Generic selectors
Exact matches only
Search in title
Search in content
Post Type Selectors
Filter by Categories
15th National Conference of the IAOMFP, Chennai, 2006
Abstract
Abstracts from current literature
Acne in India: Guidelines for management - IAA Consensus Document
Addendum
Announcement
Art & Psychiatry
Article
Articles
Association Activities
Association Notes
Award Article
Book Review
Brief Report
Case Analysis
Case Letter
Case Letters
Case Notes
Case Report
Case Reports
Clinical and Laboratory Investigations
Clinical Article
Clinical Studies
Clinical Study
Commentary
Conference Oration
Conference Summary
Continuing Medical Education
Correspondence
Corrigendum
Cosmetic Dermatology
Cosmetology
Current Best Evidence
Current Issue
Current View
Derma Quest
Dermato Surgery
Dermatopathology
Dermatosurgery Specials
Dispensing Pearl
Do you know?
Drug Dialogues
e-IJDVL
Editor Speaks
Editorial
Editorial Remarks
Editorial Report
Editorial Report - 2007
Editorial report for 2004-2005
Errata
Erratum
Focus
Fourth All India Conference Programme
From Our Book Shelf
From the Desk of Chief Editor
General
Get Set for Net
Get set for the net
Guest Article
Guest Editorial
History
How I Manage?
IADVL Announcement
IADVL Announcements
IJDVL Awards
IJDVL AWARDS 2015
IJDVL Awards 2018
IJDVL Awards 2019
IJDVL Awards 2020
IJDVL International Awards 2018
Images in Clinical Practice
In Memorium
Inaugural Address
Index
Knowledge From World Contemporaries
Leprosy Section
Letter in Response to Previous Publication
Letter to Editor
Letter to the Editor
Letter to the Editor - Case Letter
Letter to the Editor - Letter in Response to Published Article
LETTER TO THE EDITOR - LETTERS IN RESPONSE TO PUBLISHED ARTICLES
Letter to the Editor - Observation Letter
Letter to the Editor - Study Letter
Letter to the Editor - Therapy Letter
Letter to the Editor: Articles in Response to Previously Published Articles
Letters in Response to Previous Publication
Letters to the Editor
Letters to the Editor - Letter in Response to Previously Published Articles
Letters to the Editor: Case Letters
Letters to the Editor: Letters in Response to Previously Published Articles
Medicolegal Window
Messages
Miscellaneous Letter
Musings
Net Case
Net case report
Net Image
Net Letter
Net Quiz
Net Study
New Preparations
News
News & Views
Obituary
Observation Letter
Observation Letters
Oration
Original Article
ORIGINAL CONTRIBUTION
Original Contributions
Pattern of Skin Diseases
Pearls
Pediatric Dermatology
Pediatric Rounds
Perspective
Presedential Address
Presidential Address
Presidents Remarks
Quiz
Recommendations
Regret
Report
Report of chief editor
Report of Hon : Treasurer IADVL
Report of Hon. General Secretary IADVL
Research Methdology
Research Methodology
Resident page
Resident's Page
Resident’s Page
Residents' Corner
Residents' Corner
Residents' Page
Retraction
Review
Review Article
Review Articles
Revision Corner
Self Assessment Programme
SEMINAR
Seminar: Chronic Arsenicosis in India
Seminar: HIV Infection
Short Communication
Short Communications
Short Report
Snippets
Special Article
Specialty Interface
Studies
Study Letter
Study Letters
Supplement-Photoprotection
Supplement-Psoriasis
Symposium - Contact Dermatitis
Symposium - Lasers
Symposium - Pediatric Dermatoses
Symposium - Psoriasis
Symposium - Vesicobullous Disorders
SYMPOSIUM - VITILIGO
Symposium Aesthetic Surgery
Symposium Dermatopathology
Symposium-Hair Disorders
Symposium-Nails Part I
Symposium-Nails-Part II
Systematic Review and Meta-Analysis
Systematic Reviews and Meta-analyses
Systematic Reviews and Meta-analysis
Tables
Technology
Therapeutic Guideline-IADVL
Therapeutic Guidelines
Therapeutic Guidelines - IADVL
Therapeutics
Therapy
Therapy Letter
Therapy Letters
View Point
Viewpoint
What’s new in Dermatology
View/Download PDF

