Content uploaded by Ariyati Yosi
Author content
All content in this area was uploaded by Ariyati Yosi on Feb 18, 2020
Content may be subject to copyright.
International Journal of Scientific and Research Publications, Volume 10, Issue 1, January 2020 219
ISSN 2250-3153
http://dx.doi.org/10.29322/IJSRP.10.01.2020.p9734 www.ijsrp.org
Differences of Superoxide Dismutase (SOD) Enzyme
Levels Based on the Severity of Androgenetic Alopecia in
Men
Erty W.L Toruan*, Rointan Simanungkalit**, Ariyati Yosi**
*Post graduate of Dermatology and Venereology, Faculty of Medicine, Universitas Sumatera Utara, Medan, Indonesia
**Departement of Dermatology and Venereology, Faculty of Medicine, Universitas Sumatera Utara, Medan, Indonesia
DOI: 10.29322/IJSRP.10.01.2020.p9734
http://dx.doi.org/10.29322/IJSRP.10.01.2020.p9734
Abstract
Introduction: Androgenetic alopecia or male pattern hair loss is
a progressive hair loss caused by genetic and androgenic factors
in hair follicles with characteristic shortening of the anagen
phase, telogen phase elongation, and miniaturization of hair
follicles which causes the hair shaft to grow thinner in each
cycle. Enzyme Superoxide Dismutase (SOD) is one of the body's
antioxidant defense systems. Superoxide Dismutase is important
in almost all cells that are exposed to oxygen, decreased levels or
their activity can cause oxidative stress status of body cells
including hair keratinocytes. The severity of androgenetic
alopecia in men is classified on a Hamilton-Norwood scale
consisting of types I to VII.
Objective: To analyze differences of SOD enzyme levels based
on the severity of androgenetic alopecia in men.
Methods: This study was an observational analytic study with a
cross-sectional design involving 30 men with androgenetic
alopecia who was treated at Departement of Dermatology and
Venereology H. Adam Malik General Hospital Medan. The
severity of androgenetic alopecia of each participant was
classified into mild, moderate and severe based on Hamilton-
Norwood scale and we also performed examination of SOD
level.
Results: There was no significant difference in SOD enzyme
levels based on the severity of androgenetic alopecia in men.
Conclusion: Androgenetic alopecia is baldness which is
influenced by internal factors such as genetic and androgen, and
external factors such as microinflammation. SOD levels are
strongly related to the characteristics of each individual such as
aging and lifestyle.
index term: Alopecia androgenetica, severity, SOD, Hamilton-
Norwood scale
I.INTRODUCTION
Androgenetic alopecia or male pattern hair loss is a
common progressive hair loss caused by genetic and androgenic
factors in hair follicles. Its characteristics are similar in both
sexes characterized by shortening of the anagen phase,
elongation of the telogen phase, and miniaturization of hair
follicles which causes the hair shaft grow thinner in each cycle.1-
3
The severity of androgenetic alopecia in men is
classified with the Hamilton-Norwood scale consist of types I to
VII.1-3According to Colgecen E et al and Abbasi J et al, the
severity can be categorized into mild (I and II), moderate (IIA,
III, IIIA and IV), and severe (IVA, V, VA, VI and VII).4,5
The pathogenesis of androgenetic alopecia in men
influenced by androgen hormon and genetic factors.1,3
Microinflammation also plays a role in the pathogenesis of
androgenetic alopecia in which DHT will increase secretion of
interleukin (IL) -6 and also TGF-β1. Later it will influence
oxidative stress on dermal papilla cells and inhibits proliferation
of hair matrix epithelial. In addition, environmental factors such
as nutrition, metabolic syndrome, smoking and ultraviolet (UV)
radiation also play a role in the pathogenesis of androgenetic
alopecia.6 These environmental factors influence the occurrence
of oxidative stress which in turn causes an increase in free
radicals and reactive oxygen compounds in androgenetic
