Emerging Diseases from Animals
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December 2013, an outbreak of the deadly Ebola virus began in a small village in southern Guinea, the first outbreak of the Zaire Ebola strain in West Africa. Within a year’s time, the outbreak, which was not officially noticed by health authorities until March 2014, had led to approximately 18,000 known human cases and 6,300 deaths, posing an unprecedented challenge to global public health. Air travel helped the disease leap from West Africa to other continents, including North America and Europe.
KeywordsSevere Acute Respiratory Syndrome Simian Immunodeficiency Virus Zoonotic Disease Severe Acute Respiratory Syndrome Rift Valley Fever
December 2013, an outbreak of the deadly Ebola virus began in a small village in southern Guinea, the first outbreak of the Zaire Ebola strain in West Africa. Within a year’s time, the outbreak, which was not officially noticed by health authorities until March 2014, had led to approximately 18,000 known human cases and 6,300 deaths, posing an unprecedented challenge to global public health. Air travel helped the disease leap from West Africa to other continents, including North America and Europe.1
Despite global attention and response, 12 months into the outbreak the initial source of human infection still had not been identified. Prior Ebola outbreaks in humans, as well as a concurrent outbreak in the Democratic Republic of the Congo beginning in August 2014, have been linked to the hunting or handling of wild animals, with subsequent transmission among humans. Certain bat species are the suspected natural source for the virus and are thought to harbor it without signs of disease. Researchers have detected Ebola infection and mortality in wild chimpanzees, gorillas, and duiker antelopes, and evidence from human outbreaks suggests that these species have served as brief hosts for potential human infection when hunted or handled. Studies suggest that Ebola is causing severe declines in great ape populations—particularly critically endangered wild lowland gorillas—making it as much a threat to biodiversity as it is to human health.2
Around the same time that the Ebola outbreak was spreading through West Africa, a human case of a different disease, caused by another pathogen in the same family of viruses, emerged in Uganda. The infected patient experienced symptoms including fever, abdominal pain, vomiting, and diarrhea and ultimately died a few weeks into the illness, caused by the Marburg virus. While the source of this particular outbreak was not known, past human cases of Marburg originated from contact with certain species of cave-dwelling bats that serve as the natural carriers of the virus.3
Ebola and Marburg viruses are just two examples of an emerging but largely overlooked trend: the spread of infectious disease from animals to humans. The emergence of such “zoonoses,” responsible for a growing number of disease outbreaks that have sickened or killed millions, is facilitated by the human disruption of natural ecological conditions, which has allowed for increased human-animal contact. Despite the extensive public health response to these emerging infectious diseases, the focus has been on reactive rather than preventive efforts. But new strategies for dealing with these threats offer the possibility that such diseases need not be a threat and a scourge, and that humans once again can learn to live in balance with the natural ecology that supports us.
Pandemics of Animal Origin: A Growing Threat
For millennia, humans have been stricken, sometimes seriously so, by pathogens originating in animals. Many diseases that are commonly known to be transmitted among people, such as measles and (formerly) smallpox, evolved from microbes living in wildlife. And many of history’s most devastating pandemics have animal origins, including the Justinian Plague (541–542 AD), the Black Death (Europe, 1347), yellow fever (South America, sixteenth century), and the global flu outbreak of 1918—as well as modern pandemics such as HIV/AIDS, severe acute respiratory syndrome (SARS) in 2003, and the highly pathogenic H5N1 (avian) flu.
But when an endemic zoonosis crosses into a new geographical area or host species, or evolves new traits (such as drug resistance)—or when a novel pathogen is transmitted to humans for the first time and causes an outbreak—it becomes an “emerging” zoonosis. Emerging zoonoses from wildlife account for most of the emerging infectious diseases identified in people in the past 70 years. Their spread typically is facilitated by human activities, including changes in land use, population growth, alterations in behavior or social structure, international travel or trade, microbial adaptation to drug or vaccine use or to a new host species, and breakdown in public health infrastructure. These activities give zoonoses tremendous range: with more than 1 billion international travelers every year, as well as the extensive international trade of wildlife, infected individuals could potentially spread zoonotic diseases anywhere in the world.5
In the past few decades, accelerating global changes have led to the emergence of a striking number of newly described zoonoses, including hantavirus pulmonary syndrome (a respiratory disease contracted from infected rodents), monkeypox (similar to smallpox, and transmitted from a variety of animals), SARS (a pneumonia spread by small mammals), and simian immunodeficiency virus (the animal precursor to HIV). Some of these zoonoses, such as HIV, have become established as serious diseases that now pass from person to person without repeated animal-to-human transmission.
