ORIGINAL RESEARCH

The Serum Level of Oxidative Stress

ABSTRACT
BACKGROUND: Psoriasis is a chronic, immune-
mediated, inflammatory disease. Previous studies
have indicated a possible role of oxidative stress in the
and Antioxidant Markers in Patients
with Psoriasis: A Cross-sectional Study
by SAFOURA SHAKOEI, MD; MANOUCHEHR NAKHJAVANI, MD;
HOSSEIN MIRMIRANPOOR, MD; MOHANA ALINEJAD MOTLAGH, MD;
ARGHAVAN AZIZPOUR, MD; and ROBABEH ABEDINI, MD
Drs. Shakoei and Motlagh are with the Department of Dermatology at Imam Khomeini Hospital, Tehran University of Medical
Sciences in Tehran, Iran. Drs. Nakhjavani and Mirmiranpoor are with the Endocrinology and Metabolism Research Center at
Vali-Asr Hospital, Tehran University of Medical Sciences in Tehran, Iran. Drs. Azizpour and Abedini are with the Department of
Dermatology at Razi Hospital, Tehran University of Medical Sciences in Tehran, Iran.
J Clin Aesthet Dermatol. 2021;14(7):38–41.

pathogenesis of psoriasis. OBJECTIVE: We sought
to compare special oxidative stress and antioxidant
markers in psoriatic patients. METHODS: This
study included 35 patients with psoriasis and 35
healthy controls. Serum levels of oxidant markers,
including advanced glycation end products (AGEs)
and advanced oxidation protein products (AOPPs),
as well as antioxidant enzymes, including lecithin-
cholesterol acyltransferase (LCAT), paraoxonase-1
(PON1), and ferric-reducing ability of plasma (FRAP),
were measured. RESULTS: The mean age of the
subjects was 39.63±13 years in the case group and
39.37±12.62 years in the control group (p=0.92). The
mean Psoriasis Area and Severity Index (PASI) scores of
these groups were 15.27 and 10.47. The mean levels
of fasting blood sugar and C-reactive protein were
significantly higher in the case group than the control
group (p=0.04 and p=0.02, respectively). Moreover,
the mean levels of AGEs and AOPPs in the case group
were significantly higher than in the control group
(p=0.001), while the mean levels of FRAP, PON1, and
LCAT were significantly lower in the case group than in
the control group (p=0.001). There was no significant
association between PASI and oxidant or antioxidant
markers, except for AOPP, which had a negative
association with PASI. CONCLUSIONS: Our findings
suggest an imbalance among oxidative stress and
antioxidant markers in the pathogenesis of psoriasis.
The oxidant-antioxidant enzymatic system is impaired
in psoriasis as a result of increased oxidant products
and reduced antioxidant activity.
KEY WORDS: Psoriasis, advanced glycation end
products, advanced oxidation protein products,
lecithin-cholesterol acyltransferase, paraoxonase-1
P
Psoriasis is a chronic, immune-mediated,
inflammatory disease that affects the skin and
joints. The prevalence of this disease varies
between 0.6 and 4.8 percent.1 Although it can
present at any age from birth to older age, the
peak age ranges of onset are 15 to 20 and 55 to
60 years.2 The exact etiology of psoriasis remains
unclear. However, genetic, immunological,
psychological, hormonal, and environmental
factors might be involved. The pathogenesis of
psoriasis might be associated with abnormal
interactions between innate immune cells,
T-cells, and keratinocytes; activation of the
immune system; the release of excess pro-
inflammatory substances; and tissue or organ
damage.3,4
Psoriasis lesions are characterized by localized
or widespread pruritic erythematous plaques
with thick, silvery-white scales.5 Recently,
several studies have evaluated the role of
reactive oxygen species and oxidative stress in
the pathogenesis of psoriasis. Oxidative stress
by disruption of redox signaling might cause
molecular damage.6,7 It can also activate dendritic
cells, lymphocytes, and keratinocytes and
increase the levels of enzymatic/nonenzymatic
antioxidants and lipid peroxidation products,
leading to angiogenesis, inflammation, cell
necrosis, and apoptosis.8 Reactive oxygen species
are oxidative stress markers. Pyrolyzed proteins,
protein carbonyl compounds (PCCs), and
advanced oxidation protein products (AOPPs) are
some protein oxidative stress marker products.
