A novel, patient-specific mathematical pathology approach for assessment of surgical volume: Application to ductal carcinoma in situ of the breast

Analytical Cellular Pathology

Volumn 34, Issue 5, 2011, Pages 247-263

  Edgerton, Mary E ^a   Chuang, Yao Li ^b,c   MacKlin, Paul ^c,e,f   Yang, Wei ^d   Bearer, Elaine L ^b   Cristini, Vittorio ^b,c  

^a UNIVERSITY OF TEXAS MEDICAL SCHOOL   (United States)

^b UNIVERSITY OF NEW MEXICO SCHOOL OF MEDICINE   (United States)

^c UNIVERSITY OF TEXAS   (United States)

^d UNIVERSITY OF TEXAS MD ANDERSON CANCER CENTER   (United States)

^e UNIVERSITY OF DUNDEE   (United Kingdom)

^f UNIVERSITY OF SOUTHERN CALIFORNIA   (United States)

Author keywords

cell death; cell proliferation; DCIS; IHC analysis; mathematical model; patient histology

Indexed keywords

CASPASE 3; KI 67 ANTIGEN;

APOPTOSIS; ARTICLE; CANCER GRADING; CANCER PATIENT; CELL PROLIFERATION; DIAGNOSTIC ACCURACY; DIFFUSION; HUMAN; HUMAN TISSUE; IMMUNOHISTOCHEMISTRY; INTRADUCTAL CARCINOMA; MAMMOGRAPHY; MATHEMATICAL MODEL; MITOSIS; MORPHOMETRICS; NUTRIENT; PRIORITY JOURNAL; PROGNOSIS; PROTEIN CLEAVAGE; SIMULATION; TREATMENT PLANNING; TUMOR BIOPSY; TUMOR GROWTH; TUMOR VOLUME;

APOPTOSIS; BREAST NEOPLASMS; CARCINOMA, INTRADUCTAL, NONINFILTRATING; CASPASE 3; CELL PROLIFERATION; COMPUTER SIMULATION; DECISION SUPPORT TECHNIQUES; DIFFUSION; ENERGY METABOLISM; FEMALE; HUMANS; IMMUNOHISTOCHEMISTRY; KI-67 ANTIGEN; MAMMOGRAPHY; MASTECTOMY; MITOTIC INDEX; MODELS, BIOLOGICAL; PATIENT SELECTION; RETROSPECTIVE STUDIES; TIME FACTORS; TUMOR BURDEN;

EID: 80054995386     PISSN: 22107177     EISSN: 22107185     Source Type: Journal    
DOI: 10.3233/ACP-2011-0019     Document Type: Article

References (59)

