Behavioural plasticity of Anopheles coluzzii and Anopheles arabiensis undermines LLIN community protective effect in a Sudanese-savannah village in Burkina Faso.


Journal

Parasites & vectors
ISSN: 1756-3305
Titre abrégé: Parasit Vectors
Pays: England
ID NLM: 101462774

Informations de publication

Date de publication:
01 Jun 2020
Historique:
received: 08 01 2020
accepted: 21 05 2020
entrez: 4 6 2020
pubmed: 4 6 2020
medline: 2 2 2021
Statut: epublish

Résumé

Despite the overall major impact of long-lasting insecticide treated nets (LLINs) in eliciting individual and collective protection to malaria infections, some sub-Saharan countries, including Burkina Faso, still carry a disproportionately high share of the global malaria burden. This study aims to analyse the possible entomological bases of LLIN limited impact, focusing on a LLIN-protected village in the Plateau Central region of Burkina Faso. Human landing catches (HLCs) were carried out in 2015 for 12 nights both indoors and outdoors at different time windows during the highest biting activity phase for Anopheles gambiae (s.l.). Collected specimens were morphologically and molecularly identified and processed for Plasmodium detection and L1014F insecticide-resistance allele genotyping. Almost 2000 unfed An. gambiae (s.l.) (54% Anopheles coluzzii and 44% Anopheles arabiensis) females landing on human volunteers were collected, corresponding to a median number of 23.5 females/person/hour. No significant differences were observed in median numbers of mosquitoes collected indoors and outdoors, nor between sporozoite rates in An. coluzzii (6.1%) and An. arabiensis (5.5%). The estimated median hourly entomological inoculation rate (EIR) on volunteers was 1.4 infective bites/person/hour. Results do not show evidence of the biting peak during night hours typical for An. gambiae (s.l.) in the absence of bednet protection. The frequency of the L1014F resistant allele (n = 285) was 66% in An. coluzzii and 38% in An. arabiensis. The observed biting rate and sporozoite rates are in line with the literature data available for An. gambiae (s.l.) in the same geographical area before LLIN implementation and highlight high levels of malaria transmission in the study village. Homogeneous biting rate throughout the night and lack of preference for indoor-biting activity, suggest the capacity of both An. coluzzii and An. arabiensis to adjust their host-seeking behaviour to bite humans despite bednet protection, accounting for the maintenance of high rates of mosquito infectivity and malaria transmission. These results, despite being limited to a local situation in Burkina Faso, represent a paradigmatic example of how high densities and behavioural plasticity in the vector populations may contribute to explaining the limited impact of LLINs on malaria transmission in holo-endemic Sudanese savannah areas in West Africa.

Sections du résumé

BACKGROUND BACKGROUND
Despite the overall major impact of long-lasting insecticide treated nets (LLINs) in eliciting individual and collective protection to malaria infections, some sub-Saharan countries, including Burkina Faso, still carry a disproportionately high share of the global malaria burden. This study aims to analyse the possible entomological bases of LLIN limited impact, focusing on a LLIN-protected village in the Plateau Central region of Burkina Faso.
METHODS METHODS
Human landing catches (HLCs) were carried out in 2015 for 12 nights both indoors and outdoors at different time windows during the highest biting activity phase for Anopheles gambiae (s.l.). Collected specimens were morphologically and molecularly identified and processed for Plasmodium detection and L1014F insecticide-resistance allele genotyping.
RESULTS RESULTS
Almost 2000 unfed An. gambiae (s.l.) (54% Anopheles coluzzii and 44% Anopheles arabiensis) females landing on human volunteers were collected, corresponding to a median number of 23.5 females/person/hour. No significant differences were observed in median numbers of mosquitoes collected indoors and outdoors, nor between sporozoite rates in An. coluzzii (6.1%) and An. arabiensis (5.5%). The estimated median hourly entomological inoculation rate (EIR) on volunteers was 1.4 infective bites/person/hour. Results do not show evidence of the biting peak during night hours typical for An. gambiae (s.l.) in the absence of bednet protection. The frequency of the L1014F resistant allele (n = 285) was 66% in An. coluzzii and 38% in An. arabiensis.
CONCLUSIONS CONCLUSIONS
The observed biting rate and sporozoite rates are in line with the literature data available for An. gambiae (s.l.) in the same geographical area before LLIN implementation and highlight high levels of malaria transmission in the study village. Homogeneous biting rate throughout the night and lack of preference for indoor-biting activity, suggest the capacity of both An. coluzzii and An. arabiensis to adjust their host-seeking behaviour to bite humans despite bednet protection, accounting for the maintenance of high rates of mosquito infectivity and malaria transmission. These results, despite being limited to a local situation in Burkina Faso, represent a paradigmatic example of how high densities and behavioural plasticity in the vector populations may contribute to explaining the limited impact of LLINs on malaria transmission in holo-endemic Sudanese savannah areas in West Africa.

