- Email: [email protected]
Anatomical restrictions in the surgical excision of scalp squamous cell carcinomas: does this affect local recurrence and regional nodal metastases?
Int. J. Oral Maxillofac. Surg. 2014; 43: 142–146 http://dx.doi.org/10.1016/j.ijom.2013.08.018, available online at http://www.sciencedirect.com
Clinical Paper Head and Neck Oncology
Anatomical restrictions in the surgical excision of scalp squamous cell carcinomas: does this affect local recurrence and regional nodal metastases?
G. Jenkins, A. B. Smith, A. N. Kanatas, D. R. Houghton, M. R. Telfer Department of Oral and Maxillofacial Surgery, York Teaching Hospital, York, UK
G. Jenkins, A.B. Smith, A.N. Kanatas, D.R. Houghton, M.R. Telfer: Anatomical restrictions in the surgical excision of scalp squamous cell carcinomas: does this affect local recurrence and regional nodal metastases?. Int. J. Oral Maxillofac. Surg. 2014; 43: 142–146. # 2013 International Association of Oral and Maxillofacial Surgeons. Published by Elsevier Ltd. All rights reserved. Abstract. Squamous cell carcinomas (SCCs) of the skin of the scalp have the potential for regional metastases. Microscopically, clearance may be less than the optimal dimensions. We report 101 SCCs of the scalp treated surgically under the care of a single oral and maxillofacial surgeon. Forty-two of the study patients had deep margins that were clear by less than 2 mm, of whom five had margins that involved pericranium skull. Our study demonstrated a local recurrence rate of 6% and a regional recurrence rate of 7%. All patients presented with relapse of the disease within 18 months of primary surgery. The evidence presented in this study suggests that in SCCs of the scalp, less than ideal surgical margin clearance, entirely due to anatomical restrictions, does not appear to substantially affect regional recurrence, but increases the risk of local recurrence.
Non-melanoma skin cancer is the most common cancer worldwide and its incidence has continued to rise over the decades.1 Ninety percent of cutaneous malignancies occur in the head and neck region,2 secondary to the lifetime accumulation of ultraviolet radiation damage3 in conjunction with skin type. It is approximated that between 10% and 20% of these malignancies are squamous cell carcinomas (SCCs).4 0901-5027/020142 + 05 $36.00/0
SCC has the potential for regional metastases, although early surgical management reduces this risk to around 5%.5 It has been recognized in the literature that particular sites of the head and neck represent a so-called ‘danger-area’ for increased risk of recurrence and metastases.2,4,6 In a recent multicentre study in Australia documenting the patterns of nodal metastases in head and neck patients diagnosed with cutaneous SCC, the scalp
Ke y w o r d s : c u t a n e o u s s q u a m o u s c e l l carcinoma; scalp; recurrence rates. Accepted for publication 29 August 2013 Available online 13 October 2013
represented the primary in the order of 10%.7 Anatomically the scalp is the cutaneous covering of the cranial vault, extending from the external occipital protuberance and superior nuchal lines to the supraorbital margins.8 The scalp has five anatomical layers that are of finite thickness, which show individual variation. However there can be some confusion with the term forehead, which encompasses the area
# 2013 International Association of Oral and Maxillofacial Surgeons. Published by Elsevier Ltd. All rights reserved.
Surgical excision of scalp SCCs marked by the hairline superiorly to the supraorbital ridges inferiorly and bound laterally by the temporal ridge.9 The recommended clinical margins for the excision of a cutaneous SCC are 4 mm for a ‘low-risk’ SCC and 6 mm for a ‘highrisk’ SCC in order to achieve a 95% histological clearance rate (there are no guidelines in millimetres for histological clearance).10,11 These distances, and greater, are usually easily achieved clinically at the peripheral margins of scalp lesions, but deep clearance is restricted by the anatomical thickness of the scalp. The purpose of this study was to address whether narrow (0.1–1.9 mm) clearance at the deep surgical margin, as measured histologically, results in a rate of local or regional recurrence above that stated in the literature, and when compared to groups with greater (2–6 mm and >6 mm) clearance at the deep surgical margin. Patients and methods
Patients recruited into the study were those treated in the maxillofacial department of the hospital. The estimated population covered by this hospital is 700,000. Data were recorded retrospectively. Ethical approval for this study was received from the hospital clinical audit department, set in the context of service evaluation. The inclusion criteria were set as follows: (1) treatment under the care of a single oral and maxillofacial surgeon in the department (MRT). (2) Patients treated between the years 2005 and 2009. This enabled appropriate follow-up in accordance with National Institute for Health and Clinical Excellence (NICE) guidelines,12 namely 6 months or less formal follow-up for ‘low-risk’ SCCs and locally agreed follow-up for ‘high-risk’ SCCs. (3) SCCs of the scalp, not including the forehead, as indicated by the anatomical description above. (4) SCCs treated primarily by surgical excision. At the study institution, cutaneous malignancies are subject to standard light microscopy histopathological preparation, namely fixation, preparation, embedding, sectioning, and finally appropriate staining. All cutaneous SCCs are discussed at a skin multi-disciplinary team (MDT) meeting. During this time-frame, 101 consecutive SCCs of the scalp were surgically removed under the care of the one oral and maxillofacial surgeon. Histopathology reports were reviewed looking specifically at the size of the lesion, differentiation of the neoplasm, and distance to the closest deep margin. Clinical
notes were appraised, verifying subsequent management, paying particular attention to local and regional recurrence. Histopathological data sets were compliant with the cancer data standard. Descriptive data were analysed using SPSS version 20 (IBM Corp., Armonk, NY, USA) and Microsoft Excel (Microsoft, Seattle, WA, USA). Results Patient demographics
Patient demographics are shown in Table 1; these fall roughly in line with the expected distribution. The mean age of the study participants was 81.7 years.
