BSE and variant CJD: Emerging science, public pressure and the vagaries of policy-making ☆ William D. HuestonCorresponding author contact information, E-mail the corresponding author Abstract Classical bovine spongiform encephalopathy (BSE) was first recognized in 1987 in the United Kingdom and ultimately spread to cattle across Europe and to the Middle East, North America and Japan through the movement of infected animals and contaminated meat and bone meal. The human expression of BSE, variant Creutzfeldt–Jakob Disease (vCJD), likewise was first identified in the UK and now has been observed in many countries due to human exposure to BSE contaminated products or to vCJD contaminated human tissues through transplantation and injection. BSE provides an example of an emerging infectious disease that demonstrates the challenges of policy-making in the face of rapidly changing science and public outrage pushing for action. Lessons learned through the BSE epidemic include: (1) beware of facts as new science continues to emerge; (2) complex issues rarely have simple solutions; (3) evaluate epidemics from a macro-epidemiologic perspective to understand their complexity and devise effective risk management strategies; (4) options always exist for prevention/control; (5) risk communications play a vital role before and during an emerging disease epidemic; and (6) risk management progress involves both science and politics. Adoption of One Health approaches involving systems thinking and shared leadership hold the most promise for effectively managing complex emergency global health issues like BSE. Keywords Bovine spongiform encephalopathy (BSE); Risk communication; Epidemiology; Policy-making 1. Introduction In 1989 the Chief Veterinary Officer of the USA asked me to organize a country-level risk assessment for Bovine Spongiform Encephalopathy (BSE), a new and emerging disease described 2 years earlier in the United Kingdom (Wells et al., 1987 and Wilesmith et al., 1988). Thus began my more than 20 years of active involvement with BSE as an epidemiologist, risk analyst, government policy-maker, consultant, expert witness, educator and communicator. Twenty years working at the interface of science, politics and beliefs provided me insights into the dynamics of policy-making where the science is continually changing and public pressure is pushing for government action. Six ‘lessons learned’ from BSE will be illustrated: beware of ‘facts’; complex issues rarely have simple solutions; evaluate epidemics from a macro-epidemiologic perspective; options always exist for prevention/control; risk communications play a vital role; and risk management progress involves both science and politics. These lessons learned illustrate some of the many challenges faced in responding to emerging infectious diseases of global concern. 2. Beware of ‘facts’ Bovine Spongiform Encephalopathy (BSE) is now recognized as a neuro-degenerative disease of cattle that also can affect a number of other ruminants, primates and humans. BSE is classified as one of a family of diseases of humans and other animals called transmissible spongiform encephalopathies. Our knowledge of BSE continues to evolve, hence the ‘facts’ of the disease change. Change is the norm for science; the scientific method is an ongoing process of data collection and testing of hypotheses. Counter intuitively, the scientific method does not prove facts; facts simply represent the prevailing hypotheses that have not been refuted. However, the scientific method of conjecture and refutation can be difficult to explain to non-scientists so that changes in the facts appear to undermine credibility in media communications and policy-making where well-intentioned spokespersons want to demonstrate certainty and convey that the situation is under control. Thus, scientific facts can be represented as dogmas when in fact they simply represent the best available hypothesis. The history of BSE demonstrates evolving science, where dogma was later disproven or revised as more evidence emerged on causation, host specificity and distribution. In 1987 when BSE was first recognized as similar histopathologically to scrapie in sheep, a ‘slow virus’ was the prevailing hypothesis regarding the etiologic agent of scrapie. Stanley Pruisners prion hypothesis (1982) was met initially by skepticism and ridicule – “proteins can’t cause infectious diseases”. Accumulated evidence from epidemiology and bench science ultimately corroborated the prion hypothesis, although this too may change in the future as more evidence is collected. Other examples of the evolving science refuting earlier facts include host specificity (“BSE is a cattle disease that does not affect humans”), transmission dynamics (“the minimum infective dose is X”) and the distribution of the disease (“Country X has no BSE” and “We won’t get BSE here…”). In each case, the prevailing scientific