Prevalence and Correlates of Accelerated Atherosclerosis in Systemic Lupus Erythematosus
Mary J. Roman, M.D., Beth-Ann Shanker, A.B., Adrienne Davis, A.B., Michael D. Lockshin, M.D., Lisa Sammaritano, M.D., Ronit Simantov, M.D., Mary K. Crow, M.D., Joseph E. Schwartz, Ph.D., Stephen A. Paget, M.D., Richard B. Devereux, M.D., and Jane E. Salmon, M.D.
Background Although systemic lupus erythematosus is associatedwith premature myocardial infarction, the prevalence of underlyingatherosclerosis and its relation to traditional risk factorsfor cardiovascular disease and lupus-related factors have notbeen examined in a case–control study.
Methods In 197 patients with lupus and 197 matched controls,we performed carotid ultrasonography, echocardiography, andan assessment for risk factors for cardiovascular disease. Thepatients were also evaluated with respect to their clinicaland serologic features, inflammatory mediators, and diseasetreatment.
Results The risk factors for cardiovascular disease were similaramong patients and controls. Atherosclerosis (carotid plaque)was more prevalent among patients than the controls (37.1 percentvs. 15.2 percent, P<0.001). In multivariate analysis, onlyolder age, the presence of systemic lupus erythematosus (oddsratio, 4.8; 95 percent confidence interval, 2.6 to 8.7), anda higher serum cholesterol level were independently relatedto the presence of plaque. As compared with patients withoutplaque, patients with plaque were older, had a longer durationof disease and more disease-related damage, and were less likelyto have multiple autoantibodies or to have been treated withprednisone, cyclophosphamide, or hydroxychloroquine. In multivariateanalyses including patients with lupus, independent predictorsof plaque were a longer duration of disease, a higher damage-indexscore, a lower incidence of the use of cyclophosphamide, andthe absence of anti-Smith antibodies.
Conclusions Atherosclerosis occurs prematurely in patients withsystemic lupus erythematosus and is independent of traditionalrisk factors for cardiovascular disease. The clinical profileof patients with lupus and atherosclerosis suggests a role fordisease-related factors in atherogenesis and underscores theneed for trials of more focused and effective antiinflammatorytherapy.
The diagnostic criteria for systemic lupus erythematosus, theprototypical autoimmune disease, focus on its major clinicalmanifestations, particularly renal, neurologic, and hematologicdisease. In 1976, Urowitz et al. noted premature myocardialinfarction among patients with lupus,1 a finding confirmed bysubsequent studies.2,3
However, the reported cardiovascular outcomes are based on relativelyfew events, and the prevalence of atherosclerosis among patientswith lupus and its relation to that in a control populationare unknown. Furthermore, controversy remains regarding themechanism of premature atherosclerosis. The prevailing hypothesisholds that premature atherosclerosis in lupus is attributableto an increased frequency of conventional risk factors, suchas hypertension, dyslipidemia, and diabetes, all of which maybe provoked or exacerbated by corticosteroid therapy.4,5,6 Arecent study,7 however, suggested that lupus itself may be atherogenicthrough chronic activation of the immune system. This hypothesisis supported by data demonstrating an inflammatory componentin atherosclerosis in the general population.8,9,10,11
In view of the profound alterations in immune function and inflammationthat characterize lupus, we used a case–control approachto assess the prevalence of atherosclerosis and risk factorsfor cardiovascular disease in a population of patients withlupus. We hypothesized that atherosclerosis would be more prevalentamong the patients and would not be attributable to traditionalrisk factors. We also assessed whether disease factors, treatment,and immune and inflammatory mediators are independently relatedto atherosclerosis in lupus.
Methods
Study Population
A total of 204 sequential nonhospitalized patients with systemiclupus erythematosus who were enrolled in the Autoimmune DiseaseRegistry at the Hospital for Special Surgery in New York wererecruited at the time of outpatient visits. Patients were recruitedbetween April 1999 and October 2002. All patients met the diagnosticcriteria of the American College of Rheumatology.12 Patientswere excluded if they were younger than 18 years of age, werepregnant, or had renal failure (defined by a serum creatininelevel of 3.0 mg per deciliter [265 µmol per liter] ormore or a creatinine clearance of no more than 30 ml per minute).Eight patients had preexisting clinical coronary disease: myocardialinfarction in two (documented on the basis of segmental wall-motionabnormalities) and angina in six (as defined by abnormal resultson coronary angiography in five and an abnormal perfusion studyin one). Cerebrovascular disease was present in 17, of whom8 had had a transient ischemic attack (including 1 with angina),and 9 had had a stroke.
