r-n-jРоссийский неврологический журналRussian neurological journal2658-79472686-7192МИА10.30629/2658-7947-2023-28-5-21-27r-n-j-480Research ArticleОБЗОРЫREVIEWSМинимальная печеночная энцефалопатия: клинические, нейрофизиологические, нейровизуализационные маркерыMinimal hepatic encephalopathy: clinical, neurophysiological, neuroimaging markershttps://orcid.org/0000-0002-4626-6520КузнецоваП. И.KuznetsovaP. I.

Кузнецова Полина Игоревна,

Москва.

Kuznetsova Polina I.

Moscow.

angioneurology0@gmail.comhttps://orcid.org/0000-0003-0522-767XРаскуражевА. А.RaskurazhevA. A.

Москва.

Moscow.

rasckey@live.comhttps://orcid.org/0000-0002-9093-344XМорозоваС. Н.MorozovaS. N.

Москва.

Moscow.

morozova@neurology.ruhttps://orcid.org/0000-0003-3282-2116ЛовчевИ. М.LovchevI. M.

Москва.

Moscow.

lovchevim@rambler.ruhttps://orcid.org/0000-0002-6362-7914НоврузбековМ. С.NovruzbekovM. S.

Москва.

Moscow.

nms@transpl.moscow.ruhttps://orcid.org/0000-0002-5883-8119ТанашянМ. М.TanashyanM. M.

Москва.

Moscow.

M_Tanashyan2004@mail.ruФГБНУ Научный центр неврологииРоссияResearch Center of NeurologyRussian FederationРоссийский национальный исследовательский медицинский университет имени Н.И. Пирогова Минздрава РоссииРоссияN.I. Pirogov Russian National Research Medical UniversityRussian Federation2023251120232852127Copyright © Кузнецова П.И., Раскуражев А.А., Морозова С.Н., Ловчев И.М., Новрузбеков М.С., Танашян М.М., 20232023Кузнецова П.И., Раскуражев А.А., Морозова С.Н., Ловчев И.М., Новрузбеков М.С., Танашян М.М.Kuznetsova P.I., Raskurazhev A.A., Morozova S.N., Lovchev I.M., Novruzbekov M.S., Tanashyan M.M.Данная работа распространяется под лицензией Creative Commons Attribution 4.0.This work is licensed under a Creative Commons Attribution 4.0 License.https://www.r-n-j.com/jour/article/view/480

Печеночная энцефалопатия на начальных стадиях — сложно диагностируемый клинический феномен, в основе которого лежит накопление аммиака. Симптомы энцефалопатии чрезвычайно разнообразны: от легкого снижения когнитивного статуса и минимальных аффективных расстройств до угнетения сознания и комы на терминальных стадиях заболевания. Однако не всегда тяжесть патологии печени и данные нейрофизиологических и нейровизуализационных исследований коррелируют со степенью выраженности энцефалопатии. Наибольшие трудности при диагностике возникают на начальных этапах заболевания, а вовремя распознанный и установленный диагноз может не только замедлить прогрессирование когнитивного дефицита, характерологических изменений, но и существенно улучшить прогноз пациента.

Hepatic encephalopathy in the initial stages is a diagnostically challenging clinical phenomenon, based on the accumulation of ammonia. Symptoms of encephalopathy are extremely varied: from a slight cognitive decrease and minimal affective disorders to disorders of consciousness and coma in the terminal stages. However, the severity of liver pathology and neurophysiological and neuroimaging data do not always correlate with the severity of encephalopathy. The greatest difficulties in diagnosis arise at the initial stage of the disease, and a timely recognized and established diagnosis can not only slow down the progression of cognitive deficits and characterological changes, but also significantly improve the patient’s prognosis.

