doi: 10.1111/1346-8138.12721

Journal of Dermatology 2015; 42: 148–153

ORIGINAL ARTICLE

Association between psoriasis and leisure-time physical activity: Findings from the National Health and Nutrition Examination Survey Young Kyung DO,1,2 Naheed LAKHANI,3 Rahul MALHOTRA,4 Brian HALSTATER,5 Colin THENG,6 Truls ØSTBYE4,5 1

Department of Health Policy and Management, Seoul National University College of Medicine, 2Institute of Health Policy and Management, Seoul National University Medical Research Center, Seoul, Korea, 3Emory University, Atlanta, Georgia, 5Duke University Medical Center, Durham, North Carolina, USA, 4Duke-NUS Graduate Medical School Singapore, and 6National Skin Center, Singapore, Singapore

ABSTRACT Despite evidence that physical activity can reduce the cardiometabolic risk of patients with psoriasis, these patients may engage in less physical activity than those without psoriasis. The aim of this study was to examine the association of the extent of psoriatic skin lesions with the likelihood of participating in leisure-time moderate to vigorous physical activity (MVPA) and metabolic equivalent task (MET)-minutes of MVPA amongst those who participated. The National Health and Nutrition Examination Survey (NHANES) is a population-based survey among US adults. A total of 6549 persons aged 20–59 years responded to the 2003–2006 NHANES dermatology questionnaires, which asked about participation in leisure-time MVPA and MET-minutes of MVPA amongst those who participated. Compared with individuals without psoriasis, those with psoriasis were less likely to have engaged in leisure MVPA in the past 30 days, although this association was not statistically significant. Amongst those who participated in leisure-time MVPA, MET-minutes of leisure-time MVPA were lower on average for patients currently having few to extensive cutaneous lesions (but not for those currently having little or no psoriatic patches), relative to individuals never diagnosed with psoriasis by approximately 30%. Clinicians should encourage patients with psoriasis, especially those with more severe disease, to be more physically active; they should help identify and address possible psychological and physical barriers to their patients’ physical activity.

Key words:

cardiometabolic risk, epidemiology, physical activity, psoriasis, public health.

INTRODUCTION Psoriasis affects 2% of the US population,1,2 with a bimodal age of onset of between 15 and 20 years and 55 and 60 years.1,3–5 A nationally representative survey of US adults showed that metabolic syndrome was approximately twice as common in those with psoriasis compared with those without, independent of age, sex, race/ethnicity, smoking status and C-reactive protein levels.6 The risk of developing diseases associated with metabolic syndrome is positively correlated with psoriasis and disease severity.7,8 Physical activity can not only reduce the severity of psoriasis lesions, but can also prevent or reduce the occurrence of metabolic syndrome through decreased adiposity, inflammation, oxidative stress and adhesion molecules.6 Nevertheless, there is a concern that patients with psoriasis engage in less physical activity than those without psoriasis. In

addition to chronic cutaneous manifestations, psoriasis patients also often experience problems with self-esteem, body image, depression, stigmatization and social rejection.9,10 A survey amongst 104 patients with psoriasis found that 11.5% avoided leaving their home, 64% avoided communal showers, 64% avoided wearing shorts or short-sleeved shirts, 72% avoided swimming and 40% avoided sports; these behaviors could decrease the level of engagement in physical activity both directly and indirectly.11 Three other studies found that approximately one-third of psoriasis patients in each study reported difficulty playing sports.12–14 In addition to psychosocial reasons for avoidance of physical activity, physiological factors also likely play a role. Psoriatic skin lesions interfere with sweating because sweating rate is proportional to the amount of healthy skin, which is reduced in patients with active lesions. During exercise, patients with psoriasis also have comparatively higher heart rates than those without psoriasis,

Correspondence: Young Kyung Do, M.D., M.P.H., Ph.D., Department of Health Policy and Management, Seoul National University College of Medicine, 103 Daehak-ro, Jongno-gu, Seoul 110-799, Korea. Email: [email protected] Received 23 April 2014; accepted 8 October 2014.

