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Correlation between 3790 qPCR positives samples and positive cell cultures including 1941 SARS-CoV-2 isolates

DOI: 10.1093/cid/ciaa1491
Authors:
Rita Jaafar at Aix-Marseille Université
Rita Jaafar
Sarah Aherfi at Assistance Publique Hôpitaux de Marseille
Sarah Aherfi
Nathalie Wurtz
Nathalie Wurtz
Clio Grimaldier
Clio Grimaldier
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Correlation between 3790 qPCR positives samples and positive cell cultures including
1941 SARS-CoV-2 isolates
Rita Jaafar a,b, Sarah Aherfi a,b, Nathalie Wurtz a,b, Clio Grimaldiera,b, Van Thuan Hoanga,c,d,
Philippe Colsona,b, Didier Raoulta,b, Bernard La Scolaa,b*
aIHU-Méditerranée Infection, Marseille, France.
bAix Marseille Univ, IRD, APHM, MEPHI, Marseille, France.
cAix Marseille Univ, IRD, AP-HM, SSA, VITROME, Marseille, France.
dThai Binh University of Medicine and Pharmacy, Thai Binh, Viet Nam
*Corresponding author:
Bernard La Scola bernard.la-scola@univ-amu.fr
Accepted Manuscript
2
Dear Editor -
Since the beginning of the outbreak of the emerging epidemic (Covid-19) due to
SARS-CoV-2, declared as a pandemic on March 12th 2020 by the WHO [1], a major issue
has been to correlate viral RNA load obtained after RT-PCR and expressed in cycle threshold
(Ct) with contagiousness and therefore duration of eviction from contacts and discharge from
specialized infectious disease wards. Several works published recently and based on more
than 100 studies attempt to propose such cut off for Ct value and duration of eviction with a
consensus at approximately Ct > 30 and at least 10 days, respectively [25]. However, in an
article published in this journal, a group reported that patients could be not be contagious
above 25 Ct as the virus was not detected in culture above this Ct [6]. This limit was then
evoked in the French media during the interview with the member of the French Scientific
Council Covid-19 as a possible value above which patients are no longer contagious [7]. At
the beginning of the outbreak, we correlated the Ct values obtained by our PCR technique
based on the amplification of the E gene and the results of the culture [8]. Since the beginning
of the epidemic, we have performed in our institute 250,566 SARS-CoV-2 RT-PCR for
179,151 patients, of which 13,161 (7.3%) tested positive. Up to the end of May, 3 790 of
these samples reported positives on naso-pharyngeal samples were inoculated and managed
for culture as previously described [8]. Of these 3 790 inoculated samples, 1941 SARS-Cov-2
isolates could be obtained after the first inoculation or up to 2 blind subcultures. The
correlation between the scanner values and the positivity of the culture allows us to observe
that the image obtained with ten times more isolates than our preliminary work (1941 versus
129) does not change significantly (Figure 1). It can be observed that at Ct=25, up to 70% of
patients remain positive in culture and that at Ct=30 this value drops to 20%. At Ct=35, the
value we used to report positive result for PCR, less than 3% of culture are negative. Our Ct
value of 35 initially based on the results obtained by RT-PCR on control negative samples in
Accepted Manuscript
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our laboratory and initial results of cultures [8] is validated by the present work and is in
correlation with what was proposed i.e. in Korea [9] or Taiwan [10]. We could observe that
subcultures, especially the first one, allow increasing percentage of viral isolation on high Ct
samples, confirming that these high Ct are mostly correlated with low viral loads. From our
cohort, we now need to try to understand and define the duration and frequency of live virus
shedding in patients on a case-by-case basis, in the rare cases where the PCR is positive
beyond 10 days, often at a Ct above 30. In any cases, these rare cases should not impact
public health decisions.
Accepted Manuscript
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Acknowledgments.
Ethical approval :            
     -01). All subjects provided informed
consent in accordance with the Declaration of Helsinki.
Funding:           
         Agence Nationale de la
Recherche (ANR, French National Agency for Research), (reference: Méditerranée Infection
10-IAHU-03), by Région Provence-Alpes-     
PRIMI.
Conflict of Interest: D.R. reports grants from Hitachi High-Tech Corporation, outside the
submitted work. The others authors declare no conflict of interest.
Accepted Manuscript
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hypersensibilite-des-tests-pcr-entre-intox-et-vrai-debat_6051528_4355770.html. Accessed 20
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Diagnosis of COVID-19 for Timely Diagnosis. Diagnostics 2020; 10:333.
