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Erschienen in: Metabolic Brain Disease 1/2015

01.02.2015 | Research Article

Acute hyperammonaemia induces a sustained decrease in vigilance, which is modulated by caffeine

verfasst von: E. P. Casula, P. S. Bisiacchi, M. Corrias, S. Schiff, C. Merkel, P. Amodio, S. Montagnese

Erschienen in: Metabolic Brain Disease | Ausgabe 1/2015

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Abstract

Hyperammonaemia is observed after prolonged, intense exercise, or in patients with hepatic failure. In the latter, it is associated with a set of neurological and psychiatric abnormalities termed hepatic encephalopathy. The aims of our study were: 1. to measure vigilance in a condition of induced hyperammonaemia; 2. to assess whether caffeine modulates the effects of hyperammonaemia on vigilance, if any. Ten healthy volunteers (28.5 ± 5 years; 5 males) underwent three experimental sessions consisting of two-hourly measurements of capillary ammonia, subjective sleepiness (Karolinska Sleepiness Scale) and vigilance (Psychomotor Vigilance Task, PVT), in relation to the intake of breakfast (+/−coffee), an amino acid mixture which induces hyperammonaemia (amino acid challenge; AAC), and AAC+coffee (only for participants who had coffee with their standard breakfast). The AAC resulted in: 1. the expected increase in capillary ammonia levels, with highest values at approximately 4 h after the administration; 2. a significant increase in subjective sleepiness ratings; 3. a sustained increase in PVT-based reaction times. When caffeine was administered after the AAC, both subjective sleepiness and the slowing in RTs were significantly milder than in the AAC-only condition. In conclusion, acute hyperammonaemia induces an increase in subjective sleepiness and a sustained decrease in vigilance, which are attenuated by the administration of a single espresso coffee.
Literatur
Zurück zum Zitat Agrawal A, Sharma BC, Sharma P, Sarin SK (2012) Secondary prophylaxis of hepatic encephalopathy in cirrhosis: an open-label, randomized controlled trial of lactulose, probiotics, and no therapy. Am J Gastroenterol 107:1043–1050PubMedCrossRef Agrawal A, Sharma BC, Sharma P, Sarin SK (2012) Secondary prophylaxis of hepatic encephalopathy in cirrhosis: an open-label, randomized controlled trial of lactulose, probiotics, and no therapy. Am J Gastroenterol 107:1043–1050PubMedCrossRef
Zurück zum Zitat Åkerstedt T, Gillberg M (1990) Subjective and objective sleepiness in the active individual. Int J Neurosci 52:29–37PubMedCrossRef Åkerstedt T, Gillberg M (1990) Subjective and objective sleepiness in the active individual. Int J Neurosci 52:29–37PubMedCrossRef
Zurück zum Zitat Arnal M, Obled C, Attaix D, Patureau-Mirand P, Bonin D (1987) Dietary control of protein turnover. Diabete Metab 13:630–642PubMed Arnal M, Obled C, Attaix D, Patureau-Mirand P, Bonin D (1987) Dietary control of protein turnover. Diabete Metab 13:630–642PubMed
Zurück zum Zitat Bersagliere A, Raduazzo ID, Nardi M, Schiff S, Gatta A, Amodio P, Achermann P, Montagnese S (2012) Induced hyperammonemia may compromise the ability to generate restful sleep in patients with cirrhosis. Hepatology 55:869–878PubMedCrossRef Bersagliere A, Raduazzo ID, Nardi M, Schiff S, Gatta A, Amodio P, Achermann P, Montagnese S (2012) Induced hyperammonemia may compromise the ability to generate restful sleep in patients with cirrhosis. Hepatology 55:869–878PubMedCrossRef
Zurück zum Zitat Bersagliere A, Raduazzo ID, Schiff S, Gatta A, Merkel C, Amodio P, Achermann P, Montagnese S (2013) Ammonia-related changes in cerebral electrogenesis in healthy subjects and patients with cirrhosis. Clin Neurophysiol 124:492–496PubMedCrossRef Bersagliere A, Raduazzo ID, Schiff S, Gatta A, Merkel C, Amodio P, Achermann P, Montagnese S (2013) Ammonia-related changes in cerebral electrogenesis in healthy subjects and patients with cirrhosis. Clin Neurophysiol 124:492–496PubMedCrossRef
