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Comparison of Classic and Endoscopic Lymphadenectomy for Staging Breast Cancer
February 2003, Vol. 10, No. 1
The Journal of the American Association of Gynecologic Laparoscopists
Comparison of Classic and Endoscopic Lymphadenectomy for Staging Breast Cancer R. L. de Wilde, M.D., Ph.D., E. H. Schmidt, M.D., Ph.D., M. Hesseling, M.D., R. Mildner, M.D., V. Frank, M.D., and M. Tenger, M.D.
Abstract Study Objective. To compare endoscopic and classic axillary lymphadenectomy staging of breast cancer with respect to operation-induced changes such as seroma formation, pain, neurologic sensations, lymphedema, infection, and reduction of shoulder-arm mobility. Design. Prospective, randomized study (Canadian Task Force classification I). Setting. University-affiliated hospital. Patients. Eighty consecutive women with histopathologically confirmed invasive breast cancer who had clinically and sonographically negative axillary lymph nodes (<1 cm). Intervention. Classic and endoscopic lymphadenectomies. Measurements and Main Results. We attempted to obtain 10 axillary lymph nodes/patient. After 1, 3, 5, 7, 9, 42, and 84 days, clinical and ultrasonographic examinations were conducted to evaluate operation-induced changes. Short-term results showed that, with endoscopic technique, a representative number of axillary lymph nodes was removed, with reduced axillary infiltration and seroma induction, as well as less impaired shoulder-arm mobility. During the first month, postoperative infection, lymphedema, and neurologic complaints were comparable in both groups, with more stretching pain in the classic group and predominantly paresthesia in the endoscopic group. After 3 months no differences in postoperative complications were detected. Conclusion. Endoscopic axillary lymphadenectomy avoids short-term reduction of shoulder-arm mobility. Longterm studies are necessary to prove if this technique is as safe as the classic procedure with regard to local axillary recurrence. If so, endoscopy could become the method of choice for staging breast cancer in women with clinically negative lymph nodes. (J Am Assoc Gynecol Laparosc 10(1):75–79, 2003)
of axillary lymph nodes is gaining attention as a less invasive technique, raising the question as to whether it could become a real alternative.
Breast cancer affects 1 in 10 women in the Western hemisphere. Surgical treatment of choice is lumpectomy or mastectomy, depending on various factors, such as tumor size, multifocality, and patient age. Whichever technique is performed, axillary lymphadenectomy is mandatory for staging and thus for determining further therapy. Classic lymphadenectomy was the method of choice for staging. After this procedure, however, 80% of women have at least one postoperative complication in the arms (swelling, paresthesia, reduced mobility).1 Endoscopic removal
Materials and Methods We compared endoscopic and conventional lymph node dissection in 80 women with primary breast cancer to determine advantages and limitations of both procedures especially with regard to postoperative changes. Inclusion criteria were histopathologic
From the Department of Obstetrics and Gynecology, Pius-Clinic, Oldenburg, Germany (all authors). Address reprint requests to R. L. de Wilde, M.D., Department of Obstetrics and Gynecology, Pius-Clinic, Georgstr. 12, D - 26121 Oldenburg, Germany; fax 49 441 229 1525. Accepted for publication July 8, 2002. Reprinted from the JOURNAL OF THE AMERICAN ASSOCIATION OF GYNECOLOGIC LAPAROSCOPISTS, February 2003, Vol. 10 No. 1 © 2003 The American Association of Gynecologic Laparoscopists. All rights reserved. This work may not be reproduced in any form or by any means without written permission from the AAGL. This includes but is not limited to, the posting of electronic files on the Internet, transferring electronic files to other persons, distributing printed output, and photocopying. To order multiple reprints of an individual article or request authorization to make photocopies, please contact the AAGL.
