Cancer recurrence in routine histopathology of mastectomy scars during breast reconstruction: a systematic review

Introduction

Breast cancer is the most common cancer among Danish women, with approximately 5,000 new cases diagnosed every year (1). The treatment of breast cancer depends on the stage of the disease and typically involves a multidisciplinary approach consisting of surgery, radiotherapy, and chemotherapy (2). In 2022, 65% of Danish breast cancer patients underwent breast-conserving surgery, while 30% required mastectomy (3). Among women who have a unilateral mastectomy, some receive a contralateral prophylactic or symmetrizing mastectomy. Additionally, women who are at high risk of developing breast cancer may choose to have a bilateral prophylactic mastectomy, even without a current breast cancer diagnosis. In 2015, 40% of Danish women who had a mastectomy opted for breast reconstruction (BR), either as primary breast reconstruction (PBR) or delayed breast reconstruction (DBR) (4). This trend is on the rise because of an increasing demand from patients for reconstructive procedures.

The practice of routine histological examination of mastectomy scars during BR or implant replacement was first advocated by Granick et al. in 1987 (5). This approach became a standard of care until its necessity was questioned by Soldin et al. in 2004 (6). Since then, several studies have questioned the value of routine histological examination of mastectomy scars at the time of BR. The practice of routine histological examination of mastectomy scars results in an increased workload for surgeons, nurses, and pathologists. In the current era of cost-effective and evidence-based medicine, it is essential to ensure optimal use of healthcare resources. However, some studies have reported incidental findings of breast cancer recurrence in mastectomy scars sent for routine examination, leading the authors to conclude that routine histology is important (7-9).

It is crucial to acknowledge that patients undergoing DBR and immediate, staged, implant-based reconstruction represent diverse populations, with varying oncologic time points and reasons for undergoing mastectomy. DBR is performed at different time intervals post-mastectomy and is influenced by factors such as adjuvant radiotherapy, skin flap quality, and the preferences of both surgeons and patients (10,11). The heterogeneous treatment course for these patients may impact their risk of breast cancer relapse at the time of DBR.

A systematic review from 2021 found that the median time to local recurrence of breast cancer ranged between 13.2 and 38 months (12). The most common sites of local recurrence were skin and chest wall near the location of the original tumour. Mastectomy scars may contain metastasis caused by spillage of tumour cells during the initial curative surgery (13,14). Additionally, scars from prophylactic mastectomies can contain breast cancer due to de novo invasive or non-invasive tumours that may have developed in residual glandular tissue that was left behind or spilled during initial surgery. Differences in cancer treatment protocols and timing of surgical intervention across countries can potentially impact the risk of cancer recurrence. Similarly local treatment strategies from different centres across the world present different regimes regarding routine histological examination of mastectomy scars. In Denmark, despite following national guidelines for breast cancer treatment, there is a lack of consensus among hospitals regarding the submission of mastectomy scars for routine histological examination. To date, no studies in Denmark have evaluated the risk of in-scar recurrence through routine histology at the time of BR.

To the authors’ knowledge, no comprehensive systematic review has yet been published that investigates the value of routine histological examination of mastectomy scars during BR and breast implant replacement. We present this article in accordance with the PRISMA reporting checklist (available at https://abs.amegroups.com/article/view/10.21037/abs-24-38/rc) (15).

Methods

This study has been registered in The International Prospective Register of Systematic Reviews (PROSPERO) under ID number 424647. A PICO-analysis was performed to clarify the aim and objectives of this study.

Literature search

A systematic search was conducted on MEDLINE/PubMed, Web of Science, Embase, and Scopus. A systematic search was performed on the 23^rd of July 2023 based on the following search string: ((((((mastectom*)) OR (mastectomy, segmental[MeSH Major Topic])) OR (Mastectomy, Segmental*)) OR (mastectomy, modified radical*[MeSH Terms])) AND (((((((cicatrix / etiology[MeSH Terms]) OR (cicatrix / pathology[MeSH Terms])) OR (Cicatrix / pathology* [MeSH Terms])) OR (Cicatrix / surgery[MeSH Terms])) OR (histopatholog*[Title/Abstract])) OR (scar*[Title/Abstract])) OR (histologic*[Title/Abstract]))) AND ((((((((((((breast neoplasms[MeSH Terms]) OR (breast cancer[Title/Abstract])) OR (breast carcinoma[Title/Abstract])) OR (breast tumours[Title/Abstract])) OR (cancer of breast[MeSH Terms])) OR (tumours, breast[Title/Abstract])) OR (breast implants[MeSH Terms])) OR (breast reconstruction[MeSH Terms])) OR (mammoplasty)) OR (breast reduction)) OR (neoplasm recurrence[MeSH Terms])) OR (neoplasm recurrence)).