facts were rejected and replaced by a new working hypothesis as a result of more complete understanding of the disease and its dynamics. Current scientific knowledge is critically important for optimal prevention and control of emerging diseases. However, policy decisions cannot wait until all the relevant scientific questions are answered. The science of emerging diseases evolves rapidly, so much so that the rate of scientific discovery usually outpaces legislative and regulatory processes, resulting in situations where laws and regulations are based on outdated scientific knowledge. Caution must be exercised in creating prescriptive legislation and regulations, those that explicitly define the requirements and methods needed for compliance, even when the evidence appears indisputable. Descriptive policy instruments work better in the face of rapidly changing science. Descriptive policy instruments define the overall policy objectives and outline how scientific evidence will inform the policy implementation. Consequently, they provide flexibility to adapt as new evidence and understanding emerge. For example, specifying by regulation the exact diagnostic test, how samples are to be collected and the number of samples for a surveillance program fails to account for the continual progress being made in diagnostic tools and surveillance strategies. Describing the level of certainty needed by the surveillance system allows the utilization of new testing methods and surveillance designs as they become available. In the case of BSE, requiring that the surveillance system meet or exceed the international standards developed by World Organization for Animal Health allows the surveillance design and test methods to evolve as the global standards are updated. 3. Complex issues rarely have simple solutions While the disease BSE can be described fairly simply, control of the global BSE and related vCJD epidemic was complex. The etiologic agent of BSE may be described simply as prion particles but the determinants of the global BSE epidemic are numerous and include genetic improvement of cattle and the search for high quality protein sources, feed formulation and industry consolidation, and international trade of cattle and feed ingredients. The early epidemiologic investigations led by Wilesmith (1988) pointed to rendered animal protein product meal and bone meal as the primary transmission vehicle for BSE. Exquisite exposure experiments concluded that most BSE infectivity was concentrated in the cattle brain and spinal cord with lesser amounts in distal ileum and nerve bundles such as the spinal ganglia (Wells et al., 1998). Hence the simplest risk management strategy for cattle feed appeared to be prohibition of the use of cattle brain, spinal cord, spinal ganglia and distal ileum as raw material for rendering. While this was scientifically sound as a prevention strategy, it proved to be impractical. Complete removal of these specified risk materials from dead cattle is nearly impossible under commercial conditions. Further, no quick and reliable test was available to assure that the finished meat and bone meal (MBM) was free of these specified risk materials. Completely preventing cattle exposure to contaminated meat and bone meal has proven to be difficult once BSE is widespread in the population. Ultimately, prohibition of all mammalian meat and bone meal in ruminant feeds was implemented in the most affected countries until additional controls could be put in place such as segregating rendering facilities by raw material type so that only rendering facilities handling no ruminant raw materials could provide MBM for cattle feed use. Trade of infected cattle or contaminated MBM represents the largest risk for international spread of BSE. Early in the development of the global BSE epidemic many countries focused their attention on restricting imports of British cattle and MBM. Unfortunately, these simple control approaches provided false assurance to many countries. Restricting imports was complicated by three factors: (1) the lack of identification systems so that imported animals or MBM could be tracked, (2) transshipment of cattle and MBM through third countries, e.g., imports which entered from an intermediate country that had received them from the UK, and (3) the lack of test methods to assure the absence of ruminant-derived MBM from imported feedstuffs. Simple solutions are appealing because they can be explained easily and make intuitive sense. In practice, however, simple solutions rarely work effectively for complex problems. Often the purported simple solutions simply make the situation worse by creating a false sense of security. 