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Radiation therapy targets and the risk of breast cancer-related lymphedema: a systematic review and network meta-analysis

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An Erratum to this article was published on 09 February 2017

Abstract

Purpose

New indications have been found for regional nodal irradiation (RNI) in breast cancer treatment, yet the relationship of RNI and lymphedema risk is uncertain. We sought to determine the association of RNI and lymphedema.

Methods

We searched MEDLINE, EMBASE, and Scopus for articles in English on humans published from 1995 to 2015, using search terms breast neoplasm, treatment, and morbidity. Two investigators independently selected articles and extracted information, including manuscripts reporting incidence of lymphedema by radiation targets. Meta-analyses, review papers, case–control studies, matched-pair studies, repetitive datasets, and retrospective studies were excluded. A total of 2399 abstracts were identified and 323 corresponding articles reviewed. Twenty-one studies met inclusion criteria. Data were pooled using a random effects mixed model. Network meta-analyses were performed to determine the association of radiation targets alone and radiation targets plus extent of axillary surgery on incidence of lymphedema.

Results

The addition of RNI to breast/CW irradiation was associated with an increased incidence of lymphedema (OR 2.85; 95% CI 1.24–6.55). In patients treated with sentinel lymph node biopsy or axillary sampling, there was no association of lymphedema with the addition of RNI to breast/CW irradiation (OR 1.58; 95% CI 0.54–4.66; pooled incidence 5.7 and 4.1%, respectively). Among patients treated with axillary lymph node dissection (ALND), treatment with RNI in addition to breast/CW radiation was associated with a significantly higher risk of lymphedema (OR 2.74; 95% CI 1.38–5.44; pooled incidence 18.2 and 9.4%, respectively).

Conclusions

RNI is associated with a significantly higher risk of lymphedema than irradiation of the breast/CW, particularly after ALND.

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References

  1. Deutsch M, Land S, Begovic M, Sharif S (2008) The incidence of arm edema in women with breast cancer randomized on the National Surgical Adjuvant Breast and Bowel Project study B-04 to radical mastectomy versus total mastectomy and radiotherapy versus total mastectomy alone. Int J Radiat Oncol Biol Phys 70(4):1020–1024. doi:10.1016/j.ijrobp.2007.07.2376

    Article  PubMed  Google Scholar 

  2. Kwan W, Jackson J, Weir LM, Dingee C, McGregor G, Olivotto IA (2002) Chronic arm morbidity after curative breast cancer treatment: prevalence and impact on quality of life. J Clin Oncol 20(20):4242–4248

    Article  PubMed  Google Scholar 

  3. Heiney SP, McWayne J, Cunningham JE, Hazlett LJ, Parrish RS, Bryant LH, Vitoc C, Jansen K (2007) Quality of life and lymphedema following breast cancer. Lymphology 40(4):177–184

    CAS  PubMed  Google Scholar 

  4. Jager G, Doller W, Roth R (2006) Quality-of-life and body image impairments in patients with lymphedema. Lymphology 39(4):193–200

    CAS  PubMed  Google Scholar 

  5. Schipper H, Clinch J, McMurray A, Levitt M (1984) Measuring the quality of life of cancer patients: the Functional Living Index-Cancer: development and validation. J Clin Oncol 2(5):472–483

    Article  CAS  PubMed  Google Scholar 

  6. Földi M (2012) Textbook of Lymphology For Physicians and Lymphedema Therapists. Mosby Inc,

  7. Klernas P, Kristjanson LJ, Johansson K (2010) Assessment of quality of life in lymphedema patients: validity and reliability of the Swedish version of the Lymphedema Quality of Life Inventory (LQOLI). Lymphology 43(3):135–145

    CAS  PubMed  Google Scholar 

  8. Cidon EU, Perea C, Lopez-Lara F (2011) Life after breast cancer: dealing with lymphoedema. Clin Med Insights Oncol 5:9–14. doi:10.4137/CMO.S6389

    Article  PubMed  PubMed Central  Google Scholar 

  9. Stamatakos M, Stefanaki C, Kontzoglou K (2011) Lymphedema and breast cancer: a review of the literature. Breast Cancer 18(3):174–180. doi:10.1007/s12282-010-0246-1

