Signs and Symptoms of Central Nervous System Involvement and Their Pathogenesis in COVID-19 According to The Clinical Data (Review)
https://doi.org/10.15360/1813-9779-2021-3-65-77
Abstract
Detailed clinical assessment of the central nervous system involvement in SARS-CoV-2 infection is relevant due to the low specificity of neurological manifestations, the complexity of evaluation of patient complaints, reduced awareness of the existing spectrum of neurological manifestations of COVID-19, as well as low yield of the neurological imaging.
The aim. To reveal the patterns of central nervous system involvement in COVID-19 and its pathogenesis based on clinical data.
Among more than 200 primary literature sources from various databases (Scopus, Web of Science, RSCI, etc.), 80 sources were selected for evaluation, of them 72 were published in the recent years (2016-2020). The criteria for exclusion of sources were low relevance and outdated information.
The clinical manifestations of central nervous system involvement in COVID-19 include smell (5-98% of cases) and taste disorders (6-89%), dysphonia (28%), dysphagia (19%), consciousness disorders (3-53%), headache (0-70%), dizziness (0-20%), and, in less than 3% of cases, visual impairment, hearing impairment, ataxia, seizures, stroke. Analysis of the literature data revealed the following significant mechanisms of the effects of highly contagious coronaviruses (including SARS-CoV-2) on the central nervous system: neurodegeneration (including cytokine- induced); cerebral thrombosis and thromboembolism; damage to the neurovascular unit; immune-mediated damage of nervous tissue, resulting in infection and allergy-induced demyelination.
The neurological signs and symptoms seen in COVID-19 such as headache, dizziness, impaired smell and taste, altered level of consciousness, bulbar disorders (dysphagia, dysphonia) have been examined. Accordingly, we discussed the possible routes of SARS-CoV-2 entry into the central nervous system and the mechanisms of nervous tissue damage.
Based on the literature analysis, a high frequency and variability of central nervous system manifestations of COVID-19 were revealed, and an important role of vascular brain damage and neurodegeneration in the pathogenesis of COVID-19 was highlighted.
About the Authors
N. V. TsyganRussian Federation
Nikolay V. Tsygan
mkr. Orlova roshcha, Gatchina, Leningrad region, 188300; 1 Akademika Kurchatova Sq., 123182 Moscow; 6 Akademika Lebedeva Str., 194044 Saint Petersburg
A. P. Trashkov
Russian Federation
Alexandr P. Trashkov
1 mkr. Orlova roshcha, Gatchina, Leningrad region, 188300; 1 Akademika Kurchatova Sq., 123182 Moscow
A. V. Ryabtsev
Russian Federation
Alexandr V. Ryabtsev
1 mkr. Orlova roshcha, Gatchina, Leningrad region, 188300; 1 Akademika Kurchatova Sq., 123182 Moscow; 6 Akademika Lebedeva Str., 194044 Saint Petersburg
V. A. Yakovleva
Russian Federation
Victoria A. Yakovleva
1 mkr. Orlova roshcha, Gatchina, Leningrad region, 188300; 1 Akademika Kurchatova Sq., 123182 Moscow; 6 Akademika Lebedeva Str., 194044 Saint Petersburg
A. L. Konevega
Russian Federation
Andrey L. Konevega
1 mkr. Orlova roshcha, Gatchina, Leningrad region, 188300; 1 Akademika Kurchatova Sq., 123182 Moscow
A. G. Vasiliev
Russian Federation
Andrey G. Vasiliev
2 Litovskaya Str., 194100 St. Petersburg
V. N. Tsygan
Russian Federation
Vasily N. Tsygan
6 Akademika Lebedeva Str., 194044 Saint Petersburg
M. M. Odinak
Russian Federation
Miroslav M. Odinak
6 Akademika Lebedeva Str., 194044 Saint Petersburg
I. V. Litvinenko
Russian Federation
Igor V Litvinenko
6 Akademika Lebedeva Str., 194044 Saint Petersburg
References
1. Moein S.T., Hashemian S.M., Mansourafshar B., Khorram-Tousi A., Tabarsi P, Doty R.L. Smell dysfunction: a biomarker for COVID-19. Int. Forum of Allergy Rhinol. 2020; 10 (8): 944-950. DOI: 10.1002/alr.22587. PMID: 32301284.
2. Mao L., Jin H., WangM., Hu Y., Chen S., He Q., Chang J., Hong C., Zhou Y., WangD., Miao X., Li Y., Hu B. Neurologic Manifestations of Hospitalized Patients With Coronavirus Disease 2019 in Wuhan, China. JAMA Neurology. 2020; 77 (6): 683-690. DOI: 10.1001/jamaneu-rol.2020.1127.
3. Yan C.H., Faraji F., Prajapati D.P, Ostrander B.T., DeConde A.S. Selfreported olfactory loss associates with outpatient clinical course in COVID-19. Int. Forum ofAllergy Rhinol. 2020; 10 (7): 821-831. DOI: 10.1002/alr.22592. PMID: 32329222.
4. Yan C.H., Faraji F., Prajapati D.P., Boone C.E., DeConde A.S. Association of chemosensory dysfunction and COVID-19 in patients presenting with influenza-like symptoms. Int. Forum ofAllergy Rhinol. 2020; 10 (7): 806-813. DOI: 10.1002/alr.22579. PMID: 32279441.
