Annals of Medicine

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Melanoma screening: A plan for improving early

detection

Richard Shellenberger, Mohammed Nabhan & Sweta Kakaraparthi

To cite this article: Richard Shellenberger, Mohammed Nabhan & Sweta Kakaraparthi (2016)
Melanoma screening: A plan for improving early detection, Annals of Medicine, 48:3, 142-148,
DOI: 10.3109/07853890.2016.1145795

To link to this article: https://doi.org/10.3109/07853890.2016.1145795

Published online: 25 Feb 2016.

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ANNALS OF MEDICINE, 2016
VOL. 48, NO. 3, 142–148
http://dx.doi.org/10.3109/07853890.2016.1145795

REVIEW ARTICLE

Melanoma screening: A plan for improving early detection

Richard Shellenberger, Mohammed Nabhan and Sweta Kakaraparthi
Internal Medicine Department, St. Joseph Mercy Hospital, Ann Arbor, MI, USA

ABSTRACT ARTICLE HISTORY

Malignant melanoma ranks fifth in the number of new cases annually in the United States (US). Received 7 November 2015
Despite increasing incidence and lack of recent improvement in mortality, national melanoma Revised 7 January 2016
screening guidelines are currently not in existence. Our purpose was to review the evidence Accepted 19 January 2016
regarding screening whole-body skin examinations for early detection and a possible mortality Published online 24 February
2016
benefit for malignant melanoma. Data sources for our review were MEDLINE Complete, PubMed,
Cochrane Library, Cochrane Database of Systematic Reviews, and ClinicalTrials.gov. Study selection KEYWORDS
included: epidemiologic data from the US and European cancer surveillance registries, popula- Malignant melanoma
tion-based case-control screening trials, computer-simulated Markov model trials, and survey tri- epidemiology; whole-body
als. Studies were limited to those published in the English language. Data was extracted using a skin examination; early
dual extraction method. Data from studies have shown that the mortality of malignant melanoma detection improves
is highly predicated on the tumor thickness at the time of diagnosis. Our data review is in sup- outcomes; primary care
port of the implementation of whole-body skin examinations, performed by primary care physi- awareness; resident
cians, for the purpose of early detection of melanoma. A large national population-based, case- education
control, skin cancer screening trial in Germany has shown a reduction in melanoma-specific mor-
tality. In conclusion, our review of the evidence supports physicians performed whole-body skin
examination can lead to the detection of earlier stage melanomas as well as to a reduction in dis-
ease-specific mortality. We found a paucity of randomized trials to be a limitation of screening
studies for many cancers, including melanoma. To improve screening rates and early detection of
malignant melanoma, we propose making skin cancer education part of the curriculum in US pri-
mary care residency programs to become the genesis for widespread melanoma screening. Our
study had no funding.

ä KEY MESSAGES
 Malignant melanoma is the fifth leading cancer in the United States (US).
 In the US and many countries worldwide, the incidence and mortality rates have not
declined despite advances seen in the detection and treatment of many cancers.
 Whole-body skin examination is non-invasive and has shown to be cost effective.
 There is evidence supporting a mortality benefit using routine, widespread skin cancer
examinations.
 Primary care physicians have been shown to effectively use skin cancer examination for early
detection and reduced melanoma mortality.
 The majority of US primary care residents are inadequately trained in skin cancer
examination.
 There is a possible survival advantage and cost effectiveness for melanoma screening.

