10.5826/dpc.1401a6
Introduction: Alopecia areata is an organ-specific autoimmune disease. In addition, treatment options are limited in pediatric patients. Topical immunotherapy treatment may be preferred, especially in pediatric patients with severe and/or refractory alopecia areata.
Objectives: In this study, it was aimed to examine the effect of atopic dermatitis, which is one of the poor prognostic factors in pediatric alopecia areata, on topical immunotherapy treatment.
Methods: The data of patients aged 18 years and younger who received at least 20 sessions of topical immunotherapy with the diagnosis of alopecia areata in our clinic between January 2018 and December 2020 were analyzed.
Results: A total of 139 patients were included in the study. The mean age of the patients was 10.29 years, 67 (48.20%) of the patients were female, 72 (51.80%) were male, 24 (17.26%) of the patients had mild disease, 115 of them (82.73%) had severe disease. Atopic dermatitis accompanying alopecia areata was detected in 38 of the patients. Inadequate response was obtained in 60 (43.17%) patients and adequate response was obtained in 79 (56.83%) patients with topical immunotherapy treatment. In addition, the presence of atopic dermatitis in the patient group with inadequate response to treatment was found to be statistically significantly higher than the patient group with adequate response to treatment.
Conclusions: Topical immunotherapy treatment was found to be effective in 56.83% of pediatric alopecia areata patients included in the study. Our study showed that questioning pediatric alopecia areata patients for atopic dermatitis before topical immunotherapy treatment can predict the response to treatment.
text/xml
2160-9381
3248
en
Zekayi Kutlubay
https://creativecommons.org/licenses/by-nc/4.0
Dermatology Practical & Conceptual
topical immunotherapy
Retrospective Analysis of the Effect of Comorbid Atopic Dermatitis on the Treatment Response to Topical Immunotherapy in Pediatric Alopecia Areata Patients
Text.Serial.Journal
https://dpcj.org/index.php/dpc
Original Article
2024-01-31
2023-02-15
2024-01-31
2024-02-21
e2024006
Dermatol Pract Concept
Introduction: Alopecia areata is an organ-specific autoimmune disease. In addition, treatment options are limited in pediatric patients. Topical immunotherapy treatment may be preferred, especially in pediatric patients with severe and/or refractory alopecia areata.
Objectives: In this study, it was aimed to examine the effect of atopic dermatitis, which is one of the poor prognostic factors in pediatric alopecia areata, on topical immunotherapy treatment.
Methods: The data of patients aged 18 years and younger who received at least 20 sessions of topical immunotherapy with the diagnosis of alopecia areata in our clinic between January 2018 and December 2020 were analyzed.
Results: A total of 139 patients were included in the study. The mean age of the patients was 10.29 years, 67 (48.20%) of the patients were female, 72 (51.80%) were male, 24 (17.26%) of the patients had mild disease, 115 of them (82.73%) had severe disease. Atopic dermatitis accompanying alopecia areata was detected in 38 of the patients. Inadequate response was obtained in 60 (43.17%) patients and adequate response was obtained in 79 (56.83%) patients with topical immunotherapy treatment. In addition, the presence of atopic dermatitis in the patient group with inadequate response to treatment was found to be statistically significantly higher than the patient group with adequate response to treatment.
Conclusions: Topical immunotherapy treatment was found to be effective in 56.83% of pediatric alopecia areata patients included in the study. Our study showed that questioning pediatric alopecia areata patients for atopic dermatitis before topical immunotherapy treatment can predict the response to treatment.
Zekayi Kutlubay
2024/01/31
10.5826/dpc.1401a6
e2024006
Istanbul University-Cerrahpaşa, Cerrahpaşa Medical Faculty, Dermatology Department, Istanbul, Turkey
2160-9381
topical immunotherapy
en
e2024006
Zerbinati N, Esposito C, D'Este E, Calligaro A, Valsecchi R. Topical Immunotherapy of Alopecia Areata: A Large Retrospective Study. Dermatol Ther (Heidelb). 2018;8(1):101-110. DOI: 10.1007/s13555-018-0226-5. PMID: 29442292. PMCID: PMC5825331.
Retrospective Analysis of the Effect of Comorbid Atopic Dermatitis on the Treatment Response to Topical Immunotherapy in Pediatric Alopecia Areata Patients
https://dpcj.org/index.php/dpc/article/download/3248/2417
    Retrospective Analysis of the Effect of Comorbid
      Atopic Dermatitis on the Treatment Response
     to Topical Immunotherapy in Pediatric Alopecia
                    Areata Patients
                  Ayşe Mine Gök1, Özge Aşkın2, Server Serdaroğlu2, Zekayi Kutlubay2


