Impact of variants of concern on SARS-CoV-2 viral dynamics in non-human primates
The impact of variants of concern (VoC) on SARS-CoV-2 viral dynamics remains poorly understood and essentially relies on observational studies subject to various sorts of biases. In contrast, experimental models of infection constitute a powerful model to perform controlled comparisons of the viral...
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| creator | Marc, Aurélien Marlin, Romain Donati, Flora Prague, Mélanie Kerioui, Marion Hérate, Cécile Alexandre, Marie Dereuddre-Bosquet, Nathalie Bertrand, Julie Contreras, Vanessa Behillil, Sylvie Maisonnasse, Pauline Van Der Werf, Sylvie Le Grand, Roger Guedj, Jérémie |
| description | The impact of variants of concern (VoC) on SARS-CoV-2 viral dynamics remains poorly understood and essentially relies on observational studies subject to various sorts of biases. In contrast, experimental models of infection constitute a powerful model to perform controlled comparisons of the viral dynamics observed with VoC and better quantify how VoC escape from the immune response. Here we used molecular and infectious viral load of 78 cynomolgus macaques to characterize in detail the effects of VoC on viral dynamics. We first developed a mathematical model that recapitulate the observed dynamics, and we found that the best model describing the data assumed a rapid antigen-dependent stimulation of the immune response leading to a rapid reduction of viral infectivity. When compared with the historical variant, all VoC except beta were associated with an escape from this immune response, and this effect was particularly sensitive for delta and omicron variant (p |
| doi_str_mv | 10.1371/journal.pcbi.1010721 |
| format | Article |
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In contrast, experimental models of infection constitute a powerful model to perform controlled comparisons of the viral dynamics observed with VoC and better quantify how VoC escape from the immune response. Here we used molecular and infectious viral load of 78 cynomolgus macaques to characterize in detail the effects of VoC on viral dynamics. We first developed a mathematical model that recapitulate the observed dynamics, and we found that the best model describing the data assumed a rapid antigen-dependent stimulation of the immune response leading to a rapid reduction of viral infectivity. When compared with the historical variant, all VoC except beta were associated with an escape from this immune response, and this effect was particularly sensitive for delta and omicron variant (p<10-6 for both). Interestingly, delta variant was associated with a 1.8-fold increased viral production rate (p = 0.046), while conversely omicron variant was associated with a 14-fold reduction in viral production rate (p<10-6). During a natural infection, our models predict that delta variant is associated with a higher peak viral RNA than omicron variant (7.6 log10 copies/mL 95% CI 6.8-8 for delta; 5.6 log10 copies/mL 95% CI 4.8-6.3 for omicron) while having similar peak infectious titers (3.7 log10 PFU/mL 95% CI 2.4-4.6 for delta; 2.8 log10 PFU/mL 95% CI 1.9-3.8 for omicron). These results provide a detailed picture of the effects of VoC on total and infectious viral load and may help understand some differences observed in the patterns of viral transmission of these viruses.</description><identifier>ISSN: 1553-7358</identifier><identifier>ISSN: 1553-734X</identifier><identifier>EISSN: 1553-7358</identifier><identifier>DOI: 10.1371/journal.pcbi.1010721</identifier><identifier>PMID: 37556476</identifier><language>eng</language><publisher>United States: Public Library of Science</publisher><subject>Analysis ; Animal models ; Animals ; Antigens ; Biodiversity ; Biology and Life Sciences ; Confidence intervals ; Dynamics ; Emerging diseases ; Health aspects ; Human health and pathology ; Immune response ; Immune system ; Immunology ; Infection ; Infections ; Infectious diseases ; Infectivity ; Innate immunity ; Life Sciences ; Mathematical models ; Medical research ; Medicine and Health Sciences ; Medicine, Experimental ; Microbiology and Parasitology ; Observational studies ; Populations and Evolution ; Primates ; Reduction ; Severe acute respiratory syndrome coronavirus 2 ; Vaccines ; Viral diseases ; Virology ; Viruses</subject><ispartof>PLoS computational biology, 2023-08, Vol.19 (8), p.e1010721-e1010721</ispartof><rights>Copyright: © 2023 Marc et al. This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.