Old Diseases, Emergent Diseases: The Evolution of Health in the Swine Industry
Published: July 24, 2008
By: P.R. Davies (BVSc, PhD) - Allen D. Leman Chair in Swine Health and Productivity, Department of Veterinary Population Medicine, College of Veterinary Medicine, University of Minnesota (XIII Congresso Brasileiro de Veterinários Especialistas em Suínos)
An Epidemic of Emerging Diseases?
Variability in disease patterns is an inherent feature of the "world of living things". From the biblical plagues to today's airport literature foretelling the next pandemic, we intuitively appreciate that the occurrence of diseases in plants and animals can fluctuate abruptly. Emerging diseases are defined as diseases that "have newly appeared in a population, or are rapidly increasing in incidence or geographic range" (Morse 2004).25 Out of curiosity I recently searched PubMED for reviews of "emerging disease" from 1965 to 1980 and was delivered only nine papers (with just two pertaining to infectious diseases). An identical search from 1995 (the year of the first volume of the Emerging Infectious Diseases journal) to 2007 yielded over 5600 reviews, and 473 when the word "infectious" was included. It is hard to believe that this torrent of publications about emerging diseases parallels any real shift that may have occurred in the rate of emergence (rather than detection) of novel or reemerging diseases. Many factors may have contributed to this (not the least being the ongoing expansion of scientific journals and fashions in medical writing), but recent experiences such as BSE, SARS and H5N1 influenza have reawakened the biomedical community to the intrinsic lability of biological systems.
Since the days of Koch and Pasteur we have compiled an impressive understanding of proximate causes of infectious diseases, and molecular biology has delivered "nanoscale" insight into mechanisms of disease in individual hosts. However, our understanding of what drives change in disease patterns at higher levels of aggregation (herds, regions, nations, global), and over longer timeframes, remains relatively rudimentary. The human trait of desire to control our destiny prompts questions about how anthropogenic activities have, and might, influence the history of disease, particularly in Homo sapiens and in those species of domesticated plants and animals with which we most closely coexist. During in the 20th century, phenomenal advances in biomedical disciplines brought a wave of optimism about man's power to employ modern science to subjugate nature. The wisdom of Hans Zinnser was overcome by enthusiasm among even the most learned:
- In 1962, Sir Macfarlane Burnet, Nobel laureate in medicine, stated "One can think of the middle of the 20th century as the end of one of the most important social revolutions in history - the virtual elimination of the infectious disease as a significant factor in social life".
- A US Surgeon General in the 1960s is widely cited to have stated "it is time to close the book on infectious diseases".
- In 1976, the Dean of Yale Medical School told students that "there were no new diseases to be discovered".
With the power of hindsight we know these declarations of victory have been shattered by the discovery of more than 30 new human pathogens, and most notably by the tragic impact of AIDS throughout the world. In North America, predictions about the future importance of infectious diseases of swine traced a similar path. In 1993, an eminent swine disease researcher predicted "knowledge of disease agents per se will continue to be of lesser importance to the profitability of pig farms" (Harris, 1993).16 Subsequently, persistent problems with hyperendemic viral diseases such as Porcine Reproductive and Respiratory Syndrome (PRRS) and the global emergence of Porcine Circovirus type 2 disease (PCVD) have ensured that infectious disease remains a preeminent concern for the industry. Other events such as the emergence of Nipah virus in Malaysia in 1998, the human Streptococcus suis epidemic in China in 2005, and the "high fever" PRRS related syndromes now devastating herds in China (Tian, 2007)37 and Vietnam suggest that perhaps the best we can hope for in swine health is a short term fragile equilibrium. Predictably, beyond pigs and people, there has also been a steady stream of reports of emerging diseases across the plant and animal kingdoms. As Zinnser would have told us, the unveiling of apparently novel diseases is more than a process of discovery of an existing reality. Genuine emergence of diseases as a function of changing ecological and epidemiological circumstances is an indelible element of our biosphere that seems to occur with unexpected frequency.(Walker 1996,39; Morris 2000,24 ; Woteki 200343) In this paper I will discuss some changes observed in the landscape of swine diseases over the last 20 years, focusing on the role of changing production practices in developed countries.
