AXILLARY LYMPH NODES AND ARM LYMPHATIC DRAINAGE …

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Lymphology 44 (2011) 103-112

AXILLARY LYMPH NODES AND ARM LYMPHATIC DRAINAGE PATHWAYS ARE SPARED DURING ROUTINE COMPLETE AXILLARY

CLEARANCE IN MAJORITY OF WOMEN UNDERGOING BREAST CANCER 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 OncologyCenter (RH,MB,JF), Wroclaw, Poland

ABSTRACT

Alterations in axillary lymph nodes(ALNs) after complete axillary lymph nodedissection (ALND) in comparison to thepreoperative status were evaluated usinglymphoscintigraphy performed preoperativelyand 1-6 weeks after surgery in 30 women witha new diagnosis of unilateral, invasive breastcarcinoma. Analysis of lymphoscintigramsrevealed that ALNs after surgery were presentin 26 of 30 examined women. In comparisonto preoperative status, they were visualized in the same location (12 women), in the same and additionally in different locations (9 women), or only in different locations (4 women). No lymph nodes were visualized inone woman and lymphocoele were in 4 women.Thus, after ALND, a variable number ofaxillary lymph nodes remain and were visu-alized on lymphoscintigraphy in the majorityof women. The classical ALND, therefore,does not allow complete dissection andremoval of axillary nodes with total disruptionof axillary lymphatic pathways, accounting inpart for the variable incidence and severity oflymphedema after the procedure.

Keywords: breast cancer, axillary lymph node dissection, lymphoscintigraphy,lymphedema, lymphatic transport,photoplethysmography

Axillary lymph node dissection (ALND)is performed for local cancer control and forstaging in breast carcinoma. The number ofaxillary lymph nodes removed correlates withfrequency of ipsilateral axillary recurrence,recurrence-free survival and overall survival(1,2). The absence or presence of cancer cells in axillary lymph nodes defines furtheroncological treatment and is the mostimportant prognostic factor for patients withbreast cancer (3).

ALND is, however, associated withmarked morbidity. Breast cancer-relatedlymphedema (BCRL) remains frequent anddistressing postoperative complication inwomen undergoing axillary clearance. BCRLaffects about one-third of all breast cancersurvivors and develops usually after a latentperiod of months or years after breast cancertreatment (4,5). BCRL frequently leads tosignificant disability, caused by impaired armmobility, pain, and recurrent infections

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(dermatolymphangitis -DLA) (6,7). Surgicaldissection of axillary lymph nodes, resultingin disruption of lymphatic vessels drainingthe arm, is recognized as the major risk factorof BCRL (5). However, the etiology of BCRLis not well understood and likely to becomplex and multifactorial (5,8-10). Theobservation that arm lymphedema does notaffect two-thirds of breast cancer survivorsdespite receiving similar treatment thatimpacts the anatomy and function of axillarystructures is still unexplained. Suggestedprotective mechanisms include openinganatomical peripheral lymphovenouscommunications (11,12) and development ofcollateral lymphatic circulation (13,14).Another mechanism might include thenumber of lymph nodes that remain afterALND (13).

As we have previously reported, presenceof functional axillary lymph nodes visualizedby lymphoscintigraphy within the axilla afterALND was associated with no or only mildlymphedema, whereas severe cases oflymphedema demonstrated no axillary lymphnodes (13). The majority of studies of theeffects of axillary lymph node clearancesurgery, including our prior study, have beenconducted on patients after ALND or withestablished BCRL. Preoperative evaluation of patients before surgery may providefurther clues to a better understanding of thepathogenesis of lymphedema.

The purpose of this study was to evaluatealterations in upper extremity lymphoscin-tigraphic patterns after breast cancer surgery with complete axillary clearance incomparison to the preoperative status.

