The Veterinary Journal 1999, 158, 613 Article No. tvjl.1998.0338, available online at http://www.idealibrary.

com on

Review The Role of Small Ruminants in the Epidemiology and Transmission of Foot-and-Mouth Disease
P.V. BARNETT and S.J. COX Institute for Animal Health, Pirbright Laboratory, Ash Road, Pirbright, Working, Surrey, GU24 0NF, UK

SUMMARY Despite representing the largest part of the worlds foot-and-mouth disease (FMD)-susceptible domestic livestock, sheep and goats have generally been neglected with regard to their epidemiological role. This is partly due to the often inapparent nature of the disease in these hosts. Nevertheless, their ability to become carriers represents a reservoir for further infection and spread of disease, and so trade of live sheep and goats present a major risk of entry of FMD to disease-free countries. Research and epidemiological studies continue to be necessary in order both to prevent the entry of the virus and to assist in control should the disease reoccur. This review concentrates primarily on more recent studies relating to sheep and goats and, in particular, considers the importance of these hosts in the overall epidemiology of FMD. KEYWORDS: Foot-and-mouth disease; sheep; goats; epidemiology; transmission.

INTRODUCTION Foot-and-mouth disease virus (FMDV) is the causal agent of a highly contagious illness of more than 33 domesticated or wild species of animals. In comparison to other agriculturally important species, studies on sheep and goats have been very limited. Only in the last 30 years have small ruminants gained any prominence experimentally, and readers are referred to the reviews by Sharma (1981) and Pay (1988), and the recommendations made at the XIII Conference of the Permanent Commission on Foot-and-Mouth Disease of the Office International des Epizooties (Anon., 1972), which highlighted the possible risk of spread of FMD from sheep and goats. The disease has a wide spectrum of clinical signs

Correspondence to: Dr P.V. Barnett at the above address. Tel: +44 1483 232 441; Fax: +44 1483 236 430 1090-0233/99/040006 + 08 $12.00/0

(Geering, 1967; Littlejohn, 1970; Sharma, 1981; Pay, 1988) which are probably influenced by the virus strain, the breed of sheep or goat and to some extent by the environment (Geering, 1967). There is, however, general agreement that the disease in naturally acquired infections often takes on a milder form in small ruminants than in cattle and pigs, and in many cases may be vague. Incubation is commonly between 3 and 8 days. Fever, anorexia and lassitude have been observed, and lameness occurs in the presence or absence of foot lesions. Such lesions are in the interdigital cleft, along the coronary bands and on the bulb of the heels. Hoof shedding sometimes happens in sheep. Oral lesions are less common than on the feet and have often disappeared by the time foot lesions appear. When they occur, they are likely to be on the posterior aspects of the dorsum of the tongue rather than the tip, being more necrotic than vesicular, or on the dental pad. Such mouth lesions, which are
1999 Baillire Tindall

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generally small, can also be distributed inside the upper lip and on the lower gums, although these sites are rarer. Occasionally, sloughing may occur, leaving haemorrhagic ulcers. Lesions may also occur on the teats, vulva, prepuce and rumenal mucosa. The disease in goats can be even milder. Lameness and agalactia (Nazlioglu, 1972) are the most common signs, although some outbreaks have been recorded in which pyrexia, nasal discharge and salivation were observed (Pay, 1988; Shukla et al., 1974). Mouth lesions are more likely to occur in goats (Olah et al., 1976). Mortality is often seen in lambs and kids in the absence of any clinical signs and is generally the result of myocarditis or myocardial lesions (Geering, 1967; Pay, 1988). In some parts of the world, such as Australia, New Zealand, North America, Chile, the Patagonian region of Argentina and parts of Europe, which have large sheep populations, FMDV could be economically catastrophic in terms of lost productivity, restrictions on international trade, cost of vaccination and other control measures. The adoption by the European Union (EU) of a nonvaccination policy for the control of FMD, to allow greater movement of livestock and their products within the Single Market (Directive 90/423/EEC), and increase trade with other FMD-free regions (Donaldson & Doel, 1992; Davies, 1993) also leaves the European domestic livestock population highly susceptible to FMD should the virus be introduced. Recent outbreaks of FMD within and around the EU (Leforban, 1996; Kitching, 1998) serve as reminders of the threat of FMD. EPIDEMIOLOGY Although some areas of the world with large sheep and goat populations, such as Australia, New Zealand, North America and parts of South America, continue to remain free from FMD, the disease is endemic or sporadic in many of the countries of Asia, Africa and Eastern Europe (Kitching, 1998). During the late 1980s and early 1990s an epidemic spread across North Africa from Libya and Tunisia to Morocco. The virus, type O, is believed to have originated from the Middle East and to have had predilection for sheep (Taylor & Tufan, 1996). Outbreaks also occurred in Turkey during 1995 and 1996 (Kitching, 1998), in which 20% of the total cases were associated with sheep and goats (Taylor & Tufan, 1996). As recently as

