Breast Cancer Research and Treatment

, Volume 157, Issue 2, pp 229–240 | Cite as

The need for preoperative baseline arm measurement to accurately quantify breast cancer-related lymphedema

  • Fangdi Sun
  • Melissa N. Skolny
  • Meyha N. Swaroop
  • Bhupendra Rawal
  • Paul J. Catalano
  • Cheryl L. Brunelle
  • Cynthia L. Miller
  • Alphonse G. Taghian
Preclinical study
First Online:
Received:
Accepted:

Abstract

Breast cancer-related lymphedema (BCRL) is a feared outcome of breast cancer treatment, yet the push for early screening is hampered by a lack of standardized quantification. We sought to determine the necessity of preoperative baseline in accounting for temporal changes of upper extremity volume. 1028 women with unilateral breast cancer were prospectively screened for lymphedema by perometry. Thresholds were defined: relative volume change (RVC) ≥10 % for clinically significant lymphedema and ≥5 % including subclinical lymphedema. The first postoperative measurement (pseudo-baseline) simulated the case of no baseline. McNemar’s test and binomial logistic regression models were used to analyze BCRL misdiagnoses. Preoperatively, 28.3 and 2.9 % of patients had arm asymmetry of ≥5 and 10 %, respectively. Without baseline, 41.6 % of patients were underdiagnosed and 40.1 % overdiagnosed at RVC ≥ 5 %, increasing to 50.0 and 54.8 % at RVC ≥ 10 %. Increased pseudo-baseline asymmetry, increased weight change between baselines, hormonal therapy, dominant use of contralateral arm, and not receiving axillary lymph node dissection (ALND) were associated with increased risk of underdiagnosis at RVC ≥ 5 %; not receiving regional lymph node radiation was significant at RVC ≥ 10 %. Increased pseudo-baseline asymmetry, not receiving ALND, and dominant use of ipsilateral arm were associated with overdiagnosis at RVC ≥ 5 %; increased pseudo-baseline asymmetry and not receiving ALND were significant at RVC ≥ 10 %. The use of a postoperative proxy even early after treatment results in poor sensitivity for identifying BCRL. Providers with access to patients before surgery should consider the consequent need for proper baseline, with specific strategy tailored by institution.

Keywords

Lymphedema Breast cancer Quantification Standardization Treatment morbidity Temporal baseline 

Abbreviations

BCRL

Breast cancer-related lymphedema

RVC

Relative volume change

DCIS

Ductal carcinoma in situ

BMI

Body mass index

CW

Chest wall

ALND

Axillary lymph node dissection

SLNB

Sentinel lymph node biopsy

PBI

Partial breast irradiation

RLNR

Regional lymph node radiation

OR

Odds ratio

CI

Confidence interval

This is a preview of subscription content, log in to check access.

Notes

Acknowledgments

The study described was supported by Award Number R01CA139118 (AGT) and Award Number P50CA089393 (AGT) from the National Cancer Institute and the Adele McKinnon Research Fund for BCRL. The content is solely the responsibility of the authors and does not necessarily represent the official views of the National Cancer Institute or the National Institutes of Health.

Compliance with ethical standards

Conflicts of interest

The authors declare that they have no conflicts of interest.

