Seminars in Diagnostic Pathology
Volume 27, Issue 1 , Pages 49-61 , February 2010

Lobular breast carcinoma and its variants

  • Emad A. Rakha, PhD, FRCPath

      Affiliations

    • Corresponding Author InformationAddress reprint requests and correspondence: Emad A. Rakha, PhD, FRCPath, Department of Histopathology, Nottingham University Hospitals NHS Trust, Nottingham City Hospital, Hucknall Road, Nottingham, NG5 1PB, United Kingdom
    • ,
  • Ian O. Ellis, MD, FRCPath

References 

  1. Foote FW, Stewart FW. Lobular carcinoma in situ (A rare form of mammary cancer). Am J Pathol. 1941;17:491–496
  2. Wheeler JE, Enterline HT. Lobular carcinoma of the breast in situ and infiltrating. Pathol Annu. 1976;11:161–188
  3. Dunnwald LK, Rossing MA, Li CI. Hormone receptor status, tumor characteristics, and prognosis: A prospective cohort of breast cancer patients. Breast Cancer Res. 2007;9:R6
  4. Li CI, Uribe DJ, Daling JR. Clinical characteristics of different histologic types of breast cancer. Br J Cancer. 2005;93:1046–1052
  5. 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
  6. 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–R156
  7. Henson D, Tarone R. A study of lobular carcinoma of the breast based on the third national cancer survey in the United States of America. Tumori. 1979;65:133–142
  8. Li CI, Anderson BO, Daling JR, et al. Trends in incidence rates of invasive lobular and ductal breast carcinoma. JAMA. 2003;289:1421–1424
  9. Li CI, Anderson BO, Porter P, et al. Changing incidence rate of invasive lobular breast carcinoma among older women. Cancer. 2000;88:2561–2569
  10. Bonnier P, Romain S, Giacalone PL, et al. Clinical and biologic prognostic factors in breast cancer diagnosed during postmenopausal hormone replacement therapy. Obstet Gynecol. 1995;85:11–17
  11. Li CI, Daling JR, Malone KE, et al. Relationship between established breast cancer risk factors and risk of seven different histologic types of invasive breast cancer. Cancer Epidemiol Biomarkers Prev. 2006;15:946–954
  12. Rakha EA, Gill MS, El-Sayed ME, et al. The biological and clinical characteristics of breast carcinoma with mixed ductal and lobular morphology. Breast Cancer Res Treat. 2008;114:243–250
  13. Martinez V, Azzopardi JG. Invasive lobular carcinoma of the breast: Incidence and variants. Histopathology. 1979;3:467–488
  14. 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
  15. Stange DE, Radlwimmer B, Schubert F, et al. High-resolution genomic profiling reveals association of chromosomal aberrations on 1q and 16p with histologic and genetic subgroups of invasive breast cancer. Clin Cancer Res. 2006;12:345–352
  16. Weigelt B, Geyer FC, Natrajan R, et al. The molecular underpinning of lobular histological growth pattern: A genome-wide transcriptomic analysis of invasive lobular carcinomas and grade- and molecular subtype-matched invasive ductal carcinomas of no special type. J Pathol. 2010;220:45–57
  17. Shelley Hwang E, Nyante SJ, Yi Chen Y, et al. Clonality of lobular carcinoma in situ and synchronous invasive lobular carcinoma. Cancer. 2004;100:2562–2572
  18. Loo LW, Grove DI, Williams EM, et al. Array comparative genomic hybridization analysis of genomic alterations in breast cancer subtypes. Cancer Res. 2004;64:8541–8549
  19. Domagala W, Markiewski M, Kubiak R, et al. Immunohistochemical profile of invasive lobular carcinoma of the breast: Predominantly vimentin and p53 protein negative, cathepsin D and oestrogen receptor positive. Virchows Arch A Pathol Anat Histopathol. 1993;423:497–502
  20. 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;77:113–120
