Неинвазивное измерение метаболизма кислорода, часть 2: новые методики в ПЭТ и МРТ

Метаболизм кислорода является ключевым фактором жизни живого организма. Статья является второй частью обзора методов измерения метаболизма кислорода.

Цель исследования: Дать представление о новых методиках измерения перфузии, основанных на МРТ и КТ, сравнить их точность с «золотым стандартом» - измерениями на основе ПЭТ с H₂¹⁵O, а также описать их роль в клинической практике.

Материалы и методы. Проанализировано более 200 работ из базы научных публикаций Pubmed по ключевым словам «perfusion, MRI, CT, ASL, oxygen metabolism», также изучались релевантные ссылки в данных публикациях, не содержащие указанных ключевых слов, либо содержащие их в иной формулировке.

Результаты. В рамках данного обзора была отобраны 42 публикации, описывающие КТ- и МР- перфузию с использованием контрастирующих препаратов и МР ASL перфузию. Приведены примеры использования описанных методик в фундаментальных исследованиях и прикладной медицине.

Заключение. Результаты, полученные с помощью новых неинвазивных методик молекулярной визуализации в большинстве случаев сопоставимы с данными ПЭТ с H₂¹⁵O, что позволяет шире применять МРТ и КТ исследования метаболизма кислорода в клинической практике.

1. Van Der Veldt A.A.M., Hendrikse N.H., Harms H.J. et al. Quantitative parametric perfusion images using 15O-labeled water and a clinical PET/CT scanner: Test-retest variability in lung cancer. J. Nucl. Med. 2010; 51 (11): 1684–1690. https://doi.org/10.2967/jnumed.110.079137

2. Rosen B.R., Belliveau J.W., Vevea J.M., Brady T.J. Perfusion imaging with NMR contrast agents. Magn. Reson. Med. 1990; 14 (2): 249–265. https://doi.org/10.1002/mrm.1910140211

3. Copen W.A., Lev M.H., Rapalino O. Brain Perfusion: Computed Tomography and Magnetic Resonance Techniques. Vol 135. 1st ed. Elsevier B.V.; 2016. https://doi.org/10.1016/B978-0-444-53485-9.00006-4

4. Wannamaker R., Buck B., Butcher K. Multimodal CT in Acute Stroke. Curr. Neurol. Neurosci Rep. 2019; 19 (9): 63. https://doi.org/10.1007/s11910-019-0978-z

5. Vilela P., Rowley H.A. Brain ischemia: CT and MRI techniques in acute ischemic stroke. Eur. J. Radiol. 2017; 96 (May): 162–172. https://doi.org/10.1016/j.ejrad.2017.08.014

6. Batalov A.I., Zakharova N.E., Pronin I.N. et al. 3D pCASL-perfusion in preoperative assessment of brain gliomas in large cohort of patients. Sci Rep. 2022; 12 (1): 2121. https://doi.org/10.1038/s41598-022-05992-4

7. Batalov A.I., Zakharova N.E., Chekhonin I. V. et al. Arterial Spin Labeling Perfusion in Determining the IDН1 Status and Ki-67 Index in Brain Gliomas. Diagnostics. 2022; 12 (6): 1–12. https://doi.org/10.3390/diagnostics12061444

8. Shults E.I., Pronin I.N., Batalov A.I., et al. CT-perfusion in assessment of the malignant gliomas hemodynamics. Med Vis. 2020; 24 (2): 105–118. https://doi.org/10.24835/1607-0763-2020-2-105-118 (In Russian)

9. Ibaraki M., Ohmura T., Matsubara K., Kinoshita T. Reliability of CT perfusion-derived CBF in relation to hemodynamic compromise in patients with cerebrovascular steno-occlusive disease: A comparative study with 15O PET. J. Cereb. Blood Flow. Metab. 2015; 35 (8): 1280–1288. https://doi.org/10.1038/jcbfm.2015.39

10. Lassen N., Indvar D. Brain regions involved in voluntary movements as revealed by radioisotopic mapping of CBF or CMR-glucose changes. Rev Neurol (Paris). 1990; 146 (10): 620–625.

