Atherosclerosis and connective tissue diseases

doi:10.1016/S1297-319X(01)00330-X

Joint Bone Spine

Volume 68, Issue 6, December 2001, Pages 564-575

https://doi.org/10.1016/S1297-319X(01)00330-X Get rights and content

Abstract

Large increases in mortality related to premature atherosclerosis with coronary artery disease and stroke have been reported in patients with systemic lupus erythematosus (SLE), antiphospholipid syndrome (APLS), or rheumatoid arthritis (RA). Studies found relative risks of 5 for myocardial infarction, 6 to 10 for stroke in SLE patients, and 3.6 for cardiovascular deaths in RA patients. The main risk factors for atherosclerosis included not only the classic factors identified in epidemiological studies such as the Framingham study (advanced age, high cholesterol levels, hypertension, diabetes mellitus, and obesity), but also prolonged glucocorticoid therapy, long duration of SLE, postmenopausal status, and heart failure. SLE per se is an independent risk factor. The current pathogenic hypothesis for atherosclerosis involves an inflammatory response (erythrocyte sedimentation rate, C-reactive protein, and fibrin), autoantibodies, immune complexes (containing antibodies to phospholipids, to oxidized LDLs, and to endothelial cells), cytokine-producing activated T cells, and bacterial or viral infections responsible for an immune response against heat shock proteins (endogenous HSP60 and its equivalent, bacterial HSP65). Early risk factor intervention and effective control of inflammation should be incorporated into the management of connective tissue disease with the goal of protecting patients against atherosclerosis.

Section snippets

Epidemiologiy of cardiovascular and cerebrovascular disease in patients with conenctive tissue disease: the example of SLE

SLE, a disease with a marked predominance in women, is commonly responsible for angina and myocardial infarction, which can be fatal. As early as 1976, Urowitz et al. showed that mortality over time is bimodal in patients with SLE: in their series of 110 patients, there were six early deaths related to SLE activity or to infectious complications and five deaths after a mean follow-up of 8.6 years, of which four were caused by myocardial infarction. This contribution of cardiovascular disease to

Atherosclerosis and rheumatoid arthritis

Although more fragmentary, data on rheumatoid arthritis (RA) are consistent with those on SLE: several large epidemiological studies found excess cardiovascular mortality in RA patients as compared to controls 33, 34, 35, 36, 37, 38, 39. This excess mortality, expressed as the standardized mortality ratio (SMR), ranged from 1.3 to 3.64, with this higher value being obtained in women aged 15 to 49 years. Myocardial infarction was the main source of excess mortality (SMR, 1.54). Whether RA

Main risk factors for atherosclerosis

Prospective epidemiological studies conducted from 1947 onward, such as the Framingham study, have played a major role in confirming the main risk factors for atherosclerosis, some of which, including hypercholesterolemia, were first identified in 1913 by the Russian pathologists Anitschkov and Chalatov. Table III recapitulates the risk factors identified in these studies. Recently identified risk factors are biochemical or immunological characteristics whose relative impact requires

Lupus and risk factors for atherosclerosis

Classic risk factors for atherosclerosis are often present in SLE patients, as shown by a prospective study in a cohort of 264 patients 〚2〛 with a total number of visits of 3,000. Nine factors yielded significant odds ratios as predictors of CAD (table IV). The cumulative glucocorticoid dose was a risk factor, whereas a high daily dosage was not 〚2〛. Hypercholesterolemia was also a risk factor for CAD in the multiple logistic regression model; the mean maximal level was 2.72 g/L in patients

Rheumatoid arthritis and risk factors for cardiovacular events

Studies of classic risk factors for CAD in patients with RA found that the following factors were associated with excess cardiovascular mortality: male gender, older age at RA onset, arterial hypertension, a previous cardiovascular event, and a numerous joints with inflammation 〚44〛.

