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Published in: Malaria Journal 1/2020

Open Access 01-12-2020 | Malaria | Research

High levels of imported asymptomatic malaria but limited local transmission in KwaZulu-Natal, a South African malaria-endemic province nearing malaria elimination

Authors: Jaishree Raman, Laura Gast, Ryleen Balawanth, Sofonias Tessema, Basil Brooke, Rajendra Maharaj, Givemore Munhenga, Power Tshikae, Vishan Lakan, Tshiama Mwamba, Hazel Makowa, Lindi Sangweni, Moses Mkhabela, Nompumelelo Zondo, Ernest Mohulatsi, Zuziwe Nyawo, Sifiso Ngxongo, Sipho Msimang, Nicole Dagata, Bryan Greenhouse, Lyn-Marie Birkholtz, George Shirreff, Rebecca Graffy, Bheki Qwabe, Devanand Moonasar

Published in: Malaria Journal | Issue 1/2020

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Abstract

Background

KwaZulu-Natal, one of South Africa’s three malaria endemic provinces, is nearing malaria elimination, reporting fewer than 100 locally-acquired cases annually since 2010. Despite sustained implementation of essential interventions, including annual indoor residual spraying, prompt case detection using malaria rapid diagnostics tests and treatment with effective artemisinin-based combination therapy, low-level focal transmission persists in the province. This malaria prevalence and entomological survey was therefore undertaken to identify the drivers of this residual transmission.

Methods

Malaria prevalence as well as malaria knowledge, attitudes and practices among community members and mobile migrant populations within uMkhanyakude district, KwaZulu-Natal were assessed during a community-based malaria prevalence survey. All consenting participants were tested for malaria by both conventional and highly-sensitive falciparum-specific rapid diagnostic tests. Finger-prick filter-paper blood spots were also collected from all participants for downstream parasite genotyping analysis. Entomological investigations were conducted around the surveyed households, with potential breeding sites geolocated and larvae collected for species identification and insecticide susceptibility testing. A random selection of households were assessed for indoor residual spray quality by cone bioassay.

Results

A low malaria prevalence was confirmed in the study area, with only 2% (67/2979) of the participants found to be malaria positive by both conventional and highly-sensitive falciparum-specific rapid diagnostic tests. Malaria prevalence however differed markedly between the border market and community (p < 0001), with the majority of the detected malaria carriers (65/67) identified as asymptomatic Mozambican nationals transiting through the informal border market from Mozambique to economic hubs within South Africa. Genomic analysis of the malaria isolates revealed a high degree of heterozygosity and limited genetic relatedness between the isolates supporting the hypothesis of limited local malaria transmission within the province. New potential vector breeding sites, potential vector populations with reduced insecticide susceptibility and areas with sub-optimal vector intervention coverage were identified during the entomological investigations.

