Skip directly to site content Skip directly to page options Skip directly to A-Z link Skip directly to A-Z link Skip directly to A-Z link
Volume 18, Number 3—March 2012

Prevalence of Nontuberculous Mycobacteria Infection, China, 2004–2009

Cite This Article

To the Editor: Pulmonary nontuberculous mycobacteria (NTM) diseases share clinical signs with tuberculosis (TB), causing a clinical dilemma with regard to therapy for patients with these diseases (1). In the past 30 years (post-AIDS era), NTM have increasingly been associated with pulmonary diseases in humans (2). Recent studies in urban areas of the People’s Republic of China have shown that the prevalence of NTM (isolation rate of NTM among all mycobacteria) is increasing; for example, prevalence in Shanghai increased from 4.26% in 2005 to 6.38% in 2008 (3). To investigate NTM prevalence in rural areas of China, we evaluated the NTM isolation rates, species distribution, and drug-resistance profiles through a population-based TB sentinel surveillance study in Shandong Province, the second largest province in China. The study protocol was approved by the Institutional Review Board of Shandong Provincial Chest Hospital (Jinan, Shandong, China).

Clinical samples were collected through the ongoing sentinel TB surveillance project, which first began in 7 counties in Shandong Province in 2004 and expanded to 13 counties in 2008. Of the total surveillance population, rural populations accounted for ≈80%. Each sample collected in this study was identified only by a unique participant number. Each surveillance site sent sputum samples from all patients with suspected TB to the TB Reference Laboratory of Shandong Provincial Chest Hospital for mycobacterial culture, drug-susceptibility testing, and species identification.

From January 1, 2004, through December 31, 2009, Mycobacteria spp. were isolated from sputum specimens from 3,949 patients with suspected pulmonary TB. Of these patients, mean age ± SD was 48.7 ± 20.4 years (range 1–92 years), 74.6% were male, and 300 were being re-treated for TB.

Identification of Mycobacteria spp. was first conducted by conventional biochemical testing—p-nitrobenzoic acid and 2-thiophene carboxylic acid hydrazide testing—following a standard protocol (4). Mycobacteria spp. were further identified by 16S rRNA gene sequence analysis (MicroSeq ID Microbial Indentification Software, version 2.0; Applied Biosystems, Foster City, CA, USA) to the species level as described (5). Drug-susceptibility testing was performed according to standard procedures recommended by the World Health Organization, and quality control was conducted by inter-laboratory confirmation testing by reference laboratories recognized by the World Health Organization in South Korea and in Hong Kong Special Administrative Region, China (6,7). The drug panel included 4 first-line anti-TB drugs: isoniazid, rifampin, streptomycin, and ethambutol.

The conventional biochemical testing of the 3,949 Mycobacteria spp. strains identified 68 NTM strains, among which the 16s rRNA gene sequence analysis confirmed 64 (1.6%) NTM strains and identified 3 M. tuberculosis complex strains and 1 Nocardia glanders strain. Among the 64 NTM strains, 52 (81.2%) were M. intracellulare, 5 (7.8%) were M. kansasii, 3 (4.7%) were M. fortuitum, 2 (3.1%) were M. chelonae, 1 (1.6%) was M. gordonae, and 1 (1.6%) was M. scrofulaceum. The first-line anti-TB drug resistance rates of the 64 NTM strains were 100% for isoniazid, 98.4% for streptomycin, 78.1% for rifampin, and 51.6% for ethambutol (Table). Among the 3,949 Mycobacteria spp. strains, 163 (4.1%) were resistant to at least isoniazid and rifampin, of which 50 (30.7%) strains were identified as NTM. Among 300 TB re-treatment cases, 12 (4.0%) were caused by clinically significant NTM infections. Over the 6 study years, NTM isolation rates among the study population did not show a substantial increasing or decreasing trend.

Our data suggest that the NTM isolation rate among patients with suspected pulmonary TB in rural China (1.6%) is relatively lower and more stable than that for urban areas (mean rate 5.09% in Shanghai) and that the Mycobacterium spp. differ from those in other areas of China (3,810). In China and most other developing countries to which TB is endemic, the decision to initiate pulmonary TB treatment is based only on finding a positive sputum smear by microscopy examination, not on Mycobacteria culture, species identification, and drug-resistance testing results. Among our study population, NTM strains showed high drug resistance to first-line anti-TB drugs and accounted for 30.7% of suspected multidrug-resistant TB (MDR-TB) cases and 4.0% of TB re-treatment cases.

