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Published in: Breast Cancer Research and Treatment 1/2013

01-05-2013 | Clinical Trial

A longitudinal study of shoulder and arm morbidity in breast cancer survivors 7 years after sentinel lymph node biopsy or axillary lymph node dissection

Authors: Jan J. Kootstra, Pieter U. Dijkstra, Hans Rietman, Jaap de Vries, Peter Baas, Jan H. B. Geertzen, Harald J. Hoekstra, Josette E. H. M. Hoekstra-Weebers

Published in: Breast Cancer Research and Treatment | Issue 1/2013

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Abstract

Knowledge about long-term consequences of breast cancer treatment on shoulder and arm function and volume in stages I–II breast cancer survivors is limited. The effects of shoulder–arm function shortly after surgery on long-term function are unknown. One hundred and ninety-four women were examined pre-surgery (T0) and 6 weeks after surgery (T1). Of those, 110 were re-examined 7 years later (T2). Thirty-four women underwent sentinel lymph node biopsy (SLNB) and 76 underwent axillary lymph node dissection (ALND). Differences between affected and unaffected side were calculated for four ranges of motion functions, three strength functions and arm volume. These were used to analyse time and group effects. Differences exceeding 20° in range of motion, 20 % in strength and 200 ml in arm volume were considered clinically relevant. Multivariate regression analyses examined the effect of shoulder–arm function at T1 on shoulder–arm function at T2. Additional predictor variables included were age, follow-up time, Body Mass Index, complications, chemotherapy, radiation, SLNB/ALND and type of breast surgery. At T2, range of motion (except external rotation), abduction strength and arm volume were impaired compared to T0. After ALND, women had significantly more forward flexion impairment, increased arm volume and clinically relevant impairments (70 %) than after SLNB (41 %). T1 external rotation, abduction–external rotation, grip strength and arm volume were the strongest predictors of these variables at T2. Age was the strongest predictor of the remaining four variables. ALND predicted arm volume only. Seven years after breast cancer surgery, two-fifth of the women after SLNB and seven out of ten women after ALND had impairments. Impairments were found in five of eight shoulder–arm functions. After SLNB, women have less forward flexion impairment and less arm volume increase than after ALND. Shoulder–arm function at 6 weeks after surgery and age are the strongest predictors of long-term shoulder–arm function.
Literature
1.
go back to reference Giuliano AE, Kirgan DM, Guenther JM, Morton DL (1994) Lymphatic mapping and sentinel lymphadenectomy for breast cancer. Ann Surg 220:391–398PubMedCrossRef Giuliano AE, Kirgan DM, Guenther JM, Morton DL (1994) Lymphatic mapping and sentinel lymphadenectomy for breast cancer. Ann Surg 220:391–398PubMedCrossRef
2.
go back to reference Krag DN, Weaver DL, Alex JC, Fairbank JT (1993) Surgical resection and radiolocalization of the sentinel lymph node in breast cancer using a gamma probe. Surg Oncol 2:335–339PubMedCrossRef Krag DN, Weaver DL, Alex JC, Fairbank JT (1993) Surgical resection and radiolocalization of the sentinel lymph node in breast cancer using a gamma probe. Surg Oncol 2:335–339PubMedCrossRef
3.
go back to reference Lyman GH, Giuliano AE, Somerfield MR et al (2005) American Society of Clinical Oncology guideline recommendations for sentinel lymph node biopsy in early-stage breast cancer. J Clin Oncol 23:7703–7720PubMedCrossRef Lyman GH, Giuliano AE, Somerfield MR et al (2005) American Society of Clinical Oncology guideline recommendations for sentinel lymph node biopsy in early-stage breast cancer. J Clin Oncol 23:7703–7720PubMedCrossRef
4.
go back to reference Krag DN, Anderson SJ, Julian TB et al (2007) Technical outcomes of sentinel-lymph-node resection and conventional axillary-lymph-node dissection in patients with clinically node-negative breast cancer: results from the NSABP B-32 randomised phase III trial. Lancet Oncol 8:881–888PubMedCrossRef Krag DN, Anderson SJ, Julian TB et al (2007) Technical outcomes of sentinel-lymph-node resection and conventional axillary-lymph-node dissection in patients with clinically node-negative breast cancer: results from the NSABP B-32 randomised phase III trial. Lancet Oncol 8:881–888PubMedCrossRef
5.
