Abstract
A cross-sectional study was conducted to determine the seroprevalence and the risk factors associated with C. burnetii infection in cattle in the state of Setif in northeastern Algeria from March 2016 to April 2018. A total of 678 cows animals aged at least 24 months and belonging to 90 herds were randomly selected. A serum sample from each cow was tested for antibodies against C. burnetii using an indirect enzyme-linked immunosorbent assay (ELISA). A structured questionnaire focusing on risk factors for C. burnetii infection was administered to farm owners involved in the study. The individual animal prevalence was 11.36% (77/678) (95%CI 8.97–13.75%), the herd prevalence was 45.56% (41/90) (95%CI 35.27–55.84%), and the within-herd prevalence ranged from 9.09 to 57.14% (mean 23.71%; Q1 11.11%, Q2 or median 20%, Q3 30%). Multivariable logistic regression analysis revealed that contact with other herds (odds ratio (OR) 1.95, 95 CI 1.12–3.42) and purchased animals (OR 2.05, 95 CI 1.14–3.68) was identified as risk factors for seropositivity to C. burnetii, while the use of disinfectants (OR 0.32, 95 CI 0.14–0.72) was identified as protective factor. The results from the present study indicate that C. burnetii is circulating into cattle herds in the region of Setif in Northeastern of Algeria. It is recommended to implement good hygienic practices and measures of biosecurity to reduce the spread of infection between cattle herds and possible exposure of humans.
Similar content being viewed by others
References
Abdelhadi, F.Z., Abdelhadi, S.A., Niar, A., Benallou, B., Meliani, S., Smail, N.L., Mahmoud, D., 2015. Abortions in Cattle on the Level of Tiaret Area ( Algeria ). Global Veterinaria, 14, 638–645.
Adamu, S.G., Kabir, J., Umoh, J.U., Raji, M.A., 2018. Seroprevalence of brucellosis and Q fever (Coxiellosis) in cattle herds in Maigana and Birnin Gwari agro-ecological zone of Kaduna State, Nigeria. Tropical Animal Health and Production, 50, 1583–1589.
Agag, S., Kaidi, R., Khelef, D., 2017. Séroprévalence de la fièvre Q chez les bovins de la région de Bejaïa (Algérie). Revue d’élevage et de médecine vétérinaire des pays tropicaux, 69, 155–159.
Agerholm, J.S., 2013. Coxiella burnetii associated reproductive disorders in domestic animals-a critical review. Acta Veterinaria Scandinavica, 55, 13.
Alvarez, J., Perez, A., Mardones, F.O., Pérez-Sancho, M., García-Seco, T., Pagés, E., Mirat, F., Díaz, R., Carpintero, J., Domínguez, L., 2012. Epidemiological factors associated with the exposure of cattle to Coxiella burnetii in the Madrid region of Spain. Veterinary Journal, 194, 102–107.
Angelakis, E., Raoult, D., 2010. Q fever. Veterinary Microbiology, 140, 297–309.
Astobiza, I., Barandika, J. F., Ruiz-Fons, F., Hurtado, A., Povedano, I., Juste, R. A., & García-Pérez, A. L. 2011. Coxiella burnetii shedding and environmental contamination at lambing in two highly naturally-infected dairy sheep flocks after vaccination. Research in veterinary science, 91, e58-e63.
Bielawska-Drózd, A., Cieślik, P., Mirski, T., Bartoszcze, M., Knap, J.P., Gaweł, J., Zakowska, D., 2013. Q fever - selected issues. Annals of Agricultural and Environmental Medicine, 20, 222–232.
Biswas, S., Bandyopadhyay, S., Dimri, U., H. Patra, P., 2013. Bovine herpesvirus-1 (BHV-1) - a re-emerging concern in livestock: a revisit to its biology, epidemiology, diagnosis, and prophylaxis. Veterinary Quarterly, 33, 68–81.
Cantas, H., Muwonge, A., Sareyyupoglu, B., Yardimci, H., Skjerve, E., 2011. Q fever abortions in ruminants and associated on-farm risk factors in northern Cyprus. BMC Veterinary Research, 7, 13.
Capuano, F., Landolfi, M.C., Monetti, D.M., 2001. Influence of three types of farm management on the seroprevalence of Q fever as assessed by an indirect immunofluorescence assay. Veterinary Record, 149, 669–671.
