Dermatoscopy of pigmented Bowen’s disease

Alan Cameron, MBBS,a Cliff Rosendahl, MBBS,a Philipp Tschandl, CandMed,b Elisabeth Riedl, MD,b

and Harald Kittler, MDb

Brisbane, Australia and Vienna, Austria

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Background: Pigmented Bowen’s disease is not well characterized.

Objective: To characterize the clinical and dermatoscopic appearance of pigmented Bowen’s disease.

Methods: We performed a retrospective analysis of 52 consecutive cases of pigmented Bowen’s disease.

Results: Of 951 histopathologically verified cases of Bowen’s disease that underwent biopsy during thestudy period, 52 (5.5%) were pigmented. Dermatoscopically pigmented Bowen’s disease is typified by apattern of dots and/or structureless zones. In 21.2% (n = 11), we observed brown or gray dots arranged in alinear fashion. Vessels were identified in 67.3% of lesions with a predomination of coiled vessels. A lineararrangement of vessels was seen in 11.5%.

Limitations: Conclusions are limited by the fact that this was a retrospective, uncontrolled study.

Conclusions: Pigmented Bowen’s disease has a characteristic dermatoscopic pattern. Linear arrangementof brown and/or gray dots and/or coiled vessels is a specific clue to pigmented Bowen’s disease. ( J AmAcad Dermatol 2010;62:597-604.)

Key words: Bowen’s disease; dermatopathology; dermatoscopy; non-melanoma skin cancer.

Abbreviations used:

BD: Bowen’s diseasepBD: pigmented Bowen’s disease

INTRODUCTIONBowen’s disease (BD) is a superficial variant

of cutaneous squamous cell carcinoma. Histo-pathologically it is characterized by abnormal andpleomorphic keratinocytes that at first involve onlythe lower part of the epidermis and, in time, the fullthickness of it. Clinically it most commonly presentsas a pink scaly plaque. In Caucasians, exposure toultraviolet radiation is the dominant causative fac-tor, but exposure to chemicals (most notably arse-nic), immunosuppression (particularly iatrogenic inorgan transplantation), and infection with humanpapillomavirus have also been implicated.

the School of Medicine, University of Queensland, Brisbane,a

d the Department of Dermatology, Division of General

ermatology, Medical University of Vienna.b

ing sources: None.

licts of interest: None declared.

pted for publication June 4, 2009.

int requests: Harald Kittler, MD, Department of Dermatology,

ivision of General Dermatology, Medical University of Vienna,

ahringer Gurtel 18-20, 1090 Vienna, Austria. E-mail: harald.

ttler@meduniwien.ac.at.

ished online January 18, 2010.

-9622/$36.00

10 by the American Academy of Dermatology, Inc.

0.1016/j.jaad.2009.06.008

Like actinic keratosis, BD has a pigmented variant(pBD). The differential diagnosis of pBD includespigmented actinic keratosis, solar lentigo, seborrheickeratosis, lichen planuselike keratosis, differenttypes of melanocytic nevi, melanoma, and pig-mented basal cell carcinoma. Previous descriptionsof the dermatoscopy of pBD have been case reportsand small case series.1-8 Our study describes thedermatoscopic patterns of pBD in a series of 52 casesand correlates these findings with histopathology.

MATERIALS AND METHODThe 52 lesions included in this study were col-

lected between September 2006 and November 2008in two primary care private practices (A. C., C. R.) inQueensland, Australia. The inclusion criteria were asfollows: (1) histopathologically proven BD; (2) pres-ence of any brown, gray, black, or blue pigmentationdermatoscopically; and (3) availability of dermato-scopic images. Histopathologically BD is typified bythe presence of abnormal (neoplastic) keratinocytes

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throughout a thickened epidermis, mitoses (inclu-ding abnormal mitotic figures), involvement ofacrotrichia, and absence of criteria typical for actinickeratosis (alternation of orthokeratosis and paraker-atosis, suprabasal clefts, acantholytic dyskeratoticcells). As authors Rosendahl and Cameron routinelyphotodocument all pigmented lesions that are biop-

CAPSULE SUMMARY

d Pigmented Bowen’s disease is not wellcharacterized clinically ordermatoscopically, and the clinicaldifferential diagnoses are manifold.

