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 Table of Contents  
ORIGINAL ARTICLE
Year : 2021  |  Volume : 10  |  Issue : 3  |  Page : 301-306

Survival of Mycobacterium abscessus complex organisms on coins


Laboratory for Disinfection and Pathogen Elimination Studies, Northern Ireland Public Health Laboratory, Nightingale Hospital, Belfast, Northern Ireland, UK

Date of Submission09-Jul-2021
Date of Acceptance17-Aug-2021
Date of Web Publication03-Sep-2021

Correspondence Address:
John E Moore
Laboratory for Disinfection and Pathogen Elimination Studies, Northern Ireland Public Health Laboratory, Belfast City Hospital, Belfast BT9 7AD
UK
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Source of Support: None, Conflict of Interest: None


DOI: 10.4103/ijmy.ijmy_138_21

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  Abstract 


Background: To date, there have been no reports on the occurrence of nontuberculous mycobacterial (NTM) organisms (nor tuberculosis [TB]) on money, currency, banknotes, or coins, where these may act as fomites in the potential transmission of mycobacterial organisms around communities, especially in developing nations, where physical currency is still the popular mainstay of the economy, compared to electronic and digital forms of currency transaction. It was therefore the aim of this study to examine the survival of the Mycobacterium abscessus complex organisms on coins. Methods: Coins from 17 countries were examined for the presence of M. abscessus complex organisms by broth enrichment in Middlebrook 7H9 for 2 months. Nickel-plated steel and copper-plated steel coins were artificially contaminated individually with M. abscessus complex (circa 107 [7 log10] organisms/coin), including M. abscessus subsp. massiliense (n = 2), M. abscessus subsp. bolletti (n = 2), and M. abscessus subsp. abscessus (n = 1) and their surviving cells enumerated at weekly period up to 5-week postinoculation. Results: NTM organisms were not isolated from coins from the 17 currencies examined. In all three subspecies of M. abscessus, the copper-plated steel coins caused a more rapid decline in organism numbers, which were statistically very significant (P < 0.0001), compared to the paired survival on the nickel-plated steel coins, whereby organisms were none detectable after 3-week storage on the copper-plated coins. NTM organisms survived better on the nickel-plated coins, with a mean count across all subspecies of log10 1.84 colony forming units per coin after 5 weeks of storage (range: 0.6–2.69 log10 cfu/coin). There was no statistically significant difference (P > 0.05; 5%) in the survival dynamics among the three subspecies with storage on either coin type. Conclusions: Health-care professionals should be aware of the survival of M. abscessus complex organisms on coins for up to 12 weeks, which may be particular relevant in high-risk areas of health-care institutions where TB or NTM is prevalent and where there are opportunities for the transmission of such organisms through contaminated fomites, including coins, through opportunities including payment for treatments/medicines/dressings, coin-operated payment facilities, such as hospital car parking, self-service vending machines, hospital canteens, coffee shops and dining halls and hospital shops, whether static or mobile onward visits. To mitigate potential infection consequences of handling coins contaminated with M. abscessus complex organisms, other NTMs organisms and TB, the authors support re-establishing the principles of basic hygiene, including proper handwashing and the avoidance of handling money when working with food or dressing wounds and skin lesions, as well as when working with respiratory devices, including nebulizers.

Keywords: Banknotes, coin, currency, environment, money, Mycobacterium abscessus complex, survival, transmission


How to cite this article:
Moore JE, Millar BC. Survival of Mycobacterium abscessus complex organisms on coins. Int J Mycobacteriol 2021;10:301-6

How to cite this URL:
Moore JE, Millar BC. Survival of Mycobacterium abscessus complex organisms on coins. Int J Mycobacteriol [serial online] 2021 [cited 2021 Dec 8];10:301-6. Available from: https://www.ijmyco.org/text.asp?2021/10/3/301/325500




  Introduction Top


Several recent reports have highlighted the growing clinical concern with the global emergence of nontuberculous mycobacterial (NTM) infections in humans, particularly with Mycobacterium abscessus, in respiratory, skin, and mucosal infections.[1],[2],[3] This emergence has been observed in people with cystic fibrosis (CF) and severely complicates clinical treatment due to its persistence in the CF lung and difficulty in its treatment with antibiotics, due to its highly resistant nature,[4],[5] as well as its resistance to eradication within the clinical environmental with biocides.[6] In response to these threats, novel innovations in discovery of new approaches to tackle such antimicrobial resistance with such NTM organism have been recently reviewed and discussed.[7],[8]

The emergence and clinical mischief that these organisms are now causing can in part be attributed to their environmental origins and the intrinsic biology and strategies that these species have developed to become successful and persistent organisms within the environment. Their spread into the health-care environment and their establishment of chronic infections in susceptible patient populations, including those with CF, has led to an urgency in being able to eradicate them from both the physical environment, as well as from sites of chronic colonization and persistence.

