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Published in: Malaria Journal 1/2016

Open Access 01-12-2016 | Research

Epidemiological and entomological studies of a malaria outbreak among French armed forces deployed at illegal gold mining sites reveal new aspects of the disease’s transmission in French Guiana

Authors: Vincent Pommier de Santi, Romain Girod, Marie Mura, Aissata Dia, Sébastien Briolant, Félix Djossou, Isabelle Dusfour, Alexandre Mendibil, Fabrice Simon, Xavier Deparis, Frédéric Pagès

Published in: Malaria Journal | Issue 1/2016

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Abstract

Background

In December 2010, a Plasmodium vivax malaria outbreak occurred among French forces involved in a mission to control illegal gold mining in French Guiana. The findings of epidemiological and entomological investigations conducted after this outbreak are presented here.

Methods

Data related to malaria cases reported to the French armed forces epidemiological surveillance system were collected during the epidemic period from December 2010 to April 2011. A retrospective cohort study was conducted to identify presumed contamination sites. Anopheles mosquitoes were sampled at the identified sites using Mosquito Magnet and CDC light traps. Specimens were identified morphologically and confirmed using molecular methods (sequencing of ITS2 gene and/or barcoding). Anopheles infections with Plasmodium falciparum and P. vivax were tested by both enzyme-linked immunosorbent assay and real-time PCR.

Results

Seventy-two P. vivax malaria cases were reported (three were mixed P. falciparum/P. vivax infections), leading to a global attack rate of 26.5 % (72/272). Lack of compliance with vector control measures and doxycycline chemoprophylaxis was reported by patients. Two illegal gold mining sites located in remote areas in the primary forest were identified as places of contamination. In all, 595 Anopheles females were caught and 528 specimens were formally identified: 305 Anopheles darlingi, 145 Anopheles nuneztovari s.l., 63 Anopheles marajoara and 15 Anopheles triannulatus s.l. Three An. darlingi were infected by P. falciparum (infection rate: 1.1 %) and four An. marajoara by P. vivax (infection rate: 6.4 %).

Discussion

The main drivers of the outbreak were the lack of adherence by military personnel to malaria prevention measures and the high level of malaria transmission at illegal gold mining sites. Anopheles marajoara was clearly implicated in malaria transmission for the first time in French Guiana. The high infection rates observed confirm that illegal gold mining sites must be considered as high level malaria transmission areas in the territory.

