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JEADV (2004) 18 , 27–36

ORIGINAL ARTICLE

ORIGINAL ARTICLE

Self-reported stress reactivity and psoriasis-related stress of Nordic psoriasis sufferers

R Zachariae,†* H Zachariae,‡ K Blomqvist,§ S Davidsson,¶ L Molin,†† C Mørk,‡‡ B Sigurgeirsson§§ Psychooncology Research Unit, Aarhus University Hospital, Denmark, Department of Dermatology, Aarhus University Hospital, Denmark, § Department of Dermatology, Helsinki University Hospital, Finland, Department of Dermatology, University Hospital Reykjavik, Iceland, †† Department of Dermatology, Örebro Medical Centre Hospital, Sweden, ‡‡ Department of Dermatology, Rikshospitalet University Hospital, Oslo, Norway, §§ Department of Dermatology, University of Iceland, Reykjavik, Iceland (representing the Faroe Islands). * Corresponding author, Psychooncology Research Unit, Aarhus University Hospital, Barthsgade 5,3, 8200 Århus N, Denmark, Tel. +45 89 49 36 55; Fax +45 89 49 36 60; E-mail: bzach@akh.aaa.dk

Blackwell Publishing Ltd.

ABSTRACT

Objectives The purpose of the study was to investigate the perceived influence of stress on psoriasis onset and disease severity in a large sample of psoriatics and to compare stress reactors and non-reactors with respect to psoriasis-related stress, disease severity, family history of psoriasis and sociodemographic factors. Patients/methods A total of 5795 members of the Nordic psoriasis associations and 702 patients recruited from Nordic dermatologists or university clinics were asked whether their first outbreak of psoriasis occurred during times of worry and stress. They were also asked to rate the degree to which their psoriasis was influenced by stress and to complete the Psoriasis Life Stress Index, the Psoriasis Disability Index and a number of additional questions concerning sociodemographic factors. Results Seventy-one per cent of the members and 66% of the patients reported that their psoriasis was exacerbated by stress, and 35% in both groups reported that the onset of their psoriasis occurred during a time of worry and stress. Stress reactors, scoring above the median on stress reactivity, reported greater dis- ease severity, psoriasis-related stress and impairment of disease-related quality of life. They also reported more frequent use of tobacco, tranquillizers and antidepressants. More women than men were stress reactors, and stress reactors were more likely to have a family history of psoriasis. Conclusion Our findings confirm and extend the results of previous studies and indicate that a subgroup of psoriatics may be more psychologically reactive to their disease and its influence on everyday life. Whether this group is also physiologically more reactive to psychosocial stress remains to be investigated.

Key words: family history, psoriasis, quality of life, stress

Received: 12 June 2002, accepted 5 September 2002

Introduction

Psoriasis is a multifactorial disorder with a genetic component that requires additional factors, 1 possibly including psycho- social factors, to be manifested as lesional psoriasis. While a disfiguring disease like psoriasis may serve as a stressor in itself and influence the social and psychological well-being of the patient, 2,3 stressful life events have been considered possible aetiological factors influencing the onset of psoriasis. It has also been suggested that periods with increased disease activity may be preceded by increased distress. 4

© 2004 European Academy of Dermatology and Venereology

Several avenues of research have been pursued. Some researchers have attempted to measure the extent of stressful life events and correlated the results with outbreaks and/or severity of psoriasis symptoms, and results of uncontrolled investiga- tions indicate that distress or stressful events may have an im- pact on psoriasis. Hellgren 5 reported that 53% of 163 patients found that their psoriasis appeared after stressful life situations, and two studies of 100 and 179 psoriatics by Polenghi et al . 6,7 revealed that approximately 70% of the patients reported that they had experienced a stressful event about 1 month before the onset of the disease. Others have studied the possible effect of

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stressful life events on symptom severity. The results so far are conflicting. Baughman and Sobel 8 found significant cor- relations between life event scores and self-reported psoriasis severity in 252 patients during the previous 5 years, while Poikolainen et al . 9 did not find an association between life events and severity in a group of 55 patients. A number of controlled investigations comparing stress of psoriatics with healthy con- trols or other patient groups have also found associations between stress and psoriasis. Seville 10 compared 132 psoriasis patients with 73 patients with skin tumours and 132 patients recruited from general practice. While 39% of the psoriatics recalled stressful life events within 1 month before the onset of psoriasis, the percentages for the other two groups were only 5% and 10%. Fava et al . 11 found that 89% of 20 psoriatics reported a stressful event before disease onset, compared with only 50% of 20 patients with fungal infections. Similar results have been found in other controlled studies. 12,13,14,15 Not all studies have yielded positive results. Thus Payne et al . 16 were unable to find any association between stress and psoriasis in a study of 16 psoriatics and 16 controls, a result which could be due to the small sample size. The majority of studies have relied on retrospective measures

of stress, and only few prospective studies have been conducted.

