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Review | ONLINE FIRST

Psoriasis and the Risk of Diabetes Mellitus:  A Systematic Review and Meta-analysis FREE

April W. Armstrong, MD, MPH; Caitlin T. Harskamp, BA; Ehrin J. Armstrong, MD, MSc
[+] Author Affiliations

Author Affiliations: Departments of Dermatology (Dr A. W. Armstrong and Ms Harskamp) and Cardiovascular Medicine (Dr E. J. Armstrong), University of California, Davis, Sacramento.


JAMA Dermatol. 2013;149(1):84-91. doi:10.1001/2013.jamadermatol.406.
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Published online

Objective To compare the prevalence and incidence of type 2 diabetes mellitus between patients with psoriasis and those without psoriasis.

Data Sources MEDLINE, EMBASE, and Cochrane Database of Systematic Reviews between January 1, 1980, and January 1, 2012.

Study Selection Observational (cohort, case-control, and cross-sectional) studies published in English that compared the prevalence or incidence of diabetes among patients with psoriasis with individuals serving as controls.

Data Extraction Two independent investigators extracted the data. The quality of evidence was assessed using a 6-point scale.

Data Synthesis Among 142 identified publications, 27 observational studies were included in the meta-analysis. Five of these studies assessed the incidence of diabetes in patients with psoriasis and were analyzed separately. Among studies assessing the prevalence, psoriasis was associated with an odds ratio (OR) of 1.59 (95% CI, 1.38-1.83) for diabetes. The pooled OR was 1.53 (95% CI, 1.16-2.04) for mild psoriasis and 1.97 (1.48-2.62) for severe psoriasis. Meta-regression of prespecified potential sources of heterogeneity revealed a nonsignificant difference (P = .10) of increased reported strength of association among studies that used medical record review (OR, 1.52 [95% CI, 1.31-1.77]) or patients' report of diabetes (2.79 [1.42-5.48]) compared with studies that used billing data (1.46 [1.01-2.09]). Among studies that assessed incidence, psoriasis was associated with a relative risk of 1.27 (95% CI, 1.16-1.40) for developing diabetes.

Conclusions Psoriasis is associated with an increased prevalence and incidence of diabetes. The association of psoriasis with diabetes may be strongest among patients with severe psoriasis.

Figures in this Article

Psoriasis is a common, chronic inflammatory skin condition that affects 2% to 4% of the world's population.1,2 Systemic inflammation associated with psoriasis may lead to elevated levels of circulating interleukin 1 (IL-1), IL-6, and tumor necrosis factor that predispose to impaired glucose tolerance and type 2 diabetes mellitus.3 Psoriasis is also associated with increased obesity and features of the metabolic syndrome, which may coexist with diabetes.4 Recent research5 has identified several comorbid conditions associated with psoriasis, including diabetes, hypertension, and dyslipidemia. These risk factors predispose to increased cardiovascular disease and may also independently lead to greater morbidity and mortality.6,7

To better understand the strength of association between psoriasis and diabetes mellitus, we performed a systematic review and meta-analysis of the prevalence and incidence of diabetes among patients with psoriasis.

DATA SOURCES AND SEARCHES

We performed a systematic search using the MEDLINE, EMBASE, and Cochrane Database of Systematic Reviews with the Medical Subject Headings psoriasis and diabetes. We then limited the search to English-language human studies published between January 1, 1980, and January 1, 2012. All the abstracts identified were read to determine eligibility of the report for inclusion in the meta-analysis. To be included, original studies needed to fulfill the following criteria: case-control, cross-sectional, cohort, or nested case-control design; evaluation of diabetes in conjunction with psoriasis; and analyses that compared patients with psoriasis vs control groups. Specifically, the studies had to evaluate the prevalence or incidence of diabetes as defined by physical examination results, patient report, medical record review, or medical billing codes.

STUDY SELECTION

The initial search yielded 142 articles (Figure 1). After manual review of all abstracts, 66 of these studies were chosen for further review. Three of these articles were excluded because they did not address the scope of the meta-analysis, 16 were excluded because they were review articles or editorials, and 6 articles were excluded because of lack of reported odds ratios (ORs), lack of a control group, or a focus only on psoriatic arthritis. After these and other exclusions, 27 articles were included in the meta-analysis.

