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Leprosy in squirrels: an ancient disease in an endangered wildlife host

Leprosy is an ancient human disease that was thought to have been eradicated from the British Isles. The last case of autochthonous human infection was documented in the 1950’s. Natural infection with leprosy bacilli in species other than humans was first described in ninebanded armadillos in the 1970s in the United States of America. Recently, both bacterial species causing leprosy, Mycobacterium leprae and Mycobacterium lepromatosis, were isolated from Eurasian red squirrels (Sciurus vulgaris, ERS) across the British Isles. ERS are endangered in this part of their range, and efforts are made for their protection. This thesis offers insight into important aspects (clinical presentation, pathology, epidemiology) of the basic description of leprosy in live ERS, based on data from two wild British island ERS populations naturally infected with leprosy bacilli. The populations, one in Scotland and one in England, were studied for 18 and 24 months respectively, with live sampling taking place every six months. Additionally, samples from ERS, Eastern grey squirrels (Sciurus carolinensis, GS) and Pallas’s squirrels (Callosciurus erythraeus, PS) were obtained from Britain (ERS, GS), Germany (ERS, PS) and Italy (ERS, GS, PS) and screened for the presence of leprosy bacilli to provide new epidemiological surveillance information on squirrel leprosy. Established, adapted, and novel tests were used to diagnose leprosy in squirrels. Accurate clinical diagnosis is important to identify populations affected by the disease. Serological methods were useful to confirm the clinical diagnosis. Molecular methods were the only way to identify leprosy bacilli in squirrels without clinical signs of disease. A diagnostic decision tree is proposed to allow optimised, consistent use of the methods now available depending on the situation in which a diagnosis is sought. ERS that are infected with M. leprae and develop clinical leprosy usually showed a multibacillary, lepromatous or borderline lepromatous form of the disease. Lepromatous leprosy is characterised by an inability of the host immune response to control bacterial replication and dissemination. Leprosy in ERS progressed slowly, and the intensity of lesions could easily be separated into four categories from mild to severe based on lesion size, structural characteristics and the presence or absence of ulceration. Several months passed between the time when the bacteria first became detectable in an ERS tissues and the onset of clinical disease. Clinical disease then progressed on varying timescales in different individuals, but usually allowed the individuals to thrive for long time frames (months – years). The maximum time period a clinically diseased ERS was followed in this study was 18 months. Prevalence and morbidity differed in individual ERS populations. In one population the total apparent two-year prevalence of leprosy was 36% with a morbidity rate of 22% for the same population and timeframe. In the other the apparent two-year prevalence was only 4% and no clinical cases of leprosy were observed. The presence of leprosy did not have a negative effect on individual ERS or whole populations that could be measured using health indicators such as body condition, weight, general health and ectoparasite burdens. As part of this study, M. leprae was identified in ERS in two new locations within the UK, but not in British GS or any squirrel species in Germany or Italy. The results indicate that leprosy alone is unlikely to be a major factor contributing to ERS mortalities and thus may not be of great conservation concern in this species. Continued research into ERS leprosy in natural systems could provide valuable insight into disease dynamics that may benefit humans and other hosts in a One Health and conservation medicine framework.

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Schilling A
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The University of Edinburgh
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