Abstract
OBJECTIVES:
Psoriasis is a hyperproliferative chronic inflammatory skin disease of unknown etiology and ocular structures and visual pathways can also be affected during the course of this disease. Subclinical optic neuritis has previously been observed in psoriatic patients in visual evoked potential studies. This trial was designed to evaluate retinal sensitivity in patients with psoriasis vulgaris.
METHODS:
A total of 40 eyes of 40 patients with chronic plaque-type psoriasis and 40 eyes of 40 age- and sex-matched control subjects were included in this study. The diagnosis of psoriasis was confirmed by skin biopsy. The severity was determined using the Psoriasis Area and Severity Index and the duration of the disease was recorded. After a full ophthalmological examination, including tests for color vision and pupil reactions, the visual field of each subject was assessed using both standard achromatic perimetry and short wavelength automated perimetry.
RESULTS:
The mean Psoriasis Area and Severity Index was 22.05±6.40′. There were no significant differences in the visual field parameters of subjects versus controls using either method. There were correlations between disease severity and the mean deviations in standard achromatic perimetry and short wavelength automated perimetry and between disease severity and the corrected pattern standard deviation and pattern standard deviation of short wavelength automated perimetry (r = -0.363, r = -0.399, r = 0.515 and r = 0.369, respectively).
CONCLUSIONS:
Retinal sensitivity appears to be affected by the severity of psoriasis vulgaris.
Psoriasis; Psoriasis Area and Severity Index; Standard Achromatic Perimetry; Short Wavelength Automated Perimetry; Visual Field
INTRODUCTION
Psoriasis is a hyperproliferative chronic inflammatory skin disease of unknown
etiology. It is characterized by red and scaly plaques caused by epidermal
hyperproliferation. It has a complex pathogenesis including immune system
alterations and systemic and/or local factors. Psychological stress, focal
infections and some drugs as well as the activation of leucocytes, which control
cellular immunity and T cell-dependent inflammatory processes, cause the growth of
epidermal and vascular cells in psoriatic skin lesions (11. Lowes MA, Bowcock AM, Krueger JG. Pathogenesis and therapy of
psoriasis. Nature. 2007;445(7130):866-73,
http://dx.doi.org/10.1038/nature05663.
http://dx.doi.org/10.1038/nature05663...
2. Coimbra S, Figueiredo A, Santos-Silva A. Brodalumab: an
evidence-based review of its potential in the treatment of moderate-to-severe
psoriasis_Core Evid. 2014;21(9):89-97,
http://dx.doi.org/10.2147/CE.S33940.
http://dx.doi.org/10.2147/CE.S33940...
3. Peter CM, van de Kerkhof, PEJ van Erp. Pathogenesis; in Peter CM.
van de Kerkhof (ed):Textbook of Psoriasis 2nd edt. Blackwell
publishing: UK, 2003 pp 83-109.
4. Her Y, Lim JW, Han SH. Dry eye and tear film functions in
patients with psoriasis. Jpn J Ophthalmol.
2013;57(4):341-6.
5. Rich SJ, Bello-Quintero CE. Advancements in the treatment of
psoriasis: role of biologic agents. J Manag Care Pharm.
2004;10(4):318-25.-66. Schottelius AJ, Moldawer LL, Dinarello CA, Asadullah K, et al.
Biology of tumor necrosis factor-alpha- implications for psoriasis. Exp
Dermatol. 2004;13(4):193-222,
http://dx.doi.org/10.1111/j.0906-6705.2004.00205.x.
http://dx.doi.org/10.1111/j.0906-6705.20...
).
Ocular structures and visual pathways can also be affected in patients suffering from
psoriasis (44. Her Y, Lim JW, Han SH. Dry eye and tear film functions in
patients with psoriasis. Jpn J Ophthalmol.
2013;57(4):341-6.,77. Rehal B, Modjtahedi BS, Morse LS, Schwab IR, Maibach HI. Ocular
psoriasis. J Am Acad Dermatol. 2011;65(6):1202-12,
http://dx.doi.org/10.1016/j.jaad.2010.10.032.
http://dx.doi.org/10.1016/j.jaad.2010.10...
