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北京大学学报（医学版） ›› 2023, Vol. 55 ›› Issue (6): 982-992. doi: 10.19723/j.issn.1671-167X.2023.06.005

• 论著 • 上一篇    下一篇

血脂异常与类风湿关节炎肺间质病变的相关性分析

吴琦1,2,蔡月明1,何娟1,黄文蒂3,王庆文1,*()   

  1. 1. 北京大学深圳医院风湿免疫科, 深圳市炎症与免疫性疾病重点实验室, 广东深圳 518000
    2. 汕头大学医学院, 广东汕头 515000
    3. 北京大学深圳医院呼吸与危重症医学科, 广东深圳 518000
  • 收稿日期:2021-07-26 出版日期:2023-12-18 发布日期:2023-12-11
  • 通讯作者: 王庆文 E-mail:wqw_sw@163.com
  • 基金资助:
    国家自然科学基金(81974253);国家自然科学基金(81901641);广东省自然科学基金面上项目(2019A1515011112);深圳市科创委重点基础研究项目(JCYJ20200109140203849);深圳市卫健委医防融合项目(0102018-2019-YBXM-1499-01-0414);深圳市卫计委学科建设能力提升项目(SZXJ2017046)

Correlation between dyslipidemia and rheumatoid arthritis associated interstitial lung disease

Qi WU1,2,Yue-ming CAI1,Juan HE1,Wen-di HUANG3,Qing-wen WANG1,*()   

  1. 1. Department of Rheumatism and Immunology, Peking University Shenzhen Hospital; Shenzhen Key Laboratory of Immunity and Inflammatory Diseases, Shenzhen 518000, Guangdong, China
    2. Shantou University Medical College, Shantou 515000, Guangdong, China
    3. Department of Pulmonary and Critical Care Medicine, Peking University Shenzhen Hospital Shenzhen, Shenzhen 518000, Guangdong, China
  • Received:2021-07-26 Online:2023-12-18 Published:2023-12-11
  • Contact: Qing-wen WANG E-mail:wqw_sw@163.com
  • Supported by:
    the National Natural Science Foundation of China(81974253);the National Natural Science Foundation of China(81901641);Natural Science Foundation of Guangdong Province(2019A1515011112);Key Project of Basic Research of Shenzhen Science and Technology Innovation Commission(JCYJ20200109140203849);Prevention and Treatment Integration Project of Shenzhen Municipal Health Commission(0102018-2019-YBXM-1499-01-0414);Project of Shenzhen Municipal Health Commission(SZXJ2017046)

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摘要：

目的: 回顾性分析了解血脂异常与类风湿关节炎肺间质病变(rheumatoid arthritis associated interstitial lung disease, RA-ILD)的相关性。方法: 收集2015年1月至2020年7月期间在北京大学深圳医院风湿免疫科住院符合《2010年美国风湿病学会/欧洲风湿病防治联合会类风湿关节炎(rheumatoid arthritis, RA)分类标准》的患者病例资料，按照有无合并肺间质病变(interstitial lung disease, ILD)分组，对一般资料、临床特征及检验检查等数据单因素检验后将差异有意义的因素纳入Logistics多因素回归分析。根据有无血脂异常分组，分析血脂异常与RA-ILD的发生率、发生的中位时间及临床表现等相关性。结果: 共纳入737例RA患者，其中282例(38.26%)发生ILD，从开始出现RA相关的临床症状至发生ILD的中位时间为13(95%CI 11.33~14.67)年。多因素Logistic回归分析结果显示：低密度脂蛋白胆固醇(low-density lipoprotein cholesterol, LDL-C)是RA-ILD可能的危险因素(OR 1.452，95%CI 1.099~1.918，P=0.009)，高密度脂蛋白胆固醇(high-density lipoprotein cholesterol，HDL-C)是RA-ILD可能的保护因素(OR 0.056，95%CI 0.025~0.125，P < 0.001)。在737例RA患者中，LDL-C升高及HDL-C降低的RA患者ILD的发生率均分别高于LDL-C正常及HDL-C正常的患者(分别为57.45% vs. 36.96%，P < 0.001；47.33% vs. 33.81%，P < 0.001)。HDL-C降低的RA患者出现ILD的中位时间明显短于HDL-C正常的RA患者[10.0(95%CI 9.33~10.67)年vs. 17.0(95%CI 14.58~19.42)年，P < 0.001]。RA患者的HDL-C水平与疾病活动呈负相关。RA-ILD患者中，HDL-C降低的患者胸部HRCT出现寻常型间质性肺炎(usual interstitial pneumonia, UIP)的比例高于HDL-C正常的患者(60.00% vs. 53.29%，P=0.002)，LDL-C升高的RA-ILD患者出现用力肺活量(forced vital capacity，FVC)下降的发生率高于LDL-C正常的RA-ILD患者(50.00% vs.21.52%，P=0.015)，HDL-C降低的RA-ILD患者出现FVC及一氧化碳弥散量(diffusing capacity of the lung for carbon monoxide, DLCO)下降的发生率高于HDL-C正常的RA-ILD患者(分别为26.92% vs.16.18%，P=0.003；80.76% vs. 50.00%，P=0.010)。结论: LDL-C可能是RA-ILD的潜在危险因素；HDL-C可能是RA-ILD的潜在保护因素；HDL-C水平与RA病情活动呈负相关；HDL-C降低的RA患者出现ILD的时间更早。

