Epidemiology of Mycobacterium bovis infection in feral ferrets (Mustela furo) in New Zealand: I. Pathology and diagnosis

Necropsies from 228 ferrets captured from eight areas in the North and South Islands provided material for an investigation into the epidemiology of tuberculosis in feral ferrets. Mycobacterial culture of pooled lymph nodes (retropharyngeal, respiratory and jejunal) identified the prevalence of infection to be much higher than that estimated from gross lesions only. Seventy-three of the 228 animals examined (32%) were diagnosed as tuberculous. Fifty-three culture-positive ferrets and 18 seemingly uninfected animals were subjected to detailed histopathological examination. The outcomes of these investigations, including the characteristics of the disease, distribution of lesions and aids to diagnosis, are presented. Of the feral carnivores found in New Zealand, the disease persists at high prevalence only in ferrets, and is probably the maintained principally by ingestion of tuberculous carrion. The course of the disease may be prolonged in some ferrets, but tuberculosis eventually causes death of many infected animals. Microscopic hepatic granulomas may be considered pathognomonic of the disease, and have potential to be used as a rapid diagnostic tool in ferrets with no gross lesions.     

A comparison of gross pathology,histopathology, and mycobacterial culture for the diagnosis of tuberculosis in elk (Cervus elaphus).

Using the isolation of Mycobacterium bovis as the reference standard, this study evaluated the sensitivity, specificity and kappa statistic of gross pathology (abattoir postmortem inspection), histopathology, and parallel or series combinations of the two for the diagnosis of tuberculosis in 430 elk and red deer. Two histopathology interpretations were evaluated: histopathology I, where the presence of lesions compatible with tuberculosis was considered positive, and histopathology II, where lesions compatible with tuberculosis or a select group of additional possible diagnoses were considered positive. In the 73 animals from which M. bovis was isolated, gross lesions of tuberculosis were most often in the lung (48), the retropharyngeal lymph nodes (36), the mesenteric lymph node (35), and the mediastinal lymph nodes (16). Other mycobacterial isolates included: 11 M. paratuberculosis, 11 M. avium, and 28 rapidly growing species or M. terrae complex. The sensitivity estimates of gross pathology and histopathology I were 93% (95% confidence limits [CL] 84.97%) and 88% [CL 77.94%], respectively, and the specificity of both was 89% [CL 85.92%]). The sensitivity and specificity of histopathology II were 89% (CL 79.95%) and 77% (CL 72.81%), respectively. The highest sensitivity estimates (93-95% [CL 84.98%]) were obtained by interpreting gross pathology and histopathology in parallel (where an animal had to be positive on at least one of the two, to be classified as combination positive). The highest specificity estimates (94-95% [CL 91-97%] were generated when the two tests were interpreted in series (an animal had to be positive on both tests to be classified as combination positive). The presence of gross or microscopic lesions showed moderate to good agreement with the isolation of M. bovis (Kappa = 65-69%). The results showed that post-mortem inspection, histopathology and culture do not necessarily recognize the same infected animals and that the spectra of animals identified by the tests overlaps.     

Epidemiology of Mycobacterium bovis infection in feral ferrets (Mustela furo) in New Zealand: I. Pathology and diagnosis

Necropsies of 228 ferrets captured from eight areas in the North and South Islands provided material for an investigation into the epidemiology of tuberculosis in feral ferrets. Mycobacterial culture of pooled lymph nodes (retropharyngeal, respiratory and jejunal) identified the prevalence of infection to be much higher than that estimated from gross lesions only. Seventy-three of the 228 animals examined (32%) were diagnosed as tuberculous. Fifty-three culture-positive ferrets and 18 seemingly uninfected animals were subjected to detailed histopathological examination. The outcomes of these investigations, including the characteristics of the disease, distribution of lesions and aids to diagnosis, are presented.