печеночная энцефалопатияаммиакМРТ головного мозгамарганецбазальные ганглииhepatic encephalopathyammoniabrain MRImanganesebasal gangliaReferencesLu K., Zimmermann M., Görg B., Bidmon H.J., Biermann B. et al. Hepatic encephalopathy is linked to alterations of autophagic flux in astrocytes. EBioMedicine. 2019;48:539–553. doi:10.1016/j.ebiom.2019.09.058Lu K., Zimmermann M., Görg B., Bidmon H.J., Biermann B. et al. Hepatic encephalopathy is linked to alterations of autophagic flux in astrocytes. EBioMedicine. 2019;48:539–553. doi:10.1016/j.ebiom.2019.09.058Hahn M., Massen O., Nencki M., Pavlov I. Die Eck’sche fistel zwischen der unteren hohlvene und der pfortader und ihre folgen fur den organismus. Arch Exp Pathol Pharm. 1893;32:161–210.Hahn M., Massen O., Nencki M., Pavlov I. Die Eck’sche fistel zwischen der unteren hohlvene und der pfortader und ihre folgen fur den organismus. Arch Exp Pathol Pharm. 1893;32:161–210.Sherlock S., Summerskill W.H.J., White L.P., Phear E.A. Portalsystemic encephalopathy. Neurological complications of liver disease. Lancet. 1954;267:453–457.Sherlock S., Summerskill W.H.J., White L.P., Phear E.A. Portalsystemic encephalopathy. Neurological complications of liver disease. Lancet. 1954;267:453–457.Amodio P. Hepatic encephalopathy: historical remarks. J Clin Exp Hepatol. 2015;5(Suppl 1):S4–6. doi: 10.1016/j.jceh.2014.12.005Amodio P. Hepatic encephalopathy: historical remarks. J Clin Exp Hepatol. 2015;5(Suppl 1):S4–6. doi: 10.1016/j.jceh.2014.12.005Córdoba J. New assessment of hepatic encephalopathy. J Hepatol. 2011;54(5):1030–40. doi: 10.1016/j.jhep.2010.11.015Córdoba J. New assessment of hepatic encephalopathy. J Hepatol. 2011;54(5):1030–40. doi: 10.1016/j.jhep.2010.11.015Кузнецова П.И., Танашян М.М., Корнилова А.А. Токсическая энцефалопатия при истинной полицитемии (клинический случай). Бюллетень сибирской медицины. 2019;18(4):249–255. https://doi.org/10.20538/1682-0363-2019-4-249-255Kuznetsova P.I., Tanashyan M.M., Kornilova A.A. Toxic encephalopathy in polycythemia vera (clinical case). Bulletin of Siberian Medicine. 2019;18(4):249–255. (In Russ). https://doi.org/10.20538/1682-0363-2019-4-249-255Peng J.K., Hepgul N., Higginson I.J., Gao W. Symptom prevalence and quality of life of patients with end-stage liver disease: A systematic review and meta-analysis. Palliat Med. 2019;33(1):24–36. doi: 10.1177/0269216318807051Peng J.K., Hepgul N., Higginson I.J., Gao W. Symptom prevalence and quality of life of patients with end-stage liver disease: A systematic review and meta-analysis. Palliat Med. 2019;33(1):24–36. doi: 10.1177/0269216318807051Tapper E.B., Parikh N.D. Diagnosis and Management of Cirrhosis and Its Complications: A Review. JAMA. 2023;329(18):1589–1602. doi: 10.1001/jama.2023.5997Tapper E.B., Parikh N.D. Diagnosis and Management of Cirrhosis and Its Complications: A Review. JAMA. 2023;329(18):1589–1602. doi: 10.1001/jama.2023.5997Xiao G., Ye Q., Han T., Yan J., Sun L., Wang F. Study of the sleep quality and psychological state of patients with hepatitis B liver cirrhosis. Hepatol Res. 2018;48(3):E275–E282. doi: 10.1111/hepr.12981Xiao G., Ye Q., Han T., Yan J., Sun L., Wang F. Study of the sleep quality and psychological state of patients with hepatitis B liver cirrhosis. Hepatol Res. 2018;48(3):E275–E282. doi: 10.1111/hepr.12981Eftekar M. The association between hepatic encephalopathy/minimal hepatic encephalopathy and depressive and anxiety disorders: a systematic review. Australas Psychiatry. 2020;28(1):61–65. doi: 10.1177/1039856219875054Eftekar M. The association between hepatic encephalopathy/minimal hepatic encephalopathy and depressive and anxiety disorders: a systematic review. Australas Psychiatry. 