<i>Schistosoma mansoni</i> Infection: A Major Contributor of Reduced Effective T Helper Responses against <i>Plasmodium falciparum</i> and <i>Schistosoma mansoni</i> Co-Infection in <i>ex vivo</i>: A Cross-Sectional Study to Assess Th1, Th2 & Th17 Immune Responses — Oak Academic Publishing
Research ArticleOpen AccessGoogle Scholar indexed
<i>Schistosoma mansoni</i> Infection: A Major Contributor of Reduced Effective T Helper Responses against <i>Plasmodium falciparum</i> and <i>Schistosoma mansoni</i> Co-Infection in <i>ex vivo</i>: A Cross-Sectional Study to Assess Th1, Th2 & Th17 Immune Responses
Microbiology Department, College of Health Sciences, Makerere University, Kampala, Uganda
,
Vector Control Division, Ministry of Health, Kampala, Uganda
,
Microbiology Department, College of Health Sciences, Makerere University, Kampala, Uganda
,
Microbiology Department, College of Health Sciences, Makerere University, Kampala, Uganda
,
Microbiology Department, College of Health Sciences, Makerere University, Kampala, Uganda
,
Microbiology Department, College of Health Sciences, Makerere University, Kampala, Uganda
,
Infectious Diseases Institute, Kampala, Uganda
,
Microbiology Department, College of Health Sciences, Makerere University, Kampala, Uganda
,
Vector Control Division, Ministry of Health, Kampala, Uganda
,
Vector Control Division, Ministry of Health, Kampala, Uganda
1 Microbiology Department, College of Health Sciences, Makerere University, Kampala, Uganda
2 Vector Control Division, Ministry of Health, Kampala, Uganda
3 Microbiology Department, College of Health Sciences, Makerere University, Kampala, Uganda
4 Microbiology Department, College of Health Sciences, Makerere University, Kampala, Uganda
5 Microbiology Department, College of Health Sciences, Makerere University, Kampala, Uganda
6 Microbiology Department, College of Health Sciences, Makerere University, Kampala, Uganda
7 Infectious Diseases Institute, Kampala, Uganda
8 Microbiology Department, College of Health Sciences, Makerere University, Kampala, Uganda
9 Vector Control Division, Ministry of Health, Kampala, Uganda
10 Vector Control Division, Ministry of Health, Kampala, Uganda
Background: Parasitic worms evade immune responses, and interactions between diseases can cause altered immunologic outcomes compared to what usually occurs with single infections. These interactions may influence vaccine and chemotherapeutic efficacy. Schistosoma mansoni and Plasmodium falciparum are co-endemic in Uganda and are the leading parasitic causes of public health problems across sub-Saharan Africa. Objectives: The overall aim was therefore, to elucidate the impact of S. mansoni infection on protective T helper immune responses on P. falciparum and S. mansoni co-infection. Methodology: This study evaluated the T helper immune responses in individuals with independent S. mansoni infection, independent P. falciparum infection, co-infection and non-infection in school attending children in a co-endemic area along Lake Victoria shores, Uganda. Immune responses were categorized into Th1, Th2, and Th17 based on unique cytokine(s) produced by the T helper subpopulation in ex vivo. Kato Katz thick smears and circulating cathodic antigen tests were performed for S. mansoni screening, whereas thick and thin blood smear techniques were performed for P. falciparum screening. Results: We observed an up regulated Th1 T helper subpopulation in independent P. falciparum infections compared to the uninfected group. Suboptimal T helper immune responses were detected in independent S. mansoni infections characterized by significantly down regulated Th1 (Z = -1.425, p = 0.0313) response in comparison to the non-infected group. Suboptimal T helper immune responses were also recorded in the co-infected individuals characterized by significantly down regulated Th1 (Z = -3.260, p = 0.0273) and Th2 (Z = -1.180, p = 0.0078) responses compared to independent P. falciparum . Conclusions: S. mansoni infection is a major contributor of a reduced effective T helper immune response against P. falciparum in P. falciparum and S. mansoni co-infection.