go back to reference Mansel RE, Fallowfield LJ, Kissin M et al (2006) Randomized multicenter trial of sentinel node biopsy versus standard axillary treatment in operable breast cancer: the ALMANAC Trial. J Natl Cancer Inst 98:599–609PubMedCrossRef Mansel RE, Fallowfield LJ, Kissin M et al (2006) Randomized multicenter trial of sentinel node biopsy versus standard axillary treatment in operable breast cancer: the ALMANAC Trial. J Natl Cancer Inst 98:599–609PubMedCrossRef
6.
go back to reference Wilke LG, McCall LM, Posther KE et al (2006) Surgical complications associated with sentinel lymph node biopsy: results from a prospective international cooperative group trial. Ann Surg Oncol 13:491–500PubMedCrossRef Wilke LG, McCall LM, Posther KE et al (2006) Surgical complications associated with sentinel lymph node biopsy: results from a prospective international cooperative group trial. Ann Surg Oncol 13:491–500PubMedCrossRef
7.
go back to reference Burak WE, Hollenbeck ST, Zervos EE, Hock KL, Kemp LC, Young DC (2002) Sentinel lymph node biopsy results in less postoperative morbidity compared with axillary lymph node dissection for breast cancer. Am J Surg 183:23–27PubMedCrossRef Burak WE, Hollenbeck ST, Zervos EE, Hock KL, Kemp LC, Young DC (2002) Sentinel lymph node biopsy results in less postoperative morbidity compared with axillary lymph node dissection for breast cancer. Am J Surg 183:23–27PubMedCrossRef
8.
go back to reference Del Bianco P, Zavagno G, Burelli P et al (2008) Morbidity comparison of sentinel lymph node biopsy versus conventional axillary lymph node dissection for breast cancer patients: results of the sentinella-GIVOM Italian randomised clinical trial. Eur J Surg Oncol 34:508–513PubMedCrossRef Del Bianco P, Zavagno G, Burelli P et al (2008) Morbidity comparison of sentinel lymph node biopsy versus conventional axillary lymph node dissection for breast cancer patients: results of the sentinella-GIVOM Italian randomised clinical trial. Eur J Surg Oncol 34:508–513PubMedCrossRef
9.
go back to reference Haid A, Kuehn T, Konstantiniuk P, Köberle-Wührer R, Knauer M, Keienberg R, Zimmermann G (2002) Shoulder–arm morbidity following axillary dissection and sentinel node only biopsy for breast cancer. Eur J Surg Oncol 28:705–710PubMedCrossRef Haid A, Kuehn T, Konstantiniuk P, Köberle-Wührer R, Knauer M, Keienberg R, Zimmermann G (2002) Shoulder–arm morbidity following axillary dissection and sentinel node only biopsy for breast cancer. Eur J Surg Oncol 28:705–710PubMedCrossRef
10.
go back to reference Husted Madsen A, Haugaard K, Soerensen J, Bokmand S, Friis E, Holtveg H, Peter Garne J, Horby J, Cristiansen P (2008) Arm morbidity following sentinel lymph node biopsy or axillary lymph node dissection: a study from the Danish Breast Cancer Cooperative Group. Breast 17:138–147PubMedCrossRef Husted Madsen A, Haugaard K, Soerensen J, Bokmand S, Friis E, Holtveg H, Peter Garne J, Horby J, Cristiansen P (2008) Arm morbidity following sentinel lymph node biopsy or axillary lymph node dissection: a study from the Danish Breast Cancer Cooperative Group. Breast 17:138–147PubMedCrossRef
11.
go back to reference Langer I, Guller U, Berclaz G et al (2007) Morbidity of sentinel lymph node biopsy (SLN) alone versus SLN and completion axillary lymph node dissection after breast cancer surgery: a prospective Swiss multicenter study on 659 patients. Ann Surg 245:452–461PubMedCrossRef Langer I, Guller U, Berclaz G et al (2007) Morbidity of sentinel lymph node biopsy (SLN) alone versus SLN and completion axillary lymph node dissection after breast cancer surgery: a prospective Swiss multicenter study on 659 patients. Ann Surg 245:452–461PubMedCrossRef
12.