MATERIAL AND METHODS

Patients

This study was approved by the LocalBioethical Committee of the WroclawMedical University. All subjects gaveinformed written consent prior to inclusion inthe study and selected demographic and

therapeutic parameters are presented in Table 1. Thirty women (mean age 55.97years; range: 29-80 years) with unilateralbreast carcinoma, who underwent breastsurgery with complete axillary dissection(ALND) were examined. ALND wasperformed by experienced team of oncologicalsurgeons. Standard procedure that encom-passes removal of levels I, II and III nodaltissue in one bloc was performed in everycase, regardless to the clinical lymph nodestatus and the axillary vein was the upperlimit of the range of surgery. The posteriorwall of the axilla, consisted of subscapularis,latissimus dorsi, and teres major muscles wasclearly seen during each ALND and both thelong thoracic and thoracodorsal nerves werealso preserved. Stripping of the axillary veinwas always avoided.

In all the patients, axillary lymph nodeswere evaluated using radionuclide lympho-scintigraphy performed preoperatively and 1-6 weeks after surgery.

Lymphoscintigraphy

Injections of 0.25 mCi of 99mTc-Nanocoll were done simultaneously in bothhands in the second and the third interdigitalspace. Total injected dose was 1mCi perpatient. Static whole body images wereacquired 10 minutes and 2 hours after theinjection. The procedure was performedpreoperatively and repeated 1-6 weeks after surgery.

Axillary lymph nodes status before andafter ALND was evaluated in every womenqualitatively and quantitatively. Qualitativeanalysis of the postoperative pattern ofaxillary lymph nodes in comparison topreoperative status was performed for everypatient independently by two physicians. The patients were divided into the followinggroups: 1- lymph nodes visualized on theoperated side in the same location, howeverweaker than before surgery as compared tothe non-operated side; 2- lymph nodes in thesame location - not changed or better


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visualized than before surgery as compared to the non-operated side; 3- lymph nodesvisualized in the same location with additionalvisualization of lymph nodes in differentlocations; 4- lymph nodes visualized on theoperated side however in different locations;5- no lymph nodes visualized on the operatedside; 6- presence of lymphocoele; 7- presenceof lymphocoele and visualization of lymphnodes on the operated side.

For quantitative analysis, symmetricalregions of interest (ROIs) were placed overthe injection site and the axilla on eachlymphoscintigram. Radioactivity in ROIs wasmeasured 10 minutes after injection (ROI0)and 2 hours later (ROI2h), before and afterALND. Quantification of lymphatic transportwas performed by calculation of the followingparameters:

(1) Axillary ratio 2 hours post injection(AR2h): the radioactivity was measured atROI over axilla 2 hours post injection(ROIax.) to radioactivity of symmetrical ROI

over injection site (ROIinj.) for each upperextremity before and after surgery by usingthe formula: AR2h = (ROIax. / ROIinj.);

(2) AR2h operated arm/AR2h non-operated arm (AR2h ratio) was calculated for every patient before and after ALND;

(3) Tracer disappearance rate from theinjection site 2 hours post injection (TD2h):the radioactivity was measured at ROI overboth sites of injection (ROIinj.) for each upperextremity before and after surgery by usingthe formula: TD2h = (ROIinj.

0/ROIinj.2h);

(4) TD2h operated arm/TD2h non-operated arm (TD2h ratio) was calculated forevery patient before and after ALND.

Photoplethysmography

Venous photoplethysmography wascarried out to assess effect of ALND onvenous flow in the upper extremities. Venousphotoplethysmography of upper limbs was

TABLE 1 Patient Demographics and Treatment Characteristics


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performed with Rheo Dopplex II PPG (HNEMedical) in 22 women before and aftersurgery on the day of lymphoscintigraphy.Examination was performed in a sittingposition with upper limbs allowed to hangdown. The photoplethysmographic sensorwas placed on the dorsal side of the wrist andthe subjects then performed 10 rhythmicalelbow flexions. The photoplethysmographiccurve was recorded during the exercises. Thevenous pump index (Vp) and venous refillingtime (RT) were automatically calculatedusing software provided by manufacturer(HNE Medical Inc.).

