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DOI: 10.1111/jdv.12845

REVIEW ARTICLE

Sexual dysfunction in psoriasis: a systematic review nez-Moleo  n,2,3 R. Naranjo-Sintes,4 J.C. Ruiz-Carrascosa4 A. Molina-Leyva,1,* J.J. Jime dico-quiru rdenas, Almerıa, Spain rgica y Venereologıa, Hospital Torreca Servicio de Dermatologıa me n Biosanitaria ibs, GRANADA, Hospitales Universitarios de blica, Instituto de Investigacio Dpto de Medicina Preventiva y Salud Pu Granada/Universidad de Granada, Granada, Spain 3 blica (CIBERESP), Granada, Spain CIBER de Epidemiologıa y Salud Pu 4 dico-quiru rgica y Venereologıa, Hospital Universitario Granada, Granada, Spain Servicio de Dermatologıa me *Correspondence: A. Molina-Leyva. E-mail: [email protected] 1 2

Abstract Background Psoriasis has been associated with numerous psychological disorders such as low self-esteem, depression, anxiety, sexual dysfunction or suicidal ideation. Recently, there has been a progressive increase in studies examining the impact of psoriasis on sexual function. This alteration seems to be considerable and can cause significant changes in quality of life. Objective The aim of this study was to elaborate recommendations for psoriasis and sexual function supported by a systematic review, to facilitate the application of new scientific findings into clinical practice and to serve as a basis for conducting future research. Methods We performed a systematic review of the available studies on psoriasis and sexual dysfunction. Results Scientific evidence shows that psoriasis patients have a higher risk of sexual dysfunction as compared to the general population. The risk of erectile dysfunction is also higher in psoriasis patients. The risk factors associated with sexual dysfunction in psoriasis patients are disease severity, female gender, psoriatic arthritis and age. Keywords: physiological, psoriasis, psychological, sexual behaviour, sexual dysfunction, sexuality. Received: 26 April 2014; Accepted: 13 October 2014

Funding sources None declared.

Conflicts of interest None declared.

Background Psoriasis is a chronic inflammatory skin disease with an estimated prevalence of 1.5% to 2% of the population in industrialized countries.1 The impact on quality of life in patients with psoriasis is intense, comparable to that of cancer, heart disease or diabetes.2,3 Psoriasis has been associated with numerous psychological disorders such as low self-esteem, depression, anxiety, sexual dysfunction or suicidal ideation.4–6 According to the World Health Organization, sexual health is a state of physical, emotional, mental and social well-being in relation to sexuality; it is not merely the absence of disease, dysfunction or infirmity. Sexual health requires a positive and respectful approach to sexuality and sexual relationships, as well as the possibility of having pleasurable and safe sexual experiences, free of coercion, discrimination and violence. For sexual health to be attained and maintained, the sexual rights of all persons must be respected, protected and fulfilled.7 Recent years

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have seen an increase in studies examining the impact of psoriasis on sexual function, an alteration that can cause significant changes in quality of life.8–11 However, the scientific evidence to date regarding psoriasis and sexual dysfunction is heterogeneous in terms of design, objectives and results. The aim of this systematic review is to synthesize the available scientific evidence regarding psoriasis and sexual function to facilitate the application of new scientific findings into clinical practice, and to serve as a basis for conducting future research.

Material and methods In June 2014, we conducted a literature search of major biomedical databases including Pubmed, Scopus, EMBASE and Cochrane Library with the following search terms: ‘psoriasis’ AND (‘sexual dysfunction’ OR ‘sexual’). The search was limited to: (i) Human data; (ii) Articles written in English, German or Spanish language; and (iii) Articles published after the first year included

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on the searching databases. All types of epidemiological studies regarding sexual function in patients with psoriasis were included. Reviews and case reports were excluded. Two independent reviewers examined the title and abstract of the articles obtained in the first search to recognize relevant studies. Full texts of all studies meeting the inclusion criteria were reviewed, and their bibliographic references were checked for additional sources. The articles upon whose relevance both reviewers agreed were included in the analysis. The variables assessed were as follows: the type of study, sample size, instruments used, statistical analysis and results.