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Figure 1. Percentage of positive viral culture of SARS-CoV-2 PCR-positive nasopharyngeal
samples from Covid-19 patients, according to Ct value (plain line). The dashed curve
indicates the polynomial regression curve.
Accepted Manuscript
Figure 1
... Besides, we also determined the level of detection of the two molecular assays by analyzing tenfold dilutions of a suspension of Vero E6 cell-cultured SARS-CoV-2 IHUMI-3 strain [10]. This strain was obtained from a nasopharyngeal swab of an RT-PCR positive patient, as previously reported [10]. ...
... Besides, we also determined the level of detection of the two molecular assays by analyzing tenfold dilutions of a suspension of Vero E6 cell-cultured SARS-CoV-2 IHUMI-3 strain [10]. This strain was obtained from a nasopharyngeal swab of an RT-PCR positive patient, as previously reported [10]. ...
Contribution of VitaPCR SARS-CoV-2 to the emergency diagnosis of COVID-19
Article
Background With the persistent COVID-19 pandemic, there is an urgent need to use rapid and reliable diagnostic tools for highly urgent cases. Antigen tests are disappointing with their lack of sensitivity. Among molecular tools allowing a diagnosis in less than an hour, only one, the Cepheid Xpert Xpress SARS-CoV-2 assay, has exhibited a good sensitivity. However, we are also facing a global shortage of reagents and kits. Thus, it is imperative to evaluate other point-of-care molecular tests. Methods We evaluated the VitaPCR™ RT-PCR assay, whose sample analysis time is of approximately 20 min, in nasopharyngeal secretions from 534 patients presenting to our Institute, for the diagnosis of COVID-19, and compared it to our routine RT-PCR assay. We also compared the two assays with tenfold dilutions of a SARS-CoV-2 strain. Results Compared to our routine RT-PCR and the previous diagnosis of COVID-19, the sensitivity, specificity, positive and negative predictive values of VitaPCR™ can be evaluated to be 99.3 % (155/156), 94.7 % (358/378), 88.6 % (155/175) and 99.7 % (358/359), respectively. Tenfold dilutions of a SARS-CoV-2 strain show that the VitaPCR™ was more sensitive that our routine RT-PCR assay. Conclusion The VitaPCR™ SARS-CoV-2 is an accurate rapid test, suitable for clinical practice that can be performed as part of a point-of-care testing, for the rapid diagnosis of COVID-19.
... The results were interpreted by the laboratories that performed the tests. In our laboratory, PCR were determined to be positive in case of Ct values lower than 35, which we were able to confirm in the largest study published to date that compared culture and PCR [4] . Since then, we have performed > 250,0 0 0 PCRs in our laboratory, diagnosed > 13,0 0 0 people, and the efficacy of HCQ on viral carriage, which was the only element we reported in our seminal article, has been confirmed in a larger set of patients by our team [5] as well as by others [6] . ...
Interpretation of SARS-CoV-2 PCR results for the diagnosis of COVID-19
Article
... whereby the positive rate was found to decline below 15% with Ct values ≥28 in presymptomatic patients who later developed a suggestive clinical picture [23]. Similar evidence has been reported in several other studies, such as those published by Basile et al. [24], La Scola et al. [25] and Jaafar et al. [26], who both also concluded that the rate of positive SARS-CoV-2 cultures is inversely associated with viral load, achieving a virtually zero likelihood of a positive culture in clinical specimens with Ct values ≥33-34. Overall, a recent meta-analysis of published studies revealed a high heterogeneity in such Ct thresholds, with no growth ranging between Ct of 24 and 32 [27], thus paving the way to additional investigations aimed to more precisely define the correlation between NAAT results and viral culture of SARS-CoV-2. ...
Clinical assessment of the Roche SARS-CoV-2 Rapid Antigen Test
Article
Full-text available
  • Dec 2020
Background. Novel point-of-care antigen assays present a promising opportunity for rapid screening for severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) infections. The purpose of this study was the clinical assessment of the new Roche SARS-CoV-2 Rapid Antigen Test. Methods. The clinical performance of Roche SARS-CoV-2 Rapid Antigen Test was evaluated versus a reverse transcription polymerase chain reaction (RT-PCR) laboratory-based assay (Seegene AllplexTM2019-nCoV) in nasopharyngeal swabs collected from a series of consecutive patients referred for SARS-CoV-2 diagnostics to the Pederzoli Hospital (Peschiera del Garda, Verona, Italy) over a 2-week period. Results. The final study population consisted of 321 consecutive patients (mean age, 46 years and IQR, 32-56 years; 181 women, 56.4%), with 149/321 (46.4%) positive for SARS-CoV-2 RNA via the Seegene AllplexTM2019-nCoV Assay, and 109/321 (34.0%) positive with Roche SARS-CoV-2 Rapid Antigen Test, respectively. The overall accuracy of Roche SARS-CoV-2 Rapid Antigen Test compared to molecular testing was 86.9%, with 72.5% sensitivity and 99.4% specificity. Progressive decline in performance was observed as cycle threshold (Ct) values of different SARS-CoV-2 gene targets increased. The sensitivity was found to range between 97-100% in clinical samples with Ct values <25, between 50-81% in those with Ct values between 25-<30, but low as 12-18% in samples with Ct values between 30-<37. Conclusions. The clinical performance of Roche SARS-CoV-2 Rapid Antigen Test is excellent in nasopharyngeal swabs with Ct values <25, which makes it a reliable screening test in patients with high viral load. However, mass community screening would require the use of more sensitive techniques.