Statistical Methods

Statistical analysis was performed usingStatistica for Windows 9.0. Differencesbetween lymphoscintigraphic and photo-plethysmographic parameters before andafter ALND were evaluated using t-test for dependent samples. Differences wereconsidered significant when p<0.05.

RESULTS

Qualitative visual analysis of lympho-scintigraphic patterns of lymph nodes beforeand after ALND in all the patients revealedthe following results:

1) lymph nodes visualized on theoperated side in the same location, howeverweaker than before surgery as compared tothe non-operated side – 10 women (33%)

2) lymph nodes in the same locationwithout change or better visualized thanbefore surgery as compared to the non-operated side – 2 women (6.6%)

3) lymph nodes visualized in the samelocation with additional visualization of lymphnodes in different location – 9 women (30%)

4) lymph nodes visualized on theoperated side in different location – 4 women(13.3%)

5) no lymph nodes visualized on theoperated side – 1 woman (3.3%)

6) presence of lymphocoele – 3 women(10%)

Fig. 1. Lymphoscintgrams before and after a left side ALND. Lymph nodes on the operated side are in the samelocation 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 liver indicates thatsome amount of the tracer entered the venous system probably at the injection site, however, opening oflymphovenous anastomoses or flow through the right side cannot be ruled out.


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7) presence of lymphocoele andvisualization of lymph nodes on the operatedside – 1 woman (3.3%)

Figs. 1-4 present the examples ofobserved alterations in lymphoscintigrams.

Quantitative analysis revealed that thedifferences between lymphoscintigraphic

axillary ratio and tracer disappearance ratebefore and after ALND were not statisticallyrelevant (Table 2). Also venous functionexamined by photoplethysmography was notaffected by surgery-venous pump index andvenous refill time did not differ before andafter surgery.

Fig. 2. Lymphoscintgrams before and after a right side ALND. Lymph nodes on the operated side after surgery arevisualized 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 atthe same location with additional visualization of lymph nodes in different location (neck) suggesting existence ofan additional lymphatic drainage pathway. Interestingly, liver can be also noticed on the postoperativelymphoscintigraphy.


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

TABLE 2Quantitative Analysis of Lymphoscintigrams

and Venous Photoplethysmography

DISCUSSION

We have attempted to compare upperextremity lymphoscintigrams and the axillarylymph node status before and after ALND inwomen undergoing breast cancer surgery. We have previously shown that the presenceof functional axillary lymph nodes after

ALND was associated with the lack of orwith mild lymphedema, whereas in severecases of upper extremity lymphedema noaxillary lymph nodes were seen (13). Thesimilar results were reported in other studies(9,15,16). However, the origin of lymph nodes visualized after ALND was notcompletely clear.


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Our current observations revealed thataxillary lymph nodes after ALND werevisualized in majority of women (87%)enrolled to this study. Lymphocele waspresent in three of four women within thegroup without clearly visible axillary lymphnodes. The lymphocoele could howeverinterfere with visualization of axillary lymphnodes, and we cannot completely excludetheir presence in these cases.

The presence of axillary lymph nodesafter ALND has been already reported in theliterature (13,15-17). Bourgeois performedpostoperative axillary lymphoscintigraphy in 313 women who had undergone a radicalmastectomy with ALND for breast cancer. He observed a presence of axillary nodes in64.2% of women in his series and heattributed this finding to incomplete surgicaldissection (15).

In our study, the axillary disappearanceratio (AR2h) before and after ALND, as wellas the tracer disappearance (TD2h) ratebefore and after ALND did not significantlydiffer, which is in agreement with our quali-tative analysis and with previous reports(18,19). These findings support the idea thatlymphatic drainage from the arm to theaxillary lymph nodes is initially notsignificantly impaired after the ALND inspite of the level I-III lymph node removal.

