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Lymphology 44 (2011) 103-112

AXILLARY NODES AND LYMPHATIC DRAINAGE PATHWAYS ARE SPARED DURING ROUTINE COMPLETE AXILLARY CLEARANCE IN MAJORITY OF WOMEN UNDERGOING SURGERY

A. Szuba, A. Chachaj, M. Koba-Wszedybylb, R. Hawro, R. Jasinski, R. Tarkowski, K. Szewczyk, M. Bebenek, J. Forgacz, A. Jodkowska, D. Jedrzejuk, D. Janczak, M. Mrozinska, U. Pilch, M. Wozniewski

Departments of Internal Medicine (AS,AC,MK-W,AJ), Oncology and Gynecological Oncology (RT,KS), and Endocrinology (DJ), Wroclaw Medical University; Faculty of Physiotherapy (AS,RH,RJ,MM,UP,MW), University School of Physical Education; and Lower Silesian Oncology Center (RH,MB,JF), Wroclaw, Poland

ABSTRACT Keywords: , axillary dissection, lymphoscintigraphy, Alterations in , lymphatic transport, (ALNs) after complete axillary lymph node photoplethysmography dissection (ALND) in comparison to the preoperative status were evaluated using Axillary lymph node dissection (ALND) lymphoscintigraphy performed preoperatively is performed for local cancer control and for and 1-6 weeks after surgery in 30 women with staging in breast carcinoma. The number of a new diagnosis of unilateral, invasive breast axillary lymph nodes removed correlates with carcinoma. Analysis of lymphoscintigrams frequency of ipsilateral axillary recurrence, revealed that ALNs after surgery were present recurrence-free survival and overall survival in 26 of 30 examined women. In comparison (1,2). The absence or presence of cancer to preoperative status, they were visualized cells in axillary lymph nodes defines further in the same location (12 women), in the oncological treatment and is the most same and additionally in different locations important prognostic factor for patients with (9 women), or only in different locations breast cancer (3). (4 women). No lymph nodes were visualized in ALND is, however, associated with one woman and lymphocoele were in 4 women. marked morbidity. Breast cancer-related Thus, after ALND, a variable number of lymphedema (BCRL) remains frequent and axillary lymph nodes remain and were visu- distressing postoperative complication in alized on lymphoscintigraphy in the majority women undergoing axillary clearance. BCRL of women. The classical ALND, therefore, affects about one-third of all breast cancer does not allow complete dissection and survivors and develops usually after a latent removal of axillary nodes with total disruption period of months or years after breast cancer of axillary lymphatic pathways, accounting in treatment (4,5). BCRL frequently leads to part for the variable incidence and severity of significant disability, caused by impaired arm lymphedema after the procedure. mobility, pain, and recurrent

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(dermatolymphangitis -DLA) (6,7). Surgical therapeutic parameters are presented in dissection of axillary lymph nodes, resulting Table 1. Thirty women (mean age 55.97 in disruption of lymphatic vessels draining years; range: 29-80 years) with unilateral the arm, is recognized as the major risk factor breast carcinoma, who underwent breast of BCRL (5). However, the etiology of BCRL surgery with complete axillary dissection is not well understood and likely to be (ALND) were examined. ALND was complex and multifactorial (5,8-10). The performed by experienced team of oncological observation that arm lymphedema does not surgeons. Standard procedure that encom- affect two-thirds of breast cancer survivors passes removal of levels I, II and III nodal despite receiving similar treatment that tissue in one bloc was performed in every impacts the and function of axillary case, regardless to the clinical lymph node structures is still unexplained. Suggested status and the axillary was the upper protective mechanisms include opening limit of the range of surgery. The posterior anatomical peripheral lymphovenous wall of the , consisted of subscapularis, communications (11,12) and development of latissimus dorsi, and teres major muscles was collateral lymphatic circulation (13,14). clearly seen during each ALND and both the Another mechanism might include the long thoracic and thoracodorsal were number of lymph nodes that remain after also preserved. Stripping of the axillary vein ALND (13). was always avoided. As we have previously reported, presence In all the patients, axillary lymph nodes of functional axillary lymph nodes visualized were evaluated using radionuclide lympho- by lymphoscintigraphy within the axilla after scintigraphy performed preoperatively and ALND was associated with no or only mild 1-6 weeks after surgery. lymphedema, whereas severe cases of lymphedema demonstrated no axillary lymph Lymphoscintigraphy nodes (13). The majority of studies of the effects of axillary lymph node clearance Injections of 0.25 mCi of 99mTc- surgery, including our prior study, have been Nanocoll were done simultaneously in both conducted on patients after ALND or with hands in the second and the third interdigital established BCRL. Preoperative evaluation space. Total injected dose was 1mCi per of patients before surgery may provide patient. Static whole body images were further clues to a better understanding of the acquired 10 minutes and 2 hours after the pathogenesis of lymphedema. injection. The procedure was performed The purpose of this study was to evaluate preoperatively and repeated 1-6 weeks alterations in upper extremity lymphoscin- after surgery. tigraphic patterns after breast cancer Axillary lymph nodes status before and surgery with complete axillary clearance in after ALND was evaluated in every women comparison to the preoperative status. qualitatively and quantitatively. Qualitative analysis of the postoperative pattern of MATERIAL AND METHODS axillary lymph nodes in comparison to preoperative status was performed for every Patients patient independently by two physicians. The patients were divided into the following This study was approved by the Local groups: 1- lymph nodes visualized on the Bioethical Committee of the Wroclaw operated side in the same location, however Medical University. All subjects gave weaker than before surgery as compared to informed written consent prior to inclusion in the non-operated side; 2- lymph nodes in the the study and selected demographic and same location - not changed or better