Results We identified 15 epidemiological studies regarding psoriasis and sexual dysfunction, summarized in Table 1.9–23 Most were cross-sectional and cross-sectional with two groups (psoriasis

and participants without psoriasis studies). The most frequently used assessment tools were the International Index of Erectile Function (IIEF), the Female Sexual Function Index (FSFI) and the 9th question of the Dermatology Quality of Life Index (DLQI) – ‘Over the last week, how much has your skin caused any sexual difficulties?’24–26 Of the 15 studies, 11 included patients with psoriasis having a range of severity from mild to severe, based on the Psoriasis Area and Severity Index (PASI), and four studies took in only patients with moderate to severe psoriasis. This fact should be underlined when comparing studies, as the PASI itself is a potential risk factor for sexual dysfunction (Table 1). Does psoriasis increase the risk of sexual dysfunction? We found three studies that addressed this question (Table 2).10,15,23 In all 15 studies, a higher frequency of sexual dysfunction was observed in patients with psoriasis. Chen et al. estimated that

Table 1 Characteristics of the studies related to sexual dysfunction and psoriasis Participants without psoriasis

Assessment tool

Main outcomes

120



Own

Sexual functioning psychological aspects

Moderate to severe

936



(SKINDEX, DLQI, PDI, IPSO) GHQ-12

Sexual functioning psychological aspects



Author

Year

Design

Psoriasis severity

Gupta

1997

Cross-sectional

Moderate to severe

Sampogna

2006

Cross-sectional

Patients

Al-Mazeedi

2006

Cross-sectional

Mild to severe

330

DQoLS

Sexual functioning

Turel Ermertcan

2006

C-S with two groups

Mild to severe

78

58

IIEF,FSFI DLQI HDRS

Sexual functioning quality of life Psychological aspects

Mercan

2008

C-S with two groups

Mild to severe

24

33

ASEX BDI

Sexual functioning depression

Meeuwis

2011

Cross-sectional

Mild to severe

487

IIEF, FSFI, SoQL-M, FSDS DLQI

Sexual functioning quality of life

Goulding

2011

C-S with two groups

Mild to severe

92

IIEF DLQI

Sexual functioning quality of life

Guenther

2011

RCT

Moderate to severe

1996



DLQI

Sexual functioning

Ruiz-Villaverde

2011

E. before–after

Moderate to severe

20



IIEF

Sexual functioning

Chen

2012

Cohorts

Mild to severe

12 300

61 500

ICD-9-CM

Sexual functioning

Chung

2012

Case–control

Mild to severe

4606

13 818

ICD-9-CM

Sexual functioning

Maaty

2013

C-S with two groups

Mild to severe

52

30

FSFI

Sexual functioning

Armstrong

2014

C-S with two groups

Mild to severe

170

6274

NHANES

Sexual behaviour

Armstrong

2014

C-S with two groups

Mild to severe

92

3370

NHANES

Sexual behaviour

Tasliyurt

2014

C-S with two groups

Mild to moderate

37

28

IIEF, BDI

Sexual functioning



130

ASEX, Arizona Sexual Experience Scale; BDI, Beck Depression Inventory; C-S with two groups, cross-sectional study with two groups (psoriasis and participants without psoriasis); DLQI, Dermatology Quality of Life Index; DQoLS, Dermatology Quality of Life Scale; FDFS, Female Sexual Distress Scale; FSFI, Female Sexual Function Index; GHQ-12, General Health Questionnaire; HDRS, Hamilton Depression Rate Scale; ICD-9-CM, International Classification of Diseases, Ninth Revision, Clinical Modification; IIEF, International Index of Erectile Function; IPSO, Impact of Psoriasis on Quality of Life Questionnaire; NHANES, National Health and Nutrition Examination Survey; PDI, Psoriasis Disability Index; RCT, Randomized Clinical Trial; SoQL-M, Sexual Quality of Life Questionnaire for Men.

