Human pathogens in marine mammal meat – a northern perspective.

Zoonoses and Public Health

REVIEW ARTICLE

Human Pathogens in Marine Mammal Meat – A Northern Perspective M. Tryland1, T. Nesbakken2, L. Robertson3, D. Grahek-Ogden4 and B. T. Lunestad5 1 2 3

4 5

Section for Arctic Veterinary Medicine, Department of Food Safety and Infection Biology, Norwegian School of Veterinary Science, Tromsø, Norway Section for Food Safety, Department of Food Safety and Infection Biology, Norwegian School of Veterinary Science, Oslo, Norway Section for Microbiology, Immunology and Parasitology, Department of Food Safety and Infection Biology, Norwegian School of Veterinary Science, Oslo, Norway Norwegian Scientific Committee for Food Safety, Oslo, Norway National Institute of Nutrition and Seafood Research, Bergen, Norway

Impacts

• Trichinella spp., Toxoplasma gondii, Salmonella and Leptospira spp. are the • •

most important zoonotic agents in marine mammal meat. In addition, botulism remains a threat among native populations in the Arctic. Mycoplasma spp., but also parapoxvirus and Mycobacterium spp., are important occupational risks for people handling marine mammals and marine mammal products. Critical hygiene points in killing, dressing, and storage on board, as well as data gaps regarding hygiene control measures of marine mammal meat are identified.

Keywords: Whale; seal; zoonosis; foodborne; human pathogen; meat hygiene Correspondence: M. Tryland. Section for Arctic Veterinary Medicine, Department of Food Safety and Infection Biology, Norwegian School of Veterinary Science, Stakkevollveien 23, Tromsø N-9010, Norway. Tel.: +47 77665400; Fax: +47 77694911; E-mail: morten.tryland@ nvh.no Received for publication July 10, 2012 doi: 10.1111/zph.12080

Summary Only a few countries worldwide hunt seals and whales commercially. In Norway, hooded and harp seals and minke whales are commercially harvested, and coastal seals (harbour and grey seals) are hunted as game. Marine mammal meat is sold to the public and thus included in general microbiological meat control regulations. Slaughtering and dressing of marine mammals are performed in the open air on deck, and many factors on board sealing or whaling vessels may affect meat quality, such as the ice used for cooling whale meat and the seawater used for cleaning, storage of whale meat in the open air until ambient temperature is reached, and the hygienic conditions of equipment, decks, and other surfaces. Based on existing reports, it appears that meat of seal and whale does not usually represent a microbiological hazard to consumers in Norway, because human disease has not been associated with consumption of such foods. However, as hygienic control on marine mammal meat is ad hoc, mainly based on spot-testing, and addresses very few human pathogens, this conclusion may be premature. Additionally, few data from surveys or systematic quality control screenings have been published. This review examines the occurrence of potential human pathogens in marine mammals, as well as critical points for contamination of meat during the slaughter, dressing, cooling, storage and processing of meat. Some zoonotic agents are of particular relevance as foodborne pathogens, such as Trichinella spp., Toxoplasma gondii, Salmonella and Leptospira spp. In addition, Mycoplasma spp. parapoxvirus and Mycobacterium spp. constitute occupational risks during handling of marine mammals and marine mammal products. Adequate training in hygienic procedures is necessary to minimize the risk of contamination on board, and acquiring further data is essential for obtaining a realistic assessment of the microbiological risk to humans from consuming marine mammal meat.

© 2013 Blackwell Verlag GmbH Zoonoses and Public Health, 2014, 61, 377–394

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Human Pathogens in Marine Mammal Meat

Introduction

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procedures are not as stringent as those in abattoirs for domestic animals. Hygienic meat control is generally limited and is based on spot tests, focussing on a few agents, mainly indicator bacteria for faecal contamination. In addition, there seems to be a general lack of knowledge on the occurrence of potentially zoonotic pathogens in marine mammal meat and products. Research reports on infections in marine mammals, and on human pathogens in particular, are relatively scarce and anecdotal, and data tend to be separated by species, populations, geography and time.

Marine mammals as food Marine mammals consist of a diverse group of roughly 120 species that live in, or are fully dependent on, the ocean and the marine food chain. This group includes cetaceans (whales, dolphins and porpoises), pinnipeds (true seals, eared seals and walruses), sirenians (dugongs and manatees) and otters (sea otters and marine otters). Polar bears (Ursus maritimus) are usually considered marine mammals, as they may spend all or most of the year on sea ice. Among marine mammals, only seals and whales are regularly used for human consumption. Marine mammals have long been recognized as valuable resources, both for food and as a source of fur, leather, blubber (oil), baleens and teeth. Commercial exploitation of many marine mammal populations peaked in the 17th and 18th centuries and continued into the 19th century, whereas whaling in Antarctic waters peaked early in the 20th century. For some species, this commercial whaling almost resulted in extinction. International cooperation on whaling regulations started in 1931 and the International Convention for the Regulation of Whaling (ICRW) was signed in 1946. The International Whaling Commission (IWC) is a part of ICRW and sets hunting quotas, based on recommendations from its Scientific Committee. Seals of different species and stocks are commercially hunted for fur and meat in Canada, Russia, Greenland, Namibia and Norway. In addition to the minke whale (Balaenoptera acutorostrata) hunt in Norway, whales are currently hunted commercially in Iceland (minke and fin whales; Balaenoptera physalus) and Japan (Antarctic minke whales; Balaenoptera bonaerensis). In addition, subsistence hunting occurs in the Faroe Islands (mainly long-finned pilot whales; Globicephala melaena), Greenland (minke, fin and bowhead whales; Balaena mysticetus), Indonesia (sperm whales; Physeter macrocephalus), Russia (gray whales; Eschrichtius robustus), and Canada and the United States of America where Inuit communities hunt bowhead whales, and also beluga (Delphinapterus leucas) and narwhals (Monodon monoceros). Some societies, such as the Inuit communities along the northern coasts of Alaska, Canada, Greenland and Russia, depend on harvesting whales and seals and also have food traditions mainly based on dried and fermented products, that is, not heat-treated. During the years 2006–2009, an average of 571 tonnes of whale meat and 11 tonnes of seal meat (mostly harp seals; Phoca groenlandica) were processed annually for human consumption in Norway. The meat is sold directly to the public, or through grocery store chains and restaurants. As the meat is distributed commercially, food safety is covered by specific regulations, but due to the relatively basic conditions on board hunting vessels, hygienic conditions and

Norway conducts an annual commercial hunt of harp seals and hooded seals in the West Ice, defined as the pack ice between Jan Mayen and Greenland, and of harp seals in the East Ice, defined as the part of the Barents Sea at the outlet of the White Sea (Russian economic zone). Sealing once represented an important income for many fishing communities, with a specific focus in the towns of Alesund and Tromsø and surrounding regions. In 1955, a total of 64 vessels caught close to 300 000 animals, whereas in the past 5 years, only a few boats have participated. Due to a decline in the hooded seal population, the commercial hunt of this species has been halted since 2007, and, in recent years, only a restricted hunt for scientific purposes has been conducted. A total of 1263 harp seals were caught in 2009, of a quota of 40 000. The quota for harp seals for 2010 was set to 42 400 animals in the West Ice, of which approximately 4500 were caught, and no commercial hunt was conducted in the East Ice in 2010. The most important products from seals have traditionally been the skin, which is used as a material for fur

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Norwegian whaling and sealing Norwegian whaling Today, Norway commercially hunts only one whale species, the minke whale, which is the smallest of the baleen whales in our waters. This hunt has probably been conducted in Norway since ancient times. The minke whale has a seasonal appearance along the Norwegian coast, visiting during spring, summer and early autumn. The minke whale hunt in Norway first became regulated in 1937, with the introduction of a mandatory licence. Today, the hunt is regulated by quotas and is restricted to the Norwegian coastline and off the coasts of Bjørnøya and Spitsbergen (Svalbard), and Jan Mayen. The minke whales in these regions all belong to the North Atlantic population. During the period 2001–2008, 535–647 animals (mean 586) were harvested annually. The total allowable catch for minke whales for 2010 and 2011 was 1286 animals each year, but the actual catch has been lower for both seasons, approximately 500–600 animals. Norwegian sealing

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products. Meat from the back of the animal (vacuumpacked and frozen on board), as well as front flippers and ribs (salted), has traditionally been consumed as a seasonal food in local communities. Seal meat is sold to local businesses and directly to the public. Recently, seal meat, including salted and smoked (not heat-treated), has become popular in some restaurants. Coastal seal hunt Based on counts from land and aerial surveys, the populations of harbour seals (Phoca vitulina) and grey seals (Halichoerus grypus) have been estimated at approximately 70 000–100 000 individuals (Nilssen and Bjørge, 2010) and approximately 7000 (Nilssen and Haug, 2007), respectively. The hunting quotas for 2010 were set to 470 and 1040 for harbour seals and grey seals, respectively. Along the coast of Northern Norway, regulations also allow hunting of harp seals and ringed seals (Pusa hispida), but these species occur only sporadically in these waters. Human pathogens


whales. However, there are no reports of foodborne disease outbreaks in Norway that have been linked directly to the consumption of marine mammal meat or products. As many of the infectious agents associated with marine mammal meat do not cause diseases with specific clinical signs, it can be difficult to associate such diseases with contact with or consumption of marine mammals. This review addresses the occurrence of potential human pathogens in marine mammals, from a Norwegian perspective, as well as the microbiota that can be present in marine mammal meat due to contamination during killing, dressing, cooling, storage and processing. We also address critical points that can increase the risk of consumers being exposed to pathogens from marine mammal meat, such as contamination, survival of infectious agents and dose– response information. Although anisakidosis, a parasitic nematode infection of mammals, is of relevance to public health, we do not consider it here, as its effect on human health is via the larvae, which occur in fish tissue, rather than via the adult stages found in marine mammals. Specific Human Pathogens Present in Marine Mammals

Human pathogens in marine mammals are defined here as infectious agents that have the potential to be transferred to humans and cause disease. Such pathogens may either be associated with the animal as a host, including the gut microbiota (Tryland, 2000), or be transferred to the animal or animal products from an environmental source. Environmental sources may be freshwater ice used for cooling the meat, seawater used for cleaning, contamination by faeces from sea birds and other types of contamination during handling and storage of the products, including transmission from humans by direct contact or by faecally contaminated seawater. Transmission of infectious agents from marine mammals to human has occurred through consumption of animal products, as well as through contact between humans and marine mammals, during hunting of wild animals and during feeding, training and handling of captive animals. Extensive outbreaks of foodborne human disease associated with consumption of whale and seal meat have been reported, involving up to several hundred persons. These have mostly occurred in communities in Greenland, Canada, Alaska and Japan, and agents involved include Trichinella spp., Toxoplasma gondii and Salmonella, as well as botulism – the latter being an intoxication after ingestion of meat in which the bacterium Clostridium botulinum has produced toxins. Seal finger (blubber finger, ‘spekkfinger’) is the most common occupational infectious disease in people handling seals and seal products, including during the Norwegian commercial sealing activity and research expeditions. Other infections may also occur through direct skin contact with seals and

Cryptosporidium spp The first report of Cryptosporidium spp. in a marine mammal was in a terminally ill dugong (Dugong dugon). Subsequent molecular analysis demonstrated the species to be C. hominis, a species generally associated with only human infection (Hill et al., 1997; Morgan et al., 2000; Appelbee et al., 2005). Since then, Cryptosporidium infections have been reported from a range of different marine mammals (Deng et al., 2000; Hughes-Hanks et al., 2005; Santin et al., 2005; Dixon et al., 2008) with prevalences of over 20% in some studies, while other studies of marine mammals have failed to identify infection with Cryptosporidium (Appelbee et al., 2005; Gaydos et al., 2008). Molecular studies to identify the Cryptosporidium to the species level have been even less extensive, although the California sea lion isolate was reported to be C. parvum (Deng et al., 2000). No transmission of Cryptosporidium to humans via infected marine mammals has been reported, and it is perhaps more likely that transmission of Cryptosporidium would result from handling of seal/whale meat from infected humans or contact with contaminated water. Several of the documented outbreaks of foodborne cryptosporidiosis are due to contamination from food-handlers (Robertson and Fayer, 2012).


