Skip to main content

Advertisement

Log in

Seroprevalence of Rift Valley fever in cattle of smallholder farmers in Kwilu Province in the Democratic Republic of Congo

  • Regular Articles
  • Published:
Tropical Animal Health and Production Aims and scope Submit manuscript

Abstract

Rift Valley fever (RVF) is a zoonotic mosquito-borne disease caused by RVF virus (RVFV) that causes abortions and high mortalities in livestock and is also associated with acute and fatal disease in humans. In the Democratic Republic of Congo (DRC), information on the epidemiology of RVF is limited, particularly among cattle reared by smallholder farmers. This cross-sectional study was conducted to investigate the seroprevalence of RVF in cattle raised by smallholder farmers in Kwilu Province of DRC, which has not yet reported an RVF epidemic. A total of 677 cattle sera were collected from four territories and tested for anti-RVFV antibodies using immunofluorescent assay and enzyme-linked immunosorbent assay. The overall seroprevalence of anti-RVFV IgG was 6.5% (44/677) (95% CI 4.81–8.7). There was a statistically significant difference in the seroprevalence among the territories (χ2 = 28.79, p < 0.001). Territory seroprevalences were as follows: Idiofa 14.08% (95% CI 9.78–19.76), Bulungu 4.14% (95% CI 1.83–8.68), Gungu 3.21% (95% CI 1.41–6.78), and Masi-Manimba 1.19% (95% CI 0.06–7.37). Seroprevalence differed significantly among age categories (p = 0.0017) and ecosystem (p < 0.001). The seroprevalence of animals aged between 1 and 2 years was 20.0% (95% CI 8.4–39.13) and was higher than group aged <1 year, between 2 and 3 years, and > 3 years. Forest area (18.92% (95% CI 12.35–27.7)) had higher seropositivity than savannah area (4.06% (95% CI 2.65–6.12)). Sex difference was not significant (χ2 = 0.14, p = 0.704). These findings indicate that cattle in Kwilu Province had been exposed to RVFV, which represents a significant risk for both livestock and human health.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2

Similar content being viewed by others

References

  • Abakar, M. F., Naré, N. B., Schelling, E., Hattendorf, J., Alfaroukh, I. O., and Zinsstag, J., 2014. Seroprevalence of Rift Valley fever, Q fever, and brucellosis in ruminants on the southeastern shore of Lake Chad. Vector-Borne and Zoonotic Diseases, 14, 757–762.

    PubMed  Google Scholar 

  • Andriamandimby, S. F., Randrianarivo-Solofoniaina, A. E., Jeanmaire, E. M., Ravololomanana, L., Razafimanantsoa, L. T., Rakotojoelinandrasana, T., Razainirina, J., Hoffmann, J., Ravalohery, J. P., Rafisandratantsoa, J. T., Rollin, P. E., and Reynes, J. M., 2010. Rift Valley fever during rainy seasons, Madagascar, 2008 and 2009. Emerging Infectious Diseases, 16, 963–970.

    PubMed  PubMed Central  CAS  Google Scholar 

  • Bird, B. H., Bawiec, D. A., Ksiazek, T. G., Shoemaker, T. R., and Nichol, S. T., 2007. Highly sensitive and broadly reactive quantitative reverse transcription-PCR assay for high-throughput detection of Rift Valley fever virus. Journal of Clinical Microbiology, 45, 3506–3513.

    PubMed  PubMed Central  CAS  Google Scholar 

  • Bird, B. H., Githinji, J. W. K., Macharia, J. M., Kasiiti, J. L., Muriithi, R. M., Gacheru, S. G., Musaa, J. O., Towner, J. S., Reeder, S. A., Oliver, J. B., Stevens, T. L., Erickson, B. R., Morgan, L. T., Khristova, M. L., Hartman, A. L., Comer, J. A., Rollin, P. E, Ksiazek, T. G., and Nichol, S. T., 2008. Multiple virus lineages sharing recent common ancestry were associated with a large Rift Valley fever outbreak among livestock in Kenya during 2006–2007. Journal of Virology, 82, 11152–11166.

    PubMed  PubMed Central  CAS  Google Scholar 

  • Bird, B. H., Ksiazek, T. G., Nichol, S. T., and MacLachlan, N. J., 2009. Rift Valley fever virus. Journal of the American Veterinary Medical Association, 234, 883–893.

