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Patients with Hidradenitis Suppurativa Have a High Psychiatric Disease Burden: A Finnish Nationwide Registry Study

  • Author Footnotes
    5 These authors contributed equally to this work.
    Laura Huilaja
    Footnotes
    5 These authors contributed equally to this work.
    Affiliations
    PEDEGO Research Unit, University of Oulu, Oulu, Finland

    Department of Dermatology and Medical Research Center Oulu, Oulu University Hospital, Oulu, Finland
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  • Author Footnotes
    5 These authors contributed equally to this work.
    Hannu Tiri
    Footnotes
    5 These authors contributed equally to this work.
    Affiliations
    PEDEGO Research Unit, University of Oulu, Oulu, Finland

    Department of Dermatology and Medical Research Center Oulu, Oulu University Hospital, Oulu, Finland
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  • Jari Jokelainen
    Affiliations
    Unit of General Practice, Oulu University Hospital, Oulu, Finland

    Center for Life Course Epidemiology and Systems Medicine, University of Oulu, Oulu, Finland
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  • Markku Timonen
    Affiliations
    Center for Life Course Epidemiology and Systems Medicine, University of Oulu, Oulu, Finland
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  • Kaisa Tasanen
    Correspondence
    Correspondence: Kaisa Tasanen, Department of Dermatology, Medical Research Center Oulu, University of Oulu, Aapistie 5A, FIN-90220 Oulu, Finland.
    Affiliations
    PEDEGO Research Unit, University of Oulu, Oulu, Finland

    Department of Dermatology and Medical Research Center Oulu, Oulu University Hospital, Oulu, Finland
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  • Author Footnotes
    5 These authors contributed equally to this work.
Open ArchivePublished:July 20, 2017DOI:https://doi.org/10.1016/j.jid.2017.06.020
      Hidradenitis suppurativa (HS) is a chronic inflammatory skin disease of hair follicles that is associated with various comorbidities. To further clarify the associations between HS and psychiatric disorders, we conducted a nationwide retrospective study that included 4,381 patients with HS, and 39,554 with psoriasis and 43,248 with melanocytic nevi as controls. Patient data were obtained from the statutory Finnish Care Register for Health Care. The incidence of HS was 3.0/100,000 persons/year. At least one psychiatric diagnosis was found in 24.1% of the patients with HS compared with 19.1% of the patients with psoriasis (odds ratio 1.34; 95% confidence interval 1.24–1.46) and 13.5% of those with melanocytic nevi (odds ratio 2.04; confidence interval 1.88–2.22). Every mental disorder examined was significantly more frequent in HS than in the two other groups. Mental disorders were more common in women than in men with HS and psoriasis. The main finding of our study is that patients with HS have a higher risk of mental disorders than patients with psoriasis. Additionally, this study reveals that HS is associated with both schizophrenia (odds ratio 1.57; confidence interval 1.24–1.98) and bipolar disorder (odds ratio 1.81; confidence interval 1.47–2.23), findings that to our knowledge have not been reported previously.

      Abbreviations:

      CI (confidence interval), HS (hidradenitis suppurativa), ICD (International Classification of Diseases), OR (odds ratio)

