A post-mortem study of respiratory disease in small mustelids in south-west England
- 1.1k Downloads
Stoat (Mustela erminea) and weasel (Mustela nivalis) populations in south-west England are declining whilst polecats (Mustela putorius), absent for over a century, are increasing. Little is known about the health status of these species nationally. This study aimed at investigating respiratory disease in specimens found dead in south-west England.
Trauma caused by road traffic, predator attack or being trapped was the predominant cause of death in 42 stoats, 31 weasels and 20 polecats; most were in good physical condition. Skrjabingylus nasicola was present in all species (weasels 37 %, polecats 39 %, stoats 41 %) and infected animals showed no evidence of loss of body condition. Even in carcases stored frozen L1 larvae were frequently alive and highly motile. Angiostrongylus vasorum infection was diagnosed in two stoats and one weasel: in stoats infections were patent and the lung lesions were likely of clinical significance. These are believed to be the first records of A. vasorum in small mustelids. Pleuritis and pyothorax was seen in two polecats, in one case due to a migrating grass awn. Histological examination of lungs showed granulomata in stoats (38 %), weasels (52 %) and polecats (50 %). Spherules consistent with Emmonsia spp. adiaspores were present in the granulomata of stoats (60 %), weasels (36 %) and polecats (29 %). Adiaspore diameter in all three species was similar (means: stoats 39 μm, weasels 30 μm, polecats 36 μm); these are markedly smaller than that normally recorded for E. crescens. Although they lie within the accepted range for spores of Emmonsia parva this arid-zone species is not found in Britain, thus raising a question over the identity of the fungus. Cases showing numerous granulomata but few or no adiaspores were Ziehl-Neelsen-stain negative for acid-fast bacilli and IHC negative for Mycobacterium spp. However, in some cases PCR analyses revealed mycobacteria, including Mycobacterium kumamotonense and Mycobacterium avium Complex. One stoat had numerous unidentified small organisms present centrally within granulomata.
Stoats, weasels and polecats in south-west England share several respiratory diseases, often of high prevalence, but the pathology would appear insufficient to impact on the health status of the populations and other ultimate causes of death should be investigated when examining these species.
KeywordsMustelid Respiratory disease Angiostrongylus Skrjabingylus Pyothorax Granuloma Adiaspore Emmonsia Mycobacterium
Stoats (Mustela erminea) and weasels (Mustela nivalis) are common and widespread in Britain but are understudied and poorly understood . Although at a national level the populations of both species are thought to be either stable or declining [2, 3], in south-west England the evidence of declines is clearer, particularly in weasels . The reasons for the declines are unknown but possibly include reduced prey availability as a result of changes in agricultural practices, secondary poisoning by rodenticides and, in the case of stoats, increased predation by an increasing fox population [2, 5, 6]. Formerly widespread, the polecat (Mustela putorius) was persecuted almost to the point of extinction during the late 1800s, with only a small number surviving along the English Welsh border. During the latter half of the 1900s this population started to recover and in recent decades polecats have recolonised most of Wales and much of central England [7, 8]. Since 2010, increasing numbers of polecats have been recorded in Somerset, Devon and Cornwall (Simpson, V., Couper, D. and Williams, J. unpublished data).
Apart from a study of stoats by McDonald and co-workers in 2001  there have been no surveys to investigate the health status of stoats, weasels and polecats in Britain. However, a number of disease conditions have been identified in British small mustelids, mostly in studies targeting a specific organism. Mycobacterium bovis infection was recorded in a small number of stoats , Mycobacterium paratuberculosis in stoats  and Neospora caninum infection in polecats . Canine distemper occurs worldwide  but whilst the disease has been well documented in mustelids in Europe  the only recorded cases in Britain were in captive stoats and weasels . Evidence of Aleutian disease has been found in various mustelids in mainland Europe [15, 16] but although a high antibody prevalence was recorded in feral American mink (Mustela vison) in south-east England , the infection has not been proven in other British small mustelids. Two conditions affecting mustelids that are well documented in Britain, as in many other countries, are adiaspiromycosis due to Emmonsia species fungi [18, 19] and upper respiratory tract infection by the nasal nematode Skrjabingylus nasicola [20, 21].
