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Saudi Journal of Kidney Diseases and Transplantation
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Year : 2015  |  Volume : 26  |  Issue : 3  |  Page : 526-535
Cardiovascular risk in lupus nephritis: Do renal disease-related and other traditional risk factors play a role?

1 Department of Clinical Medicine, Faculty of Medicine, University of Colombo, Colombo, Sri Lanka
2 University Medical Unit, National Hospital of Sri Lanka, Colombo, Sri Lanka
3 Department of Radiology, National Hospital of Sri Lanka, Colombo, Sri Lanka
4 Ministry of Health, Colombo, Sri Lanka
5 Department of Community Medicine, Faculty of Medicine, University of Colombo, Colombo, Sri Lanka
6 Clinical Medicine, Faculty of Medicine, University of Colombo, Colombo, Sri Lanka

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Date of Web Publication20-May-2015


This study was performed to evaluate the prevalence of thickened carotid intima media thickness (CIMT) in a Sri Lankan cohort of lupus nephritis (LN) patients and to identify associations between traditional cardiovascular disease (CVD) and LN-related risk factors with increased CIMT. Consecutive patients with biopsy-proven LN were evaluated for conventional CVD risk factors, renal parameters and extent of organ involvement in this cross-sectional study. Current disease activity and damage were assessed by the British Isles Lupus Activity Group (BILAG) score and the Systemic Lupus International Collaborative Clinics/American College of Rheumatology (SLICC/ACR) damage index, respectively. CIMT was assessed by B Mode grey scale ultrasonography. Increased CIMT was defined as CIMT more than the 75th percentile based on cutoffs from the "Carotid Atherosclerosis Progression Study." Forty patients (98% female), with a mean age of 38 years (age range of 20-50) and of South Asian descent, were evaluated. The mean duration of disease of 6.15 years (SD = 4.66). The overall prevalence of cardiovascular events was low and included previous acute coronary syndromes in 7.5%, stable angina in 5%, cerebrovascular accidents in 7.5% and transient ischemic attacks in 2.5% of the patients; 72.5% had hypertension (HTN) [mean blood pressure (BP) 140/80 mm Hg]; 32.5% had dyslipidemias (mean serum cholesterol 5.9; SD = 5.6) and 25% had diabetes (mean blood sugar 103.7; SD = 15.6). Forty percent were obese and 20% were overweight (Asian cutoffs). Increased CIMT (57.5%) and atherosclerotic plaques (15.36%) indicated a high CVD risk in this cohort. Diabetes (P = 0.016), HTN (P = 0.002), dyslipidemia (P = 0.002) and obesity (P = 0.048) were associated with thickened CIMT. The only LN-related risk factor associated with thickened CIMT (P <0.05) was the SLICC/ACR damage index. The independent predictors of thickened CIMT determined by logistic regression analysis were HTN and dyslipidemia.

How to cite this article:
Atukorala I, Weeratunga P, Kalubowila J, Ranasinghe H, Gunawardena N, Lanerolle R, Rathnamalala N. Cardiovascular risk in lupus nephritis: Do renal disease-related and other traditional risk factors play a role?. Saudi J Kidney Dis Transpl 2015;26:526-35

How to cite this URL:
Atukorala I, Weeratunga P, Kalubowila J, Ranasinghe H, Gunawardena N, Lanerolle R, Rathnamalala N. Cardiovascular risk in lupus nephritis: Do renal disease-related and other traditional risk factors play a role?. Saudi J Kidney Dis Transpl [serial online] 2015 [cited 2021 Jun 14];26:526-35. Available from: https://www.sjkdt.org/text.asp?2015/26/3/526/157357

   Introduction Top

Systemic lupus erythematosus (SLE) is a multisystem autoimmune disease that commonly affects the kidneys with a consequent increase in morbidity and mortality. [1] Part of the poor outcome in lupus nephritis (LN) is attributed to acute, [1],[2] chronic or recurrent damage from renal flares. [3] However, improved modalities of treatment have reduced mortality from active lupus renal disease. [4],[5],[6] Despite this, the decline in mortality due to disease is counter-balanced by increased mortality and morbidity from late complications, particularly from cardiovascular disease (CVD). [5]

