Pathology of Inflammatory Breast Cancer

  • Victor Manuel Perez-Sanchez
  • Hector Aquiles Maldonado-Martinez
  • Paula Juarez-Sanchez
  • Abelardo Meneses-Garcia


Inflammatory breast cancer (IBC) is a rare and aggressive subtype of locally advanced breast cancer (LABC). Its diagnosis is primarily clinical; however, a pathological confirmation of invasive cancer is required.

The purpose of this chapter is to review the pathological characteristics of IBC; its pattern of expression of conventional biomarkers of breast carcinoma; other biological factors currently described to be involved in its highly malignant phenotype; and the emerging data, from novel approaches as expression profiling, on its classification and biological features.


Vascular Endothelial Growth Factor Cancer Stem Cell Epithelial Growth Factor Receptor Tumor Embolus Locally Advanced Breast Cancer 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.


  1. 1.
    Bell JC. A system of operative surgery, founded on the basis of anatomy. London: Longman, Hurst, Rees, & Orne; 1807.Google Scholar
  2. 2.
    Lee BJ, Tannenbaum NE. Inflammatory carcinoma of the breast. Surg Gynecol Obstet. 1924;39:580.Google Scholar
  3. 3.
    Haagensen CD. Inflammatory carcinoma. In: Haegensen CD, editor. Diseases of the breast. 2nd ed. Philadelphia: Saunders; 1971. p. 576–84.Google Scholar
  4. 4.
    Green FL, Page DL, Fleming ID, et al., editors. AAJCC cancer staging manual. 6th ed. New York: Springer; 2002. p. 225–81.Google Scholar
  5. 5.
    Low J, Berman A, Steinber S, et al. Long term follow up for locally advanced and inflammatory breast cancer patients treated with multimodality therapy. J Clin Oncol. 2004;22:4065–74.CrossRefGoogle Scholar
  6. 6.
    Ueno NT, Buzdar AU, Singletary SE, et al. Combined modality treatment of inflammatory breast carcinoma: twenty years of experience at MD Anderson Center. Cancer Chemother Pharmacol. 1997;40:321–9.PubMedCrossRefGoogle Scholar
  7. 7.
    Dawood S, Cristofanilli M. Inflammatory breast cancer: what progress have we made? Oncology. 2011;25:3.Google Scholar
  8. 8.
    Rosen PP. Inflammatory carcinoma. In: Rosen PP, editor. Rosen’s breast pathology. 2nd ed. Philadelphia: Lippincott Williams & Wilkins; 2001. p. 676–83.Google Scholar
  9. 9.
    Resetkova E. Pathologic aspects of inflammatory breast carcinoma: part 1. Histomorphology and differential diagnosis. Semin Oncol. 2008;35:25–32.PubMedCrossRefGoogle Scholar
  10. 10.
    Bonnier P, Charpin C, Lejeune C, et al. Inflammatory carcinomas of the breast: a clinical, pathological, or a clinical and pathological definition? Int J Cancer. 1995;62:382–5.PubMedCrossRefGoogle Scholar
  11. 11.
    Charpin C, Bonnier P, Khouzami A, et al. Inflammatory breast carcinoma: an immunohistochemical study using monoclonal anti-pHer-2/neu, pS2, cathepsin, ER and PR. Anticancer Res. 1992;12:591–7.PubMedGoogle Scholar
  12. 12.
    Robertson F, Bondy M, Yang E, et al. Inflammatory breast cancer. The disease, the biology, the treatment. CA Cancer J Clin. 2010;60:351–75.PubMedCrossRefGoogle Scholar
  13. 13.
    Taylor GW, Melzer A. Inflammatory carcinoma of the breast. Am J Cancer. 1938;33:33–49.Google Scholar
  14. 14.
    Haagensen CD. Inflammatory carcinoma. In: Haagensen CD, editor. Diseases of the breast. 2nd ed. Philadelphia: Saunders; 1971. p. 576–84.Google Scholar
  15. 15.
    Salzstein S. Clinically occult inflammatory carcinoma of the breast. Cancer. 1974;34:382–8.CrossRefGoogle Scholar
  16. 16.
    Amparo RS, Angel CD, Ana LH, et al. Inflammatory breast carcinoma: pathological and clinical entity? Breast Cancer Res Treat. 2000;64:269–73.PubMedCrossRefGoogle Scholar
  17. 17.
