Evaluation of Malaria Urban Risk Using an Immuno-Epidemiological Biomarker of Human Exposure to Anopheles Bites

Dipomin F. Traoré Institut Pierre Richet (IPR), Institut Nationale de la Santé Publique (INSP), Bouaké, Côte d’Ivoire;
Institut de Recherche pour le Développement (IRD), Maladies Infectieuses et Vecteurs: Ecologie, Génétique, Evolution et Contrôle (MIVEGEC), UMR IRD.224-CNRS.5290, Université de Montpellier, Montpellier, France;
Unité de Formation et de Recherche des Sciences de la nature (UFR SN) Université Nangui Abrogoua, Abidjan, Côte d’Ivoire;

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André B. Sagna Institut Pierre Richet (IPR), Institut Nationale de la Santé Publique (INSP), Bouaké, Côte d’Ivoire;
Institut de Recherche pour le Développement (IRD), Maladies Infectieuses et Vecteurs: Ecologie, Génétique, Evolution et Contrôle (MIVEGEC), UMR IRD.224-CNRS.5290, Université de Montpellier, Montpellier, France;

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Akré M. Adja Institut Pierre Richet (IPR), Institut Nationale de la Santé Publique (INSP), Bouaké, Côte d’Ivoire;
Unité de Formation et de Recherche Biosciences (UFR Biosciences), Université Félix Houphouët Boigny, Abidjan, Côte d’Ivoire

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Dounin D. Zoh Institut Pierre Richet (IPR), Institut Nationale de la Santé Publique (INSP), Bouaké, Côte d’Ivoire;
Unité de Formation et de Recherche Biosciences (UFR Biosciences), Université Félix Houphouët Boigny, Abidjan, Côte d’Ivoire

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Kouassi N. Lingué Institut Pierre Richet (IPR), Institut Nationale de la Santé Publique (INSP), Bouaké, Côte d’Ivoire;

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Issa Coulibaly Institut Pierre Richet (IPR), Institut Nationale de la Santé Publique (INSP), Bouaké, Côte d’Ivoire;

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Bertin N’Cho Tchiekoi Institut Pierre Richet (IPR), Institut Nationale de la Santé Publique (INSP), Bouaké, Côte d’Ivoire;

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Serge B. Assi Institut Pierre Richet (IPR), Institut Nationale de la Santé Publique (INSP), Bouaké, Côte d’Ivoire;

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Anne Poinsignon Institut Pierre Richet (IPR), Institut Nationale de la Santé Publique (INSP), Bouaké, Côte d’Ivoire;
Institut de Recherche pour le Développement (IRD), Maladies Infectieuses et Vecteurs: Ecologie, Génétique, Evolution et Contrôle (MIVEGEC), UMR IRD.224-CNRS.5290, Université de Montpellier, Montpellier, France;

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Mamadou Dagnogo Unité de Formation et de Recherche des Sciences de la nature (UFR SN) Université Nangui Abrogoua, Abidjan, Côte d’Ivoire;

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Franck Remoue Institut Pierre Richet (IPR), Institut Nationale de la Santé Publique (INSP), Bouaké, Côte d’Ivoire;
Institut de Recherche pour le Développement (IRD), Maladies Infectieuses et Vecteurs: Ecologie, Génétique, Evolution et Contrôle (MIVEGEC), UMR IRD.224-CNRS.5290, Université de Montpellier, Montpellier, France;

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Urban malaria is an underestimated serious health concern in African countries. This study aimed to evaluate the risk of malaria transmission in an urban area by evaluating the level of human exposure to Anopheles bites using an Anopheles salivary biomarker (gambiae Salivary Gland Protein-6 peptide 1 [gSG6-P1] peptide). Two multidisciplinary cross-sectional studies were undertaken in five sites of Bouaké city (three urban districts and two surrounding villages, used as control; Côte d’Ivoire) during the rainy season and the dry season. Blood samples were obtained from children 6 months to 14 years of age for immunological tests. The level of anti-gSG6-P1 immunoglobulin G (IgG) antibodies was significantly higher in the rainy season than the dry season in both urban and rural sites (P < 0.0001). Interestingly, children with the highest anti-gSG6-P1 IgG responses in the rainy season were infected by Plasmodium falciparum. Surprisingly, no difference of anti-gSG6-P1 IgG level was observed between urban and rural areas, for either season. The current data suggest that children in the urban city of Bouaké could be as highly exposed to Anopheles bites as children living in surrounding villages. The immunological biomarker of human exposure to Anopheles bites may be used to accurately assess the potential risk of malaria transmission in African urban settings.