1. V. Cristini, J. Lowengrub and Q. Nie, Nonlinear simulation of tumor growth, J Math Biol 46 (2003), 191-224. (Pubitemid 38355715)
2. H.B. Frieboes, X. Zheng, C.H. Sun, B. Tromberg, R. Gatenby and V. Cristini, An integrated computational/experimental model of tumor invasion, Cancer Research 66 (2006), 1597-1604. (Pubitemid 43259943)
3. M.D. Szeto, G. Chakraborty, J. Hadley, R. Rockne, M. Muzi, E.C. Alvord Jr., A.M. Spence and K.R. Swanson, Quantitative metrics of net proliferation and invasion link biological aggressiveness assessed by MRI with hypoxia assessed by FMISO-PET in newly diagnosed glioblastomas, Cancer Research 69 (2009), 4502-4509.
4. C.H. Wang, J.K. Rockhill, M. Mrugala, D.L. Peacock, A. Lai, K. Jusenius, J.M. Wardlaw, T. Cloughesy, A.M. Spence, R. Rockne, E.C. Alvord Jr. and K.R. Swanson, Prognostic significance of growth kinetics in newly diagnosed glioblastomas revealed by combining serial imaging with a novel biomathematical model, Cancer Research 69 (2009), 9133-9140.
5. H. Hatzikirou, A. Chauviere, J.S. Lowengrub, J.D. Groot andV. Cristini, The effect of vascularization on glioma growth, Tumor Vascularture: Molecular, cellular, and tissue level aspects and implications, in: Tumor Vasculature: Molecular, Cellular, and Tissue level Aspects and Implications T. Jackson, ed., Springer, New York (2011).
6. W.D. Dupont and D.L. Page, Risk factors for breast cancer in women with proliferative breast disease, N Engl J Med 312 (1985), 146-151. (Pubitemid 15192861)
7. D.L. Page, W.D. Dupont, L.W. Rogers and M. Landenberger, Intraductal carcinoma of the breast: Follow-up after biopsy only, Cancer 49 (1982), 751-758. (Pubitemid 12165434)
8. M.E. Sanders, P.A. Schuyler, W.D. Dupont and D.L. Page, The natural history of low-grade ductal carcinoma in situ of the breast in women treated by biopsy only revealed over 30 years of long-term follow-up, Cancer 103 (2005), 2481-2484. (Pubitemid 40800525)
9. J.F. Simpson and D.L. Page, Pathology of preinvasive and excellent prognosis breast cancer, Curr Opin Oncol 13 (2001), 426-430. (Pubitemid 33027893)
10. L.C. Collins, R.M. Tamimi, H.J. Baer, J.L. Connolly, G.A. Colditz and S.J. Schnitt, Outcome of patients with ductal carcinoma in situ untreated after diagnostic biopsy: Results from the Nurses' Health Study, Cancer 103 (2005), 1778-1784. (Pubitemid 40563248)
11. V. Eusebi, E. Feudale, M.P. Foschini, A. Micheli, A. Conti, C. Riva, S. Di Palma and F. Rilke, Long-term follow-up of in situ carcinoma of the breast, Semin Diagn Pathol 11 (1994), 223-235. (Pubitemid 24308083)
12. N. Cabioglu, K.K. Hunt, A.A. Sahin, H.M. Kuerer, G.V. Babiera, S.E. Singletary, G.J. Whitman, M.I. Ross, F.C. Ames, B.W. Feig, T.A. Buchholz and F. Meric-Bernstam, Role for intraoperative margin assessment in patients undergoing breast-conserving surgery, Ann Surg Oncol 14 (2007), 1458-1471. (Pubitemid 46536814)
13. L. Cheng, N.K. Al-Kaisi, N.H. Gordon, A.Y. Liu, F. Gebrail and R.R. Shenk, Relationship between the size and margin status of ductal carcinoma in situ of the breast and residual disease, J Natl Cancer Inst 89 (1997), 1356-1360. (Pubitemid 27418026)
14. M.F. Dillon, A.A. Maguire, E.W. McDermott, C. Myers, A.D. Hill, A. O'Doherty and C.M. Quinn, Needle core biopsy characteristics identify patients at risk of compromised margins in breast conservation surgery, Mod Pathol 21 (2008), 39-45.
