The first report of meningitis in a Greenland shark (Somniosus microcephalus).

The Greenland shark (Somniosus microcephalus) is a large species of shark found in the North Atlantic and Arctic Oceans and is believed to be the longest living vertebrate. Relatively little is known about its biology, abundance, health or diseases. In March 2022, only the third reported UK stranding of this species occurred and it was the first to undergo post-mortem examination. The animal was a sexually immature female, measuring 3.96 m in length and 285 kg in weight, and was in poor nutritional state. Gross findings included haemorrhages in the skin and soft tissues, particularly of the head, and silt in the stomach suggestive of live stranding, bilateral corneal opacity, slightly turbid cerebrospinal fluid (CSF) and patchy congestion of the brain. Histopathological findings included keratitis and anterior uveitis, fibrinonecrotic and lymphohistiocytic meningitis of the brain and proximal spinal cord and fibrinonecrotizing choroid plexitis. A near pure growth of a Vibrio organism was isolated from CSF. This is believed to be the first report of meningitis in this species.

The genomic epidemiology of Escherichia albertii infecting humans and birds in Great Britain.

Escherichia albertii is a recently identified gastrointestinal bacterial pathogen of humans and animals which is typically misidentified as pathotypes of diarrhoeagenic Escherichia coli or Shigella species and is generally only detected during genomic surveillance of other Enterobacteriaceae. The incidence of E. albertii is likely underestimated, and its epidemiology and clinical relevance are poorly characterised. Here, we whole genome sequenced E. albertii isolates from humans (n = 83) and birds (n = 79) isolated in Great Britain between 2000 and 2021 and analysed these alongside a broader public dataset (n = 475) to address these gaps. We found human and avian isolates typically (90%; 148/164) belonged to host-associated monophyletic groups with distinct virulence and antimicrobial resistance profiles. Overlaid patient epidemiological data suggested that human infection was likely related to travel and possibly foodborne transmission. The Shiga toxin encoding stx2f gene was associated with clinical disease (OR = 10.27, 95% CI = 2.98-35.45 p = 0.0002) in finches. Our results suggest that improved future surveillance will further elucidate disease ecology and public and animal health risks associated with E. albertii.

Hinfluences severe disease-mediated population declines in two of the most common garden bird species in Great Britain.

The influence of supplementary feeding of wildlife on disease transmission and its consequent impacts on population dynamics are underappreciated. In Great Britain, supplementary feeding is hypothesised to have enabled the spread of the protozoan parasite, Trichomonas gallinae, from columbids to finches, leading to epidemic finch trichomonosis and a rapid population decline of greenfinch (Chloris chloris). More recently, chaffinch (Fringilla coelebs), has also declined markedly from the second to fifth commonest bird in Britain. Using citizen science data, we show that both declines were driven primarily by reduced adult survival, with the greatest reductions occurring in peri-domestic habitats, where supplementary food provision is common. Post-mortem examinations showed a proportional increase in chaffinch trichomonosis cases, near-contemporaneous with its population decline. Like greenfinches, chaffinches often use supplementary food, but are less associated with human habitation. Our results support the hypothesis that supplementary feeding can increase parasite transmission frequency within and between common species. However, the dynamics behind resultant population change can vary markedly, highlighting the need for integrating disease surveillance with demographic monitoring. Other species susceptible to T. gallinae infection may also be at risk. Supplementary feeding guidelines for wildlife should include disease mitigation strategies to ensure that benefits to target species outweigh risks.

Combining host and vector data informs emergence and potential impact of an Usutu virus outbreak in UK wild birds.

Following the first detection in the United Kingdom of Usutu virus (USUV) in wild birds in 2020, we undertook a multidisciplinary investigation that combined screening host and vector populations with interrogation of national citizen science monitoring datasets to assess the potential for population impacts on avian hosts. Pathological findings from six USUV-positive wild passerines were non-specific, highlighting the need for molecular and immunohistochemical examinations to confirm infection. Mosquito surveillance at the index site identified USUV RNA in Culex pipiens s.l. following the outbreak. Although the Eurasian blackbird (Turdus merula) is most frequently impacted by USUV in Europe, national syndromic surveillance failed to detect any increase in occurrence of clinical signs consistent with USUV infection in this species. Furthermore, there was no increase in recoveries of dead blackbirds marked by the national ringing scheme. However, there was regional clustering of blackbird disease incident reports centred near the index site in 2020 and a contemporaneous marked reduction in the frequency with which blackbirds were recorded in gardens in this area, consistent with a hypothesis of disease-mediated population decline. Combining results from multidisciplinary schemes, as we have done, in real-time offers a model for the detection and impact assessment of future disease emergence events.

