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 Table of Contents  
Year : 2016  |  Volume : 5  |  Issue : 3  |  Page : 288-293

Prevalence and species spectrum of both pulmonary and extrapulmonary nontuberculous mycobacteria isolates at a tertiary care center

1 Department of Microbiology, Sanjay Gandhi Postgraduate Institute of Medical Sciences, Raebareli Road, Lucknow; Department of Microbiology, Sri Satya Sai University of Technology and Medical Sciences, Bhopal, India
2 Department of Microbiology, Sanjay Gandhi Postgraduate Institute of Medical Sciences, Raebareli Road, Lucknow, India
3 Department of Microbiology, Sri Satya Sai University of Technology and Medical Sciences, Bhopal, India

Date of Web Publication13-Feb-2017

Correspondence Address:
Tapan N Dhole
Department of Microbiology, Sanjay Gandhi Postgraduate Institute of Medical Sciences, Raebareli Road, Lucknow 226014, Uttar Pradesh
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Source of Support: None, Conflict of Interest: None

DOI: 10.1016/j.ijmyco.2016.06.008

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Objective/background: Nontuberculous mycobacteria (NTM) infection associated with pulmonary and extrapulmonary disease has been increasing globally. Despite an increase in incidence rate of NTM infection, its prevalence, species diversity, and circulation pattern in India is largely unknown. This study sought to investigate the overall burden and diversity of NTM among both pulmonary and extrapulmonary clinical isolates from a Northern Indian population. Methods: The study was conducted in the Department of Microbiology, from January 2013 to December 2015. A total of 4620 clinical samples were collected from patients suspected to have pulmonary and extrapulmonary tuberculosis. Preliminary diagnosis was performed using Ziehl–Neelsen staining followed by liquid culture in BacT/ALERT three-dimensional system. A total of 906 positive cultures obtained were differentiated as either NTM or Mycobacterium tuberculosis complex using a biochemical and MPT64 antigen test. Further identification of NTM species was confirmed with a line probe assay. Results: Out of 906 cultures isolates, 263 (29.0%) were confirmed as NTM and 643 (71.0%) were identified as Mycobacterium tuberculosis complex. A total of 79.4% of the NTM were recovered from pulmonary and 18.2% from extrapulmonary specimens. The diversity of NTM species was high (13 species) and predominated by Mycobacterium abscessus (31.3%) followed by Mycobacterium fortuitum (22%), Mycobacterium intracellulare (13.6%), Mycobacterium chelonae (9.1%), however, M. abscessus and M. fortuitum were the predominant species in both types of clinical isolates. Men (60.4%) and older patients aged greater than 55 years were the predominated risk group for NTM infection. Conclusion: The high prevalence and species diversity of NTM suggests the need for immediate and accurate characterization of NTM for proper treatment and management of patients.

Keywords: Liquid culture, Mycobacterium tuberculosis complex, Nontuberculous mycobacteria, Species identification

How to cite this article:
Umrao J, Singh D, Zia A, Saxena S, Sarsaiya S, Singh S, Khatoon J, Dhole TN. Prevalence and species spectrum of both pulmonary and extrapulmonary nontuberculous mycobacteria isolates at a tertiary care center. Int J Mycobacteriol 2016;5:288-93

How to cite this URL:
Umrao J, Singh D, Zia A, Saxena S, Sarsaiya S, Singh S, Khatoon J, Dhole TN. Prevalence and species spectrum of both pulmonary and extrapulmonary nontuberculous mycobacteria isolates at a tertiary care center. Int J Mycobacteriol [serial online] 2016 [cited 2022 Jul 6];5:288-93. Available from: https://www.ijmyco.org/text.asp?2016/5/3/288/200067

