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Table of Contents
ORIGINAL ARTICLE
Year : 2021  |  Volume : 39  |  Issue : 3  |  Page : 125-131

The influence of gender and smoking on hidradenitis suppurativa: A retrospective study of 161 patients in Taiwan


1 Department of Dermatology, National Cheng Kung University Hospital; Institute of Basic Medical Sciences, College of Medicine, National Cheng Kung University, Tainan, Taiwan
2 Department of Dermatology, National Cheng Kung University Hospital, College of Medicine, National Cheng Kung University, Tainan, Taiwan
3 Institute of Clinical Medicine; Department of Public Health; Biostatistics Consulting Center, National Cheng Kung University Hospital, College of Medicine, National Cheng Kung University, Tainan, Taiwan
4 Department of Dermatology, National Cheng Kung University Hospital, College of Medicine; International Center for Wound Repair and Regeneration, National Cheng Kung University, Tainan, Taiwan
5 Institute of Basic Medical Sciences; Department of Physiology, College of Medicine, National Cheng Kung University, Tainan, Taiwan

Date of Submission20-Apr-2021
Date of Decision13-Jun-2021
Date of Acceptance17-Jun-2021
Date of Web Publication20-Sep-2021

Correspondence Address:
Dr. Chao-Chun Yang
Department of Dermatology, National Cheng Kung University Hospital, College of Medicine, National Cheng Kung University, 1 University Road, Tainan 70101
Taiwan
Dr. Shaw-Jenq Tsai
Department of Physiology, College of Medicine, National Cheng Kung University, 1 University Road, Tainan 70101
Taiwan
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Source of Support: None, Conflict of Interest: None


DOI: 10.4103/ds.ds_32_21

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  Abstract 


Background: Hidradenitis suppurativa (HS) is a severe dermatological disease that significantly reduces life quality. However, the etiology of this disease remains largely unknown. Objectives: We sought to identify the factors associated with clinical presentation and the severity of HS. The features of HS between genders and smokers/nonsmokers were compared. Methods: A single-center retrospective study of 161 patients with HS was conducted and analyzed. Results: The male-to-female ratio in HS was approximately 2:1 in Taiwan. The severity of HS was significantly associated with smoking (odds ratio 2.20, P = 0.018). HS in men more frequently occurred in the gluteal region. Nonsmokers in HS tended to have earlier onset age and axillary lesions. Smokers were prone to have exclusive gluteal involvement and negative family history of HS. Conclusion: Our data revealed smoking correlated with the severity of HS. Smoking status and gender influence the clinical characteristics in HS.

Keywords: Acne inversa, gender, hidradenitis suppurativa, smoking


How to cite this article:
Chu CB, Li WL, Lin SH, Hsu CK, Yang CC, Tsai SJ. The influence of gender and smoking on hidradenitis suppurativa: A retrospective study of 161 patients in Taiwan. Dermatol Sin 2021;39:125-31

How to cite this URL:
Chu CB, Li WL, Lin SH, Hsu CK, Yang CC, Tsai SJ. The influence of gender and smoking on hidradenitis suppurativa: A retrospective study of 161 patients in Taiwan. Dermatol Sin [serial online] 2021 [cited 2021 Oct 19];39:125-31. Available from: https://www.dermsinica.org/text.asp?2021/39/3/125/326270




  Introduction Top


Hidradenitis suppurativa (HS) mainly affects the intertriginous areas after puberty with relapsing painful or tenderness nodules, draining abscesses, and sinus tracts.[1] The disease causes chronic pain, malodorous discharge and inflammation, leading to a low quality of life, disfigurement, skin contractures, psychosocial problems, sexual distress, and depression.[2] Amelioration of the symptoms during pregnancy and after menopause is often observed.[3] The estimated prevalence varies from 0.05% to 4.1% in the general population.[4] The variation may result from the criteria and methods to recognize HS in different regions.[5] The typical age of onset is in the early 20s.[6] Most studies displayed a gender disparity in HS patients.[7] The risk factors of HS include obesity, smoking, family history, and premenstrual flares.[8] Gamma-secretase gene-associated mutations have been found worldwide in more than 30 families with HS in an autosomal dominant manner.[9]