... Several investigators have reported difficulty in culturing virus from patient samples with measured viral loads below approximately 1×10 5 RNA copies/mL [21][22][23][24]. However, virus has been recovered from samples with RNA levels as low as 1.2×10 4 copies/mL [25], and from samples with a Ct value of 34-35 on a range of PCR assays [26][27][28]. Using our conversion factor from the correlation of Ag and RNA levels, 1 x 10 4 copies/mL translates to 1.5 pg/mL, which is about 5 times higher than the S-PLEX Ag assay cutoff (0.32 pg/mL), suggesting that the S-PLEX Ag assay should be able to detect Ag in most if not all samples from which virus is culturable (though we note cultures themselves have variable sensitivity [29], and that lack of ability to culture virus doesn't preclude transmission). ...
Correlation of SARS-CoV-2 nucleocapsid antigen and RNA concentrations in nasopharyngeal samples from children and adults using an ultrasensitive and quantitative antigen assay
Preprint
Full-text available
  • Nov 2020
Background Diagnosis of COVID-19 by PCR offers high sensitivity, but the utility of detecting samples with high cycle threshold (Ct) values remains controversial. Currently available rapid diagnostic tests (RDTs) for SARS-CoV-2 nucleocapsid antigens (Ag) have sensitivity well below PCR. The correlation of Ag and RNA quantities in clinical nasopharyngeal (NP) samples is unknown. Methods An ultrasensitive, quantitative electrochemiluminescence immunoassay for SARS-CoV-2 nucleocapsid (the MSD ® S-PLEX ® CoV-2 N assay) was used to measure Ag in clinical NP samples from adults and children previously tested by PCR. Results The S-PLEX Ag assay had a limit of detection (LOD) of 0.16 pg/mL and a cutoff of 0.32 pg/mL. Ag concentrations measured in clinical NP samples (collected in 3.0 mL media) ranged from less than 160 fg/mL to 2.7 ug/mL. Log-transformed Ag concentrations correlated tightly with Ct values. In 35 adult and 101 pediatric PCR-positive samples, sensitivity was 91% (95% CI, 77-98%) and 79% (70-87%), respectively. In samples with Ct ≤ 35, sensitivity was 100% (88-100%) and 96% (88-99%), respectively. In 50 adult and 40 pediatric PCR-negative specimens, specificity was 100% (93-100%) and 98% (87-100%), respectively. Conclusions Nucleocapsid concentrations in clinical NP samples span 8 orders of magnitude and correlate closely with RNA concentrations (Ct values). The S-PLEX Ag assay had 96-100% sensitivity in samples from children and adults with Ct values ≤ 35, and 98-100% specificity. These results clarify Ag concentration distributions in clinical samples, providing insight into the performance of Ag RDTs and offering a new approach to diagnosis of COVID-19. Key points SARS-CoV-2 nucleocapsid concentrations in clinical nasopharyngeal samples, measured with an ultrasensitive assay, spanned an 8-log range and correlated closely with PCR Ct values. The assay was 96-100% sensitive in pediatric/adult samples with Ct values ≤ 35, and 98-100% specific.
... The positive samples that are most likely to be missed because of dilution are those with the highest C t values before dilution-that is, those with the lowest viral load. The individuals concerned are likely to be the least infectious 24,25 . Conversely, those individuals-whether symptomatic or asymptomatic-whose samples have the lowest C t values, which are the least affected by sample dilution, are the most important to detect as they are likely to be the most infectious. ...
