Nontuberculous Mycobacteria: Ecology and Impact on Animal and Human Health

A special issue of Microorganisms (ISSN 2076-2607).

Deadline for manuscript submissions: closed (30 September 2021) | Viewed by 28915

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Guest Editor
Faculty of Regional Development and International Studies, Mendel University in Brno, Brno, Czech Republic
Interests: bovine tuberculosis; avian mycobacteriosis; paratuberculosis; environmental saprophytic mycobacteria; ecology of nontuberculous mycobacteria
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Special Issue Information

Dear Colleagues,

Nontuberculous mycobacteria (NTM) represent an important group of environmentally saprophytic and potentially pathogenic bacteria which can cause serious mycobacterioses in humans and animals. The sources of infections often remain undetected except for water-borne, water-washed, water-based or water-related infections caused by the group of the Mycobacterium avium complex, Mycobacterium fortuitum and other NTM species, Mycobacterium marinum infection known as fish tank granuloma, and Mycobacterium ulcerans infection described as Buruli ulcer.

NTM could also be considered soil-borne pathogens (sapronoses). Currently, there is an increasing amount of interest in mycobacterioses diagnosed in humans and in husbandry animals (especially pigs) caused by NTM species present in peat bogs, potting soil, and other matrices. A lot of clinically relevant NTM species could be considered due to the currently published data as permanent, periodic, transient, and incidental sapronoses.

NTM are present in dust particles and in aerosol, which represent serious risk factors during aerogenous infection in immunocompetent and immunosuppressed host organisms. The ecology of Mycobacterium kansasii causing endemic infections in mining areas is not exactly described.

In 2019, a new taxonomy was suggested, and since 1896, the known Mycobacterium genus with more than 170 species and subspecies has been divided into five genera: Mycobacterium, Mycobacteroides, Mycolicibacillus, Mycolicibacter, and Mycolicibacterium. The clinical relevance and ecology of these new genera are currently intensively studied.

The aim of this Special Issue of Microorganisms is to present a collection of articles that provide a current view of the research in NTM epidemiology and ecology. Manuscripts covering all aspects of research relating to NTM sources, clinical relevance, therapy and especially prevention of mycobacterioses are welcome.

Prof. Ivo Pavlík
Guest Editor

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Keywords

  • molecular epidemiology and epizootiology of mycobacterioses
  • new detection and diagnostic methods
  • multidrug resistance
  • phenotypes for resistance and susceptibility to mycobacterioses

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Published Papers (10 papers)

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Editorial

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7 pages, 235 KiB  
Editorial
Nontuberculous Mycobacteria: Ecology and Impact on Animal and Human Health
by Ivo Pavlik, Vit Ulmann and Joseph O. Falkinham III
Microorganisms 2022, 10(8), 1516; https://doi.org/10.3390/microorganisms10081516 - 27 Jul 2022
Cited by 5 | Viewed by 2772
Abstract
Nontuberculous mycobacteria (NTM) represent an important group of environmentally saprophytic and potentially pathogenic bacteria that can cause serious mycobacterioses in humans and animals. The sources of infections often remain undetected except for soil- or water-borne, water-washed, water-based, or water-related infections caused by groups [...] Read more.
Nontuberculous mycobacteria (NTM) represent an important group of environmentally saprophytic and potentially pathogenic bacteria that can cause serious mycobacterioses in humans and animals. The sources of infections often remain undetected except for soil- or water-borne, water-washed, water-based, or water-related infections caused by groups of the Mycobacterium (M.) avium complex; M. fortuitum; and other NTM species, including M. marinum infection, known as fish tank granuloma, and M. ulcerans infection, which is described as a Buruli ulcer. NTM could be considered as water-borne, air-borne, and soil-borne pathogens (sapronoses). A lot of clinically relevant NTM species could be considered due to the enormity of published data on permanent, periodic, transient, and incidental sapronoses. Interest is currently increasing in mycobacterioses diagnosed in humans and husbandry animals (esp. pigs) caused by NTM species present in peat bogs, potting soil, garden peat, bat and bird guano, and other matrices used as garden fertilizers. NTM are present in dust particles and in water aerosols, which represent certain factors during aerogenous infection in immunosuppressed host organisms during hospitalization, speleotherapy, and leisure activities. For this Special Issue, a collection of articles providing a current view of the research on NTM—including the clinical relevance, therapy, prevention of mycobacterioses, epidemiology, and ecology—are addressed. Full article