d In this series of 52 cases we identifieddermatoscopic criteria that enable theclinician to differentiate pigmentedBowen’s disease from other pigmentedskin lesions.

d A linear arrangement of brown and/orgray dots and/or coiled vessels has notbeen described previously in otherlesions and represents a specific clue topigmented Bowen’s disease.

sied or excised, this seriesrepresents all cases of pBDdiagnosed by the authors inthis time period. Clinicalgross images were also avail-able for 46 of these lesions.Dermatoscopic images wereobtained by using a varietyof dermatoscopes and digitalcameras. These images wereanalyzed independently by4 of us (A.C., C.R., P.T., andH.K.) on a computer screen,using the method of patternanalysis described by Kittler.9

Vascular structures were de-scribed using the classifica-tion system of Kittler et al.10

Both these classifications areoutlined later in this article.

Histopathologic sections stained with hematoxylinand eosin were available from 48 cases. The sectionsof 4 cases could not be used for dermatoscopic/der-matopathologic correlation because they were toosuperficial. The evaluation of the remaining 44 slideswas performed by two dermatopathologists (E. R.,H. K.) without knowledge of the correspondingdermatoscopic image. We rated the cases with regardto hyperpigmentation of basal keratinocytes, mela-nophages in the dermis, inflammation, and dilatedvessels. We used the following 3 categories to ratethese features: absent, weakly to moderately present,and striking. We also looked for histopathologic signsof ultraviolet damage (solar elastosis) and recordedadjacent solar lentigines.

Pattern analysisFor the purpose of this study we used the method

of pattern analysis as described by Kittler9 fordermatoscopic analysis. This method uses a stan-dardized description of pigmented lesions based onpatterns, colors, and clues. Basic elements includingdots, lines, clods, and circles are given objectivegeometric definitions. A dot is a tiny round spot (nolength, no breadth). A line is a structure with paralleledges in which the length is much greater than thebreadth. A clod is any solid object larger than a dotand may have any shape. A circle is a curved line

equidistant from a fixed point. An area without anyof the basic elements dominating is termedstructureless.

A pattern is a collection of multiple basic elementsof the same type that covers a significant part of thelesion. A pigmented lesion may consist of one patternor more than one pattern. If more than one pattern is

present, the arrangement ofpatterns may be symmetric orasymmetric.

Colors observed by der-matoscopy may be due tothe presence of melanin orto other pigments, such ashemoglobin. Melanin mayappear brown, black, gray,or blue, depending on itsposition in the skin. If mel-anin is mixed with keratin,it may appear orange. Forthe purpose of this study,white, pink, or skin-coloredzones are described as‘‘hypopigmented’’.

A clue is a given feature(eg, a certain arrangement ofbasic elements or a particular

appearance of vessels) that is correlated with aspecific diagnosis.

Vascular structures may appear as dots, clods, orlines.10 If they appear as lines, vessels may be straight(no bend), curved (one gentle bend), looped (onemajor bend approximating 180 degrees), serpentine(multiple bends, snakelike), helical (multiple bendsalong a central axis), or coiled (multiple tight bends,convoluted compactly). Prominent coiled vesselscorrespond to what has been described as ‘‘glomer-ular’’ vessels by other authors.11,12 If one type ofvessel clearly dominates, the vascular pattern istermed ‘‘monomorphous’’; if two or more types ofvessels are present, we call it ‘‘polymorphous’’.

Statistical analysisContinuous data are given as mean and standard

deviation. The chi-square test or Fisher’s exact testwas used for the comparison of proportions. Allgiven P values are two tailed and a P value of lessthan .05 was regarded as indicating statisticalsignificance.

RESULTSGeneral data

Of 951 histopathologically verified cases of BDthat underwent biopsy during the study period,52 (5.5%) were pigmented. Twenty-three cases

Table I. Dermatoscopic characteristics ofpigmented Bowen’s disease

Criterion No. of cases (%)

PatternsOne pattern only

Only dots 2 (3.8)Only structureless 25 (48.1)

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(44.2%) of pBD occurred on the extremities, 20(38.5%) on the trunk, and 9 (17.3%) on the head orneck. The mean age of the patients was 67 years(SD 6 12 years), and 40.3% (n = 21) of them werefemale. According to the original histopathologicdiagnosis, 17.3% (n = 9) occurred in association witha seborrheic keratosis.

