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University of Toronto, Joint Department of Medical Imaging – University Health Network, Sinai Health System, Women's College Hospital, 610 University Avenue, M5G 2M9 Toronto, Ontario, Canada
University of Toronto, Joint Department of Medical Imaging – University Health Network, Sinai Health System, Women's College Hospital, 610 University Avenue, M5G 2M9 Toronto, Ontario, Canada
University of Toronto, Joint Department of Medical Imaging – University Health Network, Sinai Health System, Women's College Hospital, 610 University Avenue, M5G 2M9 Toronto, Ontario, Canada
University of Toronto, Joint Department of Medical Imaging – University Health Network, Sinai Health System, Women's College Hospital, 610 University Avenue, M5G 2M9 Toronto, Ontario, Canada
University of Toronto, Joint Department of Medical Imaging – University Health Network, Sinai Health System, Women's College Hospital, 610 University Avenue, M5G 2M9 Toronto, Ontario, Canada
University of Toronto, Joint Department of Medical Imaging – University Health Network, Sinai Health System, Women's College Hospital, 610 University Avenue, M5G 2M9 Toronto, Ontario, Canada
University of Toronto, Joint Department of Medical Imaging – University Health Network, Sinai Health System, Women's College Hospital, 610 University Avenue, M5G 2M9 Toronto, Ontario, Canada
University of Toronto, Joint Department of Medical Imaging – University Health Network, Sinai Health System, Women's College Hospital, 610 University Avenue, M5G 2M9 Toronto, Ontario, Canada
During the COVID-19 pandemic to limit the spread of the disease, healthcare institutions worldwide have postponed non-urgent medical care to patients.
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During the COVID-19 pandemic, mammography findings considered non-suspicious for malignancy had the investigation postponed.
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Delaying call back from mammography, whether required, can be a potential safe recommendation due to low cancer detection rate.
Abstract
Objective
To determine the frequency and distinguishing imaging characteristics of breast cancers detected on screening mammography which was initially evaluated as a probably benign lesion and the workup was delayed due to the COVID-19 pandemic.
Materials and methods
REB-approved multicenter retrospective screening mammography studies and patient's chart review carried out between February 2020 and March 2020. According to an institutional decision, the frequency and imaging findings deemed probably benign on screening mammography after review by a breast fellowship-trained radiologist with workup deferred until after the first pandemic wave plateau in late July 2020 were recorded. Results were correlated with histopathology if tissue sample performed or an uneventful 2 years follow-up. Descriptive statistical analysis was used to describe the retrieved data set.
Results
Out of 1816 mammography screening between February 2020 and March 2020, 99 women, median age 58 years (range 35–84), 99 mammography had possibly benign findings with workup delayed, and two patients, age 49 and 56, had cancers (2.02%), misinterpreted as benign findings. Both malignant cases were focal asymmetries, with pathology of invasive ductal carcinoma, 12 mm and 9 mm in size. No in-situ carcinoma was detected.
Conclusion
The low rate of cancer detected suggests that a delay callback may be a reasonable option for some likely benign findings when immediate callback is not an option, such as during a pandemic. Larger studies would be helpful to support our findings and may allow us to translate the adoption of such a model during potential future pandemic.
Clinical relevance
The results of this study may be helpful for a future situation when delaying a call back from screening mammography is again required.
COVID-19 caused by the severe acute respiratory syndrome coronavirus 2 (SARS-CoV2) that originated in Wuhan, China, in late 2019. It became a world pandemic on March 11, 2020.
As part of the operational measures adopted to limit the spread of the disease, healthcare institutions worldwide have postponed non-urgent medical care to patients.
if findings on the screening mammography were deemed to be not suspicious for malignancy, the workup of the abnormality was postponed to after the pandemic plateau, straight from screening.
It is noted that according to the BI-RADS lexicon,
short-term follow up recommendation of a probably benign lesion should be made only after a complete diagnostic breast imaging workup rather than at screening mammography. There are two major advantages to the recommended approach. The first is prompt identification of truly benign findings. A large-scale Breast Cancer Surveillance Consortium (BCSC) study has shown that recall imaging significantly increases the identification of characteristically benign lesions, thus promptly establishing a benign diagnosis, reducing anxiety, and preventing short-interval follow-up examination.
For example, prompt workup of a mass seen on screening mammography may demonstrate a benign cyst, and the patient would not need short-interval follow-up examinations. The second is ascertaining the benign features or demonstrating the suspicious features of a seeming benign lesion for follow-up or workup and more prompt identification of some rapidly growing cancers.
potentially impacting treatment and/or prognosis. Efforts to improve the specificity and cost-effectiveness of screening mammography led to the development and widespread acceptance of short-term follow-up of specific, probably benign findings. The short-term follow-up algorithm aims to reduce false-positive results while retaining a high sensitivity for early-stage breast cancer.
