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British Journal of Oral and Maxillofacial Surgery xxx (2012) xxxxxx

De-escalation of surgery for early oral cancer is it oncologically safe?

Conor P. Barry a, , Chetan Katre b , Elena Papa c , James S. Brown a , Richard J. Shaw a,d , Fazilet Bekiroglu a , Derek Lowe a , Simon N. Rogers a,e
a

Regional Maxillofacial Unit, University Hospital Aintree, Liverpool L9 7LN, UK Maxillofacial Unit, North Manchester General Hospital, Manchester M85RB, UK c Maxillofacial Unit, University Hospital Evagelismos, Athens, Greece d Department of Surgery and Oncology, School of Cancer Studies, University of Liverpool, Liverpool, UK e Evidence-Based Practice Research Centre (EPRC), Faculty of Health, Edge Hill University, St Helens Road, Ormskirk L39 4QP, UK
b

Accepted 24 February 2012

Abstract This study is a review of practice for patients with T1 or T2 squamous cell carcinoma (SCC) of the anterior tongue and oor of the mouth who presented to the regional maxillofacial unit in Liverpool between 1992 and 2007. We examined trends in management and analysed their effects on resection margins, recurrence, and survival. The Liverpool head and neck oncology database was used to identify patients, and to retrieve their clinical, surgical, and pathological data. When data were missing the case notes and pathology records were reviewed. Follow up was taken to January 2011. A total of 382 patients were included. Despite more conservative treatment with closer resection margins (27% in 19921995 and 60% in 20042007), fewer free aps (79% in 19921995 and 38% in 20042007), and less adjuvant radiotherapy (37% in 19921995 and 22% in 20042007), there has been no signicant increase in local recurrence (14% in 19921996 and 8% in 20042007), and overall survival has not been adversely affected. This is most striking when T1 tumours are considered in isolation with a consistent trend towards fewer clear margins (95% in 19921995 and 28% in 20042007) and fewer free aps (53% in 19921995 and 11% in 20042007). The case mix was similar over the study period. These data support a more conservative approach to the management of early oral cancer. 2012 Published by Elsevier Ltd on behalf of The British Association of Oral and Maxillofacial Surgeons.
Keywords: Survival; Recurrence; Pathological margins; Mouth neoplasm; Surgery; Radiotherapy; Oral cancer; Free ap

Introduction The principal management for oral squamous cell carcinoma (SCC) with curative intent is radical primary operation, which aims to remove the entire tumour with resection margins

Corresponding author at: Regional Maxillofacial Unit, University Hospital Aintree, Liverpool L9 7LN, UK. Tel.: +44 151 529 5287; fax: +44 151 529 5288. E-mail addresses: conorbarry1@gmail.com (C.P. Barry), ckatre@doctors.org.uk (C. Katre), pappaelena@hotmail.com (E. Papa), brownjs@doctors.org.uk (J.S. Brown), Richard.Shaw@liverpool.ac.uk (R.J. Shaw), fbekiroglu@doctors.org.uk (F. Bekiroglu), astraglobeltd@btconnect.com (D. Lowe), snrogers@doctors.co.uk (S.N. Rogers).

of 1.5 cm of normal tissue. This is followed by reconstruction using free tissue transfer where indicated to promote the most functional outcome. Selective neck dissection is done when invasion is estimated to exceed 4 mm in depth or to provide access to vessels in the neck to facilitate reconstruction. Prescription for adjuvant radiotherapy is based on the histopathological ndings of the resection specimen. Various predictors of locoregional recurrence and survival have been described,13 and the adverse prognostic implications of compromised resection margins for local recurrence and survival have been well documented.35 Published data from this unit suggest that local recurrence could be doubled if the margin is close (15 mm),3 but this is for all stages of oral cancer and not just for T1 and T2. Some recent evidence has called into question what constitutes a safe margin.69

0266-4356/$ see front matter 2012 Published by Elsevier Ltd on behalf of The British Association of Oral and Maxillofacial Surgeons.