A time series analysis of stress and disease severity measures

reported by four psoriasis patients once a week over a 20-week period revealed a modest, but significant, positive association between psoriasis symptom severity and psychological distress. 17

Another recent study of 69 psoriasis patients 18 showed that emotional expression, active coping and seeking social sup- port – all factors found to buffer stress 19 – were associated with improved mental and physical health 1 year later. That stress may play a role in the exacerbation of psoriasis has also received indirect support from both case studies and controlled investigations, indicating that psychological intervention techniques may be effective in reducing psoriasis symptoms. Hypnotherapy, imagery, relaxation and stress management have thus been reported to help patients suffering from

psoriasis. 20,21,22,23,24

Other investigators have studied the role of stress in onset or relapse of psoriasis using questionnaire surveys of larger sam- ples of patients. In an early questionnaire survey of 2144 psori- atics in the USA, Farber et al . 25,26 found that 40% reported that their psoriasis appeared at times characterized by ‘worry’ and that 37% reported ‘worsening’ of their psoriasis at such times. In a continuation of this survey including a total of 5600 patients, approximately 33% stated that new patches of psori- asis appeared at times of worry, 33% said that they did not, and the remaining 33% were uncertain. Subsequent studies with small samples have confirmed that a substantial number of psoriatics believe their disease to be influenced by stress 27,28,29 and a recent review of the literature indicates that the proportion

of

patients believing that stress plays a role in the onset or acts

as

an exacerbating factor in psoriasis ranges from 37% to 78%. 4

In spite of the relatively large body of literature, only few investigators have attempted to differentiate stress reactors from non-reactors. When comparing 64 psoriasis in-patients characterized as high stress reactors to 63 patients who reported no significant association between stress and their psoriasis,

Gupta et al . 30 found that stress reactors had more severe psori- asis, reported more flare-ups during the 6 months prior to admission, and experienced more psoriasis-related stress as measured on the Psoriasis Life Stress Inventory (PLSI). While Gupta et al . thus found a positive association between stress reactivity and disease severity, others have found that the beliefs held by psoriasis patients were unrelated to clinical disease severity. One would perhaps expect that psoriasis more clearly associated with a genetic component, e.g. as expressed in the presence of a family history of psoriasis, would be perceived by the patients as being less associated with stress than psoriasis in the absence of a family history. The results from the available studies, however, are inconsistent. In one study, perceived stress reactivity was found to be independent of the presence or absence of a family history of psoriasis. In contrast, the results

of another study indicate an association of both stressful life

events and the presence of a family history with guttate psoriasis – a form associated with streptococcal pharyngitis. Ta ke n together, a substantial proportion of psoriasis patients report the onset of their disease to be preceded by stressful events or to take place during times of ‘worry’ and that stress exacerbates their psoriasis. Most studies are based on relatively small clinical samples, and the only large survey of US psori- atics, which was conducted more than 30 years ago, was limited

to few questions concerning stress. The purpose of the present

study was therefore to investigate the perceived influence of stress on psoriasis onset and disease activity in a large sample of psoriatics recruited from several countries and to compare their reports with those of patients recruited from dermatologists or university clinics. Furthermore, we wished to compare stress reactors and non-reactors with respect to several factors,

including psoriasis-related stress, disease severity, family his- tory of psoriasis and sociodemographic factors. The particip- ants in the study took part in a questionnaire-based study of psoriasis-related quality of life (QoL) of members of the Nordic psoriasis associations and psoriasis patients recruited from dermatologists or university clinics. The results of this survey concerning QoL have been published elsewhere 31 .

Materials and methods

Patients

A questionnaire package was mailed to randomly selected

members of the psoriasis associations from Denmark, Finland,

Norway and Sweden and to all members of the associations from Iceland and the Faroe Islands. The numbers were 4000 from Sweden, 2000 from each of the three countries Denmark,

© 2004 European Academy of Dermatology and Venereology JEADV (2004) 18 , 27–36

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Norway and Finland, 1127 from Iceland and 173 from the Faroe Islands. The responders were 1356 (67.8%) from Denmark,

1125 (56.3%) from Finland, 451 (40.0%) from Iceland, 903

(45.2%) from Norway, 1828 (45.7%) from Sweden and 76 (44.0%) from the Faroe Islands, yielding a total of 5739 psoria- tics. Dermatologists from all Nordic countries were invited to

participate with up to five consecutive patients each, as was each university dermatology clinic with 10 consecutive psoriatic patients from their outpatient clinics and 10 from the wards.

A total of 387 patients recruited by dermatologists and 385

patients recruited at the dermatology departments completed the questionnaires. To control for possible seasonal variation, an additional 800 questionnaires were mailed out 6 months later to randomly selected members of the Danish, Norwegian, Swedish and Finnish psoriasis associations. A total of 341

(42.6%) psoriatics returned the questionnaires. The total number

of psoriatics who had completed the questionnaire package was

6849 and the average response rate for the total member sample

was 50.2%. Patients were excluded if they were under 18 years

old, and only patients who had their diagnosis of psoriasis made

or confirmed by a dermatologist were included in the study, resulting in a total sample of 6497 subjects.