References

  1. 1.
    Cheville AL, McGarvey CL, Petrek JA et al (2003) The grading of lymphedema in oncology clinical trials. Semin Radiat Oncol 13:214–225CrossRefPubMedGoogle Scholar
  2. 2.
    Shih YC, Xu Y, Cormier JN et al (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 27:2007–2014CrossRefPubMedGoogle Scholar
  3. 3.
    Burckhardt M, Belzner M, Berg A et al (2014) Living with breast cancer-related lymphedema: a synthesis of qualitative research. Oncol Nurs Forum 41:E220–E237CrossRefPubMedGoogle Scholar
  4. 4.
    Jammallo LS, Miller CL, Horick NK et al (2014) Factors associated with fear of lymphedema after treatment for breast cancer. Oncol Nurs Forum 41:473–483CrossRefPubMedGoogle Scholar
  5. 5.
    O’Toole J, Jammallo LS, Miller CL et al (2013) Screening for breast cancer-related lymphedema: the need for standardization. Oncologist 18:350–352CrossRefPubMedPubMedCentralGoogle Scholar
  6. 6.
    DiSipio T, Rye S, Newman B et al (2013) Incidence of unilateral arm lymphoedema after breast cancer: a systematic review and meta-analysis. Lancet Oncol 14:500–515CrossRefPubMedGoogle Scholar
  7. 7.
    Tsai RJ, Dennis LK, Lynch CF et al (2009) The risk of developing arm lymphedema among breast cancer survivors: a meta-analysis of treatment factors. Ann Surg Oncol 16:1959–1972CrossRefPubMedGoogle Scholar
  8. 8.
    Armer JM, Stewart BR (2005) A comparison of four diagnostic criteria for lymphedema in a post-breast cancer population. Lymphat Res Biol 3:208–217CrossRefPubMedGoogle Scholar
  9. 9.
    Cornish BH, Chapman M, Hirst C et al (2001) Early diagnosis of lymphedema using multiple frequency bioimpedance. Lymphology 34:2–11PubMedGoogle Scholar
  10. 10.
    Hayes S, Janda M, Cornish B et al (2008) Lymphedema secondary to breast cancer: how choice of measure influences diagnosis, prevalence, and identifiable risk factors. Lymphology 41:18–28PubMedGoogle Scholar
  11. 11.
    Ancukiewicz M, Miller CL, Skolny MN et al (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 135:145–152CrossRefPubMedPubMedCentralGoogle Scholar
  12. 12.
    Paskett ED (2008) Breast cancer-related lymphedema: attention to a significant problem resulting from cancer diagnosis. J Clin Oncol 26:5666–5667CrossRefPubMedPubMedCentralGoogle Scholar
  13. 13.
    Armer JM (2005) The problem of post-breast cancer lymphedema: impact and measurement issues. Cancer Invest 23:76–83CrossRefPubMedGoogle Scholar
  14. 14.
    Hayes SC, Johansson K, Stout NL et al (2012) Upper-body morbidity after breast cancer: incidence and evidence for evaluation, prevention, and management within a prospective surveillance model of care. Cancer 118:2237–2249CrossRefPubMedGoogle Scholar
  15. 15.
    Devoogdt N, Van Kampen M, Christiaens MR et al (2011) Short- and long-term recovery of upper limb function after axillary lymph node dissection. Eur J Cancer Care (Engl) 20:77–86CrossRefGoogle Scholar
  16. 16.
    Helyer LK, Varnic M, Le LW et al (2010) Obesity is a risk factor for developing postoperative lymphedema in breast cancer patients. Breast J 16:48–54CrossRefPubMedGoogle Scholar
  17. 17.
    Bennett Britton TM, Buczacki SJ, Turner CL et al (2007) Venous changes and lymphoedema 4 years after axillary surgery for breast cancer. Br J Surg 94:833–834CrossRefPubMedGoogle Scholar
  18. 18.
    Nesvold IL, Dahl AA, Lokkevik E et al (2008) Arm and shoulder morbidity in breast cancer patients after breast-conserving therapy versus mastectomy. Acta Oncol 47:835–842CrossRefPubMedGoogle Scholar
  19. 19.
    Celebioglu F, Perbeck L, Frisell J et al (2007) Lymph drainage studied by lymphoscintigraphy in the arms after sentinel node biopsy compared with axillary lymph node dissection following conservative breast cancer surgery. Acta Radiol 48:488–495CrossRefPubMedGoogle Scholar
  20. 20.
    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 26:5213–5219CrossRefPubMedPubMedCentralGoogle Scholar
  21. 21.
    Wernicke AG, Goodman RL, Turner BC et al (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 125:893–902CrossRefPubMedPubMedCentralGoogle Scholar
  22. 22.
    Thomas-Maclean RL, Hack T, Kwan W et al (2008) Arm morbidity and disability after breast cancer: new directions for care. Oncol Nurs Forum 35:65–71CrossRefPubMedGoogle Scholar
  23. 23.
    Yang EJ, Park WB, Seo KS et al (2010) Longitudinal change of treatment-related upper limb dysfunction and its impact on late dysfunction in breast cancer survivors: a prospective cohort study. J Surg Oncol 101:84–91CrossRefPubMedGoogle Scholar
  24. 24.