Identifiants

pubmed: 32487147
doi: 10.1186/s13071-020-04142-x
pii: 10.1186/s13071-020-04142-x
pmc: PMC7268364
doi:

Substances chimiques

Insecticides 0

Types de publication

Journal Article

Langues

eng

Sous-ensembles de citation

IM

Pagination

277

Subventions

Organisme : Seventh Framework Programme
ID : 265660
Organisme : Sapienza Università di Roma (IT) "Avvio alla Ricerca 2019"
ID : AR11916B4CC76BF1
Organisme : Sapienza Università di Roma (IT) "Progetti di Ricerca Medi"
ID : RM11916B7AFEA99E

Références

Acta Trop. 2018 Jun;182:149-157
pubmed: 29476726
Malar J. 2009 Sep 28;8:220
pubmed: 19785766
Malar J. 2007 Aug 13;6:111
pubmed: 17697325
Trans R Soc Trop Med Hyg. 1999 Sep-Oct;93(5):473-9
pubmed: 10696400
BMJ Glob Health. 2017 Apr 26;2(2):e000198
pubmed: 28589015
Evol Appl. 2017 Oct 05;10(10):1102-1120
pubmed: 29151864
Parasit Vectors. 2012 Mar 31;5:65
pubmed: 22463735
Malar J. 2019 May 8;18(1):165
pubmed: 31068189
Malar J. 2017 Dec 29;16(1):498
pubmed: 29284476
BMC Ecol. 2009 May 21;9:17
pubmed: 19460146
Med Vet Entomol. 2008 Jun;22(2):93-108
pubmed: 18498608
Emerg Infect Dis. 2012 Feb;18(2):272-8
pubmed: 22305090
Malar J. 2010 Jun 28;9:187
pubmed: 20579399
Med Vet Entomol. 2000 Jun;14(2):171-80
pubmed: 10872861
Malar J. 2011 Dec 13;10:356
pubmed: 22165904
Parasit Vectors. 2017 Jan 11;10(1):22
pubmed: 28077167
Malar J. 2017 Feb 28;16(1):91
pubmed: 28241888
Malar J. 2014 Aug 30;13:340
pubmed: 25176292
Proc Natl Acad Sci U S A. 2019 Jul 23;116(30):15086-15095
pubmed: 31285346
Acta Trop. 2010 Jul-Aug;115(1-2):131-6
pubmed: 20206111
Parasit Vectors. 2012 Sep 26;5:212
pubmed: 23013551
Malar J. 2016 May 23;15(1):289
pubmed: 27216484
Malar J. 2012 Jun 08;11:188
pubmed: 22681999
Malar J. 2014 Aug 23;13:330
pubmed: 25149656
Med Vet Entomol. 2012 Mar;26(1):9-17
pubmed: 21501199
J Med Entomol. 1997 Jul;34(4):396-403
pubmed: 9220672
Am J Trop Med Hyg. 2009 Dec;81(6):1023-9
pubmed: 19996432
Malar J. 2013 Apr 11;12:124
pubmed: 23577656
Evolution. 2013 Apr;67(4):1218-30
pubmed: 23550770
BMC Ecol. 2009 May 21;9:16
pubmed: 19460144
Parasit Vectors. 2010 Dec 03;3:117
pubmed: 21129198
Trans R Soc Trop Med Hyg. 2004 Nov;98(11):644-52
pubmed: 15363644
Malar J. 2011 Jul 28;10:207
pubmed: 21798023
PLoS One. 2017 Nov 2;12(11):e0187059
pubmed: 29095834
Med Vet Entomol. 2018 Sep;32(3):372-377
pubmed: 29344968
Parasit Vectors. 2015 Sep 17;8:458
pubmed: 26382583
Wellcome Open Res. 2018 Dec 23;3:164
pubmed: 30756096
Malar J. 2013 Jan 08;12:13
