Seroprevalence and Risk Factors of Crimean–Congo Hemorrhagic Fever Exposure in Wild and Domestic Animals in Benin
Abstract
:1. Introduction
2. Materials and Methods
2.1. Study Area
2.2. Animal Sample Collection
2.3. Serological Analysis
2.4. Statistical Analysis
3. Results
4. Discussion
5. Conclusions
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Conflicts of Interest
References
- Chala, B.; Hamde, F. Emerging and re-emerging vector-borne infectious diseases and the challenges for control: A review. Front. Public Health 2021, 9, 715759. [Google Scholar] [CrossRef]
- Hanagandi, P.B.; Gonçalves, F.G.; do Amaral, L.L.F.; Chong, J.J.R.; Chankowsky, J.; Torres, C.I.; del Carpio, R.; Vakharia, R.J.; Torres, C.; Jaggi, S. Multidisciplinary Approach to Tropical and Subtropical Infectious Diseases: Imaging with Pathologic Correlation. Neurographics 2015, 5, 258–278. [Google Scholar] [CrossRef]
- Temur, A.I.; Kuhn, J.H.; Pecor, D.B.; Apanaskevich, D.A.; Keshtkar-Jahromi, M. Epidemiology of Crimean-Congo hemorrhagic fever (CCHF) in Africa—Underestimated for decades. Am. J. Trop. Med. Hyg. 2021, 104, 1978. [Google Scholar] [CrossRef]
- Belobo, J.T.E.; Kenmoe, S.; Kengne-Nde, C.; Emoh, C.P.D.; Bowo-Ngandji, A.; Tchatchouang, S.; Sowe Wobessi, J.N.; Mbongue Mikangue, C.A.; Tazokong, H.R.; Kingue Bebey, S.R. Worldwide epidemiology of Crimean-Congo Hemorrhagic Fever Virus in humans, ticks and other animal species, a systematic review and meta-analysis. PLoS Negl. Trop. Dis. 2021, 15, e0009299. [Google Scholar] [CrossRef]
- Bouchard, C.; Dibernardo, A.; Koffi, J.; Wood, H.; Leighton, P.A.; Lindsay, L.R. Climate change and infectious diseases: The challenges: N Increased risk of tick-borne diseases with climate and environmental changes. Can. Commun. Dis. Rep. 2019, 45, 83. [Google Scholar] [CrossRef]
- Spengler, J.R.; Estrada-Peña, A. Host preferences support the prominent role of Hyalomma ticks in the ecology of Crimean-Congo hemorrhagic fever. PLoS Negl. Trop. Dis. 2018, 12, e0006248. [Google Scholar] [CrossRef]
- Nasirian, H. Crimean-Congo hemorrhagic fever (CCHF) seroprevalence: A systematic review and meta-analysis. Acta Trop. 2019, 196, 102–120. [Google Scholar] [CrossRef]
- White, N.J.; Watson, J.A.; Uyoga, S.; Williams, T.N.; Maitland, K.M. Substantial misdiagnosis of severe malaria in African children. Lancet 2022, 400, 807. [Google Scholar] [CrossRef]
- Vonesch, N.; Binazzi, A.; Bonafede, M.; Melis, P.; Ruggieri, A.; Iavicoli, S.; Tomao, P. Emerging zoonotic viral infections of occupational health importance. Pathog. Dis. 2019, 77, ftz018. [Google Scholar] [CrossRef]
- Spengler, J.R.; Bergeron, É.; Rollin, P.E. Seroepidemiological studies of Crimean-Congo hemorrhagic fever virus in domestic and wild animals. PLoS Negl. Trop. Dis. 2016, 10, e0004210. [Google Scholar] [CrossRef]
