The Open Public Health Journal




ISSN: 1874-9445 ― Volume 13, 2020
REVIEW ARTICLE

Investigating the Resurgence of Malaria Prevalence in South Africa Between 2015 and 2018: A Scoping Review



Gbenga J. Abiodun1, *, Babatope. O. Adebiyi2, Rita O. Abiodun3, Olanrewaju Oladimeji4, 5, 6, Kelechi E. Oladimeji4, 7, Abiodun M. Adeola8, 9, Olusola S. Makinde10, Kazeem O. Okosun11, Ramsès Djidjou-Demasse12, Yves J. Semegni13, Kevin Y. Njabo14, Peter J. Witbooi15, Alejandro Aceves1
1 Department of Mathematics, Southern Methodist University, Dallas, TX 75275, USA
2 Child and Family Studies, Unit Faculty of Community and Health Sciences, University of the Western Cape, Private Bag x17 Bellville 7535, South Africa
3 School of Nursing, University of the Western Cape, Bellville7535, South Africa
4 Center for Community Healthcare, Research and Development, Abuja, Nigeria
5 Human Sciences Research Council, Pretoria, South Africa
6 Department of Public Health, Walter Sisulu University, Eastern Cape, South Africa
7 Department of Public Health, University of Fort Hare, Eastern Cape, South Africa
8 South African Weather Service, Private Bag X097, Pretoria0001, South Africa
9 School of Health Systems and Public Health, Faculty of Health Sciences, University of Pretoria, South Africa
10 Department of Statistics, Federal University of Technology, P.M.B 704, Akure, Nigeria
11 Department of Mathematics, University of Kansas, Lawrence, KS 66045 - 7594, USA
12 MIVEGEC, IRD, CNRS, University of Montpellier, Montpellier, France
13 Department of Mathematics and Applied Mathematics, North West University, South Africa
14 Institute of the Environment and Sustainability, University of California, Los Angeles, CA, USA
15 Department of Mathematics and Applied Mathematics, University of the Western Cape, Bellville7535, South Africa

Abstract

Background:

Malaria remains a serious concern in most African countries, causing nearly one million deaths globally every year. This review aims to examine the extent and nature of the resurgence of malaria transmission in South Africa.

Methods:

Using the Arksey and O'Malley framework, this scoping review includes articles published between the years 2015 and 2018 on the resurgence of malaria occurrence in South Africa. Articles were searched between October 2018 to January 2019 using the following electronic databases: CINAHL, Pubmed, Science Direct and SCOPUS. Grey literature from Google Scholar was also hand searched. Key search terms and subject headings such as climate variables, climate changes, climatic factors, malaria resurgence, malaria reoccurrence and malaria increase over epidemic regions in South Africa were used to identify relevant articles. Three independent reviewers performed the selection and characterization of articles, and the data collected were synthesized qualitatively.

Results:

A total number of 534 studies were identified. Among these, 24 studies met the inclusion criteria. The results were grouped by factors (four main themes) that influenced the malaria resurgence: Climatic, Epidemiological, Socio-economic, and Environmental factors. Climatic factors were found to be the major factor responsible for the resurgence of malaria, as more than 55% of the selected articles were climate-focused. This was followed by epidemiological, socio-economic and environmental factors, in that order. Grey literature from Google Scholar yielded no results.

Conclusion:

This study shows that malaria transmission in South Africa is more associated with climate. Climate-based malaria models could be used as early warning systems for malaria over the epidemic regions in South Africa. Since epidemiological factors also play significant roles in malaria transmission, regular and unrelaxed use of Indoor Residual Spraying (IRS) should be encouraged in these regions. Individuals should also be educated on the importance and the usefulness of these deliveries. While some studies have indicated that the vectors have developed resistance to insecticides, continuous research on developing new insecticides that could alter the resistance are encouraged. Furthermore, all efforts to eradicate malaria in South Africa must also target malaria-endemic neighbouring countries.

Keywords: Malaria resurgence, Climate change, South Africa, IRS, Environmental factors, Mosquitoes.


Article Information


Identifiers and Pagination:

Year: 2020
Volume: 13
First Page: 119
Last Page: 125
Publisher Id: TOPHJ-13-119
DOI: 10.2174/1874944502013010119

Article History:

Received Date: 12/11/2019
Revision Received Date: 07/02/2020
Acceptance Date: 11/02/2020
Electronic publication date: 24/04/2020
Collection year: 2020

© 2020 Abiodun et al.

open-access license: This is an open access article distributed under the terms of the Creative Commons Attribution 4.0 International Public License (CC-BY 4.0), a copy of which is available at: https://creativecommons.org/licenses/by/4.0/legalcode. This license permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.


* Address correspondence to this author at the Department of Mathematics, Southern Methodist University, Dallas, Texas75275, 6425 Boaz Lane, USA; Tel: +2148155464; E-mail: abiodun234@gmail.com





1. INTRODUCTION

Malaria continues to be a major threat in most African countries in the south of the Sahara, claiming a significant number of lives every year [1WHO, 2018. World Malaria Report: World Health Organization. Available from: https://www.who.int/malaria/publications/orld-malaria -report-2018/en/.]. Although its burden has declined recently in sub-Saharan countries due to improvement in prevention, diagnosis and treatment [1WHO, 2018. World Malaria Report: World Health Organization. Available from: https://www.who.int/malaria/publications/orld-malaria -report-2018/en/., 2O’Meara WP, Mangeni JN, Steketee R, Greenwood B. Changes in the burden of malaria in sub-Saharan Africa. Lancet Infect Dis 2010; 10(8): 545-55.
[http://dx.doi.org/10.1016/S1473-3099(10)70096-7] [PMID: 20637696]
], the region still carries the largest share of the global malaria burden [1WHO, 2018. World Malaria Report: World Health Organization. Available from: https://www.who.int/malaria/publications/orld-malaria -report-2018/en/.]. In South Africa, malaria-endemic is mainly found in three epidemic provinces, namely; Limpopo, Mpumalanga and KwaZulu-Natal [3South African Malaria Elimination Strategic Plan. 2012. Available from: http://www.ccoat.uct.ac.za/sites/default/files/image_tool/images/ 229/SA%20Malaria%20Elimination%20Strategic%20Plan%20%202012.pdf., 4National Department of Health (NDoH) - Annual Report. 2018. Available from: http://www.health.gov.za/index.php/2014-08-15-12- 56-31?download=2924:annual-report-2018.]. The vector mainly responsible for malaria transmission in South Africa is the female Anopheles mosquito (An. arabiensis and An. funestus), which transmit Plasmodium falciparum [1WHO, 2018. World Malaria Report: World Health Organization. Available from: https://www.who.int/malaria/publications/orld-malaria -report-2018/en/.-7National Institute for Communicable Diseases (NICD). 2017. Available from: http://www.nicd.ac.za/wp-content/uploads/2017/05/ Malaria-update.pdf.]. In sub-Saharan Africa, three Anopheles species, Anopheles gambiae, Anopheles arabiensis and Anopheles funestus are the major vectors responsible for malaria transmission. The first two species are considered to be the most effective malaria vectors and are classified under the An. gambiae complex group [1WHO, 2018. World Malaria Report: World Health Organization. Available from: https://www.who.int/malaria/publications/orld-malaria -report-2018/en/.]. Also, An. arabiensis and An. funestus live in sympatry in South Africa living [5Adeola AM, Olwoch JM, Botai JO, et al. Landsat satellite derived environmental metric for mapping mosquitoes breeding habitats in the Nkomazi municipality, Mpumalanga Province, South Africa. S Afr Geogr J 2017; 99(1): 14-28.
[http://dx.doi.org/10.1080/03736245.2015.1117012]
].