Conclusions

Illegal gold mining activities are challenging the control of malaria in French Guiana. Collaboration with neighbouring countries is necessary to take into account mobile populations such as gold miners. Malaria control strategies in the French armed forces must be adapted to P. vivax malaria and sylvatic Anopheles species.
Literature
2.
go back to reference Chocho A, Bellony S, Azor P, Chantilly S. Lieux présumés de contamination palustre répertoriés sur le littoral de la Guyane - 2009. Bull Veille Sanitaire Antilles-Guyane. 2011;1:6–10. Chocho A, Bellony S, Azor P, Chantilly S. Lieux présumés de contamination palustre répertoriés sur le littoral de la Guyane - 2009. Bull Veille Sanitaire Antilles-Guyane. 2011;1:6–10.
3.
go back to reference Ardillon V, Carvalho L, Prince C, Abboud P, Djossou F. Bilans 2013 et 2014 de la situation du paludisme en Guyane. Bull Veille Sanitaire Antilles-Guyane. 2015;1:16–20. Ardillon V, Carvalho L, Prince C, Abboud P, Djossou F. Bilans 2013 et 2014 de la situation du paludisme en Guyane. Bull Veille Sanitaire Antilles-Guyane. 2015;1:16–20.
6.
go back to reference Carme B, Ardillon V, Girod R, Grenier C, Joubert M, Djossou F, et al. Update on the epidemiology of malaria in French Guiana. Med Trop. 2009;69:19–25 (in French). Carme B, Ardillon V, Girod R, Grenier C, Joubert M, Djossou F, et al. Update on the epidemiology of malaria in French Guiana. Med Trop. 2009;69:19–25 (in French).
7.
go back to reference Musset L, Pelleau S, Girod R, Ardillon V, Carvalho L, Dusfour I, et al. Malaria on the Guiana Shield: a review of the situation in French Guiana. Mem Inst Oswaldo Cruz. 2014;109:522–33.CrossRef Musset L, Pelleau S, Girod R, Ardillon V, Carvalho L, Dusfour I, et al. Malaria on the Guiana Shield: a review of the situation in French Guiana. Mem Inst Oswaldo Cruz. 2014;109:522–33.CrossRef
10.
go back to reference Sawyer DR. Malaria on the Amazon frontier: economic and social aspects of transmission and control. Southeast Asian J Trop Med Public Health. 1986;17:342–5.PubMed Sawyer DR. Malaria on the Amazon frontier: economic and social aspects of transmission and control. Southeast Asian J Trop Med Public Health. 1986;17:342–5.PubMed
12.
go back to reference Spencer BR. Gold mining and malaria in the Brazilian Amazon. Masters thesis. New Haven:Yale University; 1996. Spencer BR. Gold mining and malaria in the Brazilian Amazon. Masters thesis. New Haven:Yale University; 1996.
13.
go back to reference Duarte EC, Fontes CJ. Association between reported annual gold mining extraction and incidence of malaria in Mato Grosso-Brazil, 1985–1996. Rev Soc Bras Med Trop. 2002;35:665–8.CrossRefPubMed Duarte EC, Fontes CJ. Association between reported annual gold mining extraction and incidence of malaria in Mato Grosso-Brazil, 1985–1996. Rev Soc Bras Med Trop. 2002;35:665–8.CrossRefPubMed
14.
go back to reference Barbieri AF, Sawyer DO. Heterogeneity of malaria prevalence in alluvial gold mining areas in Northern Mato Grosso State, Brazil. Cad Saude Publica. 2007;23:2878–86.CrossRefPubMed Barbieri AF, Sawyer DO. Heterogeneity of malaria prevalence in alluvial gold mining areas in Northern Mato Grosso State, Brazil. Cad Saude Publica. 2007;23:2878–86.CrossRefPubMed
15.
go back to reference Hiwat H, Issaly J, Gaborit P, Somai A, Samjhawan A, Sardjoe P, et al. Behavioral heterogeneity of Anopheles darlingi (Diptera: Culicidae) and malaria transmission dynamics along the Maroni River, Suriname, French Guiana. Trans R Soc Trop Med Hyg. 2010;104:207–13. doi:10.1016/j.trstmh.2009.07.007.CrossRefPubMed Hiwat H, Issaly J, Gaborit P, Somai A, Samjhawan A, Sardjoe P, et al. Behavioral heterogeneity of Anopheles darlingi (Diptera: Culicidae) and malaria transmission dynamics along the Maroni River, Suriname, French Guiana. Trans R Soc Trop Med Hyg. 2010;104:207–13. doi:10.​1016/​j.​trstmh.​2009.​07.​007.CrossRefPubMed
16.