Ecology of Disease
Like any infection, zoonoses emerge when a chain of infection is activated—a process whereby the pathogen or infectious agent passes from the reservoir host in which it naturally occurs, or from an intermediate host species, to a susceptible host and is ultimately pathogenic to humans. For infection to occur, all six elements of the chain of infection must be present, from the disease-causing agent, to the mode of transmission, to the susceptible host. (See Box 8–1.) In its simplest form, this chain is straightforward—but any of the elements can present complications.6
Consider a case where an animal species, such as a small rodent, can be a reservoir host (carrying the infectious agent), but it also can host ticks (a vector for spread of infection of some pathogens)—thus complicating and potentially increasing the opportunities for dissemination. White-footed mice are a natural reservoir of the bacteria that cause Lyme disease and can spread the bacteria to ticks that feed on the mice, enabling the infection to spread to other species that the ticks feed on, including humans. Some zoonoses can have several reservoirs or intermediate host species, each of which might have a different role in a pathogen’s emergence. The Nipah virus, which lives in fruit bat reservoir hosts in Malaysia, also became established in domestic pig populations in the 1990s, amplifying viral transmission and leading to a large human outbreak in 1998–99 that killed 100 people and led to the slaughter of more than a million pigs as a control measure.7
Human activities can change the ecologies underlying the chain of infection of zoonoses, such as when these activities alter the size of the host population. Reducing the population of a preferred animal host, such as a large, hoofed animal, can cause a transmitter, such as a mosquito, to shift its feeding patterns to humans, leading to a disease outbreak. After cattle imported from Asia introduced a viral disease known as rinderpest, or “cattle plague,” to Africa, both cattle and wildebeest populations in Africa declined rapidly and tsetse flies switched to feeding on people, causing a large epidemic of sleeping sickness.8
Box 8–1. The Chain of Infection
Development of an infection has six components:
Agent of disease. The disease-causing organism, or pathogen, which can take the form of a bacteria, virus, fungus, or parasite.
Reservoir. The species—human, animal, or insect—in which the pathogen naturally resides. Pathogens can live in a reservoir for long periods without emerging to cause an epidemic. Reservoir hosts may not be seriously harmed by the pathogen.
Portal of exit. The path by which a pathogen leaves its reservoir or host. Examples include the respiratory tract, urinary tract, rectum, and cuts or lesions in skin.
Mode of transmission. The way a pathogen spreads from its reservoir host to the susceptible host. This can occur directly, via skin-to-skin contact or sexual relations, or through the spread of droplets from coughing or sneezing. It also can occur indirectly, as when organisms are carried on airborne particles, when intermediate objects such as handkerchiefs or bedding are the vehicle of transmission, or when mosquitoes, ticks, and other vectors carry the pathogen.
Portal of entry. The place a pathogen enters a susceptible host. The mouth and nose are common portals of entry. Others include the skin (for hookworm), mucous membranes (for influenza or syphilis), and blood (for hepatitis B and HIV).
Susceptible host. Some host species can acquire the pathogen but do not naturally carry it, and may be affected or unaffected by it, potentially transmitting it to other species or populations or serving as a dead-end for transmission.
Importantly, human activities can facilitate the transmission of a pathogen at any of these six places—by, for example, enabling contact between reservoir and host species or inducing genetic selection for virulent strains that are more likely to be pathogenic to humans. Conversely, human intervention around any of the six components can stop the spread of an infectious disease.
Source: See endnote 6.
