LETTERS

Prevalence and
Drug Resistance of
Nontuberculous
Mycobacteria,
Northern China,
20082011
To the Editor: Nontuberculous
mycobacteria (NTM), defned as mem-
bers of Mycobacterium species other
than those in the M. tuberculosis com-
plex or M. leprae, are mostly consid-
ered to be opportunistic pathogens (1).
However, many NTM can and do cause
disease in immune-competent hosts.
Pulmonary infection by NTM can be
a source of diagnostic uncertainty, es-
pecially in locations such as in China,
where acid-fast staining of sputum
samples is the mainstay of diagnosis
for tuberculosis (2). NTM are also rela-
tively resistant to many of the frst- and
second-line drugs used to treat tubercu-
losis, thus making accurate diagnosis
and drug-susceptibility testing critical
to clinical management of NTM in-
fections (3). The medical and public
health communities have been con-
cerned about increasing prevalence of
NTM infection in China, and 2 recent
surveys, 1 from Shanghai and another
from a rural population in Shandong
Province, gave somewhat confict-
ing reports of the prevalence of these
infections (4,5). We therefore decided
to conduct a survey of NTM isolates in
Beijing from the National Tuberculo-
sis Clinical Laboratory of the Beijing
Chest Hospital. We also tested isolates
from specimens collected in this labo-
ratory against an extended drug sus-
ceptibility panel to determine which
drug regimens would be most useful in
therapy for various NTM infections.
During January 2008December
2011, sputum samples collected from
3,714 patients attending the Beijing
Chest Hospital with suspected pul-
monary tuberculosis were positive for
mycobacterial spp. Among the sur-
veillance population, 92% were from
northern China, including 13 provinces
and the 2 major urban conurbations
of Beijing and Tianjin. From our sur-
vey, the Han ethnic group accounted
for 82% of patients, and 61% of total
patients were from urban, rather than
rural, areas. Most (59%) of the patients
were male, and 40% were attending the
hospital for re-treatment of pulmonary
tuberculosis; mean age was 51 20
years. Of these mycobacterial isolates,
95 (2.6%) were positive for NTM;
NTM were identifed during initial
screening for resistance to p-nitroben-
zoic acid. We identifed the strains to
species level by sequencing the internal
transcribed spacer region of the 16S-
23S rRNA and 16S rRNA genes (6),
which is able to discriminate between
even closely related species such as M.
chelonae and M. abscessus (7).
Of the 95 NTM isolates, 38 (40%)
were M. intracellulare and 28 (29%)
were M. abscessus (Table). Five ad-
ditional species were also identifed:
M. fortuitum (8%), M. gordonae (8%),
M. kansasii (7%), M. avium (5%), and
M. parascrofulaceum (1%). A survey
performed recently in Shandong Prov-
ince also identifed M. intracellulare
as the most common isolate (4), but in
that study, it represented 52 (81%) of
64 cases. By contrast, 2 previous sur-
veys found M. chelonae to be the most
commonly isolated species (20% and
27% of isolates) (5,8). However, none
of the isolates from our study were M.
chelonae. Differences in isolates may
represent the representative patient
population from which they were de-
rived; M. chelonae was most common-
ly isolated from hospitals in southern
China (5,8). The most common NTM
species found in eastern Asia was M.
avium complex, in keeping with fnd-
ings from our study (9). Documenting
another trend, the International Union
Against Tuberculosis and Lung Dis-
ease reported that M. fortuitum was the
most frequently encountered species in
Turkey (33.9%), the Czech Republic
(17.5%), Portugal (16.5%), and other
countries in Europe (10).
Drug susceptibility testing (DST)
was performed by the proportion meth-
od according to the WHO Guidelines
for the Programmatic Management
of Drug-resistant Tuberculosis, 2011
Update (http://whqlibdoc.who.int/
publications/2011/9789241501583_
eng.pdf). We tested 3 frst-line anti-tu-
berculosis drugs (rifampin, isoniazid,
and ethambutol) and 7 second-line
agents (streptomycin, capreomycin,
amikacin, protionamide, para-amino
salicylic acid, ofoxacin, and levo-
foxacin) (Table). If a patient had mul-
tiple positive NTM isolates, DST was
performed on the last isolate. In agree-
ment with other studies (4,5), etham-
butol remained the most useful agent
against NTM; its overall resistance
rate among isolates tested was 42%.
Ranking of second or third agents,
however, should be guided by species
identifcation and DST. For example,
levofoxacin appears to be a good
choice for M. kansasii, M. gordonae,
or M. fortiutum infections (overall re-
sistance rate 22%), but a poor choice
against M. avium complex infections
(overall resistance rate 95%). The
second most prevalent species in our
study (28% of isolates), M. abscessus,
was resistant to the test drugs in >90%
of cases, highlighting the diffculties
associated with treatment for some
NTM infections.
Our study suggests that there
has been no substantial increase in
the prevalence of NTM in respira-
tory isolates from persons in north-
ern China. Most of the isolates show
substantial and extensive drug resis-
tance, providing major therapeutic
challenges for clinicians, especially
if patients are treated as they would
be for drug susceptible tuberculosis.
To guide therapy, both species-level
identifcation and DST of NTM iso-
lates should be performed. Our data
suggest that testing the effcacy of
some second-line agents, in particu-
lar, fuoroquinolones, may be ben-
efcial in identifying further options
for therapy.
1252 Emerging Infectious Diseases www.cdc.gov/eid Vol. 20, No. 7, July 2014
LETTERS
Acknowledgments
We thank all participants in this study.
This work was supported by the re-
search funding from Infectious Diseases
Special Project, Minister of Health of Chi-
na (2012ZX10003002).
The NTM isolates used in this proj-
ect were originated from the Beijing
Bio-Bank of clinical resources on Tu-
berculosis (D09050704640000), Beijing
Chest Hospital.
Xiaobo Wang,
1
Hao Li,
1