). Subclinical optic neuritis has previously been shown in psoriatic
patients in visual evoked potential studies. Elongation of P100 latency and a
reduction in the response amplitude, which designate myelin and axonal involvement
of the optic nerve, have also been observed (88. Grzybowski A, Grzybowski G, Druzdz A, Zaba R. Visual evoked
potentials in patients with psoriasis vulgaris. Doc Ophthalmol.
2001;103(3):187-94, http://dx.doi.org/10.1023/A:1013059807998.
http://dx.doi.org/10.1023/A:101305980799...
,99. Perossini M, Turio E, Perossini T, Romagnoli M, et al. Pattern
VEP alterations in psoriatic patients may indicate a sub clinic optic neuritis.
Doc Ophthalmol. 2005;110(2-3):203-7,
http://dx.doi.org/10.1007/s10633-005-4830-1.
http://dx.doi.org/10.1007/s10633-005-483...
). Electroretinography
responses revealed impairment in overall retinal electrophysiologic functions (1010. Shoeibi N, Taheri AR, Nikandish M, Omidtabrizi A, Khosravi N.
Electrophysiologic evaluation of retinal function in patients with psoriasis and
vitiligo. Doc Ophthalmol. 2014;128(2):131-6,
http://dx.doi.org/10.1007/s10633-014-9425-2.
http://dx.doi.org/10.1007/s10633-014-942...
). Visual field assessment is a functional
measurement method that documents central and peripheral sensitivity of the retina
in both pathological and normal situations (1111. Menghini M, Duncan JL. Diagnosis and complementary examinations;
Casaroli -Marano RP, Zarbin MA (eds): Cell-Based Therapy for Retinal
Degenerative Disease. Dev Ophthalmol, Basel, Karger. 2014,
pp:53-61.). Standard achromatic perimetry (SAP) and short wavelength automated
perimetry (SWAP) use white and blue light stimuli, respectively, of different sizes
and intensities to evaluate the retinal sensitivity and SWAP was found to be more
sensitive for detecting early visual field changes. In light of these findings, the
objective of this study was to examine the visual field in psoriatic patients
without any pathology of the retina and/or optic nerve with the aim of evaluating
retinal sensitivity.
MATERIALS AND METHODS
A total of 40 eyes of 40 patients with newly diagnosed plaque-type psoriasis and 40 eyes of 40 age- and sex-matched control subjects were included in the study. The diagnosis of psoriasis was based on both histopathological and clinical findings. The severity was determined using the Psoriasis Area and Severity Index (PASI) and the duration of the disease recorded. Possible reasons for exclusion included the following: a history of neurological diseases, space-occupying lesions, optic neuropathy, high refractive errors, glaucoma, retinal pathology, color vision defects and cataracts, the use of systemic and/or topical retinoic acid or immunosuppressive medication, and undergoing ultraviolet therapy. Each patient underwent a full ophthalmological examination, including measurement of pupil reactions and application of the Ishihara test for color vision.
All visual field tests were performed using the central 30-2 threshold strategy with a Humphrey Field Analyzer (750i; Humphrey Instruments, San Leandro, California, USA) with SAP (using a Goldmann size III stimulus) and SWAP (using a Goldmann size V stimulus). Each test was performed by the same technician and the patients were instructed to rest before the examination of the other eye. For each subject, only one eye with reliable visual field parameters (fixation loss of less than 20%, false positive rate of less than 33%, false negative rate of less than 33%) was included in the study. Global indices (mean deviation (MD), pattern standard deviation (PSD), short-term fluctuation (SF) and corrected pattern standard deviation (CPSD)) were evaluated. This study was conducted according to the guidelines of the Declaration of Helsinki and patients provided their informed consent after the nature and purpose of the study were fully explained to them.
The Kolmogorov-Smirnov test was used to evaluate whether the variables were normally distributed. A two-tailed independent samples t test was used to compare the ophthalmologic parameters between the experimental and control groups. A paired sample t-test was used to compare the ophthalmologic parameters between the SAP and SWAP methods (separately for each group). A repeated measures two-way ANOVA was used to analyze differences in the methods between the experimental and control groups. The Pearson correlation coefficient was calculated to determine the significance of the association between two random variables. Continuous variables are presented as the mean±standard deviation. Categorical variables were compared using the chi-square test and presented as numerical variables and percentages. A p-value of <0.05 was considered significant. Analyses were performed using commercial software (IBM SPSS Statistics 19; SPSS Inc., an IBM Co., Somers, NY, USA).