doi:10.1016/j.bjoms.2012.02.014

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Table 1 Patients characteristics at presentation. Data are number (%) unless otherwise stated. All patients with T1 or T2 tumours Clinical T1 T2 Sex Male Mean (SD) age (years) Tumour site Tongue (anterior 2/3) Floor of mouth Clinical N+ Patients with T1 tumours Sex Male Mean (SD) age (years) Tumour site Tongue (anterior 2/3) Floor of mouth Clinical N+ Patients with T2 tumours Sex Male Mean (SD) age (years) Tumour site Tongue (anterior 2/3) Floor of mouth Clinical N+

19921995 (n = 63) 19 (30) 44 (70) 40 (63) 58 (11) 32 (51) 31 (49) 12 (19) (n = 19) 11 (58) 61 (10) 9 (47) 10 (53) 1 (5) (n = 44) 29 (66) 56 (11) 23 (52) 21 (48) 11 (25)

19961999 (n = 89) 39 (44) 50 (56) 59 (66) 61 (13) 46 (52) 43 (48) 12 (13) (n = 39) 25 (64) 60 (13) 20 (51) 19 (49) 1 (3) (n = 50) 34 (68) 62 (13) 26 (52) 24 (48) 11 (22)

20002003 (n = 99) 50 (51) 49 (49) 63 (64) 62 (13) 53 (54) 46 (46) 21 (21) (n = 50) 30 (60) 63 (14) 29 (58) 21 (42) 4 (8) (n = 49) 33 (67) 60 (12) 24 (49) 25 (51) 17 (35)

20042007 (n = 131) 65 (50) 66 (50) 82 (63) 62 (13) 82 (63) 49 (37) 25 (19) (n = 65) 33 (51) 61 (13) 44 (68) 21 (32) 5 (8) (n = 66) 49 (74) 61 (13) 38 (58) 28 (42) 20 (30)

P-value*

0.05

0.96 0.28 0.27 0.57

0.57 0.77 0.25 0.71

0.77 0.15 0.83 0.51

Chi-square test between the four time periods apart from one-way ANOVA for age.

There is however consensus about the prognostic importance of extracapsular spread (ECS) in cervical lymph nodes, which has been shown to double the chances of local recurrence and distant metastasis, and triple the chances of regional recurrence.10 While cure and survival are of primary concern to the patient and the surgeon, radical surgery causes serious morbidity. Free aps are necessary for the reconstruction of large and composite defects, and they have enabled large oral tumours to be resected adequately without destructive functional and aesthetic morbidity. However, for early stage oral SCC, free tissue transfer can be associated with poorer functional outcome11 and health-related quality of life12,13 than if primary closure, local aps, or healing by secondary intention were possible. Also, operations that last a day, admission to the ITU, and prolonged hospital stay, are a large burden on the healthcare budget.14,15 There is a clinical impression in our unit that we have adopted a more conservative approach to primary surgery for early oral SCC of the anterior tongue and oor of the mouth (smaller resections, and fewer free aps and neck dissections). We aimed to examine this trend and to analyse the

effects of a de-escalation of primary surgery on recurrence, need for adjuvant radiotherapy, and survival.

Patients and methods Since 1992 all patients diagnosed with head and neck cancer at the regional maxillofacial unit, University Hospital, Aintree, have had their details entered on to a computerised head and neck database. We used the database to identify patients with clinically staged T1 and T2 primary SCC of the anterior tongue and oor of the mouth who presented to the unit between January 1992 and December 2007. Clinical, surgical, and pathological details, and data on recurrence relating to the primary tumour were retrieved from the database, and case notes and pathology records were reviewed for missing data. Mortality was tracked through the Ofce for National Statistics (ONS) to 1 January 2011. We divided the 16-year period (19922007) into 4-year periods to consider temporal trend. Results are presented and interpreted primarily for all early tumours combined, but the tables are split so that results for T1 and T2 stages can be