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An overview of human pathogens associated with marine mammals is summarized in Table 1. Parasites


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Table 1. Human pathogens and potential human pathogens that can be present in free ranging and captive marine mammals

Infectious agent Parasites Cryptosporidium spp.

Giardia duodenalis

Toxoplasma gondii

Trichinella spp.

Bacteria Mycoplasma spp.

Marine mammal species found positive in previous studiesa,b

Marine mammal species found negative in studies performed to date

Ringed seal, California sea lion, Right whale, Bowhead whale, Dugong

Harp seal, Hooded seal, Bearded seal, Harbour seal (Pacific), Northern elephant seal, Northern bottlenose whale Beluga whale (white whale)

No case reports, but C. hominis, regarded as usually infecting only humans, have been isolated from dugong

Harp seal, Ringed seal, Minke whale

High seroprevalence in Inuit communities. Uncooked (dried etc.) or undercooked meat and products

Harp seal

Outbreaks reported, particularly from consumption of walrus

Harp and hooded seals are most likely carrying Mycoplasma spp. (not investigated/reported) Status unknown for hooded seal

Assumed cause of seal finger, a frequently reported zoonosis. Local infection of hands Older reports of large outbreaks of human salmonellosis after consumption of marine mammal meat One laboratory infection and three cases of CNS infections reported (B. pinnipedialis) – zoonotic potential uncertain

Status for Norwegian commercial species unknown

A seal trainer developed tuberculosis – aerosol transmission. Probably bacteria belonging to the M. tuberculosis complex. M. mageritense, a human pathogen, is isolated from a harbour porpoise with pneumonia No case reports. Mainly non-pathogenic species, but C. jejuni has been isolated

Ringed seal, Harp seal, Hooded seal, Grey seal, Harbour seal, Bearded seal, California sea lion, Bowhead whale, Right whale, Short-beaked common dolphin, Atlantic white-sided dolphin, Risso’s dolphin, Harbour porpoise Harbour seal, Hooded seal, Grey seal, Walrus, Beluga whale (white whale), Humpback whale, Harbour porpoise, Short-beaked common dolphin, Bottlenose dolphin, Sea otter, Polar bear Hooded seal, Grey seal Atlantic walrus, Bearded seal, Ringed seal

Harbour seal

Salmonella spp.

Harp seal, Grey seal, Beluga whale

Brucella sp.

Hooded seal, Harp seal, Ringed seal, Harbour seal, Grey seal, Atlantic walrus, Steller sea lion, Hawaiian monk seal, Weddell seal, Antarctic fur seal, Leopard seal, Minke whale, Fin whale, Sei whale, Pilot whale, Bryde’s whale, Killer whale, Harbour porpoise, Common dolphin, Atlantic whitesided dolphin, Striped dolphin, Bottlenose dolphin, Other dolphin species California sea lion, New Zealand fur seal, Australian fur seal, Australian sea lion, South American sea lion, Subantarctic fur seal, Harbour porpoise

Mycobacteria

Campylobacter spp.

Leptospira sp. Nocardia sp.

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Harbour seal (Phoca vitulina), Harbour porpoise (Phocoena phocoena, Northern elephant seals (Mirounga angustirostris) Sea lion, Northern fur seal, Common dolphin, Humpback whale, Harp seal Pilot wale, Beluga whale (white whale), Pacific bottlenose dolphin, Killer whale


Most Cetaceans

Potential risk to public health

No case reports, but isolates considered zoonotic, have been detected in a range of marine mammal species

Zoonotic isolates detected in a range of marine mammal species Zoonotic isolates detected in a range of marine mammal species


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Table 1. (Continued)

Infectious agent

Marine mammal species found positive in previous studiesa,b

Clostridium botulinum

Ubiquitous in the marine environment

Coxiella burnetii

Pacific harbour seal, Northern fur seal, Steller sea lion, harbour porpoise

Viruses Influenza A virus

Influenza B virus Poxvirus

Calicivirus

Rotavirus

Marine mammal species found negative in studies performed to date

Potential risk to public health


Marine mammal meat has been the source of botulism among northern native humans Risk for transmission via marine mammal meat unknown

Harbour seal, Hooded seal, Harp seal, Pilot whale Harbour seal Harbour seal, Grey seal, Weddell seal, California sea lion, Steller sea lion, South American sea lion, Spotted seal, Mediterranean monk seal Walrus, Californian sea lion, Steller sea lion, Northern fur seal, Northern elephant seal, Pacific dolphin, Bowhead whale, Gray whale, Fin whale, Sei whale, Sperm whale Galapagos sea lion, Galapagos fur seal

No serological screenings reported

Contact transmission and conjunctivitis reported. Potential for aerosol transmission Seals may be a reservoir species Transmission through bites or contact with saliva and skin (lesions), especially people caring for seals in captivity. Single cases, no documented spread between humans

No serological screening of commercially harvested marine mammals reported

One confirmed human case reported – skin infection in an animal handler

No serological screening of commercially harvested marine mammals reported

Oral infection. Zoonotic potential unknown

a

Isolation of agent (underlined) or detection of specific antibodies (serology). Species that are hunted (commercially or game) in Norway are in bold. See text for specific references.

b

Giardia duodenalis

Toxoplasma gondii

The first study that investigated the occurrence of Giardia in Canadian marine mammals was prompted by the high prevalence of giardiosis in native Inuit on Baffin Island, and epidemics of giardiosis in northern communities in Alaska (Olson et al., 1997). This study also identified Giardia cysts in faeces from 3 of 15 ringed seals (20%), but not from 16 beluga whales. Other studies have detected Giardia in other marine mammals (Measures and Olson, 1999; Appelbee et al., 2005; Hughes-Hanks et al., 2005; Dixon et al., 2008; Gaydos et al., 2008; LasekNesselquist et al., 2008). Prevalences in some species were reported as rather high, being 64.5% in ringed seals and 71.4% in right whales in one study (Hughes-Hanks et al., 2005) and 80% prevalence in ringed seals and 75% prevalence in bearded seals in another study (Dixon et al., 2008). Genotyping studies have mostly detected zoonotic isolates (Dixon et al., 2008; Lasek-Nesselquist et al., 2008; Appelbee et al., 2010), but other studies found no zoonotic genotypes (Gaydos et al., 2008). No cases of transmission of Giardia to humans via infected marine mammals have been documented.

Cases of symptomatic toxoplasmosis have been reported from a range of different species of marine mammals including seals, dolphins and whales (Dubey et al., 2003), while various surveys have reported serological evidence of Toxoplasma gondii infection in a range of marine mammals. Regarding marine mammals in the North Atlantic, a survey including 316 harp seals, 48 ringed seals, 78 hooded seals and 202 minke whales reported all samples to be seronegative (Oksanen et al., 1998). However, a more recent study reported a seroprevalence of 18.7% among ringed seals and 66.7% among adult bearded seals from Svalbard, but no sign of antibodies in bearded seal pups, harbour seals, beluga whales or narwhals from the same area (Jensen et al., 2010). The authors hypothesize that the apparent increase in seroprevalence may be due to warmer water temperatures, resulting in influxes of temperate marine invertebrate filterfeeders that could be vectors for oocysts, as well as potential anthropogenic or zoological factors (Jensen et al., 2010). The mechanism of T. gondii infection in marine mammals has been debated considerably without clear resolution, and it is unknown whether vertical (transplacental)


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transmission is a significant path of infection in these mammals (Fujii et al., 2007). The dietary habits of most marine mammals (eating fish or invertebrates, or being exclusively herbivorous) mean that ingestion of T. gondiiinfected meat is unlikely (Dubey et al., 2003), although it has been postulated for transmission of Trichinella to seals and walrus (see section below). This means that oocysts excreted from felids are the most likely source of infection, possibly concentrated in transport hosts such as filter-feeding molluscs (Robertson, 2007) or fish (Massie et al., 2010). As marine mammals are clearly at risk from infection with T. gondii, there is the potential for zoonotic infection by ingestion of undercooked T. gondii-infected meat. Inuit communities are considered to be particularly at risk. A survey showed almost 60% seropositivity to T. gondii amongst adults living in Nunavik, Quebec, Canada (Messier et al., 2009). This is considered to be relatively high, considering that there is a general absence of felids in the region. An outbreak of toxoplasmosis amongst a small group of pregnant women in Nunavik, identified consumption of dried seal meat and consumption of seal liver as risk factors for becoming seropositive (McDonald et al., 1990). Presently, consumption of seal meat seems a much more important risk factor for human infection than drinking untreated water (Davidson et al., 2011). In Kuujjuaraapik, in Northern Quebec (Nunavik), the T. gondii seroprevalence among Inuit, who have a dietary preference for raw, dried meat from marine mammals, was 80%, while among the Cree population in the same community, with a dietary preference for cooked terrestrial mammals, only 10% were seropositive (Levesque et al., 2007; Messier et al., 2009). However, it should be noted that there are a range of other risk factors for toxoplasmosis, including consumption of a range of other raw or undercooked meats and, in some situations, eating raw vegetables. A study on the infectivity of T. gondii in traditional northern foods (a fermented product, a dried product and a salted and spiced product) prepared with meat from experimentally infected seals found that it was non-infective for cats, despite cats becoming infected when fed the source seal meat raw and without any other preparation (Forbes et al., 2009). Temperature and duration of storage may have reduced the infectivity.