      Introduction

      Hidradenitis suppurativa (HS) is a chronic, recurrent inflammatory disease characterized by inflamed lesions in the apocrine gland-bearing areas of the skin, most commonly in the axillary, inguinal, and anogenital regions (
      • Revuz J.
      Hidradenitis suppurativa.
      ). Previously, HS was considered to be an orphan disease, but recent studies estimate its prevalence to be between 1% and 4% in Western countries (
      • Jemec G.B.
      • Kimball A.B.
      Hidradenitis suppurativa: epidemiology and scope of the problem.
      ). HS occurs more frequently in women than in men (
      • Alikhan A.
      • Lynch P.J.
      • Eisen D.B.
      Hidradenitis suppurativa: a comprehensive review.
      ) and has its peak prevalence among young adults (
      • Vinding G.R.
      • Miller I.M.
      • Zarchi K.
      • Ibler K.S.
      • Ellervik C.
      • Jemec G.B.
      The prevalence of inverse recurrent suppuration: a population-based study of possible hidradenitis suppurativa.
      ). The painful, suppurative, deep-seated, and scarring lesions characteristic of HS greatly diminish patients’ quality of life (
      • Gooderham M.
      • Papp K.
      The psychosocial impact of hidradenitis suppurativa.
      ,
      • Matusiak L.
      • Bieniek A.
      • Szepietowski J.C.
      Psychophysical aspects of hidradenitis suppurativa.
      ), and therefore HS is one of the most life-impacting skin disorders (
      • Wolkenstein P.
      • Loundou A.
      • Barrau K.
      • Auquier P.
      • Revuz J.
      Quality of Life Group of the French Society of Dermatology. Quality of life impairment in hidradenitis suppurativa: a study of 61 cases.
      ). HS has several known comorbidities (
      • Kohorst J.J.
      • Kimball A.B.
      • Davis M.D.
      Systemic associations of hidradenitis suppurativa.
      ).
      Dermatology patients have a higher prevalence of psychiatric disorders compared with the general population (
      • Dalgard F.J.
      • Gieler U.
      • Tomas-Aragones L.
      • Lien L.
      • Poot F.
      • Jemec G.B.
      • et al.
      The psychological burden of skin diseases: a cross-sectional multicenter study among dermatological out-patients in 13 European countries.
      ,
      • Hughes J.E.
      • Barraclough B.M.
      • Hamblin L.G.
      • White J.E.
      Psychiatric symptoms in dermatology patients.
      ). An Italian survey (
      • Picardi A.
      • Abeni D.
      • Melchi C.F.
      • Puddu P.
      • Pasquini P.
      Psychiatric morbidity in dermatological outpatients: an issue to be recognized.
      ) showed that as many as quarter of all dermatology patients have at least one psychiatric comorbidity, and even higher prevalence rates of psychiatric disorders have been found among patients with psoriasis, acne, and eczemas (
      • Picardi A.
      • Abeni D.
      • Melchi C.F.
      • Puddu P.
      • Pasquini P.
      Psychiatric morbidity in dermatological outpatients: an issue to be recognized.
      ). In a Norwegian study, the odds for anxiety and depression were threefold higher among patients with chronic, recurrent skin diseases compared with healthy controls, whereas in patients with skin tumors (e.g., benign or precancerous lesions, nonmelanoma skin cancer or malignant melanoma), there was no difference from healthy controls in the odds for depression (
      • Balieva F.
      • Lien L.
      • Kupfer J.
      • Halvorsen J.A.
      • Dalgard F.
      Are common skin diseases among Norwegian dermatological outpatients associated with psychological problems compared with controls? An observational study.
      ). In a recent European multicenter study, clinical anxiety was present in 17% and depression in 10% of the more than 3,500 dermatology patients studied (
      • Dalgard F.J.
      • Gieler U.
      • Tomas-Aragones L.
      • Lien L.
      • Poot F.
      • Jemec G.B.
      • et al.
      The psychological burden of skin diseases: a cross-sectional multicenter study among dermatological out-patients in 13 European countries.
      ).
      There is strong evidence that psychiatric comorbidities are more frequent in patients with psoriasis compared with the general population (
      • Kurd S.K.
      • Troxel A.B.
      • Crits-Christoph P.
      • Gelfand J.M.
      The risk of depression, anxiety, and suicidality in patients with psoriasis: a population-based cohort study.
      ). Similarly, psychiatric comorbidities are associated with HS (
      • Kohorst J.J.
      • Kimball A.B.
      • Davis M.D.
      Systemic associations of hidradenitis suppurativa.
      ). A case-control study, conducted in the USA, found that psychiatric disorders were the most common group of comorbidities in patients with HS, with 57% of 1,776 patients having at least one psychiatric disorder (
      • Shlyankevich J.
      • Chen A.J.
      • Kim G.E.
      • Kimball A.B.
      Hidradenitis suppurativa is a systemic disease with substantial comorbidity burden: a chart-verified case-control analysis.
      ). A recent registry study from Israel showed that depression and anxiety are more common among patients with HS (n = 3,207) than in the general population (
      • Shavit E.
      • Dreiher J.
      • Freud T.
      • Halevy S.
      • Vinker S.
      • Cohen A.D.
      Psychiatric comorbidities in 3207 patients with hidradenitis suppurativa.
      ). A population-based study from the USA found that almost 43% of patients with HS (n = 268) had a diagnosis of depression (
      • Vazquez B.G.
      • Alikhan A.
      • Weaver A.L.
      • Wetter D.A.
      • Davis M.D.
      Incidence of hidradenitis suppurativa and associated factors: a population-based study of Olmsted County, Minnesota.
      ). In contrast, a Danish-Dutch hospital-based study found no difference in the rate of depression between patients with HS and patients with other dermatological conditions, although quality of life and mood were significantly impaired in patients with HS (
      • Onderdijk A.J.
      • van der Zee H.H.
      • Esmann S.
      • Lophaven S.
      • Dufour D.N.
      • Jemec G.B.
      • et al.
      Depression in patients with hidradenitis suppurativa.
      ).
      To clarify the associations between HS and its psychiatric comorbidities at a national level, we conducted a retrospective study using the Finnish Care Register for Health Care. Patients with psoriasis were chosen as a control group because they have an elevated risk of psychological comorbidities (
      • Dalgard F.J.
      • Gieler U.
      • Tomas-Aragones L.
      • Lien L.
      • Poot F.
      • Jemec G.B.
      • et al.
      The psychological burden of skin diseases: a cross-sectional multicenter study among dermatological out-patients in 13 European countries.
      ), and proinflammatory cytokines play a major role in the pathogenesis of both psoriasis and HS (
      • Boyman O.
      • Hefti H.P.
      • Conrad C.
      • Nickoloff B.J.
      • Suter M.
      • Nestle F.O.
      Spontaneous development of psoriasis in a new animal model shows an essential role for resident T cells and tumor necrosis factor-alpha.
      ,
      • van der Zee H.H.
      • de Ruiter L.
      • van den Broecke D.G.
      • Dik W.A.
      • Laman J.D.
      • Prens E.P.
      Elevated levels of tumour necrosis factor (TNF)-alpha, interleukin (IL)-1beta and IL-10 in hidradenitis suppurativa skin: a rationale for targeting TNF-alpha and IL-1beta.
      ). Patients diagnosed to have melanocytic nevi, but not melanoma, were chosen as another control group. To the best of our knowledge, our HS cohort of 4,381 patients is one of the largest HS cohorts described to date, and the incidence of psychiatric comorbidities in patients with HS has not been previously compared with that in patients with psoriasis.

