Disregarding reservoirs of disease vectors: A surveillance paradox in Africa.

Abstract

Vector borne diseases (VBDs) continue to sustain the huge burden of communicable diseases in Africa, as efficient indigenous and invasive vectors expand their range and abundance. Consequently, malaria, lymphatic filariasis, and arboviral diseases, such as chikungunya, dengue, yellow fever and Zika virus disease, Rift Valley fever and West Nile fever persist [[1]Alonso P. Engels D. Reeder J Renewed push to strengthen vector control globally.Lancet. 2017; 389: 2270-2271Summary Full Text Full Text PDF PubMed Scopus (14) Google Scholar]. Efficient mosquito vectors, Aedes aegypti, Aedes albopictus, Culex quinquefasciatus and the invasive Anopheles stephensi thrive in urban areas, are climate sensitive, epidemic prone and problematic given the high urban population in Africa (43.8%) and the inherent annual growth rate (4.1%) [[2]Sinka M.E. Pironon S. Masseyc N.C. Longbottom J. Hemingway J. Moyes C.L. Willis K.J. A new malaria vector in Africa: predicting the expansion range of Anopheles stephensi and identifying the urban populations at risk.PNAS. 2020; : 1-9https://doi.org/10.1073/pnas.2003976117Crossref Scopus (45) Google Scholar]. The risk of malaria and arboviral diseases is exemplified by recurrent epidemics, with some declared as public health emergencies of international concern [[1]Alonso P. Engels D. Reeder J Renewed push to strengthen vector control globally.Lancet. 2017; 389: 2270-2271Summary Full Text Full Text PDF PubMed Scopus (14) Google Scholar,[3]UN High-Level Panel on the Global Response to Health Crises. Protecting humanity from future health crises. New York: United Nations; 2016. Accessed 17 September 2020 http://www.un.org/News/dh/infocus/HLP/2016-02-05_Final_Report_Global_Response_to_Health_Crises.pdf.Google Scholar]. In 2016, a high-level panel on Global Response to Health Crises recommended strengthening emergency preparedness and response for various diseases including VBDs with emphasis on surveillance, and increasing resources for research and development for vaccines, therapeutics and diagnostics [[3]UN High-Level Panel on the Global Response to Health Crises. Protecting humanity from future health crises. New York: United Nations; 2016. Accessed 17 September 2020 http://www.un.org/News/dh/infocus/HLP/2016-02-05_Final_Report_Global_Response_to_Health_Crises.pdf.Google Scholar]. Accordingly, the World Health Organization underscores surveillance in the Global Vector Control Response 2017-2030 (GVCR) to inform evidence-based integrated vector management (IVM) [[4]WHOGlobal vector control response 2017–2030. World Health Organization, Geneva2016http://www.who.int/malaria/global-vector-control-response/Google Scholar]. Integrated entomological surveillance for arboviral diseases, malaria and lymphatic filariasis is key for effective vector control in urban areas [[5]Wilke A.B.B. Vasquez C. Carvajal A. et al.Cemeteries in Miami-Dade County, Florida are important areas to be targeted in mosquito management and control efforts.PLoS ONE. 2020; 15e0230748https://doi.org/10.1371/journal.pone.0230748Crossref PubMed Scopus (5) Google Scholar]. Cemeteries are usually situated in highly populated urbanized localities and serve as a harborage for populations of vector mosquito species due to availability of natural resources [[5]Wilke A.B.B. Vasquez C. Carvajal A. et al.Cemeteries in Miami-Dade County, Florida are important areas to be targeted in mosquito management and control efforts.PLoS ONE. 2020; 15e0230748https://doi.org/10.1371/journal.pone.0230748Crossref PubMed Scopus (5) Google Scholar]. While global surveillance on apposite vectors of arboviruses, urban malaria and lymphatic filariasis has been extensive and encompassing cemeteries, efforts remain outstandingly less exhaustive in Africa. Ae. aegypti is the primary vector of arboviruses and the invasive Ae. albopictus is a secondary vector, both breed in artificial water-filled containers like tyres, cisterns, flowerpots, vases, bromeliads, discarded jars, metal drums and construction sites. Lymphatic filariasis is primarily transmitted by