Summary

1. Introduction

Endoscopic-assisted breast surgery (EABS) has been reported to provide better cosmetic outcomes [1–5] and comparable oncological results [1, 3, 6] for breast cancer patients compared with conventional surgery, using small incisions in inconspicuous areas such as the axilla or lateral chest. However, in patients with high-burden axillary lymph node (ALN) metastasis requiring axillary lymph node dissection (ALND), we often extend the EABS incision by 1-2 cm to access the deep and limited space of the axilla for the conventional ALND. This extension, along with the need for heavy assistant retraction and extensive surgical dissection to achieve adequate exposure [7–10], may compromise the benefits of small incisions in EABS and result in patient morbidities such as lymphedema or chronic arm numbness.

Compared with conventional ALND, multiple-incision two-dimensional (2D) endoscopic-assisted ALND has demonstrated acceptable numbers of harvested ALNs, lower postoperative pain, better shoulder range of motion, and noncompromised short- to medium-term oncological outcomes [7–14]. Therefore, we adapted the concept of our single-port air-insufflated breast cancer surgery [15] to develop the single-port three-dimensional endoscopic-assisted axillary dissection (S-P 3D E-ALND) performed via the single EABS incision without the need for wound extension. This approach aims to improve visualization of the deep axilla and increase the chances of preserving all neurovascular structures, thereby preventing the risk of arm morbidity. In addition, this technique can be an alternative for breast cancer patients undergoing EABS with high-burden ALN metastasis requiring ALND.

In this study, we aim to describe the surgical technique of the S-P 3D E-ALND using three different types of energy devices: monopolar Endo hook, or bipolar sealing instrument (LigaSure, Medtronic, Minneapolis, Minnesota, USA), or ultrasound energy device (Sonicision, Medtronic, Minneapolis, Minnesota, USA). We also report our preliminary results regarding perioperative outcomes, complications, and short-term oncological outcomes herein.

2. Materials and Methods

This study proposes the surgical technique of the S-P 3D E-ALND and reports its preliminary clinical outcomes. Breast cancer patients with pathological ALN metastasis undergoing the S-P 3D E-ALND between January 2023 to September 2023 at Changhua Christian Hospital (CCH), a tertiary medical center at central Taiwan, were included. The clinicopathological characteristics of patients including patient’s age, body mass index, tumor histology and molecular subtypes, cancer staging, neoadjuvant treatment, and types of surgery were retrospectively retrieved. Perioperative parameters and postoperative outcomes were reviewed. All data were collected by specially trained nurses and confirmed by the principal investigator (HWL) subsequently.

The study was approved by the Institutional Review Board of the CCH (CCH IRB no. 230219). This report includes data and photos of several patients who had agreed and signed the consent for publication of their pictures at the outpatient clinic during the follow-up time when we started conducting this study.

2.1. Surgical Technique

2.1.1. Indications for S-P 3D E-ALND

Patients are evaluated for eligibility for the S-P 3D EABS and E-ALND using preoperative breast sonography, mammography, and/or breast magnetic resonance imaging. In addition, liver sonography, chest x-ray, and whole-body bone scan are used to exclude the possibility of distant metastasis. Indications for the S-P 3D E-ALND are similar to the conventional ALND, including those with biopsy-proven ALN metastasis in clinically palpable ALNs or high ALN disease burden on ultrasonography or MRI, as well as clinically node-positive status after neoadjuvant systemic therapy. The S-P 3D E-ALND is offered to patients scheduled for the S-P 3D EABS as the therapeutic breast cancer surgery and is performed in the same operation following EABS.

2.1.2. Sentinel Lymph Node Biopsy (SLNB) With Dual Tracers and Axillary Reverse Mapping

In the operating room, the patient is aligned at supine position with her arm abduction to 90° (Figures 1(a), 1(b), and 2(a)). We place surgical drapes underneath her scapula to elevate it to 30° (Figure 2(a)). We routinely conduct the SLNB with dual tracers, which include colloidal human serum albumin labeled with technetium-99m (Tc-99m) and indocyanine green (ICG), and combine with the axillary reverse mapping [16, 17] with patent blue dye. A 2.5–4 cm incision is created at lower axilla, over the location of the most intense radioactivity from Tc-99m indicating the location of sentinel nodes (Figures 1(c) and 2(b)). During the dissection, sentinel nodes displaying high radioactive signal and/or ICG fluorescence are removed (Figures 2(c) and 2(d)). If a blue-stained arm node is found, preservation of that node is considered to minimize the risk of postoperative lymphedema (Figures 2(e) and 2(f)). After removal of the SLNs, a gamma probe is used to confirm the absence of high residual radioactive signal in the axillary cavity. An intra-operative frozen section analysis of the SLNs is done. While awaiting the result, an EABS, either endoscopic-assisted breast-conserving surgery (E-BCS) or endoscopic-assisted nipple sparing mastectomy (E-NSM), is performed, which techniques are described in previous publications [4, 15, 18]. In case whose metastasis is identified in the SLNs meeting the criteria for ALND, the S-P 3D E-ALND is performed [19–21].

