More Than Smell-COVID-19 Is Associated With Severe Impairment of Smell, Taste, and Chemesthesis

doi:10.1093/chemse/bjaa041

. 2020 Oct 9;45(7):609-622.

doi: 10.1093/chemse/bjaa041.

More Than Smell-COVID-19 Is Associated With Severe Impairment of Smell, Taste, and Chemesthesis

Valentina Parma¹, Kathrin Ohla², Maria G Veldhuizen³, Masha Y Niv⁴, Christine E Kelly⁵, Alyssa J Bakke⁶, Keiland W Cooper⁷, Cédric Bouysset⁸, Nicola Pirastu⁹, Michele Dibattista¹⁰, Rishemjit Kaur¹¹, Marco Tullio Liuzza¹², Marta Y Pepino¹³, Veronika Schöpf¹⁴, Veronica Pereda-Loth¹⁵, Shannon B Olsson¹⁶, Richard C Gerkin¹⁷, Paloma Rohlfs Domínguez¹⁸, Javier Albayay¹⁹, Michael C Farruggia²⁰, Surabhi Bhutani²¹, Alexander W Fjaeldstad²², Ritesh Kumar²³, Anna Menini²⁴, Moustafa Bensafi²⁵, Mari Sandell^{26

27}, Iordanis Konstantinidis²⁸, Antonella Di Pizio²⁹, Federica Genovese³⁰, Lina Öztürk³, Thierry Thomas-Danguin³¹, Johannes Frasnelli³², Sanne Boesveldt³³, Özlem Saatci³⁴, Luis R Saraiva^{30

35}, Cailu Lin³⁰, Jérôme Golebiowski⁸, Liang-Dar Hwang³⁶, Mehmet Hakan Ozdener³⁰, Maria Dolors Guàrdia³⁷, Christophe Laudamiel³⁸, Marina Ritchie³⁹, Jan Havlícek⁴⁰, Denis Pierron⁴¹, Eugeni Roura⁴², Marta Navarro⁴², Alissa A Nolden⁴³, Juyun Lim⁴⁴, Katherine L Whitcroft⁴⁵, Lauren R Colquitt³⁰, Camille Ferdenzi²⁵, Evelyn V Brindha⁴⁶, Aytug Altundag⁴⁷, Alberto Macchi⁴⁸, Alexia Nunez-Parra⁴⁹, Zara M Patel⁵⁰, Sébastien Fiorucci⁸, Carl M Philpott⁵¹, Barry C Smith⁵², Johan N Lundström^{30

53}, Carla Mucignat⁵⁴, Jane K Parker⁵⁵, Mirjam van den Brink⁵⁶, Michael Schmuker²³, Florian Ph S Fischmeister⁵⁷, Thomas Heinbockel⁵⁸, Vonnie D C Shields⁵⁹, Farhoud Faraji⁶⁰, Enrique Santamaría⁶¹, William E A Fredborg⁶², Gabriella Morini⁶³, Jonas K Olofsson⁶², Maryam Jalessi⁶⁴, Noam Karni⁶⁵, Anna D'Errico⁶⁶, Rafieh Alizadeh⁶⁷, Robert Pellegrino⁶⁸, Pablo Meyer⁶⁹, Caroline Huart⁷⁰, Ben Chen⁷¹, Graciela M Soler⁷², Mohammed K Alwashahi⁷³, Antje Welge-Lüssen⁷⁴, Jessica Freiherr⁷⁵, Jasper H B de Groot⁷⁶, Hadar Klein⁴, Masako Okamoto⁷⁷, Preet Bano Singh⁷⁸, Julien W Hsieh⁷⁹; GCCR Group Author; Danielle R Reed³⁰, Thomas Hummel⁸⁰, Steven D Munger^{81

