Identification and characterization of nontuberculous mycobacteria isolated from suspected pulmonary tuberculosis patients in eastern china from 2009 to 2019 using an identification array system

Zhu, Yelei; Hua, Wenya; Liu, Zhengwei; Zhang, Mingwu; Wang, Xiaomeng; Wu, Beibei; Wang, Zhen; Chen, Jiazhen

doi:10.1016/j.bjid.2022.102346

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Original Article • Braz J Infect Dis 26 (02) • 2022 • https://doi.org/10.1016/j.bjid.2022.102346 copy

Identification and characterization of nontuberculous mycobacteria isolated from suspected pulmonary tuberculosis patients in eastern china from 2009 to 2019 using an identification array system

Authorship SCIMAGO INSTITUTIONS RANKINGS

Abstract

Objective

Nontuberculous mycobacteria (NTM) species are increasingly being isolated and have become a key factor affecting public health by causing pulmonary diseases. Most NTM species do not respond to conventional tuberculosis (TB) drugs. This study aimed to identify NTM isolated from suspected pulmonary TB patients from the Zhejiang province and analyze their distribution in the region.

Methods

A total of 1,113 NTM isolates from patients suspected to be suffering from acid-fast bacilli-positive tuberculosis were identified at the species level, using the CapitalBio Mycobacterium identification array and polymerase chain reaction amplification and sequencing of 16S-23S gene internal transcribed spacer (ITS), 16S rRNA, and hsp65.

Results

Of the 23,138 isolates, we identified 1,102 NTM (4.8%), mainly including Mycobacterium intracellulare (54.81%, 604/1,102), M. chelonae-M. abscessus (16.52%, 182/1,102), M. avium (13.16%, 145/1,102), M. kansasii (8.17%, 90/1,102), and M. gordonae (3.27%, 36/1,102).

Conclusion

The distribution of NTM species observed in patients with suspected pulmonary tuberculosis provides guidance for the diagnosis and treatment of NTM pulmonary diseases.

Keywords
Identification; Nontuberculous mycobacteria; Pulmonary tuberculosis; NTM pulmonary diseases

Gene	Direction^* ⁎ F and R represent forward and reverse, respectively.	Sequence (5′3′)	Conditions
16S-23S ITS	F	GGG TAC TGA GAT GTT TCA CTT C	95°C for 5 min
	R	TCA CCT CCT TTC TAA GGA GCA CC	35 cycles (94°C for
16s rRNA	F	AGT TTG ATC CTG GCT CAG	35 s; 64/56/60°C for 30 s; 72°C for 50 s)
	R	GGT TAC CTT GTT ACG ACT T
hsp65	F	ACC AAC GAT GGT GTG TCC AT
	R	CTT GTC GAA CCG CAT ACC CT	72°C for 10 min

species	count	proportion	methods
M. intracellulare	604	54.81%
M. chelonae and M. abscessus	182	16.52%
M. avium	145	13.16%
M. kansasii	90	8.17%
M. gordonae	36	3.27%
M. fortuitum	9	0.82%	CapitalBio
M. scrofulaceum	5	0.45%	Mycobacterium
M. terrae	3	0.27%	identification
M. marinum and M. ulcerans	2	0.18%	array
M. smegmatis	2	0.18%
M. xenopi	2	0.18%
M. phlei	1	0.09%
M. szulgai and M. malmoense	1	0.09%
M. peregrinum	5	0.45%
M. intermedium	4	0.36%
M. monacense	2	0.18%
M. seoulense	2	0.18%
M. thermoresistibile	2	0.18%	Genes
M. chubuense	1	0.09%	Sequencing
M. mucogenicum	1	0.09%
M. arupense	1	0.09%
M. parascrofulaceum	1	0.09%
M. shigaense	1	0.09%
sum	1,102	100%

