http://informahealthcare.com/jdt ISSN: 0954-6634 (print), 1471-1753 (electronic) J Dermatolog Treat, Early Online: 1–3 ! 2015 Informa UK Ltd. DOI: 10.3109/09546634.2015.1034083
ORIGINAL ARTICLE
Excision versus incision biopsy in the management of malignant melanoma* Kavita S. Sharma, Philip Lim, and Micheal T. Brotherston
J Dermatolog Treat Downloaded from informahealthcare.com by Nyu Medical Center on 07/13/15 For personal use only.
Plastic Surgery Department, Royal Hallamshire Hospital, Sheffield, UK
Abstract
Keywords
Introduction: The incidence of melanoma has increased over the last decade. The Breslow thickness is one of the most important histological parameters. The gold standard for histological diagnosis is an excision biopsy. Incisional, punch or shave biopsies are not recommended as they are often incomplete and can result in false negatives. Objective: To assess the validity of incision versus excision biopsies in the prediction of Breslow thickness in the histopathological analysis of malignant melanoma. Methods: A retrospective review of histopathological records was conducted for all patients undergoing incision biopsy for malignant melanoma. The Breslow thicknesses of the incisional biopsies were matched to the later corresponding excisional biopsies. The demographical data, site of melanoma and histological subtype were also examined. Results: Sixty patients between 1st January 2005 and 31st December 2013 were identified. The most common area biopsied was the upper and lower limbs – 50%. The Breslow thickness and Clark’s level were found to be significantly increased in excision versus incision biopsy specimens. Nine patients had differing mitotic rates which were all higher in the excision biopsy samples. Conclusion: Our data supports the UK national guidelines on the management of malignant melanoma in that incisional biopsies are not indicated in the diagnostic pathway of malignant melanoma.
Breslow thickness, excision biopsy, incision biopsy, malignant melanoma
Introduction The incidence of cutaneous melanoma is on the rise and this is set to continue in the coming years (1). Furthermore, it is becoming more evident that there has been a rapid increase in melanoma and its associated morbidity and mortality amongst the elderly population (465 years) (2). With an ageing population as that of the United Kingdom and many other developed countries, melanoma will undoubtedly become an increasingly important national health issue. The most important predictors of mortality according to the American Joint Committee on Cancer (AJCC) are tumor characteristics, such as Breslow thickness, ulceration, mitotic rate and the presence of metastases (3). Therefore, an accurate biopsy is crucial as an initial step in assessment. The current guidelines on the management of malignant melanoma in the United Kingdom set out a defined pathway to the clinician from screening and clinical assessment in primary care to follow-up after the completion of treatment (4). According to the current guidance, patients with a suspicious pigmented lesion should proceed to have an excision biopsy. The recommendation is for a 2 mm peripheral margin with a deep margin consisting of a rim of subcutaneous fat. This enables diagnosis, staging and determines the need for further investigations like computed topography scans.
History Received 19 March 2015 Accepted 22 March 2015 Published online 17 April 2015
Furthermore, the guidelines highlight that there is no role for using incision biopsy outside the recommendation of the multidisciplinary team, as they do not allow for complete histological staging. It is only acceptable for large lesions in cosmetically sensitive areas where clinical doubt exists about the diagnosis. This is not as pertinent in non-melanoma skin cancers as guidelines in these areas recommend the use of incision biopsy in these circumstances (5). With the increasing number of excisions of thin melanomas, dysplastic nevi and other pigmented lesions suspicious of melanoma this raises the question of whether the standard excisional biopsies can be replaced in some cases by incisional biopsies, which are easier to perform. Many studies have looked at patient mortality and recurrence as outcomes in those who have had excisional versus incisional biopsies. It is not surprising that many of these studies showed no significant difference. However, differences in the variability of histological data obtained by incisional versus excisional biopsies have not been thoroughly investigated. As a result, the aim of our study was to determine if the Breslow thickness, Clark’s level and mitotic rates in the histological assessment of malignant melanoma were significantly different in incision versus excision biopsy specimens from the same sample.
