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 Table of Contents  
ORIGINAL ARTICLE
Year : 2022  |  Volume : 11  |  Issue : 4  |  Page : 423-428

Novel and rare species of nontuberculous mycobacteria by Hsp-65 gene sequencing


1 Department of Microbiology, Nizams Institute of Medical Sciences, Panjagutta, Hyderabad, India
2 Department of Pulmonary Medicine, Nizams Institute of Medical Sciences, Panjagutta, Hyderabad, India

Date of Submission01-Aug-2022
Date of Decision20-Sep-2022
Date of Acceptance22-Oct-2022
Date of Web Publication10-Dec-2022

Correspondence Address:
Neelima Angaali
Raja Residency, Flat - 201, Street No. 7, Himayat Nagar - 500 029, Hyderabad
India
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Source of Support: None, Conflict of Interest: None


DOI: 10.4103/ijmy.ijmy_175_22

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  Abstract 


Background: Nontuberculosis mycobacterium (NTM) is the emerging group of organisms being recognized as etiological agents for diverse clinical conditions such as lymphadenitis, cutaneous, and pulmonary or disseminated lesions. Diverse background patients can acquire these infections such as immunocompetent, immunocompromised patients, or postoperative settings. Rapid addition of newer strains to this group necessitates heightened suspicion in the clinical settings. Specific requirements for cultures, biochemical testing, and molecular methods are needed to diagnose these organisms. Methods: The prospective study conducted at Nizam's Institute of Medical Sciences from January 2019 to December 2021 using various clinical samples using molecular techniques such as line probe assay and hsp-65 gene sequencing to discover new NTM species. The management is challenging since it requires prolonged treatment, multiple drugs, drug resistance, and individualization of treatment in the combination of surgery if needed. In this article, we describe three different NTM species which were not reported in India and highlight to consider these organisms in adequate clinical situation. Results: Mycobacterium iranicum is a rare strain with quick growth and scotochromogenic colonies that are orange-colored. Eight distinct strains were discovered in clinical samples from six different countries: Two each from Iran, Italy, Greece, the Netherlands, Sweden, and the United States. Two of the strains were recovered from cerebrospinal fluid, which is unusual. Mycobacterium species AW6 is an unidentified and unclassified Mycobacterium according to NCBI taxonomy. Mycobacteria malmoense has been linked to lymphadenitis, notably cervical adenitis in children, and pulmonary infection in the majority of cases. Using Line Probe Assay and hsp-65 gene sequencing, novel and uncommon species of NTM were detected from a clinical samples, including sputum and tissue. Conclusion: We report three unusual species of NTMs: M. iranicum, M. species-AW6, and M. malmoense for the first time in India. Novel and rare emerging species of NTMs need to be considered in diverse clinical situations for appropriate therapy and good clinical outcomes.

Keywords: Mycobacterium iranicum, Mycobacterium malmoense, Mycobacterium species-AW6


How to cite this article:
Kadasu R, Teja VD, Angaali N, Rao Patil MA, Paramjyothi G K, Bhaskar K. Novel and rare species of nontuberculous mycobacteria by Hsp-65 gene sequencing. Int J Mycobacteriol 2022;11:423-8

How to cite this URL:
Kadasu R, Teja VD, Angaali N, Rao Patil MA, Paramjyothi G K, Bhaskar K. Novel and rare species of nontuberculous mycobacteria by Hsp-65 gene sequencing. Int J Mycobacteriol [serial online] 2022 [cited 2023 Feb 5];11:423-8. Available from: https://www.ijmyco.org/text.asp?2022/11/4/423/363164




  Introduction Top


The genus mycobacterium includes well-known human pathogens such as Mycobacterium tuberculosis, Mycobacterium leprae, and a wide range of Nontuberculosis mycobacterium (NTM).[1] Around 200 species and 13 subspecies are included in the taxonomy of the genus Mycobacterium.[2],[3],[4] Mycobacterium iranicum is a novel NTM species that has been isolated in the Americas, Asia, and Europe. M. iranicum was first reported from Iran hence it is name. It has been isolated from various sites, including sputum, cerebrospinal fluid, and wound with very few case reports that have been published internationally. M. iranicum was identified as a new species based on 16S rRNA gene sequencing that showed the characteristic signature of rapidly growing mycobacteria but also showed uniqueness in its pattern of four-nucleotide deletions and rpoB gene sequences. It resembles Mycobacterium gilvum the most, although it also resembles Mycobacterium farcinogenes, Mycobacterium senegalense, Mycobacterium fortuitum, and Mycobacterium houstonense.[5] M. iranicum produces a yellow-orange pigment on LJ medium.[6] M. iranicum can be identified by sequencing the 65-kDa heat shock protein gene (hsp-65) and 16S rRNA gene sequencing.[7]

