Altered auditory brainstem responses are post-acute sequela of SARS-CoV-2 (PASC)

  • Moghimi, N. et al. The neurological manifestations of post-acute sequelae of SARS-CoV-2 infection. Curr. Neurol. Neurosci. Rep. 21, 1–17 (2021).

    Article 
    MATH 

    Google Scholar
     

  • Parker, A. M. et al. Addressing the post-acute sequelae of SARS-CoV-2 infection: A multidisciplinary model of care. Lancet Respiratory Med. 9 (11), 1328–1341 (2021).

    Article 
    CAS 
    MATH 

    Google Scholar
     

  • Vehar, S., Boushra, M., Ntiamoah, P. & Biehl, M. Post-acute sequelae of SARS-CoV-2 infection: Caring for the ‘long-haulers’. Cleve Clin. J. Med. 88 (5), 267–272 (2021).

    Article 
    PubMed 

    Google Scholar
     

  • Sudre, C. H. et al. Attributes and predictors of long COVID. Nat. Med. 27 (4), 626–631 (2021).

    Article 
    CAS 
    PubMed 
    PubMed Central 
    MATH 

    Google Scholar
     

  • Carfì, A., Bernabei, R. & Landi, F. Persistent symptoms in patients after acute COVID-19. Jama 324 (6), 603–605 (2020).

    Article 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Islam, M. F., Cotler, J. & Jason, L. A. Post-viral fatigue and COVID-19: Lessons from past epidemics. Fatigue Biomed. Health Behav. 8 (2), 61–69. https://doi.org/10.1080/21641846.2020.1778227 (2020).

    Article 
    MATH 

    Google Scholar
     

  • Wu, Y. et al. Nervous system involvement after infection with COVID-19 and other coronaviruses. Brain. Behav. Immun. 87, 18–22 (2020).

    Article 
    CAS 
    PubMed 
    PubMed Central 
    MATH 

    Google Scholar
     

  • Khateb, M., Bosak, N. & Muqary, M. Coronaviruses and central nervous system manifestations. Front. Neurol. 11doi https://doi.org/10.3389/fneur.2020.00715 (2020).

  • Haider, H. F. & Szczepek, A. J. Neurotological consequences of long COVID. Front. Neurol. 13, 1087896 (2022).

    Article 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Junior, G. Z. et al. Neurologic and neuropsychiatric symptoms in long-COVID 19 syndrome: A systematic review (Research Square Platform LLC, 2022).

  • Wu, Y. et al. Nervous system involvement after infection with COVID-19 and other coronaviruses. Brain Behav. Immun.. 87, 18–22. https://doi.org/10.1016/j.bbi.2020.03.031 (2020).

    Article 
    CAS 
    MATH 

    Google Scholar
     

  • Alves de Sousa, F., Costa, R., Xará, S., Pinto, A. & Almeida, E. S. SARS-CoV-2 and hearing: An audiometric analysis of COVID-19 hospitalized patients. J. Otol.(2021).

  • Verma, H., Shah, J., Akhilesh, K. & Shukla, B. Patients’ perspective about speech, swallowing and hearing status post-SARS-CoV-2 (COVID-19) recovery: E-survey. Eur. Arch. Otorhinolaryngol. 279 (5), 2523–2532. https://doi.org/10.1007/s00405-021-07217-2 (2022).

    Article 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Almishaal, A. A. & Alrushaidan, A. A. Short- and long-term self-reported audiovestibular symptoms of SARS-CoV-2 infection in hospitalized and nonhospitalized patients. Audiol. Neurotol. 1–15. (2022).

  • De Luca, P. et al. Long COVID, audiovestibular symptoms and persistent chemosensory dysfunction: A systematic review of the current evidence. Acta Otorhinolaryngol. Ital. 42, S87–S93 (2022).

    Article 
    PubMed 
    PubMed Central 
    MATH 

    Google Scholar
     

  • Gedik, Ö., Hüsam, H., Başöz, M., Tas, N. & Aksoy, F. The effect of coronavirus disease 2019 on the hearing system. J. Laryngol. Otol. 135 (9), 810–814. https://doi.org/10.1017/s0022215121001961 (2021).

