164 CLINICAL REPORT Ultrasound Assessment of Psoriatic Onychopathy: A Cross-sectional ActaDV Study Comparing Psoriatic Onychopathy with Onychomycosis Mireia MORENO1, Maria Pilar LISBONA2†, Fernando GALLARDO3, Gustavo DEZA3, Marta FERRAN3, Caridad PONTES4, Jesús LUELMO5, Joan MAYMÓ2 and Jordi GRATACÓS1 1 Department of Rheumatology, 4Clinical Pharmacology and 5Department of Dermatology, Hospital Universitari Parc Taulí, Sabadell, 2 Department of Rheumatology, Parc de Salut Mar, 3Department of Dermatology, Parc de Salut Mar, Universitat Autònoma de Barcelona/ Universitat Pompeu Fabra, Barcelona, Spain † Dr Lisbona died just before completion of the study. Acta Dermato-Venereologica This cross-sectional study evaluated the usefulness of an ultrasound technique in assessment of nail chan- SIGNIFICANCE ges in 35 patients with psoriatic onychopathy and 25 Ultrasound is an emerging, non-invasive, inexpensive, ima- with nail dystrophy secondary to onychomycosis. All ging technique with proven evidence for use in the assess- patients underwent 3 examinations: a complete clini- ment of different skin disorders. The aim of this study was cal assessment; a nail ultrasound study; and fungal to differentiate nail psoriasis from onychomycosis using culture. Nails of patients with psoriatic onychopathy an ultrasound technique, since clinical differentiation of presented a thinner nail plate and nail bed, measured these conditions is challenging, especially if psoriasis pre- by ultrasound, than did those with onychomycosis. The sents with nail disease alone. The long-term therapy and percentage of patients with a power Doppler signal ≥2 prognosis for these disorders are different, therefore early at nail bed was significantly higher in psoriatic ony- and adequate diagnosis is essential. Presence of structural chopathy than in onychomycosis, and structural bone bone damage and a high-power Doppler signal were the lesions were more frequent in psoriatic onychopathy main observed ultrasonographic findings supporting a di- than in onychomycosis. These results suggest that the agnosis of nail psoriasis and suggesting an association with presence of structural damage and high-power Dopp- psoriatic arthritis. ler signal are the main ultrasound findings supporting a diagnosis of psoriatic onychopathy. oil spot/salmon patch). The NAPSI (4) is an objective ActaDV Key words: ultrasound; nail; psoriatic onychopathy; onycho- and reproducible tool for estimating the severity of PsO, mycosis. intended as a good measurement of the efficacy of thera- Accepted Oct 3, 2018; E-published Oct 3, 2018 peutic interventions. Ultrasound (US) has proven a useful, non-invasive and Acta Derm Venereol 2019; 99: 164–169. inexpensive imaging technique for screening superficial Corr: Fernando Gallardo, Department of Dermatology, Parc de Salut Mar, tissues, such as the nails (5–7). Substantial evidence for Universitat Autònoma de Barcelona/Universitat Pompeu Fabra, ES-08003 Barcelona, Spain. E-mail: fgallardo.fg@gmail.com the role of US in the assessment of onychopathy in PsA has been published (8, 9). However, to our knowledge, Advances in dermatology and venereology no previous studies have analysed the capacity of this P soriatic arthritis (PsA) is a heterogeneous chronic inflammatory disease with a wide clinical spectrum and variable course. Early diagnosis and treatment of PsA imaging technique to help clinicians differentiate PsO from other nail changes. Onychomycosis (OM) affects 3–4% of the population, with prevalence increasing with could contribute to the prevention of clinical and radio- age (10, 11). Clinical differentiation between PsO and logical progression and functional deterioration (1, 2). OM is challenging, especially when nail disease alone Nail involvement is common in patients with psoriasis. is present. PsO and OM have different clinical and Nails are affected in 15–50% of patients with psoriasis, prognostic implications and require different long-term with the lifetime incidence