pubmed: 23297732
Malar J. 2009 Jul 28;8:171
pubmed: 19638219
Bull Entomol Res. 1949 May;40(1):149-68
pubmed: 18130380
Trop Med Int Health. 2002 Dec;7(12):1022-30
pubmed: 12460393
Malar J. 2012 Dec 28;11:435
pubmed: 23273022
PLoS One. 2012;7(11):e48412
pubmed: 23189131
Sci Rep. 2018 Aug 24;8(1):12806
pubmed: 30143698
Parasit Vectors. 2016 Sep 30;9(1):527
pubmed: 27716416
Malar J. 2017 Sep 15;16(1):373
pubmed: 28915892
Parasit Vectors. 2014 Feb 24;7:79
pubmed: 24564957
Med Vet Entomol. 1997 Jan;11(1):71-8
pubmed: 9061680
Med Trop (Mars). 1999;59(4):349-54
pubmed: 10816746
Malar J. 2019 Apr 2;18(1):113
pubmed: 30940141
Evol Appl. 2015 Apr;8(4):326-45
pubmed: 25926878
Clin Microbiol Infect. 2013 Oct;19(10):902-7
pubmed: 23910459
Acta Trop. 2008 Jan;105(1):28-34
pubmed: 17964522
Infect Genet Evol. 2008 Sep;8(5):737-46
pubmed: 18640289
J Vector Ecol. 2008 Jun;33(1):70-5
pubmed: 18697309
Nature. 2015 Oct 8;526(7572):207-211
pubmed: 26375008
Malar J. 2011 Jul 07;10:184
pubmed: 21736750
Bull Soc Pathol Exot. 2015 Dec;108(5):360-8
pubmed: 26419486
Malar J. 2011 Jul 29;10:211
pubmed: 21801344
Trop Med Int Health. 2003 Jul;8(7):643-9
pubmed: 12828548
Parasit Vectors. 2013 Nov 04;6(1):319
pubmed: 24499508
Trans R Soc Trop Med Hyg. 2007 Sep;101(9):867-80
pubmed: 17631372
PLoS One. 2012;7(12):e52719
pubmed: 23285168
Malar J. 2018 Aug 22;17(1):307
pubmed: 30134912
PLoS One. 2014 Jul 31;9(7):e101484
pubmed: 25077792
Trends Parasitol. 2011 Feb;27(2):91-8
pubmed: 20843745
Malar J. 2010 Feb 26;9:62
pubmed: 20187956
Am J Trop Med Hyg. 2003 Apr;68(4 Suppl):121-7
pubmed: 12749495
Malar J. 2012 Jun 10;11:193
pubmed: 22682161
Acta Trop. 2018 May;181:84-94
pubmed: 29452110
Malar J. 2012 Jul 16;11:232
pubmed: 22799568
Malar J. 2008 Sep 15;7:177
pubmed: 18793416
Malar J. 2011 Apr 09;10:80
pubmed: 21477321
J Med Entomol. 2002 Mar;39(2):350-5
pubmed: 11931035
Malar J. 2015 Aug 14;14:314
pubmed: 26268225
PLoS One. 2012;7(6):e39453
pubmed: 22745756
Parasit Vectors. 2014 Aug 20;7:380
pubmed: 25141761
Med Vet Entomol. 2006 Dec;20(4):425-37
pubmed: 17199754
Malar J. 2014 Mar 19;13:109
pubmed: 24645751
Parasite Epidemiol Control. 2017 May 02;2(2):61-69
pubmed: 29774282
PLoS One. 2013;8(1):e50036
pubmed: 23320064
Parasit Vectors. 2014 Oct 07;7:450
pubmed: 25292318
Malar J. 2009 Nov 16;8:256
pubmed: 19917119
PLoS One. 2013 May 21;8(5):e63849
pubmed: 23704944
Parasit Vectors. 2012 Aug 08;5:163
pubmed: 22873930
Malar J. 2008 Aug 25;7:163
pubmed: 18724871

