Incursions of foot-and-mouth disease virus into Europe between 1985 and 2006.

Foot-and-mouth disease (FMD) is one of the biggest threats to animal health in European countries. In the last 22 years (1985-2006), FMD has occurred 37 times in 14 European countries. Serotype O was most frequently involved in these outbreaks followed by A, C and Asia 1. Sometimes, epidemics were very limited and at other times, they were the cause of devastating economic losses. In most cases (22/37), the origin of the outbreaks could not be determined. For some of these outbreaks, however, routes of introduction and spread were identified through epidemiological inquiries. Moreover, in some cases, the origin of the virus was also traced by phylogenetic analysis of the partial or complete sequences of VP1 genes. Lessons learned from the outbreaks are still useful as most of the same risk factors persist. However, efforts made by FMD-free countries to help those where the disease is endemic are a valuable strategy for the reduction of the global risk. The present and the future potential sources of FMD infection need to be identified to best focus European efforts.

Epidemiological patterns of foot-and-mouth disease worldwide.

Foot-and-Mouth Disease (FMD) is a clinical syndrome in animals due to FMD virus that exists in seven serotypes, whereby recovery from one sero-type does not confer immunity against the other six. So when considering intervention strategies in endemic settings, it is important to take account of the characteristics of the different serotypes in different ecological systems. FMD serotypes are not uniformly distributed in the regions of the world where the disease still occurs. For example, the cumulative incidence of FMD serotypes show that six of the seven serotypes of FMD (O, A, C, SAT-1, SAT-2, SAT-3) have occurred in Africa, while Asia contends with four sero-types (O, A, C, Asia-1), and South America with only three (O, A, C). Periodically there have been incursions of Types SAT-1 and SAT-2 from Africa into the Middle East. This paper describes the global dynamics for the seven sero-types and attempts to define FMD epidemiological clusters in the different regions of the world. These have been described on a continent by continent basis. The review has reaffirmed that the movement of infected animals is the most important factor in the spread of FMD within the endemically infected regions. It also shows that the eco-system based approach for defining the epidemiological patterns of FMD in endemic, which was originally described in South America, can apply readily to other parts of the world. It is proposed that any coordinated regional or global strategy for FMD control should be based on a sound epidemiological assessment of the incidence and distribution of FMD, identifying risk sources as either primary or secondary endemic eco-systems.

Planning for the progressive control of foot-and-mouth disease worldwide.

In the wake of on-going successful programmes for global eradication of rinderpest and the current effort to contain the spread of avian influenza, the progressive world-wide control of FMD must be regarded as a major contribution to the international public good. FMD is the single most animal disease constraint to international trade in animal products. Its control is relevant, on the one hand, to protecting the livestock industries of industrialised countries and, on the other, to the livelihoods and income generation of developing countries, where, as a general rule, FMD continues to be endemic. The strategy that is advocated in this paper is one that is based on progressive risk reduction of FMD in the context of progressive market access of livestock commodities from developing countries. It is suggested that FMD control should be linked to improvement in livelihoods of livestock dependent communities in the FMD endemic settings. It is expected that this in turn will lead to increasing demand for effective national veterinary services and disease surveillance. This strategy has also taken lessons from the global rinderpest eradication programme and regional FMD control programmes in Europe and South America. The strategy that is advocated for the progressive control of FMD in the endemic settings is based on a seven stage process within a horizon of about 30 years, namely: (1) Assessing and defining national FMD status; (2) instituting vaccination and movement control; (3) suppressing virus transmission to achieve absence of clinical disease; (4) achieving freedom from FMD with vaccination in accordance with the OIE standards; (5) achieving freedom from FMD without vaccination in accordance with the OIE standards; (6) extending FMD free zones; and (7) maintaining FMD Freedom. Concomitant with progressive FMD control, there needs be the encouragement of such risk reduction measures as in-country commodity processing in order to encourage regulated trade in livestock commodities without unduly increasing the risk of disease spread. Finally, the progressive control of FMD should also be seen as part of reducing the overall, world-wide threat of infectious diseases to human health and economic development.

The epidemiology of peste des petits ruminants in Pakistan and possible control policies.

Peste des petits ruminants made its first clinical appearance in Pakistan during an epidemic in Punjab Province in 1991, but its level of activity in subsequent years was never systematically recorded. In 2003, 2004 and 2005 teams trained in participatory disease surveillance methods visited a large number of villages throughout Pakistan to record the prevalence and impact of key livestock diseases. Peste des petits ruminants has emerged from their study as a common and economically damaging disease of small ruminants within the country, appearing to be endemic in the north of Punjab and epidemic in Azad Jammu and Kashmir, and Sindh during the study period. It should be possible to reduce the incidence level using a combination of zoosanitary measures and the intensive use of vaccine.

