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01.04.2011 | Magnetic Resonance

Analysing the response in R2* relaxation rate of intracranial tumours to hyperoxic and hypercapnic respiratory challenges: initial results

verfasst von: A. Müller, S. Remmele, I. Wenningmann, H. Clusmann, F. Träber, S. Flacke, R. König, J. Gieseke, W. A. Willinek, H. H. Schild, P. Mürtz

Erschienen in: European Radiology | Ausgabe 4/2011

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Abstract

Objective

To investigate the response in R2* relaxation rate of human intracranial tumours during hyperoxic and hypercapnic respiratory challenges.

Methods

In seven patients with different intracranial tumours, cerebral R2* changes during carbogen and CO₂/air inhalation were monitored at 3 T using a dynamic multigradient-echo sequence of high temporal and spatial resolution. The R2* time series of each voxel was tested for significant change. Regions of interest were analysed with respect to response amplitude and velocity.

Results

The tumours showed heterogeneous R2* responses with large interindividual variability. In the ‘contrast-enhancing’ area of five patients and in the ‘non-tumoral’ tissue most voxels showed a decrease in R2* for carbogen. For the ‘contrast-enhancing’ area of two patients hardly any responses were found. In areas of ‘necrosis’ and perifocal ‘oedema’ typically voxels with R2* increase and no response were found for both gases. For tissue responding to CO₂/air, the R2* changes were of the same order of magnitude as those for carbogen. The response kinetic was generally attenuated in tumoral tissue.

Conclusion

The spatially resolved determination of R2* changes reveals the individual heterogeneous response characteristic of intracranial human tumours during hyperoxic and hypercapnic respiratory challenges.

Yen PS, Teo BT, Chiu CH, Chen SC, Chiu TL, Su CF (2009) White Matter tract involvement in brain tumors: a diffusion tensor imaging analysis. Surg Neurol 72:464–469PubMedCrossRef

Lu S, Ahn D, Johnson G, Law M, Zagzag D, Grossman RI (2004) Diffusion-tensor MR imaging of intracranial neoplasia and associated peritumoral edema: introduction of the tumor infiltration index. Radiology 232:221–228PubMedCrossRef

Ludemann L, Warmuth C, Plotkin M, Forschler A, Gutberlet M, Wust P, Amthauer H (2009) Brain tumor perfusion: comparison of dynamic contrast enhanced magnetic resonance imaging using T1, T2, and T2* contrast, pulsed arterial spin labeling, and H2(15)O positron emission tomography. Eur J Radiol 70:465–474PubMedCrossRef

Zaharchuk G (2007) Theoretical basis of hemodynamic MR imaging techniques to measure cerebral blood volume, cerebral blood flow, and permeability. AJNR Am J Neuroradiol 28:1850–1858PubMedCrossRef

Gerstner ER, Sorensen AG, Jain RK, Batchelor TT (2008) Advances in neuroimaging techniques for the evaluation of tumor growth, vascular permeability, and angiogenesis in gliomas. Curr Opin Neurol 21:728–735PubMedCrossRef

Swanson KR, Chakraborty G, Wang CH, Rockne R, Harpold HL, Muzi M, Adamsen TC, Krohn KA, Spence AM (2009) Complementary but distinct roles for MRI and 18F-fluoromisonidazole PET in the assessment of human glioblastomas. J Nucl Med 50:36–44PubMedCrossRef

Nehmeh SA, Lee NY, Schroder H, Squire O, Zanzonico PB, Erdi YE, Greco C, Mageras G, Pham HS, Larson SM, Ling CC, Humm JL (2008) Reproducibility of intratumor distribution of (18)F-fluoromisonidazole in head and neck cancer. Int J Radiat Oncol Biol Phys 70:235–242PubMedCrossRef

Barrett T, Brechbiel M, Bernardo M, Choyke PL (2007) MRI of tumor angiogenesis. J Magn Reson Imaging 26:235–249PubMedCrossRef

Padhani AR, Krohn KA, Lewis JS, Alber M (2007) Imaging oxygenation of human tumours. Eur Radiol 17:861–872PubMedCrossRef

10.

Baudelet C, Gallez B (2005) Current issues in the utility of blood oxygen level dependent MRI for the assessment of modulations in tumor oxygenation. Curr Med Imaging Rev 1:229–243CrossRef

11.