Tobacco smoking is closely associated with HS. A meta-analysis reported a significant relationship between current smokers and HS (odds ratio, 4.26; 95% confidence interval, 3.68–4.94).[10] In the United States, HS incidence in smokers and nonsmokers was 0.20% and 0.11%, respectively.[11] The smoking status also influences the treatment outcome, prognosis, and involving areas in HS. First, the response to the first-line HS treatment was better in nonsmokers. Second, the chance of remission in the long-term follow-up was lower in current smokers (29%) than noncurrent smokers (49%, including nonsmoker and ex-smokers).[12] Third, the smokers were prone to have more than two body areas with HS lesions than nonsmokers.[13] The role of smoking in the pathogenesis of HS is still speculative. Nicotine, an addictive chemical in tobacco, can stimulate the glandular secretion of apocrine glands and eccrine glands, which may participate in follicular occlusion.[14] Nicotine also can cause epidermal hyperplasia of the skin and hair follicles which are the typical pathologic characteristic in HS. Moreover, nicotinic nonneuronal acetylcholine receptors are highly expressed in the epidermis of the intrafollicular and interfollicular regions.[15] On the other hand, elevated serum interleukin (IL)-36α, IL-36 β, and IL-36 γ levels were reported in current smokers of HS patients.[16] Smokers also have a higher serum level of tumor necrosis factor-α (TNF-α).[17] TNF-α and IL-36 can induce inflammatory responses and are related to many autoimmune and skin diseases, such as psoriasis, inflammatory bowel disease, and rheumatoid arthritis. The TNF-α antagonist, adalimumab, is one of the standard treatments for moderate-to-severe HS.[18] The above studies suggest that nicotine and the cytokines induced by smoking could contribute to the pathogenesis of HS.

The location of HS lesions is different in men and women. A cohort study in Italy reported that gluteal lesions were more common in men (men 32.3% vs. women 8.7%, P < 0.001).[19] In Korea, women with HS were prone to have lesions on the axillary and groins, whereas men with HS were more common with lesions on the gluteal area.[20] In addition, the gluteal, perianal, and atypical lesions (such as chest and ears) were predominantly involved among male HS patients in the Dutch and French studies.[21],[22]

Hormonal changes during the menstrual cycle, pregnancy, or menopause may also influence the activity of HS. About 43%–62% of women with HS reported perimenstrual flare-up of the disease activity.[23],[24] In one study that used an anonymous questionnaire, HS usually worsened in the week before menstruation, accounting for 78.9% of HS patients with perimenstrual flares.[24] During pregnancy, the symptoms were improved in 20%–32%, stationary in 54%–72%, and worsened in 8%–16% HS patients. Postpartum exacerbation occurred in 40% of pregnancy in HS patients.[25] Remission related to menopause was reported by 48% of women with HS in a long-term cross-sectional study.[12]

Epidemiological studies revealed geographic differences regarding the demographic and clinical characteristics of HS.[7],[26],[27],[28] Frequent gluteal involvement had been observed in Asia.[26] Women are affected two to three times more often than men in Europe[21],[22],[29],[30],[31] and North America.[32],[33],[34] In comparison, HS is more common in men in Asia, including Japan,[26],[27] Korea,[20],[35] Malaysia,[36],[37] Singapore,[38] and Turkey.[39],[40],[41]

There are limited numbers of retrospective cohort and epidemiological studies on HS in Asia. Therefore, we collected and analyzed the data of 161 patients with HS in Taiwan and focused on the different clinical characteristics between genders, smoking, and the risk factors for disease severity.


  Methods Top


Patients

Consecutive patients between October 1988 and October 2020, with the diagnosis of HS, were collected from the patient database of a tertiary medical center in Southern Taiwan. HS was diagnosed according to the following: (1) typical lesions: deep-seated nodules, abscesses, sinus tracts, or scarring; (2) locations: including at least one of axillae, groins, gluteal, anogenital and infra-and inter-mammary area; and (3) a chronic and relapsing course.[42] All three criteria need to be met to diagnose HS. The protocol was approved by the Institutional Review Board of National Cheng Kung University Hospital (B-BR-109-060). The patient consent was waived by the IRB.

Data collection

The clinical characteristics were obtained from the medical records and photographs. Disease severity was assessed by Hurley classification[43] for the area with the highest severity by clinical inspection or photographic review. Positive family history was defined as a patient-reported history of HS symptoms in first-degree or second-degree relatives. Overweight and obesity were defined as body mass index (BMI) between 25 and 30 kg/m2, and more than 30 kg/m2, respectively. The diagnosis of dissecting cellulitis of the scalp was established either clinically by the presence of multiple recurrent interconnecting nodules or abscesses on the scalp or with pathological confirmation.[44] The diagnosis of the pilonidal sinus was based on pathology or skin depressions in the midline of the intergluteal fold.[45]

Data analysis

All statistical analyses were performed using the SPSS 25.0 software (IBM SPSS, Armonk, NY, USA). The comparison of BMI between subgroups was performed using Student's t-test. Categorical data, including gender, obesity status, smoking status, family history of HS, acne history, comorbid diseases, affected regions, and Hurley stage, were compared by the Fisher exact test or Chi-square test. The Mann–Whitney U-test was used for analyzing the onset age and diagnosis age, which were variables in nonnormally distribution. The univariable and multivariable ordinal logistic regression was used to identify the factors related to disease severity. The significant risk factors (P < 0.05) identified by the univariable analysis would be put into the model of multivariate analysis. Statistical significance was considered when P < 0.05.