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TABLE 1 Patient Demographics and Treatment Characteristics

visualized than before surgery as compared over injection site (ROIinj.) for each upper to the non-operated side; 3- lymph nodes extremity before and after surgery by using 2h visualized in the same location with additional the formula: AR = (ROIax. / ROIinj.); visualization of lymph nodes in different (2) AR2h operated arm/AR2h non- locations; 4- lymph nodes visualized on the operated arm (AR2h ratio) was operated side however in different locations; calculated for every patient before 5- no lymph nodes visualized on the operated and after ALND; side; 6- presence of lymphocoele; 7- presence (3) Tracer disappearance rate from the of lymphocoele and visualization of lymph injection site 2 hours post injection (TD2h): nodes on the operated side. the radioactivity was measured at ROI over For quantitative analysis, symmetrical both sites of injection (ROIinj.) for each upper regions of interest (ROIs) were placed over extremity before and after surgery by using 2h 0 2h the injection site and the axilla on each the formula: TD = (ROIinj. /ROIinj. ); lymphoscintigram. Radioactivity in ROIs was (4) TD2h operated arm/TD2h non- measured 10 minutes after injection (ROI0) operated arm (TD2h ratio) was calculated for and 2 hours later (ROI2h), before and after every patient before and after ALND. ALND. Quantification of lymphatic transport was performed by calculation of the following Photoplethysmography parameters: (1) Axillary ratio 2 hours post injection Venous photoplethysmography was (AR2h): the radioactivity was measured at carried out to assess effect of ALND on ROI over axilla 2 hours post injection venous flow in the upper extremities. Venous (ROIax.) to radioactivity of symmetrical ROI photoplethysmography of upper limbs was

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Fig. 1. Lymphoscintgrams before and after a left side ALND. Lymph nodes on the operated side are in the same location with reduced visibility and the loss of distal nodes could be due to operative dissection (arrows). Interestingly, axillary lymph nodes on the right side are also less visible. Visualization of the indicates that some amount of the tracer entered the venous system probably at the injection site, however, opening of lymphovenous anastomoses or flow through the right side cannot be ruled out.

performed with Rheo Dopplex II PPG (HNE RESULTS Medical) in 22 women before and after surgery on the day of lymphoscintigraphy. Qualitative visual analysis of lympho- Examination was performed in a sitting scintigraphic patterns of lymph nodes before position with upper limbs allowed to hang and after ALND in all the patients revealed down. The photoplethysmographic sensor the following results: was placed on the dorsal side of the wrist and 1) lymph nodes visualized on the the subjects then performed 10 rhythmical operated side in the same location, however flexions. The photoplethysmographic weaker than before surgery as compared to curve was recorded during the exercises. The the non-operated side – 10 women (33%) venous pump index (Vp) and venous refilling 2) lymph nodes in the same location time (RT) were automatically calculated without change or better visualized than using software provided by manufacturer before surgery as compared to the non- (HNE Medical Inc.). operated side – 2 women (6.6%) 3) lymph nodes visualized in the same Statistical Methods location with additional visualization of lymph nodes in different location – 9 women (30%) Statistical analysis was performed using 4) lymph nodes visualized on the Statistica for Windows 9.0. Differences operated side in different location – 4 women between lymphoscintigraphic and photo- (13.3%) plethysmographic parameters before and 5) no lymph nodes visualized on the after ALND were evaluated using t-test operated side – 1 woman (3.3%) for dependent samples. Differences were 6) presence of lymphocoele – 3 women considered significant when p<0.05. (10%)

