Prediction of pseudoprogression in post-treatment glioblastoma using dynamic susceptibility contrast-derived oxygenation and microvascular transit time heterogeneity measures

Ji Eun Park; Ho Sung Kim; Nak Young Kim; Ronald Borra; Kim Mouridsen; Mikkel Bo Hansen; Young Hoon Kim; Chang Ki Hong; Jeong Hoon Kim

doi:10.1007/s00330-023-10324-9

Prediction of pseudoprogression in post-treatment glioblastoma using dynamic susceptibility contrast-derived oxygenation and microvascular transit time heterogeneity measures

Ji Eun Park, Ho Sung Kim^*, Nak Young Kim, Ronald Borra, Kim Mouridsen, Mikkel Bo Hansen, Young Hoon Kim, Chang Ki Hong, Jeong Hoon Kim

^*Corresponding author for this work

Department of Clinical Medicine - Center of Functionally Integrative Neuroscience

Research output: Contribution to journal/Conference contribution in journal/Contribution to newspaper › Journal article › Research › peer-review

Abstract

Objectives: To evaluate the added value of MR dynamic susceptibility contrast (DSC)-perfusion-weighted imaging (PWI)-derived tumour microvascular and oxygenation information with cerebral blood volume (CBV) to distinguish pseudoprogression from true progression (TP) in post-treatment glioblastoma. Methods: This retrospective single-institution study included patients with isocitrate dehydrogenase (IDH) wild-type glioblastoma and a newly developed or enlarging measurable contrast-enhancing mass within 12 weeks after concurrent chemoradiotherapy. CBV, capillary transit time heterogeneity (CTH), oxygen extraction fraction (OEF), and cerebral metabolic rate of oxygen (CMRO₂) were obtained from DSC-PWI. Predictors were selected using univariable logistic regression, and performance was measured with adjusted diagnostic odds with tumour volume and area under the curve (AUC) of receiver operating characteristics analysis. Results: A total of 103 patients were included (mean age, 59.6 years; 59 women), with 67 cases of TP and 36 cases of pseudoprogression. Pseudoprogression exhibited higher CTH (4.0 vs. 3.4, p =.019) and higher OEF (12.7 vs. 10.7, p =.014) than TP, but a similar CBV (1.48 vs. 1.53, p =.13) and CMRO₂ (7.7 vs. 7.3s, p =.598). Independent of tumour volume, both high CTH (adjusted odds ratio [OR] 1.52; 95% confidence interval [CI]: 1.11–2.09, p =.009) and high OEF (adjusted OR 1.17; 95% CI:1.03–1.33, p =.016) were predictors of pseudoprogression. The combination of CTH, OEF, and CBV yielded higher diagnostic performance (AUC 0.71) than CBV alone (AUC 0.65). Conclusion: High intratumoural capillary transit heterogeneity and high oxygen extraction fraction derived from DSC-PWI have enhanced the diagnostic value of CBV in pseudoprogression of post-treatment IDH-wild type glioblastoma. Clinical relevance statement: In the early post-treatment stage of glioblastoma, pseudoprogression exhibited both high oxygen extraction fraction and high capillary transit heterogeneity and these dynamic susceptibility contrast-perfusion weighted imaging derived parameters have added value in cerebral blood volume-based noninvasive differentiation of pseudoprogression from true progression. Key Points: • Capillary transit time heterogeneity and oxygen extraction fraction can be measured noninvasively through processing of dynamic susceptibility contrast imaging. • Pseudoprogression exhibited higher capillary transit time heterogeneity and higher oxygen extraction fraction than true progression. • A combination of cerebral blood volume, capillary transit time heterogeneity, and oxygen extraction fraction yielded the highest diagnostic performance (area under the curve 0.71).

Original language	English
Journal	European Radiology
Volume	34
Issue	5
Pages (from-to)	3061-3073
Number of pages	13
ISSN	0938-7994
DOIs	https://doi.org/10.1007/s00330-023-10324-9
Publication status	Published - May 2024

Keywords

Capillary beds
Glioblastoma
Oxygen consumption
Perfusion-weighted MRI
Radiation-induced abnormalities

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10.1007/s00330-023-10324-9

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Park, J. E., Kim, H. S., Kim, N. Y., Borra, R., Mouridsen, K., Hansen, M. B., Kim, Y. H., Hong, C. K., & Kim, J. H. (2024). Prediction of pseudoprogression in post-treatment glioblastoma using dynamic susceptibility contrast-derived oxygenation and microvascular transit time heterogeneity measures. European Radiology, 34(5), 3061-3073. https://doi.org/10.1007/s00330-023-10324-9