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Table 2 Studies investigating link between psoriasis and sexual dysfunction Author

Risk factors

Effect parameter

P

Psoriasis (female)

24.09  5.53 vs. 28.12  3.48†

P < 0.01

Psoriasis (male)

54.27  13.07 vs. 61.69  9.49†

P < 0.05

Mercan

Psoriasis

16.9  7.13 vs. 13.97  3.94‡

P < 0.05

Chen*

Psoriasis

1.27 (1.11–1.46)§

P < 0.01

Psychiatric morbidities

1.83 (1.38–2.43)§

P < 0.01

Diabetes

1.21 (1.01–1.46)§

P = 0.04

Dyslipidaemia

1.35 (1.11–1.64)§

P < 0.01

Coronary vascular disease

1.62 (1.26–2.07)§

P < 0.01

Turel Ertmertcan

*Only men. †Mann–Whitney U-test with Bonferroni correction. Comparison of total mean score of the Female Sexual Function Index and the International Index of Erectile Function, respectively, psoriasis vs. participants without psoriasis. ‡One-way ANOVA comparison of total mean score of Arizona Sexual Experience Scale. §Cox proportional hazard regression analysis. Adjusted odds ratio of sexual dysfunction.

psoriasis per se increased the risk of sexual dysfunction in men with respect to the normal population [adjusted odds ratio (OR) 1.27 (95% CI: 1.11–1.46, P = 0.001)].23 A considerable number of studies analyse the risk factors for sexual dysfunction exclusively in the population of patients with psoriasis. We found seven studies exploring the factors associated with increased alterations in sexual function in psoriasis patients (Table 3).9,11,14,17–19 The estimated prevalence of sexual dysfunction in patients with psoriasis ranged from 22.6% to 71.3% depending on the characteristics of the sample and the assessment tool used.11,17 The factors associated with increased sexual dysfunction were as follows: psoriasis severity evaluated by PASI or Self-Administered PASI, the presence of lesions in the genital area, the presence of disturbances in mood status, especially depression, age, psoriatic arthritis and female gender (Table 3).27–33 There was no difference in sexual function with relation to psoriasis treatment modality. Altogether, five studies – two as the main objective, plus the aforementioned studies of Chen et al. and Ertmertcan Turel et al. as a secondary objective – analysed the risk of erectile dysfunction in patients with psoriasis (Table 4),10,12,13,23 the latter reporting no significant differences in IIEF outcomes in patients with psoriasis considering the diagnosis of depression as a stratification factor.10 However, the other four studies found an increased frequency of erectile dysfunction in patients with psoriasis.12,13,23 Regarding the causal role of psoriasis per se in the genesis of erectile dysfunction, the results are heterogeneous. Goulding et al. found no independent association between psoriasis and erectile dysfunction, whereas other organic factors such as hypertension and its treatment were secondary factors in this relationship. In contrast, Chung et al. arrived at an independent association between psoriasis per se and erectile dysfunction, OR: 3.85 (95% CI: 2.72–5.44; P < 0.001), and observed that other risk factors of sexual dysfunction (diabetes, hypertension) were more prevalent in patients with psoriasis; yet smoking, an important factor for erectile dysfunction, was not

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considered.34 Tasliyurt et al. observed an independent association between PASI score, age, depression and erectile dysfunction.22 Three studies evaluated the improvement of sexual function in psoriasis with therapy.11,16,17. Sampogna et al. reported that PASI 75 response is associated with a significant improvement of sexual function.17 Ruiz-Villaverde et al. obtained similar results at their 6-month follow-up of patients with biological treatment assessing PASI 75 response, as did Guenther et al. at 12 weeks in patients treated with placebo vs. ustekinumab.13,16 The results of these studies are consistent with the finding that psoriasis severity is correlated with sexual dysfunction.22 Armstrong et al. explored the sexual behaviour of men and women with psoriasis20,21 (Table 5). No differences in sexual orientation (heterosexual, not heterosexual) among men and women with psoriasis as compared with the general population were observed. Heterosexual men with psoriasis reportedly have an earlier age at their first sexual intercourse and fewer oral sex partners throughout life when compared to subjects without psoriasis OR 0.65 (0.45–0.95, P = 0.027).20 However, there were no statistically significant differences in the number of last-year or whole-life female partners or in the frequency of unprotected sex. Non-heterosexual men with psoriasis showed no differences compared to non-heterosexual men without psoriasis. With regard to women, non-heterosexual women with psoriasis had an earlier age of first sexual encounter and fewer female sex partners throughout life than non-heterosexual women without psoriasis. Heterosexual women with psoriasis had a higher frequency of unprotected sex (without a condom) than heterosexual women without psoriasis OR 1.14 (1.04–1.24, P = 0.003).21 In a study by Meeuwis et al., 43% of participants indicated that they would like more attention and direct questioning about sexual problems during medical consultations.9 Goulding et al., considering all the dermatology patients included in the study (with and without psoriasis), found that only 9% had been asked about erectile problems, whereas 68% of subjects were

