Screening for Skin Cancer: An Evidence Update for the U.S. Preventive Services Task Force

Project Summary Title and Description

Title
Screening for Skin Cancer: An Evidence Update for the U.S. Preventive Services Task Force
Description
Structured Abstract Objective: We conducted this review to support the United States Preventive Services Task Force (USPSTF) in updating its 2016 recommendation on screening for skin cancer. The objective was to review benefits and harms of routine skin cancer screening in asymptomatic screening populations aged ≥15 years. Data Sources: We searched MEDLINE ALL via Ovid, Embase via Elsevier, and the Cochrane Central Register of Controlled Trials via Wiley. We updated the search used in the 2016 systematic review on January 12, 2021, and we ran a bridge search on January 7, 2022. A research librarian developed and executed the search strategy. Studies included in the prior review to support the 2016 recommendation and studies referenced in recently published reviews were also considered for inclusion. Study Selection: We reviewed 20,320 abstracts and 522 full-text articles against prespecified inclusion criteria. Eligible studies were English-language randomized controlled trials (RCTs), controlled clinical trials, nonrandomized studies with contemporaneous controls reporting morbidity or mortality associated with skin cancer, or all-cause mortality, stage or lesion thickness at detection of skin cancer or precancerous lesions, and harms of skin cancer screening. At least two investigators independently critically appraised all studies. Data were extracted by one investigator and checked for accuracy by a second. Data Analysis: We extracted relevant study details and outcomes from fair- or good-quality studies. We provided narrative synthesis of results and used summary tables to facilitate comparisons across studies. The overall strength of evidence was graded as high, moderate, low, or insufficient based on criteria adapted from the Evidence-based Practice Center (EPC) Program. Results: We included three studies (10 articles, n=NR in one study; 1,791,615 in the other two) on the direct benefits of skin cancer screening and two studies (3 articles, n=232) on persistent harms of skin cancer screening. We included six studies (7 articles, n=2,947,595) on the association between routine clinician skin examination and stage or lesion thickness at skin cancer detection. We included nine studies (9 articles, n=1,326,051) on the association between stage at skin cancer detection and melanoma or all-cause mortality. Seventeen studies were newly identified in this update. Direct evidence on effectiveness of skin cancer screening. Three non-randomized studies (one good-quality; two fair-quality) evaluated the association between melanoma mortality and skin cancer screening over 4 to 10 years followup. At 10-years of followup of the Skin Cancer Research to Provide Evidence for Effectiveness of Screening in Northern Germany (SCREEN) study, population melanoma mortality rates in the SCREEN region compared to the rest of Germany suggest no mortality benefit to routine skin cancer screening. Similarly, at 5-year followup of the German National Screening Program, no mortality benefit was observed based on national population statistics. One non-randomized study of melanoma mortality in individuals with documented skin cancer screening provided through German statutory health insurance found an absolute decrease in mortality suggesting a screening benefit at four-year followup, but this difference was attenuated on multivariate analysis and adjustment for lead time bias. No included studies reported all-cause mortality, skin squamous cell carcinoma mortality, basal cell carcinoma mortality, or skin cancer morbidity. Harms. Evidence on the persistent psychosocial or cosmetic harms of screening was minimal. In a fair-quality study conducted in Germany (n=45), 27 patients rated 7 percent (4 out of 56) of shave biopsy sites having poor cosmetic outcomes at 6-month followup. A fair-quality United States study (n=187) that assessed psychological wellbeing at 5 and 8 months after skin cancer examination by trained primary care providers found that participants scored within the normal range on measures of anxiety and depression, with none to minimal psychological impacts of screening. Overdiagnosis and subsequent overtreatment of early-stage melanoma is a potential harm of skin cancer screening based on population incidence rates, but no direct evidence was available. Indirect evidence: association between routine clinician skin examination and stage or thickness at skin cancer