Inclusion and exclusion criteria

All studies including patients who underwent mastectomy (whether curative or prophylactic) followed by PBR or DBR were included. There were no restrictions regarding study design and year of publication. However, case reports involving clinically suspected recurrences and duplicate studies were excluded.

Data extraction

Search results from all databases as well as initial abstracts were imported and automatically de-duplicated by Covidence (Covidence Ltd., Melbourne, Australia). Title and abstracts were initially screened for inclusion by two independent reviewers. Subsequently, full-text articles were retrieved and further screened to ensure that the inclusion criteria were met. Any uncertainties or disagreements at any stage of the process were resolved through consensus with a third independent reviewer. Finally, a reference and citation search were conducted on the included studies, which were screened in the same manner as the primary studies identified during the systematic search. A flowchart illustrating the selection process is presented in Figure 1.

Figure 1 PRISMA flowchart of the study selection process.

Outcomes

The primary outcome of interest was evidence of histopathological recurrence of breast cancer in mastectomy scars at the time of BR. Secondary outcome measures were type of primary surgery (prophylactic vs. curative), type of secondary surgery (method of reconstruction), time interval between primary and secondary surgery, type of breast cancer, neoadjuvant chemotherapy, and adjuvant chemo- and radiotherapy. In addition, patient demographics, follow-up periods, and information on whether the recurrence was clinically suspected were recorded.

Risk of bias and level of evidence

The STrengthening the Reporting of OBservational studies in Epidemiology (STROBE) statement was applied to evaluate the risk of bias and quality of the included observational studies (16). All studies were individually assessed by two authors and classified as sufficient (+) or insufficient (−). Discrepancies were resolved by consensus with a third author. Based on these individual judgements, each study was assigned an overall risk of bias category: low risk, moderate risk or high risk. Furthermore, all studies were rated according to the American Society of Plastic Surgeons (ASPS) Levels of Evidence Scale (17).

Results

A total of 11,081 studies were identified through PubMed (n=5,618), Web of Science (n=3,490), Scopus (n=1,883), and citation searching (n=90). After removing duplicates (n=3,282) and conducting a full-text screening, a total of 12 studies were found eligible for inclusion. The PRISMA flow chart illustrating this process is presented in Figure 1. The included studies published between 2004 and 2018 involve six retrospective cohort studies, one case report, and five letters to the editor. The included studies identified 1,905 patients with a mean age of 48.39 years (based on seven studies). A total of 2,737 mastectomy scars were submitted for routine histological examination at the time of BR. In addition, Nahabedian et al. reports having performed over 1,000 BRs, with all associated mastectomy scars being submitted for routine histological examination (18). A total of 2,260 scars were from curative mastectomies, while 373 were from prophylactic mastectomies (see Table 1). Additionally, data for 104 scars are missing. The mean interval between mastectomy and scar sampling ranged between 254 days and 12 years. Fourteen mastectomy scars revealed recurrence of breast cancer and is highlighted in Table 2. Six scars had macroscopic lesions that raised clinical suspicion of recurrence at the time of excision, while the remaining eight scars showed no clinical signs of cancer recurrence; these recurrences were only identified through routine histological examination. The average age of the patients with recurrence was approximately 46 years (range, 36–58 years), with the average interval between primary surgery and recurrence being approximately 5 years (range, 6 months–12 years). None of the recurrences appeared after prophylactic mastectomies and recurrences were primarily breast carcinoma in various multifocal, invasive and infiltrative types (see Table 2). Soldin et al. reported five clinically evident recurrences prior to DBR, but did not specify the timeframe between primary surgery and cancer recurrence (6). Similarly, Alam et al. reported one clinically evident local recurrence prior to surgery, also without specifying the time interval between mastectomy and BR (19). Warner et al. found local recurrence in four scars from three patients without clinical suspicion of recurrence prior to excision (21). The time between primary surgery and scar sampling was reported to be 6, 2, and 9 years, respectively. Hsieh et al. presented a case report of a single patient who had a clinically unsuspected recurrence 5 years and 7 months after mastectomy (7). Zambacos et al. reported one clinically unsuspected recurrence 2 years after mastectomy (8). Nahabedian et al. described one patient with clinically unsuspected recurrence in the mastectomy scar at the time of reconstruction, but did not provide a timeframe for the recurrence (18). Finally, Sinha et al. reported one patient who underwent DBR 12 years after mastectomy, during which routine histological examination revealed recurrence of cancer (9). The use of diagnostic imaging prior to BR is described in only 1 out of the 12 included studies (7). It is likely that the use of preoperative diagnostic imaging varies among the studies due to variations in guidelines across different countries.

