Nasal basal cell carcinomas. Can we reduce surgical margins to 3 mm with complete excision?

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ANNPLA-1191; No. of Pages 7 Annales de chirurgie plastique esthétique (2016) xxx, xxx—xxx

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ORIGINAL ARTICLE

Nasal basal cell carcinomas. Can we reduce surgical margins to 3 mm with complete excision? Les carcinomes basocellulaires du nez. Des marges de 3 mm ´ re ` se comple ` te de la le ´ sion ? sont-elles compatibles avec une exe S. Konopnicki a,*, O. Hermeziu a, R. Bosc a, I. Abd Alsamad b, J.P. Meningaud a a

´ tique, centre hospitalier universitaire Henri-Mondor, Service de chirurgie plastique reconstructrice et esthe ´ chal-de-Lattre-de-Tassigny, 94010 Cre ´ teil, France AP—HP, 51, avenue du Mare b ´ teil, 40, avenue de Verdun, 94010 Service d’anatomopathologie, centre hospitalier intercommunal de Cre ´ teil, France Cre Received 29 October 2015; accepted 11 January 2016

KEYWORDS Basal cell carcinomas; Surgical excision; Surgical margins; Incomplete excision rate; Nose neoplasms

Summary Background. — The purpose of this study was to evaluate the incomplete excision rate of nasal basal cell carcinomas (BCC) resected with different margins to demonstrate that 3-mm surgical margins could be used as safety margins to reduce esthetic consequences with a low risk of incomplete excision. Methods. — All patients with BCC of the nose excised from January 1st 2008 to December 31st 2011 were included. Data were analyzed and reviewed retrospectively. Tumors were treated with different surgical margins of excision: 3 mm, 4 mm, and 5 mm. The primary outcome variable was the rate of incomplete excision. Other study variables were the histologic subtype, size, and recurrent lesions. Results. — Of the 132 patients, 115 were included corresponding on with 127 BCC. Median age was 75.5 (64—83) and sex ratio M:F = 1.05. Of the 127 BCC, 80 were aggressive histologic subtype (63%), and 11 were recurrent (8.7%). The overall rate of incomplete excision was 17.3% (n = 22). Of these 22, 17 (77.3%) were of an aggressive subtype. The incomplete excision rates within the groups were 12.5% (n = 4), 22.2% (n = 10), and 16% (n = 8), respectively within the group with 3-, 4- and 5-mm surgical margins. No significant difference was observed between the groups

* Corresponding author. E-mail address: [email protected] (S. Konopnicki). http://dx.doi.org/10.1016/j.anplas.2016.01.001 0294-1260/# 2016 Elsevier Masson SAS. All rights reserved.

Please cite this article in press as: Konopnicki S, et al. Nasal basal cell carcinomas. Can we reduce surgical margins to 3 mm with complete excision?. Ann Chir Plast Esthet (2016), http://dx.doi.org/10.1016/j.anplas.2016.01.001

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S. Konopnicki et al. (P = .519). The incomplete excision rate was not independently associated with the surgical margins, histologic subtype and recurrent type (P > .05). Conclusion. — Three-millimeters margins could possibly be used to treat nasal BCC in chosen cases. Regarding the high rate of incomplete excision, reconstruction should be performed after receiving the pathologic report. # 2016 Elsevier Masson SAS. All rights reserved.

MOTS CLÉS Carcinomes basocellulaires ; Chirurgie carcinologique ; Marges chirurgicales ; Taux d’exérèse incomplète ; Tumeurs du nez

