More Than Smell—COVID-19 Is Associated With Severe Impairment of Smell, Taste, and Chemesthesis
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 measur...
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Veröffentlicht in: | Chemical senses 2020-10, Vol.45 (7), p.609-622 |
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creator | Parma, Valentina Ohla, Kathrin Veldhuizen, Maria G Niv, Masha Y Kelly, Christine E Bakke, Alyssa J Cooper, Keiland W Bouysset, Cédric Pirastu, Nicola Dibattista, Michele Kaur, Rishemjit Liuzza, Marco Tullio Pepino, Marta Y Schöpf, Veronika Pereda-Loth, Veronica Olsson, Shannon B Gerkin, Richard C Rohlfs Domínguez, Paloma Albayay, Javier Farruggia, Michael C Bhutani, Surabhi Fjaeldstad, Alexander W Kumar, Ritesh Menini, Anna Bensafi, Moustafa Sandell, Mari Konstantinidis, Iordanis Di Pizio, Antonella Genovese, Federica Öztürk, Lina Thomas-Danguin, Thierry Frasnelli, Johannes Boesveldt, Sanne Saatci, Özlem Saraiva, Luis R Lin, Cailu Golebiowski, Jérôme Hwang, Liang-Dar Ozdener, Mehmet Hakan Guàrdia, Maria Dolors Laudamiel, Christophe Ritchie, Marina Havlícek, Jan Pierron, Denis Roura, Eugeni Navarro, Marta Nolden, Alissa A Lim, Juyun Whitcroft, Katherine L Colquitt, Lauren R Ferdenzi, Camille Brindha, Evelyn V Altundag, Aytug Macchi, Alberto Nunez-Parra, Alexia Patel, Zara M Fiorucci, Sébastien Philpott, Carl M Smith, Barry C Lundström, Johan N Mucignat, Carla Parker, Jane K van den Brink, Mirjam Schmuker, Michael Fischmeister, Florian Ph S Heinbockel, Thomas Shields, Vonnie D C Faraji, Farhoud Santamaría, Enrique Fredborg, William E A Morini, Gabriella Olofsson, Jonas K Jalessi, Maryam Karni, Noam D’Errico, Anna Alizadeh, Rafieh Pellegrino, Robert Meyer, Pablo Huart, Caroline Chen, Ben Soler, Graciela M Alwashahi, Mohammed K Welge-Lüssen, Antje Freiherr, Jessica de Groot, Jasper H B Klein, Hadar Okamoto, Masako Singh, Preet Bano Hsieh, Julien W Reed, Danielle R Hummel, Thomas Munger, Steven D Hayes, John E |
description | 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. |
doi_str_mv | 10.1093/chemse/bjaa041 |
format | Article |
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Ohla, Kathrin ; Veldhuizen, Maria G ; Niv, Masha Y ; Kelly, Christine E ; Bakke, Alyssa J ; Cooper, Keiland W ; Bouysset, Cédric ; Pirastu, Nicola ; Dibattista, Michele ; Kaur, Rishemjit ; Liuzza, Marco Tullio ; Pepino, Marta Y ; Schöpf, Veronika ; Pereda-Loth, Veronica ; Olsson, Shannon B ; Gerkin, Richard C ; Rohlfs Domínguez, Paloma ; Albayay, Javier ; Farruggia, Michael C ; Bhutani, Surabhi ; Fjaeldstad, Alexander W ; Kumar, Ritesh ; Menini, Anna ; Bensafi, Moustafa ; Sandell, Mari ; Konstantinidis, Iordanis ; Di Pizio, Antonella ; Genovese, Federica ; Öztürk, Lina ; Thomas-Danguin, Thierry ; Frasnelli, Johannes ; Boesveldt, Sanne ; Saatci, Özlem ; Saraiva, Luis R ; Lin, Cailu ; Golebiowski, Jérôme ; Hwang, Liang-Dar ; Ozdener, Mehmet Hakan ; Guàrdia, Maria Dolors ; Laudamiel, Christophe ; Ritchie, Marina ; Havlícek, Jan ; Pierron, Denis ; Roura, Eugeni ; Navarro, Marta ; Nolden, Alissa A ; Lim, Juyun ; Whitcroft, Katherine L ; Colquitt, Lauren R ; Ferdenzi, Camille ; Brindha, Evelyn V ; Altundag, Aytug ; Macchi, Alberto ; Nunez-Parra, Alexia ; Patel, Zara M ; Fiorucci, Sébastien ; Philpott, Carl M ; Smith, Barry C ; Lundström, Johan N ; Mucignat, Carla ; Parker, Jane K ; van den Brink, Mirjam ; Schmuker, Michael ; Fischmeister, Florian Ph S ; Heinbockel, Thomas ; Shields, Vonnie D C ; Faraji, Farhoud ; Santamaría, Enrique ; Fredborg, William E A ; Morini, Gabriella ; Olofsson, Jonas K ; Jalessi, Maryam ; Karni, Noam ; D’Errico, Anna ; Alizadeh, Rafieh ; Pellegrino, Robert ; Meyer, Pablo ; Huart, Caroline ; Chen, Ben ; Soler, Graciela M ; Alwashahi, Mohammed K ; Welge-Lüssen, Antje ; Freiherr, Jessica ; de Groot, Jasper H B ; Klein, Hadar ; Okamoto, Masako ; Singh, Preet Bano ; Hsieh, Julien W ; Reed, Danielle R ; Hummel, Thomas ; Munger, Steven D ; Hayes, John E</creator><creatorcontrib>Parma, Valentina ; Ohla, Kathrin ; Veldhuizen, Maria G ; Niv, Masha Y ; Kelly, Christine E ; Bakke, Alyssa J ; Cooper, Keiland W ; Bouysset, Cédric ; Pirastu, Nicola ; Dibattista, Michele ; Kaur, Rishemjit ; Liuzza, Marco Tullio ; Pepino, Marta Y ; Schöpf, Veronika ; Pereda-Loth, Veronica ; Olsson, Shannon B ; Gerkin, Richard C ; Rohlfs Domínguez, Paloma ; Albayay, Javier ; Farruggia, Michael C ; Bhutani, Surabhi ; Fjaeldstad, Alexander W ; Kumar, Ritesh ; Menini, Anna ; Bensafi, Moustafa ; Sandell, Mari ; Konstantinidis, Iordanis ; Di Pizio, Antonella ; Genovese, Federica ; Öztürk, Lina ; Thomas-Danguin, Thierry ; Frasnelli, Johannes ; Boesveldt, Sanne ; Saatci, Özlem ; Saraiva, Luis R ; Lin, Cailu ; Golebiowski, Jérôme ; Hwang, Liang-Dar ; Ozdener, Mehmet Hakan ; Guàrdia, Maria Dolors ; Laudamiel, Christophe ; Ritchie, Marina ; Havlícek, Jan ; Pierron, Denis ; Roura, Eugeni ; Navarro, Marta ; Nolden, Alissa A ; Lim, Juyun ; Whitcroft, Katherine L ; Colquitt, Lauren R ; Ferdenzi, Camille ; Brindha, Evelyn V ; Altundag, Aytug ; Macchi, Alberto ; Nunez-Parra, Alexia ; Patel, Zara M ; Fiorucci, Sébastien ; Philpott, Carl M ; Smith, Barry C ; Lundström, Johan N ; Mucignat, Carla ; Parker, Jane K ; van den Brink, Mirjam ; Schmuker, Michael ; Fischmeister, Florian Ph S ; Heinbockel, Thomas ; Shields, Vonnie D C ; Faraji, Farhoud ; Santamaría, Enrique ; Fredborg, William E A ; Morini, Gabriella ; Olofsson, Jonas K ; Jalessi, Maryam ; Karni, Noam ; D’Errico, Anna ; Alizadeh, Rafieh ; Pellegrino, Robert ; Meyer, Pablo ; Huart, Caroline ; Chen, Ben ; Soler, Graciela M ; Alwashahi, Mohammed K ; Welge-Lüssen, Antje ; Freiherr, Jessica ; de Groot, Jasper H B ; Klein, Hadar ; Okamoto, Masako ; Singh, Preet Bano ; Hsieh, Julien W ; Reed, Danielle R ; Hummel, Thomas ; Munger, Steven D ; Hayes, John E ; GCCR Group Author ; GCCR Group Author</creatorcontrib><description>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.</description><identifier>ISSN: 0379-864X</identifier><identifier>ISSN: 1464-3553</identifier><identifier>EISSN: 1464-3553</identifier><identifier>DOI: 10.1093/chemse/bjaa041</identifier><identifier>PMID: 32564071</identifier><language>eng</language><publisher>UK: Oxford University Press</publisher><subject>Adult ; Aged ; Betacoronavirus - isolation & purification ; Coronavirus Infections - complications ; Coronavirus Infections - diagnosis ; Coronavirus Infections - virology ; COVID-19 ; Female ; Food and Nutrition ; Food engineering ; head and neck surgery ; Humans ; Life Sciences ; Male ; Medicin och hälsovetenskap ; Middle Aged ; olfaction ; Olfaction Disorders - etiology ; Olfaction Disorders - virology ; Original ; Pandemics ; Pneumonia, Viral - complications ; Pneumonia, Viral - diagnosis ; Pneumonia, Viral - virology ; SARS-CoV-2 ; Self Report ; Smell ; somatosensation ; Somatosensory Disorders - etiology ; Somatosensory Disorders - virology ; Surveys and Questionnaires ; Taste ; Taste Disorders - etiology ; Taste Disorders - virology ; Young Adult</subject><ispartof>Chemical senses, 2020-10, Vol.45 (7), p.609-622</ispartof><rights>The Author(s) 2020. Published by Oxford University Press. All rights reserved. For permissions, please e-mail: journals.permissions@oup.com 2020</rights><rights>The Author(s) 2020. Published by Oxford University Press. All rights reserved. For permissions, please e-mail: journals.permissions@oup.com.</rights><rights>Attribution - NonCommercial - NoDerivatives</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c653t-4052f179c0765e55d9c66287ca25fdcaa07956f5390198655c2547170dac2ee53</citedby><cites>FETCH-LOGICAL-c653t-4052f179c0765e55d9c66287ca25fdcaa07956f5390198655c2547170dac2ee53</cites><orcidid>0000-0001-9065-6326 ; 0000-0002-1125-3236 ; 0000-0002-3529-8981 ; 0000-0002-2940-3378 ; 0000-0002-0856-0569 ; 0000-0001-8909-7758 ; 0000-0002-3132-9904 ; 0000-0002-8345-7633 ; 0000-0001-9052-4497 ; 0000-0003-4079-0396 ; 0000-0002-9135-6920 ; 0000-0001-7265-0449 ; 0000-0001-6708-1253 ; 0000-0002-1781-8912 ; 0000-0002-9073-9946 ; 0000-0001-5572-0361 ; 0000-0002-2991-3036 ; 0000-0003-0276-7072 ; 0000-0002-3675-1952 ; 0000-0003-2245-0478 ; 0000-0002-5306-6754 ; 0000-0002-9756-355X ; 0000-0002-4374-6107 ; 0000-0002-7814-8158 ; 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G</creatorcontrib><creatorcontrib>Niv, Masha Y</creatorcontrib><creatorcontrib>Kelly, Christine