Skip to main content

Advertisement

SpringerLink
Log in

Axillary evaluation and lymphedema in women with ductal carcinoma in situ

  • Epidemiology
  • Published:
Breast Cancer Research and Treatment Aims and scope Submit manuscript

Abstract

Axillary evaluation in women with ductal carcinoma in situ (DCIS) is increasing; however, this may introduce additional morbidity with unclear benefit. Our objective was to examine the morbidity and mortality associated with axillary evaluation in DCIS. We conducted a retrospective cohort study of 10,504 women aged 65–90 years with DCIS who underwent breast conserving surgery between 2002 and 2012 using SEER-Medicare database. Patients were categorized by receipt of axillary evaluation with either sentinel lymph node biopsy (SLNB) or axillary node dissection (ALND). We determined the incidence of lymphedema treatment as defined by diagnostic and procedural codes, as well as 10-year breast cancer-specific and all-cause mortality. 18.3 % of those treated with BCS and 69.4 % of those treated with mastectomy had an axillary evaluation. One year after treatment, 8.2 % of women who had an axillary evaluation developed lymphedema, compared to 5.9 % of those who did not. In a multivariable Cox proportional hazard model, the incidence of lymphedema was higher among those who underwent axillary evaluation (HR 1.22, 95 % CI 1.04–1.45). Overall 10-year breast cancer-specific survival was similar between both groups (HR 0.83, 95 % CI 0.40–1.74). Only 44 (0.40 %) women died of breast cancer; receipt of axillary evaluation did not alter overall survival. Axillary evaluation is commonly performed in women with DCIS, especially those undergoing mastectomy. However, women who receive an axillary evaluation have higher rates of lymphedema, without breast cancer-specific or overall survival benefit. Efforts should be made to determine the population of women with DCIS who benefit from this procedure.

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

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1

Similar content being viewed by others

References

  1. Siziopikou KP (2013) Ductal carcinoma in situ of the breast: current concepts and future directions. Arch Pathol Lab Med 137(4):462–466

    Article  CAS  PubMed  Google Scholar 

  2. Patani N, Cutuli B, Mokbel K (2008) Current management of DCIS: a review. Breast Cancer Res Treat 111(1):1–10

    Article  PubMed  Google Scholar 

  3. Lyman GH, Giuliano AE, Somerfield MR, Benson AB 3rd, Bodurka DC, Burstein HJ, Cochran AJ, Cody HS 3rd, Edge SB, Galper S et al (2005) American Society of Clinical Oncology guideline recommendations for sentinel lymph node biopsy in early-stage breast cancer. J Clin Oncol Off J Am Soc Clin Oncol 23(30):7703–7720

    Article  Google Scholar 

  4. Lyman GH, Temin S, Edge SB, Newman LA, Turner RR, Weaver DL, Benson AB 3rd, Bosserman LD, Burstein HJ, Cody H 3rd et al (2014) Sentinel lymph node biopsy for patients with early-stage breast cancer: American Society of Clinical Oncology clinical practice guideline update. J Clin Oncol Off J Am Soc Clin Oncol 32(13):1365–1383

    Article  Google Scholar 

  5. Coromilas EJ, Wright JD, Huang Y, Feldman S, Neugut AI, Chen L, Hershman DL (2015) The influence of hospital and surgeon factors on the prevalence of axillary lymph node evaluation in ductal carcinoma in situ. JAMA Oncol 1(3):323–332

    Article  PubMed  Google Scholar 

  6. Yeoh EK, Denham JW, Davies SA, Spittle MF (1986) Primary breast cancer. complications of axillary management. Acta Radiol Oncol 25(2):105–108

    Article  CAS  PubMed  Google Scholar 

  7. Ivens D, Hoe AL, Podd TJ, Hamilton CR, Taylor I, Royle GT (1992) Assessment of morbidity from complete axillary dissection. Br J Cancer 66(1):136–138