Translate this page into:

Brief Report
ARTICLE IN PRESS
doi:
10.25259/IJDVL_228_20

Oxidative stress and antioxidant markers in patients with alopecia areata: A comparative cross-sectional study

Department of Dermatology, Imam Khomeini Hospital, Tehran, Iran
Endocrinology and Metabolism Research Center (EMRC), Vali-Asr Hospital, Tehran, Iran
Dermatology, Razi Hospital, Tehran University of Medical Sciences (TUMS), Tehran, Iran
Corresponding author: Dr. Safoura Shakoei, Department of Dermatology, Imam Khomeini Hospital, Tehran University of Medical Sciences (TUMS), Tehran, Iran. dr.shakoei@gmail.com
Licence
This is an open-access article distributed under the terms of the Creative Commons Attribution-Non Commercial-Share Alike 4.0 License, which allows others to remix, transform, and build upon the work non-commercially, as long as the author is credited and the new creations are licensed under the identical terms.

How to cite this article: Shakoei S, Mirmiranpoor H, Nakhjavani M, Nasimi M, Bakhshi G, Azizpour A. Oxidative stress and antioxidant markers in patients with alopecia areata: A comparative cross-sectional study. Indian J Dermatol Venereol Leprol 2022 doi: 10.25259/IJDVL_228_20

Abstract

Background

Alopecia areata is a chronic inflammatory skin disease. Oxidative stress may contribute to the pathogenesis of this condition.

Aim

To evaluate the serum oxidative stress markers and antioxidant capacity in patients with alopecia areata.

Methods

This cross-sectional study was performed on 40 patients with alopecia areata and 40 healthy controls. The fasting blood sugar, C-reactive protein, lipid profile, and serum oxidative markers, including advanced glycation end products and advanced oxidation protein products, were measured in this study. Also, antioxidant enzymes, including paraoxonase-1, lecithin-cholesterol acyltransferase and serum ferric-reducing antioxidant power, were determined.

Results

The serum levels of advanced glycation end products and advanced oxidation protein products were significantly higher in patients with alopecia areata, compared to the controls (P < 0.001), whereas the levels of ferric-reducing antioxidant power, paraoxonase-1 and lecithin-cholesterol acyltransferase were significantly lower in patients with alopecia areata, compared to the controls (P < 0.001). The mean fasting blood sugar level was significantly higher in patients with alopecia areata, compared to the controls. The ferric reducing antioxidant power level was significantly associated with the percentage of hair loss (P = 0.01, r = 0.4) and the serum C-reactive protein level (P = 0.03, r = -0.3) in patients with alopecia areata.

Limitations

Since the current study had a cross-sectional design, no cause-effect relationship was established between alopecia areata and oxidative stress. The sample size of our study was also small.

Conclusion

Based on the present results, the oxidant-antioxidant enzymatic system is impaired in alopecia areata due to the increased oxidative products and decreased antioxidant activity.

Keywords

Alopecia areata
advanced glycation end product
lecithin-cholesterol acyltransferase
oxidative stress
PON1

Plain Language Summary

Alopecia areata (AA) is a chronic inflammatory disease. Oxidative stress may contribute to the pathogenesis of this condition. So, we evaluated the serum oxidative stress markers and antioxidant capacity in patients with alopecia areata. This cross-sectional study was performed on 40 patients with alopecia areata and 40 healthy controls. Serum oxidative markers, including advanced glycation end products (AGEs) and advanced oxidation protein products (AOPPs), were measured. Paraoxonase-1 (PON1), lecithin-cholesterol acyltransferase (LCAT) and serum ferric-reducing antioxidant power (FRAP) were determined for antioxidant enzymes in our study. The serum levels of AGEs and AOPPs were significantly higher in patients with alopecia areata, compared to the controls (P < 0.001), whereas the levels of FRAP, PON1, and LCAT were significantly lower in patients with alopecia areata (P < 0.001). According to the results of this study, the oxidant-antioxidant enzymatic system is impaired in alopecia areata due to the increased oxidative products and decreased antioxidant activity.

