Yield of Surveillance Mammography in Autologous Reconstructed Breasts After Mastectomy: A Tertiary Care Study

Abstract

French

Objective:

The primary outcome of this study was to determine the cancer detection rate (CDR) of surveillance mammography in the autologous reconstructed breast post mastectomy.

Materials and Methods:

In this research ethics board approved retrospective study, chart review was performed at a single academic centre to identify women who had undergone mastectomy with AR who underwent annual mammography surveillance of both ipsilateral (reconstructed) and contralateral breasts with a minimum 1 year of clinical and imaging follow-up between 2012 and 2020. Clinical information, imaging, method of detection, pathology and immunohistochemical findings, location of ipsilateral malignancy, and the interval between mastectomy and loco-regional recurrence (LRR) were calculated. The CDR of surveillance mammography, interval cancers, abnormal recall rate (ACR), and PPV1, PPV2, and PPV3 were determined.

Results:

We included 2127 screening examinations in 371 patients median age was 58 years (25-86 years). The average number of screens per patient was 5.73 (range: 1-17). No screen-detected cancers (CDR 0/1000) were identified in the ipsilateral breast for an abnormal recall rate of 0.42% (9/2127) and 3 benign biopsies. Three interval cancers were detected clinically in the ipsilateral breast.

Conclusion:

No benefit was found for surveillance mammography and detection of non-palpable cancers in autologous reconstructed breasts post mastectomy in this study. Further multicentric studies with larger number of patients may be needed for confirmation of lack of benefit.

Keywords

breast cancer screening post-mastectomy surveillance autologous breast reconstruction breast cancer detection rate mammographic screening

Introduction

In the era of personalised cancer therapy, breast reconstructive surgery rates have shown a steady rise over the past decade globally.^1,2 Broadly classified into 2 types; breast reconstruction can be implant based or performed using an autologous graft. Majority of breast reconstructive surgeries are implant based.^1,3-6 However, autologous reconstruction (AR) still accounts for a substantial proportion of cases ranging from 19% to 50%.^1,7 More than one third patients who can be treated with breast conserving surgery opt for mastectomy.⁸ Ongoing concerns regarding implant safety, development in microsurgical techniques, introduction of DIEP flaps to reduce abdominal morbidity and personal preferences related to autologous grafts providing a more natural mould have been attributed to increasing rates of AR.^4,5,8-11

The changes in trends concerning the curative management of early breast cancer have not been reflected in screening recommendations for this population. Although ipsilateral surveillance mammographic surveillance is not considered appropriate for women with post mastectomy women with implant reconstruction,⁵ the recommendations for ipsilateral surveillance mammography in patients treated with AR are equivocal.^5-7 There is considerable disparity in the guidelines for screening of the autologous breast at national/organisational levels. The National Comprehensive Cancer Network recommends against routine imaging surveillance of the autologous breast² whereas the American College of Radiology considers it as “may be appropriate.”⁵ Within Canada, breast cancer follow-up care clinical guidance summary suggests that there is insufficient evidence and reports low rates of cancer detection of LRR after AR to support the use of postmastectomy mammography.¹² Furthermore, different school of thoughts exists within the surgical community on screening recommendations for this cohort of women. Some authors consider the theoretical possibility of recurrence developing in the minimal breast tissue left behind the autologous graft during reconstructive surgery.^6,9 Locoregional recurrence (LRR) after AR have been found to be 2% to 4%, lower than 2% to 7.50% in those undergoing mastectomy without reconstruction.¹² Previous investigators have reported that the non-palpable cancer detection rate (CDR) should achieve a similar screening benefit to asymptomatic women who are 40 years of age.^6,9 A study by Noroozian et al reported a CDR of 1.5 cancer per 1000 women.⁶ Many investigators suggest that screening may not be beneficial in the autologous breast as most local recurrences are detected clinically by physical palpation.^9,12,13

The paradigm improvement in multidisciplinary management of breast cancer over the last decade, paucity of existing literature, and varied practices and administrative policies underscore the need for data-based recommendations on the role of mammography in the screening of the autologous reconstructed breast post mastectomy. Furthermore, the judicious use of imaging services may potentially reduce patient anxiety and unnecessary appointments,¹⁴ especially in resource limited health care settings. A better understanding of the value of mammography in patients with autologous reconstruction is essential to formulate evidence based follow up surveillance protocols. The purpose of this study was to determine the cancer detection rate (CDR) of surveillance mammography in the autologous reconstructed breast post mastectomy.

