Seal Distemper Outbreak 2002 Tom Barrett, Pramoda Sahoo & Paul D. Jepson
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Seal distemper outbreak 2002 Tom Barrett, Pramoda Sahoo & Paul D. Jepson Morbilliviruses, Phocine distemper the group of viruses virus for which the human The past 15 years have measles virus is witnessed the emergence of several newly recognized the type virus, have members of the genus recently been found Morbillivirus as significant to infect diverse causes of disease outbreaks species of marine and mortality in marine mammals. Over the mammals belonging to past 15 years the orders Pinnipedia (seals) epizootics of these and Cetacea (whales, por- viruses have caused poises and dolphins). mass die offs, The first morbillivirus mainly of seals and with potentially severe dolphins, in widely ecological consequences for marine mammals was dispersed locations. identified in harbour (Phoca vitulina; Fig. 1) and grey The epizootic of (Halichoerus grypus) seals which died in large numbers off Interstitial emphysema phocine distemper the coasts of northern Europe in 1988. At first, based on virus (PDV) that clinical and antigenic similarities, the seal virus was occurred in northern thought to be canine distemper virus (CDV), the main European seals in pathological feature being acute pneumonia (see Fig. 2). April 2002 caused The interest which resulted from finding morbillivirus the deaths of more in marine mammals for the first time meant that all than 22,000 available resources were quickly employed to harbour and grey characterize the new virus. These analyses soon showed seals before finally that the seal virus was most closely related to, but distinct from, CDV and was classified as a new member burning out in late of the genus Morbillivirus and named phocine distemper September. virus (PDV). The most severely affected species was the harbour seal from the North Sea and north-western Atlantic, with grey seals from the same areas proving more resistant to the virus. Since then three other morbilliviruses have been found to infect various species of marine mammals: CDV itself has been found in seals and polar bears, a morbillivirus (PMV) has been isolated from porpoises and another Lake Baikal seals (Phoca sibirica) suffered an unusual and from dolphins (DMV). The latter two viruses are severe mortality. Subsequently CDV, rather than PDV, genetically very closely related to each other, but they are was shown to have been the aetiological agent. Similarly, not species-specific as the porpoise virus has been found a mass die off that occurred in Caspian Sea seals (Phoca in dolphins. They are best regarded as variants of a caspica) in 1997, and again in 2000, was also attributed to cetacean morbillivirus virus (CeMV). Many cetacean CDV infection. Although not proven, the source of the species worldwide have been reported to be seropositive virus is likely to have been terrestrial carnivores, such as for this virus. The pilot whale (Globicephala spp.), which wolves, which prey on seal pups. Retrospective serolo- has a worldwide distribution, appears to be the reservoir gical evidence also links this virus with deaths of thou- and vector for transmission of CeMV to other species as sands of crabeater (Lobodon carcinophagus) seals near a base TOP RIGHT: they move in large groups, known as pods, over great with sledge dogs in the Antarctic in the 1950s. There are Fig. 1. A harbour seal. ocean distances. Over 90 % of pilot whales that were no terrestrial carnivores in the Antarctic and so it is likely COURTESY DR PAUL THOMPSON, involved in mass strandings between 1982 and 1993 that sledge dogs used at that time were the original ST ANDREWS UNIVERSITY were morbillivirus-seropositive. source of CDV, or possibly the animals were infected by contact with carnivores in New Zealand or South America LOWER RIGHT: Other morbilliviruses affecting seals during migrations. The virus appears to have established Fig. 2. Infected seal lung showing severe interstitial Apart from PDV infections, other morbilliviruses can itself in the crabeater seal population as a subsequent pneumonia. also cause mortality in seal populations. In the winter of serological survey of Antarctic seals showed them to have COURTESY T. BARRETT 1987–1988, just prior to the European seal epizootic, a high prevalence of CDV-specific antibodies. 