Anesthesia with dexmedetomidine and low-dose isoflurane increases solute transport via the glymphatic pathway in rat brain when compared with high-dose isoflurane

Anesthesiology

Volumn 127, Issue 6, 2017, Pages 976-988

  Benveniste, Helene ^a   Lee, Hedok ^a   Ding, Fengfei ^b   Sun, Qian ^b   Al Bizri, Ehab ^c   Makaryus, Rany ^c   Probst, Stephen ^c   Nedergaard, Maiken ^b   Stein, Elliot A ^d   Lu, Hanbing ^d  

^a YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b UNIVERSITY OF ROCHESTER MEDICAL CENTER   (United States)

^c Stony Brook School of Dental Medicine   (United States)

^d NATIONAL INSTITUTE ON DRUG ABUSE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

DEXMEDETOMIDINE; ISOFLURANE; AMYLOID BETA PROTEIN; GADOLINIUM PENTETATE; HYPNOTIC SEDATIVE AGENT; INHALATION ANESTHETIC AGENT; ISOENZYME; LACTATE DEHYDROGENASE; LACTATE DEHYDROGENASE 3;

ANESTHESIA; ANGIOGRAPHY; ANIMAL EXPERIMENT; ARTICLE; BLOOD VESSEL DIAMETER; BRAIN; BRAIN SIZE; CEREBROSPINAL FLUID; CONTROLLED STUDY; DRUG DOSE COMPARISON; DRUG MEGADOSE; DRUG TRANSPORT; ELECTRIC ACTIVITY; ELECTROENCEPHALOGRAM; FEMALE; GRAY MATTER; LOW DRUG DOSE; NONHUMAN; NUCLEAR MAGNETIC RESONANCE; NUCLEAR MAGNETIC RESONANCE IMAGING; OSCILLATION; PRIORITY JOURNAL; RAT; SOLUTE; WHITE MATTER; ANIMAL; BRAIN CIRCULATION; COMBINATION DRUG THERAPY; COMPARATIVE STUDY; DIAGNOSTIC IMAGING; DOSE RESPONSE; DRUG EFFECTS; FISCHER 344 RAT; HIPPOCAMPUS; METABOLISM; PHYSIOLOGY; PROCEDURES; SIGNAL TRANSDUCTION; TRANSPORT AT THE CELLULAR LEVEL;

AMYLOID BETA-PEPTIDES; ANESTHETICS, INHALATION; ANIMALS; BIOLOGICAL TRANSPORT; CEREBROVASCULAR CIRCULATION; DEXMEDETOMIDINE; DOSE-RESPONSE RELATIONSHIP, DRUG; DRUG THERAPY, COMBINATION; FEMALE; GADOLINIUM DTPA; HIPPOCAMPUS; HYPNOTICS AND SEDATIVES; ISOENZYMES; ISOFLURANE; L-LACTATE DEHYDROGENASE; MAGNETIC RESONANCE IMAGING; RATS; RATS, INBRED F344; SIGNAL TRANSDUCTION;

EID: 85037683609     PISSN: 00033022     EISSN: 15281175     Source Type: Journal    
DOI: 10.1097/ALN.0000000000001888     Document Type: Article

References (52)

