veterinary sciences Article Seroprevalence and Risk Factors Associated with Brucella Infection in Camels in the Puntland State of Somalia Ahmed Said Mohamud 1,2,* , John Pilate Kothowa 3, Ruth Lindizyani Mfune 1,4 , Melai Mubanga 5, Jacques Godfroid 6 and John B. Muma 1 1 Department of Disease Control, School of Veterinary Medicine, The University of Zambia, Lusaka P.O. Box 32379, Zambia; [email protected] (R.L.M.); [email protected] (J.B.M.) 2 Faculty of Veterinary Medicine, Red Sea University, Galkayo RC2F+WC, Somalia 3 Department of Animal Health and Livestock Development, BLADD, Mpemba P.O. Box 34, Malawi; [email protected] 4 Department of Public Health, Michael Chilufya Sata School of Medicine, The Copperbelt University, Ndola P.O. Box 71769, Zambia 5 Department of Environmental Health, School of Medicine and Health Sciences, Eden University, Lusaka P.O. Box 37727, Zambia; [email protected] 6 Department of Arctic and Marine Biology, UiT—The Arctic University of Norway, 9037 Tromsø, Norway; [email protected] * Correspondence: [email protected]; Tel.: +252-907-772737 Abstract: Brucellosis is an important zoonotic disease caused by members of the genus Brucella. Camel brucellosis has been reported in almost all camel-rearing countries in Africa and Asia. A cross- sectional study was conducted between February 2020 and February 2021 in Galkayo, Garowe, and Bosaso districts in the Puntland State of Somalia to investigate the seroprevalence and risk factors of brucellosis in camels. A competitive enzyme-linked immunosorbent assay (c-ELISA) was used to Citation: Mohamud, A.S.; Kothowa, detect anti-Brucella antibodies, while a structured questionnaire was used to collect epidemiological J.P.; Mfune, R.L.; Mubanga, M.; data. A total of 441 camel sera were screened against Brucella antibodies. Thirty-one (7%; 95% CI: Godfroid, J.; Muma, J.B. 4.8–9.8%) samples were positive, and thirteen (54.2%; 95% CI: 32.8–74.4%) out of the twenty-four Seroprevalence and Risk Factors farms sampled had at least one seropositive animal. Galkayo district had the highest number of Associated with Brucella Infection in Camels in the Puntland State of Brucella-seropositive camels (10.3%), followed by Bosaso district (8.6%), while Garowe district had Somalia. Vet. Sci. 2021, 8, 137. the lowest number of seropositive camels (1.4%). The binary logistic regression model revealed that https://doi.org/10.3390/vetsci8070137 camels in Galkayo district (p = 0.015; OR: 9.428; 95% CI: 1.539–57.755), camels from large herd sizes of >50 animals (p = 0.019; OR: 5.822; 95% CI: 1.336–25.371), and those in contact with small ruminants Academic Editor: Devendra H. Shah (p = 0.011; OR: 10.941; 95% CI: 1.728–69.285) were significantly associated with seropositive cases of camel brucellosis in the Puntland State of Somalia. The present study shows that Brucella infections Received: 19 May 2021 in camels are prevalent in the three districts covered by the study. This poses a public health risk, Accepted: 29 June 2021 because milk from these camels is used for human consumption. Studies focusing on the isolation of Published: 19 July 2021 Brucella strains in camels and investigating brucellosis in ruminants and humans are recommended in the study area. Validation of serological tests—including c-ELISA—for Brucella antibody detection Publisher’s Note: MDPI stays neutral in camels is also needed. with regard to jurisdictional claims in published maps and institutional affil- Keywords: Brucella; camels; seroprevalence; Puntland State of Somalia iations. 1. Introduction Copyright: © 2021 by the authors. Camelus dromedarius Licensee MDPI, Basel, Switzerland. Somalia has the world’s largest dromedary camel ( ) population, This article is an open access article with more than seven million [1]. In addition to their social and cultural importance to distributed under the terms and Somali pastoralists, camels play a vital role in food security and national economy in conditions of the Creative Commons the country. Interest in dromedary camel (one-humped camel) rearing has increasingly Attribution (CC BY) license (https:// developed in arid countries, including Somalia, as dromedaries are more drought tolerant creativecommons.org/licenses/by/ than any other domestic animals [2]. Camels are not only kept for milk, but also provide 4.0/). meat, and are used as a means of transportation. As a result of camels being the main Vet. Sci. 2021, 8, 137. https://doi.org/10.3390/vetsci8070137 https://www.mdpi.com/journal/vetsci Vet. Sci. 2021, 8, 137 2 of 8 source of milk in Somalia, intensification of camels for milk production in many parts of the country was started in the last few years. Camels are, however, affected by a number of diseases, including brucellosis. Brucel- losis is an important zoonotic disease caused by members of the genus Brucella. The disease can affect almost all domestic animals, and cross-transmission can occur between