Colley DG, Bustinduy AL, Secor WE, King CH, 2014. Human schistosomiasis. Lancet 383: 2253–2264.
Stothard JR, Sousa-Figueiredo JC, Betson M, Bustinduy A, Reinhard-Rupp J, 2013. Schistosomiasis in African infants and preschool children: let them now be treated! Trends Parasitol 29: 197–205.
van Riet E, Hartgers FC, Yazdanbakhsh M, 2007. Chronic helminth infections induce immunomodulation: consequences and mechanisms. Immunobiology 212: 475–490.
Friedman JF, Kanzaria HK, McGarvey ST, 2005. Human schistosomiasis and anemia: the relationship and potential mechanisms. Trends Parasitol 21: 386–392.
Coutinho HM, Leenstra T, Acosta LP, Su L, Jarilla B, Jiz MA, Langdon GC, Olveda RM, McGarvey ST, Kurtis JD, Friedman JF, 2006. Pro-inflammatory cytokines and C-reactive protein are associated with undernutrition in the context of Schistosoma japonicum infection. Am J Trop Med Hyg 75: 720–726.
Coutinho HM, McGarvey ST, Acosta LP, Manalo DL, Langdon GC, Leenstra T, Kanzaria HK, Solomon J, Wu H, Olveda RM, Kurtis JD, Friedman JF, 2005. Nutritional status and serum cytokine profiles in children, adolescents, and young adults with Schistosoma japonicum-associated hepatic fibrosis, in Leyte, Philippines. J Infect Dis 192: 528–536.
Alves Oliveira LF, Moreno EC, Gazzinelli G, Martins-Filho OA, Silveira AM, Gazzinelli A, Malaquias LC, LoVerde P, Leite PM, Correa-Oliveira R, 2006. Cytokine production associated with periportal fibrosis during chronic schistosomiasis mansoni in humans. Infect Immun 74: 1215–1221.
Mutapi F, Winborn G, Midzi N, Taylor M, Mduluza T, Maizels RM, 2007. Cytokine responses to Schistosoma haematobium in a Zimbabwean population: contrasting profiles for IFN-gamma, IL-4, IL-5 and IL-10 with age. BMC Infect Dis 7: 139.
Bustinduy AL, Parraga IM, Thomas CL, Mungai PL, Mutuku F, Muchiri EM, Kitron U, King CH, 2013. Impact of polyparasitic infections on anemia and undernutrition among Kenyan children living in a Schistosoma haematobium-endemic area. Am J Trop Med Hyg 88: 433–440.
Peters PA, Mahmoud AA, Warren KS, Ouma JH, Siongok TK, 1976. Field studies of a rapid, accurate means of quantifying Schistosoma haematobium eggs in urine samples. Bull World Health Organ 54: 159–162.
Katz N, Chaves A, Pellegrino J, 1972. A simple device for quantitative stool thick-smear technique in schistosomiasis mansoni. Rev Inst Med Trop Sao Paulo 14: 397–400.
World Health Organization, 2008. Worldwide Prevalence of Anaemia 1993–2005. WHO Database on Anaemia. Benoist B, McLean E, Egli I, Cogswell M ed. Geneva, Switzerland: World Health Organization.
De Onis M, World Health Organization, Department of Nutrition for Health and Development, 2009. WHO Child Growth Standards: Growth Velocity Based on Weight, Length and Head Circumference: Methods and Development. Geneva, Switzerland: World Health Organization.
Maddison SE, Slemenda SB, Tsang VC, Pollard RA, 1985. Serodiagnosis of Schistosoma mansoni with microsomal adult worm antigen in an enzyme-linked immunosorbent assay using a standard curve developed with a reference serum pool. Am J Trop Med Hyg 34: 484–494.
Hoffmann KF, Wynn TA, Dunne DW, 2002. Cytokine-mediated host responses during schistosome infections: walking the fine line between immunological control and immunopathology. Adv Parasitol 52: 265–307.
Mutuku FM, King CH, Bustinduy AL, Mungai PL, Muchiri EM, Kitron U, 2011. Impact of drought on the spatial pattern of transmission of Schistosoma haematobium in coastal Kenya. Am J Trop Med Hyg 85: 1065–1070.
Clennon JA, Mungai PL, Muchiri EM, King CH, Kitron U, 2006. Spatial and temporal variations in local transmission of Schistosoma haematobium in Msambweni, Kenya. Am J Trop Med Hyg 75: 1034–1041.
