An Update of the Evidence for the U.S. Preventive Services Task Force
February 2009
Prepared by Tracy Wolff, MD, MPH; Eric Tai, MD, MS; and Therese Miller, DrPH.
The information in this report is intended to help clinicians, employers, policymakers, and others make informed decisions about the provision of health care services. This report is intended as a reference and not as a substitute for clinical judgment.
This report may be used, in whole or in part, as the basis for the development of clinical practice guidelines and other quality enhancement tools, or as a basis for reimbursement and coverage policies. AHRQ or U.S. Department of Health and Human Services endorsement of such derivative products may not be stated or implied.
This report was first published in Annals of Internal Medicine in
February 2009 (Ann Intern Med 2009;150:194-8. http://www.annals.org).
Contents
Abstract
Introduction
Methods
Results
Discussion
References
Abstract
Background: Skin cancer is the most commonly diagnosed cancer
in the United States. The majority of skin cancer is nonmelanoma
cancer, either basal cell cancer or squamous cell cancer. The incidence
of both melanoma and nonmelanoma skin cancer has been
increasing over the past 3 decades. In 2001, the U.S. Preventive
Services Task Force (USPSTF) found insufficient evidence to recommend
for or against routine screening for skin cancer by using a
total-body skin examination for early detection of skin cancer.
Purpose: To update the evidence of benefits and harms of screening
for skin cancer in the general population.
Data Sources: MEDLINE® and Cochrane Library searches from 1
June 1999 to 9 August 2005 for English-language articles; recent
systematic reviews; reference lists of retrieved articles; and expert
suggestions.
Study Selection: English-language studies were selected to answer
the following key question: Does screening in asymptomatic persons
with a whole-body examination by a primary care clinician or
by self-examination reduce morbidity and mortality from skin cancer?
Randomized, controlled trials and case—control studies of
screening for skin cancer were selected. One author selected English-language
studies to answer the following contextual questions: Can
screening with whole-body examination by primary care clinicians
or by self-examination accurately detect skin cancers? Does screening
with whole-body examination or by self-examination detect
melanomas at an earlier stage (thinner lesions)?
Data Extraction: All studies for the key question were reviewed,
abstracted, and rated for quality by using predefined USPSTF
criteria.
Data Synthesis: No new evidence from controlled studies was
found that addressed the benefit of screening for skin cancer with
a whole-body examination by a physician. One article of fair quality,
which reanalyzed data from a 1996 study previously identified
for the 2001 report for the USPSTF, provides limited but insufficient
evidence on the benefit of skin self-examination in the reduction of
morbidity and mortality from melanoma.
Limitations: Direct evidence linking skin cancer screening to improved
health outcomes is lacking. Information is limited on the
accuracy of screening by physicians or patients using real patients
and lesions.
Conclusion: The limited evidence prevents an accurate estimation
of the benefits of screening for skin cancer in the general primary
care population.
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Introduction
Skin cancer is the most commonly diagnosed cancer in
the United States (1). The majority of skin cancer is
nonmelanoma cancer, either basal cell cancer or squamous
cell cancer (2). In the United States, melanoma of the skin
is the sixth most common type of cancer in white men and
women (3). The incidence of both melanoma and non-melanoma
skin cancer has been increasing over the past 3
decades (4). Several preventive strategies have been proposed
by professional organizations, including routine
screening.
The U.S. Preventive Services Task Force (USPSTF)
last reviewed screening for skin cancer in 2001 and concluded
that evidence was insufficient to recommend for or
against routine screening for skin cancer by using a total-body
skin examination for the early detection of cutaneous
melanoma, basal cell cancer, or squamous cell cancer (5).
The USPSTF made this statement after reviewing the
available evidence and identifying 2 major gaps: the lack of
quality evidence that links screening to improved health
outcomes and limited information about the ability of primary
care providers to perform adequate examinations in
the context of usual care. To update its recommendation,
the USPSTF determined that an update of the evidence
would need to focus on these 2 issues.
