Nonliposuction Endoscopic Sentinel Lymph Node Biopsy Through the Periareolar Incision

Abstract

Background. Sentinel lymph node biopsy (SLNB) has been an alternative to axillary lymph node dissection as a standard procedure for breast cancer patients with clinically negative lymph nodes. Endoscopic technique has been developed for over 20 years but remains to be mastered by a slice of surgeons. Suction and squeezing in the liposuction endoscopic procedures may increase risk of local recurrence and metastasis. In this study, we present our method of SLNB procedure through the periareolar incision which improves the shape of the breast-conserving surgery. Patients and Procedures. Twenty-eight breast cancer patients with clinically negative lymph nodes received this procedure. Methylene blue dye and technetium-99m sulfur colloid were used to be the tracker of sentinel lymph nodes (SLNs). Periareolar incision was the main surgical technique. The STORZ HD endoscopic system and some special instruments were used during the operation. Results. SLNs can be accurately located and biopsied under an endoscope without additional incisions. The SLNs detection rate, sensitivity, and false-negative rate are 88%, 80%, and 11.1%, respectively. And, the complications such as paresthesia and upper limb lymphedema are similar compared with traditional breast-conserving surgery (10.7% vs 9.8% and 7.1% vs 7.8%). Conclusion. Endoscopic technique can be used to accurately assess the status of SLNs in patients with breast cancer. Nonliposuction endoscopic breast-conserving surgery is one of the safe and alternative surgical procedures for early breast cancer.

Keywords

nonliposuction endoscopy sentinel lymph node biopsy axillary lymph node dissection

Introduction

As we all know, breast cancer has been the most serious malignant disease harming women’s health. In the past 100 years, surgery for breast cancer has been developed from local excision, extensive radical operation to modified radical mastectomy. Axillary lymph node status is an important indicator of breast cancer staging and prognosis. Many research studies supported that sentinel lymph node biopsy (SLNB) was accurate and safe to predict the outcomes of patients’ survival who can avoid axillary lymph node dissection (ALND) if the biopsy result was negative.^1-3 In the late 90s, SLNB became the standard process for breast cancer surgery to identify whether patients would receive ALND in Europe and America. And, the mainstream clinical practice guidelines for breast cancer were gradually emphasizing the importance of SLNB for breast surgery.^4,5 Nowadays SLNB has replaced routine ALND and become the standard surgical treatment for breast cancer. In China, methylene blue is one of the most commonly used sentinel node tracers in breast treatment centers because of its simple operation, low cost, and high labeling success rate. The sulfur colloid labeled with 99mTc has the advantages of high detection rate and low false-negative rate, which is recognized by many researchers. Niebling et al.⁶ studied the ability of different tracers to identify the SLN. The detection rates of methylene blue group, radionuclide group, methylene blue combined radionuclide group, and indocyanine green (ICG) group and ICG combined radionuclides group were 87.0%, 97.0%, 97.0%, 100.0%, and 96.0%, respectively, and the false-negative rates were 2.9%, 2.3%, 1.7%, 2.5%, and 3.3%, respectively. At present, the method of double tracer of nuclides combined with dyes is the preferred tracer method recommended by guidelines.^7,8 The trial of NSABP b-32 (ref. 9) indicated that the false-negative rate was 17.7% when 1 SLN was found, 10% when 2 SLNs were found, 6.9% when 3 SLNs were found, 5.5% when 4 SLNs were found, and 1% when 5 or more SLNs were found. To ensure the validity of the SLNB results, the dual tracer method (blue dye and radionuclide) is recommended to be used, and at least 3 SLNs should be detected at the same time.