Research

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14 pages, 578 KiB  
Article
Nontuberculous Mycobacteria Prevalence in Aerosol and Spiders’ Webs in Karst Caves: Low Risk for Speleotherapy
by Dana Hubelova, Vit Ulmann, Pavel Mikuska, Roman Licbinsky, Lukas Alexa, Helena Modra, Milan Gersl, Vladimir Babak, Ross Tim Weston and Ivo Pavlik
Microorganisms 2021, 9(12), 2573; https://doi.org/10.3390/microorganisms9122573 - 13 Dec 2021
Cited by 7 | Viewed by 2644
Abstract
A total of 152 aerosol and spider web samples were collected: 96 spider’s webs in karst areas in 4 European countries (Czech Republic, France, Italy, and Slovakia), specifically from the surface environment (n = 44), photic zones of caves (n = [...] Read more.
A total of 152 aerosol and spider web samples were collected: 96 spider’s webs in karst areas in 4 European countries (Czech Republic, France, Italy, and Slovakia), specifically from the surface environment (n = 44), photic zones of caves (n = 26), and inside (aphotic zones) of caves (n = 26), 56 Particulate Matter (PM) samples from the Sloupsko-Sosuvsky Cave System (speleotherapy facility; n = 21) and from aerosol collected from the nearby city of Brno (n = 35) in the Czech Republic. Nontuberculous mycobacteria (NTM) were isolated from 13 (13.5%) spider’s webs: 5 isolates of saprophytic NTM (Mycobacterium gordonae, M. kumamotonense, M. terrae, and M. terrae complex) and 6 isolates of potentially pathogenic NTM (M. avium ssp. hominissuis, M. fortuitum, M. intracellulare, M. peregrinum and M. triplex). NTM were not isolated from PM collected from cave with the speleotherapy facility although mycobacterial DNA was detected in 8 (14.3%) samples. Temperature (8.2 °C, range 8.0–8.4 °C) and relative humidity (94.7%, range 93.6–96.6%) of air in this cave were relatively constant. The average PM2.5 and PM10 mass concentration was 5.49 µg m−3 and 11.1 µg m−3. Analysed anions (i.e., F, Cl, NO2, SO42−, PO43− and NO3) originating largely from the burning of wood and coal for residential heating in nearby villages in the surrounding area. The air in the caves with speleotherapy facilities should be monitored with respect to NTM, PM and anions to ensure a safe environment. Full article
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20 pages, 1475 KiB  
Article
Nontuberculous Mycobacteria Prevalence in Bats’ Guano from Caves and Attics of Buildings Studied by Culture and qPCR Examinations
by Ivo Pavlik, Vit Ulmann, Helena Modra, Milan Gersl, Barbora Rantova, Jan Zukal, Katerina Zukalova, Ondrej Konecny, Vlastislav Kana, Pavel Kubalek, Vladimir Babak and Ross Tim Weston
Microorganisms 2021, 9(11), 2236; https://doi.org/10.3390/microorganisms9112236 - 27 Oct 2021
Cited by 10 | Viewed by 2564
Abstract
A total of 281 guano samples were collected from caves (N = 181) in eight European countries (Bulgaria, Czech Republic, France, Hungary, Italy, Romania, Slovakia and Slovenia) and attics in the Czech R. (N = 100). The correlation of detection of mycobacteria between [...] Read more.
A total of 281 guano samples were collected from caves (N = 181) in eight European countries (Bulgaria, Czech Republic, France, Hungary, Italy, Romania, Slovakia and Slovenia) and attics in the Czech R. (N = 100). The correlation of detection of mycobacteria between Ziehl–Neelsen (ZN) microscopy and culture examination and qPCR was strong. ZN microscopy was positive in guano from caves (58.6%) more than double than positivity in guano from attics (21.0%; p < 0.01). From 89 mycobacterial isolates (73 isolates from cave guano and 16 isolates from attics’ guano), 68 (76.4%) isolates of 19 sp., ssp. and complex were identified as members of three Groups (M. fortuitum, M.chelonae, and M. mucogenicum) and four complexes (M. avium, M. terrae, M.vaccae, and M.smegmatis). A total of 20 isolates (22.5%) belonged to risk group 1 (environmental saprophytes), 48 isolates (53.9%) belonged to risk group 2 (potential pathogens), and none of the isolates belonged to risk group 3 (obligatory pathogens). When comparing bat guano collected from caves and attics, differences (p < 0.01; Mann–Whitney test) were observed for the electrical conductivity, total carbon, total organic, and total inorganic carbon. No difference (p > 0.05; Mann–Whitney test) was found for pH and oxidation-reduction potential parameters. Full article
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18 pages, 12090 KiB  
Article
Recovery of Mycobacteria from Heavily Contaminated Environmental Matrices
by Vit Ulmann, Helena Modrá, Vladimir Babak, Ross Tim Weston and Ivo Pavlik
Microorganisms 2021, 9(10), 2178; https://doi.org/10.3390/microorganisms9102178 - 19 Oct 2021
Cited by 12 | Viewed by 2386
Abstract
For epidemiology studies, a decontamination method using a solution containing 4.0% NaOH and 0.5% tetradecyltrimethylammonium bromide (TDAB) represents a relatively simple and universal procedure for processing heavily microbially contaminated matrices together with increase of mycobacteria yield and elimination of gross contamination. A contamination [...] Read more.
