0
We're unable to sign you in at this time. Please try again in a few minutes.
Retry
We were able to sign you in, but your subscription(s) could not be found. Please try again in a few minutes.
Retry
There may be a problem with your account. Please contact the AMA Service Center to resolve this issue.
Contact the AMA Service Center:
Telephone: 1 (800) 262-2350 or 1 (312) 670-7827  *   Email: subscriptions@jamanetwork.com
Error Message ......
Study |

The Contribution of Nodular Subtype to Melanoma Mortality in the United States, 1978 to 2007 FREE

Waqas R. Shaikh, BS; Michael Xiong, BA; Martin A. Weinstock, MD, PhD
[+] Author Affiliations

Author Affiliations: Dermatoepidemiology Unit, Veterans Affairs Medical Center, Department of Dermatology, Rhode Island Hospital, and Departments of Dermatology and Community Health, Brown University, Providence.


Arch Dermatol. 2012;148(1):30-36. doi:10.1001/archdermatol.2011.264.
Text Size: A A A
Published online

Objective To gain insight into reducing melanoma mortality by examining epidemiologic trends by subtype with emphasis on the contribution of each subtype to melanoma-related death.

Design Retrospective population-based cohort study.

Setting Original 9 registries of the Surveillance, Epidemiology, and End Results Program from 1978 to 2007.

Participants A total of 111  478 patients with histologically confirmed invasive melanoma.

Main Outcome Measure Proportion of ultimately fatal melanomas by subtype.

Results Among melanomas of known subtype, superficial spreading melanoma comprised 66% of incident melanomas and 46% of ultimately fatal melanomas; nodular melanoma comprised 14% of incident melanomas and 37% of ultimately fatal melanomas. For superficial spreading melanoma, overall incidence per 100  000 per year increased (from 4.28 to 6.63), ultimately fatal incidence remained stable (at 0.56 to 0.51), and 10-year relative survival increased (from 90.6% to 96.5%) when comparing successive 5-year intervals. In contrast, for nodular melanoma, the overall incidence (1.30-1.32), ultimately fatal incidence (0.46-0.44), and 10-year relative survival rate (61.8%-61.5%) remained stable. Epidemiologic trends of melanoma, not otherwise specified, were similar to superficial spreading melanoma. There was a strong negative correlation between the proportion of melanoma, not otherwise specified, among all melanomas, and the proportion of superficial spreading melanoma, among melanomas of known subtype (r  =   −0.80; P  =  .01), across the registries.

Conclusions Superficial spreading and nodular melanoma constitute similar proportions of ultimately fatal melanomas. Although incidence of and survival from superficial spreading melanoma have increased from 1978 to 2007, neither the incidence of nor survival from nodular melanoma has changed. Public health efforts should include a focus on nodular melanoma for maximum reduction of melanoma mortality.

Although melanoma incidence has been rising in the United States for many decades, the mortality rate has been relatively stable since the early 1990s.1,2 Secondary prevention via improved early detection is thought to be responsible for stabilizing mortality and improving survival.3,4 Traditional public health efforts have focused on the ABCD (asymmetry, border irregularity, color variegation, and diameter >6 mm) warning signs for melanoma.5 These signs, however, are better at detecting superficial spreading melanoma (SSM) than nodular melanoma (NM).6 Tumor thickness is the most important marker for melanoma mortality and prognosis.7,8 Although NM comprises only 10% to 30% of melanomas, it accounts for most thick melanomas.912 The subtype classification system13 is based not only on histopathologic features but on practically relevant clinical ones as well.14,15 Because optimal clinical detection methods for SSM and NM differ, this study aimed (1) to determine the population-based contribution of subtypes to melanoma-related deaths, and (2) to analyze epidemiologic trends by subtype to guide public health efforts.

DATA SOURCE

Frequency, incidence, and survival data from 1978 to 2007 were obtained from the National Cancer Institute's Surveillance, Epidemiology, and End Results (SEER) Program.16 Analysis was restricted to patients diagnosed as having invasive melanoma in the original 9 SEER registries (Atlanta, Georgia; Connecticut; Detroit, Michigan; Hawaii; Iowa; New Mexico; San Francisco-Oakland, California; Seattle –Puget Sound, Washington; and Utah), which were established in the 1970s and comprise approximately 10% of the US population. Other SEER registries, which were added later, were not included in the analysis because of the interest in looking at trends over decades. Information on the data collection, reporting, and quality control methods for the SEER Program can be found at http://www.seer.cancer.gov. Institutional review board approval was not required because the data used were from a publicly available US government database.

DEFINITIONS

The International Classification of Diseases for Oncology, Third Edition, histology codes were used to define grouped histologic subtypes as followed: SSM (code 8743), NM (code 8721), lentigo maligna melanoma (LMM; code 8742), acral lentiginous melanoma (ALM; code 8744), amelanotic melanoma (AM; code 8730), other subtypes (Other; codes 8722, 8723, 8728, 8740, 8741, 8745, 8746, 8761, 8770-8774, and 8780), and melanoma, not otherwise specified (NOS; code 8720). Incident melanoma was defined as all cases of invasive melanoma. Ultimately fatal melanoma was defined as a case of incident melanoma in which the patient died during the study period, and the cause of death listed on the death certificate was melanoma.

Relative survival is the probability of survival in the absence of other causes of death. It is calculated by dividing the observed survival of a cohort group by the expected survival of a similar group while controlling for race, sex, age, and date at which the age was coded (SEER*Stat software, version 6.6.2; available at the SEER Program, National Cancer Institute, Web site: http://seer.cancer.gov/seerstat). Standard SEER exclusion criteria for survival analysis were applied (ie, cases that were coded as death certificate only, autopsy only, ≥2 primary cancers, and alive with no survival time). Because overall relative survival for melanoma stabilizes after 9 years (data not shown), analysis was limited to melanomas diagnosed during the period 1978 to 1997 with follow-up through 2007 when evaluating relative survival and rates of ultimately fatal melanoma. When evaluating incident cases and overall incidence rates, cases were analyzed from 1978 to 2007.