Of the feral carnivores found in New Zealand, the disease persists at high prevalence only in ferrets, and is probably maintained principally by ingestion of tuberculous carrion. The course of the disease may be prolonged in some ferrets, but tuberculosis eventually causes the death of many infected animals. Microscopic hepatic granulomas may be considered pathognomonic of the disease, and have potential to be used as a rapid diagnostic tool in ferrets with no gross lesions.     

Epidemiology and pathogenesis of Mycobacterium bovis infection of red deer (Cervus elaphus) in New Zealand

AIMS: This study was initiated to investigate aspects of the epidemiology, pathogenesis and transmission of tuberculosis in wild red deer, with the aim of determining whether this species may be considered a reservoir host of Mycobacterium bovis in New Zealand. METHOD: One hundred and six wild red deer (Cervus elaphus) carcasses from the Castlepoint and Hauhungaroa Range areas, which are endemic for bovine tuberculosis, were examined for the presence of M. bovis infection. Samples were also examined from 46 skin test-positive farmed deer killed at two deer slaughter premises. Where possible, a standard set of tissues and excretion site samples was collected for mycobacteriological examination. RESULTS: Fifty-eight infected deer were identified, and of these 28% showed no gross lesions. The prevalence of tuberculosis confirmed by culture in the wild deer was 32%. Only one of 18 deer younger than 1 year was infected. Mature deer (>2 years) were 12 times more likely to be infected than those under 1 year of age. Infected older deer were less likely to show typical gross lesions than younger animals. Mycobacterium bovis was isolated from the oropharyngeal tonsil of 34 of 56 (61%) of the infected deer, and this was the most commonly infected site. Gross lesions were found in 18 of the 34 infected tonsils and only one of these showed a purulent tonsillitis. Mycobacterium bovis was recovered from four of 53 nasopharyngeal tonsils, four of 53 oropharyngeal swabs, one of 53 tracheal and nasal swabs, and one of 46 faecal samples, but not from any urine specimens. CONCLUSION: These findings suggest that significant bacillary excretion from infected deer was uncommon, and is more likely to occur in severely affected animals. This study has confirmed the importance of mucosa-associated lymphoid tissues (MALT), particularly the oropharyngeal tonsil, in the pathogenesis of tuberculosis in deer. The findings justify investigation of the hypotheses that the prevalence of tuberculosis in wild deer in New Zealand is high due to transmission of infection from possums, and that in the absence of an infected possum population, the prevalence of tuberculosis in deer is likely to be low, and spatially patchy. CLINICAL RELEVANCE: The results suggest that about one quarter of infected deer show no detectable gross lesions. This implies that many infected carcasses may enter the food chain unrecognised and that the estimated sensitivity and specificity of diagnostic tests may be erroneous if there is a difference in test performance between those conducted on deer with or without gross lesions. Diagnostic sensitivity following slaughter may be improved by routine culture of oropharyngeal tonsils and careful examination of lungs for adhesions and small subpleural tubercles.     

Prevalence of bovine tuberculosis in slaughter cattle in Kenya: a postmortem, microbiological and DNA molecular study

A study to determine the presence and prevalence of bovine tuberculosis in slaughter cattle in Kenya was carried out in two abattoirs from July to November 2009. Routine postmortem meat inspection was performed on a subpopulation of 929 cattle selected randomly from among 4,984. Carcases were inspected for gross tuberculous lesions which were then examined for acid-fast bacilli, (AFB), cultured for isolation of mycobacteria and the isolates characterised by DNA molecular analysis. Of the carcases examined, 176 (18.95?%, 95?% CI) had lesions suggestive of tuberculosis. AFB were observed in 63/176 of the lesioned cattle and mycobacteria were isolated from 64 of them. The isolates were identified as Mycobacterium bovis (19/64), Mycobacterium tuberculosis, (2/64) and mycobacteria other than tuberculosis (43/64). The prevalence of M. bovis by molecular analysis was 2.05?% (95?% CI). This study documents for the first time the presence of bovine tuberculosis among slaughter cattle in Kenya. There is therefore a need to formulate and implement control programmes in order to minimise transmission among animals and to humans. Isolation of M. tuberculosis from cattle underscores the risk tuberculous humans pose to animals.     

