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COMMENTARY

Onychomycosis: A proposed revision of the


clinical classification
Roderick J. Hay, DM, FRCP,a and Robert Baran, MDb,c
London, United Kingdom; and Villejuif and Cannes, France

The classification of onychomycosis, infection of the nail apparatus caused by fungi, has changed over time
with the recognition of new pathways of nail infection, new organisms, and new variations in the
appearance of diseased infected nail. Taking into account published descriptions of nail morphology in
fungal infection, the following forms of onychomycosis are recognized: distal and lateral subungual,
superficial, endonyx, proximal subungual, mixed, totally dystrophic, and secondary onychomycosis. These
can be subdivided, where appropriate, by color and pattern of nail plate change. The purpose of the
revised classification is to provide a framework to assist selection of treatment, estimate prognosis, and
evaluate new diagnostic methods. ( J Am Acad Dermatol 2011;65:1219-27.)

Key words: classification; fungus; nail disease; onychomycosis; prognosis; revised.

ince Zaias1 proposed a classification of fungal

S nail disease in 1972 there have been a number


of developments and modifications to our
understanding of the process by which fungi invade
Abbreviations used:
CMC: chronic mucocutaneous candidosis
DLSO: distal and lateral subungual
onychomycosis
the human nail apparatus, the range of organisms EO: endonyx onychomycosis
involved, and their response to therapy. The original MPO: mixed pattern onychomycosis
PSO: proximal subungual onychomycosis
classification proposed 3 distinct forms of nail plate SO: superficial onychomycosis
invasion: distal and lateral2 subungual onychomyco- TDO: totally dystrophic onychomycosis
sis (DLSO), where invasion originates from the distal
and lateral undersurface of the plate; superficial
white onychomycosis, where invasion originates
from the upper surface; and proximal subungual onychomycosis,3 where the nail plate is attacked
onychomycosis (PSO), where the attack starts from from the distal end of the nail plate causing deeper
the undersurface of the proximal nailfold. These penetration of fungal hyphae and, more recently, a
were reflected by the clinical appearances of the nail. revision of the concept of superficial white onycho-
The concept of totally dystrophic onychomycosis mycosis and PSO,4 largely as a result of the identifi-
(TDO) was introduced later2 to explain the fact that, cation of new fungal causes, mixed patterns, and the
in some patients, the nail plate and, often, surround- effect of different types of immunosuppression on
ing periungual tissue may be involved by the infec- depth of penetration. The Zaias1 classification and
tion. Subsequently there have been a number of the subsequent additions and revisions have been
modifications that were introduced to explain new useful in promoting the development of scientific
findings, such as the concept of endonyx explanations for the clinical pattern of nail disease in
relation to the principle sites of invasion.
From the Department of Dermatology, Kings College Hospital However, changes are necessary for a number of
National Health Service Trust, Denmark Hill, Londona; Nail different reasons. We now understand that a much
Disease Center, Cannesb; and Gustave Roussy Cancer Institute, wider range of organisms can attack and break down
Villejuif.c nail keratin. Although some, such as Scopulariopsis
Funding sources: None.
Conflicts of interest: None declared.
brevicaulis, have been known for many years as nail
Reprint requests: Roderick J. Hay, DM, FRCP, Dermatology pathogens that cause DLSO, there are others, such as
Department, Department of Dermatology, Kings College Fusarium species, that can produce distinct changes
Hospital National Health Service Trust, Denmark Hill, London ranging from paronychia to PSO through to TDO.5
SE5 9RS. United Kingdom. E-mail: roderick.hay@ifd.org. Candida species, often associated with invasion of
Published online April 19, 2011.
0190-9622/$36.00
the nail plate as opposed to the nailfold (paronychia)
2010 by the American Academy of Dermatology, Inc. on the basis of positive cultures from nail clippings,
doi:10.1016/j.jaad.2010.09.730 are now recognized to be less common causes of