Snow, R.W., Guerra, C.A., Noor, A.M., Myint, H.Y. and Hay, S.I. (2005) The Global Distribution of Clinical Episodes of Plasmodium falciparum Malaria. Nature, 434, 214-217. https://doi.org/10.1038/nature03342
Steinmann, P., Keiser, J., Bos, R., Tanner, M. and Utzinger, J. (2006) Schistosomiasis and Water Resources Development: Systematic Review, Metaanalysis, and Estimates of People at Risk. The Lancet Infectious Diseases, 6, 411-425.
WHO (2010) World Health Report. World Health Organization, Geneva.
Urban, B.C., Ferguson, D.J., Pain, A., Willcox, N., Plebanski, M., Austyn, J.M. and Roberts, D.J. (1999) Plasmodium falciparum-Infected Erythrocytes Modulate the Maturation of Dendritic Cells. Nature, 400, 73-77. https://doi.org/10.1038/21900
Wan-Chung (2013) Human Immune Responses to Plasmodium falciparum Infection: Molecular Evidence for a Suboptimal TH αβ and TH17 bias\over Ideal and Effective Traditional TH1 Immune Response. Malaria Journal, 12, 392. https://doi.org/10.1186/1475-2875-12-392
BD (2015) Assay Procedure for Th1/Th2/Th17 Phenotyping Kit. Technical Data Sheet BD Pharmingen Production Information. Material Number: 560751. Size: 50 Tests.
Cooke, A. (2008) Review Series on Helminths, Immune Modulation and the Hygiene Hypothesis: How Might Infection Modulate the Onset of Type 1 Diabetes? Immunology, 126, 12-17. https://doi.org/10.1111/j.1365-2567.2008.03009.x
Correale, J. and Farez, M. (2007) Association between Parasitic Infection and Immune Response in Multiple Sclerosis. Annals of Neurology, 61, 97-108. https://doi.org/10.1002/ana.21067
Bashir, M.E.H., Anderson, P., Fuss, I., et al. (2002) An Enteric Helminth Infection Protects against an Allergic Response to Dietary Antigen. The Journal of Immunology, 169, 3284-3292. https://doi.org/10.4049/jimmunol.169.6.3284
Weinstock, J.V., Summer, R. and Elliott, D. (2005) Role of Helminths in Regulating Mucosal Inflammation. Seminars in Immunopathology, 27, 249-271. https://doi.org/10.1007/s00281-005-0209-3
Osada, Y. and Kanazawa, T. (2010) Parasitic Helminths: New Weapons against Immunological Disorders. Journal of Biomedicine and Biotechnology, 2010, Article ID: 743758. https://doi.org/10.1155/2010/743758
Rook, G.A.W. (2008) Review Series on Helminths, Immune Modulation and the Hygiene Hypothesis: The Broader Implications of the Hygiene Hypothesis. Immunology, 126, 3-11. https://doi.org/10.1111/j.1365-2567.2008.03007.x
T Helper Immune Response
<
i>
Ex Vivo<
/i>
Moreels, T.G., Nieuwendijk, R.J., Elliot, D.E., et al. (2004) Concurrent Infection with Schistosoma mansoni Attenuates Inflammation Induced Changes in Colonic Morphology, Cytokine Levels, and Smooth Muscle Contractility of Trinitrobenzenesulphonic Acid Induced Colitis in rats. Gut, 53, 99-107. https://doi.org/10.1136/gut.53.1.99
Melendez, A.J., Harnett, M., Pushparaj, P., et al. (2007) Inhibition of Fceri-Mediated Mast Cell Responses by ES-62, a Product of Parasitic Filarial Nematodes. Nature Medicine, 13, 1375-1381. https://doi.org/10.1038/nm1654
Supali, T., et al. (2010) Polyparasitism and Its Impact on the Immune System. International Journal for Parasitology, 40, 1171-1176.
