Evaluations of modes of pooling specimens for COVID-19 screened by quantitative PCR and droplet digital PCR.


Journal

Scientific reports
ISSN: 2045-2322
Titre abrégé: Sci Rep
Pays: England
ID NLM: 101563288

Informations de publication

Date de publication:
13 05 2024
Historique:
received: 11 08 2023
accepted: 08 05 2024
medline: 14 5 2024
pubmed: 14 5 2024
entrez: 13 5 2024
Statut: epublish

Résumé

Though pooling samples for SARS-CoV-2 detection has effectively met the need for rapid diagnostic and screening tests, many factors can influence the sensitivity of a pooled test. In this study, we conducted a simulation experiment to evaluate modes of pooling specimens and aimed at formulating an optimal pooling strategy. We focussed on the type of swab, their solvent adsorption ability, pool size, pooling volume, and different factors affecting the quality of preserving RNA by different virus solutions. Both quantitative PCR and digital PCR were used to evaluate the sampling performance. In addition, we determined the detection limit by sampling which is simulated from the virus of different titers and evaluated the effect of sample-storage conditions by determining the viral load after storage. We found that flocked swabs were better than fibre swabs. The RNA-preserving ability of the non-inactivating virus solution was slightly better than that of the inactivating virus solution. The optimal pooling strategy was a pool size of 10 samples in a total volume of 9 mL. Storing the collected samples at 4 °C or 25 °C for up to 48 h had little effect on the detection sensitivity. Further, we observed that our optimal pooling strategy performed equally well as the single-tube test did. In clinical applications, we recommend adopting this pooling strategy for low-risk populations to improve screening efficiency and shape future strategies for detecting and managing other respiratory pathogens, thus contributing to preparedness for future public health challenges.

Identifiants

pubmed: 38740976
doi: 10.1038/s41598-024-61631-0
pii: 10.1038/s41598-024-61631-0
doi:

Substances chimiques

RNA, Viral 0

Types de publication

Journal Article

Langues

eng

Sous-ensembles de citation

IM

Pagination

10923

Subventions

Organisme : National Natural Science Foundation of China
ID : 82041027
Organisme : The Capital Health Development and Research of Special
ID : 2022-1G-3014
Organisme : National Key R&D Program of China
ID : 2021ZD0114100
Organisme : National Key R&D Program of China
ID : 2021ZD0114103
Organisme : Beijing Science and Technology Planning Project of Beijing Science and Technology Commission
ID : Z211100002521015
Organisme : Beijing Science and Technology Planning Project of Beijing Science and Technology Commission
ID : Z211100002521019
Organisme : the Cultivation Fund of Beijing Center for Disease Prevention and Control
ID : 2020-BJYJ-22
Organisme : Horizontal scientific research cooperation project
ID : 2022-jk-cd-021
Organisme : High-level public health technical talent construction project
ID : Key member-02-11

Informations de copyright

© 2024. The Author(s).

