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Serum level of interleukin-17 and its relation to interleukin-6 and tumor necrosis factor alpha level in patients with rheumatoid arthritis

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To investigate serum level of interleukin-17 in rheumatoid arthritis patients and to assess the relationship of this cytokine with serum levels of IL-6 and tumor necrosis factor α. Subjects and methods: 82 patients with rheumatoid arthritis and 30 healthy volunteers were enrolled in the study. Disease activity was determined by disease activity score (DAS28) in patients with rheumatoid arthritis.

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SERUM LEVEL OF INTERLEUKIN-17 AND ITS RELATION TO INTERLEUKIN-6 AND TUMOR NECROSIS FACTOR ALPHA

LEVEL IN PATIENTS WITH RHEUMATOID ARTHRITIS

Nguyen Huy Thong 1 ; Nguyen Dang Dung 2 ; Quyen Dang Tuyen 1

SUMMARY

Objectives: To investigate serum level of interleukin-17 in rheumatoid arthritis patients and to assess the relationship of this cytokine with serum levels of IL-6 and tumor necrosis factor α Subjects and methods: 82 patients with rheumatoid arthritis and 30 healthy volunteers were

enrolled in the study Disease activity was determined by disease activity score (DAS28) in patients with rheumatoid arthritis Serum levels of IL-6, IL-17 and TNF-α were measured by fluorescence covalent microbead immunosorbent assay Results: Serum level of IL-17 in rheumatoid arthritis patients and controls were 0.59 ± 0.92 and 0.62 ± 0.94 pg/mL, respectively There was no difference in serum levels of IL-17 in RA patients compared to that in controls (p > 0.05) Serum IL-17 level, however, seemed to be correlated with changes in serum levels of IL-6 and TNF-α in rheumatoid arthritis patients: in patients with elevated serum levels of IL-17, the IL-6 and TNF-α were higher compared to those in patients with normal serum level of IL-17

Conclusions: Serum level of IL-17 in patients with rheumatoid arthritis did not differ from that in healthy people Higher serum level of IL-17 correlated with higher serum levels of of IL-6 and TNF-α

* Keywords: Rheumatoid arthritis; IL-6; IL-17; TNF-α

INTRODUCTION

Rheumatoid arthritis (RA) is a chronic

inflammatory disease characterized by joint

swelling, joint tenderness, and destruction

of synovium, leading to severe disability

and premature mortality of patients [1]

Cytokine networks play a fundamental

role in the processes that cause

inflammation, articular destruction of RA

[2] IL-17 possesses properties of a

pro-inflammatory cytokine, and plays very

important roles in pathogenesis of RA [3]

IL-17 is a cytokine that stimulates the

production of a variety of inflammatory

mediators, and plays a leading role in regulating the relationship between pro-inflammatory cytokines In this role, IL-17 activates not only B cells to produce antibodies, but also macrophages, synovial fibroblasts, chondrocytes to secret cytokines, such as IL-1, IL-6, TNF-α, and matrix metalloproteinase (MMPs) [4, 5].That is the reason why serum IL-17 may be related

to serum IL-6 and TNF-α in RA patients

Thus, the aim of this study was: To

evaluate serum levels of IL-17 and its relation serum IL-6 and TNF-α levels in

RA patients

1 103 Military Hospital

2 Vietnam Military Medical University

Corresponding author: Nguyen Dang Dung (dzungmd@yahoo.com)

Date received: 26/06/2019

Date accepted: 06/08/2019

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SUBJECTS AND METHODS

1 Subjects

* Patients:

This study was carried out at Department

of Rheumatology and Endocrinology of

103 Military Hospital between May 2012

and June 2015

Eighty two patients, 71 women and 11

men, with the diagnosis of RA fulfilled the

ACR/EULAR 2010 RA classification

criteria [1] Before entering study, 43 and

4 patients were taken glucocorticoids and

conventional synthetic disease-modifying

respectively Patients with other

concomitant rheumatic diseases, severe

infections, chronic autoimmune diseases,

and/or taking bio-DMARDs which may

influence laboratory and cytokine profile

were excluded from the study

* Healthy subject population: thirty

sex-matched healthy controls (mean age

41.60 ± 4.57; range, 35 - 50 years, 26

women and 4 men) were included in the

study

2 Methods

* Clinical assessment:

Disease activity was assessed by the

28-joint disease activity score C-reactive

protein (DAS28 CRP) [6] in RA patients

Patient global assessment of disease

activity and provider global assessment

of disease activity were evaluated

using Visual Analog Scale Formats for

assessment of disease activity [7] Erythrocyte Sedimentation Rate (ESR) and C-reactive protein (CRP) were also recorded

