Abstract
Background
Alopecia areata (AA) is common non-scarring hair loss disease. Sleep distrubance has been regarded as a triggering or aggravating factor for AA. However, objective evaluation of sleep disturbance and its clinical effect on AA has not been clearly demonstrated.
Objective
This study investigated objective sleep evaluation tool for AA patients and their clinical correlation.
Methods
Patients presenting with new-onset AA or recurrences of pre-existing AA were included, and those who reported sleep disturbance in the preliminary survey were designated as the sleep disturbance group (SD group). Sleep quality was investigated for them using three self-administered questionnaires: Pittsburgh Sleep Quality Index (PSQI), Insomnia Severity Index (ISI), and Epworth Sleep Scale (ESS). Demographic information and clinical features of AA were analyzed according to sleep quality.
Results
A total of 400 participants were enrolled, and 53 were categorized into the SD group. The incidence of stressful events was significantly higher in the SD group (54.7%) than in the non-SD group (25.1%) (p<0.001). Based on the PSQI, 77.3% of participants were objective poor sleepers (score of 5 or more), and they showed a significantly higher incidence of stressful events compared to good sleepers (p=0.019). The proportion of poor sleepers was significantly lower in patients with mild AA (S1) than in those with moderate to severe AA (S2~S5) (p=0.045).
Conclusion
This study demonstrated a positive correlation among stress, SD, and AA. The degree of SD was objectively represented by the PSQI score, showing different scores according to AA severity.
Keywords: Alopecia areata, Psychological stress, Sleep wake disorders
INTRODUCTION
Alopecia areata (AA) is a common autoimmune inflammatory disease characterized by non-scarring hair loss presenting as one or multiple round to oval patches1. It usually occurs on the scalp, beard, eyebrow, or eyelid, with other areas of the body sometimes affected1,2. AA can affect individuals of all ages and both sexes, occurring in approximately 2% of the general population3. Psychological stress is known to trigger and exacerbate AA; however, the precise role of anxiety and depression in AA etiopathogenesis has not been established3,4. Likewise, progressive and recurrent episodes of hair loss easily increase anxiety levels and evoke various psychological complications in AA patients1,3.
A recent study has described the relationship between AA and sleep disorders5. However, a detailed association between sleep disturbance and AA has not been well elucidated. Given the multifactorial nature of the sleep process, it would be useful to consider multiple evaluation tools. Thus, we investigated and compared several sleep evaluation tools to elucidate the effects of sleep disturbance on AA.
MATERIALS AND METHODS
This study was approved by the Institutional Review Board of the Inje University Busan Paik Hospital (IRB No. 15-0246). Informed consent was obtained from all participants.
Patients presenting with new-onset AA or a recurrence of pre-existing AA at Busan Paik Hospital between 2015 and 2017 were included. Participants were allocated into two groups based on results of a preliminary self-survey for sleep disturbance using the question “Do you have any problem with your sleep?” Those who answered in the affirmative were designated as the sleep disturbance (SD group). Further investigations regarding sleep quality were conducted in the SD group using three self-administered questionnaires: Pittsburgh Sleep Quality Index (PSQI) (Supplementary Material 1), Insomnia Severity Index (ISI) (Supplementary Material 2), and Epworth Sleep Scale (ESS) (Supplementary Material 3).
The PSQI is a self-reported 19-item questionnaire to evaluate seven sleep components: subjective sleep quality, sleep latency, sleep duration, sleep efficiency, sleep disturbance, use of sleep medication, and daytime dysfunction. The score of each component ranges from 0 to 3 and total score is calculated by adding the component scores6.
The ISI is a self-reported questionnaire to evaluate seven components: sleep onset, sleep maintenance, early morning awakening, sleep dissatisfaction, daytime dysfunction, noticeability of sleep problem by others, and distress caused by sleep difficulties. The score of each component ranges from 0 to 4 and total score ranges from 0 to 287.
The ESS is a self-reported questionnaire to evaluate daytime sleepiness, comprised of eight situations in daily life. The score of each component ranges from 0 to 3 and total score ranges from 0 to 248. The Korean version of the PSQI, ISI, and ESS has been validated by previous studies in Korean population6,7,8. The PSQI score of 5 or more indicated poor sleep quality, while ISI score of 15 or more indicated clinical insomnia and ESS score of 10 or more indicated excessive daytime sleepiness.
