Premature Coronary-Artery Atherosclerosis in Systemic Lupus Erythematosus
Yu Asanuma, M.D., Ph.D., Annette Oeser, B.S., Ayumi K. Shintani, Ph.D., M.P.H., Elizabeth Turner, M.D., Nancy Olsen, M.D., Sergio Fazio, M.D., Ph.D., MacRae F. Linton, M.D., Paolo Raggi, M.D., and C. Michael Stein, M.D.
Background Premature coronary artery disease is a major causeof illness and death in patients with systemic lupus erythematosus,but little is known about the prevalence, extent, and causesof coronary-artery atherosclerosis.
Methods We used electron-beam computed tomography to screenfor the presence of coronary-artery calcification in 65 patientswith systemic lupus erythematosus (mean [±SD] age, 40.3±11.6years) and 69 control subjects (mean age, 42.7±12.6 years)with no history of coronary artery disease. When calcificationwas detected, the extent was measured by means of the Agatstonscore. The frequency of risk factors for coronary artery diseasewas compared in patients and controls, and the relation betweenthe patients' clinical characteristics and the presence or absenceof coronary-artery calcification was examined.
Results The two groups were similar with respect to age, race,and sex. Coronary-artery calcification was more frequent inpatients with lupus (20 of 65 patients) than in control subjects(6 of 69 subjects) (P=0.002). The mean calcification score was68.9±244.2 in the patients and 8.8±41.8 (P<0.001)in controls. Levels of total, high-density lipoprotein, andlow-density lipoprotein cholesterol were not elevated in patientswith lupus, but levels of triglycerides (P=0.02) and homocysteine(P<0.001) were. Among patients with lupus, measures of diseaseactivity were similar in those with and those without coronary-arterycalcification, but those with calcification were more likelyto be older (P<0.001) and male (P=0.008).
Conclusions In patients with systemic lupus erythematosus, theprevalence of coronary-artery atherosclerosis is elevated andthe age at onset is reduced. Early detection of atherosclerosismay provide an opportunity for therapeutic intervention.
Systemic lupus erythematosus is a chronic inflammatory, autoimmunedisease that affects mainly young women, a group usually freeof atherosclerosis. Treatment for lupus has improved, and long-termsurvival has increased; however, it has become clear that patientswith lupus have substantially increased morbidity and mortalityfrom cardiovascular disease.1,2,3 The incidence of myocardialinfarction is 5 times as high in patients with lupus as in thegeneral population, and in young women the age-specific incidenceis increased by a factor of as much as 50.4 The reasons forthese differences are poorly understood. Traditional coronaryrisk factors such as hypercholesterolemia, smoking, and hypertensionhave been implicated5 but do not account for the increase inatherosclerotic disease.6 This finding has raised the questionwhether chronic inflammation or the drugs used to treat it,such as corticosteroids, or other risk factors have a role.The possibility that inflammation associated with lupus couldpromote atherosclerosis is of particular interest, since thepathogenesis of atherosclerosis is thought to be, in part, mediatedby inflammation.7
A surrogate measure of coronary atherosclerosis, the presenceof carotid-artery plaque, was found to be increased in patientswith lupus in an uncontrolled study8; however, the prevalenceand extent of coronary-artery atherosclerosis remain poorlycharacterized. Coronary-artery atherosclerosis can be detectednoninvasively with the use of electron-beam computed tomography(CT).9,10 The extent of coronary-artery calcification correlateswith findings on coronary angiography and with the extent ofatherosclerosis in pathological specimens and is predictiveof future cardiac events.9,11,12,13,14,15
We examined the hypothesis that the prevalence and extent ofcoronary-artery calcification are increased in patients withlupus, as compared with a control group matched for age, race,and sex, and are related to the patients' clinical characteristics.
Methods
Subjects
Between January 2000 and October 2002, we studied 65 patientswith lupus and 69 control subjects who were frequency-matchedfor age, race, and sex. Consecutive eligible patients olderthan 18 years of age who met the classification criteria forsystemic lupus erythematosus16 and who had had the disease longerthan one year were enrolled. Controls did not meet the classificationcriteria for lupus. Patients and controls with a history ofcardiovascular disease (previous stroke, myocardial infarction,or angina) were excluded. Patients were recruited from the practicesof local rheumatologists, through a Lupus Foundation newsletter,and by advertisements. Control subjects were recruited fromthe patients' acquaintances, by advertisement, and from a database of volunteers maintained by the General Clinical ResearchCenter at Vanderbilt University School of Medicine. The studywas approved by the institutional review board of VanderbiltUniversity Hospital, and all subjects gave written informedconsent.
Information was obtained through a structured interview, physicalexamination, laboratory tests, and electron-beam CT, and inthe case of patients, review of medical records. Current andcumulative use of medications was determined by combining theinformation provided by patients and medical records. The medicalrecord was reviewed to confirm the medical history and to obtainthe results of tests for antinuclear antibody, anti–double-strandedDNA, anticardiolipin antibodies, and lupus anticoagulant. Patientswere considered to have antiphospholipid antibodies if theyhad a positive test for anticardiolipin antibodies (more than23 IgG phospholipid units or more than 11 IgM phospholipid units)or lupus anticoagulant (defined by a prolonged partial-thromboplastintime or Russell's viper–venom time).17
A family history of coronary artery disease was defined as afirst-degree relative who had had a myocardial infarction orstroke before the age of 55 years in males or before the ageof 65 years in females.18 Height and weight were measured, andthe body-mass index was calculated as the weight in kilogramsdivided by the square of the height in meters. Blood pressurewas determined as the average of two measurements obtained 5minutes apart after subjects had rested quietly in the supineposition for 10 minutes. Subjects were considered to have hypertensionif they were taking antihypertensive agents or if they had asystolic blood pressure of at least 140 mm Hg or a diastolicpressure of at least 90 mm Hg. Disease activity and accumulatedorgan damage were measured in patients with lupus with the useof the Systemic Lupus Erythematosus Disease Activity Index andthe Systemic Lupus International Collaborating Clinics damageindex, respectively.19,20
Blood was collected after an overnight fast for the measurementof a complete blood count and levels of creatinine, total cholesterol,high-density lipoprotein cholesterol, low-density lipoproteincholesterol, triglycerides, Lp(a) lipoprotein by cholesterolcontent, and homocysteine. In patients with lupus, C-reactiveprotein levels, the Westergren erythrocyte sedimentation rate,and the total hemolytic complement were also determined.