alopecia.6-8 Oxidative stress is a state of imbalance between the
production of free radicals or reactive oxygen compounds with
antioxidant defense systems in the body.7
International Journal of Scientific and Research Publications, Volume 10, Issue 1, January 2020 220
ISSN 2250-3153
http://dx.doi.org/10.29322/IJSRP.10.01.2020.p9734 www.ijsrp.org
The body's defense system consist of antioxidant
enzymes and non-enzymes. Antioxidant enzymes are Superoxide
Dismutase (SOD) contained in the mitochondria and cytosol,
Glutathione Peroxidase (GPX), lutathionereductase, and catalase
(CAT). Whereas non-enzymatic antioxidant defenses are
micronutrient like β-carotene, vitamin C and vitamin E.7,8 SOD
is an antioxidant enzyme that is important in almost all cells
exposed to oxygen, decreased levels or activity can cause
oxidative stress status of body cells including hair keratinocytes.9
Study of Roshdy OH et al showed that the mean serum SOD
level in patients with androgenetic alopecia was 67.60 ± 12.49 U
/ g Hb, which decreased compared to control 85.60 ± 6.6 U / g
Hb (p <0.001).10 It was supported by study of Amirnia et al. that
examined level of zinc, copper, and SOD, GPX, and
malondialdehyde in androgenetic alopecia, it was found that the
mean serum SOD level in patients with androgenetic alopecia
was 1816.57 ± 98.79 µg / dl which decreased significantly
compared to the control of 2296.77 ± 286.89 µg / dl (p < 0.005).9
Prie BE et al in his study of oxidative stress in androgenetic
alopecia showed that the mean serum level of SOD enzymes in
androgenetic alopecia patients was 441.35 ± 26.83 U / g Hb
while control was 546.85 ± 21.99 U / g Hb (p <0.01).
Nowaday, there is only few literature which discusses
the differences in SOD enzyme level based on the severity of
androgenetic alopecia, so we interested to know about the
difference of serum levels of SOD enzymes based on the severity
of androgenetic alopecia in men.
II. METHOD
This research was conducted from June 2018 to
December 2019. It was an observational analytic study with a
cross-sectional design involving 30 men with androgenetic
alopecia who came to Departement of Dermatology and
Venereology H. Adam Malik General Hospital Medan. Each
participant will sign an informed consent and will undergo
anamnesis, dermatological examination and blood test for SOD
levels. This research was carried out after obtaining permission
from the Research Ethics Commission of the Faculty of
Medicine, Universitas Sumatera Utara and a research permit
from the Directorate of Human Resources and Education of the
Research and Development Installation of H. Adam Malik
General Hospital Medan.
III.RESULTS
A total of 30 subjects, with majority androgenetic
alopecia in the age group of 60-69 years as many as 10 people
(33.3%) while at least in the age group> 70 years (3.3%). From
the above results it can be seen that there is an increase in the
prevalence of androgenetic alopecia with increasing decades of
age, except at> 70 years of age. (table 1)
Table 1 Distribution by age group
Age Group (year)
n
%
30-39
5
16,7
40-49
7
23,3
50-59
7
23,3
60-69
10
33,3
>70
1
3,3
Total
30
100
From all the subjects, majority had family history of
androgenetic alopecia as much as 21 people (70%). (table 2)
Table 2 Distribution by family history
Family history
n
%
Yes
21
70
None
9
30
Total
30
100
Based on our study, the mean of duration of alopecia was 24
months with a minimum value is 6 months and a maximum value
is 72 months. (table 3)
Table 3 Distribution by duration of alopecia
Median (Min-Max)
Alopecia
duration
24 months (6 months-72 months)
Based on table 4, the severity of mild androgenetic alopecia is
predominantly found in the 30-39 years and 40-49 years age
groups with 50% each, for the moderate severity majority in 50-
59 years age group is 60%, and for the severity severe majority
in the 60-69 year age group.