@article{178b8673ae6f453b84723e23cde877a7,

title = "Prediction of pseudoprogression in post-treatment glioblastoma using dynamic susceptibility contrast-derived oxygenation and microvascular transit time heterogeneity measures",

abstract = "Objectives: To evaluate the added value of MR dynamic susceptibility contrast (DSC)-perfusion-weighted imaging (PWI)-derived tumour microvascular and oxygenation information with cerebral blood volume (CBV) to distinguish pseudoprogression from true progression (TP) in post-treatment glioblastoma. Methods: This retrospective single-institution study included patients with isocitrate dehydrogenase (IDH) wild-type glioblastoma and a newly developed or enlarging measurable contrast-enhancing mass within 12 weeks after concurrent chemoradiotherapy. CBV, capillary transit time heterogeneity (CTH), oxygen extraction fraction (OEF), and cerebral metabolic rate of oxygen (CMRO2) were obtained from DSC-PWI. Predictors were selected using univariable logistic regression, and performance was measured with adjusted diagnostic odds with tumour volume and area under the curve (AUC) of receiver operating characteristics analysis. Results: A total of 103 patients were included (mean age, 59.6 years; 59 women), with 67 cases of TP and 36 cases of pseudoprogression. Pseudoprogression exhibited higher CTH (4.0 vs. 3.4, p =.019) and higher OEF (12.7 vs. 10.7, p =.014) than TP, but a similar CBV (1.48 vs. 1.53, p =.13) and CMRO2 (7.7 vs. 7.3s, p =.598). Independent of tumour volume, both high CTH (adjusted odds ratio [OR] 1.52; 95% confidence interval [CI]: 1.11–2.09, p =.009) and high OEF (adjusted OR 1.17; 95% CI:1.03–1.33, p =.016) were predictors of pseudoprogression. The combination of CTH, OEF, and CBV yielded higher diagnostic performance (AUC 0.71) than CBV alone (AUC 0.65). Conclusion: High intratumoural capillary transit heterogeneity and high oxygen extraction fraction derived from DSC-PWI have enhanced the diagnostic value of CBV in pseudoprogression of post-treatment IDH-wild type glioblastoma. Clinical relevance statement: In the early post-treatment stage of glioblastoma, pseudoprogression exhibited both high oxygen extraction fraction and high capillary transit heterogeneity and these dynamic susceptibility contrast-perfusion weighted imaging derived parameters have added value in cerebral blood volume-based noninvasive differentiation of pseudoprogression from true progression. Key Points: • Capillary transit time heterogeneity and oxygen extraction fraction can be measured noninvasively through processing of dynamic susceptibility contrast imaging. • Pseudoprogression exhibited higher capillary transit time heterogeneity and higher oxygen extraction fraction than true progression. • A combination of cerebral blood volume, capillary transit time heterogeneity, and oxygen extraction fraction yielded the highest diagnostic performance (area under the curve 0.71).",

keywords = "Capillary beds, Glioblastoma, Oxygen consumption, Perfusion-weighted MRI, Radiation-induced abnormalities",

author = "Park, {Ji Eun} and Kim, {Ho Sung} and Kim, {Nak Young} and Ronald Borra and Kim Mouridsen and Hansen, {Mikkel Bo} and Kim, {Young Hoon} and Hong, {Chang Ki} and Kim, {Jeong Hoon}",

year = "2024",

month = may,

doi = "10.1007/s00330-023-10324-9",

language = "English",

volume = "34",

pages = "3061--3073",

journal = "European Radiology",

issn = "0938-7994",

publisher = "Springer",

number = "5",

}

Prediction of pseudoprogression in post-treatment glioblastoma using dynamic susceptibility contrast-derived oxygenation and microvascular transit time heterogeneity measures. / Park, Ji Eun; Kim, Ho Sung; Kim, Nak Young et al.
In: European Radiology, Vol. 34, No. 5, 05.2024, p. 3061-3073.

Research output: Contribution to journal/Conference contribution in journal/Contribution to newspaper › Journal article › Research › peer-review

TY - JOUR

T1 - Prediction of pseudoprogression in post-treatment glioblastoma using dynamic susceptibility contrast-derived oxygenation and microvascular transit time heterogeneity measures