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  8. Li CZ, Zhang P, Li RW, Wu CT, Zhang XP, Zhu HC (2015) Axillary lymph node dissection versus sentinel lymph node biopsy alone for early breast cancer with sentinel node metastasis: a meta-analysis. Eur J Surg Oncol J Eur Soc Surg Oncol Br Assoc Surg Oncol 41(8):958–966

    CAS  Google Scholar 

  9. Krag DN, Anderson SJ, Julian TB, Brown AM, Harlow SP, Costantino JP, Ashikaga T, Weaver DL, Mamounas EP, Jalovec LM et al (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

    Article  PubMed  PubMed Central  Google Scholar 

  10. Zavagno G, De Salvo GL, Scalco G, Bozza F, Barutta L, Del Bianco P, Renier M, Racano C, Carraro P, Nitti D et al (2008) A randomized clinical trial on sentinel lymph node biopsy versus axillary lymph node dissection in breast cancer: results of the Sentinella/GIVOM trial. Ann Surg 247(2):207–213

    Article  PubMed  Google Scholar 

  11. Chen AY, Halpern MT, Schrag NM, Stewart A, Leitch M, Ward E (2008) Disparities and trends in sentinel lymph node biopsy among early-stage breast cancer patients (1998–2005). J Natl Cancer Inst 100(7):462–474

    Article  PubMed  Google Scholar 

  12. Mansel RE, Fallowfield L, Kissin M, Goyal A, Newcombe RG, Dixon JM, Yiangou C, Horgan K, Bundred N, Monypenny I 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(9):599–609

    Article  PubMed  Google Scholar 

  13. Blanchard DK, Donohue JH, Reynolds C, Grant CS (2003) Relapse and morbidity in patients undergoing sentinel lymph node biopsy alone or with axillary dissection for breast cancer. Arch Surg 138(5):482–487 (discussion 487–488)

    Article  PubMed  Google Scholar 

  14. Verbelen H, Gebruers N, Eeckhout FM, Verlinden K, Tjalma W (2014) Shoulder and arm morbidity in sentinel node-negative breast cancer patients: a systematic review. Breast Cancer Res Treat 144(1):21–31

    Article  PubMed  Google Scholar 

  15. Gebruers N, Verbelen H, De Vrieze T, Coeck D, Tjalma W (2015) Incidence and time path of lymphedema in sentinel node negative breast cancer patients: a systematic review. Arch Phys Med Rehabil 96(6):1131–1139

    Article  PubMed  Google Scholar 

  16. Potosky AL, Riley GF, Lubitz JD, Mentnech RM, Kessler LG (1993) Potential for cancer related health services research using a linked medicare-tumor registry database. Med Care 31(8):732–748

    Article  CAS  PubMed  Google Scholar 

  17. Charlson ME, Pompei P, Ales KL, MacKenzie CR (1987) A new method of classifying prognostic comorbidity in longitudinal studies: development and validation. J Chronic Dis 40(5):373–383

    Article  CAS  PubMed  Google Scholar 

  18. Panageas KS, Schrag D, Riedel E, Bach PB, Begg CB (2003) The effect of clustering of outcomes on the association of procedure volume and surgical outcomes. Ann Intern Med 139(8):658–665

    Article  PubMed  Google Scholar 

  19. Klabunde CN, Potosky AL, Legler JM, Warren JL (2000) Development of a comorbidity index using physician claims data. J Clin Epidemiol 53(12):1258–1267

    Article  CAS  PubMed  Google Scholar 

  20. Porembka MR, Abraham RL, Sefko JA, Deshpande AD, Jeffe DB, Margenthaler JA (2008) Factors associated with lymph node assessment in ductal carcinoma in situ: analysis of 1988–2002 seer data. Ann Surg Oncol 15(10):2709–2719

    Article  PubMed  Google Scholar 

  21. Ponti A, Lynge E, James T, Majek O, von Euler-Chelpin M, Anttila A, Fitzpatrick P, Mano MP, Kawai M, Scharpantgen A et al (2014) International variation in management of screen-detected ductal carcinoma in situ of the breast. Eur J Cancer 50(15):2695–2704