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Transmission of Trichinella spp. is between carnivorous or omnivorous hosts, and therefore, with regards to marine mammals, most infections occur in polar bears and walrus, although benthic bivalve molluscs are the preferred diet of the latter. Of the cetaceans, species such as killer whales (Orcinus orca) are likely candidates for Trichinella infection, due to

their carnivorous diet. However, there is no evidence for Trichinella infection in these whales, nor clinical cases of human trichinellosis associated with them (Forbes, 2000). As seals are generally piscivorous, they are unlikely to be infected with Trichinella. However, various studies have suggested that bearded seals and ringed seals may be occasionally infected (as reviewed by Forbes, 2000), and another study (Moller, 2007) identified T. nativa larvae in muscle tissue samples from one ringed seal and five hooded seals, giving a prevalence of 0.2% and 2.3%, respectively. More recently, a study in the Baltic Sea identified Trichinella nativa in 1 of 171 grey seal samples (Isomursu and Kunnasranta, 2011). Two studies have been conducted on harp and hooded seals from Norwegian hunting areas. Examination of diaphragms from 1955 harp seals and 192 hooded seals between 1949 and 1953 was found negative by trichinoscopy (Thorshaug and Rosted, 1956), while a study from 1992 including 1000 harp seals and 174 hooded seals hunted north of Jan Mayen, and 175 harp seals from the Barents Sea, in which diaphragm samples were analysed using the digestion method, also gave no indication of Trichinella infection (Handeland et al., 1995). It is speculated that natural transmission to seals may occur from occasional scavenging on small amounts of infected tissue from other Arctic mammals, particularly pieces discarded by hunters or left by predators (Kapel et al., 2003), or from ingestion of crustaceans and fish containing low numbers of Trichinella larvae, as these have been shown experimentally to have the potential to act as vectors (Hulebak, 1980). A survey in a hunting community in Greenland demonstrated seroprevalence of below 1.4% in persons under 40 years, but over 12% in persons over 60 years. In addition to increasing age, risk factors were found to be consumption of polar bear meat and occupation as hunter or fisherman (Moller et al., 2010). Most outbreaks of trichinellosis are associated with consumption of walrus meat rather than that from polar bears, as the latter is usually cooked, while walrus is often eaten raw, fermented or airdried (Proulx et al., 2002; Moller et al., 2005). Several outbreaks of trichinellosis associated with consumption of walrus meat have been documented (Margolis et al., 1979; Viallet et al., 1986; MacLean et al., 1989; McDonald et al., 1990; Serhir et al., 2001; Moller et al., 2005). Although one field investigation suggested that traditional preparation processes of walrus meat (fermentation, air-drying, smoking) may result in T. nativa larvae being inactivated (Leclair et al., 2004), another study in laboratory-controlled conditions suggested that Trichinella larvae from experimentally infected seals survived in traditionally prepared foods for at least 5 months (Forbes et al., 2003). Larvae of some species/genotypes of Trichinella are resistant to freezing; indeed, it is well documented that T. nativa larvae are freeze-tolerant for prolonged periods, and it

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has also been demonstrated that they can survive repeated cycles of freeze–thaw (Davidson et al., 2008). Bacteria Salmonella Salmonella has been isolated from many animal species in the marine environment, including marine mammals (Minette, 1986). From published reports, it is clear that whales may be hosts for Salmonella. In Umanak, Greenland, 400 inhabitants acquired salmonellosis after consumption of meat from a stranded, dead beluga whale (Boggild, 1969). In Tununak, Alaska (1972), 99 persons consumed meat and blubber from a stranded whale, and 93 of them became ill, with various symptoms including fever, shivering and diarrhoea. Salmonella enteritidis was cultured both from the food and from rectal swabs from the patients (Bender et al., 1972). In Japan (1950), 172 persons developed salmonellosis after consumption of meat obtained from a moribund whale found floating in the sea (Nakaya, 1950). These examples show that whales may have infections with Salmonella and that whales can be a source of infection for humans. A wide range of Salmonella serovars including S. enteritidis and S. typhimurium, which are known human pathogens, have been isolated from many different seal species (Foster et al., 1998; Aschfalk et al., 2002; Stoddard, 2005; Stoddard et al., 2008a). S. newport, S. bovismorbificans and S. typhimurium have been isolated from harbour seals, and S. typhimurium also from grey seals. However, such isolations have not been reported from the two commercial seal species for Norway, the harp and the hooded seals. A serological survey for Salmonella-specific antibodies in 93 harp seals from the Greenland Sea, using a mixture of LPS-antigen from S. typhimurium and S. cholerasuis, revealed a seroprevalence of 2.2% (Aschfalk et al., 2002), indicating that Salmonella may be present, but are not common pathogens in these seals.


and harp seals from Canada (Forbes et al., 2000) and from minke whale (Clavareau et al., 1998) and hooded seals from the North-East Atlantic Ocean. In the latter case, hooded seals had a prevalence of 38% and bacteria were recovered from a wide range of organs, with the spleen and lung lymph nodes most frequently infected (Tryland et al., 2005). Characterization of isolates obtained from a wide range of marine mammal species, by conventional typing methods, as well as by restriction length fragment polymorphism (RLFP), and by PCR and sequencing, has revealed that they should be classified as distinct species, Brucella ceti and Brucella pinnipedialis in whales and seals, respectively, and not be regarded as classical bacterial species from terrestrial mammals invading new host species (Jahans et al., 1997; Clavareau et al., 1998; Bricker et al., 2000; Maquart et al., 2009). Although marine mammal brucellae infected a laboratory worker (Brew et al., 1999) and have been associated with intracerebral granulomas and spinal osteomyelitis (Sohn et al., 2003; McDonald et al., 2006), the zoonotic potential of the marine Brucella species is unclear. As the clinical picture in humans can be expected to be of a general, flulike character, it may be difficult to associate clinical cases specifically with Brucella infections. Mycobacterium spp

Infections with Brucella spp. have been reported from a wide range of marine mammal species, based on presence of antibodies or the isolation of bacteria (Nymo et al., 2011) (Table 1). As for many terrestrial mammal species, such infections have been associated with reproductive problems in dolphins, such as abortions (Ewalt et al., 1994), whereas no specific pathology has been identified in seals (Nymo et al., 2011). In the North Atlantic, antibodies against Brucella spp. have been detected in minke whales, fin whales and sei whales (Balaenoptera borealis), as well as in harp, hooded and ringed seals (Tryland et al., 1999). Brucella bacteria have been isolated from ringed

Mycobacterial infections in marine mammals are probably transmitted by aerosols in aquariums and rehabilitation facilities and may not be linked to human consumption of marine mammal meat. Nevertheless, such infections represent a threat to humans having close contact with marine mammals (Hunt et al., 2008). Disease associated with M. tuberculosis in marine mammals has mostly occurred in captive settings (Ehlers, 1965; Montali et al., 2001). Tuberculosis caused by M. bovis has been diagnosed in fur seals (Arctocephalus forsteri) and sea lions (Neophoca cinerea), indicating that the animals brought the bacteria into the facility at the time of capture (Cousins et al., 1990). Another report from a marine park documents the transmission of M. bovis from seals with fatal tuberculosis to a seal trainer who then developed pulmonary tuberculosis (Thompson et al., 1993). Characterization of other marine mammal mycobacterial isolates has grouped them as being a novel member of the M. tuberculosis complex, Mycobacterium pinnipedii sp. novum (Cousins et al., 2003; Kiers et al., 2008). Atypical (non-tuberculous) mycobacteria, found in soil and water, have also caused disease in captive seals of different species (Boever et al., 1976; Morales et al., 1985; Gutter et al., 1987; Lewis, 1987).


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Brucella spp


Campylobacter spp There are very few reports of Campylobacter spp. in marine mammals. One report described the isolation of a new species, Campylobacter insulaenigrae sp. nov., from three harbour seals (Phoca vitulina) and a harbour porpoise (Phocoena phocoena) in Scotland (Foster et al., 2004). Campylobacter jejuni, Campylobacter lari and an unknown Campylobacter species have been isolated from northern elephant seals (Mirounga angustirostris) in California (Stoddard, 2005; Stoddard et al., 2008b). There is no documented link between Campylobacter in marine mammals and human disease. Leptospira sp The first reported case of leptospirosis in marine mammals was published in 1971 (Higgins, 2000). Since then, many reports of leptospirosis in pinnipeds have been published, but so far no infections in cetaceans have been described. Infections by L. interrogans serovar Pomona include sea lions (Zalophus californianus) (Gulland et al., 1996) and Northern fur seals (Callorhinus ursinus) (Smith et al., 1974). Smith et al. (1977) reported a herd seroprevalence of L. interrogans serovar Pomona of between 7.0% and 15.4% among adult female Northern fur seals from the Bering Sea. In a study conducted by Bogomolni et al. (2008), tissues from 109 animals, either marine mammals or birds, were examined for Leptospira spp. by molecular methods. Of these samples, 11 samples of nine species were positive for Leptospira spp., including the common dolphin (Delphinus delphis), humpback whale and harp seal. The zoonotic potential of Leptospira spp. from pinnipeds is not clear. However, Messier et al. (2012) reported on the seroprevalence for Leptospira spp. among 917 inhabitants at Nunavik, Quebec (Canada), and found 5.9% of the blood samples to be positive. No association between positive blood samples and food preparation habits, including the handling of raw meat from marine mammals, was detected. Nocardia sp Several Nocardia species have been isolated from the respiratory organs, intestinal tract or from abscesses of pinnipeds and cetaceans (Higgins, 2000; Leger et al., 2009). Nocardia asteroides has been isolated from the respiratory system of a diseased pilot wale (Globicephala melaena), Indo-Pacific bottlenose dolphin (Tursiops adunculus, former T. truncatus) and killer whale and from dolphins, and N. brasiliensis and N. caviae have been found in the pacific bottlenose dolphin (Migaki and Jones, 1983). The number of reported cases among humans has increased during the last two decades, due to a higher number of immunocom384

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promised persons and better diagnostic tools (Sorrell et al., 2010). However, there have been no reports of animal-tohuman transmission of Nocardia sp. (Sorrell et al., 2010). Clostridium botulinum Several authors have reported on the prevalence of C. botulinum in fish and marine mammals (Gram, 2001; Fach et al., 2002; Horowitz, 2010). C. botulinum type E is the most prevalent type found in seafood products from coldwater areas such as Scandinavia (Huss, 1994). The risk of contracting botulism after eating meat from marine mammals in a raw or under-processed state has been documented among the native population of Alaska, Canada and Greenland (Hauschild and Gauvreau, 1985; Shaffer et al., 1990; Sorensen et al., 1993; Johnson, 2007; Horowitz, 2010). From these studies, it can be estimated that up to 60% of the botulism cases were caused by meat from marine mammals that has been incorrectly handled and/or stored, and exacerbated by the use of plastic wrapping that contributes to creating anaerobic storage conditions. In Norway, a total of 35 cases of foodborne botulism, excluding infant botulism, were reported in the period 1977– 2010, but none of these cases were linked to consumption of marine mammals (MSIS, 2011). Coxiella burnetii Coxiella burnetii, the causative agent of the disease ‘Q fever’ in human, has the past few years been detected in several marine mammal species along the Pacific coast of North America. Placentitis was documented in a pregnant Pacific harbour seal (P. v. richardsi) in 1998 (Lapointe et al., 1999). A recent screening of placenta samples for C. burnetii by PCR revealed that coxiella-specific DNA was present in 17 of 27 Pacific harbour seals, two of six harbour porpoises and one of two Steller sea lions (Eumetopias jubatus), and antibodies were detected in harbour seals of both sexes (Kersh et al., 2012). Coxiella burnetii has also been isolated and detected by PCR in placentas from northern fur seals in Alaska (Duncan et al., 2012), and a serological screening revealed antibodies in northern fur seals and Steller sea lions, increasing in fur seals from 49% in 1994 to 69% in 2009 and 2011 (Minor et al., 2013). These findings indicate that Coxiella burnetii may be increasingly common in marine mammals of this region and that the possibility of human exposure exists. Seal finger (blubber finger, «spekkfinger») agent (Mycoplasma spp.) Seal finger is a relatively severe and extremely painful local infection on the hands of persons handling seals or seal © 2013 Blackwell Verlag GmbH Zoonoses and Public Health, 2014, 61, 377–394