  21. 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;111:121–127
  22. Wheeler DT, Tai LH, Bratthauer GL, et al. Tubulolobular carcinoma of the breast: An analysis of 27 cases of a tumor with a hybrid morphology and immunoprofile. Am J Surg Pathol. 2004;28:1587–1593
  23. Hanby AM, Hughes TA. In situ and invasive lobular neoplasia of the breast. Histopathology. 2008;52:58–66
  24. El-Sayed ME, Rakha EA, Reed J, et al. Predictive value of needle core biopsy diagnoses of lesions of uncertain malignant potential (B3) in abnormalities detected by mammographic screening. Histopathology. 2008;53:650–657
  25. Beute BJ, Kalisher L, Hutter RV. Lobular carcinoma in situ of the breast: Clinical, pathologic, and mammographic features. AJR Am J Roentgenol. 1991;157:257–265
  26. Menon S, Porter GJ, Evans AJ, et al. The significance of lobular neoplasia on needle core biopsy of the breast. Virchows Arch. 2008;452:473–479
  27. Georgian-Smith D, Lawton TJ. Calcifications of lobular carcinoma in situ of the breast: Radiologic-pathologic correlation. AJR Am J Roentgenol. 2001;176:1255–1259
  28. Abdel-Fatah TM, Powe DG, Hodi Z, et al. Morphologic and molecular evolutionary pathways of low nuclear grade invasive breast cancers and their putative precursor lesions: Further evidence to support the concept of low nuclear grade breast neoplasia family. Am J Surg Pathol. 2008;32:513–523
  29. Abdel-Fatah TM, Powe DG, Hodi Z, et al. High frequency of coexistence of columnar cell lesions, lobular neoplasia, and low grade ductal carcinoma in situ with invasive tubular carcinoma and invasive lobular carcinoma. Am J Surg Pathol. 2007;31:417–426
  30. Leibl S, Regitnig P, Moinfar F. Flat epithelial atypia (DIN 1a, atypical columnar change): An underdiagnosed entity very frequently coexisting with lobular neoplasia. Histopathology. 2007;50:859–865
  31. Lakhani SR. In-situ lobular neoplasia: Time for an awakening. Lancet. 2003;361:96
  32. Renshaw AA, Cartagena N, Derhagopian RP, et al. Lobular neoplasia in breast core needle biopsy specimens is not associated with an increased risk of ductal carcinoma in situ or invasive carcinoma. Am J Clin Pathol. 2002;117:797–799
  33. Simpson PT, Gale T, Fulford LG, et al. The diagnosis and management of pre-invasive breast disease: Pathology of atypical lobular hyperplasia and lobular carcinoma in situ. Breast Cancer Res. 2003;5:258–262
  34. Marshall LM, Hunter DJ, Connolly JL, et al. Risk of breast cancer associated with atypical hyperplasia of lobular and ductal types. Cancer Epidemiol Biomarkers Prev. 1997;6:297–301
  35. Page DL, Schuyler PA, Dupont WD, et al. Atypical lobular hyperplasia as a unilateral predictor of breast cancer risk: A retrospective cohort study. Lancet. 2003;361:125–129
  36. Haagensen CD, Lane N, Lattes R, et al. Lobular neoplasia (so-called lobular carcinoma in situ) of the breast. Cancer. 1978;42:737–769
  37. Warnberg F, Yuen J, Holmberg L. Risk of subsequent invasive breast cancer after breast carcinoma in situ. Lancet. 2000;355:724–725
  38. Li CI, Malone KE, Saltzman BS, et al. Risk of invasive breast carcinoma among women diagnosed with ductal carcinoma in situ and lobular carcinoma in situ, 1988-2001. Cancer. 2006;106:2104–2112
  39. Fisher ER, Land SR, Fisher B, et al. Pathologic findings from the National Surgical Adjuvant Breast and Bowel Project: Twelve-year observations concerning lobular carcinoma in situ. Cancer. 2004;100:238–244
  40. Hwang H, Barke LD, Mendelson EB, et al. Atypical lobular hyperplasia and classic lobular carcinoma in situ in core biopsy specimens: Routine excision is not necessary. Mod Pathol. 2008;21:1208–1216