of nail involvement being therapy with potential side-effects, it is essential to ensure approximately 80% (3). Although psoriatic onychopathy both an early and adequate diagnosis (12). (PsO) is diagnosed solely on the basis of clinical signs, The aims of this study are to evaluate the usefulness it is considered a major clinical marker for the presence of US in the assessment of PsO, and to differentiate PsO or development of PsA. Moreover, PsO is often the only US findings from those found in OM. psoriatic finding at the time of PsA diagnosis in cases with no other cutaneous lesions of psoriasis. Eight features of PsO have been identified for the Nail METHODS Psoriasis Severity Index (NAPSI) score: 4 involve the Design and patients nail matrix (pitting, leukonychia, red spots in the lunula, This was a cross-sectional study in which consecutive psoriatic and nail plate crumbling) and 4 the nail bed (onycholysis, patients with nail involvement (with or without PsA according splinter haemorrhages, subungueal hyperkeratosis, and to Classification Criteria for Psoriatic Arthritis (CASPAR) clas- doi: 10.2340/00015555-3060 This is an open access article under the CC BY-NC license. www.medicaljournals.se/acta Acta Derm Venereol 2019; 99: 164–169 Journal Compilation © 2019 Acta Dermato-Venereologica. Nail ultrasound in psoriasis and onychomycosis 165 sification criteria) (13) and patients with suspected OM attending and loss of trilaminar structure of the ventral and dorsal nail plate rheumatology and dermatology out-patient clinics in Barcelona sections (type IV) (15). ActaDV and Sabadell (Spain) for 1 year, were invited to participate. Ethi- The thickness of the nail plate was defined as the distance cal approval was obtained from the local ethics committee, and between the dorsal and ventral plates, which appears in the US patients provided written consent. view as 2 hyperechoic lines with a hypoechoic space in between. The nail plate was assessed in longitudinal and transversal planes. The nail bed was assessed in both longitudinal and transversal Procedures planes. Its thickness was defined as the distance between the ven- All included patients underwent 3 examinations performed by tral nail plate and the cortical surface of the DIP, which appears in different clinicians: a complete clinical assessment; a nail US the US view as the hypoechoic region under the nail plate. study; and a fungal culture. Patients with nail injuries, current oral The nail matrix is the echoic region at the proximal end of the or topic antifungal therapy or those with concomitant PsO and nail plate; measurements were taken between this area and the Acta Dermato-Venereologica positive fungal culture were excluded from the study. Only those cortical bone of the DIP in the longitudinal plane. patients with positive confirmed dermato­phyte cultures and no past Extensor tendon US measurements included the tendon thick- medical (personal and familial) history of psoriasis were included ness at the level of the DIP joint and the PD signal within the in the OM control group. No systemic or biologic treatments for tendon. To evaluate the PD signal, we used a 500–600 Hz pulse PsO were prescribed at the time of US examination. repetition frequency (PRF) with a dynamic range of 20–25 dB to Subjects were interviewed and examined by 4 experienced increase the contrast between contiguous structures. Ultrasono- dermatologists for the diagnosis of PsO or OM. Age, sex, duration graphers were allowed to adjust the settings in order to produce of nail disease, severity of nail involvement, treatments, a count the best quality images. The PD signal obtained was graded on of finger and toe nails affected by psoriasis, and the presence of the basis of the semi-quantitative validated scoring system from 0 pitting, onycholysis, salmon patches, subungueal hyperkerato- to 3 (0: no signal PD; 1: confluent signal in < 25% of the nail bed sis, thickening of the nail plate and splinter haemorrhages were area; 