Questionnaires

All subjects received a questionnaire package, which included questions regarding their perception of the influence of stress on psoriasis, perceived psoriasis severity and family history of psoriasis. The subjects also completed the Psoriasis Disability Index (PDI) 32,33 and the PLSI. 34

Perceived influence of stress on psoriasis

The subjects were asked to indicate: (1) Does your psoriasis have a tendency to break out during times of worry and stress?; (2) Does your psoriasis become worse during times of worry and stress?; (3) Did you experience your first outbreak of psoriasis during a period of worry and stress? The response format was ‘yes’, ‘no’ or ‘not sure’. The subjects were also asked to rate the influence of stress on their psoriasis on an 11-point scale with end-points representing ‘not at all’ and ‘to a very high degree’.

Psoriasis severity

The respondents were asked to indicate which parts of their body were afflicted and to rate their subjective experience of psoriasis severity, including the degree of erythema, scaling, plaque thickness and itch as well as their general assessment of severity on 11-point scales with end-points representing ‘not at all’ and ‘to a very high degree’. They were also asked to rate the area of their psoriasis on a scale from 0% to 100%. For the 695 psoriatics recruited at dermatology departments and by der- matologists, disease severity was also assessed by dermatologists

using the Psoriasis Area and Severity Index (PASI) scoring system 35 , where the area involved together with severity of erythema, infiltration and desquamation are graded, resulting in a range of total scores from 0 to 72. A detailed PASI instruction booklet had been mailed out to all dermatologists to increase the comparability of the PASI scores across countries, clinics and departments. A principal components analysis with varimax rotation was conducted for erythema, scaling, plaque thickness, itch and afflicted area. All variables loaded on one factor with factor loadings ranging from 0.90 (scaling) to 0.65 (area). A continuous total severity scale was therefore computed as the sum of the first four variables (scoring ranges 0–10) plus the area (0–100) divided by 5. Total severity is presented as percentage scores. This total severity scale was significantly correlated with both self-reported severity (Spearman’s R = 0.85; P < 0.01) and total PASI scores (Pearson’s R = 0.40; P < 0.01).

Family history of psoriasis

The subjects were asked whether their father, mother or siblings had psoriasis. The response format was ‘yes’, ‘no’ or ‘not sure’. A family history of psoriasis score of 0–3 was computed, with 0 representing no relatives with psoriasis and 3 indicating that father, mother and one or more siblings had psoriasis.

The PDI

The PDI consists of 15 disease-specific items with the total score reflecting the impact psoriasis has had on the daily life and activities of the respondent over the previous month. The PDI had been translated into the Nordic languages using the translation- back translation method 36 and validated in a preliminary sample. Total scores and score distributions of the individual items were similar and internal consistencies were found acceptable with internal reliability coefficients (Cronbach’s α ) ranging from 0.80 (Iceland) to 0.92 (Sweden). The total score is calculated as a percentage score (0% 100%).

The PLSI

In contrast to the PDI, which measures the impact of psoriasis on specific aspects of daily living, the PLSI measures the degree of subjective stress related to psoriasis experienced by the respondent within the last month. The PLSI consists of 15 items, covering different aspects of psoriasis-related stress. Two scores are computed. The PLSI-A score reflects the number of items experienced by the respondent during the last month, while the PLSI-B score reflects the degree of stress experienced by the respondent for each of these items as rated on four-point Likert scales. The PLSI was translated into the Nordic languages and tested in a preliminary sample using the same procedure as described for the PDI. As for the PDI, total scores and score distributions of the individual items were similar and internal

© 2004 European Academy of Dermatology and Venereology JEADV (2004) 18 , 27–36

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Zachariae et al.

consistencies were found acceptable with reliability coefficients (Cronbach’s α ) ranging from 0.77 (Iceland) to 0.88 (Norway). Total PLSI-A scores range from 0 to 15, and total PLSI-B scores are presented as percentage scores (0% 100%). When conducting a factor analysis of this measure, as previously done by Fortune and colleagues 37 , we found that the items loaded on two separate factors related to (1) stress resulting from anticipation of other people’s reactions leading to avoidance or worry (e.g. not going to a public place when you would have liked to) and (2) stress resulting from actual experiences of being evaluated by others on the basis of the skin condition (e.g. people making a conscious effort not to touch you). Two sepa- rate subscales, PLSI-avoidance and PLSI-experience, were thus constructed by excluding items loading on more than one factor (i.e. with a difference between loadings less than 0.30). Total scores for both scales are presented as percentage scores.

Additional questions

In a question aimed at determining a ‘value’ that the respond- ents place on their skin condition 38 , the subjects were asked how much time they would be prepared to spend on treating the skin each day if there was a daily treatment which could clear their skin completely. The response categories were 5 min, 10 min, 30 min, 1 h, 2 h and 3 h. The remaining questions concerned diagnosed comorbidity of arthritis, marital status, educational status, employ- ment, use of tranquillizers, sleep medication, antidepressants, drinking and smoking habits, and use of alternative treatments.

