Abstract
Previous studies have found a positive association between psoriasis and diabetes/diabetes-related complications, but the association has not been studied in a nationally representative U.S. sample. Our analysis of NHANES data indicated that psoriasis was not associated with diabetes but was positively associated with hypertension, overweight/obesity and waist circumference.
Introduction
Psoriasis is an autoimmune disease affecting 7.5 million Americans(1). There is increasing evidence that psoriasis is associated with the prevalence and incidence of diabetes and diabetes-related complications(2–9). Prospective studies from several countries have found that the risk of developing diabetes is increased among those with psoriasis, especially among those with more severe psoriasis(10–13). Although the mechanism is unclear, the chronic inflammatory state of psoriasis may impact the development of diabetes, which is also associated with inflammatory processes(14).
To our knowledge, there are no nationally representative studies in the United States (U.S.) on the relationship between psoriasis and diabetes; the current study investigates the association between psoriasis and diabetes and diabetes-related complications in the National Health and Nutrition Examination Survey (NHANES).
Materials and Methods
NHANES is a stratified multistage probability survey conducted in the non-institutionalized U.S. population(15). Self-reported data on psoriasis were available in 2003–2006 and 2009–2010. In 2003–2006, a dermatology questionnaire was implemented; participants were asked “Have you ever been told by a health care provider that you had psoriasis?” If participants answered “yes,” they were further queried on severity. Psoriasis was ascertained using the same question in 2009–2010 but the question was included as part of a list of medical conditions and participants were not asked about severity. To determine diabetes status, all participants were asked “Other than during pregnancy, have you ever been told by a doctor or health professional that you have diabetes?” The total study sample included 12,737 adults age ≥20 years (n=345 with psoriasis and n=1,084 with diabetes). Smoking status, history of cardiovascular disease (CVD) or stroke, and retinopathy were self-reported. Obesity was determined using measured height and weight to determine body mass index; waist circumference was measured. Blood pressure was determined based on the average of up to three measurements. High density lipoprotein (HDL) cholesterol was directly measured. Chronic kidney disease was determined using the Chronic Kidney Disease Epidemiology Collaboration equation(16). Participants with an albumin/creatinine ratio of 30–300 mg/g or >300mg/g were considered to have microalbuminuria or macroalbuminuria, respectively.
The unadjusted prevalences of diabetes and diabetes-related complications were determined by psoriasis status. Multivariable logistic regression (odds ratios, 95% confidence intervals) was used to evaluate the association of psoriasis with diabetes and diabetes-related complications in the total population and among those with diabetes. Models were initially adjusted for age, sex, race/ethnicity and then additionally adjusted for smoking and obesity. Data were analyzed using SUDAAN software (version 11.0; Research Triangle Institute, Research Triangle Park, North Carolina) to account for the complex sampling design.
Results
The mean age of participants was 46.9 years with women accounting for 51.9% of the study population. The majority of participants were non-Hispanic white (70.1%) and the prevalence of psoriasis was 3.3%.
The prevalence of self-reported diabetes was 8.1% among adults with psoriasis and 8.5% among those without psoriasis (p≥0.05) (Table 1). The prevalence of history of cardiovascular disease, hypertension, overweight and obesity, and high waist circumference were significantly higher among participants with compared to those without psoriasis. The prevalence of a history of stroke and retinopathy were lower among participants with compared to those without psoriasis.
Table 1.