Mass vaccination and herd immunity: cattle and buffalo.

The design of effective programmes for emergency response to incursion of epizootic diseases of cattle, for exclusion of such diseases and for implementation of progressive control in enzootic situations leading to eventual virus elimination, is currently largely empirical. This needs to be remedied to provide more cost-effective use of vaccines and more effective control. At population level, protective effects of immunisation can extend well beyond the individual, influencing the dynamics of viral propagation within the whole population, non-vaccinated as well as vaccinated. This concept of herd immunity and application of the resulting epidemiological principles, combined with experience gained from disease control programmes such as the Global Rinderpest Eradication Programme has much to offer in designing effective science-based control programmes. This paper explores practical exploitation of the herd immunity principle by considering some of the factors which militate against mass vaccination achieving effective levels of herd immunity and, with these in mind, suggesting ways to optimise the efficiency of mass vaccination programmes.

Participatory epidemiology in disease surveillance and research.

Participatory epidemiology is the application of participatory methods to epidemiological research and disease surveillance. It is a proven technique which overcomes many of the limitations of conventional epidemiological methods, and has been used to solve a number of animal health surveillance and research problems. The approach was developed in small-scale, community animal health programmes, and then applied to major international disease control efforts. The Global Rinderpest Eradication Program adopted participatory epidemiology as a surveillance tool for controlling rinderpest. This approach was subsequently used in both rural and urban settings in Africa and Asia, for foot and mouth disease, peste des petits ruminants and highly pathogenic avian influenza. Participatory disease surveillance has made an important contribution towards controlling both rare and common diseases. This paper reviews the principal applications of participatory epidemiology and highlights the lessons learned from field applications. In addition, the authors examine future challenges and consider new areas for research.

A heterogeneous population model for contagious bovine pleuropneumonia transmission and control in pastoral communities of East Africa.

Pastoral cattle live in highly structured communities characterized by complex contact patterns. The present paper describes a spatially heterogeneous model for the transmission of contagious bovine pleuropneumonia (CBPP) developed specifically for pastoral communities of East Africa. The model is validated against serological data on the prevalence of CBPP infection in several communities of southern Sudan and against livestock owner information on community structure, livestock contact and cattle exchange. The model is used to assess the impact of alternative control strategies including mass and elective vaccination programmes, potential treatment regimes and the combination of vaccination and treatment in a single unified strategy. The results indicate that the eradication of CBPP using mass vaccination with currently available vaccines is unlikely to succeed. On the other hand, elective control programmes based on herd level vaccination, treatment of clinical cases or a combination of both vaccination and treatment enabled individual livestock owners to capture a large benefit in terms of reduced animal-level prevalence and mortality experience. The most promising intervention scenario was a programme which combined the vaccination of healthy animals with treatment of clinical cases.

Origin and evolution of highly pathogenic H5N1 avian influenza in Asia.

Outbreaks of highly pathogenic avian influenza caused by H5N1 viruses were reported almost simultaneously in eight neighbouring Asian countries between December 2003 and January 2004, with a ninth reporting in August 2004, suggesting that the viruses had spread recently and rapidly. However, they had been detected widely in the region in domestic waterfowl and terrestrial poultry for several years before this, and the absence of widespread disease in the region before 2003, apart from localised outbreaks in the Hong Kong Special Autonomous Region (SAR), is perplexing. Possible explanations include limited virus excretion by domestic waterfowl infected with H5N1, the confusion of avian influenza with other serious endemic diseases, the unsanctioned use of vaccines, and the under-reporting of disease as a result of limited surveillance. There is some evidence that the excretion of the viruses by domestic ducks had increased by early 2004, and there is circumstantial evidence that they can be transmitted by wild birds. The migratory birds from which viruses have been isolated were usually sick or dead, suggesting that they would have had limited potential for carrying the viruses over long distances unless subclinical infections were prevalent. However, there is strong circumstantial evidence that wild birds can become infected from domestic poultry and potentially can exchange viruses when they share the same environment. Nevertheless, there is little reason to believe that wild birds have played a more significant role in spreading disease than trade through live bird markets and movement of domestic waterfowl. Asian H5N1 viruses were first detected in domestic geese in southern China in 1996. By 2000, their host range had extended to domestic ducks, which played a key role in the genesis of the 2003/04 outbreaks. The epidemic was not due to the introduction and spread of a single virus but was caused by multiple viruses which were genotypically linked to the Goose/GD/96 lineage via the haemagglutinin gene. The H5N1 viruses isolated from China, including the Hong Kong SAR, between 1999 and 2004 had a range of genotypes and considerable variability within genotypes. The rising incidence and widespread reporting of disease in 2003/04 can probably be attributed to the increasing spread of the viruses from existing reservoirs of infection in domestic waterfowl and live bird markets leading to greater environmental contamination. When countries in the region started to report disease in December 2003, others were alerted to the risk and disease surveillance and reporting improved. The H5N1 viruses have reportedly been eliminated from three of the nine countries that reported disease in 2003/04, but they could be extremely difficult to eradicate from the remaining countries, owing to the existence of populations and, possibly, production and marketing sectors, in which apparently normal birds harbour the viruses.

