Abstract
Objective
The role of cardiovascular disease (CVD) risk factors in psoriatic arthritis (PsA) is poorly understood. We examined the prevalence of CVD risk factors at initial onset of PsA and compared the observed incidence of CVD events with that predicted by the Framingham risk score (FRS) to determine its applicability in this patient population.
Methods
A population-based incidence cohort of 158 patients with PsA who fulfilled ClASsification of Psoriatic ARthritis (CASPAR) criteria for PsA in 1989–2008 was assembled. Medical records were reviewed to ascertain CVD risk factors and CVD events. Future risk of CVD disease was estimated using the FRS algorithm.
Results
Mean age was 43.4 years (range: 19–74 years), 61% were men and 44% were obese (body mass index ≥30kg/m2). Fifty-four (34%) patients presented with ≥2 CVD risk factors at PsA incidence. Among 126 patients aged ≥ 30 years at PsA incidence with no prior history of CVD, 33% had FRS ≥10% with 11% having FRS ≥ 20% and 18 experienced a CVD event in the first 10 years of disease duration. The 10 year cumulative incidence of CVD events was 17% (95% confidence interval [CI]: 10–24%), almost twice as high as the predicted incidence based on the FRS (Standardized incidence ratio: 1.80; 95% CI: 1.14–2.86; p=0.012).
Conclusion
The majority of newly diagnosed PsA patients have a >10% risk of CVD disease within 10 years of PsA incidence. The CVD risk in these patients is higher than expected and underestimated by the FRS.
Keywords: Psoriatic arthritis, cardiovascular disease, cardiovascular risk factors
Patients with psoriasis and psoriatic arthritis (PsA) are at an increased risk for premature cardiovascular disease (CVD), metabolic syndrome, type 2 diabetes, dyslipidemia, hypertension, and obesity (1–9). Psoriasis severity and age of onset may increase CVD risk, independent of traditional risk factors (4, 7, 10, 11). Systemic inflammation from PsA may play a role in promoting accelerated atherosclerosis related to endothelial dysfunction (12, 13).
There is an association between rheumatoid arthritis (RA) and CVD due to traditional and non-traditional cardiovascular risk factors (i.e., elevated inflammatory markers; rheumatoid factor seropositivity; corticosteroid use) (14–16). CVD risk in patients with PsA is less well understood, and available studies may be limited by selection bias, heterogenous patient groups, and definition of outcome assessments (5, 13). Yet, the consequences of underestimating CVD risk in the PsA population in clinical practice may result in a missed opportunity to intervene early due to a lack of accurate detection tools (17). Hence, the potential link between PsA and increased CVD risk deserves further exploration.
The Framingham risk score (FRS) algorithm has been used to identify patients at risk for an adverse cardiac event in 10 years (18). The variables of age, gender, smoking status, hypertension, diabetes, total cholesterol and high-density lipoprotein (HDL) cholesterol are used to derive a risk score for 10-year absolute cardiovascular risk to stratify patients into low, intermediate, and high risk groups (18, 19). D ’Agostino et al. (19) broadened the Framingham tool to develop a sex-specific multivariable prediction model that not only assesses the general CVD risk, but also the risk of CVD complications such as coronary artery disease, cerebrovascular disease, peripheral arterial disease and heart failure events for guiding preventive management. The aims of our study were to assess the prevalence of CVD risk factors at onset of PsA, examine the incidence of CVD among patients newly diagnosed with PsA, and compare the observed incidence of CVD events with CVD events predicted by FRS to determine its applicability in this patient population.
METHODS
Study design
This was a retrospective, population-based, cohort study. The study was approved by the Mayo Clinic and Olmsted Medial Center institutional review boards and was conducted using the resources of the Rochester Epidemiology Project (REP), as previously described (20). The REP system links inpatient and outpatient medical records generated by health care providers over years, maintains an electronic index of diagnoses and surgical interventions, and provides an ongoing census of individuals living in the community over time. All contemporary and archived medical records are easily accessible for chart review and validation of diagnoses, treatments, and disease signs and symptoms.