1 Şırnak State Hospital Dermatology Department, Şırnak, Turkey
2 Istanbul University-Cerrahpaşa, Cerrahpaşa Medical Faculty, Dermatology Department, Istanbul, Turkey



Key words: alopecia areata, atopic dermatitis, topical immunotherapy
Citation: Gok AM, Aşkın Ö, Serdaroglu S, Kutlubay Z. Retrospective Analysis of the Effect of Comorbid Atopic Dermatitis on the
Treatment Response to Topical Immunotherapy in Pediatric Alopecia Areata Patients. Dermatol Pract Concept. 2024;14(1):e2024006.
DOI: https://doi.org/10.5826/dpc.1401a6
Accepted: July 30, 2023; Published: January 2024
Copyright: ©2024 Gok et al. This is an open-access article distributed under the terms of the Creative Commons Attribution-
NonCommercial License (BY-NC-4.0), https://creativecommons.org/licenses/by-nc/4.0/, which permits unrestricted noncommercial use,
distribution, and reproduction in any medium, provided the original authors and source are credited.
Funding: None.
Competing Interests: None.
Authorship: All authors have contributed significantly to this publication.
Corresponding Author: Ayşe Mine Gök, Cizre Street Şırnak State Hospital, Şırnak, Turkey. E-mail: draysebayazit@gmail.com




  ABSTRACT             Introduction: Alopecia areata is an organ-specific autoimmune disease. In addition, treatment options
                       are limited in pediatric patients. Topical immunotherapy treatment may be preferred, especially in
                       pediatric patients with severe and/or refractory alopecia areata.
                       Objectives: In this study, it was aimed to examine the effect of atopic dermatitis, which is one of the
                       poor prognostic factors in pediatric alopecia areata, on topical immunotherapy treatment.
                       Methods: The data of patients aged 18 years and younger who received at least 20 sessions of topical
                       immunotherapy with the diagnosis of alopecia areata in our clinic between January 2018 and Decem-
                       ber 2020 were analyzed.
                       Results: A total of 139 patients were included in the study. The mean age of the patients was 10.29 years,
                       67 (48.20%) of the patients were female, 72 (51.80%) were male, 24 (17.26%) of the patients had mild
                       disease, 115 of them (82.73%) had severe disease. Atopic dermatitis accompanying alopecia areata was
                       detected in 38 of the patients. Inadequate response was obtained in 60 (43.17%) patients and adequate
                       response was obtained in 79 (56.83%) patients with topical immunotherapy treatment. In addition, the
                       presence of atopic dermatitis in the patient group with inadequate response to treatment was found to be
                       statistically significantly higher than the patient group with adequate response to treatment.
                       Conclusions: Topical immunotherapy treatment was found to be effective in 56.83% of pediatric alopecia
                       areata patients included in the study. Our study showed that questioning pediatric alopecia areata patients
                       for atopic dermatitis before topical immunotherapy treatment can predict the response to treatment.


