VETERINARY PUBLIC HEALTH

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In 1999, a study group on veterinary public health (VPH), convened jointly by the World Health Organization (WHO), the Food and Agriculture Organization of the United Nations (FAO), and the Office International des Epizooties (OIE), and including twenty-eight experts from eighteen countries, defined veterinary public health as "The contribution to the complete physical, mental, and social well-being of humans through an understanding and application of veterinary medical science."

The contribution of veterinary science to human health has been fundamental and sustained over millennia. It is not generally appreciated that this contribution pertains not only to livestock and food production, animal power, and transportation, which have laid the basis for most urban societies around the world. The study and management of animal diseases have also laid the basis for much of what is known about the dynamics and management of infectious human diseases, and has aided in the promotion of environmental quality.

Calvin Schwabe, one of the most important figures in veterinary public health in the twentieth century, has traced and documented the roots of the healing professions to healer-priests in the Nile Valley. Because cattle and horses were so important for sustainable food supplies, transport, and the military cohesion of ancient empires, these animals were very carefully observed and husbanded. In addition, the integrative view of healers in Egyptian and Greek cultures allowed lessons of comparative anatomy and diseases learned from the slaughter, hunting, and sacrifice of animals to be applied readily to the healing of primates. Even today, both human and veterinary medical practice draw upon the same pool of comparative, multispecies biomedical research.

RELATIONSHIPS TO PUBLIC HEALTH

If we narrow the focus of veterinary public health to those aspects that are directly pertinent to the practice of public health, rather than to human health in general, three broad areas of involvement become clear. Although these are sometimes characterized in historical terms, or in terms of "rich country-poor country" divisions, these different facets of veterinary public health are in fact ongoing, in complementary and often synergistic fashion, in most parts of the world.

Veterinary public health, in the first place, grows from its relationship to food production, usually by investigating and controlling animal diseases that threaten either food supplies or animal transportation and labor, which are essential elements in food production throughout much of the world. A second facet of veterinary public health relates to control of the transmission of zoonotic diseases, either directly or through foods. This is reflected in a wide array of activities, including research and control of infectious agents in meat and milk, rabies vaccination campaigns (both of wildlife and domestic animals), monitoring arboviruses and Lyme borreliosis in populations in wildlife, and hydatid disease control programs.

These first two facets are widely recognized as veterinary public health activities. The third facet, however, is less widely known. In many parts of the world, veterinarians, because of their knowledge of animal diseases, as well as the ecological, economic, and human cultural contexts of these diseases, have been instrumental in developing and implementing new methods of promoting sustainable public health that are ecosystemically grounded, culturally feasible, and economically realistic.

Many veterinary public health activities are reflected in the nature of veterinary involvement in public health institutions in North America and Europe. Veterinary activities involving disease control and health management in animal populations, and their integration of clinical, pathological, and epidemiological practices, often preceded similar activities in human medicine by decades, or, in some cases, centuries. It was in the area of food hygiene, however, that veterinary contributions to public health were first formally institutionalized. In Europe, particularly in Germany. veterinarians in the nineteenth and twentieth centuries were integral to the development of food hygiene laws and meat inspection systems, initially to curb large outbreaks of trichinosis.

In the aftermath of World War II. the U.S. Public Health Service's Communicable Disease Center, later named the Centers for Disease Control and Prevention (CDC) established a veterinary public health unit. James Steele, the first chief public health veterinarian in the CDC, was also active in promoting the veterinary public health unit in the World Health Organization. Martin Kaplan, another American veterinarian, became the first director of this unit. Both men expanded the traditional European emphasis on veterinary-directed food-safety programs to include investigations into the epidemiology and control of zoonoses. The 1960s and 1970s saw a reduced interest in veterinary public health, particularly in North America, because major infectious diseases were thought to be under control, and public health epidemiologists focused their efforts largely on chronic diseases such as heart disease and cancer. Although veterinarians were deeply involved in improving the understanding of these conditions by studying them in animal populations, many scientists and laypeople still had an image of veterinary public health practitioners as meat inspectors in a slaughterhouse. In 1975, the veterinary public health unit within the CDC was officially disbanded. Even during this time, however, several veterinarians were making strong contributions to public health through the CDC. Joe Held, a graduate of the Epidemic Intelligence Service of CDC, went on to become director of the National Institutes of Health Division of Research Services, Assistant Surgeon General, and director of the Pan American Zoonoses Center in Argentina .