Sometimes, a naturally occurring or environmental change can lead to a change in the size of host populations, increasing the risk of transmission to humans. El Niño events in 1991–92 and 1997–98 led to the appearance of human hantavirus cases in the southwestern United States, via an ecological cascade: increased precipitation caused vegetation growth, which supported increased populations and densities of rodents, which, in turn, facilitated hantavirus infections in rodents. These changes increased the risk of infection in people.9
Ecological principles also apply to the dynamics of pathogens within individual hosts. Pathogen populations living within an infected host grow and evolve according to the same competitive principles that govern the growth of plants or animals living freely outside a host. This competition between pathogens and other microbes within a host, in addition to molecular factors and the mode of transmission, can determine how great a threat the pathogen poses to human health. Shifting the diet of beef cattle before slaughter, for example, creates new environmental conditions within the gut of the animal that can increase the population of human pathogens, such as the foodborne bacterium E coli that can result in illness and even death.10
The community of commensal (or co-existing) bacteria—such as the “good bacteria” in the gut that help with the digestive process—also plays an important part in combating pathogens. Disruption of this community through changes in diet or through the use of antimicrobial remedies can allow the growth of other organisms, some of which might be pathogenic. This disruption may explain some of the increased risk of zoonotic infections for salmonella, for example. The vital role played by commensal bacteria underscores the importance of studying the full microbial community within a host, and not just pathogens.11
Livestock and Wild Animals
People eat a wide range of animals, both farm raised and wild, and many of these can harbor bacteria, viruses, or parasites that can be transmitted to humans. This makes the production, processing, and consumption of livestock, as well as the hunting, preparation, and consumption of wild meat, potential paths of disease transmission.12
As human societies develop, each era of livestock revolution presents new health challenges and new opportunities for the emergence of zoonotic pathogens. Pathogens found in livestock production processes have caused repeated outbreaks of bovine tuberculosis, brucellosis, salmonellosis, and other illnesses that result from new cultural and farming practices. Livestock production practices that can create challenges for animal health include high stocking rates, mixing of species, prophylactic use of antimicrobials for growth promotion, and poor implementation of disease surveillance and control measures. These practices often are found in areas where the veterinary infrastructure is weak and where the public-private partnerships, policies, and capacities to support and strengthen it are insufficient.13
In addition, methods of slaughtering and processing animals; storing, packing, and transporting products; and preparing foods in the home can facilitate outbreaks of foodborne diseases. Incomplete cooking of pigs and wild boars can lead to trichinosis and cysticercosis, the latter afflicting 50 million people annually (often subsistence farmers in developing countries) and resulting in epilepsy and even death. Echinococcosis, caused by the larval stages of a tapeworm that is transmitted via hoofed animal hosts, is spread through the ingestion of inadequately prepared food, affecting 200,000 people every year and costing more than $4 billion annually for treatment and control. Other notable parasites transmitted through inadequate food processing and preparation include trematodes (liver, lung, and intestinal tapeworms), a neglected disease group that poses a serious threat to public health and economic prosperity in Southeast Asia.15
Globally, people consume far fewer wildlife products than they do livestock, but the human demand for wild meat is not inconsequential: in central African countries alone, people eat an estimated 1 million tons of wild meat annually. Human contact with animals through the hunting, preparation, and consumption of wild animals has led to the transmission of deadly diseases such as HIV/AIDS (linked to the butchering of hunted chimpanzee), SARS (which emerged in wildlife markets and among restaurant workers in southern China), and Ebola. In each case, the organisms or pathogens exploited new opportunities that resulted from changes in human behavior.16
Large-scale changes in land use contribute to the spread of many zoonoses, by affecting biodiversity and the relations between animal reservoirs and other animal hosts or vectors, people, and pathogens. Land modification can lead to changes in vegetation patterns, microclimates, human contact with animals (both domestic and wild), and the abundance, distribution, and demographics of vector and host species, all of which are critical factors in disease ecology.