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Table 3 Studies investigating risk factors of sexual dysfunction in patients with psoriasis Author

Risk factors

Effect parameter

Gupta

Joint pain

77% vs. 54%†

P = 0.01

Inguinal involvement

6.0  3.2 vs. 4.8  3.3‡

P = 0.07

Grade of desquamation

5.3  2.9 vs. 4.3  3.2‡

P = 0.06

Itch severity

5.9  2.6 vs. 2.6‡

P = 0.07

Depression

15.3  7.7 vs. 11.9  7.4§

P = 0.02

Alcohol abuse

41  63 vs. 20  64¶

P = 0.08

Psychological morbidities

7.4 (4.7-11.8)**

P < 0.05

SAPASI > 20

4.9 (2.3–10.5)**

P < 0.05

Female gender

1.8 (1.1–2.8)**

P < 0.05

Psoriasis arthritis

2.5 (1.0–6.8)**

P < 0.05

Meeuwis

Female genital psoriasis

16.1  12.1 vs. 10.1  9.7††

P = 0.01

Al-Maazedi

PASI

38.9% vs. 29.7% vs. 30.8%‡‡

P = 0.59

Guenther

Depression

41.7% vs. 14.7%§§



Anxiety

37.4% vs. 10.9%¶¶



PASI female

53.6% vs. 40.4% vs. 21.9%***



PASI male

30.0% vs. 28.4% vs. 16.0%***



Female gender

27.8% vs. 20.8%†††



Age 41–60 years

1.32 (1.09–1.61)‡‡‡

P < 0.01

Age > 60 years

1.42 (1.12–1.81)‡‡‡

P < 0.01

Psoriasis arthritis

1.78 (1.08–2.91)‡‡‡

P = 0.02

Sampogna

Chen

Maaty*

PASI Genital psoriasis Age

0.332§§§ 64.71% vs. 35.29%¶¶¶ 0.347§§§

P = 0.02 P = 0.03 P = 0.02

*Only women. †Chi-square test. Joint pain vs. no joint pain in patients with sexual dysfunction. ‡Two-sample t test. 10-point scale (0 = not at all, 9 = very severe), patients with sexual dysfunction vs. patients without sexual dysfunction. §Two-sample t test. Comparison of total mean scores of Carroll Rating Scale for Depression, patients with sexual dysfunction and patients without sexual dysfunction. ¶Two-sample t test. Comparison of average daily ethanol consumption (last 6 months) (grams) in patients with sexual dysfunction vs. patients without sexual dysfunction. **Logistic regression analysis of sexual dysfunction according to the quantitative results of Impact of Psoriasis on Quality of life Questionnaire. Adjusted odds ratio of sexual dysfunction. ††Independent Student’s t-test. Comparison of total mean score of the Female Sexual Function Index, patients with genital lesions vs. patients without genital lesions. ‡‡Chi-square test. Patients with severe psoriasis vs. moderate psoriasis vs. mild psoriasis and sexual dysfunction. §§Patients with depression vs. patients without depression and sexual dysfunction at baseline and at 12 weeks. ¶¶Patients with anxiety vs. patients without anxiety and sexual dysfunction at baseline and at 12 weeks. ***Patients with sexual dysfunction and PASI > 30 vs. PASI >20 ≤ 30 vs. PASI 10 ≤ 20. †††Female vs. male patients with sexual dysfunction. ‡‡‡Cox proportional hazard regression analysis. Adjusted odds ratio of sexual dysfunction. §§§Pearson/Spearman correlation. R values. Score of the Female Sexual Function Index. ¶¶¶Chi-square test. Patients with lesions and sexual dysfunction vs. patients without genital lesions and sexual dysfunction. PASI, Psoriasis Area and Severity Index; SAPASI, Self-Administered PASI.