Introduction past three decades (2). We have seen a threefold

increase in melanoma cases since 1975 and current
The purpose of our review is to examine the status of lifetime risk for Americans is 1:48 (3). With current
current evidence and trends in malignant melanoma advances in cancer detection and treatment, the mor-
screening as practiced in the United States (US). tality rates for many cancers have decreased; however,
Melanoma ranks fifth in a number of new cases annu- such a decline has not been seen for melanoma. In
ally in this nation (1). Of the seven most common US fact, melanoma is one of only three cancers in which
cancers, only melanoma’s incidence continues to rise, the mortality in men is rising (4,5). In respect to a num-
and both incidence and mortality rates throughout ber of new cases and death rates, melanoma compares
most of the developed world have increased over the closely with combining cervical and endometrial

CONTACT Richard Shellenberger richard.shellenberger@stjoeshealth.org Internal Medicine Department, St. Joseph Mercy Hospital, Suite 3009, 5333
McAuley Dr, Ypsilanti, Ann Arbor, MI 48197, USA
ß 2016 Informa UK Limited, trading as Taylor & Francis Group
 ANNALS OF MEDICINE 143

cancers in the US. Yearly incidence of melanoma in controlled trials (2,14–18). Mortality benefits of screen-
both sexes and all races is only 20% lower than ing for distal colon cancer from randomized controlled
cancers of the colon and rectum. Current screening trials have been shown with sigmoidoscopy and not
rates in the US for cancers of the cervix, endometrium, for colonoscopy (15). Interestingly, mortality has
colon, rectum, breast, and prostate are much higher declined substantially for these five cancers over the
than those for malignant melanoma (5). past several decades. Is there an opportunity for a
The growth in melanoma incidence in the US has similar decline in melanoma mortality by instituting
been seen particularly in men over 50. Since 1975, our more widespread screening?
incidence in men has doubled in age 50–59, quad- The US Preventative Services Task Force (USPSTF)
rupled in age 60–69 and risen sevenfold in age over in 2009 published a review of the evidence and
80 (2). These middle-aged and older men average recommendations for skin cancer screening (19).
between three and four visits to their primary care The conclusion stated the current evidence was
doctors yearly, providing an opportunity for screening. insufficient to assess the balance of benefits and
Mortality in melanoma is best predicted by the thick- harms of using whole-body skin examinations by
ness of cancer and regional spread at the time of diag- primary care clinicians for the early detection of
nosis. Physician examinations detect melanomas of less cutaneous melanoma. Recognizing the importance
thickness and thus lower stages when compared of melanoma, the USPSTF prioritized a 2015 Draft
with patient self-examinations. Stage 1 disease (tumor Recommendation Statement (20). Once again, they
thickness of less than 1 mm) is found by physician concluded the current evidence is insufficient to
examinations 67% as compared with 33% by patient’s support skin cancer screening. This was largely due
self-examination (6). to the lack of randomized controlled trials to
Are primary care physicians looking at their evaluate the efficacy of whole-body skin examin-
patient’s skin? (7) Melanoma screening has not been ation. A proposal by Geller, to perform a random-
adopted as a mainstream practice with fewer than ized study of melanoma screening in the US
25% of Americans report having received a skin exam- would take approximately 12 years, with over one
ination (8–12). However, patients are thinking about million patients at a cost of up to $40 million dol-
skin cancer. University of Texas, MD Anderson lars (21). We will discuss the results from the most
Cancer Center has developed a program, called the impactful studies which were not a part of the
Moon Shots Program, in which they have outlined database used for the USPSTF 2009 clinical guide-
plans to quickly improve the survival rates for some lines. The challenge to impact the mortality of
of the deadliest cancers. Melanoma is one of the malignant melanoma by the implementation of rou-
seven cancers targeted in this program. When asked tine melanoma screening remains a daunting task.
which Moon Shots Program patients were excited Our aim is to improve skin cancer examination
about, melanoma ranked second behind breast cancer (SCE) education in our primary care residency pro-
and ahead of lung cancer (13). The National Cancer grams with the goal of heightened early detection
Institute, as well as other organizations also has initia- of this disease.
tives to lower melanoma mortality through early
detection.
Methods
The standard and most accepted method for melan-
oma screening is the whole-body skin examination. To begin our narrative review, we searched MEDLINE
This non-invasive screening examination is performed Complete, PubMed, Cochrane Library, Cochrane
much less frequently than examinations screening for Database of Systematic Reviews, and ClinicalTrials.gov
colorectal, breast, prostate, cervical, and endometrial database from April 13 to September 9, 2015. We com-
cancers in the US (15–18). In our review of the current bined the following keywords in our searches: melan-
evidence, there is a lack of strong evidence from oma, melanoma detection, skin cancer, skin
randomized controlled trials showing significant mor- examination, mortality, cost-effectiveness, primary care,
tality benefit for screening for any of these later five internal medicine residency, family medicine residency,
malignancies. Despite the paucity of evidence, the rate skin examination education. The list of references from
of screening for all five of these cancers is much identified sources was searched to find additional rele-
higher than for skin cancers (14). National Cancer vant studies. Cohort and case-controlled trials were
Institute data from 2013 shows that 58.8% of US evaluated based on the Newcastle-Ottawa Quality
patients 50–75 have received colorectal cancer screen- Assessment Tool (22) See Table 1 for the Quality
ing despite the lack of evidence from randomized Assessment Worksheet.
144 R. SHELLENBERGER ET AL.