Author Notes

Address correspondence to Dipomin F. Traoré, Institut Pierre Richet (IPR), Institut Nationale de la Santé Publique (INSP), Bouaké, Côte d’Ivoire, Institut de Recherche pour le Développement (IRD), Maladies Infectieuses et Vecteurs: Ecologie, Génétique, Evolution et Contrôle (MIVEGEC), UMR IRD.224-CNRS.5290, Université de Montpellier, Montpellier, France and Unite de Formation et de Recherche des Sciences de la nature (UFR SN) Universite Nangui Abrogoua, Abidjan, Cote d’Ivoire. E-mail: francois-dipomin.traore@ird.fr

Financial support: This research was integrated into the “Jeune Equipe Associée à l’IRD” EVAPAL-CI multidisciplinary study funded by the IRD (Institut de Recherche pour le Développement; Département des Programmes de Recherche et de la Formation au Sud; convention of February 18, 2013). D. F. Traore and D. D. Zoh were supported by PhD fellowships provided by the IRD (Département des Programmes de Formation au Sud) and A. B. Sagna by a fellowship provided by the “Méditeranée Infection” Foundation (Marseille, France).

Authors’ addresses: Dipomin F. Traoré, Institut Pierre Richet (IPR), Institut Nationale de la Santé Publique (INSP), Bouaké, Côte d’Ivoire, Institut de Recherche pour le Développement (IRD), Maladies Infectieuses et Vecteurs: Ecologie, Génétique, Evolution et Contrôle (MIVEGEC), UMR IRD.224-CNRS.5290, Université de Montpellier, Montpellier, France, and Unité de Formation et de Recherche des Sciences de la nature (UFR SN) Université Nangui Abrogoua, Abidjan, Côte d’Ivoire, E-mail: francois-dipomin.traore@ird.fr. André B. Sagna, Anne Poinsignon, and Franck Remoue, Institut Pierre Richet (IPR), Institut Nationale de la Santé Publique (INSP), Bouaké, Côte d’Ivoire, and Institut de Recherche pour le Développement (IRD), Maladies Infectieuses et Vecteurs: Ecologie, Génétique, Evolution et Contrôle (MIVEGEC), UMR IRD.224-CNRS.5290, Université de Montpellier, Montpellier, France, E-mails: sagna.ab@gmail.com, anne.poinsignon@ird.fr, and franck.remoue@ird.fr. Akré M. Adja and Dounin D. Zoh, Institut Pierre Richet (IPR), Institut Nationale de la Santé Publique (INSP), Bouaké, Côte d’Ivoire, and Unité de Formation et de Recherche Biosciences (UFR Biosciences), Université Félix Houphouët Boigny, Abidjan, Côte d’Ivoire, E-mails: adjamaurice@yahoo.fr and zohdounin@yahoo.fr. Kouassi N. Lingué, Issa Coulibaly, Bertin N’Cho Tchiekoi, and Serge B. Assi, Institut Pierre Richet (IPR), Institut Nationale de la Santé Publique (INSP), Bouaké, Côte d’Ivoire, E-mails: linguek@yahoo.fr, coulibalyissadocta@gmail.com, tchiekoi@yahoo.fr, and assisergi@yahoo.fr. Mamadou Dagnogo, Unité de Formation et de Recherche des Sciences de la nature (UFR SN) Université Nangui Abrogoua, Abidjan, Côte d’Ivoire, E-mail: mdagnogo2017@gmail.com.

  • 1.

    OMS, 2016. Paludisme Aide-mémoire 94. Available at: http://cdrwww.who.int/mediacentre/factsheets/fs094/fr/. Accessed July 15, 2016.

    • PubMed
    • Export Citation
  • 2.

    Pages F, Orlandi-Pradines E, Corbelc V, 2007. Vectors of malaria: biology, diversity, prevention, and individual protection. Med Mal Infect 37: 153161.

  • 3.

