10.5826/dpc.1302a81
Introduction: Hair loss is one of the most common disorders after coronavirus disease 2019 (COVID-19) infection. This study aimed to investigate the relationship between COVID-19-related hair loss and antinuclear antibody (ANA) positivity and patterns.
Methods: ANA positivity and patterns were analyzed in 30 female COVID-19 patients with hair loss complaints and compared in terms of the presence of autoimmunity between patients with and without COVID-19 exhibiting hair loss.
Results: ANA positivity and cytoplasmic patterns were detected in 40% of the patients with COVID-19 infection and hair loss. Trichodynia and diffuse hair loss were observed in 63.3% and 53.3%, respectively.
Conclusions: In patients with COVID-19-related hair loss, diffuse hair loss and ANA positivity may be related to the high antibody levels triggered by COVID-19 infection.
text/xml
2160-9381
2641
en
Ayşe Esra Koku Aksu
https://creativecommons.org/licenses/by-nc/4.0
Dermatology Practical & Conceptual
Trichodynia
Antinuclear Antibody Positivity in Patients With Hair Loss After COVID-19 Infection
Text.Serial.Journal
https://dpcj.org/index.php/dpc
Original Article
2023-04-29
2022-06-09
2023-04-29
2023-05-31
e2023081
Dermatol Pract Concept
Introduction: Hair loss is one of the most common disorders after coronavirus disease 2019 (COVID-19) infection. This study aimed to investigate the relationship between COVID-19-related hair loss and antinuclear antibody (ANA) positivity and patterns.
Methods: ANA positivity and patterns were analyzed in 30 female COVID-19 patients with hair loss complaints and compared in terms of the presence of autoimmunity between patients with and without COVID-19 exhibiting hair loss.
Results: ANA positivity and cytoplasmic patterns were detected in 40% of the patients with COVID-19 infection and hair loss. Trichodynia and diffuse hair loss were observed in 63.3% and 53.3%, respectively.
Conclusions: In patients with COVID-19-related hair loss, diffuse hair loss and ANA positivity may be related to the high antibody levels triggered by COVID-19 infection.
Ayşe Esra Koku Aksu
2023/04/29
10.5826/dpc.1302a81
e2023081
Department of Dermatology, University of Health Sciences, İstanbul Training and Research Hospital, İstanbul, Turkey
2160-9381
Trichodynia
en
e2023081
Di Landro A, Naldi L, Glaser E, Paus R, Tosti A. Pathobiology questions raised by telogen effluvium and trichodynia in COVID-19 patients. Exp Dermatol. 2021;30(7):999-1000. DOI: 10.1111/exd.14352. PMID: 33838048. PMCID: PMC8250761.
Antinuclear Antibody Positivity in Patients With Hair Loss After COVID-19 Infection
https://dpcj.org/index.php/dpc/article/download/2641/2070
      Antinuclear Antibody Positivity in Patients With
            Hair Loss After COVID-19 Infection
                             Vildan Manav1,2, Duygu Erdil1, Ayşe Esra Koku Aksu1


1 Department of Dermatology, University of Health Sciences, İstanbul Training and Research Hospital, İstanbul, Turkey
2 Cosmetology, İstanbul University Graduate School of Medicine, İstanbul, Turkey



Key words: SARS-CoV-19, hair loss, antinuclear antibody positivity, trichodynia
Citation: Manav V, Erdil D, Koku Aksu A. Antinuclear Antibody Positivity in Patients with Hair Loss after COVID-19 Infection. Dermatol
Pract Concept. 2023;13(2):e2023081. DOI: https://doi.org/10.5826/dpc.1302a81
Accepted: August 29, 2022; Published: April 2023
Copyright: ©2023 Manav 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: Vildan Manav, MD, Istanbul Training and Research Hospital, Department of Dermatology, Kasap İlyas Mah.
Org. Abdurrahman Nafiz Gürman Cd. PK: 34098, Istanbul, Turkey. Phone: +905334323524. Fax: +9002126320060,
E-mail: drvildanmanav@gmail.com




  ABSTRACT             Introduction: Hair loss is one of the most common disorders after coronavirus disease 2019
                       (COVID-19) infection. This study aimed to investigate the relationship between COVID-19-related
                       hair loss and antinuclear antibody (ANA) positivity and patterns.
                       Methods: ANA positivity and patterns were analyzed in 30 female COVID-19 patients with hair
                       loss complaints and compared in terms of the presence of autoimmunity between patients with and
                       ­without COVID-19 exhibiting hair loss.
                       Results: ANA positivity and cytoplasmic patterns were detected in 40% of the patients with
                       COVID-19 infection and hair loss. Trichodynia and diffuse hair loss were observed in 63.3% and
                       53.3%, ­respectively.
                       Conclusions: In patients with COVID-19-related hair loss, diffuse hair loss and ANA positivity may
                       be related to the high antibody levels triggered by COVID-19 infection.




