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Effects of hypoxia on the brain: Neuroimaging and neuropsychological findings following carbon monoxide poisoning and obstructive sleep apnea

Published online by Cambridge University Press:  06 February 2004

SHAWN D. GALE  and
RAMONA O. HOPKINS
SHAWN D. GALE
Affiliation:
Department of Clinical Neuropsychology, Barrow Neurological Institute, St. Joseph's Hospital and Medical Center, Phoenix, Arizona
RAMONA O. HOPKINS
Affiliation:
Psychology Department and Neuroscience Center, Brigham Young University, Provo, Utah Department of Medicine, Pulmonary and Critical Care Divisions, LDS Hospital, Salt Lake City, Utah
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Abstract

Hypoxia damages multiple organ systems especially those with high oxygen utilization such as the central nervous system. The purpose of this study was to compare the neuropathological and neuropsychological effects of hypoxia in patients with either carbon monoxide poisoning or obstructive sleep apnea. Neuroimaging revealed evidence of hippocampal atrophy in both groups although a linear relationship between hippocampal volume and memory performance was found only for selected tests and only in the sleep apnea group. There were significant correlations between hippocampal volume and performance on measures related to nonverbal/information processing. Generalized brain atrophy, as measured by the ventricle-to-brain ratio, was more common in the carbon monoxide poisoning group compared to the obstructive sleep apnea group. Performance on tests of executive function improved following treatment with nasal continuous positive airway pressure treatment in the obstructive sleep apnea group but there was no associated improvement in general intellectual function. We found that hypoxia due to obstructive sleep apnea and CO poisoning resulted in neuropathological changes and neuropsychological impairments. The observed group differences provide insight into the relationship between etiology of injury, neuropathological changes, and clinical presentation. (JINS, 2004, 10, 60–71.)

Keywords

Quantitative magnetic resonance imagingCarbon monoxideObstructive sleep apnea
Type
Research Article
Information
Journal of the International Neuropsychological Society , Volume 10 , Issue 1 , January 2004 , pp. 60 - 71
Copyright
© 2004 The International Neuropsychological Society

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References

REFERENCES

Agency for Health Care Policy and Research. (1998). Systematic Review of the Literature Regarding the Diagnosis of Sleep Apnea. Summary, Evidence Report/Technology Assessment: Number 1, December 1998. Rockville, MD. Retrieved from http://www.ahrq.gov/clinic/apnea.htm.
Altman, D.G. (1991). Practical statistics for medical research. London: Chapman and Hall.
Barbe, F., Mayorala, L.R., Duran, J., Masa, J.F., Maimo, A., Montserrat, J.M., Monasterio, C., Bosch, M., Ladaria, A., Rubio, M., Rubio, R., Medinas, M., Hernandez, L., Vidal, S., Douglas, N.J., & Agusti, A.G.N. (2001). Treatment with continuous positive airway pressure is not effective in patients with sleep apnea but no daytime sleepiness. Annals of Internal Medicine, 134, 1015–1023.CrossRefGoogle Scholar
Barker, L.H., Bigler, E.D., Johnson, S.C., Anderson, C.V., Russo, A.A., Boineau, B., & Blatter, D.D. (1999). Polysubstance abuse and traumatic brain injury: Quantitative magnetic resonance imaging and neuropsychological outcome in older adolescents and young adults. Journal of the International Neuropsycholgical Society, 5, 593–608.Google Scholar
Barth, J.T., Findley, L.J., Zillmer, E.A., Gideon, D.A., & Suratt, P.M. (1993). Obstructive sleep apnea, hypoxemia, and personality functioning: Implications for medical psychotherapy assessment. Advances in Medical Psychotherapy, 6, 29–36.Google Scholar
Beck, A.T. (1987). Beck Depression Inventory. San Antonio, TX: The Psychological Corporation.