    Article  PubMed  Google Scholar 

  10. Pusic AL, Cemal Y, Albornoz C, Klassen A, Cano S, Sulimanoff I, Hernandez M, Massey M, Cordeiro P, Morrow M, Mehrara B (2013) Quality of life among breast cancer patients with lymphedema: a systematic review of patient-reported outcome instruments and outcomes. J Cancer Surviv 7(1):83–92. doi:10.1007/s11764-012-0247-5

    Article  PubMed  Google Scholar 

  11. McWayne J, Heiney SP (2005) Psychologic and social sequelae of secondary lymphedema: a review. Cancer 104(3):457–466. doi:10.1002/cncr.21195

    Article  PubMed  Google Scholar 

  12. Engel J, Kerr J, Schlesinger-Raab A, Sauer H, Holzel D (2003) Axilla surgery severely affects quality of life: results of a 5-year prospective study in breast cancer patients. Breast Cancer Res Treat 79(1):47–57

    Article  PubMed  Google Scholar 

  13. Janz NK, Mujahid M, Chung LK, Lantz PM, Hawley ST, Morrow M, Schwartz K, Katz SJ (2007) Symptom experience and quality of life of women following breast cancer treatment. J Womens Health (Larchmt) 16(9):1348–1361. doi:10.1089/jwh.2006.0255

    Article  Google Scholar 

  14. Petrek JA, Senie RT, Peters M, Rosen PP (2001) Lymphedema in a cohort of breast carcinoma survivors 20 years after diagnosis. Cancer 92(6):1368–1377

    Article  CAS  PubMed  Google Scholar 

  15. Shih YC, Xu Y, Cormier JN, Giordano S, Ridner SH, Buchholz TA, Perkins GH, Elting LS (2009) Incidence, treatment costs, and complications of lymphedema after breast cancer among women of working age: a 2-year follow-up study. J Clin Oncol 27(12):2007–2014. doi:10.1200/JCO.2008.18.3517

    Article  PubMed  Google Scholar 

  16. Armer JM, Whitman M (2002) The problem of lymphedema following breast cancer treatment: prevlance, symptoms, and self-management. Lymphology 35:153–159

    Google Scholar 

  17. Newman ML, Brennan M, Passik S (1996) Lymphedema complicated by pain and psychological distress: a case with complex treatment needs. J Pain Symptom Manag 12(6):376–379

    Article  CAS  Google Scholar 

  18. Krag DN, Anderson SJ, Julian TB, Brown AM, Harlow SP, Costantino JP, Ashikaga T, Weaver DL, Mamounas EP, Jalovec LM, Frazier TG, Noyes RD, Robidoux A, Scarth HM, Wolmark N (2010) Sentinel-lymph-node resection compared with conventional axillary-lymph-node dissection in clinically node-negative patients with breast cancer: overall survival findings from the NSABP B-32 randomised phase 3 trial. Lancet Oncol 11(10):927–933. doi:10.1016/S1470-2045(10)70207-2

    Article  PubMed  PubMed Central  Google Scholar 

  19. Giuliano AE, Hunt KK, Ballman KV, Beitsch PD, Whitworth PW, Blumencranz PW, Leitch AM, Saha S, McCall LM, Morrow M (2011) Axillary dissection vs no axillary dissection in women with invasive breast cancer and sentinel node metastasis: a randomized clinical trial. JAMA 305(6):569–575. doi:10.1001/jama.2011.90

    Article  CAS  PubMed  Google Scholar 

  20. Donker M, van Tienhoven G, Straver ME, Meijnen P, van de Velde CJ, Mansel RE, Cataliotti L, Westenberg AH, Klinkenbijl JH, Orzalesi L, Bouma WH, van der Mijle HC, Nieuwenhuijzen GA, Veltkamp SC, Slaets L, Duez NJ, de Graaf PW, van Dalen T, Marinelli A, Rijna H, Snoj M, Bundred NJ, Merkus JW, Belkacemi Y, Petignat P, Schinagl DA, Coens C, Messina CG, Bogaerts J, Rutgers EJ (2014) Radiotherapy or surgery of the axilla after a positive sentinel node in breast cancer (EORTC 10981-22023 AMAROS): a randomised, multicentre, open-label, phase 3 non-inferiority trial. Lancet Oncol 15(12):1303–1310. doi:10.1016/S1470-2045(14)70460-7

