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17-11-2016 | Breast cancer | Book chapter | Article

8. Breast Cancer Screening

Author: Ismail Jatoi

Publisher: Springer International Publishing

Abstract

Breast cancer screening is a major public health issue. Decisions concerning breast cancer screening should be based upon the results of randomized controlled trials, not observational studies. There are three important biases associated with observational studies that examine the effect of screening: lead time, length, and selection biases. Randomized trials have shown that mammography screening reduces breast cancer-specific mortality in postmenopausal women. Additionally, randomized trials are underway to assess the efficacy of screening clinical breast examination (CBE) and screening breast ultrasound. Two large randomized trials have failed to demonstrate a benefit of screening breast self-examination (BSE) in reducing breast cancer-specific mortality. Screening breast MRI is often utilized in mutation carriers and those with increased risk of breast cancer based upon family history, but there are no randomized trials that have examined its efficacy. There are also potential hazards of screening that should be considered: lead time, false-positives, radiation exposure (from screening mammography), overdiagnosis, and cost. Women should be informed about both the potential risks and the benefits of breast cancer screening.
Literature
1.
MacDonald I. Biological predeterminism in human cancer. Surg Gynecol Obstet. 1951;92:443–52.PubMed
2.
Black MM, Speer FD. Biological variability of breast carcinoma in relation to diagnosis and therapy. NY State J Med. 1953;53:1560–3.
3.
Devitt JE. Breast cancer: have we missed the forest because of the tree? Lancet. 1994;344:734–5.PubMedCrossRef
4.
Haagensen CD. Diseases of the breast. Philadelphia: WB Saunders; 1956.
5.
Jatoi I. Breast cancer screening. Am J Surg. 1999;177:518–24.PubMedCrossRef
6.
Jatoi I. Breast cancer: a systemic or local disease? Am J Clin Oncol. 1997;20:536–9.PubMedCrossRef
7.
Cole P, Morrison AS. Basic issues in population screening for cancer. J Natl Cancer Inst. 1980;64:1263–72.PubMed
8.
Nielsen C, Lang RS. Principles of screening. Med Clin North Am. 1999;83:1323–37.PubMedCrossRef
9.
Anderson TJ, Lamb J, Alexander F, et al. Comparative pathology of prevalent and incident cancers detected by breast cancer screening: Edinburgh breast screening project. Lancet. 1986;1:519–23.PubMedCrossRef
10.
Gilliland FD, Joste N, Stauber PM, et al. Biologic characteristics of interval and screen-detected breast cancer. J Natl Cancer Inst. 2000;92:743–9.PubMedCrossRef
11.
Xu IL, Prorok PC. Non-parametric estimation of the post-lead-time survival distribution of screen-detected cancer cases. Stat Med. 1995;14:2715–25.PubMedCrossRef
12.
Black WC, Welch HG. Advances in diagnostic imaging and overestimation of disease prevalence and the benefits of therapy. N Engl J Med. 1993;328:1237–43.PubMedCrossRef
13.
Kiemi PJ, Joensuu H, Toikkanen S, et al. Aggressiveness of breast cancers found with and without screening. Br Med J. 1992;304:467–9.CrossRef
14.
Schmidt JG. The epidemiology of mass breast cancer screening—a plea for a valid measure of benefit. J Clin Epidemiol. 1990;43:215–22.PubMedCrossRef
15.
Monsees BS, Destouet JM. A screening mammography program: staying alive and making it work. Radiol Clin North Am. 1992;30:211–9.PubMed
16.
Hurley SF, Kaldor JM. The benefits and risks of mammographic screening for breast cancer. Epidemiol Rev. 1992;14:101–30.PubMedCrossRef
17.
Salomon A. Beitrage zur pathologie und klinik der maminacrcinome. Arch f klin Chir. 1913;101:573–668.
18.
Warren SL. A roentgenologic study of the breast. Am J Roentgenol. 1930;24:113–24.
19.