      Results

      Characteristics of patients with HS and controls

      The characteristics of the patients with HS and controls are summarized in Supplementary Table S1 online. The initial database query yielded records for 4,381 patients with HS, 39,554 with psoriasis, and 43,248 with melanocytic nevi and without melanoma. When HS and psoriasis patient groups were matched by age and sex in the ratio of 1:4, 36 patients with HS were left with no controls, leaving a matched analysis population that consisted of 4,337 patients in the HS group and 17,318 patients in the psoriasis group. Only 1.0% (n = 44) of the cases in the HS group had fewer than four patients with psoriasis as controls. When patients with HS and melanocytic nevi were correspondingly matched, there were 4,372 patients with HS and 17,488 cases with melanocytic nevi in the analysis. For HS, the age-adjusted incidence was 3.0/100,000 persons/year and for psoriasis 27.8/100,000 persons/year. HS was most commonly (26.1%) diagnosed in individuals aged between 30 and 39 years, whereas psoriasis was most frequently diagnosed in those older than 60 (28.8%).

      Psychiatric disorders of patients with HS, psoriasis, and melanocytic nevi

      The mental disorders studied (Supplementary Table S2 online) were clearly more common in patients with HS than in those with psoriasis or melanocytic nevi: at least one mental disorder was diagnosed in 24.1% of patients with HS compared with 19.1% of patients with psoriasis (odds ratio [OR] 1.34, 95% confidence interval [CI] 1.24–1.46) and 13.5% of patients with melanocytic nevi (OR 2.04, 95% CI 1.88–2.22; Table 1).
      Table 1Comorbidities in patients with HS (N = 4,337 for psoriasis and N = 4,372 for melanocytic nevi) versus matched psoriasis (N = 17,318) and melanocytic nevi (N = 17,488) controls
      ComorbiditiesGroupN (%)OR (95% CI)OR (95% CI)
      All psychiatric disordersHS1,044 (24.1)1.34 (1.24–1.46)2.04 (1.88–2.22)
      Psoriasis3,315 (19.1)Reference
      Nevi2,366 (13.5)Reference
      All psychotic disordersHS203 (4.7)1.46 (1.24–1.72)2.74 (2.29–3.28)
      Psoriasis566 (3.3)Reference
      Nevi304 (1.7)Reference
      Schizophrenia or schizotypal disorderHS103 (2.4)1.57 (1.24–1.98)3.38 (2.59–4.39)
      Psoriasis267 (1.5)Reference
      Nevi124 (0.7)Reference
      Bipolar disorder or manic episodesHS135 (3.1)1.81 (1.47–2.23)2.82 (2.25–3.52)
      Psoriasis301 (1.7)Reference
      Nevi196 (1.1)Reference
      Major depressionHS663 (15.3)1.31 (1.19–1.44)2.00 (1.81–2.22)
      Psoriasis2,099 (12.1)Reference
      Nevi1,462 (8.3)Reference
      Anxiety, dissociative, stress-related, somatoform, and other nonpsychotic mental disordersHS484 (11.2)1.30 (1.16–1.45)1.68 (1.50–1.88)
      Psoriasis1,529 (8.8)Reference
      Nevi1,231 (7.0)Reference
      Anxiety disordersHS301 (6.9)1.41 (1.23–1.62)1.90 (1.65–2.19)
      Psoriasis866 (5.0)Reference
      Nevi666 (3.8)Reference
      Disorders of adult personality and behaviorHS141 (3.3)1.41 (1.16–1.71)2.33 (1.88–2.87)
      Psoriasis404 (2.3)Reference
      Nevi248 (1.4)Reference
      Abbreviations: CI, confidence interval; HS, hidradenitis suppurativa; Nevi, melanocytic nevi; OR, odds ratio.
      Major depression was the most common mental disorder in all three groups. However, it was more common in the HS group than in the psoriasis group (15.3% vs. 12.1%, OR 1.31, 95% CI 1.19–1.44) and in the melanocytic nevi group (8.3%, OR 2.00, 95% CI 1.81–2.22). Anxiety disorders were diagnosed in 6.9% of patients with HS compared with 5.0% of patients with psoriasis (OR 1.41, 95% CI 1.23–1.62) and 3.8% of patients with melanocytic nevi (OR 1.90, 95% CI 1.65–2.19; Table 1).
      The total prevalence of psychotic disorders was 4.7% in the HS group compared with 3.3% in the psoriasis group (OR 1.46, 95% CI 1.24–1.72) and 1.7% in the melanocytic nevi group (OR 2.74, 95% CI 2.29–3.28). Specifically, “schizophrenia or schizotypal disorder” was more frequent in the HS group than in patients with psoriasis (2.4% vs. 1.5%, OR 1.57, 95% CI 1.24–1.98) or in patients with melanocytic nevi (2.4% vs.0.7%, OR 3.38, 95% CI 2.59–4.39; Table 1).
      “Disorders of adult personality and behavior” were more frequent in patients with HS than in patients with psoriasis (3.3% vs. 2.3%, OR 1.41, 95% CI 1.16–1.71) or in those with melanocytic nevi (3.3% vs. 1.4%, OR 2.33, 95% CI 1.88–2.87). The prevalence of “bipolar disorder or manic episodes” was 3.1% in the HS group compared with 1.7% in the psoriasis group (OR 1.81, 95% CI 1.47–2.23) and 1.1% in the melanocytic nevi group (OR 2.82, 95% CI 2.25–3.52; Table 1).