5. Lechien J.R., Chiesa-Estomba C.M., De Siati D.R., Horoi M., Le Bon S.D., Rodriguez A., Dequanter D., Blecic S., El Afia F, Distinguin L., Chekkoury-Idrissi Y., Hans S., Delgado I.L., Calvo-Henriquez C., La-vigne P, Falanga C., Barillari M.R., Cammaroto G., Khalife M., Leich P., Souchay C., Rossi C., Journe F., Hsieh J., Edjlali M., Carlier R., Ris L., Lovato A., De Filippis C., Coppee F., Fakhry N., Ayad T., Saussez S. Olfactory and gustatory dysfunctions as a clinical presentation of mild-to-moderate forms of the coronavirus disease (COVID-19): a multicenter European study. Eur. arch. otorhinolaryngol. 2020; 277 (8): 2251-2261. DOI: 10.1007/s00405-020-05965-1. PMID: 32253535.
6. Vaira L.A., Salzano G., Riu G.D. The importance of olfactory and gustatory disorders as early symptoms of coronavirus disease (COVID-19). Br. J. Oral Maxillofac. Surg. 2020; 58 (5): 615-616. DOI: 10.1016/j.bjoms.2020.04.024. PMID: 32362452.
7. Beltran-Corbellini A., Chico-Garcia J.L., Martinez-Poles J., Rodriguez-Jorge F., Natera-Villalba E., Gomez-Corral J., Gomez-Lopez A., Monreal E., Parra-Diaz P., Cortes-Cuevas J.L., Galan J.C., Fragola-Arnau C., Porta-Etessam J., Masjuan J., Alonso-Canovas A. Acute-onset smell and taste disorders in the context of COVID-19: a pilot multicentre polymerase chain reaction based case-control study. Eur. J. Neurol. 2020; 27 (9): 1738-1741. DOI: 10.1111/ene.14273. PMID: 32449247.
8. Lechien J.R., Chiesa-Estomba C.M., Place S., Laethem Y.V., Cabaraux P, Mat Q., Huet K., Plzak J., Horoi M., Hans S., Barillari M.R., Camma-roto G., Fakhry N., Martiny D., Ayad T., Jouffe L., Hopkins C., Saussez S. Clinical and epidemiological characteristics of 1420 European patients with mild-to-moderate coronavirus disease 2019. J. Intern. Med. 2020; 288 (3): 335-344. DOI: 10.1111/joim.13089. PMID: 32352202.
9. Tostmann A., Bradley J., Bousema T., Yiek W.K., Holwerda M., Bleeker-Rovers C., Oever J., Meijer C., Rahamat-Langendoen J., Hopman J., Geest-Blankert N. van der, Wertheim H. Strong associations and moderate predictive value of early symptoms for SARS-CoV-2 test positivity among healthcare workers, the Netherlands, March 2020. Euro. Surveill. 2020; 25 (16): 2000508. DOI: 10.2807/1560-7917.ES.2020.25.16.2000508. PMID: 32347200.
10. Aggarwal S., Garcia-Telles N., Aggarwal G., Lavie C., Lippi G., Henry B. M. Clinical features, laboratory characteristics, and outcomes of patients hospitalized with coronavirus disease 2019 (COVID-19): Early report from the United States. Diagnosis (Berl). 2020; 7 (2): 9196. DOI: 10.1515/dx-2020-0046. PMID: 32352401.
11. Kim G.U., Kim M.J., Ra S.H., Lee J., Bae S., Jung J., Kim S.H. Clinical characteristics of asymptomatic and symptomatic patients with mild COVID-19. Clin. Microbiol. Infect. 2020; 26 (7): 948.e1-948.e3. DOI: 10.1016/j.cmi.2020.04.040. PMID: 32360780.
12. Benezit F, Turnier P.L., Declerck C., Paille C., RevestM., Dubee V, Tat-tevin P, Arvieux C., Baldeyrou M., Chapplain J.M., ComacleP, Patrat-Delon S., Maillard A., PoinotM., Pronier C., Souala F., Thibault V, Abgueguen P, Cormier H., Delbos V, Chapelle M., Ducancelle A., Mahieu R., Rabier V, Rehaiem S., Vandamme Y., Biron C., Brochon J., Boutoille D., Chauveau M., Deschanvres C., Gaborit B.J., Jenvrin J., Lecomte R., Lefebvre M., Raffi F Utility of hyposmia and hypogeusia for the diagnosis of COVID-19. Lancet Infect. Dis. 2020; 20 (9): 1014-1015. DOI: 10.1016/S1473-3099 (20)30297-8. PMID: 32304632.
13. Martin-Sanz E., Riestra J., Yebra L., Larran A., Mancino F, Yanes-Diaz J., Garrote M., Colmenero M., Montiel E., Molina C., Moreno D., Rodriguez A., Monedero G., Sanz-Fernandez R., Gonzalez R., Esteban-Sanchez J. Prospective Study in 355 Patients With Suspected COVID-19 Infection: Value of Cough, Subjective Hyposmia, and Hy-pogeusia. Laryngoscope. 2020; 130 (11): 2674-2679. DOI: 10.1002/lary.28999. PMID: 32686164.
