Originally published as JCO Early Release 10.1200/JCO.2002.02.026 on July 9 2002

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Revision of the American Joint Committee on Cancer Staging System for Breast Cancer

From the University of Texas M.D. Anderson Cancer Center and Baylor College of Medicine, Houston, and Scott and White Memorial Hospital, Temple, TX; University of California Los Angeles–Jonsson Comprehensive Cancer Center, Los Angeles, CA; University of Alabama at Birmingham, Birmingham, AL; Memorial Sloan-Kettering Cancer Center, New York, and Roswell Park Cancer Institute, Buffalo, NY; University of Michigan, Ann Arbor, MI; WellStar Kennestone Hospital, Atlanta, GA; International Union Against Cancer representative, Livingston, NJ; Northwestern University, Chicago, IL; Vanderbilt University Medical Center, Nashville, TN; Beth Israel Deaconess Medical Center, Boston, MA; University of Oklahoma Health Science Center, Oklahoma City, OK; University of Vermont, Burlington, VT; National Surgical Adjuvant Breast and Bowel Project, Pittsburgh, PA; and Carolinas Medical Center, Charlotte NC.

This article was published ahead of print at www.jco.org.Address reprint requests to S. Eva Singletary, MD, Department of Surgical Oncology, The University of Texas M.D. Anderson Cancer Center, 1515 Holcombe Blvd, Box 444, Houston, TX 77030-4095; email: esinglet{at}mdanderson.org

	ABSTRACT

TOP ABSTRACT INTRODUCTION THE REVISED TNM STAGING... REFERENCES

 
PURPOSE: To revise the American Joint Committee on Cancer staging system for breast carcinoma.

MATERIALS AND METHODS: A Breast Task Force submitted recommended changes and additions to the existing staging system that were (1) evidence-based and/or consistent with widespread clinical consensus about appropriate diagnostic and treatment standards and (2) useful for the uniform accrual of outcome information in national databases.

RESULTS: Major changes included the following: size-based discrimination between micrometastases and isolated tumor cells; identifiers to indicate usage of innovative technical approaches; classification of lymph node status by number of involved axillary lymph nodes; and new classifications for metastasis to the infraclavicular, internal mammary, and supraclavicular lymph nodes.

CONCLUSION: This revised staging system will be officially adopted for use in tumor registries in January 2003.

	INTRODUCTION

TOP ABSTRACT INTRODUCTION THE REVISED TNM STAGING... REFERENCES

 
TWO YEARS AGO, A Breast Task Force was constituted to serve in an advisory role to the American Joint Committee on Cancer (AJCC) for the revision of the breast cancer chapter in the sixth edition of the Cancer Staging Manual. This task force comprised internationally recognized experts in the field of breast cancer management and was charged with recommending changes to the breast cancer staging system that reflected published clinical data and current treatment standards. The changes recommended by the Breast Task Force were submitted to the AJCC in the fall of 2001 and in the formulation of the final draft of the chapter.

The need for substantive changes in the staging system for breast cancer stemmed from continuing developments in the field of breast cancer diagnosis and management. First, with the now widespread use of screening mammography, most breast tumors are first detected when they are very small. Even among these small tumors, however, there is a remarkable heterogeneity of outcomes. While some can be successfully treated with surgery alone, others are inherently more malignant and, if identified, would justify aggressive treatment. To assist in this differentiation, additional descriptors, including histologic observations or measurement of serum or tumor markers, were suggested to complement the anatomic factors (tumor size, presence of nodal metastasis, presence of distant metastasis) represented in the tumor-node-metastasis (TNM) staging system. Much discussion has centered around whether such factors can predict outcome independently of TNM, and whether they can be reliably measured.