Nookala, S., Srinivasan, S., Kaliraj, P., Narayanan, R.B. and Nutman, T.B. (2004) Impairment of Tetanus-Specific Cellular and Humoral Responses Following Tetanus Vaccination in Human Lymphatic Filariasis. Infection and Immunity, 72, 2598-2604. https://doi.org/10.1128/IAI.72.5.2598-2604.2004
Sabin, E.A., Araujo, M.I., Carvalho, E.M. and Pearce, E.J. (1996) Impairment of Tetanus Toxoid-Specific Th1-Like Immune Responses in Humans Infected with Schistosoma mansoni. The Journal of Infectious Diseases, 173, 269-272. https://doi.org/10.1093/infdis/173.1.269
Sabah, A.A., Fletcher, C., Webbe, G. and Doenhoff, M.J. (1985) Schistosoma mansoni: Reduced Efficacy of Chemotherapy in Infected T-Cell Deprived Mice. Experimental Parasitology, 60, 348-354.
Berger, B.J. and Fairlamb, A.H. (1992) Interactions between Immunity and Chemotherapy in Treatment of the Trypanosomiasis and Leishmaniasis. Parasitology, 105, S71-S78.
Masaki, T., Elena, S.T., Scott, L., John, M.M. and Jay, A.B. (2009) Synergistic Enhancement of CD8+ T Cell Mediated Tumor Vaccine Efficacy by an Anti-Transforming Growth Factor-β Monoclonal Antibody. Clinical Cancer Research, 15, 6560.
Zhang, Y., Koukounari, A., Kabatereine, N., Fleming, F., Kazibwe, F., et al. (2007) Parasitological Impact of 2-Year Preventive Chemotherapy on Schistosomiasis and Soil-Transmitted Helminthiasis in Uganda. BMC Medicine, 5, 27. https://doi.org/10.1186/1741-7015-5-27
Sedegah, M., Finkelman, F. and Hoffman, S.L. (1994) Interleukin 12 Induction of Interferon Gamma-Dependent Protection against Malaria. Proceedings of the National Academy of Sciences, 91, 10700-10702. https://doi.org/10.1073/pnas.91.22.10700
Su, Z. and Stevenson, M.M. (2000) Central Role of Endogenous Gamma Interferon in Protective Immunity against Blood-Stage Plasmodium chabaudi AS Infection. Infection and Immunity, 68, 4399-4406. https://doi.org/10.1128/iai.68.8.4399-4406.2000
Keller, C.C., Yamo, O., Ouma, C., Ong’echa, J.M., Ounah, D., Hittner, J.B., Vulule, J.M. and Perkins, D.J. (2006) Acquisition of Hemozoin by Monocytes Down-Regulates Interleukin-12 p40 (IL-12p40) Transcripts and Circulating IL-12p70 through an IL-10-Dependent Mechanism: In Vivo and in Vitro Findings in Severe Malarial Anemia. Infection and Immunity, 74, 5249-5260. https://doi.org/10.1128/IAI.00843-06
Boutlis, C.S., Lagog, M., Chaisavaneeyakorn, S., Misukonis, M.A., Bockarie, M.J., Mgone, C.S., Wang, Z., Morahan, G., Weinberg, J.B., Udhayakumar, V. and Anstey, N.M. (2003) Plasma Interleukin-12 in Malaria-Tolerant Papua New Guineans: Inverse Correlation with Plasmodium falciparum Parasitemia and Peripheral Blood Mononuclear Cell Nitric Oxide Synthase Activity. Infection and Immunity, 71, 6354-6357. https://doi.org/10.1128/IAI.71.11.6354-6357.2003
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 Schistosomiasismansoni. The Journal of Infectious Diseases, 185, 98-105. https://doi.org/10.1086/324668
Araujo, M.I., Bacellar, O., Ribeiro, D.J.A. and Carvalho, E.M. (1994) The Absence of Gamma-Interferon Production of S. Mansoni Antigens in Patients with Schistosomiasis. Brazilian Journal of Medical and Biological Research, 27, 1619-1625.