75
Comparison of Classic and Endoscopic Lymphadenectomy to Stage Breast Cancer de Wilde et al
confirmation as well as negative clinical and sonographic lymph node status (<1 cm). Consecutive patients were randomized into one of two groups in order of enrollment. Women in group A (mean age 64.9 yrs, range 41–92 yrs) underwent conventional lymph node dissection.2 Those in group B (mean age 58.4 yrs, range 35–79 yrs) had endoscopic lymph node removal.3 Patients in both groups were comparable regarding tumor stage. The goal was to collect 10 lymph nodes for staging purposes. Women in both groups were examined 1, 3, 5, 7, 9, 42, and 84 days after lymph node dissection to determine and compare short-term side effects, with special attention to seroma development, arm-shoulder mobility, pain, neurologic complications, lymphedema, and wound infections. Women had clinical and ultrasound assessments, all done by the same investigator who was not the surgeon.
Results
Operative Techniques Two methods of endoscopic lymphadenectomy are with liposuction3 and without liposuction. Both methods offer a complete view of axillary anatomy, making meticulous removal of lymph nodes possible. The basic axilloscopy set includes a video unit, xenon light source, insufflation unit, zero-degree endoscope, 11-mm cannula, two 6-mm cannulas, grasping forceps, monopolar scissors, bipolar forceps, and Karmann curette for liposuction. The patient was positioned on the operating table with head slightly elevated. The ipsilateral arm was bent at 90 degrees. First, the axilla was infiltrated with 400 ml of a hypotonic solution (200 ml 0.9% NaCl, 200 ml aqua dest., 40 ml 1% Xylocaine, 1 ml Suprarenin). After about 20 minutes lipolysis was complete. Liposuction was performed with an 0.8-mm bar through the lower axillary pole for less than 1 minute to gain access to axillary structures. After liposuction the 11-mm cannula was inserted into the axillary cavity. The cavity was inflated with carbon dioxide (CO2) at a maximum pressure of 8 mm Hg. After insufflation the endoscope was inserted. Under view, two 6-mm cannulas were inserted into the axilla laterally. Despite blind liposuction, there was no bleeding. The rest of the connective tissue was coagulated and transsected, thus presenting the insufflated axillary space to allow identification and preparation of nerves, arteries, and veins, and monobloc extirpation of lymph nodes.
Stagea
Operating time was 36 minutes (range 19–66 min) in group A and 62 minutes (range 42–126 min) in group B. Operating time after 50 patients (learning curve) was 36 minutes (range 24–85 min)/10 extirpated nodes starting with insertion of the optic and ending with skin closure. Analysis of tumor stage in both groups showed comparable results (Table 1). In group A the mean number of collected lymph nodes from levels 1 and 2 was 12 (range 1–22). In group B the number was 11 (4–21). On three-dimensional sonographic check-up, 37 (92%) of 40 women in group A had seroma induction TABLE 1. Comparison of Stages Group A
pTis pT1 + pT2 pT3 pT4 pN0 pN1 pN2 pM ovar/M oss M oss/hep. pM1 axill. soft tissue M0 Total metastases
Group B
No.
%
No.