Patients with lupus were individually matched to control subjectson the basis of age (within five years), sex, race, and hypertensionstatus. Control subjects were drawn from normotensive and hypertensivesubjects participating in studies performed at Cornell Universityand funded by the National Institutes of Health.13,14 Thesesubjects were participants in studies that used a similar imagingprotocol to examine the effect of job strain, aging, and hypertensionon preclinical cardiovascular disease. The traditional riskfactors assessed were the presence or absence of a family historyof premature myocardial infarction (before 55 years of age infirst-degree male relatives or before 65 years in female relatives),smoking status, the presence or absence of hypertension (asdefined by a blood pressure of at least 140/90 mm Hg or theuse of antihypertensive medications), the presence or absenceof diabetes mellitus, and the cholesterol level after an overnightfast. None of the control subjects had clinical evidence ofmyocardial infarction or cerebrovascular disease. Control subjectswith hypertension were studied after antihypertensive medicationshad been withheld for at least three weeks. Brachial blood pressureswere obtained immediately after the ultrasound studies. Of 204patients with lupus, 6 young women could not be matched to suitablecontrol subjects and 1 patient did not complete the study protocolowing to equipment failure.
All patients were interviewed and examined with the use of astandardized data-collection instrument. Disease activity anddisease-related damage were assessed at the time of enrollmentin the study with use of the Systemic Lupus Erythematosus DiseaseActivity Index15 and the Systemic Lupus International CollaboratingClinics damage index,16 respectively. Comprehensive medicationhistories were obtained through interviews with the patientsand chart review. The use of corticosteroid therapy was categorizedas current, former, or none and quantified in terms of the averagedaily dose over the preceding five years. The study protocolwas approved by the institutional review board; all participantsgave written informed consent.
Ultrasonographic Studies
The extracranial carotid arteries were examined ultrasonographicallywith the use of a standardized protocol.14 In brief, both theright and left common, internal, and external carotid arterieswere examined in multiple projections to identify the presenceof atherosclerosis — that is, plaque, defined as a focalprotrusion of more than 50 percent of the surrounding wall.The intimal–medial thickness and diameters of the commoncarotid arteries were measured from two-dimensionally guidedM-mode images during several cycles, and the values were averaged.Carotid cross-sectional area, a measure of vascular volume ormass, was calculated as previously described.14
Echocardiography, performed with the use of standard techniques,17included identification of the presence and degree of pulmonaryhypertension from the peak velocity of the tricuspid regurgitationsignal with use of the modified Bernoulli equation, the presenceof Libman–Sacks lesions (focal leaflet thickening of anature unlikely to represent age-related valvular thickening),and the presence of pericardial thickening, effusion, or both.All ultrasonographic studies were performed on the day of thestudy visit by an experienced research technician and interpretedby a single cardiologist who was unaware of the clinical characteristicsof the patients and control subjects.
Laboratory Assessment
Patients with lupus were assessed at the time of the study visitby means of routine chemical analyses; a complete blood count;measurement of Lp(a) lipoprotein by cholesterol content; measurementof serum complement (C3 and C4); tests for antibodies againstdouble-stranded DNA, Smith (Sm), ribonuclear protein (RNP),and antiphospholipid antibody (considered positive if the levelof either anticardiolipin IgG or IgM exceeded 40 isotype phospholipidunits per milliliter or if lupus anticoagulant was present18);and a high sensitivity test for C-reactive protein. CD40 ligandin serum was measured as previously described.19 These testswere performed by the same clinical laboratory with use of assaysthat were invariant during the study period. Serum interleukin-6,tumor necrosis factor p55 receptor, and tumor necrosis factorp75 receptor were measured with the use of kits (Biosource International).Soluble intracellular adhesion molecule 1 and vascular-celladhesion molecule 1 were measured with an enzyme-linked immunosorbentassay. Fasting homocysteine levels were measured before andafter the oral administration of 5 g of methionine.20
Statistical Analysis
Comparisons between patients and control subjects and betweenpatients with and those without atherosclerosis were made bymeans of two-sample t-tests or Mann–Whitney tests (inthe case of non-normal distribution) for continuous variablesand by chi-square analysis for categorical variables. The independenceof the association with atherosclerosis was assessed with useof a stepwise, forward-selection logistic-regression procedurein which all variables that had a significant bivariate relation(as defined by a P value of less than 0.05) with the outcomewere evaluated for inclusion in the model; results are reportedas odds ratios with 95 percent confidence intervals. Two-sidedP values of less than 0.05 were considered to indicate statisticalsignificance.