Introduction                                                             2019 [1]. It has been reported that 80% of patients with
                                                                         COVID-19 infection develop one or more long-term symp-
More than 175 million people were infected with c­ oronavirus            toms. The most common symptoms are fatigue (58%), head-
disease 2019 (COVID-19) within one year of the first                     ache (44%), attention deficit (24%), and hair loss (25%) [2].
COVID-19 infection reported in China in early December                   Skin findings have received increasing attention for the early



Original Article | Dermatol Pract Concept. 2023;13(2):e2023081                                                                       1
diagnosis of COVID-19. COVID-19-related skin findings in-            collected. Hair loss was recorded using the hair-shedding
clude vascular eruptions, maculopapular eruptions ­(atypical         ­visual scale [12] as follows: < 50, 50–100, 100–150, and >
forms of pityriasis rosea) [3], urticarial rash, v­esicular,         150 hairs/day. Additionally, a pull test was performed at four
petechiae/purpuric eruptions, erythema multiforme–like
­                                                                    locations on the scalp. The pull test was considered posi-
rash, palmar erythema, perifollicular eruption, pruritus,            tive when more than 10% of the hair at each location was
­mucosal rash, and androgenetic alopecia [4].                        ­removed after applying steady traction.
    Autoimmune diseases that develop or worsen after                     Chemiluminescence enzyme immunoassays were per-
COVID-19 infection have also been increasingly reported.             formed to measure vitamin B12 and ferritin levels using an Im-
These include connective tissue diseases (rheumatoid arthri-         munity 2000 device (Diagnostic Products Corporation). TSH
tis, systemic lupus erythematosus vasculitis, myositis, sys-         (thyroid stimulating hormone) and anti-TPO (anti-thyroid
temic sclerosis, and psoriatic arthritis) [5], multiple sclerosis,   peroxidase) levels were measured using an ­
                                                                                                               ARCHITECT
and autoimmune hepatitis [6] in adults, as well as rheumatic         ci16200 Integrated System (Abbot Diagnostics).
diseases [7,8] and type 1 diabetes in children [9].                       Antinuclear antibody titers and patterns were studied
    Antinuclear antibody (ANA) tests were mainly developed           using enzyme-linked immunosorbent assays and immunoflu-
for systemic lupus erythematosus screening. However, ANA             orescence, with human epithelioma type 2 (HEp-2) cells used
positivity has also been detected in many rheumatic diseases         as the substrate. The ANA tests were first run at titers of
and is an indicator of autoimmunity [10]. ANA positivity is          1:100 with both kits, and positive samples were reanalyzed
not expected in non-scarring hair loss. In only one study, the       with further serial dilutions (1:160, 1:320, 1:640, 1:1280,
rate of ANA positivity was reported in patients with pattern         1:2560, and 1:5120). C3 and C4 levels were measured using
hair loss (30.4%) [11].                                              a Behring nephelometer and Beckman Reagent kits.
                                                                         This study was approved by the tertiary hospital ethics
                                                                     committee (No. 2939; October 8, 2021). Written informed
Objectives
                                                                     consent was obtained from all participants.
Since COVID-19 can trigger autoimmunity, and as hair loss
is one of the most common symptoms after COVID-19 infec-             Statistical Analysis
tion, this study aimed to evaluate the relationship between the      Statistical analyses were performed using SPSS version 25.0
two and investigate the differences between autoimmunity-            (IBM). Histograms and the Kolmogorov–Smirnov test were
and non-autoimmunity-related hair loss.                              used to assess data normality. In descriptive analyses, means
                                                                     ± standard deviations and medians were used. Categorical
Methods                                                              variables were compared using Pearson chi-squared test. The
                                                                     Mann–Whitney U test was used to evaluate non-normally
This cross-sectional case-control study was performed                distributed (nonparametric) variables between the case and
­between June and September 2021. The case group con-                control groups, and the Kruskal–Wallis test was used for
sisted of 30 patients who had contracted COVID-19 up to              comparisons between more than two variables. Spearman
12 weeks previously and had hair loss complaints. The con-           correlation coefficient was used to investigate correlations
trol group consisted of 60 patients who complained about             between variables. The ability of C3 and C4 values to predict
hair loss but did not have COVID-19. For the control group,          ANA positivity was investigated using receiver operating
each patient consisted of 2 consecutive patients who came            characteristic (ROC) curves. Values of P < 0.05 were consid-
to the dermatology outpatient clinic immediately after the           ered statistically significant.
patient selected for COVID-19- related hair loss.
    Patients under the age of 18 years, patients with ­autoimmune
                                                                     Results
or inflammatory diseases or acute or chronic infections, pa-
tients receiving any medications (­corticosteroids, biological       The mean ages of the patients in the case and control groups
agents, antibiotics, or vitamin or mineral s­upplements), and        were 30.0 ± 11.2 and 29.2 ± 8.3 years, respectively. The
pregnant or lactating women were excluded from the study.            difference was not statistically significant (P = 0.952). All
COVID-19 infection was confirmed using nasopharyngeal                ­patients were female.
swabs and polymerase chain reaction tests.                               There were no statistically significant differences in
    Demographic characteristics (age and gender) and clinical        standard laboratory test values between the two groups
findings (date of COVID-19 infection, duration of hair loss          (Table 1). Conversely, the duration of hair loss was signifi-
after COVID-19 infection (time from hair loss onset to pre-          cantly longer in the control group than in the case group
sentation to the clinic), severity of hair loss, and presence of     (P < 0.001). In the case group, hair loss started 5.2 ± 3.4 weeks
trichodynia, oily scalp, dandruff, and diffuse hair loss) were       after COVID-19 infection.