Methods *This paper was presented in the ESPRAS International Plastic Surgery Conference, Edinburgh, July 2014. Correspondence: Miss. K. Sharma, Plastic Surgery Department, Royal Hallamshire Hospital, Sheffield, Glossop Road, Sheffield, South Yorkshire S10 2JF, UK. E-mail: [email protected]
A retrospective review of pathology records was undertaken in a regional plastic surgery unit. The inclusion criteria consisted of pathological specimens with a diagnosis of invasive malignant melanoma where an incisional biopsy was performed.
2
K. S. Sharma et al.
J Dermatolog Treat, Early Online: 1–3
Incision biopsy was defined as a specimen obtained as part of, but not the entire suspected lesion. Other biopsies considered as part of the spectrum of incisional biopsy included punch and shave biopsies. Furthermore, in order to be included in the review each incisional biopsy sample had to have a matching excisional biopsy performed at a later date. The Breslow thickness, mitotic rates and Clark’s level were collected for the two samples and analyzed for significant differences. Other histological data collected included patient demographics, subtype of melanoma, mitotic rate and Clark’s level. Statistical analysis was performed using the sign test to determine if there was a significant difference in the two reported values of the Breslow thicknesses, Clark’s levels and mitotic rates between incision and excision biopsies.
J Dermatolog Treat Downloaded from informahealthcare.com by Nyu Medical Center on 07/13/15 For personal use only.
Results Sixty patients met the inclusion criteria between 1st January 2005 and 31st December 2013. The male to female ratio was 1:1 and the median age at diagnosis was 70.5 years (range 41–97 years). The most common sites in which an incision biopsy was undertaken included the upper and lower limbs (50%), head and neck region (38%) and trunk (12%). The most common histological subtypes found are illustrated in Figure 1. The mean Breslow thickness recorded for the incision biopsy specimens was 2.004 (s.d. ¼ 2.419). The corresponding value for the excision biopsy was 2.998 (s.d. ¼ 4.166). The sign test was 2.774 (p ¼ 0.0055) (Table 1). Forty-eight percent of the excisional biopsy specimens had a Clark’s level between II and III and 52% between IV and V. This was similar for the incision biopsy specimens as 50% had an average Clark’s level II–III and 50% between IV and V. Nine samples in our study had differing mitotic rates in the excision versus incision biopsy samples. The excision biopsy samples had in all cases a higher mitotic rate. Most of the incision biopsies were noted to be carried out in the primary care setting, with the referral being made when sample indicated a diagnosis of malignant melanoma (Figure 2).
Discussion In the past, the type of biopsy technique utilized in the initial diagnosis of malignant melanoma depended on the location and size of the pigmented lesion and the physician’s experience and judgment. However with the advent of more structured patient
pathways and national guidelines, these practices have been standardized and patient care in melanoma is centered on decisions made at the level of the multidisciplinary team. There has been concern that incision biopsy techniques lead to incomplete excision of the melanoma resulting in local, regional or systemic tumor dissemination. Punch biopsies have been postulated to increase the level of tumor invasion. A study by Griffiths et al. concluded that incisional biopsies resulted in an unacceptably high incidence of tumor distortion, which precluded measurement of maximal tumor thickness in almost one-third of cases. As a result it is to be regarded as an unacceptable procedure for skin lesions suspicious of malignant melanoma (6). This was later supported by Lees et al. In their cohort, 8.8% of patients were initially diagnosed with incision biopsy type technique and found that it rendered 40% of the lesions not fully assessable on the histopathological criteria needed for the reporting of melanomas at that time. This was significantly higher than the other techniques. They also concluded that suspicious lesions should be subjected to excision rather than incision biopsy techniques in order to avoid compromising histological assessment, as tumor thickness is a key prognostic factor in treatment and prognosis (7). It has been well established that tumor thickness is one of the most significant predictors of survival and therefore accurate, consistent determination of this is crucial in the management of malignant melanoma (8). There are practical advantages of performing incision biopsies to aid diagnosis. Firstly, it is less time consuming and technical, requiring less equipment and resources. This makes it ideal for it to be undertaken in between larger reconstructive cases. It is advantageous if the lesion turns out to be benign in a cosmetically sensitive area like the face or Table 1. Illustrating mean, standard deviation, median and range of Breslow thickness and Clark’s level in excision versus incision biopsies. Excision biopsy Breslow thickness (mm) Mean SD Median Range Clark’s level II–III IV–V
Incision biopsy
2.998 4.166 1.4 0.2–22
2.004 2.419 1 0.1–12
48% (25) 52% (27)
50% (26) 50% (26)
Sign. test
p Value
2.774
0.0055
5.824
50.0001
8% 10%
25%
20, 38% 6%
26, 50% 9% 17%
6, 12%
Extremity Trunk Head and Neck
Figure 1. Pie chart illustrating the site distribution of melanoma.
