Supportive Care in Cancer

, Volume 26, Issue 9, pp 3277–3287 | Cite as

Prospective study of shoulder strength, shoulder range of motion, and lymphedema in breast cancer patients from pre-surgery to 5 years after ALND or SLNB

  • Roser Belmonte
  • Monique Messaggi-Sartor
  • Montse Ferrer
  • Angels Pont
  • Ferran Escalada
Original Article



Determine the changes in shoulder strength, shoulder range of motion, and arm volume in breast cancer patients treated with sentinel lymph node biopsy (SLNB) or axillary lymph node dissection (ALND)


Sixty-eight SLNB and 44 ALND patients were followed up from pre-surgery to 5 years after surgery. Primary outcomes were the differences between affected and non-affected sides for the following: shoulder strength measured by dynamometry, shoulder range of motion measured by goniometry, and lymphedema measured by volume. As a secondary outcome, health-related quality of life (HRQL) was assessed by the Short Form-36 Health Survey (SF-36) and the Functional Assessment of Cancer Therapy for breast cancer (FACT-B+4) questionnaires. Changes over time were tested for SLNB and ALND using univariate repeated measures analysis of variance. Generalized estimating equation models were constructed to assess the effect of SLNB and ALND over time.


After 5 years, the ALND group had significant loss of strength for internal rotators (1.39 kg, p = 0.001) and significant arm volume increase (132.45 mL, p = 0.031). The ALND group had a greater number of patients with clinically relevant internal rotator strength loss (38.7 vs. 13.6%, p = 0.012) and a greater number of lymphedema requiring treatment (33.3 vs. 3.4%, p < 0.001) than the SLNB group. A loss of strength for shoulder external rotators, shoulder range of motion, and HRQL in physical and arm domains persisted at 5 years in both SLNB and ALND groups.


These results could help understand and plan the prevention, needs, and long-term care of breast cancer patients.


Breast cancer Lymphedema Shoulder Quality of life 


Funding information

This study was sponsored by the hospital where authors work and partially from a grant of Instituto de Salud Carlos III - ISCIII FEDER (PI/06/90070) and one from DIUE of Generalitat de Catalunya (2014 SGR 748); there was no other external financial support.

Compliance with ethical standards

The Research Ethics Committee approved the study and it was conducted in accordance with the Declaration of Helsinki. Written informed consent was obtained from participants before being included.

Conflict of interest

The authors declare that they have no conflict of interest.

Supplementary material

520_2018_4186_MOESM1_ESM.docx (32 kb)
ESM 1 (DOCX 31 kb)
520_2018_4186_MOESM2_ESM.docx (53 kb)
ESM 2 (DOCX 53 kb)