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products and has been described in the medical literature since the beginning of the 20th century (Bidenknap, 1907; Candolin, 1953). Most clinical cases have been reported from Scandinavia, Canada and Greenland, but also from Alaska, Falkland Islands and South Georgia (Hartley and Pitcher, 2002). The infectious agent enters through skin abrasions or wounds. After the incubation period (3 days to 3 weeks), the involved finger become red, oedematous and tender, and adjacent finger joints may be involved, which, if untreated, may lead to permanent stiffness of inter-phalangeal joints. The aetiology of seal finger has been a matter of dispute. Micrococcus sp. was suggested over 50 years ago (Thjotta and Kvittingen, 1949), and also Staphylococcus aureus and S. albus (Eadie et al., 1990). The bacterium Erysipelothrix rhusiopathia, associated with whales and other wildlife species (Wood and Shuman, 1981; Hjetland et al., 1995), causes the condition erysipeloid, which may resemble seal finger, with local cellulitis of fingers and hands. All these agents, however, are normally penicillin-sensitive, suggesting another causative agent for seal finger, because seal finger infections do not respond to treatment with penicillin. The drug of choice for seal finger is tetracycline (Krag and Schonheyder, 1996; Baker et al., 1998; Hartley and Pitcher, 2002). In 1990, two identical isolates of Mycoplasma phocacerebrale were obtained from a seal trainer with seal finger and from the mouth of the seal which had bitten her (Madoff et al., 1991; Baker et al., 1998). This, together with isolation of three species of mycoplasma from seals (M. phocidae, M. phocarhinis and M. phocacerebrale) (Madoff et al., 1982; Kirchhoff et al., 1989), suggest that a Mycoplasma sp. is the causative agent of seal finger. This pathogen is the one most commonly transmitted from seals to humans, being an occupational hazard for professional sealers and other persons handling seals and seal products. Viruses Influenza virus Influenza virus is transmitted by direct contact with infected individuals, by contact with contaminated objects and by inhalation of virus-containing aerosols. It would seem unlikely that influenza virus is transferred from marine mammals to humans through hunting activity (sealing and whaling) or through marine mammal meat and products. Influenza A virus is one of few zoonotic pathogens known to have caused epizootics in marine mammals. In 1979–80, more than 400 harbour seals died of acute pneumonia associated with Influenza A virus along the coast of New England, USA (Geraci et al., 1982), and persons handling diseased and dead seals contracted conjunctivitis (Webster et al., 1981). Nucleoproteins of marine mammal influenza viruses have been characterized as avian-like (Lvov et al., 1978; © 2013 Blackwell Verlag GmbH Zoonoses and Public Health, 2014, 61, 377–394


Hinshaw et al., 1984; Callan et al., 1995), supporting the theory of inter-species transmission of Influenza A virus from the avian host reservoir to marine mammals (Mandler et al., 1990). No epizootic due to Influenza A virus among seals has been observed in the North-East Atlantic Ocean or the Barents Sea, but an overall seroprevalence of 18% in harp seals (n = 183) and 8% in hooded seals (n = 100) has been recorded (Stuen et al., 1994). Influenza B virus is a human pathogen with an unknown reservoir in nature. An influenza B virus isolate was obtained from a naturally infected harbour seal in the Netherlands, and seals may thus be one species that can harbour Influenza B virus in nature (Osterhaus et al., 2000). Influenza B virus may also be transmitted from humans to seals (Ohishi et al., 2002). Poxvirus Nodular proliferative skin lesions in seals, reported as ‘sealpox’, have been found in Californian sea lions (Wilson et al., 1969), South American sea lions (Otaria byronia), northern fur seals, harbour seals and grey seals (Wilson and Poglayen-Neuwall, 1971; Wilson et al., 1972; Simpson et al., 1994) (Table 1). The diagnosis has been based on the presence of characteristic skin nodules with a characteristic histopathologic appearance (Okada and Fujimoto, 1984) and verified by the finding of typical parapoxvirus particles (genus Parapoxvirus, family Poxviridae) by negative contrast transmission electron microscopy (Wilson and Sweeney, 1970). Parapoxvirus isolated from seals are called sealpox virus, a tentative species of genus Parapoxvirus (Tryland, 2011a). Following transfer of free-ranging harbour seals from the coast of Germany into a facility, an outbreak of parapoxvirus infection occurred in which 26 animals were affected (Muller et al., 2003). Two persons handling grey seals with sealpox lesions were infected and developed typical nodular lesions on their hands. The lesion on the finger of the first person resolved over a period of 3–4 months, whereas the other experienced several relapses during a period of several months (Hicks and Worthy, 1987). Another marine mammal technician developed parapoxvirus lesions on the hand after being superficially bitten by a captive grey seal, and PCR amplicon analysis indicated homology to parapoxvirus previously isolated from seals (Clark et al., 2005). Calicivirus Calicivirus isolation and calicivirus antibody detection have been conducted in a wide range of seal and whale species (Barlough et al., 1986, 1987, 1998; Smith and Boyt, 1990; 385


O’Hara et al., 1998) (Table 1). After handling northern fur seals (Callorhinus ursinus), a researcher developed flulike illness followed by fluid-filled blisters of 1 cm in diameter on all four extremities, from which a calicivirus was isolated. A comparison of RT-PCR amplicon sequences from the isolate revealed high homology with the calicivirus San Miguel sea lion serotype 5 (Smith et al., 1998). The San Miguel sea lion virus, as well as possibly other caliciviruses in seals and whales, may thus be regarded as potential human pathogens. Close contact with infected seals is probably necessary to be infected, and thus, seal handlers, hunters and researchers are particular risk groups. Rotavirus Rotavirus-specific antibodies have been detected in blood from pups of Galapagos sea lion (Zalophus wollebaeki) and Galapagos fur seals (Arctocephalus galapagoensis), and rotavirus-specific RNA was detected in a rectal swab obtained from a Galapagos sea lion pup (Coria-Galindo et al., 2009). These investigations confirm that rotavirus can be present in seals and sea lions, but whether rotaviruses in marine mammals have the potential to cause human infections is unknown.

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3. Difficulties in removing visible contamination, often untreated seawater is used for this purpose. Dressing is performed on deck, and equipment for the two-knife method routinely used in abattoirs is not installed. Even facilities for washing hands, knives and equipment may be unavailable on deck. Another potential source of contamination is faeces from seabirds, known to harbour potential human pathogens, such as Salmonella and Campylobacter (Kapperud and Rosef, 1983; Refsum et al., 2002). After removing the skin with the blubber, meat from the back is retrieved and further processed for vacuum packing. The fore-flippers and the ribs are removed, without skin and fur, and salted on board. The veterinary inspector on board conducts a general evaluation of the animal (body condition, wounds, signs of disease) before meat for human consumption is processed. In addition, microbiological spot tests, focussing on indicator bacteria for faecal contamination, may be conducted on land by the Norwegian Food Safety Authority. Slaughter and dressing of whales

Seals are killed following a regulated protocol; having been shot, clubbed (by ‘hakapik’ or a special hooked club for pups) and bled on the ice, they are taken on board for further processing. Some hygienic challenges on board are as follows: 1. Time from killing to obtaining the meat, which may vary from minutes to several hours. 2. Lack of dedicated space for trimming and packing the meat. The deck may be contaminated by blood, urine and faeces, and these may contaminate the meat directly or indirectly through contaminated equipment and through handling.

Many of the aspects described for seals are also valid for slaughtering and dressing whales. Whales are killed by a grenade harpoon supplied with 240 g penthrite that explodes inside the animal, preferably in the heart and lung region (Knudsen and Øen, 2003). In the 2001 hunting season, approximately 80% of the whales were killed instantly (Øen, 2002). However, if the whale does not die immediately, a second harpoon is shot, or the animal is towed to the boat and killed by a rifle shot to the brain. The animal is brought on board, and the anal opening is immediately plugged applying a piece of fabric. Subsequently the animal is bled, and the viscera and blubber removed. Then, the whale carcass is deboned and the meat divided into pieces (‘luns’) of 50–100 kg or more, and those pieces are stored on wooden pallets on the deck. The pallets enable air circulation and thus quicker cooling and also hold the meat above the deck surface. Cooling time depends on latitude, season and weather conditions, and during this process, the meat pieces may be covered by plastic or tarpaulins. The working space on the deck is often limited, and the crew may sometimes have to scramble over the meat, especially when several whales are caught during a short period of time. This may increase the risk of contamination of the meat. When handling meat, it is common to use invasive hooks, which are also very handy for handling the intestines and other organs. As contaminated hooks may introduce a deep inoculum and favour anaerobic bacterial growth, Clostridium spp., and especially C. perfringens, faecal streptococci are of particular concern in whale meat control.

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Hygienic Aspects Regarding Slaughtering and Dressing of Seals and Whales During slaughter and dressing of seals and whales, only partial control of pathogenic bacteria can be achieved, compared with slaughtering and dressing of animals in abattoirs. In order for these procedures to be conducted properly, it is important that the operators are skilled and experienced. However, due to the seasonal nature of sealing, obtaining personnel trained in hygienic procedures may be difficult. Thus, comprehensive training programmes for slaughtering and dressing of these animals should be mandatory. Slaughter and dressing of seals

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Thus, using different hooks for different procedures, or ensuring thorough cleaning and disinfection between different operations, is imperative. Similarly, if the shot used for killing the animal results in rupture of the gastro-intestinal tract, contamination with these bacteria may be significant. Contamination of meat during removal of intestines and poor hygiene, in addition to depletion of glycogen reserves during the hunt and agony (which leads to a higher pH), may play a large role as one of the prerequisites for growth of these bacteria on the ‘luns’. If contamination with clostridia is significant and if growing conditions are favourable, considerable quantities of butyric acid and so-called gas meat, containing NH3 and H2S, may be produced. After the storage period on the deck (1–2 days), the meat is stored on ice, for perhaps as long as a few weeks. The meat will usually stay fresh for some days, but will be followed by growth of frigophilic bacteria, which will reduce the quality of the surface. In addition, unprotected whale meat may acquire a rancid taste, due to oxidation of fat. These processes can also occur during long-term storage of frozen meat, depending on the duration of storage, temperature and the amount of unsaturated fatty acids. During storage, most of the whale meat is not surrounded and protected by muscle fasciae, and the surfaces will leach water to the surroundings. Over time, this will result in dehydration of the meat and reduce its quality (‘ice-burning’). Separating the meat and the ice with plastic during on board storage reduces this problem. Whale meat is landed at certified meat plants, where it is subject to organoleptic control by a veterinarian. Smell and taste are checked on a slice of meat obtained from the centre of a ‘luns’, as reduced quality is expected at the meat surface. Control also focusses on gas-producing, anaerobic clostridia, usually indicated by a hollow sound upon percussion of the meat. Measuring the pH of the whale meat might provide information on conditions during the hunt and slaughter of a particular whale. A study by Flisnes (1994) showed that typical pH values in minke whale meat were between 5.5 and 5.9, with some individuals having a pH as high as 6.0– 7.0. The latter values may be related to the hunt, the time from shooting the whale until death and also the nutritional status of the whale. In a hygienic context, pH values higher than six might also encourage growth of cold-tolerant pathogens. Superficial parts of the meat ‘luns’ are usually discarded. The rest is sorted into different beef qualities of different sizes, wrapped and sold fresh or frozen. Bacteriological tests are usually only conducted under particular circumstances, or as spot tests, conducted by the Norwegian Food Safety Authority. © 2013 Blackwell Verlag GmbH Zoonoses and Public Health, 2014, 61, 377–394