2: confluent signal in > 25% and < 50% of the nail bed area; recorded. and 3: PD signal in > 50% of the nail bed area) (16, 17). For estimation of the severity of PsO, NAPSI index evaluation Finally, the DIP joints were assessed in search of synovial fluid, was performed. NAPSI is a standard method for the evaluation synovial hypertrophy, joint PD signal, bone erosion and bone of PsO severity, but an approximation to quantification using proliferation, according to OMERACT US group guidelines (18). the NAPSI index was also applied to OM changes in order to Prior to the study, the ultrasonographers reached a consensus on compare the severity of nail disease in these disorders. Each nail US acquisition, measurements and definitions of morpho-structural was divided into 4 quadrants. Each quadrant was evaluated for findings in the nail, based on existing literature. Test–re-test ana- the presence of any manifestation of psoriasis in the nail matrix lysis was carried out for almost all relevant US findings from the or nail bed. The lesion(s) of nail matrix and nail bed were given first included 16 patients, in whom the images were evaluated a a score of 1 in each quadrant, yielding a matrix score of 0–4 and second time to assess inter-observer reliability. Intra-observer ActaDV a nail bed score of 0–4 per nail, with a total maximum score of 8 reliability was also measured in a second reading of the images. and a minimum score of 0 per nail (14). Nail samples for fungal cultures were obtained by clipping the US nail assessment was performed by 3 rheumatologists who nail plate with a sterile nail clipper. Subungueal crumbling debris used US imaging on a regular basis, and who were blinded to from underneath the nail plate was obtained for mycological cul- clinical assessment and fungal culture results. An Esaote My Lab ture in Sabouraud agar following standard procedures. Only those 60© Ultrasound System (Esaote, Genova, Italy) with a transducer results that were positive for dermatophyte infection were included frequency range of 7–13 MHz, equipped with Doppler, was used. in the OM control group. In patients with negative fungal culture The most affected nail in each subject was selected to be scanned who were previously included due to a high clinical suspicion of in grey-scale mode in order to detect morphological changes, fungal infection, a second sample was collected 1 month later from and subsequently with power Doppler (PD) to detect abnormal the same nail. If the second culture was also negative, these patients blood flow. within the OM group were excluded from the study. Advances in dermatology and venereology Nails were scanned with the patient seated with the hand or foot in a standard position over the examination table, in a darkened Statistical analysis room with a temperature between 22ºC and 25ºC. The probe was placed gently over the nail, with the transducer directed perpen- Means (standard deviation; SD) or counts and percentages were dicular to the surface and large amount of gel applied to the area calculated for all continuous variables, and normality of sample examined in order to provide a correct acoustic interface. distribution was assessed with the Shapiro–Wilk test. Both the The US routine included the assessment in grey-scale of quanti- test–retest reliability and inter-rater reliability of US were assessed tative parameters: thickness of the interplate space, ventral and with intra-class correlation coefficient (ICC2,2) with a 2-way mixed dorsal nail plate contours, interplate space, longitudinal thickness average measures model and absolute agreement. To interpret the of nail plate and bed (see below for definitions), matrix thickness results we adopted the classification by Brennan & Silman (19), in and length, distal interphalangeal (DIP) periosteal surface, DIP which ICC values > 0.8 indicate near-perfect agreement, 0.61–0.8 space and contour, and distance between proximal nail plate and substantial agreement, 0.41–0.61 