Malaquias, L.C., Falcao, P.L., Silveira, A.M., Gazzinelli, G., Prata, A., Coffman, R.L., Pizziolo, V., Souza, C.P., Colley, D.G. and Correa-Oliveira, R. (1997) Cytokine Regulation of Human Immune Response to Schistosoma mansoni: Analysis of the Role of IL-4, IL-5 and IL-10 on Peripheral Blood Mononuclear Cell Responses. Scandinavian Journal of Immunology, 46, 393-398. https://doi.org/10.1046/j.1365-3083.1997.d01-136.x
Joseph, S., Jones, F.M., Kimani, G., Mwatha, J.K., Kamau, T., Kazibwe, F., Kemijumbi, J., Kabatereine, N.B., Booth, M., Kariuki, H.C., Ouma, J.H., Vennervald, B.J. and Dunne, D.W. (2004) Cytokine Production in Whole Blood Cultures from a Fishing Community in an Area of Highendemicity for Schistosoma mansoni in Uganda: The Differential Effect of Parasite Worm and Egg Antigens. Infection and Immunity, 72, 728-734. https://doi.org/10.1128/IAI.72.2.728-734.2004
Ribeiro de Jesus, A., Araújo, I., Bacellar, O., Magalhães, A., Pearce, E., Harn, D., Strand, M. and Carvalho, E.M. (2000) Human Immune Responses to Schistosoma mansoni Vaccine Candidate Antigens. American Society for Microbiology. Infection and Immunity, 68, 2797-2803.
Henderson, G.S., Lu, X., McCurley, T.L. and Colley, D.G. (1992) In Vivo Molecular Analysis of Lymphokines Involved in the Murine Immune Response during Schistosoma mansoni Infection. II. Quantification of IL-4 mRNA, IFN-g mRNA, and IL-2 mRNA Levels in the Granulomatous Livers, Mesenteric Lymph Nodes, and Spleens during the Course of Modulation. The Journal of Immunology, 148, 855-860.
Cook, G.A., Metwali, A., Blum, A., Mathew, R. and Weinstock, J.V. (1993) Lymphokine Expression in Granulomas of Schistosoma mansoni-Infected Mice. Cellular Immunology, 152, 49. https://doi.org/10.1006/cimm.1993.1266
Zhu, Y., Lukacs, N.W. and Boros, D.L. (1994) Cloning of Th0 and Th2 Type Helper Lymphocytes form Liver Granulomas of Schistosoma mansoni-Infected Mice. Infection and Immunity, 62, 994.
Chikunguwo, S.M., Kanazawa, T., Dayal, Y. and Stadecker, M.J. (1991) The Cell-Mediated Response to Schistosomal Antigens at the Clonal Level. The Journal of Immunology, 147, 3921.
Wynn, T.A. and Cheever, A.W. (1995) Cytokine Regulation of Granuloma Formation in Schistosomiasis. Current Opinion in Immunology, 7, 505.
Wynn, T.A., Eltoum, I., Cheever, A.W., Lewis, F.A., Gause, W.C. and Sher, A. (1993) Analysis of Cytokine mRNA Expression during Primary Granuloma Formation Induced by Eggs of Schistosoma mansoni. The Journal of Immunology, 151, 1430.
Pearce, E.J., Casper, P., Grzych, J.-M., Lewis, F.A. and Sher, A. (1991) Downregulation of TH1 Cytokine Production Accompanies Induction of TH2 Responses by a Parasitic Helminth, Schistosoma mansoni. The Journal of Experimental Medicine, 173, 159-166. https://doi.org/10.1084/jem.173.1.159
Kamal, S.M. and Khalifa, K.E.S. (2006) Immune Modulation by Helminthic Infections: Worms and Viral Infections. Parasite Immunology, 28, 483-496. https://doi.org/10.1111/j.1365-3024.2006.00909.x
Mayer, G. and Nylandat, J. (2016) Cell-Mediated Immunity: Cell-Cell Interactions in Specific Immune Responses. Immunology-Chapter Twelve. University of South Carolina School of Medicine, Columbia.
Vector Control Division (2009) The Countrywide Surveillance on the Intestinal Helthminths and Malaria Distribution in Uganda. Ministry of Health.