Malaria transmission over the South African region is seasonal, with the greatest risk between September and May, with peaks in January and April [5Adeola AM, Olwoch JM, Botai JO, et al. Landsat satellite derived environmental metric for mapping mosquitoes breeding habitats in the Nkomazi municipality, Mpumalanga Province, South Africa. S Afr Geogr J 2017; 99(1): 14-28.
[http://dx.doi.org/10.1080/03736245.2015.1117012]
]. It is well established that weather fluctuations significantly affect not only the life expectancy or completion of the life-cycle of the mosquito but also the development of the sporogonic stages of the malarial parasite within the mosquito’s body [8Tompkins AM, Ermert V. A regional-scale, high resolution dynamical malaria model that accounts for population density, climate and surface hydrology. Malar J 2013; 12(1): 65.
[http://dx.doi.org/10.1186/1475-2875-12-65] [PMID: 23419192]
, 9Paaijmans KP, Blanford S, Bell AS, Blanford JI, Read AF, Thomas MB. Influence of climate on malaria transmission depends on daily temperature variation. Proc Natl Acad Sci USA 2010; 107(34): 15135-9.
[http://dx.doi.org/10.1073/pnas.1006422107] [PMID: 20696913]
]. The biting rate and gonotrophic processes are also temperature-dependent [8Tompkins AM, Ermert V. A regional-scale, high resolution dynamical malaria model that accounts for population density, climate and surface hydrology. Malar J 2013; 12(1): 65.
[http://dx.doi.org/10.1186/1475-2875-12-65] [PMID: 23419192]
-10Ermert V. Risk assessment with regard to the occurrence of malaria in Africa under the influence of observed and projected climate change Available from: https://kups.ub.uni-koeln.de/3109/]. For these reasons, a qualitative relationship between the vector abundance and the climate variables could help identify the peaks of the vector population through meteorological monitoring and forecast [11Abiodun GJ, Njabo KY, Witbooi PJ, et al. Exploring the influence of daily climate variables on malaria transmission and abundance of Anopheles arabiensis over Nkomazi local municipality, mpumalanga province, South Africa. J Environ Public Health 2018; 20183143950
[http://dx.doi.org/10.1155/2018/3143950] [PMID: 30584427]
, 12Craig MH, Sharp BL, Mabaso ML, Kleinschmidt I. Developing a spatial-statistical model and map of historical malaria prevalence in Botswana using a staged variable selection procedure. Int J Health Geogr 2007; 6(1): 44.
[http://dx.doi.org/10.1186/1476-072X-6-44] [PMID: 17892584]
]. As part of the Malaria Elimination Strategic Plan (MESP), South Africa and a few other African countries are working towards the eradication of malaria since the major outbreak in 2000 across all the epidemic provinces [3South African Malaria Elimination Strategic Plan. 2012. Available from: http://www.ccoat.uct.ac.za/sites/default/files/image_tool/images/ 229/SA%20Malaria%20Elimination%20Strategic%20Plan%20%202012.pdf., 4National Department of Health (NDoH) - Annual Report. 2018. Available from: http://www.health.gov.za/index.php/2014-08-15-12- 56-31?download=2924:annual-report-2018.].

Several control activities and interventions have been put in place across the endemic provinces. For instance, efforts are currently ongoing to increase the coverage of Indoor Residual Spraying (IRS) to over 85% for successful control of the vectors (An. funestus near zero and low density of An. arabiensis), annually by spray teams [3South African Malaria Elimination Strategic Plan. 2012. Available from: http://www.ccoat.uct.ac.za/sites/default/files/image_tool/images/ 229/SA%20Malaria%20Elimination%20Strategic%20Plan%20%202012.pdf., 4National Department of Health (NDoH) - Annual Report. 2018. Available from: http://www.health.gov.za/index.php/2014-08-15-12- 56-31?download=2924:annual-report-2018.]. Although these activities significantly reduced malaria transmission from 2004 through 2014, the nation recently experienced a noticeable resurgence between 2015 and 2018 across the three epidemic provinces [5Adeola AM, Olwoch JM, Botai JO, et al. Landsat satellite derived environmental metric for mapping mosquitoes breeding habitats in the Nkomazi municipality, Mpumalanga Province, South Africa. S Afr Geogr J 2017; 99(1): 14-28.
[http://dx.doi.org/10.1080/03736245.2015.1117012]
-11Abiodun GJ, Njabo KY, Witbooi PJ, et al. Exploring the influence of daily climate variables on malaria transmission and abundance of Anopheles arabiensis over Nkomazi local municipality, mpumalanga province, South Africa. J Environ Public Health 2018; 20183143950
[http://dx.doi.org/10.1155/2018/3143950] [PMID: 30584427]
].