Superficial Spreading Lengo Maligna Nodular Lenginous Superficial spreading/lengo mixed Misc
25%
Figure 2. Pie chart illustrating pathological subtypes of melanoma.
Incisional biopsy in malignant melanoma
J Dermatolog Treat Downloaded from informahealthcare.com by Nyu Medical Center on 07/13/15 For personal use only.
DOI: 10.3109/09546634.2015.1034083
scalp region. Furthermore for larger indeterminate lesions, a tissue sample can be beneficial as it can allow planning and possibly wide excision and reconstruction in the same setting, which saves additional procedures. For the elderly or infirm or medically unfit this technique has proven to be quite useful as it is of a short duration using local anesthetic. Most published studies have focused on recurrence and survival after excisional versus incisional biopsies. Some of these studies hypothesized that tumor cells could be displaced deep to the deep dermis in the incisional biopsy specimens (9). Furthermore, it was postulated that due to the small amount of subcutaneous fat in the head and neck region, cutting into tumor in this region could seed cells directly into the blood vessels (10). On the other hand, some studies found no significant differences in survival between the two groups and these bore the recommendations of performing it in large lesions and those in cosmetically sensitive areas (6,7,11). In this study, we aimed to compare matched samples from the same specimen biopsied at two different points in time to determine if there was a difference in the Breslow thickness reported between the incision and excision biopsy samples. In addition, other prognostic indicators like Clark’s level and mitotic rates were also assessed. Our data show that there was a significant difference in these values between the incision and excision biopsy samples. The excision biopsy samples were of a greater Breslow thickness and Clark’s level compared to the initial incision biopsy counterpart. This suggests the validity of current recommendations however there are several points that can explain the observed differences. Firstly, the part of the specimen that is biopsied in the incision sample may not represent the true lesion. The darkest or ulcerated part of a pigmented lesion may not be the deepest area of invasion. Furthermore, there is a great deal of variability in technique, tissue handling and storage. As a result the tested sample may not be a true indication of the entire lesion. Given the degree of variability associated with this technique, the question of its usefulness comes into play. Ultimately histological data represented in this study show that there is a significant difference therefore treatment is ideally based on the standard excision biopsy sample unless the lesion has an exceptionally large surface area. In these situations multiple incision biopsies have a role as they can indicate a diagnosis. However for lesions in cosmetically sensitive areas, definitive treatment is ideal, not only for staging purposes but to offer the patient more definitive care. In these situations it may be beneficial to refer the patients to a plastic and reconstructive surgeon for the primary excision biopsy.
3
This study supports the recommendations made by Marsden et al. in not performing incisional biopsies in the initial management of malignant melanoma unless the case has been discussed and recommended at the level of the local or regional multidisciplinary team. The recommendation to perform an incision biopsy may be justified in very large, ulcerated lesions, which is not amenable to complete excision for an initial histological analysis.
Declaration of interest The authors report no conflicts of interest. The authors alone are responsible for the content and writing of this article.
