IJCA-17987; No of Pages 3 International Journal of Cardiology xxx (2014) xxx–xxx

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Letter to the Editor

A nationwide population-based retrospective cohort study: Increased risk of acute myocardial infarction in systemic lupus erythematous patients Chi-Hung Chou a,1, Cheng-Li Lin b, Shih-Ni Chang b,c, Ming-Chia Lin d,1, Chia-Hung Kao e,f,⁎, Yi-Jia Huang d a

Division of Cardiology, Department of Internal Medicine, Changhua Christian Hospital, Yunlin Branch, Yunlin, Taiwan Management Office for Health Data, China Medical University Hospital, Taichung, Taiwan c Department of Medical Research, Taichung Veterans General Hospital, Taiwan d Department of Nuclear Medicine, E-DA Hospital, Kaohsiung, Taiwan e Graduate Institute of Clinical Medical Science and School of Medicine, College of Medicine, China Medical University, Taichung, Taiwan f Department of Nuclear Medicine and PET Center, China Medical University Hospital, Taichung, Taiwan b

a r t i c l e

i n f o

Article history: Received 28 March 2014 Accepted 4 April 2014 Available online xxxx Keywords: Cohort study Acute myocardial infarction (AMI) Systemic lupus erythematous (SLE)

Acute myocardial infarction (AMI) includes any condition that suddenly blocks blood flow to the heart, necrotizing a substantial portion of the myocardium. Male sex, hypertension, smoking, hyperlipidemia, and diabetes mellitus are known cardiovascular (CV) risk factors [1,2]. Systemic lupus erythematous (SLE) is a systemic autoimmune disease that often affects young women. A nationwide study in Sweden considered whether hospitalization for immunemediated diseases such as SLE and rheumatoid arthritis was predictive of subsequent hospitalization for coronary artery disease [3]. CV disease is a primary cause of both morbidity and premature mortality among women with SLE [4–7]. The pathogenesis of premature CV disease in women with lupus is likely multifactorial, related to underlying vascular inflammation and arterial wall injuries, the adverse effects of corticosteroids, the high prevalence of renal disease and hypertension, and increased thrombosis in the setting of antiphospholipid antibodies. This study uses a large cohort representing 99% of Taiwan's population to analyze the incidence

⁎ Corresponding author at: Graduate Institute of Clinical Medical Science and School of Medicine, College of Medicine, China Medical University, No. 2, Yuh-Der Road, Taichung 40447, Taiwan. Tel.: +886 4 22052121x7412; fax: +886 4 22336174. E-mail address: [email protected] (C.-H. Kao). 1 Ming-Chia Lin and Chi-Hung Chou contributed equally to this work.

of AMI in disabled SLE patients. The results may guide future care of SLE patients and AMI prevention. This research used the Taiwan National Health Insurance Research Database (NHIRD) claim data to identify 10,954 patients diagnosed with SLE between 1998 and 2008 and 43,816 comparison patients. The risk of SLE patients developing AMI was measured using a Cox proportional hazard model. The SLE cohort included 10,954 patients and the comparison cohort included 43,816 patients of almost the same average age (39.5 y vs 39.77, p = 0.23) and sex ratio (male: 11.7%, p = 0.99). The proportion of AMI associated with diabetes, hypertension, or hyperlipidemia comorbidities in the SLE cohort was much higher than that in the comparison cohort (p b 0.0001). The incidence of AMI development in the SLE cohort was 12.7 per 10,000 person-years and was 2.66 times higher than that in the comparison cohort (Table 1). Fig. 1 shows the Kaplan–Meier estimated cumulative incidence curves for the two study cohorts and indicates that the SLE cohort incidence curve is significantly greater than that of the comparison cohort (log-rank test, p b 0.001). After adjusting for potential confounding factors, the SLE cohort was 2.74 times more likely to develop AMI than the comparison cohort (HR = 2.74, 95%; CI =2.09–3.06). Table 1 also shows the demographic-specific and comorbidityspecific incidence of developing AMI for the two cohorts. Relative to the comparison cohort, younger SLE patients had the highest risk of developing AMI (b 34 y, HR = 12.9; 35–49 y, HR = 2.78; 50–64 y, HR = 2.14; ≥ 65 y, HR = 2.14). Women and men in the SLE cohort were more likely to develop AMI than those in the comparison cohort (female, HR = 3.36; male, HR = 2.01). In Table 2, we stratified patients according to comorbidities. A lack of hypertension (HR = 2.93, 95% CI = 1.86–4.63), diabetes (HR = 3.11, 95% CI = 2.23–4.33), hyperlipidemia (HR = 2.81, 95% CI = 2.07–3.80), COPD (HR = 2.74, 95% CI = 2.05–3.65), and proteinuria (HR = 2.69, 95% CI = 2.05–3.54) was significantly associated with an increased risk of AMI. However, the risk of AMI was significantly elevated in SLE patients who exhibited CVA (HR = 2.67, 95% CI = 1.51–4.74) or ESRD (HR = 4.44, 95% CI = 1.09–18.1). Our study showed a significantly higher frequency of hypertension, diabetes mellitus, hyperlipidemia, CVA, COPD, ESRD, and proteinuria

http://dx.doi.org/10.1016/j.ijcard.2014.04.086 0167-5273/© 2014 Elsevier Ireland Ltd. All rights reserved.