Zurück zum Zitat Bjerring PN, Dale N, Larsen FS (2014) Acute hyperammonemia and systemic inflammation is associated with increased extracellular brain adenosine in rats: a biosensor study. Neurochem Res Bjerring PN, Dale N, Larsen FS (2014) Acute hyperammonemia and systemic inflammation is associated with increased extracellular brain adenosine in rats: a biosensor study. Neurochem Res
Zurück zum Zitat Boy C, Meyer PT, Kircheis G, Holschbach MH, Herzog H, Elmenhorst D, Kaiser HJ, Coenen HH, Haussinger D, Zilles K, Bauer A (2008) Cerebral A1 adonosine receptors (A1AR) in liver cirrhosis. Eur J Nucl Med Mol Imaging 35:589–597PubMedCrossRef Boy C, Meyer PT, Kircheis G, Holschbach MH, Herzog H, Elmenhorst D, Kaiser HJ, Coenen HH, Haussinger D, Zilles K, Bauer A (2008) Cerebral A1 adonosine receptors (A1AR) in liver cirrhosis. Eur J Nucl Med Mol Imaging 35:589–597PubMedCrossRef
Zurück zum Zitat Burra P, Masier A (2004) Dynamic tests to study liver function. Eur Rev Med Pharmacol Sci 8:19–21PubMed Burra P, Masier A (2004) Dynamic tests to study liver function. Eur Rev Med Pharmacol Sci 8:19–21PubMed
Zurück zum Zitat Butterworth RF (1998) Effects of hyperammonaemia on brain function. J Inherit Metab Dis 21(Suppl 1):6–20PubMedCrossRef Butterworth RF (1998) Effects of hyperammonaemia on brain function. J Inherit Metab Dis 21(Suppl 1):6–20PubMedCrossRef
Zurück zum Zitat De Rui M, Schiff S, Aprile D, Angeli P, Bombonato G, Bolognesi M, Sacerdoti D, Gatta A, Merkel C, Amodio P, Montagnese S (2013) Excessive daytime sleepiness and hepatic encephalopathy: it is worth asking. Metab Brain Dis 28:245–248PubMedCrossRef De Rui M, Schiff S, Aprile D, Angeli P, Bombonato G, Bolognesi M, Sacerdoti D, Gatta A, Merkel C, Amodio P, Montagnese S (2013) Excessive daytime sleepiness and hepatic encephalopathy: it is worth asking. Metab Brain Dis 28:245–248PubMedCrossRef
Zurück zum Zitat Dinges DI, Powell JW (1985) Microcomputer analysis of performance on a portable, simple visual RT task sustained operations. Behav Res Meth Ins C 17:652–655CrossRef Dinges DI, Powell JW (1985) Microcomputer analysis of performance on a portable, simple visual RT task sustained operations. Behav Res Meth Ins C 17:652–655CrossRef
Zurück zum Zitat Dinges DF, Pack F, Williams K, Gillen KA, Powell JW, Ott GE, Aptowicz C, Pack AI (1997) Cumulative sleepiness, mood disturbance, and psychomotor vigilance performance decrements during a week of sleep restricted to 4–5 hours per night. Sleep 20:267–277PubMed Dinges DF, Pack F, Williams K, Gillen KA, Powell JW, Ott GE, Aptowicz C, Pack AI (1997) Cumulative sleepiness, mood disturbance, and psychomotor vigilance performance decrements during a week of sleep restricted to 4–5 hours per night. Sleep 20:267–277PubMed
Zurück zum Zitat Douglass A, Al Mardini H, Record C (2001) Amino acid challenge in patients with cirrhosis: a model for the assessment of treatments for hepatic encephalopathy. J Hepatol 34:658–664PubMedCrossRef Douglass A, Al Mardini H, Record C (2001) Amino acid challenge in patients with cirrhosis: a model for the assessment of treatments for hepatic encephalopathy. J Hepatol 34:658–664PubMedCrossRef
Zurück zum Zitat Dudley GA, Staron RS, Murray TF, Hagerman FC, Luginbuhl A (1983) Muscle fiber composition and blood ammonia levels after intense exercise in humans. J Appl Physiol 54:582–586PubMed Dudley GA, Staron RS, Murray TF, Hagerman FC, Luginbuhl A (1983) Muscle fiber composition and blood ammonia levels after intense exercise in humans. J Appl Physiol 54:582–586PubMed
Zurück zum Zitat Ferenci P, Lockwood A, Mullen K, Tarter R, Weissenborn K, Blei AT (2002) Hepatic encephalopathy–definition, nomenclature, diagnosis, and quantification: final report of the working party at the 11th World Congresses of Gastroenterology, Vienna, 1998. Hepatology 35:716–721PubMedCrossRef Ferenci P, Lockwood A, Mullen K, Tarter R, Weissenborn K, Blei AT (2002) Hepatic encephalopathy–definition, nomenclature, diagnosis, and quantification: final report of the working party at the 11th World Congresses of Gastroenterology, Vienna, 1998. Hepatology 35:716–721PubMedCrossRef
