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Published in: Malaria Journal 1/2019

Open Access 01-12-2019 | Plasmodium Falciparum | Research

Anopheles parensis contributes to residual malaria transmission in South Africa

Authors: Ashley Burke, Yael Dahan-Moss, Frances Duncan, Bheki Qwabe, Maureen Coetzee, Lizette Koekemoer, Basil Brooke

Published in: Malaria Journal | Issue 1/2019

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Abstract

Background

Understanding the contribution of outdoor-resting Anopheles mosquitoes to residual malaria transmission is important in terms of scaling up vector control towards malaria elimination in South Africa. The aim of this project was to assess the potential role of Anopheles parensis and other Anopheles species in residual malaria transmission, using sentinel surveillance sites in the uMkhanyakude District of northern KwaZulu-Natal Province.

Methods

Monthly vector surveillance was conducted at the sentinel sites from January 2017 to May 2018. Outdoor-placed clay pot resting traps were used to collect male and female adult Anopheles mosquitoes. All Anopheles gambiae complex and Anopheles funestus group specimens collected were identified to species and all females were screened for Plasmodium falciparum circumsporozoite protein (CSP) by enzyme-linked immunosorbent assay (ELISA). Samples showing infectivity for P. falciparum were further verified by a nested PCR and subsequent DNA sequence analysis.

Results

From a sample of 491 anophelines, Anopheles arabiensis (n = 228) and An. parensis (n = 194) were the most abundant. Other species collected included Anopheles merus (n =11), Anopheles quadriannulatus (n = 10), Anopheles leesoni (n = 29), Anopheles rivulorum (n =18), and Anopheles vaneedeni (n =1). Of the 317 female specimens screened for P. falciparum CSP, one Anopheles arabiensis and one An. parensis showed positive by ELISA and Plasmodium nested PCR. For the An. parensis specimen, confirmation of its species identity was based on sequence analysis of the ITS2 region, and the presence of P. falciparum DNA was further confirmed by sequence analysis.