143
Table 2. Histological differential of tumours. Histological differentiation
N
Poorly differentiated Moderately differentiated Well differentiated
25 53 23
therapy; this group was not relevant to this study. We were therefore left with the main groups: 37 patients with histological marginal clearance of less than 2 mm and 39 patients with a marginal clearance of 2–6 mm, which when combined gave a group of 76 patients with marginal clearance of less than 6 mm. The last group of 20 patients had deep margin clearance greater than 6 mm; no patients in this group developed either local or regional recurrence.
Characteristics of the primary lesion
The majority of scalp SCCs treated measured between 10 mm and 50 mm in both width (56%) and length (52%). In terms of the depth of the tumour, the majority of lesions measured were less than 10 mm (59%). There was a broad range of differentiations reported on histology (Table 2). Surgical treatment – deep margin clearance
Figure 1 demonstrates the deep marginal clearance from the invasive edge of the carcinoma, broken down into groups. The standard surgical practice in this unit is resection at the deepest aspect of the lax areolar layer, i.e. on the pericranium, leaving only a very thin layer of the latter. A small number of patients for whom flap repair was planned had the pericranium removed, but as this is histologically only equivalent to 0.1 mm thick its impact is minimal. Five patients had full thickness SCCs involving the pericranium bone treated by excision including the outer table of the skull and appropriate flap repair. We expected these patients to be at higher risk and hence their cases were discussed at the MDT for consideration of adjuvant
Disease relapse – local recurrence
Figure 2 demonstrates local recurrence in the cohort. In the deep marginal clearance group of 2 mm, three patients developed local recurrence. No patients in the 2– 6 mm group developed local recurrence. The overall local recurrence rate in this study was 6%, including those involving the skull. None of the cohort had positive radial margins. However, removal of the cohort with involved pericranium or skull resulted in an overall local recurrence rate of 3% for those patients with clear histological soft tissue margins. The absolute risk of developing local recurrence with a deep margin of 2 mm with non-involved margins was 8%. Both these figures coincide with the current literature. Disease relapse – regional recurrence
Sex
Number
When reviewing regional recurrence (Fig. 3), some difference was noted. Seven patients developed regional recurrence, two patients in the 2 mm group and five patients in the 2–6 mm group. This gave an overall regional recurrence rate of 7%, coinciding with the current literature. The relative risk values of the two groups, 2 mm and >2 mm, demonstrated deep marginal clearance not to be a key factor in regional recurrence (Table 3).
Male Female Patient age ranges, years 61–65 66–70 71–75 76–80 81–85 86–90 91–95
79 22
Discussion
2 4 19 22 29 15 10
A cutaneous SCC has the potential for invasive growth, metastasis, and mortality. The risk factors for the development of a cutaneous SCC are well documented in the literature and include, but are not limited to, ultraviolet radiation, fair skin, phototherapy, ionizing radiation, chemical
Table 1. Patient demographics.
144
Jenkins et al.
Deep Margin Clearance Histologically determined clearance
20
of depth margin 6mm
39 2mm 37 Involving
Pericranium
5 Cranium
Fig. 1. Deep margin clearance from the invasive edge of the carcinoma.
carcinogens, immunosuppression, and inflammatory skin disorders.13 Figure 4 illustrates a high-risk SCC that required not only removal of the pericranium but also the outer table of the skull, necessitating flap repair. Figure 5 illustrates a conundrum. It still allows resection of the pericranium facilitating repair with a graft or flap, but anatomical restrictions mean the deep margin will be quite small. The purpose of this study was to ask the question whether reduced soft tissue clearance at the deep margin increases recurrence rates, comparing our long-term follow-up results to the current literature, and between the two chosen main groups
in the study: 2 mm and 2–6 mm deep histological clearance. If there is an increase in recurrence rates, should we be considering modifications to the current standard management of local surgical repair and monitoring as per NICE guidelines? The rates of loco-regional recurrence vary throughout the literature. Surgical departments that act as tertiary referral centres for cutaneous SCCs are likely to see higher rates when compared to dermatology centres. The general inference from the literature is that the local recurrence of SCCs ranges from 3% to 16%.2,3,14 Metastatic rates are reported at 1% to 4% for a ‘low-risk’ cutaneous SCC lesion.2 Scalp
Local Recurrence Histologically determined clearance
20
of depth margin 6mm
39 2mm 37 (3) Involving
Pericranium
5 (3)
( ) Local recurrence
Cranium
Fig. 2. Local recurrence corresponding to deep marginal clearance.