Inclusion criteria
Using this data resource, we assembled an incidence cohort of adult patients (age 18 and over) of Olmsted County, Minnesota with PsA who first fulfilled the CASPAR (21) criteria between January 1, 1989 and December 31, 2008. This cohort was identified and followed until death, migration, or April 10, 2013. The characteristics of this early PsA incidence cohort previously have been described as predominantly middle-aged patients demonstrating oligoarticular involvement and enthesopathy (22), similar to other early PsA cohorts (23, 24). The complete medical records of all potential subjects with PsA were identified and reviewed by two rheumatologists (FCE or MSM) using a standardized, pre-tested data abstraction form. For inclusion into the study, patients had inflammatory articular disease (joint, spinal, entheseal) documented by either a primary care physician or a rheumatologist, and met the CASPAR criteria at that visit by attaining a score ≥ 3 among the five CASPAR categories (21, 22). Patients who did not fulfill CASPAR criteria or who were diagnosed outside the study time period were excluded.
CVD risk assessment
The 10 year risk of CVD was estimated using the predictive model from the Framingham risk score algorithm (19). This is a multi-variable risk factor algorithm that assesses the general CVD risk by incorporating the traditional CVD risk factors, i.e. age; total and high density lipoprotein cholesterol, systolic blood pressure, hypertension, smoking, and diabetes, as well as the risk for CVD events related to coronary, cerebrovascular, peripheral artery disease, and heart failure. CVD risk factors were ascertained at the time of PSA incidence (± 1 year) (MSM). Cigarette smoking status (current, former and never) was assessed at baseline (PsA incidence date). Diabetes mellitus was defined as at least 2 measurements of fasting plasma glucose ≥ 126mg/dl or the 2-hour plasma glucose level ≥ 200mg/dl, or a history of diabetes or treatment with hypoglycemic agents (25). Patients were categorized as obese if body mass index (BMI) was ≥ 30kg/m2, based on the Expert Panel on the Identification, Evaluation and Treatment of Overweight and Obesity in Adults clinical guidelines (26, 27). Hypertension was defined as 2 or more ambulatory blood pressure readings of 140 mmHg systolic and/or 90mmHg diastolic, or a physician’s diagnosis of hypertension or if patients received treatment with antihypertensive agents (28). Dyslipidemia was defined as total cholesterol ≥ 240mg/dl, low-density lipoprotein cholesterol ≥ 160mg/dl, high-density lipoprotein cholesterol ≤ 40mg/dl, or triglycerides ≥ 150mg/dl, or a history of dyslipidemia or treatment with lipid-lowering therapy (27).
CVD outcomes
All CVD diagnoses and arterial vascular procedures were abstracted from the medical charts before and after PsA diagnosis (KW and FCE) on a standardized abstraction form. These included the following: myocardial infarction; angina; cardiovascular death; revascularization procedures (i.e., percutaneous coronary angioplasty; coronary artery bypass grafts); congestive heart failure; cerebrovascular disease events (i.e., stroke; transient ischemic attack); and peripheral arterial disease events (i.e., abdominal aortic aneurysm; peripheral vascular disease; renal artery stenosis; arterial thrombosis). Death dates and cause of death were recorded.
Statistical analysis
Descriptive statistics (means, medians, ranges, percentages, etc.) were used to summarize the data. Comparisons of patient characteristics were performed using chi-square and rank sum tests. The FRS for general cardiovascular disease was calculated for patients with available risk factor data (based on age, sex, total cholesterol, high-density lipoprotein cholesterol, systolic blood pressure, smoking status and diabetes mellitus) (19). Some patients did not have lipid measures; hence, the office-based FRS, which does not require lipid values, was also computed according to previously published algorithms (18, 19).