The increased risk of CVD is inherent to all SLE patients. [7] Most SLE patients have a higher prevalence of conventional risk factors, [8] either due to the disease or due to its treatment. CVD is the most common cause of death in SLE patients with long-standing disease, [9] with fatal myocardial infarction occurring three times more frequently than in age- and gender-matched controls. [10] In addition, the prevalence of asymptomatic CVD in SLE may be of even greater magnitude than symptomatic disease. [11] Studies using carotid B mode ultrasound as a surrogate for subclinical atherosclerosis in SLE [12] have demonstrated a higher prevalence of increased carotid intima medial thickness (CIMT) and atherosclerotic plaques in SLE, [13] with accelerated plaque progression in these patients. [12] Autopsy findings [14] and myocardial perfusion scanning [15] have further corroborated this trend toward increased prevalence of CVD in SLE.

The risk of CVD in SLE is greater than the risk conferred by the high prevalence of conventional cardiovascular risk factors. [16] Furthermore, the risk of CVD is higher in patients with LN than in SLE patients without LN. [17] This may in part be accounted for by the higher prevalence of traditional risk factors and associated immunological abnormalities such as anti-phospholipid antibodies in patients with LN. [18] Elevated serum creatinine and proteinuria as well as aggressive use of corticosteroids in active LN are other potential contributors that increase the burden of CVD in patients with LN. [19]

It is well established that South Asians are at greater risk of developing CVD [20] because of lifestyle determinants, [21] genetics [22] and a high prevalence of conventional risk factors, [23],[24] including obesity, higher glycemia-independent HbA1C [23] and higher leptin levels. [25] However, to the best of our knowledge, there is no published research on the assessment of CVD risk in South Asian patients with LN. Moreover, there is little evidence on the magnitude of contribution of LN-related risk factors to the occurrence of CVD in relatively homogenous cohorts of LN patients, even though this knowledge is critical for the comprehensive management of patients with LN in South Asian communities.

This study explores these critical research gaps by assessing the magnitude of association between increased cardiovascular risk and conventional CVD-related risk factors, LN and other SLE-disease-related risk factors in a South Asian cohort of patients. CIMT was used as a surrogate of CVD risk.

   Methods Top

The study population for this cross-sectional study was selected from the University Medical Unit, National Hospital of Sri Lanka. Consecutive patients with LN who received treatment between January 2011 and January 2012 were selected for the study. The 1997 updated version of the 1982 American College of Rheumatology Revised Criteria for Classification of Systemic Lupus Erythematosus [26] was used to diagnose SLE. Only renal biopsy-proven LN patients were selected.

All study subjects were assessed for socio-demographic data and disease characteristics including organ involvement and renal parameters. Current disease activity was evaluated based on the British Isles Lupus Activity Group (BILAG) score [27],[28] and disease damage was assessed based on the Systemic Lupus International Collaborative Clinics/American College of Rheumatology (SLICC/ACR) damage index. [29],[30] Traditional CVD, SLE and renal-related risk factors were evaluated. Traditional CVD risk factors assessed included age, gender, smoking, history of hypertension (HTN), diabetes mellitus, dyslipidemia, past history of ischemic heart disease (IHD), including stable angina and acute coronary syndromes, and family history of IHD. Significant family history of IHD was defined as a first-degree relative aged <55 years in men and <65 years in women having IHD. Clinical examination included assessment of the body mass index (BMI) and the cutoff definitions for overweight and obesity were based on the following Asian cutoffs: Normal <23, overweight ≥23-24, obese ≥25. [31]

SLE-related risk factors assessed included erythrocyte sedimentation rate (ESR), C-reactive protein (CRP), anti-nuclear antibody (ANA), anti-phospholipid antibody profiling, seropositivity and complement levels. The association of disease activity as measured by the BILAG and disease damage as measured by the SLICC/ACR damage index was evaluated.