References 1. de Vries E, van de Poll-Franse LV, Louwman WJ, et al. Predictions of skin cancer incidence in the Netherlands up to 2015. Br J Dermatol. 2005;152:481–8. 2. Gaudette LA, Gao RN. Changing trends in melanoma incidence and mortality. Health Rep. 1998;10:29–41. 3. Balch CM, Bunzaid AC, Soong SJ, et al. Final version of the American Joint Committee on Cancer staging system for cutaneous melanoma. J Clin Oncol. 2001;19:3635–48. 4. Marsden JR, Newton-Bishop JA, Burrows L, et al.; British Association of Dermatologists (BAD) Clinical Standards Unit. Revised UK guidelines for the management of cutaneous melanoma 2010. J Plast Reconstr Aesthet Surg. 2010;63:1401–19. 5. Telfer NR, Colver GB, Morton CA. Guidelines for the management of basal cell carcinoma. Br J Dermatol. 2008;159:35–48. 6. Griffiths R, Briggs JC. Biopsy procedures, primary wide excisional surgery and long term prognosis in primary clinical stage I invasive cutaneous malignant melanoma. Ann R Coll Surg Engl. 1985;67: 75–8. 7. Lees VC, Briggs JC. Effect of initial biopsy procedure on prognosis in Stage 1 invasive cutaneous malignant melanoma: review of 1086 patients. Br J Surg. 1991;78:1108–10. 8. Balch CM, Soong SJ, Gershenwald JE, et al. Prognostic factors analysis of 17,600 melanoma patients: validation of the American Joint Committee on Cancer melanoma staging system. J Clin Oncol. 2001;19:3622–34. 9. Epstein E, Bragg K, Linden G. Biopsy and prognosis of malignant melanoma. JAMA. 1969;208:1369–71. 10. Austin JR, Byers RM, Brown WD. Influence of biopsy on the prognosis of cutaneous melanoma of the head and neck. Head Neck. 1996;18:107–17. 11. Lederman JS, Sober AJ. Does biopsy type influence survival in clinical stage I cutaneous melanoma? J Am Acad Dermatol. 1985; 13:983–7.
ORIGINAL ARTICLE
Excision versus incision biopsy in the management of malignant melanoma* Kavita S. Sharma, Philip Lim, and Micheal T. Brotherston
J Dermatolog Treat Downloaded from informahealthcare.com by Nyu Medical Center on 07/13/15 For personal use only.
Plastic Surgery Department, Royal Hallamshire Hospital, Sheffield, UK
Abstract
Keywords
Introduction: The incidence of melanoma has increased over the last decade. The Breslow thickness is one of the most important histological parameters. The gold standard for histological diagnosis is an excision biopsy. Incisional, punch or shave biopsies are not recommended as they are often incomplete and can result in false negatives. Objective: To assess the validity of incision versus excision biopsies in the prediction of Breslow thickness in the histopathological analysis of malignant melanoma. Methods: A retrospective review of histopathological records was conducted for all patients undergoing incision biopsy for malignant melanoma. The Breslow thicknesses of the incisional biopsies were matched to the later corresponding excisional biopsies. The demographical data, site of melanoma and histological subtype were also examined. Results: Sixty patients between 1st January 2005 and 31st December 2013 were identified. The most common area biopsied was the upper and lower limbs – 50%. The Breslow thickness and Clark’s level were found to be significantly increased in excision versus incision biopsy specimens. Nine patients had differing mitotic rates which were all higher in the excision biopsy samples. Conclusion: Our data supports the UK national guidelines on the management of malignant melanoma in that incisional biopsies are not indicated in the diagnostic pathway of malignant melanoma.