McDonald and co-workers  concluded that the stoats that they examined from eastern England were remarkably healthy apart from respiratory disease of undetermined aetiology. In the absence of other surveys to determine the health status of stoats, weasels or polecats in Britain the pathology and epidemiology of any diseases that may affect them are largely unknown . The purpose of the present study was to examine further the causes of respiratory disease in these three species of small mustelids in south-west England and to consider their possible impact on the health of the populations.
This was an opportunistic study during 1999 to 2014 in which small mustelids found dead in south-west England were collected by members of the public and conservation bodies and submitted for post-mortem examination. The first polecats were submitted in 2011 when several were trapped on an estate in Somerset as part of its normal pest control programme; thereafter most were road traffic casualties submitted by members of the public. Polecats whose pelage was not consistent with that of a true polecat  were not included in the study. Carcases submitted in a fresh state were normally examined on the day of receipt or, failing that, within 24 h. Carcases submitted frozen were kept at -20 °C until they could conveniently be thawed and examined. Each specimen was given a unique identification number, weighed, and sexed prior to post-mortem examination. Animals were aged as adult, subadult or immature based on their size, dental wear and gonadal development. Body condition was subjectively assessed, based separately on fat deposits and muscle condition. In each case, fat and muscle condition were assigned to one of three categories: good; moderate; and poor/nil. In some instances it was not possible to reliably assess condition, due to autolysis and/or trauma. In freshly dead specimens with lesions suggestive of a bacterial infection tissue samples or swabs were submitted to Animal Health and Veterinary Laboratories Agency (AHVLA), Truro, for bacteriological examination. Irrespective of whether gross pathological lesions were seen, samples of lung and heart were routinely placed in 10 % buffered formal saline, processed routinely through graded alcohols, embedded in paraffin wax, sectioned at 5 μm, stained by haematoxylin and eosin and, in selected cases, by per-iodic acid Schiff (PAS), Giemsa, Gram and Ziehl-Neelsen (ZN). Granulomata and spores were measured, where possible, using an eye-piece micrometer calibrated against a stage micrometer. Mean granulomata and spore diameters for each mustelid species were derived by pooling the measurements of each granuloma or spore from each individual specimen, using a maximum of 10 values per specimen. The same procedure was deployed to examine histological sections of ten Eurasian otters’ (Lutra lutra) lungs held in one author’s (VRS) archive from previous studies [19, 24, 25]. Nasal passages were routinely irrigated via the nasopharynx with a small quantity of tap water and a drop of recovered fluid placed on a microscope slide and examined by direct microscopy for parasites. In selected cases scrapes of tracheal mucus and wet impressions from cut surface of lung were also examined by direct microscopy. A variation on the Baermann technique was used to examine the lungs of a stoat for first stage larvae of Angiostrongylus vasorum. Briefly, representative samples of each lobe were pooled, macerated in water and enclosed in a piece of cotton gauze. This was then held in the neck of a conical centrifuge tube and tap water slowly added until no air space remained in the tube. After standing overnight, the gauze and lung tissue was removed, the bulk of the water pipetted off and a sample from the bottom of the tube transferred to a microscope slide for examination by direct light microscopy.
