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Article ; Online: New evidence suggests SARS-CoV-2 neuroinvasion along the nervus terminalis rather than the olfactory pathway.

von Bartheld, Christopher S / Butowt, Rafal

2024 Volume 147, Issue 1, Page(s) 10

MeSH term(s)	Humans ; Olfactory Pathways ; SARS-CoV-2 ; COVID-19
Language	English
Publishing date	2024-01-06
Publishing country	Germany
Document type	Journal Article
ZDB-ID	1079-0
ISSN	1432-0533 ; 0001-6322
ISSN (online)	1432-0533
ISSN	0001-6322
DOI	10.1007/s00401-023-02664-z
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Article ; Online: Timing and cause of olfactory deciliation in COVID-19.

Butowt, Rafal / von Bartheld, Christopher S

Physiological reviews

2023 Volume 104, Issue 2, Page(s) 589–590

MeSH term(s)	Humans ; COVID-19/complications ; Olfaction Disorders/etiology
Language	English
Publishing date	2023-08-09
Publishing country	United States
Document type	Letter
ZDB-ID	209902-0
ISSN	1522-1210 ; 0031-9333
ISSN (online)	1522-1210
ISSN	0031-9333
DOI	10.1152/physrev.00035.2023
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Article ; Online: The route of SARS-CoV-2 to brain infection: have we been barking up the wrong tree?

Butowt, Rafal / von Bartheld, Christopher S

Molecular neurodegeneration

2022 Volume 17, Issue 1, Page(s) 20

Abstract: This letter draws attention to recent work supporting the notion that the SARS-CoV-2 virus may use the nervus terminalis rather than the olfactory nerve as a shortcut route from the nasal cavity to infect the brain. ...

Abstract	This letter draws attention to recent work supporting the notion that the SARS-CoV-2 virus may use the nervus terminalis rather than the olfactory nerve as a shortcut route from the nasal cavity to infect the brain.
MeSH term(s)	Brain ; COVID-19 ; Humans ; SARS-CoV-2
Language	English
Publishing date	2022-03-15
Publishing country	England
Document type	Letter ; Research Support, N.I.H., Extramural
ZDB-ID	2244557-2
ISSN	1750-1326 ; 1750-1326
ISSN (online)	1750-1326
ISSN	1750-1326
DOI	10.1186/s13024-022-00529-9
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Article ; Online: Olfactory dysfunction in COVID-19: new insights into the underlying mechanisms.

Butowt, Rafal / Bilinska, Katarzyna / von Bartheld, Christopher S

Trends in neurosciences

2022 Volume 46, Issue 1, Page(s) 75–90

Abstract: The mechanisms of olfactory dysfunction in COVID-19 are still unclear. In this review, we examine potential mechanisms that may explain why the sense of smell is lost or altered. Among the current hypotheses, the most plausible is that death of infected ... ...

Abstract	The mechanisms of olfactory dysfunction in COVID-19 are still unclear. In this review, we examine potential mechanisms that may explain why the sense of smell is lost or altered. Among the current hypotheses, the most plausible is that death of infected support cells in the olfactory epithelium causes, besides altered composition of the mucus, retraction of the cilia on olfactory receptor neurons, possibly because of the lack of support cell-derived glucose in the mucus, which powers olfactory signal transduction within the cilia. This mechanism is consistent with the rapid loss of smell with COVID-19, and its rapid recovery after the regeneration of support cells. Host immune responses that cause downregulation of genes involved in olfactory signal transduction occur too late to trigger anosmia, but may contribute to the duration of the olfactory dysfunction.
MeSH term(s)	Humans ; COVID-19/complications ; Smell/physiology ; SARS-CoV-2 ; Olfaction Disorders/etiology ; Olfactory Mucosa
Language	English
Publishing date	2022-11-16
Publishing country	England
Document type	Journal Article ; Review ; Research Support, N.I.H., Extramural ; Research Support, Non-U.S. Gov't
ZDB-ID	282488-7
ISSN	1878-108X ; 0378-5912 ; 0166-2236
ISSN (online)	1878-108X
ISSN	0378-5912 ; 0166-2236
DOI	10.1016/j.tins.2022.11.003
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Article ; Online: Why Does the Omicron Variant Largely Spare Olfactory Function? Implications for the Pathogenesis of Anosmia in Coronavirus Disease 2019.