Atypical Knemidokoptosis in Two Dunnocks (Prunella modularis) in Southern England.

Avian knemidokoptosis, caused by knemidokoptid mites (Knemidokoptinae: Epidermoptidae), has been reported in wild and domestic birds globally. We report two cases of severe knemidokoptosis in Dunnocks (Prunella modularis) from separate sites in Great Britain, where the disease has previously been reported predominantly in finches and, less frequently, in corvids.

Detection of Usutu virus infection in wild birds in the United Kingdom, 2020.

In August 2020, as part of a long-term disease surveillance programme, Usutu virus was detected in five Eurasian blackbirds (Turdus merula) and one house sparrow (Passer domesticus) from Greater London, England. This was initially detected by reverse transcription-PCR and was confirmed by virus isolation and by immunohistochemical detection of flavivirus in tissues. Phylogenetic analysis identified Usutu virus African 3.2 lineage, which is prevalent in the Netherlands and Belgium, suggesting a potential incursion from mainland Europe.

Isolation and characterisation of Vibrio cholerae from fish examined postmortem at ZSL London Zoo between 2014 and 2018.

BACKGROUND: When suspect Vibrio cholerae were cultured from fish at ZSL London Zoo, investigations were carried out to determine whether they were possible causes of cholera. METHODS: Bacterial culture was carried out on fish examined postmortem and colonies were identified using standard techniques including the API 20NE biochemical test kits. Suspect isolates were submitted to the Public Health England laboratory for additional testing. Separately, a number of fish were submitted for routine histopathology. RESULTS: On 13 occasions between 2014 and 2018, suspected V cholerae were cultured from individuals of eight different freshwater fish species. Archived cultures for eight of these (from six different fish species) were investigated and seven isolates (from five fish species) were confirmed as V cholerae, but all were non-O1, non-O139 strains. Whole-genome sequencing showed that the five fish species had unique V cholerae multilocus sequence types (three isolates from Aphanius danfordii were identical), all of which were genetically distant from human isolates. CONCLUSIONS: There was no evidence that these isolates could cause cholera. Histopathological changes consistent with vibriosis were seen in several fish, suggesting that V cholerae were causing the disease, but there were also concurrent infections or predisposing stress factors.

Novel Salmonella Variant Associated with Mortality in Two Great Spotted Woodpeckers (Dendrocopos major).

Two adult Great Spotted Woodpeckers (Dendrocopos major) from separate sites in Great Britain were examined postmortem in 2013 and 2016. A Salmonella sp. was isolated from multiple tissues in both birds. Histopathology and immunohistochemistry confirmed disseminated salmonellosis. Whole-genome sequencing and biochemical analyses putatively identified both isolates as a novel variant of Salmonella enterica subsp. enterica serovar Hessarek (S. Hessarek). Salmonellosis has seldom been reported in Piciformes, and never before in association with S. Hessarek infection. These findings, therefore, add to current knowledge regarding the range of wild bird species susceptible to this Salmonella serovar, and our understanding of the pathogens affecting Great Spotted Woodpeckers, in particular.

LISTERIA MONOCYTOGENES INFECTION OF FREE-LIVING WESTERN EUROPEAN HEDGEHOGS (ERINACEUS EUROPAEUS).

Listeria monocytogenes is a ubiquitous environmental bacterium that causes disease in a wide range of species. Infection with this pathogen is most frequently diagnosed in ruminant livestock, but is also known to infect people and occasionally wildlife. Postmortem examinations of Western European hedgehogs (Erinaceus europaeus) in Great Britain (2011-2017) identified five (5/266, 2%, 95% confidence interval: 0.8-4.3%) animals with L. monocytogenes infection. The L. monocytogenes isolates comprised three serogroup 1/2a and two serogroup 4 from three multilocus sequence types (2, 37, and 121), all of which were different by single-nucleotide polymorphism analysis, indicating they were distinct and epidemiologically unrelated. These findings are consistent with hedgehogs contracting sporadic infection from the environment, perhaps through eating soil-dwelling invertebrates. Examination of data from scanning surveillance programs focused on other British wildlife species indicates that the hedgehog is one of the wildlife species from which L. monocytogenes has been most frequently identified to date in Great Britain. However, further studies of multiple taxa with comparable sampling efforts are required to assess the relative frequency of L. monocytogenes infection in different wildlife species. The bacterium was isolated from extraintestinal sites in multiple hedgehogs, which may indicate septicemia. However, histological examination was limited and could not discriminate subclinical infection from disease (i.e., listeriosis). Although L. monocytogenes is a zoonotic pathogen, disease in people is typically contracted from the ingestion of contaminated foods. The risk to immunocompetent people of contracting listeriosis from hedgehogs is considered very low to negligible.