    Article  PubMed  PubMed Central  Google Scholar 

  21. Whelan TJ, Olivotto IA, Parulekar WR, Ackerman I, Chua BH, Nabid A, Vallis KA, White JR, Rousseau P, Fortin A, Pierce LJ, Manchul L, Chafe S, Nolan MC, Craighead P, Bowen J, McCready DR, Pritchard KI, Gelmon K, Murray Y, Chapman JAW, Chen BE, Levine MN (2015) Regional nodal irradiation in early-stage breast cancer. N Engl J Med 373(4):307–316. doi:10.1056/NEJMoa1415340

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  22. Poortmans PM, Collette S, Kirkove C, Van Limbergen E, Budach V, Struikmans H, Collette L, Fourquet A, Maingon P, Valli M, De Winter K, Marnitz S, Barillot I, Scandolaro L, Vonk E, Rodenhuis C, Marsiglia H, Weidner N, van Tienhoven G, Glanzmann C, Kuten A, Arriagada R, Bartelink H, Van den Bogaert W, Oncology ER, Breast Cancer G (2015) Internal mammary and medial supraclavicular irradiation in breast cancer. N Engl J Med 373(4):317–327. doi:10.1056/NEJMoa1415369

    Article  CAS  PubMed  Google Scholar 

  23. Armer JM, Stewart BR (2010) Post-breast cancer lymphedema: incidence increases from 12 to 30 to 60 months. Lymphology 43(3):118–127

    CAS  PubMed  PubMed Central  Google Scholar 

  24. Mills EJ, Thorlund K, Ioannidis JP (2013) Demystifying trial networks and network meta-analysis. BMJ 346:f2914. doi:10.1136/bmj.f2914

    Article  PubMed  Google Scholar 

  25. Medicine CfE-B (2009) Oxford Centre for Evidence-based Medicine—Levels of Evidence. http://www.cebm.net/oxford-centre-evidence-based-medicine-levels-evidence-march-2009/. Accessed 8 June 2016

  26. Ahmed RL, Schmitz KH, Prizment AE, Folsom AR (2011) Risk factors for lymphedema in breast cancer survivors, the Iowa Women’s Health Study. Breast Cancer Res Treat 130(3):981–991. doi:10.1007/s10549-011-1667-z

    Article  PubMed  PubMed Central  Google Scholar 

  27. Chafe S, Moughan J, McCormick B, Wong J, Pass H, Rabinovitch R, Arthur DW, Petersen I, White J, Vicini FA (2013) Late toxicity and patient self-assessment of breast appearance/satisfaction on RTOG 0319: a phase 2 trial of 3-dimensional conformal radiation therapy-accelerated partial breast irradiation following lumpectomy for stages I and II breast cancer. Int J Radiat Oncol Biol Phys 86(5):854–859. doi:10.1016/j.ijrobp.2013.04.005

    Article  PubMed  Google Scholar 

  28. Chen D, Lai L, Duan C, Yan M, Xing M, Chen J, Zhang F (2014) Conservative surgery plus axillary radiotherapy vs. modified radical mastectomy in patients with stage i breast cancer. Clin Breast Cancer 14(1):e10–e13. doi:10.1016/j.clbc.2013.09.007

    Article  PubMed  Google Scholar 

  29. Galecki JHA, Bujko K, Grudzien-Kowalska M, Hicer-Grzenkowicz J, Zalucki W, Niwinska A, Kukolowicz P, Michalski W (2007) Preliminary results of adjuvant radiotherapy in breast cancer patients using a shortened overall treatment time-a population study. Nowotw J Oncol 57(1):7e–15e

    Google Scholar 

  30. Gartner R, Mejdahl MK, Andersen KG, Ewertz M, Kroman N (2014) Development in self-reported arm-lymphedema in Danish women treated for early-stage breast cancer in 2005 and 2006-a nationwide follow-up study. Breast 23(4):445–452. doi:10.1016/j.breast.2014.03.001

