Skip to main content
Top
Published in: Virology Journal 1/2022

01-12-2022 | Herpes Virus | Research

Herpesvirus and neurological manifestations in patients with severe coronavirus disease

Authors: Vanessa Cristine de Souza Carneiro, Soniza Vieira Alves-Leon, Dmitry José de Santana Sarmento, Wagner Luis da Costa Nunes Pimentel Coelho, Otacilio da Cruz Moreira, Andreza Lemos Salvio, Carlos Henrique Ferreira Ramos, Carlos Henrique Ferreira Ramos Filho, Carla Augusta Barreto Marques, João Paulo da Costa Gonçalves, Luciane Almeida Amado Leon, Vanessa Salete de Paula

Published in: Virology Journal | Issue 1/2022

Login to get access

Abstract

Background

Certain clinical manifestations of coronavirus disease (COVID-19) mimic those associated with human herpesvirus (HHV) infection. In this study, we estimated the prevalence of herpesvirus in patients with COVID-19 and determined if coinfection is associated with poorer outcomes and neurological symptoms.

Methods

We analyzed samples of 53 patients diagnosed with COVID-19. The samples were evaluated for the presence of alphaherpesviruses, betaherpesviruses, and gammaherpesviruses, and the viral loads were quantified using quantitative polymerase chain reaction (qPCR) method.

Results

Among the patients, in 79.2% had detection at least one type of herpesvirus. HHV-6 (47.2%), cytomegalovirus (43.3%), and HHV-7 (39.6%) showed the highest detection rates. Patients with a high severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) load were more likely to show herpes simplex virus 1 detection (p = 0.037). Among patients coinfected with SARS-CoV-2 and HHVs, 26.4% showed central nervous system-associated neurological symptoms and herpetic manifestations. A statistically significant association was observed between neurological changes and HHV-6 detection (p = 0.034).