Butowt, Rafal / Bilińska, Katarzyna / von Bartheld, Christopher

The Journal of infectious diseases

2022 Volume 226, Issue 8, Page(s) 1304–1308

Abstract: The omicron variant of severe acute respiratory syndrome coronavirus 2 causes much less olfactory dysfunction than the previous variants. There are several potential mechanisms for how omicron may change tissue tropism and spare olfactory function. The ... ...

Abstract	The omicron variant of severe acute respiratory syndrome coronavirus 2 causes much less olfactory dysfunction than the previous variants. There are several potential mechanisms for how omicron may change tissue tropism and spare olfactory function. The new mutations make omicron more hydrophobic and alkaline than previous variants, which may reduce penetration of the mucus layer. Overall, the new mutations minimally change receptor binding affinity, but entry efficiency into host cells is reduced in cells expressing transmembrane serine protease 2 (TMPRSS2). Because the support cells in the olfactory epithelium abundantly express TMPRSS2, these main target cells in the olfactory epithelium may become infected less by the new omicron variant.
MeSH term(s)	Angiotensin-Converting Enzyme 2 ; Anosmia ; COVID-19 ; Humans ; SARS-CoV-2 ; Spike Glycoprotein, Coronavirus/metabolism
Chemical Substances	Spike Glycoprotein, Coronavirus ; spike protein, SARS-CoV-2 ; Angiotensin-Converting Enzyme 2 (EC 3.4.17.23)
Language	English
Publishing date	2022-04-04
Publishing country	United States
Document type	Journal Article ; Research Support, N.I.H., Extramural
ZDB-ID	3019-3
ISSN	1537-6613 ; 0022-1899
ISSN (online)	1537-6613
ISSN	0022-1899
DOI	10.1093/infdis/jiac113
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Article ; Online: Anosmia in COVID-19: A Bumpy Road to Establishing a Cellular Mechanism.

Bilinska, Katarzyna / Butowt, Rafal

ACS chemical neuroscience

2020 Volume 11, Issue 15, Page(s) 2152–2155

Abstract: It has become clear since the pandemic broke out that SARS-CoV-2 virus causes reduction of smell and taste in a significant fraction of COVID-19 patients. The olfactory dysfunction often occurs early in the course of the disease, and sometimes it is the ... ...

Abstract	It has become clear since the pandemic broke out that SARS-CoV-2 virus causes reduction of smell and taste in a significant fraction of COVID-19 patients. The olfactory dysfunction often occurs early in the course of the disease, and sometimes it is the only symptom in otherwise asymptomatic carriers. The cellular mechanisms for these specific olfactory disturbances in COVID-19 are now beginning to be elucidated. Several very recent papers contributed to explaining the key cellular steps occurring in the olfactory epithelium leading to anosmia/hyposmia (collectively known as dysosmia) initiated by SARS-CoV-2 infection. In this Viewpoint, we discuss current progress in research on olfactory dysfunction in COVID-19 and we also propose an updated model of the SARS-CoV-2-induced dysosmia. The emerging central role of sustentacular cells and inflammatory processes in the olfactory epithelium are particularly considered. The proposed model of anosmia in COVID-19 does not answer unequivocally whether the new coronavirus exploits the olfactory route to rapidly or slowly reach the brain in COVID-19 patients. To answer this question, new systematic studies using an infectious virus and appropriate animal models are needed.
MeSH term(s)	Animals ; Betacoronavirus ; COVID-19 ; Coronavirus Infections/complications ; Coronavirus Infections/metabolism ; Humans ; Olfaction Disorders/etiology ; Olfaction Disorders/metabolism ; Olfaction Disorders/virology ; Olfactory Receptor Neurons/cytology ; Olfactory Receptor Neurons/metabolism ; Olfactory Receptor Neurons/virology ; Pandemics ; Pneumonia, Viral/complications ; Pneumonia, Viral/metabolism ; SARS-CoV-2 ; Smell/physiology
Keywords	covid19
Language	English
Publishing date	2020-07-16
Publishing country	United States
Document type	Journal Article ; Review
ISSN	1948-7193
ISSN (online)	1948-7193
DOI	10.1021/acschemneuro.0c00406
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Article ; Online: SARS-CoV-2: Olfaction, Brain Infection, and the Urgent Need for Clinical Samples Allowing Earlier Virus Detection.