Some within the CDC have argued that veterinary skills have been put to much broader use since the disbanding of the veterinary public health unit. In 1997, Peter Schantz, a veterinary parasitologist at CDC, documented that there were fifty-nine veterinarians at CDC assigned to eleven different centers, institutes, or program offices. Besides programs carrying out research and control of zoonotic diseases, veterinarians worked as epidemiologists and research scientists on other infectious diseases — including HIV/AIDS (human immunodeficiency virus/acquired immunodeficiency syndrome) — and on the national immunization program, environmental health, occupational health, and international health.

It was really only when infectious diseases began to reemerge as a global problem in the 1980s and 1990s that veterinary public health came back into prominence. This is largely because veterinary education, traditionally oriented to farm livestock, has been at the forefront of understanding the epidemiological features of infectious diseases in populations. It is no accident, for instance, that the protective effects for a population of vaccinating part of that population is termed a "herd effect." Furthermore, the wide scope of veterinary education lends itself well to studying and controlling zoonotic and food-borne illnesses, which became important areas of interest at the beginning of the twenty-first century.

Animal diseases may threaten human health in two ways: (1) they may threaten the animal populations that serve as food, transportation, or traction power in the fields; and (2) through zoonotic diseases, that are transmissable to humans.

NONZOONOTIC ANIMAL DISEASES OF PUBLIC HEALTH IMPORTANCE

Cattle plague, or rinderpest, which affects all cloven-hoofed animals, may serve as an example of how an epidemic disease in animals may have catastrophic effects on public health through a variety of indirect ways. The virus which causes rinderpest, related to canine distemper and human measles, was once endemic in Central Asia and made periodic forays into Europe, where it killed off tens of millions of cattle in the eighteenth century, despite strong quarantine measures, stimulating the creation of Europe's first veterinary schools. Rinderpest arrived in the lower Nile Valley with the British campaigns into the Sudan in 1884 through 1885. The prosperous cattle cultures further south, however, were initially protected by the Sahara Desert. Then, in 1889, the Italian army invading Eritrea brought cattle with them for provisioning. The disease then spread south in great devastating waves, killing millions of cattle and destroying the wealthy, cattle-based sub-Saharan civilizations. A third of the Ethiopian human population is estimated to have died as a result of this cattle plague. In what is today Tanzania, fewer than 5 percent of 4.5 million cattle survived. Villages disappeared, pastoral people were forced to become sedentary, and sedentary people lost their beasts of burden. About two-thirds of the Masai people starved to death. The way was opened up for European settlers and Bantu agriculturalists, who, of course, viewed their conquests as signs of superiority rather than as an exercise in carpet-bagging. One white South African source is quoted as saying that "the ravages of rinderpest, although reducing the native to poverty, has not been without beneficial results, and the native has now learnt humility to those to whom he is subordinate." Many wildlife species, especially large ungulates like buffalo, eland, giraffe, and kudu were decimated, and carnivores, deprived of their normal food, took to open attacks on people and other nonsusceptible species.

The disease also destroyed, initially, the natural hosts for tsetse flies, which spread blood-borne trypanosome parasites that cause sleeping sickness in people; the disease thus disappeared from wide areas of its historic habitat. Both wildlife and the scrub woodlands that support tsetse flies rebounded more quickly than the cattle and their associated grasslands. This created misconceptions among Europeans about the nature of African civilizations, the ecology of Africa in general, and about the zoonotic nature of sleeping sickness. Many sub-Saharan African ecosystems have, at different points in history, self-organized around wildlife-woodland species and cattle-grassland species. Current conservation efforts have been directed to conserve the wildlife-woodland system, which is also more hospitable to tsetse flies and endemic sleeping sickness. This is one of many examples where the veterinary activities, if allowed to take their appropriate place alongside ecologists and human health practitioners, can make profound contributions to our understanding of sustainable public health.

