Viral zoonoses at the human-animal interface in southern Africa: A systematic review

Abstract

Objective: To collate and summarize reports of viral zoonoses occurring at the human-animal interface in Southern Africa, along with their associated risk factors.
Methods: A comprehensive search was implemented in PubMed, Web of Science, Scopus and ProQuest databases for English language publications. The search used a combination of keywords for viral zoonoses, human-animal interface*, risk factor*, and countries in Southern Africa. The search covered the period from 1 January 2000 to 18 April 2024.
Results: A total of 893 records were retrieved from the database, with 17 articles included after screening. An additional 6 articles were identified through reference list tracking, yielding a total of 23 included articles. Domestic dog bites were identified as the primary source of rabies transmission across southern Africa, with only few cases linked to jackals, mongooses, and cats. Reported exposures for Rift Valley fever, Crimean-Congo hemorrhagic fever, influenza, hantavirus and Wesselsbron virus were all associated with occupational activities.
Conclusions: Preventive and mitigative strategies, such as dog rabies vaccination, post-exposure prophylaxis, and the use of personal protective equipment among animal workers - should be intensified across the region.

Keywords

Viral zoonoses / Human-animal interface / Spillover / Southern Africa

Conflict of interest statement

The authors claim there is no conflict of interest.

Funding

The study received no extramural funding.

Data availability statement

The data supporting the findings of this study are available from the corresponding author upon request.

Authors’ contributions

Epstein JH and Balami AD conceived the study. Epstein JH, Balami AD, Munro S, Ball S, and Sullivan A participated in the study design and manuscript review. Balami AD and Munro S did the data analysis and manuscript writing. All authors read and approved the final manuscript.

References

[1] Filho WL, Ternova L, Parasnis SA, Kovaleva M, Nagy GJ. Climate change and zoonoses: A review of concepts, definitions, and bibliometrics. Int J Environ Res Public Health 2022; 19(9): 5574.

[2] Jones KE, Patel NG, Levy MA, Storeygard A, Balk D, Gittleman JL, et al. Global trends in emerging infectious diseases. Nature 2008; 21(7181): 990-993.

[3] Reed KD. Viral Zoonoses. In: Reference module in biomedical sciences. Amsterdam: Elsevier; 2018.

[4] Kadam SB, Sukhramani GS, Bishnoi P, Pable AA, Barvkar VT. SARS-CoV-2, the pandemic coronavirus: Molecular and structural insights. J Basic Microbiol 2021; 18(3): 180-202.

[5] Fontanet A, Autran B, Lina B, Kieny MP, Karim SSA, Sridhar D. SARS-CoV-2 variants and ending the COVID-19 pandemic. Lancet 2021; 397(10278): 952-954.

[6] Chauhan RP, Dessie ZG, Noreddin A, El Zowalaty ME. Systematic review of important viral diseases in Africa in light of the ‘One Health’ concept. Pathogens 2020; 9(4): 301.

[7] Simpson G, Quesada F, Chatterjee P, Kakkar M, Chersich MF, Thys S. Research priorities for control of zoonoses in South Africa. Trans R Soc Trop Med Hyg 2021; 115(5): 538-550.

[8] Munang’andu HM, Mweene AS, Siamudaala V, Muma JB, Matandiko W. Rabies status in Zambia for the period 1985-2004. Zoonos Public Health 2011; 58(1): 21-27.

[9] Babaniyi O, Songolo P, Matapo B, Masaninga F, Mulenga F, Michelo C, et al. Epidemiological characteristics of rabies in Zambia: A retrospective study (2004-2013). Clin Epidemiol Glob Health 2016; 4(2): 83-88.

[10] Coetzer A, Gwenhure L, Makaya P, Markotter W, Nel L. Epidemiological aspects of the persistent transmission of rabies during an outbreak (2010-2017) in Harare, Zimbabwe. PLoS One 2019; 14(1): e0210018.