Unadjusted prevalence of diabetes, diabetes comorbidities, and diabetes-related complications by the presence of psoriasis, NHANES 2003–2006 and 2009–2010
| Psoriasis | No Psoriasis | |
|---|---|---|
| % (SE) | % (SE) | |
| Diabetes | 8.1 (2.51) | 8.5 (0.37) |
| History CVD | 11.8 (2.38) | 6.3 (0.41)* |
| History of Stroke | 1.3 (0.61) | 2.6 (0.20)* |
| Retinopathy† | 7.2 (3.92) | 18.0 (1.50)* |
| Chronic kidney disease | 8.6 (1.48) | 8.8 (0.68) |
| Microalbuminuria‡ | 11.6 (2.67) | 8.6 (0.50) |
| Macroalbuminuria | 0.8 (0.46) | 1.4 (0.15) |
| Hypertension§ | 62.2 (4.39) | 47.5 (1.35)* |
| Body mass index ≥ 25 kg/m2 | 80.8 (3.19) | 68.2 (0.75)* |
| Body mass index ≥ 30 kg/m2 | 45.8 (3.48) | 35.2 (0.95)* |
| High waist circumference | 67.5 (3.32) | 54.5 (0.99)* |
| Low HDL | 37.6 (3.44) | 31.9 (0.87) |
P-value<0.05 compared those with psoriasis
Among people with diabetes
Microalbuminuria: Albumin creatinine ratio 30–300mg/g; Macroalbuminuria: Albumin creatinine ratio >300mg/g
Blood pressure ≥140/80mmHg or currently taking blood pressure medication
Psoriasis was not associated with diabetes, CVD, stroke, or microvascular diseases in logistic regression models (Table 2). Those with psoriasis were significantly more likely to have hypertension, be overweight, and have a high risk waist circumference after adjusting for age, sex, race/ethnicity, smoking, and obesity.
Table 2.
Odds ratios (95% confidence intervals) of diabetes comorbidities and diabetes-related complications associated with psoriasis, NHANES 2003–2006 and NHANES 2009–2010
| Total Population | Diabetes Population | |||||
|---|---|---|---|---|---|---|
| Model 1 | Model 2 | Model 3 | Model 1 | Model 2 | Model 3 | |
| OR (95% CI) | OR (95% CI) | OR (95% CI) | OR (95% CI) | OR (95% CI) | OR (95% CI) | |
| Diabetes | 0.94 (0.46–1.90) | 0.95 (0.46–1.99) | 0.86 (0.39–1.88) | |||
| Cardiovascular disease† | 1.14 (0.86–1.51) | 1.00 (0.75–1.35) | 1.13 (0.65–1.98) | 1.05 (0.35–3.14) | 0.86 (0.27–2.73) | 0.40 (0.10–1.59) |
| Stroke | 0.48 (0.20–1.17) | 0.46 (0.21–1.02) | 0.50 (0.18–1.44) | 0.15 (0.02–1.20) | 0.14 (0.02–1.14) | ¶ |
| Retinopathy‡ | 0.35 (0.10–1.20) | 0.38 (0.11–1.32) | 0.24 (0.02–2.37) | 0.35 (0.10–1.20) | 0.38 (0.11–1.32) | 0.24 (0.02–2.37) |
| Chronic kidney disease | 0.97 (0.64–1.48) | 1.03 (0.59–1.80) | 0.99 (0.58–1.71) | 0.35 (0.08–1.59) | 0.29 (0.07–1.12) | 0.17 (0.04–0.76) |
| Micro-/ Macroalbuminuria§ | 1.27 (0.74–2.17) | 1.31 (0.75–2.28) | 1.35 (0.76–2.38) | 0.58 (0.12–2.70) | 0.59 (0.14–2.53) | 0.55 (0.10–2.85) |
| Hypertension|| | 1.82 (1.28–2.60) | 1.80 (1.20–2.71) | 1.73 (1.11–2.68) | 1.20 (0.21–6.71) | 1.17 (0.19–7.29) | 0.96 (0.16–5.68) |
| Body mass index ≥ 25 kg/m2 | 1.97 (1.29–3.00) | 2.03 (1.33–3.12) | 2.06 (1.34–3.18) | 2.93 (0.66–12.95) | 2.79 (0.70–11.09) | 2.84 (0.69–11.73) |
| Body mass index ≥ 30 kg/m2 | 1.56 (1.15–2.11) | 1.59 (1.16–2.17) | 1.60 (1.17–2.19) | 1.62 (1.29–2.04) | 1.55 (0.46–5.24) | 1.60 (0.48–5.37) |
| High waist circumference | 1.73 (1.27–2.36) | 1.74 (1.19–2.54) | 1.74 (1.19–2.55) | 3.74 (1.01–13.86) | 3.42 (1.09–10.73) | 3.44 (1.10–10.78) |
| Low HDL | 1.28 (0.97–1.70) | 1.29 (0.97–1.71) | 1.09 (0.81–1.46) | 2.60 (1.00–6.79) | 2.56 (1.02–6.44) | 2.25 (0.88–5.71) |
Model 1: Unadjusted
Model 2: Adjusted for age, sex, race/ethnicity
Model 3: Adjusted for age, sex, race/ethnicity, obesity and smoking (obesity not included in models with body mass index, waist circumference, or obesity as the outcome)
In NHANES, cardiovascular disease includes heart failure, coronary heart disease, angina, or heart attack
Among people with diabetes
Microalbuminuria/macroalbuminuria: Albumin creatinine ratio ≥ 30mg/g
Blood pressure ≥ 140/80 mmHg or currently taking blood pressure medication
1 case with both psoriasis and the outcome
Among participants with diabetes, those with psoriasis were significantly more likely to have a high waist circumference; they were less likely to have chronic renal disease after adjusting for age, sex, race/ethnicity, smoking, and obesity (Table 2).