Imaging Procedures
All subjects underwent imaging with an Imatron C-150 scanner(Imatron). Imaging was performed with a 100-msec scanning timeand a single-slice thickness of 3 mm. A total of 40 slices wereobtained during single breath-holding periods. Tomographic imagingwas electrocardiographically triggered at 60 percent of theinterval between R waves. All areas of calcification withinthe borders of a coronary artery with a minimal attenuationof 130 Hounsfield units were computed. A calcified coronaryplaque was considered present if at least three consecutivepixels were measured (voxel size, 1.03 mm3). The acquired imageswere reviewed at the core electron-beam CT laboratory on a NetraMDworkstation (ScImage). Subjects were included in this studyonly if complete data were available from their scans, withoutmisregistration of slices owing to artifacts of motion, respiration,or asynchronous electrocardiographic triggering. To ensure thecontinuity and consistency of the interpretation of scores,a single expert investigator who was unaware of the subjects'clinical status read all the scans.
Calculation of Calcium Scores
The degree of coronary-artery calcification was calculated asdescribed by Agatston et al.21 The sum of the scores for allarterial lesions provides an overall score for each subject.21The correlation between this score and other variables, suchas coronary risk factors, inflammatory markers, and lupus diseaseactivity, was determined.
Statistical Analysis
Assuming the frequency of coronary-artery calcification is 15percent among asymptomatic 40-year-old women,22 the study required65 patients and 65 controls to have 85 percent power to detecta minimal frequency of coronary-artery calcification of 35 percentamong patients with lupus. Statistical analyses were performedin two phases. First, the prevalence of coronary-artery calcificationand coronary risk factors was compared in patients with lupusand control subjects. The distribution of coronary risk factorswas assessed with the use of exact Mann–Whitney U testsfor continuous variables and Fisher's exact tests for categoricalvariables. The exact Mann–Whitney U test was used to comparethe distribution of coronary calcium scores between patientsand controls. Because of the skewed distribution of calciumscores, an association between coronary-artery calcificationand disease was further assessed according to the presence orabsence of any coronary calcification.
Adjusted odds ratios were obtained with the use of a logistic-regressionmodel to determine independent associations between the presenceof coronary-artery calcium and disease status after controllingfor covariates. Covariates were identified if the P value wasless than 0.05 on the basis of the univariate analyses. Ageand sex were also included in the multivariable logistic-regressionmodel. We performed a similar analysis using logistic regressionto evaluate the association between disease status and threelevels of coronary calcification (none, low, and high). Thedifference in the rates of increase in the prevalence of coronary-arterycalcification according to age between patients and controlswas assessed with the use of logistic regression with an interactionterm.
The second exploratory part of the analysis included only patientswith lupus. The patients' characteristics were compared withthe use of exact Mann–Whitney U tests and Fisher's exacttests. Logistic regression was used to obtain age- and sex-adjustedodds ratios for the presence of coronary calcium.
All analyses used a two-sided significance level of 5 percentand were performed with the use of SAS software (version 8.02,SAS Institute) and Proc-LogExact (version 4, Cytel Software).
Results
Characteristics of Patients and Controls
The demographic characteristics and cardiovascular risk factorsfor the 65 patients with lupus and the 69 control subjects areshown in Table 1. Patients and controls were successfully matchedfor age, sex, and race. The subjects were predominantly welleducated, with 97 percent having 12 or more years of education,and young, with an average age of approximately 40 years, andpredominantly female (approximately 85 percent) and white (approximately75 percent). The mean (±SD) duration of disease fromthe time of the diagnosis of systemic lupus erythematosus bya physician was 9.9±8.7 years.
Table 1. Clinical Characteristics of Patients with Lupus and Control Subjects.
Hypertension was more common among the patients than the controls(48 percent vs. 25 percent, P=0.007). Thirty percent of controlsand 50 percent of patients had ever smoked. More patients thancontrols currently smoked (35 percent vs. 16 percent, P=0.02)(Table 1). Two patients with lupus had undergone renal transplantation,and one was receiving long-term hemodialysis.
Levels of total, high-density lipoprotein, and low-density lipoproteincholesterol and Lp(a) lipoprotein were similar in the two groups,but levels of triglycerides (P=0.02) and homocysteine (P<0.001)were significantly higher among the patients (Table 1).
Coronary-Artery Calcification
Coronary-artery calcium scores averaged 68.9±244.2 (range,0 to 1526) in the patients and 8.8±41.8 (range, 0 to243.4) in controls (P<0.001). The frequency of a calcificationscore of zero and of values above or below 64 is shown in Table 2.Coronary-artery calcification was more prevalent in patientswith lupus than controls. Calcification was present in 20 of65 patients (31 percent) and in 6 of 69 control subjects (9percent, P=0.002), and the unadjusted odds ratio was 4.7 (95percent confidence interval, 1.7 to 12.6). After we controlledfor age, sex, total pack-years of smoking, presence or absenceof hypertension, triglyceride levels, and homocysteine levels,the adjusted odds ratios for the presence of coronary-arterycalcification in patients with lupus was 9.8 (P=0.001), as comparedwith controls. Low and high levels of coronary-artery calcificationwere defined with the use of a calcium score above or belowthe median calcium score of patients with calcification (64Agatston units). The odds ratios for having low and high levelsof coronary calcification (with the absence of calcificationused as the reference level) were 4.6 for both levels, and theadjusted odds ratios were 10.0 and 9.6, respectively. Coronary-arterycalcium was present in one of two patients who had undergonerenal transplantation and was not present in the patient whowas receiving hemodialysis.
Table 2. Prevalence of Coronary-Artery Calcification and Calcification Scores in Patients with Lupus and Control Subjects.
The frequency of calcification scores indicative of coronary-arteryatherosclerosis of varying severity in patients with lupus andcontrols is shown in Figure 1. A calcium score of zero representsthe absence of detectable calcium, whereas a score of greaterthan 400 indicates the presence of extensive coronary-arterycalcification. None of the control subjects had a calcium scoregreater than 400, whereas three patients with lupus did.
Figure 1. Frequency of Coronary-Artery Calcium Scores among Patients with Lupus and Control Subjects, According to Age.
Higher scores indicate more extensive calcification.
The prevalence and extent of coronary-artery calcification inthe general population increase with age.23 Therefore, the prevalenceof coronary-artery calcification in patients and controls indifferent age groups was compared (Figure 2). Coronary-arterycalcification occurred at a younger age in patients with lupusthan controls, and the prevalence increased with increasingage. The absence of coronary calcium in the elderly controlgroup is most likely due to the small number of subjects inthis subgroup (seven). However, this absence does not materiallyaffect the interpretation of the data, since when we performedan analysis excluding the subgroup of patients older than 60years of age, coronary-artery calcium was present in 17 of 62patients with lupus and 6 of 62 controls (P=0.01).