Methods

In this research ethics board approved retrospective chart review study, a search of the radiology information system (RIS) was performed from August 1, 2012, to December 31, 2021. The search used institutional descriptors including TRAM (transverse rectus abdominis myocutaneous), DIEP (deep inferior epigastric artery perforator), autologous myocutaneous flap, AMF, and latissimus dorsi. At our institution, standard practice included annual ipsilateral surveillance mammography and clinical follow-up for all patients treated with mastectomy and autologous reconstruction (in addition to surveillance of the contralateral breast). Women who had undergone therapeutic total mastectomy with autologous flap reconstruction (TRAM or DIEP) of the same breast as prior cancer, and at least 1 year of clinical follow up and annual mammographic surveillance of their reconstructed breast were included. Women with therapeutic mastectomy with implant-based reconstruction, prophylactic bilateral mastectomy, subtotal mastectomy, nipple-sparing mastectomy, or those who declined imaging surveillance were excluded. A chart analysis was performed by 2 breast imaging fellowship-trained radiologists with 1 year and over 20 years of experience respectively. This review was performed through the hospital information system EPIC and PACS, and information recorded included age at the time of last imaging study, BI-RADS categories and pathologic findings if a biopsy was performed. Demographic information including family history, lifetime breast cancer risk, menopausal status, and details of the primary malignancy was not available in our records and therefore not collected for this analysis. If a breast malignancy was detected, additional information including HR status, tumour grade, pathologic stage (AJCC v8), and location of ipsilateral malignancy (within the skin/flap/chest wall/axilla). During the chart analysis, the distinction was made on the method of detection, if the abnormality was clinically identified or detected on surveillance imaging.

Locoregional recurrence was defined as a biopsy-proven breast cancer in the ipsilateral reconstructed breast, skin flap, axilla, or deep chest wall. Two authors who were not blinded to clinical information retrospectively reviewed the images of interval cancers to determine, by consensus, whether malignancy was apparent on the preceding surveillance mammogram. Interval cancer was defined as breast cancer in the autologous reconstructed breast identified within 12 months of a normal screen. Cancer detection rate (CDR) of surveillance mammography post-mastectomy was limited to the group of patients who have had a therapeutic mastectomy with autologous reconstruction. The CDR of surveillance mammography and the number of interval cancers in the reconstructed breast were determined. In addition, the abnormal recall rate (ACR), positive predictive values for recall (PPV1), for recommendation for biopsy (PPV2), and biopsy performed (PPV3) were calculated as outlined in the BI-RADS lexicon.¹⁵

Results

Study Observations

In this study, 371 women were identified who had undergone therapeutic total mastectomy with autologous reconstruction (AR) of the same side as prior cancer, without nipple or skin preservation, and who underwent mammographic surveillance from 2012 to 2020 (Figure 1). The median age at the time of last imaging study was 58 years (25-86 years).

Figure 1.

Study flowchart showing the number of studies retrieved and screening parameters.

Of the 371 patients included in the study, 35 were recalled for a screening-detected abnormality in either breast. One patient was recalled for bilateral breast findings on the same screening visit, and this was assumed as 2 recalls for each breast to simplify the calculation of results. 37.14% (13/35) of recalls were assigned BI-RADS 2, 25.71% (9/35) BI-RADS 3, 17.14% (6/35) BI-RADS 4A, 11.43% (4/35) BI-RADS 4B, 2.86% (1/35) BI-RADS 4C, and 5.71% (2/35) BI-RADS 5.

