Surgical management of breast cancer has evolved dramatically over recent decades.1,2,3,4 Surgical interventions have been de-escalated with techniques such as breast conserving surgery (BCS), oncoplastic breast surgery (OPBS), and sentinel lymph node biopsy (SLNB).2,3 These developments in surgical care have been matched with improved neoadjuvant and adjuvant therapies.2,3 Taken together, these advancements have led to improved oncologic and esthetic outcomes for patients, with decreased morbidity.2

Professional societies and regulatory bodies from across the world have published quality indicators for breast surgery and minimum quality standards for breast centers.5,6,7,8,9,10,11 Quality indicators include preoperative workup of breast cancers, discussion of cases at multidisciplinary tumor boards, and adherence to guidelines.5 Indicators specific to surgical care for breast cancer include breast conservation rates, re-excision rates, and referral for immediate reconstruction in eligible patients.5 The heterogeneity in quality indicators across geographic regions, together with the variability in breast surgical oncology practice, highlight a lack of consensus in the definition of high-quality care in breast surgery.5

The modern breast surgeon must balance appropriate management of the underlying pathology with functional and esthetic outcomes. Many surgeon factors influencing breast surgery outcomes have been described with the goal of standardizing the quality of care in breast surgery. Surgeon practice volume has been linked to improved outcomes and may be associated with achievement of quality care indicators.12,13,14,15,16,17,18 Sub-specialization in surgical oncology or oncoplastic breast surgery has also been associated with improved outcomes.19,20,21 Furthermore, the use of oncoplastic techniques has been shown to provide similar oncologic outcomes to standard breast conserving surgery, while extending eligibility for breast conservation and improving cosmetic outcomes.22,23 This study aims to define the characteristics of a high-quality modern-day breast surgeon through a systematic examination of the existing literature describing modifiable surgeon factors influencing breast surgery outcomes.

Methods

Literature Search and Study Selection

This scoping review was conducted according to PRISMA-ScR guidelines.24 A comprehensive search encompassing five databases [OVID Medline, OVID EMBASE, Cochrane Library (CDSR and Central), PROSPERO, and SCOPUS] was conducted. Search terms included “surgeons”, “surgeon characteristics”, “breast cancer”, “outcomes”. Searches were limited to 1 January 2000–8 November 2021 to capture modern breast surgery practices (Appendix 1). After duplicates were removed, the search identified 2315 results (Appendix 1). Two independent reviewers screened 2315 titles and abstracts (JFR, ANR) through COVIDENCE software (Veritas Health Innovation, Melbourne Australia) and disagreements were resolved by consensus. Full text review was completed for 149 abstracts and 54 studies met inclusion criteria for the final analysis. Backward citation searching was conducted for each article, identifying 127 articles with 37 meeting inclusion criteria (Fig. 1).

Fig. 1
figure 1

PRSIMA flow diagram for study screening and inclusion; Source: Page MJ, McKenzie JE, Bossuyt PM, Boutron I, Hoffmann TC, Mulrow CD, et al. The PRISMA 2020 statement: an updated guideline for reporting systematic reviews. BMJ 2021;372:n71. https://doi.org/10.1136/bmj.n71

Full size image

Inclusion and Exclusion Criteria

Articles describing at least one modifiable surgeon factor influencing breast surgery outcomes were included. Only full-length articles published in English were included. Additionally, studies describing institutional factors but not modifiable surgeon factors were excluded. Articles published prior to the year 2000 or those describing patient cohorts treated exclusively prior to the year 2000 were excluded.

Data Extraction and Qualitative Analysis

Outcome measures included: oncologic, esthetic, and patient-reported outcomes, as well as surgical complications. All extracted outcome data are represented according to the primary statistical analyses reported in the original study. Only statistically significant findings are presented, unless otherwise described as a “trend” or as “no difference.” No additional statistical analyses on previously published data were completed for this scoping review.

Extracted data were qualitatively analyzed, summarized, and organized by surgeon factor. Surgeon factors were grouped into four themes; surgeon volume, use of oncoplastic techniques, fellowship or subspecialty training in surgical oncology or breast surgery, and participation in professional development or quality improvement activities. Non-modifiable surgeon factors such as surgeon age, gender, and years in practice were not recorded.

