Latent tuberculosis infection rate and risk factors in patients with rheumatic diseases: a multi-center, cross-sectional study

doi:10.19982/j.issn.1000-6621.20230207

Chinese Journal of Antituberculosis ›› 2024, Vol. 46 ›› Issue (1): 29-39.doi: 10.19982/j.issn.1000-6621.20230207

• Original Articles • Previous Articles Next Articles

Latent tuberculosis infection rate and risk factors in patients with rheumatic diseases: a multi-center, cross-sectional study

Zhang Lifan¹^,²^,³, Ma Yanan¹, Zou Xiaoqing¹^,⁴, Zhang Yueqiu¹, Zhang Fengchun⁵, Zeng Xiaofeng⁵, Zhao Yan⁵, Liu Shengyun⁶, Zuo Xiaoxia⁷, Wu Huaxiang⁸, Wu Lijun⁹, Li Hongbin¹⁰, Zhang Zhiyi¹¹, Chen Sheng¹², Zhu Ping¹³, Zhang Miaojia¹⁴, Qi Wencheng¹⁵, Liu Yi¹⁶, Liu Huaxiang¹⁷, Shi Xiaochun¹^,³(), Liu Xiaoqing¹^,²^,³(), the Epidemiological Study and Therapeutic Evaluation of Rheumatic Patients with Tuberculosis Study Team

¹Division of Infectious Diseases, Department of Internal Medicine, State Key Laboratory of Complex Severe and Rare Disease, Peking Union Medical College Hospital, Chinese Academy of Medical Sciences and Peking Union Medical College, Beijing 100730, China
²Clinical Epidemiology Unit, International Epidemiology Network, Chinese Academy of Medical Sciences and Peking Union Medical College, Beijing 100730, China
³Centre for Tuberculosis Research, Chinese Academy of Medical Sciences and Peking Union Medical College, Beijing 100730, China
⁴School of Population Medicine and Public Health, Chinese Academy of Medical Sciences and Peking Union Medical College, Beijing 100730, China
⁵Department of Rheumatology and Clinical Immunology, Peking Union Medical College Hospital, Chinese Academy of Medical Sciences and Peking Union Medical College, National Clinical Research Center for Dermatologic and Immunologic Diseases, State Key Laboratory of Complex Severe and Rare Disease, Key Laboratory of Rheumatology and Clinical Immunology, Ministry of Education, Beijing 100730, China
⁶Department of Rheumatology and Immunology, The First Affiliated Hospital of Zhengzhou University, Zhengzhou 450052, China
⁷Department of Rheumatology and Immunology, Xiangya Hospital, Central South University, Changsha 410008, China
⁸Department of Rheumatology, The Second Affiliated Hospital of Zhejiang University School of Medicine, Hangzhou 310009, China
⁹Department of Rheumatology, People’s Hospital of Xinjiang Uygur Autonomous Region, Urumqi 830001, China
¹⁰ Department of Rheumatology and Immunology, The Affiliated Hospital of Inner Mongolia Medical University, Hohhot 010000, China
¹¹ Department of Rheumatology and Immunology, The First Affiliated Hospital of Harbin Medical University, Harbin 150001, China
¹² Department of Rheumatology, Renji Hospital, School of Medicine, Shanghai Jiao Tong University, Shanghai 200001, China
¹³ Department of Clinical Immunology, Xijing Hospital, Fourth Military Medical University, Xi’an 710032, China
¹⁴ Department of Rheumatology, The First Affiliated Hospital of Nanjing Medical University, Nanjing 210029, China
¹⁵ Department of Rheumatology, Tianjin First Central Hospital, Tianjin 300192, China
¹⁶ Department of Rheumatology and Immunology, West China Hospital, Sichuan University, Chengdu 610041, China
¹⁷ Department of Rheumatology, Qilu Hospital of Shandong University, Ji’nan 250012, China

Received:2023-06-16 Online:2024-01-10 Published:2024-01-04
Contact: Shi Xiaochun, Email: shixch7722@163.com;Liu Xiaoqing, Email: liuxq@pumch.cn
Supported by:
Central High Level Hospital Clinical Research Project(2022-PUMCH-C-013);National Major Science and Technology Special Project for the 13th Five Year Plan(2017ZX10201302);National Science and Technology Major Special Project for the 12th Five Year Plan(2014ZX10003003)

Abstract

Abstract:

Objective: This study aimed to screen latent tuberculosis infection (LTBI) among patients with rheumatic diseases in China using the T-SPOT.TB assay and investigate factors affecting the results of T-SPOT.TB. Methods: Rheumatic diseases patients (n=3715) were enrolled from 13 tertiary hospitals in Eastern, Middle, and Western China from September 2014 to March 2016 and were screened by the T-SPOT.TB assay to detect LTBI. Basic information about the subjects were collected, including gender, age, region, body mass index, course of disease, smoking history, underlying disease, close contact history of tuberculosis patients, evidence of previous tuberculosis, the use of glucocorticoids, immunosuppressants and biologics, laboratory tests, and diagnosis of rheumatic disease, etc. Univariate analysis and multivariable logistic regression were performed to identify factors affecting the results of T-SPOT.TB. Results: out Of the 3715 patients, 672 were positive in T-SPOT.TB, the positive rate was 18.1% (95%CI: 16.9%-19.3%). There was a statistically significant difference in the positive rate of T-SPOT.TB test among patients with different types of rheumatic immune diseases (χ²=79.003, P<0.001), patients with Behcet’s syndrome had the highest positive rate (44.4%, 32/72), while patients with mixed connective tissue disease had the lowest positive rate (8.9%, 4/45). The positive rate of T-SPOT.TB test in male patients with rheumatic immune disease was 23.6% (168/711), which was significantly higher than that in females (16.8%, 504/3004, χ²=18.213, P<0.001). There was a statistically significant difference in the positive rate of T-SPOT.TB test among patients with rheumatic immune disease in different age groups (χ²=67.189, P<0.001), the 51-60 years old group had the highest positive rate (24.8%, 143/577), while the 16-20 years old group had the lowest positive rate (8.1%, 13/160). Multivariate logistic regression analysis showed that age≥41 years (aOR=1.81, 95%CI: 1.48-2.23), smoking ≥21 cigarettes/d (aOR=1.66, 95%CI: 1.15-2.40), previous history of tuberculosis (aOR=3.88, 95%CI: 2.71-5.57), and Behcet’s syndrome (aOR=3.00, 95%CI: 1.70-5.28) were independent related factors of T-SPOT.TB positive results; using high-dose hormones (aOR=0.67, 95%CI: 0.47-0.96) or biological agents (aOR=0.55, 95%CI: 0.36-0.84), low lymphocyte count (aOR=0.39, 95%CI: 0.25-0.62), hypoalbuminemia (aOR=0.72, 95%CI: 0.52-0.99), and multiple myositis/dermatomyositis (aOR=0.54, 95%CI: 0.29-0.99), systemic lupus erythematosus (aOR=0.75, 95%CI: 0.57-0.99) were independent correlation factors for negative T-SPOT.TB test results. Conclusion: Among patients with rheumatic diseases, the overall prevalence of LTBI is 18.1%. There is a significant difference in the positive rate of T-SPOT.TB test among different diseases. When patients are treated with high-dose glucocorticoids or biologics, have low lymphocyte counts, hypoalbuminemia, or suffer from systemic lupus erythematosus, more attention should be paid to potential false-negative results.

Key words: Rheumatic diseases, Mycobacterium tuberculosis, Infection, Immunologic techniques, Cross-sectional studies

CLC Number:

R593
R52

Zhang Lifan, Ma Yanan, Zou Xiaoqing, Zhang Yueqiu, Zhang Fengchun, Zeng Xiaofeng, Zhao Yan, Liu Shengyun, Zuo Xiaoxia, Wu Huaxiang, Wu Lijun, Li Hongbin, Zhang Zhiyi, Chen Sheng, Zhu Ping, Zhang Miaojia, Qi Wencheng, Liu Yi, Liu Huaxiang, Shi Xiaochun, Liu Xiaoqing, the Epidemiological Study and Therapeutic Evaluation of Rheumatic Patients with Tuberculosis Study Team. Latent tuberculosis infection rate and risk factors in patients with rheumatic diseases: a multi-center, cross-sectional study[J]. Chinese Journal of Antituberculosis, 2024, 46(1): 29-39. doi: 10.19982/j.issn.1000-6621.20230207