RESULTS
Demographic data are summarized in Table 1. There were no statistically significant intergroup differences in the age or gender of the patients. None of the study patients has systemic signs of psoriasis. The ophthalmologic examinations, including color vision tests and pupil reactions, revealed unremarkable results in both groups. The best corrected visual acuity was 20/20 in both study groups and none of the study subjects presented with retinal and/or optic nerve pathology or ocular pathology. The visual field parameters are summarized in Table 2. No significant differences were observed between the two groups; however, correlations were noted between disease severity (PASI) and the mean deviations of SAP and SWAP and between PASI and the CPSD and PSD of SWAP (r = -0.363, r = -0.399, r = 0.515, and r = 0.369, respectively) (Table 3).
DISCUSSION
Psoriasis is an organ-specific autoimmune disease that is characterized by
exacerbation and remission (11. Lowes MA, Bowcock AM, Krueger JG. Pathogenesis and therapy of
psoriasis. Nature. 2007;445(7130):866-73,
http://dx.doi.org/10.1038/nature05663.
http://dx.doi.org/10.1038/nature05663...
,44. Her Y, Lim JW, Han SH. Dry eye and tear film functions in
patients with psoriasis. Jpn J Ophthalmol.
2013;57(4):341-6.). Psoriasis activity increases with
psychological stress, which has been explained by the common origin of keratinocytes
and nervous cells during embryogenesis (33. Peter CM, van de Kerkhof, PEJ van Erp. Pathogenesis; in Peter CM.
van de Kerkhof (ed):Textbook of Psoriasis 2nd edt. Blackwell
publishing: UK, 2003 pp 83-109.,88. Grzybowski A, Grzybowski G, Druzdz A, Zaba R. Visual evoked
potentials in patients with psoriasis vulgaris. Doc Ophthalmol.
2001;103(3):187-94, http://dx.doi.org/10.1023/A:1013059807998.
http://dx.doi.org/10.1023/A:101305980799...
,99. Perossini M, Turio E, Perossini T, Romagnoli M, et al. Pattern
VEP alterations in psoriatic patients may indicate a sub clinic optic neuritis.
Doc Ophthalmol. 2005;110(2-3):203-7,
http://dx.doi.org/10.1007/s10633-005-4830-1.
http://dx.doi.org/10.1007/s10633-005-483...
). Any part of the eye may be affected by psoriasis: the
eyelids, conjunctiva, cornea, uvea, retina, optic nerve and lens may be involved in
the disease process. Ocular symptoms are reported to occur during exacerbation of
the disease (44. Her Y, Lim JW, Han SH. Dry eye and tear film functions in
patients with psoriasis. Jpn J Ophthalmol.
2013;57(4):341-6.,77. Rehal B, Modjtahedi BS, Morse LS, Schwab IR, Maibach HI. Ocular
psoriasis. J Am Acad Dermatol. 2011;65(6):1202-12,
http://dx.doi.org/10.1016/j.jaad.2010.10.032.
http://dx.doi.org/10.1016/j.jaad.2010.10...
). The current gold standard for the assessment of psoriasis
severity is PASI, which evaluates the redness, thickness and scaliness of the
lesions. PASI is a scoring system that takes into account the localization, extent
and severity of the skin signs and provides a single score for psoriasis severity
ranging from 0 to 72 (1212. Langley RG, Ellis CN. Evaluating psoriasis with Psoriasis Area
and Severity Index, Psoriasis Global Assessment, and Lattice System
Physician's Global Assessment. J Am Acad Dermatol. 2004;51(4):563-9,
http://dx.doi.org/10.1016/j.jaad.2004.04.012.
http://dx.doi.org/10.1016/j.jaad.2004.04...
13. Carlin CS, Feldman SR, Krueger JG, Menter A, Krueger GG. A 50%
reduction in the Psoriasis Area and Severity Index (PASI 50) is a clinically
significant endpoint in the assessment of psoriasis. J Am Acad Dermatol.