In the region surrounding the town of Lyme, Connecticut, a repeated cycle of deforestation, reforestation, and habitat fragmentation changed the dynamics of predator-prey populations and led to the emergence and spread of Lyme disease, now the most common vectorborne illness in the United States. The mobility of ticks and other carriers has enabled the disease’s observed northward and westward spread over the past decade. Similarly, the origin of human alveolar echinococcosis, a disease associated with a tapeworm that often resides in small mammals (especially rodents), has been traced to Tibet, where overgrazing and degradation of pastures increased the population densities of small mammals, which served as intermediate hosts for the disease and passed it to humans.17
Many tropical regions are emerging disease hotspots, rich in diversity of both wildlife and microbes—many of which have not yet been encountered by people. The opening up of tropical forests for plantation development and extractive industries such as mining, logging, and oil and gas may increase the risk of zoonotic disease by changing the composition of habitats and vector communities, altering the distribution of wild and domestic animal populations, and increasing exposure to pathogens through increased human-animal contact. Among the infectious diseases associated with changes in tropical land use are Chagas disease, leishmaniasis, and yellow fever—all of which are life-threatening illnesses spread via infected insects.18
Human contact with wildlife is increasing on a large scale through road building, the establishment of settlements, and the rising mobility of people, as well as through the extractive processes themselves. In areas where such changes take place, the hunting, consumption, and trade of wildlife for food often rises. If a site is poorly managed, the growing human population can strain existing infrastructure, leading to overcrowding, poor sanitary conditions, improper waste disposal, and a lack of potable water. All of these changes increase the risk of cross-species transmission of pathogens, resulting in zoonotic disease. Recent human immigrants to an area may not have immunity to zoonotic diseases that are endemic to that area, making them particularly susceptible to infection.19
Although extractive industry companies often do assessments of the environmental and social impacts of their activities, these studies rarely include principles of disease ecology because standard operating procedures in developing countries and specific laws or regulations often do not require the assessment of health risks at a community level. And although some assessments do include zoonotic disease from domestic animals in their guidelines, few adequately address the full range of potential zoonotic pathogens, especially from wildlife.20
Resistance to Antimicrobial Drugs
Injudicious use of antibiotics and other antimicrobial remedies in animals can leave people vulnerable to the spread of infectious disease. The most direct mechanism for the evolution of antimicrobial-resistant infectious diseases in people is the use of antibiotics in treating human infections. But the widespread use of antimicrobial drugs in livestock production—both to prevent disease and to promote animal growth—has led to worries about this being another possible route for emerging antibiotic resistance in people. Not only may genetic selection pressures from antimicrobial use lead to development of resistant strains, potentially posing food security risks and zoonotic disease risks for livestock handlers, but antimicrobial exposure may also occur via the food chain as well as through environmental dispersion (e.g., through manure, runoff, etc.).21
From an ecological perspective, antimicrobial resistance is a natural occurrence. Genes conferring resistance probably originated as an evolutionary response to antimicrobial compounds that bacteria, fungi, and plants living freely in the environment produced to protect themselves from infection or competition. The early antibiotics used in human medicine all were derived from natural bacterial and fungal sources. Over time, use of these compounds resulted in selection for resistance in bacteria, and horizontal transfer allowed these genes to spread rapidly through microbial populations and communities. Today, antimicrobial resistance is emerging based on these same evolutionary principles, with microbial populations adapting through competition and selection. But because the use of antimicrobial agents in people is far more widespread now than it was when these drugs were developed, the potential for emergence of resistance is likely much more rapid.22
The common practice of administering antimicrobials to livestock may be contributing to this trend. Increased intensification of livestock production over the past half century has created dense host populations that readily transmit disease. In response, agricultural industries introduced a range of antimicrobial drugs to combat the spread of infection among closely confined animals. In addition to being used prophylactically, some of these antibiotics are used in animal feed to enhance growth rates, improve feeding efficiencies, and decrease the animals’ waste output.23
The question of whether antibiotic use in agriculture has exacerbated drug resistance in people is widely debated. Farm workers who were exposed to antibiotics through their jobs showed an increased prevalence of resistant bacteria in their gut, and studies have reported instances of farm animals containing resistant pathogens of relevance to human medicine—including a strain of Staphylococcus aureus that is resistant to methicillin, a first-line antibiotic once commonly used to prevent Staph infections. It is possible, however, that these bacteria were passed to the animals from people.
