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Figure 1.
Nodal involvement by hormone receptor status in 163 patients with T1a or T1b breast cancer. ER indicates estrogen receptor; PR, progesterone receptor; plus sign, positive; and minus sign, negative.

Nodal involvement by hormone receptor status in 163 patients with T1a or T1b breast cancer. ER indicates estrogen receptor; PR, progesterone receptor; plus sign, positive; and minus sign, negative.

Figure 2.
Nodal involvement by tumor size. Shaded areas indicate absolute numbers of patients with lymph node involvement in each tumor size group (corresponding to the percentages above each bar).

Nodal involvement by tumor size. Shaded areas indicate absolute numbers of patients with lymph node involvement in each tumor size group (corresponding to the percentages above each bar).

Figure 3.
Nodal involvement by tumor grade. Relationship between nodal involvement and tumor grade was significant (P = .02).

Nodal involvement by tumor grade. Relationship between nodal involvement and tumor grade was significant (P = .02).

Table 1. 
Tumor Characteristics Stratified by Tumor Size*
Tumor Characteristics Stratified by Tumor Size*
Table 2. 
Incidence of Axillary Lymph Node Metastases for T1a and T1b Invasive Breast Cancer
Incidence of Axillary Lymph Node Metastases for T1a and T1b Invasive Breast Cancer
1.
Siegel  BMMayzel  KALove  SM Level I and II axillary dissection in the treatment of early-stage breast cancer: an analysis of 259 consecutive patients. Arch Surg. 1990;1251144- 1147Article
2.
Moore  MPKinne  DW Axillary lymphadenectomy: a diagnostic and therapeutic procedure. J Surg Oncol. 1997;662- 6Article
3.
Perez  EA The role of axillary node dissection in patients with invasive breast cancer: a medical oncology perspective.  Program and abstracts of the 80th International Congress on Anti-Cancer Treatment February 3-6, 1998 Paris, France124
4.
Cady  B Is axillary lymph node dissection necessary in routine management of breast cancer? no. Important Adv Oncol. 1996;12251- 265
5.
McGuire  WLClark  GM Prognostic factors and treatment decisions in axillary-node–negative breast cancer. N Engl J Med. 1992;3261756- 1761Article
6.
Warmuth  MABowen  GProsnitz  LR  et al.  Complications of axillary lymph node dissection for carcinoma of the breast: a report based on a patient survey. Cancer. 1998;831362- 1368Article
7.
Hortobagyi  GNSingletary  SEStrom  EA Treatment of locally advanced and inflammatory breast cancer. Harris  JLippman  MMorrow  MOsborne  CKDiseases of the Breast. Philadelphia, Pa Lippincott Williams & Wilkins2000;645- 660
8.
Silverstein  MJGierson  EDWaisman  JRSenofsky  GMColburn  WJGamagami  P Axillary lymph node dissection for T1a breast carcinoma: is it indicated? Cancer. 1994;73664- 667Article
9.
Pandelidis  SMPeters  KLWalusimbi  MS  et al.  The role of axillary dissection in mammographically detected carcinoma. J Am Coll Surg. 1997;184341- 345
10.
Chontos  AJMaher  DPRatzer  ERFenoglio  ME Axillary lymph node dissection: is it required in T1a breast cancer? J Am Coll Surg. 1997;184493- 498
11.
Barth  ACraig  PHSilverstein  MJ Predictors of axillary lymph node metastases in patients with T1 breast carcinoma. Cancer. 1997;791918- 1922Article
12.
White  REVezeridis  MPKonstadoulakis  MCole  BFWanebo  HJBland  KI Therapeutic options and results for the management of minimally invasive carcinoma of the breast: influence of axillary dissection for treatment of T1a and T1b lesions. J Am Coll Surg. 1996;183575- 582
13.
Mustafa  IACole  BWanebo  HJBland  KIChang  HR The impact of histopathology on nodal metastases in minimal breast cancer. Arch Surg. 1997;132384- 391Article
14.
McGee  JMYoumans  RClingan  FMalnar  KBellefeuille  CBerry  B The value of axillary dissection in T1a breast cancer. Am J Surg. 1996;172501- 504Article
15.
Mann  GBPort  ERRizza  CTan  LKBorgen  PIVan Zee  KJ Six-year follow-up of patients with microinvasive, T1a and T1b breast carcinoma. Ann Surg Oncol. 1999;6591- 598Article
16.
Port  ERTan  LKBorgen  PIVan Zee  KJ Incidence of axillary lymph node metastases in T1a and T1b breast carcinoma. Ann Surg Oncol. 1998;523- 27Article
17.
Parmigiani  GBerry  DAWiner  EPTebaldi  CIglehart  JDProsnitz  LR Is axillary lymph node dissection indicated for early-stage breast cancer? A decision analysis. J Clin Oncol. 1999;171465- 1473
18.
Carter  CLAllen  CHenson  DE Relation of tumor size, lymph node status, and survival in 24,740 breast cancer cases. Cancer. 1989;63181- 187Article
19.
Conover  WJed Practical Nonparametric Statistics. 2nd ed. New York, NY John Wiley & Sons1980;
20.
Walker  SHDuncan  DB Estimation of the probability of an event as a function of several independent variables. Biometrika. 1967;54167- 179Article
21.
Krag  DWeaver  DAshikaga  T  et al.  The sentinel node in breast cancer: a multicenter validation study. N Engl J Med. 1998;339941- 946Article
22.
Giuliano  AEKirgan  DMGuenther  JMMorton  DL Lymphatic mapping and sentinel lymphadenectomy for breast cancer. Ann Surg. 1994;220391- 398Article
23.
Bass  SSDauway  EMahatme  A  et al.  Lymphatic mapping with sentinel lymph node biopsy in patients with breast cancers <1 centimeter (T1A-T1B). Am Surg. 1999;65857- 861
24.
Veronesi  UPaganelli  GViale  G  et al.  Sentinel lymph node biopsy and axillary dissection in breast cancer: results in a large series. J Natl Cancer Inst. 1999;91368- 373Article
25.
Cody  HSHill  ADTran  KN  et al.  Credentialing for breast lymphatic mapping: how many cases are enough? Ann Surg. 1999;229723- 726Article
Original Article
July 2001

