Comparison of single-pore non-liposuction near-infrared laparoscopy with conventional open surgery for axillary sentinel lymph node biopsy in patients with early breast cancer: a single-center, small-sample retrospective study

Endoscopic axillary lymph node surgery for early breast cancer (EBC) has historically been conducted using liposuction [1‐5]. Liposuction allows smooth construction of the cavity, the axillary lymph nodes can be clearly displayed, and the difficulty of the surgery is reduced; thus, this technique is generally beneficial. However, liposuction increases axillary trauma, and its safety regarding the tumor is also questioned by some experts [6, 7]. Is it possible to perform an endoscopic sentinel lymph node biopsy (SLNB) using a non-liposuction method? We reviewed domestic and foreign literature and found several reports on this topic; however, most involved traditional endoscopic and single dyeing methods [8, 9], which is contrary to the fact that pigment combined with the fluorescence double dyeing method is widely used in domestic clinical practice to reduce the false negativity rate of SLNB [10]. In addition, the traditional endoscope has no near-infrared (NIR) fluorescence function, which limits its application as this form of fluorescence is used as a tracer in domestic mainstream SLNB. However, recently developed NIR endoscopes with fluorescence capabilities can address this issue. Can these be applied for non-liposuction SLNB? At present, no relevant reports have been published domestically or internationally, and only a few studies have been reported on SLNB by NIR endoscopy with the liposuction method [11]. The tumor safety of the liposuction method remains controversial [6, 7]. For this reason, we retrospectively analyzed the clinical data of early breast cancer patients with indocyanine green (ICG) fluorescence combined with a carbon nanoparticle suspension (CNS) as a tracer using a non-liposuction single-pore NIR endoscopic technique for axillary SLNB. The effects of this approach were compared with those of traditional open incision surgery in the same period to elucidate the efficacy and safety of this technique. This study was supported by the Medical Research Program of the Foshan Health and Family Planning Commission and the Foshan High-Level Medical Talent Training Fund, and approved by the ethics committee of the hospital (Approved on March 8, 2022, No.: 2022142).

Endoscopic technology is widely used in gynecology [14], gastrointestinal surgery [15], hepatobiliary surgery [16], cardiothoracic surgery [17, 18], and thyroid surgery [19]; however, it is relatively rare in breast surgery and is mostly limited to gynecomastia [20] and axillary lymph node dissection [1‐5]. The reason may be the lack of natural cavities in the breast and axilla. The foundation for the successful implementation of endoscopic surgery is the establishment and maintenance of an operating space, which is a challenge in breast surgery. However, in recent years, through exploration by domestic and foreign scholars, endoscopic technology for breast surgery [21, 22] has been greatly developed, and some hospitals have even conducted robotic breast surgery [23, 24].

In this study, 30 patients with early-stage breast cancer in the Endoscopy group were treated with ICG fluorescence in combination with CNS pigment double-dyeing and received axillary SLNB from the axillary midline approach of the transverse thorax using a single-hole non-liposuction method. The SLNB operation had a 100% success rate. The mean operation time, the volume of intraoperative bleeding, the postoperative axillary extubation time, and the complications (poor wound healing, upper limb function restriction, and upper limb edema) did not differ between the open and endoscopic groups. Notably, the endoscopic surgery time was not significantly longer than the open surgery time. The results revealed that the volume of axillary drainage after surgery was greater in the open group than in the Endoscopic group, and this difference was significant. This finding may be due to the ultrasonic knives used for dissection during endoscopic surgery, which are more favorable than the high-frequency electrospray knives used to close the tiny lymphatic vessels in the axilla, reducing the probability of lymphatic leakage. However, one patient in the Endoscopic group had mild to moderate impairment of upper arm function on the affected side after surgery, with a DASH score of 56. The reason may be that endoscopic axillary SLNB surgery is not mature enough at an early stage, the operation time is relatively long, and the upper arm of the affected side is excessively tightly bandaged. The “full moon” position, which retains elbow flexion and elevation on a head frame for a prolonged time, is related to the patient’s forearm musculocutaneous nerve injury, which recovered within 2 months after surgery after acupuncture and intermediate frequency pulse electrical stimulation treatments. These findings suggest that single-hole non-liposuction NIR endoscopy for SLNB in early-stage breast cancer patients is as safe and feasible as open surgery, with manageable complications.

