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Abstract
We show antagonisms and synergisms between Schistosoma haematobium, Ascaris lumbricoides, and Trichuris trichiura in co-infected hosts in southwest Cameroon. The mean intensity of each of the parasites varied according to whether the co-infecting parasite was S. haematobium, A. lumbricoides, or T. trichiura. Using immunological phenomena already described in the literature, we suggest reasons for these interactions between the parasites.
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References
- Anderson RC . Nematode parasites of vertebrates: Their development and transmission, 2nd ed, Willingford, UK, CABI Publishing, 650 pp, 2010.
- Bahia-Oliveira LMG, Azevedo da Silva J, Peixoto-Rangel AL, Boechat MSB, Oliveira AMWA, Massara CL, Peixe RG. Host immune response to Toxoplasma gondii and Ascaris lumbricoides in a highly endemic area: evidence of parasitic co-immunomodulation properties influencing the outcome of both infections. Mem Inst Oswaldo Cruz 104: 273-280, 2009.
- Booth M, Bundy DAP, Albonico M, Chwaya H, Alawi K. Association among multiple infections in schoolchildren in Pemba Island. Parasitology 116 : 85-93, 1998.
- Booth M, Bundy DAP. Estimating the number of multiple species geohelminth infections in human communities. Parasitology 111: 645-653, 1995.
- Bradley JE, Jackson JA. Immunity, immunoregulation and ecology of trichuriasis and ascariasis. Parasite Immunol 26: 429-41, 2004.
- Brooker S, Akhwale W, Pullan R, Estambale B, Clarke SE, Snow RW, Hotez PJ. Epidemiology of Plasmodium-helminth co-infection in Africa: population at risk, potential impact on anemia, and prospects for combining control. Am J Trop Med Hyg 77: 88 – 98, 2007.
- Brooker S, Miguel E, Moulin S, Luoba A, Bundy D, Kremer M. Epidemiology of single and multiple species of helminth infections among school children in Busia District, Kenya. East Afr Med J 77: 157-161, 2000.
- Chow SC, Brown A, Pritchard D. Human infections with Ascaris lumbricoides is associated with suppression of the interleukin-2 response to recombinant cholera toxin B subunit following vaccination with live oral cholera vaccine CVD 103-HgR. Infect Immun 69 : 1574-1580, 2000.
- Cooper PJ, Chico M, Sandoval C, Espinel I, Guevara A, Kennedy MW, Urban JF Jr, Griffin GE, Nutman TB. Human infection with Ascaris lumbricoides is associated with a polarized Th2 cytokine phenotype. J Infect Dis 182: 1207-1213, 2000.
- Corrêa-Oliveira R, Golgher DB, Oliveira GC, Carvalho OS, Massara CL, Caldas IR, Colley DG, Gazzinelli G. Infection with Schistosoma mansoni correlates with altered immune responses to Ascaris lumbricoides and hookworm. Acta Trop 83: 123-132, 2002.
- Curry AJ, Else KJ, Jones F, Bancroft A, Grencis RK, Dunne DW. Evidence that cytokine-mediated immune interactions induced by Schistosoma mansoni alter disease outcome in mice concurrently infected with Trichuris muris. J Exp Med 181 : 769-774, 1995.
- Dzik JM. Molecules released by helminth parasites involved in host colonisation. Acta Biochim Pol 53: 33-64, 2006.
- Duke BO, Moore PJ. The use of molluscide in conjunction with chemotherapy to control Schistosoma haematobium at the Baromi lake foci in Cameroon. Urinary examination methods, the use of nitridazole to attack the parasite in man and the effect on transmission from man to snail. Trop Med Parasitol 27: 489-504, 1976.
- Faulkner H, Turner J, Kamgno J, Pion SD, Boussinsq M, Bradley JE. Age- and infection-intensity-dependent cytokine and antibody production in human trichuriasis: the importance of IgE. J Infect Dis 185: 665-672, 2004.
- Figueiredo CA, Barreto ML, Rodrigues LC, Cooper PJ, Silva NB, Amorim LD, Alcantara-Neves NM. Chronic intestinal helminth infections are associated with immune hyporesponsiveness and induction of a regulatory network. Infect Immun 78: 3160-7, 2010.
