A comparative study of learning curves among general surgery residents for intraoperative ultrasound-guided breast-conserving surgery (2025)

Introduction

Breast cancer is one of the most crucial health problems in women and the leading cause of cancer-related deaths globally1. The incidence of early-stage breast cancer in women has been steadily increasing owing to advancements in imaging techniques, improvements in patient awareness, and widespread use of screening mammography2. Breast-conserving surgery (BCS) with adjuvant radiotherapy has become the standard treatment of choice for early-stage breast cancer because of its equivalent survival rate to mastectomy3. The critical point in reducing recurrence rates and omitting secondary interventions is achieving negative surgical margins during index surgery4,5. Ultrasound imaging is one of the most extensively used tools for the preoperative assessment and intraoperative localization of breast cancer. Since the introduction of intraoperative ultrasound (IOUS) guidance in 1988, the value of IOUS has been confirmed for both palpable and nonpalpable lesions, with significant improvements in achieving negative lumpectomy margins6,7. Moreover, IOUS has major advantages in improving cosmetic outcomes, increasing surgical margin accuracy and patient comfort, and reducing time and cost8. However, the success of IOUS guidance largely depends on operator training and experience9,10,11. There is no objective, concrete criteria for accurately evaluating the expertise required for surgeons to employ this technique. This study compared the rates of achieving negative surgical margins using real-time IOUS guidance between breast surgeons and general surgical residents. Additionally, we aimed to determine the learning curve required for residents to master IOUS, thereby revealing the impact of training and experience on surgical outcomes.

Methods

In this prospective study conducted between December 2022 and December 2023, 96 consecutive patients with non-palpable breast lesions determined via screening mammography (BIRADS 4–5) and diagnosed with invasive breast cancer with core needle biopsy were included. All patients underwent IOUS-guided BCS and cavity shavings from the tumor bed as the standard of operative protocol. Breast surgeons and residents performed ex vivo sonographic evaluation of surgical margins in specimens removed via IOUS-guided BCS. This study included female patients aged > 18years who had undergone BCS. Patients requiring secondary surgery because of recurrence or margin positivity and those planned for mastectomy were excluded. The study commenced after obtaining ethical approval and written informed consent from patients. Operative choice (quadrantectomy, segmental resection, lumpectomy, or oncoplastic reconstruction) depended on patient factors, patient decisions, and the breast surgeon’s preferences. A handheld wireless ultrasound device [Clarius], [L15 HD3 Linear Scanner, Canada] was used for all IOUS and ex vivo specimen margin assessments. The excised specimen was marked with sutures to ensure correct orientation for subsequent imaging and histopathological examinations. The same team (the attending breast surgeon and the three residents in operation) performed IOUS-guided BCS and margin evaluations for each case. Ex vivo sonographic evaluation of six surgical margins (anterior, posterior, superior, inferior, lateral, and medial) of the specimen was conducted in a stepwise manner to ensure thorough and unbiased assessment. Residents attended basic simulative ultrasound training to ensure the primary objective of assessing learning curves. Initially, the evaluation was performed by a first-year surgical resident (R1) with no prior experience in breast surgery. Following this, two third-year surgical residents (R2 and R3), each with one year of experience in breast surgery, performed their evaluations independently. Finally, the attending breast surgeon, with extensive expertise in breast surgery, conducted the assessment. All evaluations were performed in a blinded manner to eliminate potential bias and ensure objectivity. The findings from each evaluation were meticulously recorded in the database for subsequent analysis and comparison. If the sonographically measured distance between the tumor and the surgical margin in the specimen was ≥ 1mm, it was classified as sufficient and recorded as negative (N0). However, if tumor continuity was detected at the margin or suspicious sonographic features of tumor continuity (as determined by either the breast surgeon or residents), these specimen margins were classified as insufficient and thus recorded as positive (N1) (Fig.1). After coding and documenting all margins as sonographically positive or negative, the breast surgeon re-evaluated the specimen using ex vivo sonography to make a final decision regarding the performance of selective cavity shaving. Subsequently, the oriented excised specimens and shaved cavity margins were weighed, embedded in formalin, and sent for permanent histological examination. The recorded IOUS data for the residents and attending breast surgeons were compared with the histopathological findings, which are regarded as the gold standard. This comparison aimed to determine the number of cases required for residents to achieve competency in IOUS and complete their learning curve.

Intraoperative ultrasound images demonstrating the assessment of surgical margins during breast-conserving surgery.