14. Nouchi A., Chastang J., Miyara M., Lejeune J., Soares A., Ibanez G., Saadoun D., Morelot-Panzini C., Similowski T., Amoura Z., Boddaert J., Caumes E., Bleibtreu A., Lorenzo A., Tubach F., Pourcher V Prevalence of hyposmia and hypogeusia in 390 COVID-19 hospitalized patients and outpatients: a cross-sectional study. Eur. J. Clin. Microbiol. Infect. Dis. 2020. DOI: 10.1007/s10096-020-04056-7. PMID: 33033955.
15. Liang Y., Xu J., Chu M., Mai J., Lai N., Tang W., Yang T., Zhang S., Guan C. , ZhongF, YangL., Liao G. Neurosensory dysfunction: A diagnostic marker of early COVID-19. Int. J. Infect. Dis. 2020; 98: 347-352. DOI: 10.1016/j.ijid.2020.06.086. PMID: 32615326.
16. Bagheri S.H., Asghari A., Farhadi M., Shamshiri A.R., Kabir A., Kam-rava S.K., Jalessi M., Mohebbi A., Alizadeh R., Honarmand A.A., Gha-lehbaghi B., Salimi A., Dehghani Firouzabadi F. Coincidence of COVID-19 epidemic and olfactory dysfunction outbreak in Iran. Med. J. Islam. Repub. Iran. 2020; 34: 62. DOI: 10.34171/mjiri.34.62. PMID: 32974228.
17. Mishra P, Gowda V, Dixit S., Kaushik M. Prevalence of New Onset Anosmia in COVID-19 Patients: Is The Trend Different Between European and Indian Population? Indian. J. Otolaryngol. Head. Neck. Surg. 2020; 72 (4): 484-487. DOI: 10.1007/s12070-020-01986-8. PMID: 32837939.
18. Giacomelli A., Pezzati L., Conti F, Bernacchia D., Siano M., Oreni L., Rusconi S., Gervasoni C., Ridolfo A.L., Rizzardini G., Antinori S., Galli M. Self-reported Olfactory and Taste Disorders in Patients With Severe Acute Respiratory Coronavirus 2 Infection: A Cross-sectional Study. Clin. Infect. Dis. 2020; 71 (15): 889-890. DOI: 10.1093/cid/ciaa330. PMID: 32215618.
19. Klopfenstein T., Kadiane-Oussou N.J., Toko L., Royer P.Y., Lepiller Q., Gendrin V, ZayetS. Features of anosmia in COVID-19. Med. Mal. Infect. 2020; 50 (5): 436-439. DOI: 10.1016/j.medmal.2020.04.006. PMID: 32305563.
20. Chiesa-Estomba C.M., Lechien J.R., Portillo-Mazal P, Martinez F, Cuauro-Sanchez J., Calvo-Henriquez C., Saussez S. Olfactory and gustatory dysfunctions in COVID-19. First reports of Latin-American ethnic patients. Am. J. Otolaryngol. 2020; 41 (5): 102605. DOI: 10.1016/j.amjoto.2020.102605. PMID: 32531619.
21. Chary E., Carsuzaa F, Trijolet J.P., Capitaine A.L., Roncato-Saberan M., FouetK., Cazenave-RoblotF, Catroux M., Allix-Beguec C., Dufour X. Prevalence and Recovery From Olfactory and Gustatory Dysfunctions in Covid-19 Infection: A Prospective Multicenter Study. Am. J. Rhinol. Allergy. 2020; 34 (5): 686-693. DOI: 10.1177/1945892420930954. PMID: 32527141.
22. Carignan A., Valiquette L., Grenier C., Musonera J.B., Nkengurutse D., Marcil-Heguy A., Vettese K., Marcoux D., Valiquette C., XiongW.T., Fortier PH., Genereux M., Pepin J. Anosmia and dysgeusia associated with SARS-CoV-2 infection: an age-matched case-control study. CMAJ. 2020; 192 (26): E702-E707. DOI: 10.1503/cmaj.200869. PMID: 32461325.
23. Zhao XY., Xu X.X., Yin H.S., Hu Q.M., Xiong T., Tang Y.Y., Yang A.Y., Yu B.P, Huang Z.P. Clinical characteristics of patients with 2019 corona-virus disease in a non-Wuhan area of Hubei Province, China: a retrospective study. BMC Infect. Dis. 2020; 20 (1): 311. DOI: 10.1186/s12879-020-05010-w. PMID: 32345226.
24. Garg S. Hospitalization Rates and Characteristics of Patients Hospitalized with Laboratory-Confirmed Coronavirus Disease 2019 — COVID-NET, 14 States, March 1-30, 2020. MMWR. Morb. Mortal. Wkly. Rep. 2020; 69. DOI: 10.15585/mmwr.mm6915e3. PMID: 32298251.
25. Li X., Xu S., Yu M., WangK., Tao Y., Zhou Y., Shi J., Zhou M., Wu B., Yang Z., Zhang C., Yue J., Zhang Z., Renz H., Liu X., Xie J., Xie M., Zhao J. Risk factors for severity and mortality in adult COVID-19 inpatients in Wuhan. J. Allergy Clin. Immunol. 2020; 146 (1): 110-118. DOI: 10.1016/j.jaci.2020.04.006. PMID: 32294485.