Conclusions

Anopheles parensis is a potential vector of malaria in South Africa although its contribution to transmission is likely to be minimal at best owing to its strong zoophilic tendency. By contrast, An. arabiensis is a major vector that is primarily responsible for the bulk of residual malaria transmission in South Africa. As all recently collected sporozoite-positive Anopheles mosquitoes were found in outdoor-placed resting traps, it is necessary to introduce interventions that can be used to control outdoor-resting vector populations while maintaining the efficacy of South Africa’s indoor house spraying operations.
Literature
1.
go back to reference Maharaj R, Raman J, Morris N, Moonasar D, Durrheim DN, Seocharan I, et al. Epidemiology of malaria in South Africa: from control to elimination. S Afr Med J. 2013;103(10 Suppl 2):779–83.CrossRef Maharaj R, Raman J, Morris N, Moonasar D, Durrheim DN, Seocharan I, et al. Epidemiology of malaria in South Africa: from control to elimination. S Afr Med J. 2013;103(10 Suppl 2):779–83.CrossRef
2.
go back to reference Raman J, Morris N, Frean J, Brooke B, Blumberg L, Kruger P, et al. Reviewing South Africa’s malaria elimination strategy (2012–2018): progress, challenges and priorities. Malar J. 2016;15:438.CrossRef Raman J, Morris N, Frean J, Brooke B, Blumberg L, Kruger P, et al. Reviewing South Africa’s malaria elimination strategy (2012–2018): progress, challenges and priorities. Malar J. 2016;15:438.CrossRef
3.
go back to reference World Health Organization. World malaria report. Geneva: World Health Organization; 2018. World Health Organization. World malaria report. Geneva: World Health Organization; 2018.
4.
go back to reference Christian R, Dahan-Moss Y, Braack L, Munhenga G, Kaiser M, Lobb L, et al. Malaria vector surveillance report, South Africa, January–December, 2017. NICD Bulletin. 2018;6:1. Christian R, Dahan-Moss Y, Braack L, Munhenga G, Kaiser M, Lobb L, et al. Malaria vector surveillance report, South Africa, January–December, 2017. NICD Bulletin. 2018;6:1.
5.
go back to reference Brooke BD, Koekemoer L, Kruger P, Urbach J, Misiani E, Coetzee M. Malaria vector control in South Africa. S Afr Med J. 2013;103:784–8.CrossRef Brooke BD, Koekemoer L, Kruger P, Urbach J, Misiani E, Coetzee M. Malaria vector control in South Africa. S Afr Med J. 2013;103:784–8.CrossRef
6.
go back to reference Coetzee M, Hunt RH, Wilkerson R, Della Torre A, Coulibaly MB, Besanksky NJ. Anopheles coluzzii and Anopheles amharicus, new members of the Anopheles gambiae complex. Zootaxa. 2013;3619:246.CrossRef Coetzee M, Hunt RH, Wilkerson R, Della Torre A, Coulibaly MB, Besanksky NJ. Anopheles coluzzii and Anopheles amharicus, new members of the Anopheles gambiae complex. Zootaxa. 2013;3619:246.CrossRef
7.
go back to reference Dandalo LC, Brooke BD, Munhenga G, Lobb LN, Zikhali J, Ngxongo SP, et al. Population dynamics and Plasmodium falciparum (Haemosporida: Plasmodiidae) infectivity rates for the malaria vector Anopheles arabiensis (Diptera: Culicidae) at Mamfene, KwaZulu-Natal. J Med Entomol. 2017;54(6):1758–66.CrossRef Dandalo LC, Brooke BD, Munhenga G, Lobb LN, Zikhali J, Ngxongo SP, et al. Population dynamics and Plasmodium falciparum (Haemosporida: Plasmodiidae) infectivity rates for the malaria vector Anopheles arabiensis (Diptera: Culicidae) at Mamfene, KwaZulu-Natal. J Med Entomol. 2017;54(6):1758–66.CrossRef
8.
go back to reference Cuamba N, Mendis C. The role of Anopheles merus in malaria transmission in an area of southern Mozambique. J Vector Borne Dis. 2009;46:157–9.PubMed Cuamba N, Mendis C. The role of Anopheles merus in malaria transmission in an area of southern Mozambique. J Vector Borne Dis. 2009;46:157–9.PubMed
9.
go back to reference Mbokazi F, Coetzee M, Brooke B, Govere J, Reid A, Owiti P, et al. Changing distribution and abundance of the malaria vector Anopheles merus in Mpumalanga Province, South Africa. Public Health Action. 2018;8(Suppl 1):S39–43.CrossRef Mbokazi F, Coetzee M, Brooke B, Govere J, Reid A, Owiti P, et al. Changing distribution and abundance of the malaria vector Anopheles merus in Mpumalanga Province, South Africa. Public Health Action. 2018;8(Suppl 1):S39–43.CrossRef
10.
go back to reference Coetzee M, Craig M, Le Sueur D. Distribution of African malaria mosquitoes belonging to the Anopheles gambiae complex. Parasitol Today. 2000;16:74–7.CrossRef Coetzee M, Craig M, Le Sueur D. Distribution of African malaria mosquitoes belonging to the Anopheles gambiae complex. Parasitol Today. 2000;16:74–7.CrossRef