STATISTICAL ANALYSIS

The overall incidence and ultimately fatal incidence age-adjusted to the 2000 US population standard and the 10-year relative survival for invasive melanoma with 95% CIs were calculated using SEER*Stat software, version 6.6.2. Incidence of ultimately fatal melanomas was purposefully used instead of the melanoma mortality rate. The former tabulates death using the year of diagnosis, allowing for year-to-year comparison with the overall incidence, which also uses year of diagnosis. The latter tabulates death using the year of death, which does not allow for year-to-year comparison with the overall incidence because there is a lag between year of diagnosis and year of death. Relative survival was calculated using the Kaplan-Meier method. Stata SE software (version 8; StataCorp, College Station, Texas) was used to calculate correlation coefficients between the proportion of melanoma NOS, among all melanomas, and the proportion of each other grouped subtype, among known subtypes, across the SEER 9 registries. P values for correlation coefficients were calculated using a t test with the null hypothesis being that for each correlation, the correlation coefficient equals zero.17 All P values were 2-sided with statistical significance set as P   <  .05.

INCIDENT CASES AND ULTIMATELY FATAL CASES BY SUBTYPE

In the SEER 9 registries from 1978 to 2007, 111  478 incident cases of invasive melanoma were reported, including 9904 cases of ultimately fatal invasive melanoma initially diagnosed from 1978 to 1997. Superficial spreading melanoma and NM constituted 66% (43  427 cases) and 14% (8973 cases) of incident melanomas of known subtypes, respectively. From 1978 to 2007, there was no substantial change in the proportions of known subtypes. Table 1 provides details of the frequency and proportions for all subtypes, including melanoma NOS in 5-year time periods. In contrast to incident melanomas, SSM and NM constitute an approximately similar number and percentage (2343 cases [46%] and 1854 cases [37%], respectively) of ultimately fatal melanomas of known subtypes; no other subtype accounts for more than 6% of the total. The proportions remained relatively stable from 1978 to 1997. The fact that at least 1 in 5 cases of NM (1854 of 8973) is ultimately fatal and at least 1 in 19 cases of SSM (2343 of 43  427) is ultimately fatal is accounted for by the 10-year relative survival rates of NM and SSM of 61.5% and 96.5%, respectively. Proportions of ultimately fatal cases by subtype did not vary when stratified by sex: from 1978 to 1997, SSM and NM accounted for 45% (1458 cases) and 37% (1186 cases) of ultimately fatal melanomas, respectively, for males, and 48% (884 cases) and 36% (668 cases) of ultimately fatal melanomas, respectively, for females. Proportions of incident melanomas by subtype were also similar between sexes: SSM and NM contributed to 62% (22  051 cases) and 15% (5321 cases) of incident melanomas, respectively for males, and 71% (21  376 cases) and 12% (3652 cases) of incident melanomas, respectively for females. Table 2 provides details of the frequency and proportions for all subtypes, including melanoma NOS among ultimately fatal cases in 5-year time periods from 1978 to 1997.

Table Graphic Jump LocationTable 1. Melanoma Frequency Trends by Subtype in 111 478 Patients in SEER 9 Registries
Table Graphic Jump LocationTable 2. Melanoma Frequency Trends by Subtype Among Ultimately Fatal Cases in 9904 Patients in SEER 9 Registries
EPIDEMIOLOGIC TRENDS BY SUBTYPE

For NM and ALM, the overall incidence, ultimately fatal incidence, and 10-year relative survival were all relatively stable during the 30-year study period. This contrasted with SSM and LMM, for which overall incidence increased, ultimately fatal incidence remained stable, and 10-year relative survival increased during the study period. Tables 3, 4, and 5 provide details of the epidemiologic trends for all melanomas of known subtype and for melanoma NOS.

Table Graphic Jump LocationTable 3. Trends in Age-Adjusted Overall Incidence Rate per 100  000  (95% CI) by Subtype in 111  478 Patients in SEER 9 Registriesa
Table Graphic Jump LocationTable 4. Trends in Age-Adjusted Ultimately Fatal Incidence Rate per 100  000  (95% CI) by Subtype in 9904 Patients in SEER 9 Registriesa
Table Graphic Jump LocationTable 5. Trends in 10-Year Relative Survival Rate (95% CI) by Subtype in 50  491 Patients in SEER 9 Registriesa
ANALYSIS OF THE COMPOSITION OF MELANOMA NOS

From the SEER 9 registry data set, melanoma NOS accounted for 46  108 cases of all incident melanomas (41%) and 4832 cases of all ultimately fatal melanomas (49%). Because melanoma NOS comprises such a high proportion of diagnosed cases, attempts were made to find clues to its composition. Trends in overall incidence, ultimately fatal incidence, and 10-year relative survival were similar between melanoma NOS and SSM and LMM (Tables 3-5). The proportion of melanoma NOS, among all incident cases, negatively correlated most closely with the proportion of SSM, among melanomas of known subtype, across the SEER 9 registries (r  =   −0.80; P  =  .01) (Table 6). When restricting the data set to ultimately fatal cases, the proportion of melanoma NOS negatively correlated most closely with the proportion of SSM across the SEER 9 registries (r  =   −0.66; P  =  .05) (Table 6).

Table Graphic Jump LocationTable 6. Relationship Between Melanoma NOS and Each Known Subtype in SEER 9 Registries: Correlation Between the Proportion of Melanoma NOS Among All Melanomas and the Proportion of Each Subtype Among Known Melanoma Subtypes

This study has several major findings. First, NM accounts for a high proportion of ultimately fatal cases of invasive melanoma (37%). Second, over the past 30 years the overall incidence, ultimately fatal incidence, and relative survival for NM have not changed. However, for SSM the overall incidence and relative survival have gradually increased, whereas the ultimately fatal incidence has not changed. Third, there are similarities between melanoma NOS and SSM, as demonstrated by similar trends in overall incidence, ultimately fatal incidence, and relative survival; further support is demonstrated by the statistically significant, strong, negative correlation between melanoma NOS and SSM among both incident and ultimately fatal cases across the SEER registries.