The cumulative incidence of CVD was estimated using product-limit life table methods. Patients with CVD prior to PsA incidence date were excluded from this analysis. To compare the events predicted by FRS to the observed events, observed follow up was truncated at 10 years after PsA incidence. For patients with < 10 years of follow up, the predicted risk of CVD was adjusted proportionately (29). Standardized incidence ratios (SIR), which are ratios of observed CVD in PsA to that predicted by FRS, were calculated assuming that predicted rates are fixed and observed CVD events follow a Poisson distribution. Cox proportional hazards models were used to examine the association between PsA characteristics at time of PsA diagnosis and the risk of CVD events adjusting for age and sex. For the observed curve on the figure, predictions of 10 year CVD risk according to age were obtained from a Cox model adjusted for sex. Smoothing splines were used to model the age effect in order to allow for non-linear relationships. The predicted line on the figure was obtained by applying a smoothing function to the FRS estimates from each patient according to age.
RESULTS
Clinical characteristics
The baseline characteristics of 158 patients in the PsA incidence cohort are in Table 1. Mean age at PsA incidence was 43.4 years (minimum:19 years, maximum:74 years) and 61% were men. One hundred and forty eight (94%) patients had inflammatory joint disease, followed by enthesopathy in 58 (37%) patients, and spine PsA in 16 (10%) patients. At PsA incidence, 96% of patients had either concurrent psoriasis or a personal history of psoriasis, whereas 26% reported a family history of psoriasis. Nail dystrophy and dactylitis were present in 72 (46%) and 59 (38%) patients, respectively. Rheumatoid factor testing was performed in 128 patients and was negative in 124 (97%) patients. Radiographic findings of 64 patients with baseline joint radiographs are in Table 1: erosions (59%), periostitis (19%), and bilateral sacroiliitis (16%) were common. At PsA incidence, mean erythrocyte sedimentation rate was 17 (SD: 15.8) mm/hr and mean C-reactive protein (available in 44 patients) was 18.3 (SD: 20.4) mg/L.
Table 1.
Baseline characteristics of 158 patients with incident psoriatic arthritis (PsA) in 1989–2009
| (N=158) | |
|---|---|
| Age at PsA incidence, years, mean (±SD) | 43.4 (12.5) |
| Male sex | 96 (61%) |
| PsA Disease Characteristics | |
| Joint PsA | 148 (94%) |
| Spine PsA | 16 (10%) |
| Enthesitis | 58 (37%) |
| Current psoriasis at PsA incidence | 147 (93%) |
| Personal history of psoriasis | 5 (3%) |
| Family history of psoriasis | 40 (26%) |
| Nail dystrophy | 72 (46%) |
| Negative rheumatoid factor (among 128 patients tested) | 124 (97%) |
| Dactylitis | 59 (38%) |
| Radiologic findings | |
| Patients with Radiographs | 64 |
| Osteolysis | 7 (11%) |
| Periostitis | 12 (19%) |
| Erosions DIP joints | 8 (12%) |
| Bilateral sacroiliitis | 10 (16%) |
| Unilateral Sacroiliitis | 5 (8%) |
| Erosions | 38 (59%) |
| Erythrocyte Sedimentation Rate (ESR)* | |
| Mean (±SD) | 17.0 (15.8) |
| Median (Q1, Q3) | 12.0 (5.0,27.0) |
| Range | (0.0–85.0) |
| C-reactive protein* | |
| Mean (±SD) | 18.3 (20.4) |
| Median (Q1, Q3) | 8.0 (5.0, 29.0) |
| Range | (1.1–89.7) |
Baseline ESR values were available for 119 patients. Baseline C-reactive protein values were available for 44 patients.
