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Nomograms for Predicting the Risk of Arm Lymphedema after Axillary Dissection in Breast Cancer

Annals of Surgical Oncology volume 19, pages 2580–2589 (2012)Cite this article

Abstract

Background

Lymphedema (LE) after axillary lymph node dissection (ALND) is a multifactorial, chronic, and disabling condition that currently affects an estimated 4 million people worldwide. Although several risk factors have been described, it is difficult to estimate the risk in individual patients. We therefore developed nomograms based on a large data set.

Methods

Clinicopathologic features were collected from a prospective cohort comprising 1,054 women with unilateral breast cancer undergoing ALND as part of their surgical treatment from August 2001 to November 2002. LE was defined as a volume difference of at least 200 ml between arms at 6 months or more after surgery. The cumulative incidence of LE was ascertained by the Kaplan–Meier method, and Cox proportional hazard models were used to predict the risk of developing LE on the basis of the available data at each time point: model 1, preoperatively; model 2, within 6 months from surgery; and model 3, at 6 months or later after surgery.

Results

The 5 year cumulative incidence of LE was 30.3%. Independent risk factors for LE were age, body mass index, ipsilateral arm chemotherapy infusions, level of ALND, location of radiotherapy field, development of postoperative seroma, infection, and early edema. When applied to the validation set, the concordance indices were 0.706, 0.729, and 0.736 for models 1, 2, and 3, respectively.

Conclusions

The proposed nomograms can help physicians and patients predict the 5 year probability of LE after ALND for breast cancer. Free online versions of the nomograms are available at http://www.lymphedemarisk.com/.

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References

  1. Ferlay J, Bray F, Pisani P, Parkin DM. GLOBOCAN 2008, Cancer incidence and mortality worldwide. IARC CancerBase No. 10. Lyon, France: International Agency for Research on Cancer; 2010. http://globocan.iarc.fr.

  2. American Cancer Society. Cancer facts and figures, 2010. Atlanta: American Cancer Society; 2010.

    Google Scholar 

  3. Surveillance, Epidemiology, and End Results. Cancer of the breast (invasive)—estimated United States cancer prevalence counts on January 1, 2007, by race/ethnicity, sex and years since diagnosis (table 4.25). SEER Cancer Statistics Review, 1975–2007. http://seer.cancer.gov/csr/1975_2007/browse_csr.php?section=4&page=sect_04_table.25.html.

  4. International Data Base (IDB)—World population summary. US Census Bureau, Population Division, December 11, 2010. http://www.census.gov/ipc/www/idb/worldpopinfo.php.

  5. McLaughlin SA, Wright MJ, Morris KT, et al. Prevalence of lymphedema in women with breast cancer 5 years after sentinel lymph node biopsy or axillary dissection: objective measurements. J Clin Oncol. 2008;26:5213–9.

    Article  PubMed  Google Scholar 

  6. Tsai RJ, Dennis LK, Lynch CF, Snetselaar LG, Zamba GK, Scott-Conner C. The risk of developing arm lymphedema among breast cancer survivors: a meta-analysis of treatment factors. Ann Surg Oncol. 2009;16:1959–72.

    Article  PubMed  Google Scholar 

  7. Bevilacqua JL, Kattan MW, Fey JV, Cody HS III, Borgen PI, Van Zee KJ. Doctor, what are my chances of having a positive sentinel node? A validated nomogram for risk estimation. J Clin Oncol. 2007;25:3670–9.

    Article  PubMed  Google Scholar 

  8. Voogd AC, Coebergh JW, Repelaer van Driel OJ, et al. The risk of nodal metastases in breast cancer patients with clinically negative lymph nodes: a population-based analysis. Breast Cancer Res Treat. 2000;62:63–9.

    Article  PubMed  CAS  Google Scholar 

  9. Edwards TL. Prevalence and aetiology of lymphoedema after breast cancer treatment in southern Tasmania. Aust N Z J Surg. 2000;70:412–8.

    Article  PubMed  CAS  Google Scholar 

  10. Kuehn T, Klauss W, Darsow M, et al. Long-term morbidity following axillary dissection in breast cancer patients—clinical assessment, significance for life quality and the impact of demographic, oncologic and therapeutic factors. Breast Cancer Res Treat. 2000;64:275–86.