关键词: 类风湿关节炎, 肺间质病变, 血脂异常

Abstract:

Objective: To study the correlation between dyslipidemia and rheumatoid arthritis associa-ted interstitial lung disease (RA-ILD) by retrospective analysis of the clinical data. Methods: The clinical data of patients with rheumatoid arthritis (RA), who were hospitalized in the Department of Rheumatism and Immunology of Peking University Shenzhen Hospital from January 2015 to July 2020 and fulfilled the criteria of the 2010 Rheumatoid Arthritis Classification Criteria established by American College of Rheumatology/European League Against Rheumatism collaborative initiative, were collected and analyzed. Results: There were 737 RA patients included, of whom 282(38.26%)were with interstitial lung disease (ILD). The median time from the onset of the first RA-related clinical symptoms to the onset of ILD was 13 years (95%CI 11.33-14.67). By multivariate Logistic regression analysis, we found that low-density lipoprotein cholesterol (LDL-C) was an independent risk factor for RA-ILD (OR 1.452, 95%CI 1.099-1.918, P=0.009), whereas high-density lipoprotein cholesterol (HDL-C) was a protective factor for RA-ILD (OR 0.056, 95%CI 0.025-0.125, P < 0.001). The RA patients with high LDL-C or low HDL-C had higher incidence of ILD than that of the RA patients with normal LDL-C or HDL-C(57.45% vs. 36.96%, P < 0.001; 47.33% vs. 33.81%, P < 0.001, respectively). The median time of ILD onset in the RA patients with low HDL-C was shorter than that of the RA patients with normal HDL-C [10.0(95%CI 9.33-10.67)years vs.17.0 (95%CI 14.58-19.42) years, P < 0.001]. HDL-C level was negatively correlated with disease activity. Among the RA-ILD patients, the patients with low HDL-C had higher percentage of usual interstitial pneumonia (UIP) then that of the patients with normal HDL-C (60.00% vs. 53.29%, P=0.002). The RA-ILD patients with high LDL-C had higher incidence rate of decrease in forced vital capacity (FVC) than that of the RA-ILD patients with normal LDL-C (50.00% vs. 21.52%, P=0.015). The RA-ILD patients with low HDL-C had higher incidence rate of decrease in FVC (26.92% vs. 16.18%, P=0.003) and carbon monoxide diffusion (80.76% vs. 50.00%, P=0.010) than that of RA-ILD patients with normal HDL-C. Conclusion: LDL-C was possibly a potential independent risk factor for RA-ILD. HDL-C was possibly a potential protective factor for RA-ILD. HDL-C level was negatively correlated with disease activity of RA. The median time of ILD onset in the RA patients with low HDL-C was significantly shorter than that of the RA patients with normal HDL-C.

