One Health approach for conducting an outbreak investigation and research in human and animal populations: a case study of Brucellosis

One Health approach for conducting an outbreak investigation and research in human and animal populations: a case study of Brucellosis

John Baligwamunsi Kaneene^1,&, Samuel Majalijja², Francis Ejobi², James Tumwine³

¹Center for Comparative Epidemiology, Michigan State University, 736 Wilson Road, Room A-109, East Lansing, Michigan, 48824, USA, ²College of Veterinary Medicine, Animal Resources and Biosecurity, Makerere University, PO Box 7062, Kampala, Uganda, ³College of Health Sciences, Makerere University, PO Box 7072, Kampala, Uganda

^&Corresponding author
John Baligwamunsi Kaneene, Center for Comparative Epidemiology, Michigan State University, 736 Wilson Road, Room A-109, East Lansing, Michigan, 48824, USA

Introduction    

Outbreaks of disease (the occurrence of more cases than expected) occur frequently [1]. The decisions regarding whether and how extensively to investigate a potential outbreak depend on a variety of factors, including: the severity of the illness, the number of cases, the source, mode or ease of transmission, and the availability of prevention and control measures [1]. Outbreak investigations are a vital tool in epidemiology, preventive, and clinical medicine. There are three goals for conducting outbreak investigations [1]. The first goal (also referred to as the fundamental goal) is to stop the outbreak as soon as possible; many times without even identifying the specific etiological cause of the disease. The second goal is to generate information for understanding the various inter-related risk factors associated with the outbreak. The third goal is to use the information generated from the outbreak investigation to formulate hypotheses about the transmission dynamics and causality of the disease. Due to the aforementioned goals, disease outbreak investigations have to be properly designed and implemented well in order for the results to be useful in meeting the three goals. The design and implementation of a zoonotic disease outbreak or research is particularly challenging to plan and implement as it often involves several hosts (humans and animals), many government agencies, and several disciplines.

One Health is generally viewed as having four pillars [2]: 1) animal health (including domestic and wildlife), 2) human health, 3) environment/ecosystems, and 4) food and water security. Cross-cutting these four pillars are communication and policy considerations. Outbreak investigations involving zoonotic diseases, therefore, are best conducted using a One Health approach. This approach has several benefits and provides opportunity to generate results that can be used to design intervention strategies and policy actions. A real life example will be used to illustrate benefits of applying a One Health approach in a major zoonotic disease; brucellosis in Uganda [3-5]. An apparent increase in the number of human cases of brucellosis was reported in two health centers within two districts of Uganda. At the same time, reports of increased abortions in cattle were reported in the same districts. Brucellosis is a zoonotic disease that affects humans and many animal species. While there are more than eight species of Brucella, five species of brucellosis (B. abortus, B. Melitensis, B. suis, B. ovis, and B. Canis) cause abortions, arthritis, and orchitis in animals. In humans the disease, causes undulating fever, neurological disease, endocarditis, and arthritis, commonly misdiagnosed as malaria in developing countries. Thus, brucellosis is both a public health and economic concern in many countries of the world. Several authors have published on the importance of one health [6-10]; however, there is limited published data documenting the economic benefits in specific disease settings. The objectives of this paper, therefore, are to illustrate the: 1) critical steps in conducting outbreak investigations using a One Health approach, and 2) the economic benefits of a One Health approach.

Methods     

Brucellosis being a zoonotic disease that had been reported in other areas of Uganda [3, 4 ], it was decided to conduct a One Health - based outbreak investigation to get to the route of the problem using the following phases below.