The recent resurgence spurred several studies to investigate the possible factors influencing malaria transmission over the nation. These studies established that malaria parasites are very sensitive to climatic conditions [12Craig MH, Sharp BL, Mabaso ML, Kleinschmidt I. Developing a spatial-statistical model and map of historical malaria prevalence in Botswana using a staged variable selection procedure. Int J Health Geogr 2007; 6(1): 44.
[http://dx.doi.org/10.1186/1476-072X-6-44] [PMID: 17892584]
-15Tanser FC, Sharp B, le Sueur D. Potential effect of climate change on malaria transmission in Africa. Lancet 2003; 362(9398): 1792-8.
[http://dx.doi.org/10.1016/S0140-6736(03)14898-2] [PMID: 14654317]
], with the resulting epidemics strongly dependent on climate variability. Also, since mosquitoes thrive better in warm moist environments, there is a big concern that the projected global warming may make malaria parasites spread over more regions across the nation, thereby exposing more people to the deadly disease [12Craig MH, Sharp BL, Mabaso ML, Kleinschmidt I. Developing a spatial-statistical model and map of historical malaria prevalence in Botswana using a staged variable selection procedure. Int J Health Geogr 2007; 6(1): 44.
[http://dx.doi.org/10.1186/1476-072X-6-44] [PMID: 17892584]
-15Tanser FC, Sharp B, le Sueur D. Potential effect of climate change on malaria transmission in Africa. Lancet 2003; 362(9398): 1792-8.
[http://dx.doi.org/10.1016/S0140-6736(03)14898-2] [PMID: 14654317]
]. Anopheles arabiensis, one of the main vectors of malaria in South Africa, are more aggressive in the summer and do not lay eggs in winter [16le Sueur D, Sharp BL. The breeding requirements of three members of the Anopheles gambiae Giles complex (Diptera: Culicidae) in the endemic malaria area of Natal, South Africa Bull Entomol Res 1988; 78(4): 549-60.
[http://dx.doi.org/10.1017/S0007485300015418]
, 17Maharaj R. Life table characteristics of Anopheles arabiensis (Diptera: Culicidae) under simulated seasonal conditions J Med Entomol 2003; 40(6): 737-42.
[http://dx.doi.org/10.1603/0022-2585-40.6.737] [PMID: 14765646]
]. Due to climate or other factors, new malaria-transmitting mosquito species are likely to be found. For example, a new mosquito species carrying malaria parasite was recently found in South Africa in the provinces of Mpumalanga and KwaZulu-Natal [18Burke A, Dandalo L, Munhenga G, et al. A new malaria vector mosquito in South Africa. Scientific reports 2017; 7: 43779.
[http://dx.doi.org/10.1038/srep43779]
].

Furthermore, other studies have linked malaria transmission in South Africa to factors other than climate. For instance, the transmission has been associated with malaria-drug resistance [19Barnes KI, Durrheim DN, Little F, et al. Effect of artemether-lumefantrine policy and improved vector control on malaria burden in KwaZulu-Natal, South Africa. PLoS Med 2005; 2(11): e330.
[http://dx.doi.org/10.1371/journal.pmed.0020330] [PMID: 16187798]
], mosquito resistance to insecticides [20Hargreaves K, Koekemoer LL, Brooke BD, Hunt RH, Mthembu J, Coetzee M. Anopheles funestus resistant to pyrethroid insecticides in South Africa. Med Vet Entomol 2000; 14(2): 181-9.
[http://dx.doi.org/10.1046/j.1365-2915.2000.00234.x] [PMID: 10872862]
] and socio-economic factors [21Govere J, Durrheim D, la Grange K, Mabuza A, Booman M. Community knowledge and perceptions about malaria and practices influencing malaria control in Mpumalanga Province, South Africa. S Afr Med J 2000; 90(6): 611-6.https://www.ajol.info/index.php/samj/ article/view/157669/147271
[PMID: 10918892]
]. The current study aims to establish the major factor responsible for the recent malaria resurgence in South Africa between 2015 and 2018.

2. METHODS

In this study, we adapted the Arksey and O’Malley [2O’Meara WP, Mangeni JN, Steketee R, Greenwood B. Changes in the burden of malaria in sub-Saharan Africa. Lancet Infect Dis 2010; 10(8): 545-55.
[http://dx.doi.org/10.1016/S1473-3099(10)70096-7] [PMID: 20637696]
] framework for conducting scoping reviews. This framework was considered appropriate for the aim of our study, and has been used in other studies [22Puts MTE, Toubasi S, Andrew MK, et al. Interventions to prevent or reduce the level of frailty in community-dwelling older adults: A scoping review of the literature and international policies. Age Ageing 2017; 46(3): 383-92.
[http://dx.doi.org/10.1093/ageing/afw247] [PMID: 28064173]
, 23Adebiyi BO, Mukumbang FC, Erasmus C. The distribution of available prevention and management interventions for fetal alcohol Spectrum disorder (2007 to 2017): Implications for collaborative actions. Int J Environ Res Public Health 2019; 16(12): 2244.
[http://dx.doi.org/10.3390/ijerph16122244] [PMID: 31242673]
]. The framework includes (1) framing of questions for the review; (2) identifying relevant work; (3) assessing the quality of studies; (4) summarizing the evidence; and (5) interpreting the findings. However, steps that we considered irrelevant to this study were omitted.

2.1. Framing of the Question for the Review

The question for the review was framed using PICO (Population- Malaria, Intervention- Factors that are responsible for the resurgence, Comparison- Factors not responsible for the resurgence, and Outcome- Resurgence of malaria) mnemonics [24Schardt C, Adams MB, Owens T, Keitz S, Fontelo P. Utilization of the PICO framework to improve searching PubMed for clinical questions. BMC Med Inform Decis Mak 2007; 7(1): 16.
[http://dx.doi.org/10.1186/1472-6947-7-16] [PMID: 17573961]
]. This addressed the factors responsible for the resurgence of malaria prevalence in South Africa between 2015 and 2018.

2.2. Identifying Relevant Studies

The search for relevant studies was conducted by three (3) reviewers using four (4) databases: CINAHL, PubMed, Science Direct and SCOPUS, while grey literature was searched using Google Scholar. Terms that described climate variables combined using the Boolean operator (e.g. factors) with terms that described malaria resurgence (e.g. malaria reoccurrence) were used. An initial search using all identified keywords and index terms were undertaken across all included databases. The text words contained in the title and abstract, and in the index and medical subject heading (MeSH) terms were used to ensure that all relevant materials were captured. Secondly, the reference list of all identified articles was searched for additional studies to identify studies that could not be located through this search strategy.

After key concepts were identified and databases selected, search terms were combined with Bloom operators and searches were run in selected databases. The articles were imported to Endnote reference manager, where titles and abstracts were screened and full-text articles were reviewed for eligibility based on the inclusion criteria (PICO). A grey literature search using Google Scholar with keywords and search terms was also conducted. We used the “sort by relevance ranking” within Google Scholar to bring the most relevant results to the top of the list. We further set the page numbers to be screened to the first ten pages of each search result. This strategy ensures that the most relevant results are captured and also that a reasonable amount is screened. The results were further screened using the inclusion criteria for the review.

2.3. Selection of Studies Included

2.3.1. Inclusion Criteria

- Articles focused on malaria epidemic regions in South Africa between 2015 and 2018.

- Phenomenon of interest/Outcome: This review focused on malaria resurgence, malaria re-occurrence or malaria increase.

- Type of study: This review considered empirical studies, but not limited to designs such as non-experimental observational studies, descriptive studies and case studies conducted in South Africa.

- The search included published articles from 2015-2018 in South Africa on malaria resurgence during this period.

- The search was restricted to English language papers and studies conducted in South Africa.