    PubMed  Google Scholar 

  • Boko, M., Niang, I., Nyong, A., Vogel, C., Githeko, A., Medany, M., Osman-Elasha, B., Tabo, R., and Yanda, P., 2008. Africa, Climate change 2007: impacts, adaptation and vulnerability. Contribution of Working Group II to the Fourth Assessment Report of the Intergovernmental Panel on Climate Change.

  • Bouloy, M., and Weber, F., 2010. Molecular biology of Rift Valley fever virus. The Open Virology Journal, 4, 8–14.

    PubMed  PubMed Central  CAS  Google Scholar 

  • Chengula, A. A., Kasanga, C. J., Mdegela, R. H., Sallu, R., and Yongolo, M., 2014. Molecular detection of Rift Valley fever virus in serum samples from selected areas of Tanzania. Tropical Animal Health and Production, 46, 629–634.

    PubMed  Google Scholar 

  • Chevalier, V., de la Rocque S., Baldet, T., Vial, L., and Roger, F., 2004. Epidemiological processes involved in the emergence of vector-borne diseases: West Nile fever, Rift Valley fever, Japanese encephalitis and Crimean-Congo haemorrhagic fever. Revue Scientifique et Technique de l’OIE, 23, 535–555.

    PubMed  CAS  Google Scholar 

  • Chevalier, V., Rakotondrafara, T., Jourdan, M., Heraud, J. M., Andriamanivo, H. R., Durand, B., Ravaomanana, J., Rollin, P. E., and Rakotondravao, R., 2011. An unexpected recurrent transmission of Rift Valley fever virus in cattle in a temperate and mountainous area of Madagascar. PLoS Neglected Tropical Diseases, 5: e1423.

    PubMed  PubMed Central  Google Scholar 

  • Coetzer, J. A., 1977. The pathology of Rift Valley fever. I. Lesions occurring in natural cases in new-born lambs. The Onderstepoort Journal of Veterinary Research, 44, 205–211.

    PubMed  CAS  Google Scholar 

  • Coetzer, J. A., 1982. The pathology of Rift Valley fever. II. Lesions occurring in field cases in adult cattle, calves and aborted foetuses. The Onderstepoort Journal of Veterinary Research, 49, 11–17.

    PubMed  CAS  Google Scholar 

  • Coetzer, J. A. W., Thomson, G. R., and Tustin, R. C., 1994. Infectious diseases of livestock with special reference to Southern Africa. African horsesickness. Oxford University Press Oxford, United Kingdom, pp. 460–475.

  • Davies, F. G., 2010. The historical and recent impact of Rift Valley fever in Africa. American Journal of Tropical Medicine and Hygiene, 83, 73–74.

    PubMed  Google Scholar 

  • Davies, F. G., Linthicum, K. J., and James, A. D., 1985. Rainfall and epizootic Rift Valley fever. Bulletin of the World Health Organization, 63, 941–943.

    PubMed  PubMed Central  CAS  Google Scholar 

  • Davies, F. G., and Martin, V., 2003. Recognizing Rift Valley fever. Food and Agriculture Organisation, viewed n.d, vol (17).

  • Dohoo, I. R., Martin, W., and Stryhn, H., 2003. Veterinary epidemiologic research. AVC Incorporated Charlottetown, Canada, p.27–407.

  • Fafetine, J., Neves, L., Thompson, P. N., Paweska, J. T., Rutten, V. P. M. G., and Coetzer, J. A. W., 2013. Serological evidence of Rift Valley fever virus circulation in sheep and goats in Zambézia Province, Mozambique. PLoS Neglected Tropical Diseases, 7, e2065.

    PubMed  PubMed Central  Google Scholar 

  • Faye, O., Diallo, M., Diop, D., Bezeid, O. E., Bâ, H., Niang, M., Dia, I., Mohamed, S. A.O., Ndiaye, K., Diallo, D., Ly, P. O., Diallo, B., Nabeth, P., Simon, F., Lô, B., and Diop, O. M., 2007. Rift Valley fever outbreak with East-Central African virus lineage in Mauritania, 2003. Emerging Infectious Diseases, 13, 1016–1024.

    PubMed  PubMed Central  CAS  Google Scholar 

  • Fontenille, D., Traore-Lamizana, M., Diallo, M., Thonnon, J., Digoutte, J. P., and Zeller, H. G., 1998. New vectors of Rift Valley fever in West Africa. Emerging Infectious Diseases, 4, 289–293.