Re ´sume ´ Objectif. — L’objectif de l’étude était d’évaluer si les marges de résection des carcinomes basocellulaires (CBC) de 3 mm étaient envisageables au niveau de la région nasale afin de limiter les séquelles esthétiques sans augmenter le risque d’exérèse incomplète. Me ´thodes. — Tous les patients avec un CBC du nez excisé du 1er janvier 2008 au 31 décembre 2011 ont été inclus. Les données ont été analysées rétrospectivement. Les tumeurs ont été réséquées avec différentes marges chirurgicales : 3, 4 et 5 mm. Le taux d’exérèse incomplète était évalué en fonction des marges chirurgicales. Les autres variables étaient le sous-type histologique, la taille, et le type récurrent. Re ´sultats. — Sur les 132 patients, 115 ont été inclus correspondant à 127 CBC. L’âge médian était de 75,5 (64—83). Sur les 127 CBC, 80 étaient de sous-type histologique agressifs (63 %), et 11 étaient récurrents (8,7 %). Le taux global d’exérèse incomplète était de 17,3 % (n = 22). Les taux d’excision incomplète dans les groupes étaient de 12,5 % (n = 4), 22,2 % (n = 10) et 16 % (n = 8), respectivement au sein du groupe de 3, 4 et 5 mm de marges chirurgicales. Aucune différence significative n’a été observée entre les groupes ( p = 0,519). Le taux d’exérèse incomplète n’a pas été associé de façon indépendante avec les marges chirurgicales, le soustype histologique et le type de récidive ( p > 0,05). Conclusion. — Trois millimètres de marges de résection pourraient être utilisées pour traiter les CBC du nez dans certains cas précis. # 2016 Elsevier Masson SAS. Tous droits réservés.

Introduction

Patients and methods

Skin basal cell carcinomas (BCC) are the most common cancers in the Caucasian population, and incidence is increasing due to aging of population and increased sun exposure [1,2]. Sunlight and UV exposure are the main risk factors associated with fair skin and light sensitivity [1,3,4]. Sun-exposed areas are most often affected in particular the head and neck region [5] and especially the nose [6,7]. Nasal BCC are responsible for significant aesthetic consequences, exhibit the higher risk of recurrence [7,8], and incomplete excision [9,10]. Surgical excision with oncological safely margins is the most commonly and effective treatment [11]. Despite recent advances of surgical procedures, reconstruction of the nose remains difficult. Regarding the complexity of nasal defects reconstruction, surgeons sometimes limit the excision margins to 3 mm. BCC optimal surgical margins used to reduce incomplete excision and recurrence rate have been evaluated by numerous reports and metaanalysis [12], but no study relates especially BCC of the nose. Based on these analysis, margins of 5 mm ensure to reduce recurrence rate but 3 mm margins could be safely used to limit the aesthetic prejudice for well demarcated BCC lesions 2 cm or smaller with 95% of cure rate [12]. The purpose of this study was to evaluate the incomplete excision rate of basal cell carcinoma of the nose resected with 3 different sizes of surgical margins. Three millimeters excision margins of nasal BCCs were evaluated as safety margins to reduce esthetic consequences with a complete excision.

Patients All patients with BCC of the nose excised by surgeons from the department of plastic and reconstructive surgery from January 1st 2008 to December 31st 2011 were included. Data were analyzed and reviewed retrospectively. Before surgery, all patients underwent an incisional biopsy, surgical resection and the margins were determined at the multidisciplinary meeting of surgical oncology including plastic surgeons, dermatologists, and oncologists. Smaller margins were accepted at the multidisciplinary meeting if there were easily delineated. During the surgery, all excisions were gauged by naked eye assessments by the plastic surgeon only. After surgical excision, reconstruction was performed immediately using skin graft or local flap either with frozen section procedure of the margins or not, or in a second step surgery after complete pathologic analysis. When the margins were incomplete, re-excision was performed.

Data management Data were collected from patients’ records, operative and pathologic reports, multidisciplinary meeting of dermatologic oncology reports, and were computerized using Excel1 software. Variable collected were age, sex, size, location of the lesion, lateral surgical excision margin, histologic subtype, if primary or recurrent lesion, and lateral positive histologic margins.

Please cite this article in press as: Konopnicki S, et al. Nasal basal cell carcinomas. Can we reduce surgical margins to 3 mm with complete excision?. Ann Chir Plast Esthet (2016), http://dx.doi.org/10.1016/j.anplas.2016.01.001

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Surgical excision margins (taken by the surgeon) were 3 to  5 mm and divided into 3 groups: group 1: 3 mm, group 2: 4 mm and group 3:  5 mm. Variables were analyzed for each group. The primary outcome variable was the rate of incomplete excision. Other study variables were the histologic subtype, size, location, and recurrent lesions. We defined incomplete excision or positive histologic margins if the edge of the tumor was exactly where the surgeons made the cut or if negative pathologic margins were under 1 mm. Histologic subtypes were divided into non-aggressive (nodular, superficial, pagetoïd) or aggressive (morpheaform, infiltrative, nodulo-infiltrative). When BCC had two different subtypes the most aggressive was retained.