    Hahnel R, Woodings T, Vivian AB. Prognostic value of estrogen receptors in primary breast cancer. Cancer. 1979;44:671–5.PubMedCrossRefGoogle Scholar
  18. 18.
    Allred DC, Harvey JM, Berardo M, et al. Prognostic and predictive factors in breast cancer by ­immunohistochemical analysis. Mod Pathol. 1998;11:155–68.PubMedGoogle Scholar
  19. 19.
    Nadji M, Gómez-Fernández C, Ganjei-Azar P, et al. Immunohistochemistry of estrogen and progesterone receptors reconsidered: experience with 5,993 breast cancers. Am J Clin Pathol. 2005;123:21–7.PubMedCrossRefGoogle Scholar
  20. 20.
    Mohsin SK, Weiss H, Havighurst T, et al. Progesterone receptor by immunohistochemistry and clinical outcome in breast cancer: a validation study. Mod Pathol. 2004;17:1545–54.PubMedCrossRefGoogle Scholar
  21. 21.
    Charafe-Jauffret E, Tarpin C, Viens P, et al. Defining the molecular biology of inflammatory breast cancer. Semin Oncol. 2008;35:41–50.PubMedCrossRefGoogle Scholar
  22. 22.
    Paradiso A, Tomassi S, Brandi M, et al. Cell kinetics and hormonal receptor status in inflammatory breast carcinoma. Comparison with locally advanced disease. Cancer. 1989;64:1922–7.PubMedCrossRefGoogle Scholar
  23. 23.
    Somlo G, Frankel P, Chow W, et al. Prognostic indicators and survival in patients with stage IIIB inflammatory breast carcinoma after dose-intense chemotherapy. J Clin Oncol. 2004;22:1839–48.PubMedCrossRefGoogle Scholar
  24. 24.
    Eccles S. The epidermal growth factor receptor/Erb-B/HER family in normal and malignant breast biology. Int J Dev Biol. 2011;55:685–96. doi: 10.1387/ijdb.113396se.PubMedCrossRefGoogle Scholar
  25. 25.
    Gong Y. Pathologic aspects on inflammatory breast cancer: part 2. Biologic insights into its aggressive phenotype. Semin Oncol. 2008;35:33–40.PubMedCrossRefGoogle Scholar
  26. 26.
    Le MG, Arriagada R, Bahi J, et al. Are risk factors for breast cancer similar in women with inflammatory breast cancer and in those with non-inflammatory breast cancer? Breast. 2006;15:355–62.PubMedCrossRefGoogle Scholar
  27. 27.
    Nieto Y, Nawaz F, Jones RB, et al. Prognostic significance of overexpression and phosphorylation of epidermal growth factor receptor (EGFR) and the presence of truncated EFGRvIII in locoregionally advanced breast cancer. J Clin Oncol. 2007;21:4405–13.CrossRefGoogle Scholar
  28. 28.
    Rodríguez S, Huynh-Do U. The role of PTEN in tumor angiogenesis. J Oncol. 2012;11 p. doi: 10.1155/2012/141236. Article ID 141236.
  29. 29.
    Fan F, Schimming A, Jaeger D, et al. Targeting the tumor microenvironment: focus on angiogenesis. J Clin Oncol. 2012;16 p. doi: 10.1155/2012/281261. Article ID 281261.
  30. 30.
    Folkman J. Tumor angiogenesis therapeutic implications. N Engl J Med. 1971;285:1182–6.PubMedCrossRefGoogle Scholar
  31. 31.
    Torres IP, Filho M, Leunig F, et al. Noninvasive measurement of microvascular and interstitial oxygen profiles in a human tumor in SCID mice. Proc Natl Acad Sci USA. 1994;91:2081–5.CrossRefGoogle Scholar
  32. 32.
    Ch’ng ES, Jaafar H, Tuan Sharif SE. Breast tumor angiogenesis and tumor-associated macrophages: Histopathologist’s perspective. Pathol Res Int. 2011; 13 p. doi: 10.4061/2011/572706. Article ID 572706.
  33. 33.