      Differences between genders

      Mental disorders were found more frequently in female (OR 1.28; 95% CI 1.15–1.41) than male (OR 1.46, 95% CI 1.28–1.66) patients with HS (25.5% and 22.0%, respectively); a similar pattern was found in patients with psoriasis (21.2% vs. 16.3%, respectively). All psychiatric disorders were more common in female than male patients with HS, with the exception of “schizophrenia or schizotypal disorder” (2.1% in women [OR 1.36, 95% CI 0.99–1.86] vs. 2.7% in men [OR 1.88, 95% CI 1.33–2.66]). In total, psychotic disorders were equally frequent in women and men (4.7% for each sex, OR 1.49, 95% CI 1.19–1.85 for women and OR 1.43, 95% CI 1.11–1.84 for men).
      In patients with psoriasis, all mental disorders were more frequent in women than men but “psychotic disorders,” “schizophrenia or schizotypal disorder,” and “bipolar disorder or manic episodes” were found in similar proportions in both sexes. Anxiety disorders were diagnosed in 7.5% of women with HS (OR 1.29, 95% CI 1.08–1.52) and in 6.2% of men with HS (OR 1.7, 95% CI 1.35–2.13), whereas in patients with psoriasis the prevalence rates were 5.9% and 3.8%, respectively.
      In the gender-stratified analysis, the association between HS and mental disorders was significantly stronger in men than in women (OR 1.46 in men vs. 1.28 in women, P = 0.02). A weaker gender pattern was seen in patients with psoriasis. When observing the mental disorders separately, the risk of anxiety disorders was significantly stronger in men than in women in the HS group (OR = 1.70 in men vs. 1.29 in women, P = 0.003). There was also a trend toward a stronger association between HS and “schizophrenia or schizotypal disorder” in men than in women (OR = 1.88 in men vs. 1.36 in women, P = 0.05) (Figure 1).
      Figure 1
      Figure 1Gender-stratified odds ratios for psychiatric disorders in patients with HS.

