Neuroimaging evaluations of olfactory, gustatory, and neurological deficits in patients with long-term sequelae of COVID-19.
Ageusia
Anosmia
COVID-19
Hyposmia
Neuroimaging, olfactory dysfunction
Journal
Brain imaging and behavior
ISSN: 1931-7565
Titre abrégé: Brain Imaging Behav
Pays: United States
ID NLM: 101300405
Informations de publication
Date de publication:
28 Sep 2024
28 Sep 2024
Historique:
accepted:
17
09
2024
medline:
28
9
2024
pubmed:
28
9
2024
entrez:
28
9
2024
Statut:
aheadofprint
Résumé
The World Health Organization indicated that around 36 million of patients in the European Region showed long COVID associated with olfactory and gustatory deficits. The precise mechanism underlying long COVID clinical manifestations is still debated. The aim of this study was to evaluate potential correlations between odor threshold, odor discrimination, odor identification, and the activation of specific brain areas in patients after COVID-19. Sixty subjects, 27 patients (15 women and 12 men) with long COVID and a mean age of 40.6 ± 13.4 years, were compared to 33 age-matched healthy controls (20 women and 13 men) with a mean age of 40.5 ± 9.8 years. Our data showed that patients with long COVID symptoms exhibited a significant decrease in odor threshold, odor discrimination, odor identification, and their sum TDI score compared to age-matched healthy controls. In addition, our results indicated significant correlations between odor discrimination and the increased activation in the right hemisphere, in the frontal pole, and in the superior frontal gyrus. This study indicated that the resting-state fMRI in combination with the objective evaluation of olfactory and gustatory function may be useful for the evaluation of patients with long COVID associated with anosmia and hyposmia.
Identifiants
pubmed: 39340624
doi: 10.1007/s11682-024-00936-0
pii: 10.1007/s11682-024-00936-0
doi:
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Informations de copyright
© 2024. The Author(s).
Références
Altunisik, E., Baykan, A. H., Sahin, S., Aydin, E., & Erturk, S. M. (2021). Quantitative analysis of the olfactory system in COVID-19: An MR imaging study. American Journal of Neuroradiology, 42(12), 2207–2214.
pubmed: 34556477
pmcid: 8805742
doi: 10.3174/ajnr.A7278
Beck, A. T., Ward, C. H., Mendelson, M., Mock, J., & Erbaugh, J. (1961). An inventory for measuring depression. Archives of General Psychiatry, 4(6), 561–571.
pubmed: 13688369
doi: 10.1001/archpsyc.1961.01710120031004
Bullmore, E. T., Suckling, J., Overmeyer, S., Rabe-Hesketh, S., Taylor, E., & Brammer, M. J. (1999). Global, Voxel, and cluster tests, by theory and permutation, for a difference between two groups of structural MR images of the brain. IEEE Transactions on Medical Imaging, 18(1), 32–42.
pubmed: 10193695
doi: 10.1109/42.750253
Buschhüter, D., Smitka, M., Puschmann, S., Gerber, J. C., Witt, M., Abolmaali, N. D., & Hummel, T. (2008). Correlation between olfactory bulb volume and olfactory function. Neuroimage, 42(2), 498–502.
pubmed: 18555701
doi: 10.1016/j.neuroimage.2008.05.004
Carfì, A., Bernabei, R., & Landi, F. (2020). Persistent symptoms in patients after acute COVID-19. Jama, 324(6), 603–605.
pubmed: 32644129
pmcid: 7349096
doi: 10.1001/jama.2020.12603
Collins, D. L., Neelin, P., Peters, T. M., & Evans, A. C. (1994). Automatic 3D intersubject registration of MR volumetric data in standardized Talairach space. Journal of Computer Assisted Tomography, 18(2), 192–205.
pubmed: 8126267
doi: 10.1097/00004728-199403000-00005
Conti, S., Bonazzi, S., Laiacona, M., Masina, M., & Coralli, M. V. (2015). Montreal Cognitive Assessment (MoCA)-Italian version: Regression based norms and equivalent scores. Neurological Sciences, 36, 209–214.