Second, sentinel lymph node dissection has become a treatment standard in the management of early-stage breast cancer, fueling an increased use of immunochemical and molecular techniques for the detection of metastatic tumor deposits. Minute lesions that would have been undetectable 10 years ago are now being considered in clinical treatment decisions, even though data to support such decisions remain scanty. A standard diagnostic approach and nomenclature system is needed to accrue the data that will be necessary to critically analyze the usefulness of these new approaches.

Third, widespread clinical experience, supported by maturing clinical data, has called into question decisions made in the past about the clinical importance of metastases to level III axillary lymph nodes (infraclavicular) and to nodal basins outside of the axilla (eg, supraclavicular, internal mammary [IM]).

Many of these issues were initially addressed during an AJCC consensus conference on cancer prognostic factors held in January 1998.¹ The working group at that conference believed that there were insufficient data to allow the incorporation of serum markers or tumor markers into the TNM system, a conclusion that was later supported in a consensus statement from the College of American Pathologists.² The AJCC working group suggested numerous changes for the TNM system, all of which were considered in depth by the Breast Task Force before final recommendations were made.

The Breast Task Force used the following guidelines in deciding which changes and additions should be made to the TNM staging system for breast cancer. (1) The revisions should be evidence-based, stemming from published clinical outcome data. (2) The revisions should reflect a widespread clinical consensus about appropriate diagnostic and treatment standards. (3) The revisions should result in a nomenclature and coding system that support the uniform accrual of outcome information in national databanks.

	THE REVISED TNM STAGING SYSTEM FOR BREAST CANCER

TOP ABSTRACT INTRODUCTION THE REVISED TNM STAGING... REFERENCES

 
The revised TNM staging system for breast cancer, as approved by the AJCC, is shown in Table 1. Thefinal stage groupings are shown in Table 2. The principle changes in this system, as compared with those presented in the fifth edition of the AJCC Cancer Staging Manual,³ are summarized in Table 3. These changes are of two types. Some reflect the growing use of molecular and immunohistochemical (IHC) technology since the publication of the fifth edition. Most changes proposed in this category define a nomenclature and coding system that will standardize the collection of important data that may affect treatment in the future. Other changes are amendments of prior staging criteria. These amendments were made in cases where clinical evidence or widespread clinical consensus no longer supported a previous criterion. These changes will significantly alter treatment recommendations for certain classes of patients. The new staging system will be officially adopted for use in tumor registries in January 2003.

In the fifth edition of the AJCC Cancer Staging Manual,³ micrometastases were defined as metastatic lesions no larger than 2.0 mm in greatest dimension. Such lesions were recognized as clinically relevant and classified as pN1 in the absence of larger nodal metastases. Is there a lower size limit, below which these lesions are no longer clinically relevant? Unfortunately, there are not yet sufficient data to answer this question. This is due in part to the lack of an adequate system to track these data and in part to the tendency of physicians to treat patients with any IHC-identified nodal lesions as node-positive, regardless of the size of the metastatic lesion. A definitive answer to this question will require the collection of a large body of outcome data in which the distinction between micrometastases and isolated tumor cells has been made according to uniform quantitative criteria. Thus, the sixth edition of the AJCC Cancer Staging Manual^3a has assigned a lower size limit for micrometastases, which are now defined as metastatic lesions that are larger than 0.2 mm in diameter and no larger than 2.0 mm in diameter. These lesions may have histologic evidence of malignant activity, such as proliferation or stromal reaction, but this is not an absolute requirement. Isolated tumor cells (single cells or cell deposits) will now be defined as tumor cell deposits no larger than 0.2 mm in diameter that may or may not (but usually do not) show histologic evidence of malignant activity. Pending further information, isolated tumor cells will be classified as node-negative, because it is believed that the unknown benefits of providing treatment for these small lesions would not outweigh the morbidity caused by the treatment itself.