      Discussion

      The main finding of our study is that patients with HS have high psychiatric burden: every mental disorder examined was significantly more frequent in patients with HS than in patients with psoriasis. This is remarkable because, until now, psoriasis has been regarded as the dermatological diagnosis most strongly associated with psychiatric comorbidity (
      • Dalgard F.J.
      • Gieler U.
      • Tomas-Aragones L.
      • Lien L.
      • Poot F.
      • Jemec G.B.
      • et al.
      The psychological burden of skin diseases: a cross-sectional multicenter study among dermatological out-patients in 13 European countries.
      ). We found that 24.1% of patients with HS had at least one mental disorder. Previously, a US study found that up to 57% of patients with HS (n = 1,776) had also been diagnosed with a psychiatric disorder (
      • Shlyankevich J.
      • Chen A.J.
      • Kim G.E.
      • Kimball A.B.
      Hidradenitis suppurativa is a systemic disease with substantial comorbidity burden: a chart-verified case-control analysis.
      ). Of note is that the data from the US study were collected from a large academic referral center, which might have resulted in a sample of patients with more severe manifestation of HS than those identified by our national database query.
      The incidence of HS was 3.0/100,000 persons/year in our study population. To the best of our knowledge, there are only two previous studies on the incidence of HS and neither of them was nationwide (
      • Bettoli V.
      • Pasquinucci S.
      • Caracciolo S.
      • Piccolo D.
      • Cazzaniga S.
      • Fantini F.
      • et al.
      The hidradenitis suppurativa patient journey in Italy: current status, unmet needs and opportunities.
      ,
      • Vazquez B.G.
      • Alikhan A.
      • Weaver A.L.
      • Wetter D.A.
      • Davis M.D.
      Incidence of hidradenitis suppurativa and associated factors: a population-based study of Olmsted County, Minnesota.
      ). Our result is in line with a recent HS registry-based Italian study in which the overall age-standardized incidence of HS was 3.2/100,000 persons/year (
      • Bettoli V.
      • Pasquinucci S.
      • Caracciolo S.
      • Piccolo D.
      • Cazzaniga S.
      • Fantini F.
      • et al.
      The hidradenitis suppurativa patient journey in Italy: current status, unmet needs and opportunities.
      ). However,
      • Vazquez B.G.
      • Alikhan A.
      • Weaver A.L.
      • Wetter D.A.
      • Davis M.D.
      Incidence of hidradenitis suppurativa and associated factors: a population-based study of Olmsted County, Minnesota.
      reported a higher annual incidence of HS (6.0/100,000 persons/year), but their data were collected from all levels of medical care, which is probably reflected in the study’s results. The incidence of psoriasis was 27.8/100,000 persons/year in our study. Surprisingly, there are only few previous reports of the incidence of psoriasis despite it being one of the most studied skin diseases. In a US study, the incidence rate was 60.4/100,000 persons/year, but the study was limited by short observation period and identified only 132 patients with psoriasis, most of whom (58%) had mild psoriasis (
      • Bell L.M.
      • Sedlack R.
      • Beard C.M.
      • Perry H.O.
      • Michet C.J.
      • Kurland L.T.
      Incidence of psoriasis in Rochester, Minn, 1980–1983.
      ). In contrast, it is likely that our hospital-based study population had more severe disease. In an Italian study of more than 500,000 individuals, the estimated incidence of psoriasis was particularly high, at 230–321/100,000 persons/year (
      • Vena G.A.
      • Altomare G.
      • Ayala F.
      • Berardesca E.
      • Calzavara-Pinton P.
      • Chimenti S.
      • et al.
      Incidence of psoriasis and association with comorbidities in Italy: a 5-year observational study from a national primary care database.
      ). This study was based on patient records only from primary care physicians, which might have resulted in an overestimation of incidence. Because our current study is based on a hospital discharge registry, selection bias may occur with the exclusion of patients with HS or psoriasis who either did not seek medical advice or were not sent for consultation or treatment beyond primary care. Thus, our study may not have captured data from patients with the mildest HS or psoriasis, and the real incidences of these skin disorders in Finland may be higher.
      It has been stated that women are three times more frequently affected by HS than men (
      • Jemec G.B.
      Clinical practice. Hidradenitis suppurativa.
      ), although the ratios ranging from 2:1 to 5:1 have also been reported (
      • Wiseman M.C.
      Hidradenitis suppurativa: a review.
      ). Our results (58.7% women) resemble the gender distribution of a recent Israeli study (61.6% women) (
      • Shalom G.
      • Freud T.
      • Harman-Boehm I.
      • Polishchuk I.
      • Cohen A.D.
      Hidradenitis suppurativa and metabolic syndrome: a comparative cross-sectional study of 3207 patients.
      ,
      • Shavit E.
      • Dreiher J.
      • Freud T.
      • Halevy S.
      • Vinker S.
      • Cohen A.D.
      Psychiatric comorbidities in 3207 patients with hidradenitis suppurativa.
      ) and suggest that the difference between genders may not be so substantial. However, comparatively high proportion of men in our study may be explained by the fact that our data were retrieved from a hospital-based registry, which contains data on patients with HS with more severe disease who are more likely to be male than female (
      • Canoui-Poitrine F.
      • Revuz J.E.
      • Wolkenstein P.
      • Viallette C.
      • Gabison G.
      • Pouget F.
      • et al.
      Clinical characteristics of a series of 302 French patients with hidradenitis suppurativa, with an analysis of factors associated with disease severity.
      ,
      • Vazquez B.G.
      • Alikhan A.
      • Weaver A.L.
      • Wetter D.A.
      • Davis M.D.
      Incidence of hidradenitis suppurativa and associated factors: a population-based study of Olmsted County, Minnesota.
      ).
      In our study, major depression was found in 15.3%, anxiety disorders in 6.9%, and psychotic disorders in 4.7% of patients with HS. In an Israeli study of patients with HS (n = 3,207), the prevalence of all these comorbidities was lower (5.8, 3.8, and 1.3%, respectively) (