According to NCBI BLAST, Mycobacterium species AW6 is an unclassified mycobacterial species. It is a high G+C Gram-positive bacterium with the genetic code: Table of translations 11 (Bacterial, Archaeal and Plant Plastid). Cellular creatures, Bacteria of the Terrabacteria group, Actinobacteria, Actinomycetia, Corynebacteriales, Mycobacteriaceae, Mycobacterium, and Unclassified Mycobacterium make up the whole list of lineages.

Mycobacterium malmoense identified in patients with lung infection in Malmo, Sweden, where the organism gets its name. However, multiple reports, the most from the United States, have identified M. malmoense as a causal infection in North America.[8],[9] The majority of published case reports have their origins in Northern Europe and the United Kingdom. M. malmoense typically causes lung infection, just like other NTM species. In addition, lymphadenitis has been linked to it, particularly cervical adenitis in children, as seen in Nova Scotia,[10] skin and soft-tissue infections, in rare case causes disseminated disease.[11],[12] The majority of patients with concurrent structural lung diseases, such as chronic obstructive pulmonary disease, bronchiectasis, cystic fibrosis, prior tuberculosis, and occupational exposure (such as pneumoconiosis), develop pulmonary infections caused by NTM.[11] M. malmoense related pulmonary infection frequently manifests as a variety of nonspecific symptoms, such as coughing, dyspnea, hemoptysis, sputum production, malaise, and weight loss.[11] Patients must satisfy one or more microbiologic criteria in addition to the clinical criteria in order to be diagnosed. Since several common anti-tuberculosis drugs, like isoniazid, are ineffective against M. malmoense, confirmatory culture to identify the specific pathogen is advised to guarantee that the right treatment is administered.[11],[13],[14]


  Methods Top


Sample collection

All the samples collected were clinically suspected and met the criteria of AST/IDSA.

Sample 1 (sputum)

Patient presented with severe productive cough, weight loss, and a low grade fever and had a past history of TB. Her chest imaging showed right lung volume loss, homogenous opacities in the upper and lower zones, two cavitary lesions with associated fibrosis in the mid and lower zones, and thickening of the bronchial wall with patchy consolidation and nodular opacities in the upper zone.

Sample 2 (sputum)

DM, HTN, and CVA presented with a fever, cough with mucopurulent sputum, mMRC grade 2 breathlessness and loss of appetite of 45 days duration.

Sample 3 (sputum)

Pus sample taken from pustular lesions of hand in a postrenal transplant patient.

DNA isolation

Emulsify a loopful of culture growth in 1,000 ml of sterile, deionized water in a screw-cap tube, spin the mixture for 10 min at 17,000 × g (13,000 rpm), and then carefully discard the supernatant. Resuspend the pellet by pipetting up and down while adding 180 μl of the lysozyme mixture (20 mg/ml lysozyme; 20 mM Tris-HCl [pH 8.0]; 2 mM EDTA; 1.2 percent Triton®). In a thermal block, incubate for at least 1 h at 37°C, centrifuge briefly to remove drops from the inside of the lid. 200 mL of AL buffer and 20 mL of Proteinase K should be added and incubated for 30 min at 56°C. Short centrifuge to get the drips out of the interior of the lid. Incubated 15 min at 95°C (incubation time should not be exceeded as this may cause DNA degradation). The sample should be cooled to the room temperature. Short centrifuge to get the drips out of the interior of the lid. 200 μl of 96%–100% ethanol should be added to the sample, and it should be vortexed again for 15 s. After combining, quickly centrifuge the 1.5 ml mini centrifuge tube to get rid of any drips that may have gotten inside the lid. Apply the mixture from step 6 (in a 2 ml collection tube) carefully to the QIAamp Mini spin column without soaking the rim. Centrifuge for 1 min at 6000 × g (8000 rpm) with the cap on. In a clean 2 ml collection tube (supplied), place the QIAamp Mini spin column. Discard the filtrate-containing tube. Open the QIAamp Mini spin column carefully, and without soaking the rim, add 500 l of Buffer AW1. Centrifuge for 1 min at 6000 × g (8000 rpm) with the cap on. In a clean 2 ml collection tube (supplied), place the QIAamp Mini spin column. Discard the collection tube containing the filtrate. Open the QIAamp Mini spin column carefully, and without soaking the rim, add 500 l of Buffer AW2. Centrifuge for 3 min at high speed (20,000 × g; 14,000 rpm) after sealing the cap. Recommended: A fresh 2 ml collection tube (not included) should be used to hold the QIAamp Mini spin column and the old one should be discarded together with the filtrate. 1 min of full-speed centrifuging this action aids in removing the potential for Buffer AW2 carryover. In a clean 1.5 ml microcentrifuge tube (not included), place the QIAamp Mini spin column. Discard the collection tube containing the filtrate. Open the QIAamp Mini spin column with caution and pour 200 μl of Buffer AE or distilled water into it. After 1 min of incubation at ambient temperature (15°C–25°C), centrifuge for 1 min at 6000 × g (8000 rpm). The quality of the extracted DNA will be examined using a NANO-DROP spectrophotometer.