Conclusions

The findings showed a high prevalence of herpesvirus in patients with COVID-19. Furthermore, even though SARS-CoV-2 and HHV coinfection was not associated with poorer outcomes, the findings demonstrated the association between neurological symptoms and HHV-6 detection.
Appendix
Available only for authorised users
Literature
2.
go back to reference Chou SH-Y, Beghi E, Helbok. Global incidence of neurological manifestations among patients hospitalized with COVID-19-A report for the GCS-NeuroCOVID consortium and the ENERGY consortium. JAMA Netw Open. 2021;4(5):e2112131.PubMedPubMedCentralCrossRef Chou SH-Y, Beghi E, Helbok. Global incidence of neurological manifestations among patients hospitalized with COVID-19-A report for the GCS-NeuroCOVID consortium and the ENERGY consortium. JAMA Netw Open. 2021;4(5):e2112131.PubMedPubMedCentralCrossRef
3.
go back to reference Recalcati S. Cutaneous manifestations in COVID-19: a first perspective. J Eur Acad Dermatol Venereol. 2020;34(5):e212–3.PubMedCrossRef Recalcati S. Cutaneous manifestations in COVID-19: a first perspective. J Eur Acad Dermatol Venereol. 2020;34(5):e212–3.PubMedCrossRef
4.
go back to reference Sarı E, UygurKülcü N, Erdede O, UyurYalçın E, SezerYamanel RG. New-onset dizziness associated with COVID-19. Pediatr Neurol. 2021;115:72.PubMedCrossRef Sarı E, UygurKülcü N, Erdede O, UyurYalçın E, SezerYamanel RG. New-onset dizziness associated with COVID-19. Pediatr Neurol. 2021;115:72.PubMedCrossRef
5.
go back to reference Mao L, Jin H, Wang M, et al. Neurologic manifestations of hospitalized patients with Coronavirus disease 2019 in Wuhan, China. JAMA Neurol. 2020;77(6):683–90.PubMedCrossRef Mao L, Jin H, Wang M, et al. Neurologic manifestations of hospitalized patients with Coronavirus disease 2019 in Wuhan, China. JAMA Neurol. 2020;77(6):683–90.PubMedCrossRef
6.
7.
go back to reference Grandolfo M, Romita P, Bonamonte D, et al. Drug reaction with eosinophilia and systemic symptoms syndrome to hydroxychloroquine, an old drug in the spotlight in the COVID-19 era. Dermatol Ther. 2020;33(4):e13499.PubMedCrossRef Grandolfo M, Romita P, Bonamonte D, et al. Drug reaction with eosinophilia and systemic symptoms syndrome to hydroxychloroquine, an old drug in the spotlight in the COVID-19 era. Dermatol Ther. 2020;33(4):e13499.PubMedCrossRef
8.
go back to reference Llamas-Velasco M, Rodríguez-Jiménez P, Chicharro P, De Argila D, Muñoz-Hernández P, Daudén E. Reply to “Varicella-like exanthem as a specific COVID-19-associated skin manifestation: multicenter case series of 22 patients”—to consider varicella-like exanthem associated with COVID-19, virus varicella zoster and virus herpes simplex must be ruled out. J Am Acad Dermatol. 2020;83(3):e253–4.PubMedPubMedCentralCrossRef Llamas-Velasco M, Rodríguez-Jiménez P, Chicharro P, De Argila D, Muñoz-Hernández P, Daudén E. Reply to “Varicella-like exanthem as a specific COVID-19-associated skin manifestation: multicenter case series of 22 patients”—to consider varicella-like exanthem associated with COVID-19, virus varicella zoster and virus herpes simplex must be ruled out. J Am Acad Dermatol. 2020;83(3):e253–4.PubMedPubMedCentralCrossRef
9.
go back to reference Herlinge AL, Monteiro FLL, D’arc M, et al. Identification and characterisation of SARS-CoV-2 and Human alphaherpesvirus 1 from a productive coinfection in a fatal COVID-19 case. Mem Inst Oswaldo Cruz. 2022;116:e210176.CrossRef Herlinge AL, Monteiro FLL, D’arc M, et al. Identification and characterisation of SARS-CoV-2 and Human alphaherpesvirus 1 from a productive coinfection in a fatal COVID-19 case. Mem Inst Oswaldo Cruz. 2022;116:e210176.CrossRef
10.