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indicating that patients with psoriasis do not tolerate the same exercise intensity in hot or humid conditions.15 Furthermore, individuals with psoriasis are at risk of developing psoriatic arthritis,16 and adults with arthritis are less physically active.17 Pruritus is also a common feature of psoriasis, and ambient heat and sweating, common elements of physical activity, exacerbate the itchiness.18,19 Finally, psoriatic skin lesions may also develop at the site of trauma or injury (Koebner’s phenomenon), which is particularly common amongst athletes.1 Overall, there is limited research examining physical activity amongst patients with psoriasis. A recent review identified nine such studies;20 however, these were primarily based on small, non-nationally representative samples. These studies also did not consider the relationship between severity of psoriasis and physical activity or used very crude measures of physical activity. In fact, the review concluded that further exploration of the relationship between the severity of psoriasis and physical activity is needed. This relationship is of interest to the clinicians caring for patients with psoriasis, especially dermatologists, who are well positioned to address both physiological and psychosocial barriers to exercise and physical activity amongst these patients. The current study is based on a large, nationally representative sample of US adults. The objective is to examine the association of the extent of psoriatic skin lesions with the likelihood of participating in leisure-time moderate to vigorous physical activity (MVPA) and metabolic equivalent task (MET)-minutes of MVPA.

METHODS These analyses are based on data from the National Health and Nutrition Examination Survey (NHANES). The NHANES is a program under the Centers for Disease Control and Prevention (CDC) designed to assess the health and nutritional status of adults and children in the USA. A nationally representative sample of approximately 5000 persons is examined each year.21 Our analysis sample comprised individuals who were selected to answer the 2003–2004 and 2005–2006 NHANES dermatology questionnaires which included questions regarding respondents’ psoriasis status. By using a complex study design, the respondents selected were representative of the non-institutionalized US civilian population aged 20–59 years from 2003 through 2006. The NHANES datasets from 2003– 2004 and 2005–2006 were combined to increase statistical reliability, as recommended by the NHANES analytic guidelines.22 The two study outcomes were the indicator variable of any participation in leisure-time MVPA in the past 30 days (1 if “yes”, 0 if “no”) and the natural logarithm of MET-minutes of leisure-time MVPA over the past 30 days prior to the survey. These two outcomes were derived from responses to four survey questions on leisure-time activities (where “SP” refers to “sample person”): (i) “what (vigorous/moderate) activities did (you/SP) do?”; (ii) reported intensity level of activity; (iii) “how often did (you/SP) do (activity)?”; and (iv) “on average, approximately how long did (you/SP) do (activity) each time?” Participation in leisure-time MVPA was determined by whether the

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respondent had taken part in any leisure-time MVPA in the past 30 days. MET-minutes of leisure-time MVPA in the past 30 days was calculated by summing for each respondent the products of (iii), (iv) and the MET (in kilocalories per kilogram of bodyweight per hour) associated with (ii) for each of his/her responses to (i).23–25 The variable of MET-minutes of leisuretime MVPA was log-transformed to better account for its rightskewed distribution in the linear regression model. The predictor of interest was the presence of a psoriasis diagnosis and the extent of psoriatic skin lesions. This was determined by responses to two questions in the dermatology questionnaire: “(have you/ has SP) ever been told by a healthcare provider that (you/he/she) had psoriasis (sore-eye-asis)?” and for those who responded “yes”, the question “(do you/ does SP) currently have: (i) little or no psoriasis; (ii) only a few patches (that could be covered by one or two palms of [your/ his/her] hand); (iii) scattered patches (that could be covered between three and 10 palms of [your/his/her] hand); or (iv) extensive psoriasis (covering large areas of the body, that would be more than 10 palms of [your/his/her] hand)?” For our analysis, we combined (ii), (iii) and (iv) due to small frequency counts. Informed by the published work on the factors associated with physical activity,26 the following covariates were included based on the availability of relevant variables in the data: age, sex, race (“white”, “black”, “other”), education level (“less than 9th grade”, “9th–11th grade, including 12th grade with no diploma”, “high school graduate, GED or equivalent”, “some college or AA degree”, “college graduate or above”), body mass index (BMI), household size (“1–2 persons”, “3–4 persons”, “5 or more persons”) and marital status (“married”, “widowed”, “divorced/separated”, “living with partner”, “never married”). We examined the association of the presence and extent of psoriatic skin lesions with the likelihood of participating in leisure-time MVPA using logistic regression and with the natural logarithm of MET-minutes of leisure-time MVPA using linear regression. After examining the unadjusted associations, regression models, adjusting for age, sex, race, education, BMI, household size, marital status, and survey year, were estimated. Sample weights and the complex survey design were taken into account. All statistical analyses were performed using Stata version 12 (StataCorp LP, College Station, TX, USA). This study was approved by the National University of Singapore institutional review board on 24 December 2012 (reference code: 12-485).