Gross and microscopic lesions of naturally occurring tuberculosis in a captive herd of wapiti (Cervus elaphus nelsoni) in Colorado.

A Mycobacterium bovis-infected herd of captive wapiti (Cervus elaphus nelsoni) in Colorado was depopulated after lesions of bovine tuberculosis were confirmed in 8 of 10 tuberculin skin test reactors. Of the 43 animals > 1 year of age, 26 had gross lesions suggestive of tuberculosis, 24 had microscopic lesions of tuberculosis, and 23 had acid-fast bacilli associated with the lesions. Lungs and retropharyngeal lymph nodes were the most frequently affected sites. Most lesions grossly and microscopically resembled tuberculosis in cattle; however, some lesions resembled abscesses or ovine caseous lymphadenitis lesions. Special stains and immunohistochemical techniques labeled few to numerous mycobacteria associated with the lesions.     

Evaluation of supraglottic airway device use during inhalation anesthesia in healthy African pygmy hedgehogs (Atelerix albiventris)

ObjectiveTo evaluate a supraglottic airway device (SGAD) designed for rabbits in African pygmy hedgehogs (Atelerix albiventris) during inhalation anesthesia.Study designProspective, randomized, blinded experimental study.AnimalsA total of 12 adult African pygmy hedgehogs (seven male, five female).MethodsHedgehogs were placed in a chamber and anesthesia was induced using isoflurane in oxygen. Oropharyngeal endoscopy was performed and video recorded. The SGAD (v-gel R1) was inserted and connected to a Mapleson D circuit. Capnography, pulse oximetry and physiologic variables were measured during anesthesia, and lung inflation was tested at 10 and 20 cmH₂O. With the SGAD temporarily disconnected, anesthetized hedgehogs were randomly positioned into right and left lateral, dorsal and sternal recumbency to evaluate the effect of a change in body position on SGAD placement. Oropharyngeal endoscopy was repeated at the end of anesthesia, and recovery time was recorded. Pre- and post-SGAD placement endoscopy videos were retrospectively reviewed and scored for gross trauma.ResultsThe median [interquartile range (IQR)] time to successful SGAD placement was 38 (16–68) seconds. The time to SGAD placement decreased as the study progressed. SGAD required repositioning in six hedgehogs, median 2.5 (IQR, 1–3.5) adjustments each, to successfully perform lung inflation or maintain capnography readings. Lung inflation at 10 cmH₂O was successfully performed without leakage in nine animals, and in the other three animals after adjusting the SGAD at 1–2 time points. Inflation at 20 cmH₂O was rarely achieved without an air leak. Changes in heart and respiratory rates during anesthesia were not clinically relevant. Median endoscopic scores were 0 (no lesions) for both pre-and postplacement.Conclusions and clinical relevanceThe SGAD was relatively quickly and easily placed, permitted lung inflation and caused no significant oropharyngeal damage. The SGAD is a practical option for airway management in African pygmy hedgehogs.     

Unilateral proptosis and orbital cellulitis in eight African hedgehogs (Atelerix albiventris).

Eight African hedgehogs (Atelerix albiventris) were presented with unilateral proptosis. Six animals presented specifically for an ocular problem, whereas two had concurrent neurologic disease. Enucleation and light microscopic examination of tissues was performed in five animals, and euthanasia followed by complete postmortem examination was performed in three animals. Histopathologic findings in all hedgehogs included orbital cellulitis, panophthalmitis, and corneal ulceration, with perforation in seven of eight eyes. The etiology of the orbital cellulitis was not determined, but it appeared to precede proptosis. Orbits in hedgehogs are shallow and the palpebral fissures are large, which may predispose them to proptosis, similar to brachycephalic dogs. This clinical presentation was seen in 15% (8/54) of African hedgehogs presented to the Western College of Veterinary Medicine over a 2-yr period from January 1995 to December 1996 and warrants further investigation.     