go back to reference Xu R, Zhou Y, Cai L, et al. Co-reactivation of the human herpesvirus alpha subfamily (herpes simplex virus-1 and varicella zoster virus) in a critically ill patient with COVID-19. Br J Dermatol. 2020;183(6):1145–7.PubMedCrossRef Xu R, Zhou Y, Cai L, et al. Co-reactivation of the human herpesvirus alpha subfamily (herpes simplex virus-1 and varicella zoster virus) in a critically ill patient with COVID-19. Br J Dermatol. 2020;183(6):1145–7.PubMedCrossRef
11.
go back to reference Ramani A, Müller L, Ostermann PN, Gabriel E, Abida-Islam P, Müller-Schiffmann A, et al. SARS-CoV-2 targets neurons of 3D human brain organoids. EMBO J. 2020;39(20):e106230.PubMedPubMedCentralCrossRef Ramani A, Müller L, Ostermann PN, Gabriel E, Abida-Islam P, Müller-Schiffmann A, et al. SARS-CoV-2 targets neurons of 3D human brain organoids. EMBO J. 2020;39(20):e106230.PubMedPubMedCentralCrossRef
12.
go back to reference Aamodt AH, Høgestøl EA, Popperud TH, et al. Blood neurofilament light concentration at admittance: a potential prognostic marker in COVID-19. bioRxiv. 2020. Aamodt AH, Høgestøl EA, Popperud TH, et al. Blood neurofilament light concentration at admittance: a potential prognostic marker in COVID-19. bioRxiv. 2020.
13.
go back to reference Kremer S, Lersy F, Anheim M, et al. Neurologic and neuroimaging findings in patients with COVID-19: a retrospective multicenter study—a retrospective multicenter study. Neurology. 2020;95(13):e1868–82.PubMedCrossRef Kremer S, Lersy F, Anheim M, et al. Neurologic and neuroimaging findings in patients with COVID-19: a retrospective multicenter study—a retrospective multicenter study. Neurology. 2020;95(13):e1868–82.PubMedCrossRef
14.
go back to reference Espíndola OM, Brandão CO, Gomes YCP, et al. Cerebrospinal fluid findings in neurological diseases associated with COVID-19 and insights into mechanisms of disease development. Int J Infect Dis. 2021;102:155–62.PubMedCrossRef Espíndola OM, Brandão CO, Gomes YCP, et al. Cerebrospinal fluid findings in neurological diseases associated with COVID-19 and insights into mechanisms of disease development. Int J Infect Dis. 2021;102:155–62.PubMedCrossRef
15.
go back to reference Neumann B, Schmidbauer ML, Dimitriadis K, et al. Cerebrospinal fluid findings in COVID-19 patients with neurological symptoms. J Neurol Sci. 2020;418(117090):117090.PubMedPubMedCentralCrossRef Neumann B, Schmidbauer ML, Dimitriadis K, et al. Cerebrospinal fluid findings in COVID-19 patients with neurological symptoms. J Neurol Sci. 2020;418(117090):117090.PubMedPubMedCentralCrossRef
17.
go back to reference Walker PJ, Siddell SG, Lefkowitz EJ, et al. Changes to virus taxonomy and the International Code of Virus Classification and Nomenclature ratified by the International Committee on Taxonomy of Viruses (2019). Arch Virol. 2019;164(9):2417–29.PubMedCrossRef Walker PJ, Siddell SG, Lefkowitz EJ, et al. Changes to virus taxonomy and the International Code of Virus Classification and Nomenclature ratified by the International Committee on Taxonomy of Viruses (2019). Arch Virol. 2019;164(9):2417–29.PubMedCrossRef
18.
go back to reference Zarrouk K, Piret J, Boivin G. Herpesvirus DNA polymerases: structures, functions and inhibitors. Virus Res. 2017;234:177–92.PubMedCrossRef Zarrouk K, Piret J, Boivin G. Herpesvirus DNA polymerases: structures, functions and inhibitors. Virus Res. 2017;234:177–92.PubMedCrossRef
19.
go back to reference Hirsch MS. Herpes group virus infections in the compromised host. In: Rubin RH, Young LS, editors. Clinical approach to infection in the compromised host. Boston: Springer; 1994. p. 379–96.CrossRef Hirsch MS. Herpes group virus infections in the compromised host. In: Rubin RH, Young LS, editors. Clinical approach to infection in the compromised host. Boston: Springer; 1994. p. 379–96.CrossRef
