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Brief Report
ARTICLE IN PRESS
doi:
10.25259/IJDVL_894_2022

Enthesopathy in patients with nail psoriasis – a cross-sectional evaluation of clinical, onychoscopic and ultrasonographic features

Department of Dermatology and STD, University College of Medical Sciences (UCMS) and Guru Teg Bahadur Hospital, Delhi, India
Corresponding author: Dr. Chander Grover, Professor, Department of Dermatology and STD, University College of Medical Sciences (UCMS) and Guru Teg Bahadur (GTB) Hospital, Delhi, India, chandergroverkubba76@gmail.com
Licence
This is an open-access article distributed under the terms of the Creative Commons Attribution-Non Commercial-Share Alike 4.0 License, which allows others to remix, transform, and build upon the work non-commercially, as long as the author is credited and the new creations are licensed under the identical terms.

How to cite this article: Bhoi AK, Grover C, Singal A, Tandon A. Enthesopathy in patients with nail psoriasis – a cross-sectional evaluation of clinical, onychoscopic and ultrasonographic features. Indian J Dermatol Venereol Leprol doi: 10.25259/IJDVL_894_2022

Abstract

Background

Nail involvement in psoriasis is common and may be an indicator not only of disease severity, but also of the presence of psoriatic arthritis. However, the relationship of nail psoriasis with enthesitis remains under-explored.

Aims

This study was conducted to evaluate the clinical, onychoscopic (nail dermatoscopic) and ultrasonographic features in patients with nail psoriasis.

Materials and Methods

All nails of twenty adult patients with nail psoriasis were examined clinically and onychoscopically. Patients were evaluated for psoriatic arthritis (Classification Criteria for Psoriatic Arthritis), the severity of cutaneous disease (Psoriasis Area Severity Index) and nail disease (Nail Psoriasis Severity Index). Ultrasonography of the clinically involved digits was performed for evidence of distal interphalangeal joint enthesitis.

Results

Out of 20 patients, 18 patients had cutaneous psoriasis and 2 had isolated nail involvement. Among the 18 patients with skin psoriasis, 4 had associated psoriatic arthritis. The most commonly observed clinical and onychoscopic features were pitting (31.2% and 42.2%), onycholysis (36% and 36.5%) and subungual hyperkeratosis (30.2% and 30.5%), respectively. Ultrasonographic evidence of distal interphalangeal joint enthesitis was seen in 57% (175/307) of the digits with clinical nail involvement. Enthesitis was more common in patients with psoriatic arthritis (77% vs 50.6%). Nail thickening, crumbling and onychorrhexis (all features of nail matrix involvement) were significantly associated with enthesitis (P < 0.005).

Limitation

The major limitation was the small sample size and lack of controls. Only the clinically involved digits were evaluated for enthesitis.

Conclusion

Enthesitis was frequently detected on ultrasonography in patients with nail psoriasis, even in clinically asymptomatic individuals. Nail features of thickening, crumbling and onychorrhexis may predict underlying enthesitis and the potential development of arthritis. A comprehensive evaluation could help identify patients with psoriasis at risk for arthritis, helping improve long-term outcomes.

Keywords

Enthesitis
nail psoriasis
psoriatic arthritis
nail dermoscopy.

Plain Language Summary

Ultrasonographic evaluation of distal interphalangeal joint involvement in nail psoriasis

Nail psoriasis is more frequent as well as more severe in patients with psoriatic arthritis. Through this study we explore its association with distal interphalangeal joint (DIP) enthesitis. Ultrasonographic evidence of DIP joint enthesitis was found to be commonly present in 307 digits of 20 patients, manifesting nail psoriasis. This was present even when the patient did not have any clinical evidence of psoriatic arthritis. We also found that nails with thickening, crumbling, or onychorrhexis had evidence of enthesitis more commonly. This study highlights that nail psoriasis should be comprehensively evaluated and treatment options chosen with a long-term aim to prevent joint damage.

Introduction

Isolated nail involvement may be seen in 5–10% of patients with psoriasis and the incidence of nail involvement has been estimated to be up to 90% over a lifetime. 1,2 Nail psoriasis significantly affects the quality of life 35 and correlates with increased disease severity, longer duration and higher frequency of joint involvement.

Clinical features of nail psoriasis are variable, determined by the site of involvement within the nail unit. The nail bed rests directly on the periosteum of the distal phalanx and the nail matrix lies in proximity to the distal interphalangeal joint and the insertion of the digital extensor tendon. This explains the frequent association of nail psoriasis with distal interphalangeal joint arthritis and enthesitis.