Please cite this article as: Chou C-H, et al, A nationwide population-based retrospective cohort study: Increased risk of acute myocardial infarction in systemic lupus erythema..., Int J Cardiol (2014), http://dx.doi.org/10.1016/j.ijcard.2014.04.086

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C.-H. Chou et al. / International Journal of Cardiology xxx (2014) xxx–xxx

Table 1 Comparison of incidence and hazard ratio of AMI stratified by sex, and age between with and without systemic lupus erythematosus patients. Variables

Systemic lupus erythematosus No

All Sex Female Male Stratify age ≤34 35–49 50–64 65+

IRR⁎ (95% CI)

Adjusted HR† (95% CI)

Yes Event

PY

Rate#

4.78

95

74,712

12.7

2.66 (2.51, 2.83)⁎⁎⁎

2.74 (2.09, 3.60)⁎⁎⁎

278,771 35,347

3.19 17.3

65 30

66,829 7883

9.73 38.1

3.05 (2.86, 3.25)⁎⁎⁎ 2.21 (1.87, 2.60)⁎⁎⁎

3.36 (2.40, 4.71)⁎⁎⁎ 2.01 (1.26, 3.20)⁎⁎

139,618 110,162 44,725 19,613

0.14 1.72 11.0 40.8

16 21 27 31

35,132 26,173 9858 3548

4.55 8.02 27.4 87.4

31.8 (27.6, 36.6)⁎⁎⁎ 4.65 (1.19, 5.16)⁎⁎⁎ 2.50 (2.15, 2.90)⁎⁎⁎ 2.14 (1.76, 2.61)⁎⁎⁎

12.9 (2.62, 63.1)⁎⁎ 2.78 (1.41, 5.47)⁎⁎ 2.14 (1.29, 3.55)⁎⁎ 2.14 (1.41, 3.26)⁎⁎⁎

Event

PY

150

314,118

89 61 2 19 49 80

#

Rate

Rate#, incidence rate, per 1000 person-years; IRR⁎, incidence rate ratio. Adjusted HR†: multivariable analysis including age, sex, hypertension, diabetes, hyperlipidemia, CVA, COPD, ESRD and proteinuria. ⁎⁎ p b 0.01. ⁎⁎⁎ p b 0.001.

among SLE patients compared with non-SLE patients. Asians with SLE exhibited increased rates of renal involvement, and CV involvement was a leading cause of death [8]. Wells and Ward observed that nephritis was associated with 2.8-fold increased risk of AMI among SLE patients [9]. It is necessary to do appropriate interventions with these patients to reduce CV risk and improve longevity and quality of life. The study has certain limitations. First, crucial data were missing from the NHIRD regarding major risk factors of AMI such as smoking habits, body mass index, socioeconomic status, and family history of systemic diseases. Second, because all beneficiaries listed on the NHIRD are protected by anonymity, we could not obtain individual clinical (blood pressure), imaging, pathologic, or laboratory data (including lipid profile, fasting blood glucose, inflammatory markers such as CRP or ESR, and SLE disease activity index) for each study participant. Third, we were unable to contact the patients to inquire on the use of their most common non-steroidal anti-inflammatory drugs. Our findings indicate that SLE patients exhibit an increased risk of AMI. Identifying subgroups that exhibit various risk levels would facilitate evaluating prognoses. To conclude, SLE patients exhibit a higher risk of AMI compared with the general population.