The characteristics of these markers can be
quantified, including early production, stability,
reliability, and long lifespan.8,9
Advanced glycation end products (AGEs) are
produced through the oxidation of sugars, lipids,
and amino acids and form aldehydes. Aldehydes
can bind to proteins and accumulate in tissues,
resulting in hyperglycemia, hyperlipidemia,
and oxidative or carbonyl stress.10 On the other
hand, lecithin-cholesterol acyltransferase (LCAT),
paraoxonase-1 (PON1), and ferric-reducing
ability of plasma (FRAP) as antioxidant factors
can protect cells against lipid oxidation and the
accumulation of oxidized low-density lipoprotein
(LDL) and improve the antioxidant properties of
high-density lipoprotein (HDL).11–13
Previous studies have indicated a possible role
of oxidative stress and antioxidant markers in the
pathogenesis of psoriasis, but there are still some
controversies in this area. The objective of this
cross-sectional study was to compare the serum
levels of oxidative stress markers and antioxidant
markers, including AGEs, LCAT, PON1, AOPPs,
and FRAP, between patients with psoriasis and
healthy controls. This study evaluated different
oxidant and antioxidant factors among patients
with psoriasis. Identification of some risk factors

FUNDING: This study was funded and supported by the Tehran University of Medical Sciences (grant no. 97-01-30-34656).
DISCLOSURES: The authors report no conflicts of interest relevant to the content of this article.
CORRESPONDENCE: Safoura Shakoei, MD; Email: dr.shakoei@gmail.com

JCAD JOURNAL OF CLINICAL AND AESTHETIC DERMATOLOGY July 2021 • Volume 14 • Number 7
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 ORIGINAL RESEARCH
can provide more valuable information about the
treatment of this disease.
METHODS
This cross-sectional study was conducted in
the dermatology outpatient departments of
two hospitals between 2018 and 2019. Patients
with a diagnosis of psoriasis were considered
as the case group. The severity of disease was
determined according to the Psoriasis Area
and Severity Index (PASI).14 Total PASI scores of
less than seven, 7 to 15, and greater than 15
represented mild, moderate, and severe psoriasis,
respectively.15 Sex- and age-matched healthy
individuals with cosmetic complaints were also
recruited to the control group.
The exclusion criteria were as follows:
1) history of concurrent autoimmune or
inflammatory diseases, immunodeficiency
disorders, or cancers; 2) underlying diseases
(e.g., diabetes, familial hypercholesterolemia,
metabolic syndrome, renal disease, and
liver dysfunction); 3) consumption of oral
contraceptive pills, vitamin C or E, diuretics,
or anti-inflammatory drugs in the past three
months; 4) recent surgery; and 5) excessive
exercises. Individuals with alcohol consumption
or smoking habits, as well as patients undergoing
systemic treatment in the past six months,
were also excluded. The study population was
informed about the study and asked to sign
informed consent forms. Then, demographic and
clinical data were gathered and recorded. The
body mass index was calculated as a person’s
weight in kilograms divided by the square of
height in meters (kg/m2).
Laboratory measurements. Venous
blood samples (10mL) were collected after
overnight fasting. They were centrifuged for 15
minutes, stored frozen at −70°C, and sent to the
laboratory. The serum levels of AOPPs, AGEs, and
FRAP were determined via spectrofluorimetry. A
commercially available kit (423901; Calbiochem,
San Diego, California) was used to assess the
LCAT activity by the fluorometric method. The
serum PON1 level was also assessed using an
automated paraoxonase assay kit (V31137;
ZellBio, Berlin, Germany) by the colorimetric
method.
