Lymph-node metastases in invasive lobular carcinoma are different from those in ductal carcinoma of the breast

Journal of Clinical Pathology

Volumn 64, Issue 11, 2011, Pages 995-1000

  Fernández, Beatriz ^a   Paish, E Claire ^a   Green, Andrew R ^a   Lee, Andrew H S ^a   Macmillan, R Douglas ^a   Ellis, Ian O ^a   Rakha, Emad A ^a  

^a NOTTINGHAM UNIVERSITY HOSPITALS NHS TRUST   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

ARTICLE; AXILLARY LYMPH NODE; BREAST CARCINOMA; CANCER GRADING; CANCER RECURRENCE; CANCER STAGING; CANCER SURVIVAL; CLINICAL FEATURE; CONTROLLED STUDY; FEMALE; HISTOPATHOLOGY; HUMAN; HUMAN TISSUE; INTRADUCTAL CARCINOMA; INVASIVE CARCINOMA; LYMPH NODE METASTASIS; MAJOR CLINICAL STUDY; PRIORITY JOURNAL;

ADULT; AGED; AXILLA; BREAST NEOPLASMS; CARCINOMA, DUCTAL, BREAST; CARCINOMA, LOBULAR; FEMALE; HUMANS; LYMPHATIC METASTASIS; MIDDLE AGED; PROGNOSIS; SURVIVAL ANALYSIS;

EID: 80054896999     PISSN: 00219746     EISSN: 14724146     Source Type: Journal    
DOI: 10.1136/jclinpath-2011-200151     Document Type: Article

References (62)

