Effect of Hyperoxia and Hypercapnia on Tissue Oxygen and Perfusion Response in the Normal Liver and Kidney

Overview

Journal PLoS One

Specialties General Medicine
Science

Date 2012 Jul 14

PMID 22792349

Citations 8

Authors

Hai-Ling Margaret Cheng

Affiliations

Soon will be listed here.

Abstract

Objective: Inhalation of air with altered levels of oxygen and carbon dioxide to manipulate tissue oxygenation and perfusion has both therapeutic and diagnostic value. These physiological responses can be measured non-invasively with magnetic resonance (MR) relaxation times. However, interpreting MR measurements is not straight-forward in extra-cranial organs where gas challenge studies have only begun to emerge. Inconsistent results have been reported on MR, likely because different organs respond differently. The objective of this study was to elucidate organ-specific physiological responses to gas challenge underlying MR measurements by investigating oxygenation and perfusion changes in the normal liver and kidney cortex.

Materials And Methods: Gas challenges (100% O(2), 10% CO(2), and carbogen [90% O(2)+10% CO(2)]) interleaved with room air was delivered to rabbits to investigate their effect on tissue oxygenation and perfusion. Real-time fiber-optic measurements of absolute oxygen and relative blood flow were made in the liver and kidney cortex.

Results: Only the liver demonstrated a vasodilatory response to CO(2). Perfusion changes to other gases were minimal in both organs. Tissue oxygenation measurements showed the liver responding only when CO(2) was present and the kidney only when O(2) was present.

Conclusion: This study reveals distinct physiological response mechanisms to gas challenge in the liver and kidney. The detailed characterization of organ-specific responses is critical to improving our understanding and interpretation of MR measurements in various body organs, and will help broaden the application of MR for non-invasive studies of gas challenges.

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References

Davis T, Kwong K, Weisskoff R, Rosen B . Calibrated functional MRI: mapping the dynamics of oxidative metabolism. Proc Natl Acad Sci U S A. 1998; 95(4):1834-9. PMC: 19199. DOI: 10.1073/pnas.95.4.1834. View

Baudelet C, Gallez B . Effect of anesthesia on the signal intensity in tumors using BOLD-MRI: comparison with flow measurements by Laser Doppler flowmetry and oxygen measurements by luminescence-based probes. Magn Reson Imaging. 2004; 22(7):905-12. DOI: 10.1016/j.mri.2004.02.005. View

Wise R, Pattinson K, Bulte D, Chiarelli P, Mayhew S, Balanos G . Dynamic forcing of end-tidal carbon dioxide and oxygen applied to functional magnetic resonance imaging. J Cereb Blood Flow Metab. 2007; 27(8):1521-32. DOI: 10.1038/sj.jcbfm.9600465. View

Foadoddini M, Esmailidehaj M, Mehrani H, Sadraei S, Golmanesh L, Wahhabaghai H . Pretreatment with hyperoxia reduces in vivo infarct size and cell death by apoptosis with an early and delayed phase of protection. Eur J Cardiothorac Surg. 2010; 39(2):233-40. DOI: 10.1016/j.ejcts.2010.05.036. View

Uematsu H, Takahashi M, Hatabu H, Chin C, Wehrli S, Wehrli F . Changes in T1 and T2 observed in brain magnetic resonance imaging with delivery of high concentrations of oxygen. J Comput Assist Tomogr. 2007; 31(5):662-5. DOI: 10.1097/rct.0b013e3180319114. View

Stone J, Wells J, DRAPER W, WHITEHEAD R . Changes in renal blood flow in dogs during the inhalation of 30% carbon dioxide. Am J Physiol. 1958; 194(1):115-9. DOI: 10.1152/ajplegacy.1958.194.1.115. View

Tadamura E, Hatabu H, Li W, Prasad P, Edelman R . Effect of oxygen inhalation on relaxation times in various tissues. J Magn Reson Imaging. 1997; 7(1):220-5. DOI: 10.1002/jmri.1880070134. View