- Bernard, C.; Holzmuller, P.; Bah, M.T.; Bastien, M.; Combes, B.; Jori, F.; Grosbois, V.; Vial, L. Systematic review on Crimean–Congo hemorrhagic fever enzootic cycle and factors favoring virus transmission: Special focus on France, an apparently free-disease area in Europe. Front. Vet. Sci. 2022, 9, 932304. [Google Scholar] [CrossRef]
- Corniaux, C.; Thébaud, B.; Powell, A.; Apolloni, A.; Touré, I. Cross-Border Livestock Mobility: Challenges for Wet Africa; Academia: San Francisco, CA, USA, 2018. [Google Scholar]
- Estrada-Peña, A.; Gray, J.S.; Kahl, O.; Lane, R.S.; Nijhoff, A.M. Research on the ecology of ticks and tick-borne pathogens—Methodological principles and caveats. Front. Cell. Infect. Microbiol. 2013, 3, 29. [Google Scholar] [CrossRef]
- Spengler, J.R.; Estrada-Peña, A.; Garrison, A.R.; Schmaljohn, C.; Spiropoulou, C.F.; Bergeron, É.; Bente, D.A. A chronological review of experimental infection studies of the role of wild animals and livestock in the maintenance and transmission of Crimean-Congo hemorrhagic fever virus. Antivir. Res. 2016, 135, 31–47. [Google Scholar] [CrossRef]
- Mukhaye, E.; Akoko, J.M.; Nyamota, R.; Mwatondo, A.; Muturi, M.; Nthiwa, D.; Kirwa, L.J.; Bargul, J.L.; Abkallo, H.M.; Bett, B. Exposure patterns and the risk factors of Crimean Congo hemorrhagic fever virus amongst humans, livestock and selected wild animals at the human/livestock/wildlife interface in Isiolo County, upper eastern Kenya. PLoS Negl. Trop. Dis. 2024, 18, e0012083. [Google Scholar] [CrossRef]
- Muzammil, K.; Rayyani, S.; Abbas Sahib, A.; Gholizadeh, O.; Naji Sameer, H.; Jwad Kazem, T.; Badran Mohammed, H.; Ghafouri Kalajahi, H.; Zainul, R.; Yasamineh, S. Recent Advances in Crimean-Congo Hemorrhagic Fever Virus Detection, Treatment, and Vaccination: Overview of Current Status and Challenges. Biol. Proced. Online 2024, 26, 20. [Google Scholar] [CrossRef]
- Daodu, O.B.; Eisenbarth, A.; Schulz, A.; Hartlaub, J.; Olopade, J.O.; Oluwayelu, D.O.; Groschup, M.H. Molecular detection of dugbe orthonairovirus in cattle and their infesting ticks (Amblyomma and Rhipicephalus (Boophilus)) in Nigeria. PLoS Negl. Trop. Dis. 2021, 15, e0009905. [Google Scholar] [CrossRef]
- Hartlaub, J.; Daodu, O.B.; Sadeghi, B.; Keller, M.; Olopade, J.; Oluwayelu, D.; Groschup, M.H. Cross-Reaction or Co-Infection? Serological Discrimination of Antibodies Directed against Dugbe and Crimean-Congo Hemorrhagic Fever Orthonairovirus in Nigerian Cattle. Viruses 2021, 13, 1398. [Google Scholar] [CrossRef] [PubMed]
- Matthews, J.; Secka, A.; McVey, D.S.; Dodd, K.A.; Faburay, B. Serological Prevalence of Crimean–Congo Hemorrhagic Fever Virus Infection in Small Ruminants and Cattle in The Gambia. Pathogens 2023, 12, 749. [Google Scholar] [CrossRef]