[11] Jori F, Alexander KA, Mokopasetso M, Munstermann S, Moagabo K, Paweska JT. Serological evidence of Rift Valley fever virus circulation in domestic cattle and African buffalo in northern Botswana (2010-2011). Front Vet Sci 2015; 2: 63.

[12] Moiane B, Mapaco L, Thompson P, Berg M, Albihn A, Fafetine J. High seroprevalence of Rift Valley fever phlebovirus in domestic ruminants and African Buffaloes in Mozambique shows need for intensified surveillance. Infect Ecol Epidemiol 2017; 7(1): 1416248.

[13] Lysholm S, Fischer K, Lindahl JF, Munyeme M, Wensman JJ. Seropositivity rates of zoonotic pathogens in small ruminants and associated public health risks at informal urban markets in Zambia. Acta Trop 2022; 225: 106217.

[14] van den Bergh C, Venter EH, Swanepoel R, Thompson PN. High seroconversion rate to rift valley fever virus in cattle and goats in far northern Kwazulu-Natal, South Africa, in the absence of reported outbreaks. PLoS Negl Trop Dis 2019; 13(5): e0007296.

[15] Pawęska JT, Msimang V, Kgaladi J, Hellferscee O, Weyer J, van Vuren PJ. Rift Valley fever virus seroprevalence among humans, Northern KwaZulu-Natal Province, South Africa, 2018-2019. Emerg Infect Dis 2021; 27(12): 3159-3162.

[16] Changula K, Kajihara M, Mori-Kajihara A, Eto Y, Miyamoto H, Yoshida R, et al. Seroprevalence of filovirus infection of rousettus aegyptiacus bats in Zambia. J Infect Dis 2018; 218(Suppl 5): S312-S317.

[17] Ogawa H, Miyamoto H, Nakayama E, Yoshida R, Nakamura I, Sawa H, et al. Seroepidemiological prevalence of multiple species of filoviruses in fruit bats (Eidolon helvum) migrating in Africa. J Infect Dis 2015; 212: S101-S108.

[18] Sinclair M, Brückner GK, Kotze JJ. Avian influenza in ostriches: Epidemiological investigation in the Western Cape Province of South Africa. Vet Ital 2006; 42(2): 69-76.

[19] Molini U, Yabe J, Meki IK, Ouled Ahmed Ben Ali H, Settypalli TBK, Datta S, et al. Highly pathogenic avian influenza H5N1 virus outbreak among Cape cormorants (Phalacrocorax capensis) in Namibia, 2022. Emerg Microbes Infect 2023; 12(1): 2167610.

[20] Muleya W, Sasaki M, Orba Y, Ishii A, Thomas Y, Nakagawa E, et al. Molecular epidemiology of paramyxoviruses in Frugivorous Eidolon helvum bats in Zambia. J Vet Med Sci 2014; 76(4): 611-614.

[21] Mortlock M, Geldenhuys M, Dietrich M, Epstein JH, Weyer J, Pawęska JT, et al. Seasonal shedding patterns of diverse henipavirus-related paramyxoviruses in Egyptian rousette bats. Sci Rep 2021; 11(1): 24262.

[22] Geldenhuys M, Mortlock M, Weyer J, Bezuidt O, Seamark ECJ, Kearney T, et al. A metagenomic viral discovery approach identifies potential zoonotic and novel mammalian viruses in Neoromicia bats within South Africa. PLoS One 2018; 13(3): e0194527.

[23] Chidoti V, De Nys H, Pinarello V, Mashura G, Missé D, Guerrini L, et al. Longitudinal survey of coronavirus circulation and diversity in insectivorous bat colonies in Zimbabwe. Viruses 2022; 14(4): 781.

[24] Ellwanger JH, Chies JAB. Zoonotic spillover: Understanding basic aspects for better prevention. Genet Mol Biol 2021; 44(1 Suppl 1): e20200355.

[25] Reperant LA, Cornaglia G, Osterhaus AD. The importance of understanding the human-animal interface: From early hominins to global citizens. Curr Top Microbiol Immunol 2013; 365: 49-81.

