Abstract
Purpose
The impact of opportunistic screening mammography in the United States is difficult to quantify, partially due to lack of inclusion regarding method of detection (MOD) in national registries. This study sought to determine the feasibility of MOD collection in a multicenter community registry and to compare outcomes and characteristics of breast cancer based on MOD.
Methods
We conducted a retrospective study of breast cancer patients from a multicenter tumor registry in Missouri from January 2004 - December 2018. Registry data were extracted by certified tumor registrars and included MOD, clinicopathologic information, and treatment. MOD was assigned as screen-detected or clinically detected. Data were analyzed at the patient level. Chi-squared tests were used for categorical variable comparison and Mann-Whitney-U test was used for numerical variable comparison.
Results
5351 women (median age, 63 years; interquartile range, 53–73 years) were included. Screen-detected cancers were smaller than clinically detected cancers (median size 12 mm vs. 25 mm; P < .001) and more likely node-negative (81% vs. 54%; P < .001), lower grade (P < .001), and lower stage (P < .001). Screen-detected cancers were more likely treated with lumpectomy vs. mastectomy (73% vs. 41%; P < .001) and less likely to require chemotherapy (24% vs. 52%; P < .001). Overall survival for patients with invasive breast cancer was higher for screen-detected cancers (89% vs. 74%, P < .0001).
Conclusion
MOD can be routinely collected and linked to breast cancer outcomes through tumor registries, with demonstration of significant differences in outcome and characteristics of breast cancers based on MOD. Routine inclusion of MOD in US tumor registries would help quantify the impact of opportunistic screening mammography in the US.
Similar content being viewed by others
Data Availability
The datasets analysed during the current study are not publicly available due to their linkage to personal health information but are available from the corresponding author on reasonable request.
References
Shapiro S (1977) Evidence on screening for breast cancer from a randomized trial. Cancer 39(6 Suppl):2772–2782
Andersson I, Aspegren K, Janzon L, Landberg T, Lindholm K, Linell F, Ljungberg O, Ranstam J, Sigfússon B (1988) Mammographic screening and mortality from breast cancer: the Malmö mammographic screening trial. BMJ 297(6654):943–948
Tabár L, Fagerberg CJ, Gad A, Baldetorp L, Holmberg LH, Gröntoft O, Ljungquist U, Lundström B, Månson JC, Eklund G et al (1985) Reduction in mortality from breast cancer after mass screening with mammography. Randomised trial from the breast Cancer screening Working Group of the Swedish National Board of Health and Welfare. Lancet 1(8433):829–832
Roberts MM, Alexander FE, Anderson TJ, Chetty U, Donnan PT, Forrest P, Hepburn W, Huggins A, Kirkpatrick AE, Lamb J et al (1990) Edinburgh trial of screening for breast cancer: mortality at seven years. Lancet 335(8684):241–246
Tabár L, Vitak B, Chen HH, Yen MF, Duffy SW, Smith RA (2001) Beyond randomized controlled trials: organized mammographic screening substantially reduces breast carcinoma mortality. Cancer 91(9):1724–1731
Duffy SW, Tabár L, Chen HH, Holmqvist M, Yen MF, Abdsalah S, Epstein B, Frodis E, Ljungberg E, Hedborg-Melander C et al (2002) The impact of organized mammography service screening on breast carcinoma mortality in seven swedish counties. Cancer 95(3):458–469
Otto SJ, Fracheboud J, Looman CW, Broeders MJ, Boer R, Hendriks JH, Verbeek AL, de Koning HJ (2003) Initiation of population-based mammography screening in dutch municipalities and effect on breast-cancer mortality: a systematic review. Lancet 361(9367):1411–1417
Coldman A, Phillips N, Wilson C, Decker K, Chiarelli AM, Brisson J, Zhang B, Payne J, Doyle G, Ahmad R (2014) Pan-canadian study of mammography screening and mortality from breast cancer. J Natl Cancer Inst 106(11):1–7