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Figure 1. Literature search and study selection process. Ps indicates psoriasis; PsA, psoriatic arthritis; and QoL, quality of life.

DATA EXTRACTION AND QUALITY ASSESSMENT

The Meta-analysis of Observational Studies in Epidemiology guidelines were used to guide the analysis.8 Two reviewers (A.W.A. and C.T.H.) independently extracted the data and performed the systematic review, and any disagreements were adjudicated by consensus. For each study included, we recorded the study's year, country in which the study population lived, setting in which the study took place, study design, numbers of the cases and controls, age, sex, whether the results were adjusted for comorbidities, data collection processes (prospective or retrospective), whether the results were a primary or secondary analysis of the publication, and whether the psoriasis disease severity was assessed. To measure study quality, we used a 6-point scale, with values of 0 or 1 assigned to study design, assessment of exposure, assessment of outcome, control for confounding, evidence of bias, and assessment of psoriasis severity. Studies with a score of 0 to 3 were categorized as lower quality and studies with a score of 4 to 6 were categorized as higher quality.9

DATA SYNTHESIS AND ANALYSIS

All studies were observational. Most were cross-sectional or case-control and reported ORs, but one study10 of diabetes incidence consisted of 3 cohorts and was therefore analyzed as 3 studies for meta-analysis. One study11 of prevalence consisted of 2 different cohorts and, for meta-analysis, was treated as 2 studies. Studies that reported prevalence (n = 22) were analyzed separately from those that reported incidence (n = 5). For each study of prevalence, the crude ORs were identified based on the publication. In cases where multivariate adjustment was reported (n = 12), the effect size and reported upper and lower bounds of the 95% CI were log-transformed. The inverse variance method was then used to calculate the pooled OR (for prevalence studies) or relative risk (RR) (for incidence studies). To estimate the pooled RR, we used the fixed-effects and random-effects models of DerSimonian and Laird.12 Study heterogeneity was assessed using the I2 statistic. Because of significant study heterogeneity, reported pooled ORs and RRs were based on random-effects modeling.

Publication bias was assessed using visual inspection of a funnel plot of the study size vs standard error, with formal statistical testing using the Begg adjusted-rank correlation test.13,14 To explore sources of study heterogeneity, we performed meta-regression using prespecified variables and random-effects meta-analysis. Prespecified sources of heterogeneity included study country, subject location (ambulatory or inpatient), multivariate adjustment for confounders, prospective vs retrospective study design, ascertainment of prevalence vs incidence, primary vs secondary analysis, ascertainment of psoriasis disease severity, measure of outcome, case-control vs cohort design, and study quality (0-3 vs 4-6). All analyses were performed using commercial software (Stata, version 11.2; StataCorp).

Twenty-two publications11,1535 reported associations between psoriasis and the prevalence of diabetes (Table 1 and Table 2); all studies were either cross-sectional (n = 6) or case-control (n = 16) in design. The studies were conducted in diverse settings, including large outpatient databases, insurance claims, or inpatient samples. Most of these studies used outpatient medical records or billing codes to identify patients with diabetes, with some studies based on large databases of International Classification of Diseases codes to ascertain the presence of diabetes. Among the 12 studies that adjusted for comorbid conditions,2022,2426,28,29,31,3335the adjusted OR for diabetes among patients with psoriasis ranged from 1.0 to 3.7, with most studies reporting adjusted ORs between 1.3 and 2.0.