1219
1220 Hay and Baran J AM ACAD DERMATOL
DECEMBER 2011

primary nail dystrophy after nail plate invasion6; the change seen, we now recognize that melanonychia
clinical appearances are very similar to those seen can occur both with DLSO and superficial nail plate
with DLSO caused by other organisms including invasion.13,14 Other color changes have been re-
distal nail plate erosion and discoloration. Invasive ported such as orange discoloration caused by
Candida onychomycosis, though, can be associated Paecilomyces.15 Secondly the emergence of new
with other conditions such as chronic mucocutane- treatments that result in profound immunosuppres-
ous candidosis (CMC)6 or HIV/AIDS.7 There remains sion, and disease such as HIV/AIDS where naturally
some debate about whether acquired immunosuppres-
Candida is commoner as a sion occurs, has resulted in
true primary nail pathogen in CAPSULE SUMMARY the appearance of new forms
the tropics,8 but there is no of nail plate invasion.16,17
dThe following forms of onychomycosis
hard evidence that these Thirdly the direct spread of
are recognized under the current
cases show fungal nail plate fungi from the stratum cor-
classification: distal and lateral
invasion. Candida species neum of the surrounding skin
subungual, superficial white, endonyx,
commonly colonize the un- to the nail plate is core to the
proximal subungual, and totally
dersurface of the nail and, original classification. Yet this
dystrophic. These reflected the
therefore, to establish inva- does not explain the appear-
recognized patterns of nail invasion.
sion of the nail plate a posi- ance of PSO18 and certain
tive culture is insufficient d
Using more recent literature we have types of superficial onycho-
proof without microscopic extended this to include mixed and mycosis (SO)4,19 emerging
evidence. secondary forms of infection and refined from the proximal nailfold,
The word paronychia the definition of superficial and proximal as there is no histologic evi-
describes an inflammation subungual infection. These changes are dence that the fungi gain en-
of the nailfold that is a clini- necessary because infections are caused try via the superior aspect of
cal syndrome with multiple by a broader range of fungi than the nailfold. Although in
causes that may include in- previously reported and some may be some case these infections
fection, inflammatory skin associated with immunosuppression. may have been derived from
disease such as pemphigus,9 dThis revised classification will help a preceding, and now recov-
and adverse drug reactions clinicians to decide: (a) whether detailed ered, distal and lateral sub-
such as protease inhibitors.10 mycological investigation such as ungual nail plate extending
Candida infection can cause identification of species is necessary; and from the distal nail to the
paronychia, but, together (b) the most successful treatment proximal nailfold, nail inva-
with bacteria, yeasts can options. sion as a form of recurrence,
readily grow in a distended this can only account for
nailfold and infection may some cases that have already
therefore be a primary event or secondary to other received treatment. Alternative explanations have
conditions including irritant or allergic dermatitis.11 been proposed that include sequestration of orga-
There is often associated lateral onycholysis of the nisms in lymphatics and blood stream dissemination,
nail plate in patients with paronychia and Candida which is known to occur in certain fungal infections
species can be isolated and seen in microscopy. of the nails such as Fusarium infection in the
These lateral nail plate changes often respond to immunosuppressed.20 Bloodstream spread is also
antifungals suggesting that lateral nail dystrophy, recognized in some forms of deep dermatophyte
secondary to the presence of Candida in the nail- infection, such as maladie dermatophytique.21 In this
12
fold, is an invasive process. This can be confirmed rare deep infection there is also histologically proven
by biopsying the lateral plate to show penetration by involvement of lymph nodes. However, the method
Candida hyphae for a short distance into the under- of traffic between circulation and the nail plate is not
surface of the nail plate. known.
There are other areas where there are new Finally it is clear that in individual patients
observations including nail color, the presence of some nails show the features of more than one
immunosuppression, routes of nail plate invasion, pattern of nail infection.4 For instance where there
and mixed patterns of infection. is onychomycosis of the distal and lateral subun-
Firstly there is a wide range of color change gual type affecting a toenail, SO may develop
or dyschromia that follows nail plate invasion. on the same nail, particularly where another toe
Although in earlier reports white or yellow discol- overrides it. Fungal infection of the nail plate may
oration was the commonest form of pigmentary also arise secondary to other conditions such as
J AM ACAD DERMATOL Hay and Baran 1221
VOLUME 65, NUMBER 6

psoriasis22 or keratoderma23 and in these cases it Table I. Revised classification of onychomycosis