E</creatorcontrib><creatorcontrib>Bakke, Alyssa J</creatorcontrib><creatorcontrib>Cooper, Keiland W</creatorcontrib><creatorcontrib>Bouysset, Cédric</creatorcontrib><creatorcontrib>Pirastu, Nicola</creatorcontrib><creatorcontrib>Dibattista, Michele</creatorcontrib><creatorcontrib>Kaur, Rishemjit</creatorcontrib><creatorcontrib>Liuzza, Marco Tullio</creatorcontrib><creatorcontrib>Pepino, Marta Y</creatorcontrib><creatorcontrib>Schöpf, Veronika</creatorcontrib><creatorcontrib>Pereda-Loth, Veronica</creatorcontrib><creatorcontrib>Olsson, Shannon B</creatorcontrib><creatorcontrib>Gerkin, Richard C</creatorcontrib><creatorcontrib>Rohlfs Domínguez, Paloma</creatorcontrib><creatorcontrib>Albayay, Javier</creatorcontrib><creatorcontrib>Farruggia, Michael C</creatorcontrib><creatorcontrib>Bhutani, Surabhi</creatorcontrib><creatorcontrib>Fjaeldstad, Alexander W</creatorcontrib><creatorcontrib>Kumar, Ritesh</creatorcontrib><creatorcontrib>Menini, Anna</creatorcontrib><creatorcontrib>Bensafi, Moustafa</creatorcontrib><creatorcontrib>Sandell, Mari</creatorcontrib><creatorcontrib>Konstantinidis, Iordanis</creatorcontrib><creatorcontrib>Di Pizio, Antonella</creatorcontrib><creatorcontrib>Genovese, Federica</creatorcontrib><creatorcontrib>Öztürk, Lina</creatorcontrib><creatorcontrib>Thomas-Danguin, Thierry</creatorcontrib><creatorcontrib>Frasnelli, Johannes</creatorcontrib><creatorcontrib>Boesveldt, Sanne</creatorcontrib><creatorcontrib>Saatci, Özlem</creatorcontrib><creatorcontrib>Saraiva, Luis R</creatorcontrib><creatorcontrib>Lin, Cailu</creatorcontrib><creatorcontrib>Golebiowski, Jérôme</creatorcontrib><creatorcontrib>Hwang, Liang-Dar</creatorcontrib><creatorcontrib>Ozdener, Mehmet Hakan</creatorcontrib><creatorcontrib>Guàrdia, Maria Dolors</creatorcontrib><creatorcontrib>Laudamiel, Christophe</creatorcontrib><creatorcontrib>Ritchie, Marina</creatorcontrib><creatorcontrib>Havlícek, Jan</creatorcontrib><creatorcontrib>Pierron, Denis</creatorcontrib><creatorcontrib>Roura, Eugeni</creatorcontrib><creatorcontrib>Navarro, Marta</creatorcontrib><creatorcontrib>Nolden, Alissa A</creatorcontrib><creatorcontrib>Lim, Juyun</creatorcontrib><creatorcontrib>Whitcroft, Katherine L</creatorcontrib><creatorcontrib>Colquitt, Lauren R</creatorcontrib><creatorcontrib>Ferdenzi, Camille</creatorcontrib><creatorcontrib>Brindha, Evelyn V</creatorcontrib><creatorcontrib>Altundag, Aytug</creatorcontrib><creatorcontrib>Macchi, Alberto</creatorcontrib><creatorcontrib>Nunez-Parra, Alexia</creatorcontrib><creatorcontrib>Patel, Zara M</creatorcontrib><creatorcontrib>Fiorucci, Sébastien</creatorcontrib><creatorcontrib>Philpott, Carl M</creatorcontrib><creatorcontrib>Smith, Barry C</creatorcontrib><creatorcontrib>Lundström, Johan N</creatorcontrib><creatorcontrib>Mucignat, Carla</creatorcontrib><creatorcontrib>Parker, Jane K</creatorcontrib><creatorcontrib>van den Brink, Mirjam</creatorcontrib><creatorcontrib>Schmuker, Michael</creatorcontrib><creatorcontrib>Fischmeister, Florian Ph S</creatorcontrib><creatorcontrib>Heinbockel, Thomas</creatorcontrib><creatorcontrib>Shields, Vonnie D C</creatorcontrib><creatorcontrib>Faraji, Farhoud</creatorcontrib><creatorcontrib>Santamaría, Enrique</creatorcontrib><creatorcontrib>Fredborg, William E A</creatorcontrib><creatorcontrib>Morini, Gabriella</creatorcontrib><creatorcontrib>Olofsson, Jonas K</creatorcontrib><creatorcontrib>Jalessi, Maryam</creatorcontrib><creatorcontrib>Karni, Noam</creatorcontrib><creatorcontrib>D’Errico, Anna</creatorcontrib><creatorcontrib>Alizadeh, Rafieh</creatorcontrib><creatorcontrib>Pellegrino, Robert</creatorcontrib><creatorcontrib>Meyer, Pablo</creatorcontrib><creatorcontrib>Huart, Caroline</creatorcontrib><creatorcontrib>Chen, Ben</creatorcontrib><creatorcontrib>Soler, Graciela M</creatorcontrib><creatorcontrib>Alwashahi, Mohammed K</creatorcontrib><creatorcontrib>Welge-Lüssen, Antje</creatorcontrib><creatorcontrib>Freiherr, Jessica</creatorcontrib><creatorcontrib>de Groot, Jasper H B</creatorcontrib><creatorcontrib>Klein, Hadar</creatorcontrib><creatorcontrib>Okamoto, Masako</creatorcontrib><creatorcontrib>Singh, Preet Bano</creatorcontrib><creatorcontrib>Hsieh, Julien W</creatorcontrib><creatorcontrib>Reed, Danielle R</creatorcontrib><creatorcontrib>Hummel, Thomas</creatorcontrib><creatorcontrib>Munger, Steven D</creatorcontrib><creatorcontrib>Hayes, John E</creatorcontrib><creatorcontrib>GCCR Group Author</creatorcontrib><creatorcontrib>GCCR Group Author</creatorcontrib><title>More Than Smell—COVID-19 Is Associated With Severe Impairment of Smell, Taste, and Chemesthesis</title><title>Chemical senses</title><addtitle>Chem Senses</addtitle><description>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.