Original Article | Dermatol Pract Concept. 2024;14(1):e2024006                                                                       1
Introduction                                                         dermatitis accompanying alopecia areata on the treat-
                                                                     ment of pediatric alopecia areata patients receiving topical
Alopecia areata is an autoimmune disease characterized by            immunotherapy.
non-cicatricial alopecia of the scalp and/or body with an un-
predictable course [1]. Alopecia areata affects approximately
2% of the general population throughout life [2]. The epide-         Methods
miology, clinical features and treatment of childhood alope-
                                                                     Patient Selection
cia areata have been less studied [3].
    Although the pathogenesis of alopecia areata is still un-        In our study, the clinical data of patients aged 18 years and
known, the common theory in the pathogenesis is the loss             younger who received at least 20 sessions of topical immu-
of immune privilege in the hair follicle caused by immune            notherapy (SADBE/DPCP) treatment with the diagnosis of
­mechanisms [4]. Alopecia areata is accepted as a tissue-­specific   alopecia areata in our clinic between January 2018 and De-
autoimmune disease that occurs with an environmental trig-           cember 2020 were retrospectively analyzed. Patients with a
gering factor on the basis of genetic predisposition [5-7].­         follow-up period of less than 6 months and receiving addi-
Relationships have been reported between alopecia areata             tional treatment were excluded from the study.
and autoimmune diseases such as autoimmune thyroid dis-
eases, vitiligo, type 1 diabetes mellitus and celiac disease         Patient Evaluation
[8]. It has also been reported that atopic conditions such as        Pre-treatment hair loss severity was evaluated according to
atopic dermatitis, allergic rhinitis, and asthma are common          the criteria defined in the alopecia areata research evaluation
comorbid diseases in alopecia areata [9].                            guidelines: S0: no hair loss, S1:<25%, S2:25-49%, S3:50-
    Treatment decision in alopecia areata; it is given by eval-      74%, S4:75%-99, S5:100% hair loss as classified. S1 and S2
uating factors such as the age of the patient, the severity of       were considered mild disease and S3, S4 and S5 were consid-
the disease, the duration of the disease, access to treatment        ered severe disease.
and the cost of treatment [10]. However, there is currently no          The patients response to treatment was evaluated ac-
curative treatment. Topical treatments used in pediatric al-         cording to the improvement in the percentage of baseline
opecia areata include contact immunotherapy, cryotherapy,            SALT score. Accordingly, good response ≥50% improve-
topical minoxidil, topical calcineurin inhibitors, topical and       ment, moderate response 25%-49% improvement, poor re-
intralesional steroids, and topical prostaglandins. Systemic         sponse 1%-24%, and the same SALT score before and after
treatments used include systemic steroids, methotrexate, sul-        treatment were considered as non-response. Good and mod-
fasalazine, hydroxychloroquine and jack inhibitors. The use          erate responders were graded as adequate response, poor
of systemic steroids is limited due to significant side effects,     response, and non-responders as inadequate response, and
while the use of systemic JAK inhibitors is limited due to           statistics were made accordingly.
their safety profile and cost [11]. Topical immunotherapy               In addition, the presence of atopic dermatitis, which was
offers the best efficacy and safety in long-term treatment in        determined using Hanifin Rajka diagnostic criteria, was re-
patients with treatment-resistant alopecia areata [12].              corded in the patients before treatment. In patients with atopic
    Agents used in topical immunotherapy; contact sen-               dermatitis, atopic dermatitis disease severity was graded using
sitizing agents such as diphenylcyclopropenone (DPCP),               the SCORing Atopic Dermatitis (SCORAD) scoring system.
dinitrochlorobenzene (DNCB), squaric acid dibutylester                  This study was approved by the tertiary hospital ethics
(SADBE). Although the mechanism of action is not fully               committee (No. 154281; August 6, 2021). Written informed
known, it is thought that they act by reducing the CD4+/             consent was obtained from all participants.
CD8+ lymphocyte ratio around the follicle, directing T lym-
phocytes from the perifollicular area to the interfollicular         Statistical Methods
area and dermis, and attracting new T lymphocytes to the             Statistical analyses in the study were made with the NCSS
treated area, which eliminates the antigenic stimulus [13].          (Number Cruncher Statistical System) 2007 Statistical Soft-
                                                                     ware package program. In the evaluation of the data, besides
                                                                     descriptive statistical methods (mean, standard deviation
Objectives
                                                                     [sd], median, etc), the distribution of variables was examined
The search for effective and safe treatment in alopecia              with the Shapiro-Wilk test of normality. Binary groups of
areata, especially in severe and treatment-resistant pediatric       normally distributed variables independent t-test was used
patients, is still ongoing. Topical immunotherapy treatment          for comparison and Mann-Whitney U test was used for com-
is frequently preferred in this patient group. In this study,        parison of binary groups of variables that did not show nor-
we aimed to retrospectively evaluate the effect of atopic            mal distribution. Chi-square test was used in the comparison



