Medical Radiology and Radiation Safety. 2016. Vol. 61. No. 4. P. 68-75

REVIEW

I.A. Znamenskiy1,2, A.K. Kondakov1,2, V.V. Mil’kin1, D.Ju. Mosin1, A.V. Grechko1

Positron Emission Tomography with Oxygen-15 in Neurological Practice. Part 2. Clinical Application

1. Hospital for incurable patients -Scientific and Medical Rehabilitation Center, Moscow, Russia, e-mail: This email address is being protected from spambots. You need JavaScript enabled to view it. ; 2. N.I. Pirogov Russian National Research Medical University, Moscow, Russia.

ABSTRACT

Purpose: To analyze clinical application of positron-emission tomography with radiopharmaceuticals based on oxygen-15 and to determine the field of its application.

Material and methods: The review of sources, selected from international bibliographic databases.

Results: It is shown that PET with radiopharmaceuticals based on oxygen-15 leads to deep exploration of pathophysiologic basis of a number of brain diseases, among which is ischemic stroke which occupies an important place. Furthermore, the review presents clinical application of PET for chronic cerebrovascular diseases and as a gold standard for validation of other neuroimaging modalities.

Conclusion: PET with radiopharmaceuticals based on oxygen-15 is the only one direct validated method of measurement of a number of quantities characterizing the perfusion and functional capacity of the brain. It may be used in the evaluation of penumbra, quality control of treatment for chronic cerebrovascular diseases and in research. Wide application of this method is prevented by a need of implementation of a large number of costly technical measures.

