Abstract
Breast cancer prognosis is a subject undergoing intense study due to its high clinical relevance for effective therapeutic management and a great patient interest in disease progression. Prognostic value of fractal and gray level co-occurrence matrix texture analysis algorithms has been previously established on tumour histology images, but without any direct performance comparison. Therefore, this study was designed to compare the prognostic power of the monofractal, multifractal and co-occurrence algorithms on the same set of images. The investigation was retrospective, with 51 patients selected on account of non-metastatic IBC diagnosis, stage IIIB. Image analysis was performed on digital images of primary tumour tissue sections stained with haematoxylin/eosin. Bootstrap-corrected Cox proportional hazards regression P-values indicated a significant association with metastasis outcome of at least one of the features within each group. AUC values were far better for co-occurrence (0.66–0.77) then for fractal features (0.60–0.64). Correction by the split-sample cross-validation likewise indicated the generalizability only for the co-occurrence features, with their classification accuracies ranging between 67 and 72 %, while accuracies of monofractal and multifractal features were reduced to nearly random 52–55 %. These findings indicate for the first time that the prognostic value of texture analysis of tumour histology is less dependent on the morphological complexity of the image as measured by fractal analysis, but predominantly on the spatial distribution of the gray pixel intensities as calculated by the co-occurrence features.
Similar content being viewed by others
References
M. Aldana, E. Balleza, S. Kauffman, O. Resendiz, J. Theor. Biol. 245, 433 (2007)
D. G. Altman, L. M. McShane, W. Sauerbrei, S. E. Taube, BMC Med 10, 51 (2012)
H. K. Angell, N. Gray, C. Womack, D. I. Pritchard, R. W. Wilkinson, M. Cumberbatch, Br. J. Cancer 109, 1618 (2013)
S. Arivazhagan, L. Ganesan, Pattern Recogn. Lett. 24, 1513 (2003)
C. Atupelage, H. Nagahashi, M. Yamaguchi, M. Sakamoto, A. Hashiguchi, Anal Cell Pathol (Amst) 35, 123 (2012)
S. Banik, R. M. Rangayyan, J. E. Desautels, IEEE Transactions on Medical Imaging 30, 279 (2011)
A. Basavanhally, M. Feldman, N. Shih, C. Mies, J. Tomaszewski, S. Ganesan, A. Madabhushi, J Pathol Inform 2, S1 (2011)
A.H. Beck, A.R. Sangoi, S. Leung, R.J. Marinelli, T.O. Nielsen, M.J. van de Vijver, R.B. West, M. van de Rijn, D. Koller, Sci Transl Med 3, 108ra113 (2011).
H. J. Bloom, W. W. Richardson, Br. J. Cancer 11, 359 (1957)
B. Braverman, M. Tambasco, Comput Math Methods Med 2013, 262931 (2013)
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)
A. B. Chhabra, C. Meneveau, R. V. Jensen, K. R. Sreenivasan, Phys Rev A 40, 5284 (1989)
D. R. Cox, J. R. 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. E. Cutting, J. J. Garvin, Perception and Psychophysics 42, 365 (1987)
L. Dettori, L. Semler, Comput. Biol. Med. 37, 486 (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)
C. W. Elston, I. O. Ellis, Histopathology 41, 154 (2002)
T. R. Faisal, N. Hristozov, A. D. Rey, T. L. Western, D. Pasini, Phys Rev E Stat Nonlin Soft Matter Phys 86, 031921 (2012)
M. Galloway, Computer Graphics and Image Processing 4, 172 (1975)
A. Giordano, H. Gao, S. Anfossi, E. Cohen, M. Mego, B. N. Lee, S. Tin, M. De Laurentiis, C. A. Parker, R. H. Alvarez, V. Valero, N. T. Ueno, S. De Placido, S. A. Mani, F. J. Esteva, M. Cristofanilli, J. M. Reuben, Mol. Cancer Ther. 11, 2526 (2012)
W. Gomez, W. C. Pereira, A. F. Infantosi, IEEE Transactions on Medical Imaging 31, 1889 (2012)
R. M. Haralick, Proc. IEEE 67, 786 (1979)
R. Haralick, K. Shanmugam, I. H. Dinstein, Systems, Man and Cybernetics. IEEE Transactions on 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)
A. C. Justice, K. E. Covinsky, J. A. Berlin, Ann. Intern. Med. 130, 515 (1999)
A. Karperien, H. Ahammer, H. F. Jelinek, Front. Cell. Neurosci. 7, 3 (2013)