Auteurs

Eleonora Perugini (E)

Dipartimento di Sanità Pubblica e Malattie Infettive, Laboratory affiliated to Istituto Pasteur Italia, Fondazione Cenci Bolognetti, Sapienza Università di Roma, Rome, 00185, Italy.

Wamdaogo Moussa Guelbeogo (WM)

Centre National de Recherche et Formation sur le Paludisme (CNRFP), Ouagadougou 01, BP 2208, Burkina Faso.

Maria Calzetta (M)

Dipartimento di Sanità Pubblica e Malattie Infettive, Laboratory affiliated to Istituto Pasteur Italia, Fondazione Cenci Bolognetti, Sapienza Università di Roma, Rome, 00185, Italy.

Sara Manzi (S)

Dipartimento di Sanità Pubblica e Malattie Infettive, Laboratory affiliated to Istituto Pasteur Italia, Fondazione Cenci Bolognetti, Sapienza Università di Roma, Rome, 00185, Italy.

Chiara Virgillito (C)

Dipartimento di Sanità Pubblica e Malattie Infettive, Laboratory affiliated to Istituto Pasteur Italia, Fondazione Cenci Bolognetti, Sapienza Università di Roma, Rome, 00185, Italy.
Dipartimento di Biodiversità ed Ecologia Molecolare, Centro Ricerca e Innovazione, Fondazione Edmund Mach, San Michele all'Adige, Trento, Italy.

Beniamino Caputo (B)

Dipartimento di Sanità Pubblica e Malattie Infettive, Laboratory affiliated to Istituto Pasteur Italia, Fondazione Cenci Bolognetti, Sapienza Università di Roma, Rome, 00185, Italy.

Verena Pichler (V)

Dipartimento di Sanità Pubblica e Malattie Infettive, Laboratory affiliated to Istituto Pasteur Italia, Fondazione Cenci Bolognetti, Sapienza Università di Roma, Rome, 00185, Italy.

Hilary Ranson (H)

Department of Vector Biology, Liverpool School of Tropical Medicine, Liverpool, L3 5QA, UK.

N'Fale Sagnon (N)

Centre National de Recherche et Formation sur le Paludisme (CNRFP), Ouagadougou 01, BP 2208, Burkina Faso.

Alessandra Della Torre (A)

Dipartimento di Sanità Pubblica e Malattie Infettive, Laboratory affiliated to Istituto Pasteur Italia, Fondazione Cenci Bolognetti, Sapienza Università di Roma, Rome, 00185, Italy. ale.dellatorre@uniroma1.it.

Marco Pombi (M)

Dipartimento di Sanità Pubblica e Malattie Infettive, Laboratory affiliated to Istituto Pasteur Italia, Fondazione Cenci Bolognetti, Sapienza Università di Roma, Rome, 00185, Italy. marco.pombi@uniroma1.it.

Articles similaires

[Redispensing of expensive oral anticancer medicines: a practical application].

Lisanne N van Merendonk, Kübra Akgöl, Bastiaan Nuijen
1.00
Humans Antineoplastic Agents Administration, Oral Drug Costs Counterfeit Drugs

Smoking Cessation and Incident Cardiovascular Disease.

Jun Hwan Cho, Seung Yong Shin, Hoseob Kim et al.
1.00
Humans Male Smoking Cessation Cardiovascular Diseases Female
Humans United States Aged Cross-Sectional Studies Medicare Part C
1.00
Humans Yoga Low Back Pain Female Male

Classifications MeSH