    Article 
    CAS 
    MATH 

    Google Scholar
     

  • Öztürk, B., Kavruk, H. & Aykul, A. Audiological findings in individuals diagnosed with COVID-19. Am. J. Otolaryngol. 43 (3), 103428 (2022).

    Article 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Dorobisz, K., Pazdro-Zastawny, K., Misiak, P., Kruk-Krzemień, A. & Zatoński, T. Sensorineural hearing loss in patients with Long-COVID-19: Objective and behavioral audiometric findings. Infect. Drug Resist. 16, 1931–1939 (2023).

    Article 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Burkard, R. F. & Sims, D. The human auditory brainstem response to high click rates. (2001).

  • Don, M., Allen, A. R. & Starr, A. Effect of click rate on the latency of auditory brain stem responses in humans. Ann. Otol. Rhinol. Laryngol. 86 (2), 186–195 (1977).

    Article 
    CAS 
    MATH 

    Google Scholar
     

  • Yagi, T. & Kaga, K. The effect of the click repetition rate on the latency of the auditory evoked brain stem response and its clinical use for a neurological diagnosis. Arch. Oto-Rhino-Laryngol. 222 (2), 91–97. https://doi.org/10.1007/bf00469746 (1979).

    Article 
    CAS 
    MATH 

    Google Scholar
     

  • Paludetti, G., Maurizi, M. & Ottaviani, F. Effects of stimulus repetition rate on the auditory brain stem responses (ABR). Otol. Neurotol. 4 (3), 226–234 (1983).

    CAS 
    MATH 

    Google Scholar
     

  • Jacobson, J. T., Murray, T. & Deppe, U. The effects of ABR stimulus repetition rate in multiple sclerosis. Ear Hear. 8 (2), 115–120 (1987).

    Article 
    CAS 
    PubMed 
    MATH 

    Google Scholar
     

  • Johannesen, P. T. & Lopez-Poveda, E. A. Age-related central gain compensation for reduced auditory nerve output for people with normal audiograms, with and without tinnitus. Iscience 24(6) (2021).

  • Rumschlag, J. A. et al., Age-related central gain with degraded neural synchrony in the auditory brainstem of mice and humans. Neurobiol. Aging. 115, 50–59. https://doi.org/10.1016/j.neurobiolaging.2022.03.014 (2022).

  • White, K. R., Forsman, I., Eichwald, J. & Munoz, K. Apr. The evolution of early hearing detection and intervention programs in the United States. Seminars Perinatol. 34 (2), 170–179 (2010). https://doi.org/10.1053/j.semperi.2009.12.009

  • Caspary, D. M., Milbrandt, J. C. & Helfert, R. H. Central auditory aging: GABA changes in the inferior colliculus. Exp. Gerontol. 30 (3–4), 349–360 (1995).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Harris, K. C. et al. Afferent loss, GABA, and central gain in older adults: Associations with speech recognition in noise. J. Neurosci. 42 (38), 7201–7212. https://doi.org/10.1523/jneurosci.0242-22.2022 (2022).

    Article 
    CAS 
    PubMed 
    PubMed Central 
    MATH 

    Google Scholar
     

  • Auerbach, B. D., Rodrigues, P. V. & Salvi, R. J. Central gain control in tinnitus and hyperacusis. Rev. Front. Neurol.. 24 (206) (2014). https://doi.org/10.3389/fneur.2014.00206 (2014).

  • Roberts, L. E. & Salvi, R. Overview Hearing Loss, Tinnitus, Hyperacusis, and the Role of Central Gain, p. 1–7 (Elsevier, 2019).

  • Baguley, D., McFerran, D., Hall, D. & Tinnitus Lancet 382 (9904), 1600–1607 (2013).

    Article 
    PubMed 

    Google Scholar
     

  • Shulman, A., Goldstein, B. & Strashun, A. M. Central nervous system neurodegeneration and tinnitus: A clinical experience. Int. Tinnitus J. 13, 118–131 (2007).