    Article  PubMed  CAS  Google Scholar 

  11. Hojris I, Andersen J, Overgaard M, Overgaard J. Late treatment-related morbidity in breast cancer patients randomized to postmastectomy radiotherapy and systemic treatment versus systemic treatment alone. Acta Oncol. 2000;39:355–72.

    Article  PubMed  CAS  Google Scholar 

  12. Johansen J, Overgaard J, Blichert-Toft M, Overgaard M. Treatment of morbidity associated with the management of the axilla in breast-conserving therapy. Acta Oncol. 2000;39:349–54.

    Article  PubMed  CAS  Google Scholar 

  13. Schrenk P, Rieger R, Shamiyeh A, Wayand W. Morbidity following sentinel lymph node biopsy versus axillary lymph node dissection for patients with breast carcinoma. Cancer. 2000;88:608–14.

    Article  PubMed  CAS  Google Scholar 

  14. Isaksson G, Feuk B. Morbidity from axillary treatment in breast cancer—a follow-up study in a district hospital. Acta Oncol. 2000;39:335–6.

    Article  PubMed  CAS  Google Scholar 

  15. Petrek JA, Senie RT, Peters M, Rosen PP. Lymphedema in a cohort of breast carcinoma survivors 20 years after diagnosis. Cancer. 2001;92:1368–77.

    Article  PubMed  CAS  Google Scholar 

  16. Freitas R Jr, Ribeiro LFJ, Tala L, Kajita D, Fernandes MV, Queiroz G. Lymphedema in breast cancer patients submitted to modified radical mastectomy. Rev Bras Ginecol Obstet. 2001;23:205–8.

    Article  Google Scholar 

  17. Ververs JM, Roumen RM, Vingerhoets AJ, et al. Risk, severity and predictors of physical and psychological morbidity after axillary lymph node dissection for breast cancer. Eur J Cancer. 2001;37:991–9.

    Article  PubMed  CAS  Google Scholar 

  18. Sener SF, Winchester DJ, Martz CH, et al. Lymphedema after sentinel lymphadenectomy for breast carcinoma. Cancer. 2001;92:748–52.

    Article  PubMed  CAS  Google Scholar 

  19. Duff M, Hill AD, McGreal G, Walsh S, McDermott EW, O’Higgins NJ. Prospective evaluation of the morbidity of axillary clearance for breast cancer. Br J Surg. 2001;88:114–7.

    Article  PubMed  CAS  Google Scholar 

  20. Herd-Smith A, Russo A, Muraca MG, Del Turco MR, Cardona G. Prognostic factors for lymphedema after primary treatment of breast carcinoma. Cancer. 2001;92:1783–7.

    Article  PubMed  CAS  Google Scholar 

  21. Meric F, Buchholz TA, Mirza NQ, et al. Long-term complications associated with breast-conservation surgery and radiotherapy. Ann Surg Oncol. 2002;9:543–9.

    Article  PubMed  Google Scholar 

  22. Almeida AM, Prado MAS, Guidorizzi LLF, Rossini FP. Mulheres com câncer de mama: estudo de morbidade. Acta Oncol Bras. 2002;22:263–9.

    Google Scholar 

  23. Beaulac SM, McNair LA, Scott TE, LaMorte WW, Kavanah MT. Lymphedema and quality of life in survivors of early-stage breast cancer. Arch Surg. 2002;137:1253–7.

    Article  PubMed  Google Scholar 

  24. Swenson KK, Nissen MJ, Ceronsky C, Swenson L, Lee MW, Tuttle TM. Comparison of side effects between sentinel lymph node and axillary lymph node dissection for breast cancer. Ann Surg Oncol. 2002;9:745–53.

    Article  PubMed  Google Scholar 

  25. Temple LK, Baron R, Cody HS III, et al. Sensory morbidity after sentinel lymph node biopsy and axillary dissection: a prospective study of 233 women. Ann Surg Oncol. 2002;9:654–62.

    Article  PubMed  Google Scholar 

  26. Rampaul RS, Mullinger K, Macmillan RD, et al. Incidence of clinically significant lymphoedema as a complication following surgery for primary operable breast cancer. Eur J Cancer. 2003;39:2165–7.