Results
Comparison of Patients and Controls
The two groups were similar with respect to all demographicvariables and risk factors for cardiovascular disease (Table 1)except blood pressure; the control subjects had higher bloodpressure than the patients at the time of study. The overallprevalence of atherosclerosis (plaque) was higher among thepatients than the controls (relative risk, 2.4; 95 percent confidenceinterval, 1.7 to 3.6; P<0.001) in every age group (Figure 1),especially the youngest age group; the prevalence was 5.6times as high among patients less than 40 years of age as amongcontrol subjects in this age group. A similar trend was seenin older patients, but the small numbers in each group precludedthe difference from being statistically significant. Intimal–medialthickness was significantly less and the luminal diameter waslarger in the patients than in the controls (Table 1), resultingin a slight but significant reduction in vascular mass or carotidcross-sectional area.
Figure 1. Prevalence of Atherosclerotic Plaque among Control Subjects and Patients with Systemic Lupus Erythematosus, According to Decade of Life.
In a multivariate analysis that included age, hypertension status,diabetes status, smoking status, fasting cholesterol level,and lupus status, only age (odds ratio, 2.4 per 10 years; 95percent confidence interval, 1.8 to 3.1), the presence of lupus(odds ratio, 4.8; 95 percent confidence interval, 2.6 to 8.7),and the serum cholesterol level (odds ratio, 1.1 per 10 mg perdeciliter [0.26 mmol per liter]; 95 percent confidence interval,1.0 to 1.5) were independently associated with atherosclerosis.The exclusion of patients with clinical cardiovascular diseaseand their controls did not alter the results.
Comparison of Patients with and Those without Atherosclerotic Plaque
In univariate analyses, patients with lupus who had plaque wereolder, were more likely to be white and postmenopausal, andhad higher systolic blood pressures and total and low-densitylipoprotein cholesterol levels than those without plaque (Table 2).Patients with plaque were older at the time of diagnosis,had had lupus longer, and had higher scores on the damage index.Twenty-two percent of the patients with plaque had damage-indexscores of at least 4, as compared with 11 percent of the patientswithout plaque (P=0.03). Since the scores for the damage indexmay also represent adverse effects of therapy, we repeated theanalyses using a revised index that excluded conditions suchas cataracts, osteoporosis, ovarian failure, avascular necrosis,diabetes, alopecia, and cancer. The damage-index scores remainedhigher in patients with plaque than in those without plaque(1.2 vs. 0.8, P=0.07). Likewise, the scores remained higherin patients with plaque when coronary events were excluded (1.9vs. 1.2, P=0.02). Patients with plaque were more likely to havepulmonary hypertension and preexisting coronary artery disease(angina or a history of myocardial infarction), but not clinicalcerebrovascular disease, than patients without plaque.
Table 2. Characteristics of Patients with Systemic Lupus Erythematosus, According to the Presence or Absence of Plaque.
Comparison of serologic markers of lupus showed that antibodiesagainst Sm and RNP were less frequent in patients with plaquethan in those without plaque; antibodies against any of theribonuclear proteins (Sm, RNP, La, and Ro) were present in 60.2percent of patients without plaque and in 40.8 percent of thosewith plaque (P=0.009). The frequency of anti–double-strandedDNA and any antiphospholipid antibodies did not differ significantlybetween patients with and those without plaque, nor were theseantibodies associated with the presence of clinical coronaryor cerebrovascular disease (data not shown). However, when thecomponents of antiphospholipid-antibody status (anticardiolipinantibodies and lupus anticoagulant) were examined individually,anticardiolipin antibodies were less common in patients withplaque than in those without plaque.
Drug therapy differed between patients with plaque and thosewithout plaque. Former or current treatment with prednisonetended to be less frequent in patients with plaque; the averagedose of prednisone was also lower in these patients. Use ofcyclophosphamide and hydroxychloroquine (defined as currentor former) was lower in those with plaque. There were no significantdifferences between the groups in the use of warfarin, nonsteroidalantiinflammatory drugs, or lipid-lowering agents (data not shown).
The levels of inflammatory mediators associated with cardiovasculardisease in the general population are compared in the two groupsof patients in Table 3. Although average values were increasedin the patients as a whole, there were no significant differencesin the levels between patients with and those without plaque.Similarly, the presence of abnormal elevations of these mediatorswas not associated with plaque.
