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Inferring Mycobacterium Tuberculosis Drug Resistance and Transmission using Whole-genome Sequencing in a High TB-burden Setting in China

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Biomedical and Environmental Sciences 2024年第2期37卷 157-169页

作者： FAN Yu Feng LIU Dong Xin CHEN Yi Wang OU Xi Chao MAO Qi Zhi yanG Ting Ting WANG Xi Jiang HE Wen Cong zhao Bing LIU Zhen Jiang ABULIMITI Maiweilanjiang AIHEMUTI Maimaitiaili GAO Qian zhao yan lin Key Laboratory of Medical Molecular Virology(MOE/NHC/CAMS) School of Basic Medical SciencesShanghai Medical CollegeFudan UniversityShanghai 200032China National Tuberculosis Reference Laboratory Chinese Center for Disease Control and PreventionBeijing 102206China Hangzhou Red Cross Hospital Hangzhou 310005ZhejiangChina Xinjiang Uygur Autonomous Region Center for Disease Control and Prevention Urumqi 830026XinjiangChina Tuberculosis Dispensary of Kashgar Prefecture Kashgar 844099XinjiangChina

Objective China is among the 30 countries with a high burden of tuberculosis(TB)worldwide,and TB remains a public health concern.Kashgar Prefecture in the southern Xinjiang Autonomous Region is considered as one of the highest TB burden regions in China.However,molecular epidemiological studies of Kashgar are lacking.Methods A population-based retrospective study was conducted using whole-genome sequencing(WGS)to determine the characteristics of drug resistance and the transmission patterns.Results A total of 1,668 isolates collected in 2020 were classified into lineages 2(46.0%),3(27.5%),and 4(26.5%).The drug resistance rates revealed by WGS showed that the top three drugs in terms of the resistance rate were isoniazid(7.4%,124/1,668),streptomycin(6.0%,100/1,668),and rifampicin(3.3%,55/1,668).The rate of rifampicin resistance was 1.8%(23/1,290)in the new cases and 9.4%(32/340)in the previously treated cases.Known resistance mutations were detected more frequently in lineage 2 strains than in lineage 3 or 4 strains,respectively:18.6%vs.8.7 or 9%,Plineage,and drug resistance were the risk factors for recent transmission.Despite the low rate of drug resistance,drug-resistant strains had a higher risk of recent transmission than the susceptible strains(adjusted odds ratio,1.414;95%CI,1.023–1.954;P=0.036).Among all patients with drug-resistant tuberculosis(DR-TB),78.4%(171/218)were attributed to the transmission of DR-TB strains.Conclusion Our results suggest that drug-resistant strains are more transmissible than susceptible strains and that transmission is the major driving force of the current DR-TB epidemic in Kashgar.

关键词： Mycobacterium tuberculosis Whole-genome sequencing(WGS) Transmission Drug resistance Xinjiang

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Changes in Notified Incidence of Pulmonary Tuberculosis in China,2005–2020

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Biomedical and Environmental Sciences 2023年第2期36卷 117-126页

作者： DONG Zhe YAO Hong yan YU Shi Cheng HUANG Fei LIU Jian Jun zhao yan lin WANG Qi Qi Epidemiology Office Chinese Center for Disease Control and PreventionBeijing 102206China