20.
go back to reference Sousa IP Jr, Dos Santos FB, de Paula VS, et al. Viral and prion infections associated with central nervous system syndromes in Brazil. Viruses. 2021;13(7):1370.PubMedPubMedCentralCrossRef Sousa IP Jr, Dos Santos FB, de Paula VS, et al. Viral and prion infections associated with central nervous system syndromes in Brazil. Viruses. 2021;13(7):1370.PubMedPubMedCentralCrossRef
22.
go back to reference Sarigecili E, Arslan I, Ucar HK, Celik U. Pediatric anti-NMDA receptor encephalitis associated with COVID-19. Childs Nerv Syst. 2021;37(12):3919–22.PubMedCrossRef Sarigecili E, Arslan I, Ucar HK, Celik U. Pediatric anti-NMDA receptor encephalitis associated with COVID-19. Childs Nerv Syst. 2021;37(12):3919–22.PubMedCrossRef
23.
go back to reference Vasilevska V, Guest PC, Bernstein H-G, Schroeter ML, Geis C, Steiner J. Molecular mimicry of NMDA receptors may contribute to neuropsychiatric symptoms in severe COVID-19 cases. J Neuroinflamm. 2021;18(1):245.CrossRef Vasilevska V, Guest PC, Bernstein H-G, Schroeter ML, Geis C, Steiner J. Molecular mimicry of NMDA receptors may contribute to neuropsychiatric symptoms in severe COVID-19 cases. J Neuroinflamm. 2021;18(1):245.CrossRef
24.
go back to reference Kleinschmidt-DeMasters BK, Gilden DH. The expanding spectrum of herpesvirus infections of the nervous system. Brain Pathol. 2001;11(4):440–51.PubMedCrossRef Kleinschmidt-DeMasters BK, Gilden DH. The expanding spectrum of herpesvirus infections of the nervous system. Brain Pathol. 2001;11(4):440–51.PubMedCrossRef
25.
26.
go back to reference Donati D, Akhyani N, Fogdell-Hahn A, Cermelli C, Cassiani-Ingoni R, Vortmeyer A, et al. Detection of human herpesvirus-6 in mesial temporal lobe epilepsy surgical brain resections. Neurology. 2003;61(10):1405–11.PubMedCrossRef Donati D, Akhyani N, Fogdell-Hahn A, Cermelli C, Cassiani-Ingoni R, Vortmeyer A, et al. Detection of human herpesvirus-6 in mesial temporal lobe epilepsy surgical brain resections. Neurology. 2003;61(10):1405–11.PubMedCrossRef
27.
go back to reference Bartolini L, Theodore WH, Jacobson S, Gaillard WD. Infection with HHV-6 and its role in epilepsy. Epilepsy Res. 2019;153:34–9.PubMedCrossRef Bartolini L, Theodore WH, Jacobson S, Gaillard WD. Infection with HHV-6 and its role in epilepsy. Epilepsy Res. 2019;153:34–9.PubMedCrossRef
28.
go back to reference Nagel C-H, Döhner K, Fathollahy M, et al. Nuclear egress and envelopment of herpes simplex virus capsids analyzed with dual-color fluorescence HSV1(17+). J Virol. 2008;82(6):3109–24.PubMedCrossRef Nagel C-H, Döhner K, Fathollahy M, et al. Nuclear egress and envelopment of herpes simplex virus capsids analyzed with dual-color fluorescence HSV1(17+). J Virol. 2008;82(6):3109–24.PubMedCrossRef
29.
go back to reference Ferreira BIS, da Silva-Gomes NL, Coelho WLCNP, et al. Validation of a novel molecular assay to the diagnostic of COVID-19 based on real time PCR with high resolution melting. PLoS ONE. 2021;16(11):e0260087.PubMedPubMedCentralCrossRef Ferreira BIS, da Silva-Gomes NL, Coelho WLCNP, et al. Validation of a novel molecular assay to the diagnostic of COVID-19 based on real time PCR with high resolution melting. PLoS ONE. 2021;16(11):e0260087.PubMedPubMedCentralCrossRef
30.
go back to reference Lima LRP, da Silva AP, Schmidt-Chanasit J, de Paula VS. Diagnosis of human herpes virus 1 and 2 (HHV-1 and HHV-2): use of a synthetic standard curve for absolute quantification by real time polymerase chain reaction. Mem Inst Oswaldo Cruz. 2017;112(3):220–3.PubMedPubMedCentralCrossRef Lima LRP, da Silva AP, Schmidt-Chanasit J, de Paula VS. Diagnosis of human herpes virus 1 and 2 (HHV-1 and HHV-2): use of a synthetic standard curve for absolute quantification by real time polymerase chain reaction. Mem Inst Oswaldo Cruz. 2017;112(3):220–3.PubMedPubMedCentralCrossRef
