Cardiovascular risk markers (computed tomography‑coronary artery calcium and carotid intima‑media thickness) in patients with rheumatoid arthritis and controls
- Authors:
- Published online on: July 12, 2024 https://doi.org/10.3892/mi.2024.176
- Article Number: 52
-
Copyright : © Fatima et al. This is an open access article distributed under the terms of Creative Commons Attribution License [CC BY 4.0].
Abstract
Introduction
Rheumatic illnesses are a general umbrella term for almost 200 different disorders affecting the musculoskeletal system (1). The causes and therapies for the almost 100 different types of arthritis have been well-documented. In humans, rheumatoid arthritis (RA) and osteoarthritis are the most well-known types of arthritis. RA, also referred to as an autoimmune disease or a progressive disease, is an example of a chronic systemic condition (2). It is characterized by destructive joint disease and prolonged inflammation, although its etiology is uncertain (3). There are two subtypes of this disease, namely ‘seropositive’ and ‘seronegative’. Elevated blood levels of rheumatoid factor (RF) autoantibodies and, more recently, antibodies to citrullinated protein/peptide antigens (ACPAs) can be used to determine seropositivity (4). RF autoantibodies are a type of antibody that are produced by the immune system.
RA is far more common in certain populations than in others. France (0.19%) and Italy (0.41%) have been found to have a lower reported prevalence of RA compared to other countries of the world, where it varies from 0.19 to 1.1% (5,6). The prevalence of RA in Germany and Sweden has been reported to be ~0.65% (7,8). RA has been reported to affect between 0.5 and 1% of North Americans (8-10). RA is estimated to afflict 0.75% of individuals in India (10,11).
Furthermore, coronary artery calcium (CAC) as it is commonly known, is a characteristic of coronary atherosclerosis (12). Consistent, dependable and convincing evidence of a substantial association between CAC and significant cardiovascular events has also been found in a number of asymptomatic individuals (13,14). Initially, CAC was evaluated using chest X-ray, fluoroscopy, or digital subtraction of fluoroscopy; following the introduction of electron beam computed tomography and multidetector computed tomography, these devices were found to be more useful. The most useful information on cardiovascular risk, or the likelihood of suffering a heart attack or stroke, may be obtained from coronary calcium scores for females aged 35 to 70 years and for males aged 40 to 60 years (15).
The disease activity score (DAS) was developed by a group of Dutch rheumatologists with the goal of offering a standardized method to compare and contrast results from clinical trials of novel medications for the treatment of RA. Clinical practices often use disease activity measurements related to RA. The DAS28, which evaluates a total of 28 joints, is one such instrument.
The present study aimed to examine the association between cardiovascular risk (using CAC) and CIMT in patients with RA and healthy controls, using the DAS28 as a proxy.
Patients and methods
Study population
The present case-control study was carried out at a tertiary care center over the course of 2 academic years (2020-2022). Each individual who met the American College of Rheumatology (ACR) criteria (Table SI) for a diagnosis of RA was included in the analysis as the cases, while those who were healthy, and age- and sex-matched individuals served as the controls. All patients were subjected to routine blood and radiological investigations. Patients with Inflammatory joint disease other than RA, a history of any cardiovascular/cerebrovascular events, known diabetes and obesity [body mass index (BMI) >30 kg/m2] and patients who were critically ill were excluded from the study. The Institutional Ethical Committee of Era's Lucknow Medical College and Hospital, Lucknow, India gave its approval for the research to go on. All patients were asked to provide their written and informed permission.
All controls and patients with RA who were identified using the aforementioned criteria were referred to the Radiology Department of the same hospital for evaluation of CIMT by carotid intima-media thickness ultrasonography and coronary artery calcium(CAC) burden by dual-energy computed tomography under the supervision of competent radiologists. These criteria categorize newly presented patients with confirmed clinical synovitis in at least one joint when no other medical condition seems to fit into the category. A score of ≥6 fulfils the requirements for definite RA. The classification criteria used in the present study for the patients with RA are listed in Table SI (16).
DAS
Dutch rheumatologists first created the DAS in order to standardize and compare outcomes in RA medication clinical trials. Over time, the DAS28 has also found its way into everyday clinical settings. DAS28 is a metric for assessing the efficacy of RA therapy and management. Treatments may reduce the inflammation caused by RA, which in turn attenuates the damage inflicted to joints that causes disability and suffering. As a result, DAS28 (Table SII) (17) plays a crucial role in determining the optimal strategy for the disease management of each individual affected.