What if lesions are detected only by IHC staining techniques? H&E staining viewed with conventional light microscopy is the gold standard for the detection of metastatic lesions in the axillary lymph nodes, and it offers more definitive histologic evidence of malignancy than is usually available from IHC preparations. However, IHC staining techniques have been able to detect micrometastases in 12% to 29% of patients who were judged to be node-negative by H&E staining,^4-9 and some studies have shown decreased disease-free survival in patients in whom micrometastases were detected by IHC techniques.^6,8,9 The recommended practice has been to verify the metastatic potential of lesions identified by IHC using follow-up H&E staining, and this is still the preferred approach because of the more detailed cytologic information that can be gained. However, this practice is being abandoned in many clinical venues, reflecting the growing consensus among pathologists that it does not matter how you look for nodal metastases but whether or not you consider them to be clinically significant. Most pathologists favor size of the nodal lesion as the most important criterion of metastatic potential, regardless of how it was detected. Recognizing this, the Breast Task Force nonetheless believed that this was still a sufficiently gray area to warrant some caution. The sixth edition of the AJCC Cancer Staging Manual therefore records an additional descriptor (i) for "immunohistochemical" in cases that are histologically negative by H&E for lymph node metastasis and in which IHC techniques were used. For example, the designation pN0(i+) would indicate a case that was H&E-negative but in which an isolated tumor cell deposit not greater than 0.2 mm in greatest dimension was identified by IHC. Likewise, the designation pN1mi(i+) would indicate a case that was H&E-negative but in which a micrometastasis greater than 0.2 mm but not greater than 2.0 mm in greatest dimension was identified by IHC (Table 1).

Over the last 20 years, the RT-PCR technique has revolutionized the field of molecular biology, and it is likely to have an equally significant effect in clinical medicine. RT-PCR is technically able to identify single cells and has been able to identify neoplastic markers in a significant number of sentinel nodes that were negative for disease by both histologic and IHC staining.¹⁰ However, metastasis is a complex process, and it is unlikely that most of these cells would become clinically significant. For isolated tumor cells in the blood stream, for instance, less than 0.05% survive and form a metastatic focus.¹¹ The sixth edition of the AJCC Cancer Staging Manual designates lesions identified by RT-PCR alone as pN0, the classification they would have had by standard H&E staining. In order to facilitate data collection, an additional descriptor (mol) for "molecular" is used to designate those cases that were histologically negative by H&E staining for regional lymph node metastasis and in which an additional examination for tumor cells was made with RT-PCR (for example, pN0(mol+)).

Number of Involved Axillary Lymph Nodes Clinical consensus has long held that the absolute number of positive axillary lymph nodes is one of the most important prognostic factors in breast cancer. Somewhat surprisingly, this consensus has not been reflected in the AJCC staging system, which has used similar definitions for clinical lymph node status (N) and pathologic lymph node status (pN). Thus, a patient with one positive lymph node and a patient with 10 positive nodes were both classified as N1. The absolute number of positive nodes was relegated to subcategories of the pN1 classification.

In this revision, the pathologic staging system has been reorganized to reflect current clinical practice standards for stratifying patients for prognosis and treatment. Patients with one to three positive axillary lymph nodes (with at least one tumor deposit > 2.0 mm and all tumor deposits > 0.2 mm) are classified as pN1a, patients with four to nine positive axillary lymph nodes are classified as pN2a, and patients with 10 or more positive axillary lymph nodes are classified as pN3a. The decision to divide patients with one to three positive nodes from patients with four or more positive nodes is consistent with the 5-year survival data presented by Carter et al¹² in a study of 24,740 breast cancer cases recorded in the Surveillance, Epidemiology, and End Results program. They grouped patients by tumor size (< 2 cm, 2 to 5 cm, > 5 cm) and found an inverse relationship between overall survival and number of positive nodes in each size group. The decision to separate patients with 10 or more positive axillary lymph nodes into the N3a category reflects common clinical practice^13-16 and is supported by a study of 20,547 cases of breast carcinoma collected by the American College of Surgeons, as reported by Nemoto et al.¹⁷ In that study, the expected survival declined linearly with increasing number of histologically positive axillary lymph nodes, up to a total of 21 positive nodes.