Only circles 1 (1.9)More than one pattern

Structureless and dots 18 (34.6)Structureless and lines 3 (5.8)Structureless and circles 3 (5.8)

ColorsOne color only

Brown 23 (44.2)Gray 1 (1.9)

More than one colorBrown and pink 14 (26.9)Brown and gray 8 (15.4)

Clinical appearanceThe most common clinical presentation was a flat

or slightly elevated, sharply demarcated, light brownor variegated papule or plaque with varying degreesof scaling. The differential diagnosis clinically in-cluded melanocytic lesions (either a nevus or amelanoma), solar lentigo, or seborrheic keratosis,lichen planuselike keratosis, pigmented actinic ker-atosis, and pigmented basal cell carcinoma.

Brown, pink, and gray 6 (11.5)Clues*

Brown or gray dots arranged inlinear fashion

11 (21.2)

Hypopigmented (pink, skin colored orwhite) structureless zone

35 (67.3)

Coiled vessels 23 (44.2)Vessels arranged in linear fashion 6 (11.5)Vessels arranged in clusters 3 (5.8)No clue 5 (9.6)

*Frequencies do not sum to 100% because more than one clue

may be present per lesion.

Dermatoscopic appearanceTwenty-eight cases of pBD (53.8%) had only one

pattern, 46.2% (n = 24) showed two or more pat-terns. If two or more patterns were present, theywere arranged symmetrically in 12% (n = 3) andasymmetrically in 88% (n = 22). Twenty-five pBDs(48.1%) were only structureless, 18 (34.6 %) showeda combination of structureless and dots, and 8(17.3%) showed other patterns (Table I). With regardto pigmentation, 37 pBDs (71.2%) were only brown,14 (26.9%) were brown and gray, and 1 (1.9%) wasonly gray. In addition to pigmented areas, hypopig-mented (pink, skin colored, or white) structurelesszones were present in 35 cases (67.2%). If dots werepresent, they were either brown (n = 5) or gray(n = 3), or brown and gray (n = 12). In all cases ofpBD, the distribution of pigment resulted in a varie-gated appearance. An important clue to pBD ob-served in our series were brown or gray dotsarranged in a linear fashion. This feature was ob-served in 21.2% (n = 11) and occurred most often atthe periphery of the lesion with the lines orientedradially. In 35 cases (67.3%), we were able to identifyvessels by dermatoscopy. The majority of cases(82.9%, n = 29) showed a monomorphic vascularpattern (one type of vessel clearly dominates). Ifvessels were visible, coiled vessels were the pre-dominant vessel type. They were present in 44.2% ofpBDs (n = 23). Vessels appearing as dots were foundin 15.4% (n = 8) and other types of vessels in 9.6%(n = 5). With regard to the arrangement of vessels, wefound that coiled vessels or vessels appearing as dotswere arranged in a linear fashion in 11.5% of cases(n = 6). Clustered vessels were found in only 3 cases(5.8%).

Dermatoscopic/dermatopathologiccorrelation

Histopathologic sections were suitable for derma-toscopic/dermatopathologic correlation in 44 cases.pBD occurred in association with a seborrheic ker-atosis in 13.6% (n = 6) of all cases available forhistopathologic review. Solar lentigines were pre-sent in close proximity to pBD in 17 cases (38.6%).

Hyperpigmentation of basal keratinocytes wasabsent in only 6 cases (13.6%), all of them showinglarge hypopigmented zones dermatoscopically. TwopBDs (4.5%) showed striking hyperpigmentationthat corresponded to a relatively intense dark brownhue dermatoscopically; the remaining cases (n = 36,81.9%) showed mild to moderate hyperpigmenta-tion. Melanophages in the dermis were absent in 11cases (25.0%), sparse in 14 cases (31.8%), and densein 19 cases (43.2%). If melanophages were absenthistopathologically (n = 11, 25.0%), gray dots wereabsent dermatoscopically. If melanophages weresparse (n = 14, 31.8%), gray dots were present in21.4%; if melanophages were dense (n = 19, 43.2%),the frequency of gray dots was 47.4% (P value for