Estimation of CAC score
The estimation of the CAC score was achieved using a 384-slice dual source machine, SOMATOM Force (Siemens Healthineers), for coronary calcium scoring at the Department of Radiology, Era's Lucknow Medical College and Hospital. The arteries which were focused on were the following: Left main, left circumflex, right circumflex and left anterior descending. The CAC score calculated using the Agatston score.
Method of calculation
The calculation is based on the weighted density score given to the highest attenuation value (HU) multiplied by area of the calcification speck. The density factor assigned to each HU corresponds as 130-199 HU=1; 200-299 HU=2; 300-399 HU=3 and 400+ HU= 4. For example, if a calcified speck has maximum attenuation value of 400 HU and occupies 8 sq mm area, then its calcium score is 32. The severity is then graded as demonstrated in Table SIII (18).
Statistical analysis
Statistical analysis was performed using SPSS version 21.0 statistical analysis software (IBM Corp.). The values are presented as number and percentage, or as the mean ± standard deviation (SD). Categorical variables were analyzed using the Chi-squared test or Fisher's exact test and continuous variables were analyzed using the unpaired student's t-test. Bivariate Pearson's (r-value) correlation analysis was used to determine the correlations among variables. A P-value <0.05 was considered to indicate a statistically significant difference.
Results
The present study examined 45 patients with RA who fulfilled the aforementioned inclusion criteria. These patients were then classified as the cases and another 45 healthy individuals were included as the controls. As demonstrated in Fig. 1, although the sex ratios between the patients with (53.3% females) and the controls (60% males) were comparable, the RA patient group had a higher number of females. The demographic profiles of both groups are presented in Table I.
Only 2 (4.4%) of the 45 patients with RA had a DAS ≤2.6, which is indicative of remission. A total of 40 patients of 45 cases (88.9%), had disease activity ratings that ranged from moderate to high (range, >3.2), whereas 3 patients, which is equivalent to 6.7% of the sample, had low disease activity scores (range, 2.6-3.2) (Table II).
Compared with the controls, the cases had a significantly higher total leucocyte count (TLC; 9311±2877 vs. 8049±1780 per microliter), erythrocyte sedimentation rate (ESR) in the first hour (19.18±6.34 vs. 16.62±3.56 mm/h), C-reactive protein (CRP; 11.36±5.84 vs. 2.44±1.69 mg/l), serum urea (24.76±7.96 vs. 21.99±3.53 mg/dl), serum potassium (4.18±0.69 vs. 3.95±0.23 mmol/l), serum magnesium (1.95±0.18 vs. 2.02±0.14 mg/dl), serum glutamic pyruvic transaminase (SGPT; 44.82±18.60 vs. 37.69±9.58 units/l), serum alkaline phosphatase (ALP; 96.02±36.12 vs. 81.96±21.19 IU/l), serum cholesterol (160.88±30.11 vs. 145.35±17.40 mg/dl), serum high-density lipoprotein (HDL; 7.20±15.83 vs. 43.91±8.17 mg/dl), serum low-density lipoprotein (LDL; 107.74±23.75 vs. 98.11±16.66 mg/dl) and the LDL-HDL ratio (2.85±1.58 vs. 1.57±3.27 mg/dl) (Table III). The results of the analysis of the correlation between the DAS, and BMI, CRP, serum cholesterol, serum triglycerides, serum HDL, serum LDL and serum very low-density lipoprotein (VLDL) are presented in Table IV. An inverse correlation was observed between the DAS and HDL levels. In addition, a strong correlation was found between the DAS and the CRP level. However, a moderate or weak correlation was observed between DAS and the remaining variables, although some correlations were significant.
None of the controls had moderate risk (score 101-400) or severe risk (score ≥401), and the majority of the controls exhibited no evidence of CAD (CAC score 0; 88.9%). The remaining controls had a minimum risk (score 1-10) or mild risk (score 11-100). By contrast, according to the CAC scores, only 22.2% of the patients with RA exhibited no signs of CAD, another 22.2% had a low risk, and the remaining 55.5% had a mild to severe risk. This difference was found to be statistically significant. The proportion of cases was higher as compared to controls in all the risk categories: Minimal (22.2 vs. 6.7%), mild (13.3 vs. 4.4%), moderate (24.4 vs. 0.0%) and severe risk (17.8 vs. 0.0%) (Table V).