11.
go back to reference Coetzee M, Koekemoer LL. Molecular systematics and insecticide resistance in the major African malaria vector Anopheles funestus. Annu Rev Entomol. 2013;58:393–412.CrossRef Coetzee M, Koekemoer LL. Molecular systematics and insecticide resistance in the major African malaria vector Anopheles funestus. Annu Rev Entomol. 2013;58:393–412.CrossRef
12.
go back to reference Burke A, Dandalo L, Munhenga G, Dahan-Moss Y, Mbokazi F, Ngxongo S, et al. A new malaria vector mosquito in South Africa. Sci Rep. 2017;7:43779.CrossRef Burke A, Dandalo L, Munhenga G, Dahan-Moss Y, Mbokazi F, Ngxongo S, et al. A new malaria vector mosquito in South Africa. Sci Rep. 2017;7:43779.CrossRef
13.
go back to reference Wilkes TJ, Matola YG, Charlwood JD. Anopheles rivulorum, a vector of human malaria in Africa. Med Vet Entomol. 1996;10:108–10.CrossRef Wilkes TJ, Matola YG, Charlwood JD. Anopheles rivulorum, a vector of human malaria in Africa. Med Vet Entomol. 1996;10:108–10.CrossRef
14.
go back to reference Temu EA, Minjas JN, Tuno N, Kawada H, Takagi M. Identification of four members of the Anopheles funestus (Diptera: Culicidae) group and their role in Plasmodium falciparum transmission in Bagamoyo coastal Tanzania. Acta Trop. 2007;102:119–25.CrossRef Temu EA, Minjas JN, Tuno N, Kawada H, Takagi M. Identification of four members of the Anopheles funestus (Diptera: Culicidae) group and their role in Plasmodium falciparum transmission in Bagamoyo coastal Tanzania. Acta Trop. 2007;102:119–25.CrossRef
15.
go back to reference Kyalo D, Amratia P, Mundia CW, Mbogo CM, Coetzee M, Snow RW. A geo-coded inventory of anophelines in the Afrotropical Region south of the Sahara: 1898–2016. Wellcome Open Res. 2017;2:57.CrossRef Kyalo D, Amratia P, Mundia CW, Mbogo CM, Coetzee M, Snow RW. A geo-coded inventory of anophelines in the Afrotropical Region south of the Sahara: 1898–2016. Wellcome Open Res. 2017;2:57.CrossRef
16.
go back to reference Kawada H, Dida GO, Sonye G, Njenga SM, Mwandawiro C, Minakawa N. Reconsideration of Anopheles rivulorum as a vector of Plasmodium falciparum in western Kenya: some evidence from biting time, blood preference, sporozoite positive rate, and pyrethroid resistance. Parasit Vectors. 2012;5:230.CrossRef Kawada H, Dida GO, Sonye G, Njenga SM, Mwandawiro C, Minakawa N. Reconsideration of Anopheles rivulorum as a vector of Plasmodium falciparum in western Kenya: some evidence from biting time, blood preference, sporozoite positive rate, and pyrethroid resistance. Parasit Vectors. 2012;5:230.CrossRef
17.
go back to reference Ogola EO, Fillinger U, Ondiba IM, Villinger J, Masiga DK, Torto B, et al. Insights into malaria transmission among Anopheles funestus mosquitoes, Kenya. Parasit Vectors. 2018;11:577.CrossRef Ogola EO, Fillinger U, Ondiba IM, Villinger J, Masiga DK, Torto B, et al. Insights into malaria transmission among Anopheles funestus mosquitoes, Kenya. Parasit Vectors. 2018;11:577.CrossRef
18.
go back to reference Kamau L, Koekemoer LL, Hunt RH, Coetzee M. Anopheles parensis: the main member of the Anopheles funestus species group found resting inside human dwellings in Mwea area of central Kenya toward the end of the rainy season. J Am Mosq Control Assoc. 2003;19:130–3.PubMed Kamau L, Koekemoer LL, Hunt RH, Coetzee M. Anopheles parensis: the main member of the Anopheles funestus species group found resting inside human dwellings in Mwea area of central Kenya toward the end of the rainy season. J Am Mosq Control Assoc. 2003;19:130–3.PubMed
19.
go back to reference Mouatcho JC, Hargreaves K, Koekemoer LL, Brooke BD, Oliver SV, Hunt RH, et al. Indoor collections of the Anopheles funestus group (Diptera: Culicidae) in sprayed houses in northern KwaZulu-Natal, South Africa. Malar J. 2007;6:30.CrossRef Mouatcho JC, Hargreaves K, Koekemoer LL, Brooke BD, Oliver SV, Hunt RH, et al. Indoor collections of the Anopheles funestus group (Diptera: Culicidae) in sprayed houses in northern KwaZulu-Natal, South Africa. Malar J. 2007;6:30.CrossRef
20.
go back to reference Mulamba JC, Hargreaves K, Koekemoer LL, Brooke BD, Oliver SV, Hunt RH, et al. Contrasting Plasmodium infection rates and insecticide susceptibility profiles between the sympatric sibling species Anopheles parensis and Anopheles funestus s.s.: a potential challenge for malaria vector control in Uganda. Parasit Vectors. 2014;7:71.CrossRef Mulamba JC, Hargreaves K, Koekemoer LL, Brooke BD, Oliver SV, Hunt RH, et al. Contrasting Plasmodium infection rates and insecticide susceptibility profiles between the sympatric sibling species Anopheles parensis and Anopheles funestus s.s.: a potential challenge for malaria vector control in Uganda. Parasit Vectors. 2014;7:71.CrossRef