Statistical analyses Descriptive statistics of categorical variables focused on proportions. Medians and interquartile ranges were reported for continuously coded variables. The Chi2 test was used to compare proportions. Covariates were tested for interactions and for non-linearities. The Anova test was used to compare means. Multivariable logistic regression was used to model the association between surgical excision margins, histologic subtype, recurrent type covariates, and the odds of incomplete excision rate. Regression yielded independent Odds ratio (OR), 95% confidence interval and P-value for each potential predictor. We performed Hosmer—Lemeshow Goodness of Fit statistic to evaluate model discrimination for the multivariable regression model. All statistical analyses were performed using SPSS1 21.0, with a two-sided significance level set at P < .05.

Results From January 1st 2008 to December 31st 2011, 132 patients were treated for BCC of the nose with surgical resection by Table 1

plastic surgeons, corresponding on 145 lesions. Of the 132 patients, 17 were excluded, corresponding on 18 of 145 lesions, due to a lack of data in the operative reports (n = 10), absence of BCC in the pathologic analysis because of complete excision at the biopsy (n = 6), existence of BCC and squamous cell carcinoma (SCC) in the pathology examination (n = 2), or SCC alone in the report despite BCC at the biopsy (n = 1). Of the 132 patients, 115 were included corresponding on 127 BCC. Median age was 75.5 (64—83) with 59 males (51.3%) and 56 females (48.7%), sex ratio M:F = 1.05. In all, 80 of 127 BCC were aggressive histologic subtype (63%), and 11 were recurrent (8.7%). Among 127 BCC excisions, 32 were resected with 3 mm surgical margins (group 1), 45 with 4 mm (group 2), and 50 with 5 mm (group 3). Table 1 summarized the characteristics recorded per groups. The overall incomplete excision rate (positive surgical margins) was 17.3% (n = 22). The incomplete excision rates within the groups were 12.5% (n = 4), 22.2% (n = 10), and 16% (n = 8) respectively within group 1 (3 mm), group 2 (4 mm) and group 3 (5 mm). The positive margin rate was not significantly different between the groups (Chi2, P = .513) (Fig. 1). Of the 22 incomplete excisions, 17 (77.3%) BCCs were aggressive subtype while 63 of the 105 negative pathologic margins BCCs (60%) were aggressive. No significant difference was observed between the aggressive histologic subtype rate of the incompletely excised BCCs and the negative pathologic margins’ BCCs (Chi2, P = .127). The incomplete excision rate was not significantly different between the aggressive histologic subtype BCCs (21.3%) and the non-aggressive BCCs (10.6%) (Chi2, P = .127). The number of aggressive histologic subtype was significantly different within the groups: 13 of 32 in the group 1 (40.6%), 27 of 45 in the group 2 (60%), and 40 of 50 in the group 3 (80%) (Chi2, P = .001). One BCC was recurrent within the group 1 (3.1%), 4 were recurrent within the group 2 (8.9%), and 6 within the group 3 (12%) but no significant difference was observed between the groups (Chi2,

Lesion characteristics per group.

Groups (margins)

Histological subtype

Size

n (%)

Mm

n (%)

5 6—9 10—19  20 Missing 5 6—9 10—19  20 Missing

6 4 14 1 7 7 14 11 2 11

(24) (16) (56) (4) (21.9) (20.6) (41.2) (32.3) (5.9) (24.4)

Alar Tip Dorsal Sidewall

18 8 4 3

(56.3) (25) (12.5) (9.4)

Alar Tip Dorsal Sidewall

20 6 10 9

5 6—9 10—19  20 Missing

6 9 17 6 12

(15.8) (23.7) (44.7) (15.8) (24)

Alar Tip Dorsal Sidewall

18 12 10 8

Group 1 3 mm (n = 32)

Superficial Nodular Infiltrative Morpheaform

2 (6.3) 17 (53.1) 13 (40.6) 0

Group 2 4 mm (n = 45)