Neeman M, Dafni H (2003) Structural, functional, and molecular MR imaging of the microvasculature. Annu Rev Biomed Eng 5:29–56PubMedCrossRef

12.

Yetkin FZ, Mendelsohn D (2002) Hypoxia imaging in brain tumors. Neuroimaging Clin N Am 12:537–552PubMedCrossRef

13.

Ogawa S, Lee TM, Kay AR, Tank DW (1990) Brain magnetic resonance imaging with contrast dependent on blood oxygenation. Proc Natl Acad Sci U S A 87:9868–9872PubMedCrossRef

14.

Punwani S, Ordidge RJ, Cooper CE, Amess P, Clemence M (1998) MRI measurements of cerebral deoxyhaemoglobin concentration [dHb]–correlation with near infrared spectroscopy (NIRS). NMR Biomed 11:281–289PubMedCrossRef

15.

Mürtz P, Flacke S, Müller A, Soehle M, Wenningmann I, Kovacs A, Träber F, Willinek WA, Gieseke J, Schild HH, Remmele S (2010) Changes in the MR relaxation rate R2* induced by respiratory challenges at 3.0 T: a comparison of two quantification methods. NMR Biomed doi:10.1002/nbm.1532

16.

Ashkanian M, Borghammer P, Gjedde A, Ïstergaard L, Vafaee M (2008) Improvement of brain tissue oxygenation by inhalation of carbogen. Neuroscience 156:932–938PubMedCrossRef

17.

Baudelet C, Gallez B (2002) How does blood oxygen level-dependent (BOLD) contrast correlate with oxygen partial pressure (pO2) inside tumors? Magn Reson Med 48:980–986PubMedCrossRef

18.

Howe FA, Robinson SP, McIntyre DJ, Stubbs M, Griffiths JR (2001) Issues in flow and oxygenation dependent contrast (FLOOD) imaging of tumours. NMR Biomed 14:497–506PubMedCrossRef

19.

Heyn C, Poublanc J, Crawley A, Mandell D, Han JS, Tymianski M, Terbrugge K, Fisher JA, Mikulis DJ (2010) Quantification of Cerebrovascular Reactivity by Blood Oxygen Level-Dependent MR Imaging and Correlation with Conventional Angiography in Patients with Moyamoya Disease. AJNR Am J Neuroradiol 31:862–867PubMedCrossRef

20.

Goode SD, Krishan S, Alexakis C, Mahajan R, Auer DP (2009) Precision of cerebrovascular reactivity assessment with use of different quantification methods for hypercapnia functional MR imaging. AJNR Am J Neuroradiol 30:972–977PubMedCrossRef

21.

Yezhuvath US, Lewis-Amezcua K, Varghese R, Xiao G, Lu H (2009) On the assessment of cerebrovascular reactivity using hypercapnia BOLD MRI. NMR Biomed 22:779–786PubMedCrossRef

22.

Ziyeh S, Rick J, Reinhard M, Hetzel A, Mader I, Speck O (2005) Blood oxygen level-dependent MRI of cerebral CO2 reactivity in severe carotid stenosis and occlusion. Stroke 36:751–756PubMedCrossRef

23.

van der Zande FH, Hofman PA, Backes WH (2005) Mapping hypercapnia-induced cerebrovascular reactivity using BOLD MRI. Neuroradiology 47:114–120PubMedCrossRef

24.

Kastrup A, Kruger G, Neumann-Haefelin T, Moseley ME (2001) Assessment of cerebrovascular reactivity with functional magnetic resonance imaging: comparison of CO(2) and breath holding. Magn Reson Imaging 19:13–20PubMedCrossRef

25.

Vesely A, Sasano H, Volgyesi G, Somogyi R, Tesler J, Fedorko L, Grynspan J, Crawley A, Fisher JA, Mikulis D (2001) MRI mapping of cerebrovascular reactivity using square wave changes in end-tidal PCO2. Magn Reson Med 45:1011–1013PubMedCrossRef

26.

Rostrup E, Law I, Blinkenberg M, Larsson HB, Born AP, Holm S, Paulson OB (2000) Regional differences in the CBF and BOLD responses to hypercapnia: a combined PET and fMRI study. NeuroImage 11:87–97PubMedCrossRef

27.

