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

Author:

Parma Valentina1,Ohla Kathrin2ORCID,Veldhuizen Maria G3,Niv Masha Y4,Kelly Christine E5,Bakke Alyssa J6,Cooper Keiland W7,Bouysset Cédric8,Pirastu Nicola9,Dibattista Michele10,Kaur Rishemjit11,Liuzza Marco Tullio12ORCID,Pepino Marta Y13,Schöpf Veronika14,Pereda-Loth Veronica15,Olsson Shannon B16,Gerkin Richard C17ORCID,Rohlfs Domínguez Paloma18,Albayay Javier19,Farruggia Michael C20,Bhutani Surabhi21,Fjaeldstad Alexander W22ORCID,Kumar Ritesh23,Menini Anna24,Bensafi Moustafa25ORCID,Sandell Mari2627,Konstantinidis Iordanis28,Di Pizio Antonella29,Genovese Federica30,Öztürk Lina3,Thomas-Danguin Thierry31,Frasnelli Johannes32,Boesveldt Sanne33,Saatci Özlem34,Saraiva Luis R3035ORCID,Lin Cailu30ORCID,Golebiowski Jérôme8,Hwang Liang-Dar36,Ozdener Mehmet Hakan30,Guàrdia Maria Dolors37,Laudamiel Christophe38,Ritchie Marina39,Havlícek Jan40,Pierron Denis41,Roura Eugeni42ORCID,Navarro Marta42,Nolden Alissa A43,Lim Juyun44ORCID,Whitcroft Katherine L45,Colquitt Lauren R30,Ferdenzi Camille25ORCID,Brindha Evelyn V46,Altundag Aytug47,Macchi Alberto48,Nunez-Parra Alexia49,Patel Zara M50,Fiorucci Sébastien8,Philpott Carl M51ORCID,Smith Barry C52ORCID,Lundström Johan N3053ORCID,Mucignat Carla54,Parker Jane K55,van den Brink Mirjam56,Schmuker Michael23,Fischmeister Florian Ph S57,Heinbockel Thomas58,Shields Vonnie D C59,Faraji Farhoud60,Santamaría Enrique61,Fredborg William E A62,Morini Gabriella63,Olofsson Jonas K62ORCID,Jalessi Maryam64,Karni Noam65,D’Errico Anna66,Alizadeh Rafieh67ORCID,Pellegrino Robert68,Meyer Pablo69,Huart Caroline70,Chen Ben71,Soler Graciela M72,Alwashahi Mohammed K73,Welge-Lüssen Antje74,Freiherr Jessica75ORCID,de Groot Jasper H B76,Klein Hadar4,Okamoto Masako77,Singh Preet Bano78,Hsieh Julien W79,Abdulrahman Olagunju,Dalton Pamela,Yan Carol H,Voznessenskaya Vera V,Chen Jingguo,Sell Elizabeth A,Walsh-Messinger Julie,Archer Nicholas S,Koyama Sachiko,Deary Vincent,Roberts S Craig,Yanık Hüseyin,Albayrak Samet,Nováková Lenka Martinec,Croijmans Ilja,Mazal Patricia Portillo,Moein Shima T,Margulis Eitan,Mignot Coralie,Mariño Sajidxa,Georgiev Dejan,Kaushik Pavan K,Malnic Bettina,Wang Hong,Seyed-Allaei Shima,Yoluk Nur,Razzaghi-Asl Sara,Justice Jeb M,Restrepo Diego,Reed Danielle R30,Hummel Thomas80,Munger Steven D8182,Hayes John E6ORCID,

Affiliation:

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

Abstract

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.

Funder

Pennsylvania State University

Publisher

Oxford University Press (OUP)

Subject

Behavioral Neuroscience,Physiology (medical),Sensory Systems,Physiology

Reference83 articles.

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