Line probe assay

DNA extraction form LJ culture growth was done using GenoLyse kit for extraction of bacterial DNA (Hain-Life Sciences). Amplification of extracted DNA was done by Amplification mixes (AM-A and Am-B) AM-A 10 μl and AM-B 30 μl, respectively, with 5 μl extracted DNA using GenoType Mycobacterium CM VER 2.0 (Hain-Life Sciences). Amplification profile for thermal cycler was followed 95°C for 15 min – 1 cycle (initial denaturation), 95°C for 30 s – and 65°C for 2 min – 10 cycle (denaturation and annealing/extension), 95°C for 25 s, 50°C for 40 s and 70°C for 40 s (denaturation, annealing, and extension) 70°C for 8 min – 1 cycle (Final extension).

Hybridization of amplified product 20 μl was dispensed in 20 μl of denaturation solution (DEN, blue) in a corner of the wells used, pipette up and down to mix well and incubate at the room temperature for 5 min. Carefully added to well 1 ml of prewarmed at (37°C–45°C) Hybridization Buffer (HYB, green). Gently shake the tray until the solution has a homogenous color. Placed a strip in well. Placed tray in shaking water bath/TwinCubator and incubate for 30 min at 45°C. Completely aspirated hybridization buffer. Added 1 ml of Stringent Wash Solution (STR, red) to strip and incubated for 15 min at 45°C in shaking water bath/TwinCubator. Completely removed stringent wash solution. Wash each strip once with 1 ml of Rinse Solution (RIN) for 1 min on shaking platform/TwinCubator (pour out RIN after incubation). Added 1 ml of diluted Conjugate 1:100 (CON-C with CON-D) to each strip and incubate for 30 min on shaking platform/TwinCubator. Remove solution and wash each strip twice for 1 min with 1 ml of Rinse Solution (RIN) and once for 1 min with approx. 1 ml of distilled water (e.g. use wash bottle) on shaking platform/TwinCubator (pour out solution each time). Added 1 ml of diluted substrate 1:100 (SUB-C with SUB-D) to each strip and incubate protected from light without shaking. Stop reaction as soon as bands are clearly visible by briefly rinsing twice with distilled water. Using tweezers, remove strips from the tray and dry them between two layers of absorbent paper.

Interpretation of test results was evaluated by using interpretation chat provided in GenoType Mycobacterium CM VER 2.0 kit Hain Life Sciences.