Renal disease-associated risk factors evaluated included the following: Stage of chronic kidney disease (CKD) based on the estimated glomerular filtration rate, which was calculated from serum creatinine using the Modification of Diet in Renal Disease (MDRD) formula, [32] biopsy staging of LN based on the International Society of Nephrology and renal pathology society classification, serum creatinine levels and degree of proteinuria based on 24-h quantification.

Carotid ultrasonography was performed as outlined in the standard American Echocardiographic guidelines using B mode ultrasonography.

The carotid duplex was performed using a Philips Envisor C.1.3 and 12 MHz linear probe. The patient was positioned supine with an extended neck. B Mode grey scale scanning was performed both longitudinally and transversely from the origin of both common carotid arteries up to the proximal internal and external carotid arteries. The CIMT, defined as the distance from the leading edge of the lumen- intima interface to the leading edge of the media-adventitia interface of the far wall, was measured at 2 cm proximal to the carotid bulb and was measured bilaterally, three samples on each side (six samples all together) and the average was calculated. Intima-media thickness was measured at the midpoint of each common carotid artery 2 cm proximal to the carotid bulb. Vessels were imaged by color Doppler and spectral imaging and velocities were recorded in cases where there were plaques and narrowing. The carotid duplex was performed by an investigator blinded to the clinical data of the patient. The CIMT was used as a surrogate marker of cardiovascular risk. No reference values for CIMT exist for the Sri Lankan population. Therefore, the cutoffs and definitions were derived from the "carotid atherosclerosis progression study." [33] CIMT ≥75th percentile for the patient's age and sex was considered to be abnormal. Atherosclerotic plaque was defined as the presence of focal thickening that was at least ≥50% than the surrounding wall or a thickness of ≥1.5 mm.

Ethical clearance for the study was obtained from the Ethics Review committees of the Faculty of Medicine (ERC 10-45), University of Colombo and the National Hospital of Sri Lanka. Informed written consent was obtained from all participants prior to inclusion using an information sheet and specifically designed consent form.

   Statistical Analysis Top

Normality testing was performed for all variables and dichotomized based on the mean in normally distributed variables and the median in non-normally distributed variables. Associations were examined between increased CIMT and traditional, disease-related and SLE-related risk variables using chi square testing. Independent associations were derived using backward logistic regression models.

   Results Top

Forty patients with biopsy-proven LN who fulfilled the American College of Rheumatologists classification criteria for SLE were selected for this study. All study subjects were selected from a single center, the Lupus Clinic at the University Medical Clinic, during a 1year period.

General descriptive and clinical data are summarized in [Table 1]. It is evident that majority of the study subjects were young [mean age = 38 years (range -20-50)] and female (98%).
Table 1: Descriptive statistics of the epidemiological and disease-related features of the study population.

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The prevalence of previous cardiovascular system involvement was low: Acute coronary syndrome was seen in three (7.5%) and stable angina in two patients (5%). In addition, two patients each (5%) gave a history of limb gangrene and intermittent claudication. Twelve of the study subjects were obese according to Asian cutoffs. The overall prevalence of traditional CVD risk factors was low: 29 (72.5%), 13 (32.5%) and 10 (25%) patients, respectively, had HTN, hyper-cholesterolemia and diabetes and six (15%) gave a family history of CVD. There were no smokers in this cohort.

The majority of study subjects had class IV LN (n = 24, 60%) as per the World Health Organization and the International Society of Nephrology/Renal Pathology Society 2003 (ISN/ RPS) classifications. [34],[35] One patient (2.5%) had Class I, five patients (12.5%) had Class II, eight patients (20%) had Class III and two patients (5%) had Class V LN on biopsy. There were no patients with end-stage LN in this study. The stages of CKD in the study population, [36] based on the National Kidney Foundation's Kidney Disease Outcomes Quality Initiative staging system, were as follows: Stage 1 = 14 (35%), stage 2 = 16 (43%) and stage 3 = 10 (24%). Thirteen patients (32.5%) had nephrotic syndrome at diagnosis and 27 patients (67.5%) had a mixed or a nephritic clinical presentation [Table 2].
Table 2: Renal parameters of the study population.

