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Quantitative Polymerase Chain Reaction from Malaria Rapid Diagnostic Tests to Detect Borrelia crocidurae, the Agent of Tick-Borne Relapsing Fever, in Febrile Patients in Senegal
Ndiaye El Hadji Ibrahima
Ndiaye El Hadji Ibrahima
Aix Marseille Univ, Institut de Recherche pour le Développement (IRD), APHM, SSA, Vecteurs–Infections Tropicales et Méditerranéennes (VITROME), Marseille, France;
Institut Hospitalo-Universitaire (IHU) Méditerranée Infection, Marseille, France;
VITROME, IRD UMR 257, Campus International IRD-UCAD Hann, Dakar, Sénégal
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Institut Hospitalo-Universitaire (IHU) Méditerranée Infection, Marseille, France;
VITROME, IRD UMR 257, Campus International IRD-UCAD Hann, Dakar, Sénégal
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Georges Diatta
Georges Diatta
VITROME, IRD UMR 257, Campus International IRD-UCAD Hann, Dakar, Sénégal
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Diarra Adama Zan
Diarra Adama Zan
Aix Marseille Univ, Institut de Recherche pour le Développement (IRD), APHM, SSA, Vecteurs–Infections Tropicales et Méditerranéennes (VITROME), Marseille, France;
Institut Hospitalo-Universitaire (IHU) Méditerranée Infection, Marseille, France;
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Institut Hospitalo-Universitaire (IHU) Méditerranée Infection, Marseille, France;
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Hubert Bassene
Hubert Bassene
VITROME, IRD UMR 257, Campus International IRD-UCAD Hann, Dakar, Sénégal
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Cheikh Sokhna
Cheikh Sokhna
Institut Hospitalo-Universitaire (IHU) Méditerranée Infection, Marseille, France;
VITROME, IRD UMR 257, Campus International IRD-UCAD Hann, Dakar, Sénégal
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VITROME, IRD UMR 257, Campus International IRD-UCAD Hann, Dakar, Sénégal
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Philippe Parola
Philippe Parola
Aix Marseille Univ, Institut de Recherche pour le Développement (IRD), APHM, SSA, Vecteurs–Infections Tropicales et Méditerranéennes (VITROME), Marseille, France;
Institut Hospitalo-Universitaire (IHU) Méditerranée Infection, Marseille, France;
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Institut Hospitalo-Universitaire (IHU) Méditerranée Infection, Marseille, France;
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ABSTRACT.
In endemic malaria areas, Plasmodium is currently diagnosed mainly through the use of rapid diagnostic tests (RDTs). However, in Senegal, many causes of fever remain unknown. Tick-borne relapsing fever, an often-neglected public health problem, is the main cause of consultation for acute febrile illness after malaria and flu in rural areas. Our objective was to test the feasibility of extracting and amplifying DNA fragments by quantitative polymerase chain reaction (qPCR) from malaria-negative RDTs for Plasmodium falciparum (malaria Neg RDTs P.f) to detect Borrelia spp. and other bacteria. Between January and December 2019, malaria Neg RDTs P.f were collected on a quarterly basis in 12 health facilities in four regions of Senegal. The DNA extracted from the malaria Neg RDTs P.f was tested using qPCR and the results were confirmed by standard PCR and sequencing. Only Borrelia crocidurae DNA was detected in 7.22% (159/2,202) of RDTs. The prevalence of B. crocidurae DNA was higher in July (16.47%, 43/261) and August (11.21%, 50/446). The annual prevalence was 9.2% (47/512) and 5.0% (12/241) in Ngayokhem and Nema-Nding, respectively, health facilities in the Fatick region. Our study confirms that B. crocidurae infection is a frequent cause of fever in Senegal, with a high prevalence of cases in health facilities in the regions of Fatick and Kaffrine. Malaria Neg RDTs P.f are potentially a good source of pathogen sampling for the molecular identification of other causes of fever of unknown origin, even in the most remote areas.