1996, the Balkan countries of Albania, Former Yugoslav Republic of Macedonia and Former Republic of Yugoslavia experienced a type A epidemic that also involved small ruminants (Leforban, 1996). A stamping out policy was adopted and ring vaccination implemented in Albania in which a total of 137 190 sheep and 61 101 goats were vaccinated together with 59 234 cattle and 7422 pigs. In the Former Yugoslav Republic of Macedonia, only cattle were vaccinated. In recent years, Great Britain and most other EU Members have been free from FMD, the exceptions being Italy, which reported 57 outbreaks in 1993, and Greece, which had epidemics in 1994 and 1996 (Kitching, 1998). The 1994 Greek epidemic originated from the movement of infected sheep from the island of Lesvos. The causal agent was a type O, similar to endemic strains in the Middle East. A total of 95 outbreaks were finally recorded. The epidemic was controlled by stamping out and movement restrictions. No evidence of a predilection of the strain for sheep and goats (as seen in the Middle East) was recognised, as cattle present on affected premises showed high morbidity. During the course of the outbreaks, 12 450 sheep, 4738 goats, 1241 cattle and 139 pigs were killed, but no vaccination was implemented. Thirty-nine outbreaks of FMD type O also occurred in Greece during 1996, probably as a consequence of the illegal importation of live sheep from Turkey. Approximately 5000 sheep and goats, 1800 cattle and 30 pigs were destroyed from clinically affected flocks/herds or following contact with infected animals. These outbreaks serve to demonstrate several important points; firstly, the role of the Middle East as a reservoir of FMD, and the potential for spread from the region (via Eastern Europe and countries that border the Mediterranean to the rest of Europe); and secondly, the probable role of sheep and goats in disease transmission (88.4% of the regions livestock are small ruminants; Anon., 1993). The large number of live animal imports into the Middle East from FMD endemic areas results in the frequent introduction of new strains of virus (Yadin & Cloudia, 1995). Strains that circulated during the 1990s seemed to have a predilection for sheep and goats although they spread into the dairy herds, in spite of regular vaccinations (Kitching, 1994). Studies in Nigeria (Obi & Newman, 1988) and South America (Fernandez A. et al., 1975; Fernandez T. et al., 1975), where communal farming of cattle, sheep and goats also

