Patient-specific metrics of invasiveness reveal significant prognostic benefit of resection in a predictable subset of gliomas

Anne L. Baldock, Sunyoung Ahn, Russell Rockne, Sandra Johnston, Maxwell Neal, David Corwin, Kamala Clark-Swanson, Greg Sterin, Andrew D. Trister, Hani Malone, Victoria Ebiana, Adam M. Sonabend, Maciej Mrugala, Jason K. Rockhill, Daniel L. Silbergeld, Albert Lai, Timothy Cloughesy, Guy M. McKhann, Jeffrey N. Bruce, Robert C. RostomilyPeter Canoll, Kristin Swanson

Research output: Contribution to journalArticle

25 Citations (Scopus)

Abstract

Object: Malignant gliomas are incurable, primary brain neoplasms noted for their potential to extensively invade brain parenchyma. Current methods of clinical imaging do not elucidate the full extent of brain invasion, making it difficult to predict which, if any, patients are likely to benefit from gross total resection. Our goal was to apply a mathematical modeling approach to estimate the overall tumor invasiveness on a patient-by-patient basis and determine whether gross total resection would improve survival in patients with relatively less invasive gliomas.

Methods: In 243 patients presenting with contrast-enhancing gliomas, estimates of the relative invasiveness of each patient's tumor, in terms of the ratio of net proliferation rate of the glioma cells to their net dispersal rate, were derived by applying a patient-specific mathematical model to routine pretreatment MR imaging. The effect of varying degrees of extent of resection on overall survival was assessed for cohorts of patients grouped by tumor invasiveness.

Results: We demonstrate that patients with more diffuse tumors showed no survival benefit (P = 0.532) from gross total resection over subtotal/biopsy, while those with nodular (less diffuse) tumors showed a significant benefit (P = 0.00142) with a striking median survival benefit of over eight months compared to sub-totally resected tumors in the same cohort (an 80% improvement in survival time for GTR only seen for nodular tumors).

Conclusions: These results suggest that our patient-specific, model-based estimates of tumor invasiveness have clinical utility in surgical decision making. Quantification of relative invasiveness assessed from routinely obtained pre-operative imaging provides a practical predictor of the benefit of gross total resection.

Original languageEnglish (US)
Article numbere99057
JournalPLoS One
Volume9
Issue number10
DOIs
StatePublished - Oct 28 2014
Externally publishedYes

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resection
Glioma
Tumors
neoplasms
Neoplasms
Brain
Survival
image analysis
brain
Imaging techniques
mathematical models
Biopsy
Medical imaging
Brain Neoplasms
Decision making
Mathematical models
biopsy
decision making
Decision Making
Theoretical Models

ASJC Scopus subject areas

  • Agricultural and Biological Sciences(all)
  • Biochemistry, Genetics and Molecular Biology(all)
  • Medicine(all)

Cite this

Patient-specific metrics of invasiveness reveal significant prognostic benefit of resection in a predictable subset of gliomas. / Baldock, Anne L.; Ahn, Sunyoung; Rockne, Russell; Johnston, Sandra; Neal, Maxwell; Corwin, David; Clark-Swanson, Kamala; Sterin, Greg; Trister, Andrew D.; Malone, Hani; Ebiana, Victoria; Sonabend, Adam M.; Mrugala, Maciej; Rockhill, Jason K.; Silbergeld, Daniel L.; Lai, Albert; Cloughesy, Timothy; McKhann, Guy M.; Bruce, Jeffrey N.; Rostomily, Robert C.; Canoll, Peter; Swanson, Kristin.

In: PLoS One, Vol. 9, No. 10, e99057, 28.10.2014.