Fatal phaeohyphomycosis due to Exophiala sp. infection in a free-living common toad Bufo bufo.

A wild adult female common toad Bufo bufo found dead in Scotland in September 2016 was observed to have hepatomegaly, a large soft tissue mass in the coelomic cavity (2.7 g, 3.5 × 2.3 × 1.8 cm) and numerous dark-red papules (1-2 mm diameter) in the skin and subjacent tissue over the back and dorsal aspects of the limbs. Histopathological examination identified marked hepatitis and coelomitis associated with pigmented fungal hyphae, which are results consistent with a diagnosis of phaeohyphomycosis. Sequencing of the internal transcribed spacer region and the D1-D2 region of the large subunit of the ribosomal RNA gene from affected liver tissue identified the presence of Exophiala (Chaetothyriales) sp., a black yeast previously identified as a cause of amphibian phaeohyphomycosis. To our knowledge, this is the first published report of Exophiala sp. in a wild or captive amphibian in Europe and the first description of phaeohyphomycosis affecting a free-living amphibian in Great Britain. Exophiala spp. are saprobes and opportunistic pathogens. It has been postulated that phaeohyphomycosis is a disease of immunocompromised amphibians; however, we found no evidence of significant concurrent infection or generalised debility in this common toad. Phaeohyphomycosis appears to be a sporadic cause of mortality in amphibians, and this report adds to the growing list of pathogens known to affect wild amphibians in Europe.

Spatio-temporal dynamics and aetiology of proliferative leg skin lesions in wild British finches.

Proliferative leg skin lesions have been described in wild finches in Europe although there have been no large-scale studies of their aetiology or epizootiology to date. Firstly, disease surveillance, utilising public reporting of observations of live wild finches was conducted in Great Britain (GB) and showed proliferative leg skin lesions in chaffinches (Fringilla coelebs) to be widespread. Seasonal variation was observed, with a peak during the winter months. Secondly, pathological investigations were performed on a sample of 39 chaffinches, four bullfinches (Pyrrhula pyrrhula), one greenfinch (Chloris chloris) and one goldfinch (Carduelis carduelis) with proliferative leg skin lesions and detected Cnemidocoptes sp. mites in 91% (41/45) of affected finches and from all species examined. Fringilla coelebs papillomavirus (FcPV1) PCR was positive in 74% (23/31) of birds tested: a 394 base pair sequence was derived from 20 of these birds, from all examined species, with 100% identity to reference genomes. Both mites and FcPV1 DNA were detected in 71% (20/28) of birds tested for both pathogens. Histopathological examination of lesions did not discriminate the relative importance of mite or FcPV1 infection as their cause. Development of techniques to localise FcPV1 within lesions is required to elucidate the pathological significance of FcPV1 DNA detection.

Salmonella Enteritidis ST183: emerging and endemic biotypes affecting western European hedgehogs (Erinaceus europaeus) and people in Great Britain.

The impacts of hedgehog (Erinaceus europaeus) Salmonella infection on public health and on animal welfare and conservation are unknown. We isolated Salmonella Enteritidis multi-locus sequence-type (ST)183 from 46/170 (27%) hedgehog carcasses (27 S. Enteritidis phage type (PT)11, 18 of a novel PT66 biotype and one with co-infection of these PTs) and from 6/208 (3%) hedgehog faecal samples (4 PT11, 2 PT66) from across Great Britain, 2012-2015. Whole genome phylogenetic analysis of the hedgehog isolates and ST183 from people in England and Wales found that PT11 and PT66 form two divergent clades. Hedgehog and human isolates were interspersed throughout the phylogeny indicating that infections in both species originate from a common population. PT11 was recovered from hedgehogs across England and Scotland, consistent with endemic infection. PT66 was isolated from Scotland only, possibly indicating a recent emergence event. People infected with ST183 were four times more likely to be aged 0-4 years than people infected by the more common ST11 S. Enteritidis. Evidence for human ST183 infection being non-foodborne included stronger correlation between geographic and genetic distance, and significantly increased likelihood of infection in rural areas, than for ST11. These results are consistent with hedgehogs acting as a source of zoonotic infection.

