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PloS one2020; 15(6); e0232381; doi: 10.1371/journal.pone.0232381

Applications of minimally invasive multimodal telemetry for continuous monitoring of brain function and intracranial pressure in macaques with acute viral encephalitis.

Abstract: Alphaviruses such as Venezuelan equine encephalitis virus (VEEV) and Eastern equine encephalitis virus (EEEV) are arboviruses that can cause severe zoonotic disease in humans. Both VEEV and EEEV are highly infectious when aerosolized and can be used as biological weapons. Vaccines and therapeutics are urgently needed, but efficacy determination requires animal models. The cynomolgus macaque (Macaca fascicularis) provides a relevant model of human disease, but questions remain whether vaccines or therapeutics can mitigate CNS infection or disease in this model. The documentation of alphavirus encephalitis in animals relies on traditional physiological biomarkers and behavioral/neurological observations by veterinary staff; quantitative measurements such as electroencephalography (EEG) and intracranial pressure (ICP) can recapitulate underlying encephalitic processes. We detail a telemetry implantation method suitable for continuous monitoring of both EEG and ICP in awake macaques, as well as methods for collection and analysis of such data. We sought to evaluate whether changes in EEG/ICP suggestive of CNS penetration by virus would be seen after aerosol exposure of naïve macaques to VEEV IC INH9813 or EEEV V105 strains compared to mock-infection in a cohort of twelve adult cynomolgus macaques. Data collection ran continuously from at least four days preceding aerosol exposure and up to 50 days thereafter. EEG signals were processed into frequency spectrum bands (delta: [0.4 - 4Hz); theta: [4 - 8Hz); alpha: [8-12Hz); beta: [12-30] Hz) and assessed for viral encephalitis-associated changes against robust background circadian variation while ICP data was assessed for signal fidelity, circadian variability, and for meaningful differences during encephalitis. Results indicated differences in delta, alpha, and beta band magnitude in infected macaques, disrupted circadian rhythm, and proportional increases in ICP in response to alphavirus infection. This novel enhancement of the cynomolgus macaque model offers utility for timely determination of onset, severity, and resolution of encephalitic disease and for the evaluation of vaccine and therapeutic candidates.
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Publication Date: 2020-06-25 PubMed ID: 32584818PubMed Central: PMC7316240DOI: 10.1371/journal.pone.0232381Google Scholar: Lookup
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Summary

This research summary has been generated with artificial intelligence and may contain errors and omissions. Refer to the original study to confirm details provided. Submit correction.

This research paper presents a new method for the continuous telemetry monitoring of brain function and intracranial pressure in macaques infected with acute viral encephalitis, specifically from alphaviruses like the Venezuelan equine encephalitis virus (VEEV) and Eastern equine encephalitis virus (EEV). The study provides evidence of changes in electroencephalography (EEG) and intracranial pressure (ICP) suggestive of central nervous system virus penetration. The findings represent an enhancement to the use of the cynomolgus macaque model in the research of encephalitic disease, and the search for vaccines and therapeutics.

Research Objectives and Methods

  • The primary objective of the study was to develop a minimally invasive telemetry method that could continuously monitor EEG and ICP in awake macaques – a model organism commonly used in researching human diseases. This continuous monitoring was expected to provide better understanding of the manifestations of alphavirus encephalitis in the central nervous system.
  • The researchers evaluated the effects of infection from aerosolized VEEV and EEEV on the EEG and ICP of macaques.
  • The study involved exposing macaques to the VEEV and EEEV. Controls were mock-infected. Data was collected continually from four days prior to exposure to up to 50 days after exposure.

Data Collection and Analysis

  • EEG signals were categorized into four bands: delta, theta, alpha, and beta, and analyzed for changes associated with viral encephalitis against robust background circadian variation.
  • ICP data was assessed for signal reliability, circadian variability, and any significant differences during the stages of encephalitis.

Results and Implications

  • The study found notable differences in delta, alpha, and beta band magnitude in the EEG readouts from infected macaques. Additionally, circadian rhythm disruptions and increases in ICP were observed in response to alphavirus infection.
  • The tailored telemetry implantation method and the observed changes in brain function and ICP in the macaques provide an improved way to understand and research the progress and resolution of encephalitic diseases.
  • Furthermore, they offer a useful model for evaluating potential vaccines and treatment options for dangerous zoonotic diseases caused by alphaviruses.