moderate agreement, 0.21–0.40 DIP. All measurements were repeated twice, and the mean value fair agreement, and < 0.2 poor agreement. was used for the study. All the structures were assessed in longi- Comparisons between the US results of PsO and OM were tested tudinal and transversal planes. In addition, the US qualitatively using independent Student’s t-test for normally distributed data, examined (echogenicity and lesions) the nail bed, plate and matrix, or Mann-Whitney U test, as appropriate. To assess the ability of the extensor tendon and DIP. US to discriminate between OM and PsO, we estimated the area Regarding the nail plate, 4 types of morphologic features were under the curve (AUC) of a ROC curve, with the diagnosis of the recorded according to Wortsman classification: focal hyperechoic dermatologist as classification variable and nail bed power Doppler deposits of the distal ventral plate (type I), loosening of the proxi- signal as test variable. Statistical analyses were performed using mal ventral plate and normal dorsal plate (type II), appearance Stata version 14 (College Station, TX, USA). p-values less than of wavy nail plates in both ventral and dorsal sections (type III) 0.05 were considered statistically significant. Acta Derm Venereol 2019 166 M. Moreno et al. Table III. Quantitative ultrasound parameters of the studied nails. Comparison between psoriatic onychopathy and onychomycosis ActaDV Psoriatic onychopathy Onychomycosis n = 35 n = 25 Mean ± SD Mean ± SD p-value Nail plate thickness, cm Longitudinal 0.087 ±  0.024 0.103 ±  0.023 0.013* Transverse 0.081 ±  0.024 0.098 ±  0.022 0.008* Nail bed thickness, cm Longitudinal 0.262 ±  0.088 0.331 ±  0.078 0.003* Transverse 0.258 ±  0.079 0.319 ±  0.085 0.007* Germinal matrix 0.169 ±  0.051 0.191±  0.053 0.117 Extensor tendon 0.097 ±  0.020 0.102 ±  0.020 0.385 Fig. 1. Flow-chart of patients who met inclusion/exclusion criteria Acta Dermato-Venereologica for the study population (n = 88). *p < 0.05. RESULTS or very good (0.64–0.93), being less optimal for tendon thickness. The inter-reader ICC was 0.77 and 0.87 for nail A total of 88 patients with nail involvement were eligible plate, and 0.87 and 0.93 for nail bed (in transverse and for the study. Six patients were excluded due to nail longitudinal planes, respectively). These findings were injuries that made the US difficult to interpret. Twenty again lower for assessment of tendon thickness (Table patients (36%) with PsO and positive fungal culture were II). Nail bed and plate showed significantly less thickness also excluded, as well as 2 patients with a high clinical in PsO compared with nails with OM (Table III). More suspicion of OM despite repeatedly negative cultures. than 80% of PsO and OM nails showed abnormalities A final total of 60 patients (35 with PsO and 25 with on the nail plate. No significant differences were found confirmed OM due to dermatophyte infection) were in- according to nail plate disease based on Wortsman’s clas- cluded in the study (Fig. 1) (60% women, mean age 50 sification of PsO and OM, although the most prevalent years). OM was less frequent in hand nails (12%) than in type of nail plate disease was type II (28%) for PsO and toenails, while PsO occurred mainly in hand nails (57.2%; type IV (32%) for OM (Table IV). p < 0.001). The severity of nail alterations when applying Patients with PsO had a significantly higher percen- NAPSI evaluation (for PsO and OM as well) was greater in tage of PD signal of nail bed graded 2 or higher than did OM (66%) than in PsO (35%) (Table I) although this did patients with OM (60% vs. 16%; p < 0.006). The AUC to ActaDV not reach statistical significance. The intra-reader ICC for discriminate OM/PsO for nail bed PD signal was 0.706 the US measurements of nail plate and nail bed were good (95% confidence interval (95% CI) 0.578–0.834) for a cut-off point of 3, sensitivity was 22.9%, and specifi- Table I. Socio-demographic and Nail Psoriasis Severity Index city was 96% (Table