Statistical analyses

Proportions and ordinal data were analysed with χ 2 tests and other non-parametric tests. Continuous data were analysed with t tests for independent samples and univariate and multiple factorial analyses of variance (ANOVA) with post hoc pairwise comparisons, controlled for multiple comparisons. Further analyses were conducted with multiple logistic regres- sion analyses. Due to the large sample, even small differences may reach statistical significance. To better compare differences between groups, standardized mean differences (Cohen’s d ) were calculated for a number of variables 39 . All significance levels reported are two-tailed.

Results

Demographic characteristics, disease severity and duration

No differences ( P = 0.17) in mean self-reported severity were found between members and the seasonal control group and the two groups were therefore pooled in subsequent analyses. Unless otherwise indicated, the analyses have been conducted on the total group of psoriasis association members (member

group) and the group of psoriasis patients recruited at dermatology departments and by practising dermatologists (patient group). While there were no differences in the propor- tions of men to women between the six countries, significant differences were found between countries for age, with Finnish members being significantly older than the Swedish members, who were significantly older than the members from the remaining four countries ( P < 0.05; Scheffe post hoc multiple comparison tests). A multiple analysis of variance (MANOVA) revealed significant differences between countries for both total self-reported severity and duration, but not for afflicted area. Members had longer disease duration than the patient sample, and patients had greater severity scores and greater afflicted area than members (results of the statistical analysis not shown). The results are shown in Table 1. There were no differences between countries in PASI total scores and scores for head, trunk and upper and lower limb, and no differences between the three groups in the proportion of members (30%) or patients (30%) who had been diagnosed with arthritis (data not shown).

Perceived influence of stress

Compared to the remaining five countries, more Finnish and fewer Danish and Swedish members reported that their psoriasis had a tendency to break out during times of worry and stress (0.001 < P < 0.05). More Finnish and Norwegian members and fewer Danish and Swedish members reported that their psoriasis worsened during times of worry and stress (0.0001 < P < 0.05). More Finnish and fewer Icelandic and Faroe Island members reported that they had their first outbreak of psoriasis during a time of worry and stress (0.0001 < P < 0.05) than for the remaining countries. Norwegian members rated the influence of stress on an 11-point scale significantly higher than Swedish members ( P < 0.05; Scheffe test). When comparing patients, differences between countries did not reach statistical significance for any of the four stress reactivity measures. The results are shown in Table 1. Significantly more members reported that their psoriasis had a tendency to break out (68.7%) and worsen (70.7%) during stress than patients (63.1% and 66.1%). More patients (24.2% and 21.8%) reported that they were ‘not sure’ than members (17.2% and 16.8%) for these two items. No differences were found between members and patients for the remaining two items on the influence of stress on psoriasis. χ 2 tests showed that more participants with longer disease duration (median 27 years) were ‘unsure’ (57%) or responded ‘no’ (53%) to the question ( P < 0.001). On the other hand, fewer older participants (median 52 years) were ‘unsure’ (48%) or responded ‘no’ (43%).

Comparing stress reactors and non-reactors

Based on the degree (score 0–11) to which they believed stress to influence their psoriasis, the subjects were grouped into stress

© 2004 European Academy of Dermatology and Venereology JEADV (2004) 18 , 27–36

Psoriasis-related stress

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Influence of stress, 0–10

5.5 (2.8)

5.4 (3.2)

4.2 (3.5)

5.4 (3.0)

5.2 (3.2)

6.0 (3.0)

5.7 (2.9)

5.9 (2.9)

5.2 (3.0)

5.2 (3.1)

5.4 (3.1)

4.9 (3.1)

5.1 (3.5)

5.5 (3.1)

Table 1 Mean (SD) disease severity scores, disease duration and reported influence of stress on psoriasis of Nordic psoriasis association members and patients recruited by dermatologists

First outbreak during stress?, Yes/No (%)

33/26

36/26

35/26

24/38

32/27

38/22

36/33

35/25

35/25

35/25

34/21

25/16

21/26

44/17

Worse during stress?, Yes/No (%)

63/00

63/40

66/07

74/10

75/10

71/09

66/12

67/13

68/13

52/13

69/15

76/11

71/13

61/13

Outbreak during stress?, Yes/No (%)

66/07

70/09

52/22

69/14

60/16

65/16

64/10

67/17

72/13

63/13

68/13

63/11

71/13

61/13

10.50 (10.19)

9.34 (8.20)

7.56 (4.96)

7.52 (4.97)

9.20 (6.43)

9.21 (8.27)

9.31 (8.72)

PASI, 0–72

Duration, years

33.9 (12.5)

25.8 (15.8)

29.6 (15.4)

25.8 (15.6)

28.9 (14.9)

27.7 (14.3)

26.0 (13.7)

24.4 (16.0)

21.2 (14.9)

21.2 (15.2)

20.1 (13.8)

21.0 (15.2)

17.8 (11.7)

17.5 (11.8)

