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ORIGINAL ARTICLE

Evaluation of IL-34 in psoriasis and psoriatic

arthritis patients: Correlation with disease activity

and severity

Dina A. Farrag

a,*

, Marwa K. Asaad

b

, Christine K. Ghobrial

b

a

Physical Medicine, Rheumatology and Rehabilitation Department, Faculty of Medicine, Ain Shams University, Cairo, Egypt

b

Dermatology, Venereology and Andrology Department, Faculty of Medicine, Ain Shams University, Cairo, Egypt

Received 17 May 2016; accepted 28 May 2016

KEYWORDS

IL-34; Psoriasis; Arthritis;

Composite psoriasis disease activity index (CPDAI); Psoriasis skin area severity index (PASI);

Modified Sharp-van der Heijde

Abstract Introduction: Interleukin-34 (IL-34) is a newly discovered cytokine essential for skin homoeostasis. It is involved in macrophage differentiation, osteoclastogenesis and inflammation. This could suggest a potential role in the pathogenesis of psoriasis and psoriatic arthritis (PsA).

Aim of the work: To assess serum IL-34 level in psoriatic patients with and without arthritis and to correlate it with disease activity and severity.

Patients and methods: Serum IL-34 level was measured in 45 psoriasis patients (21 had PsA) and 20 healthy controls. Patients were clinically assessed using psoriasis skin area severity index (PASI), composite psoriasis disease activity index (CPDAI) and peripheral joint score (PJS). Radiological assessment of hands and feet was done using modified Sharp-van der Heijde (mSvH) scoring method for PsA.

Results: The mean age of the PsA patients (47.4 ± 10.2 years) was comparable with the psoriasis only patients (42.5 ± 7.5 years) and control (43.4 ± 7 years). Serum IL-34 was significantly higher among PsA patients compared to those without arthritis and controls (median = 2500 ng/L, 512 ng/L and 325 ng/L, respectively). CPDAI was significantly higher in PsA compared to patients without arthritis. PASI scores were comparable between patients. Serum IL-34 level correlated sig-nificantly with each of PASI, CPDAI and PJS but not with the mSvH score. Receiver operator characteristic curve analysis revealed that serum IL-34 testing showed excellent diagnostic perfor-mance for PsA in psoriasis patients.

* Corresponding author at: 1 Mohy-Eldin Abu-Elezz St., Almaza, Heliopolis, Cairo, Egypt. Tel.: +20 22916441, mobile: +20 1001843100. E-mail address:dinaaboubakr@yahoo.com(D.A. Farrag).

Peer review under responsibility of Egyptian Society for Rheumatic Diseases.

Production and hosting by Elsevier

Egyptian Society of Rheumatic Diseases

The Egyptian Rheumatologist

www.rheumatology.eg.net

www.elsevier.com/locate/ejr

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Conclusion: The markedly elevated IL-34 serum level in PsA patients compared to non-arthritic ones and its remarkable correlation with PsA disease activity, suggest its importance as a marker for arthritis in psoriasis patients.

Ó2016 Egyptian Society of Rheumatic Diseases. Publishing services provided by Elsevier B.V. This is an open access article under the CC BY-NC-ND license (http://creativecommons.org/licenses/by-nc-nd/4.0/).

1. Introduction

Psoriasis is a common immune-mediated skin disease[1]. Pso-riatic arthritis (PsA) is a chronic inflammatory arthritis that develops in at least 0.1–1% of the general population[2]and 5.8–30% of patients with psoriasis[3]. The diagnosis of PsA in psoriatic patients can be missed because most of the patients present with symptoms other than frank arthritis[4]. Inflam-matory cytokines play an essential role in the immune-pathogenesis of psoriasis and PsA[5].

Psoriatic arthritis is characterized by extensive bone resorp-tion. Myeloid derived cells differentiate into osteoclasts in the presence of macrophage colony stimulating factor (MCSF) and receptor activator nuclear kappa beta ligand (RANKL). RANK and colony stimulating factor 1 receptor (c-Fms) are expressed on osteoclast precursors in inflamed synovium and subchondral bone and upon stimulation with MCSF and RANKL develop into mature bone resorbing cells[6,7].

