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Analysis of Microscopic Examination of Pulled Out Hair in Telogen Effluvium Patients

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Background: Telogen effluvium (TE) is characterized by massive hair shedding and results from an abrupt conversion of anagen to telogen. Differentiation of TE with other hair disorders showing massive hair shedding is difficult. Objective: To evaluate the morphologic characteristics of pulled out hair of TE. Methods: We analyzed microscopic examination of pulled out hairs by hair pull test in TE patients, and compared these hairs with pulled out hairs in diffuse alopecia areata (AA) patients and healthy volunteers. Results: Hair microscopic examination in 44 TE patients (370 hairs) and 30 healthy volunteers (295 hairs) were as follows: typical club hair, 32.7%, 62.7%; club hair with tail, 23.5%, 23.7%; club hair with remnant sheath, 23.0%, 6.8%; club hair with both tail and remnant sheath, 18.9%, 5.4%; and unclassified hair, 1.9%, 1.4%. The examination in 7 diffuse AA patients (63 hairs) was as follows: typical club hair, 23.9%; atypical club hair, 47.7%; and distinctive AA hair, 28.4%. There was statistical difference between TE patients and healthy volunteers group (p=0.000). Conclusion: Increased atypical club hair in microscopic hair examination might be characteristics of TE.
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Microscopic Examination of Telogen Effluvium
Vol. 32, No. 2, 2020
141
Received October 21, 2019, Revised November 22, 2019, Accepted for
publication December 7, 2019
Corresponding author: Hyojin Kim, Department of Dermatology, Busan Paik
Hospital, Inje University College of Medicine, 75 Bokji-ro, Busanjin-gu,
Busan 47392, Korea. Tel: 82-51-890-6135, Fax: 82-51-897-6391, E-mail:
derma09@hanmail.net
ORCID: https://orcid.org/0000-0003-0987-4938
T
his is an Open Access article distributed under the terms of the Creative
Commons Attribution Non-Commercial License (http://creativecommons.
org/licenses/by-nc/4.0) which permits unrestricted non-commercial use,
distribution, and reproduction in any medium, provided the original work
is properly cited.
Copyright © The Korean Dermatological Association and The Korean
Society for Investigative Dermatology
pISSN 1013-9087eISSN 2005-3894
Ann Dermatol Vol. 32, No. 2, 2020 https://doi.org/10.5021/ad.2020.32.2.141
ORIGINAL ARTICLE
Analysis of Microscopic Examination of Pulled Out Hair
in Telogen Effluvium Patients
So Hee Park, Jung Eun Seol, Do Hyeong Kim, Hyojin Kim
Department of Dermatology, Busan Paik Hospital, Inje University College of Medicine, Busan, Korea
Background: Telogen effluvium (TE) is characterized by mas-
sive hair shedding and results from an abrupt conversion of
anagen to telogen. Differentiation of TE with other hair dis-
orders showing massive hair shedding is difficult. Objective:
To evaluate the morphologic characteristics of pulled out
hair of TE. Methods: We analyzed microscopic examination
of pulled out hairs by hair pull test in TE patients, and com-
pared these hairs with pulled out hairs in diffuse alopecia
areata (AA) patients and healthy volunteers. Results: Hair mi-
croscopic examination in 44 TE patients (370 hairs) and 30
healthy volunteers (295 hairs) were as follows: typical club
hair, 32.7%, 62.7%; club hair with tail, 23.5%, 23.7%; club
hair with remnant sheath, 23.0%, 6.8%; club hair with both
tail and remnant sheath, 18.9%, 5.4%; and unclassified hair,
1.9%, 1.4%. The examination in 7 diffuse AA patients (63
hairs) was as follows: typical club hair, 23.9%; atypical club
hair, 47.7%; and distinctive AA hair, 28.4%. There was stat-
istical difference between TE patients and healthy volunteers
group (p=0.000). Conclusion: Increased atypical club hair
in microscopic hair examination might be characteristics of
TE. (Ann Dermatol 32(2) 141145, 2020)
-Keywords-
Alopecia, Alopecia areata, Hair
INTRODUCTION
Telogen effluvium (TE) is caused by an abrupt conversion
of anagen hairs to telogen hairs on the scalp irrespective
of the cause1,2. TE is diagnosed quantitatively, and pres-
ents with massive, diffuse hair shedding on scalp (more
than 100 telogen hairs per day)3. It generally occurs about
3 months after a major illness or other stress (surgery, child-
birth, rapid weight loss, nutritional deficiency, high fever
or massive hemorrhage), medication or thyroid dysfunc-
tion2. There are many relevant investigations for diagnosis
of TE, which include hair loss count, hair pull test (HPT),
hair pluck test, unit area trichogram, phototrichogram, his-
topathology, dermatoscopy, and laboratory test (complete
blood count, serum ferritin, serum thyroid stimulating hor-
mone, etc.)1. However, differentiation of TE with other hair
disorders showing massive hair shedding is still difficult.