Key words: Rheumatoid arthritis, Interstitial lung disease, Dyslipidemia

中图分类号: 

  • R593.2

表1

RA-ILD组与RA-nILD组临床合并症比较[n(%)]"

Clinical complication RA-ILD (n =282) RA-nILD (n =455) χ2 P
PAH 16 (5.67) 15 (3.30) 3.079a 0.079
Arteriosclerosis 84 (29.79) 85 (18.68) 12.151a < 0.001*
Valve disorder 48 (17.02) 33 (7.25) 17.434a < 0.001*
Arrhythmia 56 (19.86) 48 (10.55) 12.579a < 0.001*
Coronary heart disease 4 (1.42) 4 (0.88) 0.472b 0.492
Diabetes 36 (12.77) 21 (4.62) 16.208a < 0.001*
Hypertension 59 (20.92) 55 (12.09) 10.391a 0.001*
Pericardial efusion 3 (1.06) 1 (0.22) 2.303b 0.129
Cardiomyopathy 1 (0.35) 1 (0.22) 0.116b 0.733
Dyslipidemia 150 (53.19) 148 (32.53) 30.866a < 0.001*
  Hypertriglyceridemia 25 (8.87) 11 (2.42) 15.578a < 0.001*
  Hypercholesterolemia 17 (6.03) 16 (3.52) 2.568a 0.109
  High LDL-C 27 (9.57) 20 (4.40) 7.821a 0.005*
  Low HDL-C 15 (40.78) 128 (28.13) 12.603a < 0.001*

表2

RA-ILD组和RA-nILD组实验室检验指标比较"

Laboratory test indicator RA-ILD RA-nILD Z/t/χ2 P
n Data n Data
RF/(IU/mL), M (P25, P75) 282 211.52 (26.65，213.33) 455 149.41 (20.30，164.50) 3.474a 0.010*
ESR/(mm/h), M (P25, P75) 282 35.00 (19.00，56.00) 455 28.00 (14.00，46.00) -3.646a < 0.001*
hs-CRP/(mg/L), M (P25, P75) 281 24.39 (3.36，29.72) 455 14.7 (1.41，16.84) -5.188a < 0.001*
Ferritin/(μg/L), M (P25, P75) 62 193.64 (58.25，383.05) 100 79.65 (20.98，197.05) -3.601a < 0.001*
KL-6/(U/mL), M (P25, P75) 72 310.57 (155.00，327.00) 114 175.1 (129.00，244.75) -3.3474a 0.001*
Interleukin-6/(ng/L), M (P25, P75) 48 14.48 (3.29，34.57) 90 10.7 (3.50, 34.25) -0.020a 0.984
TNF-α, M (P25, P75) 20 10.25 (8.29，15.73) 33 9.5 (7.62，13.90) -0.642a 0.521
Uric acid/(μmol/L), $\bar x \pm s$ 282 304.07±95.16 455 286.86±86.24 2.359b 0.019*
FBG/(mmol/L), $\bar x \pm s$ 282 4.92±1.01 455 4.65±0.80 4.144b < 0.001*
TG/(mmol/L), $\bar x \pm s$ 282 1.30±0.74 455 1.08±0.66 4.065b < 0.001*
TC/(mmol/L), $\bar x \pm s$ 282 4.51±1.02 455 4.31±0.93 2.678b 0.008*
HDL-C/(mmol/L), $\bar x \pm s$ 282 1.03±0.19 455 1.24±0.53 -4.853b < 0.001*
LDL-C/(mmol/L), $\bar x \pm s$ 282 2.99±0.73 455 2.74±0.69 4.534b < 0.001*
Anti-CCP≥3 times, n(%) 282 230 (81.56) 455 339 (74.51) 4.924c 0.026*

表3

RA-ILD相关因素Logistic回归分析"