Cite This Article

APA
Ma H, Lundy JD, Cottle EL, O'Malley KJ, Trichel AM, Klimstra WB, Hartman AL, Reed DS, Teichert T. (2020). Applications of minimally invasive multimodal telemetry for continuous monitoring of brain function and intracranial pressure in macaques with acute viral encephalitis. PLoS One, 15(6), e0232381. https://doi.org/10.1371/journal.pone.0232381

Publication

PloS one
ISSN: 1932-6203
NlmUniqueID: 101285081
Country: United States
Language: English
Volume: 15
Issue: 6
Pages: e0232381
PII: e0232381

Researcher Affiliations

Ma, Henry
  • Center for Vaccine Research, University of Pittsburgh, Pittsburgh, Pennsylvania, United States of America.
Lundy, Jeneveve D
  • Center for Vaccine Research, University of Pittsburgh, Pittsburgh, Pennsylvania, United States of America.
Cottle, Emily L
  • Center for Vaccine Research, University of Pittsburgh, Pittsburgh, Pennsylvania, United States of America.
O'Malley, Katherine J
  • Center for Vaccine Research, University of Pittsburgh, Pittsburgh, Pennsylvania, United States of America.
Trichel, Anita M
  • Center for Vaccine Research, University of Pittsburgh, Pittsburgh, Pennsylvania, United States of America.
Klimstra, William B
  • Center for Vaccine Research, University of Pittsburgh, Pittsburgh, Pennsylvania, United States of America.
Hartman, Amy L
  • Center for Vaccine Research, University of Pittsburgh, Pittsburgh, Pennsylvania, United States of America.
Reed, Douglas S
  • Center for Vaccine Research, University of Pittsburgh, Pittsburgh, Pennsylvania, United States of America.
  • Department of Immunology, University of Pittsburgh School of Medicine, Pittsburgh, Pennsylvania, United States of America.
Teichert, Tobias
  • Department of Psychiatry, University of Pittsburgh School of Medicine, Pittsburgh, Pennsylvania, United States of America.
  • Department of Bioengineering, University of Pittsburgh, Pittsburgh, Pennsylvania, United States of America.

MeSH Terms

  • Alphavirus / isolation & purification
  • Alphavirus / pathogenicity
  • Alphavirus Infections / metabolism
  • Alphavirus Infections / pathology
  • Animals
  • Biomarkers / metabolism
  • Brain / physiology
  • Circadian Rhythm
  • Disease Models, Animal
  • Electroencephalography / methods
  • Encephalitis, Viral / metabolism
  • Encephalitis, Viral / pathology
  • Female
  • Intracranial Pressure / physiology
  • Macaca
  • Male
  • Severity of Illness Index
  • Telemetry

Conflict of Interest Statement

The authors have declared that no competing interests exist. The funders had no role in the design of the study; in the collection, analyses, or interpretation of data; in the writing of the manuscript, or in the decision to publish the results. None of the submitted work was carried out in the presence of any personal, professional, or financial relationships that could be potentially construed as a conflict of interest; none of the authors listed owns controlling interest in any of the vendors or suppliers listed in this manuscript.

