The muskrat (Ondatra zibethicus) as a new reservoir for puumala-like hantavirus strains in Europe
Introduction
The infection of humans by rodent borne hantavirus in Europe is mainly caused by puumala (PUU)-like virus strains (Niklasson and LeDuc, 1987a, Groen et al., 1995). The virus is transmitted to humans by direct contact with infected rodent excreta. PUU infection causes a relatively mild form of hemorrhagic fever with renal syndrome (HFRS) known as nephropathia epidemica (NE). However, in some case reports severe manifestations caused by PUU-like viruses are documented (Alexeyev and Baranov, 1993, Clement et al., 1994a, Schreiber et al., 1996Pilaski et al. 1994, Schreiber et al. 1996). PUU strains from different geographic areas show similar but not identical genotypic and antigenic properties (Lundkvist and Niklasson, 1992, Chu et al., 1994). This might be one of the reasons why NE is characterized by various symptoms ranging from fever, headache, myalgia, nausea, to renal insufficiency. Besides these clinical manifestations several other symptoms such as hepatitis, encephalitis, and pneumonia can also be predominant.
The main reservoir of PUU virus in Europe is the bank vole, Clethrionomys glareolus, belonging to the subfamily Arvicolinae of Muridae family. Besides C. glareolus other rodents are also known to be reservoirs for PUU hantavirus strains (Diglisic et al., 1994, Kariwa et al., 1995). Apodemus mice are generally associated with hantaan viruses (HAN) which cause a severe form of hantavirus disease known as HFRS or korean hemorrhagic fever (KHF). Also wild rats (Rattus norvegicus) have been described as a reservoir for Seoul hantavirus (Lee et al., 1982). The northamerican rodents Peromyscus maniculatus, Microtus pennsylvanicus, and Lagurus curtatus are generally associated with Sin Nombre virus (SN) (Childs et al., 1994, Rowe et al., 1995, Douglass et al., 1996, Jay et al., 1997), the hantavirus strains causing the highly lethal hantavirus pulmonary syndrom (HPS). Recently, in southern Argentina an unusual hantavirus outbreak was observed that gave, however, the first evidence that hantaviruses can be transmitted from person to person (Wells et al., 1997). Usually, humans become infected only after direct contact to rodent carriers or inhaling either aerosolized droplets of urine or particulates contaminated with rodent excreta. Thus, a higher risk for rodent-to-human transmission might exist for people hunting rodents (Zöller et al., 1995) or sleeping outside on the ground (Xu et al., 1985, Antoniadis et al., 1987). Also military personel are at higher risk since contact with rodents or their excreta is possible on field exercises (Clement et al., 1996a, Markotic et al., 1996). Risk of rodent-to-human transmission is also linked to the absolute frequency of hantavirus carriers in the specific area. The rodent density and seroprevalence in areas where NE had occurred was significantly higher than in control areas where NE did not occur in the last year (Ahlm et al. 1997).
Since infection of humans is caused by rodent contaminated materials it is important to study population densities and the prevalence of hantavirus-specific antibodies in Clethrionomys and Apodemus mice, the well-known hantavirus carriers. Besides rodents, birds (Baek and Lee, 1993, Slovona et al., 1992), bats (Kim et al., 1994), shrews (Carey et al., 1971) and moles (Verhagen et al., 1987, Clement et al., 1994b) have been described as hantavirus carriers. In a study on domestic animals like cats and dogs no PUU-specific antibodies were found (Groen et al., 1995) but cat ownership was described as a risk factor in epidemiological studies in China (Xu et al., 1987). However, the role of these animals in hantavirus transmission to humans is still unclear. Rodents are by far the most important vectors and therefore it is of high importance to analyse different wild-living rodents. A possible hantavirus reservoir could be the muskrat (Ondatra zibethicus), a medium size member of the rodent family (Danell, 1982) originating from North America and introduced to Europe in 1905. Based on their semi-aquatic life style the muskrat quickly conquered watershed areas like marshes, swamps, rivers, and ponds and is presently distributed all over Europe. Contact to humans might be possible since muskrats are trapped for several reasons. In North Amerika the muskrat is a most valuable fur animal and many thousands are trapped each year. In some regions at least eighty percent of the meat of the captured animals is consumed as food. In northwestern Ohio for example ‘muskrat suppers’ are organized in the winter to raise money and many muskrat recipes can be received via the Internet. In the Northwest Territories of Canada muskrat meat is part of the traditional food of the Inuvialuit (Wein and Freeman, 1992). In Europe, muskrats are also trapped for their pelts but also hunted by some people by bow and arrow and consumed as food. In the Netherlands, Belgium and Germany government-hired muskrat-trappers are responsible to thin them out since they represent an ecological problem by undermining dikes and destroying shelf belts.
It was the aim of the study to see if the muskrat could act as a reservoir for hantavirus infections in Europe. This report describes the detection of hantavirus using RT-PCR and indirect IFA.