  Introduction Top

Nontuberculous mycobacteria (NTM) has been identified in human pulmonary and extrapulmonary diseases and are of great concern for clinicians and microbiologists because of their increasing global incidence [1]. An increasing pattern of NTM was recently reported from India with a prevalence rate from 0.7% to 34% [2],[3]. Geographical variance has also been documented in both prevalence and species spectrum of NTM. Mycobacterium avium, Mycobacterium fortuitum, and Mycobacterium scrofulaceum are the most frequently occurring species as major etiological agents in human infections out of 42 disease-causing NTM species among all known NTM species [2],[4]. In India, fewer studies have been documented for the species wise prevalence of NTM in pulmonary and extrapulmonary specimens. Depending on the species isolated and its susceptibility profile, the treatment options differ [5]. Additionally, most of the NTMs are resistant to the drugs and antibiotics that are being used to treat the patients infected with Mycobacterium tuberculosis complex (MTBC). Studies regarding this aspect are scarce in our geographical location. Therefore, the determination of the species spectrum of NTM at a particular geographical location is very necessary.

False diagnosis of NTM as tuberculosis (TB) or multidrug resistant-TB (MDR-TB) poses a significant challenge for developing an effective patient care strategy. Conventional methods like biochemical tests for NTM diagnosis are labor intensive, error prone, as well as requiring safety procedures to perform them [6]. However, newer techniques like high performance liquid chromatography, chemiluminescent DNA probe, nucleic acid amplification, and sequencing of 16S ribosomal RNA genes are quite sensitive but require highly sophisticated and expensive instruments which limits their utility in clinical diagnosis. However, the GenoType Mycobacterium common mycobacteria/additional species assay is rapid and can accurately differentiate different NTM species. With this background, the objective of our study is to estimate the prevalence of NTM among pulmonary and extrapulmonary isolates and differentiate the NTM species among both types of pulmonary and extrapulmonary isolates at this geographical part of the country.

  Materials and methods Top

Study site, design, and ethical clearance

The prospective study was performed at the Sanjay Gandhi Postgraduate Institute of Medical Sciences, Lucknow. TB suspected patients from visiting indoor patient departments, outdoor patient departments, and various wards between January 2013 and December 2015 were screened for the study. The study was approved by the Institutional Ethical Committee of the Institute and a written informed consent was obtained from all patients prior to their recruitment in the study.

Data collection

Approximately 2–10 mL of respiratory (sputum, broncho-alveolar lavage fluid, and lung tissue) and nonrespiratory specimens (lymph node aspirate, cold abscesses, pleural fluid, cerebrospinal fluid, synovial fluid, ascetic fluid, urine, gastric aspirate, pus, bone marrow, wound, and pus swab) were collected consecutively from 4620 nonrepeated patients having extrapulmonary and pulmonary TB. Patients who belong to north Indian ethnicity were enrolled for the present study. Patients of all age groups were considered for the study and included both male and female populations.

Microbiological methods

All the clinical specimens received were subjected to smear microscopy using the Ziehl–Neelsen (ZN) staining method [7]. Specimens, which contain normal commensal bacterial flora, were decontaminated with the standard N-acetyl-l-cysteine-NaOH method [8]. Specimens were centrifuged and the sediment was inoculated into the vials of the BacT/ALERT three-dimensional (3D) system (BioMerieux, Marcy l'Etoile, France) containing modified Middlebrook 7H9 with an antibiotic supplement (amphotericin B: 0.018% weight/volume [wt/vol]; azlocillin: 0.0034% wt/vol; nalidixic acid: 0.04% wt/vol; trimethoprim: 0.00105% wt/vol; polymyxin B: 10,000 U; and vancomycin: 0.0005% wt/vol). BacT/ALERT 3D vials were monitored continuously with the BacT/ALERT 3D system [9]. Samples with positive growth vials were removed from the machine and then were subjected to smear microscopy for the presence of acid fast bacilli (AFB). Samples that failed to show any growth after 6 weeks of incubation in the machine were removed and treated as negative for mycobacteria.

Cultures with positive growth on the BacT/ALERT 3D and presence of AFB by ZN stain were screened with biochemical tests which included niacin production, catalase activity at 68 °C at pH 7, and were tested with a rapid TB antigen assay (SD-Bioline Ag MPT64 Rapid TM assay; Standard Diagnostics, Kyonggi-do, Korea) which identifies antigens specific to MTBC. Isolates confirmed as MTB then went through a drug susceptibility test with the polymerase chain reaction based Genotype MTBDR plus test (Hain Lifescience, Nehren, Germany). Cultures with positive growth on BacT/ALERT 3D and the presence of AFB by ZN stain but that were negative for MTBC using the SD-Bioline assay were further identified for the species level.