Lipid profile and fasting blood sugar (FBS)
were assayed by standard enzymatic colorimetric
methods using enzymatic assays (Parsazmun Co.
Ltd., Tehran, Iran). LDL was also calculated based
on the Friedewald formula. The serum C-reactive
protein (CRP) level was assessed in all subjects
using a two-site enzyme-linked immunosorbent
assay (Diagnostic Biochem, Ontario, Canada).
Data were analyzed to compare the serum
oxidative and antioxidant markers between
the case and control groups as the primary
outcome. Moreover, correlations between some
demographic factors and concentrations of
serum markers were evaluated in both groups.
Sample size. According to a study by Yazici
et al,9 the mean levels of AOPPs were 62.4±20.6
and 36.1±13.2 μmol/L among psoriasis patients
and controls, respectively. The sample size was
calculated to be 35 subjects per group. With a
total sample size of 70 patients, the study had a
power of 90 percent and an alpha error of 0.05.
Statistical analysis. All statistical analyses
were conducted using the Statistical Package for
the Social Sciences version 19 (IBM Corporation,
Armonk, New York). Quantitative variables with
a normal distribution were reported as mean
± standard deviation and percentage values,
while quantitative variables without a normal
distribution were presented as median, range
(min–max), and quartile values. Qualitative
variables were also reported as percentages. Also,
the Mann-Whitney test, analysis of variance,
Kruskal-Wallis test, Pearson’s correlation test,
Spearman’s correlation test, and t-test were used
to analyze the correlations between variables.
P-values of less than 0.05 were considered to be
statistically significant.
Ethical considerations. The present study
was extracted from a medical student thesis.
Ethical approval was obtained according to the
international guidelines of the Declaration of
Helsinki. Written informed consent was obtained
from the included patients.
RESULTS
This study was conducted on 35 patients with
psoriasis and 35 subjects in the control group. In
total, 18 (51.4%) women and 17 (48.6%) men
were included in each group. The mean age of
the subjects was 39.63±13 years in the case
group (range: 17–77 years) and 39.37±12.62
years in the control group (range: 18–75 years)
(p=0.92). The mean body mass index in the
case group was significantly higher than that
of the controls (27.94±4.20 vs. 26.01±4.68 kg/
m2; p=0.04). Based on these findings, the mean
age at onset of disease was 26.86±12.61 years
(range: 9–57 years), and the mean disease
duration was 10.37±8.67 years (range: 1–37
JCAD JOURNAL OF CLINICAL AND AESTHETIC DERMATOLOGY July 2021 • Volume 14 • Number 7
years).
The mean PASI score and body surface area
(BSA) were 10.47 and 15.27m2, respectively. The
mean levels of oxidative stress and antioxidant
markers were significantly different between the
two groups: the mean levels of AGEs and AOPPs
were significantly higher in psoriasis patients
(p=0.001), while the mean levels of FRAP, PON1,
and LCAT were significantly lower in psoriasis
patients (p=0.001). The mean FBS and CRP levels
in the case group were also significantly higher
than in the control group (p=0.04 and p=0.02,
respectively). However, no significant differences
were observed regarding the lipid profile
between the groups (p>0.05). Detailed data of
the case group are presented in Table 1.
The mean serum PON1 level was inversely
correlated with the CRP level (r = −0.352;
p=0.041). No significant relationship was found
between CRP level and BSA (p=0.351) or PASI
score (p=0.532). Also, the grade of psoriasis
severity (mild, moderate, and severe) had no
significant correlation with serum oxidative/
antioxidant markers (p>0.05). Correlations
between serum markers and some risk factors
were also assessed in this study. Spearman’s
correlation and Mann-Whitney tests showed that
age and sex had no significant associations with
oxidative stress or antioxidant markers in the
case and control groups (p>0.05) (Table 2).