    United Nations Department of Economic and Social Affairs, 2008. World Urbanization Prospects: The 2007 Revision (Highlights), ESA/P/WP/205 (New York). Available at: https://selectra.co.uk/sites/selectra.co.uk/files/pdf/2007WUP_Highlights_web.pdf. Accessed July 15, 2016.

    • PubMed
    • Export Citation
  • 4.

    OMS, 2009. Bidonvilles, changement climatique et santé humaine en Afrique sub-saharienne. Bull World Health Organ 87: 886.

  • 5.

    Martens P, Hall L, 2000. Malaria on the move: human population movement and malaria transmission. Emerg Infect Dis 6: 103109.

  • 6.

    Byrne N, 2007. Urban malaria risk in sub-Saharan Africa: where is the evidence? Travel Med Infect Dis 5: 135137.

  • 7.

    Robert V, Macintyre K, Keating J, Trape JF, Duchemin JB, Warren M, Beier JC, 2003. Malaria transmission in urban sub-Saharan Africa. Am J Trop Med Hyg 68: 169176.

  • 8.

    Coluzzi M, Sabatini A, Petrarca V, Deco MA, 1979. Chromosomal differentiation and adaptation to human environments in the Anopheles gambiae complex. Trans R Soc Trop Med Hyg 73: 483497.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 9.

    Carnevale P, Robert V, Le Goff G, Etienne F, Manga L, Agogbeto M, Chippaux JP, Mouchet J, 1993. Données entomologiques sur le paludisme urbain en Afrique tropicale. Cahier Santé 3: 239245.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 10.

    Hay SI, Guerra CA, Tatem AJ, Atkinson PM, Snow RW, 2005. Urbanization, malaria transmission and disease burden in Africa. Nat Rev Microbiol 3: 8190.

  • 11.

    Adja AM, N’Goran KE, Kengne P, Koudou GB, Toure M, Koffi AA, Tia E, Fontenille D, Chandre F, 2006. Tranmission vectorielle du paludisme en savane arborée à Gansé en Côte d’Ivoire. Med Trop 66: 445449.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 12.

    Betsi NA, Koudou BG, Cissé G, Tschannen AB, Pignol AM, Ouattara Y, Madougou M, Tanner M, Utzinger J, 2007. Effect of an armed conflict on human resources and health systems in Côte d’Ivoire. Trop Med Int Health 8: 903906.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 13.

    Chouaibou M, Simard F, Chandre F, Etang J, Darriet F, Hougard JM, 2006. Efficacy of bifenthrin-impregnated bednets against Anopheles funestus and pyrethroid-resistant Anopheles gambiae in north Cameroon. Malar J 5: 77.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 14.

    Govella NJ, Chaki PP, Geissbuhler Y, Kannady K, Okumu F, Charlwood JD, Anderson RA, Killeen GF, 2009. A new tent trap for sampling exophagic and endophagic members of the Anopheles gambiae complex. Malar J 8: 157.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 15.

    Mboera LE, 2005. Sampling techniques for adult Afrotropical malaria vectors and their reliability in the estimation of entomological inoculation rate. Tanzan Health Res Bull 3: 117124.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 16.

    Smith T, Killeen G, Lengeler C, Tanner M, 2004. Relationships between the outcome of Plasmodium falciparum infection and the intensity of transmission in Africa. Am J Trop Med Hyg 71: 8086.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 17.

    Remoue F, Cornelie S, Ngom A, Boulanger D, Simondon F, 2005. Immune responses to arthropod bites during vector-borne diseases. Garraud O, ed. Update in Tropical Immunology. Kerala, India: Transworld Research Network, 377400.

    • PubMed
    • Export Citation
  • 18.

    Schwartz B, Ribeiro J, Goldstein M, 1990. Anti-tick antibodies: an epidemiologic tool in Lyme disease research. Am J Epidemiol 132: 5866.

  • 19.

    Poinsignon A et al. 2008. Novel peptide marker corresponding to salivary protein gSG6 potentially identifies exposure to Anopheles bites. PLoS One 3: e2472.

  • 20.

    Drame PM et al. 2012. IgG responses to the gSG6-P1 salivary peptide for evaluating human exposure to Anopheles bites in urban areas of Dakar region, Senegal. Malar J 11: 72.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 21.

