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Age-Stratified Profiles of Serum IL-6, IL-10, and TNF-α Cytokines Among Kenyan Children with Schistosoma haematobium, Plasmodium falciparum, and Other Chronic Parasitic Co-Infections

Amaya L. BustinduyCenter for Global Health and Diseases, Case Western Reserve University School of Medicine, Cleveland, Ohio; Institute of Immunity and Infection, St. George's University of London, London, United Kingdom; Division of Vector Borne and Neglected Tropical Diseases, Ministry of Public Health and Sanitation, Nairobi, Kenya; Department of Environmental Sciences, Emory University, Atlanta, Georgia

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Laura J. SutherlandCenter for Global Health and Diseases, Case Western Reserve University School of Medicine, Cleveland, Ohio; Institute of Immunity and Infection, St. George's University of London, London, United Kingdom; Division of Vector Borne and Neglected Tropical Diseases, Ministry of Public Health and Sanitation, Nairobi, Kenya; Department of Environmental Sciences, Emory University, Atlanta, Georgia

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Alicia Chang-CojulunCenter for Global Health and Diseases, Case Western Reserve University School of Medicine, Cleveland, Ohio; Institute of Immunity and Infection, St. George's University of London, London, United Kingdom; Division of Vector Borne and Neglected Tropical Diseases, Ministry of Public Health and Sanitation, Nairobi, Kenya; Department of Environmental Sciences, Emory University, Atlanta, Georgia

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Indu MalhotraCenter for Global Health and Diseases, Case Western Reserve University School of Medicine, Cleveland, Ohio; Institute of Immunity and Infection, St. George's University of London, London, United Kingdom; Division of Vector Borne and Neglected Tropical Diseases, Ministry of Public Health and Sanitation, Nairobi, Kenya; Department of Environmental Sciences, Emory University, Atlanta, Georgia

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Adam S. DuVallCenter for Global Health and Diseases, Case Western Reserve University School of Medicine, Cleveland, Ohio; Institute of Immunity and Infection, St. George's University of London, London, United Kingdom; Division of Vector Borne and Neglected Tropical Diseases, Ministry of Public Health and Sanitation, Nairobi, Kenya; Department of Environmental Sciences, Emory University, Atlanta, Georgia

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Jessica K. FairleyCenter for Global Health and Diseases, Case Western Reserve University School of Medicine, Cleveland, Ohio; Institute of Immunity and Infection, St. George's University of London, London, United Kingdom; Division of Vector Borne and Neglected Tropical Diseases, Ministry of Public Health and Sanitation, Nairobi, Kenya; Department of Environmental Sciences, Emory University, Atlanta, Georgia

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Peter L. MungaiCenter for Global Health and Diseases, Case Western Reserve University School of Medicine, Cleveland, Ohio; Institute of Immunity and Infection, St. George's University of London, London, United Kingdom; Division of Vector Borne and Neglected Tropical Diseases, Ministry of Public Health and Sanitation, Nairobi, Kenya; Department of Environmental Sciences, Emory University, Atlanta, Georgia

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Eric M. MuchiriCenter for Global Health and Diseases, Case Western Reserve University School of Medicine, Cleveland, Ohio; Institute of Immunity and Infection, St. George's University of London, London, United Kingdom; Division of Vector Borne and Neglected Tropical Diseases, Ministry of Public Health and Sanitation, Nairobi, Kenya; Department of Environmental Sciences, Emory University, Atlanta, Georgia

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Francis M. MutukuCenter for Global Health and Diseases, Case Western Reserve University School of Medicine, Cleveland, Ohio; Institute of Immunity and Infection, St. George's University of London, London, United Kingdom; Division of Vector Borne and Neglected Tropical Diseases, Ministry of Public Health and Sanitation, Nairobi, Kenya; Department of Environmental Sciences, Emory University, Atlanta, Georgia

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Uriel KitronCenter for Global Health and Diseases, Case Western Reserve University School of Medicine, Cleveland, Ohio; Institute of Immunity and Infection, St. George's University of London, London, United Kingdom; Division of Vector Borne and Neglected Tropical Diseases, Ministry of Public Health and Sanitation, Nairobi, Kenya; Department of Environmental Sciences, Emory University, Atlanta, Georgia

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Charles H. KingCenter for Global Health and Diseases, Case Western Reserve University School of Medicine, Cleveland, Ohio; Institute of Immunity and Infection, St. George's University of London, London, United Kingdom; Division of Vector Borne and Neglected Tropical Diseases, Ministry of Public Health and Sanitation, Nairobi, Kenya; Department of Environmental Sciences, Emory University, Atlanta, Georgia

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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.

Author Notes

* Address correspondence to Amaya L. Bustinduy, Pembroke Place, Liverpool, L3 5QA, United Kingdom. E-mails: Amaya.Bustinduy@doctors.org.uk or bustinji06@gmail.com

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.

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