Antimicrobial-resistant pathogens may be transmitted from livestock to people in several ways, including food consumption, direct contact with treated animals, waste management, use of manure as fertilizer, fecal contamination of runoff, and relocation or migration of animals. Additionally, some 30–90 percent of veterinary antibiotics are excreted after being administered to livestock—mostly in an unmetabolized form—providing a route for dissemination and potentially exposure in the environment.24
Understanding the ecology of zoonotic diseases is a complex challenge. It requires knowledge of animal and human medicine, ecology, sociology, microbial ecology, and evolution, as well as of the underlying dynamics that increase the transmission of pathogens in humans, wildlife, and livestock. The so-called One Health perspective, which considers this wider web of interactions and dynamics, incorporates a critical understanding of how the environment is changing, and how these changes, in turn, affect microbial dynamics. Because of the wide range of disciplines involved, preventing and responding to zoonotic diseases requires a multidisciplinary effort, with collaboration among ministries of health, environment, and agriculture; within and across governments; and with intergovernmental agencies involved in health, trade, food production, and the environment.26
As one key to a multisectoral approach to zoonosis prevention, ecologists and clinicians need to collaborate in early-detection and control programs. Combining ecological science and real-time clinical data could improve the accuracy of mathematical models, the design of prospective and retrospective studies, and the outcomes of field studies seeking to identify key risk factors. In addition, great value would accrue if public health scientists (who use epidemiological techniques and rely on human case data) collaborated closely with disease ecologists (who often work with wildlife or livestock data) to model risk in human beings. Such disease ecology approaches might be useful not only in containing an established outbreak, but also in predicting the emergence and spread of new zoonoses. Understanding the relationship between environmental changes; the dynamics of wildlife, domestic animal, and human populations; and the dynamics of their microbes can be used to forecast the risk of human infection from zoonoses.27
Frequently, the dynamics of pathogens in the non-human reservoirs of a zoonosis (apes, mosquitoes, mice, etc.) determine the risk of outbreak in people. This risk can vary with geography, the season, or across multiyear cycles, and is influenced by changes in land use, weather, climate, and the environment. Knowing the dynamics of zoonotic pathogens in their wildlife reservoirs could help in creating an early-warning system to alert authorities of the risk of an outbreak in livestock or people. In the case of Rift Valley fever, the density of vegetation correlates with breeding sites for the mosquito vectors, and satellite monitoring of this density has been used to forecast cases of the disease in people and to predict the need for vaccines. Such approaches can be refined and developed, and eventually used to predict the risk of future disease emergence.28
Other ways to further global disease prevention capacity and efforts include implementing the World Health Organization’s International Health Regulations, which make it easier to report a broad range of human disease events, and supporting implementation of the World Organisation for Animal Health’s international standards for animal health, which require the reporting of animal diseases, including zoonoses. Improving veterinary services in many low-income and middle-income countries can help to expand awareness of zoonotic diseases, the ability to detect and prevent them in animals (including wildlife), and the ability to quantify and report their occurrences. Because of the high economic costs of zoonotic diseases to both commerce and society, it could prove more cost effective to try to prevent and control these diseases by integrating science-based control strategies in animals, rather than seeking to control the illnesses in people alone.29
New avenues of research are needed to understand the complex ecology of antimicrobial resistance and foodborne zoonoses, including how the microbiomes of both humans and the animals that we interact with work, and what causes zoonotic microbes to proliferate. The effects of antibiotic use in livestock are not well understood, but involving physicians, veterinarians, and ecologists in the design and interpretation of studies could advance our understanding of this area. Standardized data collection, long-term monitoring, and risk assessments are needed to better understand the development of multidrug resistance and multibacterial infections, from the use of antimicrobials in livestock as well as from wildlife. To reduce the need for antimicrobial use in people and animals, alternatives such as probiotics, diets to promote healthy or protective gastro-intestinal flora, and new methods of immune system modulation need to be explored.31
Extractive industries, such as mining and oil production, can be part of disease prevention as well, by helping to minimize the opportunities that enable transmission of pathogens that are new to human hosts. Guidelines are needed urgently for safe or best practices that include ecological knowledge to reduce the risk of disease emergence or occurrence. Disease risk analysis tools can be used to determine the potential health impacts of ecological change from potential human activities, allowing for proactive interventions that will mitigate risks. For example, industries establishing work sites (such as mining operations) in remote areas could be required to provide food sources for their employees to reduce subsistence hunting of wildlife. Such guidelines could be required by development banks or other public agencies that finance large-scale projects, or by insurers.