Objective To evaluate the trend of notified incidence of pulmonary tuberculosis(PTB)in China at different periods by population and region and to explore the effect of TB prevention and control in recent years.Methods Using pooled data on TB cases reported by the TB Information Management Reporting System(TBIMS)from 2005 to 2020,we calculated the annual percentage change(APC)using the Joinpoint regression model.Results From 2005 to 2020,a total of 16.2 million cases of PTB were reported in China,with an average notified incidence of 75.5 per 100,000 population.The age standardization rate(ASR)continued to decline from 116.9(/100,000)in 2005 to 47.6(/100,000)in 2020,with an average annual decrease of5.6%[APC=-5.6,95%confidence interval(CI):-7.0 to-4.2].The smallest decline occurred in2011–2018(APC=-3.4,95%CI:-4.6 to-2.3)and the largest decrease in 2018–2020(APC=-9.2,95%CI:-16.4 to-1.3).From 2005 to 2020,the ASR in males(159.8 per 100,000 in 2005,72.0 per 100,000 in2020)was higher than that in females(62.2 per 100,000 in 2005,32.3 per 100,000 in 2020),with an average annual decline of 6.0%for male and 4.9%for female.The average notified incidence was the highest among older adults(65 years and over)(182.3/100,000),with an average annual decline of6.4%;children(0–14 years)were the lowest(4.8/100,000),with an average annual decline of 7.3%,but a significant increase of 3.3%between 2014 and 2020(APC=3.3,95%CI:1.4 to 5.2);middle-aged(35–64years)decreased by 5.8%;and youth(15–34 years)decreased by an average annual rate of 4.2%.The average ASR in rural areas(81.3/100,000)is higher than that in urban areas(76.1/100,000).The average annual decline in rural areas was 4.5%and 6.3%in urban areas.South China had the highest average ASR(103.2/100,000),with an average annual decline of 5.9%,while North China had the lowest(56.5/100,000),with an average annual decline of 5.9%.The average ASR in the southwest was 95.3(/100,000),with the smallest annual decline(APC=-4.5,95%CI:-5.5 to-3.5);the average ASR in the Northwest China was

关键词： Tuberculosis Notified incidence Joinpoint regression model Trends China

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Cost-Effectiveness Analysis of Combined Chemotherapy Regimen Containing Bedaquiline in the Treatment of Multidrug-Resistant Tuberculosis in China

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Biomedical and Environmental Sciences 2023年第6期36卷 501-509页

作者： XU Cai Hong QIU Ying Peng HE Zi Long HU Dong Mei YUE Xiao CHEN Zhong Dan XU Yuan Yuan zhao yan lin National Center for Tuberculosis Control and Prevention China CDCBeijing 100226China China National Health Development Research Center Beijing 100226China The University of Sheffield S102TNSheffieldThe United Kingdom The Central South University Changsha 410083HunanChina World Health Organization Representative Office for China Beijing 100600China

Objective This study aims to estimate the cost-effectiveness of the combined chemotherapy regimen containing Bedaquiline(BR)and the conventional treatment regimen(CR,not containing Bedaquiline)for the treatment of adults with multidrug-resistant tuberculosis(MDR-TB)in China.Methods A combination of a decision tree and a Markov model was developed to estimate the cost and effects of MDR patients in BR and CR within ten years.The model parameter data were synthesized from the literature,the national TB surveillance information system,and consultation with experts.The incremental cost-effectiveness ratio(ICER)of BR vs.CR was determined.Results BR(vs.CR)had a higher sputum culture conversion rate and cure rate and prevented many premature deaths(decreased by 12.8%),thereby obtaining more quality-adjusted life years(QALYs)(increased by 2.31 years).The per capita cost in BR was as high as 138,000 yuan,roughly double that of CR.The ICER for BR was 33,700 yuan/QALY,which was lower than China's 1×per capita Gross Domestic Product(GDP)in 2020(72,400 yuan).Conclusion BR is shown to be cost effective.When the unit price of Bedaquiline reaches or falls below57.21 yuan per unit,BR is expected to be the dominant strategy in China over CR.

关键词： Bedaquiline Cost-effectiveness Multidrug-resistant tuberculosis China

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Evaluation of Microsphere-based xMAP Test for gyrA Mutation Identification in Mycobacterium Tuberculosis

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Biomedical and Environmental Sciences 2023年第4期36卷 384-387页

作者： OU Xi Chao zhao Bing SONG Ze Xuan PEI Shao Jun WANG Sheng Fen HE Wen Cong LIU Chun Fa LIU Dong Xin XING Rui Da XIA Hui zhao yan lin National Center for Tuberculosis Control and Prevention Chinese Center for Disease Control and PreventionBeijing 102206China School of Public Health Peking UniversityBeijing 100191China