Table 3. Comparison of Serum Levels of Inflammatory Mediators in Patients with Systemic Lupus Erythematosus, According to the Presence or Absence of Plaque.
We used logistic-regression analyses to examine demographicvariables and risk factors for cardiovascular disease that weresignificantly more common in patients with plaque than in thosewithout plaque; only age remained in the model. A second analysisexamined disease-related factors that were significant in univariateanalyses; the age at diagnosis, the duration of disease, thedamage-index score, and the presence of anti-Sm antibodies remainedin the model. A final analysis (Table 4) added significant treatmentvariables to disease-related variables. Independent correlatesof atherosclerosis included an older age at diagnosis, a longerduration of disease, a higher damage-index score, absence ofthe use of cyclophosphamide, and the absence of anti-Sm or anticardiolipinantibody. Restriction of analyses to patients who were youngerthan 35 years of age when the disease began confirmed the associationof atherosclerosis with a longer duration of the disease, ahigher damage-index score, and the lack of immunosuppressivetherapy.
Table 4. Logistic-Regression Analysis of Independent Predictors of Atherosclerosis in Patients with Systemic Lupus Erythematosus.
Discussion
This case–control study assessed the presence or absence,magnitude, and determinants of atherosclerosis in patients withsystemic lupus erythematosus in a population-based sample. Themain findings, confirming those of our pilot study,21 are thatthe prevalence of atherosclerosis is significantly increasedamong patients with lupus and that this increase is not attributableto traditional risk factors for cardiovascular disease. Similarfindings are reported elsewhere in this issue of the Journal.22Our finding of an association of atherosclerosis with a longerduration of disease, a higher damage-index score, and less aggressiveimmunosuppressive therapy argues strongly that chronic inflammationis atherogenic in this population.
We determined the correlates of preclinical atherosclerosisin patients with systemic lupus erythematosus. One previouscase–control study23 found greater carotid intimal–medialthickness in patients with lupus who had had a myocardial infarction,angina, stroke, or claudication than in those without clinicalcardiovascular disease. The small sample size (26 in each group)precluded a determination of the prevalence and independentcorrelates of atherosclerosis. An observational study of womenenrolled in the Pittsburgh Lupus Registry reported a prevalenceof plaque that was similar to that in our study (40 percentand 37 percent, respectively); the risk of plaque was independentlyrelated to older age, higher systolic blood pressure, a higherlevel of low-density cholesterol, and a history of myocardialinfarction or angina.24 Differences between these findings andours may relate to the higher proportion of whites in the Pittsburghstudy (87 percent and 55 percent, respectively) and the greaterprevalence of clinical coronary disease (8.6 percent and 3.9percent, respectively).
Interestingly, although the Pittsburgh study24 did not includea control population, the mean intimal–medial thicknessin women with lupus was slightly lower than that in women participatingin the Women's Healthy Lifestyle Project conducted at the sameinstitution (0.68 mm vs. 0.71 mm). This observation is similarto our finding in a case–control study and demonstratesthe potential for dissociation between intimal–medialthickness, commonly considered a marker of early or diffuseatherosclerosis, and unequivocal evidence of atherosclerosis(i.e., plaque). The presence of plaque is a more potent predictorof clinical events, usually myocardial infarction, than is intimal–medialthickness.25,26 The independent association of atherosclerosiswith the duration of disease and extent of disease-induced damageis noteworthy, because the damage index is a marker of the cumulativeseverity of disease.
In the general population, increased serum levels of C-reactiveprotein, intracellular adhesion molecule 1, and CD40 ligandare associated with an increased risk of cardiovascular events.8,9,10,11Although these inflammatory mediators were elevated in our patientswith lupus who had plaque, there were no significant differencesbetween these patients and those without plaque. This findingsuggests that these markers lose their discriminatory powerwith respect to cardiovascular outcomes among patients withconditions in which levels of inflammatory molecules are elevated,such as lupus, in contrast to the general population, wheremost values fall within the normal range. Nevertheless, levelsof these markers of inflammation were abnormal in many patientswith lupus, and longitudinal, rather than cross-sectional, studiesmay yet define their relation to the development and progressionof atherosclerosis.