DISCUSSION
The present findings demonstrated
associations between psoriasis and serum levels
of different oxidative stress and antioxidant
biomarkers. According to the results, the mean
level of AGEs in patients with psoriasis was
significantly higher than that among healthy
controls. It is known that psoriasis stimulates
pro-inflammatory responses and chronic
inflammation by activation of monocytes,
macrophages, neutrophils, and endothelial cells.
This activation of the immune system results in
the production of more cytokines and reactive
oxygen forms and the accumulation of AGEs.16
The role of AGEs has been confirmed in the
pathogenesis of inflammatory diseases, such as
diabetes and psoriasis.17
Oxidative stress is suggested to play a critical
role in the pathogenesis of autoimmune
disorders, including vitiligo, alopecia areata, and
pemphigus vulgaris.7,18,19
Consistent with our findings, Damasiewicz-
Bodzek et al16 reported a significant increase
39
 ORIGINAL RESEARCH

TABLE 1. Comparison of characteristics data and serum factors in case and control groups Haberka et al21 reported that AOPPs were
CASE GROUP CONTROL GROUP significantly higher in patients with mild to
CHARACTERISTIC P-VALUE* moderate psoriasis compared to controls.
(N=35) (N=35)
Sex, n (%) 1 Yazici et al9 also indicated an increase in
Male 17 (48.6) 17 (48.6) - protein oxidation in mild to severe psoriatic
Female 18 (51.4) 18 (51.4) - patients. They demonstrated that psoriasis-
Age (years) 39.63±13.00 39.37±12.62 0.92
related inflammation, phagocytic cell oxidation,
and oxidation reactions of myeloperoxidase–
Body mass index (kg/m2) 27.94 z 4.20 26.01±4.68 0.04
hypochlorous acid could cause protein oxidation,
Duration of disease (years), mean ± SD 10.37±8.67 - -
reflected by increased levels of oxidative markers,
The mean of PASI (points) mean ± SD 10.47±8.53 - - such as AOPPs.9 Conversely, Skoie et al22 did not
The mean of BSA (m2), mean ± SD 15.27±15.5 - - show any significant difference between patients
The severity of disease, % with psoriasis and healthy subjects regarding
Mild 45.7 - - plasma AOPP concentrations (p=0.75). Moreover,
Moderate 31.4 - - our results showed that AOPP concentration
Severe 22.9 - - had negative associations with PASI and BSA.
Oxidative and antioxidant markers, mean ± SD 0.001 However, such correlations have not been
AGEs 79.68±3.72 47.08±4.11 - reported by other research.9,22 The AOPP plasma
AOPP 181.28±3.88 102.18±17.16 - level was increased in patients with alopecia
FRAP 810.48±25.67 1411.77±133.49 -
areata compared to healthy controls; however,
the difference was statistically insignificant.23
PON 103.74±3.72 204.25±7.74 -
Based on the present results, the levels of
LCAT 37.68±2.47 56.02±3.13 -
FRAP, PON1, and LCAT as antioxidant biomarkers
Lipid profiles, mean ± SD 0.001
were significantly lower in the case group
Cholesterol 166.20±28.65 142.46±84.69 0.11 compared to in the control group. In line with our
Triglycerides 129.12±57.07 179.09±37.77 0.42 findings, Barygina et al24 showed a significant
High-density lipoprotein 36.59±7.21 38.66±7.36 0.24 decrease in the mean total antioxidant capacity
Low-density lipoprotein 103.59±24.51 112.23±29.82 0.19 of psoriasis patients as compared with among
Fasting blood sugar, mean ± SD 106.71±30.32 95.06±11.01 0.04 controls. Some research has demonstrated a
C-reactive protein, mean ± SD 5.43±9.01 2.17±64 0.02 significant decrease in PON1 activity among
PASI: Psoriasis Area and Severity Index; BSA: body surface area; AGEs: advanced glycation end products; AOPP: advanced
patients with psoriasis and patients with alopecia
oxidation protein products; FRAP: ferritin-reducing ability of plasma; PON: paraoxonase-1; LCAT: lecithin-cholesterol areata compared to among healthy controls.25,26