The traditional process of SLNB needs to mark the SLNs by injecting blue dye or radioisotope preoperation in subcutaneous areola tissue or tumor surrounding; then, a small incision was made near the armpits. Finally, surgeons began to search for the lymphatic duct and lymph nodes and resect the stained targets. This procedure was mastered by many breast surgeons. For the purpose of reducing the traumas and increasing the satisfactory appearance after the operation, many well-skilled surgeons have developed some innovation tactics on this therapeutic method. Some surgeons may finish this process with only a 2 cm length of incision next to the armpits. Some others also developed endoscopy-assisted breast surgery to improve appearance.^10-12 Lipolytic endoscopic surgery may be suitable for this purpose which emphasis prior liposuction and then resect the lymph nodes to pathological examination.¹³ This method remains argument for its potential increasing risk of disease’s recurrence, although there are some reviews indicate that it would not increase risk of disease free survival and overall survival (OS) for breast cancer patients.¹⁴ But the fact is that the outcomes are not exhibiting its better appearance with small scar on lower armpits. And the key-point is that the breast has no cavity and is full of fat and glands, for which limited endoscopic technique is used clinically. Many breast surgeons have not mastered this technique. So rarely can reports be seen in the breast surgical field.

In our study, we try to develop a new method to achieve SLNB. Neither additional incisions on the armpits nor liposuction on the breast was made during the operation. Methylene blue dye and radionuclide were the sentinel lymph node (SLN) tracers in our department. Some experience is summarized and shared here.

Patients and Procedures

Patients with upper outer quadrant tumors were the candidates to this surgery. We finally chose 28 patients to receive this surgical technique (Table 1). The age range of patients was 27 to 58 years with an average of 43.39 ± 6.92 years. The tumor size ranged from .8 cm to 4 cm diameter with average 2.0 ± .77 cm. All patients were diagnosed with malignant tumor disease by core needle biopsy with the punctures located on the periareolar incisions. Preopeative ultrasound assessment of axillary lymph nodes was made to identify the result that the axillary lymph nodes (ALNs) were clinically negative in all 28 patients. Other assessments such as blood routine, blood biochemistry, coagulation function, electrocardiogram, and chest and abdomen CT scans were accomplished before the surgery. All patients were told and understood well the risk of the operation and may receive ALND if SLNB was unsuccessfully practiced. And they all agree to receive this therapeutic method.

SLNs were stained by 2 kinds of dyes. One was blue dye and the other was radiolabeled sulfur colloid dye. First, all the patients were diagnosed with breast cancer by core needle biopsy (Figure 1A). The day before surgery, a sulfur colloid was injected subcutaneously around the tumor to mark the SLNs (Figure 1B). A radionuclide scan was then performed to determine the location of the sentinel nodes. Methylene blue was injected subcutaneously around the tumor 10 minutes before the operation began to ensure that the SLNs could be stained for visual recognition during the operation. Radionuclide probes are used to identify labeled SLN signals before surgery begins (Figure 1C). A circular areola incision was made, and the tumor in the outer upper quadrant of the breast was completely removed (Figure 1D). The SLNs were then excised along the lumen with the assistance of the endoscopic system. The removed SLN was again identified with a radionuclide probe and sent for pathology (Figure 1E).

Table 1.

Patient and Tumor Characteristics.

Parameter	Endoscopic BCS (n = 28)		Traditional BCS (n = 51)
Parameter	No.	%	No.	%
Age (years)
Mean	43.39 ± 6.92		48.46 ± 9.21
Range	27-58		23-65
Tumor size (cm)
Mean	2.02 ± .77		2.51 ± .63
Range	.8-4		.5-4.6
T-stage
T1	15	53.6	31	60.8
T2	13	46.4	19	37.2
N-stage
N0	19	67.9	33	64.7
N+	13	46.4	18	35.3
Quadrant
Upper outer	28	100	27	52.9
Upper inter	0		6	11.8
Lower outer	0	0	11	21.6
Lower inter	0		7	13.7
Areolar	0		0
Histological type
Invasive breast cancer	24		46
Mucinous breast cancer	1
Ductal carcinoma in situ	3		5
Estrogen receptor status
Positive	19	67.6	32	62.7
Negative	9	32.4	19	37.3
Progesterone receptor status
Positive	19	67.6	31	60.8
Negative	9	32.4	20	39.2
Human epidermal growth factor receptor-2 status
Positive	5	17.9	13	25.5
Negative	23	82.1	38	74.5
Clinical stages
TisN0M0	3		5
T1N0M0	9	32.1	22	43.1
T1N_minM0	2		1
T1N1M0	2		4
T1N2M0	0		1
T2N0M0	5	17.9	6	11.8
T2N1M0	6	21.4	9	17.6
T2N2M0	1		3

Abbreviation: BCS = breast-conserving surgery.

