Introduction
In Arctic and subarctic areas of the Holarctic region, most carnivores at the top of the food chain act as a reservoir for Trichinella nativa (Rausch, Reference Rausch and Gould1970; Kumar et al., Reference Kumar, Pozio, de Borchgrave, Mortelmans and De Meurichy1990; Forbes, Reference Forbes2000; Rah et al., Reference Rah, Chomel, Follmann, Kasten, Hew, Farver, Garner and Amstrup2005; Pozio & Murrell, Reference Pozio and Murrell2006; www.iss.it/site/Trichinella/index.asp). An important biological characteristic of this Trichinella species is that muscle larvae survive in frozen carnivore muscles for up to 5 years, favouring the transmission from one carnivore host to another under extreme conditions, such as those existing in these areas (Pozio & Murrell, Reference Pozio and Murrell2006).
In Iceland, Trichinella infection has never been documented in humans or in domestic or wild animals living on the island (Skírnisson et al., Reference Skírnisson, Richter, Eydal, Akuffo, Linder, Ljungström and Wahlgren2003). However, in 1963, a polar bear (Ursus maritimus), shot in the area of Hornvík (66°23′17″N, 22°40′58″W) but transported immediately on a boat to the town of Ísafjörður, was found to have Trichinella sp. larval infection (Pálsson, Reference Pálsson1964). Given that the meat from this infected bear had been distributed for human consumption, the health authorities warned the local population not to eat polar bear meat, although it became clear that most of them had already done so. However, no cases of human infection were reported or suspected, probably because the meat had been thoroughly cooked (Pálsson, Reference Pálsson1964).
Polar bears are one of the most important reservoirs of T. nativa in Alaska, Canada, Greenland, the Barents and Norwegian Seas and the Chukotsk peninsula, with a prevalence of infection of up to 61% (Weyermann et al., Reference Weyermann, Worley and SeeSee1993). In Iceland, most polar bears arrive when pack ice is stranded ashore or comes into close proximity of the northern or north-western coasts. Documentation of their presence dates back to the ‘Icelandic Saga’, written in the 13th and 14th centuries, and over the centuries more than 500 polar bears have been recorded, 50 of them in the past 100 years (Haraldsson & Hersteinsson, Reference Haraldsson, Hersteinsson and Hersteinsson2004). Over the past centuries, many of the bears were killed, although in some cases they returned to the ice and disappeared (Haraldsson & Hersteinsson, Reference Haraldsson, Hersteinsson and Hersteinsson2004). In 2008, a polar bear that had swum to Iceland was found to have been infected with T. nativa. The objective of the present study was to describe this second case of a Trichinella-infected polar bear and to evaluate the epidemiological features that allowed T. nativa to spread in Arctic regions. We also provide epidemiological information that could explain the reason why T. nativa seems not to have been transmitted in terrestrial ecosystems of Iceland, at least in the past two centuries.
Materials and methods
In June 2008, when the nearest edge of the pack ice was 100 nautical miles (185 km) off the northern coast of Iceland, two polar bears, a male and a female, swam to Skagi (66°06′53″N, 20°08′51″W). Soon after their arrival, the bears were shot for security reasons by a team led by police officers: the male was shot on 3 June and the female on 16 June.
The bear carcasses were transported to the Institute for Experimental Pathology at Keldur, University of Iceland, and various biological samples were collected. To estimate the age of the bears, growth layer groups were counted in the cementum region of I1 in both animals (Skírnisson, Reference Skírnisson2009). To detect Trichinella sp. larvae, muscle samples (50 g each) were collected from the masseter, diaphragm and tongue, and were digested using the standard method (Nöckler & Kapel, Reference Nöckler, Kapel, Dupouy-Camet and Murrell2007). After digestion, the larvae were collected, stored in 95% ethyl alcohol and sent to the International Trichinella Reference Centre (ITRC, www.iss.it/site/Trichinella/index.asp) for species identification. At the ITRC, 20 single larvae were analysed by a validated multiplex polymerase chain reaction (PCR) analysis, following a previously described method (Pozio & La Rosa, Reference Pozio and La Rosa2003).
