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      The sero-prevalence of brucellosis in cattle and their herders in Bahr el Ghazal region, South Sudan

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          Abstract

          Background

          Brucellosis is a worldwide recognized bacterial zoonotic disease. There is currently no information on bovine brucellosis sero-prevalence in South Sudan regardless of the economic, social and public health impact on populations. Therefore, for the first time in 33 years, we report the sero-prevalence of brucellosis in cattle and their herders. Furthermore, we characterize the drivers associated with the disease at the human-animal interface in Bahr el Ghazal region, South Sudan.

          Methods

          A total of 893 and 87 animal and human sera respectively were examined between December 2015 and May 2016. Rose Bengal Plate Test (RBPT) and Competitive Enzyme Linked Immuno Sorbent Assay (c-ELISA) were used in parallel to detect anti- Brucella antibodies. Questionnaires were administered to collect relevant metadata used for the association analysis in R version 3.2.3. Odds Ratio (OR) and Confidence Intervals (CI) were determined.

          Results

          Overall bovine brucellosis prevalence was 31% (95%CI = 28.0–34.2), with the highest 63% (95%CI = 53–70) and lowest 10% (95%CI = 4.5–20.1) prevalence estimates in Wau and Gogrial states respectively. The bovine sero-prevalence was approximately equally distributed among the male 30.4% (26.9–34.2) and the females 32.5% (26.8–38.7). Poor body condition (OR = 0.22; 95%CI = 0.07–0.54) and larger herd sizes (OR = 0.05; 95%CI = 0.008–0.173) were protective factors for brucellosis, while the opposite was true for the second (OR = 1.70; 95%CI = 1.08–2.67) and third (OR = 2.5; 95%CI = 1.46–4.47) lactation stage. The overall brucellosis sero-prevalence in herders was estimated at 33.3% (23.9–44.3).

          Conclusion

          We report a high prevalence of anti- Brucella antibodies in cattle and their herders in Bahr el Ghazal, indicating an enzootic status in the cattle population being an important source of infection for humans. This represents a genuine public health challenge. Therefore, there is need to raise awareness and build capacity and infrastructure in this fragile state to underwrite future public health strategies for brucellosis.

          Author summary

          Enzootic brucellosis is a bacterial infectious disease, which represents millions of dollars in production losses in livestock, as well as Disability- Adjusted Life Years (DALYS) associated with health and treatment in the human populations for Low and Middle Income Countries (LMICs). Despite these unequivocally known challenges, there has not been any reporting on this disease in livestock and humans in the recent past. The limitations the disease puts on livestock health and production, coupled with the zoonotic form, which is primarily driven by risky food consumption habits, and interaction with livestock in an enzootic setting with uncontrolled animal movement, means that this disease is not only of veterinary public health, but of trans-boundary importance as well.

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          Most cited references36

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          From the discovery of the Malta fever's agent to the discovery of a marine mammal reservoir, brucellosis has continuously been a re-emerging zoonosis.

          Brucellosis is not a sustainable disease in humans. The source of human infection always resides in domestic or wild animal reservoirs. The routes of infection are multiple: food-borne, occupational or recreational, linked to travel and even to bioterrorism. New Brucella strains or species may emerge and existing Brucella species adapt to changing social, cultural, travel and agricultural environment. Brucella melitensis is the most important zoonotic agent, followed by Brucella abortus and Brucella suis. This correlates with the fact that worldwide, the control of bovine brucellosis (due to B. abortus) has been achieved to a greater extent than the control of sheep and goat brucellosis (due to B. melitensis), these latter species being the most important domestic animals in many developing countries. The long duration and high cost of treatment of human brucellosis reduces the efficacy of the therapy. There is no human vaccine for brucellosis and the occurrence of brucellosis is directly linked to the status of animal brucellosis in a region. In this context, the Word Health Organization has defined the development of a human vaccine, besides the implementation of control and eradication programs in animals, as a high priority. The pathogenicity for humans of B. suis biovars 1, 3 and 4 is well established, whereas B. suis biovar 2 seems to be less pathogenic. Indeed, although hunters and pig farmers have repeatably experienced infectious contact with B. suis biovar 2 (found in wild boar and outdoor-rearing pigs in Europe), isolation of B. suis biovar 2 from human samples have only been seldom reported. Marine mammal brucellosis, due to two new proposed Brucella species i.e. B. cetaceae and B. pinnipediae, represents a new zoonotic threat but the pathogenicity for humans of the different Brucella species found in cetaceans and pinnipeds still has to be clearly established.
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            Brucellosis in sub-Saharan Africa: epidemiology, control and impact.

            Brucellosis is an important disease among livestock and people in sub-Saharan Africa. In general, the incidence is the highest in pastoral production systems and decreases as herd size and size of landholding decreases. The prevalence of risk factors for infections are best understood for bovine brucellosis and to a lesser extent for ovine and caprine brucellosis. The occurrence and epidemiology of brucellosis in pigs is poorly understood. This species bias is also reflected in control activities. As with other public-sector animal health services, the surveillance and control of brucellosis in sub-Saharan Africa is rarely implemented outside southern Africa. Brucellosis is even more ignored in humans and most cases go undiagnosed and untreated, leading to considerable suffering for those affected. Decision-making to determine the importance of brucellosis control relative to other public concerns and what brucellosis control strategies should be applied is urgently required. A strategy for how brucellosis decision-making might be considered and applied in future is outlined. Copyright 2002 Elsevier Science B.V.
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              Incidence and control of brucellosis in the Near East region.