Total severity, %

Patients recruited by dermatologists and departments

48.3 (20.2)

48.0 (20.4)

36.1 (20.0)

41.8 (20.7)

39.2 (18.8)

39.1 (20.0)

44.8 (18.9)

49.7 (14.3)

46.3 (21.2)

46.4 (21.2)

40.5 (19.0)

36.7 (19.1)

35.1 (19.7)

53.2 (18.1)

Area, %

24 (23)

23 (23)

34 (27)

26 (24)

23 (22)

26 (23)

37 (23)

34 (29)

36 (26)

32 (26)

25 (24)

36 (27)

19 (20)

21 (21)

Psoriasis association members

219

1422

19

960

398

68

702

165

1811

23

115

164

1136

N

Denmark (DE) Faroe Is. (FA) Finland (FI) Iceland (IC) Norway (NO) Sweden (SW) Total

Denmark (DE) Faroe Is. (FA) Finland (FI) Iceland (IC) Norway (NO) Sweden (SW) Total

reactors, defined as subjects scoring above the median (score 6), and non-reactors (score < 6). Compared to the remaining five countries, more Finnish and Norwegian and fewer Swedish subjects were characterized as stress reactors ( P < 0.05) (data not shown). There was no difference in the proportion of stress reactors and non-reactors between the member and patient samples. Comparisons corrected for multiple comparisons between the two groups are shown in Table 2. Stress reactors also reported significantly greater use of alternative medicine, other alternative treatments and dietary measures both within the last week and previously than non-reactors (data not shown). More women than men used antidepressants ( P < 0.01). We therefore conducted a logistic regression analysis with stress reactivity entered as the dependent variable, and sex and use of antidepressants entered as independent variables at the first and second step. Being female was a significant predictor ( B , 0.20; P < 0.001; odds ratio, 0.81) and continued to be so when con- trolling for use of antidepressants ( B , 0.20; P < 0.001; odds ratio, 0.82), although use of antidepressants also was signific- antly related to stress reactivity ( B , 0.52; P < 0.001; odds ratio, 1.68). There were no differences in the percentage of stress reac- tors or the reported use of antidepressants between the seasonal control and the main sample. A hierarchical, logistic regression analysis was conducted with stress reactors versus non-reactors as the dependent variable and sex, age, family history of psoriasis, educational background and country recoded as dummy variables, and total self-reported disease severity and disease duration entered as predictors at each step. As seen in Table 3, the final model showed that being characterized as a stress reactor was significantly associated with being female, younger age, having a family history of psoriasis, higher educational level, belonging to the Finnish sample versus belonging to the other country samples, and having higher self- reported disease severity. Self-reported disease severity and age contributed more to the variability in stress reactivity than the remaining predictors, which were only very modest predictors of stress reactivity. To analyse stress reactivity as a predictor of psoriasis QoL, a multiple linear hierarchical regression was con- ducted with PDI scores as the dependent variable, stress reac- tivity entered at the first step, and age, sex, education, disease severity and duration entered as a block at the second step. When entered alone, stress reactivity was a significant predictor of PDI scores ( β = 0.24; P < 0.001; R 2 = 0.06). When controlling for the remaining factors previously shown to influence QoL, stress reactivity continued to be a significant predictor ( β = 0.11; P < 0.001). Age, education, severity and duration were also significant predictors ( P < 0.05–0.001), explaining an addi- tional 28% of the variation.

Visibility and severity

The number of visible areas (head, face, hands, nails) and non- visible areas (trunk, arms, legs) were computed and correlated

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Table 2 Demographic characteristics, disease severity, quality of life, psoriasis-related stress, number of cigarettes, alcohol consumption, and medication use of psoriasis sufferers characterized as stress reactors and non-reactors

Variable

Stress reactors

Non-reactors

P <<<<

P <<<< 0.01

Effect size, Cohen’s d b

Sex (per cent women) Age (mean (SD)) First outbreak during stress (per cent yes) Family history of psoriasis (mean number of relatives) Arthritis diagnosis (per cent yes) Educational background (high) Married/living with a partner (per cent yes) Total self-reported disease severity (mean per cent score (SD)) PASI score (mean score (SD)) Disease duration (mean number of years (SD)) PDI (mean per cent score (SD)) PLSI-A (mean score (SD)) PLSI-B (mean score (SD)) PLSI anticipationavoidance behaviours (mean count (SD)) PLSI actual experience (mean count (SD)) PLSI anticipationavoidance related stress (mean (SD)) PLSI actual experience related stress (mean (SD)) Time willing to spend on treatment (min/day) (mean (SD)) Cigarettes per day (mean (SD)) Glasses of wine per week (mean (SD)) Number of beers per week (mean (SD)) Liquor (2 cL) per week (mean (SD)) Total alcohol consumption per week (mean (SD)) Use of tranquillizers (per cent yes) Use of sleep medication (per cent yes) Use of antidepressants (per cent yes)

 

56.4%

51.3%

0.0001

a

0.11

49.2 (13.2)