    Article  PubMed  CAS  Google Scholar 

  27. Deutsch M, Flickinger JC. Arm edema after lumpectomy and breast irradiation. Am J Clin Oncol. 2003;26:229–31.

    PubMed  Google Scholar 

  28. Schijven MP, Vingerhoets AJ, Rutten HJ, et al. Comparison of morbidity between axillary lymph node dissection and sentinel node biopsy. Eur J Surg Oncol. 2003;29:341–50.

    Article  PubMed  CAS  Google Scholar 

  29. Yap KP, McCready DR, Narod S, Manchul LA, Trudeau M, Fyles A. Factors influencing arm and axillary symptoms after treatment for node negative breast carcinoma. Cancer. 2003;97:1369–75.

    Article  PubMed  Google Scholar 

  30. Golshan M, Martin WJ, Dowlatshahi K. Sentinel lymph node biopsy lowers the rate of lymphedema when compared with standard axillary lymph node dissection. Am Surg. 2003;69:209–11.

    PubMed  Google Scholar 

  31. Blanchard DK, Donohue JH, Reynolds C, Grant CS. Relapse and morbidity in patients undergoing sentinel lymph node biopsy alone or with axillary dissection for breast cancer. Arch Surg. 2003;138:482–7.

    Article  PubMed  Google Scholar 

  32. Veronesi U, Paganelli G, Viale G, et al. A randomized comparison of sentinel-node biopsy with routine axillary dissection in breast cancer. N Engl J Med. 2003;349:546–53.

    Article  PubMed  Google Scholar 

  33. Goffman TE, Laronga C, Wilson L, Elkins D. Lymphedema of the arm and breast in irradiated breast cancer patients: risks in an era of dramatically changing axillary surgery. Breast J. 2004;10:405–11.

    Article  PubMed  Google Scholar 

  34. Deo SV, Ray S, Rath GK, et al. Prevalence and risk factors for development of lymphedema following breast cancer treatment. Indian J Cancer. 2004;41:8–12.

    PubMed  CAS  Google Scholar 

  35. Ozaslan C, Kuru B. Lymphedema after treatment of breast cancer. Am J Surg. 2004;187:69–72.

    Article  PubMed  Google Scholar 

  36. Silberman AW, McVay C, Cohen JS, et al. Comparative morbidity of axillary lymph node dissection and the sentinel lymph node technique: implications for patients with breast cancer. Ann Surg. 2004;240:1–6.

    Article  PubMed  Google Scholar 

  37. Armer J, Fu MR, Wainstock JM, Zagar E, Jacobs LK. Lymphedema following breast cancer treatment, including sentinel lymph node biopsy. Lymphology. 2004;37:73–91.

    PubMed  CAS  Google Scholar 

  38. van der Veen P, De Voogdt N, Lievens P, Duquet W, Lamote J, Sacre R. Lymphedema development following breast cancer surgery with full axillary resection. Lymphology. 2004;37:206–8.

    PubMed  Google Scholar 

  39. Bergmann A. Diagnóstico de linfedema: análise dos métodos empregados na avaliação do membro superior após linfadenectomia axilar para tratamento do câncer de mama. Rev Bras Cancerol. 2004;50:311–20.

    Google Scholar 

  40. Bergmann A, Koifman RJ, Ribeiro MJP, Mattos IE. Upper limb lymphedema following breast cancer surgery: prevalence and associated factors. Lymphology. 2007;40(Suppl.):96–106.

    Google Scholar 

  41. Bergmann A. Incidência e fatores de risco do linfedema após tratamento cirúrgico para câncer de mama: Estudo de uma coorte hospitalar. Rio de Janiero: Escola Nacional de Saúde Pública, Fundação Oswaldo Cruz; 2005.

  42. Leidenius M, Leivonen M, Vironen J, von Smitten K. The consequences of long-time arm morbidity in node-negative breast cancer patients with sentinel node biopsy or axillary clearance. J Surg Oncol. 2005;92:23–31.

    Article  PubMed  CAS  Google Scholar 

  43. Rönkä R, von Smitten K, Tasmuth T, Leidenius M. One-year morbidity after sentinel node biopsy and breast surgery. Breast. 2005;14:28–36.