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Author Notes
Authors’ addresses: Ndiaye El Hadji Ibrahima, Aix Marseille Univ, Institut de Recherche pour le Développement (IRD), Vecteurs–Infections Tropicales et Méditerranéennes (VITROME), Marseille, France, Institut Hospitalo-Universitaire (IHU) Méditerranée Infection, Marseille, France, and Campus International de Recherche IRD-UCAD Hann, UMR 257 VITROME, Dakar, Sénégal, E-mail: el-hadji-ibrahima.ndiaye@ird.fr. Georges Diatta, Campus International de Recherche IRD-UCAD Hann, UMR 257 VITROME, Dakar, Sénégal, E-mail: georges.diatta@ird.fr. Diarra Adama Zan, Aix Marseille Univ, IRD, VITROME, Marseille, France, and IHU Méditerranée Infection, Marseille, France, E-mail: adamazandiarra@gmail.com. Hubert Bassene, Campus International de Recherche IRD-UCAD Hann, UMR 257 VITROME, Dakar, Sénégal, E-mail: hubert.bassene@ird.fr. Cheikh Sokhna, IHU Méditerranée Infection, Marseille, France, and Campus International de Recherche IRD-UCAD Hann, UMR 257 VITROME, Dakar, Sénégal, E-mail: cheikh.sokhna@ird.fr. Philippe Parola, Aix Marseille Univ, IRD, VITROME, Marseille, France, and IHU Méditerranée Infection, Marseille, France, E-mail: philippe.parola@univ-amu.fr.
ProCite
RefWorks
Reference Manager
BibTeX
Zotero
EndNote
-
1.
Sokhna C , Mediannikov O , Fenollar F , Bassene H , Diatta G , Tall A , Trape J-F , Drancourt M , Raoult D , 2013. Point-of-care laboratory of pathogen diagnosis in rural Senegal. PLoS Negl Trop Dis 7: e1999.
-
2.
Wotodjo AN , Doucoure S , Gaudart J , Diagne N , Diene Sarr F , Faye N , Tall A , Raoult D , Sokhna C , 2017. Malaria in Dielmo, a Senegal village: is its elimination possible after seven years of implementation of long-lasting insecticide-treated nets? PLoS One 12: e0179528.
-
3.
Bhargava A , Ralph R , Chatterjee B , Bottieau E , 2018. Assessment and initial management of acute undifferentiated fever in tropical and subtropical regions. BMJ 363: k4766.
-
4.
Parola P , Diatta G , Socolovschi C , Mediannikov O , Tall A , Bassene H , Trape JF , Raoult D , 2011. Tick-borne relapsing fever borreliosis, rural Senegal. Emerg Infect Dis 17: 883–885.
-
5.
Diatta G et al., 2016. An alternative strategy of preventive control of tick-borne relapsing fever in rural areas of Sine-Saloum, Senegal. Am J Trop Med Hyg 95: 537–545.
-
6.
Ndiaye EHI , Diouf FS , Ndiaye M , Bassene H , Raoult D , Sokhna C , Parola P , Diatta G , 2021. Tick-borne relapsing fever borreliosis, a major public health problem overlooked in Senegal. PLoS Negl Trop Dis 15: e0009184.
-
7.
Trape J-F et al., 2014. The rise and fall of malaria in a West African rural community, Dielmo, Senegal, from 1990 to 2012: a 22 year longitudinal study. Lancet Infect Dis 14: 476–488.
-
8.
Diallo MA , Kane BS , Ndiaye M , Dieng M , Diongue K , Badiane AS , Seck MC , Ndiaye D , 2017. Plasmodium falciparum malaria co-infection with tick-borne relapsing fever in Dakar. Malar J 16: 24.
-
9.
Hovette P , Aubron C , Perrier-Gros-Claude JD , Schieman R , N’Dir MC , Camara P , 2001. Value of quantitative buffy coat (QBC) in borreliasis-malaria co-infection. Med Trop (Mars) 61: 196–197.
-
10.
Flatau E , Reichman N , Elias M , Raz R , 2000. Malaria and Borrelia co-infection. J Travel Med 7: 98–99.