  41. Rudloff U, Brogi E, Brockway JP, et al. Concurrent lobular neoplasia increases the risk of ipsilateral breast cancer recurrence in patients with ductal carcinoma in situ treated with breast-conserving therapy. Cancer. 2009;115:1203–1214
  42. Middleton LP, Grant S, Stephens T, et al. Lobular carcinoma in situ diagnosed by core needle biopsy: When should it be excised?. Mod Pathol. 2003;16:120–129
  43. Lakhani SR, Audretsch W, Cleton-Jensen AM, et al. The management of lobular carcinoma in situ (LCIS) (Is LCIS the same as ductal carcinoma in situ (DCIS)?). Eur J Cancer. 2006;42:2205–2211
  44. Hwang ES, Nyante SJ, Yi Chen Y, et al. Clonality of lobular carcinoma in situ and synchronous invasive lobular carcinoma. Cancer. 2004;100:2562–2572
  45. 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;114:190–196
  46. Jacobs TW, Pliss N, Kouria G, et al. Carcinomas in situ of the breast with indeterminate features: Role of E-cadherin staining in categorization. Am J Surg Pathol. 2001;25:229–236
  47. Simpson PT, Reis-Filho JS, Lambros MB, et al. Molecular profiling pleomorphic lobular carcinomas of the breast: Evidence for a common molecular genetic pathway with classic lobular carcinomas. J Pathol. 2008;215:231–244
  48. In:  Perry NM,  Broeders M,  de Wolf CJM, et al. editor. European Guidelines for Quality Assurance in Mammography Screening. 4th ed.. Luxembourg: Office for Official Publications of the European Communities; 2006;
  49. NHSBSP Breast Screening Programme. Guidelines for Non-Operative Diagnostic Procedures and Reporting in Breast Cancer Screening. Sheffield, United Kingdom: NHSBSP Breast Screening Programme; 2001;NHSBSP Pub. No 50
  50. Fadare O, Dadmanesh F, Alvarado-Cabrero I, et al. Lobular intraepithelial neoplasia [lobular carcinoma in situ] with comedo-type necrosis: A clinicopathologic study of 18 cases. Am J Surg Pathol. 2006;30:1445–1453
  51. Ciocca RM, Li T, Freedman GM, et al. Presence of lobular carcinoma in situ does not increase local recurrence in patients treated with breast-conserving therapy. Ann Surg Oncol. 2008;15:2263–2271
  52. Pathology reporting of breast disease (A Joint Document Incorporating the Third Edition of the NHS Breast Screening Programme's Guidelines for Pathology Reporting in Breast Cancer Screening and the Second Edition of The Royal College of Pathologists' Minimum Dataset for Breast Cancer Histopathology). Sheffield, United Kingdom: NHS Cancer Screening Programmes and The Royal College of Pathologists; 2005;
  53. Howat AJ, Armour A, Ellis IO. Microinvasive lobular carcinoma of the breast. Histopathology. 2000;37:477–478
  54. Toikkanen S, Pylkkanen L, Joensuu H. Invasive lobular carcinoma of the breast has better short- and long-term survival than invasive ductal carcinoma. Br J Cancer. 1997;76:1234–1240
  55. Evans WP, Warren Burhenne LJ, Laurie L, et al. Invasive lobular carcinoma of the breast: Mammographic characteristics and computer-aided detection. Radiology. 2002;225:182–189
  56. Cornford EJ, Wilson AR, Athanassiou E, et al. Mammographic features of invasive lobular and invasive ductal carcinoma of the breast: A comparative analysis. Br J Radiol. 1995;68:450–453
  57. Silverstein MJ, Lewinsky BS, Waisman JR, et al. Infiltrating lobular carcinoma (Is it different from infiltrating duct carcinoma?). Cancer. 1994;73:1673–1677
  58. Broet P, de la Rochefordiere A, Scholl SM, et al. Contralateral breast cancer: Annual incidence and risk parameters. J Clin Oncol. 1995;13:1578–1583
