Anosmia in COVID-19: Underlying Mechanisms and Assessment of an Olfactory Route to Brain Infection
Open accessAbstract
In recent months it has emerged that the novel coronavirus—responsible for the COVID-19 pandemic—causes reduction of smell and taste in a large fraction of patients. The chemosensory deficits are often the earliest, and sometimes the only signs in otherwise asymptomatic carriers of the SARS-CoV-2 virus. The reasons for the surprisingly early and specific chemosensory dysfunction in COVID-19 are now beginning to be elucidated. In this hypothesis review, we discuss implications of the recent finding that the prevalence of smell and taste dysfunction in COVID-19 patients differs between populations, possibly because of differences in the spike protein of different virus strains or because of differences in the host proteins that enable virus entry, thus modifying infectivity. We review recent progress in defining underlying cellular and molecular mechanisms of the virus-induced anosmia, with a focus on the emerging crucial role of sustentacular cells in the olfactory epithelium. We critically examine the current evidence whether and how the SARS-CoV-2 virus can follow a route from the olfactory epithelium in the nose to the brain to achieve brain infection, and we discuss the prospects for using the smell and taste dysfunctions seen in COVID-19 as an early and rapid diagnostic screening tool.
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Integrity signals
Registry
Cites
Statistics
Claims the paper makes
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Claims other papers make about this one
Each is checked against this paper’s own text: does it say what the citing paper says it does?
Chemosensory deficits in COVID-19 are often short-lived, with most symptoms resolving in 7-10 days, and sense of smell often returning slightly earlier than taste.
“Such chemosensory deficits experienced in COVID‐19 are often short‐lived, with most symptoms resolving in 7‐10 days, with sense of smell often returning slightly earlier than taste.”
From The oral microbiome: Role of key organisms and complex networks in oral health and disease (2021) · cites this paper as [299]
Self-check
Percentages, sums and reported differences re-computed from the paper’s own numbers.
The self-check needs the paper’s full text.
Cites
Clinical characteristics of coronavirus disease 2019 in China
Guan, W.-J., Ni, Z.-Y., Hu, Y., Liang, W.-H., Ou, C.-Q., He, J.-X., Liu, L., Shan, H., Lei, C.-L., Hui, D. S. C., et al. (2020) · New England Journal of Medicine · doi:10.1056/nejmoa2002032 · Cited by 30,246 · see citing works
Chen, N., Zhou, M., Dong, X., Qu, J., Gong, F., Han, Y., Qiu, Y., Wang, J., Liu, Y., Wei, Y., et al. (2020) · The Lancet · doi:10.1016/s0140-6736(20)30211-7 · Cited by 21,415 · see citing works
A new coronavirus associated with human respiratory disease in China
Wu, F., Zhao, S., Yu, B., Chen, Y.-M., Wang, W., Song, Z.-G., Hu, Y., Tao, Z.-W., Tian, J.-H., Pei, Y.-Y., et al. (2020) · Nature · doi:10.1038/s41586-020-2008-3 · Cited by 11,688 · see citing works
Neurologic manifestations of hospitalized patients with coronavirus disease 2019 in Wuhan, China
Mao, L., Jin, H., Wang, M., Hu, Y., Chen, S., He, Q., Chang, J., Hong, C., Zhou, Y., Wang, D., et al. (2020) · JAMA Neurology · doi:10.1001/jamaneurol.2020.1127 · Cited by 7,166 · see citing works
Detection of SARS-CoV-2 in Different Types of Clinical Specimens
Wang, W., Xu, Y., Gao, R., Lu, R., Han, K., Wu, G., & Tan, W. (2020) · JAMA · doi:10.1001/jama.2020.3786 · Cited by 5,019 · see citing works
SARS-CoV-2 Viral Load in Upper Respiratory Specimens of Infected Patients
Zou, L., Ruan, F., Huang, M.-X., Liang, L.-J., Huang, H., Hong, Z.-S., Yu, J.-X., Kang, M., Song, Y.-C., Xia, J., et al. (2020) · New England Journal of Medicine · doi:10.1056/nejmc2001737 · Cited by 4,590 · see citing works
Korber, B., Fischer, W. M., Gnanakaran, S., Yoon, H., Theiler, J., Abfalterer, W., Hengartner, N., Giorgi, E. E., Bhattacharya, T., Foley, B., et al. (2020) · Cell · doi:10.1016/j.cell.2020.06.043 · Cited by 4,281 · see citing works
Structural basis of receptor recognition by SARS-CoV-2
Shang, J., Ye, G., Shi, K., Wan, Y., Luo, C., Aihara, H., Geng, Q., Auerbach, A., & Li, F. (2020) · Nature · doi:10.1038/s41586-020-2179-y · Cited by 3,661 · see citing works
High expression of ACE2 receptor of 2019-nCoV on the epithelial cells of oral mucosa
Xu, H., Zhong, L., Deng, J., Peng, J., Dan, H., Zeng, X., Li, T., & Chen, Q. (2020) · International Journal of Oral Science · doi:10.1038/s41368-020-0074-x · Cited by 2,838 · see citing works
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., et al. (2020) · European Archives of Oto-Rhino-Laryngology · doi:10.1007/s00405-020-05965-1 · Cited by 2,668 · see citing works
Ziegler, C. G. K., Allon, S. J., Nyquist, S. K., Mbano, I. M., Miao, V. N., Tzouanas, C. N., Cao, Y., Yousif, A. S., Bals, J., Hauser, B. M., et al. (2020) · Cell · doi:10.1016/j.cell.2020.04.035 · Cited by 2,284 · see citing works
Prevalence of Asymptomatic SARS-CoV-2 Infection
Oran, D. P., & Topol, E. J. (2020) · Annals of Internal Medicine · doi:10.7326/m20-3012 · Cited by 2,280 · see citing works
Baig, A. M., Khaleeq, A., Ali, U., & Syeda, H. (2020) · ACS Chemical Neuroscience · doi:10.1021/acschemneuro.0c00122 · Cited by 2,207 · see citing works
Nervous system involvement after infection with COVID-19 and other coronaviruses
Wu, Y., Xu, X., Chen, Z., Duan, J., Hashimoto, K., Yang, L., Liu, C., & Yang, C. (2020) · Brain, Behavior, and Immunity · doi:10.1016/j.bbi.2020.03.031 · Cited by 2,046 · see citing works
A first case of meningitis/encephalitis associated with SARS-Coronavirus-2
Moriguchi, T., Harii, N., Goto, J., Harada, D., Sugawara, H., Takamino, J., Ueno, M., Sakata, H., Kondo, K., Myose, N., et al. (2020) · International Journal of Infectious Diseases · doi:10.1016/j.ijid.2020.03.062 · Cited by 2,024 · see citing works
Genomewide Association Study of Severe Covid-19 with Respiratory Failure
The Severe Covid-19 GWAS Group (2020) · New England Journal of Medicine · doi:10.1056/nejmoa2020283 · Cited by 1,986 · see citing works
CD147-spike protein is a novel route for SARS-CoV-2 infection to host cells
Wang, K., Chen, W., Zhang, Z., Deng, Y., Lian, J., Du, P. F., Wei, D., Yang, Z., Sun, X., Gong, L., et al. (2020) · Signal Transduction and Targeted Therapy · doi:10.1038/s41392-020-00426-x · Cited by 1,592 · see citing works
Real-time tracking of self-reported symptoms to predict potential COVID-19
Menni, C., Valdes, A. M., Freidin, M. B., Sudre, C. H., Nguyen, L. H., Drew, D. A., Ganesh, S., Varsavsky, T., Cardoso, M. J., El-Sayed Moustafa, J. S., et al. (2020) · Nature Medicine · doi:10.1038/s41591-020-0916-2 · Cited by 1,517 · see citing works
SARS-CoV-2 Reverse Genetics Reveals a Variable Infection Gradient in the Respiratory Tract
Hou, Y. J., Okuda, K., Edwards, C. E., Martinez, D. R., Asakura, T., Dinnon, K. H., Kato, T., Lee, R. E., Yount, B. L., Mascenik, T. M., et al. (2020) · Cell · doi:10.1016/j.cell.2020.05.042 · Cited by 1,488 · see citing works
Meinhardt, J., Radke, J., Dittmayer, C., Franz, J., Thomas, C., Mothes, R., Laue, M., Schneider, J., Brünink, S., Greuel, S., et al. (2021) · Nature Neuroscience · doi:10.1038/s41593-020-00758-5 · Cited by 1,458 · see citing works
The Impact of Mutations in SARS-CoV-2 Spike on Viral Infectivity and Antigenicity
Li, Q., Wu, J., Nie, J., Zhang, L., Hao, H., Liu, S., Zhao, C., Zhang, Q., Liu, H., Nie, L., et al. (2020) · Cell · doi:10.1016/j.cell.2020.07.012 · Cited by 1,420 · see citing works
Friedrich, G., & Soriano, P. M. (1991) · Genes & Development · doi:10.1101/gad.5.9.1513 · Cited by 1,403 · see citing works
SARS-CoV-2 spike-protein D614G mutation increases virion spike density and infectivity