</description><subject>Adult</subject><subject>Aged</subject><subject>Betacoronavirus - isolation & purification</subject><subject>Coronavirus Infections - complications</subject><subject>Coronavirus Infections - diagnosis</subject><subject>Coronavirus Infections - virology</subject><subject>COVID-19</subject><subject>Female</subject><subject>Food and Nutrition</subject><subject>Food engineering</subject><subject>head and neck surgery</subject><subject>Humans</subject><subject>Life Sciences</subject><subject>Male</subject><subject>Medicin och hälsovetenskap</subject><subject>Middle Aged</subject><subject>olfaction</subject><subject>Olfaction Disorders - etiology</subject><subject>Olfaction Disorders - virology</subject><subject>Original</subject><subject>Pandemics</subject><subject>Pneumonia, Viral - complications</subject><subject>Pneumonia, Viral - diagnosis</subject><subject>Pneumonia, Viral - virology</subject><subject>SARS-CoV-2</subject><subject>Self Report</subject><subject>Smell</subject><subject>somatosensation</subject><subject>Somatosensory Disorders - etiology</subject><subject>Somatosensory Disorders - virology</subject><subject>Surveys and Questionnaires</subject><subject>Taste</subject><subject>Taste Disorders - etiology</subject><subject>Taste Disorders - virology</subject><subject>Young Adult</subject><issn>0379-864X</issn><issn>1464-3553</issn><issn>1464-3553</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2020</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><sourceid>D8T</sourceid><recordid>eNqFks9u1DAQxi0EokvhyhHlCNKm9X_HF6TVFuhKi3roUrhZrjNpUjbxYieLuPEQPCFPglfZthSp4mRr_Pu-mfEMQi8JPiJYs2NXQxvh-PLaWszJIzQhXPKcCcEeowlmSueF5F8O0LMYrzEmnNHiKTpgVEiOFZkg-9EHyFa17bLzFtbr3z9_zc8uFic50dkiZrMYvWtsD2X2uenr7By2kPhFu7FNaKHrM1-Nwmm2srGHaWa7MpunqiD2NcQmPkdPKruO8GJ_HqJP79-t5qf58uzDYj5b5k4K1uccC1oRpR1WUoAQpXZS0kI5S0VVutSe0kJWgmlMdCGFcFRwRRQuraMAgh2ifPSN32EzXJpNaFobfhhvG7MPfU03MFxhxnHi9YP8JvjyTnQjJFwQrQq9004f1J40FzPjw5WJgyGFppIm_O2IJ7aF0qV_C3Z9P-O9l66pzZXfGsWYkpIngzejQf2P7HS2NLsYppoQzPCWJPb1Plnw34Y0BdM20aUJ2Q78EA3lRBSMU6ETejSiLvgYA1S33gSb3XqZcb3Mfr2S4NXfjdziN_t0V6gfNv8z-wOFSNxB</recordid><startdate>20201009</startdate><enddate>20201009</enddate><creator>Parma, Valentina</creator><creator>Ohla, Kathrin</creator><creator>Veldhuizen, Maria G</creator><creator>Niv, Masha Y</creator><creator>Kelly, Christine E</creator><creator>Bakke, Alyssa J</creator><creator>Cooper, Keiland W</creator><creator>Bouysset, Cédric</creator><creator>Pirastu, Nicola</creator><creator>Dibattista, Michele</creator><creator>Kaur, Rishemjit</creator><creator>Liuzza, Marco Tullio</creator><creator>Pepino, Marta Y</creator><creator>Schöpf, Veronika</creator><creator>Pereda-Loth, Veronica</creator><creator>Olsson, Shannon B</creator><creator>Gerkin, Richard C</creator><creator>Rohlfs Domínguez, Paloma</creator><creator>Albayay, Javier</creator><creator>Farruggia, Michael C</creator><creator>Bhutani, Surabhi</creator><creator>Fjaeldstad, Alexander W</creator><creator>Kumar, Ritesh</creator><creator>Menini, Anna</creator><creator>Bensafi, Moustafa</creator><creator>Sandell, Mari</creator><creator>Konstantinidis, Iordanis</creator><creator>Di Pizio, Antonella</creator><creator>Genovese, Federica</creator><creator>Öztürk, Lina</creator><creator>Thomas-Danguin, Thierry</creator><creator>Frasnelli, Johannes</creator><creator>Boesveldt, Sanne</creator><creator>Saatci, Özlem</creator><creator>Saraiva, Luis R</creator><creator>Lin, Cailu</creator><creator>Golebiowski, Jérôme</creator><creator>Hwang, Liang-Dar</creator><creator>Ozdener, Mehmet Hakan</creator><creator>Guàrdia, Maria