</rights><rights>COPYRIGHT 2023 Public Library of Science</rights><rights>2023 Marc et al. This is an open access article distributed under the terms of the Creative Commons Attribution License: http://creativecommons.org/licenses/by/4.0/ (the “License”), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. Notwithstanding the ProQuest Terms and Conditions, you may use this content in accordance with the terms of the License.</rights><rights>Attribution</rights><rights>2023 Marc et al 2023 Marc et al</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c696t-b03ab0a03455c17048f124438fb95dc1ff4f826464262f84042b2ac3edc369f63</citedby><cites>FETCH-LOGICAL-c696t-b03ab0a03455c17048f124438fb95dc1ff4f826464262f84042b2ac3edc369f63</cites><orcidid>0000-0002-3557-7075 ; 0000-0002-5534-5482 ; 0000-0001-8932-0171 ; 0000-0003-2862-9751 ; 0000-0002-6936-5388 ; 0000-0002-6568-1041 ; 0000-0001-9809-7848</orcidid></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC10441782/pdf/$$EPDF$$P50$$Gpubmedcentral$$Hfree_for_read</linktopdf><linktohtml>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC10441782/$$EHTML$$P50$$Gpubmedcentral$$Hfree_for_read</linktohtml><link.rule.ids>230,314,723,776,780,860,881,2096,2915,23845,27901,27902,53766,53768,79342,79343</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/37556476$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink><backlink>$$Uhttps://hal.science/hal-04225046$$DView record in HAL$$Hfree_for_read</backlink></links><search><creatorcontrib>Marc, Aurélien</creatorcontrib><creatorcontrib>Marlin, Romain</creatorcontrib><creatorcontrib>Donati, Flora</creatorcontrib><creatorcontrib>Prague, Mélanie</creatorcontrib><creatorcontrib>Kerioui, Marion</creatorcontrib><creatorcontrib>Hérate, Cécile</creatorcontrib><creatorcontrib>Alexandre, Marie</creatorcontrib><creatorcontrib>Dereuddre-Bosquet, Nathalie</creatorcontrib><creatorcontrib>Bertrand, Julie</creatorcontrib><creatorcontrib>Contreras, Vanessa</creatorcontrib><creatorcontrib>Behillil, Sylvie</creatorcontrib><creatorcontrib>Maisonnasse, Pauline</creatorcontrib><creatorcontrib>Van Der Werf, Sylvie</creatorcontrib><creatorcontrib>Le Grand, Roger</creatorcontrib><creatorcontrib>Guedj, Jérémie</creatorcontrib><title>Impact of variants of concern on SARS-CoV-2 viral dynamics in non-human primates</title><title>PLoS computational biology</title><addtitle>PLoS Comput Biol</addtitle><description>The impact of variants of concern (VoC) on SARS-CoV-2 viral dynamics remains poorly understood and essentially relies on observational studies subject to various sorts of biases. In contrast, experimental models of infection constitute a powerful model to perform controlled comparisons of the viral dynamics observed with VoC and better quantify how VoC escape from the immune response. Here we used molecular and infectious viral load of 78 cynomolgus macaques to characterize in detail the effects of VoC on viral dynamics. We first developed a mathematical model that recapitulate the observed dynamics, and we found that the best model describing the data assumed a rapid antigen-dependent stimulation of the immune response leading to a rapid reduction of viral infectivity. When compared with the historical variant, all VoC except beta were associated with an escape from this immune response, and this effect was particularly sensitive for delta and omicron variant (p<10-6 for both). Interestingly, delta variant was associated with a 1.8-fold increased viral production rate (p = 0.046), while conversely omicron variant was associated with a 14-fold reduction in viral production rate (p<10-6). During a natural infection, our models predict that delta variant is associated with a higher peak viral RNA than omicron variant (7.6 log10 copies/mL 95% CI 6.8-8 for delta; 5.6 log10 copies/mL 95% CI 4.8-6.3 for omicron) while having similar peak infectious titers (3.7 log10 PFU/mL 95% CI 2.4-4.6 for delta; 2.8 log10 PFU/mL 95% CI 1.9-3.8 for omicron). These results provide a detailed picture of the effects of VoC on total and infectious viral load and may help understand some differences observed in the patterns of viral transmission of these viruses.