31.
go back to reference Raposo JV, Alves ADR, Dos Santos da Silva A, et al. Multiplex qPCR facilitates identification of betaherpesviruses in patients with acute liver failure of unknown etiology. BMC Infect Dis. 2019;19(1):773.PubMedPubMedCentralCrossRef Raposo JV, Alves ADR, Dos Santos da Silva A, et al. Multiplex qPCR facilitates identification of betaherpesviruses in patients with acute liver failure of unknown etiology. BMC Infect Dis. 2019;19(1):773.PubMedPubMedCentralCrossRef
32.
go back to reference Raposo JV, Sarmento DJDS, Pinto RBDS, et al. Longitudinal study on oral shedding of human betaherpesviruses 6 and 7 in renal transplant recipients reveals active replication. J Oral Microbiol. 2020;12(1):1785801.PubMedPubMedCentralCrossRef Raposo JV, Sarmento DJDS, Pinto RBDS, et al. Longitudinal study on oral shedding of human betaherpesviruses 6 and 7 in renal transplant recipients reveals active replication. J Oral Microbiol. 2020;12(1):1785801.PubMedPubMedCentralCrossRef
33.
go back to reference de Oliveira LA, Spitz N, Martinelli KG, et al. Introduction of human gammaherpesvirus 8 genotypes A, B, and C into Brazil from multiple geographic regions. Virus Res. 2020;276(197828):197828. de Oliveira LA, Spitz N, Martinelli KG, et al. Introduction of human gammaherpesvirus 8 genotypes A, B, and C into Brazil from multiple geographic regions. Virus Res. 2020;276(197828):197828.
34.
go back to reference Fellner MD, Durand K, Rodriguez M, Irazu L, Alonio V, Picconi MA. Duplex realtime PCR method for Epstein–Barr virus and human DNA quantification: its application for post-transplant lymphoproliferative disorders detection. Braz J Infect Dis. 2014;18(3):271–80.PubMedCrossRef Fellner MD, Durand K, Rodriguez M, Irazu L, Alonio V, Picconi MA. Duplex realtime PCR method for Epstein–Barr virus and human DNA quantification: its application for post-transplant lymphoproliferative disorders detection. Braz J Infect Dis. 2014;18(3):271–80.PubMedCrossRef
35.
go back to reference Simonnet A, Engelmann I, Moreau A-S, et al. High incidence of Epstein–Barr virus, cytomegalovirus, and human-herpes virus-6 reactivations in critically ill patients with COVID-19. Infect Dis Now. 2021;51(3):296–9.PubMedPubMedCentralCrossRef Simonnet A, Engelmann I, Moreau A-S, et al. High incidence of Epstein–Barr virus, cytomegalovirus, and human-herpes virus-6 reactivations in critically ill patients with COVID-19. Infect Dis Now. 2021;51(3):296–9.PubMedPubMedCentralCrossRef
36.
go back to reference Hosomi S, Nishida Y, Fujiwara Y. The impact of human herpesviruses in clinical practice of inflammatory bowel disease in the era of COVID-19. Microorganisms. 2021;9(9):1870.PubMedPubMedCentralCrossRef Hosomi S, Nishida Y, Fujiwara Y. The impact of human herpesviruses in clinical practice of inflammatory bowel disease in the era of COVID-19. Microorganisms. 2021;9(9):1870.PubMedPubMedCentralCrossRef
37.
go back to reference Lopes AO, Lima LRP, Tozetto-Mendoza TR, et al. Low prevalence of human gammaherpesvirus 8 (HHV-8) infection among HIV-infected pregnant women in Rio De Janeiro, Brazil. J Matern Fetal Neonatal Med. 2021;34(20):3458–61.PubMedCrossRef Lopes AO, Lima LRP, Tozetto-Mendoza TR, et al. Low prevalence of human gammaherpesvirus 8 (HHV-8) infection among HIV-infected pregnant women in Rio De Janeiro, Brazil. J Matern Fetal Neonatal Med. 2021;34(20):3458–61.PubMedCrossRef
38.