Dolors</creator><creator>Laudamiel, Christophe</creator><creator>Ritchie, Marina</creator><creator>Havlícek, Jan</creator><creator>Pierron, Denis</creator><creator>Roura, Eugeni</creator><creator>Navarro, Marta</creator><creator>Nolden, Alissa A</creator><creator>Lim, Juyun</creator><creator>Whitcroft, Katherine L</creator><creator>Colquitt, Lauren R</creator><creator>Ferdenzi, Camille</creator><creator>Brindha, Evelyn V</creator><creator>Altundag, Aytug</creator><creator>Macchi, Alberto</creator><creator>Nunez-Parra, Alexia</creator><creator>Patel, Zara M</creator><creator>Fiorucci, Sébastien</creator><creator>Philpott, Carl M</creator><creator>Smith, Barry C</creator><creator>Lundström, Johan N</creator><creator>Mucignat, Carla</creator><creator>Parker, Jane K</creator><creator>van den Brink, Mirjam</creator><creator>Schmuker, Michael</creator><creator>Fischmeister, Florian Ph S</creator><creator>Heinbockel, Thomas</creator><creator>Shields, Vonnie D C</creator><creator>Faraji, Farhoud</creator><creator>Santamaría, Enrique</creator><creator>Fredborg, William E A</creator><creator>Morini, Gabriella</creator><creator>Olofsson, Jonas K</creator><creator>Jalessi, Maryam</creator><creator>Karni, Noam</creator><creator>D’Errico, Anna</creator><creator>Alizadeh, Rafieh</creator><creator>Pellegrino, Robert</creator><creator>Meyer, Pablo</creator><creator>Huart, Caroline</creator><creator>Chen, Ben</creator><creator>Soler, Graciela M</creator><creator>Alwashahi, Mohammed K</creator><creator>Welge-Lüssen, Antje</creator><creator>Freiherr, Jessica</creator><creator>de Groot, Jasper H B</creator><creator>Klein, Hadar</creator><creator>Okamoto, Masako</creator><creator>Singh, Preet Bano</creator><creator>Hsieh, Julien W</creator><creator>Reed, Danielle R</creator><creator>Hummel, Thomas</creator><creator>Munger, Steven D</creator><creator>Hayes, John E</creator><general>Oxford University Press</general><general>Oxford University Press (OUP)</general><scope>CGR</scope><scope>CUY</scope><scope>CVF</scope><scope>ECM</scope><scope>EIF</scope><scope>NPM</scope><scope>AAYXX</scope><scope>CITATION</scope><scope>7X8</scope><scope>1XC</scope><scope>VOOES</scope><scope>5PM</scope><scope>ABAVF</scope><scope>ADTPV</scope><scope>AOWAS</scope><scope>D8T</scope><scope>DG7</scope><scope>ZZAVC</scope><orcidid>https://orcid.org/0000-0001-9065-6326</orcidid><orcidid>https://orcid.org/0000-0002-1125-3236</orcidid><orcidid>https://orcid.org/0000-0002-3529-8981</orcidid><orcidid>https://orcid.org/0000-0002-2940-3378</orcidid><orcidid>https://orcid.org/0000-0002-0856-0569</orcidid><orcidid>https://orcid.org/0000-0001-8909-7758</orcidid><orcidid>https://orcid.org/0000-0002-3132-9904</orcidid><orcidid>https://orcid.org/0000-0002-8345-7633</orcidid><orcidid>https://orcid.org/0000-0001-9052-4497</orcidid><orcidid>https://orcid.org/0000-0003-4079-0396</orcidid><orcidid>https://orcid.org/0000-0002-9135-6920</orcidid><orcidid>https://orcid.org/0000-0001-7265-0449</orcidid><orcidid>https://orcid.org/0000-0001-6708-1253</orcidid><orcidid>https://orcid.org/0000-0002-1781-8912</orcidid><orcidid>https://orcid.org/0000-0002-9073-9946</orcidid><orcidid>https://orcid.org/0000-0001-5572-0361</orcidid><orcidid>https://orcid.org/0000-0002-2991-3036</orcidid><orcidid>https://orcid.org/0000-0003-0276-7072</orcidid><orcidid>https://orcid.org/0000-0002-3675-1952</orcidid><orcidid>https://orcid.org/0000-0003-2245-0478</orcidid><orcidid>https://orcid.org/0000-0002-5306-6754</orcidid><orcidid>https://orcid.org/0000-0002-9756-355X</orcidid><orcidid>https://orcid.org/0000-0002-4374-6107</orcidid><orcidid>https://orcid.org/0000-0002-7814-8158</orcidid><orcidid>https://orcid.org/0000-0002-0358-9645</orcidid><orcidid>https://orcid.org/0000-0003-1383-6774</orcidid><orcidid>https://orcid.org/0000-0002-7365-6217</orcidid><orcidid>https://orcid.org/0000-0001-9713-0183</orcidid><orcidid>https://orcid.org/0000-0002-1685-2000</orcidid></search><sort><creationdate>20201009</creationdate><title>More Than Smell—COVID-19 Is Associated With Severe Impairment of Smell, Taste, and Chemesthesis</title><author>Parma, Valentina ; Ohla, Kathrin ; Veldhuizen, Maria G ; Niv, Masha Y ; Kelly, Christine E ; Bakke, Alyssa J ; Cooper, Keiland W ; Bouysset, Cédric ; Pirastu, Nicola ; Dibattista, Michele ; Kaur, Rishemjit ; Liuzza, Marco Tullio ; Pepino, Marta Y ; Schöpf, Veronika ; Pereda-Loth, Veronica ; Olsson, Shannon B ; Gerkin, Richard C ; Rohlfs Domínguez, Paloma ; Albayay, Javier ; Farruggia, Michael C ; Bhutani, Surabhi ; Fjaeldstad, Alexander W ; Kumar, Ritesh ; Menini, Anna ; Bensafi, Moustafa ; Sandell, Mari ; Konstantinidis, Iordanis ; Di Pizio, Antonella ; Genovese, Federica ; Öztürk, Lina ; Thomas-Danguin, Thierry ; Frasnelli, Johannes ; Boesveldt, Sanne ; Saatci, Özlem ; Saraiva, Luis R ; Lin, Cailu ; Golebiowski, Jérôme ; Hwang, Liang-Dar ; Ozdener, Mehmet Hakan ; Guàrdia, Maria Dolors ; Laudamiel, Christophe ; Ritchie, Marina ; Havlícek, Jan ; Pierron, Denis ; Roura, Eugeni ; Navarro, Marta ; Nolden, Alissa A ; Lim, Juyun ; Whitcroft, Katherine L ; Colquitt, Lauren R ; Ferdenzi, Camille ; Brindha, Evelyn V ; Altundag, Aytug ; Macchi, Alberto ; Nunez-Parra, Alexia ; Patel, Zara M ; Fiorucci, Sébastien ; Philpott, Carl M ; Smith, Barry C ; Lundström, Johan N ; Mucignat, Carla ; Parker, Jane K ; van den Brink, Mirjam ; Schmuker, Michael ; Fischmeister, Florian Ph S ; Heinbockel, Thomas ; Shields, Vonnie D C ; Faraji, Farhoud ; Santamaría, Enrique ; Fredborg, William E A ; Morini, Gabriella ; Olofsson, Jonas K ; Jalessi, Maryam ; Karni, Noam ; D’Errico, Anna ; Alizadeh, Rafieh ; Pellegrino, Robert ; Meyer, Pablo ; Huart, Caroline ; Chen, Ben ; Soler, Graciela M ; Alwashahi, Mohammed K ; Welge-Lüssen, Antje ; Freiherr, Jessica ; de Groot, Jasper H B ; Klein, Hadar ; Okamoto, Masako ; Singh, Preet Bano ; Hsieh, Julien W ; Reed, Danielle R ; Hummel, Thomas ; Munger, Steven D ; Hayes, John E</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c653t-4052f179c0765e55d9c66287ca25fdcaa07956f5390198655c2547170dac2ee53</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2020</creationdate><topic>Adult</topic><topic>Aged</topic><topic>Betacoronavirus - isolation & purification</topic><topic>Coronavirus Infections - complications</topic><topic>Coronavirus Infections - diagnosis</topic><topic>Coronavirus Infections - virology</topic><topic>COVID-19</topic><topic>Female</topic><topic>Food and Nutrition</topic><topic>Food engineering</topic><topic>head and neck surgery</topic><topic>Humans</topic><topic>Life Sciences</topic><topic>Male</topic><topic>Medicin och hälsovetenskap</topic><topic>Middle Aged</topic><topic>olfaction</topic><topic>Olfaction Disorders - etiology</topic><topic>Olfaction Disorders - virology</topic><topic>Original</topic><topic>Pandemics</topic><topic>Pneumonia, Viral - complications</topic><topic>Pneumonia, Viral - diagnosis</topic><topic>Pneumonia, Viral - virology</topic><topic>SARS-CoV-2</topic><topic>Self Report</topic><topic>Smell</topic><topic>somatosensation</topic><topic>Somatosensory Disorders - etiology</topic><topic>Somatosensory Disorders - virology</topic><topic>Surveys and Questionnaires</topic><topic>Taste</topic><topic>Taste Disorders - etiology</topic><topic>Taste Disorders - virology</topic><topic>Young Adult</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Parma, Valentina</creatorcontrib><creatorcontrib>Ohla, Kathrin</creatorcontrib><creatorcontrib>Veldhuizen, Maria G</creatorcontrib><creatorcontrib>Niv, Masha Y</creatorcontrib><creatorcontrib>Kelly, Christine E</creatorcontrib><creatorcontrib>Bakke, Alyssa J</creatorcontrib><creatorcontrib>Cooper, Keiland W</creatorcontrib><creatorcontrib>Bouysset, Cédric</creatorcontrib><creatorcontrib>Pirastu, 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C</creatorcontrib><creatorcontrib>Faraji, Farhoud</creatorcontrib><creatorcontrib>Santamaría, Enrique</creatorcontrib><creatorcontrib>Fredborg, William E A</creatorcontrib><creatorcontrib>Morini, Gabriella</creatorcontrib><creatorcontrib>Olofsson, Jonas K</creatorcontrib><creatorcontrib>Jalessi, Maryam</creatorcontrib><creatorcontrib>Karni, Noam</creatorcontrib><creatorcontrib>D’Errico, Anna</creatorcontrib><creatorcontrib>Alizadeh, Rafieh</creatorcontrib><creatorcontrib>Pellegrino, Robert</creatorcontrib><creatorcontrib>Meyer, Pablo</creatorcontrib><creatorcontrib>Huart, Caroline</creatorcontrib><creatorcontrib>Chen, Ben</creatorcontrib><creatorcontrib>Soler, Graciela