WHO/TDR, 2002. Strategic Direction for Research: Schistosomiasis. Geneva: World Health Organization.
de Jesus AR, Silva A, Santana LB, Magalhaes A, de Jesus AA, de Almeida RP, Rego MA, Burattini MN, Pearce EJ, Carvalho EM, 2002. Clinical and immunologic evaluation of 31 patients with acute schistosomiasis mansoni. J Infect Dis 185: 98–105.
Gazzinelli G, Colley DG, 1992. Human immune responses during schistosomiasis mansoni. Rev Soc Bras Med Trop 25: 125–134.
Williams ME, Montenegro S, Domingues AL, Wynn TA, Teixeira K, Mahanty S, Coutinho A, Sher A, 1994. Leukocytes of patients with Schistosoma mansoni respond with a Th2 pattern of cytokine production to mitogen or egg antigens but with a Th0 pattern to worm antigens. J Infect Dis 170: 946–954.
Finkelman FD, Shea-Donohue T, Goldhill J, Sullivan CA, Morris SC, Madden KB, Gause WC, Urban JF Jr, 1997. Cytokine regulation of host defense against parasitic gastrointestinal nematodes: lessons from studies with rodent models. Annu Rev Immunol 15: 505–533.
Sturrock RF, 2001. Schistosomiasis epidemiology and control: how did we get here and where should we go? Mem Inst Oswaldo Cruz 96 (Suppl) 17–27.
Bergquist R, Utzinger J, McManus DP, 2008. Trick or treat: the role of vaccines in integrated schistosomiasis control. PLoS Negl Trop Dis 2: e244.
McManus DP, Loukas A, 2008. Current status of vaccines for schistosomiasis. Clin Microbiol Rev 21: 225–242.
Cardoso FC, Macedo GC, Gava E, Kitten GT, Mati VL, de Melo AL, Caliari MV, Almeida GT, Venancio TM, Verjovski-Almeida S, Oliveira SC, 2008. Schistosoma mansoni tegument protein Sm29 is able to induce a Th1-type of immune response and protection against parasite infection. PLoS Negl Trop Dis 2: e308.
Lopes DO, Paiva LF, Martins MA, Cardoso FC, Rajao MA, Pinho JM, Caliari MV, Correa-Oliveira R, Mello SM, Leite LC, Oliveira SC, 2009. Sm21.6 a novel EF-hand family protein member located on the surface of Schistosoma mansoni adult worm that failed to induce protection against challenge infection but reduced liver pathology. Vaccine 27: 4127–4135.
Tendler M, Brito CA, Vilar MM, Serra-Freire N, Diogo CM, Almeida MS, Delbem AC, Da Silva JF, Savino W, Garratt RC, Katz N, Simpson AS, 1996. A Schistosoma mansoni fatty acid-binding protein, Sm14, is the potential basis of a dual-purpose anti-helminth vaccine. Proc Natl Acad Sci USA 93: 269–273.
Pacheco LG, Zucconi E, Mati VL, Garcia RM, Miyoshi A, Oliveira SC, de Melo AL, Azevedo V, 2005. Oral administration of a live Aro attenuated Salmonella vaccine strain expressing 14-kDa Schistosoma mansoni fatty acid-binding protein induced partial protection against experimental schistosomiasis. Acta Trop 95: 132–142.
Pacifico LG, Fonseca CT, Chiari L, Oliveira SC, 2006. Immunization with Schistosoma mansoni 22.6 kDa antigen induces partial protection against experimental infection in a recombinant protein form but not as DNA vaccine. Immunobiology 211: 97–104.
Hirsch C, Zouain CS, Alves JB, Goes AM, 1997. Induction of protective immunity and modulation of granulomatous hypersensitivity in mice using PIII, an anionic fraction of Schistosoma mansoni adult worm. Parasitology 115: 21–28.
Fahel JS, Macedo GC, Pinheiro CS, Caliari MV, Oliveira SC, 2010. IPSE/alpha-1 of Schistosoma mansoni egg induces enlargement of granuloma but does not alter Th2 balance after infection. Parasite Immunol 32: 345–353.