4. Evaluate epidemics from a macro-epidemiologic perspective Livestock disease outbreak investigations tend to focus on the animal health issues alone. In the case of BSE and many other trans-boundary diseases, the dynamics of the disease also are affected by non-animal health issues like government structure, legal authorities, economics and trade. BSE spread widely across Europe in part because of the collective failure to understand all the systems involved from a macro-epidemiologic perspective. The livestock production system is interdependent on a wide array of other systems including animal feed, human food, medical devices, pet foods, industrial chemicals, pharmaceuticals, furniture (leather) and fashion (cosmetics) among others. While the initial animal disease response focused on the affected and exposed animals, it was these other systems that largely accounted for the global spread of the disease in animals and the exposure of humans. The animal feed system illustrates the need for a macro-epidemiologic perspective for the effective control and eventual eradication of BSE. Controlling the production and movement of MBM and its use in cattle feed proved even more challenging than tracking UK origin cattle exports. The rendering industry developed to transform an abundant source of raw materials (dead animals and offal) into high quality feed and fuel ingredients (MBM and tallow, respectively). Meat and bone meal proved to be the vector through which the BSE agent was spread across Europe because commercial rendering processes did not inactivate the agent completely. The use of MBM in animal feed was heavily dependent on its price relative to the price of alternative ingredients with similar nutrient values. Since feed accounts for the highest proportion of the cost of animal production, least-cost feed formulations have become the norm. The composition of specific animal feeds regularly changes with market conditions. When MBM was banned from ruminant feeds in the UK, its price dropped. Meat and bone meal continued to enter the marketplace after the ban because it was still legal for use in non-ruminant and poultry feeds. The price drop also affected the international movement of this feed ingredient. Since transportation costs factor into the cost of different feed ingredients, when the price at the production site drops, the MBM can be shipped further and still be competitively priced. After the ruminant feed ban, large batches of UK MBM were purchased by traders and moved internationally. Once the MBM entered the international marketplace, its identity of origin was very difficult to establish. Switzerland was one of the early continental European countries to find BSE in domestic cattle, despite their well-documented lack of either cattle or MBM importation directly from the UK; trans-shipped MBM of UK origin appears to be the source of BSE spread to Switzerland (Hornlimann et al., 1994). Macro-epidemiologic principles were applied in the development of risk assessment tools related to BSE. Analyzing relevant systems allowed countries to better understand their own risks for BSE and supported policy decisions on risk management strategies (Walker et al., 1991). Expanding the macro-epidemiologic framework to include the environmental fate of the BSE agent served as the foundation of quantitative BSE risk assessments (Comer and Huntly, 2003). These macro-epidemiological principles also were used to characterize the relative likelihood that a country would experience BSE (Heim et al., 2006). An early example of this type of assessment was the examination of 1985–1989 cattle export data from the UK. The number of cattle exported to the European Union member countries was compared to their number of reported cases of BSE (Schreuder et al., 1997). Countries that imported large numbers of British cattle during this period were considered highly likely to have introduced BSE into their domestic cattle regardless of their number of cases reported. 5. Options always exist for prevention and control One of the benefits of working with complex problems is the breadth of options that exist for making substantial progress in prevention and control. As BSE spread, prevention and control measures were considered on local, national and international levels. A number of stakeholders were engaged including government animal health and trade officials, producers and livestock industries, feed and food companies and consumers. While all countries wished to prevent spread of BSE, individual countries enacted an array of prevention and control strategies. The shared objective contributed to the global control of BSE, while individual measures were tailored to meet the macro-epidemiologic factors in that country, its political climate and funding available. The US approach to cattle imports from the UK provides an example of the identification of prevention options amid the dynamic interplay of science, legal authorities and politics. A 1991 assessment of the likelihood of BSE occurring in the US suggested that imported British cattle represented a clear risk (Walker et al., 1991). This