Figure 2. The Prevalence of Coronary-Artery Calcification among Patients with Lupus and Control Subjects, According to Age.
The rate of increase in the prevalence of calcium with age was significantly higher in patients than controls (P=0.02).
Older age (P<0.001) and male sex (P=0.008) were more commonin patients with coronary-artery calcification than in thosewithout calcification, but the groups did not differ significantlywith respect to other risk factors for atherosclerosis or markersof inflammation or disease activity (Table 3). The average creatininelevel was slightly higher in patients with calcification (0.9±0.1mg per deciliter [80±9 µmol per liter]) than inthose without calcification (0.8±0.4 mg per deciliter[71±35 µmol per liter], P<0.001), but this differencewas not significant after adjustment for age and sex (Table 3).There was no significant relation between the use of corticosteroidsand the presence of coronary-artery calcification. The use ofhydroxychloroquine in patients with and those without calcificationdid not differ significantly.
Table 3. Characteristics of Patients with Lupus, According to the Presence or Absence of Coronary-Artery Calcification.
Discussion
Our results indicate that coronary-artery calcification, asdetected by electron-beam CT, occurs more frequently and ata younger age in patients with lupus than in control subjects.This study shows that asymptomatic atherosclerosis is frequentlypresent in patients with lupus and cannot be predicted by thepresence or absence of other cardiovascular risk factors. Complementaryfindings are reported elsewhere in this issue of the Journal.24
Previous evidence from autopsies and clinical studies has suggestedthat the prevalence of subclinical atherosclerosis is increasedin patients with lupus.25 Manzi et al. used B-mode ultrasonographyto measure carotid-artery plaques and intimal–medial thicknessin 175 women with lupus, 15 percent of whom had already hada cardiovascular event.8 They found that 40 percent of womenwith lupus had at least one focal carotid-artery plaque, a higherfrequency than would have been expected to occur among healthywomen. Another study retrospectively compared patients withlupus who had a history of cardiovascular disease and thosewho had no such history and found that carotid-artery intimal–medialthickness was greater in patients with a history of cardiovasculardisease.26 However, in this study, as in that by Manzi et al.,8carotid-artery intimal–medial thickness — a measureoften considered to be associated with coronary atherosclerosis27— in patients without a previous cardiovascular eventdid not differ from values in the general population.26
Attempts to address the extent and severity of coronary arterydisease in patients with lupus more directly have used single-photon-emissionCT dual-isotope myocardial perfusion imaging. Such studies detectedabnormalities in 35 percent of patients.28 However, the prevalenceof coronary-artery atherosclerosis in patients with lupus hasremained unclear because it is difficult to measure noninvasively.
The ability to measure coronary-artery calcification by electron-beamCT has provided a reproducible and quantitative method for thedetection of subclinical coronary-artery atherosclerosis thatyields information about the risk of cardiovascular events inaddition to that provided by other risk factors.29 In the presentstudy we used electron-beam CT to study subjects with no historyof cardiovascular disease and found an increased prevalenceof coronary-artery calcification, indicating increased coronaryatherosclerosis and cardiovascular risk, among patients withlupus, most of whom were relatively young women.
Because the prevalence of myocardial infarction is increasedamong patients with lupus, several studies have measured cardiovascularrisk factors in this group.5,8 Age and the presence of hypertensionwere associated with clinical coronary artery disease.6 Elevatedlevels of homocysteine have been reported in patients with lupusand have been associated with stroke and arterial thromboticevents.30 We found that hypertension occurred more frequentlyin patients with lupus than in controls and that the patientsalso had elevated levels of triglycerides and homocysteine.By contrast, the levels of traditional cardiovascular risk factorssuch as low-density lipoprotein and high-density lipoproteincholesterol, which are commonly measured as a means of predictingcardiovascular risk in the general population,18 did not differsignificantly between patients and control subjects.
The relation between cardiovascular risk factors and coronary-arterycalcium is of particular interest, since a strong relation wouldallow clinicians to identify patients with undetected coronary-arteryatherosclerosis by means of such risk markers. Therefore, wecompared patients with coronary-artery calcium and those withoutit. After adjustment for age and sex, no cardiovascular riskfactor, acute-phase reactant, or disease-activity index wassignificantly associated with the presence of coronary-arterycalcium. However, given the wide confidence intervals for somevariables, these findings should be regarded as exploratoryrather than definitive. Antiphospholipid antibodies are thoughtto promote atherosclerosis.31 In our study, patients with anti–double-strandedDNA and antiphospholipid antibodies were younger than thosewithout them. Thus, the apparent trend toward a lower frequencyof coronary-artery calcification in patients with these antibodieswas no longer present after adjustment for age.
The cause of accelerated atherosclerosis in patients with lupusremains unclear. However, we did not measure many inflammatorymediators, such as cytokines, cellular adhesion molecules, CD40ligand, and markers of oxidative stress, that have been implicatedin the pathogenesis of atherosclerosis.32 Furthermore, a singlemeasurement of an inflammatory marker provides only a cross-sectionalmeasure of inflammation, whereas atherosclerosis is a chronicprocess.
Our findings suggest that coronary-artery atherosclerosis ismore prevalent among patients with lupus than in the generalpopulation and cannot be predicted by the measurement of traditionalrisk factors or markers of disease activity. This suppositionis concordant with the results of a retrospective study, whichfound that, even after accounting for base-line cardiovascularrisk factors as defined in the Framingham Study, the risk ofadverse cardiovascular outcomes was increased by a factor of7 to 17 in patients with lupus as compared with the Framinghamcohort.6 Thus, to identify asymptomatic patients with lupuswho are at high risk for a cardiovascular event, the use ofFramingham risk factors alone is inadequate, and the use ofnovel markers of cardiovascular risk should be explored. Coronary-arterycalcification may be such a marker,33 since high calcium scoresare associated with an increased probability of the presenceof vulnerable plaque, and although they do not identify specificvulnerable lesions,34 the predictive value of these scores shouldbe explored in patients with lupus.
In conclusion, asymptomatic coronary-artery atherosclerosis,as detected by electron-beam CT, is more common in patientswith lupus than in the general population but is not associatedwith traditional coronary risk factors, lupus disease activity,or corticosteroid therapy. Lupus should be added to the listof conditions that raise cardiovascular risk independent ofconventional risk factors.