- Fleming FM, Brooker S, Geiger SM, Caldas IR, Correa-Oliveira R, Hotez PJ, Bethony JM. Synergistic association between hookworm and other helminth species in a rural community in Brazil. Trop Med Int Health 11: 56-64, 2006.
- Fletcher RH, Fletcher SW. Clinical epidemiology: The Essentials, 4th ed, Lippincott Williams & Wilkins, Philadelphia, Pensylvania, USA, 288pp, 2005.
- Geiger SM, Massara CL, Bethony J, Soboslay PT, Carvalho OS, Correa-Oliveira R. Cellular responses and cytokine profiles in Ascarsi lumbricoides and Trichuris trichiura infected patients. Parasite Immunol 24: 499-509, 2002.
- Glinz D, Silué KD, Knopp S, Lohourignon LK, Yao KP, Steinmann P, Rinaldi L, Cringoli G, N'Goran EK, Utzinger J. Comparing Diagnostic Accuracy of Kato-Katz, Koga Agar Plate, Ether-Concentration, and FLOTAC for Schistosoma mansoni and Soil-Transmitted Helminths. PLoS Negl Trop Dis 4(7): e754. doi:10.1371/journal.pntd.0000754, 2010
- Gnana Mani G, Tat Rao S, Madhavi R. Estimation of hookworm intensity by anthelminthic expulsion in primary school children in South India. Trans R Soc Trop Med Hyg 87 (6): 634-5, 1993.
- Graham AL. When T-helper cells don’t help : immunopathology during concomitant infection. Q Rev Biol 77: 409-434, 2002.
- Hall A, Hoilland C. Geographical variation in Ascaris lumbricoides fecundity and its implications for helminth control. Parasitol Today 16: 540-544, 2000.
- Hsieh GC-F, Loukas A, Wahl AM, Bhatia M, Wang Y, Williamson AL, Kehn KW, Maruyama H, Hotez PJ, Leitenberg D, Bethony J, Constant SL. A Secreted Protein from the Human Hookworm Necator americanus Binds Selectively to NK Cells and Induces IFN- Production. J Immunol 173: 2699-2704, 2004.
- Jackson JA, Turner JD, Rentoul L, Faulkner H, Behnke JM, Hoyle M, Grecis RK, Else KJ, Kamgno J, Boussinesq M, Bradley JE. Th2 responsiveness predicts future susceptibility to gastrointestinal nematodes in humans. J Infect Dis 190:1804–11, 2004a.
- Jackson JA, Turner JD, Rentoul L, Faulkner H, Behnke JM, Hoyle M, Grecis RK, Else KJ, Kamgno J, Bradley JE, Boussinesq M. Cytokine response profiles predict species-specific infection patterns in human GI nematodes. Int J Parasitol 34:1237–1244, 2004b.
- Jackson JA, Friberg IM, Little S, Bradley JE. Review series on helminths, immune modulation and the hygiene hypothesis: immunity against helminths and immunological phenomena in modern human populations: coevolutionary legacies? Immunology 126: 18–27, 2009.
- Keiser J, N'Goran EK, Traoré M, Lohourignon KL, Singer BH, Lengeler C, Tanner M, Utzinger J. Polyparasitism with Schistosoma mansoni, goehelminths, and intestinal protozoa in rural Côte d’Ivoire. J Parasitol 88: 461-466, 2002.
- Loukas A, Prociv P. Immune responses in hookworm infections. Clin Microbiol Rev 14: 689-703, 2001.
- MacDonald AS, Araujo MI, Pearce EJ. Immunology of parasitic helminth infections. Infect Immun 70: 427–433, 2002.
- Mduluza T, Mutapi F, Ruwona T, Kaluka D, Midzi N Ndhlova PD. Similar cellular responses after treatment with either praziquantel or oxamniquine in Schistosoma mansoni infection. Malawi Med J 21: 176-181, 2009.
- Moyou SR, Tagni ZD, Kouamou J, Enyong P, Ripert C. Epidemiologic and radiologic study of urinary bilharziasis in the focus of Barombi lake (Meme Department), Cameroon. Bull Soc Pathol Exot 80: 813-825, 1987.
