The Spectrum of Spitz Nevi a Clinicopathologic Study of 83 Cases

STUDY The Spectrum of Spitz Nevi A Clinicopathologic Study of 83 Cases

Gerardo Ferrara, MD; Giuseppe Argenziano, MD; H. Peter Soyer, MD; Sergio Chimenti, MD; Arturo Di Blasi, MD; Giovanni Pellacani, MD; Ketty Peris, MD; Domenico Piccolo, MD; Pietro Rubegni, MD; Stefania Seidenari, MD; Stefania Staibano, MD; Iris Zalaudek, MD; Gaetano De Rosa, MD

Objective: To achieve a clinicopathologic classifica- Results: Overlapping clinical, dermoscopic, and histo- tion of Spitz nevi by comparing their clinical, dermo- pathologic findings were observed among PSN, RN, and scopic, and histopathologic features. PSRN, thereby justifying their inclusion into the single PSRN diagnostic category. Asymmetry was the most fre- Design: Eighty-three cases were independently reviewed quent indicator of histopathologic ASN (79%; n=11); in by 3 histopathologists and preliminarily classified into clas- only 4 cases did dermoscopic asymmetry show no his- sic or desmoplastic Spitz nevus (CDSN, n=11), pigmented topathologic counterpart, and in those cases the discrep- Spitz nevus (PSN, n=14), Reed nevus (RN, n=16), or atypi- ancy was probably the result of an artifact of the gross cal Spitz nevus (ASN, n=14); the remaining 28 cases were sampling technique carried out with no attention to the then placed into an intermediate category (pigmented Spitz- dermoscopic features. Reed nevus, PSRN) because a unanimous diagnosis of either PSN or RN was not reached. Conclusions: Among Spitz nevi, histopathologic distinction between PSN and RN is difficult, not reproduc- Setting: University dermatology and pathology depart- ible, and may be clinically useless. A simple clinicopatho- ments and general hospital pathology departments. logic classification of these neoplasms might therefore be structured as CDSN, PSRN, and ASN. Asymmetry Patients: A sample of subjects with excised melano- should be assessed using both dermoscopic and histo- cytic lesions. pathologic analysis, and reliability in histopathologic diagnosis may be enhanced by the simultaneous evalua- Main Outcome Measure: Frequency of dermoscopic tion of the corresponding dermoscopic images. patterns within the different histopathologic subtypes of Spitz nevi. Arch Dermatol. 2005;141:1381-1387

N 1948, SOPHIE SPITZ1 DESCRIBED in young adults on the lower extremities. Author Affiliations: Pathologic a series of “melanomas of child- Although some authors continue to use the Anatomy Service, Gaetano hood” as lesions fulfilling the nosologic peculiarityReed nevus (RN),6,7,10-15 Rummo General Hospital, biologic as well as the histopatho- others regard the RN as a variant of PSN.16-21 Benevento (Drs Ferrara and logic criteria of malignancy. In- The clinicopathologic distinction between Di Blasi); Departments of deed, just 1 year later, Arthur C. Allen2 in- PSN and RN is highly controversial even Dermatology, Second University I cluded juvenile melanomas in the category among expert dermatologists and histopa- of Naples, Naples (Dr Argenziano), University of of the benign melanocytic lesions. The le- thologists. The terms spindle-cell nevus and Tor Vergata, Rome sion was originally thought to occur largely epithelioid cell nevus, introduced by Kernen 1,2 22 (Dr Chimenti), University in children, but it is now well recognized and Ackerman in 1960, have been largely of Modena, Modena that more than half of Spitz nevus cases are adopted in recent years as unifying diag- (Drs Pellacani and Seidenari), detected in patients older than 14 years,3 and nostic categories.4,6,7,19,23-27 University of L’Aquila, L’Aquila about one fourth of the cases occur in pa- In the last 20 years, dermoscopy,a (Drs Peris and Piccolo), and tients older than 30 years.4-6 A Spitz nevus term coined by Friedman et al28 in 1991 University of Siena, Siena usually presents as a solitary lesion on the (and also known as dermatoscopy, (Dr Rubegni), Italy; Department lower extremities or the face.7,8 In its clas- epiluminescence microscopy, and skin of Dermatology, Medical sic clinical appearance it is pink-red be- surface microscopy), has been increas- University of Graz, Graz, Austria (Drs Soyer and cause of the scarcity of melanin; however, ingly used as a noninvasive diagnostic Zalaudek); and the Pathology tan, brown, and even black pigmented Spitz technique for the in vivo observation 29-43 Institute of the Federico II nevi (PSN) are common as well. of pigmented skin lesions. Dermos- University of Naples, Naples In 1975, Reed et al9 described a deeply copy allows a cutaneous lesion to be (Drs Staibano and De Rosa). pigmentedmelanocyticlesion,foundmostly inspected using a handheld lens, hand-