    Drame PM, Diallo A, Poinsignon A, Boussari O, Dos Santos S, Machault V, Lalou R, Cornelie S, LeHesran JY, Remoue F, 2013. Evaluation of the effectiveness of malaria vector control measures in urban settings of Dakar by a specific Anopheles salivary biomarker. PLoS One 8: e66354.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 22.

    Dossou-Yovo J, Doannio JMC, Diarrassouba S, Chauvancy G, 1998. Impact d’aménagements de rizières sur la transmission du paludisme dans la ville de Bouaké, Côte d’Ivoire. Bull Soc Pathol Exot 91: 327333.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 23.

    Kouassi AM, Kouamé KF, Koffi YB, Dje BK, Paturel JE, Oulare S, 2010. Analysis Of Climate Variability And Its Influences On Seasonal Rainfall Patterns In West Africa: The Case Of The Watershed Of N’zi (Bandama) In Ivory Coast. Cybergeo: European Journal of Geography, Environment, Nature, Landscape, Document 513. Available at: https://cybergeo.revues.org/23388. Accessed February 9, 2017.

    • PubMed
    • Export Citation
  • 24.

    Gillies M, Coetzee M, 1987. A Supplement to the Anophelinae of Africa South of the Sahara (Afrotropical Region), No. 55. Johannesburg, South Africa: The South African Institute for Medical Research.

    • PubMed
    • Export Citation
  • 25.

    Sagna AB et al. 2013. Plasmodium falciparum infection during dry season: IgG responses to Anopheles gambiae salivary gSG6-P1 peptide as sensitive biomarker for malaria risk in northern Senegal. Malar J 12: 301.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 26.

    Robert V, Carnevale P, 1984. Les vecteurs des paludismes en Afrique subsaharienne. Etudes Médicales 2: 7990.

  • 27.

    Robert V, Carnevale P, Ouedraogo V, Petrarca V, Coluzzi M, 1988. La transmission du paludisme humain dans un village de savane du Sud-Ouest du Burkina Faso. Ann Soc Belg Med Trop 68: 107121.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 28.

    Dossou-Yovo J, Doannio JMC, Diarrassouba S, Chauvancy G, 1998. Impact d’aménagements de rizières sur la transmission du paludisme dans la ville de Bouaké, Côte d’Ivoire. Bull Soc Pathol Exot 91: 327333.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 29.

    Poinsignon A, Cornelie S, Ba F, Boulanger D, Sow C, Rossignol M, Sokhna C, Cisse B, Simondon F, Remoue F, 2009. Human IgG response to a salivary peptide, gSG6-P1, as a new immuno-epidemiological tool for evaluating low-level exposure to Anopheles bites. Malar J 8: 198.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 30.

    Poinsignon A et al. 2010. First attempt to validate the gSG6-P1 salivary peptide as an immuno-epidemiological tool for evaluating human exposure to Anopheles funestus bites. Trop Med Int Health 15: 11981203.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 31.

    Londono-Renteria B et al. 2015. An. gambiae gSG6-P1 evaluation as a proxy for human-vector contact in the Americas: a pilot study. Parasit Vectors 8: 533.

  • 32.

    Dye C, Hasibeder G, 1986. Population dynamics of mosquito-borne disease: effects of flies which bite some people more frequently than others. Trans R Soc Trop Med Hyg 80: 6977.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 33.

    Takken W, Knols BG, 1999. Odor-mediated behavior of Afrotropical malaria mosquitoes. Annu Rev Entomol 44: 131157.

  • 34.

    Qui YT, Smallegange RC, Van Lool JJA, Ter Braak CJF, Takken W, 2006. Interindividual variation in the attractiveness of human odours to the malaria mosquito Anopheles gambiae s.s. Med Vet Entomol 20: 280287.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 35.

    Sagna AB et al. 2013. gSG6-P1 salivary biomarker discriminates micro-geographical heterogeneity of human exposure to Anopheles bites in low and seasonal malaria areas. Parasit Vectors 6: 68.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 36.

    Drame PM et al. 2010. Human antibody responses to the Anopheles salivary gSG6-P1 peptide: a novel tool for evaluating the efficacy of ITNs in malaria vector control. PLoS One 5: e15596.

    • PubMed
    • Search Google Scholar
    • Export Citation
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