HPT is quick, noninvasive clinical examinations to mon-
itor hair loss disorders4. To perform this test, the clinician
selects 50 to 60 hairs and holds the bundle close to the
scalp between the thumb, index finger, and long finger5.
The clinician then firmly pulls on the bundle using slow
traction as the fingers slide down the hair shaft5. If more
than 10% of the hairs in each bundle are removed from a
scalp area, the HPT is considered positive6.
There is no investigation about morphologic character-
istics of pulled out hairs in TE patients. Hair shaft micro-
scopic examination is useful diagnostic examination for
hair loss diseases. Characteristics of hair in alopecia areata
(AA) are well-known and helpful for diagnosis. However,
those in TE is not well established. Herein, we inves-
tigated the morphologic characteristics of pulled out hairs
in TE.
SH Park, et al
142
Ann Dermatol
Fig. 2. Distinctive AA hairs include
hair with tapering of proximal hair
shaft (A), hair with breakage of prox-
imal hair shaft (B) and hair with sur-
face undulation (C) (AC: ×40).
Fig. 1. Pulled out hairs were clas-
sified microscopically by morpho-
logy into typical club hair (A), club
hair with tail (B), club hair with rem-
nant sheath (C), and club hair with
both tail and remnant sheath (D) (A
D: ×40).
MATERIALS AND METHODS
This study enrolled TE and diffuse AA patients from June
2013 to July 2015 in the Department of Dermatology in
Busan Paik Hospital. TE met following criteria: (1) history
of increased hair shedding; (2) absence of hair loss patch
at initial and follow up visit; and (3) no past history of AA.
The following criteria were applied to diagnose diffuse
AA: (1) history of increased hair shedding; and (2) absence
of hair loss patches at initial visit with occurrence of them
in follow-up visits. Pulled-out hairs were harvested by gen-
tle hair pulling using thumb and index finger. This was
performed by one investigator.
Healthy volunteers who had neither hair loss disorders
nor scalp disease were enrolled. In our study, around 10
hairs were obtained by gentle hair pulling performed by
each subjects. Microscopic examination of pulled out hair
performed in TE patients, diffuse AA patients and healthy
volunteers. This study was approved by the institutional
review board of the Inje University Busan Paik Hospital
(approval no. 15-0270) and received consent form from all
participants.
Analysis of morphologic characteristics of pulled out hair
was based on classification of hairs into three categories;
typical club hair, atypical club hair and distinctive AA
hair. Typical club hair was defined as bulbous enlarge-
ment of proximal hair root without following feature of
atypical club hair or distinctive AA hair (Fig. 1A). Atypical
club hair was subcategorized into club hair with tail, club
hair with remnant sheath, club hair with both tail and rem-
nant sheath and unclassified hair. Club hair with tail was
defined as typical club hair with linear structure attached
on proximal hair tip. Club hair with remnant sheath was
defined as typical club hair with sheath surrounding prox-
imal hair shaft (Fig. 1BD). Distinctive AA hair was de-
fined as hair with at least one of following characterestics;
tapering of proximal hair shaft, breakage of proximal hair
shaft and hair with surface undulation (Fig. 2).
