Epizootiology and Pathologic Findings Associated With a Newly Described Adenovirus in the Red Squirrel, Sciurus Vulgaris

Abstract

An infectious disease caused by Squirrelpox virus has contributed to the decline of red squirrels, Sciurus vulgaris, in the British Isles. Because of the heightened disease surveillance activity in red squirrels, adenovirus infection with associated mortality has been detected. Adenoviral disease is described in other rodent species usually associated with stressors. Here we 1) describe the pathologic findings in red squirrels found dead with adenoviral infection and gastrointestinal disease, and 2) investigate the epizootiology of the disease through pathologic investigation, scanning surveillance, and virologic studies. Ten red squirrels involved in conservation studies were diagnosed with adenoviral infection by electron microscopy or PCR. All squirrels exhibited diarrhea and small intestinal inflammation or hemorrhage was evident in seven cases. Lesions indicative of splenic lymphocytolysis were observed in one squirrel and leukocytic hepatitis in another. No adenovirus was detected in grey squirrels, Sciurus carolinensis, inhabiting the same forest area, but previous serologic studies showed that grey squirrels cannot be discounted as a reservoir of the virus. Scanning surveillance showed that 12% of 493 red squirrels had diarrheal disease and two of 13 free-living red squirrels with diarrheal disease had adenovirus infection. Adenoviral disease in declining free-living wild red squirrel populations in the British Isles occurs at a detectable frequency and its impact on the conservation of this species deserves further attention.

Ljungan Virus and an Adenovirus in Italian Squirrel Populations

“…Outbreaks of enteric adenovirus infections associated with gastrointestinal disease and mortality have been described in both free-living and captive red squirrels in Germany and the UK (e.g., Martínez-Jimé nez et al 2011;Peters et al 2011), where subclinical adenovirus infections among introduced gray squirrels have also been reported (Everest et al 2009). …”

Incorporating habitat distribution in wildlife disease models: conservation implications for the threat of squirrelpox on the Isle of Arran

“…Alternatively, the squirrel Adenovirus may have similarities with the results of the chronic infection since it is less virulent than SQPV but can cause mortality when associated with other stress factors. Adenovirus has been reported in natural red squirrel populations that are free from grey squirrels with the disease persisting for many years (Everest et al, 2013;Martínez-Jiménez et al, 2011). Detailed investigations into the prevalence of Adenovirus in red populations is ongoing (Everest et al, 2013) but our modelling results suggest that the chronic nature of the disease may allow it to spread and persist should it be introduced into a naive population -such as the red population on Arran.…”

Enhancement of wildlife disease surveillance using multiplex quantitative PCR: development of qPCR assays for major pathogens in UK squirrel populations

“…However, differences in selection, geography and time of year may also have been responsible for or contributed to the data obtained. In red squirrels, SADV is believed to be an enteric infection although systemic effects are witnessed, with splenitis commonly reported (Martinez-Jimenez et al 2011;Sainsbury et al 2001). This is supported by our data, with the gastrointestinal tract, liver, blood and spleen showing the highest intensities and prevalence of SADV infection.…”

“…The cause of death of these two squirrels was thought to be due to anaemia, It should be noted that the swab/blood samples appear to be superior to tissue samples in all instances apart from adenovirus in red squirrels when using the qPCR developed in this study secondary to parasitism (Duff et al 2010;Larose et al 2010;Simpson et al 2013b). However, haemorrhage has been reported in 70 % (7/10) of case studies of SADV infection (Martinez-Jimenez et al 2011). The prevalence of SADV in lice found on infected individuals was 80 % (4/5: 95 % CI, 30-99 %), which combined with the relatively high occurrence of viral DNA in blood (67 % (6/9); 95 % CI 31-91 %) may suggest a potential role of the parasite in pathogen transmission.…”

“…This pathogen is thought to have been introduced with the grey squirrel, a theory supported by a high prevalence of exposure despite an absence of clinical disease (Bruemmer et al 2010;Sainsbury et al 2000), an association between seropositive grey squirrels and the appearance of clinical cases of squirrelpox in red squirrels (McInnes et al , 2013Sainsbury et al 2008) and an association of the pathogen in both squirrel species during an outbreak of disease in red squirrels (Chantrey et al 2014). Programmes to reintroduce red squirrels in the UK have been hampered by disease: by SQPV in Norfolk (Carroll et al 2009) and adenovirus in squirrels (SADV) in other areas of the UK (Everest et al 2008(Everest et al , 2012bMartinez-Jimenez et al 2011). SADV appears to cause mortality in wild red squirrels (Duff et al 2007;Everest et al 2012a), although the impact on a population scale is largely unknown with subclinical infections also reported (Everest et al 2014).…”