Infiltrating basal cell carcinoma: a stellate peri-tumor dermatoscopy pattern as a clue to diagnosis

Background: Infiltrating basal cell carcinoma (BCC) has associated features that may be readily identified using dermatoscopy. Objective: Investigate a stellate dermatoscopy pattern extending from the peripheral margin of infiltrating BCC. Methods: A total of 741 consecutive cases of BCC were assessed retrospectively using non-polarized dermatoscopy. Following histopathologic examination, cases were categorized into six different BCC subtypes. Infiltrating cases numbered 107. This stellate feature was defined as a geometric star shaped pattern extending outwards from the circumferential peripheral edge of the tumor, and identified by white lines, vessels or uneven skin surface morphology. The percentages of infiltrating subtype within the tumor mass and tumor depth were compared, with and without the stellate pattern. Results: Infiltrating BCC displayed the stellate pattern more than other BCC subtypes. Concordance between the two observers was almost perfect for white lines: Kappa coefficient of 0.87 (95% CI: 0.0.79–0.95) P<0.01 and substantial for vessels: Kappa coefficient of 0.71 95% CI: 0.59–0.84) P<0.01. Folds were only recorded in infiltrating cases (n=3). Compared to other BCC subtypes the stellate pattern had a sensitivity of 31.7% and specificity of 94.1%. A higher mean fraction of the tumor mass containing infiltrating subtype was found when comparing stellate pattern observed to stellate pattern not observed (P<0.01). No statistically significant association was found between the tumor depth with and without the stellate pattern. Conclusion: This study found a higher incidence of the stellate pattern within infiltrating BCC compared to the other BCC subtypes. As the percentage of the infiltrating subtype within the tumors increased the incidence of the stellate pattern also increased.


Methods
Data collection occurred from 2010 to 2012 in a primary care skin cancer practice in Sydney, Australia. All cases were selected from the routine workflow. All cases were imaged using a non-polarized DermLite FOTO dermatoscope, coupled with a Canon EOS 550D camera. Following imaging, full excision and histopathologic examination, all cases were allocated to various BCC subtypes. Cases were not subjected to a preliminary partial biopsy by punch or shave to determine the histological diagnosis. Cases were excised down to subcutaneous fat as a single surgical procedure, guided by a dermatoscopy tumor margin of at least 1 mm. The authors concede that this did not fully excise all cases due to poor clinical or dermatoscopy margin definition. However, the Authors consider the residual tumor tissue volume in such cases as too small to adversely affect the relevant study results. Data collection was prospective, while dermatoscopy image assessment was retrospective. Each observer was blinded to the BCC subtype diagnosis and to the recordings of the other observer. None of the observers were treating clinicians for any of the study cases.

Inclusion criteria
All consecutive cases excised within the study timeframe were considered for inclusion. After applying the exclusion criteria, all remaining cases were included in the study.

Exclusion criteria
Any diagnostic entity other than BCC was excluded. Any collision situation with a BCC and another non-BCC diagnostic entity was excluded. These collisions were based on either clinical, dermatoscopic, or histopathologic assessments. Any known previous surgical or medical intervention involving the BCC or site of excision also led to exclusion. Sites juxtaposed to scars were excluded, as were cases occurring on sites unable to be imaged with dermatoscopy.

Introduction
Basal cell carcinoma (BCC) is a common primary malignancy of the skin. Different histopathologic subtypes have been recognized and associated with different tumor behaviors.
Tumors of the nodular and superficial subtype tend to have indolent behavior compared to those of the infiltrative subtype [1]. Defining key histopathologic features of infiltrating BCC include collagen and fibroblasts in the tumor stroma, basaloid tumor cells in small spiky or angular nests [2] and poorly defined tumor margins. Mixed subtypes are common, particularly infiltrating and nodular subtypes. Examining BCC using dermatoscopy can identify the features associated with these different subtypes. Various pigmented [3][4][5][6] and vascular [6,7]  Compared with more indolent BCC subtypes, infiltrative BCC have higher rates of incomplete surgical excision [9,10] and perineural invasion [1]. An increased incidence of infiltrating BCC has been reported following involvement, which leads to exenteration of the orbit [11]. Identifying these lesions before surgery can assist planning and management. Anecdotal observation led the authors of this study to investigate a geometrical feature surrounding some BCC observed using dermatoscopy. This feature radiates outwards from the peripheral tumor margin, in a star-like geometrical pattern. The authors propose the term "stellate pattern" to describe this feature.
Blood vessels in a radial distribution have been reported with ulcerated BCC [12]. These vessels are within the dermatoscopy-identified tumor "footprint" or margin. In contrast, the radial blood vessels featured in the stellate pattern extend from the tumor margin out into the surrounding background skin.
Recent studies [13,14] have found differences in dermatoscopy between infiltrating and other BCC subtypes. These   As well as identifying the BCC subtypes present, the percentage of the tumor that displayed an infiltrative subtype on the histopathology slides was also assessed. This was graded in increments of 10%. As the percentage of infiltrating subtype increased within the tumor mass, the stellate pattern was recorded with a higher incidence (see Table 2).
An assessment was performed of any association between tumor depth and the percentage of infiltrating subtype present under stellate pattern (observed or not observed). Only one correlation was found to be statistically significant at -0.25 (95% CI: -0.46 to -0.03) for the scenario involving no stellate pattern and observer two (see Table 3).

Discussion
The data from this study indicate that the stellate pattern has a higher incidence in BCC with the infiltrating or other sidered significant. Statistical analyses were conducted using

Central ulceration on the stellate pattern: a comparison of different basal cell carcinoma subtypes based on central ulceration on the stellate pattern
A cicatricial process from ulceration could be a confounding factor in the presentation of the stellate pattern. To investigate this possible confounding effect a sub-study was performed comparing stellate cases for central ulceration present or absent from the center of the stellate cases for different BCC subtypes.

Results
Following the application of the inclusion and exclusion criteria, a total of 741 cases remained. These 741 cases were identified on 523 patients who ranged in age from 27 to 98, with a mean age of 61. One of four different pathologists examined each specimen for histological assessment.   Table 4.
To assess the potential for the stellate pattern to be confounded by ulcer induced cicatrization within infiltrating BCC we compared the presence or absence of central ulceration on stellate cases between different subtypes of BCC.   The three stellate pattern features are either: white lines, vessels or folds. The presence of a stellate pattern was defined as having one or more of any of the three stellate pattern features associated with any lesion. All the above cases were identified by both observers as either stellate present or absent.

Conclusion
BCC may display a stellate pattern extending from the periphery of the tumor when examined using dermatoscopy. These stellate patterns may be represented by white lines, blood vessels or surface folds in a circumferential radial pattern extending outwards beyond the tumor margin. When present, these stellate patterns may offer a clue to the presence of an infiltrating BCC subtype.