15. N. Patani, B. Cutuli and K. Mokbel, Current management of DCIS: A review, Breast Cancer Res Treat 111 (2008), 1-11.
16. M.J. Silverstein, Predicting residual disease and local recurrence in patients with ductal carcinoma in situ, J Natl Cancer Inst 89 (1997), 1330-1331.
17. E.M. Nichols, A.A. Dhople, M.M. Mohiuddin, T.W. Flannery, C.X. Yu and W.F. Regine, Comparative analysis of the post lumpectomy target volume versus the use of pre-lumpectomy tumor volume for early-stage breast cancer: Implications for the future, Int J Radiation Oncology Biol Phys 77 (2010), 197-202.
18. A. Bankhead, 3rd, N.S. Magnuson and R.B. Heckendorn, Cellular automaton simulation examining progenitor hierarchy structure effects on mammary ductal carcinoma in situ, J Theor Biol 246 (2007), 491-498. (Pubitemid 46669565)
19. S.J. Franks, H.M. Byrne, H.S. Mudhar, J.C. Underwood and C.E. Lewis, Mathematical modelling of comedo ductal carcinoma in situ of the breast, Math Med Biol 20 (2003), 277-308. (Pubitemid 37526838)
20. S.J. Franks, H.M. Byrne, J.C. Underwood and C.E. Lewis, Biological inferences from a mathematical model of comedo ductal carcinoma in situ of the breast, J Theor Biol 232 (2005), 523-543. (Pubitemid 39575095)
21. R.A. Gatenby, E.T. Gawlinski, A.F. Gmitro, B. Kaylor and R.J. Gillies, Acid-mediated tumor invasion: A multidisciplinary study, Cancer Res 66 (2006), 5216-5223. (Pubitemid 43844945)
22. R.A. Gatenby, K. Smallbone, P.K. Maini, F. Rose, J. Averill, R.B. Nagle, L.Worrall and R.J. Gillies, Cellular adaptations to hypoxia and acidosis during somatic evolution of breast cancer, Br J Cancer 97 (2007), 646-653. (Pubitemid 47339892)
23. Y. Kim, M.A. Stolarska and H.G. Othmer, The role of the microenvironment in tumor growth and invasion, Prog Biophys Mol Biol 106 (2011), 353-379.
24. P. Macklin, M.E. Edgerton, A.M. Thompson and V. Cristini, Patient-calibrated agent-based modelling of ductal carcinoma in situ (DCIS): From microscopic measurements to macroscopic predictions of clinical progression, J Theor Biol (in review).
25. K.A. Norton, M.Wininger, G. Bhanot, S. Ganesan, N. Barnard and T. Shinbrot, A 2D mechanistic model of breast ductal carcinoma in situ (DCIS) morphology and progression, J Theor Biol 263 (2010), 393-406.
26. K.A. Rejniak and A.R. Anderson, A computational study of the development of epithelial acini: II. Necessary conditions for structure and lumen stability, Bull Math Biol 70 (2008), 1450-1479.
27. K.A. Rejniak and A.R. Anderson, A computational study of the development of epithelial acini: I. Sufficient conditions for the formation of a hollow structure, Bull Math Biol 70 (2008), 677-712.
28. A.S. Silva, R.A. Gatenby, R.J. Gillies and J.A. Yunes, A quantitative theoretical model for the development of malignancy in ductal carcinoma in situ, J Theor Biol 262 (2010), 601-613.
29. L. Sontag and D.E. Axelrod, Evaluation of pathways for progression of heterogeneous breast tumors, J Theor Biol 232 (2005), 179-189. (Pubitemid 39458046)
30. P. Macklin, M.E. Edgerton and V. Cristini, Agent-based cell modeling: Application to breast cancer, in: Multiscale Modeling of Cancer: An Integrated Experimental and Mathematical Modeling Approach, V. Cristini and J. Lowengrub, Cambridge University Press, Cambridge, (2010) pp. 206-234.
31. H. Frieboes, M.E. Edgerton, J.P. Fruehauf, F.R.A.J. Rose, L.K. Worral, R. Gatenby, M. Ferrari and V. Cristini, Prediction of drug response in breast cancer using integrative experimental/computational modeling, Cancer Res 69 (2009), 4484-4492.