Previously, there have been numerous reports on diverse range of environments and fomites that these organisms are able to colonize and persist on.[9] Previously, money in the form of banknotes and coins has been shown to be a reservoir of bacterial organisms, including predominantly Gram-positive organisms.[10],[11] To date, there have been no reports on the occurrence of NTM organisms (nor tuberculosis [TB]) on money, currency, banknotes, or coins, where these may act as fomites in the potential transmission of mycobacterial organisms around communities, especially in developing nations, where physical currency is still the popular mainstay of the economy, compared to electronic and digital forms of currency transaction. It was therefore the aim of this study to examine the survival of the M. abscessus complex organisms on coins.


  Methods Top


Isolation of Mycobacterium abscessus complex organisms from global currencies

Monetary currency in the form of coins from the following 17 countries was examined for the presence of M. abscessus complex organisms: Austria (50 g), Brazil (6.2 g), Canada (32.1 g), China (2.5 g), Denmark (16.4 g), France (11.6 g), Greece (9.0 g), Hong Kong (50 g), Ireland (50 g), Israel (50 g), Japan (50 g), Norway (50 g), Singapore (18.6 g), Sri Lanka (8.7 g), Thailand (50 g), United Kingdom (50 g; silver), United Kingdom (50 g; copper), and USA (50 g). Coins from each currency were aseptically placed in Middlebrook 7H9 broth (20 ml) (Sigma M0178) with glycerol (2 g/450 ml) and incubated at 30°C for 2 months. Broths were examined at 1-month and after 2-month incubation, by plating 10 μl Middlebrook broth onto Columbia Blood Agar (CBA; Oxoid CM0031, Oxoid Ltd., Basingstoke, UK), supplemented with 5% (v/v) defibrinated horse blood (Oxoid SR0050) and incubated aerobically for 2 weeks at 30°C.

Survival of Mycobacterium abscessus complex organisms on coins

Two types of coins were selected for the survival studies, including UK “Silver (5p)” and “Copper (2p)” coins. These were sourced from UK currency that had been in recent general circulation in the community in Northern Ireland, UK. Coins were initially sterilized by autoclaving at 121°C for 15 min and 15 PSI. 5p coins had the following specifications: diameter (18.0 mm), weight (3.25 g), thickness (1.7 mm), and composition nickel-plated steel. 2p coins had the following composition: diameter (25.9 mm), weight (7.12 g), thickness (2.03 mm), and composition copper-plated steel.

Five strains of M. abscessus complex, including M. abscessus subsp. massiliense (n = 2), M. abscessus subsp. bolletti (n = 2), and M. abscessus subsp. abscessus (n = 1), were employed in this study. All isolates were initially prepared by culturing on CBA supplemented with 5% (v/v) defibrinated horse blood (Oxoid SR0050) and incubated aerobically for 2 weeks at 30°C. Inocula of each strain was prepared by emulsifying colonies of each isolate individually into 0.1% (w/v) peptone saline diluent (Oxoid) (9 ml), followed by inoculation of sterile coins, as prepared above, by adding 100 μl of inoculum of each of the five strains individually to both 5p and 2p coins [Figure 1]. Coins were stored aerobically in sterile  Petri dish More Detailses (Sterilin Ltd., UK) with the lids closed and placed in a Class II biological safety cabin (MicroFlow Ltd., UK) at ambient temperature (Circa. 18°C) for 5 weeks. Quantitative enumeration counts, expressed as log10 colony forming units per coin (log10 cfu/coin), were performed at weekly intervals for 5-week storage of coins. At each sampling time point, the stored coin with dried inoculum was aseptically removed from the plate and placed in Middlebrook 7H9 broth (5 ml) and vortexed vigourously for 1 min, followed by quantitative plating onto Standard Plate Count Agar (Oxoid, CM0463) in duplicate and incubated at 30°C for 1 week.
Figure 1: Inoculum of Mycobacterium abscessus complex organisms on the surface of UK (a) 2p coins and (b) 5p coins

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Statistical analysis was performed employing a two-tailed paired student's t-test, and probability values less than 5% (<0.05) were considered significant.