Figures/Tables 4

因素	阴性	阳性	单因素分析
因素	阴性	阳性	OR(95%CI)值	P值
性别[例(构成比,%)]
女性	2500(83.2)	504(16.8)	1.00
男性	543(76.4)	168(23.6)	1.53(1.26~1.87)	<0.001
年龄组[例(构成比,%)]
16~40岁	1601(86.6)	248(13.4)	1.00
≥41岁	1442(77.3)	424(22.7)	1.90(1.60~2.26)	<0.001
体质量指数[M(Q₁,Q₃)]	22.04(20.0,24.5)	22.3(20.0,25.0)	1.00(0.99~1.01)	0.770
病程[月,M(Q₁,Q₃)]	16.00(1.0,57.0)	16.0(2.0,62.0)	1.00(1.00~1.00)	0.249
吸烟≥21支/d [例(构成比,%)]
否	2901(82.6)	612(17.4)	1.00
是	124(69.7)	54(30.3)	2.06(1.48~2.88)	<0.001
糖尿病史[例(构成比,%)]
无	2872(82.1)	627(17.9)	1.00
有	143(78.6)	39(21.4)	1.25(0.87~1.80)	0.231
肝硬化[例(构成比,%)]
无	3027(81.9)	669(18.1)	1.00
有	12(92.3)	1(7.7)	0.38(0.05~2.91)	0.349
肿瘤史[例(构成比,%)]
无	3025(82.0)	663(18.0)	1.00
有	15(71.4)	6(28.6)	1.83(0.71~4.72)	0.215
结核病患者密切接触史[例(构成比,%)]
无	2989(82.2)	646(17.8)	1.00
有	36(73.5)	13(26.5)	1.67(0.88~3.17)	0.116
结核病既往史[例(构成比,%)]
无	2951(83.3)	592(16.7)	1.00
有	84(51.5)	79(48.5)	4.69(3.41~6.45)	<0.001
现用激素[例(构成比,%)]
无	539(75.6)	174(24.4)	1.00
有	2499(83.4)	498(16.6)	0.62(0.51~0.75)	<0.001
现用激素剂量[例(构成比,%)]^a
0~29mg/d	1960(79.8)	496(20.2)	1.00
30~59mg/d	650(84.4)	120(15.6)	0.73(0.59~0.91)	0.005
≥60mg/d	395(88.6)	51(11.4)	0.51(0.38~0.69)	<0.001
使用免疫抑制剂[例(构成比,%)]
否	1248(82.3)	268(17.7)	1.00
是	1795(81.6)	404(18.4)	1.05(0.88~1.24)	0.589
使用环磷酰胺[例(构成比,%)]
否	2616(81.6)	590(18.4)	1.00
是	427(83.9)	82(16.1)	0.85(0.66~1.10)	0.212
使用吗替麦考酚酯[例(构成比,%)]
否	2646(81.6)	595(18.4)	1.00
是	397(83.8)	77(16.2)	0.86(0.67~1.12)	0.264
使用甲氨蝶呤[例(构成比,%)]
否	2622(82.4)	559(17.6)	1.00
是	421(78.8)	113(21.2)	1.26(1.00~1.58)	0.047
使用硫唑嘌呤[例(构成比,%)]
否	2964(81.9)	656(18.1)	1.00
是	79(83.2)	16(16.8)	0.92(0.53~1.58)	0.749
使用来氟米特[例(构成比,%)]
否	2747(82.1)	599(17.9)	1.00
是	296(80.2)	73(19.8)	1.13(0.86~1.48)	0.373
使用环孢素A [例(构成比,%)]
否	2973(81.9)	656(18.1)	1.00
是	70(81.4)	16(18.6)	1.04(0.60~1.80)	0.900
使用他克莫司[例(构成比,%)]
否	2945(81.6)	664(18.4)	1.00
是	98(92.5)	8(7.5)	0.36(0.18~0.75)	0.006
使用生物制剂[例(构成比,%)]
否	2791(81.5)	634(18.5)	1.00
是	252(86.9)	38(13.1)	0.66(0.47~0.94)	0.022
使用肿瘤坏死因子α拮抗剂[例(构成比,%)]
否	2859(94.0)	640(95.2)	1.00
是	184(6.0)	32(4.8)	0.78(0.53~1.14)	0.199
使用依那西普[例(构成比,%)]
否	2931(81.8)	652(18.2)	1.00
是	112(84.8)	20(15.2)	0.80(0.50~1.30)	0.373
使用英夫利昔单抗[例(构成比,%)]
否	3005(81.9)	663(18.1)	1.00
是	38(80.9)	9(19.1)	1.07(0.52~2.23)	0.850
使用阿达木单抗[例(构成比,%)]
否	3006(81.8)	669(18.2)	1.00
是	37(92.5)	3(7.5)	0.36(0.11~1.19)	0.093
使用托珠单抗[例(构成比,%)]
否	3012(81.8)	668(18.2)	1.00
是	31(88.6)	4(11.4)	0.58(0.21~1.65)	0.310
使用利妥昔单抗[例(构成比,%)]
否	3013(81.8)	671(18.2)	1.00
是	30(96.8)	1(3.2)	0.15(0.02~1.10)	0.062
白细胞计数[例(构成比,%)]
≥4×10⁹/L	2567(81.3)	589(18.7)	1.00
<4×10⁹/L	461(86.3)	73(13.7)	0.69(0.53~0.90)	0.006
中性粒细胞计数[例(构成比,%)]
≥1.5×10⁹/L	2843(81.9)	629(18.1)	1.00
<1.5×10⁹/L	183(84.3)	34(15.7)	0.84(0.58~1.22)	0.363
淋巴细胞计数[例(构成比,%)]
≥0.5×10⁹/L	2761(81.3)	636(18.7)	1.00
<0.5×10⁹/L	261(90.9)	26(9.1)	0.43(0.29~0.65)	<0.001
血红蛋白[例(构成比,%)]
≥90g/L	2725(81.4)	624(18.6)	1.00
<90g/L	298(88.7)	38(11.3)	0.56(0.39~0.79)	0.001
血小板计数[例(构成比,%)]
<300×10⁹/L	2551(82.7)	534(17.3)	1.00
≥300×10⁹/L	473(78.8)	127(21.2)	1.28(1.03~1.59)	0.025
白蛋白[例(构成比,%)]
≥30g/L	2412(80.9)	569(19.1)	1.00
<30g/L	414(87.3)	60(12.7)	0.61(0.46~0.82)	0.001
谷丙转氨酶[例(构成比,%)]
正常	2579(81.5)	584(18.5)	1.00
升高	414(84.8)	74(15.2)	0.79(0.61~1.03)	0.078
尿素氮[例(构成比,%)]
≤7.1mmol/L	2290(81.7)	514(18.3)	1.00
>7.1mmol/L	442(80.8)	105(19.2)	1.06(0.84~1.34)	0.634
肌酐[例(构成比,%)]
正常	2779(81.8)	619(18.2)	1.00
升高	145(82.9)	30(17.1)	0.93(0.62~1.39)	0.719
血红细胞沉降率[例(构成比,%)]
正常	1321(82.9)	273(17.1)	1.00
升高	1602(81.3)	368(18.7)	1.11(0.94~1.32)	0.230
C-反应蛋白[例(构成比,%)]
≤8mg/L	1308(81.9)	290(18.1)	1.00
>8mg/L	616(78.9)	165(21.1)	1.21(0.98~1.50)	0.083
病种分类[例(构成比,%)]
类风湿关节炎	422(76.2)	132(23.8)	1.00
系统性红斑狼疮	1895(85.0)	334(15.0)	0.56(0.45~0.71)	<0.001
干燥综合征	116(80.0)	29(20.0)	0.80(0.51~1.26)	0.331
系统性硬化	40(71.4)	16(28.6)	1.28(0.69~2.36)	0.431
混合性结缔组织病	41(91.1)	4(8.9)	0.31(0.11~0.89)	0.029
多发性肌炎/皮肌炎	118(86.8)	18(13.2)	0.49(0.29~0.83)	0.008
大动脉炎	27(75.0)	9(25.0)	1.07(0.49~2.32)	0.873
白塞综合征	40(55.6)	32(44.4)	2.56(1.55~4.24)	<0.001
其他血管炎^a	64(77.1)	19(22.9)	0.95(0.55~1.64)	0.852
强直性脊柱炎	255(79.2)	67(20.8)	0.84(0.60~1.17)	0.304
银屑病关节炎	25(67.6)	12(32.4)	1.54(0.75~3.14)	0.241