    Article  PubMed  Google Scholar 

  31. Haviland JS, Owen JR, Dewar JA, Agrawal RK, Barrett J, Barrett-Lee PJ, Dobbs HJ, Hopwood P, Lawton PA, Magee BJ, Mills J, Simmons S, Sydenham MA, Venables K, Bliss JM, Yarnold JR, Group ST (2013) The UK Standardisation of Breast Radiotherapy (START) trials of radiotherapy hypofractionation for treatment of early breast cancer: 10-year follow-up results of two randomised controlled trials. Lancet Oncol 14(11):1086–1094. doi:10.1016/S1470-2045(13)70386-3

    Article  PubMed  Google Scholar 

  32. Hojris I, Andersen J, Overgaard M, Overgaard J (2000) Late treatment-related morbidity in breast cancer patients randomized to postmastectomy radiotherapy and systemic treatment versus systemic treatment alone. Acta Oncol 39(3):355–372

    Article  CAS  PubMed  Google Scholar 

  33. Johansen J, Overgaard J, Blichert-Toft M, Overgaard M (2000) Treatment of morbidity associated with the management of the axilla in breast-conserving therapy. Acta Oncol 39(3):349–354

    Article  CAS  PubMed  Google Scholar 

  34. Johansson KIC, Albertsson M, Ekdahl C (2001) Arm lymphoedema, shoulder mobility and muscle strength after breast cancer treatment-a prospective 2-year study. Adv Physiother 3:55–66

    Google Scholar 

  35. Liljegren G, Holmberg L (1997) Arm morbidity after sector resection and axillary dissection with or without postoperative radiotherapy in breast cancer stage I. Results from a randomised trial. Uppsala-Orebro Breast Cancer Study Group. Eur J Cancer 33(2):193–199

    Article  CAS  PubMed  Google Scholar 

  36. Lucci A, McCall LM, Beitsch PD, Whitworth PW, Reintgen DS, Blumencranz PW, Leitch AM, Saha S, Hunt KK, Giuliano AE (2007) Surgical complications associated with sentinel lymph node dissection (SLND) plus axillary lymph node dissection compared with SLND alone in the American College of Surgeons Oncology Group Trial Z0011. J Clin Oncol 25(24):3657–3663. doi:10.1200/JCO.2006.07.4062

    Article  PubMed  Google Scholar 

  37. Morgan DA, Berridge J, Blamey RW (2002) Postoperative radiotherapy following mastectomy for high-risk breast cancer. A randomised trial. AEur J Cancer 38(8):1107–1110

    CAS  Google Scholar 

  38. Olson JA Jr, McCall LM, Beitsch P, Whitworth PW, Reintgen DS, Blumencranz PW, Leitch AM, Saha S, Hunt KK, Giuliano AE (2008) Impact of immediate versus delayed axillary node dissection on surgical outcomes in breast cancer patients with positive sentinel nodes: results from American College of Surgeons Oncology Group Trials Z0010 and Z0011. J Clin Oncol 26(21):3530–3535. doi:10.1200/JCO.2007.15.5630

    Article  PubMed  Google Scholar 

  39. Ragaz J, Jackson SM, Le N, Plenderleith IH, Spinelli JJ, Basco VE, Wilson KS, Knowling MA, Coppin CM, Paradis M, Coldman AJ, Olivotto IA (1997) Adjuvant radiotherapy and chemotherapy in node-positive premenopausal women with breast cancer. N Engl J Med 337(14):956–962. doi:10.1056/NEJM199710023371402

    Article  CAS  PubMed  Google Scholar 

  40. Tausch C, Baege A, Dietrich D, Vergin I, Heuer H, Heusler RH, Rageth C (2013) Can axillary reverse mapping avoid lymphedema in node positive breast cancer patients? Eur J Surg Oncol 39(8):880–886. doi:10.1016/j.ejso.2013.05.009

    Article  CAS  PubMed  Google Scholar 

  41. Vishwanathan N, Bhaskar N, Supe SS, Swamy K, Ravichandran R, Kannan V, Ramesh C (1998) Role of electron beam treatment in postoperative management of carcinoma of the breast. Indian J Cancer 35(1):1–9

    CAS  PubMed  Google Scholar 

  42. Warren LEG, Miller CL, Horick N, Skolny MN, Jammallo LS, Sadek BT, Shenouda MN, O’Toole JA, Macdonald SM, Specht MC, Taghian AG (2014) The impact of radiation therapy on the risk of lymphedema after treatment for breast cancer: a prospective cohort study. Int J Radiat Oncol Biol Phys 88(3):565–571. doi:10.1016/j.ijrobp.2013.11.232