    PubMed 

    Google Scholar
     

  • Vasilkov, V. et al. Evidence of cochlear neural degeneration in normal-hearing subjects with tinnitus. Sci. Rep. 13 (1). https://doi.org/10.1038/s41598-023-46741-5 (2023).

  • Auerbach, B. D., Radziwon, K. & Salvi, R. Testing the central gain model: Loudness growth correlates with central auditory gain enhancement in a rodent model of hyperacusis. Neurosci. 21, 407:93–107. https://doi.org/10.1016/j.neuroscience.2018.09.036 (2019).

    Article 
    CAS 
    MATH 

    Google Scholar
     

  • Valderrama, J. T. et al. Effects of lifetime noise exposure on the middle-age human auditory brainstem response, tinnitus and speech-in-noise intelligibility. Hear. Res. 365, 36–48. https://doi.org/10.1016/j.heares.2018.06.003 (2018). 2018/08/01/.

    Article 
    PubMed 
    MATH 

    Google Scholar
     

  • Gu, J. W., Halpin, C. F., Nam, E-C., Levine, R. A. & Melcher, J. R. Tinnitus, diminished sound-level tolerance, and elevated auditory activity in humans with clinically normal hearing sensitivity. J. Neurophysiol. (2010).

  • Milloy, V., Fournier, P., Benoit, D., Noreña, A. & Koravand, A. Auditory brainstem responses in tinnitus: A review of who, how, and what? Front. Aging Neurosci. 9, 237 (2017).

    Article 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Gu, J. W., Herrmann, B. S., Levine, R. A. & Melcher, J. R. Brainstem auditory evoked potentials suggest a role for the ventral cochlear nucleus in tinnitus. J. Assoc. Res. Otolaryngol. 13 (6), 819–833. https://doi.org/10.1007/s10162-012-0344-1 (2012).

    Article 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Bramhall, N. F., Konrad-Martin, D. & McMillan, G. P. Tinnitus and auditory perception after a history of noise exposure: Relationship to auditory brainstem response measures. Ear Hear. 39 (5), 881–894. https://doi.org/10.1097/aud.0000000000000544 (2018).

    Article 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Schaette, R. & McAlpine, D. Tinnitus with a normal audiogram: Physiological evidence for hidden hearing loss and computational model. J. Neurosci. Off. J. Soc. Neurosci. 21 (38), 13452–13457. https://doi.org/10.1523/jneurosci.2156-11.2011 (2011).

    Article 

    Google Scholar
     

  • Tampas, J. W. & Harkrider, A. W. Auditory evoked potentials in females with high and low acceptance of background noise when listening to speech. J. Acoust. Soc. Am. 119 (3), 1548–1561 (2006).

    Article 
    ADS 
    PubMed 
    MATH 

    Google Scholar
     

  • Shargorodsky, J., Curhan, G. C. & Farwell, W. R. Prevalence and characteristics of tinnitus among US adults. Am. J. Med. 123 (8), 711–718 (2010).

    Article 
    PubMed 
    MATH 

    Google Scholar
     

  • Kramer, S. E., Kapteyn, T. S., Festen, J. M. & Tobi, H. Factors in subjective hearing disability. Audiol.. 34 (6), 311–320 (1995).

    Article 
    CAS 

    Google Scholar
     

  • Beck, A. T., Steer, R. A. & Brown, G. K. Beck depression inventory. San Antonio TX (1987).

  • Beck, A. T., Epstein, N., Brown, G. & Steer, R. Beck anxiety inventory. J. Consult. Clin. Psychol. (1993).

  • Beck, A. T., Steer, R. A. & Brown, G. K. BDI-II, Beck Depression Inventory 2nd edn vi (Psychological Corp, 1996).

  • Chalder, T. et al. Development of a fatigue scale. J. Psychosom. Res. 37 (2), 147–153. https://doi.org/10.1016/0022-3999(93)90081-p (1993).

