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Brucellosis in the Kakheti Region of The DISSERTATION A SYSTEMIC REVIEW OF BRUCELLOSIS IN THE KAKHETI REGION OF THE COUNTRY OF GEORGIA: AN EVALUATION OF THE DISEASE ECOLOGY, RISK FACTORS AND SUGGESTIONS FOR DISEASE CONTROL Submitted by Karyn Alicia Havas Department of Clinical Sciences In partial fulfillment of the requirements For the Degree of Doctor of Philosophy Colorado State University Fort Collins, Colorado Fall 2011 Doctoral Committee: Advisor: Mo D. Salman Ashley E. Hill Robert J. Callan Shana C. Gillette Ann L. Magennis Copyright by Karyn A. Havas 2011 All rights reserved ABSTRACT A SYSTEMIC REVIEW OF BRUCELLOSIS IN THE KAKHETI REGION OF THE COUNTRY OF GEORGIA: AN EVALUATION OF THE DISEASE ECOLOGY, RISK FACTORS AND SUGGESTIONS FOR DISEASE CONTROL Human brucellosis is a neglected disease of poverty often found in highly agrarian, livestock dependent societies (World Health Organization, 2006). It is a purely zoonotic disease in that animals infect humans but there is not human-to-human transmission (Corbel, 2006). The highest human incidence of brucellosis in the country of Georgia is in the eastern region of Kakheti (Navdarashvili et al., 2005), which is also home to the majority of the country’s sheep and a significant portion of the country’s cattle population (Kvinikadze et al., 2009). In humans, brucellosis is acquired from animals either through direct contact with infected and shedding animals or their afterbirth or via consumption of contaminated dairy products made from the raw milk of a shedding animal. In Georgia, B. melitensis is the predominant species cultured from ill humans and has been cultured from sheep as well (Malania et al., 2009; Onashvili et al., 2009). It is likely that this Brucella spp. is also present in the cattle population. The overall aim of this project was to conduct a systemic analysis of the ecology and cause of brucellosis in the Kakheti region of Georgia so as to be able to provide recommendations for disease control. A systemic analysis is an all-encompassing look at ii a situation in order to understand its medical, political, economic, social, environmental and cultural aspects. This project studied the risk factors of brucellosis in Georgia and the dairy production and animal management systems associated with the human-animal interaction and how they differ based on the area of Kakheti and ethnic group. The human-animal interface data and the risk factors as well as available population level data from Georgia were used to create an agent-based model. This model simulated the impact of animal level disease interventions on the flock and herd prevalence and human brucellosis incidence. In the spring of 2010, a rapid assessment of Georgian animal management and pasturing practices as well as the dairy production and distribution practices was done in order to understand the human-animal interface. This study identified the distinction between male and female roles; the use of sheep and cattle; the management of sheep and cattle including any seasonal trends; the pasturing practices; dairy production methodologies and product distribution; and the identification of ethnic group differences in the use and management of the livestock and their associated dairy products. In order to identify the risk factors associated with brucellosis in the human population a non-matched, hospital-based case-control study was done using incident cases and controls from the Institute of Parasitology and Infectious Diseases in Tbilisi, Georgia in 2010. Findings indicated at a significance level of 10% that sheep ownership (OR: 19.3; 95% CI: 4, 94), living in Kakheti (OR: 278.1; 95% CI: 5, 15454), being older than 44 years of age (OR: 9.3; 95% CI: 0.7, 129) and making dairy products from cow milk (OR: 12.4; 95% CI: 1, 173) were all high-risk groups. The potential reason that the age group of 44 years of age and older had a greater odds of disease as compared to iii students and young children, the referent, could be due to a larger role in animal care, or a potential bias from the control group, which had more young people in comparison to the cases. All types of occupations – animal and non-animal related – had increased odds of disease due to the fact that, irrespective of the type of work, individuals cared for animals at the home. The sample population was hospital-based from a highly centralized health care system. Diagnosis for cases and controls required travel to Tbilisi, the capitol city, and thus external validity may be questionable. Also, different strains of Brucella spp. have different levels of virulence in human hosts and different levels of dose based on the method of exposure. Therefore, B. melitensis and exposure from direct contact may be over-represented among the population as compared to the lesser virulent B. abortus and methods of exposure which have a lower dose associated with them, such as from contaminated dairy product consumption. Finally the agent-based model (ABM) was built to evaluate the impact of animal level interventions on herd and flock prevalence and human disease incidence. It further analyzed the disease impact among shepherds, herders, cow and sheep milkers and cow milk dairy producers. A sheep milker also makes the dairy products and thus incorporates that risk. An agent-based model was used because patterns of human- livestock interactions in the Kakheti region elucidated by rapid assessment could be simulated using ABM whereas without regional or national human-livestock effective contact rates and prevalence statistics, population-based modeling was not possible. The results indicated that the lower the proportion of individuals involved in agriculture, the less impact animal-based interventions had on the human incidence rate; that at least five iv years were needed to control the disease (bring the animal prevalence to <2%); and that disease in cattle had the greatest influence on human disease incidence. This dissertation project provided an in-depth encompassing look at the transmission of brucellosis between livestock and humans in the Kakheti region of Georgia. Further, it provides a broader understanding of the disease ecology in this region due to the fact that it incorporates a study to understand the complexity of the human-livestock interface that is the source of disease transmission from livestock to humans. v TABLE OF CONTENTS Abstract .............................................................................................................................. ii List of Tables .................................................................................................................... ix List of Figures ................................................................................................................... xi Chapter 1: Introduction and Research Objectives ........................................................ 1 Brucellosis in the country of Georgia .......................................................................... 1 Characteristics of the country of Georgia .................................................................. 4 The Post-Soviet Georgian State .................................................................................. 5 Agriculture in Georgia ................................................................................................ 8 Millennium Development Goals and Current Standards .......................................... 11 Research Objectives and Scope ................................................................................. 11 Chapter 2: Brucellosis .................................................................................................... 14 Bacteriological characteristics and taxonomy .......................................................... 14 Epidemiology and pathophysiology ........................................................................... 16 Disease spread among livestock ............................................................................... 16 Disease spread from livestock to humans ................................................................. 18 Pathogenesis in Livestock and Humans .................................................................... 20 Clinical Disease ............................................................................................................ 23 Disease in livestock ................................................................................................... 23 Disease in humans ..................................................................................................... 25 Diagnostic Testing ....................................................................................................... 26 Serologic tests in livestock ........................................................................................ 26 Serologic tests in humans .......................................................................................... 32 Culture of Brucella spp. ............................................................................................ 35 Polymerase Chain Reaction ...................................................................................... 36 Disease Control and Eradication ............................................................................... 40 Vaccination in disease control programs .................................................................. 41 Food safety in disease control programs ................................................................... 45 Components of an eradication
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