2020;28(1):61–65. doi: 10.1177/1039856219875054Shah N.M., Malhotra A.M., Kaltsakas G. Sleep disorder in patients with chronic liver disease: a narrative review. J Thorac Dis. 2020;12(Suppl 2):S248–S260. doi: 10.21037/jtd-cus-2020-012Shah N.M., Malhotra A.M., Kaltsakas G. Sleep disorder in patients with chronic liver disease: a narrative review. J Thorac Dis. 2020;12(Suppl 2):S248–S260. doi: 10.21037/jtd-cus-2020-012Hardeland R. Melatonin metabolism in the central nervous system. Curr Neuropharmacol. 2010;8(3):168–81. doi: 10.2174/157015910792246244Hardeland R. Melatonin metabolism in the central nervous system. Curr Neuropharmacol. 2010;8(3):168–81. doi: 10.2174/157015910792246244Chojnacki C., Wachowska-Kelly P., Błasiak J., Reiter R.J., Chojnacki J. Melatonin secretion and metabolism in patients with hepatic encephalopathy. J Gastroenterol Hepatol. 2013;28(2):342–7. doi: 10.1111/jgh.12055Chojnacki C., Wachowska-Kelly P., Błasiak J., Reiter R.J., Chojnacki J. Melatonin secretion and metabolism in patients with hepatic encephalopathy. J Gastroenterol Hepatol. 2013;28(2):342–7. doi: 10.1111/jgh.12055Velissaris D., Karamouzos V., Polychronopoulos P., Karanikolas M. Chronotypology and melatonin alterations in minimal hepatic encephalopathy. J Circadian Rhythms. 2009;7:6. doi: 10.1186/1740-3391-7-6Velissaris D., Karamouzos V., Polychronopoulos P., Karanikolas M. Chronotypology and melatonin alterations in minimal hepatic encephalopathy. J Circadian Rhythms. 2009;7:6. doi: 10.1186/1740-3391-7-6Cordoba J., Steindl P., Blei A.T. Melatonin arrhythmia is corrected after liver transplantation. Am J Gastroenterol. 2009;104(7):1862–3. doi: 10.1038/ajg.2009.171Cordoba J., Steindl P., Blei A.T. Melatonin arrhythmia is corrected after liver transplantation. Am J Gastroenterol. 2009;104(7):1862–3. doi: 10.1038/ajg.2009.171Harding E.C., Franks N.P., Wisden W. The Temperature Dependence of Sleep. Front Neurosci. 2019;13:336. doi: 10.3389/fnins.2019.00336Harding E.C., Franks N.P., Wisden W. The Temperature Dependence of Sleep. Front Neurosci. 2019;13:336. doi: 10.3389/fnins.2019.00336Kräuchi K., Cajochen C., Werth E., Wirz-Justice A. Warm feet promote the rapid onset of sleep. Nature. 1999;401(6748):36–7. doi: 10.1038/43366Kräuchi K., Cajochen C., Werth E., Wirz-Justice A. Warm feet promote the rapid onset of sleep. Nature. 1999;401(6748):36–7. doi: 10.1038/43366Garrido M., Saccardo D., De Rui M., Vettore E., Verardo A., Carraro P., Di Vitofrancesco N., Mani A.R., Angeli P., Bolognesi M., Montagnese S. Abnormalities in the 24-hour rhythm of skin temperature in cirrhosis: Sleep-wake and general clinical implications. Liver Int. 2017;37(12):1833–1842. doi: 10.1111/liv.13525Garrido M., Saccardo D., De Rui M., Vettore E., Verardo A., Carraro P., Di Vitofrancesco N., Mani A.R., Angeli P., Bolognesi M., Montagnese S. Abnormalities in the 24-hour rhythm of skin temperature in cirrhosis: Sleep-wake and general clinical implications. Liver Int. 2017;37(12):1833–1842. doi: 10.1111/liv.13525Bosoi C.R., Rose C.F. Oxidative stress: a systemic factor implicated in the pathogenesis of hepatic encephalopathy. Metab Brain Dis. 2013;28:175–8.Bosoi C.R., Rose C.F. Oxidative stress: a systemic factor implicated in the pathogenesis of hepatic encephalopathy. Metab Brain Dis. 2013;28:175–8.Jayakumar A.R., Norenberg M.D. Hyperammonemia in Hepatic Encephalopathy. J Clin Exp Hepatol. 2018;8(3):272–280. doi: 10.1016/j.jceh.2018.06.007Jayakumar A.R., Norenberg M.D. Hyperammonemia in Hepatic Encephalopathy. J Clin Exp Hepatol. 