  59. Berg WA, Gutierrez L, NessAiver MS, et al. Diagnostic accuracy of mammography, clinical examination, US, and MR imaging in preoperative assessment of breast cancer. Radiology. 2004;233:830–849
  60. Uchiyama N, Miyakawa K, Moriyama N, et al. Radiographic features of invasive lobular carcinoma of the breast. Radiat Med. 2001;19:19–25
  61. Kepple J, Layeeque R, Klimberg VS, et al. Correlation of magnetic resonance imaging and pathologic size of infiltrating lobular carcinoma of the breast. Am J Surg. 2005;190:623–627
  62. Moore MM, Borossa G, Imbrie JZ, et al. Association of infiltrating lobular carcinoma with positive surgical margins after breast-conservation therapy. Ann Surg. 2000;231:877–882
  63. Mann RM, Loo CE, Wobbes T, et al: The impact of preoperative breast MRI on the re-excision rate in invasive lobular carcinoma of the breast. Breast Cancer Res Treat (in press)
  64. Hwang S, Ioffe O, Lee I, et al. Cytologic diagnosis of invasive lobular carcinoma: Factors associated with negative and equivocal diagnoses. Diagn Cytopathol. 2004;31:87–93
  65. Tan SM, Behranwala KA, Trott PA, et al. A retrospective study comparing the individual modalities of triple assessment in the pre-operative diagnosis of invasive lobular breast carcinoma. Eur J Surg Oncol. 2002;28:203–208
  66. Cariaggi MP, Bulgaresi P, Confortini M, et al. Analysis of the causes of false negative cytology reports on breast cancer fine needle aspirates. Cytopathology. 1995;6:156–161
  67. Wellings SR, Jensen HM, Marcum RG. An atlas of subgross pathology of the human breast with special reference to possible precancerous lesions. J Natl Cancer Inst. 1975;55:231–273
  68. Yoder BJ, Wilkinson EJ, Massoll NA. Molecular and morphologic distinctions between infiltrating ductal and lobular carcinoma of the breast. Breast J. 2007;13:172–179
  69. Dixon JM, Anderson TJ, Page DL, et al. Infiltrating lobular carcinoma of the breast. Histopathology. 1982;6:149–161
  70. Korkola JE, DeVries S, Fridlyand J, et al. Differentiation of lobular versus ductal breast carcinomas by expression microarray analysis. Cancer Res. 2003;63:7167–7175
  71. 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;23:41–48
  72. du Toit RS, Locker AP, Ellis IO, et al. An evaluation of differences in prognosis, recurrence patterns and receptor status between invasive lobular and other invasive carcinomas of the breast. Eur J Surg Oncol. 1991;17:251–257
  73. du Toit RS, Locker AP, Ellis IO, et al. Invasive lobular carcinomas of the breast—The prognosis of histopathological subtypes. Br J Cancer. 1989;60:605–609
  74. WHO Classification of Tumours: Pathology and Genetics. Lyon, France: IARC press; 2003;
  75. Newman W. Lobular carcinoma of the female breast (Report of 73 cases). Ann Surg. 1966;164:305–314
  76. DiCostanzo D, Rosen PP, Gareen I, et al. Prognosis in infiltrating lobular carcinoma (An analysis of “classical” and variant tumors). Am J Surg Pathol. 1990;14:12–23
  77. Eusebi V, Magalhaes F, Azzopardi JG. Pleomorphic lobular carcinoma of the breast: An aggressive tumor showing apocrine differentiation. Hum Pathol. 1992;23:655–662
  78. Middleton LP, Palacios DM, Bryant BR, et al. Pleomorphic lobular carcinoma: Morphology, immunohistochemistry, and molecular analysis. Am J Surg Pathol. 2000;24:1650–1656
  79. Fisher ER, Gregorio RM, Redmond C, et al. Tubulolobular invasive breast cancer: A variant of lobular invasive cancer. Hum Pathol. 1977;8:679–683
  80. Orvieto E, Maiorano E, Bottiglieri L, et al. Clinicopathologic characteristics of invasive lobular carcinoma of the breast: Results of an analysis of 530 cases from a single institution. Cancer. 2008;113:1511–1520