2004;50(6):859-66,
http://dx.doi.org/10.1016/j.jaad.2003.09.014.
http://dx.doi.org/10.1016/j.jaad.2003.09...
-1414. Schäfer I, Hacker J, Rustenbach SJ, Radtke M, Franzke N,
Augustin M. Concordance of the Psoriasis Area and Severity Index (PASI) and
patient-reported outcomes in psoriasis treatment. Eur J Dermatol.
2010;20(1):62-7.).
Abnormalities in the visual field may be observed in patients with normal central
vision. In recent years, the sensitivity of SWAP was compared to that of SAP. SWAP
was found to be more sensitive for detecting early glaucomatous and
neuro-ophthalmologic visual field changes and was able to reveal functional
abnormalities in the retina and optic nerve in patients with normal ocular
structures (1515. Wild JM. Short wavelenght automated perimetry. Acta Ophthalmol
Scan. 2001;79(6):546-59,
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16. Heijl A. Ordering a test; in Heijl A (ed): Essential Perimetry
3th edt. Jena: Germany: Carl Zeiss Meditec Inc., 2002. pp
25-43.
17. Keltner JL, Johnson CA. Short-wavelength automated perimetry in
neuro-ophthalmologic disorders. Arch Ophthalmol. 1995;113(4):475-81,
http://dx.doi.org/10.1001/archopht.1995.01100040095033.
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-1818. Fujimoto N, Kubota M, Saeki N, Adachi-Usami E. Use of
blue-on-yellow perimetry for detection of sectoranopia. Eye. 2004;18(3):338-41,
http://dx.doi.org/10.1038/sj.eye.6700665.
http://dx.doi.org/10.1038/sj.eye.6700665...
).
To the best of our knowledge, the visual field has not yet been studied in psoriasis patients. We evaluated the visual field of the study group using both SAP and SWAP and we did not detect any statistically significant difference between patients and controls; however, we found a correlation between the visual field parameters and PASI. Our study group consisted of patients with moderate psoriasis, which might explain the statistically insignificant intergroup difference in the visual field parameters. When we examined the correlation between visual field parameters and disease activity and severity, we found a negative correlation between the MD of both visual field analyses and PASI. Retinal sensitivity appears to decrease when psoriasis is exacerbated. We also found that the CPSD and PSD of SWAP were positively correlated with PASI, which may indicate localized defects in the visual field during exacerbation periods. SWAP appears to be more sensitive for detecting early functional changes in severe and active psoriasis.
Psoriasis is known as a skin disease and it has been shown to have a complex
pathophysiology and a strong relationship with proinflammatory cytokines, including
tumor necrosis factor-alpha (TNF-α), interferon-gamma (IFN-γ) and
interleukins 6 and 8 (IL-6 and IL-8). Although one of the limitations of the current
study is the lack of data regarding plasma proinflammatory cytokine levels of the
study subjects, the role of cytokines has been extensively studied in patients with
psoriasis. Serum TNF-α and IFN-γ levels were significantly higher in
patients with active psoriasis and these high serum levels were positively
correlated with the clinical severity and activity of the disease (1919. Abdel-Hamid MF, Aly DG, Saad NE, Emam HM, Emam HM, Ayoub DF.
Serum levels of interleukin-8, tumor necrosis factor-α and
γ-interferon in Egyptian psoriatic patients and correlation with disease
severity. J Dermatol. 2011;38(5):442-6,
http://dx.doi.org/10.1111/j.1346-8138.2010.01018.x.
http://dx.doi.org/10.1111/j.1346-8138.20...
,2020. Arican O, Aral M, Sasmaz S, Ciragil P. Serum levels of
TNF-alpha, IFN-gamma, IL-6, IL-8, IL-12, IL-17, and IL-18 in patients with
active psoriasis and correlation with disease severity. Mediators Inflamm.
2005;24(5):273-9, http://dx.doi.org/10.1155/MI.2005.273.
http://dx.doi.org/10.1155/MI.2005.273...
).
The serum levels of these cytokines were reported to serve as a follow-up marker for
monitoring disease severity (1919. Abdel-Hamid MF, Aly DG, Saad NE, Emam HM, Emam HM, Ayoub DF.