    Reid PE, Brown NJ, Holen I. Breast cancer cells stimulate osteoprotegerin (OPG) production by endothelial cells through direct cell contact. Mol Cancer. 2009;8:49.PubMedCrossRefGoogle Scholar
  34. 34.
    Cross SS, Yang Z, Brown NJ, et al. Osteoprotegerin (OPG)- a potential new role in the regulation of endothelial cell phenotype and tumour angiogenesis? Int J Cancer. 2006;118(8):1901–8.PubMedCrossRefGoogle Scholar
  35. 35.
    Hayashida T, Takahashi F, Chiba N, et al. HOXB9, a gene overexpressed in breast cancer, promotes tumorigenicity and lung metastasis. Proc Natl Acad Sci USA. 2010;107(3):1100–5.PubMedCrossRefGoogle Scholar
  36. 36.
    Greer P. Closing in on the biological functions of Fps/Fes and Fer. Nat Rev Mol Cell Biol. 2002;3(4):278–89.PubMedCrossRefGoogle Scholar
  37. 37.
    Zhang S, Chitu V, Stanley ER, et al. Fes tyrosine kinase expression in the tumor niche correlates with enhanced tumor growth, angiogenesis, circulating tumor cells, metastasis, and infiltrating macrophages. Cancer Res. 2011;71(4):1465–73.PubMedCrossRefGoogle Scholar
  38. 38.
    Weidner N, Semple JP, Welch WR, et al. Tumor angiogenesis and metastasis- correlation in invasive breast carcinoma. N Engl J Med. 1991;324(1):1–8.PubMedCrossRefGoogle Scholar
  39. 39.
    Hansen S, Sørensen FB, Vach W, et al. Microvessel density compared with the Chalkley count in a prognostic study of angiogenesis in breast cancer patients. Histopathology. 2004;44:428–36.PubMedCrossRefGoogle Scholar
  40. 40.
    McCarthy NJ, Yang X, Linnoila IR, et al. Microvessel density, expression of estrogen receptor alpha, MIB-1, p53, and c-erbB-2 in inflammatory breast cancer. Clin Cancer Res. 2002;8:3857–62.PubMedGoogle Scholar
  41. 41.
    Vermeulen PB, Van Golen KL, Dirix LY. Angiogenesis, lymphangiogenesis, growth pattern, and tumor emboli in inflammatory breast cancer. Cancer. 2010;116 Suppl 11:2748–54.PubMedCrossRefGoogle Scholar
  42. 42.
    Van der Auwera I, Van Laere SJ, Van den Eynden GG, et al. Increased angiogenesis and lymphangiogenesis in inflammatory versus noninflammatory breast cancer by real-time reverse transcriptase-PCR gene expression quantification. Clin Cancer Res. 2004;10:7965–71.PubMedCrossRefGoogle Scholar
  43. 43.
    Bièche I, Lerebours F, Tozlu S, et al. Molecular profiling of inflammatory breast cancer: identification of a poor-prognosis gene expression signature. Clin Cancer Res. 2004;10:6789–95.PubMedCrossRefGoogle Scholar
  44. 44.
    Shirakawa K, Kobayashi H, Sobajima J, et al. Inflammatory breast cancer. Vasculogenic mimicry and its hemodynamics of an inflammatory breast cancer xenograft model. Breast Cancer Res. 2003;5:136–9.PubMedCrossRefGoogle Scholar
  45. 45.
    Mahooti S, Porter K, Alpaugh ML, et al. Breast carcinomatous tumoral emboli can result from encircling lymphovasculogenesis rather than lymphovascular invasion. Oncotarget. 2010;1(2):131–47.PubMedGoogle Scholar
  46. 46.
    Sugino T, Kusakabe T, Hoshi N, et al. An invasion-independent pathway of blood-borne metastasis. A new murine mammary tumor model. Am J Pathol. 2002;160:1973–80.PubMedCrossRefGoogle Scholar
  47. 47.
    Heimann R, Lan F, McBride R, et al. Separating favorable from unfavorable prognostic markers in breast cancer: the role of E-cadherin. Cancer Res. 2000;60:298–304.PubMedGoogle Scholar
  48. 48.
    Christofori G, Semb H. The role of the cell-adhesion molecule E-cadherin as a tumour-suppressor gene. Trends Biochem Sci. 1999;24:73–6.PubMedCrossRefGoogle Scholar
  49. 49.
