Dermoscopy of Pigmented Seborrheic Keratosis a Morphological Study

STUDY Dermoscopy of Pigmented Seborrheic Keratosis A Morphological Study

Ralph Peter Braun, MD; Harold S. Rabinovitz, MD; Joachim Krischer, MD; Ju¨rgen Kreusch, MD; Margaret Oliviero, ARNP; Luigi Naldi, MD; Alfred W. Kopf, MD; Jean H. Saurat, MD

Objectives: To describe morphological features of seb- Main Outcome Measures: Identification of new orrheic keratosis as seen by dermoscopy and to investi- morphological criteria and evaluation of frequency. gate their prevalence. Results: A total of 15 morphological dermoscopic crite- Design: Prospective cohort study using macrophotog- ria were identified. Standard criteria such as milialike cysts raphy and dermoscopy for the documentation of sebor- and comedolike openings were found in a high number of rheic keratosis. cases (135 and 144, respectively). We found network and networklike structures to be present in 94 lesions (46%). Using standard diagnostic criteria for seborrheic kerato- Settings: Seborrheic keratoses were prospectively col- sis, 30 lesions would not have been diagnosed as such. lected in 2 sites: a private practice in Plantation, Fla (site 1), and the Department of Dermatology at the Univer- Conclusions: The classic dermoscopic criteria for seb- sity Hospital Geneva in Switzerland (site 2). orrheic keratosis (milialike cysts and comedolike openings) have a high prevalence but the use of additional der- Patients: A total of 203 pigmented seborrheic kerato- moscopic criteria such as fissures, hairpin blood vessels, ses (from 192 patients) with complete documentation sharp demarcation, and moth-eaten borders improves the were collected (111 from site 1 and 93 from site 2). diagnostic accuracy. The proper identification of pigment network and networklike structures is important Interventions: Screening for new morphological fea- for the correct diagnosis. tures of seborrheic keratosis and evaluation of all lesions for the prevalence of these criteria. Arch Dermatol. 2002;138:1556-1560

N THE PAST 2 decades, there has includes 2 different levels. In the first level, been a rising incidence of malig- one must determine if a lesion is of mela- nant melanoma.1-6 Due to a lack of nocytic or nonmelanocytic origin. For this adequate therapies for metastatic decision, an algorithm using morphologi- melanoma, the best treatment is cal key criteria has been proposed. Once the still early diagnosis and prompt surgical lesion is identified to be of melanocytic ori- I 3 From the Pigmented Skin excision of the primary cancer. Dermo- gin, it must be categorized as benign, sus- Lesion Clinic, Department scopy (also known as epiluminescence pect, or malignant (second level). To ac- of Dermatology, University microscopy, dermatoscopy, and skin- complish this, 4 different approaches have Hospital Geneva, Geneva, surface microscopy) is a simple, noninva- been proposed: ABCD rule of dermos- Switzerland (Drs Braun, 24,28 17,29,30 Krischer, Naldi, and Saurat); sive, in vivo method that has been de- copy, Menzies method, 7-point 10 19 Skin and Cancer Associates, scribed as a useful tool for the early checklist, and pattern analysis. Diagno- Plantation, Fla, and recognition of malignant melanoma.7-24 The sis of seborrheic keratosis is, in general, a Department of Dermatology, performance of dermoscopy has been in- clinical diagnosis, but in a certain percent- University of Miami School vestigated by many authors. Its use in- age of cases, differential diagnosis be- of Medicine, Miami, Fla creases diagnostic accuracy 5% to 30% over tween pigmented seborrheic keratosis and (Dr Rabinovitz and clinical visual inspection alone, depend- malignant melanoma is difficult. The most Ms Oliviero); and Ronald ing on the type of skin lesions and experi- common dermoscopic characteristics for O. Perelman Department 25,26 of Dermatology, New York ence of the physician. According to the seborrheic keratoses are comedolike open- University School of Medicine, guidelines of the Consensus NetMeeting on ings and milialike cysts (Figure 1). Mil- 27 New York (Dr Kopf). Dermoscopy (held in Rome in February ialike cysts are round, whitish or yellow- Dr Kreusch is in private 2001; see Web site at http://www ish structures that correspond to small practice in Lu¨beck, Germany. .dermoscopy.org), the diagnostic strategy intraepidermal, keratin-filled cysts.17,31-35