Zhang, L., Jackson, C. B., Mou, H., Ojha, A., Peng, H., Quinlan, B. D., Rangarajan, E. S., Pan, A., Vanderheiden, A., Suthar, M. S., et al. (2020) · Nature Communications · doi:10.1038/s41467-020-19808-4 · Cited by 1,387 · see citing works
Multiple organ infection and the pathogenesis of SARS
Gu, J., Gong, E., Zhang, B., Zheng, J., Gao, Z., Zhong, Y., Zou, W., Zhan, J., Wang, S., Xie, Z., et al. (2005) · The Journal of Experimental Medicine · doi:10.1084/jem.20050828 · Cited by 1,379 · see citing works
Pathogenesis and transmission of SARS-CoV-2 in golden hamsters
Sia, S. F., Yan, L.-M., Chin, A. W. H., Fung, K., Choy, K.-T., Wong, A. Y. L., Kaewpreedee, P., Perera, R. A. P. M., Poon, L. L. M., Nicholls, J. M., et al. (2020) · Nature · doi:10.1038/s41586-020-2342-5 · Cited by 1,303 · see citing works
Netland, J., Meyerholz, D. K., Moore, S., Cassell, M., & Perlman, S. (2008) · Journal of Virology · doi:10.1128/jvi.00737-08 · Cited by 1,293 · see citing works
Intranasal delivery of biologics to the central nervous system
Lochhead, J. J., & Thorne, R. G. (2012) · Advanced Drug Delivery Reviews · doi:10.1016/j.addr.2011.11.002 · Cited by 1,214 · see citing works
Brann, D. H., Tsukahara, T., Weinreb, C., Lipovsek, M., Van den Berge, K., Gong, B., Chance, R., Macaulay, I. C., Chou, H.-J., Fletcher, R. B., et al. (2020) · Science Advances · doi:10.1126/sciadv.abc5801 · Cited by 1,198 · see citing works
The pathogenicity of SARS-CoV-2 in hACE2 transgenic mice
Bao, L., Deng, W., Huang, B., Gao, H., Liu, J., Ren, L., Wei, Q., Yu, P., Xu, Y., Qi, F., et al. (2020) · Nature · doi:10.1038/s41586-020-2312-y · Cited by 1,126 · see citing works
Clinical Features of 69 Cases With Coronavirus Disease 2019 in Wuhan, China
Wang, Z., Yang, B., Li, Q., Wen, L., & Zhang, R. (2020) · Clinical Infectious Diseases · doi:10.1093/cid/ciaa272 · Cited by 1,063 · see citing works
Desforges, M., Le Coupanec, A., Dubeau, P., Bourgouin, A., Lajoie, L., Dubé, M., & Talbot, P. J. (2019) · Viruses · doi:10.3390/v12010014 · Cited by 1,048 · see citing works
Phylogenetic network analysis of SARS-CoV-2 genomes
Forster, P., Forster, L., Renfrew, C., & Förster, M. (2020) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.2004999117 · Cited by 1,026 · see citing works
McCray, P. B., Pewe, L., Wohlford-Lenane, C., Hickey, M., Manzel, L., Shi, L., Netland, J., Jia, H. P., Halabi, C., Sigmund, C. D., et al. (2007) · Journal of Virology · doi:10.1128/jvi.02012-06 · Cited by 1,010 · see citing works
Receptor and viral determinants of SARS‐coronavirus adaptation to human ACE2
Li, W., Zhang, C., Sui, J., Kuhn, J. H., Moore, M. J., Luo, S., Wong, S.-K., Huang, I., Xu, K., Vasilieva, N. Y., et al. (2005) · The EMBO Journal · doi:10.1038/sj.emboj.7600640 · Cited by 976 · see citing works
Central nervous system involvement by severe acute respiratory syndrome coronavirus-2 (SARS-CoV-2)
Paniz‐Mondolfi, A., Bryce, C., Grimes, Z., Gordon, R. E., Reidy, J., Lednicky, J., Sordillo, E. M., & Fowkes, M. (2020) · Journal of Medical Virology · doi:10.1002/jmv.25915 · Cited by 975 · see citing works
Zubair, A. S., McAlpine, L. S., Gardin, T., Farhadian, S., Kuruvilla, D. E., & Spudich, S. (2020) · JAMA Neurology · doi:10.1001/jamaneurol.2020.2065 · Cited by 923 · see citing works
Comparative pathogenesis of COVID-19, MERS, and SARS in a nonhuman primate model
Rockx, B., Kuiken, T., Herfst, S., Bestebroer, T., Lamers, M. M., Oude Munnink, B. B., de Meulder, D., van Amerongen, G., van den Brand, J., Okba, N. M. A., et al. (2020) · Science · doi:10.1126/science.abb7314 · Cited by 901 · see citing works
Cao, Y., Li, L., Feng, Z., Wan, S., Huang, P., Sun, X., Wen, F., Huang, X., Ning, G., & Wang, W. (2020) · Cell Discovery · doi:10.1038/s41421-020-0147-1 · Cited by 865 · see citing works
Position paper on olfactory dysfunction
Hummel, T. R., Whitcroft, K. L., Andrews, P. J., Altundağ, A., Cinghi, C., Costanzo, R. M., Damm, M., Frasnelli, J., Gudziol, H., Gupta, N., et al. (2017) · Rhinology Journal · doi:10.4193/rhino16.248 · Cited by 846 · see citing works
SARS-CoV-2 invades host cells via a novel route: CD147-spike proteinPreprint
Wang, K., Chen, W., Zhou, Y., et al. (2020) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2020.03.14.988345 · Cited by 698 · see citing works
Anosmia and Ageusia: Common Findings in COVID ‐19 Patients
Vaira, L. A., Salzano, G., Deiana, G., & RIU, G. D. (2020) · The Laryngoscope · doi:10.1002/lary.28692 · Cited by 659 · see citing works
Grant, M. C., Geoghegan, L., Arbyn, M., Mohammed, Z., McGuinness, L. A., Clarke, E. L., & Wade, R. G. (2020) · PLoS ONE · doi:10.1371/journal.pone.0234765 · Cited by 652 · see citing works
A Mouse Model of SARS-CoV-2 Infection and Pathogenesis
Sun, S.-H., Chen, Q., Gu, H.-J., Yang, G., Wang, Y.-X., Huang, X.-Y., Liu, S.-S., Zhang, N.-N., Li, X.-F., Xiong, R., et al. (2020) · Cell Host & Microbe · doi:10.1016/j.chom.2020.05.020 · Cited by 617 · see citing works
Tong, J. Y., Wong, A., Zhu, D., Fastenberg, J. H., & Tham, T. (2020) · Otolaryngology · doi:10.1177/0194599820926473 · Cited by 614 · see citing works
CD209L (L-SIGN) is a receptor for severe acute respiratory syndrome coronavirus
Jeffers, S. A., Tusell, S. M., Gillim-Ross, L., Hemmila, E. M., Achenbach, J. E., Babcock, G. J., Thomas, W. D., Thackray, L. B., Young, M. D., Mason, R. J., et al. (2004) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0403812101 · Cited by 606 · see citing works
The D614G mutation in the SARS-CoV-2 spike protein reduces S1 shedding and increases infectivityPreprint
Zhang, L., Jackson, C. B., Mou, H., et al. (2020) · bioRxiv · doi:10.1101/2020.06.12.148726 · Cited by 576 · see citing works
Pathogenesis of SARS-CoV-2 in Transgenic Mice Expressing Human Angiotensin-Converting Enzyme 2
Jiang, R.-D., Liu, M.-Q., Chen, Y., Shan, C., Zhou, Y.-W., Shen, X.-R., Li, Q., Zhang, L., Zhu, Y., Si, H.-R., et al. (2020) · Cell · doi:10.1016/j.cell.2020.05.027 · Cited by 541 · see citing works
Prevalence and Duration of Acute Loss of Smell or Taste in COVID-19 Patients
Lee, Y., Min, P., Lee, S., & Kim, S.-W. (2020) · Journal of Korean Medical Science · doi:10.3346/jkms.2020.35.e174 · Cited by 528 · see citing works
Neural regeneration and the peripheral olfactory system
Schwob, J. E. (2002) · The Anatomical Record · doi:10.1002/ar.10047 · Cited by 506 · see citing works
More Than Smell—COVID-19 Is Associated With Severe Impairment of Smell, Taste, and Chemesthesis
Parma, V., Ohla, K., Veldhuizen, M. G., Niv, M. Y., Kelly, C. E., Bakke, A. J., Cooper, K. W., Bouysset, C., Pirastu, N., Dibattista, M., et al. (2020) · Chemical Senses · doi:10.1093/chemse/bjaa041 · Cited by 503 · see citing works
Axonal Transport Enables Neuron-to-Neuron Propagation of Human Coronavirus OC43
Dubé, M., Le Coupanec, A., Wong, A. H. M., Rini, J. M., Desforges, M., & Talbot, P. J. (2018) · Journal of Virology · doi:10.1128/jvi.00404-18 · Cited by 452 · see citing works
Smell and Taste Dysfunction in Patients With COVID-19: A Systematic Review and Meta-analysis
Agyeman, A. A., Chin, K. L., Landersdorfer, C. B., Liew, D., & Ofori‐Asenso, R. (2020) · Mayo Clinic Proceedings · doi:10.1016/j.mayocp.2020.05.030 · Cited by 452 · see citing works
Vaira, L. A., Deiana, G., Fois, A. G., Pirina, P., Madeddu, G., VITO, A. D., Babudieri, S., Petrocelli, M., Serra, A., Bussu, F., et al. (2020) · Head & Neck · doi:10.1002/hed.26204 · Cited by 440 · see citing works
Generation of a Broadly Useful Model for COVID-19 Pathogenesis, Vaccination, and Treatment
Sun, J., Zhuang, Z., Zheng, J. H., Li, K., Wong, R. L.-Y., Liu, D., Huang, J., He, J., Zhu, A., Zhao, J., et al. (2020) · Cell · doi:10.1016/j.cell.2020.06.010 · Cited by 434 · see citing works
Isolated Sudden Onset Anosmia in COVID-19 Infection. A Novel Syndrome?