11. Gur D., Good W.F., Wolfson S.K. et al. In vivo mapping of local cerebral blood flow by xenon-enhanced computed tomography. Science (80- ). 1982; 215 (4537): 1267–1268. https://doi.org/10.1126/science.7058347

12. Yonas H., Darby J.M., Marks E.C. et al. CBF measured by Xe-CT: Approach to analysis and normal values. J. Cereb. Blood Flow. Metab. 1991; 11 (5): 716–725. https://doi.org/10.1038/jcbfm.1991.128

13. Kety S.S., Schmidt C.F. the Nitrous Oxide Method for the Quantitative Determination of Cerebral Blood Flow in Man: Theory, Procedure and Normal Values. J. Clin. Invest. 1948; 27 (4): 476–483. https://doi.org/10.1172/JCI101994

14. Mullins M.E. Stroke Imaging with Xenon-CT. Semin. Ultrasound, CT MRI. 2006; 27 (3): 219–220. https://doi.org/10.1053/j.sult.2006.02.006

15. Yonas H., Pindzola R.R., Johnson D.W. Xenon / Computed Tomography Cerebral Blood Flow and its use in Clinical Management. Neurosurg. Clin. N. Am. 1996; 7 (4): 605–616. https://doi.org/10.1016/S1042-3680(18)30349-8

16. Svedung Wettervik T., Engquist H., Hånell A. et al. Cerebral Blood Flow and Oxygen Delivery in Aneurysmal Subarachnoid Hemorrhage: Relation to Neurointensive Care Targets. Neurocrit. Care. 2022; 37 (1): 281–292. https://doi.org/10.1007/s12028-022-01496-1

17. Williams D.S., Detre J.A., Leigh J.S., Koretsky A.P. Magnetic resonance imaging of perfusion using spin inversion of arterial water. Proc. Natl. Acad. Sci U S A. 1992; 89 (1): 212–216. https://doi.org/10.1073/pnas.89.1.212

18. Fan A.P., Jahanian H., Holdsworth S.J., Zaharchuk G. Comparison of cerebral blood flow measurement with [15 O]-water positron emission tomography and arterial spin labeling magnetic resonance imaging: A systematic review. J. Cereb. Blood Flow. Metab. 2015; 36 (5): 842–861. https://doi.org/10.1177/0271678X16636393

19. De Vis J.B., Hendrikse J., Groenendaal F. et al. Impact of neonate haematocrit variability on the longitudinal relaxation time of blood: Implications for arterial spin labelling MRI. NeuroImage Clin. 2014; 4: 517–525. https://doi.org/10.1016/j.nicl.2014.03.006

20. Steen R.G., Gronemeyer S.A., Kingsley P.B., Reddick W.E., Langston J.S., Taylor J.S. Precise and accurate measurement of proton T1 in human brain in vivo: Validation and preliminary clinical application. J. Magn. Reson. Imaging. 1994; 4 (5): 681–691. https://doi.org/10.1002/jmri.1880040511

21. Heijtel D.F.R., Mutsaerts H.J.M.M., Bakker E. et al. Accuracy and precision of pseudo-continuous arterial spin labeling perfusion during baseline and hypercapnia: A head-to-head comparison with 15O H2O positron emission tomography. Neuroimage. 2014; 92: 182–192. https://doi.org/10.1016/j.neuroimage.2014.02.011

22. Puig O., Vestergaard M.B., Lindberg U. et al. Phase contrast mapping MRI measurements of global cerebral blood flow across different perfusion states – A direct comparison with 15O-H2O positron emission tomography using a hybrid PET/MR system. J. Cereb. Blood Flow. Metab. 2019; 39 (12): 2368–2378. https://doi.org/10.1177/0271678X18798762

23. Puig O., Henriksen O.M., Vestergaard M.B. et al. Comparison of simultaneous arterial spin labeling MRI and 15O-H2O PET measurements of regional cerebral blood flow in rest and altered perfusion states. J. Cereb. Blood Flow. Metab. 2020; 40 (8): 1621–1633. https://doi.org/10.1177/0271678X19874643