%
5/40 33/88 0/40 2/40 27/40 13/40 0/40 1/40 1/40 1/40 37/40 13/40
12 41 0 5 68 32 0 2 2 2 92 32
7/40 32/80 0/40 1/40 30/40 10/40 0/40 0/40 0/40 0/40 40/40 10/40
17 40 0 2 75 25 0 0 0 0 100 25
aStaging by UICC classification: pTis = carcinoma in situ as
staged by histopathology; pT1 = tumor smaller than 2 cm as staged by histopathology; pT2 = tumor between 2 and 5 cm as staged by histopathology; pT3 = tumor more than 5 cm in diameter as staged by histopathology; pT4 = tumor infiltrating skin and/or thorax muscle; pN0 = no metastases in the lymph nodes as staged by histopathology; pN1 = homolateral mestastases in the axillary lymph nodes as staged by histopathology; pN2 = several metastases in the lymph nodes form an axillary tumor as staged by histopathology; pMovar = metastases in the ovaries as staged by histopathology; pMos = metastases in the bones staged by clinical and radiological investigations; Mhep = metastases in the liver as staged by ultrasonography or radiology; pM1 = axill. soft tissue metastases in the axilla but not in the lymph nodes; M0 = no metastases can be found by clinical and/or radiological investigations
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February 2003, Vol. 10, No. 1
The Journal of the American Association of Gynecologic Laparoscopists
in the axilla, with mean volume of 8.7 ml (range 0.6–122 ml). In group B, seroma was seen in 90% of patients, with mean volume of 6.4 ml (range 0.1–120 ml; Figure 1). Measurements of shoulder-arm mobilty started at 90-degree abduction and elevation, with 180-degree
elevation representing 100% (Figure 2). Short-term checks showed less limitation of mobility in group B. After approximately 3 months mobility in both groups was no longer significantly different. Postoperative pain mapping showed that more women in group A than in group B complained of pain
FIGURE 1. Seroma induction after classic and endosurgical lymphadenectomy.
FIGURE 2. Postoperative shoulder-arm mobility after classic and endosurgical lymphadenectomy (p <0.05, χ2 test).
77
Comparison of Classic and Endoscopic Lymphadenectomy to Stage Breast Cancer de Wilde et al
in the shoulder-arm region (Figure 3). Paresthesia, also measured by mapping, was predominantly found in group B compared with group A (Figure 4). Nine cases of lymphedema (≥1 cm difference in arm circumference) were found in group A (22%),
and eight (20%) in group B. In both groups the condition was mild (<2 cm arm diameter) and the difference was not statistically significant. Wound infections without elevated body temperature but with pain, erythema, and swelling were seen
FIGURE 3. Postoperative pain after classic and endosurgical lymphadenectomy (p <0.01, Fisher’s test).
FIGURE 4. Paresthesia in the shoulder-arm region after classic and endosurgical lymphadenectomy (p <0.01, Fisher’s test).
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February 2003, Vol. 10, No. 1
The Journal of the American Association of Gynecologic Laparoscopists
operative pain during the first 3 months. Long-term studies must determine if the technique has the same safety with respect to local axillary recurrence. If so, it could become the method of choice for staging in breast cancer in women with clinically negative lymph nodes. Studies are under way to evaluate the possibility of endoscopic techniques for sentinel lymphadenectomy in breast cancer.4
in four patients (10%) in group A and two (5%) in group B. All six women were treated with antibiotics and none required surgical reintervention. Due to current regulations in the German health system in which medical insurance companies pay fixed fees for operative procedures involving breast cancer, there was no difference in hospital charges. Discussion
References
In this comparison of endoscopic and conventional axillary lymphadenectomy we found differences in short-term side effects possibly due to better preservation of fine axillary structures by the former method. The endoscopic technique caused less shoulder stiffness. Neurologic complaints such as paresthesia were more common in group B, however, but more shoulder-arm pain was seen in group A. These side effects were documented within the first 6 postoperative weeks. After 3 months there were no differences in side effects between groups. We conclude that, compared with classic lymphadenectomy, endoscopic axillary dissection improves postoperative shoulder-arm mobility and reduces post-
1. Hladiuk M, Hutchcroft S, Temple W, et al: Arm function after axillary dissection for breast cancer. J Surg Oncol 50:47–52, 1992 2. Nemoto T, Vana J, Bedwani RN, et al: Management and survival of female breast cancer. Cancer 45:2917–2924, 1980 3. Suzanne F, Emering C, Wattiez A, et al: Le curage axillaire par lipo-aspiration et prelevement endoscopique. Chirurgie 122:138–143, 1997 4. Veronesi U, Paganelli G, Galimberti V, et al: Sentinel node biopsy to avoid axillary dissection in breast cancer with clinically negative lymph nodes. Lancet 349: 1864–1867, 1997
79
The Journal of the American Association of Gynecologic Laparoscopists
Comparison of Classic and Endoscopic Lymphadenectomy for Staging Breast Cancer R. L. de Wilde, M.D., Ph.D., E. H. Schmidt, M.D., Ph.D., M. Hesseling, M.D., R. Mildner, M.D., V. Frank, M.D., and M. Tenger, M.D.
