Effectiveness of rapid SARS-CoV-2 genome sequencing in supporting infection control for hospital-onset COVID-19 infection: multicenter, prospective study

Oliver Stirrup; James Blackstone; Fiona Mapp; Alyson MacNeil; Monica Panca; Alison Holmes; Nicholas Machin; Gee Yen Shin; Tabitha Mahungu; Kordo Saeed; Tranprit Saluja; Yusri Taha; Nikunj Mahida; Cassie Pope; Anu Chawla; Maria-Teresa Cutino-Moguel; Asif Tamuri; Rachel Williams; Alistair Darby; David L Robertson; Flavia Flaviani; Eleni Nastouli; Samuel Robson; Darren Smith; Kenneth Laing; Irene Monahan; Beatrix Kele; Sam Haldenby; Ryan George; Matthew Bashton; Adam A Witney; Matthew Byott; Francesc Coll; Michael Chapman; Sharon J Peacock; Joseph Hughes; Gaia Nebbia; David G Partridge; Matthew Parker; James Richard Price; Christine Peters; Sunando Roy; Luke B Snell; Thushan I de Silva; Emma Thomson; Paul Flowers; Andrew Copas; Judith Breuer

doi:10.7554/elife.78427

Effectiveness of rapid SARS-CoV-2 genome sequencing in supporting infection control for hospital-onset COVID-19 infection: multicenter, prospective study

Oliver Stirrup, James Blackstone, Fiona Mapp, Alyson MacNeil, Monica Panca, Alison Holmes, Nicholas Machin, Gee Yen Shin, Tabitha Mahungu, Kordo Saeed, Tranprit Saluja, Yusri Taha, Nikunj Mahida, Cassie Pope, Anu Chawla, Maria-Teresa Cutino-Moguel, Asif Tamuri, Rachel Williams, Alistair Darby, David L RobertsonFlavia Flaviani, Eleni Nastouli, Samuel Robson, Darren Smith, Kenneth Laing, Irene Monahan, Beatrix Kele, Sam Haldenby, Ryan George, Matthew Bashton, Adam A Witney, Matthew Byott, Francesc Coll, Michael Chapman, Sharon J Peacock, Joseph Hughes, Gaia Nebbia, David G Partridge, Matthew Parker, James Richard Price, Christine Peters, Sunando Roy, Luke B Snell, Thushan I de Silva, Emma Thomson, Paul Flowers, Andrew Copas, Judith Breuer

Psychology

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Abstract

Background:

Viral sequencing of SARS-CoV-2 has been used for outbreak investigation, but there is limited evidence supporting routine use for infection prevention and control (IPC) within hospital settings.

Methods:

We conducted a prospective non-randomised trial of sequencing at 14 acute UK hospital trusts. Sites each had a 4-week baseline data collection period, followed by intervention periods comprising 8 weeks of ‘rapid’ (<48 hr) and 4 weeks of ‘longer-turnaround’ (5–10 days) sequencing using a sequence reporting tool (SRT). Data were collected on all hospital-onset COVID-19 infections (HOCIs; detected ≥48 hr from admission). The impact of the sequencing intervention on IPC knowledge and actions, and on the incidence of probable/definite hospital-acquired infections (HAIs), was evaluated.

Results:

A total of 2170 HOCI cases were recorded from October 2020 to April 2021, corresponding to a period of extreme strain on the health service, with sequence reports returned for 650/1320 (49.2%) during intervention phases. We did not detect a statistically significant change in weekly incidence of HAIs in longer-turnaround (incidence rate ratio 1.60, 95% CI 0.85–3.01; p=0.14) or rapid (0.85, 0.48–1.50; p=0.54) intervention phases compared to baseline phase. However, IPC practice was changed in 7.8 and 7.4% of all HOCI cases in rapid and longer-turnaround phases, respectively, and 17.2 and 11.6% of cases where the report was returned. In a ‘per-protocol’ sensitivity analysis, there was an impact on IPC actions in 20.7% of HOCI cases when the SRT report was returned within 5 days. Capacity to respond effectively to insights from sequencing was breached in most sites by the volume of cases and limited resources.