Zurück zum Zitat Finelli LA, Baumann H, Borbely AA, Achermann P (2000) Dual electroencephalogram markers of human sleep homeostasis: correlation between theta activity in waking and slow-wave activity in sleep. Neuroscience 101:523–529PubMedCrossRef Finelli LA, Baumann H, Borbely AA, Achermann P (2000) Dual electroencephalogram markers of human sleep homeostasis: correlation between theta activity in waking and slow-wave activity in sleep. Neuroscience 101:523–529PubMedCrossRef
Zurück zum Zitat Horne JA, Östberg O (1976) A self-assessment questionnaire to determine morningness-eveningness in human circadian rhythms. Int J Chronobiol 4:97–110PubMed Horne JA, Östberg O (1976) A self-assessment questionnaire to determine morningness-eveningness in human circadian rhythms. Int J Chronobiol 4:97–110PubMed
Zurück zum Zitat Huizenga JR, Gips CH, Conn HO, Jansen PL (1995) Determination of ammonia in ear-lobe capillary blood is an alternative to arterial blood ammonia. Clin Chim Acta 239:65–70PubMedCrossRef Huizenga JR, Gips CH, Conn HO, Jansen PL (1995) Determination of ammonia in ear-lobe capillary blood is an alternative to arterial blood ammonia. Clin Chim Acta 239:65–70PubMedCrossRef
Zurück zum Zitat Kribbs NB, Dinges DF (1994) Vigilance decrement and sleepiness. In: Ogilvie RD, Harsh JR (eds) Sleep onset: normal and abnormal processes. American Psychological Association, Washington DC, pp 113–125CrossRef Kribbs NB, Dinges DF (1994) Vigilance decrement and sleepiness. In: Ogilvie RD, Harsh JR (eds) Sleep onset: normal and abnormal processes. American Psychological Association, Washington DC, pp 113–125CrossRef
Zurück zum Zitat Landolt HP (2008) Sleep homeostasis: a role for adenosine in humans? Biochem Pharmacol 75:2070–2079PubMedCrossRef Landolt HP (2008) Sleep homeostasis: a role for adenosine in humans? Biochem Pharmacol 75:2070–2079PubMedCrossRef
Zurück zum Zitat Landolt HP, Retey JV, Tonz K, Gottselig JM, Khatami R, Buckelmuller I, Achermann P (2004) Caffeine attenuates waking and sleep electroencephalographic markers of sleep homeostasis in humans. Neuropsychopharmacology 29:1933–1939PubMedCrossRef Landolt HP, Retey JV, Tonz K, Gottselig JM, Khatami R, Buckelmuller I, Achermann P (2004) Caffeine attenuates waking and sleep electroencephalographic markers of sleep homeostasis in humans. Neuropsychopharmacology 29:1933–1939PubMedCrossRef
Zurück zum Zitat Lauridsen MM, Jepsen P, Vilstrup H (2011) Critical flicker frequency and continuous reaction times for the diagnosi of minimal hepatic encehphalopathy. A comparative study of 154 patients with liver desease. Metab Brain Dis 26:135–139PubMedCrossRef Lauridsen MM, Jepsen P, Vilstrup H (2011) Critical flicker frequency and continuous reaction times for the diagnosi of minimal hepatic encehphalopathy. A comparative study of 154 patients with liver desease. Metab Brain Dis 26:135–139PubMedCrossRef
Zurück zum Zitat Marchetti P, D’Avanzo C, Orsato R, Montagnese S, Schiff S, Kaplan PW, Piccione F, Merkel C, Gatta A, Sparacino G, Toffolo GM, Amodio P (2011) Electroencephalography in patients with cirrhosis. Gastroenterology 141:1680–1689PubMedCrossRef Marchetti P, D’Avanzo C, Orsato R, Montagnese S, Schiff S, Kaplan PW, Piccione F, Merkel C, Gatta A, Sparacino G, Toffolo GM, Amodio P (2011) Electroencephalography in patients with cirrhosis. Gastroenterology 141:1680–1689PubMedCrossRef
Zurück zum Zitat Molloy JW, Calcagno CJ, Williams CD, Jones FJ, Torres DM, Harrison SA (2012) Association of coffee and caffeine consumption with fatty liver disease, nonalcoholic steatohepatitis, and degree of hepatic fibrosis. Hepatology 55:429–436PubMedCrossRef Molloy JW, Calcagno CJ, Williams CD, Jones FJ, Torres DM, Harrison SA (2012) Association of coffee and caffeine consumption with fatty liver disease, nonalcoholic steatohepatitis, and degree of hepatic fibrosis. Hepatology 55:429–436PubMedCrossRef
Zurück zum Zitat Montagnese S, Jackson C, Morgan MY (2007) Spatio-temporal decomposition of the electroencephalogram in patients with cirrhosis. J Hepatol 46:447–458PubMedCrossRef Montagnese S, Jackson C, Morgan MY (2007) Spatio-temporal decomposition of the electroencephalogram in patients with cirrhosis. J Hepatol 46:447–458PubMedCrossRef