32. M. Edgerton, Y. Chuang, P. Macklin, S. Sanga, J. Kim, G. Tomaiuolo, Y. Wang, A. Broom, K. Do and V. Cristini, Using mathematical models to understand the time dependence of the growth of ductal carcinoma in situ, Cancer Research 69 (Suppl 2) (2009), 1165.
33. P. Macklin, J. Kim, G. Tomaiuolo, M.E. Edgerton and V. Cristini, Agent-based modeling of ductal carcinoma in situ: application to patient-specific breast cancer modeling, in: Computational Biology: Issues and Applications in Oncology, T. Pham, eds., Springer, New York, (2009), pp. 77-112.
34. P. Macklin, M.E. Edgerton, J.S. Lowengrub and V. Cristini, Discrete cell modeling, in: Multiscale Modeling of Cancer: An Integrated Experimental and Mathematical Modeling Approach,V. Cristini and J. Lowengrub, Cambridge University Press, Cambridge, 2010, pp. 88-122.
35. H. Kuerer, C. Albarracin, W. Yang, R. Cardiff, A. Brewster, W. Symmans, N. Hylton, L. Middleton, S. Krishnamurthy, G. Perkins, G. Babiera, M. Edgerton, B. Czerniecki, B. Arun and G. Hortobagyi, Ductal carcinoma in situ, state of the science and roadmap to advance the field, J Clin Onc 27 (2009), 279-288.
36. K.D. Mannes, M.E. Edgerton, J.F. Simpson, R.A. Jensen and D.L. Page, pagetoid spread in ductal Carcinoma in situ, characterization and computer simulation, United States and Conadian Academy of Pathology (USCAP) Annual Meeting 2002.
37. M.R. Owen, H.M. Byrne and C.E. Lewis, Mathematical modelling of the use of macrophages as vehicles for drug delivery to hypoxic tumour sites, J Theor Biol 226 (2004), 377-391. (Pubitemid 38169378)
38. S. Lee, S.K. Mohsin, S. Mao, S.G. Hilsenbeck, D. Medina and D.C. Allred, Hormones, receptors, and growth in hyperplastic enlarged lobular units: Early potential precursors of breast cancer, Breast Cancer Res 8 (2006), R6.
39. J.L. Scarlett, P.W. Sheard, G. Hughes, E.C. Ledgerwood, H.H. Ku and M.P. Murphy, Changes in mitochondrial membrane potential during staurosporine-induced apoptosis in Jurkat cells, FEBS Lett 475 (2000), 267-272. (Pubitemid 30408466)
40. Z. Hu, K. Yuri, H. Ozawa, H. Lu and M. Kawata, The in vivo time course for elimination of adrenalectomy-induced apoptotic profiles from the granule cell layer of the rat hippocampus, J Neurosci 17 (1997), 3981-3989. (Pubitemid 27220589)
41. J.F. Kerr, C.M. Winterford and B.V. Harmon, Apoptosis. Its significance in cancer and cancer therapy, Cancer 73 (1994), 2013-2026. (Pubitemid 24107952)
42. J.P. Ward and J.R. King, Mathematical modelling of avascular-tumour growth, IMA J Math Appl Med Biol 14 (1997), 39-69. (Pubitemid 127463789)
43. J. Gerdes, H. Lemke, H. Baisch, H.H.Wacker, U. Schwab and H. Stein, Cell cycle analysis of a cell proliferation-associated human nuclear antigen defined by the monoclonal antibody Ki-67, J Immunology 133 (1984), 1710-1715. (Pubitemid 14035254)
44. W.R. Duan, D.S. Garner, S.D.Williams, C.L. Funckes-Shippy, I.S. Spath and E.A.G. Blomme, Comparison of immunohistochemistry for activated caspase-3 and cleaved cytokeratin 18 with the TUNEL method for quantification of apoptosis in histological sections of PC-3 subcutaneous xenografts, J Pathol 199 (2003).
45. Y.-l. Chuang, M.E. Edgerton, P. Macklin, J. Kim, A. Segura, G. Tomaiuolo, S. Sanga and V. Cristini, Bridging the gap between mathematical modeling and pathological data: An application of multiscale modeling to ductal carminoma in situ, in: Biophysical Modeling of Cancer in Silico V. Cristini, Springer, New York, 2012 (in preparation).