Demographic information (sex, age), underlying disease, and clinical features of AA (onset age, duration, severity, hair pull test positivity, recent stressful events other than AA, history of AA, and treatment response) were reviewed. The severity of AA was categorized into two groups: mild (S1, <25% area of hair loss) or moderate to severe (S2~S5, 26%~100% area of hair loss) based on the severity of alopecia tool (SALT) score. Treatment response was divided into five grades: grade 1 (no reduction in SALT score), grade 2 (<25% reduction in SALT score), grade 3 (25%~49% reduction in SALT score), grade 4 (50%~74% reduction in SALT score), and grade 5 (>75% reduction in SALT score).
Statistical analysis was performed using SPSS software (SPSS Statistics 23.0; IBM Corp.). Subgroup analysis was performed according to the characteristics of sleep disturbance (PSQI, ISI, and ESS questionnaires), demographic information, and clinical features of AA. For statistical analysis, Pearson’s chi-squared test, linear-by-linear association, independent two-sample t-tests were performed. Logistic regression analysis was conducted to adjust risk factors (demographics and clinical features of AA) for being poor sleepers in PSQI criteria. Analysis of covariance was conducted to distinguish significant component of PSQI contributing to being poor sleepers in PSQI criteria. Results were considered statistically significant at a p-value of less than 0.05.
RESULTS
Comparison of clinical information between the SD and non-SD groups
General clinical information for the participants is shown in Table 1. A total of 400 participants were enrolled, and 53 were categorized into the SD group based on a preliminary survey of sleep disturbance. Mean age was slightly higher in the non-SD group (37.5 years) than in the SD group (35.6 years). The proportions of patients with onset at ages 20~29 and 30~39 years were higher in the SD group (33.9% and 28.3%, respectively) than in the non-SD group (18.8% and 16.1%, respectively); however, the difference was not statistically significant. The duration of AA was significantly different between the two groups, with a higher proportion of durations above 12 months in the non-SD group (p=0.038). The proportion of participants with stressful events was significantly higher in the SD group (54.7%) than in the non-SD group (25.1%) (p<0.001).
Table 1. Clinical information of overall participants.
| Characteristic | Number (%) | Sleep disturbance (+) | Sleep disturbance (–) | p-value* | |
| Total no. | 400 (100) | 53 (13.2) | 347 (86.8) | ||
| Male | |||||
| Yes | 180 (45.0) | 22 (41.5) | 158 (45.5) | 0.583 | |
| No | 220 (55.0) | 31 (58.5) | 189 (54.5) | ||
| Age (yr) | |||||
| <20 | 57 (14.3) | 3 (5.7) | 54 (15.6) | 0.219 | |
| 20~29 | 87 (21.7) | 19 (35.8) | 68 (19.6) | ||
| 30~39 | 72 (18.0) | 14 (26.4) | 58 (16.7) | ||
| 40~49 | 78 (19.5) | 9 (17.0) | 69 (19.9) | ||
| ≥50 | 106 (26.5) | 8 (15.1) | 98 (28.2) | ||
| Onset age (yr) | |||||
| <20 | 69 (17.3) | 5 (9.4) | 64 (18.4) | 0.133 | |
| 20~29 | 83 (20.7) | 18 (33.9) | 65 (18.8) | ||
| 30~39 | 71 (17.8) | 15 (28.3) | 56 (16.1) | ||
| 40~49 | 84 (21.0) | 10 (18.9) | 74 (21.3) | ||
| ≥50 | 93 (23.2) | 5 (9.4) | 88 (25.4) | ||
| Duration (mo) | |||||
| <1 | 73 (18.2) | 9 (17.0) | 64 (18.4) | 0.038 | |
| 1~3 | 132 (33.0) | 24 (45.3) | 108 (31.1) | ||
| 3~6 | 76 (19.0) | 11 (20.8) | 65 (18.8) | ||
| 6~12 | 51 (12.8) | 7 (13.1) | 44 (12.7) | ||
| ≥12 | 68 (17.0) | 2 (3.8) | 66 (19.0) | ||
| Severity | |||||
| Mild | 259 (64.8) | 36 (67.9) | 223 (64.3) | 0.603 | |
| Moderate to severe | 141 (35.2) | 17 (32.1) | 124 (35.7) | ||
| Stressful event | |||||
| (+) | 116 (29.0) | 29 (54.7) | 87 (25.1) | <0.001 | |
| (–) | 284 (71.0) | 24 (45.3) | 260 (74.9) | ||
| Past AA history | |||||
| (+) | 70 (17.5) | 11 (20.8) | 59 (17.0) | 0.503 | |
| (–) | 330 (82.5) | 42 (79.2) | 288 (83.0) | ||
Values are presented as number (%). AA: alopecia areata. *Student’s t-test or chi-square test were performed.