2                                                                        Original Article | Dermatol Pract Concept. 2023;13(2):e2023081
    Table 1. Comparison of standard laboratory test values of patients with covid-related hair loss
                                and without covid-related hair loss.
                           Covid-related hair loss
                                   group                            Control                            Total
                           Mean       SD        Medin      Mean       SD       Median     Mean         SD      Median        Pa
 Age (years)               30.03    ±11.22      27.00       29.15    ±8.32      27.00      29.44     ±9.33      27.00      0.952
 Duration of hair          13.87     ±7.54      12.00       20.50    ±6.47      20.00      18.29     ±7.49      20.00     <0.001
 loss (weeks)
 Vitamin                295.83     ±125.18      280.50     300.13   ±117.86    279.00     298.70 ±119.66       279.50      0.911
 B12(ng/L)
 Ferritin (μgr/L)          36.35    ±28.63      32.60       33.33   ±32.62      25.47      34.34    ±31.22      26.38      0.419
 C3(g/L)                   1.27      ±0.27       1.26       1.23     ±0.30       1.26      1.24      ±0.29       1.26      0.945
 C4(g/L)                   0.64      ±2,20       0.25       0.29     ±0.19       0.26      0.41      ±1.28       0.25      0.566
 TSH (mU/L)                2.65      ±2.36       1.98       2.12     ±0.97       2.04      2.30      ±1.58       2.04      0.939