21.
go back to reference Gillies MT, Coetzee M. A supplement to the Anophelinae of Africa South of the Sahara (Afrotropical region). Johannesburg: South African Institute for Medical Research; 1987. Gillies MT, Coetzee M. A supplement to the Anophelinae of Africa South of the Sahara (Afrotropical region). Johannesburg: South African Institute for Medical Research; 1987.
22.
go back to reference Scott JA, Brogdon WG, Collins FH. Identification of single specimens of the Anopheles gambiae complex by the polymerase chain reaction. Am J Trop Med Hyg. 1993;49:520–9.CrossRef Scott JA, Brogdon WG, Collins FH. Identification of single specimens of the Anopheles gambiae complex by the polymerase chain reaction. Am J Trop Med Hyg. 1993;49:520–9.CrossRef
23.
go back to reference Koekemoer LL, Kamau L, Hunt RH, Coetzee M. A cocktail polymerase chain reaction assay to identify members of the Anopheles funestus (diptera: culicidae) group. Am J Trop Med Hyg. 2002;6:804–11.CrossRef Koekemoer LL, Kamau L, Hunt RH, Coetzee M. A cocktail polymerase chain reaction assay to identify members of the Anopheles funestus (diptera: culicidae) group. Am J Trop Med Hyg. 2002;6:804–11.CrossRef
24.
go back to reference Cohuet A, Simard F, Toto JC, Kengne P, Coetzee M, Fontenille D. Species identification within the Anopheles funestus group of malaria vectors in Cameroon and evidence for a new species. Am J Trop Med Hyg. 2003;69:200–5.CrossRef Cohuet A, Simard F, Toto JC, Kengne P, Coetzee M, Fontenille D. Species identification within the Anopheles funestus group of malaria vectors in Cameroon and evidence for a new species. Am J Trop Med Hyg. 2003;69:200–5.CrossRef
25.
go back to reference Wirtz RA, Zavala F, Charoenvit Y, Campbell GH, Burkot TR, Schneider I, et al. Comparative testing of monoclonal antibodies against Plasmodium falciparum sporozoites for ELISA development. Bull World Health Organ. 1987;65:39–45.PubMedPubMedCentral Wirtz RA, Zavala F, Charoenvit Y, Campbell GH, Burkot TR, Schneider I, et al. Comparative testing of monoclonal antibodies against Plasmodium falciparum sporozoites for ELISA development. Bull World Health Organ. 1987;65:39–45.PubMedPubMedCentral
26.
go back to reference Burkot TR, Williams JL, Schneider I. Identification of Plasmodium falciparum-infected mosquitoes by a double antibody enzyme-linked immunosorbent assay. Am J Trop Med Hyg. 1984;33:783–8.CrossRef Burkot TR, Williams JL, Schneider I. Identification of Plasmodium falciparum-infected mosquitoes by a double antibody enzyme-linked immunosorbent assay. Am J Trop Med Hyg. 1984;33:783–8.CrossRef
27.
go back to reference Durnez L, Van Bortel W, Denis L, Roelants P, Veracx A, Trung HD, et al. False positive circumsporozoite protein ELISA: a challenge for the estimation of the entomological inoculation rate of malaria and for vector incrimination. Malar J. 2011;10:195.CrossRef Durnez L, Van Bortel W, Denis L, Roelants P, Veracx A, Trung HD, et al. False positive circumsporozoite protein ELISA: a challenge for the estimation of the entomological inoculation rate of malaria and for vector incrimination. Malar J. 2011;10:195.CrossRef
28.
go back to reference Snounou G, Viriyakosol S, Zhu XP, Jarra W, Pinheiro L, Rosario VE, et al. High sensitivity of detection of human malaria parasites by the use of nested polymerase chain reaction. Mol Biochem Parasitol. 1993;6:315–20.CrossRef Snounou G, Viriyakosol S, Zhu XP, Jarra W, Pinheiro L, Rosario VE, et al. High sensitivity of detection of human malaria parasites by the use of nested polymerase chain reaction. Mol Biochem Parasitol. 1993;6:315–20.CrossRef
29.
go back to reference Norris LC, Norris DE. Phylogeny of anopheline (Diptera: Culicidae) species in southern Africa, based on nuclear and mitochondrial genes. J Vector Ecol. 2015;40:16–27.CrossRef Norris LC, Norris DE. Phylogeny of anopheline (Diptera: Culicidae) species in southern Africa, based on nuclear and mitochondrial genes. J Vector Ecol. 2015;40:16–27.CrossRef
30.