An early diagnosis of enthesitis and distal interphalangeal joint arthritis by radiological imaging (ultrasonography, magnetic resonance imaging) may permit choice of appropriate therapy, thus enabling optimal therapeutic outcomes, improving prognosis and preventing deformities. Ultrasonography is cheaper and more easily available than magnetic resonance imaging and is a sensitive, repeatable and real-time assessment.

The nature and characteristics of nail unit changes have not been comprehensively evaluated and data regarding the link between nail psoriasis and enthesitis of the corresponding digital extensor tendon is scant. To bridge this gap, we evaluated clinical and onychoscopic features of patients with nail psoriasis along with an ultrasonographic assessment of the DIP joints and entheses.

Materials and Methods

A convenience sample of 20 consecutive adult patients with nail psoriasis presenting to the Skin OPD of the Department of Dermatology and STD, University College of Medical Sciences and Guru Teg Bahadur Hospital, Delhi, India, was recruited after approval by the Institutional Ethical Committee. The study protocol was explained and written informed consent obtained from each study participant.

A detailed history and complete mucocutaneous examination documenting the site(s) of cutaneous involvement and cutaneous disease severity (using the Psoriasis Area Severity Index) was performed. The nails of all fingers and toes were examined under good light, and the severity of nail involvement was recorded using the Nail Psoriasis Severity Index. Nail dermoscopy (onychoscopy) was performed with a USB dermatoscope (Dinolite edge Digital Microscope AM7515MZT, AnMo Electronics Corporation, Taipei, Taiwan) and the changes noted. A detailed musculoskeletal examination was conducted and the presence of psoriatic arthritis was documented using the Classification criteria for Psoriatic Arthritis (CASPAR).

Ultrasonographic assessment (Samsung RS80 EVO, Samsung Electronics Co. Ltd, Seoul, South Korea) of the distal interphalangeal joint and entheses was performed on all digits with clinically involved nails using a linear probe (frequency of 3–16 Hz). We used the OMERACT 7 (Outcome Measures in Rheumatoid Arthritis Clinical Trials) definitions for ultrasonographic pathology and a loss of normal fibrillary architecture of the digital extensor tendon, the presence of enthesophytes at the point of bony insertion or bony changes, including erosions, were documented as enthesitis. 6

All data were recorded in MS Excel and statistical analysis was performed using IBM SPSS Statistics for Windows, version 20.0 (IBM Corp., Armonk, N.Y., USA). Means and proportions were calculated. Appropriate statistical tests of significance including t-test (for means), Chi-square test and Fisher’s exact test (for proportions) were applied to evaluate statistical significance of differences between study groups.

Results

The ages of the study subjects ranged from 18–60 years (mean 38.1 ± 12.7 years). Men outnumbered women (1.85:1) and the duration of psoriasis ranged from 1 to 13 years (mean 5.9 ± 3.4 years) [Table 1]. Of the 20 patients with nail psoriasis, 4 had associated psoriatic arthritis, 2 patients had isolated nail involvement, while the rest had only cutaneous involvement. The Psoriasis Area Severity Index (PASI) of the 18 patients with cutaneous disease ranged from 1.6 to 50.8 (mean 12.2 ± 10.9).

Table 1: Clinical profile and ultrasonography finding in patients with nail psoriasis
Nail psoriasis (n = 20) Nail psoriasis without psoriatic arthritis (n = 16) Nail psoriasis with psoriatic arthritis (n = 4)
Gender Male:Female 1.85:1 1.6:1 3:1
Age (years) Mean ± standard deviation 38.1 ± 12.65 38.18 ± 13.67 37.75 ± 7.25
Disease duration (years) Mean ± standard deviation 5.85 ± 3.39 5.4 ± 3.39 7.5 ± 2.87
PASI Score (Mean ± standard deviation) 12.22 ± 10.9 13.4 0 ±11.67 7.5 ± 4.57

Nail psoriasis severity index score Mean ± standard deviation

52.1 ± 33.42 42 ± 24.62 92.5 ± 33.47
Number of nails involved per patient 15.35 ± 4.0 14.56 ± 4.03 18.5 ± 1.65
Ultrasonography evaluation of distal interphalangeal joint
Total number of clinically involved nails (examined by ultrasonography) 307 233 74
Presence of radiological evidence of distal interphalangeal enthesopathy 175 (57%) 118 (50.64%) 57 (77.02%)
Ultrasonography features seen
Enthesophyte formation 143 (46.57%) 103 (44.2%) 40 (70.17%)
Bony erosion 10 (3.25%) 3 (1.28%) 7 (9.45%)
Loss of normal fibrillary architecture 22 (7.16%) 12 (5.15%) 10 (13.5%)