Patterns of spread and persistence of foot-and-mouth disease types A, O and Asia-1 in Turkey: a meta-population approach.

Despite significant control efforts, foot-and-mouth disease (FMD) persists in Turkey, and new strains of serotypes A, O and Asia-1 are periodically reported to enter the country from the east. The status of FMD in Turkey is important regionally because the country forms a natural bridge between Asia where the disease is endemic, and Europe which has disease-free status. This study analysed spatial and temporal patterns of FMD occurrence in Turkey to explore factors associated with the disease's persistence and spread. Annual records of FMD distribution in Turkish provinces throughout 1990-2002, grouped by serotype (O, A and Asia 1), were analysed using geostatistical techniques to explore their spatial and temporal patterns. A meta-population model was used to test how disease status, expressed in terms of presence/absence, extinction, and colonization, and measured at the province level throughout the periods 1990-1996 and 1997 2002, could be predicted using province-level data on: ruminant livestock numbers; meat production-demand discrepancy (as a surrogate measure of animal and animal products marketing, i.e. long-distance contagion through the traffic of mainly live animals to urban centres); and the disease prevalence distribution as recorded for the previous year. A drastic overall reduction in FMD occurrence was observed from the period 1990-1996 to 1997-2002 when the disease was shown to retract into persistence islands. FMD occurrence was associated with host abundance, short distance contagion from adjacent provinces, and meat production-demand discrepancies. With FMD retracting into identified provinces, a shift in predictors of FMD occurrence was observed with a lower contribution of short-distance contagion, and a relatively higher association with meat production-demand discrepancies leading to live animal transport over long distances, and hence presenting opportunities for identifying critical-control points. The pattern of persistence differed according to serotype groups and is discussed in relation to their differential affinity to cattle and small ruminant hosts.

A model of lineage-1 and lineage-2 rinderpest virus transmission in pastoral areas of East Africa.

The development of a stochastic, state-transition model of rinderpest transmission dynamics is described using parameter estimates obtained from both laboratory and participatory research. Using serological data, the basic reproduction numbers for lineage-1 rinderpest virus in southern Sudan and for lineage-2 rinderpest virus in Somali livestock were estimated as 4.4 and between 1.2 and 1.9, respectively. The model predictions for the inter-epidemic period in Sudan and Somalia (1.2 and 4.2 years, respectively) were in agreement with analysis of livestock-owner reports (1-2 years and 5 years, respectively).

Experience with eradicating rinderpest by vaccination.

Rinderpest was such a devastating disease throughout Africa, Asia and Europe, capable of shaping the destinies of governments as well as the livelihoods of producers and consumers alike, that all sectors of society demanded that scientists should strive to develop a means of protecting cattle against the constant risk. The history of vaccination as a tool for the control of rinderpest is a long one but finally spawned a vaccine which certainly ranks highly among the safest and most efficacious of vaccines. Having this Tissue Culture Rinderpest Vaccine (TCRV) available generated aspirations of global rinderpest control and even eradication, which could now be considered feasible.

Use of participatory epidemiology in studies of the persistence of lineage 2 rinderpest virus in East Africa.