Table 1. Assessment of data quality worksheet

Aitken Swetter Breitbart Schneider
et al. (24) et al. (25) et al. (26) et al. (23)
1. Was the research question or objective in this paper clearly stated? Y Y Y Y
2. Was the study population clearly specified and defined? Y Y Y Y
3. Was the participation rate of eligible persons at least 50%? Y Y N NA
4. Were all the subjects selected or recruited from the same or similar populations (including Y Y Y Y
the same time period)? Were inclusion and exclusion criteria for being in the study pre-
specified and applied uniformly to all participants?
5. Was a sample size justification, power description, or variance and effect estimates N N N N
provided?
6. For the analyses in this paper, were the exposure(s) of interest measured prior to the out- N NA NA Y
come(s) being measured?
7. Was the timeframe sufficient so that one could reasonably expect to see an association Y N N Y
between exposure and outcome if it existed?
8. For exposures that can vary in amount or level, did the study examine different levels of NA NA NA NA
the exposure as related to the outcome (for example, categories of exposure or exposure
measured as continuous variable)?
9. Were the exposure measures (independent variables) clearly defined, valid, reliable, and Y Y Y Y
implemented consistently across all study participants?
10. Was the exposure(s) assessed more than once over time? N N N N
11. Were the outcome measures (dependent variables) clearly defined, valid, reliable, and Y Y Y Y
implemented consistently across all study participants?
12. Were the outcome assessors blinded to the exposure status of participants? N N N N
13. Was loss to follow-up after baseline 20% or less? N NR NR NR
14. Were key potential confounding variables measured and adjusted statistically for their Y Y NR Y
impact on the relationship between exposure(s) and outcome(s)?
Y: yes; N: no; NA: not applicable; NR: not reported.