    Article 
    CAS 
    PubMed 
    MATH 

    Google Scholar
     

  • Cella, M. & Chalder, T. Measuring fatigue in clinical and community settings. J. Psychosom. Res. 69 (1), 17–22. https://doi.org/10.1016/j.jpsychores.2009.10.007 (2010).

    Article 
    MATH 

    Google Scholar
     

  • Loge, J. H., Ekeberg, O. & Kaasa, S. Fatigue in the general Norwegian population: Normative data and associations. J. Psychosom. Res. 45 (1), 53–65. https://doi.org/10.1016/s0022-3999(97)00291-2 (1998).

    Article 
    CAS 
    MATH 

    Google Scholar
     

  • Cicerone, K. D. & Kalmar, K. Persistent postconcussion syndrome: The structure of subjective complaints after mild traumatic brain injury. J. Head Trauma Rehabil. 10 (3), 1–17 (1995).

    Article 
    MATH 

    Google Scholar
     

  • Caplan, L. J. et al. The structure of postconcussive symptoms in 3 US military samples. J. Head Trauma Rehabil. 25 (6), 447–458 (2010).

    Article 
    MATH 

    Google Scholar
     

  • Liberman, M. C. & Kujawa, S. G. Cochlear synaptopathy in acquired sensorineural hearing loss: Manifestations and mechanisms. Hear. Res. Jun. 349, 138–147. https://doi.org/10.1016/j.heares.2017.01.003 (2017).

    Article 
    MATH 

    Google Scholar
     

  • Hamdy, M. M., Hosny, N. A., Farag, R. G. & Elbohy, Z. M. Y. Assessment of cortical evoked potential (P300) and auditory brainstem response (ABR) in post-COVID-19 patients. Egypt. J. Otolaryngol. 40 (1). https://doi.org/10.1186/s43163-024-00612-6 (2024).

  • Yong, S. J. Persistent brainstem dysfunction in Long-COVID: A hypothesis. ACS Chem. Neurosci.. 17 (4), 573–580. https://doi.org/10.1021/acschemneuro.0c00793 (2021).

    Article 
    CAS 
    MATH 

    Google Scholar
     

  • Reichard, R. R. et al. Neuropathology of COVID-19: A spectrum of vascular and acute disseminated encephalomyelitis (ADEM)-like pathology. Acta Neuropathol. 140, 1–6 (2020).

    Article 
    CAS 
    PubMed 
    PubMed Central 
    MATH 

    Google Scholar
     

  • Yong, S. J. Persistent brainstem dysfunction in long-COVID: A hypothesis. ACS Chem. Neurosci. 12 (4), 573–580 (2021).

    Article 
    CAS 
    PubMed 
    MATH 

    Google Scholar
     

  • Yong, S. J. Long COVID or post-COVID-19 syndrome: Putative pathophysiology, risk factors, and treatments. Infect. Dis. 53 (10), 737–754 (2021).

    Article 
    CAS 
    MATH 

    Google Scholar
     

  • DeLuca, J., Genova, H. M., Hillary, F. G. & Wylie, G. Neural correlates of cognitive fatigue in multiple sclerosis using functional MRI. J. Neurol. Sci. 270 (1–2), 28–39 (2008).

    Article 
    PubMed 
    MATH 

    Google Scholar
     

  • Krupp, L. B. & Elkins, L. E. Fatigue and declines in cognitive functioning in multiple sclerosis. Neurology 55 (7), 934–939 (2000).

    Article 
    CAS 
    PubMed 
    MATH 

    Google Scholar
     

  • Robinson, K. & Rudge, P. The stability of the auditory evoked potentials in normal man and patients with multiple sclerosis. J. Neurol. Sci. 36 (1), 147–156 (1978).

    Article 
    CAS 
    PubMed 
    MATH 

    Google Scholar
     

  • Vasilkov, V. et al. Evidence of cochlear neural degeneration in normal-hearing subjects with tinnitus. Sci. Rep. 13 (1), 19870 (2023).