V), with a positive and negative (NAPSI) score from the included patients likelihood ratio of 5.7 and 0.8, respectively (Fig. 2). Psoriatic onychopathy Onychomycosis (n = 35) (n = 25) p-value Table IV. Morphological alterations detected by ultrasound in psoriatic onychopathy and onychomycosis patients Age, years, mean ±  SD 51 ±  9 52 ±  12 0.890 Advances in dermatology and venereology Women, n (%) 17 (49) 17 (68) 0.134 Psoriatic Origin, n (%) onychopathy Onychomycosis Mediterranean 33 (94) 20 (80) n = 35 n = 25 Northern European – 1 (4) n (%) n (%) p-value South American 1 (3) 3 (12) Nail plate Asian 1 (3) – Wortsman classification North African – 1 (4) 0.224 Normal 6 (17) 5 (20) 0.778 Toe nails, n (%) 15 (43) 22 (88) < 0.001* Grade I 8 (23) 4 (16) 0.512 NAPSI 1–2, n (%) 22 (65) 10 (44) 0.080 Grade II 10 (29) 6 (24) 0.693 NAPSI > 3, n (%) 13 (35) 15 (66) Grade III 5 (14) 2 (8) 0.454 SD: standard deviation. *p < 0.05. Grade IV 6 (17) 8 (32) 0.179 Nail bed PD signal Table II. Intra- and inter-rater test–re-test from a sample of Grade 0–1 14 (40) 21 (84) 0.006* patients (n = 16) Grade 2–3 21 (60) 4 (16) Extensor tendon Intra-rater reliability Inter-rater reliability Positive PD signal 2 (6) 1 (4) 0.999 ICC (95% CI) ICC (95% CI) Distal interphalangeal joint Nail plate Synovitis Longitudinal 0.64 (0.21–0.85) 0.87 (0.67–0.95) Overall 8 (23) 5 (20) 0.791 Transverse 0.79 (0.49–0.92) 0.77 (0.45–0.91) Positive PD signal 7 4 Nail bed Structural damage Longitudinal 0.90 (0.74–0.96) 0.93 (0.84–0.98) Overall 22 (63) 2 (8) <0.001* Transverse 0.79 (0.51–0.92) 0.87 (0.69–0.95) Erosions 1 0 Nail root 0.74 (0.40–0.93) 0.96 (0.89–0.98) Cortical irregularities 10 0 Extensor tendon thickness 0.52 (0.08–0.80) 0.60 (0.18–0.84) Bone proliferation 11 2 ICC: intraclass correlation coefficient; CI: confidence interval. *p < 0.05. PD: power-Doppler. www.medicaljournals.se/acta Nail ultrasound in psoriasis and onychomycosis 167 In the current study, the difference between PsO and 1.00 OM in terms of nail bed flow detected by US is the ActaDV most relevant finding. Preliminary results demonstrated the potential role of PD signal in assessing the changes 0.75 in blood flow in psoriatic plaque and PsO (8, 23, 24). Sandobal et al. (25), in agreement with our results, re- ported a high PD signal in the nailbed and DIP joints of 0.50 patients with psoriatic arthritis. On the other hand, there Area under ROC curve = 0.706 (95% CI: 0.578–0.834) are no studies assessing nail-bed blood-flow in patients with OM. Since OM is considered a disease with a very 0.25 Acta Dermato-Venereologica slow progression, the low PD signal we found was not unexpected. 0.00 The presence of arthritis in DIP joints, usually in the 0.00 0.25 0.50 1 - Specificity 0.75 1.00 same finger that presents nail PsO, is a well-known Fig. 2. Receiver operating characteristic (ROC) curve and area psoriatic finding, and very plausibly corresponds to an under the curve (AUC) for nail bed power Doppler signal 0.706, extension of nail enthesopathy (10, 26–28). In this line, 95% confidence interval (95% CI) of AUC: 0.578–0.834, cut-off point ≥3, sensitivity=22.86%, specificity=96%, LR+ 5.7 LR– 0.8. LR: likelihood ratio. using US, we observed a significantly high percentage of patients with PsO who presented structural damage in the DIP compared with OM. Only 2 patients with In addition, nails with PsO showed significantly more OM presented structural damage, specifically bone frequent US structural damage in the DIP joint (erosions, proliferation. Both of these patients had hallux rigidus, irregularities or bone proliferation) than did nails with and this bone proliferation was visible on radiographs. OM (62.8 vs. 8%; p < 0.001). There were no significant In contrast, we did not find more synovitis in PsO than differences when comparing the presence of synovitis in OM. In our study, only 22.9% of patients with PsO in PsO vs. OM (Table IV). For the rest of the clinically showed synovitis in the DIP joint on US, and 66% were