Gane, S. B., Kelly, C., & Hopkins, C. (2020) · Rhinology Journal · doi:10.4193/rhin20.114 · Cited by 430 · see citing works
Bilińska, K., Jakubowska, P., von Bartheld, C. S., & Butowt, R. (2020) · ACS Chemical Neuroscience · doi:10.1021/acschemneuro.0c00210 · Cited by 430 · see citing works
Self-citationAsselta, R., Paraboschi, E. M., Mantovani, A., & Duga, S. (2020) · Aging · doi:10.18632/aging.103415 · Cited by 422 · see citing works
SARS-like WIV1-CoV poised for human emergence
Menachery, V. D., Yount, B. L., Sims, A. C., Debbink, K., Agnihothram, S. S., Gralinski, L. E., Graham, R. L., Scobey, T., Plante, J. A., Royal, S. R., et al. (2016) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1517719113 · Cited by 418 · see citing works
COVID-19 and anosmia: A review based on up-to-date knowledge
Meng, X., Deng, Y., Dai, Z., & Meng, Z. (2020) · American Journal of Otolaryngology · doi:10.1016/j.amjoto.2020.102581 · Cited by 407 · see citing works
Zhou, Z., Kang, H., Li, S., & Zhao, X. (2020) · Journal of Neurology · doi:10.1007/s00415-020-09929-7 · Cited by 397 · see citing works
van Riel, D., Verdijk, R., & Kuiken, T. (2015) · The Journal of Pathology · doi:10.1002/path.4461 · Cited by 394 · see citing works
COVID‐19 Anosmia Reporting Tool: Initial Findings
Kaye, R. J., Chang, C. W. D., Kazahaya, K., Brereton, J. M., & Denneny, J. C. (2020) · Otolaryngology · doi:10.1177/0194599820922992 · Cited by 389 · see citing works
Sudden and Complete Olfactory Loss of Function as a Possible Symptom of COVID-19
Eliezer, M., Hautefort, C., Hamel, A.-L., Verillaud, B., Herman, P., Houdart, E., & Eloit, C. (2020) · JAMA Otolaryngology–Head & Neck Surgery · doi:10.1001/jamaoto.2020.0832 · Cited by 373 · see citing works
Politi, L. S., Salsano, E., & Grimaldi, M. (2020) · JAMA Neurology · doi:10.1001/jamaneurol.2020.2125 · Cited by 369 · see citing works
Self‐reported olfactory loss associates with outpatient clinical course in COVID‐19
Yan, C. H., Faraji, F., Prajapati, D. P., Ostrander, B. T., & DeConde, A. S. (2020) · International Forum of Allergy & Rhinology · doi:10.1002/alr.22592 · Cited by 359 · see citing works
Making Sense of Mutation: What D614G Means for the COVID-19 Pandemic Remains Unclear
Grubaugh, N. D., Hanage, W. P., & Rasmussen, A. L. (2020) · Cell · doi:10.1016/j.cell.2020.06.040 · Cited by 359 · see citing works
Smell and taste dysfunction in patients with COVID-19
Xydakis, M. S., Dehgani‐Mobaraki, P., Holbrook, E. H., Geisthoff, U. W., Bauer, C. A., Hautefort, C., Herman, P., Manley, G. T., Lyon, D. M., & Hopkins, C. L. (2020) · The Lancet Infectious Diseases · doi:10.1016/s1473-3099(20)30293-0 · Cited by 352 · see citing works
Butowt, R., & Bilinska, K. (2020) · ACS Chemical Neuroscience · doi:10.1021/acschemneuro.0c00172 · Cited by 346 · see citing works
Self-citationCOVID-19 and the Chemical Senses: Supporting Players Take Center Stage
Cooper, K. W., Brann, D. H., Farruggia, M. C., Bhutani, S., Pellegrino, R., Tsukahara, T., Weinreb, C., Joseph, P. V., Larson, E. D., Parma, V., et al. (2020) · Neuron · doi:10.1016/j.neuron.2020.06.032 · Cited by 335 · see citing works
Presentation of New Onset Anosmia During the COVID-19 Pandemic
Hopkins, C., Šurda, P., & Kumar, B. N. (2020) · Rhinology Journal · doi:10.4193/rhin20.116 · Cited by 327 · see citing works
No evidence for increased transmissibility from recurrent mutations in SARS-CoV-2
van Dorp, L., Richard, D., Tan, C. C. S., Shaw, L. P., Acman, M., & Balloux, F. (2020) · Nature Communications · doi:10.1038/s41467-020-19818-2 · Cited by 310 · see citing works
Bryche, B., Deliot, A. S.-A., Murri, S., Lacôte, S., Pulido, C., Gouilh, M. A., Lesellier, S., Servat, A., Wasniewski, M., Meyer, E. P., et al. (2020) · Brain Behavior and Immunity · doi:10.1016/j.bbi.2020.06.032 · Cited by 306 · see citing works
COVID-19 and the endocrine system: exploring the unexplored
Pal, R., & Banerjee, M. (2020) · Journal of Endocrinological Investigation · doi:10.1007/s40618-020-01276-8 · Cited by 292 · see citing works
Fodoulian, L., Tuberosa, J., Rossier, D., Boillat, M., Kan, C., Pauli, V., Egervari, K., Lobrinus, J. A., Landis, B. N., Carleton, A., et al. (2020) · doi:10.1101/2020.03.31.013268 · Cited by 286 · see citing works
Potential pathogenesis of ageusia and anosmia in COVID‐19 patients
Vaira, L. A., Salzano, G., Fois, A. G., Piombino, P., & RIU, G. D. (2020) · International Forum of Allergy & Rhinology · doi:10.1002/alr.22593 · Cited by 283 · see citing works
von Bartheld, C. S., Hagen, M. M., & Butowt, R. (2020) · ACS Chemical Neuroscience · doi:10.1021/acschemneuro.0c00460 · Cited by 283 · see citing works
Self-citationReconstitution of the rat olfactory epithelium after methyl bromide‐induced lesion
Schwob, J. E., Youngentob, S. L., & Mezza, R. C. (1995) · The Journal of Comparative Neurology · doi:10.1002/cne.903590103 · Cited by 267 · see citing works
Li, Z., Liu, T., Yang, N., Han, D., Mi, X., Li, Y., Liu, K., Vuylsteke, A., Xiang, H., & Guo, X. (2020) · Frontiers of Medicine · doi:10.1007/s11684-020-0786-5 · Cited by 267 · see citing works
Benetti, E., Tita, R., Spiga, O., Ciolfi, A., Birolo, G., Bruselles, A., Doddato, G., Giliberti, A., Marconi, C., Musacchia, F., et al. (2020) · European Journal of Human Genetics · doi:10.1038/s41431-020-0691-z · Cited by 259 · see citing works
Single-cell analysis of olfactory neurogenesis and differentiation in adult humans
Durante, M. A., Kurtenbach, S., Sargi, Z. B., Harbour, J. W., Choi, R., Kurtenbach, S., Goss, G. M., Matsunami, H., & Goldstein, B. J. (2020) · Nature Neuroscience · doi:10.1038/s41593-020-0587-9 · Cited by 254 · see citing works
Yang, X. H., Deng, W., Tong, Z., Liu, Y., Zhang, L. F., Zhu, H., Gao, H., Huang, L., Liu, Y. I., Ma, C. M., et al. (2007) · PubMed · Cited by 252 · see citing works
Chen, M., Shen, W., Rowan, N. R., Kulaga, H. M., Hillel, A. T., Ramanathan, M., & Lane, A. P. (2020) · European Respiratory Journal · doi:10.1183/13993003.01948-2020 · Cited by 246 · see citing works
Tseng, C.-T. K., Huang, C., Newman, P. C., Wang, N., Narayanan, K., Watts, D. M., Makino, S., Packard, M. M., Zaki, S. R., Chan, T., et al. (2006) · Journal of Virology · doi:10.1128/jvi.01702-06 · Cited by 244 · see citing works
A lifetime of neurogenesis in the olfactory system
Brann, J. H., & Firestein, S. (2014) · Frontiers in Neuroscience · doi:10.3389/fnins.2014.00182 · Cited by 238 · see citing works
Utility of hyposmia and hypogeusia for the diagnosis of COVID-19
Bénézit, F., Turnier, P. L., Declerck, C., Paillé, C., Revest, M., Dubée, V., Tattevin, P., Arvieux, C., Baldeyrou, M., Chapplain, J.-M., et al. (2020) · The Lancet Infectious Diseases · doi:10.1016/s1473-3099(20)30297-8 · Cited by 213 · see citing works
Olfaction and Its Alteration by Nasal Obstruction, Rhinitis, and Rhinosinusitis
Doty, R. L., & Mishra, A. (2001) · The Laryngoscope · doi:10.1097/00005537-200103000-00008 · Cited by 208 · see citing works
Hannum, M. E., Ramirez, V. A., Lipson, S. J., Herriman, R. D., Toskala, A. K., Lin, C., Joseph, P. V., & Reed, D. R. (2020) · Chemical Senses · doi:10.1093/chemse/bjaa064 · Cited by 204 · see citing works
Loss of Smell and Taste in 2013 European Patients With Mild to Moderate COVID-19
Lechien, J. R., Chiesa-Estomba, C. M., Hans, S., Barillari, M. R., Jouffe, L., & Saussez, S. (2020) · Annals of Internal Medicine · doi:10.7326/m20-2428 · Cited by 188 · see citing works
Heydel, J., Coelho, A., Thiebaud, N., Legendre, A., Bon, A. L., Fauré, P., Neiers, F., Artur, Y., Golebiowski, J., & Briand, L. V. (2013) · The Anatomical Record · doi:10.1002/ar.22735 · Cited by 172 · see citing works
Serrano-Castro, P. J., Estivill‐Torrús, G., Cabezudo‐García, P., Bueno, J. A. R., Ciano-Petersen, N. L., Aguilar-Castillo, M. J., Suárez-Pérez, J., Jiménez-Hernández, M. D., Moya-Molina, M. Á., Oliver‐Martos, B., et al. (2020) · Neurología · doi:10.1016/j.nrl.2020.04.002 · Cited by 172 · see citing works
Qiu, C., Cui, C., Hautefort, C., Haehner, A., Zhao, J. F., Yao, Q., Zeng, H., Nisenbaum, E. J., Liu, L., Zhao, Y., et al. (2020) · Otolaryngology · doi:10.1177/0194599820934376 · Cited by 171 · see citing works
Wang, L., Shen, Y., Li, M., Chuang, H.-Y., Ye, Y., Zhao, H., & Wang, H. (2020) · Journal of Neurology · doi:10.1007/s00415-020-09974-2 · Cited by 171 · see citing works
Anosmia in COVID-19 Associated with Injury to the Olfactory Bulbs Evident on MRI
Aragão, M. F. V. V., Gouveia, M. D. C. L., Filho, O. Q. C., Fonseca, T., & Valênça, M. M. (2020) · American Journal of Neuroradiology · doi:10.3174/ajnr.a6675 · Cited by 169 · see citing works
Saraiva, L. R., Ibarra-Soria, X., Khan, M., Omura, M., Scialdone, A., Mombaerts, P., Marioni, J. C., & Logan, D. W. (2015) · Scientific Reports · doi:10.1038/srep18178 · Cited by 168 · see citing works
Proinflammatory Cytokines in the Olfactory Mucosa Result in COVID-19 Induced Anosmia
Torabi, A., Mohammadbagheri, E., Dilmaghani, N. A., Bayat, A., Fathi, M., Vakili, K. G., Alizadeh, R., Rezaeimirghaed, O., Hajiesmaeili, M., Ramezani, M., et al. (2020) · ACS Chemical Neuroscience · doi:10.1021/acschemneuro.0c00249 · Cited by 168 · see citing works
Ou, J., Zhou, Z., Dai, R., Zhang, J., Zhao, S., Wu, X., Lan, W., Ren, Y., Cui, L., Lan, Q., et al. (2021) · Journal of Virology · doi:10.1128/jvi.00617-21 · Cited by 162 · see citing works
Neural Map Formation in the Mouse Olfactory System
Sakano, H. (2010) · Neuron · doi:10.1016/j.neuron.2010.07.003 · Cited by 161 · see citing works
Neuromechanisms of SARS-CoV-2: A Review
DosSantos, M. F. H., Devalle, S., Aran, V., Capra, D., Roque, N. R., Coelho‐Aguiar, J. D. M., Spohr, T. C. L. D. S. E., Subilhaga, J. G., Pereira, C. M., Meira, I. D., et al. (2020) · Frontiers in Neuroanatomy · doi:10.3389/fnana.2020.00037 · Cited by 154 · see citing works
Olfactory neuropathy in severe acute respiratory syndrome: report of A case.
Hwang, C. (2006) · PubMed · Cited by 150 · see citing works
A primer on viral‐associated olfactory loss in the era of COVID‐19
Soler, Z. M., Patel, Z. M., Turner, J. H., & Holbrook, E. H. (2020) · International Forum of Allergy & Rhinology · doi:10.1002/alr.22578 · Cited by 146 · see citing works
Norwood, J. N., Zhang, Q., Card, D., Craine, A., Ryan, T. M., & Drew, P. J. (2019) · eLife · doi:10.7554/elife.44278 · Cited by 144 · see citing works
Meinhardt, J., Radke, J., Dittmayer, C., et al. (2020) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2020.06.04.135012 · Cited by 137 · see citing works
Effect of olfactory bulb ablation on spread of a neurotropic coronavirus into the mouse brain.