Role of Axillary Node Dissection in Patients With T1a and T1b Breast CancerMayo Clinic Experience

Author Affiliations

From the Division of General Internal Medicine (Dr Mincey), Department of Surgery (Dr Bammer), and Division of Hematology/Oncology (Dr Perez), Mayo Clinic, Jacksonville, Fla; and Section of Biostatistics, Mayo Clinic and Mayo Foundation, Rochester, Minn (Ms Atkinson).

Arch Surg. 2001;136(7):779-782. doi:10.1001/archsurg.136.7.779
Abstract

Hypothesis  The incidence of nodal positivity in patients with early breast cancer is low, and axillary lymph node dissection may not be justified in all such patients.

Design  Retrospective case series.

Setting  Tertiary institution.

Patients  All patients with T1a and T1b breast cancer who had both primary breast surgery and axillary lymph node dissection at Mayo Clinic in Jacksonville, Fla, from January 1, 1992, through February 28, 1998.

Interventions  None.

Main Outcome Measures  Tumor size and biological grade, estrogen and progesterone receptor status, number of nodes harvested, and number of nodes positive for disease.

Results  Of 163 patients studied, 39 had T1a and 124 had T1b tumors. Node positivity was 0% for T1a and 11.3% for T1b tumors (P = .03). Lymph node involvement and estrogen receptor status were not related (P = .29). However, the risk of lymph node positivity for progesterone receptor–negative (P = .01) and estrogen receptor–negative/progesterone receptor–negative tumors was significantly higher than for progesterone and estrogen/progesterone receptor–positive tumors (P = .04). Furthermore, the risk of lymph node positivity was significantly higher as tumor size increased (P = .002). Finally, higher tumor grade conferred a higher risk of lymph node involvement (P = .02).

Conclusions  T1a tumors have minimal risk of nodal positivity and may not require subsequent axillary lymph node dissection in the future. T1b tumors should be managed with routine analysis of axillary lymph node status. Whether sentinel node mapping can change this standard awaits further study.