To investigate possible infection by Mycobacterium species in five selected mustelids with granulomata, various PCRs were performed. DNA was extracted from 20 μm sections of formalin fixed, paraffin embedded tissue. Briefly, paraffin was removed by the addition of xylene, the tissue pelleted and then washed twice with ethanol. The tissue was lysed using 0.1 mm silica beads (Lysing Matrix B, MP Biomedicals) in AQL tissue lysing buffer (Qiagen DNeasy Kit) in a FastPrep™ FP120 (Thermo Savant) for three cycles of 20 s at 6 m/s with cooling on ice in between. Beads and debris were pelleted in a microfuge and the supernatant transferred to a fresh microcentrifuge tube. After overnight treatment with Proteinase K, DNA was extracted using the spin column procedure according to Qiagen DNeasy Kit instructions. A pan mycobacteria PCR targeting the hsp65 gene was performed as described by Telenti et al. . Sections of ovine ileum with multibacillary paratuberculosis were used as extraction and positive controls and sterile distilled water as a PCR negative control. Amplified DNA was extracted from a 2 % agarose gel using a QIAquick PCR purification kit (Qiagen) and then sequenced (MWG BioTech) to identify the Mycobacterium species present. To differentiate further between members of the Mycobacterium avium Complex, PCRs for IS900 specific for Mycobacterium avium subsp. paratuberculosis  and IS901specific for Mycobacterium avium subspecies silvaticum and subspecies avium  were performed. Using material from the same five animals, immunohistochemistry specific for Mycobacterium spp. was performed on 3.5 μm thick tissue sections placed on coated microscope slides (FLEX IHC microscope slides, Dako, Agilent technologies, Glostrup, Denmark). Sections were dewaxed in xylene, rehydrated in graded alcohols and then endogenous peroxidase was blocked by immersion in 3 % H2O2 in methanol solution (v/v) for 30 min in darkness at room temperature. Slides were subsequently rinsed twice in PBS (pH 7.4) and incubated with rabbit anti-Mycobacterium avium sbsp paratuberculosis polyclonal antiserum (which is known to detect several diverse species of mycobacteria; Julio Benavides, Mark Dagleish personal observations), diluted 1/9000 in PBS  overnight at 4 °C in a humidified chamber. After extensive washing in PBS, sections were incubated with a commercial visualisation kit (EnVision®+/HRP solution, Dako, Agilent technologies, Glostrup, Denmark) as per manufacturer’s instruction for 40 min at room temperature. After washing in PBS, antibody localization was visualised with AEC substrate-chromogen (AEC plus, Dako, Agilent technologies, Glostrup, Denmark). Sections were counterstained with Mayer’s haematoxylin for 10 s prior to mounting. Appropriate species- and isotype- matched immunoglobulins were used as negative controls.
To determine if the presence of S. nasicola, or the presence of pulmonary granulomata were associated with body condition, Fisher’s exact test was performed for each of the following: fat condition and the presence of S. nasicola; fat condition and the presence of pulmonary granulomata; muscle condition and the presence of S. nasicola; and finally muscle condition and the presence of pulmonary granulomata. Significance was assigned for p < 0.05. Analyses were run in R version 3.1.0.
Mortality due to trauma: the number of each species submitted, the number and proportion killed by road traffic, predation or other forms of trauma
Road traffic (%)
Other trauma (%)
Total trauma (%)
In stoats and weasels killed by predators the pattern of the bite wounds was similar, with the majority of punctures across the caudal neck and thorax. In stoats the size and spacing of the bite wounds was mostly consistent with attack by foxes, or possibly similar size dogs, but in weasels the wounds, and often the history, was consistent with them being killed by domestic cats. No polecats were killed by predators and most of the non-road traffic deaths were caused by traps. No details of the traps were available but the pattern of bruising and haemorrhage to the skin over the neck and thorax suggested they were Fenn-type spring traps.
Upper respiratory tract
The prevalence of infection with Skrjabingylus nasicola for stoats, weasels and polecats
% positive (95 % CI)
Bone deformity due to the presence of S. nasicola was not common and in most cases the lesion was considered to be of little clinical significance. Fisher’s exact test confirmed that there was no statistically significant association between the presence of S. nasicola and body condition based on either fat deposits or muscle condition: in each analysis p>> 0.05.
Lower respiratory tract and heart
The second polecat with pleuritis (Fig. 3b) was a subadult female in good body condition. The right side of the thoracic cavity contained a large amount of dark reddish-brown fluid, the lobes of the right lung were collapsed, distorted and consolidated and there were extensive adhesions to the parietal pleura, pericardium and mediastinum. Within the adhesions and fluid was an approximately 25 mm long grass awn. The left lung showed mild, patchy congestion. Gram stained impression smears of the pleura showed masses of cellular debris but no organisms. There were subcutaneous lesions over the head and neck that were consistent with the animal having been killed in a spring trap. The stomach contained the undigested remains of a small mammal showing that, despite the pleuritic lesions, the animal had been hunting shortly before it was killed.