Figure 1.

(A) Pathological biopsy by a hollow needle. (B) Radionuclide tracer was injected to stain the sentinel lymph nodes. (C) Nuclide signals were detected by probe preoperation. (D) Methylene blue tracer was injected and the tumor was removed through the periareolar incision. (E) Process of sentinel lymph node biopsy under endoscopy.

The specific surgical procedures are as follows.

Staining with radiolabeled sulfur colloid was done 16 hours before the surgery. 1 mL technetium-99 m sulfur colloid (1 mCi [37 MBq]) was injected into the breast around the tumor and subcutaneous areola tissue. Then, 2 hours after the injection, patients were sent to receive emission computer tomography examination to locate the labeled sites (Figure 2A).

The patients were placed in a supine position with the ipsilateral arm at 90° abduction. Surgical instruments such as ultrasonic scalpel, cautery hooks, disposable trocars, and hemostatic forceps were prepared. Then, patients received general anesthesia to begin the operation.

After general anesthesia, radionuclide probes were used to detect surface marking signals in SLNs (Figure 2B). And the patient received lumpectomy through periareolar incision, and the margin was identified as pathological negative during the operation. Then, we began the next endoscopic step.

In this step, we used the endoscopic operating system (STORZ HD Xenon Nova 300 System) as the main instrument. Before the endoscopy was taken into practice, 2 trocars (10 mm one and 5 mm the other) were placed in the cavity through the periareolar incision. The wound between the 2 trocars was sewed up to ensure that CO₂ gas would not leak out. The third trocar was placed in the cavity through the other .5-cm incision located on the anterior axillary line. A 30° 10-mm endoscope was inserted through the 10-mm trocar. CO₂ gas was infused into the cavity to about 6–8 mm Hg pressure (Figure 2C).

Searching for SLNs: 10 minutes after the labeled dye was injected in the right position, we began to separate subcutaneous tissue along the pectoralis muscle to the axillary direction. SLNs are often located outside the margin of the pectoralis minor muscle superficial layer of fascia coracocleidopectoralis. In this step, we use a nuclide probe to detect the signal in the cavity (Figure 2D). The location of the sentinel node is identified, and blue-stained sentinel nodes can be found (Figures 3A and 4D). The lymph nodes were confirmed and sent for pathology examination (Figure 3B).

Patients with pathologically positive SLNs would receive ALND (Figure 4B). And if the pathological report indicates that a patient has no SLN metastasis, then the surgery will end.

Tissues were removed by a specimen bag and taken out through the areola incision (Figure 4A). After washing with distilled water, the wound was closed and incision sewed up, with the anterior axillary line incision placed with a drainage tube (Figure 4C).

Figure 2.

(A) Sentinel lymph nodes were shown on the emission computer tomography image. (B) Nuclide signals were detected before surgery. (C) Incision path of endoscopic surgery. (D) Nuclide signals were detected to verify the right direction by a probe under endoscopy.

Figure 3.

(A) Sentinel lymph node stained by blue dye was separated out under endoscopy. (B) Separated out tissue was detected by a nuclide probe. (C) Incisions at 3 months after endoscopic surgery. (D) Appearance 3 months after endoscopic surgery.

Figure 4.

(A) Excised tissue was removed with a specimen under endoscopy. (B) Important structures such as axillary vein, long thoracic nerve, thoracodorsal vessel, and nerve were preserved after endoscopic axillary lymph node dissection. (C) Drainage tube was placed through the anterior axillary line incision, and the periareolar incision was sewed up. (D) Sentinel lymph node stained by blue dye was separated out under endoscopy.

