Top

Published in:

01-01-2017 | Functional Neuroradiology

Perfusion imaging of brain gliomas using arterial spin labeling: correlation with histopathological vascular density in MRI-guided biopsies

Authors: Di Ningning, Pang Haopeng, Dang Xuefei, Cheng Wenna, Ren Yan, Wu Jingsong, Yao Chengjun, Yao Zhenwei, Feng Xiaoyuan

Published in: Neuroradiology | Issue 1/2017

Abstract

Introduction

This study was designed to determine if cerebral blood flow (CBF) derived from arterial spin labeling (ASL) perfusion imaging could be used to quantitatively evaluate the microvascular density (MVD) of brain gliomas on a “point-to-point” basis by matching CBF areas and surgical biopsy sites as accurate as possible.

Methods

The study enrolled 47 patients with treatment-naive brain gliomas who underwent preoperative ASL, 3D T1-weighted imaging with gadolinium contrast enhancement (3D T1C+), and T2 fluid acquisition of inversion recovery (T2FLAIR) sequences before stereotactic surgery. We histologically quantified MVD from CD34-stained sections of stereotactic biopsies and co-registered biopsy locations with localized CBF measurements. The correlation between CBF and MVD was determined using Spearman’s correlation coefficient. P ≤ .05 was considered statistically significant.

Results

Of the 47 patients enrolled in the study, 6 were excluded from the analysis because of brain shift or poor co-registration and localization of the biopsy site during surgery. Finally, 84 biopsies from 41 subjects were included in the analysis. CBF showed a statistically significant positive correlation with MVD (ρ = 0.567; P = .029).

Conclusion

ASL can be a useful noninvasive perfusion MR method for quantitative evaluation of the MVD of brain gliomas.

Provenzale JM, Mukundan S, Barboriak DP (2006) Diffusion weighted and perfusion MR imaging for brain tumor characterization and assessment of treatment response. Radiology 239:632–649CrossRefPubMed

Detre JA, Rao H, Wang DJ, Chen YF, Wang Z (2012) Applications of arterial spin labeled MRI in the brain. J Magn Reson Imaging 35:1026–1037CrossRefPubMedPubMedCentral

Kuo PH, Kanal E, Abu-Alfa AK, Cowper SE (2007) Gadolinium-based MR contrast agents and nephrogenic systemic fibrosis. Radiology 242:647–649CrossRefPubMed

Warmuth C, Gunther M, Zimmer C (2003) Quantification of blood flow in brain tumors: comparison of arterial spin labeling and dynamic susceptibility-weighted contrast-enhanced MR imaging. Radiology 228:523–532CrossRefPubMed

Hirai T, Kitajima M, Nakamura H et al (2011) Quantitative blood flow measurements in gliomas using arterial spin-labeling at 3T: intermodality agreement and inter- and intraobserver reproducibility study. AJNR Am J Neuroradiol 32:2073–2079CrossRefPubMed

Nael K, Meshksar A, Liebeskind DS, Coull BM, Krupinski EA, Villablanca JP (2013) Quantitative analysis of hypoperfusion in acute stroke: arterial spin labeling versus dynamic susceptibility contrast. Stroke 44:3090–3096CrossRefPubMedPubMedCentral

Chen J, Zhao B, Bu C, Xie G (2014) Relationship between the hemodynamic changes on multi-Td pulsed arterial spin labeling images and the degrees of cerebral artery stenosis. Magn Reson Imaging 32:1277–1283CrossRefPubMed

Mak HK, Qian W, Ng KS et al (2014) Combination of MRI hippocampal volumetry and arterial spin labeling MR perfusion at 3-Tesla improves the efficacy in discriminating Alzheimer’s disease from cognitively normal elderly adults. J Alzheimers Dis 41:749–758PubMed

Dangouloff-Ros V, Deroulers C, Foissac F et al (2016) Arterial spin labeling to predict brain tumor grading in children: correlations between histopathologic vascular density and perfusion MR imaging. Radiology 281:1–14CrossRef

10.

Noguchi T, Yoshiura T, Hiwatashi A et al (2008) Perfusion imaging of brain tumors using arterial spin-labeling: correlation with histopathologic vascular density. AJNR Am J Neuroradiol 29:688–693CrossRefPubMed

11.