Angiostrongylosis was also diagnosed in a second stoat and a weasel. The stoat was an adult male and had been killed by road traffic. It had a well-circumscribed, firm, consolidated swelling in the caudal half of the left diaphragmatic lobe and the bronchial and mediastinal lymph nodes were enlarged. Microscopic examination of wet impressions from the cut surface of the lung revealed many first stage larvae of A. vasorum. Bacteriological cultures of lung and lymph nodes for Mycobacterium spp. proved negative. Histological examination of lung showed little normal pulmonary parenchyma but multiple, coalescing, granulomata enclosing groups of embryonated eggs and nematode larvae. The weasel was an adult male killed by road traffic and in good body condition. Extensive trauma prevented detailed gross examination of the lungs but histological examination showed adult nematodes with the morphological features of Angiostrongylus species within branches of the pulmonary artery (Fig. 6 inset).
Summary of histological examination of lungs, showing the number and proportion which contained granulomata and metaplastic foci of bone or osteoid and the number and proportion of the granuloma cases that had adiaspores
Granuloma + ve (%)
Adiaspore + ve (%)
Bone/osteoid + ve (%)
Infection of stoats, weasels, polecats and other small mustelids by the metastrongyloid parasite Skrjabingylus nasicola has been well documented in Europe and elsewhere in the World [30, 31]. Although a range of gastropods act as intermediate hosts it is thought that these are rarely eaten by small mustelids and it is likely that they become infected by eating small mammals which act as paratenic hosts, notably wood mice (Apodemus sylvaticus), bank voles (Clethrionomys (Myodes) glareolus) and, in some areas, shrews (Sorex sp.) [32, 33]. In the final host, ingested larvae migrate to the central nervous system and travel via the subarachnoid space to the front of the brain. Here they follow the olfactory nerves through the cribriform plate to enter the nasal sinuses where they mature . The irritation caused by the adult worms can result in erosion, remodelling and deformity of the frontal bones.
The lesions to the frontal area of the skull are often considered pathognomonic for S. nasicola infection and have been widely used in studies to determine the prevalence and distribution of the parasite [30, 35, 36]. However, infection with the trematode Troglotrema acutum can also result in similar skull lesions that cannot be reliably distinguished from those caused by S. nasicola [37, 38]. Although T. acutum is commonly found in small mustelids in Continental Europe, especially in polecats [37, 38], there appear to be no confirmed records of it occurring in the UK (, Harris, E. personal communication). Trematode eggs that morphologically resembled those of T. acutum were recovered from the nasal passages of two polecats in the present study but they were significantly smaller than those typically recorded for T. acutum [37, 38]. It appears that no trematode species has been recorded in the upper respiratory system of polecats in the UK (Bray, R and Harris, E personal communication) and further studies are required to collect and identify the trematodes demonstrated in this study.
In the present study, many specimens, especially those killed by road traffic, had suffered severe damage to the head which often precluded meaningful examination for skull lesions. However, the technique of irrigating the naso-pharynx, nasal passages and turbinates with a small amount of water and then looking for first stage larvae in recovered fluid not only overcame the problem caused by trauma but also identified early stage infection where bone lesions were not apparent. The fact that the larvae were normally highly motile, even in carcases that had been frozen, made them easy to locate when only small numbers were present in a sample. The prevalence figures in the present study are comparable with those reported previously in England and elsewhere in Europe  and, as has been observed previously , infection with S. nasicola did not appear to adversely affect an animal’s body condition.
Angiostrongylus vasorum is possibly the most significant parasite of dogs in Britain. Its common epithet ‘French Heartworm’ alludes to the fact that the first description and most of the pioneering work on the parasite was performed in Toulouse in south-west France [40, 41]. Since then, particularly during the mid to late 1900s, the parasite has extended its range remarkably and is now found on most continents. The first reports of autochthonous infection in domestic dogs in Britain were from Cornwall in the early 1980s [42, 43] and the first cases in foxes in 1996 . During the next 30 or so years the parasite spread steadily northwards throughout most of England and Wales  and its range now extends to all but the northern part of Scotland [46, 47]. The principal means of spread in Britain has almost certainly been due to the translocation of infected dogs. However, foxes also play a role in the epidemiology of the disease by maintaining local reservoirs of infection.
Apart from foxes there has, until now, been no evidence of A. vasorum infection in other free-living species of wildlife in Britain. Larvae identified as those of A. vasorum were seen in the lungs of a single Eurasian otter (Lutra lutra) in Denmark  but post-mortem examinations on 700 otters in Britain, many of which came from known endemic areas of infection, all proved negative for the parasite . Kirk and co-workers , citing Guilhon , suggested that Eurasian otters could act as an alternative final host but this was in error as Guilhon  made no mention of infection in otters. Although A. vasorum has been reported in badgers (Meles meles) in Spain and Italy [51, 52], large numbers of badgers have been examined in Britain in connection with the control of bovine tuberculosis and, whilst occasional cases of Aelurostrongylus falciformis have been seen (, A. Barlow, pers. comm.), there have been no reports of A. vasorum infection.