ALNs that remain after ALND may beconsidered as lymph nodes within theoperated area omitted during the surgery orlymph nodes beyond operative area serving as a drainage pathway of the upper extremity.Although regeneration of regional lymphnodes might be an interesting assumption(20), taking into account short time betweenoperation and the second lymphoscintigraphy,the possibility of regeneration of axillarylymph nodes in women examined in ourstudy is rather impossible.

The most prevailing recognition ofremaining axillary lymph nodes after ALNDis that they had been missed during operation(13,15,21). Such factors as oncologic andgeneral training of the surgeon, type of insti-

tution at which the operation was performed(tertiary referral center versus otherhospitals), or even bias toward performing amore aggressive surgical approach in patientswith locally advanced cancer certainly canimpact the number of axillary lymph nodesretrieved during ALND (21).

However, in this study, the operationswere performed by the experienced team ofoncologic surgeons, with long term outcomessimilar to other oncology referral centers inEurope. All breast operations wereaccompanied by complete and careful level I,II, and III axillary lymph node dissectionwith minimal chance to miss lymph nodeswithin predefined for level III dissectionaxillary operative area. We believe thatfunctional axillary lymph nodes remainingafter axillary lymph node dissection representnot unusual finding and result from specificaxillary lymphatic anatomy rather thanincomplete dissection due to technical issues.

Therefore, we propose the hypothesisthat the presence of axillary lymph nodesafter ALND is a result of a standard opera-tive ALND procedure that defines the limitsof axillary penetration and does not enablethe dissection of all the axillary lymph nodesin the majority of women.

Axillary lymph nodes have been dividedby anatomists into five groups as follows:anterior (drains lymph from the anteriorchest wall, including the ipsilateral breast),posterior (drains posterior chest wall), lateral(drains upper extremity), central (gets lymphfrom anterior and lateral group) and apical(= subclavian, gets lymph from central groupand drains into the thoracic duct on the leftor directly into the brachiocephalic vein onthe right) (22-24). Lymphatic vessels of theupper extremity, both superficial and deep,mainly drain through the axillary lateralgroup which consists of 4-6 lymph nodes (22-24). Besides, there are some minor lymphdrainage pathways from upper extremity, i.e.,some of the superficial radial lymph vesselsform a trunk that ascends with the cephalicvein to reach the deltopectoral lymph nodes


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or continue with the cephalic vein and enterto the apical group of the axillary nodes (24).However, knowledge about the lymphaticsystem is largely dependent on the studiesperformed in the nineteenth century with theuse of mercury injected into human cadavers(25). There are only a few newer publishedstudies on lymphatic anatomy of the breastand upper extremity. Suami et al usedhydrogen peroxide to identify lymphaticvessels and then visualized them with radio-paque and color dyes in 14 cadavers. Hereported that most lymph vessels of upperextremity were seen to flow into one main(sentry) lymph node in the axillary regionand that the rest of lymph vessels ran alongthe posterior forearm, bypassing the “sentry”node to reach other smaller nodes withinaxilla (25).

Unlike anatomists, surgeons identifythree levels of axillary lymph nodes using the pectoralis minor muscle as a reference –level I is below, level II is posterior to, andlevel III is superior to the pectoralis minormuscle (26). A traditional ALND, which was undertaken in the women enrolled in this study, removes all the lymph nodes of the level I, II, and III. The number of lymphnodes retrieved during an ALND variessignificantly, even from 4 to 65 (21). Removalof at least 10 axillary lymph nodes isgenerally considered as reliable for adequatelymph node staging (27).

We presume that traditional ALNDremoves anterior and central lymph nodes,whereas the remaining groups of axillarylymph nodes are, at least partially, spared inthe majority of women. Three-dimensionalvisualization of axillary lymph nodes beforeand after surgery would help to documentand prove this hypothesis (28).