    PubMed  PubMed Central  CAS  Google Scholar 

  • Formenty, P., Domenech, J., and Zeller, H. G., 1992. Enquête sérologique sur la fièvre de la vallée du Rift, chez les ovins, en Côte d’Ivoire. Revue d’élevage et de Médecine Vétérinaire Des Pays Tropicaux, 45, 221–226.

    PubMed  CAS  Google Scholar 

  • Gad, A. M., Feinsod, F. M., Allam, I. H., Eisa, M., Hassan, A. N., Soliman, B. A., el Said, S., and Saah, A. J., 1986. A possible route for the introduction of Rift Valley fever virus into Egypt during 1977. The Journal of Tropical Medicine and Hygiene, 89, 233–236.

    PubMed  CAS  Google Scholar 

  • Georges, T. M., Justin, M., Victor, M., Marie, K. J., Mark, R., and Léopold, M. M. K., 2018. Seroprevalence and virus activity of Rift Valley fever in cattle in eastern region of Democratic Republic of the Congo. Journal of Veterinary Medicine, 2018.

  • Gerrard, S. R., and Nichol, S. T., 2007. Synthesis, proteolytic processing and complex formation of N-terminally nested precursor proteins of the Rift Valley fever virus glycoproteins. Virology, 357, 124–133.

    PubMed  CAS  Google Scholar 

  • International Committee on Taxonomy of Viruses. Virus taxonomy, 2018. Available at https://talk.ictvonline.org/taxonomy.

  • Jeanmaire, E. M., Rabenarivahiny, R., Biarmann, M., Rabibisoa, L., Ravaomanana, F., Randriamparany, T., Fy Andriamandimby, S., Diaw, C. S., Fenozara, P., de La Rocque, S., and Reynes, J.-M., 2011. Prevalence of Rift Valley fever infection in ruminants in Madagascar after the 2008 outbreak. Vector-Borne and Zoonotic Diseases, 11, 395–402.

    PubMed  Google Scholar 

  • Kifaro, E. G., Nkangaga, J., Joshua, G., Sallu, R., Yongolo, M., Dautu, G., and Kasanga, C. J., 2014. Epidemiological study of Rift Valley fever virus in Kigoma, Tanzania. The Onderstepoort Journal of Veterinary Research, 81, 1–5.

    Google Scholar 

  • LaBeaud, A. D., Muchiri, E. M., Ndzovu, M., Mwanje, M. T., Muiruri, S., Peters, C. J., and King, C. H., 2008. Interepidemic Rift Valley fever virus seropositivity, northeastern Kenya. Emerging Infectious Diseases, 14, 1240–1246.

    PubMed  PubMed Central  Google Scholar 

  • Laughlin, L. W., Meegan, J. M., Strausbaugh, L. J., Moren, D. M., and Watten, R. H., 1979. Epidemic Rift Valley fever in Egypt: observations of the spectrum of human illness. Transactions of the Royal Society of Tropical Medicine and Hygiene, 73, 630–633.

    PubMed  CAS  Google Scholar 

  • Lernout, T., Cardinale, E., Jego, M., Desprès, P., Collet, L., Zumbo, B., Tillard, E., Girard, S., and Filleul, L., 2013. Rift Valley fever in humans and animals in Mayotte, an endemic situation? PLos One, 8: e74192.

    PubMed  PubMed Central  CAS  Google Scholar 

  • Linthicum, K. J., Bailey, C. L., Davies, F. G., and Tucker, C. J., 1987. Detection of Rift Valley fever viral activity in Kenya by satellite remote sensing imagery. Science 80, 235, 1656–1659.

    Google Scholar 

  • Linthicum, K. J., Britch, S. C. and Anyamba, A., 2016. Rift Valley fever: an emerging mosquito-borne disease. Annual Review of Entomology, 61, 395–415.

    PubMed  CAS  Google Scholar 

  • Madani, T. A., Al-Mazrou, Y. Y., Al-Jeffri, M. H., Mishkhas, A. A., Al-Rabeah, A. M., Turkistani, A. M., Al-Sayed, M. O., Abodahish, A. A., Khan, A. S., Ksiazek, T. G., and Shobokshi, O., 2003. Rift Valley fever epidemic in Saudi Arabia: epidemiological, clinical, and laboratory characteristics. Clinical Infectious Diseases, 37, 1084–1092.