Clinical nail involvement

All 400 nails of the 20 patients were examined and 307 of these were affected clinically. The mean number of nails involved in each patient was 15 (SD ± 4; range 9–20) and the mean Nail Psoriasis Severity Index (NAPSI) was 52.1 (SD ± 33.4; range 15–120). The mean Nail Psoriasis Severity Index was higher in patients with psoriatic arthritis in comparison with those without (92.5 vs 42). A weak correlation between nail psoriasis severity index and psoriasis area severity index was noted (Pearson’s correlation coefficient (r) = 0.208) but this was not statistically significant (P = 0.376). A total of 74/80 nails (92.5%) were involved in the 4 patients with psoriatic arthritis, while 118/320 nails (36.9%) were involved in psoriasis patients without arthritis.

The features of nail psoriasis on clinical examination are shown in Figure 1. Pitting was the commonest nail matrix change [Figure 2a] followed by thickening and crumbling [Figure 3a]. The most frequent nail bed changes were onycholysis, subungual hyperkeratosis and splinter haemorrhages, in that order [Figure 4a]. Pitting was most frequent finding in fingernails and distal onycholysis with subungual hyperkeratosis was the commonest change in toenails. A statistically significant difference was notable between the finger and toenails with respect to the incidence of some features such as pitting, thickening and crumbling, onychorrhexis, onycholysis and subungual hyperkeratosis [Table 2].

Figure 1: Frequency distribution of nail psoriasis features on clinical examination and onychoscopy
Figure 2a: Clinical evidence of pitting in nail psoriasis seen as multiple, irregularly arranged pits
Figure 2b: Nail dermoscopy (onychoscopy) showing psoriatic nail pitting with pits that are irregular in distribution, size, shape and depth (black arrows). Few have associated scaling (red arrow) (Dinolite AM7515MZT nonpolarised ×35)
Figure 3a: Clinical finding of extensive psoriasis with thickened and crumbling nails with yellowish discolouration
Figure 3b: Onychoscopic image of thickened and crumbling nail plate. Yellow discolouration and opaque nail plate with the nail bed not visible (Dinolite AM7515MZT nonpolarised ×35)
Figure 4a: Clinical evidence of nail bed psoriasis seen as distal onycholysis, salmon patch and splinter haemorrhages seen involving multiple nails
Figure 4b: Onychoscopic image showing distal disruption of onychodermal band (onycholysis) (black arrows) with proximal erythema (red stars) and multiple splinter haemorrhages (blue arrowheads) (Dinolite AM7515MZT polarised ×60)
Table 2: Comparative frequency of clinical and onychoscopic features in fingernails and toenails of patients with nail psoriasis
Clinical examination
Onychoscopic examination
Fingernails n (%) Toenails n (%) P value Fingernails n (%) Toenails n (%) P-value
Total nails examined 200 200 200 200
Nail matrix features
Pitting 105 (53%) 20 (10%) 0.0001* 127 (64%) 42 (21%) 0.00001*
Thickening and Crumbling 40 (20%) 65 (33%) 0.004* 40 (20%) 64 (32%) 0.465
Leukonychia 4 (2%) 1 (0.5%) 0.371 9 (5%) 1 (0.5%) 0.02*
Red spot in lunula 0 0 0 0
Longitudinal ridging 8 (4%) 2 (1%) 0.105 18 (9%) 6 (3%) 0.011*
Beau’s line 20 (10%) 21 (11%) 0.869 23 (12%) 21 (11%) 0.749
Onychoschizia 1 (0.5%) 4 (2%) 0.371 1 (0.5%) 4 (2%) 0.371
Onychorrhexis 2 (2%) 14 (7%) 0.003* 3 (1.5%) 20 (10%) 0.0003*
Longitudinal Melanonychia 3 (1.5%) 2 (1%) 1 3 (1.5%) 2 (1%) 1
Nail bed features
Onycholysis 54 (27%) 90 (45%) 0.001* 53 (27%) 93 (47%) 0.288
Oil spot 7 (4%) 0 0.014* 6 (3%) 0 0.03
Subungual hyperkeratosis 43 (22%) 78 (39%) 0.0001* 43 (22%) 79 (40%) 0.00009*
Splinter haemorrhages 8 (4%) 1 (0.5%) 0.037* 27 (14%) 5 (3%) 0.0001
A P value of <0.05 was taken as significant

Onychoscopy (Nail Dermatoscopy)

Onychoscopic involvement alone (without clinical changes) was noted in 8 nails (i.e. a total of 315 nails were involved on onychoscopy) [Table 2; Figure 1]. Pitting, thickening and crumbling were the most common nail matrix features noted on onychoscopy [Figures 2b and 3b]. The most frequent nail bed changes were onycholysis, subungual hyperkeratosis and splinter haemorrhages, in that order [Figure 4b].