Schramm G, Mohrs K, Wodrich M, Doenhoff MJ, Pearce EJ, Haas H, Mohrs M, 2007. Cutting edge: IPSE/alpha-1, a glycoprotein from Schistosoma mansoni eggs, induces IgE-dependent, antigen-independent IL-4 production by murine basophils in vivo. J Immunol 178: 6023–6027.
Schramm G, Falcone FH, Gronow A, Haisch K, Mamat U, Doenhoff MJ, Oliveira G, Galle J, Dahinden CA, Haas H, 2003. Molecular characterization of an interleukin-4-inducing factor from Schistosoma mansoni eggs. J Biol Chem 278: 18384–18392.
Dunne DW, Butterworth AE, Fulford AJ, Kariuki HC, Langley JG, Ouma JH, Capron A, Pierce RJ, Sturrock RF, 1992. Immunity after treatment of human schistosomiasis: association between IgE antibodies to adult worm antigens and resistance to reinfection. Eur J Immunol 22: 1483–1494.
Rihet P, Demeure CE, Bourgois A, Prata A, Dessein AJ, 1991. Evidence for an association between human resistance to Schistosoma mansoni and high anti-larval IgE levels. Eur J Immunol 21: 2679–2686.
Hagan P, Blumenthal UJ, Dunn D, Simpson AJ, Wilkins HA, 1991. Human IgE, IgG4 and resistance to reinfection with Schistosoma haematobium. Nature 349: 243–245.
Roberts M, Butterworth AE, Kimani G, Kamau T, Fulford AJ, Dunne DW, Ouma JH, Sturrock RF, 1993. Immunity after treatment of human schistosomiasis: association between cellular responses and resistance to reinfection. Infect Immun 61: 4984–4993.
Iskander R, Das PK, Aalberse RC, 1981. IgG4 antibodies in Egyptian patients with schistosomiasis. Int Arch Allergy Appl Immunol 66: 200–207.
Grogan JL, Kremsner PG, van Dam GJ, Metzger W, Mordmuller B, Deelder AM, Yazdanbakhsh M, 1996. Antischistosome IgG4 and IgE responses are affected differentially by chemotherapy in children versus adults. J Infect Dis 173: 1242–1247.
Caldas IR, Correa-Oliveira R, Colosimo E, Carvalho OS, Massara CL, Colley DG, Gazzinelli G, 2000. Susceptibility and resistance to Schistosoma mansoni reinfection: parallel cellular and isotypic immunologic assessment. Am J Trop Med Hyg 62: 57–64.
Wilkins HA, Blumenthal UJ, Hagan P, Hayes RJ, Tulloch S, 1987. Resistance to reinfection after treatment of urinary schistosomiasis. Trans R Soc Trop Med Hyg 81: 29–35.
Barbour AD, 1985. The importance of age and water contact patterns in relation to Schistosoma haematobium infection. Trans R Soc Trop Med Hyg 79: 151–153.
Correa-Oliveira R, Pearce EJ, Oliveira GC, Golgher DB, Katz N, Bahia LG, Carvalho OS, Gazzinelli G, Sher A, 1989. The human immune response to defined immunogens of Schistosoma mansoni: elevated antibody levels to paramyosin in stool-negative individuals from two endemic areas in Brazil. Trans R Soc Trop Med Hyg 83: 798–804.
Viana IR, Sher A, Carvalho OS, Massara CL, Eloi-Santos SM, Pearce EJ, Colley DG, Gazzinelli G, Correa-Oliveira R, 1994. Interferon-gamma production by peripheral blood mononuclear cells from residents of an area endemic for Schistosoma mansoni. Trans R Soc Trop Med Hyg 88: 466–470.
Viana IR, Correa-Oliveira R, Carvalho Odos S, Massara CL, Colosimo E, Colley DG, Gazzinelli G, 1995. Comparison of antibody isotype responses to Schistosoma mansoni antigens by infected and putative resistant individuals living in an endemic area. Parasite Immunol 17: 297–304.