Nine screening detected recalls were identified in the autologous reconstructed breast. Calcifications were the most common screen-detected abnormality, accounting for 5/9 (55.56%), followed by masses at 3/9 (33.33%) and asymmetry at 1/9 (11.11%). No screen-detected cancers were identified in the ipsilateral breasts. Three clinically palpable cancers were identified (Figures 2 –4). Three benign biopsies were identified for screening detected findings in the ipsilateral breast. Table 1 shows the total number of interval cancers found in the autologous breast in the study. Table 2 shows the screening performance indicators for the autologous reconstructed breast in the study. The average number of years screened per patient was 5.73 years (2127/371, range of 1-17 years). The CDR by screening mammography in the ipsilateral reconstructed breast was 0/1000 while CDR in the contralateral native breast was 2.82/1000 (6/2127). The overall ACR was 1.65% (35/2127), while ACR for the ipsilateral breast was 0.42% (9/2127) and for the contralateral breast was 1.22% (26/2127). The overall ACR in our study is 1.65%, which is lower when compared to average recall rates for screening mammography (7%-8%).

Figure 2.

(a-d) Forty-one-year-old woman, BRCA 1 gene carrier with previous history of breast cancer treated with bilateral mastectomies with DIEP flap reconstruction, presented with multiple clinically palpable nodules and skin induration in the same breast as previous cancer. Diagnostic CC and MLO views (a, c), compared with the prior normal surveillance mammograms, 9 months earlier (b, d). Skin markers (white arrows) indicating the palpable abnormalities helped to identify multiple small skin lesions and a targeted diagnostic ultrasound was performed next for further evaluation. (e, f) Diagnostic ultrasound (e) and ultrasound-guided biopsy (f) of the palpable abnormality demonstrated multiple subcutaneous suspicious masses, which were found to be multifocal grade 3 ER + HER 2-invasive ductal carcinoma with micropapillary features on pathology. As she presented with a clinical concern 9 months after a normal surveillance mammography assessment, this was categorised as an interval cancer.

Figure 3.

(a-d) Forty-eight-year-old woman with an interval cancer diagnosed due to palpable abnormality within the skin of the autologous flap 6 months after normal surveillance mammogram, 7 years post therapeutic mastectomy and AR. Diagnostic mammograms with metallic BB (white arrows) to indicate the skin lesion in CC (a) and MLO views (c) were compared with the prior normal surveillance mammograms, 6 months earlier (b, d). (e) Diagnostic US of skin lesion (short arrow) shows a small corresponding irregular subcutaneous mass. A punch biopsy by the surgeon yielded a diagnosis of grade 2 invasive ductal carcinoma with lobular features and categorised as an interval cancer.

Figure 4.

(a, b) Sixty-two-year-old female with palpable concern in the reconstructed right breast. Diagnostic CC (a) mammogram shows a high-density mass in the inner right breast (white arrow), new from prior screening mammogram 38 months before (b). Diagnostic MLO (c-e) mammogram shows that the palpable mass in the inferior right breast (white arrow) was present in retrospect on the prior single view screening mammogram (black arrow) performed 26 months before at another institution (missed 12 months prior due to Covid pandemic). No CC views were obtained at this time. Diagnostic ultrasound (f, g) shows an irregular hypoechoic mass at the 7:00 position palpable mass in the right breast and an enlarged axillary lymph node. These were biopsied and found to be invasive ductal carcinoma and metastatic axillary lymph node. Based on consensus, this was categorized as an interval cancer, missed on imaging.

Table 1.

Total Number of Interval Cancers Found in the Autologous Breast in the Study.