Models of Causation
Any discussion of disease emergence must be founded on a theory of causation. The dogma of the "germ theory" of disease, embodied in Koch's postulates, has nurtured much one-dimensional thinking about disease causation by focusing almost entirely on individual microbial agents and their interactions with the host. The current ease and accessibility of microbial sub-typing and nucleic acid sequencing methods has reinforced this perspective, furthering emphasis on the potential importance of genetic variation in agents, rather than other factors, in the occurrence of epidemics. Without disputing the huge benefits that "agent oriented" research has delivered for human and animal health, nor that genetic change in agents can be important in disease emergence (particularly for RNA viruses such as influenza and PRRS) much broader approaches are needed to understand population level phenomena and their evolution over time.
Multifactorial models of disease causation, embodied in the "host-agent-environment triangle", are now the staple of human and veterinary epidemiology courses. However, the "epidemiological triangle" model in its simple form still has some shortcomings as it does not explicitly incorporate temporal effects or relationships (such as the coevolution of host resistance and agent virulence and transmissibility), nor is it easily applied to complex systems (e.g. multiple host species and competing agents across diverse geographical areas). However it does convey the pivotal role of interactions between host, agent and environmental factors and their temporospatial relatedness (Morris, 2002).24 Changes to any of these components will cause shifts in disease incidence, severity or duration. The key to understanding the evolution of diseases is to understand the underlying ecological processes that cause observable changes in disease in populations. Apart from genetic diseases and toxicoses, there are few diseases (e.g., some vector borne and parasitic diseases) where our knowledge is sufficient to explain observed variation in incidence, severity or geographic range or to predict such changes. From a practical perspective, perhaps the most important step in pig production is to try and understand the impact on disease emergence of the management practices that we devise and implement.
The host-agent-environment triangle is also the standard causal model of researchers of plant diseases, who hold different perspectives regarding the relative importance of the host, agent and environment components in disease emergence (Anderson 2004,1 Scholthof 2007,34) While biomedical research is primarily focused on microbial agents and host-pathogen relationships at the "micro" level, in the plant world the environment is viewed as the predominant determinant of disease incidence (Anderson 2004).1 While the biomedical fraternity is heavily oriented towards "agent" research (particularly vaccines) to achieve control, the plant fraternity places relatively greater emphasis on host resistance and environmental effects. Anderson (2004)1 considered anthropogenic introduction of parasites (facilitated by trade and globalization), followed by severe weather events, to be the major driver of disease emergence in plants. Similar to the situation in animals, knowledge of emerging diseases of plants is largely confined to crop plants, and much less is known about wild plants. In both the plant and animal kingdoms, wild populations constitute poorly understood, but likely important, reservoirs for known and undiscovered pathogens (Scholthof, 200734; Bengis, 20043). Modern systems of pig production that minimize interspecies contact should reduce the risk of novel diseases arising through interspecies transmission.
Emergence Vs. Discovery - Origins and Impact of Nipah Virus and Hepatitis E Virus
Transmission of agents between species is recognized as an important trigger for disease emergence and most agents are potentially multihost pathogens. Consequently, until there is evidence to the contrary, all apparently novel agents are under suspicion as zoonotic agents. The range of potential outcomes (in terms of industry impact) from apparently novel diseases is exemplified in the scenarios surrounding the emergence of Nipah virus in Malaysia and the discovery of swine hepatitis E virus in the United States. These events took place almost concurrently but had very different outcomes for the respective industries. In 1998, a novel paramyxovirus (now known as Nipah virus) causing systemic infections in humans, pigs and other mammals emerged in northern Malaysia. A total of 265 human cases were identified, predominantly adult Chinese males having contact with pigs. The case fatality rate in humans was of the order of 40%, and some survivors suffered recurrent episodes of encephalitis (Tan, 200335). Fruit bats were identified as the natural reservoir hosts of the virus, and it appears that spillover of the endemic bat virus into the domestic swine population occurred due to a combination of ecological changes, and the open design of piggeries located adjacent to orchards. Fortunately, secondary human transmission did not occur and further human cases were prevented by elimination of the disease from pigs. However, despite any evidence for foodborne transmission of Nipah virus, the outbreak had devastating impacts on both domestic pork consumption and loss of exports to Singapore and Thailand valued at $120 million (Nor, 200026).