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Table 2 Treatment and neck dissection. Data are number (%). All patients with early T1 or T2 tumours Operation alone Operation and adjuvant radiotherapy No free ap Soft ap Composite ap No neck dissection Neck dissection Patients with T1 tumours Operation alone Operation and adjuvant radiotherapy No free ap Soft ap Composite ap No neck dissection Neck dissection Patients with T2 tumours Operation alone Operation and adjuvant radiotherapy No free ap Soft ap Composite ap No neck dissection Neck dissection

19921995 (n = 63) 40 (63) 23 (37) 13 (21) 45 (71) 5 (8) 11 (17) 52 (83) (n = 19) 16 (84) 3 (16) 9 (47) 9 (47) 1 (5) 8 (42) 11 (58) (n = 44) 24 (55) 20 (45) 4 (9) 36 (82) 4 (9) 3 (7) 41 (93)

19961999 (n = 89) 67 (75) 22 (25) 32 (36) 54 (61) 3 (3) 24 (27) 65 (73) (n = 39) 35 (90) 4 (10) 29 (74) 10 (26) 0 22 (56) 17 (44) (n = 50) 32 (64) 18 (36) 3 (6) 44 (88) 3 (6) 2 (4) 48 (96)

20002003 (n = 99) 75 (76) 24 (24) 53 (54) 42 (42) 4 (4) 36 (36) 63 (64) (n = 50) 48 (96) 2 (4) 40 (80) 9 (18) 1 (2) 31 (62) 19 (38) (n = 49) 27 (55) 22 (45) 13 (27) 33 (67) 3 (6) 5 (10) 44 (90)

20042007 (n = 131) 102 (78) 29 (22) 81 (62) 48 (37) 2 (2) 42 (32) 89 (68) (n = 65) 59 (91) 6 (9) 58 (89) 7 (11) 0 34 (52) 31 (48) (n = 66) 43 (65) 23 (35) 23 (35) 41 (62) 2 (3) 8 (12) 58 (88)

P-value* 0.18

<0.001 0.06

0.43

0.006 0.48

0.55

0.002 0.44

Chi-square test between the four time periods.

seen separately. Differences in the demographic and clinical characteristics of patients, and recurrence between the time periods (Tables 14) were tested using the chi square test. KaplanMeier methods were used to describe, and the log-rank test was used to compare, survival. Cox-regression multivariable modelling was used to extract a parsimonious set of independent predictors of all-cause survival.

Rates of local or regional recurrence, or both, were 24%, 8%, 15%, and 18%, respectively, over the four periods (p = 0.06) (Table 4), but the trend was less strong during the last three periods (p = 0.12), and it was broadly similar to 1996 for patients with T1 and T2 tumours. All-causes survival varied signicantly by period (p = 0.001) (Fig. 1), but the

Results A total of 382 patients with at least 36 months follow-up were included. Mean (SD) age was 61 (13) years and there was no signicant difference between the four time periods (range 58-61 in mean age, one way ANOVA p = 0.28). There were no other notable differences over time in regard to baseline characteristics of the patients (Table 1), but there was a suggestion that those in the 19921995 and 20042007 groups had slightly more advanced disease and more positive nodes, ECS, and p-stage 34 disease than those from 1996 to 2003. Over time, patients were treated less aggressively at the primary site with fewer free aps (7938%, Table 2) and more close margins (2760%, Table 3). The trend is even more striking when T1 tumours are considered in isolation (Table 3). There was no increase in the use of radiotherapy to compensate for the more conservative surgical approach (Table 2).

Fig. 1. KaplanMeier survival curves by time period when patients presented.