M</creatorcontrib><creatorcontrib>Alwashahi, Mohammed K</creatorcontrib><creatorcontrib>Welge-Lüssen, Antje</creatorcontrib><creatorcontrib>Freiherr, Jessica</creatorcontrib><creatorcontrib>de Groot, Jasper H B</creatorcontrib><creatorcontrib>Klein, Hadar</creatorcontrib><creatorcontrib>Okamoto, Masako</creatorcontrib><creatorcontrib>Singh, Preet Bano</creatorcontrib><creatorcontrib>Hsieh, Julien W</creatorcontrib><creatorcontrib>Reed, Danielle R</creatorcontrib><creatorcontrib>Hummel, Thomas</creatorcontrib><creatorcontrib>Munger, Steven D</creatorcontrib><creatorcontrib>Hayes, John E</creatorcontrib><creatorcontrib>GCCR Group Author</creatorcontrib><creatorcontrib>GCCR Group Author</creatorcontrib><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>MEDLINE - Academic</collection><collection>Hyper Article en Ligne (HAL)</collection><collection>Hyper Article en Ligne (HAL) (Open Access)</collection><collection>PubMed Central (Full Participant titles)</collection><collection>SWEPUB Stockholms universitet full text</collection><collection>SwePub</collection><collection>SwePub Articles</collection><collection>SWEPUB Freely available online</collection><collection>SWEPUB Stockholms universitet</collection><collection>SwePub Articles full text</collection><jtitle>Chemical senses</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Parma, Valentina</au><au>Ohla, Kathrin</au><au>Veldhuizen, Maria G</au><au>Niv, Masha Y</au><au>Kelly, Christine E</au><au>Bakke, Alyssa J</au><au>Cooper, Keiland W</au><au>Bouysset, Cédric</au><au>Pirastu, Nicola</au><au>Dibattista, Michele</au><au>Kaur, Rishemjit</au><au>Liuzza, Marco Tullio</au><au>Pepino, Marta Y</au><au>Schöpf, Veronika</au><au>Pereda-Loth, Veronica</au><au>Olsson, Shannon B</au><au>Gerkin, Richard C</au><au>Rohlfs Domínguez, Paloma</au><au>Albayay, Javier</au><au>Farruggia, Michael C</au><au>Bhutani, Surabhi</au><au>Fjaeldstad, Alexander W</au><au>Kumar, Ritesh</au><au>Menini, Anna</au><au>Bensafi, Moustafa</au><au>Sandell, Mari</au><au>Konstantinidis, Iordanis</au><au>Di Pizio, Antonella</au><au>Genovese, Federica</au><au>Öztürk, Lina</au><au>Thomas-Danguin, Thierry</au><au>Frasnelli, Johannes</au><au>Boesveldt, Sanne</au><au>Saatci, Özlem</au><au>Saraiva, Luis R</au><au>Lin, Cailu</au><au>Golebiowski, Jérôme</au><au>Hwang, Liang-Dar</au><au>Ozdener, Mehmet Hakan</au><au>Guàrdia, Maria Dolors</au><au>Laudamiel, Christophe</au><au>Ritchie, Marina</au><au>Havlícek, Jan</au><au>Pierron, Denis</au><au>Roura, Eugeni</au><au>Navarro, Marta</au><au>Nolden, Alissa A</au><au>Lim, Juyun</au><au>Whitcroft, Katherine L</au><au>Colquitt, Lauren R</au><au>Ferdenzi, Camille</au><au>Brindha, Evelyn V</au><au>Altundag, Aytug</au><au>Macchi, Alberto</au><au>Nunez-Parra, Alexia</au><au>Patel, Zara M</au><au>Fiorucci, Sébastien</au><au>Philpott, Carl M</au><au>Smith, Barry C</au><au>Lundström, Johan N</au><au>Mucignat, Carla</au><au>Parker, Jane K</au><au>van den Brink, Mirjam</au><au>Schmuker, Michael</au><au>Fischmeister, Florian Ph S</au><au>Heinbockel, Thomas</au><au>Shields, Vonnie D C</au><au>Faraji, Farhoud</au><au>Santamaría, Enrique</au><au>Fredborg, William E A</au><au>Morini, Gabriella</au><au>Olofsson, Jonas K</au><au>Jalessi, Maryam</au><au>Karni, Noam</au><au>D’Errico, Anna</au><au>Alizadeh, Rafieh</au><au>Pellegrino, Robert</au><au>Meyer, Pablo</au><au>Huart, Caroline</au><au>Chen, Ben</au><au>Soler, Graciela M</au><au>Alwashahi, Mohammed K</au><au>Welge-Lüssen, Antje</au><au>Freiherr, Jessica</au><au>de Groot, Jasper H B</au><au>Klein, Hadar</au><au>Okamoto, Masako</au><au>Singh, Preet Bano</au><au>Hsieh, Julien W</au><au>Reed, Danielle R</au><au>Hummel, Thomas</au><au>Munger, Steven D</au><au>Hayes, John E</au><aucorp>GCCR Group Author</aucorp><aucorp>GCCR Group Author</aucorp><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>More Than Smell—COVID-19 Is Associated With Severe Impairment of Smell, Taste, and Chemesthesis</atitle><jtitle>Chemical senses</jtitle><addtitle>Chem Senses</addtitle><date>2020-10-09</date><risdate>2020</risdate><volume>45</volume><issue>7</issue><spage>609</spage><epage>622</epage><pages>609-622</pages><issn>0379-864X</issn><issn>1464-3553</issn><eissn>1464-3553</eissn><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.