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Clinical Characteristics of Pruritus in Patients with Scalp Psoriasis and Their Relation with Intraepidermal Nerve Fiber Density

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Clinical Characteristics of Pruritus in Patients with Scalp Psoriasis and Their Relation with Intraepidermal Nerve Fiber Density Assessment of Pruritus in Scalp Psoriasis Ann Dermatol Vol. 26, No. 6, 2014 http://dx.doi.org/10.5021/ad.2014.26.6.727 ORIGINAL ARTICLE Clinical Characteristics of Pruritus in Patients with Scalp Psoriasis and Their Relation with Intraepidermal Nerve Fiber Density Tae-Wook Kim1, Woo-Haing Shim1, Joung-Min Kim1, Je-Ho Mun1, Margaret Song1, Hoon-Soo Kim1, Hyun-Chang Ko1,3, Moon-Bum Kim1,2, Byung-Soo Kim1,2 1Department of Dermatology, Pusan National University School of Medicine, 2Biomedical Research Institute, Pusan National University Hospital, Busan, 3Research Institute for Convergence of Biomedical Science and Technology, Pusan National University Yangsan Hospital, Yangsan, Korea Background: The scalp is frequently affected in psoriasis between IENF density and PSSI score, and IENF density and patients, and pruritus can adversely affect the quality of life pruritus intensity were insignificant. Conclusion: These of affected patients. Few studies have assessed pruritus in results indicate that pruritus prevalence is high in patients scalp psoriasis. Objective: To determine the correlation with scalp psoriasis, and pruritus considerably influences the among the clinical characteristics of pruritus, psoriasis scalp patients’ daily lives and quality of life. In addition, high IENF severity index (PSSI), and intraepidermal nerve fiber (IENF) density in psoriatic scalp lesions may play a role in the density in psoriatic scalp lesions. Methods: Eighty patients development of pruritus in scalp psoriasis. (Ann Dermatol (53 men, 27 women; mean age, 46.4 years; mean PSSI, 19.9) 26(6) 727∼732, 2014) with scalp psoriasis were evaluated by using the PSSI and the Leuven itch scale. Biopsies were obtained from the lesional -Keywords- and nonlesional skin of 19 patients (10 men, 9 women; mean Nerve fibers, Pruritus, Psoriasis, Scale, Scalp dermatoses age, 37.8 years; mean PSSI, 25.8). Immunofluorescence staining of protein gene product 9.5 was performed to determine the IENF density. Results: Sixty-four patients (80%) complained of pruritus associated with scalp INTRODUCTION psoriasis, which negatively affected their quality of life to Pruritus is the most common symptom of dermatologic varying degrees. A moderate positive relation between PSSI disorders. Previous studies have reported that pruritus score and pruritus intensity was identified (r=0.225 and frequency is associated with psoriasis severity to varying p=0.044). The IENF density in psoriatic lesions was degrees1,2. Many possible mediators have been suggested significantly higher than that in the nonlesional scalp to transmit or modulate pruritus in psoriasis; however, the (6.2±1.2 vs. 4.2±1.6, p＜0.001). However, the correlations precise mechanism and the mediators involved are still unclear3. Neurogenic factors, including altered innervat- Received November 6, 2013, Revised February 6, 2014, Accepted for ions, neuropeptides, opioids, and nerve growth factors publication March 14, 2014 (NGFs), have been implicated as important mediators in Corresponding author: Byung-Soo Kim, Department of Dermatology, psoriatic skin4. Nakamura et al.4 reported high numbers of Pusan National University School of Medicine and Biomedical Research Institute, Pusan National University Hospital, 179 protein gene product 9.5 (PGP 9.5)-immunoreactive nerve Gudeok-ro, Seo-gu, Busan 602-739, Korea. Tel: 82-51-240-7338, Fax: fibers in the epidermis and upper dermis, and of 82-51-245-9467, E-mail: [email protected] perivascular nerve fibers containing substance P (SP) in This is an Open Access article distributed under the terms of the psoriatic lesions. These findings indicate that hyperinner- Creative Commons Attribution Non-Commercial License (http:// vation in psoriatic lesions is involved in the pathogenesis creativecommons.org/licenses/by-nc/3.0) which permits unrestricted non-commercial use, distribution, and reproduction in any medium, of pruritus associated with psoriasis. However, other provided the original work is properly cited. investigators have reported conflicting results, showing Vol. 26, No. 6, 2014 727 TW Kim, et al decreased nerve density in psoriatic lesions compared Skin biopsies and immunohistochemistry with that in nonlesional skin5. The scalp is the most frequently affected area in patients Punch biopsies (4 mm diameter) were taken from the site with psoriasis. A previous study indicated that 57% of with the most itch at the time of the biopsy in the psoriatic patients with scalp psoriasis believed that it was a psycho- scalp and from the nonlesional scalp (nonlesional and social handicap, and that the most annoying symptom was nonpruritic site ≤10 mm from the site of the primary itching6. The scalp has a complex neuroanatomy with an lesion) of 19 patients. Tissues were rapidly dissected, abundance of sensory neural end organs in the piloseba- post-fixed in fixative solution (4% paraformaldehyde and ceous unit7. Therefore, understanding the clinical