cattle, sheep, goats, and camels [2]. Brucella infection in camels is mainly caused by B. abortus and B. melitensis. Camels are not known to be the primary host for Brucella spp., and infection in camels depends on contact with other primary host animals [3]. Clinical disease in camels is very rare; however, infected camels are silent carriers of the Brucella pathogen, and the possible shedding of the organism in the milk may lead to transmission of the pathogen to humans [4–6]. Additionally, this disease imposes restrictions on the livestock trade. Camel brucellosis has been reported in most camel-rearing countries in Africa and Asia [7]. In East Africa, camel brucellosis has been reported in Somalia, Ethiopia, Kenya, Sudan, and Eritrea [2]. However, there are no sufficient data about the real status of the disease in many countries of the world, and research on the epidemiology of camel brucellosis is very scarce [8,9]. Despite the fact that no test has been specifically validated in camels, a number of serological tests—including RBPT, ELISA, and the complement fixation test (CFT)—can be used for the diagnosis of camel brucellosis [10]. There is sufficient evidence indicating that brucellosis is present in sheep and goats [11,12], cattle [13,14], camels [3,15], and humans [16] in Somalia. However, there is currently little information available about the epidemiology of the disease in Somalia, and its occurrence in both livestock and humans is poorly estimated. Few studies have been conducted in south and central Somalia, or in Somaliland (northern Somalia) [3,15]. One study reported 3.9% individual seroprevalence in camels in northern Somalia [3], while 4.4% individual seroprevalence of camel brucellosis was reported in Mogadishu, southern Somalia [15]. However, no information is available on camel brucellosis in the Puntland State of Somalia (northeastern Somalia). According to the Food and Agriculture Organization of the United Nations (2014), livestock exports—especially sheep, goats, cattle, and camels—are the most traded commodity in Somalia. Brucellosis can hinder this huge livestock trade in the country. Furthermore, many Somali people consume raw camel milk without heat treat- ment [15]; thus, Brucella-infected camels can pose health risks to the camel milk consumers in the country. Currently, there is no national control program for brucellosis in Somalia—a situation that might lead to spread of the disease among animals, resulting in huge eco- nomic losses to the livestock industry and negatively impacting public health. Therefore, this study was designed to investigate the seroprevalence and potential risk factors of brucellosis in camels in northeastern Somalia (the Puntland State of Somalia). 2. Materials and Methods This study was conducted in the Puntland State of Somalia, a federal member state in northeastern Somalia. Puntland is bordered by Somaliland to its west, the Gulf of Aden to the north, the Indian Ocean to the east, the central Galmudug region to the south, and Ethiopia to the southwest. Puntland is semi-arid, with an average daily temperature range of 27–37 ◦C. The total area of the state is about 212,510 km2, with a population estimated at 4,334,633 in 2016 [17]. According to the Intergovernmental Authority on Development (IGAD) Centre for Pastoral Areas and Livestock Development (ICPALD), the estimated camel population stands at 1,868,000 in the Puntland State of Somalia as of 2013 [18]. Camels in Puntland State are mainly raised for milk and meat production under a nomadic system using traditional husbandry practices. However, commercialization of dairy camels, and keeping them in a semi-intensive production system, began in the last few years. This cross-sectional study was conducted between February 2020 and February 2021, to determine the seroprevalence and risk factors of brucellosis in camels in the Puntland State of Somalia. Three districts were covered—namely, Bosaso (in the Bari region), Garowe (in the Nugal region) and Galkayo (in the Mudug region). Only commercially kept dairy Vet. Sci. 2021, 8, 137 3 of 8 camels were targeted, and these three districts were purposely selected because they represent the main dairy camel farming areas in the state. The number of animals to be sampled was calculated based on an assumed individual Brucella seroprevalence (unknown seroprevalence) of 50%, within a 95% confidence level and 5% desired precision. Sample size was obtained using the following formula [19]: 1.962 × Pex × (1 − Pex) n = (d)2 where n = sample size, d = desired absolute precision, and Pex= expected prevalence; thus, the desired sample size for Pex = 0.5 was n = 384. To account for non-response, a 10% adjustment was made, bringing the required sample size to 423 camels. However, at the end of the study, 441 camels were sampled. A proportionally representative sample was allocated to each district based on its estimated number of dairy camel farms.