A literature study of diseases of stoats and closely related mustelids found no record of infection with A. vasorum  and a post-mortem study of stoats from various locations in eastern England by McDonald and co-workers also proved negative for the parasite . The latter study did detect nematodes in the lungs of five stoats but these were not identified; however, a figure in the article  showed adult females within which were numerous larval forms in various stages of development. The nematodes were in the pulmonary parenchyma but not in the pulmonary artery. These features, together with the fact that larvae but no eggs were present in the parenchyma, suggest that the parasite was probably Aelurostrongylus falciformis. No similar parasites were seen in any of the mustelids in the present study but there was unequivocal evidence of A. vasorum infection in two stoats. Confirmation of the identity of the parasite in the weasel was lacking, but their location within the pulmonary artery, the characteristic morphology with lateral chords, and the fact that no other Angiostrongylus species is known to exist in south-west England, all support the presumptive identification of A. vasorum. The clinical significance of the pulmonary lesions in the stoats in this study is uncertain but they may well have been sufficient to impair the animal’s hunting ability.
Like S. nasicola, A. vasorum is a metastrongyloid parasite with a life cycle that depends on a gastropod intermediate host. Domestic dogs are thought to become infected by eating slugs whilst foxes, especially cubs, are known to eat various molluscs. Foxes will also eat frogs, which are considered to be a paratenic host for A. vasorum . However, as stoats and weasels are thought to rarely eat any of these prey items the question arises whether, as with S. nasicola, another paratenic host exists for A. vasorum.
Pleuritis associated with pyothorax was seen in two polecats but not in any of the stoats or weasels. One case was due to a grass awn which had most likely been inhaled, migrated through the lung parenchyma and penetrated the pleura. This is a well-recognised cause of pyothorax in dogs, especially those used for hunting or living in rural environments, and may also occur in cats . The cause of pyothorax in the other case was not established but it may also have been due to a grass awn as they can be nearly impossible to find where there is copious pleural exudate . Pyothorax occurs in Eurasian otters where it is typically associated with either septic bite wounds caused by intraspecific aggression or septic tooth lesions  but the polecat was a young animal with emerging, apparently healthy, permanent teeth and no visible bite wounds. One stoat died as a result of a Pasteurella multocida septicaemia. This is a well-recognised cause of mortality in small mammals, bats and small birds submitted to wildlife hospitals, especially where there is a history of them having been bitten by domestic cats. External lesions are often minimal but septicaemia and death typically occurs around 3 days after being bitten [56, 57].
The predominant histological feature in the lungs of all three species was the presence of small granulomata, some of which contained a central spore. The morphology and staining of the spores was consistent with the adiaspores of Emmonsia (Chrysosporium) species. These fungi have a saprophytic phase where mycelia growing on decaying plant material in soil produce sporangia that release aleuriospores. If these spores are inhaled by a mammal their small size (ca 2–4 μm) enables them to enter alveolar spaces; here they produce a double layered wall and increase markedly in volume to become adiaspores. The life cycle cannot progress until the mammalian host dies and the adiaspores are released into the environment. The genus Emmonsia contains two species that are capable of producing adiaspores, E. crescens, which is the predominant species in Europe and produces multinucleate adiaspores of 200–700 μm in diameter, and E. parva which is found in hotter, dryer climates and produces mononuclear adiaspores that typically only grow to around 20–40 μm [58, 59].