24. Zhang K., Herzog H., Mauler J. et al. Comparison of cerebral blood flow acquired by simultaneous [ 15O]water positron emission tomography and arterial spin labeling magnetic resonance imaging. J. Cereb Blood. Flow. Metab. 2014; 34 (8): 1373–1380. https://doi.org/10.1038/jcbfm.2014.92

25. van Golen L.W., Kuijer J.P.A., Huisman M.C. et al. Quantification of Cerebral Blood Flow in Healthy Volunteers and Type 1 Diabetic Patients: Comparison of MRI Arterial Spin Labeling and [ 15 O ] H 2 O Positron Emission Tomography ( PET ). J. Magn. Reson. Imaging. 2014; 40: 1300–1309. https://doi.org/10.1002/jmri.24484

26. Puig O., Henriksen O.M., Andersen F.L. et al. Deep-learning-based attenuation correction in dynamic [15O]H2O studies using PET/MRI in healthy volunteers. J. Cereb. Blood Flow. Metab. 2021; 41 (12): 3314–3323. https://doi.org/10.1177/0271678X211029178

27. Fan A.P., Khalighi M.M., Guo J. et al. Identifying hypoperfusion in moyamoya disease with arterial spin labeling and an [15O]-Water positron emission tomography/magnetic resonance imaging normative database. Stroke. 2019; 50 (2): 373–380. https://doi.org/10.1161/STROKEAHA.118.023426

28. Zhao M.Y., Fan A.P., Chen D.Y.T., et al. Using arterial spin labeling to measure cerebrovascular reactivity in Moyamoya disease: Insights from simultaneous PET/MRI. J. Cereb. Blood Flow. Metab. 2022; 42 (8): 1493–1506. https://doi.org/10.1177/0271678X221083471

29. Itagaki H., Kokubo Y., Kawanami K. et al. Arterial spin labeling magnetic resonance imaging at short post-labeling delay reflects cerebral perfusion pressure verified by oxygen-15-positron emission tomography in cerebrovascular steno-occlusive disease. Acta Radiol. 2021; 62 (2): 225–233. https://doi.org/10.1177/0284185120917111

30. Besheli L.D., Ahmed A., Hamam O. et al. Arterial Spin Labeling technique and clinical applications of the intracranial compartment in stroke and stroke mimics – A case-based review. Neuroradiology. 2022; 35 (4): 437–453. https://doi.org/10.1177/19714009221098806

31. Soldozy S., Galindo J., Snyder H. et al. Clinical utility of arterial spin labeling imaging in disorders of the nervous system. Neurosurg. Focus. 2019; 47 (6): E5. https://doi.org/10.3171/2019.9.FOCUS19567

32. Dolui S., Fan A.P., Zhao M.Y. et al. Reliability of arterial spin labeling derived cerebral blood flow in periventricular white matter. Neuroimage: Reports. 2021; 1 (4): 100063. https://doi.org/10.1016/j.ynirp.2021.100063

33. Ssali T., Anazodo U.C., Thiessen J.D. et al. A noninvasive method for quantifying cerebral blood flow by hybrid PET/MRI. J. Nucl. Med. 2018; 59 (8): 1329–1334. https://doi.org/10.2967/jnumed.117.203414

34. Narciso L., Ssali T., Iida H., St Lawrence K. A non-invasive reference-based method for imaging the cerebral metabolic rate of oxygen by PET/MR: Theory and error analysis. Phys. Med. Biol. 2021; 66 (6). https://doi.org/10.1088/1361-6560/abe737

35. Siripongsatian D., Kunawudhi A., Promteangtrong C. et al. Alterations in 18F-FDG PET/MRI and 15O-Water PET Brain Findings in Patients with Neurological Symptoms after COVID-19 Vaccination: A Pilot Study. Clin. Nucl. Med. 2022; 47 (3): E230–E239. https://doi.org/10.1097/RLU.0000000000004041