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Statistical analysis

Analyses were conducted using Statistical Package for Social Sciences (SPSS Inc., Chicago, IL, USA) version 22. Descriptive data are presented as n (%) for categorical variables and mean ± standard deviation (mean ± SD) for continuous variables. The normality of the distribution of continuous variables was assessed using the Kolmogorov–Smirnov test. The Mann–Whitney U test was used to compare two independent groups. Cohen’s kappa analysis was used to test the agreement between residents and attending surgeons. According to the Kappa statistic, < 0.000 was interpreted as poor, 0.00–0.20 as insignificant, 0.21–0.40 as low, 0.41–0.60 as moderate, 0.61–0.80 as substantial, and 0.81–1.00 as almost perfect agreement. Differences were considered statistically significant at p < 0.05.

Ethical approval

This study was reviewed and approved by the Ethics Committee of Zonguldak Bülent Ecevit University (approval number: 2022/22-7, dated 14th December 2022). All methods were performed following the relevant guidelines and regulations.

Results

A total of 96 patients with a mean age of 56.2 ± 11.8years (range: 31–84) were included. When examining the localization of the tumors, 53.1% were on the left side, and 46.9% were on the right side, with an average tumor size of 1.6 ± 0.5cm. Regarding tumor type, 80.2% were invasive ductal carcinomas, 11.5% were invasive lobular carcinomas, 5.2% were invasive mucinous carcinomas, and 3.1% were ductal carcinomas in situ. According to the pathology results, 3.1% of all pathologies were positive, and 96.9% were negative. Similarly, based on the shaved pathology results, 3.1% of all specimens were positive, and 96.9% were negative. Histopathological analysis of the tissues obtained through cavity shavings in 3.1% of the cases indicated tumor positivity, at least at one margin in the cavity specimens, necessitating re-excision, all of which were ductal carcinomas in situ (DCIS) (Table 1).

Full size table

The agreement between the first resident and the breast surgeon was poor in the anterior (κ < 0.000; p < 0.001), posterior (κ < 0.000; p < 0.001), inferior (κ < 0.000; p < 0.001), and medial (κ < 0.000; p < 0.001) directions. Moderate agreement was observed in the superior (κ = 0.492, p < 0.001) and lateral (κ = 0.546, p < 0.001) directions. Anterior (κ < 0.000; p < 0.001), posterior (κ < 0.000; p < 0.001), inferior (κ < 0.000; p < 0.001), and medial (κ < 0.000; p < 0.001) directions. There was low agreement in the superior direction (κ = 0.392; p < 0.001), and substantial agreement in the lateral direction (κ = 0.663; p < 0.001). Agreement between the third and breast surgeons was poor in the anterior (κ < 0.000; p < 0.001), posterior (κ < 0.000; p < 0.001), inferior (κ < 0.000; p < 0.001), and medial (κ < 0.000; p < 0.001) directions. Substantial agreement was observed in the superior (κ = 0.796, p < 0.001) and lateral (κ = 0.746, p < 0.001) directions (Table 2). When comparing the decisions made by the first and second surgical residents using IOUS with the pathology results, the highest accuracy was observed in the anterior region (100%). For the third surgical resident, the highest accuracy was observed in the anterior (100%), posterior (100%), and lateral (100%) regions when comparing IOUS decisions with pathology results. The decisions made by the breast surgeon using IOUS were 100% accurate in all regions compared to the pathology results. When evaluating the overall accuracy rates, the first surgical resident had an accuracy of 96.9% or higher, the second surgical resident had 99% or higher accuracy, the third surgical resident had 97.9% accuracy, and the breast surgeon had 100% accuracy. Diagnostic values of the surgical residents and breast surgeon compared to the pathology results are presented in Table 3.

Full size table
Full size table

No significant differences were observed in terms of tumor size and patient age between the accuracy of the surgical residents and the breast surgeon, the presence of re-excision, or the positivity of the surgical margins (p > 0.05) (Table 4). The breast surgeon accurately determined the surgical margin status by using IOUS in all 96 cases. The first surgical resident accurately determined the surgical margin status using IOUS in 88 of 96 cases (91.7%) but failed in eight cases (8.3%). The second surgical resident accurately determined the surgical margin status in 92 out of 96 cases (95.8%) but failed in 4 cases (4.2%). The third surgical resident accurately determined the surgical margin status in 91 of 96 cases (94.8%) but failed in 5 cases (5.2%). Initially, surgical residents observed low accuracy rates with IOUS. However, a significant increase in the cumulative accuracy rate was observed after the 14th case for the first resident, after the 9th case for the second resident, and after the 12th case for the third resident. When evaluating the learning curves of the three residents, it was observed that after an average of 12 cases, their cumulative accuracy rates reached the level of the breast surgeon. This indicates that the residents showed a significant improvement in the use of IOUS as they gained experience and worked on more cases (Fig.2).