Conclusions:

While we did not demonstrate a direct impact of sequencing on the incidence of nosocomial transmission, our results suggest that sequencing can inform IPC response to HOCIs, particularly when returned within 5 days.

Original language	English
Article number	e78427
Number of pages	31
Journal	eLife
Volume	11
Early online date	13 Sept 2022
DOIs	https://doi.org/10.7554/elife.78427
Publication status	Published - 13 Sept 2022

Keywords

COVID-19
viral genomics
hospital-acquired infections
healthcare-associated infections
infection prevention and control
molecular epidemiology
SARS-CoV-2

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10.7554/elife.78427Licence: CC BY 4.0

Stirrup-etal-eLife-2022-Effectiveness-of-rapid-SARS-CoV-2-genome-sequencing-in-supporting-infection-controlFinal published version, 2.22 MBLicence: CC BY 4.0

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Stirrup, O., Blackstone, J., Mapp, F., MacNeil, A., Panca, M., Holmes, A., Machin, N., Shin, G. Y., Mahungu, T., Saeed, K., Saluja, T., Taha, Y., Mahida, N., Pope, C., Chawla, A., Cutino-Moguel, M.-T., Tamuri, A., Williams, R., Darby, A., ... Breuer, J. (2022). Effectiveness of rapid SARS-CoV-2 genome sequencing in supporting infection control for hospital-onset COVID-19 infection: multicenter, prospective study. eLife, 11, Article e78427. https://doi.org/10.7554/elife.78427

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title = "Effectiveness of rapid SARS-CoV-2 genome sequencing in supporting infection control for hospital-onset COVID-19 infection: multicenter, prospective study",

abstract = "Background:Viral sequencing of SARS-CoV-2 has been used for outbreak investigation, but there is limited evidence supporting routine use for infection prevention and control (IPC) within hospital settings.Methods:We conducted a prospective non-randomised trial of sequencing at 14 acute UK hospital trusts. Sites each had a 4-week baseline data collection period, followed by intervention periods comprising 8 weeks of {\textquoteleft}rapid{\textquoteright} (<48 hr) and 4 weeks of {\textquoteleft}longer-turnaround{\textquoteright} (5–10 days) sequencing using a sequence reporting tool (SRT). Data were collected on all hospital-onset COVID-19 infections (HOCIs; detected ≥48 hr from admission). The impact of the sequencing intervention on IPC knowledge and actions, and on the incidence of probable/definite hospital-acquired infections (HAIs), was evaluated.Results:A total of 2170 HOCI cases were recorded from October 2020 to April 2021, corresponding to a period of extreme strain on the health service, with sequence reports returned for 650/1320 (49.2%) during intervention phases. We did not detect a statistically significant change in weekly incidence of HAIs in longer-turnaround (incidence rate ratio 1.60, 95% CI 0.85–3.01; p=0.14) or rapid (0.85, 0.48–1.50; p=0.54) intervention phases compared to baseline phase. However, IPC practice was changed in 7.8 and 7.4% of all HOCI cases in rapid and longer-turnaround phases, respectively, and 17.2 and 11.6% of cases where the report was returned. In a {\textquoteleft}per-protocol{\textquoteright} sensitivity analysis, there was an impact on IPC actions in 20.7% of HOCI cases when the SRT report was returned within 5 days. Capacity to respond effectively to insights from sequencing was breached in most sites by the volume of cases and limited resources.Conclusions:While we did not demonstrate a direct impact of sequencing on the incidence of nosocomial transmission, our results suggest that sequencing can inform IPC response to HOCIs, particularly when returned within 5 days.",

keywords = "COVID-19, viral genomics, hospital-acquired infections, healthcare-associated infections, infection prevention and control, molecular epidemiology, SARS-CoV-2",