Factor P OR 95% CI
Age of onset < 0.001* 1.051 1.037-1.065
Visiting ages < 0.001* 1.064 1.049-1.079
Male 0.008* 1.720 1.154-2.565
Smoke 0.001* 2.365 1.397-4.004
Disease duration < 0.001* 1.096 1.066-1.128
DAS28-ESR 0.032* 1.271 1.021-1.583
RF/(IU/mL) 0.364 1.000 1.000-1.001
Anti-CCP≥3 times 0.039* 1.524 1.022-2.273
KL-6>300 U/mL 0.030* 2.570 1.093-6.041
Ferritin/(μg/L) 0.308 1.001 0.999-1.003
TG/(mmol/L) 0.344 1.191 0.829-1.710
TC/(mmol/L) 0.300 0.653 0.292-1.461
HDL-C/(mmol/L) < 0.001* 0.056 0.025-0.125
LDL-C/(mmol/L) 0.009* 1.452 1.099-1.918
Uric acid/(μmol/L) 0.791 1.001 0.996-1.005
Arteriosclerosis 0.584 0.878 0.551-1.399
Valve disorder 0.141 1.522 0.870-2.663
Coronary heart disease 0.715 0.733 0.138-3.882
Hypertension 0.399 0.793 0.462-1.360
Arrhythmia 0.137 1.453 0.888-2.375
Diabetes 0.238 1.476 0.773-2.820
Use of glucocorticoid 0.179 2.842 0.620-3.015

表4

有无血脂异常的RA患者合并症比较[n(%)]"

Complication Normal LDL-C
(n=690)		 High LDL-C
(n=47)		 χ2/Fisher P Normal HDL-C
(n =494)		 Low HDL-C
(n =243)		 χ2/Fisher P
ILD 255 (36.96) 27 (57.45) 12.806a < 0.001* 167 (33.81) 115 (47.33) 12.603a < 0.001*
PAH 26 (3.77) 5 (10.64) 2.173a 0.140 20 (4.05) 12 (4.94) 0.318a 0.573
Coronary heart disease 7 (1.01) 1 (2.13) 0.063b 0.802 1 (0.20) 7 (2.88) 10.881b 0.001*
Hypertension 97 (14.06) 17 (36.17) 5.825a 0.016* 68 (13.77) 46 (18.93) 3.323a 0.068
Arteriosclerosis 146 (21.16) 23 (48.94) 4.244a 0.039* 103 (20.85) 66 (27.16) 3.674a 0.055
Valve disorder 74 (10.72) 7 (14.89) 1.159a 0.282 50 (10.12) 31 (12.76) 1.150a 0.284
Arrhythmia 90 (13.04) 14 (29.79) 3.608a 0.057 66 (13.36) 38 (15.64) 0.739a 0.390
Cardiomyopathy 2 (0.29) 0 (0.00) 0.198c 0.656 1 (0.20) 1 (0.41) 0.244b 0.622
Pericardial efusion 4 (0.58) 0 (0.00) 0.397c 0.529 3 (0.61) 1 (0.41) 0.116b 0.733
Diabetes 49 (7.10) 8 (17.02) 1.927a 0.165 24 (4.86) 33 (13.58) 17.364c < 0.001*

图1

有无HDL-C降低RA患者出现ILD的时间比较"

表5

LDL-C及HDL-C在性别、吸烟分层后RA-ILD组及RA-nILD组血脂比较"

Stratification LDL-C/(mmol/L), $\bar x \pm s$ HDL-C/(mmol/L), $\bar x \pm s$
RA-ILD RA-nILD t P RA-ILD RA-nILD t P
Male (n=144) 2.95±0.69 2.90±0.64 0.382 0.703 0.98±0.22 1.07±0.33 -2.011 0.046*
Female (n =593) 3.01±0.75 2.71±0.72 4.599 < 0.001* 1.11±0.20 1.26±0.54 4.599 < 0.001*
Smoker (n =91) 2.92±0.65 2.84±0.51 2.038 0.502 0.99±0.23 1.04±0.32 -3.327 0.001*
Nonsmoker (n =646) 3.01±0.75 2.73±0.71 6.099 < 0.001* 1.09±0.21 1.25±0.54 -5.938 < 0.001*

表6

LDL-C及HDL-C与其他因素的相关性分析"

