Entomological Characteristics of Malaria Transmission across Benin: An Essential Element for Improved Deployment of Vector Control Interventions

Tatchémè Filémon Tokponnon; Razaki Ossè; Germain Gil Padonou; Cyriaque Dossou Affoukou; Aboubakar Sidick; Wilfried Sewadé; Arsène Fassinou; Côme Z. Koukpo; Bruno Akinro; Louisa A. Messenger; Mariam Okê; Alexis Tchévoédé; Aurore Ogouyemi-Hounto; Dorothée Kinde Gazard; Martin Akogbeto

doi:10.3390/insects14010052

journal article Open Access Jan 05, 2023

Entomological Characteristics of Malaria Transmission across Benin: An Essential Element for Improved Deployment of Vector Control Interventions

Tatchémè Filémon Tokponnon Razaki Ossè Germain Gil Padonou Cyriaque Dossou Affoukou Aboubakar Sidick Wilfried Sewadé Arsène Fassinou Côme Z. Koukpo Bruno Akinro Louisa A. Messenger

Mariam Okê Alexis Tchévoédé Aurore Ogouyemi-Hounto Dorothée Kinde Gazard Martin Akogbeto

Insects Vol. 14 No. 1 pp. 52 · MDPI AG

View at Publisher Save 10.3390/insects14010052

Abstract

Entomological surveillance in Benin has historically been limited to zones where indoor residual spraying was performed or where long-standing sentinel surveillance sites existed. However, there are significant country-wide gaps in entomological knowledge. The National Malaria Control Program (NMCP) assessed population dynamics of Anopheles vectors and malaria transmission in each of Benin’s 12 departments to create an entomological risk profile. Two communes per department (24/77 communes) were chosen to reflect diverse geographies, ecologies and malaria prevalence. Two villages per commune were selected from which four households (HH) per village were used for human landing catches (HLCs). In each HH, an indoor and outdoor HLC occurred between 7 p.m. and 7 a.m. on two consecutive nights between July–September 2017. Captured Anopheles were identified, and ovaries were dissected to determine parous rate. Heads and thoraces were tested for Plasmodium falciparum sporozoites by ELISA. The Entomological Inoculation Rate (EIR) was calculated as the product of mosquito bite rate and sporozoite index. Bite rates from An. gambiae s.l., the primary vector species complex, differed considerably between communes; average sporozoite infection index was 3.5%. The EIR ranged from 0.02 infectious bites (ib) per human per night in the departments of Ouémé and Plateau to 1.66 ib/human/night in Collines. Based on transmission risk scales, Avrankou, Sakété and Nikki are areas of low transmission (0 < EIR < 3 ib/human/year), Adjarra, Adja Ouèrè, Zè, Toffo, Bopa, Pehunco, Pèrèrè and Kandi are of medium transmission (3 < EIR < 30 ib/human/year), and the other remaining districts are high transmission (EIR > 30 ib/human/year). The heterogeneous and diverse nature of malaria transmission in Benin was not readily apparent when only assessing entomological surveillance from sentinel sites. Prospectively, the NMCP will use study results to stratify and deploy targeted vector control interventions in districts with high EIRs to better protect populations most at-risk.

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References

65

[1]

Collins "Malaria: Current and future prospects for control" Annu. Rev. Entomol. (1995) 10.1146/annurev.en.40.010195.001211

[2]

The global distribution of clinical episodes of Plasmodium falciparum malaria

Robert W. Snow, Carlos A. Guerra, Abdisalan M. Noor et al.

Nature 2005 10.1038/nature03342

[3]

WHO (2021). Malaria World Report, World Health Organization.

[4]

WHO (2018). Global Report on Insecticide Resistance in Malaria Vectors: 2010–2016, World Health Organization.

[5]

Kazembe "Spatial analysis and mapping of malaria risk in Malawi using point-referenced prevalence of infection data" Int. J. Health Geograph. (2006) 10.1186/1476-072x-5-41

[6]

Malaria, R.B. (2018, February 26). The Global Malaria Action Plan 2012. 2013. Available online: http://www.rollbackmalaria.org/gmap.