26. Godaert L., Proye E., Demoustier-Tampere D., Coulibaly P.S., Hequet F., DrameM. Clinical characteristics of older patients: The experience of a geriatric short-stay unit dedicated to patients with COVID-19 in France. J. Infect. 2020; 81 (1): e93-e94. DOI: 10.1016/j.jinf.2020.04.009. PMID: 32305489.
27. Helms J., Kremer S., Merdji H., Clere-Jehl R., Schenck M., Kummerlen C., Collange O., Boulay C., Fafi-Kremer S., Ohana M., Anheim M., Me-ziani F. Neurologic Features in Severe SARS-CoV-2 Infection. N. Eng. J. Med. 2020; 382 (23): 2268-2270. DOI: 10.1056/NEJMc2008597. PMID: 32294339.
28. Li K., Wohlford-Lenane C., Perlman S., Zhao J., Jewell A.K., Reznikov L.R., Gibson-Corley K.N., Meyerholz D.K., McCray P.B. Middle East Respiratory Syndrome Coronavirus Causes Multiple Organ Damage and Lethal Disease in Mice Transgenic for Human Dipeptidyl Peptidase 4. J. Infect. Dis. 2016; 213 (5): 712-722. DOI: 10.1093/infdis/jiv499. PMID: 26486634.
29. Netland J., Meyerholz D.K., Moore S., Cassell M., Perlman S. Severe Acute Respiratory Syndrome Coronavirus Infection Causes Neuronal Death in the Absence of Encephalitis in Mice Transgenic for Human ACE2. J. Virol. 2008; 82 (15): 7264-7275. DOI: 10.1128/JVI.00737-08. PMID: 18495771.
30. Fazzini E., Fleming J., Fahn S. Cerebrospinal fluid antibodies to coronavirus in patients with Parkinson’s disease. Mov. Disord. 1992; 7 (2): 153-158. DOI: 10.1002/mds.870070210. PMID: 1316552.
31. Dessau R.B., Lisby G., Frederiksen J.L. Coronaviruses in brain tissue from patients with multiple sclerosis. Acta Neuropathol. 2001; 101 (6): 601-604. DOI: 10.1007/s004010000331. PMID: 11515789.
32. Burks J.S., DeVald B.L., Janko vsky L.D., Gerdes J.C. Two coronaviruses isolated from central nervous system tissue of two multiple sclerosis patients. Science. 1980; 209 (4459): 933-934. DOI: 10.1126/science.7403860. PMID: 7403860.
33. TanakaR., Iwasaki Y., Koprowski H. Intracisternal virus-like particles in brain of a multiple sclerosis patient. J. Neurol. Sci. 1976; 28 (1): 121126. DOI: 10.1016/0022-510X(76)90053-8. PMID: 932771.
34. Salmi A., Ziola B., Hovi T., Reunanen M. Antibodies to coronaviruses OC43 and 229E in multiple sclerosis patients. Neurology. 1982; 32 (3): 292-295. DOI: 10.1212/wnl.32.3.292. PMID: 6278362.
35. Murray R.S., Brown B., Brian D., Cabirac G.F Detection of coronavirus RNA and antigen in multiple sclerosis brain. Ann. Neurol. 1992; 31 (5): 525-533. DOI: 10.1002/ana.410310511. PMID: 1596089
36. Chana-Cuevas P., Salles-Gandara P., Rojas-Fernandez A., Salinas-Re-bolledo C., Milan-Sole A. The Potential Role of SARS-COV-2 in the Pathogenesis of Parkinson’s Disease. Front Neurol. 2020; 11. DOI: 10.3389/fneur.2020.01044. PMID: 33041985.
37. Yeh E.A., Collins A., Cohen M.E., Duffner P.K., Faden H. Detection of coronavirus in the central nervous system of a child with acute disseminated encephalomyelitis. Pediatrics. 2004; 113 (1 Pt 1): e73-76. DOI: 10.1542/peds.113.1.e73. PMID: 14702500.
38. Liu K., Fang Y.Y., Deng Y., Liu W., Wang M.F, Ma J.P., Xiao W., Wang Y.N., ZhongM.H., Li C.H., Li G.C., Liu H.G. Clinical characteristics of novel coronavirus cases in tertiary hospitals in Hubei Province. Chin. Med. J. 2020; 133 (9): 1025-1031. DOI: 10.1097/CM9.0000000000000744. PMID: 32044814.
39. Xu X.W., Wu XX., JiangX.G., Xu K.J., YingL.J., Ma C.L., Li S.B., Wang H.Y., ZhangS., Gao H.N., ShengJ.F., Cai H.L., Qiu Y.Q., Li L.J. Clinical findings in a group of patients infected with the 2019 novel corona-virus (SARS-Cov-2) outside of Wuhan, China: retrospective case series. BMJ. 2020; 368. DOI: 10.1136/bmj.m606. PMID: 32075786.
40. Liu M., He P, Liu H.G., WangX.J., Li F.J., Chen S., Lin J., Chen P, Liu J.H., Li C.H. Clinical characteristics of 30 medical workers infected with new coronavirus pneumonia. Zhonghua Jie He He Hu Xi Za Zhi. 2020; 43 (0): E016. DOI: 10.3760/cma.j.issn.1001-0939.2020.0016. PMID: 32164090.