Gershon-Cohen I, Ingleby H, Moore L. Can mass X-ray surveys be used in detection of early cancer of the breast? JAMA. 1956;161:1069–71.CrossRef
20.
Gershon-Cohen I, Hermel MB, Berger SM. Detection of breast cancer by periodic X-ray examinations. JAMA. 1961;176:1114–6.PubMedCrossRef
21.
Egan RL. Mammography, an aid to diagnosis of breast carcinoma. JAMA. 1962;182:839–43.CrossRef
22.
Fletcher SW, Black W, Harris R, et al. Report of the international workshop on screening for breast cancer. J Natl Cancer Inst. 1993;85:1644–56.PubMedCrossRef
23.
Shapiro S, Venet W, Strax P, et al. Ten-to fourteen-year effect of screening on breast cancer mortality. J Natl Cancer Inst. 1982;69:349–55.PubMed
24.
Eddy DM, Hasselblad V, McGivney W, et al. The value of mammography screening in women under age 50 years. JAMA. 1988;259:1512–9.PubMedCrossRef
25.
Shapiro S, Venet W, Strax P, et al. Periodic screening for breast cancer: the health insurance plan project and its Sequelae, 1963–1986. Baltimore: Johns Hopkins University; 1988.
26.
Nystrom L, Rutqvist LE, Wall S et al. Breast cancer screening with mammography: overview of Swedish randomized trials. Lancet. 1993;34(l):973–8.
27.
Organizing Committee and Collaborators. Breast cancer screening with mammography in women aged 40–49 years: report of the Organizing Committee and Collaborators, Falun Meeting, Falun, Sweden (21 and 22 March 1996). Int J Cancer. 1996;68:693–9.CrossRef
28.
Hendrick RE, Smith RA, Rutlege JH, et al. Benefit of screening mammography in women aged 40–49: a new meta-analysis of randomized controlled trials. Monogr Natl Cancer Inst. 1997;22:87–92.CrossRef
29.
Alexander FE, Anderson TI, Brown H, et al. The Edinburgh randomised trial of breast cancer screening: results after 10 years of follow-up. Br J Cancer. 1994;70:542–8.PubMedPubMedCentralCrossRef
30.
Alexander FE. The Edinburgh randomized trial of breast cancer screening. Monogr Natl Cancer Inst. 1997;22:31–5.CrossRef
31.
Alexander FE, Anderson TI, Brown HK, et al. 14 years of follow-up from the Edinburgh randamised trial of breast cancer screening. Lancet. 1999;353:1903–8.PubMedCrossRef
32.
Miller AB, Baines CI, To T, et al. Canadian national breast screening study I. Breast cancer detection and death rates among women aged 40 to 49 years. Can Med Assoc J. 1992;147:1459–76.
33.
Miller AB, Baines CJ, To T, et al. Canadian national breast screening study II. Breast cancer detection and death rates among women aged 50 to 59 years. Can Med Assoc J. 1992;147:1477–88.
34.
Miller AB, To T, Baines CI, Wall C. Canadian national breast screening study-2: 13-year results of a randomized trial in women aged 50–59 years. J Natl Cancer Inst. 2000;92:1490–9.PubMedCrossRef
35.
Miller AB, Wall C, Baines CJ, Sun P, To T, Narod SA. Twenty five year follow-up for breast cancer incidence and mortality of the Canadian National Breast Screening Study: randomised screening trial. Br Med J. 2014;348:g366.CrossRef
36.
Mosss SM, Cuckle H, Evans A, Johns L, Waller M, Bobrow L. Trial management group. Effect of mammographic screening from age 40 years on breast cancer mortality at 10 years’ follow-up: a randomized controlled trial. Lancet. 2006;368(9552):2053–60.CrossRef
37.
Moss SM, Wale C, Smith R, Evans A, Cuckle H, Duffy SW. Effect of mammographic screening from age 40 years on breast cancer mortality in the UK Age trial at 17 years’ follow-u: a randomised controlled trial. Lancet Oncology. 2015;16:1123–32.PubMedCrossRef
38.