Indicator organisms and meat control findings Foodborne infectious agents are often transmitted by contamination of foods by faecal material. Bacteria can also be disseminated due to rupture of the gastro-intestinal tract by missiles, as well as via contamination during the slaughter and dressing procedures. Several groups of microorganisms are used as indicators of faecal contamination in foods, of which the most common ones are coliforms, Escherichia coli, cocci of faecal origin (enterococci, faecal streptococci), clostridia and faecal bacteriophages. Based upon available data from spot tests of whale and seal meat in Norway, the microbiological quality has generally been regarded as good. However, very few spot controls have been conducted, and only a very restricted range of bacteria, and no parasites or viruses, have been addressed. In seals, coliform bacteria and Aeromonas hydrophila have been detected, but investigations for Salmonella, Yersinia enterocolitica and Listeria monocytogenes have been negative (Tryland et al., 2011b). During summer 2002, three series of samples from minke whales landed at the same processing plant were subject to microbiological quality control, and the results between the original ‘luns’ and the same meat packed in consumer packages were compared. Staphylococcus sp. was isolated from one ‘luns’, but not from the corresponding consumer package. Vibrio spp. and Aeromonas spp. were isolated from five and ten samples, respectively, but Salmonella, Listeria monocytogenes or Clostridium spp. were not detected. Coliform bacteria were detected from both ‘luns’ and consumer packages. This comparison indicated that surface trimming of the ‘luns’ is an efficient approach to reducing the bacterial flora in consumer packages (Tryland et al., 2011b).

Discussion Transmission of pathogens to humans In Norway, except for cases of ‘seal finger’, which are probably under-reported due to self-treatment with antibiotics on board the vessels, the incidence of zoonotic infections acquired from marine mammals is largely unknown. This includes whalers, sealers, researchers and persons handling skins and other products, as well as consumers of marine mammal meat. The most important source of information on zoonoses in Norway is an official monitoring system for infectious disease (MSIS), which collates notifications from physicians, microbiological laboratories and hospitals. For diseases that are notifiable to MSIS, the degree of underreporting varies considerably. Factors that affect reporting probably include the severity of the disease, the sensitivity of the diagnostic methods and the agents considered by medical diagnostic laboratories, and for some diseases, the 387


numbers reported to MSIS probably represent only a small fraction of the actual cases. It is often difficult to identify the sources of infection, particularly for sporadic cases, and many illnesses caused by microorganisms associated with marine mammals are not notifiable to MSIS. Thus, based on the MSIS reporting system alone, there is no evidence that indicates that microorganisms from marine mammals pose a significant risk to Norwegian consumers or marine mammal workers. Occurrence, prevalence and incidence of pathogens: not a static issue

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one infectious agent in one population and investigate a restricted number of individuals. In addition, the hygienic quality control and food safety procedures of marine mammal meat are limited. Results and information from these procedures are difficult to obtain and are of modest value in terms of number of animals tested. Data from quality control testing are also difficult to compare due to a lack of standardization in procedures, and no real systematic investigations have been reported in recent times. The range of infectious organisms tested for in marine mammal meat is also limited, traditionally focussing on Trichinella spp. (Thorshaug and Rosted, 1956; Handeland et al., 1995), general bacterial counts (colony forming units; CFU) and faecal indicator organisms, although some analyses have been conducted for sulphur-reducing Clostridium spp. and, in some cases, Salmonella, Listeria monocytogenes and Yersinia enterocolitica.

Through their varied prey, including fish, squid, crustaceans, shellfish and plankton, marine mammals have broad contact with other species in the marine food web. In addition, many marine mammal species, such as the pelagic harp and hooded seals and minke whales, undertake seasonal migrations over huge distances, thereby coming into contact with a range of environments and ecosystems, including other marine mammal populations. Thus, they are exposed to substances and infectious agents that have originated far from our waters. Infectious agents may also change their distribution through changes in the ecosystems. Climate change, resulting in higher water temperatures, has probably increased the northern distribution of several fish species (Loeng and Drinkwater, 2007; Ellingsen et al., 2008). This may also affect marine mammals that prey on fish and also probably contributes to a different distribution of infectious agents (De La Rocque, 2008; Tryland et al., 2009; Jensen et al., 2010). Tourism, the discharge of ballast water from boats, increased cargo transport at sea, the oil exploration industry and new sea routes, such as the prospective use of an ice-free Northeast Passage, may also contribute to the transport and introduction of infectious agents in marine ecosystems. Further, the exposure of marine mammals to compounds such as oil, heavy metals and persistent organohalogen contaminants (OHCs) (Skaare et al., 2002; Letcher et al., 2010) may, through immunomodulation, affect the ability of marine mammals to resist infections (Ross et al., 1996; de Swart et al., 1996; Das et al., 2008).

The wide range of parasites, bacteria and viruses that infect seals and whales, and that are also potential human pathogens (Table 1), suggests a need for systematic epidemiological studies. The most important zoonotic pathogens that can be transferred to humans from marine mammal meat appear to be Trichinella spp., Toxoplasma gondii, Salmonella and Leptospira spp. For other potential pathogens, such as Brucella pinnipedialis, their zoonotic potential is uncertain. Other human pathogens found in marine mammals, such as Cryptosporidium spp. and Giardia duodenalis, may be considered as minor threats, as they are generally not transmitted through consumption of meat and meat products. These parasites, and most other pathogens, are generally heat sensitive and represent minor threats if marine mammal meat and products are heat-treated. Some pathogens are probably better classified as occupational hazards, such as Mycoplasma spp., influenza A virus, calicivirus and poxvirus. Broad-scale research projects that focus on human pathogens will increase our knowledge of the risks that these human pathogens represent and also provide reference data that can be used for comparisons over time.

Lack of data and knowledge gaps

Critical points: killing, dressing, handling and storage

It is evident that there is a general lack of data on the occurrence and possible effect of human pathogens in marine mammal meat and products. Although some scientific investigations have included a reasonable number of individuals, several animal species and different sampling years (Handeland et al., 1995; Oksanen et al., 1998; Tryland et al., 1999), most scientific reports usually focus on only

Many factors, such as the killing, bleeding and evisceration of the animal, as well as handling, processing and storage of marine mammal meat, affect the contamination, survival and possible growth of potential human pathogens. Contamination of meat with pathogens from the skin and the alimentary tract of the animal, the environment (in particular contaminants from birds and water), equipment and

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personnel is considered both possible and likely on board sealing and whaling vessels. Meat from seals is generally assumed to be of good microbiological status, given that the animal is healthy, that the meat is not contaminated by faeces during killing and that the animal has been bled properly. As meat from seals is usually frozen on board, following dressing and consumer-packaging, this product may be similar in food safety quality to that from domestic animals slaughtered in abattoirs. Meat from whales may be exposed to more food safety challenges during processing, due to vessel space limitations for handling large animals, open air cooling on deck, handling with invasive tools and storage for weeks on ice before processing on land. It is also possible that psychrophilic bacteria may be active and multiply during storage on ice. Freezing meat from minke whales on board is currently not allowed by Norwegian authorities. Although it may seem obvious that freezing of whale meat on board would maintain the microbiological quality and reduce wastage when the meat is processed, it may also affect the ageing of the meat, as well as logistical limitations due to the size of the vessels.


References

Based on reports from Norwegian Food Safety Authority, it seems that meat quality control, as conducted today, does not adequately address both human pathogens in the animals and faecal contamination, that is, indicator organisms. There is a long history of whaling and sealing in Norway; this activity is regarded as a natural approach to harvesting from marine resources and may be an important source of income for some communities. It is thus important to ensure that these hunts, and subsequent quality controls, are conducted such that the marine mammal products obtained are safe for human consumption. The personnel involved in sealing and whaling are not professional slaughterhouse workers, and proper training is crucial for ensuring good hygiene during all the relevant processes. It is important that unhealthy animals are recognized and that moribund individuals, animals with poor body condition, severe wounds, trauma or abscesses are separated from further processing. In recent years, Norwegian sealing and whaling have not been limited by the quotas set by the authorities, but rather by the market situation, that is, restrictions and difficulties in export, and reduced interest in the national market. Nevertheless, a sustainable future market will demand documentation of safety and quality of seal and whale meat, including knowledge regarding the presence of zoonotic pathogens.

Appelbee, A. J., R. C. Thompson, and M. E. Olson, 2005: Giardia and Cryptosporidium in mammalian wildlife – current status and future needs. Trends Parasitol. 21, 370–376. Appelbee, A. J., R. C. A. Thompson, L. M. Measures, and M. E. Olson, 2010: Giardia and Cryptosporidium in harp and hooded seals from the Gulf of St. Lawrence, Canada. Vet. Parasitol. 173, 19–23. Aschfalk, A., L. Folkow, H. Rud, and N. Denzin, 2002: Apparent seroprevalence of Salmonella spp. in harp seals in the Greenland Sea as determined by enzyme-linked immunosorbent assay. Vet. Res. Commun. 26, 523–530. Baker, A. S., K. L. Ruoff, and S. Madoff, 1998: Isolation of Mycoplasma species from a patient with seal finger. Clin. Infect. Dis. 27, 1168–1170. Barlough, J. E., E. S. Berry, D. E. Skilling, A. W. Smith, and F. H. Fay, 1986: Antibodies to marine caliciviruses in the Pacific walrus (Odobenus rosmarus divergens Illiger). J. Wildl. Dis. 22, 165–168. Barlough, J. E., E. S. Berry, A. W. Smith, and D. E. Skilling, 1987: Prevalence and distribution of serum neutralizing antibodies to Tillamook (bovine) calicivirus in selected populations of marine mammals. J. Wildl. Dis. 23, 45–51. Barlough, J. E., D. O. Matson, D. E. Skilling, T. Berke, E. S. Berry, R. F. Brown, and A. W. Smith, 1998: Isolation of reptilian calicivirus Crotalus type 1 from feral pinnipeds. J. Wildl. Dis. 34, 451–456. Bender, T. R., T. S. Jones, W. E. DeWitt, G. J. Kaplan, A. R. Saslow, S. E. Nevius, P. S. Clark, and E. J. Gangarosa, 1972: Salmonellosis associated with whale meat in an Eskimo community. Serologic and bacteriologic methods as adjuncts to an epidemiologic investigation. Am. J. Epidemiol. 96, 153– 160. Bidenknap, J. H. 1907: Spækflegmonen (de norske ishavsfareres Spækfinger). Nor. Mag. Lægevidenskap. 68, 515–523 Boever, W. J., C. O. Thoen, and J. D. Wallach, 1976: Mycobacterium chelonei infection in a natterer manatee. J. Am. Vet. Med. Assoc. 169, 927–929. Boggild, J., 1969: Hygienic problems in Greenland. Arch. Environ. Health 18, 138–143. Bogomolni, A. L., R. J. Gast, J. C. Ellis, M. Dennett, K. R. Pugliares, B. J. Lentell, and M. J. Moore, 2008: Victims or vectors: a survey of marine vertebrate zoonoses from coastal waters of the Northwest Atlantic. Dis. Aquat. Org. 81, 13–38. Brew, S. D., L. L. Perrett, J. A. Stack, A. P. MacMillan, and N. J. Staunton, 1999: Human exposure to Brucella recovered from a sea mammal. Vet. Rec. 144, 483. Bricker, B. J., D. R. Ewalt, A. P. MacMillan, G. Foster, and S. Brew, 2000: Molecular characterization of Brucella strains isolated from marine mammals. J. Clin. Microbiol. 38, 1258– 1262. Callan, R. J., G. Early, H. Kida, and V. S. Hinshaw, 1995: The appearance of H3 influenza viruses in seals. J. Gen. Virol. 76 (Pt 1), 199–203.


