometric means of eggs per gram are not appropriate indicators to estimate the impact of control measures in helminth infections. Transactions of the Royal Society of Tropical Medicine and Hygiene 101, 773–776.CrossRefGoogle Scholar
Mukhopadhyay, B., Saha, S., Maiti, S., Mitra, D., Banerjee, T. J., Jha, M., Mukhopadhyay, M., Samanta, N. and Das, S. (2001). Clinical appraisal of Ascaris lumbricoides, with special reference to surgical complications. Pediatric Surgery International 17, 403–405.CrossRefGoogle ScholarPubMed
Muller-Myhsok, B., Stelma, F. F., Guisse-Sow, F., Muntau, B., Thye, T., Burchard, G. D., Gryseels, B. and Horstmann, R. D. (1997). Further evidence suggesting the presence of a locus, on human chromosome 5q31-q33, influencing the intensity of infection with Schistosoma mansoni. American Journal of Human Genetics 61, 452–454.CrossRefGoogle ScholarPubMed
Mwatha, J. K., Kimani, G., Kamau, T., Mbugua, G. G., Ouma, J. H., Mumo, J., Fulford, A. J., Jones, F. M., Butterworth, A. E., Roberts, M. B. and Dunne, D. W. (1998). High levels of TNF, soluble TNF receptors, soluble ICAM-1, and IFN-gamma, but low levels of IL-5, are associated with hepatosplenic disease in human schistosomiasis mansoni. Journal of Immunology 160, 1992–1999.CrossRefGoogle ScholarPubMed
O'Lorcain, P. and Holland, C. V. (2000). The public health importance of Ascaris lumbricoides. Parasitology 121 (Suppl.), S51–S71.CrossRefGoogle ScholarPubMed
Peisong, G., Yamasaki, A., Mao, X. Q., Enomoto, T., Feng, Z., Gloria-Bottini, F., Bottini, E., Shirakawa, T., Sun, D. and Hopkin, J. M. (2004). An asthma-associated genetic variant of STAT6 predicts low burden of Ascaris worm infestation. Genes and Immunity 5, 58–62.CrossRefGoogle ScholarPubMed
Petit, J. M., Minello, A., Jooste, V., Bour, J. B., Galland, F., Duvillard, L., Verges, B., Olsson, N. O., Gambert, P. and Hillon, P. (2005). Decreased plasma adiponectin concentrations are closely related to steatosis in hepatitis C virus-infected patients. The Journal of Clinical Endocrinology and Metabolism 90, 2240–2243.CrossRefGoogle ScholarPubMed
Quinnell, R. J., Pritchard, D. I., Raiko, A., Brown, A. P. and Shaw, M. A. (2004). Immune responses in human necatoriasis: association between interleukin-5 responses and resistance to reinfection. Journal of Infectious Diseases 190, 430–438.CrossRefGoogle ScholarPubMed
Raso, G., Luginbühl, A., Adjoua, C. A., Ian-Bi, N. T., Silué, K. D., Matthys, B., Vounatsou, P., Wang, Y., Dumas, M. E., Holmes, E., Singer, B. H., Tanner, M., N'goran, E. K. and Utzinger, J. (2004). Multiple parasite infections and their relationship to self-reported morbidity in a community of rural Côte d'Ivoire. International Journal of Epidemiology 33, 1092–1102.CrossRefGoogle Scholar
Ritter, D. M. and McKerrow, J. H. (1996). Intercellular adhesion molecule 1 is the major adhesion molecule expressed during schistosome granuloma formation. Infection and Immunity 64, 4706–4713.CrossRefGoogle ScholarPubMed
Rodrigues, V. Jr., Abel, L., Piper, K. and Dessein, A. J. (1996). Segregation analysis indicates a major gene in the control of interleukin-5 production in humans infected with Schistosoma mansoni. American Journal of Human Genetics 59, 453–461.Google Scholar
Ross, A. G., Sleigh, A. C., Li, Y. S., Williams, G. M., Aligui, G. D. and McManus, D. P. (2000). Is there immunity to Schistosoma japonicum? Parasitology Today 16, 159–164.CrossRefGoogle ScholarPubMed
Ross, A. G., Sleigh, A. C., Li, Y. S., Williams, G. M., Li, Y., Waine, G. J., Tang, G. T., Forsyth, S. J. and McManus, D. P. (1998). Epidemiological identification of Chinese individuals putatively susceptible or insusceptible to Schistosoma japonicum: a prelude to immunogenetic study of human resistance to Asian schistosomiasis. Annals of Tropical Medicine and Parasitology 92, 765–774.CrossRefGoogle ScholarPubMed
Ross, A. G., Vickers, D., Olds, G. R., Shah, S. M. and McManus, D. P. (2007). Katayama syndrome. Lancet Infectious Diseases 7, 218–224.CrossRefGoogle ScholarPubMed
Sandouk, F., Haffar, S., Zada, M. M., Graham, D. Y. and Anand, B. S. (1997). Pancreatic-biliary ascariasis: experience of 300 cases. American Journal of Gastroenterology 92, 2264–2267.Google ScholarPubMed
