Limitations: Risk factors studied limited to variables collected in screenee enrollment form.

Transcription

1 Risk factors for presumptive melanoma in skin cancer screening: American Academy of Dermatology National Melanoma/Skin Cancer Screening Program experience Matthew S. Goldberg, BA, a John T. Doucette, PhD, b HenryW.Lim,MD, c James Spencer, MD, d John A. Carucci, MD, PhD, e and Darrell S. Rigel, MD f New York, New York, and Detroit, Michigan Background: Since its inception in 1985, the American Academy of Dermatology (AAD) National Melanoma/Skin Cancer Screening Program has strived to enhance early detection of cutaneous malignant melanoma (MM) by providing nationwide skin cancer education campaigns in combination with free skin cancer screenings. Objective: To analyze the AAD screening data from 2001 to 2005 in order to identify factors associated with MM detection, and thereby derive a model of increased likelihood for MM detection through visual skin examinations at screenings. Materials and Methods: Patients completed a standardized AAD pre-screening form with historical and phenotypic information. Clinicians then recorded suspected clinical findings noted at visual skin examination. Statistical analyses were conducted using SPSS 14 (SPSS Inc., Chicago, Ill). Results: Five factors, which can be remembered with the acronym HARMM, independently increased the likelihood of suspected MM being found in the 362,804 persons screened: History of previous melanoma (odds ratio [OR] = 3.3; 95% confidence interval [CI], ); Age over 50 (OR = 1.2; 95% CI, ); Regular dermatologist absent (OR = 1.4; 95% CI, ); Mole changing (OR = 2.0; 95% CI, ); and Male gender (OR = 1.4; 95% CI, ). Individuals at highest risk (4 or 5 factors) comprised only 5.8% of the total population, yet accounted for 13.6% of presumptive MM findings, and were 4.4 times (95% CI, ) more likely to be diagnosed with suspected MM than individuals at lowest risk (0 or 1 factor). Receipt of a total skin examination at screening independently increased the likelihood for identifying suspected MM (OR = 1.4; 95% CI, ). However, significantly fewer screenees in the highest risk group versus those in the lowest risk group underwent total skin examinations (53.7% vs 62.5%). Limitations: Risk factors studied limited to variables collected in screenee enrollment form. Conclusions: A higher-risk subgroup of the skin cancer screening population can be identified through assessment of MM risk factors using the HARMM criteria. Refocusing efforts to provide a total skin examination to those individuals with multiple risk factors has the potential to both reduce costs and increase yields for suspected MM in future mass screening initiatives. ( J Am Acad Dermatol 2007;57:60-6.) From the Departments of Community and Preventive Medicine b and Dermatology, d Mount Sinai School of Medicine, a New York; Department of Dermatology, c Henry Ford Hospital, Detriot; Mohs Micrographic and Dermatologic Surgery, e Weill Medical College of Cornell University, New York; and the Department of Dermatology, f New York University Medical Center. Supported by a Mount Sinai School of Medicine Alumni Summer Research Fellowship awarded in May, 2006 to Matthew S. Goldberg. Conflicts of interest: None declared. Presented in both abstract and poster form on the 2006 Mount Sinai Medical Student Research Day, November 10, 2006, New York, New York. Reprints not available from the authors. Correspondence to: Darrell S. Rigel, MD, 35 East 35th St, Ste 208, New York, NY. darrell.rigel@gmail.com. Published online May 7, /$32.00 ª 2007 by the American Academy of Dermatology, Inc. doi: /j.jaad

2 JAM ACAD DERMATOL VOLUME 57, NUMBER 1 Goldberg et al 61 Although cutaneous malignant melanoma (MM) is one of the most preventable and treatable of cancers, the incidence of MM in the United States is currently rising a trend that will likely continue. 1-3 Current estimates project that 62,190 new cases of MM will be diagnosed in 2006, and that MM will be responsible for 7910 deaths during the same time period. 2 The direct and indirect costs associated with MM in 2004 reached an estimated $3.1 billion. 4 While population incidence remains low, at current rates, one in 52 men and one in 77 women will develop this invasive and potentially lethal cancer during their lifetime. 