1. Iliff JJ, Wang M, Liao Y, Plogg BA, Peng W, Gundersen GA, Benveniste H, Vates GE, Deane R, Goldman SA, Nagelhus EA, Nedergaard M: A paravascular pathway facilitates CSF flow through the brain parenchyma and the clearance of interstitial solutes, including amyloid β. Sci Transl Med 2012; 4:147ra111
2. Iliff JJ, Chen MJ, Plog BA, Zeppenfeld DM, Soltero M, Yang L, Singh I, Deane R, Nedergaard M: Impairment of glymphatic pathway function promotes tau pathology after traumatic brain injury. J Neurosci 2014; 34:16180-93
3. Lundgaard I, Lu ML, Yang E, Peng W, Mestre H, Hitomi E, Deane R, Nedergaard M: Glymphatic clearance controls state-dependent changes in brain lactate concentration. J Cereb Blood Flow Metab 2017; 37:2112-24
4. Peng W, Achariyar TM, Li B, Liao Y, Mestre H, Hitomi E, Regan S, Kasper T, Peng S, Ding F, Benveniste H, Nedergaard M, Deane R: Suppression of glymphatic fluid transport in a mouse model of Alzheimer's disease. Neurobiol Dis 2016; 93:215-25
5. Bechter K, Hof PR, Benveniste H: On the flow dynamics of cerebrospinal fluid. Neurol Psychiatry Brain Res. 2015; 21: 96-103
6. Cserr HF, Cooper DN, Suri PK, Patlak CS: Efflux of radiolabeled polyethylene glycols and albumin from rat brain. Am J Physiol 1981; 240:F319-28
7. Louveau A, Smirnov I, Keyes TJ, Eccles JD, Rouhani SJ, Peske JD, Derecki NC, Castle D, Mandell JW, Lee KS, Harris TH, Kipnis J: Structural and functional features of central nervous system lymphatic vessels. Nature 2015; 523:337-41
8. Zakharov A, Papaiconomou C, Djenic J, Midha R, Johnston M: Lymphatic cerebrospinal fluid absorption pathways in neonatal sheep revealed by subarachnoid injection of Microfil. Neuropathol Appl Neurobiol 2003; 29:563-73
9. Kress BT, Iliff JJ, Xia M, Wang M, Wei HS, Zeppenfeld D, Xie L, Kang H, Xu Q, Liew JA, Plog BA, Ding F, Deane R, Nedergaard M: Impairment of paravascular clearance pathways in the aging brain. Ann Neurol 2014; 76:845-61
10. Zeppenfeld DM, Simon M, Haswell JD, D'Abreo D, Murchison C, Quinn JF, Grafe MR, Woltjer RL, Kaye J, Iliff JJ: Association of perivascular localization of aquaporin-4 with cognition and Alzheimer disease in aging brains. JAMA Neurol 2017; 74:91-9
11. Sakka L, Coll G, Chazal J: Anatomy and physiology of cerebrospinal fluid. Eur Ann Otorhinolaryngol Head Neck Dis 2011; 128:309-16
12. Iliff JJ, Wang M, Zeppenfeld DM, Venkataraman A, Plog BA, Liao Y, Deane R, Nedergaard M: Cerebral arterial pulsation drives paravascular CSF-interstitial fluid exchange in the murine brain. J Neurosci 2013; 33:18190-9
13. Xie L, Kang H, Xu Q, Chen MJ, Liao Y, Thiyagarajan M, O'Donnell J, Christensen DJ, Nicholson C, Iliff JJ, Takano T, Deane R, Nedergaard M: Sleep drives metabolite clearance from the adult brain. Science 2013; 342:373-7
14. Lee H, Xie L, Yu M, Kang H, Feng T, Deane R, Logan J, Nedergaard M, Benveniste H: The effect of body posture on brain glymphatic transport. J Neurosci 2015; 35:11034-44
15. Ding F, O'Donnell J, Xu Q, Kang N, Goldman N, Nedergaard M: Changes in the composition of brain interstitial ions control the sleep-wake cycle. Science 2016; 352:550-5
16. Keating GM, Hoy SM, Lyseng-Williamson KA: Dexmedetomidine: A guide to its use for sedation in the US. Clin Drug Investig 2012; 32:561-7
