Comparison of analytical performance and economic value of two biosurveillance methods for tracking SARS-COV-2 variants of concern

ABSTRACTThe development of biosurveillance programs with strong analytical performance and economically accessible protocols is essential for monitoring viral pathogens. Throughout the COVID-19 pandemic, whole-genome sequencing (WGS) has been the prevailing technology for SARS-CoV-2 variant of conce...

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Main Authors: Nicholas P. Pinkhover, Kerriann M. Pontbriand, Kelli P. Fletcher, Eduardo Sanchez, Kenneth Okello, Liam M. Garvey, Alex Pum, Kurvin Li, Gabriel DeOliveira, Teddie Proctor, Jelena D. M. Feenstra, Océane Sorel, Manoj Gandhi, Jared R. Auclair
Format: Article
Language:English
Published: American Society for Microbiology 2024-02-01
Series:Microbiology Spectrum
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Online Access:https://journals.asm.org/doi/10.1128/spectrum.03484-23
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author Nicholas P. Pinkhover
Kerriann M. Pontbriand
Kelli P. Fletcher
Eduardo Sanchez
Kenneth Okello
Liam M. Garvey
Alex Pum
Kurvin Li
Gabriel DeOliveira
Teddie Proctor
Jelena D. M. Feenstra
Océane Sorel
Manoj Gandhi
Jared R. Auclair
author_facet Nicholas P. Pinkhover
Kerriann M. Pontbriand
Kelli P. Fletcher
Eduardo Sanchez
Kenneth Okello
Liam M. Garvey
Alex Pum
Kurvin Li
Gabriel DeOliveira
Teddie Proctor
Jelena D. M. Feenstra
Océane Sorel
Manoj Gandhi
Jared R. Auclair
author_sort Nicholas P. Pinkhover
collection DOAJ
description ABSTRACTThe development of biosurveillance programs with strong analytical performance and economically accessible protocols is essential for monitoring viral pathogens. Throughout the COVID-19 pandemic, whole-genome sequencing (WGS) has been the prevailing technology for SARS-CoV-2 variant of concern (VOC) detection. While WGS offers benefits, it is a lengthy process, financially and technically straining for scalable viral tracking. The aim of this study was to compare the analytical performance and economic feasibility of WGS and PCR mutation panels for distinguishing six known VOCs: Alpha (B.1.1.7 and Q.4), Gamma (P.1), Delta (B.1.617.2 and AY.4.2), and Omicron. (B.1.1.529.1). In all, 78 SARS-CoV-2-positive samples were collected from April to December 2021 at Northeastern University (Cabot Testing Site, Boston, MA, USA) for genotyping PCR and WGS analysis. MagMax Viral/Pathogen II Nucleic Acid Isolation and TaqPath COVID-19 Combo Kits were used for RNA extraction and SARS-CoV-2 confirmation. VOC discrimination was assessed using two TaqMan SARS-CoV-2 single nucleotide polymorphism (SNP) assay layouts, and Ion Torrent WGS. In November 2021, the mutation panel demonstrated marked versatility by detecting the emerging Omicron variant reported by South Africa. SNP panel analysis yielded the following 78 VOC identifications: Alpha B.1.1.7 (N = 20), Alpha Q.4 (N = 3), Gamma P.1 (N = 1), Delta B.1.617.2 (N = 30), Delta AY.4.2 (N = 3), and Omicron B.1.1.529.1 (N = 20) with one undetermined (N = 1) sample. Genotyping mutation panels designated lineages in 77 of 78 samples, 46/78 were confirmed by WGS, while 32 samples failed WGS lineage assignment. RT-PCR genotyping panels offer pronounced throughput and sensitivity and provide an economically advantageous technique for SARS-CoV-2 biosurveillance.IMPORTANCEThe results presented in our manuscript demonstrate how the value of simplistic and reliable molecular assays coupled with the core scientific principle of standardization can be overlooked by the charm of more sophisticated assays and instrumentation. This effect can often be amplified during tumultuous public health events, such as the COVID-19 pandemic. By adapting standardized PCR mutation panels to detect prominently circulating SARS-CoV-2 variants, we were able to better assess the potential health impacts of rising positivity rates and transmission clusters within the Northeastern University population. While several literature publications utilizing genotyping PCR and NGS have a similar scope to ours, many investigations lack sufficiently standardized genotyping PCR and NGS bioinformatics inclusionary/exclusionary criteria for SARS-CoV-2 variant identification. Finally, the economic benefits of standardized PCR mutation panels would allow for global implementation of biosurveillance, rather than reserving biosurveillance to more economically developed nations.