53.7 (14.6)

0.0001

a

0.32

47.2%

23.9%

0.0001

a

0.58

0.70

0.63

0.0001

a

0.11

31.7%

28.7%

0.01

NS

0.08

46.3%

41.5%

0.0001

a

0.11

50.2%

49.8%

NS

NS

0.01

44.4 (19.7)

35.8 (19.7)

0.0001

a

0.44

9.9 (8.5)

8.5 (7.8)

0.05

NS

0.17

26.9 (14.3)

29.0 (15.4)

0.0001

a

0.14

15.8 (15.3)

10.1 (12.4)

0.0001

a

0.42

4.5 (3.4)

3.0 (3.0)

0.0001

a

0.47

17.0 (16.8)

9.7 (12.8)

0.0001

a

0.49

2.2 (2.0)

1.5 (1.8)

0.0001

a

0.37

0.9 (1.3)

0.5 (1.0)

0.0001

a

0.35

24.1 (24.4)

14.4 (19.5)

0.0001

a

0.44

7.0 (12.8)

3.2 (8.3)

0.0001

a

0.35

78.6 (57.4)

65.9 (53.8)

0.0001

a

0.23

5.0 (8.1)

4.3 (7.7)

0.0001

a

0.09

1.9 (3.6)

2.0 (3.8)

NS

NS

0.03

2.0 (4.5)

2.1 (4.6)

NS

NS

0.02

1.2 (3.5)

1.4 (4.2)

0.05

NS

0.05

5.1 (7.5)

5.4 (8.4)

NS

NS

0.04

10.6%

6.9%

0.0001

a

0.26

13.0%

11.7%

NS

NS

0.07

8.0%

4.8%

0.0001

a

0.30

a Corrected for multiple comparisons. b Effect size conventions: 0.2 (small); 0.5 (medium); 0.8 (large).

 

Independent variable

B

SE

Significance

Odds ratio

Table 3 Significant predictors of self-reported stress reactivity in a sample of 6497 Nordic psoriasis sufferers – results of a hierachical, logistic regression

Sex (male/female) Age (year) Family history of psoriasis (yes/no) Educational background (high/basic) Finnish nationality (Finland vs other countries) Self-reported severity (0%100%)

0.19

0.05

0.001

0.82

0.02

0.00

0.001

0.98

0.12

0.05

0.05

1.12

0.18

0.06

0.001

1.21

0.71

0.27

0.01

2.03

0.02

0.00

0.001

1.02

with the number of avoidance behaviours, actual experiences of being evaluated, and the reported distress associated with avoidance and experiences. Significant correlations (R = 0.15– 0.35; P < 0.0001) were found for numbers of both visible and non-visible areas. The correlation between number of visible areas and distress related to being evaluated (R = 0.21) was significantly greater (P < 0.001) than the correlation between number of non-visible areas and distress related to being evaluated (z = 3.14; R = 0.15). The correlations between distress related to avoidance behaviours and the number of visible (0.29) and non-visible (0.30) areas did not differ statistically (z = 1.02; P = 0.30). To assess whether stress reactivity was associated with certain aspects of psoriasis severity, the non-parametric correlations

between self-reported stress reactivity and the self-reported scores on the degree of itching, scaling, erythema, thickness of plaque (scores: 0–10) and afflicted body area in per cent were calculated. All aspects were positively correlated (P < 0.0001) with the degree of stress reactivity, with moderate to small cor- relations ranging from 0.22 (itching) to 0.20 (thickness of pla- que). The correlation with the calculated total severity scores was 0.25 (P < 0.0001).

Discussion

In the first survey of Farber et al. 25 , 37% of the participants reported that their psoriasis became worse during ‘times of worry’, while 22% answered that it did not. When asked