go back to reference Leidenius M, Leppänen E, Krogerus L, von Smitten K (2003) Motion restriction and axillary web syndrome after sentinel node biopsy and axillary clearance in breast cancer. Am J Surg 185:127–130PubMedCrossRef Leidenius M, Leppänen E, Krogerus L, von Smitten K (2003) Motion restriction and axillary web syndrome after sentinel node biopsy and axillary clearance in breast cancer. Am J Surg 185:127–130PubMedCrossRef
13.
go back to reference Leidenius M, Leivonen M, Vironen J, von Smitten K (2005) The consequences of long-time arm morbidity in node-negative breast cancer patients with sentinel node biopsy or axillary clearance. J Surg Oncol 92:23–31PubMedCrossRef Leidenius M, Leivonen M, Vironen J, von Smitten K (2005) The consequences of long-time arm morbidity in node-negative breast cancer patients with sentinel node biopsy or axillary clearance. J Surg Oncol 92:23–31PubMedCrossRef
14.
go back to reference Peintinger F, Reitsamer R, Stranzl H, Ralph G (2003) Comparison of quality of life and arm complaints after axillary lymph node dissection vs sentinel lymph node biopsy in breast cancer patients. Br J Cancer 89:648–652PubMedCrossRef Peintinger F, Reitsamer R, Stranzl H, Ralph G (2003) Comparison of quality of life and arm complaints after axillary lymph node dissection vs sentinel lymph node biopsy in breast cancer patients. Br J Cancer 89:648–652PubMedCrossRef
15.
go back to reference Purushotham AD, Upponi S, Klevesath MB, Bobrow L, Millar K, Myles JP, Duffy SW (2005) Morbidity after sentinel lymph node biopsy in primary breast cancer: results from a randomized controlled trial. J Clin Oncol 23:4312–4321PubMedCrossRef Purushotham AD, Upponi S, Klevesath MB, Bobrow L, Millar K, Myles JP, Duffy SW (2005) Morbidity after sentinel lymph node biopsy in primary breast cancer: results from a randomized controlled trial. J Clin Oncol 23:4312–4321PubMedCrossRef
16.
go back to reference Ronka R, von Smitten K, Tasmuth T, Leidenius M (2005) One-year morbidity after sentinel node biopsy and breast surgery. Breast 14:28–36PubMedCrossRef Ronka R, von Smitten K, Tasmuth T, Leidenius M (2005) One-year morbidity after sentinel node biopsy and breast surgery. Breast 14:28–36PubMedCrossRef
17.
go back to reference Schrenk P, Rieger R, Shamiyeh A, Wayand W (2000) Morbidity following sentinel lymph node biopsy versus axillary lymph node dissection for patients with breast carcinoma. Cancer 88:608–614PubMedCrossRef Schrenk P, Rieger R, Shamiyeh A, Wayand W (2000) Morbidity following sentinel lymph node biopsy versus axillary lymph node dissection for patients with breast carcinoma. Cancer 88:608–614PubMedCrossRef
18.
go back to reference Temple LK, Baron R, Cody HS III et al (2002) Sensory morbidity after sentinel lymph node biopsy and axillary dissection: a prospective study of 233 women. Ann Surg Oncol 9:654–662PubMedCrossRef Temple LK, Baron R, Cody HS III et al (2002) Sensory morbidity after sentinel lymph node biopsy and axillary dissection: a prospective study of 233 women. Ann Surg Oncol 9:654–662PubMedCrossRef
19.
go back to reference Veronesi U, Paganelli G, Viale G et al (2003) A randomized comparison of sentinel-node biopsy with routine axillary dissection in breast cancer. N Engl J Med 349:546–553PubMedCrossRef Veronesi U, Paganelli G, Viale G et al (2003) A randomized comparison of sentinel-node biopsy with routine axillary dissection in breast cancer. N Engl J Med 349:546–553PubMedCrossRef
20.