Results A 2010 Australian population-based, case-control

trial also reported evidence for physician whole-body
Our main objective was to find evidence which sup-
skin examination which correlated with finding thinner
ported the following three premises. First, can whole-
melanomas (24) Telephone interviews were conducted
body skin examinations detect malignant melanoma at
with Queensland residents aged 20–75 years with a
an earlier stage or thinner Breslow thickness? The
histologically confirmed first primary invasive cutane-
Breslow thickness is the standard measured of tumor
ous melanoma diagnosed during a 3-year period, with
thickness used for staging of melanoma. Second, can
employment of routine whole-body skin examinations 3762 cases and 3824 controls receiving telephone
reduce the mortality of malignant melanoma? And interviews. Whole-body skin examination in the 3 years
finally, can periodic whole-body skin examinations per- prior to diagnosis was associated with a 14% lower risk
formed for melanoma screening be cost effective? of being diagnosed with a melanoma thicker than
A community-based screening program and the 0.75 mm (OR ¼ 0.86, 95 CI: 0.75–0.98) and by 40% for
educational campaign were conducted with employees melanomas 3 mm (OR ¼ 0.60, 95% CI: 0.43–0.83). The
of Lawrence Livermore National Laboratory in screening was associated with a 38% higher risk of
California (23). This was a three-phase trial, published being diagnosed with a thin invasive melano-
in 2008, which included a pre-awareness period ma 0.75 mm (OR ¼ 1.38, 95% CI: 1.22–1.56).
(1969–1975); early awareness of increased melanoma In 2012, Swetter et al. (25) published a community-
risk (1976–1984), and screening program (1984–1996). based survey study by having 566 patients with inva-
In this screening trial, crude incidence of melanoma sive melanoma complete a questionnaire within 3
thicker than 0.75 mm decreased during the three peri- months of their diagnosis. The questionnaire evaluated
ods from 22.1 to 15.3 to 4.62 cases per 100,000 person demographics, health care access, self-skin examination
years (p ¼ 0.001). The largest decrease was found in (SSE), and physician skin examination (PSE). For our
the screening program. No mortality was seen in the purpose, the most important attribute of this study
screening period, whereas the expected number of was the finding of thinner melanomas in those
deaths was calculated to be 3.39 (p ¼ 0.034). The edu- patients who had undergone a whole-body skin exam-
cation, self-examination, and screening program gener- ination by a physician in the year prior to the diagno-
ated the largest reduction of melanoma thicker than sis of melanoma. Whole-body PSE was associated with
0.75 mm in this study group. Of note, this study was melanoma less than 1 mm in thickness (OR: 2.51: 95%
not included in the 2009 USPSTF update on skin can- CI: 1.62–3.87) and particularly in men older than age
cer screening (19). 60 (OR: 4.09, 95% CI: 1.88–8.99). In this study, thinner
 ANNALS OF MEDICINE 145

tumors were also associated with age <60 years, national health plan to adopt a widespread screening
women, higher education levels, and use of melanoma program; however, this trial did not evaluate cost
picture aids along with SSE. effectiveness.
The best evidence to date to validate melanoma
screening comes from the largest population-based
Discussion
skin cancer screening project in the world. In 2003, the
German Association of Dermatological Prevention Based on the results of SCREEN, Germany has adopted
implemented the Skin Cancer Research to Provide a nationwide melanoma screening which includes
Evidence for Effectiveness of Screening in Northern whole-body skin exams every 2 years. It should also be
Germany (SCREEN) project (26). After a 2-year public noted, the incidence of melanoma in Germany is
campaign for skin cancer awareness, 360,288 patients approximately 71% of that in the US (1,4). Data from
older than 20 years, living in the German state of the first 5 years of this program has been recently
Schleswig-Holstein, received a visual whole-body skin published as Skin Cancer Screening in Germany (28).