Nodular melanoma accounts for a disproportionate fraction of ultimately fatal cases compared with incident cases (37% vs 14%). Because NM accounts for 37% of ultimately fatal cases of melanoma, early detection of NM is needed to reduce melanoma mortality. This finding is consistent with those of previous studies that have associated NM with proxies for case fatality, such as tumor thickness,9,10,1820 biologic aggressiveness,10 rate of growth,21 mitotic rate,11 ulceration,11 Clark level,11 and incidence of recurrence in the sentinel lymph node basin.22,23 These “aggressive ” characteristics may be associated with distinct genetic pathways of NM compared with other subtypes, although more research is needed. Nodular melanoma is more likely to have loss of p16 expression24 and lower rates of BRAF mutation25 compared with SSM. In addition, NM compared with other subtypes is associated with NRAS mutation26 and overexpression of securin, a protein encoded by proto-oncogene hPTTG.27 The association between melanoma subtype and genetic mutations may provide the framework for a new classification system that not only highlights the different clinical presentations of melanoma but also predicts therapeutic response.14,15

This study's results show that the overall incidence, ultimately fatal incidence, and relative survival for NM have been relatively stable during the past 30 years. Evaluation of the progress against cancer is made by simultaneously interpreting trends in overall incidence, ultimately fatal incidence, and relative survival.28 Analysis of NM trends shows that there has been a lack of progress concerning NM both in terms of detection and treatment. Awareness and early detection campaigns have generally used the ABCD criteria.29 Although these criteria can sometimes detect NM, usually in late presentations, oftentimes they fail to detect NM.30,31 Thus, a lack of progress in detecting NM may not be surprising. In addition, melanoma treatment has made only marginal advances in survival.32 In a major academic center in the United States, there were no changes in NM tumor thickness or ulceration status between the time periods 1972 to 1982 and 2002 to 2007.11 Similar results for thickness trends for NM were found in Italy.33 The findings of both studies are consistent with this study's results of an unchanged ultimately fatal incidence and relative survival for NM and further underscore the importance of making progress against NM.

If the goal is to reduce melanoma mortality, then a key challenge is to detect thin NMs. Nodular melanomas commonly occur in men older than 50 years on the head and neck.10 Because those lesions often do not meet the ABCD criteria, the E criterion (evolving) was added to help detect NM, among other reasons.3,29 In addition, the EFG (elevation, firm, growing) criteria were introduced to highlight important clinical features of NM.6 These additional diagnostic aids are relatively new, and time will tell if they can help to detect NM at an early stage of development. Geller et al34 analyzed clinical characteristics of NM and discovered that in comparison with SSM, thick NM tended to be pale, with no color, blisterlike, and raised or lumpy, and discovered in patients who had not been examined by a physician within the past 3 years. Changes in size, shape, or color were more likely in thin NMs than in thick NMs.34 Warycha et al11 found that most NMs were elevated and reported a shorter median duration of change in comparison with SSM (5 months vs 9 months, respectively). One case series evaluated 11 cases of thin NMs.12 They concluded that NMs often possess unremarkable clinical features and that physicians need to be suspicious of new or changing lesions as a key warning sign.12 Furthermore, they found that dermoscopic features, such as “homogenous disorganized pattern, asymmetry, a blue-white veil, structureless areas, and atypical vascular structures, ”12(pp316-317) provided clues to the cancerous nature of the lesion. Further research is needed about the early warning signs of NM.

Superficial spreading melanoma is the most common subtype and accounts for the largest number of fatal cases. Progress in the detection and treatment of SSM is suggested by an improved relative survival. Controversies have arisen as to the discrepancy between a rising overall incidence rate and a stable overall mortality rate. One explanation is overdiagnosis or misdiagnosis of indolent melanomas3539 owing to increased rates of biopsy40,41 and a lowered histologic threshold for the diagnosis of malignant disease. However, this argument does not explain the increase in thicker melanomas,42,43 especially among lower socioeconomic groups.44 The likely explanation is both a rise in overdiagnosis or misdiagnosis of indolent melanomas and a real rise in the burden of invasive melanomas. Despite the ultimately fatal incidence remaining relatively stable, the 10-year relative survival has improved. Survival rates provide a good measure of progress against cancer.28 This improvement in survival is believed to be related to a combination of education, screening, early detection, and excision of primary tumors in the early stage of development,3,4 as there have been no major advancements in melanoma treatment.45

To understand the composition of the melanoma NOS category, a comparison of epidemiologic trends of melanoma NOS with known subtypes was made. The overall incidence, ultimately fatal incidence, and relative survival trends for melanoma NOS were similar to those of SSM. Further analysis revealed a statistically significant, strong, negative correlation between the proportion of SSM, among known subtypes, and the proportion of melanoma NOS, among all melanomas, across the SEER registries. Presuming that the proportion of each known melanoma subtype is constant throughout the different SEER registries, then any change in the proportion of melanoma NOS with a corresponding reciprocal change in the proportion of a known subtype suggests the transfer of that subtype into the melanoma NOS category. Both of these findings suggest that a significant proportion of SSM is included in the melanoma NOS subcategory. A previous study that analyzed the same SEER database found that “the distribution and median thickness of melanoma NOS ”9(p749) resembled that of SSM rather than that of NM. Although not conclusive, all these findings suggest that a high proportion of melanoma NOS are SSM. If this is true, then the true proportion of NM among ultimately fatal cases would be lower than was calculated.