Streptococcus pyogenes Infection in a Free-Living European Hedgehog (Erinaceus europaeus).

Streptococcus pyogenes, a common pathogen of humans, was isolated from the carcass of a free-living European hedgehog (Erinaceus europaeus) found in northern England in June 2014. The animal had abscessation of the deep right cervical lymph node, mesenteric lymph nodes and liver. The S. pyogenes strain isolated from the lesions, peritoneal and pleural cavities was characterised as emm 28, which can be associated with invasive disease in humans. This is the first known report of S. pyogenes in a hedgehog and in any free-living wild animal that has been confirmed by gene sequencing. As close associations between wild hedgehogs and people in England are common, we hypothesise that this case might have resulted from anthroponotic infection.

Aprocta cylindrica (Nematoda) infection in a European Robin (Erithacus rubecula) in Britain.

A European Robin (Erithacus rubecula) found dead in England had marked blepharitis and periocular alopecia associated with Aprocta cylindrica (Nematoda: Aproctidae) and concurrent mixed fungal infections. Aprocta cylindrica should be considered a differential diagnosis in periocular abnormalities of robins and other insectivorous, migratory passerines in Western Europe.

Epidemiological evidence that garden birds are a source of human salmonellosis in England and Wales.

The importance of wild bird populations as a reservoir of zoonotic pathogens is well established. Salmonellosis is a frequently diagnosed infectious cause of mortality of garden birds in England and Wales, predominantly caused by Salmonella enterica subspecies enterica serovar Typhimurium definitive phage types 40, 56(v) and 160. In Britain, these phage types are considered highly host-adapted with a high degree of genetic similarity amongst isolates, and in some instances are clonal. Pulsed field gel electrophoresis, however, demonstrated minimal variation amongst matched DT40 and DT56(v) isolates derived from passerine and human incidents of salmonellosis across England in 2000-2007. Also, during the period 1993-2012, similar temporal and spatial trends of infection with these S. Typhimurium phage types occurred in both the British garden bird and human populations; 1.6% of all S. Typhimurium (0.2% of all Salmonella) isolates from humans in England and Wales over the period 2000-2010. These findings support the hypothesis that garden birds act as the primary reservoir of infection for these zoonotic bacteria. Most passerine salmonellosis outbreaks identified occurred at and around feeding stations, which are likely sites of public exposure to sick or dead garden birds and their faeces. We, therefore, advise the public to practise routine personal hygiene measures when feeding wild birds and especially when handling sick wild birds.

Evidence of spread of the emerging infectious disease, finch trichomonosis, by migrating birds.

Finch trichomonosis emerged in Great Britain in 2005 and led to epidemic mortality and a significant population decline of greenfinches, Carduelis chloris and chaffinches, Fringilla coelebs, in the central and western counties of England and Wales in the autumn of 2006. In this article, we show continued epidemic spread of the disease with a pronounced shift in geographical distribution towards eastern England in 2007. This was followed by international spread to southern Fennoscandia where cases were confirmed at multiple sites in the summer of 2008. Sequence data of the ITS1/5.8S/ITS2 ribosomal region and part of the small subunit (SSU) rRNA gene showed no variation between the British and Fennoscandian parasite strains of Trichomonas gallinae. Epidemiological and historical ring return data support bird migration as a plausible mechanism for the observed pattern of disease spread, and suggest the chaffinch as the most likely primary vector. This finding is novel since, although intuitive, confirmed disease spread by migratory birds is very rare and, when it has been recognised, this has generally been for diseases caused by viral pathogens. We believe this to be the first documented case of the spread of a protozoal emerging infectious disease by migrating birds.

Pulsed-field gel electrophoresis supports the presence of host-adapted Salmonella enterica subsp. enterica serovar Typhimurium strains in the British garden bird population.