[26] Reperant LA, Osterhaus AD. The human-animal interface. In: Mackenzie JS, Jeggo M, Daszak P, Richt JA (Eds). One Health: The human-animal-environment interfaces in emerging infectious diseases. Washington, DC, USA: ASM Press; 2014. p. 33-52.

[27] Dreyer S, Dreier M, Dietze K. Demystifying a buzzword: Use of the term “human-animal-interface” in One Health oriented research based on a literature review and expert interviews. One Health 2023; 16: 100560.

[28] Alexander KA, McNutt JW. Human behavior influences infectious disease emergence at the human-animal interface. Front Ecol Environ 2010; 8(10): 522-526.

[29] Hassell JM, Begon M, Ward MJ, Fèvre EM. Urbanization and disease emergence: Dynamics at the wildlife-livestock-human interface. Trends Ecol Evol 2017; 32(1): 55-67.

[30] Magouras I, Brookes VJ, Jori F, Martin A, Pfeiffer DU, Dürr S. Emerging zoonotic diseases: Should we rethink the animal-human interface? Front Vet Sci 2020; 7: 582743.

[31] Sabin NS, Calliope AS, Simpson SV, Arima H, Ito H, Nishimura T, et al. Implications of human activities for (re)emerging infectious diseases, including COVID-19. J Physiol Anthropol 2020; 39(1): 29.

[32] Moher D. Preferred reporting items for systematic reviews and meta-analyses: The PRISMA Statement. Ann Intern Med 2009; 151(4): 264.

[33] Ouzzani M, Hammady H, Fedorowicz Z, Elmagarmid A. Rayyan-a web and mobile app for systematic reviews. Syst Rev 2016; 5(1): 210.

[34] Moola S, Munn Z, Tufanaru C, Aromataris E, Sears K, Sfetcu R, et al. Systematic reviews of etiology and risk. In: JBI Manual for Evidence Synthesis. Adelaide (AU): JBI; 2020.

[35] Galadima AN, Zulkefli NAM, Said SM, Ahmad N. Factors influencing childhood immunisation uptake in Africa: A systematic review. BMC Public Health 2021; 21(1): 1475.

[36] Szmyd-Potapczuk AV. Molecular epidemiology of human rabies diagnosed in South Africa between 1983 and 2007 [dissertation (MSc)]. University of Pretoria (South Africa); 2009.

[37] Weyer J, Le Roux CA, Kajese C, Fernandes L. A dog bite study in a dog rabies-affected area in South Africa. S Afr J Infect Dis 2020; 35(1): 1-7.

[38] Kubheka V, Govender P, Margot B, Kuonza LR. Dog bites and human rabies in the Uthungulu District of KwaZulu-Natal Province, 2008-2010: A review of surveillance data. S Afr J Epidemiol Infect 2013; 28(1): 33-40.

[39] Mollentze N, Weyer J, Markotter W, Le Roux K, Nel LH. Dog rabies in southern Africa: Regional surveillance and phylogeographical analyses are an important component of control and elimination strategies. Virus Genes 2013; 47(3): 569-573.

[40] Pfukenyi DM, Pawandiwa D, Makaya PV, Ushewokunze-Obatolu U. A retrospective study of rabies in humans in Zimbabwe, between 1992 and 2003. Acta Trop 2007; 102(3): 190-196.

[41] Chikanya E, Macherera M, Maviza A. An assessment of risk factors for contracting rabies among dog bite cases recorded in Ward 30, Murewa District, Zimbabwe. PLoS Negl Trop Dis 2021; 15(3): e0009305.

[42] Salomão C, Nacima A, Cuamba L, Gujral L, Amiel O, Baltazar C, et al. Epidemiology, clinical features and risk factors for human rabies and animal bites during an outbreak of rabies in Maputo and Matola cities, Mozambique, 2014: Implications for public health interventions for rabies control. PLoS Negl Trop Dis 2017; 11(7): e0005787.