Introduction

Alopecia areata is a common autoimmune skin disorder, with an overall pooled prevalence of 2.11%.1,2 Infiltration of T-cell lymphocytes around the hair follicles during the anagen phase plays a pivotal role in this disorder.3 Other triggering factors, including oxidative stress and genetics are also associated with the development of alopecia areata.4,5 It is known that the skin is continuously exposed to reactive oxygen species, generated by both endogenous and exogenous sources. A balance between oxidative damage and antioxidant protection is necessary for different biological processes.6 Also, reactive oxygen species plays a key role in apoptosis for reacting with all macromolecules (e.g., lipids, proteins, and carbohydrates) on the cell membrane.7

Paraoxonase-1 and lecithin-cholesterol acyltransferase are enzymes with antioxidant activities.8-10 The ferric reducing antioxidant power assay is used to measure the antioxidant potential of body samples.11 Also, advanced glycation end products are glycated proteins that lead to the formation of reactive oxygen species through interactions with advanced glycation end product-specific receptors and result in increased oxidative stress.12 On the other hand, advanced oxidation protein products are oxidized protein products, with a similar structure and biological activity to advanced glycation end products formed during oxidative stress.13

The role of products derived from glycosylation, protein oxidation, lecithin-cholesterol acyltransferase and ferric-reducing antioxidant power has been evaluated in a wide range of inflammatory diseases10,13-15; but limited studies have been done in alopecia areata patients. Protein and glycation end-products are more stable than lipids and may be better markers of oxidative stress.12,13 Therefore, in this cross-sectional study, we aimed to investigate and compare the levels of oxidative markers (i.e., advanced oxidation protein product and advanced glycation end product) and antioxidants (i.e., paraoxonase-1, lecithin-cholesterol acyltransferase and ferric-reducing antioxidant power) in patients with alopecia areata and healthy controls.

Methods

This cross-sectional study was performed on 40 patients with alopecia areata who were treated in outpatient dermatology clinics of Razi and Imam Komeini Hospitals during 2018-2019. Forty age-, gender- and body mass index (BMI)-matched healthy individuals with aesthetic complaints were also allocated to the control group. An experienced dermatologist confirmed the diagnosis of alopecia areata. The exclusion criteria were as follows: History of inflammatory or autoimmune diseases other than alopecia areata; infection; diabetes mellitus; familial hyperlipidemia; liver or kidney disorders; malignancies; pregnancy or lactation; consumption of antioxidants, vitamins and topical or systemic anti-inflammatory drugs within the past three months; recent history of major surgery; obesity; alcohol or tobacco use; and, professional athlete.

In agreement with the study conducted by Bilgili et al. the sample size was calculated using G*power version 3.1.9.4 (d = 0.64, α = 0.05 and power = 0.8), with an equal allocation ratio for the two-tailed test and assumption of a normal parent distribution. Finally, 40 samples were calculated for each group.8 The study was conducted according to the principles outlined in the Declaration of Helsinki and the Medical Research Involving Human Subjects Act.

The clinical information and demographic data of the subjects were documented. The severity of alopecia areata was determined using the Severity of Alopecia Tool.16 Their BMIs were calculated as weight in kilograms divided by the square of height (kg/m2). A 10-mL venous blood sample was taken from each participant at around 8-9 AM after a 12-hour fasting period to measure the fasting blood sugar level, C-reactive protein level, lipid profile and other laboratory markers. The lipid profile and fasting blood sugar levels were measured using standard enzymatic-colourimetric methods (Pars Azmun Co. Ltd., Tehran, Iran). The serum C-reactive protein level was assessed using a two-site ELISA assay (Diagnostic Biochem, Ontario, Canada).