    Armer JM, Stewart BR (2010) Post-breast cancer lymphedema: incidence increases from 12 to 30 to 60 months. Lymphology 43:118–127PubMedPubMedCentralGoogle Scholar
  25. 25.
    Bundred NJ, Stockton C, Keeley V et al (2015) Comparison of multi-frequency bioimpedance with perometry for the early detection and intervention of lymphoedema after axillary node clearance for breast cancer. Breast Cancer Res Treat 151:121–129CrossRefPubMedGoogle Scholar
  26. 26.
    Karlsson KY, Wallenius I, Nilsson-Wikmar LB et al (2015) Lymphoedema and health-related quality of life by early treatment in long-term survivors of breast cancer. A comparative retrospective study up to 15 years after diagnosis. Support Care Cancer 23:2965–2972CrossRefPubMedGoogle Scholar
  27. 27.
    Sackey H, Johansson H, Sandelin K et al (2015) Self-perceived, but not objective lymphoedema is associated with decreased long-term health-related quality of life after breast cancer surgery. Eur J Surg Oncol 41:577–584CrossRefPubMedGoogle Scholar
  28. 28.
    Sagen A, Kaaresen R, Sandvik L et al (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 95:875–881CrossRefPubMedGoogle Scholar
  29. 29.
    Bulley C, Coutts F, Blyth C et al (2014) A Morbidity Screening Tool for identifying fatigue, pain, upper limb dysfunction and lymphedema after breast cancer treatment: a validity study. Eur J Oncol Nurs 18:218–227CrossRefPubMedGoogle Scholar
  30. 30.
    Framework Lymphoedema (2006) Best practice for the management of lymphoedema. International consensus. London, MEP LtdGoogle Scholar
  31. 31.
    Deltombe T, Jamart J, Recloux S et al (2007) Reliability and limits of agreement of circumferential, water displacement, and optoelectronic volumetry in the measurement of upper limb lymphedema. Lymphology 40:26–34PubMedGoogle Scholar
  32. 32.
    Brunelle C, Skolny M, Ferguson C et al (2015) Establishing and sustaining a prospective screening program for breast cancer-related lymphedema at the massachusetts general hospital: lessons learned. J Pers Med 5:153–164CrossRefPubMedPubMedCentralGoogle Scholar
  33. 33.
    Tierney S, Aslam M, Rennie K et al (1996) Infrared optoelectronic volumetry, the ideal way to measure limb volume. Eur J Vasc Endovasc Surg 12:412–417CrossRefPubMedGoogle Scholar
  34. 34.
    Stanton AW, Northfield JW, Holroyd B et al (1997) Validation of an optoelectronic limb volumeter (Perometer). Lymphology 30:77–97PubMedGoogle Scholar
  35. 35.
    O’Toole J, Jammallo LS, Skolny MN et al (2013) Lymphedema following treatment for breast cancer: a new approach to an old problem. Crit Rev Oncol Hematol 88:437–446CrossRefPubMedPubMedCentralGoogle Scholar
  36. 36.
    Ancukiewicz M, Russell TA, Otoole J et al (2011) Standardized method for quantification of developing lymphedema in patients treated for breast cancer. Int J Radiat Oncol Biol Phys 79:1436–1443CrossRefPubMedPubMedCentralGoogle Scholar
  37. 37.
    Specht MC, Miller CL, Russell TA et al (2013) Defining a threshold for intervention in breast cancer-related lymphedema: what level of arm volume increase predicts progression? Breast Cancer Res Treat 140:485–494CrossRefPubMedPubMedCentralGoogle Scholar
  38. 38.
    Swaroop MN, Ferguson CM, Horick NK et al (2015) Impact of adjuvant taxane-based chemotherapy on development of breast cancer-related lymphedema: results from a large prospective cohort. Breast Cancer Res Treat 151:393–403PubMedPubMedCentralGoogle Scholar
  39. 39.
    NLN Medical Advisory Committee (2013) Position statement of national lymphedema network: screening and measurement for early detection of breast cancer related lymphedema 2015Google Scholar
  40. 40.
    Golshan M, Smith B (2006) Prevention and management of arm lymphedema in the patient with breast cancer. J Support Oncol 4:381–386PubMedGoogle Scholar
  41. 41.
    Karlsson KY, Wallenius I, Nilsson-Wikmar LB et al (2015) Lymphoedema and health-related quality of life by early treatment in long-term survivors of breast cancer. A comparative retrospective study up to 15 years after diagnosis. Support Care Cancer 23:2965–2972CrossRefPubMedGoogle Scholar
  42. 42.
    Stout NL, Pfalzer LA, Springer B et al (2012) Breast cancer-related lymphedema: comparing direct costs of a prospective surveillance model and a traditional model of care. Phys Ther 92:152–163CrossRefPubMedPubMedCentralGoogle Scholar
  43. 43.
    Asim M, Cham A, Banerjee S et al (2012) Difficulties with defining lymphoedema after axillary dissection for breast cancer. N Z Med J 125:29–39PubMedGoogle Scholar
  44. 44.