Breslow thickness, excision biopsy, incision biopsy, malignant melanoma
Introduction The incidence of cutaneous melanoma is on the rise and this is set to continue in the coming years (1). Furthermore, it is becoming more evident that there has been a rapid increase in melanoma and its associated morbidity and mortality amongst the elderly population (465 years) (2). With an ageing population as that of the United Kingdom and many other developed countries, melanoma will undoubtedly become an increasingly important national health issue. The most important predictors of mortality according to the American Joint Committee on Cancer (AJCC) are tumor characteristics, such as Breslow thickness, ulceration, mitotic rate and the presence of metastases (3). Therefore, an accurate biopsy is crucial as an initial step in assessment. The current guidelines on the management of malignant melanoma in the United Kingdom set out a defined pathway to the clinician from screening and clinical assessment in primary care to follow-up after the completion of treatment (4). According to the current guidance, patients with a suspicious pigmented lesion should proceed to have an excision biopsy. The recommendation is for a 2 mm peripheral margin with a deep margin consisting of a rim of subcutaneous fat. This enables diagnosis, staging and determines the need for further investigations like computed topography scans.
History Received 19 March 2015 Accepted 22 March 2015 Published online 17 April 2015
Furthermore, the guidelines highlight that there is no role for using incision biopsy outside the recommendation of the multidisciplinary team, as they do not allow for complete histological staging. It is only acceptable for large lesions in cosmetically sensitive areas where clinical doubt exists about the diagnosis. This is not as pertinent in non-melanoma skin cancers as guidelines in these areas recommend the use of incision biopsy in these circumstances (5). With the increasing number of excisions of thin melanomas, dysplastic nevi and other pigmented lesions suspicious of melanoma this raises the question of whether the standard excisional biopsies can be replaced in some cases by incisional biopsies, which are easier to perform. Many studies have looked at patient mortality and recurrence as outcomes in those who have had excisional versus incisional biopsies. It is not surprising that many of these studies showed no significant difference. However, differences in the variability of histological data obtained by incisional versus excisional biopsies have not been thoroughly investigated. As a result, the aim of our study was to determine if the Breslow thickness, Clark’s level and mitotic rates in the histological assessment of malignant melanoma were significantly different in incision versus excision biopsy specimens from the same sample.
Methods *This paper was presented in the ESPRAS International Plastic Surgery Conference, Edinburgh, July 2014. Correspondence: Miss. K. Sharma, Plastic Surgery Department, Royal Hallamshire Hospital, Sheffield, Glossop Road, Sheffield, South Yorkshire S10 2JF, UK. E-mail: [email protected]
A retrospective review of pathology records was undertaken in a regional plastic surgery unit. The inclusion criteria consisted of pathological specimens with a diagnosis of invasive malignant melanoma where an incisional biopsy was performed.
2
K. S. Sharma et al.
J Dermatolog Treat, Early Online: 1–3
Incision biopsy was defined as a specimen obtained as part of, but not the entire suspected lesion. Other biopsies considered as part of the spectrum of incisional biopsy included punch and shave biopsies. Furthermore, in order to be included in the review each incisional biopsy sample had to have a matching excisional biopsy performed at a later date. The Breslow thickness, mitotic rates and Clark’s level were collected for the two samples and analyzed for significant differences. Other histological data collected included patient demographics, subtype of melanoma, mitotic rate and Clark’s level. Statistical analysis was performed using the sign test to determine if there was a significant difference in the two reported values of the Breslow thicknesses, Clark’s levels and mitotic rates between incision and excision biopsies.
J Dermatolog Treat Downloaded from informahealthcare.com by Nyu Medical Center on 07/13/15 For personal use only.
Results Sixty patients met the inclusion criteria between 1st January 2005 and 31st December 2013. The male to female ratio was 1:1 and the median age at diagnosis was 70.5 years (range 41–97 years). The most common sites in which an incision biopsy was undertaken included the upper and lower limbs (50%), head and neck region (38%) and trunk (12%). The most common histological subtypes found are illustrated in Figure 1. The mean Breslow thickness recorded for the incision biopsy specimens was 2.004 (s.d. ¼ 2.419). The corresponding value for the excision biopsy was 2.998 (s.d. ¼ 4.166). The sign test was 2.774 (p ¼ 0.0055) (Table 1). Forty-eight percent of the excisional biopsy specimens had a Clark’s level between II and III and 52% between IV and V. This was similar for the incision biopsy specimens as 50% had an average Clark’s level II–III and 50% between IV and V. Nine samples in our study had differing mitotic rates in the excision versus incision biopsy samples. The excision biopsy samples had in all cases a higher mitotic rate. Most of the incision biopsies were noted to be carried out in the primary care setting, with the referral being made when sample indicated a diagnosis of malignant melanoma (Figure 2).