The range of CIMT in the patients with RA was 0.712-1.310 mm, while that in the controls was 0.412-0.518 mm. In the patients with RA, the CIMT was determined to be 1.050±0.218 mm, which was substantially larger than the value of the control group (0.479±0.040 mm) (Table VI).
The CIMT exhibited a significant correlation with CRP, serum cholesterol, triglycerides, serum HDL (inverse), LDL and VLDL. A strong correlation was found between CIMT and CRP was strong; however, a moderate or weak correlation was found between CIMT and the remaining variables, although some correlations were significant. The CAC score also exhibited a significant correlation with CRP, serum cholesterol and serum triglycerides, serum VLDL and serum LDL. A moderate correlation was found between the CAC score and CRP, serum triglycerides and VLDL. The CAC scores and CIMT levels of both sexes were comparable. Age was not found to significantly correlate with the aforementioned two markers (CAC and CIMT) (Table VII).
Discussion
As a chronic inflammatory joint condition, RA restricts everyday activities due to the pain, stiffness, and exhaustion that patients experience regularly. The link between inflammation and the development of cardiovascular disease was recognized only ~10 years ago. Researchers found that patients with RA had a 1.5-2.0-fold greater risk of developing coronary artery disease (CAD) than the general population (18). Another study demonstrated that patients with RA had a prevalence of myocardial infarction (MI) that was >3-fold higher than that of patients without RA (19). Thus, CAD is already more likely to occur before RA is even diagnosed clinically. The signs and symptoms of CAD vary with the disease process throughout time. In certain cases, there may be no obvious symptoms of damage.
The present study aimed to evaluate CIMT and computed tomography-CAC, two relatively novel cardiovascular risk indicators, in patients with RA. For this purpose, the present study recruited 45 patients with RA and 45 individuals who served as the healthy controls. The enrolled patients with RA had an average age of 49.07±12.38 years (ranging from 24 to 80 years), with 53.3% being female. Specifically, the controls in the present study were matched for both sex and age. Although RA may develop at any age, the majority of epidemiological research has shown that the condition is most common in individuals who are in their 50 and 60s. Other studies have suggested a later onset of the illness (19-23).
The mean age of patients with RA included in the clinical studies by Schott et al (24) (53.3 years) and Targońska-Stepniak et al (25) (42.6±8.0 years; range, 27-59) was also very close to that in the present study. In the study by Udachkina et al (26), the median age of the patients was 56 years.
In the present study, two-thirds (53.3%) of the patients had a DAS >5.2 (high disease activity), and16 patients had a DAS of 3.3-5.2 (35.6%) (moderate disease activity). Out of the 45 patients with RA, 2 (4.4%) were not on therapy, 6 (13.3%) were on disease-modifying antirheumatic drugs (DMARDs) treatment for <6 months, and the remaining 37 (82.22%) were on DMARDS treatment for >6 months. The DAS exhibited a substantial correlation with serum cholesterol, LDL and CRP levels among the CAD risk factors. Sengul et al (27) examined Turkish individuals with RA and their DAS28-ESR and DAS28-CRP criteria. While the DAS28-CRP was based on DAS28 without the ESR, the DAS28-ESR was based on the DAS with 28 joints (27). According to that study, the DAS28-CRP and DAS28-ESR exhibited a substantial association, whereas the individual components only exhibited a modest correlation (27).
In the present study, significant differences in the laboratory parameters (TLC, first-hour ESR, CRP, serum urea, serum potassium, serum magnesium, SGPT and serum ALP, and lipid levels) of the RA cases and healthy controls were observed. The TLC, ESR and CRP levels are inflammatory markers and have been found to be increased in ~40% of patients with RA (28). It has been shown that anti-inflammatory medications increase total, HDL and LDL cholesterol levels in patients with RA (29,30). Oxidative alterations caused by chronic inflammation modify the structure of HDL and decrease apolipoprotein-A1 in patients with active RA (31).
In the present study, the CAC score of the patients with RA was significantly higher compared with that of the controls (246.80±330.81 vs. 0.600±0.251). Of note, ~55.6% of patients with RA had been found to have a mild to severe risk of developing CAD (score, 11->400). A significant correlation between CAC and CRP, and lipid levels (apart from HDL) was found. These findings are supported by the findings in the study by Wahlin et al (32), who studied the computed tomography-CAC of 22 patients with RA (mean age, 65 years). They also found that 55.5% of the patients had a CAC score >10(32).