Planning

Professionals from Makerere University, College of Veterinary Medicine, Animal resources, and Biosecurity, and the School of Public Health (COVAB), and from the Government of Uganda (Ministry of Agriculture, Animal Industry, Fisheries and Wildlife, and the Ministry of Health) were assembled to plan how the outbreak investigation should be carried out. From the aforementioned institutions and governmental agencies, an interdisciplinary team was formed. The team consisted of epidemiologists, microbiologists, veterinary pathologists, wildlife ecologists, physicians, veterinarians, laboratory technologists, and media specialists. A communication strategy was determined ahead of time, and a single person was to be in charge of communication within the outbreak investigation team. Communication to the media was to be jointly done by animal health and public health authorities, protocols for sample collection, preservation, transporting, and processing were jointly developed (Figure 1, Figure 2, Figure 3 and Figure 4). Two short questionnaires were developed for collection of data during the investigation. The first questionnaire was used to collect data from humans relating to potential risk factors for acquiring brucellosis. Data describing each human included: age, gender, history of fever, consumption of raw milk, contact with livestock, with animals giving birth, contact with slaughtered animals, wildlife, family history of symptoms consistent with brucellosis, consumption of raw dairy products, sources of water, water treatment, and sharing of water with livestock. Individual identification of participants were deleted in the record. The second questionnaire was used to collect data relating to animal health and management risk factors for brucellosis. Data describing each animal included: a unique animal identification number, breed (local, exotic and mixed), gender, age, date of most recent calving or kidding, and abortion history (yes or no). Consent forms were administered to individuals prior to data and specimen collection.

Training

Prior to starting the investigation, a short training session was held. The training lasted three days. The first day covered the principles of outbreak investigation and ethical conduct of research, the second covered the type of questionnaires and different ways of administering them. The two questionnaires (one for human subjects and the other for livestock) that were going to be used were discussed, and because they were going to be administered in person, professional and cultural sensitivities were discussed in detail. The third day was devoted to how to assemble a team and preparation of the supplies needed. The individuals who were going to collect blood from humans were nurses and laboratory technologists familiar with blood collection. Individuals who were going to collect blood and milk from cattle and goats were veterinarians and veterinary technicians familiar with collection of the samples.

Implementation

Livestock farms that reported abortions were identified and the Outbreak Investigation Team (OIT) visited them together and administered two short questionnaires. Prior to administering the questionnaires and any specimen collection, subjects were asked to sign consent forms. Similarly, farmers signed consent forms prior to the collection of samples from their animals and collection of data about their animals. The first questionnaire (human) was administered to the persons on the farm who came in contact with animals. The second questionnaire (animal) was administered to one person who was in charge of the livestock. From the available livestock (cattle and goats), blood and milk (where appropriate) were collected and blood was collected from the humans on the farm. The collected specimens were taken to a single regional laboratory for testing. The Rose Bengal Plate Test (RBPT) with B. abortus and B. melitensis and the Milk Ring Test were used to test for evidence of Brucella exposure in cattle and goats. The Brucella Micro agglutination Test (BMAT) and the Lateral Flow Assay (LFA) for IgG and igM were used on samples from humans.

Data analysis - Due to the few positive results for the outbreak investigation portion, statistical analysis was not conducted. The research portion had a much larger sample and positive results, so rigorous statistical analysis was conducted and has been published elsewhere [5].

Results     

The work was conducted during June, 2014 and covered two districts in western Uganda (Kiruhura and Bushenyi). A total of 15 farms were involved in the outbreak investigation (all farms had both cattle & goats) with a total of 168 cattle, 131 goats, and 136 human samples were tested. The outbreak investigation showed evidence of brucellosis in humans, cattle, goats, and milk. The seroprevalence was 10% for cattle, 12% for goats, and 8% for humans from the outbreak investigation and 14% in cattle, 17%, in goats, and 11% in humans from the research study. Information from the outbreak investigation was used to design and conduct a detailed research study, whose results have been published [5]. Some of the major outcomes of the investigation include: 1) the development of protocols for specimen collection, shipment, and laboratory testing, 2) training programs for disease investigation using a One Health approach, 3) development of outreach programs for farmers about the disease transmission between animals and from animals to humans, and 4) joint communication of results to the public by representatives of the Ministry of Health and Ministry of Agriculture, Animal Industry, Fisheries and Wildlife.

