Differential Diagnosis of Nail Psoriasis and Onychomycoses: A Report Based on 40 Years of Specialised Nail Consultations

Author: Eckart Haneke

Inselspital Universitatsspital Bern, Bern, Switzerland Correspondence to [email protected]

Disclosure: The author has declared no conflicts of interest.

Received: 09.01.20

Accepted: 05.03.20

Keywords: Asymmetric gait nail unit syndrome, differential diagnosis, histopathology, mycology, nail psoriasis, , reactive .

Citation: EMJ Dermatol. 2020;DOI/10.33590/emjdermatol/20-00008

Abstract Ungual psoriasis and onychomycosis are common nail diseases. Despite their different aetiology and course, surprisingly they have much in common both clinically and histopathologically, rendering their distinction often very challenging. Because their treatments are fundamentally different, anti- inflammatory–immunosuppressive for psoriasis and anti-infective for onychomycoses, an exact diagnosis is crucial for their management. Psoriasis is the dermatosis with the most frequent nail involvement. Pits, ivory-coloured spots, salmon or oil spots, subungual hyperkeratosis, , and splinter haemorrhages are the most common nail signs. Onychomycoses are thought to be the most frequent nail diseases. This statement is disputed for toenails, for which orthopaedic abnormalities are said to be even more frequent and mimic fungal nail infections.

INTRODUCTION patients have nail alterations at any time, but 80–90% will experience nail changes at least once 2,7 Nail disorders account for approximately during their lifetime. Nail psoriasis is frequently 10–15% of the workload of dermatologists. Patients associated with arthritis, particularly of the distal request, and deserve, an accurate diagnosis and interphalangeal . The nails are even more 8 treatment.1,2 This can be difficult when the most often involved in . Fingernails 2,7 frequent onychopathies such as nail psoriasis, are more frequently affected than toenails. onychomycoses,3,4 and nail alterations of the In contrast to cutaneous psoriasis, there is asymmetric gait nail unit syndrome are clinically no association of nail psoriasis and psoriatic 7 very similar.5 They all have a severe impact on a arthritis with HLA-C0602. Nail psoriasis is patient’s quality of life.6 also frequently associated with enthesitis, an of tendon and ligament insertions. This is interpreted as being a Köbner phenomenon UNGUAL PSORIASIS rather than an autoimmune disease.9

Psoriasis is the dermatosis that most frequently Psoriasis causes both specific and less affects the nails.2 Approximately half of psoriasis characteristic nail alterations (Figure 1A).10,11

DERMATOLOGY • August 2020 EMJ Pits are the most frequent alterations of matrix the distal matrix may be seen as red spots in the psoriasis.2 They develop from minute psoriatic lunula and those in the mid-matrix may cause foci in the apical matrix resulting in circumscribed psoriatic leuconychia. The most common parakeratotic mounds that break out and leave signs of nailbed involvement are subungual a small depression in the nail plate surface.12 hyperkeratosis and oil or salmon spots. However, some parakeratotic foci often remain When the latter grow to the hyponychium and are seen as small whitish to ivory-coloured they result in onycholysis, which is typically spots. The pits and spots are of relatively bordered proximally by a reddish-brown regular depth and size with random distribution; band reflecting an active psoriatic lesion.2,12 however, they are sometimes arranged in Small, thin, longitudinally arranged dark lines horizontal or longitudinal lines. More than 10 pits are splinter haemorrhages and correspond per nail or a total of more than 60 pits and spots to microthromboses of the longitudinally are generally seen as confirming the diagnosis arranged nailbed capillaries;2 thus, they are of nail psoriasis (Figure 1A).2 Psoriatic lesions in comparable to Auspitz’s phenomenon.

A B

C D

Figure 1:

A) Nail psoriasis; B) deep type of superficial white onychomycosis;C) massive nail thickening, discolouration, onycholysis, distal bulge formation, and lateral deviation in right-sided congenital malalignment of the big toenail; D) AGNUS of both big toenails: inward rotation of the toes, slight hallux erectus, and onycholysis of the distal lateral nail portion.