Results and discussion
Both of the polar bears were unusually small and lean: the male weighed 220 kg and had a body length of 209 cm; the female weighed 142 kg, with a body length of 194 cm. The female was estimated to be 14.5 years old and the male at least 22.5 years old. Trichinella sp. larvae were only detected in the male (8.5 larvae/g in the tongue, 6.8 larvae/g in the masseter and 4.4 larvae/g in the diaphragm). The larvae were identified as T. nativa (isolate code 2229; www.iss.it/site/Trichinella/index.asp) and this is the first report of T. nativa infection in Iceland.
Polar bears have a circumpolar distribution. They range throughout the Arctic region surrounding the North Pole. The limits of their range are determined by the ice pack of the Arctic Ocean and the landfast ice of surrounding coastal areas (DeMaster & Stirling, Reference DeMaster and Stirling1981; Nowak, Reference Nowak1999). The prevalence of T. nativa infection in polar bears varies by geographic area and increases with age (Henriksen et al., Reference Henriksen, Born, Eiersted, Campbell, Pozio and Bruschi1994), although it is generally quite high: 10–60.9% in Alaska (Fay, Reference Fay1960; Rausch, Reference Rausch and Gould1970; Weyermann et al., Reference Weyermann, Worley and SeeSee1993); 59% in the Barent's and Norwegian Seas (Thorshaug & Rosted, Reference Thorshaug and Rosted1956); 23–32% in Greenland (Madsen, Reference Madsen1961; Born & Henriksen, Reference Born and Henriksen1990; Henriksen et al., Reference Henriksen, Born, Eiersted, Campbell, Pozio and Bruschi1994); and 31.4% on the Svalbard Islands (Larsen & Kjos-Hanssen, Reference Larsen and Kjos-Hanssen1983). In polar bears from the Beaufort and Chukchi Seas, anti-Trichinella antibodies were detected serologically in 55.6% (278/500) of the animals (Rah et al., Reference Rah, Chomel, Follmann, Kasten, Hew, Farver, Garner and Amstrup2005). This very high serological prevalence is due to the fact that the polar bear is at the top of the food chain and that its life span is longer than that of other carnivores, reaching up to 30 years in the wild and 45 years in captivity (Hemstock, Reference Hemstock1999).
Iceland first began to be populated by Norse settlers in ad 874. These settlers brought with them livestock (sheep, horses, cattle, pigs and poultry), pets (dogs and cats) and probably both the house mouse (Mus musculus) and the field mouse (Apodemus sylvaticus) (Skírnisson et al., Reference Skírnisson, Richter, Eydal, Akuffo, Linder, Ljungström and Wahlgren2003). When the settlers arrived, the only terrestrial mammal present was the arctic fox (Alopex lagopus) (Haraldsson & Hersteinsson, Reference Haraldsson, Hersteinsson and Hersteinsson2004), which is still common in Iceland. Its population has increased markedly in recent decades, with an estimated autumn population of approximately 6000 (Hersteinsson, Reference Hersteinsson and Hersteinsson2004a). Although Trichinella sp. has never been detected in arctic foxes in Iceland, this species does act as a reservoir of T. native in the Arctic, with a prevalence of infection of 12% (16/136) in Greenland, 8.5% (59/697) on the Svalbard Islands, 7% (16/222) in Alaska, 11.5% (23/200) in the Chukotsk peninsula, and 13% (35/270) in the Iamal peninsula (Madsen, Reference Madsen1961; Rausch, Reference Rausch and Gould1970; Prestrud et al., Reference Prestrud, Stuve and Holt1993; Kapel et al., Reference Kapel, Henriksen, Berg and Nansen1996).
