Carbon dioxide-mediated vasomotion of extra-cranial cerebral arteries in humans: a role for prostaglandins?

Journal of Physiology

Volumn 594, Issue 12, 2016, Pages 3463-3481

  Hoiland, Ryan L ^a   Tymko, Michael M ^a   Bain, Anthony R ^a   Wildfong, Kevin W ^a   Monteleone, Brad ^a   Ainslie, Philip N ^a  

^a UNIVERSITY OF BRITISH COLUMBIA   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

CARBON DIOXIDE; INDOMETACIN; KETOROLAC; NAPROXEN; PROSTAGLANDIN; PROSTAGLANDIN SYNTHASE;

ADULT; ARTICLE; BLOOD FLOW VELOCITY; BLOOD VESSEL FUNCTION; CONTROLLED STUDY; END TIDAL CARBON DIOXIDE TENSION; ENZYME INHIBITION; FEMALE; HUMAN; HUMAN EXPERIMENT; HYPERCAPNIA; HYPOCAPNIA; IN VITRO STUDY; IN VIVO STUDY; INTERNAL CAROTID ARTERY; MALE; NORMAL HUMAN; PRIORITY JOURNAL; RANDOMIZED CONTROLLED TRIAL; VASOMOTION; VASOMOTOR REFLEX;

EID: 84974712299     PISSN: 00223751     EISSN: 14697793     Source Type: Journal    
DOI: 10.1113/JP272012     Document Type: Article

References (63)