Conclusion

If KwaZulu-Natal is to successfully halt local malaria transmission and prevent the re-introduction of malaria, greater efforts need to be placed on detecting and treating malaria carriers at both formal and informal border crossings with transmission blocking anti-malarials, while ensuring optimal coverage of vector control interventions is achieved.
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Literature
1.
go back to reference South Africa National Department of Health. Malaria elimination strategy for South Africa 2012–2018. Pretoria: South African National Department of Health; 2012. South Africa National Department of Health. Malaria elimination strategy for South Africa 2012–2018. Pretoria: South African National Department of Health; 2012.
2.
go back to reference South African Development Community. SADC Malaria Status Report, 2017. South African Development Community. SADC Malaria Status Report, 2017.
4.
go back to reference South Africa National Department of Health. Malaria elimination strategic plan for South Africa 2019–2023. Pretoria: South African National Department of Health; 2019. South Africa National Department of Health. Malaria elimination strategic plan for South Africa 2019–2023. Pretoria: South African National Department of Health; 2019.
5.
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
6.
go back to reference Bredenkamp BL, Sharp BL, Mtembu SD, Durrheim DN, Barnes KI. Failure of sulfadoxine-pyrimethamine in treating Plasmodium falciparum malaria in KwaZulu-Natal. S Afr Med J. 2001;91:970–2.PubMed Bredenkamp BL, Sharp BL, Mtembu SD, Durrheim DN, Barnes KI. Failure of sulfadoxine-pyrimethamine in treating Plasmodium falciparum malaria in KwaZulu-Natal. S Afr Med J. 2001;91:970–2.PubMed
7.
go back to reference Roper C, Pearce R, Bredenkamp B, Gumede J, Drakeley C, Mosha F, et al. Antifolate antimalarial resistance in southeast Africa: a population-based analysis. Lancet. 2003;316:1174–81.CrossRef Roper C, Pearce R, Bredenkamp B, Gumede J, Drakeley C, Mosha F, et al. Antifolate antimalarial resistance in southeast Africa: a population-based analysis. Lancet. 2003;316:1174–81.CrossRef
8.
go back to reference Hargreaves K, Koekemoer LL, Brooke BD, Hunt RH, Mthembu J, Coetzee M. Anopheles funestus resistant to pyrethroid insecticide in South Africa. Med Vet Entomol. 2000;14:181–9.CrossRef Hargreaves K, Koekemoer LL, Brooke BD, Hunt RH, Mthembu J, Coetzee M. Anopheles funestus resistant to pyrethroid insecticide in South Africa. Med Vet Entomol. 2000;14:181–9.CrossRef
9.
go back to reference Barnes KI, Durrheim DN, Little F, Jackson A, Mehta U, Allen E, et al. Effect of artemether–lumefantrine policy and improved vector control on malaria burden in KwaZulu-Natal, South. PLoS Med. 2005;11:e330.CrossRef Barnes KI, Durrheim DN, Little F, Jackson A, Mehta U, Allen E, et al. Effect of artemether–lumefantrine policy and improved vector control on malaria burden in KwaZulu-Natal, South. PLoS Med. 2005;11:e330.CrossRef
10.
go back to reference Maharaj R, Mthembu DJ, Sharp BL. Impact of DDT re-introduction on malaria transmission in KwaZulu-Natal. S Afr Med J. 2005;95:871–4.PubMed Maharaj R, Mthembu DJ, Sharp BL. Impact of DDT re-introduction on malaria transmission in KwaZulu-Natal. S Afr Med J. 2005;95:871–4.PubMed
11.
go back to reference Maharaj R, Moonasar D, Baltazar C, Kunene S, Morris N. Sustaining control: lessons from the Lubombo spatial development initiative in southern Africa. Malar J. 2016;15:409.CrossRef Maharaj R, Moonasar D, Baltazar C, Kunene S, Morris N. Sustaining control: lessons from the Lubombo spatial development initiative in southern Africa. Malar J. 2016;15:409.CrossRef
13.