detection. Based on data from four fair-quality evaluations of three skin cancer screening programs (n=2,344,210), and one good-quality physician-focused skin examination initiative (n=595,799), routine clinician skin examination is not associated with increased detection of keratinocyte carcinoma, melanoma, or skin cancer precursor lesions compared to usual care or lesion-directed examination. Similarly, routine skin examination is not associated with stage at detection for invasive melanoma. Evidence is inconsistent on whether clinician skin examination is associated with higher detection of in situ melanoma based on two studies (n=2,530 melanoma cases), or with thinner lesions (<1mm or <2mm) at melanoma detection based on three studies (n=6,133 melanoma cases). Indirect evidence: association between stage at skin cancer detection and melanoma mortality or all-cause mortality. Three nonrandomized studies (two good-quality, one fair-quality; n=407,133) reported melanoma-specific mortality, and three nonrandomized studies (one good-quality, 2 fair-quality; n=473,660) reported all-cause mortality. Later stage at detection was consistently associated with increased risk of melanoma mortality. Compared to in situ disease at detection, adjusted hazard ratios for melanoma mortality were 5.8 (95% CI, 5.3 to 6.3) for localized, 31.5 (95% CI, 28.9 to 34.2) for regional, and 169.6 (95% CI, 154.2 to 186.6) for distant stage in one U.S.-based study (n=185,219). Two studies using localized stage at detection as the referent group found a similar pattern of increasing melanoma mortality risk with increasing stage. No included studies evaluated the association between stage at diagnosis and skin cancer morbidity. In two nonrandomized studies (1 good-quality, 1 fair-quality; n=135,490), melanoma mortality was higher for males than for females. Three studies with overlapping populations (n=708,814) examined melanoma mortality risk for specific racial and ethnic groups. One study found similar odds of melanoma mortality risk for White and Black persons within each stage at detection. In two other studies with overlapping populations, melanoma mortality risk was higher among Black, Asian American, Native American, Pacific Islanders (AANAPI), and Hispanic adults with melanoma AJCC Stage I and SEER localized stages compared to White adults. In one of these studies, the risk for melanoma mortality among Hispanic persons with regional or distant melanoma stage was also higher than among White adults. Regarding all-cause mortality, the same pattern was observed over three large nonrandomized studies. In one study (n=185,219), the risk for all-cause mortality was adjHR 1.5 (95% CI, 1.5 to 1.5) for localized, 3.9 (95% CI, 3.8 to 4.1) for regional, 15.8 (95% CI, 14.9 to 16.7) for distant disease, compared to in situ melanoma at detection. No included studies addressed keratinocyte carcinoma mortality by stage at detection. Limitations: The body of evidence for benefits and harms of screening is small and derived from nonrandomized studies primarily conducted outside of the United States. The applicability to United States primary care settings might be low. Conclusions: A substantial observational evidence base suggests a clear association between earlier stage at skin cancer detection and decreased mortality risk. However, ecological studies suggest no melanoma mortality benefit associated with skin cancer screening in adolescents or adults in regions with implemented routine screening compared to regions without routine screening. Nonrandomized evidence suggests no association between routine clinician skin examination and earlier stage at melanoma detection; evidence is inconsistent on whether clinician skin examination is associated with thinner melanoma lesions at detection. There is little direct evidence on harms of screening, however; other than overdiagnosis and overtreatment, there are few hypothesized serious harms.
Attribution
Kaiser Permanente Evidence-based Practice Center Kaiser Permanente Center for Health Research; Portland, OR Kaiser Permanente Washington Health Research Institute; Seattle, WA
Authors of Report
Nora B. Henrikson, Ph.D., M.P.H. Ilya Ivlev, M.D., Ph.D., M.B.I. Paula R. Blasi, M.P.H. Matt B. Nguyen, M.P.H. Caitlyn A. Senger, M.P.H. Leslie A. Perdue, M.P.H. Jennifer S. Lin, M.D., M.C.R.
Methodology description
Systematic Review
PROSPERO
N/A
DOI
10.1001/jama.2023.3262
Notes
https://www.uspreventiveservicestaskforce.org/uspstf/document/final-evidence-review/skin-cancer-screening https://pubmed.ncbi.nlm.nih.gov/37071090/
Funding Source
Agency for Healthcare Research and Quality