Table Graphic Jump LocationTable 1. Study Population Characteristics: Psoriasis and Prevalence of Diabetes Mellitus
Table Graphic Jump LocationTable 2. Study Outcomes: Psoriasis and Prevalence of Diabetes Mellitus

Meta-analysis of diabetes prevalence among patients with psoriasis revealed significant between-study heterogeneity (I2 = 96%). With random-effects modeling, the OR of diabetes was 1.59 (95% CI, 1.38-1.83) (Figure 2). Visual inspection of a funnel plot revealed possible publication bias, but formal testing did not reveal any statistically significant association (P = .9). Exploration of prespecified potential sources of heterogeneity revealed a nonsignificant difference (P = .10) of increased reported strength of association among studies that used medical record review (OR, 1.52 [95% CI, 1.31-1.77])or patients' report of diabetes (2.79 [1.42-5.48]) as compared with studies that used billing data (1.46 [1.01-2.09]). There was no significant effect of study location, relative study quality, or type of analysis on the associated prevalence of diabetes among patients with psoriasis (Table 3).

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Figure 2. Random-effects meta-analysis of the prevalence of diabetes in patients with psoriasis compared with controls. OR indicates odds ratio; dashed vertical line, estimated pooled effect size estimate; lines with solid diamonds, odds ratios (ORs) and 95% CIs; and open diamond, a visual summary of the overall 95% CI of the effect estimate of psoriasis on the prevalence of diabetes (1.38-1.83).

Table Graphic Jump LocationTable 3. Potential Prespecified Sources of Heterogeneity Explored Among the Studies Reporting an Association Between Psoriasis and Diabetes

Four studies systematically examined the relative association of mild psoriasis with the prevalence of diabetes, and 5 studies assessed the association of severe psoriasis with diabetes.15,23,26,33,35 Neimann et al26 reported an adjusted OR for diabetes of 1.13 (95% CI, 1.08-1.18) for mild psoriasis and 1.62 (1.3-2.01) for severe psoriasis. Subsequent studies reported similar levels of association, with a trend toward increased diabetes prevalence among patients with severe compared with mild psoriasis. The pooled OR was 1.53 (95% CI, 1.16-2.04) for mild psoriasis and 1.97 (1.48-2.62) for severe psoriasis (Figure 3).

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Figure 3. Random-effects meta-analysis of the prevalence of diabetes. A, Patients with mild psoriasis compared with controls. B, Patients with moderate to severe psoriasis compared with controls. OR indicates odds ratio; dashed vertical line, pooled effect size estimate; lines with solid diamonds, ORs and 95% CIs; and open diamond, a visual summary of the overall 95% CI of the effect estimate of psoriasis on the prevalence of diabetes.

Five studies10,3639 assessed the incidence of diabetes among patients with psoriasis (Table 4 and Table 5). These studies used large cohorts, including the UK-based General Practice Research Database and the US-based Nurses' Health Study, to assess incident diabetes among patients with psoriasis. Most of these studies did not completely adjust for other covariates that may predispose to diabetes. The most comprehensive study10 combined 3 US-based cohorts and also assessed the relative strength of association of diabetes with psoriasis as a function of age. In this analysis, psoriasis was associated with increased incidence of diabetes among patients younger than 60 years (multivariate RR, 1.26 [95% CI, 1.08-1.46]) but not among older patients with psoriasis (0.91 [95% CI, 0.69-1.20]).

Table Graphic Jump LocationTable 4. Study Population Characteristics: Psoriasis and Incidence of Diabetes Mellitus
Table Graphic Jump LocationTable 5. Study Outcomes: Psoriasis and Incidence of Diabetes Mellitus

Similar to the studies of prevalence, there was significant between-study heterogeneity (I2 = 94.8%). Random-effects meta-analysis was used to assess the association of psoriasis with incident diabetes (Figure 4). The pooled RR of diabetes in patients with psoriasis was 1.27 (95% CI, 1.16-1.40). Prespecified meta-regression did not reveal any association between study location, relative study quality, or other factors on the risk of incident diabetes (data not shown).

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Figure 4. Random-effects meta-analysis of the incidence of diabetes in patients with psoriasis compared with controls. HPFS indicates Health Professionals Follow-up Study; NHS, Nurses' Health Study; OR, odds ratio; RR, relative risk; dashed vertical line, pooled effect size estimate; lines with solid diamonds, ORs and 95% CIs; and open diamond, a visual summary of the overall 95% CI of the effect estimate of psoriasis on the prevalence of diabetes.