go back to reference South African Development Community, SADC Malaria Status by 2014 Report, 2015. South African Development Community, SADC Malaria Status by 2014 Report, 2015.
14.
go back to reference South African National Department of Health. National guidelines for the treatment of malaria, South Africa, 2018. Pretoria: Technical report, South African Department of Health; 2018. South African National Department of Health. National guidelines for the treatment of malaria, South Africa, 2018. Pretoria: Technical report, South African Department of Health; 2018.
15.
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, South Africa. J Med Entomol. 2017;54:1758–66.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, South Africa. J Med Entomol. 2017;54:1758–66.CrossRef
17.
go back to reference Hsaing MS, Lin M, Dokomajilar C, Kemere J, Plicher CD, Dorsey G, et al. PCR-based pooling of dried blood spots for detection of malaria parasites: optimization and application to a cohort of Ugandan children. J Clin Microbiol. 2010;48:3539–43.CrossRef Hsaing MS, Lin M, Dokomajilar C, Kemere J, Plicher CD, Dorsey G, et al. PCR-based pooling of dried blood spots for detection of malaria parasites: optimization and application to a cohort of Ugandan children. J Clin Microbiol. 2010;48:3539–43.CrossRef
18.
go back to reference Talundzic E, Chenet SM, Goldman IF, Patel DS, Nelson JA, Plucinski MM, et al. Genetic analysis and species specific amplification of the artemisinin resistance-associated kelch propeller domain in P. falciparum and P. vivax. PLoS ONE. 2015;10:e0136099.CrossRef Talundzic E, Chenet SM, Goldman IF, Patel DS, Nelson JA, Plucinski MM, et al. Genetic analysis and species specific amplification of the artemisinin resistance-associated kelch propeller domain in P. falciparum and P. vivax. PLoS ONE. 2015;10:e0136099.CrossRef
19.
go back to reference Price RN, Uhlemann AC, Brockman A, McGready R, Ashley E, Phaipun L, et al. Mefloquine resistance in Plasmodium falciparum and increased pfmdr1 gene copy number. Lancet. 2004;364:438–47.CrossRef Price RN, Uhlemann AC, Brockman A, McGready R, Ashley E, Phaipun L, et al. Mefloquine resistance in Plasmodium falciparum and increased pfmdr1 gene copy number. Lancet. 2004;364:438–47.CrossRef
20.
go back to reference Sutherland CJ, Haustein T, Gadalla N, Amstrong M, Doherty JF, Choidini PL. Chloroquine-resistant Plasmodium falciparum infections among UK travellers returning with malaria after chloroquine prophylaxis. Antimicrob Agents Chemother. 2007;59:1197–9.CrossRef Sutherland CJ, Haustein T, Gadalla N, Amstrong M, Doherty JF, Choidini PL. Chloroquine-resistant Plasmodium falciparum infections among UK travellers returning with malaria after chloroquine prophylaxis. Antimicrob Agents Chemother. 2007;59:1197–9.CrossRef
21.
go back to reference Tessema S, Wesolowski A, Chen A, Murphy M, Wilheim J, Mupiri A-R, et al. Using parasite genetic and human mobility data to infer local and cross border malaria connectivity in Southern Africa. eLife. 2019;8:e43510.CrossRef Tessema S, Wesolowski A, Chen A, Murphy M, Wilheim J, Mupiri A-R, et al. Using parasite genetic and human mobility data to infer local and cross border malaria connectivity in Southern Africa. eLife. 2019;8:e43510.CrossRef
22.
go back to reference Mlambo G, Vasquez Y, LeBlanc R, Sullivan D, Kumar N. Short report: a filter paper method for the detection of Plasmodium falciparum gametocytes by reverse transcription-polymerase chain reaction. Am J Trop Med Hyg. 2008;78:114–6.CrossRef Mlambo G, Vasquez Y, LeBlanc R, Sullivan D, Kumar N. Short report: a filter paper method for the detection of Plasmodium falciparum gametocytes by reverse transcription-polymerase chain reaction. Am J Trop Med Hyg. 2008;78:114–6.CrossRef
23.