Age	Detection (clinical/imaging)	Pathology	IHC ER	IHC PR	IHC HER2NEU	Tumour grade	Stage	Interval between mastectomy & LRR (y)	Previous cancer histology
41	Clinical (skin lesion)	IDC with micropapillary features	Positive	Positive	Negative	2	T1N1M1	4	IDC and non calcified DCIS
48	Clinical (skin lesion)	IDC with lobular features	Positive	Positive	Negative	2	T2N0M0	8	DCIS cribriform type
62	Palpable mass involving the skin	IDC positive for lymph node metastasis	Positive	Positive	Negative	2	T4b N1 M0	4	IDC

Note. CL = contralateral; IL = ipsilateral (autologous); IDC = invasive ductal cancer; ER = oestrogen receptor; PR = progesterone receptor; LRR = locoregional recurrence.

Table 2.

Screening Performance Indicators for Ipsilateral AR Breasts.

Total no. of patients satisfying the inclusion criteria	371
No. of years screened per patient	5.73 (371/2127). Range 1-17 y
Total no. of screening examinations	2127
No. of recalls in AR breasts	9
No. of non palpable cancers in AR breasts	0
No. of benign biopsies in AR breasts	3
Recall rate in AR breasts	0.42% (9/2127)

Discussion

A large cohort of consecutive women with history of breast cancer treated with therapeutic mastectomy and autologous reconstruction (AR) with imaging surveillance over 8 years found no benefit of screening mammography in the ipsilateral autologous reconstructed breast, while there was a benefit of surveillance mammography for the contralateral native breast. The CDR of 0 cancers/1000 screens was lower than the CDR of native breast and did not meet the Canadian target for screening average risk women, of 3 or more per 1000.^9,16 The 3 locoregional recurrences detected in autologous breasts reconstructed in our study were clinically palpable. In addition, screening the ipsilateral autologous breasts led to 3 benign biopsies.

Our results are similar to previous studies, as shown in Table 3. There is a considerable difference in conclusions of these studies, with some studies suggesting the potential benefit of screening mammography in AR breasts, whereas others advocate no role. A group of studies, including a recent study of 183 women with 653 mammograms, found screening mammography beneficial in AR and found a CDR of 0.5%.⁸ A 2018 study by Noroozian et al, which is the largest study to date, included 515 women and found a CDR of 1.5 per 1000 women,⁶ similar for an age-matched woman with native breast. These authors did not find any benefit of screening mammography in women with bilateral prophylactic mastectomy.⁶ Similar results were found in a 2002 study by Helvie et al in 106 women who found a CDR of 1.9 per 1000 women.⁴ Other group of studies have shown no benefit of screening mammography in AR. This includes a 2014 study by Freyvogel et al in 397 women,⁹ in which none of the recurrent cancers in the autologous breast were detected with screening mammography. A 2008 study by Lee et al, including 554 mammograms, also showed a CDR of 0%.¹⁷ Furthermore, the 3 benign biopsies in ipsilateral AR breasts in this study highlight potential downsides of screening, including unnecessary procedures, patient anxiety, and additional healthcare costs associated with false-positive findings.^14,18

Table 3.

Comparison of Observations of the Present Study With Research From Previous Investigators.

Authors	Year	Number of patients with imaging follow up	Number of screens per patient	Total cancers in autologous breast	Cancers detected by screening mammography	Cancers detected in autologous breast (per 1000) of screening mammography
Hastings-Robinson et al⁸	2023	183	3 (median)	3	3	5
Noroozian et al⁶	2018	515	NA (6.7 mammograms per autologous flap)	13	5	1.5
Freyvogel et al⁹	2014	397	5.36	2 (both palpable on follow up)	0	5
Lee et al¹⁵	2008	267	2.07	0	0	0
Helvie et al⁴	2002	106	NA	2	2	19
Our study	2021-2022	371	6.10	1	0	0

