Endoneurial oxygen tension and radial topography in nerve edema

doi:10.1016/0006-8993(85)91482-9

Brain Research

Volume 341, Issue 1, 19 August 1985, Pages 147-154

https://doi.org/10.1016/0006-8993(85)91482-9 Get rights and content

Abstract

Endoneurial edema occurs in numerous human and experimental neuropathies. We tested the hypothesis that the resultant increase in intercapillary distance (ICD) may result in endoneurial hypoxia. Experimental galactose neuropathy (EGN) was chosen since in this model, edema is due to the accumulation of galactitol, which does not directly damage nerve fibers, so that it was possible to study the role of endoneurial edema alone. We measured endoneurial oxygen tensions (P_nO₂) using oxygen-sensitive microelectrodes and related P_nO₂ radial topography to ICD. We also determined local oxygen consumption (V_LO2) and critical P_nO₂ (P_critO₂). and age-matched controls were studied at 4 months. (1) Caudal nerve conduction velocity was reduced in EGN. (2) The P_nO₂ values were reduced in EGN and the P_nO₂ histogram was shifted into the hypoxic range. These changes were parallel by a significant increase in ICD in EGN. (3) The radial topography of P_nO₂ in EGN differed from the relatively uniform distribution in control nerves. In EGN the subperineurial P_nO₂ was significantly lower than the P_nO₂ at the center of the fascicle. These changes were paralleled by a significantly greater increase in ICD in the periphery. (4) That the P_nO₂ reduction in EGN was significant is suggested by the marked reduction in ·V_LO2 and the large percentage (> 75%) of intrafascicular regions that fell below P_critO₂ in EGN.

Reference (27)

KarnesJ. et al.
Computerized image recognition for morphometry of nerve attribute of shape of sampled transverse sections of myelinated fibers which best estimates their average diameter
J. neurol. Sci.
(1977)
LowP.A. et al.
Measurement of endoneurial fluid pressure and polyethylene matrix capsules
Brain Research
(1977)
LowP.A. et al.
Mammalian peripheral nerve sheath has unique responses to chronic elevations of endoneurial fluid pressure
Exp. Neurol.
(1980)
LowP.A.
In vitro study of acute elevations of endoneurial pressure in mammalian peripheral nerve sheath
Exp. Neurol.
(1981)
LowP.A. et al.
Peripheral nerve conduction studies in galactose poisoned rats
J. neurol. Sci.
(1983)
MooreJ.W. et al.
Simulations of conduction in uniform myelinated fibers. Relative sensitivity to changes in nodal and internodal parameters
Biophys. J.
(1978)
SendroyJ. et al.
Studies of gas and electrolyte equilibria in blood
J. Biol. Chem.
(1934)
DyckP.J. et al.
Pathologic alterations of the peripheral nervous system of humans
GreeneD.A. et al.
Impaired rat sciatic nerve sodium-potassium adenosine triphosphate in acute streptozotocin diabetes and its correction by dietary myoinositol supplementation
J. clin. Invest.
(1983)
HiyashiN. et al.
Local blood flow, oxygen tension and oxygen consumption in the rat spinal cord
J. Neurosurg.
(1983)

HodgkinA.L. et al.

Measurement of current-voltage relations in the membrane of the giant axon of Loligo

J. Physiol. (Lond.)

(1952)

Leninger-FollertE.

Direct determination of local oxygen consumption of the brain cortex in vivo

LowP.A. et al.

Increased endoneurial fluid pressure in experimental lead neuropathy

Nature (Lond.)

(1977)

Cited by (50)