RESULTS Our combined dataset consisted of a total of 6549 respondents, comprising 3140 respondents from the 2003–2004 survey and 3409 respondents from the 2005–2006 survey. Three hundred and eighty-three (5.8%) observations with missing values for at least one of the study variables were dropped from our analysis. Table 1 presents a summary of statistics by extent of psoriatic skin lesion. Approximately 1.7% reported having been diagnosed with psoriasis but currently having little

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Table 1. Summary statistics, by extent of psoriatic skin lesion

Percentage (weight-applied) Any leisure-time MVPA in past 30 days, % MET–minutes of leisure-time MVPA if any, mean Mean age, years Female, % Race, % White Black Other Education, % Less than 9th grade Less than 12th grade completion High school graduate Some college or AA degree College graduate or above Body mass index Household size, % 1–2 persons 3–4 persons ≥5 persons Marital status Married Widowed Divorced/separated Living with partner Never married

Never diagnosed with psoriasis (n = 6011) 96.8

Little or no psoriasis (n = 84) 1.7

Few patches to extensive psoriasis (n = 71) 1.5

69.7 6769.1

66.5 8360.4

64.5 3772.1

39.1 50.8

41.9 59.6

41.0 49.3

68.6 12.3 19.2

77.7 8.9 13.4

89.7 5.9 4.4

4.8 10.8 25.1 33.6 25.7 28.4

1.4 6.1 20.0 36.6 35.9 29.5

2.2 12.6 21.9 40.9 22.4 31.7

38.5 41.7 19.8

42.5 39.7 17.9

45.3 40.1 14.7

57.0 1.3 12.3 9.1 20.3

62.9 0.4 13.0 10.5 13.3

68.4 0.0 8.4 4.3 18.9

Sampling weight-applied means (continuous variables) and percentages (for categorical variables) are presented. MET, metabolic equivalent task; MVPA, moderate to vigorous physical activity.

or no psoriasis, while 1.5% reported currently having few to extensive patches. The probability of participating in any leisure-time MVPA was lower in both groups of individuals with psoriasis. Amongst individuals who participated in any leisuretime MVPA in the past 30 days, individuals with little or no psoriatic skin patches spent more MET-minutes than those never diagnosed with psoriasis, while those with few patches or more extensive skin lesions spent much less MET-minutes.

Several notable differences in demographic and other characteristics exist, particularly with regard to race and BMI. Table 2 shows the association of the extent of psoriatic skin lesions with leisure-time MVPA. The odds of participation in leisure-time MVPA for an individual ever diagnosed with psoriasis, irrespective of the extent of skin lesions, was lower than that of someone never diagnosed with psoriasis but not statistically significantly different at the 5% level in both unadjusted

Table 2. Association of the extent of psoriatic skin lesions with leisure-time moderate to vigorous physical activity Any MVPA in past 30 days Dependent variable Extent of psoriatic skin lesion Never diagnosed with psoriasis (ref.) Little or no psoriasis Few patches to extensive psoriasis n

Logged MET–minutes of leisure-time MVPA

Unadjusted

Adjusted

Unadjusted

Adjusted

OR

95% CI

OR

95% CI

b

b

1



1



0

0.86 0.79

0.53 to 1.41 0.40 to 1.55

0.72 0.75

0.41 to 1.26 0.36 to 1.57

0.34 0.36*

6166

95% CI –

95% CI 0

0.04 to 0.72 0.69 to 0.03

0.37 0.31*

– 0.02 to 0.76 0.57 to 0.05

3992

*P < 0.05. Adjusted logistic regression (any MVPA in past 30 days) and linear regression (logged MET-minutes of leisure-time MVPA) account for age, sex, race, education, body mass index, marital status, household size and survey year. CI, confidence interval; MET, metabolic equivalent task; MVPA, moderate to vigorous physical activity; OR, odds ratio.