NTM species identification

Characterization of species was carried out with the reverse hybridization-based line probe assay as per the manufacturer's instructions [10]. Genotype CM (Hain Lifescience, Nehren Germany) was used for primary identification of the most common mycobacterium species. Unidentified isolates or additional mycobacterium species from the above assay was performed using Genotype Mycobacterium AS kit (Hain Lifescience, Nehren, Germany). Interpretation of the final results after hybridization was done based on the presence and absence of different bands and compared with reference band as provided in the kit.

Data analysis

The clinical and demographic data were analyzed by using the SPSS version 19.0 (IBM, NY, USA) software package.

  Results Top

A total of 4,620 clinical specimens were analyzed during this study period. Of these, 109 (25.6%) and 906 (19.6%) were positive for AFB by ZN staining and culture method, respectively. Out of 906 culture isolates, 263 (29.0%) were confirmed as NTM and 643 (71.0%) were identified as MTBC. Among 263 NTM, 209 (79.4%) were from pulmonary sites and 54 (18.2%) were from extrapulmonary sites. Mixed infection of mycobacterium could not be observed in any case.

The median age of NTM-positive patients was 48 years; the predominant age group was >55 years (36.2%) followed by 26–45 years (30.4%), 46–54 years (18.2%), 18–25 years (10.6%), and 1–17 years (4.1%) age group, respectively. Men were (60.4%) more predominant than female (39.5%) patients. Thirty five cases of type two diabetes mellitus and three cases of human immunodeficiency virus (HIV) infection were also found to be positive for NTM ([Table 1]).
Table 1: Demographic characteristic of nontuberculous mycobacterial cases.

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The majority of NTM were isolated from pulmonary specimens, including 189 sputum (74.5%), 19 bronchial lavage/wash (7.2%), and one lung tissue biopsy (0.38%). In extrapulmonary specimens, NTM were identified from five urine (1.9%) specimens, 13 lymph node (3.4%), 19 pus (6.0%), seven biopsy (2.2%), three pleural fluid (1.1%), two bone marrow (0.8%), one gastric aspirate (0.8%), two cerebrospinal fluid (0.8%), one breast tissue (0.8%), and one from ascetic fluid (0.8%; [Table 2]).
Table 2: Sample wise distribution of nontuberculous mycobacteria isolates.

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Diversity of NTM species

A wide range of NTM species (13) were observed ([Figure 1]). The rapid growing species include Mycobacterium abscessus (31.3%) followed by M. fortuitum (22%) and Mycobacterium chelonae Scientific Name Search  (9.1%). The slow growing species mainly consisted of Mycobacterium intracellulare (13.6%), M. avium (7.2%), Mycobacterium interjectum (3.4%), Mycobacterium simiae (3.4%), Mycobacterium gordonae (2.6%), M. scrofulaceum (19%), Mycobacterium kansasii (1.9%), Mycobacterium szulgai (1.7%), Mycobacterium malmoense (0.7%), and Mycobacterium intermedium (0.7%), respectively ([Figure 1]).
Figure 1: Diversity of nontuberculosismycobacteria in pulmonary and extrapulmonary clinical isolates. NTM = nontuberculous mycobacteria.

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NTM species distribution in pulmonary and extrapulmonary isolates

M. interjectum, M. simiae, M. gordonae, M. kansasii, Mycobacterium szulgai, M. intermedium, and M. malmoense were only reported from pulmonary specimens. Whereas M. abscessus, M. fortuitum, M. intracellulare, M. chelonae, M. avium, and M. scrofulaceum were frequently isolated from both types ([Table 2]).

  Discussion Top

NTM is an emerging public health problem, especially in developing countries of the world. MTBC and NTM were found to be responsible for various pulmonary, skin and soft tissue, and disseminated infections. Our study addresses the prevalence of NTM and their species diversity in pulmonary and extrapulmonary specimens obtain from Northern Indian population.

