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 Table of Contents  
ORIGINAL ARTICLE
Year : 2021  |  Volume : 10  |  Issue : 3  |  Page : 293-300

Skin and soft-tissue infections due to rapidly growing mycobacteria: An overview


1 Department of Microbiology, Vallabhbhai Patel Chest Institute, University of Delhi, Delhi, India
2 Department of Microbiology, Maharshi Dayanand University, Rohtak, Haryana, India

Date of Submission12-May-2021
Date of Acceptance10-Jul-2021
Date of Web Publication03-Sep-2021

Correspondence Address:
Mandira Varma-Basil
Department of Microbiology, Vallabhbhai Patel Chest Institute, University of Delhi, Delhi - 110 007
India
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Source of Support: None, Conflict of Interest: None


DOI: 10.4103/ijmy.ijmy_110_21

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  Abstract 


Background: Rapidly growing mycobacteria (RGM) are increasingly being recognized as potential pathogens. RGM, particularly Mycobacterium abscessus, Mycobacterium fortuitum, and Mycobacterium chelonae, have been observed in both pulmonary and extrapulmonary infections including cutaneous, soft-tissue, and wound infections. However, there are limited reports of these potential pathogens from skin and soft-tissue infections. Moreover, the drug susceptibility profile of RGM is largely unknown in several regions of the world. Methods: We analyzed reports on RGM isolated from skin and soft-tissue infections globally for details of RGM species and drug susceptibility profile. We also analyzed the drug susceptibility profile of four RGM isolates, obtained from skin and soft-tissue infections in our laboratory, by broth microdilution method. Results: In the reports reviewed, the most common RGM isolated from skin and soft-tissue infections were M. abscessus (184/475, 38.7%), M. fortuitum (150/475, 31.5%), M. chelonae (72/475, 15%), and M. chelonae–M. abscessus complex (46/475, 9.6%). However, drug susceptibility was tested only in 26/39 (66.6%) reports. In our own laboratory, we obtained three isolates of M. abscessus and one isolate of M. fortuitum from one case of breast abscess and three cases of postsurgical wound infections. Maximum susceptibility of M. abscessus was observed to clarithromycin, amikacin, and linezolid. The M. fortuitum isolate was susceptible to clarithromycin, amikacin, clofazimine, and linezolid. Conclusion: Paucity of information available on RGM isolated from skin and soft-tissue infections highlights the need to be aware of the pathogenic potential and the drug susceptibility profile of these organisms.

Keywords: Drug susceptibility profile, rapidly growing mycobacteria, skin and soft-tissue infections


How to cite this article:
Kumar C, Shrivastava K, Singh A, Chauhan V, Varma-Basil M. Skin and soft-tissue infections due to rapidly growing mycobacteria: An overview. Int J Mycobacteriol 2021;10:293-300

How to cite this URL:
Kumar C, Shrivastava K, Singh A, Chauhan V, Varma-Basil M. Skin and soft-tissue infections due to rapidly growing mycobacteria: An overview. Int J Mycobacteriol [serial online] 2021 [cited 2021 Dec 3];10:293-300. Available from: https://www.ijmyco.org/text.asp?2021/10/3/293/325487




  Introduction Top


Comprising nearly one-half of the currently validated mycobacterial species, rapidly growing mycobacteria (RGM) are the Runyon Group IV organisms that usually form colonies within 7 days of incubation. RGM are divided into six major groups including Mycobacterium fortuitum group, Mycobacterium chelonae/Mycobacterium abscessus complex, Mycobacterium smegmatis group, Mycobacterium mucogenicum group, Mycobacterium mageritense/Mycobacterium wolinskyi, and the pigmented RGM. Of all the RGM, M. fortuitum, M. chelonae, and M. abscessus are the most common clinically relevant species.[1]

RGM are being increasingly seen to cause a wide spectrum of infections including pulmonary infections, skin and soft-tissue infections, bloodstream infections, osteomyelitis, and lymphadenitis.[2],[3],[4],[5] These organisms are commonly found in abscesses formed after a puncture wound or a traumatic injury. Nosocomial infections occurring after surgeries or due to invasive therapeutic interventions such as long-term intravenous catheters can also be infected by RGM, particularly M. fortuitum, M. abscessus, or M. chelonae.

Moreover, RGM have extensive resistance to antimicrobial agents, underscoring the importance of not only ascertaining the extent of occurrence of infections due to RGM but also their drug susceptibility profile for adequate management. Here, we report the RGM isolated from skin and soft-tissue infections in Delhi. We also attempt to determine the cases reported on skin and soft-tissue infections caused by RGM globally, and the drug susceptibility profile of the isolates.