Table 4. The severity of androgenetic alopecia by age group
Age group
severity of androgenetic alopecia
Mild
Moderate
Severe
N
%
n
%
n
%
30-39
5
50
0
0
0
0
40-49
5
50
2
20
0
0
50-59
0
0
6
60
1
10
60-69
0
0
2
20
8
80
>70
0
0
0
0
1
10
Total
10
100
10
100
10
100
International Journal of Scientific and Research Publications, Volume 10, Issue 1, January 2020 221
ISSN 2250-3153
http://dx.doi.org/10.29322/IJSRP.10.01.2020.p9734 www.ijsrp.org
Based on table 5, participant with family history of alopecia,
90% had a moderate severity androgenetic alopecia, while study
subjects who had no family history, 60% had mild androgenetic
alopecia.
Table 5. The severity of androgenetic alopecia by family history
Family
history
Severity of androgenetic alopecia
Mild
Moderate
Severe
N
%
n
%
n
%
Yes
4
40
9
90
8
80
None
6
60
1
10
2
20
Total
10
100
10
100
10
100
Based on table 6 it can be seen that the highest SOD enzyme
levels are at moderate androgenetic alopecia which is 106.51
(0.01-1054.80) U / L and the lowest level at severe androgenetic
alopecia is 24.61 (0.04-595.37) U / L. The results of the kruskal-
wallis test showed the value of p> 0.05 so, there was no
significant difference in SOD levels based on the severity of
androgenetic alopecia in men.
Table 6. The difference of SOD enzyme levels based on the
severity of androgenetic alopecia
Severity of
androgenetic
alopecia
Median (Min-
Max)
U/L
p*
Mild
35,89 (0,03-
401.92)
0,679
Moderate
106,51 (0,01-
1054.80)
Severe
24,61 (0,04-
595,37)
Based on table 7 it can be seen that the highest SOD enzyme
levels are in the 50-59 years age group which is 94.06 (0.01-
492.07) U / L while the lowest levels in the 40-49 years age
group are 9.22 (0 , 05-1054.80) U / L. The results of the kruskal-
wallis test p value> 0.05 so there was no significant difference in
SOD levels based on the age group of androgenetic alopecia in
men.
Table 7. Differences of SOD enzyme levels by age group
Age group
(years)
Median (Min-Max)
U/L
p*
30-39
62,09 (0,03-113,52)
0,783
40-49
9,22 (0,05-1054,80)
50-59
94,06 (0,01-492,07)
60-69
49,82 (0,04-595,37)
>70
62,09
Based on table 8 it can be seen that SOD enzyme levels are
higher in men with a family history of alopecia that is 73.75
(0.02-1054.80) U / L. The results of the kruskal-wallis test
showed p values> 0.05, so there was no significant difference in
SOD levels based on a family history of androgenetic alopecia.
Table 8. Differences of SOD enzyme levels based on family
history
Family
history
Median (Min-Max)
U/L
p*
Yes
73,75 (0,02-1054,80)
0,402
None
9,22 (0,01-595,37)
IV.DISCUSSION
The increasing of androgenetic alopecia prevalence by
decades of age shows a connection between the aging and
microinflammatory processes in androgenetic alopecia. The
accumulation of oxidative stress in aging activates the
inflammatory pathway mediated by IL-1α, IL-6, IL-8, which
causes cellular damage to the hair's peripherals.11
Family history of alopecia has an important role in the onset of
androgenetic alopecia which genetic factors are considered has
role that greatly influences the occurrence of androgenetic
alopecia.The duration of androgenetic alopecia varies depending
on the onset. The onset of androgenetic alopecia usually begins
after puberty and before the age of 40.3 Study of Lee WS showed
there is a link between the history of alopecia in families with
early onset other than that the early onset of androgenetic
alopecia otherwise the early onset will increases the risk more
severe androgenetic alopecia.12
Family history of alopecia has an important role in the
onset of androgenetic alopecia. Genetic factors are considered as
a very influential role in the occurrence of androgenetic
alopecia.12 Polygenic inheritance patterns are considered
important in clinical phenotypes and an increased risk of the
number of family members affected by alopecia.13
According to this study there was no significant
difference in SOD levels based on the severity of androgenetic
alopecia in men. Roshdy et al's study showed there were
differences in SOD levels in androgenetic alopecia patients
compared to controls (67.60 ± 12.49 U / L and 85 ± 6.60 U / L (p
<0.05)).10 Armirnia et al also revealed the same, with a value of
1861.57 ± 98.79 U / L for patients with androgenetic alopecia
and 2290.77 ± 286.89 U / L for control (p <0.005).9 However,
many studies have revealed differences in SOD levels in each
degree of severity of alopecia androgenetics are very limited.