INITIAL MANAGEMENT of invasive breast cancer involves a surgical procedure to establish local control and to determine the presence or absence of risk factors for recurrence, knowledge of which is used to guide subsequent management decisions. Currently, axillary lymph node dissection (ALND), with a minimum of 10 nodes harvested from axillary levels I and II, is a standard part of surgical treatment for patients with invasive breast cancer, regardless of tumor size. The continued inclusion of complete ALND in patients with small tumors (≤10 mm) has been a subject of controversy for several years.114 Some authors have suggested that the incidence of node positivity is so low that routine ALND should be eliminated. Others have maintained that it should remain the standard of care because of its role in determining prognosis and making decisions about adjuvant systemic therapy.

Nodal status is the most important prognostic factor for patients with resectable breast cancer.3,5,7 However, ALND probably contributes very little to overall survival and is associated with considerable morbidity and a potential decrease in quality of life.58 Warmuth et al6 showed that numbness or pain develops in 33% of patients and arm edema in 15%; 8% have limitation of arm movement and report episodes of infection or inflammation after ALND.

Some authors have reported a low incidence of axillary lymph node involvement in small tumors, but results have varied widely among different single-institution studies. Axillary node involvement has been documented in as few as 3% and as many as 23% of patients with T1a (≤5-mm) or T1b (6- to 10-mm) tumors.817 Of the 339 T1a tumors analyzed in the Surveillance, Epidemiology, and End Results Program of the National Cancer Institute, 20.6% of the nodes were positive for disease.18 Chontos et al10 suggested that the data from the Surveillance, Epidemiology, and End Result Program were flawed, because histologic confirmation of axillary lymph node status was not required. White et al12 reported that patients with T1a and T1b tumors who did not undergo ALND had a reduction in overall, disease-free, and breast cancer–specific survival compared with that of patients with similar tumor stage who had pathological assessment of axillary lymph node status by dissection.

The aim of our study was to develop an institutional database of lymph node status based on the size of the primary breast cancer as an aid to making future decisions about management of T1a and T1b tumors.

PATIENTS AND METHODS

All patients with T1a or T1b tumors treated at Mayo Clinic, Jacksonville, Fla, from January 1, 1992, to February 28, 1998, were identified through the Mayo Clinic Tumor Registry. Each medical record was reviewed and the following data were recorded: tumor size, histologic type, tumor grade, hormone receptor (estrogen [ER] and progesterone [PR]) status, number of harvested nodes, and number of nodes positive for disease.

We examined the influence of ER and PR status, tumor size (both grouped and continuous) and grade, and number of nodes pathologically evaluated on the likelihood of finding at least 1 lymph node positive for disease. The χ2 test was used to measure the association of axillary lymph node positivity with hormone receptor status.19 The Wilcoxon rank sum test was used to measure the association of axillary lymph node positivity with tumor size, tumor grade, and number of lymph nodes examined.19 Stepwise logistic regression analysis was used to determine the set of variables that best predicted lymph node involvement.20

RESULTS

From January 1, 1992, through February 28, 1998, 50 patients with T1a breast cancer and 144 with T1b breast cancer underwent lumpectomy or mastectomy with ALND at Mayo Clinic. Two of the 194 patients were men. Four observations were documented from 2 women, each of whom had 2 tumors. Of the 194 patients, 163 had data available about nodal status. Thus, the rest of the analysis was concerned only with these patients. For all patients, the median number of lymph nodes harvested was 13 (range, 2-42). Lymph node involvement was documented in 8.6% of the entire group of patients (n = 163) with T1a and T1b tumors (Table 1). None of the patients with T1a tumors had documented lymph node involvement, but of those with T1b tumors, 11.3% had at least 1 lymph node positive for malignancy (P = .03). T1a tumors were ER positive in 74.3% of patients, PR positive in 94.3%, and ER/PR positive in 74.3%; T1b tumors were ER positive in 88.8%, PR positive in 86.2%, and ER/PR positive in 80.2%. The association between ER status and axillary lymph node positivity was not significant (P = .29 for difference in nodal status between patients with ER-negative tumors and those with ER-positive ones) (Figure 1). However, there was a significantly higher risk (P = .01) for nodal involvement in patients with PR-negative tumors (23.5% were node positive) than in those with PR-positive tumors (6.0% were node positive), and in patients with ER/PR-negative tumors compared with those with ER/PR-positive tumors (25.0% vs 5.9%; P = .04).