    Alpaugh ML, Tomlinson JS, Shao ZM, et al. A novel human xenograft model of inflammatory breast cancer. Cancer Res. 1999;59:5079–84.PubMedGoogle Scholar
  50. 50.
    Tomlinson JS, Alpaugh ML, Barsky SH. An intact overexpressed E-cadherin/alpha, beta-catenin axis characterizes the lymphovascular emboli of inflammatory breast carcinoma. Cancer Res. 2001;61:5231–41.PubMedGoogle Scholar
  51. 51.
    Hoffmeyer MR, Wall KM, Dharmawardhane SF. In vitro analysis of the invasive phenotype of SUM 149, an inflammatory breast cancer cell line. Cancer Cell Int. 2005;5:11.PubMedCrossRefGoogle Scholar
  52. 52.
    Kleer CG, van Golen KL, Braun T, et al. Persistent E-cadherin expression in inflammatory breast cancer. Mod Pathol. 2001;14:458–64.PubMedCrossRefGoogle Scholar
  53. 53.
    Colpaert CG, Vermeulen PB, Benoy I, et al. Inflammatory breast cancer shows angiogenesis with high endothelial proliferation rate and strong E-cadherin expression. Br J Cancer. 2003;88:718–25.PubMedCrossRefGoogle Scholar
  54. 54.
    Liotta LA, Saidel MG, Kleinerman J. The significance of hematogenous tumor cell clumps in the metastatic process. Cancer Res. 1976;36:889–94.PubMedGoogle Scholar
  55. 55.
    Alpaugh ML, Tomlinson JS, Kasraeian S, et al. Cooperative role of E-cadherin and sialyl-Lewis X/A-deficient MUC1 in the passive dissemination of tumor emboli in inflammatory breast carcinoma. Oncogene. 2002;21:3631–43.PubMedCrossRefGoogle Scholar
  56. 56.
    Alpaugh ML, Barsky SH. Reversible model of spheroid formation allows for high efficiency of gene delivery ex vivo and accurate gene assessment in vivo. Hum Gene Ther. 2002;13:1245–58.PubMedCrossRefGoogle Scholar
  57. 57.
    Dong HM, Liu G, Hou YF, et al. Dominant-negative E-cadherin inhibits the invasiveness of inflammatory breast cancer cells in vitro. J Cancer Res Clin Oncol. 2007;133:83–92.PubMedCrossRefGoogle Scholar
  58. 58.
    Silvera D, Arju R, Darvishian F, et al. Essential role for eIF4GI overexpression in the pathogenesis of inflammatory breast cancer. Nat Cell Biol. 2009;11:903–8.PubMedCrossRefGoogle Scholar
  59. 59.
    Alpaugh ML, Tomlinson JS, Ye Y, et al. Relationship of sialyl-Lewis(x/a) underexpression and E-cadherin overexpression in the lymphovascular embolus of inflammatory breast carcinoma. Am J Pathol. 2002;161:619–28.PubMedCrossRefGoogle Scholar
  60. 60.
    van Golen KL, Wu ZF, Qiao XT, et al. RhoC GTPase, a novel transforming oncogene for human mammary epithelial cells that partially recapitulates the inflammatory breast cancer phenotype. Cancer Res. 2000;60:5832–8.PubMedGoogle Scholar
  61. 61.
    van Golen KL, Davies S, Wu ZF, et al. A novel putative low-affinity insulin-like growth factor-binding protein, LIBC (lost in inflammatory breast cancer), and RhoC-GTPase correlate with the inflammatory breast cancer phenotype. Clin Cancer Res. 1999;5:2511–9.PubMedGoogle Scholar
  62. 62.
    Kleer CG, Zhang Y, Pan Q, et al. WISP3 is a novel tumor suppressor gene of inflammatory breast cancer. Oncogene. 2002;21:3172–80.PubMedCrossRefGoogle Scholar
  63. 63.
    Kleer CG, van Golen KL, Zhang Y, et al. Characterization of RhoC expression in benign and malignant breast disease: a potential new marker for small breast carcinomas with metastatic ability. Am J Pathol. 2002;160:579–84.PubMedCrossRefGoogle Scholar
  64. 64.