A pooled testing strategy for identifying SARS-CoV-2 at low prevalence
Article
Full-text available
Suppressing SARS-CoV-2 will likely require the rapid identification and isolation of infected individuals on an ongoing basis. Reverse transcription polymerase chain reaction (RT-PCR) tests are accurate but costly, making regular testing of every individual expensive. The costs are a challenge for all countries and particularly for developing countries. Cost reductions can be achieved by pooling (or combining) subsamples and testing them in groups1–7. A balance must be struck between increasing the group size and retaining test sensitivity, since sample dilution increases the likelihood of false negatives for individuals with low viral load in the sampled region at the time of the test⁸. Likewise, minimising the number of tests to reduce costs must be balanced against minimising the time testing takes to reduce the spread of infection. Here we propose an algorithm for pooling subsamples based on the geometry of a hypercube that, at low prevalence, accurately identifies infected individuals in a small number of tests and rounds of testing. We discuss the optimal group size and explain why, given the highly infectious nature of the disease, largely parallel searches are preferred. We report proof of concept experiments in which a positive subsample was detected even when diluted 100-fold with negative subsamples (cf. 30-fold to 48-fold dilution in Refs. 9–11). We quantify the loss of sensitivity due to dilution and discuss how it may be mitigated by frequent re-testing of groups, for example. With the use of these methods, the cost of mass testing could be reduced by a large factor which, furthermore, increases as the prevalence falls. Field trials of our approach are under way in Rwanda and South Africa. The use of group testing on a massive scale to closely and continually monitor infection in a population, along with rapid and effective isolation of infected people, provides a promising pathway to the longterm control of COVID-19.
... Use of such a test in a clinical situation (as in pillar 1) was very helpful as a rapid screen but the testing strategy now seems to be driving policy. The problem of functional false positive rates has still not been addressed and particularly in the context of low prevalence of disease whereby false positives are likely to exceed true positives substantially and moreover correlate poorly with the person being infectious [12], [13]. Alongside this we have the issue that it is normal to see an increase in illness and deaths during the winter months. ...
Covid nov 2020 - First do no harm open letter
Presentation
Full-text available
  • Nov 2020
Are you becoming more and more concerned about the impact of lockdowns and a narrative of fear on the overall health and wellbeing of the nation, and in particular on children? Are you seeing more patients with deterioration in their mental health? Are you seeing delays in cancer diagnosis and treatment? This is without even considering the economic impact and the known adverse effects of poverty on health. We, the undersigned, are scientists and health professionals, trained to look at balance of risks and work to the tenet 'First do no harm'. If you think that Covid measures are now disproportionate and doing more harm than good, then please sign this letter and share it with colleagues. Let us together build on the work of many to change the current single focus strategy. https://usforthem.co.uk/open-letter-from-health-professionals-and-scientists-to-the-prime-minister
... Une étude récente a montré que le virus avait pu être cultivé pour 1941 des 3790 échantillons rhino-pharyngés prélevés chez des patients testés positifs par RT-PCR pour SARS-CoV-2. Pour ces échantillons dont le virus avait pu être isolé par culture cellulaire, 87,6% d'entre eux avaient été prélevés la première semaine de l'infection, 9,6% la deuxième semaine et 2,8% la troisième semaine [6]. Dans d'autres études comportant des cultures cellulaires, du virus infectieux a pu être isolé jusqu'à 10 jours après le début des symptômes chez les sujets présentant une forme modérée de Covid-19 [2,[7][8][9] et jusqu'à 20 jours après le début des symptômes -avec une médiane de 8 joursdans les formes sévères [10]. ...
Haut Conseil de la santé publique AVIS Haut Conseil de la santé publique AVIS Haut Conseil de la santé publique 1/22 Cet avis doit être diffusé dans sa totalité, sans ajout ni modification relatif à l’inscription de l’encéphalite à tiques sur la liste des maladies à déclaration obligatoire
Technical Report
Full-text available
  • Nov 2020
Duration of infectiousness and correlation with RT-PCR cycle threshold values in cases of COVID-19, England, January to May 2020
Article
Full-text available
  • Aug 2020
Severe acute respiratory syndrome coronavirus 2 viral load in the upper respiratory tract peaks around symptom onset and infectious virus persists for 10 days in mild-to-moderate coronavirus disease (n = 324 samples analysed). RT-PCR cycle threshold (Ct) values correlate strongly with cultivable virus. Probability of culturing virus declines to 8% in samples with Ct > 35 and to 6% 10 days after onset; it is similar in asymptomatic and symptomatic persons. Asymptomatic persons represent a source of transmissible virus.