Guanglu Jiang,
Liping Zhao,Yifeng Ma,
Babak Javid,
and Hairong Huang
Author affliations: Beijing Tuberculosis and
Thoracic Tumor Institute, Beijing, China (X.
Wang, G. Jiang, L. Zhao, Y. Ma, H. Huang);
Tsinghua University, Beijing (H. Li, B. Ja-
vid); and Collaborative Innovation Centre
for Diagnosis and Treatment of Infectious
Disease, Hangzhou, China (B. Javid)
DOI: http://dx.doi.org/10.3201/eid2007.131801
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Address for correspondence: Hairong Huang,
Beijing Tuberculosis and Thoracic Tumor
Institute, Beijing 101100, China; email: hairong.
[email protected]
Emerging Infectious Diseases www.cdc.gov/eid Vol. 20, No. 7, July 2014 1253
1
These authors contributed equally to
this article.

Table. Species and drug-resistance profiles of 95 nontuberculous mycobacteria strains, northern China, 20082011*
Drugs
No. (%) resistant strains in Mycobacterium spp.
Total M. intracellulare M.abscessus M.fortuitum M. gordonae M.kansassi M. avium M.parascrofulaceum
INH 37 (97.37) 28 (100) 7 (87.5) 6 (75) 3 (42.86) 5 (100) 1 (100) 87 (91.58)
RIF 34 (89.47) 28 (100) 7 (87.5) 2 (25) 0 5 (100) 1 (100) 77 (81.05)
EMB 4 (10.53) 26 (92.86) 7 (87.5) 1 (12.5) 0 2 (40) 0 40 (42.11)
SM 38 (100) 28 (100) 7 (87.5) 4 (50) 6 (85.71) 5 (100) 1 (100) 89 (93.68)
CPM 31 (81.58) 26 (92.86) 4 (50) 1 (12.5) 2 (28.57) 3 (60) 1 (100) 68 (71.58)
AK 31 (81.58) 25 (89.29) 4 (50) 1 (12.5) 1 (14.29) 4 (80) 0 66 (69.43)
PTO 25 (65.79) 27 (96.43) 6 (75) 4 (50) 0 4 (80) 1 (100) 67 (70.53)
PAS 38 (100) 28 (100) 7 (87.5) 8 (100) 7 (100) 4 (80) 1 (100) 93 (97.89)
OFLX 38 (100) 28 (100) 3 (37.5) 3 (37.5) 1 (14.29) 5 (100) 1 (100) 79 (83.16)
LVFX 36 (94.74) 28 (100) 3 (37.5) 2 (25) 0 5 (100) 1 (100) 75 (78.95)
Total 38 (40) 28 (29.47) 8 (8.42) 8 (8.42) 7 (7.37) 5 (5.26) 1 (1.05) 95 (100)
*INH, isoniazid; RIF, rifampin; EMB, ethambutol; SM, streptomycin; CPM, capreomycin; AK, amikacin; PTO, protionamide; PAS, para-aminosalicylic acid;
OFLX, ofloxacin; LVFX, levofloxacin.

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