Theoritical, there is no significant differences in SOD
levels were found in each of the severity of androgenetic
International Journal of Scientific and Research Publications, Volume 10, Issue 1, January 2020 222
ISSN 2250-3153
http://dx.doi.org/10.29322/IJSRP.10.01.2020.p9734 www.ijsrp.org
alopecia, could be influenced by several things, like the presence
of oxidative stress factors that can originate from irritants,
pollution, and ultraviolet radiation. In addition, individual
lifestyles can also affect oxidative stress status such as exercise
habits, antioxidant supplementation, and smoking.14-16 The
results of this study can be influenced by several things,
especially the presence of oxidative stress factors that came from
irritants, pollution, and ultraviolet radiation. However, individual
lifestyles can also affect oxidative stress status such as exercise
habits, antioxidant supplementation, and smoking.15-16
V.CONCLUSIONS
Androgenetic alopecia is baldness which is influenced
by internal factors such as genetics and androgens, as well as
external factors such as microinflammation. Genetics play an
important role in the family's history of androgenetic alopecia.
Whereas the SOD level is highly related to the characteristics of
each individual such as aging and lifestyle.
VI. SUGGESTION
This research can be done with a larger sample size and
age distribution in each group that is similar and has no family
history, other than that by minimizing the presence of bias
factors such as smoking and the use of antioxidants.
REFERENCES
1. Otberg N, Shapiro J. Hair growth disorders. Dalam:
Goldsmith LA, Katz SI, Gilchrest BA, Paller AS, Leffell
DJ, Wolff K, editor. Fitzpatrick’s dermatology in general
medicine. Volume 1. Edisi kedelapan. New York: The
McGraw Hill Companies; 2012: 979-1008.
2. Messenger AG. Androgenetic alopecia. Dalam: McMichael
AJ, Hordinsky MK, editor. Hair and scalp diseases:
medical, surgical, and cosmetic treatments. New York:
Informa Healthcare; 2008: 107-18.
3. Arias-Santiago S, Buendía-Eisman A, Gutiérrez-Salmerón
MT, Serrano-Ortega S. Male androgenetic alopecia. Dalam:
Preedy VR, editor. Handbook of hair in health and disease.
Wageningen: Wageningen Academic Publishers; 2012: 99-
116.
4. Colgecen E, Ede H, Erkoc FM, Akyuz Y, Erbay A. The
relation of androgenetic alopecia severity with epicardial fat
thickness. Ann Dermatol. [Internet]. 2016 [Diakses pada
2018 Juni 22]; 28 (2): 205-10. Tersedia di:
http://dx.doi.org/10/5021/ad.2016.28.2.205
DOI:10/5021/ad.2016.28.2.205
5. Abbasi J, Abbasi M, Lee KC, Tan KC, Tan SE, et al. Cap
wearing and quality of life in patients with androgenetic
alopecia amongst Indian population. J Comm Pub Health
Nursing. 2017; 3 (2): 1-10
6. Rajput JR. Role of non androgenic factors in hair loss and
hair regrowth. J Cosmo Trichol. [Internet]. 2017 [Diakses
pada 2018 Juni 21]; 3(2): 118-22. Tersedia di:
https://www.omicsonline.org/open-access/role-of-non-
androgenic-factors-in-hair-loss-and-hair-regrowth-2471-
9323-1000118.pdf
7. Erdogan HK, Bulur I, Kocaturk E, Yildiz B, Saracoglu ZN,
Alatas O. The role of oxidative stress in early-onset
androgenetic alopecia. Journal of Cosmetic Dermatology.