    Johansson K, Branje E (2010) Arm lymphoedema in a cohort of breast cancer survivors 10 years after diagnosis. Acta Oncol 49:166–173CrossRefPubMedGoogle Scholar
  45. 45.
    Kosir MA, Rymal C, Koppolu P et al (2001) Surgical outcomes after breast cancer surgery: measuring acute lymphedema. J Surg Res 95:147–151CrossRefPubMedGoogle Scholar
  46. 46.
    Pain SJ, Vowler S, Purushotham AD (2005) Axillary vein abnormalities contribute to development of lymphoedema after surgery for breast cancer. Br J Surg 92:311–315CrossRefPubMedGoogle Scholar
  47. 47.
    Quinlan E, Thomas-MacLean R, Hack T et al (2009) The impact of breast cancer among Canadian women: disability and productivity. Work 34:285–296PubMedGoogle Scholar
  48. 48.
    Edwards TL (2000) Prevalence and aetiology of lymphoedema after breast cancer treatment in southern Tasmania. Aust N Z J Surg 70:412–418CrossRefPubMedGoogle Scholar
  49. 49.
    Tengrup I, Tennvall-Nittby L, Christiansson I et al (2000) Arm morbidity after breast-conserving therapy for breast cancer. Acta Oncol 39:393–397CrossRefPubMedGoogle Scholar
  50. 50.
    Cormier JN, Xing Y, Zaniletti I et al (2009) Minimal limb volume change has a significant impact on breast cancer survivors. Lymphology 42:161–175PubMedPubMedCentralGoogle Scholar
  51. 51.
    Buragadda S, Alhusaini AA, Melam GR et al (2015) Effect of complete decongestive therapy and a home program for patients with post mastectomy lymphedema. J Phys Ther Sci 27:2743–2748CrossRefPubMedPubMedCentralGoogle Scholar
  52. 52.
    Hayes S, Di Sipio T, Rye S et al (2011) Prevalence and prognostic significance of secondary lymphedema following breast cancer. Lymphat Res Biol 9:135–141CrossRefPubMedGoogle Scholar
  53. 53.
    Zakaria S, Johnson R, Pockaj BA et al (2007) Breast cancer presenting as unilateral arm edema. J Gen Intern Med 22:675–676CrossRefPubMedPubMedCentralGoogle Scholar
  54. 54.
    Vignes S, Arrault M, Bonhomme S et al (2007) Upper limb lymphedema revealing breast cancer. Rev Med Interne 28:631–634CrossRefPubMedGoogle Scholar
  55. 55.
    Hayes SC, Janda M, Cornish B et al (2008) Lymphedema after breast cancer: incidence, risk factors, and effect on upper body function. J Clin Oncol 26:3536–3542CrossRefPubMedGoogle Scholar
  56. 56.
    Norman SA, Localio AR, Kallan MJ et al (2010) Risk factors for lymphedema after breast cancer treatment. Cancer Epidemiol Biomarkers Prev 19:2734–2746CrossRefPubMedPubMedCentralGoogle Scholar
  57. 57.
    Park JH, Lee WH, Chung HS (2008) Incidence and risk factors of breast cancer lymphoedema. J Clin Nurs 17:1450–1459CrossRefPubMedGoogle Scholar
  58. 58.
    Ozaslan C, Kuru B (2004) Lymphedema after treatment of breast cancer. Am J Surg 187:69–72CrossRefPubMedGoogle Scholar
  59. 59.
    Griffiths CL, Olin JL (2012) Triple negative breast cancer: a brief review of its characteristics and treatment options. J Pharm Pract 25:319–323CrossRefPubMedGoogle Scholar
  60. 60.
    International Society of Lymphology (2013) The diagnosis and treatment of peripheral lymphedema: 2013 Consensus Document of the International Society of Lymphology. Lymphology 46:1–11Google Scholar
  61. 61.
    Cancer Therapy Evaluation Program (2006) Common terminology criteria for adverse events, version 3.0. DCTD, NCI, NIH, DHHSGoogle Scholar
  62. 62.
    Tuttle TM, Habermann EB, Grund EH et al (2007) Increasing use of contralateral prophylactic mastectomy for breast cancer patients: a trend toward more aggressive surgical treatment. J Clin Oncol 25:5203–5209CrossRefPubMedGoogle Scholar
  63. 63.
    Fu Y, Zhuang Z, Dewing M et al (2015) Predictors for contralateral prophylactic mastectomy in breast cancer patients. Int J Clin Exp Pathol 8:3748–3764PubMedPubMedCentralGoogle Scholar
  64. 64.
    Miller CL, Specht MC, Horick N et al (2013) A novel, validated method to quantify breast cancer-related lymphedema (BCRL) following bilateral breast surgery. Lymphology 46:64–74PubMedGoogle Scholar

Copyright information

© Springer Science+Business Media New York 2016

Authors and Affiliations

  • Fangdi Sun
    • 1
  • Melissa N. Skolny
    • 1
  • Meyha N. Swaroop
    • 1
  • Bhupendra Rawal
    • 2
  • Paul J. Catalano
    • 2
  • Cheryl L. Brunelle
    • 3
  • Cynthia L. Miller
    • 1
  • Alphonse G. Taghian
    • 1
  1. 1.Department of Radiation OncologyMassachusetts General Hospital, Harvard Medical SchoolBostonUSA
  2. 2.Department of Biostatistics and Computational BiologyDana-Farber Cancer InstituteBostonUSA
  3. 3.Department of Physical and Occupational TherapyMassachusetts General Hospital, Harvard Medical SchoolBostonUSA

Personalised recommendations