SCCs, however, showed a metastatic rate of around 10%.15 A prospective audit examining the prognostic factors for possible local or regional recurrence found that tumour size and thickness, patient immunosuppression, and localization at the ear were independent parameters determining the risk of metastasis in cutaneous SCC. Tumour thickness and grade affected the risk of local recurrence.3,15,16 A study reported by Baker et al.,17 with a study population of 227 cutaneous SCCs of which 20% (45 patients) were scalp SCCs, documented a local recurrence rate of 4%. However the most relevant aspect of this article was that the scalp represented 69% of the SCCs that were incompletely excised (16 of 227) and the deep margin was involved in all but one of the cases. Of the 11 cases not offered further treatment, only three went on to develop a recurrence. In our study, three out of five cases with involved skull at the time of surgery went on to develop local recurrence; these patients were subsequently offered radiotherapy. Though secondary treatment consists predominantly of radiotherapy, there are protagonists of more radical therapy, namely craniectomy and free tissue transfer.18 Although mentioned, this group was excluded from the current study as there was no soft tissue clearance. In the study groups, three cases developed local recurrence despite histologically clear margins, and all were in the 2 mm group. All patients presented with relapse of the disease within 18 months of primary surgery. Management of these patients consisted of further surgery and the offer of radiotherapy. The absolute risk demonstrated an increased risk of local recurrence with deep marginal clearance of 2 mm. Our study demonstrated a metastatic rate of 7%, consistent with the current literature. Again all patients presented with relapse of the disease within 18 months of primary surgery. The relative risk demonstrated deep marginal clearance not to be a key factor in regional recurrence, thus reinforcing the conclusions of previous studies that other factors probably play a more significant part in determining the risk of developing regional recurrence. As authors we accept that there are limitations to this study, particularly with reference to confounding factors when analysing risk factors for local and regional recurrence, e.g. tumour depth and differentiation. Despite the high number of patients recruited into this study, the
Surgical excision of scalp SCCs Table 3. Regional recurrence – deep margin (not including five patients with involved deep margin). Regional recurrence – deep margin
2 mm
>2 mm
Total
Yes No Relative risk
2 35 0.47
5 54 0.44
7 89
relatively low numbers who presented with recurrence make allowances for those confounding factors difficult. Continuation of the study with recruitment of patients treated from 2009 onwards, with appropriate time for follow-up, is in progress; this will target these concerns, allowing for a multivariate analysis. Additionally we plan to assess whether there is a statistical difference within the narrow clearance banding, i.e. between 1 mm clearance and 1–2 mm clearance. The scalp is one of the largest areas of sun-exposed skin, but is a relatively uncommon site for the development of metastatic SCC.5 Other ‘high-risk’ areas (ear and cheek – both expected to have similar exposure to ultraviolet radiation) have demonstrated a metastatic rate of around 20%.7 The following has been postulated: (1) the scalp is described as a unique part of the skin whose anatomy influences the behaviour of its primary neoplasms in a vital way.19 Its distinct layers, but mainly the aponeurosis, pericranium, and bony calvarium, show increased resistance to infiltration of the neoplastic cells. It is this innate resistance to infiltration that predisposes to lateral spread of the neoplastic cells, and hence an increased number of larger diameter lesions.20 (2) A patient’s hair may play a protective role in the prevention of a scalp SCC, and explains why cutaneous SCC is uncommonly found in the hair-bearing area.5 This also provides a probable explanation for the higher incidence of scalp SCCs in males than in females, as demonstrated in this study and others.4 (3) The ‘metastatic basin’ of the head and neck has been described extensively in the literature for lymphatic drainage to the parotid gland.21 The anatomical configuration of the lymphatic channels of the ear and cheek in comparison to the scalp, may explain the higher metastatic rate from these locations. All seven of the patients who developed a regional recurrence presented with enlargement of a parotid lymph node. All had deep margin clearance of the primary lesion, with two patients having clearance of 2 mm and the remaining five with
145
Regional Recurrence Histologically determined clearance
20
of depth margin 6mm
39 (5) 2mm 37 (3) (2) Involving
Pericranium
5 (3)
( ) Local recurrence
Cranium
( ) Regional recurrence Fig. 3. Regional recurrence corresponding to deep marginal clearance.
Fig. 4. SCC of the scalp requiring removal of the outer table of the skull.
Fig. 5. Intact pericranium following removal of the SCC.