-
11.
Nordstrand A , Bunikis I , Larsson C , Tsogbe K , Schwan TG , Nilsson M , Bergström S , 2007. Tickborne relapsing fever diagnosis obscured by malaria, Togo. Emerg Infect Dis 13: 117–123.
-
12.
Trape J-F et al., 2013. The epidemiology and geographic distribution of relapsing fever borreliosis in West and North Africa, with a review of the Ornithodoros erraticus complex (Acari: Ixodida). PLoS One 8: e78473.
-
13.
Wotodjo AN , Doucoure S , Diagne N , Sarr FD , Parola P , Gaudart J , Sokhna C , 2021. The impact of renewing long-lasting insecticide-treated nets in the event of malaria resurgence: lessons from 10 years of net use in Dielmo, Senegal. Am J Trop Med Hyg 104: 255–262.
-
14.
Mediannikov O , Socolovschi C , Bassene H , Diatta G , Ratmanov P , Fenollar F , Sokhna C , Raoult D , 2014. Borrelia crocidurae infection in acutely febrile patients, Senegal. Emerg Infect Dis 20: 1335–1338.
-
15.
National Malaria Control Program (PNLP) , 2021. PLAN STRATEGIQUE NATIONAL DE LUTTE CONTRE LE PALUDISME AU SENEGAL 2021–2025. Available at: https://senegal-cocreation.com/wp-content/uploads/2021/02/PSN_PNLP_Senegal_Version-finale_-Fevrier-2021.pdf. Accessed January 25, 2023.
-
16.
National Malaria Control Program (PNLP) , 2015. PLAN STRATEGIQUE NATIONAL 2011–2015. Available at: https://pspdb.dev.gouv.bj/server/storage/app/PolitiqueFichiers/57_Plan_strategique_2011_2015.pdf. Accessed January 25, 2023.
-
17.
Thwing J et al., 2017. Declines in malaria burden and all-cause child mortality following increases in control interventions in Senegal, 2005–2010. Am J Trop Med Hyg 97: 89–98.
-
18.
Abat C , Colson P , Chaudet H , Rolain J-M , Bassene H , Diallo A , Mediannikov O , Fenollar F , Raoult D , Sokhna C , 2016. Implementation of syndromic surveillance systems in two rural villages in Senegal. PLoS Negl Trop Dis 10: e0005212.
-
19.
Davis KM , Gibson LE , Haselton FR , Wright DW , 2014. Simple sample processing enhances malaria rapid diagnostic test performance. Analyst (Lond) 139: 3026–3031.
-
20.
Veron V , Carme B , 2006. Recovery and use of Plasmodium DNA from malaria rapid diagnostic tests. Am J Trop Med Hyg 74: 941–943.
-
21.
Cnops L , Boderie M , Gillet P , Van Esbroeck M , Jacobs J , 2011. Rapid diagnostic tests as a source of DNA for Plasmodium species-specific real-time PCR. Malar J 10: 67.
-
22.
Ishengoma DS , Lwitiho S , Madebe RA , Nyagonde N , Persson O , Vestergaard LS , Bygbjerg IC , Lemnge MM , Alifrangis M , 2011. Using rapid diagnostic tests as source of malaria parasite DNA for molecular analyses in the era of declining malaria prevalence. Malar J 10: 6.
-
23.
Morris U et al., 2013. Rapid diagnostic tests for molecular surveillance of Plasmodium falciparum malaria—assessment of DNA extraction methods and field applicability. Malar J 12: 106.
-
24.
Srisutham S , Suwannasin K , Mathema VB , Sriprawat K , Smithuis FM , Nosten F , White NJ , Dondorp AM , Imwong M , 2020. Utility of Plasmodium falciparum DNA from rapid diagnostic test kits for molecular analysis and whole genome amplification. Malar J 19: 193.
-
25.
Diatta G , Vial L , Niang O , Bouganali C , Trape J-F , 2005. Enquête sur la borréliose à tiques à Borrelia crocidurae au Sénégal. Available at: https://horizon.documentation.ird.fr/exl-doc/pleins_textes/num-dakar-02/010039439.pdf. Accessed January 27, 2023.