go back to reference Gillies MT, de Meillion BL. The Anophelinae of Africa south of the Sahara (Afrotropical Region). Johannesburg: South African Institute for Medical Research; 1968. Gillies MT, de Meillion BL. The Anophelinae of Africa south of the Sahara (Afrotropical Region). Johannesburg: South African Institute for Medical Research; 1968.
24.
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.
26.
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;66:804–11.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;66:804–11.CrossRef
27.
go back to reference Scott JA, Brogdon WG, Collins FH. Identification of single specimens of the Anopheles gambiae complex. 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. Am J Trop Med Hyg. 1993;49:520–9.CrossRef
28.
go back to reference Strano E, Viana MP, Sorichetta A, Tatem AJ. Mapping road network communities for guiding disease surveillance and control strategies. Sci Rep. 2019;8:4744.CrossRef Strano E, Viana MP, Sorichetta A, Tatem AJ. Mapping road network communities for guiding disease surveillance and control strategies. Sci Rep. 2019;8:4744.CrossRef
29.
go back to reference Silal SP, Little F, Barnes KI, White LJ. Predicting the impact of border control on malaria transmission: a simulated focal screen and treat campaign. Malar J. 2015;14:268.CrossRef Silal SP, Little F, Barnes KI, White LJ. Predicting the impact of border control on malaria transmission: a simulated focal screen and treat campaign. Malar J. 2015;14:268.CrossRef
30.
go back to reference Tatem AJ, Jai P, Ordanovich D, Falkerner M, Huang Z, Howes R, et al. The geography of imported malaria to non-endemic countries: a meta-analysis of nationally reported statistics. Lancet Infect Dis. 2017;17:98–107.CrossRef Tatem AJ, Jai P, Ordanovich D, Falkerner M, Huang Z, Howes R, et al. The geography of imported malaria to non-endemic countries: a meta-analysis of nationally reported statistics. Lancet Infect Dis. 2017;17:98–107.CrossRef
31.
go back to reference Saita A, Pan-ngum W, Phuanukoonnon S, Sriwichai P, Silawan T, White LJ, et al. Human population movement and behavioural patterns in malaria hotspots on the Thai–Myanmar border: implications for malaria elimination. Malar J. 2019;18:64.CrossRef Saita A, Pan-ngum W, Phuanukoonnon S, Sriwichai P, Silawan T, White LJ, et al. Human population movement and behavioural patterns in malaria hotspots on the Thai–Myanmar border: implications for malaria elimination. Malar J. 2019;18:64.CrossRef
32.
go back to reference Moonasar D, Maharaj R, Kunene S, Candrinho B, Saute F, Ntshalintshali N, et al. Towards malaria elimination in the MOSASWA (Mozambique, South Africa and Swaziland) region. Malar J. 2016;15:419.CrossRef Moonasar D, Maharaj R, Kunene S, Candrinho B, Saute F, Ntshalintshali N, et al. Towards malaria elimination in the MOSASWA (Mozambique, South Africa and Swaziland) region. Malar J. 2016;15:419.CrossRef
33.
go back to reference Mwesigwa J, Slater H, Bradley J, Saidy B, Ceesay F, Wittaker C, et al. Field performance of the highly sensitive rapid diagnostic test in a setting of varying malaria transmission. Malar J. 2019;18:288.CrossRef Mwesigwa J, Slater H, Bradley J, Saidy B, Ceesay F, Wittaker C, et al. Field performance of the highly sensitive rapid diagnostic test in a setting of varying malaria transmission. Malar J. 2019;18:288.CrossRef
34.
go back to reference Girma S, Cheaveau J, Mohon AN, Marasignhe D, Legese R, Balasingam N, et al. Prevalence and epidemiological characteristics of asymptomatic malaria based on ultrasensitive diagnostics: a cross-sectional study. Clin Infect Dis. 2019;69:1003–10.CrossRef Girma S, Cheaveau J, Mohon AN, Marasignhe D, Legese R, Balasingam N, et al. Prevalence and epidemiological characteristics of asymptomatic malaria based on ultrasensitive diagnostics: a cross-sectional study. Clin Infect Dis. 2019;69:1003–10.CrossRef
