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Mycobacterium Microti Infections in Free-Ranging Red Deer (Cervus Elaphus) Giovanni Ghielmetti, Anne M

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Mycobacterium Microti Infections in Free-Ranging Red Deer (Cervus Elaphus) Giovanni Ghielmetti, Anne M SYNOPSIS Mycobacterium microti Infections in Free-Ranging Red Deer (Cervus elaphus) Giovanni Ghielmetti, Anne M. Kupca, Matthias Hanczaruk, Ute Friedel, Hubert Weinberger, Sandra Revilla-Fernández, Erwin Hofer, Julia M. Riehm, Roger Stephan, Walter Glawischnig (Sorex araneus), are considered to be primary reservoirs Infections with Mycobacterium microti, a member of the M. tuberculosis complex, have been increasingly reported in for M. microti, several other hosts have been identifi ed, humans and in domestic and free-ranging wild animals. At including domestic and wild animals (3,4). Overall, cats postmortem examination, infected animals may display his- (5,6), New World camelids (7), and free-ranging wild topathologic lesions indistinguishable from those caused by boar (8–10) seem to be prone to M. microti infections; hu- M. bovis or M. caprae, potentially leading to misidentifi ca- mans (11–14) and other animal species, including pigs tion of bovine tuberculosis. We report 3 cases of M. microti (15), goats (16), cattle (17,18), dogs (19), captive meerkats infections in free-ranging red deer (Cervus elaphus) from (20), squirrel monkeys (21), and ferrets (14), are most western Austria and southern Germany. One diseased ani- likely incidental hosts. mal displayed severe pyogranulomatous pleuropneumonia This broad host range, however, highlights the and multifocal granulomas on the surface of the pericardi- pathogenic potential of M. microti and the need to um. Two other animals showed alterations of the lungs and reveal its virulence mechanisms. Comparative ge- associated lymph nodes compatible with parasitic infesta- tion. Results of the phylogenetic analysis including multiple nomics studies have identifi ed >100 genes whose animal strains from the study area showed independent presence are facultative and differ among members infection events, but no host-adapted genotype. Person- of MTBC. Many of these genes occur in chromosom- nel involved in bovine tuberculosis–monitoring programs al regions of difference (RD) that have been deleted should be aware of the fastidious nature of M. microti, its from certain species and that may confer differences pathogenicity in wildlife, and zoonotic potential. in phenotype, host range, and virulence (22). Isolates of the animal-adapted ecotype defi ned as M. microti uberculosis (TB) is one of the most prevalent zoonot- are characterized by the deletion of the RD1mic in the Tic diseases worldwide and remains the leading cause RD1 region, which includes open reading frame cod- of death from a single infectious agent (1). The causative ing for well-known virulence factors, such as early pathogens of TB in humans and animals are a group secreted antigenic target (ESAT) 6, locus tag Rv3875, of closely related acid-fast bacilli commonly known as and CFP-10, a culture fi ltrate protein encoded by the the Mycobacterium tuberculosis complex (MTBC). One neighboring gene Rv3874 (23). Strains lacking RD1 animal-adapted sublineage within the complex, M. mi- are likely to be less virulent or pathogenic than other croti, was fi rst isolated from fi eld voles (Microtus agres- members of the MTBC possessing an intact locus tis) that had granulomatous tuberculosis-like lesions (22). However, pulmonary and disseminated M. mi- (2). Although wild rodents, such as bank voles (Myodes croti infections have been described in both immu- glareolus), wood mice (Apodemus sylvaticus), and shrews nocompromised and immunocompetent human pa- tients in different countries in Europe (11,12,14,24). Author affi liations: Institute for Food Safety and Hygiene, Section Until recently, reports of M. microti infections were of Veterinary Bacteriology, Vetsuisse Faculty University of Zurich, geographically restricted to continental Europe and Zurich, Switzerland (G. Ghielmetti, U. Friedel, R. Stephan); the United Kingdom. However, a recent study from Bavarian Health and Food Safety Authority, Oberschleissheim, South Africa revealed the presence of this Mycobac- Germany (A.M. Kupca, M. Hanczaruk, J.M. Riehm); Institute for terium species in 1.9% of local human tuberculosis Veterinary Disease Control, Austrian Agency for Health and Food cases (25). These fi ndings highlight the potential of Safety (AGES), Innsbruck and Mödling, Austria (H. Weinberger, M. microti to cause clinical illness in immunocompe- S. Revilla-Fernández, E. Hofer, W. Glawischnig) tent patients and suggest that the pathogenicity of DOI: https://doi.org/10.3201/eid2708.210634 certain strains is higher than previously estimated. Emerging Infectious Diseases • www.cdc.gov/eid • Vol. 27, No. 8, August 2021 2025 SYNOPSIS