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Limited meat quality control and training


M. Tryland et al.

Candolin, Y., 1953: Seal finger (Spekkfinger) and its occurrence in the Gulfs of the Baltic Sea. Acta. Chir. Scand. Suppl. 177, 1–51. Clark, C., P. G. McIntyre, A. Evans, C. J. McInnes, and S. LewisJones, 2005: Human sealpox resulting from a seal bite: confirmation that sealpox virus is zoonotic. Br. J. Dermatol. 152, 791–793. Clavareau, C., V. Wellemans, K. Walravens, M. Tryland, J. M. Verger, M. Grayon, A. Cloeckaert, J. J. Letesson, and J. Godfroid, 1998: Phenotypic and molecular characterization of a Brucella strain isolated from a minke whale (Balaenoptera acutorostrata). Microbiology 144(Pt 12), 3267–3273. Coria-Galindo, E., E. Rangel-Huerta, A. Verdugo-Rodriguez, D. Brousset, S. Salazar, and L. Padilla-Noriega, 2009: Rotavirus infections in Galapagos sea lions. J. Wildl. Dis. 45, 722–728. Cousins, D. V., B. R. Francis, B. L. Gow, D. M. Collins, C. H. McGlashan, A. Gregory, and R. M. Mackenzie, 1990: Tuberculosis in captive seals: bacteriological studies on an isolate belonging to the Mycobacterium tuberculosis complex. Res. Vet. Sci. 48, 196–200. Cousins, D. V., R. Bastida, A. Cataldi, V. Quse, S. Redrobe, S. Dow, P. Duignan, A. Murray, C. Dupont, N. Ahmed, D. M. Collins, W. R. Butler, D. Dawson, D. Rodriguez, J. Loureiro, M. I. Romano, A. Alito, M. Zumarraga, and A. Bernardelli, 2003: Tuberculosis in seals caused by a novel member of the Mycobacterium tuberculosis complex: Mycobacterium pinnipedii sp. nov.. Int. J. Syst. Evol. Microbiol. 53, 1305–1314. Das, K., U. Siebert, A. Gillet, A. Dupont, C. Dipoi, S. Fonfara, G. Mazzucchelli, E. De Pauw, and M. C. De Pauw-Gillet, 2008: Mercury immune toxicity in harbour seals: links to in vitro toxicity. Environ. Health 7, 52. Davidson, R. K., K. Handeland, and C. M. Kapel, 2008: High tolerance to repeated cycles of freezing and thawing in different Trichinella nativa isolates. Parasitol. Res. 103, 1005–1010. Davidson, R., M. Simard, S. J. Kutz, C. M. O. Kapel, I. S. Hamnes, and L. J. Robertson, 2011: Arctic parasitology: why should we care? Trends Parasitol. 27, 238–244. De La Rocque, S., 2008: Climate change: impact on the epidemiology and control of animal diseases – Introduction. Rev. Sci. Tech. 27, 303–304. Deng, M. Q., R. P. Peterson, and D. O. Cliver, 2000: First findings of Cryptosporidium and Giardia in California sea lions (Zalophus californianus). J. Parasitol. 86, 490–494. Dixon, B. R., L. J. Parrington, M. Parenteau, D. Leclair, M. Santin, and R. Fayer, 2008: Giardia duodenalis and Cryptosporidium spp. in the intestinal contents of ringed seals (Phoca hispida) and bearded seals (Erignathus barbatus) in Nunavik, Quebec, Canada. J. Parasitol. 94, 1161–1163. Dubey, J. P., R. Zarnke, N. J. Thomas, S. K. Wong, B. W. Van, M. Briggs, J. W. Davis, R. Ewing, M. Mense, O. C. Kwok, S. Romand, and P. Thulliez, 2003: Toxoplasma gondii, Neospora caninum, Sarcocystis neurona, and Sarcocystis canis-like infections in marine mammals. Vet. Parasitol. 116, 275–296. Duncan, C., G. J. Kersh, T. Spraker, K. A. Patyk, K. A. Fitzpatrick, R. F. Massung, and T. Gelatt, 2012: Coxiella burnetii in

northern fur seal (Callorhinus ursinus) placentas from St. Paul Island, Alaska. Vector Borne Zoonotic Dis. 12, 192–195. Eadie, P. A., T. C. Lee, Z. Niazi, and D. Lawlor, 1990: Seal finger in a wildlife ranger. Ir. Med. J. 83, 117–118. Ehlers, K., 1965: Records of the hooded seal (Cystophora cristata) and other animals in Bremerhavens Zoo. Intern. Zoo Yearbook 5, 149–152. Ellingsen, I., P. Dalpadado, D. Slagstad, and H. Loeng, 2008: Impact of climatic change on the biological production in the Barents Sea. Clim. Change 87, 155–175. Ewalt, D. R., J. B. Payeur, B. M. Martin, D. R. Cummins, and W. G. Miller, 1994: Characteristics of a Brucella species from a bottlenose dolphin (Tursiops truncatus). J. Vet. Diagn. Invest. 6, 448–452. Fach, P., S. Perelle, F. Dilasser, J. Grout, C. Dargaignaratz, L. Botella, J. M. Gourreau, F. Carlin, M. R. Popoff, and V. Broussolle, 2002: Detection by PCR-enzyme-linked immunosorbent assay of Clostridium botulinum in fish and environmental samples from a coastal area in northern France. Appl. Environ. Microbiol. 68, 5870–5876. Flisnes, G. 1994: Laboratoriekontroll av hvalkjøtt. Notes presented on the postgraduation course Meat Control in Marine Mammals, The Norwegian Veterinary AssociationTromsø, Norway, April. 11–12. Forbes, L. B., 2000: The occurrence and ecology of Trichinella in marine mammals. Vet. Parasitol. 93, 321–334. Forbes, L. B., O. Nielsen, L. Measures, and D. R. Ewalt, 2000: Brucellosis in ringed seals and harp seals from Canada. J. Wildl. Dis. 36, 595–598. Forbes, L. B., L. Measures, A. Gajadhar, and C. Kapel, 2003: Infectivity of Trichinella nativa in traditional northern (country) foods prepared with meat from experimentally infected seals. J. Food Prot. 66, 1857–1863. Forbes, L. B., L. Measures, and A. Gajadhar, 2009: Infectivity of Toxoplasma gondii in northern traditional (country) foods prepared with meat from experimentally infected seals. J. Food Prot. 72, 1756–1760. Foster, G., H. M. Ross, I. A. Patterson, R. J. Reid, and D. S. Munro, 1998: Salmonella typhimurium DT104 in a grey seal. Vet. Rec. 142, 615. Foster, G., B. Holmes, A. G. Steigerwalt, P. A. Lawson, P. Thorne, D. E. Byrer, H. M. Ross, J. Xerry, P. M. Thompson, and M. D. Collins, 2004: Campylobacter insulaenigrae sp. nov., isolated from marine mammals. Int. J. Syst. Evol. Microbiol. 54, 2369–2373. Fujii, K., C. Kakumoto, M. Kobayashi, S. Saito, T. Kariya, Y. Watanabe, X. Xuan, I. Igarashi, and M. Suzuki, 2007: Seroepidemiology of Toxoplasma gondii and Neospora caninum in seals around Hokkaido, Japan. J. Vet. Med. Sci. 69, 393–398. Gaydos, J. K., W. A. Miller, C. Johnson, H. Zornetzer, A. Melli, A. Packham, S. J. Jeffries, M. M. Lance, and P. A. Conrad, 2008: Novel and canine genotypes of Giardia duodenalis in harbor seals (Phoca vitulina richardsi). J. Parasitol. 94, 1264–1268. Geraci, J. R., D. J. St Aubin, I. K. Barker, R. G. Webster, V. S. Hinshaw, W. J. Bean, H. L. Ruhnke, J. H. Prescott, G. Early,

390


M. Tryland et al.


A. S. Baker, S. Madoff, and R. T. Schooley, 1982: Mass mortality of harbor seals: pneumonia associated with influenza A virus. Science 215, 1129–1131. Gram, L., 2001: Potential hazards in cold-smoked fish: Clostridium botulinum type E. J. Food Sci. 66, 1082–1087. Gulland, F. M., M. Koski, L. J. Lowenstine, A. Colagross, L. Morgan, and T. Spraker, 1996: Leptospirosis in California sea lions (Zalophus californianus) stranded along the central California coast, 1981–1994. J. Wildl. Dis. 32, 572–580. Gutter, A. E., S. K. Wells, and T. R. Spraker, 1987: Generalised mycobacteriosis in a California Sea Lion (Zalophus californicus). J. Zoo Anim. Med. 18, 120. Handeland, K., T. Slettbakk, and O. Helle, 1995: Freeze-resistant Trichinella (Trichinella nativa) established on the Scandinavian peninsula. Acta Vet. Scand. 36, 149–151. Hartley, J. W., and D. Pitcher, 2002: Seal finger–tetracycline is first line. J. Infect. 45, 71–75. Hauschild, A. H., and L. Gauvreau, 1985: Food-borne botulism in Canada, 1971–84. Can. Med. Assoc. J. 133, 1141–1146. Hicks, B. D., and G. A. Worthy, 1987: Sealpox in captive grey seals (Halichoerus grypus) and their handlers. J. Wildl. Dis. 23, 1–6. Higgins, R., 2000: Bacteria and fungi of marine mammals: a review. Can. Vet. J. 41, 105–116. Hill, B. D., I. R. Fraser, and H. C. Prior, 1997: Cryptosporidium infection in a dugong (Dugong dugon). Aust. Vet. J. 75, 670–671. Hinshaw, V. S., W. J. Bean, R. G. Webster, J. E. Rehg, P. Fiorelli, G. Early, J. R. Geraci, and D. J. St Aubin, 1984: Are seals frequently infected with avian influenza viruses? J. Virol. 51, 863–865. Hjetland, R., E. Søgnen, and V. V age 1995: Erysipelothrix rhusiopathiae – arsak til erysipeloid og endokarditt. Tidsskr. Norske Læge. pp. 2780–2782. Horowitz, B. Z., 2010: Type E botulism. Clin. Toxicol. (Phila) 48, 880–895. Hughes-Hanks, J. M., L. G. Rickard, C. Panuska, J. R. Saucier, T. M. O’Hara, L. Dehn, and R. M. Rolland, 2005: Prevalence of Cryptosporidium spp. and Giardia spp. in five marine mammal species. J. Parasitol. 91, 1225–1228. Hulebak, K. L., 1980: Mechanical transmission of larval Trichinella by arctic crustacea. Can. J. Zoolog. 58, 1388–1390. Hunt, T. D., M. H. Ziccardi, F. M. Gulland, P. K. Yochem, D. W. Hird, T. Rowles, and J. A. Mazet, 2008: Health risks for marine mammal workers. Dis. Aquat. Org. 81, 81–92. Huss, H. H., 1994: Assurance of food safety. FAO Fish. Tech. Paper 334, 8–26. Isomursu, M., and M. Kunnasranta, 2011: Trichinella nativa in grey seal Halichoerus grypus: spill-over from a highly endemic terrestrial ecosystem. J. Parasitol. 97, 735–736. Jahans, K. L., G. Foster, and E. S. Broughton, 1997: The characterisation of Brucella strains isolated from marine mammals. Vet. Microbiol. 57, 373–382. Jensen, S. K., J. Aars, C. Lydersen, K. M. Kovacs, and K. Asbakk, 2010: The prevalence of Toxoplasma gondii in polar bears and their marine mammal prey: evidence for a marine transmission pathway? Polar Biol. 33, 599–606.