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The mean CIMT for this group was 45.4 mm (SD = 8.9). When compared with age- and sex-matched controls from the Carotid Atherosclerosis Progression Study (CAPS) and, using the 75th percentile as the cutoff, 23 patients (57.5%) had thickened CIMT and six patients (15.4%) had carotid plaques. Descriptive data on traditional cardiovascular risk factors are presented in [Table 3].
Table 3: Descriptive statistics of traditional cardiovascular risk factors.

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The mean age of the study patients did not correlate significantly with increased CIMT. However, the traditional risk factors of hyper-tension, hyperlipidemia, diabetes and increased BMI were significantly associated with in-creased CIMT. 39.1% of patients with LN with increased CIMT had diabetes compared with those without increased CIMT. Similar associations were detected with HTN and dyslipidemia [Table 4].
Table 4: Comparative analysis of the risk factors for increased carotid intima media thickness (traditional, disease-related and renal).

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Markers of current active disease or increased disease activity, namely ESR, CRP, complement and BILAG were not associated with increased CIMT. Furthermore, increased renal disease scores on BILAG were also not associated with increased CIMT. However, the SLICC/ACR index, a marker of disease damage, was significantly associated with increased CIMT [Table 4]. However, no association was detected between duration of disease and presence of anti-phospholipid antibodies.

Backward logistic regression was used to identify the best model of risk factors independently associated with increased CIMT in this study population with LN. All parameters with a P-value >0.2 on univariate analysis were included in the model. These parameters included HTN, dyslipidemia, diabetes, increased BMI, nephrotic syndrome and the SLICC/ACR index. This model identified HTN and dyslipidemia as significant independent contributory risk factors for increased CIMT in this study population [Table 5]. This model had a Nagelkerke R2 of 0.466.
Table 5: Backward logistic regression model of independent associations.

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   Discussion Top

The survival rates in lupus have improved when compared with the survival in previous decades. [6],[37] However, the mortality of SLE patients continues to be significantly higher than that of normal populations, [37] with CVD being the most common cause of death, particularly in patients who have had SLE for more than five years. [9] The prevalence of clinically apparent CVD differs in different populations, with reported ranges varying from 8-16%. [6],[37] Furthermore, the risk of myocardial infarction is greater than nineto 50-fold when compared with ageand gender-matched controls. [16] Multiple pathogenic mechanisms have been postulated to account for this increased risk, including atherosclerosis, arteritis, embolization, spasm and abnormal coronary flow. [10],[38] However, it is clear that the risk of CVD in SLE is much greater than can be accounted by the higher prevalence of risk factors for CVD. [16],[19] Therefore, this increased risk is attributed to complex interactions between traditional risk factors and risk factors associated with the disease itself. [16],[39],[40] Previous studies have examined the cardiovascular risk of heterogenous populations of LN of mixed ethnicities and with diverse patterns of major organ involvement. [40],[41] In contrast, this study examined the prevalence of CVD risk factors in a relatively homogenous cohort of patients, all of South Asian descent and having predominant renal involvement. It has previously been demonstrated that South Asian lupus patients have a higher risk of coronary heart disease when compared with Western populations. [42],[43] Therefore, it is felt that this particular study population will allow for a more accurate assessment of the impact of disease-related risk factors for CVD. As LN itself is associated with a greater risk of CVD than other forms of lupus organ involvement, [44] it was believed that examining LN cohorts will provide more useful insights into the identification of risk determinants for CVD than other disease manifestations.

This study population consisted of LN patients with a mean age of 38 years. Despite this relatively young age, the prevalence of increased CIMT was 57%, nearly double that of previously described prevalence of increased intimal thickness in some less-homogenous lupus cohorts, [41] and in one LN cohort from Malaysia of mixed ethnicity. [45] In addition, the prevalence of previous cardiovascular events in the study cohort was comparable to the occurrence of CVD in older Caucasian lupus cohorts. There is paucity of data on South Asian LN populations, but these findings are comparable with the little data available from SLE patients with diverse end-organ involvement originating from India. [42],[43]

Univariate analysis showed strong association between traditional risk factors such as increased BMI, HTN, diabetes and dyslipidemia and increased CIMT. However, backward logistic regression showed only two adjusted risk factors, HTN and dyslipidemia, as being statistically significant. These findings are comparable with a previous study by Doria et al on a cohort of slightly older Caucasian patients with a greater prevalence of traditional risk factors such as HTN, family history of CVD and smoking. [41] However, the only other study on CVD determinants in LN in a Malaysian cohort did not show a similar association. [45] This difference may be accounted for the slightly younger age of the Malaysian patients (33.6 ± 10 years) compared with our study population.