The difference in incidence of pitting, leukonychia, longitudinal ridging, onychorrhexis and subungual hyperkeratosis between finger and toenails was statistically significant (P < 0.05) [Table 2]. Pitting, longitudinal ridging and splinter haemorrhages were significantly more frequently seen on onychoscopy as compared with the clinical examination [Table 3].

Table 3: Frequency of nail psoriasis features on clinical and onychoscopy examination
Clinical examination n = 200 (%) Onychoscopic examination n = 200 (%) P-value
Total nails involved 307 (76%) 315 (78%) 0.496
Nail matrix features
Pitting 125 (31%) 169 (42%) 0.001*
Thickening and crumbling 105 (26%) 104 (26%) 0.9
Leukonychia 5 (1%) 10 (3%) 0.192
Red spot in the lunula 0 0
Longitudinal ridging 10 (3%) 24 (6%) 0.014*
Beau’s line 41 (10%) 44 (11%) 0.712
Onychoschizia 5 (1%) 5 (1%) 1
Onychorrhexis 16 (4%) 23 (6%) 0.25
Longitudinal Melanonychia 5 (1%) 5 (1%) 1
Nail bed features
Onycholysis 144 (36%) 146 (37%) 0.883
Oil spot 7 (2%) 6 (2%) 0.779
Subungual HK 121 (30%) 122 (31%) 0.938
Splinter haemorrhage 9 (2%) 32 (8%) 0.0002*
A P value of <0.05 was taken as significant
Table 4: Statistical analysis of the nail features with regard to distal interphalangeal joint enthesitis
Variables Nail features
Enthesitis
P-value
Present Absent Present Absent
Pitting n = 125 n = 182 n = 75 n = 50 0.772
Thickening and crumbling n = 105 n = 202 n = 68 n = 37 0.04*
Beau’s line n = 41 n = 266 n =19 n = 22 0.138
Onychorrhexis n = 16 n = 291 n = 3 n = 13 0.002*
Onycholysis n = 144 n = 163 n = 82 n = 62 0.984
Oil spot n = 7 n = 300 n = 3 n = 4 0.468
Subungual Hyperkeratosis n = 121 n = 186 n = 76 n = 45 0.097
Splinter haemorrhages n = 9 n = 298 n = 6 n = 3 0.736
A P value of <0.05 was taken as significant

Ultrasonography

All 20 patients had enthesitis on ultrasonography and 57% of the clinically affected digits (175/307) demonstrated changes [Figures 5 and 6 and Table 1]. Enthesitis was documented in 77% (57 of 74) of the clinically affected nails of the 4 patients with psoriatic arthritis, but in only 51% (118/233) in those without arthritis.

Figure 5: Longitudinal scan of distal interphalangeal joint showing enthesophyte (yellow arrow)
Figure 6: Longitudinal scan of distal interphalangeal joint showing bony erosion (white star)

Enthesophyte formation (143 digits, 46.6%] was the commonest ultrasonography feature seen, while loss of normal fibrillary architecture (22 digits, 7.2%) and bony erosions (10 digits, 3.3%) were less commonly observed. Thickening and crumbling of the nail plate and onychorrhexis were frequently associated with enthesitis (P value of <0.05) [Table 4].

Discussion

Nail involvement in psoriasis is a common and important indicator of psoriatic arthritis and enthesitis. Ideally, nail psoriasis should influence long-term treatment choices, but in clinical practice it is often overlooked during diagnosis and management.

The mean number of nails involved per patient (18.5 vs 14.6) and the mean nail psoriasis severity index (92.5 vs 42) was higher in patients with psoriatic arthritis in our study, similar to previous reports. 5,7,8 This positive correlation of the frequency and severity of nail disease with psoriatic arthritis emphasizes the importance of a comprehensive nail evaluation.

The commonest clinical nail feature was onycholysis, followed by pitting and subungual hyperkeratosis [Table 3]. These have been variably reported to be onycholysis and splinter haemorrhages, 9 or pitting and onycholysis. 10 The most common onychoscopic feature was pitting, followed by onycholysis and subungual hyperkeratosis. The difference in frequency distribution between fingernails and toenails was statistically significant for some nail features [Table 2]. In contrast, Chauhan et al. reported significant differences for all nail features except Beau’s line and onychomadesis. 11 We found a statistically significant difference in the frequency of detection for pitting, splinter haemorrhages and longitudinal ridging on onychoscopic examination as compared to clinical examination [Table 3]. Thus, onychoscopy is a useful adjunct in the evaluation of nail changes that may not otherwise visible.