According to the ASPS classification of evidence, the six retrospective studies are categorised as level III evidence, whilst the remaining studies are classified as level V (see Table 3). A risk of bias assessment using the STROBE criteria was conducted for the six retrospective studies (see Table 4). Of these, four studies were determined to have a “moderate” overall risk of bias, whereas the other two were assessed as having a “low” and “high” overall risk of bias, respectively. Additionally, one study was a case report, and the remaining five studies were published as letters to the editor. These publications were evaluated as having a high risk of bias due to their level of evidence.

Discussion

Key findings and explanation

This review identified 14 cases of breast cancer recurrence across all studies (see Table 3). In eight of these scars, there was no clinical suspicion of malignancy. It is important to note that half of the included studies comprise letters to the editor and a case report. Since most of these studies focus on a single case or small case series, they do not provide a reliable estimate of the true recurrence rates. In contrast, the retrospective studies with larger patient cohorts offer a more representative estimate of the recurrence rates in mastectomy scars. When reviewing only the retrospective studies, a total of 2,630 mastectomy scars were analysed, including scars from both prophylactic and curative mastectomies. Among these, 10 scars had cancer recurrence. Notably, in four of these scars, there was no clinical suspicion of recurrence at the time of surgery. This suggests that the detection of malignancy in routine histology of mastectomy scars during BR is rare in clinically unsuspected scars. Furthermore, none of the scars from prophylactic mastectomies showed signs of malignancy.

Warner et al., Fishman et al., and Momeni et al. found no in-scar recurrence despite examining a total of 1,994 mastectomy scars (21-23). Notably, the majority of these scars were analysed within the first 3 years after mastectomy, a time period previously reported as being associated with the highest risk of cancer recurrence (12,21-23). In contrast, Soldin et al. found recurrence in 5 out of 48 mastectomy scars (6), and Alam et al. found recurrence in 1 out of 133 mastectomy scars (19). As a result, the authors of these studies concluded that routine submission of mastectomy scars for histological examination at the time of BR provides little to no value. In these studies, the scars analysed were predominantly from curative mastectomies.

The findings of Warner et al. stand out, as this is the only retrospective study to find in-scar recurrence in clinically benign scars (see Table 3) (21). Cancer recurrence was detected in four scars from three patients. The first patient had multifocal, grade II, ductal carcinoma. Six years after mastectomy followed by adjuvant chemo- and radiotherapy, the patient underwent BR with a latissimus dorsi flap. Intraoperatively, clinical suspicion of lymph node involvement prompted histological examination of the lymph node and mastectomy scar, which both revealed recurrence of the primary tumour. This case is quite surprising, given the extended time interval between the mastectomy and scar sampling. However, in this case, the intraoperative findings would have likely warranted histological examination regardless of any routine histology protocol. The second patient had bilateral multifocal breast carcinoma with axillary involvement, which was treated with bilateral mastectomy and adjuvant chemotherapy. Despite no clinical signs of malignancy, scar sampling during BR 2 years later showed cancer recurrence. Multifocal carcinoma and bilateral disease suggest a more aggressive form of cancer, and axillary lymph node involvement is a sign of a more advanced stage of the disease. Moreover, in contrast to the first case, the time to local recurrence in this patient is not unusual. The third patient, who was treated with a wide local excision and adjuvant radiotherapy for an infiltrating lobular carcinoma, experienced two cancer recurrences over the next 6 years. The first recurrence was treated with mastectomy and chemotherapy, while the second was managed with wide excision, bilateral salpingo-oophorectomy, and tamoxifen. After more than 3 years without evidence of cancer, the patient opted for BR. The histology report revealed in-scar recurrence despite no clinical suspicion during surgery. Two cancer recurrences prior to the BR suggest a more aggressive form of breast cancer. Even in the absence of clinical suspicion, the surgeon would have been highly likely to perform scar sampling due to the patient’s previous recurrences. Unfortunately, the authors did not provide details regarding preoperative diagnostic imaging, which could have an impact on the risk of finding cancer recurrence in mastectomy scars during BR.