    Kleer CG, Griffith KA, Sabel MS, et al. RhoC-GTPase is a novel tissue biomarker associated with biologically aggressive carcinomas of the breast. Breast Cancer Res Treat. 2005;93:101–10.PubMedCrossRefGoogle Scholar
  65. 65.
    van Golen KL, Wu ZF, Qiao XT, et al. RhoC GTPase overexpression modulates induction of angiogenic factors in breast cells. Neoplasia. 2000;2:418–25.PubMedCrossRefGoogle Scholar
  66. 66.
    Wu M, Wu ZF, Kumar-Sinha C, et al. RhoC induces differential expression of genes involved in invasion and metastasis in MCF10A breast cells. Breast Cancer Res Treat. 2004;84:3–12.PubMedCrossRefGoogle Scholar
  67. 67.
    Kleer CG, Zhang Y, Pan Q, et al. WISP3 and RhoC guanosine triphosphatase cooperate in the development of inflammatory breast cancer. Breast Cancer Res. 2004;6:R110–5.CrossRefGoogle Scholar
  68. 68.
    Nigro JM, Baker SJ, Preisinger AC, et al. Mutations in the p53 gene occur in diverse human tumour types. Nature. 1989;342:705–8.PubMedCrossRefGoogle Scholar
  69. 69.
    Davidoff AM, Humphrey PA, Iglehart JD, et al. Genetic basis for p53 overexpression in human breast cancer. Proc Natl Acad Sci USA. 1991;88:5006–10.PubMedCrossRefGoogle Scholar
  70. 70.
    Overmoyer BA. Inflammatory breast cancer: novel preoperative therapies. Clin Breast Cancer. 2010;10:27–32.PubMedCrossRefGoogle Scholar
  71. 71.
    Moll UM, Riou G, Levine AJ. Two distinct mechanisms alter p53 in breast cancer: mutation and nuclear exclusion. Proc Natl Acad Sci USA. 1992;89:7262–6.PubMedCrossRefGoogle Scholar
  72. 72.
    Riou G, Le MG, Travagli JP, et al. Poor prognosis of p53 gene mutation and nuclear overexpression of p53 protein in inflammatory breast carcinoma. J Natl Cancer Inst. 1993;85:1765–7.PubMedCrossRefGoogle Scholar
  73. 73.
    Faille A, De Cremoux P, Extra JM, et al. p53 mutations and overexpression in locally advanced breast cancers. Br J Cancer. 1994;69:1145–50.PubMedCrossRefGoogle Scholar
  74. 74.
    Van Laere S, Van der Auwera I, Van den Eynden GG, et al. Distinct molecular signature of inflammatory breast cancer by cDNA microarray analysis. Breast Cancer Res Treat. 2005;93:237–46.PubMedCrossRefGoogle Scholar
  75. 75.
    Van Laere SJ, Van der Auwera I, Van den Eynden GG, et al. Nuclear factor-kappaB signature of inflammatory breast cancer by cDNA microarray validated by quantitative real-time reverse transcription-PCR, immunohistochemistry, and nuclear factor-kappaB DNA-binding. Clin Cancer Res. 2006;12:3249–56.PubMedCrossRefGoogle Scholar
  76. 76.
    Van Laere SJ, Van der Auwera I, Van den Eynden GG, et al. NF-kB activation in inflammatory breast cancer is associated with oestrogen receptor downregulation, secondary to EGFR and/or ErbB2 overexpression and MAPK hyperactivation. Br J Cancer. 2007;97:659–69.PubMedCrossRefGoogle Scholar
  77. 77.
    Cabioglu N, Gong Y, Islam R, et al. Expression of growth factor and chemokine receptors: new insights in the biology of inflammatory breast cancer. Ann Oncol. 2007;18:1021–9.PubMedCrossRefGoogle Scholar
  78. 78.
    Parrett ML, Harris RE, Joarder FS, Ross MS, Clausen KP, Robertson FM. Cyclooxygenase-2 gene expression in human breast cancer. Int J Oncol. 1997;10:503–7.PubMedGoogle Scholar
  79. 79.
    González-Angulo AM, Guarneri V, Gong Y, et al. Downregulation of the cyclin-dependent kinase inhibitor p27kip1 might correlate with poor disease-free and overall survival in inflammatory breast cancer. Clin Breast Cancer. 2006;7:326–30.PubMedCrossRefGoogle Scholar
  80. 80.