Perlman, S. M., Evans, G., & Afifi, A. K. (1990) · The Journal of Experimental Medicine · doi:10.1084/jem.172.4.1127 · Cited by 129 · see citing works
Williams, F. M. K., Freidin, M. B., Mangino, M., Couvreur, S., Visconti, A., Bowyer, R. C. E., Roy, C. I. L., Falchi, M., Mompeó, O., Sudre, C. H., et al. (2020) · Twin Research and Human Genetics · doi:10.1017/thg.2020.85 · Cited by 128 · see citing works
Olfactory Dysfunction: A Highly Prevalent Symptom of COVID‐19 With Public Health Significance
Sedaghat, A. R., Gengler, I. M., & Speth, M. M. (2020) · Otolaryngology · doi:10.1177/0194599820926464 · Cited by 123 · see citing works
Jia, Y., Shen, G., Nguyen, S. A., Zhang, Y., Huang, K., Ho, H.-Y., Hor, W.-S., Yang, C.-H., Bruning, J. B., Li, C., et al. (2020) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2020.04.09.034942 · Cited by 121 · see citing works
Plakhov, I. V., Arlund, E. E., Aoki, C. J., & Reiss, C. S. (1995) · Virology · doi:10.1006/viro.1995.1252 · Cited by 119 · see citing works
Smell and taste disorders during COVID ‐19 outbreak: Cross‐sectional study on 355 patients
Dell’Era, V., Farri, F., Garzaro, G., Gatto, M., Valletti, P. A., & Garzaro, M. (2020) · Head & Neck · doi:10.1002/hed.26288 · Cited by 108 · see citing works
Sauvé, F., Nampoothiri, S. S., Clarke, S. A., Fernandois, D., Coêlho, C. F. F., Dewisme, J., Mills, E., Ternier, G., Cotellessa, L., Iglesias, C., et al. (2023) · EBioMedicine · doi:10.1016/j.ebiom.2023.104784 · Cited by 106 · see citing works
Ou, J., Zhou, Z., Dai, R., et al. (2020) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2020.03.15.991844 · Cited by 100 · see citing works
Herpesviruses hijack host exosomes for viral pathogenesis
Sadeghipour, S., & Mathias, R. A. (2017) · Seminars in Cell and Developmental Biology · doi:10.1016/j.semcdb.2017.03.005 · Cited by 97 · see citing works
18FDG PET/CT Scan Reveals Hypoactive Orbitofrontal Cortex in Anosmia of COVID-19
Karimi‐Galougahi, M., Yousefi-Koma, A., Karam, M. B., Raad, N., & Haseli, S. (2020) · Academic Radiology · doi:10.1016/j.acra.2020.04.030 · Cited by 95 · see citing works
Larsell, O. (1950) · Annals of Otology Rhinology & Laryngology · doi:10.1177/000348945005900211 · Cited by 93 · see citing works
No evidence for increased transmissibility from recurrent mutations in SARS-CoV-2Preprint
van Dorp, L., Richard, D., Tan, C. C. S., et al. (2020) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2020.05.21.108506 · Cited by 92 · see citing works
Quantifying additional COVID-19 symptoms will save lives
Menni, C., Sudre, C. H., Steves, C. J., Sebastien Ourselin, A., & Spector, T. D. (2020) · The Lancet · doi:10.1016/s0140-6736(20)31281-2 · Cited by 92 · see citing works
Naik, S. B., Shetty, N., & Maben, E. V. S. (2010) · European Journal of Internal Medicine · doi:10.1016/j.ejim.2010.01.017 · Cited by 91 · see citing works
COVID-19 and anosmia in Tehran, Iran
Gilani, S., Roditi, R. E., & Naraghi, M. (2020) · Medical Hypotheses · doi:10.1016/j.mehy.2020.109757 · Cited by 91 · see citing works
Evidence of SARS-CoV2 Entry Protein ACE2 in the Human Nose and Olfactory Bulb
Klingenstein, M., Klingenstein, S., Neckel, P. H., Mack, A. F., Wagner, A., Kleger, A., Liebau, S., & Milazzo, A. (2020) · Cells Tissues Organs · doi:10.1159/000513040 · Cited by 91 · see citing works
Williams, F. M. K., Freidin, M. B., Mangino, M., et al. (2020) · medRxiv · doi:10.1101/2020.04.22.20072124 · Cited by 87 · see citing works
The role of self-reported smell and taste disorders in suspected COVID‑19
Printza, A., & Constantinidis, J. (2020) · European Archives of Oto-Rhino-Laryngology · doi:10.1007/s00405-020-06069-6 · Cited by 85 · see citing works
Sustentacular Cell Enwrapment of Olfactory Receptor Neuronal Dendrites: An Update
Liang, F. (2020) · Genes · doi:10.3390/genes11050493 · Cited by 77 · see citing works
Safety profiles of the angiotensin converting enzyme inhibitors captopril and enalapril
Irvin, J. D., & Viau, J. M. (1986) · The American Journal of Medicine · doi:10.1016/0002-9343(86)90945-9 · Cited by 73 · see citing works
Strafella, C., Caputo, V., Termine, A., Barati, S., Gambardella, S., Borgiani, P., Caltagirone, C., Novelli, G., Giardina, E., & Cascella, R. (2020) · Genes · doi:10.3390/genes11070741 · Cited by 70 · see citing works
Briguglio, M., Bona, A. R., Porta, M., Dell’Osso, B. M., Pregliasco, F. E., & Banfi, G. (2020) · Frontiers in Physiology · doi:10.3389/fphys.2020.00671 · Cited by 69 · see citing works
Development of the Nervus Terminalis in Mammals Including Toothed Whales and Humans
Oelschläger, H., Buhl, E. H., & Dann, J. F. (1987) · Annals of the New York Academy of Sciences · doi:10.1111/j.1749-6632.1987.tb36316.x · Cited by 67 · see citing works
Taste and smell as chemosensory dysfunctions in COVID-19 infection.
Passarelli, P. C., López, M. A., Bonaviri, G. N. M., Garcı́a-Godoy, F., & D’Addona, A. (2020) · PubMed · Cited by 67 · see citing works
Genomics of mature and immature olfactory sensory neurons
Nickell, M. D., Breheny, P. J., Stromberg, A. J., & McClintock, T. S. (2012) · The Journal of Comparative Neurology · doi:10.1002/cne.23052 · Cited by 66 · see citing works
COVID-19 Pulmonary and Olfactory Dysfunctions: Is the Chemokine CXCL10 the Common Denominator?
Oliviero, A., de Castro, F., Coperchini, F., Chiovato, L., & Rotondi, M. (2020) · The Neuroscientist · doi:10.1177/1073858420939033 · Cited by 64 · see citing works
Wang, Z., Zhou, J., Marshall, B., Rekaya, R., Ye, K., & Liu, H. (2020) · ACS Pharmacology & Translational Science · doi:10.1021/acsptsci.0c00062 · Cited by 64 · see citing works
The Cellular basis of loss of smell in 2019-nCoV-infected individuals
Gupta, K., Mohanty, S. K., Mittal, A., Kalra, S., Kumar, S., Mishra, T., Ahuja, J., Sengupta, D., & Ahuja, G. (2020) · Briefings in Bioinformatics · doi:10.1093/bib/bbaa168 · Cited by 62 · see citing works
Internalization of odorant-binding proteins into the mouse olfactory epithelium
Strotmann, J. M., & Breer, H. (2011) · Histochemistry and Cell Biology · doi:10.1007/s00418-011-0850-y · Cited by 57 · see citing works
Topographical representation of odor hedonics in the olfactory bulb
Kermen, F., Midroit, M., Kuczewski, N., Forest, J., Thévenet, M., Sacquet, J., Benetollo, C., Richard, M., Didier, A., & Mandairon, N. (2016) · Nature Neuroscience · doi:10.1038/nn.4317 · Cited by 55 · see citing works
Krolewski, R. C., Packard, A. I., & Schwob, J. E. (2012) · The Journal of Comparative Neurology · doi:10.1002/cne.23204 · Cited by 54 · see citing works
Jia, C., Roman, C., & Hegg, C. C. (2010) · Toxicological Sciences · doi:10.1093/toxsci/kfq071 · Cited by 54 · see citing works
Rodriguez, S., Cao, L., Rickenbacher, G. T., Benz, E. G., Magdamo, C., Gomez, L. A. R., Holbrook, E. H., Albers, A. D., Gallagher, R., Westover, M. B., et al. (2020) · medRxiv · doi:10.1101/2020.06.14.20131128 · Cited by 50 · see citing works
Sato, T., Ueha, R., Goto, T., Yamauchi, A., Kondo, K., & Yamasoba, T. (2020) · The Laryngoscope · doi:10.1002/lary.29132 · Cited by 49 · see citing works
Villar, P. S., Delgado, R., Vergara, C., Reyes, J. G., & Bacigalupo, J. (2017) · Journal of Neuroscience · doi:10.1523/jneurosci.2640-16.2017 · Cited by 47 · see citing works
Paranasal sinuses computed tomography findings in anosmia of COVID-19
Naeini, A. S., Karimi‐Galougahi, M., Raad, N., Ghorbani, J., Taraghi, A., Haseli, S., Mehrparvar, G., & Karam, M. B. (2020) · American Journal of Otolaryngology · doi:10.1016/j.amjoto.2020.102636 · Cited by 47 · see citing works
Tudrej, B. V., Sebo, P., Lourdaux, J., Cuzin, C., Floquet, M., Haller, D. M., & Maisonneuve, H. (2020) · Journal of General Internal Medicine · doi:10.1007/s11606-020-05933-9 · Cited by 45 · see citing works
Zonal ablation of the olfactory sensory neuroepithelium of the mouse: effects on odorant detection
Vedin, V., Slotnick, B. M., & Berghard, A. (2004) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.2004.03634.x · Cited by 43 · see citing works
Phelan, J. E., Deelder, W., Ward, D., Campino, S. G., Hibberd, M. L., & Clark, T. G. (2020) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2020.04.28.066977 · Cited by 28 · see citing works
Qiu, C., Cui, C., Hautefort, C., et al. (2020) · medRxiv · doi:10.1101/2020.05.13.20100198 · Cited by 25 · see citing works
Strafella, C., Caputo, V., Termine, A., et al. (2020) · doi:10.21203/rs.3.rs-28871/v1 · Cited by 21 · see citing works
Ueha, R., Kondo, K., Kagoya, R., Shichino, S., Ueha, S., & Yamasoba, T. (2020) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2020.05.15.097352 · Cited by 18 · see citing works
Sayın, İ., & Yazıcı, Z. M. (2020) · ACS Chemical Neuroscience · doi:10.1021/acschemneuro.0c00296 · Cited by 18 · see citing works
The Nervus Terminalis in the Mouse: Light and Electron Microscopic Immunocytochemical Studies
Jennes, L. (1987) · Annals of the New York Academy of Sciences · doi:10.1111/j.1749-6632.1987.tb36295.x · Cited by 16 · see citing works
Baxter, B. D., Larson, E. D., Merle, L., Feinstein, P. G., Polese, A. G., Bubak, A. N., Niemeyer, C. S., Hassell, J., Shepherd, D., Ramakrishnan, V. R., et al. (2020) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2020.05.14.096016 · Cited by 15 · see citing works
The molecular basis of loss of smell in 2019-nCoV infected individualsPreprint
Gupta, K., Mohanty, S. K., Kalra, S., Mittal, A., Mishra, T., Ahuja, J., Sengupta, D., & Ahuja, G. (2020) · doi:10.21203/rs.3.rs-19884/v1 · Cited by 11 · see citing works
