Meticulous plasma isolation is essential to avoid false low-level viraemia in Roche Cobas HIV-1 viral load assays
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1 Meticulous plasma isolation is essential to avoid false low-level viraemia in Roche Cobas HIV-1 viral load assays Virginie Mortier, Leen Vancoillie, Kenny Dauwe, Delfien Staelens, Els Demecheleer, Marlies Schauvliege, Sylvie Dinakis, Tom Van Maerken, Géraldine Dessilly, Jean Ruelle, Chris Verhofstede Antiviral Therapy 2017; /IMP3203 Submission date 21st August 2017 Acceptance date 11th October 2017 Publication date 24th October 2017 This provisional PDF matches the article and figures as they appeared upon acceptance. Copyedited and fully formatted PDF and full text (HTML) versions will be made available soon. For information about publishing your article in Antiviral Therapy go to International Medical Press ISSN
2 Short communication Meticulous plasma isolation is essential to avoid false low-level viraemia in Roche Cobas HIV-1 viral load assays Virginie Mortier 1, Leen Vancoillie 1, Kenny Dauwe 1, Delfien Staelens 1, Els Demecheleer 1, Marlies Schauvliege 1, Sylvie Dinakis 1, Tom Van Maerken 2, Géraldine Dessilly 3, Jean Ruelle 3, Chris Verhofstede 1 * 1 AIDS Reference Laboratory, Department of Clinical Chemistry, Microbiology and Immunology, Ghent University, Ghent, Belgium 2 Department of Pediatrics and Medical Genetics, Ghent University, Ghent, Belgium 3 AIDS Reference Laboratory, Université Catholique de Louvain, Medical Microbiology Unit, Brussels, Belgium *Corresponding author chris.verhofstede@ugent.be Abstract Background: Pre-analytical sample processing is often overlooked as a potential cause of inaccurate assay results. Here we demonstrate how plasma, extracted from standard EDTA- containing blood collection tubes, may contain traces of blood cells consequently resulting in a false low-level HIV-1 viral load when using Roche Cobas HIV-1 assays. Methods: The presence of human DNA in Roche Cobas 4800 RNA extracts and in RNA extracts from the Abbott HIV-1 RealTime assay was assessed by quantifying the human albumin gene by means of qpcr. RNA was extracted from plasma samples before and after an additional centrifugation and tested for viral load and DNA contamination. The relation between total DNA content and viral load was defined. Results: Elevated concentrations of genomic DNA were detected in 28 out of 100 Cobas 4800 extracts and were significantly more frequent in samples processed outside of the Aids Reference Laboratory. An association between genomic DNA presence and spurious low-level viremia results was demonstrated. Supplementary centrifugation of plasma before RNA extraction eliminated the contamination and the false viremia. Conclusions: Plasma isolated from standard EDTA-containing blood collection tubes may contain traces of HIV DNA leading to false viral load results above the clinical cut-off. Supplementary centrifugation of plasma before viral load analysis may eliminate the occurrence of this spurious low-level viremia. Accepted 11 October 2017, published online 24 October 2017 Running head: False low-level viremia with Roche HIV-1 Cobas viral load assays
3 Introduction Viral load testing is standard of care for follow-up of HIV-infected patients on therapy [1]. Assays for viral load determination, in general, comprise an automated extraction of viral RNA from blood plasma followed by real-time reverse transcription PCR. In the viral load assays developed by Roche (Roche, Pleasanton, California), the RNA extraction procedure is based on silica binding and is not RNA specific. In contrast, the Abbott HIV-1 RealTime assay (Abbott, Chicago, Illinois) uses a magnetic microparticle extraction technology that is RNA-specific. A false low viral load in the Roche assay can arise from DNA contamination in plasma, as has been reported for plasma isolated after freezing from Plasma Preparation Tubes with a barrier gel (PPT-tubes) [2 4]. The freezing affected the barrier function of the gel, inducing leakage of blood cells in the plasma. False positive viral load results due to presence of viral DNA in plasma isolated from standard ethylene diamine tetra-acetic acid (EDTA)-containing blood collection tubes, have also been observed though occasionally [3,5]. Soon after implementing the Roche Cobas 4800 instrument for RNA extraction, we noticed lowlevel viremia in 4 successively processed samples (440, 329, 250, and 46 copies (c)/ml) collected from patients on long-term suppressive antiretroviral therapy. Analysis of a follow-up sample failed to confirm the detectable viremia. No direct indications for cross-contamination or technical errors were found. Therefore, the Cobas 4800 extracts of these 4 samples and 96 additional arbitrarily chosen Cobas 4800 extracts were investigated for the presence of DNA. Although all plasma samples originated from standard EDTA tubes, viral DNA was detected in 28 of the 100 Cobas RNA extracts and their presence was clearly associated with false low-level viremia. Methods Plasma isolation Venous blood collected in EDTA-containing blood collection devices was centrifuged at 1900 g for 10 minutes within 24h after collection and plasma was immediately transferred to a clean vial for storage at - 20 C. For about 70% of the samples analyzed for viral load in the Aids Reference Laboratory (ARL) of Ghent University, plasma isolation is performed on-site. The remaining 30% are plasma samples isolated at the hospital s core laboratory (CL) or in a peripheral laboratory (PL). As required by the ISO/EN 15189:2012 accreditation, all external partners are provided with standard operating procedures for blood and plasma collection including a statement on the need to centrifuge the blood within 24 h of collection and to transfer the plasma immediately after centrifugation. Plasma isolated at the ARL is transferred to barcode-labeled 4.5 ml Sarstedt tubes suitable for use on the Cobas Plasma isolated at the CL or in a PL is thawed just before initiation of the viral load determination and then transferred to a Sarstedt tube.