The proportion of the participant having at least one underlying disease was 33.7% and 22.6%, respectively in the non-SD and SD group (p=0.108). In non-SD group, the most common underlying disease was hypertension (6.9%), followed by atopic dermatitis (4.3%), hyperlipidemia (4.0%), hypo- or hyperthyroidism (2.5%), diabetes mellitus (2.5%), and major depressive disorder (2.3%). In SD group, hypo- or hyperthyroidism was most common (5.6%), followed by atopic dermatitis (3.7%), and glaucoma (3.7%).
Mean grade of treatment response was 3.96 and 4.18, respectively in the non-SD and SD group (p=0.14). In the non-SD group, the proportion was 0.5%, 8.9%, 23.0%, 27.9%, and 39.7% respectively from grade 1 to 5. In the SD group, the proportion was 1.8%, 5.6%, 11.3%, 33.9%, and 47.4% respectively from grade 1 to 5.
Subgroup analysis of AA according to PSQI, ISI, and ESS scores in the SD group
Among the 53 participants in the SD group, 41 (77.4%) were categorized as poor sleepers by scoring 5 or more on the PSQI, while the others (22.6%) were classified as good sleepers (Table 2). The mean PSQI scores of the overall SD group, good sleepers, and poor sleepers were 8.9, 3.2, and 10.4, respectively, showing a significant difference between good and poor sleepers (p<0.001). Stressful events were more likely to be present in poor sleepers (63.4%) than in good sleepers (25.0%) (p=0.019). In addition, the proportion of moderate to severe AA was significantly higher in poor sleepers (39.0%) than in good sleepers (8.3%) (p=0.045). The mean PSQI score was significantly higher in patients with moderate to severe AA than in those with mild AA (p=0.03). In logistic regression analysis, adjusted odds ratio for the presence of stressful event was significantly increased (4.83, 95% confidence interval 1.08~21.58, p=0.039).
Table 2. Clinical information of subgroups according to PSQI score in SD group.
| Characteristic | Number (%) | PSQI score | p-value | Logistic regression | |||
|---|---|---|---|---|---|---|---|
| Good sleeper (<5) | Poor sleeper (≥5) | Adjusted OR (95% CI) | p-value | ||||
| Total no. | 53 (100) | 12 (22.6) | 41 (77.4) | ||||
| Mean PSQI score* | 8.9 | 3.2 | 10.4 | <0.001 | |||
| Male | |||||||
| Yes | 22 (41.5) | 5 (41.7) | 17 (41.5) | 0.990 | 1.16 (0.25~5.20) | 0.845 | |
| No | 31 (58.5) | 7 (58.3) | 24 (58.5) | ||||
| Age (yr) | |||||||
| <20 | 3 (5.7) | 2 (16.7) | 1 (2.4) | >0.999 | 0.93 (0.83~1.05) | 0.282 | |
| 20~29 | 19 (35.8) | 2 (16.7) | 17 (41.5) | ||||
| 30~39 | 14 (26.4) | 4 (33.3) | 10 (24.4) | ||||
| 40~49 | 9 (17.0) | 2 (16.7) | 7 (17.1) | ||||
| ≥50 | 8 (15.1) | 2 (16.7) | 6 (14.6) | ||||
| Onset age (yr) | |||||||
| <20 | 5 (9.4) | 3 (25.0) | 2 (4.9) | 0.526 | 1.06 (0.93~1.21) | 0.335 | |
| 20~29 | 18 (33.9) | 2 (16.7) | 16 (39.0) | ||||
| 30~39 | 15 (28.3) | 4 (33.3) | 11 (26.8) | ||||
| 40~49 | 10 (18.9) | 2 (16.7) | 8 (19.5) | ||||
| ≥50 | 5 (9.4) | 1 (8.3) | 4 (9.8) | ||||
| Duration (mo) | |||||||