go back to reference Girod R, Roux E, Berger F, Stefani A, Gaborit P, Carinci R, et al. Unravelling the relationships between Anopheles darlingi (Diptera: Culicidae) densities, environmental factors and malaria incidence: understanding the variable patterns of malarial transmission in French Guiana (South America). Ann Trop Med Parasitol. 2011;105:107–22. doi:10.1179/136485911X12899838683322.PubMedCentralCrossRefPubMed Girod R, Roux E, Berger F, Stefani A, Gaborit P, Carinci R, et al. Unravelling the relationships between Anopheles darlingi (Diptera: Culicidae) densities, environmental factors and malaria incidence: understanding the variable patterns of malarial transmission in French Guiana (South America). Ann Trop Med Parasitol. 2011;105:107–22. doi:10.​1179/​136485911X128998​38683322.PubMedCentralCrossRefPubMed
17.
go back to reference Girod R, Gaborit P, Carinci R, Issaly J, Fouque F. Anopheles darlingi bionomics and transmission of Plasmodium falciparum, Plasmodium vivax and Plasmodium malariae in Amerindian villages of the Upper-Maroni Amazonian forest, French Guiana. Mem Inst Oswaldo Cruz. 2008;103:702–10.CrossRefPubMed Girod R, Gaborit P, Carinci R, Issaly J, Fouque F. Anopheles darlingi bionomics and transmission of Plasmodium falciparum, Plasmodium vivax and Plasmodium malariae in Amerindian villages of the Upper-Maroni Amazonian forest, French Guiana. Mem Inst Oswaldo Cruz. 2008;103:702–10.CrossRefPubMed
18.
19.
go back to reference Tadei WP, Thatcher BD, Santos JM, Scarpassa VM, Rodrigues IB, Rafael MS. Ecologic observations on anopheline vectors of malaria in the Brazilian Amazon. Am J Trop Med Hyg. 1998;59:325–35.PubMed Tadei WP, Thatcher BD, Santos JM, Scarpassa VM, Rodrigues IB, Rafael MS. Ecologic observations on anopheline vectors of malaria in the Brazilian Amazon. Am J Trop Med Hyg. 1998;59:325–35.PubMed
20.
go back to reference Pajot FX, Le Pont F, Molez JF, Degallier N. Agressivité d’Anopheles (Nyssorhynchus) darlingi Root, 1926 (Diptera, Culicidae) en Guyane française. Cah ORSTOM SerEnt Med Parasitol. 1977;15:15–22. Pajot FX, Le Pont F, Molez JF, Degallier N. Agressivité d’Anopheles (Nyssorhynchus) darlingi Root, 1926 (Diptera, Culicidae) en Guyane française. Cah ORSTOM SerEnt Med Parasitol. 1977;15:15–22.
21.
go back to reference Lourenco-de-Oliveira R, Guimaraes AE, Arle M, da Silva TF, Castro MG, Motta MA, et al. Anopheline species, some of their habits and relation to malaria in endemic areas of Rondonia State, Amazon region of Brazil. Mem Inst Oswaldo Cruz. 1989;84:501–14.CrossRefPubMed Lourenco-de-Oliveira R, Guimaraes AE, Arle M, da Silva TF, Castro MG, Motta MA, et al. Anopheline species, some of their habits and relation to malaria in endemic areas of Rondonia State, Amazon region of Brazil. Mem Inst Oswaldo Cruz. 1989;84:501–14.CrossRefPubMed
22.
go back to reference de Barros FS, Honorio NA. Man biting rate seasonal variation of malaria vectors in Roraima, Brazil. Mem Inst Oswaldo Cruz. 2007;102:299–302.CrossRefPubMed de Barros FS, Honorio NA. Man biting rate seasonal variation of malaria vectors in Roraima, Brazil. Mem Inst Oswaldo Cruz. 2007;102:299–302.CrossRefPubMed
23.
go back to reference Molez JF. Myths concerning malarial transmission among Amazonian Indians and their relation with 2 types of transmission encountered in the Amazonian forest. Sante. 1999;9:157–62 (in French).PubMed Molez JF. Myths concerning malarial transmission among Amazonian Indians and their relation with 2 types of transmission encountered in the Amazonian forest. Sante. 1999;9:157–62 (in French).PubMed
24.
go back to reference de Oliveira-Ferreira J, Lourenco-de-Oliveira R, Teva A, Deane LM, Daniel-Ribeiro CT. Natural malaria infections in anophelines in Rondonia State, Brazilian Amazon. Am J Trop Med Hyg. 1990;43:6–10.PubMed de Oliveira-Ferreira J, Lourenco-de-Oliveira R, Teva A, Deane LM, Daniel-Ribeiro CT. Natural malaria infections in anophelines in Rondonia State, Brazilian Amazon. Am J Trop Med Hyg. 1990;43:6–10.PubMed
25.
go back to reference Dusfour I, Issaly J, Carinci R, Gaborit P, Girod R. Incrimination of Anopheles (Anopheles) intermedius Peryassu, An. (Nyssorhynchus) nuneztovari Gabaldon, An. (Nys.) oswaldoi Peryassu as natural vectors of Plasmodium falciparum in French Guiana. Mem Inst Oswaldo Cruz. 2012;107:429–32.CrossRefPubMed Dusfour I, Issaly J, Carinci R, Gaborit P, Girod R. Incrimination of Anopheles (Anopheles) intermedius Peryassu, An. (Nyssorhynchus) nuneztovari Gabaldon, An. (Nys.) oswaldoi Peryassu as natural vectors of Plasmodium falciparum in French Guiana. Mem Inst Oswaldo Cruz. 2012;107:429–32.CrossRefPubMed