Items LDL-C HDL-C
r P r P
DAS28-ESR
  RA 0.021 0.590 -0.316 < 0.001*
  RA-ILD 0.089 0.151 -0.451 0.001*
  RA-nILD 0.007 0.883 -0.156 0.002
ESR
  RA -0.056 0.151 -0.149 < 0.001
  RA-ILD -0.146 0.019 -0.192 0.002
  RA-nILD -0.054 0.291 -0.093 0.068
hs-CRP
  RA -0.108 0.006* -0.203 < 0.001*
  RA-ILD -0.197 0.010 -0.247 < 0.001*
  RA-nILD -0.062 0.222 -0.165 0.001
RF
  RA 0.011 0.772 -0.104 0.008
  RA-ILD 0.017 0.781 -0.154 0.013
  RA-nILD -0.045 0.383 -0.059 0.247
Anti-CCP
  RA -0.014 0.350 -0.092 0.074
  RA-ILD -0.010 0.998 -0.182 0.004*
  RA-nILD -0.052 0.319 0.011 0.838
KL-6
  RA 0.272 0.001* -0.098 0.239
  RA-ILD 0.312 0.004* -0.034 0.792
  RA-nILD 0.260 0.042 -0.055 0.622
Age
  RA 0.156 < 0.001* -0.143 < 0.001*
  RA-ILD 0.141 0.023* -0.054 0.381
  RA-nILD 0.155 < 0.001* -0.082 0.107

表7

有无血脂异常的RA-ILD患者胸部HRCT表现比较[n(%)]"

Chest HRCT Normal LDL-C
(n =255)		 High LDL-C
(n=27)		 χ2 P Normal HDL-C
(n =167)		 Low HDL-C
(n=115)		 χ2 P
UIP 145 (56.86) 13 (48.15) 0.753a 0.386 89 (53.29) 69 (60.00) 9.810a 0.002*
NSIP 77 (30.20) 10 (37.04) 0.536a 0.464 57 (34.13) 30 (26.09) 2.066a 0.151
OP 18 (7.06) 2 (7.41) 0.005b 0.947 13 (7.78) 7 (6.09) 0.380a 0.845
DIP 9 (3.53) 1 (3.70) 0.002b 0.963 5 (2.99) 5 (4.35) 0.365a 0.546
LIP 6 (2.35) 1 (3.70) 0.184b 0.668 3 (1.80) 4 (3.48) 1.868b 0.172

表8

有无血脂异常的RA及RA-ILD患者肺功能比较[n(%)]"