Therefore, it is crucial to identify clinical MTBC iso- were macroscopically inspected; subsequently, histo- lates at the species level, and the zoonotic risk posed pathologic and bacteriologic examinations of the lungs by M. microti should be further evaluated. and lymph nodes were performed. The mode of infection of M. microti can only be speculated for humans, animals, and in particular her- Mycobacterial Analyses and Histologic Examination bivores, such as free-ranging red deer. Similar to that We isolated mycobacteria following a standardized for M. caprae, transmission of M. microti is likely to oc- protocol as described elsewhere (32). In brief, 2–3 g cur indirectly through a contaminated environment. of minced tissue samples were homogenized in 5 mL Wounds in the oral cavity may play an important role 0.9% NaCl solution by using a rotating-blade macera- as entry ports for M. microti; involvement of the lungs, tor system (Ultra-Turrax IKA, https://www.ika.com). heart, and eventually additional organs is most likely a The suspension was decontaminated by using 1% N- consequence of bacteremia, as it is in other animal spe- acetyl-L-cystein-NaOH solution and neutralized with cies (3,5). The first confirmed M. caprae TB case in deer 20 mL phosphate buffer (pH 6.8). We centrifuged the in western Austria was recorded in 1998. Subsequent solution for 20 min at 3300 × g and plated the obtained infections in cattle, deer, and humans were reported in pellet on 2 growth media: Löwenstein-Jensen medium the same area (26). As a consequence, an ongoing wild- with glycerin and PACT (polymyxin B, amphotericin life surveillance program monitoring M. caprae in deer B, carbenicillin, and trimethoprim) and Stonebrink was started in 2008 (27). Furthermore, Germany in 2007 medium with pyruvate and PACT (BD, https://www. and Switzerland in 2013 reported anecdotal outbreaks bd.com). Cultures of lung and lymph node specimens in cattle (28,29). During 2011–2013, a monitoring pro- on solid Stonebrink medium yielded growth of suspi- gram coordinated by the EMIDA ERA-Net (Coordi- cious mycobacterial colonies after 4–6 wk of incubation nation of European Research on Emerging and Major at 37°C. The isolates were identified by using Geno- Infectious Diseases of Livestock European Research Type MTBC reversed line blotting (Hain Lifescience, Area Networks) partnership and including specific re- https://www.hain-lifescience.de). For histologic ex- gions of Austria, Switzerland, Germany, and Italy was amination, we fixed tissue samples in 10% nonbuf- conducted with the aim of investigating the prevalence fered formalin for ≈48 h, then trimmed and routinely of bovine tuberculosis (bTB) in red deer and additional embedded them in paraffin wax. Sections of 3–4 μm wildlife species such as wild boar, chamois, and roe were prepared and stained with hematoxylin and eo- deer (30,31). We report 3 TB cases in red deer identified sin (HE) and Ziehl Neelsen (ZN) or modified ZN (33). within the framework of these monitoring programs. Investigation of Phylogenetic Relationships Study Material and Methods DVR spoligotyping (direct variable repeat spacer oligonucleotide typing) was performed using a com- Cases mercial microarray system (Alere Technologies, Three cases of natural M. microti infections in red deer https://www.globalpointofcare.abbott) with inte- were identified (Table 1). The deer in case 1, a highly grated data analysis as described elsewhere (29). emaciated 9-year-old stag from the province of Vorarl- Multilocus variable-number tandem repeats analysis berg, Austria, was humanely killed by a local game (MLVA) was conducted based on the 24-loci panel warden, who submitted the lungs, heart, and lymphatic standardized for M. tuberculosis typing (34). We am- tissues (including medial retropharyngeal, tracheobron- plified the single markers by endpoint PCR and sub- chial, and mediastinal lymph nodes) fresh for pathoana- sequently analyzed them by using a capillary electro- tomic inspection. Thereafter, histologic examination and phoresis device (29). To investigate the phylogenetic mycobacterial analysis of the lungs were performed. relationships between the 3 isolates from red deer, we The deer in case 2 was a stag 1–3 years of age and in case analyzed 8 additional strains isolated from different 3 a hind >2 years of age, both in the province of Mies- wild and domestic hosts that originated from the re- bach, Germany, where deer are regularly hunted. The gions bordering Germany, Austria, and Switzerland heads, lungs, intestines, and associated lymph nodes by MLVA (Table 2). We calculated a neighbor-joining Table 1. Overview of 3 cases of tuberculosis caused by Mycobacterium microti in red deer, Austria and Germany Case Age, y/sex Year isolated Main findings Country 1 9/M 2017 Severe pyogranulomatous pleuropneumonia, multifocal to coalescing granulomas Austria on the epicardium
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