Kimura H, Takeuchi H, Koshimoto Y et al (2006) Perfusion imaging of meningioma by using continuous arterial spin-labeling: comparison with dynamic susceptibility-weighted contrast-enhanced MR images and histopathologic features. AJNR Am J Neuroradiol 27:85–93PubMed

12.

Yamamoto T, Takeuchi H, Kinoshita K, Kosaka N, Kimura H (2014) Assessment of tumor blood flow and its correlation with histopathologic features in skull base meningiomas and schwannomas by using pseudo-continuous arterial spin labeling images. Eur J Radiol 83:817–823CrossRefPubMed

13.

Gerlinger M, Rowan AJ, Horswell S et al (2012) Intratumor heterogeneity and branched evolution revealed by multiregion sequencing. N Engl J Med 366:883–892CrossRefPubMedPubMedCentral

14.

Goh V, Halligan S, Daley F, Wellsted DM, Guenther T, Bartram CI (2008) Colorectal tumor vascularity: quantitative assessment with multidetector CT—do tumor perfusion measurements reflect angiogenesis? Radiology 249:510–517CrossRefPubMed

15.

Dighe S, Blake H, Jeyadevan N et al (2013) Perfusion CT vascular parameters do not correlate with immunohistochemically derived microvessel density count in colorectal tumors. Radiology 268:400–410CrossRefPubMed

16.

Weidner N (1995) Current pathologic methods for measuring intratumoral microvessel density within breast carcinoma and other solid tumors. Breast Cancer Res Treat 36:169–180CrossRefPubMed

17.

Louis DN, Perry A, Reifenberger G et al (2016) The 2016 World Health Organization Classification of Tumors of the Central Nervous System: a summary. Acta Neuropathol 6:803–820CrossRef

18.

Ostrom QT, Bauchet L, Davis FG et al (2014) The epidemiology of glioma in adults: a “state of the science” review. Neuro-Oncology 16:896–913CrossRefPubMedPubMedCentral

19.

Folkman J (1989) What is evidence that tumors are angiogenesis dependent? J Natl Cancer Inst 82:4–6CrossRef

20.

Sorensen AG, Emblem KE, Polaskova P et al (2012) Increased survival of glioblastoma patients who respond to antiangiogenic therapy with elevated blood perfusion. Cancer Res 72:402–407CrossRefPubMed

21.

Tolaney SM, Boucher Y, Duda DG et al (2015) Role of vascular density and normalization in response to neoadjuvant bevacizumab and chemotherapy in breast cancer patients. Proc Natl Acad Sci U S A 112:14325–14330CrossRefPubMedPubMedCentral

22.

Knopp EA, Cha S, Johnson G et al (1999) Glial neoplasms: dynamic contrast-enhanced T2*-weighted MR imaging. Radiology 211:791–798CrossRefPubMed

23.

Hu LS, Eschbacher JM, Dueck AC et al (2012) Correlations between perfusion MR imaging cerebral blood volume, microvessel quantification, and clinical outcome using stereotactic analysis in recurrent high-grade glioma. AJNR Am J Neuroradiol 33:69–76CrossRefPubMed

24.

Ellingson B, Zaw T, Cloughesy TF et al (2012) Comparison between intensity normalization techniques for dynamic susceptibility contrast (DSC)-MRI estimates of cerebral blood volume (CBV) in human gliomas. J Magn Reson Imaging 25:1472–1477CrossRef

25.

Boxerman JL, Schmainda KM, Weisskoff RM (2006) Relative cerebral blood volume maps corrected for contrast agent extravasation significantly correlate with glioma tumor grade, whereas uncorrected maps do not. AJNR Am J Neuroradiol 27:859–867PubMed

26.

Boxerman JL, Prah DE, Paulson ES, Machan JT, Bedekar D, Schmainda KM (2012) The role of preload and leakage correction in gadolinium-based cerebral blood volume estimation determined by comparison with MION as a criterion standard. AJNR Am J Neuroradiol 33:1081–1087CrossRefPubMedPubMedCentral

27.

Chen Y, Wang DJ, Detre JA (2011) Test-retest reliability of arterial spin labeling with common labeling strategies. J Magn Reson Imaging 33:940–949CrossRefPubMedPubMedCentral

28.

Golay X, Hendrikse J, Lim TC (2004) Perfusions imaging using arterial spin labeling. Top Magn Reson Imaging 15:10–27CrossRefPubMed

29.