- Mwatha JK, Kimani G, Kamau T, Mbugua GG, Ouma JH, Mumo J, Fulford AJC, Jones FM, Butterworth AE, Roberts MB, Dunne DW. 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. J Immunol 160:1992-1999, 2009.
- Naish S, McCarthy J, Williams GM. Prevalene, intensity, and risk factors for helminth infection in a South Indian fishing village. Acta Tropica 91 (2): 177-87, 2004.
- Ndamukong KL, Ayuk MA, Dinga AS, Akenji TN, Ndiforchu VA, Titanji VP. Prevalence and intensity of urinary schistosomiasis in primary school children at the Kott-Barombi health area, Cameroon. East Afr Med J 78: 287-289, 2001.
- Ndamukong KJ, Ayuk MA, Dinga AS, Akenji TN, Ndiforchu VA Titanji VP. Infection patterns of Schistosoma haematobium in primary school children of the Kumba Health District, South-West Cameroon. Afr J Health Sci 7: 98-102, 2000.
- Needham C, Kim HT, Hoa NV, Cong LD, Michael E, Drake L, Hall A, Bundy DA. Epidemiology of soil transmitted nematode infections in Ha Nam Province, Vietnam. Trop Med Int Health 3: 904-912, 1998.
- Nkengazong L, Njiokou F, Wanji S, Teukeng F, Enyong P, Asoganyi T. Prevalence of soil transmitted helminthes and impact of Albendazole on parasitic indices in Kotto Barombi and Marumba II villages (South-West Cameroon). Afr J Env Sci Technol 4: 115-121, 2010.
- Nkengazong L, Njiokou F, Teukeng F, Enyong P, Wanji S. Reassessment of endemicity level of urinary Schistomiasis in Kott-Barombi focus (South-West Cameroon) and impact of mass drug administration (MDA) on parasitic indices. J Cell Anim Biol 3: 159-164, 2009.
- Quihui-Cota L, Valencia ME, Crompton DW, Philips S, Hagan P, Diaz-Camacho SP, Triana Tejas A. Prevalence and intensity of intestinal parasitic infections in relation to nutritional starus in Mexican school children. Trans R Soc Trop Med Hyg 98(11): 853-9, 2004.
- Quinnell RJ. Genetics of susceptibility to human helminth infection. International Journal for Parasitology 33: 1219–1231, 2003.
- Rupert J. Quinnell RJ. Genetics of susceptibility to human helminth infection. International Journal for Parasitology 33: 1219–1231, 2003.
- Raso G, Luginbühl A, Adjoua CA, Tian-Bi NT, Silué KD, Matthys B, Vounatsou, P, Wang Y, Dumas M-E, Holmes E, Singer BH, Tanner M, N’Goran EK, Utzinger J. Multiple parasite infections and their relationship with self-reported morbidity in a community in rural Côte d’Ivoire. Int J Epidemiol 33: 1092-1102, 2004.
- Ratard CR, Kouemeni LE, Bessala MME, Ndankou CN, Greer GJ, Spilsburg J, Cline BC. Human schistosomiasis in Cameroon.1. Distribution of schistosomiasis. Am J Trop Med Hyg 42: 561-572, 1990.
- Shakespeare TP, Gebski VJ, Veness MJ, Sime J. Improving interpretation of clinical studies by use of confidence levels, clinical significance curves, and risk-benefit contours. Lancet 357: 1349-1353, 2001.
- Tchuem Tchuente LA, Behnke JM, Gilbert FS, Southgate VR, Vercruysse J. Polyparasitism with Schistosoma haematobium and soil-transmitted helminth infections among school children in Loum, Cameroon. Trop Med Int Health 8: 1-12, 2003.
- Turner JD, Faulkner H, Kamgno J, Cormont F, Van Snick J, Else KJ, Grencis RK, Behnke JM, Boussinesq M, Bradley JE. Th2 cytokines are associated with reduced worm burdens in a human interstinal helminth infection. J Infect Dis 188: 1768-1775, 2003.
- Woolhouse ME, Taylor P, Matanhire D, Chandiwana SK. Acquired immunity and epidemiology of Schistosoma haematobium. Nature 351: 757-759, 1991.
- Wynn TA. IL-13 effector function. Annu Rev Immunol 12: 425-456, 2003.