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Table 3 Histological results. Data are number (%). All patients with T1 or T2 tumours Tumour differentiation Poor Moderate Well Margins Clear Close Involved Positive nodes Extracapsular spread P-stage 3/4 Patients with T1 tumours Tumour differentiation Poor Moderate Well Margins Clear Close Involved Positive nodes Extracapsular spread P-stage 3/4 Patients with T2 tumours Tumour differentiation Poor Moderate Well Margins Clear Close Involved Positive nodes Extracapsular spread P-stage 3/4

19921995 (n = 63) 7 (11) 36 (57) 20 (32) 40 (63) 17 (27) 6 (10) 26 (41) 15 (24) 31 (49) (n = 19) 1 (5) 11 (58) 7 (37) 18 (95) 1 (5) 0 3 (16) 2 (11) 3 (16) (n = 44) 6 (14) 25 (57) 13 (30) 22 (50) 16 (36) 6 (14) 23 (52) 13 (30) 28 (64)

19961999 (n = 89) 6/86 (7) 51/86 (59) 29/86 (34) 54 (61) 24 (27) 11 (12) 22 (25) 8 (9) 26 (29) (n = 39) 1/36 (3) 19/36 (53) 16/36 (44) 26 (67) 11 (28) 2 (5) 4 (10) 0 4 (10) (n = 50) 5 (10) 32 (64) 13 (26) 28 (56) 13 (26) 9 (18) 18 (36) 8 (16) 22 (44)

20002003 (n = 99) 2/86 (2) 52/86 (60) 32/86 (37) 41/96 (43) 50/96 (52) 5/96 (5) 20/96 (21) 13/96 (14) 28 (29) (n = 50) 0/38 14/38 (37) 24/38 (63) 24/48 (50) 23/48 (48) 1/48 (2) 4 (8) 3 (6) 5 (10) (n = 49) 2/48 (4) 38/48 (79) 8/48 (17) 17/48 (35) 27/48 (56) 4/48 (8) 16/46 (35) 10/46 (22) 23 (47)

20042007 (n = 131) 4/113 (4) 66/113 (58) 43/113 (38) 35/124 (28) 74/124 (60) 15/124 (12) 38/124 (31) 25/124 (20) 46/129 (36) (n = 65) 1/54 (2) 30/54 (56) 23/54 (43) 17/60 (28) 36/60 (60) 7/60 (12) 9/63 (14) 5/63 (8) 10/63 (16) (n = 66) 3/59 (5) 36/59 (61) 20/59 (34) 18/64 (28) 38/64 (59) 8/64 (13) 29/61 (48) 20/61 (33) 36 (55)

P-value*

0.82**

<0.001

0.03 0.05 0.03

0.15**

<0.001

0.69 0.30 0.74

0.24**

0.009

0.23 0.19 0.23

Chi square test between the four time periods. Poor or moderate compared with well differentiated.

difference was not apparent (p = 0.45) when the rst period was omitted. However, overall survival for 20042007 was lower than for 19961999 and 20002003. Age, clinical T-stage, clinical N-stage, operation with or without radiotherapy, free-ap surgery, p-stage, positive nodes, and ECS were found to be predictors of poor survival. It was clear that by far the strongest single predictor was ECS (5-year survival 25%, SE 6%) and in stepwise Cox regression modelling (with entry at p < 0.01), ECS (p < 0.001) was selected rst, and age (p < 0.001) and then margins (p = 0.003) were selected as independent predictors. No other variables, including time period, were independent predictors of survival. One in six patients (61/372) had ECS and if they are omitted from analysis then the four survival curves for the four periods were not signicantly different (p = 0.97, Fig. 2). Survival was similar for 20002003 and 20042007, and

these seemed to be slightly better than for 19961999 and 19921995. Rates of local or regional recurrence, or both, for patients without ECS were 19% (9/48), 9% (7/81), 13% (11/83), and 13% (13/99), respectively, over the four periods (p = 0.43). Rates for T1 tumours were 0% (0/17), 8% (3/39), 15% (7/47), and 14% (8/58), respectively, and for T2 tumours were 29% (9/31), 10% (4/42), 11% (4/36), and 12% (5/41), respectively.