More recently, the public health effects of major epidemics of such nonzoonotic animal diseases as foot-and-mouth disease and both classical and African swine fever have been buffered and softened by social and economic safety nets, as well as rapid veterinary, public health, and economic responses.

ZOONOSES

The second way in which animal diseases may be of importance for public health is when the agents that cause them can be transmitted to people. The World Health Organization (WHO) defines zoonoses as "those diseases and infections, [the agents of] which are naturally transmitted between [other] vertebrate animals and [people]." This is a good, clear definition, and includes most of the diseases, such as rabies, brucellosis, tuberculosis, Q Fever, Lyme disease, salmonellosis, hydatid disease and sleeping sickness, which are conventionally viewed as being zoonoses. However, this definition is often stretched to include many infections that people share with other animals, either directly or indirectly. In some cases (such as histoplasmosis and blastomycosis), animals create conditions which allow the disease organisms to proliferate more easily. This broader net also includes other animal-associated illnesses — such as allergies — as well as the beneficial effects of animal ownership, ranging from lowered blood pressure and survival after heart attacks to serving as substitute social networks in time of crisis for elderly people.

Most often, humans are accidental hosts of zoonotic agents. The exceptions are some tapeworms, such as Taenia solium. Taenia saginata. and Diphyllobothrium latum. for which humans are the definitive host. In these cases, the agent is recycled back to people when they ingest meat from pigs, cattle, and fish, respectively, which have had the misfortune of ingesting infested human feces. These diseases are clearly tied to public hygiene measures as well as animal feeding practices.

Zoonoses may be classified according to their maintenance cycles. Direct zoonoses, such as leptospirosis, hantaviruses, and anthrax, may be perpetuated in nature by a single vertebrate species. Cyclozoonoses have maintenance cycles that require more than one vertebrate species, but no invertebrates. Echinococcus multilocularis. a tapeworm of canids that goes through intermediate stages in ruminants or omnivores, is an example. Metazoonoses require both vertebrates and invertebrates, such as ticks or mosquitoes, to complete their life cycle. American trypanosomiasis (Chagas disease, spread by triatomid "kissing bugs"), Lyme Disease (spread by deer ticks), plague (spread by rat fleas), and leishmaniasis (Kala-Azar, spread by sand flies) are metazoonotic diseases.

Saprozoonoses depend on inanimate reservoirs or development sites, such as soil, water, or plants, as well as vertebrate hosts. Toxoplasmosis, a single-celled intestinal parasite of cats which requires days to weeks in the environment to develop into an infective larval stage, and which infects people either through environmental contamination or through undercooked meat, is one example. Toxocara canis and T. catis. which exist as roundworm infections in dogs and cats, require an external environment to become infective for people. Children pick these larvae up in contaminated playgrounds and develop visceral larva migrans (VLM) or ocular larva migrans (OLM) when the larval forms move through the human body. Finally, mycotic infections such as blastomycosis, which can spend their entire life cycles externally, are also examples of saprozoonoses.

FOOD-BORNE ZOONOSES

After a half century of seeming to be under control, food-borne diseases reemerged in the 1980s as a major class of human infections. Most of the agents associated with the current worldwide increases in cases of food-borne diseases — Salmonella DT 104; Salmonella enteritidis ; Escherichia coli 0157:H7; Campylobacter jejuni ; Listeria monocytogenes ; and the prions associated with bovine spongiform encephalopathy (mad cow disease) and its human form, new variant Creuzfeldt-Jakob disease (nvCJD) — have their reservoirs in animal populations. In most cases, they cannot be controlled without a full, multispecies understanding of the food chain, from "stable to table." Veterinary public health has therefore become a much more active field of inquiry and activity than it was in the mid – twentieth century.

The reasons for the global increases in food-borne diseases are complex, and have revealed weaknesses in how modern agriculture is organized. Industrialized agriculture tends to encourage economies of scale to keep prices down, and large groups of animals are often gathered into one place. Poultry and swine are often kept in large groups throughout their lives. Cattle may be kept in a dispersed manner when young, but are then gathered into large feedlots for fattening. Since the conditions which promote epidemics are a function of the size of the susceptible population and the probability of adequate contact (itself a function of

the agents and the methods of spread), these large populations of animals are vulnerable to epidemic diseases. In an attempt to control this vulnerability, veterinarians have worked closely with various livestock industries to set up "herd health" or "flock health" programs. When these have broken down — as all programs eventually do, especially those requiring high labor, energy, or educational inputs — there have been catastrophic epidemics of diseases such as hog cholera, salmonella, or foot-and-mouth disease. But these economies of scale have also created epidemic conditions for agents which may not only affect the livestock themselves.