Results

A total of 28 cases were treated with endoscopic-assisted breast-conserving surgery (BCS) in our department during 2016.01–2018.12 (Table 1). The mean age was 43.39 ± 6.92 years. The largest tumor was 4 cm, the smallest was .8 cm, and the average was 2.02 ± .77 cm. In all cases, the tumors were in the outer upper breast quadrant. Among them, there were 15 patients with the pathological stage T1 and 13 patients with T2. Breast ultrasound, mammography, and breast MRI showed no signs of axillary lymph node metastasis. In the control group, we included a total of 51 cases of traditional breast-conserving surgery (TBCS) in our department under similar conditions during the same period. In the endoscopic breast-conserving surgery (EBCS) group, all the tumors were located in the upper outer quadrant. Among the postoperative pathology, there were 24 cases of invasive carcinoma, 1 case of mucinous carcinoma, 3 cases of ductal carcinoma in situ, 19 lymph node–negative cases, and 13 lymph node–positive cases. The total number of patients with clinical stage T_1-2N_0-1M₀ was 71.4%, and the control group was 72.5%. The postoperative pathology is shown in Table 1.

The statistical results in Tables 2 and 3 show that a total of 25 patients underwent SLNB at an average operative time of 29.56 ± 5.82 minutes in the endoscopic group, while the other 7 patients (including 3 patients with SLNs unknown and 1 patient ALN positive) received only ALND, with the mean operating time of 54.08 ± 6.76 minutes. In the endoscopic group, there were 22 patients with SLNs detected; the detection rate was 88% (22/25), with an average of 3.56. Of the 22 patients detected, 4 had positive SLNs and 17 negative. SLNs and ALNs were all positive in 4 cases. One of the 3 patients with no SLNs detected had pathology-confirmed positive ALNs. One patient was diagnosed SLN negative but ALN positive. The success rate of SLN detection was 88% (22/25), the sensitivity rate was 80% (4/5), and the false-negative rate was 11.1% (1/9). The mean drainage volume after SLNB and ALND was 60.35 ± 7.36 mL and 165.42 ± 25.45 mL, respectively, and the mean time drainage was placed was 6.16 days. The operation time of the traditional BCS group was shorter than that of the endoscopic group, while the SLN detection rate and sensitivity rate were higher (98% vs 88% and 88.9% vs 80%). And, the false-negative rate was lower (5.6% vs 11.1%). The mean time of SLNB and ALND was 14.81 ± 3.21 minutes and 32.62 ± 4.63 minutes, respectively. There was less drawing fluid for SLNB (43.65 ± 5.62 mL) and more drawing fluid for ALND (182.65 ± 20.63 mL). All patients underwent systemic review every 3 months after surgery, and the median follow-up time was 25.18 ± 9.76 months. In the statistics of postoperative complications, 3 patients in the endoscopic group had paresthesia in the upper limb and 2 patients had lymphedema, while 5 patients in the traditional group had paresthesia in the upper limb, 3 patients had subcutaneous effusion in the wound, 4 patients had lymphedema, and 2 patients had wound flap necrosis. The median follow-up time after surgery was 25.18 + 9.76 months in the EBCS group and 26.6 + 8.6 months in the TBCS group. In the EBCS group, 1 patient had chest wall tumor recurrence and 1 patient had regional lymph node metastasis. In the TBCS group, there were 2 patients with chest wall recurrence, 2 patients with regional lymph node metastasis, and 1 patient with distant metastasis. The progression-free survival rate was 92.9% and 90.2%, respectively, and the OS rate of the 2 groups was 100%.

Table 2.

Clinical Results.

Clinical Result	Endoscopic BCS (n = 28)		Traditional BCS (n = 51)
Clinical Result	No.	%	No.	%
SLNB alone	17		33
ALND	7
SLNB and ALND		28.6		35.3
SLN(+) and ALND	4		16
SLN(unknown) and ALND	3		1
SLN(−) and ALND(+)	1		1
SLN detection rate		88.0		98.0
SLN sensitivity		80		88.9
SLN false-negative rate		11.1		5.6
Operative time (minutes)
Average operation time of ALND	54.08 ± 6.76		32.62 ± 4.63
Drainage flow of ALND	165.42 ± 25.45		182.65 ± 20.63
Volume of drainage (mL)
Drainage flow of SLNB	60.35 ± 7.36		43.65 ± 5.62
Drainage flow of ALND	165.42 ± 25.45		182.65 ± 20.63
Average duration of drainage (days)	6.16 ± 1.61	4.38 ± 2.32
Complication
Paresthesia (pain and numbness)	3	10.7	5	9.8
Wound effusion	0		3	5.9
Upper limb lymphedema	2	7.1	4	7.8
Flap necrosis	0		2	3.9
Shoulder joint movement disorder	0		0
Lymph node number (mean)
Average of SLNs from patients	3.56 ± .65		3.54 ± .36
Average of ALNs from patients	17.35 ± 2.54		18.66 ± 4.34