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©2002 American Medical Association. All rights reserved. Downloaded From: https://jamanetwork.com/ on 10/02/2021 Frequencies and Distribution of the Criteria Identified in Step 1 According to Elementary Lesion Type

No. (%) of Lesions

Papule/ Total Patch Plaque Nodule No. Face 18 (64) 8 (29) 2 (7) 28 Border Moth eaten 31 (33) 44 (47) 19 (20) 94 Sharply demarcated 32 (17) 91 (50) 60 (33) 183 Criteria Hairpin vessels 8 (6) 65 (50) 56 (43) 129 Comedolike openings 13 (9) 79 (55) 52 (36) 144 Fissures 12 (10) 69 (56) 43 (35) 124 Milialike cysts 19 (14) 68 (50) 48 (36) 135 Networklike structures 27 (29) 54 (57) 13 (14) 94 Prominent network 19 (29) 37 (56) 10 (15) 66 Thickened network 11 (19) 38 (66) 9 (16) 58 Heterogenic network 23 (38) 31 (51) 7 (11) 61 Fingerprinting 10 (100) 0 0 10 Blotch 0 12 (75) 4 (25) 16 Crust 0 13 (42) 18 (58) 31 Dots 9 (35) 14 (54) 3 (12) 26 Whitish veil 0 0 3 (100) 3 Exophytic papillary structure 0 12 (75) 4 (25) 16 Colors Light brown 38 (20) 97 (51) 56 (29) 191 Dark brown 38 (20) 100 (52) 55 (28) 193 Blue gray 12 (11) 55 (51) 41 (38) 108 Yellowish 1 (8) 4 (33) 7 (58) 12 Figure 1. A, Macroscopic photograph of a seborrheic keratosis Maroonish 0 4 (44) 5 (56) 9 (papular/nodular type). B, Dermoscopy shows a sharply demarcated lesion Black 4 (8) 23 (47) 22 (45) 49 with multiple milialike cysts (arrows) and comedolike openings (asterisk). Total 39 (19) 101 (50) 63 (31) 203

They may also be seen in some congenital nevi and in request or in difficult cases (ie, melanocytic lesion could not some papillomatous melanocytic nevi. Comedolike be ruled out with certainty). All slides (clinical and dermo- openings (pseudofollicular openings, crypts) are scopic), were reviewed by 2 physicians experienced in dermos- mainly seen in seborrheic keratosis or papillomatous copy (R.P.B. and H.S.R.). During this first evaluation, both authors recorded all morphological findings to define more melanocytic nevi. Keratin-filled invaginations of the precisely the entity of seborrheic keratosis. In the second step, epidermis correspond histopathologically to comedo- both authors reevaluated all lesions for presence or absence of 17,31-35 like structures. the morphological features previously identified. For the de- The purpose of this report was to review dermo- scriptive statistics, the SPSS 9.0 software package (SPSS Inc, scopic criteria of pigmented seborrheic keratosis, some Chicago, Ill) was used. of which have not been clearly defined in the literature. RESULTS METHODS A total of 203 pigmented seborrheic keratoses were col- Two sources of clinical cases were used in this study. These lected (111 lesions from site 1 and 92 lesions from site sites were Skin and Cancer Associates, Plantation, Fla (site 1), and the Pigmented Skin Lesion Clinic, Department of Der- 2). Histopathologic examination was performed in 99 le- matology, University Hospital Geneva, Geneva, Switzerland sions (89/2%) from site 1 and 85 lesions (91%) from site (site 2). 2. In the first step (examination of both macroscopic and All pigmented seborrheic keratoses were examined by ex- dermoscopic photographs of all lesions by both investi- perienced “dermoscopists” using a handheld dermoscope (Der- gators), a total of 15 morphological dermoscopic crite- matoscope [Heine AG], Episcope [Welch-Allyn], or Dermo- ria and 6 colors were identified (Table). The elemen- Genius basic [Rodenstock Pra¨zisionsoptik]). All pigmented tary lesion (patch, plaque, and papular/nodular) was seborrheic keratoses data were collected prospectively (3 years identified on the clinical image. The reticulated type of at site 1 and 6 months at site 2). A macroscopic clinical pho- seborrheic keratosis was mainly found in patch lesions tograph (Slue imaging system; Canfield Clinical Systems, Fair- and the acanthotic type was mainly found in thicker le- field, NJ) and documentation of the dermoscopic finding (Der- maphot lens, Heine AG) was performed for every lesion. Since sions (plaque and papular/nodular). the diagnosis of pigmented seborrheic keratoses is usually clini- In the second step, all lesions were evaluated for cal, we considered systematic biopsy (and histopathologic ex- the presence of the morphological criteria identified in amination) as unethical, even though this might introduce a the first step. The frequencies of the criteria are shown selection bias. Therefore, a biopsy was performed on patient in the Table. We found 28 lesions of the face while 175