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clearance between 2 and 6 mm. Six patients were offered surgery and subsequent radiotherapy, and one patient palliative radiotherapy only. The literature defends the use of adjuvant radiotherapy and surgery for operable metastatic cutaneous SCC.22 As supported in the literature,23 treatment of nodal metastases has a grave outcome and 43% died of the disease. In conclusion, all SCCs of the scalp need to be treated effectively because of the inherent risk involved. The aim of surgery remains identical to that of any cutaneous SCC, i.e. to excise with clear histological margins. The evidence presented in this study suggests that in SCCs of the scalp, less than ideal surgical margin clearance, entirely due to anatomical restrictions, does not appear to substantially affect regional recurrence, but increases the risk of local recurrence. However, the current treatment regime remains appropriate and there is no indication for more aggressive treatment unless other significant high-risk factors are present. In light of the local recurrence risk of 8% in the 2 mm group, but not involving bone, we would suggest patients be fully informed and appropriate agreed follow-up arranged. Funding
None. Competing interests
None declared. Ethical approval
Hospital clinical audit department. References 1. Gray DT, Suman VJ, Su WP, Clay RP, Harmsen WS, Roenigk RK. Trends in the population-based incidence of squamous cell carcinoma of the skin first diagnosed between 1984 and 1992. Arch Dermatol 1997;133:735–40.
2. Rowe DE, Carroll RJ, Day Jr CL. Prognostic factors for local recurrence, metastasis, and survival rates in squamous cell carcinoma of the skin, ear, and lip. Implications for treatment modality selection. J Am Acad Dermatol 1992;26:976–90. 3. Brantsch KD, Meisner C, Schonfisch B, Trilling B, Wehner-Caroli J, Rocken M, et al. Analysis of risk factors determining prognosis of cutaneous squamous-cell carcinoma: a prospective study. Lancet Oncol 2008;9:713–20. 4. Ang P, Tan AW, Goh CL. Comparison of completely versus incompletely excised cutaneous squamous cell carcinomas. Ann Acad Med Singapore 2004;33:68–70. 5. Howle JR, Morgan GJ, Kalnins I, Palme CE, Veness MJ. Metastatic cutaneous squamous cell carcinoma of the scalp. ANZ J Surg 2008;78:449–53. 6. Miller SJ, Moresi JM. Actinic keratosis, basal cell carcinoma and squamous cell carcinoma. In: Bolognia JL, Jorizzo JL, Rapini RP, editors. Dermatology. London: Mosby; 2003. p. 1677–96. 7. Vauterin TJ, Veness MJ, Morgan GJ, Poulsen MG, O’Brien C. Patterns of lymph node spread of cutaneous squamous cell carcinoma of the head and neck. Head Neck 2006;28:785–91. 8. Agur AM, Lee MJ, Grant JC. Grant’s atlas of anatomy. 9th ed. Baltimore, MD: Lippincott Williams & Wilkins; 1991: 464. 9. Knize DM, Drisko M. The forehead and temporal fossa: anatomy and technique. Philadelphia, PA: Lippincott Williams & Wilkins; 2001: 3–11. 10. Brodland DG, Zitelli JA. Surgical margins for excision of primary cutaneous squamous cell carcinoma. J Am Acad Dermatol 1992;27:241–8. 11. Motley RJ, Preston PW, Lawrence CM. Multi-professional guidelines for the management of the patient with primary cutaneous squamous cell carcinoma. London, UK: British Association of Dermatologists; 2009. 12. National Institute for Health and Clinical Excellence. Improving outcomes for people with skin tumours including melanoma. The manual. N0957. London, UK: NICE; 2006. 13. Alam M, Ratner D. Cutaneous squamous cell carcinoma. N Engl J Med 2001;344:975–83.
14. Leibovitch I, Huilgol SC, Selva D, Hill D, Richards S, Paver R. Cutaneous squamous cell carcinoma treated with Mohs micrographic surgery in Australia. Experience over 10 years. J Am Acad Dermatol 2005;53:253–60. 15. Clayman GL, Lee JJ, Holsinger FC, Zhou X, Duvic M, El-Naggar AK, et al. Mortality risk from squamous cell skin cancer. J Clin Oncol 2005;23:759–65. 16. Ch’ng S, Clark JR, Brunner M, Palme CE, Morgan GJ, Veness MJ. Relevance of the primary lesion in the prognosis of metastatic cutaneous squamous cell carcinoma. Head Neck 2013;35:190–4. 17. Baker NJ, Webb AA, Macpherson D. Surgical management of cutaneous squamous cell carcinoma of the head and neck. Br J Oral Maxillofac Surg 2001;39:87–90. 18. Abo Sedira M, Amin AA, Rifaat MA. Locally advanced tumours of the scalp: the Egyptian National Cancer Institute experience. J Egypt Natl Canc Inst 2006;18:250–7. 19. Ratzer ER, Strong EW. Squamous cell carcinoma of the scalp. Am J Surg 1967;114: 67–76. 20. Mohs FE, Zitelli JA. Microscopically controlled surgery in the treatment of carcinoma of the scalp. Arch Dermatol 1981;117: 764–9. 21. O’Brien CJ. The parotid gland as a metastatic basin for cutaneous cancer. Arch Otolaryngol Head Neck Surg 2005;131: 551–5. 22. Veness MJ, Porceddu S, Palme CE, Morgan GJ. Cutaneous head and neck squamous cell carcinoma metastatic to parotid and cervical lymph nodes. Head Neck 2007;29: 621–31. 23. Lang PG, Martin MS, Kwatra R. Aggressive squamous cell carcinoma of the scalp. Dermatol Surg 2006;142:755–8.