pubmed: 25139107
doi: 10.1007/s10072-014-1921-3
Cormiea, S., & Fischer, J. (2023). Odor discrimination is immune to the effects of verbal labels. Scientific Reports, 13(1), 1742.
pubmed: 36720925
pmcid: 9889793
doi: 10.1038/s41598-023-28134-w
Desikan, R. S., Ségonne, F., Fischl, B., Quinn, B. T., Dickerson, B. C., Blacker, D., Buckner, R. S., Dale, A. M., Maguire, R. P., Hyman, B. T., Albert, M. S., & Killiany, R. J. (2006). An automated labeling system for subdividing the human cerebral cortex on MRI scans into gyral based regions of interest. Neuroimage, 31(3), 968–980.
pubmed: 16530430
doi: 10.1016/j.neuroimage.2006.01.021
Doty, R. L. (2022). Olfactory dysfunction in COVID-19: Pathology and long-term implications for brain health. Trends in Molecular Medicine, 28(9), 781–794.
pubmed: 35810128
pmcid: 9212891
doi: 10.1016/j.molmed.2022.06.005
Ercoli, T., Masala, C., Pinna, I., Orofino, G., Solla, P., Rocchi, L., & Defazio, G. (2021). Qualitative smell/taste disorders as sequelae of acute COVID-19. Neurological Sciences, 42, 4921–4926.
pubmed: 34557966
pmcid: 8459812
doi: 10.1007/s10072-021-05611-6
Fjaeldstad, A. W., Stiller-Stut, F., Gleesborg, C., Kringelbach, M. L., Hummel, T., & Fernandes, H. M. (2021). Validation of olfactory network based on brain structural connectivity and its association with olfactory test scores. Frontiers in Systems Neuroscience, 15, 638053.
pubmed: 33927597
pmcid: 8078209
doi: 10.3389/fnsys.2021.638053
Frosolini, A., Parrino, D., Fabbris, C., Fantin, F., Inches, I., Invitto, S., Spinato, G., & De Filippis, C. (2022). Magnetic resonance imaging confirmed olfactory bulb reduction in long COVID-19: Literature review and case series. Brain Sciences, 12(4), 430.
pubmed: 35447962
pmcid: 9029157
doi: 10.3390/brainsci12040430
Gottfried, J. A. (2010). Central mechanisms of odour object perception. Nature Reviews Neuroscience, 11(9), 628–641.
pubmed: 20700142
pmcid: 3722866
doi: 10.1038/nrn2883
Hedner, M., Larsson, M., Arnold, N., Zucco, G. M., & Hummel, T. (2010). Cognitive factors in odor detection, odor discrimination, and odor identification tasks. Journal of Clinical and Experimental Neuropsychology, 32(10), 1062–1067.
pubmed: 20437286
doi: 10.1080/13803391003683070
Hintschich, C. A., Fischer, R., Hummel, T., Wenzel, J. J., Bohr, C., & Vielsmeier, V. (2022). Persisting olfactory dysfunction in post-COVID-19 is associated with gustatory impairment: Results from chemosensitive testing eight months after the acute infection. PLoS One, 17(3), e0265686.
Huang, C., Huang, L., Wang, Y., et al. (2021). 6-month consequences of COVID-19 in patients discharged from hospital: A cohort study. Lancet, 397(10270), 220–232.
pubmed: 33428867
pmcid: 7833295
doi: 10.1016/S0140-6736(20)32656-8
Hummel, T., Sekinger, B., Wolf, S. R., Pauli, E., & Kobal, G. (1997). Sniffin’sticks’: Olfactory performance assessed by the combined testing of odor identification, odor discrimination and olfactory threshold. Chemical Senses, 22(1), 39–52.
pubmed: 9056084
doi: 10.1093/chemse/22.1.39
Hummel, T., Damm, M., Vent, J., Schmidt, M., Theissen, P., Larsson, M., & Klussmann, J. P. (2003). Depth of olfactory sulcus and olfactory function. Brain Research, 975(1–2), 85–89.