Adiaspiromycosis has been recorded in many species of small mammals throughout the World, especially members of the Family Mustelidae [18, 19, 60, 61, 62, 63, 64]. A notable feature in all three species in the present study was the consistently small size of the adiaspores, with none greater than 70.5 μm and mean values for each mustelid species of less than 40 μm. This is markedly smaller than those typically reported in otters where they often exceed 200 μm [18, 19, 65] and strikingly less than the mean value of 216 μm for the ten otters examined in this study (Fig. 10b). Granulomata due to Emmonsia infection are readily seen during gross pathological examination of otters  but none were observed in the small mustelids in this study. These results raise a question over the identity of the species infecting the stoats, weasels and polecats, especially as E. parva is not known to exist in south west England. In an earlier study of adiaspiromycosis in weasels in Finland the authors also commented on the fact that the adiaspores, measuring 28–64 μm, were significantly smaller than those in the rodents on which the weasels preyed and questioned whether weasels were better able to supress the growth of adiaspores . If the adiaspores found in small mustelids are those of E. crescens and their small size is due to a host response, the quoting of size ranges in the literature as a means of differentiating between E. crescens and E. parva cannot be justified. Alternative explanations for the atypically small spores found in small mustelids are that they belong to neither of the two recognised species of Emmonsia capable of producing adiaspores or that they belong to another fungus species.
The high proportion of granulomata that did not contain an adiaspore in this study was in contrast to earlier studies in Eurasian otters where the majority of granulomata in a section of lung contained an adiaspore [19, 65]. A possible explanation for this would be the small size of the spores relative to that of the granulomata; more than 12 sections cut at 6 μm might be needed to locate a 40 μm spore within a 200 μm granuloma. A second reason might be that a higher proportion of spores are destroyed by the host response in the small mustelids than in otters. Ossification of scar tissue following the destruction of an adiaspore may be the reason for the foci of metaplastic bone and osteoid seen in many cases. The possibility of multiple infections in the small mustelids cannot be ruled out and some granulomata could be the consequence of another causal agent.
In an earlier histological study of stoats from East Anglia  the authors considered granulomatous inflammation to be the most significant pulmonary change. In some cases this had progressed to form distinct microgranulomata with central cores of macrophages, surrounded by a cuff of lymphoid cells. However, no causal agent was demonstrated. In those cases in the present study where numerous granulomata were present but no spores were seen consideration was given to the possibility that an infection other than adiaspiromycosis was present. Lesions of Mycobacterium species infection, especially M. bovis, can be confused with those of adiaspiromycosis [64, 66] and bovine tuberculosis is of particular concern in south west England where M. bovis is prevalent in the abundant badger population . None of the ZN- stained sections in this study revealed evidence of acid-fast bacilli but mycobacteria can be sparse and difficult to locate in chronic lesions. However, investigation by PCR did not detect M. bovis but revealed the presence of M. kumamotonense and members of the M.avium Complex (M.a. paratuberculosis and M.a. avium/silvaticum). M. kumamotonense is related to the M. terrae Complex and has been misidentified as M. tuberculosis Complex by commercial probes. It is possible that the granulomata observed could be the result of infection by a number of different mycobacteria but further investigations would require laser capture microdissection and highly sensitive PCR techniques which were outside the scope of this study. The lack of labelling of Mycobacterium spp. by IHC was probably a sensitivity issue as PCR is an exceptionally more sensitive technique. Further screening of small mustelids in south west England for mycobacteria by bacteriological and molecular biological techniques would seem prudent.
Respiratory disease is common in stoats, weasels and polecats in south-west England, all three species being particularly vulnerable to Skrjabingylus nasicola infection and pulmonary granulomatosis. There was no apparent loss of body condition associated with either disease but this was possibly influenced by the fact the animals had died prematurely due to trauma. The granulomata in approximately a third of cases, irrespective of species, contained fungal spores consistent with adiaspores of Emmonsia species but the spores were markedly smaller than the size normally quoted for E. crescens which raises doubts over their true identity. The detection of Mycobacterium species by PCR in several animals exhibiting large numbers of granulomata might be interpreted as a causal relationship. However, the failure to demonstrate mycobacteria by IHC using a polyclonal antibody makes it questionable as to whether the mycobacteria were actually responsible for the lesions. At present, it is only possible to say that the causes of granulomata in the three species of small mustelids in this study include a fungus, probably an Emmonsia species and an as yet unidentified organism. Pleuritis and pyothorax was seen in polecats but not in stoats or weasels. The demonstration of Angiostrongylus vasorum infections in stoats and weasels, which were proved to be patent in the stoats, means these species have the potential to play a role in the epidemiology of the disease. Overall, the pathology observed in the stoats and weasels in this study was not sufficiently different from that in polecats and would seem unlikely that the diseases observed could be responsible for stoat or weasel population declines in south-west England when polecats are increasing. However, in view of the expanding polecat population and the high prevalence of bovine tuberculosis in the region, it is recommended that further studies be carried out to identify and clarify the agent(s) responsible for the pulmonary granulomata.
