Abstract
Purpose
Molecular testing is a critical component of breast cancer care used to identify the presence of estrogen and/or progesterone receptors (jointly hormone receptors—HRs) and the expression of human epidermal growth factor 2 (HER2) on a tumor. Our objective was to characterize trends and predictors of lack of molecular testing among female breast cancer patients overall and by sociodemographic characteristics.
Methods
We examined data on female breast cancer patients diagnosed between 2010 and 2016 from Surveillance Epidemiology and End Results-18. Joinpoint regression analyses assessed annual percent change (APC) in lack of ER, PR, or HER2 testing. Multivariable, multilevel logistic regression models identified factors associated with lack of molecular testing.
Results
A nominally lower proportion of rural patients did not receive molecular testing (e.g., 1.8% in rural vs. 2.3% in urban for HER2). For all tests, a higher proportion of Hispanic and non-Hispanic Black women were not tested. Across all characteristics, improvement in testing was noted, although disparities among groups remained. For example, lack of HER2 testing improved from 3.2 to 1.7% in White patients (APC = − 10.05) but was consistently higher in Black patients 3.9 to 2.3% (APC = − 8.21). Multivariable, multilevel models showed that older, non-Hispanic Black, and unpartnered women were at greater odds of not receiving molecular testing.
Conclusions
While lack of molecular testing of breast cancer patients is relatively rare, racial/ethnic, insurance status, and age-related disparities have been identified. To reduce testing and downstream treatment and outcome disparities, it is imperative for all breast cancer patients to receive molecular testing.
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Data availability
Enquiries about data availability should be directed to the authors.
References
American Cancer Society, Atlanta. Cancer Facts & Figures 2021. https://www.cancer.org/content/dam/cancer-org/research/cancer-facts-and-statistics/annual-cancer-facts-and-figures/2021/cancer-facts-and-figures-2021.pdf. Accessed 17 Sept 2021
USCS data visualizations. https://gis.cdc.gov/grasp/USCS/DataViz.html. Accessed 27 July 2021
Adams SA, Butler WM, Fulton J, Heiney SP, Williams EM, Delage AF, Khang L, Hebert JR (2012) Racial disparities in breast cancer mortality in a multi-ethnic cohort in the Southeast. Cancer 118(10):2693–2699. https://doi.org/10.1002/cncr.26570
Weaver K, Strom C, Johnson A, Lee J, Sutfin EL (2016) Call to action: addressing rural cancer health disparities, Alexandria, Virginia. Community anti-drug coalitions of america, geographic health equity alliance. http://www.nohealthdisparities.org/.
Charlton M, Schlichting J, Chioreso C, Ward M, Vikas P (2015) Challenges of rural cancer care in the United States. Oncology 29(9):633–640
Meilleur A, Subramanian S, Plascak JJ, Fisher JL, Paskett ED, Lamont EB (2013) Rural residence and cancer outcomes in the US: issues and challenges. Cancer Epidemiol Biomarkers Prevent. https://doi.org/10.1158/1055-9965.EPI-13-0404
Jackson DK, Li Y, Eskander MF, Tsung A, Oppong BA, Bhattacharyya O, Paskett ED, Obeng-Gyasi S (2021) Racial disparities in low-value surgical care and time to surgery in high-volume hospitals. J Surg Oncol 123(2):676–686. https://doi.org/10.1002/jso.26320
Babatunde OA, Eberth JM, Felder TM, Moran R, Hughes-Halbert C, Truman S, Hebert JR, Heiney S, Adams SA (2022) Racial disparities and diagnosis-to-treatment time among patients diagnosed with breast cancer in South Carolina. J Racial Ethn Health Disparities 9(1):124–134. https://doi.org/10.1007/s40615-020-00935-z