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©2005 American Medical Association. All rights reserved. Downloaded From: http://archderm.jamanetwork.com/ by a UQ Library User on 11/12/2015 held scope (also called dermatoscope), stereomicro- face, with artifactual clefts at the interface between the nests scope, camera, or a digital imaging system. Dermos- of melanocytes and the hyperplastic epidermis. It is also copy is an in vivo microscopic observation, and, not characterized by cytologic features akin to the spindle- and surprisingly, several articles have already elucidated epithelioid-cell component of the CDSN as well as by ancil- the histopathologic correlates of the structures shown lary features of the CDSN. by means of this technique.38-43 The present study was conceived to compare dermoscopic and histopatho- Reed Nevus logic findings in a series of 83 Spitz cell nevi, as has 23,42,43 An (almost) exclusively junctional neoplasm, the RN is com- already been attempted in smaller series. posed of heavily pigmented, monomorphic, small to medium- sized spindle melanocytes, mainly arranged parallel to the skin METHODS surface. Typically, the RN is structured without sharp demarcation between the nests of melanocytes and the overlying epidermis, with the latter showing little or no hyperkeratosis- STUDY DESIGN acanthosis. Ancillary findings can include a bandlike dermal infiltration of melanophages. The cases reported in the present study were retrieved from the pathology files of the University of Graz in Austria and Atypical Spitz Nevus of the Universities of L’Aquila, Modena, Naples (Federico II University), and Siena, Italy. All of these cases had been diagnosed as either Spitz nevus or RN by the referring histo- A junctional or compound lesion not fulfilling the histopathologists. Clinical data as well as dermoscopic images pathologic criteria of melanoma, the atypical Spitz nevus were obtained from the referring physicians; none of the col- (ASN) has at least 1 of the following histopathologic fea- lected lesions had been known to recur or metastasize over a tures: asymmetry, poor lateral circumscription, predomi- follow-up period of 18 to 75 months (mean follow-up time, nance of single melanocytes over nests in lesions of at least 4 30.4 months). mm in diameter, ulceration, presence of large dermal sheets The study was conceived as a comparative evaluation of spe- of melanocytes, lack of maturation in the dermis, evidence cific histopathologic diagnoses and specific dermoscopic pat- of deep dermal mitotic figures, and extensive involvement of terns with the aim of achieving a clinicopathologic classifica- the subcutis. tion of Spitz nevi. Therefore, both histopathologic slides and dermoscopic images were first blindly reviewed by the respec- Pigmented Spitz-Reed Nevus tive experts and then reevaluated to produce a combined set of dermoscopic and histopathologic data. Moreover, to refine A further provisional category was introduced after the his- dermoscopic and histopathologic criteria used to differentiate topathologic study: pigmented Spitz-Reed nevus (PSRN). This melanoma from benign lesions, special attention was paid to category included lesions that had been diagnosed as either lesions showing atypical dermoscopic and/or histopathologic PSN or RN by each histopathologist but without unanimous features. agreement. The lack of unanimity was probably owing to the presence of largely overlapping microscopic features. The PSRN category was adopted only a posteriori to compensate HISTOPATHOLOGIC EVALUATION for the strict requirement from the beginning of the study that the histopathologists arrive at a definitive diagnosis in In each case, the detailed histopathologic classification was based every case. Cases were discarded if any other diagnostic dis- on a single hematoxylin-eosin–stained slide, which had been crepancy was raised. considered representative of the lesion by the referring pathologists. Paraffin blocks were not available for further studies. The microscopic slides were independently reviewed by 3 DERMOSCOPIC EVALUATION of us (G.F., H.P.S., and S.C.) with the adoption of the following 5 provisional categories. Clinical data concerning the age and sex of patients and the size and location of the lesions were collected from the referring physicians, who had also recorded the color of the lesions and clas- Classic or Desmoplastic Spitz Nevus sified them as pink-red, brown, or black. Cases with incomplete clinical data were excluded from the study. A junctional, compound, or dermal melanocytic neoplasm as- Dermoscopic images were available as JPEG files either ob- sociated with conspicuous epidermal hyperkeratosis or acan- tained from 35-mm color slides acquired by a Dermaphot lens thosis and with little or no pigment deposition was classified (Heine Optotechnik, Herrsching, Germany) mounted on a stan- as a classic or desmoplastic Spitz nevus (CDSN). Cytomorpho- dard reflex camera or by using a digital imaging dermoscopy sys- logically, the CDSN was characterized by melanocytes with large tem (Videocap system; DS Medica, Milan, Italy, or Molemax sys- nuclei, prominent nucleoli, and abundant ground-glass cyto- tem; Derma Instruments, Vienna, Austria). plasm with polygonal (epithelioid) and often also cigar- Reevaluation of the dermoscopic images was made by 1 of shaped (spindle) outlines. Ancillary features include Kamino us (G.A.) blinded to the histopathologic diagnosis. Dermo- bodies, edema, teleangiectasias, and fibrosis of the papillary der- scopic evaluation was made using the standard pattern analy- mis. Extensive dermal desmoplasia encircling single melano- sis criteria set forth by Pehamberger et al29 and recently re- cytes is seen in the desmoplastic variant. fined by Argenziano et al.30 Pigmented Spitz Nevus RESULTS The PSN is a junctional or compound neoplasm composed of heavily pigmented, highly cohesive spindle and/or epithe- Eighty-three cases were obtained from 25 male and 58 lioid melanocytes, parallel and perpendicular to the skin sur- female patients ranging in age from 1 to 58 years