Bahia-Oliveira LM, Gazzinelli G, Eloi-Santos SM, Cunha-Melo JR, Alves-Oliveira LF, Silveira AM, Viana IR, Carmo J, Souza A, Correa-Oliveira R, 1992. Differential cellular reactivity to adult worm antigens of patients with different clinical forms of Schistosoma mansoni. Trans R Soc Trop Med Hyg 86 57–61.
Brito CF, Caldas IR, Coura Filho P, Correa-Oliveira R, Oliveira SC, 2000. CD4+ T cells of schistosomiasis naturally resistant individuals living in an endemic area produce interferon-gamma and tumour necrosis factor-alpha in response to the recombinant 14KDA Schistosoma mansoni fatty acid-binding protein. Scand J Immunol 51: 595–601.
Grant AV, Araujo MI, Ponte EV, Oliveira RR, Cruz AA, Barnes KC, Beaty TH, 2008. High heritability but uncertain mode of inheritance for total serum IgE level and Schistosoma mansoni infection intensity in a schistosomiasis-endemic Brazilian population. J Infect Dis 198: 1227–1236.
Araujo MI, Hoppe B, Medeiros M Jr, Alcantara L, Almeida MC, Schriefer A, Oliveira RR, Kruschewsky R, Figueiredo JP, Cruz AA, Carvalho EM, 2004. Impaired T helper 2 response to aeroallergen in helminth-infected patients with asthma. J Infect Dis 190: 1797–1803.
World Health Organization, 2002. Prevention and control of schistosomiasis and soil-transmitted helminthiasis. World Health Organ Tech Rep Ser 912: 1–57.
Swindale A, Bilinsky P, 2006. Development of a universally applicable household food insecurity measurement tool: process, current status, and outstanding issues. J Nutr 136: 1449S–1452S.
Ewing JA, 1984. Detecting alcoholism. The CAGE questionnaire. JAMA 252: 1905–1907.
Lima e Costa MF, Magalhaes MH, Rocha RS, Antunes CM, Katz N, 1987. Water-contact patterns and socioeconomic variables in the epidemiology of schistosomiasis mansoni in an endemic area in Brazil. Bull World Health Organ 65: 57–66.
Katz N, Coelho PM, Pellegrino J, 1970. Evaluation of Kato’s quantitative method through the recovery of Schistosoma mansoni eggs added to human feces. J Parasitol 56: 1032–1033.
Cardoso LS, Araujo MI, Goes AM, Pacifico LG, Oliveira RR, Oliveira SC, 2007. Polymyxin B as inhibitor of LPS contamination of Schistosoma mansoni recombinant proteins in human cytokine analysis. Microb Cell Fact 6: 1.
Naus CW, Kimani G, Ouma JH, Fulford AJ, Webster M, van Dam GJ, Deelder AM, Butterworth AE, Dunne DW, 1999. Development of antibody isotype responses to Schistosoma mansoni in an immunologically naive immigrant population: influence of infection duration, infection intensity, and host age. Infect Immun 67: 3444–3451.
Ribeiro de Jesus A, Araujo I, Bacellar O, Magalhaes A, Pearce E, Harn D, Strand M, Carvalho EM, 2000. Human immune responses to Schistosoma mansoni vaccine candidate antigens. Infect Immun 68: 2797–2803.
Souza-Atta ML, Araujo MI, D’Oliveira Junior A, Ribeiro-de-Jesus A, Almeida RP, Atta AM, Carvalho EM, 1999. Detection of specific IgE antibodies in parasite diseases. Braz J Med Biol Res 32: 1101–1105.
Mayfield D, McLeod G, Hall P, 1974. The CAGE questionnaire: validation of a new alcoholism screening instrument. Am J Psychiatry 131: 1121–1123.
King M, 1986. At risk drinking among general practice attenders: validation of the CAGE questionnaire. Psychol Med 16: 213–217.
Gazzinelli A, Bethony J, Fraga LA, LoVerde PT, Correa-Oliveira R, Kloos H, 2001. Exposure to Schistosoma mansoni infection in a rural area of Brazil. I: water contact. Trop Med Int Health 6: 126–135.