The wide gaps that exist between industrialized and developing countries in public health, veterinary, and medical infrastructure and training affect efforts to prevent, monitor, and control disease. In addition, ecological approaches for preventing and controlling zoonotic disease are not used in most countries. These challenges need urgent attention, and the One Health approach provides a promising holistic framework for achieving this aim.
Although the causes and risks of zoonoses vary widely across regions and cultures, increasing global connectedness demands the attention and alertness of health professionals everywhere. Because human activities are a driving force for where and how zoonoses occur, not only are improved healthcare systems needed, but multisectoral approaches to mediate the impact of human activities on disease dynamics are indispensable to contain zoonoses and prevent the emergence of new ones.
Sylvain Baize et al., “Emergence of Zaire Ebola Virus Disease in Guinea,” New England Journal of Medicine 371 (October 9, 2014): 1418–25.
World Health Organization (WHO), “Situation Reports: Ebola Response Roadmap,” www.who.int/csr/disease/ebola/situation-reports.en/; E. M. Leroy et al., “Multiple Ebola Virus Transmission Events and Rapid Decline of Central African Wildlife,” Science 303, no. 5658 (January 16, 2004): 387–90; Heinz Feldmann and Thomas W. Geisbert, “Ebola Haemorrhagic Fever,” The Lancet 377, no. 9768 (March 5, 2011): 849–62; Leroy et al., “Multiple Ebola Virus Transmission Events and Rapid Decline of Central African Wildlife.”
WHO, “Marburg Virus Disease – Uganda,” October 10, 2014, www.who.int/csr/don/10-october-2014-marburg/en/; Feldmann and Geisbert, “Ebola Haemorrhagic Fever.”
International Livestock Research Institute, Mapping of Poverty and Likely Zoonoses Hotspots, Zoonoses Project 4, report to U.K. Department for International Development (Nairobi: 2012).
Kate E. Jones et al., “Global Trends in Emerging Infectious Diseases,” Nature 451 (February 21, 2008): 990–93; J. Newcomb, T. Harrington, and S. Aldrich, The Economic Impact of Selected Infectious Disease Outbreaks (Cambridge, MA: Bio Economic Research Associates, 2011); Mark S. Smolinski, Margaret A. Hamburg, and Joshua Lederberg, Committee on Emerging Microbial Threats to Health in the 21st Century, Microbial Threats to Health: Emergence, Detection, and Response (Washington, DC: The National Academies Press, 2003).
Box 8–1 from U.S. Centers for Disease Control and Prevention, “Lesson 1: Introduction to Epidemiology,” in Principles of Epidemiology in Public Health Practice, Third Edition. An Introduction to Applied Epidemiology and Biostatistics, Self-Study Course SS1978, www.cdc.gov/ophss/csels/dsepd/SS1978/Lesson1/Section10.html.
D. T. Haydon et al., “Identifying Reservoirs of Infection: A Conceptual and Practical Challenge,” Emerging Infectious Diseases 8, no. 12 (December 2002): 1468–73; J. R. C. Pulliam et al. and the Henipavirus Ecology Research Group (HERG), “Agricultural Intensification, Priming for Persistence and the Emergence of Nipah Virus: A Lethal Bat-borne Zoonosis, Journal of The Royal Society Interface 9, no. 66 (January 2012): 89–101.
John Ford, The Role of Trypanosomiasis in African Ecology (Oxford, U.K.: Clarendon Press, 1971).
B. Hjelle and G. E. Glass, “Outbreak of Hantavirus Infection in the Four Corners Region of the United States in the Wake of the 1997–1998 El Nino-southern Oscillation,” The Journal of Infectious Diseases 181, no. 5 (May 2000): 1569–73.
Todd R. Callaway et al., “Diet, Escherichia coli O:157:H7, and Cattle: A Review After 10 Years,” Current Issues in Molecular Biology 11, no. 2 (2009): 67–79.