2                                                                        Original Article | Dermatol Pract Concept. 2024;14(1):e2024006
of qualitative data and logistic regression analysis was used    atopy were found to be statistically significantly higher than
to determine the factors affecting response to treatment. The    the patient group without atopic dermatitis (P values, re-
results were evaluated at the significance level of P < 0.05.    spectively: 0,0001, 0,036, 0,001). When the severity of the
                                                                 disease was evaluated according to the pre-treatment SALT

Results                                                          scores; in the group with atopic dermatitis, mild disease was
                                                                 detected in 4 patients (10.53%), while severe disease was de-
A total of 139 patients, 69 of whom received SADBE and           tected in 34 patients (84.47%), in the group without atopic
70 of whom received DPCP treatment, were included in the         dermatitis, mild disease was found in 20 patients (19.80%)
study. Sixty-seven (48.20%) of the patients were female and      and severe disease was found in 81 patients (80.20%). How-
72 (51.80%) were male. The mean age was 10.29 years (sd:         ever, these evaluations were not found suitable for statistical
3.77 years) and the mean disease duration was 4.02 years         interpretation in terms of their distribution (Table 1).
(sd: 2.84 years). In addition, 44 (31.65%) patients had nail        When the response to topical immunotherapy treat-
involvement (due to alopecia areata), 31 (22.3%) had a           ment was evaluated according to the improvement in the
family history of alopecia areata, 31 (22.3%) had a family       percentage of baseline SALT score, 37 (26.62%) of the pa-
history of atopic disease. The mean value of the total IgE       tients had no response, 23 (16.55%) had a poor response,
level of the patients before the treatment was 283.87 IU/ml      and 14 (10.07%) moderate response was obtained, and 65
(sd:864.28 IU/ml), and the lowest value was 0 and the high-      (46.76%) had good response. When the conditions affecting
est value was 9024 IU/ml (normal value:0-100 IU/ml).             the response to treatment were examined; when the data of
    However, 38 (27.34%) patients had atopic dermatitis.         60 patients who responded inadequately to treatment with
When the data of 38 patients with atopic dermatitis were         topical immunotherapy treatment and 79 patients who re-
compared with the data of 101 patients without atopic der-       sponded adequately to treatment were compared. There
matitis; no significant difference was observed between the      was no statistically significant difference between the two
two groups in terms of gender distribution, mean age, dis-       groups in terms of: gender distribution, mean age, distribu-
ease duration (years), and the presence of a family history of   tion of treatment type (SADBE/DPCP), mean duration of
alopecia areata (P values, respectively: 0.378, 0.329, 0.780,    disease (years), presence of nail involvement (due to alope-
0.810). In the patient group with atopic dermatitis, the mean    cia areata), presence of family history of alopecia areata and
of total IgE values, the presence of nail involvement (due       mean total IgE (P values ​​respectively: 0.092, 0.123, 0.448,
to alopecia areata), and the presence of a family history of     0.798, 0.271, 0.281, 0.170). The presence of family history



  Table 1. Comparison of the data of the patient group with atopic dermatitis and the patient group
                                     without atopic dermatitis.
                                                                 Atopic Dermatitis       Atopic Dermatitis (+)
                                                                    (-) N = 101                 N = 38                  P
 Age (Years)                             Mean±Standard                 10.49±3.90                9.79±3.38           0.333
                                         Deviation
 Gender                                  Male                     50         49.50%         22       57.89%          0.378
                                         Female                   51         50.50%         16       42.11%
 Disease duration (years)                Mean±Standard                 4.08±2.92                 3.84±2.67           0.780
                                         Deviation
                                         Median (IQR)                    4 (2-6)                 3 (2-5.25)
 Nail involvement                        (-)                      37         36.63%          7       18.42%          0.04
 (due to alopecia areata)                (+)                      64         63.37%         31       81.58%
 Family history of alopecia areata       (-)                      79         78.22%         29       76.32%          0.810
                                         (+)                      22         21.78           9       23.68%
 Family history of atopy                 (-)                      89         88.12%         24       63.16%          0.001
                                         (+)                      12         11.88%         14       36.84%
 Total IgE                               Mean±Standard             133.46±310.21            683.63±1516.59           0.0001
 (IU/ml)                                 Deviation
                                         Median (IQR)            43.32 (15.7-91.77)      251.5 (36.92-617.55)