1. Adelstein R & Conti M (1978). Phosphorylation of smooth muscle myosin catalytic subunit of adenosine 3′: 5′-monophosphate-dependent protein kinase. J Biol Chem 253, 8347–8350.
2. 2 reactivity and chemoreflex control of breathing: mechanisms of regulation, measurement, and interpretation. Am J Physiol Regul Integr Comp Physiol 296, R1473–R1495.
3. Ainslie PN & Hoiland RL (2014). Transcranial Doppler ultrasound: valid, invalid, or both? J Appl Physiol 117, 1081–1083.
4. Bain AR, Smith KJ, Lewis NC, Foster GE, Wildfong KW, Willie CK, Hartley GL, Cheung SS & Ainslie PN (2013). Regional changes in brain blood flow during severe passive hyperthermia: effects of and extracranial blood flow. J Appl Physiol 115, 653–659.
5. Brothers RM, Lucas RAI, Zhu YS, Crandall CG & Zhang R (2014). Cerebral vasomotor reactivity: steady-state versus transient changes in carbon dioxide tension. Exp Physiol 99, 1499–1510.
6. Bruhn H, Fransson P & Frahm J (2001). Modulation of cerebral blood oxygenation by indomethacin: MRI at rest and functional brain activation. J Magn Reson Imaging 13, 325–334.
7. Busija D & Heistad D (1983). Effects of indomethacin on cerebral blood flow during hypercapnia in cats. Am J Physiol 244, H519–H524.
8. Chemtob S, Beharry K, Barna T, Varma DR & Aranda J V (1991). Differences in the effects in the newborn piglet of various nonsteroidal antiinfla mmatory drugs on cerebral blood flow but not on cerebrovascular prostaglandins. Pediatr Res 30, 106–111.
9. Coverdale NS, Gati JS, Opalevych O, Perrotta A & Shoemaker JK (2014). Cerebral blood flow velocity underestimates cerebral blood flow during modest hypercapnia and hypocapnia. J Appl Physiol 117, 1090–1096.
10. Coverdale NS, Lalande S, Perrotta A & Shoemaker JK (2015). Hetergeneous patterns of vasoreactivity in the middle cerebral and internal carotid arteries. Am J Physiol Heart Circ Physiol 308, H1030–H1038.
11. Davis RJ, Murdoch CE, Ali M, Purbrick S, Ravid R, Baxter GS, Tilford N, Sheldrick RLG, Clark KL & Coleman RA (2004). EP4 prostanoid receptor-mediated vasodilatation of human middle cerebral arteries. Br J Pharmacol 141, 580–585.
12. Eriksson S, Hagenfeldt L, Law D, Patrono C, Pinca E & Wennmalm A (1983). Effect of prostaglandin synthesis inhibitors on basal and carbon dioxide stimulated cerebral blood flow in man. Acta Physiol Scand 117, 203–211.
13. 2 gradients. Am J Physiol Regul Integr Comp Physiol 298, R1648–R1658.
14. Fog M (1939). Cerebral circulation: II. Reaction of pial arteries to increase in blood pressure. Arch Neurol Psychiatry 41, 260–268.
15. Giller CA, Bowman G, Dyer H, Mootz L & Krippner W (1993). Cerebral arterial diameters during changes in blood pressure and carbon dioxide during craniotomy. Neurosurgery 32, 732–737.
16. Goueli SA & Ahmed K (1980). Indomethacin and inhibition of protein kinase reactions. Nature 287, 171–172.
17. Green DJ, Jones H, Thijssen D, Cable NT & Atkinson G (2011). Flow-mediated dilation and cardiovascular event prediction: does nitric oxide matter? Hypertension 57, 363–369.
18. Green RS, Leffler CW, Busija DW, Fletcher AM & Beasley DG (1987). Indomethacin does not alter the circulating catecholamine response to asphyxia in the neonatal piglet. Pediatr Res 21, 534–537.
19. Heistad DD, Marcus ML & Abboud FM (1978). Role of large arteries in regulation of cerebral blood flow in dogs. J Clin Invest 62, 761.
20. Hoiland RL, Ainslie PN, Wildfong KW, Smith KJ, Bain AR, Willie CK, Foster G, Monteleone B & Day TA (2015). Indomethacin-induced impairment of regional cerebrovascular reactivity: implications for respiratory control. J Physiol 593, 1291–1306.
21. Hoiland RL, Day TA, Wildfong KW, Smith KJ, Bain AR, Willie CK, Foster GE, Monteleone B & Ainslie PN (2014). Hypercapnia induces dilation of large cerebral arteries and is mediated via a non-selective cyclooxygenase pathway (LB704). FASEB J 28, suppl. LB704.
22. 2 in the hypocapnic–hypercapnic range in humans. J Appl Physiol 95, 129–137.
23. Ide K, Worthley M, Anderson T & Poulin MJ (2007). Effects of the nitric oxide synthase inhibitor l-NMMA on cerebrovascular and cardiovascular responses to hypoxia and hypercapnia in humans. J Physiol 584, 321–332.
24. Inaba Y, Chen JA & Bergmann SR (2010). Prediction of future cardiovascular outcomes by flow-mediated vasodilatation of brachial artery: a meta-analysis. Int J Cardiovasc Imaging 26, 631–640.
25. Jallad NS, Garg DC, Martinez JJ, Mroszczak EJ & Weidler DJ (1990). Pharmacokinetics of single-dose oral and intramuscular ketorolac tromethamine in the young and elderly. J Clin Pharmacol 30, 76–81.
26. Jung D, Mroszczak EJ, Wu A, Ling TL, Sevelius H & Bynum L (1989). Pharmacokinetics of ketorolac and p-hydroxyketorolac following oral administration of ketorolac tromethamine. Pharm Res 6, 62–65.
27. Kantor H & Hampton M (1978). Indomethacin in submicromolar concentrations inhibits cyclic AMP-dependent protein kinase. Nature 276, 841–842.
28. Kerrick WG & Hoar PE (1981). Inhibition of smooth muscle tension by cyclic AMP-dependent protein kinase. Nature 292, 253–255.
29. Kety SS & Schmidt CF (1948). The effects of altered arterial tensions of carbon dioxide and oxygen on cerebral blood flow and cerebral oxygen consumption of normal young men. J Clin Invest 27, 484–492.
30. Kontos H, Wei E, Navari RM, Levasseur JE, Rosenblum WI & Patterson JL (1978). Responses of cerebral arteries and arterioles to acute hypotension and hypertension. Am J Physiol 234, H371–H383.
31. Kraaier V, Van Huffelen AC, Wieneke GH, Van Der Worp HB & Bär PR (1992). Quantitative EEG changes due to cerebral vasoconstriction. Indomethacin versus hyperventilation-induced reduction in cerebral blood flow in normal subjects. Electroencephalogr Clin Neurophysiol 82, 208–212.