For epidemiology studies, a decontamination method using a solution containing 4.0% NaOH and 0.5% tetradecyltrimethylammonium bromide (TDAB) represents a relatively simple and universal procedure for processing heavily microbially contaminated matrices together with increase of mycobacteria yield and elimination of gross contamination. A contamination rate only averaging 7.3% (2.4% in Cluster S; 6.9% in Cluster R and 12.6% in Cluster E) was found in 787 examined environmental samples. Mycobacteria were cultured from 28.5% of 274 soil and water sediments samples (Cluster S), 60.2% of 251 samples of raw and processed peat and other horticultural substrates (Cluster R), and 29.4% of 262 faecal samples along with other samples of animal origin (Cluster E). A total of 38 species of slow and rapidly growing mycobacteria were isolated. M. avium ssp. hominissuis, M. fortuitum and M. malmoense were the species most often isolated. The parameters for the quantitative detection of mycobacteria by PCR can be significantly refined by treating the sample suspension before DNA isolation with PMA (propidium monoazide) solution. This effectively eliminates DNA residue from both dead mycobacterial cells and potentially interfering DNA segments present from other microbial flora. In terms of human exposure risk assessment, the potential exposure to live non-tuberculous mycobacteria can be more accurately determined. Full article
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10 pages, 4114 KiB  
Article
Validation of a Novel Diagnostic Approach Combining the VersaTREK™ System for Recovery and Real-Time PCR for the Identification of Mycobacterium chimaera in Water Samples
by Roberto Zoccola, Alessia Di Blasio, Tiziana Bossotto, Angela Pontei, Maria Angelillo, Alessandro Dondo, Maria Goria and Simona Zoppi
Microorganisms 2021, 9(5), 1031; https://doi.org/10.3390/microorganisms9051031 - 11 May 2021
Cited by 3 | Viewed by 2708
Abstract
Mycobacterium chimaera is an emerging pathogen associated with endocarditis and vasculitis following cardiac surgery. Although it can take up to 6–8 weeks to culture on selective solid media, culture-based detection remains the gold standard for diagnosis, so more rapid methods are urgently needed. [...] Read more.
Mycobacterium chimaera is an emerging pathogen associated with endocarditis and vasculitis following cardiac surgery. Although it can take up to 6–8 weeks to culture on selective solid media, culture-based detection remains the gold standard for diagnosis, so more rapid methods are urgently needed. For the present study, we processed environmental M. chimaera infected simulates at volumes defined in international guidelines. Each preparation underwent real-time PCR; inoculates were placed in a VersaTREK™ automated microbial detection system and onto selective Middlebrook 7H11 agar plates. The validation tests showed that real-time PCR detected DNA up to a concentration of 10 ng/µL. A comparison of the isolation tests showed that the PCR method detected DNA in a dilution of ×102 CFU/mL in the bacterial suspensions, whereas the limit of detection in the VersaTREK™ was <10 CFU/mL. Within less than 3 days, the VersaTREK™ detected an initial bacterial load of 100 CFU. The detection limit did not seem to be influenced by NaOH decontamination or the initial water sample volume; analytical sensitivity was 1.5 × 102 CFU/mL; positivity was determined in under 15 days. VersaTREK™ can expedite mycobacterial growth in a culture. When combined with PCR, it can increase the overall recovery of mycobacteria in environmental samples, making it potentially applicable for microbial control in the hospital setting and also in environments with low levels of contamination by viable mycobacteria. Full article
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12 pages, 465 KiB  
Article
Gene Sequencing and Phylogenetic Analysis: Powerful Tools for an Improved Diagnosis of Fish Mycobacteriosis Caused by Mycobacterium fortuitum Group Members
by Davide Mugetti, Mattia Tomasoni, Paolo Pastorino, Giuseppe Esposito, Vasco Menconi, Alessandro Dondo and Marino Prearo
Microorganisms 2021, 9(4), 797; https://doi.org/10.3390/microorganisms9040797 - 10 Apr 2021
Cited by 12 | Viewed by 2886
Abstract
The Mycobacterium fortuitum group (MFG) consists of about 15 species of fast-growing nontuberculous mycobacteria (NTM). These globally distributed microorganisms can cause diseases in humans and animals, especially fish. The increase in the number of species belonging to MFG and the diagnostic techniques panel [...] Read more.
The Mycobacterium fortuitum group (MFG) consists of about 15 species of fast-growing nontuberculous mycobacteria (NTM). These globally distributed microorganisms can cause diseases in humans and animals, especially fish. The increase in the number of species belonging to MFG and the diagnostic techniques panel do not allow to clarify their real clinical significance. In this study, biomolecular techniques were adopted for species determination of 130 isolates derived from fish initially identified through biochemical tests as NTM belonging to MFG. Specifically, gene sequencing and phylogenetic analysis were used based on a fragment of the gene encoding the 65 KDa heat shock protein (hsp65). The analyzes made it possible to confirm that all the isolates belong to MFG, allowing to identify the strains at species level. Phylogenetic analysis substantially confirmed what was obtained by gene sequencing, except for six strains; this is probably due to the sequences present in NCBI database. Although the methodology used cannot represent a univocal identification system, this study has allowed us to evaluate its effectiveness as regards the species of MFG. Future studies will be necessary to apply these methods with other gene fragments and to clarify the real pathogenic significance of the individual species of this group of microorganisms. Full article
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Review