  Methods Top


Literature search and data abstraction

A review of the reports available globally on RGM isolated from skin and soft-tissue infections was conducted in accordance with PRISMA guidelines.[6] We searched PubMed, Scopus, EMBASE, and Copernicus for publications on RGM involved in skin and soft-tissue infections from January 2005 to December 2020 using the search terms rapidly growing mycobacteria and skin and soft-tissue infections.

Titles and abstracts of all the articles obtained in the database search were screened and full-text copies of those found to be relevant to our search obtained. For all relevant articles, we extracted the following data using a data extraction sheet: research setting, study period, population tested, RGM species isolated, and drug susceptibility tests performed. At least two authors reviewed each article.

Reporting the rapidly growing mycobacteria associated with skin and soft-tissue infections in Delhi, India

Clinical specimens and mycobacterial isolates

A total of four RGM isolates obtained from skin and soft-tissue infections were retrospectively analyzed. The isolates had been obtained in the Department of Microbiology, Vallabhbhai Patel Chest Institute, Delhi, India, during the period December 2013 to January 2015 after approval from the Institutional Ethical Committee. The samples from which the isolates were obtained were pus from breast abscess (n = 1) and postsurgical wounds (n = 3). The clinical isolates were characterized by their colony morphology on Lowenstein–Jensen medium and were subjected to duplex polymerase chain reaction targeting the genes hsp65 and Rv1458c to differentiate between M. tuberculosis and nontuberculous mycobacteria (NTM).[7] Species identification of the isolates was performed by GenoType Mycobacterium CM/AS (Hain Lifescience GmbH, Germany).[8]

Minimum inhibitory concentration

Minimum inhibitory concentrations (MICs) of the RGM were performed by broth microdilution method[9] in U-bottomed microtiter plates (Falcon, New York) using various concentrations of drugs as described previously.[10] The strains of RGM were characterized as susceptible, intermediate susceptible, and resistant as previously described.[11]


  Results Top


Literature search

We reviewed the available literature globally, between January 2005 and December 2020, on skin and soft-tissue infections wherein RGM had been isolated. We obtained 132 articles from the databases searched using the search terms rapidly growing mycobacteria and skin and soft-tissue infections. After excluding reviews and editorials, we identified 39 reports[12],[13],[14],[15],[16],[17],[18],[19],[20],[21],[22],[23],[24],[25],[26],[27],[28],[29],[30],[31],[32],[33],[34],[35],[36],[37],[38],[39],[40],[41],[42],[43],[44],[45],[46],[47],[48],[49],[50] [Table 1]. The maximum number of reports was from the USA (8/39, 20.5%), followed by Taiwan and India (5/39, 12.8%). There were three reports each (3/39, 7.7%) from Switzerland and Korea and two each (2/39, 5.1%) from Australia, Germany, France, and Venezuela. Canada, Mexico, China, Pakistan, Vietnam, Singapore, and Spain had one study (1/39, 2.5%) each. Molecular methods of identification were used in 29/39 (74.3%) studies. The most common RGM species identified was M. abscessus (184/475, 38.7%), followed by M. fortuitum (150/475, 31.5%), M. chelonae (72/475, 15%), and M. chelonae–M. abscessus complex (46/475, 9.6%) [Figure 1]a. Mycobacterium massiliense (7/475, 1.5%) was identified in three countries, namely Korea, the USA, and Switzerland [Figure 1]b. Mycobacterium conceptionense and M. mucogenicum were found in smaller numbers (2/475, 0.42%). These were followed by one isolate each of Mycobacterium arupense, Mycobacterium brisbanense, Mycobacterium flavescens, Mycobacterium sp. JAN1, M. wolinskyi, Mycobacterium chubuense, and Mycobacterium peregrinum (1/475, 0.2%) [Figure 1]b.
Figure 1: (a) The most common species of rapidly growing mycobacteria, namely Mycobacterium fortuitum, Mycobacterium abscessus, Mycobacterium chelonae, and Mycobacterium chelonaeabscessus complex, identified in skin and soft-tissue infections in the studies reviewed. The graph depicts the distribution of rapidly growing mycobacteria in various countries. (b) The distribution of Mycobacterium massiliense, Mycobacterium conceptionense, Mycobacterium mucogenicum, Mycobacterium arupense, Mycobacterium brisbanense, Mycobacterium flavescens, Mycobacterium JAN1, Mycobacterium wolinskyi, Mycobacterium chubuense, and Mycobacterium peregrinum in various countries

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Table 1: Description of the reports included in the study

