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Mapping the Distribution of Anopheles Funestus Across Benin Highlights A Wellcome Open Research 2017, 1:28 Last updated: 02 JUN 2021 RESEARCH ARTICLE Mapping the distribution of Anopheles funestus across Benin highlights a sharp contrast of susceptibility to insecticides and infection rate to Plasmodium between southern and northern populations [version 2; peer review: 2 approved] Rousseau Djouaka 1*, Romaric Akoton 1,2*, Genevieve M. Tchigossou1,2, Seun M. Atoyebi 1,3, Helen Irving4, Michael O. Kusimo 1, Innocent Djegbe5, Jacob M. Riveron4, Eric Tossou1,2, Akadiri Yessoufou2, Charles S. Wondji 4 1International Institute of Tropical Agriculture, Cotonou, Benin 2University of Abomey-Calavi, Cotonou, Benin 3Cell Biology and Genetics Unit, Department of Zoology, University of Ibadan, Ibadan, Nigeria 4Liverpool School of Tropical Medicine, Liverpool, UK 5University of Sciences, Arts and Techniques of Natitingou, Ecole Normale Supérieure de Natitingou, Natitingou, Benin * Equal contributors v2 First published: 14 Dec 2016, 1:28 Open Peer Review https://doi.org/10.12688/wellcomeopenres.10213.1 Latest published: 03 Mar 2017, 1:28 https://doi.org/10.12688/wellcomeopenres.10213.2 Reviewer Status Invited Reviewers Abstract Background. Malaria remains an important public health issue in 1 2 Benin, with Anopheles gambiae s.l. and Anopheles funestus s.s being the predominant vectors. This study was designed to generate version 2 information on An. funestus distribution, molecular speciation, (revision) Plasmodium infection rate and insecticide susceptibility status across 03 Mar 2017 Benin. Methods. Mosquito samples were collected from December 2014 to January 2016 in 46 localities in Benin. These samples were version 1 mapped and An. funestus collected were speciated to the molecular 14 Dec 2016 report report level. Plasmodium infection rate was determined using a Taqman assay and susceptibility to insecticides was assessed using the WHO guidelines. The genotyping of the L119F- Gste2 mutation was also 1. Mouhamadou S. Chouaibou , Centre carried out. Results. An. funestus was found in 8 out of the 46 localities Suisse de Recherches Scientifiques en Côte surveyed with a high presence in Tanongou (wet Sudanese ecological d'Ivoire, Abidjan, Cote d'Ivoire zone), Kpome, Doukonta and Pahou (sub-equatorial ecological zone). Molecular identifications revealed that only An. funestus s.s was 2. Mamadou Ousmane Ndiath , Institut present in southern Benin, whereas in Tanongou (northern Benin) An. funestus s.s. and An. leesoni were found in sympatry at proportions of Pasteur of Madagascar, BP 1274, 77.7% and 22.3% respectively. Plasmodium infection rate of An. Page 1 of 18 Wellcome Open Research 2017, 1:28 Last updated: 02 JUN 2021 funestus was higher in southern Benin at a range of 13 to 18% compared to 5.6% recorded in Tanongou. High DDT (8±0.5%) and Ambatofotsikely Avaradoha, 101 permethrin (11±0.5%) resistance were observed in Doukonta, Kpome Antananarivo, Madagascar and Pahou, contrasting with relatively low resistance profiles: mortality-DDT=90±3.18% and mortality-permethrin=100% in Any reports and responses or comments on the Tanongou. Genotyping analysis revealed high frequency of the article can be found at the end of the article. resistant 119F allele in the South (Kpome and Doukonta) compared to the North (Tanongou). Discussion and Conclusion. The high presence of An. funestus in the South compared to the North could be due to favorable environmental and climatic conditions found in both regions. A significant Plasmodium infection rate was recorded across the country. A high resistance profile was recorded in the southern Benin; this raises the need for further investigations on resistance selection factors. Keywords Anopheles funestus, distribution, Plasmodium infection, insecticide resistance, South-North, Benin Corresponding author: Rousseau Djouaka ([email protected]) Competing interests: No competing interests were disclosed. Grant information: This work is supported by the Wellcome Trust [099864], [101893]. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript. Copyright: © 2017 Djouaka R et al. This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited. How to cite this article: Djouaka R, Akoton R, Tchigossou GM et al. Mapping the distribution of Anopheles funestus across Benin highlights a sharp contrast of susceptibility to insecticides and infection rate to Plasmodium between southern and northern populations [version 2; peer review: 2 approved] Wellcome Open Research 2017, 1:28 https://doi.org/10.12688/wellcomeopenres.10213.2 First published: 14 Dec 2016, 1:28 https://doi.org/10.12688/wellcomeopenres.10213.1 Page 2 of 18 Wellcome Open Research 2017, 1:28 Last updated: 02 JUN 2021 national control programs need better knowledge on key malaria REVISED Amendments from Version 1 vectors nationwide, including their geographical distribution, sus- We did not remove any of the already published information, ceptibility profile to insecticides and contribution to malaria trans- rather few insertions were made in the manuscript based of the mission, as well as understanding the vectorial complexity of these second reviewer’s comments. Briefly, information inserted are as species. Such information already exists for Anopheles gambiae follows: across Benin2,4,5, but this is not the case for the other major vec- Methods tor An. funestus, for which only limited information is available, 6,7 Comment 1: I recommend the authors to give the different mainly from few coastal populations . sequences of the primers used (P. ovale, vivax, malariae and falciparum) for Plasmodium infection rate detection. An. funestus Giles is one of the key malaria-transmitting mos- Primers- Forward (F), PlasF (5’- quitoes in Africa. The vectorial capacity of this mosquito vector GCTTAGTTACGATTAATAGGAGTAGCTTG-3’) and reverse (R), PlasR (5’- GAAAATCTAAGAATTTCACCTCTGACA-3’). is close to and could exceed that of An. gambiae, the most docu- mented malaria vector in some countries8. An. funestus Giles group Specific probes for plasmodium species detection: 9,10 5’-TCTGAATACGAATGTC-3’ labelled with FAM and 5’- is made up of nine species distributed across sub-Saharan Africa . CTGAATACAAATGCC-3’ labelled with HEX. These nine species of the An. funestus group are as follows: An. funestus Giles (s.s), An. vaneedeni Gillies and Coetzee, Insecticides susceptibility An. leesoni Evans, An. parensis Gillies, An. rivulorum Leeson, Comment 2: I suggest the authors to develop this part by giving An. fuscivenosus Leeson, An. brucei Service, An. aruni Sobti information about: and An. confusus Evans and Leeson. These species are not easily the number of ovipositing females: for Doukonta, 9 mosquitoes distinguishable using morphological keys9,10. oviposited out of 15 while 75 oviposited out of 110 mosquitoes subjected to forced-egg laying technique. The number of tested mosquitoes per molecules (DDT and The vectorial capacity of members of the An. funestus group permethrin) and the number of replicates: 100 mosquitoes were varies significantly, with most species being zoophilic, except tested for each insecticide in 4 and 5 replicates in Doukonta and An. funestus s.s., which is the main Plasmodium vector in this group. Tanongou respectively. Indeed high infection rates have been reported for An. funestus s.s., The origin of impregnated papers (from Vector Control such as 22%11 and 27%12 documented in South Africa, 11% in Research Unit, University Sains Malaysia, Penang, Malaysia??): Tanzania13, 50% in Burkina Faso14 and 18% in Benin7. However, Impregnated papers were purchased from Vector Biology Department, Liverpool School of Tropical Medicine, UK. other members of the group, such as An. rivulorum has a high anthropophilic rate of 40% (42/106) in the southern region of Test and insectary conditions (relative humidity and temperature): 15 Insectary and test room were at a temperature of 25–27°C and Nigeria , but presents a low contribution to malaria transmission relative humidity of 80±5%. in Tanzania16. As for An. vaneedeni, this species could be either exophilic or anthrophilic, but can easily carry the Plasmodium Data analysis and Results parasite under laboratory conditions17, whereas An. parensis Comments 3 & 4: Statistical tests used: Fisher’s exact test was is endophilic, but does not carry the malaria parasite15,18,19. In used to determine the significant levels of Plasmodium infection rates and L119F-GSTe2 mutation detected. most parts of Africa, An. funestus s.s. and other members of the An. funestus group live in sympatry9,15,18, and if appropriate iden- Figures and Tables: tification is not made this could lead to wrong vectorial characteri- Comment 5: For clarity please add the collection dates in the zation of An. funestus s.s. This relevant information on An. funestus titles, specify what f(S) and f(R) represent in the title of Figure 4. in Benin has been documented in some parts of the southern coastal The data in Figure 3 represent mortality rate? means? medians? localities of Ouidah, Kpomasse, Tori and Pahou6,20, but no extensive with 95% confidence intervals? Please make clear: These comments have been addressed in this version of the article. study has so far been carried out in a North-South Benin transect to determine the extent of the distribution of this species in the See referee reports
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