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©2005 American Medical Association. All rights reserved. Downloaded From: http://archderm.jamanetwork.com/ by a UQ Library User on 11/12/2015 Table 1. Clinical Characteristics of 83 Cases of Spitz Nevus by Provisional Histopathologic Type*

Nevus Type

CDSN PSN RN PSRN ASN Characteristic (n = 11) (n = 14) (n = 16) (n = 28) (n = 14) Patient age, range (mean), y 5-50 (19.3) 2-48 (21.6) 1-58 4-55 (22.2) 8-34 (17.3) (22.0) Sex ratio, M:F 3:8 5:9 6:10 8:20 3:11 Lesion site, No. Head or neck 0 1 0 1 1 Trunk 2 1 4 5 1 Limbs 9 12 12 22 12 Size, range (mean), mm 5-9 (7.0) 4-8 (5.4) 3-6 (4.6) 3-7 (4.8) 4-9 (6.1) Color, No. Pink-red 5 0 0 0 1 Brown 6 5 5 7 9 Black 0 9 11 21 4

Abbreviations: ASN, atypical Spitz nevus; CDSN, classic or desmoplastic Spitz nevus; PSN, pigmented Spitz nevus; PSRN, pigmented Spitz-Reed nevus; RN, Reed nevus. *See the “Methods” section for a definition of these nevus types.

Table 2. Dermoscopic Patterns of 83 Cases of Spitz Nevus by Provisional Histopathologic Type*

Nevus Type

Dermoscopic Pattern CDSN PSN RN PSRN ASN Total Starburst 0 8 9 16 2 35 Globular 6 2 2 4 2 16 Atypical and/or multicomponent 1 2 1 3 8 15 Homogeneous 0 2 2 1 0 5 Reticular, classic 0 0 0 1 1 2 Reticular, superficial 0 0 2 3 1 6 Hypopigmented 4 0 0 0 0 4 Total 11 14 16 28 14 83