Interleukin-34 (IL-34) is a newly discovered cytokine pro-duced by keratinocytes in the epidermis and by neurons in the brain. It has a non-redundant function in skin homoeosta-sis[8]. It shares a common receptor (c-Fms) with MCSF[9]. Although, they shared this common receptor on monocytes, their signal transduction mechanism and biological activity were found to be non-identical[10]. An overlap, however, in the function of IL-34 and MCSF in bone proved IL-34 is important for osteoclastogenesis and macrophage differentia-tion[11]. It has been shown that IL-34 could substitute MCSF entirely for its RANKL-induced osteoclastogenesis[12]. Injec-tion of IL-34 into mice increased the number of osteoclast pre-cursors and enhanced bone resorption[13]. The inflammatory role of IL-34 is elaborated in monocyte activation and in the up-modulation of chemokines [14,15]. Pro-inflammatory cytokines such as tumour necrosis factor alpha (TNFa) and interleukin-1 beta (IL-1b) can stimulate IL-34 expression [16] whereas IL-34 can increase the production of interleukin-17 (IL-17)[17,18]. TNFaand IL-17 are both involved in patho-genesis of psoriasis and inflammatory arthritis like rheumatoid arthritis (RA) and PsA[19,20]. Antibodies against the receptor that block binding of IL-34 and MCSF-1 to (c-Fms) receptors on macrophages has been shown to downregulate peripheral blood monocyte implicated in inflammatory arthritis [21]. Also, it completely blocked osteoclastogenesis and bone ero-sions induced by TNFa injection or inflammatory arthritis [22].

It was previously observed that MCSF in synovial fluid of PsA patients was not elevated to the same extent as in RA[23] even though the inflamed synovium in PsA resembles that of RA[24]. Previous work in RA patients revealed, RA derived fibroblast like synoviocytes and osteoblasts were found to pro-duce IL-34 in response to TNFa [14,25]. This could make us hypothesize that IL-34 may replace MCSF and contribute to pathogenesis of PsA. In this work we aimed to assess serum

IL-34 level as a possible biomarker in psoriasis with or without PsA and to correlate its level with clinical disease activity and severity.

2. Patients and methods

This cross-sectional study included 45 patients diagnosed with psoriasis vulgaris, 21 of whom also had PsA. Patients were randomly recruited from outpatient clinics of Dermatology, Photo-therapy and Physical Medicine and Rheumatology at Ain Shams University Hospital. The control group consisted of 20 healthy age and sex matched volunteers with no history of joint problem and no family history of psoriasis. Both patients and controls had no history suggestive of diabetes, infection, cancer or other chronic inflammatory disease. Patients on steroids, disease modifying drugs or biological therapy for at least the last 6 months were excluded from the study. The study was conducted in accordance with the World Medical Association Declaration of Helsinki for human sub-jects and approved by the ethics committee of the Faculty of Medicine Ain Shams University, and all participants gave us their written informed consent.

Patients were subjected to full history taking and thorough clinical examination including skin, hair, mucous membrane and joint examination. The diagnosis of Psoriasis was made clinically based on characteristic lesions. PsA patients fulfilled the diagnostic criteria defined according to the Classification Criteria for Psoriatic Arthritis (CASPAR)[4].

Functional assessment of the patients was performed according to the

Dermatology life quality index(DLQI): It is a 10-item ques-tionnaire used to assess the effect of a dermatologic condition on a patient’s quality of life (QoL) over the last week. Each question scores 0–3 (total possible score of 0–30). Higher scores present a greater effect on QoL[26].

Modified health assessment questionnaire (MHAQ): con-tains 20 items divided into 8 domains; dressing, grooming, aris-ing, eataris-ing, walkaris-ing, hygiene, reach, grip and common daily activities. Each item has a score range of 0 (no difficulty) to 3 (unable to do). The highest scores are summed (0–24) and divided by the number of scored domains to yield a score from 0 to 3[27].