162 MICROBIOLOGYTODAY VOL 30/NOV03 Moray Firth identical course to that of 1988, starting at the end of LEFT: April, also originating from the island of Anholt Fig. 3. Location of PDV outbreaks around the coasts of the The Wash (population ~12,000 harbour seals). Through May the British Isles during 2002. virus spread from the initial focus in the Kattegat and spread through The Skagerrak and then into the Dutch BELOW: Wadden Sea and the North Sea. In the UK, as in 1988, Fig. 4. Seal mortality resulting the first PDV-positive harbour seal was identified in from the European PDV epizootic in 2002. The numbers of dead The Wash in April. By mid-August an epizootic- seals in the different areas type increase in harbour seal mortality began in the affected, excluding the Baltic immediate area, peaking in mid-September when Sea, are given for comparison. more than 400 seals were washed up dead each week. By Kat, Kattegat; Ska, Skagerrak. The inset panel shows the weekly seal then PDV had reached Scotland and was first identified death figures in The Wash. in a harbour seal found in Dornoch in the Moray Firth. Shortly afterwards a small number of dead seals was found in Northern Ireland and along the west coast of Ireland and PDV infection was confirmed. No PDV- Diagnosing morbillivirus infections positive seals were found along the Welsh coast (see When wildlife species show clinical disease with signs Fig. 3 for location of UK outbreaks). Although further resembling distemper, a morbillivirus infection may be PDV-positive harbour and grey seals were identified in involved. As CDV and PDV infections in seals are east and west Scotland (including Orkney) in late 2002, clinically similar, differential diagnosis has to be made unlike 1988, no noticeable increase in Scottish seal between these two viruses and this is most easily done mortality was apparent. by RT-PCR using universal morbillivirus primer The total death toll in European waters eventually sets and primer sets specific for each morbillivirus reached over 22,000 based on dead seal counts, species. Some evidence also links the CeMV with seal approaching 60 % of harbour seals in the worst affected mortality, although not on the same massive scale seen areas, although these figures may be revised following with PDV or CDV. The rare monk seal population of analysis of aerial survey data. Approximately 10 % of the eastern Mediterranean was not severely affected these were found in The Wash, the vast majority being during an outbreak of this virus which killed thousands harbour seals (see Fig. 4). of striped dolphins (Stenella coeruleoalba) around the Mediterranean coasts in 1990–1991. However, CeMV Transmission of PDV was found in carcasses of monk seals that died in large The small size and scattered nature of European seal numbers off the coast of Mauritania in 1997. At the time populations makes it is unlikely that they could main- an algal bloom was also considered to be a primary or an tain this virus in circulation as morbilliviruses need a exacerbating factor which may have contributed to the constant supply of new susceptible hosts since, following very high mortality among adult seals. recovery, infection induces life-long immunity to the Recent outbreaks of PDV 12,000 Until last year the most devastating virus-induced mass mortality event in European seals occurred in 1988, 500 when PDV killed more than 18,000 seals around 10,000 400 northern European coasts, the vast majority being harbour seals. That epizootic began on the Danish island 300 8,000 of Anholt in the Kattegat and then spread to Sweden, 200 the Netherlands, Norway, Germany, the UK and Ireland. Since 1989 there has been no convincing 100 serological evidence for persistence of PDV in European 6,000 0 seals. A minor outbreak of disease in seals occurred 1998 13579111315 along the Belgian and northern French coasts and No. of dead seals Week 4,000 morbillivirus antigen and nucleic acid were detected in tissues from sick animals. However, most of the viruses involved were genetically closely related to either CeMV 2,000 or CDV. Unfortunately, in 2002 we again witnessed the recurrence of a major PDV outbreak, again mainly affecting harbour seals. The epizootic followed an almost Kat/Ska Wadden Sea UK coast MICROBIOLOGY TODAY VOL 30/NOV03 163 Further reading virus. The curious course of the epizootic on both Control of wildlife diseases is extremely difficult and occasions, starting from the Danish coast, moving first vaccination of wild animal populations, which in any Barrett, T. et al.(1993). Dolphin and porpoise to the Dutch and then on to English coasts and finally case is logistically very difficult, would raise ethical morbilliviruses are genetically ending in Scotland, may be explained by the migratory questions concerning uncontrolled spread of the vaccine distinct from phocine distemper and breeding habits of the seals. There is growing virus. Protection of vulnerable animals in seal sanctuaries virus. Virology193, 1010–1012. consensus among some seal biologists that grey seals would be acceptable as the animals could be confined Bengtson, J.L. et al.(1991). may act as vectors for the transmission of PDV between until the excretion of any vaccine virus had ceased. In Antibodies to canine distemper harbour seal colonies in European waters, especially any event, there is no currently licensed vaccine for use virus in Antarctic seals. Mar where large geographical jumps are made. Harbour seals in seals. Because of the close antigenic relationship Mamm Sci71, 85–87. usually return to the same haulout, whereas grey seals do between morbilliviruses, strong cross-protection to Dietz, R.