Additionally, the levels of the advanced glycation end product and advanced oxidation protein product were measured, using the spectrophotometric method (FLUOstar OPTIMA reader, BMG, Germany).13 The serum paraoxonase-1 level was also measured, using an automated paraoxonase assay kit (V31137, ZellBio Co., Germany), following a colourimetric method. Also, to determine the lecithin-cholesterol acyltransferase activity, a commercially available kit (Calbiochem Co., USA) was used, based on the fluorometric method, and the results were expressed as the ratio of wavelengths (470 nm/390 nm). Finally, ferric-reducing antioxidant power was measured using spectrophotometry.11

Data analysis was performed using SPSS version 24 (Chicago, IL, USA). For group comparisons, independent sample t -test, Mann-Whitney U test and Chi-square tests were used. Linear regression analysis was also performed to determine the relationships between continuous variables. A P -value of less than 0.05 was considered statistically significant.

Results

This study was conducted on 40 patients with alopecia areata and 40 healthy controls, including 21 (52.5%) females and 19 (47.5%) males in each group. The mean age of the subjects was 29.23 ± 10.69 years in the alopecia areata group and 29.32 ± 11.81 years in the control group (P = 0.96). Other baseline demographics, clinical characteristics and laboratory findings of the patients and healthy controls are presented in Table 1.

Table 1:: Baseline demographics, clinical characteristics and laboratory findings of patients with alopecia areata and healthy controls
Characteristic Patients with alopecia areata (n = 40) Healthy controls(n = 40) P-value*
Gender, n (%) 1
 Female 21 21
 Male 19 19
Age, years 29.22 ± 10.69 29.32 ± 11.81 0.96
BMI 25.07 ± 4.183 26.21 ± 7.15 0.38
Duration of current disease, months 36.71 ± 66.69 -
Onset of disease, years 18.4 ± 10.90 -
Type of alopecia areata, No. (%)
Patchy 55 -
Ophiasis 0 -
Totalis 7.5 -
Universalis 37.5 -
Nail involvement, n (%) 62.5 -
FBS 100.87 ± 15.03 92.82 ± 11.62 <0.001
Total cholesterol, mg/dL 162.50 ± 43.06 172.35 ± 33.26 0.25
LDL, mg/dL 103.27 ± 33.71 107.83 ± 23.80 0.48
HDL, mg/dL 36.62 ± 8.63 39.75 ± 8.85 0.11
TG, mg/dL 113 ± 59.93 123.85 ± 82.49 0.50
CRP 2.78 ± 3.55 2.96 ± 3.04 0.80
AGE (µmol/L) 78.25 ± 4.44 46.48 ± 4.75 <0.001
AOPP (µmol/L) 182.82 ± 5.99 106.88 ± 7.99 <0.001
FRAP (µmol/L) 822.50 ± 49.43 1400 ± 165.74 <0.001
PON1 (U/l) 96.96 ± 10.90 206.82 ± 8.62 <0.001
LCAT (nmol/ml/hr.) 34.87 ± 3.91 55.46 ± 3.07 <0.001

N: number, BMI: body mass index, FBS: fasting blood sugar, LDL: low-density lipoprotein, HDL: high-density lipoprotein, TG: triglyceride, CRP: c-reactive protein, AGE: advanced glycation end product, AOPP: advanced oxidation protein product, FRAP: ferric-reducing antioxidant power, PON1: paraoxonase 1, LCAT: lecithin cholesterol acyltransferase, *a P -value of less than 0.05 is considered significant

The mean serum levels of advanced glycation end products and advanced oxidation protein product were significantly higher in patients with alopecia areata (78.25 ± 4.44 and 182.82 ± 5.99, respectively), compared to the controls (46.48 ± 4.75 and 106.88 ± 7.99, respectively) (P < 0.001). In contrast, the mean serum levels of antioxidant markers, including ferric-reducing antioxidant power, paraoxonase-1 and lecithin-cholesterol acyltransferase, were significantly lower in the alopecia areata group (822.50 ± 49.43, 96.96 ± 10.90 and 34.87 ± 3.91, respectively), compared to the controls (1400 ± 165.74, 206.82 ± 8.62 and 55.46 ± 3.07, respectively) (P < 0.001) [Table 1]. The results showed that the mean fasting blood sugar level was significantly higher in the alopecia areata group, compared to the controls (100.87 ± 15.03 vs. 92.82 ± 11.62; P < 0.001).