Morphologic characteristics of pulled out hairs in TE pa-
tients were compared with that of diffuse AA patients and
healthy volunteers. In TE group, further comparative anal-
ysis was performed according to concurrent androgenetic
alopecia (AGA) and degree of shedding based on the num-
ber of pulled out hair (TE10 vs. TE10). Comparison be-
tween initial visit and follow-up visit was also performed.
Pearson’s chi-square test and Fisher’s exact test were used
for statistical analysis of morphologic characteristics of pull-
ed out hairs. Results were considered statistically signifi-
cant at a p0.05.
Microscopic Examination of Telogen Effluvium
Vol. 32, No. 2, 2020
143
Fig. 3. Analysis of morphologic characteristics of pulled out hairs between 3 groups of telogen effluvium patients, diffuse alopecia
areata patients, and healthy volunteers (*p0.05). Distinctive AA hairs were excluded in this analysis. TE: telogen effluvium, AA:
alopecia areata.
Table 1. Demographic and clinical information of telogen effluvium
patients
Characteristic
Subjects (n=44)
n (%) Mean (range)
Sex
Male 3 (6.8)
Female 41 (93.2)
Age 54.4 (982)
Alopecia
TE only 30 (68.2)
TE with AGA 14 (31.8)
Trigger factors of TE
Idiopathic 17 (38.6)
Major illness 11 (25.0)
Drug 7 (15.9)
Emotional stress 4 (9.1)
Weight loss 3 (6.8)
Childbirth 2 (4.6)
TE: telogen effluvium, AGA: androgenetic alopecia.
RESULTS
Demographic and clinical information of subjects
Forty-four TE patients were enrolled in this study (3 males
and 41 females) with a mean age of 54.4 years (range, 9
82). Most common etiology was idiopathic (38.6%), fol-
lowed by major illness (25.0%). Fourteen subjects (31.8%)
had concomitant AGA. The characteristics of TE patients
are shown in Table 1.
There were 7 enrolled patients with diffuse AA (4 males
and 3 females) with a mean age of 39.7 years (range, 5
74) and 30 healthy volunteers (6 males and 24 females)
with a mean age of 45.1 years (range, 2282).
Microscopic examination of pulled-out hair in TE
The results of morphologic evaluation of pulled out hairs
are shown in Fig. 3. A total of 370 hairs in TE patients group
were analyzed (2 to 35 hairs in each patient). Atypical
club hair was 67.3%, and club hair with tail was the most
common. In atypical club hair, club hair with tail occu-
pied highest proportion (23.5%), followed by club hair
with remnant sheath (23.0%), club hair with both tail and
remnant sheath (18.9%), and unclassified hair (1.9%).
In further analysis of TE 10 group, the number of pulled-
out hair was from 11 to 35 (mean 19.6). The percentage of
typical club hair was ranging 18.2%91.7%. However,
there was no significant statistical difference. The distri-
bution of TE according to concurrent AGA was not signifi-
cantly different (Table 2).
