Abstract
Inflammatory breast cancer (IBC) is a rare and aggressive type of locally advanced breast cancer. The purpose of this study was to determine the value of microscopic tumour histomorphology texture for prognosis of local and systemic recurrence at the time of initial IBC diagnosis. This retrospective study included a group of 52 patients selected on the basis of non-metastatic IBC diagnosis, stage IIIB. Gray-Level-Co-Occurrence-Matrix (GLCM) texture analysis was performed on digital images of primary tumour tissue sections stained with haematoxylin/eosin. Obtained values were categorized by use of both data- and outcome-based methods. All five acquired GLCM texture features significantly associated with metastasis outcome. By accuracies of 69–81 % and AUCs of 0.71–0.81, prognostic performance of GLCM parameters exceeded that of standard major IBC clinical prognosticators such as tumour grade and response to induction chemotherapy. Furthermore, a composite score consisting of tumour grade, contrast and correlation as independent features resulted in further enhancement of prognostic performance by accuracy of 89 %, discrimination efficiency by AUC of 0.93 and an outstanding hazard ratio of 71.6 (95 %CI, 41.7–148.4). Internal validation was successfully performed by bootstrap and split-sample cross-validation, suggesting that the model is generalizable. This study indicates for the first time the potential use of primary breast tumour histology texture as a highly accurate, simple and cost-effective prognostic indicator of metastasis risk in IBC. Clinical relevance of the obtained results rests on the role of prognosis in decisions on induction chemotherapy and the resulting impact on quality of life and survival.
Similar content being viewed by others
References
D.G. Altman, L.M. McShane, W. Sauerbrei, S.E. Taube, PLoS Med. 9, e1001216 (2012)
H.K. Angell, N. Gray, C. Womack, D.I. Pritchard, R.W. Wilkinson, M. Cumberbatch, Br. J. Cancer 109, 1618 (2013)
A. Basavanhally, M. Feldman, N. Shih, C. Mies, J. Tomaszewski, S. Ganesan, A. Madabhushi, J. Pathol. Inf. 2, S1 (2011)
M. Buyse, S. Loi, L. van’t Veer, G. Viale, M. Delorenzi, A.M. Glas, M.S. d’Assignies, J. Bergh, R. Lidereau, P. Ellis, A. Harris, J. Bogaerts, P. Therasse, A. Floore, M. Amakrane, F. Piette, E. Rutgers, C. Sotiriou, F. Cardoso, M.J. Piccart, J. Natl. Cancer Inst. 98, 1183 (2006)
Y.C. Cheng, G. Rondon, Y. Yang, T.L. Smith, J.L. Gajewski, M.L. Donato, E.J. Shpall, R. Jones, G.N. Hortobagyi, R.E. Champlin, N.T. Ueno, Biol. Blood Marrow Transplant. 10, 794 (2004)
D.R. Cox, J. Roy. Stat. Soc. Ser. B Methodol. 34, 187 (1972)
M. Cristofanilli, V. Valero, A.U. Buzdar, S.W. Kau, K.R. Broglio, A.M. Gonzalez-Angulo, N. Sneige, R. Islam, N.T. Ueno, T.A. Buchholz, S.E. Singletary, G.N. Hortobagyi, Cancer 110, 1436 (2007)
J.M. Dunn, T. Hveem, M. Pretorius, D. Oukrif, B. Nielsen, F. Albregtsen, L.B. Lovat, M.R. Novelli, H.E. Danielsen, Br. J. Cancer 105, 1218 (2011)
B. Efron, Ann. Stat. 7, 1 (1979)
W. Gomez, W.C. Pereira, A.F. Infantosi, IEEE Trans. Med. Imaging 31, 1889 (2012)
R. Haralick, K. ShanmugamI, H. Dinstein, Systems, man and cybernetics. IEEE Trans. SMC 3, 610 (1973)
K. Holli, A.L. Laaperi, L. Harrison, T. Luukkaala, T. Toivonen, P. Ryymin, P. Dastidar, S. Soimakallio, H. Eskola, Acad. Radiol. 17, 135 (2010)
W. Huang, X. Li, Y. Chen, M.C. Chang, M.J. Oborski, D.I. Malyarenko, M. Muzi, G.H. Jajamovich, A. Fedorov, A. Tudorica, S.N. Gupta, C.M. Laymon, K.I. Marro, H.A. Dyvorne, J.V. Miller, D.P. Barbodiak, T.L. Chenevert, T.E. Yankeelov, J.M. Mountz, P.E. Kinahan, R. Kikinis, B. Taouli, F. Fennessy, J. Kalpathy-Cramer, Transl. Oncol. 7, 153 (2014)
A.C. Justice, K.E. Covinsky, J.A. Berlin, Ann. Intern. Med. 130, 515 (1999)
M.R. Kell, M. Morrow, Breast Dis. 22, 67 (2005)
D. Kolarevic, Z. Tomasevic, R. Dzodic, D. Gavrilovic, M. Zegarac, J. BUON 17, 21 (2012)
A. Laurinavicius, A. Laurinaviciene, D. Dasevicius, N. Elie, B. Plancoulaine, C. Bor, P. Herlin, Anal. Cell. Pathol. 35, 75 (2012)
A. Laurinavicius, B. Plancoulaine, A. Laurinaviciene, P. Herlin, R. Meskauskas, I. Baltrusaityte, J. Besusparis, D. Dasevi Ius, N. Elie, Y. Iqbal, C. Bor, I.O. Ellis, Breast Cancer Res. 16, R35 (2014)
G.A. Losa, C. Castelli, Cell Tissue Res. 322, 257 (2005)
C. Loukas, S. Kostopoulos, A. Tanoglidi, D. Glotsos, C. Sfikas, D. Cavouras, Comput. Math. Methods Med. 2013, 829461 (2013)
Marchionni A. Curr. Pharm. Des. 2013.