analysed variables no statistically significant differences in remission. The low activity we observed, together were found between groups. with a possible lack of sensitivity in detecting synovitis due to the US machines or probes used could explain ActaDV DISCUSSION this absence of a difference. Some reports have described thickening of the extensor To our knowledge, this is the first report comparing the tendon insertion region, measured by US, in patients US features of PsO and data for fungal infection. As a who presented PsO in the adjacent nail (27, 29, 30). In main finding, we observed significantly higher PD signal our study, however, we did not observe any significant at the nail bed and US DIP alterations in patients with differences between PsO and OM in the thickness or PsO compared with those with OM. The present study is in the PD signal of the extensor tendon enthesis. This relevant, since PsO may precede cutaneous or joint invol- result may be explained by the low number of patients vement in some patients and the morphological features with PD signal in the extensor tendon described in our Advances in dermatology and venereology of PsO are not exclusive to this disease. Furthermore, study, the type of probe used with low frequency (7–14 differential diagnosis from other conditions, especially MHz), or the poor inter- and intra-observer reliability for OM, is a great challenge in clinical practice. During the tendon assessment. last decade, research in the field of imaging in psoriatic In our study, the mean nail bed thickness for PsO was arthritis has focused on the assessment of joints, entheses, higher than the cut-off point established previously for or tendons, but little attention has been paid to finger unaffected nail bed (approximately 0.2 cm) (25, 29, 31). and nail disease. Recently, imaging techniques, such However, we found that fungal infection of the nail pro- as US, magnetic resonance image techniques or optical duces even greater nail-bed thickening than is observed coherence tomography, have been applied to the study in psoriasis. These results are in agreement with previous of psoriatic nails (17, 20–22). reports (15, 29, 31), although the differences we obser- ved were not large despite their statistical significance, Table V. Diagnostic utility analysis of the nail bed power-Doppler suggesting that this finding may not help substantially in signal distinguishing between both entities. The most frequent Sensitivity, Specificity, Correctly types of morphological change in the nail plate observed Cut-point % % classified, % LR+ LR– using Worstman typology (15) were type II in nail PSO (≥0) 100.00 0.00 58.33 1.0000 and type IV in OM, similar to the changes observed by (≥1) 80.00 32.00 60.00 1.1765 0.6250 (≥2) 60.00 84.00 70.00 3.7500 0.4762 Sandobal et al. (25). In this sense, our data support the (≥3) 22.86 96.00 53.33 5.7143 0.8036 fact that nail fungal infection represents a more advanced (>3) 0.00 100.00 41.67 1.0000 stage of nail involvement than PsO. From a clinical point Acta Derm Venereol 2019 168 M. Moreno et al. of view, patients with PsO more frequently presented The authors have no conflicts of interest to declare. hand involvement and notably less severe symptoms ActaDV than did patients with OM according to NAPSI score. Although we cannot exclude a potential bias related to REFERENCES the inclusion of patients with PsO, the data observed are 1. Coates LC, Kavanaugh A, Mease PJ, Soriano ER, Laura Acosta-Felquer M, Armstrong AW, et al. Group for Research in accordance with previous reports (12). and Assessment of Psoriasis and Psoriatic Arthritis 2015 Treatment Recommendations for Psoriatic Arthritis. Arthritis Rheumatol 2016; 68: 1060–1071. Study limitations 2. Jiaravuthisan MM, Sasseville D, Vender RB, Murphy F, Muhn This study is a cross-sectional study with a limited num- CY. Psoriasis of the nail: anatomy, pathology, clinical pre- sentation, and a review of the literature on therapy. J Am ber of patients, despite