  1. 1.
    Lu W, Cui Y, Zheng Y, Gu K, Cai H, Li Q, Zheng W, Shu XO (2007) Impact of newly diagnosed breast cancer on HRQL among Chinese women. Breast Cancer Res Treat 102:201–210. CrossRefPubMedGoogle Scholar
  2. 2.
    Mols F, Vingerhoets AJJM, Coebergh JW, van de Poll-Franse LV (2005) HRQL among long-term breast cancer survivors: a systematic review. Eur J Cancer 41:2613–2619. CrossRefPubMedGoogle Scholar
  3. 3.
    Koch L, Jansen L, Herrmann A, Stegmaier C, Holleczek B, Singer S, Brenner H, Arndt V (2013) HRQL in long-term breast cancer survivors—a 10-year longitudinal population-based study. Acta Oncol 52:1119–1128. CrossRefPubMedGoogle Scholar
  4. 4.
    Sato F, Arinaga Y, Sato N, Ishida T, Ohuchi N (2016) The perioperative educational program for improving upper arm dysfunction in patients with breast cancer at 1-year follow-up: a prospective, controlled trial. Tohoku J Exp Med 238:229–236. CrossRefPubMedGoogle Scholar
  5. 5.
    Montazeri A, Vahdaninia M, Harirchi I et al (2008) HRQL in patients with breast cancer before and after diagnosis: an eighteen months follow-up study. BMC Cancer 8:330. CrossRefPubMedPubMedCentralGoogle Scholar
  6. 6.
    Fleissig A, Fallowfield LJ, Langridge CI, Johnson L, Newcombe RG, Dixon JM, Kissin M, Mansel RE (2006) Post-operative arm morbidity and HRQL. 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 95:279–293. CrossRefPubMedGoogle Scholar
  7. 7.
    Rietman JS, Dijkstra PU, Debreczeni R, Geertzen JHB, Robinson DPH, de Vries J (2004) Impairments, disabilities and health related HRQL after treatment for breast cancer: a follow-up study 2.7 years after surgery. Disabil Rehabil 26:78–84. CrossRefPubMedGoogle Scholar
  8. 8.
    Hayes SC, Rye S, Battistutta D et al (2010) Upper-body morbidity following breast cancer treatment is common, may persist longer-term and adversely influences HRQL. Heal Qual Life Outcomes 8:92. CrossRefGoogle Scholar
  9. 9.
    Sagen A, Karesen R, Skaane P, Risberg MA (2009) Validity for the simplified water displacement instrument to measure arm lymphedema as a result of breast cancer surgery. Arch Phys Med Rehabil 90:803–809. CrossRefPubMedGoogle Scholar
  10. 10.
    DiSipio T, Rye S, Newman B, Hayes S (2013) Incidence of unilateral arm lymphoedema after breast cancer: a systematic review and meta-analysis. Lancet Oncol 14:500–515. CrossRefPubMedGoogle Scholar
  11. 11.
    Nesvold IL, Reinertsen KV, Fosså SD, Dahl AA (2011) The relation between arm/shoulder problems and HRQL in breast cancer survivors: a cross-sectional and longitudinal study. J Cancer Surviv 5:62–72. CrossRefPubMedGoogle Scholar
  12. 12.
    Lee TS, Kilbreath SL, Refshauge KM, Pendlebury SC, Beith JM, Lee MJ (2008) HRQL of women treated with radiotherapy for breast cancer. Support Care Cancer 16:399–405. CrossRefPubMedGoogle Scholar
  13. 13.
    Lee TS, Kilbreath SL, Refshauge KM, Herbert RD, Beith JM (2008) Prognosis of the upper limb following surgery and radiation for breast cancer. Breast Cancer Res Treat 110:19–37. CrossRefPubMedGoogle Scholar
  14. 14.
    Kootstra JJ, Dijkstra PU, Rietman H, de Vries J, Baas P, Geertzen JHB, Hoekstra HJ, Hoekstra-Weebers JEHM (2013) A longitudinal study of shoulder and arm morbidity in breast cancer survivors 7 years after sentinel lymph node biopsy or axillary lymph node dissection. Breast Cancer Res Treat 139:125–134. CrossRefPubMedGoogle Scholar
  15. 15.
    Helms G, Kuhn T, Moser L et al (2009) Shoulder-arm morbidity in patients with sentinel node biopsy and complete axillary dissection—data from a prospective randomised trial. Eur J Surg Oncol 35:696–701. CrossRefPubMedGoogle Scholar
  16. 16.