Heiney SP, Truman S, Babatunde OA, Felder TM, Eberth JM, Crouch E, Wickersham KE, Adams SA (2020) Racial and geographic disparities in endocrine therapy adherence among younger breast cancer survivors. Am J Clin Oncol 43(7):504–509. https://doi.org/10.1097/COC.0000000000000696
Zardavas D, Irrthum A, Swanton C, Piccart M (2015) Clinical management of breast cancer heterogeneity. Nat Rev Clin Oncol 12(7):381–394. https://doi.org/10.1038/nrclinonc.2015.73
Samson ME, Porter NG, Hurley DM, Adams SA, Eberth JM (2016) Disparities in breast cancer incidence, mortality, and quality of care among african american and european american women in South Carolina. Southern Med J 109(1):24–30
Amend K, Hicks D, Ambrosone CB (2006) Breast cancer in African-American women: Differences in tumor biology from European-American women. Can Res 66(17):8327–8330. https://doi.org/10.1158/0008-5472.CAN-06-1927
Wolff AC, Hammond MEH, Allison KH, Harvey BE, Mangu PB, Bartlett JMS, Bilous M, Ellis IO, Fitzgibbons P, Hanna W, Jenkins RB, Press MF, Spears PA, Vance GH, Viale G, McShane LM, Dowsett M (2018) Human epidermal growth factor receptor 2 testing in breast cancer: american society of clinical oncology/college of american pathologists clinical practice guideline focused update. J Clin Oncol 36(20):2105–2122. https://doi.org/10.1200/JCO.2018.77.8738
Hagemann IS (2016) Molecular testing in breast cancer: a guide to current practices. Arch Pathol Lab Med 140(8):815–824. https://doi.org/10.5858/arpa.2016-0051-RA
Anderson WF, Rosenberg PS, Katki HA (2014) Tracking and evaluating molecular tumor markers with cancer registry data: HER2 and breast cancer. J Natl Cancer Instit 106(5):dju93
Allison KH, Hammond MEH, Dowsett M, McKernin SE, Carey LA, Fitzgibbons PL, Hayes DF, Lakhani SR, Chavez-MacGregor M, Perlmutter J, Perou CM, Regan MM, Rimm DL, Symmans WF, Torlakovic EE, Varella L, Viale G, Weisberg TF, McShane LM, Wolff AC (2020) Estrogen and progesterone receptor testing in breast cancer: ASCO/CAP guideline update. J Clin Oncol 38(12):1346–1366. https://doi.org/10.1200/JCO.19.02309
DeSantis CE, Ma J, Gaudet MM, Newman LA, Miller KD, Goding Sauer A, Jemal A, Siegel RL (2019) Breast cancer statistics, 2019. CA A Cancer J Clin 69(6):438–451. https://doi.org/10.3322/caac.21583
Romond EH, Perez EA, Bryant J, Suman VJ, Geyer CE, Davidson NE, Tan-Chiu E, Martino S, Paik S, Kaufman PA, Swain SM, Pisansky TM, Fehrenbacher L, Kutteh LA, Vogel VG, Visscher DW, Yothers G, Jenkins RB, Brown AM, Wolmark N (2005) Trastuzumab plus adjuvant chemotherapy for operable HER2-positive breast cancer. N Engl J Med 353(16):1673–1684. https://doi.org/10.1056/NEJMoa052122
Early Breast Cancer Trialists’ Collaborative Group (EBCTCG) (2005) Effects of chemotherapy and hormonal therapy for early breast cancer on recurrence and 15-year survival: An overview of the randomized trials. Lancet 365(9472):1687–1717. https://doi.org/10.1016/S0140-6736(05)66544-0
Rutqvist LE, Johansson LE, Stockholm Breast Cancer Study Group (2007) Long-term follow-up of the randomized Stockholm trial on adjuvant tamoxifen among postmenopausal patients with early-stage breast cancer. Acta Oncol 46(2):133–145. https://doi.org/10.1080/02841860601034834
Kurian AW, Carlson RW (2010) Principles of breast cancer therapy. In: Li C (Ed), Breast Cancer Epidemiology (pp 371–388). Springer. https://doi.org/10.1007/978-1-4419-0685-4_17.