References

This article includes 65 references
  1. Lury KM, Castillo M. Eastern equine encephalitis: CT and MRI findings in one case.. Emerg Radiol 2004 Aug;11(1):46-8.
    doi: 10.1007/s10140-004-0350-7pubmed: 15309665google scholar: lookup
  2. DE WEBSTER HF. Eastern equine encephalomyelitis in Massachusetts; report of two cases, diagnosed serologically, with complete clinical recovery.. N Engl J Med 1956 Aug 9;255(6):267-70.
    doi: 10.1056/NEJM195608092550604pubmed: 13348851google scholar: lookup
  3. Reed DS, Lackemeyer MG, Garza NL, Norris S, Gamble S, Sullivan LJ, Lind CM, Raymond JL. Severe encephalitis in cynomolgus macaques exposed to aerosolized Eastern equine encephalitis virus.. J Infect Dis 2007 Aug 1;196(3):441-50.
    doi: 10.1086/519391pubmed: 17597459google scholar: lookup
  4. Lennette EH, Koprowski H. Human infection with Venezuelan equine encephalomyelitis virus: a report on eight cases of infection acquired in the laboratory.. Journal of the American Medical Association 1943;123(17):1088–95.
  5. KOPROWSKI H, COX HR. Human laboratory infection with Venezuelan equine encephalomyelitis virus; report of four cases.. N Engl J Med 1947 May 1;236(18):647-54.
    doi: 10.1056/NEJM194705012361801pubmed: 20295009google scholar: lookup
  6. Kehn-Hall K, Narayanan A, Lundberg L, Sampey G, Pinkham C, Guendel I, Van Duyne R, Senina S, Schultz KL, Stavale E, Aman MJ, Bailey C, Kashanchi F. Modulation of GSK-3β activity in Venezuelan equine encephalitis virus infection.. PLoS One 2012;7(4):e34761.
    pmc: PMC3319612pubmed: 22496857doi: 10.1371/journal.pone.0034761google scholar: lookup
  7. Moran GJ. Threats in bioterrorism. II: CDC category B and C agents.. Emerg Med Clin North Am 2002 May;20(2):311-30.
    doi: 10.1016/s0733-8627(01)00003-7pubmed: 12120481google scholar: lookup
  8. Burns DL. Licensure of vaccines using the Animal Rule.. Curr Opin Virol 2012 Jun;2(3):353-6.
    doi: 10.1016/j.coviro.2012.01.004pubmed: 22709520google scholar: lookup
  9. US Food and Drug Administration. Guidance for industry: product development under the animal rule. Draft Guidance 2014.. .
  10. Gronvall GK, Trent D, Borio L, Brey R, Nagao L. The FDA animal efficacy rule and biodefense.. Nat Biotechnol 2007 Oct;25(10):1084-7.
    doi: 10.1038/nbt1007-1084pubmed: 17921984google scholar: lookup
  11. LIVESAY HR. Isolation of eastern equine encephalomyelitis virus from naturally infected monkey (Macacus philippinensis).. J Infect Dis 1949 May-Jun;84(3):306-9.
    doi: 10.1093/infdis/84.3.306pubmed: 18127637google scholar: lookup
  12. Reed DS, Lind CM, Sullivan LJ, Pratt WD, Parker MD. Aerosol infection of cynomolgus macaques with enzootic strains of venezuelan equine encephalitis viruses.. J Infect Dis 2004 Mar 15;189(6):1013-7.
    doi: 10.1086/382281pubmed: 14999604google scholar: lookup
  13. Reed DS, Larsen T, Sullivan LJ, Lind CM, Lackemeyer MG, Pratt WD, Parker MD. Aerosol exposure to western equine encephalitis virus causes fever and encephalitis in cynomolgus macaques.. J Infect Dis 2005 Oct 1;192(7):1173-82.
    doi: 10.1086/444397pubmed: 16136459google scholar: lookup
  14. Ma H, Lundy JD, O'Malley KJ, Klimstra WB, Hartman AL, Reed DS. Electrocardiography Abnormalities in Macaques after Infection with Encephalitic Alphaviruses.. Pathogens 2019 Nov 16;8(4).