17. Jorm CM, Stamford JA: Actions of the hypnotic anaesthetic, dexmedetomidine, on noradrenaline release and cell firing in rat locus coeruleus slices. Br J Anaesth 1993; 71:447-9
18. Purdon PL, Sampson A, Pavone KJ, Brown EN: Clinical electroencephalography for anesthesiologists: Part I-Background and basic signatures. ANESTHESIOLOGY 2015; 123:937-60
19. Mashour GA, Forman SA, Campagna JA: Mechanisms of general anesthesia: From molecules to mind. Best Pract Res Clin Anaesthesiol 2005; 19:349-64
20. Kushikata T, Hirota K, Kotani N, Yoshida H, Kudo M, Matsuki A: Isoflurane increases norepinephrine release in the rat preoptic area and the posterior hypothalamus in vivo and in vitro: Relevance to thermoregulation during anesthesia. Neuroscience 2005; 131:79-86
21. Iliff JJ, Lee H, Yu M, Feng T, Logan J, Nedergaard M, Benveniste H: Brain-wide pathway for waste clearance captured by contrast-enhanced MRI. J Clin Invest 2013; 123:1299-309
22. Stollberger R, Wach P: Imaging of the active B1 field in vivo. Magn Reson Med 1996; 35:246-51
23. Frahm J: Rapid FLASH NMR imaging. Naturwissenschaften 1987; 74:415-22
24. Chang LC, Koay CG, Basser PJ, Pierpaoli C: Linear leastsquares method for unbiased estimation of T1 from SPGR signals. Magn Reson Med 2008; 60:496-501
25. Cheng HL, Wright GA: Rapid high-resolution T(1) mapping by variable flip angles: Accurate and precise measurements in the presence of radiofrequency field inhomogeneity. Magn Reson Med 2006; 55:566-74
26. Deoni SC, Peters TM, Rutt BK: Determination of optimal angles for variable nutation proton magnetic spin-lattice, T1, and spin-spin, T2, relaxation times measurement. Magn Reson Med 2004; 51:194-9
27. Ashburner J, Friston KJ: Unified segmentation. Neuroimage 2005; 26:839-51
28. Valdés-Hernández PA, Sumiyoshi A, Nonaka H, Haga R, Aubert-Vásquez E, Ogawa T, Iturria-Medina Y, Riera JJ, Kawashima R: An in vivo MRI template set for morphometry, tissue segmentation, and fMRI localization in rats. Front Neuroinform 2011; 5:26
29. Lee H, Mortensen K, Sanggaard S, Koch P, Brunner H, Quistorff B, Nedergaard M, Benveniste H: Quantitative Gd-DOTA uptake from cerebrospinal fluid into rat brain using 3D VFA-SPGR at 9.4T. Magn Reson Med 2017 Jun 19 [Epub ahead of print]
30. Li Y, Shen Q, Huang S, Li W, Muir ER, Long JA, Duong TQ: Cerebral angiography, blood flow and vascular reactivity in progressive hypertension. Neuroimage 2015; 111:329-37
31. Veasey SC, Valladares O, Fenik P, Kapfhamer D, Sanford L, Benington J, Bucan M: An automated system for recording and analysis of sleep in mice. Sleep 2000; 23:1025-40
32. Prielipp RC, Wall MH, Tobin JR, Groban L, Cannon MA, Fahey FH, Gage HD, Stump DA, James RL, Bennett J, Butterworth J: Dexmedetomidine-induced sedation in volunteers decreases regional and global cerebral blood flow. Anesth Analg 2002; 95:1052-9
33. Matta BF, Heath KJ, Tipping K, Summors AC: Direct cerebral vasodilatory effects of sevoflurane and isoflurane. ANESTHESIOLOGY 1999; 91:677-80
34. Johnston M, Zakharov A, Koh L, Armstrong D: Subarachnoid injection of Microfil reveals connections between cerebrospinal fluid and nasal lymphatics in the non-human primate. Neuropathol Appl Neurobiol 2005; 31:632-40
35. Callado LF, Stamford JA: Alpha2A- but not alpha2B/Cadrenoceptors modulate noradrenaline release in rat locus coeruleus: Voltammetric data. Eur J Pharmacol 1999; 366:35-9