2.1.3. S-P 3D E-ALND

The surgeon and camera assistance stand next to the patient’s torso and the endoscopic station is set at the opposite side (Figures 1(a), 1(b), and 2(g)). After EABS, if the S-P 3D E-ALND is indicated, a glove-made single port (Figures 1(d), 1(e), and 2(h)) or a commercial port (Glove Port; Nelis, Gyeonggi-do, South Korea, Figure 1(f)) is reapplied. Our glove-made single port is created with Alexis wound protector (Applied Medical, Rancho Santa Margarita, California, USA, Figure 1(e)), a surgical glove, two 5-mm trocars, and a 12-mm trocar, which are arranged as in Figures 1(c) and 1(d). An optional 5-mm trocar may be added if additional grasper forceps are required to retract the pectoralis major border during the dissection (Figure 2(h)). After the port placement, carbon dioxide insufflation with the air pressure at 12 mmHg is applied to create a space for the S-P 3D E-ALND. A 30° 10-mm diameter camera TIPCAM 1 S 3D VIDEO Endoscope (KARL STORZ, Tuttlingen, Germany) is used for visualization (Figures 1(c) and 1(g)).

We perform the S-P 3D E-ALND using either one of the 3 different energy devices; monopolar Endo hook (Figure 1(g)), LigaSure (Figure 1(h)), or Sonicision (Figure 1(i)). The decision to use the certain energy device depends on the surgeon’s experience and the patient’s financial status. Specifically, in the initial phase, advanced energy sealing devices have been considered to control intraoperative bleeding. Later, once we became accustomed to the procedure or when patients could not afford the cost of advanced equipment, we performed the S-P 3D E-ALND with a monopolar Endo hook. All endoscopic instruments are demonstrated in Figure 1(d), 1(e), 1(f), 1(g), and 1(i).

When the S-P 3D E-ALND is performed, an axillary cavity is divided into four quadrants based on an intersection between lateral thoracic vein and the second intercostobrachial nerve (Figure 1(j)). We start the dissection at lateral border of pectoralis major muscle, which is the easiest part to access (Figure 2(i)). The dissection begins at a lower–inner quadrant (Figure 2(j)) and follows by upper–inner (Figure 2(k)), upper–outer (Figure 2(l)), and lower–outer quadrants (Figure 2(m)), respectively. An axillary content in each quadrant is subsequently removed to complete the standard level I and II ALND. The resected axillary specimens are temporarily placed above the pectoralis major muscle in E-NSM (Figure 2(n)) and in the glove part of the single port in E-BCS. Then, inflated gas is discontinued and a single port is taken off so that all axillary contents can be removed through an axillary incision (Figures 2(o) and 2(p)). The second intercostobrachial nerve, lateral thoracic vein, axillary vein, long thoracic nerve, and thoracodorsal neurovascular bundle are identified and preserved (Figure 2(q)). The wound is irrigated with warm distilled water and hemostasis is assured. Then, closed-suction drains are placed, and the incision is closed with Vicryl 3-0 and Monocryl 4-0 (Figure 2(r)).

The surgical technique of S-P 3D E-ALND is demonstrated in Figure 2 and Supporting Video 1 (monopolar Endo hook), Video 2 (Sonicision) and Video 3 (LigaSure).

3. Results

4. Discussion

In this study, we propose our new technique of the S-P 3D E-ALND and report preliminary results of this procedure. We enrolled 11 consecutive breast cancer patients with ALN metastasis undergoing the S-P 3D E-ALND. The clinical efficacy and short-term oncological outcomes of the S-P 3D E-ALND were retrospectively analyzed. The success rate of our S-P 3D E-ALND was 100%. None of the patients reported complication, total sensory loss of medial arm, or frozen shoulder during the median follow-up time of 7 months.

Despite the trend of de-escalating axillary surgery, NCCN guideline still recommends ALND for those with locally advanced or high ALN burden and residual nodal disease after neoadjuvant systemic therapy [21]. In our study, majority of the patients (72.7%) were in stage II–IV and had received neoadjuvant treatment (Table 1). Consequently, if micro- or macrometastasis was detected in a sentinel node during intraoperative frozen section analysis, ALND was indicated according to current standards of care [21]. This is reflected in our results, where the median number of metastatic ALNs identified was only 1 (Table 2).