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Gazzinelli A, Velasquez-Melendez G, Crawford SB, LoVerde PT, Correa-Oliveira R, Kloos H, 2006. Socioeconomic determinants of schistosomiasis in a poor rural area in Brazil. Acta Trop 99: 260–271.
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Detailed knowledge of factors associated with resistance to Schistosoma mansoni infection in endemic areas might facilitate more effective schistosomiasis control. We conducted a cross-sectional study of persons resistant to schistosomiasis and found no association between socioeconomic status and resistance to infection. Mononuclear cells of resistant subjects produced higher levels of interleukin-5 (IL-5), IL-13 and interferon-γ upon stimulation with soluble egg antigen (SEA) compared with infected persons. When stimulated with Sm21.6 or Sm22.6, levels of IL-10 were higher in cell culture of resistant persons. Levels of IgE against soluble adult worm antigen (SWAP) and against interleukin-4–inducing principle from S. mansoni eggs (IPSE) and levels of IgG4 against SWAP, SEA, and Sm22.6 were lower in the resistant group compared with the susceptible group. Our data suggest that socioeconomic status could not fully explain resistance to S. mansoni infection observed in the studied area. However, a mixture of Th1 and Th2 immune responses and low levels of specific IgG4 against parasite antigens could be mediating resistance to infection.
Financial support: This study was supported by the Brazilian National Research Council (CNPq) Universal (482064/2010-2). Ricardo R. Oliveira and Marshall J. Glesby were supported in part by the Fogarty/Ellison International Clinical Research Scholars Program and National Institutes of Health/National Institutes of Allergy and Infectious Diseases grant K24Al078884, respectively. Kathleen C. Barnes was supported in part by the Mary Beryl Patch Turnbull Scholar Program. Maria Ilma Araújo and Edgar M. Carvalho are investigators supported by CNPq.
Authors’ addresses: Ricardo R. Oliveira, Serviço de Imunologia, Hospital Universitário Prof Edgard Santos, Universidade Federal da Bahia, Salvador, Bahia, Brazil; Instituto Nacional de Ciência e Tecnologia de Doenças Tropicais (INCT-DT/CNPq), Salvador, Bahia, Brazil, E-mail: ricardoriccio@gmail.com. Joanemile P. Figueiredo, Serviço de Imunologia, Hospital Universitário Prof Edgard Santos, Universidade Federal da Bahia, Salvador, Bahia, Brazil, E-mail: milepf@yahoo.com.br. Luciana S. Cardoso, Serviço de Imunologia, Hospital Universitário Prof Edgard Santos, Universidade Federal da Bahia, Salvador, Bahia, Brazil; Departamento de Ciências da Vida, Universidade do Estado da Bahia, Salvador, Bahia, Brazil; Instituto Nacional de Ciência e Tecnologia de Doenças Tropicais (INCT-DT/CNPq), Salvador, Bahia, Brazil, E-mail: luciana.imuno@gmail.com. Rafael L. Jabar and Robson P. Souza, Serviço de Imunologia, Hospital Universitário Prof Edgard Santos, Universidade Federal da Bahia, Salvador, Bahia, Brazil, E-mails: rafajabar@hotmail.com and robson.imuno@gmail.com. Martin T. Wells, Department of Biological Statistics and Computational Biology, Cornell University, Ithaca, NY, E-mail: martin.t.wells@gmail.com. Edgar M. Carvalho, Serviço de Imunologia, Hospital Universitário Prof Edgard Santos, Universidade Federal da Bahia, Salvador, Bahia, Brazil; Escola Bahiana de Medicina e Saúde Pública, Salvador, Bahia, Brazil; Instituto Nacional de Ciência e Tecnologia de Doenças Tropicais (INCT-DT/CNPq), Salvador, Bahia, Brazil, E-mail: edgar@ufba.br. Daniel W. Fitzgerald, Center for Global Health, Division of Infectious Diseases, Department of Medicine, Weill Cornell Medical College, New York, NY, E-mail: dfitzgerald@gheskio.org. Kathleen C. Barnes, Division of Allergy and Clinical Immunology, Department of Medicine, Johns Hopkins University, Baltimore, MD, E-mail: kbarnes5@jhmi.edu. Maria Ilma Araújo, Serviço de Imunologia, Hospital Universitário Prof Edgard Santos, Universidade Federal da Bahia, Salvador, Bahia, Brazil; Escola Bahiana de Medicina e Saúde Pública, Salvador, Bahia, Brazil; Instituto Nacional de Ciência e Tecnologia de Doenças Tropicais (INCT-DT/CNPq), Salvador, Bahia, Brazil, E-mail: mia@ufba.br. Marshall J. Glesby, Center for Global Health, Division of Infectious Diseases, Department of Medicine, Weill Cornell Medical College, New York, NY, E-mail: mag2005@med.cornell.ed.