Beck, A.T. & Steer, R.A. (1993). Beck Anxiety Inventory. San Antonio, TX: The Psychological Corporation.
Bédard, M.A., Montplaisir, J., Malo, J., Richer, F., & Rouleau, I. (1993). Persistent neuropsychological deficits and vigilance impairment in sleep apnea syndrome after treatment with nasal continuous positive airway pressure (CPAP). Journal of Clinical and Experimental Neuropsychology, 15, 330–341.CrossRefGoogle Scholar
Bédard, M., Montplaisir, J., Richer, F., Rouleau, I., & Malo, J. (1991). Obstructive sleep apnea syndrome: Pathogenesis of neuropsychological deficits. Journal of Clinical and Experimental Neuropsychology, 13, 950–964.Google Scholar
Beebe, D.W. & Gozal, D. (2002). Obstructive sleep apnea and the prefrontal cortex: Towards a comprehensive model linking nocturnal upper airway obstruction to daytime cognitive and behavioral deficits. Journal of Sleep Research, 11, 1–16.Google Scholar
Berry, D.T.R., Webb, W.B., Block, A.J., Bauer, R.M., & Switzer, D.A. (1986). Nocturnal hypoxia and neuropsychological variables. Journal of Clinical and Experimental Neuropsychology, 8, 229–238.CrossRefGoogle Scholar
Bigler, E.D., Lowry, C.M., Anderson, C.V., Johnson, S.C., Terry, J., & Steed, M. (2000). Dementia, quantitative neuroimaging, and apolipoprotein E genotype. American Journal of Neuroradiology, 21, 1857–1868.Google Scholar
Bigler, E.D., Blatter, D.D., Anderson, C.V., Johnson, S.C., Gale, S.D., Hopkins, R.O., & Burnett, B. (1997). Hippocampal volume in normal aging and traumatic brain injury. American Journal of Neuroradiology, 18, 11–23.Google Scholar
Biomedical Imaging Resource. (1993). ANALYZE 6.0 [Computer software]. Rochester, MN: Mayo Foundation.
Blatter, D.D., Bigler, E.D., Gale, S.D., Johnson, S.C., Anderson, C.V., Burnett, B.M., Ryser, D., Macnamara, S.E., & Bailey, B.J. (1997). MRI based brain and CSF quantification following traumatic brain injury: Correlation with neuropsychological outcome. American Journal of Neuroradiology, 18, 1–10.Google Scholar
Blatter, D.D., Bigler, E.D., Gale, S.D., Johnson, S.C., Anderson, C.V., Burnett, B.M., Parker, N., Kurth, S., & Horn, S.D. (1995). Quantitative volumetric analysis of brain MRI: Normative database spanning five decades of life. American Journal of Neuroradiology, 16, 241–251.Google Scholar
Bliwise, D.L., King, A.C., & Harris, R.B. (1994). Habitual sleep durations and health in a 50–65 year old population. Journal of Clinical Epidemiology, 47, 35–41.CrossRefGoogle Scholar
Caine, D. & Watson, J. (2000). Neuropsychological and neuropathological sequelae of cerebral anoxia: A critical review. Journal of the International Neuropsychological Society, 6, 86–99.Google Scholar
Cheshire, K., Engleman, H., Deary, I., Shapiro, C., & Douglas, N.J. (1992). Factors impairing daytime performance in patients with sleep apnea/hypopnea syndrome. Archives of Internal Medicine, 152, 538–541.CrossRefGoogle Scholar
Choi, I.S. (1983). Delayed neurologic sequelae in carbon monoxide intoxication. Archives of Neurology, 40, 433–435.Google Scholar
Davis, H.P., Tribuna, J., Pulsinelli, W.A., & Volpe, B.T. (1986). Reference and working memory of rats following hippocampal damage induced by transient forebrain ischemia. Physiology and Behavior, 37, 387–392.CrossRefGoogle Scholar
Derogatis, L.R. (1994). Symptom Checklist–90–Revised (3rd ed.). Minneapolis, MN: National Computer Systems Inc.