is difficult to separate nail changes caused by
DLSO
fungal invasion and those caused by the underly-
Clinical features include hyperkeratosis and range of
ing disease. dyschromias including melanonychia, onycholysis
For all these reasons a review of the current (which may be sole abnormality), and longitudinal
classification of nail disease is now required. streaking in mid or lateral nail plate regions
SO (white or black)
REVISED CLASSIFICATION a) patchy or transverse
The proposed classification set out in this article b) originating from beneath proximal nailfold
(Table I) is the result of these newer observations - patchy
and forms a revised description of the different forms - transverse: this pattern is commonest presenta-
of nail disease caused by fungi (Table II). Making tion for superficial nail plate infections originat-
ing from beneath proximal nailfold
such a classification is timely and relevant; as the
c) with deep penetration: fungi invade from
availability of more effective antifungal drugs and a
superficial to deep aspects of nail plate
range of topically applied antifungal medications
Endonyx onychomycosis (EO)
may ensure that the treatment is, in part, determined
PSO
by the form of nail plate invasion. a) patchy
We are proposing to modify the basic model1 and b) striate (transverse or longitudinal)
to include subsequent changes such as the following c) secondary to paronychia*
subtypes of fungal nail plate invasion; it is also useful Mixed pattern onychomycosis (MPO): examples include
to specify whether onychomycosis is primary or following patterns on same nail
secondary to some other nail disease. DLSO plus SO
SO plus DLSO
Distal and lateral subungual onychomycosis SO plus PSO
DLSO remains the commonest form of fungal DLSO plus PSO
invasion of the nail plate, where the site of invasion is Totally dystrophic onychomycosis (TDO)
from the lateral or distal undersurface of the nail This may occur as secondary change to advanced states
of other patterns of nail plate invasion; alternatively it
plate (Fig 1). The main features are onycholysis with
may occur as primary change where it is associated
hyperkeratosis and varying forms of dyspigmenta- either with disease with severe immunodeficiency, eg,
tion. Most commonly this is white or yellowish but, HIV/AIDS or in chronic mucocutaneous candidosis
on occasion, other color changes such as brown, Secondary onychomycosis
black, and orange discoloration have been described Fungal nail plate invasion may occur secondary to other
as well.14,15,24,25 nail pathologies, eg, psoriasis; here clinical changes
This pattern of nail plate invasion may be com- are dominated by morphologic features of underlying
plicated by other changes, as in some cases it is disease.
associated with longitudinal streaking of the nail,
DLSO, Distal and lateral subungual onychomycosis; PSO, proximal
sometimes called a dermatophytoma.26,27 This may subungual onychomycosis; SO, superficial onychomycosis.
be confined to the lateral nail border or to another *Paronychia where fungi are present may be complicated by nail
part of the nail plate. However, it is associated with plate invasion (PSO) or nail plate invasion, commonly DLSO, may
the presence of underlying spongy keratin often be followed by infection of nailfold (eg, Scytalidium infection).
infiltrated with either fungi or bacteria and treatment
failure is common unless the area is excised.
Clustering of fungal arthrospores in the nail plate treatment. It is important, though, when onycholysis
associated with cell wall thickening and the emer- is the only sign of nail abnormality, that due care is
gence of spaces in the surrounding keratin is seen in given to ensure that the presence of fungal invasion
many nail plate infections28 and it is thought that of the nail plate is established, such as by micros-
these streaks are extreme examples of the same copy; adherence of fungi to the undersurface of the
phenomenon. Streaking or dermatophytoma can be nail may also indicate carriage. This is common with
seen in other patterns of onychomycosis but is Candida, less so with dermatophytes, and when it
commonest with DLSO. With Scytalidium infections, occurs with the latter may be a prelude to invasion of
paronychia may be associated with DLSO. the nail plate.29
Onycholysis is occasionally the only physical DLSO is associated with a variety of different fungi
abnormality associated with distal and lateral nail (Table II and Fig 2) and equally a wide variety of
plate invasion. For instance it has been described different species are seen with the rare cases of
with dermatophytosis and responds to antifungal melanonychia (Fig 3).30
1222 Hay and Baran J AM ACAD DERMATOL
DECEMBER 2011

Table II. Onychomycosis: organisms most


commonly associated with different types
Organisms commonly
Type associated
DLSO
Dermatophytes (T rubrum,
T mentagrophytes,
E floccosum*)
C albicans
Fusarium species
Scytalidium species Fig 1. Distal and lateral subungual onychomycosis caused
Scopulariopsis brevicaulis by Trichophyton mentagrophytes.