L. Marchionni, B. Afsari, D. Geman, J.T. Leek, BMC Genomics 14, 336 (2013)
Matro JM, Li T, Cristofanilli M, Hughes ME, Ottesen RA, Weeks JC, Wong YN. Clin Breast. Cancer. 2014.
A. Mohd Khuzi, R. Besar, W. Wan Zaki, N. Ahmad, Biomed. Imaging. Interv. J 5, e17 (2009)
M. Oger, M. Allaoui, N. Elie, J. Marnay, P. Herlin, B. Plancoulaine, J. Chasle, V. Becette, C. Bor-Angelier, Diagostic. Pathol. 8, S43 (2013)
I. Pantic, S. Pantic, J. Paunovic, Microsc. Microanal. 18, 1054 (2012a)
I. Pantic, S. Pantic, G. Basta-Jovanovic, Microsc. Microanal. 18, 470 (2012b)
I. Pantic, D. Nesic, D. Stevanovic, V. Starcevic, S. Pantic, V. Trajkovic, Microsc. Microanal. 19, 553 (2013a)
I. Pantic, G. Basta-Jovanovic, V. Starcevic, J. Paunovic, S. Suzic, Z. Kojic, S. Pantic, Nephrology 18, 117 (2013b)
S. Petushi, F.U. Garcia, M.M. Haber, C. Katsinis, A. Tozeren, BMC Med. Imaging 6, 14 (2006)
G. Somlo, P. Frankel, W. Chow, L. Leong, K. Margolin, R. Morgan Jr., S. Shibata, P. Chu, S. Forman, D. Lim, P. Twardowski, J. Weitzel, J. Alvarnas, N. Kogut, J. Schriber, E. Fermin, Y. Yen, L. Damon, J.H. Doroshow, J. Clin. Oncol. 22, 1839 (2004)
M. Tambasco, A.M. Magliocco, Hum. Pathol. 39, 740 (2008)
M. Tambasco, M. Eliasziw, A.M. Magliocco, J. Transl. Med. 8, 140 (2010)
N.T. Ueno, A.U. Buzdar, S.E. Singletary, F.C. Ames, M.D. McNeese, F.A. Holmes, R.L. Theriault, E.A. Strom, B.J. Wasaff, L. Asmar, D. Frye, G.N. Hortobagyi, Cancer Chemother. Pharmacol. 40, 321 (1997)
M.J. van de Vijver, Y.D. He, L.J. van’t Veer, H. Dai, A.A. Hart, D.W. Voskuil, G.J. Schreiber, J.L. Peterse, C. Roberts, M.J. Marton, M. Parrish, D. Atsma, A. Witteveen, A. Glas, L. Delahaye, T. van der Velde, H. Bartelink, S. Rodenhuis, E.T. Rutgers, S.H. Friend, R. Bernards, N. Engl. J. Med. 347, 1999 (2002)
S.J. Van Laere, N.T. Ueno, P. Finetti, P. Vermeulen, A. Lucci, F.M. Robertson, M. Marsan, T. Iwamoto, S. Krishnamurthy, H. Masuda, P. van Dam, W.A. Woodward, P. Viens, M. Cristofanilli, D. Birnbaum, L. Dirix, J.M. Reuben, F. Bertucci, Clin. Cancer Res. 19, 4685 (2013)
van Uden DJ, van Laarhoven HW, Westenberg AH, de Wilt JH, Blanken-Peeters CF. Crit. Rev. Oncol. Hematol. 2014.
D.G. Vince, K.J. Dixon, R.M. Cothren, J.F. Cornhill, Comput. Med. Imaging Graph. 24, 221 (2000)
Conflict of interest
The authors declare that they have no conflict of interest.
Funding
This work was supported by the research Grant No. 175068 from the Ministry of Education and Science of the Republic of Serbia.
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Kolarevic, D., Tomasevic, Z., Dzodic, R. et al. Early prognosis of metastasis risk in inflammatory breast cancer by texture analysis of tumour microscopic images. Biomed Microdevices 17, 92 (2015). https://doi.org/10.1007/s10544-015-9999-9
Published:
DOI: https://doi.org/10.1007/s10544-015-9999-9