SD = standard deviation.
a
 Mann Whitney U Test




    The rate of patients in the case group losing more than
                                                                    Conclusions
100 hairs per day was 86%, whereas the corresponding rate
in the control group was only 26% (P < 0.001). Trichodynia,         ANA positivity is detected in many viral and autoimmune
oily scalp, and diffuse hair loss were significantly more com-      diseases. However, studies on antibody responses after
mon in the case group than in the control group (­Table 2).         COVID-19 infection have not produced definitive results
Moreover, the case group had a significantly higher number          [13,14]. It remains unclear whether hair loss after COVID-19
of ANA-positive patients (40.0%) than the control group             infection is caused by the infection itself, the autoimmune re-
(11.6%) (P = 0.002). The rate of cytoplasmic ANA patterns           sponse to the infection, or stress triggered by the COVID-19
in the case group was 83%, which was significantly higher           pandemic. To our knowledge, the relationship between
than that in the control group (P = 0.001). In the control          COVID-19-related ANA positivity and hair loss developing
group, granular ANA patterns represented 71.4% of the               after the infection has not been previously investigated.
patients. There was no significant relationship between                In this study, we detected ANA positivity in 40% of pa-
ANA patterns and the severity of hair loss in the case group        tients exhibiting hair loss after COVID-19 infection. This
(Table 3).                                                          is consistent with previous studies reporting rates ranging
    The relationships between ANA positivity and clinical           from 21% to 64% [15-20]. Nevertheless, it is important
findings are shown in Table 4. In the covid-related hair            to note that all COVID-19 patients in those studies had
loss group, the relationship between ANA positivity and             severe or moderate COVID-19, whereas the patients in-
trichodynia, duration of hair loss (week), oilyscalp, dan-          cluded in our study had mild COVID-19 and did not require
druff, diffuse loss of hair volume, pull test was investigated.     hospitalization.
Accordingly, in the covid-related hair loss group, all ANA             The rate of ANA positivity observed in this study is also
positive patients had diffuse hair loss (12/12) whereas only        in line with studies on hair diseases triggering stronger au-
%22 of ANA negative patients (4/18) had diffuse hair loss           toimmunity. Such studies have reported rates of 21.2% in
and pull test positivity were statistically significantly higher    telogen effluvium [21], 30.4% in pattern hair loss [11], and
in patients with ANA positivity.In the case group, there            46% in lichen planopilaris [22].
were no significant relationships between ANA positivity               Surprisingly, in this study, cytoplasmic ANA patterns
and pattern or trichodynia (P = 0.279 and P = 0.670, re-            were observed in 83.3% of the patients with hair loss af-
spectively). Likewise, there was no significant correlation         ter COVID-19 infection. Trachtenberg et al., who reported
between hair loss duration and ANA positivity (r = −0.012,          64% ANA positivity, found a highly dense and fine-speckled
P = 0.949).                                                         cytoplasmic pattern associated with COVID-19 worsening
    No significant relationships were observed between ANA          clinical severity scores [20]. However, as previously noted,
positivity and C3 or C4 levels in the case group (P = 0.735         all patients with hair loss in our study had mild COVID-19.
and P = 0.566, respectively). Furthermore, the ROC analysis            Chang et al detected cytoplasmic patterns at titers
indicated no significant cut-off values.                            higher than 1:160 [23], whereas in this study, we observed



Original Article | Dermatol Pract Concept. 2023;13(2):e2023081                                                                    3
    Table 2. Comparison of clinical examination and laboratory findings of patients with covid-related
                              hair loss and without covid-related hair loss.
                                                             Covid-related hair
                                                                loss group                 Control                Total
                                                                   N (%)                    N (%)                N (%)            Pa
 Pre-exisiting TE             No                                 20 (66.67)               41 (68.33)           61 (67.78)        0.873
                              Yes                                10 (33.33)               19 (31.67)           29 (32.22)
 Amount of hair loss          50hairs/day                         0 (0.00)                 5 (8.33)             5 (5.56)       <0.001
                              50-100hairs/day                    4 (13.33)                39 (65.00)           43 (47.78)
                              100-150hairs/day                   24 (80.00)               16 (26.67)           40 (44.44)
                              >150hairs/day                       2 (6.67)                 0 (0.00)             2 (2.22)
 Trichodynia                  No                                 11 (36.67)               42 (70.00)           53 (58.89)        0.002
                              Yes                                19 (63.33)               18 (30.00)           37 (41.11)
 Oilyscalp                    No                                 15 (50.00)               44 (73.33)           59 (65.56)        0.028
                              Yes                                15 (50.00)               16 (26.67)           31 (34.44)
 Dandruff                     No                                 11 (36.67)               35 (58.33)           46 (51.11)        0.053
                              Yes                                19 (63.33)               25 (41.67)           44 (48.89)
 Diffuse loss of hair         No                                 14 (46.67)               45 (75.00)           59 (65.56)        0.008
 volume                       Yes                                16 (53.33)               15 (25.00)           31 (34.44)
 Pull test                    Negative                           9 (30.00)                15 (25.00)           24 (26.67)        0.613
                              Positive                           21 (70.00)               45 (75.00)           66 (73.33)
 ANA positivity               Negative                           18 (60.00)               53 (88.33)           71 (78.89)        0.002
                              Positive                           12 (40.00)                7 (11.67)           19 (21.11)
 ANA pattern                  Cytoplasmic                        10 (83.33)                0 (0.00)            10 (52.63)        0.001
                              Granular                            0 (0.00)                 5 (71.43)            5 (26.32)
                              Nucleolar                           1 (8.33)                 0 (0.00)             1 (5.26)
                              Nuclear/Granular                    1 (8.33)                 2 (28.57)            3 (15.79)
 AntiTPO μL                   <9                                 29 (96.67)               57 (95.00)           86 (95.56)        0.718
                              >9                                  1 (3.33)                 3 (5.00)             4 (4.44)