- Yoshida, A., Maruyama, H., Yabu, Y., Amano, T., Kobayakawa, T. Ohta, N. Immune responses against protozoal and nematodal infection in mice with underlying Schistosoma mansoni infection. Parasitol International 48:73-79, 1999.
References
Anderson RC . Nematode parasites of vertebrates: Their development and transmission, 2nd ed, Willingford, UK, CABI Publishing, 650 pp, 2010.
Bahia-Oliveira LMG, Azevedo da Silva J, Peixoto-Rangel AL, Boechat MSB, Oliveira AMWA, Massara CL, Peixe RG. Host immune response to Toxoplasma gondii and Ascaris lumbricoides in a highly endemic area: evidence of parasitic co-immunomodulation properties influencing the outcome of both infections. Mem Inst Oswaldo Cruz 104: 273-280, 2009.
Booth M, Bundy DAP, Albonico M, Chwaya H, Alawi K. Association among multiple infections in schoolchildren in Pemba Island. Parasitology 116 : 85-93, 1998.
Booth M, Bundy DAP. Estimating the number of multiple species geohelminth infections in human communities. Parasitology 111: 645-653, 1995.
Bradley JE, Jackson JA. Immunity, immunoregulation and ecology of trichuriasis and ascariasis. Parasite Immunol 26: 429-41, 2004.
Brooker S, Akhwale W, Pullan R, Estambale B, Clarke SE, Snow RW, Hotez PJ. Epidemiology of Plasmodium-helminth co-infection in Africa: population at risk, potential impact on anemia, and prospects for combining control. Am J Trop Med Hyg 77: 88 – 98, 2007.
Brooker S, Miguel E, Moulin S, Luoba A, Bundy D, Kremer M. Epidemiology of single and multiple species of helminth infections among school children in Busia District, Kenya. East Afr Med J 77: 157-161, 2000.
Chow SC, Brown A, Pritchard D. Human infections with Ascaris lumbricoides is associated with suppression of the interleukin-2 response to recombinant cholera toxin B subunit following vaccination with live oral cholera vaccine CVD 103-HgR. Infect Immun 69 : 1574-1580, 2000.
Cooper PJ, Chico M, Sandoval C, Espinel I, Guevara A, Kennedy MW, Urban JF Jr, Griffin GE, Nutman TB. Human infection with Ascaris lumbricoides is associated with a polarized Th2 cytokine phenotype. J Infect Dis 182: 1207-1213, 2000.
Corrêa-Oliveira R, Golgher DB, Oliveira GC, Carvalho OS, Massara CL, Caldas IR, Colley DG, Gazzinelli G. Infection with Schistosoma mansoni correlates with altered immune responses to Ascaris lumbricoides and hookworm. Acta Trop 83: 123-132, 2002.
Curry AJ, Else KJ, Jones F, Bancroft A, Grencis RK, Dunne DW. Evidence that cytokine-mediated immune interactions induced by Schistosoma mansoni alter disease outcome in mice concurrently infected with Trichuris muris. J Exp Med 181 : 769-774, 1995.
Dzik JM. Molecules released by helminth parasites involved in host colonisation. Acta Biochim Pol 53: 33-64, 2006.
Duke BO, Moore PJ. The use of molluscide in conjunction with chemotherapy to control Schistosoma haematobium at the Baromi lake foci in Cameroon. Urinary examination methods, the use of nitridazole to attack the parasite in man and the effect on transmission from man to snail. Trop Med Parasitol 27: 489-504, 1976.
Faulkner H, Turner J, Kamgno J, Pion SD, Boussinsq M, Bradley JE. Age- and infection-intensity-dependent cytokine and antibody production in human trichuriasis: the importance of IgE. J Infect Dis 185: 665-672, 2004.
Figueiredo CA, Barreto ML, Rodrigues LC, Cooper PJ, Silva NB, Amorim LD, Alcantara-Neves NM. Chronic intestinal helminth infections are associated with immune hyporesponsiveness and induction of a regulatory network. Infect Immun 78: 3160-7, 2010.
Fleming FM, Brooker S, Geiger SM, Caldas IR, Correa-Oliveira R, Hotez PJ, Bethony JM. Synergistic association between hookworm and other helminth species in a rural community in Brazil. Trop Med Int Health 11: 56-64, 2006.