Discussion
Although several studies have shown that psoriasis is associated with diabetes and its complications, results from the current study did not support previous findings. There was no association between psoriasis and diabetes in unadjusted models and after adjusting for demographic factors, obesity and smoking status. In addition, there was no association between psoriasis and CVD, stroke, and microvascular diseases.
However, there were associations between psoriasis and hypertension, obesity, and waist circumference which are risk factors for diabetes and CVD. Previous literature has documented these associations(6, 13, 17, 18). In this cross-sectional study it might be expected that there would be a stronger association with risk factors since they are more proximate in the natural history of disease than diabetes and CVD.
Previous studies have found associations between psoriasis and diabetes only among those with more severe psoriasis(3, 6, 10). NHANES had some information on severity, but too few participants reported having severe psoriasis and diabetes (n=5) to investigate the association by severity. In addition, participants may mistakenly include non-psoriasis skin lesions when self-reporting a diagnosis of the disease. To the authors’ knowledge, the validity of self-reported psoriasis has not been documented.
Strengths of the study include data from a nationally representative sample and use of a data-rich survey. A limitation was that few people had both psoriasis and diabetes, which may have resulted in substantial random variability limiting the ability to detect a true association. However, the odds ratio for psoriasis and diabetes and cardiovascular disease was robust in unadjusted and adjusted models.
Despite no significant association between psoriasis and diabetes, there were several significant associations with comorbid risk factors, including hypertension and obesity. Further research is needed in large nationally representative samples with valid information on psoriasis diagnosis and severity to better assess the association of psoriasis with diabetes and diabetes-related complications in the general population.
Acknowledgments
The findings and conclusions in this report are those of the authors and do not necessarily represent the views of the National Institute of Diabetes and Digestive and Kidney Diseases (NIDDK). This work has been approved by the NIDDK.
Footnotes
Conflicts of Interest
The authors have no conflicts of interest to disclose.
Publisher's Disclaimer: This is a PDF file of an unedited manuscript that has been accepted for publication. As a service to our customers we are providing this early version of the manuscript. The manuscript will undergo copyediting, typesetting, and review of the resulting proof before it is published in its final citable form. Please note that during the production process errors may be discovered which could affect the content, and all legal disclaimers that apply to the journal pertain.