Salmonellosis is a frequently diagnosed infectious disease of passerine birds in garden habitats within Great Britain with potential implications for human and domestic animal health. Postmortem examinations were performed on 1,477 garden bird carcasses of circa 50 species from England and Wales, 1999 to 2007 inclusive. Salmonellosis was confirmed in 263 adult birds of 10 passerine species in this 11-year longitudinal study. A subset of 124 fully biotyped Salmonella enterica subsp. enterica serovar Typhimurium isolates was examined using pulsed-field gel electrophoresis to investigate the hypothesis that these strains are host adapted and to determine whether this molecular technique offers greater resolution in understanding the epidemiology of Salmonella Typhimurium infection than phage typing alone. For the two most common phage types, definitive type (DT) 40 and DT56v, which together accounted for 97% (120/124) of isolates, pulsed-field gel electrophoresis groupings closely correlated with phage type with remarkably few exceptions. A high degree of genetic similarity (>90%) was observed within and between the two most common pulsed-field gel electrophoresis groups. No clustering or variation was found in the pulsed-field gel electrophoresis groupings by bird species, year, or geographical region beyond that revealed by phage typing. These findings support the hypothesis that there are currently two host-adapted Salmonella phage types, S. Typhimurium DT40 and DT56v, circulating widely in British garden birds and that the reservoir of infection is maintained within wild bird populations. Large-scale multilocus sequence typing studies are required to further investigate the epidemiology of this infection.

A clonal strain of Trichomonas gallinae is the aetiologic agent of an emerging avian epidemic disease.

Trichomonas gallinae is a protozoan parasite that is well characterised as a cause of trichomonosis in columbid and raptor species world-wide. The parasite emerged as a novel infection of British passerines in 2005, leading to epidemic mortality associated with significant declines of breeding populations of greenfinches (Carduelis chloris) and chaffinches (Fringilla coelebs). We characterised the extent of T. gallinae genotypic heterogeneity within the affected wild British avifauna by analysing individual isolates from 17 of the species affected. To do so, we employed improved platform-based multilocus typing tools as well as the hydrogenosomal Fe-hydrogenase gene as a single marker locus for fine-typing. We found no evidence of heterogeneity amongst the parasites infecting British passerines, indicating that a clonal strain of T. gallinae is the causative agent of this emerging infectious disease.

Acute necrotising pneumonitis associated with Suttonella ornithocola infection in tits (Paridae).

Suttonella ornithocola, first isolated from the lungs of British tit species in 1996, was found to be a novel bacterium belonging to the family Cardiobacteriaceae. Comprehensive surveillance of garden bird mortality across Great Britain between April 2005 and April 2009 involved post mortem and microbiological examination of 82 tits (Paridae; multiple species) and six long-tailed tits (Aegithalidae; Aegithalos caudatus). S. ornithocola was isolated from six birds submitted from six incidents of morbidity and mortality involving Paridae and Aegithalidae species with a wide geographical distribution. The mortality incidents occurred sporadically at low incidence throughout the study period, which suggested that the infection is endemic in native bird populations, with a seasonal peak during early spring. Histopathological examination showed multiple foci of acute pulmonary necrosis associated with gram-negative cocco-bacillary bacteria. These findings supported the hypothesis that S. ornithocola is a primary pathogen of tits in Great Britain.

Emerging infectious disease leads to rapid population declines of common British birds.

Emerging infectious diseases are increasingly cited as threats to wildlife, livestock and humans alike. They can threaten geographically isolated or critically endangered wildlife populations; however, relatively few studies have clearly demonstrated the extent to which emerging diseases can impact populations of common wildlife species. Here, we report the impact of an emerging protozoal disease on British populations of greenfinch Carduelis chloris and chaffinch Fringilla coelebs, two of the most common birds in Britain. Morphological and molecular analyses showed this to be due to Trichomonas gallinae. Trichomonosis emerged as a novel fatal disease of finches in Britain in 2005 and rapidly became epidemic within greenfinch, and to a lesser extent chaffinch, populations in 2006. By 2007, breeding populations of greenfinches and chaffinches in the geographic region of highest disease incidence had decreased by 35% and 21% respectively, representing mortality in excess of half a million birds. In contrast, declines were less pronounced or absent in these species in regions where the disease was found in intermediate or low incidence. Also, populations of dunnock Prunella modularis, which similarly feeds in gardens, but in which T. gallinae was rarely recorded, did not decline. This is the first trichomonosis epidemic reported in the scientific literature to negatively impact populations of free-ranging non-columbiform species, and such levels of mortality and decline due to an emerging infectious disease are unprecedented in British wild bird populations. This disease emergence event demonstrates the potential for a protozoan parasite to jump avian host taxonomic groups with dramatic effect over a short time period.