On the basis of an analytic framework (Figure), the
USPSTF determined that this evidence update would focus
on a systematic review of the evidence of controlled
trials on screening for skin cancer with morbidity and mortality
outcomes to answer the following key question: Does
screening in asymptomatic persons with whole-body examination
by a primary care clinician or by self-examination reduce morbidity and mortality from skin cancer? In addition,
the USPSTF asked for information concerning several
contextual questions. The issues for this review that
were identified as contextual questions that were non-systematically
reviewed are:
Contextual Question 1. Can screening with whole-body
examination by primary care clinicians or by self-examination
accurately detect skin cancers?
Contextual Question 2. Does screening with whole-body
examination or by self-examination detect melanomas
at an earlier stage (thinner lesions)?
This review does not include evidence on counseling
for skin cancer. The USPSTF previously reviewed the evidence
for counseling; the evidence review and recommendation
can be found at http://www.preventiveservices.ahrq.gov.
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Methods
Data Sources and Searches
We searched for English-language literature in MEDLINE®
to identify randomized, controlled trials (RCTs) or
case-control trials published from 1 June 1999 to 9 August
2005 to answer the following key question: Can
screening reduce morbidity and mortality from skin cancer?
We used terms skin neoplasms, squamous cell neoplasms,
basal cell neoplasms, melanoma, and mass screening. In addition
to the MEDLINE® search, we identified further literature
by reviewing reference lists of review articles and editorials
and by consulting with experts. For the contextual
questions, we performed targeted literature searches, reviewed
the searches performed for other questions, identified
studies from reference lists, and consulted with experts.
Study Selection
Two reviewers independently reviewed the title lists,
abstracts, and full articles for the key question. We excluded
studies if they did not address skin cancer, did not
report morbidity or mortality outcomes, were editorials or
review articles, had no control group, or had a study population
that included only persons with rare skin cancer
syndromes. We also excluded studies if the intervention
was not screening with whole-body visual examination by a
physician or by the patient, was not performed in a primary
care setting, or was designed to improve diagnostic
ability (and not screening). We discussed studies selected
by fewer than 2 reviewers and based selection on consensus.
A third reviewer was consulted if necessary. For contextual
question 1, 1 author selected studies published
since June 1999 that provided information on accuracy of
screening examinations by primary care clinicians or by
patient self-examination. For contextual question 2, 1 author
selected studies published since June 1999 that provided
information on thinness of lesions detected by
screening examinations.
Data Extraction and Quality Assessment
For all citations that met the eligibility criteria for the
key question, 2 reviewers independently reviewed, abstracted,
and quality-rated the full articles. The 2 reviewers
achieved consensus about article inclusion, content, and
quality through discussion; a third reviewer resolved disagreements.
We extracted data on the following items from
the studies included for the key question: identification of
case patients, case definition, selection of control participants,
comorbid conditions, sun exposures, demographics
of case patients and control participants, definition of
screening examination, exposure to screening, rates of
follow-up, and results. We performed quality evaluations
of articles for the key question by using standard USPSTF
methodology on internal and external validity (6). We
evaluated the quality of RCTs and cohort studies on the
following items: initial assembly of comparable groups,
maintenance of comparable groups, important differential
loss to follow-up or overall high loss to follow-up, measurements
(equality, reliability, and validity of outcome measurements),
clear definition of the interventions, and appropriateness
of outcomes. We evaluated the quality of
case–control studies on the following items: accurate ascertainment
of cases, nonbiased selection of case patients and
control participants with exclusion criteria applied equally
to both, response rate, diagnostic testing procedures applied
equally to each group, accurate measurement of exposure
applied equally to each group, measurement of exposure
accurate and applied equally to each group, and
appropriate attention to potential confounding variables.
Data Synthesis and Analysis
Data from the included studies was synthesized qualitatively
in a narrative format.
