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Molecular and Serological Footprints of Mycobacterium Avium Subspecies Infections in Zoo Animals

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Molecular and Serological Footprints of Mycobacterium Avium Subspecies Infections in Zoo Animals veterinary sciences Article Molecular and Serological Footprints of Mycobacterium avium Subspecies Infections in Zoo Animals Marco Roller 1,2,3, Sören Hansen 2, Susanne Böhlken-Fascher 2, Tobias Knauf-Witzens 1, 2, 3, 2,4, , Claus-Peter Czerny y, Ralph Goethe z and Ahmed Abd El Wahed * z 1 Wilhelma Zoological-Botanical Gardens Stuttgart, Wilhelma 13, D-70376 Stuttgart, Germany; [email protected] (M.R.); [email protected] (T.K.-W.) 2 Department of Animal Sciences, Division of Microbiology and Animal Hygiene, Faculty of Agricultural Science, Georg-August-University, Burckhardtweg 2, D-37077 Göttingen, Germany; [email protected] (S.H.); [email protected] (S.B.-F.); [email protected] (C.-P.C.) 3 Institute for Microbiology, University of Veterinary Medicine Hannover, Foundation, Bischofsholer Damm 15, D-30173 Hannover, Germany; [email protected] 4 Institute of Animal Hygiene and Veterinary Public Health, University of Leipzig, An den Tierkliniken 43, D-04103 Leipzig, Germany * Correspondence: [email protected]; Tel.: +49-176-6136-0325 RIP. y Senior authorship. z Received: 22 July 2020; Accepted: 19 August 2020; Published: 23 August 2020 Abstract: Background: Mycobacteria of the Mycobacterium avium complex (MAC) pose a significant risk to zoological collections. Mycobacterium avium subspecies paratuberculosis (MAP) is a member of MAC and the causative agent of Johne’s disease. Despite many reports in animals kept in zoological gardens, systemic surveillance has rarely been reported. Methods: In this study, archived serum samples collected from animal species at the Wilhelma Zoological and Botanical Gardens in Stuttgart, Germany, were screened for the presence of antibodies against MAC and MAP. In addition, molecular investigations were performed on necropsy, fecal, and environmental samples. Results: In total, 30/381 serum samples of various mammalian species were positive for MAC antibodies in ELISA, while one sample of a reticulated giraffe (Giraffa camelopardalis reticulata) was positive in MAP-specific ELISA. Samples from many species were positive in pan-Mycobacterium real-time PCR (40/43 fecal samples, 27/43 environmental samples, and 31/90 necropsy samples). Surprisingly, no sample was positive in the MAP-specific molecular assays. However, two environmental samples from primate enclosures were positive in Mycobacterium avium subspecies hominissuis (MAH)-specific real-time PCR. Conclusions: The results reveal serological indications of MAC infections in the zoological collection. However, the presence of a MAP-contaminated environment by a high-shedding individual animal or MAP-infected population is unlikely. Keywords: Mycobacterium avium subspecies paratuberculosis; Johne’s disease; paratuberculosis; Mycobacterium avium complex; zoo animals; serological assays; molecular assays; surveillance; monitoring 1. Introduction The Mycobacterium avium complex (MAC) comprises Mycobacterium avium subspecies avium (MAA), Mycobacterium avium subspecies paratuberculosis (MAP), Mycobacterium avium subspecies silvaticum Vet. Sci. 2020, 7, 117; doi:10.3390/vetsci7030117 www.mdpi.com/journal/vetsci Vet. Sci. 2020, 7, x FOR PEER REVIEW 2 of 17 Vet. Sci. 2020, 7, 117 2 of 14 silvaticum (MAS), and Mycobacterium avium subspecies hominissuis (MAH) [1–3]. Members of MAC are(MAS), not andspecies-specificMycobacterium and avium are frequentlysubspecies associatedhominissuis with(MAH) animal [1–3 ].or Membershuman diseases of MAC causing are not tuberculousspecies-specific lesions and are in frequently lymph associatednodes and, with occa animalsionally, or human parenchymato diseases causingus organs tuberculous [4]. lesionsMAC mycobacteriain lymph nodes and, and, in occasionally,particular, MAP, parenchymatous pose a signif organsicant risk [4]. to MAC zoological mycobacteria collections and, [5–7]. in particular, MAP is anMAP, acid-fast pose abacterium significant causing risk to a zoological contagious, collections chronic, and [5–7 typically]. MAP isfatal, an acid-fast enteric disease bacterium of domestic causing anda contagious, nondomestic chronic, ruminants and typically name fatal,d paratuberculosis enteric disease of(Johne’s domestic disease and nondomestic (JD)) [8]. ruminantsCommon characteristicsnamed paratuberculosis of paratuberculosis (Johne’s diseaseare latent (JD)) and [8 asymptomatic]. Common characteristics infections, while of paratuberculosis only a few animals are oflatent the herd and asymptomaticdevelop clinical infections, symptoms. while Affected only a anim few animalsals in the of advanced the herd developstages of clinical the disease symptoms. suffer fromAffected