examination. Melanoma mortality rates were compared The mortality benefit was seen in the pilot study (27)
before and after screening in the same locale as well was not seen in this arm of the trial. These confound-
as matched non-screened areas elsewhere in Germany. ing results may be explained by the lack of the poten-
All participating physicians (dermatologists, general tial effects of the public education campaign used in
practitioners, gynecologists, internists, surgeons, and the initial trial along with possible differences in the
urologists) were required to attend an 8-h training intensity and quality of the performed screening.
course designed to standardize a visual, whole-body Patient selection bias, the time interval of screening,
skin examination for the purpose of screening for skin and difficulties with dermatology referrals were also
cancers. Most remarkably, this study, employed non- suggested as possible factors affecting the quality of
dermatologist physicians for a majority (77%) of the screening.
initial whole-body skin examinations, while demon- Many suggest we need to replicate this data in the
strating a 47% and 49% respective reduction in mortal- US before adopting a similar screening program and to
ity in men and women. This study also found a 23% further assess for cost effectiveness and benefits
increase in finding Stage 1 melanoma (thick- weighed against the risk of harm. Evidence on harms
ness <1 mm). This resulted in the German Federal Joint for melanoma screening is limited (29,30). The majority
Committee including skin cancer screening as part of of skin biopsies are benign. Cosmetic, functional, or
the nationwide services provided by their Health psychological adverse effects may occur although
Insurance Fund. The study has been expanded to all there are few data available on the frequency or spe-
Germans over the age of 35. Since 2008, 20 million cifics of these adverse effects. Over diagnosis and over
people had been screened and nearly 45,000 physi- treatment are also potentials for harm, but research is
cians had received the training. In contrast to the pilot limited to estimate the potential burden of these fac-
study, mortality data from 2008 to 2013, for malignant tors in the case of skin cancer (20).
melanoma, has not declined in this arm of the SCREEN Far from any conclusions, we do know we have
trial (27). work to do to make an impact on malignant melan-
The next question necessary in the evaluation of oma in this country. We feel the evidence supports a
melanoma screening is cost effectiveness. There benefit for melanoma screening which is at least as
have been several studies, which vary widely in their good as the evidence for many other cancers for
design, due to the selection of patient cohorts. In the which well-established screening practices already
US, Losina et al. (28) performed a cost-effectiveness exist. Our present goal is to heighten public and pro-
analysis to evaluate the impact of melanoma screening fessional awareness and improve the current screening
in the general population as well as high-risk popula- rate, with the ultimate aim to help establish new
tions. They observed an incremental cost-effectiveness guidelines. Identifying patients at high risk of develop-
ratio of $10,100/quality-adjusted life year (QALY) for a ing melanoma is particularly important for Caucasian
one-time screening of the general population older men over age 50 as they have a higher risk of dying
than age 50. They found screening every 2 years in from this disease (25,31,32). Other risk factors, such as
siblings of patients with melanoma resulted in a cost- personal history of melanoma, first-degree relative with
effectiveness ratio of $35,500/QALY. These authors melanoma, presence of >40 nevi at least 2 mm in
concluded these to be cost-effective screenings as diameter, congenital and clinically atypical nevi, and
compared with other cancers screening programs. evolving nevi, should also warrant more frequent
The results of the SCREEN study led to the German screening.
146 R. SHELLENBERGER ET AL.