The considerable gaps in the present literature have resulted in lack of standard guidelines for mammographic screening in women with mastectomy and AR. This has significant implications on the healthcare infrastructure as reconstructive surgeries with AR are gaining more acceptance amongst women with breast cancer.^1,3,6 Many factors should be considered to ascertain the value of screening mammography in women with AR. A large number of patients and multicentric studies are necessary to formulate data-based screening recommendations. All studies to date are single institution based and have small sample sizes. It is also important to note that a woman’s need for screening mammography depends on personalised cancer risk assessment. The existing population of women with AR may have vastly different cancer risk, with many women not even aware of their cancer risk. Awareness about genetic testing and the relative ease of estimation of a woman’s lifetime risk of breast cancer play a key role in optimising personalised cancer surveillance regimens. Incidence of locoregional recurrence may be different based on tumour immunohistochemistry, with a recent study reflecting that young women with triple-negative breast cancer are at an increased risk of developing locoregional recurrence after AR.³ The 3 locoregional recurrences detected in autologous breasts reconstructed in our study were clinically palpable. One interval cancer was retrospectively visible 26 months prior. Theoretically, if this cancer was screening detected on annual mammographic surveillance, this would imply potential benefit of surveillance mammography in women with AR. It is also noted that, this will yield a CDR of 1 per 1000 screens for autologous breasts, which is below the Canadian screening target of ≥3 cancers per 1000 women.¹⁶ Advocating a blanket statement for screening recommendation may be counterproductive. Furthermore, current guidelines clearly recommend regular surveillance of normal breast in women with unilateral AR, and not evaluating the reconstructed breast on screening visits may be a missed opportunity in these women. Additionally, an autologous reconstructed breast has a largely fatty/non-dense component and can be readily evaluated on a screening mammogram for non-palpable recurrence. The theoretical possibility of locoregional occurrence occurring in the residual native breast tissue deep to the autologous flap is low but cannot be completely negated.^6,7

We recognise several limitations of our study. The retrospective, single-centre design resulted in a relatively small cohort. However, given our institutional policy of performing screening mammography for the ipsilateral autologous reconstructed breasts allowed a large enough cohort to be screened an average of 5.7 times during the study. Our institutional policy recommends annual surveillance mammography and clinical follow-up for all patients with breast cancer treated with mastectomy and autologous reconstruction (AR). However, our analysis was limited to women who underwent imaging surveillance, which may have introduced selection bias by excluding patients managed solely with clinical follow-up (predominantly women who declined mammograms or were lost to follow-up). As such, our cancer detection estimates reflect outcomes primarily in women who followed our standard imaging protocol rather than the broader AR population. While our institutional policy recommends annual surveillance mammography, the frequency and regularity of actual imaging surveillance was not standardised in a patient with clinically palpable cancer (Figure 3) included in this analysis, which may have contributed to the absence of screen-detected subclinical recurrence observed in the study. Additionally, the retrospective image review of interval cancers was performed by readers aware of the cancer diagnosis, which may have introduced retrospective review bias when assessing whether findings were apparent on prior screening examinations. Furthermore, various factors, including differences in institutional protocols, clinicians’ preferences in recommending screening to women with ARs, could be potential sources of bias and make it difficult to compare to the current literature. Demographic risk factors including family history, menopausal status, and primary tumour characteristics were unavailable in our records. The utility of other screening modalities such as ultrasound and MRI was not assessed in our study. Long term outcomes such as morbidity and mortality were also not evaluated.

In this study, we found no benefit between surveillance mammography and detection rate of non-palpable cancers in the breast previously treated with AR in patients who underwent imaging surveillance. As such, present data should be considered with caution and is insufficient to make screening recommendations in broader populations of women with mastectomy and AR. Rising rates of women with breast cancer opting for mastectomy with AR and the lack of substantial data to formulate screening recommendations underscores the need of larger scale multicentric research.

Footnotes

ORCID iDs

Amit Katyan

Raman Verma

Jean M. Seely

Funding

The authors received no financial support for the research, authorship, and/or publication of this article.

Declaration of Conflicting Interests

The authors declared no potential conflicts of interest with respect to the research, authorship, and/or publication of this article.

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