Full size table

The learning curve of general surgery residents in assessing the surgical margin status of a breast specimen with intraoperative ultrasound.

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Discussion

This prospective comparative study was an isolated evaluation focused on systematic sonographic measurement of ex vivo specimen margins via real-time IOUS after BCS by a breast surgeon and surgical residents, providing new insights into surgical training and learning curves. Initially, the accuracy of the residents’ IOUS assessments was inferior to that of the breast surgeon, but showed marked improvement, starting from an average of the 12th case. This increase in accuracy suggests that residents’ proficiency in ultrasonography significantly improved with greater experience and handling of more cases. Krekel et al. found that performing eight procedures is sufficient for a surgeon to gain the expertise necessary to combine ultrasound with palpation guidance during surgery12. Similarly, a 2019 study by Esgueva et al. on the learning curves for IOUS-guided surgery in breast cancer indicated that IOUS is easy to implement and that surgeons can acquire the necessary skills to perform the technique in only 11 cases13. In our study, the slightly higher number of cases required for the learning curve compared to other studies might be attributed to several factors. First, the differences in the participating surgeons’ experience and basic ultrasound skills may have contributed to this. In addition, the complexity of the cases in our study may have extended the learning process. Finally, our study focused solely on measuring the learning curve, which may have resulted in more precise and detailed results.

IOUS is a non-invasive method compared with other techniques that require breast compression or puncture, reducing the psychological stress experienced by patients before surgery. IOUS allows surgeons full freedom to choose the most appropriate oncoplastic surgical approach. As it can be performed directly in the operating room and entirely by the surgeon, it alleviates organizational issues and the need for coordination between departments. This enables surgeons to maintain full control over the surgical process and to perform the operation more efficiently14,15. Ultrasonography has gained popularity in breast surgery as an intraoperative tool for localizing benign and malignant lesions. It enables surgeons to visualize the three-dimensional boundaries of a lesion in real-time, significantly enhancing the precision of excision. This real-time feedback method is invaluable for achieving accurate margins and reducing the need for reoperation16. Additionally, IOUS enables the precise excision of suspicious margins, reducing the need for extensive tissue removal, typically required by systematic margin shaves10. Whitehouse et al. demonstrated that surgeon-performed breast ultrasound achieved high accuracy, with a sensitivity of 98.3% and specificity of 91.7% in distinguishing between benign and malignant lesions, and showed 96% concordance with radiologist-performed ultrasound17. In our study, based on permanent pathological examination of excised specimens, the breast surgeon accurately determined the surgical margin status using IOUS in all 96 cases. In contrast, the surgical margin status of the first surgical resident was accurately determined in 88 of 96 cases (91.7%) but failed in eight cases (8.3%). The second surgical resident accurately determined the surgical margin status in 92 out of 96 cases (95.8%) but failed in 4 cases (4.2%). The third surgical resident accurately determined the surgical margin status in 91 of 96 cases (94.8%) but failed in 5 cases (5.2%). Notably, residents’ accuracy improved over time. A recent study found that when IOUS was used for excision, negative margins were achieved during primary surgery in 92.4% of nonpalpable tumors and 91% of palpable lesions18. Similarly, our study achieved a negative-margin rate of 96.9%. Cakmak et al. stated that only five patients (2.4%) required a secondary intervention, with no statistically significant difference between palpable and nonpalpable lesions18. Similarly, our finding that 3.1% of patients required re-excision after BCS aligns with the recent data on re-excision rates. The consistent integration of ultrasound in each case resulted in less tissue removal, with negative surgical margins. In contrast, Fisher et al. found that re-excision rates varied significantly according to the patient and tumor characteristics. They reported re-excision rates of 19% among patients who initially underwent BCS, with higher rates observed in patients with larger tumors and those treated in specific regions19. The SHAVE and SHAVE2 trials indicated that patient age and tumor size are critical factors influencing margin status, underscoring their importance as predictors of margin status20. However, in our study, no significant differences were found between the general surgery residents and the breast surgeons regarding the accuracy of identifying surgical margins, the presence of re-excision, and surgical margin positivity when considering tumor size and patient age (p > 0.05). The fact that the margin was positive in 3 cases despite cavity shavings, and all of these cases were DCIS, emphasizes that IOUS-guidance may not be an effective method in DCIS.