Serum levels of interleukin-8, tumor necrosis factor-α and
γ-interferon in Egyptian psoriatic patients and correlation with disease
severity. J Dermatol. 2011;38(5):442-6,
http://dx.doi.org/10.1111/j.1346-8138.2010.01018.x.
http://dx.doi.org/10.1111/j.1346-8138.20...
,2020. Arican O, Aral M, Sasmaz S, Ciragil P. Serum levels of
TNF-alpha, IFN-gamma, IL-6, IL-8, IL-12, IL-17, and IL-18 in patients with
active psoriasis and correlation with disease severity. Mediators Inflamm.
2005;24(5):273-9, http://dx.doi.org/10.1155/MI.2005.273.
http://dx.doi.org/10.1155/MI.2005.273...
). Overexpression of TNF-α has been
demonstrated in the plasma and skin lesions of psoriatic patients (11. Lowes MA, Bowcock AM, Krueger JG. Pathogenesis and therapy of
psoriasis. Nature. 2007;445(7130):866-73,
http://dx.doi.org/10.1038/nature05663.
http://dx.doi.org/10.1038/nature05663...
,55. Rich SJ, Bello-Quintero CE. Advancements in the treatment of
psoriasis: role of biologic agents. J Manag Care Pharm.
2004;10(4):318-25.,66. Schottelius AJ, Moldawer LL, Dinarello CA, Asadullah K, et al.
Biology of tumor necrosis factor-alpha- implications for psoriasis. Exp
Dermatol. 2004;13(4):193-222,
http://dx.doi.org/10.1111/j.0906-6705.2004.00205.x.
http://dx.doi.org/10.1111/j.0906-6705.20...
,1919. Abdel-Hamid MF, Aly DG, Saad NE, Emam HM, Emam HM, Ayoub DF.
Serum levels of interleukin-8, tumor necrosis factor-α and
γ-interferon in Egyptian psoriatic patients and correlation with disease
severity. J Dermatol. 2011;38(5):442-6,
http://dx.doi.org/10.1111/j.1346-8138.2010.01018.x.
http://dx.doi.org/10.1111/j.1346-8138.20...
,2020. Arican O, Aral M, Sasmaz S, Ciragil P. Serum levels of
TNF-alpha, IFN-gamma, IL-6, IL-8, IL-12, IL-17, and IL-18 in patients with
active psoriasis and correlation with disease severity. Mediators Inflamm.
2005;24(5):273-9, http://dx.doi.org/10.1155/MI.2005.273.
http://dx.doi.org/10.1155/MI.2005.273...
) and
anti-TNF-α therapy has gained popularity in recent years (11. Lowes MA, Bowcock AM, Krueger JG. Pathogenesis and therapy of
psoriasis. Nature. 2007;445(7130):866-73,
http://dx.doi.org/10.1038/nature05663.
http://dx.doi.org/10.1038/nature05663...
,66. Schottelius AJ, Moldawer LL, Dinarello CA, Asadullah K, et al.
Biology of tumor necrosis factor-alpha- implications for psoriasis. Exp
Dermatol. 2004;13(4):193-222,
http://dx.doi.org/10.1111/j.0906-6705.2004.00205.x.
http://dx.doi.org/10.1111/j.0906-6705.20...
).
TNF-α, an immunomediator and proinflammatory cytokine, is a potent neurotoxic
substance that induces apoptotic cell death (2121. Tezel G, Li LY, Patil RV, Wax MB. TNF-alpha and TNF-alpha
receptor-1 in the retina of normal and glaucomatous eyes. Invest Ophthalmol Vis
Sci. 2001;42(8):1787-94.
22. Tezel G, Yang X, Yang J, Wax MB. Role of tumor necrosis factor
receptor-1 in the death of retinal ganglion cells following optic nerve crush
injury in mice. Brain Res. 2004;996(2):202-12,
http://dx.doi.org/10.1016/j.brainres.2003.10.029.
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24. Bai Y, Shi Z, Zhuo Y, Liu J, Malakhov A, Ko E, Burgess K, et al.