    pmc: PMC6969904pubmed: 31744158doi: 10.3390/pathogens8040240google scholar: lookup
  15. Pratt WD, Gibbs P, Pitt ML, Schmaljohn AL. Use of telemetry to assess vaccine-induced protection against parenteral and aerosol infections of Venezuelan equine encephalitis virus in non-human primates.. Vaccine 1998 May-Jun;16(9-10):1056-64.
    doi: 10.1016/s0264-410x(97)00192-8pubmed: 9682359google scholar: lookup
  16. Aréchiga-Ceballos N, Aguilar-Setién A. Alphaviral equine encephalomyelitis (Eastern, Western and Venezuelan).. Rev Sci Tech 2015 Aug;34(2):491-501.
    doi: 10.20506/rst.34.2.2374pubmed: 26601451google scholar: lookup
  17. Baron S. Alphaviruses (Togaviridae) and Flaviviruses (Flaviviridae)—Medical Microbiology.. University of Texas Medical Branch at Galveston; 1996.
  18. Cavadini G, Petrzilka S, Kohler P, Jud C, Tobler I, Birchler T, Fontana A. TNF-alpha suppresses the expression of clock genes by interfering with E-box-mediated transcription.. Proc Natl Acad Sci U S A 2007 Jul 31;104(31):12843-8.
    pmc: PMC1937554pubmed: 17646651doi: 10.1073/pnas.0701466104google scholar: lookup
  19. Majde JA, Krueger JM. Links between the innate immune system and sleep.. J Allergy Clin Immunol 2005 Dec;116(6):1188-98.
    doi: 10.1016/j.jaci.2005.08.005pubmed: 16337444google scholar: lookup
  20. Opp MR, Kapás L, Toth LA. Cytokine involvement in the regulation of sleep.. Proc Soc Exp Biol Med 1992 Oct;201(1):16-27.
    doi: 10.3181/00379727-201-43474pubmed: 1382300google scholar: lookup
  21. Yoshida H, Peterfi Z, García-García F, Kirkpatrick R, Yasuda T, Krueger JM. State-specific asymmetries in EEG slow wave activity induced by local application of TNFalpha.. Brain Res 2004 May 29;1009(1-2):129-36.
    pubmed: 15120590doi: 10.1016/j.brainres.2004.02.055google scholar: lookup
  22. Deresiewicz RL, Thaler SJ, Hsu L, Zamani AA. Clinical and neuroradiographic manifestations of eastern equine encephalitis.. N Engl J Med 1997 Jun 26;336(26):1867-74.
    doi: 10.1056/NEJM199706263362604pubmed: 9197215google scholar: lookup
  23. Wendell LC, Potter NS, Roth JL, Salloway SP, Thompson BB. Successful management of severe neuroinvasive eastern equine encephalitis.. Neurocrit Care 2013 Aug;19(1):111-5.
    doi: 10.1007/s12028-013-9822-5pubmed: 23733173google scholar: lookup
  24. Garlick J, Lee TJ, Shepherd P, Linam WM, Pastula DM, Weinstein S, Schexnayder SM. Locally Acquired Eastern Equine Encephalitis Virus Disease, Arkansas, USA.. Emerg Infect Dis 2016 Dec;22(12):2216-2217.
    doi: 10.3201/eid2212.160844pmc: PMC5189158pubmed: 27662563google scholar: lookup
  25. National Research Council. Guide for the care and use of laboratory animals. National Academies, Washington, DC.
  26. Aebersold P. FDA experience with medical countermeasures under the animal rule.. Advances in preventive medicine 2011;2012.
  27. Homan RW. The 10–20 electrode system and cerebral location.. American Journal of EEG Technology 1988;28(4):269–79.
  28. Lackemeyer MG, Kok-Mercado Fd, Wada J, Bollinger L, Kindrachuk J, Wahl-Jensen V, Kuhn JH, Jahrling PB. ABSL-4 aerobiology biosafety and technology at the NIH/NIAID integrated research facility at Fort Detrick.. Viruses 2014 Jan 7;6(1):137-50.