dissatisfied with their erectile function and reported wanting more information on erectile dysfunction.13

Discussion Studies on the sexual problems of psoriasis patients are on the rise. Most studies rely on the DLQI to assess sexual function. While we believe that the DLQI may be a useful screening tool for sexual dysfunction in patients with psoriasis, as it is a widely implemented in routinely clinical practice,35 it was not designed for this purpose. Given its unidimensionality, it could overlook cases of sexual dysfunction that the patient does not consider to be directly related to psoriasis but rather to its comorbidities.36 The use of more specific tools, such as the IIEF and FSFI, provides much more reliable information, but they are time

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consuming and difficult to implement in routine clinical practice. Regarding to design, most of the available studies have a cross-sectional design with two groups (psoriasis and participants without psoriasis), not true case–control studies. Therefore, no causality hypothesis can be confirmed, because it is impossible to determine which variable is cause and which variable is effect. There is a need for prospective longitudinal studies to investigate causality. Diverse hypotheses attempt to explain sexual dysfunction in psoriasis patients. The greater frequency of sexual dysfunction in association with psoriasis may respond to different factors. On the one hand, psoriasis can cause an alteration in body image that could produce feelings of low self-esteem, stigmatization and decreased confidence; these could lead to sexual dysfunction,

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Sexual dysfunction in psoriasis

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– – – – Table based on the studies of Armstrong et al. *Multivariate analysis. RR, rate ratios.

0.46 (0.15–1.41) 0.65 (0.45–0.95) Number of lifetime female oral sexual partners

P < 0.05

P = 0.17

P < 0.01

P = 0.37 1.81 (0.49–6.71) P = 0.51 0.61 (0.14–2.69)

– –

0.11 (0.04–0.33) P = 0.53

P < 0.05

P P

Table 5 Sexual behaviour in psoriasis patients

just as genital involvement may be a direct impediment to sex.5,29,30,37,38 In addition, however, we must consider the accumulation of physical and psychological conditions associated with the sexual dysfunction in patients with psoriasis: diabetes, dyslipidaemia or depression could play an important role in this relationship.31,39–41 Recently, Tasliyurt et al. founded that depression is independently associated with erectile dysfunction in psoriasis patients. However, no study, to date, analyses the impact of anxiety on erectile dysfunction in psoriasis. This factor should be taken into account, given that erectile dysfunction may be triggered by psychological factors and that patients with psoriasis have an elevated prevalence of anxiety.40–42 Therefore, the increase in erectile dysfunction in association with psoriasis probably responds to a multifactorial mechanism.43 In short, both organic and psychological factors could play a causal role. For instance, hypertension and its treatment are very prevalent in psoriasis and well characterized causes of erectile dysfunction, along with other factors listed in Table 4.44 In relation to sexual behaviour, the most remarkable facts are the slight higher frequency of unprotected sex in heterosexual women with psoriasis and the earlier age of first sexual encounter in heterosexual men with psoriasis compared to individuals without psoriasis. Rieder et al. suggest the inclination of

Non-heterosexual men

*Organic erectile dysfunction. †Kruskal–Wallis and Mann–Whitney U-test with Bonferroni correction. Comparison of total mean scores of the International Index of Erectile Function, erectile function domain, participants with psoriasis vs. participants without psoriasis. ‡Multivariable regression analysis. Adjusted odds ratio of erectile dysfunction. §Chi-square test. Participants with psoriasis and erectile dysfunction vs. participants without psoriasis and erectile dysfunction. ¶Conditional logistic regression. Adjusted odds ratio of erectile dysfunction. **Pearson/Spearman correlation. R values. Score of the International Index of Erectile Function.