82}, John E Hayes⁶

Collaborators, Affiliations

Affiliations

¹ Department of Psychology, Temple University, Philadelphia, PA, USA.
² Institute of Neuroscience and Medicine (INM-3), Research Center Jülich, Wilhelm-Johnen-Straße, Jülich, Germany.
³ Department of Anatomy, Faculty of Medicine, Mersin University, Çiftlikköy Campus, Yenişehir, Mersin, Turkey.
⁴ Institute of Biochemistry, Food Science and Nutrition, The Hebrew University of Jerusalem, Rehovot, Israel.
⁵ AbScent, Andover, Hampshire, UK.
⁶ Department of Food Science, The Pennsylvania State University, Erickson Food Science Building, University Park, PA, USA.
⁷ Center for the Neurobiology of Learning and Memory, University of California and Qureshey Research Laboratory, Irvine, CA, USA.
⁸ Institut de Chimie de Nice, UMR CNRS 7272, Université Côte d'Azur, Avenue Valrose, Nice, France.
⁹ Centre for Global Health Research, Usher Institute, The University of Edinburgh, Old Medical School, Teviot Place, Edinburgh, UK.
¹⁰ Department of Basic Medical Sciences, Neuroscience and Sensory Organs, Università degli Studi di Bari A. Moro, P.zza G. Cesare, Bari, Italy.
¹¹ CSIR-Central Scientific Instruments Organisation, Chandigarh, India.
¹² Department of Medical and Surgical Sciences, "Magna Graecia" University of Catanzaro, Viale Europa (Loc. Germaneto), Catanzaro, Italy.
¹³ Department of Food Science and Human Nutrition and Division of Nutritional Sciences, University of Illinois at Urbana Champaign, Urbana, IL, USA.
¹⁴ Department of Biomedical Imaging and Image-guided Therapy, Medical University of Vienna, Währinger Gürtel, Vienna, Austria.
¹⁵ Laboratoire d'Anthropologie Moléculaire et Imagerie de Synthese, UMR 5288 CNRS, Universitéde Toulouse, Toulouse, France.
¹⁶ National Centre for Biological Sciences, Tata Institute of Fundamental Research, GKVK Campus, Bengaluru, India.
¹⁷ School of Life Sciences, Arizona State University, Tempe, AZ, USA.
¹⁸ Department of Psychology and Anthropology, University of Extremadura, Avenida de la Universidad, s/n, Cáceres, Spain.
¹⁹ Department of General Psychology, University of Padova, Via Venezia, Padova, Italy.
²⁰ Department of Psychiatry, Yale University School of Medicine, New Haven, CT, USA.
²¹ School of Exercise and Nutritional Sciences, 5500 Campanile Drive, San Diego State University, San Diego, CA, USA.
²² Flavour Clinic, Department of Otorhinolaryngology, Regional Hospital West Jutland, Central Denmark Region, Laegaardvej, Holstebro, Denmark.
²³ Biocomputation Group, Department of Computer Science, University of Hertfordshire, Hatfield, UK.
²⁴ Neuroscience Area, International School for Advanced Studies, SISSA, Via Bonomea, Trieste, Italy.
²⁵ Neuropop Team, Lyon Neuroscience Research Center, CNRS UMR5292-INSERM U1028-University Claude Bernard Lyon 1, 95 bd Pinel, Bron, France.
²⁶ Department of Food and Nutrition, University of Helsinki, Helsinki, Finland.
²⁷ Functional Foods Forum, University of Turku, Turku, Finland.
²⁸ 2nd Academic Otorhinolaryngology Department, Aristotle University, Thessaloniki, Greece.
²⁹ Leibniz-Institute for Food Systems Biology at the Technical University of Munich, Lise-Meitner-Str., Freising, Germany.
³⁰ Monell Chemical Senses Center, Philadelphia, PA, USA.
³¹ CSGA-Centre for Taste and Feeding Behavior, INRAE, CNRS, AgroSup Dijon, Université Bourgogne Franche-Comté, 17 rue Sully, Dijon, France.
³² Department of Anatomy, Université du Québec à Trois-Rivières, boul. des Forges, Trois-Rivières, QC, Canada.
³³ Division of Human Nutrition and Health, Wageningen University, Stippeneng, WE Wageningen, the Netherlands.
³⁴ Department of Otorhinolaryngology, Medical Science University, Emek, Sancaktepe-İstanbul, Turkey.
³⁵ Sidra Medicine, Out Patient Clinic, Doha, Qatar.
³⁶ The University of Queensland Diamantina Institute, The University of Queensland, Woolloongabba, QLD, Australia.
³⁷ IRTA-Food Technology Programme, IRTA, Finca Camps i Armet, Monells, Girona, Spain.
³⁸ DreamAir LLC, Department of Scent Engineering, Broadway, New York, NY, USA.
³⁹ Department of Neurobiology and Behavior, University of California, Irvine, Irvine, CA, USA.
⁴⁰ Department of Zoology, Charles University, Viničná, Nové Město, Czechia.
⁴¹ Équipe de Médecine Evolutive, UMR5288 CNRS/Université Toulouse III, faculté de chirurgie dentaire, 3 Chemin des Maraîchers, Toulouse, France.
⁴² Centre for Nutrition and Food Sciences, Queensland Alliance for Agriculture and Food Innovation, The University of Queensland, St Lucia, QLD, Australia.