1. Sastre-Garau X, Jouve M, Asselain B, et al. Infiltrating lobular carcinoma of the breast. Clinicopathologic analysis of 975 cases with reference to data on conservative therapy and metastatic patterns. Cancer 1996;77:113-20. (Pubitemid 26002745)
2. Li CI, Anderson BO, Daling JR, et al. Trends in incidence rates of invasive lobular and ductal breast carcinoma. JAMA 2003;289:1421-4. (Pubitemid 37430310)
3. Arpino G, Bardou VJ, Clark GM, et al. Infiltrating lobular carcinoma of the breast: tumor characteristics and clinical outcome. Breast Cancer Res 2004;6:R149-56.
4. Rakha EA, El-Sayed ME, Powe DG, et al. Invasive lobular carcinoma of the breast: response to hormonal therapy and outcomes. Eur J Cancer 2008;44:73-83. (Pubitemid 350256943)
5. Chikman B, Lavy R, Davidson T, et al. Factors affecting rise in the incidence of infiltrating lobular carcinoma of the breast. Isr Med Assoc J 2010;12:697-700.
6. Lamovec J, Bracko M. Metastatic pattern of infiltrating lobular carcinoma of the breast: an autopsy study. J Surg Oncol 1991;48:28-33.
7. Poen JC, Tran L, Juillard G, et al. Conservation therapy for invasive lobular carcinoma of the breast. Cancer 1992;69:2789-95.
8. Silverstein MJ, Lewinsky BS, Waisman JR, et al. Infiltrating lobular carcinoma. Is it different from infiltrating duct carcinoma? Cancer 1994;73:1673-7. (Pubitemid 24085268)
9. Soslow RA, Carlson DL, Horenstein MG, et al. A comparison of cell cycle markers in well-differentiated lobular and ductal carcinomas. Breast Cancer Res Treat 2000;61:161-70. (Pubitemid 30456236)
10. Coradini D, Pellizzaro C, Veneroni S, et al. Infiltrating ductal and lobular breast carcinomas are characterised by different interrelationships among markers related to angiogenesis and hormone dependence. Br J Cancer 2002;87;1105-11. (Pubitemid 35418105)
11. Ferlicot S, Vincent-Salomon A, Medioni J, et al. Wide metastatic spreading in infiltrating lobular carcinoma of the breast. Eur J Cancer 2004;40:336-41. (Pubitemid 38121269)
12. Molland JG, Donnellan M, Janu NC, et al. Infiltrating lobular carcinomada comparison of diagnosis, management and outcome with infiltrating duct carcinoma. Breast 2004;13:389-96. (Pubitemid 39549788)
13. Jayasinghe UW, Bilous AM, Boyages J. Is survival from infiltrating lobular carcinoma of the breast different from that of infiltrating ductal carcinoma? Breast J 2007;13:479-85. (Pubitemid 47329335)
14. Lee JH, Park S, Park HS, et al. Clinicopathological features of infiltrating lobular carcinomas comparing with infiltrating ductal carcinomas: a case control study. World J Surg Oncol 2010;8:34.
15. Wasif N, Maggard MA, Ko CY, et al. Invasive lobular vs. ductal breast cancer: a stage-matched comparison of outcomes. Ann Surg Oncol 2010;17:1862-9.
16. Casolo P, Raspadori A, Drei B, et al. [Natural history of breast cancer: lobular carcinoma versus ductal carcinoma in our experience]. Ann Ital Chir 1997;68:43-7;discussion 48. [in Italian].
17. Mersin H, Yildirim E, Gülben K, et al. Is invasive lobular carcinoma different invasive ductal carcinoma? Eur J Surg Oncol 2003;29:390-5. (Pubitemid 36675699)
18. Classe JM, Loussouarn D, Campion L, et al. Validation of axillary sentinel lymph node detection in the staging of early lobular invasive breast carcinoma. Cancer 2004;100:935-41. (Pubitemid 38222853)
19. Hsiao YH, Tsai HD, Chou MC, et al. The myoepithelial cell layer may serve as a potential factor for different outcomes of sage-matched invasive lobular and ductal breast cancers. Int J Biol Sci 2011;7:147-53.
20. Truong PT, Berthelet E, Lee J, et al. The prognostic significance of the percentage of positive/dissected axillary lymph nodes in breast cancer recurrence and survival in patients with one to three positive axillary lymph nodes. Cancer 2005;103:2006-14. (Pubitemid 40605106)
21. Fitzgibbons PL, Page DL, Weaver D, et al. Prognostic factors in breast cancer. College of American Pathologists Consensus Statement 1999. Arch Pathol Lab Med 2000;124:966-78.
22. Singletary SE, Allred C, Ashley P, et al. Revision of the American Joint Committee on Cancer staging system for breast cancer. J Clin Oncol 2002;20:3628-36. (Pubitemid 34983222)
23. Galea MH, Blamey RW, Elston CE, et al. The Nottingham Prognostic Index in primary breast cancer. Breast Cancer Res Treat 1992;22:207-19.
24. Carter CL, Allen C, Henson DE. Relation of tumor size, lymph node status and survival in 24,740 breast cancer cases. Cancer 1989;63:181-7. (Pubitemid 19032001)
25. Axelsson CK, Mouridsen HT, Zedeler K. Axillary dissection of level I and II lymph nodes is important in breast cancer classification. The Danish Breast Cancer Cooperative Group (DBCCG). Eur J Cancer 1992;28:1415-18.
26. Voordeckers M, Vinh-Hung V, Van de Steene J, et al. The lymph node ratio as prognostic factor in node-positive breast cancer. Radiother Oncol 2004;70:225-30. (Pubitemid 38520153)
27. Edge SB, Byrd DR, Compton CC, et al. AJCC Cancer Staging Manual. 7th edn. New York: Springer, 2010.
28. Vinh-Hung V, Verschraegen C, Promish DI, et al. Ratios of involved nodes in early breast cancer. Breast Cancer Res 2004;6:R680-8.
29. Woodward WA, Vinh-Hung V, Ueno NT, et al. Prognostic value of nodal ratios in node-positive breast cancer. J Clin Oncol 2006;24:2910-16. (Pubitemid 46630594)
30. Vinh-Hung V, Verkooijen HM, Fioretta G, et al. Lymph node ratio as an alternative to pN staging in node-positive breast cancer. J Clin Oncol 2009;27:1062-8.
31. van der Wal BC, Butzelaar RM, van der Meij S, et al. Axillary lymph node ratio and total number of removed lymph nodes: predictors of survival in stage I and II breast cancer. Eur J Surg Oncol 2002;28:481-9. (Pubitemid 35446775)
32. Megale Costa LJ, Soares HP, Gaspar HA, et al. Ratio between positive lymph nodes and total dissected axillary lymph nodes as an independent prognostic factor for disease-free survival in patients with breast cancer. Am J Clin Oncol 2004;27:304-6. (Pubitemid 38737808)