    doi: 10.3390/v6010137pmc: PMC3917435pubmed: 24402304google scholar: lookup
  29. Reed DS, Bethel LM, Powell DS, Caroline AL, Hartman AL. Differences in aerosolization of Rift Valley fever virus resulting from choice of inhalation exposure chamber: implications for animal challenge studies.. Pathog Dis 2014 Jul;71(2):227-33.
    doi: 10.1111/2049-632X.12157pmc: PMC4809971pubmed: 24532259google scholar: lookup
  30. Bohannon JK, Honko AN, Reeder RJ, Cooper K, Byrum R, Bollinger L, Kuhn JH, Wada J, Qin J, Jahrling PB, Lackemeyer MG. Comparison of respiratory inductive plethysmography versus head-out plethysmography for anesthetized nonhuman primates in an animal biosafety level 4 facility.. Inhal Toxicol 2016 Dec;28(14):670-676.
    doi: 10.1080/08958378.2016.1247199pubmed: 27919178google scholar: lookup
  31. Bowling JD, O'Malley KJ, Klimstra WB, Hartman AL, Reed DS. A Vibrating Mesh Nebulizer as an Alternative to the Collison Three-Jet Nebulizer for Infectious Disease Aerobiology.. Appl Environ Microbiol 2019 Sep 1;85(17).
    doi: 10.1128/AEM.00747-19pmc: PMC6696971pubmed: 31253680google scholar: lookup
  32. Delorme A, Makeig S. EEGLAB: an open source toolbox for analysis of single-trial EEG dynamics including independent component analysis.. J Neurosci Methods 2004 Mar 15;134(1):9-21.
    doi: 10.1016/j.jneumeth.2003.10.009pubmed: 15102499google scholar: lookup
  33. Molaee-Ardekani B, Senhadji L, Shamsollahi MB, Wodey E, Vosoughi-Vahdat B. Delta waves differently modulate high frequency components of EEG oscillations in various unconsciousness levels.. Annu Int Conf IEEE Eng Med Biol Soc 2007;2007:1294-7.
    pmc: PMC2774447pubmed: 18002200doi: 10.1109/iembs.2007.4352534google scholar: lookup
  34. Brandenberger G, Ehrhart J, Piquard F, Simon C. Inverse coupling between ultradian oscillations in delta wave activity and heart rate variability during sleep.. Clin Neurophysiol 2001 Jun;112(6):992-6.
    doi: 10.1016/s1388-2457(01)00507-7pubmed: 11377256google scholar: lookup
  35. Feinberg I, March JD, Floyd TC, Jimison R, Bossom-Demitrack L, Katz PH. Homeostatic changes during post-nap sleep maintain baseline levels of delta EEG.. Electroencephalogr Clin Neurophysiol 1985 Aug;61(2):134-7.
    doi: 10.1016/0013-4694(85)91051-xpubmed: 2410222google scholar: lookup
  36. Gwin JT, Ferris DP. Beta- and gamma-range human lower limb corticomuscular coherence.. Front Hum Neurosci 2012;6:258.
    doi: 10.3389/fnhum.2012.00258pmc: PMC3438504pubmed: 22973219google scholar: lookup
  37. Otomo E. Beta wave activity in the electroencephalogram in cases of coma due to acute brain-stem lesions.. J Neurol Neurosurg Psychiatry 1966 Oct;29(5):383-90.
    doi: 10.1136/jnnp.29.5.383pmc: PMC496066pubmed: 5926461google scholar: lookup
  38. Krause G, Ullsperger P, Beyer L, Gille HG. Changes in EEG power density spectrum during static muscle work.. Eur J Appl Physiol Occup Physiol 1983;51(1):61-6.
    doi: 10.1007/BF00952538pubmed: 6684033google scholar: lookup
  39. Rachalski A, Authier S, Bassett L, Pouliot M, Tremblay G, Mongrain V. Sleep electroencephalographic characteristics of the Cynomolgus monkey measured by telemetry.. J Sleep Res 2014 Dec;23(6):619-627.