go back to reference Zavagno G, De Salvo GL, Scalco G et al (2008) A randomized clinical trial on sentinel lymph node biopsy versus axillary lymph node dissection in breast cancer: results of the Sentinella/GIVOM trial. Ann Surg 247:207–213PubMedCrossRef Zavagno G, De Salvo GL, Scalco G et al (2008) A randomized clinical trial on sentinel lymph node biopsy versus axillary lymph node dissection in breast cancer: results of the Sentinella/GIVOM trial. Ann Surg 247:207–213PubMedCrossRef
21.
go back to reference Haid A, Köberle-Wührer R, Knauer M et al (2002) Morbidity of breast cancer patients following complete axillary dissection or sentinel node biopsy only: a comparative evaluation. Breast Cancer Res Treat 73:31–36PubMedCrossRef Haid A, Köberle-Wührer R, Knauer M et al (2002) Morbidity of breast cancer patients following complete axillary dissection or sentinel node biopsy only: a comparative evaluation. Breast Cancer Res Treat 73:31–36PubMedCrossRef
22.
go back to reference Arnaud S, Houvenaeghel G, Moutardier V et al (2004) Patients’ and surgeons’ perspectives on axillary surgery for breast cancer. Eur J Surg Oncol 30:735–743PubMedCrossRef Arnaud S, Houvenaeghel G, Moutardier V et al (2004) Patients’ and surgeons’ perspectives on axillary surgery for breast cancer. Eur J Surg Oncol 30:735–743PubMedCrossRef
23.
go back to reference Kootstra J, Hoekstra-Weebers JE, Rietman H, de Vries J, Baas PC, Geertzen JH, Hoekstra HJ (2008) Quality of life after sentinel lymph node biopsy or axillary lymph node dissection in stage I/II breast cancer patients: a prospective longitudinal study. Ann Surg Oncol 15:2533–2541PubMedCrossRef Kootstra J, Hoekstra-Weebers JE, Rietman H, de Vries J, Baas PC, Geertzen JH, Hoekstra HJ (2008) Quality of life after sentinel lymph node biopsy or axillary lymph node dissection in stage I/II breast cancer patients: a prospective longitudinal study. Ann Surg Oncol 15:2533–2541PubMedCrossRef
24.
go back to reference Rietman JS, Geertzen JH, Hoekstra HJ, Baas PC, Dolsma WV, de Vries J, Groothoff JW, Eisma WH, Dijkstra PU (2006) Long term treatment related upper limb morbidity and quality of life after sentinel lymph node biopsy for stage I or II breast cancer. Eur J Surg Oncol 32:148–152PubMedCrossRef Rietman JS, Geertzen JH, Hoekstra HJ, Baas PC, Dolsma WV, de Vries J, Groothoff JW, Eisma WH, Dijkstra PU (2006) Long term treatment related upper limb morbidity and quality of life after sentinel lymph node biopsy for stage I or II breast cancer. Eur J Surg Oncol 32:148–152PubMedCrossRef
25.
go back to reference Rietman JS, Dijkstra PU, Geertzen JH, Baas PC, de Vries J, Dolsma WV, Groothoff JW, Eisma WH, Hoekstra HJ (2004) Treatment-related upper limb morbidity 1 year after sentinel lymph node biopsy or axillary lymph node dissection for stage I or II breast cancer. Ann Surg Oncol 11:1018–1024PubMedCrossRef Rietman JS, Dijkstra PU, Geertzen JH, Baas PC, de Vries J, Dolsma WV, Groothoff JW, Eisma WH, Hoekstra HJ (2004) Treatment-related upper limb morbidity 1 year after sentinel lymph node biopsy or axillary lymph node dissection for stage I or II breast cancer. Ann Surg Oncol 11:1018–1024PubMedCrossRef
26.
go back to reference Kootstra JJ, Hoekstra-Weebers JE, Rietman H, de Vries J, Baas PC, Geertzen JH, Hoekstra HJ (2010) A longitudinal comparison of arm morbidity in stage I–II breast cancer patients treated with sentinel lymph node biopsy, sentinel lymph node biopsy followed by completion lymph node dissection, or axillary lymph node dissection. Ann Surg Oncol 17:2384–2394PubMedCrossRef Kootstra JJ, Hoekstra-Weebers JE, Rietman H, de Vries J, Baas PC, Geertzen JH, Hoekstra HJ (2010) A longitudinal comparison of arm morbidity in stage I–II breast cancer patients treated with sentinel lymph node biopsy, sentinel lymph node biopsy followed by completion lymph node dissection, or axillary lymph node dissection. Ann Surg Oncol 17:2384–2394PubMedCrossRef
27.