author = "Oliver Stirrup and James Blackstone and Fiona Mapp and Alyson MacNeil and Monica Panca and Alison Holmes and Nicholas Machin and Shin, {Gee Yen} and Tabitha Mahungu and Kordo Saeed and Tranprit Saluja and Yusri Taha and Nikunj Mahida and Cassie Pope and Anu Chawla and Maria-Teresa Cutino-Moguel and Asif Tamuri and Rachel Williams and Alistair Darby and Robertson, {David L} and Flavia Flaviani and Eleni Nastouli and Samuel Robson and Darren Smith and Kenneth Laing and Irene Monahan and Beatrix Kele and Sam Haldenby and Ryan George and Matthew Bashton and Witney, {Adam A} and Matthew Byott and Francesc Coll and Michael Chapman and Peacock, {Sharon J} and Joseph Hughes and Gaia Nebbia and Partridge, {David G} and Matthew Parker and Price, {James Richard} and Christine Peters and Sunando Roy and Snell, {Luke B} and {de Silva}, {Thushan I} and Emma Thomson and Paul Flowers and Andrew Copas and Judith Breuer",

year = "2022",

month = sep,

day = "13",

doi = "10.7554/elife.78427",

language = "English",

volume = "11",

journal = "eLife",

issn = "2050-084X",

}

Stirrup, O, Blackstone, J, Mapp, F, MacNeil, A, Panca, M, Holmes, A, Machin, N, Shin, GY, Mahungu, T, Saeed, K, Saluja, T, Taha, Y, Mahida, N, Pope, C, Chawla, A, Cutino-Moguel, M-T, Tamuri, A, Williams, R, Darby, A, Robertson, DL, Flaviani, F, Nastouli, E, Robson, S, Smith, D, Laing, K, Monahan, I, Kele, B, Haldenby, S, George, R, Bashton, M, Witney, AA, Byott, M, Coll, F, Chapman, M, Peacock, SJ, Hughes, J, Nebbia, G, Partridge, DG, Parker, M, Price, JR, Peters, C, Roy, S, Snell, LB, de Silva, TI, Thomson, E, Flowers, P, Copas, A & Breuer, J 2022, 'Effectiveness of rapid SARS-CoV-2 genome sequencing in supporting infection control for hospital-onset COVID-19 infection: multicenter, prospective study', eLife, vol. 11, e78427. https://doi.org/10.7554/elife.78427

TY - JOUR

T1 - Effectiveness of rapid SARS-CoV-2 genome sequencing in supporting infection control for hospital-onset COVID-19 infection