SARS-CoV-2, SARS-CoV-1 and MERS-CoV viral load dynamics, duration of viral shedding and infectiousness -a living systematic review and meta-analysis
Preprint
Full-text available
  • Jul 2020
Background Viral load kinetics and the duration of viral shedding are important determinants for disease transmission. We aim i) to characterise viral load dynamics, duration of viral RNA, and viable virus shedding of SARS-CoV-2 in various body fluids and ii) to compare SARS-CoV-2 viral dynamics with SARS-CoV-1 and MERS-CoV. Methods: Medline, EMBASE, Europe PMC, preprint servers and grey literature were searched to retrieve all articles reporting viral dynamics and duration of SARS-CoV-2, SARS-CoV-1 and MERS-CoV shedding. We excluded case reports and case series with < 5 patients, or studies that did not report shedding duration from symptom onset. PROSPERO registration: CRD42020181914. Findings: Seventy-nine studies on SARS-CoV-2, 8 on SARS-CoV-1, and 11 on MERS-CoV were included. Mean SARS-CoV-2 RNA shedding duration in upper respiratory tract, lower respiratory tract, stool and serum were 17.0, 14.6, 17.2 and 16.6 days, respectively. Maximum duration of SARS-CoV-2 RNA shedding reported in URT, LRT, stool and serum was 83, 59, 35 and 60 days, respectively. Pooled mean duration of SARS-CoV-2 RNA shedding was positively associated with age (p=0.002), but not gender (p = 0.277). No study to date has detected live virus beyond day nine of illness despite persistently high viral loads. SARS-CoV-2 viral load in the upper respiratory tract appears to peak in the first week of illness, while SARS-CoV-1 and MERS-CoV peak later. Conclusion: Although SARS-CoV-2 RNA shedding in respiratory and stool can be prolonged, duration of viable virus is relatively short-lived. Thus, detection of viral RNA cannot be used to infer infectiousness. High SARS-CoV-2 titres are detectable in the first week of illness with an early peak observed at symptom onset to day 5 of illness. This review underscores the importance of early case finding and isolation, as well as public education on the spectrum of illness. However, given potential delays in the isolation of patients, effective containment of SARS-CoV-2 may be challenging even with an early detection and isolation strategy. Funding: No funding was received.
Optimization of the CDC Protocol of Molecular Diagnosis of COVID-19 for Timely Diagnosis
Article
Full-text available
  • May 2020
Coronavirus disease 2019 (COVID-19), the current uncontrolled outbreak of infectious disease, has caused significant challenges throughout the world. A reliable rapid diagnostic test for COVID-19 is demanded worldwide. The real-time reverse transcriptase polymerase chain was one of the most quickly established methods in the novel viral pandemic and was considered as the gold standard for the detection of severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2). In this report, we illustrate our experience of applying a protocol from the Taiwan CDC and achieving assay optimization in the immediate circumstances to meet the urgent medical and public health needs.
Interpreting the COVID-19 Test Results: a Guide for Physiatrists
Article
Full-text available
Viral RNA load as determined by cell culture as a management tool for discharge of SARS-CoV-2 patients from infectious disease wards
Article
Full-text available
In a preliminary clinical study, we observed that the combination of hydroxychloroquine and azithromycin was effective against SARS-CoV-2 by shortening the duration of viral load in Covid-19 patients. It is of paramount importance to define when a treated patient can be considered as no longer contagious. Correlation between successful isolation of virus in cell culture and Ct value of quantitative RT-PCR targeting E gene suggests that patients with Ct above 33-34 using our RT-PCR system are not contagious and thus can be discharged from hospital care or strict confinement for non-hospitalized patients.
Viral cultures for COVID-19
  • T Jefferson
  • E Spencer
  • J Brassey
  • C Heneghan
Jefferson T, Spencer E, Brassey J, Heneghan C. Viral cultures for COVID-19
Duration of SARS-CoV-2 Infectivity: When is it Safe to Discontinue Isolation?
  • Jan 2020
  • CLIN INFECT DIS
  • 1249
  • C Rhee
  • S Kanjilal
  • M Baker
  • M Klompas
Rhee C, Kanjilal S, Baker M, Klompas M. Duration of SARS-CoV-2 Infectivity: When is it Safe to Discontinue Isolation? Clin Infect Dis 2020; :ciaa1249.
Predicting Infectious Severe Acute Respiratory Syndrome Coronavirus 2 From Diagnostic Samples
  • Jan 2020
  • CLIN INFECT DIS
  • J Bullard
  • K Dust
  • D Funk
Bullard J, Dust K, Funk D, et al. Predicting Infectious Severe Acute Respiratory Syndrome Coronavirus 2 From Diagnostic Samples. Clin Infect Dis 2020; :ciaa638. 7. Covid-19 ' PCR, x . L ..
Duration of infectiousness and correlation with RT-PCR cycle threshold values in cases of COVID-19
  • May 2020
  • Euro Surveill
  • A Singanayagam
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