Abstract Study Objective. To compare endoscopic and classic axillary lymphadenectomy staging of breast cancer with respect to operation-induced changes such as seroma formation, pain, neurologic sensations, lymphedema, infection, and reduction of shoulder-arm mobility. Design. Prospective, randomized study (Canadian Task Force classification I). Setting. University-affiliated hospital. Patients. Eighty consecutive women with histopathologically confirmed invasive breast cancer who had clinically and sonographically negative axillary lymph nodes (<1 cm). Intervention. Classic and endoscopic lymphadenectomies. Measurements and Main Results. We attempted to obtain 10 axillary lymph nodes/patient. After 1, 3, 5, 7, 9, 42, and 84 days, clinical and ultrasonographic examinations were conducted to evaluate operation-induced changes. Short-term results showed that, with endoscopic technique, a representative number of axillary lymph nodes was removed, with reduced axillary infiltration and seroma induction, as well as less impaired shoulder-arm mobility. During the first month, postoperative infection, lymphedema, and neurologic complaints were comparable in both groups, with more stretching pain in the classic group and predominantly paresthesia in the endoscopic group. After 3 months no differences in postoperative complications were detected. Conclusion. Endoscopic axillary lymphadenectomy avoids short-term reduction of shoulder-arm mobility. Longterm studies are necessary to prove if this technique is as safe as the classic procedure with regard to local axillary recurrence. If so, endoscopy could become the method of choice for staging breast cancer in women with clinically negative lymph nodes. (J Am Assoc Gynecol Laparosc 10(1):75–79, 2003)
of axillary lymph nodes is gaining attention as a less invasive technique, raising the question as to whether it could become a real alternative.
Breast cancer affects 1 in 10 women in the Western hemisphere. Surgical treatment of choice is lumpectomy or mastectomy, depending on various factors, such as tumor size, multifocality, and patient age. Whichever technique is performed, axillary lymphadenectomy is mandatory for staging and thus for determining further therapy. Classic lymphadenectomy was the method of choice for staging. After this procedure, however, 80% of women have at least one postoperative complication in the arms (swelling, paresthesia, reduced mobility).1 Endoscopic removal
Materials and Methods We compared endoscopic and conventional lymph node dissection in 80 women with primary breast cancer to determine advantages and limitations of both procedures especially with regard to postoperative changes. Inclusion criteria were histopathologic
From the Department of Obstetrics and Gynecology, Pius-Clinic, Oldenburg, Germany (all authors). Address reprint requests to R. L. de Wilde, M.D., Department of Obstetrics and Gynecology, Pius-Clinic, Georgstr. 12, D - 26121 Oldenburg, Germany; fax 49 441 229 1525. Accepted for publication July 8, 2002. Reprinted from the JOURNAL OF THE AMERICAN ASSOCIATION OF GYNECOLOGIC LAPAROSCOPISTS, February 2003, Vol. 10 No. 1 © 2003 The American Association of Gynecologic Laparoscopists. All rights reserved. This work may not be reproduced in any form or by any means without written permission from the AAGL. This includes but is not limited to, the posting of electronic files on the Internet, transferring electronic files to other persons, distributing printed output, and photocopying. To order multiple reprints of an individual article or request authorization to make photocopies, please contact the AAGL.