CVD risk factors and events
The mean follow-up time was 11.6 years (total 1837 person-years). Table 2 details the CVD risk factors. At PsA onset, half of the patients were either current (23%) or former smokers (27%). Mean BMI was 30.5 (6.4) kg/m2, and 44% of patients were classified as obese with a BMI ≥30 kg/m2. The prevalence of dyslipidemia, hypertension and type 2 diabetes mellitus was 39%, 37% and 5%, respectively. At PsA incidence, the mean systolic blood pressure was 131.2 (SD: 18.7) mmHg and the mean diastolic blood pressure was 79.1 (SD: 10.9) mmHg. Serum lipid measurements were available in 106 patients and the lipid panel values were as follows: mean total cholesterol was 199.4 (SD: 36.5) mg/dL; mean HDL was 49.3 (SD: 14.5) mg/dL; mean LDL was 121.5 (SD: 31.3 mg/dL; and mean triglycerides were 144.3 (SD: 89.0) mg/dL. Eight patients had their first CVD event prior to PsA incidence. Among the remaining 150 PsA patients, a total of 32 patients experienced at least one cardiovascular event during follow-up. This included 9 patients with MI, 9 with angina, 7 with revascularization procedures, 12 with heart failure, 14 with cerebrovascular events and 10 with peripheral artery disease. This yielded an absolute risk of 17.4 per 1000 person years.
Table 2.
Cardiovascular risk factors in 158 patients with psoriatic arthritis
| (N=158) | |
|---|---|
| Smoking, N (%) | |
| Never | 77 (50%) |
| Current smoker | 36 (23%) |
| Former smoker | 41 (27%) |
| Missing | 4 |
| Type 2 Diabetes Mellitus, N (%) | 8 (5%) |
| Obesity, N (%) | 66 (44%) |
| Body mass index, kg/m2, mean (SD) | 30.5 (6.4) |
| Body mass index, kg/m2 | |
| ≤20 | 2 (1%) |
| 20–25 | 25 (17%) |
| 25–30 | 56 (38%) |
| 30–35 | 37 (25%) |
| >35 | 29 (19%) |
| Missing | 9 |
| Hypertension, N (%) | 58 (37%) |
| Systolic blood pressure, mmHg, mean (SD)* | 131.2 (18.7) |
| Diastolic blood pressure, mmHg, mean (SD)* | 79.1 (10.9) |
| Hypertension Treatment, N (%) | 28 (18%) |
| Dyslipidemia, N (%)** | 41 (39%) |
| Total cholesterol, mg/dl, mean (SD) | 199.4 (36.5) |
| HDL, mg/dl, mean (SD) | 49.3 (14.5) |
| LDL, mg/dl, mean (SD) | 121.5 (31.3) |
| Triglycerides, mg/dl, mean (SD) | 144.3 (89.0) |
Systolic and diastolic blood pressure values were available for 155 patients.
Lipid values were available for 106 (total cholesterol), 102 (HDL), 103 (LDL), 104 (triglycerides) patients. Dyslipidemia status could not be ascertained for 52 patients due to missing laboratory values.
Observed CVD events compared to FRS
There were 126 patients who did not have a prior cardiovascular history and were age ≥ 30 years at PsA incidence; they were included in the analysis that compared observed CVD events in the first 10 years of PsA disease duration to the 10 year CVD risk predicted by the FRS. The mean FRS was 9.7% (SD 10.4%) (Table 3). There were no significant differences between men and women with PsA in the number of CVD risk factors (including current smoking, diabetes mellitus, obesity, hypertension and dyslipidemia) or in FRS (Table 4). During the first 10 years of follow-up after PsA incidence, 18 patients developed CVD (10 males and 8 female). The 10 year cumulative incidence of CVD was 17% (95% confidence interval [CI]: 10%, 24%). This was almost twice as high as the predicted 10 events based on the FRS (SIR: 1.80; 95% CI: 1.14, 2.86; p=0.012). Figure 1 shows the observed 10 year CVD risk according to age along with the average FRS. This figure demonstrates that the observed 10 year CVD risk is consistently twice as high as the FRS beginning after age 40 years.
Table 3.