District/nation	year	NTM proportion	Species rank	methods	source
China, Zhejiang province	2009-2019	4.8% (1,112/23,138)	M. intracellulare (54.81%); M. chelonae and M. abscessus (16.52%); M. avium (13.16%); M. kansasii (8.17%)	CapitalBio Mycobacterium identification assay	This study
China	2013	6.4% (317/4,917)	MABC (36.0%); MAC (34.1%); M. kansaii (9.8%); M.paragordonae (5.4%)	MALDI-TOF MS	²¹21 Liu CF, Song YM, He WC, et al. Nontuberculous mycobacteria in China: incidence and antimicrobial resistance spectrum from a nationwide survey. Infect Dis Poverty. 2021;10: 59.
China, Fujian province	2011	4.2% (60/1,425)	M. intracellulare (68.3%); M. abscessus (10.0%); M. avium (6.7%); M. kansasii (6.7%);	16S rRNA, hsp65, rpoB, 16S-23S rRNA ITS	²²22 Lin S, Wei S, Zhao Y, Lin J, Pang Y.Epidemiology of human pulmonary infection with nontuberculous mycobacteria in Southeast China: a prospective surveillance study. Infect Drug Resist, 2019, 12.
China, Guangdong province	2013-2016	-	MAC (44.5%); MABC (40.5%); M. kansasii (10.0%); M. fortuitum (2.8%)	-	²⁷27 Tan Y, Su B, Shu W, et al. Epidemiology of pulmonary disease due to nontuberculous mycobacteria in Southern China, 2013-2016. BMC Pulm Med. 2018;18:168.
Japan	2006-2016	-	MAC (87.3%); MABC (5.5%); M. kansasii (3.9%)	-	²⁸28 Furuuchi K, Morimoto K, Yoshiyama T, et al. Interrelational changes in the epidemiology and clinical features of nontuberculous mycobacterial pulmonary disease and tuberculosis in a referral hospital in Japan. Respir Med. 2019;152:74-80.
America	2005-2015	-	MAC (83.2%); M. kansasii (7.7%); M. abscessus (3.4%)	-	²⁹29 Abate G, Stapleton JT, Rouphael N, et al. Variability in the management of adults with pulmonary nontuberculous mycobacterial disease. Clin Infect Dis. 2021;72:1127-37.
Northern Tunisia	2019	0.6% (60/10,466)	M. kansasii subtype 1(23.3%); M. fortuitum (16.6%); M. novocastrense (16.6%); M. chelonae(10.0%);	rpoB, 16S rRNA, hsp65, sodA	²³23 Gharbi R, Mhenni B, Ben Fraj S, Mardassi H. Nontuberculous mycobacteria isolated from specimens of pulmonary tuberculosis suspects, Northern Tunisia: 2002-2016. BMC Infect Dis. 2019;19:819.
Ghana	2017	2.5% (43/1,755)	M. intracellulare(41.9%); M. avium subsp paratuberculosis (30.2%); M. abscessus (11.3%); M. mucogenicum (7.0%)	IS6110, hsp65	¹³13 Otchere ID, Asante-Poku A, Osei-Wusu S, Aboagye SY, Yeboah-Manu D.Isolation and characterization of nontuberculous mycobacteria from patients with pulmonary tuberculosis in Ghana. Int J Mycobacteriol. 2017;6:70-5.
Korea	2009	7.1% (68/958)	M. abscessus (31%); M. fortuitum (15%); M. avium complex (8%); M. gordonae (8%);	rpoB	²⁴24 Jun HJ, Jeon K, Um SW, Kwon OJ, Lee NY, Koh WJ.Nontuberculous mycobacteria isolated during the treatment of pulmonary tuberculosis. Respir Med. 2009;103:1936-40.
Iran	2018	15.1% (62/410)	M. simiae (38.7%); M. fortuitum (19.3%); M. kansasii (17.7%); M. avium complex (8.0%);	16S rRNA, rpoB, hsp65, ITS	²⁰20 Nasiri MJ, Dabiri H, Fooladi AAI, Amini S, Hamzehloo G, Feizabadi MM.High rates of nontuberculous mycobacteria isolation from patients with presumptive tuberculosis in Iran. New Microbes New Infect. 2018;21.

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[1] ⁎Corresponding author. wangzhen@cdc.zj.cn (Z. Wang), jiazhen_chen@163.com (J. Chen).