    Article 
    ADS 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Kaltenbach, J. A. Tinnitus: models and mechanisms. Hear. Res. 276 (1–2), 52–60 (2011).

    Article 
    PubMed 
    MATH 

    Google Scholar
     

  • Bhat, R. et al. Inhibitory role for GABA in autoimmune inflammation. Proc. Natl. Acad. Sci. 107 (6), 2580–2585 (2010).

    Article 
    ADS 
    CAS 
    PubMed 
    PubMed Central 
    MATH 

    Google Scholar
     

  • Versace, V. et al. Intracortical GABAergic dysfunction in patients with fatigue and dysexecutive syndrome after COVID-19. Clin. Neurophysiol. 132 (5), 1138–1143 (2021).

    Article 
    PubMed 
    PubMed Central 
    MATH 

    Google Scholar
     

  • Marinkovic, K. et al. Cortical GABA levels are reduced in post-Acute COVID-19 syndrome. Brain Sci. 13 (12), 1666 (2023).

    Article 
    CAS 
    PubMed 
    PubMed Central 
    MATH 

    Google Scholar
     

  • Isler, B. et al. Lower glutamate and GABA levels in auditory cortex of tinnitus patients: A 2D-JPRESS MR spectroscopy study. Sci. Rep. 12 (1). https://doi.org/10.1038/s41598-022-07835-8 (2022).

  • Petty, F. GABA and mood disorders: A brief review and hypothesis. J. Affect. Disord. 34 (4), 275–281 (1995).

    Article 
    CAS 
    PubMed 
    MATH 

    Google Scholar
     

  • Baldwin, C. L. Auditory Cognition and Human Performance: Research and Applications (CRC, 2012).

  • Pichora-Fuller, M. K. et al. Hearing impairment and cognitive energy: The framework for Understanding effortful listening (FUEL). Ear Hear. 37 (1), 5S–27S. https://doi.org/10.1097/aud.0000000000000312 (2016).

    Article 
    PubMed 

    Google Scholar
     

  • Chaudhuri, A. & Behan, P. O. Fatigue and basal ganglia. J. Neurol. Sci. 179 (1–2), 34–42 (2000).

    Article 
    CAS 
    PubMed 
    MATH 

    Google Scholar
     

  • Chaudhuri, A. & Behan, P. O. Fatigue in neurological disorders. Lancet 363 (9413), 978–988 (2004).

    Article 
    PubMed 
    MATH 

    Google Scholar
     

  • Lange, G. et al. Objective evidence of cognitive complaints in chronic fatigue syndrome: A BOLD fMRI study of verbal working memory. NeuroImage 26, 513–524 (2005).

    Article 
    CAS 
    PubMed 
    MATH 

    Google Scholar
     

  • Stockard, J. J. & Rossiter, V. S. Clinical and pathologic correlates of brain stem auditory response abnormalities. Neurology 27 (4), 316–316 (1977).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Kamerer, A. M. et al. The role of cognition in common measures of peripheral synaptopathy and hidden hearing loss. Am. J. Audiol. 28 (4), 843–856 (2019).

    Article 
    PubMed 
    PubMed Central 
    MATH 

    Google Scholar
     

  • Allen, P. & Allan, C. Auditory processing disorders: Relationship to cognitive processes and underlying auditory neural integrity. Int. J. Pediatr. Otorhinolaryngol. 78 (2), 198–208 (2014).

    Article 
    PubMed 
    MATH 

    Google Scholar
     

  • Caspary, D. M., Ling, L., Turner, J. G. & Hughes, L. F. Inhibitory neurotransmission, plasticity and aging in the mammalian central auditory system. J. Exp. Biol. 211 (11), 1781–1791 (2008).