THE VETERINARY JOURNAL, 158, 1

occurs, identified a high prevalence of antibodies against the virus-infection-associated (VIA) antigen (indicative of active infection with FMDV rather than vaccination) in sheep and goats in the absence of clinical signs. This suggests that small ruminants have an important role in the epidemiology of FMD elsewhere in the world. Owing in part to the threat to Europe posed by outbreaks in North Africa and the Middle East, the desire for up-to-date information on the current disease situation, and to establish the significance of small ruminants in the epidemiology of FMD infection, several recent serological surveys have been carried out in Morocco (Mackay, 1994; Mackay & Rendle, 1996) and Greece (Mackay et al., 1994). Ten-thousand sera samples were collected from unvaccinated sheep and goats throughout Morocco in 1992, when FMDV was widespread. Overall prevalence of infected flocks was determined to be 29%. Prevalence was lower in an area where vaccination had taken place, suggesting that prophylaxis had an influence in reducing the spread of disease. A further survey carried out during 1995 reported that the number of seropositive animals had decreased from 18.4% reported in 1992 to 7.6%. Herds which practised transhumance or were nomadic had a higher prevalence than fixed herds. Moreover, those herds in which infection had been previously recorded also gave a higher prevalence of seropositivity (22.2% as opposed to 6.2%). Herds which had been previously vaccinated (pre-November 1993) were not shown to have an increased prevalence of seropositive animals, thus ruling out the possibility that the antibody detected was due to vaccination. These results suggest that since the last reported case of clinical FMD in Morocco in September 1992, FMD virus had been persisting at a low level in the absence of clinical disease. It is unlikely that this low seroprevalence is either an under- or over-estimate of seropositive animals, as a liquid phase blocking ELISA (Hamblin et al., 1986), a reliable, sensitive and reproducible assay (Haas, 1995), was used throughout these surveys. Another survey conducted in Greece during 199495 also supports the occurrence of low-level, subclinical infection, as small clusters of sheep continued to be identified as seropositive several months after the last clinical case had been reported. The killing of seropositive animals did not prevent subsequent seroconversion of animals on the same holding. It was concluded that further

work was necessary to validate the findings of these surveys and establish whether seropositive flocks represent a real danger in terms of virus spread. Additionally, there have been several reports of animals known to have been exposed to FMDV, under experimental conditions, not seroconverting (Gibbs et al., 1975; Donaldson & Kitching, 1989). Other methods of identifying animals which have contracted the virus and which may still be virus positive should therefore be used, wherever possible, in conjunction with serology. The development of serological tests that reliably distinguish antibody produced following infection from that due to vaccination together with information relating to the rate of spread of FMDV within and between flocks, which is currently under investigation (P. Kitching, personal communication), will greatly assist epidemiological studies and the development of control strategies. VIRAL PERSISTENCE No attempts were made to recover virus from the sheep in the above serological surveys, but many workers have reported that the carrier state can be established in sheep and goats after recovery from disease and in vaccinated animals exposed to virus. The duration of the carrier stage in small ruminants, however, is shorter than that in cattle (Burrows, 1968; McVicar & Sutmoller, 1969). During the acute phase of the disease, virus is present in most tissues and organs and high quantities of virus are excreted. In the carrier animal, virus is restricted to the pharyngeal area (soft palate and tonsils) and the amounts excreted are relatively very low. McVicar and Sutmoller (1969) demonstrated virus for up to 9 months following intranasal exposure to FMDV, and Burrows (1968) recovered virus from sheep oesophageal-pharyngeal (OP) fluids between 15 months post infection. Virus recovery from carriers is often intermittent and of low titre (Salt, 1993). Consequently, the role of persistence in natural disease spread has remained elusive. Some studies have reported a low incidence of carrier sheep and goats (Garland et al., 1981; Anderson et al., 1976; Yadin & Cloudia, 1995; Fondevila et al., 1996), suggesting that these animals play an insignificant role in disease transmission. On the other hand, other studies refute this (Sharma et al., 1981; Gurhan et al., 1993; Hancock & Prado, 1993). When considering any studies relating to persistence and the carrier state,