    Nguyen DM, Sam K, Tsimelzon A, et al. Molecular heterogeneity of inflammatory breast cancer: a hyperproliferative phenotype. Clin Cancer Res. 2006;12:5047–54.PubMedCrossRefGoogle Scholar
  81. 81.
    Turpin E, Bièche I, Bertheau P, et al. Increased incidence of ERBB2 overexpression and TP53 mutation in inflammatory breast cancer. Oncogene. 2002;21:7593–7.PubMedCrossRefGoogle Scholar
  82. 82.
    Ben Hamida AB, Labidi IS, Mrad K, et al. Markers of subtypes in inflammatory breast cancer studied by immunohistochemistry: prominent expression of P-cadherin. BMC Cancer. 2008;8:28.PubMedCrossRefGoogle Scholar
  83. 83.
    Charafe-Jauffret E, et al. Immunophenotypic analysis of inflammatory breast cancers: identification of an “inflammatory signature”. J Pathol. 2004;202(3):265–73.PubMedCrossRefGoogle Scholar
  84. 84.
    Van Laere S, Limame R, Van Marck EA, et al. Is there a role for mammary stem cells in inflammatory breast carcinoma? A review of evidence from cell line, animal model, and human tissue sample experiments. Cancer. 2010;116 Suppl 11:2794–805.PubMedCrossRefGoogle Scholar
  85. 85.
    Smalley M, Ashworth A. Stem cells and breast cancer: a field in transit. Nat Rev Cancer. 2003;3:832–44.PubMedCrossRefGoogle Scholar
  86. 86.
    Pardal R, Clarke MF, Morisson SJ. Applying the principles of stem-cell biology to cancer. Nat Rev Cancer. 2003;3:895–902.PubMedCrossRefGoogle Scholar
  87. 87.
    Diallo R, Schaefer KL, Poremba C, et al. Monoclonality in normal epithelium and in hyperplastic and neoplastic lesions of the breast. J Pathol. 2001;193:27–32.PubMedCrossRefGoogle Scholar
  88. 88.
    Dontu G, Abdallah WM, Foley JM, et al. In vitro propagation and transcriptional profiling of human mammary stem/progenitor cells. Genes Dev. 2003;17:1253–70.PubMedCrossRefGoogle Scholar
  89. 89.
    Dontu G, Wicha MS. Survival of mammary stem cells in suspension culture: implications for stem cell biology and neoplasia. J Mammary Gland Biol Neoplasia. 2005;10:75–86.PubMedCrossRefGoogle Scholar
  90. 90.
    Al-Hajj M, Wicha MS, Benito-Hernández A, et al. Prospective identification of tumorigenic breast cancer cells. Proc Natl Acad Sci USA. 2003;100:3983–8.PubMedCrossRefGoogle Scholar
  91. 91.
    Ginestier C, Hur MH, Charafe-Jauffret E, et al. ALDH1 is a marker of normal and malignant human mammary stem cells and a predictor of poor clinical outcome. Cell Stem Cell. 2007;1:555–67.PubMedCrossRefGoogle Scholar
  92. 92.
    Wright MH, Calcagno AM, Salcido CD, et al. Brca1 breast tumors contain distinct CD44þ/CD24- and CD133þ cells with cancer stem cell characteristics. Breast Cancer Res. 2008;10:R10.PubMedCrossRefGoogle Scholar
  93. 93.
    Smalley MJ, Clarke RB. The mammary gland “side population”: a putative stem/progenitor cell marker? J Mammary Gland Biol Neoplasia. 2005;10:37–47.PubMedCrossRefGoogle Scholar
  94. 94.
    Clayton H, Titley I, Vivanco M. Growth and differentiation of progenitor/stem cells derived from the human mammary gland. Exp Cell Res. 2004;297:444–60.PubMedCrossRefGoogle Scholar
  95. 95.
    Bailey JM, Singh PK, Hollingsworth MA. Cancer metastasis facilitated by developmental pathways: sonic hedgehog, notch, and bone morphogenic proteins. J Cell Biochem. 2007;102:829–39.PubMedCrossRefGoogle Scholar
  96. 96.
    Korkaya H, Paulson A, Charafe-Jauffret E, et al. Regulation of mammary stem/progenitor cells by PTEN/Akt/beta-catenin signaling. PLoS Biol. 2009;7:e1000121.PubMedCrossRefGoogle Scholar
  97. 97.