Items Normal LDL-C
(n =79)		 High LDL-C
(n =15)		 χ2/Fisher P Normal HDL-C
(n =68)		 Low HDL-C
(n =26)		 χ2/Fisher P
VC decreased
  RA 23 (29.11) 6 (40.00) 1.047a 0.306 18 (26.47) 12 (46.15) 2.197a 0.138
  RA-ILD 16 (20.25) 5 (33.33) 1.901a 0.168 11 (16.18) 11 (42.31) 1.901a 0.051
  RA-nILD 7 (8.86) 1 (6.67) 0.074b 0.786 7 (10.29) 1 (3.85) 0.074b 0.562
FVC decreased
  RA 22 (27.85) 8 (53.33) 4.670a 0.031* 14 (25.00) 7 (26.92) 5.227a 0.022*
  RA-ILD 17 (21.52) 7 (46.67) 5.973a 0.015* 8 (16.18) 7 (26.92) 8.686a 0.003*
  RA-nILD 4 (5.06) 1 (6.67) 0.010b 0.921 6 (8.82) 0 (0.00) 1.857c 0.173
FEV1 decreased
  RA 14 (17.72) 7 (46.67) 0.163a 0.687 16 (23.53) 4 (15.38) 0.487b 0.485
  RA-ILD 8 (10.13) 7 (46.67) 1.418a 0.234 11 (16.18) 3 (11.54) 0.589b 0.443
  RA-nILD 6 (7.59) 0 (0.00) 1.857c 0.173 5 (7.35) 1 (3.85) 0.010b 0.921
FVC/FEV1 decreased
  RA 2 (2.53) 0 (0.00) 0.562c 0.567 2 (2.94) 0 (0.00) 0.362c 0.547
  RA-ILD 1 (1.27) 0 (0.00) 0.278c 0.573 1 (1.47) 0 (0.00) 0.178c 0.673
  RA-nILD 1 (1.27) 0 (0.00) 0.193c 0.672 1 (1.47) 0 (0.00) 0.189c 0.664
TCL decreased
  RA 20 (25.32) 5 (33.33) 0.654a 0.419 16 (23.53) 10 (38.46) 1.293a 0.255
  RA-ILD 16 (20.25) 4 (26.67) 0.578b 0.447 12 (17.65) 9 (34.62) 1.108a 0.293
  RA-nILD 4 (5.06) 1 (6.67) 0.101b 0.750 4 (5.88) 1 (3.85) 0.002b 0.961
RV decreased
  RA 17 (21.52) 2 (13.33) 0.383b 0.536 14 (20.59) 6 (23.08) 0.001a 0.981
  RA-ILD 13 (16.46) 1 (6.67) 0.844b 0.358 11 (16.18) 4 (15.38) 0.440b 0.507
  RA-nILD 4 (5.06) 1 (6.67) 0.101b 0.750 3 (4.41) 2 (7.69) 1.719b 0.190
DLCO decreased
  RA 59 (74.68) 12 (80.00) 0.801a 0.371 46 (67.65) 24 (92.30) 5.882a 0.015*
  RA-ILD 46 (58.23) 10 (66.67) 2.309a 0.129 34 (50.00) 21 (80.76) 6.707a 0.010*
  RA-nILD 13 (16.46) 2 (13.33) 0.115b 0.735 12 (17.65) 3 (11.54) 0.014b 0.907

表9

治疗药物对血脂异常的影响分析[n(%)]"

Items Normal LDL-C
(n =690)		 High LDL-C
(n =47)		 χ2/Fisher P Normal HDL-C
(n =494)		 Low HDL-C
(n =243)		 χ2/Fisher P
NSAIDs 0.011a 0.918 0.043a 0.837
  Yes 569 (82.46) 37 (78.72) 403 (81.58) 203 (83.54)
  No 121 (17.54) 10 (21.28) 91 (18.42) 40 (16.46)
Glucocorticoid 0.056a 0.814 1.816a 0.178
  Yes 562 (81.45) 42 (89.36) 404 (81.78) 200 (82.31)
  No 128 (18.55) 5 (10.64) 90 (18.22) 43 (17.69)
Methotrexate 1.107a 0.293 0.009a 0.923
  Yes 534 (77.39) 37 (78.72) 386 (78.13) 185 (76.13)
  No 156 (22.61) 10 (21.28) 108 (21.87) 58 (23.87)
Leflunomide 0.116a 0.733 3.166a 0.075
  Yes 310 (44.93) 14 (30.00) 227 (45.95) 97 (39.92)
  No 380 (55.07) 33 (70.00) 267 (44.05) 146 (60.08)
Cyclophosphamide 1.068c 0.301 0.040a 0.842
  Yes 17 (2.46) 0 (0.00) 11 (2.22) 6 (2.47)
  No 673 (97.54) 47 (100.00) 483 (97.78) 237 (97.53)
Hydroxychloroquine 0.008a 0.927 1.536a 0.215
  Yes 156 (22.61) 8 (17.02) 120 (24.29) 44 (18.11)
  No 534 (77.39) 39 (82.98) 374 (75.71) 199 (81.89)
Total glucosides of
paeonia		 0.002a 0.965 2.274a 0.132
  Yes 232 (33.63) 15 (31.91) 170 (34.41) 77 (31.69)
  No 458 (66.37) 32 (68.09) 324 (65.59) 166 (68.31)
Tripterygium glycosides 1.374a 0.241 0.013a 0.91
  Yes 138 (20.00) 17 (36.17) 96 (19.43) 59 (24.28)
  No 552 (80.00) 30 (63.83) 398 (80.57) 184 (75.72)
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