      • Shavit E.
      • Dreiher J.
      • Freud T.
      • Halevy S.
      • Vinker S.
      • Cohen A.D.
      Psychiatric comorbidities in 3207 patients with hidradenitis suppurativa.
      ). However, the Israeli study was unable to access information from psychiatric clinics, whereas our data include details of diagnoses from psychiatric hospitals, which may explain the differences. In a Danish-Dutch study (n = 211), depression was found only in 9% of patients with HS (compared with 6% in dermatological control patients) (
      • Onderdijk A.J.
      • van der Zee H.H.
      • Esmann S.
      • Lophaven S.
      • Dufour D.N.
      • Jemec G.B.
      • et al.
      Depression in patients with hidradenitis suppurativa.
      ), but the limited sample size might have had an effect on their findings. According to a US study, depression was diagnosed in more than 40% of patients with HS (
      • Vazquez B.G.
      • Alikhan A.
      • Weaver A.L.
      • Wetter D.A.
      • Davis M.D.
      Incidence of hidradenitis suppurativa and associated factors: a population-based study of Olmsted County, Minnesota.
      ). This study was larger (n = 1,263), but limited to one county and included diagnoses at all levels of medical care.
      Schizophrenia and bipolar disorder have been shown to be more common in patients with psoriasis than in healthy controls (
      • Chen S.J.
      • Chao Y.L.
      • Chen C.Y.
      • Chang C.M.
      • Wu E.C.
      • Wu C.S.
      • et al.
      Prevalence of autoimmune diseases in in-patients with schizophrenia: nationwide population-based study.
      ,
      • Han C.
      • Lofland J.H.
      • Zhao N.
      • Schenkel B.
      Increased prevalence of psychiatric disorders and health care-associated costs among patients with moderate-to-severe psoriasis.
      ), and also in our study, these disorders were more frequent in patients with psoriasis than those with melanocytic nevi. Here we demonstrate, to our knowledge, a previously unreported association between these psychiatric disorders and HS; both “schizophrenia or schizotypal disorder” and “bipolar disorder or manic episodes” were significantly more frequent in the HS group than in the control groups. Previously,
      • Shavit E.
      • Dreiher J.
      • Freud T.
      • Halevy S.
      • Vinker S.
      • Cohen A.D.
      Psychiatric comorbidities in 3207 patients with hidradenitis suppurativa.
      found a trend toward significance in the association of HS between schizophrenia and bipolar disorder, but as discussed earlier, the lack of data from psychiatric hospitals may have affected their results.
      In our study, mental disorders in general were more frequently found in women (25.5%) than in men (22.0%) with HS. This is in line with a previous study, which showed that anxiety and depression were clearly more common in female than male patients with HS (
      • Shavit E.
      • Dreiher J.
      • Freud T.
      • Halevy S.
      • Vinker S.
      • Cohen A.D.
      Psychiatric comorbidities in 3207 patients with hidradenitis suppurativa.
      ). In contrast, “schizophrenia or schizotypal disorder” was more common in men (2.7%) than in women (2.1%) with HS. This is surprising because the prevalence of schizophrenia is considered to be similar in both genders (
      • Perälä J.
      • Suvisaari J.
      • Saarni S.I.
      • Kuoppasalmi K.
      • Isometsä E.
      • Pirkola S.
      • et al.
      Lifetime prevalence of psychotic and bipolar I disorders in a general population.
      ). On the whole, “all psychotic disorders” were equally common (4.7%) in men and women.
      In a gender-stratified analysis, we investigated whether the association between HS and mental disorders differs between male and female patients. Interestingly, when compared with psoriasis controls, the association between HS and psychiatric disorders was stronger in men than in women. Anxiety disorders were clearly more frequent in men with HS than in men with psoriasis (6.2% vs. 3.8%). The difference between corresponding prevalence rates was not so substantial in women (7.5% vs. 5.9%). This may reflect that the discomfort of HS symptoms equally affects the quality of life of patients with HS in both genders (
      • Matusiak L.
      • Bieniek A.
      • Szepietowski J.C.
      Psychophysical aspects of hidradenitis suppurativa.
      ), whereas women perceive a greater negative impact of psoriasis on their mental health than do men (
      • Bohm D.
      • Stock Gissendanner S.
      • Bangemann K.
      • Snitjer I.
      • Werfel T.
      • Weyergraf A.
      • et al.
      Perceived relationships between severity of psoriasis symptoms, gender, stigmatization and quality of life.
      ).
      At the moment, it is largely unknown why mental disorders are so common in patients with HS. There is some evidence that proinflammatory cytokines (e.g., IL-10 and tumor necrosis factor-α) may contribute to the pathogenesis of mood disorders, such as depression (
      • Kohler C.A.
      • Freitas T.H.
      • Maes M.
      • de Andrade N.Q.
      • Liu C.S.
      • Fernandes B.S.
      • et al.
      Peripheral cytokine and chemokine alterations in depression: a meta-analysis of 82 studies.
      ). These cytokines are, at least partly, involved in the pathogenesis of HS (
      • Kelly G.
      • Prens E.P.
      Inflammatory mechanisms in hidradenitis suppurativa.
      ,
      • van der Zee H.H.
      • de Ruiter L.
      • van den Broecke D.G.
      • Dik W.A.
      • Laman J.D.
      • Prens E.P.
      Elevated levels of tumour necrosis factor (TNF)-alpha, interleukin (IL)-1beta and IL-10 in hidradenitis suppurativa skin: a rationale for targeting TNF-alpha and IL-1beta.
      ). Chronic inflammation is also thought to be involved in the pathogenesis of bipolar disorder and schizophrenia, but at the moment, the role of cytokine alterations in these disorders remains controversial (
      • Goldstein B.I.
      • Kemp D.E.
      • Soczynska J.K.
      • McIntyre R.S.
      Inflammation and the phenomenology, pathophysiology, comorbidity, and treatment of bipolar disorder: a systematic review of the literature.
      ,
      • Miller B.J.
      • Buckley P.
      • Seabolt W.
      • Mellor A.
      • Kirkpatrick B.