Discussion In the past, the type of biopsy technique utilized in the initial diagnosis of malignant melanoma depended on the location and size of the pigmented lesion and the physician’s experience and judgment. However with the advent of more structured patient
pathways and national guidelines, these practices have been standardized and patient care in melanoma is centered on decisions made at the level of the multidisciplinary team. There has been concern that incision biopsy techniques lead to incomplete excision of the melanoma resulting in local, regional or systemic tumor dissemination. Punch biopsies have been postulated to increase the level of tumor invasion. A study by Griffiths et al. concluded that incisional biopsies resulted in an unacceptably high incidence of tumor distortion, which precluded measurement of maximal tumor thickness in almost one-third of cases. As a result it is to be regarded as an unacceptable procedure for skin lesions suspicious of malignant melanoma (6). This was later supported by Lees et al. In their cohort, 8.8% of patients were initially diagnosed with incision biopsy type technique and found that it rendered 40% of the lesions not fully assessable on the histopathological criteria needed for the reporting of melanomas at that time. This was significantly higher than the other techniques. They also concluded that suspicious lesions should be subjected to excision rather than incision biopsy techniques in order to avoid compromising histological assessment, as tumor thickness is a key prognostic factor in treatment and prognosis (7). It has been well established that tumor thickness is one of the most significant predictors of survival and therefore accurate, consistent determination of this is crucial in the management of malignant melanoma (8). There are practical advantages of performing incision biopsies to aid diagnosis. Firstly, it is less time consuming and technical, requiring less equipment and resources. This makes it ideal for it to be undertaken in between larger reconstructive cases. It is advantageous if the lesion turns out to be benign in a cosmetically sensitive area like the face or Table 1. Illustrating mean, standard deviation, median and range of Breslow thickness and Clark’s level in excision versus incision biopsies. Excision biopsy Breslow thickness (mm) Mean SD Median Range Clark’s level II–III IV–V
Incision biopsy
2.998 4.166 1.4 0.2–22
2.004 2.419 1 0.1–12
48% (25) 52% (27)
50% (26) 50% (26)
Sign. test
p Value
2.774
0.0055
5.824
50.0001
8% 10%
25%
20, 38% 6%
26, 50% 9% 17%
6, 12%
Extremity Trunk Head and Neck
Figure 1. Pie chart illustrating the site distribution of melanoma.
Superficial Spreading Lengo Maligna Nodular Lenginous Superficial spreading/lengo mixed Misc
25%
Figure 2. Pie chart illustrating pathological subtypes of melanoma.
Incisional biopsy in malignant melanoma
J Dermatolog Treat Downloaded from informahealthcare.com by Nyu Medical Center on 07/13/15 For personal use only.