2 What is more, the burden of disease falls disproportionately on those at elevated risk, and often those at greatest risk for developing MM have the most rapidly increasing mortality rate. 5,6 The American Academy of Dermatology (AAD)e sponsored National Melanoma/Skin Cancer Screening Program (NMSP) began in 1985, and has now screened more than 1.6 million individuals for cancerous and precancerous skin lesions. 7 Created at a moment when dermatologists began to recognize both the increasing incidence of MM and the feasibility of national screening campaigns for cancer prevention, the program serves the dual purpose of educating the public and providing free skin exams to a self-selected group of at-risk individuals The accuracy of visual skin examinations conducted by dermatologists at mass screenings has been verified by histologic confirmation in previous analyses (positive predictive value [PPV] of histologically confirmed MM = %) Early detection is key to increased MM survival because prognosis strongly correlates with lesion thickness at initial biopsy. 17,18 Previous analyses of the AAD NMSP have shown that the AAD has succeeded in targeting individuals at above average risk for MM, and demonstrated that dermatologists were able to identify thinner MM lesions with improved 5-year mortalities. 11,18,19 Cost-benefit analysis grounded in such evidence has shown that the cost effectiveness of skin cancer screenings is comparable to other cancer screening initiatives when they take place for populations with higher than average prevalence of melanoma (prevalence $ 9 per 10,000). 20 Although the risk factors for MM are well documented, designing and implementing screening interventions that reach those at greatest risk remains a major challenge. 15,25-30 Advocates of mass screening for MM have focused on targeting individuals at elevated risk in order to increase yields of MM diagnosed among screenees and achieve cost effectivness Given the importance of early detection in MM, screening programs that successfully increase early detection could improve survival Other studies have proposed statistical models that identify MM risk factors and strategies to target high-risk population subsets in mass MM screening campaigns. 31,32,39,40 The total skin examination is a practical and effective screening tool for MM, applicable to the mass screening setting, 12,41 and the rising rates of MM on the trunk and lower extremities highlight the central role of a total skin examination in the identification of suspected MM. 42 The purpose of this analysis of the AAD NMSP data from 2001 to 2005 was therefore to identify a higher risk cohort for MM, and develop a clinical screening tool that could be used to enhance early MM detection in future mass screening initiatives by promoting the total skin examination among those at greatest risk for MM. MATERIALS AND METHODS Data used in this analysis were collected from the AAD NMSP screenings conducted between January 2001 and December Procedures for data collection followed protocols outlined in the previous studies of the NMSP. 18 Upon arrival at the screening site, screenees completed a 1-page form with basic demographic and MM risk related questions. A dermatologist then conducted the visual skin examination and all relevant clinical information was recorded by the physician. Screenees were informed that all diagnoses were presumptive, and that histologic confirmation would be necessary to confirm any of the suspected clinical findings identified in the visual skin examination. Data from the screenings were entered into an electronic database on a yearly basis. All statistical analyses were conducted using SPSS 14 software (SPSS Inc., Chicago, Ill). The primary data cleaning steps were as follows: (1) because of the age distribution of MM, those cases younger than 18 and older than 100 were excluded from the study; and (2) cases in which incoherent data were encountered for any single response were excluded from the study. We used x 2 tests to highlight statistically significant relationships, and all clinically relevant variables were entered into a multivariate stepwise logistic regression to predict for suspected MM. Variables identified in these models as the key MM risk factors were then utilized to stratify subjects into four melanoma risk groups by the number of corresponding MM risk factors that they had (0 to 1, 2, 3, or 4 to 5). Finally, the number of MM risk factors was entered into a univariate logistic regression to predict for suspected MM, and x 2 tests were once again used to evaluate relationships between groups within the dataset.