Results

Study Characteristics

A total of 91 studies met inclusion criteria. A variety of study designs were represented, including surveys (21 studies), retrospective (56 studies) and prospective cohorts (13 studies), reviews or meta-analyses (3 studies), retrospective case control (4 studies), and randomized controlled trials (1 study). Six studies utilized more than one methodology (for example, survey and retrospective cohort). Studies included patients and surgeons from North America, Europe, Asia, and South America, with 18 countries represented.

Surgeon factors were categorized into four themes: surgeon volume (45 studies), use of oncoplastic techniques/oncoplastic training (41 studies), fellowship or subspecialty training in surgical oncology or breast surgery (9 studies), and participation in professional development and quality improvement activities (5 studies) (Fig. 2). Nine studies investigated more than one surgeon factor; in these cases, the data were reported individually. Surgeon factors and associated outcome measures are summarized in Tables 1, 2, 3 and 4.

Fig. 2
figure 2

Number of studies reporting surgeon factors by category

Full size image
Table 1 Outcomes associated with surgeon volume and proportion of breast surgery practice
Full size table
Table 2 Outcomes associated with the use of oncoplastic breast surgery techniques
Full size table
Table 3 Outcomes associated with surgical oncology or breast surgery specialization
Full size table
Table 4 Outcomes associated with participation in professional development activities
Full size table

Surgeon Volume and Proportion of Practice in Breast Surgery

A total of 45 studies identified surgeon volume as key a factor impacting outcomes in breast surgery (Table 1). This was reported as either an interval volume or as a proportion of the surgeon’s practice dedicated to breast surgical oncology. Among these studies, there was no standardized definition of a high-volume surgeon.

Seventeen studies examined surgical techniques in relation to surgical volume. Higher surgical volume was associated with increased use of BCS16,25,26,27,28,29,30,31 and deceased completion mastectomy rates.32,33 Furthermore, high-volume surgeons were less likely to routinely use or report use of axillary lymph node dissection (ALND)34,35 and were more likely to use or report use of SLNB,36,37,38 with decreased rates of SLNB failure.39 High-volume surgeons were also less likely to evaluate the axilla surgically in DCIS cases.40 Finally, patients of high-volume surgeons were more likely to be successful in same-day discharge and home recovery and demonstrated decreased incidence of surgical site infections.41,42

Regarding local control of disease, higher-volume surgeons were less likely to obtain positive margins in one study,15 had lower re-excision rates in seven studies,13,14,20,33,43,44,45 and exhibited a trend toward lower re-excision rates for pathologically negative margins in one study.46 High-volume surgeons were also more likely to employ techniques to reduce re-excision rates such as cavity shave margins.15 Finally, one study noted decreased breast-cancer-specific mortality for patients of high-volume surgeons, while another did not identify any differences.17,47

With respect to other quality indicators, high surgical volume has also been demonstrated to be associated with increased completion of radiation therapy after BCS.12,17,18,48 Higher-volume surgeons were also more likely to utilize preoperative needle biopsy for diagnosis15,20,49,50 and intraoperative gross margin assessment by a pathologist.50 Patients of high-volume surgeons were more likely to undergo immediate reconstruction after mastectomy.51 There was disagreement between studies regarding patient satisfaction with involvement in decision-making;52,53 however, patients described increased satisfaction with the surgeon–patient relationship with a high-volume surgeon.53 Finally, surgeons with a higher practice volume were more likely to agree with published margin guidelines for invasive breast cancer54 and trended toward increased rates of attendance at multidisciplinary tumor boards.55

Use of Oncoplastic Techniques

The use of oncoplastic techniques is a modifiable surgeon factor that has been evaluated in 41 studies (Table 2). In the studies included in this review, the specific oncoplastic techniques were variable between studies. Level I (≤ 20% volume excision without skin excision)2 and level II (20–50% volume excision with skin excision or mammoplasty)2 oncoplastic techniques were most commonly described. A minority of studies included a small percentage of volume replacement techniques (such as latissimus dorsi miniflaps) in their data analyses. The use of oncoplastic techniques was described in comparison to standard BCS and mastectomy with reconstruction.