[7]

Toto "High malaria transmission intensity in a village close to Yaounde, the capital city of Cameroon" J. Med. Entomol. (2002) 10.1603/0022-2585-39.2.350

[8]

White "Plasmodium knowlesi: The fifth human malaria parasite" Clin. Infect. Dis. (2008) 10.1086/524889

[9]

Carnevale, P., and Robert, V. (2009). Les Anophèles, Biologie, Transmission du Paludisme et Lutte Antivectorielle, IRD Montpellier France Editions. 10.4000/books.irdeditions.10374

[10]

Fontenille "Unravelling complexities in human malaria transmission dynamics in Africa through a comprehensive knowledge of vector populations" Comp. Immun. Microbiol. Infect. Dis. (2004) 10.1016/j.cimid.2004.03.005

[11]

Tokponnon "Involvement of Anopheles nili in Plasmodium falciparum transmission in North Benin" Malar. J. (2019)

[12]

Chandra "Nutritional evaluation of NB-21 hybrid Napier grass for goats" Indian J. Small Rum. (2012)

[13]

WHO (2017). World Malaria Report 2017, World Health Organization.

[14]

Moiroux "Changes in Anopheles funestus biting behavior following universal coverage of long-lasting insecticidal nets in Benin" J. Infect. Dis. (2012) 10.1093/infdis/jis565

[15]

Ministère de la santé du Bénin (2019). Annuaire des Statistiques Sanitaires 2018 des Départements du Benin, Ministère de la santé du Bénin.

[16]

(2020, January 05). Institut National de la Statistique et de l’Analyse Économique (INSAE) et ICF. 2018. Enquête Démographique et de Santé au Bénin, 2017–2018: Indicateurs Clés. Cotonou, Bénin et Rockville, Maryland, USA: INSAE et ICF. Available online: https://www.google.com.hk/url?sa=t&rct=j&q=&esrc=s&source=web&cd=&cad=rja&uact=8&ved=2ahUKEwij7sLAn7D8AhXJr1YBHXk-BowQFnoECBgQAQ&url=https%3A%2F%2Finstad.bj%2Fimages%2Fdocs%2Finsae-statistiques%2Fsociales%2FSante%2FEnqu%25C3%25AAte%2520D%25C3%25A9mographique%2520et%2520de%2520Sant%25C3%25A9%2520au%2520B%25C3%25A9nin%2520.

[17]

Moiroux "Culicidae diversity, malaria transmission and insecticide resistance alleles in malaria vectors in Ouidah–Kpomasse–Tori district from Benin (West Africa): A pre-intervention study" Parasite Vectors (2010) 10.1186/1756-3305-3-83

[18]

Gnanguenon "Transmission patterns of Plasmodium falciparum by Anopheles gambiae in Benin" Malar. J. (2014) 10.1186/1475-2875-13-444

[19]

Azondekon "Six years of experience in entomological surveillance of indoor residual spraying against malaria transmission in Benin: Lessons learned, challenges and outlooks" Malar. J. (2015) 10.1186/s12936-015-0757-5

[20]

Tokponnon "Vector resistance to pyrethroids and impact on the efficacy of insecticide-treated mosquito nets in Southern Benin" JPVB (2018)

[21]

PNLP-Bénin (2017). Plan Stratégique National de Lutte contre le paludisme 2017–2021, PNLP.

[22]

"Lagoonal and coastal malaria at Cotonou: Entomological findings" Santé (2000)

[23]

Padonou "Biology of Anopheles gambiae and insecticide resistance: Entomological study for a large scale of indoor residual spraying in South East" J. Parasitol. Vector Biol. (2011)

[24]

Gnanguenon "A shift from indoor residual spraying (IRS) with bendiocarb to Long-Lasting Insecticidal (mosquito) Nets (LLINs) associated with changes in malaria transmission indicators in pyrethroid resistance areas in Benin" Parasites Vectors (2013) 10.1186/1756-3305-6-73

[25]

Sovi "Impact of land-use on malaria transmission in the plateau region, southeastern Benin" Parasites Vectors (2013) 10.1186/1756-3305-6-352

[26]

Tokponon "Good performances but short lasting efficacy of Actellic 50 EC Indoor Residual Spraying (IRS) on malaria transmission in Benin. West Africa" Parasites Vectors (2014) 10.1186/1756-3305-7-256

