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Journal of Peking University (Health Sciences) ›› 2023, Vol. 55 ›› Issue (6): 982-992. doi: 10.19723/j.issn.1671-167X.2023.06.005

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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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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

CLC Number: 

  • R593.2

Table 1

Comparison of clinical complications between RA-ILD and RA-nILD [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*

Table 2

Comparison of laboratory test indicators between RA-ILD and RA-nILD"

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*

Table 3

Logistic regression analysis of related factors for RA-ILD"

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

Table 4

Comparison of complications between RA patients with and without dyslipidemia [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*

Figure 1

Comparison of onset time for RA-ILD between patients with low HDL-C and normal HDL-C RA, rheumatoid arthritis; HDL-C, high-density lipoprotein cholesterol; ILD, interstitial lung disease."

Table 5

Comparison of LDL-C or HDL-C between RA-ILD and RA-nILD after stratification by gender and smoking"

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*

Table 6

Correlation analysis of LDL-C and HDL-C with other factors"

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

Table 7

Comparison of chest HRCT of RA-ILD patients with or without dyslipidemia [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

Table 8

Comparison of pulmonary function of RA and RA-ILD patients with or without dyslipidemia [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

Table 9

Analysis of treatment to dyslipidemia impact [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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