41. Chen N., Zhou M., Dong X., Qu J., Gong F., Han Y., Qiu Y., Wang J., Liu Y., Wei Y., Xia J., Yu T., Zhang X., Zhang L. Epidemiological and clinical characteristics of 99 cases of 2019 novel coronavirus pneumonia in Wuhan, China: a descriptive study. Lancet. 2020; 395 (10223): 507513. DOI: 10.1016/S0140-6736 (20)30211-7. PMID: 32007143.
42. Huang C., Wang Y., Li X., Ren L., Zhao J., Hu Y., Zhang L., Fan G., Xu J., Gu X., ChengZ., Yu T., Xia J., Wei Y., Wu W., Xie X., Yin W., Li H., Liu M., Xiao Y., Gao H., Guo L., Xie J., Wang G., Jiang R., Gao Z., Jin Q., Wang J., Cao B. Clinical features of patients infected with 2019 novel corona-virus in Wuhan, China. Lancet. 2020; 395 (10223): 497-506. DOI: 10.1016/S0140-6736(20)30183-5. PMID: 31986264.
43. Jin X., Lian J.S., Hu J.H., Gao J., ZhengL., Zhang Y.M., Hao S.R., Jia H.Y., Cai H., ZhangX.L., Yu G.D., Xu K.J., WangX.Y., Gu J.Q., ZhangS.Y., Ye C.Y., Jin C.L., Lu Y.F, Yu X., Yu XP., HuangJ.R., Xu K.L., Ni Q., Yu C.B., Zhu B., Li Y.T., Liu J., Zhao H., Zhang X., Yu L., Guo Y.Z., Su J.W., Tao J.J., Lang G.J., Wu X.X., Wu W.R., Qv T.T., XiangD.R., Yi P, Shi D., Chen Y., Ren Y., Qiu Y.Q., Li L.J., Sheng J., Yang Y. Epidemiological, clinical and virological characteristics of 74 cases of coronavirus-infected disease 2019 (COVID-19) with gastrointestinal symptoms. Gut. 2020; 69 (6): 1002-1009. DOI: 10.1136/gutjnl-2020-320926. PMID: 32213556.
44. Zhang X., Cai H., Hu J., Lian J., Gu J., Zhang S., Ye C., Lu Y., Jin C., Yu G., Jia H., Zhang Y., Sheng J., Li L., Yang Y. Epidemiological, clinical characteristics of cases of SARS-CoV-2 infection with abnormal imaging findings. Int. J. Infect. Dis. 2020; 94: 81-87. DOI: 10.1016/j.ijid.2020.03.040. PMID: 32205284.
45. Yan Y., Yang Y., WangF., Ren H., ZhangS., Shi X., Yu X., DongK. Clinical characteristics and outcomes of patients with severe covid-19 with diabetes. BMJ Open Diabetes Res. Care. 2020; 8 (1): e001343. DOI: 10.1136/bmjdrc-2020-001343. PMID: 32345579.
46. Duanmu Y., Bro wn I.P, Gibb W.R., Singh J., Matheson L.W., Blomkalns A.L., Govindarajan P. Characteristics of Emergency Department Patients With COVID-19 at a Single Site in Northern California: Clinical Observations and Public Health Implications. Acad. Emerg. Med. 2020; 27 (6): 505-509. DOI: 10.1111/acem.14003. PMID: 32344458.
47. Meng Y., Wu P, Lu W., Liu K., Ma K., HuangL., Cai J., Zhang H., Qin Y., Sun H., Ding W., Gui L., Wu P. Sex-specific clinical characteristics and prognosis of coronavirus disease-19 infection in Wuhan, China: A retrospective study of 168 severe patients. PLoS pathog. 2020; 16 (4): e1008520. DOI: 10.1371/journal.ppat.1008520. PMID: 32343745.
48. Chen Q., ZhengZ., Zhang C., ZhangX., Wu H., Wang J., Wang S., Zheng C. Clinical characteristics of 145 patients with corona virus disease 2019 (COVID-19) in Taizhou, Zhejiang, China. Infection. 2020; 1-9. DOI: 10.1007/s15010-020-01432-5. PMID: 32342479.