Drug-resistant(DR) tuberculosis(TB) is a growing threat to public health[1]. Fluoroquinolone(FQ) antibiotics have long been used as anti-tuberculosis drugs, and their widespread application has led to the development ... 详细信息

关键词： tuberculosis drugs Mycobacterium

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Genetic Diversity and Drug Susceptibility of Mycobacterium tuberculosis Isolates in a Remote Mountain Area of China

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Biomedical and Environmental Sciences 2018年第5期31卷 351-362页

作者： ma ai jing wang sheng fen fan jia le zhao bing he guang xue zhao yan lin national institute for communicable disease control and prevention chinese center for disease control and preventionBeijing 102206China national center for tb control and prevention chinese center for disease control and preventionBeijing 102206China science and technology department chinese center for disease control and preventionBeijing 102206China

Objective We determined the genetic diversity of Mycobacterium tuberculosis（MTB） in a remote mountainous area of southwest China and evaluated the resolving ability of single nucleotide polymorphism（SNP） genotyping combined with variable number tandem repeat（VNTR） genotyping for Beijing family strains in association with drug resistance status.Methods Three hundred thirty-one MTB strains were isolated from patients living in mountainous regions of southwest China,and 8-loci SNP,VNTR-15 genotyping assays,and drug susceptibility testing of 9 drugs were performed.Results A total of 183 [55.29%（183/331）] strains were classified into the Beijing family.Of the 183 strains,111（60.66%） were defined as modern Beijing strains.The most predominant modern Beijing sub-lineage and ancient Beijing sub-lineage were Bmyc10 [39.34%（72/183）] and Bmyc25 [20.77%（38/183）],respectively.Of the isolates,19.64%（65/331） were resistant to at least 1 of the 9 anti-TB drugs and 17 [4.98%（17/331）] MTB isolates were multi-drug resistant tuberculosis（MDR-TB）.Two hundred sixty-one isolates showed a clustering rate of 14.18%（37/261） and a discriminatory index of 0.9990.The Beijing lineage exhibited a significantly higher prevalence of MDR-TB,as well as resistance to isoniazid（INH）,rifampin（RIF）,and para-aminosalicylic acid（PAS） when analyzed independently（P = 0.005,P = 0.017,P = 0.014,and P = 0.006 respectively）.The Beijing lineage was not associated with genetic clustering or resistance to any drug.In addition,genetic clustering was not associated with drug resistance.Conclusion MTB strains demonstrate high genetic diversity in remote mountainous areas of southwest China.Beijing strains,especially modern Beijing strains,are predominant in remote mountainous area of China.The combination of 8-loci SNPs and VNTR-15 genotyping is a useful tool to study the molecular epidemiology of MTB strains in this area.

关键词： Mycobacterium tuberculosis Beijing strains Variable number tandem repeat （VNTR） Singlenucleotide polymorphism （SNP）

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Prevalence and Risk Factors of Primary Drug-Resistant Tuberculosis in China

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Biomedical and Environmental Sciences 2016年第2期29卷 91-98页

作者： WANG Sheng Fen ZHOU yang PANG Yu ZHENG Hui Wen zhao yan lin National Center for Tuberculosis Control and Prevention Chinese Center for Disease Control and Prevention

Objective To investigate the prevalence of primary drug-resistant tuberculosis（TB） and associated risk factors in China. We also explored factors contributing to the transmission of multidrug-resistant tuberculosis（MDR-TB）. Methods A total of 2794 representative, Mycobacterium tuberculosis isolates from treatment-naive patients were subjected to drug susceptibility testing, and risk factors for drug-resistant TB were analyzed. We also analyzed MDR-TB strain sublineages, drug-resistance-conferring mutations, and risk factors associated with clustered primary MDR strains. Results Among 2794 Mycobacterium tuberculosis isolates from treatment-naive patients, the prevalence of any resistance to first-line drugs was 33.2% and the prevalence of MDR-TB was 5.7%. We did not find any risk factors significantly associated with resistance to first-line drugs. The 93 primary MDR-TB isolates were classified into six sublineages, of which, 75（80.6%） isolates were the RD105-deleted Beijing lineage. The largest sublineage included 65（69.9%） isolates with concurrent deletions of RD105, RD207, and RD181. Twenty-nine（31.2%） primary MDR strains grouped in clusters; MDR isolates in clusters were more likely to have S531 L rpoB mutation. Conclusion This study indicates that primary drug-resistant TB and MDR-TB strains are prevalent in China, and multiple measures should be taken to address drug-resistant TB.