Références

Zou, L. et al. SARS-CoV-2 viral load in upper respiratory specimens of infected patients. N. Engl. J. Med. 382, 1177–1179 (2020).
doi: 10.1056/NEJMc2001737 pubmed: 32074444 pmcid: 7121626
Umakanthan, S. et al. Origin, transmission, diagnosis and management of coronavirus disease 2019 (COVID-19). Postgrad. Med. J. 96, 753–758. https://doi.org/10.1136/postgradmedj-2020-138234 (2020).
doi: 10.1136/postgradmedj-2020-138234 pubmed: 32563999
Majumder, J. & Minko, T. Recent developments on therapeutic and diagnostic approaches for COVID-19. AAPS J. 23, 14. https://doi.org/10.1208/s12248-020-00532-2 (2021).
doi: 10.1208/s12248-020-00532-2 pubmed: 33400058
Langford, B. J. et al. Bacterial co-infection and secondary infection in patients with COVID-19: A living rapid review and meta-analysis. Clin. Microbiol. Infect. 26, 1622–1629. https://doi.org/10.1016/j.cmi.2020.07.016 (2020).
doi: 10.1016/j.cmi.2020.07.016 pubmed: 32711058 pmcid: 7832079
Li, L. et al. Effect of convalescent plasma therapy on time to clinical improvement in patients with severe and life-threatening COVID-19: A randomized clinical trial. JAMA 324, 460–470. https://doi.org/10.1001/jama.2020.10044 (2020).
doi: 10.1001/jama.2020.10044 pubmed: 32492084
Zhou, Y. et al. Sensitivity evaluation of 2019 novel coronavirus (SARS-CoV-2) RT-PCR detection kits and strategy to reduce false negative. PLoS One 15, e0241469. https://doi.org/10.1371/journal.pone.0241469 (2020).
doi: 10.1371/journal.pone.0241469 pubmed: 33206690 pmcid: 7673793
Smith, E. et al. Analytical and clinical comparison of three nucleic acid amplification tests for SARS-CoV-2 detection. J. Clin. Microbiol. 58, e01134-01120 (2020).
doi: 10.1128/JCM.01134-20
Sharfstein, J. M., Becker, S. J. & Mello, M. M. Diagnostic testing for the novel coronavirus. JAMA 323, 1437–1438. https://doi.org/10.1001/jama.2020.3864 (2020).
doi: 10.1001/jama.2020.3864 pubmed: 32150622
Corman, V. M. et al. Detection of 2019 novel coronavirus (2019-nCoV) by real-time RT-PCR. Euro Surveill. https://doi.org/10.2807/1560-7917.ES.2020.25.3.2000045 (2020).
doi: 10.2807/1560-7917.ES.2020.25.3.2000045 pubmed: 33243353 pmcid: 7693167
Chaimayo, C. et al. Rapid SARS-CoV-2 antigen detection assay in comparison with real-time RT-PCR assay for laboratory diagnosis of COVID-19 in Thailand. Virol. J. 17, 177. https://doi.org/10.1186/s12985-020-01452-5 (2020).
doi: 10.1186/s12985-020-01452-5 pubmed: 33187528 pmcid: 7665091
Lohse, S. et al. Pooling of samples for testing for SARS-CoV-2 in asymptomatic people. Lancet Infect. Dis. 20, 1231–1232. https://doi.org/10.1016/s1473-3099(20)30362-5 (2020).
doi: 10.1016/s1473-3099(20)30362-5 pubmed: 32530425 pmcid: 7194818
Yu, J., Huang, Y. & Shen, Z. J. Optimizing and evaluating PCR-based pooled screening during COVID-19 pandemics. Sci. Rep. 11, 21460. https://doi.org/10.1038/s41598-021-01065-0 (2021).
doi: 10.1038/s41598-021-01065-0 pubmed: 34728759 pmcid: 8564549
Mercer, T. R. & Salit, M. Testing at scale during the COVID-19 pandemic. Nat. Rev. Genet. 22, 415–426. https://doi.org/10.1038/s41576-021-00360-w (2021).
doi: 10.1038/s41576-021-00360-w pubmed: 33948037 pmcid: 8094986
Lagopati, N. et al. Sample pooling strategies for SARS-CoV-2 detection. J. Virol. Methods 289, 114044. https://doi.org/10.1016/j.jviromet.2020.114044 (2021).
doi: 10.1016/j.jviromet.2020.114044 pubmed: 33316285
de Salazar, A. et al. Sample pooling for SARS-CoV-2 RT-PCR screening. Clin. Microbiol. Infect. 26, 1687 e1681-1687 e1685. https://doi.org/10.1016/j.cmi.2020.09.008 (2020).
doi: 10.1016/j.cmi.2020.09.008
Abdalhamid, B. et al. Assessment of specimen pooling to conserve SARS CoV-2 testing resources. Am. J. Clin. Pathol. 153, 715–718. https://doi.org/10.1093/ajcp/aqaa064 (2020).
doi: 10.1093/ajcp/aqaa064 pubmed: 32304208 pmcid: 7188150
Abid, S. et al. Assessment of sample pooling for SARS-CoV-2 molecular testing for screening of asymptomatic persons in Tunisia. Diagn. Microbiol. Infect. Dis. 98, 115125. https://doi.org/10.1016/j.diagmicrobio.2020.115125 (2020).
doi: 10.1016/j.diagmicrobio.2020.115125 pubmed: 32768876 pmcid: 7335417
Hogan, C. A., Sahoo, M. K. & Pinsky, B. A. Sample pooling as a strategy to detect community transmission of SARS-CoV-2. JAMA 323, 1967–1969. https://doi.org/10.1001/jama.2020.5445 (2020).
doi: 10.1001/jama.2020.5445 pubmed: 32250394 pmcid: 7136853
Lohse, S. et al. Challenges and issues of SARS-CoV-2 pool testing—Authors’ reply. Lancet Infect. Dis. 20, 1234–1235. https://doi.org/10.1016/s1473-3099(20)30455-2 (2020).
doi: 10.1016/s1473-3099(20)30455-2 pubmed: 32679086 pmcid: 7836822