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B B

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Figure 2. A, Macroscopic photograph of a seborrheic keratosis Figure 3. A, Macroscopic photograph of a seborrheic keratosis (plaque type). (papular/nodular type). B, Dermoscopy shows a sharply demarcated lesion B, Dermoscopy shows a sharply demarcated lesion with multiple fissures that with a moth-eaten border (arrows), networklike structures (asterisks), give the lesion a brainlike appearance. milialike cysts, and some comedolike openings.

lesions were located elsewhere. Elementary lesions (47%), and 19 papular/nodular lesions (20%). By defini- were distributed as follows: 39 patch lesions (19%), 101 tion, a “moth-eaten” border is sharply demarcated, but not plaque lesions (50%), and 63 papular/nodular lesions all sharply demarcated lesions have a moth-eaten border. (31%). Hairpin vessels were found in 129 lesions (63%). They were mainly found in thicker lesions (94% COMMENT plaque or papular/nodular lesions). Of the 203 seborrheic keratoses, 183 lesions were sharply demarcated There are many publications on the differential diagno- (90%). sis of pigmented skin lesions. According to the proposal Comedolike openings were found in 144 lesions (71%) by the Board of the Consensus NetMeeting on Dermos- (Figure 1 and Figure 2) and 91% of the lesions with com- copy, 2 decisions on different levels have to be made: the edolike openings were plaque or papular/nodular lesions. first decision (level I) is whether the lesion is of mela- Milialike cysts (Figures 1 and 2) were found in 135 le- nocytic or nonmelanocytic origin.27 sions (66%) and 86% of them were either plaque or papular/ Once the lesion is identified as melanocytic, it is fur- nodular lesions. The number of milialike cysts ranged from ther classified as benign, suspect, or malignant (level II 1 to 184, with a mean of 15 (median, 4). decision). For seborrheic keratosis, the first level deci- Lesions were light brown in 191 (94%) and dark brown sion (melanocytic vs nonmelanocytic) is the most im- in 193 (95%). Blue-gray was present in 108 (53%) lesions portant. If a seborrheic keratosis is considered to be a me- (57% of the lesions from site 1 and 43% from site 2). lanocytic lesion, the lesion might be classified as malignant Network (Figure 2) was found in 94 lesions (46%): in many cases. prominent network in 66 lesions (32%), thickened net- One of the key criterion of the algorithm is the pres- work in 58 (28%), and heterogenic network in 61 le- ence of pigment network in the first step of the algo- sions (30%). An exophytic papillary structure was found rithm. The term “pigment network” corresponds to the in 8% of the seborrheic keratoses (75% in plaque and 25% thin, gridlike network consisting of pigmented “lines” and papular/nodular lesions).36 Fissures (Figure 3) were hypopigmented “holes”31 and should be reserved for me- found in 124 lesions (61%): 12 (10%) of them were patch lanocytic lesions.17,32-35 The anatomical basis of the latter lesions, 69 were plaque lesions (56%), and 43 (35%) were is melanin pigment in keratinocytes or in melanocytes along papular/nodular lesions. A total of 90% of lesions with the dermoepidermal junction. The reticulation (net- fissures were thicker lesions (plaque or papular/nodular). work) represents the rete ridge pattern of the epidermis. A moth-eaten border (Figure 2) was found in 94 le- The relatively hypomelanotic holes in the network corre- sions (46%): 31 patch lesions (33%), 44 plaque lesions spond to tips of the dermal papillae37 and the overlying