There were significance differences in distribution be-
tween pulled out hairs in initial visit and those of follow-
up visits. The rate of typical club hair was higher in those
of follow-up visit. In further analysis conducted on 18 sub-
jects in whom both pulled-out hairs of initial visit and
those of follow visit was obtained, there were statistical
significance and the rate of typical club hair in initial visit
SH Park, et al
144
Ann Dermatol
Table 2. Analysis of morphologic characteristics of pulled out hairs
Variable Shedding
10 (n=33)
Shedding
10 (n=11)
TE without AGA
patients (n=30)
TE with AGA
patients (n=14) Initial visit Follow-up
visits
Typical club hair 54 (35.1) 67 (31.0) 87 (31.1) 34 (37.8) 13 (19.4) 72 (37.7)
Atypical club hair 100 (64.9) 149 (69.0) 193 (68.9) 56 (62.2) 54 (80.6) 119 (62.3)
Statistical analysis* No statistical difference (p=0.413) No statistical difference (p=0.238) Statistical difference (p=0.006)
Typical club hair 54 (35.1) 67 (31.0) 87 (31.1) 34 (37.8) 13 (19.4) 72 (37.7)
Club hair with tail 32 (20.8) 55 (25.5) 65 (23.2) 22 (24.4) 19 (28.4) 46 (24.1)
Club hair with remnant sheath 36 (23.4) 49 (22.7) 68 (24.3) 17 (18.9) 13 (19.4) 44 (23.0)
Club hair with tail and remnant sheath 31 (20.1) 39 (18.1) 54 (19.3) 16 (17.8) 19 (28.4) 26 (13.6)
Unclassified hair 1 (0.6) 6 (2.7) 6 (2.1) 1 (1.1) 3 (4.5) 3 (1.6)
Statistical analysis
No statistical difference (p=0.453) No statistical difference (p=0.679) Statistical difference (p=0.001)
Values are presented as number (%). We divided groups by (1) TE according to degree of shedding, (2) telogen effluvium patients
with and without androgenetic alopecia, and (3) initial visit and those of follow-up visits. Pulled out hairs were evaluated with i)
‘typical club hair’ vs. ‘atypical club hair’, ii) ‘typical club hair’ vs. ‘club hair with tail’ vs. ‘club hair with remnant sheath’ vs. ‘club
hair with tail and remnant sheath’ vs .‘unclassified hair’ respectively. AGA: androgenetic alopecia, TE: telogen effluvium. *The
comparison was analyzed by chi-square analysis. The comparison was analyzed by linear by linear analysis.
was much lower (Table 2).
Microscopic examination of pulled-out hair in diffuse
AA patients and healthy volunteers
In 7 patients diagnosed as diffuse AA (total 63 hairs, 2 to
31 hairs in each patient), atypical club hair was the most
common (47.7%), however distinctive AA hair (28.4%)
was also observed considerably in amount. The distribution
of distinctive AA hair was as follow: tapering of proximal
hair shaft (21.6%), breakage of proximal hair shaft (3.4%)
and hair with surface undulation (3.4%).
In 30 healthy volunteers (total 295 hairs, 8 to 10 in each
subject), typical club hair was the most common (62.7%).
Among atypical club hair, club hair with tail was the most
common in this group.
Comparison of distribution of microscopic examination
in three groups
Mean number of pulled out hair was 8.4, 12.6, 9.8 in TE,
diffuse AA patients and healthy volunteer respectively
(p0.05). Also, we analyzed the distribution of typical
club hair and atypical club hair in three group (distinctive
AA hairs in diffuse AA patients such as ‘dystrophic hair’,
‘dysplastic hair’, and ‘broken hair’ were excluded in this
analysis). There was statistical difference in hair morphol-
ogy among 3 groups in distributions of whole atypical
club hair as well as its subclassification in those of sub-
categorization. Post-hoc comparison between each 2 groups
also showed statistically significant difference with one ex-
ception of distribution of whole atypical club hair be-
tween TE and diffuse AA (Fig. 3).
DISCUSSION
Approximately 86% of scalp hairs are anagen hair, 1% are
catagen hair, and 13% are telogen hair in physiologic con-
ditions1. The anagen phase lasts for 3 to 7 years, and is fol-
lowed by catagen for 2 weeks. In catagen phase, protein
and pigment production is stopped, involution of hair fol-
licles begins, and reorganization of extracellular matrix
occurs7. In telogen phase, hair follicles involute reaching
50% of its anagen size. Hair does not fall out promptly
in telogen phase, but rather stays in hair follicles for a
while7. Recently the term ‘exogen’ has been used to de-
scribe the timing of hair falling. It is suggested that there
will be many processes before hair falling in telogen phase,
such as loss of desmoglein 3 (acting as anchoring protein
of telogen hair)7,8. Morphologically, remaining parts in tel-
ogen phase is a peg of epithelial cells above the resting
dermal papilla7.