There is growing evidence that somewomen have a defined, hereditary, orconstitutive predisposition to BCRLdevelopment, consisting of such factors as:individual weakness or underdevelopment oflymphatics and veins (9,12,29,30), specificlymphatic and vein networks, including

presence of lymphovenous anastomoses(31,32), or higher peripheral filtration rates of the lymph (33). It may be postulated thatindividual anatomical arrangement ofaxillary lymph nodes also may be part of thehereditary predisposition to BCRL. Britton et al studied concurrently lymphatic drainagepathways of the upper extremity and of thebreast using lymphoscintigraphy with twodifferent radiotracers. He was able todetermine how often sentinel lymph node(SLN) draining the breast was the same nodeas the SLN draining the upper limb. He hasfound that the majority of women (13 of 15)had different pathways of lymphatic drainagefrom upper extremity and the breast, and inonly the other 2 patients was the sentinellymph node the same for breast and theupper extremity (32). In the study of Cloughet al in 238 patients (98.2%) the axillary SLNfor breast was located medially, and in onlyfour patients (1.8%) the SLN was locatedlaterally in the axilla (34). Nos and co-workers have shown that the dominant nodedraining the arm is usually situated in thelateral part of the axilla, underneath theaxillary vein (35). Patients in whom thesentinel lymph node is the same for the breastand upper extremity may be at increased riskof developing BCRL after ALND.

Axillary lymph nodes in 11 of 30 womenevaluated in our research were visualized in different localizations in comparison to thepreoperative lymphoscintigrams (9 women –in only different locations and 2 in differentplus the same locations as before operation).This may indicate that collateral lymphaticpathways were utilized in these subjects repre-senting a compensatory mechanism aftersurgical injury of axillary lymphatic system.

Suami described in detail compensatorymechanisms in a cadaver that had undergoneunilateral radical mastectomy and radicalaxillary dissection for breast cancer 11 yearsearlier. He used both upper limbs harvestedfrom cadaver to examine the changes in thelymphatic structure of upper extremity after ALND. He noted presence of some


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lymph nodes within the operated axilla andthe following alterations in comparison to the non-operated limb: interval lymph nodeenlargement, obliteration of superficiallymphatic vessels, dermal backflow, andunusual communication between the super-ficial and deep lymphatics. These changesseem to facilitate lymph drainage afterblockage of the lymph tract and couldprevent the development of lymphedema in those women (17).

The importance of the absence of axillarylymph nodes in the pathology of BCRL wasdemonstrated in the study of the long-termresults following autologous lymph nodetransplantation (ALNT). ALNT is a novelmicrosurgical technique for lymphedematreatment. Becker presented that after ALNT,postmastectomy lymphedema disappeared in 40% of patients and it notably improved in 48%. Improvement in lymphedema even in women without lymphoscintigraphic signs of lymphatic pathways restoration isdifficult to explain and requires furtherinvestigations (36).

CONCLUSIONS

Axillary lymph nodes can be detected inmajority of women who underwent surgicaldissection of axillary lymph nodes due tobreast cancer surgery.

Current operative technique of levelI+II+III axillary dissection does not allowdissection of all lymph nodes within operatedaxilla.

Visualization of axillary lymph nodes in different locations in comparison to thepreoperative status in almost half of thewomen indicates that collateral lymphaticpathways were recruited and may represent a compensatory mechanism after impairmentof axillary lymphatic circulation.

ACKNOWLEDGMENT

The study was supported by the PolishMinistry of Science and Higher Educationgrant no: N40406631/3041.

REFERENCES

1. Graversen, HP, K Zedeler, JA Andersen, et al: Axillary dissection in primary surgicaltreatment of breast cancer: Risk of false-negative axillary status. Ugeskr. Laeger 154(1992), 3392-3395.