WHO/TDR, 2002. Strategic Direction for Research: Schistosomiasis. Geneva: World Health Organization.
de Jesus AR, Silva A, Santana LB, Magalhaes A, de Jesus AA, de Almeida RP, Rego MA, Burattini MN, Pearce EJ, Carvalho EM, 2002. Clinical and immunologic evaluation of 31 patients with acute schistosomiasis mansoni. J Infect Dis 185: 98–105.
Gazzinelli G, Colley DG, 1992. Human immune responses during schistosomiasis mansoni. Rev Soc Bras Med Trop 25: 125–134.
Williams ME, Montenegro S, Domingues AL, Wynn TA, Teixeira K, Mahanty S, Coutinho A, Sher A, 1994. Leukocytes of patients with Schistosoma mansoni respond with a Th2 pattern of cytokine production to mitogen or egg antigens but with a Th0 pattern to worm antigens. J Infect Dis 170: 946–954.
Finkelman FD, Shea-Donohue T, Goldhill J, Sullivan CA, Morris SC, Madden KB, Gause WC, Urban JF Jr, 1997. Cytokine regulation of host defense against parasitic gastrointestinal nematodes: lessons from studies with rodent models. Annu Rev Immunol 15: 505–533.
Sturrock RF, 2001. Schistosomiasis epidemiology and control: how did we get here and where should we go? Mem Inst Oswaldo Cruz 96 (Suppl) 17–27.
Bergquist R, Utzinger J, McManus DP, 2008. Trick or treat: the role of vaccines in integrated schistosomiasis control. PLoS Negl Trop Dis 2: e244.
McManus DP, Loukas A, 2008. Current status of vaccines for schistosomiasis. Clin Microbiol Rev 21: 225–242.
Cardoso FC, Macedo GC, Gava E, Kitten GT, Mati VL, de Melo AL, Caliari MV, Almeida GT, Venancio TM, Verjovski-Almeida S, Oliveira SC, 2008. Schistosoma mansoni tegument protein Sm29 is able to induce a Th1-type of immune response and protection against parasite infection. PLoS Negl Trop Dis 2: e308.
Lopes DO, Paiva LF, Martins MA, Cardoso FC, Rajao MA, Pinho JM, Caliari MV, Correa-Oliveira R, Mello SM, Leite LC, Oliveira SC, 2009. Sm21.6 a novel EF-hand family protein member located on the surface of Schistosoma mansoni adult worm that failed to induce protection against challenge infection but reduced liver pathology. Vaccine 27: 4127–4135.
Tendler M, Brito CA, Vilar MM, Serra-Freire N, Diogo CM, Almeida MS, Delbem AC, Da Silva JF, Savino W, Garratt RC, Katz N, Simpson AS, 1996. A Schistosoma mansoni fatty acid-binding protein, Sm14, is the potential basis of a dual-purpose anti-helminth vaccine. Proc Natl Acad Sci USA 93: 269–273.
Pacheco LG, Zucconi E, Mati VL, Garcia RM, Miyoshi A, Oliveira SC, de Melo AL, Azevedo V, 2005. Oral administration of a live Aro attenuated Salmonella vaccine strain expressing 14-kDa Schistosoma mansoni fatty acid-binding protein induced partial protection against experimental schistosomiasis. Acta Trop 95: 132–142.
Pacifico LG, Fonseca CT, Chiari L, Oliveira SC, 2006. Immunization with Schistosoma mansoni 22.6 kDa antigen induces partial protection against experimental infection in a recombinant protein form but not as DNA vaccine. Immunobiology 211: 97–104.