DERMATOLOGY • August 2020 EMJ Creative Commons Attribution-Non Commercial 4.0 August 2020 • DERMATOLOGY Involvement of the proximal nailfold leads to helps to distinguish it from onychomycosis.7,13 psoriatic with spontaneous loss of For scientific reasons and therapeutic studies, the cuticle. Affection of the entire nail apparatus nail psoriasis grading systems were established causes complete nail destruction. Depending on to reproducibly determine the extent and severity the extent and severity of the involvement of of ungual psoriasis. The Nail Psoriasis Severity the different parts of the nail, extremely variable Index (NAPSI) is used most frequently although intra- and interindividual clinical patterns can several other grading systems were created that be seen. Finger and toenail involvement often also cover other aspects. present different clinical aspects. The distal phalanx is swollen in psoriatic arthritis and the ONYCHOMYCOSES may be stiffened in a slightly bent position. Psoriatic is almost Fungal infections of the nail unit are commonly exclusively observed on big toes with minor or designated as onychomycoses. They are said to no nail changes.13 be the most frequent nail diseases constituting All three forms of pustular psoriasis affect the 40–50% of all nail disorders. They are nails.2 Small yellowish spots are seen under the distinguished by their responsible pathogens nail in generalised pustular psoriasis of von and the route of infection determining the nail Zumbusch, whereas larger lakes of pus can be structures primarily involved.19,20 This classification observed under the nail together with larger is particularly important for onychomycosis surface defects called elkonyxis in palmar treatment and prognosis. plantar pustular psoriasis.2,7 Acrodermatitis The most common pathogens of onychomycoses continua suppurativa of Hallopeau is an excessively recalcitrant disease, mostly isolated are dermatophytes, which contain specific on the tip of a digit. This may turn red, inflamed, capable of degrading keratin. develop small to medium-sized pustules that Trichophyton rubrum, followed by T. interdigitale destroy the nail, and finally result in a rounded (mentagrophytes) are the leading pathogens; naked digit tip without a nail.13 Concomitant T. soudanense, T. violaceum, T. tonsurans, and 21 psoriasis lesions elsewhere on the may Microsporum spp. rarely cause nail infections. develop but this is rather rare. As seen in Some Candida species contain acid peptidases generalised pustular psoriasis, an IL-36 receptor that can digest nail keratin, although they are antagonist defect was found in acrodermatitis more commonly found in chronic paronychia continua suppurativa.14 Because of its frequent of fingers.C. albicans and C. parapsilosis are monodigital involvement, acrodermatitis the leading yeasts, but C. glabrata, C. tropicalis, continua suppurativa often remains undiagnosed and C. krusei are uncommon. Nondermatophyte for years. An important differential diagnosis moulds are now also accepted as being primary is nail involvement in .13 nail pathogens, particularly Scopulariopsis Additionally, nail psoriasis is also observed in brevicaulis22 and Fusarium spp., with the latter children. The diagnosis is often missed because presenting as new emerging nail pathogens.23 paediatricians commonly do not think of psoriasis There are differences in the spectrum of nail in this age group.15 pathogens depending on geography, climate, and common habits;24,25 however, clinical distinction of Approximately 5% of cases are isolated nail the different pathogens is usually not possible.19 2,4 psoriasis without skin lesions. A diagnostic Yeasts and nondermatophyte moulds are adjunct to the clinical diagnosis and to avoid comparatively more frequent in psoriatic nails.26,27 an invasive biopsy is the histopathological examination of nail clippings with as much of the Estimates of the prevalence of onychomycoses subungual hyperkeratosis as possible.11,12,16-18 As differ.24 Between 3% and 8% of the population nail psoriasis has a serious negative impact on are said to have fungal nail infections; however, the quality of life, an early and exact diagnosis in some professional groups, the prevalence was is warranted. Chronic trauma and professional 8–40%. Of patients with tinea pedum, 20–30% stress to the digit aggravate nail psoriasis. The have onychomycoses. Men appear to be affected common course is chronic or chronic recurrent. more frequently than women and the frequency This waxing and waning of nail lesions often increases steadily with age.28 The susceptibility