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Of the 39 reports we had obtained, 26/39 (66.6%) performed drug susceptibility testing of the isolates [Table 1] using either broth microdilution method (10/26, 38.4%), disc diffusion assay (4/26, 15.3%), or E-test (1/26, 3.8%). The remaining studies (11/26, 42.3%) did not specify the method used for drug susceptibility testing [Table 1]. Of the 26 studies, detailed data were not given in 14; hence, the data were analyzed for the remaining 12 studies [Table 2]. Thus, considering these 12 studies, drug susceptibility profile was evaluated for 90 isolates of M. abscessus, 82 isolates of M. fortuitum, 20 isolates of M. chelonae, and 1 isolate each of M. chelonae–abscessus, M. massiliense, M. wolinskyi, and M. conceptionense [Table 2]. The various studies reported drug susceptibility profile to different antibiotics, hence the drug susceptibility tests were not uniform throughout the panel of RGM reviewed [Table 2]. Although variable susceptibility was observed for all the antimicrobial agents tested, maximum sensitivity of M. abscessus was seen to clofazimine (63/63, 100%), tigecycline (63/63, 100%), clarithromycin (88/90, 97.7%), amikacin (86/90, 95.5%), and linezolid (61/76, 80%). M. fortuitum was maximally susceptible to tigecycline (67/67, 100%), moxifloxacin (71/71, 100%), ofloxacin (3/3, 100%), amikacin (81/82, 98.7%), levofloxacin (64/67, 95.5%), linezolid (68/72, 94.4%), ciprofloxacin (74/81, 91.3%), and imipenem (72/81, 88%), while M. chelonae showed maximum susceptibility to clofazimine (13/13, 100%), tigecycline (13/13, 100%), and tobramycin (12/13, 92.3%) [Table 2].
Table 2: Drug susceptibility pattern for various drugs in the reviewed reports

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Although drug susceptibility profile was reported in three studies from India,[20],[21],[24] one study[20] did not elaborate on the drug susceptibility pattern of individual species and hence was not included in the final analysis.

Rapidly growing mycobacteria isolated from skin and soft-tissue infections in Delhi, India

We isolated M. abscessus (n = 3) and M. fortuitum (n = 1) from one case of breast abscess and three cases of postsurgical wound infections. Of these, two isolates of M. abscessus were obtained from postsurgical wound infections and one isolate of M. abscessus was obtained from the case of breast abscess.

Drug susceptibility profile of rapidly growing mycobacteria isolated in Delhi

All the M. abscessus isolates (n = 3) were susceptible to clarithromycin (MIC ≤2 μg/ml), amikacin (MIC ≤16 μg/ml), and linezolid (MIC ≤8 μg/ml), while susceptibility to levofloxacin was seen in 2/3 (66.6%) isolates. The M. fortuitum isolate (n = 1) was susceptible to amikacin (MIC = 8 μg/ml), linezolid (MIC ≤1 μg/ml), clarithromycin (MIC = 0.25 μg/ml), and clofazimine (MIC = 0.5 μg/ml). The isolate was resistant to imipenem (MIC ≥128 μg/ml) [Table 3].
Table 3: Minimum inhibitory concentration of various antimicrobial agents observed in the rapidly growing mycobacteria isolated in the present study

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  Discussion Top


RGM are important causes of infection due to NTM. Reports of RGM infection have been steadily increasing in the past few years, with M. abscessus, M. fortuitum, and M. chelonae being the most common species reported. RGM are known to cause various infections, including infections of the respiratory tract, skin and soft tissue, bone and joint, lymphadenitis, etc. Skin and soft-tissue infections may occur after a traumatic injury due to accidental contamination of wounds. Hematogenous spread of infection in immune-compromised hosts can also not be ruled out.[51] In addition, several studies have documented occurrence of postsurgical infections due to RGM. In fact, it has been observed that RGM that are transmitted through potable water can lead to postsurgery wound infections due to contaminated instruments.[33] The water used during sterilization processes seems to contribute to contamination of instruments.[31] In spite of the increase in awareness of RGM infections, there is limited information on skin and soft-tissue infections due to RGM. Of the 39 reports we reviewed, the maximum number of reports was from the USA (8/39, 20.5%), Taiwan (5/39, 12.8%), and India (5/39, 12.8%). In Europe, there were three reports from Switzerland (3/39, 7.6%), two (2/39, 5%) from France and Germany, and one report from Spain (1/39, 2.5%). There were limited reports from South Asia.[20],[21],[22],[23],[24] The most common RGM species identified was M. abscessus (184/475, 38.7%). This was followed by M. fortuitum (150/475, 31.5%). M. chelonae (72/475, 15%) and M. chelonae–M. abscessus complex (46/475, 9.6%) were reported in smaller numbers. A study by Kannaiyan et al. did not elaborate on individual species and hence was not included in the final analysis.[20] In the present study conducted in Delhi, we isolated M. abscessus (n = 3) and M. fortuitum (n = 1) from patients with skin and soft-tissue infections.