Fletcher RH, Fletcher SW. Clinical epidemiology: The Essentials, 4th ed, Lippincott Williams & Wilkins, Philadelphia, Pensylvania, USA, 288pp, 2005.
Geiger SM, Massara CL, Bethony J, Soboslay PT, Carvalho OS, Correa-Oliveira R. Cellular responses and cytokine profiles in Ascarsi lumbricoides and Trichuris trichiura infected patients. Parasite Immunol 24: 499-509, 2002.
Glinz D, Silué KD, Knopp S, Lohourignon LK, Yao KP, Steinmann P, Rinaldi L, Cringoli G, N'Goran EK, Utzinger J. Comparing Diagnostic Accuracy of Kato-Katz, Koga Agar Plate, Ether-Concentration, and FLOTAC for Schistosoma mansoni and Soil-Transmitted Helminths. PLoS Negl Trop Dis 4(7): e754. doi:10.1371/journal.pntd.0000754, 2010
Gnana Mani G, Tat Rao S, Madhavi R. Estimation of hookworm intensity by anthelminthic expulsion in primary school children in South India. Trans R Soc Trop Med Hyg 87 (6): 634-5, 1993.
Graham AL. When T-helper cells don’t help : immunopathology during concomitant infection. Q Rev Biol 77: 409-434, 2002.
Hall A, Hoilland C. Geographical variation in Ascaris lumbricoides fecundity and its implications for helminth control. Parasitol Today 16: 540-544, 2000.
Hsieh GC-F, Loukas A, Wahl AM, Bhatia M, Wang Y, Williamson AL, Kehn KW, Maruyama H, Hotez PJ, Leitenberg D, Bethony J, Constant SL. A Secreted Protein from the Human Hookworm Necator americanus Binds Selectively to NK Cells and Induces IFN- Production. J Immunol 173: 2699-2704, 2004.
Jackson JA, Turner JD, Rentoul L, Faulkner H, Behnke JM, Hoyle M, Grecis RK, Else KJ, Kamgno J, Boussinesq M, Bradley JE. Th2 responsiveness predicts future susceptibility to gastrointestinal nematodes in humans. J Infect Dis 190:1804–11, 2004a.
Jackson JA, Turner JD, Rentoul L, Faulkner H, Behnke JM, Hoyle M, Grecis RK, Else KJ, Kamgno J, Bradley JE, Boussinesq M. Cytokine response profiles predict species-specific infection patterns in human GI nematodes. Int J Parasitol 34:1237–1244, 2004b.
Jackson JA, Friberg IM, Little S, Bradley JE. Review series on helminths, immune modulation and the hygiene hypothesis: immunity against helminths and immunological phenomena in modern human populations: coevolutionary legacies? Immunology 126: 18–27, 2009.
Keiser J, N'Goran EK, Traoré M, Lohourignon KL, Singer BH, Lengeler C, Tanner M, Utzinger J. Polyparasitism with Schistosoma mansoni, goehelminths, and intestinal protozoa in rural Côte d’Ivoire. J Parasitol 88: 461-466, 2002.
Loukas A, Prociv P. Immune responses in hookworm infections. Clin Microbiol Rev 14: 689-703, 2001.
MacDonald AS, Araujo MI, Pearce EJ. Immunology of parasitic helminth infections. Infect Immun 70: 427–433, 2002.
Mduluza T, Mutapi F, Ruwona T, Kaluka D, Midzi N Ndhlova PD. Similar cellular responses after treatment with either praziquantel or oxamniquine in Schistosoma mansoni infection. Malawi Med J 21: 176-181, 2009.
Moyou SR, Tagni ZD, Kouamou J, Enyong P, Ripert C. Epidemiologic and radiologic study of urinary bilharziasis in the focus of Barombi lake (Meme Department), Cameroon. Bull Soc Pathol Exot 80: 813-825, 1987.
Mwatha JK, Kimani G, Kamau T, Mbugua GG, Ouma JH, Mumo J, Fulford AJC, Jones FM, Butterworth AE, Roberts MB, Dunne DW. 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. J Immunol 160:1992-1999, 2009.