| <1 | 9 (17.0) | 0 (0.0) | 9 (22.0) | 0.343 | 0.97 (0.83~1.14) | 0.773 | |
| 1~3 | 24 (45.3) | 6 (50.0) | 18 (43.9) | ||||
| 3~6 | 11 (20.8) | 4 (33.3) | 7 (17.1) | ||||
| 6~12 | 7 (13.1) | 2 (16.7) | 5 (12.2) | ||||
| ≥12 | 2 (3.8) | 0 (0.0) | 2 (4.9) | ||||
| Severity* | |||||||
| Mild | 36 (67.9) | 11 (91.7) | 25 (61.0) | 0.045 | 6.41 (0.71~57.32) | 0.096 | |
| Moderate to severe | 17 (32.1) | 1 (8.3) | 16 (39.0) | ||||
| HPT | |||||||
| (+) | 27 (50.9) | 5 (41.7) | 22 (53.7) | 0.465 | 1.02 (0.20~5.11) | 0.977 | |
| (–) | 26 (49.1) | 7 (58.3) | 19 (46.3) | ||||
| Stressful event* | |||||||
| (+) | 29 (54.7) | 3 (25.0) | 26 (63.4) | 0.019 | 4.83 (1.08~21.58) | 0.039 | |
| (–) | 24 (45.3) | 9 (75.0) | 15 (36.6) | ||||
| Past AA history | |||||||
| (+) | 11 (20.8) | 2 (16.7) | 9 (22.0) | 0.691 | 4.48 (0.36~54.91) | 0.240 | |
| (–) | 42 (79.2) | 10 (83.3) | 32 (78.0) | ||||
Values are presented as number (%). PSQI: Pittsburgh Sleep Quality Index, SD: sleep disturbance, CI: confidence interval, OR: odds ratio, HPT: hair pull test, AA: alopecia areata. *p<0.05 in Student’s t-test or chi-square test.
The mean value of all seven components of the PSQI were significantly higher in poor sleepers than good sleepers, indicated by student’s t-test (p<0.05) (Table 3). In both the overall SD group and poor sleepers, the mean score of ‘sleep latency’ was the highest, and ‘use of sleep medications’ was lowest among all components. In further analysis of covariance, sleep latency (p<0.001) and sleep duration (p=0.002) were significantly associated with being poor sleepers, independently with other components including sleep quality, sleep-wake pattern, sleep disturbance, sleep medication, and daytime dysfunction.
Table 3. Comparison of the scores in each sleep component of PSQI between good and poor sleepers in SD group.
| Total SD group (n=53) | Good sleeper (n=12) | Poor sleeper (n=41) | p-value (student’s t-test) | |
|---|---|---|---|---|
| PSQI total score | 8.9±3.95 | 3.2±0.3 | 10.4±0.6 | <0.001 |
| Sleep quality | 1.49±0.87 | 0.7±0.5 | 1.7±0.8 | <0.001 |
| Sleep latency* | 1.89±0.93 | 0.8±0.8 | 2.2±0.7 | <0.001 |
| Sleep duration* | 1.68±1.12 | 0.3±0.5 | 2.1±0.9 | <0.001 |
| Sleep-wake patterns | 1.25±1.24 | 0.1±0.3 | 1.6±1.2 | <0.001 |
| Sleep disturbances | 1.17±0.51 | 0.9±0.3 | 1.2±0.5 | 0.009 |
| Use of sleep medications | 0.25±0.55 | 0.0±0.0 | 0.3±0.7 | 0.002 |
| Daytime dysfunction | 1.04±0.78 | 0.4±0.5 | 1.2±0.8 | 0.001 |
Values are presented as mean±standard deviation. PSQI: Pittsburgh Sleep Quality Index, SD: sleep disturbance. *p<0.05 in analysis of covariance.
The mean ISI and ESS scores were 9.6 and 5.9, respectively, in the overall SD group. Among the 53 participants in the SD group, 11 (20.7%) and 8 (15.1%) scored above the threshold values of ISI and ESS, respectively. The male proportion was significantly higher in participants with excessive daytime sleepiness according to the ESS criteria (75.0% vs. 35.6%) (p=0.037).