Kerlikowske K, Grady D, Rubin SM, et al. Efficacy of screening mammography. A meta-analysis. JAMA. 1995;273:149–54.PubMedCrossRef
39.
Smart CR, Hendrick RE, Rutledge JH III, et al. Benefit of mammography screening in women ages40 to 49 years: current evidence from randomized controlled trials. Cancer. 1995;75:1619–25.PubMedCrossRef
40.
Humphrey LL, Helfand M, Chan BK, Woolf SH. Breast cancer screening: a summary of the evidence for the U.S. preventive services task force. Ann Intern Med. 2002;137:347–60.PubMedCrossRef
41.
Gotzsche PC, Olsen O. Is screening for breast cancer with mammography justifiable? Lancet. 2000;355:129–34.PubMedCrossRef
42.
Duffy SW, Tabar L. Screening mammography re-evaluated. Lancet. 2000;355:747–8.PubMedCrossRef
43.
Dean PB. Final comment. The articles by Gotzsche and Olsen are not Official Cochrane reviews and lack scientific merit. Lakartidningen. 2000;97:3106.PubMed
44.
Gotzsche PC, Nielsen M. Screening for breast cancer with mammography. Cochrane Database Syst Rev. 2006;(4):CD001877.
45.
Nelson HD, Fu R, Cantor A, Pappas M, Daeges M, Humphrey L. Effectiveness of breast cancer screening: systematic review and meta-analysis to update the 2009 U.S. preventive services task force recommendation. Ann Intern Med. 2016;164(4):1–12.CrossRef
46.
Jatoi I. The case against mammographic screening for women in their forties. In: Jatoi I, editor. Breast cancer screening. Austin: Landes Biosciences; 1997. p. 35–49.
47.
Jatoi I, Baum M. American and European recommendations for screening mammography in younger women: a cultural divide? RMJ. 1993;307:1481–3.
48.
Davis DL, Love SM. Mammographic screening. JAMA. 1994;271:152–3.PubMedCrossRef
49.
Fletcher SW. Breast cancer screening among women in their forties: an overview of the issues. Monogr Natl Cancer Inst. 1997;22:5–9.CrossRef
50.
Kerlikowske K. Efficacy of screening mammography among women aged 40 to 49 years and 40 to 69 years: comparison of relative and absolute benefit. Monogr Natl Cancer Inst. 1997;22:79–86.CrossRef
51.
de Koning HJ, Boer R, Warmerdam PG, et al. Quantitative interpretations of age-specific mortality reductions from the Swedish breast cancer screening trials. J Nati Cancer Inst. 1995;87:1217–23.CrossRef
52.
Kopans DB. The case in favor of mammographic screening for women in their forties. In: Jatoi I, editor. Breast cancer screening. Austin: Landes Biosciences; 1997. p. 9–34.
53.
Elwood JM, Cox B, Richardson AK. The effectiveness of breast cancer screening by mammography in younger women. Online J Curr Clin Trials. 1993 (Doc No. 32).
54.
Clemmensen J. Carcinoma of the breast: results from statistical research. Br J Radiol. 1948;21:583.CrossRef
55.
Jatoi I, Anderson WF, Rosenberg PS. Qualitative age-interactions in breast cancer: a tale of two diseases? Am J Clin Oncol. 2008;31:504–6.PubMedCrossRef
56.
Willett W. Nutritional epidemiology. New York: Oxford University; 1990.
57.
Henderson IC. Biologic variations of tumors. Cancer. 1992;69:1888–95.PubMedCrossRef
58.
Baines CJ. Mammography screening: are women really giving informed consent? J Natl Cancer Inst. 2003;95(20):1512–3.PubMedCrossRef
59.
Tabar L, Fagerberg G, Day NE, et al. What is the optimum interval between mammographic screening examinations? An analysis based on the latest results of the Swedish two-county breast cancer screening trial. Br J Cancer. 1987;55:547–51.PubMedPubMedCentralCrossRef
60.