Metastasis to Infraclavicular Lymph Nodes The infraclavicular lymph nodes lie medial to the medial margin of the pectoralis minor muscle. Although grouped with other axillary lymph nodes in previous editions of the AJCC Cancer Staging Manual, clinicians have become increasingly aware that metastasis to the infraclavicular lymph nodes is associated with an extremely poor prognosis. In a recent article by Newman et al,¹⁸ ultrasound was used to detect infraclavicular (level III) disease in patients with locally advanced breast cancer. Nearly one third of these patients had infraclavicular lymph node involvement by ultrasound imaging, and this group showed significantly worse disease-free and overall survival compared with patients with no infraclavicular node involvement (50% v 68% and 58% v 83%, respectively). These findings mirrored the consensus opinion of the Breast Task Force, which recommended that metastasis to the infraclavicular lymph nodes be added to the classification system as N3a.

Metastasis to Nonaxillary Lymph Nodes Lymphatic drainage from the breast occurs primarily to the axillary lymph nodes but can also involve the IM nodes and the supraclavicular lymph nodes (SCLNs). The IM nodes lie in the intercostal spaces along the edge of the sternum in the endothoracic fascia. The SCLNs lie in the supraclavicular fossa, bounded by the omohyoid muscle and tendon, the internal jugular vein, and the clavicle and subclavian vein.

In the fifth edition of the AJCC Cancer Staging Manual,³ metastases to the IM nodes were classified as N3, and this is supported by several studies indicating a poor prognosis in IM-positive versus IM-negative patients. L.L. Douglas (personal communication, November 2002) used data from the National Cancer Data Base (1985 to 1991) to analyze 5-year relative survival rates in all stage IIIB breast cancer patients compared with only those stage IIIB patients who were IM-positive. The survival rates were similar for both groups (47.6% and 45.2%, respectively). Veronesi et al¹⁹ analyzed patients from a randomized trial in which 342 patients were treated with extended mastectomy. Of these, the 5-year overall survival rate was 44% in IM-positive patients compared with 78% in IM-negative patients. In both of these studies, however, IM status was not considered independently of axillary node status. Through a series of studies recently reviewed by Klauber-DeMore et al,²⁰ it has become apparent that the survival impact of positive internal mammary nodes is highly dependent on the status of the other regional nodes. When IM nodes and axillary lymph nodes are considered independently, similar survival rates are seen in IM-positive/axillary lymph node–negative patients compared with IM-negative/axillary lymph node–positive patients. In patients who are both IM-positive and axillary lymph node–positive, there is a significant decrease in survival. Decreased survival is also associated with increased size of the IM nodes. Nodes that are large enough to be detected by clinical examination or imaging studies carry a worse prognosis than nodes detected by sentinel node mapping and not detectable by imaging studies (not including lymphoscintigraphy). To reflect these complex clinical findings, this revision of the AJCC Cancer Staging Manual has been altered as follows: For surgeons who decide to pursue mapping of the IM nodal basin, positive IM nodes detected by sentinel lymph node dissection but not by imaging studies (excluding lymphoscintigraphy) are classified as pN1b in the absence of positive axillary lymph nodes, pN1c in the presence of one to three positive axillary lymph nodes, and pN3b in the presence of four or more positive axillary lymph nodes (to reflect increased tumor burden). Positive IM nodes detected by clinical examination or imaging studies (including computed tomography scanning or ultrasonography but excluding lymphoscintigraphy) are classified as N2b/pN2b in the absence of positive axillary lymph nodes and as N3b/pN3b in the presence of positive axillary lymph nodes.