Fig 1. Clinical (at left) and corresponding dermatoscopic images (at right) of 3 cases of pBD.Typical examples for pigmented BD with structureless pattern on dermatoscopy (right column:B, D, F). Clinically (left column), a slightly variegated brown plaque with no (A, C) or moderate(E) surface scale is visible, representing a wide range of differential diagnoses includingseborrheic keratosis, melanocytic nevus, basal cell carcinoma, and melanoma. Dermatoscopi-cally, the overall pattern is structureless and colors are light brown and skin colored. A few graydots visible in F are in line with the diagnosis of pigmented BD. D and F, Presence of coiledvessels allows diagnosis of pBD with confidence. B, Some vessels appear as dots, others assmall coils.

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difference between groups \.001). Inflammationwas absent in 15.9% (n = 7), sparse in 36.4%(n = 16), and dense in 45.5% (n = 20). Inflammationdid not correlate with dermatoscopic features.Dilated vessels in the papillary dermis were seen in63.3% of cases (n = 28). If dilated vessels wereprominent histopathologically (n = 17, 38.6%),coiled vessels were visible dermatoscopically in58.8% (n = 10). If dilated vessels were sparse(n = 11, 25%), coiled vessels were present in45.5% (n = 5); if dilated vessels were absent

histopathologically (n = 16, 36.4%), coiled vesselswere visible dermatoscopically in 25% (P value forthe difference between groups \.001).

DISCUSSIONThe pigmented variant of BD has been considered

rare. Previous published reports have been casestudies and one series of 14 cases.1-8 In a review of420 cases of BD, only 7 (1.7%) were pigmented.5 Ourfindings are markedly different. Audits conducted atthe participating practices during the course of this

Fig 2. Clinical and dermatoscopic images of a case of pBD. Differential diagnoses of theclinical image (A) include lichen planuselike keratosis, basal cell carcinoma, and melanoma. B,Dermatoscopically this case is a typical example of pigmented BD with two patterns: dots andstructureless. Scaly clinical appearance (A), the focal arrangement of gray dots in lines (C), andcoiled vessels (D, arrows) allow this lesion to be confidently diagnosed as pigmented BD.

Fig 3. Clinical and dermatoscopic images of a case of pBD. (n = 23) A, Differential diagnoses ofthe clinical image include lichen planuselike keratosis, seborrheic keratosis, basal cellcarcinoma, and melanoma. B, Dermatoscopically, this typical case of pBD shows two patterns:dots and structureless. The structureless zone is skin colored; dots are brown. The scaly clinicalappearance (A), the focal arrangement of brown dots in lines (C, rectangle), and coiled vessels(D, arrows) allow this lesion to be confidently diagnosed as pBD.

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Fig 4. pBD as a simulator of other pigmented lesions. pBD clinically simulating melanoma ( toprow, left), pigmented seborrheic keratosis (middle row, left), or lichen planuselike keratosis(bottom row, left). At lesions’ periphery, dermatoscopy shows lines of brown dots ( top row,middle and right), coiled vessels (middle row, middle and right) and gray dots (bottom row,middle and right), suggesting the diagnosis of pBD.

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study show that 5.5% of all cases of BD werepigmented according to the definition used in thisstudy. In these audit periods, pBD was more com-mon than invasive melanoma (52 pBD and 36invasive melanomas).

Like most other pigmented lesions, pBD may takea variety of clinical and dermatoscopic appearances.The most common appearance noted in our serieswas the structureless pattern seen in nearly half ofour cases (Fig 1). Brown was the predominant colorin these lesions, with variegation present in varyingdegrees. Variants of this structureless brown patternwere seen, with some circles or dots seen on astructureless brown background. As ‘‘structureless’’is the least specific dermatoscopic pattern, pBD withthis pattern and no vessels may not be able to bespecifically diagnosed by dermatoscopy alone. Themost common differential diagnosis of this appear-ance in practice will be from seborrheic keratosis and

various melanocytic lesions, both benign and malig-nant, and, less commonly, basal cell carcinoma. Thepresence of coiled vessels (Fig 1, C and E ) may allowa diagnosis of pBD to be reached.