    Article  PubMed  PubMed Central  Google Scholar 

  22. van Steenbergen LN, Voogd AC, Roukema JA, Louwman WJ, Duijm LE, Coebergh JW, van de Poll-Franse LV (2014) Time trends and inter-hospital variation in treatment and axillary staging of patients with ductal carcinoma in situ of the breast in the era of screening in Southern Netherlands. Breast 23(1):63–68

    Article  PubMed  Google Scholar 

  23. Baxter NN, Virnig BA, Durham SB, Tuttle TM (2004) Trends in the treatment of ductal carcinoma in situ of the breast. J Natl Cancer Inst 96(6):443–448

    Article  PubMed  Google Scholar 

  24. Velanovich V, Szymanski W (1999) Quality of life of breast cancer patients with lymphedema. Am J Surg 177(3):184–187 (discussion 188)

    Article  CAS  PubMed  Google Scholar 

  25. Beaulac SM, McNair LA, Scott TE, LaMorte WW, Kavanah MT (2002) Lymphedema and quality of life in survivors of early-stage breast cancer. Arch Surg 137(11):1253–1257

    Article  PubMed  Google Scholar 

  26. Maunsell E, Brisson J, Deschenes L (1993) Arm problems and psychological distress after surgery for breast cancer. Can J Surg J Canadien de Chirurgie 36(4):315–320

    CAS  Google Scholar 

  27. Fleissig A, Fallowfield LJ, Langridge CI, Johnson L, Newcombe RG, Dixon JM, Kissin M, Mansel RE (2006) Post-operative arm morbidity and quality of life. 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(3):279–293

    Article  PubMed  Google Scholar 

  28. Lucci A, McCall LM, Beitsch PD, Whitworth PW, Reintgen DS, Blumencranz PW, Leitch AM, Saha S, Hunt KK, Giuliano AE et al (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 Off J Am Soc Clin Oncol 25(24):3657–3663

    Article  Google Scholar 

  29. Ashikaga T, Krag DN, Land SR, Julian TB, Anderson SJ, Brown AM, Skelly JM, Harlow SP, Weaver DL, Mamounas EP et al (2010) Morbidity results from the NSABP B-32 trial comparing sentinel lymph node dissection versus axillary dissection. J Surg Oncol 102(2):111–118

    Article  PubMed  PubMed Central  Google Scholar 

  30. Langer I, Guller U, Berclaz G, Koechli OR, Schaer G, Fehr MK, Hess T, Oertli D, Bronz L, Schnarwyler B et al (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(3):452–461

    Article  PubMed  PubMed Central  Google Scholar 

  31. Narod SA, Iqbal J, Giannakeas V, Sopik V, Sun P: Breast Cancer Mortality After a Diagnosis of Ductal Carcinoma In Situ. JAMA Oncol 2015

  32. Habel LA, Daling JR, Newcomb PA, Self SG, Porter PL, Stanford JL, Seidel K, Weiss NS (1998) Risk of recurrence after ductal carcinoma in situ of the breast. Cancer Epidemio Biomark Prev Publ Am Assoc Cancer Res Cosponsored Am Soc Prev Oncol 7(8):689–696

    CAS  Google Scholar 

  33. Solin LJ, Fourquet A, Vicini FA, Taylor M, Olivotto IA, Haffty B, Strom EA, Pierce LJ, Marks LB, Bartelink H et al (2005) Long-term outcome after breast-conservation treatment with radiation for mammographically detected ductal carcinoma in situ of the breast. Cancer 103(6):1137–1146

    Article  PubMed  Google Scholar 

  34. Warnberg F, Bergh J, Zack M, Holmberg L (2001) Risk factors for subsequent invasive breast cancer and breast cancer death after ductal carcinoma in situ: a population-based case-control study in Sweden. Cancer Epidemio Biomark Prev Publ Am Assoc Cancer Res Cosponsored Am Soc Prev Oncol 10(5):495–499