King CL, Malhotra I, Mungai P, Wamachi A, Kioko J, Muchiri E, Ouma JH, 2001. Schistosoma haematobium-induced urinary tract morbidity correlates with increased tumor necrosis factor-alpha and diminished interleukin-10 production. J Infect Dis 184: 1176–1182.
Booth M, Mwatha JK, Joseph S, Jones FM, Kadzo H, Ireri E, Kazibwe F, Kemijumbi J, Kariuki C, Kimani G, Ouma JH, Kabatereine NB, Vennervald BJ, Dunne DW, 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. J Immunol 172: 1295–1303.
Coutinho HM, Acosta LP, Wu HW, McGarvey ST, Su L, Langdon GC, Jiz MA, Jarilla B, Olveda RM, Friedman JF, Kurtis JD, 2007. Th2 cytokines are associated with persistent hepatic fibrosis in human Schistosoma japonicum infection. J Infect Dis 195: 288–295.
Lyke KE, Dicko A, Dabo A, Sangare L, Kone A, Coulibaly D, Guindo A, Traore K, Daou M, Diarra I, Sztein MB, Plowe CV, Doumbo OK, 2005. Association of Schistosoma haematobium infection with protection against acute Plasmodium falciparum malaria in Malian children. Am J Trop Med Hyg 73: 1124–1130.
Lyke KE, Dabo A, Sangare L, Arama C, Daou M, Diarra I, Plowe CV, Doumbo OK, Sztein MB, 2006. Effects of concomitant Schistosoma haematobium infection on the serum cytokine levels elicited by acute Plasmodium falciparum malaria infection in Malian children. Infect Immun 74: 5718–5724.
Diallo TO, Remoue F, Schacht AM, Charrier N, Dompnier JP, Pillet S, Garraud O, N'Diaye AA, Capron A, Capron M, Riveau G, 2004. Schistosomiasis co-infection in humans influences inflammatory markers in uncomplicated Plasmodium falciparum malaria. Parasite Immunol 26: 365–369.
Montenegro SM, Miranda P, Mahanty S, Abath FG, Teixeira KM, Coutinho EM, Brinkman J, Goncalves I, Domingues LA, Domingues AL, Sher A, Wynn TA, 1999. Cytokine production in acute versus chronic human schistosomiasis mansoni: the cross-regulatory role of interferon-gamma and interleukin-10 in the responses of peripheral blood mononuclear cells and splenocytes to parasite antigens. J Infect Dis 179: 1502–1514.
Henri S, Chevillard C, Mergani A, Paris P, Gaudart J, Camilla C, Dessein H, Montero F, Elwali NE, Saeed OK, Magzoub M, Dessein AJ, 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. J Immunol 169: 929–936.
Supali T, Verweij JJ, Wiria AE, Djuardi Y, Hamid F, Kaisar MM, Wammes LJ, van Lieshout L, Luty AJ, Sartono E, Yazdanbakhsh M, 2010. Polyparasitism and its impact on the immune system. Int J Parasitol 40: 1171–1176.
Arnaud V, Li J, Wang Y, Fu X, Mengzhi S, Luo X, Hou X, Dessein H, Jie Z, Xin-Ling Y, He H, McManus DP, Li Y, Dessein A, 2008. Regulatory role of interleukin-10 and interferon-gamma in severe hepatic central and peripheral fibrosis in humans infected with Schistosoma japonicum. J Infect Dis 198: 418–426.
Kabatereine NB, Vennervald BJ, Ouma JH, Kemijumbi J, Butterworth AE, Dunne DW, Fulford AJ, 1999. Adult resistance to schistosomiasis mansoni: age-dependence of reinfection remains constant in communities with diverse exposure patterns. Parasitology 118: 101–105.
Kurtis JD, Friedman JF, Leenstra T, Langdon GC, Wu HW, Manalo DL, Su L, Jiz M, Jarilla B, Pablo AO, McGarvey ST, Olveda RM, Acosta LP, 2006. Pubertal development predicts resistance to infection and reinfection with Schistosoma japonicum. Clin Infect Dis 42: 1692–1698.
Andrade ZA, Baptista AP, Santana TS, 2006. Remodeling of hepatic vascular changes after specific chemotherapy of schistosomal periportal fibrosis. Mem Inst Oswaldo Cruz 101 (Suppl 1): 267–272.