26.
go back to reference Branquinho MS, Lagos CB, Rocha RM, Natal D, Barata JM, Cochrane AH, et al. Anophelines in the state of Acre, Brazil, infected with Plasmodium falciparum, P. vivax, the variant P. vivax VK247 and P. malariae. Trans R Soc Trop Med Hyg. 1993;87:391–4.CrossRefPubMed Branquinho MS, Lagos CB, Rocha RM, Natal D, Barata JM, Cochrane AH, et al. Anophelines in the state of Acre, Brazil, infected with Plasmodium falciparum, P. vivax, the variant P. vivax VK247 and P. malariae. Trans R Soc Trop Med Hyg. 1993;87:391–4.CrossRefPubMed
27.
go back to reference Pajot FX, Molez JF, Le Pont F. Anophèles et paludisme sur le haut Oyapock (Guyane française). Cah ORSTOM SerEnt Med Parasitol. 1978;16:105–11. Pajot FX, Molez JF, Le Pont F. Anophèles et paludisme sur le haut Oyapock (Guyane française). Cah ORSTOM SerEnt Med Parasitol. 1978;16:105–11.
30.
go back to reference Service MW. Mosquito ecology. New York: Wiley; 1976. Service MW. Mosquito ecology. New York: Wiley; 1976.
31.
go back to reference Shannon RC. Anophelines of the Amazon valley. Proc Entomol Soc Wash. 1933;35:117–43. Shannon RC. Anophelines of the Amazon valley. Proc Entomol Soc Wash. 1933;35:117–43.
32.
go back to reference Floch H, Abonnenc E. Anophèles de la Guyane Française. Arch Inst Pasteur Guyane. 1951;236:1–92. Floch H, Abonnenc E. Anophèles de la Guyane Française. Arch Inst Pasteur Guyane. 1951;236:1–92.
33.
go back to reference Fauran P, Pajot FX. Complement to the catalog of the Culidae Recorded from French Guiana (South America). Mosq News. 1974;6:99–110. Fauran P, Pajot FX. Complement to the catalog of the Culidae Recorded from French Guiana (South America). Mosq News. 1974;6:99–110.
34.
go back to reference Fauran P. Catalogue annoté des Culicidés signalés en Guyane Française. Arch Inst Pasteur Guyane. 1961;22:1–15. Fauran P. Catalogue annoté des Culicidés signalés en Guyane Française. Arch Inst Pasteur Guyane. 1961;22:1–15.
35.
go back to reference Dusfour I, Carinci R, Gaborit P, Issaly J, Girod R. Evaluation of four methods for collecting malaria vectors in French Guiana. J Econ Entomol. 2010;103:973–6.CrossRefPubMed Dusfour I, Carinci R, Gaborit P, Issaly J, Girod R. Evaluation of four methods for collecting malaria vectors in French Guiana. J Econ Entomol. 2010;103:973–6.CrossRefPubMed
37.
go back to reference Zapata MA, Cienfuegos AV, Quiros OI, Quinones ML, Luckhart S, Correa MM. Discrimination of seven Anopheles species from San Pedro de Uraba, Antioquia, Colombia, by polymerase chain reaction-restriction fragment length polymorphism analysis of its sequences. Am J Trop Med Hyg. 2007;77:67–72.PubMed Zapata MA, Cienfuegos AV, Quiros OI, Quinones ML, Luckhart S, Correa MM. Discrimination of seven Anopheles species from San Pedro de Uraba, Antioquia, Colombia, by polymerase chain reaction-restriction fragment length polymorphism analysis of its sequences. Am J Trop Med Hyg. 2007;77:67–72.PubMed
38.
39.
go back to reference Burkot TR, Zavala F, Gwadz RW, Collins FH, Nussenzweig RS, Roberts DR. Identification of malaria-infected mosquitoes by a two-site enzyme-linked immunosorbent assay. Am J Trop Med Hyg. 1984;33:227–31.PubMed Burkot TR, Zavala F, Gwadz RW, Collins FH, Nussenzweig RS, Roberts DR. Identification of malaria-infected mosquitoes by a two-site enzyme-linked immunosorbent assay. Am J Trop Med Hyg. 1984;33:227–31.PubMed
40.
43.
go back to reference Dusfour I, Jarjaval F, Gaborit P, Mura M, Girod R, Pages F. Confirmation of the occurrence of Anopheles (Nyssorhynchus) marajoara in French Guiana. J Am Mosq Control Assoc. 2012;28:309–11.CrossRefPubMed Dusfour I, Jarjaval F, Gaborit P, Mura M, Girod R, Pages F. Confirmation of the occurrence of Anopheles (Nyssorhynchus) marajoara in French Guiana. J Am Mosq Control Assoc. 2012;28:309–11.CrossRefPubMed
45.