DERMATOLOGY • August 2020 EMJ to develop an onychomycosis is an autosomal the classical form of WSO extends under the dominant trait evidenced by the frequent vertical proximal nailfold and, because of this occlusion, spread within affected families.29 Those with can invade into the nail plate (Figure 1B). Proximal psoriasis will experience fungal nail infections subungual white onychomycosis develops when a more frequently, making the differential diagnosis pathogenic fungus breaks the barrier of the difficult or impossible.2,4,12 Toenails growing only cuticle and grows along the eponychium one-third of the rate of fingernails are 7–10 in a proximal direction until it reaches the times more frequently infected. Mixed infections matrix from where it is both included into make up for 5% of all onychomycoses,19,20,30 and the growing nail plate and actively invades immunosuppressed individuals are prone to rare distally towards the nailbed. A rare form caused fungal species that are usually difficult to treat.19 almost exclusively either by T. soudanense or T. violaceum is endonyx onychomycosis, which The differentiation of onychomycoses according histopathologically shows fungal organisms in to the route of invasion is important in clinical the middle layer of the nail plate but without practice because it also explains the severity nailbed involvement. and chances of a successful therapy.31 By far the most common type is distal lateral subungual C. albicans has enzymes capable of splitting onychomycosis (DLSO).1 From the infected skin up keratin. Particularly in hot climates, an of the tip of the digit and lateral nail folds, the infection similar to DLSO is observed whereas fungus grows into the hyponychium and then in temperate climates, paronychia may develop. invades the nailbed. This reacts with a mild Proximal subungual white onychomycosis caused distal hyperkeratosis that extends proximally by Candida spp. is occasionally observed in and thickens eventually raising the nail. The neonates. Nondermatophytes are increasingly 5 overlying nail plate covers the infection and only found in onychomycoses; however, their later gets invaded, which is seen by the loss of aetiopathogenetic role is not always clear. transparency and fragility of the plate (Figure All forms of onychomycosis can ultimately 1B).19,31 Histopathology of nail clippings with develop into total dystrophic onychomycoses, subungual hyperkeratosis demonstrates fungi in in which the nail is destroyed and substituted the keratin and undersurface of the nail. It shows by keratotic debris. A primary total dystrophic that the nail is not the primary target but rather onychomycosis is characteristic for chronic 33 a barrier for the fungus.12 The further course of mucocutaneous candidiasis. the infection is characterised by slow invasion into the direction of the matrix; however, this DIAGNOSIS OF FUNGAL NAIL may remain stable for months or years in many INFECTIONS cases. Dermatoscopy often shows a fringed proximal border compared to an aurora borealis.32 Although onychomycoses are often diagnosed Another feature not infrequently seen in toenails on clinical grounds alone, this should not be is the development of a yellow spike pointing the standard because treatment is always long, proximally, extremely rich in thick-walled fungi tedious, and potentially associated with serious including both short filaments and spores, and side effects.34 The most common examinations therefore also called dermatophytoma. It is very are direct microscopy of subungual keratotic recalcitrant and usually requires mechanical material after clearing with potassium hydroxide debridement for treatment. After years or plus mycological cultures. Direct microscopy decades, this DLSO can involve the entire nail is rapid, easy, and inexpensive, but often and destroy it. White superficial onychomycosis nonspecific. Although capable of identifying (WSO) is divided into 3 subtypes. The classical the fungus, cultures take 4–6 weeks, give form of WSO exhibits chalk-white spots with a false-negative results in 30–50% of cases, and lustreless surface on toenails and arises due to a cannot distinguish between a true invasive particular growth pattern of T. mentagrophytes. onychomycosis and colonisation. Histopathology Another form is seen in immunocompromised of nail clippings only takes 1–3 days, is twice as patients, primarily observed on fingernails, arises sensitive as cultures, insensitive to contamination, due to T. rubrum, and has a shiny surface. The third allows the differentiation between infection form is the ‘deep’ WSO, which develops when and contamination to be made, and gives