33. Lale Atahan I, Yildiz F, Ozyigit G, et al. Percent positive axillary lymph node metastasis predicts survival in patients with non-metastatic breast cancer. Acta Oncol 2008;47:232-8. (Pubitemid 351164892)
34. Hatoum HA, Jamali FR, El-Saghir NS, et al. Ratio between positive lymph nodes and total excised axillary lymph nodes as an independent prognostic factor for overall survival in patients with non-metastatic lymph node-positive breast cancer. Ann Surg Oncol 2009;16:3388-95.
35. Paish EC, Green AR, Rakha EA, et al. Three-dimensional reconstruction of sentinel lymph nodes with metastatic breast cancer indicates three distinct patterns of tumour growth. J Clin Pathol 2009;62:617-23.
36. Blamey RW, Ellis IO, Pinder SE, et al. Survival of invasive breast cancer according to the Nottingham Prognostic Index in cases diagnosed in 1990e1999. Eur J Cancer 2007;43:1548-55. (Pubitemid 46901016)
37. Rakha EA, El-Sayed ME, Lee AH, et al. Prognostic significance of Nottingham histologic grade in invasive breast carcinoma. J Clin Oncol 2008;26:3153-8.
38. Ellis IO, Galea M, Broughton N, et al. Pathological prognostic factors in breast cancer. II. Histological type. Relationship with survival in a large study with long-term follow-up. Histopathology 1992;20:479-89.
39. Elston CW, Ellis IO. Pathological prognostic factors in breast cancer I. The value of histological grade in breast cancer: experience from a large study with long-term follow-up. Histopathology 1991;19:403-10.
40. Pinder SE, Ellis IO, Galea M, et al. Pathological prognostic factors in breast cancer. III. Vascular invasion: relationship with recurrence and survival in a large study with long-term follow-up. Histopathology 1994;24:41-7. (Pubitemid 24223138)
41. Rakha EA, El-Sayed ME, Menon S, et al. Histologic grading is an independent prognostic factor in invasive lobular carcinoma of the breast. Breast Cancer Res Treat 2008;111:121-7. (Pubitemid 352009237)
42. Kurien T, Boyce RW, Paish EC, et al. Three dimensional reconstruction of a human breast carcinoma using routine laboratory equipment and immunohistochemistry. J Clin Pathol 2005;58:968-72. (Pubitemid 41265283)
43. Giuliano AE, Dale PS, Turner RR, et al. Improved axillary staging of breast cancer with sentinel lymphadenectomy. Ann Surg 1995;222:394-9.
44. Albertini JJ, Lyman GH, Cox C, et al. Lymphatic mapping and sentinel node biopsy in the patient with breast cancer. JAMA 1996;276:1818-22. (Pubitemid 26406231)
45. Dixon JM, Anderson TJ, Page DL, et al. Infiltrating lobular carcinoma of the breast. Histopathology 1982;6:149-61. (Pubitemid 12150073)
46. Yoder BJ, Wilkinson EJ, Massoll NA. Molecular and morphologic distinctions between infiltrating ductal and lobular carcinoma of the breast. Breast J 2007;13:172-9. (Pubitemid 46280603)
47. Johnson S, Brown S, Porter G, et al. Staging primary breast cancer. Are there tumour pathological features that correlate with a false-negative axillary ultrasound? Clin Radiol. 2011;66:497-9.
48. Schrenk P, Konstantiniuk P, Wolfl S, et al. Intraoperative frozen section examination of the sentinel lymph node in breast cancer. Rozhl Chir 2005;84:217-22.
49. Berx G, Cleton-Jansen AM, Strumane K, et al. E-cadherin is inactivated in a majority of invasive human lobular breast cancers by truncation mutations throughout its extracellular domain. Oncogene 1996;13:1919-25. (Pubitemid 26397451)
50. Rakha EA, Patel A, Powe DG, et al. Clinical and biological significance of E-cadherin protein expression in invasive lobular carcinoma of the breast. Am J Surg Pathol 2010;34:1472-9.
51. Lehr HA, Folpe A, Yaziji H, et al. Cytokeratin 8 immunostaining pattern and E-cadherin expression distinguish lobular from ductal breast carcinoma. Am J Clin Pathol 2000;114:190-6. (Pubitemid 33051866)
52. Rakha EA, Abd El Rehim D, Pinder SE, et al. E-cadherin expression in invasive nonlobular carcinoma of the breast and its prognostic significance. Histopathology 2005;46:685-93. (Pubitemid 40834828)
53. Cleton-Jansen AM. E-cadherin and loss of heterozygosity at chromosome 16 in breast carcinogenesis: different genetic pathways in ductal and lobular breast cancer? Breast Cancer Res 2002;4:5-8.
54. Korkola JE, DeVries S, Fridlyand J, et al. Differentiation of lobular versus ductal breast carcinomas by expression microarray analysis. Cancer Res 2003;63:7167-75. (Pubitemid 37413454)
55. Zhao H, Langerod A, Ji Y, et al. Different gene expression patterns in invasive lobular and ductal carcinomas of the breast. Mol Biol Cell 2004;15:2523-36. (Pubitemid 38691844)
56. Borst MJ, Ingold JA. Metastatic patterns of invasive lobular versus invasive ductal carcinoma of the breast. Surgery 1993;114:637-41; discussion 641-2.
57. Winston CB, Hadar O, Teitcher JB, et al. Metastatic lobular carcinoma of the breast: patterns of spread in the chest, abdomen, and pelvis on CT. Am J Roentgenol 2000;175:795-800.
58. Winchester DJ, Chang HR, Graves TA, et al. A comparative analysis of lobular and ductal carcinoma of the breast: presentation, treatment and outcomes. J Am Coll Surg 1998;186:416-22. (Pubitemid 28169363)
59. Cristofanilli M, Gonzalez-Angulo A, Sneige N, et al. Invasive lobular carcinoma classic type: response to primary chemotherapy and survival outcomes. J Clin Oncol 2005;23:41-8. (Pubitemid 41702621)
60. Cserni G, Bianchi S, Vezzosi V, et al. The value of cytokeratin immunohistochemistry in the evaluation of axillary sentinel lymph nodes in patients with lobular breast carcinoma. J Clin Pathol 2006;59:518-22.
61. Van den Eynden GG, Van der Auwera I, Van Laere SJ, et al. Distinguishing blood and lymph vessel invasion in breast cancer: a prospective immunohistochemical study. Br J Cancer 2006;11:1643-9. (Pubitemid 43924927)
62. Lee AH. Inflammation and vascularity in carcinoma of the breast. MD thesis. Cambridge: University of Cambridge, 2008.