There was a significant difference in the advanced glycation end product level between female and male patients with alopecia areata (79.9 ± 3.8 in females vs. 76.42 ± 4.5 in males; P = 0.01). A negative correlation was found between the serum advanced glycation end product and cholesterol levels in the alopecia areata group (r = -0.03, P = 0.04). Statistical analysis based on Spearman’s rho test on the alopecia areata group revealed a positive correlation between the ferric-reducing antioxidant power level and the percentage of hair loss (P = 0.01, r = 0.4), and a negative correlation between ferric-reducing antioxidant power level and C-reactive protein (P = 0.03, r = -0.3). Moreover, the serum triglyceride level was negatively correlated with the paraoxonase-1 activity in this group (P = 0.02, r = -0.35) [Table 2]. The oxidative and antioxidant markers had no significant associations with hair-loss patterns (P > 0.05) [Table 3].

Table 2:: Correlations between serum markers and risk factors in AA patients
Source AGES * AOPP * FRAP * PON1 * LCAT *
Age 0.50(-0.11) 0.18(0.21) 0.34(-0.15) 0.42(-0.12) 0.11(-0.25)
Onset age of disease 0.41(0.13) 0.70(0.06) 0.14(-0.23) 0.94(-0.01) 0.98(-0.004)
SALT score 0.7(-0.06) 0.83(-0.03) 0.01(0.4) 0.87(0.02) 0.97(0.004)
FBS 0.57(-0.09) 0.34(0.15) 0.05(0.31) 0.77(-0.04) 0.26(0.17)
Cholesterol 0.04(-0.03) 0.07(0.28) 0.46(0.12) 0.23(-0.19) 0.17(-0.21)
TG 0.53(-0.1) 0.21(0.2) 0.29(0.16) 0.02(-0.35) 0.92(0.01)
HDL 0.4(-0.13) 0.41(0.13) 0.34(-0.15) 0.48(0.03) 0.21(-0.12)
LDL 0.1(-0.25) 0.07(0.28) 0.34(0.15) 0.48(-0.11) 0.21(-0.2)
CRP 0.34(0.15) 0.44(-0.12) 0.03(-0.33) 0.5(0.1) 0.62(0.08)

*P -value (Correlation Coefficient, CI), P -value of less than 0.05 is considered significant. AGEs: Advanced glycation end products, AOPP: Advanced oxidation protein products, FRAP: Ferritin reducing the ability of plasma, PON: Paraoxonase1, LCAT: Lecithin cholesterol acyltransferase, SALT score: the Severity of Alopecia Tool, FBS: fasting blood sugar, LDL: low-density lipoprotein, HDL: high-density lipoprotein, TG: triglyceride, CRP: c-reactive protein

Table 3:: Evaluation of the relationship between involvement pattern and oxidative and antioxidative markers in patients group
Mean ± SD P-value
Patchy Totalis Universalis
AGES 78.77 ± 4.18 75 ± 5.19 78.13 ± 4.71 0.39
AOPP 183.34 ± 6.05 191.99 ± 6.52 182.82 ± 5.99 0.8
FRAP 808.55 ± 51.82 855 ± 67.43 836.47 ± 37.25 0.11
PON1 96.92 ± 10.93 95.87 ± 6.53 97.23 ± 12.07 0.98
LCAT 35.04 ± 3.69 34.43 ± 4.54 34.72 ± 4.38 0.95