For almost a century, clinicians have recognized that metastasis to the SCLNs is associated with a poor prognosis, with 5-year survival rates ranging from 5% to 34%.^21,22 Because of this, the fifth edition of the AJCC Cancer Staging Manual classified SCLN metastasis as distant metastasis (M1) rather than as an advanced regional lymph node metastasis (N3). Because patients with distant metastases are considered incurable, this has resulted in the use of largely palliative treatment measures in SCLN-positive patients. The appropriateness of this treatment approach has been called into question by a recent study published by Brito et al.²³ In that study, 70 patients with SCLN-positive breast cancer received aggressive treatment that included induction chemotherapy, surgery, postsurgical chemotherapy, and irradiation. At a median follow-up time of 8.5 years, the disease-free survival and overall survival seen in these patients was equivalent to that seen in stage IIIB patients without distant metastasis and significantly better than that seen in stage IV patients. Thus, classifying SCLN as a distant metastasis may lead to undertreatment of patients. This revision classifies metastasis to the SCLN as N3c/pN3c. A new stage (stage IIIC) has been introduced that includes any T, N3 (pN3a, pN3b, pN3c).

Sentinel Lymph Node Dissection Sentinel lymph node dissection is rapidly becoming the standard of care for clinically node-negative patients with small (T1, T2) tumors.²⁴ Attention is also turning to the use of sentinel lymph node dissection in patients with locally advanced breast cancer who have received preoperative chemotherapy.^25-32 As this transition takes place, however, unanswered questions remain. In many cases in which the sentinel node is positive, it appears to be the only positive node.²⁴ In such cases, what are the clinical implications of omitting axillary dissection? In cases in which occult metastases are found in histologically negative sentinel nodes by IHC staining, will axillary dissection affect survival? Ongoing clinical trials (for example, the Z0010 and Z0011 trials initiated by the American College of Surgeons and the B-32 trial initiated by the National Surgical Adjuvant Breast and Bowel Project) will provide long-term prospective data addressing these questions. Additional data will be available from national databases, facilitated by the addition of appropriate descriptors in the TNM staging system. A case in which the classification is based only on sentinel lymph node dissection will be given the additional designation (sn) for "sentinel node" (for example, pN1 (sn)). In cases in which a preliminary classification was based on sentinel lymph node dissection but a standard axillary lymph node dissection was subsequently performed, the classification is based on the total results of the axillary lymph node dissection (including the sentinel lymph node dissection) and does not carry the (sn) designation.

HISTOLOGIC GRADE
Perhaps the most heavily debated issue considered by the Breast Task Force in revising the AJCC Cancer Staging Manual was whether or not to incorporate histologic grade into the TNM staging system. As early as the 19th century, it was recognized that the morphologic appearance of tumors was related to the degree of malignancy,³³ and formal grading systems date back to the early 20th century.³⁴ Until recently, however, the reproducibility of tumor grading was adversely affected by the variety of approaches used and by the inherently subjective nature of tumor grading. Because the TNM staging system is used for data collection and coding for national cancer registrars, it is critical that the system is reproducible from institution to institution.

To make grading criteria more quantitative, Elston and Ellis³⁵ designed a modification of the Bloom and Richardson grading system. Named the Nottingham combined histologic grade, this new system was based on the semiquantitative evaluation of three morphologic features (percentage of tubule formation, degree of nuclear pleomorphism, and accurate mitotic count in a defined field area). The numerical score assigned to each feature is used in the compilation of an overall grade. In a study of 1,831 patients, Elston and Ellis found a very strong correlation (P < .0001) between long-term survival and Nottingham combined histologic grade.³⁵ Subsequent studies have shown improved interobserver agreement with the Nottingham combined histologic grade compared with other systems,^36-38 and it is recommended by the College of American Pathologists.²