2018;8(3):272–280. doi: 10.1016/j.jceh.2018.06.007Chen Z., Ruan J., Li D., Wang M., Han Z., Qiu W., Wu G. The Role of Intestinal Bacteria and Gut-Brain Axis in Hepatic Encephalopathy. Front Cell Infect Microbiol. 2021;10:595759. doi: 10.3389/fcimb.2020.595759Chen Z., Ruan J., Li D., Wang M., Han Z., Qiu W., Wu G. The Role of Intestinal Bacteria and Gut-Brain Axis in Hepatic Encephalopathy. Front Cell Infect Microbiol. 2021;10:595759. doi: 10.3389/fcimb.2020.595759Perazzo J.C., Tallis S., Delfante A., Souto P.A., Lemberg A., Eizayaga F.X., Romay S. Hepatic encephalopathy: An approach to its multiple pathophysiological features. World J Hepatol. 2012;4(3):50–65. doi: 10.4254/wjh.v4.i3.50Perazzo J.C., Tallis S., Delfante A., Souto P.A., Lemberg A., Eizayaga F.X., Romay S. Hepatic encephalopathy: An approach to its multiple pathophysiological features. World J Hepatol. 2012;4(3):50–65. doi: 10.4254/wjh.v4.i3.50Josephs K.A., Ahlskog J.E., Klos K.J., Kumar N., Fealey R.D., Trenerry M.R., Cowl C.T. Neurologic manifestations in welders with pallidal MRI T1 hyperintensity. Neurology. 2005;64(12):2033–9. doi: 10.1212/01.WNL.0000167411.93483.A1Josephs K.A., Ahlskog J.E., Klos K.J., Kumar N., Fealey R.D., Trenerry M.R., Cowl C.T. Neurologic manifestations in welders with pallidal MRI T1 hyperintensity. Neurology. 2005;64(12):2033–9. doi: 10.1212/01.WNL.0000167411.93483.A1Kaplan P.W., Rossetti A.O. EEG patterns and imaging correlations in encephalopathy: encephalopathy part II. J Clin Neurophysiol. 2011;28(3):233–51. doi: 10.1097/WNP.0b013e31821c33a0Kaplan P.W., Rossetti A.O. EEG patterns and imaging correlations in encephalopathy: encephalopathy part II. J Clin Neurophysiol. 2011;28(3):233–51. doi: 10.1097/WNP.0b013e31821c33a0Karanfi lian B.V., Park T., Senatore F., Rustgi V.K. Minimal Hepatic Encephalopathy. Clin Liver Dis. 2020;24(2):209–218. doi: 10.1016/j.cld.2020.01.012Karanfi lian B.V., Park T., Senatore F., Rustgi V.K. Minimal Hepatic Encephalopathy. Clin Liver Dis. 2020;24(2):209–218. doi: 10.1016/j.cld.2020.01.012Koul R., Maiwall R., Ramalingam A., Kumar S., Dhamija R.M., Pamecha V., Sarin S.K. Role of EEG in Predicting Outcome of Hepatic Encephalopathy Patients. Neurodiagn J. 2020;60(4):272–288. doi: 10.1080/21646821.2020.1824959Koul R., Maiwall R., Ramalingam A., Kumar S., Dhamija R.M., Pamecha V., Sarin S.K. Role of EEG in Predicting Outcome of Hepatic Encephalopathy Patients. Neurodiagn J. 2020;60(4):272–288. doi: 10.1080/21646821.2020.1824959Montagnese S., Balistreri E., Schiff S., De Rui M., Angeli P., Zanus G., Cillo U., Bombonato G., Bolognesi M., Sacerdoti D., Gatta A., Merkel C., Amodio P. Covert hepatic encephalopathy: agreement and predictive validity of different indices. World J Gastroenterol. 2014;20(42):15756–62. doi: 10.3748/wjg.v20.i42.15756Montagnese S., Balistreri E., Schiff S., De Rui M., Angeli P., Zanus G., Cillo U., Bombonato G., Bolognesi M., Sacerdoti D., Gatta A., Merkel C., Amodio P. Covert hepatic encephalopathy: agreement and predictive validity of different indices. World J Gastroenterol. 2014;20(42):15756–62. doi: 10.3748/wjg.v20.i42.15756Rose C., Butterworth R.F., Zayed J., Normandin L., Todd K., Michalak A., Spahr L., Huet P.M., Pomier-Layrargues G. Manganese deposition in basal ganglia structures results from both portal-systemic shunting and liver dysfunction. Gastroenterology. 1999;117(3):640–4. doi: 10.1016/s0016-5085(99)70457-9Rose C., Butterworth R.F., Zayed J., Normandin L., Todd K., Michalak A., Spahr L., Huet P.M., Pomier-Layrargues G. Manganese deposition in basal ganglia structures results from both portal-systemic shunting and liver dysfunction. Gastroenterology. 