75
Comparison of Classic and Endoscopic Lymphadenectomy to Stage Breast Cancer de Wilde et al
confirmation as well as negative clinical and sonographic lymph node status (<1 cm). Consecutive patients were randomized into one of two groups in order of enrollment. Women in group A (mean age 64.9 yrs, range 41–92 yrs) underwent conventional lymph node dissection.2 Those in group B (mean age 58.4 yrs, range 35–79 yrs) had endoscopic lymph node removal.3 Patients in both groups were comparable regarding tumor stage. The goal was to collect 10 lymph nodes for staging purposes. Women in both groups were examined 1, 3, 5, 7, 9, 42, and 84 days after lymph node dissection to determine and compare short-term side effects, with special attention to seroma development, arm-shoulder mobility, pain, neurologic complications, lymphedema, and wound infections. Women had clinical and ultrasound assessments, all done by the same investigator who was not the surgeon.
Results
Operative Techniques Two methods of endoscopic lymphadenectomy are with liposuction3 and without liposuction. Both methods offer a complete view of axillary anatomy, making meticulous removal of lymph nodes possible. The basic axilloscopy set includes a video unit, xenon light source, insufflation unit, zero-degree endoscope, 11-mm cannula, two 6-mm cannulas, grasping forceps, monopolar scissors, bipolar forceps, and Karmann curette for liposuction. The patient was positioned on the operating table with head slightly elevated. The ipsilateral arm was bent at 90 degrees. First, the axilla was infiltrated with 400 ml of a hypotonic solution (200 ml 0.9% NaCl, 200 ml aqua dest., 40 ml 1% Xylocaine, 1 ml Suprarenin). After about 20 minutes lipolysis was complete. Liposuction was performed with an 0.8-mm bar through the lower axillary pole for less than 1 minute to gain access to axillary structures. After liposuction the 11-mm cannula was inserted into the axillary cavity. The cavity was inflated with carbon dioxide (CO2) at a maximum pressure of 8 mm Hg. After insufflation the endoscope was inserted. Under view, two 6-mm cannulas were inserted into the axilla laterally. Despite blind liposuction, there was no bleeding. The rest of the connective tissue was coagulated and transsected, thus presenting the insufflated axillary space to allow identification and preparation of nerves, arteries, and veins, and monobloc extirpation of lymph nodes.
Stagea
Operating time was 36 minutes (range 19–66 min) in group A and 62 minutes (range 42–126 min) in group B. Operating time after 50 patients (learning curve) was 36 minutes (range 24–85 min)/10 extirpated nodes starting with insertion of the optic and ending with skin closure. Analysis of tumor stage in both groups showed comparable results (Table 1). In group A the mean number of collected lymph nodes from levels 1 and 2 was 12 (range 1–22). In group B the number was 11 (4–21). On three-dimensional sonographic check-up, 37 (92%) of 40 women in group A had seroma induction TABLE 1. Comparison of Stages Group A
pTis pT1 + pT2 pT3 pT4 pN0 pN1 pN2 pM ovar/M oss M oss/hep. pM1 axill. soft tissue M0 Total metastases
Group B
No.
%
No.