There are several limitations. First, 41% of incident and 49% of ultimately fatal melanomas were recorded as melanoma NOS. These numbers are high, and, depending on the subtype composition of melanoma, NOS can greatly influence the ultimate relative proportions of each subtype among incident and ultimately fatal cases. There are suggestions that melanoma NOS is composed mainly of SSM, but no firm conclusion can be reached. The second limitation is that there is underreporting and delayed reporting to the SEER registries.39,4649 Given that there is some controversy regarding NM as a distinct entity,50,51 some pathologists may not be recording NM in pathology reports, which in turn would make this study's results for NM more pronounced. Third, there is no independent verification as to the accuracy of the subtype coding by the SEER registries.52 Finally, Breslow thickness was not included in the analysis because it does not have the practical relevance in optimizing clinical detection.14,15

Despite these limitations, this study has major strengths. The use of the SEER population-based database provides quality-controlled data with a high number of cases across geographically diverse areas over a 30-year time period that is largely characteristic of the US population. The use of ultimately fatal incidence instead of mortality rate allows for fair year-to-year comparisons to the overall incidence. Finally, the use of relative survival instead of melanoma-specific survival captures both direct and indirect causes of mortality while circumventing reliance on the accuracy of death certificate coding.28,5356

Given the recent plateauing of melanoma mortality, new strategies are needed. Based on the results of this study that NM makes a substantial contribution to melanoma mortality with no change in overall incidence, ultimately fatal incidence, and relative survival over the past 3 decades, the authors recommend that public health efforts should include a focus on NM for maximum reduction of melanoma mortality. Although the classification of melanoma into subtypes does not correlate to prognosis as well as tumor thickness, ulceration status, and mitotic activity, it does identify clinically relevant and unique forms of melanoma.14,15 Emphasis on the E criterion and the EFG rule may be useful since the ABCD warning signs preferentially detect SSM. Widespread use and competence in dermoscopy may also allow for earlier detection when historical or clinical features are limited. Individuals at high risk for NM (especially men > 50 years) can be targeted. Given that NMs often have a history of change with a median duration of 5 months, recommendation of the monthly thorough skin self-examination11,57 to patients is even more crucial. Finally, given the relatively high proportion of melanoma NOS in the SEER database, we recommend the complete and accurate reporting of cases to the SEER registries, which is essential for detailed characterization of melanoma.

Correspondence: Martin A. Weinstock, MD, PhD, Dermatoepidemiology Unit-111D, Veterans Affairs Medical Center, 830 Chalkstone Ave, Providence, RI 02908-4799 (maw@brown.edu).

Accepted for Publication: July 12, 2011.

Published Online: September 19, 2011. doi:10.1001/archdermatol.2011.264

Author Contributions: Dr Weinstock had full access to all of the data in the study and takes responsibility for the integrity of the data and the accuracy of the data analysis. Study concept and design: Shaikh, Xiong, and Weinstock. Acquisition of data: Weinstock. Analysis and interpretation of data: Shaikh, Xiong, and Weinstock. Drafting of the manuscript: Shaikh and Weinstock. Critical revision of the manuscript for important intellectual content: Shaikh, Xiong, and Weinstock. Statistical analysis: Shaikh, Xiong, and Weinstock. Obtained funding: Weinstock. Administrative, technical, and material support: Weinstock. Study supervision: Weinstock.

Financial Disclosure: None reported.

Funding/Support: This study was supported in part by the Department of Veterans Affairs Office of Research and Development Co-operative Studies Program (Mr Shaikh and Dr Weinstock), the Melanoma Research Alliance Team Science Award (Mr Shaikh and Dr Weinstock), and grants R01AR49342/R25CA087972 from the National Institutes of Health (Weinstock).

Role of the Sponsors: The sponsors had no role in the design and conduct of the study; in the collection, analysis, and interpretation of data; or in the preparation, review, or approval of the manuscript.