Characteristics of Impaired Chemosensory Function in Hospitalized COVID-19 PatientsPreprint
Bertlich, M., Stihl, C., Weiss, B. G., Canis, M., Haubner, F., & Ihler, F. (2020) · SSRN Electronic Journal · doi:10.2139/ssrn.3576889 · Cited by 10 · see citing works
Walsh‐Messinger, J., Kaouk, S., Manis, H., Kaye, R. J., Cecchi, G., Meyer, P., & Malaspina, D. (2021) · European Journal of Neuroscience · doi:10.1111/ejn.15430 · Cited by 10 · see citing works
Tudrej, B. V., Sebo, P., Lourdaux, J., et al. (2020) · doi:10.21203/rs.3.rs-28701/v1 · Cited by 10 · see citing works
Lovato, A., Antonini, A., & de Filippis, C. (2020) · Otolaryngology · doi:10.1177/0194599820934761 · Cited by 5 · see citing works
Flagged first, then by citations
Research works printed but not linked: 4
- Dos Santos NPC, Khayat AS, Rodrigues JCG, Pinto P, de Araujo GS, Pastana LF, and others. 2020. TMPRSS2 variants and their susceptibility to COVID-19: focus in East Asian and European populations. MedRxiv Preprint. 10.1101/2020.06.09.20126680 [DOI] [Google Scholar] · DOI
- Nampoothiri S, Sauve S, Ternier G, Fernandois D, Coelho C, Imbernon M, and others. 2020. The hypothalamus as a hub for putative SARS-CoV-2 brain infection. bioRxiv preprint. doi: 10.1101/2020.06.08.139329 [DOI] [Google Scholar] · DOI
- Sato T, Ueha R, Goto T, Yamauchi A, Kondo K, Yamasoba T. 2020. Expression of ACE2 and TMPRSS2 proteins in the upper and lower aerodigestive tracts of rats. Preprint bioRxiv. doi: 10.1101/2020.05.14.097204. [DOI] [PubMed] [Google Scholar] · DOI
- Walsh-Messinger J, Sahar K, Manis H, Kaye R, Cecchi G, Meyer P, and others. 2020. Standardized testing demonstrates altered odor detection sensitivity and hedonics in asymptomatic college students as SARS-CoV-2 emerged locally. Preprint medRxiv. doi: 10.1101/2020.06.17.20106302 [DOI] · DOI
Cited by
Sorted by citations
The oral microbiome: Role of key organisms and complex networks in oral health and disease
Sedghi, L., DiMassa, V., Harrington, A., Lynch, S. V., & Kapila, Y. L. (2021) · Periodontology 2000 · doi:10.1111/prd.12393 · Cited by 755 · see citing works
Safety, tolerability and viral kinetics during SARS-CoV-2 human challenge in young adults
Killingley, B., Mann, A., Kalinova, M., Boyers, A., Goonawardane, N., Zhou, J., Lindsell, K., Hare, S. S., Brown, J. C., Frise, R., et al. (2022) · Nature Medicine · doi:10.1038/s41591-022-01780-9 · Cited by 532 · see citing works
Influenza virus and SARS-CoV-2: pathogenesis and host responses in the respiratory tract
Flerlage, T., Boyd, D. F., Meliopoulos, V., Thomas, P. G., & Schultz‐Cherry, S. (2021) · Nature Reviews Microbiology · doi:10.1038/s41579-021-00542-7 · Cited by 406 · see citing works
von Bartheld, C. S., Hagen, M. M., & Butowt, R. (2020) · ACS Chemical Neuroscience · doi:10.1021/acschemneuro.0c00460 · Cited by 283 · see citing works
Self-citationZazhytska, M., Kodra, A. L., Hoagland, D. A., Frere, J. J., Fullard, J. F., Shayya, H. J., McArthur, N. G., Møller, R., Uhl, S. A., Omer, A. D., et al. (2022) · Cell · doi:10.1016/j.cell.2022.01.024 · Cited by 248 · see citing works
COVID-19 and chronic fatigue syndrome: Is the worst yet to come?
Wostyn, P. (2021) · Medical Hypotheses · doi:10.1016/j.mehy.2020.110469 · Cited by 229 · see citing works
“observed in most COVID-19 patients [22].”
BackgroundInfluentialTan, B. K. J., Han, R., Zhao, J. J., Tan, N. K. W., Quah, E. S. H., Tan, C. J., Chan, Y. H., Teo, N. W. Y., Charn, T. C., See, A., et al. (2022) · BMJ · doi:10.1136/bmj-2021-069503 · Cited by 222 · see citing works
“Sensorineural mechanisms are currently thought to be the predominant mechanism of covid-19 related smell dysfunction, 54 55 although conductive mechanisms have been implicated too.”
Self-citationAddison, A. B., Wong, B. L. K., Ahmed, T., Macchi, A., Konstantinidis, I., Huart, C., Frasnelli, J., Fjældstad, A. W., Ramakrishnan, V. R., Rombaux, P., et al. (2021) · Journal of Allergy and Clinical Immunology · doi:10.1016/j.jaci.2020.12.641 · Cited by 138 · see citing works
“Current thinking regarding the mechanism of chemosensory dysfunction in COVID-19 infection suggests that it is caused by viral entry via angiotensin-converting enzyme 2 receptors, with infection and death of sustentacular cells in the olfactory epithelium; this does not necessarily lead to infection, damage, death, or…”
BackgroundNeurological complications and infection mechanism of SARS-CoV-2
Wan, D., Du, T., Hong, W., Chen, L., Que, H., Lu, S., & Peng, X. (2021) · Signal Transduction and Targeted Therapy · doi:10.1038/s41392-021-00818-7 · Cited by 132 · see citing works
SARS-CoV-2 infects neurons and induces neuroinflammation in a non-human primate model of COVID-19
Beckman, D., Bonillas, A. C., Diniz, G. B., Ott, S. P., Roh, J. W., Elizaldi, S. R., Schmidt, B., Sammak, R. L., Rompay, K. K. A. V., Iyer, S. S., et al. (2022) · Cell Reports · doi:10.1016/j.celrep.2022.111573 · Cited by 134 · see citing works
International consensus statement on allergy and rhinology: Olfaction
Patel, Z., Holbrook, E., Turner, J., Adappa, N., Albers, M. W., Altundağ, A., Appenzeller, S., Costanzo, R., Croy, I., Davis, G. E., et al. (2022) · International Forum of Allergy and Rhinology · doi:10.1002/alr.22929 · Cited by 119 · see citing works
Mutiawati, E., Fahriani, M., Mamada, S. S., Fajar, J. K., Frediansyah, A., Maliga, H. A., Ilmawan, M., Emran, T. B., Ophinni, Y., Ichsan, I., et al. (2021) · F1000Research · doi:10.12688/f1000research.28393.1 · Cited by 126 · see citing works
Boscolo‐Rizzo, P., Hummel, T. R., Hopkins, C. L., Dibattista, M., Menini, A., Spinato, G., Fabbris, C., Emanuelli, E., D’Alessandro, A., Marzolino, R., et al. (2021) · Rhinology Journal · doi:10.4193/rhin21.249 · Cited by 127 · see citing works
“While the expression of ACE2 receptor in sustentacular cells of the olfactory neuroepithelium (OE) was consistently demonstrated in several studies ((35)), the expression of the ACE2 receptor in taste buds was confirmed only in a very recent investigation demonstrating the colocalization of ACE2 receptor, SARS-CoV-2,…”
BackgroundResultThe UGT2A1/UGT2A2 locus is associated with COVID-19-related loss of smell or taste
Shelton, J. F., Shastri, A. J., Fletez‐Brant, K., The 23andMe COVID-19 Team, Auton, A., Chubb, A., Fitch, A., Kung, A., Altman, A., Kill, A., et al. (2022) · Nature Genetics · doi:10.1038/s41588-021-00986-w · Cited by 123 · see citing works
Butowt, R., Meunier, N., Bryche, B., & von Bartheld, C. S. (2021) · Acta Neuropathologica · doi:10.1007/s00401-021-02314-2 · Cited by 122 · see citing works
“Alternative mechanisms of transfer of SARS-CoV-2 from the nose to the brain include the crossing of the blood–brain-barrier after uptake in leukocytes [5, 14, 77, 108], or entering through the endothelial cells of blood vessels [16, 75, 108], reaching CSF-containing spaces associated with the olfactory nerve [14, 19],…”
BackgroundResultInfluentialSelf-citationOlfactory dysfunction in COVID-19: new insights into the underlying mechanisms
Butowt, R., Bilińska, K., & von Bartheld, C. S. (2022) · Trends in Neurosciences · doi:10.1016/j.tins.2022.11.003 · Cited by 127 · see citing works
“provides a plausible mechanism for COVID-19 induced anosmia [10-11,24,62].”
InfluentialSelf-citationMagusali, N., Graham, A. C., Piers, T. M., Panichnantakul, P., Yaman, U., Shoai, M., Reynolds, R. H., Botia, J. A., Brookes, K. J., Guetta-Baranes, T., et al. (2021) · Brain · doi:10.1093/brain/awab337 · Cited by 111 · see citing works
“41–45 There is accumulating evidence that these brain structures and cells are infected with SARS-CoV-2 and are altering the cytokine profile of the brain.”
BackgroundBoscolo-Rizzo, P., Tirelli, G., Meloni, P., Hopkins, C., Madeddu, G., Vito, A. D., Gardenal, N., Valentinotti, R., Tofanelli, M., Borsetto, D., et al. (2022) · medRxiv · doi:10.1002/alr.22995 · Cited by 81 · see citing works
Principles of odor coding in vertebrates and artificial chemosensory systems
Manzini, I., Schild, D., & Natale, C. D. (2021) · Physiological Reviews · doi:10.1152/physrev.00036.2020 · Cited by 84 · see citing works
Wang, W. B., Liang, Y., Jin, Y. Q., Zhang, J., Su, J. G., & Li, Q. M. (2021) · Journal of Molecular Graphics and Modelling · doi:10.1016/j.jmgm.2021.108035 · Cited by 80 · see citing works
“Compared with the original SARS-CoV-2 strains, the 501Y.V1, 501Y.V2 and 501Y.V3 variants are potentially more transmissible, which may also reduce the effectiveness of the current vaccines and neutralizing antibodies[27].”
InfluentialAssociation of COVID-19 with Comorbidities: An Update
Chatterjee, S., Nalla, L. V., Sharma, M., Sharma, N., Singh, A. A., Malim, F. M., Ghatage, M., Mukarram, M., Pawar, A., Parihar, N., et al. (2023) · ACS Pharmacology & Translational Science · doi:10.1021/acsptsci.2c00181 · Cited by 87 · see citing works
Neurological Manifestations in COVID-19 Patients: A Meta-Analysis
Vitalakumar, D., Sharma, A., Kumar, A., & Flora, S. J. S. (2021) · ACS Chemical Neuroscience · doi:10.1021/acschemneuro.1c00353 · Cited by 82 · see citing works
ACE2 expression in rat brain: Implications for COVID-19 associated neurological manifestations
Hernández, V. S., Zetter, M. A., Guerra, E. C., Hernández‐Araiza, I., Karuzin, N., Hernández‐Pérez, O. R., Eiden, L. E., & Zhang, L. (2021) · Experimental Neurology · doi:10.1016/j.expneurol.2021.113837 · Cited by 76 · see citing works
“One of the most classical symptoms of COVID-19 is the loss of taste and smell (Butowt and von Bartheld 2020, Mao, Jin et al. 2020).”