-
26.
Diatta G et al., 2012. Epidemiology of tick-borne borreliosis in Morocco. PLoS Negl Trop Dis 6: e1810.
-
27.
Diouf I , Rodriguez Fonseca B , Caminade C , Thiaw WM , Deme A , Morse AP , Ndione J-A , Gaye AT , Diaw A , Ndiaye MKN , 2020. Climate variability and malaria over West Africa. Am J Trop Med Hyg 102: 1037–1047.
-
28.
Fall NS , Diagne N , Mediannikov O , Fenollar F , Parola P , Sokhna C , Raoult D , Lagier J-C , 2020. Detection of Borrelia crocidurae in a vaginal swab after miscarriage, rural Senegal, western Africa. Int J Infect Dis 91: 261–263.
-
29.
Parola P , Raoult D , 2001. Ticks and tickborne bacterial diseases in humans: an emerging infectious threat. Clin Infect Dis 32: 897–928.
-
30.
Sutherland C, Ropper C, Raman J, Naidoo I, Ishengoma D, Alifrangis M, Cnops L, Jacobs J , 2011. Preparation of rapid diagnostic tests (RDTs) for DNA extraction v1.1. Molecular Module, WorldWide Antimalarial Resistance Network, Procedure MOL06. Available at: https://www.wwarn.org/sites/default/files/MOL06_RDTsForDNAExtraction.pdf. Accessed January 25, 2023.
-
31.
Elbir H et al., 2013. Multiplex real-time PCR diagnostic of relapsing fevers in Africa. PLoS Negl Trop Dis 7: e2042.
-
32.
Schwan TG , Schrumpf ME , Hinnebusch BJ , Anderson DE , Konkel ME , 1996. GlpQ: an antigen for serological discrimination between relapsing fever and Lyme borreliosis. J Clin Microbiol 34: 2483–2492.
-
33.
Ndiaye EHI , Diatta G , Diarra AZ , Berenger JM , Bassene H , Mediannikov O , Bouganali C , Sokhna C , Parola P , 2022. Morphological, molecular and MALDI-TOF MS identification of bedbugs and associated Wolbachia species in rural Senegal. J Med Entomol 59: 1019–1032.
-
34.
Assous MV , Wilamowski A , Bercovier H , Marva E , 2006. Molecular characterization of tickborne relapsing fever Borrelia, Israel. Emerg Infect Dis 12: 1740–1743.
-
35.
Diarra AZ , Almeras L , Laroche M , Berenger J-M , Koné AK , Bocoum Z , Dabo A , Doumbo O , Raoult D , Parola P , 2017. Molecular and MALDI-TOF identification of ticks and tick-associated bacteria in Mali. PLoS Negl Trop Dis 11: e0005762.
-
36.
Medkour H et al., 2021. Potential zoonotic pathogens hosted by endangered bonobos. Sci Rep 11: 6331.
-
37.
Toledo A , Anda P , Escudero R , Larsson C , Bergstrom S , Benach JL , 2010. Phylogenetic analysis of a virulent Borrelia species isolated from patients with relapsing fever. J Clin Microbiol 48: 2484–2489.
-
38.
Diarra AZ et al., 2020. Molecular detection of microorganisms associated with small mammals and their ectoparasites in Mali. Am J Trop Med Hyg 103: 2542–2551.
-
39.
Rahal M , Medkour H , Diarra AZ , Bitam I , Parola P , Mediannikov O , 2020. Molecular identification and evaluation of Coxiella-like endosymbionts genetic diversity carried by cattle ticks in Algeria. Ticks Tick Borne Dis 11: 101493.
-
40.
Vial L , Diatta G , Tall A , Hadj Ba E , Bouganali H , Durand P , Sokhna C , Rogier C , Renaud F , Trape J-F , 2006. Incidence of tick-borne relapsing fever in West Africa: longitudinal study. Lancet 368: 37–43.
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