An. mosquito species in rural areas and by Cx. quinquefasciatus in urban and peri-urban areas. An. stephensi breeds in man-made water storage containers such as wells, roof gutters, cisterns, domestic wells and water tanks alongside Ae. Aegypti and Cx. quinquefasciatus, both vectors of Rift Valley fever and West Nile fever [[2]Sinka M.E. Pironon S. Masseyc N.C. Longbottom J. Hemingway J. Moyes C.L. Willis K.J. A new malaria vector in Africa: predicting the expansion range of Anopheles stephensi and identifying the urban populations at risk.PNAS. 2020; : 1-9https://doi.org/10.1073/pnas.2003976117Crossref Scopus (45) Google Scholar]. These vectors also have differences and similarities in their bionomics including biting behavior, whereas Ae. aegypti is a day biting species, An. stephensi and Cx. quinquefasciatus biting times range from crepuscular to nocturnal. An. stephensi is an established malaria vector in Asia and the Middle East, and responsible for urban malaria epidemics. The species has invaded countries in the Horn of Africa in Djibouti, Ethiopia, Sudan and Somalia. Consequently, in 2019 a WHO Technical consultation assessed the situation and a vector alert was produced to prompt action [[6]WHO. Vector Alert: anopheles stephensi invasion and spread. https://www.who.int/news-room/detail/26-08-2019-vector-alert-anopheles-stephensiinvasion-and-spread. Accessed 17 September 2020.Google Scholar]. Insecticide resistance has developed in An. stephensi, Ae. aegypti and Cx. quinquefasciatus and threaten to compromise effective control of the peri‑domestic breeding and biting vectors [[7]Hemingway J. Ranson H. Magill A. et al.Averting a malaria disaster: will insecticide resistance derail malaria control?.Lancet. 2016; 387: 1785-1788Summary Full Text Full Text PDF PubMed Scopus (232) Google Scholar]. Given that Ae. aegypti and Cx. quinquefasciatus have been characterized in cemeteries [[8]Vezzani D Review: artificial container-breeding mosquitoes and cemeteries: a perfect match.Trop Med Int Health. 2007; 12: 299-313Crossref PubMed Scopus (89) Google Scholar], and data on An. stephensi, Ae. aegypti and Cx. quinquefasciatus in African cemeteries is non-existent (Table 1), integration with current malaria surveillance and research is essential.Table 1Mosquito vector species breeding in water-filled artificial containers including vases, flowerpots, bromeliads, discarded jars and bottles and natural habitats like bamboo stumps and tree-holes within cemeteries and the notable gap of data for Africa.Mosquito vector speciesGeographic location/ RegionReferencesAmericasEuropeSouth East Asia/ PacificAfricaAedes (Stegomyia) aegypti+++–(2,8)Aedes (Stegomyia) albopictus+++–(2,8)Ochlerotatus japonicas/Ochlerotatus triseriatus+++–(8,10)Culex quinquefasciatus+–+–(2,8)Culex pipiens complex+–+–(8)Culiseta incidens/ Cs. inornata+–––(8) Open table in a new tab Chikungunya, dengue, and Zika virus disease are devoid of specific treatment with challenging diagnoses, and candidate vaccines exists for chikungunya and Zika virus disease but licensed ones are not currently available. Vector control is the only available intervention albeit with minimal effectiveness in epidemics, necessitating innovation in development of tools that are amenable in epidemic and emergence settings [[9]Paixão E.S. Teixeira M.G. Rodrigues L.C Zika, chikungunya and dengue: the causes and threats of new and re-emerging arboviral diseases.BMJ Glob Health. 2017; 3e000530Google Scholar], particularly Wolbachia, gene drives, sterile insect technique, vector traps, attractive toxic sugar baits and spatial repellents. While effectiveness of vector control is contingent on entomological and epidemiological evidence, transformation from reactive to proactive and sustainable strategies including integration of neglected areas is critical [[9]Paixão E.S. Teixeira M.G. Rodrigues L.C Zika, chikungunya and dengue: the causes and threats of new and re-emerging arboviral diseases.BMJ Glob Health. 2017; 3e000530Google Scholar]. Cemeteries are potentially significant foci for proliferation of Aedes and Culex mosquito vectors [[8]Vezzani D Review: artificial container-breeding mosquitoes and cemeteries: a perfect match.Trop Med Int Health. 