Daily longitudinal sampling of SARS-CoV-2 infection reveals substantial heterogeneity in infectiousness

Ruian Ke; Pamela P. Martinez; Rebecca L. Smith; Laura L. Gibson; Agha Mirza; Madison Conte; Nicholas Gallagher; Chun Huai Luo; Junko Jarrett; Ruifeng Zhou; Abigail Conte; Tongyu Liu; Mireille Farjo; Kimberly K.O. Walden; Gloria Rendon; Christopher J. Fields; Leyi Wang; Richard Fredrickson; Darci C. Edmonson; Melinda E. Baughman; Karen K. Chiu; Hannah Choi; Kevin R. Scardina; Shannon Bradley; Stacy L. Gloss; Crystal Reinhart; Jagadeesh Yedetore; Jessica Quicksall; Alyssa N. Owens; John Broach; Bruce Barton; Peter Lazar; William J. Heetderks; Matthew L. Robinson; Heba H. Mostafa; Yukari C. Manabe; Andrew Pekosz; David D. McManus; Christopher B. Brooke

doi:10.1038/s41564-022-01105-z

Daily longitudinal sampling of SARS-CoV-2 infection reveals substantial heterogeneity in infectiousness

Ruian Ke, Pamela P. Martinez, Rebecca L. Smith, Laura L. Gibson, Agha Mirza, Madison Conte, Nicholas Gallagher, Chun Huai Luo, Junko Jarrett, Ruifeng Zhou, Abigail Conte, Tongyu Liu, Mireille Farjo, Kimberly K.O. Walden, Gloria Rendon, Christopher J. Fields, Leyi Wang, Richard Fredrickson, Darci C. Edmonson, Melinda E. BaughmanKaren K. Chiu, Hannah Choi, Kevin R. Scardina, Shannon Bradley, Stacy L. Gloss, Crystal Reinhart, Jagadeesh Yedetore, Jessica Quicksall, Alyssa N. Owens, John Broach, Bruce Barton, Peter Lazar, William J. Heetderks, Matthew L. Robinson, Heba H. Mostafa, Yukari C. Manabe, Andrew Pekosz, David D. McManus, Christopher B. Brooke

Research output: Contribution to journal › Article › peer-review

Abstract

The dynamics of SARS-CoV-2 replication and shedding in humans remain poorly understood. We captured the dynamics of infectious virus and viral RNA shedding during acute infection through daily longitudinal sampling of 60 individuals for up to 14 days. By fitting mechanistic models, we directly estimated viral expansion and clearance rates and overall infectiousness for each individual. Significant person-to-person variation in infectious virus shedding suggests that individual-level heterogeneity in viral dynamics contributes to ‘superspreading’. Viral genome loads often peaked days earlier in saliva than in nasal swabs, indicating strong tissue compartmentalization and suggesting that saliva may serve as a superior sampling site for early detection of infection. Viral loads and clearance kinetics of Alpha (B.1.1.7) and previously circulating non-variant-of-concern viruses were mostly indistinguishable, indicating that the enhanced transmissibility of this variant cannot be explained simply by higher viral loads or delayed clearance. These results provide a high-resolution portrait of SARS-CoV-2 infection dynamics and implicate individual-level heterogeneity in infectiousness in superspreading.

Original language	English (US)
Pages (from-to)	640-652
Number of pages	13
Journal	Nature microbiology
Volume	7
Issue number	5
DOIs	https://doi.org/10.1038/s41564-022-01105-z
State	Published - May 2022

ASJC Scopus subject areas

Applied Microbiology and Biotechnology
Microbiology (medical)
Genetics
Cell Biology
Microbiology
Immunology

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10.1038/s41564-022-01105-z

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Ke, R., Martinez, P. P., Smith, R. L., Gibson, L. L., Mirza, A., Conte, M., Gallagher, N., Luo, C. H., Jarrett, J., Zhou, R., Conte, A., Liu, T., Farjo, M., Walden, K. K. O., Rendon, G., Fields, C. J., Wang, L., Fredrickson, R., Edmonson, D. C., ... Brooke, C. B. (2022). Daily longitudinal sampling of SARS-CoV-2 infection reveals substantial heterogeneity in infectiousness. Nature microbiology, 7(5), 640-652. https://doi.org/10.1038/s41564-022-01105-z

Ke, R, Martinez, PP, Smith, RL, Gibson, LL, Mirza, A, Conte, M, Gallagher, N, Luo, CH, Jarrett, J, Zhou, R, Conte, A, Liu, T, Farjo, M, Walden, KKO, Rendon, G, Fields, CJ, Wang, L, Fredrickson, R, Edmonson, DC, Baughman, ME, Chiu, KK, Choi, H, Scardina, KR, Bradley, S, Gloss, SL, Reinhart, C, Yedetore, J, Quicksall, J, Owens, AN, Broach, J, Barton, B, Lazar, P, Heetderks, WJ, Robinson, ML , Mostafa, HH , Manabe, YC , Pekosz, A, McManus, DD & Brooke, CB 2022, 'Daily longitudinal sampling of SARS-CoV-2 infection reveals substantial heterogeneity in infectiousness', Nature microbiology, vol. 7, no. 5, pp. 640-652. https://doi.org/10.1038/s41564-022-01105-z