    doi: 10.1111/jsr.12189pubmed: 25109588google scholar: lookup
  40. Authier S, Paquette D, Gauvin D, Sammut V, Fournier S, Chaurand F, Troncy E. Video-electroencephalography in conscious non human primate using radiotelemetry and computerized analysis: refinement of a safety pharmacology model.. J Pharmacol Toxicol Methods 2009 Jul-Aug;60(1):88-93.
    doi: 10.1016/j.vascn.2008.12.003pubmed: 19414069google scholar: lookup
  41. Ferri R, Cosentino FI, Elia M, Musumeci SA, Marinig R, Bergonzi P. Relationship between Delta, Sigma, Beta, and Gamma EEG bands at REM sleep onset and REM sleep end.. Clin Neurophysiol 2001 Nov;112(11):2046-52.
    doi: 10.1016/s1388-2457(01)00656-3pubmed: 11682342google scholar: lookup
  42. Uchida S, Maloney T, Feinberg I. Sigma (12-16 Hz) and beta (20-28 Hz) EEG discriminate NREM and REM sleep.. Brain Res 1994 Oct 3;659(1-2):243-8.
    doi: 10.1016/0006-8993(94)90886-9pubmed: 7820669google scholar: lookup
  43. Benoit O, Daurat A, Prado J. Slow (0.7-2 Hz) and fast (2-4 Hz) delta components are differently correlated to theta, alpha and beta frequency bands during NREM sleep.. Clin Neurophysiol 2000 Dec;111(12):2103-6.
    doi: 10.1016/s1388-2457(00)00470-3pubmed: 11090758google scholar: lookup
  44. Zacks MA, Paessler S. Encephalitic alphaviruses.. Vet Microbiol 2010 Jan 27;140(3-4):281-6.
    doi: 10.1016/j.vetmic.2009.08.023pmc: PMC2814892pubmed: 19775836google scholar: lookup
  45. Badar Z, Thakur D, Hameedi. CT and MRI findings in a pediatric case of eastern equine encephalitis.. Pediatric Infectious Disease 2014;6(2):66–71.
  46. Taha AR. Central Nervous System Infection. In Highly Infectious Diseases in Critical Care 2020. (pp. 147–174). Springer, Cham.
  47. Silverman MA, Misasi J, Smole S, Feldman HA, Cohen AB, Santagata S, McManus M, Ahmed AA. Eastern equine encephalitis in children, Massachusetts and New Hampshire,USA, 1970-2010.. Emerg Infect Dis 2013 Feb;19(2):194-201; quiz 352.
    doi: 10.3201/eid1902.120039pmc: PMC3559032pubmed: 23343480google scholar: lookup
  48. Vacca V. Encephalitis in adults: Outcomes in critical care.. Nursing Critical Care 2016;11(2):14–22.
  49. Solomon T, Whitley RJ. Arthropod-borne viral encephalitides. Infections of the central nervous system, Second edition Philidelphia, PA: Lippincott Williams and Wilkins; 2004.
  50. Albeck MJ, Børgesen SE, Gjerris F, Schmidt JF, Sørensen PS. Intracranial pressure and cerebrospinal fluid outflow conductance in healthy subjects.. J Neurosurg 1991 Apr;74(4):597-600.
    doi: 10.3171/jns.1991.74.4.0597pubmed: 2002373google scholar: lookup
  51. Chapman PH, Cosman ER, Arnold MA. The relationship between ventricular fluid pressure and body position in normal subjects and subjects with shunts: a telemetric study.. Neurosurgery 1990 Feb;26(2):181-9.
    doi: 10.1097/00006123-199002000-00001pubmed: 2308665google scholar: lookup
  52. Masuda H, Ogata T, Kikuchi K. Physiological changes during temporary occlusion of the superior vena cava in cynomolgus monkeys.. Ann Thorac Surg 1989 Jun;47(6):890-6.
    doi: 10.1016/0003-4975(89)90030-1pubmed: 2757446google scholar: lookup
  53. Kim CY, Han SS. Characteristics of home cage locomotion in cynomolgus monkeys.. J Toxicol Sci 2006 Dec;31(5):529-35.