Johnson, E. A., 2007: Clostridium botulinum. In: Doyle, M. P., and L. R. Beuchat (eds), Food microbilogy, Fundamentals and Frontiers, pp. 401–421. ASM Press, Washington. Kapel, C. M., L. Measures, L. N. Moller, L. Forbes, and A. Gajadhar, 2003: Experimental Trichinella infection in seals. Int. J. Parasitol. 33, 1463–1470. Kapperud, G., and O. Rosef, 1983: Avian wildlife reservoir of Campylobacter fetus subsp. jejuni, Yersinia spp., and Salmonella spp. in Norway. Appl. Environ. Microbiol. 45, 375–380. Kersh, G. J., D. M. Lambourn, S. A. Raverty, K. A. Fitzpatrick, J. S. Self, A. M. Akmajian, S. J. Jeffries, J. Huggins, C. P. Drew, S. R. Zaki, and R. F. Massung, 2012: Coxiella burnetii infection of marine mammals in the Pacific Northwest, 1997–2010. J. Wildl. Dis. 48, 201–206. Kiers, A., A. Klarenbeek, B. Mendelts, D. van Soolingen, and G. Ko€eter, 2008: Transmission of Mycobacterium pinnipedii to humans in a zoo with marine mammals. Int. J. Tuberc. Lung Dis. 12, 1469–1473. Kirchhoff, H., A. Binder, B. Liess, K. T. Friedhoff, J. Pohlenz, M. Stede, and T. Willhaus, 1989: Isolation of mycoplasmas from diseased seals. Vet. Rec. 124, 513–514. Knudsen, S. K., and E. O. Øen, 2003: Blast-induced neurotrauma in whales. Neurosci. Res. 46, 377–386. Krag, M. L., and H. C. Schonheyder, 1996: Seal fingers and other infections transmitted from seals. Ugeskr. Laeg. 158, 5015–5017. Lapointe, J. M., F. M. Gulland, D. M. Haines, B. C. Barr, and P. J. Duignan, 1999: Placentitis due to Coxiella burnetii in a pacific harbor seal (Phoca vitulina richardsi). J. Vet. Diagn. Invest. 11, 541–543. Lasek-Nesselquist, E., A. L. Bogomolni, R. J. Gast, D. M. Welch, J. C. Ellis, M. L. Sogin, and M. J. Moore, 2008: Molecular characterization of Giardia intestinalis haplotypes in marine animals: variation and zoonotic potential. Dis. Aquat. Org. 81, 39–51. Leclair, D., L. B. Forbes, S. Suppa, J. F. Proulx, and A. A. Gajadhar, 2004: A preliminary investigation on the infectivity of Trichinella larvae in traditional preparations of walrus meat. Parasitol. Res. 93, 507–509. Leger, J. A. S., L. Begeman, M. Fleetwood, S. Frasca, M. M. Garner, S. Lair, S. Trembley, M. J. Linn, and K. A. Terio, 2009: Comparative pathology of nocardiosis in marine mammals. Vet. Pathol. 46, 299–308. Letcher, R. J., J. O. Bustnes, R. Dietz, B. M. Jenssen, E. H. Jorgensen, C. Sonne, J. Verreault, M. M. Vijayan, and G. W. Gabrielsen, 2010: Exposure and effects assessment of persistent organohalogen contaminants in arctic wildlife and fish. Sci. Total Environ. 408, 2995–3043. Levesque, B., V. Messier, Y. Bonnier-Viger, M. Couillard, S. Cote, B. J. Ward, M. D. Libman, S. Gingras, D. Dick, and E. Dewailly, 2007: Seroprevalence of zoonoses in a Cree community (Canada). Diagn. Microbiol. Infect. Dis. 59, 283–286. Lewis, J. C. M., 1987: Cutaneous mycobacteriosis in a southern sea lion. Aquat. Mammals 13, 105–108. Loeng, H., and K. Drinkwater, 2007: An overview of the ecosystems of the Barents and Norwegian Seas and their response to


391


M. Tryland et al.

climate variability. Deep Sea Res. Part 2 Top. Stud. Oceanogr. 54, 2478–2500. Lvov, D. K., V. M. Zdanov, A. A. Sazonov, N. A. Braude, E. A. Vladimirtceva, L. V. Agafonova, E. I. Skljanskaja, N. V. Kaverin, V. I. Reznik, T. V. Pysina, A. M. Oserovic, A. A. Berzin, I. A. Mjasnikova, R. Y. Podcernjaeva, S. M. Klimenko, V. P. Andrejev, and M. A. Yakhno, 1978: Comparison of influenza viruses isolated from man and from whales. Bull. World Health Organ. 56, 923–930. MacLean, J. D., J. Viallet, C. Law, and M. Staudt, 1989: Trichinosis in the Canadian Arctic: report of five outbreaks and a new clinical syndrome. J. Infect. Dis. 160, 513–520. Madoff, S., R. T. Schooley, and H. L. Ruhnke, 1982: Mycoplasmal pneumonia in phocid (harbour) seals. Rev. Infect. Dis. 4 (Suppl), 241. Madoff, S., K. Ruoff, and A. S. Baker, 1991: Isolation of a Mycoplasma species from a case of seal finger. Abstract of the annual meeting of the American Society for Microbiology, Dallas, Texas, 1991, May 5–9; pp. 135. Mandler, J., O. T. Gorman, S. Ludwig, E. Schroeder, W. M. Fitch, R. G. Webster, and C. Scholtissek, 1990: Derivation of the nucleoproteins (NP) of influenza A viruses isolated from marine mammals. Virology 176, 255–261. Maquart, M., F. P. Le, G. Foster, M. Tryland, F. Ramisse, B. Djonne, D. S. Al, I. Jacques, H. Neubauer, K. Walravens, J. Godfroid, A. Cloeckaert, and G. Vergnaud, 2009: MLVA-16 typing of 295 marine mammal Brucella isolates from different animal and geographic origins identifies 7 major groups within Brucella ceti and Brucella pinnipedialis. BMC Microbiol. 9, 145. Margolis, H. S., J. P. Middaugh, and R. D. Burgess, 1979: Arctic trichinosis: two Alaskan outbreaks from walrus meat. J. Infect. Dis. 139, 102–105. Massie, G. N., M. W. Ware, E. N. Villegas, and M. W. Black, 2010: Uptake and transmission of Toxoplasma gondii oocysts by migratory, filter-feeding fish. Vet. Parasitol. 169, 296–303. McDonald, J. C., T. W. Gyorkos, B. Alberton, J. D. MacLean, G. Richer, and D. Juranek, 1990: An outbreak of toxoplasmosis in pregnant women in northern Quebec. J. Infect. Dis. 161, 769–774. McDonald, W. L., R. Jamaludin, G. Mackereth, M. Hansen, S. Humphrey, P. Short, T. Taylor, J. Swingler, C. E. Dawson, A. M. Whatmore, E. Stubberfield, L. L. Perrett, and G. Simmons, 2006: Characterization of a Brucella sp. strain as a marinemammal type despite isolation from a patient with spinal osteomyelitis in New Zealand. J. Clin. Microbiol. 44, 4363–4370. Measures, L. N., and M. Olson, 1999: Giardiasis in pinnipeds from eastern Canada. J. Wildl. Dis. 35, 779–782. Messier, V., B. Levesque, J. F. Proulx, L. Rochette, M. D. Libman, B. J. Ward, B. Serhir, M. Couillard, N. H. Ogden, E. Dewailly, B. Hubert, S. Dery, C. Barthe, D. Murphy, and B. Dixon, 2009: Seroprevalence of Toxoplasma gondii among Nunavik Inuit (Canada). Zoonoses Public Health 56, 188–197. Messier, V., B. Levesque, J. F. Proulx, L. Rochette, B. Serhir, M. Couillard, B. J. Ward, M. D. Libman, E. Dewailly, and S. Dery,

2012: Seroprevalence of Seven Zoonotic Infections in Nunavik, Quebec (Canada). Zoonoses Public Health 59, 107–117. Migaki, M., and S. R. Jones, 1983: Mycotic diseases in marine mammals. In: Howard, E. B. (ed.), Pathobiology of Marine Mammal Diseases, pp. 1–25. CRC Press, Boca Raton, Florida, USA. Minette, H. P., 1986: Salmonellosis in the marine environment. A review and commentary. Int. J. Zoonoses. 13, 71–75. Minor, C., G. J. Kersh, T. Gelatt, A. V. Kondas, K. L. Pabilonia, C. B. Weller, B. R. Dickerson, and C. G. Duncan, 2013: Coxiella burnetii in Northern fur seals and Steller sea lions of Alaska. J. Wildl. Dis. 49, 441–446. Moller, L. N., 2007: Epidemiology of Trichinella in Greenland– occurrence in animals and man. Int. J. Circumpolar Health 66, 77–79. Moller, L. N., E. Petersen, C. M. Kapel, M. Melbye, and A. Koch, 2005: Outbreak of trichinellosis associated with consumption of game meat in West Greenland. Vet. Parasitol. 132, 131–136. Moller, L. N., A. Koch, E. Petersen, T. Hjuler, C. M. Kapel, A. Andersen, and M. Melbye, 2010: Trichinella infection in a hunting community in East Greenland. Epidemiol. Infect. 138, 1252–1256. Montali, R. J., S. K. Mikota, and L. I. Cheng, 2001: Mycobacterium tuberculosis in zoo and wildlife species. Rev. Sci. Tech. 20, 291–303. Morales, P., S. H. Madin, and A. Hunter, 1985: Systemic Mycobacterium marinum infection in an Amazon manatee. J. Am. Vet. Med. Assoc. 187, 1230–1231. Morgan, U. M., L. Xiao, B. D. Hill, P. O’Donoghue, J. Limor, A. Lal, and R. C. Thompson, 2000: Detection of the Cryptosporidium parvum “human” genotype in a dugong (Dugong dugon). J. Parasitol. 86, 1352–1354. MSIS, 2011: Norwegian Surveillance System for Communicable Diseases (MSIS), at www.fhi.no, (accessed December 2011). Muller, G., S. Groters, U. Siebert, T. Rosenberger, J. Driver, M. Konig, P. Becher, U. Hetzel, and W. Baumgartner, 2003: Parapoxvirus infection in harbor seals (Phoca vitulina) from the German North Sea. Vet. Pathol. 40, 445–454. Nakaya, R., 1950: Salmonella enteritidis in a whale. Jpn. Med. J. (Natl. Inst. Health Jpn.) 3, 279–280. Nilssen, K. T., and A. Bjørge, 2010: Sel- havert og steinkobbe (in Norwegian). Fisken og havet. Særnummer 1–2010, 142–143. Nilssen, K. T., and T. Haug, 2007: Status of grey seals (Halichoerus grypus) in Norwegian waters. NAMMCO Sci. Publ. 6, 23–31. Nymo, I. H., M. Tryland, and J. Godfroid, 2011: A review of Brucella infection in marine mammals, with special emphasis on Brucella pinnipedialis in the hooded seal (Cystophora cristata). Vet. Res. 42, 93. Øen, E. O. 2002. Norwegian whaling in 2001. Rep. Int. Whaling Comm. IWC/54/WKM&AWI 6 O’Hara, T. M., C. House, J. A. House, R. S. Suydam, and J. C. George, 1998: Viral serologic survey of bowhead whales in Alaska. J. Wildl. Dis. 34, 39–46. Ohishi, K., A. Ninomiya, H. Kida, C. H. Park, T. Maruyama, T. Arai, E. Katsumata, T. Tobayama, A. N. Boltunov, L. S.