No matter how they are kept, most livestock, or livestock products such as milk, are processed in centralized facilities. At some point in the modern food system, the bacteria and viruses from a wide variety of sources are brought together in one place. This allows not only for cross-contamination, but for wide dispersal of the agents so gathered, since these centralized processing industries must, in order to remain economically viable, serve large populations.

The biological effects of these economies of scale have been exacerbated by the economic pressure to become more efficient; hence animal "wastes" (organs and parts of animals not considered fit for human consumption) have been reprocessed (rendered) into protein supplements (meat and bone meal, or MBM) through various heat and chemical processes. These allow animals to grow faster or produce more milk. Economically, this seems to make sense. Ecologically, however, this has created ideal conditions for the spread and enhancement of food-borne illnesses. Well before the epidemic of BSE in Britain in the 1980s and 1990s, salmonellosis was known to increase and be magnified throughout the food system through the synergistic effects associated with scale and efficiency.

The epidemic of BSE in the United Kingdom had several contributory factors. Not the least of these was a large ratio of sheep (40 million, compared with 8 million in the United States) to cattle (12 million, compared to 104 million in the United States). Furthermore, there was a high prevalence of scrapie-infected sheep in the United Kingdom (scrapie is a well-known but little understood transmissible spongiform encephalopathy of sheep). Thus, in the United Kingdom, rendered animal protein was 14 percent sheep-derived, compared to 0.6 percent in the United States, and much of the sheep-derived MBM came from scrapie-infected sheep. Then, in the late 1970s, changes in the economic value of tallow and fats and deregulation of the rendering industry affected the proportion of MBM processed with hydrocarbon fat solvents, which fell from about 70 percent in the mid-1970s to about 10 percent in the early 1980s. It is hypothesized that this helped create conditions which allowed infective prions to slip through the system.

The BSE epidemic not only clarified some of the weaknesses in how post – Word War II agriculture was organized. It also uncovered some structural problems in the relationships between veterinary and human public health. The first cases of BSE in cattle were reported in 1986. Within two years, it became clear that there was a serious epidemic of a new disease in cattle underway, and a series of well-designed veterinary epidemiological studies were done. As the epidemic unfolded, the emphasis shifted between concerns for BSE as an animal disease, to BSE as a public health, economic, and sociopolitical problem. Although the epidemic was brought rapidly under control through various draconian measures, the lack of formal structures to link these various concerns in a systemic manner has been costly not only in terms of lives lost to nvCJD, but also through the broad, preventable, public health impacts mediated through economic and agricultural restructuring. Public health workers have tended to view transmissible spongiform encephalopathies (TSEs) such as CJD as rare, geographically widespread, and species-specific. However, those who worked with animal TSEs such as scrapie saw them as endemic in many countries, with evidence that they were capable of crossing species barriers. An integrated veterinary public health system might have made much earlier use of this information.

As indicated earlier, Salmonella epidemics in poultry had identified the recycling of animal proteins back into animal feeds for reasons of efficiency as problematic even before the BSE epidemic. Similarly, the use of antimicrobials in animal feeds — again for reasons of efficiency and cost — had underlined the fact that there could be serious public health consequences to such practices. There was evidence in the 1970s that feeding of antimicrobials to animals for growth promotion or as prophylaxis could promote the spread of resistant bacteria. What also became apparent was how easily bacteria can share genetic coding for resistance, and the degree to which resistance to various drugs might be linked. An understanding of the ecology of microbial populations in the food chain has improved, even as new strains of multidrug resistant bacteria, such as Salmonella DT 104, have emerged as serious human pathogens in North America and Europe. The links between microbial ecology, veterinary practices, and public health have made this an increasing area of concern for veterinary public health practitioners.