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the methods of virus detection and their sensitivity must be considered. Tissue culture techniques are superior to mouse inoculation methods, and cell cultures vary in their sensitivity. Bovine thyroid cells are the most sensitive cells for detecting FMDV (Straver et al., 1970; Khukhorov et al., 1973; Gurhan et al., 1993). However, successful virus isolation from OP samples is highly dependant on competent sampling, suitable storage and rapid delivery to the laboratory, and is constrained because of the presence of neutralizing antibodies to FMDV in the sample (De Clercq et al., 1997). Alternative methods of detection, such as an antigen detection ELISA and/or PCR, which do not rely on live virus, may prove more useful and reliable in establishing the extent of viral persistence in sheep and goats. A recent study by De Clercq et al. (1997) showed the advantage of an RT-PCRELISA in confirming the presence of FMDV in more samples and for a longer period of time than conventional methods. VIRUS EXCRETION The detection of persistent virus in sheep and goats, however, is not enough to establish that they are important in FMDV transmission. The route by which most ruminants are likely to encounter FMDV under field conditions is via the respiratory tract and therefore the amount of virus excreted into the environment is important. Sheep and goats have been shown to excrete similar amounts of airborne virus (Sellers & Parker, 1969; Donaldson et al., 1970). The maximal yields were obtained from both species within a few days of contact exposure (Donaldson, 1979). The amount of airborne virus excreted depends on the serotype and strain of virus involved (Donaldson et al., 1970). Sellers et al. (1977), following an experimental infection of sheep, reported that FMDV could be readily detected at two time points after aerosol exposure to virus firstly, between 30 min and 22 h, attributable to virus trapped in the wool during initial exposure to virus, and secondly between 2 and 7 days, attributable to limited replication in the respiratory tract. Such virus was detectable from both susceptible and vaccinated animals. Control of movement for 2 weeks after infection was therefore recommended as a means of preventing disease spread. This period of production of airborne FMDV corresponds to the period of high titres of virus iso-

lated from OP fluids identified by McVicar and Sutmoller (1969). No data, however, is available reporting the amount of virus exhaled by carrier sheep and goats. With the possible exception of an experiment by De Clercq et al. (1997) involving two sentinel pigs, experimental transmission of FMDV from carriers to susceptible in-contacts has not been clearly demonstrated. Since isolation of virus from the OP samples of carrier animals is frequently intermittent, it is likely that a low level of virus replication occurs during the carrier state with occasional periods of higher virus excretion. Experimental evidence from studies in cattle has shown a decline in titre and frequency of virus recovery throughout the carrier period (Rossi et al., 1988). Donaldson and Kitching (1989) concluded that the amounts of virus recovered from OP fluids were generally below the level required for transmission of FMDV to other susceptible animals by natural routes. Woodbury (1995) concluded from experimental and field evidence that transmission from carrier to susceptible animals is probably a rare event, and so is most probable when there is a high ratio of susceptible to carrier animals. It is therefore unlikely to occur in areas where vaccination is practised. In conclusion, sheep and goats are most likely to be involved in the transmission of FMDV during the early stages of either clinical or subclinical FMD infection, rather than when they are carriers, and the period of greatest risk of transmission is up to 7 days after contract with the infection. SPECIES ADAPTATION AND VIRULENCE When considering the role of small ruminants in the transmission of FMDV, the virulence of FMDV strains from sheep and goats for other hosts must be considered. Strains which are adapted to sheep and goats may vary in their virulence for other species, such as cattle and pigs, particularly if they have been replicating for some time in the small ruminant host. Limited experimental evidence suggests that this might be the case (Bauer et al., 1977). Furthermore, field cases have been reported in which sheep and goats have been diagnosed seropositive for FMDV in the absence of any recent outbreaks, and in co-existence with cattle that have remained seronegative (Mackay, 1994; Mackay & Rendle, 1996). However, strains first isolated from sheep/goats have also been highly virulent for cattle and pigs (McVicar & Sutmoller, 1969;

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Khukhorov et al., 1973 Yadin & Cloudia, 1995; Leforban, 1996; Kitching, 1998), and in fact the 1967/68 epidemic in the UK is suspected to have originated from imported contaminated frozen lamb (Anon., 1968).
Serum antibody (LOG 10)