  Results Top


Following long-term enrichment of coins in Middlebrook 7H9 broth for 2 months, no NTM organisms were isolated from coins from the 17 currencies examined. Middlebrook broth enrichments of the coins grew filamentous fungi, Bacillus spp., and Kocuria rhizophila.

Survival of M. abscessus complex organisms on UK nickel-plated (5p coins) and copper-plated steel (2p coins) coins, which had been artificially spiked with known numbers of organisms, is shown in [Figure 2],[Figure 3],[Figure 4]. [Figure 2] shows the survival of M. abscessus subsp. abscessus, [Figure 3] shows the survival of M. abscessus subsp. Bolletii, and [Figure 4] shows the survival of M. abscessus subsp. massiliense. [Figure 5] shows the survival of the three subspecies combined and expressed as the M. abscessus complex. In all three subspecies of M. abscessus, the copper-plated steel coins caused a more rapid decline in organism numbers, which were statistically very significant (P < 0.0001), compared to the paired survival on the nickel-plated steel coins, whereby organisms were none detectable after 3-week storage on the copper-plated coins. NTM organisms survived better on the nickel-plated coins, with a mean count across all subspecies of log10 1.84 colony forming units per coin after 5 weeks of storage (range: 0.6–2.69 log10 cfu/coin). There was no statistically significant difference (P > 0.05; 5%) in the survival dynamics among the three subspecies with storage on either coin type.
Figure 2: Survival of Mycobacterium abscessus subsp. abscessus on coins

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Figure 3: Survival of Mycobacterium abscessus subsp. bolletii (n = 2) on coins

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Figure 4: Survival of Mycobacterium abscessus subsp. massiliense (n = 2) on coins

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Figure 5: Survival of Mycobacterium abscessus complex organisms on coins

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  Discussion Top


NTM organisms are bacterial experts at adaptation at the environment/anthropogenic interface, where they can be important etiological agents of disease transmission. An example of such a scenario is the environmental contamination and persistence of NTM organisms in hospital ice machines, as previously described.[12] Public health epidemiologists should be aware of other potential similar scenarios that give TB and NTM organisms a unique opportunity to create a public health issue of potential clinical relevance. Previous studies have identified coins as being contaminated with several different bacteria.[10] In a study examining the microflora of coins from 17 countries, Gram-positive organisms were the most frequently isolated, including the genus Bacillus (including B. megaterium, B. lentus, B. litoralis, B. subtilis, B. circulans, and other Bacillus spp.), which accounted for 40% of isolates recovered, as well as Staphylococcus spp. (Staph. aureus, Staph. epidermidis, Staph. hominis, Staph. schleiferi).[10] Additional studies have examined the survival of epidemic strains of nosocomial- and community-acquired methicillin-resistant Staphylococcus aureus and have shown that survival lasted 4-h postinoculation on the coins.[13] Given that NTM organisms have different biology to the Gram-positive bacteria (see below) which could influence their survival on coins, it is therefore important to establish the survival dynamics of NTM organisms on coins to help elucidate this mechanism of potential dissemination within the community.

Neither rapidly growing NTM organisms were isolated from coins from different currencies in this study nor have there been any TB or NTM organisms described in such studies from other countries. In the present study, we also wished to look specifically employing bacteriological culture techniques for NTM organisms from coin currencies from 17 countries. Likewise, we were unable to isolate any NTMs in this study, even when employing mycobacterial-specific microbiological enrichment techniques enabling the detection of small numbers of naturally contaminating NTM bacterial cells. We, therefore, wished to know as to why there were no detectable M. abscessus organisms on the coins? Was this due to the coins truly being negative for these organisms or was this due to the survival dynamics of these organisms on coins? Therefore, we wished to investigate more about the survival/persistence dynamics of NTM organisms when placed on coins.