Baudelet C, Cron GO, Gallez B (2006) Determination of the maturity and functionality of tumor vasculature by MRI: correlation between BOLD-MRI and DCE-MRI using P792 in experimental fibrosarcoma tumors. Magn Reson Med 56:1041–1049PubMedCrossRef

28.

Neeman M, Dafni H, Bukhari O, Braun RD, Dewhirst MW (2001) In vivo BOLD contrast MRI mapping of subcutaneous vascular function and maturation: validation by intravital microscopy. Magn Reson Med 45:887–898PubMedCrossRef

29.

Gilad AA, Israely T, Dafni H, Meir G, Cohen B, Neeman M (2005) Functional and molecular mapping of uncoupling between vascular permeability and loss of vascular maturation in ovarian carcinoma xenografts: the role of stroma cells in tumor angiogenesis. Int J Cancer 117:202–211PubMedCrossRef

30.

Baudelet C, Ansiaux R, Jordan BF, Havaux X, Macq B, Gallez B (2004) Physiological noise in murine solid tumours using T2*-weighted gradient-echo imaging: a marker of tumour acute hypoxia? Phys Med Biol 49:3389–3411PubMedCrossRef

31.

Rodrigues LM, Howe FA, Griffiths JR, Robinson SP (2004) Tumor R2* is a prognostic indicator of acute radiotherapeutic response in rodent tumors. J Magn Reson Imaging 19:482–488PubMedCrossRef

32.

Landuyt W, Hermans R, Bosmans H, Sunaert S, Beatse E, Farina D, Meijerink M, Zhang H, Van Den BW, Lambin P, Marchal G (2001) BOLD contrast fMRI of whole rodent tumour during air or carbogen breathing using echo-planar imaging at 1.5 T. Eur Radiol 11:2332–2340PubMedCrossRef

33.

Abramovitch R, Dafni H, Smouha E, Benjamin LE, Neeman M (1999) In vivo prediction of vascular susceptibility to vascular susceptibility endothelial growth factor withdrawal: magnetic resonance imaging of C6 rat glioma in nude mice. Cancer Res 59:5012–5016PubMed

34.

Robinson SP, Collingridge DR, Howe FA, Rodrigues LM, Chaplin DJ, Griffiths JR (1999) Tumour response to hypercapnia and hyperoxia monitored by FLOOD magnetic resonance imaging. NMR Biomed 12:98–106PubMedCrossRef

35.

Kuperman VY, River JN, Lewis MZ, Lubich LM, Karczmar GS (1995) Changes in T2*-weighted images during hyperoxia differentiate tumors from normal tissue. Magn Reson Med 33:318–325PubMedCrossRef

36.

Sedlacik J, Kutschbach C, Rauscher A, Deistung A, Reichenbach JR (2008) Investigation of the influence of carbon dioxide concentrations on cerebral physiology by susceptibility-weighted magnetic resonance imaging (SWI). NeuroImage 43:36–43PubMedCrossRef

37.

Rauscher A, Sedlacik J, Fitzek C, Walter B, Hochstetter A, Kalff R, Kaiser WA, Reichenbach JR (2005) High resolution susceptibility weighted MR-imaging of brain tumors during the application of a gaseous agent. Röfo 177:1065–1069PubMed

38.

Losert C (2004) Sauerstoff-induzierte Signaländerungen in der MRT von Hirntumoren. Dissertation. University of Munich, Germany

39.

Rijpkema M, Schuuring J, Bernsen PL, Bernsen HJ, Kaanders JH, van der Kogel AJ, Heerschap A (2004) BOLD MRI response to hypercapnic hyperoxia in patients with meningiomas: correlation with Gadolinium-DTPA uptake rate. Magn Reson Imaging 22:761–767PubMedCrossRef

40.

Rijpkema M, Kaanders JH, Joosten FB, van der Kogel AJ, Heerschap A (2002) Effects of breathing a hyperoxic hypercapnic gas mixture on blood oxygenation and vascularity of head-and-neck tumors as measured by magnetic resonance imaging. Int J Radiat Oncol Biol Phys 53:1185–1191PubMedCrossRef

41.

Taylor NJ, Baddeley H, Goodchild KA, Powell ME, Thoumine M, Culver LA, Stirling JJ, Saunders MI, Hoskin PJ, Phillips H, Padhani AR, Griffiths JR (2001) BOLD MRI of human tumor oxygenation during carbogen breathing. J Magn Reson Imaging 14:156–163PubMedCrossRef

42.