(mean age, 20.9 years). The most common lesion sites Table 2 details the distribution of the 83 lesions ac- were the limbs (81%; n=67), followed by the trunk (14%; cording to the dermoscopic pattern and the histopatho- n=12). Only 3 cases (5%) occurred on the face. Most neo- logic diagnosis. A great variability was observed in the plasms were described as brown (39%; n=32) or black dermoscopic appearance of Spitz nevi. Remarkably, how- (54.2%; n=45). Only 6 lesions (7%) were pink-red. Their ever, the starburst, globular, and atypical patterns ac- sizes ranged from 3 to 9 mm (mean size, 5.4 mm). counted for 66 (80%) of the 83 cases, thus representing Based on the given criteria, all 3 histopathologists the major dermoscopic patterns of Spitz nevi. unanimously agreed on the diagnoses in 11 cases (13%) Cases of PSN, RN, and PSRN basically showed a simi- as CDSN; 14 cases (17%) as PSN; 16 cases (19%) as RN; lar distribution of dermoscopic patterns. In particular, and 14 cases (17%) as ASN. The remaining 28 cases (34%) the starburst pattern, previously reported as highly char- received a diagnosis of either PSN or RN by each histo- acteristic of RN,23,30 was present in 9 (56%) of 16 cases pathologist without unanimous agreement.These cases of RN but also in 8 (57%) of 14 cases of PSN and in 16 were thus placed into the PSRN category. (57%) of 28 cases of PSRN. Figures 1, 2, 3, and 4 il- Table 1 summarizes the clinical features of the 83 lustrate the dermoscopic-pathologic correlations in cases cases classified according to the histopathologic diag- of RN and PSN, with both lesions showing a starburst nosis: PSN, RN, and PSRN were diagnosed at almost the pattern on dermoscopy. Because of the largely overlap- same mean age (mean age range, 21.6-22.2 years); pa- ping clinical, dermoscopic, and histopathologic fea- tients with ASN were significantly younger at the time tures among PSN, RN, and PSRN, we propose the de- of diagnosis (mean age, 17.3 years). Lesions diagnosed nomination PSRN as a unifying diagnostic category for as PSN, RN, and PSRN were usually smaller and more all of these cases. often black than lesions in the other histopathologic The association between dermoscopic and histopatho- categories. logic atypia was remarkable but not absolute. Asymme-

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©2005 American Medical Association. All rights reserved. Downloaded From: http://archderm.jamanetwork.com/ by a UQ Library User on 11/12/2015 Figure 1. Clinical (inset) and dermoscopic images from case 1, a pigmented Figure 4. Histopathologic images from case 2, a pigmented lesion on the lesion on the back of a 32-year-old man. The stereotypical starburst pattern thigh of a 28-year-old woman. A symmetric proliferation of spindle-shaped is characterized by numerous streaks regularly distributed at the periphery. melanocytes was found, with epidermal hyperplasia, hyperkeratosis, and Dermoscopic diagnosis: pigmented spindle-cell nevus of Reed. hypergranulosis. Note the discrete nests of highly cohesive melanocytes with clefts between the junctional nests and the epidermis (inset). Histopathologic diagnosis: pigmented Spitz-Reed nevus (prevailing features of Spitz nevus) (hematoxylin-eosin, original magnification ϫ25).

Figure 2. Histopathologic images from case 1, a pigmented lesion on the back of a 32-year-old man. A symmetric and deeply pigmented junctional proliferation of melanocytes was found, with bandlike dermal melanophages. Note the junctional nests of spindle melanocytes and lack of sharp Figure 5. Clinical (inset) and dermoscopic images from case 4, a lesion on demarcation between nests of melanocytes and the epidermis (inset). the thigh of a 16-year-old girl. The asymmetrically hyperpigmented lesion is Histopathologic diagnosis: pigmented Spitz-Reed nevus (prevailing features dermoscopically typified by pigmented streaks irregularly distributed at the of Reed nevus) (hematoxylin-eosin, original magnification ϫ100). periphery, black blotches, and a blue-whitish veil in the center. Dermoscopic diagnosis: melanoma.