</description><subject>Analysis</subject><subject>Animal models</subject><subject>Animals</subject><subject>Antigens</subject><subject>Biodiversity</subject><subject>Biology and Life Sciences</subject><subject>Confidence intervals</subject><subject>Dynamics</subject><subject>Emerging diseases</subject><subject>Health aspects</subject><subject>Human health and pathology</subject><subject>Immune response</subject><subject>Immune system</subject><subject>Immunology</subject><subject>Infection</subject><subject>Infections</subject><subject>Infectious diseases</subject><subject>Infectivity</subject><subject>Innate immunity</subject><subject>Life Sciences</subject><subject>Mathematical models</subject><subject>Medical research</subject><subject>Medicine and Health 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dynamics remains poorly understood and essentially relies on observational studies subject to various sorts of biases. In contrast, experimental models of infection constitute a powerful model to perform controlled comparisons of the viral dynamics observed with VoC and better quantify how VoC escape from the immune response. Here we used molecular and infectious viral load of 78 cynomolgus macaques to characterize in detail the effects of VoC on viral dynamics. We first developed a mathematical model that recapitulate the observed dynamics, and we found that the best model describing the data assumed a rapid antigen-dependent stimulation of the immune response leading to a rapid reduction of viral infectivity. When compared with the historical variant, all VoC except beta were associated with an escape from this immune response, and this effect was particularly sensitive for delta and omicron variant (p<10-6 for both). Interestingly, delta variant was associated with a 1.8-fold increased viral production rate (p = 0.046), while conversely omicron variant was associated with a 14-fold reduction in viral production rate (p<10-6). During a natural infection, our models predict that delta variant is associated with a higher peak viral RNA than omicron variant (7.6 log10 copies/mL 95% CI 6.8-8 for delta; 5.6 log10 copies/mL 95% CI 4.8-6.3 for omicron) while having similar peak infectious titers (3.7 log10 PFU/mL 95% CI 2.4-4.6 for delta; 2.8 log10 PFU/mL 95% CI 1.9-3.8 for omicron). 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| source | DOAJ Directory of Open Access Journals; Elektronische Zeitschriftenbibliothek - Frei zugängliche E-Journals; PubMed Central; Public Library of Science (PLoS) |
| subjects | Analysis Animal models Animals Antigens Biodiversity Biology and Life Sciences Confidence intervals Dynamics Emerging diseases Health aspects Human health and pathology Immune response Immune system Immunology Infection Infections Infectious diseases Infectivity Innate immunity Life Sciences Mathematical models Medical research Medicine and Health Sciences Medicine, Experimental Microbiology and Parasitology Observational studies Populations and Evolution Primates Reduction Severe acute respiratory syndrome coronavirus 2 Vaccines Viral diseases Virology Viruses |
| title | Impact of variants of concern on SARS-CoV-2 viral dynamics in non-human primates |
| url | https://sfx.bib-bvb.de/sfx_tum?ctx_ver=Z39.88-2004&ctx_enc=info:ofi/enc:UTF-8&ctx_tim=2025-02-09T10%3A50%3A36IST&url_ver=Z39.88-2004&url_ctx_fmt=infofi/fmt:kev:mtx:ctx&rfr_id=info:sid/primo.exlibrisgroup.com:primo3-Article-gale_plos_&rft_val_fmt=info:ofi/fmt:kev:mtx:journal&rft.genre=article&rft.atitle=Impact%20of%20variants%20of%20concern%20on%20SARS-CoV-2%20viral%20dynamics%20in%20non-human%20primates&rft.jtitle=PLoS%20computational%20biology&rft.au=Marc,%20Aur%C3%A9lien&rft.date=2023-08-09&rft.volume=19&rft.issue=8&rft.spage=e1010721&rft.epage=e1010721&rft.pages=e1010721-e1010721&rft.issn=1553-7358&rft.eissn=1553-7358&rft_id=info:doi/10.1371/journal.pcbi.1010721&rft_dat=%3Cgale_plos_%3EA763760552%3C/gale_plos_%3E%3Curl%3E%3C/url%3E&disable_directlink=true&sfx.directlink=off&sfx.report_link=0&rft_id=info:oai/&rft_pqid=2865519845&rft_id=info:pmid/37556476&rft_galeid=A763760552&rft_doaj_id=oai_doaj_org_article_9cc6ae673b14459eb5cbc824b3092773&rfr_iscdi=true |