    Hidding JT, Beurskens CHG, van der Wees PJ, van Laarhoven HWM, Nijhuis-van der Sanden MWG (2014) Treatment related impairments in arm and shoulder in patients with breast cancer: a systematic review. PLoS One 9:e96748. CrossRefPubMedPubMedCentralGoogle Scholar
  17. 17.
    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 93:109–119. CrossRefPubMedGoogle Scholar
  18. 18.
    McLaughlin SA, Wright MJ, Morris KT et al (2008) Prevalence of lymphedema in women with breast cancer 5 years after sentinel lymph node biopsy or axillary dissection: objective measurements. J Clin Oncol 26:5213–5219. CrossRefPubMedPubMedCentralGoogle Scholar
  19. 19.
    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 15:1996–2005. CrossRefPubMedGoogle Scholar
  20. 20.
    Belmonte R, Garin O, Segura M, Pont A, Escalada F, Ferrer M (2012) Quality-of-life impact of sentinel lymph node biopsy versus axillary lymph node dissection in breast cancer patients. Value Health 15:907–915. CrossRefPubMedGoogle Scholar
  21. 21.
    Purushotham AD, Upponi S, Klevesath MB et al (2005) Morbidity after sentinel lymph node biopsy in primary breast cancer: results from a randomized controlled trial. J Clin Oncol 23:4312–4321. CrossRefPubMedGoogle Scholar
  22. 22.
    Rietman JS, Geertzen JHB, Hoekstra HJ, Baas P, Dolsma WV, de Vries J, Groothoff JW, Eisma WH, Dijkstra PU (2006) Long term treatment related upper limb morbidity and HRQL after sentinel lymph node biopsy for stage I or II breast cancer. Eur J Surg Oncol 32:148–152. CrossRefPubMedGoogle Scholar
  23. 23.
    De Gournay E, Guyomard A, Coutant C et al (2013) Impact of sentinel node biopsy on long-term HRQL in breast cancer patients. Br J Cancer 109:2783–2791. CrossRefPubMedPubMedCentralGoogle Scholar
  24. 24.
    Runowicz CD, Leach CR, Henry NL, Henry KS, Mackey HT, Cowens-Alvarado RL, Cannady RS, Pratt-Chapman ML, Edge SB, Jacobs LA, Hurria A, Marks LB, LaMonte SJ, Warner E, Lyman GH, Ganz PA (2016) American Cancer Society/American Society of Clinical Oncology Breast Cancer Survivorship Care Guideline. J Clin Oncol 34:611–635. CrossRefPubMedGoogle Scholar
  25. 25.
    Kvale EA, Huang C-HS, Meneses KM, Demark-Wahnefried W, Bae S, Azuero CB, Rocque GB, Bevis KS, Ritchie CS (2016) Patient-centered support in the survivorship care transition: outcomes from the patient-owned survivorship care plan intervention. Cancer 122:3232–3242. CrossRefPubMedGoogle Scholar
  26. 26.
    Gass J, Dupree B, Pruthi S, Radford D, Wapnir I, Antoszewska R, Curtis A, Johnson N (2016) Breast cancer survivorship: why, what and when? Ann Surg Oncol 23:3162–3167. CrossRefPubMedGoogle Scholar
  27. 27.
    Khatcheressian JL, Hurley P, Bantug E, Esserman LJ, Grunfeld E, Halberg F, Hantel A, Henry NL, Muss HB, Smith TJ, Vogel VG, Wolff AC, Somerfield MR, Davidson NE, American Society of Clinical Oncology (2013) Breast cancer follow-up and management after primary treatment: American Society of Clinical Oncology clinical practice guideline update. J Clin Oncol 31:961–965. CrossRefPubMedGoogle Scholar
  28. 28.
    Grunfeld E, Julian JA, Pond G, Maunsell E, Coyle D, Folkes A, Joy AA, Provencher L, Rayson D, Rheaume DE, Porter GA, Paszat LF, Pritchard KI, Robidoux A, Smith S, Sussman J, Dent S, Sisler J, Wiernikowski J, Levine MN (2011) Evaluating survivorship care plans: results of a randomized, clinical trial of patients with breast cancer. J Clin Oncol 29:4755–4762. CrossRefPubMedGoogle Scholar
  29. 29.
    Khan F, Amatya B, Ng L, Demetrios M, Zhang NY, Turner-Stokes L, Cochrane Breast Cancer Group (2012) Multidisciplinary rehabilitation for follow-up of women treated for breast cancer. Cochrane Database Syst Rev 12:CD009553. PubMedCrossRefGoogle Scholar