Address: Glyndwr W. Jenkins Department of Oral and Maxillofacial Surgery York Teaching Hospital Wigginton Road York YO31 8HE UK Tel.: +44 07941 537245 E-mail: [email protected]
Clinical Paper Head and Neck Oncology
Anatomical restrictions in the surgical excision of scalp squamous cell carcinomas: does this affect local recurrence and regional nodal metastases?
G. Jenkins, A. B. Smith, A. N. Kanatas, D. R. Houghton, M. R. Telfer Department of Oral and Maxillofacial Surgery, York Teaching Hospital, York, UK
G. Jenkins, A.B. Smith, A.N. Kanatas, D.R. Houghton, M.R. Telfer: Anatomical restrictions in the surgical excision of scalp squamous cell carcinomas: does this affect local recurrence and regional nodal metastases?. Int. J. Oral Maxillofac. Surg. 2014; 43: 142–146. # 2013 International Association of Oral and Maxillofacial Surgeons. Published by Elsevier Ltd. All rights reserved. Abstract. Squamous cell carcinomas (SCCs) of the skin of the scalp have the potential for regional metastases. Microscopically, clearance may be less than the optimal dimensions. We report 101 SCCs of the scalp treated surgically under the care of a single oral and maxillofacial surgeon. Forty-two of the study patients had deep margins that were clear by less than 2 mm, of whom five had margins that involved pericranium skull. Our study demonstrated a local recurrence rate of 6% and a regional recurrence rate of 7%. All patients presented with relapse of the disease within 18 months of primary surgery. The evidence presented in this study suggests that in SCCs of the scalp, less than ideal surgical margin clearance, entirely due to anatomical restrictions, does not appear to substantially affect regional recurrence, but increases the risk of local recurrence.
Non-melanoma skin cancer is the most common cancer worldwide and its incidence has continued to rise over the decades.1 Ninety percent of cutaneous malignancies occur in the head and neck region,2 secondary to the lifetime accumulation of ultraviolet radiation damage3 in conjunction with skin type. It is approximated that between 10% and 20% of these malignancies are squamous cell carcinomas (SCCs).4 0901-5027/020142 + 05 $36.00/0
SCC has the potential for regional metastases, although early surgical management reduces this risk to around 5%.5 It has been recognized in the literature that particular sites of the head and neck represent a so-called ‘danger-area’ for increased risk of recurrence and metastases.2,4,6 In a recent multicentre study in Australia documenting the patterns of nodal metastases in head and neck patients diagnosed with cutaneous SCC, the scalp
Ke y w o r d s : c u t a n e o u s s q u a m o u s c e l l carcinoma; scalp; recurrence rates. Accepted for publication 29 August 2013 Available online 13 October 2013
represented the primary in the order of 10%.7 Anatomically the scalp is the cutaneous covering of the cranial vault, extending from the external occipital protuberance and superior nuchal lines to the supraorbital margins.8 The scalp has five anatomical layers that are of finite thickness, which show individual variation. However there can be some confusion with the term forehead, which encompasses the area
# 2013 International Association of Oral and Maxillofacial Surgeons. Published by Elsevier Ltd. All rights reserved.
Surgical excision of scalp SCCs marked by the hairline superiorly to the supraorbital ridges inferiorly and bound laterally by the temporal ridge.9 The recommended clinical margins for the excision of a cutaneous SCC are 4 mm for a ‘low-risk’ SCC and 6 mm for a ‘highrisk’ SCC in order to achieve a 95% histological clearance rate (there are no guidelines in millimetres for histological clearance).10,11 These distances, and greater, are usually easily achieved clinically at the peripheral margins of scalp lesions, but deep clearance is restricted by the anatomical thickness of the scalp. The purpose of this study was to address whether narrow (0.1–1.9 mm) clearance at the deep surgical margin, as measured histologically, results in a rate of local or regional recurrence above that stated in the literature, and when compared to groups with greater (2–6 mm and >6 mm) clearance at the deep surgical margin. Patients and methods
Patients recruited into the study were those treated in the maxillofacial department of the hospital. The estimated population covered by this hospital is 700,000. Data were recorded retrospectively. Ethical approval for this study was received from the hospital clinical audit department, set in the context of service evaluation. The inclusion criteria were set as follows: (1) treatment under the care of a single oral and maxillofacial surgeon in the department (MRT). (2) Patients treated between the years 2005 and 2009. This enabled appropriate follow-up in accordance with National Institute for Health and Clinical Excellence (NICE) guidelines,12 namely 6 months or less formal follow-up for ‘low-risk’ SCCs and locally agreed follow-up for ‘high-risk’ SCCs. (3) SCCs of the scalp, not including the forehead, as indicated by the anatomical description above. (4) SCCs treated primarily by surgical excision. At the study institution, cutaneous malignancies are subject to standard light microscopy histopathological preparation, namely fixation, preparation, embedding, sectioning, and finally appropriate staining. All cutaneous SCCs are discussed at a skin multi-disciplinary team (MDT) meeting. During this time-frame, 101 consecutive SCCs of the scalp were surgically removed under the care of the one oral and maxillofacial surgeon. Histopathology reports were reviewed looking specifically at the size of the lesion, differentiation of the neoplasm, and distance to the closest deep margin. Clinical
notes were appraised, verifying subsequent management, paying particular attention to local and regional recurrence. Histopathological data sets were compliant with the cancer data standard. Descriptive data were analysed using SPSS version 20 (IBM Corp., Armonk, NY, USA) and Microsoft Excel (Microsoft, Seattle, WA, USA). Results Patient demographics
Patient demographics are shown in Table 1; these fall roughly in line with the expected distribution. The mean age of the study participants was 81.7 years.