David A. Relman, “Microbial Genomics and Infectious Diseases,” New England Journal of Medicine 365 (July 28, 2011): 347–57; A. R. Manges et al., “Comparative Metagenomic Study of Alterations to the Intestinal Microbiota and Risk of Nosocomial Clostridum difficile-associated Disease, The Journal of Infectious Diseases 202, no. 12 (December 15, 2010): 1877–84; M. Crhanova et al., “Immune Response of Chicken Gut to Natural Colonization by Gut Microflora and to Salmonella enterica Serovar Enteritidis Infection, Infection and Immunity 79, no. 7 (July 2011): 2755–63; Relman, “Microbial Genomics and Infectious Diseases.”
Christopher Delgado et al., Livestock to 2020: The Next Food Revolution, Food, Agriculture, and the Environment Discussion Paper (Washington, DC: International Food Policy Research Institute, 1999).
Richard Coker et al., “Towards a Conceptual Framework to Support One-Health Research for Policy on Emerging Zoonoses, The Lancet Infectious Diseases 11, no. 4 (April 2011): 326–31; Delgado et al., Livestock to 2020: The Next Food Revolution; D. H. Molyneux, “Control of Human Parasitic Disease: Context and Overview, Advances in Parasitology 61 (2006): 1–43; WHO, Interagency Meeting on Planning the Prevention and Control of Neglected Zoonotic Diseases (NZDs), Geneva, Switzerland, July 5–6, 2011.
The Writing Committee of the WHO Consultation on Human Influenza A/H5, “Avian Influenza A (H5N1) Infection in Humans,” New England Journal of Medicine 353 (September 29, 2005): 1374–85; William B. Karesh et al., “Wildlife Trade and Global Disease Emergence,” Emerging Infectious Diseases 11, no. 7 (July 2005): 1000–02.
Trichinosis from D. G. Newell et al., “Food-borne Diseases – The Challenges of 20 Years Ago Still Persist While New Ones Continue to Emerge,” International Journal of Food Microbiology 139, Supplement 1 (May 30, 2010): S3–15; 50 million from International Livestock Research Institute, Mapping of Poverty and Likely Zoonoses Hotspots; WHO, “WHO Consultation to Develop a Strategy to Estimate the Global Burden of Foodborne Diseases (Geneva: 2006); L. D. Sims et al., “Origin and Evolution of Highly Pathogenic H5N1 Avian Influenza in Asia,” Veterinary Record 157, no. 6 (August 6, 2005): 159–64.
Karesh et al., “Wildlife Trade and Global Disease Emergence”; chimpanzees from Beatrice H. Hahn et al., “AIDS as a Zoonosis: Scientific and Public Health Implications, Science 287, no. 5453 (January 28, 2000): 607–14; Y. Guan et al., “Isolation and Characterization of Viruses Related to the SARS Coronavirus from Animals in Southern China,” Science 302, no. 5643 (October 10, 2003): 276–78; P. Rouquet et al., “Wild Animal Mortality Monitoring and Human Ebola Outbreaks, Gabon and Republic of Congo, 2001–2003,” Emerging Infectious Diseases 11, no. 2 (February 2005): 283–90.
J. A. Patz et al. and the Working Group on Land Use Change and Disease Emergence, “Unhealthy Landscapes: Policy Recommendations on Land Use Change and Infectious Disease Emergence,” Environmental Health Perspectives 112, no. 10 (July 2004): 1092–98; A. Marm Kilpatrick and Sarah E. Randolph, “Drivers, Dynamics, and Control of Emerging Vector-borne Zoonotic Diseases,” The Lancet 380, no. 9857 (December 1, 2012): 1946–55; P. S. Craig and the Echinococcosis Working Group in China, “Epidemiology of Human Alveolar Echinococcosis in China,” Parasitology International 55, Supplement (2006): S221–25.
Jones et al., “Global Trends in Emerging Infectious Diseases”; Patz et al. and the Working Group on Land Use Change and Disease Emergence, “Unhealthy Landscapes: Policy Recommendations on Land Use Change and Infectious Disease Emergence”; J. F. Walsh, D. H. Molyneux, and M. H. Birley, “Deforestation: Effects on Vectorborne Disease,” Parasitology 106, Supplement S1 (January 1993): S55–75; yellow fever and leishmaniasis from Bruce A. Wilcox and Brett Ellis, “Forests and Emerging Infectious Diseases of Humans,” Unasylva 57, no. 224 (2006): 11–18.