Key words: positron emission tomography, 15O, perfusion, brain, review

REFERENCES

  1. Znamenskii I.A., Kondakov A.K., Grechko A.V. Pozitronno-emissionnaya tomografiya s kislorodom-15 v nevrologii. Chast' 1. Osnovnye svedeniya i istoricheskii obzor. Medical Radiology and Radiation Safety. 2015. Vol. 60. No. 6. P. 48-54. (In Russ.). (In Russ.).
  2. Lassen N.A. The luxury-perfusion syndrome and its possible relation to acute metabolic acidosis localized within the brain. Lancet. 1996. Vol. 2. No. 7473. P. 1113-1115.
  3. Baron J.C., Bousser M.G., Rey A. et al. Reversal of focal “misery-perfusion syndrome” by extra-intracranial arterial bypass in hemodynamic cerebral ischemia. A case study with 15O positron emission tomography. Stroke. 1981. Vol. 12. No. 4. P. 454-459.
  4. 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. 1948. Vol. 27. No. 4. P. 476-483.
  5. Kudomi N., Hirano Y., Koshino K. et al. Rapid quantitative CBF and CMRO(2) measurements from a single PET scan with sequential administration of dual (15)O-labeled tracers. J. Cereb. Blood Flow Metab. 2013. Vol. 33. No. 3. P. 440-448.
  6. Ibaraki M., Shimosegawa E., Miura S. et al. PET measurements of CBF, OEF, and CMRO2 without arterial sampling in hyperacute ischemic stroke: method and error analysis. Ann. Nucl. Med. 2004. Vol. 18. No. 1. P. 35-44.
  7. Powers W.J. Cerebral blood flow and metabolism: regulation and pathophysiology in cerebrovascular disease. In: Stroke: Pathophysiology, Diagnosis, and Management. 6th ed., ed. by Grotta J.C., Albers G.W., Broderick J.P. et al. Elsevier Health Sci. 2015. P. 28-43.
  8. Raichle M.E., Grubb R.L.. J., Eichling J.O. et al. Measurement of brain oxygen utilization with radioactive oxygen-15: experimental verification. J. Appl. 1976. Vol. 40. No. 4. P. 638-640.
  9. Lebrun-Grandie P., Baron J.-C., Soussaline F. et al. Coupling between regional blood flow and oxygen utilization in the normal human brain. A study with positron tomography and oxygen-15. Arch. Neurol. 1983. Vol. 40. No. 4. P. 230-236.
  10. Sette G., Baron J.C., Mazoyer B. et al. Local brain haemodynamics and oxygen metabolism in cerebrovascular disease. Positron emission tomography. Brain. 1989. Vol. 112. Pt. 4. P. 931-951.
  11. Leblanc R., Yamamoto Y.L., Tyler J.L. et al. Borderzone ischemia. Ann. Neurol. 1987. Vol. 22. No. 6. P. 707-713.
  12. Gibbs J.M., Wise R.J., Leenders K.L. et al. Evaluation of cerebral perfusion reserve in patients with carotidartery occlusion. Lancet. 1984. Vol. 1. No. 8372. P. 310-314.
  13. Ackerman R.H., Correia J.A., Alpert N.M. et al. Positron imaging in ischemic stroke disease using compounds labeled with oxygen 15. Initial results of clinicophysiologic correlations. Archives of neurology. 1981. Vol. 38. No. 9. P. 537-543.
  14. Wise R.J., Bernardi S., Frackowiak R.S. et al. Serial observations on the pathophysiology of acute stroke. The transition from ischaemia to infarction as reflected in regional oxygen extraction. Brain. 1983. Vol. 106. Pt. 1. P. 197-222.
  15. Hakim A.M., Pokrupa R.P., Villanueva J. et al. The effect of spontaneous reperfusion on metabolic function in early human cerebral infarcts. Ann. 1987. Vol. 21. No. 3. P. 279-289.
  16. Baron, J.C., Bousser M.G., Comar D. Human hemispheric infarction studied by positron emission tomography and the 15O continuous inhalation technique. In: Computerized tomography ed. By Caille J.M., Salamon G. New York: Springer Verlag. 1980. P. 231-237.
  17. Baron J.C., Jones T. Oxygen metabolism, oxygen extraction and positron emission tomography: Historical perspective and impact on basic and clinical neuroscience. Neuroimage. 2012. Vol. 61. No. 2, 492-504.
  18. Powers W.J., Grubb R.L., Darriet D. et al. Cerebral blood flow and cerebral metabolic rate of oxygen requirements for cerebral function and viability in humans. J. Cereb. Blood Flow Metab. 1985. Vol. 5. No. 4. P. 600-608.
  19. Touzani O., Young A.R., Derlon J.M. et al. Progressive impairment of brain oxidative metabolism reversed by reperfusion following middle cerebral artery occlusion in anaesthetized baboons. Brain Res. 1997. Vol. 767. No. 1. P. 17-25.
  20. Marchal G., Benali K., Iglesias S. et al. Voxel-based mapping of irreversible ischaemic damage with PET in acute stroke. Brain. 1999. Vol. 122. Pt. 1. P. 2387-2400.
  21. Frykholm P., Andersson J.L., Valtysson J. et al. A metabolic threshold of irreversible ischemia demonstrated by PET in a middle cerebral artery occlusion-reperfusion primate model. Acta Neurol. 2000. Vol. 102. No. 1. P. 18-26.