</abstract><cop>UK</cop><pub>Oxford University Press</pub><pmid>32564071</pmid><doi>10.1093/chemse/bjaa041</doi><tpages>14</tpages><orcidid>https://orcid.org/0000-0001-9065-6326</orcidid><orcidid>https://orcid.org/0000-0002-1125-3236</orcidid><orcidid>https://orcid.org/0000-0002-3529-8981</orcidid><orcidid>https://orcid.org/0000-0002-2940-3378</orcidid><orcidid>https://orcid.org/0000-0002-0856-0569</orcidid><orcidid>https://orcid.org/0000-0001-8909-7758</orcidid><orcidid>https://orcid.org/0000-0002-3132-9904</orcidid><orcidid>https://orcid.org/0000-0002-8345-7633</orcidid><orcidid>https://orcid.org/0000-0001-9052-4497</orcidid><orcidid>https://orcid.org/0000-0003-4079-0396</orcidid><orcidid>https://orcid.org/0000-0002-9135-6920</orcidid><orcidid>https://orcid.org/0000-0001-7265-0449</orcidid><orcidid>https://orcid.org/0000-0001-6708-1253</orcidid><orcidid>https://orcid.org/0000-0002-1781-8912</orcidid><orcidid>https://orcid.org/0000-0002-9073-9946</orcidid><orcidid>https://orcid.org/0000-0001-5572-0361</orcidid><orcidid>https://orcid.org/0000-0002-2991-3036</orcidid><orcidid>https://orcid.org/0000-0003-0276-7072</orcidid><orcidid>https://orcid.org/0000-0002-3675-1952</orcidid><orcidid>https://orcid.org/0000-0003-2245-0478</orcidid><orcidid>https://orcid.org/0000-0002-5306-6754</orcidid><orcidid>https://orcid.org/0000-0002-9756-355X</orcidid><orcidid>https://orcid.org/0000-0002-4374-6107</orcidid><orcidid>https://orcid.org/0000-0002-7814-8158</orcidid><orcidid>https://orcid.org/0000-0002-0358-9645</orcidid><orcidid>https://orcid.org/0000-0003-1383-6774</orcidid><orcidid>https://orcid.org/0000-0002-7365-6217</orcidid><orcidid>https://orcid.org/0000-0001-9713-0183</orcidid><orcidid>https://orcid.org/0000-0002-1685-2000</orcidid><oa>free_for_read</oa></addata></record> |
fulltext | fulltext |
identifier | ISSN: 0379-864X |
ispartof | Chemical senses, 2020-10, Vol.45 (7), p.609-622 |
issn | 0379-864X 1464-3553 1464-3553 |
language | eng |
recordid | cdi_swepub_primary_oai_swepub_ki_se_470340 |
source | MEDLINE; SWEPUB Freely available online; Oxford University Press Journals All Titles (1996-Current); EZB-FREE-00999 freely available EZB journals; Alma/SFX Local Collection; Free Full-Text Journals in Chemistry |
subjects | Adult Aged Betacoronavirus - isolation & purification Coronavirus Infections - complications Coronavirus Infections - diagnosis Coronavirus Infections - virology COVID-19 Female Food and Nutrition Food engineering head and neck surgery Humans Life Sciences Male Medicin och hälsovetenskap Middle Aged olfaction Olfaction Disorders - etiology Olfaction Disorders - virology Original Pandemics Pneumonia, Viral - complications Pneumonia, Viral - diagnosis Pneumonia, Viral - virology SARS-CoV-2 Self Report Smell somatosensation Somatosensory Disorders - etiology Somatosensory Disorders - virology Surveys and Questionnaires Taste Taste Disorders - etiology Taste Disorders - virology Young Adult |
title | More Than Smell—COVID-19 Is Associated With Severe Impairment of Smell, Taste, and Chemesthesis |
url | https://sfx.bib-bvb.de/sfx_tum?ctx_ver=Z39.88-2004&ctx_enc=info:ofi/enc:UTF-8&ctx_tim=2024-12-24T21%3A27%3A05IST&url_ver=Z39.88-2004&url_ctx_fmt=infofi/fmt:kev:mtx:ctx&rfr_id=info:sid/primo.exlibrisgroup.com:primo3-Article-proquest_swepu&rft_val_fmt=info:ofi/fmt:kev:mtx:journal&rft.genre=article&rft.atitle=More%20Than%20Smell%E2%80%94COVID-19%20Is%20Associated%20With%20Severe%20Impairment%20of%20Smell,%20Taste,%20and%20Chemesthesis&rft.jtitle=Chemical%20senses&rft.au=Parma,%20Valentina&rft.aucorp=GCCR%20Group%20Author&rft.date=2020-10-09&rft.volume=45&rft.issue=7&rft.spage=609&rft.epage=622&rft.pages=609-622&rft.issn=0379-864X&rft.eissn=1464-3553&rft_id=info:doi/10.1093/chemse/bjaa041&rft_dat=%3Cproquest_swepu%3E2415834259%3C/proquest_swepu%3E%3Curl%3E%3C/url%3E&disable_directlink=true&sfx.directlink=off&sfx.report_link=0&rft_id=info:oai/&rft_pqid=2415834259&rft_id=info:pmid/32564071&rft_oup_id=10.1093/chemse/bjaa041&rfr_iscdi=true |