Discussion This detailed review of a specic group of patients with clinical T1 and T2 SCC of the oral tongue and oor of the mouth conrms the perceived clinical impression of a pattern of deescalation in terms of resection and free tissue transfer and

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Table 4 Recurrence. Data are number (%). All patients with early T1 or T2 tumours Local Regional Local or regional, or both Distant Patients with T1 tumours Local Regional Local or regional, or both Distant Patients with T2 tumours Local Regional Local or regional, or both Distant

1992995 (n = 63) 9 (14) 8 (13) 15 (24) 2 (3) (n = 19) 0 0 0 0 (n = 44) 9 (20) 8 (18) 15 (34) 2 (5)

1996999 (n = 89) 2 (2) 5 (6) 7 (8) 4 (4) (n = 39) 0 3 (8) 3 (8) 1 (3) (n = 50) 2 (4) 2 (4) 4 (8) 3 (6)

2000003 (n = 99) 5 (5) 10 (10) 15 (15) 5 (5) (n = 50) 4 (8) 3 (6) 7 (14) 1 (2) (n = 49) 1 (2) 7 (14) 8 (16) 4 (8)

2004007 (n = 131) 10 (8) 15 (11) 23 (18) 10 (8) (n = 65) 4 (6) 7 (11) 10 (15) 3 (5) (n = 66) 6 (9) 8 (12) 13 (20) 7 (11)

P value* 0.03 0.44 0.06 0.56

0.22 0.44 0.23 0.70

0.008 0.18 0.01 0.64

Chi square test between the four time periods.

shows that a more conservative approach to surgery for early oral cancer is safe oncologically. To our knowledge this is the largest series to date to look specically at outcomes in early stage disease. The ndings are strengthened by the consecutive nature and size of the group with detailed prospectively gathered histological and outcome data. We accept the limitations inherent in any retrospective analysis so data should be considered with caution. The inclusion criteria were based on clinical rather than pathological stage because clinical stage is available

Fig. 2. KaplanMeier survival curves by time period for patients without extracapsular spread.

to the surgeon when planning treatment. Inevitably, the pathological ndings will cause a proportion of patients to be upstaged. Disease seemed to be more severe in the 19921995 group with a higher percentage of T2 tumours (Table 1). There was also a higher incidence of ECS (Table 3), which was by far the strongest predictor of survival. The increased severity of disease may reect a change in referral pattern, as before the advent of the multidisciplinary team (Tumour Board) in 2003, many patients with early cancers were still being treated in local hospitals. It may also reect an improvement in the awareness of oral cancer, and faster referral.16 From 1996 to 2007, the three groups were similar in terms of age and severity of disease, although the 20042007 group had a second peak in incidence of ECS. Overall, we have found a denite trend towards a more conservative surgical approach with closer resection margins, fewer neck dissections, and fewer free aps (Table 2). The increase in close margins is associated with a reduction in clear margins, but the incidence of involved margins has remained constant at about 10%, which is within the reported range for resections of oral SCC.3,6,9 The de-escalation is most striking when T1 tumours are considered in isolation. This shift in treatment reects an increased awareness that while local control should not be compromised by inadequate resection, unnecessary functional morbidity caused by over resection should also be avoided. As expected, outcome for the 19921995 group in terms of recurrence and overall survival was poorer than for the other groups (Table 4; Fig. 1). Overall survival has improved over the study period. A slight dip in 20042007 may be accounted for by the increase in ECS in this group, but when we excluded ECS from the analysis, the trend reverted to a gradual improvement (Fig. 2). These results mirror improvements in survival already reported from this unit4 and others.17