35.
go back to reference Awandu SS, Raman J, Bousema T, Birkholtz L-M. Ultralow-density Plasmodium falciparum infections in African settings. Clin Infect Dis. 2019;69:1463–4.CrossRef Awandu SS, Raman J, Bousema T, Birkholtz L-M. Ultralow-density Plasmodium falciparum infections in African settings. Clin Infect Dis. 2019;69:1463–4.CrossRef
36.
go back to reference Chen I, Clarke SE, Gosling R, Hamainza B, Killeen G, Magill A, et al. Asymptomatic malaria: a chronic and debilitating infection that should be treated. PLoS Med. 2016;19:e1001942.CrossRef Chen I, Clarke SE, Gosling R, Hamainza B, Killeen G, Magill A, et al. Asymptomatic malaria: a chronic and debilitating infection that should be treated. PLoS Med. 2016;19:e1001942.CrossRef
37.
go back to reference Imwong M, Nguyen TN, Tripura R, Peto TJ, Lee SJ, Lwin KM, et al. The epidemiology of subclinical malaria infections in South–East Asia: findings from cross-sectional surveys in Thailand–Myanmar border areas, Cambodia and Vietnam. Malar J. 2015;14:381.CrossRef Imwong M, Nguyen TN, Tripura R, Peto TJ, Lee SJ, Lwin KM, et al. The epidemiology of subclinical malaria infections in South–East Asia: findings from cross-sectional surveys in Thailand–Myanmar border areas, Cambodia and Vietnam. Malar J. 2015;14:381.CrossRef
38.
go back to reference Manana PN, Kuonza L, Musekiwa A, Mpangane HD, Koekemoer LL. Knowledge, attitudes and practices on malaria transmission in Mamfene, KwaZulu-Natal Province, South Africa 2015. BMC Public Health. 2018;18:41.CrossRef Manana PN, Kuonza L, Musekiwa A, Mpangane HD, Koekemoer LL. Knowledge, attitudes and practices on malaria transmission in Mamfene, KwaZulu-Natal Province, South Africa 2015. BMC Public Health. 2018;18:41.CrossRef
39.
go back to reference Stuckey EM, Miller JM, Littrell M, Chitnis N, Steketee R. Operational strategies of anti-malarial drug campaigns for malaria elimination in Zambia’s southern province: a simulation study. Malar J. 2016;15:148.CrossRef Stuckey EM, Miller JM, Littrell M, Chitnis N, Steketee R. Operational strategies of anti-malarial drug campaigns for malaria elimination in Zambia’s southern province: a simulation study. Malar J. 2016;15:148.CrossRef
40.
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
41.
go back to reference Riveron JM, Huijben S, Tchapga W, Tchouakui M, Wondji MM, Tchoupo M, et al. Escalation of pyrethroid resistance in the malaria vector Anopheles funestus induces a loss of efficacy of PBO-based insecticide-treated nets in Mozambique. J Infect Dis. 2019;220:467–75.CrossRef Riveron JM, Huijben S, Tchapga W, Tchouakui M, Wondji MM, Tchoupo M, et al. Escalation of pyrethroid resistance in the malaria vector Anopheles funestus induces a loss of efficacy of PBO-based insecticide-treated nets in Mozambique. J Infect Dis. 2019;220:467–75.CrossRef
Metadata
Title
High levels of imported asymptomatic malaria but limited local transmission in KwaZulu-Natal, a South African malaria-endemic province nearing malaria elimination
Authors
Jaishree Raman
Laura Gast
Ryleen Balawanth
Sofonias Tessema
Basil Brooke
Rajendra Maharaj
Givemore Munhenga
Power Tshikae
Vishan Lakan
Tshiama Mwamba
Hazel Makowa
Lindi Sangweni
Moses Mkhabela
Nompumelelo Zondo
Ernest Mohulatsi
Zuziwe Nyawo
Sifiso Ngxongo
Sipho Msimang
Nicole Dagata
Bryan Greenhouse
Lyn-Marie Birkholtz
George Shirreff
Rebecca Graffy
Bheki Qwabe
Devanand Moonasar
Publication date
01-12-2020
Publisher
BioMed Central
Keyword
Malaria
Published in
Malaria Journal / Issue 1/2020
Electronic ISSN: 1475-2875
DOI
https://doi.org/10.1186/s12936-020-03227-3

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