M. abscessus complex organisms survived for several weeks depending on the compositional metal of the coin. Nickel-plated coins sustained the survival of organisms significantly longer than copper-plated coins (P < 0.0001), irrespective of subspecies of M. abscessus examined, under standardized, controlled, and paired conditions. Mean reduction in culturable counts of M. abscessus complex organisms was approximately 5.67 log10 cfu/nickel-plated steel coin after five weeks and approximately 7.5 log10 cfu/copper-plated steel coin after three weeks. By extrapolating the graph [Figure 5], approximately 12 weeks would be required to reduce mycobacterial counts to nondetectable levels on nickel-plated coins. This is in contrast to the survival dynamics of mycobacterial organisms on copper-plated coins, where counts were reduced to nondetectable levels consistently in only 3 weeks for all NTM subspecies examined. This, therefore, suggests that the metal composition of the coin is important in determining the survival of the NTM organisms on the coins. Of the 30 high TB burden countries, listed by the WHO,[14] eight of these (India [26%], Indonesia [8.5%], China [8.4%], the Philippines [6.0%], Pakistan [5.7%], Nigeria [4.4%], Bangladesh [3.6%], and South Africa [3.6%]), collectively account for two-thirds of the global total of TB disease incidence eight countries, listed by the WHO.[14] Several of the coins currently in circulation in these countries are not minted from copper-based alloys but from a variety of other materials, including aluminum, stainless steel, and nickel-plated steel. There is an association between the reliance of the country's economy in using physical coinage and the burden of TB disease, i.e. those countries which rely significantly using physical money, including metal coinage, and their TB disease. However, this has not proven to be causal. Of the 30 high TB burden countries, listed by the WHO, particularly those countries in central and southern Africa, most of these rely heavily on using monetary coinage for domestic day-to-day purchases within the community. Therefore, further work is required to examine the survival of NTMs and TB organisms on their national coins to estimate the involvement of contaminated coins (if any) in harboring and transmitting mycobacterial organisms.

The presence of copper within the composition of the coin had a negative effect on mycobacterial survival. At this stage, it is not clear if such antimycobacterial activity was due directly to elemental copper or a copper salt present on the surface of the coin. Other work has shown that environmental mycobacteria did not grow as prolifically in copper water pipes in comparison with polyvinyl chloride (PVC) pipes,[15] with a reduction of approximately 3 log cycles. Recently, high-throughput screening has identified several compounds, involving copper ions as inhibitors against Mycobacterium tuberculosis (MTB).[16] Therefore, further and urgent work is now required to exploit potential benefits of copper acting in a antimycobacterial capacity.

There are several biological factors associated with mycobacteria that may aid its persistence on the surface of coins, including (1) cell wall structure and related architecture and (2) slow growth and dormancy, as we have previously described.[17]

Mycobacterium spp. are unique in nature that they have a highly unusual cell wall structure, which differs from conventional Gram-positive and Gram-negative bacteria and represents one of the most complicated architectural structures within the prokaryotes. In addition, this hydrophobic cell wall structure aids their resistance to several antibiotics. Mycobacterial cell walls are dominated by lipids and carbohydrates that provide a permeability barrier against hydrophilic drugs and are crucial for its survival and virulence. The cell wall consists of (1) a cell membrane, (2) periplasm, (3) peptidoglycan layer, (4) arabinogalactan layer, (5) mycobacterial outer membrane consisting of mycolic acids, glycolipids, and free lipids, and (6) a capsule consisting of α-glucans and arabinans, as well as capsular proteins and lipids. The richness of lipids in its cell wall architecture may provide NTM with a mechanism to maintain cell wall fluidity under adverse storage conditions, including dehydration, thereby aiding its survival on coin surfaces.[17]

Characteristic slow growth associated with the NTM organisms allows them to adapt to unfavorable and stressful conditions, thus making them less susceptible to antibiotics and disinfectants. Investment of energy by the NTM organisms away from cell replication/multiplication into long-chain lipid outer membrane synthesis confers environmental survival advantages that allow the persistence of the organism in harsh conditions, which many other Gram-positive and Gram-negative organisms would be unable to tolerate.[18] Dormancy is well described for MTB but not so for the NTMs.[19] The ability of NTM to enter a phase of metabolic dormancy is important to aid their survival, during times of environmental stress, particularly nutrient depletion and starvation. While mycobacterial organisms do not have the ability to be fully protected against such extreme environmental stresses through the production of endospores, they have been shown to have protective mechanisms that they may utilize, including formation of the viable but nonculturable (VBNC) state. The VBNC phase has under suboptimal conditions resulted in a reduced growth rate or maximal cell concentration, where the organism enters the VBNC phase after 3–4-day incubation in stationary phase.[20] It remains unclear if any of the other NTM organisms can utilize this VBNC phase as a means to survive in harsh environmental conditions, such as on coins. Furthermore, NTM organisms are noted for their ability to form biofilm-like structures, on account of their high surface hydrophobicity.[18] Hydrophobic interactions between fatty acid tails of the glycopeptidolipids of NTM and the hydrophobic solid surface enable attachment to surfaces and biofilm formation.[21]