References [1] Pencina MJ, D'Agostino Sr RB, Larson MG, et al. Predicting the 30-year risk of cardiovascular disease: the Framingham Heart Study. Circulation 2009;119:3078–84. [2] Greenland P, Alpert JS, Beller GA, et al. 2010 ACCF/AHA guideline for assessment of cardiovascular risk in asymptomatic adults: a report of the American College of Cardiology Foundation/American Heart Association Task Force on Practice Guidelines. J Am Coll Cardiol 2010;56:e50-103. [3] Zoller B, Li X, Sundquist J, et al. Risk of subsequent coronary heart disease in patients hospitalized for immune-mediated diseases: a nationwide follow-up study from Sweden. PLoS One 2012;7:e33442. [4] Petn M, Perez-Gutthann S, Spence D, et al. Risk factors for coronary artery disease in patients with systemic lupus erythematosus. Am J Med 1992;93:513–9. [5] Urowitz MB, Bookman AM, Koehler BE, et al. The bimodal mortality pattern of systemic lupus erythematosus. Am J Med 1976;60:221–5. [6] Tsakraklides VG, Blieden LC, Edwards JE. Coronary atherosclerosis and myocardial infarction associated with systemic lupus erythematosus. Am Heart J 1974;87:637–41. [7] Jensen G, Sigurd B. Systemic lupus erythematosus and acute myocardial infarction. Chest 1973;64:653–4. [8] Jakes RW, Bae SC, Louthrenoo W, et al. Systematic review of the epidemiology of systemic lupus erythematosus in the Asia-Pacific region: prevalence, incidence, clinical features, and mortality. Arthritis Care Res 2012;64:159–68. [9] Wells DK, Ward MM. Nephritis and the risk of acute myocardial infarction in patients with systemic lupus erythematosus. Clin Exp Rheumatol 2010;28:223–9.

Fig. 1. Cummulative incidence of acute myocardial infarction compared between with and without systemic lupus erythematosus cohorts.

Please cite this article as: Chou C-H, et al, A nationwide population-based retrospective cohort study: Increased risk of acute myocardial infarction in systemic lupus erythema..., Int J Cardiol (2014), http://dx.doi.org/10.1016/j.ijcard.2014.04.086

C.-H. Chou et al. / International Journal of Cardiology xxx (2014) xxx–xxx

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Table 2 Comparison of incidence and hazard ratio of AMI stratified by comorbidities between with and without systemic lupus erythematosus patients. Variables

Systemic lupus erythematosus No

Adjusted HR† (95% CI)

Yes PY

Rate

Event

PY

Rate#

53 97

290,204 23,914

1.83 40.6

33 62

59,048 15,663

5.59 39.6

3.06 (2.86, 3.28)⁎⁎⁎ 0.98 (0.83, 1.14)

2.93 (1.86, 4.63)⁎⁎⁎ 2.07 (1.45, 2.95)⁎⁎⁎

86 64

299,805 14,314

2.87 44.7

75 20

71,147 3564

10.5 56.1

3.67 (3.46, 3.91)⁎⁎⁎ 1.26 (0.97, 1.63)

3.11 (2.23, 4.33)⁎⁎⁎ 1.56 (0.92, 2.64)

112 38

307,423 6696

3.64 56.8

76 19

70,015 4697

10.9 40.5

2.98 (2.80, 3.17)⁎⁎⁎ 0.71 (0.53, 0.95)⁎

2.81 (2.07, 3.80)⁎⁎⁎ 1.44 (0.75, 2.77)

114 36

305,101 9018

3.74 39.9

73 22

70,194 4518

10.4 48.7

2.78 (2.62, 2.96)⁎⁎⁎ 1.22 (0.95, 1.57)

2.60 (1.90, 3.55)⁎⁎⁎ 2.67 (1.51, 4.74)⁎⁎⁎

134 16

309,504 4615

4.33 34.7

85 10

71,986 2726

11.8 36.7

2.73 (2.57, 2.90)⁎⁎⁎ 1.06 (0.75, 1.50)

2.74 (2.05, 3.65)⁎⁎⁎ 1.85 (0.79, 4.38)

146 4

312,519 1599

4.67 25.0

83 12

70,721 3991

11.7 30.1

2.51 (2.36, 2.67)⁎⁎⁎ 1.20 (0.75, 1.94)

2.57 (1.94, 3.41)⁎⁎⁎ 4.44 (1.09, 18.1)⁎⁎⁎

150 0

313,959 160

4.78 0.00

87 8

71,691 3020

12.1 26.5

2.54 (2.39, 2.70)⁎⁎⁎ –

2.69 (2.05, 3.54)⁎⁎⁎ –

Event Hypertension No Yes Diabetes No Yes Hyperlipidemia No Yes CVA No Yes COPD No Yes ESRD No Yes Proteinuria No Yes

IRR⁎ (95% CI)

#

Rate#, incidence rate, per 1000 person-years; IRR⁎, incidence rate ratio. Adjusted HR†: multivariable analysis including age, sex, hypertension, diabetes, hyperlipidemia, CVA, COPD, ESRD and proteinuria. ⁎ p b 0.05. ⁎⁎⁎ p b 0.001.

Please cite this article as: Chou C-H, et al, A nationwide population-based retrospective cohort study: Increased risk of acute myocardial infarction in systemic lupus erythema..., Int J Cardiol (2014), http://dx.doi.org/10.1016/j.ijcard.2014.04.086

A nationwide population-based retrospective cohort study: increased risk of acute myocardial infarction in systemic lupus erythematous patients.

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