References
- 1.National Psoriasis Foundation. Symptoms and Prevalence. 2013 [Google Scholar]
- 2.Armstrong AW, Harskamp CT, Armstrong EJ. Psoriasis and the risk of diabetes mellitus: a systematic review and meta-analysis. JAMA Dermatol. 2013;149(1):84–91. doi: 10.1001/2013.jamadermatol.406. [DOI] [PubMed] [Google Scholar]
- 3.Armstrong AW, Schupp C, Bebo B. Psoriasis comorbidities: results from the National Psoriasis Foundation surveys 2003 to 2011. Dermatology. 2012;225(2):121–6. doi: 10.1159/000342180. [DOI] [PubMed] [Google Scholar]
- 4.Cheng J, Kuai D, Zhang L, Yang X, Qiu B. Psoriasis increased the risk of diabetes: a meta-analysis. Arch Dermatol Res. 2012;304(2):119–25. doi: 10.1007/s00403-011-1200-6. [DOI] [PubMed] [Google Scholar]
- 5.Husted JA, Thavaneswaran A, Chandran V, Eder L, Rosen CF, Cook RJ, et al. Cardiovascular and other comorbidities in patients with psoriatic arthritis: a comparison with patients with psoriasis. Arthritis Care Res (Hoboken) 2011;63(12):1729–35. doi: 10.1002/acr.20627. [DOI] [PubMed] [Google Scholar]
- 6.Neimann AL, Shin DB, Wang X, Margolis DJ, Troxel AB, Gelfand JM. Prevalence of cardiovascular risk factors in patients with psoriasis. J Am Acad Dermatol. 2006;55(5):829–35. doi: 10.1016/j.jaad.2006.08.040. [DOI] [PubMed] [Google Scholar]
- 7.Yeung H, Takeshita J, Mehta NN, Kimmel SE, Ogdie A, Margolis DJ, et al. Psoriasis Severity and the Prevalence of Major Medical Comorbidity: A Population-Based Study. JAMA Dermatol. 2013 doi: 10.1001/jamadermatol.2013.5015. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 8.Reich K. The concept of psoriasis as a systemic inflammation: implications for disease management. J Eur Acad Dermatol Venereol. 2012;26 (Suppl 2):3–11. doi: 10.1111/j.1468-3083.2011.04410.x. [DOI] [PubMed] [Google Scholar]
- 9.Janin B. Psoriasis plus diabetes equals heightened vascular risk. Family Practice News. 2012 [Google Scholar]
- 10.Azfar RS, Seminara NM, Shin DB, Troxel AB, Margolis DJ, Gelfand JM. Increased risk of diabetes mellitus and likelihood of receiving diabetes mellitus treatment in patients with psoriasis. Arch Dermatol. 2012;148(9):995–1000. doi: 10.1001/archdermatol.2012.1401. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 11.Khalid U, Hansen PR, Gislason GH, Lindhardsen J, Kristensen SL, Winther SA, et al. Psoriasis and New-Onset Diabetes Mellitus: A Danish nationwide cohort study. Diabetes Care. 2013 doi: 10.2337/dc12-2330. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 12.Li W, Han J, Hu FB, Curhan GC, Qureshi AA. Psoriasis and risk of type 2 diabetes among women and men in the United States: a population-based cohort study. J Invest Dermatol. 2012;132(2):291–8. doi: 10.1038/jid.2011.319. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 13.Qureshi AA, Choi HK, Setty AR, Curhan GC. Psoriasis and the risk of diabetes and hypertension: a prospective study of US female nurses. Arch Dermatol. 2009;145(4):379–82. doi: 10.1001/archdermatol.2009.48. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 14.Wellen KE, Hotamisligil GS. Inflammation, stress, and diabetes. J Clin Invest. 2005;115(5):1111–9. doi: 10.1172/JCI25102. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 15.Centers for Disease Control and Prevention (CDC). National Center for Health Statistics (NCHS); Centers for Disease Control and Prevention, editor. US Department of Health and Human Services. Hyattsville, MD: 2005–2010. National Health and Nutrition Examination Survey. [Google Scholar]
- 16.Levey AS, Stevens LA, Schmid CH, Zhang YL, Castro AF, 3rd, Feldman HI, et al. A new equation to estimate glomerular filtration rate. Ann Intern Med. 2009;150(9):604–12. doi: 10.7326/0003-4819-150-9-200905050-00006. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 17.Herron MD, Hinckley M, Hoffman MS, Papenfuss J, Hansen CB, Callis KP, et al. Impact of obesity and smoking on psoriasis presentation and management. Arch Dermatol. 2005;141(12):1527–34. doi: 10.1001/archderm.141.12.1527. [DOI] [PubMed] [Google Scholar]
- 18.Sterry W, Strober BE, Menter A. Obesity in psoriasis: the metabolic, clinical and therapeutic implications. Report of an interdisciplinary conference and review. Br J Dermatol. 2007;157(4):649–55. doi: 10.1111/j.1365-2133.2007.08068.x. [DOI] [PubMed] [Google Scholar]