32. 2. Am J Physiol 277, H1878–H1883.
33. Leffler CW, Mirro R, Thompson C, Shibata M, Armstead WM, Pourcyrous M & Thelin O (1991). Activated oxygen species do not mediate hypercapnia-induced cerebral vasodilation in newborn pigs. Am J Physiol 261, H335–H342.
34. Lucas SJE, Tzeng YC, Galvin SD, Thomas KN, Ogoh S & Ainslie PN (2010). Influence of changes in blood pressure on cerebral perfusion and oxygenation. Hypertension 55, 698–705.
35. Markus HS, Vallance P & Brown MM (1994). Differential effect of three cyclooxygenase inhibitors on human cerebral blood flow velocity and carbon dioxide reactivity. Stroke 25, 1760–1764.
36. Nowak J & Wennmalm Å (1978). Influence of indomethacin and of prostaglandin E1 on total and regional blood flow in man. Acta Physiol Scand 102, 484–491.
37. Numan T, Bain AR, Hoiland RL, Smirl JD, Lewis NC & Ainslie PN (2014). Static autoregulation in humans: a review and reanalysis. Med Eng Phys 36, 1487–1495.
38. 2 and cerebral circulation in newborn pigs: cyclic nucleotides and prostanoids in vascular regulation. Am J Physiol 266, H1494–H1501.
39. Parfenova H, Zuckerman S & Leffler CW (1995). Inhibitory effect of indomethacin on prostacyclin receptor-mediated cerebral vascular responses. Am J Physiol 268, H1884–H1890.
40. CO2. J Physiol 584, 347–357.
41. Peltonen GL, Harrell JW, Rousseau CL, Ernst BS, Marino ML, Crain MK & Schrage WG (2015). Cerebrovascular regulation in men and women: stimulus-specific role of cyclooxygenase. Physiol Rep 3, e12451.
42. Phillis JW & DeLong RE (1987). An involvement of adenosine in cerebral blood flow regulation during hypercapnia. Gen Pharmacol 18, 133–139.
43. Pickard J, Tamura A, Stewart M, McGeorge A & Fitch W (1980). Prostacycline, indomethacin and the cerebral circulation. Brain Res 197, 425–431.
44. Portegies MLP, de Bruijn RFAG, Hofman A, Koudstaal PJ & Ikram MA (2014). Cerebral vasomotor reactivity and risk of mortality: the Rotterdam Study. Stroke 45, 42–47.
45. Querido JS, Ainslie PN, Foster GE, Henderson WR, Halliwill JR, Ayas NT & Sheel AW (2013). Dynamic cerebral autoregulation during and following acute hypoxia: role of carbon dioxide. J Appl Physiol 114, 1183–1190.
46. Regan RE, Fisher JA & Duffin J (2014). Factors affecting the determination of cerebrovascular reactivity. Brain Behav 4, 775–788.
47. 2 in human internal and external carotid and vertebral arteries. J Physiol 590, 3277–3290.
48. Serrador JM, Picot PA, Rutt BK, Shoemaker JK & Bondar RL (2000). MRI measures of middle cerebral artery diameter in conscious humans during simulated orthostasis. Stroke 31, 1672–1678.
49. 2 reactivity in anterior and posterior cerebral circulations. Respir Physiol Neurobiol 189, 76–86.
50. Smith JJ, Hillard CJ, Lee JG, Hudetz AG, Bosnjak ZJ & Kampine JP (1997). The role of nitric oxide in the cerebrovascular to hypercapnia. Anesth Analg 84, 363–369.
51. St Lawrence KS, Ye FQ, Lewis BK, Weinberger DR, Frank JA & McLaughlin AC (2002). Effects of indomethacin on cerebral blood flow at rest and during hypercapnia: an arterial spin tagging study in humans. J Magn Reson Imaging 15, 628–635.
52. Staessen J, Cattaert AN, Fagard R, Lijnen P, Moerman E, De Schaepdryver A & Amery A (1984). Hemodynamic and humoral effects of prostaglandin inhibition in exercising humans. J Appl Physiol 56, 39–45.
53. 2 gas gradients at low- and high-altitude during dynamic end-tidal forcing. Am J Physiol Regul Integr Comp Physiol 308, R895–R906.
54. 2: a technical consideration for the end-tidal-to-arterial gas gradient. J Appl Physiol 120, 282–296.
55. Verbree J, Bronzwaer AGT, Ghariq E, Versluis MJ, Daeman MJAP, van Buchem MA, Dahan A, van Lieshout JJ & van Osch MJP (2014). Assessment of middle cerebral artery diameter during hypocapnia and hypercapnia in humans using ultra high-field MRI. J Appl Physiol 117, 1084–1089.
56. Wennmalm A, Carlsson I, Edlund A, Eriksson S, Kaijser L & Nowak J (1984). Central and peripheral haemodynamic effects of non-steroidal anti-inflammatory drugs in man. Arch Toxicol Suppl 7, 350–359.
57. Wennmalm Å, Eriksson S & Wahren J (1981). Effect of indomethacin on basal and carbon dioxide stimulated cerebral blood flow in man. Clin Physiol 1, 227–234.
58. Willie CK, Colino FL, Bailey DM, Tzeng YC, Binsted G, Jones LW, Haykowsky MJ, Bellapart J, Ogoh S, Smith KJ, Smirl JD, Day TA, Lucas SJ, Eller LK & Ainslie PN (2011). Utility of transcranial Doppler ultrasound for the integrative assessment of cerebrovascular function. J Neurosci Methods 196, 221–237.
59. Willie CK, Macleod DB, Shaw AD, Smith KJ, Tzeng YC, Eves ND, Ikeda K, Graham J, Lewis NC, Day TA & Ainslie PN (2012). Regional brain blood flow in man during acute changes in arterial blood gases. J Physiol 590, 3261–3275.
60. Wolff HG & Lennox WG (1930). Cerebral circulation: XII. The effect on pial vessels of variations in the oxygen and carbon dioxide content of the blood. Arch Neurol Psychiatry 23, 1097.
61. Woodman RJ, Playford DA, Watts GF, Cheetham C, Reed C, Taylor RR, Puddey IB, Beilin LJ, Burke V, Mori TA & Green DJ (2001). Improved analysis of brachial artery ultrasound using a novel edge-detection software system. J Appl Physiol 91, 929–937.
62. Xie A, Skatrud JB, Khayat R, Dempsey JA, Morgan B & Russell D (2005). Cerebrovascular response to carbon dioxide in patients with congestive heart failure. Am J Respir Crit Care Med 172, 371–378.
63. Xie A, Skatrud JB, Morgan B, Chenuel B, Khayat R, Reichmuth K, Lin J & Dempsey JA (2006). Influence of cerebrovascular function on the hypercapnic ventilatory response in healthy humans. J Physiol 577, 319–329.