Supported by grants (HL04012, HL65082, DK26657, and GM5MO1-RR00095)from the National Institutes of Health and by a grant from theLupus Foundation of America, Nashville Chapter. Dr. Asanumawas supported by a Merck Sharp and Dohme Foundation InternationalFellowship in Clinical Pharmacology and by the Japan ResearchFoundation for Clinical Pharmacology.
We are indebted to Mr. Daniel Byrne for insightful review ofthe manuscript and statistical advice.
Source Information
From the Divisions of Clinical Pharmacology (Y.A., A.O., C.M.S.), General Internal Medicine (A.K.S.), Rheumatology (E.T., N.O., C.M.S.), and Cardiovascular Medicine (S.F., M.F.L.), Vanderbilt University School of Medicine, Nashville; and the Section of Cardiology, Tulane University School of Medicine, New Orleans (P.R.).
References
Abu-Shakra M, Urowitz MB, Gladman DD, Gough J. Mortality studies in systemic lupus erythematosus: results from a single center. I. Causes of death. J Rheumatol 1995;22:1259-1264. [Web of Science][Medline]
Ward MM. Premature morbidity from cardiovascular and cerebrovascular diseases in women with systemic lupus erythematosus. Arthritis Rheum 1999;42:338-346. [CrossRef][Web of Science][Medline]
Rubin LA, Urowitz MB, Gladman DD. Mortality in systemic lupus erythematosus: the bimodal pattern revisited. Q J Med 1985;55:87-98. [Web of Science][Medline]
Manzi S, Meilahn EN, Rairie JE, et al. Age-specific incidence rates of myocardial infarction and angina in women with systemic lupus erythematosus: comparison with the Framingham Study. Am J Epidemiol 1997;145:408-415. [Free Full Text]
Petri M, Perez-Gutthann S, Spence D, Hochberg MC. Risk factors for coronary artery disease in patients with systemic lupus erythematosus. Am J Med 1992;93:513-519. [CrossRef][Web of Science][Medline]
Esdaile JM, Abrahamowicz M, Grodzicky T, et al. Traditional Framingham risk factors fail to fully account for accelerated atherosclerosis in systemic lupus erythematosus. Arthritis Rheum 2001;44:2331-2337. [CrossRef][Web of Science][Medline]
Ross R. Atherosclerosis -- an inflammatory disease. N Engl J Med 1999;340:115-126. [Free Full Text]
Manzi S, Selzer F, Sutton-Tyrrell K, et al. Prevalence and risk factors of carotid plaque in women with systemic lupus erythematosus. Arthritis Rheum 1999;42:51-60. [CrossRef][Web of Science][Medline]
Budoff MJ, Diamond GA, Raggi P, et al. Continuous probabilistic prediction of angiographically significant coronary artery disease using electron beam tomography. Circulation 2002;105:1791-1796. [Free Full Text]
Callister TQ, Raggi P, Cooil B, Lippolis NJ, Russo DJ. Effect of HMG-CoA reductase inhibitors on coronary artery disease as assessed by electron-beam computed tomography. N Engl J Med 1998;339:1972-1978. [Free Full Text]
Rumberger JA, Sheedy PF III, Breen JF, Schwartz RS. Coronary calcium, as determined by electron beam computed tomography, and coronary disease on arteriogram: effect of patient's sex on diagnosis. Circulation 1995;91:1363-1367. [Free Full Text]
Rumberger JA, Simons DB, Fitzpatrick LA, Sheedy PF, Schwartz RS. Coronary artery calcium area by electron-beam computed tomography and coronary atherosclerotic plaque area: a histopathologic correlative study. Circulation 1995;92:2157-2162. [Free Full Text]
Sangiorgi G, Rumberger JA, Severson A, et al. Arterial calcification and not lumen stenosis is highly correlated with atherosclerotic plaque burden in humans: a histologic study of 723 coronary artery segments using nondecalcifying methodology. J Am Coll Cardiol 1998;31:126-133. [Free Full Text]
Keelan PC, Bielak LF, Ashai K, et al. Long-term prognostic value of coronary calcification detected by electron-beam computed tomography in patients undergoing coronary angiography. Circulation 2001;104:412-417. [Free Full Text]
Arad Y, Spadaro LA, Goodman K, Newstein D, Guerci AD. Prediction of coronary events with electron beam computed tomography. J Am Coll Cardiol 2000;36:1253-1260. [Free Full Text]
Tan EM, Cohen AS, Fries JF, et al. The 1982 revised criteria for the classification of systemic lupus erythematosus. Arthritis Rheum 1982;25:1271-1277. [Web of Science][Medline]
Levine JS, Branch DW, Rauch J. The antiphospholipid syndrome. N Engl J Med 2002;346:752-763. [Free Full Text]
Executive summary of the Third Report of the National Cholesterol Education Program (NCEP) Expert Panel on Detection, Evaluation, and Treatment of High Blood Cholesterol in Adults (Adult Treatment Panel III). JAMA 2001;285:2486-2497. [Free Full Text]
Bombardier C, Gladman DD, Urowitz MB, Caron D, Chang CH. Derivation of the SLEDAI: a disease activity index for lupus patients. Arthritis Rheum 1992;35:630-640. [Web of Science][Medline]
Gladman DD, Urowitz MB, Goldsmith CH, et al. The reliability of the Systemic Lupus International Collaborating Clinics/American College of Rheumatology Damage Index in patients with systemic lupus erythematosus. Arthritis Rheum 1997;40:809-813. [Web of Science][Medline]
Agatston AS, Janowitz WR, Hildner FJ, Zusmer NR, Viamonte M Jr, Detrano R. Quantification of coronary artery calcium using ultrafast computed tomography. J Am Coll Cardiol 1990;15:827-832. [Abstract]
Raggi P, Cooil B, Callister TQ. Use of electron beam tomography data to develop models for prediction of hard coronary events. Am Heart J 2001;141:375-382. [CrossRef][Web of Science][Medline]
Schmermund A, Erbel R, Silber S. Age and gender distribution of coronary artery calcium measured by four-slice computed tomography in 2,030 persons with no symptoms of coronary artery disease. Am J Cardiol 2002;90:168-173. [CrossRef][Web of Science][Medline]
Roman MJ, Shanker B-A, Davis A, et al. Prevalence and correlates of accelerated atherosclerosis in systemic lupus erythematosus. N Engl J Med 2003;349:2399-2406. [Free Full Text]