              In countries of the Near East region, brucellosis was reported in almost all domestic animals, particularly cattle, sheep and goats. Brucellosis in camels has been reported in Saudi Arabia, Kuwait, Oman, Iraq, Iran, Sudan, Egypt, Libya and Somalia. It has been reported even in racing camels in the United Arab Emirates. In Egypt, brucellosis has been reported also in buffaloes, equines and swine. Brucella melitensis biovar 3 is the most commonly isolated species from animals in Egypt, Jordan, Israel, Tunisia and Turkey. B. melitensis biovar 2 was reported in Turkey and Saudi Arabia, and B. melitensis biovar 1 in Libya, Oman and Israel. B. abortus biovar 1 was reported in Egypt, biovar 2 in Iran, biovar 3 in Iran and Turkey, and biovar 6 in Sudan. The countries with the highest incidence of human brucellosis are Saudi Arabia, Iran, Palestinian Authority, Syria, Jordan and Oman. Bahrain is reported to have zero incidence. Most human cases are caused by B. melitensis, particularly biovar 3. However, B. abortus has been responsible for an increasing number of cases in recent years, e.g. in Yemen, where B. abortus was identified in 45 cases and B. melitensis in 7 cases out of 330 cultures performed in 1995. Concerning control of brucellosis in animals, there is a controversy on the choice of policy. In some countries, the test and slaughter policy together with the vaccination of young females is adopted, in others, particularly with regard to sheep and goats; mass vaccination has been recently started. The most commonly used vaccines are B. abortus S19 and B. melitensis Rev.1 vaccines. B. abortus RB51 vaccine is used in some countries on small scale. Vaccination is limited to cattle and small ruminants. Copyright 2002 Elsevier Science B.V.
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                Author and article information

                Contributors
                Role: ConceptualizationRole: Data curationRole: Formal analysisRole: MethodologyRole: Writing – original draftRole: Writing – review & editing
                Role: ConceptualizationRole: Data curationRole: Formal analysisRole: MethodologyRole: SupervisionRole: VisualizationRole: Writing – original draftRole: Writing – review & editing
                Role: Data curationRole: Formal analysisRole: MethodologyRole: Writing – original draftRole: Writing – review & editing
                Role: ConceptualizationRole: MethodologyRole: SupervisionRole: Writing – original draftRole: Writing – review & editing
                Role: ConceptualizationRole: MethodologyRole: SupervisionRole: Writing – review & editing
                Role: ConceptualizationRole: Data curationRole: Formal analysisRole: MethodologyRole: Writing – original draftRole: Writing – review & editing
                Role: ConceptualizationRole: Formal analysisRole: MethodologyRole: Project administrationRole: SupervisionRole: ValidationRole: Writing – original draftRole: Writing – review & editing
                Role: ConceptualizationRole: Funding acquisitionRole: MethodologyRole: Project administrationRole: ResourcesRole: SupervisionRole: Writing – original draftRole: Writing – review & editing
                Role: Editor
                Journal
                PLoS Negl Trop Dis
                PLoS Negl Trop Dis
                plos
                plosntds
                PLoS Neglected Tropical Diseases
                Public Library of Science (San Francisco, CA USA )
                1935-2727
                1935-2735
                20 June 2018
                June 2018
                : 12
                : 6
                : e0006456
                Affiliations
                [1 ] Department of Clinical Studies, Faculty of Veterinary Science, University of Bahr el Ghazal, Wau, South Sudan
                [2 ] Department of Biosecurity, Ecosystems &Veterinary Public Health (BEP), College of Vet. Animal Resources & Biosecurity (COVAB), Makerere University, Kampala, Uganda
                [3 ] Div. Genetics and Genomics, The Roslin Institute, Royal (Dick) School of Veterinary Studies, University of Edinburgh, Easter Bush, Midlothian, United kingdom
                [4 ] Department of Disease Control, School of Veterinary Medicine, University of Zambia, Lusaka Zambia
                [5 ] Department of Arctic and Marine Biology, University of Tromsø, Tromsø, Norway
                Yale University Yale School of Public Health, UNITED STATES
                Author notes

                The authors have declared that no competing interests exist.

                Author information
                http://orcid.org/0000-0002-6982-912X
                Article
                PNTD-D-17-01157
                10.1371/journal.pntd.0006456
                6010255
                29924843
                079cd1f2-0675-4ffa-a343-daf6a826c860
                © 2018 Madut et al

                This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.

                History
                : 21 July 2017
                : 17 April 2018
                Page count
                Figures: 1, Tables: 3, Pages: 14
                Funding
                The authors received no specific funding for this work.
                Categories
                Research Article
                Medicine and Health Sciences
                Infectious Diseases
                Bacterial Diseases
                Brucellosis
                Medicine and Health Sciences
                Tropical Diseases
                Neglected Tropical Diseases
                Brucellosis
                Medicine and Health Sciences
                Infectious Diseases
                Zoonoses
                Brucellosis
                Biology and Life Sciences
                Agriculture
                Livestock
                Biology and Life Sciences
                Veterinary Science
                Veterinary Diseases
                Medicine and Health Sciences
                Public and Occupational Health
                People and places
                Geographical locations
                Africa
                South Sudan
                Biology and Life Sciences
                Organisms
                Eukaryota
                Animals
                Vertebrates
                Amniotes
                Mammals
                Bovines
                Medicine and Health Sciences
                Infectious Diseases
                Zoonoses
                Biology and Life Sciences
                Organisms
                Eukaryota
                Animals
                Vertebrates
                Amniotes
                Mammals
                Bovines
                Cattle
                Biology and Life Sciences
                Organisms
                Eukaryota
                Animals
                Vertebrates
                Amniotes
                Mammals
                Ruminants
                Cattle
                Custom metadata
                All relevant data are within the paper and its Supporting Information files.

                Infectious disease & Microbiology
                Infectious disease & Microbiology

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