Other classic risk factors seem associated with ischemic cardiovascular events of any kind 〚39〛: high body mass index, elevations in parameters for inflammation (erythrocyte sedimentation rate, C-reactive protein,

Pathogenesis of atherosclerosis

Atherosclerosis is a multifactorial disease. Genetic, environmental, metabolic, inflammatory, infectious, and immunological factors have been implicated 〚47〛. Although plaque build-up in arteries results from accumulation of lipids within the artery wall, hyperlipidemia is not the sole determinant of atherosclerosis. One of the events that initiates the vascular lesion is penetration of atherogenic lipoproteins within the arterial intima, where they remain captive in the subendothelial matrix

Chronic inflammation

Inflammatory reactions associated with vascular alterations seem to play a major role in the development of atheromatous plaque 〚50〛. Epidemiological studies have established that a high C-reactive protein level is an independent risk factor for myocardial infarction and stroke in men with or without other risk factors 〚51〛. The efficacy of statins in secondary prevention may be ascribable in part to their ability to return C-reactive protein levels to normal 〚52〛 and in part to their

How can cardiovascular morbidity/mortality be reduced in patients with connective tissue disease?

A retrospective study in 24 Canadian patients (18 women and six men) with a history of myocardial infarction or unstable angina identified the following risk factors: hypertension (n = 16), obesity (n = 19), smoking (n = 16), hypercholesterolemia (n = 11), glucocorticoid use (n = 22), hyperglycemia (n = 4), and cardiac involvement with SLE (n = 4). 〚92〛. Only half these patients had been offered appropriate risk reduction interventions.

Clearly, early prevention of atheroma is essential given

Conclusion

Connective tissue disease, most notably SLE and antiphospholipid syndrome, are characterized by a high incidence of ischemic coronary and cerebral events. These events are associated not only with the classic risk factors but also with the treatments used (glucocorticoids, methotrexate, etc.) and with the inflammatory disease itself, which exhibits many etiopathogenic similarities with atheroma. The major excess mortality from atheroma seen in patients with connective tissue disease requires

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Cited by (27)