49. Kujawski SA., Wong K.K., Collins J.P, Epstein L., Killerby M.E., Midgley C.M., Abedi G.R., Ahmed N.S., Almendares O., Alvarez FN., Anderson K. N., Balter S., Barry V, Bartlett K., Beer K., Ben-Aderet MA., Benowitz I., Biggs H.M., Binder A.M., Black S.R., Bonin B., Bozio C.H., Brown C.M., Bruce H., Bryant-Genevier J., Budd A., Buell D., Bystritsky R., Cates J., CharlesE.M., Chatham-StephensK., CheaN., ChiouH., Christiansen D., Chu V, Cody S., Cohen M., ConnersE.E., CurnsA.T., Dasari V, Dawson P, DeSalvo T., Diaz G., DonahueM., Donovan S., DucaL.M., Erickson K., Esona M.D., Evans S., Falk J., Feldstein L.R., Fenstersheib M., Fischer M., Fisher R., Foo C., Fricchione M.J., Friedman O., Fry A., Galang R.R., Garcia M.M., Gerber S.I., Gerrard G., Ghinai I., Gounder P, Grein J., Grigg C., Gunzenhauser J.D., Gutkin G.I., HaddixM., Hall A.J., Han G.S., Harcourt J., Harriman K., Haupt T., Haynes A.K., Holshue M., Hoover C., Hunter J.C.,JacobsM.W.,JarashowC., JoshiK., Kamali T.,Kamili S., KimL.,Kim M., King J., Kirking H.L., Kita-Yarbro A., Klos R., Kobayashi M., Kocharian A., Komatsu K.K., Koppaka R., Layden J.E., Li Y., Lindquist S., Lindstrom S., Link-Gelles R., Lively J., Livingston M., Lo K., Lo J., Lu X., Lynch B., Ma-doff L., Malapati L., Marks G., Marlow M., Mathisen G.E., McClung N., McGovern O., McPherson T.D., Mehta M., Meier A., Mello L., Moon S., Morgan M., Moro R.N., Murray J., Murthy R., Novosad S., Oliver S.E., O’Shea J., Pacilli M., Paden C.R., Pallansch MA., Patel M., Patel S., Ped-raza I., Pillai S.K., Pindyck T., Pray I., Queen K., Quick N., Reese H., Reporter R., Rha B., Rhodes H., Robinson S., Robinson P, Rolfes MA., Routh JA., Rubin R., Rudman S.L., Sakthivel S.K., Scott S., Shepherd C., Shetty V., Smith E.A., Smith S., Stierman B., Stoecker W., Sunenshine R., Sy-San-tos R., Tamin A., Tao Y., Terashita D., Thornburg N.J., Tong S., Traub E., Tural A., Uehara A., Uyeki T.M., Vahey G., Verani J.R., Villarino E., Wallace M., Wang L., Watson J.T., WestercampM., Whitaker B., WilkersonS., WoodruffR.C., Wortham J.M., Wu T., Xie A., Yousaf A., Zahn M., Zhang J. Clinical and virologic characteristics of the first 12 patients with coronavirus disease 2019 (COVID-19) in the United States. Nat. Med. 2020; 26 (6): 861-868. DOI: 10.1038/s41591-020-0877-5. PMID: 32327757.
50. Zheng S., Fan J., Yu F, Feng B., Lou B., Zou Q., Xie G., Lin S., Wang R., YangX., Chen W., Wang Q., Zhang D., Liu Y., Gong R., Ma Z., Lu S., Xiao Y., Gu Y., Zhang J., Yao H., Xu K., Lu X., Wei G., Zhou J., Fang Q., Cai H., Qiu Y., Sheng J., Chen Y., Liang T. Viral load dynamics and disease severity in patients infected with SARS-CoV-2 in Zhejiang province, China, January-March 2020: retrospective cohort study. BMJ. 2020; 369. DOI: 10.1136/bmj.m1443. PMID: 32317267.
51. Zhou Y., Han T., Chen J., Hou C., Hua L., He S., Guo Y., Zhang S., Wang Y., Yuan J., Zhao C., Zhang J., Jia Q., Zuo X., Li J., Wang L., Cao Q., Jia E. Clinical and Autoimmune Characteristics of Severe and Critical Cases of COVID-19. Clin. Transl. Sci. DOI: 10.1111/cts.12805. PMID: 32315487.
52. Jie B., Liu X., Suo H., Qiao G., Zheng Q., Xu W., Liu Z. Clinical and Dynamic Computed Tomography Features of 24 Patients With Corona-virus Disease 2019. Can. Assoc. Radiol. J. 2020; 846537120918834. DOI: 10.1177/0846537120918834. PMID: 32306755.
53. Chen R., Liang W., Jiang M., Guan W., Zhan C., Wang T., Tang C., Sang L. , Liu J., Ni Z., Hu Y., Liu L., Shan H., Lei C., Peng Y., Wei L., Liu Y., Hu Y., Peng P, Wang J., Liu J., Chen Z., Li G., ZhengZ., Qiu S., Luo J., Ye C., Zhu S., Liu X., Cheng L., Ye F., Zheng J., Zhang N., Li Y., He J., Li S., Zhong N. Risk Factors of Fatal Outcome in Hospitalized Subjects With Coronavirus Disease 2019 From a Nationwide Analysis in China. Chest. 2020; 158 (1): 97-105. DOI: 10.1016/j.chest.2020.04.010. PMID: 32304772.
54. WangX., Liu W., Zhao J., Lu Y., WangX., Yu C., Hu S., Shen N., Liu W., Sun Z., Li W. Clinical characteristics of 80 hospitalized frontline medical workers infected with COVID-19 in Wuhan, China. J. Hosp. Infect. 2020. DOI: 10.1016/j.jhin.2020.04.019. PMID: 32302722.
55. Du W., Yu J., WangH., ZhangX., Zhang S., Li Q., ZhangZ. Clinical characteristics of COVID-19 in children compared with adults in Shandong Province, China. Infection. 2020; 1-8. DOI: 10.1007/s15010-020-01427-2. PMID: 32301099.
56. Ma J., Yin J., Qian Y., Wu Y. Clinical characteristics and prognosis in cancer patients with COVID-19: A single center’s retrospective study. J. Infect. 2020; 81 (2): 318-356. DOI: 10.1016/j.jinf.2020.04.006. PMID: 32298677.
57. Chen T., Dai Z., Mo P., Li X., Ma Z., Song S., Chen X., Luo M., Liang K. , Gao S., Zhang Y., Deng L., Xiong Y. Clinical Characteristics and Outcomes of Older Patients with Coronavirus Disease 2019 (COVID-19) in Wuhan, China: A Single-Centered, Retrospective Study. J. Gerontol. A. Bio.l Sci. Med. Sci. DOI: 10.1093/gerona/glaa089. PMID: 32279081.