risk assessment suggested that removing these imported cattle from the US animal feed and human food chains would be a sound strategy for reducing the risk of BSE. However, US Federal law at that time only allowed for ‘taking’ of animals if they were exposed or diseased or imported in violation of US requirements (Personal communication, Thomas E. Bundy). Since no ante mortem test existed for screening imported cattle for BSE exposure or infection and the cattle were not imported in violation of any law or regulation, the US Federal government could not require the destruction of any cattle from the UK even though the likelihood of their having been exposed was high. Through active engagement of state government officials and cattle producer organizations, alternatives were devised to accomplish much the same thing. Some states had broader authority to destroy animals deemed at risk and other states could issue ‘hold orders’ that prevented owners from moving animals to slaughter or rendering without prior approval. In other situations, cattle breed organizations stepped forward to purchase and subsequently destroy imported animals. The Federal government found a way to participate, supporting the States through cooperative funding agreements and buying other imported cattle ‘for research’ in order to move them to a laboratory for testing and destruction. Through this combination of activities, the risk of BSE introduction by UK imports was reduced. In contrast, Canadian law allowed for the complete destruction (or re-export back to UK) of all living UK imports after one of them was diagnosed with BSE in 1993. 6. Risk communications play a vital role Communicating about risk is difficult regardless of the circumstances. Understanding how humans perceive risk and the impact of stress on our cognitive abilities explains some of the difficulty. The science of risk communication has emerged as distinct from the one-way risk messaging over the last 30 years. The National Research Council characterized risk communication as “an interactive process of exchange of information and opinion among individuals, groups and institutions” ( 1989). Further, the NRC concluded that “risk communication is successful only to the extent that it raises the level of understanding of relevant issues or actions and satisfies those involved that they are adequately informed within the limits of available knowledge”. Trust and credibility are keys to effective risk communications and paradoxically, trust and credibility must be built among government agencies and key stakeholders before crises occur. It is difficult to establish trust and credibility in the face of an outbreak if no relationship already exists. Bovine spongiform encephalopathy provided a case study of risk communication failures and successes from the very beginning. The very nature of BSE fuels public confusion, anxiety and demands for action. The unique causative agent, subtle clinical signs, lack of live-animal diagnostic test and invariable fatal outcome of the disease makes BSE particularly difficult to explain. Furthermore, aggressive action does not lead to immediate results; even the most effective prevention strategies curtailing further exposure will take 4–5 years to be reflected in a downturn of new cases because of the long incubation period. The identification of variant Creutzfield–Jakob Disease (vCJD) in humans amplified the communication challenges. Three different applications of risk communication deserve special mention with regards to BSE: precaution advocacy, outrage management and crisis and emergency risk communication. The three relate to different situations with regard to the true hazard and the level of public outrage as described by Sandman (2012). The rapidly emerging science and competing hypotheses to explain the disease occurrence further complicated effective BSE risk communications. Risk communication efforts in the US regarding BSE provide a good example of the need for all three different types of risk communications. Precaution advocacy represents the situation where the risk is real but not recognized or acted upon by a particular stakeholder group. In the early 1990s, as the BSE epidemic raged in the UK, precaution advocacy was used with veterinarians and producer groups in the US to heighten recognition of the perils of the disease and stimulate critical stakeholders to take preventive action. Outrage management approaches were used a number of times with different audiences. For example, consumers were largely disinterested in BSE until the identification of vCJD in 1996 (Will et al., 1996). This new disease was described as affecting young people, incurable and ultimately fatal in all cases. The public response to the link between BSE and vCJD was huge as media pictures of hospitalized patients purportedly suffered ‘mad cow disease’ and families grieving the loss of a