3 2.5 2 1.5 1 0.5 0 3 2.5 2 1.5 1 0.5 0

SV71 SV72 SV73

14

21

28 56

70 112 168 SV77 SV78 SV79

VACCINATION The role of sheep and goats in the maintenance of FMD remains uncertain, so the design of appropriate disease control measures is problematical. In particular, it is not proven that prophylactic vaccination of small ruminants is essential to eradicate the disease, and there is some evidence that FMD in sheep and goats is self-limiting (Anderson et al., 1976). Owing to the cost of vaccination, small ruminants tend not to be routinely vaccinated, unless there is an association with large numbers of cattle and swine. This is despite the recommendation that they are included in vaccination campaigns unless it can be clearly shown to be unnecessary (Anon., 1972). When vaccination does take place, however, a conventional saponin aluminium hydroxide, inactivated vaccine (one-third to onequarter of the normal bovine dose) has generally been used, as recommended by Fontaine et al. (1966, 1969) and Pappous et al. (1972). Protection from challenge (as measured by antibody response or the absence of virus) has been shown from 21 days to 6 months after vaccination (Sharma & Dutt, 1968; Oral et al., 1970; Pappous et al., 1972). More recent studies have concentrated on vaccine formulations and regimes (Nair & Sen, 1992, 1993a, b; Hunter, 1996) to improve and generate long-term protection for use in areas where FMDV is endemic or prophylactic vaccination is carried out. Some experimental studies have indicated that oil adjuvanted formulations give an improved antibody response, although animals were not challenged to check the protective capacity of these vaccines (Nair & Sen, 1992; Hunter, 1996). Our recent studies with sheep vaccinated with A22 Iraq antigen, formulated as an oil emulsion (Montanide ISA 25 or 206, Seppic) or as an aluminium hydroxide saponin vaccine, and monitored over a 6month period, showed similarly rapid antibody responses, regardless of adjuvant, which peaked 721 days post vaccination (Fig. 1). However, only the sheep vaccinated with the ISA 206 oil formulation maintained high titres of antibody for the duration of the trial. Further studies with these aqueous and ISA 206 oil formulated emergency

0 3 2.5 2 1.5 1 0.5 0

14

21

28

56

70 112 168 SV74 SV75 SV76

7 14 21 28 56 70 112 168 Days post vaccination

Fig. 1. Serum antibody responses in sheep following vaccination with FMDV type A22 Iraq as measured by microneutralization assay. Groups of three animals were each immunized with a 1 mL volume of vaccine (equivalent to a 0.5 bovine dose), adjuvanted with either (a) Al(OH)3/saponin, (b) Montanide ISA 25 or (c) Montanide ISA 206, and monitored over a 6-month period.

vaccines, using other inactivated antigens, namely O1 Lausanne, Asia 1 India and C1 Oberbayern, showed that all were able to protect sheep against airborne homologous FMDV challenge within 4 days of vaccination (Cox et al., 1999). Volpina et al. (1996) recently reported the development of a synthetic peptide vaccine using a dipalmitoyl derivative of the 135159 fragment of VP1 protein of the foot-and-mouth disease strain A22 which, in association with the adjuvant polymethylsiloxane oil, was found to protect all sheep, following a single administration, for at least 7 months, and 90% of the vaccinates after 1 year. An advantage of synthetic vaccines is their safety, as they do not require the culture and inactivation of live FMDV. However, as with previous studies, high levels of peptide (2 mg/sheep) need to be administered to afford such protection. Vaccination, particularly emergency vaccination, besides conferring protection should also reduce local virus replication in the respiratory tract,

EPIDEMIOLOGY AND TRANSMISSION OF FMD

11

thereby dampening down the amount of virus in the environment and reducing the risk of spread. Gibson et al. (1984) administered three- to six-fold doses of conventional aqueous vaccine to sheep and challenged the animals 1 week later by airborne exposure. Following challenge, viraemia was prevented but not local virus replication or excretion of FMDV in OP fluids. More recent studies by Barnett and Cox with emergency vaccine formulations have indicated that aqueous and oil formulations are equally efficient at reducing local virus replication (Cox et al., 1998). Fondevila et al. (1996) concluded that vaccination in the ovine reduces infection and the probability of establishing the carrier state. CONCLUSIONS There is much circumstantial evidence to suggest that sheep and goats may be important in the field transmission of FMDV. Using more reliable, sensitive techniques, further studies, both during and after field outbreaks, should be carried out to identify virus carriers as well as seropositive animals which may or may not be infectious, in order that the role of each in the epidemiology of FMD can be elucidated. In the meantime, for countries where FMD is endemic or where policies are underway to eradicate FMD, it is advisable to include sheep and goats in the routine vaccination campaigns, particularly in areas of high livestock density. Elsewhere, in FMD-free regions, strategic reserves of FMD antigen held in vaccine banks, such as the International Vaccine Bank at Pirbright, must be capable of producing formulated vaccines that induce rapid protection and reduce local virus replication in both sheep and goats. REFERENCES
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STRAVER, P. J., BOOL, P. H., CLASSENS, A. M. J. M. & VAN BEKKUM, J. G. (1970). Some properties of carrier strains of FMDV. Archiv fur die Gesamte Virusforschung 29, 11326. TAYLOR, M. N. & TUFAN, M. (1996). Detailed investigations, using farmer interviews, to assess the losses caused by FMD outbreaks in Turkey. Report of Turkish-German Animal health Information Project (GTZ), Ministry of Agriculture and Rural Affairs (MARA), Republic of Turkey. VOLPINA, O. M., YAROV, A. V., ZHMAK, M. N., KUPRIANOVA, M. A., CHEPURKIN, A. V., TOLOKNOV, A. S. & IVANOV, V. T. (1996). Synthetic vaccine against foot-and-mouth