More than half (8/15; 53%) of the lesions showing an atypical and/or multicomponent dermoscopic pattern were found to be histopathologically atypical as well. Figure 5 and Figure 6 illustrate a case of a Spitz nevus showing dermoscopic and histopathologic features, respectively, of atypia. Among the lesions showing dermoscopic atypia with no histopathologic counterpart (7/ 15), 3 lesions showed a dermoscopic image characterized by a diffuse bluish pigmentation suggestive of a regression structure or a blue-whitish veil. In these cases histopathologic analysis revealed that the bluish pigmentation was simply due to a bandlike infiltrate of melanophages. Figure 3. Clinical (inset) and dermoscopic images from case 2, a pigmented More interestingly, in 4 cases, dermoscopic atypia lesion on the thigh of a 28-year-old woman. The hyperpigmented symmetric lesion is characterized by pigmented streaks regularly distributed at its was due to a striking asymmetry that was not repre- periphery. Dermoscopic diagnosis: pigmented spindle-cell nevus of Reed. sented on histopathologic sections. This finding might point toward an underestimated limitation of histopathologic examination, namely, gross sampling car- try was by far the most common histopathologic feature ried out with no special attention to the clinical (der- of ASN (11/14; 79%) followed by the presence of deep moscopic) features of a given pigmented lesion. It has dermal mitotic figures (n=3). been already demonstrated that dermoscopy can turn

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©2005 American Medical Association. All rights reserved. Downloaded From: http://archderm.jamanetwork.com/ by a UQ Library User on 11/12/2015 Figure 6. Histopathologic images from case 4, a lesion on the thigh of a Figure 7. Clinical (inset) and dermoscopic images of case 5: a pigmented 16-year-old girl. Despite the striking architectural asymmetry, melanocytes lesion on the shoulder of a 15-year-old girl. This asymmetrically are mainly arranged in nests, are highly cohesive, and have no tendency to hyperpigmented lesion was dermoscopically typified by pigmented streaks upward spread into the epidermis. Note also the clefts above nests of irregularly distributed at the periphery, black blotches, and a blue-whitish veil melanocytes in the left part of the lesion. Histopathologic diagnosis: atypical largely replacing the streaks at the left side of the lesion. The white line Spitz nevus (hematoxylin-eosin, original magnification ϫ25). indicates the area of presumed macroscopic section further detailed in the legend to Figure 8. Dermoscopic diagnosis: melanoma.

histopathologists’ attention to the suggestive area in melanocytic lesions8; therefore, the histopathologic diagnosis can be radically different when dermoscopic information is not taken into account. Figure 7 and Figure 8 display dermoscopic and histopathologic images, respectively, of a Spitz nevus in which a poor gross sampling technique presumably led to discrep- ancies between dermoscopic and histopathologic features.

COMMENT

In recent years, dermoscopy has become the conceptual and practical link between the macrocosm of clinical dermatology and the microcosm of histopathology, allow- Figure 8. Histopathologic images from case 5, a pigmented lesion on the ing the clinician to visualize structures that are not dis- shoulder of a 15-year-old girl. Overall, the lesion appears to be small and symmetric. The junctional proliferation of melanocytes with transepidermal cernible by the naked eye. The present study provides elimination of nests is composed of highly cohesive spindle cells arranged an example of how dermoscopy can integrate the clini- perpendicular to the skin surface with clefts around some nests of cal and histopathologic data about melanocytic skin neo- melanocytes. The epidermis is consistently hyperplastic. There are only a few plasms. dermal melanophages, which cannot account for the large blue-whitish veil seen on dermoscopy (Figure 7). This discrepancy between dermoscopic and Our starting point was the adoption of a provisional histopathologic analysis can be explained by a macroscopic section histopathologic classification, which clearly demon- presumably taken along the line drawn at the right side of the lesion strated the great difficulties in distinguishing PSN (Figure 7). Histopathologic diagnosis: pigmented spindle-cell nevus (prevailing features of Spitz nevus) (hematoxylin-eosin, original from RN because of frequent overlapping histopatho- magnification ϫ100). logic findings between these 2 entities. Moreover, PSN and RN, as well as their intermediate provisional counterpart, PSRN, showed basically the same dermo- and RN. In our opinion, these data suggest that, in most scopic features; in fact, the 3 major dermoscopic cases, a clinicopathologic distinction between PSN patterns—starburst, globular, and atypical—accounted and RN cannot be adequately supported. We therefore for most cases included in this study (66/83; 80%), propose the following clinicopathologic classification with no preferential distribution among cases of PSN, of Spitz nevi. RN, and PSRN. Indeed, even the starburst pattern, pre- 1. CDSN: A subdivision of this category into 2 viously considered to be typical of RN,23,30 was separate entities is justified on the basis of the observed in 56% of cases (n=8) classified by histopa- previous histopathologic data.14,18,19 However, further thologists as clear-cut PSN. studies on larger series are needed to elucidate the der- As a corollary, the growth sequence reported by Piz- moscopic correlates of these types of melanocytic neo- zichetta et al37 in a case of PSN—–the progressive trans- plasms. formation of a globular pattern into a starburst and, in 2. PSRN: This category includes the provisional en- turn, into a homogeneous one—underscores the obser- tities PSN, RN, and PSRN of the present study. A further vation that there is no close correlation between dermo- subclassification of this category is difficult to apply, nec- scopic patterns and the histopathologic categories of PSN essarily subjective, and clinically useless.