3 62 Goldberg et al JAM ACAD DERMATOL JULY 2007 Table I. Demographics and melanoma statistics Demographics % Total population* % Suspected melanoma* % Suspected MM by demographic y All valid 362, Gender Male Female Age (yr) Over Under Regular dermatologist Yes No Mole changing Yes No History of previous melanoma Yes No Race White Black/Hispanic/other Family history of melanoma Yes No Health insurance Yes No Skin type I/II Yes No risk factors risk factors risk factors risk factors *Values represent % of the total population in each demographic category. y Values represent % prevalence suspected MM in each demographic category. RESULTS There were 364,804 individuals between the ages of 18 and 100 at the time of their screening for whom there was valid data. The demographics of the screened population was similar to previous interval analyses of the AAD NMSP (Table I). 18 Of those screened, the following suspected clinical diagnoses were made: actinic keratoses (17.5%), non-melanoma skin cancer (7.6%), and MM (0.9%). The prevalence of suspected MM remained relatively stable across the 5 years studied, with rates ranging from 0.7% in 2003 to 1.2% in Although 32.9% of those screened had been to a previous skin cancer Table II. Variables included in multivariate logistic analysis Race Previous skin cancer Family history of melanoma Would see doctor without screening No health insurance Male gender* Regular dermatologist absent* History of previous melanoma* Mole changing* Age over 50* *Indicates inclusion in final melanoma risk models. screening, this population had a lower prevalence of suspected MM as compared to those who had never been to a screening before (0.85% vs 0.97%). Of those screened, 98.0% had at least a high school education, and 61.0% had a college education level or greater. Though women were more likely to go to screenings than men (61.8% of total screenees were women), they only accounted for 53.9% of the total suspected MMs identified. Even more striking, men over 50 comprised only 23.4% of the population yet accounted for 31.6% of the total suspected MM identified. The demographic variables that were significantly associated with suspected MM (P\.05), were entered into a stepwise logistic regression model to predict for this outcome (Table II). Designed to create an effective clinical screening tool, this modified stepwise logistic regression identified 5 variables as key MM risk factors based on measures of statistical significance, clinical relevance, and acceptable levels of missing data (n = 310,967 with 0.9% suspected MM). The five variables included in the resulting MM risk model can be summarized by the acronym HARMM: History of previous melanoma (odds ratio [OR] = 3.3; 95% confidence interval [CI], ); Age over 50 (OR = 1.2; 95% CI, ); Regular dermatologist absent (OR = 1.4; 95% CI, ); Mole changing (OR = 2.0; 95% CI, ); and Male gender (OR = 1.4; 95% CI, ). The adjusted ORs did not differ appreciably from the unadjusted ORs (Table III). After stratification of data into MM risk factor groups by categorizing each case as holding 0 to 1, 2, 3, or 4 to 5 risk factors, the data was reanalyzed to evaluate the association between the number of risk factors present and suspected MM. These risk factors were widely held across the study population as 98% had at least one risk factor, 75.4% had two or more risk factors, 32.7% had three or more risk factors, and 5.8% had four or five risk factors. Prevalence of suspected MM significantly increased in each

4 JAM ACAD DERMATOL VOLUME 57, NUMBER 1 Goldberg et al 63 Table III. HARMM melanoma risk model Melanoma univariate analyses OR (95% CI)* Melanoma multivariate analysis adjusted OR (95% CI)* History of previous 3.5 ( ) 3.3 ( ) melanoma Age over ( ) 1.2 ( ) Regular dermatologist 1.3 ( ) 1.4 ( ) absent Mole changing 2.0 ( ) 2.0 ( ) Male gender 1.4 ( ) 1.4 ( ) Total valid cases = 334,422; total valid melanoma = *All P values \.001. subsequent MM risk group (x 2 test for trend = 522.4; P \.001). 43 Having additional risk factors corresponded to a significantly increased likelihood of suspected MM (Table IV). Specifically, an individual with four or five melanoma risk factors was 4.4 times more likely to be diagnosed with suspected MM at a skin cancer screening than an individual with zero or one MM risk factor. Those who received a total skin examination during the screening were more likely to be diagnosed with suspected MM than an individual who received a specific lesion or a face and arms examination (OR = 1.4; 95% CI, ). In addition, the prevalence of suspected MM among patients who received a total skin examination was higher than that of patients who received other exams for every MM risk group (Table V). However, there was a decrease in the proportion of total skin examinations given to each group of subsequently higher risk patients, as only 53.7% of those with four or five risk factors received total skin examination, compared with 62.5% of those with zero or one risk factors (Table VI). DISCUSSION The purpose of mass screening initiatives for MM is to enhance early detection and identify suspicious lesions at the time when MM is most