143
Table 2. Histological differential of tumours. Histological differentiation
N
Poorly differentiated Moderately differentiated Well differentiated
25 53 23
therapy; this group was not relevant to this study. We were therefore left with the main groups: 37 patients with histological marginal clearance of less than 2 mm and 39 patients with a marginal clearance of 2–6 mm, which when combined gave a group of 76 patients with marginal clearance of less than 6 mm. The last group of 20 patients had deep margin clearance greater than 6 mm; no patients in this group developed either local or regional recurrence.
Characteristics of the primary lesion
The majority of scalp SCCs treated measured between 10 mm and 50 mm in both width (56%) and length (52%). In terms of the depth of the tumour, the majority of lesions measured were less than 10 mm (59%). There was a broad range of differentiations reported on histology (Table 2). Surgical treatment – deep margin clearance
Figure 1 demonstrates the deep marginal clearance from the invasive edge of the carcinoma, broken down into groups. The standard surgical practice in this unit is resection at the deepest aspect of the lax areolar layer, i.e. on the pericranium, leaving only a very thin layer of the latter. A small number of patients for whom flap repair was planned had the pericranium removed, but as this is histologically only equivalent to 0.1 mm thick its impact is minimal. Five patients had full thickness SCCs involving the pericranium bone treated by excision including the outer table of the skull and appropriate flap repair. We expected these patients to be at higher risk and hence their cases were discussed at the MDT for consideration of adjuvant
Disease relapse – local recurrence
Figure 2 demonstrates local recurrence in the cohort. In the deep marginal clearance group of 2 mm, three patients developed local recurrence. No patients in the 2– 6 mm group developed local recurrence. The overall local recurrence rate in this study was 6%, including those involving the skull. None of the cohort had positive radial margins. However, removal of the cohort with involved pericranium or skull resulted in an overall local recurrence rate of 3% for those patients with clear histological soft tissue margins. The absolute risk of developing local recurrence with a deep margin of 2 mm with non-involved margins was 8%. Both these figures coincide with the current literature. Disease relapse – regional recurrence
Sex
Number
When reviewing regional recurrence (Fig. 3), some difference was noted. Seven patients developed regional recurrence, two patients in the 2 mm group and five patients in the 2–6 mm group. This gave an overall regional recurrence rate of 7%, coinciding with the current literature. The relative risk values of the two groups, 2 mm and >2 mm, demonstrated deep marginal clearance not to be a key factor in regional recurrence (Table 3).
Male Female Patient age ranges, years 61–65 66–70 71–75 76–80 81–85 86–90 91–95
79 22
Discussion
2 4 19 22 29 15 10
A cutaneous SCC has the potential for invasive growth, metastasis, and mortality. The risk factors for the development of a cutaneous SCC are well documented in the literature and include, but are not limited to, ultraviolet radiation, fair skin, phototherapy, ionizing radiation, chemical
Table 1. Patient demographics.
144
Jenkins et al.
Deep Margin Clearance Histologically determined clearance
20
of depth margin 6mm
39 2mm 37 Involving
Pericranium
5 Cranium
Fig. 1. Deep margin clearance from the invasive edge of the carcinoma.
carcinogens, immunosuppression, and inflammatory skin disorders.13 Figure 4 illustrates a high-risk SCC that required not only removal of the pericranium but also the outer table of the skull, necessitating flap repair. Figure 5 illustrates a conundrum. It still allows resection of the pericranium facilitating repair with a graft or flap, but anatomical restrictions mean the deep margin will be quite small. The purpose of this study was to ask the question whether reduced soft tissue clearance at the deep margin increases recurrence rates, comparing our long-term follow-up results to the current literature, and between the two chosen main groups
in the study: 2 mm and 2–6 mm deep histological clearance. If there is an increase in recurrence rates, should we be considering modifications to the current standard management of local surgical repair and monitoring as per NICE guidelines? The rates of loco-regional recurrence vary throughout the literature. Surgical departments that act as tertiary referral centres for cutaneous SCCs are likely to see higher rates when compared to dermatology centres. The general inference from the literature is that the local recurrence of SCCs ranges from 3% to 16%.2,3,14 Metastatic rates are reported at 1% to 4% for a ‘low-risk’ cutaneous SCC lesion.2 Scalp
Local Recurrence Histologically determined clearance
20
of depth margin 6mm
39 2mm 37 (3) Involving
Pericranium
5 (3)
( ) Local recurrence
Cranium
Fig. 2. Local recurrence corresponding to deep marginal clearance.