2.3.2. Exclusion Criteria

- Articles before 2015 were excluded.

- Any article not written in the English language.

- Literature reviews/ meta-analysis.

- Studies not specific to South Africa for example studies conducted in sub-Sahara Africa.

2.4. Extraction and Charting of Data from Included Studies

We reviewed articles for inclusion, manually extracted data from the selected articles using Microsoft Excel and summarized in a tabular form. Extracted data included: authors, article title, year of publication, study location, study population, aims of the study, methodology/instruments, outcome measure, and importance of the result (Supplementary Table). The table enabled the identification of differences, similarities and common themes in the studies. The extracted data were synthesized, summarized and presented in a narrative summary.

3. RESULTS AND DISCUSSION

The initial 534 records and 4 from other sources are highlighted (Fig. 1). After duplicates were removed, 449 records were left. A further 363 records (irrelevant) were excluded based on the inclusion criteria discussed above. A total of 86 potentially relevant articles after the title and abstract screening were screened for full-text, of which a further 62 were excluded. Finally, 24 papers were left for review and any further citation search yielded no new articles.

3.1. Climatic Factors

With various approaches, malaria transmission in South Africa has been linked to climatic conditions. For instance, 14 studies (58.3%) out of 24 presented in supplementary table highlighted the significant roles that climate plays on the resurgence. Although some of the 14 studies also mentioned other factors, the emphasis was more on climate. However, climatic factors affecting malaria transmission in South Africa cannot be generalized across the epidemic regions [5Adeola AM, Olwoch JM, Botai JO, et al. Landsat satellite derived environmental metric for mapping mosquitoes breeding habitats in the Nkomazi municipality, Mpumalanga Province, South Africa. S Afr Geogr J 2017; 99(1): 14-28.
[http://dx.doi.org/10.1080/03736245.2015.1117012]
]. For instance, the temperature seems to be the major factor in KwaZulu-Natal province, as highlighted in 4 of the 14 studies [25Okuneye K, Abdelrazec A, Gumel AB. Mathematical analysis of a weather-driven model for the population ecology of mosquitoes. Math Biosci Eng 2018; 15(1): 57-93.
[http://dx.doi.org/10.3934/mbe.2018003] [PMID: 29161827]
-28Abiodun GJ, Witbooi PJ, Okosun KO, Maharaj R. Exploring the impact of climate variability on malaria transmission using a dynamic mosquito-human malaria model. Open Infect Dis J 2018; 10: 88-100.https://dx.doi.org/10.2174%2F1874279301810010088
[http://dx.doi.org/10.2174/1874279301810010088] [PMID: 30906484]
]. However, two of the four studies [25Okuneye K, Abdelrazec A, Gumel AB. Mathematical analysis of a weather-driven model for the population ecology of mosquitoes. Math Biosci Eng 2018; 15(1): 57-93.
[http://dx.doi.org/10.3934/mbe.2018003] [PMID: 29161827]
, 27Abiodun GJ, Witbooi P, Okosun KO. Modelling the impact of climatic variables on malaria transmission. Hacet J Math Stat 2018; 47(2): 219-35.https://dergipark.org.tr/en/pub/hujms/issue/38251/441620] also acknowledge the importance of rainfall on malaria transmission over the province. Rainfall seems more significant on malaria resurgence in Limpopo than temperature as indicated by four other studies [5Adeola AM, Olwoch JM, Botai JO, et al. Landsat satellite derived environmental metric for mapping mosquitoes breeding habitats in the Nkomazi municipality, Mpumalanga Province, South Africa. S Afr Geogr J 2017; 99(1): 14-28.
[http://dx.doi.org/10.1080/03736245.2015.1117012]
, 6Ikeda T, Behera SK, Morioka Y, et al. Seasonally lagged effects of climatic factors on malaria incidence in South Africa. Sci Rep 2017; 7(1): 2458.
[http://dx.doi.org/10.1038/s41598-017-02680-6] [PMID: 28555071]
, 29Komen K, Olwoch J, Rautenbach H, Botai J, Adebayo A. Long-run relative importance of temperature as the main driver to malaria transmission in Limpopo Province, South Africa: a simple econometric approach. EcoHealth 2015; 12(1): 131-43.
[http://dx.doi.org/10.1007/s10393-014-0992-1] [PMID: 25515074]
, 30Behera SK, Morioka Y, Ikeda T, et al. Malaria incidences in South Africa linked to a climate mode in southwestern Indian Ocean. Environ Dev 2018; 27: 47-57.
[http://dx.doi.org/10.1016/j.envdev.2018.07.002]
]. Also, two of the four likewise pointed to the significance of temperature [5Adeola AM, Olwoch JM, Botai JO, et al. Landsat satellite derived environmental metric for mapping mosquitoes breeding habitats in the Nkomazi municipality, Mpumalanga Province, South Africa. S Afr Geogr J 2017; 99(1): 14-28.
[http://dx.doi.org/10.1080/03736245.2015.1117012]
, 30Behera SK, Morioka Y, Ikeda T, et al. Malaria incidences in South Africa linked to a climate mode in southwestern Indian Ocean. Environ Dev 2018; 27: 47-57.
[http://dx.doi.org/10.1016/j.envdev.2018.07.002]
]. In addition, Behera et al. [30Behera SK, Morioka Y, Ikeda T, et al. Malaria incidences in South Africa linked to a climate mode in southwestern Indian Ocean. Environ Dev 2018; 27: 47-57.
[http://dx.doi.org/10.1016/j.envdev.2018.07.002]
] attributed malaria resurgence over the province to El Niño/La Niña and sea surface temperature (SST) from the south-western Indian Ocean. We found only three studies [5Adeola AM, Olwoch JM, Botai JO, et al. Landsat satellite derived environmental metric for mapping mosquitoes breeding habitats in the Nkomazi municipality, Mpumalanga Province, South Africa. S Afr Geogr J 2017; 99(1): 14-28.
[http://dx.doi.org/10.1080/03736245.2015.1117012]
, 11Abiodun GJ, Njabo KY, Witbooi PJ, et al. Exploring the influence of daily climate variables on malaria transmission and abundance of Anopheles arabiensis over Nkomazi local municipality, mpumalanga province, South Africa. J Environ Public Health 2018; 20183143950
[http://dx.doi.org/10.1155/2018/3143950] [PMID: 30584427]
, 31Kapwata T, Gebreslasie MT. Random forest variable selection in spatial malaria transmission modelling in Mpumalanga Province, South Africa. Geospat Health 2016; 11(3): 434.
[http://dx.doi.org/10.4081/gh.2016.434] [PMID: 27903050]
] linking the resurgence to the climate in Mpumalanga province over the study period. Kapwata and Gebreselassie [31Kapwata T, Gebreslasie MT. Random forest variable selection in spatial malaria transmission modelling in Mpumalanga Province, South Africa. Geospat Health 2016; 11(3): 434.
[http://dx.doi.org/10.4081/gh.2016.434] [PMID: 27903050]
] and Adeola et al. [5Adeola AM, Olwoch JM, Botai JO, et al. Landsat satellite derived environmental metric for mapping mosquitoes breeding habitats in the Nkomazi municipality, Mpumalanga Province, South Africa. S Afr Geogr J 2017; 99(1): 14-28.
[http://dx.doi.org/10.1080/03736245.2015.1117012]
] believe that transmission over the province is associated with surface land temperature and other non-climatic factors, while Abiodun et al. [11Abiodun GJ, Njabo KY, Witbooi PJ, et al. Exploring the influence of daily climate variables on malaria transmission and abundance of Anopheles arabiensis over Nkomazi local municipality, mpumalanga province, South Africa. J Environ Public Health 2018; 20183143950
[http://dx.doi.org/10.1155/2018/3143950] [PMID: 30584427]
] found that rainfall and relative humidity are more significant.