  30. 30.
    Pusic AL, Cemal Y, Albornoz C, Klassen A, Cano S, Sulimanoff I, Hernandez M, Massey M, Cordeiro P, Morrow M, Mehrara B (2013) HRQL among breast cancer patients with lymphedema: a systematic review of patient-reported outcome instruments and outcomes. J Cancer Surviv 7:83–92. CrossRefPubMedGoogle Scholar
  31. 31.
    Donatelli R, Ellenbecker TS, Ekedahl SR, Wilkes JS, Kocher K, Adam J (2000) Assessment of shoulder strength in professional baseball pitchers. J Orthop Sports Phys Ther 30:544–551. CrossRefPubMedGoogle Scholar
  32. 32.
    De Lisa JA (1993) Rehabilitation medicine, Chapter 4 Clinical evaluation, 2nd edn. JB Lippincott Company Philadelphia. ISBN0-397-51262-7Google Scholar
  33. 33.
    Taylor R, Jayasinghe UW, Koelmeyer L, Ung O, Boyages J (2006) Reliability and validity of arm volume measurements for assessment of lymphedema. Phys Ther 86:205–214PubMedGoogle Scholar
  34. 34.
    Alonso J, Regidor E, Barrio G, Prieto L, Rodríguez C, de la Fuente L (1998) Population reference values of the Spanish version of the Health Questionnaire SF-36. Med Clin 111:410–416Google Scholar
  35. 35.
    Vilagut G, Valderas JM, Ferrer M et al (2008) Interpretation of SF-36 and SF-12 questionnaires in Spain: physical and mental components. Med Clin 130:726–735CrossRefGoogle Scholar
  36. 36.
    Brady MJ, Cella DF, Mo F, Bonomi AE, Tulsky DS, Lloyd SR, Deasy S, Cobleigh M, Shiomoto G (1997) Reliability and validity of the Functional Assessment of Cancer Therapy-Breast quality-of-life instrument. J Clin Oncol 15:974–986CrossRefPubMedGoogle Scholar
  37. 37.
    Coster S, Poole K, Fallowfield LJ (2001) The validation of a HRQL scale to assess the impact of arm morbidity in breast cancer patients post-operatively. Breast Cancer Res Treat 68:273–282CrossRefPubMedGoogle Scholar
  38. 38.
    Belmonte Martinez R, Garin Boronat O, Segura Badia M et al Functional Assessment of Cancer Therapy Questionnaire for Breast Cancer (FACT-B+4). Spanish version validation. Med Clin 137:685–688.
  39. 39.
    Hislop HJ, Montgomery J (2007) Techniques of manual examination, Daniels & Wortinghan’s muscle testing, 8th edn. Saunders Elsevier, St. LouisGoogle Scholar
  40. 40.
    Sagen A, Kaaresen R, Sandvik L, Thune I, Risberg MA (2014) Upper limb physical function and adverse effects after breast cancer surgery: a prospective 2.5-year follow-up study and preoperative measures. Arch Phys Med Rehabil 95:875–881. CrossRefPubMedGoogle Scholar
  41. 41.
    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 349:546–553. CrossRefPubMedGoogle Scholar
  42. 42.
    Langer I, Guller U, Berclaz G, Koechli OR, Schaer G, Fehr MK, Hess T, Oertli D, Bronz L, Schnarwyler B, Wight E, Uehlinger U, Infanger E, Burger D, Zuber M (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 245:452–461. CrossRefPubMedPubMedCentralGoogle Scholar
  43. 43.
    Peintinger F, Reitsamer R, Stranzl H, Ralph G (2003) Comparison of HRQL and arm complaints after axillary lymph node dissection vs sentinel lymph node biopsy in breast cancer patients. Br J Cancer 89:648–652. CrossRefPubMedPubMedCentralGoogle Scholar
  44. 44.
    Mansel RE, Fallowfield L, 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 98:599–609. CrossRefPubMedGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2018

Authors and Affiliations

  1. 1.Hospital Mar-Esperança, Parc de Salut MarBarcelonaSpain
  2. 2.Universitat Autònoma de BarcelonaBellaterraSpain
  3. 3.IMIM (Hospital del Mar Medical Research Institute)BarcelonaSpain
  4. 4.CIBER en Epidemiología y Salud Pública, CIBERESPMadridSpain

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