SO (white or black)
Patchy T mentagrophytes, T rubrum
Transverse Fusarium, Acremonium
Scytalidium
T rubrum, Fusarium

Endonyx onychomycosis
T soudanense
T violaceum

PSO
Patchy, striate transverse, T rubrum, Fusarium
longitudinal
Mixed pattern
onychomycosis examples
include following on
same nail
DLSO plus SO T rubrum
SO plus DLSO T rubrum, Fusarium
SO plus PSO T rubrum, Fusarium
DLSO plus PSO T rubrum Fig 2. Distal and lateral subungual onychomycosis caused
Totally dystrophic by Scopulariopsis brevicaulis.
onychomycosis Dermatophytes
C albicans
Scytalidium Superficial onychomycosis
SO may present with a range of dyschromias
Paronychia depending on the organism involved; so use of the
With onychomycosis Candida species term superficial white onychomycosis is restric-
(usually DLSO or PSO) Fusarium tive. For instance, superficial black onychomycosis
Scytalidium caused by Trichophyton rubrum has been de-
Without onychomycosisy Candida species scribed31 as has Scytalidium dimidiatum.32
Fusarium As stated previously the pattern of nail plate
invasion may present with superficial patches
(patchy type) or be organized in transverse
C, Candida; DLSO, distal and lateral subungual onychomycosis;
E, Epidermophyton; PSO, proximal subungual onychomycosis;
striaeestriate leukonychia (Fig 4).4,19 Several nails
SO, superficial onychomycosis; T, Trichophyton. may be involved at the same time, with clinical
*Other dermatophytes may also cause DLSO. changes affecting similar levels. It may also appear
y
As described above infection of nailfold may be direct result of de novo on the superficial nail plate or emerge from
fungal infection but is often, particularly in established cases, under the proximal nailfold; each has different
associated with other cause of nail plate inflammation, eg, irritant
dermatitis.
therapeutic implications. In some cases there is
deep penetration of the nail plate from the superficial
aspect19,33; immunosuppression is associated in
some patients (Fig 5). These have been discussed
previously, but the main implication of the striate
J AM ACAD DERMATOL Hay and Baran 1223
VOLUME 65, NUMBER 6

Fig 3. Fungal melanonychia caused by Trichophyton


rubrum.
Fig 5. Superficial onychomycosis with deep penetration
caused by Fusarium.

Fig 4. Superficial onychomycosis caused by Trichophyton


mentagrophytes.

form is that where the infection emerges from under


the proximal nailfold it is impracticable to use topical
therapy as it is seldom effective; there is also an
increased risk that there is co-incident infection of
the undersurface of the nail plate, in this case PSO
(Fig 6). In these patients oral therapy is likely to be
more effective. In the classic forms that present with Fig 6. Striate superficial onychomycosis originating as
patchy infiltration of the upper aspect of the nail proximal subungual onychomycosis caused by Fusarium.
plate topical therapy can be used as initial treatment.
However, as yet there are no large clinical therapeu-
of inflammation and fungi in the nail bed or of
tic studies to support this advice. subungual hyperatosis but many fungal hyphae in
the interior of the nail plate.
Endonyx onychomycosis (EO) It was originally described as an infection with
The nail plate invasion is distinguished by the T soudanense (Fig 7), which most commonly causes
combination of lamellar splitting of the nail, discol- hair shaft invasion and tinea capitis.3,34 However,
oration of the nail plate (eg, milky patches), and cases caused by other organisms, such as T viola-
absence of nail bed invasion but internal nail plate ceum, have been seen. It is not clear if this is only
invasion. The route of infection is thought to follow seen with organisms that have the capacity to invade
fungal hyphae penetrating the distal nail plate, hair as well or why T soudanense in particular seems
directly. It is distinguished pathologically by absence to be mainly associated with the infection.
1224 Hay and Baran J AM ACAD DERMATOL
DECEMBER 2011

Fig 7. Endonyx onychomycosis caused by Trichophyton Fig 9. Proximal subungual onychomycosis caused by
soudanense. Candida albicans causing paronychium.