    doi: 10.2131/jts.31.529pubmed: 17202765google scholar: lookup
  54. Lawley JS, Petersen LG, Howden EJ, Sarma S, Cornwell WK, Zhang R, Whitworth LA, Williams MA, Levine BD. Effect of gravity and microgravity on intracranial pressure.. J Physiol 2017 Mar 15;595(6):2115-2127.
    doi: 10.1113/JP273557pmc: PMC5350445pubmed: 28092926google scholar: lookup
  55. Raboel PH, Bartek J Jr, Andresen M, Bellander BM, Romner B. Intracranial Pressure Monitoring: Invasive versus Non-Invasive Methods-A Review.. Crit Care Res Pract 2012;2012:950393.
    pmc: PMC3376474pubmed: 22720148doi: 10.1155/2012/950393google scholar: lookup
  56. Wyckoff RW, Tesar WC. Equine encephalomyelitis in monkeys.. The Journal of Immunology 1939;37(4):329–43.
  57. Hurst EW. Infection of the rhesus monkey (Macaca mulatta) and the guinea‐pig with the virus of equine encephalomyelitis.. The Journal of Pathology and Bacteriology 1936;42(1):271–302.
  58. Rossi SL, Russell-Lodrigue KE, Killeen SZ, Wang E, Leal G, Bergren NA, Vinet-Oliphant H, Weaver SC, Roy CJ. IRES-Containing VEEV Vaccine Protects Cynomolgus Macaques from IE Venezuelan Equine Encephalitis Virus Aerosol Challenge.. PLoS Negl Trop Dis 2015 May;9(5):e0003797.
    pmc: PMC4447396pubmed: 26020513doi: 10.1371/journal.pntd.0003797google scholar: lookup
  59. Roy CJ, Adams AP, Wang E, Leal G, Seymour RL, Sivasubramani SK, Mega W, Frolov I, Didier PJ, Weaver SC. A chimeric Sindbis-based vaccine protects cynomolgus macaques against a lethal aerosol challenge of eastern equine encephalitis virus.. Vaccine 2013 Mar 1;31(11):1464-70.
    doi: 10.1016/j.vaccine.2013.01.014pmc: PMC3581708pubmed: 23333212google scholar: lookup
  60. Dickmeis T. Glucocorticoids and the circadian clock.. J Endocrinol 2009 Jan;200(1):3-22.
    doi: 10.1677/JOE-08-0415pubmed: 18971218google scholar: lookup
  61. Yan J, Wang H, Liu Y, Shao C. Analysis of gene regulatory networks in the mammalian circadian rhythm.. PLoS Comput Biol 2008 Oct;4(10):e1000193.
    pmc: PMC2543109pubmed: 18846204doi: 10.1371/journal.pcbi.1000193google scholar: lookup
  62. Rottenberg M, Kristensson K. Effects of interferon-gamma on neuronal infections.. Viral Immunol 2002;15(2):247-60.
    doi: 10.1089/08828240260066206pubmed: 12081010google scholar: lookup
  63. Darko DF, Miller JC, Gallen C, White J, Koziol J, Brown SJ, Hayduk R, Atkinson JH, Assmus J, Munnell DT, Naitoh P, McCutchan JA, Mitler MM. Sleep electroencephalogram delta-frequency amplitude, night plasma levels of tumor necrosis factor alpha, and human immunodeficiency virus infection.. Proc Natl Acad Sci U S A 1995 Dec 19;92(26):12080-4.
    pmc: PMC40300pubmed: 8618848doi: 10.1073/pnas.92.26.12080google scholar: lookup
  64. Keren AS, Yuval-Greenberg S, Deouell LY. Saccadic spike potentials in gamma-band EEG: characterization, detection and suppression.. Neuroimage 2010 Feb 1;49(3):2248-63.
    doi: 10.1016/j.neuroimage.2009.10.057pubmed: 19874901google scholar: lookup
  65. Yilmaz G, Ungan P, Sebik O, Uginčius P, Türker KS. Interference of tonic muscle activity on the EEG: a single motor unit study.. Front Hum Neurosci 2014;8:504.
    doi: 10.3389/fnhum.2014.00504pmc: PMC4092367pubmed: 25071531google scholar: lookup