Leitch AM, Dodd GD, Constanza M, et al. American cancer society guidelines for the early detection of breast cancer: update 1997. CA Cancer J Clin. 1997;47:150–3.PubMedCrossRef
61.
Larsson LG, Nystrom L, Wall S, et al. The Swedish randomized mammography screening trials. J Med Screen. 1996;3:129–32.PubMedCrossRef
62.
Kerlikowske K, Salzmann P, Phillips KA, et al. Continuing screening mammography in women aged 70 to 79 years: impact on life expectancy and cost-effectiveness. JAMA. 1999;282:2156–63.PubMedCrossRef
63.
Jatoi I, Miller AB. Breast cancer screening in elderly women: primum non nocere. JAMA Surgery. 2015;150(12):1107–8.PubMedCrossRef
64.
Jatoi I, Miller AB. Why is breast cancer mortality declining? Lancet Oncology. 2003;4:251–4.PubMedCrossRef
65.
Jatoi I. The impact of advances in treatment on the efficacy of mammography screening. Prev Med. 2011;53:103–4.PubMedCrossRef
66.
Kuhl CK. The “coming of age” of nonmammographic screening for breast cancer. JAMA. 2008;299(18):2203–5.PubMedCrossRef
67.
Berg WA, Blume JD, Cormack JB. Combined screening with ultrasound and mammography vs mammography alone in women at elevated risk of breast cancer. JAMA. 2008;299(18):2151–63.PubMedPubMedCentralCrossRef
68.
Tohno E, Ueno E, Watanabe H. Ultrasound screening of breast cancer. Breast Cancer. 2009;16(1):18–22.PubMedCrossRef
69.
Ohuchi N, Suzuki A, Sobue T, et al. Sensitivity and specificity of mammography and adjunctive ultrasonography to screen for breast cancer in the Japan Strategic Anti-cancer Randomized Trial (J-START): a randomised controlled trial. Lancet. 2016;387:341–8.PubMedCrossRef
70.
Jatoi I, Anderson WF. Management of women who have a genetic predisposition for breast cancer. Surg Clin North Am. 2008;88(4):845–61.PubMedCrossRef
71.
Kriege M, Brekelmans CT, Boetes C, et al. Efficacy of MRI and mammography for breast cancer screening in women with a familial or genetic predisposition. N Engl J Med. 2004;351(5):427–37.PubMedCrossRef
72.
Saslow D, Boetes C, Burke W, et al. American cancer society guidelines for breast screening with MRI as an adjunct to mammography. CA Cancer J Clin. 2007;57(2):75–89.PubMedCrossRef
73.
Bums RB, Freund KM, Ash AS, et al. As mammography use increases, are some providers omitting clinical breast examination? Arch Intern Med. 1996;156:741–4.CrossRef
74.
Saslow D, Hannan J, Osuch J, et al. Clinical breast examination: practical recommendations for optimizing performance and reporting. CA Cancer J Clin. 2004;54:327–44.PubMedCrossRef
75.
Mittra I, Baum M, Thornton H, et al. Is clinical breast examination an acceptable alternative to mammographic screening? BMJ. 2000;321:1071–3.PubMedPubMedCentralCrossRef
76.
Report of the Working Group to review the National Cancer Institute-American Cancer Society breast cancer detection demonstration projects. J Nati Cancer Inst. 1979;62:639–709.
77.
Pisani P, Parkin DM, Ngelangel C, Esteban D, et al. Outcome of screening by clinical examination of the breast in a trial in the Philippines. Int J Cancer. 2006;118(1):149–54.PubMedCrossRef
78.
Barton MB, Harris R, Fletcher SW. Does this patient have breast cancer? The screening clinical breast examination: should it be done? How? JAMA. 1999;282:1270–80.PubMedCrossRef
79.
Kosters JP, Gotzsche PC. Regular self-examination or clinical examination for early detection of breast cancer. Cochrane Database Syst Rev. 2003;2(CD003373). doi:10.​1002/​14651858.​CD003373.