Neurophysiologic responses of peripheral nerve to repeated episodes of anoxia
2013, Clinical Neurophysiology
Citation Excerpt :
The nervous system is especially vulnerable to hypoxia and ischemia (Astrup et al., 1977; Harden et al., 1966). There have been a large number of in vivo studies of the response of the peripheral nervous system in humans to ischemia using the tourniquet-ischemia model (CruzMartinez et al., 1980; Caruso et al., 1973; Abramson et al., 1971; Seneviratne and Peiris, 1968; Schmelzer et al., 1989; Stohr, 1981; Korthals and Wisniewski, 1975; Bostock et al., 1994) and a growing number of studies on ischemia using in vivo animal models (Schmelzer et al., 1989; Fowler and Gilliatt, 1981; Low et al., 1985, 1986; Kihara et al., 1996; Mitsui et al., 1999). These studies have demonstrated the initial electrophysiologic changes of ischemia appear roughly 10–30 min after onset and include decline in the NAP amplitude and velocity.
Determine the effects of serial episodes of anoxia in an in vitro peripheral nerve preparation.
The nerve action potential (NAP) from rat sciatic nerve was recorded during 5 cycles of anoxia and reperfusion. Multiple NAP parameters were analyzed as well as stimulus response curves.
The amplitude of the NAP declined to half baseline in 865 s on the first cycle of anoxia and recovered to half baseline during recovery in 470 s. These times increased with successive cycles of anoxia. The current required to produce a half maximal NAP showed a variable initial decrease before increasing with anoxia. The paired-pulse response showed a decline at 2–3 ms interstimulus interval during anoxia but was less dependent of interstimulus interval during recovery. NAP amplitude and velocity decrease over successive cycles of anoxia at a rate greater than in the absence of anoxia.
The NAP declines slowly when peripheral nerve is exposed to anoxia but returns at least twice as quickly when re-exposed to oxygen. Short periods of anoxia produce long lasting changes in the nerve suggesting greater resistance to anoxia. With serial episodes of anoxia there is gradual NAP amplitude reduction and increase in duration and latency.
Anoxic-preconditioning appears in isolated peripheral nerve.
Time course of tissue remodelling and electrophysiology in the rat sciatic nerve after spiral cuff electrode implantation
2007, Journal of Neuroimmunology
Implantation of nerve cuff electrodes induces inflammatory cell infiltration and loose connective tissue accumulation. Along with time, morphological changes evolve towards a thicker epi/perineurium as part of mechanisms that protect nerve functionality when a foreign body is wrapped around it. The rise in electrode impedance is linked to the nature of the epineurial tissue. Changes involve an increased expression of neuroprotective factors that is stronger in the endoneurium with axonal degeneration. Our data indicate that epineurial and endoneurial changes after electrode cuff implantation are part of axonal protection mechanisms. Their control is important to improve the yield of FES applications.
Nerve Blood Flow and Microenvironment
2005, Peripheral Neuropathy: 2-Volume Set with Expert Consult Basic
Nerve Blood Flow and Microenvironment
2005, Peripheral Neuropathy
A computational solution of mathematical model for oxygen transport in peripheral nerve
2004, Computers in Biology and Medicine
Time-dependent transport of oxygen in a peripheral nerve by simulating oxygen release, diffusion, chemical reactions and consumption in capillaries and surrounding peripheral nerve tissue using Krogh cylinder symmetry has been studied. Radial diffusion of oxygen is from a capillary to a surrounding cylinder tissue and axial diffusion to arterial distance to veins. A monoexponential or bioexponential function characterizes the approach of the oxygen tension to a new value. The time-dependent transport of oxygen in peripheral nerve with forward and backward reactions has been considered in this mathematical model which makes it different from earlier-studied models. A numerical technique has been used to find the solution.
Nerve conduction velocity, laser Doppler flow, and axonal caliber in galactose and streptozotocin diabetes
1998, Brain Research
In an initial study, the effects of galactose intoxication on nerve laser Doppler blood flow (NLDF) and nerve conduction velocity (NCV) were assessed after 1–16 weeks of galactose feeding in pentobarbital-anesthetized rats. NLDF was not significantly changed at any time point. NCV was significantly reduced after 16, but not 1 or 4, weeks of galactose feeding. In a second study, NLDF was not significantly changed by 4 weeks of galactose intoxication, but streptozotocin-diabetic NLDF was significantly reduced compared to both control (P<0.001) and galactose-intoxicated rats (P<0.05). Compared to control animals, sciatic motor NCV was significantly (P<0.001) reduced in the galactose group, while sciatic and saphenous sensory NCVs were not significantly changed. In the streptozotocin-diabetic rats, motor and sensory NCVs were all significantly reduced (P<0.001). In contrast to the NCV findings, mean caliber of myelinated axons in both the saphenous and sciatic nerves was reduced in galactose-intoxicated, but not streptozotocin-diabetic rats. The observed sequence of changes associated with these two models of diabetic neuropathy is not consistent with the proposed roles of ischemia and axonal dwindling in the reported nerve conduction deficits.

View all citing articles on Scopus

View full text

Endoneurial oxygen tension and radial topography in nerve edema

Abstract

J. neurol. Sci.

Brain Research

Exp. Neurol.

Exp. Neurol.

J. neurol. Sci.

Biophys. J.

J. Biol. Chem.

Pathologic alterations of the peripheral nervous system of humans

Impaired rat sciatic nerve sodium-potassium adenosine triphosphate in acute streptozotocin diabetes and its correction by dietary myoinositol supplementation

J. clin. Invest.

Local blood flow, oxygen tension and oxygen consumption in the rat spinal cord

J. Neurosurg.

Measurement of current-voltage relations in the membrane of the giant axon of Loligo

J. Physiol. (Lond.)

Direct determination of local oxygen consumption of the brain cortex in vivo

Increased endoneurial fluid pressure in experimental lead neuropathy

Nature (Lond.)