Watkins, A. E. et al. Pooling saliva to increase SARS-CoV-2 testing capacity. medRxiv https://doi.org/10.1101/2020.09.02.20183830 (2020).
doi: 10.1101/2020.09.02.20183830 pubmed: 32909003 pmcid: 7480055
Chen, F. et al. Comparing two sample pooling strategies for SARS-CoV-2 RNA detection for efficient screening of COVID-19. J. Med. Virol. 93, 2805–2809. https://doi.org/10.1002/jmv.26632 (2021).
doi: 10.1002/jmv.26632 pubmed: 33107614
Christoff, A. P. et al. Swab pooling: A new method for large-scale RT-qPCR screening of SARS-CoV-2 avoiding sample dilution. PLoS One 16, e0246544. https://doi.org/10.1371/journal.pone.0246544 (2021).
doi: 10.1371/journal.pone.0246544 pubmed: 33539474 pmcid: 7861376
Centers For Disease Control And Prevention, Interim Guidance for Use of Pooling Procedures in SARS-CoV-2 Diagnostic and Screening Testing. https://www.cdc.gov/coronavirus/2019-ncov/lab/pooling-procedures.html (2021).
Ambrosi, C. et al. SARS-CoV-2: Comparative analysis of different RNA extraction methods. J. Virol. Methods https://doi.org/10.1016/j.jviromet.2020.114008 (2021).
doi: 10.1016/j.jviromet.2020.114008 pubmed: 33160015
Dang, Y. et al. Comparison of qualitative and quantitative analyses of COVID-19 clinical samples. Clin. Chim. Acta 510, 613–616. https://doi.org/10.1016/j.cca.2020.08.033 (2020).
doi: 10.1016/j.cca.2020.08.033 pubmed: 32858058 pmcid: 7446654
Li, H. et al. Application of droplet digital PCR to detect the pathogens of infectious diseases. Biosci. Rep. https://doi.org/10.1042/bsr20181170 (2018).
Garg, J. et al. Evaluation of sample pooling for diagnosis of COVID-19 by real time-PCR: A resource-saving combat strategy. J. Med. Virol. 93, 1526–1531. https://doi.org/10.1002/jmv.26475 (2020).
doi: 10.1002/jmv.26475 pubmed: 32869865
Tan, C. et al. Applications of digital PCR in COVID‐19 pandemic. View https://doi.org/10.1002/viw.20200082 (2021).
doi: 10.1002/viw.20200082 pubmed: 34766158
Wagner, K. et al. A multiplexed, paired-pooled droplet digital PCR assay for detection of SARS-CoV-2 in saliva. Sci. Rep. https://doi.org/10.1038/s41598-023-29858-5 (2023).
doi: 10.1038/s41598-023-29858-5 pubmed: 38114575 pmcid: 10730523
Mahmoud, S. A. et al. Evaluation of pooling of samples for testing SARS-CoV-2 for mass screening of COVID-19. BMC Infect. Dis. https://doi.org/10.1186/s12879-021-06061-3 (2021).
doi: 10.1186/s12879-021-06061-3 pubmed: 34284735 pmcid: 8293485
Vasudevan, H. N. et al. Digital droplet PCR accurately quantifies SARS-CoV-2 viral load from crude lysate without nucleic acid purification. Sci. Rep. https://doi.org/10.1038/s41598-020-80715-1 (2021).
doi: 10.1038/s41598-020-80715-1 pubmed: 34599198 pmcid: 8486835
Weng, Y., Zhou, J. & Shi, Y. A virus preservation solution that inactivates the virus while maintaining the virus particle intact. Ann. Transl. Med. 10, 1064–1064. https://doi.org/10.21037/atm-22-4295 (2022).
doi: 10.21037/atm-22-4295 pubmed: 36330392 pmcid: 9622497
Lian, J.-S. et al. Comparison of epidemiological and clinical characteristics of COVID-19 patients with and without Wuhan exposure. J. Zhejiang Univ. Sci. B 21, 369–377. https://doi.org/10.1631/jzus.B2000112 (2020).
doi: 10.1631/jzus.B2000112 pubmed: 32425002 pmcid: 7210103
Wu, H.-X. et al. Clinical evaluation of bacterial DNA using an improved droplet digital PCR for spontaneous bacterial peritonitis diagnosis. Front. Cell. Infect. Microbiol. https://doi.org/10.3389/fcimb.2022.876495 (2022).
doi: 10.3389/fcimb.2022.876495 pubmed: 36846550 pmcid: 9813413
Perez-Zabaleta, M. et al. Long-term SARS-CoV-2 surveillance in the wastewater of Stockholm: What lessons can be learned from the Swedish perspective?. Sci. Total Environ. https://doi.org/10.1016/j.scitotenv.2022.160023 (2023).
doi: 10.1016/j.scitotenv.2022.160023 pubmed: 37120021

Auteurs

Daitao Zhang (D)

Institute for Infectious Disease and Endemic Disease Control, Beijing Center for Disease Prevention and Control, Beijing Research Center for Respiratory Infectious Diseases, Beijing, 100013, China.

Lingyu Shen (L)

Institute for Infectious Disease and Endemic Disease Control, Beijing Center for Disease Prevention and Control, Beijing Research Center for Respiratory Infectious Diseases, Beijing, 100013, China.

Zhichao Liang (Z)

Institute for Infectious Disease and Endemic Disease Control, Beijing Center for Disease Prevention and Control, Beijing Research Center for Respiratory Infectious Diseases, Beijing, 100013, China.

Shujuan Cui (S)

Institute for Infectious Disease and Endemic Disease Control, Beijing Center for Disease Prevention and Control, Beijing Research Center for Respiratory Infectious Diseases, Beijing, 100013, China. csjbjcdc1@126.com.

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