* Laboratory analysis:

Blood samples of patients and controls were collected and put in a sterile plain tube and stored frozen at -80oC until analysis We used commercially available human Fluorescence covalent microbead immunesorbent assay (FCMIA) kits for

IL-6, IL-17 and TNF-α (R&D systems MN, USA) The assay was performed according

to the instructions provided by the manufacturer Serum levels of cytokines were reported as pg/mL

The cut-off values of serum IL-6, IL-17 and TNF-α were determined by ROC (Receiver Operating Curve)

* Statistical analysis:

All statistical analyses were performed using the Statistical Package for the Social Sciences (SPSS) for Windows, version 18.0 (SPSS, Chicago, IL, USA) Continuous variables are presented as mean ± standard deviation or median The normality of the distribution for all variables was assessed by Kolmogorov-Smirnov test Intergroup comparisons

were made using the student’s t-test for

normally distributed variables and

Mann-Whitney U test for non-parametric

variables Difference with p value being less than 0.05 was considered statistically significant

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RESULTS

1 Patients and demographic, clinical characteristics

Table 1: Demographic and clinical characteristics of RA patients and controls

RA group (n = 82)

Control group (n = 30)

Mean tender joint count ± SD (range 0 - 28) 14.13 ± 9.08; 13.00

7.16 ± 2.25

Mean provider global assessment of disease

5.65 ± 1.92

DAS28 CRP

Pre-study

treatment

(DAS28 (CRP) is missing in three patients)

(Anti-CCP: Anti-cyclic citrulinated peptide; CRP: C-reative protein; DAS28: Disease Activity Score; ESR: Erythrocyte Sedimentation Rate)

Patients and healthy people in the control group did not significantly differ in sex distribution The mean age of controls was considerably lower than that in RA patients The mean disease duration in RA patients was 4.29 ± 5.34 years The mean DAS28 CRP was 6.19 ± 1.36 (range, 2.81 - 8.50) The proportion of patients had low or moderate and high disease activity based on DAS28 CRP was 20.5% (17/83 patients)

and 79.5% (66/86 patients), respectively

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2 Changes in serum levels of IL-17, IL-6, TNF-α and relations between serum IL-17 and serum IL-6, TNF-α in RA patients

Table 2: The comparison of serum IL-6, IL-17 and TNF-α levels of patients and controls

Serum cytokines

IL-6

< 0.05*

IL-17

> 0.05

TNF-α

< 0.001*

(*: Test Mann - Whitney, IQR: Interquartile Range)

Statistics shows that the median of serum IL-6 of patients was considerably higher than that in controls (p < 0.05) There was no significant difference in the median of serum IL-17 levels between patients and controls The median of serum TNF-α of patients was significantly lower than that in controls (p < 0.001)

Chart 1: The distributions of RA according to serum IL-17 levels

The percentage of patients with elevated serum cytokine levels (elevated serum levels of 1, 2 or 3 cytokines) was 73.20%, among which the percentage of patients with elevated serum IL-17 (either single elevation of IL-17 level, or elevated IL-17 in combination with IL-6 and/or serum TNF-α) was 56.10%; meanwhile, only 17.10% of

RA patients had elevated IL-6 and/or TNF-α level

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Table 3: The comparison of serum IL-6 and serum TNF-α based on serum IL-17 groups

Serum IL-17

p

Serum IL-6 (pg/mL)

0.068*

Serum TNF-α (pg/mL)

< 0.05*

(*: Test Mann - Whitney; IQR: Interquartile Range)

Assessing the change of serum IL-6, TNF-α according to serum IL-17 groups of RA patients, the results showed that the median of serum TNF-α of patient group with elevated serum IL-17 was higher than that of healthy group (p < 0.05) The median serum IL-6 had an increased trend in patients with elevated serum IL-17 compared to healthy group (p = 0.068)

DISCUSSION

In the present study, serum levels of

IL-17 as well as IL-6 and TNF-α cytokine

were evaluated in patients with RA

Additionally, the relationships between

serum IL-17 and serum IL-6, TNF-α were

also assessed

Our results showed that there was no

significant difference in median value of

serum IL-17 level of the patients compared

to that of the controls (p = 0.879, by

Mann-Whitney test) (table 2) However,

the percentage of RA patients having

elevated serum IL-17 level was 56.10%,

which was higher than that of IL-6 and

TNF-α (chart 1)