Given that histologic grading as assessed by the Nottingham combined histologic grade has strong prognostic value and improved interobserver reproducibility, how could it best be incorporated into the revision of the TNM staging system? Large tumors (T3, T4) tend to be high grade and nearly always carry a recommendation for adjuvant chemotherapy. Therefore, adding grading information at this end of the existing staging system would not significantly affect treatment decisions. The addition of a histologic grading system would be expected to have the greatest value in making treatment decisions for small (T1, T2), node-negative tumors. Unfortunately, however, the interaction between tumor size and histologic grade as they relate to outcome for these small tumors remains poorly understood. Table 4 shows the results of eight retrospective studies that analyzed outcome as a function of histologic grade in early-stage breast cancer.^39-46 Comparisons among these studies are difficult because of the variety of follow-up times, grading systems, patient samples, and measured outcomes. Grade 1 and grade 3 are clearly differentiated in all studies, but the position of grade 2 is ambiguous, sometimes grouping with grade 1 and sometimes with grade 3. In studies that used the Nottingham combined histologic grade,^42,43,45 grade 2 either clustered with grade 3 or else was intermediate between grade 1 and grade 3. Studies that looked only at the smallest tumors (T1a,b)^41,43,44 tended to show somewhat smaller outcome differences between grade 1 and grade 3 than studies that included larger tumors. The overall sparseness and variability of the information suggests that available data are not yet mature enough to support the addition of histologic grade to the TNM staging system for breast cancer.

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Submitted February 7, 2002; accepted May 22, 2002.

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				C. Liedtke, C. Hatzis, W. F. Symmans, C. Desmedt, B. Haibe-Kains, V. Valero, H. Kuerer, G. N. Hortobagyi, M. Piccart-Gebhart, C. Sotiriou, et al. Genomic Grade Index Is Associated With Response to Chemotherapy in Patients With Breast Cancer J. Clin. Oncol., July 1, 2009; 27(19): 3185 - 3191. [Abstract] [Full Text] [PDF]

				F. Rojo, I. Gonzalez-Navarrete, R. Bragado, A. Dalmases, S. Menendez, M. Cortes-Sempere, C. Suarez, C. Oliva, S. Servitja, V. Rodriguez-Fanjul, et al. Mitogen-Activated Protein Kinase Phosphatase-1 in Human Breast Cancer Independently Predicts Prognosis and Is Repressed by Doxorubicin Clin. Cancer Res., May 15, 2009; 15(10): 3530 - 3539. [Abstract] [Full Text] [PDF]

				J. P. Breyer, M. E. Sanders, D. C. Airey, Q. Cai, B. L. Yaspan, P. A. Schuyler, Q. Dai, F. Boulos, M. G. Olivares, K. M. Bradley, et al. Heritable Variation of ERBB2 and Breast Cancer Risk Cancer Epidemiol. Biomarkers Prev., April 1, 2009; 18(4): 1252 - 1258. [Abstract] [Full Text] [PDF]

				B. Y. Reddy, S. J. Greco, P. S. Patel, K. A. Trzaska, and P. Rameshwar RE-1-silencing transcription factor shows tumor-suppressor functions and negatively regulates the oncogenic TAC1 in breast cancer cells PNAS, March 17, 2009; 106(11): 4408 - 4413. [Abstract] [Full Text] [PDF]

				V. Vinh-Hung, H. M. Verkooijen, G. Fioretta, I. Neyroud-Caspar, E. Rapiti, G. Vlastos, C. Deglise, M. Usel, J.-M. Lutz, and C. Bouchardy Lymph Node Ratio as an Alternative to pN Staging in Node-Positive Breast Cancer J. Clin. Oncol., March 1, 2009; 27(7): 1062 - 1068. [Abstract] [Full Text] [PDF]

				C. H. Ahern and Y. Shen Cost-Effectiveness Analysis of Mammography and Clinical Breast Examination Strategies: A Comparison with Current Guidelines Cancer Epidemiol. Biomarkers Prev., March 1, 2009; 18(3): 718 - 725. [Abstract] [Full Text] [PDF]