go back to reference Ngassa Mbenda HG, Das A. Molecular evidence of Plasmodium vivax mono and mixed malaria parasite infections in Duffy-negative native Cameroonians. PLoS One. 2014;9:e103262.CrossRef Ngassa Mbenda HG, Das A. Molecular evidence of Plasmodium vivax mono and mixed malaria parasite infections in Duffy-negative native Cameroonians. PLoS One. 2014;9:e103262.CrossRef
31.
go back to reference Erlank E, Koekemoer LL, Coetzee M. The importance of morphological identification of African anopheline mosquitoes (Diptera: Culicidae) for malaria control programmes. Malar J. 2018;17:43.CrossRef Erlank E, Koekemoer LL, Coetzee M. The importance of morphological identification of African anopheline mosquitoes (Diptera: Culicidae) for malaria control programmes. Malar J. 2018;17:43.CrossRef
32.
go back to reference Bass C, Nikou D, Blagborough AM, Vontas J, Sinden RE, Martin S, Williamson MS, et al. PCR-based detection of Plasmodium in Anopheles mosquitoes: a comparison of a new high-throughput assay with existing methods. Malar J. 2008;7:177.CrossRef Bass C, Nikou D, Blagborough AM, Vontas J, Sinden RE, Martin S, Williamson MS, et al. PCR-based detection of Plasmodium in Anopheles mosquitoes: a comparison of a new high-throughput assay with existing methods. Malar J. 2008;7:177.CrossRef
33.
go back to reference Kefi M, Mavridis K, Simões ML, Dimopoulos G, Siden-Kiamos I, Vontas J. New rapid one-step PCR diagnostic assay for Plasmodium falciparum infective mosquitoes. Sci Rep. 2018;8:1462.CrossRef Kefi M, Mavridis K, Simões ML, Dimopoulos G, Siden-Kiamos I, Vontas J. New rapid one-step PCR diagnostic assay for Plasmodium falciparum infective mosquitoes. Sci Rep. 2018;8:1462.CrossRef
34.
go back to reference Muturi EJ, Kamau L, Jacob BG, Muriu S, Mbogo CM, Shililu J, et al. Spatial distribution, blood feeding pattern, and role of Anopheles funestus complex in malaria transmission in central Kenya. Parasitol Res. 2009;105:1041–6.CrossRef Muturi EJ, Kamau L, Jacob BG, Muriu S, Mbogo CM, Shililu J, et al. Spatial distribution, blood feeding pattern, and role of Anopheles funestus complex in malaria transmission in central Kenya. Parasitol Res. 2009;105:1041–6.CrossRef
35.
go back to reference Gillies MT, De Meillon B. The Anophelinae of Africa south of the Sahara (Ethiopian zoogeographical region). Johannesburg: South African Institute for Medical Research; 1968. Gillies MT, De Meillon B. The Anophelinae of Africa south of the Sahara (Ethiopian zoogeographical region). Johannesburg: South African Institute for Medical Research; 1968.
36.
go back to reference Kweka EJ, Mahande AM, Nkya WM, Assenga C, Lyatuu EE, Nyale E, et al. Vector species composition and malaria infectivity rates in Mkuzi, Muheza District, north-eastern Tanzania. Tanzan J Health Res. 2008;10:46–9.CrossRef Kweka EJ, Mahande AM, Nkya WM, Assenga C, Lyatuu EE, Nyale E, et al. Vector species composition and malaria infectivity rates in Mkuzi, Muheza District, north-eastern Tanzania. Tanzan J Health Res. 2008;10:46–9.CrossRef
37.
go back to reference Kamau L, Munyekenye GO, Koekemoer LL, Hunt RH, Coetzee M. A survey of the Anopheles funestus (Diptera: Culicidae) group of mosquitoes from 10 sites in Kenya with special emphasis on population genetic structure based on chromosomal inversion karyotypes. J Med Entomol. 2003;40:664–71.CrossRef Kamau L, Munyekenye GO, Koekemoer LL, Hunt RH, Coetzee M. A survey of the Anopheles funestus (Diptera: Culicidae) group of mosquitoes from 10 sites in Kenya with special emphasis on population genetic structure based on chromosomal inversion karyotypes. J Med Entomol. 2003;40:664–71.CrossRef
38.
go back to reference Sinka ME, Bangs MJ, Manguin S, Rubio-Palis Y, Chareonviriyaphap T, Coetzee M, et al. A global map of dominant malaria vectors. Parasit Vectors. 2012;5:69.CrossRef Sinka ME, Bangs MJ, Manguin S, Rubio-Palis Y, Chareonviriyaphap T, Coetzee M, et al. A global map of dominant malaria vectors. Parasit Vectors. 2012;5:69.CrossRef
39.
go back to reference Hall TA. BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Symp Ser. 1999;41:95–8. Hall TA. BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Symp Ser. 1999;41:95–8.
Metadata
Title
Anopheles parensis contributes to residual malaria transmission in South Africa
Authors
Ashley Burke
Yael Dahan-Moss
Frances Duncan
Bheki Qwabe
Maureen Coetzee
Lizette Koekemoer
Basil Brooke
Publication date
01-12-2019
Publisher
BioMed Central
Published in
Malaria Journal / Issue 1/2019
Electronic ISSN: 1475-2875
DOI
https://doi.org/10.1186/s12936-019-2889-5

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