In contrast, it was reported that in RA

patients, serum level of IL-17 was

significantly higher than that in healthy

people [8, 9, 10], as well as that of

patients with osteoarthritis [11] IL-17 level

was not only elevated in serum, but also

in synovial fluid of RA patients at early stage of the disease without treatment, and the level of IL-17 in synovial fluid was proportionally correlated with that in serum [9, 12]

The results of current study showed that serum IL-17 levels in RA patients were not elevated compared to that in healthy people This was probably because in RA patients at the clinical period of the disease, serum IL-17 level might be lower than that before the disease onset, which was in accordance with remarks by Kokkonen H et al (2010),

in which the authors found that median value of serum IL-17 levels of RA patients before disease onset was 28.7 pg/mL and then it decreased to 6.0 pg/mL during the illness period of the disease, which was lower than that in healthy people at the same age and gender distribution (being

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21.1 pg/mL) The difference in serum

IL-17 level of the RA patients and of the

controls was significant with p value being

6.1 x 10-5 [13]

Additionally, it was reported that the

production and secretion of most of Th1

cytokines (IL-1β, IL-2, IL-3, IL-6, TNF,

interferon-γ) and Th17 cytokines (IL-17,

GM-CSF) were down-regulated by

corticoids [14] In this study, 50.6% of RA

patients were treated by corticoids before

having serum cytokines testing (table 1),

and it might be one possible cause of the

low level of serum IL-17 we have observed

However, when analyzing data, the results

of this study indicated that there was no

significant difference between median

values of serum IL-17 levels of the RA

patients who underwent corticoid treatment

compared to that of treatment-nạve ones

Furthermore, in this study, the change

in serum IL-17 level seemed to influence

the change in serum IL-6 and TNF-α

levels The results of chart 1 and table 3

indicated that serum IL-17 levels of RA

patients were increased along with elevation

of serum IL-6 and TNF-α levels These

findings were in accordance with a report

by Miossec P (2007), in that IL-17 seemed

to play a central role in pathogenesis of

RA by stimulating synovial macrophages,

fibroblasts and dendritic cells to produce

and secrete pro-inflammatory cytokines,

including IL-6 and TNF-α [4], and in the

meantime, IL-17 was the "conductor" that

regulated the interaction between cytokines

[5]

Our study has some limitations The

sample size of patients was relatively

small, many patients were on medication

treatment, including glucocorticoids as

well as DMARDs, before enrolment in this research Treatment regimens might influence the serum levels of cytokines

On the other hand, this study was designed as a cross-sectional one, and cytokines profile was not evaluated in comparison with that in treatment-naive

RA patients Furthermore, patients of this study were mainly in an established period of RA disease

CONCLUSION

This study demonstrated that there was no difference in serum IL-17 between

RA patients and healthy people Serum IL-17 seemed to influence the changes in serum IL-6 and TNF-α in RA patients However, further follow-up research involving large samples are required to clarify the precise role of IL-17 in relationships with IL-6 and TNF-α in the development of RA disease

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Rheumatoid arthritis classification criteria: An American College of Rheumatology/European League Against Rheumatism collaborative

initiative Arthritis & Rheumatism 2010, 62

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2 Shah A, St Clair E.W Rheumatoid

Arthritis In: Harrison's Principles of Internal Medicine 19 edition, McGraw-Hill Education

2015, pp.2136-2148

3 Gaffen S.L The role of interleukin-17 in

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Current Rheumatology Reports 2009, 11 (5), pp.365-370

4 Miossec P Interleukin-17 in fashion, at

last: Ten years after its description, its cellular

source has been identified Arthritis &

Rheumatism 2007, 56 (7), pp.2111-2115

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5 Veldhoen M Interleukin-17 is a chief

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9 Metawi S.A, Abbas D, Kamal M.M et al

Serum and synovial fluid levels of

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10 Hanan M.A, Gaber R.A Zaytoun H.A

Th-17 cells and serum IL-17 in rheumatoid arthritis patients: Correlation with disease

Rheumatologist 2016, pp.381-387

11 Zhao P.W, Jiang W.G, Wang L et al

Plasma levels of IL-37 and correlation with TNF-alpha, IL-17A, and disease activity during

DMARD treatment of rheumatoid arthritis

Public Library of Science One 2014, 9 (5), e95346

12 Rosu A, Margaritescu C, Stepan A et

al IL-17 patterns in synovium, serum and

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et al Up-regulation of cytokines and chemokines

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