Mean platelet volume and β-thromboglobulin levels in familial mediterranean fever: Effect of colchicine use?
2012, European Journal of Internal Medicine
Citation Excerpt :
In recent years the possible causative role of systemic inflammation in some rheumatic diseases on atherosclerosis development have been investigated [9–11]. Increased mortality rates were determined to be associated with early atherosclerosis development in patients with Systemic Lupus Erythematosus, antiphospholipid syndrome and rheumatoid arthritis [12]. A few of the recent studies revealed that risk of atherosclerosis had increased in FMF patients [13–16].
Many studies have shown that subclinical inflammation persisted during remission period of Familial Mediterranean Fever (FMF) patients but long term effects of subclinical inflammation in these patients aren't clearly known. Besides, a few of the recent studies revealed that risk of atherosclerosis had increased in FMF patients. β-Thromboglobulin (β-TG) is considered as a sensitive marker of platelet activation. In this study Mean Platelet Volume (MPV) and β-TG levels were evaluated in FMF patients.
Following the Local Ethics Committee's consent, 25 FMF patients were included in the study. Twenty eight age and sex matched healthy volunteers were recruited as a control group. Lipid profile, inflammatory parameters, hemogram, β-TG, MPV were assessed. Statistical analysis was performed with SPSS for Windows 16.00.
Group I consisted of 25 FMF cases (16 females, 9 males; mean age: 35.72 ± 12.34 years), Group II consisted of 28 cases (22 females, 6 males; mean age 31.78 ± 10.31 years). There was no statistically significant difference between the groups in terms of age and gender distribution, smoking status, total cholesterol, triglyceride, LDL and MPV (p > 0.05). HDL levels were found to be statistically lower in Group I (p:0.04). Median β-TG levels was significantly higher in Group II than Group I (129.50 (range:372.00) ng/mL versus 104.00 (range:212.80) ng/mL respectively; p:0.03).
In this study MPV and β-TG were evaluated for FMF cases and healthy controls, β-TG levels were found significantly lower among patients; we hypothesized that this difference may have resulted from the effect of colchicine use on platelet functions.
Anti-CRP antibodies in lupus
2010, Revue du Rhumatisme (Edition Francaise)
La protéine C-réactive (CRP) est une protéine de la phase aiguë de l’inflammation dont la concentration plasmatique augmente très rapidement lors d’une réaction inflammatoire (× 1000). La CRP appartient à une famille de protéines appelées pentraxines, dont une propriété importante est d’opsoniser les cellules en apoptose, permettant leur phagocytose sans déclencher de réaction inflammatoire telle que celle observée en cas de nécrose cellulaire. Les taux faibles de CRP dans le lupus participeraient au défaut d’épuration des particules d’apoptose et favoriseraient l’auto-immunité vis-à-vis des constituants des vésicules d’apoptose. Le taux sérique de la CRP dans une population normale est inférieure à 5 ou 10 mg/l. Un dosage ultrasensible montre que, dans cette zone dite normale, la population générale se répartit en cinq « quintiles » ; les sujets occupant le quintile supérieur en permanence font plus de décès cardiovasculaires et de récidives d’infarctus que les sujets du quintile le plus bas. Ainsi, la CRP us est-elle un facteur de risque vasculaire au même titre que les facteurs classiques de Framingham. La CRP intervient dans la physiopathologie de l’athérome par ses propriétés chimiotactiques vis-à-vis des macrophages qui constitueront les cellules spumeuses de la plaque d’athérome. Toute maladie inflammatoire chronique qui augmente la production de CRP peut conduire à un athérome accéléré. Paradoxalement, l’inflammation lupique s’accompagne d’une augmentation relativement faible de la CRP, suffisante cependant pour augmenter le risque cardiovasculaire. Les auto-anticorps anti-CRP, détectés chez 35 à 40 % des lupiques sont susceptibles de majorer ce risque en interagissant avec la forme monomérique (dégradée) de la CRP. Les complexes immuns CRP anti-CRP formés dans la paroi artérielle favoriseraient la croissance de la plaque d’athérome.
Anti-CRP antibodies in systemic lupus erythematosus
2010, Joint Bone Spine
C-reactive protein (CRP) is an acute-phase protein whose concentration rises sharply during the inflammatory response (1000-fold). CRP belongs to the pentraxin family of proteins, of which a key property is the ability to opsonize apoptotic cells, which can then undergo phagocytosis without triggering an inflammatory response, in marked contrast to the phagocytosis of necrotic cells. The low CRP concentrations in patients with systemic lupus erythematosus (SLE) may contribute to defective clearance of apoptotic particles, thereby promoting the development of autoimmunity to apoptotic vesicle components. In normal populations, serum CRP concentrations remain below 5–10 mg/L. Within this normal range, five quintiles of CRP concentrations can be distinguished using an ultrasensitive CRP assay. Individuals who are consistently within the highest quintile are at higher risk for cardiovascular death and recurrent myocardial infarction than are individuals in the lowest quintile. Thus, the ultrasensitive CRP concentration (US-CRP) is a cardiovascular risk factor, together with the classic risk factors identified by the Framingham studies. CRP plays a role in atheroma plaque development via its ability to attract macrophages, which convert to foam cells. Any chronic inflammatory disease associated with increased CRP production can accelerate the development of atheroma. Paradoxically, the inflammatory process in patients with SLE is associated with a fairly small elevation of serum CRP concentrations. Nevertheless, this elevation is sufficient to increase the cardiovascular risk. Anti-CRP autoantibodies, which are found in 35 to 40% of SLE patients, increase the cardiovascular risk by interacting with the monomeric (degraded) form of CRP. CRP/anti-CRP immune complexes developed in the arterial wall may promote growth of the atheroma plaque.