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©2005 American Medical Association. All rights reserved. Downloaded From: http://archderm.jamanetwork.com/ by a UQ Library User on 11/12/2015 3. ASN, Either Epithelioid or Spindle-Cell Type: We pling errors by customizing the gross sampling tech- retain this category because our review of data from the nique to the dermoscopic picture of the same lesion. In literature on cases of metastasizing spitzoid neoplasms these cases, the first cut made according to the rule of demonstrates that the presence of even 1 atypical fea- halves might be guided by the most representative der- ture can be associated with an aggressive clinical course moscopic features. (data not shown). In cases in which melanoma is difficult to diagnose, The occurrence of an atypical (multicomponent) der- the attention of the histopathologist should be directed moscopic pattern in Spitz nevi is well recognized, as is to the areas of highest diagnostic relevance by means of the occurrence of melanomas with dermoscopic fea- dermoscopy.32 Data from the present study suggest that tures of Spitz nevi.23 There are some theoretical and prac- asymmetry is an important indicator of histopathologic tical reasons why the dermoscopic-pathologic correla- atypia in Spitz nevi and that this feature deserves special tion of this group of lesions is often problematic. First, attention in a setting of dermoscopic-pathologic corre- some concepts introduced in the literature have been con- lation. fusing, and among these is the relationship between the so-called Spitz nevus with atypia and metastasis27 and the Accepted for Publication: April 1, 2005. classic spitzoid melanoma. Moreover, the histopatho- Correspondence: H. Peter Soyer, MD, Department of Der- logic features of lesions with spitzoid features are often matology, Medical University of Graz, Auenbruggerplatz not definitive, creating substantial diagnostic interob- 8, A-8036 Graz, Austria ([email protected]). server disagreement.34 Finally, when dermoscopy clearly Financial Disclosure: None. reveals features of a Spitz nevus, sometimes the histo- Acknowledgment: We are very grateful to Barbara J. pathologic analysis of the same lesion supports a diag- Rutledge, PhD, for critical review and editing assis- nosis of a melanoma. Remarkably, the “spitzoid mela- tance. We are also indebted to Rosamaria Corona, MD, noma” does not have a distinctive dermoscopic for her suggestions on statistical issues related to the pres- counterpart. These diagnostic problems have led to the ent study. common practice in recent years of surgically removing all lesions in adults that show dermoscopic features akin REFERENCES to Spitz nevi.

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News and Notes

The Certifying Examination of the American Board of Dermatology (ABD) will be held at the Crowne Plaza Hotel, Chicago O’Hare, in Rosemont, Ill, on August 13 and 14, 2006. The deadline for receipt of applications is March 1, 2006. The recertification examination of the ABD will be administered online from May 1 to June 15, 2006. The deadline for receipt of applications for the recertification examination is December 15, 2005. The examination for subspecialty certification in Dermatopathology will be administered September 19, 2006, at the testing center of the American Board of Pathology in Tampa, Fla. The deadline for receipt of applications is May 1, 2006. (Dermatologists must submit applications to the ABD and pathologists to the American Board of Pa- thology.) The examination for subspecialty certification in Pediatric Derma- tology will be administered October 23, 2006. Location to be determined. The In-Training Examination for Dermatology residents (administered online at dermatology residency training centers in the United States and Canada) will be held on April 6, 2006. Deadline for receipt of applications is February 1, 2006. For further information about these examinations, contact Antoinette F. Hood, MD, American Board of Dermatology, Henry Ford Health System, One Ford Place, Detroit, MI 48202-3450 (phone: 313-874-1088; fax: 313-872-3221; e-mail: [email protected]), or check the ABD Web site at www.abderm.org.

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