As outlined above, evidence exists for PSE identify- been accomplished with the aid of a national health
ing melanoma which is thinner and indicates a more care system which mandates physician participation. A
favorable prognosis. We have also gained new insight similar program would be difficult to duplicate in the
into patient education and screening programs having US given differences in health care systems. Therefore,
a potential impact on improving the mortality of this the approach necessary is to implement education for
cancer. Patients do go to their primary care physicians SCE in our primary care residency training programs. In
with concerns about their skin. In the Rochester the past, clinical training for SCE has been infrequently
Epidemiology Project, the Mayo Clinic studied 142,377 taught in US primary care residents in a survey of four
Olmsted County residents over a 4-year period. The residency programs (42). During their residency, 75.8%
researchers found skin disorders were the number one were never trained in SCE, 55.3% never observed an
reason for physician visits (33). An obvious disparity, SCE and 57.4% never practiced the examined. It was
given the alarming statistic of less than 25% of not surprising that only 15.9% of residents reported
Americans report having received a skin examination being skilled in SCE. Educating primary care residents
(9–12). The average American goes to their primary in whole-body skin examinations is the first step in
physician almost twice yearly and the rate doubles in enhancing melanoma screening in the US. In our insti-
the middle-aged and older population, with its higher tution, we aim to develop a uniform and generalizable
melanoma incidence (34). curriculum for the internal medicine residency program
Our challenge is to engauge – not to impugn – US in collaboration with dermatology, which can be
primary care physicians. Existing barriers must be extended to primary care residency programs nation-
examined and overcome, which exist and result in wide. This could lead to the genesis of widespread
such a low rates of skin examinations by our nation’s melanoma screening in the US.
physicians. Combined, there are >300,000 practicing
family practitioners and internists in the US (35,36)
Conclusion
With less than 10,000 dermatologists currently practic-
ing, a combined effort between primary care and Given the alarming epidemiology of malignant melan-
dermatology will be necessary to accomplish more oma, we conclude it is necessary to improve screening
widespread screening. In the SCREEN study, primary practices for early detection in the US and many other
care physicians performed most of the initial skin countries. Prevention and early detection may have
examinations and dermatology performed most of the the largest impact to improve the unfavorable trend in
diagnostic evaluations and skin biopsies. This is similar incidence as well as mortality. Our review, focusing on
to the US, where primary care physicians perform less data published since the USPSTF original 2009 recom-
than 13% of the initial biopsies for melanoma (37) mendations (19) on skin cancer screening, warrants fur-
Dermoscopy may further assist in the accuracy of their ther discussion and evaluation for future guidelines.
skin examinations. Evidence supports primary care We do note a limitation in advocating for melanoma
physicians using dermoscopy improves the sensitivity screening is the lack of high-quality evidence from
of the diagnosis of melanoma and reduces the number randomized controlled trials. The authors of SCREEN
of excisions of benign lesions (38,39). The Optoderma intended on randomization but were not permitted by
study was a randomized clinic trial of Dutch primary the German government. As we noted above screen-
care physician using dermoscopy for suspected malig- ing practices of many other cancers are much more
nant lesions. Researches in this study found the cost- widely practiced in the US, despite the lack of high-
effectiveness for dermoscopy was e89 per each cor- quality supporting evidence for efficacy. Ethical and
rectly diagnosed patient (38). The implementation of practical reasons may limit the ability to conduct
dermoscopy should be considered in future trials, as randomized controlled studies evaluating the effective-
both data and expert opinion suggest its importance ness of cancer screening. Detection of earlier stage
in skin cancer diagnosis. melanomas and the possible reduction in mortality,
Barriers to skin examination need to be identified with the use of whole-body skin examinations, is sup-
and broken. Time, competing comorbidities, patient ported by recent population-based and case-control
embarrassment, and lack of exposure to SCE have trials. Whole-body skin examination is non-invasive and
been identified as the most common barriers (40,41). has been shown to be cost effective. Improving the
Of these barriers, the lack of exposure to the skin mortality of any cancer is complex with many chal-
examination is the one most amenable to change. In lenges. One of the most difficult challenges we face is
Germany, the SCREEN program has now educated the courage to implement change. For malignant mel-
>95% of physicians chosen to participate. This has anoma, change is paramount in achieving success in
 ANNALS OF MEDICINE 147