go back to reference Helms G, Kühn T, Moser L, Remmel E, Kreienberg R (2009) Shoulder–arm morbidity in patients with sentinel node biopsy and complete axillary dissection—data from a prospective randomised trial. Eur J Surg Oncol 35:696–701PubMedCrossRef Helms G, Kühn T, Moser L, Remmel E, Kreienberg R (2009) Shoulder–arm morbidity in patients with sentinel node biopsy and complete axillary dissection—data from a prospective randomised trial. Eur J Surg Oncol 35:696–701PubMedCrossRef
28.
go back to reference Ashikga T, Krag DN, Land SR, Julian TB, Anderson SJ, Brown AM, Skelly JM, Harlow SP, Weaver DL, Mamounas EP, Costantino JP, Wolmark N (2010) Morbidity results from the NSABP B-32 trial comparing sentinel lymph node dissection versus axillary dissection. J Surg Oncol 102:111–118CrossRef Ashikga T, Krag DN, Land SR, Julian TB, Anderson SJ, Brown AM, Skelly JM, Harlow SP, Weaver DL, Mamounas EP, Costantino JP, Wolmark N (2010) Morbidity results from the NSABP B-32 trial comparing sentinel lymph node dissection versus axillary dissection. J Surg Oncol 102:111–118CrossRef
29.
go back to reference Schulze T, Mucke J, Markwardt J, Schlag PM, Bembenek A (2006) Long-term morbidity of patients with early breast cancer after sentinel lymph node biopsy compared to axillary lymph node dissection. J Surg Oncol 93:109–119PubMedCrossRef Schulze T, Mucke J, Markwardt J, Schlag PM, Bembenek A (2006) Long-term morbidity of patients with early breast cancer after sentinel lymph node biopsy compared to axillary lymph node dissection. J Surg Oncol 93:109–119PubMedCrossRef
30.
go back to reference Crane-Okada R, Wascher RA, Elashoff D, Giuliano AE (2008) Long-term morbidity of sentinel node biopsy versus complete axillary dissection for unilateral breast cancer. Ann Surg Oncol 15:1996–2005PubMedCrossRef Crane-Okada R, Wascher RA, Elashoff D, Giuliano AE (2008) Long-term morbidity of sentinel node biopsy versus complete axillary dissection for unilateral breast cancer. Ann Surg Oncol 15:1996–2005PubMedCrossRef
31.
go back to reference McLaughlin SA, Wright MJ, Morris KT, Giron GL, Sampson MR, Brockway JP, Hurley KE, Riedel ER, Van Zee KJ (2008) Prevalence of lymphedema in women with breast cancer 5 years after sentinel lymph node biopsy or axillary dissection: objective measurements. J Clin Oncol 26:5213–5219PubMedCrossRef McLaughlin SA, Wright MJ, Morris KT, Giron GL, Sampson MR, Brockway JP, Hurley KE, Riedel ER, Van Zee KJ (2008) Prevalence of lymphedema in women with breast cancer 5 years after sentinel lymph node biopsy or axillary dissection: objective measurements. J Clin Oncol 26:5213–5219PubMedCrossRef
32.
go back to reference Swenson KK, Nissen MJ, Ceronsky C, Swenson L, Lee MW, Tuttle TM (2002) Comparison of side effects between sentinel lymph node and axillary lymph node dissection for breast cancer. Ann Surg Oncol 9:745–753PubMedCrossRef Swenson KK, Nissen MJ, Ceronsky C, Swenson L, Lee MW, Tuttle TM (2002) Comparison of side effects between sentinel lymph node and axillary lymph node dissection for breast cancer. Ann Surg Oncol 9:745–753PubMedCrossRef
33.