⁴³ Department of Food Science, University of Massachusetts, Holdsworth Way, Amherst, MA, USA.
⁴⁴ Department of Food Science and Technology, Oregon State University, Corvallis, OR, USA.
⁴⁵ Ear Institute, University College London, London, UK.
⁴⁶ Department of Electrical and Electronics Engineering, Karunya Institute of Technology and Sciences, Karunya Nagar, Coimbatore, Tamilnadu, India.
⁴⁷ Otorhinolaryngology Department, Biruni University, Protokol Yolu, Topkapı, Zeytinburnu, Istanbul, Turkey.
⁴⁸ Italian Academy of Rhinology Asst Settelaghi-University of Insubriae, via Guicciardini, Varese, Italy.
⁴⁹ Department of Biology, Universidad de Chile, Las Palmeras, Santiago, Chile.
⁵⁰ Department of Otolaryngology-Head and Neck Surgery, Stanford University School of Medicine, Palo Alto, CA, USA.
⁵¹ The Norfolk Smell and Taste Clinic, University of East Anglia, Norwich Research Park, Norwich, UK.
⁵² Centre for the Study of the Senses, Institute of Philosophy, School of Advanced Study, University of London, London, UK.
⁵³ Department of Clinical Neuroscience, Karolinska Institutet, Nobels väg, Stockholm, Sweden.
⁵⁴ Department of Molecular Medicine, University of Padova, via Marzolo, Padova, Italy.
⁵⁵ Department of Food and Nutritional Sciences, University of Reading, Whiteknights, Reading, UK.
⁵⁶ Laboratory of Behavioural Gastronomy, Maastricht University Campus Venlo, Nassaustraat, BV Venlo, the Netherlands.
⁵⁷ Institute of Psychology, University of Graz, Universitätsplatz 2, Graz, Austria.
⁵⁸ Department of Anatomy, College of Medicine, Howard University, N.W., Washington, DC, USA.
⁵⁹ Biological Sciences Department, Fisher College of Science and Mathematics, Towson University, Towson, MD USA.
⁶⁰ Division of Otolaryngology, Head & Neck Surgery, University of California San Diego Health, MC La Jolla, CA, USA.
⁶¹ Clinical Neuroproteomics Unit, Navarrabiomed, Complejo Hospitalario de Navarra (CHN), Universidad pública de Navarra (UPNA), Instituto de Investigación Sanitaria de Navarra (IDISNA), Proteored-ISCIII, Pamplona, Spain.
⁶² Department of Psychology, Stockholm University, Frescativägen, Stockholm, Sweden.
⁶³ University of Gastronomic Sciences, Piazza Vittorio Emanuele II 9, Bra, Pollenzo, CN, Italy.
⁶⁴ Skull Base Research Center, The Five Senses Institute, Iran University of Medical Sciences, Rasoul Akram Hospital, Sattarkhan Ave., Tehran, Iran.
⁶⁵ Internal Medicine Department, Hadassah Medical Center, Kiryat Hadassah, Jerusalem, Israel.
⁶⁶ Department of Molecular and Cellular Neurobiology, Goethe Universität Frankfurt, Goethe Universität Frankfurt, Max von Laue Strasse, Frankfurt am Main, Germany.
⁶⁷ ENT and Head and Neck Research Center and Department, Hazrat Rasoul Hospital, The Five Senses Institute, Iran University of Medical Sciences, Iran University of Medical Sciences, Shahid Hemmat Highway, Tehran, Iran.
⁶⁸ Food Science Department, University of Tennessee, Knoxville, TN, USA.
⁶⁹ Health Care and Life Sciences, IBM T. J. Watson Research Center, Yorktown Heights, NY, USA.
⁷⁰ Department of Otorhinolaryngology, Cliniques Universitaires Saint-Luc, Avenue Hippocrate, Brussels, Belgium.
⁷¹ Department of Psychiatry, The Affiliated Brain Hospital of Guangzhou Medical University, Liwan District, Guangzhou City, China.
⁷² Department of Otorhinolaringology, Buenos Aires University and GEOG (Grupo de Estudio de Olfato y Gusto), Calle Paraguay, Piso 3. CABA (Ciudad Autónoma de Buenos Aires), Argentina.
⁷³ Surgery Department, ENT Division, Sultan Qaboos University Hospital, Al Khoud, Muscat, Oman.
⁷⁴ Department of Otorhinolaryngology, University Hospital Basel, Petersgraben, Basel, Switzerland.
⁷⁵ Department of Psychiatry and Psychotherapy, Friedrich-Alexander-Universität Erlangen-Nürnberg, Schwabachanlage, Erlangen, Germany.
⁷⁶ Department of Psychology, Utrecht University, Heidelberglaan 1, CS Utrecht, The Netherlands.
⁷⁷ Department of Applied Biological Chemistry, The University of Tokyo, Yayoi, Bunkyo-ku, Tokyo, Japan.
⁷⁸ Department of Oral Surgery and Oral Medicine, Faculty of Dentistry, University of Oslo, Blindern, Oslo, Norway.
⁷⁹ Rhinology-Olfactology Unit, ENT Department, Geneva University Hospitals, Rue Gabrielle-Perret-Gentil, Geneva, Switzerland.
⁸⁰ Department of Otorhinolaryngology, TU Dresden, Helmholtzstr., Dresden, Germany.
⁸¹ Center for Smell and Taste, University of Florida, , Rm LG-101D, Gainesville, FL, USA.
⁸² Department of Pharmacology and Therapeutics, University of Florida, Gainesville, FL, USA.