36. Khalighi M.M., Deller T.W., Fan A.P., et al. Image-derived input function estimation on a TOF-enabled PET/MR for cerebral blood flow mapping. J. Cereb. Blood Flow. Metab. 2018; 38 (1): 126–135. https://doi.org/10.1177/0271678X17691784

37. Zhang B.L., Liu J., Lei Y. et al. An Epigenetic Mechanism of High Gdnf Transcription in Glioma Cells Revealed by Specific Sequence Methylation. Mol Neurobiol. 2015; 53 (7): 4352–4362. https://doi.org/10.1007/s12035-015-9365-1

38. Lan X., Younis M.H., Li K., Cai W. First clinical experience of 106 cm , long axial field-of-view ( LAFOV ) PET / CT: an elegant balance between standard axial (23 cm ) and total-body (194 cm ) systems. Eur. J. Nucl. Med. Mol. Imaging. 2021; 48: 3755–3759. https://doi.org/10.1007/s00259-021-05505-x

39. Gupta A., Chazen J.L., Hartman M. et al. Cerebrovascular Reserve and Stroke Risk in Patients With Carotid Stenosis or Occlusion A Systematic Review and Meta-Analysis. Stroke. 2012; 43: 2884–2891. https://doi.org/10.1161/STROKEAHA.112.663716

40. Ishii K., Kitagaki H., Kono M., Mon E. Decreased Medial Temporal Oxygen Metabolism in Alzheimer ’ s Disease Shown by PET. J. Nucl. Med. 1996; 37: 1159–1165.

41. Cho J., Lee J., An H. et al. Cerebral oxygen extraction fraction (OEF): Comparison of challenge-free gradient echo QSM+qBOLD (QQ) with 15O PET in healthy adults. J. Cereb. Blood Flow. Metab. 2021; 41 (7): 1658–1668. https://doi.org/10.1177/0271678X20973951

42. Jiang D., Deng S., Franklin C.G. et al. Validation of T2-based oxygen extraction fraction measurement with 15O positron emission tomography. Magn. Reson. Med. 2021; 85 (1): 290–297. https://doi.org/10.1002/mrm.28410

43. Ogawa S., Lee T.M., Kay A.R., Tank D.W. Brain magnetic resonance imaging with contrast dependent on blood oxygenation. Proc. Natl. Acad. Sci. 1990; 87: 9868–9872. https://doi.org/10.1073/pnas.87.24.9868

44. He X., Zhu M., Yablonskiy D.A. Validation of Oxygen Extraction Fraction Measurement by qBOLD Technique. Magn. Reson. Med. 2008; 60: 882–888. https://doi.org/10.1002/mrm.21719

45. Lu H., Xu F., Grgac K. et al. Calibration and Validation of TRUST MRI for the Estimation of Cerebral Blood Oxygenation. Magn Reson Med. 2012; 67: 42–49. https://doi.org/10.1002/mrm.22970

46. Wehrli F.W., Rodgers Z., Jain V. et al. Time-Resolved MRI Oximetry for Quantifying CMRO 2 and Vascular Reactivity. Acad Radiol. 2014; 21 (2): 207–214. https://doi.org/10.1016/j.acra.2013.11.001

47. Jain V., Langham M.C., Wehrli F.W. MRI estimation of global brain oxygen consumption rate. J Cereb Blood Flow Metab. 2010; 30 (9): 1598–1607. https://doi.org/10.1038/jcbfm.2010.49

48. Li W., Xu F., Zhu D., Zijl P.C.M. Van. T2 -oximetry – based cerebral venous oxygenation mapping using Fourier-transform – based velocity-selective pulse trains. Magn Reson Med. 2022; 88 (3): 1292–1302. https://doi.org/10.1002/mrm.29300

49. Ponto L.L.B., Moser D.J., Menda Y. et al. Early Phase PIB-PET as a Surrogate for Global and Regional Cerebral Blood Flow Measures. J. Neuroimaging. 2019; 29 (1): 85–96. https://doi.org/10.1111/jon.12582