AU - Park, Ji Eun

AU - Kim, Ho Sung

AU - Kim, Nak Young

AU - Borra, Ronald

AU - Mouridsen, Kim

AU - Hansen, Mikkel Bo

AU - Kim, Young Hoon

AU - Hong, Chang Ki

AU - Kim, Jeong Hoon

PY - 2024/5

Y1 - 2024/5

N2 - Objectives: To evaluate the added value of MR dynamic susceptibility contrast (DSC)-perfusion-weighted imaging (PWI)-derived tumour microvascular and oxygenation information with cerebral blood volume (CBV) to distinguish pseudoprogression from true progression (TP) in post-treatment glioblastoma. Methods: This retrospective single-institution study included patients with isocitrate dehydrogenase (IDH) wild-type glioblastoma and a newly developed or enlarging measurable contrast-enhancing mass within 12 weeks after concurrent chemoradiotherapy. CBV, capillary transit time heterogeneity (CTH), oxygen extraction fraction (OEF), and cerebral metabolic rate of oxygen (CMRO2) were obtained from DSC-PWI. Predictors were selected using univariable logistic regression, and performance was measured with adjusted diagnostic odds with tumour volume and area under the curve (AUC) of receiver operating characteristics analysis. Results: A total of 103 patients were included (mean age, 59.6 years; 59 women), with 67 cases of TP and 36 cases of pseudoprogression. Pseudoprogression exhibited higher CTH (4.0 vs. 3.4, p =.019) and higher OEF (12.7 vs. 10.7, p =.014) than TP, but a similar CBV (1.48 vs. 1.53, p =.13) and CMRO2 (7.7 vs. 7.3s, p =.598). Independent of tumour volume, both high CTH (adjusted odds ratio [OR] 1.52; 95% confidence interval [CI]: 1.11–2.09, p =.009) and high OEF (adjusted OR 1.17; 95% CI:1.03–1.33, p =.016) were predictors of pseudoprogression. The combination of CTH, OEF, and CBV yielded higher diagnostic performance (AUC 0.71) than CBV alone (AUC 0.65). Conclusion: High intratumoural capillary transit heterogeneity and high oxygen extraction fraction derived from DSC-PWI have enhanced the diagnostic value of CBV in pseudoprogression of post-treatment IDH-wild type glioblastoma. Clinical relevance statement: In the early post-treatment stage of glioblastoma, pseudoprogression exhibited both high oxygen extraction fraction and high capillary transit heterogeneity and these dynamic susceptibility contrast-perfusion weighted imaging derived parameters have added value in cerebral blood volume-based noninvasive differentiation of pseudoprogression from true progression. Key Points: • Capillary transit time heterogeneity and oxygen extraction fraction can be measured noninvasively through processing of dynamic susceptibility contrast imaging. • Pseudoprogression exhibited higher capillary transit time heterogeneity and higher oxygen extraction fraction than true progression. • A combination of cerebral blood volume, capillary transit time heterogeneity, and oxygen extraction fraction yielded the highest diagnostic performance (area under the curve 0.71).

AB - Objectives: To evaluate the added value of MR dynamic susceptibility contrast (DSC)-perfusion-weighted imaging (PWI)-derived tumour microvascular and oxygenation information with cerebral blood volume (CBV) to distinguish pseudoprogression from true progression (TP) in post-treatment glioblastoma. Methods: This retrospective single-institution study included patients with isocitrate dehydrogenase (IDH) wild-type glioblastoma and a newly developed or enlarging measurable contrast-enhancing mass within 12 weeks after concurrent chemoradiotherapy. CBV, capillary transit time heterogeneity (CTH), oxygen extraction fraction (OEF), and cerebral metabolic rate of oxygen (CMRO2) were obtained from DSC-PWI. Predictors were selected using univariable logistic regression, and performance was measured with adjusted diagnostic odds with tumour volume and area under the curve (AUC) of receiver operating characteristics analysis. Results: A total of 103 patients were included (mean age, 59.6 years; 59 women), with 67 cases of TP and 36 cases of pseudoprogression. Pseudoprogression exhibited higher CTH (4.0 vs. 3.4, p =.019) and higher OEF (12.7 vs. 10.7, p =.014) than TP, but a similar CBV (1.48 vs. 1.53, p =.13) and CMRO2 (7.7 vs. 7.3s, p =.598). Independent of tumour volume, both high CTH (adjusted odds ratio [OR] 1.52; 95% confidence interval [CI]: 1.11–2.09, p =.009) and high OEF (adjusted OR 1.17; 95% CI:1.03–1.33, p =.016) were predictors of pseudoprogression. The combination of CTH, OEF, and CBV yielded higher diagnostic performance (AUC 0.71) than CBV alone (AUC 0.65). Conclusion: High intratumoural capillary transit heterogeneity and high oxygen extraction fraction derived from DSC-PWI have enhanced the diagnostic value of CBV in pseudoprogression of post-treatment IDH-wild type glioblastoma. Clinical relevance statement: In the early post-treatment stage of glioblastoma, pseudoprogression exhibited both high oxygen extraction fraction and high capillary transit heterogeneity and these dynamic susceptibility contrast-perfusion weighted imaging derived parameters have added value in cerebral blood volume-based noninvasive differentiation of pseudoprogression from true progression. Key Points: • Capillary transit time heterogeneity and oxygen extraction fraction can be measured noninvasively through processing of dynamic susceptibility contrast imaging. • Pseudoprogression exhibited higher capillary transit time heterogeneity and higher oxygen extraction fraction than true progression. • A combination of cerebral blood volume, capillary transit time heterogeneity, and oxygen extraction fraction yielded the highest diagnostic performance (area under the curve 0.71).

KW - Capillary beds

KW - Glioblastoma

KW - Oxygen consumption

KW - Perfusion-weighted MRI

KW - Radiation-induced abnormalities

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U2 - 10.1007/s00330-023-10324-9

DO - 10.1007/s00330-023-10324-9

M3 - Journal article

C2 - 37848773

AN - SCOPUS:85174291670

SN - 0938-7994

VL - 34

SP - 3061

EP - 3073

JO - European Radiology

JF - European Radiology

IS - 5

ER -

Prediction of pseudoprogression in post-treatment glioblastoma using dynamic susceptibility contrast-derived oxygenation and microvascular transit time heterogeneity measures

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