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25 pages, 2333 KiB  
Review
Nontuberculous Mycobacteria as Sapronoses: A Review
by Ivo Pavlik, Vit Ulmann, Dana Hubelova and Ross Tim Weston
Microorganisms 2022, 10(7), 1345; https://doi.org/10.3390/microorganisms10071345 - 3 Jul 2022
Cited by 24 | Viewed by 4113
Abstract
Mycobacteria are a unique group of microorganisms. They are characterised by exceptional adaptability and durability. They are capable of colonisation and survival even in very unfavourable conditions. In addition to the well-known obligate human pathogens, Mycobacterium tuberculosis and M. leprae, more than [...] Read more.
Mycobacteria are a unique group of microorganisms. They are characterised by exceptional adaptability and durability. They are capable of colonisation and survival even in very unfavourable conditions. In addition to the well-known obligate human pathogens, Mycobacterium tuberculosis and M. leprae, more than 200 other species have been described. Most of them form a natural part of the microflora of the external environment and thrive in aquatic and soil environments especially. For many of the mycobacterial species associated with human disease, their natural source has not yet been identified. From an ecological point of view, mycobacteria are saprophytes, and their application in human and animal diseases is opportunistic. Most cases of human disease from saprophytic mycobacteria occur in immunocompromised individuals. This adaptability and resilience to environmental pressures makes treatment of mycobacterial diseases (most often sapronoses and less often zoonoses) and permanent eradication of mycobacteria from the environment very difficult. Saprophytic mycobacterial diseases (sapronoses) are chronic and recurrent due to the fact of repeated endogenous or exogenous re-exposure. Therefore, knowledge regarding their occurrence in soil and dust would aid in the prevention of saprophytic mycobacterioses. In conjunction, their presence and ecological significance in the environment can be revealed. Full article
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10 pages, 271 KiB  
Review
Ecology of Nontuberculous Mycobacteria
by Joseph O. Falkinham III
Microorganisms 2021, 9(11), 2262; https://doi.org/10.3390/microorganisms9112262 - 30 Oct 2021
Cited by 44 | Viewed by 3537
Abstract
Nontuberculous mycobacteria (NTM) are opportunistic human pathogens that are widespread in the human environment. In fact, NTM surround humans. The basis for their widespread presence in soils and natural and human-engineered waters lies primarily in their disinfectant resistance, biofilm formation, and adaptability to [...] Read more.
Nontuberculous mycobacteria (NTM) are opportunistic human pathogens that are widespread in the human environment. In fact, NTM surround humans. The basis for their widespread presence in soils and natural and human-engineered waters lies primarily in their disinfectant resistance, biofilm formation, and adaptability to fluctuating environmental conditions. As NTM in drinking water surround humans, a major route of infection is through aerosols. The characteristics of NTM, including resistance to disinfection, adherence to surfaces and biofilm formation, present challenges to contemporary water treatment processes developed for control of Escherichia coli and fecal coliforms. Full article