    CAS  Google Scholar 

  35. Ernster VL, Barclay J, Kerlikowske K, Grady D, Henderson C (1996) Incidence of and treatment for ductal carcinoma in situ of the breast. JAMA 275(12):913–918

    Article  CAS  PubMed  Google Scholar 

  36. Ernster VL, Barclay J, Kerlikowske K, Wilkie H, Ballard-Barbash R (2000) Mortality among women with ductal carcinoma in situ of the breast in the population-based surveillance, epidemiology and end results program. Arch Intern Med 160(7):953–958

    Article  CAS  PubMed  Google Scholar 

  37. Benson JR, Wishart GC (2013) Predictors of recurrence for ductal carcinoma in situ after breast-conserving surgery. Lancet Oncol 14(9):e348–e357

    Article  PubMed  Google Scholar 

  38. Harding C, Pompei F, Burmistrov D, Welch HG, Abebe R, Wilson R (2015) Breast Cancer Screening, Incidence, and Mortality Across US Counties. JAMA Intern Med 175(9):1483–1489

    Article  PubMed  Google Scholar 

  39. Anderson WF, Jatoi I, Devesa SS (2006) Assessing the impact of screening mammography: breast cancer incidence and mortality rates in Connecticut (1943–2002). Breast Cancer Res Treat 99(3):333–340

    Article  PubMed  Google Scholar 

  40. Welch HG, Black WC (1997) Using autopsy series to estimate the disease “reservoir” for ductal carcinoma in situ of the breast: how much more breast cancer can we find? Ann Intern Med 127(11):1023–1028

    Article  CAS  PubMed  Google Scholar 

  41. Sanders ME, Schuyler PA, Dupont WD, Page DL (2005) The natural history of low-grade ductal carcinoma in situ of the breast in women treated by biopsy only revealed over 30 years of long-term follow-up. Cancer 103(12):2481–2484

    Article  PubMed  Google Scholar 

  42. Romero L, Klein L, Ye W, Holmes D, Soni R, Silberman H, Lagios MD, Silverstein MJ (2004) Outcome after invasive recurrence in patients with ductal carcinoma in situ of the breast. Am J Surg 188(4):371–376

    Article  PubMed  Google Scholar 

  43. Donker M, Litiere S, Werutsky G, Julien JP, Fentiman IS, Agresti R, Rouanet P, de Lara CT, Bartelink H, Duez N et al (2013) Breast-conserving treatment with or without radiotherapy in ductal carcinoma In Situ: 15-year recurrence rates and outcome after a recurrence, from the EORTC 10853 randomized phase III trial. J Clin Oncol Off J Am Soc Clin Oncol 31(32):4054–4059

    Article  Google Scholar 

  44. Esserman L, Yau C: Rethinking the Standard for Ductal Carcinoma In Situ Treatment. JAMA oncology 2015

  45. Wapnir IL, Dignam JJ, Fisher B, Mamounas EP, Anderson SJ, Julian TB, Land SR, Margolese RG, Swain SM, Costantino JP et al (2011) Long-term outcomes of invasive ipsilateral breast tumor recurrences after lumpectomy in NSABP B-17 and B-24 randomized clinical trials for DCIS. J Natl Cancer Inst 103(6):478–488

    Article  PubMed  PubMed Central  Google Scholar 

  46. Dominguez FJ, Golshan M, Black DM, Hughes KS, Gadd MA, Christian R, Lesnikoski BA, Specht M, Michaelson J, Smith BL (2008) Sentinel node biopsy is important in mastectomy for ductal carcinoma in situ. Ann Surg Oncol 15(1):268–273

    Article  PubMed  Google Scholar 

  47. Leonard GD, Swain SM (2004) Ductal carcinoma in situ, complexities and challenges. J Natl Cancer Inst 96(12):906–920

    Article  PubMed  Google Scholar 

  48. Silverstein MJ, Gierson ED, Colburn WJ, Rosser RJ, Waisman JR, Gamagami P (1991) Axillary lymphadenectomy for intraductal carcinoma of the breast. Surg Gynecol Obstet 172(3):211–214