				J.-M. Classe, V. Bordes, L. Campion, H. Mignotte, F. Dravet, J. Leveque, C. Sagan, P. F. Dupre, G. Body, and S. Giard Sentinel Lymph Node Biopsy After Neoadjuvant Chemotherapy for Advanced Breast Cancer: Results of Ganglion Sentinelle et Chimiotherapie Neoadjuvante, a French Prospective Multicentric Study J. Clin. Oncol., February 10, 2009; 27(5): 726 - 732. [Abstract] [Full Text] [PDF]

				G. H. Lyman, K. J. Van Zee, and S. B. Edge Impact and Remaining Challenges in the Use of Sentinel Lymph Node Biopsy in Early-stage Breast Cancer ASCO Educational Book, January 1, 2009; 2009(1): 346 - 353. [Abstract] [Full Text] [PDF]

				R. Largillier, J.-M. Ferrero, J. Doyen, J. Barriere, M. Namer, V. Mari, A. Courdi, J. M. Hannoun-Levi, F. Ettore, I. Birtwisle-Peyrottes, et al. Prognostic factors in 1038 women with metastatic breast cancer Ann. Onc., December 1, 2008; 19(12): 2012 - 2019. [Abstract] [Full Text] [PDF]

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				R. C. Chen, N. U. Lin, M. Golshan, J. R. Harris, and J. R. Bellon Internal Mammary Nodes in Breast Cancer: Diagnosis and Implications for Patient Management--A Systematic Review J. Clin. Oncol., October 20, 2008; 26(30): 4981 - 4989. [Abstract] [Full Text] [PDF]

				D. Fuster, J. Duch, P. Paredes, M. Velasco, M. Munoz, G. Santamaria, M. Fontanillas, and F. Pons Preoperative Staging of Large Primary Breast Cancer With [18F]Fluorodeoxyglucose Positron Emission Tomography/Computed Tomography Compared With Conventional Imaging Procedures J. Clin. Oncol., October 10, 2008; 26(29): 4746 - 4751. [Abstract] [Full Text] [PDF]

				C. Nos, G. Kaufmann, K. B. Clough, M.-A. Collignon, E. Zerbib, P. Cusumano, and F. Lecuru Combined Axillary Reverse Mapping (ARM) Technique for Breast Cancer Patients Requiring Axillary Dissection Ann. Surg. Oncol., September 1, 2008; 15(9): 2550 - 2555. [Abstract] [Full Text] [PDF]

				E. A. Rakha, M. E. El-Sayed, A. H.S. Lee, C. W. Elston, M. J. Grainge, Z. Hodi, R. W. Blamey, and I. O. Ellis Prognostic Significance of Nottingham Histologic Grade in Invasive Breast Carcinoma J. Clin. Oncol., July 1, 2008; 26(19): 3153 - 3158. [Abstract] [Full Text] [PDF]

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				A. H. Wu, R. Wang, W.-P. Koh, F. Z. Stanczyk, H.-P. Lee, and M. C. Yu Sleep duration, melatonin and breast cancer among Chinese women in Singapore Carcinogenesis, June 1, 2008; 29(6): 1244 - 1248. [Abstract] [Full Text] [PDF]

				V. Ludovini, S. Gori, M. Colozza, L. Pistola, E. Rulli, I. Floriani, E. Pacifico, F. R. Tofanetti, A. Sidoni, C. Basurto, et al. Evaluation of serum HER2 extracellular domain in early breast cancer patients: correlation with clinicopathological parameters and survival Ann. Onc., May 1, 2008; 19(5): 883 - 890. [Abstract] [Full Text] [PDF]

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				W. F. Symmans, F. Peintinger, C. Hatzis, R. Rajan, H. Kuerer, V. Valero, L. Assad, A. Poniecka, B. Hennessy, M. Green, et al. Measurement of Residual Breast Cancer Burden to Predict Survival After Neoadjuvant Chemotherapy J. Clin. Oncol., October 1, 2007; 25(28): 4414 - 4422. [Abstract] [Full Text] [PDF]