Puliti D, Bucchi L, Mancini S, Paci E, Baracco S, Campari C, Canuti D, Cirilli C, Collina N, Conti GM et al (2017) Advanced breast cancer rates in the epoch of service screening: the 400,000 women cohort study from Italy. Eur J Cancer 75:109–116
Paap E, Holland R, den Heeten GJ, van Schoor G, Botterweck AA, Verbeek AL, Broeders MJ (2010) A remarkable reduction of breast cancer deaths in screened versus unscreened women: a case-referent study. Cancer Causes Control 21(10):1569–1573
Otto SJ, Fracheboud J, Verbeek AL, Boer R, Reijerink-Verheij JC, Otten JD, Broeders MJ, de Koning HJ (2012) Mammography screening and risk of breast cancer death: a population-based case-control study. Cancer Epidemiol Biomarkers Prev 21(1):66–73
Coldman A, Phillips N, Warren L, Kan L (2007) Breast cancer mortality after screening mammography in British Columbia women. Int J Cancer 120(5):1076–1080
Webb ML, Cady B, Michaelson JS, Bush DM, Calvillo KZ, Kopans DB, Smith BL (2014) A failure analysis of invasive breast cancer: most deaths from disease occur in women not regularly screened. Cancer 120(18):2839–2846
Spencer DB, Potter JE, Chung MA, Fulton J, Hebert W, Cady B (2004) Mammographic screening and disease presentation of breast cancer patients who die of disease. Breast J 10(4):298–303
Duffy SW, Tabár L, Yen AM, Dean PB, Smith RA, Jonsson H, Törnberg S, Chen SL, Chiu SY, Fann JC et al (2020) Mammography screening reduces rates of advanced and fatal breast cancers: results in 549,091 women. Cancer 126(13):2971–2979
Siu AL (2016) Screening for breast Cancer: U.S. Preventive Services Task Force Recommendation Statement. Ann Intern Med 164(4):279–296
Oeffinger KC, Fontham ET, Etzioni R, Herzig A, Michaelson JS, Shih YC, Walter LC, Church TR, Flowers CR, LaMonte SJ et al (2015) Breast Cancer screening for women at average risk: 2015 Guideline Update from the American Cancer Society. JAMA 314(15):1599–1614
Monticciolo DL, Malak SF, Friedewald SM, Eby PR, Newell MS, Moy L, Destounis S, Leung JWT, Hendrick RE, Smetherman D (2021) Breast Cancer Screening Recommendations Inclusive of all women at average risk: update from the ACR and society of breast imaging. J Am Coll Radiol 18(9):1280–1288
Reeves MJ, Newcomb PA, Remington PL, Marcus PM (1995) Determinants of breast cancer detection among Wisconsin (United States) women, 1988-90. Cancer Causes Control 6(2):103–111
Nakhleh RE, Zarbo RJ (2001) Surgical pathology-based outcomes assessment of breast cancer early diagnosis: a College of American Pathologists Q-Probes study in 199 institutions. Arch Pathol Lab Med 125(3):325–331
Dong W, Berry DA, Bevers TB, Kau SW, Hsu L, Theriault RL, Shen Y (2008) Prognostic role of detection method and its relationship with tumor biomarkers in breast cancer: the university of Texas M.D. Anderson Cancer Center experience. Cancer Epidemiol Biomarkers Prev 17(5):1096–1103
Puvanesarajah S, Gapstur SM, Patel AV, Sherman ME, Flanders WD, Gansler T, Troester MA, Gaudet MM (2019) Mode of detection and breast cancer mortality by follow-up time and tumor characteristics among screened women in Cancer Prevention Study-II. Breast Cancer Res Treat 177(3):679–689
Farwell MF, Foster RS Jr, Costanza MC (1993) Breast cancer and earlier detection efforts. Realized and unrealized impact on stage. Arch Surg 128(5):510–513
Kaplan HG, Malmgren JA, Atwood MK, Calip GS (2015) Effect of treatment and mammography detection on breast cancer survival over time: 1990–2007. Cancer 121(15):2553–2561
Hayse B, Hooley RJ, Killelea BK, Horowitz NR, Chagpar AB, Lannin DR (2016) Breast cancer biology varies by method of detection and may contribute to overdiagnosis. Surgery 160(2):454–462
McPherson CP, Swenson KK, Jolitz G, Murray CL (1997) Survival of women ages 40–49 years with breast carcinoma according to method of detection. Cancer 79(10):1923–1932
Maibenco D, Daoud Y, Phillips E, Saxe A (1999) Relationship between method of detection of breast cancer and stage of disease, method of treatment, and survival in women aged 40 to 49 years. Am Surg 65(11):1061–1066