Carbonero, A., Guzmán, L.T., Montaño, K., Torralbo, A., Arenas-Montes, A., Saa, L.R., 2015. Coxiella burnetii seroprevalence and associated risk factors in dairy and mixed cattle farms from Ecuador. Preventive Veterinary Medecine, 118, 427–435.
Ceylan, E., Berktas, M., Keles, I., Agaoglu, Z., 2009. Seroprevalence of Q Fever in Cattle and Sheep in the East of Turkey. Asian Journal of Animal and Veterinary Advances (AJAVA), 4, 114–121.
Dabaja, M.F., Greco, G., Villari, S., Vesco, G., Bayan, A., Bazzal, B. El, Ibrahim, E., Gargano, V., Sciacca, C., Lelli, R., Ezzedine, M., Mortada, H., Tempesta, M., Mortada, M., 2019. Occurrence and risk factors of Coxiella burnetii in domestic ruminants in Lebanon. Comparative Immunology, Microbiology and Infectious Diseases, 64, 109–116
Dohoo, I.R., Ducroc, C., Fourichon, C., Donald, A., Hurnik, D., 1996. An overview of techniques for dealing with large numbers of independent variables in epidemiologic studies. Preventive Veterinary Medecine, 29, 221–239
Dechicha, A., Gharbi, S., Kebbal, S., Chatagnon, G., Tainturier, D., Ouzrout, R., Guetarni, D., 2010. Serological survey of etiological agents associated with abortion in two Algerian dairy cattle breeding farms. Journal of Veterinary Medecine and Animal Health, 2, 001–005.
Derdour, S.-Y., Hafsi, F., Azzag, N., Tennah, S., Laamari, A., China, B., Ghalmi, F., 2017. Prevalence of the main infectious causes of abortion in dairy cattle in Algeria. Journal of Veterinary Research. 61,337–343.
EFSA, Panel on Animal Health and Welfare (AHAW), 2010. Scientific Opinion on Q fever., EFSA Journal, 8, 1–114. http://www.efsa.europa.eu/en/efsajournal/pub/1595. (Accessed 15 sep 2018)
Elandalousi, R.B., Ghram, A., Maaroufi, A., Mnif, W., 2015. Séroprévalence des maladies abortives zoonotiques chez les ruminants au nord de la Tunisie. Research fr, 2, 1419.
Guatteo, R., Beaudeau, F., Berri, M., Rodolakis, A., Joly, A., Seegers, H., 2006. Shedding routes of Coxiella burnetii in dairy cows: implications for detection and control. Veterinary Research, 37, 827–833.
Guatteo, R., Beaudeau, F., Joly, A., Seegers, H., 2007. Coxiella burnetii shedding by dairy cows. Veterinary Research, 38, 849–860.
Guatteo, R., Seegers, H., Taurel, A.F., Joly, A., Beaudeau, F., 2011. Prevalence of Coxiella burnetii infection in domestic ruminants: A critical review. Veterinary Microbiology, 149, 1–16.
Gürtler. L., Bauerfeind, U., Blümel, J., Burger, R., Drosten, C., Gröner, A., Heiden M, Hildebrandt M., Jansen B., Offergeld R., Pauli G., Seitz R., Schlenkrich U., Schottstedt V., Strobel, J., Willkommen, H., 2014. Coxiella burnetii - Pathogenic Agent of Q (Query) Fever. transfusion medicine hemotherapy, 41,60–72
Hosmer, D.W., Lemeshow, S., 2000. Applied logistic regression, (John Wiley & Sons, New York) 375.
Hussien, M.O., Enan, K.A., Alfaki, S.H., Gafar, R.A., Taha, K.M., Rahim, A., El, M., 2017. Seroprevalence of Coxiella burnetii in Dairy Cattle and Camel in Sudan. International Journal of Infection, 4, e42945.
Kamga-Waladjo, A.R., Gbati, O.B., Kone, P., Lapo, R.A., Chatagnon, G., Bakou, S.N., Pangui, L.J., Diop, P.E.H., Akakpo, J.A., Tainturier, D., 2010. Seroprevalence of Neospora caninum antibodies and its consequences for reproductive parameters in dairy cows from Dakar-Senegal, West Africa. Tropical Animal Health and Production, 42, 953–959.