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Fig. 2. Lymphoscintgrams before and after a right side ALND. Lymph nodes on the operated side after surgery are visualized at the same location with more intensity than before ALND. Liver is also visualized.

Fig. 3. Lymphoscintgrams before and after a right side ALND. Lymph nodes on the operated side are visualized at the same location with additional visualization of lymph nodes in different location (neck) suggesting existence of an additional lymphatic drainage pathway. Interestingly, liver can be also noticed on the postoperative lymphoscintigraphy.

7) presence of lymphocoele and axillary ratio and tracer disappearance rate visualization of lymph nodes on the operated before and after ALND were not statistically side – 1 woman (3.3%) relevant (Table 2). Also venous function Figs. 1-4 present the examples of examined by photoplethysmography was not observed alterations in lymphoscintigrams. affected by surgery-venous pump index and Quantitative analysis revealed that the venous refill time did not differ before and differences between lymphoscintigraphic after surgery.

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Fig. 4. Lymphoscintgrams before and after a right side ALND. After the operation, axillary lymph nodes on the operated side (right) are visualized. In addition, there is a presence of right side lymphocoele highlighted with tracer filling (arrow).

TABLE 2 Quantitative Analysis of Lymphoscintigrams and Venous Photoplethysmography

DISCUSSION ALND was associated with the lack of or with mild lymphedema, whereas in severe We have attempted to compare upper cases of upper extremity lymphedema no extremity lymphoscintigrams and the axillary axillary lymph nodes were seen (13). The lymph node status before and after ALND in similar results were reported in other studies women undergoing breast cancer surgery. (9,15,16). However, the origin of lymph We have previously shown that the presence nodes visualized after ALND was not of functional axillary lymph nodes after completely clear.

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Our current observations revealed that tution at which the operation was performed axillary lymph nodes after ALND were (tertiary referral center versus other visualized in majority of women (87%) hospitals), or even bias toward performing a enrolled to this study. Lymphocele was more aggressive surgical approach in patients present in three of four women within the with locally advanced cancer certainly can group without clearly visible axillary lymph impact the number of axillary lymph nodes nodes. The lymphocoele could however retrieved during ALND (21). interfere with visualization of axillary lymph However, in this study, the operations nodes, and we cannot completely exclude were performed by the experienced team of their presence in these cases. oncologic surgeons, with long term outcomes The presence of axillary lymph nodes similar to other oncology referral centers in after ALND has been already reported in the Europe. All breast operations were literature (13,15-17). Bourgeois performed accompanied by complete and careful level I, postoperative axillary lymphoscintigraphy II, and III axillary lymph node dissection in 313 women who had undergone a radical with minimal chance to miss lymph nodes mastectomy with ALND for breast cancer. within predefined for level III dissection He observed a presence of axillary nodes in axillary operative area. We believe that 64.2% of women in his series and he functional axillary lymph nodes remaining attributed this finding to incomplete surgical after axillary lymph node dissection represent dissection (15). not unusual finding and result from specific In our study, the axillary disappearance axillary lymphatic anatomy rather than ratio (AR2h) before and after ALND, as well incomplete dissection due to technical issues. as the tracer disappearance (TD2h) rate Therefore, we propose the hypothesis before and after ALND did not significantly that the presence of axillary lymph nodes differ, which is in agreement with our quali- after ALND is a result of a standard opera- tative analysis and with previous reports tive ALND procedure that defines the limits (18,19). These findings support the idea that of axillary penetration and does not enable lymphatic drainage from the arm to the the dissection of all the axillary lymph nodes axillary lymph nodes is initially not in the majority of women. significantly impaired after the ALND in Axillary lymph nodes have been divided spite of the level I-III lymph node removal. by anatomists into five groups as follows: ALNs that remain after ALND may be anterior (drains lymph from the anterior considered as lymph nodes within the chest wall, including the ipsilateral breast), operated area omitted during the surgery or posterior (drains posterior chest wall), lateral lymph nodes beyond operative area serving (drains upper extremity), central (gets lymph as a drainage pathway of the upper extremity. from anterior and lateral group) and apical Although regeneration of regional lymph (= subclavian, gets lymph from central group nodes might be an interesting assumption and drains into the thoracic duct on the left (20), taking into account short time between or directly into the brachiocephalic vein on operation and the second lymphoscintigraphy, the right) (22-24). Lymphatic vessels of the the possibility of regeneration of axillary upper extremity, both superficial and deep, lymph nodes in women examined in our mainly drain through the axillary lateral study is rather impossible. group which consists of 4-6 lymph nodes The most prevailing recognition of (22-24). Besides, there are some minor lymph remaining axillary lymph nodes after ALND drainage pathways from upper extremity, i.e., is that they had been missed during operation some of the superficial radial lymph vessels (13,15,21). Such factors as oncologic and form a trunk that ascends with the cephalic general training of the surgeon, type of insti- vein to reach the deltopectoral lymph nodes