hsp-65 gene sequencing

According to van Soolingen et al. instructions.[15] DNA from NTM isolates was extracted. In order to lyse the cells, a loop-full of NTM growth was suspended in 500 μl of 1X TE buffer (10 mM Tris-HC1, 1 mM EDTA, pH 8.0). The cells were then heated at 90°C for 30 min. Proteinase K (at a concentration of 10 mg/ml) and 70 μl of 10% sodium dodecyl sulphate (W/V) were added to the mixture and it was incubated for 10 min at 65°C before the DNA was extracted using the phenol-chloroform technique. Prior to the next stages, the extracted DNA samples were kept in a −20°C freezer. The NTM species was determined using polymerase chain reaction (PCR) amplification and heat shock protein-65 gene sequencing. Tb-11 F-ACCAACGATGGTGTCTCCAT and Tb-12 R-CTTGTCGAACCGCATACCCT, each measuring 439 base pairs, were utilised as the hsp-65 gene primer sets.[16] 10 mM Tris-HCl (pH 8.3), 50 mM KCl, 2 mM MgCl2, 0.2 mM dNTP mix, 0.1 U μl_ 1 Taq polymerase, 0.5 M of each primer, DNA template, and nuclease-free water were used in the PCR procedures. PCR cycle conditions for amplification of the genes hsp-65 were as follows: 94°C for 5 min followed by 40 cycles of 94°C for 30 s, 60°C for 30 s, and 72°C for 30 s, and then final extension at 72°C for 10 min. 3 μl of the PCR results (amplicon) were subjected to electrophoresis on 1.5% gel agarose for analysis. GelRedTM DNA stains were used to stain the gel, and the gel documentation system used UV light to see the fragments (Gel Doc, ATP Co). Sanger sequencing (3130 xl-3730 xl genetic analyzer, applied biosystem 16/48 capillaries of 50 cm leanth) was used to evaluate the PCR products after they had been purified using a QIA quick PCR purification kit (QIAGEN, Germany). The sequencing outcomes of the hsp-65 genes were examined using DNASTAR Lasergene Software (version 7.1). Using the online NCBI BLAST software (http://hsp65blast.phsa.ca/blast/blast.html) of the National Center for Biotechnology Information, the sequences were compared with related sequences of the species in Gene Bank.


  Results Top


Mycobacterium iranicum

A 22-year-old woman presented with severe productive cough, weight loss, and a low grade fever of 3 months duration. She had a history of usage of antituberculous therapy elsewhere for 6 months with persistent sputum positivity. Her chest imaging showed right lung volume loss, homogenous opacities in the upper and lower zones, two cavitary lesions with associated fibrosis in the mid and lower zones, and thickening of the bronchial wall with patchy consolidation and nodular opacities in the upper zone. Investigations showed sputum smear for AFB is positive [Figure 1], GeneXpert for MTB is negative, mycobacterium culture exhibits rapid growth with significant yellow-orange pigmented colonies [Figure 2], MPT-64 antigen test is negative and growth on blood agar is positive from culture growth, and gene sequencing by hsp-65 gene reveals NTM species M. iranicum.
Figure 1: AFB smear positive by Auramine Rhodamine staining

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Figure 2: Mycobacterium iranicum growth on LJ medium

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Mycobacterium species-AW6

A 60-year-old man with DM, HTN, and CVA presented with a fever, cough with mucopurulent sputum, mMRC grade 2 breathlessness and loss of appetite of 45 days' duration. He received antibiotics without clinical response and presented to our institution. His sputum grew Mycobacterium culture shows growth after 3 weeks of incubation [Figure 3], secondary smear from culture growth shows acid fast bacilli in ZN smear, MPT-64 antigen test is negative and growth on blood agar is positive from culture growth, and on gene sequencing by hsp-65 gene shows NTM species M. species-AW6 strain.
Figure 3: Mycobacterium species AW-6 growth on LJ medium

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Mycobacterium malmoense

A 37-year-old male, who underwent DDRT in 2021 for chronic kidney disease due to chronic interstitial nephritis. He received basiliximab, methyl prednisolone, tacrolimus, and MMF in the posttransplant period. For in the transaminitis after 6 months, he was evaluated and found to be HCV reactivation. He was started on Sofosbuvir and velpatasvir. After 1 month, he started having arthralgias, popular lesions over the right hand fingers and neck swelling [Figure 4]. FNAC of the lymph node was AFB positive, genexpert negative, culture showed growth of MTB after 1 week, using Line Probe Assay results reveled NTM species the M. malmoense, MPT-64 antigen test is negative and growth on blood agar is positive from culture growth [Figure 5]. He was started on rifampicin, clarithromycin, levofloxacin, and ethambutol with good clinical response.
Figure 4: Cervical lymphadenopathy and multiple small and large joint swellings

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Figure 5: Mycobacterium malmoense growth on LJ medium

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  Discussion Top


M. iranicum is a Gram-positive, nonmotile, nonspore-forming, acid-alcohol-fast bacillus produce smooth, yellow-orange, and scotochromogenic colonies 1–4 mm in diameter in 4 days when grown at 37°C (25 and 40°C) on solid media. No growth is observed on MacConkey agar without crystal violet 5% (w/v) NaCl. The species is positive for urease, iron uptake, tellurite reduction, arylsulfatase, and heat-stable catalase, while negative for niacin production, nitrate reduction, Tween 80 hydrolysis, and semiquantitative catalase. According to a genotypic perspective, the hsp65's PRA patterns are distinct, and the divergence from every other mycobacterium is extremely high in each of the four genetic areas examined.[5]