P -value of less than 0.05 is considered significant. AGEs: advanced glycation end products, AOPP: advanced oxidation protein products, FRAP: ferritin reducing the ability of plasma, PON: paraoxonase1, LCAT: lecithin cholesterol acyltransferase

Discussion

The present results revealed that the mean serum levels of markers of oxidative stress were significantly higher in patients with alopecia areata, compared to the controls, whereas the mean antioxidant activity was significantly lower in the alopecia areata group, compared to the controls. The SALT score and the hair-loss pattern had no significant associations with oxidative and antioxidant markers. Moreover, we found a negative correlation between C-reactive protein and ferric-reducing antioxidant power levels. C-reactive protein (CRP) is an inflammatory mediator and was significantly increased in alopecia areata patients.17 Although our study did not support this result, the possible role of oxidative stress and decreased antioxidative markers like ferric-reducing antioxidant power with inflammatory biomarkers in the development of alopecia areata. CRP level was not higher in alopecia areata cases. But the possible role of oxidative stress and decreased antioxidative markers like FRAP with inflammatory biomarkers in the development of alopecia areata were indicated.

Generally, it is suggested that oxidative stress plays a critical role in the pathogenesis of autoimmune disorders, including psoriasis,18 vitiligo19 and pemphigus vulgaris,20 by causing inflammation, inducing cell apoptosis, and reducing immune tolerance. Although some studies have supported the role of oxidative stress in the pathogenesis of alopecia areata,21,22 the results are inadequate and conflicting.23,24

There are also reports of increased lipid peroxidation and decreased activities of antioxidants, such as glutathione, glutathione peroxidase, and superoxide dismutase, in patients with alopecia areata, compared to the controls.25 In this regard, Barky and Bilgili et al. found that the mean total antioxidant capacity in the serum was significantly lower in patients with alopecia areata, compared to the controls.8,22 Our results also showed that the antioxidant activity was significantly lower in patients with alopecia areata compared to healthy controls. On the other hand, Akar et al. found an increase in the antioxidant activity of superoxide dismutase and glutathione peroxidase in the scalp of patients with alopecia areata, especially in the early stages of the disease, whereas no reduction was observed in the lipid peroxidation rate.24 The results of an Akar study were contrary to our study.

Evidence suggests that paraoxonase-1 is significantly reduced in patients with alopecia areata. This enzyme is majorly influenced by gender, as its activity is higher in females than males.26 However, the present study showed that paraoxonase-1 decrease in patients with alopecia areata but did not confirm any link between paraoxonase-1 activity and gender in alopecia areata patients. It is known that advanced oxidation protein products and advanced glycation end products activate the membrane receptors for the latter to trigger reactive oxygen species generation and oxidative stress, which is involved in inflammatory diseases.13,14 However, most previous studies have addressed the lipid peroxidation rate as a marker of oxidative stress in alopecia areata.24,27,28 In this regard, Cwynar et al. reported a statistically non-significant higher plasma level of advanced oxidation protein products in patients with alopecia areata compared to the controls; however.29 However, this difference in our study was statistically significant.

The reduced serum levels of lecithin-cholesterol acyltransferase and ferric-reducing antioxidant power have been reported in a wide range of inflammatory diseases, including psoriasis and chronic kidney disease.18,30,31 Our results also showed that the serum levels of ferric-reducing antioxidant power and lecithin-cholesterol acyltransferase were significantly lower in patients with alopecia areata, compared to the healthy controls.

Several studies have shown that oxidative stress is involved in the pathogenesis of psoriasis.32 The total oxidant status and malondialdehyde4 levels were significantly higher in psoriasis patients, whereas total antioxidant status and catalase levels in these patients were significantly lower than in healthy controls.33 Based on our study results, the imbalance of oxidative and antioxidant activity may be involved in the pathogenesis of alopecia areata, as it is in psoriasis.

This study had some limitations. First, the sample size was small. Second, most correlations, although significant, were weak and difficult to generalise. Therefore, future research with a larger sample size is necessary to confirm our findings.