pubmed: 12763595
doi: 10.1016/S0006-8993(03)02589-7
Hummel, T., Kobal, G., Gudziol, H., & Mackay-Sim, A. J. E. A. (2007). Normative data for the Sniffin’sticks including tests of odor identification, odor discrimination, and olfactory thresholds: An upgrade based on a group of more than 3,000 subjects. European Archives of Oto-Rhino-Laryngology, 264, 237–243.
pubmed: 17021776
doi: 10.1007/s00405-006-0173-0
Hummel, T., Whitcroft, K. L., Andrews, P., et al. (2017). Position paper on olfactory dysfunction. Rhinology, 54, 1–30.
pubmed: 29528615
doi: 10.4193/Rhino16.248
Joshi, A., Hornstein, H., Thaploo, D., Faria, V., Warr, J., & Hummel, T. (2023). Neural processing of odors with different well-being associations—findings from two consecutive neuroimaging studies. Brain Sciences, 13(4), 576.
pubmed: 37190541
pmcid: 10136803
doi: 10.3390/brainsci13040576
Lamyae Benzakour, Patrice, H., Lalive, K. O., Lövblad, O., Braillard, M., Nehme, M., Coen, J., Serratrice, J. L., & Reny Jérôme Pugin, Idris Guessous, Basile N Landis, Alessandra Griffa, Dimitri Van De Ville, Frederic Assal, Julie A Péron.
Landis, B. N., Welge-Luessen, A., Brämerson, A., Bende, M., Mueller, C. A., Nordin, S., & Hummel, T. (2009). Taste Strips–a rapid, lateralized, gustatory bedside identification test based on impregnated filter papers. Journal of Neurology, 256, 242–248.
pubmed: 19221845
doi: 10.1007/s00415-009-0088-y
Lv, H., Wang, Z., Tong, E., et al. (2018). Resting-state functional MRI: Everything that nonexperts have always wanted to know. American Journal of Neuroradiology, 39(8), 1390–1399.
pubmed: 29348136
pmcid: 6051935
Masala, C., Saba, L., Cecchini, M. P., Solla, P., & Loy, F. (2018). Olfactory function and age: A sniffin’sticks extended test study performed in Sardinia. Chemosensory Perception, 11, 19–26.
doi: 10.1007/s12078-017-9233-7
Masala, C., Käehling, C., Fall, F., & Hummel, T. (2019). Correlation between olfactory function, trigeminal sensitivity, and nasal anatomy in healthy subjects. European Archives of Oto-Rhino-Laryngology, 276, 1649–1654.
pubmed: 30843174
doi: 10.1007/s00405-019-05367-y
Muccioli, L., Sighinolfi, G., Mitolo, et al. (2023). Cognitive and functional connectivity impairment in post-COVID-19 olfactory dysfunction. NeuroImage: Clinical, 38, 103410.
pubmed: 37104928
doi: 10.1016/j.nicl.2023.103410
Nasreddine, Z. S., Phillips, N. A., Bédirian, V., Charbonneau, S., Whitehead, V., Collin, I., Cummings, J. L., & Chertkow, H. (2005). The Montreal Cognitive Assessment, MoCA: A brief screening tool for mild cognitive impairment. Journal of the American Geriatrics Society, 53(4), 695–699.
pubmed: 15817019
doi: 10.1111/j.1532-5415.2005.53221.x
Nieto-Castanon, A. (2020). Handbook of functional connectivity magnetic resonance imaging methods in CONN. Hilbert.