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Histological ndings resulted in 13% of patients with T2 disease being upstaged to pT3 or pT4, and survival was similar to that previously reported for T3 and T4 oral SCC,2 which suggests that they were not disadvantaged by their initial understaging. Despite the increase in close margins, there has been no signicant increase in local recurrence in this study, and of note, there has been no increase in radiotherapy to compensate for less aggressive surgery. However, there was a slight upward trend in recurrence. While this may be partly accounted for by increased ECS, it also serves as a warning against treatment being too conservative. Our local recurrence rates compare well with those from other published series,68 but accurate comparison is difcult as few papers conne their results to T1 and T2 disease of the anterior tongue and oor of the mouth. There is a lack of consensus internationally as to what constitutes an adequate margin. The UK guidelines (which we follow) record the status of mucosal and deep margins, and designate margins of 5 mm or more as clear, 15 mm as close, and less than 1 mm as involved. The division between clear and close margins at 5 mm seems to be arbitrary. Nason et al.6 reported recurrence in patients with margins of 34 mm that was identical to those with margins of 5 mm or more. However, their data do not make clear the extent to which postoperative radiotherapy had confounded the results. Brandwein-Gensler et al.7 reported that status of resection margins was not an independent predictor of local recurrence in patients having similar treatments. Weijers et al.8 compared non-involved deep surgical margins of less than 5 mm with those of more than 5 mm and found no signicant difference in risk of local recurrence. However, Sutton et al.3 and Rogers et al.4 who both reported data from this unit, described a signicantly adverse prognostic outcome associated with close margins (15 mm). It is possible that the inclusion of patients with margins of 12 mm and those with margins of 35 mm has biased their results in this regard, and that re-examination of the data may show results that concur more closely with those of Nason et al.6 and Brandwein-Gensler et al.7 Al Rajhi et al.5 examined the signicance of resection margins specically for T1 or T2 disease of the anterior tongue and reported much lower recurrence-free survival for patients with margins of less than 5 mm, but this included tumours with involved margins. The slight reduction in the rate of neck dissections partly reects a lower demand for access to vessels in the neck for microvascular surgery. Our unit still advocates elective neck dissections for tumours that have invaded to an estimated depth of more than 4 mm18 and when the risk of nodal metastasis is thought to exceed 20%.19 In this group, 70% of patients (45% with T1 and 91% with T2) had neck dissection. The role of elective neck dissection remains controversial in this group and is being addressed by the SEND trial (the role of selective neck dissection used electively in patients with early oral squamous cell carcinoma and no clinical evidence of lymph node metastasis in the neck: NCT00571883).

However, the nding that 10% of patients with T1 or T2 tumours and a clinically N0 neck had ECS reinforces the fact that early stage disease can be aggressive, and emphasises the need for a reliable preoperative method to screen the neck. The avoidance of free aps where possible results in a better quality of life,12,13 and in better functional outcomes.11 The duration of operation and hospital stay,15 and consequently chances for postoperative medical complications in this population, many of whom are elderly, are greatly reduced with primary closure or local reconstruction. Not only is this benecial to the patient but it also reduces the burden on healthcare resources.14 Treatment in our unit for early SCC of the anterior tongue and oor of the mouth has shifted towards more conservative surgery with closer margins and fewer free aps. In selected cases, these tumours can be treated safely by wide local excision with smaller margins than has previously been thought. However, the slight increase in involved margins and recurrence, and the levelling of the survival curve for the 20042007 group may serve as a warning that we have reached the safe limits of de-escalation. Further work is required to quantify what is a safe resection margin, and to discover any improvement in function or quality of life that is associated with more conservative operations.

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12. Rogers SN, Scott J, Chakrabati A, Lowe D. The patients account of outcome following primary surgery for oral and oropharyngeal cancer using a quality of life questionnaire. Eur J Cancer Care (Engl) 2008;17:1828. 13. Rogers SN, Lowe D, Yueh B, Weymuller Jr EA. The physical function and social-emotion function subscales of the University of Washington Quality of Life Questionnaire. Arch Otolaryngol Head Neck Surg 2010;136:3527. 14. McCrory AL, Magnuson JS. Free tissue transfer versus pedicled ap in head and neck reconstruction. Laryngoscope 2002;112:21615. 15. Rogers SN, Lowe D, Brown JS, Vaughan ED. The relationship between length of stay and health-related quality of life in patients treated by

16. 17. 18.

19.

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