Similar findings were established over some South African neighbouring countries such as Zimbabwe [32Hartman J, Ebi K, McConnell KJ, Chan N, Weyant J. Climate suitability: for stable malaria transmission in Zimbabwe under different climate change scenarios. Glob Change Hum Health 2002; 3(1): 42.
[http://dx.doi.org/10.1023/A:1019621231796]
, 33Mabaso ML, Vounatsou P, Midzi S, Da Silva J, Smith T. Spatio-temporal analysis of the role of climate in inter-annual variation of malaria incidence in Zimbabwe. Int J Health Geogr 2006; 5(1): 20.
[http://dx.doi.org/10.1186/1476-072X-5-20] [PMID: 16700905]
], Mozambique [34Abellana R, Ascaso C, Aponte J, et al. Spatio-seasonal modeling of the incidence rate of malaria in Mozambique. Malar J 2008; 7(1): 228.
[http://dx.doi.org/10.1186/1475-2875-7-228] [PMID: 18976458]
, 35Zacarias OP, Andersson M. Spatial and temporal patterns of malaria incidence in Mozambique. Malar J 2011; 10(1): 189.
[http://dx.doi.org/10.1186/1475-2875-10-189] [PMID: 21752284]
], Botswana [36Thomson MC, Mason SJ, Phindela T, Connor SJ. Use of rainfall and sea surface temperature monitoring for malaria early warning in Botswana. Am J Trop Med Hyg 2005; 73(1): 214-21.
[http://dx.doi.org/10.4269/ajtmh.2005.73.214] [PMID: 16014862]
] and the East African highlands [37Hay SI, Cox J, Rogers DJ, et al. Climate change and the resurgence of malaria in the East African highlands. Nature 2002; 415(6874): 905-9.
[http://dx.doi.org/10.1038/415905a] [PMID: 11859368]
-39Ruiz D, Brun C, Connor SJ, Omumbo JA, Lyon B, Thomson MC. Testing a multi-malaria-model ensemble against 30 years of data in the Kenyan highlands. Malar J 2014; 13(1): 206.
[http://dx.doi.org/10.1186/1475-2875-13-206] [PMID: 24885824]
].

It is established that rainfall contributes to the proliferation of mosquito breeding sites, while temperature contributes to the development of the sporogonic stages of the malaria parasite within the mosquito’s body. The biting rate and gonotrophic processes are also temperature-dependent [8Tompkins AM, Ermert V. A regional-scale, high resolution dynamical malaria model that accounts for population density, climate and surface hydrology. Malar J 2013; 12(1): 65.
[http://dx.doi.org/10.1186/1475-2875-12-65] [PMID: 23419192]
-11Abiodun GJ, Njabo KY, Witbooi PJ, et al. Exploring the influence of daily climate variables on malaria transmission and abundance of Anopheles arabiensis over Nkomazi local municipality, mpumalanga province, South Africa. J Environ Public Health 2018; 20183143950
[http://dx.doi.org/10.1155/2018/3143950] [PMID: 30584427]
].