Rheumatoid Arthritis
2010, Current Clinical Medicine: Expert Consult Premium Edition - Enhanced Online Features and Print
Auto-antibodies do not influence development of atherosclerotic plaques in rheumatoid arthritis
2008, Joint Bone Spine
Citation Excerpt :
Several diagnostic methods such as carotid ultrasound (US), myocardium perfusion scintillography, and coronary artery angiography showed that rheumatoid arthritis (RA) patients have a high frequency of carotid atherosclerosis, cerebrovascular, ischemic, and coronary disease [1–5]. In fact, a higher risk of cardiovascular events was observed in RA compared to general population [6] and attention should be given to conventional risk factors [6–8]. In normal population, besides the important role of dyslipoproteinemia, systemic arterial hypertension and smoking in the pathogenesis of atherosclerosis, some markers of systemic inflammation such as fibrinogen and C-reactive protein (CRP) have also been implicated to this risk which supports the notion that this process is a consequence of an inflammatory process in artery vessels [9,10].
Many questions remain unanswered about premature atherosclerosis in rheumatoid arthritis (RA). Besides inflammation, some studies have suggested the role of autoantibodies on its pathogenesis.
The aim of this study was to investigate the presence of antibodies against phospholipids, beta2-glycoprotein1 (beta2-gp1), lipoprotein lipase, and heat shock proteins (Hsp) in RA patients and to evaluate their possible association with subclinical carotid atherosclerosis.
Seventy-one RA patients and 53 age- and sex-matched controls were selected to perform anticardiolipin antibodies (aCL) (IgG and IgM), anti-beta2-gp1 (IgG, IgM, and IgA), anti-lipoprotein lipase (anti-LPL), anti-Hsp 60, and anti-Hsp 65 by ELISA tests. Intima-medial thickness (IMT) of common carotid and presence of plaques were assessed by high-resolution B-mode ultrasonography. Exclusion criteria were smoking, diabetes, and arterial hypertension. Lipoproteins, erythrocyte sedimentation rate (ESR), C-reactive protein (CRP), and fibrinogen levels, as well as health assessment questionnaire (HAQ) and disease activity score (DAS) 28 were also evaluated.
Age (48.93 ± 12.31 vs. 45.37 ± 9.37 years; p = 0.20) and body mass index (BMI) (p = 0.69) were similar in RA and controls, as well as female gender (p = 0.56). The mean IMT was similar between RA and controls (0.721 ± 0.16 vs. 0.667 ± 0.14 mm, p = 0.07) but the frequency of plaques was higher in RA (14.1% vs. 1.9%; p = 0.02). In RA patients, IMT measurements did not differ according to the presence or absence of these antibodies: IgG aCL (0.62 ± 0.64 vs. 0.72 ± 0.17 mm, p = 0.24), IgM aCL (0.65 ± 0.79 vs. 0.73 ± 0.17 mm, p = 0.33), anti-Hsp 60 (0.78 ± 0.20 vs. 0.71 ± 0.16 mm, p = 0.27), anti-Hsp 65 (0.73 ± 0.16 vs. 0.72 ± 0.17 mm, p = 0.77), IgG anti-beta2-gp1 (0.73 ± 0.16 vs. 0.71 ± 0.17 mm, p = 0.72), and anti-CCP (0.71 ± 0.16 vs. 0.76 ± 0.20 mm, p = 0.36). In addition, IMT did not correlate with antibodies titers: IgG aCL (r = − 0.09, p = 0.47), IgM aCL (r = − 0.15, p = 0.21), anti-Hsp 60 (r = 0.10, p = 0.42), anti-Hsp 65 (r = 0.05, p = 0.69), IgG anti-beta2-gp1 (r = − 0.07, p = 0.57), IgM anti-beta2-gp1 (r = − 0.05, p = 0.69), IgA anti-beta2-gp1 (r = 0.03, p = 0.79), and anti-CCP (r = − 0.07, p = 0.57). RA patients with plaques had a significantly higher age compared to those without plaques (p = 0.001), as well as higher mean IMT (p < 0.001), total cholesterol (p = 0.001), and LDL (p = 0.003).
In RA a clear association between all autoantibodies studied herein and increased IMT or presence of plaques was not observed. The great prevalence of carotid atherosclerosis in RA was related to age, total and LDL cholesterol, as identified in normal population.
Severe atherosclerosis in rheumatoid arthritis and hyperhomocysteinemia: Is there a link?
2008, Joint Bone Spine
Citation Excerpt :
Finally, anticoagulant and antiplatelet therapy was given, as well as a statin. RA is associated with a high risk of cardiovascular morbidity and mortality [1–4]. The standardized mortality ratio for cardiovascular disease has ranged across studies from 1.3 to 2.4 in RA patients [1,3,4].
Rheumatoid arthritis (RA) is a chronic inflammatory joint disease whose main complication is accelerated atheroma responsible for high rates of cardiovascular morbidity and mortality. Hyperhomocysteinemia is among the factors incriminated in RA-associated atheroma. We managed a 46-year-old patient with RA who required admission to evaluate severe arterial and venous disease with involvement of the coronary, renal, and peripheral arteries. She had no laboratory evidence of rheumatoid vasculitis or conventional cardiovascular risk factors (diabetes and hypercholesterolemia) and had never smoked. Her serum homocysteine level was elevated to 20.9 μmol/L as a result of a homozygous C667T mutation in the methylenetetrahydrofolate (MTHFR) gene. Folate and vitamin B12 levels were normal. A circulating anticoagulant was identified.
Hyperhomocysteinemia, which is defined as a homocysteine level greater than 15 μmol/L, is a risk factor for arterial and venous disease. Hyperhomocysteinemia is found in 20%–42% of patients with RA. Methotrexate therapy is the most common causative factor. Other causes include MTHFR deficiency, vitamin B12 deficiency, renal failure, old age, and smoking. Whatever the underlying cause, folic acid supplementation returns the homocysteine level to normal.