In this outbreak, the costs of conducting the investigation at the Animal Health Department and those by the Public Health Department were estimated to be $6,885 and $8,343, respectively, for a combined total of $15,228. These costs involved personnel time, field supplies, laboratory supplies, travel costs, and other miscellaneous costs. In contrast, by conducting the outbreak investigation using a One Health approach where both the Public Health and Animal Health Departments and related disciplines planned the investigations together, visited the farms together, shared supplies, laboratory facilities, and personnel, the total cost was estimated to be $9,631, which is a savings of $5,597. The estimates were made by the government officials who are familiar with the costs that could have been associated with investigating such an outbreak. Humans who were identified as positive were seen by doctors and referred to hospitals for treatment of brucellosis, and there were no mortalities. Farmers that had infected cattle and goats were provided information on how to minimize contracting brucellosis from their animals and animal products, and information on how to control and prevent the disease in cattle and goats (vaccinations and best management practices) was also provided.

Discussion     

Disease outbreak investigations are essential functions of any health system (human or animal), and can produce very useful information that can be used to stop the outbreak in question, learn more information about the various risk factors associated with the disease occurrence, design future intervention strategies, prepare policy briefs, and formulate hypotheses for future studies. By their nature, outbreaks have a strong time element in that they have to be addressed as soon as they occur. Due to the time element, the planning and implementation of theses outbreak investigations are extremely important and can be very challenging in terms of available resources (personnel, supplies, transportation needs etc.), logistics, communication, and laboratory facilities. This challenge is particularly significant where a major zoonotic disease (such as brucellosis) is involved.

In this disease outbreak, joint training of field and laboratory workers was conducted where team work, professionalism, and respect for each individual´s contribution was emphasized. The collection of specimens, handling, and laboratory testing were highly appreciated by the field and laboratory personnel. A highly appreciated aspect of the investigation was the fact that both Public Health and Animal Health teams were able to talk to the farmers jointly. The discussions covered disease transmission, signs, symptoms, treatment, and prevention of transmission of the disease in animal populations and transmission from animals to humans. This awareness of the disease was highly appreciated by the farmers. In this study we demonstrated that using a One Health approach is more efficient and less costly in investigating a zoonotic disease outbreak.

One major benefit of using a One Health approach in outbreak investigation or research is the reduction of tension with the farming community. In a non-One Health disease outbreak investigation or research, different agencies would visit the farms at different times (some visits would be from the Public Health team and others from the Animal Health team) and this is viewed by most farmers as too much waste of their time. Commonly, the Public Health team would be asked about disease in animals and the food products, such as milk and meat, questions, which they would not answer. Similarly, the Animal Health team would be asked about the disease in farmers, and would not be able to answer the questions. Inability to answer those questions and receiving these officials multiple times results in tension between farmers and Animal and Public Health authorities. One Health approach, therefore, minimizes this kind of tension and builds a healthy relationship.

As illustrated in the results, conducting the outbreak investigation using a One Health approach was estimated to be much cheaper than conducting two separate investigations (one by the Public Health Team and the other by the Animal Health Team) on the same farms. In low resource countries, such savings is very significant and should be encouraged.

Conclusion     

The value of the One Health approach in dealing with a zoonotic disease, such as brucellosis, would be: 1) developing integrated protocols and approaches that will consider the role of the human, domesticated animals, wildlife, and environment in the epidemiology of the disease, 2) opportunities for shared resources; such as data & information, facilities and personnel, integrated training of students and staff from the various disciplines, and 3) economic benefit (reduced cost of the investigation when a One Health approach is used).

Competing interests     

The authors declare no competing interest.

Authors´ contributions     

All the co-authors contributed in the implementation of the study and reviewed several drafts, and approval of the version to be published. Additionally, all authors were collaborators on the CIMTRADZ project and played a significant role in its implementation. All authors have read and agreed to the final version of this manuscript.

Acknowledgments     

The authors wish to acknowledge valuable financial support provided by the United States Agency for International Development (USAID) under The Africa-US Higher Education Initiative of American Council on Education (ACE), Association of Public and Land grant Universities (APLU) and Higher Education for Development (HED). The authors would also like to thank the farmers and staff from the Ministries of Health and Agriculture for their cooperation.

Figures     

Figure 1: protocol for human blood sample processing

Figure 2: protocol for animal blood sample processing

Figure 3: protocol for cow milk sample processing

Figure 4: protocol for goat milk processing

References     

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