We were unable to find any previous reports about serum ferric-reducing antioxidant power, lecithin-cholesterol acyltransferase and advanced glycation end-product levels in patients with alopecia areata. Our results indicated an imbalance of the oxidant-antioxidant enzymatic system in alopecia areata. Therefore, the administration of agents with antioxidant activities may be useful in the management of alopecia areata.

Declaration of patient consent

The authors certify that they have obtained all appropriate patient consent.

Financial support and sponsorship

The research is supported by Tehran University of Medical Science.

Conflicts of interest

There are no conflicts of interest.

References

  1. , , , . Alopecia areata of the beard: A review of the literature. Am J Clin Dermatol. 2017;18:789-96.
    [CrossRef] [PubMed] [Google Scholar]
  2. , , , , , , et al. Adverse events of non-ablative fractional laser photothermolysis: A retrospective study of 856 treatments in 362 patients. J Dermatolog Treat. 2014;25:304-07.
    [CrossRef] [PubMed] [Google Scholar]
  3. , , , , , , et al. Investigation of oxidative stress in patients with alopecia areata by measuring the levels of malondialdehyde and ceruloplasmin in the blood. Postepy Dermatol Alergol. 2018;35:572-76.
    [CrossRef] [PubMed] [Google Scholar]
  4. , , , , , . Evaluation of serum paraoxonase, arylesterase, prolidase activities and oxidative stress in patients with alopecia areata. Skin Pharmacol Physiol. 2019;32:59-4.
    [CrossRef] [PubMed] [Google Scholar]
  5. , , , . Investigation of oxidative stress in patients with alopecia areata and its relationship with disease severity, duration, recurrence and pattern. Clin Exp Dermatol. 2015;40:617-21.
    [CrossRef] [PubMed] [Google Scholar]
  6. , . Oxidative stress and autoimmune skin disease. Eur J Dermatol. 2013;23:5-13.
    [CrossRef] [PubMed] [Google Scholar]
  7. , . Oxidative stress and apoptosis. Pathophysiology. 2000;7:153-63.
    [CrossRef] [PubMed] [Google Scholar]
  8. , , , , , , et al. Serum paraoxonase activity and oxidative status in subjects with alopecia areata. Cutan Ocul Toxicol. 2013;32:290-93.
    [CrossRef] [PubMed] [Google Scholar]
  9. , , , , , . Influence of nutritional factors and the PON1 C(-107)T polymorphism on paraoxonase-1 activity in childhood. Jornal de pediatria. 2020;96:495-502.
    [CrossRef] [PubMed] [Google Scholar]
  10. , , , , . Alterations in lipoprotein defense against oxidative stress in metabolic syndrome. Curr Atheroscler Rep. 2006;8:501-9.
    [CrossRef] [PubMed] [Google Scholar]
  11. , . The ferric reducing ability of plasma (FRAP) as a measure of “antioxidant power”: The FRAP assay. Anal Biochem. 1996;239:70-6.
    [CrossRef] [PubMed] [Google Scholar]
  12. , , , . The road to advanced glycation end products: A mechanistic perspective. Curr Med Chem. 2007;14:1653-71.
    [CrossRef] [PubMed] [Google Scholar]
  13. , , . Advanced glycation end-products and advanced oxidation protein products in patients with diabetes mellitus. Physiol Res. 2002;51:597-604.
    [PubMed] [Google Scholar]
  14. , , , , . Advanced glycation end products in the pathogenesis of psoriasis. Int J Mol Sci. 2017;18:2471.
    [CrossRef] [PubMed] [Google Scholar]
  15. , , , , . Receptor for advanced glycation end products is overexpressed in psoriatic plaques independent of disease severity. J Dermatol Venereol Leprol. 2017;83:556-60.
    [CrossRef] [PubMed] [Google Scholar]