Previously, when conventional ALND was required during the EABS, we faced challenges that necessitated extending the incision by 1-2 cm and relied heavily on assistant retraction to achieve adequate exposure in the deep and limited axillary space [7–10]. To address these challenges, we developed the S-P 3D E-ALND. This technique enhances visualization and minimizes the risk of neurovascular injury while allowing us to perform ALND effectively.

Another crucial indication for ALND is to establish adequate nodal status, which is essential for guiding adjuvant therapy, such as nodal irradiation [24] and the administration of CDK-4/6 inhibitors, given that nodal status remains a pivotal factor in treatment decisions [25, 26]. Therefore, the S-P 3D E-ALND can be an alternative in these settings.

From our results, the conversion rate to open surgery was 0, indicating the successful completion of the intended S-P 3D E-ALND procedure for all patients. The average operative time (E-ALND time) was comparable with those reported in previous studies [8–12, 14, 22] (Table 3). Intraoperative blood loss was counted for the entire operation as a routine practice in our center. However, we estimated minimal blood loss (3 [IQR = 3, 5] mL) during the specific period of S-P 3D E-ALND. These outcomes can be attributed to the high level of experience and expertise of the surgeons involved in our institution.

An advantage of gas inflation system and image magnification of 3D camera in the S-P 3D E-ALND allows for an adequate exposure of the operative field [15, 18, 27, 28] without the need for extending the incision nor assistant retraction, which is typically required in conventional ALND. Moreover, the image magnification system aids in the clear identification and preservation of all neurovascular structures, thereby reducing the risk of associated morbidities. As a result, none of the patients in our study experienced lymphedema, shoulder stiffness, or chronic arm numbness postoperatively.

In this study, we share our experience with 3 different energy devices; monopolar Endo hook, which rarely used in previous studies [8–12, 22] (Table 3), and advance sealing devices, LigaSure & Sonicision. Operative time and blood loss from three energy devices showed no significant difference (Table 4). From our experience, monopolar Endo hook appears to be effective to stop bleeding and can reduce the operative cost. In additionally, monopolar Endo hook is more available especially in low-middle income countries, which may facilitate an accessibility to this innovative technique. However, LigaSure and Sonicision seem to produce less blood loss and less drainage volume in breast and axillary surgery reported in previous studies [29, 30]. Therefore, we suggest using advance sealing devices in the patients who have a high risk of bleeding or high-output drainage.

Nevertheless, some limitations were considered in our study. First, our study was a preliminary report with a small sample size, which may restrict the generalizability of our findings. To address this limitation, we have been conducting a prospective study involving a larger cohort of patients to compare our results with conventional ALND and to evaluate patient satisfaction and aesthetic outcomes. Second, the median follow-up period of 7 months in our study may be considered relatively short for assessing medium- to long-term oncological safety. We have been extending the follow-up duration to gather more comprehensive and reliable long-term outcomes. Despite these limitations, we propose an innovative minimal-access technique for ALND using various energy devices and highlight its perioperative safety for patients undergoing EABS as therapeutic breast cancer surgery, aligning with the trend toward MABS.

5. Conclusions

The S-P 3D E-ALND can serve as an alternative approach for ALND in breast cancer patients undergoing EABS, as our findings indicate it results in only minor complications. However, we have been conducting further studies to gather long-term oncological outcomes and patient’s satisfaction.

Ethics Statement

This study was approved by the Institutional Review Board of the Changhua Christian Hospital (CCH IRB no. 230219).

Consent

All the individual person’s data included in this study have consent for publication.

Conflicts of Interest

The authors declare no conflicts of interest.

Author Contributions

H.-W.L. did the surgery and conceptualized the study. C.S.-L. drafted the manuscript. H.-W.L. and S.-L.L. did the revision and proof reading of the manuscript. R.H.-H. did the pathology review. P.C. illustrated the figures. S.-T.C., D.-R.C., and H.-I.H. reviewed and added comments. All the authors have read and approved the final manuscript.

Funding

This study was sponsored by research funding provided by the Changhua Christian Hospital 109-CCH-IRP-093, 110-CCH-IRP-042, 110-CCH-ICO-155, 112-CCH-IRP-051, 112-CCH-IRP-082, 112-CCH-IRP-091, and 112-CCH-HCR-158.

Supporting Information

Additional supporting information can be found online in the Supporting Information section.