Naish S, McCarthy J, Williams GM. Prevalene, intensity, and risk factors for helminth infection in a South Indian fishing village. Acta Tropica 91 (2): 177-87, 2004.
Ndamukong KL, Ayuk MA, Dinga AS, Akenji TN, Ndiforchu VA, Titanji VP. Prevalence and intensity of urinary schistosomiasis in primary school children at the Kott-Barombi health area, Cameroon. East Afr Med J 78: 287-289, 2001.
Ndamukong KJ, Ayuk MA, Dinga AS, Akenji TN, Ndiforchu VA Titanji VP. Infection patterns of Schistosoma haematobium in primary school children of the Kumba Health District, South-West Cameroon. Afr J Health Sci 7: 98-102, 2000.
Needham C, Kim HT, Hoa NV, Cong LD, Michael E, Drake L, Hall A, Bundy DA. Epidemiology of soil transmitted nematode infections in Ha Nam Province, Vietnam. Trop Med Int Health 3: 904-912, 1998.
Nkengazong L, Njiokou F, Wanji S, Teukeng F, Enyong P, Asoganyi T. Prevalence of soil transmitted helminthes and impact of Albendazole on parasitic indices in Kotto Barombi and Marumba II villages (South-West Cameroon). Afr J Env Sci Technol 4: 115-121, 2010.
Nkengazong L, Njiokou F, Teukeng F, Enyong P, Wanji S. Reassessment of endemicity level of urinary Schistomiasis in Kott-Barombi focus (South-West Cameroon) and impact of mass drug administration (MDA) on parasitic indices. J Cell Anim Biol 3: 159-164, 2009.
Quihui-Cota L, Valencia ME, Crompton DW, Philips S, Hagan P, Diaz-Camacho SP, Triana Tejas A. Prevalence and intensity of intestinal parasitic infections in relation to nutritional starus in Mexican school children. Trans R Soc Trop Med Hyg 98(11): 853-9, 2004.
Quinnell RJ. Genetics of susceptibility to human helminth infection. International Journal for Parasitology 33: 1219–1231, 2003.
Rupert J. Quinnell RJ. Genetics of susceptibility to human helminth infection. International Journal for Parasitology 33: 1219–1231, 2003.
Raso G, Luginbühl A, Adjoua CA, Tian-Bi NT, Silué KD, Matthys B, Vounatsou, P, Wang Y, Dumas M-E, Holmes E, Singer BH, Tanner M, N’Goran EK, Utzinger J. Multiple parasite infections and their relationship with self-reported morbidity in a community in rural Côte d’Ivoire. Int J Epidemiol 33: 1092-1102, 2004.
Ratard CR, Kouemeni LE, Bessala MME, Ndankou CN, Greer GJ, Spilsburg J, Cline BC. Human schistosomiasis in Cameroon.1. Distribution of schistosomiasis. Am J Trop Med Hyg 42: 561-572, 1990.
Shakespeare TP, Gebski VJ, Veness MJ, Sime J. Improving interpretation of clinical studies by use of confidence levels, clinical significance curves, and risk-benefit contours. Lancet 357: 1349-1353, 2001.
Tchuem Tchuente LA, Behnke JM, Gilbert FS, Southgate VR, Vercruysse J. Polyparasitism with Schistosoma haematobium and soil-transmitted helminth infections among school children in Loum, Cameroon. Trop Med Int Health 8: 1-12, 2003.
Turner JD, Faulkner H, Kamgno J, Cormont F, Van Snick J, Else KJ, Grencis RK, Behnke JM, Boussinesq M, Bradley JE. Th2 cytokines are associated with reduced worm burdens in a human interstinal helminth infection. J Infect Dis 188: 1768-1775, 2003.
Woolhouse ME, Taylor P, Matanhire D, Chandiwana SK. Acquired immunity and epidemiology of Schistosoma haematobium. Nature 351: 757-759, 1991.
Wynn TA. IL-13 effector function. Annu Rev Immunol 12: 425-456, 2003.
Yoshida, A., Maruyama, H., Yabu, Y., Amano, T., Kobayakawa, T. Ohta, N. Immune responses against protozoal and nematodal infection in mice with underlying Schistosoma mansoni infection. Parasitol International 48:73-79, 1999.