[43] Hikufe EH, Freuling CM, Athingo R, Shilongo A, Ndevaetela EE, Helao M, et al. Ecology and epidemiology of rabies in humans, domestic animals and wildlife in Namibia, 2011-2017. PLoS Negl Trop Dis 2019; 13(4): e0007355.

[44] Archer BN, Thomas J, Weyer J, Cengimbo A, Landoh DE, Jacobs C, et al. Epidemiologic investigations into outbreaks of Rift Valley fever in humans, South Africa, 2008-2011. Emerg Infect Dis 2013; 19(12): 1918-1925.

[45] Gummow B. A survey of zoonotic diseases contracted by South African veterinarians. J S Afr Vet Assoc 2003; 74(3): 72-76.

[46] Msimang V, Thompson PN, van Vuren PJ, Tempia S, Cordel C, Kgaladi J, et al. Rift valley fever virus exposure amongst farmers, farm workers, and veterinary professionals in central South Africa. Viruses 2019; 11(2): 140.

[47] Van Vuren PJ, Kgaladi J, Patharoo V, Ohaebosim P, Msimang V, Nyokong B, et al. Human cases of Rift Valley fever in South Africa, 2018. Vector-Borne Zoonotic Diss 2018; 18(12): 713-715.

[48] Vawda S, Goedhals D, Bester PA, Burt F. Seroepidemiologic survey of crimean-congo hemorrhagic fever virus in selected risk groups, South Africa. Emerg Infect Dis 2018; 24(7): 1360-1363.

[49] Msimang V, Weyer J, le Roux C, Kemp A, Burt FJ, Tempia S, et al. Risk factors associated with exposure to Crimean-Congo haemorrhagic fever virus in animal workers and cattle, and molecular detection in ticks, South Africa. PLoS Negl Trop Dis 2021; 15(5): e0009384.

[50] Oludele J, Alho P, Chongo I, Maholela P, Magaia V, Muianga A, et al. Emerging Zoonotic diseases among pastoral communities of Caia and Búzi districts, Sofala, Mozambique: Evidence of antibodies against brucella, leptospira, rickettsia, and Crimean-Congo hemorrhagic fever virus. Viruses 2023; 15(12): 2379.

[51] El Zowalaty ME, Abdelgadir A, Borkenhagen LK, Ducatez MF, Bailey ES, Gray GC. Influenza A viruses are likely highly prevalent in South African swine farms. Transbound Emerg Dis 2022; 69(4): 2373-2383.

[52] Venter M, Treurnicht FK, Buys A, Tempia S, Samudzi R, McAnerney J, et al. Risk of human infections with Highly Pathogenic H5N2 and Low Pathogenic H7N1 Avian Influenza strains during outbreaks in ostriches in South Africa. J Infect Dis 2017; 216(suppl_4): S512-S519.

[53] Venter M, Steyl J, Human S, Weyer J, Zaayman D, Blumberg L, Leman PA, Paweska J, Swanepoel R. Transmission of West Nile virus during horse autopsy. Emerg Infect Dis 2010; 16(3): 573-575.

[54] Van Eeden C, Venter M. Investigation of viral causes of undiagnosed neurological disease in animals and their zoonotic risk to humans in South Africa. PhD dissertation. Pretoria (South Africa): University of Pretoria; 2014.

[55] Simpson GJG, Quan V, Frean J, Knobel DL, Rossouw J, Weyer J, et al. Prevalence of selected zoonotic diseases and risk factors at a human-wildlife-livestock interface in Mpumalanga Province, South Africa. Vector Borne Zoonotic Dis 2018; 18(6): 303-310.

[56] van der Westhuizen CG, Burt FJ, van Heerden N, van Zyl W, Anthonissen T, Musoke J. Prevalence and occupational exposure to zoonotic diseases in high-risk populations in the Free State Province, South Africa. Front Microbiol 2023; 14: 1196044.

[57] Weyer J, Thomas J, Leman PA, Grobbelaar AA, Kemp A, Paweska JT. Human cases of Wesselsbron disease, South Africa 2010-2011. Vector Borne Zoonotic Dis 2013; 13(5): 330-336.