DERMATOLOGY • August 2020 EMJ Creative Commons Attribution-Non Commercial 4.0 August 2020 • DERMATOLOGY permanent preparations. It does not, however, overlapping toes, or sports activities. The permit species identification.35,36 For superficial asymmetric gait nail unit syndrome is a white onychomycosis, a thin slice from the characteristic condition seen in individuals with nail surface may be taken with a No. 15 scalpel orthopaedic abnormalities that may begin in the blade and for proximal subungual white vertebral column, continue over the hip to the onychomycosis, a disc of nail plate may be punched knees, but is usually most obvious in the feet.5,56,57 out and then divided into halves for culture and This is associated with distal lateral or distal histopathology. Nail clipping histopathology medial onycholysis in the innermost toes with also allows psoriasis and onychomycoses a smooth border and without a reddish-brown to be differentiated by their differentmargin (Figure 1D). It is commonly mistaken and parakeratosis distribution.37,38 for a fungal nail infection. Histopathology and Immunohistochemistry should theoretically cultures are usually negative for pathogenic fungi. allow species identificationin situ, but there were, However, dystrophic nails are more often infected until now, no reliable antibodies on the market. by fungi.58 Congenital malalignment of the big Similar problems exist for in situ hybridisation. toenails is characterised by early onset lateral New diagnostic techniques include PCR and deviation of the nails, discolouration, oyster shell- matrix assisted laser desorption ionisation – time like surface, and severe onycholysis (Figure 1C).59 39 of flight (MALDI-TOF) mass spectroscopy. Both Trachyonychia, or rough nails, could affect single are expensive, require specialised laboratories, nails or almost all nails, particularly in 20-nail and cannot differentiate between true infection dystrophy of childhood. It describes nail changes and contamination. that may be idiopathic or due to atopic eczema, , psoriasis, or, although rarely, some DIFFERENTIAL DIAGNOSES other dermatoses. Clinically, they typically cannot be distinguished, and their exact diagnosis The most important differential diagnosis of requires the histopathological examination of nail psoriasis is onychomycosis and vice versa.40 a nail biopsy. Nail lichen planus is characterised They have many clinical and histopathological by longitudinal ridging and splitting, as well as features in common, though to a variable degree permanent scarring and pterygium formation. (Figure 1A and 1B) (Table 1). Onychoscopy may Nail eczema exhibits irregular pitting and help in the differential diagnosis.41 Compared to transverse bulges and ridging, the proximal nail onychomycosis, a thinner nail plate, structural fold is often thickened, and the cuticle is lost. changes, and a higher power Doppler signal Rough nails may also be due to fungal infection, 42 was found in nail psoriasis by ultrasonography. characteristically chronic mucocutaneous Confocal laser scanning microscopy and optical candidiasis. Chronic toenail conditions, particularly coherence microscopy may identify intraungual in the elderly and weaker individuals, may lead 43,44 fungi. Recently, a genetic susceptibility to to , which is defined by ram’s acquire onychomycosis in psoriasis was found horn-like nails. These may show fungi in with HLA-DR*08 and HLA-DR*01, likely increasing histopathology slides, but they are not the real cause 45 the susceptibility to fungal nail infection. of onychogryphosis. Pseudomonas aeruginosa The prevalence of onychomycosis in psoriasis often colonises predamaged nails causing a patients is estimated to be between less than a greenish discolouration. and quarter to one-third,46-52 but was found in 50% other habits occur both on finger and toenails of patients in a recent study from Italy; however, and are often mistaken for a mycotic infection. yeasts were statistically significantly more Nail alterations in reactive arthritis may be frequent in the non-psoriatic control group.53 In a almost indistinguishable from those of pustular case-control study from Pakistan, nearly one-third psoriasis but are often more marked and the of nail psoriasis patients had onychomycosis.54 pustules have a brownish tinge due to frequent It was assumed that the pathogenic fungus erythrocyte admixture. Palmar plantar lesions are benefits from the damaged nail of psoriasis.55 seen as so-called keratoderma blenorrhagicum, Other very frequent differential diagnoses and oral mucosal involvement is characteristic. of toenail changes are caused by mechanical Scabies may infest the nail unit, particularly in its irritation such as friction from footwear, crusted variant.60,61