关键词： Mycobacterium tuberculosis Primary drug resistance Multi-drug resistant tuberculosis

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Mutual Impact of Diabetes Mellitus and Tuberculosis in China

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Biomedical and Environmental Sciences 2017年第5期30卷 384-389页

作者： CHENG Jun ZHANG Hui zhao yan lin WANG Li Xia CHEN Ming Ting National Center for Tuberculosis Control and Prevention Chinese Center for Disease Control and Prevention Beijing102206 China

China has a double burden of diabetes mellitus and tuberculosis, and many studies have been carried out on the mutual impact of these two diseases. This paper systematically reviewed studies conducted in China covering the mutual impact of epidemics of diabetes and tuberculosis, the impact of diabetes on multi-drug resistant tuberculosis and on the tuberculosis clinical manifestation and treatment outcome, the yields of bi-directional screening, and economic evaluation for tuberculosis screening among diabetes patients.

关键词： Impact Tuberculosis Diabetes mellitus China

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Comparing the Genotype and Drug Susceptibilities between Mycobacterium avium and Mycobacterium intracellulare in China

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Biomedical and Environmental Sciences 2017年第7期30卷 517-525页

作者： ZHENG Hui Wen PANG Yu HE Guang Xue SONG Yuan Yuan zhao yan lin National institute for communicable disease control and prevention Chinese center for disease control and prevention Beijing 102206 China National Tuberculosis Reference Laboratory Chinese Center for Disease Control and Prevention Beijing 102206 China Science and Technology Department Chinese Center for Disease Control and Prevention Beijing 102206 China

Objective Mycobacterium avium （M. avium） and Mycobacterium intracellulare （M. intracellulare） are the major causative agents of nontuberculous mycobacteria （NTM）-related pulmonary infections. However, little is known about the differences in drug susceptibility profiles between these two species. Methods A total of 393 NTM isolates were collected from Shanghai Pulmonary Disease Hospital. Sequencing of partial genes was performed to identify the strains at species level. The minimum inhibitory concentration （MIC） was used to evaluate the drug susceptibility against 20 antimicrobial agents. Variable number of tandem repeat （VNTR） typing was conducted to genotype these two species. Results A total of 173 （44.0%） M. avium complex （MAC） isolates were identified, including 41 （10.4%） M. avium isolates and 132 （33.6%） M. intracellulare isolates. Clarithromycin and amikacin were the two most effective agents against MAC isolates. The Hunter-Gaston Discriminatory Index （HGDI） values for VNTR typing of M. avium and M. intracellulare isolates were 0.993 and 0.995, respectively. Levofloxacin resistance was more common among the unclustered strains than among the clustered strains of M. intracellulare. Conclusion M. intrecellulare was the most common NTM species in China. Clarithromycin and amikacin had high antimicrobial activities against MAC. VNTR typing of MAC isolates revealed a high discriminatory power. Levofloxacin resistance was associated with unclustered strains of M. intracellulare.