go back to reference Levy EW, Pfalzer LA, Danoff J, Springer BA, McGarvey C, Shieh C, Morehead-Gee A, Gerber LH, Stout NL (2012) Predictors of functional shoulder recovery at 1 and 12 months after breast cancer surgery. Breast Cancer Res Treat 134:315–324PubMedCrossRef Levy EW, Pfalzer LA, Danoff J, Springer BA, McGarvey C, Shieh C, Morehead-Gee A, Gerber LH, Stout NL (2012) Predictors of functional shoulder recovery at 1 and 12 months after breast cancer surgery. Breast Cancer Res Treat 134:315–324PubMedCrossRef
35.
go back to reference Rutgers EJ, Jansen L, Nieweg OE, de Vries J, Schraffordt KH, Kroon BB (1998) Technique of sentinel node biopsy in breast cancer. Eur J Surg Oncol 24:316–319PubMedCrossRef Rutgers EJ, Jansen L, Nieweg OE, de Vries J, Schraffordt KH, Kroon BB (1998) Technique of sentinel node biopsy in breast cancer. Eur J Surg Oncol 24:316–319PubMedCrossRef
37.
go back to reference Green S, Buchbinder R, Forbes A, Bellamy N (1998) A standardized protocol for measurement of range of movement of the shoulder using the Plurimeter-V inclinometer and assessment of its intrarater and interrater reliability. Arthritis Care Res 11:43–52PubMedCrossRef Green S, Buchbinder R, Forbes A, Bellamy N (1998) A standardized protocol for measurement of range of movement of the shoulder using the Plurimeter-V inclinometer and assessment of its intrarater and interrater reliability. Arthritis Care Res 11:43–52PubMedCrossRef
38.
go back to reference van der Ploeg RJ, Fidler V, Oosterhuis HJ (1991) Hand-held myometry: reference values. J Neurol Neurosurg Psychiatry 54:244–247PubMedCrossRef van der Ploeg RJ, Fidler V, Oosterhuis HJ (1991) Hand-held myometry: reference values. J Neurol Neurosurg Psychiatry 54:244–247PubMedCrossRef
39.
go back to reference Mathiowetz V, Weber K, Volland G, Kashman N (1984) Reliability and validity of grip and pinch strength evaluations. J Hand Surg (Am) 9:222–226 Mathiowetz V, Weber K, Volland G, Kashman N (1984) Reliability and validity of grip and pinch strength evaluations. J Hand Surg (Am) 9:222–226
40.
go back to reference Swedborg I, Borg G, Sarnelid M (1981) Somatic sensation and discomfort in the arm of post-mastectomy patients. Scand J Rehabil Med 13:23–29PubMed Swedborg I, Borg G, Sarnelid M (1981) Somatic sensation and discomfort in the arm of post-mastectomy patients. Scand J Rehabil Med 13:23–29PubMed
41.
go back to reference Sitzia J (1995) Volume measurement in lymphoedema treatment: examination of formulae. Eur J Cancer Care (Engl) 4:11–16CrossRef Sitzia J (1995) Volume measurement in lymphoedema treatment: examination of formulae. Eur J Cancer Care (Engl) 4:11–16CrossRef
42.
go back to reference Voogd AC, Ververs JM, Vingerhoets AJ, Roumen RM, Coebergh JW, Crommelin MA (2003) Lymphoedema and reduced shoulder function as indicators of quality of life after axillary lymph node dissection for invasive breast cancer. Br J Surg 90:76–81PubMedCrossRef Voogd AC, Ververs JM, Vingerhoets AJ, Roumen RM, Coebergh JW, Crommelin MA (2003) Lymphoedema and reduced shoulder function as indicators of quality of life after axillary lymph node dissection for invasive breast cancer. Br J Surg 90:76–81PubMedCrossRef
43.
go back to reference Pain SJ, Purushotham AD (2000) Lymphoedema following surgery for breast cancer. Br J Surg 87:1128–1141PubMedCrossRef Pain SJ, Purushotham AD (2000) Lymphoedema following surgery for breast cancer. Br J Surg 87:1128–1141PubMedCrossRef
44.