Study limitations

First, the coins in our study were artificially contaminated with NTM isolates, as opposed to being naturally contaminated coins obtained from the real-world environment. Naturally contaminated fomites are superior to artificially contaminated fomites, as the former represents real-world events and related modeling that happens spontaneously. The artificial or “spiked” scenario finds difficulty in absolutely mimicking the diverse range of other microflora present, which constitutes a significant difference with the microbiome/ecosystem of the artificially-contaminated coins being studied, including the presence of skin cells, sebaceous material, respiratory secretions, all of which may influence the coin microbiome, as well as the real-world stresses and challenges presented. Furthermore, these data were acquired from a limited number of isolates (n = 5) from the M. abscessus complex. Given the diversity of microbiology and microbiological characteristics from other species within this diverse genus, including the M. tuberculosis complex, it is not possible to readily extrapolate the survival dynamics from M. abscessus and apply directly to related mycobacterial species. Such studies as this would therefore have to be completed for the species under examination. Finally, the chemical composition of the coins may have an important influence on the survival of organisms. The current study showed that copper-plated coins had a significantly altered and diminished survival profile than coins which were nickel plated. Each country may mint its coinage using different metal/alloy specifications, so again, it would be important to establish such survival dynamics employing specific currencies.


  Conclusions Top


From the data presented by this study, health-care professionals should be aware of the survival of M. abscessus complex organisms on coins for up to 12 weeks. This is a relatively long period of time for opportunities of transmission to other fomites or new human hosts, including vulnerable patients, to occur, as well as the opportunity for coins to be become newly contaminated with different strains or species of Mycobacterium. This may be of particular relevance in high-risk areas of health-care institutions where TB or NTM is prevalent and where there are opportunities for the transmission of such organisms through contaminated fomites, including coins, through opportunities including payment for treatments/medicines/dressings, coin-operated payment facilities, such as hospital-car parking, self-service vending machines, hospital canteens, coffee shops and dining halls and hospital shops, whether static or mobile on ward visits. To mitigate potential infection consequences of handling coins contaminated with M. abscessus complex organisms, other NTMs organisms, and TB, the authors support re-establishing the principles of basic hygiene, including proper handwashing and the avoidance of handling money when working with food or dressing wounds and skin lesions, as well as when working with respiratory devices, including nebulizers. Further work is now required to establish survival dynamics of other species of Mycobacterium on coins, particularly M. tuberculosis complex organisms, as well as the influence of different metals and metal alloys of coin composition on bacterial survival.

Ethical clearance

This article does not contain any studies with human participants or animals performed by any of the authors.

Acknowledgment

The authors wish to acknowledge with thanks support from Mr. Alan Murphy, Media Department, Northern Ireland Public Health Laboratory, Belfast City Hospital, for preparation of the culture media employed in this study and Mr. John McCaughan, Department of Medical Microbiology, the Royal Group of Hospitals, Belfast, Northern Ireland, UK, for identification of NTM organisms through MALDI-TOF analyses.

Financial support and sponsorship

Nil.

Conflicts of interest

There are no conflicts of interest.