being one of the largest studies Acta Dermato-Venereologica Acad Dermatol 2007; 57: 1–27. published on this subject. The study mostly included 3. Brazzelli V, Carugno A, Alborghetti A, Grasso V, Cananzi R, cases of oil-drop lesions, so we cannot apply the data Fornara L, et al. Prevalence, severity and clinical features of psoriasis in fingernails and toenails in adult patients: presented here to other PsO alterations. Although there Italian experience. J Eur Acad Dermatol Venereol 2012; 26: is a wide clinical spectrum of nail disease related to PsO, 1354–1359. oil-drop or salmon nail patches are not pathognomonic 4. Rich P, Scher RK. Nail Psoriasis Severity Index: a useful tool for evaluation of nail psoriasis. J Am Acad Dermatol 2003; for PsO, but are quite frequent and represent the most 49: 206–212. controversial clinical sign in the differentiated diag- 5. Grassi W, Gutierrez M. Psoriatic arthritis: need for ultrasound nosis (32). In addition, histopathological examination in everyday clinical practice. J Rheumatol Suppl 2012; 89: 39–43. would detect cases of OM with negative culture, and 6. Gutierrez M, Filippucci E, De Angelis R, Filosa G, Kane D, we selected only those cases with positive culture in the Grassi W. A sonographic spectrum of psoriatic arthritis: “the OM group, and repeatedly negative in the PsO group in five targets”. Clin Rheumatol 2010; 29: 133–142. 7. Gutierrez M, Filippucci E, Salaffi F, Di Geso L, Grassi W. Dif- order to minimize cases of PsO with concomitant OM. ferential diagnosis between rheumatoid arthritis and psoriatic Furthermore, the probe used for evaluation of superfi- arthritis: the value of ultrasound findings at metacarpopha- cial tissues was of low frequency, which is a recognized langeal joints level. Ann Rheum Dis 2011; 70: 1111–1114. 8. Wortsman X, Jemec GB. Ultrasound imaging of nails. Der- limitation in nail US studies, and the ultrasonographers matol Clin 2006; 24: 323–328. could not be completely blinded to the skin psoriatic 9. Wortsman X, Gutierrez M, Saavedra T, Honeyman J. The role lesions in patients with severe disease despite being in of ultrasound in rheumatic skin and nail lesions: a multi- ActaDV specialist approach. Clin Rheumatol 2011; 30: 739–748. a dark room. Finally, we did not include patients with 10. Williamson L, Dalbeth N, Dockerty JL, Gee BC, Weatherall PsO and concomitant OM, so our results cannot exclude R, Wordsworth BP. Extended report: nail disease in psoriatic this possibility. Studying a greater number of cases would arthritis – clinically important, potentially treatable and often overlooked. Rheumatology 2004; 43: 790–794. allow patients to be grouped according to the severity of 11. Jesudanam TM, Rao GR, Lakshmi DJ, Kumari GR. Onycho- nail changes and the location of altered nails for a better mycosis: a significant medical problem. Indian J Dermatol comparison. These aspects are relevant when considering Venereol Leprol 2002; 68: 326–329. 12. Eisman S, Sinclair R. Fungal nail infection: diagnosis and using US findings to distinguish differences in nail bed or management. BMJ 2014; 348: g1800. nail plate morphology between OM and PsO in a limited 13. Taylor W, Gladman D, Helliwell P, Marchesoni A, Mease P, number of cases. Mielants H, et al. Classification criteria for psoriatic arthritis: Advances in dermatology and venereology development of new criteria from a large international study. Arthritis Rheum 2006; 54: 2665–2673. Conclusion 14. Cassell SE, Bieber JD, Rich P, Tutuncu ZN, Lee SJ, Kalunian KC, et al. The modified Nail Psoriasis Severity Index: valida- In summary, this is the first study to explore the utility of tion of an instrument to assess psoriatic nail involvement in patients with psoriatic arthritis. J Rheumatol 2007; 34: US in differential diagnosis of PsO and OM. The results 123–129. demonstrate a higher PD signal and a more frequent pre- 15. Wortsman X, Holm EA, Jemec GB, Gniadecka M, Wulf HC: sence of structural damage in DIP joints in PsO (oil-drop [High resolution ultrasound (15 MHz) in the study of the psoriatic nail]. Revista Chilena de Radiología 2004; 10: patches) compared with OM. These findings may help in 6–11 (in Spanish). distinguishing PsO from OM. However, further studies 16. Gutierrez M, Filippucci E, Bertolazzi C, Grassi W. Sonogra­ using higher resolution US probes are necessary to va- phic monitoring of psoriatic plaque. J Rheumatol 2009; 36: 850–851. lidate these results. 