In the present study, 29% of NTM were isolated from pulmonary and extrapulmonary samples. However, NTM was predominantly reported from pulmonary specimens. Species found in pulmonary specimens were M. abscessus, M. fortuitum, M. intracellulare, M. chelonae, M. avium, M. interjectum, M. simiae, M. gordonae, M. kansasii, M. szulgai, M. intermedium, and M. malmoense. In extrapulmonary specimens we found M. abscessus, M. fortuitum, M. intracellulare, M. chelonae, and M. scrofulaceun, M. abscessus, and M. fortuitum were common in both clinical specimens. However, variation in incidence of NTM reported from different regions of India. In Chandigarh, NTM incidence was found to be 7.4%, similarly from Delhi where it is reported to be around 8.3% and M. fortuitum was predominant in both places [11],[12]. From Kolkata, 17.4% NTM was documented from sputum [13]. The study conducted in a tertiary care center in South India reported 8.6% NTM in pulmonary specimens and M. avium/M. intracellulare were the predominated species [14]. These differences may be as a result of different geographical distribution of NTM throughout India. M. scrofulaceum has been reported for the first time from our center in both pulmonary and extrapulmonary specimens; however, this was previously reported from South India.

In an international context, a study involving 30 different countries from six different continents documented a higher prevalence of Mycobacterium avium complex from North and South America and Europe. M. intracellulare was predominantly reported from South Africa and Australia [15]. This is in contrast to our study in which M. abscessus and M. fortuitum were identified as predominant species among patients with pulmonary and extrapulmonary disease. Our study is in agreement with previous studies carried out in China, South Arabia, and Taiwan in which M. abscessus was the predominant NTM species [16],[17],[18],[19]. The second most common species that was reported in our study was M. fortuitum which was in agreement with the finding of a study carried out in Shanghai [20].

Our study shows that men were the predominant risk group (60.4%), which was in agreement with previous studies considering sex as a risk factor for NTM infection [21],[22]. Patients of a higher age group, above 55 years, were a demographical risk group for NTM infection in our study. In various studies the role of older age as a demographic risk factor for NTM infection has also been previously described [22],[23]. This could be because older people are more prone to preexisting lung disease, which may favor NTM colonization and infection.

Diabetes and HIV infection are known to suppress the cellular arm of immunity and hence predispose the patient to NTM infection. Both are considered as important risk factors for NTM infection. In the current study, the HIV positivity rate was found to be lower in NTM patients which is in agreement with previous studies conducted in China, Denmark, and the USA, with 0.99%, 2.4%, and 3.4% of HIV infected NTM patients, respectively [24],[25],[26],[27]. We isolated M. abscessus identified in two HIV positive patients and M. avium was identified in another one patient. In the study, 13% cases with diabetes were found in NTM infected patients. This could be because of the higher number of diabetic cases reported from India.

In our study, the most frequent NTM species found in pulmonary and extrapulmonary disease was M. abscessus; this suggests its high prevalence could be the result of its abundance in this region and its feature of drug resistance and pathogenicity promote its persistence in this region [28].

Fewer NTM data were reported from India. The reason could be due to limited funds, disorganized laboratory structure, other disease burden in the hospital, as well as lack of awareness among physicians and microbiologists especially in rural settings. NTM infection is often misdiagnosed with MDR-TB, as clinical, image findings, and microscopy were similar in both infections. Also, resistance to first-line drugs and some second-line drugs often occur in NTM which may lead to the misdiagnosis of NTM as MDR-TB. A delay in an accurate diagnosis of NTM leads to an increase in mortality and morbidity. In summary, our study warrants the need of patient management as well as the development of prevention strategies against NTM.

  Conflicts of interest Top

The authors declare no competing interest.

  Acknowledgments Top

Ms. Jyoti Umrao is thankful to the Indian Council of Medical Research, New Delhi (80/806/2013-ECD-I) for providing the fellowship.

  References Top

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