80.
Mittra I, Mishra GA, Singh S, et al. A cluster randomized, controlled trial of breast and cervix cancer screening in Mumbai, India: methodology and interim results after three rounds of screening. Int J Cancer. 2010;126:976–84.PubMed
81.
Sankaranarayanan R, Ramadas K, Thara S, et al. Clinical breast examination: preliminary results from a cluster randomized controlled trial in India. J Natl Cancer Inst. 2011;103:1–5.CrossRef
82.
Adair FE. Clinical manifestations of early cancer of the breast—with a discussion on the subject of biopsy. N Engl J Med. 1933;208:1250–5.CrossRef
83.
Semiglazov VF, Moiseyenko VM, Bavli JL, Migmanova N, et al. The role of breast self-examination in early breast cancer detection (results of the 5-year USSR/WHO randomized study in Leningrad). Eur J Epidemiol. 1992;8(4):498–502.PubMedCrossRef
84.
Semiglazov VF, Moiseyenko VM, Manikhas AG, Protsenko SA, Kharikova RS, Ivanow VG, et al. Role of breast self-examination in early detection of breast cancer: Russia/WHO prospective randomized trial in St. Petersburg. Cancer Strategy. 1999;1:145–51.
85.
Thomas DB, Gao DL, Ray RM, Wang WW, Allison CJ, Chen FL, et al. Randomized trial of breast self-examination: final results. J Natl Cancer Inst. 2002;94(19):1445–57.PubMedCrossRef
86.
Fletcher SW, Elmore JG. False-positive mammograms—can the USA learn from Europe? Lancet. 2005;365:7–8.PubMedCrossRef
87.
Elmore JG, Barton MB, Moceri VM, et al. Ten-year risk of false-positive screening mammograms and clinical breast examinations. N Engl J Med. 1998;338:1089–96.PubMedCrossRef
88.
Hofvind S, Thorsen S, Tretli S. The cumulative risk of a false-positive recall in the Norwegian breast cancer screening program. Cancer. 2004;101:1501–7.PubMedCrossRef
89.
Schwartz LM, Woloshin S, Sox HC, et al. U.S. women’s attitudes to false-positive mammography results and detection of ductal carcinoma in situ: cross sectional survey. BMJ. 2000;320:1635–40.PubMedPubMedCentralCrossRef
90.
Jatoi I, Zhu K, Shah M, Lawrence W. Psychological distress in U.S. women who have experienced false-positive mammograms. Breast Cancer Res Treat. 2006;101:191–200.CrossRef
91.
Bailar JC. Mammography: a contrary view. Ann Intern Med. 1976;84:77–84.PubMedCrossRef
92.
Beemsterboer PM, Warmerdam PG, Boer R, et al. Radiation risk of mammography related to benefit in screening programmes: a favourable balance? J Med Screen. 1998;5:81–7.PubMedCrossRef
93.
Swift M, Morrell D, Massey RB, et al. Incidence of cancer in 161 families affected by ataxia-telangiectasia. N Engl J Med. 1991;325:1831–6.PubMedCrossRef
94.
Werneke U. Ataxia telangiectasia and risk of breast cancer. Lancet. 1997;350:739–40.PubMedCrossRef
95.
Robson M, Offit K. Clinical practice. Management of an inherited predisposition to breast cancer. N Engl J Med. 2007;357(2):154–62.PubMedCrossRef
96.
Vaidya JS, Baum M. Benefits and risks of screening mammography in women with BRCA1 and BRCA2 mutations. JAMA. 1997;278:290.PubMedCrossRef
97.
Pijpe A, Andrieu N, Easton DF, et al. Exposure to diagnostic radiation and risk of breast cancer among carriers of BRCA ½ mutations: retrospective cohort study (GENE-RAD-RISK). Br Med J. 2012;345:1–15.CrossRef
98.
de Gonzalez AM, Berg CD, Visvanathan K, Robson M. Estimated risk of radiation-induced breast cancer from mammographic screening for young BRCA mutation carriers. J Natl Cancer Inst. 2009;101:205–9.CrossRef
99.