Abbreviations: BCS = breast-conserving surgery; SLNB = sentinel lymph node biopsy; ALND = axillary lymph node dissection; SLN = sentinel lymph node; ALN = axillary lymph node.

Table 3.

Prognosis.

Prognosis	Endoscopic BCS (n = 28)		Traditional BCS (n = 51)
Prognosis	No.	%	No.	%	P
Follow-up time (months)
Period	2016.01-2018.12		2016.01-2018.12
Median follow-up time	25.18 ± 9.76		26.6 ± 8.6 m
Progression-free survival	26	92.9	46	90.2	<.05
Chest wall recurrence	1	3.6	2	3.9
Regional lymph node metastasis	1	3.6	2	3.9
Distant metastasis	0		1	2.0
Overall survival	28	100	51	100	<.05

Abbreviation: BCS = breast-conserving surgery.

Figures 3C and 3D present the appearance of the breast at 3 months after surgery. The patient received endoscopic SLNB and ALND in our department. The postoperative clinical pathological stage was T1N1M0 II A, and the patient was receiving chemotherapy in our hospital when the photo was taken.

Discussion

With the continuous progress of modern medical technology, the biological behavior of breast cancer has received more and more in-depth understanding. Surgery is still the first choice for the treatment of early breast cancer, but the scope of surgery is moving toward minimally invasive and better cosmetic preservation on the premise of treatment effect. In the past 20 years, many research studies have confirmed that SLNB is accurate and safe to predict whether breast cancer patients can avoid ALND which would bring favorable outcomes and more function protections.^1,2,15-17 And, SLNB has been the standard process of breast cancer surgery recommended by some main guidelines.^4,5

The choice of SLN tracer. The methylene blue we use is a SLN tracer commonly used in major breast centers in China. The advantage is that it has good visibility. The disadvantage is that the target line is poor and the secondary lymph nodes are easily stained to affect the accuracy of the results.¹⁸ The radionuclide tracer has the advantages of high detection rate and low false-negative rate. The disadvantage is that it needs radiation protection during storage and use. The combination of the 2 methods for dual tracing is the preferred tracing method recommended by guidelines.^19,20 In practice, we could accurately determine the location of the marked SLNs by detecting the radionuclide labeling signal. Under the endoscopic field, we could accurately dissect and isolate the blue-stained lymph nodes. After taking out the specimen tissue, it was further verified by detecting the radionuclide signal. Through the above methods, the difficulty of endoscopic SLNB was reduced, and the accuracy of the results was improved. Other commonly used SLN tracers are ICG and superparamagnetic tracers. ICG requires the near-infrared light source of the fluorescent vascular imaging system to be excited in real time, and the imaging device is used to observe the subcutaneous lymphatic drainage pathway to mark the SLN.²¹ Superparamagnetic iron oxide is represented by mononuclear macrophages in the lymphatic system. Through the action of an external magnetic field, iron oxide produces magnetism to achieve its tracking effect. And, the superparamagnetic tracer is a brown liquid, which can stain the lymphatic vessels and SLNs and make the SLNs visible. During the operation, the SLNB is guided by the strength of the sound emitted by the magnetometer.²² The lack of an endoscopic near-infrared camera and special magnetometer limits our practical application of these methods. And its safety, reliability, and effectiveness need to be proved by further practice.