In the case report by Hsieh et al., the authors described an unusual case of cancer recurrence in a clinically unsuspected mastectomy scar during BR (7). The patient subsequently opted for a contralateral prophylactic mastectomy and BR. Surprisingly, the specimen from the prophylactic mastectomy also revealed invasive lobular carcinoma. These findings are remarkable due to the prolonged time until detection of recurrence at 5 years and 7 months, as well as the rare occurrence of detecting occult invasive cancer in the contralateral breast after prophylactic mastectomy. A study by King et al. found occult malignancy in the contralateral breast in 24 (6%) of 407 included patients who underwent mastectomy for unilateral cancer and contralateral prophylactic mastectomy (26). Among these 24 patients, only five had invasive cancer, while the remaining 19 had carcinoma in situ. All five patients with invasive cancer underwent preoperative mammography and magnetic resonance imaging (MRI). In one case, the mammogram revealed calcifications with enhancement on MRI, but the biopsy results were benign. Another patient had several areas of enhancement on MRI but chose not to get a biopsy prior to surgery.

Both Nahabedian et al. and Sinha et al. (9,18) commented on the retrospective study by Woerdeman et al. (20). Nahabedian reports having performed over 1,000 BRs, during which he only encountered one instance of in-scar recurrence identified through routine histology without prior clinical suspicion at the time of surgery. Additionally, he found cancer recurrence in a benign appearing capsule during expander-to-implant exchange. Despite the rarity of in-scar recurrence, Nahabedian advocates for the routine histological examination of mastectomy scars. Sinha et al. presented a patient with in-scar recurrence 15 years after the initial treatment consisting of wide local excision, axillary clearance, and adjuvant radiotherapy. While in-scar recurrences without any clinical suspicion after such a long interval are extremely rare, this patient had previously experienced a recurrence 3 years after completing cancer treatment. Additionally, the surgeons found “what appeared to be dense scar tissue in the medial part of the mastectomy scar and under the superior skin flap”. Such suspicious intraoperative findings should always lead to histological examination of the scar tissue regardless of any routine histology protocol.

Zambacos et al. reported one instance of in-scar recurrence in a series of 14 BRs over a period of 4 months (8). The patient had eight positive lymph nodes and underwent both adjuvant radio- and chemotherapy. Scar sampling during BR 2 years later revealed cancer recurrence. As a result, Zambacos et al. concluded that routine submission of mastectomy scars for histology is necessary. In contrast, Mathen et al. and Agostini et al. found no benefit of this practice after having reviewed 19 and 72 mastectomy scars, respectively, without any in-scar recurrences (24,25). Agostini et al. still recommended routine histology in selected cases, e.g., after skin-sparing or nipple-sparing mastectomy. However, the low number of scars evaluated by Zambacos et al. (8), Mathen et al. (24), and Agostini et al. (25) raises questions about the validity of their conclusions.