  Results Top


The clinical characteristics of hidradenitis suppurativa patients

A total of 161 patients with HS were included, of whom 110 (68.3%) were male and 51 (31.7%) were female. The patients were Taiwanese except for two male Caucasians. The mean onset age of HS symptoms was 23.3 ± 8.9 years. The mean age of HS diagnosis was 28.2 ± 9.8 years (range: 8–56 years). The percentage of Hurley Stage I, II, and III was 42.9%, 42.2%, and 14.9%, respectively.

The mean BMI of the participants was 27.2 ± 5.8 kg/m2. Nearly two-thirds of the participants were overweight (31.3%) or obese (30.6%). One-fourth of the participants, in whom the family history was available in the medical chart (n = 57), reported a positive family history of HS. Fifty-four patients (36%) were current smokers, 4 (2.7%) were ex-smokers, whereas 92 (61.3%) patients were nonsmokers.

The most commonly affected anatomic regions were the axillary (60.2%), gluteal (58.4%), and groin (22.4%) regions, following by chest (19.3%), thighs (11.2%), and nape (10.6%). Less than 10% of patients had lesions on the pubis, perianal, abdomen, genital, anterior neck, and inframammary areas. Thirty-eight (23.6%) patients had the lesions exclusively on the gluteal regions.

The comparison between male and female hidradenitis suppurativa patients

The characteristics of male and female HS patients are listed in detail and compared in [Table 1]. Male patients outnumbered female patients by more than two folds (68.3% vs. 31.7%) in HS. The smoking rate was significantly higher in male HS patients than female HS patients (current smoker and ex-smoker, 51.5% vs. 12.2%; P < 0.001). The involvement of gluteal regions was more frequent in men. There was no significant difference in disease severity, age of disease diagnosis and onset, BMI, family history of HS, the coexistence of diabetes mellitus, hypertension, and hyperlipidemia between male and female HS patients. Male HS patients more commonly had a history of severe acne than female HS patients (41.8% vs. 13.7%; P < 0.001).
Table 1: Demographical characteristics of hidradenitis suppurativa patients by gender

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The comparison between smokers and nonsmokers in hidradenitis suppurativa patients

The characteristics of smokers (including current and ex-smokers) and nonsmokers in HS patients are summarized in [Table 2]. The age of disease onset and diagnosis was earlier in nonsmokers than smokers (disease onset: 22.2 ± 8.4 vs. 25.8 ± 10.3 years, disease diagnosis: 26.3 ± 8.3 vs. 32.4 ± 11.1 years). A family history of HS was more common in nonsmokers than smokers (35.5% vs. 4.3%; P = 0.01). Nonsmokers in HS had a higher proportion of axillary involvement than smokers.(69.6% vs. 48.3%; P = 0.01) In contrast, exclusive gluteal involvement was more common in smokers than in nonsmokers (32.8% vs. 14.1%; P = 0.008).
Table 2: Demographical characteristics of hidradenitis suppurativa patients by smoking status

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Comorbid diseases in hidradenitis suppurativa patients

Dyslipidemia (12.4%), hypertension (11.8%), and diabetes mellitus (11.2%) were the highest coexisting diseases, followed by allergic rhinitis (6.2%), dissecting cellulitis of the scalp (6.2%), polycystic ovaries syndrome (4.3%), perianal abscess or fistula (4.3%), hepatitis B (3.7%), pilonidal sinus (3.1%), asthma (3.1%), atopic dermatitis (3.1%), anemia (3.1%), and psychiatric disorders (3.1%). There were six patients with autoimmune diseases (two with ankylosing spondylitis, one with ulcerative colitis, one with Sjogren syndrome, and one with systemic juvenile rheumatoid arthritis).