因素	β值	s $x ˉ$ 值	Wald χ²值	P值	aOR(95%CI)值
年龄
16~40岁					1.00
≥41岁	0.594	0.105	32.156	<0.001	1.81(1.48~2.23)
吸烟≥21支/d
否					1.00
是	0.505	0.189	7.164	0.007	1.66(1.15~2.40)
结核病既往史
无					1.00
有	1.356	0.184	54.207	<0.001	3.88(2.71~5.57)
现用激素剂量
0~29mg/d					1.00
30~59mg/d	-0.216	0.128	2.821	0.093	0.81(0.63~1.04)
≥60mg/d	-0.394	0.182	4.704	0.030	0.67(0.47~0.96)
使用他克莫司
否					1.00
是	-0.702	0.384	3.336	0.068	0.50(0.23~1.05)
使用生物制剂
否					1.00
是	-0.597	0.216	7.674	0.006	0.55(0.36~0.84)
淋巴细胞计数(×10⁹/L)
≥0.5					1.00
<0.5	-0.940	0.236	15.856	<0.001	0.39(0.25~0.62)
白蛋白(g/L)
≥30					1.00
<30	-0.335	0.167	4.023	0.045	0.72(0.52~0.99)
病种分类
类风湿关节炎					1.00
系统性红斑狼疮	-0.284	0.141	4.054	0.044	0.75(0.57~0.99)
干燥综合征	-0.083	0.252	0.110	0.741	0.92(0.56~1.51)
系统性硬化	0.273	0.328	0.694	0.405	1.31(0.69~2.50)
混合性结缔组织病	-0.829	0.552	2.255	0.133	0.44(0.15~1.29)
多发性肌炎/皮肌炎	-0.625	0.312	4.005	0.045	0.54(0.29~0.99)
大动脉炎	0.529	0.442	1.434	0.231	1.70(0.71~4.03)
白塞综合征	0.159	0.317	0.251	<0.001	3.00(1.70~5.28)
其他血管炎^a	1.098	0.289	14.457	0.616	1.17(0.63~2.18)
强直性脊柱炎	0.171	0.201	0.721	0.396	1.19(0.80~1.76)
银屑病关节炎	0.460	0.407	1.277	0.259	1.58(0.71~3.51)