17. Gutierrez M, Di Geso L, Salaffi F, Bertolazzi C, Tardella M, Filosa G, et al. Development of a preliminary US power Doppler composite score for monitoring treatment in PsA. ACKNOWLEDGEMENTS Rheumatology 2012; 51: 1261–1268. 18. Wakefield RJ, Balint PV, Szkudlarek M, Filippucci E, Backhaus The authors are indebted to Silvia Iniesta (Research Nurse, De- M, D’Agostino MA, et al. Musculoskeletal ultrasound including partment of Rheumatology, Hospital del Mar, Parc Salut Mar) for definitions for ultrasonographic pathology. J Rheumatol 2005; her outstanding help. 32: 2485–2487. www.medicaljournals.se/acta Nail ultrasound in psoriasis and onychomycosis 169 19. Brennan P, Silman A. Statistical methods for assessing edema detected by magnetic resonance imaging predicts observer variability in clinical measures. BMJ 1992; 304: development of onycholysis and hyperkeratosis. J Rheumatol ActaDV 1491–1494. 2012; 39: 841–843. 20. Gutierrez M, De Angelis R, Bertolazzi C, Filippucci E, Grassi 27. Tan AL, Benjamin M, Toumi H, Grainger AJ, Tanner SF, Emery W, Filosa G. Clinical images: multi-modality imaging moni- P, et al. The relationship between the extensor tendon en- toring of anti-tumor necrosis factor alpha treatment at the thesis and the nail in distal interphalangeal joint disease in joint and skin level in psoriatic arthritis. Arthritis Rheum psoriatic arthritis – a high-resolution MRI and histological 2010; 62: 3829. study. Rheumatology 2007; 46: 253–256. 21. Gutierrez M, Filippucci E, De Angelis R, Bertolazzi C, Becciolini 28. Scarpa R, Soscia E, Peluso R, Atteno M, Manguso F, Del Pu- A, Ariani A, et al. The ultrasound assessment of the psoriatic ente A, et al. Nail and distal interphalangeal joint in psoriatic arthritis: from joint to skin. Reumatismo 2009, 61: 309–315. arthritis. J Rheumatol 2006; 33: 1315–1319. 22. Vidal D, Alfageme F, Ruiz-Villaverde R, Arias-Santiago S, Mar- 29. Aydin SZ, Castillo-Gallego C, Ash ZR, Marzo-Ortega H, Emery torell A. Ultrasound characterization of psoriasis of the nails: a P, Wakefield RJ, et al. Ultrasonographic assessment of nail case-control study. Actas Dermosifiliogr 2017; 108: 968–969. in psoriatic disease shows a link between onychopathy and Acta Dermato-Venereologica 23. Dogra A, Arora AK. Nail psoriasis: the journey so far. Indian distal interphalangeal joint extensor tendon enthesopathy. J Dermatol 2014; 59: 319–333. Dermatology 2012; 225: 231–235. 24. Gutierrez M, Wortsman X, Filippucci E, De Angelis R, Filosa 30. McGonagle D. Enthesitis: an autoinflammatory lesion linking G, Grassi W. High-frequency sonography in the evaluation nail and joint involvement in psoriatic disease. J Eur Acad of psoriasis: nail and skin involvement. J Ultrasound Med Dermatol Venereol 2009; 23: 9–13. 2009; 28: 1569–1574. 31. Gisondi P, Idolazzi L, Girolomoni G. Ultrasonography reveals 25. Sandobal C, Carbo E, Iribas J, Roverano S, Paira S. Ultrasound nail thickening in patients with chronic plaque psoriasis. Arch nail imaging on patients with psoriasis and psoriatic arthritis Dermatol Res 2012; 304: 727–732. compared with rheumatoid arthritis and control subjects. J 32. Love TJ, Gudjonsson JE, Valdimarsson H, Gudbjornsson B. Clin Rheumatol 2014; 20: 21–24. Psoriatic arthritis and onycholysis – results from the cross- 26. Dalbeth N, Pui K, Lobo M, Doyle A, Jones PB, Taylor WJ, et sectional Reykjavik psoriatic arthritis study. J Rheumatol al. Nail disease in psoriatic arthritis: distal phalangeal bone 2012; 39: 1441–1444. ActaDV Advances in dermatology and venereology Acta Derm Venereol 2019