Butowt, Rafal / Bilinska, Katarzyna

ACS chemical neuroscience

2020 Volume 11, Issue 9, Page(s) 1200–1203

Abstract: The novel SARS-CoV-2 virus has very high infectivity, which allows it to spread rapidly around the world. Attempts at slowing the pandemic at this stage depend on the number and quality of diagnostic tests performed. We propose that the olfactory ... ...

Abstract	The novel SARS-CoV-2 virus has very high infectivity, which allows it to spread rapidly around the world. Attempts at slowing the pandemic at this stage depend on the number and quality of diagnostic tests performed. We propose that the olfactory epithelium from the nasal cavity may be a more appropriate tissue for detection of SARS-CoV-2 virus at the earliest stages, prior to onset of symptoms or even in asymptomatic people, as compared to commonly used sputum or nasopharyngeal swabs. Here we emphasize that the nasal cavity olfactory epithelium is the likely site of enhanced binding of SARS-CoV-2. Multiple non-neuronal cell types present in the olfactory epithelium express two host receptors, ACE2 and TMPRSS2 proteases, that facilitate SARS-CoV-2 binding, replication, and accumulation. This may be the underlying mechanism for the recently reported cases of smell dysfunction in patients with COVID-19. Moreover, the possibility of subsequent brain infection should be considered which begins in olfactory neurons. In addition, we discuss the possibility that olfactory receptor neurons may initiate rapid immune responses at early stages of the disease. We emphasize the need to undertake research focused on additional aspects of SARS-CoV-2 actions in the nervous system, especially in the olfactory pathway.
MeSH term(s)	Angiotensin-Converting Enzyme 2 ; Animals ; Betacoronavirus/growth & development ; Betacoronavirus/immunology ; Betacoronavirus/isolation & purification ; Brain/immunology ; Brain/physiopathology ; Brain/virology ; COVID-19 ; Coronavirus Infections/diagnosis ; Coronavirus Infections/immunology ; Coronavirus Infections/physiopathology ; Coronavirus Infections/transmission ; Early Diagnosis ; Humans ; Immunity, Innate ; Mass Screening/methods ; Mass Screening/standards ; Mice ; Olfactory Mucosa/cytology ; Olfactory Mucosa/immunology ; Olfactory Mucosa/metabolism ; Olfactory Mucosa/virology ; Olfactory Receptor Neurons/immunology ; Olfactory Receptor Neurons/metabolism ; Olfactory Receptor Neurons/virology ; Pandemics ; Peptidyl-Dipeptidase A/metabolism ; Pneumonia, Viral/diagnosis ; Pneumonia, Viral/immunology ; Pneumonia, Viral/physiopathology ; Pneumonia, Viral/transmission ; Respiratory Mucosa/metabolism ; Respiratory Mucosa/virology ; SARS-CoV-2 ; Serine Endopeptidases/metabolism ; Smell ; Virus Replication
Chemical Substances	Peptidyl-Dipeptidase A (EC 3.4.15.1) ; ACE2 protein, human (EC 3.4.17.23) ; Ace2 protein, mouse (EC 3.4.17.23) ; Angiotensin-Converting Enzyme 2 (EC 3.4.17.23) ; Serine Endopeptidases (EC 3.4.21.-) ; TMPRSS2 protein, human (EC 3.4.21.-)
Keywords	covid19
Language	English
Publishing date	2020-04-13
Publishing country	United States
Document type	Journal Article ; Research Support, Non-U.S. Gov't
ISSN	1948-7193
ISSN (online)	1948-7193
DOI	10.1021/acschemneuro.0c00172
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Article ; Online: New study on prevalence of anosmia in COVID-19 implicates the D614G virus mutation as a major contributing factor to chemosensory dysfunction.

von Bartheld, Christopher S / Mathew, Dennis / Butowt, Rafal

European archives of oto-rhino-laryngology : official journal of the European Federation of Oto-Rhino-Laryngological Societies (EUFOS) : affiliated with the German Society for Oto-Rhino-Laryngology - Head and Neck Surgery

2021 Volume 278, Issue 9, Page(s) 3593–3594

MeSH term(s)	Anosmia ; COVID-19 ; Humans ; Mutation ; Olfaction Disorders/etiology ; Olfaction Disorders/genetics ; Prevalence ; SARS-CoV-2
Language	English
Publishing date	2021-03-31
Publishing country	Germany
Document type	Letter
ZDB-ID	1017359-6
ISSN	1434-4726 ; 0937-4477
ISSN (online)	1434-4726
ISSN	0937-4477
DOI	10.1007/s00405-021-06759-9
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Article ; Online: The D614G Virus Mutation Enhances Anosmia in COVID-19 Patients: Evidence from a Systematic Review and Meta-analysis of Studies from South Asia.

von Bartheld, Christopher S / Hagen, Molly M / Butowt, Rafal

ACS chemical neuroscience

2021 Volume 12, Issue 19, Page(s) 3535–3549

Abstract: The prevalence of chemosensory dysfunction in patients with COVID-19 varies greatly between populations. It is unclear whether such differences are due to factors at the level of the human host, or at the level of the coronavirus, or both. At the host ... ...

