Epidemiology, geographical distribution, and economic consequences of swine zoonoses: a narrative review

OPEN Emerging Microbes and Infections (2013) 2, e92; doi:10.1038/emi.2013.87 ß 2013 SSCC. All rights reserved 2222-1751/13 www.nature.com/emi REVIEW Epidemiology, geographical distribution, and economic consequences of swine zoonoses: a narrative review Salah Uddin Khan1,2, Kalina R Atanasova1,2, Whitney S Krueger1,2, Alejandro Ramirez3 and Gregory C Gray1,2 We sought to review the epidemiology, international geographical distribution, and economic consequences of selected swine zoonoses. We performed literature searches in two stages. First, we identified the zoonotic pathogens associated with swine. Second, we identified specific swine-associated zoonotic pathogen reports for those pathogens from January 1980 to October 2012. Swine-associated emerging diseases were more prevalent in the countries of North America, South America, and Europe. Multiple factors were associated with the increase of swine zoonoses in humans including: the density of pigs, poor water sources and environmental conditions for swine husbandry, the transmissibility of the pathogen, occupational exposure to pigs, poor human sanitation, and personal hygiene. Swine zoonoses often lead to severe economic consequences related to the threat of novel pathogens to humans, drop in public demand for pork, forced culling of swine herds, and international trade sanctions. Due to the complexity of swine-associated pathogen ecology, designing effective interventions for early detection of disease, their prevention, and mitigation requires an interdisciplinary collaborative ‘‘One Health’’ approach from veterinarians, environmental and public health professionals, and the swine industry. Emerging Microbes and Infections (2013) 2, e92; doi:10.1038/emi.2013.87; published online 24 December 2013 Keywords: swine; zoonoses; epidemiology; transmission; review INTRODUCTION The history of pig raising goes back as far as ,9000 BC, likely with the domestication of wild boars in Eurasia.1 Since then, pork has served as a major source of human nutrition. In the last 50 years, the consumption of pork and the demands of products from pigs have increased, causing the global pig population to grow from 406 million to 966 million heads.2 Pigs are anatomically and physiologically similar to humans in terms of dentition, ocular, dermal, cardiovascular, renal, and digestive systems.3 While these have led to great advances in human and pig health, including substituting human organs with swine organs, these shared biological characteristics sometimes have the potential to permit pathogens to cross the species barrier.4,5 Although, pigs have been long known to serve as reservoirs for zoonotic pathogens, our understanding regarding zoonotic disease ecology in pigs is rather superficial.6,7 As such, although many swine pathogens are well-controlled, some zoonotic pathogens have become well-established in swine populations, imparting health and economic burdens. Some of these viruses, bacteria and parasites are emerging or re-emerging in nature, while others appear sporadically or transmit to man only under certain circumstances.8 Reducing these diseases in animals and humans often requires adopting primary or secondary prevention techniques, or a combination of both.9 However, doing so requires extensive understanding of husbandry practices, ecological preconditions, human risk behaviors, and the modes of transmission for swine-associated zoonoses. To facilitate a better understanding of their prevention and control, this review discusses the epidemiology, geographical distribution, and economic consequences of selected swine zoonoses from a global perspective. LITERATURE REVIEW AND DATA SUMMARIZATION We performed literature searches in two stages: first, to identify the zoonotic pathogens associated with swine and second, to identify the literature describing specific zoonotic pathogens. For the first stage, we performed a literature review in PubMed and in Google Scholar (English only) for articles published from January 1980 to October 2012, and searched by using the following terms: (swine or pig or boar or Sus scrofa) and (zoonoses or zoonosis or zoonotic). Additional relevant articles and books published between 1970 and 2012 were identified by reviewing the references from the collection of reports and through examining the authors’ collections of publications. We included other swine-associated zoonotic diseases by reviewing lists compiled by the World Organization for Animal Health (www.oie.int) and the Merck Veterinary Manual (http://www.merckmanuals.com). Once the list of zoonoses was identified, we performed disease specific literature reviews to gather epidemiology and population level disease burden data from PubMed, Google Scholar, and in authors’ personal files using the following terms: (disease name or pathogen name) and (swine or pig or boar or Sus scrofa). We classified the swine-associated zoonoses in three major categories: emerging, endemic, and sporadic. An emerging zoonosis was defined when ‘‘the disease did not occur in humans before, or had occurred previously but affected only a small number of people in an 1 Department of Environmental and Global Health, College of Public Health and Health Professions, University of Florida, Gainesville, FL 32611, USA; 2Emerging Pathogens Institute, University of Florida, Gainesville, FL 32611, USA and 3Veterinary Diagnosis and Production Animal Medicine, Iowa State University, Iowa, IA 5011, USA Correspondence: GC Gray E-mail: Received 19 August 2013; revised 22 November 2013; accepted 25 November 2013 Global review of swine zoonoses SU Khan et al 2 isolated place, or had occurred in a population but was not recognized as a distinct disease’’.10 Diseases were defined as endemic where they appeared to cluster geographically but not in time and as sporadic when they were clustered only in time.11 Zoonoses were sub-categorized into two groups: global occurrence and occurrence limited to a region(s) or geography. Additionally, we briefly reviewed the overall economic consequence data of swine zoonoses and swine-associated pathogens with zoonotic potential. To demonstrate global distribution of the swine-associated zoonoses, we performed ‘‘geographically weighted regression’’, an exploratory spatial analysis to develop a risk map for the emerging, endemic, and sporadic swine associated zoonoses after adjusting for population and swine density (2011) for each of the countries.12 We obtained human population density data from World Bank reports (www. worldbank.org), and pig density data from World Organization for Animal Health (www.oie.int). We did not obtain formal ethical approval because this study reviewed data from already published literatures. For this body of research, the role of the funding agencies was to provide monetary support only. They did not have any role in the project’s conception, design, analysis, or manuscript preparation. A detailed list of t (...truncated)