    Article 
    CAS 
    PubMed 
    MATH 

    Google Scholar
     

  • Sivagurunathan, N. & Calivarathan, L. SARS-CoV-2 infection to premature neuronal aging and neurodegenerative diseases: Is there any connection with hypoxia? CNS Neurol. Disord Drug Targets. 23 (4), 431–448. https://doi.org/10.2174/1871527322666230418114446 (2024).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Petersen, M. et al., Brain imaging and neuropsychological assessment of individuals recovered from a mild to moderate SARS-CoV-2 infection. Proc. Natl. Acad. Sci. 120 (22)https://doi.org/10.1073/pnas.2217232120 (2023).

  • Auerbach, B. D., Rodrigues, P. V. & Salvi, R. J. Central gain control in tinnitus and hyperacusis. Front. Neurol. 5. https://doi.org/10.3389/fneur.2014.00206 (2014).

  • Noreña, A. J. An integrative model of tinnitus based on a central gain controlling neural sensitivity. Neurosci. Biobehav. Rev. 35 (5), 1089–1109 (2011).

    Article 
    MATH 

    Google Scholar
     

  • Sedley, W. Tinnitus: Does gain explain? Neuroscience 407, 213–228 (2019).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Ting, K-C., Chang, C-C., Huang, C-Y., Chen, Y-F. & Cheng, Y-F. Are electrocochleographic changes an early sign of cochlear synaptopathy? A prospective study in tinnitus patients with normal hearing. Diagnostics 12 (4), 802. https://doi.org/10.3390/diagnostics12040802 (2022).

    Article 
    PubMed 
    PubMed Central 
    MATH 

    Google Scholar
     

  • Shim, H. J., An, Y. H., Kim, D. H., Yoon, J. E. & Yoon, J. H. Comparisons of auditory brainstem response and sound level tolerance in tinnitus ears and non-tinnitus ears in unilateral tinnitus patients with normal audiograms. PLoS ONE. 12 (12), e0189157. https://doi.org/10.1371/journal.pone.0189157 (2017).

    Article 
    CAS 
    PubMed 
    PubMed Central 
    MATH 

    Google Scholar
     

  • Hackenberg, B. et al. Tinnitus and its relation to depression, anxiety, and stress—a population-based cohort study. J. Clin. Med. 12 (3), 1169 (2023).

    Article 
    PubMed 
    PubMed Central 
    MATH 

    Google Scholar
     

  • Searchfield, G. D. Tinnitus what and where: An ecological framework. Front. Neurol. 5, 122255 (2014).

    Article 

    Google Scholar
     

  • Colagrosso, E. M., Fournier, P., Fitzpatrick, E. M. & Hébert, S. A qualitative study on factors modulating tinnitus experience. Ear Hear. 40 (3), 636–644 (2019).

    Article 
    PubMed 

    Google Scholar
     

  • Newman, C. W., Jacobson, G. P. & Spitzer, J. B. Development of the tinnitus handicap inventory. Arch. Otolaryngol.–Head Neck Surg. 122 (2), 143–148 (1996).

    Article 
    CAS 
    MATH 

    Google Scholar
     

  • Song, Z. et al. Tinnitus is associated with extended high-frequency hearing loss and hidden high-frequency damage in young patients. Otol. Neurotol. 42 (3), 377–383 (2021).

    Article 
    PubMed 
    MATH 

    Google Scholar
     

  • Jafari, Z., Baguley, D., Kolb, B. E. & Mohajerani, M. H. A systematic review and meta-analysis of extended high-frequency hearing thresholds in tinnitus with a normal audiogram. Ear Hear. 43 (6), 1643–1652 (2022).

    Article 
    PubMed 

    Google Scholar
     

  • Ahmed, S. H. et al. SARS-CoV-2 vaccine-associated-tinnitus: A review. Ann. Med. Surg. 75, 103293 (2022).

    Article 
    MATH 

    Google Scholar
     

  • Source link

    Get RawNews Daily

    Stay informed with our RawNews daily newsletter email

    Altered auditory brainstem responses are post-acute sequela of SARS-CoV-2 (PASC)

    Increasing fruit, fiber, dairy and caffeine linked to lower risk of tinnitus

    Super Iron Foundry IPO: Listing, Performance, and Analysis

    Giants Sell 10% Ownership Stake To Private Equity Firm