To our knowledge, according to the BI-RADS lexicon, there are no previous published studies that have suggested short-term follow up of screen-detected breast imaging findings without further workup. This strategy of delaying the callback without the necessary workup may fail to diagnose a malignancy mimicking a benign lesion or a cancer with an unusual appearance that could have been overlooked and for which the workup was delayed.
Therefore, this study aims to determine the frequency and distinguishing imaging characteristics of breast cancers detected on screening mammography, which was initially evaluated as a probably benign lesion and the workup was delayed due to the COVID-19 pandemic. For these lesions, short-term follow up was recommended straight from screening. The results of this study may be helpful for a future situation when delaying a callback from screening mammography is again required, e.g., in another pandemic, to avoid delay in the diagnosis and treatment of missed breast cancers.
2. Materials and methods
2.1 Study population
The institutional review board approved a retrospective case review study with a waiver of the requirement for informed consent. In compliance with REB approval, consecutive screening mammography studies of the radiology department at three tertiary care centers, Sinai Health System, University Health Network (UHN), and Women's College Hospital (WCH), affiliated with the University of Toronto, were searched. The inclusion criteria were any patient who underwent a screening mammogram immediately before and when the pandemic was announced (February 2020–March 2020), with a detected lesion requiring additional workup scheduled during March 2020, but the callback case was deferred by a breast imaging fellowship-trained radiologists with at least 5 years of experience. Patients with a negative screening mammogram, those who had lesions on screening mammogram for which the findings were considered suspicious or highly suspicious based on BI-RADS lexicon criteria
and workup was considered essential, and those patients who self-selected to delay further workup given the risk of exposure to the virus were excluded.
2.2 Data sources
The following data were obtained from our breast imaging information system (UHN's Montage Search and Analytics) and the Electronic Patient Record (EPR) to extract the clinical and imaging data.
2.3 Imaging assessment
In all mammography screening cases, full-field digital mammography (FFDM) was performed in both standard views (cranio-caudal and medio-lateral-oblique). In addition, digital breast tomosynthesis was added for baseline screening cases.
After the announcement of the COVID-19 pandemic on March 12, 2020, all screening mammograms from February and March 2020 initially scored BI-RADS 0 due to imaging findings that required additional workup, which had not yet been performed, were reviewed by a fellowship-trained breast radiologist with at least more than five years of experience as part of an institutional decision to minimize the widespread of the virus. It is noteworthy that this evaluation was considered “incomplete” since at this point no additional images such as magnification views or SPOT compression views had yet been performed. According to the literature,
three most common findings to which a probably benign assessment is applied include the presence of a solitary cluster of round or punctuated calcifications, a solitary well-circumscribed uncalcified mass or a focal asymmetry without calcification or architectural distortion. As such, these findings were considered safe to defer investigation to until after the plateau of the COVID-19 pandemic, and hence, were selected to have the callback delayed. All other imaging findings did not have investigation delayed and the callback and investigation were carried out immediately despite the COVID pandemic.
In our study, all mammograms were retrospectively reviewed independently by two breast fellowship-trained radiologists with at least more than five years of experience, who were blinded as to whether cancer had been detected. The mammographic lesions were characterized by size, density, morphological features, and visibility on two views. The discrepancy between the radiologists was resolved by consensus.
2.4 Study endpoint
The study endpoint was defined as frequency of breast cancer detected by screening mammography and their distinct imaging features, for which immediate callback was delayed due to the COVID-19 pandemic.
3. Results
Out of 1816 mammography screening studies performed between February 2020 and March 2020, 224 studies with mammogram findings (12%) were scheduled for additional work-up in March 2020, when the pandemic was announced. While no discrepancies between the original report and the review were identified, out of 224 studies, 99 studies (44%) in 99 women fulfilled the study criteria, including 99 screening mammograms (5.5%) with imaging findings considered not suspicious for malignancy, with the workup delayed to after the pandemic plateau for a few months, median 132 days (range 64–363).
The demographic and Imaging Features of the Cohort of Mammography Screening Patients with Delayed Workup due to the COVID-19 pandemic is summarized in Table 1.
Table 1Demographic and imaging features of the cohort of mammography screening patients with delayed workup due to the COVID-19 pandemic.