    Xiao Y, Ye Y, Yearsley K, Jones S, Barsky SH. The lymphovascular embolus of inflammatory breast cancer expresses a stem cell-like phenotype. Am J Pathol. 2008;173:561–74.PubMedCrossRefGoogle Scholar
  98. 98.
    Charafe-Jauffret E, Ginestier C, Iovino F, et al. Breast cancer cell lines contain functional cancer stem cells with metastatic capacity and a distinct molecular signature. Cancer Res. 2009;69:1302–13.PubMedCrossRefGoogle Scholar
  99. 99.
    Gong Y, González-Angulo AM, Broglio K, et al. Expression of Notch-1 and b-catenin: defining the molecular portrait of inflammatory breast cancer. Breast Cancer Res Treat. 2006;100:S299.Google Scholar
  100. 100.
    Polyak K, Weinberg RA. Transitions between epithelial and mesenchymal states: acquisition of malignant and stem cell traits. Nat Rev Cancer. 2009;9:265–73.PubMedCrossRefGoogle Scholar
  101. 101.
    Mani SA, Guo W, Liao MJ, et al. The epithelial-mesenchymal transition generates cells with properties of stem cells. Cell. 2008;133:704–15.PubMedCrossRefGoogle Scholar
  102. 102.
    Zhang D, LaFortune TA, Krishnamurthy S, et al. Epidermal growth factor receptor tyrosine kinase inhibitor reverses mesenchymal to epithelial phenotype and inhibits metastasis in inflammatory breast cancer. Clin Cancer Res. 2009;15:6639–48.PubMedCrossRefGoogle Scholar
  103. 103.
    Bertucci F, Finetti P, Birnbaum D, et al. Gene expression profiling of inflammatory breast cancer. Cancer. 2010;116 Suppl 11:2783–93.PubMedCrossRefGoogle Scholar
  104. 104.
    Bertucci F, Finetti P, Rougemont J, et al. Gene expression profiling identifies molecular subtypes of inflammatory breast cancer. Cancer Res. 2005;65:2170–8.PubMedCrossRefGoogle Scholar
  105. 105.
    Van Laere SJ, Van den Eynden GG, Van der Auwera I, et al. Identification of cell-of-origin breast tumor subtypes in inflammatory breast cancer by gene expression profiling. Breast Cancer Res Treat. 2006;95:243–55.PubMedCrossRefGoogle Scholar
  106. 106.
    Van Laere S, Van der Auwera I, Van den Eynden G, et al. Distinct molecular phenotype of inflammatory breast cancer compared to non-inflammatory breast cancer using Affymetrix-based genome-wide gene-expression analysis. Br J Cancer. 2007;97:1165–74.PubMedCrossRefGoogle Scholar
  107. 107.
    Iwamoto T, Bianchini G, Qi Y, et al. Different gene expressions are associated with the different molecular subtypes of inflammatory breast cancer. Breast Cancer Res Treat. 2011;125:785–95.PubMedCrossRefGoogle Scholar
  108. 108.
    Boersma BJ, Reimers M, Yi M, et al. A stromal gene signature associated with inflammatory breast cancer. Int J Cancer. 2008;122:1324–32.PubMedCrossRefGoogle Scholar
  109. 109.
    Van der Auwera I, Limame R, Van Dam P, et al. Integrated miRNA and mRNA expression profiling of the inflammatory breast cancer subtype. Br J Cancer. 2010;103:532–41.PubMedCrossRefGoogle Scholar

Copyright information

© Springer-Verlag London 2013

Authors and Affiliations

  • Victor Manuel Perez-Sanchez
    • 1
  • Hector Aquiles Maldonado-Martinez
    • 1
  • Paula Juarez-Sanchez
    • 2
  • Abelardo Meneses-Garcia
    • 3
  1. 1.Department of PathologyInstituto Nacional de Cancerologia-MexicoMexico CityMexico
  2. 2.Department of PathologyInstituto Nacional de Cancerologia-Mexico (INCan), SsaMexico CityMexico
  3. 3.Department of Medical DirectionInstituto Nacional de Cancerologia-MexicoTlalpan, Mexico CityMexico

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