Superficial Nodular Infiltrative Morpheaform

3 (6.7) 16 (35.6) 26 (57.8) 0

Superficial Nodular Infiltrative Morpheaform

1 9 32 8

Group 3 (n = 50)  5 mm 5 mm(n = 38) 6 mm (n = 1) 10 mm (n = 1) AU (n = 10)

(2) (18) (64) (16)

Location

Recurrent type n (%)

Histological (margins)

n (%)

Mm

n (%)

Recurrent Primary

1 (3.1) 31 (96.9)

(44.4) (13.3) (22.2) (20)

Recurrent Primary

4 (8.9) 41 (91.1)

1 2 3 4 5 0 2 3 4 5

4 9 11 3 5 10 3 6 17 9

(12.5) (28.1) (34.4) (9.4) (15.6) (22.2) (6.7) (13.3) (37.8) (20)

(36) (24) (20) (16)

Recurrent Primary

6 (12) 44 (88)

1 2 3 4 5

8 3 6 8 25

(16) (6) (12) (16) (50)

AU: aesthetic nasal units.

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Figure 1 Rate of incomplete excision, aggressive histologic subtype, recurrent type and large ( 1 cm) basal cell carcinomas within the group 1 (3 mm), group 2 (4 mm), and group 3 (5 mm). *P < 0.05. BCC: basal cell carcinomas.

P = .378) (Fig. 1). Mean lesion sizes were not significantly different within the groups with 9.2 mm, 9.3 mm, and 11.9 mm respectively within the group 1, 2 and 3 (Anova, P = .09). In the multivariate logistic regression analysis, the incomplete excision rate was not independently associated with the surgical margins, histologic subtype and recurrent type (Table 2).

Discussion Non-melanoma skin cancers are the most frequent cancer in the Caucasian population with highest incidence of basal cell carcinoma of the nose due to sun exposure. Nasal BCC most effective management requires surgical resection, which remains a challenge in reconstructive surgery. The current Table 2 Multivariate analysis. Association between surgical excision margins, histologic subtype, recurrent type, and incomplete excision rate. Variables Margins, mm 3 4 5 Histologic subtype Non-aggressive Aggressive Recurrence Primary Recurrent Ref.: referent variable.

Odds ratio (95% Confidence interval)

P-value

Ref. 1.67 (0.46—6.09) 0.94 (0.24—3.64)

0.435 0.928

Ref. 2.32 (0.76—7.10)

— 0.139

Ref. 1.80 (0.42—7.65)

0.429

French recommendations for the treatment of BCC of the face advocate lateral margins of 3—4 mm for primary, non-aggressive tumors (superficial, nodular), smaller than 1 cm and non nasal BCC; 4 mm  frozen section procedure or two steps surgery for recurrent superficial BCC, nodular extra-nasal BCC with size more than 1 cm, or nasal BCC smaller than 1 cm. Tumors with high rate of recurrence such as morpheaform, infiltrative, recurrent nodular, or nodular nasal BCC larger than 1 cm, require safety margins of more than 5 mm  frozen section analysis, two stages surgery or Mohs micrographic surgery (MMS). Recommended deep margins for BCC the nose reach the perichondrium. Frozen section procedure and resection in two stages are particularly indicated in cases requiring complex local flap reconstruction, resulting on laborious surgery in case of incomplete excision [13]. Mohs micrographic surgery is still underdeveloped in France due to its cost, lack of technical facilities and surgeons’ training. Furthermore, it has not been shown its superiority to surgical excision in terms of oncological and aesthetic results for primary BCC and is twice the cost [14,15]. However, MMS has been shown to be preferred over surgical excision in recurrent, aggressive, poorly defined BCC and in areas with high rates of recurrence such as the nose [14,15]. Despite the recommendations, surgeons sometimes limit the surgical margins of BCC of the nose to 3 mm instead of 5 mm to avoid esthetic consequences. Therefore, we analyzed those patients retrospectively to evaluate if there is a difference of the incomplete excision rate using 3 mm margins in comparison with larger margins. We did not show any significant difference of incomplete excision rate between the 3 groups, meaning that 3 mm surgical margins may be used to treat nasal BCCs. Median age was 75.5 years old. In the literature, median age vary from 60 [9] to 76.3 years old [16]. Regarding the histologic subtype, 63% were aggressive which is higher than