Butowt, R., Bilińska, K., & von Bartheld, C. S. (2020) · ACS Chemical Neuroscience · doi:10.1021/acschemneuro.0c00596 · Cited by 76 · see citing works
Self-citationCOVID 19-Induced Smell and Taste Impairments: Putative Impact on Physiology
Meunier, N., Briand, L. V., Jacquin, A., Brondel, L., & Pénicaud, L. (2021) · Frontiers in Physiology · doi:10.3389/fphys.2020.625110 · Cited by 69 · see citing works
“Better mouse models are in development to implement a humanized ACE2 with a physiological expression profile (Butowt and von Bartheld, 2020; Sun et al., 2020).”
BackgroundSarubbo, F., Haji, K. E., Vidal-Balle, A., & Bargay, J. (2021) · Brain Behavior & Immunity - Health · doi:10.1016/j.bbih.2021.100399 · Cited by 67 · see citing works
“Bibliography published so far include cohort studies and case reports, being the prevalence of anosmia in COVID-19 patients calculated to be around 44%, and the prevalence of hypogeusia around 43% (Butowt and von Bartheld, 2020).”
InfluentialTorices, S., Cabrera, R., Stangis, M., Naranjo, O., Fattakhov, N. S., Téglás, T., Adesse, D., & Toborek, M. J. (2021) · Journal of Neuroinflammation · doi:10.1186/s12974-021-02210-2 · Cited by 65 · see citing works
“COVID-19 patients also experience rhabdomyolysis (13), myositis (14) or peripheral nervous system symptoms, including Guillain-Barré syndrome (15), and taste or olfactory impairment (16, 17), The incidence of neurological complications is estimated to be around 37% in SARS-CoV-2-infected patients (5).”
Brain imaging in patients with COVID-19: A systematic review
Najt, P., Richards, H. L., & Fortune, D. G. (2021) · Brain Behavior & Immunity - Health · doi:10.1016/j.bbih.2021.100290 · Cited by 65 · see citing works
“Viral infection resulted in The brain is among the targets of SARS-CoV-2, resulting in neurological symptoms such as loss of smell and taste (Butowt and Bartheld, 2020).”
Potential pharmacologic treatments for COVID-19 smell and taste loss: A comprehensive review
Khani, E., Khiali, S., Beheshtirouy, S., & Entezari‐Maleki, T. (2021) · European Journal of Pharmacology · doi:10.1016/j.ejphar.2021.174582 · Cited by 64 · see citing works
Brain Mechanisms of COVID-19-Sleep Disorders
Semyachkina-Glushkovskaya, O. V., Mamedova, A., Telnova, V., Klimova, M., Saranceva, E. I., Ageev, V., Yu, T., Zhu, D. Y., Penzel, T., & Kurths, J. (2021) · International Journal of Molecular Sciences · doi:10.3390/ijms22136917 · Cited by 62 · see citing works
“H ) The SARS-CoV-2 via the ACE2 receptor on the centers (olfactory bulb and cortex), thereby reducing smell sensations [150–156].”
Backgroundvon Bartheld, C. S., Hagen, M. M., & Butowt, R. (2021) · ACS Chemical Neuroscience · doi:10.1021/acschemneuro.1c00542 · Cited by 60 · see citing works
Self-citationSelf-reported Taste and Smell Disorders in Patients with COVID-19: Distinct Features in China
Song, J., Deng, Y., Wang, H., Wang, Z., Liao, B., Ma, J., He, C., Li, P., Liu, Y., Alobid, I., et al. (2021) · Current Medical Science · doi:10.1007/s11596-021-2312-7 · Cited by 60 · see citing works
Pathophysiology of infection with SARS‐CoV ‐2— What is known and what remains a mystery
Sridhar, S., & Nicholls, J. M. (2021) · Respirology · doi:10.1111/resp.14091 · Cited by 62 · see citing works
“Within the olfactory mucosa, there has been much attention focused on the sustentacular cells as a target for viral entry.(19) ACE2 has been identified on the motile cilia of the airway epithelial cells,(20) but the use of angiotensinconverting enzyme inhibitors or receptor blockers did not increase susceptibility to…”
BackgroundInterventions for the treatment of persistent post-COVID-19 olfactory dysfunction
O’Byrne, L. M., Webster, K. E., MacKeith, S. A. C., Philpott, C. M., Hopkins, C. L., & Burton, M. J. (2021) · Cochrane Database of Systematic Reviews · doi:10.1002/14651858.cd013876.pub2 · Cited by 59 · see citing works
Neta, F. I., Fernandes, A. C. L., Vale, A. J. M., Pinheiro, F. I., Cobucci, R. N., de Azevedo, E. P., & Gúzen, F. P. (2021) · Current Research in Pharmacology and Drug Discovery · doi:10.1016/j.crphar.2021.100035 · Cited by 55 · see citing works
“The main cause of the latter is the direct damage that SARS-CoV-2 causes in olfactory receptor neurons located in the olfactory epithelium (Kanjanaumporn et al., 2020; Butowt and Bartheld, 2020).”
Long-Term Complications of COVID-19 Infection in Adolescents and Children
Thallapureddy, K., Thallapureddy, K., Zerda, E., Suresh, N. V., Kamat, D., Rajasekaran, K., & Moreira, A. G. (2022) · Current Pediatrics Reports · doi:10.1007/s40124-021-00260-x · Cited by 53 · see citing works
Addressing Post-COVID Symptoms: A Guide for Primary Care Physicians
Vance, H., Maslach, A., Stoneman, E. K., Harmes, K. M., Ransom, A., Seagly, K., & Furst, W. (2021) · The Journal of the American Board of Family Medicine · doi:10.3122/jabfm.2021.06.210254 · Cited by 49 · see citing works
“32 Although the explanation is currently not clear, 33 possible explanations as to what may cause anosmia during COVID-19 infection include congestion, damage to the olfactory nerve, in fl ammation in cells within the lining of the nasal cavity, and viral effects on the cranial nerves within the…”
BackgroundRelationship between COVID‐19 and movement disorders: A narrative review
Schneider, S. A., Hennig, A., & Martino, D. (2021) · European Journal of Neurology · doi:10.1111/ene.15217 · Cited by 50 · see citing works
“Genetic variability and the mutation rate within the receptor binding domain of the virus's spike protein influence the prevalence of olfactory disorders in different populations [47].”
BackgroundReyna, R. A., Kishimoto‐Urata, M., Urata, S., Makishima, T., Paessler, S., & Maruyama, J. (2022) · Scientific Reports · doi:10.1038/s41598-021-04622-9 · Cited by 48 · see citing works
Mohamad, S. A., Badawi, A. M., & Mansour, H. F. (2021) · International Journal of Pharmaceutics · doi:10.1016/j.ijpharm.2021.120600 · Cited by 47 · see citing works
Bussière, N., Mei, J., Lévesque-Boissonneault, C., Blais, M., Carazo, S., Gros‐Louis, F., Serres, G. D., Dupré, N., & Frasnelli, J. (2021) · Chemical Senses · doi:10.1093/chemse/bjab038 · Cited by 44 · see citing works
The Upper Nasal Space: Option for Systemic Drug Delivery, Mucosal Vaccines and “Nose-to-Brain”
Shrewsbury, S. B. (2023) · Pharmaceutics · doi:10.3390/pharmaceutics15061720 · Cited by 44 · see citing works
“Entry of the virus via the nose and, specifically, the olfactory mucosa of the nasal cavity is thought to be responsible for a number of the symptoms of COVID, including anosmia [33] and central nervous system effects [34].”
BackgroundPathophysiological relationship between COVID-19 and olfactory dysfunction: A systematic review
Lima, M. H. D. L. C., Cavalcante, A. L. B., & Leão, S. C. (2021) · Brazilian Journal of Otorhinolaryngology · doi:10.1016/j.bjorl.2021.04.001 · Cited by 43 · see citing works
Is loss of smell an early predictor of COVID-19 severity: a systematic review and meta-analysis
Purja, S., Shin, H., Lee, J.-Y., & Kim, E. Y. (2021) · Archives of Pharmacal Research · doi:10.1007/s12272-021-01344-4 · Cited by 42 · see citing works
Structural brain changes in post‐acute COVID‐19 patients with persistent olfactory dysfunction
Campabadal, A., Oltra, J., Junqué, C., Guillén, N., Boti, M. A., Sala‐Llonch, R., Monté, G. C., Lledó, G. M., Bargalló, N., Rami, L., et al. (2022) · Annals of Clinical and Translational Neurology · doi:10.1002/acn3.51710 · Cited by 45 · see citing works
Interventions for Improving Long COVID-19 Symptomatology: A Systematic Review
Veronese, N., Bonica, R., Cotugno, S., Tulone, O., Camporeale, M., Smith, L., Trott, M., Bruyère, O., Mirarchi, L., Rizzo, G., et al. (2022) · Viruses · doi:10.3390/v14091863 · Cited by 40 · see citing works
“Although the pathogenetic mechanisms underlying COVID-19-related anosmia/dysosmia are still unclear [19], some rehabilitation of the olfactory pathway was achieved in this study.”
BackgroundMental health symptoms one year after acute COVID-19 infection: Prevalence and risk factors
Colizzi, M., Peghin, M., Martino, M. D., Bontempo, G., Gerussi, V., Palese, A., Isola, M., Tascini, C., & Balestrieri, M. (2022) · Revista de Psiquiatría y Salud Mental · doi:10.1016/j.rpsm.2022.05.008 · Cited by 41 · see citing works
Is There Less Alteration of Smell Sensation in Patients With Omicron SARS-CoV-2 Variant Infection?
Rodríguez‐Sevilla, J. J., Güerri‐Fernández, R., & Recasens, B. B. (2022) · Frontiers in Medicine · doi:10.3389/fmed.2022.852998 · Cited by 40 · see citing works
“One of the possible rationales could implicate that Caucasians have more often an Angiotensin-converting enzyme 2 (ACE2) variant expressed in the olfactory epithelium (12, 13) (presumably in the sustentacular cells of the olfactory epithelium).”
BackgroundTherapeutic Approaches to the Neurologic Manifestations of COVID-19
Graham, E. L., Koralnik, I. J., & Liotta, E. M. (2022) · Neurotherapeutics · doi:10.1007/s13311-022-01267-y · Cited by 37 · see citing works
“However, SARS-CoV-2 has been found in the sustentacular cells in olfactory epithelium, cells that support the olfactory sensory neurons [181, 182].”