In contrast to the circumstances of "true" disease emergence with Nipah virus due to spillover between species, the circumstances for swine hepatitis E virus were those of discovery of an agent whose implications for animal and human health remain uncertain (Emerson, 200313; Meng, 200321). As hepatitis E viruses (HEV) cannot be easily isolated, their epidemiology is being unraveled with the contemporary tools of molecular biology, which have the power to both enlighten and confuse us. Variants of HEV (now categorized into 4 major genotypes) have been identified in a range of species across the world, with regional variability increasingly being documented (Meng, 200321; Wang, 200240; Meng, 200323). Infection of pigs is common in many countries, regardless of the frequency of clinical disease in humans. Some authors have inferred that "the risk of zoonotic transmission is rather low and currently of no practical consequence for food handling procedures (Koopmans, 2004).19 Recent evidence from full genome sequencing suggests that considerable variability exists between human and swine isolates of HEV (Inoue, 2006).17 There is certainly evidence indicating that people with occupational exposure to swine are more likely to be seropositive to these viruses (Drobeniuc, 200112; Meng, 200223; Bouwknegt, 20074) but increased risk of clinical disease in these groups has not been documented. Given the genetic diversity now being revealed in this group of viruses around the world, general statements about the zoonotic potential of HEV are probably unwise, and different animal reservoirs may harbour different viral genotypes (Drobeniuc, 200112; Wang, 200240). Current evidence suggests that the risk of direct or foodborne transmission of pathogenic HEV from pigs to people is extremely low, but any such events could have devastating impact on domestic demand for pork and trade access. There is some comfort in the fact that until now the zoonotic uncertainties during the early discovery phase of hepatitis E viruses in swine did not translate into food safety or occupational health paranoia. These examples raise important issues of risk communication regarding emerging diseases in food animal species. With increasingly powerful tools for detection, we can anticipate further "discoveries" of apparently novel agents whose pathogenic potential for pigs or people will at first be unknown. The capacity of industries to rapidly and effectively assess and communicate such risks is likely to become increasingly important to ensuring consumer confidence and market access for pork.
Industrialization of Swine Production - Implications for Disease Emergence
If we accept the environmental factors influence disease occurrence, it is inevitable that the dramatic changes witnessed in swine production systems of developed countries must have influenced disease patterns. Some of these changes [e.g., all-in/all-out (AIAO) management] were motivated precisely by the desire to improve herd health, while others (e.g., increasing herd size) were driven by other considerations and may have negative implications for herd health. It is important to remember that although modern confinement systems for pork production are increasingly uniform across many countries, specific practices remain diverse. Some of the key components that are likely to influence disease rates include herd sizes, population structure and dynamics; sources and health status of incoming stock; area density of pigs and other species; biosecurity practices; group sizes and animal density; replacement practices in breeding herds; pig flow (e.g., AIAO vs. continuous flow); housing systems; ventilation systems and air quality; sources, quality and delivery systems of feed and water; hygiene and effluent management; nutritional programs; weaning age; and health interventions (e.g., antibiotic use; vaccination). Some of the major innovations in swine health management are listed in Table 1. These developments were primarily directed at reducing the impact of endemic swine diseases and specific details are published elsewhere (Dial, 19929; Harris, 199917).
These changes to swine systems have reduced the impact of some important health problems. For example, sarcoptic mange and swine dysentery were once widespread problems that are very uncommon in modern systems. However, each of these strategies, probably with the exception of improved biosecurity, may have some negative or problematic consequences that collectively have opened the door to a different spectrum of diseases (Figure 1). The shifts we have seen in swine health in the last 20 years have been dramatic and primarily driven by anthropogenic changes to the environment and population dynamics of swine herds. However the role of these changes in the emergence of some major swine diseases (PRRS, PCVD) is unknown.
In most developed countries (and most food animal industries), evolution of production systems has occurred in concert with considerable industry concentration and specialization. Aside from the impact on pig health, the demographic changes in food animal populations have brought concerns related to potential for disease emergence, heightened epidemic risk and emergence of antibiotic resistance (Saenz, 200633; Gilchrist, 200715). The societal and environmental implications of concentration of animal production are also topical concerns that are beyond the scope of this discussion (Donham, 2000)11.
Figure 1.Health in balance: some examples of infectious diseases of swine that have increased or diminished in importance in the era of industrialized swine production in the USA.
