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.
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.
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.
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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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.
American Cancer Society. Cancer facts and figures, 2010. Atlanta: American Cancer Society; 2010.
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.
International Data Base (IDB)—World population summary. US Census Bureau, Population Division, December 11, 2010. http://www.census.gov/ipc/www/idb/worldpopinfo.php.
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.
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.
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.
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.
Edwards TL. Prevalence and aetiology of lymphoedema after breast cancer treatment in southern Tasmania. Aust N Z J Surg. 2000;70:412–8.
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.
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.
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.
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.
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.
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.
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.
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.
Sener SF, Winchester DJ, Martz CH, et al. Lymphedema after sentinel lymphadenectomy for breast carcinoma. Cancer. 2001;92:748–52.
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.
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.
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.
Almeida AM, Prado MAS, Guidorizzi LLF, Rossini FP. Mulheres com câncer de mama: estudo de morbidade. Acta Oncol Bras. 2002;22:263–9.
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.
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.
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.
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.
Deutsch M, Flickinger JC. Arm edema after lumpectomy and breast irradiation. Am J Clin Oncol. 2003;26:229–31.
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.
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.
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.
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.
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.
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.
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.
Ozaslan C, Kuru B. Lymphedema after treatment of breast cancer. Am J Surg. 2004;187:69–72.
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.
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.
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.
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.
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.
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.
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.
Rönkä R, von Smitten K, Tasmuth T, Leidenius M. One-year morbidity after sentinel node biopsy and breast surgery. Breast. 2005;14:28–36.
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.
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.
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.
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.
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.
Armer JM, Radina ME, Porock D, Culbertson SD. Predicting breast cancer–related lymphedema using self-reported symptoms. Nurs Res. 2003;52:370–9.
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.
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.
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.
Hinrichs CS, Watroba NL, Rezaishiraz H, et al. Lymphedema secondary to postmastectomy radiation: incidence and risk factors. Ann Surg Oncol. 2004;11:573–80.
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.
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.
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.
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.
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.
Casley-Smith JR. Measuring and representing peripheral oedema and its alterations. Lymphology. 1994;27:56–70.
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.
Mathers C, Fat DM, Boerma JT, World Health Organization. The global burden of disease 2004 update. Geneva: World Health Organization; 2008.
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.
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.
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.
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.
National Comprehensive Cancer Network (NCCN). Clinical practice guidelines in oncology, version 2, 2011. http://www.nccn.org/.
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.
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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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
- Breast Cancer
- Sentinel Lymph Node
- Sentinel Lymph Node Biopsy
- Axillary Lymph Node Dissection