National Population Census Report (2014) Population by District, Sex, Residence and Population Type, Uganda, 2014. Daily Monitor Publication, Wednesday November 19 2014. www.monitor.co.ug
Mulago Hospital (2006) Standard Operating Procedures: Protocol Manual for Sample Collection in the Clinical Laboratories of Mulago Hospital, Uganda. (Unpublished)
Carneiro, T.R., Pinheiro, M.C., de Olveira, S.M., Hanemann, A.L., Queiroz, J.A. and Bezarra, F.S. (2012) Increased Detection of Schistosomiasis with Kato Katz and Swap-IgG Elisa in a Northeastern Brazil Low-Intensity Transmission Area. Revista da Sociedade Brasileira de Medicina Tropical, 45, 510-513. https://doi.org/10.1590/S0037-86822012000400019
Xu, B., Feng, Z., Xu, X.J. and Hu, W. (2011) Evaluation of Kato Katz Technique Combined with Stool Hatching Test in Diagnosis of Schistosomiasis Japonica. Chinese Journal of Schistosomiasis Control, 23, 321-323.
Tankeshwar, A. (2016) Kato Katz Technique: Principle, Procedure and Results.
Rapid Medical Diagnostic (2015) Urine CCA Test for Schistosomiasis (Bilharzia) Manual. Rapid Medical Diagnostic. EN ISO 13485/07.03 CE CK2002/064368/23. www.rapid-diagnostics.com
Norgan, A.P., Arguello, H.E., Sloan, L.M., Fernholz, E.C. and Pritt, B.S. (2013) A Method for Reducing the Sloughing of Thick Blood Films for Malaria Diagnosis. Malaria Journal, 12, 231. https://doi.org/10.1186/1475-2875-12-231
University of Thessaly (2012) Malaria Laboratory Diagnosis Intergraded Surveillance and Control Programme for West Nile Virus and Malaria in Greece. Laboratory of Hygiene and Epidemiology School of Health Sciences Faculty of Medicine, University of Thessaly, Thessaly.
Center for Disease Control (2013) Diagnostic Procedure for Laboratory Identification of Parasitic Diseases of Public Health Concern. Global Health Division of Parasitic Diseases and Malaria. Centers for Disease Control and Prevention, Atlanta.
Makerere University (2012) Standard Operating Procedures: Protocol for Peripheral Blood Mononuclear Cells (PBMCs) Isolation and Thawing. Version 3, Immunology Laboratory of College of Health Sciences, Makerere University, Kampala. (Unpublished)
Stevenson, M.M. and Riley, M.E. (2004) Innate Immunity to Malaria. Nature Reviews Immunology, 4, 169-180. https://doi.org/10.1038/nri1311
Stothard, J.R., Sousa-Figuereido, J.C., Betson, M., Adriko, M., Arinaitwe, M., et al. (2011) Schistosoma Mansoni Infections in Young Children: When Are Schistosome Antigens in Urine, Eggs in Stool and Antibodies to Eggs First Detectable? PLOS Neglected Tropical Diseases, 5, e938. https://doi.org/10.1371/journal.pntd.0000938
Doumbo, S., Tran, T.M., Sangala, J., Li, S., Doumtabe, D., Kone, Y., Abdrahamane, T., Bathily, A., Sogoba, N., Coulibaly, M.E., Huang, C.-Y., Ongoiba, A., Kayentao, K. and Traore, B. (2014) Co-Infection of Long-Term Carriers of Plasmodium falciparum with Schistosomahaematobium Enhances Protection from Febrile Malaria: A Prospective Cohort Study in Mali. PLOS Neglected Tropical Diseases, 8, e3154. https://doi.org/10.1371/journal.pntd.0003154
Picquet, M., Ernould, J.C., Vercruysse, J., Southgate, V.R., Mbaye, A., et al. (1996) Royal Society of Tropical Medicine and Hygiene meeting at Manson House, London, 18 May 1995. The Epidemiology of Human Schistosomiasis in the Senegal River Basin. Transactions of the Royal Society of Tropical Medicine and Hygiene, 90, 340-346.
Nacher, M. (2001) Malaria Vaccine Trials in a Wormy World. Trends in Parasitology, 17, 563-565.
Hartgers, F.C., Obeng, B.B., Boakye, D. and Yazdanbakhsh, M. (2008) Immune Responses during Helminth-Malaria Co-Infection: A Pilot Study in Ghanaian School Children. Parasitology, 135, 855-860. https://doi.org/10.1017/S0031182008000401
Taylor-Robinson, A.W. (1998) Immunoregulation of Malarial Infection: Balancing the Vices and Virtues. International Journal for Parasitology, 28, 135-148.