    PubMed  Google Scholar 

  • Matilla, F., Velleman, Y., Harrison, W., and Nevel, M., 2018. Animal influence on water, sanitation and hygiene measures for zoonosis control at the household level: a systematic literature review. PLoS Neglected Tropical Diseases, 12, e0006619.

    PubMed  PubMed Central  Google Scholar 

  • Mroz, C., Gwida, M., El-Ashker, M., El-Diasty, M., El-Beskawy, M., Ziegler, U., Eiden, M., and Groschup, M. H., 2017. Seroprevalence of Rift Valley fever virus in livestock during inter-epidemic period in Egypt, 2014/15. BMC Veterinary Research, 13, 87.

    PubMed  PubMed Central  Google Scholar 

  • Mulumba-Mfumu, L. K., Pongombo, B. P., Mande, J. M., Poweska, J. C., and Steyl, J. C. A., 2009. Rift Valley fever in Central Africa: serological evidence and virus antigen detection in cattle in the Democratic Republic of Congo. Proceedings of the FAO/IAEA International Symposium on Sustainable Improvement of Animal Production and Health, Vienna, Austria, p. p. 400.

  • Munyua, P., Murithi, R. M., Wainwright, S., Githinji, J., Hightower, A., Mutonga, D., Macharia, J., Ithondeka, P. M., Musaa, J., Breiman, R. F., Bloland, P., and Kariuki Njenga, M., 2010. Rift Valley fever outbreak in livestock in Kenya, 2006–2007. American Journal of Tropical Medicine and Hygiene, 83, 58–64.

    PubMed  Google Scholar 

  • Nderitu, L., Lee, J. S., Omolo, J., Omulo, S., O’Guinn, M. L., Hightower, A., Mosha, F., Mohamed, M., Munyua, P., Nganga, Z., Hiett, K., Seal, B., Feikin, D. R., Breiman, R. F., and Njenga, M. K., 2011. Sequential Rift Valley fever outbreaks in Eastern Africa caused by multiple lineages of the virus. Journal of Infectious Diseases, 203, 655–665.

    PubMed  Google Scholar 

  • Njenga, M. K. and Bett, B., 2018. Rift Valley fever virus—how and where virus is maintained during inter-epidemic periods. Current Clinical Microbiology Reports, pp. 1–7.

  • Olaleye, O., Tomori, O., and Schmitz, H., 1996. Rift Valley fever in Nigeria: infections in domestic animals. Revue Scientifique et Technique, 15, 937–946.

    PubMed  CAS  Google Scholar 

  • Onono, J. O., Wieland, B., and Rushton, J., 2013. Constraints to cattle production in a semiarid pastoral system in Kenya. Tropical Animal Health and Production, 45, 1415–1422.

    PubMed  Google Scholar 

  • Ould El Mamy, A. B., Baba, M. O., Barry, Y., Isselmou, K., Dia, M. L., Hampate, B., Diallo, M. Y., El Kory, M. O. B., Diop, M., Lo, M. M., Thiongane, Y., Bengoumi, M., Puech, L., Plee, L., Claes, F., de la Rocque, S., and Doumbia, B., 2011. Unexpected Rift Valley fever outbreak, Northern Mauritania. Emerging Infectious Diseases, 17, p.1984.

  • Rich, K. M., and Perry, B. D., 2011. The economic and poverty impacts of animal diseases in developing countries: new roles, new demands for economics and epidemiology. Preventive Veterinary Medicine, 101, 133–147.

    PubMed  Google Scholar 

  • Saasa, N., Kajihara, M., Dautu, G., Mori-Kajihara, A., Fukushi, S., Sinkala, Y., Morikawa, S., Mweene, A., Takada, A., Yoshimatsu, K., and Arikawa, J., 2018. Expression of a recombinant nucleocapsid protein of Rift Valley fever virus in Vero cells as an immunofluorescence antigen and its use for serosurveillance in traditional cattle herds in Zambia. Vector-Borne and Zoonotic Diseases, 18, 273–277.

    PubMed  Google Scholar 

  • Shope, R. E., Peters, C. J., and Davies, F. G., 1982. The spread of Rift Valley fever and approaches to its control. Bulletin of the World Health Organization, 60, 299–304.