    Article  PubMed  Google Scholar 

  44. Clark B, Sitzia J, Harlow W. Incidence and risk of arm oedema following treatment for breast cancer: a three-year follow-up study. QJM. 2005;98:343–8.

    Article  PubMed  CAS  Google Scholar 

  45. Mansel RE, Fallowfield L, Kissin M, et al. Randomized multicenter trial of sentinel node biopsy versus standard axillary treatment in operable breast cancer: the ALMANAC trial. J Natl Cancer Inst. 2006;98:599–609.

    Article  PubMed  Google Scholar 

  46. Langer I, Guller U, Berclaz G, et al. 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. 2007;245:452–61.

    Article  PubMed  Google Scholar 

  47. Lucci A, McCall LM, Beitsch PD, et al. 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. 2007;25:3657–63.

    Article  PubMed  Google Scholar 

  48. McLaughlin SA, Wright MJ, Morris KT, et al. Prevalence of lymphedema in women with breast cancer 5 years after sentinel lymph node biopsy or axillary dissection: patient perceptions and precautionary behaviors. J Clin Oncol. 2008;26:5220–6.

    Article  PubMed  Google Scholar 

  49. Armer JM, Radina ME, Porock D, Culbertson SD. Predicting breast cancer–related lymphedema using self-reported symptoms. Nurs Res. 2003;52:370–9.

    Article  PubMed  Google Scholar 

  50. Bani HA, Fasching PA, Lux MM, et al. Lymphedema in breast cancer survivors: assessment and information provision in a specialized breast unit. Patient Educ Couns. 2007;66:311–8.

    Article  PubMed  Google Scholar 

  51. Clark GM. Prognostic and Predictive Factors. In: Harris JR, Lippman ME, Morrow M, Osborne CK, editors. Diseases of the breast. Philadelphia: Lippincott Williams & Wilkins; 1996. p. 461–85.

  52. Coen JJ, Taghian AG, Kachnic LA, Assaad SI, Powell SN. Risk of lymphedema after regional nodal irradiation with breast conservation therapy. Int J Radiat Oncol Biol Phys. 2003;55:1209–15.

    Article  PubMed  Google Scholar 

  53. Hinrichs CS, Watroba NL, Rezaishiraz H, et al. Lymphedema secondary to postmastectomy radiation: incidence and risk factors. Ann Surg Oncol. 2004;11:573–80.

    Article  PubMed  Google Scholar 

  54. Johansson K, Ohlsson K, Ingvar C, Albertsson M, Ekdahl C. Factors associated with the development of arm lymphedema following breast cancer treatment: a match pair case-control study. Lymphology. 2002;35:59–71.

    PubMed  CAS  Google Scholar 

  55. Langer S, Guenther JM, Haigh PI, DiFronzo LA. Lymphatic mapping improves staging and reduces morbidity in women undergoing total mastectomy for breast carcinoma. Am Surg. 2004;70:881–5.

    PubMed  Google Scholar 

  56. Mathew J, Barthelmes L, Neminathan S, Crawford D. Comparative study of lymphoedema with axillary node dissection versus axillary node sampling with radiotherapy in patients undergoing breast conservation surgery. Eur J Surg Oncol. 2006;32:729–32.

    Article  PubMed  CAS  Google Scholar 

  57. Meeske KA, Sullivan-Halley J, Smith AW, et al. Risk factors for arm lymphedema following breast cancer diagnosis in Black women and White women. Breast Cancer Res Treat. 2009;113:383–91.

    Article  PubMed  Google Scholar 

  58. Moskovitz AH, Anderson BO, Yeung RS, Byrd DR, Lawton TJ, Moe RE. Axillary web syndrome after axillary dissection. Am J Surg. 2001;181:434–9.

    Article  PubMed  CAS  Google Scholar 

  59. Casley-Smith JR. Measuring and representing peripheral oedema and its alterations. Lymphology. 1994;27:56–70.

    PubMed  CAS  Google Scholar 

  60. Clarke D, Martinez A, Cox RS, Goffinet DR. Breast edema following staging axillary node dissection in patients with breast carcinoma treated by radical radiotherapy. Cancer. 1982;49:2295–9.