Engleman, H.M., Martin, S.E., Deary I.J., &Douglas N.J. (1997). Effect of CPAP therapy on daytime function in patients with mild sleep apnoea/hypopnoea syndrome. Thorax, 52, 114–119.Google Scholar
Findley, L.J., Barth, J.T., Powers, D.C., Wilhoit, S.C., Boyd, D.G., & Suratt, P.M. (1986). Cognitive impairment in patients with obstructive sleep apnea and associated hypoxemia. Chest, 90, 686–690.CrossRefGoogle Scholar
Gale, S.D., Hopkins, R.O., Weaver, L.K., Bigler, E.D., Booth, E.D., & Blatter, D.D. (1999). MRI, quantitative MRI, SPECT, and neuropsychological findings following carbon monoxide poisoning. Brain Injury, 13, 229–243.Google Scholar
Gale, S.D., Hopkins, R.O., Weaver, L.K., Walker, J.M., Bigler, E.D., & Cloward, T.V. (2000). Hippocampal atrophy following sleep apnea and carbon monoxide poisoning: Similarities and differences. Journal of the International Neuropsychological Society, 6, 154.Google Scholar
Gale, S.D., Johnson, S.C., Bigler, E.D., & Blatter, D.D. (1995). Nonspecific white matter degeneration following traumatic brain injury. Journal of the International Neuropsychological Society, 1, 17–28.Google Scholar
Geffen, G., Moar, K.J., O'Hanlon, A.P., Clark, C.R., & Geffen, L.B. (1990). Performance measures of 16- to 86-year old males and females on the auditory verbal learning test. Clinical Neuropsychologist, 4, 45–63.Google Scholar
Greenberg, G.D., Watson, R.K., & Deptula, D. (1987). Neuropsychological dysfunction in sleep apnea. Sleep, 10, 254–262.Google Scholar
Guilleminault, C., van den Hoed, J., & Mitler, M.M. (1978). Clinical overview of the sleep apnea syndromes. In C. Guilleminault & W.C. Dement (Eds.), Sleep apnea syndromes (pp. 1–12). New York: Alan R. Liss.
Heaton, R.K., Grant, I., & Matthews, C.G. (1991). Comprehensive norms for an expanded Halstead-Reitan Battery: Demographic corrections, research findings and clinical applications. Odessa, FL: Psychological Assessment Resources, Inc.
Hopkins, R.O., Gale, S.D., Johnson, S.D., Anderson, C.V., Bigler, E.D., Blatter, D.D., & Weaver, L.K. (1995a). Severe anoxia with and without concomitant brain atrophy and neuropsychological impairments. Journal of the International Neuropsychological Society, 1, 501–509.Google Scholar
Hopkins, R.O., Weaver, L.K., & Kesner, R.P. (1993). Long term memory impairments and hippocampal magnetic resonance imaging in carbon monoxide poisoned subjects. Abstracts, Undersea and Hyperbaric Society Annual Scientific Meeting, Vol. 20 (Suppl.), 15.
Hopkins, R.O., Kesner, R.P., & Goldstein, M. (1995b). Item and order recognition memory in subjects with hypoxic brain injury. Brain and Cognition, 27, 180–201.Google Scholar
Jarrard, L.E. & Meldrum, B.S. (1993). Selective excitotoxic pathology in the rat hippocampus. Neuropathology and Applied Neurobiology, 19, 381–389.Google Scholar
Johnson, R.A. & Wichern, D.W. (2002). Applied multivariate statistical analysis (5th ed.). Upper Saddle River, NJ: Prentice Hall.