Risk factors associated with the severity of hidradenitis suppurativa

In univariate ordinal logistic regression analysis, the Hurley score was significantly associated with smoking, history of severe acne, and axillae involvement. There was no significant link between gender, onset age, BMI, and family history of HS. The multivariate ordinal logistic regression analysis revealed that smoking (odds ratio 2.20, P = 0.018) was the risk factor for disease severity [Table 3].
Table 3: Risk factors associated with disease severity of hidradenitis suppurativa

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  Discussion Top


In this retrospective study, the characteristics of HS between genders and between smokers and nonsmokers were compared, and the risk factors associated with disease severity of HS were identified. Smoking, severe acne, and gluteal area involvement were significantly more common in male HS patients than the female counterpart. On the other hand, female HS patients were more likely to have axillary involvement. Our study demonstrated smokers are more common to have exclusive gluteal involvement than nonsmokers in HS. The smoking status and gender affected the clinical presentation of HS. Canoui-Poitrine et al. first used a statistical method of latent class analysis to survey 618 h patients.[46] They proposed three clinical subtypes: Axillary-mammary type, follicular type, and gluteal type. The smoking rate in the gluteal phenotype was 82.3%, followed by axillary-mammary type (66.9%) and follicular phenotype (74.5%).[46]

Our results showed that the smoking rate was significantly higher in male HS patients than female HS patients (P < 0.001). The smoking rate in HS patients was higher than the general population of Taiwan,[47] supporting the role of smoking in the pathogenesis of HS.[10],[11] In the United States, smokers were prone to develop HS than nonsmokers, and the odds ratio was 1.9.[11] Smoking status also influent the treatment response of first-line therapy in HS patients. Nonsmokers seemed to have more improvement than smokers.[48]

The pathogenic mechanism in smoking effect on HS is still unclear. Nicotine in the cigarette can induce epidermal hyperplasia of the skin[15] and increase Staphylococcus aureus growth.[49] The dioxin-like compound of the cigarette can also activate the aryl hydrocarbon receptor.[50] Serum TNF-α,[17] IL-36α, IL-36 β, and IL-36 γ[16] levels were increased in current smokers of HS patients.

In [Table 3], the severity of HS was associated with axillary involvement but not gluteal involvement. The reason might be the higher frequency of axillary involvement and the lower frequency of gluteal involvement in HS patients of higher severity. In our data, axillary involvement was noted in 47.8% of HS patients in Hurley I and 69.5% in Hurley II-III. In contrast, the gluteal involvement was 65.2% in Hurley I and 53.3% in Hurley II-III. Our results are consistent with a study of 846 Dutch HS patients, which found that axillary involvement was the risk factor for disease severity.[21]

HS occurs more commonly in men than in women in Asia. The male-to-female ratios were 1.4:1 in Singapore,[38] 2.5:1 in Korea,[20] 2.7:1 in Japan,[27] and 5.2:1 in Malaysia.[36] The male-to-female ratio was about 2.2:1 in Taiwan, which was similar to Japan and Korea. The geographic gender difference in HS may result from genetics, hormones, or smoking. The family history of HS is 24.0% in Singapore,[38] 25.8% in Malaysia,[36] and 25.0% in Taiwan. However, the positive family history in Japan[27] and Korea[20] was 1.5% and 5.3%, respectively. The reason for the difference in Asia's countries was not clear and may include different diagnostic criteria or recruitment strategies.

The epidemiology studies of North America and Europe revealed female predominance in HS. In contrast, the male-to-female ratio is the opposite (1.42–5.20) in the Asian countries and this study.[20],[26],[27],[35],[36],[37],[38],[39],[40],[41] The possible cause for the geographic gender difference in HS prevalence was genetics, hormones, or smoking.[7],[26],[27],[51] HS patients in Sweden, France, Greece, Ireland, Finland, and Denmark had a higher rate of positive family history (35.3%–41.6%) than patients in Korea and Japan (1.5% and 5.3%, respectively).[20],[22],[27],[30],[52],[53],[54],[55] The smoking rates in HS patients were higher in North American and European countries than in Asian countries. The severity of HS, based on Hurley stage, showed great diversity among different countries.

The limitations of this study were mainly from its retrospective nature. The assessment of the Hurley stage might not be accurate because some features, including sinus tract formation, were difficult to be assessed by photography review. The result was from a single referral medical center, and statistical power was restricted by sample size. Future studies will be required to investigate the role of smoking and gender difference in the pathogenesis of HS.


  Conclusion Top


Our study suggests that smoking is a critical factor with the influence of disease severity in HS. The female prominence was similar to other Asia countries. Exclusive gluteal involvement was significantly linked with smoking. Therefore, the smoking status should be obtained when encountering HS patients in the clinic. Physicians should emphasize the association between smoking and HS. Smoking cessation should be considered as a part of HS treatment.

Financial support and sponsorship

This study was funded by a grant from the Clinical Research Fund of National Cheng Kung University Medical Center (NCKUH-11004023) and in part by the Ministry of Science and Technology, Taiwan (MOST 108-2321-B-006-006).

Conflicts of interest

Dr. Chao-Kai Hsu and Prof. Chao-Chun Yang, editorial board members at Dermatologica Sinica, had no roles in the peer review process of or decision to publish this article. The other authors declared no conflicts of interest in writing this paper.



 
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  [Table 1], [Table 2], [Table 3]



 

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