IQR = interquartile range.



Original Article | Dermatol Pract Concept. 2024;14(1):e2024006                                                                3
                           Table 2. Distribution of factors affecting treatment response.
                                                                      Inadequate response             Adequate
                                                                          to treatment               response to
                                                                              N = 60              treatment N = 79             P
 Age (years)                                                                  9.73±3.25               10.72±4.08           0.123
 Gender                                   Male                           36        60.00%          36       45.57%         0.092
                                          Female                         24        40.00%          43       54.43%
 Type of treatment                        SADBE Treatment                32       %3.33%           37       46.84%         0.448
                                          DPCP Treatment                 28        46.67%          42       53.16%
 Disease duration (years)                 Mean±Standard                       3.88±2.63                 4.12±3.01          0.798
                                          Deviation
                                          Median (IQR)                         3 (2-6)                   3 (2-6)
 Nail involvement (due to alopecia        (-)                            16        26.67%          28       35.44%         0.271
 areata)                                  (+)                            44        73.33%          51       64.56%
 Family history of alopecia areata        (-)                            44        73.33%          64       81.01%         0.281
                                          (+)                            16        26.67%          15       18.99%
 Patient’s history of atopy               (-)                            39        65.00%          69       87.34%         0.002
                                          (+)                            21        35.00%          10       12.66%
 Family history of atopy                  (-)                            44        73.33%          69       87.34%         0.036
                                          (+)                            16        26.67%          10       12.66%
 Total IgE (IU/ml)                        Mean±Standard                   491.33±1267.14            126.3±220.89           0.170
                                          Deviation
                                          Median (IQR)                  65.82 (11.97-395.5)              43.32
                                                                                                     (22.11-135.7)
 Atopic Dermatitis                        (-)                            38        63.33%          63       79.75%         0.032
                                          (+)                            22        36.67%          16       20.25%
 SCORAD Score                             Mean±Standard                     45.43±16.61              23.48±13.95           0.0001
                                          Deviation
                                          Median (IQR)                  44.98 (36.58-57.13)       22.20 (12.8-30.55)

DPCP = diphenylcyclopropenone; IQR = interquartile range SADBE = squaric acid dibutylester.



of atopy, the presence of atopy history in the patient, the             In addition, many diseases that accompany alopecia areata
presence of atopic dermatitis in the patient group with inade-      and can determine the prognosis of the disease have been re-
quate response to the treatment were found to be statistically      ported. Considering the accompanying diseases [15] it was
significantly higher than the patient group with adequate re-       determined that the risk of atopic dermatitis increased espe-
sponse to the treatment (P values respectively:
                                  ​​            0.036, 0.002,       cially in patients with alopecia areata younger than 10 years
0.032). In addition, the SCORAD score averages calculated           of age [16]. In addition, treatment options are limited in pedi-
in the patients with atopic dermatitis in the patient group         atric alopecia areata patients due to concerns about treatment
with inadequate response to the treatment were found to be          tolerance. Topical immunotherapy treatments are one of the
statistically significantly higher than the patient group with      most frequently applied treatment methods, especially in treat-
adequate response to the treatment (P 0.0001) (Table 2). Ad-        ment-resistant and severe pediatric alopecia areata cases.
ditionally, photographs of patients with and without atopic             In a study, diseases that may accompany alopecia areata
dermatitis before and after topical immunotherapy treat-            in patients with pediatric alopecia areata were examined, and
ment are shown in Figures 1 and 2. (Figure 1 and Figure 2)          atopic dermatitis was detected in 17.4% of alopecia areata
                                                                    patients and in 2.2% of controls, and it was determined as