Axillary lymph node involvement was correlated with larger tumor size (median, 10 mm vs 8 mm; P = .002; Figure 2). Of 14 tumors with positive lymph nodes, 11 tumors had a diameter of 10 mm. Node-positive tumors also had higher histologic grade: 10 of 14 node-positive tumors were grade 3 or higher (P = .02; Figure 3). No histologic tumor type demonstrated higher risk of lymph node involvement. After adjustment for tumor size in the multivariate analysis, only the number of nodes examined predicted for axillary node positivity.

COMMENT

The need for ALND in the management of T1a or T1b breast tumors is controversial. Other investigators have reported axillary node positivity rates of 3% to 12% for T1a and 11% to 23% for T1b tumors (Table 2). In our study, pathological evaluation of axillary lymph nodes had the potential to change prognosis and to affect the use of adjuvant systemic therapy in patients with T1b tumors, but not in those with T1a tumors. Our finding of a relationship between PR status and lymph node positivity should be corroborated in larger data sets.

Although ALND may provide important prognostic information with therapeutic implications, its associated morbidity and added financial cost make it a less than ideal test.4 Also, ALND confers significant morbidity, with 10% to 20% of patients having decreased range of motion of the shoulder, an approximately 80% rate of numbness in the distribution of the intercostal brachial nerves, and a 2% to 30% incidence of arm edema.4,6,10 Our data suggest that routine ALND may not be indicated in patients with T1a invasive breast cancer, but it is useful in those with T1b tumors.

In the future, sentinel lymph node detection (SLND) and biopsy are likely to be an alternative to ALND for many women in whom the sentinel node is negative. The rationale, technique, sensitivity, and specificity of SLND have been discussed elsewhere.2125 In expert hands, this procedure identifies the sentinel node in more than 90% of women. However, several facts need to be acknowledged before sentinel lymph node detection is considered a standard substitute for ALND. The procedure can be technically challenging, and both the location of the primary tumor and the experience of the multidisciplinary team (surgeon, nuclear medicine physician, and pathologist) influence its accuracy. The type of pathological evaluation (the standard hematoxylin-eosin stain vs immunohistochemistry and polymerase chain reaction) might influence the positivity rate. The effect on prognosis of lymph node positivity detected by immunohistochemistry or polymerase chain reaction and the subsequent implication for adjuvant therapy for patients who have had SLND as the only method to assess axillary status is uncertain. Therefore, before SLND may be considered the standard of care, it should be performed as part of clinical studies until it has been demonstrated to be accurate enough for the individual practicing surgeon.

We propose to continue to assess the nodal status of patients with small invasive breast cancer (especially those with T1b tumors) until data suggesting the validity of SLND allow it to be the new standard of care. We anticipate that SLND will soon replace the old standard of ALND as the procedure of choice.

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Article Information

We thank Lenay Washington for her expert secretarial assistance in preparation of the manuscript.

Corresponding author and reprints: Edith A. Perez, MD, Division of Hematology/Oncology, Mayo Clinic, 4500 San Pablo Rd, Jacksonville, FL 32224 (e-mail: perez.edith@mayo.edu).