Peeters PH, Verbeek AL, Straatman H, et al. Evaluation of over-diagnosis of breast cancer in screening with mammography: results of the Nijmegen programme. Int J Epidemiol. 1989;18:295–9.PubMedCrossRef
100.
Zackrisson S, Andersson I, Janzon L, Manjer J, Garne JP. Rate of over-diagnosis of breast cancer 15 years after end of Malmo mammographic screening trial: follow-up study. Br Med J. 2006;332(7543):689–92.CrossRef
101.
Bleyer A, Welch HG. Effect of three decades of screening mammography on breast cancer incidence. N Engl J Med. 2012;367:1998–2005.PubMedCrossRef
102.
Zahl P, Maehlen J, Welch HG. The natural history of invasive breast cancers detected by screening mammography. Arch Intern Med. 2008;168(21):2311–6.PubMedCrossRef
103.
Jatoi I, Baum M. Mammographically detected ductal carcinoma in situ: are we overdiagnosing breast cancer? Surgery. 1995;118:118–20.PubMedCrossRef
104.
Welch HG, Woloshin S, Schwartz LM. The sea of uncertainty surrounding ductal carcinoma in situ—the price of screening mammography. J Natl Cancer Inst. 2008;100(4):228–9.PubMedCrossRef
105.
Moore MM. Treatment of ductal carcinoma in situ of the breast. Semin Surg Oncol. 1991;7:267–70.PubMedCrossRef
106.
Emster VL, Barclay J, Kerlikowske K, et al. Incidence of and treatment for ductal carcinoma in situ of the breast. JAMA. 1996;275:913–8.CrossRef
107.
Nielsen M, Thomsen JL, Primdahl S, et al. Breast cancer and atypia among young and middle aged women: a study of 110 medicolegal autopsies. Br J Cancer. 1987;56:814–9.PubMedPubMedCentralCrossRef
108.
Rosen PR, Braun DW Jr, Kinne DE. The clinical significance of pre-invasive breast carcinoma. Cancer. 1980;46:919–25.PubMedCrossRef
109.
Page DL, Dupont WD, Rogers LW, et al. Intraductal carcinoma of the breast: follow-up after biopsy only. Cancer. 1982;49:751–8.PubMedCrossRef
110.
Alpers CE, Wellings SR. The prevalence of carcinoma in situ in normal and cancer-associated breasts. Hum Pathol. 1985;16:796–807.PubMedCrossRef
111.
Kattlove H, Liberati A, Keeler B, et al. Benefits and costs of screening and treatment for early breast cancer: development of a basic benefit package. JAMA. 1995;273:142–8.PubMedCrossRef
112.
Okonkwo QL, Draisma G, der Kinderen A, Brown ML, de Koning HJ. Breast cancer screening policies in developing countries: a cost-effectiveness analysis for India. J Natl Cancer Inst. 2008;100:1290–300.PubMedCrossRef
113.
Black WC, Nease RF, Tosteson AN. Perceptions of breast cancer risk and screening effectiveness in women younger than 50 years of age. J Natl Cancer Inst. 1995;87:720–31.PubMedCrossRef
114.
Berry DA, Cronin KA, Plevritis SK, et al. Effect of screening and adjuvant therapy on mortality from breast cancer. N Engl J Med. 2005;353(17):1784–92.PubMedCrossRef
115.
Jatoi I, Chen BE, Anderson WF, Rosenberg PS. Breast cancer mortality trends in the United States according to estrogen receptor status and age at diagnosis. J Clin Oncol. 2007;25(13):1683–90.PubMedCrossRef
116.
Jatoi I, Anderson WF, Rao SR, Devesa SS. Breast cancer trends among black and white women in the United States. J Clin Oncol. 2006;23(31):7836–41.CrossRef