wasting animals and in gradual the advanced emaciation stages [9]. ofthe Clinical disease paratuberculosis suffer from wasting has andbeen gradual diagnosed emaciation in a wide [9]. diversityClinical paratuberculosis of captive and hasfree-ranging been diagnosed ruminant in a wideand diversitypseudoruminant of captive species, and free-ranging with considerably ruminant differentand pseudoruminant clinical and species,pathological with considerablypictures [10,11]. diff erentHowever, clinical MAP and can pathological also infect pictures nonruminant [10,11]. animalHowever, species, MAP with can alsoless infectclear symptoms nonruminant [12]. animal species, with less clear symptoms [12]. In zoological gardens, various populations of diverse animal species are artificially artificially managed in limited space. They They are are susceptible susceptible to to epidemiologica epidemiologicall situations, situations, similar similar to to livestock livestock herds, herds, such such as high animal density and exposure to a high concentrationconcentration of infectious agents in the population. Hence, MAC infection in zoo animals may be of significant significant relevance in terms of animal welfare and conservationconservation eefforts.fforts. Indeed,Indeed, paratuberculosis paratuberculosis outbreaks outbreaks and and systematic systematic surveys surveys for infectionfor infection and anddisease disease have beenhave reportedbeen reported for several for zoosseveral [13– 19zoos]. Some [13–19]. of these Some studies of these have studies included have investigations included investigationsin nonruminant in speciesnonruminant [20–24 ].species As a result, [20–24]. paratuberculosis As a result, paratuberculosis has become an has essential become part an of essential disease partprevention of disease and prevention surveillance and protocols surveillance of many protocols zoological of many institutions, zoological which institutions, include which preshipment include preshipmentveterinary test veterinary requirements test requirements and strict hygiene and st andrict quarantinehygiene and measures quarantine (see measures the workshop (see the on workshopdiagnosis, on prevention, diagnosis, and prevention, control of and Johne’s control disease of Johne’s in nondomestic disease in hoofstocknondomestic [25]). hoofstock [25]). In this this study, study, we performed a retrospective su surveyrvey on frozen-stored mammalian serum samples collected in the the Wilhelma Wilhelma Zoological and Botanical Botanical Gardens Gardens in in Stuttgart, Stuttgart, Germany, Germany, between 2010 and 2019. The The screening screening was was performed performed using an indirect indirect ELISA specific specific for the antibody of MAC, as well as a second assay targeting the MAP-specific MAP-specific antibody antibody.. In order to identify active or subclinical MAP infection, aa mobilemobile molecularmolecular assay assay based based on on a recombinasea recombinase polymerase polymerase amplification amplification (RPA) (RPA) assay assay was wasapplied applied in the in zoological the zoological garden forgarden onsite for molecular onsite detectionmolecular ofdetection MAP in fecalof MAP and environmentalin fecal and environmentalsamples. The results samples. of the The field results settings of the were field followed settings were by laboratory-based followed by laboratory-based real-time PCR real-time targeting PCRpan- Mycobacteriumtargeting pan-Mycobacteriumspecies MAP, MAA, species and MAP, MAH MAA, (Figure and1 ).MAH (Figure 1). Animal collection of the Zoological and Botanical Gardens Wilhelma Serological Investigations Molecular Investigations Serum samples Fecal samples Environmental samples Necropsy samples 2010-2019; n=381 43 species 43 species 30 animals (3 samples each) MAC ELISA PCR RPA-MAP PCR RPA-MAP PCR 16S rRNA 16S rRNA 16S rRNA 30 positives (Mycobacteria (Mycobacteria (Mycobacteria ) ) ) MAP ELISA IS900-MAP IS900-MAP IS900-MAP IS901-MAA IS901-MAA IS901-MAA IS1245- IS1245- IS1245- MAH MAH MAH Figure 1. Flow chart of the methods used to screen the collected samples. Figure 1. Flow chart of the methods used to screen the collected samples. Vet. Sci. 2020, 7, 117 3 of 14 2. Materials and Methods 2.1. Sample Collection Ethical statement: All samples were collected in accordance with the guidelines of good veterinary practice and the law of the Federal Republic of Germany. The regional administrative authority in Stuttgart, Germany (Regierungspräsidium Stuttgart, Abteilung 3-Landwirtschaft, Ländlicher Raum, Veterinär- und Lebensmittelwesen), has been notified of the study under file number 35-9185.82/0347. 2.1.1. Serum Samples A serologic survey for Mycobacterium avium complex antibodies was performed on frozen-stored serum samples from mammalian species, collected between 2010 and 2019. A total of 381 samples
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