Seto, E. Y., Lee, Y. J., Liang, S. and Zhong, B. (2007). Individual and village-level study of water contact patterns and Schistosoma japonicum infection in mountainous rural China. Tropical Medicine & International Health 12, 1199–1209.CrossRefGoogle ScholarPubMed
Seto, E. Y., Wu, W., Liu, H. Y., Chen, H. G., Hubbard, A., Holt, A. and Davis, G. M. (2008). Impact of changing water levels and weather on Oncomelania hupensis hupensis populations, the snail host of Schistosoma japonicum, downstream of the Three Gorges Dam. Ecohealth 5, 149–158.Google ScholarPubMed
Seto, E. Y., Zhong, B., Kouch, J., Hubbard, A. and Spear, R. C. (2005). Genetic and household risk factors for Schistosoma japonicum infection in the presence of larger scale environmental differences in the mountainous transmission areas of China. American Journal of Tropical Medicine and Hygiene 73, 1145–1150.CrossRefGoogle ScholarPubMed
Simon, H. U., Plotz, S. G., Dummer, R. and Blaser, K. (1999). Abnormal clones of T cells producing interleukin-5 in idiopathic eosinophilia. New England Journal of Medicine 341, 1112–1120.CrossRefGoogle ScholarPubMed
Song, Y., Xiao, S. H., Wu, W., Zhang, S. J., Xie, H. Q., Xu, X. P., Hu, X. Y., Cui, Q., Chen, M. G. and Zheng, J. (1998). Preventive effect of artemether on schistosome infection. Chinese Medical Journal 111, 123–127.Google ScholarPubMed
Sookoian, S., Castano, G., Burgueno, A. L., Gianotti, T. F., Rosselli, M. S. and Pirola, C. J. (2008). A diagnostic model to differentiate simple steatosis from nonalcoholic steatohepatitis based on the likelihood ratio form of Bayes theorem. Clinical Biochemistry, [Epub ahead of print].Google ScholarPubMed
Spear, R. C., Seto, E., Liang, S., Birkner, M., Hubbard, A., Qiu, D., Yang, C., Zhong, B., Xu, F., Gu, X. and Davis, G. M. (2004). Factors influencing the transmission of Schistosoma japonicum in the mountains of Sichuan Province of China. American Journal of Tropical Medicine and Hygiene 70, 48–56.CrossRefGoogle ScholarPubMed
Steinmann, P., Du, Z. W., Wang, L. B., Wang, X. Z., Jiang, J. Y., Li, L. H., Marti, H., Zhou, X. N. and Utzinger, J. (2008 a). Extensive multiparasitism in a village of Yunnan province, People's Republic of China, revealed by a suite of diagnostic methods. American Journal of Tropical Medicine and Hygiene 78, 760–769.CrossRefGoogle Scholar
Steinmann, P., Zhou, X. N., Du, Z. W., Jiang, J. Y., Xiao, S. H., Wu, Z. X., Zhou, H. and Utzinger, J. (2008 b). Tribendimidine and albendazole for treating soil-transmitted helminths, Strongyloides stercoralis and Taenia spp.: open-label randomized trial. PLoS Neglected Tropical Diseases 2, e322.CrossRefGoogle ScholarPubMed
Steinmann, P., Zhou, X. N., Li, Y. L., Li, H. J., Chen, S. R., Yang, Z., Fan, W., Jia, T. W., Li, L. H., Vounatsou, P. and Utzinger, J. (2007). Helminth infections and risk factor analysis among residents in Eryuan county, Yunnan province, China. Acta Tropica 104, 38–51.CrossRefGoogle ScholarPubMed
Stephenson, L. S., Holland, C. V. and Cooper, E. S. (2000 a). The public health significance of Trichuris trichiura. Parasitology 121, S73–S95.CrossRefGoogle ScholarPubMed
Stephenson, L. S., Latham, M. C. and Ottesen, E. A. (2000 b). Malnutrition and parasitic helminth infections. Parasitology 121, S23–S38.CrossRefGoogle ScholarPubMed
Tchuem Tchuenté, L. A., Behnke, J. M., Gilbert, F. S., Southgate, V. R. and Vercruysse, J. (2003). Polyparasitism with Schistosoma haematobium and soil-transmitted helminth infections among school children in Loum, Cameroon. Tropical Medicine & International Health 8, 975–986.CrossRefGoogle ScholarPubMed
Teixeira, M. M., Talvani, A., Tafuri, W. L., Lukacs, N. W. and Hellewell, P. G. (2001). Eosinophil recruitment into sites of delayed-type hypersensitivity reactions in mice. Journal of Leukocyte Biology 69, 353–360.CrossRefGoogle ScholarPubMed
Tian, Z., Xiao, S. H., Xiao, J. W., Zhou, Y. C., Liu, D. S., Zheng, J., Chen, M. G., Qu, G. S., Zhang, X. Y., Yao, X. M., Zhang, X. Z. and Zhang, D. L. (1997). Reduction of Schistosoma japonicum infection in an endemic area in islet with embankment after prophylaxis with oral artemether throughout the transmission season. Chinese Journal of Parasitology and Parasitic Diseases 15, 208–211.Google Scholar