References
1.
Siegel  BMMayzel  KALove  SM Level I and II axillary dissection in the treatment of early-stage breast cancer: an analysis of 259 consecutive patients. Arch Surg. 1990;1251144- 1147Article
2.
Moore  MPKinne  DW Axillary lymphadenectomy: a diagnostic and therapeutic procedure. J Surg Oncol. 1997;662- 6Article
3.
Perez  EA The role of axillary node dissection in patients with invasive breast cancer: a medical oncology perspective.  Program and abstracts of the 80th International Congress on Anti-Cancer Treatment February 3-6, 1998 Paris, France124
4.
Cady  B Is axillary lymph node dissection necessary in routine management of breast cancer? no. Important Adv Oncol. 1996;12251- 265
5.
McGuire  WLClark  GM Prognostic factors and treatment decisions in axillary-node–negative breast cancer. N Engl J Med. 1992;3261756- 1761Article
6.
Warmuth  MABowen  GProsnitz  LR  et al.  Complications of axillary lymph node dissection for carcinoma of the breast: a report based on a patient survey. Cancer. 1998;831362- 1368Article
7.
Hortobagyi  GNSingletary  SEStrom  EA Treatment of locally advanced and inflammatory breast cancer. Harris  JLippman  MMorrow  MOsborne  CKDiseases of the Breast. Philadelphia, Pa Lippincott Williams & Wilkins2000;645- 660
8.
Silverstein  MJGierson  EDWaisman  JRSenofsky  GMColburn  WJGamagami  P Axillary lymph node dissection for T1a breast carcinoma: is it indicated? Cancer. 1994;73664- 667Article
9.
Pandelidis  SMPeters  KLWalusimbi  MS  et al.  The role of axillary dissection in mammographically detected carcinoma. J Am Coll Surg. 1997;184341- 345
10.
Chontos  AJMaher  DPRatzer  ERFenoglio  ME Axillary lymph node dissection: is it required in T1a breast cancer? J Am Coll Surg. 1997;184493- 498
11.
Barth  ACraig  PHSilverstein  MJ Predictors of axillary lymph node metastases in patients with T1 breast carcinoma. Cancer. 1997;791918- 1922Article
12.
White  REVezeridis  MPKonstadoulakis  MCole  BFWanebo  HJBland  KI Therapeutic options and results for the management of minimally invasive carcinoma of the breast: influence of axillary dissection for treatment of T1a and T1b lesions. J Am Coll Surg. 1996;183575- 582
13.
Mustafa  IACole  BWanebo  HJBland  KIChang  HR The impact of histopathology on nodal metastases in minimal breast cancer. Arch Surg. 1997;132384- 391Article
14.
McGee  JMYoumans  RClingan  FMalnar  KBellefeuille  CBerry  B The value of axillary dissection in T1a breast cancer. Am J Surg. 1996;172501- 504Article
15.
Mann  GBPort  ERRizza  CTan  LKBorgen  PIVan Zee  KJ Six-year follow-up of patients with microinvasive, T1a and T1b breast carcinoma. Ann Surg Oncol. 1999;6591- 598Article
16.
Port  ERTan  LKBorgen  PIVan Zee  KJ Incidence of axillary lymph node metastases in T1a and T1b breast carcinoma. Ann Surg Oncol. 1998;523- 27Article
17.
Parmigiani  GBerry  DAWiner  EPTebaldi  CIglehart  JDProsnitz  LR Is axillary lymph node dissection indicated for early-stage breast cancer? A decision analysis. J Clin Oncol. 1999;171465- 1473
18.
Carter  CLAllen  CHenson  DE Relation of tumor size, lymph node status, and survival in 24,740 breast cancer cases. Cancer. 1989;63181- 187Article
19.
Conover  WJed Practical Nonparametric Statistics. 2nd ed. New York, NY John Wiley & Sons1980;
20.
Walker  SHDuncan  DB Estimation of the probability of an event as a function of several independent variables. Biometrika. 1967;54167- 179Article
21.
Krag  DWeaver  DAshikaga  T  et al.  The sentinel node in breast cancer: a multicenter validation study. N Engl J Med. 1998;339941- 946Article
22.
Giuliano  AEKirgan  DMGuenther  JMMorton  DL Lymphatic mapping and sentinel lymphadenectomy for breast cancer. Ann Surg. 1994;220391- 398Article
23.
Bass  SSDauway  EMahatme  A  et al.  Lymphatic mapping with sentinel lymph node biopsy in patients with breast cancers <1 centimeter (T1A-T1B). Am Surg. 1999;65857- 861
24.
Veronesi  UPaganelli  GViale  G  et al.  Sentinel lymph node biopsy and axillary dissection in breast cancer: results in a large series. J Natl Cancer Inst. 1999;91368- 373Article
25.
Cody  HSHill  ADTran  KN  et al.  Credentialing for breast lymphatic mapping: how many cases are enough? Ann Surg. 1999;229723- 726Article
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