3.2. Epidemiological Factors

Half of the 24 papers highlight the importance of mosquito abundance on malaria resurgence across the epidemic regions in South Africa [5Adeola AM, Olwoch JM, Botai JO, et al. Landsat satellite derived environmental metric for mapping mosquitoes breeding habitats in the Nkomazi municipality, Mpumalanga Province, South Africa. S Afr Geogr J 2017; 99(1): 14-28.
[http://dx.doi.org/10.1080/03736245.2015.1117012]
, 11Abiodun GJ, Njabo KY, Witbooi PJ, et al. Exploring the influence of daily climate variables on malaria transmission and abundance of Anopheles arabiensis over Nkomazi local municipality, mpumalanga province, South Africa. J Environ Public Health 2018; 20183143950
[http://dx.doi.org/10.1155/2018/3143950] [PMID: 30584427]
, 18Burke A, Dandalo L, Munhenga G, et al. A new malaria vector mosquito in South Africa. Scientific reports 2017; 7: 43779.
[http://dx.doi.org/10.1038/srep43779]
, 25Okuneye K, Abdelrazec A, Gumel AB. Mathematical analysis of a weather-driven model for the population ecology of mosquitoes. Math Biosci Eng 2018; 15(1): 57-93.
[http://dx.doi.org/10.3934/mbe.2018003] [PMID: 29161827]
-28Abiodun GJ, Witbooi PJ, Okosun KO, Maharaj R. Exploring the impact of climate variability on malaria transmission using a dynamic mosquito-human malaria model. Open Infect Dis J 2018; 10: 88-100.https://dx.doi.org/10.2174%2F1874279301810010088
[http://dx.doi.org/10.2174/1874279301810010088] [PMID: 30906484]
, 40Agusto FB, Gumel AB, Parham PE. Qualitative assessment of the role of temperature variations on malaria transmission dynamics. J Biol Syst 2015; 23(04)1550030
[http://dx.doi.org/10.1142/S0218339015500308]
-44Davies C, Coetzee M, Lyons CL. Effect of stable and fluctuating temperatures on the life history traits of Anopheles arabiensis and An. quadriannulatus under conditions of inter- and intra-specific competition. Parasit Vectors 2016; 9(1): 342.
[http://dx.doi.org/10.1186/s13071-016-1630-2] [PMID: 27301875]
]. For example, using climate-based mathematical models, the impact of mosquito (mainly An. arabiensis) population dynamics on malaria transmission was investigated over KwaZulu-Natal [25Okuneye K, Abdelrazec A, Gumel AB. Mathematical analysis of a weather-driven model for the population ecology of mosquitoes. Math Biosci Eng 2018; 15(1): 57-93.
[http://dx.doi.org/10.3934/mbe.2018003] [PMID: 29161827]
, 26Abiodun GJ, Maharaj R, Witbooi P, Okosun KO. Modelling the influence of temperature and rainfall on the population dynamics of Anopheles arabiensis. Malar J 2016; 15(1): 364.
[http://dx.doi.org/10.1186/s12936-016-1411-6] [PMID: 27421769]
, 28Abiodun GJ, Witbooi PJ, Okosun KO, Maharaj R. Exploring the impact of climate variability on malaria transmission using a dynamic mosquito-human malaria model. Open Infect Dis J 2018; 10: 88-100.https://dx.doi.org/10.2174%2F1874279301810010088
[http://dx.doi.org/10.2174/1874279301810010088] [PMID: 30906484]
, 40Agusto FB, Gumel AB, Parham PE. Qualitative assessment of the role of temperature variations on malaria transmission dynamics. J Biol Syst 2015; 23(04)1550030
[http://dx.doi.org/10.1142/S0218339015500308]
, 43Abiodun GJ, Witbooi P, Okosun KO. Modeling and analyzing the impact of temperature and rainfall on mosquito population dynamics over Kwazulu-Natal, South Africa. Int J Biomath 2017; 10(04)1750055
[http://dx.doi.org/10.1142/S1793524517500553]
], Limpopo [28Abiodun GJ, Witbooi PJ, Okosun KO, Maharaj R. Exploring the impact of climate variability on malaria transmission using a dynamic mosquito-human malaria model. Open Infect Dis J 2018; 10: 88-100.https://dx.doi.org/10.2174%2F1874279301810010088
[http://dx.doi.org/10.2174/1874279301810010088] [PMID: 30906484]
] and Mpumalanga provinces [11Abiodun GJ, Njabo KY, Witbooi PJ, et al. Exploring the influence of daily climate variables on malaria transmission and abundance of Anopheles arabiensis over Nkomazi local municipality, mpumalanga province, South Africa. J Environ Public Health 2018; 20183143950
[http://dx.doi.org/10.1155/2018/3143950] [PMID: 30584427]
]. Other studies also confirm that the vector population correlates with the resurgence [5Adeola AM, Olwoch JM, Botai JO, et al. Landsat satellite derived environmental metric for mapping mosquitoes breeding habitats in the Nkomazi municipality, Mpumalanga Province, South Africa. S Afr Geogr J 2017; 99(1): 14-28.
[http://dx.doi.org/10.1080/03736245.2015.1117012]
, 42Malahlela OE, Olwoch JM, Adjorlolo C. Evaluating Efficacy of Landsat-Derived Environmental Covariates for Predicting Malaria Distribution in Rural Villages of Vhembe District, South Africa. EcoHealth 2018; 15(1): 23-40.
[http://dx.doi.org/10.1007/s10393-017-1307-0] [PMID: 29330677]
, 44Davies C, Coetzee M, Lyons CL. Effect of stable and fluctuating temperatures on the life history traits of Anopheles arabiensis and An. quadriannulatus under conditions of inter- and intra-specific competition. Parasit Vectors 2016; 9(1): 342.
[http://dx.doi.org/10.1186/s13071-016-1630-2] [PMID: 27301875]
]. More importantly, the resurgence has been traced to the arrival of new mosquito species across the epidemic regions [18Burke A, Dandalo L, Munhenga G, et al. A new malaria vector mosquito in South Africa. Scientific reports 2017; 7: 43779.
[http://dx.doi.org/10.1038/srep43779]
, 45Cornel AJ, Lee Y, Almeida APG, et al. Mosquito community composition in South Africa and some neighboring countries. Parasit Vectors 2018; 11(1): 331.
[http://dx.doi.org/10.1186/s13071-018-2824-6] [PMID: 29859109]
]. Under suitable conditions, mosquitoes bite more aggressively to produce more eggs, and in the process, transmit malaria faster than usual.

Similarly, the importance of mosquito abundance on malaria transmission has been investigated in Zimbabwe [46Lukwa N, Nyazema NZ, Curtis CF, Mwaiko GL, Chandiwana SK. People’s perceptions about malaria transmission and control using mosquito repellent plants in a locality in Zimbabwe. Cent Afr J Med 1999; 45(3): 64-8.
[http://dx.doi.org/10.4314/cajm.v45i3.8456] [PMID: 10565064]
, 47Munhenga G, Masendu HT, Brooke BD, Hunt RH, Koekemoer LK. Pyrethroid resistance in the major malaria vector Anopheles arabiensis from Gwave, a malaria-endemic area in Zimbabwe. Malar J 2008; 7(1): 247.
[http://dx.doi.org/10.1186/1475-2875-7-247] [PMID: 19038063]
], Mozambique [48Mendis C, Jacobsen JL, Gamage-Mendis A, et al. Anopheles arabiensis and An. funestus are equally important vectors of malaria in Matola coastal suburb of Maputo, southern Mozambique. Med Vet Entomol 2000; 14(2): 171-80.
[http://dx.doi.org/10.1046/j.1365-2915.2000.00228.x] [PMID: 10872861]
, 49Munguambe K, Pool R, Montgomery C, et al. What drives community adherence to indoor residual spraying (IRS) against malaria in Manhiça district, rural Mozambique: a qualitative study. Malar J 2011; 10(1): 344.
[http://dx.doi.org/10.1186/1475-2875-10-344] [PMID: 22111698]
] and Namibia [50Chanda E, Ameneshewa B, Angula HA, et al. Strengthening tactical planning and operational frameworks for vector control: the roadmap for malaria elimination in Namibia. Malar J 2015; 14(1): 302.
[http://dx.doi.org/10.1186/s12936-015-0785-1] [PMID: 26242587]
].

Fig (1)
A flow chart for the selection process.