58. ZhengF., Tang W., Li H., Huang Y.X., Xie Y.L., Zhou Z.G. Clinical characteristics of 161 cases of corona virus disease 2019 (COVID-19) in Changsha. Eur. Rev. Med. Pharmacol. Sci. 2020; 24 (6): 3404-3410. DOI: 10.26355/eurrev_202003_20711. PMID: 32271459.
59. WangL., He W., Yu X., Hu D., Bao M., Liu H., Zhou J., Jiang H. Corona-virus disease 2019 in elderly patients: Characteristics and prognostic factors based on 4-week follow-up. J. Infect. 2020; 80 (6): 639-645. DOI: 10.1016/j.jinf.2020.03.019. PMID: 32240670.
60. WangX., Fang J., Zhu Y., Chen L., DingF, Zhou R., Ge L., WangF, Chen Q. , Zhang Y., Zhao Q. Clinical characteristics of non-critically ill patients with novel coronavirus infection (COVID-19) in a Fangcang Hospital. Clin. Microbiol. Infect. 2020; 26 (8): 1063-1068. DOI: 10.1016/j.cmi.2020.03.032. PMID: 32251842.
61. Wan S., Xiang Y., Fang W., Zheng Y., Li B., Hu Y., Lang C., Huang D., Sun Q., Xiong Y., HuangX., Lv J., Luo Y., Shen L., Yang H., Huang G., Yang R. Clinical features and treatment of COVID-19 patients in northeast Chongqing. J. Med. Virol. 2020; 92 (7): 797-806. DOI: 10.1002/jmv.25783. PMID: 32198776.
62. Wang D., Hu B., Hu C., Zhu F., Liu X., Zhang J., Wang B., Xiang H., ChengZ., Xiong Y., Zhao Y., Li Y., WangX., PengZ. Clinical Characteristics of 138 Hospitalized Patients With 2019 Novel Coronavirus-In-fected Pneumonia in Wuhan, China. JAMA. 2020; 323 (11): 1061-1069. DOI: 10.1001/jama.2020.1585. PMID: 32031570.
63. Yu X., Sun X., Cui P., Pan H., Lin S., Han R., Jiang C., Fang Q., Kong D., Zhu Y., Zheng Y., GongX., Xiao W., Mao S., Jin B., Wu H., Fu C. Epidemiological and clinical characteristics of 333 confirmed cases with co-ronavirus disease 2019 in Shanghai, China. Transbound. Emerg. Dis. 2020; 67 (4): 1697-1707. DOI: 10.1111/tbed.13604. PMID: 32351037.
64. Alberici F, Delbarba E., Manenti C., Econimo L., Valerio F, Pola A., Maffei C. , Possenti S., Zambetti N., Moscato M., Venturini M., Affatato S., Gag-giotti M., Bossini N., Scolari F. A single center observational study of the clinical characteristics and short-term outcome of 20 kidney transplant patients admitted for SARS-CoV2 pneumonia. Kidney Int. 2020; 97 (6): 1083-1088. DOI: 10.1016/j.kint.2020.04.002. PMID: 32354634.
65. Yan J., Guo J., Fan C., Juan J., Yu X., Li J., FengL., Li C., Chen H., Qiao Y., LeiD., WangC., XiongG., Xiao F, He W., Pang Q., HuX., WangS., Chen D. ,ZhangY., PoonL.C., YangH. Coronavirus disease 2019 in pregnant women: a report based on 116 cases. Am. J. Obstet. Gynecol. 2020; 223 (1): 111.e1-111.e14. DOI: 10.1016/j.ajog.2020.04.014. PMID: 32335053.
66. Pereira M.R., Mohan S., Cohen D.J., Husain S.A., Dube G.K., Ratner L.E., Arcasoy S., Aversa M.M., Benvenuto L.J., Dadhania D.M., Kapur S., Dove L. M., Brown R.S., Rosenblatt R.E., Samstein B., UrielN., Farr MA., Satlin M. , Small C.B., Walsh T.J., Kodiyanplakkal R.P., Miko BA., Aaron J.G., Tsapepas D.S., Emond J.C., Verna E.C. COVID-19 in solid organ transplant recipients: Initial report from the US epicenter. Am. J. Transplant. 2020; 20 (7): 1800-1808. DOI: 10.1111/ajt.15941. PMID: 32330343.
67. Han C., Duan C., Zhang S., Spiegel B., Shi H., Wang W., Zhang L., Lin R. , Liu J., DingZ., Hou X Digestive Symptoms in COVID-19 Patients With Mild Disease Severity: Clinical Presentation, Stool Viral RNA Testing, and Outcomes. Am. J. Gastroenterol. 2020; 115 (6): 916-923. DOI: 10.14309/ajg.0000000000000664. PMID: 32301761.
68. Feng Y., Ling Y., Bai T., Xie Y., Huang J., Li J., Xiong W., Yang D., Chen R., Lu F, Lu Y., Liu X., Chen Y., Li X., Li Y., Summah H.D., Lin H., Yan J., Zhou M., Lu H., Qu J. COVID-19 with Different Severities: A Multicenter Study of Clinical Features. Am. J. Respir. Crit. Care Med. 2020; 201 (11): 1380-1388. DOI: 10.1164/rccm.202002-0445OC. PMID: 32275452.