Psoriasis area and severity index(PASI): was measured for all patients: the PASI measures both surface area and lesional severity of psoriasis. Four items are measured (surface area, severity of erythema [redness], induration [thickness], and desquamation [scale]) evaluated for 4 body areas (head, trunk and upper and lower extremities) assessed separately and then combined using weighting based on the surface area repre-sented by each area (head = 0.1, upper extremities = 0.2, trunk = 0.3, and lower extremities = 0.4). The degree of ery-thema, induration, and scale in each area is judged on a 0–4 scale, the sum of which represents disease severity. The area

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of involvement of each area is graded from 0 to 6, depending on the estimated percentage of lesional area (0 = 0%, 1 = 10%, 2 = 10–29%, 3 = 30–49%, 4 = 50–69%, 5 = 70– 89%, and 6 = 90–100%). Body scores are multiplied by the disease severity score and the weighting for each body area, yielding a score between 0 and 72[28].

Peripheral joint score (PJS): was used to assess peripheral joints with one point for each joint involved (range 0–70). Joint involvement was defined as synovial swelling and/or joint deformity not solely attributed to osteoarthritis[29].

Disease activity was assessed using thecomposite psoriatic disease activity index (CPDAI). Disease involvement was assessed in up to five domains: peripheral joints, skin, enthesi-tis, dactylitis and spinal manifestations. Domains were scored from 0 (uninvolved) to 3 (severe). Peripheral joint score depends on number of joints involved and the presence or absence of impaired function using the health assessment ques-tionnaire (in our work MHAQ score <0.3 was considered nor-mal function). Skin disease score depends on (PASI) and (DLQI). Enthesitis and dactylitis were scored according to the number of involved sites/fingers and the presence or absence of impaired function. Spinal manifestations were scored using Bath ankylosing spondylitis activity index (BAS-DAI)[30]and presence or absence of impaired function. Indi-vidual domain scores were summed giving an overall composite score (range 0–15)[31].

Serum IL-34 level was assessed using quantitative ELISA (enzyme linked immuno-sorbent assay) by (WH-1752, Wkea Med Supplies Corp, Changchun, Jilin, China). 2 ml of venous blood was collected and kept at 70°C until analysed. This assay employs sandwich enzyme immunoassay technique. A monoclonal antibody specific for IL-34 has been pre-coated onto a micro plate. Standards and samples are pipetted into the wells and any IL-34 present is bound by the immobilized antibody. After washing away any unbound substances, an enzyme-linked polyclonal antibody specific for Il-34 is added to the wells. Following a wash to remove any unbound antibody-enzyme reagent, a substrate solution is added to the wells and colour develops in proportion to the amount of IL-34 bound in the initial step. The colour development is stopped and the intensity of the colour is measured.

C-reactive protein (CRP) was measured using latex in patients and controls.

Radiological examination in the patients included: Plain X-ray: postero-anterior view of the hands and feet were obtained for PsA patients. Radiographs were scored for erosions and joint space narrowing (JSN) according to modi-fied Sharp-van der Heijde (mSvH) scoring method for PsA [32]. The maximum score for erosions was 200 for hands and 120 for feet (max. erosions 320). The maximum score for JSN was 160 for hands and 48 for feet (max. JSN 208). Max-imum possible total score is 528.

Dual energy X-ray absorptiometry (DEXA): bone mineral density (BMD) was measured for PsA patients only (as part of their routine workup available at time of study). Instrument used for scans was GE Medical Systems, Lunar (DPX-MD+) at femoral neck and lumbar spine (L1–L4) in anterior and pos-terior projections. By DEXA, results were recorded for each patient as T-scores (difference in SD from the mean of a healthy young adult) and Z-scores (difference in SD from the mean of patients same age and sex). Osteoporosis and

osteope-nia (low bone mass) were defined as T-scores less than 2.5 and T-score between 1 and 2.5 respectively[33].

Statistical analysis: data were coded, tabulated, and statisti-cally analysed using IBM SPSS statistics software version 22.0, IBM Corp., Chicago, USA, 2013. Quantitative data were pre-sented as mean ± SD and range (minimum–maximum) for parametric and as median and 1st–3rd inter-quartile range for non-parametric variables while qualitative data were pre-sented as number and percentage. Comparison of two para-metric quantitative variables was done using independentt -test and by Mann–Whitney U between non-parametric data. Qualitative data were compared using Chi square test for dif-ferences between proportions. Comparison of more than 2 groups was done by analysis of variance (ANOVA). Correla-tions were done using Spearman rho test for numerical non parametric data. Receiver operator characteristic (ROC) curve was used to evaluate the performance of serum IL-34 to differ-entiate PsA patients from those with psoriasis only and sensi-tivity, specificity, positive likelihood ratio (LR), negative LR and diagnostic accuracy of different cut off points were calcu-lated.Pvalue <0.05 was considered significant.