DOI: 10.3109/09546634.2015.1034083
scalp region. Furthermore for larger indeterminate lesions, a tissue sample can be beneficial as it can allow planning and possibly wide excision and reconstruction in the same setting, which saves additional procedures. For the elderly or infirm or medically unfit this technique has proven to be quite useful as it is of a short duration using local anesthetic. Most published studies have focused on recurrence and survival after excisional versus incisional biopsies. Some of these studies hypothesized that tumor cells could be displaced deep to the deep dermis in the incisional biopsy specimens (9). Furthermore, it was postulated that due to the small amount of subcutaneous fat in the head and neck region, cutting into tumor in this region could seed cells directly into the blood vessels (10). On the other hand, some studies found no significant differences in survival between the two groups and these bore the recommendations of performing it in large lesions and those in cosmetically sensitive areas (6,7,11). In this study, we aimed to compare matched samples from the same specimen biopsied at two different points in time to determine if there was a difference in the Breslow thickness reported between the incision and excision biopsy samples. In addition, other prognostic indicators like Clark’s level and mitotic rates were also assessed. Our data show that there was a significant difference in these values between the incision and excision biopsy samples. The excision biopsy samples were of a greater Breslow thickness and Clark’s level compared to the initial incision biopsy counterpart. This suggests the validity of current recommendations however there are several points that can explain the observed differences. Firstly, the part of the specimen that is biopsied in the incision sample may not represent the true lesion. The darkest or ulcerated part of a pigmented lesion may not be the deepest area of invasion. Furthermore, there is a great deal of variability in technique, tissue handling and storage. As a result the tested sample may not be a true indication of the entire lesion. Given the degree of variability associated with this technique, the question of its usefulness comes into play. Ultimately histological data represented in this study show that there is a significant difference therefore treatment is ideally based on the standard excision biopsy sample unless the lesion has an exceptionally large surface area. In these situations multiple incision biopsies have a role as they can indicate a diagnosis. However for lesions in cosmetically sensitive areas, definitive treatment is ideal, not only for staging purposes but to offer the patient more definitive care. In these situations it may be beneficial to refer the patients to a plastic and reconstructive surgeon for the primary excision biopsy.
3
This study supports the recommendations made by Marsden et al. in not performing incisional biopsies in the initial management of malignant melanoma unless the case has been discussed and recommended at the level of the local or regional multidisciplinary team. The recommendation to perform an incision biopsy may be justified in very large, ulcerated lesions, which is not amenable to complete excision for an initial histological analysis.
Declaration of interest The authors report no conflicts of interest. The authors alone are responsible for the content and writing of this article.
References 1. de Vries E, van de Poll-Franse LV, Louwman WJ, et al. Predictions of skin cancer incidence in the Netherlands up to 2015. Br J Dermatol. 2005;152:481–8. 2. Gaudette LA, Gao RN. Changing trends in melanoma incidence and mortality. Health Rep. 1998;10:29–41. 3. Balch CM, Bunzaid AC, Soong SJ, et al. Final version of the American Joint Committee on Cancer staging system for cutaneous melanoma. J Clin Oncol. 2001;19:3635–48. 4. Marsden JR, Newton-Bishop JA, Burrows L, et al.; British Association of Dermatologists (BAD) Clinical Standards Unit. Revised UK guidelines for the management of cutaneous melanoma 2010. J Plast Reconstr Aesthet Surg. 2010;63:1401–19. 5. Telfer NR, Colver GB, Morton CA. Guidelines for the management of basal cell carcinoma. Br J Dermatol. 2008;159:35–48. 6. Griffiths R, Briggs JC. Biopsy procedures, primary wide excisional surgery and long term prognosis in primary clinical stage I invasive cutaneous malignant melanoma. Ann R Coll Surg Engl. 1985;67: 75–8. 7. Lees VC, Briggs JC. Effect of initial biopsy procedure on prognosis in Stage 1 invasive cutaneous malignant melanoma: review of 1086 patients. Br J Surg. 1991;78:1108–10. 8. Balch CM, Soong SJ, Gershenwald JE, et al. Prognostic factors analysis of 17,600 melanoma patients: validation of the American Joint Committee on Cancer melanoma staging system. J Clin Oncol. 2001;19:3622–34. 9. Epstein E, Bragg K, Linden G. Biopsy and prognosis of malignant melanoma. JAMA. 1969;208:1369–71. 10. Austin JR, Byers RM, Brown WD. Influence of biopsy on the prognosis of cutaneous melanoma of the head and neck. Head Neck. 1996;18:107–17. 11. Lederman JS, Sober AJ. Does biopsy type influence survival in clinical stage I cutaneous melanoma? J Am Acad Dermatol. 1985; 13:983–7.