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变量	赋值	变量	赋值
年龄	1=16~40岁,2=≥41岁	淋巴细胞计数	1=≥0.5×10⁹/L,2=<0.5×10⁹/L
吸烟≥21支/d	1=否,2=是	淋巴细胞计数	1=≥0.5×10⁹/L,2=<0.5×10⁹/L
吸烟≥21支/d	1=否,2=是	白蛋白	1=≥30g/L,2=<30g/L
结核病既往史	1=无,2=有	白蛋白	1=≥30g/L,2=<30g/L
结核病既往史	1=无,2=有	病种分类	1=类风湿关节炎,2=系统性红斑狼疮,3=干燥综合征,4=系统性硬化,5=混合性结缔组织病,6=多发性肌炎/皮肌炎,7=大动脉炎,8=白塞综合征,9=其他血管炎^a,10=强直性脊柱炎,11=银屑病关节炎
现用激素剂量	1=0~29mg/d,2=30~59mg/d,3=≥60mg/d
使用他克莫司	1=否,2=是
使用生物制剂	1=否,2=是

Latent tuberculosis infection rate and risk factors in patients with rheumatic diseases: a multi-center, cross-sectional study

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特征	患者数 (例)	结核感染T细胞斑点试验		χ²值	P值
特征	患者数 (例)	阳性(例)	阳性率(%,95%CI)	χ²值	P值
病种分类				79.003	<0.001
类风湿关节炎	554	132	23.8(20.3~27.4)
系统性红斑狼疮	2229	334	15.0(13.5~16.5)
干燥综合征	145	29	20.0(13.4~26.6)
系统性硬化	56	16	28.6(16.4~40.8)
混合性结缔组织病	45	4	8.9(0.2~17.5)
多发性肌炎/皮肌炎	136	18	13.2(7.5~19.0)
大动脉炎	36	9	25.0(10.1~39.9)
白塞综合征	72	32	44.4(32.7~56.2)
其他血管炎^a	83	19	22.9(13.7~32.1)
强直性脊柱炎	322	67	20.8(16.3~25.3)
银屑病关节炎	37	12	32.4(16.6~48.3)
性别				18.213	<0.001
男性	711	168	23.6(20.4~26.6)
女性	3004	504	16.8(15.5~18.1)
年龄组(岁)				67.189	<0.001
16~20	160	13	8.1(3.8~12.4)
21~30	923	109	11.8(9.6~13.8)
31~40	810	140	17.3(14.8~20.0)
41~50	820	162	19.8(17.0~22.5)
51~60	577	143	24.8(21.3~28.3)
61~83	425	105	24.7(20.6~28.8)
合计	3715	672	18.1(16.9~19.3)

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