@article{f738fb1ce17b4760b3122259aebdbdad,

title = "Daily longitudinal sampling of SARS-CoV-2 infection reveals substantial heterogeneity in infectiousness",

abstract = "The dynamics of SARS-CoV-2 replication and shedding in humans remain poorly understood. We captured the dynamics of infectious virus and viral RNA shedding during acute infection through daily longitudinal sampling of 60 individuals for up to 14 days. By fitting mechanistic models, we directly estimated viral expansion and clearance rates and overall infectiousness for each individual. Significant person-to-person variation in infectious virus shedding suggests that individual-level heterogeneity in viral dynamics contributes to {\textquoteleft}superspreading{\textquoteright}. Viral genome loads often peaked days earlier in saliva than in nasal swabs, indicating strong tissue compartmentalization and suggesting that saliva may serve as a superior sampling site for early detection of infection. Viral loads and clearance kinetics of Alpha (B.1.1.7) and previously circulating non-variant-of-concern viruses were mostly indistinguishable, indicating that the enhanced transmissibility of this variant cannot be explained simply by higher viral loads or delayed clearance. These results provide a high-resolution portrait of SARS-CoV-2 infection dynamics and implicate individual-level heterogeneity in infectiousness in superspreading.",

author = "Ruian Ke and Martinez, {Pamela P.} and Smith, {Rebecca L.} and Gibson, {Laura L.} and Agha Mirza and Madison Conte and Nicholas Gallagher and Luo, {Chun Huai} and Junko Jarrett and Ruifeng Zhou and Abigail Conte and Tongyu Liu and Mireille Farjo and Walden, {Kimberly K.O.} and Gloria Rendon and Fields, {Christopher J.} and Leyi Wang and Richard Fredrickson and Edmonson, {Darci C.} and Baughman, {Melinda E.} and Chiu, {Karen K.} and Hannah Choi and Scardina, {Kevin R.} and Shannon Bradley and Gloss, {Stacy L.} and Crystal Reinhart and Jagadeesh Yedetore and Jessica Quicksall and Owens, {Alyssa N.} and John Broach and Bruce Barton and Peter Lazar and Heetderks, {William J.} and Robinson, {Matthew L.} and Mostafa, {Heba H.} and Manabe, {Yukari C.} and Andrew Pekosz and McManus, {David D.} and Brooke, {Christopher B.}",

note = "Publisher Copyright: {\textcopyright} 2022, The Author(s), under exclusive licence to Springer Nature Limited.",

year = "2022",

month = may,

doi = "10.1038/s41564-022-01105-z",

language = "English (US)",

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AU - Ke, Ruian

AU - Martinez, Pamela P.

AU - Smith, Rebecca L.

AU - Gibson, Laura L.

AU - Mirza, Agha

AU - Conte, Madison

AU - Gallagher, Nicholas

AU - Luo, Chun Huai

AU - Jarrett, Junko

AU - Zhou, Ruifeng

AU - Conte, Abigail

AU - Liu, Tongyu

AU - Farjo, Mireille

AU - Walden, Kimberly K.O.

AU - Rendon, Gloria

AU - Fields, Christopher J.

AU - Wang, Leyi

AU - Fredrickson, Richard

AU - Edmonson, Darci C.

AU - Baughman, Melinda E.

AU - Chiu, Karen K.

AU - Choi, Hannah

AU - Scardina, Kevin R.

AU - Bradley, Shannon

AU - Gloss, Stacy L.

AU - Reinhart, Crystal

AU - Yedetore, Jagadeesh

AU - Quicksall, Jessica

AU - Owens, Alyssa N.

AU - Broach, John

AU - Barton, Bruce

AU - Lazar, Peter

AU - Heetderks, William J.

AU - Robinson, Matthew L.

AU - Mostafa, Heba H.

AU - Manabe, Yukari C.

AU - Pekosz, Andrew

AU - McManus, David D.

AU - Brooke, Christopher B.

PY - 2022/5

Y1 - 2022/5

N2 - The dynamics of SARS-CoV-2 replication and shedding in humans remain poorly understood. We captured the dynamics of infectious virus and viral RNA shedding during acute infection through daily longitudinal sampling of 60 individuals for up to 14 days. By fitting mechanistic models, we directly estimated viral expansion and clearance rates and overall infectiousness for each individual. Significant person-to-person variation in infectious virus shedding suggests that individual-level heterogeneity in viral dynamics contributes to ‘superspreading’. Viral genome loads often peaked days earlier in saliva than in nasal swabs, indicating strong tissue compartmentalization and suggesting that saliva may serve as a superior sampling site for early detection of infection. Viral loads and clearance kinetics of Alpha (B.1.1.7) and previously circulating non-variant-of-concern viruses were mostly indistinguishable, indicating that the enhanced transmissibility of this variant cannot be explained simply by higher viral loads or delayed clearance. These results provide a high-resolution portrait of SARS-CoV-2 infection dynamics and implicate individual-level heterogeneity in infectiousness in superspreading.

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EP - 652

JO - Nature microbiology

JF - Nature microbiology

IS - 5

ER -

Daily longitudinal sampling of SARS-CoV-2 infection reveals substantial heterogeneity in infectiousness

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