Adiaspiromycosis in suspected cases of pulmonary tuberculosis in the common brushtail possum (Trichosurus vulpecula)

Pulmonary adiaspiromycosis was diagnosed in 15 of 17 common brushtail possums (Trichosurus vulpecula) examined for bovine tuberculosis. Emmonsia crescens was isolated from two of the affected animals. This is the first reported isolation of this dimorphic fungus in New Zealand. The infections varied from light to heavy with sparsely distributed, focal, 1-2 mm diameter, grey-white spherical granulomas in the lightly infected cases to innumerable foci throughout the lungs in the heavily infected cases. Histologically, the lesions were characterised by a central fungal adiaspore consistent in morphology with E. crescens located in alveolar spaces or bronchioles. These were surrounded by a cuff of granulomatous inflammation which varied in density and extent in proportion to the degree of degeneration exhibited by the organism. The lesions in most cases of adiaspiromycosis in the possum are sufficiently distinctive to allow their differentiation from tuberculosis by gross examination, but where any doubt exists over the possibility of dual infection by Emmonsia and Mycobacterium species differentiation should be made on the basis of a histological examination of the tissue and culture for mycobacterial organisms.     

A retrospective study (2006-2020) of cytology and biopsy findings in pet rabbits (Oryctolagus cuniculus), ferrets (Mustela putorius furo) and four-toed hedgehogs (Atelerix albiventris) seen at an exotic animal clinic in Tokyo,Japan

Background: Rabbits, ferrets, and four-toed hedgehogs are popular exotic pets, but comprehensive epidemiological studies in these animals have been rarely conducted. The present study aims to clarify the incidence of neoplastic and non-neoplastic diseases in pet rabbits, ferrets and four-toed hedgehogs in Japan. Methods: We histologically/cytologically investigated 1098 samples from 883 rabbits, 812 samples from 521 ferrets and 561 samples from 468 four-toed hedgehogs that were collected at Miwa Exotic Animal Hospital and submitted to the Laboratory of Veterinary Pathology, The University of Tokyo between 2006 and 2020. The examinations of necropsy samples were not included in the present study. Results: Of the 1098 samples from diseased rabbits, 721 (65.7%) were diagnosed as neoplastic and 377 (34.3%) were as non-neoplastic. Uterine adenocarcinoma (21.1%), cutaneous soft tissue sarcoma (15.1%) and mammary gland adenocarcinoma (8.2%) were the most commonly encountered neoplasms. Endometrial hyperplasia (35.8%), testicular atrophy (4.2%) and uterine adenomyosis (3.7%) were the most common non-neoplastic lesions in rabbits. Of the 812 samples from diseased ferrets, 487 (60.0%) were diagnosed as neoplastic and 325 (40.0%) were as non-neoplastic. Adrenocortical tumor (23.2%), lymphoma (19.3%) and pancreatic islet cell tumor (11.5%) were the most commonly encountered neoplasms. Extramedullary hematopoiesis in the spleen (10.5%), lymph node hyperplasia (7.7%) and cholangiohepatitis (4.6%) were the most common non-neoplastic lesions in ferrets. Of the 561 samples from diseased hedgehogs, 338 (60.2%) were diagnosed as neoplastic and 223 (39.8%) were as non-neoplastic. Endometrial stromal tumor and endometrial mixed tumor (23.7%), oral squamous cell carcinoma (13.0%) and cutaneous soft tissue sarcoma (11.5%) were the most commonly encountered neoplasms. Gingivitis/stomatitis (39.5%), endometrial hyperplasia (18.8%) and dermatitis (6.7%) were the most common non-neoplastic lesions in hedgehogs. Conclusions and clinical relevance: Information obtained from the present study will provide a useful reference for veterinarians working with these exotic animals. Based on the literature search, this is the largest-scale retrospective study on disease incidence in hedgehogs.     