Wilcox and Ellis, “Forests and Emerging Infectious Diseases of Humans”; Karesh et al., “Wildlife Trade and Global Disease Emergence”; J. R. Poulsen et al., “Bushmeat Supply and Consumption in a Tropical Logging Concession in Northern Congo,” Conservation Biology 23, no. 6 (December 2009): 1597–608; N. Pramodh, “Limiting the Spread of Communicable Diseases Caused by Human Population Movement,” Journal of Rural and Remote Environmental Health 2, no. 1 (2003): 23–32.
Mirko S. Winkler et al., “Assessing Health Impacts in Complex Eco-epidemiological Settings in the Humid Tropics: Advancing Tools and Methods,” Environmental Impact Assessment Review 30, no. 1 (January 2010): 52–61.
A. M. Bal and I. M Gould, “Antibiotic Stewardship: Overcoming Implementation Barriers,” Current Opinion in Infectious Diseases 24, no. 4 (August 2011): 357–62; Bonnie M. Marshall and Stuart B. Levy, “Food Animals and Antimicrobials: Impacts on Human Health,” Clinical Microbiology Reviews 24, no. 4 (October 2011): 718–33.
Heather K. Allen et al., “Call of the Wild: Antibiotic Resistance Genes in Natural Environments,” Nature Reviews Microbiology 8 (April 2010): 251–59; V M. D’Costa, E. Griffiths, and G. D. Wright, “Expanding the Soil Antibiotic Resistome: Exploring Environmental Diversity,” Current Opinion in Microbiology 10, no. 5 (October 2007): 481–89.
R. H. Gustafson and R. E. Bowen, “Antibiotic Use in Animal Agriculture,” Journal of Applied Microbiology 83 (1997): 531–41; Mary D. Barton, “Antibiotic Use in Animal Feed and Its Impact on Human Health,” Nutrition Research Reviews 13 (2000): 279–99.
Mary J. Gilchrist et al., “The Potential Role of Concentrated Animal Feeding Operations in Infectious Disease Epidemics and Antibiotic Resistance,” Environmental Health Perspectives 115, no. 2 (February 2007): 313–16; Marshall and Levy, “Food Animals and Antimicrobials: Impacts on Human Health”; Andreas Voss et al., “Methicillinresistant Staphylococcus aureus in Pig Farming,” Emerging Infectious Diseases 11, no. 12 (December 2005): 1965–66; Allen et al., “Call of the Wild: Antibiotic Resistance Genes in Natural Environments”; H. Heuer, H. Schmitt, and K. Smalla, “Antibiotic Resistance Gene Spread Due to Manure Application on Agricultural Fields,” Current Opinion in Microbiology 14, no. 3 (June 2011): 236–43; M. F. Davis et al., “An Ecological Perspective on U.S. Industrial Poultry Production: The Role of Anthropogenic Ecosystems on the Emergence of Drug-resistant Bacteria from Agricultural Environments,” Current Opinion in Microbiology 14, no. 3 (June 2011): 244–50; Marshall and Levy, “Food Animals and Antimicrobials: Impacts on Human Health”; Maria Sjölund et al., “Dissemination of Multidrug-resistant Bacteria into the Arctic,” Emerging Infectious Diseases 14, no. 1 (January 2008): 70–72.
Stephen S. Morse et al., “Prediction and Prevention of the Next Pandemic Zoonosis,” The Lancet 380, no. 9857 (December 1, 2012): 1956–65.
Coker et al., “Towards a Conceptual Framework to Support One-Health Research for Policy on Emerging Zoonoses”; William B. Karesh and Robert A. Cook, “The Human-Animal Link, One World – One Health,” Foreign Affairs 84 (July/August 2005): 38–50; David Molyneux et al., “Zoonoses and Marginalised Infectious Diseases of Poverty: Where Do We Stand?,” Parasites & Vectors 4 (2011): 106.
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