Characteristic
All patients (n=)
Outcomes
Benign (n=)
Malignant (n=)
Median Age (y) – (range)
58 (35–84)
59 (35–84)
52.5 (49–56)
Risk for breast cancer
Family history
12 (12.1%)
11 (11.1%)
1 (1.0%)
High-risk
1 (1.0%)
1 (1.0%)
0 (0%)
Personal history
7 (7.1%)
7 (7.1%)
0 (0%)
Not provided
79 (79.8%)
78 (78.8%)
1 (1.0%)
High-risk
Genetic mutation
0 (0%)
0 (0%)
0 (0%)
Lifetime risk >25%
1 (100%)
1 (100%)
0 (0%)
Chest irradiation
0 (0%)
0 (0%)
0 (0%)
High risk lesion
0 (0%)
0 (0%)
0 (0%)
HRT
Yes
3 (3.0%)
3 (3.0%)
0 (0%)
No
91 (91.9%)
89 (89.9%)
2 (2.0%)
Not provided
5 (5.1%)
5 (5.1%)
0 (0%)
Mammography type used in the screening
FFDM
87 (87.9%)
85 (85.9%)
2 (2.0%)
FFDM + DBT (baseline cases only)
12 (12.1%)
12 (12.1%)
0 (0%)
Breast density
A
7 (7.1%)
7 (7.1%)
0 (0%)
B
38 (38.4%)
37 (37.4%)
1 (1.0%)
C
50 (50.5%)
49 (49.5%)
1 (1.0%)
D
4 (4.0%)
4 (4.0%)
0 (0%)
Breast lesion
Mass
29 (29.3%)
29 (29.3%)
0 (0%)
Asymmetry
42 (42.4%)
42 (42.4%)
0 (0%)
Focal asymmetry
23 (23.2%)
21 (21.2%)
2 (2.0%)
Architectural distortion
0 (0%)
0 (0%)
0 (0%)
Microcalcifications
2 (2.0%)
2 (2.0%)
0 (0%)
Lymph nodes (axilla)
3 (3.0%)
3 (3.0%)
0 (0%)
Ultrasound correlate
Absent
46 (46.5%)
46 (46.5%)
0 (0%)
Present
53 (53.5%)
51 (51.5%)
2 (2.0%)
Note. Unless otherwise indicated, data are numbers of patients with percentages in parentheses.
HRT = hormone replacement therapy. FFDM – Full-field Digital Mammogram. DBT – Digital Breast Tomosynthesis. Breast Density A = Almost Entirely Fatty; Breast Density B = Scattered Fibroglandular Tissue; Breast Density C = Heterogeneous Dense; Density D = Extremely Dense.
Of the 99 women from screening mammogram, median age was 58 years (range 35–84), 12 women (12.1%) had a family history of breast cancer, 7 women (7.1%) had a personal history of breast cancer, and 1 woman (1.0%) was classified as a high-risk patient with a lifetime risk >25%. Only 3 patients (3.0%) were in use of hormone replacement therapy (HRT).
As per the BI-RADS lexicon, the overall assessment of the volume of attenuating tissues in the breast was visually assessed by the radiologists in all mammographic screening exams, with 7 (7.1%) classified as almost entirely fatty (density A), 38 (38.4%) as scattered areas of fibroglandular density (density B), 50 (50.5%) as heterogeneously dense (density C), and 4 (4.1%) as extremely dense (density D).
From the 99 breast lesions identified on mammography and deemed possibly benign, 29 (29.3%) were masses (M), 42 (42.4%) were single view asymmetries (A), 23 (23.2%) were focal asymmetries (FA), 2 (2.0%) were a group of calcifications (C) and 3 (3.0%) were prominent axillary lymph nodes (L). Additional workup was performed for these lesions after the pandemic's plateau; 53 lesions were visible on ultrasound (53.5%), and 46 had no ultrasound correlate (46,5%) and were only visible on mammography. After complete workup, 29 lesions were classified as BI-RADS 1 (29.3%), and 40 as BI-RADS 2 (40.4%). Twenty-five (25) lesions were classified as BI-RADS 3 (25.2%) with subsequent 2-year follow-up confirming benignity and, therefore, downgraded to BI-RADS 2.
However, of the 99 patients with 99 lesions, a total of five lesions (5%), 4 classified as BI-RADS 4 (4.0%) and 1 classified as BI-RADS 5 (1.0%), underwent percutaneous biopsy during follow-up, with only two (2.0%) lesions had a final pathological diagnosis of breast cancer, representing 0.11% of screening mammography studies (2 out of 1816). The imaging features of both malignant cases were focal asymmetries, size 12 mm and 9 mm respectively, corresponding to suspicious solid masses on subsequently targeted ultrasound (Fig. 1, Fig. 2). They were both invasive ductal cancers, not otherwise specified (grade 1/2); the size on final pathology was 14 mm and 16 mm, respectively. No in-situ carcinoma was detected. In one case, one benign sentinel axillary lymph node was excised; in the other, three benign sentinel axillary lymph nodes were excised. Neither case demonstrate lymphovascular invasion (Fig. 3) .