In glaucoma the upregulated truncated TrkC.T1 receptor isoform in glia causes
increased TNF-alpha production, leading to retinal ganglion cell death. Invest
Ophthalmol Vis Sci. 2010;51(12):6639-51,
http://dx.doi.org/10.1167/iovs.10-5431.
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treatments. Prog Retin Eye Res. 2002;21(5):465-84,
http://dx.doi.org/10.1016/S1350-9462(02)00012-5.
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). IFN-γ plays an
important role in autoimmune and infectious diseases (2626. Egwuagu CE, Mahdi RM, Chan CC, Sztein J, Li W, Smith JA, et al.
Expression of interferon-gamma in the lens exacerbates anterior uveitis and
induces retinal degenerative changes in transgenic Lewis rats. Clin Immunol.
1999;91(2):196-205, http://dx.doi.org/10.1006/clim.1999.4701.
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apoptosis in the retinal ganglion cell layer, resulting in photoreceptor loss and
disturbance of the axonal transport system of the affected neurons (2626. Egwuagu CE, Mahdi RM, Chan CC, Sztein J, Li W, Smith JA, et al.
Expression of interferon-gamma in the lens exacerbates anterior uveitis and
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Transgenic mice expressing IFN-gamma in the retina develop inflammation of the
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In addition, IL-8 induced cell death in cultured neurons, while IL-6 stimulated
oxidative stress (2828. Huang P, Zhang SS, Zhang C. The two sides of cytokine signaling
and glaucomatous optic neuropathy. J Ocul Biol Dis Infor. 2009;2(2):78-83,
http://dx.doi.org/10.1007/s12177-009-9026-6.
http://dx.doi.org/10.1007/s12177-009-902...
29. Kuchtey J, Rezaei KA, Jaru-Ampornpan P, Sternberg P Jr, Kuchtey
RW. Multiplex cytokine analysis reveals elevated concentration of interleukin-8
in glaucomatous aqueous humor. Invest Ophthalmol Vis Sci. 2010;51(12):6441-7,
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30. Thirumangalakudi L, Yin L, Rao HV, Grammas P. IL-8 induces
expression of matrix metalloproteinases, cell cycle and pro-apoptotic proteins,
and cell death in cultured neurons. J Alzheimers Dis.
2007;11(3):305-11.-3131. Wu WC, Hu DN, Gao HX, Chen M, Wang D, Rosen R, et al. Subtoxic
levels hydrogen peroxide-induced production of interleukin-6 by retinal pigment
epithelial cells. Mol Vis. 2010;16:1864-73.). The neurotoxic effects of these proinflammatory cytokines
have been implicated in the pathogenesis of several central nervous system diseases,
retinal ganglion cell damage and optic nerve crush (2121. Tezel G, Li LY, Patil RV, Wax MB. TNF-alpha and TNF-alpha
receptor-1 in the retina of normal and glaucomatous eyes. Invest Ophthalmol Vis
Sci. 2001;42(8):1787-94.,2222. Tezel G, Yang X, Yang J, Wax MB. Role of tumor necrosis factor
receptor-1 in the death of retinal ganglion cells following optic nerve crush
injury in mice. Brain Res. 2004;996(2):202-12,
http://dx.doi.org/10.1016/j.brainres.2003.10.029.
http://dx.doi.org/10.1016/j.brainres.200...
,2828. Huang P, Zhang SS, Zhang C. The two sides of cytokine signaling
and glaucomatous optic neuropathy. J Ocul Biol Dis Infor. 2009;2(2):78-83,
http://dx.doi.org/10.1007/s12177-009-9026-6.
http://dx.doi.org/10.1007/s12177-009-902...
).
The inflammatory response and likely the increased plasma levels of circulating proinflammatory cytokines, in active and severe psoriasis seem to affect retinal functions and decrease retinal sensitivity. Although the main target of psoriasis is the skin, based on the results of the current study, patients with psoriasis should undergo regular ophthalmological examinations to examine their retinal functions and identify potential ocular involvement. Additional studies with a larger number of participants should be performed to evaluate the retinal involvement and roles of these cytokines in psoriatic patients.
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No potential conflict of interest was reported.
Publication Dates
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Publication in this collection
Jan 2015
History
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Received
26 Sept 2014 -
Reviewed
7 Nov 2014 -
Accepted
7 Nov 2014