3.3. Socio-economic Factors

Six (25%) out of the 24 selected studies connected malaria resurgence in South Africa with socio-economic factors [6Ikeda T, Behera SK, Morioka Y, et al. Seasonally lagged effects of climatic factors on malaria incidence in South Africa. Sci Rep 2017; 7(1): 2458.
[http://dx.doi.org/10.1038/s41598-017-02680-6] [PMID: 28555071]
, 41Mutegeki E, Chimbari MJ, Mukaratirwa S. Assessment of individual and household malaria risk factors among women in a South African village. Acta Trop 2017; 175: 71-7.
[http://dx.doi.org/10.1016/j.actatropica.2016.12.007] [PMID: 27965145]
, 51Hlongwana KW, Tsoka-Gwegweni J. From malaria control to elimination in South Africa: The researchers’ perspectives. Afr J Prim Health Care Fam Med 2016; 8(1): e1-e10.
[http://dx.doi.org/10.4102/phcfm.v8i1.1078] [PMID: 27543286]
-54Manana 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 2017; 18(1): 41.
[http://dx.doi.org/10.1186/s12889-017-4583-2] [PMID: 28728572]
]. Migration from neighbouring countries for socio-economic reason was found to be a major strain on malaria control in Limpopo [5Adeola AM, Olwoch JM, Botai JO, et al. Landsat satellite derived environmental metric for mapping mosquitoes breeding habitats in the Nkomazi municipality, Mpumalanga Province, South Africa. S Afr Geogr J 2017; 99(1): 14-28.
[http://dx.doi.org/10.1080/03736245.2015.1117012]
, 6Ikeda T, Behera SK, Morioka Y, et al. Seasonally lagged effects of climatic factors on malaria incidence in South Africa. Sci Rep 2017; 7(1): 2458.
[http://dx.doi.org/10.1038/s41598-017-02680-6] [PMID: 28555071]
] and KwaZulu-Natal provinces [41Mutegeki E, Chimbari MJ, Mukaratirwa S. Assessment of individual and household malaria risk factors among women in a South African village. Acta Trop 2017; 175: 71-7.
[http://dx.doi.org/10.1016/j.actatropica.2016.12.007] [PMID: 27965145]
]. According to Adeola et al. [55Adeola A, Ncongwane K, Abiodun G, et al. Rainfall trends and malaria occurrences in limpopo province, south africa. Int J Environ Res Public Health 2019; 16(24): 5156.
[http://dx.doi.org/10.3390/ijerph16245156] [PMID: 31861127]
], imported malaria cases account for about 26% of total malaria cases recorded in Limpopo from 1998-2017. This is largely due to the cross-border movement of farmworkers, mainly from Zimbabwe and Mozambique to South Africa, who work on the large commercial farmers in Limpopo and Mpumalanga [5Adeola AM, Olwoch JM, Botai JO, et al. Landsat satellite derived environmental metric for mapping mosquitoes breeding habitats in the Nkomazi municipality, Mpumalanga Province, South Africa. S Afr Geogr J 2017; 99(1): 14-28.
[http://dx.doi.org/10.1080/03736245.2015.1117012]
, 56Adeola AM, Botai JO, Rautenbach H, et al. Climatic variables and malaria morbidity in mutale local municipality, South Africa: a 19-year data analysis. Int J Environ Res Public Health 2017; 14(11): 1360.
[http://dx.doi.org/10.3390/ijerph14111360] [PMID: 29117114]
]. Similarly, malaria is highly regarded as a disease of poverty. A recent study by Lowe et al. [56Adeola AM, Botai JO, Rautenbach H, et al. Climatic variables and malaria morbidity in mutale local municipality, South Africa: a 19-year data analysis. Int J Environ Res Public Health 2017; 14(11): 1360.
[http://dx.doi.org/10.3390/ijerph14111360] [PMID: 29117114]
] indicated that there is a significant correlation between malaria and economic status, particularly income and housing conditions. Most researchers and stakeholders working on malaria in South Africa believe that South Africa’s 2018 malaria elimination target was not realistic due to lack of new tools, resources and the capacity to fight malaria; coupled with poor cross-border collaborations; overreliance on partners to implement; poor community involvement; and poor surveillance [51Hlongwana KW, Tsoka-Gwegweni J. From malaria control to elimination in South Africa: The researchers’ perspectives. Afr J Prim Health Care Fam Med 2016; 8(1): e1-e10.
[http://dx.doi.org/10.4102/phcfm.v8i1.1078] [PMID: 27543286]
, 52Hlongwana KW, Tsoka-Gwegweni J. Towards the implementation of malaria elimination policy in South Africa: the stakeholders’ perspectives. Glob Health Action 2017; 10(1)1288954
[http://dx.doi.org/10.1080/16549716.2017.1288954] [PMID: 28475435]
]. Inadequate communication channels on malaria control, such as Sterile Insect Technique (SIT), also play significant roles in malaria transmission [54Manana 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 2017; 18(1): 41.
[http://dx.doi.org/10.1186/s12889-017-4583-2] [PMID: 28728572]
]. Practicing animal husbandry, residing in household structures that had not been sprayed were found to be associated with malaria infection over KwaZulu-Natal province [41Mutegeki E, Chimbari MJ, Mukaratirwa S. Assessment of individual and household malaria risk factors among women in a South African village. Acta Trop 2017; 175: 71-7.
[http://dx.doi.org/10.1016/j.actatropica.2016.12.007] [PMID: 27965145]
]. It has also been established that the odds of malaria infection are lower in modern, improved housing compared to traditional housing in sub-Sahara Africa [53Tusting LS, Bottomley C, Gibson H, et al. Housing improvements and malaria risk in sub-Saharan Africa: a multi-country analysis of survey data. PLoS Med 2017; 14(2)e1002234
[http://dx.doi.org/10.1371/journal.pmed.1002234] [PMID: 28222094]
]. The impacts of socio-economic factors on malaria transmission have also been highlighted in Malawi [57Lowe R, Chirombo J, Tompkins AM. Relative importance of climatic, geographic and socio-economic determinants of malaria in Malawi. Malar J 2013; 12(1): 416.
[http://dx.doi.org/10.1186/1475-2875-12-416] [PMID: 24228784]
] Gambia [58Koram KA, Bennett S, Adiamah JH, Greenwood BM. Socio-economic risk factors for malaria in a peri-urban area of The Gambia. Trans R Soc Trop Med Hyg 1995; 89(2): 146-50.
[http://dx.doi.org/10.1016/0035-9203(95)90471-9] [PMID: 7778137]
] and Ghana [59Biritwum RB, Welbeck J, Barnish G. Incidence and management of malaria in two communities of different socio-economic level, in Accra, Ghana. Ann Trop Med Parasitol 2000; 94(8): 771-8.
[http://dx.doi.org/10.1080/00034983.2000.11813601] [PMID: 11214095]
].