According to phylogenomic and hsp65, rpoB, or 16S rRNA gene focused M. iranicum is closely related to environmental and rarely pathogenic mycobacterial species.[17] In addition, M. iranicum was later separated from the vicinity of human habitation.[18] M. iranicum has been identified as a human pathogen in both immunocompromised and previously healthy patients.[19] In a comparative genome analysis, M. iranicum was found to have a close genetic association with other environmental mycobacteria.[17] Based on phylogenetic analysis, M. iranicum may be closely related to another rapid grower M. gilvum.[16] It may have acquired virulence genes through horizontal transfer with other mycobacteria, Gram-positive bacteria (Rhodococcus, Corynebacterium, and Nocardia), and Gram-negative bacteria (Achromobacter).[17] It is a recently identified species, with the earliest recorded case reports occurring in 2005.[5] M. iranicum was isolated in both immunocompetent and immunocompromising patients, such as cancer, diabetes mellitus, Crohn's disease, and HIV infection.[5],[6],[7]

In earlier cases, M. iranicum was not necessarily considered clinically relevant. For instance, isolates from the sputum of an 89-year-old Dutch woman and the cerebral fluid of a 57-year-old Greek woman were declared clinically unimportant.[5] Despite coming from sputum, six isolates did not match the American Thoracic Society's standards for clinical relevance.[6] However, M. iranicum was implicated as a real pathogen in a Japanese patient who developed peritonitis after rinsing the exit site of his peritoneal dialysis catheter with tap water that may have been contaminated with soil after he had finished growing flowers.[16] M. iranicum was also isolated three times from a hand wound of a renal transplant recipient, who was subsequently treated with amikacin.[5]

Extra-pulmonary NTM disease is typically treated with at least two antibiotics to which the organism is susceptible.[11],[16],[20] M. iranicum is often susceptible to amikacin, cefoxitin, clarithromycin, ethambutol, imipenem, minocycline, sulfamethoxazole, and linezolid based on minimum inhibitory concentrations of five clinical strains. However, it may be intermediately susceptible to ciprofloxacin, rifampicin, and streptomycin.[5]

Mycobacterium species AW6 is an unclassified mycobacterial species. This species was not found to be identified elsewhere till date.

In 1979, 11 cases of M. malmoense were reported in England and Wales, 2 of which involved cervical adenitis in young female patients, and 9 of which were lung diseases. 61 different M. malmoense strains have so far been discovered.[21] The first M. malmoense case to be documented in the country was in 1984. The organism was identified from the sputum and bronchoalveolar lavage of this 43-year-old Virginian.[9]

M. malmoense-related lung infections that were recorded in Scotland between 1982 and 1984 were examined in 1987 by France et al. They found 20 cases, the majority of which were associated to chronic lung diseases such as COPD with an incidence that was twice as high in males as it was in women.[22] By 1993, there were more than 180 recorded instances of M. malmoense in the world, of which only 5 were causative of disseminated infection.[12] 15 papers describing 21 cases of extrapulmonary and disseminated illnesses were reported between 1967 and 1992.[12] Out of the 21 cases, 13 lymphadenitis more frequently cervical, 5 were disseminated infections, and 3 were tenosynovitis.[12]

Henriques et al., in 1994 collected global reports from 1968 to 1989, where 221 patients were identified, of which 171 (79%) had respiratory tract infections, 36 had cervical lymphadenitis, and 14 had other infections.[23] Seventy-three cases of M. malmoense were reported to the CDC in the US between 1993 and 1995; however, Buchholz et al. evaluated that only 6 of the 60 patients reviewed and had illness that met the standards of the American Chest Society. One of these had cervical lymphadenitis and five of them had lung illness.[8] A retrospective research that examined instances in the Netherlands from 2002 to 2006 and identified 51 patients of which 40 (70%) had lung involvement of these cases, 80% met the American Society of Chest criteria.[24]


  Conclusion Top


We report three rare cases of NTM. To the best of our knowledge, these are the first reports in the Indian literature. This highlights the increased suspicion of atypical mycobacterial infection since diagnosis and treatment is challenging and highly individualized.