disease based on a palmitoyl derivative of the VP1 protein 135159 fragment of the A22 virus strain. Vaccine 14, 137580. WOODBURY, E. L. (1995). A review of the possible mechanisms for the persistence of foot-and-mouth disease virus. Epidemiology and Infection 114, 113. YADIN, H. & CLOUDIA, K. (1995). Small ruminants as FMD virus carriers. Report of the Session of the Research Group of the Standing Technical Committee on Control of Foot-andmouth Disease; pp2632. Vladimir, Russia: Rome: FAO.
(Accepted for publication 1 October 1998)

Book Review
Far Away Cows: Veterinary Vignettes from the Third World Guilbride, P. Lewes, Sussex, The Book Guild, 1998. 655 pp. 18.50 (hard) ISBN 1 85776 234 7 This would be an excellent volume to choose for Desert Island Discs, together with the Bible. Indeed, there are perhaps surprising parallels between the two volumes for both are, in essence, collections of books linked by a common theme. Like parts of the Bible, Far Away Cows is a progressive narrative that moves through time, with the story carried by a series of anecdotes. These are, in different places, amusing, concerning, instructive, annoying or even infuriating, as suits the point being made. Many will ring bells with veterinarians who have worked in developing countries, and it is perhaps these who will find most to empathize with in the book. However, the contrasts should also be of interest to others whose experience is limited to the developed world. At first sight, Far Away Cows is a somewhat daunting volume. It is long, perhaps overlong for a modern day autobiography. Nevertheless, it was sufficiently interesting to hold this readers attention to the end. It is the story of a personal odyssey, the authors 38-year-long career in veterinary medicine in tropical countries. It moves from colonial days in Africa, through the problems of newly independent Jamaica and Uganda, and on to working for an international professional civil service. Thus, it passes from an era in which the natives could be termed Johnny Bantu to one in which local politicians are in firm control and can easily, for their own ends, frustrate the best intentions of an international organisation and its staff. From the life of a young bachelor, it proceeds to that of the father bringing up a large family no less than six daughters and one son! in five widely disparate countries, each of which is given a distinct section, almost a book in itself. Yet the collection of books also tells a continuous and developing story. The young veterinarian with which the story begins, is thrust into a remote region of Northern Rhodesia. The international civil servant with which it ends, struggles with political ideology and bureaucratic inefficiency in Marxist Mozambique. In between lies something of an idyll as a Field Officer in Jamaica, research in Uganda, high in the Andes and in the Amazonian forest of Peru, and a most frustrating time struggling to bring to birth a research programme in Brazil, in which local interest was strictly that for a potential milch cow. There is occasional repetition and even a few howlers; that which jarred most with this helminthologist being the statement that the large white round worm [Toxocara vitulorum] of cattle is a relation of the earthworm! Nevertheless, having seen the same developments from a very different perspective, I would strongly recommend this book. It is both an informative and an instructive account of the achievements, despite many and varied frustrations, of one among the many veterinarians who have devoted their careers to the service of animals, their owners and both local and international authorities in the developing world in this century. M.M.H. SEWELL