Urogenital Schistosomiasis Is Associated with an Increased Risk of Plasmodium falciparum Infection in Burkina Faso

Mireille Ouedraogo Department of Translational Research in Medicine and Surgery, University of Pisa, Pisa, Italy;
Department of Public Health and Infectious Diseases, University of Rome La Sapienza, Rome, Italy;
Centre National de Recherche et Formation sur le Paludisme, Ouagadougou, Burkina Faso;

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Pytsje T. Hoekstra Leiden University Center for Infectious Diseases, Leiden University Medical Centre, Leiden, The Netherlands;

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Youssouf Kabore Centre National de Recherche et Formation sur le Paludisme, Ouagadougou, Burkina Faso;

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Issa Nebie Centre National de Recherche et Formation sur le Paludisme, Ouagadougou, Burkina Faso;

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Stan Hilt Leiden University Center for Infectious Diseases, Leiden University Medical Centre, Leiden, The Netherlands;

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Govert J. van Dam Leiden University Center for Infectious Diseases, Leiden University Medical Centre, Leiden, The Netherlands;

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Paul L. A. M. Corstjens Department of Cell & Chemical Biology, Leiden University Medical Center, Leiden, The Netherlands

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Fabrizio Bruschi Department of Translational Research in Medicine and Surgery, University of Pisa, Pisa, Italy;

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David Modiano Department of Public Health and Infectious Diseases, University of Rome La Sapienza, Rome, Italy;

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Valentina D. Mangano Department of Translational Research in Medicine and Surgery, University of Pisa, Pisa, Italy;

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There is significant overlap in the global distribution of malaria and neglected tropical diseases, with the largest health burden in Sub-Saharan Africa, where areas are co-endemic for malaria and schistosomiasis, soil-transmitted helminths, or lymphatic filariasis. Some studies suggest that helminth infections may increase susceptibility to malaria, but evidence is limited. This study investigated the association between urogenital schistosomiasis and the risk of Plasmodium falciparum (P. falciparum) parasitemia in rural Burkina Faso. A cohort of 424 subjects participated in five cross-sectional malaria surveys. Active Schistosoma hematobium infection was diagnosed at baseline using plasma circulating anodic antigen detection, whereas P. falciparum infection was diagnosed at each survey via blood smear microscopy. Longitudinal analysis assessed the association between baseline urogenital schistosomiasis and P. falciparum parasitemia over time, adjusting for sex, age, village, ethnicity, and hemoglobin genotype. Subjects with active urogenital schistosomiasis had a ∼ 25% increase in the cumulative incidence of P. falciparum infection (incidence rate ratio [IRR] = 1.26; 95% CI = 1.08–1.46; P = 0.004), as well as a nonsignificant trend toward higher parasite density (exponential of the β coefficient [Expβ] = 1.12; 95% CI = 0.96–1.31; P = 0.133) and higher odds of infection over five surveys (odds ratio [OR] = 1.79; 95% CI = 0.89–3.59; P = 0.104). Higher intensity of schistosomiasis increased the cumulative incidence of P. falciparum (IRR = 1.12; 95% CI = 1.05–1.19; P = 0.001) and parasite density (Expβ = 1.08; 95% CI = 1.01–1.15; P = 0.026), and a trend toward increased odds of infection was also observed (OR = 1.28; 95% CI = 0.91–1.80; P = 0.159). This study provides longitudinal evidence that urogenital schistosomiasis is associated with an increased risk of P. falciparum parasitaemia, highlighting the need for integrated control strategies for both diseases, particularly in school-aged children and adolescents.

Author Notes

Financial support: This study was supported by a research grant from Sapienza University of Rome (Fondi di Ateneo) to David Modiano and by funds from the PhD School in Microbiology, Infectious Diseases, and Public Health, Sapienza University of Rome, to M. Ouedraogo.

Disclosures: Study subjects or their guardians provided written informed consent for participation. The original malaria epidemiological study received approval from the ethical committee of the Ministry of Health of Burkina Faso (2007–048). The use of archived plasma samples for schistosomiasis research received additional approval from the ethical committee of the Ministry of Health and Public Hygiene of Burkina Faso (2022-05-15).

Authors’ contributions: M. Ouedraogo., P. T. Hoekstra., and S. Hilt conducted the experiments. Y. Kabore. and I. Nebie. coordinated the cross-sectional survey. G. J. van Dam, P. L. A. M. Corstjens, F. Bruschi, D. Modiano, and V. D. Mangano designed experiments and contributed experimental resources. D. Modiano and V. D. Mangano designed the study. V. D. Mangano performed the data analyses and wrote the manuscript. All authors revised and approved the final version of the manuscript.

Current contact information: Mireille Ouedraogo, Youssouf Kabore, and Issa Nebie, Centre National de Recherche et Formation sur le Paludisme, Ouagadougou, Burkina Faso, E-mails: omireille@ymail.com, kabyouf@yahoo.fr, and i.ouedraogo@gras.bf. Pytsje T. Hoekstra, Stan Hilt, and Govert J. van Dam, Leiden University Center for Infectious Diseases, Leiden University Medical Centre, Leiden, The Netherlands, E-mails: p.t.hoekstra-mevius@lumc.nl, s.t.hilt@lumc.nl, and g.j.van_dam@lumc.nl. Paul L. A. M. Corstjens, Department of Cell & Chemical Biology, Leiden University Medical Center, Leiden, The Netherlands, E-mail: p.l.a.m.cortjens@lumc.nl. Fabrizio Bruschi and Valentina D. Mangano, Department of Translational Research in Medicine and Surgery, University of Pisa, Pisa, Italy, E-mails: fabrizio.bruschi@unipi.it and valentina.mangano@unipi.it. David Modiano, Department of Public Health and Infectious Diseases, University of Rome La Sapienza, Rome, Italy, E-mail: david.modiano@uniroma1.it.

Address correspondence to Valentina D. Mangano, Department of Translational Research in Medicine and Surgery, University of Pisa, via Savi 10, 56126 Pisa, Italy. E-mail: valentina.mangano@unipi.it
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