Citations

This article has been cited 14 times.
  1. Langsjoen RM, Key A, Shariatzadeh N, Jackson CR, Mahmood F, Arkun K, Alexandrescu S, Solomon IH, Piantadosi A. Eastern Equine Encephalitis Virus Diversity in Massachusetts Patients, 1938-2020. Am J Trop Med Hyg 2023 Aug 2;109(2):387-396.
    doi: 10.4269/ajtmh.23-0047pubmed: 37339758google scholar: lookup
  2. Reyna RA, Weaver SC. Sequelae and Animal Modeling of Encephalitic Alphavirus Infections. Viruses 2023 Jan 28;15(2).
    doi: 10.3390/v15020382pubmed: 36851596google scholar: lookup
  3. Gardner CL, Sun C, Dunn MD, Gilliland TC Jr, Trobaugh DW, Terada Y, Reed DS, Hartman AL, Klimstra WB. In Vitro and In Vivo Phenotypes of Venezuelan, Eastern and Western Equine Encephalitis Viruses Derived from cDNA Clones of Human Isolates. Viruses 2022 Dec 20;15(1).
    doi: 10.3390/v15010005pubmed: 36680046google scholar: lookup
  4. Ma H, Albe JR, Gilliland T, McMillen CM, Gardner CL, Boyles DA, Cottle EL, Dunn MD, Lundy JD, Salama N, O'Malley KJ, Pandrea I, Teichert T, Barrick S, Klimstra WB, Hartman AL, Reed DS. Long-term persistence of viral RNA and inflammation in the CNS of macaques exposed to aerosolized Venezuelan equine encephalitis virus. PLoS Pathog 2022 Jun;18(6):e1009946.
    doi: 10.1371/journal.ppat.1009946pubmed: 35696423google scholar: lookup
  5. Portillo-Lara R, Tahirbegi B, Chapman CAR, Goding JA, Green RA. Mind the gap: State-of-the-art technologies and applications for EEG-based brain-computer interfaces. APL Bioeng 2021 Sep;5(3):031507.
    doi: 10.1063/5.0047237pubmed: 34327294google scholar: lookup
  6. Wierzbicka M, Domino M, Zabielski R, Gajewski Z. Long-Term Recording of Reticulo-Rumen Myoelectrical Activity in Sheep by a Telemetry Method. Animals (Basel) 2021 Apr 8;11(4).
    doi: 10.3390/ani11041052pubmed: 33917991google scholar: lookup
  7. Albe JR, Ma H, Gilliland TH, McMillen CM, Gardner CL, Boyles DA, Cottle EL, Dunn MD, Lundy JD, O'Malley KJ, Salama N, Walters AW, Pandrea I, Teichert T, Klimstra WB, Reed DS, Hartman AL. Physiological and immunological changes in the brain associated with lethal eastern equine encephalitis virus in macaques. PLoS Pathog 2021 Feb;17(2):e1009308.
    doi: 10.1371/journal.ppat.1009308pubmed: 33534855google scholar: lookup
  8. Huang CN, Tian XB, Jiang SM, Chang SH, Wang N, Liu MQ, Zhang QX, Li T, Zhang LJ, Yang L. Comparisons Between Infectious and Autoimmune Encephalitis: Clinical Signs, Biochemistry, Blood Counts, and Imaging Findings. Neuropsychiatr Dis Treat 2020;16:2649-2660.
    doi: 10.2147/NDT.S274487pubmed: 33177828google scholar: lookup
  9. Vail KJ, Macha BN, Hellmers L, Fischer T. Modeling Virus-Associated Central Nervous System Disease in Non-Human Primates. Int J Mol Sci 2025 Jul 17;26(14).
    doi: 10.3390/ijms26146886pubmed: 40725130google scholar: lookup
  10. Reed DS, McElroy AK, Barbeau DJ, McMillen CM, Tilston-Lunel NL, Nambulli S, Cottle E, Gilliland TC, Rannulu H, Lundy J, Olsen EL, O'Malley KJ, Xia M, Hartman AL, Luke TC, Egland K, Bausch C, Wu H, Sullivan EJ, Klimstra WB, Duprex WP. No evidence for enhanced disease with human polyclonal SARS-CoV-2 antibody in the ferret model. PLoS One 2024;19(6):e0290909.
    doi: 10.1371/journal.pone.0290909pubmed: 38900732google scholar: lookup
  11. Burke CW, Gardner CL, Goodson AI, Piper AE, Erwin-Cohen RA, White CE, Glass PJ. Defining the Cynomolgus Macaque (Macaca fascicularis) Animal Model for Aerosolized Venezuelan Equine Encephalitis: Importance of Challenge Dose and Viral Subtype. Viruses 2023 Nov 29;15(12).
    doi: 10.3390/v15122351pubmed: 38140592google scholar: lookup
  12. Hartman AL, Myler PJ. Bunyavirales: Scientific Gaps and Prototype Pathogens for a Large and Diverse Group of Zoonotic Viruses. J Infect Dis 2023 Oct 18;228(Suppl 6):S376-S389.
    doi: 10.1093/infdis/jiac338pubmed: 37849397google scholar: lookup
  13. Williams EP, Xue Y, Lee J, Fitzpatrick EA, Kong Y, Reichard W, Writt H, Jonsson CB. Deep spatial profiling of Venezuelan equine encephalitis virus reveals increased genetic diversity amidst neuroinflammation and cell death during brain infection. J Virol 2023 Aug 31;97(8):e0082723.
    doi: 10.1128/jvi.00827-23pubmed: 37560924google scholar: lookup
  14. Cao X, Yang D, Parvathareddy J, Chu YK, Kim EJ, Fitz-Henley JN, Li X, Lukka PB, Parmar KR, Temrikar ZH, Dhole P, Adcock RS, Gabbard J, Bansal S, Lee J, Zalduondo L, Hayes E, Stabenow J, Meibohm B, Fitzpatrick EA, Bailey K, Campos RK, Julander JG, Rossi SL, Chung D, Jonsson CB, Golden JE. Efficacy of a brain-penetrant antiviral in lethal Venezuelan and eastern equine encephalitis mouse models. Sci Transl Med 2023 Apr 12;15(691):eabl9344.
    doi: 10.1126/scitranslmed.abl9344pubmed: 37043558google scholar: lookup
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