The average age of the 60 female patients with RA in the study by Bernardes et al (33) was 53.6±10.4 years, and their average DAS28 score was 4. Age, BMI, hyperglycemia and cholesterol levels were shown to have a substantial correlation with the mean coronary calcium score, which was 35.192±117.786. In the present study, the CIMT varied significantly (1.050±0.218 vs. 0.479±0.040 mm) between the experimental and control groups. CIMT was substantially linked with levels of lipids and CRP.
Targońska-Stepniak et al (25) found similar results when they evaluated CIMT values in 74 patients with RA without cardiovascular risk, with an average age of 46.4±0.6 years. A total of 31 age-matched control participants had notably higher CIMT values than the controls (25).
As a chronic inflammatory disorder, RA affects more than only the joints and muscles. Multiple risk variables that are also linked to cardiovascular risk govern it. Moreover, medication for RA also has a cardiovascular impact. Aging also contributes as a common risk factor between RA and cardiovascular disorders. Thus, the screening of all patients with RA for cardiovascular disease and associated risks is recommend at regular intervals. Furthermore, according to the data indicating a much larger percentage of these surrogate indicators in patients with RA, it is imperative that more stringent measures be implemented to decrease the cardiovascular risk in this population.
In conclusion, the present study demonstrated that the CIMT and CAC differed substantially between healthy individuals and patients with RA. This difference was shown to be statistically significant. The diagnosis and planning of risk reduction measures for patients with RA may be aided by these surrogate indicators of early atherosclerosis. Consistent results between CIMT and CAC, and established CV risk variables, such as dyslipidemia, suggest that these two methods could assist prevention and treatment efforts. Chronic inflammation significantly increases the risk of developing atherosclerosis, as suggested by the link between the disease activity score, the CIMT and CAC.
Supplementary Material
Classification criteria for rheumatoid arthritis.
Disease activity score.
Severity grading of CAC score.
Acknowledgements
Not applicable.
Funding
Funding: No funding was received.
Availability of data and materials
The datasets used and/or analyzed during the current study are available from the corresponding author on reasonable request.
Authors' contributions
The study was conceptualized and planned by JF. All the data were collected, analyzed and entered into tables by MZS. JF and MZS analyzed the data and modified the final study. VS and ZS provided scientific input and helped editing protocols, contributed data or analysis tools and performed the analyses. SM helped pool information and edited the final manuscript, collected the data, and contributed data or analysis tools. Performed the analysis and Edited the paper. AAJ and ZU helped collect patient profiles and raw data. All authors have reviewed and approved the final manuscript. JF and MZS confirm the authenticity of all the raw data.
Ethics approval and consent to participate
The Institutional Ethical Committee of Era's Lucknow Medical College and Hospital, Lucknow, India gave its approval for the research to go on. All patients were asked to provide their informed permission.
Patient consent for publication
Not applicable.
Competing interests
The authors declare that they have no competing interests.
References
Mohsin Z, Asghar AA, Faiq A, Khalid I, Ul-Haque I, Rehman S, Ahmed SI, Basalat ST, Aimen A, Shafique S, et al: Prevalence of rheumatic diseases in a tertiary care hospital of Karachi. Cureus. 10(e2858)2018.PubMed/NCBI View Article : Google Scholar | |
Shi Y, Wu Y, Ren Y, Jiang Y and Chen Y: Infection risks of rituximab versus non-rituximab treatment for rheumatoid arthritis: A systematic review and meta-analysis. Int J Rheum Dis. 22:1361–1370. 2019.PubMed/NCBI View Article : Google Scholar | |