    CAS  PubMed  Google Scholar 

  49. Kotani H, Yoshimura A, Adachi Y, Ishiguro J, Hisada T, Ichikawa M, Gondou N, Hattori M, Kondou N, Sawaki M et al (2014) Sentinel lymph node biopsy is not necessary in patients diagnosed with ductal carcinoma in situ of the breast by stereotactic vacuum-assisted biopsy. Breast cancer

  50. Veronesi P, Intra M, Vento AR, Naninato P, Caldarella P, Paganelli G, Viale G (2005) Sentinel lymph node biopsy for localised ductal carcinoma in situ? Breast 14(6):520–522

    Article  CAS  PubMed  Google Scholar 

  51. Julian TB, Land SR, Fourchotte V, Haile SR, Fisher ER, Mamounas EP, Costantino JP, Wolmark N (2007) Is sentinel node biopsy necessary in conservatively treated DCIS? Ann Surg Oncol 14(8):2202–2208

    Article  PubMed  Google Scholar 

  52. Intra M, Veronesi P, Mazzarol G, Galimberti V, Luini A, Sacchini V, Trifiro G, Gentilini O, Pruneri G, Naninato P et al (2003) Axillary sentinel lymph node biopsy in patients with pure ductal carcinoma in situ of the breast. Arch Surg 138(3):309–313

    Article  PubMed  Google Scholar 

  53. 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

    Article  CAS  PubMed  Google Scholar 

  54. Klauber-DeMore N, Tan LK, Liberman L, Kaptain S, Fey J, Borgen P, Heerdt A, Montgomery L, Paglia M, Petrek JA et al (2000) Sentinel lymph node biopsy: is it indicated in patients with high-risk ductal carcinoma-in situ and ductal carcinoma-in situ with microinvasion? Ann Surg Oncol 7(9):636–642

    Article  CAS  PubMed  Google Scholar 

  55. Lyons JM 3rd, Stempel M, Van Zee KJ, Cody HS 3rd (2012) Axillary node staging for microinvasive breast cancer: is it justified? Ann Surg Oncol 19(11):3416–3421

    Article  PubMed  Google Scholar 

  56. Cox CE, Nguyen K, Gray RJ, Salud C, Ku NN, Dupont E, Hutson L, Peltz E, Whitehead G, Reintgen D et al (2001) Importance of lymphatic mapping in ductal carcinoma in situ (DCIS): why map DCIS? Am Surg 67(6):513–519 (discussion 519–521)

    CAS  PubMed  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Departments of Medicine, Gynecology, and Surgery, and the Herbert Irving Comprehensive Cancer Center, College of Physicians and Surgeons, 161 Ft Washington, New York, NY, 10032, USA

    Ellie J. Coromilas, Jason D. Wright, Yongmei Huang, Sheldon Feldman, Alfred I. Neugut, Ling Chen & Dawn L. Hershman

  2. Department of Epidemiology, Mailman School of Public Health, Columbia University, New York, NY, USA

    Jason D. Wright, Alfred I. Neugut, Grace Clarke Hillyer & Dawn L. Hershman

Authors
  1. Ellie J. Coromilas
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Jason D. Wright
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Yongmei Huang
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Sheldon Feldman
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Alfred I. Neugut
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Grace Clarke Hillyer
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Ling Chen
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Dawn L. Hershman
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Dawn L. Hershman.

Ethics declarations

Conflict of interest

The authors have no conflicts of interest to report.

Funding

Supported by a grant from the Breast Cancer Research Foundation and the American Society of Clinical Oncology (DLH). The Funders have not participated in the conduct of this study. None of the authors have any conflicts to declare with this manuscript.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Coromilas, E.J., Wright, J.D., Huang, Y. et al. Axillary evaluation and lymphedema in women with ductal carcinoma in situ. Breast Cancer Res Treat 158, 373–384 (2016). https://doi.org/10.1007/s10549-016-3890-0

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10549-016-3890-0

Keywords

Search

Navigation