Altekruse SF, Kosary CL, Krapcho M,  et al.  SEER Cancer Statistics Review, 1975-2007, National Cancer Institute. SEER Web site, 2010. http://seer.cancer.gov/csr/1975_2007/. Accessed January 3, 2011
Tucker MA. Melanoma epidemiology.  Hematol Oncol Clin North Am. 2009;23(3):383-395
PubMed   |  Link to Article
Rigel DS, Friedman RJ, Kopf AW, Polsky D. ABCDE: an evolving concept in the early detection of melanoma.  Arch Dermatol. 2005;141(8):1032-1034
PubMed   |  Link to Article
Weinstock MA. Progress and prospects on melanoma: the way forward for early detection and reduced mortality.  Clin Cancer Res. 2006;12(7, pt 2):2297s-2300s
PubMed   |  Link to Article
Rigel DS, Russak J, Friedman R. The evolution of melanoma diagnosis: 25 years beyond the ABCDs.  CA Cancer J Clin. 2010;60(5):301-316
PubMed   |  Link to Article
Kelly JW. Nodular melanoma: how current approaches to early detection are failing.  J Drugs Dermatol. 2005;4(6):790-793
PubMed
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(16):3622-3634
PubMed
Balch CM, Gershenwald JE, Soong SJ,  et al.  Final version of 2009 AJCC melanoma staging and classification.  J Clin Oncol. 2009;27(36):6199-6206
PubMed   |  Link to Article
Demierre MF, Chung C, Miller DR, Geller AC. Early detection of thick melanomas in the United States: beware of the nodular subtype.  Arch Dermatol. 2005;141(6):745-750
PubMed   |  Link to Article
Chamberlain AJ, Fritschi L, Giles GG, Dowling JP, Kelly JW. Nodular type and older age as the most significant associations of thick melanoma in Victoria, Australia.  Arch Dermatol. 2002;138(5):609-614
PubMed   |  Link to Article
Warycha MA, Christos PJ, Mazumdar M,  et al.  Changes in the presentation of nodular and superficial spreading melanomas over 35 years.  Cancer. 2008;113(12):3341-3348
PubMed   |  Link to Article
Kalkhoran S, Milne O, Zalaudek I,  et al.  Historical, clinical, and dermoscopic characteristics of thin nodular melanoma.  Arch Dermatol. 2010;146(3):311-318
PubMed   |  Link to Article
Clark WH Jr, From L, Bernardino EA, Mihm MC. The histogenesis and biologic behavior of primary human malignant melanomas of the skin.  Cancer Res. 1969;29(3):705-727
PubMed
Duncan LM. The classification of cutaneous melanoma.  Hematol Oncol Clin North Am. 2009;23(3):501-513
PubMed   |  Link to Article
Scolyer RA, Long GV, Thompson JF. Evolving concepts in melanoma classification and their relevance to multidisciplinary melanoma patient care.  Mol Oncol. 2011;5(2):124-136
PubMed   |  Link to Article
 Surveillance, Epidemiology, and End Results (SEER) Program SEER*Stat Database: Incidence —SEER 17 Research Data. National Cancer Institute Web site, DCCPS, Surveillance Research Program, Cancer Statistics Branch, released April 2010, based on the November 2009 submission. http://seer.cancer.gov/data/access.html. Accessed January 3, 2011
Hamilton LC. Statistics with STATA. Belmont, CA: Thomson Learning Inc; 2002
Bergenmar M, Hansson J, Brandberg Y. Detection of nodular and superficial spreading melanoma with tumour thickness < or  =  2.0 mm: an interview study.  Eur J Cancer Prev. 2002;11(1):49-55
PubMed   |  Link to Article
Carli P, De Giorgi V, Palli D,  et al.  Patterns of detection of superficial spreading and nodular-type melanoma: a multicenter Italian study.  Dermatol Surg. 2004;30(11):1371-1375
PubMed   |  Link to Article
Jemal A, Devesa SS, Hartge P, Tucker MA. Recent trends in cutaneous melanoma incidence among whites in the United States.  J Natl Cancer Inst. 2001;93(9):678-683
PubMed   |  Link to Article
Liu W, Dowling JP, Murray WK,  et al.  Rate of growth in melanomas: characteristics and associations of rapidly growing melanomas.  Arch Dermatol. 2006;142(12):1551-1558
PubMed   |  Link to Article
Corrigan MA, Coffey JC, O ’Sullivan MJ, Fogarty KM, Redmond HP. Sentinel lymph node biopsy: is it possible to reduce false negative rates by excluding patients with nodular melanoma?  Surgeon. 2006;4(3):153-157
PubMed   |  Link to Article
Nowecki ZI, Rutkowski P, Nasierowska-Guttmejer A, Ruka W. Survival analysis and clinicopathological factors associated with false-negative sentinel lymph node biopsy findings in patients with cutaneous melanoma.  Ann Surg Oncol. 2006;13(12):1655-1663
PubMed   |  Link to Article
Pavey SJ, Cummings MC, Whiteman DC,  et al.  Loss of p16 expression is associated with histological features of melanoma invasion.  Melanoma Res. 2002;12(6):539-547
PubMed   |  Link to Article
Liu W, Kelly JW, Trivett M,  et al.  Distinct clinical and pathological features are associated with the BRAF(T1799A(V600E)) mutation in primary melanoma.  J Invest Dermatol. 2007;127(4):900-905
PubMed   |  Link to Article
Lee JH, Choi JW, Kim YS. Frequencies of BRAF and NRAS mutations are different in histologic types and sites of origin of cutaneous melanoma: a meta-analysis.  Br J Dermatol. 2010;164(4):776-784
Link to Article
Winnepenninckx V, Debiec-Rychter M, Beli ën JA,  et al.  Expression and possible role of hPTTG1/securin in cutaneous malignant melanoma.  Mod Pathol. 2006;19(9):1170-1180
PubMed   |  Link to Article
Dickman PW, Adami HO. Interpreting trends in cancer patient survival.  J Intern Med. 2006;260(2):103-117
PubMed   |  Link to Article
Abbasi NR, Shaw HM, Rigel DS,  et al.  Early diagnosis of cutaneous melanoma: revisiting the ABCD criteria.  JAMA. 2004;292(22):2771-2776
PubMed   |  Link to Article
Kelly JW, Chamberlain AJ, Staples MP, McAvoy B. Nodular melanoma: no longer as simple as ABC.  Aust Fam Physician. 2003;32(9):706-709
PubMed
Chamberlain AJ, Fritschi L, Kelly JW. Nodular melanoma: patients' perceptions of presenting features and implications for earlier detection.  J Am Acad Dermatol. 2003;48(5):694-701
PubMed   |  Link to Article
Lee KC, Weinstock MA. Melanoma is up: are we up to this challenge?  J Invest Dermatol. 2009;129(7):1604-1606
PubMed   |  Link to Article
Crocetti E, Caldarella A, Chiarugi A, Nardini P, Zappa M. The thickness of melanomas has decreased in central Italy, but only for thin melanomas, while thick melanomas are as thick as in the past.  Melanoma Res. 2010;20(5):422-426
PubMed
Geller AC, Elwood M, Swetter SM,  et al.  Factors related to the presentation of thin and thick nodular melanoma from a population-based cancer registry in Queensland Australia.  Cancer. 2009;115(6):1318-1327
PubMed   |  Link to Article
Burton RC, Armstrong BK. Non-metastasizing melanoma?  J Surg Oncol. 1998;67(2):73-76
PubMed   |  Link to Article
Swerlick RA, Chen S. The melanoma epidemic: more apparent than real?  Mayo Clin Proc. 1997;72(6):559-564
PubMed   |  Link to Article
Edman RL, Klaus SN. Is routine screening for melanoma a benign practice?  JAMA. 2000;284(7):883-886
PubMed   |  Link to Article
Kopf AW, Rigel DS, Friedman RJ. The rising incidence and mortality rate of malignant melanoma.  J Dermatol Surg Oncol. 1982;8(9):760-761
PubMed
Hall HI, Jamison P, Fulton JP, Clutter G, Roffers S, Parrish P. Reporting cutaneous melanoma to cancer registries in the United States.  J Am Acad Dermatol. 2003;49(4):624-630
PubMed   |  Link to Article
Welch HG, Woloshin S, Schwartz LM. Skin biopsy rates and incidence of melanoma: population based ecological study.  BMJ. 2005;331(7515):481
PubMed   |  Link to Article
Qin J, Berwick M, Ashbolt R, Dwyer T. Quantifying the change of melanoma incidence by Breslow thickness.  Biometrics. 2002;58(3):665-670
PubMed   |  Link to Article
Geller AC, Miller DR, Annas GD, Demierre MF, Gilchrest BA, Koh HK. Melanoma incidence and mortality among US whites, 1969-1999.  JAMA. 2002;288(14):1719-1720
PubMed   |  Link to Article
Dennis LK. Analysis of the melanoma epidemic, both apparent and real: data from the 1973 through 1994 surveillance, epidemiology, and end results program registry.  Arch Dermatol. 1999;135(3):275-280
PubMed   |  Link to Article
Linos E, Swetter SM, Cockburn MG, Colditz GA, Clarke CA. Increasing burden of melanoma in the United States.  J Invest Dermatol. 2009;129(7):1666-1674
PubMed   |  Link to Article
Korn EL, Liu PY, Lee SJ,  et al.  Meta-analysis of phase II cooperative group trials in metastatic stage IV melanoma to determine progression-free and overall survival benchmarks for future phase II trials.  J Clin Oncol. 2008;26(4):527-534
PubMed   |  Link to Article
Koh HK, Geller A, Miller DR, Clapp RW, Lew RA. Underreporting of cutaneous melanoma in cancer registries nationwide.  J Am Acad Dermatol. 1992;27(6, pt 1):1035-1036
PubMed   |  Link to Article
Cockburn M, Swetter SM, Peng D, Keegan TH, Deapen D, Clarke CA. Melanoma underreporting: why does it happen, how big is the problem, and how do we fix it?  J Am Acad Dermatol. 2008;59(6):1081-1085
PubMed   |  Link to Article
Clegg LX, Feuer EJ, Midthune DN, Fay MP, Hankey BF. Impact of reporting delay and reporting error on cancer incidence rates and trends.  J Natl Cancer Inst. 2002;94(20):1537-1545
PubMed   |  Link to Article
Howlader N, Ries LA, Stinchcomb DG, Edwards BK. The impact of underreported Veterans Affairs data on national cancer statistics: analysis using population-based SEER registries.  J Natl Cancer Inst. 2009;101(7):533-536
PubMed   |  Link to Article
Ackerman AB. Malignant melanoma: a unifying concept.  Hum Pathol. 1980;11(6):591-595
PubMed   |  Link to Article
Heenan PJ. Nodular melanoma is not a distinct entity.  Arch Dermatol. 2003;139(3):387
PubMed   |  Link to Article
Merlino LA, Sullivan KJ, Whitaker DC, Lynch CF. The independent pathology laboratory as a reporting source for cutaneous melanoma incidence in Iowa, 1977-1994.  J Am Acad Dermatol. 1997;37(4):578-585
PubMed   |  Link to Article
Begg CB, Schrag D. Attribution of deaths following cancer treatment.  J Natl Cancer Inst. 2002;94(14):1044-1045
PubMed   |  Link to Article
Sarfati D, Blakely T, Pearce N. Measuring cancer survival in populations: relative survival vs cancer-specific survival.  Int J Epidemiol. 2010;39(2):598-610
PubMed   |  Link to Article
James DS, Bull AD. Information on death certificates: cause for concern?  J Clin Pathol. 1996;49(3):213-216
PubMed   |  Link to Article
Maudsley G, Williams EM.  “Inaccuracy ” in death certification: where are we now?  J Public Health Med. 1996;18(1):59-66
PubMed   |  Link to Article
Berwick M, Begg CB, Fine JA, Roush GC, Barnhill RL. Screening for cutaneous melanoma by skin self-examination.  J Natl Cancer Inst. 1996;88(1):17-23
PubMed   |  Link to Article