Zurück zum Zitat Nehlig A (1999) Are we dependent upon coffee and caffeine? A review on human and animal data. Neurosci Biobehav Rev 23:563–576PubMedCrossRef Nehlig A (1999) Are we dependent upon coffee and caffeine? A review on human and animal data. Neurosci Biobehav Rev 23:563–576PubMedCrossRef
Zurück zum Zitat Ong JP, Aggarwal A, Krieger D, Easley KA, Karafa MT, Van LF, Arroliga AC, Mullen KD (2003) Correlation between ammonia levels and the severity of hepatic encephalopathy. Am J Med 114:188–193PubMedCrossRef Ong JP, Aggarwal A, Krieger D, Easley KA, Karafa MT, Van LF, Arroliga AC, Mullen KD (2003) Correlation between ammonia levels and the severity of hepatic encephalopathy. Am J Med 114:188–193PubMedCrossRef
Zurück zum Zitat Porkka-Heiskanen T, Strecker RE, McCarley RW (2000) Brain site-specificity of extracellular adenosine concentration changes during sleep deprivation and spontaneous sleep: an in vivo microdialysis study. Neuroscience 99:507–517PubMedCrossRef Porkka-Heiskanen T, Strecker RE, McCarley RW (2000) Brain site-specificity of extracellular adenosine concentration changes during sleep deprivation and spontaneous sleep: an in vivo microdialysis study. Neuroscience 99:507–517PubMedCrossRef
Zurück zum Zitat Powell NB, Riley RW, Schechtman KB, Blumen MB, Dinges DF, Guilleminault C (1999) A comparative model: reaction time performance in sleep-disordered breathing versus alcohol-impaired controls. Laryngoscope 109:1648–1654PubMedCrossRef Powell NB, Riley RW, Schechtman KB, Blumen MB, Dinges DF, Guilleminault C (1999) A comparative model: reaction time performance in sleep-disordered breathing versus alcohol-impaired controls. Laryngoscope 109:1648–1654PubMedCrossRef
Zurück zum Zitat Ribeiro JA, Sebastiao AM (2010) Caffeine and adenosine. J Alzheimers Dis 20(Suppl 1):S3–S15PubMed Ribeiro JA, Sebastiao AM (2010) Caffeine and adenosine. J Alzheimers Dis 20(Suppl 1):S3–S15PubMed
Zurück zum Zitat Romero-Gomez M, Grande L, Camacho I (2004) Prognostic value of altered oral glutamine challenge in patients with minimal hepatic encephalopathy. Hepatology 39:939–943PubMedCrossRef Romero-Gomez M, Grande L, Camacho I (2004) Prognostic value of altered oral glutamine challenge in patients with minimal hepatic encephalopathy. Hepatology 39:939–943PubMedCrossRef
Zurück zum Zitat Scott NR, Stambuk D, Chakraborty J, Marks V, Morgan MY (1989) The pharmacokinetics of caffeine and its dimethylxanthine metabolites in patients with chronic liver disease. Br J Clin Pharmacol 27:205–213PubMedCentralPubMedCrossRef Scott NR, Stambuk D, Chakraborty J, Marks V, Morgan MY (1989) The pharmacokinetics of caffeine and its dimethylxanthine metabolites in patients with chronic liver disease. Br J Clin Pharmacol 27:205–213PubMedCentralPubMedCrossRef
Zurück zum Zitat Sherlock S, Summerskill WH, White LP, Phear EA (1954) Portal-systemic encephalopathy; neurological complications of liver disease. Lancet 267:454–457PubMed Sherlock S, Summerskill WH, White LP, Phear EA (1954) Portal-systemic encephalopathy; neurological complications of liver disease. Lancet 267:454–457PubMed
Zurück zum Zitat Van Dongen HP, Price NJ, Mullington JM, Szuba MP, Kapoor SC, Dinges DF (2001) Caffeine eliminates psychomotor vigilance deficits from sleep inertia. Sleep 24:813–819PubMed Van Dongen HP, Price NJ, Mullington JM, Szuba MP, Kapoor SC, Dinges DF (2001) Caffeine eliminates psychomotor vigilance deficits from sleep inertia. Sleep 24:813–819PubMed
Metadaten
Titel
Acute hyperammonaemia induces a sustained decrease in vigilance, which is modulated by caffeine
verfasst von
E. P. Casula
P. S. Bisiacchi
M. Corrias
S. Schiff
C. Merkel
P. Amodio
S. Montagnese
Publikationsdatum
01.02.2015
Verlag
Springer US
Erschienen in
Metabolic Brain Disease / Ausgabe 1/2015
Print ISSN: 0885-7490
Elektronische ISSN: 1573-7365
DOI
https://doi.org/10.1007/s11011-014-9590-8

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