In this meta-analysis of observational studies, psoriasis was associated with an increased prevalence and incidence of diabetes. These studies suggest that psoriasis is associated with a 59% increased prevalence of diabetes and a 27% increased risk of developing diabetes among patients with psoriasis. Patients with severe psoriasis, and especially younger patients, may have an even higher risk of developing diabetes.

Although there was significant between-study heterogeneity for studies of both prevalence and incidence, there was no evidence of publication bias. Meta-regression identified several potential sources of heterogeneity, most notably the data collection methods used to identify psoriasis and diabetes. Studies that used large billing databases tended to report a weaker association between the 2 diseases, which may be related to misclassification of patients as having psoriasis and a bias toward a greater percentage of patients with mild psoriasis. Somewhat surprisingly, there was no apparent effect of study location, suggesting that the association of psoriasis with diabetes may be similar among diverse patient populations, ethnic backgrounds, and baseline medical therapy. The report of an association between psoriasis and diabetes among many countries increases the overall generalizability of these results.

All studies of prevalence and all but one substudy of diabetes incidence reported an association between psoriasis and diabetes. The consistent association between psoriasis and diabetes suggests a likely pathophysiologic link between the 2 diseases. Patients with psoriasis have altered T-cell subtype 1 pathways and dysregulated oxidative and angiogenic mechanisms.40,41 Many of these immune pathways may also predispose to impaired glucose tolerance and diabetes. However, the possibility remains that unmeasured confounders may mitigate much of this association. Although most studies adjusted for baseline body mass index and obesity, none of these studies was able to adjust for other potential treatment confounders, such as systemic absorption of topical corticosteroids or use of other systemic medications for treatment of psoriasis. Whether treatment of psoriasis alters incident diabetes is unknown, although a recent study42 of incident diabetes among patients prescribed tumor necrosis factor inhibitors or methotrexate suggested that initiation of treatment with tumor necrosis factor inhibitors was associated with a decreased incidence of diabetes. Future studies should more closely investigate the association between psoriasis, anti-inflammatory agents, and diabetes.

This study has several strengths. We performed a careful systematic review using multiple data sources. Multiple authors reviewed the data independently, thereby minimizing the risk of bias or missing data. By separating prevalence and incidence in the analysis, as well as severity of psoriasis, we were better able to quantify the possible temporal association of psoriasis with diabetes. We also performed several prespecified meta-regression analyses to identify sources of heterogeneity that commonly occur during meta-analyses of observational data. Use of a formal measure for study quality also helped to identify possible issues with data quality inherent to each study design.

As in all analyses, this meta-analysis was restricted to the quality of the data provided by each study. No randomized trials have been performed to assess the effect of interventions on diabetes incidence among patients with psoriasis. Most studies assessed the prevalence of coexistent diabetes and psoriasis rather than incidence. Whether diabetes predates psoriasis in most cases is unknown, but the studies of diabetes incidence suggest that most patients develop diabetes after a diagnosis of psoriasis. None of these studies specifically examined any association between subtypes of psoriasis and diabetes; it is possible that certain subtypes of psoriasis are more strongly associated with diabetes. Most studies did not separate mild from moderate or severe psoriasis. Similar to studies examining the association between psoriasis and incident myocardial infarction, most of the relative risk for diabetes may occur among patients with more severe psoriasis. Future studies should more closely assess the relationship between psoriasis severity, age at disease onset, and diabetes.

In summary, our findings support a robust association between psoriasis and diabetes. Patients with psoriasis, especially those with severe psoriasis, should be educated about the increased risk of developing diabetes. Additionally, primary care physicians, dermatologists, and cardiologists should consider more intensive screening of such patients to identify early-onset diabetes, since several early interventions may decrease subsequent comorbidities associated with diabetes.

Accepted for Publication: August 7, 2012.

Published Online: October 15, 2012. doi:10.1001/2013.jamadermatol.406

Correspondence: April W. Armstrong, MD, Department of Dermatology, University of California, Davis, 3301 C St, Ste 1400, Sacramento, CA 95816 (aprilarmstrong@post.harvard.edu).