46. G. Cumming, F. Fidler and D.L. Vaux, Error bars in experimental biology, J Cell Biol 177 (2007), 7-11. (Pubitemid 46588396)
47. J.P.Morton, Reviewing scientific manuscripts: How much statistical knowledge should a reviewer really know? Adv Physiol Educ 33 (2009), 7-9.
48. J.H. Menell, E.A. Morris, D.D. Dershaw, A.F. Abramson, E. Brogi and L. Liberman, Determination of the presence and extent of pure ductal carcinoma in situ by mammography and magnetic resonance imaging, Breast J 11 (2005), 382-390. (Pubitemid 41743410)
49. A. Grin, G. Horne, M. Ennis and F.P. O'Malley, Measuring extent of ductal carcinoma in situ in breast excision specimens: A comparison of 4 methods, Arch Pathol Lab Med 133 (2009), 31-37.
50. L.P.Middleton, G. Vlastos, N.Q. Mirza, S. Eva and A.A. Sahin, Multicentric mammary carcinoma: Evidence of monoclonal proliferation, Cancer 94 (2002), 1910-1916. (Pubitemid 34270042)
51. J. Spratt, L. Heuser, J.G. Kuhns, H.M. Reiman, J.B. Buchanan, H.C. Polk Jr. and J. Sandoz, Association between the actual doubling times of primary breast cancer with histopathologic characteristics and Wolfe's parenchymal mammographic patterns, Cancer 47 (1981), 2265-2268. (Pubitemid 11098601)
52. J.Z. Thomson, A.J. Evans, S.E. Pinder, H.C. Burrell, A.R.M. Wilson, and I.O. Ellis, Growth pattern of ductal carcinoma in situ (DCIS): A retrospective analysis based on mammographic findings, Br J Cancer 85 (2001), 225-227. (Pubitemid 32695743)
53. A. Gandhl, P.A. Holland,W.F. Knox, C.S. Potten and N.J. Bundred, Evidence of significant apoptosis in poorly differentiated ductal carcinoma in situ of the breast, Br J Cancer 78 (1998), 788-794. (Pubitemid 28418315)
54. S. Chan, J.H. Chen, G. Agrawal, M. Lin, R.S. Mehta, P.M. Carpenter, O. Nalcloglu and M.Y. Su, Characterization of pure ductal carcinoma in situ on dynamic contrast-enhanced MR Imaging: Do nonhigh grade and high grade show different imaging features?, J Oncol 2010 (2010), 431341.
55. H. Liu andW. Peng,MRImorphological classification of ductal carcinoma in situ (DCIS) correlating with different biological behavior, Eur J Radiol (2011, in press).
56. J. Chakrabarti, A.J. Evans, J. James, I.O. Ellis, S.E. Pinder and R.D. Macmillan, Accuracy of mammography in predicting histological extent of ductal carcinoma in situ (DCIS), Eur J Surg Oncol 32 (2006), 1089-1092. (Pubitemid 44774396)
57. T.W. Yen, K.K. Hunt, M.I. Ross, N.Q. Mirza, G.V. Babiera, F. Meric-Bernstam, S.E. Singletary, W.F. Symmans, S.H. Giordano, B.W. Feig, F.C. Ames and H.M. Kuerer, Predictors of invasive breast cancer in patients with an initial diagnosis of ductal carcinoma in situ: A guide to selective use of sentinel lymph node biopsy in management of ductal carcinoma in situ, J Am Coll Surg 200 (2005), 516-526. (Pubitemid 40432319)
58. E.S. Hwang, A. Lai, Y.-Y. Chen, S. DeVries, R. Swain, J. Anderson, R. Roy and F.M. Waldman, Genomic alterations and phenotype of large compared to small high-grade ductal carcinoma in situ, Hum Pathology (2011, in press).
59. A.M. Brewster, P. Thompson, A.A. Sahin, K. Do, M.E. Edgerton, S. Tsavaschidis, R. Zhou, Y. Liu, L. Zhang, G. Mills and M. Bondy, Copy number imbalances between screen and symptom-detected breast cancers and impact on disease-free survival, Cancer Prevention Research (2011, in press).