go back to reference Le Balc’h P, Pinceaux K, Pronier C, Seguin P, Tadié J-M, Reizine F. Herpes simplex virus and cytomegalovirus reactivations among severe COVID-19 patients. Crit Care. 2020;24(1):530.PubMedPubMedCentralCrossRef Le Balc’h P, Pinceaux K, Pronier C, Seguin P, Tadié J-M, Reizine F. Herpes simplex virus and cytomegalovirus reactivations among severe COVID-19 patients. Crit Care. 2020;24(1):530.PubMedPubMedCentralCrossRef
39.
go back to reference Busani S, Bedini A, Biagioni E, Serio L, Tonelli R, Meschiari M, et al. Two fatal cases of acute liver failure due to HSV-1 infection in COVID-19 patients following immunomodulatory therapies. Clin Infect Dis. 2021;73(1):e252–5.PubMedCrossRef Busani S, Bedini A, Biagioni E, Serio L, Tonelli R, Meschiari M, et al. Two fatal cases of acute liver failure due to HSV-1 infection in COVID-19 patients following immunomodulatory therapies. Clin Infect Dis. 2021;73(1):e252–5.PubMedCrossRef
41.
go back to reference Seeßle J, Hippchen T, Schnitzler P, Gsenger J, Giese T, Merle U. High rate of HSV-1 reactivation in invasively ventilated COVID-19 patients: immunological findings. PLoS ONE. 2021;16(7):e0254129.PubMedPubMedCentralCrossRef Seeßle J, Hippchen T, Schnitzler P, Gsenger J, Giese T, Merle U. High rate of HSV-1 reactivation in invasively ventilated COVID-19 patients: immunological findings. PLoS ONE. 2021;16(7):e0254129.PubMedPubMedCentralCrossRef
42.
go back to reference Gold JE, Okyay RA, Licht WE, Hurley DJ. Investigation of long COVID prevalence and its relationship to Epstein–Barr virus reactivation. Pathogens. 2021;10(6):763.PubMedPubMedCentralCrossRef Gold JE, Okyay RA, Licht WE, Hurley DJ. Investigation of long COVID prevalence and its relationship to Epstein–Barr virus reactivation. Pathogens. 2021;10(6):763.PubMedPubMedCentralCrossRef
43.
go back to reference Ishida T, Kano Y, Mizukawa Y, Shiohara T. The dynamics of herpesvirus reactivations during and after severe drug eruptions: their relation to the clinical phenotype and therapeutic outcome. Allergy. 2014;69:798–805.PubMedCrossRef Ishida T, Kano Y, Mizukawa Y, Shiohara T. The dynamics of herpesvirus reactivations during and after severe drug eruptions: their relation to the clinical phenotype and therapeutic outcome. Allergy. 2014;69:798–805.PubMedCrossRef
45.
go back to reference Meeuwsen S, Persoon-Deen C, Bsibsi M, et al. Modulation of the cytokine network in human adult astrocytes by human herpesvirus-6A. J Neuroimmunol. 2005;164(1–2):37–47.PubMedCrossRef Meeuwsen S, Persoon-Deen C, Bsibsi M, et al. Modulation of the cytokine network in human adult astrocytes by human herpesvirus-6A. J Neuroimmunol. 2005;164(1–2):37–47.PubMedCrossRef
46.
go back to reference Patel R, Mohan A, Pokharel K, Pardi M. A rare case of human Herpesvirus 6 meningitis in an immunocompetent Asian male presented with a severe intractable headache. Cureus. 2021;13(5):e15331.PubMedPubMedCentral Patel R, Mohan A, Pokharel K, Pardi M. A rare case of human Herpesvirus 6 meningitis in an immunocompetent Asian male presented with a severe intractable headache. Cureus. 2021;13(5):e15331.PubMedPubMedCentral
47.
go back to reference Whitley RJ, Lakeman FD. Human herpesvirus 6 infection of the central nervous system: is it just a case of mistaken association? Clin Infect Dis. 2005;40(6):894–5.PubMedCrossRef Whitley RJ, Lakeman FD. Human herpesvirus 6 infection of the central nervous system: is it just a case of mistaken association? Clin Infect Dis. 2005;40(6):894–5.PubMedCrossRef
48.
go back to reference Cisneros-Herreros JM, Herrero-Romero M. Hepatitis por virus del grupo herpes. Enferm Infecc Microbiol Clin. 2006;24(6):392–8.PubMedCrossRef Cisneros-Herreros JM, Herrero-Romero M. Hepatitis por virus del grupo herpes. Enferm Infecc Microbiol Clin. 2006;24(6):392–8.PubMedCrossRef