First Page Preview

View Large
First page PDF preview

Figures

Tables

Table Graphic Jump LocationTable 1. Melanoma Frequency Trends by Subtype in 111 478 Patients in SEER 9 Registries
Table Graphic Jump LocationTable 2. Melanoma Frequency Trends by Subtype Among Ultimately Fatal Cases in 9904 Patients in SEER 9 Registries
Table Graphic Jump LocationTable 3. Trends in Age-Adjusted Overall Incidence Rate per 100  000  (95% CI) by Subtype in 111  478 Patients in SEER 9 Registriesa
Table Graphic Jump LocationTable 4. Trends in Age-Adjusted Ultimately Fatal Incidence Rate per 100  000  (95% CI) by Subtype in 9904 Patients in SEER 9 Registriesa
Table Graphic Jump LocationTable 5. Trends in 10-Year Relative Survival Rate (95% CI) by Subtype in 50  491 Patients in SEER 9 Registriesa
Table Graphic Jump LocationTable 6. Relationship Between Melanoma NOS and Each Known Subtype in SEER 9 Registries: Correlation Between the Proportion of Melanoma NOS Among All Melanomas and the Proportion of Each Subtype Among Known Melanoma Subtypes

References

Altekruse SF, Kosary CL, Krapcho M,  et al.  SEER Cancer Statistics Review, 1975-2007, National Cancer Institute. SEER Web site, 2010. http://seer.cancer.gov/csr/1975_2007/. Accessed January 3, 2011
Tucker MA. Melanoma epidemiology.  Hematol Oncol Clin North Am. 2009;23(3):383-395
PubMed   |  Link to Article
Rigel DS, Friedman RJ, Kopf AW, Polsky D. ABCDE: an evolving concept in the early detection of melanoma.  Arch Dermatol. 2005;141(8):1032-1034
PubMed   |  Link to Article
Weinstock MA. Progress and prospects on melanoma: the way forward for early detection and reduced mortality.  Clin Cancer Res. 2006;12(7, pt 2):2297s-2300s
PubMed   |  Link to Article
Rigel DS, Russak J, Friedman R. The evolution of melanoma diagnosis: 25 years beyond the ABCDs.  CA Cancer J Clin. 2010;60(5):301-316
PubMed   |  Link to Article
Kelly JW. Nodular melanoma: how current approaches to early detection are failing.  J Drugs Dermatol. 2005;4(6):790-793
PubMed
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(16):3622-3634
PubMed
Balch CM, Gershenwald JE, Soong SJ,  et al.  Final version of 2009 AJCC melanoma staging and classification.  J Clin Oncol. 2009;27(36):6199-6206
PubMed   |  Link to Article
Demierre MF, Chung C, Miller DR, Geller AC. Early detection of thick melanomas in the United States: beware of the nodular subtype.  Arch Dermatol. 2005;141(6):745-750
PubMed   |  Link to Article
Chamberlain AJ, Fritschi L, Giles GG, Dowling JP, Kelly JW. Nodular type and older age as the most significant associations of thick melanoma in Victoria, Australia.  Arch Dermatol. 2002;138(5):609-614
PubMed   |  Link to Article
Warycha MA, Christos PJ, Mazumdar M,  et al.  Changes in the presentation of nodular and superficial spreading melanomas over 35 years.  Cancer. 2008;113(12):3341-3348
PubMed   |  Link to Article
Kalkhoran S, Milne O, Zalaudek I,  et al.  Historical, clinical, and dermoscopic characteristics of thin nodular melanoma.  Arch Dermatol. 2010;146(3):311-318
PubMed   |  Link to Article
Clark WH Jr, From L, Bernardino EA, Mihm MC. The histogenesis and biologic behavior of primary human malignant melanomas of the skin.  Cancer Res. 1969;29(3):705-727
PubMed
Duncan LM. The classification of cutaneous melanoma.  Hematol Oncol Clin North Am. 2009;23(3):501-513
PubMed   |  Link to Article
Scolyer RA, Long GV, Thompson JF. Evolving concepts in melanoma classification and their relevance to multidisciplinary melanoma patient care.  Mol Oncol. 2011;5(2):124-136
PubMed   |  Link to Article
 Surveillance, Epidemiology, and End Results (SEER) Program SEER*Stat Database: Incidence —SEER 17 Research Data. National Cancer Institute Web site, DCCPS, Surveillance Research Program, Cancer Statistics Branch, released April 2010, based on the November 2009 submission. http://seer.cancer.gov/data/access.html. Accessed January 3, 2011
Hamilton LC. Statistics with STATA. Belmont, CA: Thomson Learning Inc; 2002
Bergenmar M, Hansson J, Brandberg Y. Detection of nodular and superficial spreading melanoma with tumour thickness < or  =  2.0 mm: an interview study.  Eur J Cancer Prev. 2002;11(1):49-55
PubMed   |  Link to Article
Carli P, De Giorgi V, Palli D,  et al.  Patterns of detection of superficial spreading and nodular-type melanoma: a multicenter Italian study.  Dermatol Surg. 2004;30(11):1371-1375
PubMed   |  Link to Article
Jemal A, Devesa SS, Hartge P, Tucker MA. Recent trends in cutaneous melanoma incidence among whites in the United States.  J Natl Cancer Inst. 2001;93(9):678-683
PubMed   |  Link to Article
Liu W, Dowling JP, Murray WK,  et al.  Rate of growth in melanomas: characteristics and associations of rapidly growing melanomas.  Arch Dermatol. 2006;142(12):1551-1558
PubMed   |  Link to Article
Corrigan MA, Coffey JC, O ’Sullivan MJ, Fogarty KM, Redmond HP. Sentinel lymph node biopsy: is it possible to reduce false negative rates by excluding patients with nodular melanoma?  Surgeon. 2006;4(3):153-157
PubMed   |  Link to Article
Nowecki ZI, Rutkowski P, Nasierowska-Guttmejer A, Ruka W. Survival analysis and clinicopathological factors associated with false-negative sentinel lymph node biopsy findings in patients with cutaneous melanoma.  Ann Surg Oncol. 2006;13(12):1655-1663
PubMed   |  Link to Article
Pavey SJ, Cummings MC, Whiteman DC,  et al.  Loss of p16 expression is associated with histological features of melanoma invasion.  Melanoma Res. 2002;12(6):539-547
PubMed   |  Link to Article
Liu W, Kelly JW, Trivett M,  et al.  Distinct clinical and pathological features are associated with the BRAF(T1799A(V600E)) mutation in primary melanoma.  J Invest Dermatol. 2007;127(4):900-905