Coutinho EM, Barros AF, Barbosa A Jr, Oliveira SA, Silva LM, Araujo RE, Andrade ZA, 2003. Host nutritional status as a contributory factor to the remodeling of schistosomal hepatic fibrosis. Mem Inst Oswaldo Cruz 98: 919–925.
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In a study of children having polyparasitic infections in a Schistosoma haematobium–endemic area, we examined the hypothesis that S. haematobium–positive children, compared with S. haematobium–negative children (anti-soluble worm antigen preparation [SWAP] negative and egg negative) have increased systemic production of pro-inflammatory cytokines (interleukin [IL]-6, tumor necrosis factor [TNF]-α) and decreased down-regulatory IL-10. A total of 804 children, 2–19 years of age, were surveyed between July and December 2009 and tested for S. haematobium, Plasmodium falciparum, filariasis, and soil-transmitted helminth infections. Plasma levels of IL-6, TNF-α, and IL-10 were compared for S. haematobium–positive and S. haematobium–negative children, adjusting for malaria, filaria, and hookworm co-infections, and for nutritional status, age group, sex, and geographic location. IL-10 was significantly elevated among children infected with S. haematobium, showing bimodal peaks in 7–8 and 13–14 years age groups. IL-10 was also higher among children who were acutely malnourished, whereas IL-10 levels were lower in the presence of S. haematobium–filaria co-infection. After adjustment for co-factors, IL-6 was significantly elevated among children of 5–6 years and among those with P. falciparum infection. Lower levels of IL-6 were found in malaria–hookworm co-infection. High levels of TNF-α were found in children aged 11–12 years regardless of infection status. In addition, village of residence was a strong predictor of IL-6 and IL-10 plasma levels. In adolescent children infected with S. haematobium, there is an associated elevation in circulating IL-10 that may reduce the risk of later morbidity. Although we did not find a direct link between S. haematobium infection and circulating pro-inflammatory IL-6 and TNF-α levels, future T-cell stimulation studies may provide more conclusive linkages between infection and cytokine responses in settings that are endemic for multiple parasites and multiple co-infections.
Financial support: This study was supported by the U.S. National Institutes of Health through a T32 Ruth L. Kirschstein-National Service Research Award-Training Grant and R01–TW008067 from the Fogarty International Center.
Authors' addresses: Amaya L. Bustinduy, Center for Global Health and Diseases, Case Western Reserve University School of Medicine, Cleveland, OH, and the Institute of Immunity and Infection, St. George's University of London, London, UK, E-mails: bustinji06@gmail.com or Amaya.Bustinduy@doctors.org.uk. Laura J. Sutherland, Alicia Chang-Cojulun, Indu Malhotra, Adam S. DuVall, and Charles H. King, Center for Global Health and Diseases, Case Western Reserve University, Cleveland, OH, E-mails: chikungunya.ljs@gmail.com, aliciachc18@gmail.com, ijm@case.edu, adam.s.duvall@gmail.com, and chk@case.edu. Jessica K. Fairley and Uriel Kitron, Department of Environmental Studies, Emory University, Atlanta, GA, E-mails: jfairleymd@gmail.com and ukitron@emory.edu. Peter L. Mungai, CWRU/DVBNTD, c/o CWRU/DVBNTD Filariasis-Schistosomiasis Research Unit, Msambweni, Coast, Kenya, E-mail: plmungai@yahoo.com. Eric M. Muchiri, Division of Vector Borne and Neglected Diseases, Ministry of Public Health and Sanitation, Nairobi, Kenya, E-mail: ericmmuchiri@gmail.com. Francis M. Mutuku, Department of Environmental Studies, Emory University, Atlanta, GA, and CWRU/DVBNTD, Diani, Kenya, E-mail: fmutuku73@gmail.com.
Colley DG, Bustinduy AL, Secor WE, King CH, 2014. Human schistosomiasis. Lancet 383: 2253–2264.
Stothard JR, Sousa-Figueiredo JC, Betson M, Bustinduy A, Reinhard-Rupp J, 2013. Schistosomiasis in African infants and preschool children: let them now be treated! Trends Parasitol 29: 197–205.
van Riet E, Hartgers FC, Yazdanbakhsh M, 2007. Chronic helminth infections induce immunomodulation: consequences and mechanisms. Immunobiology 212: 475–490.