Nigri, A., Ferraro, S., D’Incerti, L., Critchley, H. D., Bruzzone, M. G., & Minati, L. (2013). Connectivity of the amygdala, piriform, and orbitofrontal cortex during olfactory stimulation: A functional MRI study. Neuroreport, 24(4), 171–175.
pubmed: 23381349
doi: 10.1097/WNR.0b013e32835d5d2b
Oleszkiewicz, A., Schriever, V. A., Croy, I., Haehner, A., & Hummel, T. (2019). Updated Sniffin’sticks normative data based on an extended sample of 9139 subjects. European Archives of Oto-rhino-laryngology, 276, 719–728.
pubmed: 30554358
doi: 10.1007/s00405-018-5248-1
Ousseiran, Z. H., Fares, Y., & Chamoun, W. T. (2023). Neurological manifestations of COVID-19: A systematic review and detailed comprehension. International Journal of Neuroscience, 133(7), 754–769.
pubmed: 34433369
doi: 10.1080/00207454.2021.1973000
Pilotto, A., Cristillo, V., Piccinelli, C., S., et al. (2021). Long-term neurological manifestations of COVID-19: Prevalence and predictive factors. Neurological Sciences, 42, 4903–4907.
pubmed: 34523082
pmcid: 8439956
doi: 10.1007/s10072-021-05586-4
Plailly, J., Radnovich, A. J., Sabri, M., Royet, J. P., & Kareken, D. A. (2007). Involvement of the left anterior insula and frontopolar gyrus in odor discrimination. Human Brain Mapping, 28(5), 363–372.
pubmed: 17089374
doi: 10.1002/hbm.20290
Porcu, M., Craboledda, D., Garofalo, P., et al. (2019). Reorganization of brain networks following carotid endarterectomy: An exploratory study using resting state functional connectivity with a focus on the changes in default Mode Network connectivity. European Journal of Radiology, 110, 233–241.
pubmed: 30599866
doi: 10.1016/j.ejrad.2018.12.007
Porcu, M., Cocco, L., Cocozza, S., et al. (2021a). The association between white matter hyperintensities, cognition and regional neural activity in healthy subjects. European Journal of Neuroscience, 54(4), 5427–5443.
pubmed: 34327745
doi: 10.1111/ejn.15403
Porcu, M., Cocco, L., Puig, J., et al. (2021b). Global fractional anisotropy: Effect on resting-state neural activity and brain networking in healthy participants. Neuroscience, 472, 103–115.
pubmed: 34364954
doi: 10.1016/j.neuroscience.2021.07.021
Porcu, M., Cocco, L., Cau, R. (2022a). The mid-term effects of carotid endarterectomy on cognition and regional neural activity analyzed with the amplitude of low frequency fluctuations technique. Neuroradiology, 1–11.
Porcu, M., Cocco, L., Cau, R., et al. (2022b). The restoring of interhemispheric brain connectivity following carotid endarterectomy: An exploratory observational study. Brain Imaging and Behavior, 16(5), 2037–2048.
pubmed: 35622267
doi: 10.1007/s11682-022-00674-1
Savic, I., Gulyas, B., Larsson, M., & Roland, P. (2000). Olfactory functions are mediated by parallel and hierarchical processing. Neuron, 26(3), 735–745.
pubmed: 10896168
doi: 10.1016/S0896-6273(00)81209-X
Seubert, J., Freiherr, J., Frasnelli, J., Hummel, T., & Lundström, J. N. (2013). Orbitofrontal cortex and olfactory bulb volume predict distinct aspects of olfactory performance in healthy subjects. Cerebral Cortex, 23(10), 2448–2456.
pubmed: 22875864
doi: 10.1093/cercor/bhs230
Spinato, G., Fabbris, C., Polesel, J., Cazzador, D., Borsetto, D., Hopkins, C., & Boscolo-Rizzo, P. (2020). Alterations in smell or taste in mildly symptomatic outpatients with SARS-CoV-2 infection. Jama, 323(20), 2089–2090.
pubmed: 32320008
pmcid: 7177631
doi: 10.1001/jama.2020.6771
Stefanou, M. I., Palaiodimou, L., Bakola, E., et al. (2022). Neurological manifestations of long-COVID syndrome: A narrative review. Therapeutic Advances in Chronic Disease, 13, 20406223221076890.