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and adjusted logistic regression models. Amongst individuals who participated in any leisure-time MVPA in the past 30 days, those diagnosed with psoriasis and currently with few patches or more extensive skin lesions spent 31% (95% confidence interval, 0.57 to 0.05) less MET-minutes on leisure-time MVPA on average as compared with those never diagnosed with psoriasis, even after adjusting for demographic and other individual characteristics. Individuals diagnosed with psoriasis but currently with little or no psoriatic skin patches spent more MET-minutes on leisure-time MVPA than those never diagnosed with psoriasis, but the association was statistically insignificant at the 5% level in both unadjusted and adjusted models.

DISCUSSION The results of this study suggest that, when compared with individuals without psoriasis, those with psoriasis are less likely to engage in leisure-time MVPA in the past 30 days, although this association is not statistically significant. Amongst those who participate in leisure-time MVPA, individuals currently having few to more extensive psoriatic skin lesions tend to be less physically active when compared with those never diagnosed with psoriasis, despite the substantial health benefit of physical activity,27 particularly in this specific population group. These findings have both clinical and public health implications. While the underlying chronic inflammatory processes of psoriasis are proposed to contribute to the greater prevalence and incidence of chronic cardiometabolic risk factors amongst individuals with psoriasis, the findings suggest that reduced levels of leisure-time MVPA amongst patients with moderate to severe psoriasis may be an important modifiable risk factor for the increased cardiometabolic risk amongst patients with psoriasis. Given the well-established benefits of physical activity in preventing cardiometabolic risk, dermatologists should encourage psoriasis patients, especially those with more severe disease, to participate in activities considered to be moderate to vigorous in nature for a longer duration. They should also identify and address possible barriers to physical activity, such as psoriatic arthritis,28,29 and other comorbid conditions amongst patients with psoriasis.30 Many of these patients are also increasingly being cared for by non-dermatologists,31 including primary care physicians, who are likely to see the patients over an extended period regardless of the degree of psoriasis severity, and both dermatologists and primary care physicians have the opportunity to identify and address barriers to physical activity and other comorbid conditions. Referrals to social support groups, local community resources, social workers and psychologists can also help overcome some of the psychosocial barriers that these patients have. Patients with more significant psychological disease, such as those with more severe anxiety, agoraphobia or depression, may be treated with pharmacological therapies. Finally, given that psychosocial challenges faced by patients with psoriasis in pursuing such activities are likely to persist, the larger public health community also needs to work to reduce the perceived and actual stigma for psoriasis.