%
5/40 33/88 0/40 2/40 27/40 13/40 0/40 1/40 1/40 1/40 37/40 13/40
12 41 0 5 68 32 0 2 2 2 92 32
7/40 32/80 0/40 1/40 30/40 10/40 0/40 0/40 0/40 0/40 40/40 10/40
17 40 0 2 75 25 0 0 0 0 100 25
aStaging by UICC classification: pTis = carcinoma in situ as
staged by histopathology; pT1 = tumor smaller than 2 cm as staged by histopathology; pT2 = tumor between 2 and 5 cm as staged by histopathology; pT3 = tumor more than 5 cm in diameter as staged by histopathology; pT4 = tumor infiltrating skin and/or thorax muscle; pN0 = no metastases in the lymph nodes as staged by histopathology; pN1 = homolateral mestastases in the axillary lymph nodes as staged by histopathology; pN2 = several metastases in the lymph nodes form an axillary tumor as staged by histopathology; pMovar = metastases in the ovaries as staged by histopathology; pMos = metastases in the bones staged by clinical and radiological investigations; Mhep = metastases in the liver as staged by ultrasonography or radiology; pM1 = axill. soft tissue metastases in the axilla but not in the lymph nodes; M0 = no metastases can be found by clinical and/or radiological investigations
76
February 2003, Vol. 10, No. 1
The Journal of the American Association of Gynecologic Laparoscopists
in the axilla, with mean volume of 8.7 ml (range 0.6–122 ml). In group B, seroma was seen in 90% of patients, with mean volume of 6.4 ml (range 0.1–120 ml; Figure 1). Measurements of shoulder-arm mobilty started at 90-degree abduction and elevation, with 180-degree
elevation representing 100% (Figure 2). Short-term checks showed less limitation of mobility in group B. After approximately 3 months mobility in both groups was no longer significantly different. Postoperative pain mapping showed that more women in group A than in group B complained of pain
FIGURE 1. Seroma induction after classic and endosurgical lymphadenectomy.
FIGURE 2. Postoperative shoulder-arm mobility after classic and endosurgical lymphadenectomy (p <0.05, χ2 test).
77
Comparison of Classic and Endoscopic Lymphadenectomy to Stage Breast Cancer de Wilde et al
in the shoulder-arm region (Figure 3). Paresthesia, also measured by mapping, was predominantly found in group B compared with group A (Figure 4). Nine cases of lymphedema (≥1 cm difference in arm circumference) were found in group A (22%),
and eight (20%) in group B. In both groups the condition was mild (<2 cm arm diameter) and the difference was not statistically significant. Wound infections without elevated body temperature but with pain, erythema, and swelling were seen
FIGURE 3. Postoperative pain after classic and endosurgical lymphadenectomy (p <0.01, Fisher’s test).
FIGURE 4. Paresthesia in the shoulder-arm region after classic and endosurgical lymphadenectomy (p <0.01, Fisher’s test).
78
February 2003, Vol. 10, No. 1
The Journal of the American Association of Gynecologic Laparoscopists
operative pain during the first 3 months. Long-term studies must determine if the technique has the same safety with respect to local axillary recurrence. If so, it could become the method of choice for staging in breast cancer in women with clinically negative lymph nodes. Studies are under way to evaluate the possibility of endoscopic techniques for sentinel lymphadenectomy in breast cancer.4
in four patients (10%) in group A and two (5%) in group B. All six women were treated with antibiotics and none required surgical reintervention. Due to current regulations in the German health system in which medical insurance companies pay fixed fees for operative procedures involving breast cancer, there was no difference in hospital charges. Discussion
References
In this comparison of endoscopic and conventional axillary lymphadenectomy we found differences in short-term side effects possibly due to better preservation of fine axillary structures by the former method. The endoscopic technique caused less shoulder stiffness. Neurologic complaints such as paresthesia were more common in group B, however, but more shoulder-arm pain was seen in group A. These side effects were documented within the first 6 postoperative weeks. After 3 months there were no differences in side effects between groups. We conclude that, compared with classic lymphadenectomy, endoscopic axillary dissection improves postoperative shoulder-arm mobility and reduces post-
1. Hladiuk M, Hutchcroft S, Temple W, et al: Arm function after axillary dissection for breast cancer. J Surg Oncol 50:47–52, 1992 2. Nemoto T, Vana J, Bedwani RN, et al: Management and survival of female breast cancer. Cancer 45:2917–2924, 1980 3. Suzanne F, Emering C, Wattiez A, et al: Le curage axillaire par lipo-aspiration et prelevement endoscopique. Chirurgie 122:138–143, 1997 4. Veronesi U, Paganelli G, Galimberti V, et al: Sentinel node biopsy to avoid axillary dissection in breast cancer with clinically negative lymph nodes. Lancet 349: 1864–1867, 1997
79