1999;117(3):640–4. doi: 10.1016/s0016-5085(99)70457-9Olanow C.W. Manganese-induced parkinsonism and Parkinson’s disease. Ann N Y Acad Sci. 2004;1012:209–23. doi: 10.1196/annals.1306.018Olanow C.W. Manganese-induced parkinsonism and Parkinson’s disease. Ann N Y Acad Sci. 2004;1012:209–23. doi: 10.1196/annals.1306.018Rovira A., Alonso J., Córdoba J. MR imaging findings in hepatic encephalopathy. AJNR Am J Neuroradiol. 2008;29(9):1612–21. doi: 10.3174/ajnr.A1139Rovira A., Alonso J., Córdoba J. MR imaging findings in hepatic encephalopathy. AJNR Am J Neuroradiol. 2008;29(9):1612–21. doi: 10.3174/ajnr.A1139Cheong I., Marjańska M., Deelchand D.K., Eberly L.E., Walk D., Öz G. Ultra-High Field Proton MR Spectroscopy in Early-Stage Amyotrophic Lateral Sclerosis. Neurochem Res. 2017;42(6):1833–1844. doi: 10.1007/s11064-017-2248-2Cheong I., Marjańska M., Deelchand D.K., Eberly L.E., Walk D., Öz G. Ultra-High Field Proton MR Spectroscopy in Early-Stage Amyotrophic Lateral Sclerosis. Neurochem Res. 2017;42(6):1833–1844. doi: 10.1007/s11064-017-2248-2Lim C.G., Hahm M.H., Lee H.J. Hepatic encephalopathy on magnetic resonance imaging and its uncertain differential diagnoses: a narrative review. J Yeungnam Med Sci. 2023;40(2):136–145. doi: 10.12701/jyms.2022.00689Lim C.G., Hahm M.H., Lee H.J. Hepatic encephalopathy on magnetic resonance imaging and its uncertain differential diagnoses: a narrative review. J Yeungnam Med Sci. 2023;40(2):136–145. doi: 10.12701/jyms.2022.00689Chavarria L., Cordoba J. Magnetic resonance imaging and spectroscopy in hepatic encephalopathy. J Clin Exp Hepatol. 2015;5(Suppl 1):S69–74. doi: 10.1016/j.jceh.2013.10.001Chavarria L., Cordoba J. Magnetic resonance imaging and spectroscopy in hepatic encephalopathy. J Clin Exp Hepatol. 2015;5(Suppl 1):S69–74. doi: 10.1016/j.jceh.2013.10.001Zeng G., Penninkilampi R., Chaganti J., Montagnese S., Brew B.J., Danta M. Meta-analysis of magnetic resonance spectroscopy in the diagnosis of hepatic encephalopathy. Neurology. 2020;94(11):e1147–e1156. doi: 10.1212/WNL.0000000000008899Zeng G., Penninkilampi R., Chaganti J., Montagnese S., Brew B.J., Danta M. Meta-analysis of magnetic resonance spectroscopy in the diagnosis of hepatic encephalopathy. Neurology. 2020;94(11):e1147–e1156. doi: 10.1212/WNL.0000000000008899Никонов Е.Л., Аксенов В.А. Печеночная энцефалопатия. Доказательная гастроэнтерология. 2017;6(4):25–31. https://doi.org/10.17116/dokgastro20176425-31Nikonov E.L., Aksenov V.A. Hepatic encephalopathy. Russian Journal of Evidence-Based Gastroenterology. 2017;6(4):25–31. (In Russ.). https://doi.org/10.17116/dokgastro20176425-31Ивашкин В.Т., Маевская М.В., Жаркова М.С., Жигалова С.Б., Киценко Е.А., Манукьян Г.В., Трухманов А.С., Маев И.В., Тихонов И.Н., Деева Т.А. Клинические рекомендации Российского общества по изучению печени и Российской гастроэнтерологической ассоциации по диагностике и лечению фиброза и цирроза печени и их осложнений. Российский журнал гастроэнтерологии, гепатологии, колопроктологии. 2021;31(6):56–102. https://doi.org/10.22416/1382-4376-2021-31-6-56-102Ivashkin V.T., Maevskaya M.V., Zharkova M.S., Zhigalova S.B., Kitsenko E.A., Manukyan G.V., Trukhmanov A.S., Maev I.V., Tikhonov I.N., Deeva T.A. Clinical Recommendations of the Russian Scientific Liver Society and Russian Gastroenterological Association on Diagnosis and Treatment of Liver Fibrosis, Cirrhosis and Their Complications. Russian Journal of Gastroenterology, Hepatology, Coloproctology. 2021;31(6):56–102. (In Russ.). https://doi.org/10.22416/1382-4376-2021-31-6-56-102

The authors declare that there are no conflicts of interest present.