PMID: 32564071
PMCID: PMC7337664
DOI: 10.1093/chemse/bjaa041

More Than Smell-COVID-19 Is Associated With Severe Impairment of Smell, Taste, and Chemesthesis

Valentina Parma et al. Chem Senses. 2020.

. 2020 Oct 9;45(7):609-622.

doi: 10.1093/chemse/bjaa041.

Authors

Affiliations

¹ Department of Psychology, Temple University, Philadelphia, PA, USA.
² Institute of Neuroscience and Medicine (INM-3), Research Center Jülich, Wilhelm-Johnen-Straße, Jülich, Germany.
³ Department of Anatomy, Faculty of Medicine, Mersin University, Çiftlikköy Campus, Yenişehir, Mersin, Turkey.
⁴ Institute of Biochemistry, Food Science and Nutrition, The Hebrew University of Jerusalem, Rehovot, Israel.
⁵ AbScent, Andover, Hampshire, UK.
⁶ Department of Food Science, The Pennsylvania State University, Erickson Food Science Building, University Park, PA, USA.
⁷ Center for the Neurobiology of Learning and Memory, University of California and Qureshey Research Laboratory, Irvine, CA, USA.
⁸ Institut de Chimie de Nice, UMR CNRS 7272, Université Côte d'Azur, Avenue Valrose, Nice, France.
⁹ Centre for Global Health Research, Usher Institute, The University of Edinburgh, Old Medical School, Teviot Place, Edinburgh, UK.
¹⁰ Department of Basic Medical Sciences, Neuroscience and Sensory Organs, Università degli Studi di Bari A. Moro, P.zza G. Cesare, Bari, Italy.
¹¹ CSIR-Central Scientific Instruments Organisation, Chandigarh, India.
¹² Department of Medical and Surgical Sciences, "Magna Graecia" University of Catanzaro, Viale Europa (Loc. Germaneto), Catanzaro, Italy.
¹³ Department of Food Science and Human Nutrition and Division of Nutritional Sciences, University of Illinois at Urbana Champaign, Urbana, IL, USA.
¹⁴ Department of Biomedical Imaging and Image-guided Therapy, Medical University of Vienna, Währinger Gürtel, Vienna, Austria.
¹⁵ Laboratoire d'Anthropologie Moléculaire et Imagerie de Synthese, UMR 5288 CNRS, Universitéde Toulouse, Toulouse, France.
¹⁶ National Centre for Biological Sciences, Tata Institute of Fundamental Research, GKVK Campus, Bengaluru, India.
¹⁷ School of Life Sciences, Arizona State University, Tempe, AZ, USA.
¹⁸ Department of Psychology and Anthropology, University of Extremadura, Avenida de la Universidad, s/n, Cáceres, Spain.
¹⁹ Department of General Psychology, University of Padova, Via Venezia, Padova, Italy.
²⁰ Department of Psychiatry, Yale University School of Medicine, New Haven, CT, USA.
²¹ School of Exercise and Nutritional Sciences, 5500 Campanile Drive, San Diego State University, San Diego, CA, USA.
²² Flavour Clinic, Department of Otorhinolaryngology, Regional Hospital West Jutland, Central Denmark Region, Laegaardvej, Holstebro, Denmark.
²³ Biocomputation Group, Department of Computer Science, University of Hertfordshire, Hatfield, UK.
²⁴ Neuroscience Area, International School for Advanced Studies, SISSA, Via Bonomea, Trieste, Italy.
²⁵ Neuropop Team, Lyon Neuroscience Research Center, CNRS UMR5292-INSERM U1028-University Claude Bernard Lyon 1, 95 bd Pinel, Bron, France.