The asymmetric combination of the patterns,structureless and dots, was the other commonappearance (Fig 2). The structureless zone in theselesions is usually hypopigmented (skin-colored,white, or pink) in contrast to the brown found inthe one-pattern lesions. The structureless zone wasalmost always eccentric. In 11 lesions (21%), thesedots were arranged as radial lines in the periphery(Fig 3, C ). When brown and gray pigmentation isprominent, these lesions may mimic melanoma (seeFig 2, B). Those lesions with pink structureless zonesand fewer dots may mimic lichen planuselikekeratosis (Fig 2, D)

Two thirds of lesions had identifiable bloodvessels, somewhat less than reported for all BD

Fig 5. Dermatoscopic/dermatopathologic correlation. A, Structureless brown zone of pBDcorresponds to hyperpigmentation of basal keratinocytes (B). Because of acanthosis, noreticular lines are visible dermatoscopically. Gray dots of pBD lesion (C) correspond tomelanophages in the papillary dermis (D, arrows).

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lesions by Argenziano et al11 and Pan et al.12 Only 6lesions showed polymorphous vessels. Coiled(23/52) and dotted (8/52) vessels were the mostcommon. Pan et al12 described a clustered pattern ofvessels in 84% of unpigmented BD. In this series ofpBD, only 3 lesions showed clustering of vessels.However, we did note the arrangement of coils aslines in 6 lesions (11.5%). When vessels are seen inthis arrangement, the outline of the individual coils isusually noted to be elliptical, with the long axis of theellipses oriented in the direction of the line (see Fig 3,F ). The arrangement of dots or vessels as lines hasnot, to our knowledge, been previously noted forany lesion, but is noted in more than 20% of ourcases. We postulate that this arrangement in lines ofcoiled vessels and/or dots (gray and/or brown) is ahighly specific clue for pBD, in particular allowingdifferential diagnosis from melanoma (Fig 2, B andD, and Fig 3, C and F ).

With regard to dermatoscopic/dermatopathologiccorrelation, we found that brown pigment corre-sponds to melanin in keratinocytes. If only basalkeratinocytes are pigmented, the pattern observeddermatoscopically is structureless brown (Fig 4).Because of the marked acanthosis of the epidermiswith loss of rete ridges, hyperpigmentation of basal

keratinocytes does not usually result in reticular lines(‘‘pigment network’’), being seen in only 2 cases(3.8%). Small collections of pigment in higher levelsof the epidermis correspond to brown dots derma-toscopically. Gray dots, on the other hand, come intobeing because of the presence of melanophages inthe papillary dermis (Fig 5). Coiled vessels corre-spond to dilated vessels in the papillary dermis. Wewere not able to identify the reason for the lineararrangement of dots and vessels observed in somecases of pBD. Although linear arrangement of dotsand vessels appears to be specific for pigmented BD,linear or serpiginous arrangement of coiled vesselshas also been described as a specific feature of clearcell acanthoma. However, the differential diagnosisof pigmented BD from clear cell acanthoma is rarelydifficult in practice.

It is interesting that a considerable number ofcases of pBD arose in association with a seborrheickeratosis. This association was also reported byothers. Frequently solar lentigines were found inclose proximity to pBD, raising the possibility thatthe pigmentation of BD can be attributed to acollision with a solar lentigo. Although this may betrue for some cases, we do not regard this as the onlyexplanation. In the same way as other proliferations

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of keratinocytes (eg, seborrheic keratoses), BD mayinduce melanin production, thereby leading to hy-perpigmentation. This point of view is confirmed bythe finding that BD lesions can be pigmented even inthe absence of solar lentigines (eg, when occurringin the genital area).

In summation, we were able to characterize twoarchetypical dermatoscopic patterns of pBD, namelya structureless brown pattern and a combination ofdots and structureless pattern. We have identified thedermatoscopic feature of the arrangement in lines ofbrown and/or gray dots and/or coiled vessels.Although this feature appears to be specific to pBDand has not, to our knowledge, been reported inother lesions, the true specificity could not be calcu-lated because we did not analyze its frequency inother pigmented skin lesions.

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