Ultrasonography facilitates real-time evaluation of every component of the nail unit as well as the distal interphalangeal joint [Figure 7]. Ultrasonography nail plate changes have been classified by Wortsman et al. 12 into types I–IV, with type IV being the most severe [Figure 8]. These correlate well with psoriatic arthritis. 13 Though we could not do a comprehensive analysis of the nail plate structure in our patients, we did evaluate the entheseal structure in detail.

Figure 7: Longitudinal scan of normal distal interphalangeal joint showing digital extensor tendon attachment (white star)
Figure 8: Longitudinal scan of psoriatic nail showing thickened, irregular and wavy nail plate (NP, blue arrow) with loss of interplate hypoechoic zone and thickening of the nail bed (NB, Yellow arrow)

All our patients with nail psoriasis had evidence of enthesitis though most were asymptomatic. Ultrasonographic evidence of enthesitis was observed in 57% of involved digits. The higher frequency of distal interphalangeal joint enthesitis in patients with psoriatic arthritis was in concordance with previous data by Krajewska-Włodarczyk et al. 1416 [Table 5].

Table 5: Comparative frequency of enthesitis in clinically involved digits of nail psoriasis patients in various studies
Acosta-Felquer et al. 2017
Krajewska-Włodarczyk et al. 2018
Krajewska-Włodarczyk et al. 2019
Present study
Number of nails assessed % of enthesitis on ultrasonography Number of nails assessed % of enthesitis on ultrasonography Number of nails assessed % of enthesitis on ultrasonography Number of nails assessed % of enthesitis on ultrasonography
Number of nails with psoriasis 236 60.6% 416 46.3% 440 49.5% 307 57%
Number of nails with psoriasis without arthritis 93 61.2% 248 31% 272 38% 233 50.6%
Number of nails with psoriasis with psoriatic arthritis 143 60.1% 168 68% 168 68% 74 77%

Thickening, crumbling and onychorrhexis of the nail were significantly associated with distal interphalangeal joint enthesitis. These three features are reflective of nail matrix disease and should alert the clinician towards the presence of enthesitis. However, other workers have noted that onycholysis to be frequently associated with enthesitis. 1719 Aydin et al. 17 and Lai 19 also noted pitting and crumbling, respectively in association with enthesitis.

Enthesitis is likely an early sign of arthritis and its persistence often precedes joint damage. Its frequency positively correlates with higher disease activity and poor quality of life. 20 The association between nail psoriasis and adjacent enthesitis has been demonstrated by previous magnetic resonance imaging and ultrasonography studies. 17,21 Entheseal inflammation is closely correlated with the inflammatory involvement of the nail matrix. 22,23 This fact was reinforced in our study, with a high frequency of enthesitis in digits with involved nails, even in the absence of joint symptoms or signs.

Our findings outline a need for improving the sensitivity of diagnostic criteria for psoriatic arthritis. Patients with nail psoriasis do not have just distal interphalangeal joint enthesitis but also enthesitis involving other joints which may be in the form of higher than normal enthesitis scores for these distant joints. This suggests that enthesitis may be a systemic rather than a solely local entheseal response. 24 An early diagnosis and treatment of enthesitis is critically important for ensuring a favourable outcome, 25 and ultrasonography can thus serve as a non-invasive, relatively cheap and rapid technique for the assessment of entheseal changes.

Limitations

The major limitation of our study was the small sample size. No controls could be evaluated. Due to the small number of patients with concomitant psoriatic arthritis, we could not analyse conclusive differences. As we evaluated only the clinically involved digits, we cannot rule out the presence of subclinical enthesitis in uninvolved digits.

Conclusion

The frequency of enthesitis is very high in patients with nail psoriasis, even though clinical evidence may be lacking. The presence of nail changes like thickened and crumbling nails should alert dermatologists to plan treatment accordingly. A comprehensive clinical and onychoscopic evaluation can be a sensitive indicator in psoriasis patients at risk of psoriatic arthritis, even when the sensitivity of clinical criteria is low. Further studies with larger sample sizes involving different patient subsets can help comprehensively evaluate and validate these findings to help detect patients at risk early.

Declaration of patient consent

The authors certify that they have obtained all appropriate patient consent.

Financial support and sponsorship

NSI Thesis Research Grant 2019 (Grant no. 01/2019) provided as a partial research grant by the Nail Society of India.

Conflict of interest

There are no conflicts of interest.

References

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