BackgroundTRP channels in COVID-19 disease: Potential targets for prevention and treatment
Jaffal, S. M., & Abbas, M. A. (2021) · Chemico-Biological Interactions · doi:10.1016/j.cbi.2021.109567 · Cited by 37 · see citing works
“TRP channels anosmia, ageusia and hearing loss in COVID-19 Worldwide, it was emerged that COVID-19 infection causes a reduction or loss of taste and smell [77].”
Chaaban, N., Høier, A. T. Z. B., & Andersen, B. V. (2021) · Foods · doi:10.3390/foods10040892 · Cited by 34 · see citing works
Pathogenesis and progression of anosmia and dysgeusia during the COVID-19 pandemic
Krishnakumar, H. N., Momtaz, D., Sherwani, A., Mhapankar, A., Gonuguntla, R. K., Maleki, A., Abbas, A., Ghali, A. N., & Afif, A. A. (2022) · European Archives of Oto-Rhino-Laryngology · doi:10.1007/s00405-022-07689-w · Cited by 38 · see citing works
“While less is currently understood about the pathogenesis of dysgeusia, ACE2 is significantly expressed in tongue epithelial cells, buccal mucosa, and the oral cavity, as was found in single cell RNA-sequencing studies [14].”
BackgroundThe Molecular Mechanisms of Cognitive Dysfunction in Long COVID: A Narrative Review
Popa, E., Popa, A. E., Poroch, M., Poroch, V., Ungureanu, M. I., Slănină, A. M., Bacușcă, A. I., & Coman, A. E. (2025) · International Journal of Molecular Sciences · doi:10.3390/ijms26115102 · Cited by 38 · see citing works
“Endothelial dysfunction is a key driver of Long COVID pathology, particularly within the CNS [109,110].”
COVID-19 Is a Multi-Organ Aggressor: Epigenetic and Clinical Marks
Kgatle, M., Lawal, I. O., Mashabela, G. T., Boshomane, T. M. G., Koatale, P. C., Mahasha, P. W., Ndlovu, H., Vorster, M., Rodrigues, H. G., Zeevaart, J. R., et al. (2021) · Frontiers in Immunology · doi:10.3389/fimmu.2021.752380 · Cited by 37 · see citing works
AT1 Receptors: Their Actions from Hypertension to Cognitive Impairment
Wu, H., Sun, Q., Yuan, S., Wang, J., Li, F., Gao, H., Chen, X., Yang, R., & Xu, J. (2022) · Cardiovascular Toxicology · doi:10.1007/s12012-022-09730-0 · Cited by 37 · see citing works
Revealing the mystery of persistent smell loss in long COVID patients
Park, J. W., Wang, X., & Xu, R. (2022) · International Journal of Biological Sciences · doi:10.7150/ijbs.73485 · Cited by 36 · see citing works
“First, East Asian populations displayed a 2-3-fold lower rate of olfactory and taste defects than the populations in western countries [53].”
BackgroundInterventions for the treatment of persistent post-COVID-19 olfactory dysfunction
O’Byrne, L. M., Webster, K. E., MacKeith, S. A. C., Philpott, C. M., Hopkins, C. L., & Burton, M. J. (2022) · Cochrane Database of Systematic Reviews · doi:10.1002/14651858.cd013876.pub3 · Cited by 36 · see citing works
The Pathogenesis of Cytomegalovirus and Other Viruses Associated with Hearing Loss: Recent Updates
Shi, X., Liu, X., & Sun, Y. (2023) · Viruses · doi:10.3390/v15061385 · Cited by 39 · see citing works
A Systematic Review of Imaging Studies in Olfactory Dysfunction Secondary to COVID-19
Keshavarz, P., Haseli, S., Yazdanpanah, F., Bagheri, F., Raygani, N., & Karimi‐Galougahi, M. (2021) · Academic Radiology · doi:10.1016/j.acra.2021.08.010 · Cited by 35 · see citing works
COVID-19 and Alzheimer’s Disease: A Literature Review
Hardan, L., Filtchev, D., Kassem, R., Bourgi, R., Łukomska−Szymańska, M., Tarhini, H., Salloum-Yared, F., Mancino, D., Kharouf, N., & Haïkel, Y. (2021) · Medicina · doi:10.3390/medicina57111159 · Cited by 38 · see citing works
“MRI hypersignals of the olfactory epithelial cortex indicate infection especially with the presence of ACE2 receptors and TMPRSS2 in the olfactory epithelium [36].”
BackgroundSzabo, M. P., Iba, M., Nath, A., Masliah, E., & Kim, C. (2022) · Experimental & Molecular Medicine · doi:10.1038/s12276-022-00755-7 · Cited by 35 · see citing works
SARS-CoV-2 and neurodegenerative diseases: what we know and what we don’t
Lingor, P., Demleitner, A. F., Wolff, A. W., & Feneberg, E. (2022) · Journal of Neural Transmission · doi:10.1007/s00702-022-02500-w · Cited by 35 · see citing works
“In a more detailed study of the olfactory mucosa, the virus was found in sustentacular and stem cells of the mucosa while absent from olfactory receptor neurons (ORN) (Butowt and von Bartheld 2020).”
BackgroundRethinavel, H. S., Ravichandran, S., Radhakrishnan, R. K., & Kandasamy, M. (2021) · Journal of Chemical Neuroanatomy · doi:10.1016/j.jchemneu.2021.101965 · Cited by 35 · see citing works
New Brazilian variant of the SARS-CoV-2 (P1/Gamma) of COVID-19 in Alagoas state
da Silva, J. C., Félix, V., Leão, S. A. B. F., Filho, E. M. T., & Scorza, F. A. (2021) · The Brazilian Journal of Infectious Diseases · doi:10.1016/j.bjid.2021.101588 · Cited by 34 · see citing works
“Studies suggest that expression of ACE2 cellular proteins and TMPRSS2 protease in the olfactory epithelium cells are involved in viral access to the human body and detection in oropharyngeal secretions.(2,12) Since ACE2 proteins seem to be expressed in significantly higher levels in older people, this may explain the…”
Interventions for the prevention of persistent post-COVID-19 olfactory dysfunction
Webster, K. E., O’Byrne, L. M., MacKeith, S. A. C., Philpott, C. M., Hopkins, C. L., & Burton, M. J. (2021) · Cochrane Database of Systematic Reviews · doi:10.1002/14651858.cd013877.pub2 · Cited by 34 · see citing works
Bilińska, K., von Bartheld, C. S., & Butowt, R. (2021) · Frontiers in Cellular Neuroscience · doi:10.3389/fncel.2021.674123 · Cited by 35 · see citing works
Self-citationVelichkovsky, B. B., Razvaliaeva, A. Y., Khlebnikova, A. A., Manukyan, P. A., & Kasatkin, V. N. (2023) · Acta Psychologica · doi:10.1016/j.actpsy.2023.103838 · Cited by 33 · see citing works
Post-COVID Symptoms in Occupational Cohorts: Effects on Health and Work Ability
Magnavita, N., Arnesano, G., Prinzio, R. R. D., Gasbarri, M., Meraglia, I., Merella, M., & Vacca, M. E. (2023) · International Journal of Environmental Research and Public Health · doi:10.3390/ijerph20095638 · Cited by 33 · see citing works
“Chemosensory deficits are often the earliest, and sometimes the only signs of the SARSCoV-2 virus in otherwise asymptomatic carriers [45].”
BackgroundNobile, B., Durand, M., Olié, É., Guillaume, S., Molès, J., Haffen, É., & Courtet, P. (2021) · Frontiers in Pharmacology · doi:10.3389/fphar.2021.615695 · Cited by 31 · see citing works
Sen, A. (2021) · Medical Hypotheses · doi:10.1016/j.mehy.2021.110627 · Cited by 30 · see citing works
“Surprisingly, the recovery after anosmia is often quicker (especially in mild cases) than the time it takes for neuron replacement, cilia maturation, and the growth of the new axons from the olfactory epithelium to form synapses in the olfactory bulb [26,27].”
Dysautonomia and Implications for Anosmia in Long COVID-19 Disease
Vallée, A. (2021) · Journal of Clinical Medicine · doi:10.3390/jcm10235514 · Cited by 29 · see citing works
“A possible explanation could be that incomplete X chromosome inhibition may contribute to overexpression of ACE2 [29].”
BackgroundNeuroradiological Basis of COVID ‐19 Olfactory Dysfunction: A Systematic Review and Meta‐Analysis
Tan, C. J., Tan, B. K. J., Tan, X. Y., Liu, H., Teo, C. B., See, A., Xu, S., Toh, S. T., Kheok, S. W., Charn, T. C., et al. (2022) · The Laryngoscope · doi:10.1002/lary.30078 · Cited by 30 · see citing works
“At present, conductive mechanisms of olfactory loss in COVID-19-associated OD have largely been dismissed in favor of sensorineural mechanisms,(60,61) given the absence of significant sinonasal symptoms like nasal obstruction and mucosal congestion in COVID-19 infection.(60,62) However, our findings suggest that condu…”
BackgroundSemyachkina-Glushkovskaya, O. V., Postnov, D. E., Lavrova, A. I., Fedosov, I. V., Borisova, E. G., Nikolenko, V. N., Penzel, T., Kurths, J., & Tuchin, V. V. (2020) · IEEE Journal of Selected Topics in Quantum Electronics · doi:10.1109/jstqe.2020.3045834 · Cited by 29 · see citing works
“One of hypothesis explains that the virus infiltrates the brain, possibly from the nose, and affects olfactory centers (olfactory bulb and cortex), thereby reducing smell sensations [50].”
BackgroundSystematic review and meta-analysis of olfactory and gustatory dysfunction in COVID-19
Liu, N., Yang, D., Zhang, T., Sun, J., Fu, J., & Li, H. (2022) · International Journal of Infectious Diseases · doi:10.1016/j.ijid.2022.02.004 · Cited by 28 · see citing works
Vestibular Cochlear Manifestations in COVID-19 Cases
Kaliyappan, K., Chen, Y., & Muthaiah, V. P. K. (2022) · Frontiers in Neurology · doi:10.3389/fneur.2022.850337 · Cited by 27 · see citing works
de Erausquin, G. A., Snyder, H. M., Brugha, T. S., Seshadri, S. S., Carrillo, M. C., Sagar, R., Huang, Y., Newton, C. R. J. C., Tartaglia, M. C., Teunissen, C. E., et al. (2022) · Alzheimer s & Dementia Translational Research & Clinical Interventions · doi:10.1002/trc2.12348 · Cited by 26 · see citing works
Follow-Up of a Cohort of Patients with Post-Acute COVID-19 Syndrome in a Belgian Family Practice
Jamoulle, M., Kazeneza-Mugisha, G., & Zayane, A. (2022) · Viruses · doi:10.3390/v14092000 · Cited by 27 · see citing works
“Cerebral disorders dominate, either by thalamic and subthalamic damage (memory loss), cortical damage (brain fog, anomia, hallucination, paresthesias, abnormal movements), or by bulbar damage (anosmia, dysgeusia, dizziness, orthostatic disorder), although in anosmia, both central and peripheral alterations could be de…”
BackgroundDisruption of nuclear architecture as a cause of COVID-19 induced anosmiaPreprint
Zazhytska, M., Kodra, A. L., Hoagland, D. A., Fullard, J. F., Shayya, H. J., Omer, A. D., Firestein, S., Gong, Q., Canoll, P., Goldman, J. E., et al. (2021) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2021.02.09.430314 · Cited by 26 · see citing works
Shi, Z., Xi, L., Wang, Y., & Zhao, X. (2023) · Environmental Science & Technology · doi:10.1021/acs.est.3c04875 · Cited by 25 · see citing works
Gunder, N., Dörig, P., Witt, M., Welge–Lüssen, A., Menzel, S., & Hummel, T. R. (2023) · HNO · doi:10.1007/s00106-022-01249-8 · Cited by 25 · see citing works
“This is a possible explanation for the rapid improvement in olfactory function in many cases, since the ORNs themselves are only indirectly affected [12].”