  81. Roberts MM, Alexander FE, Anderson TJ, et al. Edinburgh trial of screening for breast cancer: Mortality at seven years. Lancet. 1990;335:241–246
  82. Ladekarl M, Sorensen FB. Prognostic, quantitative histopathologic variables in lobular carcinoma of the breast. Cancer. 1993;72:2602–2611
  83. Sinha PS, Bendall S, Bates T. Does routine grading of invasive lobular cancer of the breast have the same prognostic significance as for ductal cancers?. Eur J Surg Oncol. 2000;26:733–737
  84. Talman ML, Jensen MB, Rank F. Invasive lobular breast cancer (Prognostic significance of histological malignancy grading). Acta Oncol. 2007;46:803–809
  85. Pereira H, Pinder SE, Sibbering DM, et al. Pathological prognostic factors in breast cancer (IV: Should you be a typer or a grader? A comparative study of two histological prognostic features in operable breast carcinoma). Histopathology. 1995;27:219–226
  86. Sinn HP, Kellerhoff NM, Kellerhoff R, et al. Subtyping and prognostic assessment of invasive lobular breast carcinoma. Pathologe. 1997;18:37–44
  87. Moreno-Elola A, Aguilar A, Roman JM, et al. Prognostic factors in invasive lobular carcinoma of the breast: A multivariate analysis (A multicentre study after seventeen years of follow-up). Ann Chir Gynaecol. 1999;88:252–258
  88. Bane AL, Tjan S, Parkes RK, et al. Invasive lobular carcinoma: To grade or not to grade. Mod Pathol. 2005;18:621–628
  89. Mokbel K. Grading of infiltrating lobular carcinoma. Eur J Surg Oncol. 2001;27:609–610
  90. Paumier A, Sagan C, Campion L, et al. Accuracy of conservative treatment for infiltrating lobular breast cancer: A retrospective study of 217 infiltrating lobular carcinomas and 2155 infiltrating ductal carcinomas. J Gynecol Obstet Biol Reprod (Paris). 2003;32:529–534
  91. Zafrani B, Aubriot MH, Mouret E, et al. High sensitivity and specificity of immunohistochemistry for the detection of hormone receptors in breast carcinoma: Comparison with biochemical determination in a prospective study of 793 cases. Histopathology. 2000;37:536–545
  92. Nadji M, Gomez-Fernandez C, Ganjei-Azar P, et al. Immunohistochemistry of estrogen and progesterone receptors reconsidered: Experience with 5,993 breast cancers. Am J Clin Pathol. 2005;123:21–27
  93. Radhi JM. Immunohistochemical analysis of pleomorphic lobular carcinoma: Higher expression of p53 and chromogranin and lower expression of ER and PgR. Histopathology. 2000;36:156–160
  94. Rozan S, Vincent-Salomon A, Zafrani B, et al. No significant predictive value of c-erbB-2 or p53 expression regarding sensitivity to primary chemotherapy or radiotherapy in breast cancer. Int J Cancer. 1998;79:27–33
  95. Soomro S, Shousha S, Taylor P, et al. c-erbB-2 expression in different histological types of invasive breast carcinoma. J Clin Pathol. 1991;44:211–214
  96. Mazoujian G, Bodian C, Haagensen DE, et al. Expression of GCDFP-15 in breast carcinomas (Relationship to pathologic and clinical factors). Cancer. 1989;63:2156–2161
  97. Oyama T, Kashiwabara K, Yoshimoto K, et al. Frequent overexpression of the cyclin D1 oncogene in invasive lobular carcinoma of the breast. Cancer Res. 1998;58:2876–2880
  98. Mathieu MC, Rouzier R, Llombart-Cussac A, et al. The poor responsiveness of infiltrating lobular breast carcinomas to neoadjuvant chemotherapy can be explained by their biological profile. Eur J Cancer. 2004;40:342–351
  99. Bratthauer GL, Moinfar F, Stamatakos MD, et al. Combined E-cadherin and high molecular weight cytokeratin immunoprofile differentiates lobular, ductal, and hybrid mammary intraepithelial neoplasias. Hum Pathol. 2002;33:620–627