effectively treatable. The development of the HARMM risk assessment model from the 2001 to 2005 AAD NMSP data is an attempt to reach that goal by enabling clinicians to quickly gauge the MM risk of patients who present to skin screenings. The five risk factors for suspected MM identified in this study (history of previous melanoma, age over 50, regular dermatologist absent, mole changing, and male gender) have an order of magnitude consistent with an analysis of AAD data from a previous Table IV. Final regression model and likelihood statistics Melanoma univariate analysis OR (95% CI)* 0-1 risk factors risk factors 1.7 ( ) 3 risk factors 2.5 ( ) 4-5 risk factors 4.4 ( ) Total valid cases = 334,422; total valid melanoma = *All P values \.001. Table V. Melanoma prevalence % in risk groups by exam type Total skin examination prevalence (%) Specific lesion prevalence (%) Face and arms prevalence (%) All valid risk factor risk factors risk factors risk factors Total valid cases = 240,753; total valid melanoma = 2308, or 0.96%. interval. 31 Although the AAD NMSP continues to screen self-selected individuals who are at elevated risk for suspected MM, the identification of higher risk cohorts within the general screening population may help to improve rates of MM detection. In the integrated HARMM model, each additional risk factor confers a statistically significant increase in the likelihood of suspected MM identification through visual skin examination. The ease of determining these factors in an individual screenee validates the potential clinical viability of the proposed HARMM model. Of note, the data from this study suggest that not having a regular dermatologist independently increases the likelihood of suspected MM detection at skin cancer screening. While studies have shown that physicians diagnose thinner lesions than do their patients alone, 33,44 it has also been demonstrated that dermatologists have a greater diagnostic accuracy for pigmented lesions than do primary care physicians and that dermatologic involvement in MM patient management led to significantly improved survival. 45,46 In light of these past studies, the findings from this paper strengthen the evidence that having a regular dermatologist may be protective in the clinical management of MM. The type of exam conducted in screenings independently influenced the number of suspected MMs identified. Even after controlling for the

5 64 Goldberg et al JAM ACAD DERMATOL JULY 2007 Table VI. Exam type breakdown by risk factor % of Total % With 0-1 % With 2 % With 3 % With 4-5 population risk factor risk factors risk factors risk factors Exam Type n = 240,753 n = 82,301 n = 142,787 n = 89,805 n = 19,529 Total skin examination Face and arms Specific lesion melanoma risk groups, those who received a total skin examination were more likely to have suspected MM than were individuals who received other available screening exams. However, there was an inverse relationship between the rate of total skin examination and the level of individual MM risk (Table VI). This observed trend is troubling, and indicates an area where risk targeting can have an impact on patient care and mass screening cost efficacy. The findings of this study were limited to the MM risk factors for which data was collected from 2001 to Efforts can be made to utilize the AAD NMSP to collect data on screenees for other known and newly proposed risk factors for MM. More specific information on hair color, eye color, a simple scale for number of nevi, and history of sunburn may help to better classify the risk of future screenees. In addition, recent studies have suggested that use of artificial tanning booths may be an important predictor of MM in certain populations. 35,47-49 Mass screening data related to this specific risk behavior may better assess the direct impact of tanning on MM risk. Another limitation of the data set used for this study is its reliance on presumptive clinical assessments made through visual skin examination without histopathological confirmation. However, it is possible to use the experience of past studies to extrapolate confirmed MM prevalence from the suspected MM prevalence of 91.7 per 10,000 observed during 2001 to Assuming that the visual skin examination in the current screening yielded a PPV $ 9.8%, the prevalence of MM among all screenees would still exceed the minimum level required to achieve the established cost efficacy threshold for MM screening. 20 Among those individuals at highest risk, the prevalence of suspected MM reached per 10,000, and a PPV $ 4.2% would be sufficient to reach the same threshold. However, if the PPV was identical to the most recent experience with the NMSP (PPV = 17.0%), 11 then the prevalence of confirmed MM in the screening population would have reached 15.6 confirmed MM per 10,000 overall, with rates as high as 36.0 confirmed MM per 10,000 among those in the highest risk group. Critics have suggested that the lack of prospective studies undermines the validity of the entire cost effectiveness debate for MM screening. 