SCCs, however, showed a metastatic rate of around 10%.15 A prospective audit examining the prognostic factors for possible local or regional recurrence found that tumour size and thickness, patient immunosuppression, and localization at the ear were independent parameters determining the risk of metastasis in cutaneous SCC. Tumour thickness and grade affected the risk of local recurrence.3,15,16 A study reported by Baker et al.,17 with a study population of 227 cutaneous SCCs of which 20% (45 patients) were scalp SCCs, documented a local recurrence rate of 4%. However the most relevant aspect of this article was that the scalp represented 69% of the SCCs that were incompletely excised (16 of 227) and the deep margin was involved in all but one of the cases. Of the 11 cases not offered further treatment, only three went on to develop a recurrence. In our study, three out of five cases with involved skull at the time of surgery went on to develop local recurrence; these patients were subsequently offered radiotherapy. Though secondary treatment consists predominantly of radiotherapy, there are protagonists of more radical therapy, namely craniectomy and free tissue transfer.18 Although mentioned, this group was excluded from the current study as there was no soft tissue clearance. In the study groups, three cases developed local recurrence despite histologically clear margins, and all were in the 2 mm group. All patients presented with relapse of the disease within 18 months of primary surgery. Management of these patients consisted of further surgery and the offer of radiotherapy. The absolute risk demonstrated an increased risk of local recurrence with deep marginal clearance of 2 mm. Our study demonstrated a metastatic rate of 7%, consistent with the current literature. Again all patients presented with relapse of the disease within 18 months of primary surgery. The relative risk demonstrated deep marginal clearance not to be a key factor in regional recurrence, thus reinforcing the conclusions of previous studies that other factors probably play a more significant part in determining the risk of developing regional recurrence. As authors we accept that there are limitations to this study, particularly with reference to confounding factors when analysing risk factors for local and regional recurrence, e.g. tumour depth and differentiation. Despite the high number of patients recruited into this study, the
Surgical excision of scalp SCCs Table 3. Regional recurrence – deep margin (not including five patients with involved deep margin). Regional recurrence – deep margin
2 mm
>2 mm
Total
Yes No Relative risk
2 35 0.47
5 54 0.44
7 89
relatively low numbers who presented with recurrence make allowances for those confounding factors difficult. Continuation of the study with recruitment of patients treated from 2009 onwards, with appropriate time for follow-up, is in progress; this will target these concerns, allowing for a multivariate analysis. Additionally we plan to assess whether there is a statistical difference within the narrow clearance banding, i.e. between 1 mm clearance and 1–2 mm clearance. The scalp is one of the largest areas of sun-exposed skin, but is a relatively uncommon site for the development of metastatic SCC.5 Other ‘high-risk’ areas (ear and cheek – both expected to have similar exposure to ultraviolet radiation) have demonstrated a metastatic rate of around 20%.7 The following has been postulated: (1) the scalp is described as a unique part of the skin whose anatomy influences the behaviour of its primary neoplasms in a vital way.19 Its distinct layers, but mainly the aponeurosis, pericranium, and bony calvarium, show increased resistance to infiltration of the neoplastic cells. It is this innate resistance to infiltration that predisposes to lateral spread of the neoplastic cells, and hence an increased number of larger diameter lesions.20 (2) A patient’s hair may play a protective role in the prevention of a scalp SCC, and explains why cutaneous SCC is uncommonly found in the hair-bearing area.5 This also provides a probable explanation for the higher incidence of scalp SCCs in males than in females, as demonstrated in this study and others.4 (3) The ‘metastatic basin’ of the head and neck has been described extensively in the literature for lymphatic drainage to the parotid gland.21 The anatomical configuration of the lymphatic channels of the ear and cheek in comparison to the scalp, may explain the higher metastatic rate from these locations. All seven of the patients who developed a regional recurrence presented with enlargement of a parotid lymph node. All had deep margin clearance of the primary lesion, with two patients having clearance of 2 mm and the remaining five with
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Regional Recurrence Histologically determined clearance
20
of depth margin 6mm
39 (5) 2mm 37 (3) (2) Involving
Pericranium
5 (3)
( ) Local recurrence
Cranium
( ) Regional recurrence Fig. 3. Regional recurrence corresponding to deep marginal clearance.
Fig. 4. SCC of the scalp requiring removal of the outer table of the skull.
Fig. 5. Intact pericranium following removal of the SCC.
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clearance between 2 and 6 mm. Six patients were offered surgery and subsequent radiotherapy, and one patient palliative radiotherapy only. The literature defends the use of adjuvant radiotherapy and surgery for operable metastatic cutaneous SCC.22 As supported in the literature,23 treatment of nodal metastases has a grave outcome and 43% died of the disease. In conclusion, all SCCs of the scalp need to be treated effectively because of the inherent risk involved. The aim of surgery remains identical to that of any cutaneous SCC, i.e. to excise with clear histological margins. The evidence presented in this study suggests that in SCCs of the scalp, less than ideal surgical margin clearance, entirely due to anatomical restrictions, does not appear to substantially affect regional recurrence, but increases the risk of local recurrence. However, the current treatment regime remains appropriate and there is no indication for more aggressive treatment unless other significant high-risk factors are present. In light of the local recurrence risk of 8% in the 2 mm group, but not involving bone, we would suggest patients be fully informed and appropriate agreed follow-up arranged. Funding
None. Competing interests
None declared. Ethical approval
Hospital clinical audit department. References 1. Gray DT, Suman VJ, Su WP, Clay RP, Harmsen WS, Roenigk RK. Trends in the population-based incidence of squamous cell carcinoma of the skin first diagnosed between 1984 and 1992. Arch Dermatol 1997;133:735–40.