Teeuwisse WM, Schmid S, Ghariq E, Veer IM, van Osch MJ (2014) Time-encoded pseudocontinuous arterial spin labeling: basic properties and timing strategies for human applications. Magn Reson Med 72:1712–1722CrossRefPubMed

30.

Weber MA, Zoubaa S, Schlieter M et al (2006) Diagnostic performance of spectroscopic and perfusion MRI for distinction of brain tumors. Neurology 66:1899–1906CrossRefPubMed

31.

Guo P, Imanishi Y, Cackowski FC et al (2005) Up-regulation of angiopoietin-2, matrix metalloprotease-2, membrane type 1 metalloprotease, and laminin 5 gamma 2 correlates with the invasiveness of human glioma. Am J Pathol 166:877–890CrossRefPubMedPubMedCentral

32.

Sadeghi N, Salmon I, Decaestecker C et al (2015) Stereotactic comparison among cerebral blood volume, methionine uptake, and histopathology in brain glioma. AJNR Am J Neuroradiol 28:455–461

33.

Jain R, Gutierrez J, Narang J et al (2011) In vivo correlation of tumor blood volume and permeability with histologic and molecular angiogenic markers in gliomas. AJNR Am J Neuroradiol 32:388–394CrossRefPubMed

34.

Price SJ, Green HA, Dean AF et al (2011) Correlation of MR relative cerebral blood volume measurements with cellular density and proliferation in high-grade gliomas: an image-guided biopsy study. AJNR Am J Neuroradiol 32:501–506CrossRefPubMed

35.

Christoforidis GA, Yang M, Abduljalil A et al (2012) “Tumoral pseudoblush” identified within gliomas at high-spatial-resolution ultrahigh-field-strength gradient-echo MR imaging corresponds to microvascularity at stereotactic biopsy. Radiology 264:210–217CrossRefPubMedPubMedCentral

36.

Zhang Y, Kapur P, Yuan Q et al (2016) Tumor vascularity in renal masses: correlation of arterial spin-labeled and dynamic contrast-enhanced magnetic resonance imaging assessments. Clin Genitourin Cancer 14:e25–e36CrossRefPubMed

37.

Schor-Bardach R, Alsop DC, Pedrosa I et al (2009) Does arterial spin-labeling MR imaging-measured tumor perfusion correlate with renal cell cancer response to antiangiogenic therapy in a mouse model? Radiology 251:731–742CrossRefPubMedPubMedCentral

38.

Alexiou GA, Zikou A, Tsiouris S et al (2014) Correlation of diffusion tensor dynamic susceptibility contrast MRI and (99m)Tc-tetrofosmin brain SPECT with tumour grade and Ki-67 immunohistochemistry in glioma. Clin Neurol Neurosurg 116:41–45CrossRefPubMed

Title: Perfusion imaging of brain gliomas using arterial spin labeling: correlation with histopathological vascular density in MRI-guided biopsies
Authors: Di Ningning
Pang Haopeng
Dang Xuefei
Cheng Wenna
Ren Yan
Wu Jingsong
Yao Chengjun
Yao Zhenwei
Feng Xiaoyuan
Publication date: 01-01-2017
Publisher: Springer Berlin Heidelberg
Published in: Neuroradiology / Issue 1/2017
Print ISSN: 0028-3940
Electronic ISSN: 1432-1920
DOI: https://doi.org/10.1007/s00234-016-1756-0

Keynote webinar | Spotlight on medication adherence

Springer Medicine

Perfusion imaging of brain gliomas using arterial spin labeling: correlation with histopathological vascular density in MRI-guided biopsies

Abstract

Introduction

Methods

Results

Conclusion

Keynote webinar | Spotlight on medication adherence

Springer Medicine

Abstract

Introduction

Methods

Results

Conclusion

Please log in to get access to this content

Other articles of this Issue 1/2017

Changes of brain metabolite concentrations during maturation in different brain regions measured by chemical shift imaging

Clinical validation of synthetic brain MRI in children: initial experience

Exercise training effects on memory and hippocampal viscoelasticity in multiple sclerosis: a novel application of magnetic resonance elastography

Cerebral blood flow, transit time, and apparent diffusion coefficient in moyamoya disease before and after acetazolamide

Severe cerebral hypovolemia on perfusion CT and lower body weight are associated with parenchymal haemorrhage after thrombolysis

A contemporary framework of language processing in the human brain in the context of preoperative and intraoperative language mapping