2. Weir, L, C Speers, Y D’Yachkova, et al:Prognostic significance of the number ofaxillary lymph nodes removed in patientswith node-negative breast cancer. J. Clin.Oncol. 20 (2002), 1793-1799.

3. Carter, CL, C Allen, DE Henson: Relation oftumor size, lymph node status, and survival in24,740 breast cancer cases. Cancer 63 (1989),181-187.

4. Petrek, JA, RT Senie, M Peters, et al:Lymphedema in a cohort of breast carcinomasurvivors 20 years after diagnosis. Cancer 92(2001), 1368-1377.

5. Szuba, A, SG Rockson: Lymphedema:anatomy, physiology and pathogenesis. Vasc.Med. 2 (1997), 321-326.

6. Chachaj, A, K Malyszczak, K Pyszel, et al:Physical and psychological impairments ofwomen with upper limb lymphedemafollowing breast cancer treatment.Psychooncology 19 (2010), 299-305.

7. Hormes, JM, C Bryan, LA Lytle, et al: Impactof lymphedema and arm symptoms on qualityof life in breast cancer survivors. Lymphology43 (2010), 1-13.

8. Mak, SS, W Yeo, YM Lee, et al: Predictors oflymphedema in patients with breast cancerundergoing axillary lymph node dissection inHong Kong. Nurs. Res. 57 (2008), 416-425.

9. Rockson, SG: Precipitating factors inlymphedema: Myths and realities. Cancer 83(1998), 2814-2816.

10. van der Veen, P, N De Voogdt, P Lievens, et al: Lymphedema development followingbreast cancer surgery with full axillaryresection. Lymphology 37 (2004), 206-208.

11. O’Mahony, S, TB Britton, JR Ballinger, et al:Delivery of radiolabelled blood cells tolymphatic vessels by intradermal injection: A means of investigating lymphovenouscommunications in the upper limb. Nucl.Med. Commun. 31 (2010), 121-127.

12. Pain, SJ, AD Purushotham, RW Barber, et al:Variation in lymphatic function maypredispose to development of breast cancer-related lymphoedema. Eur. J. Surg. Oncol. 30(2004), 508-514.

13. Szuba, A, A Pyszel, D Jedrzejuk, et al:Presence of functional axillary lymph nodesand lymph drainage within arms in womenwith and without breast cancer-relatedlymphedema. Lymphology 40 (2007), 81-86.


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14. Suami, H, WR Pan, GB Mann, et al: Thelymphatic anatomy of the breast and itsimplications for sentinel lymph node biopsy:A human cadaver study. Ann. Surg. Oncol, 15(2008), 863-871.

15. Bourgeois, P, J Fruhling, J Henry:Postoperative axillary lymphoscintigraphy inthe management of breast cancer. Int. J.Radiat. Oncol. Biol. Phys. 9 (1983), 29-32.

16. Weissleder, H, R Weissleder: Lymphedema:Evaluation of qualitative and quantitativelymphoscintigraphy in 238 patients.Radiology 167 (1988), 729-735.

17. Suami, H, WR Pan, GI Taylor: Changes inthe lymph structure of the upper limb afteraxillary dissection: radiographic andanatomical study in a human cadaver. Plast.Reconstr. Surg. 120 (2007), 982-991.

18. Pain, SJ, RW Barber, CK Solanki, et al:Short-term effects of axillary lymph nodeclearance surgery on lymphatic physiology ofthe arm in breast cancer. J. Appl. Physiol. 99(2005), 2345-2351.

19. Pain, SJ, RW Barber, JR Ballinger, et al:Local vascular access of radioprotein injectedsubcutaneously in healthy subjects andpatients with breast cancer-related lymphe-dema. J. Nucl. Med. 45 (2004), 789-796.

20. Olszewski, WL: De novo lymph nodeformation in chronic inflammation of thehuman leg. Ann. NY Acad. Sci. 979 (2002),166-177; discussion 188-196.