  100. Roylance R, Gorman P, Papior T, et al. A comprehensive study of chromosome 16q in invasive ductal and lobular breast carcinoma using array CGH. Oncogene. 2006;25:6544–6553
  101. Rakha EA, Green AR, Powe DG, et al. Chromosome 16 tumor-suppressor genes in breast cancer. Genes Chromosomes Cancer. 2006;45:527–535
  102. Moll R, Mitze M, Frixen UH, et al. Differential loss of E-cadherin expression in infiltrating ductal and lobular breast carcinomas. Am J Pathol. 1993;143:1731–1742
  103. Gamallo C, Palacios J, Suarez A, et al. Correlation of E-cadherin expression with differentiation grade and histological type in breast carcinoma. Am J Pathol. 1993;142:987–993
  104. 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;13:1919–1925
  105. De Leeuw WJ, Berx G, Vos CB, et al. Simultaneous loss of E-cadherin and catenins in invasive lobular breast cancer and lobular carcinoma in situ. J Pathol. 1997;183:404–411
  106. Sarrio D, Perez-Mies B, Hardisson D, et al. Cytoplasmic localization of p120ctn and E-cadherin loss characterize lobular breast carcinoma from preinvasive to metastatic lesions. Oncogene. 2004;23:3272–3283
  107. Strathdee G. Epigenetic versus genetic alterations in the inactivation of E-cadherin. Semin Cancer Biol. 2002;12:373–379
  108. Lei H, Sjoberg-Margolin S, Salahshor S, et al. CDH1 mutations are present in both ductal and lobular breast cancer, but promoter allelic variants show no detectable breast cancer risk. Int J Cancer. 2002;98:199–204
  109. Berx G, Cleton-Jansen AM, Nollet F, et al. E-cadherin is a tumour/invasion suppressor gene mutated in human lobular breast cancers. EMBO J. 1995;14:6107–6115
  110. Acs G, Lawton TJ, Rebbeck TR, et al. Differential expression of E-cadherin in lobular and ductal neoplasms of the breast and its biologic and diagnostic implications. Am J Clin Pathol. 2001;115:85–98
  111. Goldstein NS, Bassi D, Watts JC, et al. E-cadherin reactivity of 95 noninvasive ductal and lobular lesions of the breast (Implications for the interpretation of problematic lesions). Am J Clin Pathol. 2001;115:534–542
  112. Goldstein NS, Kestin LL, Vicini FA. Clinicopathologic implications of E-cadherin reactivity in patients with lobular carcinoma in situ of the breast. Cancer. 2001;92:738–747
  113. Droufakou S, Deshmane V, Roylance R, et al. Multiple ways of silencing E-cadherin gene expression in lobular carcinoma of the breast. Int J Cancer. 2001;92:404–408
  114. Yoshiura K, Kanai Y, Ochiai A, et al. Silencing of the E-cadherin invasion-suppressor gene by CpG methylation in human carcinomas. Proc Natl Acad Sci U S A. 1995;92:7416–7419
  115. Batlle E, Sancho E, Franci C, et al. The transcription factor snail is a repressor of E-cadherin gene expression in epithelial tumour cells. Nat Cell Biol. 2000;2:84–89
  116. Vos CB, Cleton-Jansen AM, Berx G, et al. E-cadherin inactivation in lobular carcinoma in situ of the breast: An early event in tumorigenesis. Br J Cancer. 1997;76:1131–1133
  117. Mastracci TL, Tjan S, Bane AL, et al. E-cadherin alterations in atypical lobular hyperplasia and lobular carcinoma in situ of the breast. Mod Pathol. 2005;18:741–751
  118. Reis-Filho JS, Cancela Paredes J, Milanezi F, et al. Clinicopathologic implications of E-cadherin reactivity in patients with lobular carcinoma in situ of the breast. Cancer. 2002;94:2114–2115discussion 2115-2116
  119. Asgeirsson KS, Jo JG, Tryggvadottir L, et al. Altered expression of E-cadherin in breast cancer (Patterns, mechanisms and clinical significance). Eur J Cancer. 2000;36:1098–1106