Cardiovascular risk scores in 126 patients with psoriatic arthritis who were age ≥ 30 years at psoriatic arthritis incidence with no prior cardiovascular disease
| F (N=51) |
M (N=75) |
Total (N=126) |
p value | |
|---|---|---|---|---|
| Number of cardiovascular risk factors* | 0.76 | |||
| 0 | 13 (25%) | 17 (23%) | 30 (24%) | |
| 1 | 23 (45%) | 29 (39%) | 52 (41%) | |
| 2 | 9 (18%) | 18 (24%) | 27 (21%) | |
| 3+ | 6 (12%) | 11 (15%) | 17 (13%) | |
| Framingham risk score**, % | ||||
| Mean (SD) | 8.6 (9.6) | 10.5 (10.8) | 9.7 (10.4) | 0.17 |
| Median (Range) | 5.2 (0.8–57.8) | 7.6 (0.7–57.0) | 6.8 (0.7–57.8) | |
| Framingham risk score categories | 0.43 | |||
| <6% | 26 (52%) | 26 (35%) | 52 (42%) | |
| 6–10% | 10 (20%) | 22 (29%) | 32 (26%) | |
| 10–20% | 9 (18%) | 18 (24%) | 27 (22%) | |
| 20–50% | 4 (8%) | 7 (9%) | 11 (9%) | |
| >50% | 1 (2%) | 2 (3%) | 3 (2%) |
Original Framingham risk score was calculated for 85 patients.
Office-based Framingham risk score was used for the remainder (1 missing value).
Table 4.
Comparison of observed and predicted cardiovascular risk in 126 patients with psoriatic arthritis who were age ≥ 30 years at psoriatic arthritis incidence with no prior cardiovascular disease
| Group | N | Cardiovascular Events* |
Standardized Incidence Ratio (95% confidence interval) |
p- value |
|
|---|---|---|---|---|---|
| Observed | Predicted | ||||
| Total | 126 | 18 | 10.0 | 1.80 (1.14, 2.86) | 0.012 |
| Female | 51 | 8 | 3.5 | 2.28 (1.14, 4.58) | 0.019 |
| Male | 75 | 10 | 6.5 | 1.54 (0.83, 2.86) | 0.17 |
Number of patients
Figure 1.
Comparison of observed (solid line) and predicted (Framingham risk score; dashed line) cardiovascular risk according to age in 126 patients with psoriatic arthritis who were age ≥ 30 years at psoriatic arthritis incidence with no prior cardiovascular disease.
PsA characteristics and CVD risk
We assessed the association between PsA disease characteristics (presented in Table 1) and risk of CVD. There were no significant associations (data not shown) between these features, including elevated acute phase reactants (erythrocyte sedimentation rate and C-reactive protein), presence of sacroiliitis, peripheral inflammatory arthritis, and erosive radiographic disease.
DISCUSSION
In our population-based cohort study, we compared the observed incidence of CVD events with the FRS in newly diagnosed PsA patients, and found that the FRS underestimates the true cardiovascular risk. We observed a 10 year cumulative incidence rate for CVD of 17%, which was about twice as high as predicted by FRS. We also found that the prevalence of CVD risk factors was high: 34% of our patients presented with ≥2 risk factors, although the mean age was only 43 years.
Our findings suggest that the FRS may not be applicable among PsA patients. There are several potential explanations. Of importance, the prevalence of CVD risk factors in our PsA cohort is higher than individuals without PsA. For example, the prevalence of obesity in the US population was 35% in adults over age 18 in 2008–2010 (30); while in 2012, an estimated 18.1% of adults over age 18 were current smokers (31). Smoking is a well-known environmental trigger for psoriasis (32, 33). Similarly, obesity is a risk factor for plaque psoriasis (33). Forty-four percent of our PsA cohort was classified as obese, and 50% of them were either current or former smokers. Moreover, 39% of PsA patients in our cohort had dyslipidemia and 37% had hypertension at PsA onset. Saydah et al. (34) found that the prevalence of CVD risk factors such as hypertension and dyslipidemia increases as adults become overweight or obese. Hence, higher cardiovascular risk assessment scores may be more common in PsA patients than in the general population, potentially affecting the discriminative properties of the FRS. Indeed, Allal-El Asmi et al. (35) found that psoriasis patients had higher 10 year FRS than normal controls, and severe psoriasis was associated with an increased CVD risk.