Abstract	The prevalence of chemosensory dysfunction in patients with COVID-19 varies greatly between populations. It is unclear whether such differences are due to factors at the level of the human host, or at the level of the coronavirus, or both. At the host level, the entry proteins which allow virus binding and entry have variants with distinct properties, and the frequency of such variants differs between ethnicities. At the level of the virus, the D614G mutation enhances virus entry to the host cell. Since the two virus strains (D614 and G614) coexisted in the first six months of the pandemic in most populations, it has been difficult to distinguish between contributions of the virus and contributions of the host for anosmia. To answer this question, we conducted a systematic review and meta-analysis of studies in South Asian populations when either the D614 or the G614 virus was dominant. We show that populations infected predominantly with the G614 virus had a much higher prevalence of anosmia (pooled prevalence of 31.8%) compared with the same ethnic populations infected mostly with the D614 virus strain (pooled anosmia prevalence of 5.3%). We conclude that the D614G mutation is a major contributing factor that increases the prevalence of anosmia in COVID-19, and that this enhanced effect on olfaction constitutes a previously unrecognized phenotype of the D614G mutation. The new virus strains that have additional mutations on the background of the D614G mutation can be expected to cause a similarly increased prevalence of chemosensory dysfunctions.
MeSH term(s)	Anosmia ; COVID-19 ; Humans ; Mutation/genetics ; SARS-CoV-2 ; Spike Glycoprotein, Coronavirus/genetics
Chemical Substances	Spike Glycoprotein, Coronavirus
Language	English
Publishing date	2021-09-17
Publishing country	United States
Document type	Journal Article ; Meta-Analysis ; Research Support, N.I.H., Extramural ; Research Support, Non-U.S. Gov't ; Systematic Review
ISSN	1948-7193
ISSN (online)	1948-7193
DOI	10.1021/acschemneuro.1c00542
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Article: Expression of the ACE2 Virus Entry Protein in the Nervus Terminalis Reveals the Potential for an Alternative Route to Brain Infection in COVID-19.

Bilinska, Katarzyna / von Bartheld, Christopher S / Butowt, Rafal

Frontiers in cellular neuroscience

2021 Volume 15, Page(s) 674123

Abstract: Previous studies suggested that the SARS-CoV-2 virus may gain access to the brain by using a route along the olfactory nerve. However, there is a general consensus that the obligatory virus entry receptor, angiotensin converting enzyme 2 (ACE2), is not ... ...

Abstract	Previous studies suggested that the SARS-CoV-2 virus may gain access to the brain by using a route along the olfactory nerve. However, there is a general consensus that the obligatory virus entry receptor, angiotensin converting enzyme 2 (ACE2), is not expressed in olfactory receptor neurons, and the timing of arrival of the virus in brain targets is inconsistent with a neuronal transfer along olfactory projections. We determined whether nervus terminalis neurons and their peripheral and central projections should be considered as a potential alternative route from the nose to the brain. Nervus terminalis neurons in postnatal mice were double-labeled with antibodies against ACE2 and two nervus terminalis markers, gonadotropin-releasing hormone (GnRH) and choline acetyltransferase (CHAT). We show that a small fraction of CHAT-labeled nervus terminalis neurons, and the large majority of GnRH-labeled nervus terminalis neurons with cell bodies in the region between the olfactory epithelium and the olfactory bulb express ACE2 and cathepsins B and L. Nervus terminalis neurons therefore may provide a direct route for the virus from the nasal epithelium, possibly via innervation of Bowman's glands, to brain targets, including the telencephalon and diencephalon. This possibility needs to be examined in suitable animal models and in human tissues.
Language	English
Publishing date	2021-07-05
Publishing country	Switzerland
Document type	Journal Article
ZDB-ID	2452963-1
ISSN	1662-5102
ISSN	1662-5102
DOI	10.3389/fncel.2021.674123
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