© 2014 Japanese Dermatological Association

Our study provides a more complete picture of the association between psoriasis and physical activity than reported in previous studies. The limited published work on this association provides conflicting results. While most earlier studies suggest physical activity is lower amongst those with psoriasis, especially those with severe psoriasis, a few studies report absence of any association.32 Other than the variation in the definitions and measures used to assess physical activity and psoriasis, one reason for the inconsistent results could be the susceptibility of the physical activity variable to a floor effect (i.e. many individuals may have a value of zero while assessing duration or intensity of MVPA). Taking this susceptibility into consideration, our statistical models differentiated any MVPA from MET-minutes of MVPA. The overall findings of this study underscore the importance of accounting for the heterogeneity amongst patients with psoriasis and the extent of psoriatic skin lesions in relation to physical activity. As patients with more severe skin lesions are at a higher risk for cardiometabolic disease and having lower levels of physical activity, these patients require special attention from their treating clinicians. This study has several limitations that point to research questions for future studies. First, our cross-sectional data make it difficult to separate the causal effect of the severity of psoriatic skin lesions on MVPA from the alternative explanation of the association observed. Physical activity itself may reduce the risk of incidence of psoriasis,32 and exposure to sunlight during outdoor physical activity can improve psoriatic skin lesions.33,34 Second, the measure of the extent of psoriatic skin lesions and the diagnosis of psoriasis were based on selfreports and may not be comprehensive; it did not account for the morphology or the site of the skin lesions or for the duration for which individuals had had psoriasis. However, this measure has been extensively utilized before, especially in large, population-based surveys given operational challenges.12,28,35,36 Further, it is reported that individuals with psoriasis reliably report on the extent of involvement of their body surface area.37 Additionally, the classification style of questions used by NHANES has been taken from surveys conducted by the National Psoriasis Foundation.35 Nevertheless, utilization of more comprehensive scales or indices such as the SelfAdministered Psoriasis Area Severity Index37 should be considered in future studies. In addition to capturing the physical extent of psoriatic skin lesions, some researchers have suggested considering the “psychological” extent, which may not entirely correlate with the physical severity.38 This may be important in the context of physical activity as an outcome, because mood has been shown to be associated with reduced participation and extent of physical activity.39,40 Third, the limited number of patients with psoriasis included in our data precluded more detailed analysis by the extent of skin lesions or by potentially important subgroups, such as sex and race/ ethnicity. Fourth, our analysis did not contain detailed clinical information on the prevalence of psoriatic arthritis and treatment patterns, which may vary based on psoriasis severity and duration, and may directly influence the patient’s ability to participate in physical activity.41–46

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Despite these limitations, the current study is arguably the first to quantify the association between the severity of psoriasis and physical activity. The main strengths of this study include using a nationally representative sample of men and women aged 20–59 years, a well-utilized measure for the severity of psoriasis, and comprehensive measures of the duration and intensity of MVPA, which includes a clinically relevant and standardized measure of MET-minutes. Further research may help develop effective interventions to improve physical activity and long-term clinical outcomes for patients with psoriasis.

ACKNOWLEDGMENTS: Mr Kelvin Foo at Duke-NUS provided help with statistical analysis. The authors acknowledge Dr John Murray at Duke for his helpful comments on an earlier draft of the paper. The authors wish to acknowledge the US National Center for Health Statistics for making the NHANES data available for public use. CONFLICT OF INTEREST:

None reported.

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39 Poole L, Steptoe A, Wawrzyniak AJ et al. Associations of objectively measured physical activity with daily mood ratings and psychophysiological stress responses in women. Psychophysiology 2011; 48: 1165–1172. 40 Azevedo Da Silva M, Singh-Manoux A, Brunner EJ et al. Bidirectional association between physical activity and symptoms of anxiety and depression: the Whitehall II study. Eur J Epidemiol 2012; 27: 537–546. 41 Su YS, Yu HS, Li WC et al. Psoriasis as initiator or amplifier of the systemic inflammatory march: impact on development of severe vascular events and implications for treatment strategy. J Eur Acad Dermatol Venereol 2013; 27: 876–883. 42 Hjortsberg C, Bergman A, Bjarnason A et al. Are treatment satisfaction, quality of life, and self-assessed disease severity relevant parameters for patient registries? Experiences from Finnish and Swedish patients with psoriasis. Acta Derm Venereol 2011; 91: 409–414.

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43 Kanelleas A, Liapi C, Katoulis A et al. The role of inflammatory markers in assessing disease severity and response to treatment in patients with psoriasis treated with etanercept. Clin Exp Dermatol 2011; 36: 845–850. 44 Palota T, Szepietowski JC, Pec J et al. A survey of disease severity, quality of life, and treatment patterns of biologically naive patients with psoriasis in central and eastern Europe. Acta Dermatovenerol Croat 2010; 18: 151–161. 45 Ragnarson Tennvall G, Hjortsberg C, Bjarnason A et al. Treatment patterns, treatment satisfaction, severity of disease problems, and quality of life in patients with psoriasis in three Nordic countries. Acta Derm Venereol 2013; 93: 442–445. 46 Root S, Kent G, al-Abadie MS. The relationship between disease severity, disability and psychological distress in patients undergoing PUVA treatment for psoriasis. Dermatology 1994; 189: 234–237.

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Association between psoriasis and leisure-time physical activity: findings from the National Health and Nutrition Examination Survey.

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