Hirsch C, Zouain CS, Alves JB, Goes AM, 1997. Induction of protective immunity and modulation of granulomatous hypersensitivity in mice using PIII, an anionic fraction of Schistosoma mansoni adult worm. Parasitology 115: 21–28.
Fahel JS, Macedo GC, Pinheiro CS, Caliari MV, Oliveira SC, 2010. IPSE/alpha-1 of Schistosoma mansoni egg induces enlargement of granuloma but does not alter Th2 balance after infection. Parasite Immunol 32: 345–353.
Schramm G, Mohrs K, Wodrich M, Doenhoff MJ, Pearce EJ, Haas H, Mohrs M, 2007. Cutting edge: IPSE/alpha-1, a glycoprotein from Schistosoma mansoni eggs, induces IgE-dependent, antigen-independent IL-4 production by murine basophils in vivo. J Immunol 178: 6023–6027.
Schramm G, Falcone FH, Gronow A, Haisch K, Mamat U, Doenhoff MJ, Oliveira G, Galle J, Dahinden CA, Haas H, 2003. Molecular characterization of an interleukin-4-inducing factor from Schistosoma mansoni eggs. J Biol Chem 278: 18384–18392.
Dunne DW, Butterworth AE, Fulford AJ, Kariuki HC, Langley JG, Ouma JH, Capron A, Pierce RJ, Sturrock RF, 1992. Immunity after treatment of human schistosomiasis: association between IgE antibodies to adult worm antigens and resistance to reinfection. Eur J Immunol 22: 1483–1494.
Rihet P, Demeure CE, Bourgois A, Prata A, Dessein AJ, 1991. Evidence for an association between human resistance to Schistosoma mansoni and high anti-larval IgE levels. Eur J Immunol 21: 2679–2686.
Hagan P, Blumenthal UJ, Dunn D, Simpson AJ, Wilkins HA, 1991. Human IgE, IgG4 and resistance to reinfection with Schistosoma haematobium. Nature 349: 243–245.
Roberts M, Butterworth AE, Kimani G, Kamau T, Fulford AJ, Dunne DW, Ouma JH, Sturrock RF, 1993. Immunity after treatment of human schistosomiasis: association between cellular responses and resistance to reinfection. Infect Immun 61: 4984–4993.
Iskander R, Das PK, Aalberse RC, 1981. IgG4 antibodies in Egyptian patients with schistosomiasis. Int Arch Allergy Appl Immunol 66: 200–207.
Grogan JL, Kremsner PG, van Dam GJ, Metzger W, Mordmuller B, Deelder AM, Yazdanbakhsh M, 1996. Antischistosome IgG4 and IgE responses are affected differentially by chemotherapy in children versus adults. J Infect Dis 173: 1242–1247.
Caldas IR, Correa-Oliveira R, Colosimo E, Carvalho OS, Massara CL, Colley DG, Gazzinelli G, 2000. Susceptibility and resistance to Schistosoma mansoni reinfection: parallel cellular and isotypic immunologic assessment. Am J Trop Med Hyg 62: 57–64.
Wilkins HA, Blumenthal UJ, Hagan P, Hayes RJ, Tulloch S, 1987. Resistance to reinfection after treatment of urinary schistosomiasis. Trans R Soc Trop Med Hyg 81: 29–35.
Barbour AD, 1985. The importance of age and water contact patterns in relation to Schistosoma haematobium infection. Trans R Soc Trop Med Hyg 79: 151–153.
Correa-Oliveira R, Pearce EJ, Oliveira GC, Golgher DB, Katz N, Bahia LG, Carvalho OS, Gazzinelli G, Sher A, 1989. The human immune response to defined immunogens of Schistosoma mansoni: elevated antibody levels to paramyosin in stool-negative individuals from two endemic areas in Brazil. Trans R Soc Trop Med Hyg 83: 798–804.