Role of the Funding Source
The general work of the USPSTF is supported by the
Agency for Healthcare Research and Quality. This specific
review did not receive separate funding.
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Results
Key Question
Does screening in asymptomatic persons with whole-body examination
by a primary care clinician or by self-examination
reduce morbidity and mortality from skin cancer?
We found no new evidence on the effectiveness of skin
examination by a physician in reducing the morbidity or
mortality of skin cancer. One article of fair quality by Berwick
and colleagues (7), which reanalyzed data from a
1996 study identified for the 2001 report for the USPSTF
(8), provides limited but insufficient evidence on the benefit
of skin self-examination in the reduction of morbidity
and mortality from melanoma.
Data on case patients (n = 650) in Berwick and colleagues'
study (7) were obtained from the Connecticut Tumor
Registry, a National Cancer Institute Surveillance Epidemiology
and End-Results (SEER) site. Control
participants (n = 549) were identified from the general
public through random-digit dialing and were frequency-matched
on age and sex. Nurses performed a limited skin
examination to count nevi on the back and arms. Participants
were followed biannually for a mean of 5.4 years.
Identification of case patients was probably fairly complete
because of a state reporting mandate and the research
team’s active monitoring of dermatopathology laboratories.
The response rate for case patients and control participants
was 75% and 70%, respectively. The mortality tally was
probably complete because the research team used several
sources to identify deaths of the participants. Limitations
of the research design include the potential selection bias of
case patients and control participants, lack of information
on the initial comparability of the case patients and control
participants, potential recall bias because information on
many variables (including the history of any clinical screening)
relied on patient report, and lack of information on
masking of the nurse or dermatologist to the case status.
Of the original 650 case patients, 112 were excluded:
26 because of diagnosis from node or organ metastases, 95
with a diagnosis of lentigo maligno melanoma, and 1 without
follow-up. This analysis showed no significant association
between screening examination (by self-examination
or by a physician) and death from melanoma in those with
melanoma. On univariate analysis, the hazard ratio for skin
self-examination was 0.6 (95% CI, 0.2 to 1.5) and for
physician screening examination was 0.7 (CI, 0.4 to 1.3);
this does not differ greatly from the 1996 analysis that had
more participants and a slightly broader definition of the
outcome. The authors report a significant association between
"skin awareness" and death from melanoma (hazard
ratio, 0.5 [CI, 0.3 to 0.9)) after controlling for other confounders.
The authors defined skin awareness as a positive
response to "Did you ever think about your skin, how it
looked, whether there were any changes, or whether there
were any abnormal marks?"
Contextual Question 1
Can screening with whole-body examination by primary
care clinicians or by self-examination accurately detect skin
cancers?
Accuracy of screening is an important link in the chain
of evidence connecting screening in asymptomatic persons
with improved health outcomes. Evidence for the accuracy
of screening with a whole-body examination by physicians
or by patients is limited and inconsistent. A recent systematic
review (9) using pictures of lesions reported a sensitivity
that ranged from 42% to 100% and a specificity of
98%. The same systematic review reported a sensitivity of
70% to 91% and a specificity of 51% to 87% for appropriateness
of referral or biopsy, using histopathology or
expert consensus as the gold standard. Studies on the accuracy
of skin self-examination reported sensitivity and
specificity from 58% to 75% and 62% to 98%, respectively.
The studies in physicians evaluated the accuracy of
diagnosing pigmented lesions, not a screening examination,
and many of the studies on self-examination were
performed in selected patient populations. Therefore, these
results may not be generalizable to a screening examination
in the general population. In addition to the accuracy of a
physician or patient examination, there is the uncertainty
of the pathologist’s reading of the biopsy specimen. There
is some evidence of moderate disagreement among pathologists
in reading skin biopsies (10,11).