Noseworthy M, Kim J, Stainsby J, Stanisz G, Wright G . Tracking oxygen effects on MR signal in blood and skeletal muscle during hyperoxia exposure. J Magn Reson Imaging. 1999; 9(6):814-20. DOI: 10.1002/(sici)1522-2586(199906)9:6<814::aid-jmri8>3.0.co;2-5. View

Lautt W . Mechanism and role of intrinsic regulation of hepatic arterial blood flow: hepatic arterial buffer response. Am J Physiol. 1985; 249(5 Pt 1):G549-56. DOI: 10.1152/ajpgi.1985.249.5.G549. View

10.

Edrei Y, Gross E, Corchia N, Tsarfaty G, Galun E, Pappo O . Vascular profile characterization of liver tumors by magnetic resonance imaging using hemodynamic response imaging in mice. Neoplasia. 2011; 13(3):244-53. PMC: 3050867. DOI: 10.1593/neo.101354. View

11.

Robinson S, Howe F, Griffiths J . Noninvasive monitoring of carbogen-induced changes in tumor blood flow and oxygenation by functional magnetic resonance imaging. Int J Radiat Oncol Biol Phys. 1995; 33(4):855-9. DOI: 10.1016/0360-3016(95)00072-1. View

12.

Alonzi R, Padhani A, Maxwell R, Taylor N, Stirling J, Wilson J . Carbogen breathing increases prostate cancer oxygenation: a translational MRI study in murine xenografts and humans. Br J Cancer. 2009; 100(4):644-8. PMC: 2653742. DOI: 10.1038/sj.bjc.6604903. View

13.

Howe F, Robinson S, McIntyre D, Stubbs M, Griffiths J . Issues in flow and oxygenation dependent contrast (FLOOD) imaging of tumours. NMR Biomed. 2001; 14(7-8):497-506. DOI: 10.1002/nbm.716. View

14.

Winter J, Estrada M, Cheng H . Normal tissue quantitative T1 and T2* MRI relaxation time responses to hypercapnic and hyperoxic gases. Acad Radiol. 2011; 18(9):1159-67. DOI: 10.1016/j.acra.2011.04.016. View

15.

Moseley M, Chew W, White D, Kucharczyk J, Litt L, Derugin N . Hypercarbia-induced changes in cerebral blood volume in the cat: a 1H MRI and intravascular contrast agent study. Magn Reson Med. 1992; 23(1):21-30. DOI: 10.1002/mrm.1910230104. View

16.

Prisman E, Slessarev M, Han J, Poublanc J, Mardimae A, Crawley A . Comparison of the effects of independently-controlled end-tidal PCO(2) and PO(2) on blood oxygen level-dependent (BOLD) MRI. J Magn Reson Imaging. 2007; 27(1):185-91. DOI: 10.1002/jmri.21102. View

17.

Hughes R, Mathie R, Campbell D, Fitch W . Systemic hypoxia and hyperoxia, and liver blood flow and oxygen consumption in the greyhound. Pflugers Arch. 1979; 381(2):151-7. DOI: 10.1007/BF00582346. View

18.

Thews O, Kelleher D, Vaupel P . Dynamics of tumor oxygenation and red blood cell flux in response to inspiratory hyperoxia combined with different levels of inspiratory hypercapnia. Radiother Oncol. 2002; 62(1):77-85. DOI: 10.1016/s0167-8140(01)00401-7. View

19.

Dutton R, Levitzky M, Berkman R . Carbon dioxide and liver blood flow. Bull Eur Physiopathol Respir. 1976; 12(2):265-73. View

20.

Haacke E, Lai S, Reichenbach J, Kuppusamy K, Hoogenraad F, Takeichi H . In vivo measurement of blood oxygen saturation using magnetic resonance imaging: a direct validation of the blood oxygen level-dependent concept in functional brain imaging. Hum Brain Mapp. 2010; 5(5):341-6. DOI: 10.1002/(SICI)1097-0193(1997)5:5<341::AID-HBM2>3.0.CO;2-3. View