Section snippets
Muskrats
In 1994, 332 muskrats were caught by government-hired trappers using neck-breaking steel traps in the northwest of Brandenburg and in the northeast of Saxony-Anhalt, Germany. The trapping area was suited next to the three rivers Elbe, Havel and Mulde as shown in Fig. 3. All animals were stored frozen (−20°C) after trapping. Out of the 332 muskrats serum samples were taken from the thoracic cavity of 266 animals. Furthermore, from 197 muskrat’s lungs and kidney specimens were collected for
Results
Trapped muskrats were screened for hantavirus infection using an indirect IFA for anti-viral antibodies in serum. Out of the 266 muskrat sera tested 14 (5.3% CI=2.9–8.7%) showing hantavirus-specific fluorescent stainings compared to the human control serum were detected (rated+). Ten additional sera (3.8%) were considered suspect (rated+/−) having typical, but weak fluorescent stainings at a dilution of 1/10 (Table 1, Fig. 1).
In addition, lung and kidney tissue samples from 197 muskrats were
Discussion
Hantaviruses, members of the Bunyaviridae family with cosmopolitan distribution, can be found in different persistently infected rodent or insectivore hosts. The bank vole (C. glareolus) is the known major reservoir for PUU-like hantavirus strains in Europe. We now have analyzed the muskrat (O. zibethicus) for hantavirus infection. We have clearly demonstrated the presence of hantavirus-specific antibodies in muskrat serum samples and the presence of hantavirus RNA in muskrat tissue. That
Acknowledgements
Sonja Ziegelmaier, Ruth Rauhöft and L. Minke is thanked for excellent technical assistance. We also thank Solomon Odemuyiwa for critically reading the manuscript. The work was supported by local muskrat trappers of the German Federal States Saxony-Anhalt and Brandenburg.
References (53)
- et al.
Serological relationships among viruses in the Hantavirus genus, family Bunyaviridae
Virology
(1994) - et al.
Hantavirus outbreak during military manoeuvres in Germany
Lancet
(1996) - et al.
Comparison of immunofluorescence and enzyme-linked immunosorbent assays for the serology of Hantaan virus infections
J. Virol. Methods
(1989) - et al.
Haemorrhagic fever with renal syndrome in Germany
Lancet
(1991) - et al.
Coexistence of several novel hantaviruses in rodents indigenous to North America
Virology
(1995) - et al.
Hantavirus pulmonary syndrome in Germany
Lancet
(1996) - et al.
Isolation and initial characterization of a newfound hantavirus from California
Virology
(1995) - et al.
Molecular characterization of the RNA S segment of nephropathia epidemica virus strain Hällnäs B1
Virology
(1990) - et al.
Puumala virus infection without signs of renal involvement
Scand. J. Infect. Dis.
(1993) - et al.
High prevalence of hantavirus antibodies in bank voles (Clethrionomys glareolus) captured in the vicinity of households afflicted with nephropathia epidemica
Am. J. Trop. Med. Hyg.
(1997)
Clinical and epidemiological aspects of hemorrhagic fever with renal syndrome (HFRS) in Greece
Eur. J. Epidemiol.
A new natural intermediate host of Echinococcus multilocularis in France: the muskrat
Ann. Parasitol. Hum. Comp.
Thottapalayam virus: a presumptive arbovirus isolated from a shrew in India
Indian J. Med. Res.
Serologic and genetic identification of Peromyscus maniculatus as the primary rodent reservoir for a new hantavirus in the southwestern United States
J. Infect. Dis.
A household-based, case-control study of environmental factors associated with hantavirus pulmonary syndrome in the southwestern United States
Am. J. Trop. Med. Hyg.
Hantavirus pulmonary syndrome in New England and Europe
New Engl. J. Med.
Hantavirus infection: a ‘new’ exotic zoonosis among us
Bull. Mem. Acad. R. Med. Belg.
Muskrat
Isolation of a Puumala-like virus from Mus musculus captured in Yugoslavia and its association with severe hemorrhagic fever with renal syndrome
J. Infect. Dis.
Hantavirus in Montana deer mouse populations: preliminary results
J. Wildl. Dis.
Note on an exact treatment of contingency goodness of fit and other problems of significance
Biometrica
Hantavirus infections in The Netherlands: epidemiology and disease
Epidemiol. Infect.
Toxoplasmosis in wild mammals from the Czech Republic
J. Wildl. Dis.
Seroepidemiologic studies of hantavirus infection among wild rodents in California
Emerg. Infect. Dis.
Cited by (10)
Hunting harvest data in Sweden indicate precipitous decline in the native mountain hare subspecies Lepus timidus sylvaticus (heath hare)
2021, Journal for Nature ConservationCitation Excerpt :Over the past few centuries, however, increased human activity and disturbance have drastically altered the amplitude and frequency of these natural variations (Dirzo et al., 2014). For example, the introduction of non-native species to the Eurasian continent has negatively influenced a range of native taxa (e.g. Vahlenkamp et al., 1998; Carlsson et al., 2010; Keller et al., 2011; Barbar & Lambertucci, 2018). Simultaneously, large-scale changes in climate and land use have altered trophic interactions and ecosystem organisation (Scheffer et al., 2001).
Hantavirus Emergence in Rodents, Insectivores and Bats: What Comes Next?
2013, The Role of Animals in Emerging Viral DiseasesOrthohantaviruses in the Arctic: Present and Future
2022, Arctic One Health: Challenges for Northern Animals and PeoplePersistence and Meaning in Fur-Bearing Mammal Usage on the Nechako Plateau, British Columbia
2019, International Journal of Historical ArchaeologyHantavirus-induced immunity in rodent reservoirs and humans
2008, Immunological Reviews