    Article  PubMed  PubMed Central  Google Scholar 

  43. Warren LE, Miller CL, Horick N, Skolny MN, Jammallo LS, Sadek BT, Shenouda MN, O’Toole JA, MacDonald SM, Specht MC, Taghian AG (2014) The impact of radiation therapy on the risk of lymphedema after treatment for breast cancer: a prospective cohort study. Int J Radiat Oncol Biol Phys 88(3):565–571. doi:10.1016/j.ijrobp.2013.11.232

    Article  PubMed  PubMed Central  Google Scholar 

  44. Mamounas EP, Anderson SJ, Dignam JJ, Bear HD, Julian TB, Geyer CE Jr, Taghian A, Wickerham DL, Wolmark N (2012) Predictors of locoregional recurrence after neoadjuvant chemotherapy: results from combined analysis of National Surgical Adjuvant Breast and Bowel Project B-18 and B-27. J Clin Oncol 30(32):3960–3966. doi:10.1200/JCO.2011.40.8369

    Article  PubMed  PubMed Central  Google Scholar 

  45. Oncology AfCTi (2015) Comparison of Axillary Lymph Node Dissection with Axillary Radiation for Patients with Node-Positive Breast Cancer Treated with Chemotherapy. https://clinicaltrials.gov/ct2/show/NCT01901094. Accessed 14 Dec 2015

  46. Jagsi R, Chadha M, Moni J, Ballman K, Laurie F, Buchholz TA, Giuliano A, Haffty BG (2014) Radiation field design in the ACOSOG Z0011 (Alliance) trial. J Clin Oncol. doi:10.1200/JCO.2014.56.5838

    Google Scholar 

  47. Reed DR, Lindsley SK, Mann GN, Austin-Seymour M, Korssjoen T, Anderson BO, Moe R (2005) Axillary lymph node dose with tangential breast irradiation. Int J Radiat Oncol Biol Phys 61(2):358–364. doi:10.1016/j.ijrobp.2004.06.006

    Article  PubMed  Google Scholar 

  48. Schlembach PJ, Buchholz TA, Ross MI, Kirsner SM, Salas GJ, Strom EA, McNeese MD, Perkins GH, Hunt KK (2001) Relationship of sentinel and axillary level I-II lymph nodes to tangential fields used in breast irradiation. Int J Radiat Oncol Biol Phys 51(3):671–678

    Article  CAS  PubMed  Google Scholar 

  49. Armer JM, Stewart BR (2005) A comparison of four diagnostic criteria for lymphedema in a post-breast cancer population. Lymphat Res Biol 3(4):208–217. doi:10.1089/lrb.2005.3.208

    Article  PubMed  Google Scholar 

  50. Committee NMA (2013) Position Statement of the National Lymphedema Network. Topic: Screening and Measurement for Early Detection of Breast Cancer Related Lymphedema

  51. Deltombe T, Jamart J, Recloux S, Legrand C, Vandenbroeck N, Theys S, Hanson P (2007) Reliability and limits of agreement of circumferential, water displacement, and optoelectronic volumetry in the measurement of upper limb lymphedema. Lymphology 40(1):26–34

    CAS  PubMed  Google Scholar 

  52. Cormier JN, Xing Y, Zaniletti I, Askew RL, Stewart BR, Armer JM (2009) Minimal limb volume change has a significant impact on breast cancer survivors. Lymphology 42(4):161–175

    CAS  PubMed  PubMed Central  Google Scholar 

  53. Ancukiewicz M, Russell TA, Otoole J, Specht M, Singer M, Kelada A, Murphy CD, Pogachar J, Gioioso V, Patel M, Skolny M, Smith BL, Taghian AG (2011) Standardized method for quantification of developing lymphedema in patients treated for breast cancer. Int J Radiat Oncol Biol Phys 79(5):1436–1443. doi:10.1016/j.ijrobp.2010.01.001