²⁶ Department of Food and Nutrition, University of Helsinki, Helsinki, Finland.
²⁷ Functional Foods Forum, University of Turku, Turku, Finland.
²⁸ 2nd Academic Otorhinolaryngology Department, Aristotle University, Thessaloniki, Greece.
²⁹ Leibniz-Institute for Food Systems Biology at the Technical University of Munich, Lise-Meitner-Str., Freising, Germany.
³⁰ Monell Chemical Senses Center, Philadelphia, PA, USA.
³¹ CSGA-Centre for Taste and Feeding Behavior, INRAE, CNRS, AgroSup Dijon, Université Bourgogne Franche-Comté, 17 rue Sully, Dijon, France.
³² Department of Anatomy, Université du Québec à Trois-Rivières, boul. des Forges, Trois-Rivières, QC, Canada.
³³ Division of Human Nutrition and Health, Wageningen University, Stippeneng, WE Wageningen, the Netherlands.
³⁴ Department of Otorhinolaryngology, Medical Science University, Emek, Sancaktepe-İstanbul, Turkey.
³⁵ Sidra Medicine, Out Patient Clinic, Doha, Qatar.
³⁶ The University of Queensland Diamantina Institute, The University of Queensland, Woolloongabba, QLD, Australia.
³⁷ IRTA-Food Technology Programme, IRTA, Finca Camps i Armet, Monells, Girona, Spain.
³⁸ DreamAir LLC, Department of Scent Engineering, Broadway, New York, NY, USA.
³⁹ Department of Neurobiology and Behavior, University of California, Irvine, Irvine, CA, USA.
⁴⁰ Department of Zoology, Charles University, Viničná, Nové Město, Czechia.
⁴¹ Équipe de Médecine Evolutive, UMR5288 CNRS/Université Toulouse III, faculté de chirurgie dentaire, 3 Chemin des Maraîchers, Toulouse, France.
⁴² Centre for Nutrition and Food Sciences, Queensland Alliance for Agriculture and Food Innovation, The University of Queensland, St Lucia, QLD, Australia.
⁴³ Department of Food Science, University of Massachusetts, Holdsworth Way, Amherst, MA, USA.
⁴⁴ Department of Food Science and Technology, Oregon State University, Corvallis, OR, USA.
⁴⁵ Ear Institute, University College London, London, UK.
⁴⁶ Department of Electrical and Electronics Engineering, Karunya Institute of Technology and Sciences, Karunya Nagar, Coimbatore, Tamilnadu, India.
⁴⁷ Otorhinolaryngology Department, Biruni University, Protokol Yolu, Topkapı, Zeytinburnu, Istanbul, Turkey.
⁴⁸ Italian Academy of Rhinology Asst Settelaghi-University of Insubriae, via Guicciardini, Varese, Italy.
⁴⁹ Department of Biology, Universidad de Chile, Las Palmeras, Santiago, Chile.
⁵⁰ Department of Otolaryngology-Head and Neck Surgery, Stanford University School of Medicine, Palo Alto, CA, USA.
⁵¹ The Norfolk Smell and Taste Clinic, University of East Anglia, Norwich Research Park, Norwich, UK.
⁵² Centre for the Study of the Senses, Institute of Philosophy, School of Advanced Study, University of London, London, UK.
⁵³ Department of Clinical Neuroscience, Karolinska Institutet, Nobels väg, Stockholm, Sweden.
⁵⁴ Department of Molecular Medicine, University of Padova, via Marzolo, Padova, Italy.
⁵⁵ Department of Food and Nutritional Sciences, University of Reading, Whiteknights, Reading, UK.
⁵⁶ Laboratory of Behavioural Gastronomy, Maastricht University Campus Venlo, Nassaustraat, BV Venlo, the Netherlands.