Friedman JF, Kanzaria HK, McGarvey ST, 2005. Human schistosomiasis and anemia: the relationship and potential mechanisms. Trends Parasitol 21: 386–392.
Coutinho HM, Leenstra T, Acosta LP, Su L, Jarilla B, Jiz MA, Langdon GC, Olveda RM, McGarvey ST, Kurtis JD, Friedman JF, 2006. Pro-inflammatory cytokines and C-reactive protein are associated with undernutrition in the context of Schistosoma japonicum infection. Am J Trop Med Hyg 75: 720–726.
Coutinho HM, McGarvey ST, Acosta LP, Manalo DL, Langdon GC, Leenstra T, Kanzaria HK, Solomon J, Wu H, Olveda RM, Kurtis JD, Friedman JF, 2005. Nutritional status and serum cytokine profiles in children, adolescents, and young adults with Schistosoma japonicum-associated hepatic fibrosis, in Leyte, Philippines. J Infect Dis 192: 528–536.
Alves Oliveira LF, Moreno EC, Gazzinelli G, Martins-Filho OA, Silveira AM, Gazzinelli A, Malaquias LC, LoVerde P, Leite PM, Correa-Oliveira R, 2006. Cytokine production associated with periportal fibrosis during chronic schistosomiasis mansoni in humans. Infect Immun 74: 1215–1221.
Mutapi F, Winborn G, Midzi N, Taylor M, Mduluza T, Maizels RM, 2007. Cytokine responses to Schistosoma haematobium in a Zimbabwean population: contrasting profiles for IFN-gamma, IL-4, IL-5 and IL-10 with age. BMC Infect Dis 7: 139.
Bustinduy AL, Parraga IM, Thomas CL, Mungai PL, Mutuku F, Muchiri EM, Kitron U, King CH, 2013. Impact of polyparasitic infections on anemia and undernutrition among Kenyan children living in a Schistosoma haematobium-endemic area. Am J Trop Med Hyg 88: 433–440.
Peters PA, Mahmoud AA, Warren KS, Ouma JH, Siongok TK, 1976. Field studies of a rapid, accurate means of quantifying Schistosoma haematobium eggs in urine samples. Bull World Health Organ 54: 159–162.
Katz N, Chaves A, Pellegrino J, 1972. A simple device for quantitative stool thick-smear technique in schistosomiasis mansoni. Rev Inst Med Trop Sao Paulo 14: 397–400.
World Health Organization, 2008. Worldwide Prevalence of Anaemia 1993–2005. WHO Database on Anaemia. Benoist B, McLean E, Egli I, Cogswell M ed. Geneva, Switzerland: World Health Organization.
De Onis M, World Health Organization, Department of Nutrition for Health and Development, 2009. WHO Child Growth Standards: Growth Velocity Based on Weight, Length and Head Circumference: Methods and Development. Geneva, Switzerland: World Health Organization.
Maddison SE, Slemenda SB, Tsang VC, Pollard RA, 1985. Serodiagnosis of Schistosoma mansoni with microsomal adult worm antigen in an enzyme-linked immunosorbent assay using a standard curve developed with a reference serum pool. Am J Trop Med Hyg 34: 484–494.
Hoffmann KF, Wynn TA, Dunne DW, 2002. Cytokine-mediated host responses during schistosome infections: walking the fine line between immunological control and immunopathology. Adv Parasitol 52: 265–307.
Mutuku FM, King CH, Bustinduy AL, Mungai PL, Muchiri EM, Kitron U, 2011. Impact of drought on the spatial pattern of transmission of Schistosoma haematobium in coastal Kenya. Am J Trop Med Hyg 85: 1065–1070.
Clennon JA, Mungai PL, Muchiri EM, King CH, Kitron U, 2006. Spatial and temporal variations in local transmission of Schistosoma haematobium in Msambweni, Kenya. Am J Trop Med Hyg 75: 1034–1041.
King CL, Malhotra I, Mungai P, Wamachi A, Kioko J, Muchiri E, Ouma JH, 2001. Schistosoma haematobium-induced urinary tract morbidity correlates with increased tumor necrosis factor-alpha and diminished interleukin-10 production. J Infect Dis 184: 1176–1182.
Booth M, Mwatha JK, Joseph S, Jones FM, Kadzo H, Ireri E, Kazibwe F, Kemijumbi J, Kariuki C, Kimani G, Ouma JH, Kabatereine NB, Vennervald BJ, Dunne DW, 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. J Immunol 172: 1295–1303.