Bulkley BH, Roberts WC. The heart in systemic lupus erythematosus and the changes induced in it by corticosteroid therapy: a study of 36 necropsy patients. Am J Med 1975;58:243-264. [CrossRef][Web of Science][Medline]
Svenungsson E, Jensen-Urstad K, Heimburger M, et al. Risk factors for cardiovascular disease in systemic lupus erythematosus. Circulation 2001;104:1887-1893. [Free Full Text]
O'Leary DH, Polak JF, Kronmal RA, Manolio TA, Burke GL, Wolfson SK Jr. Carotid-artery intima and media thickness as a risk factor for myocardial infarction and stroke in older adults. N Engl J Med 1999;340:14-22. [Free Full Text]
Bruce IN, Burns RJ, Gladman DD, Urowitz MB. Single photon emission computed tomography dual isotope myocardial perfusion imaging in women with systemic lupus erythematosus. I. Prevalence and distribution of abnormalities. J Rheumatol 2000;27:2372-2377. [Web of Science][Medline]
Schmermund A, Denktas AE, Rumberger JA, et al. Independent and incremental value of coronary artery calcium for predicting the extent of angiographic coronary artery disease: comparison with cardiac risk factors and radionuclide perfusion imaging. J Am Coll Cardiol 1999;34:777-786. [Free Full Text]
Petri M, Roubenoff R, Dallal GE, Nadeau MR, Selhub J, Rosenberg IH. Plasma homocysteine as a risk factor for atherothrombotic events in systemic lupus erythematosus. Lancet 1996;348:1120-1124. [CrossRef][Web of Science][Medline]
Jara LJ, Medina G, Vera-Lastra O, Shoenfeld Y. Atherosclerosis and antiphospholipid syndrome. Clin Rev Allergy Immunol 2003;25:79-88. [CrossRef][Web of Science][Medline]
von der Thusen JH, Kuiper J, van Berkel TJ, Biessen EA. Interleukins in atherosclerosis: molecular pathways and therapeutic potential. Pharmacol Rev 2003;55:133-166. [Free Full Text]
Raggi P, Callister TQ, Cooil B, et al. Identification of patients at increased risk of first unheralded acute myocardial infarction by electron-beam computed tomography. Circulation 2000;101:850-855. [Free Full Text]
Pearson TA. New tools for coronary risk assessment: what are their advantages and limitations? Circulation 2002;105:886-892. [Free Full Text]
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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350:1571-1575, Apr 8, 2004.
Correspondence
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[Abstract][Full Text]
Binstadt, B. A., Hebert, J. L., Ortiz-Lopez, A., Bronson, R., Benoist, C., Mathis, D.
(2009). The same systemic autoimmune disease provokes arthritis and endocarditis via distinct mechanisms. Proc. Natl. Acad. Sci. USA
106: 16758-16763
[Abstract][Full Text]
Meroni, P., Tincani, A, Alarcon-Riquelme, M., Shoenfeld, Y, Borghi, M.
(2009). European Forum on Antiphospholipid Antibodies: research in progress. Lupus
18: 924-929
[Abstract]
O'Neill, S G, Woldman, S, Bailliard, F, Norman, W, McEwan, J, Isenberg, D A, Taylor, A M, Rahman, A
(2009). Cardiac magnetic resonance imaging in patients with systemic lupus erythematosus. Ann Rheum Dis
68: 1478-1481
[Abstract][Full Text]
Chung, C., Long, A., Solus, J., Rho, Y., Oeser, A, Raggi, P, Stein, C.
(2009). Adipocytokines in systemic lupus erythematosus: relationship to inflammation, insulin resistance and coronary atherosclerosis. Lupus
18: 799-806
[Abstract]
Recio-Mayoral, A., Mason, J. C., Kaski, J. C., Rubens, M. B., Harari, O. A., Camici, P. G.
(2009). Chronic inflammation and coronary microvascular dysfunction in patients without risk factors for coronary artery disease. Eur Heart J
30: 1837-1843
[Abstract][Full Text]
Jain, D, Halushka, M K
(2009). Cardiac pathology of systemic lupus erythematosus. J. Clin. Pathol.
62: 584-592
[Abstract][Full Text]
Pons-Estel, G. J., Gonzalez, L. A., Zhang, J., Burgos, P. I., Reveille, J. D., Vila, L. M., Alarcon, G. S.
(2009). Predictors of cardiovascular damage in patients with systemic lupus erythematosus: data from LUMINA (LXVIII), a multiethnic US cohort. Rheumatology (Oxford)
48: 817-822
[Abstract][Full Text]
Becker-Merok, A, Nossent, J.
(2009). Prevalence, predictors and outcome of vascular damage in systemic lupus erythematosus. Lupus
18: 508-515
[Abstract]
Cypiene, A, Kovaite, M, Venalis, A, Dadoniene, J, Rugiene, R, Petrulioniene, Z, Ryliskyte, L, Laucevicius, A
(2009). Arterial wall dysfunction in systemic lupus erythematosus. Lupus
18: 522-529
[Abstract]
O'Neill, S. G., Pego-Reigosa, J. M., Hingorani, A. D., Bessant, R., Isenberg, D. A., Rahman, A.
(2009). Use of a strategy based on calculated risk scores in managing cardiovascular risk factors in a large British cohort of patients with systemic lupus erythematosus. Rheumatology (Oxford)
48: 573-575
[Abstract][Full Text]
Greco, C. M., Kao, A. H., Sattar, A., Danchenko, N., Maksimowicz-McKinnon, K. M., Edmundowicz, D., Sutton-Tyrrell, K., Tracy, R. P., Kuller, L. H., Manzi, S.
(2009). Association between depression and coronary artery calcification in women with systemic lupus erythematosus. Rheumatology (Oxford)
48: 576-581
[Abstract][Full Text]
Reiss, A. B., Wan, D. W., Anwar, K., Merrill, J. T., Wirkowski, P. A., Shah, N., Cronstein, B. N., Chan, E. S. L., Carsons, S. E.
(2009). A BRIEF COMMUNICATION: Enhanced CD36 Scavenger Receptor Expression in THP-1 Human Monocytes in the Presence of Lupus Plasma: Linking Autoimmunity and Atherosclerosis. Exp Biol Med
234: 354-360
[Abstract][Full Text]
MANZI, S.
(2009). Lupus update: Perspective and clinical pearls. Cleveland Clinic Journal of Medicine
76: 137-142
[Abstract][Full Text]
NIKPOUR, M., GLADMAN, D. D., IBANEZ, D., BRUCE, I. N., BURNS, R. J., UROWITZ, M. B.
(2009). Myocardial Perfusion Imaging in Assessing Risk of Coronary Events in Patients with Systemic Lupus Erythematosus. The Journal of Rheumatology
36: 288-294
[Abstract][Full Text]
Shang, Q, Tam, L., Li, E., Yip, G., Yu, C.