Traditional farms typically reared multiple species, including pigs of various ages in continuous flow systems with often little attention to biosecurity measures (including purchase of pigs from markets and mixing of pigs from multiple sources). In the US today, most commercial swine farms typically do not raise other species; house larger numbers of animals; have less variability in animal age and immunity (e.g. specialized nursery and finishing sites); use AIAO management at room, barn or site level; and pay more attention to biosecurity. Multiple site production systems have enabled specialization of labor and strict segregation of pigs by age-group and source. However, these systems inherently involve considerable pig movement and facilitate rapid dissemination of agents across wide geographic areas. The state of Minnesota receives approximately 10,000 pigs per day from over 30 states and Canada (the largest source). Therefore these systems that were devised with the goal of improving individual herd health have augmented the risk of regional (and even international) spread with greater pig movements, particularly for those agents that appear to defy our best biosecurity efforts and spread locally among farms. Current biosecurity measures appear to have been generally more successful for constraining some bacterial diseases (with the notable exception of Mycoplasma hyopneumoniae) but less effective for viral diseases. Arguably the most problematic issue in swine health management today is the capacity of for local spread of viruses among farms (e.g. PRRS, Influenza, possibly PCV2) despite major investments in biosecurity. This issue has become magnified through the increasing use of boar studs as sources of semen. Despite major efforts to upgrade biosecurity in boar studs, recurrent problems with PRRS virus have required intensive monitoring of boars in an effort to rapidly detect introductions and avoid infection of recipient sow farms Reicks 200630; Reicks, 200631; Rovira, 200632). In Minnesota, where pig production is concentrated in areas of high farm density, filtration of incoming air is becoming a standard procedure in boar studs and is becoming increasingly considered as an option for sow farms, particularly during times of high risk (cooler months).
Among the unintended winners over the last 20 years, S. suis, H. parasuis, and L. intracellularis are essentially ubiquitous organisms that might be considered normal flora of pigs (certainly at the population level). Although on most herds these agents continue to cause predominantly sporadic problems, the risk of significant outbreaks appears to be much higher in modern systems. While it is not uncommon to see "stress" being attributed as the trigger for such diseases, outbreaks of these diseases often occurred on wellmanaged farms and in pigs with relatively high health status. Altered patterns of population immunity associated with changes in pig flow are an equally plausible explanation. One rationale for early weaning and AIAO systems was to reduce transmission of pathogens to young pigs. However, because these approaches did not exclude transmission, the net result was to delay exposure of many pigs to such endemic agents until later ages when disease outbreaks rather than sporadic cases were more likely. This hypothesis gains some support from observations that deliberate exposure of suckling pigs to S. suis or H. parasuis can reduce the risk of disease after weaning (Torremorell, 199938; Oliveira , 200127). Currently in the USA, although weaning ages would generally be considered young (18 - 21 days), there is a trend towards weaning older pigs. This is being driven by the realization that the increased breeding herd productivity (pigs weaned per sow per year) achievable with earlier weaning was more than offset by poorer performance in the growing phases (Main, 2002)20, together with the realization that the anticipated health benefits of earlier weaning were not being realized under most commercial conditions. Issues of unstable herd immunity are also implicated in difficulties in controlling PRRS virus in large herds with high rates of replacement.
The importance of herd size as a determinant of disease frequency and disease emergence is among the most discussed yet least researched questions related to modern commercial swine production. Much of the discussion is based on "first principles" along the lines that "as a general principle, the concentration of humans or animals in proximity enhances the potential for transmission of microorganisms among members of the group" (Gilchrist, 2006)15. Although "herd size" effects are commonly assumed, and in some cases have been demonstrated, the biological basis for such effects is typically poorly expounded in published studies (Gardner, 2002)14. Despite the theoretical concerns, over the last 15 years herd sizes in the USA have continue to increase, as have productivity levels. This apparent "defiance of gravity" may in part be attributed to the fact that increasing herd size has occurred in concert with management practices that have had positive benefits for herd health (e.g. AIAO management, age segregation, improved biosecurity, uniform sourcing of pigs). Such measures may have to some extent ameliorated health risks associated with larger populations, enabling producers to capture some benefits of scale in production without materially affecting overall herd health and productivity. However, the likelihood that larger herds are more at risk for introduction of agents transmitted by air (Gardner, 2002).14
May have contributed to the ongoing challenges faced by the US swine industry with respect to PRRS, influenza, and possibly PCVD. Readers seeking a more detailed discussion of the implications of herd size are referred to Gardner (2002).14
Emergence of Foodborne Pathogens and Zoonoses in Swine Production
Zoonotic agents comprise an estimated 60% of the known pathogens of humans (>1400), and about 75% of agents of "emerging" human diseases (Cleaveland, 2001).5 It has been proposed that most infectious diseases of man originated from pathogens of other mammalian species, and that this process was facilitated by domestication of animals for food and fiber production and other purposes Diamond, 1998).10 Unconditional acceptance of this paradigm has been questioned by Pearce-Duvet (2006)28 who concluded that the strongest evidence for a domestic-animal origin of human pathogens exists for measles and pertussis. For other pathogens, he considered the current evidence to be inadequate to support or refute the hypothesis of a domestic animal origin, and argued that there is evidence that transmission of some diseases (tuberculosis and taeniid worms) may have occurred from humans to domestic animals. Pearce-Duvet (2006)28 also surmised that while domestication of animals has played a role in interspecies disease transmission, more complex factors, particularly anthropogenic modification of the environment, are now of greater importance to disease emergence.