  120. Goldstein NS. Does the level of E-cadherin expression correlate with the primary breast carcinoma infiltration pattern and type of systemic metastases?. Am J Clin Pathol. 2002;118:425–434
  121. Da Silva L, Parry S, Reid L, et al. Aberrant expression of E-cadherin in lobular carcinomas of the breast. Am J Surg Pathol. 2008;32:773–783
  122. Flagiello D, Gerbault-Seureau M, Padoy E, et al. Near haploidy in breast cancer: A particular pathway of chromosome evolution. Cancer Genet Cytogenet. 1998;102:54–58
  123. Nishizaki T, Chew K, Chu L, et al. Genetic alterations in lobular breast cancer by comparative genomic hybridization. Int J Cancer. 1997;74:513–517
  124. Bertucci F, Orsetti B, Negre V, et al. Lobular and ductal carcinomas of the breast have distinct genomic and expression profiles. Oncogene. 2008;27:5359–5372
  125. Turashvili G, Bouchal J, Baumforth K, et al. Novel markers for differentiation of lobular and ductal invasive breast carcinomas by laser microdissection and microarray analysis. BMC Cancer. 2007;7:55
  126. Berx G, Becker KF, Hofler H, et al. Mutations of the human E-cadherin (CDH1) gene. Hum Mutat. 1998;12:226–237
  127. Keller G, Vogelsang H, Becker I, et al. Diffuse type gastric and lobular breast carcinoma in a familial gastric cancer patient with an E-cadherin germline mutation. Am J Pathol. 1999;155:337–342
  128. Chan JK, Wong CS. Loss of E-cadherin is the fundamental defect in diffuse-type gastric carcinoma and infiltrating lobular carcinoma of the breast. Adv Anat Pathol. 2001;8:165–172
  129. Jacquemier J, Eisinger F, Nogues C, et al. Histological type and syncytial growth pattern affect E-cadherin expression in a multifactorial analysis of a combined panel of sporadic and BRCA1-associated breast cancers. Int J Cancer. 1999;83:45–49
  130. Weigelt B, Horlings H, Kreike B, et al. Refinement of breast cancer classification by molecular characterization of histological special types. J Pathol. 2008;216:141–150
  131. Perou CM, Sorlie T, Eisen MB, et al. Molecular portraits of human breast tumours. Nature. 2000;406:747–752
  132. Ashikari R, Huvos AG, Urban JA, et al. Infiltrating lobular carcinoma of the breast. Cancer. 1973;31:110–116
  133. Mate TP, Carter D, Fischer DB, et al. A clinical and histopathologic analysis of the results of conservation surgery and radiation therapy in stage I and II breast carcinoma. Cancer. 1986;58:1995–2002
  134. Santiago RJ, Harris EE, Qin L, et al. Similar long-term results of breast-conservation treatment for stage I and II invasive lobular carcinoma compared with invasive ductal carcinoma of the breast: The University of Pennsylvania experience. Cancer. 2005;103:2447–2454
  135. Vo TN, Meric-Bernstam F, Yi M, et al. Outcomes of breast-conservation therapy for invasive lobular carcinoma are equivalent to those for invasive ductal carcinoma. Am J Surg. 2006;192:552–555
  136. Molland JG, Donnellan M, Janu NC, et al. Infiltrating lobular carcinoma—A comparison of diagnosis, management and outcome with infiltrating duct carcinoma. Breast. 2004;13:389–396
  137. Korhonen T, Huhtala H, Holli K. A comparison of the biological and clinical features of invasive lobular and ductal carcinomas of the breast. Breast Cancer Res Treat. 2004;85:23–29
  138. 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;68:43–47discussion 48
  139. Peiro G, Bornstein BA, Connolly JL, et al. The influence of infiltrating lobular carcinoma on the outcome of patients treated with breast-conserving surgery and radiation therapy. Breast Cancer Res Treat. 2000;59:49–54