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SHORT SURVEYAtherosclerosis and connective tissue diseases

Abstract

Section snippets

Epidemiologiy of cardiovascular and cerebrovascular disease in patients with conenctive tissue disease: the example of SLE

Atherosclerosis and rheumatoid arthritis

Main risk factors for atherosclerosis

Lupus and risk factors for atherosclerosis

Rheumatoid arthritis and risk factors for cardiovacular events

Pathogenesis of atherosclerosis

Chronic inflammation

How can cardiovascular morbidity/mortality be reduced in patients with connective tissue disease?

Conclusion

Semin Arthritis Rheum

Am J M

Am J M

Am J M

Am J M

J Chron Dis

Lancet

Blood

Lancet

Immunol Today

Lancet

Clin Immunol

Atherosclerosis

Clin Immunol Immunopathol

Évolution des théories sur l'athérosclérose

Rev Prat

Detection of coronary artery disease and the role of traditional risk factors in the Hopkins lupus cohort

Lupus

The bimodal mortality pattern of systemic lupus erythematosus

Am J M

Mortality in lupus nephritis

Arthritis Rheum

Systemic lupus erythematosus - survival patterns : experience with 609 patients

J Am Med Assoc

A multicenter study of outcome in systemic lupus erythematosus. II. Causes of death

Arthritis Rheum

Prevalence and mortality rates of systemic lupus erythematosus and causes of death in SLE patients in Finland

Scand J Rheumatol

Mortality in systemic lupus erythematosus : the bimodal pattern revisited

Q J M

Outcome in systemic lupus erythematosus : a prospective study of patients from a defined population

Medicine

Ischemic heart disease in systemic lupus erythematosus. A retrospective study of 65 patients treated with prednisone

Jpn J M

Prognosis in systemic lupus erythematosus : negative impact of increasing age at onset, black race, and thrombocytopenia, as well as causes of death

Arthritis Rheum

Mortality studies in systemic lupus erythematosus. Results from a single center. I. Causes of death

J Rheumatol

Causes of death in systemic lupus erythematosus

Arthritis Rheum

Changing patterns of mortality in systemic lupus erythematosus (SLE) over three decades at an urban center

Arthritis Rheum

Morbidity and mortality in systemic lupus erythematosus during a 5-year period

Medicine

Incidence studies of systemic lupus erythematosus in Southern Sweden : increasing age, decreasing frequency of renal manifestations and good prognosis

J Rheumatol

Coronary arterial disease in systemic lupus erythematosus : quantification of degree of narrowing in 22 necropsy patients (21 women) aged 16 to 37 years

Am J M

Morbidity in systemic lupus erythematosus

J Rheumatol

Manifestations cardiaques du lupus erythemateux aigu disseminé

Nouv Presse M

Dietary treatment of hyperlipidemia in patients with systemic lupus erythematosus

J Rheumatol

Contribution of traditional risk factors to coronary artery disease in patients with systemic lupus erythematosus

J Rheumatol

Premature morbidity from cardiovascular and cerebrovascular diseases in women with systemic lupus erythematosus

Arthritis Rheum

Myocardial perfusion abnormalities in asymptomatic patients with systemic lupus erythematosus

Am J M

SPECT dual isotope myocardial perfusion imaging in women with SLE. I. Prevalence and distribution of abnormalities

J Rheumatol

Premature atherosclerosis and myocardial hypertrophy in SLE and antiphospholipid antibody (APLA) syndrome

Arthritis Rheum

Prevalence and risk factors of carotid plaque in women with systemic lupus erythematosus

Arthritis Rheum

Myocardial infarction (MI) and stroke in SLE : markdedly increased incidence after controlling for risk factors

Arthritis Rheum

SHORT SURVEY
Atherosclerosis and connective tissue diseases