Coutinho HM, Acosta LP, Wu HW, McGarvey ST, Su L, Langdon GC, Jiz MA, Jarilla B, Olveda RM, Friedman JF, Kurtis JD, 2007. Th2 cytokines are associated with persistent hepatic fibrosis in human Schistosoma japonicum infection. J Infect Dis 195: 288–295.
Lyke KE, Dicko A, Dabo A, Sangare L, Kone A, Coulibaly D, Guindo A, Traore K, Daou M, Diarra I, Sztein MB, Plowe CV, Doumbo OK, 2005. Association of Schistosoma haematobium infection with protection against acute Plasmodium falciparum malaria in Malian children. Am J Trop Med Hyg 73: 1124–1130.
Lyke KE, Dabo A, Sangare L, Arama C, Daou M, Diarra I, Plowe CV, Doumbo OK, Sztein MB, 2006. Effects of concomitant Schistosoma haematobium infection on the serum cytokine levels elicited by acute Plasmodium falciparum malaria infection in Malian children. Infect Immun 74: 5718–5724.
Diallo TO, Remoue F, Schacht AM, Charrier N, Dompnier JP, Pillet S, Garraud O, N'Diaye AA, Capron A, Capron M, Riveau G, 2004. Schistosomiasis co-infection in humans influences inflammatory markers in uncomplicated Plasmodium falciparum malaria. Parasite Immunol 26: 365–369.
Montenegro SM, Miranda P, Mahanty S, Abath FG, Teixeira KM, Coutinho EM, Brinkman J, Goncalves I, Domingues LA, Domingues AL, Sher A, Wynn TA, 1999. Cytokine production in acute versus chronic human schistosomiasis mansoni: the cross-regulatory role of interferon-gamma and interleukin-10 in the responses of peripheral blood mononuclear cells and splenocytes to parasite antigens. J Infect Dis 179: 1502–1514.
Henri S, Chevillard C, Mergani A, Paris P, Gaudart J, Camilla C, Dessein H, Montero F, Elwali NE, Saeed OK, Magzoub M, Dessein AJ, 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. J Immunol 169: 929–936.
Supali T, Verweij JJ, Wiria AE, Djuardi Y, Hamid F, Kaisar MM, Wammes LJ, van Lieshout L, Luty AJ, Sartono E, Yazdanbakhsh M, 2010. Polyparasitism and its impact on the immune system. Int J Parasitol 40: 1171–1176.
Arnaud V, Li J, Wang Y, Fu X, Mengzhi S, Luo X, Hou X, Dessein H, Jie Z, Xin-Ling Y, He H, McManus DP, Li Y, Dessein A, 2008. Regulatory role of interleukin-10 and interferon-gamma in severe hepatic central and peripheral fibrosis in humans infected with Schistosoma japonicum. J Infect Dis 198: 418–426.
Kabatereine NB, Vennervald BJ, Ouma JH, Kemijumbi J, Butterworth AE, Dunne DW, Fulford AJ, 1999. Adult resistance to schistosomiasis mansoni: age-dependence of reinfection remains constant in communities with diverse exposure patterns. Parasitology 118: 101–105.
Kurtis JD, Friedman JF, Leenstra T, Langdon GC, Wu HW, Manalo DL, Su L, Jiz M, Jarilla B, Pablo AO, McGarvey ST, Olveda RM, Acosta LP, 2006. Pubertal development predicts resistance to infection and reinfection with Schistosoma japonicum. Clin Infect Dis 42: 1692–1698.
Andrade ZA, Baptista AP, Santana TS, 2006. Remodeling of hepatic vascular changes after specific chemotherapy of schistosomal periportal fibrosis. Mem Inst Oswaldo Cruz 101 (Suppl 1): 267–272.
Coutinho EM, Barros AF, Barbosa A Jr, Oliveira SA, Silva LM, Araujo RE, Andrade ZA, 2003. Host nutritional status as a contributory factor to the remodeling of schistosomal hepatic fibrosis. Mem Inst Oswaldo Cruz 98: 919–925.
Past two years | Past Year | Past 30 Days | |
---|---|---|---|
Abstract Views | 519 | 435 | 11 |
Full Text Views | 484 | 9 | 0 |
PDF Downloads | 236 | 11 | 0 |