21. Boughey, JC, JH Donohue, JW Jakub, et al:Number of lymph nodes identified at axillarydissection: effect of neoadjuvant chemotherapyand other factors. Cancer 116 (2010),3322-3329.

22. Uflacker, R (Ed): Atlas of Vascular Anatomy.An Angiographic Approach. 2nd ed. Williams& Wilkins, Philadelphia, 2007.

23. Gray, H (Ed): Anatomy of the Human Body,20th ed., rev. and re-edited by Warren H.Lewis. VIII. The Lymphatic System. 4. The Lymphatics of the Upper Extremity. 7.The Lymphatic Vessels of the Thorax. Lea &Febiger, Philadelphia, 1918, Bartleby.com,2000.

24. Doyle JR, MJ Botte: Surgical Anatomy of the Hand and Upper Extremity. LippincottWilliams & Wilkins, 2003.

25. Suami, H, GI Taylor, WR Pan: The lymphaticterritories of the upper limb: Anatomicalstudy and clinical implications. Plast.Reconstr. Surg. 119 (2007), 1813-1822.

26. Bland, KI, MP Vezeridis, EM Copeland:Principles of Surgery. 7th edn. New York:McGraw-Hill, 1999.

27. Mathiesen, O, J Carl, O Bonderup, et al:Axillary sampling and the riskof erroneousstaging of breast cancer. An analysis of 960

consecutive patients. Acta Oncol. 29 (1990),721-725.

28. Minato, M, C Hirose, M Sasa, et al: 3-dimensional computed tomographylymphography-guided identification ofsentinel lymph nodes in breast cancer patientsusing subcutaneous injection of nonioniccontrast medium: A clinical trial. J. Comput.Assist. Tomogr. 28 (2004), 46-51.

29. Stanton, AW, RH Mellor, GJ Cook, et al:Impairment of lymph drainage in subfascialcompartment of forearm in breast cancer-related lymphedema. Lymphat. Res. Biol. 1(2003), 121-132.

30. Pain, SJ, RW Barber, JR Ballinger, et al:Tissue-to-blood transport of radiolabelledimmunoglobulin injected into the web spacesof the hands of normal subjects and patientswith breast cancer-related lymphoedema. J.Vasc. Res. 41 (2004), 183-192.

31. Peters AM, JC Fowler, TB Britton, et al:Functional variation in lymph nodearrangements within the axilla. Lymphat.Res. Biol. 7 (2009), 139-144.

32. Britton, TB, CK Solanki, SE Pinder, et al:Lymphatic drainage pathways of the breastand the upper limb. Nucl. Med. Commun. 30 (2009), 427-430.

33. Stanton, AW, S Modi, TM Bennett Britton, et al: Lymphatic drainage in the muscle andsubcutis of the arm after breast cancertreatment. Breast Cancer Res. Treat. 117(2009) 549-557.

34. Clough, KB, R Nasr, C Nos, et al: Newanatomical classification of the axilla withimplications for sentinel node biopsy. Br. J.Surg. 97 (2010),1659-1665.

35. Nos, C, B Lesieur, KB Clough, et al: Blue dyeinjection in the arm in order to conserve thelymphatic drainage of the arm in breastcancer patients requiring an axillary dissection.Ann. Surg. Oncol. 14 (2007), 2490-2496.

36. Becker, C, J Assouad, M Riquet, et al.Postmastectomy lymphedema: Long-termresults following microsurgical lymph nodetransplantation. Ann. Surg.243 (2006), 313-315.

Andrzej Szuba, MD, PhD Professor of Medicine, Wroclaw Medical UniversityDepartment of Internal Medicine, Borowska 213 street50- 556 Wroclaw, PolandPhone: +48 71 736 4000Mobile: +48 504 085 101Fax: +48 71 736 4009Email: [email protected]


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AXILLARY LYMPH NODES AND ARM LYMPHATIC DRAINAGE …