- Oumorou, M.; Lejoly, J. Écologie, flore et végétation de l’inselberg Sobakpérou (nord-Bénin). Acta Bot. Gall. 2003, 150, 65–84. [Google Scholar] [CrossRef]
- Vanvanhossou, S.F.U.; Dossa, L.H.; König, S. Sustainable management of animal genetic resources to improve low-input livestock production: Insights into local Beninese cattle populations. Sustainability 2021, 13, 9874. [Google Scholar] [CrossRef]
- Yassegoungbe, F.P.; Oloukoi, D.; Aoudji, A.K.N.; Schlecht, E.; Dossa, L.H. Insights into the diversity of cow milk production systems on the fringes of coastal cities in West Africa: A case study from Benin. Front. Sustain. Food Syst. 2022, 6, 1001497. [Google Scholar] [CrossRef]
- Houessou, S.O.; Dossa, L.H.; Diogo, R.V.C.; Ahozonlin, M.C.; Dahouda, M.; Schlecht, E. Confronting pastoralists’ knowledge of cattle breeds raised in the extensive production systems of Benin with multivariate analyses of morphological traits. PLoS ONE 2019, 14, e0222756. [Google Scholar] [CrossRef]
- Ahozonlin, M.C.; Gbangboche, A.B.; Dossa, L.H. Current Knowledge on the Lagune Cattle Breed in Benin: A State of the Art Review. Ruminants 2022, 2, 271–281. [Google Scholar] [CrossRef]
- Scherf, B.D.; Pilling, D. The Second Report on the State of the World’s Animal Genetic Resources for Food and Agriculture; Food and Agriculture Organization: Rome, Italy, 2015. [Google Scholar]
- Fanelli, A.; Buonavoglia, D. Risk of Crimean Congo haemorrhagic fever virus (CCHFV) introduction and spread in CCHF-free countries in southern and Western Europe: A semi-quantitative risk assessment. One Health 2021, 13, 100290. [Google Scholar] [CrossRef]
- Kuehnert, P.A.; Stefan, C.P.; Badger, C.V.; Ricks, K.M. Crimean-Congo Hemorrhagic Fever Virus (CCHFV): A Silent but Widespread Threat. Curr. Trop. Med. Rep. 2021, 8, 141–147. [Google Scholar] [CrossRef]
- Schüpbach, G.; Silva, L.C.; Buzzell-Hatav, A. Surveillance plan proposal for early detection of zoonotic pathogens in ruminants. EFSA Support. Publ. 2023, 20, 7887E. [Google Scholar] [CrossRef]
- Bespyatova, L.A.; Bugmyrin, S.V.; Kutenkov, S.A.; Nikonorova, I.A. Abundance of Ixodid Ticks (Acari: Ixodidae) on Small Mammals in Forest Biotopes of the Middle Taiga Subzone of Karelia. Entomol. Rev. 2021, 101, 273–281. [Google Scholar] [CrossRef]
- Estrada-Peña, A.; de la Fuente, J. The ecology of ticks and epidemiology of tick-borne viral diseases. Antivir. Res. 2014, 108, 104–128. [Google Scholar] [CrossRef]
- Shah, T.; Li, Q.; Wang, B.; Baloch, Z.; Xia, X. Geographical distribution and pathogenesis of ticks and tick-borne viral diseases. Front. Microbiol. 2023, 14, 1185829. [Google Scholar] [CrossRef]
- Palomar, A.M.; Portillo, A.; Santibáñez, P.; Mazuelas, D.; Arizaga, J.; Crespo, A.; Gutiérrez, Ó.; Cuadrado, J.F.; Oteo, J.A. Crimean-Congo hemorrhagic fever virus in ticks from migratory birds, Morocco. Emerg. Infect. Dis. 2013, 19, 260. [Google Scholar] [CrossRef]