charac- 0.4% picric acid in 0.16 M sodium phosphate buffer, pH teristics and unique features of the itch mechanism in the 6.9) for 90 minutes, and rinsed in 0.1 M phosphate buffer scalp is important for the development of effective thera- (pH 7.4) containing 10% sucrose (prepared in phosphate pies. However, few studies have focused on pruritus in buffered saline [PBS]) for at least 24 hours as an optimal scalp psoriasis. cutting temperature compound (Sakura Finetek Japan Co. In the present study, we investigated the clinical charac- Ltd., Tokyo, Japan). Specimens were frozen in isopentane teristics of pruritus associated with scalp psoriasis and that was cooled with liquid nitrogen and stored at −70oC. examined intraepidermal nerve fiber (IENF) density in scalp Sections were cut (25 μm) in a cryostat and air-dried psoriatic lesions. Furthermore, we evaluated the corre- overnight at room temperature. Slide-mounted tissue lation among scalp psoriasis severity, IENF density, and sections were rehydrated briefly in PBS and incubated pruritus intensity. with blocking buffer (blocking solution with goat serum; GeneTex Inc., Irvine, CA, USA) for 1 to 3 hours at room MATERIALS AND METHODS temperature. The primary antibodies used in this study were polyclonal antibodies against the neuron-specific Subjects hydrolase PGP 9.5 (Chemicon, Temecula, CA, USA). Pri- Patients who were at least 18 years of age and diagnosed mary antibodies were diluted in PBS to the appropriate with psoriasis with scalp involvement were eligible for the working dilution (1：1,000). Blocking buffer was removed, study. Those with other underlying pruritogenic diseases of and the slides were then incubated at 4oC for 24 hours with the scalp, including seborrheic dermatitis, atopic dermatitis, primary antibodies. Sections were rinsed thrice in PBS and contact dermatitis, lichen planopilaris, folliculitis, and then incubated for 1 hour at room temperature with malignancy, were excluded. Written informed consent was secondary antibodies (Alexa Fluor 488 goat anti-rabbit obtained from all patients. IgG; Life Technologies, Carlsbad, CA, USA). Sections were The study protocol was approved by the institutional then mounted in a mixture of PBS and glycerol (1：3) review board of Pusan National University Hospital (IRB containing 0.1% p-phenylenediamine. No. D-1305-016-015), and the study was conducted accord- Semiquantitative measurements ing to the ethical guidelines of the Declaration of Helsinki. The samples were examined with a LEICA TCS SP 2 Measurement of the severity of scalp psoriasis and confocal microscope and measured using Leica confocal itching software (Leica Microsystems, Mannheim, Germany). We We used the psoriasis scalp severity index (PSSI), which scanned for subepidermal and intraepidermal nerves corresponds to the scalp-modified psoriasis area severity through two planes, horizontally along the epidermal- index (PASI). The resulting values were 0 to 72, analogous dermal border and vertically by focusing through the to the PASI values. The Leuven Itch Scale (LIS), a question- thickness of the section, to detect each nerve branch and naire that evaluates the dimensions of the itch experience, its course as suggested in the published guidelines9. The was used in this study8. All patients were asked to com- length of the epidermis was measured with Olympus DP plete a questionnaire about the scalp. We defined the soft analySIS Image Processing (version 3.2) software. In a negative impact of itching as an answer of “sometimes”, blinded manner, two trained researchers (TW. K and WH. “often”, or “always” to questions about “consequences of S) counted the total number of IENF clearly penetrating itching” in the LIS. The subjective mean itch intensity in the basement membrane in each section by following the past month was evaluated by using the visual established criteria9 at ×400 magnification; however, the analogue scale (VAS) score: from 0 (for no itch) to 10 (for intraobserver and interobserver reliabilities was untested maximum unbearable itch). and variability was not calculated. Three specimens per biopsy were counted; the mean value was determined and 728 Ann Dermatol Assessment of Pruritus in Scalp Psoriasis divided by the epidermal length of the biopsy. The IENF in the study (Table 1). Immunoreactivity to PGP 9.5 was density was calculated as the mean number of nerve fibers investigated in 19 patients. The mean VAS of pruritus was per millimeter epidermal length (IENF/mm). 3.81±3.06 for all patients and 5.84±2.95 for the 19 patients. There was a moderate positive relation between Statistical analysis PSSI score and VAS of pruritus in all scalp psoriasis patients Statistical analysis was performed with PASW Statistics ver. (Spearman rank correlation; r=0.225 and p=0.044) (Fig. 1). 18.0 for Windows (IBM Co., Armonk, NY, USA). Wilcoxon The mean VAS of distress due to itching was 4.94±3.25 test was performed to compare the IENF density between for all patients and 6.0±3.43 for the 19 patients. lesions and nonlesions. The Spearman p test was performed Clinical characteristics of pruritus associated with scalp to determine whether a significant correlation existed psoriasis among PSSI, pruritus intensity, and IENF density.
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