acyltransferase Furthermore, Hashemi et al27 demonstrated
*P-value < 0.05 is statistically significant that the plasma concentration of FRAP, as a total
antioxidant capacity marker, was significantly
TABLE 2. Correlations between serum markers and risk factors lower in psoriatic patients than in healthy
SOURCE AGES* AOPP* FRAP* PON* LCAT* controls. Conversely, Esmaeili et al28 did not find
Age 0.172 (0.236) 0.733 (–0.060) 0.689 (–0.070) 0.207 (–0.219) 0.074 (0.306)
any significant difference in terms of FRAP level
between patients and controls. Holzer et al29
Duration of disease 0.911 (0.022) 0.915 (0.021) 0.890 (0.027) 0.322 (0.191) 0.023 (0.422)
found that LCAT was reduced in patients with
PASI 0.399 (0.147) 0.031 (–0.365) 0.120 (0.268) 0.727 (0.061) 0.314 (0.175) psoriasis and suggested a possible protective
PASI: Psoriasis Area and Severity Index; AGEs: advanced glycation end products; AOPP: advanced oxidation protein effect of this antioxidant biomarker against
products; FRAP: ferritin-reducing ability of plasma; PON: paraoxonase-1; LCAT: lecithin-cholesterol acyltransferase psoriasis. They showed that antipsoriatic therapy
*P-value and correlation coefficient
could increase PON1, which prevented LCAT
inactivation.29
in AGE-peptide concentrations in patients with The results of the present study demonstrated The results of the our study revealed that
psoriasis compared to in healthy individuals. They a significant increase in AOPPs in the case group the mean FBS and CRP levels in patients with
concluded that there was a significant correlation relative to in the control group. Psoriasis may psoriasis were significantly higher than in healthy
between psoriasis and oxidative stress markers, be responsible for endothelial dysfunction controls. Other studies have confirmed these
such as protein glyco-oxidation products.16 and vascular remodeling, resulting in cytokine findings as well. Farshchian et al30 demonstrated
Moreover, Papagrigorak et al20 showed that the imbalance and increasing the level of AOPPs. a significant increase in CRP level to be a systemic
serum levels of AGEs in patients with severe The association between psoriasis and increased inflammatory biomarker in patients with
psoriasis were significantly higher than those of serum levels of AOPPs has been evaluated in psoriasis. Significantly higher levels of CRP were
healthy controls. previous studies. In line with our findings, also reported by Vadakayil et al31 among patients

JCAD JOURNAL OF CLINICAL AND AESTHETIC DERMATOLOGY July 2021 • Volume 14 • Number 7
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 ORIGINAL RESEARCH
with psoriasis compared to healthy controls. It
seems that psoriasis, because of its inflammatory
nature, might influence hormone production
and insulin resistance, resulting in elevated
blood sugar levels.32 In a study by Abedini et al,33
significantly higher levels of FBS were reported
in 123 Iranian psoriatic patients compared to
among healthy controls.33 However, this finding
was not confirmed in the study by Farshchian et
al, which also involved an Iranian population.34
Limitations. Our study was limited by its
small sample size. Our observations must be
confirmed in future studies with larger sample
sizes.
CONCLUSION
Our findings revealed that an imbalance of
oxidative stress and antioxidant factors might
contribute to the pathogenesis of psoriasis.
Higher levels of AGEs and AOPPs and lower
levels of FRAP, PON1, and LCAT were significant
among patients with psoriasis compared to the
healthy controls. Therefore, treatment based
on antioxidant strategies might be beneficial in
psoriasis management.
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