Conclusions                                                         the most common disease accompanying pediatric alopecia
                                                                    areata [17]. On the contrary, there is a study in the literature
Alopecia areata is a chronic, autoimmune disease [1,3]. Al-         reporting that no difference was found between the adult and
though alopecia areata can occur at any age, the majority of        pediatric alopecia areata patients and the control group in
cases appear before the age of 40 [14].                             terms of the frequency of atopic disease [18]. We found the



4                                                                        Original Article | Dermatol Pract Concept. 2024;14(1):e2024006
   Figure 1. (A,B) Before (A) and after (B) topical immunotherapy treatment of a patient without atopic dermatitis




  Figure 2. (A,B) Before (A) and after (B) topical immunotherapy treatment of a patient with atopic dermatitis



presence of atopic dermatitis in 27.34% of pediatric alopecia          the presence of nail involvement (due to ­alopecia areata), the
areata patients included in our study. However, since there            presence of a family history of atopy, and the total IgE aver-
was no control group in our study, this value could not be             ages statistically significantly higher in the group of patients
compared with the control group. While Th1 cell-mediated               with alopecia areata with atopic dermatitis compared to the
pathways are thought to be effective in the pathogenesis of            patient group without atopic dermatitis.
alopecia areata, especially Th2 cell-mediated pathways are                 In addition, there are many studies in the literature ex-
thought to be effective in the pathogenesis of atopic derma-           amining the factors affecting the responses obtained with
titis. Recently, it has been shown that Th1 and Th17 cell-­            topical immunotherapy, but the data are conflicting in terms
mediated pathways are also effective in the pathogenesis of            of situations that can predict treatment responses and be
atopic dermatitis, especially in the chronic period. The fre-          used as prognostic factors. In a retrospective study, disease
quently reported association of alopecia areata and atopic             severity, disease duration, atopy history (especially eczema),
dermatitis in the literature can be explained by these overlap-        and early development of contact dermatitis in the area
ping immunological pathways [19]. In many studies in the               where the topical immunotherapy agent applied for sensi-
literature, the relationship between atopy and alopecia areata         tization was applied were identified as the main factors af-
has been examined, but atopic diseases have been customized            fecting treatment responses [21]. In addition, there are very
and their relationship with alopecia areata has not been men-          few studies evaluating the response to topical immunother-
tioned much. Addressing this, one study found that patients            apy treatment, especially in pediatric patients, and examin-
with alopecia areata with atopic dermatitis and/or a family            ing the factors that may affect these treatment responses. In
history of atopic dermatitis were statistically significantly          our study, we investigated the factors that may affect the
more likely to have severe forms of alopecia areata, such as           treatment response in pediatric patients receiving topical im-
alopecia totalis and alopecia universalis, than patients with-         munotherapy treatment. And finally, the presence of atopy
out a history of atopic dermatitis [20]. In our study, we found        in the family, the presence of atopy in the patient, and the



Original Article | Dermatol Pract Concept. 2024;14(1):e2024006                                                                       5
presence of atopic dermatitis were found to be statistically             7. Simakou T, Butcher JP, Reid S, Henriquez FL. Alopecia areata: A
significantly higher in the patient group who responded in-                 multifactorial autoimmune condition. J Autoimmun. 2019;98:74-
                                                                            85. DOI: 10.1016/j.jaut.2018.12.001. PMID: 30558963.
adequately to the treatment. In addition, the SCORAD score
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                                                                            Suchonwanit P. Prevalence and Risk Factors Associated with the
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    In conclusion, with the data we obtained in our study, we
                                                                        11. Barton VR, Toussi A, Awasthi S, Kiuru M. Treatment of pedi-
determined that atopic dermatitis, which is a disease often
                                                                            atric alopecia areata: A systematic review. J Am Acad Derma-
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6                                                                             Original Article | Dermatol Pract Concept. 2024;14(1):e2024006