As mentioned, Trichinella nematodes have never been documented in humans or domestic or wild animals living on Iceland (Skírnisson et al., Reference Skírnisson, Richter, Eydal, Akuffo, Linder, Ljungström and Wahlgren2003; Hersteinsson, Reference Hersteinsson and Hersteinsson2004b). In the 1950s and 1960s, no infection was detected among domestic pigs that had been fed imported food remains which had originated from the American military base in Keflavík (Thorsteinsson, Reference Thorsteinsson1992). In the period from 1998 to 2008, diaphragm samples from more than 1600 horses that were raised in Iceland were also free of infection (Anonymous, 1998–2008). In the 1990s, none of the dozens of arctic foxes and feral minks (Mustela vison) captured in different parts of Iceland were found to have been infected, as determined by the digestion of diaphragm samples (Karl Skírnisson, unpublished data). One of the factors that could be responsible for the absence of T. nativa in Iceland's terrestrial ecosystem is the island's geographical isolation and its small size (103,000 km2). This is probably also one of the reasons why Trichinella spiralis has never been detected, in addition to the limited importation of animals potentially infected with T. spiralis, including the brown rat (Rattus norvegicus) (Skírnisson, Reference Skírnisson and Hersteinsson2004a). Potentially, migratory seals could introduce T. nativa to the island. In fact, four seal species (Phoca groenlandica, Phoca hispida, Cystophora cristata and Erignathus barbatus) have regularly been observed off and on Iceland's coast, and T. nativa has been detected in two of these species: E. barbatus, with a prevalence of infection of 0.8% (2/245) in Greenland and 0.7% (1/148) in Alaska, and P. hispida, with a prevalence of infection of 0.05% (1/1775) in Greenland and 0.7% (2/300) in Alaska (Forbes, Reference Forbes2000). Moreover, two seal species breed in coastal areas of Iceland: the harbour seal (Phoca vitulina), with a present population of 10,000 – 15,000 (Hauksson et al., Reference Hauksson, Bogason, Ólafsdóttir and Hersteinsson2004), and the grey seal (Halichoerus grypus), with a population of approximately 5000 animals (Hauksson & Ólafsdóttir, Reference Hauksson, Ólafsdóttir and Hersteinsson2004), although T. nativa has never been detected in either of these species. Seals infected with T. nativa could act as a source of infection for terrestrial mammals; in particular, seal carcasses on the beach could be consumed by the arctic fox. Nonetheless, the very low prevalence of infection and the low worm burden in seals suggest that these animals do not act as a reservoir.
Another potential source of infection is the walrus (Odobenus rosmarus), which is known to host T. nativa, with a prevalence of infection ranging from 1.0 to 9.4%. Walruses also represent an important source of infection for humans (Forbes, Reference Forbes2000). However, only on very rare occasions have they been spotted along Iceland's coasts (Thórdarson & Hauksson, Reference Thórdarson, Hauksson and Hersteinsson2004).
If T. nativa were to be introduced into Iceland's ecosystem, it is believed that both the arctic fox and the mink could maintain a sylvatic cycle. Minks were first imported for fur farming in 1931, and they soon escaped and established feral populations on all parts of the island (Skírnisson, Reference Skírnisson and Hersteinsson2004b). Furthermore, in the past 50 years there has been an approximately threefold increase in the arctic fox population (Hersteinsson, Reference Hersteinsson and Hersteinsson2004a), increasing the likelihood of the survival of T. nativa, if it were to be introduced. Although the possibility of the future introduction of T. nativa in Iceland's wildlife cannot be excluded, careful surveillance can contribute to preventing this occurrence, as was the case in 2008, when the polar bears were discovered and killed and the carcasses were destroyed to prevent them from being consumed by domestic or wild animals.
Acknowledgements
We are very grateful to Ásgeir Ástvaldsson, Guðbjörg Jónsdóttir and Signý Bjarnadóttir for their technical support. The study on the polar bears was financed by the Ministry for the Environment of Iceland. The work carried out in Italy was funded by the European Commission (contract SANCO/2006/FOODSAFETY/032).