 
  References Top

1.
Johansen MD, Herrmann JL, Kremer L. Non-tuberculous mycobacteria and the rise of Mycobacterium abscessus. Nat Rev Microbiol 2020;18:392-407.  Back to cited text no. 1
    
2.
Victoria L, Gupta A, Gómez JL, Robledo J. Mycobacterium abscessus complex: A review of recent developments in an emerging pathogen. Front Cell Infect Microbiol 2021;11:659997.  Back to cited text no. 2
    
3.
Rivero-Lezcano OM, González-Cortés C, Mirsaeidi M. The unexplained increase of nontuberculous mycobacteriosis. Int J Mycobacteriol 2019;8:1-6.  Back to cited text no. 3
[PUBMED]  [Full text]  
4.
Degiacomi G, Sammartino JC, Chiarelli LR, Riabova O, Makarov V, Pasca MR. Mycobacterium abscessus, an emerging and worrisome pathogen among cystic fibrosis patients. Int J Mol Sci 2019;20:5868.  Back to cited text no. 4
    
5.
Gross JE, Martiniano SL, Nick JA. Prevention of transmission of Mycobacterium abscessus among patients with cystic fibrosis. Curr Opin Pulm Med 2019;25:646-53.  Back to cited text no. 5
    
6.
Caskey S, Moore JE, Rendall JC. In vitro activity of seven hospital biocides against Mycobacterium abscessus: Implications for patients with cystic fibrosis. Int J Mycobacteriol 2018;7:45-7.  Back to cited text no. 6
[PUBMED]  [Full text]  
7.
Meir M, Barkan D. Alternative and experimental therapies of Mycobacterium abscessus infections. Int J Mol Sci 2020;21:6793.  Back to cited text no. 7
    
8.
Millar BC, Moore JE. Antimycobacterial strategies to evade antimicrobial resistance in the nontuberculous mycobacteria. Int J Mycobacteriol 2019;8:7-21.  Back to cited text no. 8
[PUBMED]  [Full text]  
9.
Honda JR, Virdi R, Chan ED. Global evironmental nontuberculous mycobacteria and their contemporaneous man-made and natural niches. Front Microbiol 2018;9:2029.  Back to cited text no. 9
    
10.
Xu J, Moore JE, Millar BC. Ribosomal DNA (rDNA) identification of the culturable bacterial flora on monetary coinage from 17 currencies. J Environ Health 2005;67:51-5.  Back to cited text no. 10
    
11.
Ejaz H, Javeed A, Zubair M. Bacterial contamination of Pakistani currency notes from hospital and community sources. Pak J Med Sci 2018;34:1225-30.  Back to cited text no. 11
    
12.
Tolba O, Loughrey A, Goldsmith CE, Millar BC, Rooney PJ, Moore JE. Survival of epidemic strains of nosocomial- and community-acquired methicillin-resistant Staphylococcus aureus on coins. Am J Infect Control 2007;35:342-6.  Back to cited text no. 12
    
13.
World Health Organisation (WHO). Global Tuberculosis Report; 2020. p. 32. Available from: https://www.who.int/teams/global-tuberculosis-programme/tb-reports. [Last accessed on 2021 Jul 08].  Back to cited text no. 13
    
14.
Learbuch KL, Smidt H, van der Wielen PW. Influence of pipe materials on the microbial community in unchlorinated drinking water and biofilm. Water Res 2021;194:116922.  Back to cited text no. 14
    
15.
Dalecki AG, Crawford CL, Wolschendorf F. Copper and antibiotics: Discovery, modes of action, and opportunities for medicinal applications. Adv Microb Physiol 2017;70:193-260.  Back to cited text no. 15
    
16.
Millar BC, Moore JE. Hospital ice, ice machines, and water as sources of nontuberculous mycobacteria: Description of qualitative risk assessment models to determine host-Nontuberculous mycobacteria interplay. Int J Mycobacteriol 2020;9:347-62.  Back to cited text no. 16
[PUBMED]  [Full text]  
17.
Pereira AC, Ramos B, Reis AC, Cunha MV. Non-tuberculous mycobacteria: Molecular and physiological bases of virulence and adaptation to ecological niches. Microorganisms 2020;8:1380.  Back to cited text no. 17
    
18.
Alnimr AM. Dormancy models for Mycobacterium tuberculosis: A minireview. Braz J Microbiol 2015;46:641-7.  Back to cited text no. 18
    
19.
Shleeva M, Mukamolova GV, Young M, Williams HD, Kaprelyants AS. Formation of 'non-culturable' cells of Mycobacterium smegmatis in stationary phase in response to growth under suboptimal conditions and their Rpf-mediated resuscitation. Microbiology 2004;150:1687-150  Back to cited text no. 19
    
21.
Kearns DB. A field guide to bacterial swarming motility. Nat Rev Microbiol 2010;8:634-44.  Back to cited text no. 21
    


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