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©2002 American Medical Association. All rights reserved. Downloaded From: https://jamanetwork.com/ on 10/02/2021 suprapapillary plates of the epidermis.33 In our series, 94 lesions (46%) had a network and thus would be classi- A fied as melanocytic lesions in the level I decision, and in the level II decision (benign vs suspect vs malignant), some would have been classified as malignant or “suspect.” By reviewing all seborrheic keratoses where “network” was rated positive, we realized that this structure did not correspond to the classic “pigment network” of melanocytic lesions (as described above) but resembled them. Therefore, we proposed the term “networklike structures” (Figure 2). The lines of these structures are often hyperpigmented and may end abruptly at the periphery. The grids of these “networklike structures” are much larger than the one seen in a typical pigment network and the holes do not always correspond to the tips B of the dermal papillae, but to keratin-filled structures (fissures, comedolike openings). We found these network- ∗ like structures in 46% of all lesions in our study. This high percentage might be because we focused on pigmented seborrheic keratosis and therefore might have introduced a selection bias. Another type of “network” that may be seen in a solar lentigo or an early seborrheic keratosis is “fingerprinting.”38 These are networks that are light brown and delicate, and have a fingerprint pattern. Even if one ignores the first step of the algorithm (evaluation for the presence of pigment network, branched streaks, or aggregated globules), the second step is also a Figure 4. A, Macroscopic photograph of a seborrheic keratosis potential source for misclassification. In the initial algo- (papular/nodular type). B, Dermoscopy shows a sharply demarcated lesion 34 rithm proposed by Stolz et al, the morphological criteria with multiple hairpin blood vessels surrounded by a whitish halo, some for the identification of seborrheic keratosis (step 2) were milialike cysts (arrows), and comedolike openings (asterisk). comedolike openings and milialike cysts. A total of 30 lesions (15%) did not have either criteria and would not have Fissures are irregular linear, keratin-filled depres- been identified as seborrheic keratosis. By using the addi- sions that can be seen in seborrheic keratosis. However, tional criteria presented at the Consensus NetMeeting, mis- they may be seen also in nevi with congenital patterns classification can be reduced. The use of fissures (brain- and sometimes in common melanocytic nevi. The pres- like appearance) reduces the number of misclassified cases ence of multiple fissures might give a “brainlike” appear- to 22 and the additional use of fingerprinting to 14. ance to the lesion (Figure 3). Apart from the classic criteria, 4 of the 15 morpho- The term “moth-eaten border” (Figure 2) has been logical criteria for pigmented seborrheic keratosis seemed introduced by Menzies et al17 and according to Schiffner to be helpful for the diagnosis: fissures, hairpin blood ves- et al38 is also seen in solar lentigines. Since we considered sels (clustered or grapelike), sharp demarcation, and systematic biopsy of all seborrheic keratoses to be unethi- moth-eaten border. If these 4 criteria had been added to cal, it was therefore performed on patient request or in cases the standard criteria, none of the lesions would have been where a doubt concerning the differential diagnosis re- misclassified. Since we did not test our diagnostic crite- mained (difficult cases). Even though we made this limi- ria in a set of randomly chosen pigmented skin lesions, tation, histopathological examination was performed in we are not able to determine the specificity of our crite- more than 90% of the lesions because most of the pa- ria. If one uses the algorithm for the differential diagno- tients wanted the keratoses to be removed even though sis of pigmented skin lesions, the use of these additional they were informed about its benign nature (90% of the criteria reduces the number of lesions that would have lesions that underwent biopsy). Only a minority (10% of been misclassified and therefore increases the diagnos- the cases) underwent biopsy because of a diagnostic doubt tic performance of the algorithm. and can therefore be considered as difficult lesions. This Hairpin blood vessels were found in 129 (63%) of procedure does not really introduce a selection bias be- the pigmented seborrheic keratoses (Figure 4). Accord- cause all pigmented seborrheic keratoses were included ing to Kreusch and Koch39 they correspond to long cap- in this study but not all of them underwent biopsy. illary loops, commonly seen in keratinizing tumors, and We conclude that milialike cysts and comedolike are mainly found at the border or in the periphery of the openings are excellent diagnostic criteria for the identifi- lesions. In most of the cases, clusters of blood vessels are cation of the majority of seborrheic keratoses, but that grouped together and each of them has a whitish halo the use of other criteria (fissures, hairpin blood vessels, that gives them almost a “grapelike” appearance. This typi- sharp demarcation, and moth-eaten border) decrease the cal vascular architecture is predominantly seen in seb- risk of misclassification of pigmented seborrheic kerato- orrheic keratosis. sis and has the potential to improve the diagnostic accu-