These findings suggest that pulmonary NTM infections pose substantial difficulties with regard to clinical management of NTM and MDR-TB diseases in China. Laboratory species identification is imperative before proper treatment can be determined for patients with MDR-TB. Compared with conventional biochemical testing, 16S rRNA gene sequencing analysis can more accurately identify Mycobacteria spp.



We thank the local TB control professionals affiliated with the Shandong Provincial Tuberculosis Control Center for their collaboration in this study.

The study was sponsored by the Shandong Provincial Biomedical Development Project (2007GG20002029) and the Shandong Taishan Scholar Program. X.M. was supported by US National Institutes of Health grant RO1 AI075465.


Hui Jing, Haiying Wang, Yan Wang, Yunfeng Deng, Xinxin Li, Zhimin Liu, Edward A. Graviss, and Xin MaComments to Author 
Author affiliations: Shandong Provincial Chest Hospital, Jinan, People’s Republic of China (H. Jing, H. Wang, Y. Wang, Y. Deng, X. Li, Z. Liu, X. Ma); The Methodist Hospital Research Institute, Houston, Texas, USA (E.A. Graviss, X. Ma)



  1. Griffith  DE, Aksamit  T, Brown-Elliott  BA, Catanzaro  A, Daley  C, Gordin  F, An official ATS/IDSA statement: diagnosis, treatment, and prevention of nontuberculous mycobacterial diseases. Am J Respir Crit Care Med. 2007;175:367416. DOIPubMedGoogle Scholar
  2. Gopinath  K, Singh  S. Non-tuberculous mycobacteria in TB-endemic countries: are we neglecting the danger? PLoS Negl Trop Dis. 2010;4:e615. DOIPubMedGoogle Scholar
  3. Wang  HX, Yue  J, Han  M, Yang  JH, Gao  RL, Jing  LJ, Nontuberculous mycobacteria: susceptibility pattern and prevalence rate in Shanghai from 2005 to 2008. Chin Med J (Engl). 2010;123:1847.PubMedGoogle Scholar
  4. Kent  PT, Kubica  GP. Public health mycobacteriology: a guide for the level III laboratory. Atlanta: US Department of Health and Human Services, Public Health Service, Centers for Disease Control; 1985.
  5. El Amin  NM, Hanson  HS, Pettersson  B, Petrini  B, Von Stedingk  LV. Identification of non-tuberculous mycobacteria: 16S rRNA gene sequence analysis vs. conventional methods. Scand J Infect Dis. 2000;32:4750. DOIPubMedGoogle Scholar
  6. Chinese Medical Association. Clinical techniques standard operating procedures. Tuberculosis section. Beijing: People's Military Medical Press; 2004.
  7. World Health Organization. Guidelines for the programmatic management of drug-resistant tuberculosis. Geneva: The Organization; 2006.
  8. Lai  CC, Tan  CK, Chou  CH, Hsu  HL, Liao  CH, Huang  YT, Increasing incidence of nontuberculous mycobacteria, Taiwan, 2000–2008. Emerg Infect Dis. 2010;16:2946.PubMedGoogle Scholar
  9. Weimin  L, Guanglu  J, Zhihui  L, Huakun  H, Liquan  C, Miao  T, Non-tuberculous mycobacteria in China. Scand J Infect Dis. 2007;39:13841. DOIPubMedGoogle Scholar
  10. Hosker  HS, Lam  CW, Ng  TK, Ma  HK, Chan  SL. The prevalence and clinical significance of pulmonary infection due to non-tuberculous mycobacteria in Hong Kong. Respir Med. 1995;89:38. DOIPubMedGoogle Scholar




Cite This Article

DOI: 10.3201/eid1803.110175

Related Links


Table of Contents – Volume 18, Number 3—March 2012

EID Search Options
presentation_01 Advanced Article Search – Search articles by author and/or keyword.
presentation_01 Articles by Country Search – Search articles by the topic country.
presentation_01 Article Type Search – Search articles by article type and issue.



Please use the form below to submit correspondence to the authors or contact them at the following address:

Xin Ma, 6565 Fannin St, Houston, TX 77030, USA

Send To

10000 character(s) remaining.


Page created: February 16, 2012
Page updated: February 16, 2012
Page reviewed: February 16, 2012
The conclusions, findings, and opinions expressed by authors contributing to this journal do not necessarily reflect the official position of the U.S. Department of Health and Human Services, the Public Health Service, the Centers for Disease Control and Prevention, or the authors' affiliated institutions. Use of trade names is for identification only and does not imply endorsement by any of the groups named above.