The FRS may underestimate the extent of cardiac risk in PsA patients because chronic systemic inflammation may lead to endothelial dysfunction, atherosclerosis and other adverse downstream effects not accounted for by risk assessment scoring systems (14, 25). Subclinical atherosclerosis has been detected in PsA patients without traditional cardiovascular risk factors (36). Cardiovascular risk scoring may be difficult in patients with inflammatory arthritis, such as RA, due to the poor discriminative and calibration properties of traditional risk assessment tools (37,38). Indeed, some experts suggest that FRS should be multiplied by 1.5 in RA patients since lower scores may result in missed opportunities for preventive CVD strategies (37–39). Unfortunately, there are few guidelines about preventive management of CVD risk in PsA patients (13). Yet, despite the poor discriminative properties of the FRS in PsA patients, we believe that the practice of using CVD risk assessment tools to target asymptomatic individuals is important for risk reduction strategies. For example, tobacco cessation and weight loss efforts should be emphasized as strategies, especially given the relatively young age of PsA patients at risk for CVD compared to controls (5, 35, 39).
The lack of association between the FRS and disease activity features of PsA in our cohort such as the erythrocyte sedimentation rate (ESR) is in contrast to observations seen in RA patients (14). Potential explanations may be a lower inflammatory burden, poor accuracy of selected disease activity markers in PsA, or a lack of power to assess magnitude of association. Yet, the presence of psoriasis alone may be enough to account for the increased CVD risk in our cohort (5, 35, 40).
There are several potential limitations to consider when interpreting our findings. Despite the large study population, this is a retrospective study without a comparison group. Although we examined the prevalence of CVD risk factors and the predicted FRS in this cohort, we did not compare the risk profile to age- and sex-matched individuals in the general population. Moreover, data collection was limited to disease characteristics and CVD risk factors routinely recorded in the medical records. Also, follow-up was at irregular intervals and limited to an average of 11 years; hence, the time interval may not have been adequate to observe the development of CVD. The predominantly Caucasian population in Olmsted County may limit the generalizability of these results, but likely our findings are reflective of disease risk (40). Additionally, we believe that our PsA cohort is fairly representative of early incident PsA cohorts since their disease characteristics of inflammatory arthritis in an oligoarticular pattern with enthesopathy generally mirrors early PsA patients (22–24).
This study serves to illustrate the important need for further research to focus on the development of CVD risk assessment tools specific to PsA patients. Given the role of systemic inflammation in promoting early atherosclerosis in rheumatic patients (both RA and PsA) (14, 25, 37,38), there may be increased justification for using aggressive therapy early in the arthritis course to attenuate the long-term burden of CVD (42). The strengths of our study are the large and well-characterized incidence cohort of PsA patients identified and assessed at disease onset from a comprehensive medical records system, and the use of strict definitions for CVD risk factors. In summary, our findings demonstrate that patients with newly diagnosed PsA have an increased risk for CVD, and the FRS underestimates the magnitude of this risk.
Significance & Innovations.
The Framingham risk score (FRS) underestimates the true cardiovascular risk profile in patients newly diagnosed with psoriatic arthritis (PsA).
The observed 10 year CVD risk is twice as high as the risk predicted by FRS beginning after age 40 years.
The 10 year cumulative incidence of CVD events in PsA patients was 17%.
Acknowledgments
Conflict of interest disclosure: This publication was made possible by the Rochester Epidemiology Project (R01 AG 034676 from the National Institutes of Health) and an unrestricted research grant from Amgen. Katelynn M. Wilton was supported by the National Institute of General Medical Sciences (T32 GM 65841).
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