P = 0.41

P < 0.01

1.62 (0.53–4.95)

0.485**

P = 0.23

P < 0.01

Age

2.03 (0.63–6.49)

P < 0.01

0.654**

Number of lifetime male partners

0.422**

1.19 (0.69–2.06)

PASI Depression

1.13 (1.02–1.24)

P < 0.01

P = 0.09

P < 0.01

1.24 (1.13–1.35)¶

P = 0.18

2.96 (1.87–4.67)¶

Coronary vascular disease

1.41 (0.85–2.32)

Tasliyurt

Obesity

0.35 (0.10–1.21)

P = 0.03

0.56

1.54 (1.05–2.27)¶

P = 0.80

P < 0.01

Arterial hypertension

0.96 (0.85–1.09)

1.39 (1.27–1.51)¶

0.97 (0.79–1.21)

P < 0.01

Diabetes

Number of lifetime female partners

1.43 (1.31–1.55)¶

Frequency of unprotected sex/year

P < 0.01

Dyslipidaemia

RR*

P < 0.01

Difference 1.6 years

2.31% vs. 1.82%§ 3.85 (2.75–5.45)¶

P

Psoriasis Psoriasis

P = 0.16

Chen* Chung

RR*

P < 0.01 P < 0.01

Difference 0.5 years

1.32 (1.9–1.49)‡ 2.93 (1.41–6.37)‡

P

Age (per 5 years) Arterial hypertension

P = 0.69

Goulding

RR*

P = 0.10

Difference 1.1 years

23.05  5.80 vs. 25.66  4.68†

P < 0.01

Psoriasis

Difference 0.9 years

Mercan

RR*

P

Age first had sex

Effect parameter

Heterosexual women

Risk factors

Heterosexual men

Author

Non-heterosexual women

Table 4 Studies investigating link between psoriasis and erectile dysfunction

P < 0.01

5

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psoriasis patients to self-destructive behaviours, such as eating disorders or suicidal ideation, could explain this finding by extension.5 The lowered self-esteem observed in psoriasis patients could also justify this finding, since lowered self-esteem has been associated with a higher risk of unprotected sex and earlier age of first sexual intercourse among teenagers.4–6,45,46. Beyond these hypotheses, the take-to-home message is clear; sexual education, focusing on contraception history and safe sex, should be reinforced in young psoriasis patients. Studies in sexual behaviour in psoriasis are scarce; more studies focusing in young patients and sexual risk behaviours are needed. The dermatologist is the axis of the medical care of psoriasis patients, especially those with more severe conditions. Available studies underline the central role that the dermatologist might play to improve the sexual function of patients with psoriasis by improving the skin symptoms. Therefore, the presence of sexual dysfunction could be considered a criterion of severity in psoriasis when choosing a treatment, similar to the presence of psoriasis lesions on visible areas or when there is a considerable impact on quality of life (DLQI > 10).47 Furthermore, the dermatologist could facilitate communication regarding sexual problems, speeding therapy by identifying the aetiology of the problem and referring the patient to the proper specialist. Nowadays, although it is still not possible to achieve a PASI 0 in all patients, we can try to improve their quality of life, adopting a holistic approach to the patient with psoriasis to reach this goal.

Conclusion In conclusion, patients with psoriasis are found to have an increased risk of impaired sexual function, including alterations of the erectile function in men. The main factors associated with sexual dysfunction are female gender, age, psoriasis severity, involvement of genitalia, psoriasis arthritis and mood status alterations. The role of physical comorbidities, including metabolic syndrome, remains controversial. While treatment is not associated with sexual dysfunction, improvement of the psoriasis due to treatment is followed by an improvement of the sexual function. Young psoriasis patients have a higher risk of unprotected sex and earlier age of first sexual intercourse; sexual education should be reinforced among them. Psoriasis patients wish to be asked about their sexual life, and involvement on the part of the dermatologist is essential to enhance the quality of life of patients with psoriasis – including a better sex life. More prospective longitudinal studies are needed to explore the causal factors involved in sexual dysfunction among psoriasis patients.

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Sexual dysfunction in psoriasis

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© 2014 European Academy of Dermatology and Venereology

Sexual dysfunction in psoriasis: a systematic review.

Psoriasis has been associated with numerous psychological disorders such as low self-esteem, depression, anxiety, sexual dysfunction or suicidal ideat...
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