© 2004 European Academy of Dermatology and Venereology JEADV (2004) 18, 27–36

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whether worry was associated with the appearance of psoriasis, 40% responded that their psoriasis broke out during such times and 21% said that it did not. Of the total sample in our study, 71% of the psoriasis association members and 66% of the patients recruited by dermatologists or university clinics reported that their psoriasis worsened during ‘times of worry and stress’, and only 13% and 12% responded negatively. The percentages in our sample are considerably higher than the percentages found among US psoriatics in the late 1960s. Since it is not likely that the disease of psoriasis has become more susceptible to stress, this difference may be due to either cultural differences between the USA and the Nordic countries or – more likely – changes in illness perception of psoriasis patients. Today, psoriatics may have become more familiar with the concept of stress and the possible influence of psychological factors on physiological disease. The smaller number of pso- riatics, in comparison to the study by Farber et al., 25 answering that stress and worry did not affect their psoriasis only partially explains the difference, which is also due to fewer participants answering that they are unsure. When asked whether their first outbreak occurred during times of worry and stress, 35% of both members and patients responded affirmatively. This number is considerably smaller than the number of psoriatics responding that their psoriasis flare-ups were associated with stress. This could be due to diffi- culties remembering the time when their psoriasis first appeared. This was confirmed by our finding that psoriatics with longer disease duration were significantly more likely to be ‘unsure’ than psoriatics with shorter disease duration. Since younger psoriatics were more likely than older to disagree that their first outbreak occurred during times of worry and stress, this suggests that the question whether the first outbreak was associated with stress may be more subject to memory diffi- culties and memory bias than to generational differences, and illustrates the methodological difficulties associated with retro- spective studies 40 . It is also possible, however, that the more pos- itive answers to this question obtained from older participants are due to the increased tendency to respond in a socially desirable way among older subjects 41,42 . Although the differences found between the Nordic countries reached statistical significance due to the large sample, the differences were small, suggesting only moderate effects of cross-cultural differences. The percent- age responding ‘yes’ to whether their first outbreak of psoriasis was associated with stress is also considerably smaller than the 60% of the participants in the study of Fortune et al. 29 who responded that stress was the primary cause of psoriasis. Taken together with the small differences found between countries in our study, this illustrates that the way the questions are phrased is likely to influence the responses, and may explain the large differences found between studies. This is also illustrated by our finding that, although fewer patients (66%) than members (71%) reported that their psoriasis worsened during times of worry and stress, there were no differences between the two

groups in the mean perceived influence of stress (5.4) scored on an 11-point scale. When we divided the sample into stress reactors and non- reactors using the median split, the median found in our study (7) was comparable to the median (7) found previously by Gupta et al. 30 As seen in Table 2, stress reactors were found to differ significantly from non-reactors for several variables, even when controlled for multiple comparisons. First, stress reactors reported significantly greater total disease severity than non- reactors. The associations between self-reported severity and stress reactivity were similar for all aspects of severity, including itching, thickness of plaque, erythema, area etc. When we com- pared severity as rated by a dermatologist, i.e. PASI scores, of patient stress reactors and non-reactors, the small difference found did not reach statistical significance when controlling for multiple comparisons. As seen by the larger effect size found for self-reported severity (d = 0.44) compared to PASI scores (d = 0.17), this difference is not merely a result of the smaller number of patients compared to members. Our finding is in agreement with the results of Gupta et al. showing that stress reactors and non-reactors did not differ with respect to the usual dermatological criteria of psoriasis severity, e.g. percent- age of total body surface affected, thickness of plaque etc. Gupta et al., however, found that stress reactors did have greater psori- asis severity of ‘emotionally charged’ areas such as the scalp, face, neck, forearms, hands and genital region. Similarly, when we compared the number of affected visible and non-visible areas, the differences between stress reactors and non-reactors were larger for visible than for non-visible areas. Taken together, stress reactors had greater self-reported severity, especially more afflicted visible areas, than non-reactors, while the tradi- tional dermatologist-rated severity measures (PASI) were not associated with self-reported stress reactivity. Disease duration, on the other hand, was inversely associated with stress react- ivity. The difference between groups was small, however, as revealed by the very small correlation between stress reactiv- ity and duration (r = 0.07), a correlation which was further reduced when controlling for age (r = 0.03). When comparing the PLSI scores, we found that stress reactors reported significantly more psoriasis-related stressful experiences and rated these as more distressing than non- reactors. The association between distress and stress reactivity was diminished, however, when controlling for the number of actual experiences. Our findings are in concordance with the results of Gupta et al. 30 who found that stress reactors experi- enced more psoriasis-related stress. When we distinguished between PLSI items describing stress resulting from anticipa- tion of other people’s reactions leading to avoidance or worry (anticipationavoidance) and items concerning stress resulting from actual experiences of being evaluated by others on the basis of the skin condition (actual experiences), stress reactors exhibited higher scores than non-reactors on both subscales. The difference between the two groups, however, was somewhat

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higher for anticipationavoidance (Cohen’s d = 0.44) than for actual experiences (d = 0.35), suggesting that stress reactors may be especially likely to anticipate stressful experiences. This result should be seen in the light of previous findings that stress from anticipating other people’s reactions to their psoriasis contributed more to disability in everyday life than any other medical or health status variables investigated 37 . More women than men were characterized as stress reactors, which is in concordance with the findings of Farber et al. 25 that more women than men reported their psoriasis to be influ- enced by ‘worry’. We have no ready explanation for this gender difference. On the one hand, it is theoretically possible that women with psoriasis are physiologically more reactive to stress than men. On the other hand, it is also possible that women are more attentive towards psychological and bodily symptoms, including stress 43 . Since women also have a higher incidence of depression than men 44 , and since depression has been linked to somatization 45 , it is also possible that the higher proportion of stress reactors among women could be explained by a higher incidence of depression in this group. When we analysed the association between gender and stress reactivity while control- ling for the use of antidepressants, both factors independently of each other remained highly significant predictors. As many cases of depression remain undiagnosed and go untreated, self- reported use of antidepressants is, of course, only an indirect indicator of depression. It should be noted that, although the difference found between men and women is statistically signi- ficant due to the large sample in our study, the effect size was small (d = 0.11), which may explain why gender differences have generally not been found in previous studies. Stress reactors were younger than non-reactors with a mean age difference of 4.5 years. This could be due to a generational difference, and the contrast to the difference between older and younger participants noted above could reflect that stress reactivity scored on a scale from 0 to 10 is less susceptible to social desirability than a dichotomized question. That more self-reported stress reactors had a higher education than non- reactors could be due to higher education being associated with greater familiarity with the concept of stress and its potential influence in health and disease. A multiple logistic regression analysis revealed that, while controlling for the remaining factors, sex, age, family history of psoriasis, educational background and disease severity all continued to be significant predictors of stress reactivity. In addition, belonging to the Finnish sample was significantly associated with greater stress reactivity. Since we controlled for factors differing between countries, we have no clear explanation as to why Finnish psoriatics perceived themselves as more stress reactive. When comparing disability in everyday life associated with psoriasis as measured by the PDI, stress reactors showed con- siderably more impairment of QoL than non-reactors, a result supported by our findings of more frequent smoking and use of tranquillizers and antidepressants among stress reactors than