Research output: Contribution to journalArticle

Baldock, AL, Ahn, S, Rockne, R, Johnston, S, Neal, M, Corwin, D, Clark-Swanson, K, Sterin, G, Trister, AD, Malone, H, Ebiana, V, Sonabend, AM, Mrugala, M, Rockhill, JK, Silbergeld, DL, Lai, A, Cloughesy, T, McKhann, GM, Bruce, JN, Rostomily, RC, Canoll, P & Swanson, K 2014, 'Patient-specific metrics of invasiveness reveal significant prognostic benefit of resection in a predictable subset of gliomas', PLoS One, vol. 9, no. 10, e99057. https://doi.org/10.1371/journal.pone.0099057
Baldock, Anne L. ; Ahn, Sunyoung ; Rockne, Russell ; Johnston, Sandra ; Neal, Maxwell ; Corwin, David ; Clark-Swanson, Kamala ; Sterin, Greg ; Trister, Andrew D. ; Malone, Hani ; Ebiana, Victoria ; Sonabend, Adam M. ; Mrugala, Maciej ; Rockhill, Jason K. ; Silbergeld, Daniel L. ; Lai, Albert ; Cloughesy, Timothy ; McKhann, Guy M. ; Bruce, Jeffrey N. ; Rostomily, Robert C. ; Canoll, Peter ; Swanson, Kristin. / Patient-specific metrics of invasiveness reveal significant prognostic benefit of resection in a predictable subset of gliomas. In: PLoS One. 2014 ; Vol. 9, No. 10.
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abstract = "Object: Malignant gliomas are incurable, primary brain neoplasms noted for their potential to extensively invade brain parenchyma. Current methods of clinical imaging do not elucidate the full extent of brain invasion, making it difficult to predict which, if any, patients are likely to benefit from gross total resection. Our goal was to apply a mathematical modeling approach to estimate the overall tumor invasiveness on a patient-by-patient basis and determine whether gross total resection would improve survival in patients with relatively less invasive gliomas.Methods: In 243 patients presenting with contrast-enhancing gliomas, estimates of the relative invasiveness of each patient's tumor, in terms of the ratio of net proliferation rate of the glioma cells to their net dispersal rate, were derived by applying a patient-specific mathematical model to routine pretreatment MR imaging. The effect of varying degrees of extent of resection on overall survival was assessed for cohorts of patients grouped by tumor invasiveness.Results: We demonstrate that patients with more diffuse tumors showed no survival benefit (P = 0.532) from gross total resection over subtotal/biopsy, while those with nodular (less diffuse) tumors showed a significant benefit (P = 0.00142) with a striking median survival benefit of over eight months compared to sub-totally resected tumors in the same cohort (an 80{\%} improvement in survival time for GTR only seen for nodular tumors).Conclusions: These results suggest that our patient-specific, model-based estimates of tumor invasiveness have clinical utility in surgical decision making. Quantification of relative invasiveness assessed from routinely obtained pre-operative imaging provides a practical predictor of the benefit of gross total resection.",
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AU - Baldock, Anne L.

AU - Ahn, Sunyoung

AU - Rockne, Russell

AU - Johnston, Sandra

AU - Neal, Maxwell

AU - Corwin, David

AU - Clark-Swanson, Kamala

AU - Sterin, Greg

AU - Trister, Andrew D.

AU - Malone, Hani

AU - Ebiana, Victoria

AU - Sonabend, Adam M.

AU - Mrugala, Maciej

AU - Rockhill, Jason K.

AU - Silbergeld, Daniel L.

AU - Lai, Albert

AU - Cloughesy, Timothy

AU - McKhann, Guy M.

AU - Bruce, Jeffrey N.

AU - Rostomily, Robert C.

AU - Canoll, Peter

AU - Swanson, Kristin

PY - 2014/10/28

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N2 - Object: Malignant gliomas are incurable, primary brain neoplasms noted for their potential to extensively invade brain parenchyma. Current methods of clinical imaging do not elucidate the full extent of brain invasion, making it difficult to predict which, if any, patients are likely to benefit from gross total resection. Our goal was to apply a mathematical modeling approach to estimate the overall tumor invasiveness on a patient-by-patient basis and determine whether gross total resection would improve survival in patients with relatively less invasive gliomas.Methods: In 243 patients presenting with contrast-enhancing gliomas, estimates of the relative invasiveness of each patient's tumor, in terms of the ratio of net proliferation rate of the glioma cells to their net dispersal rate, were derived by applying a patient-specific mathematical model to routine pretreatment MR imaging. The effect of varying degrees of extent of resection on overall survival was assessed for cohorts of patients grouped by tumor invasiveness.Results: We demonstrate that patients with more diffuse tumors showed no survival benefit (P = 0.532) from gross total resection over subtotal/biopsy, while those with nodular (less diffuse) tumors showed a significant benefit (P = 0.00142) with a striking median survival benefit of over eight months compared to sub-totally resected tumors in the same cohort (an 80% improvement in survival time for GTR only seen for nodular tumors).Conclusions: These results suggest that our patient-specific, model-based estimates of tumor invasiveness have clinical utility in surgical decision making. Quantification of relative invasiveness assessed from routinely obtained pre-operative imaging provides a practical predictor of the benefit of gross total resection.

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