(2008). Increased arterial stiffness correlated with disease activity in systemic lupus erythematosus. Lupus
17: 1096-1102
[Abstract]
Chan, M. Y., Andreotti, F., Becker, R. C.
(2008). Hypercoagulable States in Cardiovascular Disease. Circulation
118: 2286-2297
[Full Text]
Grisar, J., Steiner, C. W., Bonelli, M., Karonitsch, T., Schwarzinger, I., Weigel, G., Steiner, G., Smolen, J. S.
(2008). Systemic lupus erythematosus patients exhibit functional deficiencies of endothelial progenitor cells. Rheumatology (Oxford)
47: 1476-1483
[Abstract][Full Text]
Sabio, J., Zamora-Pasadas, M, Jimenez-Jaimez, J, Albadalejo, F, Vargas-Hitos, J, Rodriguez del Aguila, M., Hidalgo-Tenorio, C, Gonzalez-Gay, M., Alonso, J.
(2008). Metabolic syndrome in patients with systemic lupus erythematosus from Southern Spain. Lupus
17: 849-859
[Abstract]
Mandelbrot, D. A., Santos, P. W., Burt, R. K., Oyama, Y., Block, G. A., Ahya, S. N., Rosa, R. M., Traynor, A. E.
(2008). Resolution of SLE-related soft-tissue calcification following haematopoietic stem cell transplantation. Nephrol Dial Transplant
23: 2679-2684
[Abstract][Full Text]
Roldan, C. A
(2008). Valvular and coronary heart disease in systemic inflammatory diseases. Heart
94: 1089-1101
[Full Text]
Mathieu, S., Joly, H., Baron, G., Tournadre, A., Dubost, J.-J., Ristori, J.-M., Lusson, J.-R., Soubrier, M.
(2008). Trend towards increased arterial stiffness or intima-media thickness in ankylosing spondylitis patients without clinically evident cardiovascular disease. Rheumatology (Oxford)
47: 1203-1207
[Abstract][Full Text]
Wright, S A, O'Prey, F M, McHenry, M T, Leahey, W J, Devine, A B, Duffy, E M, Johnston, D G, Finch, M B, Bell, A L, McVeigh, G E
(2008). A randomised interventional trial of {omega}-3-polyunsaturated fatty acids on endothelial function and disease activity in systemic lupus erythematosus. Ann Rheum Dis
67: 841-848
[Abstract][Full Text]
Shoenfeld, Y., Meroni, P. L., Cervera, R.
(2008). Antiphospholipid syndrome dilemmas still to be solved: 2008 status. Ann Rheum Dis
67: 438-442
[Full Text]
Lee, S-S., Singh, S., Magder, L., Petri, M.
(2008). Predictors of high sensitivity C-reactive protein levels in patients with systemic lupus erythematosus. Lupus
17: 114-123
[Abstract]
Bertsias, G, Ioannidis, J P A, Boletis, J, Bombardieri, S, Cervera, R, Dostal, C, Font, J, Gilboe, I M, Houssiau, F, Huizinga, T, Isenberg, D, Kallenberg, C G M, Khamashta, M, Piette, J C, Schneider, M, Smolen, J, Sturfelt, G, Tincani, A, van Vollenhoven, R, Gordon, C, Boumpas, D T
(2008). EULAR recommendations for the management of systemic lupus erythematosus. Report of a Task Force of the EULAR Standing Committee for International Clinical Studies Including Therapeutics. Ann Rheum Dis
67: 195-205
[Abstract][Full Text]
Avalos, I., Chung, C. P., Oeser, A., Milne, G. L., Borntrager, H., Morrow, J. D., Raggi, P., Solus, J., Stein, C. M.
(2007). Aspirin therapy and thromboxane biosynthesis in systemic lupus erythematosus. Lupus
16: 981-986
[Abstract]
Roman, M. J., Salmon, J. E.
(2007). Cardiovascular Manifestations of Rheumatologic Diseases. Circulation
116: 2346-2355
[Full Text]
Lazzerini, P.E., Capecchi, P.L., Selvi, E., Lorenzini, S., Bisogno, S., Galeazzi, M., Laghi Pasini, F.
(2007). Hyperhomocysteinemia: a cardiovascular risk factor in autoimmune diseases?. Lupus
16: 852-862
[Abstract]
Martinez-Berriotxoa, A., Ruiz-Irastorza, G., Egurbide, M.-V., Garmendia, M., Gabriel Erdozain, J., Villar, I., Aguirre, C.
(2007). Transiently positive anticardiolipin antibodies and risk of thrombosis in patients with systemic lupus erythematosus. Lupus
16: 810-816
[Abstract]
Knockaert, D. C.
(2007). Cardiac involvement in systemic inflammatory diseases. Eur Heart J
28: 1797-1804
[Abstract][Full Text]
O'Neill, S. G, Isenberg, D. A, Rahman, A.
(2007). Could antibodies to C-reactive protein link inflammation and cardiovascular disease in patients with systemic lupus erythematosus?. Ann Rheum Dis
66: 989-991
[Full Text]
Gautier, E. L., Huby, T., Ouzilleau, B., Doucet, C., Saint-Charles, F., Gremy, G., Chapman, M. J., Lesnik, P.
(2007). Enhanced Immune System Activation and Arterial Inflammation Accelerates Atherosclerosis in Lupus-Prone Mice. Arterioscler. Thromb. Vasc. Bio.
27: 1625-1631
[Abstract][Full Text]
Edwards, N. C., Ferro, C. J., Townend, J. N., Steeds, R. P.
(2007). Myocardial disease in systemic vasculitis and autoimmune disease detected by cardiovascular magnetic resonance. Rheumatology (Oxford)
46: 1208-1209
[Full Text]
Ahmad, Y., Shelmerdine, J., Bodill, H., Lunt, M., Pattrick, M. G., Teh, L. S., Bernstein, R. M., Walker, M. G., Bruce, I. N.
(2007). Subclinical atherosclerosis in systemic lupus erythematosus (SLE): the relative contribution of classic risk factors and the lupus phenotype. Rheumatology (Oxford)
46: 983-988
[Abstract][Full Text]
Chaiamnuay, S., Bertoli, A. M, Roseman, J. M, McGwin, G., Apte, M., Duran, S., Vila, L. M, Reveille, J. D, Alarcon, G. S
(2007). African-American and Hispanic ethnicities, renal involvement and obesity predispose to hypertension in systemic lupus erythematosus: results from LUMINA, a multiethnic cohort (LUMINAXLV). Ann Rheum Dis
66: 618-622
[Abstract][Full Text]
Ait-Oufella, H., Kinugawa, K., Zoll, J., Simon, T., Boddaert, J., Heeneman, S., Blanc-Brude, O., Barateau, V., Potteaux, S., Merval, R., Esposito, B., Teissier, E., Daemen, M. J., Leseche, G., Boulanger, C., Tedgui, A., Mallat, Z.