  16. , , , , , , et al. Alopecia areata investigational assessment guidelines-Part II. National Alopecia Areata Foundation. J Am Acad Dermatol. 2004;51:440-47.
    [CrossRef] [PubMed] [Google Scholar]
  17. , , , , . Cross talk between oxidative stress and inflammation in alopecia areata. J Cosmet Dermatol. 2021;20:2305-10.
    [CrossRef] [PubMed] [Google Scholar]
  18. , , , , . Dyslipidaemia & oxidative stress in patients of psoriasis: Emerging cardiovascular risk factors. Indian J Med Res. 2017;146:708-13.
    [CrossRef] [PubMed] [Google Scholar]
  19. , , , , , , et al. Critical appraisal of the oxidative stress pathway in vitiligo: A systematic review and meta-analysis. J Eur Acad Dermatol Venereol. 2018;32:1089-98.
    [CrossRef] [PubMed] [Google Scholar]
  20. , , , , , , et al. Oxidative stress index may play a key role in patients with pemphigus vulgaris. J Eur Acad Dermatol Venereol. 2013;27:465-67.
    [CrossRef] [PubMed] [Google Scholar]
  21. , , , , . The antioxidant role of paraoxonase 1 and vitamin E in three autoimmune diseases. Skin Pharmacol Physiol. 2013;26:2-7.
    [CrossRef] [PubMed] [Google Scholar]
  22. , , , . Oxidative stress in alopecia areata: A case-control study. Am J Clin Dermatol. 2014;15:57-64.
    [CrossRef] [PubMed] [Google Scholar]
  23. , , , , , , et al. Evaluation of total antioxidant status, total oxidant status and oxidative stress index in patients with alopecia areata. Int J Clin Exp Med. 2014;7:1089-93.
    [PubMed] [Google Scholar]
  24. , , , , , . Antioxidant enzymes and lipid peroxidation in the scalp of patients with alopecia areata. J Dermatol Sci. 2002;29:85-90.
    [CrossRef] [PubMed] [Google Scholar]
  25. , . Antioxidants and lipid peroxidation status in the blood of patients with alopecia. Cell Biochem Funct. 2000;18:169-73.
    [CrossRef] [PubMed] [Google Scholar]
  26. , , , , , , et al. Sex difference: An important issue to consider in epidemiological and clinical studies dealing with serum paraoxonase-1. J Clin Biochem Nutr. 2019;64:250-56.
    [CrossRef] [PubMed] [Google Scholar]
  27. , , . Lipid peroxidation/antioxidant activity in patients with alopecia areata. J Eur Acad Dermatol Venereol. 2011;25:403-8.
    [CrossRef] [PubMed] [Google Scholar]
  28. , , , , . Changes of lipid peroxidation and antioxidant system in serum and tissues of patients with alopecia areata. Turkiye Klinikleri Journal of Dermatology. 2008;18:141-5.
    [Google Scholar]
  29. , , , , , , et al. Evaluation of selected parameters of oxidative stress in patients with alopecia areata. Postepy Dermatol Alergol. 2019;36:115-6.
    [CrossRef] [PubMed] [Google Scholar]
  30. , , , , , , et al. Anti-psoriatic therapy recovers high-density lipoprotein composition and function. J Invest Dermatol. 2014;134:635-42.
    [CrossRef] [PubMed] [Google Scholar]
  31. , , , , , , et al. Acquired lecithin: cholesterol acyltransferase deficiency as a major factor in lowering plasma HDL levels in chronic kidney disease. J Intern Med. 2015;277:552-61.
    [CrossRef] [PubMed] [Google Scholar]
  32. , , . Oxidative stress in the pathogenesis of psoriasis. Free Radic Biol Med. 2009;47:891-905.
    [CrossRef] [PubMed] [Google Scholar]
  33. , , , . Association of total oxidant status, total antioxidant status, and malondialdehyde and catalase levels with psoriasis: A systematic review and meta-analysis. Clin Rheumatol. 2019;38:2659-71.
    [CrossRef] [PubMed] [Google Scholar]
Show Sections