      Meta-analysis of cytokine alterations in schizophrenia: clinical status and antipsychotic effects.
      ). Interestingly, patients with HS and mental disorders share some behavioral factors: cigarette smoking is common among patients with HS (
      • Kohorst J.J.
      • Kimball A.B.
      • Davis M.D.
      Systemic associations of hidradenitis suppurativa.
      ) and in those with mental disorders (
      • Minichino A.
      • Bersani F.S.
      • Calo W.K.
      • Spagnoli F.
      • Francesconi M.
      • Vicinanza R.
      • et al.
      Smoking behaviour and mental health disorders—mutual influences and implications for therapy.
      ). In patients with HS, the effects of smoking include the induction of epidermal hyperplasia and alterations in cutaneous immune responses, thus activating the disease (
      • Kelly G.
      • Prens E.P.
      Inflammatory mechanisms in hidradenitis suppurativa.
      ). On the other hand, constituents of tobacco smoke affect the dopamine system in patients with psychiatric disorders (
      • Mackowick K.M.
      • Barr M.S.
      • Wing V.C.
      • Rabin R.A.
      • Ouellet-Plamondon C.
      • George T.P.
      Neurocognitive endophenotypes in schizophrenia: modulation by nicotinic receptor systems.
      ) and may also have a positive effect on the metabolism of medications used to treat the disorders (
      • Minichino A.
      • Bersani F.S.
      • Calo W.K.
      • Spagnoli F.
      • Francesconi M.
      • Vicinanza R.
      • et al.
      Smoking behaviour and mental health disorders—mutual influences and implications for therapy.
      ). Although smoking relieves psychiatric symptoms and consequently creates an urge to smoke even more, it may, besides its other well-known adverse effects, simultaneously lead to worsening of skin disease such as HS.
      One strength of our study is that it utilizes one of the largest nationwide HS cohorts ever studied. The Finnish hospital discharge register data have been shown to be accurate, and thus the diagnoses found in the registers can be considered reliable (
      • Sund R.
      Quality of the Finnish Hospital Discharge Register: a systematic review.
      ). In addition, we found prevalence rates of depression (12.1%) and anxiety (6.9%) corresponding to those found by previous studies among patients with psoriasis, further supporting the accuracy of our data (
      • Dalgard F.J.
      • Gieler U.
      • Tomas-Aragones L.
      • Lien L.
      • Poot F.
      • Jemec G.B.
      • et al.
      The psychological burden of skin diseases: a cross-sectional multicenter study among dermatological out-patients in 13 European countries.
      ,
      • Dowlatshahi E.A.
      • Wakkee M.
      • Arends L.R.
      • Nijsten T.
      The prevalence and odds of depressive symptoms and clinical depression in psoriasis patients: a systematic review and meta-analysis.
      ,
      • Han C.
      • Lofland J.H.
      • Zhao N.
      • Schenkel B.
      Increased prevalence of psychiatric disorders and health care-associated costs among patients with moderate-to-severe psoriasis.
      ). A weakness of the study is that in a register-based nationwide study, patients with HS given a wrong diagnosis, for example, folliculitis, are not captured, and it is not possible to verify the accuracy of the HS diagnosis. However, previous studies from the USA have shown that HS diagnosis in hospital registers has a reasonably high positive predictive value (
      • Kim G.E.
      • Shlyankevich J.
      • Kimball A.B.
      The validity of the diagnostic code for hidradenitis suppurativa in an electronic database.
      ,
      • Shlyankevich J.
      • Chen A.J.
      • Kim G.E.
      • Kimball A.B.
      Hidradenitis suppurativa is a systemic disease with substantial comorbidity burden: a chart-verified case-control analysis.
      ). The Finnish Care Register for Health Care contains data on patients discharged from inpatient care, day surgeries, and specialized outpatient care. Data contain information such as providers of hospital services and specialized health care, admission and discharge, diagnoses, and treatment procedures provided, but do not include information concerning clinical findings, behavioral matters, or socioeconomical status. Thus, we had no access to the information concerning the risk factors of HS or psoriasis such as obesity or smoking as well as clinical characteristics, for example, type and localization of cutaneous lesions and disease severity. Therefore, we were not able to perform any analysis regarding the possible differences between HS and control populations or the association between disease severity and psychiatric morbidity. It would also be important and interesting to clarify the temporal relationship between HS and psychiatric comorbidity. Our registry data contain information on the date when diagnosis was registered to patient files, but not the time when individual’s symptoms started. The diagnostic delay in HS is 5 to 14 years (
      • Jemec G.B.
      • Kimball A.B.
      Hidradenitis suppurativa: epidemiology and scope of the problem.
      ,
      • Klüger N.
      • Ranta M.
      • Serlachius M.
      The burden of hidradenitis suppurativa in a cohort of patients in Southern Finland: a pilot study.
      ,
      • Vazquez B.G.
      • Alikhan A.
      • Weaver A.L.
      • Wetter D.A.
      • Davis M.D.
      Incidence of hidradenitis suppurativa and associated factors: a population-based study of Olmsted County, Minnesota.
      ), and thus, we found that analyzing temporal relationships in this kind of setting is unreliable.
      Our study adds to previous reports of a high prevalence of psychiatric comorbidities in patients with HS and shows that these comorbidities are even more common among patients with HS than in patients with psoriasis. For dermatologists treating patients with HS, it is important to take into account the high psychiatric comorbidity burden in HS and consider the need of psychiatric consultation when managing patients with HS. Further studies, for example, prospective multicenter case-control studies, are required to clarify whether HS precedes psychiatric disease, or vice versa. Translational research focused on the immunopathomechanisms of HS and psychiatric disorders is required to determine whether these diseases share the same inflammatory processes.