(2007). Lactadherin Deficiency Leads to Apoptotic Cell Accumulation and Accelerated Atherosclerosis in Mice. Circulation
115: 2168-2177
[Abstract][Full Text]
Korkmaz, C., Cansu, D.U., Kasifoglu, T.
(2007). Myocardial infarction in young patients (<=35 years of age) with systemic lupus erythematosus: a case report and clinical analysis of the literature. Lupus
16: 289-297
[Abstract]
von Lukowicz, T., Silacci, M., Wyss, M. T., Trachsel, E., Lohmann, C., Buck, A., Luscher, T. F., Neri, D., Matter, C. M.
(2007). Human Antibody Against C Domain of Tenascin-C Visualizes Murine Atherosclerotic Plaques Ex Vivo. JNM
48: 582-587
[Abstract][Full Text]
Feng, X., Li, H., Rumbin, A. A., Wang, X., La Cava, A., Brechtelsbauer, K., Castellani, L. W., Witztum, J. L., Lusis, A. J., Tsao, B. P.
(2007). ApoE-/-Fas-/- C57BL/6 mice: a novel murine model simultaneously exhibits lupus nephritis, atherosclerosis, and osteopenia. J. Lipid Res.
48: 794-805
[Abstract][Full Text]
Avalos, I, Chung, C P, Oeser, A, Milne, G L, Morrow, J D, Gebretsadik, T, Shintani, A, Yu, C, Stein, C M
(2007). Oxidative stress in systemic lupus erythematosus: relationship to disease activity and symptoms. Lupus
16: 195-200
[Abstract]
Chung, C. P, Avalos, I., Oeser, A., Gebretsadik, T., Shintani, A., Raggi, P., Michael Stein, C
(2007). High prevalence of the metabolic syndrome in patients with systemic lupus erythematosus: association with disease characteristics and cardiovascular risk factors. Ann Rheum Dis
66: 208-214
[Abstract][Full Text]
Kavey, R.-E. W., Allada, V., Daniels, S. R., Hayman, L. L., McCrindle, B. W., Newburger, J. W., Parekh, R. S., Steinberger, J.
(2006). Cardiovascular Risk Reduction in High-Risk Pediatric Patients: A Scientific Statement From the American Heart Association Expert Panel on Population and Prevention Science; the Councils on Cardiovascular Disease in the Young, Epidemiology and Prevention, Nutrition, Physical Activity and Metabolism, High Blood Pressure Research, Cardiovascular Nursing, and the Kidney in Heart Disease; and the Interdisciplinary Working Group on Quality of Care and Outcomes Research: Endorsed by the American Academy of Pediatrics. Circulation
114: 2710-2738
[Abstract][Full Text]
La Rosa, J C
(2006). Atherosclerotic vascular disease in systemic lupus erythematosus and related disorders. Lupus
15: 35-38
[Abstract]
Sinclair, A, Baildon, R
(2006). Mycophenolate mofetil: an overview. Lupus
15: 70-77
Yang, M.-L., Doyle, H. A., Gee, R. J., Lowenson, J. D., Clarke, S., Lawson, B. R., Aswad, D. W., Mamula, M. J.
(2006). Intracellular Protein Modification Associated with Altered T Cell Functions in Autoimmunity. J. Immunol.
177: 4541-4549
[Abstract][Full Text]
Chung, C P, Oeser, A, Avalos, I, Raggi, P, Stein, C M
(2006). Cardiovascular risk scores and the presence of subclinical coronary artery atherosclerosis in women with systemic lupus erythematosus. Lupus
15: 562-569
[Abstract]
Ruiz-Irastorza, G, Egurbide, M-V, Pijoan, J-I, Garmendia, M, Villar, I, Martinez-Berriotxoa, A, Erdozain, J-G, Aguirre, C
(2006). Effect of antimalarials on thrombosis and survival in patients with systemic lupus erythematosus. Lupus
15: 577-583
[Abstract]
Bagi, Z, Hamar, P, Kardos, M, Koller, A
(2006). Lack of flow mediated dilation and enhanced angiotensin II-induced constriction in skeletal muscle arterioles of lupus-prone autoimmune mice. Lupus
15: 326-334
[Abstract]
Stanic, A. K., Stein, C. M., Morgan, A. C., Fazio, S., Linton, M. F., Wakeland, E. K., Olsen, N. J., Major, A. S.
(2006). Immune dysregulation accelerates atherosclerosis and modulates plaque composition in systemic lupus erythematosus. Proc. Natl. Acad. Sci. USA
103: 7018-7023
[Abstract][Full Text]
D'Cruz, D. P
(2006). Systemic lupus erythematosus.. BMJ
332: 890-894
[Full Text]
Mannino, D. M., Watt, G., Hole, D., Gillis, C., Hart, C., McConnachie, A., Davey Smith, G., Upton, M., Hawthorne, V., Sin, D. D., Man, S. F. P., Van Eeden, S., Mapel, D. W., Vestbo, J.
(2006). The natural history of chronic obstructive pulmonary disease.. Eur Respir J
27: 627-643
[Full Text]
Shaw, L. J., Bairey Merz, C. N., Pepine, C. J., Reis, S. E., Bittner, V., Kelsey, S. F., Olson, M., Johnson, B. D., Mankad, S., Sharaf, B. L., Rogers, W. J., Wessel, T. R., Arant, C. B., Pohost, G. M., Lerman, A., Quyyumi, A. A., Sopko, G., for the WISE Investigators,
(2006). Insights From the NHLBI-Sponsored Women's Ischemia Syndrome Evaluation (WISE) Study: Part I: Gender Differences in Traditional and Novel Risk Factors, Symptom Evaluation, and Gender-Optimized Diagnostic Strategies. J Am Coll Cardiol
47: S4-S20
[Abstract][Full Text]
Garcia, M A, Marcos, J C, Marcos, A I, Pons-Estel, B A, Wojdyla, D, Arturi, A, Babini, J C, Catoggio, L J, Alarcon-Segovia, D
(2005). Male systemic lupus erythematosus in a Latin-American inception cohort of 1214 patients. Lupus
14: 938-946
[Abstract]
Lin, C.-H., Lee, M.-L., Hsu, R.-B.