⁵⁷ Institute of Psychology, University of Graz, Universitätsplatz 2, Graz, Austria.
⁵⁸ Department of Anatomy, College of Medicine, Howard University, N.W., Washington, DC, USA.
⁵⁹ Biological Sciences Department, Fisher College of Science and Mathematics, Towson University, Towson, MD USA.
⁶⁰ Division of Otolaryngology, Head & Neck Surgery, University of California San Diego Health, MC La Jolla, CA, USA.
⁶¹ Clinical Neuroproteomics Unit, Navarrabiomed, Complejo Hospitalario de Navarra (CHN), Universidad pública de Navarra (UPNA), Instituto de Investigación Sanitaria de Navarra (IDISNA), Proteored-ISCIII, Pamplona, Spain.
⁶² Department of Psychology, Stockholm University, Frescativägen, Stockholm, Sweden.
⁶³ University of Gastronomic Sciences, Piazza Vittorio Emanuele II 9, Bra, Pollenzo, CN, Italy.
⁶⁴ Skull Base Research Center, The Five Senses Institute, Iran University of Medical Sciences, Rasoul Akram Hospital, Sattarkhan Ave., Tehran, Iran.
⁶⁵ Internal Medicine Department, Hadassah Medical Center, Kiryat Hadassah, Jerusalem, Israel.
⁶⁶ Department of Molecular and Cellular Neurobiology, Goethe Universität Frankfurt, Goethe Universität Frankfurt, Max von Laue Strasse, Frankfurt am Main, Germany.
⁶⁷ ENT and Head and Neck Research Center and Department, Hazrat Rasoul Hospital, The Five Senses Institute, Iran University of Medical Sciences, Iran University of Medical Sciences, Shahid Hemmat Highway, Tehran, Iran.
⁶⁸ Food Science Department, University of Tennessee, Knoxville, TN, USA.
⁶⁹ Health Care and Life Sciences, IBM T. J. Watson Research Center, Yorktown Heights, NY, USA.
⁷⁰ Department of Otorhinolaryngology, Cliniques Universitaires Saint-Luc, Avenue Hippocrate, Brussels, Belgium.
⁷¹ Department of Psychiatry, The Affiliated Brain Hospital of Guangzhou Medical University, Liwan District, Guangzhou City, China.
⁷² Department of Otorhinolaringology, Buenos Aires University and GEOG (Grupo de Estudio de Olfato y Gusto), Calle Paraguay, Piso 3. CABA (Ciudad Autónoma de Buenos Aires), Argentina.
⁷³ Surgery Department, ENT Division, Sultan Qaboos University Hospital, Al Khoud, Muscat, Oman.
⁷⁴ Department of Otorhinolaryngology, University Hospital Basel, Petersgraben, Basel, Switzerland.
⁷⁵ Department of Psychiatry and Psychotherapy, Friedrich-Alexander-Universität Erlangen-Nürnberg, Schwabachanlage, Erlangen, Germany.
⁷⁶ Department of Psychology, Utrecht University, Heidelberglaan 1, CS Utrecht, The Netherlands.
⁷⁷ Department of Applied Biological Chemistry, The University of Tokyo, Yayoi, Bunkyo-ku, Tokyo, Japan.
⁷⁸ Department of Oral Surgery and Oral Medicine, Faculty of Dentistry, University of Oslo, Blindern, Oslo, Norway.
⁷⁹ Rhinology-Olfactology Unit, ENT Department, Geneva University Hospitals, Rue Gabrielle-Perret-Gentil, Geneva, Switzerland.
⁸⁰ Department of Otorhinolaryngology, TU Dresden, Helmholtzstr., Dresden, Germany.
⁸¹ Center for Smell and Taste, University of Florida, , Rm LG-101D, Gainesville, FL, USA.
⁸² Department of Pharmacology and Therapeutics, University of Florida, Gainesville, FL, USA.