BackgroundHippocampal alterations after SARS-CoV-2 infection: A systematic review
Zorzo, C., Solares, L., Méndez, M., & Méndez-López, M. (2023) · Behavioural Brain Research · doi:10.1016/j.bbr.2023.114662 · Cited by 25 · see citing works
Stroke in SARS-CoV-2 Infection: A Pictorial Overview of the Pathoetiology
Neshin, S. A. S., Shahjouei, S., Koza, E., Friedenberg, I., Khodadadi, F., Sabra, M., Kobeissy, F. H., Ansari, S., Tsivgoulis, G. K., Li, J., et al. (2021) · Frontiers in Cardiovascular Medicine · doi:10.3389/fcvm.2021.649922 · Cited by 25 · see citing works
Callejón-Leblic, M. A., Jiménez, D. I. M., Moreno‐Luna, R., Palacios-García, J. M., Álvarez-Cendrero, M., Vizcarra-Melgar, J., Fernandez-Velez, C., Reyes-Tejero, I. M., Maza-Solano, J. M., García, J. G., et al. (2022) · Life · doi:10.3390/life12081256 · Cited by 24 · see citing works
“Although some groups have made considerable research efforts to elucidate the causes of smell and taste dysfunction in COVID-19 [7,8], the underlying mechanism by which SARS-CoV-2 infection leads to chemosensory dysfunction remains unclear.”
BackgroundParosmia post COVID-19: an unpleasant manifestation of long COVID syndrome
Saniasiaya, J., & Prepageran, N. (2021) · Postgraduate Medical Journal · doi:10.1136/postgradmedj-2021-139855 · Cited by 24 · see citing works
Salfi, F., Amicucci, G., Corigliano, D., Viselli, L., D’Atri, A., Tempesta, D., & Ferrara, M. (2023) · Brain Behavior and Immunity · doi:10.1016/j.bbi.2023.06.010 · Cited by 23 · see citing works
Chemosensory Dysfunction in Patients with COVID-19: What Do We Learn from the Global Outbreak?
Zeng, M., Wang, D. Y., Mullol, J., & Liu, Z. (2021) · Current Allergy and Asthma Reports · doi:10.1007/s11882-020-00987-5 · Cited by 23 · see citing works
Taste and Smell Impairment in Critically Ill Patients With COVID-19: An Intensive Care Unit Study
Sayın, P., Altınay, M., Çınar, A. S., & Özdemir, H. M. (2020) · Ear Nose & Throat Journal · doi:10.1177/0145561320977464 · Cited by 22 · see citing works
“Because neural structures do not contain ACE2 receptors, non-neural involvement has been suggested as a cause of COVID-19related smell and taste impairment.(8) Most patients with COVID-19 exhibit partial taste and/or smell impairment, which tends to resolve early and spontaneously.”
BackgroundGross and Histopathology of COVID-19 With First Histology Report of Olfactory Bulb Changes
Stoyanov, G. S., Petkova, L., Dzhenkov, D. L., Sapundzhiev, N. R., & Todorov, I. (2020) · Cureus · doi:10.7759/cureus.11912 · Cited by 22 · see citing works
Encephalopathy in COVID-19 Patients
Shah, P., Patel, J., Soror, N., & Kartan, R. (2021) · Cureus · doi:10.7759/cureus.16620 · Cited by 22 · see citing works
“Butowt and von Bartheld reported that neurotropism may be caused by virus-induced inflammation or vascular/systemic routes rather than olfactory neurons given that the sudden loss of smell is followed by a rapid recovery which is less than one week [10].”
BackgroundNeurological Complications of COVID-19: A Review of the Literature
Dale, L. (2022) · Cureus · doi:10.7759/cureus.27633 · Cited by 22 · see citing works
“Pathophysiologically, it is thought that COVID-19’s spike protein interacts with angiotensin-converting enzyme 2 (ACE2), and transaminase protein serine 2 (TMPRSS2) receptors on olfactory neurons [16-17].”
BackgroundShahbaz, M. A., Bernardi, F., Alatalo, A., Sachana, M., Clerbaux, L., Muñoz, A., Parvatam, S., Landesmann, B., Kanninen, K. M., & Coecke, S. (2022) · Cells · doi:10.3390/cells11193027 · Cited by 22 · see citing works
Schirinzi, T., Lattanzi, R., Maftei, D., Grillo, P., Zenuni, H., Boffa, L., Albanese, M., Simonetta, C., Bovenzi, R., Maurizi, R., et al. (2022) · Brain Behavior and Immunity · doi:10.1016/j.bbi.2022.12.017 · Cited by 22 · see citing works
MRI evidence of gray matter loss in COVID ‐19 patients with cognitive and olfactory disorders
Capelli, S., Arrigoni, A., Napolitano, A., Pezzetti, G., Remuzzi, A., Zangari, R., Lorini, F. L., Sessa, M., Caroli, A., & Gerevini, S. (2024) · Annals of Clinical and Translational Neurology · doi:10.1002/acn3.52164 · Cited by 21 · see citing works
“Instead, it may be attributed to the virus’s neurotropism: angiotensin-converting enzyme 2 (ACE2) is widely present in the olfactory system and, serving as a viral receptor, it may provide SARS-CoV-2 access to the CNS. 31,32 Propagation of viruses by retrograde axonal transport to the olfactory bulbs and to the CNS ha…”
SARS-CoV-2 invasion of the central nervous: a brief review
Siddiqui, R., Mungroo, M. R., & Khan, N. A. (2021) · Hospital Practice · doi:10.1080/21548331.2021.1887677 · Cited by 21 · see citing works
“the olfactory epithelium, brain infiltration affecting olfactory centers, and loss of olfactory receptor neurons [34].”
BackgroundUeha, R., Ito, T., Furukawa, R., Kitabatake, M., Ouji-Sageshima, N., Ueha, S., Koyama, M., Uranaka, T., Kondo, K., & Yamasoba, T. (2022) · Frontiers in Cellular and Infection Microbiology · doi:10.3389/fcimb.2022.924725 · Cited by 20 · see citing works
Neuromuscular Complications of SARS-CoV-2 and Other Viral Infections
Jacob, S. M., Kapadia, R. K., Soule, T., Luo, H., Schellenberg, K. L., Douville, R. N., & Pfeffer, G. (2022) · Frontiers in Neurology · doi:10.3389/fneur.2022.914411 · Cited by 21 · see citing works
Modeling the effectiveness of olfactory testing to limit SARS-CoV-2 transmission
Larremore, D. B., Toomre, D. K., & Parker, R. (2021) · Nature Communications · doi:10.1038/s41467-021-23315-5 · Cited by 21 · see citing works
“[20] Rafal Butowt and Christopher S von Bartheld.”
BackgroundInterventions for the prevention of persistent post-COVID-19 olfactory dysfunction
Webster, K. E., O’Byrne, L. M., MacKeith, S. A. C., Philpott, C. M., Hopkins, C. L., & Burton, M. J. (2022) · Cochrane Database of Systematic Reviews · doi:10.1002/14651858.cd013877.pub3 · Cited by 21 · see citing works
Olfaction and neurocognition after COVID-19: a scoping review
Vilarello, B. J., Jacobson, P. T., Tervo, J. P., Waring, N. A., Gudis, D. A., Goldberg, T. E., Devanand, D. P., & Overdevest, J. B. (2023) · Frontiers in Neuroscience · doi:10.3389/fnins.2023.1198267 · Cited by 19 · see citing works
“Early investigations have provided preliminary insight into the mechanisms by which COVID-19 acutely affects the olfactory system and whether olfaction provides a window into greater neurological dysfunction caused by the virus (Butowt and Bartheld, 2021; Zazhytska et al., 2022).”
BackgroundDoes the RAAS play a role in loss of taste and smell during COVID-19 infections?
Luchiari, H. R., Giordano, R. J., Sidman, R. L., Pasqualini, R., & Arap, W. (2020) · The Pharmacogenomics Journal · doi:10.1038/s41397-020-00202-8 · Cited by 18 · see citing works
“Possible mechanisms for loss of smell and taste in the course of COVID-19 disease are being explored [2, 3] but no direct role of the Renin-Angiotensinaldosterone system (RAAS) in anosmia and ageusia has been suggested until now.”
Background
- Authors
- Butowt, R., & von Bartheld, C. S.
- Affiliations
- Department of Molecular Cell Genetics, L. Rydygier Collegium Medicum, Nicolaus Copernicus University, Bydgoszcz, Poland
- Center of Biomedical Research Excellence in Cell Biology, Reno School of Medicine, University of Nevada, Reno, NV, USA
- Venue
- The Neuroscientist
- Publisher
- SAGE Publications
- Published
- 2020-09-11
- Volume
- 27
- Issue
- 6
- Pages
- 582-603
- ISSN
- 1073-8584 (ISSN-L)
- 1089-4098
- PMC
- PMC7488171
- OpenAlex
- W3084613638
- Cited by
- 345
- References
- 143
- Citations by year
- 2026: 14 · 2025: 22 · 2024: 38 · 2023: 73 · 2022: 97 · 2021: 91 · 2020: 8 · 2018: 2
- FWCI
- 23.68
- Type
- journal article
- Language
- en
- Open access
- green
- www.ncbi.nlm.nih.gov
- Locations
- The Neuroscientist (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- Funders
- national institutes of health (GM103554)
- Uniwersytet Mikolaja Kopernika w Toruniu (Excellence Initiative -Research University ID-UB)
- Topics
- Life Sciences › Neuroscience › Sensory Systems › Olfactory and Sensory Function Studies
- Health Sciences › Medicine › Neurology › Long-Term Effects of COVID-19
- Health Sciences › Medicine › Infectious Diseases › SARS-CoV-2 and COVID-19 Research
- Keywords
- anosmia, COVID-19 pandemic, SARS-CoV-2, olfactory dysfunction, taste disorders, olfactory epithelium, sustentacular cells, asymptomatic carriers
- MeSH terms
- COVID-19, Anosmia, Animals, Brain, Humans, Nasal Mucosa, Smell, Olfactory Perception
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
Are you an author, or do you see a problem with this page? Request a review