A total of 23 studies reported on the oncologic outcomes associated with OPBS. Regarding local control of disease, OPBS was associated with decreased margin positivity rates in six studies56,57,58,59,60,61 and decreased re-excision rates in eight studies.58,59,60,62,63,64,65,66 Other studies have described OPBS to be equivalent to standard BCS with regards to margin positivity,67,68,69,70,71,72,73,74,75 re-excision rates,45,57,68,69,70,76,77,78 and local recurrence.63,64,65,66,69,71,78,79 Three studies demonstrated decreased completion mastectomy rates in patients undergoing OPBS,60,62,63 while two studies reported equivalent rates.68,78 Two additional studies reported increased rates of completion mastectomy after OPBS.59,74 Time to adjuvant therapy,63,77,80 disease-free survival,71,72,73,81 and overall survival and mortality65,66,69,71,72,73,78,79,81 were equivalent between OPBS and BCS.

Nine studies noted improved esthetic outcomes with OPBS by patient-reported metrics and/or surgeon evaluation.59,63,67,69,82,83,84,85,86 Three studies reported no differences in cosmetic outcomes between OPBS and standard BCS.77,78,87 Only one study reported worse cosmetic outcomes with OPBS.76 In this study, tumor size and specimen resection weights were significantly larger in the OPBS group.76 In two out of three articles investigating patient-reported functional outcomes,63,82,84 OPBS patients had improved postoperative social functioning63 and faster return to activities.84

Regarding early postoperative complications, 11 studies demonstrated equivalent57,58,62,63,64,67,70,76,88 or decreased59,89 complication rates between oncoplastic and standard BCS. In a minority of studies, OPBS was associated with increased early postoperative morbidity such as reoperation,78 wound complications,79,90 seromas,79 bleeding,90,91 and overall 30-day morbidity90 compared with BCS. With regard to postoperative length of stay following OPBS, the data were mixed, with one study showing increased length of stay and another showing no difference after OPBS.68,75

Five studies commented on OPBS in comparison to mastectomy with reconstruction. OPBS had decreased overall and bleeding complications,91 decreased wound complications,79 and improved cosmetic and return to function scores.84 One study reported decreased rates of distant recurrence and improved disease-free and overall survival.71 Specifically in obese patients, those undergoing OPBS had fewer complications requiring reoperation or resulting in a delay to adjuvant therapy.92

Fellowship or Sub-specialization in Surgical Oncology or Breast Surgery

Nine articles examined outcomes in relation to subspecialty training (Table 3).19,20,21,37,38,49,93,94,95 Patients treated by a surgical oncologist compared with a general surgeon were less likely to undergo re-excision,20 more likely to have BCS19 and SLNB,37,38 and more likely to complete appropriate adjuvant therapy.19 These patients were more likely to participate in clinical trials, and also had improved disease-free and overall survival for stage 1–3 disease.19 Notably, one study reported increased use of preoperative diagnostic needle biopsy among surgical oncologists compared with general surgeons for patients treated from 2003 to 2007.20 In another study, patients of surgical oncologists reported higher cosmetic satisfaction.21 Finally, specialist breast surgeons were more likely to report familiarity with published guidelines.93

Participation in Professional Development and Quality Improvement Activities

Surgeon participation in professional development and quality improvement activities has been demonstrated to improve breast surgery outcomes (Table 4). For example, surgeons who regularly attended multidisciplinary tumor boards reported decreased propensity for ALND.35 Similarly, surgeons with knowledge of key trials reported increased use of SLNB.96 Additionally, being a member of the American Society of Breast Surgeons or Society of Surgical Oncology was associated with increased use of SLNB.36 If a surgeon was a member of both organizations, the effects on use of SLNB were additive.36 Participation in a community clinical oncology program linking community and academic surgeons was associated with increased use of SLNB during its early adoption period in the early 2000s.97 Finally, one study found breast surgeons participating in any type of quality improvement program had decreased re-excision rates after BCS,98 highlighting the importance of continuing education for the modern-day breast surgeon.

Discussion

Four key surgeon factors associated with improved breast surgery outcomes were identified: surgeon volume, use of oncoplastic techniques, additional training in breast surgery or surgical oncology, and participation in professional development and quality improvement activities. Each of these surgeon factors is modifiable and can be optimized through continuing education and quality improvement initiatives to raise the standard of care in breast surgery.

Internationally, quality indicators are being increasingly measured in breast surgery, and many regions have established minimum targets for achievement.5,6,7,8,9,10,11 Indicators are available for the full continuum of breast cancer care from the initial visit and diagnostic workup, to surgery, adjuvant therapies, and long-term follow-up.5,6,7,8,9,10,11 Quality indicators are variable between regions and there is documented inconsistency in compliance with these standards.5,12,99,100 As a result, some patients may receive a lower quality of care.