Kelly, D.A., Claypoole, K.H., & Coppel, D.B. (1990). Sleep apnea syndrome: Symptomatology, associated features, and neurocognitive correlates. Neuropsychology Review, 1, 323–342.CrossRefGoogle Scholar
Kesler, S.R., Hopkins, R.O., Weaver, L.K., Blatter, D.D., Edge-Booth, H., & Bigler, E.D. (2001). Verbal memory deficits associated with fornix atrophy in carbon monoxide poisoning. Journal of the International Neuropsychological Society, 7, 640–646.CrossRefGoogle Scholar
Kesner, R.P. & Hopkins, R.O. (2001). Short-term memory for duration and distance in humans: Role of the hippocampus. Neuropsychology, 15, 58–68.Google Scholar
Manns, J.R., Hopkins, R.O., Reed, J.M., Kitchener, E.G., & Squire, L.R. (2003). Recognition memory and the human hippocampus. Neuron, 37, 171–180.CrossRefGoogle Scholar
Meyers, J.E. & Meyers, K.R. (1995). Rey Complex Figure Test and Recognition Trial. Lutz, FL: PAR Inc.
Mittenberg, W., Burton, D.B., Darrow, E., & Thompson, G.B. (1992). Normative data for the Wechsler Memory Scale–Revised: 25- to 34-year-olds. Psychological Assessment, 4, 363–368.Google Scholar
Neubauer, J.A. (2001). Physiological and genomic consequences of intermittent hypoxia, invited review: Physiological and pathophysiological responses to intermittent hypoxia. Journal of Applied Physiology, 90, 1593–1599.Google Scholar
Okeda, R., Funata, N., Takano, T., Miyazaki, Y., Higashino, F., Yokoyama, K., & Manabe, M. (1981). The pathogenesis of carbon monoxide encephalopathy in the acute phase-physiological and morphological correlation. Acta Neuropathologica, 54, 1–10.Google Scholar
Piantadosi, C.A. (1987). Carbon monoxide, oxygen transport, and oxygen metabolism. Journal of Hyperbaric Medicine, 2, 27–44.Google Scholar
Piantadosi, C.A., Schmechel, D.E., & Zhang, J. (1995). Is neuronal degeneration mediated by apoptosis after carbon monoxide poisoning. Undersea and Hyperbaric Medicine, 22, 15–16.Google Scholar
Piantadosi, C.A., Zhang, J., Levin, E.D., Folz, R.J., & Schmechel, D.E. (1997a). Apoptosis and delayed neuronal damage after carbon monoxide poisoning in the rat. Experimental Neurology, 147, 103–114.Google Scholar
Piantadosi, C.A., Zhang, J., & Demchenko, I.T. (1997b). Production of hydroxyl radical in the hippocampus after CO hypoxia or hypoxic hypoxia in the rat. Free Radical Biology and Medicine, 22, 725–732.Google Scholar
Raub, J.A., Mathieu-Nolf, M., Hampson, N.B., & Thom, S.R. (2000). Carbon monoxide poisoning—a public health perspective. Toxicology, 145, 1–14.Google Scholar
Reitan, R.M. & Wolfson, D. (1985). The Halstead-Reitan Neuropsychological Test Battery: Theory and clinical interpretation (2nd ed.). Tucson, AZ: Neuropsychology Press.
Rey, A. (1941). L'examen psychologique dans les cas d'encéphalopathie traumatique [Psychological examination of cases of traumatic encephalopathy]. Archives de Psychologie, 28, 286–340.Google Scholar
Rey, A. (1964). L'examen cliniaue en psychologie [The clinical examination in psychology]. Paris: Presses Universitaires de France.