Author Contributions: Drs A. W. Armstrong, E. J. Armstrong, and Ms Harskamp had full access to all the data in the study and take responsibility for the integrity of the data and the accuracy of the data analysis. Study concept and design: A. W. Armstrong and E. J. Armstrong. Acquisition of data: A. W. Armstrong and Harskamp. Analysis and interpretation of data: A. W. Armstrong and E. J. Armstrong. Drafting of the manuscript: A. W. Armstrong, Harskamp, and E. J. Armstrong. Critical revision of the manuscript for important intellectual content: A. W. Armstrong. Statistical analysis: A. W. Armstrong and E. J. Armstrong. Administrative, technical, and material support: Harskamp. Study supervision: A. W. Armstrong and E. J. Armstrong.

Conflict of Interest Disclosures: Dr A. W. Armstrong has received research grants and/or consultant honoraria from Abbott Laboratories, Amgen, and Janssen Pharmaceuticals, Inc.

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Figures

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Graphic Jump Location

Figure 1. Literature search and study selection process. Ps indicates psoriasis; PsA, psoriatic arthritis; and QoL, quality of life.

Place holder to copy figure label and caption
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Figure 2. Random-effects meta-analysis of the prevalence of diabetes in patients with psoriasis compared with controls. OR indicates odds ratio; dashed vertical line, estimated pooled effect size estimate; lines with solid diamonds, odds ratios (ORs) and 95% CIs; and open diamond, a visual summary of the overall 95% CI of the effect estimate of psoriasis on the prevalence of diabetes (1.38-1.83).

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Graphic Jump Location

Figure 3. Random-effects meta-analysis of the prevalence of diabetes. A, Patients with mild psoriasis compared with controls. B, Patients with moderate to severe psoriasis compared with controls. OR indicates odds ratio; dashed vertical line, pooled effect size estimate; lines with solid diamonds, ORs and 95% CIs; and open diamond, a visual summary of the overall 95% CI of the effect estimate of psoriasis on the prevalence of diabetes.

Place holder to copy figure label and caption
Graphic Jump Location

Figure 4. Random-effects meta-analysis of the incidence of diabetes in patients with psoriasis compared with controls. HPFS indicates Health Professionals Follow-up Study; NHS, Nurses' Health Study; OR, odds ratio; RR, relative risk; dashed vertical line, pooled effect size estimate; lines with solid diamonds, ORs and 95% CIs; and open diamond, a visual summary of the overall 95% CI of the effect estimate of psoriasis on the prevalence of diabetes.

Tables

Table Graphic Jump LocationTable 1. Study Population Characteristics: Psoriasis and Prevalence of Diabetes Mellitus
Table Graphic Jump LocationTable 2. Study Outcomes: Psoriasis and Prevalence of Diabetes Mellitus
Table Graphic Jump LocationTable 3. Potential Prespecified Sources of Heterogeneity Explored Among the Studies Reporting an Association Between Psoriasis and Diabetes
Table Graphic Jump LocationTable 4. Study Population Characteristics: Psoriasis and Incidence of Diabetes Mellitus
Table Graphic Jump LocationTable 5. Study Outcomes: Psoriasis and Incidence of Diabetes Mellitus

References

Gelfand JM, Weinstein R, Porter SB, Neimann AL, Berlin JA, Margolis DJ. Prevalence and treatment of psoriasis in the United Kingdom: a population-based study.  Arch Dermatol. 2005;141(12):1537-1541
PubMed   |  Link to Article
Stern RS, Nijsten T, Feldman SR, Margolis DJ, Rolstad T. Psoriasis is common, carries a substantial burden even when not extensive, and is associated with widespread treatment dissatisfaction.  J Investig Dermatol Symp Proc. 2004;9(2):136-139
PubMed   |  Link to Article
Boehncke S, Thaci D, Beschmann H,  et al.  Psoriasis patients show signs of insulin resistance.  Br J Dermatol. 2007;157(6):1249-1251
PubMed   |  Link to Article
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PubMed  |  Link to Article   |  Link to Article
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