PubMed   |  Link to Article
Lee JH, Choi JW, Kim YS. Frequencies of BRAF and NRAS mutations are different in histologic types and sites of origin of cutaneous melanoma: a meta-analysis.  Br J Dermatol. 2010;164(4):776-784
Link to Article
Winnepenninckx V, Debiec-Rychter M, Beli ën JA,  et al.  Expression and possible role of hPTTG1/securin in cutaneous malignant melanoma.  Mod Pathol. 2006;19(9):1170-1180
PubMed   |  Link to Article
Dickman PW, Adami HO. Interpreting trends in cancer patient survival.  J Intern Med. 2006;260(2):103-117
PubMed   |  Link to Article
Abbasi NR, Shaw HM, Rigel DS,  et al.  Early diagnosis of cutaneous melanoma: revisiting the ABCD criteria.  JAMA. 2004;292(22):2771-2776
PubMed   |  Link to Article
Kelly JW, Chamberlain AJ, Staples MP, McAvoy B. Nodular melanoma: no longer as simple as ABC.  Aust Fam Physician. 2003;32(9):706-709
PubMed
Chamberlain AJ, Fritschi L, Kelly JW. Nodular melanoma: patients' perceptions of presenting features and implications for earlier detection.  J Am Acad Dermatol. 2003;48(5):694-701
PubMed   |  Link to Article
Lee KC, Weinstock MA. Melanoma is up: are we up to this challenge?  J Invest Dermatol. 2009;129(7):1604-1606
PubMed   |  Link to Article
Crocetti E, Caldarella A, Chiarugi A, Nardini P, Zappa M. The thickness of melanomas has decreased in central Italy, but only for thin melanomas, while thick melanomas are as thick as in the past.  Melanoma Res. 2010;20(5):422-426
PubMed
Geller AC, Elwood M, Swetter SM,  et al.  Factors related to the presentation of thin and thick nodular melanoma from a population-based cancer registry in Queensland Australia.  Cancer. 2009;115(6):1318-1327
PubMed   |  Link to Article
Burton RC, Armstrong BK. Non-metastasizing melanoma?  J Surg Oncol. 1998;67(2):73-76
PubMed   |  Link to Article
Swerlick RA, Chen S. The melanoma epidemic: more apparent than real?  Mayo Clin Proc. 1997;72(6):559-564
PubMed   |  Link to Article
Edman RL, Klaus SN. Is routine screening for melanoma a benign practice?  JAMA. 2000;284(7):883-886
PubMed   |  Link to Article
Kopf AW, Rigel DS, Friedman RJ. The rising incidence and mortality rate of malignant melanoma.  J Dermatol Surg Oncol. 1982;8(9):760-761
PubMed
Hall HI, Jamison P, Fulton JP, Clutter G, Roffers S, Parrish P. Reporting cutaneous melanoma to cancer registries in the United States.  J Am Acad Dermatol. 2003;49(4):624-630
PubMed   |  Link to Article
Welch HG, Woloshin S, Schwartz LM. Skin biopsy rates and incidence of melanoma: population based ecological study.  BMJ. 2005;331(7515):481
PubMed   |  Link to Article
Qin J, Berwick M, Ashbolt R, Dwyer T. Quantifying the change of melanoma incidence by Breslow thickness.  Biometrics. 2002;58(3):665-670
PubMed   |  Link to Article
Geller AC, Miller DR, Annas GD, Demierre MF, Gilchrest BA, Koh HK. Melanoma incidence and mortality among US whites, 1969-1999.  JAMA. 2002;288(14):1719-1720
PubMed   |  Link to Article
Dennis LK. Analysis of the melanoma epidemic, both apparent and real: data from the 1973 through 1994 surveillance, epidemiology, and end results program registry.  Arch Dermatol. 1999;135(3):275-280
PubMed   |  Link to Article
Linos E, Swetter SM, Cockburn MG, Colditz GA, Clarke CA. Increasing burden of melanoma in the United States.  J Invest Dermatol. 2009;129(7):1666-1674
PubMed   |  Link to Article
Korn EL, Liu PY, Lee SJ,  et al.  Meta-analysis of phase II cooperative group trials in metastatic stage IV melanoma to determine progression-free and overall survival benchmarks for future phase II trials.  J Clin Oncol. 2008;26(4):527-534
PubMed   |  Link to Article
Koh HK, Geller A, Miller DR, Clapp RW, Lew RA. Underreporting of cutaneous melanoma in cancer registries nationwide.  J Am Acad Dermatol. 1992;27(6, pt 1):1035-1036
PubMed   |  Link to Article
Cockburn M, Swetter SM, Peng D, Keegan TH, Deapen D, Clarke CA. Melanoma underreporting: why does it happen, how big is the problem, and how do we fix it?  J Am Acad Dermatol. 2008;59(6):1081-1085
PubMed   |  Link to Article
Clegg LX, Feuer EJ, Midthune DN, Fay MP, Hankey BF. Impact of reporting delay and reporting error on cancer incidence rates and trends.  J Natl Cancer Inst. 2002;94(20):1537-1545
PubMed   |  Link to Article
Howlader N, Ries LA, Stinchcomb DG, Edwards BK. The impact of underreported Veterans Affairs data on national cancer statistics: analysis using population-based SEER registries.  J Natl Cancer Inst. 2009;101(7):533-536
PubMed   |  Link to Article
Ackerman AB. Malignant melanoma: a unifying concept.  Hum Pathol. 1980;11(6):591-595
PubMed   |  Link to Article
Heenan PJ. Nodular melanoma is not a distinct entity.  Arch Dermatol. 2003;139(3):387
PubMed   |  Link to Article
Merlino LA, Sullivan KJ, Whitaker DC, Lynch CF. The independent pathology laboratory as a reporting source for cutaneous melanoma incidence in Iowa, 1977-1994.  J Am Acad Dermatol. 1997;37(4):578-585
PubMed   |  Link to Article
Begg CB, Schrag D. Attribution of deaths following cancer treatment.  J Natl Cancer Inst. 2002;94(14):1044-1045
PubMed   |  Link to Article
Sarfati D, Blakely T, Pearce N. Measuring cancer survival in populations: relative survival vs cancer-specific survival.  Int J Epidemiol. 2010;39(2):598-610
PubMed   |  Link to Article
James DS, Bull AD. Information on death certificates: cause for concern?  J Clin Pathol. 1996;49(3):213-216
PubMed   |  Link to Article
Maudsley G, Williams EM.  “Inaccuracy ” in death certification: where are we now?  J Public Health Med. 1996;18(1):59-66
PubMed   |  Link to Article
Berwick M, Begg CB, Fine JA, Roush GC, Barnhill RL. Screening for cutaneous melanoma by skin self-examination.  J Natl Cancer Inst. 1996;88(1):17-23
PubMed   |  Link to Article