In 1994, rinderpest virus of African lineage 2 was detected in East Africa after an apparent absence of more than 30 years. In 1996, a disease search, based on participatory epidemiological techniques supplemented by serological and virological analyses, was undertaken in southern Somalia and north-eastern Kenya to collate past and current epidemiological information about rinderpest-compatible disease events, and to test the hypothesis that African lineage 2 rinderpest virus persists in populations of transhumant cattle in the Somali ethnic areas. The findings in Afmadu in Lower Juba led the search for rinderpest to the communities in the Bardera area and then on to the Kenya/Somalia border areas between Mandera and El Wak. The herders had a specific knowledge of the clinical signs of rinderpest and provided detailed and accurate descriptions of cases. They differentiated between classical acute rinderpest and a milder syndrome characterised by an ocular discharge and diarrhoea, few oral lesions, corneal opacity and occasional mortality. The studies provided evidence for the endemic occurrence of rinderpest back to at least 1981, with a periodicity of five years in the incidence of the disease. After a period of high mortality in 1992 to 1993, around Afmadu, herders reported a mild disease, with occasional increases in mortality, from other areas of Lower Juba and the Gedo Region. Reports by herders of a rinderpest-compatible disease in the El Wak area were pursued until active cases were located and rinderpest was confirmed.

Rinderpest surveillance performance monitoring using quantifiable indicators.

This paper describes an objective system of monitoring the performance of disease surveillance. The system was developed through dialogue with a number of countries in Africa and adopted as part of the Global Rinderpest Eradication Programme of the Food and Agriculture Organization of the United Nations. The performance monitoring system uses a clinical stomatitis-enteritis case definition, an outbreak investigation classification scheme, and a series of eight performance indicators to measure the sensitivity, specificity and timeliness of the surveillance system. Field-testing indicates that the approach is successful when good record-keeping is practiced and highlights the importance of dialogue in helping to ensure that the system is simple and acceptable. The system provides a quantitative measure of the efficacy of national disease surveillance programmes and of the quality of data derived from such programmes for use in international disease control, animal health information exchange and trade risk analysis.

The control of rinderpest in Tanzania between 1997 and 1998.

In January 1997, Tanzania requested international assistance against rinderpest on the grounds that the virus had probably entered the country from southern Kenya. Over the next few months, a variety of attempts were made to determine the extent of the incursion by searching for serological and clinical evidence of the whereabouts of the virus. At the clinical level, these attempts were hampered by the low virulence of the strain, and at the serological level by the lack of a baseline against which contemporary interpretations could be made. Once it became apparent that neither surveillance tool was likely to produce a rapid result, an infected area was declared on common-sense grounds and emergency vaccination was initiated. The vaccination programme had two objectives, firstly to prevent any further entry across the international border, and secondly to contain and if possible eliminate rinderpest from those districts into which it had already entered. On the few occasions that clinical rinderpest was subsequently found, it was always within this provisional infected area. Emergency vaccination campaigns within the infected area ran from January to the end of March 1997 but were halted by the onset of the long rains. At this time, seromonitoring in two districts showed that viral persistence was still theoretically possible and therefore a second round of emergency vaccination was immediately organized. Further seromonitoring then indicated a large number of villages with population antibody prevalences of over 85%. These populations were considered to have been 'immunosterilized'. Although no clinical disease had been observed in them, it was decided to undertake additional vaccination in a group of districts to the south of the infected area. Serosurveillance indicated that rinderpest could have been present in a number of these districts prior to vaccination. Serosurveillance in 1998 suggested that numerous vaccinated animals had probably moved into districts outside the infected and additional vaccination areas, but did not rule out the continued presence of field infection.

Emerging diseases of Africa and the Middle East.

The term "emerging diseases" has been used recently to refer to different scenarios, all of which indicate changes in the dynamics of disease in the population. Of the OIE List A diseases, major changes have been experienced with rinderpest, peste des petit ruminants (PPR), contagious bovine pleuropneumonia (CBPP), foot-and-mouth disease, African swine fever, lumpy skin disease, and Rift Valley fever. Rinderpest represents a success story of the 1990s, thanks to the programs of the Pan African Rinderpest Campaign (PARC). The situation has changed from that of the 1980s when rinderpest was widespread throughout most of Tropical Africa and the Middle East. PPR is a disease that has become of increasing importance throughout Tropical Africa and the Middle East. CBPP, which had previously been reduced to sporadic incidence within endemic areas, invaded new areas, causing heavy mortality. African swine fever has extended to West Africa and to Madagascar, in both regions resulting in heavy losses. Climatic changes in both East and West Africa were associated with an upsurge of Rift Valley fever. Deficiencies in national veterinary services have contributed to failures in early detection and response; in many regions investigation and diagnosis services have deteriorated. The continuing structural adjustment program for national veterinary services will need to take into account their transformation from providers of services (e.g., vaccinations, medicines) to inspection and quality assurance services. Surveillance, early warning, and disease emergency preparedness will need to be pursued more vigorously in Africa and the Middle East as vital components of national veterinary services.