[58] Dwyer JP, Douglas TS, van As AB. Dog bite injuries in children: A review of data from a South African paediatric trauma unit. S Afr Med J 2007; 97(8): 597-600.

[59] Duncan-Sutherland N, Lissaman AC, Shepherd M, Kool B. Systematic review of dog bite prevention strategies. Injury Prev 2022; 28(3): 288-297.

[60] Dlamini BN, Mdluli S, Mudyanavana C, Chikuni NE, Masarirambi MT. Rabies in Eswatini: What are the issues and challenges? J Adv Microbiol 2020; 20(7): 21-28.

[61] Cleaveland S, Kaare M, Tiringa P, Mlengeya T, Barrat J. A dog rabies vaccination campaign in rural Africa: Impact on the incidence of dog rabies and human dog-bite injuries. Vaccine 2003; 21(17-18): 1965-1973.

[62] Sánchez-Soriano C, Gibson AD, Gamble L, Burdon Bailey JL, Mayer D, Lohr F, et al. Implementation of a mass canine rabies vaccination campaign in both rural and urban regions in Southern Malawi. PLoS Negl Trop Dis 2020; 14(1): 1-19.

[63] Hampson K, Cleaveland S, Briggs D. Evaluation of cost-effective strategies for rabies post-exposure vaccination in low-income countries. PLoS Negl Trop Dis 2011; 5(3): e982.

[64] Nicholas DE, Jacobsen KH, Waters NM . Risk factors associated with human Rift Valley fever infection: Systematic review and meta-analysis. Tropic Med Int Health 2014; 19(12): 1420-1429.

[65] Gudo ES, Lesko B, Vene S, Lagerqvist N, Candido SI, Razão de Deus N, et al. Seroepidemiologic screening for zoonotic viral infections, Maputo, Mozambique. Emerg Infect Dis 2016; 22(5): 915-917.

[66] Vonesch N, Binazzi A, Bonafede M, Melis P, Ruggieri A, Iavicoli S, et al. Emerging zoonotic viral infections of occupational health importance. Pathog Dis 2019; 77(2): ftz018.

[67] Riccò M, Peruzzi S, Ranzieri S, Magnavita N. Occupational hantavirus infections in agricultural and forestry workers: A systematic review and metanalysis. Viruses 2021; 13(11): 2150.

[68] Riccò M, Baldassarre A, Corrado S, Bottazzoli M, Marchesi F. Seroprevalence of Crimean-Congo hemorrhagic fever virus in occupational settings: Systematic review and meta-analysis. Trop Med Infect Dis 2023; 8(9): 452.

[69] Kainga H, Mponela J, Basikolo L, Phonera MC, Mpundu P, Munyeme M, et al. Assessment of knowledge, attitudes, and practices towards Rift Valley fever among livestock farmers in selected districts of Malawi. Trop Med Infect Dis 2022; 7(8): 158.

[70] Hines JZ, Fwoloshi S, Kampamba D, Barradas DT, Banda D, Zulu JE, et al. SARS-CoV-2 Prevalence among outpatients during community transmission, Zambia, July 2020. Emerg Infect Dis 2021; 27(8): 2166-2168.

[71] Tambo E, Ugwu EC, Ngogang JY. Need of surveillance response systems to combat Ebola outbreaks and other emerging infectious diseases in African countries. Infect Dis Poverty 2014; 3: 1-8.

[72] Zinsstag J, Utzinger J, Probst-Hensch N, Shan L, Zhou XN. Towards integrated surveillance-response systems for the prevention of future pandemics. Infect Dis Poverty 2020; 9(1): 140.

[73] Pawęska JT, Jansen van Vuren P, Kemp A, Storm N, Grobbelaar AA, Wiley MR, et al. Marburg virus infection in Egyptian Rousette bats, South Africa, 2013-2014. Emerg Infect Dis 2018; 24(6): 1134-1137.