Tuberculosis outbreak in a dromedary racing herd and rapid serological detection of infected camels

A recent outbreak of tuberculosis (TB) in a dromedary racing herd of 58 animals involved 3 infected animals. Disease was confirmed at necropsy by finding gross lesions from which Mycobacterium bovis (antelope type) was isolated. Sera collected from the camels in this herd were used to evaluate two new serological methods, Multiantigen Print Immunoassay (MAPIA) and rapid test (RT) developed using the lateral-flow technology, in comparison with the intradermal tuberculin tests. Antibodies were found in all three infected dromedaries by both RT and MAPIA, but not in the remaining 55 animals in the herd. With the limited number of animals tested in this study, the serological assays showed the potential for convenient, rapid, and accurate diagnosis of TB in live camels.     

Histological and immunohistochemical features of cutaneous mast cell tumor in six captive four-toed hedgehogs (Atelerix albiventris)

This report described the histopathological and immunohistochemical features of cutaneous mast cell tumor (MCT) in six hedgehogs. The hedgehogs presented single cutaneous mass with ulcer and crusting. Histologically, the neoplastic lesions were characterized by the proliferation of well-differentiated mast cells (3 cases), and atypical mast cells (3 cases) with one atypical histiocytic morphology. Immunohistochemically, tumor cells were positive for KIT and mast cell tryptase, and were negative for Iba-1. In well-differentiated MCT, all patients were clinically improved and survived more than 365 days after surgical excision, whereas an atypical histiocytic MCT showed aggressive behavior with re-recurrence, and the animal died 115 days after surgery. These findings suggest that, compatible with other animals, well-differentiated MCT has a better prognosis in hedgehogs.     

Naturally occurring tuberculosis caused by Mycobacterium bovis in brushtail possums (Trichosurus vulpecula): I. An epidemiological analysis of lesion distribution

Gross and microscopic lesion distributions and culture test results are described for 73 tuberculous possums recovered from a series of cross-sectional studies involving about 500 detailed necropsies. Pathological findings from 11 terminally ill tuberculous possums are also described. Quantitative epidemiological techniques were applied to lesion site data to assess factors influencing the pathogenesis of the disease. In possums with gross lesions, the number of distinct body sites affected varied from one to 10 per animal, with a mean of 4.6. The total number of gross plus microscopic lesions varied from one to 28 per animal with a mean of 11.6, indicating that the degree of generalisation of disease was much greater than appeared grossly. Of 119 possums with no gross lesions which were subjected to additional examinations, tuberculosis was diagnosed in ten (8.4%) by histology or culture of pooled lymph nodes. Among cross-sectional sample tuberculous possums, lesions were found in lungs in 85%, in axillary lymphocentres in 85%, in inguinal lymphocentres in 69%, and in either axillary or inguinal lymphocentres in 95%, indicating that the disease spread rapidly to multiple body sites. More males than females were infected (relative risk = 1.78). When cross-sectionally sampled infected and non-infected possums were compared, no significant associations were found between the presence/absence of disease and either age or indices of body condition, although debility was seen in animals with terminal illness.     

Prevalence of Mycobacterium bovis infection in cervids on privately owned ranches

OBJECTIVE: To determine prevalence of tuberculosis caused by infection with Mycobacterium bovis in cervids on privately owned ranches in northeastern lower Michigan. DESIGN: Epidemiologic survey. ANIMALS: Cervids on 96 privately owned ranches. PROCEDURES: A combination of slaughter and skin tuberculin testing was used to collect data. Infection with M. bovis was confirmed by use of standard necropsy and bacteriologic culture techniques. RESULTS: Cervids with tuberculosis were detected on 1 of the 96 ranches. The apparent prevalence of tuberculosis in cervids from the 96 ranches was 1.1 cases/100 cervids (21 cases/1,867 cervids tested). For the ranch with infected cervids, prevalence of infection with M. bovis was 12.1 cases/100 cervids (21 cases/174 cervids tested). No obvious gross lesions were seen in 8 of 21 white-tailed deer and 1 coyote with culture-confirmed M. bovis infection. CONCLUSIONS AND CLINICAL RELEVANCE: The lack of visible lesions in a substantial proportion of infected animals should be taken into consideration in studies involving detection and prevalence of tuberculosis.     