3.4. Environmental Factors

Four studies (16.7%) linked malaria transmission to environmental factors. A high correlation was reported between malaria cases and derived environmental metrics such as the Normalized Difference Water Index (NDVI) [5Adeola AM, Olwoch JM, Botai JO, et al. Landsat satellite derived environmental metric for mapping mosquitoes breeding habitats in the Nkomazi municipality, Mpumalanga Province, South Africa. S Afr Geogr J 2017; 99(1): 14-28.
[http://dx.doi.org/10.1080/03736245.2015.1117012]
, 31Kapwata T, Gebreslasie MT. Random forest variable selection in spatial malaria transmission modelling in Mpumalanga Province, South Africa. Geospat Health 2016; 11(3): 434.
[http://dx.doi.org/10.4081/gh.2016.434] [PMID: 27903050]
] Normalized Difference Water Index (NDWI) and altitude, water body and irrigated land [5Adeola AM, Olwoch JM, Botai JO, et al. Landsat satellite derived environmental metric for mapping mosquitoes breeding habitats in the Nkomazi municipality, Mpumalanga Province, South Africa. S Afr Geogr J 2017; 99(1): 14-28.
[http://dx.doi.org/10.1080/03736245.2015.1117012]
, 60Adeola AM, Botai OJ, Olwoch JM, et al. Environmental factors and population at risk of malaria in Nkomazi municipality, South Africa. Trop Med Int Health 2016; 21(5): 675-86.
[http://dx.doi.org/10.1111/tmi.12680] [PMID: 26914617]
] in Mpumalanga province. Furthermore, Malahlela [42Malahlela OE, Olwoch JM, Adjorlolo C. Evaluating Efficacy of Landsat-Derived Environmental Covariates for Predicting Malaria Distribution in Rural Villages of Vhembe District, South Africa. EcoHealth 2018; 15(1): 23-40.
[http://dx.doi.org/10.1007/s10393-017-1307-0] [PMID: 29330677]
] concluded that malaria resurgence in Limpopo province is traceable to vegetation moisture and vegetation greenness, which are proxy/surrogate for rainfall. The availability of an adequate amount of rainfall for the provision of ideal environmental conditions (such as open water, green vegetation) provides suitable breeding and resting places for the major vector. We found no study in this regard over KwaZulu-Natal within the study period. Environmental factors such as vegetation index, waterbody, among others have been similarly linked to malaria incidence in Kenya [61Patz JA, Strzepek K, Lele S, et al. Predicting key malaria transmission factors, biting and entomological inoculation rates, using modelled soil moisture in Kenya. Trop Med Int Health 1998; 3(10): 818-27.
[http://dx.doi.org/10.1046/j.1365-3156.1998.00309.x] [PMID: 9809915]
], Zimbabwe [62Funk C, Budde ME. Phenologically-tuned MODIS NDVI-based production anomaly estimates for Zimbabwe. Remote Sens Environ 2009; 113(1): 115-25.
[http://dx.doi.org/10.1016/j.rse.2008.08.015]
, 63Mabaso ML, Craig M, Vounatsou P, Smith T. Towards empirical description of malaria seasonality in southern Africa: the example of Zimbabwe. Trop Med Int Health 2005; 10(9): 909-18.
[http://dx.doi.org/10.1111/j.1365-3156.2005.01462.x] [PMID: 16135199]
], Botswana [12Craig MH, Sharp BL, Mabaso ML, Kleinschmidt I. Developing a spatial-statistical model and map of historical malaria prevalence in Botswana using a staged variable selection procedure. Int J Health Geogr 2007; 6(1): 44.
[http://dx.doi.org/10.1186/1476-072X-6-44] [PMID: 17892584]
] and Eritrea [64Ceccato P, Ghebremeskel T, Jaiteh M, et al. Malaria stratification, climate, and epidemic early warning in Eritrea. The American journal of tropical medicine and hygiene 2007; 77(6): 61-8.
[http://dx.doi.org/10.4269/ajtmh.2007.77.61]
]. The significant correlation of the high values of vegetation index and water body with malaria incidence is strongly associated with rainfall.

In general, climate variables play major roles in malaria transmission across all the epidemic provinces (Limpopo, Mpumalanga and KwaZulu-Natal). For instance, four of the papers suggested that both temperature and rainfall are responsible for the transmission in KwaZulu-Natal, while two suggested similar findings over Limpopo. However, three additional papers concluded that the impact of temperature on the transmission is more significant than that of rainfall on the KwaZulu-Natal and Mpumalanga provinces. This implies that the effect of temperature is more pronounced over the two provinces. Rainfall is seen to be more significant than temperature over Limpopo province.

CONCLUSION

The inclusion criteria above show that climate variables (mainly, rainfall, temperature and relative humidity) are mostly mentioned but not solely responsible for the malaria resurgence in all the epidemic regions in South Africa. Environmental and socio-economic factors were also mentioned as vital elements to be considered in order to understand the dynamics of malaria prevalence. Consequently, some preventive measures and interventions are suggested to minimize and gradually eradicate malaria from these regions.

Therefore, malaria models that integrate all variables could be used to monitor the progression of malaria and assist in intervention and prevention efforts with respect to malaria. These models could be implemented for developing methodologies necessary to detect malaria pathogen, vector and habitat preference. More importantly, climate-based malaria models should be used as a framework for strengthening the institutional capacity of malaria surveillance by providing malaria-risk management based on climate information and early warning system.

Regular and unrelaxed use of Indoor Residual Spraying (IRS) should be encouraged over epidemic regions in South Africa. Sufficient insecticides-impregnated bed nets should also be supplied to the communities in these regions, and more importantly, individuals should be educated on the importance and the usefulness of these deliveries.

Furthermore, since it has been established that most malaria cases found in South Africa are imported from neighbouring countries [6Ikeda T, Behera SK, Morioka Y, et al. Seasonally lagged effects of climatic factors on malaria incidence in South Africa. Sci Rep 2017; 7(1): 2458.
[http://dx.doi.org/10.1038/s41598-017-02680-6] [PMID: 28555071]
], it is important to strengthen cross-border control of malaria to minimize its spread. All goals to eliminate malaria in South Africa must also target the epidemic neighbouring countries (Zimbabwe, Mozambique, Botswana and Namibia).

AUTHORS' CONTRIBUTIONS

All authors made substantial contributions to study design, including the development of systematic review procedures. GJA, BA and ROA conducted the literature search and data extraction and independently assessed the methodological quality of included studies and conducted the analysis. OO, KEO, AMA and VJS adjudicated in any disagreements in methodological quality assessments and contributed to the analysis. GJA, BA, ROA, OSM and RDD drafted the original manuscript while KOO, KYN, PJW and AA critically reviewed the manuscript for important intellectual content. All authors have given approval of this final version to be published and agree to be accountable for all aspects of the work.

CONSENT FOR PUBLICATION

Not applicable.

FUNDING

This study was supported by the University of Pretoria Institute for Sustainable Malaria Control (UP ISMC) and Malaria Research Control (MRC) collaborating centre for malaria research.

CONFLICT OF INTEREST

The authors declare no conflict of interest, financial or otherwise.

ACKNOWLEDGEMENTS

We would like to thank the Expert Advisory Panel and Systematic Review Team for their guidance and assistance in the completion of this scoping review.

SUPPLEMENTARY MATERIAL

Supplementary material is available on the publishers website along with the published article.

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