2007; 12: 299-313Crossref PubMed Scopus (89) Google Scholar], as demonstrated by entomological surveillance in Europe, the Americas, and South East Asia and the pacific, except in Africa (Table 1). Although regional and national policies, guidelines and frameworks on integrated management of arbovirus vectors have been formulated and promulgated with legislation enacted, cemeteries are still disproportionately disregarded in Africa. To eliminate VBDs in Africa, reinvigorated surveillance including integration of cemeteries as part of IVM will be indispensable. Harnessing salient bionomic and environmental attributes common to vectors for lymphatic filariasis, arboviruses and urban malaria would be critical to exploit the potential of IVM. Increasing urbanization provide ideal conditions for vectors and increases potential of community awareness and engagement [[2]Sinka M.E. Pironon S. Masseyc N.C. Longbottom J. Hemingway J. Moyes C.L. Willis K.J. A new malaria vector in Africa: predicting the expansion range of Anopheles stephensi and identifying the urban populations at risk.PNAS. 2020; : 1-9https://doi.org/10.1073/pnas.2003976117Crossref Scopus (45) Google Scholar]. Salient characteristics of breeding in water-filled flowerpots, vases, bromeliads, discarded jars, bottles and rainwater collection make Ae. aegypti, An. stephensi and Cx. quinquefasciatus presence in African urban cemeteries a plausible research postulate, and their sympatric-existence in water storage containers in peri‑domestic environments could optimize vector control [[2]Sinka M.E. Pironon S. Masseyc N.C. Longbottom J. Hemingway J. Moyes C.L. Willis K.J. A new malaria vector in Africa: predicting the expansion range of Anopheles stephensi and identifying the urban populations at risk.PNAS. 2020; : 1-9https://doi.org/10.1073/pnas.2003976117Crossref Scopus (45) Google Scholar,[8]Vezzani D Review: artificial container-breeding mosquitoes and cemeteries: a perfect match.Trop Med Int Health. 2007; 12: 299-313Crossref PubMed Scopus (89) Google Scholar]. Insecticide susceptibility monitoring and evaluation in disease vectors facilitates resistance management to sustain interventions [[7]Hemingway J. Ranson H. Magill A. et al.Averting a malaria disaster: will insecticide resistance derail malaria control?.Lancet. 2016; 387: 1785-1788Summary Full Text Full Text PDF PubMed Scopus (232) Google Scholar]. Aedes-transmitted Zoonoses potentiates improvement of multisectoral active surveillance within the One Health Approach. With increasing urbanization, built up environments have encroached on sprawling cemeteries in Africa. While the framework for implementation of the GVCR in Africa includes vector surveillance, research and innovation, there is a notable dearth of information on vector proliferation in cemeteries (Table 1). This disregard may result partly from the perception of cemeteries that connote enormous cultural and spiritual sensitivity [[10]Leisnham P.T. La Deau S.L. Juliano S.A Spatial and temporal habitat segregation of mosquitoes in urban Florida.PLoS ONE. 2014; 9:: e91655Crossref PubMed Scopus (48) Google Scholar]. Considering the threat of arboviral diseases and urban malaria epidemics, proactive entomological surveillance in cemeteries is eco-epidemiologically significant and vital for health security. Methodologies would encompass early detection and monitoring of mosquito vector species, ecological approaches to establish habitat preferences, and mosquito control studies to evaluate vector control tools [[8]Vezzani D Review: artificial container-breeding mosquitoes and cemeteries: a perfect match.Trop Med Int Health. 2007; 12: 299-313Crossref PubMed Scopus (89) Google Scholar]. There is need to promote research in cemeteries to generate requisite evidence and to hearten strong collaboration among the health sector, local authorities and pertinent partners with vested interests. Other partners include the environment sector, academic and research institutions, policy makers, funders, vector control implementers and communities. EC declares no competing interests.