With respect to public health, arguably the most important swine zoonosis globally is Taenia solium, which is an emerging and serious problem in many poorer sectors of Latin America, Africa, and Asia (Phiri, 200329; Willingham, 200642). This disease in prevalent where pigs range freely, sanitation is poor, and meat inspection is absent or inadequate. It is strongly associated with poverty and backyard production, and has emerged to be a major problem in poor urbanized populations in Africa, particularly in regions where AIDS is widespread. Taenia solium is essentially absent from developed countries, and in the USA, modern confinement systems appear to offer advantages for control of some other foodborne zoonoses but not of others (Davies 1997;8 Davies 19987). Significant declines in the prevalence of Trichinella spiralis and Toxoplasma gondii in pigs in the USA appear to have resulted (based on temporal association and biological plausibility) from the implementation of management practices common to modern confinement systems (Davies 1998).7 Although human health risks of intensive swine production are regularly raised with respect to occupational health and adjacent environmental exposure (Cole, 20006; Thu, 200236; Saenz, 200633; Gilchrist, 200715), the long term implications at an ecological level have not been widely discussed.4 Referring specifically to the case of influenza, Webster (2002)41 pointed out that animal husbandry systems which incorporate biosecurity measures that reduce interspecies contact are likely to reduce the risk of disease emergence. In food animal production in developed countries, the progressive replacement of labor by capital (i.e., less direct human contact per animal produced) has occurred in association with increasing herd size (increased risk for intraspecies transmission) and specialization of enterprises (reduced rates of interspecies contact). In recent years, China and South-east Asia have retained the mantel as the global hot spot for emergence of novel zoonotic diseases arising from interspecies contact (e.g., SARS, new influenza strains, Nipah virus). In contrast, developed countries have predominantly witnessed the emergence of novel animal diseases characterized by high virulence in individual species but which appear to be relatively host specific (e.g., PRRS, PCVD, turkey poult enteritis syndrome, among others). Based on first principles, these trends are not surprising and more intensive systems of animal production may remain more likely to be troubled by emerging host-specific animal diseases than by novel zoonotic agents arising from interspecies transmission.
Summary
The challenge of meeting the food and fiber demands of the burgeoning human population is daunting. Expanding livestock production has been identified as a major cause of the world's most pressing environmental problems, including global warming, land degradation, air and water pollution, and loss of biodiversity (Anon, 2006).2 These concerns will need to be addressed in part by improving the efficiency of production. This has and will continue to drive production systems of commodity industries (as opposed to niche products from "alternative" systems in wealthier markets) further down the path of greater specialization, concentration and vertical integration. The relative importance of an animal species as a source of human disease is a function of the prevalence of zoonotic agents in that species and the probability of effective contact (direct or indirect) with susceptible humans. Clearly these factors vary dramatically among countries and regions, and changes in patterns of human and animal disease will continue to result from ecological changes at the human-animal interfaces, including changes in diet or methods of food preparation as well as changes in animal (intensification of production) and human (urbanization) demographics. In conjunction with consolidation of food industries and globalization, these factors will influence the risks of both emergence of diseases and their dissemination through trade. New production systems will continue to evolve and with them we will discover both benefits and unintended negative consequences for animal health and possibly human health. Pandora's Box of biological evolution will continue to spring new surprises with novel agents and ongoing advances in diagnostic technologies will bring previously unknown agents to light. This scenario has been with us for some time, and until now I believe the net results of our efforts have been in a positive direction. Productivity in swine production in developed countries has increased markedly without substantial negative events for human health but with continual challenges in maintaining pig health. This is not a battle that we will ever win, and just to stay in the fight we will need to continually upgrade our tools of surveillance, response, and risk assessment and communication so that pork remains a safe, affordable and acceptable food option for the future.
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