  140. Schrenk P, Konstantiniuk P, Wölfl S, et al. Intraoperative frozen section examination of the sentinel lymph node in breast cancer. Rozhl Chir. 2005;84:217–222
  141. Hess KR, Pusztai L, Buzdar AU, et al. Estrogen receptors and distinct patterns of breast cancer relapse. Breast Cancer Res Treat. 2003;78:105–118
  142. Bouvet M, Ollila DW, Hunt KK, et al. Role of conservation therapy for invasive lobular carcinoma of the breast. Ann Surg Oncol. 1997;4:650–654
  143. Cocquyt V, Van Belle S. Lobular carcinoma in situ and invasive lobular cancer of the breast. Curr Opin Obstet Gynecol. 2005;17:55–60
  144. Tovey SM, Brown S, Doughty JC, et al. Poor survival outcomes in HER2-positive breast cancer patients with low-grade, node-negative tumours. Br J Cancer. 2009;100:680–683
  145. Shousha S, Backhous CM, Alaghband-Zadeh J, et al. Alveolar variant of invasive lobular carcinoma of the breast (A tumor rich in estrogen receptors). Am J Clin Pathol. 1986;85:1–5
  146. Buchanan CL, Flynn LW, Murray MP, et al. Is pleomorphic lobular carcinoma really a distinct clinical entity?. J Surg Oncol. 2008;98:314–317
  147. Ferlicot S, Vincent-Salomon A, Medioni J, et al. Wide metastatic spreading in infiltrating lobular carcinoma of the breast. Eur J Cancer. 2004;40:336–341
  148. 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. AJR Am J Roentgenol. 2000;175:795–800
  149. Borst MJ, Ingold JA. Metastatic patterns of invasive lobular versus invasive ductal carcinoma of the breast. Surgery. 1993;114:637–641discussion 641-632
  150. Lamovec J, Bracko M. Metastatic pattern of infiltrating lobular carcinoma of the breast: An autopsy study. J Surg Oncol. 1991;48:28–33
  151. Jimeno A, Amador ML, Gonzalez-Cortijo L, et al. Initially metastatic breast carcinoma has a distinct disease pattern but an equivalent outcome compared with recurrent metastatic breast carcinoma. Cancer. 2004;100:1833–1842
  152. Tubiana-Hulin M, Stevens D, Lasry S, et al. Response to neoadjuvant chemotherapy in lobular and ductal breast carcinomas: A retrospective study on 860 patients from one institution. Ann Oncol. 2006;17:1228–1233
  153. Wenzel C, Bartsch R, Hussian D, et al. Invasive ductal carcinoma and invasive lobular carcinoma of breast differ in response following neoadjuvant therapy with epidoxorubicin and docetaxel + G-CSF. Breast Cancer Res Treat. 2007;104:109–114
  154. Katz A, Saad ED, Porter P, et al. Primary systemic chemotherapy of invasive lobular carcinoma of the breast. Lancet Oncol. 2007;8:55–62
  155. Cocquyt VF, Blondeel PN, Depypere HT, et al. Different responses to preoperative chemotherapy for invasive lobular and invasive ductal breast carcinoma. Eur J Surg Oncol. 2003;29:361–367
  156. Horobin JM, Preece PE, Dewar JA, et al. Long-term follow-up of elderly patients with locoregional breast cancer treated with tamoxifen only. Br J Surg. 1991;78:213–217
  157. Dixon JM, Jackson J, Renshaw L, et al. Neoadjuvant tamoxifen and aromatase inhibitors: Comparisons and clinical outcomes. J Steroid Biochem Mol Biol. 2003;86:295–299
  158. Dixon JM, Anderson TJ, Page DL, et al. Infiltrating lobular carcinoma of the breast: An evaluation of the incidence and consequence of bilateral disease. Br J Surg. 1983;70:513–516
  159. Davis RP, Nora PF, Kooy RG, et al. Experience with lobular carcinoma of the breast (Emphasis on recent aspects of management). Arch Surg. 1979;114:485–488

PII: S0740-2570(09)00099-9

doi: 10.1053/j.semdp.2009.12.009

Seminars in Diagnostic Pathology
Volume 27, Issue 1 , Pages 49-61 , February 2010

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