    Article  PubMed  CAS  Google Scholar 

  61. Mathers C, Fat DM, Boerma JT, World Health Organization. The global burden of disease 2004 update. Geneva: World Health Organization; 2008.

  62. Pisano ED, Gatsonis C, Hendrick E, et al. Diagnostic performance of digital versus film mammography for breast-cancer screening. N Engl J Med. 2005;353:1773–83.

    Article  PubMed  CAS  Google Scholar 

  63. Giuliano AE, McCall L, Beitsch P, et al. Locoregional recurrence after sentinel lymph node dissection with or without axillary dissection in patients with sentinel lymph node metastases: the American College of Surgeons Oncology Group Z0011 randomized trial. Ann Surg. 2010;252:426–32.

    PubMed  Google Scholar 

  64. Giuliano AE, Hunt KK, Ballman KV, et al. Axillary dissection vs no axillary dissection in women with invasive breast cancer and sentinel node metastasis: a randomized clinical trial. JAMA. 2011;305:569–75.

    Article  PubMed  CAS  Google Scholar 

  65. Weber WP, Barry M, Stempel MM, et al. A 10-year trend analysis of sentinel lymph node frozen section and completion axillary dissection for breast cancer: are these procedures becoming obsolete? Ann Surg Oncol. 2012;19:225–32.

    Article  PubMed  Google Scholar 

  66. National Comprehensive Cancer Network (NCCN). Clinical practice guidelines in oncology, version 2, 2011. http://www.nccn.org/.

  67. Baker A, Kim H, Semple JL, et al. Experimental assessment of pro-lymphangiogenic growth factors in the treatment of post-surgical lymphedema following lymphadenectomy. Breast Cancer Res. 2010;12:R70.

    Article  PubMed  Google Scholar 

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Acknowledgment

The authors would like to express their deepest gratitude to all patients, surgeons, and physical therapists at HCIII/INCA, Rio de Janeiro, Brazil; and to Dr. Kimberly Van Zee of Memorial Sloan-Kettering Cancer Center, NY; to Dr. Mauro Figueiredo Andrade of Faculdade de Medicina da Universidade de São Paulo, Brazil, for their insights, encouragement, and constructive criticism; to Dr. C. Greg Hagerty for his assistance in the computer application; and to Dr. Everardo Saad for proofreading. Supported by Fundação Carlos Chagas Filho de Amparo à Pesquisa do Estado do Rio de Janeiro (FAPERJ), Postdoctoral grant E-26/100.851/2007, Conselho Nacional de Pesquisas e Desenvolvimento Tecnológico (CNPq), and Escola Nacional de Saúde Púbica, FIOCRUZ.

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Authors and Affiliations

  1. Escola Nacional de Saúde Pública/FIOCRUZ, Rio de Janeiro, Brazil

    José Luiz B. Bevilacqua MD, PhD, Sergio Koifman MD, PhD, Inês E. Mattos MD, PhD & Rosalina J. Koifman MD, PhD

  2. Hospital Sirio-Libanes, Sao Paulo, Brazil

    José Luiz B. Bevilacqua MD, PhD

  3. Department of Quantitative Health Sciences, Cleveland Clinic, Cleveland, OH, USA

    Michael W. Kattan PhD & Yu Changhong MS

  4. Instituto Nacional de Câncer (INCA), Rio de Janeiro, Brazil

    Anke Bergmann PhD

  5. Centro Universitario Augusto Motta-UNISUAM, Rio de Janeiro, Brazil

    Anke Bergmann PhD

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  1. José Luiz B. Bevilacqua MD, PhD
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  2. Michael W. Kattan PhD
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  3. Yu Changhong MS
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  4. Sergio Koifman MD, PhD
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Correspondence to José Luiz B. Bevilacqua MD, PhD.

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Bevilacqua, J.L.B., Kattan, M.W., Changhong, Y. et al. Nomograms for Predicting the Risk of Arm Lymphedema after Axillary Dissection in Breast Cancer. Ann Surg Oncol 19, 2580–2589 (2012). https://doi.org/10.1245/s10434-012-2290-x

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