DERMATOLOGY • August 2020 EMJ Table 1: Differential diagnostic features of nail psoriasis and onychomycoses.

Psoriasis Onychomycosis Frequency Most frequent dermatosis with nail involvement; Most frequent . Up to 30–40% 80% of patients with psoriasis will develop nail of all nail disorders. psoriasis during lifetime. Course Chronic to chronic-recurrent, often with Chronic progressive, but also often stable intermittent improvement. over years. Symptoms Embarrassment, often painful, and restricting daily Embarrassment, potentially painful. activities. Signs Matrix: pits, , nail crumbling. Subungual hyperkeratosis, yellowish discoloration, onycholysis. Nail bed: salmon spots, subungual hyperkeratosis, onycholysis, splinter haemorrhages. Pits and ivory-coloured Pits and ivory-coloured spots. Rare, irregular size. spots Nail bed hyperkeratosis Frequent. Frequent. Onycholysis Frequent. Proximal border like a salmon spot. Frequent. Proximal border irregular: ruin sign or ‘aurora borealis’. Discolouration None or yellowish. Yellow to brown. Spores and hyphae Rare, mostly spores. Very frequent: spores and hyphae. Transverse ridges Rare. Very rare. Trauma May act as Köbner phenomenon. Important predisposing factor. Heredity Strong genetic component. Susceptibility to develop onychomycosis is inherited as an autosomal dominant trait. Lesions elsewhere Psoriatic plaques often present in typical Often concomitant tinea pedum. localisation. Histopathology Hyperkeratosis with parakeratosis and included Marked hyperkeratosis with neutrophils and serum globules. and serum inclusions, contains most of the pathogenic fungi. Leukocytes in subungual parakeratosis and rarely Leukocytes in subungual hyperkeratosis also in the nail plate (Munro’s microabscesses). surrounded by parakeratosis (Munro’s microabscesses). Focal hypergranulosis. Focal hypergranulosis. Papillomatous nail bed . Papillomatous nail bed hyperplasia. Spongiosis, mononuclear, and neutrophil Spongiosis, mononuclear, and rarely exocytosis. neutrophil exocytosis. Small depressions and parakeratotic mounds on Hyphae and spores in the subungual the nail surface (psoriatic pits). hyperkeratosis and underside of the nail plate.

Many nail diseases can be colonised or > Psoriasis is the dermatosis with the most superinfected with fungi; it is then usually not frequent nail involvement. possible to determine what was first. Psoriasis > Up to 80–90% of all individuals with psoriasis and onychomycosis may occur together. will develop nail lesions in their lifetime. > Onychomycoses are the most frequent and As psoriasis treatment is usually resistant fungal skin infections. immunodepressive, onychomycoses should be > Onychomycosis treatment requires proof of treated first.1 the fungal aetiology, although this is not always possible. TAKE HOME MESSAGES > Nail psoriasis and onychomycoses have many signs and symptoms in common and may co- > Onychomycoses are the most frequent occur, sometimes rendering their differential nail diseases. diagnosis very difficult.

DERMATOLOGY • August 2020 EMJ Creative Commons Attribution-Non Commercial 4.0 August 2020 • DERMATOLOGY References

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