PMID: 32564071
PMCID: PMC7337664
DOI: 10.1093/chemse/bjaa041

Erratum in

Corrigendum to: More Than Smell-COVID-19 Is Associated With Severe Impairment of Smell, Taste, and Chemesthesis.
Parma V, Ohla K, Veldhuizen MG, Niv MY, Kelly CE, Bakke AJ, Cooper KW, Bouysset C, Pirastu N, Dibattista M, Kaur R, Liuzza MT, Pepino MY, Schöpf V, Pereda-Loth V, Olsson SB, Gerkin RC, Rohlfs Domínguez P, Albayay J, Farruggia MC, Bhutani S, Fjaeldstad AW, Kumar R, Menini A, Bensafi M, Sandell M, Konstantinidis I, Di Pizio A, Genovese F, Öztürk L, Thomas-Danguin T, Frasnelli J, Boesveldt S, Saatci Ö, Saraiva LR, Lin C, Golebiowski J, Hwang LD, Ozdener MH, Guàrdia MD, Laudamiel C, Ritchie M, Havlícek J, Pierron D, Roura E, Navarro M, Nolden AA, Lim J, Whitcroft KL, Colquitt LR, Ferdenzi C, Brindha EV, Altundag A, Macchi A, Nunez-Parra A, Patel ZM, Fiorucci S, Philpott CM, Smith BC, Lundström JN, Mucignat C, Parker JK, van den Brink M, Schmuker M, Fischmeister FPS, Heinbockel T, Shields VDC, Faraji F, Santamaría E, Fredborg WEA, Morini G, Olofsson JK, Jalessi M, Karni N, D'Errico A, Alizadeh R, Pellegrino R, Meyer P, Huart C, Chen B, Soler GM, Alwashahi MK, Welge-Lüssen A, Freiherr J, de Groot JHB, Klein H, Okamoto M, Singh PB, Hsieh JW; GCCR Group Author; Reed DR, Hummel T, Munger SD, Hayes JE. Parma V, et al. Chem Senses. 2021 Jan 1;46:bjab050. doi: 10.1093/chemse/bjab050. Chem Senses. 2021. PMID: 34879393 Free PMC article. No abstract available.

Abstract

Recent anecdotal and scientific reports have provided evidence of a link between COVID-19 and chemosensory impairments, such as anosmia. However, these reports have downplayed or failed to distinguish potential effects on taste, ignored chemesthesis, and generally lacked quantitative measurements. Here, we report the development, implementation, and initial results of a multilingual, international questionnaire to assess self-reported quantity and quality of perception in 3 distinct chemosensory modalities (smell, taste, and chemesthesis) before and during COVID-19. In the first 11 days after questionnaire launch, 4039 participants (2913 women, 1118 men, and 8 others, aged 19-79) reported a COVID-19 diagnosis either via laboratory tests or clinical assessment. Importantly, smell, taste, and chemesthetic function were each significantly reduced compared to their status before the disease. Difference scores (maximum possible change ±100) revealed a mean reduction of smell (-79.7 ± 28.7, mean ± standard deviation), taste (-69.0 ± 32.6), and chemesthetic (-37.3 ± 36.2) function during COVID-19. Qualitative changes in olfactory ability (parosmia and phantosmia) were relatively rare and correlated with smell loss. Importantly, perceived nasal obstruction did not account for smell loss. Furthermore, chemosensory impairments were similar between participants in the laboratory test and clinical assessment groups. These results show that COVID-19-associated chemosensory impairment is not limited to smell but also affects taste and chemesthesis. The multimodal impact of COVID-19 and the lack of perceived nasal obstruction suggest that severe acute respiratory syndrome coronavirus strain 2 (SARS-CoV-2) infection may disrupt sensory-neural mechanisms.

Keywords: head and neck surgery; olfaction; somatosensation.

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Comment in

Altered taste in patients with COVID-19: The potential role of salivary glands.
da Silva Pedrosa M, Sipert CR, Nogueira FN. da Silva Pedrosa M, et al. Oral Dis. 2021 Apr;27 Suppl 3(Suppl 3):798-800. doi: 10.1111/odi.13496. Epub 2020 Jul 13. Oral Dis. 2021. PMID: 32564416 Free PMC article. No abstract available.

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More Than Smell-COVID-19 Is Associated With Severe Impairment of Smell, Taste, and Chemesthesis

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More Than Smell-COVID-19 Is Associated With Severe Impairment of Smell, Taste, and Chemesthesis

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