Fig. 149-year-old women, undergoing routine screening mammogram and family history of breast cancer. Only left breast is shown.
A. Left-sided digital mammogram demonstrated a focal asymmetry in the upper inner quadrant of the left breast (arrows). The imaging finding was deemed to be probably benign and the call back for workup was postponed to after the pandemic plateau.
B. Further workup with SPOT compression views demonstrated persistence of the focal asymmetry (arrows) in the upper inner left breast.
C. Targeted sonographic evaluation of the upper inner quadrant of the left breast was performed. Corresponding to the focal asymmetry on mammography there was a hypoechoic irregular mass, with angulated margins (arrows), measuring up to 12 mm. Ultrasound-guided core biopsy confirmed Invasive Ductal Carcinoma.
A. Left-sided digital mammogram demonstrated a subtle focal asymmetry in the posterior third of the central lower left breast (arrows). The imaging finding was deemed to be probably benign. Therefore, the call back for workup was postponed to after the pandemic plateau.
B. Additional SPOT compression views performed after 3–4 months, demonstrated persistence of the focal asymmetry (arrows) in the central lower left breast.
C. Targeted sonographic evaluation of the lower left breast was performed. Corresponding to the subtle focal asymmetry on the initial mammographic views, there was a hypoechoic irregular solid mass, with indistinct margins (arrows), measuring up to 9 mm. Ultrasound-guided core biopsy confirmed Invasive Ductal Carcinoma.
Our study showed a low rate (2.0%) of cancer detection after delaying the callback and suggesting a short-term follow-up of some likely benign imaging findings identified on screening mammography without immediate complete workup due to the COVID-19 pandemic. Although this was performed contrary to the recommendations of the BI-RADS lexicon, it was an institutional decision to respond to the global pandemic, in an attempt to minimize the spread the disease, even understanding that a hidden malignancy mimicking a benign lesion could be overlooked. However, our results showed that this management can be a potential safe recommendation should a future situation develop where delayed workup from screening is required.
our results demonstrate that <0.5% of women called back after an inconclusive mammogram yielded a malignant outcome. It is noteworthy that most recall result is false positive, meaning that additional testing ultimately results in a benign outcome, often revealing normal breast tissue, cysts, or other benign processes.
However, even with a low rate of malignancy, receiving a callback after a screening mammogram is not only costly, but has shown to be the major source of patient's anxiety and fear related to breast cancer screening,
A systematic review concluded that some patients report significant psychological distress from a false-positive mammogram and that it can take up to 3 years for this distress to abate.
These authors also found that these women were less likely to return for their next scheduled screening mammogram after a call back (Relative Risk (RR) = 1.2), and significantly, that this tendency was increased if they received a fine-needle (RR = 1.8) or more invasive biopsy (RR = 2.1). Therefore, efforts to reduce the number of callbacks after breast cancer screening are suggested. Based on our results, in similar situation, delaying a callback and suggesting a short-term follow-up can be used when likely benign-appearing lesions are identified in screening studies without a complete workup.
4.1 Strengths and limitations
The main strength of our study is that suggesting short-term follow-up of some likely benign imaging findings detected on screening imaging studies without immediate workup can be a safe strategy, e.g. in a pandemic. It can potentially reduce the cost of the screening, positively impacting the patient's mental health and improving the patient's adherence to breast cancer screening studies.
However, there are limitations to this study. The main limitation is its retrospective design, which may be subject to selection bias. As a result, some patients may be initially misclassified as negative screening studies and were not included in the study cohort. However, this limitation would be common to all studies in the screening setting. Additionally, given its descriptive nature and the lack of any comparison group, as only the cases where the workup was delayed were analyzed, statistical analysis is limited in this study. Moreover, our study was performed in three large academic and cancer centers where breast fellowship-trained radiologists reviewed the images, and it may not be generalizable to all centers.
5. Conclusion
The low rate of cancer detected suggests that a delay callback may be a reasonable option for some likely benign findings when immediate callback is not an option, such as during a pandemic. Larger studies would be helpful to support our findings and may allow us to translate the adoption of such a model during potential future pandemic.
CRediT authorship contribution statement
All authors contributed equally to the manuscript.
Data availability
Data generated or analyzed during the study are available from the corresponding author by request.
Declaration of competing interest
All authors have no competing interests to declare.
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