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)
D. Kolarevic, Z. Tomasevic, R. Dzodic, K. Kanjer, D. N. Vukosavljevic, M. Radulovic, Biomed. Microdevices 17, 92 (2015)
A. Kurakin, Theor Biol Med Model 8, 4 (2011)
G. Landini, J. Microsc. 241, 1 (2011)
G. Landini, P. I. Murray, G. P. Misson, Investig. Ophthalmol. Vis. Sci. 36, 2749 (1995)
A. Laurinavicius, A. Laurinaviciene, D. Dasevicius, N. Elie, B. Plancoulaine, C. Bor, P. Herlin, Anal Cell Pathol (Amst) 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)
C. Loukas, S. Kostopoulos, A. Tanoglidi, D. Glotsos, C. Sfikas, D. Cavouras, Comput Math Methods Med 2013, 829461 (2013)
B. B. Mandelbrot, The fractal geometry of nature (W.H. Freeman, New York, 1983)
K. Metze, Epigenomics 2, 601 (2010)
K. Metze, Expert. Rev. Mol. Diagn. 13, 719 (2013)
A. Mohd Khuzi, R. Besar, W. Wan Zaki, N. Ahmad, Biomed Imaging Interv J 5, e17 (2009)
V. Neumeister, S. Agarwal, J. Bordeaux, R. L. Camp, D. L. Rimm, Am. J. Pathol. 176, 2131 (2010)
F. Normant, C. Tricot, Phys Rev A 43, 6518 (1991)
M. Oger, M. Allaoui, N. Elie, J. Marnay, P. Herlin, B. Plancoulaine, J. Chasle, V. Becette, C. Bor-Angelier, Diagostic Pathology 8, S43 (2013)
I. Pantic, S. Pantic, J. Paunovic, Microsc. Microanal. 18, 1054 (2012)
I. Pantic, G. Basta-Jovanovic, V. Starcevic, J. Paunovic, S. Suzic, Z. Kojic, S. Pantic, Nephrology (Carlton) 18, 117 (2013a)
I. Pantic, D. Nesic, D. Stevanovic, V. Starcevic, S. Pantic, V. Trajkovic, Microsc. Microanal. 19, 553 (2013b)
I. Pantic, J. Paunovic, G. Basta-Jovanovic, M. Perovic, S. Pantic, N. T. Milosevic, Exp. Gerontol. 48, 926 (2013c)
I. Pantic, S. Dacic, P. Brkic, I. Lavrnja, S. Pantic, T. Jovanovic, S. Pekovic, Microsc. Microanal. 20, 1373 (2014)
L. G. Perez-Rivas, J. M. Jerez, R. Carmona, V. de Luque, L. Vicioso, M. G. Claros, E. Viguera, B. Pajares, A. Sanchez, N. Ribelles, E. Alba, J. Lozano, PLoS One 9, e91884 (2014)
S. Petushi, F. U. Garcia, M. M. Haber, C. Katsinis, A. Tozeren, BMC Med Imaging 6, 14 (2006)
J. Pribic, J. Vasiljevic, K. Kanjer, Z. N. Konstantinovic, N. T. Milosevic, D. N. Vukosavljevic, M. Radulovic, Biomark. Med 9, 1279 (2015)
J. V. Raja, M. Khan, V. K. Ramachandra, O. Al-Kadi, Dento-Maxillo-Facial. Radiology 41, 475 (2012)
K. Rajkovic, G. Bacic, D. Ristanovic, N. T. Milosevic, Biomed Res Int 2014, 812351 (2014)
R. Rouzier, P. Pronzato, E. Chereau, J. Carlson, B. Hunt, W. J. Valentine, Breast Cancer Res. Treat. 139, 621 (2013)
B. Sahiner, H. P. Chan, N. Petrick, M. A. Helvie, L. M. Hadjiiski, Med. Phys. 28, 1455 (2001)
S. J. Schnitt, Modern Pathology 23(Suppl 2), S60 (2010)
T. G. Smith Jr., G. D. Lange, W. B. Marks, J. Neurosci. Methods 69, 123 (1996)
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)
M. Tanase, P. Waliszewski, Journal of. Surg. Oncol. 112, 791 (2015)
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)
D. J. van Uden, H. W. van Laarhoven, A. H. Westenberg, J. H. de Wilt, C. F. Blanken-Peeters, Crit Rev Oncol Hematol 93, 116–126 (2014)
T. Vujasinovic, J. Pribic, K. Kanjer, N. T. Milosevic, Z. Tomasevic, Z. Milovanovic, D. Nikolic-Vukosavljevic, M. Radulovic, Microsc. Microanal. 21, 646 (2015)
E. R. Weibel, American Journal of Physiology 261, L361 (1991)
Y. **ang, V. R. Yingling, R. Malique, C. Y. Li, M. B. Schaffler, T. Raphan, Bone 40, 544 (2007)
Y. Zheng, B. M. Keller, S. Ray, Y. Wang, E. F. Conant, J. C. Gee, D. Kontos, Med. Phys. 42, 4149 (2015)
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
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.
Rights and permissions
About this article
Cite this article
Rajković, N., Kolarević, D., Kanjer, K. et al. Comparison of Monofractal, Multifractal and gray level Co-occurrence matrix algorithms in analysis of Breast tumor microscopic images for prognosis of distant metastasis risk . Biomed Microdevices 18, 83 (2016). https://doi.org/10.1007/s10544-016-0103-x
Published:
DOI: https://doi.org/10.1007/s10544-016-0103-x