36. Zilles K, Qü M, Schleicher A: Regional distribution and heterogeneity of alpha-adrenoceptors in the rat and human central nervous system. J Hirnforsch 1993; 34:123-32
37. Akeju O, Loggia ML, Catana C, Pavone KJ, Vazquez R, Rhee J, Contreras Ramirez V, Chonde DB, Izquierdo-Garcia D, Arabasz G, Hsu S, Habeeb K, Hooker JM, Napadow V, Brown EN, Purdon PL: Disruption of thalamic functional connectivity is a neural correlate of dexmedetomidine-induced unconsciousness. Elife 2014; 3:e04499
38. Pal D, Silverstein BH, Lee H, Mashour GA: Neural correlates of wakefulness, sleep, and general anesthesia: An experimental study in rat. ANESTHESIOLOGY 2016; 125:929-42
39. Gompf H, Chen J, Sun Y, Yanagisawa M, Aston-Jones G, Kelz MB: Halothane-induced hypnosis is not accompanied by inactivation of orexinergic output in rodents. ANESTHESIOLOGY 2009; 111:1001-9
40. Anzawa N, Kushikata T, Ohkawa H, Yoshida H, Kubota T, Matsuki A: Increased noradrenaline release from rat preoptic area during and after sevoflurane and isoflurane anesthesia. Can J Anaesth 2001; 48:462-5
41. Hogue CW Jr, Talke P, Stein PK, Richardson C, Domitrovich PP, Sessler DI: Autonomic nervous system responses during sedative infusions of dexmedetomidine. ANESTHESIOLOGY 2002; 97:592-8
42. Lu H, Zou Q, Gu H, Raichle ME, Stein EA, Yang Y: Rat brains also have a default mode network. Proc Natl Acad Sci USA 2012; 109:3979-84
43. Guldenmund P, Demertzi A, Boveroux P, Boly M, Vanhaudenhuyse A, Bruno MA, Gosseries O, Noirhomme Q, Brichant JF, Bonhomme V, Laureys S, Soddu A: Thalamus, brainstem and salience network connectivity changes during propofol-induced sedation and unconsciousness. Brain Connect 2013; 3:273-85
44. Abas M, Vanderpyl J, Le Prou T, Kydd R, Emery B, Foliaki SA: Psychiatric hospitalization: Reasons for admission and alternatives to admission in South Auckland, New Zealand. Aust N Z J Psychiatry 2003; 37:620-5
45. Todd MM, Weeks J: Comparative effects of propofol, pentobarbital, and isoflurane on cerebral blood flow and blood volume. J Neurosurg Anesthesiol 1996; 8:296-303
46. Nedergaard M: Neuroscience: Garbage truck of the brain. Science 2013; 340:1529-30
47. Ooms S, Overeem S, Besse K, Rikkert MO, Verbeek M, Claassen JA: Effect of 1 night of total sleep deprivation on cerebrospinal fluid β-amyloid 42 in healthy middle-aged men: A randomized clinical trial. JAMA Neurol 2014; 71:971-7
48. Roh JH, Jiang H, Finn MB, Stewart FR, Mahan TE, Cirrito JR, Heda A, Snider BJ, Li M, Yanagisawa M, de Lecea L, Holtzman DM: Potential role of orexin and sleep modulation in the pathogenesis of Alzheimer's disease. J Exp Med 2014; 211:2487-96
49. Spira AP, Gamaldo AA, An Y, Wu MN, Simonsick EM, Bilgel M, Zhou Y, Wong DF, Ferrucci L, Resnick SM: Self-reported sleep and β-amyloid deposition in community-dwelling older adults. JAMA Neurol 2013; 70:1537-43
50. Brown EN, Purdon PL, Van Dort CJ: General anesthesia and altered states of arousal: A systems neuroscience analysis. Annu Rev Neurosci 2011; 34:601-28
51. Jansson CC, Pohjanoksa K, Lang J, Wurster S, Savola JM, Scheinin M: Alpha2-adrenoceptor agonists stimulate highaffinity GTPase activity in a receptor subtype-selective manner. Eur J Pharmacol 1999; 374:137-46
52. Vemparala S, Domene C, Klein ML: Computational studies on the interactions of inhalational anesthetics with proteins. Acc Chem Res 2010; 43:103-10