Strengths and limitations

A key strength of this systematic review is the broad search criteria, which identified 11,081 studies across three major scientific databases. This represents the largest collection of literature on the routine histological examination of mastectomy scars during BR. Such a comprehensive search increases the likelihood that we have identified all relevant studies on this topic. To ensure the integrity of the selection process and minimise risk of errors, all studies were screened independently by two reviewers, with a third independent reviewer involved in cases of uncertainty or disagreement. The findings of this review are based on data extracted from 12 scientific publications, including a total of 2,737 mastectomy scars. However, it is important to note that the existing literature in this field lacks studies classified as evidence level I or II, which raises concerns regarding the overall risk of bias. The included retrospective studies, all classified as evidence level III, were single-centre, retrospective observational studies, with 5 out of 6 studies carrying a moderate to high risk of bias. A significant limitation of these studies is the inadequate description of methodology, especially in terms of inclusion and exclusion criteria, which increases the risk of selection bias and missing data bias. Additionally, the methods of histopathological analysis were not described in detail. As a result, it is difficult to draw comparisons of recurrence rates across studies. The outcomes of the studies were reported inconsistently, with a considerable variability in the details provided regarding tumour histology, staging, and the number of scars, patients, and reconstructed breasts. Unfortunately, the studies have provided limited information on their use of diagnostic imaging during the post-mastectomy follow-up period and prior to BR surgery. This information could have provided a valuable insight, as diagnostic imaging prior to BR may be sensitive in detecting breast cancer recurrence in a selected group of patients (27). Additionally, confounding factors such as patient demographics, surgical technique, and surgeon experience were not addressed sufficiently and could have influenced the time between mastectomy and reconstruction, ultimately affecting the recurrence rate. While the case report and five letters to editors included in this review provided a valuable perspective on this topic, these studies were classified as level V evidence and inherently carry a high risk of bias due to their study designs. Nevertheless, these data were included in this review as they suggest that the incidence of in-scar recurrence may be higher than indicated by the retrospective studies. Additionally, these studies highlight a lack of consistent implementation of routine histological examination of mastectomy scars during BR.

Implications and actions needed

In many hospitals, it remains standard practice to submit all mastectomy scars for routine histological examination during BR. The rationale behind this practice is that a proactive approach such as this may help to detect early local recurrence, which can have important implications for the patient’s ongoing treatment and survival. While this review found a low incidence of histologically verified cancer recurrence in clinically unsuspected mastectomy scars at the time of BR, the included studies carry a moderate to high risk of bias. Since routine histology of mastectomy scars at the time of BR was first recommended by Granick et al. in 1987 (5), there have been significant advancements in diagnostic methods, treatment strategies, and follow-up care. This may explain the rarity of in-scar recurrences in the included studies. Therefore, while routine histology of mastectomy scars during BR has been considered important for a long time, a more selective use of routine histology may be more appropriate in the current context. Furthermore, the absence of cancer recurrence in scars from prophylactic mastectomies suggests that routine histological examination of these scars is unnecessary. It is also worth noting that the impact of early detection of cancer recurrence through routine histological examination on disease-free survival or overall survival has not been investigated. The low recurrence rate observed in clinically unsuspected mastectomy scars at the time of BR highlights the need for well-designed studies to investigate this matter in the current era of breast cancer treatment. A more selective approach could optimize utilization of resources, reduce unnecessary patient anxiety, and ensure that clinical practices are aligned with current evidence and patient-centered care principles. This would entitle an individual assessment based on breast cancer recurrence risk factors such as previous cancer history, breast cancer type, age, time since primary surgery and preoperative imaging.

Conclusions

The detection of breast cancer recurrence in routine histological examination of mastectomy scars at the time of BR is rare. Consequently, routine histological examination appears to offer limited value in this context. However, larger cohort studies are required before recommending a total discontinuation of this practice. In the meantime, a more selective approach to histological examination of mastectomy scars—considering factors such as tumour characteristics, treatment history, and previous cancer recurrences, regardless of the time elapsed since recurrence—may be more appropriate. Additionally, we found no evidence supporting the routine histological examination of scars from prophylactic mastectomies and therefore do not recommend this practice.

Acknowledgments

None.

Footnote

Reporting Checklist: The authors have completed the PRISMA reporting checklist. Available at https://abs.amegroups.com/article/view/10.21037/abs-24-38/rc

Peer Review File: Available at https://abs.amegroups.com/article/view/10.21037/abs-24-38/prf

Funding: None.

Conflicts of Interest: All authors have completed the ICMJE uniform disclosure form (available at https://abs.amegroups.com/article/view/10.21037/abs-24-38/coif). The authors have no conflicts of interest to declare.

Ethical Statement: The authors are accountable for all aspects of the work in ensuring that questions related to the accuracy or integrity of any part of the work are appropriately investigated and resolved.

Open Access Statement: This is an Open Access article distributed in accordance with the Creative Commons Attribution-NonCommercial-NoDerivs 4.0 International License (CC BY-NC-ND 4.0), which permits the non-commercial replication and distribution of the article with the strict proviso that no changes or edits are made and the original work is properly cited (including links to both the formal publication through the relevant DOI and the license). See: https://creativecommons.org/licenses/by-nc-nd/4.0/.

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