3. Results

The study included 45 patients with psoriasis vulgaris with a mean age of 44.8 ± 9.1 (range: 30.0–63.0) and were 25 males and 20 females; 21 (46.7%) had PsA (group-A) and 24 (53.3%) had psoriasis without arthritis (group-B). 20 age (43.4 ± 7 years; 32–58 years) and gender (7 males and 13 females) matched healthy individuals volunteered as controls. Serum IL-34 was significantly higher among PsA patients (median = 2500 ng/L) compared to patients without arthritis (median = 512 ng/L) and controls (median = 325 ng/L; range: 300–525 ng/L) (p< 0.001); while the difference between those without arthritis and control did not reach significance (Fig. 1). The CRP was negative in the 20 controls. The demo-graphic features, clinical characteristics, functional status and disease activity as well as the serum IL-34 and CRP levels in the psoriatic patients with and without arthritis are presented in Table 1. CPDAI was significantly higher in PsA patients

Figure 1 Comparison between serum interleukin-34 level in psoriasis patients with and without arthritis and normal controls.

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compared to those without arthritis. PsA patients presented with arthritis of 0.5–10 years duration. Fourteen (67%) of them presented with poly-arthritis and 8 of which had con-comitant axial spine affection. Seven of the patients (33%) pre-sented with pauci-articular arthritis and 4 of them had concomitant spine affection. Dactylitis was present in 10 and enthesitis was detected in 14 of the patients. Bone densitometry

of lumbar spine and hip regions revealed that 38% of PsA patients were osteoporotic and 28.5% had osteopenia and 33.3% had normal BMD. Mean Z-scores of PsA patients with different degrees of bone densities and their mean IL-34 serum levels are shown in Table 2. IL-34 was significantly higher among PsA osteoporotic patients compared to those with osteopenia and normal bone density.

Table 1 Demographic features, clinical characteristics, functional status and disease activity as well as the serum IL-34 and CRP levels in the psoriatic patients with and without arthritis.

Variables PsA (N= 21) Psoriasis only (N= 24) P

Age (years) 47.4 ± 10.2 (34–63) 42.5 ± 7.5 (30–60) 0.08 Gender M:F 11:10 (52.4%:47.6%) 14:10 (58.3%:41.7%) 0.69 Ps duration (years) 10 (4.5–22.5) 4.5 (2–11.3) 0.008 PASI 10.9 (9.1–22.4) 10 (4.2–14.7) 0.23 Nail involvement 14 (66.7%) 2 (8.3%) <0.001 MHAQ 1 (0.6–1.4) 0.5 (0–1) 0.013 DLQI 13 (9–25) 0 (0–11) 0.002 CPDAI 10 (6.5–11) 1.5 (1–2) <0.001 IL-34 (ng/L) 2500 (1100–2525) 512.5 (300–1000) <0.001 +ve CRP 8 (38.1%) 6 (25%) 0.34

Results are presented as mean ± SD, median (inter-quartile range) orn(%). Ps, psoriasis; PASI, psoriasis skin area severity index; MHAQ, modified health assessment questionnaire; DLQI, dermatology life quality index; CPDAI, composite psoriasis disease activity index; IL-34, interleukin-34; CRP, C-reactive protein. Bold values are significant atp< 0.05.

Table 2 Interleukin-34 level in different grades of bone mineral density in psoriatic arthritis patients.

BMD in PsA patients (n= 21) P

Normal (n= 7) Osteopenia (n= 6) Osteoporosis (n= 8)

IL-34 level (ng/L) 1750 (1000–2500) 1200 (1000–1875) 2550 (2500–2550) <0.001

Z-score Lumbar 0.7 ( 0.9 to 0.4) 1.6 ( 2.0 to 0.4) 2.8 ( 2.9 to 2.7) <0.001

Hip 0.3 ( 0.5 to 0.1) 1.2 ( 1.7 to 0.1) 2.1 ( 2.2 to 2.0) <0.001

Results are expressed as median (inter-quartile range). BMD. bone mineral density; PsA: psoriatic arthritis; IL-34: interleukin-34. Bold values are significant atp< 0.05.