OTHER ZOONOSES

If agricultural activities have created epidemic conditions for food-borne diseases and problems with antibiotic resistance, they have also contributed — along with land use and climatic and cultural changes — to creating ecological conditions suitable for a range of other zoonoses. Among these, arboviruses — small, simple RNA viruses carried by arthropods (insects, spiders, crustaceans) — are particularly sensitive to changes in habitat and climate. Arboviruses multiply in the arthropods, which transmit them between vertebrate hosts. Thus, the incidence and spread of infection is sensitive to increases in standing water (mosquito breeding sites), which can be caused by irrigation systems as well as increased rainfall and temperature due to global climate changes. Hence, they often appear in seasonal epidemics. The feeding habits of the mosquitoes (whether they favor one host, or switch according to availability) are also important. For many of these viruses, small mammals and birds act as important reservoirs because they provide a steady supply of new, susceptible hosts.

Of the 535 arboviruses catalogued, some 100 are known to cause human illness, ranging from general fevers and muscle and joint pain to hemorrhagic symptoms and encephalitis. Many of these also cause similar illnesses in domestic animals. Large, long-lived vertebrates may actually serve to slow an epidemic since they develop strong immunity and, because they tend to develop low-level viremias, are not considered an important source of reinfection for other animals. These include various equine encephalitis viruses, which have been well studied for decades, such as those associated with Western, Eastern, and St. Louis Encephalitis; as well as others, like West Nile virus, that emerged as major concerns (at least in Europe and North America) at the turn of the millennium. They also include the agents of Rift Valley fever, yellow fever, and Japanese encephalitis. Even dengue fever, which is transmitted by the yellow fever mosquito Aedes aegypti. may have its origins in a treetop jungle cycle between wild primates and sylvatic mosquitoes.

The relationships between emerging infectious diseases and global environmental change have been stimulated not just by arboviral infections. At least two direct zoonoses — hantavirus pulmonary syndrome and leptospirosis — are sensitive to these changes. A few years ago, few people outside of military circles had ever heard of hantaviruses. Military people knew about them because they caused epidemic hemorrhagic fevers and kidney problems for troops in South Korea. Over three thousand United Nations personnel were infected. Indeed, this version of the disease has been reported around the world for many decades. Only in 1993, when a new version of the disease seemed to emerge in the American southwest, did something approaching panic spread through the medical community. This illustrates a global rule of disease emergence: diseases are important if politically or economically powerful people deem them to be so.

Being associated with drought, floods, and plagues of rodents, the story of hantavirus pulmonary syndrome has strong biblical resonances. In the spring of 1992, six years of drought in the Four Corners region of the southwestern United States ended in torrential rains. In the wake of the floods came pi ñ on nuts and grasshoppers, and then a plague of deer mice. In one year, the deer mouse population increased tenfold, bringing the little creatures into much closer contact with farmers and other rural residents. By the time the mouse population started declining in 1993, forty-two people had succumbed to an illness that started with fever, nausea, and vomiting and ended, for twenty-six of the forty-two, with fluid in the lungs, and then death. This emergence of hantavirus pulmonary syndrome demonstrated that the disruption of ecosystems, whatever the cause, was not merely an "environmental" issue.

In many ways, hantavirus infection is similar to leptospirosis. Both are associated with spiral-shaped bacteria that prosper in warm moist places like kidneys and bladders. Neither of these diseases require a flea or other invertebrate to help complete their life cycle. The difference between hantaviruses and leptospires is that the leptospiral bacteria can survive longer in the environment, and thus are more likely to be directly affected by changes in temperature and rainfall patterns as a result of global environmental changes. Leptospirosis is believed to be the mystery killer disease which appeared in Nicaragua in 1996 after extensive flooding. Both leptospires and hantaviruses, however, are spread through rat urine and its aerosolized forms and both are closely associated with agricultural and military occupations that demand intensive meddling in restructured natural environments where rats make their homes. Hantaviruses may have started as pathogens of poor housing conditions and poverty, but the North American middle-class infatuation with visiting, or living in, "natural landscapes" has spread these agents to all socioeconomic levels.