Correspondence

CME
Meets CME requirements for:
Browse CME for all U.S. States
Accreditation Information
The American Medical Association is accredited by the Accreditation Council for Continuing Medical Education to provide continuing medical education for physicians. The AMA designates this journal-based CME activity for a maximum of 1 AMA PRA Category 1 CreditTM per course. Physicians should claim only the credit commensurate with the extent of their participation in the activity. Physicians who complete the CME course and score at least 80% correct on the quiz are eligible for AMA PRA Category 1 CreditTM.
Note: You must get at least of the answers correct to pass this quiz.
You have not filled in all the answers to complete this quiz
The following questions were not answered:
Sorry, you have unsuccessfully completed this CME quiz with a score of
The following questions were not answered correctly:
Commitment to Change (optional):
Indicate what change(s) you will implement in your practice, if any, based on this CME course.
Your quiz results:
The filled radio buttons indicate your responses. The preferred responses are highlighted
For CME Course: A Proposed Model for Initial Assessment and Management of Acute Heart Failure Syndromes
Indicate what changes(s) you will implement in your practice, if any, based on this CME course.
Submit a Response

Multimedia

Some tools below are only available to our subscribers or users with an online account.

Web of Science® Times Cited: 9

Related Content

Customize your page view by dragging & repositioning the boxes below.

Articles Related By Topic
Related Collections
PubMed Articles
JAMAevidence.com