pubmed: 35198136
pmcid: 8859684
doi: 10.1177/20406223221076890
Tai, A. P. L., Leung, M. K., Lau, B. W. M., Ngai, S. P. C., & Lau, W. K. W. (2023). Olfactory dysfunction: A plausible source of COVID-19-induced neuropsychiatric symptoms. Frontiers in Neuroscience, 17, 1156914.
pubmed: 37021130
pmcid: 10067586
doi: 10.3389/fnins.2023.1156914
Thomasson, M., Voruz, P., Cionca, A., Jacot de Alcântara, I., Nuber-Champier, A., Allali, G., Benzakour, L., Lalive, P. H., Lövblad, K., Braillard, O., Nehm, M., Coen, M., Serratrice, J., Reny, J., Pugin, J., Guessous, I., Landis, B. N., Griffa, A., Van De Ville, D., Assal, F., & Péron, J. A. (2023). Markers of limbic system damage following SARS-CoV-2 infection. Brain Communications, 5(4), fcad177.
Tzourio-Mazoyer, N., Landeau, B., Papathanassiou, D., et al. (2002). Automated anatomical labeling of activations in SPM using a macroscopic anatomical parcellation of the MNI MRI single-subject brain. Neuroimage, 15(1), 273–289.
pubmed: 11771995
doi: 10.1006/nimg.2001.0978
Whitcroft, K. L., & Hummel, T. (2020). Olfactory dysfunction in COVID-19: Diagnosis and management. Jama, 323(24), 2512–2514.
pubmed: 32432682
doi: 10.1001/jama.2020.8391
Whitfield-Gabrieli, S., & Nieto-Castanon, A. (2012). Conn: A functional connectivity toolbox for correlated and anticorrelated brain networks. Brain Connectivity, 2(3), 125–141.
pubmed: 22642651
doi: 10.1089/brain.2012.0073
Wingrove, J., Makaronidis, J., Prados, F., Kanber, B., Yiannakas, M. C., Magee, C., Castellazzi, G., Grandjean, L., Golay, X., Tur, C., Ciccarelli, O., D’Angelo, E., Wheeler-Kingshott, G., & Batterham, C. A. M. (2023). R. L. Aberrant olfactory network functional connectivity in people with olfactory dysfunction following COVID-19 infection: an exploratory, observational study. EClinicalMedicine, 58.
Worsley, K. J., Marrett, S., Neelin, P., Vandal, A. C., Friston, K. J., & Evans, A. C. (1996). A unified statistical approach for determining significant signals in images of cerebral activation. Human Brain Mapping, 4(1), 58–73.
pubmed: 20408186
doi: 10.1002/(SICI)1097-0193(1996)4:1<58::AID-HBM4>3.0.CO;2-O
Xu, E., Xie, Y., & Al-Aly, Z. (2022). Long-term neurologic outcomes of COVID-19. Nature Medicine, 28(11), 2406–2415.
pubmed: 36138154
pmcid: 9671811
doi: 10.1038/s41591-022-02001-z
Xydakis, M. S., Albers, M. W., Holbrook, E. H., et al. (2021). Post-viral effects of COVID-19 in the olfactory system and their implications. The Lancet Neurology, 20(9), 753–761.
pubmed: 34339626
pmcid: 8324113
doi: 10.1016/S1474-4422(21)00182-4
Zhang, L., Zhou, L., Bao, L., et al. (2021). SARS-CoV-2 crosses the blood–brain barrier accompanied with basement membrane disruption without tight junctions alteration. Signal Transduction and Targeted Therapy, 6(1), 337.
pubmed: 34489403
pmcid: 8419672
doi: 10.1038/s41392-021-00719-9
Zou, Q. H., Zhu, C. Z., Yang, Y., Zuo, X. N., Long, X. Y., Cao, Q. J., Wang, Y. F., & Zang, Y. F. (2008). An improved approach to detection of amplitude of low-frequency fluctuation (ALFF) for resting-state fMRI: Fractional ALFF. Journal of Neuroscience Methods, 172(1), 137–141.
pubmed: 18501969
pmcid: 3902859
doi: 10.1016/j.jneumeth.2008.04.012