392


M. Tryland et al.


Khuraskin, and N. Miyazaki, 2002: Serological evidence of transmission of human influenza a and B viruses to Caspian seals (Phoca caspica). Microbiol. Immunol. 46, 639–644. Okada, K., and Y. Fujimoto, 1984: The fine structure of cytoplasmic and intranuclear inclusions of seal pox. Nihon Juigaku Zasshi 46, 401–404. Oksanen, A., M. Tryland, K. Johnsen, and J. P. Dubey, 1998: Serosurvey of Toxoplasma gondii in North Atlantic marine mammals by the use of agglutination test employing whole tachyzoites and dithiothreitol. Comp. Immunol. Microbiol. Infect. Dis. 21, 107–114. Olson, M. E., P. D. Roach, M. Stabler, and W. Chan, 1997: Giardiasis in ringed seals from the western arctic. J. Wildl. Dis. 33, 646–648. Osterhaus, A. D., G. F. Rimmelzwaan, B. E. Martina, T. M. Bestebroer, and R. A. Fouchier, 2000: Influenza B virus in seals. Science 288, 1051–1053. Proulx, J. F., J. D. MacLean, T. W. Gyorkos, D. Leclair, A. K. Richter, B. Serhir, L. Forbes, and A. A. Gajadhar, 2002: Novel prevention program for trichinellosis in inuit communities. Clin. Infect. Dis. 34, 1508–1514. Refsum, T., K. Handeland, D. L. Baggesen, G. Holstad, and G. Kapperud, 2002: Salmonellae in avian wildlife in Norway from 1969 to 2000. Appl. Environ. Microbiol. 68, 5595–5599. Robertson, L. J., 2007: The potential for marine bivalve shellfish to act as transmission vehicles for outbreaks of protozoan infections in humans: a review. Int. J. Food Microbiol. 120, 201–216. Robertson, L. J., and R. Fayer. 2012: Cryptosporidium. In: Robertson, L. J., and H. V. Smith (eds), Foodborne Protozoan Parasites, pp. 33–64. Nova Publishers, Hauppauge, New York, USA. Ross, H. M., K. L. Jahans, A. P. MacMillan, R. J. Reid, P. M. Thompson, and G. Foster, 1996: Brucella species infection in North Sea seal and cetacean populations. Vet. Rec. 138, 647– 648. Santin, M., B. R. Dixon, and R. Fayert, 2005: Genetic characterization of Cryptosporidium isolates from ringed seals (Phoca hispida) in Northern Quebec, Canada. J. Parasitol. 91, 712–716. Serhir, B., J. D. MacLean, S. Healey, B. Segal, and L. Forbes, 2001: Outbreak of trichinellosis associated with arctic walruses in northern Canada, 1999. Can. Commun. Dis. Rep. 27, 31–36. Shaffer, N., R. B. Wainwright, J. P. Middaugh, and R. V. Tauxe, 1990: Botulism among Alaska Natives. The role of changing food preparation and consumption practices. West. J. Med. 153, 390–393. Simpson, V. R., N. C. Stuart, M. J. Stack, H. A. Ross, and J. C. Head, 1994: Parapox infection in grey seals (Halichoerus grypus) in Cornwall. Vet. Rec. 134, 292–296. Skaare, J. U., H. J. Larsen, E. Lie, A. Bernhoft, A. E. Derocher, R. Norstrom, E. Ropstad, N. F. Lunn, and O. Wiig, 2002: Ecological risk assessment of persistent organic pollutants in the arctic. Toxicology 181, 193–197. Smith, A. W., and P. M. Boyt, 1990: Caliciviruses of ocean origin: a review. J. Zoo Wildl. Med. 21, 3–23.

Smith, A. W., C. M. Prato, W. G. Gilmartin, R. J. Brown, and M. C. Keyes, 1974: A preliminary report on potentially pathogenic microbiological agents recently isolated from pinnipeds. J. Wildl. Dis. 10, 54–59. Smith, A. W., R. J. Brown, D. E. Skilling, H. L. Bray, and M. C. Keyes, 1977: Naturally-occurring leptospirosis in northern fur seals (Callorhinus ursinus). J. Wildl. Dis. 13, 144–148. Smith, A. W., E. S. Berry, D. E. Skilling, J. E. Barlough, S. E. Poet, T. Berke, J. Mead, and D. O. Matson, 1998: In vitro isolation and characterization of a calicivirus causing a vesicular disease of the hands and feet. Clin. Infect. Dis. 26, 434–439. Sohn, A. H., W. S. Probert, C. A. Glaser, N. Gupta, A. W. Bollen, J. D. Wong, E. M. Grace, and W. C. McDonald, 2003: Human neurobrucellosis with intracerebral granuloma caused by a marine mammal Brucella spp. Emerg. Infect. Dis. 9, 485–488. Sorensen, H. C., K. Alboge, and J. C. Misfeldt, 1993: Botulism in Ammassalik. Ugeskr. Laeg. 155, 108–109. Sorrell, T. C., D. H. Mitchell, J. R. Iredell, S. C. A. Chen, G. L. Mandell, J. E. Bennett, and P. Dolin, 2010 (eds), Principles and Practice of Infectious Diseases, 7th edn, pp. 3199–3207. Elsevier, Philadelphia, Pennsylvania, USA. Stoddard, R. A., 2005: Salmonella and Campylobacter spp. in Northern Elephant Seals, California. Emerg. Infect. Dis. 11, 1967–1969. Stoddard, R. A., R. L. DeLong, B. A. Byrne, S. Jang, and F. M. Gulland, 2008a: Prevalence and characterization of Salmonella spp. among marine animals in the Channel Islands, California. Dis. Aquat. Org. 81, 5–11. Stoddard, R. A., E. R. Atwill, F. M. D. Gulland, M. A. Miller, H. A. Dabritz, D. M. Paradies, K. R. Worcester, S. Jang, J. Lawrence, B. A. Byrne, and P. A. Conrad, 2008b: Risk factors for infection with pathogenic and antimicrobial-resistant fecal bacteria in northern elephant seals in California. Public Health Rep. 123, 360–370. Stuen, S., P. Have, A. D. Osterhaus, J. M. Arnemo, and A. Moustgaard, 1994: Serological investigation of virus infections in harp seals (Phoca groenlandica) and hooded seals (Cystophora cristata). Vet. Rec. 134, 502–503. de Swart, R. L., P. S. Ross, J. G. Vos, and A. D. Osterhaus, 1996: Impaired immunity in harbor seals (Phoca vitulina) exposed to bioaccumulated environmental contaminants: review of a longterm feeding study. Environ. Health Perspect. 104, 823–828. Thjotta, T., and J. Kvittingen, 1949: The etiology of Sealer’s Finger (blubber finger). Acta Pathol. Microbiol. Scand. 26, 407–417. Thompson, P. J., D. V. Cousins, B. L. Gow, D. M. Collins, B. H. Williamson, and H. T. Dagnia, 1993: Seals, seal trainers, and mycobacterial infection. Am. Rev. Respir. Dis. 147, 164–167. Thorshaug, K., and A. Rosted, 1956: Researches into the prevalence of trichinosis in animals in arctic and antarctic waters. Nord. Vet. Med. 8, 115–129. Tryland, M., 2000: Zoonosis of arctic marine mammals. Rev. Infect. Dis. 2, 55–64. Tryland, M., 2011a: Seal parapoxvirus. In: Liu, D. (ed.), Molecular Detection of Human Viral Pathogens, pp. 1029–1037. CRC Press, Boca Raton, Florida, USA.


393


M. Tryland et al.

Tryland, M., L. Kleivane, A. Alfredsson, M. Kjeld, A. Arnason, S. Stuen, and J. Godfroid, 1999: Evidence of Brucella infection in marine mammals in the North Atlantic Ocean. Vet. Rec. 144, 588–592. Tryland, M., J. Klein, E. S. Nordoy, and A. S. Blix, 2005: Isolation and partial characterization of a parapoxvirus isolated from a skin lesion of a Weddell seal. Virus Res. 108, 83–87. Tryland, M., J. Godfroid, and P. Arneberg, 2009: Impact of Climate Change on Infectious Diseases of Animals in the Norwegian Arctic. Norwegian Polar Institute, Tromsø, Norway. Tryland, M., B.-T. Lunestad, L. J. Robertson, T. Nesbakken, and D. Grahek-Ogden, 2011b: Risk Assessment of Human Pathogens in Marine Mammal Meat. Norwegian Scientific Committee for Food Safety, Oslo, Norway. Viallet, J., J. D. MacLean, C. A. Goresky, M. Staudt, G. Routhier, and C. Law, 1986: Arctic trichinosis presenting as prolonged diarrhea. Gastroenterology 91, 938–946.

Webster, R. G., J. Geraci, G. Petursson, and K. Skirnisson, 1981: Conjunctivitis in human beings caused by influenza A virus of seals. N. Engl. J. Med. 304, 911. Wilson, T. M., and I. Poglayen-Neuwall, 1971: Pox in South American sea lions (Otaria byronia). Can. J. Comp. Med. 35, 174–177. Wilson, T. M., and P. R. Sweeney, 1970: Morphological studies of seal poxvirus. J. Wildl. Dis. 6, 94–97. Wilson, T. M., N. F. Cheville, and L. Karstad, 1969: Seal pox. Case history. J. Wildl. Dis. 5, 412–418. Wilson, T. M., R. W. Dykes, and K. S. Tsai, 1972: Pox in young, captive harbor seals. J. Am. Vet. Med. Assoc. 161, 611–617. Wood, R. L., and R. D. Shuman, 1981: Erysipelothrix infection. In: Davis, J. W., L. H. Karstad, and D. O. Trainer (eds), Infectious Diseases of Wild Mammals, pp. 297–305. Iowa State University Press, Ames, Iowa.

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