[27]

Tokponnon "Impact of Long-Lasting, Insecticidal Nets on Anaemia and Prevalence of Plasmodium falciparum among Children under Five Years in Areas with Highly Resistant Malaria Vectors" Malar. J. (2014) 10.1186/1475-2875-13-76

[28]

Djouaka "Multiple insecticide resistance in an infected population of the malaria vector Anopheles funestus in Benin" Parasites Vectors (2016) 10.1186/s13071-016-1723-y

[29]

PNLP (2018). Plan National de Gestion de la Résistance des Vecteurs aux Insecticides 2018–2022, PNLP.

[30]

Hemingway "Averting a malaria disaster: Will insecticide resistance derail malaria control?" Lancet (2016) 10.1016/s0140-6736(15)00417-1

[31]

Ranson "Insecticide resistance in African Anopheles mosquitoes: A worsening situation that needs urgent action to maintain malaria control" Trends Parasitol. (2016) 10.1016/j.pt.2015.11.010

[32]

WHO (2018). World Malaria Report 2018, World Health Organization.

[33]

Ministère du Cadre de vie Bénin (2015). Plan National de Sécheresse 2019–2024, Ministère du Cadre de vie Bénin.

[34]

Gillies "A Supplement to the Anophelinae of Africa South of the Sahara (Afrotropical Region)" Publ. S. Afr. Inst. Med. Res. (1987)

[35]

Detinova "Observations on the determination of the Age composition and epidemiological importance of populations of Anopheles gambiae Giles and Anopheles funestus Giles in Tanganyika" Bull. World Health Organ. (1964)

[36]

Wirtz "Comparative testing of monoclonal antibodies against Plasmodium falciparum sporozoites for ELISA development" Bull. World Health Organ. (1987)

[37]

Insertion polymorphisms of SINE200 retrotransposons within speciation islands of Anopheles gambiae molecular forms

Federica Santolamazza, Emiliano Mancini, Frédéric Simard et al.

Malaria Journal 2008 10.1186/1475-2875-7-163

[38]

A cocktail polymerase chain reaction assay to identify members of the Anopheles funestus (Diptera: Culicidae) group.

L L Koekemoer, L Kamau, R H Hunt et al.

The American Journal of Tropical Medicine and Hygi... 2002 10.4269/ajtmh.2002.66.804

[39]

Kengne "Molecular identification of the Anopheles nili group African malaria vectors" Med. Vet. Entomol. (2003) 10.1046/j.1365-2915.2003.00411.x

[40]

Chandre "Molecular characterization of pyrethroid knockdown resistance (kdr) in the major malaria vector Anopheles gambiae s.s" Insect Mol. Biol. (1998) 10.1046/j.1365-2583.1998.72062.x

[41]

Weill "The unique mutation in ace-1 giving high insecticide resistance is easily detectable in mosquito vectors" Insect Mol. Biol. (2004) 10.1111/j.1365-2583.2004.00452.x

[42]

Bloodmeal Identification by Direct Enzyme-Linked Immunosorbent Assay (Elisa), Tested on Anopheles (Diptera: Culicidae) in Kenya12

John C. Beier, Peter V. Perkins, Robert A. Wirtz et al.

Journal of Medical Entomology 1988 10.1093/jmedent/25.1.9

[43]

Robert, V. (2004). La Transmission, Composante Majeure de L’épidémiologie du Paludisme, Groupe de Recherche sur le Paludisme.

[44]

Salako "Insecticide resistance status, frequency of L1014F Kdr and G119S Ace-1 mutations, and expression of detoxification enzymes in Anopheles gambiae (s.l.) in two regions of northern Benin in preparation for indoor residual spraying" Parasites Vectors (2018) 10.1186/s13071-018-3180-2

[45]

Akogbeto "Distribution of members of the Anopheles gambiae complex and their chromosomal variants in Benin and Togo, West Africa" Afr. Zool. (1995)

[46]

Djouaka, R., Irving, H., and Tukur, Z. (2011). Exploring mechanisms of multiple insecticide resistance in a population of the malaria vector Anopheles funestus in Benin. PLoS ONE, 6. 10.1371/journal.pone.0027760