- Chumakov, M.P. Translation Editor’s Introduction. In A Translation of “Crimean Hemorrhagic Fever”: Papers from the Third Regional Workshop at Rostov-on-Don in May 1970; Chumakov, M.P., Ed.; SPIE: St Bellingham, WA, USA, 1974. [Google Scholar] [CrossRef]
- Assogbadjo, A.E.; Codjia, J.T.C.; Sinsin, B.; Ekue, M.R.M.; Mensah, G.A. Importance of rodents as a human food source in Benin. Belg. J. Zool. 2005, 135, 11–15. [Google Scholar]
- Yessinou, R.E.; Adoligbe, C.; Akpo, Y.; Adinci, J.; Youssao Abdou Karim, I.; Farougou, S. Sensitivity of Different Cattle Breeds to the Infestation of Cattle Ticks Amblyomma variegatum, Rhipicephalus microplus, and Hyalomma spp. on the Natural Pastures of Opkara Farm, Benin. J. Parasitol. Res. 2018, 2018, 2570940. [Google Scholar] [CrossRef]
- Kumsa, B.; Tamrat, H.; Tadesse, G.; Aklilu, N.; Cassini, R. Prevalence and species composition of ixodid ticks infesting horses in three agroecologies in central Oromia, Ethiopia. Trop. Anim. Health Prod. 2012, 44, 119–124. [Google Scholar] [CrossRef]
- Payne, V.K.; Mbafor, F.L.; Wabo Pone, J.; Tchoumboué, J. Preliminary study of ectoparasites of horses in the western highlands of Cameroon. Vet. Med. Sci. 2017, 3, 63–70. [Google Scholar] [CrossRef]
- Mangombi, J.B.; Roqueplo, C.; Sambou, M.; Dahmani, M.; Mediannikov, O.; Comtet, L.; Davoust, B. Seroprevalence of Crimean-Congo hemorrhagic fever in domesticated animals in Northwestern Senegal. Vector-Borne Zoonotic Dis. 2020, 20, 797–799. [Google Scholar] [CrossRef]
- Oluwayelu, D.; Afrough, B.; Adebiyi, A.; Varghese, A.; Eun-Sil, P.; Fukushi, S.; Yoshikawa, T.; Saijo, M.; Neumann, E.; Morikawa, S.; et al. Prevalence of Antibodies to Crimean-Congo Hemorrhagic Fever Virus in Ruminants, Nigeria, 2015. Emerg. Infect. Dis. 2020, 26, 744–747. [Google Scholar] [CrossRef]
- Dzikwi-Emennaa, A.A.; Meseko, C.; Emennaa, P.; Adeyinka, A.J.; Adamu, A.M.; Adegboye, O.A. Detection of Crimean-Congo Hemorrhagic Fever Virus Antibodies in Cattle in Plateau State, Nigeria. Viruses 2022, 14, 2618. [Google Scholar] [CrossRef]
- Maiga, O.; Sas, M.A.; Rosenke, K.; Kamissoko, B.; Mertens, M.; Sogoba, N.; Traore, A.; Sangare, M.; Niang, M.; Schwan, T.G. Serosurvey of Crimean–Congo hemorrhagic fever virus in cattle, Mali, West Africa. Am. J. Trop. Med. Hyg. 2017, 96, 1341. [Google Scholar] [CrossRef]
- Schulz, A.; Barry, Y.; Stoek, F.; Ba, A.; Schulz, J.; Haki, M.L.; Sas, M.A.; Doumbia, B.A.; Kirkland, P.; Bah, M.Y. Crimean-Congo hemorrhagic fever virus antibody prevalence in Mauritanian livestock (cattle, goats, sheep and camels) is stratified by the animal’s age. PLoS Negl. Trop. Dis. 2021, 15, e0009228. [Google Scholar] [CrossRef]