Quantification of the relative efficiency of factory surveillance in the disclosure of tuberculosis lesions in attested Irish cattle

In Ireland, factory surveillance of cattle for gross lesions is an important supplementary method for detecting herds infected with bovine tuberculosis (tb), and in recent years between 27 and 46 per cent of all new herd breakdowns in any year have been detected by this method. The aim of this study was to determine the relative efficiency of factories in detecting lesions among attested cattle slaughtered during 2003 and 2004. National databases were available on animal slaughter, programmes of tuberculin testing for bovine tb and laboratory confirmation of suspected lesions. Factories were ranked according to their submission risk (number of animals submitted with lesions/number of attested animals killed) and confirmation risk (number of animals with laboratory-confirmed lesions/number of animals submitted with lesions), adjusting for the risk profile of the animals slaughtered, including potential confounding factors such as their age and sex, whether they were purchased or homebred, the test history of their herd, the prevalence of bovine tb in the area and the season of slaughter. Approximately 3.7 million cattle were slaughtered in 42 Irish export-licensed factories during the two years. Complete data were available for 2,374,987 animals from 84,510 attested herds in 2845 District Electoral Divisions. Samples from 7398 animals with suspected tb lesions were submitted for laboratory examination; 4767 (64.4 per cent) were positive, 2011 were negative and 620 were inconclusive. The average unadjusted submission risk for all the factories was 22 per 10,000, ranging from 0 to 58 per 10,000. The unadjusted factory confirmation risk (excluding factories that had sent in fewer than 10 lesions) varied between 34.3 per cent and 86.3 per cent. The unadjusted and adjusted submission and confirmation risks were highly correlated, and animal-related factors (including their characteristics and origin) therefore did not contribute to the variations in factory-level submission and confirmation risks.     

The distribution of gross lesions of tuberculosis caused by Mycobacterium bovis in feral ferrets (Mustela furo) from Otago, New Zealand

The distribution of gross lesions of Mycobacterium bovis was examined in 94 tuberculous feral ferrets (Mustela furo) collected from 1992 to 1995 from areas of Otago endemic for bovine tuberculosis. Overall, 56.4% of tuberculous ferrets had single-site lesions, 24.5% had multiple infections and 19.1% had generalised infections. The mesenteric lymph node was the most common site of infection (34.5% of all lesions), with the retropharyngeal (17%) and the prescapular lymph nodes (16.4%) also frequently infected. Only 2.9% of lesions involved the respiratory tract. Of single-site lesions, 60.4% were in the mesenteric lymph node. The high proportion of lesions in the alimentary tract suggests that the ingestion of infectious material, possibly carrion or prey, is an important source of infection. Peripheral lymph nodes contributed to 24.5% of all infections, suggesting that within species transmission by social contact such as fighting and mating also occurs. Open and respiratory lesions were found in 11.7% of tuberculous ferrets, which suggests that ferrets are potentially infectious and therefore may be involved in the transmission of bovine tuberculosis to domestic stock and other mammals. The distribution of gross M. bovis lesions in ferrets is compared to those observed in possums (Trichosurus vulpecula) and badgers (Meles meles).     

Isolation of Mycobacterium avium from waterfowl with polycystic livers

An unusual gross appearance of avian tuberculosis, where fluid-filled thin-walled cysts are produced and grossly apparent in preference to granulomas, is presented. Histopathology confirmed the granulomatous nature of the lesions and the presence of intracellular acid-fast organisms. Mycobacterium avium complex was cultured from affected organs. The unusual gross presentation in these cases indicates the need to consider tuberculosis in the differential of cystic diseases of avian livers.     

Endometrial polyps in 2 African pygmy hedgehogs

Reports of spontaneously occurring endometrial polyps in animals are rare and have only involved a few species. This report is intended to advise veterinarians that older African pygmy hedgehogs may develop endometrial polyps and that these lesions can be a cause of bloody vaginal discharge, sometimes interpreted as hematuria.