the prevention, early detection, and mortality of this cancer screening practice and attitudes in primary care.
cancer. J Am Acad Dermatol. 2007;57:775–81.
15. Brenner H, Stock C, Hoffmeister M. Effect of screening
sigmoidoscopy and colonoscopy on colorectal cancer
Disclosure statement incidence and mortality: systematic review and meta-
analysis of randomized controlled trails and observa-
The study received no funding. The authors report no tional studies. BMJ. 2014;348:g2467.
declaration of interest. 16. Ko€sters JP, Gøtzsche PC. Regular self-examination or
clinical examination for early detection of breast can-
cer. Cochrane Database Syst Rev 2003;2:CD003373.
References 17. Djulbegovic M, Beyth RJ, Neuberger MM, Stoffs TL,
1. SEER Cancer Statistics Review, 1975–2010, National Vieweg J, Djulbegovic B, et al. Screening for prostate
Cancer Institute. Bethesda, MD. Available from: http:// cancer: systematic review and meta-analysis of rando-
seer.cancer.gov/csr/1975_2010. mised controlled trials. BMJ. 2010;341:c4543.
2. Jemal A, Saraiya M, Patel P, Cherala SS, Barnholz-Sloan 18. Raffle AE, Alden B, Quinn M, Babb PJ, Brett MT.
J, Kim J, et al. Recent trends in cutaneous melanoma Outcomes of screening to prevent cancer: analysis of
incidence and death rates in the United States, cumulative incidence of cervical abnormality and mod-
1992–2006. J Am Acad Dermatol. 2011;65:S17–25.e3. elling of cases and deaths prevented. BMJ.
3. Kohler BA, Sherman RL, Howlader N, Jemal A, Tyerson 2003;326:901.
AB, Henry KA, et al. Annual report to the nation on the 19. Wolff T, Tai E, Miller T. Screening for skin cancer: an
status of cancer, 1975–2011, featuring incidence of update of the evidence for the U.S. Preventive Services
breast cancer subtypes by race/ethnicity, poverty, and Task Force. Ann Intern Med. 2009;150:194–8.
state. J Natl Cancer Inst. 2015;107:djv048. doi: 10.1093/ 20. Draft recommendation statement. Skin cancer screen-
jnci/djv048. ing. U.S. Preventative Services Task Force. November
4. World Health Organization, International Agency for 2015. htp://www.uspreventiveservicestaskforce.org/
Research on Cancer. GLOBOCAN 2008. Cancer Page/Document/draft-recommendation-statement168/
Incidence and Mortality Worldwide in 2008 April 14, skin-cancer-screening2. Accessed 12/23/15.
2015; Available at http://iarc.fr/eucan. 21. Geller AC. Educational and screening campaigns to
5. American Cancer Society. Cancer facts and figures reduce deaths from melanoma. Hematol Oncol Clin
2011. Available at http://www.cancer.org/acs/groups/ North Am. 2009;23:515–27.
content/@epidemiologysurveilance/documents/docum- 22. Deeks JJ, Dinnes J, D’Amico R, Sowden AJ, Sakarovitch
net/acspc-031941.pdf. Accessed April 15, 2015. C, Song F, et al. Evaluating non-randomised interven-
6. Geller AC, Johnson TM, Miller DR, Brooks KR, Layton CJ, tion studies. Health Technol Assess. 2003;7:iii–x, 1–173.
Swetter SM. Factors associated with physician discovery 23. Schneider JS, Moore DH 2nd, Mendelsohn ML.
of early melanoma in middle-aged and older men. Screening program reduced melanoma mortality at the
Arch Dermatol. 2009;145:409–14. Lawrence Livermore National Laboratory, 1984 to 1996.
7. Terushkin V, Halpern AC. Melanoma early detection. J Am Acad Dermatol. 2008;58:741–9.
Hematol Oncol Clin North Am. 2009;23:481–500, viii. 24. Aitken JF, Elwood M, Baaden PD, Youl P, English D.
8. Shellenberger R. Making a case for melanoma screen- Clinical whole-body skin examination reduces the inci-
ing: look, listen and feel. J Family Med Prim Care. dence of thick melanomas. Int J Cancer.
2015;4:19–20. 2010;126:450–8.
9. Coups EJ, Geller AC, Weinstock MA, Heckman CJ, 25. Swetter SM, Pollitt RA, Johnson TM, Brooks DR, Geller
Manne SL. Prevalence and correlates of skin cancer AC. Behavioral determinants of successful early melan-
screening among middle-aged and older white adults oma detection: role of self and physician skin examin-
in the United States. Am J Med. 2010;123:439–45. ation. Cancer. 2012;118:3725–34.
10. Aiken JF, Youl PH, Janda M, Lowe JB, Ring IT, Elwood 26. Breitbart EW, Waldmann A, Nolte S, Capallaro M,
M. Increase in skin cancer screening during a commu- Greinert R, Volkmer B, et al. Systematic skin cancer
nity-based randomized intervention trial. Int J Cancer. screening in Northern Germany. J Am Acad Dermatol.
2006;118:1010–16. 2012;66:201–11.
11. LeBlanc WG, Vidal L, Kirsner RS, Lee DJ, Caban-Martinez 27. Katalinic A, Eisemann N, Waldmann A. Skin cancer
AJ, McCollister KE, et al. Reported skin cancer screening screening in Germany. Documenting melanoma inci-
of US adult workers. J Am Acad Dermatol. 2008; dence and mortality from 2008 to 2013. Dtsch Arztebl
59:55–63. Int. 2015;112:629–34.
12. Lakhani NA, Saraiya M, Thompson TD, King SC, Guy GP 28. Losina E, Walensky RP, Geller A, Beddingfield FC 3rd,
Jr. Total body skin examination for skin cancer screen- Wolf LL, et al. Visual screening for malignant melan-
ing among US adults from 2000 to 2010. Prev Med. oma: a cost-effectiveness analysis. Arch Dermatol.
2014;61:75–80. 2007;143:21–8.
13. Moon Shots Program. http://www.cancermoonshots. 29. Wernli KJ, Henrikson NB, Morrison CC, Nguyen M,
org. Accessed 9/8/15. Pocobelli G, Whitlock EP. Screening for skin cancer
14. Rodriguez GL, Ma F, Federman DG, Rouhnai P, in adults: an updated systematic evidence review
Chimento MM, Multach M, Kirsner RS. Predictors of skin for the U.S. Preventive Services Task Force.
148 R. SHELLENBERGER ET AL.