2. Rowe DE, Carroll RJ, Day Jr CL. Prognostic factors for local recurrence, metastasis, and survival rates in squamous cell carcinoma of the skin, ear, and lip. Implications for treatment modality selection. J Am Acad Dermatol 1992;26:976–90. 3. Brantsch KD, Meisner C, Schonfisch B, Trilling B, Wehner-Caroli J, Rocken M, et al. Analysis of risk factors determining prognosis of cutaneous squamous-cell carcinoma: a prospective study. Lancet Oncol 2008;9:713–20. 4. Ang P, Tan AW, Goh CL. Comparison of completely versus incompletely excised cutaneous squamous cell carcinomas. Ann Acad Med Singapore 2004;33:68–70. 5. Howle JR, Morgan GJ, Kalnins I, Palme CE, Veness MJ. Metastatic cutaneous squamous cell carcinoma of the scalp. ANZ J Surg 2008;78:449–53. 6. Miller SJ, Moresi JM. Actinic keratosis, basal cell carcinoma and squamous cell carcinoma. In: Bolognia JL, Jorizzo JL, Rapini RP, editors. Dermatology. London: Mosby; 2003. p. 1677–96. 7. Vauterin TJ, Veness MJ, Morgan GJ, Poulsen MG, O’Brien C. Patterns of lymph node spread of cutaneous squamous cell carcinoma of the head and neck. Head Neck 2006;28:785–91. 8. Agur AM, Lee MJ, Grant JC. Grant’s atlas of anatomy. 9th ed. Baltimore, MD: Lippincott Williams & Wilkins; 1991: 464. 9. Knize DM, Drisko M. The forehead and temporal fossa: anatomy and technique. Philadelphia, PA: Lippincott Williams & Wilkins; 2001: 3–11. 10. Brodland DG, Zitelli JA. Surgical margins for excision of primary cutaneous squamous cell carcinoma. J Am Acad Dermatol 1992;27:241–8. 11. Motley RJ, Preston PW, Lawrence CM. Multi-professional guidelines for the management of the patient with primary cutaneous squamous cell carcinoma. London, UK: British Association of Dermatologists; 2009. 12. National Institute for Health and Clinical Excellence. Improving outcomes for people with skin tumours including melanoma. The manual. N0957. London, UK: NICE; 2006. 13. Alam M, Ratner D. Cutaneous squamous cell carcinoma. N Engl J Med 2001;344:975–83.
14. Leibovitch I, Huilgol SC, Selva D, Hill D, Richards S, Paver R. Cutaneous squamous cell carcinoma treated with Mohs micrographic surgery in Australia. Experience over 10 years. J Am Acad Dermatol 2005;53:253–60. 15. Clayman GL, Lee JJ, Holsinger FC, Zhou X, Duvic M, El-Naggar AK, et al. Mortality risk from squamous cell skin cancer. J Clin Oncol 2005;23:759–65. 16. Ch’ng S, Clark JR, Brunner M, Palme CE, Morgan GJ, Veness MJ. Relevance of the primary lesion in the prognosis of metastatic cutaneous squamous cell carcinoma. Head Neck 2013;35:190–4. 17. Baker NJ, Webb AA, Macpherson D. Surgical management of cutaneous squamous cell carcinoma of the head and neck. Br J Oral Maxillofac Surg 2001;39:87–90. 18. Abo Sedira M, Amin AA, Rifaat MA. Locally advanced tumours of the scalp: the Egyptian National Cancer Institute experience. J Egypt Natl Canc Inst 2006;18:250–7. 19. Ratzer ER, Strong EW. Squamous cell carcinoma of the scalp. Am J Surg 1967;114: 67–76. 20. Mohs FE, Zitelli JA. Microscopically controlled surgery in the treatment of carcinoma of the scalp. Arch Dermatol 1981;117: 764–9. 21. O’Brien CJ. The parotid gland as a metastatic basin for cutaneous cancer. Arch Otolaryngol Head Neck Surg 2005;131: 551–5. 22. Veness MJ, Porceddu S, Palme CE, Morgan GJ. Cutaneous head and neck squamous cell carcinoma metastatic to parotid and cervical lymph nodes. Head Neck 2007;29: 621–31. 23. Lang PG, Martin MS, Kwatra R. Aggressive squamous cell carcinoma of the scalp. Dermatol Surg 2006;142:755–8.
Address: Glyndwr W. Jenkins Department of Oral and Maxillofacial Surgery York Teaching Hospital Wigginton Road York YO31 8HE UK Tel.: +44 07941 537245 E-mail: [email protected]