ANA = antinuclear antibody; Anti-TPO = anti-thyroid peroxidase; TE = Telogen Effluvium
a
 Chi-Square Test




    Table 3. The relationship between the antinuclear antibody pattern and the amount of hair loss in
                               patients in the covid-related hair loss group.
                                                                        Amount of hair loss
                                                                   50-100                 100-150                > 150
                                              50 hairs/day        hairs/day              hairs/day             hairs/day
     Covid- related hair loss group              N (%)              N (%)                  N (%)                 N (%)             P
 ANA positivity         Negative                  0(.00)            3(75.00)               14(58.33)             1(50.00)        0.784
                        Positive                  0(00)             1(25.00)               10(41.67)             1(50.00)
 ANA pattern            Cytoplasmic               0(00)             1(10.00)               9(90.00)                0(.00)        0.016
                        Granular                  0(00)              0(.00)                  0(.00)                0(.00)
                        Nucleolar                 0(00)              0(.00)                1(10.00)                0(.00)
                        Nuclear/Granular          0(00)              0(.00)                  0(.00)              1(100.00)

ANA = antinuclear antibody




4                                                                          Original Article | Dermatol Pract Concept. 2023;13(2):e2023081
    Table 4. The relationship between antinuclear antibody positivity and clinical findings in patients in
                                    the covid-related hair loss group.
                                                                                       ANA
                                                                       Negative                   Positive
                                                                         N (%)                      N (%)                  Pa
    Trichodynia                                      No                 8 (44.44)                 3 (25.00)              0.279
                                                     Yes               10 (55.56)                 9 (75.00)
    Duration of hair loss (weeks), mean ± SD                           12.89±6.48               15.33±9.00               0.520b
    Oilyscalp                                        No                 9 (50.00)                 6 (50.00)              1.000
                                                     Yes                9 (50.00)                 6 (50.00)
    Dandruff                                         No                 5 (27.78)                 6 (50.00)              0.216
                                                     Yes               13 (72.22)                 6 (50.00)
    Diffuse loss of hair volume                      No                14 (77.78)                  0 (0.00)             <0.001
                                                     Yes                4 (22.22)               12 (100.00)
    Pull test                                        Negative           8 (44.44)                  1 (8.33)              0.034
                                                     Positive          10 (55.56)                 11 (91.67)
a
 Chi-Square Test; bMann Whitney U Test
ANA = antinuclear antibody.



cytoplasmic patterns even at a titer of 1:100. Further-           ANA positivity and trichodynia or between trichodynia
more, nucleolar patterns have been shown to be dominant           and autoimmunity.
in COVID-19 [15,17,18,23]. Thus, our results differ from             Since no financial support is received, ENA ­(extractable nu-
those of previous studies in this respect. Massabki et al [24]    clear antigen) (anti-RNP, anti-Scl70, anti-Sm, ­anti-SS-A/Ro52,
and Eystathioy et al [25] suggested that cytoplasmic patterns     anti-SS-A/Ro60, or anti-SS-B/La), p-ANCA (­perinuclear
at low and moderate titers had low clinical relevance. Con-       anti-neutrophil cytoplasmic antibodies), anticardiolipin
                                                                  ­
versely, Pazini et al reported that they were associated with     IGM, and IGG, which are frequently measured in COVID-19
autoimmune diseases even at low titers [26]. In our study, the    antibody studies, were not measured and were performed.
cytoplasmic pattern of ANA was positive even at low titer,        scalp biopsies. Moreover, we did not evaluate patients stress
but it was also clinically significant.                           levels using an anxiety scale to investigate the relationship
      Trichodynia is a symptom of local paresthesia often         between hair loss and stress.
associated with telogen effluvium, androgenetic alopecia,            In conclusion, hair loss after COVID-19 infection may
and alopecia areata [27,28]. It is a crucial dermatological       be triggered by the release of autoantibodies in response to
marker of the severity of hair disease and the response to        the infection. Cytoplasmic ANA patterns may be essential
treatment [29]. The pathophysiology of trichodynia is un-         clinical markers for elucidating the pathogenesis of hair loss
clear, although substance P, a stress-related neuronal peptide,   after COVID-19 infection.
has been suggested to elicit the sensation [28]. According to
previous studies, the rates of coexistence between telogen ef-
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Original Article | Dermatol Pract Concept. 2023;13(2):e2023081                                                                         7