关键词： Nontuberculous mycobacterium, Phenotype Genotype Susceptibility Resistance

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Evaluation of Multidrug Resistant Loop-mediated Isothermal Amplification Assay for Detecting the Drug Resistance of Mycobacterium tuberculosis

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Biomedical and Environmental Sciences 2021年第8期34卷 616-622页

作者： LIU Chun Fa SONG Yi Meng HE Ping LIU Dong Xin HE Wen Cong LI yan Ming zhao yan lin National Center for Tuberculosis Control and Prevention Chinese Center for Disease Control and PreventionBeijing 102206China National Center of Gerontology Beijing HospitalBeijing 100730China National Institute for Communicable Disease Control and Prevention Chinese Center for Disease Control and PreventionBeijing 102206China National Clinical Research Center for Infection Disease Shenzhen Third People's HospitalShenzhen 518112GuangdongChina

Objective To evaluate multidrug resistant loop-mediated isothermal amplification(MDR-LAMP)assay for the early diagnosis of multidrug-resistant tuberculosis and to compare the mutation patterns associated with the rpoB,katG,and inhA genes at the Chinese Center for Disease Control and Prevention.Methods MDR-LAMP assay was evaluated using 100 Mycobacterium tuberculosis(Mtb)isolates obtained from the National Reference Laboratory for Tuberculosis in China.Phenotypic resistance to isoniazid and rifampicin and whole-genome sequencing served as reference standards.Results The sensitivity,specificity,positive predictive value(PPV),and negative predictive value(NPV)of MDR-LAMP were 85.5%,93.6%,96.7%,and 74.4%for the detection of resistance to isoniazid and rifampicin,respectively,and 80.5%,92.3%,98.6%,and 41.4%for the detection of Mtb cultured from smear-positive sputum samples,respectively.When DNA sequencing was used as the reference standard,the sensitivity,specificity,PPV,and NPV of MDR-LAMP were 93.1%,92.3%,97.2%,and 82.8%for the detection of katG and inhA gene mutations,respectively,and 89.1%,88.9%,93.4%,and 81.1%for the detection of rpoB gene mutation,respectively.Conclusion MDR-LAMP is a rapid and accessible assay for the laboratory identification of rifampicin and isoniazid resistance of Mtb isolates.

关键词： MDR-LAMP Mycobacterium tuberculosis Diagnostic method

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Comparison of Two Molecular Assays For Detecting Smear Negative Pulmonary Tuberculosis

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Biomedical and Environmental Sciences 2016年第4期29卷 248-253页

作者： LI Qiang BAO Xun Di LIU Yun OU Xi Chao PANG Yu zhao yan lin National Tuberculosis Reference Laboratory Chinese Center for Disease Control and Prevention Beijing 102206 China Anhui Chest Hospital Hefei 230032 Anhui China Xi 'an Chest Hospital Xi 'an 710061 Shaanxi China

Objective To compare the performance of MTBDRplus V2 and Xpert MTB/RIF for detecting smear negative pulmonary tuberculosis （PTB）. Methods Clinical PTB suspects were enrolled consecutively in Anhui Chest Hospital and Xi＇an Chest Hospital from January to December in 2014. The sputum samples of smear negative PTB suspects were collected and decontaminated. The sediment was used to conduct MTBDRplus V2, Xpert MTB/RIF and drug susceptibility test （DST）. All the samples with discrepant drug susceptibility result between molecular methods and phenotypic method were confirmed by DNA sequencing. Results A total of 1973 cases were enrolled in this study. The detection rates of Mycobacterium tuberculosis complex （MTBC） by MTBDRplus V2 and Xpert MTB/RIF were 27.67% and 27.98%, respectively. When setting MGIT culture result as a gold standard, the sensitivity and specificity of MTBDRplus V2 were 86.74% and 93.84%, and the sensitivity and specificity of Xpert MTB/RIF were 86.55% and 93.43%, respectively. For the detection of the resistance to rifampin, the sensitivity and specificity of MTBDRplus V2 were 94.34% and 96.62%, and the sensitivity and specificity of Xpert MTB/RIF were 88.68% and 95.96%, respectively. For the detection of the resistance to isoniazid, the sensitivity and specificity of MTBDRplus V2 were 77.38% and 98.02%, respectively. Conclusion MTBDRplus V2 and Xpert MTB/RIF can be used to detect MTBC in smear negative samples with satisfactory performance.

关键词： Smear negative pulmonary tuberculosis, Diagnosis Drug resistance

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