DISCUSSION
AA is a common hair loss disease with a broad spectrum of clinical features and age distribution1. To date, many epidemiologic studies have found the association between AA and other diseases such as asthma, atopic dermatitis, allergic rhinitis, autoimmune thyroiditis, and vitiligo9,10,11,12,13. Although the etiopathogenesis of AA is not completely established, T-cell-mediated tissue-restricted autoimmune inflammation of the hair follicle has been considered as the major pathomechanism14.
Bidirectional association between sleep disorders and the risk of AA has been suggested, however the relationship between sleep deprivation and immune dysfunction in AA is not yet fully understood5,10,15,16. Prolonged sleep disturbance is known to trigger immune dysregulation and chronic low-grade inflammation, ultimately exacerbating autoimmune diseases5,17. As various psychological problems including social anxiety or depression have been reported in AA patients, sleep quality can be easily impaired and subsequent autoimmune inflammation might have caused a vicious cycle of follicular damage.
In contrast with previous study dealing with one questionnaire, this study attempted to investigate sleep disturbance in depth employing three types of questionnaires18. Clinical performance of each questionnaire was different; almost 80% of the SD group were poor sleepers by PSQI, while only 15% to 20% of the SD group scored above thresholds in ISI and ESS. Furthermore, AA severity was significantly more severe in poor sleeper compared to good sleeper in PSQI criteria. Thus, sleep disturbance in AA patients was properly revealed through PSQI, which reflects overall sleep hygiene, however not through ISI or ESS, which are usually adopted for more specific sleep disorders such as obstructive sleep apnea.
The presence of recent stressful event, rather than sex, age, onset age, AA duration, AA severity, hair pull test positivity, past AA history, was the only significant risk factor for poor sleeper in logistic regression analysis. This indicates that stressful event strongly induced sleep disturbance independently with AA itself or age, suggesting close correlation among psychological stress, sleep disturbance, and subsequent development of AA. However, other confounding factors related to stressful events, such as nutritional status or other physical illness, might also have contributed to the occurrence of AA19.
Among all components of PSQI, especially high scores were observed in sleep latency and sleep duration, suggesting that sleep disturbance in AA patients is mainly associated with difficulty in sleep initiation and maintenance. Analysis of covariance also indicated that sleep latency and duration were independent significant factors for being poor sleeper. This finding is consistent with a previous study in Korean population, describing that both total and component-wise PSQI scores in AA patients were intermediate degree between healthy population and insomnia patients6.
Sleep disturbance was most common in patients with duration of between 1 and 3 months, and least reported in those with duration of more than 12 months. Thus, sleep disturbance appears more prevalent and more influential in the acute stage than in the chronic phase; however, further investigation is necessary to confirm this differential effect.
The relatively small sample size might be a limitation of this study. Relatively smaller size of SD group might have contributed to the dissimilar proportion of underlying disease compared with non-SD group. In addition, the assessment of detailed characteristics and temporal relationships of stressful events was insufficient. Further large-scale study and more profound analyses on stress factors and sleep behaviors would be needed.
This study suggested that subjective complaints of sleep disturbance in AA patients were well demonstrated by the PSQI, rather than by the ISI or ESS. In addition, we revealed the positive correlation among stressful events, sleep disturbance, and AA. As an easily accessible and validated method, the PSQI would be used as a practical tool for evaluation and further research of sleep disturbance in AA patients.
Footnotes
CONFLICTS OF INTEREST: The authors have nothing to disclose.
FUNDING SOURCE: None.
DATA SHARING STATEMENT
All data generated or analyzed during this study are included in this article. Further inquiries can be directed to the corresponding author.
SUPPLEMENTARY MATERIALS
Supplementary data can be found via http://anndermatol.org/src/sm/ad-22-136-s001.pdf.
Korean version of Pittsburgh Sleep Quality Index (PSQI).
Korean version of Insomnia Severity Index (ISI).
Korean version of Epworth Sleepiness Scale (ESS).
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Associated Data
This section collects any data citations, data availability statements, or supplementary materials included in this article.
Supplementary Materials
Korean version of Pittsburgh Sleep Quality Index (PSQI).
Korean version of Insomnia Severity Index (ISI).
Korean version of Epworth Sleepiness Scale (ESS).
Data Availability Statement
All data generated or analyzed during this study are included in this article. Further inquiries can be directed to the corresponding author.