Kersh, G.J., Fitzpatrick, K.A., Self, J.S., Priestley, R.A., Kelly, A.J., Ryan Lash, R., Marsden-Haug, N., Nett, R.J., Bjork, A., Massung, R.F., Andersona, A.D., 2013. Presence and Persistence of Coxiella burnetii in the environments of goat farms associated with a Q fever outbreak. Applied and Environmental Microbiology, 79, 1697–1703
Kirkan, Ş., Kaya, O., Tekbiyik, S., Parin, U., 2008. Detection of Coxiella burnetii in cattle by PCR. Turkish Journal of Veterinary and Animal Science, 32, 215–220.
Klemmer, J., Njeru, J., Emam, A., El-Sayed, A., Moawad, A.A., Henning, K., Elbeskawy, M.A., Sauter-Louis, C., Straubinger, R.K., Neubauer, H., El-Diasty, M.M., 2018. Q fever in Egypt: Epidemiological survey of Coxiella burnetii specific antibodies in cattle, buffaloes, sheep, goats and camels. PLoS One. 13, e0192188.
Lacheheb, A., Raoult, D., 2009. Seroprevalence of Q- fever in Algeria. Clinical Microbiology and Infection, 15, 167–168
Lanyon, S.R., Hill, F.I., Reichel, M.P., Brownlie, J., 2014. Bovine viral diarrhoea: Pathogenesis and diagnosis. Veterinary Journal, 199, 201–209.
Molina, V., Risalde, M.A., Sánchez-Cordón, P.J., Pedrera, M., Romero-Palomo, F., Luzzago, C., Gómez-Villamandos, J.C., 2013. Effect of infection with BHV-1 on peripheral blood leukocytes and lymphocyte subpopulations in calves with subclinical BVD. Research in Veterinary Science, 95, 115–122.
Muskens, J., Van Engelen, E., Van Maanen, C., Bartels, C., Lam, T.J.G.M., 2011. Paper: Prevalence of Coxiella burnetii infection in Dutch dairy herds based on testing bulk tank milk and individual samples by PCR and ELISA. Veterinary Record, 168, 79.
Nusinovici, S., Hoch, T., Brahim, M.L., Joly, A., Beaudeau, F., 2015. The Effect of Wind on Coxiella burnetii Transmission Between Cattle Herds: a Mechanistic Approach. transboundary and emerging diseases, 64, 585–592.
Obaidat, M.M., Kersh, G.J., 2017. Prevalence and Risk Factors of Coxiella burnetii Antibodies in Bulk Milk from Cattle, Sheep, and Goats in Jordan. Journal of Food Protection, 80, 561–566.
World Organization for Animal Health (OIE), 2018. Chapter 2.1.16. Q fever. in Manual of Diagnostic Tests and Vaccines for Terrestrial Animals. OIE, Paris. http://www.oie.int/fileadmin/Home/fr/Health_standards/tahm/2.01.16_Q_FEVER .pdf Accessed 18 September 2018.
Parker, N.R., Barralet, J.H., Bell, A.M., 2006. Seminar Q fever. Lancet, 367, 679–88.
Paul, S., Agger, J. F., Markussen, B., Christoffersen, A. B., Agerholm, J. S., 2012. Factors associated with Coxiella burnetii antibody positivity in Danish dairy cows. Preventive Veterinary Medecine.107, 57–64.
Pexara, A., Solomakos, N., Govaris, A., 2018. Q fever and prevalence of Coxiella burnetii in milk. Trends in Food Science and Technology, 71, 65–72.
Plummer, P.J., McClure, J.T., Menzies, P., Morley, P.S., Van den Brom, R., Van Metre, D.C., 2018. Management of Coxiella burnetii infection in livestock populations and the associated zoonotic risk: A consensus statement. Journal of Veterinary Internal Medicine, 32, 1481–1494.
Porter, S.R., Czaplicki, G., Mainil, J., Guattéo, R., Saegerman, C., 2011. Q fever: Current state of knowledge and perspectives of research of a neglected zoonosis. International Journal of Microbiology, 2011.
Potgieter, L.N., 1995. Immunology of bovine viral diarrhea virus. The Veterinary clinics of North America. Food animal practice, 11, 501–520.
Roest, H.I.J., Tilburg, J.J.H.C., Van Der Hoek, W., Vellema, P., Van Zijderveld, F.G., Klaassen, C.H.W., Raoult, D., 2011. The Q fever epidemic in the Netherlands: History, onset, response and reflection. Epidemiology and Infection, 139, 1–12.