    Article  PubMed  Google Scholar 

  54. Ancukiewicz M, Miller CL, Skolny MN, O’Toole J, Warren LE, Jammallo LS, Specht MC, Taghian AG (2012) Comparison of relative versus absolute arm size change as criteria for quantifying breast cancer-related lymphedema: the flaws in current studies and need for universal methodology. Breast Cancer Res Treat 135(1):145–152. doi:10.1007/s10549-012-2111-8

    Article  PubMed  PubMed Central  Google Scholar 

  55. Tierney S, Aslam M, Rennie K, Grace P (1996) Infrared optoelectronic volumetry, the ideal way to measure limb volume. Eur J Vasc Endovasc Surg 12(4):412–417

    Article  CAS  PubMed  Google Scholar 

  56. Ward LC, Czerniec S, Kilbreath SL (2009) Quantitative bioimpedance spectroscopy for the assessment of lymphoedema. Breast Cancer Res Treat 117(3):541–547. doi:10.1007/s10549-008-0258-0

    Article  CAS  PubMed  Google Scholar 

  57. Czerniec SA, Ward LC, Lee MJ, Refshauge KM, Beith J, Kilbreath SL (2011) Segmental measurement of breast cancer-related arm lymphoedema using perometry and bioimpedance spectroscopy. Support Care Cancer 19(5):703–710. doi:10.1007/s00520-010-0896-8

    Article  PubMed  Google Scholar 

  58. Barrio AV, Eaton A, Frazier TG (2015) A Prospective Validation Study of Bioimpedance with Volume Displacement in Early-Stage Breast Cancer Patients at Risk for Lymphedema. Ann Surg Oncol 22(Suppl 3):S370–S375. doi:10.1245/s10434-015-4683-0

    Article  PubMed  Google Scholar 

  59. Armer JM, Radina ME, Porock D, Culbertson SD (2003) Predicting breast cancer-related lymphedema using self-reported symptoms. Nurs Res 52(6):370–379

    Article  PubMed  Google Scholar 

  60. Coster S, Poole K, Fallowfield LJ (2001) The validation of a quality of life scale to assess the impact of arm morbidity in breast cancer patients post-operatively. Breast Cancer Res Treat 68(3):273–282

    Article  CAS  PubMed  Google Scholar 

  61. Liengsawangwong R, Yu TK, Sun TL, Erasmus JJ, Perkins GH, Tereffe W, Oh JL, Woodward WA, Strom EA, Salephour M, Buchholz TA (2007) Treatment optimization using computed tomography-delineated targets should be used for supraclavicular irradiation for breast cancer. Int J Radiat Oncol Biol Phys 69(3):711–715. doi:10.1016/j.ijrobp.2007.05.075

    Article  PubMed  PubMed Central  Google Scholar 

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Acknowledgements

Additional contributions: Special thanks to Stephanie Deming for her editorial assistance.

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Authors and Affiliations

  1. Department of Radiation Oncology, University of Texas MD Anderson Cancer Center, 1515 Holcombe Blvd, Unit 1202, Houston, TX, 77030, USA

    Simona F. Shaitelman, Benjamin D. Smith & Wendy A. Woodward

  2. Department of Surgical Oncology, University of Texas MD Anderson Cancer Center, 1515 Holcombe Blvd, Unit 1484, Houston, TX, 77030, USA

    Yi-Ju Chiang, Kate D. Griffin & Janice N. Cormier

  3. Department of Breast Surgical Oncology, University of Texas MD Anderson Cancer Center, 1515 Holcombe Blvd, Unit 1434, Houston, TX, 77030, USA

    Sarah M. DeSnyder

  4. Department of Plastic Surgery, University of Texas MD Anderson Cancer Center, 1515 Holcombe Blvd, Unit 1488, Houston, TX, 77030, USA

    Mark V. Schaverien

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  1. Simona F. Shaitelman
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Drs. Shaitelman and DeSnyder are consultants for the MD Anderson Physician’s Network.

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The original version of this article was revised: The co-author names were missed out inaadvertenly. The corrected group is updated in the article.

An erratum to this article is available at http://dx.doi.org/10.1007/s10549-017-4116-9.

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Shaitelman, S.F., Chiang, YJ., Griffin, K.D. et al. Radiation therapy targets and the risk of breast cancer-related lymphedema: a systematic review and network meta-analysis. Breast Cancer Res Treat 162, 201–215 (2017). https://doi.org/10.1007/s10549-016-4089-0

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