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those observe in reports including BCC from all sites. Bisson et al. reported only 4% of morpheaform and infiltrative subtype [17] whereas Wavreille et al. reported 51.1% of aggressive subtype [16] (Table 3). The incomplete excision rate was 17.3%, corresponding on the rate reported in the literature regarding the excision of nasal BCC [9,16,18—23]. Regarding all BCC, the incomplete excision rate in the recent literature vary from 1 [24] to 24% [21] depending on patient population, the place of the study, the country, the characteristic of the lesions, the type of specialist and surgeons’ experience [8,9,12,16—37] (Table 3). Ito et al. [24] and Pua et al. [8] found the lowest rates with respectively 1 and 1.54% while Hansen et al. reported 6.4% BCC excised incompletely in Australian general practitioner, with 14.3% of incomplete excision rate of nasal BCC of 6881 BCCs analyzed, corresponding on the highest population [9]. Recent meta-analysis of 16,066 BCCs have shown 85% of clearance rate [12]. The positive pathologic margins of nasal BCCs in studies range from 9 [23] to 38% [21]. The differences regarding the incomplete excision rate between the studies may be also related to the definition of the positive margin rate. Some studies defined the incomplete excision rate as the presence of the tumor at the edge

of the lesion excised or at the surgical margins [22,26]. In our study, excision was considered incomplete when histologic negative margins were less than 1 mm [16]. Incomplete excision rate have shown to be higher in ears, periauricular, nose, periocular, aggressive histologic subtype, with the increase size of the lesion, and recurrent characteristic [7—9,16,18—23,25—35,38,39]. In our study, incomplete excision was not associated with histologic subtype and recurrent BCC. Those finding are probably related to the high rate of aggressive subtype in our study, the analysis of only nasal BCC, and the evaluation of the lateral margins only. Indeed, the aggressive histologic subtypes could be more often incompletely excised in the deep margins. Consequently, a well-defined infiltrative BCC may possibly be removed using 3-mm lateral margins but with deep margins. We did not find any significant difference between the groups regarding the incomplete excision rate when surgical margins were compared meaning that 3-mm surgical margins may be used to treat nasal BCCs. We could find a bias because patients treated with a 3-mm margins surgery were probably selected patients with low-risk tumors. However, the mean lesion size was not significantly different within the groups

Table 3 Rate of incomplete excision and aggressive histologic subtype of basal cell carcinomas reported in the recent literature since 1999. Authors

Griffith et al. 1999 [19] Schreuder et al. 1999 [26] Kumar et al., 2000 [23] Bogadanov-Berezovsky et al., 2001 [30] Dieu et al., 2002 [25] Kumar et al., 2002 [24] Bisson et al., 2002 [17] Thomas et al. 2002 [31] Nagore et al., 2003 [21] Hussain et al. 2003 [27] Hsuan et al., 2004 [32] Wilson et al., 2004 [33] Gudi et al., 2006 [28] Fernandez-Jorge et al., 2006 [29] Su et al., 2007 [18] Griffith et al., 2007 [20] Farhi et al., 2007 [22] Staub et al., 2008 [7] Pua et al., 2009 [8] Hansen et al., 2009 [9] Gulleth et al., 2010 [12] (meta-analyse) Wavreille et al., 2012 [16] Abbas et al., 2012 [35] Patel et al., 2012 [36] Knani et al., 2014 [34] Ito et al., 2014 [24]

Median or mean age

68.6—73.7

74 70.6—72.1 72 72 66

72

73.4 67.4 64 69.8 60 67.7 76.3 65.6 64

Total lesions

Aggressive subtype (%)

1392 51 879 1478 3558 757 100 91 273 126 55

18% 4% 13.2%

0% Primary nodular periocular BCCs

3795 297 240 2582 1539 362 674 324 6881 16,066 184 518 247 169 288

Incomplete excision, all BCC (%)

Incomplete excision, nasal BCC (%)

7 13.73 4.7 10.8

12

6.3 4.5 4 2.2 24 8.6 18.2

9

38

6.2 9 9.2

27.8% 50.7%

Morpheaform excluded 51.1% 3.74% 34% (+ 10% mixed) 6.5% (Eyelid) 0% (well-defined, primary, pigmented BCC)