plate or a form that spreads rapidly at the same level


associated with immunosuppression particularly
HIV/AIDS.16 PSO is also seen with a range of orga-
nisms including dermatophytes, usually T rubrum,
and Fusarium, C albicans,35 and Aspergillus36 spe-
cies. It is a form of infection that is difficult to treat
and always requires oral therapy, although relapse is
common. Combined approaches using both oral and
topical treatment with or without surgery may be
needed.
Proximal nail plate invasion also occurs second-
ary to paronychia (Fig 9). The commonest fungi
associated with this pattern are Candida species37
and there is usually a narrow area of lateral onychol-
ysis with varying hyperkeratosis extending from the
nailfold to the distal nail margin. It also occurs with
Fusarium and other mold infections.5 These are
Fig 8. Proximal white subungual onychomycosis caused discussed in more detail below.
by Trichophyton rubrum. Paronychia and nail plate invasion caused by
fungi (onychomycosis) secondary to paronychia
merit further consideration (Table I). As stated pre-
Proximal subungual onychomycosis viously inflammation of the nailfold, paronychia, is a
PSO has also been reassessed as the changes are, clinical syndrome of which fungal infection is but
again, organized in diffuse patches or transverse one cause.29,37 In setting this out it must be recog-
striate patterns.1,4,18 Classically the infection is seen nized that where fungi such as Candida are associ-
originating from under proximal nail and nailfold ated with paronychia it is not always clear whether
(Fig 8). But those forms presenting with transverse the organisms are, at the time of presentation,
bands (striate pattern) are often associated with a causing or contributing to nailfold dystrophy.
concurrent SO (see above). The infection slowly Although this may seem a subtle distinction, other
extends distally. There are other varieties such as one factors contribute to the pathogenesis of paronychia
where there is formation of a longitudinal band such as immediate contact dermatitis to food38 and
extending from the proximal nailfold to the distal nail secondary bacterial infection. In immunosuppressed
J AM ACAD DERMATOL Hay and Baran 1225
VOLUME 65, NUMBER 6

Fig 12. Mixed pattern onychomycosis; in this case infec-


tion caused by Trichophyton rubrum causing distal and
Fig 10. Distal and lateral subungual onychomycosis lateral subungual onychomycosis and superficial
showing secondary nailfold swelling in infection caused onychomycosis.
by Scytalidium dimidiatum.

Fig 13. Totally dystrophic onychomycosis caused by


Fig 11. Digital cellulitis and mixed pattern onychomycosis
Trichophyton rubrum.
caused by Acremonium in neutropenic patient.

Mixed pattern onychomycosis (MPO)


patients, including those with CMC, Candida infec- As stated previously, different patterns of nail
tion of the nailfold is often significant. Removing plate infection are often seen both in the same
both bacteria and fungi with topical or systemic individual but also in the same nail. Although it is
antimicrobials remains a goal of treatment even less common than DLSO, a mixed form of onycho-
though treatment with anti-inflammatory agents, mycosis is proposed (Fig 12). Different patterns have
including oral, intralesional, or topical corticoste- been described but include various combinations,
roids or tacrolimus,39 is often highly effective. the commonest of which are PSO and SO or DLSO
Likewise treating lateral nail plate dystrophy, a lateral and SO.19,42 These almost always require oral
dystrophy spreading from the proximal nailfold, ie, therapy.
PSO, secondary to a paronychium with antifungals
can result in resolution of the nail abnormality. Totally dystrophic onychomycosis
It is also now known that other fungi can cause This concept has not changed since it was orig-
nailfold infection with or without nail plate invasion. inally proposed.2 TDO represents the end stage of a
The two best known examples are Scytalidium variety of different modes of nail plate invasion
dimidiatum (Fig 10) and Scytalidium hyalinum40 caused by different organisms.2,16 It most commonly
and Fusarium species.41 Recognizing these types is follows DLSO but other forms, particularly PSO, can
important not only because there are implications for result in this end stage. Here the nail plate crumbles
treatment but also in the case of Fusarium infections away and the nail bed is thickened and ridged and
inflammation of the nailfold or paronychia extend- usually covered with debris. Very extensive end-
ing proximally along the digit to produce a localized stage nail infection may be secondary to dermato-
form of cellulitis (Fig 11) may herald the develop- phytes such as T rubrum (Fig 13) and mold fungi
ment of bloodstream spread of this infection in the whose initial path of invasion is described in the
neutropenic patient.20 In both the examples cited preceding sections. In patients with CMC the whole
above (Scytalidium and Fusarium) involvement of nail unit is thickened as a result of extensive hyper-
the nailfold is secondary to one of the patterns of keratosis (Fig 14). This pattern of nail change reflects
onychomycosis described in this article. the rapidity of nail plate invasion, and in nail disease
1226 Hay and Baran J AM ACAD DERMATOL
DECEMBER 2011

development of clinical trials to test the validity of


warning signs of difficult-to-treat infections. It may
also help to clarify the role of fungi in nail change as
advances in molecular diagnostics provide new
methods such as detection of the expression of
protein indicators of nail invasion.45

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