Tokushige, K., Hashimoto, E., Tsuchiya, N., Kaneda, H., Taniai, M. and Shiratori, K. (2005). Clinical significance of soluble TNF receptor in Japanese patients with non-alcoholic steatohepatitis. Alcoholism, Clinical and Experimental Research 29, 298S–303S.CrossRefGoogle ScholarPubMed
Torre, F., Rossol, S., Pelli, N., Basso, M., Delfino, A. and Picciotto, A. (2004). Kinetics of soluble tumour necrosis factor (TNF)-alpha receptors and cytokines in the early phase of treatment for chronic hepatitis C: comparison between interferon (IFN)-alpha alone, IFN-alpha plus amantadine or plus ribavirin. Clinical and Experimental Immunology 136, 507–512.CrossRefGoogle ScholarPubMed
Turner, J. D., Faulkner, H., Kamgno, J., Cormont, F., Van Snick, J., Else, K. J., Grencis, R. K., Behnke, J. M., Boussinesq, M. and Bradley, J. E. (2003). Th2 cytokines are associated with reduced worm burdens in a human intestinal helminth infection. Journal of Infectious Diseases 188, 1768–1775.CrossRefGoogle Scholar
Wang, L. D., Chen, H. G., Guo, J. G., Zeng, X. J., Hong, X. L., Xiong, J. J., Wu, X. H., Wang, X. H., Wang, L. Y., Xia, G., Hao, Y., Chin, D. P. and Zhou, X. N. (2009). A strategy to control transmission of Schistosoma japonicum in China. New England Journal of Medicine 360, 121–128.CrossRefGoogle ScholarPubMed
World Health Organization (1999). Making a Difference. World Health Organization. Geneva, Switzerland.Google Scholar
Williams-Blangero, S., Blangero, J. and Bradley, M. (1997). Quantitative genetic analysis of susceptibility to hookworm infection in a population from rural Zimbabwe. Human Biology 69, 201–208.Google Scholar
Williams-Blangero, S., Mcgarvey, S. T., Subedi, J., Wiest, P. M., Upadhayay, R. P., Rai, D. R., Jha, B., Olds, G. R., Guanling, W. and Blangero, J. (2002). Genetic component to susceptibility to Trichuris trichiura: evidence from two Asian populations. Genetic Epidemiology 22, 254–264.CrossRefGoogle ScholarPubMed
Williams-Blangero, S., Subedi, J., Upadhayay, R. P., Manral, D. B., Rai, D. R., Jha, B., Robinson, E. S. and Blangero, J. (1999). Genetic analysis of susceptibility to infection with Ascaris lumbricoides. American Journal of Tropical Medicine and Hygiene 60, 921–926.CrossRefGoogle ScholarPubMed
Xu, L. Q., Yu, S. H., Jiang, Z. X., Yang, J. L., Lai, L. Q., Zhang, X. J. and Zheng, C. Q. (1995). Soil-transmitted helminthiases: nationwide survey in China. Bulletin of the World Health Organization 73, 507–513.Google ScholarPubMed
Xu, X. J., Wei, F. H., Yang, X. X., Dai, Y. H., Yu, G. Y., Chen, L. Y. and Su, Z. M. (2000). Possible effects of the Three Gorges dam on the transmission of Schistosoma japonicum on the Jiang Han plain, China. Annals of Tropical Medicine and Parasitology 94, 333–341.CrossRefGoogle Scholar
Zhou, H., Ross, A. G., Hartel, G. F., Sleigh, A. C., Williams, G. M., McManus, D. P., Luo, X. S., He, Y. and Li, Y. S. (1998). Diagnosis of schistosomiasis japonica in Chinese schoolchildren by administration of a questionnaire. Transactions of the Royal Society of Tropical Medicine and Hygiene 92, 245–250.CrossRefGoogle ScholarPubMed
Zhou, X. N., Guo, J. G., Wu, X. H., Jiang, Q. W., Zheng, J., Dang, H., Wang, X. H., Xu, J., Zhu, H. Q., Wu, G. L., Li, Y. S., Xu, X. J., Chen, H. G., Wang, T. P., Zhu, Y. C., Qiu, D. C., Dong, X. Q., Zhao, G. M., Zhang, S. J., Zhao, N. Q., Xia, G., Wang, L. Y., Zhang, S. Q., Lin, D. D., Chen, M. G. and Hao, Y. (2007). Epidemiology of schistosomiasis in the People's Republic of China, 2004. Emerging Infectious Diseases 13, 1470–1476.CrossRefGoogle ScholarPubMed
Zhou, X. N., Wang, L. Y., Chen, M. G., Wu, X. H., Jiang, Q. W., Chen, X. Y., Zheng, J. and Utzinger, J. (2005). The public health significance and control of schistosomiasis in China – then and now. Acta Tropica 96, 97–105.Google Scholar
Zhu, H. M., Xiang, S., Yang, K., Wu, X. H. and Zhou, X. N. (2008). Three Gorges Dam and its impact on the potential transmission of schistosomiasis in regions along the Yangtze River. Ecohealth 5, 137–148.CrossRefGoogle ScholarPubMed