    PubMed  PubMed Central  CAS  Google Scholar 

  • Soumare, B., Tempia, S., Cagnolati, V., Mohamoud, A., Van Huylenbroeck, G., and Berkvens, D., 2007. Screening for Rift Valley fever infection in northern Somalia: a GIS based survey method to overcome the lack of sampling frame. Veterinary Microbiology, 121, 249–256.

    PubMed  Google Scholar 

  • Struthers, J. K., Swanepoel, R., and Shepherd, S. P., 1984. Protein synthesis in Rift Valley fever virus-infected cells. Virology, 134, 118–124.

    PubMed  CAS  Google Scholar 

  • Sumaye, R. D., Geubbels, E., Mbeyela, E., and Berkvens, D., 2013. Inter-epidemic transmission of Rift Valley fever in livestock in the Kilombero River Valley, Tanzania: a cross-sectional survey. PLoS Neglected Tropical Diseases, 7: e2356.

    PubMed  PubMed Central  Google Scholar 

  • Sumaye, R., Jansen, F., Berkvens, D., Baets, B. De, Geubels, E., Thiry, E. and Id, M. K., 2019. Rift Valley fever: an open-source transmission dynamics simulation model. PLoS One, 14, e0209929.

    PubMed  PubMed Central  CAS  Google Scholar 

  • Tshilenge, G. M., Dundon, W. G., De Nardi, M., Mfumu, L. K. M., Rweyemamu, M., Kayembe-Ntumba, J.-M., and Masumu, J., 2019. Seroprevalence of Rift Valley fever virus in cattle in the Democratic Republic of the Congo. Tropical Animal Health and Production, 51, 537–543.

    PubMed  Google Scholar 

  • Umuhoza, T., Berkvens, D., Gafarasi, I., Rukelibuga, J., Mushonga, B., and Biryomumaisho, S., 2017. Seroprevalence of Rift Valley fever in cattle along the Akagera–Nyabarongo rivers, Rwanda. Journal of the South African Veterinary Association, 88, 1–5.

    Google Scholar 

  • Van Yelden, D. J. J., Meyer, J. D., Olivier, J., Gear, J. H. S., and McIntosh, B., 1977. Rift Valley fever affecting humans in South Africa. A clinico-pathological study. South African Medical Journal, 51, 867–871.

    Google Scholar 

  • Woodring, J. L., Higgs, S., and Beaty, B. J., 1996. Natural cycles of vector borne pathogens. In Biology of Disease Vectors, p. 632.

    Google Scholar 

  • World Health Organization, 2003. Disease outbreak reported: Rift Valley fever in Egypt. Weekly Epidemiological Record, 36(5).

  • World Health Organization, 2007a. Outbreak News: Rift Valley fever, Sudan. Weekly Epidemiological Record, 82, 401–402.

    Google Scholar 

  • World Health Organization, 2007b. Outbreaks of Rift Valley fever in Kenya, Somalia and United Republic of Tanzania, December 2006–April 2007. Weekly Epidemiological Record, 82, 169–178.

    Google Scholar 

  • Xu, F., Liu, D., Nunes, M. R. T., Travassos Da Rosa, A. P. A., Tesh, R. B., and Xiao, S. Y., 2007. Antigenic and genetic relationships among Rift Valley fever virus and other selected members of the genus Phlebovirus (Bunyaviridae). American Journal of Tropical Medicine and Hygiene, 76, 1194–1200.

    PubMed  CAS  Google Scholar 

Download references

Acknowledgments

We would like to thank the Ministry of Agriculture Breeding and Fisheries of the Democratic Republic of Congo for their support in carrying out this study. We are also grateful to officials of the Provincial Ministry of Agriculture, Fisheries and Livestock and to cattle farmers in Kwilu Province for their support.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Abdel-Amir Dib Halawi.

Ethics declarations

This study was approved by the Ministry of Agriculture, Fisheries and Livestock, Local Politico-Administrative Authorities. Consent for blood sample collection using conventional methods from cattle herds was obtained from owners.

Conflict of interest

The authors declare that they have no conflict of interest.

Additional information

Publisher’s note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Halawi, AA.D., Saasa, N., Pongombo, B.L. et al. Seroprevalence of Rift Valley fever in cattle of smallholder farmers in Kwilu Province in the Democratic Republic of Congo. Trop Anim Health Prod 51, 2619–2627 (2019). https://doi.org/10.1007/s11250-019-01978-z

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11250-019-01978-z

Keywords

Navigation