Although inflammatory mediators were not related to atherosclerosisin our patients, our data show that anti-Sm, anti-RNP, and anticardiolipinantibodies were less frequent in patients with plaque than inthose without plaque. Although antiphospholipid antibodies havebeen implicated in atherogenesis,27 possibly as a result oftheir activation of endothelial cells,28 our study, as wellas those of others, found no association between anticardiolipinantibody and carotid plaque24,29 or cardiovascular disease.23The clinical features and autoantibody specificities that differentiatepatients with lupus who have plaque from those who do not haveplaque may define two patterns of lupus: one characterized bymore prolonged and seemingly less virulent disease that fostersatherosclerosis and the other by more prominent autoimmunityand aggressive disease, which is more likely to be treated withimmunosuppressive therapies.
That treatment with corticosteroids may have a role in modifyingthe pathogenesis of atherosclerosis in systemic lupus erythematosushas been suggested.4,5 However, the average five-year dailydose of prednisone was actually significantly lower in our patientswith lupus who had plaque. The significant negative relationbetween the use of hydroxychloroquine and the presence of atherosclerosis,even with high rates of use, is also striking. This trend hasbeen noted before4 and has been attributed to reduced serumcholesterol levels.30 In our study, cholesterol levels weresimilar in patients who had taken hydroxychloroquine and thosewho had not.
The limitations of our study include difficulties in accuratelyquantifying the severity of disease and disease treatment. Systemiclupus erythematosus is a chronic disease characterized by exacerbationsand remissions; thus, measures of disease activity, laboratoryassays, and therapy vary with time. However, scores for thedisease-activity index, measured at the time of study, did notdiffer significantly between patients with plaque and thosewithout plaque, whereas the damage-index score, a summationof the cumulative effects of disease, was greater in patientswith plaque, associating chronic tissue damage with atherogenesis.Although we cannot exclude the possibility that our populationhad more severe disease than the overall population of patientswith lupus, the prevalence of clinical cardiovascular diseasein our study was similar to the rates reported by other NorthAmerican registries.4,7,24 Our case–control design precludedthe identification of a causal relation between disease factorsand atherosclerosis.
In conclusion, systemic lupus erythematosus is associated withan increased prevalence of atherosclerosis, which was most strikingin young patients. Although the traditional risk factors forcardiovascular disease are not primarily responsible for suchan accelerated development of atherosclerosis, their importancein the population as a whole is well established, and theirrole in the progression of atherosclerosis could not be examinedin this cross-sectional study. Thus, it is prudent to identifyand treat traditional risk factors aggressively in all patientswith lupus.31
In our study, the presence of systemic lupus erythematosus wasthe most important independent correlate of atherosclerosisother than age. Our results suggest two clinical patterns oflupus, one characterized by smoldering disease with higher damage-indexscores, limited production of autoantibodies, and atherosclerosis,and the other with a wider autoantibody spectrum, associatedwith more aggressive immunosuppressive therapy and a lower likelihoodof plaque.
The negative correlation between atherosclerosis and aggressivetherapy suggests that more vigorous therapy might decrease thelikelihood and burden of atherosclerosis in patients with lupusand, perhaps, in those with other chronic inflammatory diseases.Our results also suggest that the use of immunosuppressive therapyprimarily for clinical flares may not adequately control thechronic atherogenic inflammatory milieu. The identificationof biologic markers of disease activity associated with atherosclerosismay help optimize therapy for this important manifestation ofsystemic autoimmune disease.
Supported by grants from the National Institute of Arthritis,Musculoskeletal, and Skin Diseases (AR 45591); the NationalHeart, Lung, and Blood Institute (HL 47540); the Public HealthService (M10RR0047); the Mary Kirkland Center for Lupus Researchat the Hospital for Special Surgery; and the Bugher Foundation.
Source Information
From the Divisions of Cardiology (M.J.R., R.B.D.), Rheumatology (B.-A.S., A.D., M.D.L., L.S., M.K.C., S.A.P., J.E. Salmon), and Hematology–Oncology (R.S.), Weill Medical College of Cornell University, the Hospital for Special Surgery, New York; and the Department of Psychiatry, State University of New York at Stony Brook, Stony Brook (J.E. Schwartz).
Address reprint requests to Dr. Roman at the Division of Cardiology, Weill Medical College of Cornell University, 525 E. 68th St., New York, NY 10021, or at mroman{at}med.cornell.edu.
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Premature Coronary Disease in Systemic Lupus
Wurzel J., Goldman B. I., Doria A., Shoenfeld Y., Pauletto P., Violi F., Loffredo L., Ferro D., Pezzetta F., Mascitelli L., Noël B., Roman M. J., Lockshin M. D., Salmon J. E., Stein C. M., Hahn B. H.
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A correction has been published: N Engl J Med 2006;355(16):1746.
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