Table 3 Correlation between serum IL-34 and some clinical and radiological findings in psoriatic patients with and without arthritis. Serum IL-34 (ng/L)

Variablesr(p) PsA (N= 21) Psoriasis only (N= 24)

Ps duration 0.23 (0.25) 0.25 (0.24) PASI 0.92 (<0.001) 0.74 (<0.001) MHAQ 0.91 (<0.001) 0.71 (<0.001) DLQI 0.65 (<0.001) 0.75 (<0.001) Arthritis duration 0.62 (0.003) NA NA Dactylitis 0.82 (<0.001) NA NA Enthesitis 0.01 (0.95) NA NA PJS 0.63 (0.002) NA NA BASDAI 0.84 (<0.001) NA NA CPDAI 0.78 (<0.001) 0.63 (<0.001) mSvH score 0.28 (0.22) NA NA

DXA Lumbar spine 0.5 (0.02) NA NA

Hip joint 0.56 (0.008) NA NA

Ps, psoriasis; PASI, psoriasis skin area severity index; MHAQ, modified health assessment questionnaire; DLQI, dermatology life quality index; PJS, peripheral joint score, dactylitis, enthesitis; BASDAI, bath ankylosing spondylitis disease activity index; CPDAI, composite psoriasis disease activity index; mSvH, modified Sharp van der Heijde score; DXA, dual energy X-ray absorptiometry; Bold values are significant at

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Correlations detected between serum IL-34 and some clin-ical and radiologclin-ical findings in psoriatic patients with and without arthritis are shown in Table 3. Correlation between IL-34 and CPDAI among PsA patients is shown inFig. 2.

The diagnostic performance of serum IL-34 level to differ-entiate patients with and without arthritis using ROC curve analysis revealed that it was excellent with a high sensitivity and specificity and an area under curve (0.901) (Fig. 3). Serum IL-34 level cut off value atP1750 ng/L showed a specificity of 100% (95% CI 87–100%), sensitivity of 66.7% (95% CI 51.8– 66.7%), positive LR 10 (4–10), negative LR 0.3 (0.3–0.6) and a diagnostic accuracy of 84.4% (70.6–84.4%). Serum IL-34 level cut off value at P1000 ng/L showed a specificity of 54.2% (95% CI 41–54.2%), sensitivity of 100% (95% CI 85–100%), positive LR 2.2 (1.4–2.2), negative LR 0 (0–0.4) and a diagnos-tic accuracy of 75.6% (61.5–75.6%).

4. Discussion

Interleukin-34 is a cytokine essential for skin homoeostasis[8]. It is involved in macrophage differentiation, osteoclastogenesis and inflammation[11,14–17]. In our study serum IL-34 level was significantly higher among PsA patients compared to those without arthritis and normal controls. This is in accor-dance with previous work on inflammatory arthritis like RA and ankylosing spondylitis where IL-34 was elevated in serum of patients[18,34]. The CRP value was significantly higher in patients compared to controls. In the work of Tian et al.[18] on RA patients, a significant positive correlation was found between IL-34 levels and inflammation variables including CRP.

In the present work, duration of psoriasis as well as nail involvement was significantly higher in PsA compared to patients without arthritis. Skin lesions usually precede articu-lar symptoms in more than 75–80% of patients with PsA [35]. Also, nail changes are observed in about 40% of psoriasis patients, and this percentage increases to about 80% in PsA [36]. The PASI was not significantly different between PsA and psoriasis only patients. However, functional capacity indices measured in our patients using MHAQ and DLQI were significantly higher among PsA compared to psoriasis only patients. PASI measures disease severity at the time of assess-ment and does not provide any information about the patient’s psychological and mental well-being. In fact, two patients with similar PASI score, may be affected quite differently by their disease [37,38] and attributed to cumulative effect of skin and joint involvement, QoL and functioning may be further impaired in patients with PsA.