Surgeon-specific quality indicators have been described. Many of these focus on the quality of the preoperative workup.6,8,10,11 For example, the use of a minimally invasive biopsy for histologic diagnosis of malignancy prior to surgery has been cited as a key quality indicator in many jurisdictions.6,8,10 Surgeon specialization and higher case volume have both been associated with increased use of minimally invasive biopsy preoperatively.15,20,49,50,95 Another key quality indicator is the avoidance of surgical overtreatment.6,8,10,11 All four surgeon factors identified in this review have been associated with the provision of guideline-concordant care and avoidance of overtreatment of disease. Finally, rates of immediate reconstruction after mastectomy have also been noted as an important quality indicator.6,10,11 Surgeon volume was associated with improved outcomes in this domain.51 Surgeon-specific quality indicators such as those described above can be targeted for quality improvement through education programs and modification of practice patterns to achieve higher levels of compliance and standards of care.

There are currently many options available to trainees and practicing surgeons to advance their education and training in breast and oncoplastic surgery. These options include short hands-on or online courses,101,102,103,104,105 meetings held by professional societies, and formal fellowships.106,107,108,109 Breast surgery fellowships are available globally in Canada, the USA, Europe, and Australia and New Zealand.108 However, the quality of training received at all fellowship programs may not be equal.108,109 To address this issue, the Society of Surgical Oncology has made efforts to improve the overall standard of education by establishing educational objectives within its accredited programs.108,109 It should be noted that not all fellowship opportunities include oncoplastic training. Surgeons wishing to include oncoplastic breast surgery in their practice should consider this when pursuing and selecting a fellowship. In addition to formal training, other educational and professional development opportunities exist such as membership in relevant professional societies and participation in multidisciplinary rounds. For surgeons practicing in rural or regional settings, virtual regional multidisciplinary rounds and access to initiatives such as community clinical oncology programs are powerful resources.97 At this time, there is no clear evidence on how much additional training is required to see an improvement in surgical outcomes. Furthermore, it is not feasible for every surgeon practicing breast surgery to complete a formal fellowship.

While individual surgeon practice factors play an important role, it should be recognized that they are not alone in influencing breast surgery outcomes. Other factors should also be considered in the development and execution of quality improvement measures. It has been well documented in the literature that hospital/institutional factors play a role in outcomes. Similar to surgeon volume, facility volume has also been associated with improved surgical outcomes.110,111,112 Additionally, hospital academic affiliation has been described to improve outcomes.113 Moreover, many regions have strict accreditation criteria for breast centers designed to optimize patient outcomes.7,9

In this thorough review of the literature, we have identified four modifiable surgeon factors associated with improved outcomes in breast surgery. From these factors, we have developed a definition of the modern breast surgeon to help guide quality improvement and continuing education initiatives with the goal of raising the overall standard of breast surgical care. On the basis of the examined literature, the modern breast surgeon has a moderate- to high-volume surgical practice, engages in additional training opportunities in breast surgery and oncoplastics, maintains memberships in relevant societies, and remains up to date on key literature. Each component of this definition can be targeted for quality improvement and continuing education.

This review has both strengths and limitations. This study has provided a comprehensive review of the existing literature with a broad search and additional citation searching. Additionally, this review incorporates data originating from a wide geographic distribution providing multiple perspectives on the complex concept of expertise in breast surgery. Finally, the studies and data included were limited temporally to ensure a more modern context. However, there was heterogeneity in the definition of a high- versus low-volume surgeon as well as the definitions of positive and negative margins among the included studies. There was also variation in the OPBS techniques employed in studies. This was likely related to the variations in practice patterns of breast and general surgeons globally. Additionally, use of OPBS techniques was used as a surrogate marker for additional training in oncoplastics for the purpose of this paper. Finally, the breast surgeon’s practice also encompasses treatment of benign disease, however, there were no data available in the literature for surgeon factors influencing outcomes in benign breast disease.

Further research to better understand the surgeon factors influencing breast surgery outcomes should include the development of a clear evidence-based definition of high- versus low-volume surgeons. We recommend a large database study be conducted to identify benchmarks for high-, intermediate-, and low-volume surgeons that can be used going forward in future studies. As there were limited data available on the impact of professional development and quality improvement activities, further exploration to determine the best options to be used by surgeons would be beneficial. Finally, studies investigating surgeon factors and outcomes in benign breast disease would be valuable, as most breast surgeons also care for patients with benign disease.