Other

3 pages, 200 KiB  
Reply
Reply to Pavlik et al. Clinical Relevance and Environmental Prevalence of Mycobacterium fortuitum Group Members. Comment on “Mugetti et al. Gene Sequencing and Phylogenetic Analysis: Powerful Tools for an Improved Diagnosis of Fish Mycobacteriosis Caused by Mycobacterium fortuitum Group Members. Microorganisms 2021, 9, 797”
by Davide Mugetti, Mattia Tomasoni, Paolo Pastorino, Giuseppe Esposito, Vasco Menconi, Alessandro Dondo and Marino Prearo
Microorganisms 2022, 10(1), 55; https://doi.org/10.3390/microorganisms10010055 - 28 Dec 2021
Cited by 1 | Viewed by 1312
Abstract
We appreciate the valuable comment of Pavlik et al. [...] Full article
7 pages, 529 KiB  
Comment
Clinical Relevance and Environmental Prevalence of Mycobacterium fortuitum Group Members. Comment on Mugetti et al. Gene Sequencing and Phylogenetic Analysis: Powerful Tools for an Improved Diagnosis of Fish Mycobacteriosis Caused by Mycobacterium fortuitum Group Members. Microorganisms 2021, 9, 797
by Ivo Pavlik, Vit Ulmann and Ross Tim Weston
Microorganisms 2021, 9(11), 2345; https://doi.org/10.3390/microorganisms9112345 - 12 Nov 2021
Cited by 11 | Viewed by 2760
Abstract
Mycobacterium fortuitum group (MFG) members are able to cause clinical mycobacteriosis in fish and other animals including humans. M. alvei, M. arceuilense, M. brisbanense, M. conceptionense, M. fortuitum, M. peregrinum, M. porcinum, M. senegalense, M. septicum [...] Read more.
Mycobacterium fortuitum group (MFG) members are able to cause clinical mycobacteriosis in fish and other animals including humans. M. alvei, M. arceuilense, M. brisbanense, M. conceptionense, M. fortuitum, M. peregrinum, M. porcinum, M. senegalense, M. septicum, and M. setense were isolated from fish with mycobacteriosis. In other animals only three MFG species have been isolated: M. arceuilense from camels’ milk, M. farcinogenes from cutaneous infections often described as “farcy”, and M. fortuitum from different domestic and wild mammals’ species. Out of 17, only 3 MFG species (M. arceuilense, M. lutetiense and M. montmartrense) have never been reported in humans. A total of eight MFG members (M. alvei, M. brisbanense, M. conceptionense, M. fortuitum subsp. acetamidolyticum, M. houstonense, M. peregrinum, M. porcinum, and M. septicum) have been isolated from both pulmonary and extrathoracic locations. In extrathoracic tissues five MFG species (M. boenickei, M. farcinogenes, M. neworleansense, M. senegalense, and M. setense) have been diagnosed and only one MFG member (M. fortuitum subsp. acetamidolyticum) has been isolated from pulmonary infection. Full article
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