Permission granted for single print for individual use. Reproduction not permitted without permission of Journal LYMPHOLOGY. 110 or continue with the cephalic vein and enter presence of lymphovenous anastomoses to the apical group of the axillary nodes (24). (31,32), or higher peripheral filtration rates However, knowledge about the lymphatic of the lymph (33). It may be postulated that system is largely dependent on the studies individual anatomical arrangement of performed in the nineteenth century with the axillary lymph nodes also may be part of the use of mercury injected into cadavers hereditary predisposition to BCRL. Britton (25). There are only a few newer published et al studied concurrently lymphatic drainage studies on lymphatic anatomy of the breast pathways of the upper extremity and of the and upper extremity. Suami et al used breast using lymphoscintigraphy with two hydrogen peroxide to identify lymphatic different radiotracers. He was able to vessels and then visualized them with radio- determine how often paque and color dyes in 14 cadavers. He (SLN) draining the breast was the same node reported that most lymph vessels of upper as the SLN draining the . He has extremity were seen to flow into one main found that the majority of women (13 of 15) (sentry) lymph node in the axillary region had different pathways of lymphatic drainage and that the rest of lymph vessels ran along from upper extremity and the breast, and in the posterior forearm, bypassing the “sentry” only the other 2 patients was the sentinel node to reach other smaller nodes within lymph node the same for breast and the axilla (25). upper extremity (32). In the study of Clough Unlike anatomists, surgeons identify et al in 238 patients (98.2%) the axillary SLN three levels of axillary lymph nodes using for breast was located medially, and in only the pectoralis minor muscle as a reference – four patients (1.8%) the SLN was located level I is below, level II is posterior to, and laterally in the axilla (34). Nos and co- level III is superior to the pectoralis minor workers have shown that the dominant node muscle (26). A traditional ALND, which draining the arm is usually situated in the was undertaken in the women enrolled in lateral part of the axilla, underneath the this study, removes all the lymph nodes of axillary vein (35). Patients in whom the the level I, II, and III. The number of lymph sentinel lymph node is the same for the breast nodes retrieved during an ALND varies and upper extremity may be at increased risk significantly, even from 4 to 65 (21). Removal of developing BCRL after ALND. of at least 10 axillary lymph nodes is Axillary lymph nodes in 11 of 30 women generally considered as reliable for adequate evaluated in our research were visualized lymph node staging (27). in different localizations in comparison to the We presume that traditional ALND preoperative lymphoscintigrams (9 women – removes anterior and , in only different locations and 2 in different whereas the remaining groups of axillary plus the same locations as before operation). lymph nodes are, at least partially, spared in This may indicate that collateral lymphatic the majority of women. Three-dimensional pathways were utilized in these subjects repre- visualization of axillary lymph nodes before senting a compensatory mechanism after and after surgery would help to document surgical injury of axillary . and prove this hypothesis (28). Suami described in detail compensatory There is growing evidence that some mechanisms in a cadaver that had undergone women have a defined, hereditary, or unilateral radical mastectomy and radical constitutive predisposition to BCRL axillary dissection for breast cancer 11 years development, consisting of such factors as: earlier. He used both upper limbs harvested individual weakness or underdevelopment of from cadaver to examine the changes in the lymphatics and (9,12,29,30), specific lymphatic structure of upper extremity lymphatic and vein networks, including after ALND. He noted presence of some

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