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spelling doaj.art-511a292b18e945d5a1de7c9a3882293c2024-02-06T14:04:55ZengAmerican Society for MicrobiologyMicrobiology Spectrum2165-04972024-02-0112210.1128/spectrum.03484-23Comparison of analytical performance and economic value of two biosurveillance methods for tracking SARS-COV-2 variants of concernNicholas P. Pinkhover0Kerriann M. Pontbriand1Kelli P. Fletcher2Eduardo Sanchez3Kenneth Okello4Liam M. Garvey5Alex Pum6Kurvin Li7Gabriel DeOliveira8Teddie Proctor9Jelena D. M. Feenstra10Océane Sorel11Manoj Gandhi12Jared R. Auclair13Department of Chemistry and Chemical Biology, Life Sciences Testing Center, Northeastern University Innovation Campus, Burlington, Massachusetts, USADepartment of Chemistry and Chemical Biology, Life Sciences Testing Center, Northeastern University Innovation Campus, Burlington, Massachusetts, USADepartment of Chemistry and Chemical Biology, Life Sciences Testing Center, Northeastern University Innovation Campus, Burlington, Massachusetts, USADepartment of Chemistry and Chemical Biology, Life Sciences Testing Center, Northeastern University Innovation Campus, Burlington, Massachusetts, USADepartment of Chemistry and Chemical Biology, Life Sciences Testing Center, Northeastern University Innovation Campus, Burlington, Massachusetts, USADepartment of Chemistry and Chemical Biology, Life Sciences Testing Center, Northeastern University Innovation Campus, Burlington, Massachusetts, USADepartment of Chemistry and Chemical Biology, Life Sciences Testing Center, Northeastern University Innovation Campus, Burlington, Massachusetts, USADepartment of Chemistry and Chemical Biology, Life Sciences Testing Center, Northeastern University Innovation Campus, Burlington, Massachusetts, USADepartment of Chemistry and Chemical Biology, Life Sciences Testing Center, Northeastern University Innovation Campus, Burlington, Massachusetts, USAThermo Fisher Scientific, Genetic Testing Solutions, South San Francisco, California, USAThermo Fisher Scientific, Genetic Testing Solutions, South San Francisco, California, USAThermo Fisher Scientific, Genetic Testing Solutions, South San Francisco, California, USAThermo Fisher Scientific, Genetic Testing Solutions, South San Francisco, California, USADepartment of Chemistry and Chemical Biology, Life Sciences Testing Center, Northeastern University Innovation Campus, Burlington, Massachusetts, USAABSTRACTThe development of biosurveillance programs with strong analytical performance and economically accessible protocols is essential for monitoring viral pathogens. Throughout the COVID-19 pandemic, whole-genome sequencing (WGS) has been the prevailing technology for SARS-CoV-2 variant of concern (VOC) detection. While WGS offers benefits, it is a lengthy process, financially and technically straining for scalable viral tracking. The aim of this study was to compare the analytical performance and economic feasibility of WGS and PCR mutation panels for distinguishing six known VOCs: Alpha (B.1.1.7 and Q.4), Gamma (P.1), Delta (B.1.617.2 and AY.4.2), and Omicron. (B.1.1.529.1). In all, 78 SARS-CoV-2-positive samples were collected from April to December 2021 at Northeastern University (Cabot Testing Site, Boston, MA, USA) for genotyping PCR and WGS analysis. MagMax Viral/Pathogen II Nucleic Acid Isolation and TaqPath COVID-19 Combo Kits were used for RNA extraction and SARS-CoV-2 confirmation. VOC discrimination was assessed using two TaqMan SARS-CoV-2 single nucleotide polymorphism (SNP) assay layouts, and Ion Torrent WGS. In November 2021, the mutation panel demonstrated marked versatility by detecting the emerging Omicron variant reported by South Africa. SNP panel analysis yielded the following 78 VOC identifications: Alpha B.1.1.7 (N = 20), Alpha Q.4 (N = 3), Gamma P.1 (N = 1), Delta B.1.617.2 (N = 30), Delta AY.4.2 (N = 3), and Omicron B.1.1.529.1 (N = 20) with one undetermined (N = 1) sample. Genotyping mutation panels designated lineages in 77 of 78 samples, 46/78 were confirmed by WGS, while 32 samples failed WGS lineage assignment. RT-PCR genotyping panels offer pronounced throughput and sensitivity and provide an economically advantageous technique for SARS-CoV-2 biosurveillance.IMPORTANCEThe results presented in our manuscript demonstrate how the value of simplistic and reliable molecular assays coupled with the core scientific principle of standardization can be overlooked by the charm of more sophisticated assays and instrumentation. This effect can often be amplified during tumultuous public health events, such as the COVID-19 pandemic. By adapting standardized PCR mutation panels to detect prominently circulating SARS-CoV-2 variants, we were able to better assess the potential health impacts of rising positivity rates and transmission clusters within the Northeastern University population. While several literature publications utilizing genotyping PCR and NGS have a similar scope to ours, many investigations lack sufficiently standardized genotyping PCR and NGS bioinformatics inclusionary/exclusionary criteria for SARS-CoV-2 variant identification. Finally, the economic benefits of standardized PCR mutation panels would allow for global implementation of biosurveillance, rather than reserving biosurveillance to more economically developed nations.https://journals.asm.org/doi/10.1128/spectrum.03484-23SARS-CoV-2surveillancegenotypingPCRNGSsequencing
spellingShingle Nicholas P. Pinkhover
Kerriann M. Pontbriand
Kelli P. Fletcher
Eduardo Sanchez
Kenneth Okello
Liam M. Garvey
Alex Pum
Kurvin Li
Gabriel DeOliveira
Teddie Proctor
Jelena D. M. Feenstra
Océane Sorel
Manoj Gandhi
Jared R. Auclair
Comparison of analytical performance and economic value of two biosurveillance methods for tracking SARS-COV-2 variants of concern
Microbiology Spectrum
SARS-CoV-2
surveillance
genotyping
PCR
NGS
sequencing
title Comparison of analytical performance and economic value of two biosurveillance methods for tracking SARS-COV-2 variants of concern
title_full Comparison of analytical performance and economic value of two biosurveillance methods for tracking SARS-COV-2 variants of concern
title_fullStr Comparison of analytical performance and economic value of two biosurveillance methods for tracking SARS-COV-2 variants of concern
title_full_unstemmed Comparison of analytical performance and economic value of two biosurveillance methods for tracking SARS-COV-2 variants of concern
title_short Comparison of analytical performance and economic value of two biosurveillance methods for tracking SARS-COV-2 variants of concern
title_sort comparison of analytical performance and economic value of two biosurveillance methods for tracking sars cov 2 variants of concern
topic SARS-CoV-2
surveillance
genotyping
PCR
NGS
sequencing
url https://journals.asm.org/doi/10.1128/spectrum.03484-23
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