Endoscopic techniques have been used in the breast surgical field for over 20 years. Kompatscher first reported endoscopy-assisted breast contracture implant removal in 1992.²³ Endoscopy was reported to be used in other breast surgical fields since then.^24-26 ALND used to be a recommendation for breast cancer surgery 20 years ago. Since endoscopic ALND was first reported in 1996,²⁷ surgeons have developed some techniques to achieve this process, which can be divided into 2 categories: with prior liposuction^3,28-30 and nonliposuction methods.^31-34 Many scholars are concerned that intraoperative compression of tissue has the potential risk of tumor spread, although some retrospective studies supported the liposuction method would lead to safe outcomes. At present, several studies support the outcomes of endoscopic breast surgery as safe, with minor morbidity and good functional and cosmetic results.^{13,14,33,35-37} Nonliposuction endoscopy has its shortcomings that the abundant fat and glands would increase the difficulty and duration of the operation. So, axillary incision remains the most common incision in breast cancer surgery. SLNB is difficult to achieve under endoscopy. And, some surgeons accomplish this by taking an axillary incision as an operation field and do more procedures.^10,11,38 In some patients with tumors in the outer upper quadrant of the breast, with the guidance of appropriate sentinel node tracers, we found that endoscopic SLNB and ALND could be performed accurately and effectively under the cavity produced by the excision of the tumor. This procedure does not require an additional incision in the axilla. For patients with tumors in other quadrant of the breast, this procedure may also be feasible by redesigning the incision and creating another surgical cavity. However, that will undoubtedly increase the difficulty of operation, and more endoscopic experience is required.

Periareolar incision is one of the most common incisions in breast surgery, which has obvious advantages such as the removal of almost all the breast glands, concealment of the incision, less postoperative scar, and good postoperative appearance. In our department, we found through practice that, with the assistance of endoscopy, BCS can be performed through the areolar incision. The scars are unobvious. But the statistical results show that the detection rate and sensitivity of SLNs in the endoscopic group are lower than those in the traditional group, and the operation time is longer. The reasons may be summarized as follows. (1) The accumulated number of cases was small. (2) In the initial 10 cases, 2 cases were failed to performance because of the chaos of the surgical field due to improper injection of methylene blue. And in 1 case, we failed to accurately locate the SLNs due to the weak radionuclide signal. (3) As a new surgical method, we lacked endoscopic operation experience, and it is necessary to complete the learning curve. In open surgery, learning curves for SLNB have been described for 22 cases as a suitable number to reach 10% failure rate.³⁹ But in endoscopic technique, these data remain inadequate. During the operation, we found that some patients had only 1 or 2 SLNs, with scattered unmarked lymph nodes around. To improve the accuracy of the diagnosis, these lymph nodes were also removed for pathological examination to ensure that the number of SLNs in each case was ≥3. And the research results of some scholars also support our approach.⁴⁰ In order to ensure standardization of the treatment effect, axillary dissection was performed in patients whose pathologic findings indicated at least 1 SLN as positive. Through the follow-up of all cases after surgery, we found that the recurrence and metastasis rates of patients in the EBCS group were not significantly different from those in the traditional BCS group, and the 2 groups showed no difference in disease-free survival (92.9% vs 90.2%) and OS (all 100%). However, more data are needed to verify the safety and reliability of the technique and its impact on long-term survival.

At present, the survival period of breast cancer patients are constantly extended after comprehensive treatment. Many of them need not only to be treated for their disease but also to be beautiful, sexy, and have a high quality of life. And endoscopic technique may benefit some of them.

Conclusion

Endoscopic technique can be used to accurately assess the status of SLNs in patients with breast cancer. Nonliposuction EBCS is one of the safe and alternative surgical procedures for early breast cancer.

Footnotes

Acknowledgments

We would like to express our sincere thanks to all those who have lent us hands in the course of writing this paper. First is Dr Xu Shuangta: he provided all the case data and snapshots in this paper. Second is our team: in the past 4 years, we worked together and overcame all the difficulties. Also, thanks to their offering of references and information on time. Last but not the least, we would like to thank our patients for their sincere trust.

Author Contributions

Study concept and design: Shuangta Xu

Acquisition of data: Yinghui Liang

Analysis and interpretation: Yinghui Liang

Study supervision: Yinghui Liang and Shuangta Xu

Declaration of Conflicting Interests

The author(s) declared no potential conflicts of interest with respect to the research, authorship, and/or publication of this article.

Funding

The author(s) received no financial support for the research, authorship, and/or publication of this article.

ORCID iD

Yinghui Liang

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