(2005). Cardiac surgery in patients with systemic lupus erythematosus. ICVTS
4: 618-621
[Abstract][Full Text]
Hall, F. C., Dalbeth, N.
(2005). Disease modification and cardiovascular risk reduction: two sides of the same coin?. Rheumatology (Oxford)
44: 1473-1482
[Abstract][Full Text]
Bruce, I. N.
(2005). 'Not only...but also': factors that contribute to accelerated atherosclerosis and premature coronary heart disease in systemic lupus erythematosus. Rheumatology (Oxford)
44: 1492-1502
[Abstract][Full Text]
Mineo, C., Gormley, A. K., Yuhanna, I. S., Osborne-Lawrence, S., Gibson, L. L., Hahner, L., Shohet, R. V., Black, S., Salmon, J. E., Samols, D., Karp, D. R., Thomas, G. D., Shaul, P. W.
(2005). Fc{gamma}RIIB Mediates C-Reactive Protein Inhibition of Endothelial NO Synthase. Circ. Res.
97: 1124-1131
[Abstract][Full Text]
Cardoso, C R., Sales, M A., Papi, J A., Salles, G F
(2005). QT-interval parameters are increased in systemic lupus erythematosus patients. Lupus
14: 846-852
[Abstract]
Hildbrand, P., Eigenmann, C., Gugger, M., Marti, H.P., Hullin, R.
(2005). Pre-eclampsia with acute heart failure postpartum as primary manifestation of systemic lupus erythematosus. Eur J Heart Fail
7: 1057-1058
[Abstract][Full Text]
Feinbloom, D., Bauer, K. A.
(2005). Assessment of Hemostatic Risk Factors in Predicting Arterial Thrombotic Events. Arterioscler. Thromb. Vasc. Bio.
25: 2043-2053
[Abstract][Full Text]
Pinn, V. W.
(2005). Research on Women's Health: Progress and Opportunities. JAMA
294: 1407-1410
[Full Text]
Frostegard, J.
(2005). Atherosclerosis in Patients With Autoimmune Disorders. Arterioscler. Thromb. Vasc. Bio.
25: 1776-1785
[Abstract][Full Text]
Calvo-Alen, J., Alarcon, G. S., Campbell, R. Jr, Fernandez, M., Reveille, J. D., Cooper, G. S.
(2005). Lack of recording of systemic lupus erythematosus in the death certificates of lupus patients. Rheumatology (Oxford)
44: 1186-1189
[Abstract][Full Text]
Barnes, E V, Narain, S, Naranjo, A, Shuster, J, Segal, M S, Sobel, E S, Armstrong, A E, Santiago, B E, Reeves, W H, Richards, H B
(2005). High sensitivity C-reactive protein in systemic lupus erythematosus: relation to disease activity, clinical presentation and implications for cardiovascular risk. Lupus
14: 576-582
[Abstract]
Binstadt, B. A., Levine, J. C., Nigrovic, P. A., Gauvreau, K., Dedeoglu, F., Fuhlbrigge, R. C., Weindling, S. N., Newburger, J. W., Sundel, R. P.
(2005). Coronary Artery Dilation Among Patients Presenting With Systemic-Onset Juvenile Idiopathic Arthritis. Pediatrics
116: e89-e93
[Abstract][Full Text]
Buyon, J. P., Petri, M. A., Kim, M. Y., Kalunian, K. C., Grossman, J., Hahn, B. H., Merrill, J. T., Sammaritano, L., Lockshin, M., Alarcon, G. S., Manzi, S., Belmont, H. M., Askanase, A. D., Sigler, L., Dooley, M. A., Von Feldt, J., McCune, W. J., Friedman, A., Wachs, J., Cronin, M., Hearth-Holmes, M., Tan, M., Licciardi, F.
(2005). The Effect of Combined Estrogen and Progesterone Hormone Replacement Therapy on Disease Activity in Systemic Lupus Erythematosus: A Randomized Trial. ANN INTERN MED
142: 953-962
[Abstract][Full Text]
Birdas, T. J., Landis, J. T., Haybron, D., Evers, D., Papasavas, P. K., Caushaj, P. F.
(2005). Outcomes of Coronary Artery Bypass Grafting in Patients With Connective Tissue Diseases. Ann. Thorac. Surg.
79: 1610-1614
[Abstract][Full Text]
Andreotti, F., Becker, R. C.
(2005). Atherothrombotic Disorders: New Insights From Hematology. Circulation
111: 1855-1863
[Full Text]
Jadoul, M
(2005). Optimal care of lupus nephritis patients. Lupus
14: 72-76
[Abstract]
Cederholm, A., Svenungsson, E., Jensen-Urstad, K., Trollmo, C., Ulfgren, A.-K., Swedenborg, J., Fei, G.-Z., Frostegard, J.
(2005). Decreased Binding of Annexin V to Endothelial Cells: A Potential Mechanism in Atherothrombosis of Patients With Systemic Lupus Erythematosus. Arterioscler. Thromb. Vasc. Bio.
25: 198-203
[Abstract][Full Text]
Marasini, B, De Monti, M, Ghilardi, G
(2005). Risk factors for accelerated atherosclerosis in patients with systemic lupus erythematosus. Ann Rheum Dis
64: 163-164
[Full Text]
Hellmann, D. B.
(2004). Update in Rheumatology. ANN INTERN MED
141: 801-804
[Full Text]
Seyahi, E., Memisoglu, E., Hamuryudan, V., Tepe, S., Aker, U. T., Balci, H., Ongen, Z., Yurdakul, S., Yazici, H.
(2004). Coronary atherosclerosis in Behcet's syndrome: a pilot study using electron-beam computed tomography. Rheumatology (Oxford)
43: 1448-1450
[Full Text]
Sabio, J. M., Jimenez-Alonso, J., Tanvetyanon, T., Jacobsen, S., Garred, P.
(2004). Arterial Thrombosis in Systemic Lupus Erythematosus. NEJM
351: 1910-1911
[Full Text]
Houssiau, F. A.
(2004). Management of Lupus Nephritis: An Update. J. Am. Soc. Nephrol.
15: 2694-2704
[Full Text]
Bruce, I. N
(2004). Coronary heart disease (CHD) in lupus: round up the usual suspects?. Lupus
13: 557-560
Gorman, C., Isenberg, D.
(2004). Atherosclerosis and lupus. Rheumatology (Oxford)
43: 943-945
[Full Text]
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