50 The US Preventive Services Task Force does not currently recommend a total skin examination as part of routine skin cancer prevention for those at average risk of developing MM While it is beyond the scope of this paper to re-evaluate the metrics used to develop cost efficacy models for MM, given the application of modest PPV estimates from previous MM confirmation studies, the suspected MM prevalence data from 2001 to 2005 suggest that the AAD mass skin cancer screenings are currently conducted at a cost comparable to other routine cancer screening strategies. 20 This study also reinforces the contention that further savings might be possible through efforts to both sharpen the risk targeting of screening populations and to encourage total skin examinations for those with multiple MM risk factors. CONCLUSIONS This is the first study to our knowledge that has attempted to produce a model designed to help clinicians best screen those at greatest risk among individuals who present to free screening initiatives. Through the application of the simple clinical checklist derived from this study, clinicians may improve the yield of presumptive MM detection in future mass screenings and may minimize the HARMM from missed MMs. The total skin examination should be strongly encouraged for those individuals who have multiple MM risk factors to increase the likelihood of MM detection among screening participants. REFERENCES 1. Bevona C, Sober AJ. Melanoma incidence trends. Dermatol Clin 2002;20: Jemal A, Siegel R, Ward E, Murray T, Xu J, Smigal C, et al. Cancer statistics, CA Cancer J Clin 2006;56: 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:

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7 66 Goldberg et al JAM ACAD DERMATOL JULY Hall HI, Miller DR, Rogers JD, Bewerse B. Update on the incidence and mortality from melanoma in the United States. J Am Acad Dermatol 1999;40: Campbell M, Swinscow TDV. Statistics at square one (9th ed). London: BMJ Publishing Group; Epstein DS, Lange JR, Gruber SB, Mofid M, Koch SE. Is physician detection associated with thinner melanomas? JAMA 1999; 281: Chen SC, Pennie ML, Kolm P, Warshaw EM, Weisberg EL, Brown KM, et al. Diagnosing and managing cutaneous pigmented lesions: primary care physicians versus dermatologists. J Gen Intern Med 2006;21: McKenna DB, Marioni JC, Lee RJ, Prescott RJ, Doherty VR. A comparison of dermatologists, surgeons and general practitioners surgical management of cutaneous melanoma. Br J Dermatol 2004;151: Lim HW, Gilchrest BA, Cooper KD, Bischoff-Ferrari HA, Rigel DS, Cyr WH, et al. Sunlight, tanning booths, and vitamin D. J Am Acad Dermatol 2005;52: Chen YT, Dubrow R, Zheng T, Barnhill RL, Fine J, Berwick M. Sunlamp use and the risk of cutaneous malignant melanoma: a population-based case-control study in Connecticut, USA. Int J Epidemiol 1998;27: Buckel TB, Goldstein AM, Fraser MC, Rogers B, Tucker MA. Recent tanning bed use: a risk factor for melanoma. Arch Dermatol 2006;142: Helfand M, Mahon SM, Eden KB, Frame PS, Orleans CT. Screening for skin cancer. Am J Prev Med 2001;20(3 suppl): U.S. Preventive Services Task Force. Counseling to prevent skin cancer: recommendations and rationale of the U.S. Preventive Services Task Force. MMWR Recomm Rep 2003; 52(RR-15): Berg AO. Counseling to prevent skin cancer: recommendations and rationale. Am J Nurs 2004;104: US Preventive Services Task Force: Berg AO, Allan JD, Frame PS, Homer CJ, Lieu TA, Mulrow CD, et al. Screening for skin cancer: recommendations and rationale. Am J Nurs 2002; 102: AMERICAN BOARD OF DERMATOLOGY EXAMINATION DATES In 2007, the Certifying Examination of the American Board of Dermatology (ABD) will be held at the Crowne Plaza Chicago O Hare in Rosemont, Illinois, on August 13, 2007 (one day examination). The deadline for receipt of applications is March 1, A future examination will take place on August 11, 2008 in Rosemont, Illinois. The Recertification Examination of the ABD will be administered online between May 1 and June 12, The deadline for receipt of applications for the Recertification Examination is December 15, A future examination will take place from May 1 to June 12, The examination for subspecialty certification in Dermatopathology will be administrated September 17, 2007 at the testing center of the American Board of Pathology in Tampa, Florida. The deadline for receipt of applications is May 1, Dermatologists must submit applications to the ABD and pathologists to the American Board of Pathology. The examination for subspecialty certification in Pediatric Dermatology will next be administered in The deadline for receipt of applications is April 1, Date and location to be determined. The In-Training Examination for Dermatology residents (administered online at dermatology residency training centers in the United States and Canada) will be held on April 19, Deadline for receipt of applications if February 1, A future examination will take place on April 17, For further information about these examinations, please contact the ABD office (address and phone/fax numbers below) or check the ABD Web site at Antoinette F. Hood, M.D. Executive Director, American Board of Dermatology Henry Ford Health System 1 Ford Place Detroit, MI Telephone: (313) Fax: (313) abderm@hfhs.org