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Impact of age, race, and family history on COVID-19–related changes in breast cancer screening among the Boston mammography cohort study

  • Epidemiology
  • Published:
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Abstract

Purpose

We studied women enrolled in the Boston Mammography Cohort Study to investigate whether subgroups defined by age, race, or family history of breast cancer experienced differences in the incidence of screening or diagnostic imaging rates during the COVID-19 lockdown and had slower rebound in the incidence of these rates during reopening.

Methods

We compared the incidence of monthly breast cancer screening and diagnostic imaging rates over during the pre-COVID-19 (January 2019–February 2020), lockdown (March–May 2020), and reopening periods (June–December 2020), and tested for differences in the monthly incidence within the same period by age (< 50 vs ≥ 50), race (White vs non-White), and first-degree family history of breast cancer (yes vs no).

Results

Overall, we observed a decline in breast cancer screening and diagnostic imaging rates over the three time periods (pre-COVID-19, lockdown, and reopening). The monthly incidence of breast cancer screening rates for women age ≥ 50 was 5% higher (p = 0.005) in the pre-COVID-19 period (January 2019–February 2020) but was 19% lower in the reopening phase (June–December 2020) than that of women aged < 50 (p < 0.001). White participants had 36% higher monthly incidence of breast cancer diagnostic imaging rates than non-White participants (p = 0.018).

Conclusion

The rebound in screening was lower in women age ≥ 50 and lower in non-White women for diagnostic imaging. Careful attention must be paid as the COVID-19 recovery continues to ensure equitable resumption of care.

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Data availability

Data used here may be requested through the Boston Mammography Cohort Study research team upon request and approval of the institutional IRB. The data are not publicly available to protect the privacy of research participants.

References

  1. A Timeline of COVID-19 Developments in 2020. AJMC. Accessed April 25, 2022. https://www.ajmc.com/view/a-timeline-of-covid19-developments-in-2020

  2. Moreland A, Herlihy C, Tynan MA et al (2020) Timing of state and territorial COVID-19 stay-at-home orders and changes in population movement—United States, March 1–May 31, 2020. Morb Mortal Wkly Rep 69(35):1198–1203. https://doi.org/10.15585/mmwr.mm6935a2

    Article  CAS  Google Scholar 

  3. Vanni G, Pellicciaro M, Materazzo M et al (2020) Lockdown of breast cancer screening for COVID-19: possible scenario. In Vivo 34(5):3047–3053. https://doi.org/10.21873/invivo.12139

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  4. Freer PE (2021) The impact of the COVID-19 pandemic on breast imaging. Radiol Clin North Am 59(1):1–11. https://doi.org/10.1016/j.rcl.2020.09.008

    Article  PubMed  Google Scholar 

  5. Naidich JJ, Boltyenkov A, Wang JJ, Chusid J, Hughes D, Sanelli PC (2020) Impact of the coronavirus disease 2019 (COVID-19) pandemic on imaging case volumes. J Am Coll Radiol 17(7):865–872. https://doi.org/10.1016/j.jacr.2020.05.004

    Article  PubMed  PubMed Central  Google Scholar 

  6. Papautsky EL, Hamlish T (2020) Patient-reported treatment delays in breast cancer care during the COVID-19 pandemic. Breast Cancer Res Treat 184(1):249–254. https://doi.org/10.1007/s10549-020-05828-7

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  7. London JW, Fazio-Eynullayeva E, Palchuk MB, Sankey P, McNair C (2020) Effects of the COVID-19 pandemic on cancer-related patient encounters. JCO Clin Cancer Inform 4:657–665. https://doi.org/10.1200/CCI.20.00068

    Article  PubMed  Google Scholar 

  8. Maringe C, Spicer J, Morris M et al (2020) The impact of the COVID-19 pandemic on cancer deaths due to delays in diagnosis in England, UK: a national, population-based, modelling study. Lancet Oncol 21(8):1023–1034. https://doi.org/10.1016/S1470-2045(20)30388-0

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  9. Kaufman HW, Chen Z, Niles J, Fesko Y (2020) Changes in the number of us patients with newly identified cancer before and during the coronavirus disease 2019 (COVID-19) pandemic. JAMA Netw Open 3(8):e2017267. https://doi.org/10.1001/jamanetworkopen.2020.17267

    Article  PubMed  PubMed Central  Google Scholar 

  10. Patt D, Gordan L, Diaz M et al (2020) Impact of COVID-19 on cancer care: how the pandemic is delaying cancer diagnosis and treatment for american seniors. JCO Clin Cancer Inform 4:1059–1071. https://doi.org/10.1200/CCI.20.00134

    Article  PubMed  Google Scholar 

  11. Nyante SJ, Benefield TS, Kuzmiak CM, Earnhardt K, Pritchard M, Henderson LM (2021) Population-level impact of coronavirus disease 2019 on breast cancer screening and diagnostic procedures. Cancer 127(12):2111–2121. https://doi.org/10.1002/cncr.33460

    Article  CAS  PubMed  Google Scholar 

  12. Epstein MM, Sundaresan D, Fair M et al (2022) Trends in breast and prostate cancer screening and diagnostic procedures during the COVID-19 pandemic in central Massachusetts. Cancer Causes Control 33(10):1313–1323. https://doi.org/10.1007/s10552-022-01616-4

    Article  PubMed  PubMed Central  Google Scholar 

  13. Moraliyage H, De Silva D, Ranasinghe W et al (2021) Cancer in lockdown: impact of the COVID-19 pandemic on patients with cancer. Oncologist 26(2):e342–e344. https://doi.org/10.1002/onco.13604

    Article  CAS  PubMed  Google Scholar 

  14. Vanni G, Materazzo M, Pellicciaro M et al (2020) Breast cancer and COVID-19: the effect of fear on patients’ decision-making process. In Vivo 34:1651–1659. https://doi.org/10.21873/invivo.11957

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  15. Lo CH, Nguyen LH, Drew DA et al (2021) Race, ethnicity, community-level socioeconomic factors, and risk of COVID-19 in the United States and the United Kingdom. eClinicalMedicine. https://doi.org/10.1016/j.eclinm.2021.101029

    Article  PubMed  PubMed Central  Google Scholar 

  16. Smith AC, Woerner J, Perera R, Haeny AM, Cox JM (2022) An investigation of associations between race, ethnicity, and past experiences of discrimination with medical mistrust and COVID-19 protective strategies. J Racial Ethn Health Disparities 9(4):1430–1442. https://doi.org/10.1007/s40615-021-01080-x

    Article  PubMed  Google Scholar 

  17. Louis-Jean J, Cenat K, Njoku CV, Angelo J, Sanon D (2020) Coronavirus (COVID-19) and racial disparities: a perspective analysis. J Racial Ethn Health Disparities 7(6):1039–1045. https://doi.org/10.1007/s40615-020-00879-4

    Article  PubMed  PubMed Central  Google Scholar 

  18. Ojikutu BO, Bogart LM, Dong L (2022) Mistrust, empowerment, and structural change: lessons we should be learning from COVID-19. Am J Public Health 112(3):401–404. https://doi.org/10.2105/AJPH.2021.306604

    Article  PubMed  PubMed Central  Google Scholar 

  19. Du S, Carfang L, Restrepo E et al (2022) Patient-reported experiences of breast cancer screening, diagnosis, and treatment delay, and telemedicine adoption during COVID-19. Curr Oncol Tor Ont 29(8):5919–5932. https://doi.org/10.3390/curroncol29080467

    Article  Google Scholar 

  20. Fedewa SA, Cotter MM, Wehling KA, Wysocki K, Killewald R, Makaroff L (2021) Changes in breast cancer screening rates among 32 community health centers during the COVID-19 pandemic. Cancer 127(23):4512–4515. https://doi.org/10.1002/cncr.33859

    Article  CAS  PubMed  Google Scholar 

  21. Marcondes FO, Cheng D, Warner ET, Kamran SC, Haas JS (2021) The trajectory of racial/ethnic disparities in the use of cancer screening before and during the COVID-19 pandemic: a large US academic center analysis. Prev Med 151:106640. https://doi.org/10.1016/j.ypmed.2021.106640

    Article  PubMed  PubMed Central  Google Scholar 

  22. Velazquez AI, Hayward JH, Gregory B, Dixit N (2021) trends in breast cancer screening in a safety-net hospital during the COVID-19 pandemic. JAMA Netw Open 4(8):e2119929. https://doi.org/10.1001/jamanetworkopen.2021.19929

    Article  PubMed  PubMed Central  Google Scholar 

  23. Blair L, Warner ET, James P et al (2022) Exposure to natural vegetation in relation to mammographic density in a Massachusetts-based clinical cohort. Environ Epidemiol 6(4):e216. https://doi.org/10.1097/EE9.0000000000000216

    Article  PubMed  PubMed Central  Google Scholar 

  24. Siu AL (2016) Screening for breast cancer: U.S. preventive services task force recommendation statement. Ann Intern Med. https://doi.org/10.7326/M15-2886

    Article  PubMed  Google Scholar 

  25. CDCBreastCancer. What are the risk factors for breast cancer? Centers for disease control and prevention. Published March 9, 2022. Accessed July 19, 2022. https://www.cdc.gov/cancer/breast/basic_info/risk_factors.htm

  26. Smigal C, Jemal A, Ward E et al (2006) Trends in breast cancer by race and ethnicity: update 2006. CA Cancer J Clin 56(3):168–183. https://doi.org/10.3322/canjclin.56.3.168

    Article  PubMed  Google Scholar 

  27. Ulm K (1990) Simple method to calculate the confidence interval of a standardized mortality ratio (SMR). Am J Epidemiol 131(2):373–375. https://doi.org/10.1093/oxfordjournals.aje.a115507

    Article  CAS  PubMed  Google Scholar 

  28. Bernal JL, Cummins S, Gasparrini A (2017) Interrupted time series regression for the evaluation of public health interventions: a tutorial. Int J Epidemiol 46(1):348–355. https://doi.org/10.1093/ije/dyw098

    Article  PubMed  Google Scholar 

  29. Xiao H, Augusto O, Wagenaar BH (2021) Reflection on modern methods: a common error in the segmented regression parameterization of interrupted time-series analyses. Int J Epidemiol 50(3):1011–1015. https://doi.org/10.1093/ije/dyaa148

    Article  PubMed  Google Scholar 

  30. Linden A (2015) Conducting interrupted time-series analysis for single- and multiple-group comparisons. Stata J 15(2):480–500. https://doi.org/10.1177/1536867X1501500208

    Article  Google Scholar 

  31. Andrews DWK (1991) Heteroskedasticity and autocorrelation consistent covariance matrix estimation. Econometrica 59(3):817–858. https://doi.org/10.2307/2938229

    Article  Google Scholar 

  32. Zeileis A (2006) Object-oriented computation of sandwich estimators. J Stat Softw 16:1–16. https://doi.org/10.18637/jss.v016.i09

    Article  Google Scholar 

  33. Surviellance, Epidemiology, and end results (SEER) program. Cancer of the breast (Female)—cancer stat facts. SEER. Accessed June 9, 2022. https://seer.cancer.gov/statfacts/html/breast.html

  34. Li CI, Malone KE, Daling JR (2003) Differences in breast cancer stage, treatment, and survival by race and ethnicity. Arch Intern Med 163(1):49–56. https://doi.org/10.1001/archinte.163.1.49

    Article  PubMed  Google Scholar 

  35. Ooi SL, Martinez ME, Li CI (2011) Disparities in breast cancer characteristics and outcomes by race/ethnicity. Breast Cancer Res Treat 127(3):729–738. https://doi.org/10.1007/s10549-010-1191-6

    Article  PubMed  Google Scholar 

  36. Daly B, Olopade OI (2015) A perfect storm: how tumor biology, genomics, and health care delivery patterns collide to create a racial survival disparity in breast cancer and proposed interventions for change. CA Cancer J Clin 65(3):221–238. https://doi.org/10.3322/caac.21271

    Article  PubMed  Google Scholar 

  37. Sprague BL, Lowry KP, Miglioretti DL et al (2021) changes in mammography use by women’s characteristics during the first 5 months of the COVID-19 pandemic. JNCI J Natl Cancer Inst 113(9):1161–1167. https://doi.org/10.1093/jnci/djab045

    Article  CAS  PubMed  Google Scholar 

  38. Labaki C, Bakouny Z, Schmidt A et al (2021) Recovery of cancer screening tests and possible associated disparities after the first peak of the COVID-19 pandemic. Cancer Cell 39(8):1042–1044. https://doi.org/10.1016/j.ccell.2021.06.019

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  39. Miller-Kleinhenz JM, Collin LJ, Seidel R et al (2021) racial disparities in diagnostic delay among women with breast cancer. J Am Coll Radiol 18(10):1384–1393. https://doi.org/10.1016/j.jacr.2021.06.019

    Article  PubMed  PubMed Central  Google Scholar 

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Funding

The project was supported by the Breast Cancer Research Foundation (RT). Researchers were supported by the University of Louisville CIEHS P30 ES030283 (NCD), K01CA188075 (ETW), T32CA09001 (NCD, MOS, MEB) P30 ES000002 (JH, FL), and NIH/NCI K00 CA212222 (MEB). This manuscript is the responsibility of the authors and does not represent the official views of the National Institutes of Health.

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Authors and Affiliations

  1. Department of Epidemiology, Harvard T.H Chan School of Public Health, Boston, MA, USA

    Naiyu Chen & Michelle O. Sodipo

  2. Biostatistics Center, Massachusetts General Hospital, Boston, MA, USA

    David Cheng

  3. Department of Population Health Sciences, Huntsman Cancer Institute, University of Utah Intermountain Health, Salt Lake City, UT, USA

    Mollie E. Barnard

  4. Slone Epidemiology Center, Boston University Chobanian & Avedisian School of Medicine, Boston, MA, USA

    Mollie E. Barnard

  5. Department of Epidemiology and Population Health, School of Public Health and Information Sciences, University of Louisville, Louisville, KY, USA

    Natalie C. DuPre

  6. Department of Population Health Sciences, Weill Cornell Medical, New York, NY, USA

    Rulla M. Tamimi

  7. Clinical Translational Epidemiology Unit, Department of Medicine, Mongan Institute, Massachusetts General Hospital, 55 Fruit Street, Boston, MA, 02114, USA

    Erica T. Warner

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  1. Naiyu Chen
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Corresponding author

Correspondence to Erica T. Warner.

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Competing interests

Mollie E. Barnard reports personal fees from Epi Excellence LLC outside of the submitted work. All other authors have no relevant financial interests to disclose.

Ethical approval

The study was approved by the Mass General Brigham Human Research Committee, the Institutional Review Board (IRB) of Mass General Brigham. Participants provided written informed consent prior to joining the Boston Mammography Cohort Study.

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Written informed consent was obtained from all individual participants included in the study.

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Chen, N., Cheng, D., Sodipo, M.O. et al. Impact of age, race, and family history on COVID-19–related changes in breast cancer screening among the Boston mammography cohort study. Breast Cancer Res Treat 202, 335–343 (2023). https://doi.org/10.1007/s10549-023-07083-y

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