  22. Marchal G., Rioux P., Serrati C. et al. Value of acutestage positron emission tomography in predicting neurological outcome after ischemic stroke: further assessment. Stroke. 1995. Vol. 26. No. 3. P. 524-525.
  23. Marchal G., Furlan M., Beaudouin V. et al. Early spontaneous hyperperfusion after stroke. A marker of favourable tissue outcome?. Brain. 1996. Vol. 119. Pt. 2. P. 409-419.
  24. Marchal G., Young A.R., Baron J.C. Early postischemic hyperperfusion: pathophysiologic insights from positron emission tomography. J. Cereb. Blood Flow Metab. 1999. Vol. 19. P. 467-482.
  25. Tissue plasminogen activator for acute ischemic stroke. The National Institute of Neurological Disorders and Stroke rt-PA Stroke Study Group. N. Engl. J. Med. 1995. Vol. 333. No. 24. P. 1581-1587.
  26. Baron J.C., Bousser M.G., Comar D. et al. “Crossed cerebellar diaschisis” in human supratentorial braininfarction. Trans. Amer. Neurol. Assoc. 1981. Vol. 105. P. 459-461.
  27. Yamauchi H., Fukuyama H., Kimura J. Hemodynamic and metabolic changes in crossed cerebellar hypoperfusion. Stroke. 1992. Vol. 23. No. 6. P. 855-860.
  28. Baron J.C., Rougemont D., Soussaline F. et al. Local Interrelationships of Cerebral Oxygen Consumption and Glucose Utilization in Normal Subjects and in Ischemic Stroke Patients: A Positron Tomography Study. J. Cereb. Blood Flow Metab. 1984. Vol. 4. No. 2. P. 140-149.
  29. Yamauchi H., Fukuyama H., Nagahama Y. et al. Significance of increased oxygen extraction fraction in five-year prognosis of major cerebral arterial occlusive diseases. J. Nucl. Med. 1999. Vol. 40. No. 12. P. 1992-1998.
  30. Sobesky J., Thiel A., Ghaemi M. et al. Crossed cerebellar diaschisis in acute human stroke: a PET study of serial changes and response to supratentorial reperfusion. J. Cereb. Blood Flow Metab. 2005. Vol. 25. No. 12. P. 1685-1691.
  31. Pantano P., Baron J.C., Samson Y. et al. Crossed cerebellar diaschisis. Further studies. Brain. 1986. Vol. 109. Pt. 4. No. 1. P. 677-694.
  32. Serrati C., Marchal G., Rioux P. et al. Contralateral cerebellar hypometabolism: a predictor for stroke outcome?. J. Neurol. Neurosurg. Psychiatry. 1994. Vol. 57. No. 2. P. 174-179.
  33. Vinichuk S.M. Diashiz i ego rol' v razvitii reflektorno-dvigatel'nykh rasstroistv pri mozgovom insul'te. Ukrans'kii medichnii chasopis. 2013. No. 2. P. 143-147.
  34. Szelies B., Herholz K., Pawlik G. et al. Widespread functional effects of discrete thalamic infarction. Arch. Neurol. 1991. Vol. 48. No. 2. P. 178-182.
  35. Baron J.C., D’Antona R., Pantano P. et al. Effects of thalamic stroke on energy metabolism of the cerebral cortex. A positron tomography study in man. Brain. 1986. Vol. 109. Pt. 6. P. 1243-1259.
  36. Chabriat H., Pappata S., Levasseur M. et al. Cortical metabolism in posterolateral thalamic stroke: PET study. Acta Neurol. 1992. Vol. 86. No. 3. P. 285-290.
  37. Yamauchi H., Fukuyama H., Nagahama Y. et al. Uncoupling of oxygen and glucose metabolism in persistent crossed cerebellar diaschisis. Stroke. 1999. Vol. 30. No. 7. P. 1424-1428
  38. Powers W.J., Derdeyn C.P., Fritsch S.M. et al. Benign prognosis of never-symptomatic carotid occlusion. Neurology. 2000. Vol. 54. No. 4. P. 878-882.
  39. Hokari M., Kuroda S., Shiga T. et al. Impact of oxygen extraction fraction on long-term prognosis in patients with reduced blood flow and vasoreactivity because of occlusive carotid artery disease. Surg. Neurol. 2009. Vol. 71. No. 5. P. 532-538; discussion 538, 538-539.
  40. Yamauchi H., Fukuyama H., Nagahama Y. et al. Evidence of misery perfusion and risk for recurrent stroke in major cerebral arterial occlusive diseases from PET. J. Neurol. Psychiatry. 1996. Vol. 61. No. 1. P. 18-25.
  41. Yamauchi H., Higashi T., Kagawa S. et al. Is misery perfusion still a predictor of stroke in symptomatic major cerebral artery disease?. Brain. 2012. Vol. 135. No. 8. P. 2515-2526.
  42. Barnett H., Peerless S., Fox A. et al. Failure of extracranial-intracranial arterial bypass to reduce the risk of ischemic stroke. Results of an international randomized trial. The EC/IC Bypass Study Group. N. Engl. J. Med. 1985. Vol. 313. No. 19. P. 1191-1200.
  43. Schaller B. Extracranial-intracranial bypass to reduce the risk of ischemic stroke in intracranial aneurysms of the anterior cerebral circulation: a systematic review. J. Stroke Cerebrovasc. Dis. 2008. Vol. 17. No. 5. P. 287-298.