Reynolds, C.R., Hopkins, R.O., & Bigler, E.D. (1999). Continuing decline of memory skills with significant recovery of intellectual function following severe carbon monoxide exposure: Clinical, psychometric, and neuroimaging findings. Archives of Clinical Neuropsychology, 14, 235–249.Google Scholar
Roehrs, T., Merrion, M., Pedrosi, B., Stepanski, E., Zorick, F., & Roth, T. (1995). Neuropsychological function in obstructive sleep apnea syndrome (OSAS) compared to chronic obstructive pulmonary disease (COPD). Sleep, 18, 382–388.Google Scholar
Rourke, S.B. & Adams, K.M. (1996). The neuropsychological correlates of acute and chronic hypoxemia. In I. Grant & K. Adams (Eds.), Neuropsychological assessment of neuropsychiatric disorders (2nd ed., pp. 379–402). New York: Oxford University Press.
Scott, J.G., Krull, K.R., Williamson, D.J., Adams, R.L., & Iverson, G.L. (1997). Oklahoma premorbid intelligence estimation (OPIE): Utilization and clinical samples. Clinical Neuropsychologist, 11, 146–154.CrossRefGoogle Scholar
Stevens, J. (1996). Applied multivariate statistics for the social sciences (3rd ed.). Mahwah, NJ: Lawrence Erlbaum Associates.
Thom, S.R. (1990). Carbon monoxide-mediated brain lipid peroxidation in the rat. Journal of Applied Physiology, 68, 997–1003.Google Scholar
Thom, S.R., Taber, R.L., Mendiguren, I.I., Clark, J.M., Hardy, K.R., & Fisher, A.B. (1995). Delayed neurologic sequelae following carbon monoxide poisoning: Prevention by treatment with hyperbaric oxygen. Annals of Emergency Medicine, 25, 474–480.CrossRefGoogle Scholar
Tombaugh, T.N., Kozak, J., & Rees, L. (1999). Normative data stratified by age and education for two measures of verbal fluency: FAS and animal naming. Archives of Clinical Neuropsychology, 14, 167–177.Google Scholar
Uemura, K., Harada, K., Sadamitsu, D., Tsuruta, R., Takahashi, M., Aki, T., Yasuhara, M., Maekawa, T., & Yoshida, K. (2001). Apoptotic and necrotic brain lesions in a fatal case of carbon monoxide poisoning. Forensic Science International, 116, 213–219.Google Scholar
Valencia-Flores, M., Bliwise, D.L., Guilleminault, C., Cilveti, R., & Clerk, A. (1996). Cognitive function in patients with sleep apnea after acute nocturnal nasal continuous positive airway pressure (CPAP) treatment: Sleepiness and hypoxemia effects. Journal of Clinical and Experimental Neuropsychology, 18, 197–210.Google Scholar
Walker, J.M., Cloward, T.V., Gale, S.D., Hopkins, R.O., Brooks, M., & Farney, R.J. (1999). Hippocampal atrophy and long-lasting neuropsychological deficits in patients with severe obstructive sleep apnea. Abstracts, American Journal of Respiratory and Critical Care Medicine, 159, A770.Google Scholar
Weaver, L.K., Hopkins, R.O., Chan, K.J., Churchill, S., Clemmer, T.P., Elliott, C.G., Orme, J.F., Jr., Thomas, F.O., & Morris, A.H. (2002). Hyperbaric oxygen for acute carbon monoxide poisoning. New England Journal of Medicine, 347, 1057–1067.CrossRefGoogle Scholar
Wechsler, D. (1981). Manual for the Wechsler Adult Intelligence Scale–Revised. San Antonio, TX: The Psychological Corporation.
Wechsler, D. (1987). Wechsler Memory Scale–Revised. San Antonio, TX: The Psychological Corporation.
Young, T., Palta, M., Dempsey, J., Skatrud, J., Weber, S., & Badr, S. (1993). The occurrence of sleep-disordered breathing among middle-aged adults. New England Journal of Medicine, 328, 1230–1235.CrossRefGoogle Scholar
Zola-Morgan, S., Squire, L.R., Rempel, N.L., Clower, R.P., & Amaral, D.G. (1992). Enduring memory impairment in monkeys after ischemic damage to the hippocampus. Journal of Neuroscience, 12, 2582–2596.Google Scholar