Okada Y, Eyre S, Suzuki A, Kochi Y and Yamamoto K: Genetics of rheumatoid arthritis: 2018 status. Ann Rheum Dis. 78:446–453. 2019.PubMed/NCBI View Article : Google Scholar | |
Smolen JS, Aletaha D, Koeller M, Weisman MH and Emery P: New therapies for treatment of rheumatoid arthritis. Lancet. 370:1861–1874. 2007.PubMed/NCBI View Article : Google Scholar | |
Rossini M, Rossi E, Bernardi D, Viapiana O, Gatti D, Idolazzi L, Caimmi C, Derosa M and Adami S: Prevalence and incidence of rheumatoid arthritis in Italy. Rheumatol Int. 34:659–664. 2014.PubMed/NCBI View Article : Google Scholar | |
Biver E, Beague V, Verloop D, Mollet D, Lajugie D, Baudens G, Neirinck P and Flipo RM: Low and stable prevalence of rheumatoid arthritis in northern France. Joint Bone Spine. 76:497–500. 2009.PubMed/NCBI View Article : Google Scholar | |
Englund M, Jöud A, Geborek P, Felson DT, Jacobsson LT and Petersson IF: Prevalence and incidence of rheumatoid arthritis in southern Sweden 2008 and their relation to prescribed biologics. Rheumatology (Oxford). 49:1563–1569. 2010.PubMed/NCBI View Article : Google Scholar | |
Hense S, Ramos AL, Callhoff J, Albrecht K, Zink A and Hoffmann F: Prevalence of rheumatoid arthritis in Germany based on health insurance data: Regional differences and first results of the PROCLAIR study. Z Rheumatol. 75:819–827. 2016.PubMed/NCBI View Article : Google Scholar : (In German). | |
Hunter TM, Boytsov NN, Zhang X, Schroeder K, Michaud K and Araujo AB: Prevalence of rheumatoid arthritis in the United States adult population in healthcare claims databases, 2004-2014. Rheumatol Int. 37:1551–1557. 2017.PubMed/NCBI View Article : Google Scholar | |
Jean S, Hudson M, Gamache P, Bessette L, Fortin PR, Boire G and Bernatsky S: Temporal trends in prevalence, incidence, and mortality for rheumatoid arthritis in Quebec, Canada: A population-based study. Clin Rheumatol. 36:2667–2671. 2017.PubMed/NCBI View Article : Google Scholar | |
Bernatsky S, Dekis A, Hudson M, Pineau CA, Boire G, Fortin PR, Bessette L, Jean S, Chetaille AL, Belisle P, et al: Rheumatoid arthritis prevalence in Quebec. BMC Res Notes. 7(937)2014.PubMed/NCBI View Article : Google Scholar | |
Demer LL and Tintut Y: Vascular calcification: Pathobiology of a multifaceted disease. Circulation. 117:2938–2948. 2008.PubMed/NCBI View Article : Google Scholar | |
Oei HH, Vliegenthart R, Hak AE, del Sol A, Hofman A, Oudkerk M and Witteman JC: The association between coronary calcification assessed by electron beam computed tomography and measures of extracoronary atherosclerosis: The rotterdam coronary calcification study. J Am Coll Cardiol. 39:1745–1751. 2002.PubMed/NCBI View Article : Google Scholar | |
Hoffmann U, Massaro JM, Fox CS, Manders E and O'Donnell CJ: Defining normal distributions of coronary artery calcium in women and men (from the Framingham Heart Study). Am J Cardiol. 102:1136–1141. 2008.PubMed/NCBI View Article : Google Scholar | |
Yadav A, Mala M, Yadav GAM and Kumar LN: Effect of cigarette smoking on blood levels of lipid and atherogenic lipid ratios. Natl J Lab Med. 9:1–3. 2020. | |
Aletaha D, Neogi T, Silman AJ, Funovits J, Felson DT, Bingham CO III, Birnbaum NS, Burmester GR, Bykerk VP, Cohen MD, et al: 2010 rheumatoid arthritis classification criteria: An American college of rheumatology/European league against rheumatism collaborative initiative. Arthritis Rheum. 62:2569–2581. 2010.PubMed/NCBI View Article : Google Scholar | |
Kumar BS, Suneetha P, Mohan A, Kumar DP and Sarma KVS: Comparison of disease activity score in 28 joints with ESR (DAS28), clinical disease activity index (CDAI), health assessment questionnaire disability index (HAQ-DI) & routine assessment of patient index data with 3 measures (RAPID3) for assessing disease activity in patients with rheumatoid arthritis at initial presentation. Indian J Med Res. 146:S57–S62. 2017.PubMed/NCBI View Article : Google Scholar | |