loved one were very evocative. While the true risk of vCJD in the US at that time appeared low, outrage about the disease threat was high. Outrage management approaches include active listening, acknowledgment and empathy with peoples fears (Sandman, 1993). In times of outrage, empathy and caring enhance the credibility of spokespersons more than recitation of facts or the expertise of the spokesperson. Only after the outraged publics have an opportunity to voice their concerns, can they be receptive to hearing the latest science about the issue. Active listening, therefore, is one of the most effective risk communication strategies for dealing with outrage. The discovery of BSE in Canada and the US in 2003 demanded a third type of risk communication-crisis and emergency risk communication. Producers, the food industry and consumers were all rightfully concerned and upset. The discovery identified a real risk to animal and human health and outrage was high. The key strategy for effective crisis and emergency risk communication is described by the US Centers for Disease Control and Prevention as “Be first, be right, be credible” (2008). In other words, the most effective strategy is to tell people what you know, what you don’t know, what is being done to answer outstanding questions, when you’ll get back to them with more information and, with the information currently available, what they can do to protect themselves, their families, their communities and their livelihoods. An excellent example of this strategy was provided by the Canadian Chief Veterinary Officer, Dr. Brian Evans, as he dealt with the identification of BSE in Canada in May 2003. Dr. Evans responded directly to the media as soon as the disease was confirmed, providing daily press conferences with unlimited access through teleconference for reporters to join and ask questions. Each day he would review what was known, acknowledge what still was not understood, provide an update on the investigations, share guidance for consumers, producers and the food industry and remind participants of the next press briefing. His openness and candor elevated his credibility and blunted any potential criticism of secrecy or cover-up. Risk communications play a critical role in the prevention and control of emerging diseases. Not only do effective risk communications build trust and credibility among key stakeholders and the relevant government agencies, they also heighten preparedness and support effective response in meeting the needs of both the responders and those affected. 7. Risk management progress involves both science and politics Emerging diseases like BSE are frightening. Public outrage and calls for action were fueled by scientific uncertainty regarding the cause and the potential impact of the disease. Policy-makers faced a difficult decision – whether to create policy based on incomplete science or wait until the facts were clearer. However, waiting was a policy decision in itself. History now demonstrates that those countries that waited too long to implement prevention and control measures suffered much higher number of BSE cases than those that acted early. The precautionary principle emerged to address these situations of scientific uncertainty in the face of emerging health issues, allowing policy makers to take actions based on potential risks while waiting for more evidence and a scientific consensus (UNESCO, 2005). While the precautionary principle usually is invoked in cases of potential risk to human health or the environment, a similar argument is made by other stakeholders who argue that the known impacts of a proposed policy change such as an import ban, feeding restrictions, or surveillance requirements must be weighed against the future impact of hypothetical risks. When proposed prevention actions are costly, the arguments become intense as both government officials and key stakeholders are concerned about who will pay and how. Effective prevention and control of BSE and vCJD involved costly measures like the feed bans and exclusion of high risk materials from the human food chain. The emerging understanding of BSE epidemiology and transmission dynamics in the early 1990s provided an opportunity for unaffected countries to enact these measures proactively. Countries with known or high likelihood of exposure could prevent the accumulation of large numbers of exposed livestock and humans by preemptive action before the first case of BSE was diagnosed. However, convincing key stakeholders to enact costly prevention measures in the absence of diagnosed cases of BSE was difficult. BSE presented an especially challenging situation because exposure typically precedes disease by 4 years or more. Risk analysis tools were developed in part to address this situation and explore alternative prevention approaches in order to determine which approach would achieve the greatest level of prevention