In this study composite psoriasis disease activity index (CPDAI) was significantly higher in PsA patients compared to those without arthritis. This could be also attributed to involvement of skin as well as joints and enthesis in PsA[39]. A significant correlation was also detected in this work between serum IL-34 level and PASI score, functional indices

Figure 2 Correlation between serum interleukin-34 level and composite psoriasis disease activity index (CPDAI) among psori-atic arthritis patients.

Figure 3 Receiver operator characteristic (ROC) curve showing the efficacy of serum IL-34 level in differentiation between psoriatic patients with and without arthritis and the suggested cut off values. (1) ROC curve showed high sensitivity and specificity. Area under curve (AUC) = (0.901) at 95% CI = (0.82–0.99) (p< 0.001). (2) Group A = psoriatic arthritis, Group B = psoriasis only. At the cut off valueP1000 ng/L, the sensitivity and specificity were 100% (95% CI: 85–100%) and 54.2% (95% CI: 41–54.2%) respectively. At the cut off valuesP1750 ng/L were 66.7% (51.8–66.7%) and 100% (87–100%) respectively.

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and CPDAI in both groups of patients. Also in PsA group, a significant correlation was detected between serum IL-34 and each of BASDAI, PJS and dactylitis score. This signifies its association with psoriatic disease activity especially arthritis. A significant relation was found between IL-34 levels in RA patients and disease activity[18].

Regarding severity of arthritis, in our work no significant correlation was detected between IL-34 serum level and radio-graphic joint damage scores in the hands and feet calculated using the mSvH score in PsA patients. This could be attributed to long duration of un-treated arthritis and the different clini-cal presentations of arthritis in our patients which didn’t give us a better chance for comparison of patients with and without erosions. Moreover, no follow up for radiographic progression was done in our work. Previous work of Moon et al.[17]in RA patients revealed no relation between serum IL-34 level and radiological joint damage scores. However, another study revealed a significant correlation with radiographic progres-sion using mSvH score[40].

In this study BMD was measured in PsA patients knowing it’s a limitation of the study but previous work in psoriasis and PsA patients revealed they did not present with low BMD compared to controls[41]. However Attia et al. in their work demonstrated significant lower bone density in PsA patients compared to those without arthritis and normal controls, and the risk of osteoporosis in PsA patients increased with the increase in number of arthritic joints[42]. Significant neg-ative correlation was detected between IL-34 serum level in PsA patients and Z-score of lumbar spine and hip joint. Previ-ous work in vitro showed that IL-34 could promote osteoclas-togenesis and bone resorption[13,43]. In our study IL-34 mean serum level was highest among PsA patients with osteoporosis. Previous work on RA patients revealed a significant correla-tion between serum IL-34 levels and degree of osteoporosis [40]. However, Moon et al. in their work found no relation between serum IL-34 level and systemic osteoporosis[17].

The present work revealed a correlation between serum IL-34 level and systemic bone loss but not radiographic damage scores in PsA patients. Dalbeth et al.[44]revealed that MCSF (cytokine which shares receptor with IL-34) correlated with radiographic damage scores but not with total hip BMD in PsA patients[44]. These findings suggest further studies could emphasize the role of each IL-34 and MCSF in bone resorp-tion in PsA.

In this study ROC curve analysis revealed; increased sensi-tivity and specificity of serum IL-34 as a marker for arthritis in psoriasis patients. The cut-off value of (IL-34P1750 ng/L) was highly specific for confirming PsA in psoriasis patients. The cut off value of (IL-34P1000 ng/L) was more sensitive for early detection of positive arthritic cases. We suggest fur-ther evaluation of serum IL-34 as a diagnostic and screening marker for suspected PsA in a larger number of psoriasis patients. It would help with early detection and management of arthritis.

In conclusion; serum IL-34 could be a new marker for PsA disease activity. Serum IL-34 was significantly higher in PsA patients compared to those without arthritis and normal con-trols. Serum IL-34 showed a significant correlation with PASI, CPDAI and systemic bone loss but showed no relation to radi-ological joint damage scores in PsA.

Conflict of interest None.

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Figure

Table 3 Correlation between serum IL-34 and some clinical and radiological findings in psoriatic patients with and without arthritis.
Figure 3 Receiver operator characteristic (ROC) curve showing the efficacy of serum IL-34 level in differentiation between psoriatic patients with and without arthritis and the suggested cut off values

References

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