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				R. T. Chlebowski, G. L. Blackburn, C. A. Thomson, D. W. Nixon, A. Shapiro, M. K. Hoy, M. T. Goodman, A. E. Giuliano, N. Karanja, P. McAndrew, et al. Dietary Fat Reduction and Breast Cancer Outcome: Interim Efficacy Results From the Women's Intervention Nutrition Study J Natl Cancer Inst, December 20, 2006; 98(24): 1767 - 1776. [Abstract] [Full Text] [PDF]

				P. Querzoli, M. Pedriali, R. Rinaldi, A. R. Lombardi, E. Biganzoli, P. Boracchi, S. Ferretti, C. Frasson, C. Zanella, S. Ghisellini, et al. Axillary Lymph Node Nanometastases Are Prognostic Factors for Disease-Free Survival and Metastatic Relapse in Breast Cancer Patients. Clin. Cancer Res., November 15, 2006; 12(22): 6696 - 6701. [Abstract] [Full Text] [PDF]

				A. L. Moharita, M. Taborga, K. E. Corcoran, M. Bryan, P. S. Patel, and P. Rameshwar SDF-1{alpha} regulation in breast cancer cells contacting bone marrow stroma is critical for normal hematopoiesis Blood, November 15, 2006; 108(10): 3245 - 3252. [Abstract] [Full Text] [PDF]

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				W. A. Woodward, V. Vinh-Hung, N. T. Ueno, Y. C. Cheng, M. Royce, P. Tai, G. Vlastos, A. M. Wallace, G. N. Hortobagyi, and Y. Nieto Prognostic Value of Nodal Ratios in Node-Positive Breast Cancer J. Clin. Oncol., June 20, 2006; 24(18): 2910 - 2916. [Abstract] [Full Text] [PDF]

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				S. P. Linke, T. M. Bremer, C. D. Herold, G. Sauter, and C. Diamond A Multimarker Model to Predict Outcome in Tamoxifen-Treated Breast Cancer Patients Clin. Cancer Res., February 15, 2006; 12(4): 1175 - 1183. [Abstract] [Full Text] [PDF]

				B. Gerber, A. Krause, T. Reimer, I. Mylonas, J. Makovitzky, G. Kundt, and W. Janni Anastrozole versus Tamoxifen Treatment in Postmenopausal Women with Endocrine-Responsive Breast Cancer and Tamoxifen-Induced Endometrial Pathology Clin. Cancer Res., February 15, 2006; 12(4): 1245 - 1250. [Abstract] [Full Text] [PDF]

				G. Falconieri, S. Pizzolitto, and G. Gentile Comprehensive Examination of Sentinel Lymph Node in Breast Cancer: A Solution Without a Problem? International Journal of Surgical Pathology, January 1, 2006; 14(1): 1 - 8. [Abstract] [PDF]

				S. E. Singletary and J. L. Connolly Breast Cancer Staging: Working With the Sixth Edition of the AJCC Cancer Staging Manual CA Cancer J Clin, January 1, 2006; 56(1): 37 - 47. [Abstract] [Full Text] [PDF]

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				D. A. Stewart, A. H. G. Paterson, J. D. Ruether, J. Russell, P. Craighead, M. Smylie, and J. Mackey High-dose mitoxantrone-vinblastine-cyclophosphamide and autologous stem cell transplantation for stage III breast cancer: final results of a prospective multicentre study Ann. Onc., September 1, 2005; 16(9): 1463 - 1468. [Abstract] [Full Text] [PDF]

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				M. Panades, I. A. Olivotto, C. H. Speers, T. Shenkier, T. A. Olivotto, L. Weir, S. J. Allan, and P. T. Truong Evolving Treatment Strategies for Inflammatory Breast Cancer: A Population-Based Survival Analysis J. Clin. Oncol., March 20, 2005; 23(9): 1941 - 1950. [Abstract] [Full Text] [PDF]

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