Concern with food-borne and other emerging infectious diseases, many of which are zoonotic, has certainly broken down many barriers between veterinary and "mainstream" public health. The presence of veterinary epidemiologists at international public health conferences is no longer considered an aberration. Veterinarians are active in most public health departments in industrialized countries. ProMED, the important international electronic list-serve for reporting emerging infectious diseases, brings plant, animal, and human reports into one forum. Veterinary epidemiologists and pathologists, together with human health researchers and ecologists, have characterized many of the environmentally and agriculturally related public health problems of importance in the twenty-first century. All of these trends point to a return to the roots of "one medicine" as practiced by the great poly-mathic biologists of the nineteenth century. But these new activities take comparative medicine one step further, as they consider the ecological and cultural contexts in which diseases occur.

ECOSYSTEM-BASED VETERINARY PUBLIC HEALTH

Arboviruses and other wildlife and environmentally related zoonoses have renewed interest among veterinary public health practitioners in ecology and medical geography, and in techniques of investigation, analysis, and presentation involving spatial statistics and geographic information systems. These, combined with new environmental management techniques, have resulted in several innovative initiatives to promote public health through ecosystem-based approaches. The Network for Ecosystem Sustainability and Health, an international network of researchers from a variety of disciplines and communities, has had strong veterinary involvement from the beginning, as has the International Society for Ecosystem Health. The Center for Conservation Medicine links the veterinary college at Tufts University with Harvard Medical School and the Wildlife Preservation Trust. A nationally coordinated professional veterinary elective in ecosystem health was developed in 1993 and delivered jointly by the four Canadian veterinary colleges. From the point of view of understanding and promoting public health in a sustainable fashion, these integrative initiatives were long overdue.

Veterinary public health, growing from an orientation toward animal populations, and chastened by economic limits, has always drawn strongly on epidemiological methods of investigation and control. Before the twentieth century, many of these methods were based on various ecological observations, as well as military and agricultural necessity. As early as the fourth century, Marcus Terrentius Varro, observing diseases of livestock in Rome, noted that "there are bred [in swamps] certain minute creatures which cannot be seen by the eyes, which float in the air and enter the body through the mouth and nose and cause serious disease." Based on this kind of understanding, population-health management, quarantine, mass treatments, and mass vaccinations were a well-developed method of controlling animal diseases well before they became standard public health practices.

The International Society for Veterinary Epidemiology and Economics (ISVEE) symposium brings together every three years researchers and frontline workers from around the world who deal with the ecological and cultural dynamics of zoonotic and animal diseases that affect public health. As the global public health movement matures, one can only hope that veterinary and nonveterinary public health practitioners can be more openly integrated into new organizational frameworks that take advantage of their complementary and synergistic understanding of what it means to create healthy and sustainable human communities on earth.

David Waltner-Toews

(see also: Bovine Spongiform Encephalopathy; Centers for Disease Control and Prevention; Climate Change and Human Health; Ecosystems; Emerging Infectious Diseases; Epidemics; Epidemiology; Food-Borne Diseases; International Health; Prions; Salmonellosis; Vector-Borne Diseases; Zoonoses )

Bibliography

Palmer, S. R.; Soulsby, L.; and Simpson, D. I. H. (1998). Zoonoses: Biology, Clinical Practice, and Public Health Control. Oxford, UK: Oxford University Press.

Schwabe, C. W. (1978). Cattle, Priests, and Progress in Medicine. Minneapolis: University of Minnesota Press.

— — (1994). Veterinary Medicine and Human Health, 3rd edition. Baltimore, MD: Williams & Wilkins.

Van Leeuwen, N. N. O. and Waltner-Toews, D. (1998). "Ecosystem Health: An Essential Field for Veterinary Medicine." Journal of the American Veterinary Medical Association 212:53 – 57.

Waltner-Toews, D. (2001). "An Ecosystem Approach to Health and its Applications to Tropical and Emerging Diseases." Cadernas de Sa ú de Publical Reports on Public Health 17 (Supp.):7 – 22.

See also the journal Emerging Infectious Diseases at http://www.cdc.gov/ncidod/eid/ and the World Health Organization at http://www.who.int. where veterinary public health activities are integrated into various parts of the site.

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