Several studies on diagnostic and referral accuracy of
family physicians and general practitioners have been published
since 2001 (12–14); these studies evaluated accuracy
before and after educational interventions and generally
concluded that educational interventions improve the diagnostic
accuracy of skin cancer examinations. Most of
these studies were performed outside the United States,
and all used nonliving representations of lesions, including
photographs and slides of lesions, limiting the applicability
to screening accuracy in primary care.
A more recent, community-based RCT of screening in
Australia (15) involving 16,383 whole-body skin examinations
reported the specificity and positive predictive value
of screening by a primary care physician for melanoma as
86% and 2.5%, respectively. The overall positive predictive
value for all types of skin cancer was 29%. However, the
researchers did not follow the participants with negative
results, and therefore could not report the number of true-negative
results or the true specificity.
Three published studies have evaluated the accuracy of
skin self-examination (16–18). They generally showed
variable specificity and sensitivity that was higher with
greater size increases in lesions and higher with the use of
photographs. Two of these studies assessed the accuracy,
after artificial change of lesions, in the study participants'
reports of the number or appearance of moles; and 1 study
evaluated the accuracy of skin self-examination before and
after education about the asymmetry, border, color, diameter (ABCD) criteria. Again, the applicability to primary
care of studies of artificial change in lesions is questionable.
Contextual Question 2
Does screening with whole-body examination or by self-examination
detect melanomas at an earlier stage (thinner
lesions)?
We found no RCTs that compared screened and unscreened
participants with respect to thickness of melanoma
lesions. We identified 1 study that looked at a
screened population to evaluate lesion thickness at detection
(19). This study of 639,835 participants who were
screened during the American Academy of Dermatology
Skin Cancer Screening Program from 1985 to 1999 compared
the results of the American Academy of Dermatology
screening efforts with the SEER registry. In the American
Academy of Dermatology program, dermatologists
performed screening examinations that were free and open
to the public. Participants who had received screening
through the American Academy of Dermatology program
had a higher percentage of lesions smaller than 1.50 mm
than cases documented in the SEER registry: 10% and 2%,
respectively (P <0.001). Conclusions are limited because
of self-selection in the American Academy of Dermatology
program, the ecological nature of the study, and problems
with generalizing screening by a dermatologist to screening
by a primary care clinician. A study in Queensland, Australia,
reviewed the characteristics of all histologically confirmed
first melanomas in residents age 20 to 75 years (20).
They found that the rate of thin lesions (<0.75 mm) detected
by a physician (81%) was higher than the rate detected
by nonphysicians (62%).
There is evidence from retrospective studies of patients
with diagnosed melanoma that, although most melanoma
lesions are first noticed by someone other than a physician,
lesions detected by a physician are thinner. A study of 471
patients with newly diagnosed melanoma (1995 to 1998)
in New York found that 57% of patients first detected the
melanoma lesion and another 15% were found by some-one
other than a physician (primarily a spouse) (21). There
was a significant association between physician detection
and thickness less than or equal to 0.75 mm. In an Italian
study of 816 consecutive patients with melanoma (22,23),
identification by a dermatologist was associated with significantly
thinner melanoma lesions than those identified
by others (0.68 mm vs. 0.90 mm). Of note, melanoma
lesions in those participants that performed skin self-examination
were also significantly thinner than in those who
did not perform skin self-examination (0.77 mm vs. 0.95
mm); however, the definition of skin self-examination was
not reported. A study of 102 patients seen at the Johns
Hopkins Melanoma Center between June 1995 and June
1997 reported that the majority of lesions were detected by
the patient (24). The mean lesion thickness was 0.23 mm
for physician-detected lesions and 0.9 mm for self-detected
lesions. Compared with self- or other-detected lesions,
physician-detected lesions were associated with a higher
likelihood of thinner lesions (relative risk, 4.0 [CI, 1.08 to
14.3]) for lesions smaller than 0.75 mm versus those larger
than 0.75 mm.