Healthy people lose up to 100 hairs a day9. However, in
TE patients, massive shift of anagen to telogen develops
abruptly, and the ratio of anagen to telogen changes to
70:302. TE is characterized by excessive shedding of scalp
hair, sometimes loss of more than 300 hairs per day, al-
though it may occur in AA or other hair loss disease2,3,10,11.
The analysis of this study was based on morphologic
characteristics. Significance of each atypical club hair was
not evident and elucidation of each in hair cycle was not
performed. However based on previous study, when inter-
pretating tail as epithelial column, it could be presumed
that club hair with tail was compatible with late catagen
or early telogen hair according to the length12. As for club
hair with sheath, remnant sheath might be considered as
remaining inner root sheath or outer root sheath of telogen
Microscopic Examination of Telogen Effluvium
Vol. 32, No. 2, 2020
145
hair12. Accordingly, club hair with both tail and sheath
might be in transition from catagen to telogen.
Amount of hair shedding in physiologic state might influ-
enced by intrinsic cohesive force between hair shaft and
surrounding tissue which is determined by stage of hair
cycle and intrinsic characteristics of each individual such
as age, and degree and frequency of exposure of pulling
power, such as hair combing or shampooing6,13-15. In this
study, healthy volunteers showed diverse morphology in
hair microscopic examination, which was not accordant
with our assumption that almost shed hair would be typi-
cal club hair. Club hair with tail was the most common
among atypical club hair. It is probable that subject with
hair loss disease in subclinical stage might be included in
healthy volunteer.
The typical club hair-atypical club hair ratio was reversed
in TE compared with that of healthy volunteer. This result
indicated that alteration of physiologic hair cycle resulting
in qualitative as well as quantitative change. It could be
supported by the distribution of the percentage of typical
club hair in each subject in severe TE and healthy vol-
unteer. In healthy volunteer, subjects with greater than 50%
in typical club hair ratio was 21 out of 30 (20%100%),
whereas in 11 subjects in TE 10 group, only one showed
greater than 50% in typical club hair ratio (8.3%81.8%).
These results might suggest that TE is related to discor-
dance with surrounding tissue resulting morphologic change
as well as changes in duration of hair cycle. Distribution
in atypical club hair was also changed; increased club hair
with remnant sheath and club hair with both tail and
sheath. Although TE with concurrent AGA was not sig-
nificantly different from TE without AGA in this study, fur-
ther evaluation might be necessary considering TE results
from diverse pathogenesis. In addition, increased in the
rate of typical club hair in follow-up visit compared with
those in initial visit might suggest reversal of the rate of
typical club hair could be early change in recovery of TE
followed by cessation of hair shedding.
This study is significant in that it identified the qualitative
changes of pulled out hair in TE, which might be applied
in diagnosing TE directly instead of diagnosis by exclusion
of other causes of increased hair shedding. Morphologic
evaluation of pulled out hairs might be helpful in diagnos-
ing TE. Further research on the hair cycling and shed hair
morphology in physiologic state, and interpretation of each
morphology will be necessary. Lack of standardization in
shampooing schedule of subject and pulling power in
healthy volunteer could be limitation.
CONFLICTS OF INTEREST
The authors have nothing to disclose.
ORCID
So Hee Park, https://orcid.org/0000-0002-9600-799X
Jung Eun Seol, https://orcid.org/0000-0002-3029-9635
Do Hyeong Kim, https://orcid.org/0000-0001-6148-8810
Hyojin Kim, https://orcid.org/0000-0003-0987-4938
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... Over the past several years, a few studies have been performed on the microscopic morphology of pulled-out hair of patients with AA and showed characteristic changes compared with those of the healthy controls 3,4 . Our previous data revealed that the morphology of pulled-out hair in diffuse AA showed distinct findings compared with those of telogen effluvium and healthy controls 5 . ...
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