49.
go back to reference Adane T, Getawa S. Cytomegalovirus seroprevalence among blood donors: a systematic review and meta-analysis. J Int Med Res. 2021;49(8):3000605211034656.PubMedCrossRef Adane T, Getawa S. Cytomegalovirus seroprevalence among blood donors: a systematic review and meta-analysis. J Int Med Res. 2021;49(8):3000605211034656.PubMedCrossRef
50.
go back to reference Souza MA, Passos AM, Treitinger A, Spada C. Seroprevalence of cytomegalovirus antibodies in blood donors in southern, Brazil. Rev Soc Bras Med Trop. 2010;43(4):359–61.PubMedCrossRef Souza MA, Passos AM, Treitinger A, Spada C. Seroprevalence of cytomegalovirus antibodies in blood donors in southern, Brazil. Rev Soc Bras Med Trop. 2010;43(4):359–61.PubMedCrossRef
51.
go back to reference Caselli E, Di Luca D. Molecular biology and clinical associations of Roseoloviruses human herpesvirus 6 and human herpesvirus 7. New Microbiol. 2007;30(3):173–87.PubMed Caselli E, Di Luca D. Molecular biology and clinical associations of Roseoloviruses human herpesvirus 6 and human herpesvirus 7. New Microbiol. 2007;30(3):173–87.PubMed
52.
go back to reference Linhares MI, Eizuru Y, Tateno S, Minamishima Y. Seroprevalence of human herpesvirus 6 infection in Brazilian and Japanese populations in the north-east of Brazil. Microbiol Immunol. 1991;35(11):1023–7.PubMedCrossRef Linhares MI, Eizuru Y, Tateno S, Minamishima Y. Seroprevalence of human herpesvirus 6 infection in Brazilian and Japanese populations in the north-east of Brazil. Microbiol Immunol. 1991;35(11):1023–7.PubMedCrossRef
53.
go back to reference de Freitas RB, Linhares AC. Prevalence of human herpesvirus 6 antibody in the population of Belém, Pará, northern Brazil. Trans R Soc Trop Med Hyg. 1997;91(5):538–40.PubMedCrossRef de Freitas RB, Linhares AC. Prevalence of human herpesvirus 6 antibody in the population of Belém, Pará, northern Brazil. Trans R Soc Trop Med Hyg. 1997;91(5):538–40.PubMedCrossRef
54.
go back to reference Chen N, Zhou M, Dong X, Qu J, Gong F, Han Y, et al. Epidemiological and clinical characteristics of 99 cases of 2019 novel coronavirus pneumonia in Wuhan, China: a descriptive study. Lancet. 2020;395(10223):507–13.PubMedPubMedCentralCrossRef Chen N, Zhou M, Dong X, Qu J, Gong F, Han Y, et al. Epidemiological and clinical characteristics of 99 cases of 2019 novel coronavirus pneumonia in Wuhan, China: a descriptive study. Lancet. 2020;395(10223):507–13.PubMedPubMedCentralCrossRef
55.
go back to reference Franceschini E, Cozzi-Lepri A, Santoro A, et al. Herpes simplex virus re-activation in patients with SARS-CoV-2 pneumonia: a prospective, observational study. Microorganisms. 2021;9(9):1896.PubMedPubMedCentralCrossRef Franceschini E, Cozzi-Lepri A, Santoro A, et al. Herpes simplex virus re-activation in patients with SARS-CoV-2 pneumonia: a prospective, observational study. Microorganisms. 2021;9(9):1896.PubMedPubMedCentralCrossRef
Metadata
Title
Herpesvirus and neurological manifestations in patients with severe coronavirus disease
Authors
Vanessa Cristine de Souza Carneiro
Soniza Vieira Alves-Leon
Dmitry José de Santana Sarmento
Wagner Luis da Costa Nunes Pimentel Coelho
Otacilio da Cruz Moreira
Andreza Lemos Salvio
Carlos Henrique Ferreira Ramos
Carlos Henrique Ferreira Ramos Filho
Carla Augusta Barreto Marques
João Paulo da Costa Gonçalves
Luciane Almeida Amado Leon
Vanessa Salete de Paula
Publication date
01-12-2022
Publisher
BioMed Central
Published in
Virology Journal / Issue 1/2022
Electronic ISSN: 1743-422X
DOI
https://doi.org/10.1186/s12985-022-01828-9

Other articles of this Issue 1/2022

Virology Journal 1/2022 Go to the issue