Rockville, MD: Agency for Healthcare Research and 37. Goulart JM, Quigley EA, Dusza S, Jewell ST, Alexander
Quality, 2015. G, Asgari MM, et al. Skin cancer education for
30. Gambichler T, Senger E, Rapp S, Alamouti D, Altmeyer primary care physicians: a systematic review of pub-
P, Hoffmann K. Deep shave excision of macular mela- lished evaluated interventions. J Gen Intern Med.
nocytic nevi with the razor blade biopsy technique. 2011;16:127–35.
Dermatol Surg. 2000;26:662–6. 38. Koelink CJ, Vermeulen KM, Kollen BJ, de Bock GH,
31. Geller AC, Elwood M, Swetter SM, Brooks DR, Aitken J, Dekker JH, Jonkmam MF, van der Heide WK. Diagnostic
Youl PH, et al. Factors related to the presentation of accuracy and cost-effectiveness of dermoscopy in pri-
thin and thick nodular melanoma from a population- mary care: a cluster randomized clinical trial. J Eur Acad
based cancer registry in Queensland Australia. Cancer. Dermatol Venereol. 2014;28:1442–9.
2009;115:1318–27. 39. Vestergaard ME, Macaskill P, Holt PE, Menzies SW.
32. Swetter S, Johnson TM, Miller DR, Layton CJ, Brooks KR, Dermoscopy compared with naked eye examination for
Geller AC. Melanoma in middle-aged and older men: a the diagnosis of primary melanoma: a meta-analysis of
multi-institutional survey study of factors related to studies performed in a clinical setting. Br J Dermatol.
tumor thickness. Arch Dermatol. 2009;145:397–404. 2008;159:669–76.
33. St Sauver JL, Warner DO, Yawn BP, Jacobsen DJ, 40. Geller AC, O’Riordan DL, Oliveria SA, Valo S, Teuch M,
McGree ME, Pankratz JJ, et al. Why patients visit their Halpern AC. Overcoming obstacles to skin cancer
doctors: assessing the most prevalent conditions in a examinations and prevention counseling for high-risk
defined American population. Mayo Clin Proc. patients: results of a national survey of primary care
2001;88:56–67. physicians. J Am Borad Fam Pract. 2004;17:416–23.
34. Centers for Disease Control and Prevention. Health, 41. Oliveria SA, Henegnan MK, Cushman LF, Ughetta EA,
United States, 2010. Available from URL:http://cdc.gov/ Halpern AC. Skin cancer screening by dermatologists,
nchs/hus.htm. Accessed April16, 2015 family practitioners, and internists: barriers and facilitat-
35. Association of American Medical Colleges. 2014 ing factors. Arch Dermatol. 2011;147:39–44.
Physician Specialty Data Bank. Available at https:// 42. Wise E, Singh D, Moore M, Hayes B, Biello KB, Dickeson
www.aamc.org/data/. Accessed April 20, 2015. MC, et al. Rates of skin cancer screening and preven-
36. Kaiser Family Foundation. Available from http://kff.org. tion counseling by US medical residents. Arch
Accessed September 9, 2015. Dermatol. 2009;145:1131–6.