Limitations of the study

In this study, identification of Mycobacterial species was done using only one gene that is hsp-65, rest of genes like rpo-B, and 16S rRNA were not applied for genotypic identification and phenotypic identification such as biochemical reaction for the identification of mycobacteria were not subjected.

Ethical statement

This study was approved by NIMS Institutional Ethical Committee, Hyderabad, India in its 151st meeting held on 25.10.2018 (Approval No. EC/NIMS/2242/2018). The requirement for written informed consent was waived due to the prospective observational design of the study doesn't require the consent from patients.

Financial support and sponsorship

ICMR we declare the financial support from SRFship program supported by ICMR Fellowship No. Fellowship/TB/46/2020-ECD-I. which was the part of Ph.D SRF fellowship from ICMR.

Conflicts of interest

There are no conflicts of interest.



 
  References Top

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Primm TP, Lucero CA, Falkinham JO 3rd. Health impacts of environmental mycobacteria. Clin Microbiol Rev 2004;17:98-106.  Back to cited text no. 1
    
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Fedrizzi T, Meehan CJ, Grottola A, Giacobazzi E, Fregni Serpini G, Tagliazucchi S, et al. Genomic characterization of Nontuberculous Mycobacteria. Sci Rep 2017;7:45258.  Back to cited text no. 3
    
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Shojaei H, Daley C, Gitti Z, Hashemi A, Heidarieh P, Moore ER, et al. Mycobacterium iranicum sp. nov., a rapidly growing scotochromogenic species isolated from clinical specimens on three different continents. Int J Syst Evol Microbiol 2013;63:1383-9.  Back to cited text no. 5
    
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Balakrishnan N, Tortoli E, Engel SL, Breitschwerdt EB. Isolation of a novel strain of Mycobacterium iranicum from a woman in the United States. J Clin Microbiol 2013;51:705-7.  Back to cited text no. 6
    
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Buchholz UT, McNeil MM, Keyes LE, Good RC. Mycobacterium malmoense infections in the United States, January 1993 through June 1995. Clin Infect Dis 1998;27:551-8.  Back to cited text no. 8
    
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Warren NG, Body BA, Silcox VA, Matthews JH. Pulmonary disease due to Mycobacterium malmoense. J Clin Microbiol 1984;20:245-7.  Back to cited text no. 9
    
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McCrossin C, Mailman T. First Canadian reports of cervical adenitis due to Mycobacterium malmoense and a 10-year review of nontuberculous mycobacterial adenitis. Can J Infect Dis Med Microbiol 2006;17:123-7.  Back to cited text no. 10
    
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Griffith DE, Aksamit T, Brown-Elliott BA, Catanzaro A, Daley C, Gordin F, et al. An official ATS/IDSA statement: Diagnosis, treatment, and prevention of nontuberculous mycobacterial diseases. Am J Respir Crit Care Med 2007;175:367-416.  Back to cited text no. 11
    
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Zaugg M, Salfinger M, Opravil M, Lüthy R. Extrapulmonary and disseminated infections due to Mycobacterium malmoense: Case report and review. Clin Infect Dis 1993;16:540-9.  Back to cited text no. 12
    
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Hoffner SE, Hjelm U, Källenius G. Susceptibility of Mycobacterium malmoense to antibacterial drugs and drug combinations. Antimicrob Agents Chemother 1993;37:1285-8.  Back to cited text no. 13
    
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Lymperopoulou DS, Coil DA, Schichnes D, Lindow SE, Jospin G, Eisen JA, et al. Draft genome sequences of eight bacteria isolated from the indoor environment: Staphylococcus capitis strain H36, S. capitis strain H65, S. cohnii strain H62, S. hominis strain H69, Microbacterium sp. strain H83, Mycobacterium iranicum strain H39, Plantibacter sp. strain H53, and Pseudomonas oryzihabitans strain H72. Stand Genomic Sci 2017;12:17.  Back to cited text no. 18
    
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France AJ, McLeod DT, Calder MA, Seaton A. Mycobacterium malmoense infections in Scotland: An increasing problem. Thorax 1987;42:593-5.  Back to cited text no. 22
    
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Henriques B, Hoffner SE, Petrini B, Juhlin I, Wåhlén P, Källenius G. Infection with Mycobacterium malmoense in Sweden: Report of 221 cases. Clin Infect Dis 1994;18:596-600.  Back to cited text no. 23
    
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    Figures

  [Figure 1], [Figure 2], [Figure 3], [Figure 4], [Figure 5]



 

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