go back to reference Wernicke AG, Goodman RL, Turner BC, Komarnicky LT, Curran WJ, Christos PJ, Khan I, Vandris K, Parashar B, Nori D, Chao KSC (2011) A 10-year follow-up of treatment outcomes in patients with early stage breast cancer and clinically negative axillary nodes treated with tangential breast irradiation following sentinel lymph node dissection or axillary clearance. Breast Cancer Res Treat 125:893–902PubMedCrossRef Wernicke AG, Goodman RL, Turner BC, Komarnicky LT, Curran WJ, Christos PJ, Khan I, Vandris K, Parashar B, Nori D, Chao KSC (2011) A 10-year follow-up of treatment outcomes in patients with early stage breast cancer and clinically negative axillary nodes treated with tangential breast irradiation following sentinel lymph node dissection or axillary clearance. Breast Cancer Res Treat 125:893–902PubMedCrossRef
45.
go back to reference Petrek JA, Senie RT, Peters M, Rosen PP (2001) Lymphedema in a cohort of breast carcinoma survivors 20 years after diagnosis. Cancer 92:1368–1377PubMedCrossRef Petrek JA, Senie RT, Peters M, Rosen PP (2001) Lymphedema in a cohort of breast carcinoma survivors 20 years after diagnosis. Cancer 92:1368–1377PubMedCrossRef
46.
go back to reference Husen M, Paaschburg B, Flyger HL (2006) Two-step axillary operation increases risk of arm morbidity in breast cancer patients. Breast 15:620–628PubMedCrossRef Husen M, Paaschburg B, Flyger HL (2006) Two-step axillary operation increases risk of arm morbidity in breast cancer patients. Breast 15:620–628PubMedCrossRef
47.
go back to reference Fleissig A, Fallowfield LJ, Langridge CI, Johnson L, Newcombe RG, Dixon JM, Kissin M, Mansel RE (2006) Post-operative arm morbidity and quality of life. Results of the ALMANAC randomised trial comparing sentinel node biopsy with standard axillary treatment in the management of patients with early breast cancer. Breast Cancer Res Treat 95(3):279–293PubMedCrossRef Fleissig A, Fallowfield LJ, Langridge CI, Johnson L, Newcombe RG, Dixon JM, Kissin M, Mansel RE (2006) Post-operative arm morbidity and quality of life. Results of the ALMANAC randomised trial comparing sentinel node biopsy with standard axillary treatment in the management of patients with early breast cancer. Breast Cancer Res Treat 95(3):279–293PubMedCrossRef
48.
go back to reference Yap KP, McCready DR, Narod S, Manchul LA, Trudeau M, Fyles A (2003) Factors influencing arm and axillary symptoms after treatment for node negative breast carcinoma. Cancer 97(6):1369–1375PubMedCrossRef Yap KP, McCready DR, Narod S, Manchul LA, Trudeau M, Fyles A (2003) Factors influencing arm and axillary symptoms after treatment for node negative breast carcinoma. Cancer 97(6):1369–1375PubMedCrossRef
49.
go back to reference Albert US, Koller M, Kopp I, Lorenz W, Schulz KD, Wagner U (2006) Early self-reported impairments in arm functioning of primary breast cancer patients predict late side effects of axillary lymph node dissection: results from a population-based cohort study. Breast Cancer Res Treat 100(3):285–292PubMedCrossRef Albert US, Koller M, Kopp I, Lorenz W, Schulz KD, Wagner U (2006) Early self-reported impairments in arm functioning of primary breast cancer patients predict late side effects of axillary lymph node dissection: results from a population-based cohort study. Breast Cancer Res Treat 100(3):285–292PubMedCrossRef
Metadata
Title
A longitudinal study of shoulder and arm morbidity in breast cancer survivors 7 years after sentinel lymph node biopsy or axillary lymph node dissection
Authors
Jan J. Kootstra
Pieter U. Dijkstra
Hans Rietman
Jaap de Vries
Peter Baas
Jan H. B. Geertzen
Harald J. Hoekstra
Josette E. H. M. Hoekstra-Weebers
Publication date
01-05-2013
Publisher
Springer US
Published in
Breast Cancer Research and Treatment / Issue 1/2013
Print ISSN: 0167-6806
Electronic ISSN: 1573-7217
DOI
https://doi.org/10.1007/s10549-013-2509-y

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