Rousset, E., Berri, M., Durand, B., Dufour, P., Prigent, M., Delcroix, T., Touratier, A., Rodolakis, A., 2009. Coxiella burnetii shedding routes and antibody response after outbreaks of Q fever-induced abortion in dairy goat herds. Applied and Environmental Microbiology, 75, 428–433.
Schelling, E., Diguimbaye, C., Daoud, S., Nicolet, J., Boerlin, P., Tanner, M., Zinsstag, J., 2003. Brucellosis and Q-fever seroprevalences of nomadic pastoralists and their livestock in Chad. Preventive Veterinary Medecine, 61, 279–293.
Scolamacchia, F., Handel, I.G., Fèvre, E.M., Morgan, K.L., Tanya, V.N., Bronsvoort, B.M.D.C., 2010. Serological patterns of brucellosis, leptospirosis and Q fever in Bos indicus cattle in Cameroon. PLoS One, 5, e8623.
Seo, M. G., Ouh, I. O., Lee, S. H., Kim, J. W., Rhee, M. H., Kwon, O. D., , Kim, T.H., Kwak, D., 2017. Prevalence of Coxiella burnetii in cattle at South Korean national breeding stock farms. PloS one, 12, e0177478.
Srikumaran, S., Kelling, C.L., Ambagala, A., 2007. Immune evasion by pathogens of bovine respiratory disease complex. Animal Health Research Reviews, 8, 215–229.
Thrusfield, M. 2007. Veterinary Epidemiology, 3rd edn., Blackwell Science Ltd, Oxford, UK. pp. 230–238.
Tukur, H.B., Ajogi, I., Kabir, J., Umoh, J.U., 2014. Seroprevalence of Coxiella Burnetti in Cattle and Its Risk Factors in Kaduna Metropolis , Kaduna State, Nigeria. IOSR Journal of Agriculture and Veterinary Science (IOSR-JAVS), 7, 1–5.
Van Engelen, E., Schotten, N., Schimmer, B., Hautvast, J. L. A., Van Schaik, G., van Duijnhoven, Y. T. H. P., 2014. Prevalence and risk factors for Coxiella burnetii (Q fever) in Dutch dairy cattle herds based on bulk tank milk testing. Preventive Veterinary Medecine, 117, 103–109.
Vanderburg, S., Rubach, M.P., Halliday, J.E.B., Cleaveland, S., Reddy, E.A., Crump, J.A., 2014. Epidemiology of Coxiella burnetii Infection in Africa: A OneHealth Systematic Review. PLOS Neglected Tropical Diseases, 8, e2787.
Villari, S., Galluzzo, P., Arnone, M., Alfano, M., Geraci, F., Chiarenza, G., 2018. Seroprevalence of Coxiella burnetii infection (Q fever) in sheep farms located in Sicily (Southern Italy) and related risk factors. small ruminant research, 164, 82–86.
Wardrop, N.A., Thomas, L.F., Cook, E.A.J., de Glanville, W.A., Atkinson, P.M., Wamae, C.N., Fèvre, E.M., 2016. The Sero-epidemiology of Coxiella burnetii in Humans and Cattle, Western Kenya: Evidence from a Cross-Sectional Study. PLOS Neglected Tropical Diseases, 10, e0005032.
Wielders, C.C.H., Wuister, A.M.H., de Visser, V.L., de Jager-Leclercq, M.G., Groot, C.A.R., Dijkstra, F., van Gageldonk-Lafeber, A.B., van Leuken, J.P.G., Wever, P.C., van der Hoek, W., 2014. Characteristics of hospitalized acute Q fever patients during a large epidemic, The Netherlands. PLoS One, 9, e91764.
Acknowledgments
We are very grateful to the Zoonosis Laboratory of Istituto Zooprofilattico Sperimentale della Sardegna for funding all the laboratory analyses, and the staff for scientific and technical support. Also, we acknowledge the farmers for their willingness to participate and to provide information about their farms and animals.
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Ethical statement
All animal owners declared their oral consent before the collection of the blood samples as well to the related survey questions. The cattle were sampled by a qualified veterinarian following all applicable guidelines for the care and use of animal.
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
About this article
Cite this article
Menadi, S.E., Mura, A., Santucciu, C. et al. Seroprevalence and risk factors of Coxiella burnetii infection in cattle in northeast Algeria. Trop Anim Health Prod 52, 935–942 (2020). https://doi.org/10.1007/s11250-019-02083-x
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11250-019-02083-x