Griffiths JR, Taylor NJ, Howe FA, Saunders MI, Robinson SP, Hoskin PJ, Powell ME, Thoumine M, Caine LA, Baddeley H (1997) The response of human tumors to carbogen breathing, monitored by Gradient-Recalled Echo Magnetic Resonance Imaging. Int J Radiat Oncol Biol Phys 39:697–701PubMedCrossRef

43.

Remmele S, Dahnke H, Flacke S, Soehle M, Wenningmann I, Kovacs A, Traber F, Muller A, Willinek WA, Konig R, Clusmann H, Gieseke J, Schild HH, Murtz P (2010) Quantification of the magnetic resonance signal response to dynamic (C)O(2)-enhanced imaging in the brain at 3 T: R*(2) BOLD vs. balanced SSFP. J Magn Reson Imaging 31:1300–1310PubMedCrossRef

44.

Peebles K, Celi L, McGrattan K, Murrell C, Thomas K, Ainslie PN (2007) Human cerebrovascular and ventilatory CO2 reactivity to end-tidal, arterial and internal jugular vein PCO2. J Physiol 584:347–357PubMedCrossRef

45.

Hsu YY, Chang CN, Jung SM, Lim KE, Huang JC, Fang SY, Liu HL (2004) Blood oxygenation level-dependent MRI of cerebral gliomas during breath holding. J Magn Reson Imaging 19:160–167PubMedCrossRef

46.

Packard SD, Mandeville JB, Ichikawa T, Ikeda K, Terada K, Niloff S, Chiocca EA, Rosen BR, Marota JJ (2003) Functional response of tumor vasculature to PaCO2: determination of total and microvascular blood volume by MRI. Neoplasia 5:330–338PubMed

47.

Robinson SP, Rijken PF, Howe FA, McSheehy PM, van der Sanden BP, Heerschap A, Stubbs M, van der Kogel AJ, Griffiths JR (2003) Tumor vascular architecture and function evaluated by non-invasive susceptibility MRI methods and immunohistochemistry. J Magn Reson Imaging 17:445–454PubMedCrossRef

48.

O'Connor JP, Naish JH, Parker GJ, Waterton JC, Watson Y, Jayson GC, Buonaccorsi GA, Cheung S, Buckley DL, McGrath DM, West CM, Davidson SE, Roberts C, Mills SJ, Mitchell CL, Hope L, Ton NC, Jackson A (2009) Preliminary study of oxygen-enhanced longitudinal relaxation in MRI: a potential novel biomarker of oxygenation changes in solid tumors. Int J Radiat Oncol Biol Phys 75:1209–1215PubMedCrossRef

49.

Kaanders JH, Bussink J, van der Kogel AJ (2002) ARCON: a novel biology-based approach in radiotherapy. Lancet Oncol 3:728–737PubMedCrossRef

50.

Ertl-Wagner BB, Blume JD, Peck D, Udupa JK, Herman B, Levering A, Schmalfuss IM (2009) Reliability of tumor volume estimation from MR images in patients with malignant glioma. Results from the American College of Radiology Imaging Network (ACRIN) 6662 Trial. Eur Radiol 19:599–609PubMedCrossRef

51.

Schaller C, Schramm J, Haun D, Meyer B (2003) Patterns of cortical oxygen saturation changes during CO2 reactivity testing in the vicinity of cerebral arteriovenous malformations. Stroke 34:938–944PubMedCrossRef

Titel: Analysing the response in R2* relaxation rate of intracranial tumours to hyperoxic and hypercapnic respiratory challenges: initial results
verfasst von: A. Müller
S. Remmele
I. Wenningmann
H. Clusmann
F. Träber
S. Flacke
R. König
J. Gieseke
W. A. Willinek
H. H. Schild
P. Mürtz
Publikationsdatum: 01.04.2011
Verlag: Springer-Verlag
Erschienen in: European Radiology / Ausgabe 4/2011
Print ISSN: 0938-7994
Elektronische ISSN: 1432-1084
DOI: https://doi.org/10.1007/s00330-010-1948-7

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Analysing the response in R2* relaxation rate of intracranial tumours to hyperoxic and hypercapnic respiratory challenges: initial results