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Discussion
The direct evidence to support the benefits of a screening
examination by a physician or patient in reducing morbidity
and mortality is limited. We reviewed 1 new fair-quality
case-control study of skin self-examination that
used data from a study identified in the 2001 report for the
USPSTF. We found no new studies on the benefits of
screening by a physician that met our inclusion and exclusion
criteria and were of appropriate quality.
The evidence on accuracy of screening has limitations.
Several different methods have been used to study the accuracy
of screening for skin cancer by physicians and by
patients. Many studies measure accuracy through the use
of photographs of lesions of known histopathology. Other
studies measure accuracy by following the referral patterns
and ultimate histopathology of lesions from real patients.
Both of these methods have obvious problems. Using photographs
of known lesions may test the accuracy of the
diagnostic ability of a physician but does not necessarily
assess the accuracy of a full-body screening examination.
The use of referral patterns and histopathology assumes
that a dermatologist's assessment of the need for biopsy
and the resultant histopathology constitute the gold standard.
Without appropriate follow-up of patients, this
method probably underestimates the number of false-negative
results.
There is limited evidence as to whether screening by
physicians or by patients identifies lesions that are thinner
than those identified in usual care. Older ecological studies
reported conflicting results as to the association of thickness
of melanoma and screening. Newer limited evidence
from 1 large study of a self-selected screened population
and from retrospective studies indicates that physician examinations
and self-examinations identify thinner melanoma
lesions. However, the retrospective studies do not
report whether the lesions were detected during a screening
examination or coincidentally during an examination for
other reasons. Therefore, there are problems with using
this evidence to generalize about the ability of screening
examinations to identify thinner lesions in the general public.
In addition, the majority of melanoma lesions are identified
by the patient, friend, or spouse, and the question
remains whether encouraging skin self-examination would
identify more lesions or lesions at an earlier stage than are
currently being identified by nonphysicians.
Research Gaps
The literature on screening for skin cancer has several
limitations. A major limitation is the lack of direct evidence
linking skin cancer screening to improved health
outcomes. An adequately powered, population-based RCT of screening demonstrating mortality outcomes would require
approximately 800000 participants because of the
relatively low melanoma-related mortality rate in the
United States. (7,25) However, the incidence of melanoma
and mortality are higher in Australia, requiring a
smaller sample size. A 3-year RCT in 44 Australian communities
(n = 560000 adults age 30 years or older) had
been planned by Aitken and colleagues (26). The intervention
included the promotion of screening through skin
self-examination and physician examination. Unfortunately,
the study was performed only in 9 control and 9
intervention communities because of lack of funding. The
preliminary results may help inform future recommendations
on skin cancer screening. Further analyses are needed
to evaluate whether routine referral to dermatologic specialists
might be effective. Given the lack of direct evidence,
modeling studies using available indirect evidence,
including cost-effectiveness studies, may provide some information
on the usefulness of screening as a preventive
strategy.
Other limitations of the literature include a lack of
large studies on accuracy of screening in the general population
and a lack of information on whether screening in
the general population would result in the identification of
lesions at an earlier stage than regular care.
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Current Author Addresses: Drs. Wolff and Miller: Center for Primary
Care, Prevention, and Clinical Partnerships, Agency for Healthcare Research
and Quality, 540 Gaither Road, Rockville, MD 20850. Dr. Tai: Division of Cancer
Prevention and Control, Centers for Disease Control and Prevention, 4770 Buford
Highway, Northeast, MS-K57, Atlanta, GA 30341-3717.
Return to Contents
AHRQ Publication No. 09-05128-EF-4
Current as of February 2009
Internet Citation:
Wolff T, Tai E, Miller T. Screening for Skin Cancer: An
Update of the Evidence for the U.S. Preventive Services Task Force.
AHRQ Publication No. 09-05128-EF-4, February 2009. Agency for Healthcare
Research and Quality, Rockville, MD. http://www.ahrq.gov/clinic/uspstf09/skincancer/skincanart.htm
540 Gaither Road Rockville, MD 20850