At present, endoscopic techniques for SLNB in early breast cancer are mostly performed in the context of axillary liposuction [1‐5]. The anatomy of the axilla becomes clearer with liposuction, and stained lymph nodes, fluorescent lymph nodes, and radionuclide-labeled lymph nodes can be more visually displayed in the axilla, thus reducing the difficulty of SLNB and increasing its accuracy rate. However, liposuction increases trauma due to deep depression of the axilla, which affects the patient’s appearance, which some patients find difficult to accept. In addition, whether liposuction can cause tumor cell dissemination, especially for patients with potential axillary lymph node positives, is controversial [6, 7].

To avoid such controversy, this study explored the use of non-liposuction techniques for axillary SLNB. It is difficult to construct axillary cavities and accurately locate SLNs with minimal trauma without liposuction. To address this issue, we used high-frequency color ultrasound to locate and label axillary SLNs prior to surgery and a fluorescence vascular imager combined with a 4K high-definition near-infrared endoscopic method to further locate SLNs during surgery, with excellent results. The 4K HD NIR endoscope has both the white light mode of a conventional endoscope and the fluorescence mode of the endoscope itself. Therefore, the detection rate of SLNs can be improved by tracing pigments in combination with fluorescence double staining to detect both stained and fluorescent lymph nodes during SLNB operation.

In this study, we successfully detected SLNs within approximately 30 min in 30 patients in the Endoscopy group using the NIR endoscopic fluorescence method to accurately locate SLNs prior to surgery; this surgery was performed with a 100% success rate. A total of 121 SLNs were detected in the Endoscopic group (mean 4.89 ± 1.73), significantly exceeding the “no less than 3” requirement of the guidelines for reducing the false negativity rate [25, 26]. These findings were equivalent to those in the open group. The detection rates of fluorescent SLNs and stained SLNs did not differ between the endoscopic and open groups. However, it is interesting to note that there was a difference between the detection rates of fluorescent SLNs and stained SLNs within the endoscopic group. The reasons for investigating this are that the molecular diameter of the ICG is smaller than that of the CNS, which allows it to quickly penetrate smaller lymphatic vessels and expand to further lymph nodes. In addition, this finding indicates that 4K high-definition NIR endoscopy has superior fluorescence sensitivity, so much so that additional faint fluorescent lymph nodes can be found. Although the number of fluorescent SLNs was greater than the number of stained SLNs in the Endoscopy group, there was no difference in the pathological positivity rates between fluorescent SLNs and stained SLNs, indicating that it is safe to use either ICG fluorescence or CNS pigments as tracers in axillary SLNB.

Sixty-one patients were followed up for 1–24 months, and none were lost to follow-up. No local recurrences or distant metastases occurred during a mean follow-up period of 14.6 months. Similar to the findings of previous studies [27, 28], the oncology safety and reliability of the non-liposuction fluorescent endoscopic technique for axillary SLNB in early breast cancer was demonstrated.

This was a single-center, single-arm study; thus, the sample size was not large, and the follow-up time was not long. Additional shortcomings may also have affected the study results. We plan to continue to expand the sample size, reduce the bias, and obtain additional positive results.

In conclusion, based on our single-center results, single-hole non-liposuction NIR endoscopic axillary SLNB is not inferior to open SLNB and may be an appropriate option for patients with early-stage breast cancer who wish to undergo breast preservation with fewer incisions. It is recommended that this study be conducted at different centers, including more subjects.