in the shortest period of time and at the least cost. 8. Conclusion BSE and vCJD illustrate the challenge of formulating policy for emerging infectious diseases in the face of intense public pressure for action. The call for ‘science-based’ animal health policy has great appeal (Hueston, 2003). However, scientific ‘facts’ change rapidly for emerging infectious diseases. Public pressure may push for the definitive solution; however, official statements of certainty and prescriptive legislative or regulatory policy formulated on todays facts may be inappropriate tomorrow as a result of new scientific findings. Emerging infectious diseases are best handled with active risk communication and policies that outline the scientific objectives rather than the details of implementation in order to maintain flexibility. We learned many lessons from BSE: the role of risk assessment for identifying critical control points and comparing the effectiveness of different intervention strategies, the critical importance of risk communications, and the need for more robust legislation and regulatory authority for dealing with emerging infectious diseases. Many countries have successfully applied these lessons in a variety of settings. Argentina (Cané et al., 1991) and Canada used the US country BSE risk assessment (Walker et al., 1991) as a template for their assessments. These approaches evolved to become the geographical BSE risk assessments conducted by the European Community (Salman et al., 2012) and later the country risk assessment approach of the World Organization for Animal Health (2012b). Risk communications provide another excellent example as many countries learned from the positive and negative experiences of other countries when confronting BSE and vCJD. The US risk communication after the December 2003 BSE response benefited immensely from the vicarious learning gained from watching the Canadian response 7 months earlier. Finally, the experience of the US dealing with BSE in the 1990s reiterated a number of limitations of the animal health legislation existing at the time and added pressure for the passage of a new law in 2002, the Animal Health Protection Act. The global response to BSE is a success story as the disease is almost non-existent now. The UK, epicenter of the global classical BSE epidemic, registered only 7 confirmed cases in 2011 compared to the 37,280 cases in 1992 at the height of the epidemic there (World Organization for Animal Health, 2012a and World Organization for Animal Health, 2012b). The same pattern holds true for all countries where BSE has been identified. The numbers of vCJD cases have decreased dramatically also. The BSE saga clearly demonstrates the need for holistic and systems-based approaches to complex health issues at the interface of humans, animals and ecosystems. The BSE epidemic typifies a global problem that was so complex that no individual, organization or agency fully understood it. The issues were compelling and demanded attention and action, yet there was no simple technical solution. Much of the complexity of the problem related to the multiple systems involved including animal feed, cattle production, slaughter and meat processing, rendering of inedible offal, international trade of cattle, animal feed and feed ingredients, animal byproducts use, human tissue donation, waste disposal and environmental protection. Effectively managing all of these problems simultaneously required a different approach than used for technical problem-solving. Dealing with complex problems requires a One Health approach, working across disciplines using systems thinking and actively engaging all of the affected stakeholders. Since no individual or organization has the authority to address complex global issues like BSE, a shared leadership model also was necessary. National governments had to work with Intergovernmental Organizations as well as key domestic stakeholders, agriculture agencies had to work with public health and the environment, and the public sector had to work with the private sector and academia. Overall, BSE and other emerging disease issues require an adaptive leadership approach that responds as new scientific information is generated and as political realities surrounding an issue surface. Acknowledgement The author wishes to thank John Wilesmith, Gerald Wells, Danny Matthews, Kevin Walker, Stuart MacDiarmid, Philip Comer,and Peter Sandman for the collaborations that fueled these insights, and my colleagues at the US Department of Agriculture, Animal and Plant Health Inspection Service and Food Safety Inspection Service, the US Food and Drug Agency and the US Centers for Disease Control and Prevention who worked so diligently to apply these lessons. References Cané et al., 1991 B. Cané, E. Gimeno, J. Manetti, C. van Gelderen, E. Uiloa, A. Schudel Analysis of BSE risk factors in Argentina. Secretaría de