non-reactors. The same pattern emerged when indirectly assessing QoL using a utility measure of how much time the respondents were willing to spend daily on a hypothetical, effect- ive treatment. When controlling for other factors associated with both stress reactivity and QoL, including age, gender, edu- cation, disease severity and duration, stress reactivity continued to be a significant predictor of QoL, a finding which is in agree- ment with the results of a previous study 37 . A number of factors, including the presence of arthritis, marital status, and alcohol consumption, were not associated with stress reactivity. If stress reactivity is to be viewed purely as a subjective belief, unassociated with any physiological influence of stress on pso- riasis activity, one would expect that a family history of psoriasis would either be inversely associated with or unrelated to per- ceived stress reactivity. We did, however, find a small (Cohen’s d = 0.14), but significant, association between stress reactivity and the presence of a family history of psoriasis. This finding is in disagreement with the results of Fortune et al. 37 who found that patients with a family history of psoriasis were more likely to believe that their psoriasis was caused by genetic factors. Naldi et al., 15 on the other hand, found an association of stress- ful life events as well as the presence of a family history with guttate psoriasis. A family history of psoriasis, indicating the genetic influence on psoriasis, does not necessarily exclude the possibility that stress influences both onset and exacerbation of psoriasis. Social learning could be yet another possible explana- tion. Having family members with psoriasis may have ‘primed’ subjects to be subjectively more responsive to psoriasis-related stress. The hypothesis that psoriasis onset and severity may be influ- enced by psychosocial stress finds support from the results of several investigations showing that cutaneous immune and inflammatory processes are susceptible to stress 46,47 . The possible influence of stress on skin function has previously been demon- strated in studies showing that psychological stress influences epidermal permeability barrier homeostasis 48 and dermal flare activity 49 in healthy subjects, and that psoriatics show greater galvanic skin responses 6 as well as increased cathecholamine and growth hormone secretion during stress 50,51 . Ta ke n together, our results confirm and extend previous findings that a substantial number of psoriatics experience stress as influencing onset, flare-ups and exacerbation of pso- riasis. Our results also confirm that psoriatics characterized as high stress reactors report greater disease severity and psoriasis- re lated stress. We also found that more stress reactors than non- reactors reported a family history of psoriasis, and that a family history thus does not exclude perceived stress reactivity. As is the case with the large majority of the available studies, the cor- relational and retrospective nature of our measurements does not allow us to draw any conclusions regarding the causal rela- tionship between stress and psoriasis. Also, since the stress measures used were self-report measures, we are only measur- ing what the subjects are consciously aware of and willing to

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reveal. While the anonymity of the respondents may reduce the confounding influence of impression management 52 , the pos- sible role of defensiveness and self-deception cannot be ruled out. One approach in future surveys could be to include measures of defensiveness, e.g. the MarloweCrowne Social Desirability Scale 53 . Nonetheless, our results could indicate that some pso- riatics are psychologically more reactive and attentive to their disease, its symptoms and its consequences for their everyday life. Whether the skin of this subgroup of psoriatics is also particularly physiologically reactive to psychosocial stress remains to be investigated.

Acknowledgements

This study was initiated and supported by the Nordic Psoriasis Associations (NORDPSO) and a grant from Leo Pharmaceuti- cal Products Ltd, Ballerup, Denmark. The authors wish to thank all the members and the staff of the Nordic Psoriasis Associations, who either participated in or assisted practically in carrying out the survey, the members of the staff of Leo Phar- maceutical Products, who offered us practical support, and all departments and physicians engaged in the study. We in partic- ular thank Jan Monsbakken, NORDPSO, and Anette Heymann, Strategic Marketing, Leo Phamaceutical Products Ltd. We also thank Novartis Pharma AG for supplying the booklet Psoriasis Area and Severity Index (PASI) by M. Thompson and G. Feutren, Clinical Research Department, Sandoz Pharma Ltd, Basel, 1997, to all departments and physicians engaged in the study.

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