Dealing with animal disease emergencies in Africa: prevention and preparedness.

Emergency preparedness planning for animal diseases is a relatively new concept that is only now being applied in Africa. Information can be drawn from numerous recent disease epidemics involving rinderpest, contagious bovine pleuropneumonia (CBPP) and Rift Valley fever. These examples clearly demonstrate the shortcomings and value of effective early warning with ensured early reaction in the control of transboundary animal disease events. In concert, the Food and Agriculture Organization (FAO), through the Emergency Prevention-System for Transboundary Animal and Plant Pests and Diseases (EMPRES), and Organisation of African Unity/Inter-African Bureau for Animal Resources (OAU/IBAR), through the European Commission-funded Pan-African Rinderpest Campaign (PARC), have been actively promoting the concepts and application of emergency preparedness planning and should continue to do so under the proposed successor of PARC, namely: the Pan-African Programme for the Control of Epizootics (PACE). The potential partnership between the normative function of the FAO in developing and promoting emergency preparedness and the implementation of improved national and regional disease surveillance by PACE and other partners could witness the commencement of more progressive control of epidemic diseases in Africa and greater self-reliance by African countries in coping with transboundary animal disease emergencies.

Disease prevention and preparedness: the Food and Agriculture Organization Emergency Prevention System.

In 1994, the Food and Agriculture Organization undertook to revitalise its activities in the control of transboundary animal disease by establishing a new special programme known as the Emergency Prevention System (EMPRES) against transboundary animal and plant pests and diseases. The emphasis of the EMPRES livestock component is placed on pre-empting outbreaks and losses experienced by agriculture through the enhancement of local capacity to detect and react rapidly to plague events. EMPRES concentrates on the co-ordination of the Global Rinderpest Eradication Programme--a time-bound eradication programme--whilst addressing the progressive control of the most serious epidemic diseases within a broad framework of emergency preparedness. Programme activities are discussed in relation to early warning, early reaction, facilitating research and co-ordination. In addition to rinderpest, particular attention has been paid to contagious bovine pleuropneumonia, a re-emerging disease in Africa targeted for strategic attention, and foot and mouth disease, for which co-ordinated regional control in Latin America and South-East Asia has been initiated. Tactical responses to other disease emergencies such as African swine fever, classical swine fever (hog cholera), Rift Valley fever, peste des petits ruminants and lumpy skin disease are described.

Rinderpest: a case study of animal health emergency management.

The history of rinderpest and control of the disease in Africa and Asia is reviewed briefly. The present distribution of rinderpest virus in relation to its phylogenetic lineages is presented. Rinderpest-free countries bordering rinderpest-infected countries are considered to be under permanent threat of a transboundary rinderpest incursion and therefore face continuous and serious emergency situations. The nature of these emergencies in relation to the remaining foci of the three lineages is described. It is argued that the Global Rinderpest Eradication Programme (GREP) eradication strategies now need to focus on the use of epidemiological studies to define foci of infection and guide targeted, pulsed vaccination campaigns rather than broad, routine vaccination. The emergency posed by the re-emergence of African lineage 2 virus in East Africa and the challenge of mild rinderpest is explored in some detail as a phenomenon which may be more widespread than has been assumed. Points at which the future of GREP is threatened are illustrated and means of removing some of the dangers are suggested. The lessons which need to be learnt from the experience of the Indian National Project on Rinderpest Eradication and the Pan-African Rinderpest Campaign are discussed, including the value of strengthening surveillance systems in accordance with the Office International des Epizooties Pathway and how to cope with the problem associated with cryptic foci of rinderpest persistence--perhaps the greatest challenge facing GREP. The value of vaccine buffer zones is considered in detail and the authors conclude that unless those zones are of considerable depth and are well maintained, they are unlikely to prevent dissemination of the virus. The role of emergency preparedness planning in preventing the spread of rinderpest is discussed, with the understanding that effective surveillance, as a component of emergency preparedness planning, is safer than vaccination as a means of ensuring that the disease does not re-enter or penetrate a population. The swift initiation of a programme for the eradication of rinderpest from Pakistan is seen as the key issue in dealing with the Asian lineage rinderpest emergency. Development and implementation of strategies with the benefit of experience gained in Africa and India could provide a rapid resolution of the emergency.