Kalimutho M, Parsons K, Mittal D, López JA, Srihari S, Khanna KK (2015) Targeted therapies for triple-negative breast cancer: combating a stubborn disease. trends Pharmacol Sci 36(12):822–846. https://doi.org/10.1016/j.tips.2015.08.009
McCann KE, Hurvitz SA, McAndrew N (2019) Advances in targeted therapies for triple-negative breast cancer. Drugs 79(11):1217–1230. https://doi.org/10.1007/s40265-019-01155-4
Kohler BA, Sherman RL, Howlader N, Jemal A, Ryerson AB, Henry KA, Boscoe FP, Cronin KA, Lake A, Noone A-M, Henley SJ, Eheman CR, Anderson RN, Penberthy L (2015) Annual report to the nation on the Status of Cancer, 1975–2011, featuring incidence of breast cancer subtypes by race/ethnicity, poverty, and state. J Natl Cancer Instit 107(6):djv048. https://doi.org/10.1093/jnci/djv048
Howlader N, Altekruse SF, Li CI, Chen VW, Clarke CA, Ries LAG, Cronin KA (2014) US incidence of breast cancer subtypes defined by joint hormone receptor and HER2 status. J Natl Cancer Instit 106(5):dju055. https://doi.org/10.1093/jnci/dju055
Chen L, Li CI (2015) Racial disparities in breast cancer diagnosis and treatment by hormone receptor and HER2 status. Cancer Epidemiol Biomark Prev 24(11):1666–1672. https://doi.org/10.1158/1055-9965.EPI-15-0293
Howlader N, Cronin KA, Kurian AW, Andridge R (2018) Differences in breast cancer survival by molecular subtypes in the United States. Cancer Epidemiol Biomark Prev 27(6):619–626. https://doi.org/10.1158/1055-9965.EPI-17-0627
Zahnd WE, Sherman RL, Klonoff-Cohen H, McLafferty SL, Farner S, Rosenblatt KA (2019) Disparities in breast cancer subtypes among women in the lower Mississippi Delta Region states. Cancer Causes Control 30(6):591–601. https://doi.org/10.1007/s10552-019-01168-0
Krieger N, Chen JT, Ware JH, Kaddour A (2008) Race/ethnicity and breast cancer estrogen receptor status: impact of class, missing data, and modeling assumptions. Cancer Causes Control 19(10):1305–1318. https://doi.org/10.1007/s10552-008-9202-1
Kim HM, Goodman M, Kim BI, Ward KC (2011) Frequency and determinants of missing data in clinical and prognostic variables recently added to SEER. J Registry Manag 38(3):120–131
Pensa M, Swede H, Brockmeyer JA, Gregorio DI (2009) Patterns of HER2 testing in the management of primary breast cancer. Cancer Epidemiol 33(2):113–117. https://doi.org/10.1016/j.canep.2009.06.010
Lund MJ, Butler EN, Hair BY, Ward KC, Andrews JH, Oprea-Ilies G, Bayakly AR, O’Regan RM, Vertino PM, Eley JW (2010) Age/race differences in HER2 testing and in incidence rates for breast cancer triple subtypes: a population-based study and first report. Cancer 116(11):2549–2559. https://doi.org/10.1002/cncr.25016
Surveillance, Epidemiology, and End Results (SEER) Program (www.seer.cancer.gov) SEER*Stat Database: Incidence - SEER 13 Regs Research Data, Nov 2018 Sub (1992–2016) <Katrina/Rita Population Adjustment> - Linked To County Attributes - Total U.S., 1969–2017 Counties, National Cancer Institute, DCCPS, Surveillance Research Program, released April 2019, based on the November 2018 submission.
Whaley AL (2003) Ethnicity/race, ethics, and epidemiology. J Natl Med Assoc 95(8):736–742
USDA ERS - Rural-Urban Continuum Codes (2021) https://www.ers.usda.gov/data-products/rural-urban-continuum-codes.aspx. Accessed 27 July 2021
Zahnd WE, Jenkins WD, James AS, Izadi SR, Steward DE, Fogleman AJ, Colditz GA, Brard L (2018) Utility and generalizability of multistate, population-based cancer registry data for rural cancer surveillance research in the United States. Cancer Epidemiol Biomark Prev 27(11):1252–1260. https://doi.org/10.1158/1055-9965.EPI-17-1087
Street W “Breast Cancer Facts & Figures 2019–2020,” 2020, 44. https://www.cancer.org/content/dam/cancer-org/research/cancer-facts-and-statistics/breast-cancer-facts-and-figures/breast-cancer-facts-and-figures-2019-2020.pdf. Accessed 24 Sept 2021
Chiu AS, Thomas P, Killelea BK, Horowitz N, Chagpar AB, Lannin DR (2017) Regional variation in breast cancer surgery: results from the National Cancer Database (NCDB). Am J Surg 214(5):907–913. https://doi.org/10.1016/j.amjsurg.2017.07.008
Yusuf RA, Rogith D, Hovick SRA, Peterson SK, Burton-Chase AM, Fellman BM, Li Y, McKinney C, Bernstam EV, Meric-Bernstam F (2015) Attitudes toward molecular testing for personalized cancer therapy. Cancer 121(2):243–250. https://doi.org/10.1002/cncr.28966
Camacho FT, Tan X, Alcalá HE, Shah S, Anderson RT, Balkrishnan R (2017) Impact of patient race and geographical factors on initiation and adherence to adjuvant endocrine therapy in medicare breast cancer survivors. Medicine 96(24):e7147. https://doi.org/10.1097/MD.0000000000007147
Carey LA, Perou CM, Livasy CA, Dressler LG, Cowan D, Conway K, Karaca G, Troester MA, Tse CK, Edmiston S, Deming SL, Geradts J, Cheang MCU, Nielsen TO, Moorman PG, Earp HS, Millikan RC (2006) Race, breast cancer subtypes, and survival in the Carolina Breast Cancer Study. JAMA 295(21):2492–2502. https://doi.org/10.1001/jama.295.21.2492
Durbecq V, Ameye L, Veys I, Paesmans M, Desmedt C, Sirtaine N, Sotiriou C, Bernard-Marty C, Nogaret JM, Piccart M, Larsimont D (2008) A significant proportion of elderly patients develop hormone-dependant “luminal-B” tumours associated with aggressive characteristics. Crit Rev Oncol Hematol 67(1):80–92. https://doi.org/10.1016/j.critrevonc.2007.12.008
Jenkins EO, Deal AM, Anders CK, Prat A, Perou CM, Carey LA, Muss HB (2014) Age-specific changes in intrinsic breast cancer subtypes: a focus on older women. Oncologist 19(10):1076–1083. https://doi.org/10.1634/theoncologist.2014-0184
Tesarova P (2012) Breast cancer in the elderly-Should it be treated differently? Rep Pract Oncol Radiother 18(1):26–33. https://doi.org/10.1016/j.rpor.2012.05.005
Shachar SS, Hurria A, Muss HB (2016) Breast cancer in women older than 80 years. J Oncol Pract 12(2):123–132. https://doi.org/10.1200/JOP.2015.010207
Smith BD, Smith GL, Hurria A, Hortobagyi GN, Buchholz TA (2009) Future of cancer incidence in the United States: burdens upon an aging, changing nation. J Clin Oncol 27(17):2758–2765. https://doi.org/10.1200/JCO.2008.20.8983
Weir HK, Thompson TD, Soman A, Møller B, Leadbetter S (2015) The past, present, and future of cancer incidence in the United States: 1975 through 2020. Cancer 121(11):1827–1837. https://doi.org/10.1002/cncr.29258
Rugo HS, Rumble RB, Macrae E, Barton DL, Connolly HK, Dickler MN, Fallowfield L, Fowble B, Ingle JN, Jahanzeb M, Johnston SRD, Korde LA, Khatcheressian JL, Mehta RS, Muss HB, Burstein HJ (2016) Endocrine therapy for hormone receptor-positive metastatic breast cancer: american society of clinical oncology guideline. J Clin Oncol 34(25):3069–3103. https://doi.org/10.1200/JCO.2016.67.1487
Neale AV, Tilley BC, Vernon SW (1986) Marital status, delay in seeking treatment and survival from breast cancer. Social Sci Med 23(3):305–312. https://doi.org/10.1016/0277-9536(86)90352-7
Osborne C, Ostir GV, Du X, Peek MK, Goodwin JS (2005) The influence of marital status on the stage at diagnosis, treatment, and survival of older women with breast cancer. Breast Cancer Res Treat 93(1):41–47. https://doi.org/10.1007/s10549-005-3702-4
Martínez ME, Unkart JT, Tao L, Kroenke CH, Schwab R, Komenaka I, Gomez SL (2017) Prognostic significance of marital status in breast cancer survival: a population-based study. PLoS ONE 12(5):e0175515. https://doi.org/10.1371/journal.pone.0175515
Dreyer MS, Nattinger AB, McGinley EL, Pezzin LE (2018) Socioeconomic status and breast cancer treatment. Breast Cancer Res Treat 167(1):1–8. https://doi.org/10.1007/s10549-017-4490-3
Reeder-Hayes K, Peacock Hinton S, Meng K, Carey LA, Dusetzina SB (2016) Disparities in use of human epidermal growth hormone receptor 2-targeted therapy for early-stage breast cancer. J Clin Oncol 34(17):2003–2009. https://doi.org/10.1200/JCO.2015.65.8716
Reichman ME, Altekruse S, Li CI, Chen VW, Deapen D, Potts M, Wu X-C, Morrell D, Hafterson J, Phipps AI, Harlan LC, Ries LG, Edwards BK (2010) Feasibility study for collection of HER2 data by National Cancer Institute (NCI) Surveillance, Epidemiology, and End Results (SEER) Program central cancer registries. Cancer Epidemiol Biomark Prev 19(1):144–147. https://doi.org/10.1158/1055-9965.EPI-09-0807
Boffa DJ, Rosen JE, Mallin K, Loomis A, Gay G, Palis B, Thoburn K, Gress D, McKellar DP, Shulman LN, Facktor MA, Winchester DP (2017) Using the national cancer database for outcomes research: a review. JAMA Oncol 3(12):1722–1728. https://doi.org/10.1001/jamaoncol.2016.6905
Acknowledgments
This study was funded by an American Cancer Society Institutional Research Grant to the University of South Carolina (PI: Zahnd). Oluwole A. Babatunde was supported by a National Cancer Institute’s F99/K00 Fellowship grant (CA 222722) as principal investigator.
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The fund was provided by American Cancer Society through and Instiutional Research Grant to the University of South Carolina.
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WEZ conceptualized and designed the study, co-led the drafting of the article, and assisted with the data analysis and interpretation. RR co-led the drafting of the article and performed the data analysis. SAA contributed to conceptualization and design of the study, contributed to data interpretation, and provided critical review and editing of the article draft. OAB contributed to data interpretation and provided critical review and editing of the article draft.
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The University of South Carolina’s Institutional Review Board determined this study to be “not human subject research” due to the de-identified nature of the data.
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Zahnd, W.E., Ranganathan, R., Adams, S.A. et al. Sociodemographic disparities in molecular testing for breast cancer. Cancer Causes Control 33, 843–859 (2022). https://doi.org/10.1007/s10552-022-01575-w
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DOI: https://doi.org/10.1007/s10552-022-01575-w