go back to reference Michel R, Ollivier L, Meynard JB, Guette C, Migliani R, Boutin JP. Outbreak of malaria among policemen in French Guiana. Mil Med. 2007;172:977–81.CrossRefPubMed Michel R, Ollivier L, Meynard JB, Guette C, Migliani R, Boutin JP. Outbreak of malaria among policemen in French Guiana. Mil Med. 2007;172:977–81.CrossRefPubMed
49.
go back to reference Briolant S, Almeras L, Fusai T, Rogier C, Pradines B. Cyclines and malaria. Med Trop (Mars). 2007;67:86–96 (in French). Briolant S, Almeras L, Fusai T, Rogier C, Pradines B. Cyclines and malaria. Med Trop (Mars). 2007;67:86–96 (in French).
51.
go back to reference Clyde DF, Miller RM, DuPont HL, Hornick RB. Antimalarial effects of tetracyclines in man. J TropMed Hyg. 1971;74:238–42. Clyde DF, Miller RM, DuPont HL, Hornick RB. Antimalarial effects of tetracyclines in man. J TropMed Hyg. 1971;74:238–42.
52.
go back to reference Peragallo MS, Croft AM, Kitchener SJ. Malaria during a multinational military deployment: the comparative experience of the Italian, British and Australian Armed Forces in East Timor. Trans R Soc Trop Med Hyg. 2002;96:481–2.CrossRefPubMed Peragallo MS, Croft AM, Kitchener SJ. Malaria during a multinational military deployment: the comparative experience of the Italian, British and Australian Armed Forces in East Timor. Trans R Soc Trop Med Hyg. 2002;96:481–2.CrossRefPubMed
53.
go back to reference Kitchener S, Nasveld P, Russell B, Elmes N. An outbreak of malaria in a forward battalion on active service in East Timor. Mil Med. 2003;168:457–9.PubMed Kitchener S, Nasveld P, Russell B, Elmes N. An outbreak of malaria in a forward battalion on active service in East Timor. Mil Med. 2003;168:457–9.PubMed
54.
go back to reference Kitchener S. Epidemiology of malaria from East Timor among Australian Defence Force personnel. Trans R Soc Trop Med Hyg. 2002;96:376–7.CrossRefPubMed Kitchener S. Epidemiology of malaria from East Timor among Australian Defence Force personnel. Trans R Soc Trop Med Hyg. 2002;96:376–7.CrossRefPubMed
55.
go back to reference Hill DR, Baird JK, Parise ME, Lewis LS, Ryan ET, Magill AJ. Primaquine: report from CDC expert meeting on malaria chemoprophylaxis I. Am J Trop Med Hyg. 2006;75:402–15.PubMed Hill DR, Baird JK, Parise ME, Lewis LS, Ryan ET, Magill AJ. Primaquine: report from CDC expert meeting on malaria chemoprophylaxis I. Am J Trop Med Hyg. 2006;75:402–15.PubMed
56.
go back to reference Pages F. Vector control for armed forces: a historical requirement requiring continual adaptation. Med Trop. 2009;69:165–72 (in French). Pages F. Vector control for armed forces: a historical requirement requiring continual adaptation. Med Trop. 2009;69:165–72 (in French).
57.
go back to reference Deparis X, Frere B, Lamizana M, N’Guessan R, Leroux F, Lefevre P, et al. Efficacy of permethrin-treated uniforms in combination with DEET topical repellent for protection of French military troops in Cote d’Ivoire. J Med Entomol. 2004;41:914–21.CrossRefPubMed Deparis X, Frere B, Lamizana M, N’Guessan R, Leroux F, Lefevre P, et al. Efficacy of permethrin-treated uniforms in combination with DEET topical repellent for protection of French military troops in Cote d’Ivoire. J Med Entomol. 2004;41:914–21.CrossRefPubMed
59.
go back to reference Claustre J, Venturin C, Nadire M, Fauran P. Malarial vectors in French Guiana: study in an epidemic focus near Cayenne (1989–1998). Bull Soc Pathol Exot. 2001;94:353–7 (in French).PubMed Claustre J, Venturin C, Nadire M, Fauran P. Malarial vectors in French Guiana: study in an epidemic focus near Cayenne (1989–1998). Bull Soc Pathol Exot. 2001;94:353–7 (in French).PubMed
Metadata
Title
Epidemiological and entomological studies of a malaria outbreak among French armed forces deployed at illegal gold mining sites reveal new aspects of the disease’s transmission in French Guiana
Authors
Vincent Pommier de Santi
Romain Girod
Marie Mura
Aissata Dia
Sébastien Briolant
Félix Djossou
Isabelle Dusfour
Alexandre Mendibil
Fabrice Simon
Xavier Deparis
Frédéric Pagès
Publication date
01-12-2016
Publisher
BioMed Central
Published in
Malaria Journal / Issue 1/2016
Electronic ISSN: 1475-2875
DOI
https://doi.org/10.1186/s12936-016-1088-x

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