Viana IR, Sher A, Carvalho OS, Massara CL, Eloi-Santos SM, Pearce EJ, Colley DG, Gazzinelli G, Correa-Oliveira R, 1994. Interferon-gamma production by peripheral blood mononuclear cells from residents of an area endemic for Schistosoma mansoni. Trans R Soc Trop Med Hyg 88: 466–470.
Viana IR, Correa-Oliveira R, Carvalho Odos S, Massara CL, Colosimo E, Colley DG, Gazzinelli G, 1995. Comparison of antibody isotype responses to Schistosoma mansoni antigens by infected and putative resistant individuals living in an endemic area. Parasite Immunol 17: 297–304.
Bahia-Oliveira LM, Gazzinelli G, Eloi-Santos SM, Cunha-Melo JR, Alves-Oliveira LF, Silveira AM, Viana IR, Carmo J, Souza A, Correa-Oliveira R, 1992. Differential cellular reactivity to adult worm antigens of patients with different clinical forms of Schistosoma mansoni. Trans R Soc Trop Med Hyg 86 57–61.
Brito CF, Caldas IR, Coura Filho P, Correa-Oliveira R, Oliveira SC, 2000. CD4+ T cells of schistosomiasis naturally resistant individuals living in an endemic area produce interferon-gamma and tumour necrosis factor-alpha in response to the recombinant 14KDA Schistosoma mansoni fatty acid-binding protein. Scand J Immunol 51: 595–601.
Grant AV, Araujo MI, Ponte EV, Oliveira RR, Cruz AA, Barnes KC, Beaty TH, 2008. High heritability but uncertain mode of inheritance for total serum IgE level and Schistosoma mansoni infection intensity in a schistosomiasis-endemic Brazilian population. J Infect Dis 198: 1227–1236.
Araujo MI, Hoppe B, Medeiros M Jr, Alcantara L, Almeida MC, Schriefer A, Oliveira RR, Kruschewsky R, Figueiredo JP, Cruz AA, Carvalho EM, 2004. Impaired T helper 2 response to aeroallergen in helminth-infected patients with asthma. J Infect Dis 190: 1797–1803.
World Health Organization, 2002. Prevention and control of schistosomiasis and soil-transmitted helminthiasis. World Health Organ Tech Rep Ser 912: 1–57.
Swindale A, Bilinsky P, 2006. Development of a universally applicable household food insecurity measurement tool: process, current status, and outstanding issues. J Nutr 136: 1449S–1452S.
Ewing JA, 1984. Detecting alcoholism. The CAGE questionnaire. JAMA 252: 1905–1907.
Lima e Costa MF, Magalhaes MH, Rocha RS, Antunes CM, Katz N, 1987. Water-contact patterns and socioeconomic variables in the epidemiology of schistosomiasis mansoni in an endemic area in Brazil. Bull World Health Organ 65: 57–66.
Katz N, Coelho PM, Pellegrino J, 1970. Evaluation of Kato’s quantitative method through the recovery of Schistosoma mansoni eggs added to human feces. J Parasitol 56: 1032–1033.
Cardoso LS, Araujo MI, Goes AM, Pacifico LG, Oliveira RR, Oliveira SC, 2007. Polymyxin B as inhibitor of LPS contamination of Schistosoma mansoni recombinant proteins in human cytokine analysis. Microb Cell Fact 6: 1.
Naus CW, Kimani G, Ouma JH, Fulford AJ, Webster M, van Dam GJ, Deelder AM, Butterworth AE, Dunne DW, 1999. Development of antibody isotype responses to Schistosoma mansoni in an immunologically naive immigrant population: influence of infection duration, infection intensity, and host age. Infect Immun 67: 3444–3451.
Ribeiro de Jesus A, Araujo I, Bacellar O, Magalhaes A, Pearce E, Harn D, Strand M, Carvalho EM, 2000. Human immune responses to Schistosoma mansoni vaccine candidate antigens. Infect Immun 68: 2797–2803.
Souza-Atta ML, Araujo MI, D’Oliveira Junior A, Ribeiro-de-Jesus A, Almeida RP, Atta AM, Carvalho EM, 1999. Detection of specific IgE antibodies in parasite diseases. Braz J Med Biol Res 32: 1101–1105.
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