Solomon DH, Goodson NJ, Katz JN, Weinblatt ME, Avorn J, Setoguchi S, Canning C and Schneeweiss S: Patterns of cardiovascular risk in rheumatoid arthritis. Ann Rheum Dis. 65:1608–1612. 2006.PubMed/NCBI View Article : Google Scholar | |
Maradit-Kremers H, Crowson CS, Nicola PJ, Ballman KV, Roger VL, Jacobsen SJ and Gabriel SE: Increased unrecognized coronary heart disease and sudden deaths in rheumatoid arthritis: A population-based cohort study. Arthritis Rheum. 52:402–411. 2005.PubMed/NCBI View Article : Google Scholar | |
Doran MF, Pond GR, Crowson CS, O'Fallon WM and Gabriel SE: Trends in incidence and mortality in rheumatoid arthritis in Rochester, Minnesota, over a forty-year period. Arthritis Rheum. 46:625–631. 2002.PubMed/NCBI View Article : Google Scholar | |
Riise T, Jacobsen BK and Gran JT: Incidence and prevalence of rheumatoid arthritis in the county of Troms, Northern Norway. J Rheumatol. 27:1386–1389. 2000.PubMed/NCBI | |
Linos A, Worthington JW, O'Fallon WM and Kurland LT: The epidemiology of rheumatoid arthritis in Rochester, Minnesota: A study of incidence, prevalence, and mortality. Am J Epidemiol. 111:87–98. 1980.PubMed/NCBI View Article : Google Scholar | |
Gabriel SE, Crowson CS and O'Fallon WM: The epidemiology of rheumatoid arthritis in Rochester, Minnesota, 1955-1985. Arthritis Rheum. 42:415–420. 1999.PubMed/NCBI View Article : Google Scholar | |
Schott LL, Kao AH, Cunningham A, Wildman RP, Kuller LH, Sutton-Tyrrell K and Wasko MC: Do carotid artery diameters manifest early evidence of atherosclerosis in women with rheumatoid arthritis? J Womens Health (Larchmt). 18:21–29. 2009.PubMed/NCBI View Article : Google Scholar | |
Targońska-Stepniak B, Drelich-Zbroja A and Majdan M: The relationship between carotid intima-media thickness and the activity of rheumatoid arthritis. J Clin Rheumatol. 17:249–255. 2011.PubMed/NCBI View Article : Google Scholar | |
Udachkina EV, Novikova DS, Popkova TV, Kirillova IG, Markelova EI, Gorbunova YN, Karateev DE, Luchikhina EL, Demidova NV, Borisova MA, et al: Progression of Carotid Artery Atherosclerosis during treatment to target in patients with early rheumatoid arthritis. Rheumatol Sci Pract. 56:449–455. 2018. | |
Sengul I, Akcay-Yalbuzdag S, Ince B, Goksel-Karatepe A and Kaya T: Comparison of the DAS28-CRP and DAS28-ESR in patients with rheumatoid arthritis. Int J Rheum Dis. 18:640–645. 2015.PubMed/NCBI View Article : Google Scholar | |
Emery P: The dunlop-dottridge lecture: Prognosis in inflammatory arthritis: The value of HLA genotyping and the oncological analogy. J Rheumatol. 24:1436–1442. 1997.PubMed/NCBI | |
van Sijl AM, Peters MJ, Knol DL, de Vet RH, Sattar N, Dijkmans BA, Smulders YM and Nurmohamed MT: The effect of TNF-alpha blocking therapy on lipid levels in rheumatoid arthritis: A meta-analysis. Semin Arthritis Rheum. 41:393–400. 2011.PubMed/NCBI View Article : Google Scholar | |
Robertson J, Peters MJ, McInnes IB and Sattar N: Changes in lipid levels with inflammation and therapy in RA: A maturing paradigm. Nat Rev Rheumatol. 9:513–523. 2013.PubMed/NCBI View Article : Google Scholar | |
Charles-Schoeman C, Watanabe J, Lee YY, Furst DE, Amjadi S, Elashoff D, Park G, McMahon M, Paulus HE, Fogelman AM and Reddy ST: Abnormal function of high-density lipoprotein is associated with poor disease control and an altered protein cargo in rheumatoid arthritis. Arthritis Rheum. 60:2870–2879. 2009.PubMed/NCBI View Article : Google Scholar | |
Wahlin B, Meedt T, Jonsson F, Henein MY and Wållberg-Jonsson S: Coronary artery calcification is related to inflammation in rheumatoid arthritis: A long-term follow-up study. Biomed Res Int. 2016(1261582)2016.PubMed/NCBI View Article : Google Scholar | |
Bernardes M, Madureira A, Oliveira A, Martins MJ, Lucas R, Costa L, Pereira JG, Ventura F, Ramos I and Martins E: Coronary artery calcium score in female rheumatoid arthritis patients: Associations with apolipoproteins and disease biomarkers. Int J Rheum Dis. 22:1841–1856. 2019.PubMed/NCBI View Article : Google Scholar |