      Materials and Methods

      Populations and databases

      This was a retrospective database study of all HS cases diagnosed in every Finnish hospital between 1 January 1987 and 31 December 2013; patient records were obtained from the statutory Finnish Care Register for Health Care (former name: the Finnish Hospital Discharge Register) maintained by the National Institute of Health and Welfare, and selected by diagnoses based on the International Classification of Diseases (ICD-9 codes 7058C and ICD-10 code L73.2). The Care Register covers all hospitals administered by local authorities, municipal federations, and central government as well as the largest private hospitals. Each record contains the identification numbers of the patient and hospital, primary and subsidiary diagnoses, and duration of hospital stay. The Care Register also covers outpatient visits from 1998 onwards. In Finland, ICD-9 was used between 1987 and 1995 and ICD-10 since 1996. In this study, the control populations were formed of patients diagnosed with psoriasis (ICD-9 codes 6918B, 6961A and ICD-10 code L40.0) and melanocytic nevi (ICD-9 codes 2160-9A and ICD-10 codes D22) during the same period. Patients having diagnosed with melanoma (ICD-9 codes 172 and ICD-10 codes C43 and D03) were excluded from the melanocytic nevi control population.
      Patients were defined as having HS, psoriasis, or melanocytic nevi when they had at least one documented diagnosis of the disease in question in Finnish Care Register for Health Care. Records of patients aged 10 years or more at the time of the diagnosis were included in the study because HS most often occurs after puberty (
      • Liy-Wong C.
      • Pope E.
      • Lara-Corrales I.
      Hidradenitis suppurativa in the pediatric population.
      ,
      • Palmer R.A.
      • Keefe M.
      Early-onset hidradenitis suppurativa.
      ) and differences in comorbidities between early-onset HS and normal HS have not been found (
      • Deckers I.E.
      • van der Zee H.H.
      • Boer J.
      • Prens E.P.
      Correlation of early-onset hidradenitis suppurativa with stronger genetic susceptibility and more widespread involvement.
      ). Four controls per HS case were randomly selected and matched by age and sex from the psoriasis and melanocytic nevi control groups. The psychiatric diagnoses, including both primary and subsidiary diagnoses (Supplementary Table S2), were gathered for both patients with HS and control patients from the Care Register for Health Care that also includes registry data from psychiatric hospitals.

      Statistical analyses

      The characteristics of the study population are presented as proportions and means. The associations between psoriasis or HS and a history of psychiatric disorders were evaluated using a conditional logistic regression model and presented with OR and 95% CI. The crude incidence rate was calculated as the ratio of the number of new HS cases in 1 year to the number of individuals who were at risk. The age-standardized incidence was calculated using an indirect method and used as a reference the standard population of Finland between 1987 and 2013 for different age groups, provided by Statistics Finland (http://www.tilastokeskus.fi). All statistical analyses were performed using STATA (Data Analysis and Statistical Software, MP 13, StataCorp LP, College Station, TX) and the SAS software package (version 9.4; SAS Institute, Cary, NC), and two-sided P-values less than 0.05 were considered statistically significant.

      Ethical aspects and permissions

      The data of the study population and controls were obtained without identification, and patients were not contacted, which is why a statement of the ethical committee was not required. However, a study permission was obtained from the National Institute of Health and Welfare.

      Conflict of Interest

      LH has received an educational grant from Novartis, Abbvie, and LeoPharma, honoraria as consultant and/or speaker from Novartis and UCB Pharma, and is an investigator for Abbvie. HT has received an educational grant from Novartis, Abbvie, LeoPharma, MSD, GaldermaNordic, Pfizer, Meda, and Jansen-Cilag, and sits on the Advisory Board of Roche. KT has received an educational grant from Novartis and Pfizer, and honoraria as consultant and/or speaker from Novartis, Abbvie, and Lilly. MT has received honoraria as a speaker from Merck. JJ states no conflict of interest.

      Supplementary Material

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