[47]

Osse "Entomological baseline data on malaria transmission and susceptibility of Anopheles gambiae to insecticides in preparation for indoor residual spraying (IRS) in Atacora, (Benin)" J. Parasitol. Vector Biol. (2013)

[48]

Salako "Blood feeding behaviour comparison and contribution of Anopheles coluzzii and Anopheles gambiae, two sibling species living in sympatry, to malaria transmission in Alibori and Donga region, northern Benin, West Africa" Malar. J. (2018) 10.1186/s12936-018-2452-9

[49]

Akogbeto "Infectivity of Anopheles melas vis-a-vis Plasmodium falciparum in the coastal lagoon area of Benin" Bull. Soc. Pathol. Exot. (1999)

[50]

Yadouleton "Development of vegetable farming: A cause of the emergence of insecticide resistance in populations of Anopheles gambiae in urban areas of Benin" Malar. J. (2009) 10.1186/1475-2875-8-103

Showing 50 of 65 references

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References

Details

Published: Jan 05, 2023
Vol/Issue: 14(1)
Pages: 52
License: View

Authors

T

Tatchémè Filémon Tokponnon

Ministère de la Santé, Cotonou 08 BP 882, Benin; Cotonou Entomological Research Center, Cotonou 06 BP 2604, Benin; Centre Béninois de la Recherche Scientifique et de l’Innovation (CBRSI), Agbondjèdo, Étoile Rouge, Cotonou 03 BP 1665, Benin; Ecole Polytechnique d’Abomey-Calavi, Université d’Abomey-Calavi, Cotonou 01 BP 2009, Benin

R

Razaki Ossè

Cotonou Entomological Research Center, Cotonou 06 BP 2604, Benin

G

Germain Gil Padonou

Cotonou Entomological Research Center, Cotonou 06 BP 2604, Benin

C

Cyriaque Dossou Affoukou

National Malaria Control Program, Cotonou 01 BP 882, Benin

A

Aboubakar Sidick

Cotonou Entomological Research Center, Cotonou 06 BP 2604, Benin

W

Wilfried Sewadé

Cotonou Entomological Research Center, Cotonou 06 BP 2604, Benin

A

Arsène Fassinou

Cotonou Entomological Research Center, Cotonou 06 BP 2604, Benin

C

Côme Z. Koukpo

Cotonou Entomological Research Center, Cotonou 06 BP 2604, Benin

B

Bruno Akinro

Cotonou Entomological Research Center, Cotonou 06 BP 2604, Benin

L

Louisa A. Messenger

Department of Disease Control, London School of Hygiene & Tropical Medicine, London WC1E 7HT, UK; Department of Environmental and Occupational Health, School of Public Health, University of Nevada, Las Vegas, NV 89154, USA

M

Mariam Okê

Ministère de la Santé, Cotonou 08 BP 882, Benin

A

Alexis Tchévoédé

National Malaria Control Program, Cotonou 01 BP 882, Benin

A

Aurore Ogouyemi-Hounto

National Malaria Control Program, Cotonou 01 BP 882, Benin; Parasitology-Mycologie Research Unit, Faculté des Sciences de la Santé, University of Abomey-Calavi, Cotonou 01 BP 188, Benin

D

Dorothée Kinde Gazard

Parasitology-Mycologie Research Unit, Faculté des Sciences de la Santé, University of Abomey-Calavi, Cotonou 01 BP 188, Benin

M

Martin Akogbeto

Cotonou Entomological Research Center, Cotonou 06 BP 2604, Benin

Funding

Global Fund to Fight AIDS, Tuberculosis and Malaria Award: BEN-M-PNLP; 2015–2017

Cite This Article

Tatchémè Filémon Tokponnon, Razaki Ossè, Germain Gil Padonou, et al. (2023). Entomological Characteristics of Malaria Transmission across Benin: An Essential Element for Improved Deployment of Vector Control Interventions. Insects, 14(1), 52. https://doi.org/10.3390/insects14010052

Entomological Characteristics of Malaria Transmission across Benin: An Essential Element for Improved Deployment of Vector Control Interventions

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