Key Questions

1. KQ1. What is the effectiveness of routine skin cancer screening with visual skin examination by clinicians in reducing skin cancer morbidity and mortality or all-cause mortality? KQ2. Does routine skin cancer screening lead to higher rates of detection of precancerous lesions or earlier stage skin cancer compared to usual care (for example, lesion-directed skin examination)? KQ3. What are the harms of skin cancer screening and diagnostic followup? KQ4. What is the association between detection of precancerous lesions or earlier stage skin cancer and morbidity and mortality due to skin cancer or all-cause mortality?

Associated Extraction Forms

Type
Standard

Associated Studies (each link opens a new tab)

Title Authors Year
Clinical whole-body skin examination reduces the incidence of thick melanomas. Aitken JF, Elwood M, Baade PD, Youl P, English D 2010 Jan 15
A 10-Year Follow-Up Study of Subjects Recruited in a Health Campaign for the Early Diagnosis of Cutaneous Melanoma: Suggestions for the Screening Timetable. Cristofolini M, Boi S, Cattoni D, Sicher MC, Decarli A, Micciolo R 2015
Are patients benefiting from participation in the German skin cancer screening programme? A large cohort study based on administrative data. Datzmann T, Schoffer O, Meier F, Seidler A, Schmitt J 2022 Jan
Racial disparities in melanoma survival. Dawes SM, Tsai S, Gittleman H, Barnholtz-Sloan JS, Bordeaux JS 2016 Nov
Survival of cutaneous melanoma based on sex, age, and stage in the United States, 1992-2011. Enninga EAL, Moser JC, Weaver AL, Markovic SN, Brewer JD, Leontovich AA, Hieken TJ, Shuster L, Kottschade LA, Olariu A, Mansfield AS, Dronca RS 2017 Oct
Overall Survival Improved for Contemporary Patients with Melanoma: A 2004-2015 National Cancer Database Analysis. Farrow NE, Turner MC, Salama AKS, Beasley GM 2020 Dec
Deep shave excision of macular melanocytic nevi with the razor blade biopsy technique. Gambichler T, Senger E, Rapp S, Alamouti D, Altmeyer P, Hoffmann K 2000 Jul
Total-Body Examination vs Lesion-Directed Skin Cancer Screening. Hoorens I, Vossaert K, Pil L, Boone B, De Schepper S, Ongenae K, Annemans L, Chevolet I, Brochez L 2016 Jan
The effectiveness of a population-based skin cancer screening program: evidence from Germany. Kaiser M, Schiller J, Schreckenberger C 2018 Apr
Skin Cancer Screening in Germany. Documenting Melanoma Incidence and Mortality From 2008 to 2013. Katalinic A, Eisemann N, Waldmann A 2015 Sep 18
Melanoma survival is superior in females across all tumour stages but is influenced by age. Khosrotehrani K, Dasgupta P, Byrom L, Youlden DR, Baade PD, Green AC 2015 Oct
Costs of routine skin cancer screening in Germany: a claims data analysis. Krensel M, Andrees V, Mohr N, Hischke S 2021 Jul
Malignant Melanoma in African-Americans: A Population-Based Clinical Outcomes Study Involving 1106 African-American Patients from the Surveillance, Epidemiology, and End Result (SEER) Database (1988-2011). Mahendraraj K, Sidhu K, Lau CSM, McRoy GJ, Chamberlain RS, Smith FO 2017 Apr
Five-Year Outcomes of a Melanoma Screening Initiative in a Large Health Care System. Matsumoto M, Wack S, Weinstock MA, Geller A, Wang H, Solano FX, Kirkwood JM, Ferris LK 2022 May 1
The ongoing racial disparities in melanoma: An analysis of the Surveillance, Epidemiology, and End Results database (1975-2016). Qian Y, Johannet P, Sawyers A, Yu J, Osman I, Zhong J 2021 Jun
Psychosocial consequences of skin cancer screening. Risica PM, Matthews NH, Dionne L, Mello J, Ferris LK, Saul M, Geller AC, Solano F, Kirkwood JM, Weinstock MA 2018 Jun
High mortality due to cutaneous melanoma in Norway: a study of prognostic factors in a nationwide cancer registry. Robsahm TE, Helsing P, Nilssen Y, Vos L, Rizvi SMH, Akslen LA, Veierod MB 2018
Effects of the German skin cancer screening programme on melanoma incidence and indicators of disease severity. Trautmann F, Meier F, Seidler A, Schmitt J 2016 Nov
Association Between Race/Ethnicity and Survival of Melanoma Patients in the United States Over 3 Decades: A Secondary Analysis of SEER Data. Ward-Peterson M, Acuna JM, Alkhalifah MK, Nasiri AM, Al-Akeel ES, Alkhaldi TM, Dawari SA, Aldaham SA 2016 Apr
Association between tumor characteristics and second primary cancers with cutaneous melanoma survival: A nationwide cohort study. Zheng G, Chattopadhyay S, Sundquist K, Sundquist J, Forsti A, Hemminki A, Hemminki K 2020 Jul

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