- Valery, A.E.; Aimée, D.-K.C.; Maxime, D.K.; Clémence, K.K.A.R.M.; Mireille, D. Serosurvey of Crimean-Congo Haemorrhagic Fever Virus (CCHFV) in Cattle in Livestock Areas of Côte d’Ivoire, West Africa. Microbiol. Res. J. Int. 2021, 31, 11–18. [Google Scholar] [CrossRef]
- Phonera, M.C.; Simuunza, M.C.; Kainga, H.; Ndebe, J.; Chembensofu, M.; Chatanga, E.; Kanyanda, S.; Changula, K.; Muleya, W.; Mubemba, B. Seroprevalence and risk factors of Crimean-Congo hemorrhagic fever in cattle of smallholder farmers in Central Malawi. Pathogens 2021, 10, 1613. [Google Scholar] [CrossRef]
- Karanam, S.K.; Nagvishnu, K.; Uppala, P.K.; Edhi, S.; Varri, S.R. Crimean-Congo hemorrhagic fever: Pathogenesis, transmission and public health challenges. World J. Virol. 2025, 14, 100003. [Google Scholar] [CrossRef]
Variable | * n/N | Seroprevalence % ± 95% CI | Odds Ratio ± 95% CI | p-Value |
---|---|---|---|---|
Overall | 3/254 | 1.18 (0.31–3.70) | ||
Species | ||||
Giant rat | 1/84 | 1.19 (0.06–7.38) | REF | - |
Squirrel | 1/27 | 3.7 (0.19–20.89) | 0.32 (0.004; 25.53) | 0.17 |
Hare | 1/17 | 5.88 (0.31–30.76) | 0.20 (0.002; 16.07) | 0.09 |
Grasscutter | 0/49 | 0 (0.00–9.06) | - | 0.50 |
Crow | 0/3 | 0 (0.00–69.00) | - | 0.50 |
Bat | 0/30 | 0 (0.00–14.13) | - | 0.50 |
Birds | 0/21 | 0 (0.00–19.24) | - | 0.50 |
Antelope | 0/5 | 0 (0.00–53.71) | - | 0.50 |
Monkey | 0/9 | 0 (0.00–37.12) | - | 0.50 |
Cattle egret | 0/9 | 0 (0.00–37.12) | - | 0.50 |
District/wild animal | ||||
Aplahoué | 2/56 | 3.57 (0.62–13.38) | REF | - |
Matéri | 1/4 | 25 (1.32–78.06) | 8.33 (0.12–209.41) | 0.04 |
Allada | 0/65 | 0 (0.00–6.95) | - | 0.06 |
Adjarra | 0/10 | 0 (0.00–34.45) | - | 0.26 |
Kpomassè | 0/36 | 0 (0.00–12.01) | - | 0.11 |
Djidja | 0/41 | 0 (0.00–10.67) | - | 0.01 |
Adja-Ouèrè | 0/4 | 0 (0.00–60.42) | - | 0.34 |
Tanguiéta | 0/11 | 0 (0.00–32.15) | - | 0.25 |
Banikoara | 0/5 | 0 (0.00–53.71) | - | 0.33 |
Djougous | 0/9 | 0 (0.00–37.12) | - | 0.27 |
Natitingou | 0/9 | 0 (0.00–37.12) | - | 0.27 |
Parakou | 0/3 | 0 (0.00–69.00) | - | 0.36 |
Pobè | 0/1 | 0 (0.00–94.54) | - | 0.36 |
Variable | * n/N | Seroprevalence % ± 95% CI | Odds Ratio ± 95% CI | p-Value |
---|---|---|---|---|
Overall | 38/112 | 33.93 (25.42–43.56) | - | - |
Species/domestic animal | ||||
Cattle | 34/81 | 41.98 (31.26–53.46) | REF | - |
Horse | 4/24 | 16.67 (5.48–38.19) | 0.28 (0.06–0.94) | 0.013 |
Pigeon | 0/7 | 0 (0.00–43.91) | 0 (0.00–1.04) | 0.016 |
District/cattle | ||||
Tanguieta | 5/16 | 31.25 (12.13–58.52) | REF | - |
Djougou | 7/14 | 50.00 (26.80–73.20) | 0.47 (0.08–2.53) | 0.149 |
Matéri | 11/17 | 64.71 (38.62–84.74) | 0.26 (0.05–1.29) | 0.031 |
Gogounou | 4/9 | 44.44 (15.34–77.35) | 0.58 (0.08–4.30) | 0.254 |
Aplahoué | 5/13 | 38.46 (15.14–67.72) | 0.74 (0.12–4.44) | 0.339 |