11.2 8.4 10.3 11 1.54 6.4 15

12.7 24 30.6

15 2.3 11.7 22.4 1

22.3

14.3

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but a significant difference was observed regarding the histologic subtypes. Likewise, recurrent BCCs were more often treated with 5-mm surgical margins but the number of recurrent lesions was too low to differ significantly. However, this limit could be excluded because we did not find any significant difference between the incomplete excision rate of the aggressive and non-aggressive histologic subtype. Moreover, the multivariate logistic regression analysis has shown that incomplete excision rate was not independently associated neither with the surgical margins, nor with the histologic subtype and recurrent type. Regarding the literature, reports have shown significant difference of incomplete excision rate related to the surgical margins [25,38,39] and recommended 4-mm margins for small well-defined lesions to decrease the rate of incomplete excision to 5% [38] and 5 mm for morphoeic BCC [39]. Shell et al. have compared lesion size and final defect size after MMS to calculate the margins needed if surgical excision is the only option. Lesions were categorized based on histologic characteristics, size, and recurrent status. Although mean margin were 2.4 and 3.7 mm for respectively, low- and highrisk BCCs, they reported that margins required to capture 95% of lesions were 4.75 mm (low risk) and 8 mm (high risk). Nasal BCC were not included in the high-risk group based on location alone [40]. Contrariwise, recent meta-analysis of the literature did not report significant difference of incomplete excision rate between 2-, 3-, 4- and 5 mm groups (respectively 18, 15, 15, and 15%). However, they have shown significant difference regarding the relative risk of recurrence (respectively 3.96, 2.56, 1.62, and 0.39%). Nevertheless, they excluded from the analysis, studies including morpheaform subtype data [12]. Regarding the low rate of recurrence with 3-mm margin, they reported the safely use of 3-mm surgical margins for BCC lesions 2 cm or smaller with a minimum of 95% cure rate. In our study, we did not evaluate the difference between the groups regarding the risk of recurrence because all incomplete excised lesions were re-excised, modifying the surgical margins. Interestingly, new article revealed that surgical excision with a 2—3-mm margin is reliable treatment for well-defined, primary pigmented BCC defined by dermoscopy, with a complete removal rate of 99% and, that dermoscopically determined borders almost exactly corresponded to the histopathological ones [24]. Some groups may use the curettage prior to resection. However, Jih et al. have shown that curettage does not reliably delineate the extent of a tumor [41]. Despite the use of surgical margins commonly in dermatologic oncology, the meaning of surgical margins could differ between surgeons and could limit studies [42]. In our study, we did naked eye margin excisions and did not use dermoscopy or curettage to delineate the tumor during the surgery. However, the size of the tumor and the margins were defined with the dermatologist and the surgeons prior to the surgery, using dermoscopy or not at the multidisciplinary meeting of surgical oncology. Our study evaluated only 127 lesions due to inclusion criteria including only BCCs of the nose, and the exclusion of patients with a lack of data in the reports, due to the retrospective analysis. However, although prospective randomized clinical trial could avoid those limits, it may be ethical controversial due to the use of 3-mm surgical margin in aggressive and recurrent BCCs of the nose. Prospective

clinical study focused on the non-aggressive, primary, small nasal BCC including the recurrence rate should be performed to confirm our outcomes and compared naked eye excision and dermoscopically defined borders.

Conclusion Three-millimeters surgical margins could be feasible to excise well-defined nasal BCC to reduce esthetic consequences. This population of patients needs to be defined. However, regarding the high rate of incomplete excision of BCC of the nose, reconstruction with local flap should be performed after receiving the pathologic report either with fresh frozen analysis or two stages surgery. Dermoscopically defined borders and margins may reduce the incomplete excision rate. Regarding the limit of the study, large, aggressive, poorly defined, and/or recurrent should remain to be resected with at least 5-mm margins and/or fresh frozen section or MMS. MMS should be further developed in France for those cases.

Disclosure of interest The authors declare that they have no competing interest.

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Please cite this article in press as: Konopnicki S, et al. Nasal basal cell carcinomas. Can we reduce surgical margins to 3 mm with complete excision?. Ann Chir Plast Esthet (2016), http://dx.doi.org/10.1016/j.anplas.2016.01.001