2016; 0: 1-4.
8. Liguori I, Russo G, Curcio F, Bulli G, Aran L, et al.
Oxidative stress, aging, and disease. Dove Press Journal.
[Internet]. 2018 [Diakses pada 2018 Juni 21]; 13: 757-72.
Tersedia di: http://dx.doi.org/10.2147/CIA.S158513
DOI: 10.2147/CIA.S158513
9. Amirnia M, Sinafar S, Sinafar H, Nuri M. Assessment of
zinc and copper contents in scalp hair and serum and
superoxide dismutase, glutathione peroxidase and
malondialdehyde in serum of androgenetic alopecia and
alopecia areata patients. Life Science Journal. [Internet].
2013 [Diakses pada 2018 Juni 21]; 10(1): 204-9. Tersedia
di:
http://www.lifesciencesite.com/lsj/life1001/030_11559life10
01_204_209.pdf
10. Roshdy OH, Mohammad NS, Kamha ES, Omar M. Genetic
analysis of 5 α reductase type II enzyme in relation to
oxidative stress in cases of androgenetic alopecia in a
sample of egyptian population. Our Dermatol Online.
[Internet] 2013 [Diakses pada 2018 Juni 21]; 4(4): 468-74.
Tersedia di:
http://www.odermatol.com/odermatology/42013/5.Genetic-
RoshdyOH.pdf
11. Liguori I, Russo G, Curcio F, Bulli G, Aran L, et al.
Oxidative stress, aging, and disease. Dove Press Journal.
[Internet]. 2018 [Diakses pada 2018 Juni 21]; 13: 757-72.
Tersedia di: http://dx.doi.org/10.2147/CIA.S158513
DOI: 10.2147/CIA.S158513
12. Lee WS, Lee HJ. Characteristics of androgenetic alopecia in
Asian. Ann Dermatol. [Internet]. 2012 [Diakses pada 2018
Juni 19]; 24 (3): 243-52. Tersedia di:
http://dx.doi.org/10.5021/ad/2012.24.3.2443
DOI: 10.5021/ad/2012.24.3.2443
13. Rathnayake D, Sinclair R. Male androgenetic alopecia.
Informa J. [Internet] 2010 [Diakses pada 2019 Desember
11]; 11(8):1295-304. Tersedia di:
https://doi.org/10.1517/14656561003752730
14. Tang PH, Chia HP, Cheong LL, Koh D. A community
study of male androgenetic alopecia in Bishan, Singapore.
International Journal of Scientific and Research Publications, Volume 10, Issue 1, January 2020 223
ISSN 2250-3153
http://dx.doi.org/10.29322/IJSRP.10.01.2020.p9734 www.ijsrp.org
Singapore Med J. [Internet]. 2000 [Diakses pada 2018 Juni
19]; 41: 202-5.Tersedia di:
http://citeseerx.ist.psu.edu/viewdoc/download?doi=10.1.1.5
71.8614&rep=rep1&type=pdf
DOI: 10.1.1.571.8614
15. Legiawati L. Jenis kerontokan rambut dan kebotakan pasien
poliklinik kulit dan kelamin RSUPN DR. Cipto
Mangunkusumo tahun 2009-2011, Jakarta. MDVI.
[Internet]. 2013.[Diakses pada 2018 Juni 20]; 40(4): 159-
63. Tersedia di:
http://www.perdoski.or.id/doc/mdvi/fulltext/34/222/Artikel
_Asli_(2).pdf
16. Osborn, D. Inheritance of baldness. J Heredity. [Internet].
1916 [Diakses pada 2018 Juni 20]; 7, 347-355. Tersedia di:
https://doi.org/10.1093/oxfordjournals.jhered.a110746
DOI: 10.1093/oxfordjournals.jhered.a110746