The authors gratefully acknowledge the histological support given by Trevor Whitbread, Judith Hargreaves, Richard Fox, Lucy Oldroyd, Malcolm Silkstone, Sonja Rivers and Michelle Woodman at Abbey Veterinary Services. They also thank Nicholas Davison, Beverley Rule and Philip Booth, AHVLA Truro, Mark Wessels, Finn Pathologists, Luke Roberts and Eric Morgan, Bristol University, Marc Artois, Campus Vétérinaire de Lyon. Becki Lawson, Fieke Molenaar, Tamsyn Stephenson, Zoe Greatorex and Jane Simpson at Wildlife Veterinary Investigation Centre assisted with post-mortem-examinations. David Groves, Kate Stokes, Derek Lord and Cornwall Mammal Group and Cornwall Wildlife Trust members and staff, James Williams, Somerset Otter Group, and David Couper, Royal Society for the Prevention of Cruelty to Animals helped with carcase submissions. Andrew Borman, Mycology Reference Laboratory South West Health Protection Agency kindly commented on draft manuscripts. Eileen Harris and Rodney Bray at Natural History Museum are thanked for advice on parasites. Those parts of this study performed at AHVLA were funded under the Diseases of Wildlife Scheme and those performed at the Moredun Research Institute were funded by the Scottish Government Rural and Environment Science and Analytical Services Division. J. Benavides is supported by a “Ramón y Cajal” contract of the Spanish Ministry of Economy and Competitiveness. None of the authors received funding from other outside sources for this work.
- 1.Species. The Vincent Wildlife Trust http://www.vwt.org.uk/species/ (2015). Accessed 25 Mar 2016.
- 2.Harris S, Morris P, Wray S, Yaldon D: A Review of British Mammals: population estimates and conservation status of British mammals other than cetaceans. Peterborough; JNCC, 1995 http://jncc.defra.gov.uk/pdf/pub03_areviewofbritishmammalsall.pdf. Accessed 25 Mar 2016.
- 4.Davey PA, Aebischer NJ: Participation of the National Gamebag Census in the Mammal Surveillance Network. A Report to JNCC for the Year 2006/07. The Game Conservancy Trust; 2007. http://jncc.defra.gov.uk/PDF/TMP_NGC%20Report%202006-7.pdf. Accessed 25 Mar 2016.
- 6.Mulder JL. The stoat Mustela erminea in the Dutch dune region, its local extinction, and a possible cause: the arrival of the fox Vulpes vulpes. Lutra. 1990;33:1–21.Google Scholar
- 9.Delahay RJ, Smith GC, Barlow AM, Walker N, Harris A, Clifton-Hadley RS, Cheeseman CL. Bovine tuberculosis infection in wild mammals in the South-West region of England: a survey of prevalence and a semi-quantitative assessment of the relative risks to cattle. Vet J Lond Engl. 2007;173:287–301.Google Scholar
- 13.Rijks JM, Osterhaus ADME, Kuiken T, Frölich K: Morbillivirus Infections. In Infectious Diseases of Wild Mammals and Birds in Europe. Edited by Gavier-Widén D, Duff JP, Meredith A. Wiley-Blackwell: Chichester; 2012:99–118.Google Scholar
- 15.Fournier-Chambrillon C, Aasted B, Perrot A, Pontier D, Sauvage F, Artois M, Cassiède J-M, Chauby X, Dal Molin A, Simon C, Fournier P. Antibodies to Aleutian mink disease parvovirus in free-ranging European mink (Mustela lutreola) and other small carnivores from southwestern France. J Wildl Dis. 2004;40:394–402.CrossRefPubMedGoogle Scholar
- 22.McDonald RA, King CM. Stoat and Weasel. In: Harris S, Yalden D, editors. Mammals of the British Isles: Handbook. 4th ed. Southampton: Mammal Society; 2008. p. 456–76.Google Scholar