There was no correlation between the presence of anti-phospholipid antibodies and CVD risk assessed by CIMT. The low prevalence of antiphospholipid antibodies in this study sample may have attenuated the risk conferred by antiphospholipid antibodies to CVD. Also, it is noteworthy that this study cohort had a lower prevalence of anti-phospholipid antibodies than other predominantly Caucasian cohorts; [18] therefore, this study is potentially inadequately powered to detect the association. The low sensitivity and poorer quality of anti-phospholipid antibody screening tests available in Sri Lanka may have further contributed to this observation.

The disease duration of SLE did not correlate with increased CIMT. However, the SLICC/ ACR damage index, a marker of disease damage, was significantly correlated with increased CIMT. However, this association disappeared with logistic regression analysis. This difference may be attenuated if the actual duration of disease flare ups was assessed instead of the total disease duration. Another explanation for the lack of association may be the relatively shorter duration of disease in our study population.

LN-associated cardiovascular risk factors assessed in this study failed to show a positive relationship with increased CIMT. The presence of raised ESR, CRP, nephrotic range proteinuria and mixed nephritic/nephrotic picture were not associated with increased CVD as assessed by the surrogate measure. The lack of association with CRP in this population may be due to the use of a conventional CRP assay. Earlier studies reported cardiovascular risk association [46] using high-sensitivity CRP assays. Moreover, the BILAG renal score, which indicates the presence of active lupus renal disease, and C3 hypo-complementemia, [47] a measure associated with LN disease flares, was not significantly correlated with increased CIMT. However, the SLICC/ACR index, a marker of disease damage, was significantly associated with increased CIMT on univariate analysis.

CVD is a cumulative insult on the cardiovascular system and the endothelium. It is therefore to be expected that point measures of disease activity, such as BILAG and complement, failed to show an association. This argument is tenable, especially because the measure of chronic damage, the SLICC/ACR index, was found to be significantly associated with thickened CIMT.

Cumulative steroid dose was not identified as a significant predictor of increased CIMT. This may be due to the low total cumulative mean steroid doses in the cohort selected for the study.

Risk factors could not be established in this cross-sectional study as there was no control comparison. Moreover, it was difficult to compare with other previously described cohorts due to the potential for multi-factorial disparities between populations of different ethnicities. In addition, the carotid duplex cutoffs have not been validated in Sri Lankan or South Asian cohorts. Therefore, the CIMT cutoffs may result in bias.

This study revealed the increased burden of subclinical cardiovascular disease in a South Asian cohort of patients. It demonstrated that the high burden of traditional risk factors contribute to the increased risk of subclinical coronary vascular disease in LN. The study failed to show an association between measures of current disease activity and CVD.

   Conclusions Top

The results of the study underline the importance of controlling traditional risk factors in patients with LN, irrespective of age or disease duration. Future research, based on case-control studies with larger samples, is needed to validate these findings.

Competing Interests

All authors declare that they have no financial or non-financial competing interests.

Relevant Author Information

Inoshi Atukorala is a consultant Rheumatologist and Lecturer attached to the Faculty of Medicine University of Colombo.

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Klein MH, Thorner PS, Yoon SJ, Poucell S, Baumal R. Determination of Circulating Immune Complexes, C3 and C4 Complement Components and Anti-DNA Antibody in Different Classes of Lupus Nephritis. Int J Pediatr Nephrol 1984;5:75-82.  Back to cited text no. 47

Correspondence Address:
Dr. Praveen Weeratunga
University Medical Unit, National Hospital of Sri Lanka, Colombo
Sri Lanka
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DOI: 10.4103/1319-2442.157357

PMID: 26022023

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  [Table 1], [Table 2], [Table 3], [Table 4], [Table 5]


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