Malmgren JA, Parikh J, Atwood MK, Kaplan HG (2012) Impact of mammography detection on the course of breast cancer in women aged 40–49 years. Radiology 262(3):797–806
Malmgren JA, Parikh J, Atwood MK, Kaplan HG (2014) Improved prognosis of women aged 75 and older with mammography-detected breast cancer. Radiology 273(3):686–694
Shen Y, Yang Y, Inoue LY, Munsell MF, Miller AB, Berry DA (2005) Role of detection method in predicting breast cancer survival: analysis of randomized screening trials. J Natl Cancer Inst 97(16):1195–1203
Mook S, Van ‘t Veer LJ, Rutgers EJ, Ravdin PM, van de Velde AO, van Leeuwen FE, Visser O, Schmidt MK (2011) Independent prognostic value of screen detection in invasive breast cancer. J Natl Cancer Inst 103(7):585–597
Joensuu H, Lehtimäki T, Holli K, Elomaa L, Turpeenniemi-Hujanen T, Kataja V, Anttila A, Lundin M, Isola J, Lundin J (2004) Risk for distant recurrence of breast cancer detected by mammography screening or other methods. JAMA 292(9):1064–1073
Tchou J, Greshock J, Bergey MR, Sonnad SS, Sargen M, Weinstein S, Czerniecki BJ, Boraas M, Fraker DL, Rosato E et al (2008) Method of primary tumor detection as a risk factor for local and distant recurrence after breast-conservation treatment for early-stage breast cancer. Clin Breast Cancer 8(2):143–148
Jatoi I, Sung H, Jemal A (2022) The emergence of the racial disparity in U.S. breast-Cancer mortality. N Engl J Med 386(25):2349–2352
Hill DA, Nibbe A, Royce ME, Wallace AM, Kang H, Wiggins CL, Rosenberg RD (2010) Method of detection and breast cancer survival disparities in hispanic women. Cancer Epidemiol Biomarkers Prev 19(10):2453–2460
Bleyer A, Welch HG (2012) Effect of three decades of screening mammography on breast-cancer incidence. N Engl J Med 367(21):1998–2005
Breast Cancer : Method of Detection [https://www.acr.org/Clinical-Resources/Breast-Imaging-Resources/Method-of-Detection]
Funding
This work is supported by a grant from the Saint Louis University Research Institute and resources from the AHEAD Institute.
Author information
Authors and Affiliations
Contributions
All authors contributed to the study conception and design. Material preparation, data collection and analysis were performed by Debbie Bennett, Andrea Winter, Laura Billadello, Mary Catherine Lowdermilk, Christina Marie Doherty, Sakina Kazmi, and Sydney Laster. Statistical analysis was performed by Noor Al-Hammadi. The first draft of the manuscript was written by Debbie Bennett and all authors commented on previous versions of the manuscript. All authors read and approved the final manuscript.
Corresponding author
Ethics declarations
Competing interests
Linda Moy MD, reported grant support (Siemens Research Grant, Gordon and Betty Moore Foundation, Mary Kay Foundation and Google), personal fees (Lunit Insight, Inc., Advisory Board, ICAD, Guerbet Inc), meeting and travel expenses (British Society of Breast Radiology, European Society of Breast Imaging), board membership (International Society for Magnetic Resonance in Medicine and Society of Breast Imaging, and salary support (Radiological Society of North America). The remainder of the authors have no relevant financial or non-financial interests to disclose.
Ethics approval
This is an observational study. The Saint Louis University Institutional Review Board has confirmed that no ethical approval is required.
Additional information
Publisher’s Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Electronic supplementary material
Below is the link to the electronic supplementary material.
Rights and permissions
Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.
About this article
Cite this article
Bennett, D.L., Winter, A.M., Billadello, L. et al. Breast cancer outcomes based on method of detection in community-based breast cancer registry. Breast Cancer Res Treat 203, 215–224 (2024). https://doi.org/10.1007/s10549-023-07092-x
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10549-023-07092-x