Djidja | 2/12 | 16.67 (2.94–49.12) | 2.21 (0.28–28.21) | 0.197 |
District/horse | ||||
Tanguieta | 1/4 | 25.00 (1.32–78.06) | REF | - |
Djougou | 2/13 | 15.39 (2.71–46.34) | 1.76 (0.02–46.78) | 0.333 |
Matéri | 1/7 | 14.29 (0.75–57.99) | 1.87 (0.02–182.41) | 0.334 |
Risk Factors | Cattle (34/81) | ||||
---|---|---|---|---|---|
* n/N | % ± 95% CI | Odds Ratio ± 95% CI | p-Value | ||
Sex | F | 24/34 | 70.59 (52.33–84.29) | REF | - |
M | 10/34 | 29.41 (15.71–47.67) | 0.18 (0.05–0.55) | 0.00 | |
Age | [0–5[ | 5/34 | 14.71 (5.54–31.83) | REF | - |
[5–10[ | 18/34 | 52.94 (35.40–69.84) | 6.33 (1.83–26.11) | 0.00 | |
[10–→[ | 11/34 | 32.35 (17.98–50.63) | 2.73 (0.74–11.53) | 0.049 | |
Transhumance | Nomadism | 19/34 | 55.88 (38.09–72.28) | REF | - |
Sedentary | 4/34 | 11.76 (3.84–28.39) | 0.11 (0.02–0.41) | 0.00 | |
Semi-nomadism | 11/34 | 32.35 (17.98–50.63) | 0.38 (0.13–1.13) | 0.03 | |
Agroecological zone | North Benin Cotton Zone II | 4/34 | 11.76 (3.84–28.39) | REF | - |
West Atacora Zone IV | 23/34 | 67.65 (49.37–82.03) | 14.91 (3.93–73.07) | 0.00 | |
- Central Benin Cotton Zone V | 7/34 | 20.59 (9.34–38.41) | 1.93 (0.43–9.99) | 0.17 |
Disclaimer/Publisher’s Note: The statements, opinions and data contained in all publications are solely those of the individual author(s) and contributor(s) and not of MDPI and/or the editor(s). MDPI and/or the editor(s) disclaim responsibility for any injury to people or property resulting from any ideas, methods, instructions or products referred to in the content. |
© 2025 by the authors. Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (https://creativecommons.org/licenses/by/4.0/).
Share and Cite
Yessinou, R.E.; Farougou, S.; Olopade, J.O.; Oluwayelu, D.O.; Happi, A.; Happi, C.; Groschup, M. Seroprevalence and Risk Factors of Crimean–Congo Hemorrhagic Fever Exposure in Wild and Domestic Animals in Benin. Viruses 2025, 17, 387. https://doi.org/10.3390/v17030387
Yessinou RE, Farougou S, Olopade JO, Oluwayelu DO, Happi A, Happi C, Groschup M. Seroprevalence and Risk Factors of Crimean–Congo Hemorrhagic Fever Exposure in Wild and Domestic Animals in Benin. Viruses. 2025; 17(3):387. https://doi.org/10.3390/v17030387
Chicago/Turabian StyleYessinou, Roland Eric, Souaïbou Farougou, James Olukayode Olopade, Daniel Oladimeji Oluwayelu, Anise Happi, Christian Happi, and Martin Groschup. 2025. "Seroprevalence and Risk Factors of Crimean–Congo Hemorrhagic Fever Exposure in Wild and Domestic Animals in Benin" Viruses 17, no. 3: 387. https://doi.org/10.3390/v17030387
APA StyleYessinou, R. E., Farougou, S., Olopade, J. O., Oluwayelu, D. O., Happi, A., Happi, C., & Groschup, M. (2025). Seroprevalence and Risk Factors of Crimean–Congo Hemorrhagic Fever Exposure in Wild and Domestic Animals in Benin. Viruses, 17(3), 387. https://doi.org/10.3390/v17030387