69. Cao J., Tu W.J., Cheng W., Yu L., Liu Y.K., Hu X., Liu Q. Clinical Features and Short-term Outcomes of 102 Patients with Coronavirus Disease 2019 in Wuhan, China. Clin. Infect. Dis. 2020; 71 (15): 748-755. DOI: 10.1093/cid/ciaa243. PMID: 32239127.
70. Zhang L., Zhu F.., Xie L, Wang C., Wang J., Chen R., Jia P., Guan H.Q., Peng L., Chen Y., Peng P., Zhang P, Chu Q., Shen Q., Wang Y., Xu S.E, Zhao J.P., Zhou M. Clinical characteristics of COVID-19-infected cancer patients: a retrospective case study in three hospitals within Wuhan, China. Ann. Oncol.2020; 31 (7): 894-901. DOI: 10.1016/j.an-nonc.2020.03.296. PMID: 32224151.
71. Chu J., Yang N., Wei Y., Yue H., Zhang F, Zhao J., He L., Sheng G., Chen P, Li G., Wu S., Zhang B., Zhang S., Wang C., Miao X., Li J., Liu W., ZhangH. Clinical characteristics of 54 medical staff with COVID-19: A retrospective study in a single center in Wuhan, China. J. Med. Virol. 2020; 92 (7): 807-813. DOI: 10.1002/jmv.25793. PMID: 32222986.
72. Toljan K. Letter to the Editor Regarding the Viewpoint «Evidence of the COVID-19 Virus Targeting the CNS: Tissue Distribution, Host-Virus Interaction, and Proposed Neurotropic Mechanism». ACS Chem. Neurosci. 2020; 11 (8): 1192-1194. DOI: 10.1021/acschem-neuro.0c00174. PMID: 32233443.
73. Li Y., Bai W., Hashikawa T. The neuroinvasive potential of SARS-CoV2 may play a role in the respiratory failure of COVID-19 patients. J. Med.Virol. 2020. DOI: 10.1002/jmv.25728
74. Wu Y., Xu X., Chen Z., Duan J., Hashimoto K., Yang L., Liu C., Yang C. Nervous system involvement after infection with COVID-19 and other coronaviruses. Brain Behav. Immun. 2020; 87: 18-22. DOI: 10.1016/j.bbi.2020.03.031. PMID: 32240762.
75. Gusev E.I., Martyno v M.Yu., Boyko A.N., Voznyuk IA., Latsh N.Yu., Sivertseva S.A., Spirin N.N., Shamalov NA. Novel coronavirus infection (COVID-19) and nervous system involvement: pathogenesis, clinical manifestations, organization of neurological care. Zh. Nevrol. Psik-hiatr. Im. S. S. Korsakova. 2020; 120 (6): 7-16. DOI: 10.17116/jnevro20201200617. PMID: 32678542 [In Russ.].
76. Chen R., Wang K., Yu J., Howard D., French L., Chen Z., Wen C., Xu Z. The spatial and cell-type distribution of SARS-CoV-2 receptor ACE2 in human and mouse brain. bioRxiv. 2020. DOI: 10.1101/2020.04.07.030650.
77. Zairatyants O., Samsonova M., Mikhaleva L., Chernyaev A., Mishnev O., Krupnov N., Kalinin D. Pathological anatomy of COVID-19: Atlas. M.: GBU NIIOZMM DZM 2020. ISBN 978-5-907251-57-1 [In Russ.].
78. Politi L.S., Salsano E., Grimaldi M. Magnetic Resonance Imaging Alteration of the Brain in a Patient With Coronavirus Disease 2019 (COVID-19) and Anosmia. JAMA Neurol. 2020; 77 (8): 1028-1029. DOI: 10.1001/jamaneurol.2020.2125. PMID: 32469400.
79. TsyganN.V, OdinakM.M., Khubulava G.G., Tsygan VN., PeleshokA.S., AndreevR.V, KurasovE.S., Litvinenko I.VPostoperative cerebral dysfunction. Zh. Nevrol. Psikhiatr. Im. S. S. Korsakova. 2017; 117 (4): 34-39. DOI: 10.17116/jnevro20171174134-39. PMID: 28617376 (in Russian.
80. Tsygan N.V, Andreev R.V, Peleshok A.S., Kolomentsev S.V, Yakovleva V.A., Ryabtsev A.V., Gumennaya M.A., Litvinenko I.V. Perioperative stroke in heart valve surgery: pathogenesis, clinical findings, diagnosis, prevention, treatment. Zh. Nevrol. Psikhiatr. Im. S. S. Korsakova. 2018; 118 (4): 52-60. DOI: 10.17116/jnevro20181184152-60. PMID: 29863693 [In Russ.].
Review
For citations:
Tsygan N.V., Trashkov A.P., Ryabtsev A.V., Yakovleva V.A., Konevega A.L., Vasiliev A.G., Tsygan V.N., Odinak M.M., Litvinenko I.V. Signs and Symptoms of Central Nervous System Involvement and Their Pathogenesis in COVID-19 According to The Clinical Data (Review). General Reanimatology. 2021;17(3):65-77. https://doi.org/10.15360/1813-9779-2021-3-65-77