Treatment of RGM infections poses difficulties and involves a multidrug regimen with variable response rates. Furthermore, the long duration of therapy poses a risk for drug-induced toxicity. Selection of the antimicrobial agent used for therapy is based on results of drug susceptibility tests performed. Moreover, there are reports of increasing antimicrobial resistance in RGM, underscoring the need to perform drug susceptibility testing. In spite of this, very few investigators have reported the antimicrobial susceptibility profile of RGM isolated from skin and soft-tissue infections. The drug susceptibility profile varies according to the species of RGM. Pang et al. tested drug susceptibility of forty international reference RGM strains and determined that M. chelonae, M. abscessus, Mycobacterium bolletii, M. fortuitum, Mycobacterium boenickei, M. conceptionense, Mycobacterium pseudoshottsii, Mycobacterium septicum, and Mycobacterium setense were the most resistant species.[11] Other studies have also reported similar results.[52]

However, only 26/39 (66.6%) studies we reviewed had performed drug susceptibility testing of the isolates [Table 1]. The Clinical and Laboratory Standards Institute recommends broth microdilution assay for drug susceptibility testing of RGM.[53] Inconsistent results have been observed in E-test and disc diffusion methods, which are, therefore, not recommended.[53] However, only 10/26 (38.4%) studies reviewed used broth dilution for drug susceptibility testing, while 4/26 (15.3%) used disc diffusion assay and 1/26 (3.8%) used E-test. Interestingly, the antibiotics tested in different studies varied. No single antibiotic was uniformly used in all the studies reviewed [Table 2]. Maximum sensitivity of M. abscessus was seen to clofazimine and tigecycline (100% each), followed by clarithromycin (97.7%) and amikacin (95.5%). M. fortuitum was maximally susceptible to tigecycline (100%), moxifloxacin (100%), ofloxacin (100%), amikacin (98.7%), levofloxacin (95.5%), and linezolid (94.4%), and M. chelonae was susceptible to clofazimine (100%) and tigecycline (100%) [Table 2]. However, although these figures are averaged from all the ten studies included in the review, some of the susceptibilities are based on the results of single studies. There were only five studies from India[20],[21],[22],[23],[24] but none from other South Asian regions. Of the studies from India, Kannaiyan et al. reported isolation of M. fortuitum and M. chelonae from surgical site infections.[20] Antibiotic susceptibility testing was performed by Kirby–Bauer disc diffusion method. All the isolates tested were susceptible to clarithromycin, linezolid, and amikacin, with susceptibility to ciprofloxacin, tobramycin, and rifampicin,[20] though drug susceptibility pattern of individual species was not identified. Ghosh et al. obtained M. abscessus and M. fortuitum from port-site infections. The isolates were highly susceptible to clarithromycin, amikacin, and imipenem.[21] Another study from India isolated M. chelonae from three patients with traumatic or surgical wounds. The patients were treated with clarithromycin and doxycycline.[22] In our own study, all the M. abscessus isolates were susceptible to clarithromycin, amikacin, and linezolid. Previous reports also confirm that M. abscessus is a highly resistant microorganism with reliable in vitro susceptibility only to amikacin and clarithromycin.[52] The single M. fortuitum isolate was susceptible to ciprofloxacin, doxycycline, amikacin, linezolid, clofazimine, and levofloxacin but was resistant to imipenem. The American Thoracic Society recommends routine susceptibility testing for RGM to amikacin, imipenem (against M. fortuitum), doxycycline, fluoroquinolones, a sulfonamide or trimethoprim-sulfamethoxazole, cefoxitin, clarithromycin, linezolid, and tobramycin (against M. chelonae).[4] Tang et al. also tested the susceptibility of 288 RGM against tobramycin and reported resistance in 98% isolates.[30] Unfortunately, we had not tested our isolates against tobramycin.


  Conclusion Top


There are very few reports on the drug susceptibility profile of RGM from skin and soft-tissue infections from a number of regions of the world. The reports that are available did not use a uniform method for drug susceptibility testing, nor did they use a common panel of drugs. Furthermore, since there are limited options for antibiotics that can be used for RGM infections, it is important to generate data on a higher number of isolates in different regions of the world to be able to treat these infections optimally.

Ethical statement

The study was approved by the Institutional Ethics Committee.

Acknowledgment

CK (5/8/5/22/2019-ECD-1) and KS (5/3/8/6/ITR-F/2018-ITR) acknowledge the ICMR for providing fellowship.

Financial support and sponsorship

This work was supported by the Indian Council of Medical Research, India (ICMR) (No. 5/8/5/14/2013-ECD1).

Conflicts of interest

There are no conflicts of interest.



 
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