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©2002 American Medical Association. All rights reserved. Downloaded From: https://jamanetwork.com/ on 10/02/2021 racy of such (especially in difficult cases). Networklike 16. Mayer J. Systematic review of the diagnostic accuracy of dermatoscopy in structures may also be seen in seborrheic keratosis. They detecting malignant melanoma. Med J Aust. 1997;167:206-210. 17. Menzies SW, Crotty KA, Ingvar C, McCarthy WH. An Atlas of Surface Micros- have to be identified as such and should not be confused copy of Pigmented Skin Lesions. Sydney, Australia: McGraw-Hill Inc; 1996. with the typical pigment network as seen in melanocytic 18. Morton CA, MacKie RM. Clinical accuracy of the diagnosis of cutaneous malig- lesions. Otherwise, seborrheic keratoses could be mis- nant melanoma. Br J Dermatol. 1998;138:283-287. classified as melanocytic lesions. 19. Pehamberger H, Steiner A, Wolff K. In vivo epiluminescence microscopy of pigmented skin lesions, I: pattern analysis of pigmented skin lesions. J Am Acad Dermatol. 1987;17:571-583. Accepted for publication February 21, 2002. 20. Pehamberger H, Binder M, Steiner A, Wolff K. In vivo epiluminescence micros- We thank David A. Ehrlich for copyreading the copy: improvement of early diagnosis of melanoma. J Invest Dermatol. 1993; manuscript and his suggestions and comments. 100:356S-362S. Corresponding author and reprints: Ralph Peter 21. Puppin D, Salomon D, Saurat JH. Amplified surface microscopy. J Am Acad Der- Braun, MD, Pigmented Skin Lesion Clinic, Department of matol. 1998;28:923-927. 22. Schulz H. Maligne Melanome in der Auflichtmikroskopie. Hautarzt. 1994;45:15-19. Dermatology, University Hospital Geneva, 24, rue Micheli- 23. Stanganelli I, Bucchi L. Epiluminescence microscopy versus clinical evaluation du-Crest, CH-1211 Geneva 14, Switzerland (e-mail: of pigmented skin lesions: effects of operator’s training on reproducibility and [email protected]). accuracy: Dermatology and Venereology Society of the Canton of Ticino. 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