T2 - multicenter, prospective study

AU - Stirrup, Oliver

AU - Blackstone, James

AU - Mapp, Fiona

AU - MacNeil, Alyson

AU - Panca, Monica

AU - Holmes, Alison

AU - Machin, Nicholas

AU - Shin, Gee Yen

AU - Mahungu, Tabitha

AU - Saeed, Kordo

AU - Saluja, Tranprit

AU - Taha, Yusri

AU - Mahida, Nikunj

AU - Pope, Cassie

AU - Chawla, Anu

AU - Cutino-Moguel, Maria-Teresa

AU - Tamuri, Asif

AU - Williams, Rachel

AU - Darby, Alistair

AU - Robertson, David L

AU - Flaviani, Flavia

AU - Nastouli, Eleni

AU - Robson, Samuel

AU - Smith, Darren

AU - Laing, Kenneth

AU - Monahan, Irene

AU - Kele, Beatrix

AU - Haldenby, Sam

AU - George, Ryan

AU - Bashton, Matthew

AU - Witney, Adam A

AU - Byott, Matthew

AU - Coll, Francesc

AU - Chapman, Michael

AU - Peacock, Sharon J

AU - Hughes, Joseph

AU - Nebbia, Gaia

AU - Partridge, David G

AU - Parker, Matthew

AU - Price, James Richard

AU - Peters, Christine

AU - Roy, Sunando

AU - Snell, Luke B

AU - de Silva, Thushan I

AU - Thomson, Emma

AU - Flowers, Paul

AU - Copas, Andrew

AU - Breuer, Judith

PY - 2022/9/13

Y1 - 2022/9/13

N2 - Background:Viral sequencing of SARS-CoV-2 has been used for outbreak investigation, but there is limited evidence supporting routine use for infection prevention and control (IPC) within hospital settings.Methods:We conducted a prospective non-randomised trial of sequencing at 14 acute UK hospital trusts. Sites each had a 4-week baseline data collection period, followed by intervention periods comprising 8 weeks of ‘rapid’ (<48 hr) and 4 weeks of ‘longer-turnaround’ (5–10 days) sequencing using a sequence reporting tool (SRT). Data were collected on all hospital-onset COVID-19 infections (HOCIs; detected ≥48 hr from admission). The impact of the sequencing intervention on IPC knowledge and actions, and on the incidence of probable/definite hospital-acquired infections (HAIs), was evaluated.Results:A total of 2170 HOCI cases were recorded from October 2020 to April 2021, corresponding to a period of extreme strain on the health service, with sequence reports returned for 650/1320 (49.2%) during intervention phases. We did not detect a statistically significant change in weekly incidence of HAIs in longer-turnaround (incidence rate ratio 1.60, 95% CI 0.85–3.01; p=0.14) or rapid (0.85, 0.48–1.50; p=0.54) intervention phases compared to baseline phase. However, IPC practice was changed in 7.8 and 7.4% of all HOCI cases in rapid and longer-turnaround phases, respectively, and 17.2 and 11.6% of cases where the report was returned. In a ‘per-protocol’ sensitivity analysis, there was an impact on IPC actions in 20.7% of HOCI cases when the SRT report was returned within 5 days. Capacity to respond effectively to insights from sequencing was breached in most sites by the volume of cases and limited resources.Conclusions:While we did not demonstrate a direct impact of sequencing on the incidence of nosocomial transmission, our results suggest that sequencing can inform IPC response to HOCIs, particularly when returned within 5 days.

AB - Background:Viral sequencing of SARS-CoV-2 has been used for outbreak investigation, but there is limited evidence supporting routine use for infection prevention and control (IPC) within hospital settings.Methods:We conducted a prospective non-randomised trial of sequencing at 14 acute UK hospital trusts. Sites each had a 4-week baseline data collection period, followed by intervention periods comprising 8 weeks of ‘rapid’ (<48 hr) and 4 weeks of ‘longer-turnaround’ (5–10 days) sequencing using a sequence reporting tool (SRT). Data were collected on all hospital-onset COVID-19 infections (HOCIs; detected ≥48 hr from admission). The impact of the sequencing intervention on IPC knowledge and actions, and on the incidence of probable/definite hospital-acquired infections (HAIs), was evaluated.Results:A total of 2170 HOCI cases were recorded from October 2020 to April 2021, corresponding to a period of extreme strain on the health service, with sequence reports returned for 650/1320 (49.2%) during intervention phases. We did not detect a statistically significant change in weekly incidence of HAIs in longer-turnaround (incidence rate ratio 1.60, 95% CI 0.85–3.01; p=0.14) or rapid (0.85, 0.48–1.50; p=0.54) intervention phases compared to baseline phase. However, IPC practice was changed in 7.8 and 7.4% of all HOCI cases in rapid and longer-turnaround phases, respectively, and 17.2 and 11.6% of cases where the report was returned. In a ‘per-protocol’ sensitivity analysis, there was an impact on IPC actions in 20.7% of HOCI cases when the SRT report was returned within 5 days. Capacity to respond effectively to insights from sequencing was breached in most sites by the volume of cases and limited resources.Conclusions:While we did not demonstrate a direct impact of sequencing on the incidence of nosocomial transmission, our results suggest that sequencing can inform IPC response to HOCIs, particularly when returned within 5 days.

KW - COVID-19

KW - viral genomics

KW - hospital-acquired infections

KW - healthcare-associated infections

KW - infection prevention and control

KW - molecular epidemiology

KW - SARS-CoV-2

UR - https://doi.org/10.5522/04/20769637.v1

U2 - 10.7554/elife.78427

DO - 10.7554/elife.78427

M3 - Article

SN - 2050-084X

VL - 11

JO - eLife

JF - eLife

M1 - e78427

ER -

Effectiveness of rapid SARS-CoV-2 genome sequencing in supporting infection control for hospital-onset COVID-19 infection: multicenter, prospective study

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Keywords

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