- 23.Birks JDS, Kitchener AC. Polecat. In: Harris S, Yalden D, editors. Mammals of the British Isles: Handbook. 4th ed. Southampton: Mammal Society; 2008. p. 476–85.Google Scholar
- 29.Delgado L, García Marín JF, Muñoz M, Benavides J, Juste RA, García-Pariente C, Fuertes M, González J, Ferreras MC, Pérez V. Pathological findings in young and adult sheep following experimental infection with 2 different doses ofMycobacterium avium subsp. paratuberculosis. Vet Pathol. 2013;50:857–66.CrossRefPubMedGoogle Scholar
- 30.Van Soest R, Van der Land J, Van Bree P: Skrjabingylus nasicola (Nematoda) in skulls of Mustela erminea and Mustela nivalis (Mammalia) from the Netherlands. Beaufortia. Institute of Taxonomic Zoology (Zoological Museum), University of Amsterdam.1972, 20:85–98.Google Scholar
- 32.Weber JM, Mermod C. Experimental transmission of Skrjabingylus nasicola, parasitic nematode of mustelids. Acta Zool Fenn. 1983;174:237–8.Google Scholar
- 35.King CM. Age-specific prevalence and a possible transmission route for skrjabingylosis in New Zealand stoats, Mustela erminea. N Z J Ecol. 1991;15:23–30.Google Scholar
- 37.Duscher GG, Harl J, Fuehrer H-P. Evidence of Troglotrema acutum and Skrjabingylus sp. coinfection in a polecat from Lower Austria. Helminthologia. 2015;52:63–6.Google Scholar
- 39.Fauna Europaea. http://www.fauna-eu.org/. Accessed 25 Mar 2016.
- 40.Baillet C. Strongyle des vaisseaux et du Coeur du chien. Strongylus vasorum (Nobis). N Dict Pract Méde Chir Hyg Vét. 1866;8:587–8.Google Scholar
- 41.Serres ME: Entozoaires trouvés dans l’oreille droite, le ventricle correspondant et l’artère pulmonaire d’un chien. J Vét Midi. 1854;7:70–72.Google Scholar
- 48.Madsen AB, Dietz HH, Henriksen P, Clausen B. Survey of Free-Living Otters (Lutra Lutra) – a Consecutive Collection and Necropsy of Dead Bodies. IUCN Otter Specialist Group Bulletin. 1999. p. 65–75.Google Scholar
- 50.Guilhon J. Transmission of Angiostrongylus vasorum (Baillet, 1866) to wild Canidae. Compt Rend Acad Sci Paris. 1965;261:4496–7.Google Scholar
- 52.Magi M, Guardone L, Dell’Omodarme M, Prati M, Mignone W, Torracca B, Monni G, Macchioni F. Angiostrongylus vasorum in red foxes (Vulpes vulpes) and badgers (Meles meles) from Central and Northern Italy. Hystrix Ital J Mammal. 2009;20:121–6.Google Scholar
- 55.Caswell JL, Williams KJ. Respiratory system. In: Maxie MG, editor. Pathology of domestic animals. 5th ed. Edinburgh ; New York: Elsevier Saunders; 2007. p. 577–8.Google Scholar
- 56.Smit T, Moraal LG, Bakhuizen T. Pasteurella multocida infections in birds following cat bites (author’s transl). Tijdschr Diergeneesk. 1980;105:327–9.Google Scholar
- 57.Routh AR. Bats. In: Mullineaux E, Best R, Cooper JE, editors. BSAVA Manual of Wildlife Casualties. Gloucester, UK: British Small Animal Veterinary Association; 2003. p. 100.Google Scholar
- 59.Burek K: Mycotic Diseases. In Infectious Diseases of Wild Mammals. Edited by Williams ES, Barker IK. Iowa State University Press: Manson, London; 2001:515–531.Google Scholar
- 63.Rudback E, Sternberg T: Trauma is the major cause of mortality in Finnish otters. Proceedings of the European Wildlife Disease Association 3rd International Conference, Edinburgh; 1998:16–20.Google Scholar
- 67.Krebs JR, Anderson R, Clutton-Brock T, Morrison I, Young D, Donnelly C, Frost S, Woodroffe R. Bovine Tuberculosis in Cattle and Badgers. London: MAFF; 1997 [MAFF Publications].Google Scholar
Open AccessThis article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated.