Abstract
The impact of the COVID-19 pandemic on health care is vast and continuing to unfold. As much progress related to breast cancer has resulted from screening and public health measures, we analyzed the stage at which patients with breast cancer presented for surgical consultation from 2019 to 2021. From 2019 to 2021, retrospective analysis was performed on breast cancer patients, comparing differences in patient demographics and cancer stage at diagnosis pre- and post-recommendation (COVID-era) to postpone mammographic screening on March 26, 2020. Proportion analysis was performed to identify similar percentages for each stage, and a weighed stage severity score with sign test was crafted to compare overall stage for a given year. The study included 1107 breast cancer patients from breast cancer surgery registry. These groups were similar demographically. We performed analysis comparing pre-COVID and COVID-era stage severity score. This showed a statistically higher stage at presentation when comparing pre-COVID to COVID-era data (P = .0027). Additionally, we identified a higher rate of stage 3 at presentation or greater in the COVID-era with 7.79% pre-COVID vs 12.3% COVID-era (P = .016). We found that in comparing pre-COVID to COVID-era data that breast cancer patients presented with higher stages, in particular, stage 3 or higher stage disease. This analysis reveals the impact of COVID on the multidisciplinary treatment of breast cancer patients. Additional efforts are needed to address the stage migration, the disproportionate burden of disease, and the access to care.
Keywords: breast, special topics
Key Takeaways
• Breast cancer patients in a single institution retrospective analysis (2019-2021) are presented with higher stage of breast cancer in COVID-era when compared to pre-COVID, as measured by severity score analysis.
• A larger proportion of breast cancer patients presented with stage 3 or greater disease in COVID-era compared to pre-COVID.
• This increase in stage of breast cancer in COVID-era compared to pre-COVID did not correspond with any significant shift in demographics.
Introduction
The impact of the COVID-19 pandemic has been far reaching in many aspects of health care, particularly oncologic detection and cancer care. To reduce exposures to both patients and providers, in March 2020, the American Society of Breast Surgeons along with the American College of Radiology recommended significant restrictions on breast cancer screening. 1 The influence of COVID extended from the burden of the disease itself to unintended consequences of delay in care for other conditions, particularly related to breast cancer. 2 Significant reduction in disease burden has occurred with early detection and management of breast cancer via mammography. 3 The temporary suspension of breast cancer screening has been shown on population modeling to lead to advanced disease presentation. 2 However, it was unclear if this modeling and public health prediction would be evident in our institution. We identified a substantial decrease in screening and diagnostic mammograms, yet stage was not statistically different by year. 3 In attempts to address ongoing concerns with regards to breast cancer care, there was a call to action to pursue longitudinal studies investigating breast cancer outcomes after the initial impact of the COVID-19 pandemic. 4
As such, we analyzed additional data from 2019 to 2021 with subsequent analyses to better understand our stage specific longitudinal data regards to breast cancer. As much of the progress in reducing morbidity and mortality related to breast cancer has resulted from adoption of screening and public health measures, we analyzed the stage at which patients with breast cancer presented for surgical consultation from 2019 to 2021.
Materials and Methods
Retrospective analysis was performed between 2019 and 2021 on breast cancer patients, comparing differences in patient demographics and cancer stage at diagnosis pre- and post-recommendation to postpone mammographic screening on March 26, 2020.
Proportion analysis was performed to identify similar percentages for each stage, and a weighed stage severity score with sign test was crafted to compare overall stage in the pre-COVID as compared to COVID-era. Study analysis design and test statistic selection were performed with guidance from Wake Forest Clinical and Translational Science Institute. Statistical significance was with P-value less than or equal to .05 with Z-test statistics.
Results
The study included 1107 breast cancer patients who were identified in the breast cancer surgery registry utilized with TNM classification for breast cancer stage. Four hundred and forty-nine patients were included in the pre-pandemic phase from 2019 to March 26, 2020 and 658 patients since the COVID pandemic era from March 26, 2020 to 2021.
These groups were similar demographically (age and race, specifically); the average age was 63 in pre-COVID and 61 in the COVID-era. The majority of patients were female (pre- 99.6% vs 99.5% COVID-era). In both groups, the majority of patients were white, non-Hispanics (78.2% pre- vs 79% COVID-era); 19.7% black patients in pre- vs 18.8% COVID-era; 1.36% Asian/other patients in pre- vs 1.12% COVID-era; and 1.0% white, Hispanic patients in pre- vs 0.89% COVID-era. Furthermore, we did not identify any statistically significant difference representation by race in the pre-COVID as compared to the COVID-era. (Table 1)
Table 1.
Stage of Breast Cancer.
| Stage | Pre-COVID by % (n) | COVID-Era % (n) | P-Value, Proportion Analysis (P < .05) |
|---|---|---|---|
| 0 | 17% (77) | 15% (97) | P = .28 |
| 1a | 55% (248) | 46% (301) | P = .002 |
| 1b | 11% (49) | 15% (99) | P = .0477 |
| 2a | 5.8% (26) | 7.4% (49) | P = .28 |
| 2b | 3.1% (14) | 4.7% (31) | P = .19 |
| 3a | .89% (4) | .91% (6) | P = .97 |
| 3b | .67% (3) | 4.0% (26) | P = .0008 |
| 3c | 0% (0) | 1.2% (8) | P = .019 |
| 4 | 6.2% (28) | 6.2% (41) | P = 1 |
| Total | 100% (449) | 100% (658) |
Pre-COVID as compared to COVID-era by number of cases (n) as well as percentage (%) with the proposition analysis p-value, p <0.05 indicates statistical significance with bold text.
We performed analysis comparing pre-COVID and COVID-era stage severity score. This showed a statistically higher stage presentation of disease when comparing pre-COVID to COVID-era data (P = .0027). Specifically, a higher severity score was noted in COVID-era with 1.51 as compared to 1.33 pre-COVID (Z = 3). While we did not analyze mortality, this unfortunate trend is mirrored in a projection of data estimating 10,000 deaths attributed to advanced stage of breast cancer secondary to COVID-19 and impact on mammography. 5
We then performed stage-specific analyses from pre-COVID to COVID-era in attempts to identify where the difference in stage presentation was located, as seen in Figure 1. It was in this sub-analysis, we identified a higher rate of stage 3 disease presentation or greater in the COVID-era with 7.79% pre-vs 12.3% since COVID (P = .016).
Figure 1.
Stage of Breast Cancer by Percentage, Pre-COVID and COVID-era.
Furthermore, we found a higher rate of Stage IB patients in COVID-era as compared to pre-COVID (P = .048). We would propose that in addition to a stage migration, this metric suggests an impact of delay in screening. It is possible that this increase in stage IB presentation contributed to surgery selection amongst likely those with hormone-receptive positive disease, such as mastectomy over lumpectomy. Additionally, we noted that there was a decrease in stage IA disease from pre-COVID to COVID-era suggestive of a decrease in this primarily screening detection lesion (P = .002).
Discussion
In attempts to understand the ongoing impact to COVID on breast cancer, we analyzed whether our patients presented with advanced disease. Initial institution data revealed that mammography rates decreased but stage of disease at presentation was not different by year. 3 However, in further analysis, we found that in comparing pre-COVID to COVID-era data, breast cancer patients presented with higher stages, in particular, stage 3 or greater in the COVID-era.
Other authors have analyzed the impact of COVID-19 on breast care. For instance, Alagoz et al attempted to qualify this delay in symptomatic cancer diagnosis. 4 By 2030, the model projects 950 (model range = 860-1297) cumulative excess breast cancer deaths related to reduced screening and 1314 (model range = 266-1325) associated with delayed diagnosis of symptomatic cases. 4 The authors concluded that the initial pandemic-related disruptions in breast cancer care will have a small long-term effect on breast cancer mortality. 4 More data needs to be collected to evaluate future impact on morbidity and mortality related to breast cancer in this time period.
We also analyzed race with regards to overall representation in the breast cancer registry. There was no difference in the patient composition between the pre-COVID and COVID-era groups. Fascano et al found that certain racial groups, such as black and Hispanic females, were less likely to undergo screening mammography. 5 Furthermore, studies have identified that the burden of disease of those impacted by COVID-19 was 3x hospitalist rate and 2x higher mortality amongst black patients compared to white patients from the virus itself.6,7 These factors could worsen disparity over time, and ongoing research could further identify perpetuating factors.
Additionally, this analysis does not address other factors that impacted breast cancer care during this time. Many patients feared coming into the hospital to seek care. Also, patients lost their health care insurance during the pandemic which financially hindered them to seek care. Fedewa et al found that unemployed adults (2000-2018) were 4 times more likely to lack insurance than employed adults (41.4% vs 10.0%; P < .001). 8 Unemployed adults had a significantly lower up-to-date prevalence of screening for breast cancer (67.8% vs 77.5%; P < .001). This disparity was eliminated after accounting for health insurance. 8 Other qualitative factors such as transition to virtual delivery of care, restriction of visitors, and expedited discharges also require attention for the patient perception of their care during the COVID-19 pandemic. 9
The limitation of the study is that it is from a single institution in a retrospective data set. The effects of the pandemic are just able to be analyzed. However, other studies such as Zhou et al utilize a pre-COVID and COVID-era approach to this change despite short-term follow up. 10 Future investigations will need to continue to evaluate the ongoing impacts of increase in care on our breast cancer patients.
Overall, this analysis reveals increase in stage migration during the COVID pandemic at a single institution. A national examination of this phenomenon is warranted. Future steps include investigation into strategies to address any disproportionate burden of disease as well as enhanced re-entry to breast cancer screening. Further efforts are needed to address the stage migration, the disproportionate burden of disease, and the access to care.
Footnotes
The author(s) declared no potential conflicts of interest with respect to the research, authorship, and/or publication of this article.
Funding: The author(s) received no financial support for the research, authorship, and/or publication of this article.
ORCID iD
Allison Perko https://orcid.org/0000-0003-2108-9254
References
- 1.The American Society of Breast Surgeons. The American College of Radiology . Joint Statement on Breast Screening Exams during the Covid-19 Pandemic; 2021. https://www.breastsurgeons.org/news/?id=45. Accessed on January 7, 2023. [Google Scholar]
- 2.Maringe C, Spicer J, Morris M, et al. 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. 2020;21(8):1023-1034. doi: 10.1016/S1470-2045(20)30388-0 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 3.Cairns A, Jones VM, Cronin K, et al. Impact of the COVID-19 pandemic on breast cancer screening and operative treatment. Am Surg. 2022;88(6):1051-1053. doi: 10.1177/00031348221087920 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 4.Alagoz O, Lowry KP, Kurian AW, et al. Impact of the COVID-19 pandemic on breast cancer mortality in the US: Estimates from collaborative simulation modeling. J Natl Cancer Inst. 2021;113(11):1484-1494. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 5.Fasano GA, Bayard S, Bea VJ. Breast cancer disparities and the COVID-19 pandemic. Curr Breast Cancer Rep. 2022;14(4):192-198. doi: 10.1007/s12609-022-00458-y [DOI] [PMC free article] [PubMed] [Google Scholar]
- 6.Cavallo J. How delays in screening and early cancer diagnosis amid the COVID-19 pandemic may result in increased cancer mortality. The ASCO Post. https://ascopost.com/issues/september-10-2020/how-delays-in-screening-and-early-cancer-diagnosis-amid-the-covid-19-pandemic-may-result-in-increased-cancer-mortality/. Accessed January 7, 2023. [Google Scholar]
- 7.McDowell S. Breast Cancer Death Rates Are Highest for Black Women-Again: Breast Cancer Facts and Figures, 2022-2024. Atlanta, GA: American Cancer Society. https://www.cancer.org/latest-news/breast-cancer-death-rates-are-highest-for-black-women-again.html. Published October 3, 2022. Accessed January 7, 2023. [Google Scholar]
- 8.Fedewa SA, Yabroff KR, et al. Unemployment and cancer screening: Baseline estimates to inform health care delivery in the context of COVID-19 economic distress. Cancer. 2022;128(4):737-745. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 9.Tai DBG, Shah A, Doubeni CA, Sia IG, Wieland ML. The disproportionate impact of COVID-19 on racial and ethnic minorities in the United States. Clin Infect Dis. 2020;72(14):703-706. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 10.Zhou JZ, Kane S, Ramsey C, et al. Comparison of early- and late-stage breast and colorectal cancer diagnoses during vs before the COVID-19 pandemic. JAMA Netw Open. 2022;5(2):e2148581. doi: 10.1001/jamanetworkopen.2021.48581 [DOI] [PMC free article] [PubMed] [Google Scholar]