Ultrasound-guided BCS is a relatively new technique that requires a combination of knowledge and skills to interpret ultrasound images. This study suggests that the variation in the assessment of the margin status of specimens using IOUS between residents and breast surgeons can be explained by the differing levels of experience. According to García de Casasola Sánchez et al., enhancing both the practical and interpretive capabilities of USG practitioners requires a solid anatomical foundation that enables them to assess pathological occurrences based on this knowledge21. Comprehensive theoretical instruction on the features of USG equipment, detailed studies of the anatomy of specific organs and their pathologies, and hands-on training under the supervision of experienced personnel are critical to both the learning process and the practical efficacy of USG applications22. Implementing a structured ultrasound curriculum that includes pre-clinical and clinical courses significantly enhances students’ understanding of anatomy, physiology, and pathology while improving their practical skills23. To optimize the use of ultrasound in treatment decisions, it is imperative to secure standardized training and conduct specific evaluations under the guidance of a supervisor. The most crucial aspect of ultrasound is its ability to perform scans, which is fundamental for producing adequate images. Therefore, developing the visual-spatial and visual-motor skills necessary to operate a transducer and obtain images is of paramount importance24. Intraoperative real-time ultrasound-guided BCS has been performed on all patients with palpable and nonpalpable breast cancer at our institution for more than two decades. We concur with Fosko et al. regarding the clinical advantages of increasing the familiarity with and utilization of IOUS during BCS over traditional localization techniques16. Their assertion that ultrasound certification may lead to increased use of IOUS among surgeons is well-founded and aligns with current trends in surgical practice. Incorporating IOUS not only enhances the precision of tumor localization and margin assessment but also potentially improves patient outcomes by reducing the need for re-excision. Promoting ultrasound training and certification among breast surgeons could play a critical role in improving the efficacy and safety of BCS16.

The limitations of this study include its single-center design and the inclusion of only three general surgery residents. Additionally, the study did not include resident groups who had general ultrasound training but lacked IOUS experience in BCS. The limited sample size may have affected our findings’ generalizability and long-term applicability.

In conclusion, ultrasound-guided BCS is an emerging technique that combines ultrasound imaging with surgical excision. This method is straightforward, time-efficient, comfortable, and carries minimal risk of complications. General surgery residents with basic ultrasound training and experience achieved consistent accuracy after an average of 12 cases, emphasizing the completion of their learning curve. Initially, the residents felt that it was challenging to rely solely on ultrasound images and had to suppress their tactile senses. However, they quickly adapted and mastered fundamental ultrasound skills. Our findings strongly support the integration of IOUS into surgical training programs, highlighting its potential to significantly enhance surgical precision and improve both patient and financial outcomes.

Data availability

The dataset used in our study was not publicly available to ensure the privacy and confidentiality of the patients involved. Interested parties can request access to the dataset by contacting the corresponding authors. Access to the dataset will be granted upon completion of a data usage agreement, according to the guidelines set by the University’s Research Ethics Committee.

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Funding

This study received no specific grants from the public, commercial, or not-for-profit funding agencies.

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Authors and Affiliations

  1. Department of General Surgery, Bülent Ecevit University School of Medicine, Bülent Ecevit University, 67630, Esenköy-Kozlu, Zonguldak, Turkey

    Hakan Balbaloglu,Hatice Tekin,Ipek Yorgancioglu,Ilhan Tasdoven,Ufuk Tali,Mustafa Comert&Guldeniz Karadeniz Cakmak

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  1. Hakan Balbaloglu

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  2. Hatice Tekin

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  3. Ipek Yorgancioglu

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  4. Ilhan Tasdoven

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  5. Ufuk Tali

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  6. Mustafa Comert

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  7. Guldeniz Karadeniz Cakmak

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Contributions

The authors confirm contribution to the paper as follows: study conception and design: H.B. and G.K.C.; data collection: H.T., I.Y., I.T., U.T.; analysis and interpretation of results: H.B. and G.K.C.; draft manuscript preparation: H.B., M.C., and G.K.C. All authors reviewed the results and approved the final version of the manuscript.

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Correspondence to Hakan Balbaloglu.

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A comparative study of learning curves among general surgery residents for intraoperative ultrasound-guided breast-conserving surgery (3)

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Balbaloglu, H., Tekin, H., Yorgancioglu, I. et al. A comparative study of learning curves among general surgery residents for intraoperative ultrasound-guided breast-conserving surgery. Sci Rep 14, 18881 (2024). https://doi.org/10.1038/s41598-024-70040-2

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Keywords

  • Breast-conserving surgery
  • Intraoperative ultrasound
  • Surgical margins
  • Learning curve
A comparative study of learning curves among general surgery residents for intraoperative ultrasound-guided breast-conserving surgery (2025)
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