Agricultura, Ganadería y Pesca de la Nación CentroGráfico, Buenos Aires (1991) CDC, 2008 Centers for Disease Control and Prevention (CDC) Crisis + Emergency Risk Communication (Basic) – Quick Guide (2008) emergency.cdc.gov/cerc/pdf/cerc_guide_basic.pdf (accessed 27.08.12) Comer and Huntly, 2003 P. Comer, P. Huntly TSE risk assessments: a decision support tool Stat. Meth. Med. Res., 12 (2003), pp. 279–291 View Record in Scopus | Full Text via CrossRef | Cited By in Scopus (23) Heim et al., 2006 D. Heim, I. Gardner, E. Mumford, U. Kihm Risk assessment and surveillance for bovine spongiform encephalopathy Rev. Sci. Tech. Off. Int. Epiz., 25 (2006), pp. 937–950 View Record in Scopus | Cited By in Scopus (7) Hornlimann et al., 1994 B. Hornlimann, D. Guidon, C. Griot Risk assessment for importing bovine spongiform encepahalopathy (BSE) Dtsch. Tierarztl. Wochenschr., 101 (1994), pp. 295–298 View Record in Scopus | Cited By in Scopus (18) Hueston, 2003 W. Hueston Science, politics and animal health policy: epidemiology in action Prev. Vet. Med., 60 (2003), pp. 3–12 Article | PDF (60 K) | View Record in Scopus | Cited By in Scopus (12) National Research Council, 1989 National Research Council, Committee on Risk Perception and Communication Improving Risk Communication National Academies Press (1989) Available at nap.edu/catalog/1189 (accessed 29.11.12) Pruisner, 1982 S. Pruisner Novel proteinaceous infectious particles cause scrapie Science, 216 (1982), pp. 136–144 Salman et al., 2012 M. Salman, V. Silano, D. Heim, J. Kreysa Geographical BSE risk assessment and its impact on disease detection and dissemination Prev. Vet. Med., 105 (2012), pp. 255–264 Article | PDF (426 K) | View Record in Scopus | Cited By in Scopus (3) Sandman, 1993 P. Sandman Responding to Community Outrage: Strategies for Effective Risk Communication American Industrial Hygiene Association (1993) Available at psandman.cm/media/RespondingtoCommunityOutrage.pdf (accessed 29.10.12) Sandman, 2012 P. Sandman Introduction to Risk Communication (2012) Available at petersandman/index-intro.htm (accessed 27.08.12) Schreuder et al., 1997 B. Schreuder, J. Wilesmith, J. Ryan, O. Straub Risk of BSE from the import of cattle from the United Kingdom into the countries of the European Union Vet. Rec., 141 (1997), pp. 187–190 View Record in Scopus | Cited By in Scopus (36) UNESCO, 2005 United Nations Educational, Scientific and Cultural Organization (UNESCO), World Commission on the Ethics of Scientific Knowledge and Technology The Precautionary Principle (2005) Available at unesdoc.unesco.org/images/0013/001395/139578e.pdf (accessed 29.10.12) Walker et al., 1991 K. Walker, W. Hueston, H. Hurd, J. Wilesmith Comparison of bovine spongiform encephalopathy risk factors in the United States and Great Britain J. Am. Vet. Med. Assoc., 199 (1991), pp. 1554–1561 View Record in Scopus | Cited By in Scopus (6) Wells et al., 1987 G. Wells, A. Scott, C. Johnson, R. Gunning, R. Hanoek, M. Jeffrey, M. Dawson, R. Bradley A novel progressive spongiform encephalopathy in cattle Vet. Rec., 121 (1987), pp. 419–420 View Record in Scopus | Cited By in Scopus (607) Wells et al., 1998 G. Wells, S. Hawkins, R. Green, A. Austin, Il Dexter, Y. Spencer, M. Chaplin, M. Stack, M. Dawson Preliminary observations on the pathogenesis of experimental bovine spongiform encephalopathy (BSE): an update Vet. Rec., 142 (1998), pp. 103–106 View Record in Scopus | Cited By in Scopus (256) Wilesmith et al., 1988 J. Wilesmith, G. Wells, M. Cranwell, J. Ryan Bovine spongiform encephalopathy: epidemiological studies Vet. Rec., 123 (1988), pp. 638–644 View Record in Scopus | Cited By in Scopus (417) Will et al., 1996 R. Will, J. Ironside, M. Zeidler, S. Cousens, K. Estibeiro, A. Alperovitch, S. Poser, M. Pocchiari, A. Hoffman, P. Smith A new variant of Creutzfeldt–Jakob disease in the UK Lancet, 347 (1996), pp. 921–925 Article | PDF (883 K) | View Record in Scopus | Cited By in Scopus (1837) World Organization for Animal Health, 2012a World Organization for Animal Health (OIE) BSE Portal (2012) Available at oie.int/animal-health-in-the-world/bse-specific-data (accessed on 27.08.12) World Organization for Animal Health, 2012b World Organization for Animal Health (OIE) Chapter 11.5. Bovine Spongiform Encephalopathy, Article 11.5.2 The BSE Risk Status of the Cattle Population of a Country, Zone or Compartment (2012) Available at oie.int/index.php?id=169&L=0&htmfile=chapitre_1.11.5.htm (accessed 29.10.12) ☆ This paper is based on a presentation given at the 2011 Schwabe Symposium honouring the legacy of Dr. Dale D. Hancock and held during the Conference of Research Workers in Animal Diseases (CRWAD), in Chicago, IL, USA. Corresponding author contact information Correspondence address: 4330 Springwood Drive, Free Union, VA 22940, USA. Tel.: +1 612 860 1305; fax: +1 612 624 4906.
Posted on: Thu, 22 May 2014 11:50:45 +0000
Trending Topics
Recently Viewed Topics
© 2015