  44. Powers W.J., Clarke W.R., Grubb R.L. et al. Extracranial-intracranial bypass surgery for stroke prevention in hemodynamic cerebral ischemia: the Carotid Occlusion Surgery Study randomized trial. JAMA. 2011. Vol. 306. No. 18. P. 1983-1992.
  45. Persoon S., van Berckel B.N., Bremmer J.P. et al. Intervention versus standard medical treatment in patients with symptomatic occlusion of the internal carotid artery: a randomised oxygen-15 PET study. EJNMMI Res. 2013. Vol. 3. No. 1. P. 79.
  46. Powers W.J., Zazulia A.R. PET in cerebrovascular disease. PET Clin. 2010. Vol. 5. No. 1. P. 83106.
  47. Nortje J., Coles J.P., Timofeev I. et al. Effect of hyperoxia on regional oxygenation and metabolism after severe traumatic brain injury: preliminary findings. Crit. Care Med. 2008. Vol. 36. No. 1. P. 273-281.
  48. Hutchinson P.J., Gupta A.K., Fryer T.F. et al. Correlation between cerebral blood flow, substrate delivery, and metabolism in head injury: a combined microdialysis and triple oxygen positron emission tomography study. J. Cereb. Blood Flow Metab. 2002. Vol. 22. P. 735-745.
  49. Coles J.P., Steiner L.A., Johnston A.J. et al. Does induced hypertension reduce cerebral ischaemia within the traumatized human brain?. Brain. 2004. Vol. 127. No. 11. P. 2479-2490.
  50. Takasawa M., Jones P.S., Guadagno J.V. et al. How reliable is perfusion MR in acute stroke? Validation and determination of the penumbra threshold against quantitative PET. Stroke. 2008. Vol. 39. No. 3. P. 870-877.
  51. Sobesky J., Weber O.Z., Lehnhardt F.G. et al. Does the mismatch match the penumbra? Magnetic resonance imaging and positron emission tomography in early ischemic stroke. Stroke. 2005. Vol. 36. No. 5. P. 980-985.
  52. Yamauchi H., Kudoh T., Kishibe Y. et al. Selective neuronal damage and chronic hemodynamic cerebral ischemia. Ann. Neurol. 2007. Vol. 61. No. 5. P. 454-465.
  53. Yamauchi H., Kudoh T., Kishibe Y. et al. Selective neuronal damage and borderzone infarction in carotid artery occlusive disease: a 11C-flumazenil PET study. J. Nucl. Med. 2005. Vol. 46. No. 12. P. 1973-1979.
  54. Kuroda S., Shiga T., Houkin K. et al. Cerebral oxygen metabolism and neuronal integrity in patients with impaired vasoreactivity attributable to occlusive carotid artery disease. Stroke. 2006. Vol. 37. No. 2. P. 393-398.
  55. Giffard C., Landeau B., Kerrouche N. et al. Decreased chronic-stage cortical 11C-flumazenil binding after focal ischemia-reperfusion in baboons: a marker of selective neuronal loss? Stroke. 2008. Vol. 39. No. 3. P. 991-999.
  56. Fox P.T., Burton H., Raichle M.E. Mapping human somatosensory cortex with positron emission tomography. J. Neurosurg. 1987. Vol. 67. No. 1. P. 34-43.
  57. Fox P.T., Fox P.T., Miezin F.M. et al. Retinotopic organization of human visual cortex mapped with positron-emission tomography. J. Neurosci. 1987. Vol. 7. No. 3. P. 913-922.
  58. Petersen S.E., Fox P.T., Posner M.I. et al. Positron emission tomographic studies of the cortical anatomy of single-word processing. Nature. 1988. Vol. 331. No. 6157. P. 585-589.
  59. Posner M.I., Petersen S.E., Fox P.T. et al. Localization of cognitive operations in the human brain. Science. 1988. Vol. 240. No. 4859. P. 1627-1631.
  60. Feng C.-M., Narayana S., Lancaster J.L. et al. CBF changes during brain activation: fMRI vs. PET. Neuroimage. 2004. Vol. 22. No. 1. P. 443-446.
  61. Cumming P. PET Neuroimaging: The white elephant packs his trunk?. Neuroimage. 2014. Vol. 84. P. 1094-1100.
  62. Gunn R.N., Rabiner E.A. PET neuroimaging: The elephant unpacks his trunk. Neuroimage. 2014. Vol. 94. P. 408-410.
  63. Horwitz B., Simonyan K. PET neuroimaging: plenty of studies still need to be performed: comment on Cumming: “PET neuroimaging: the white elephant packs his trunk?”. Neuroimage. 2014. Vol. 84. P. 1101-1103.
  64. Siebner H.R., Strafella A.P., Rowe J.B. The white elephant revived: a new marriage between PET and MRI: comment to Cumming: “PET neuroimaging: the white elephant packs his trunk?”. Neuroimage. 2014. Vol. 84. P. 1104-1106.
  65. Werner P., Zeisig V., Saur D. et al. Simultaneous PET/MRI. A new tool for translational brain imaging early after stroke. J. Nucl. Med. 2014. Vol. 55. Suppl. No. 1. P. 412.

For citation: Znamenskiy IA, Kondakov AK, Milkin VV, Mosin DJu, Grechko AV. Positron Emission Tomography with Oxygen-15 in Neurological Practice. Part 2. Clinical Application. Medical Radiology and Radiation Safety. 2016;61(4):68-75. Russian.

PDF (RUS) Full-text article (in Russian)