4 Viral load analysis Viral load measurements were performed with the Cobas 4800 system (Roche). For the purpose of this study, a selection of samples was also tested with the Abbott RealTime PCR HIV-1 m2000 viral load run at the ARL of the Université Catholique de Louvain, Brussels. Quantification of total human DNA Presence of human genomic DNA was assessed by quantitative (q)pcr for the human albumin gene using the method described by Gault et al. [6]. The assay was run on the CobasZ480 Lightcycler (Roche). Quantification Cycle (Cq) values were used as semi-quantitative indicators of DNA content. A Cq value of < 30 was considered as indicative of above average DNA concentrations. Statistical analysis Cq values were compared using Chi square test implemented in SPSS Ethics statement All samples were anonymized left-over plasma samples from routine viral load testing. Patients provided informed consent for the use of their remaining material. Results Detection of human DNA in Cobas 4800 extracts Human albumin qpcr was run on 2 l aliquots of 100 Cobas 4800 RNA extracts, comprising 48 extracts from plasma samples isolated in the ARL, 19 from samples isolated in the CL and 33 from samples isolated in a PL. The viral load was < 20 copies (c)/ml for 53 samples, between 20 and 1000 c/ml for 40 samples and > 1000 c/ml for 7 samples. Figure 1 shows the albumin Cq values for the samples ordered by site of processing. Above average DNA contents (Cq < 30) were found for 1/48 (2.1%) of samples processed at the ARL, 14/19 (73.7%) of samples processed at the CL and 13/33 (39.4%) of samples processed in a PL. The Cq values for the samples processed at the CL or PL were significantly lower than those for samples processed at the ARL (p < 0.001). Association between DNA presence and viral load Twenty-five plasma samples with a viral load of < 1000 c/ml and sufficient left-over volume for additional testing were selected. The qpcr of the original Cobas 4800 extracts of these 25 samples showed high albumin DNA content in 11 (mean Cq 23.7; range ) and low DNA content in 14 (mean Cq 31.5; range ). The rest plasma was thawed and submitted to an additional centrifugation at 1900 g for 10 minutes. The supernatant plasma was then carefully transferred to a clean tube and retested for viral load and for the presence of human albumin DNA. The albumin Cq values of the Cobas 4800 extracts
5 increased to a mean of 30.0 (range ) for the 11 samples with high initial DNA content and remained stable at a mean of 32.0 (range ) for the 14 samples with low DNA content (Figure 2). At the same time, the viral load of the 11 samples with high DNA content dropped from a mean of c/ml (range ) to < 20 c/ml for 10 samples and 31 c/ml for one sample (Figure 3A). The 14 samples with low DNA content showed no change in mean viral load (mean c/ml, range before centrifugation versus c/ml, range < after centrifugation) (Figure 3B), but the viral load dropped to below detection level for the 3 samples with the lowest initial values (61, 49 and 32 c/ml). To further confirm the vulnerability of the Roche viral load assay for viral DNA, the reversion transcription step was removed from the real-time PCR program in the CobasZ480 Lightcycler. A selection of 15 plasma samples, 11 with and 4 without evidence of DNA contamination were tested following the standard procedure for viral load measurement but using the modified PCR cycling program. Ten of the 11 samples with evidence of DNA contamination were reported as detectable while all 4 samples without evidence of DNA contamination were reported as undetectable, clearly proving that presence of viral DNA alone is sufficient for false viral load results. Abbott viral load determination For 17 of the 25 samples, six with high and 11 with low DNA content, sufficient initial plasma was available for testing with the Abbott viral load assay. Albumin qpcr Cq values for the Abbott RNA extracts were high (mean 31.1, range ), supporting absence of DNA contamination in the extracts obtained with this method, even for the samples with high plasma DNA content. The six samples with high DNA content and a false low-level viremia in the Roche assay all had a viral load of < 40 c/ml in the Abbott assay (Figure 3A). For the 11 samples with low DNA content in plasma, the Abbott viral load was detectable in five (with loads of 389, 123, 93, 89 and 46 c/ml versus loads of 490, 275, 107, 204 and 87 c/ml with the Roche assay respectively) and undetectable (< 40 c/ml) in six (compared to loads of 126, 36, 32, 62, 49 and 32 c/ml with Roche) (Figure 3B). Discussion When determining the HIV-1 viral load in plasma obtained from blood samples, pre-analytical steps are of utmost importance although easily overlooked. Falsely elevated HIV-1 viral load results due to contamination of plasma with viral DNA have been described for PPT collection tubes, but the potential risk of viral DNA presence in plasma collected from standard EDTA tubes is generally assumed to be rare [3,5]. In our laboratory, the Roche Cobas Ampliprep extractor has been in use for HIV-1 viral load analysis since Our standard procedures at that time prescribed an additional centrifugation of the primary plasma vials after thawing and before transferring the needed plasma volume to the Cobas Ampliprep specific S-tubes. With the introduction of Cobas 4800, an instrument that accepts primary vials, the additional centrifugation step was omitted. From the results described here, we now realize that this
6 procedural change resulted in occasional spurious viral load results due to contamination of the plasma with blood cells, cell debris, or nuclei containing HIV DNA. It is important to note here that the manufacturers instructions for use of Cobas 4800 do not include specific recommendations for plasma handling. An important observation was that the extent of DNA contamination differed between sample handling laboratories. It was almost negligible when plasma was isolated by technicians familiar with viral load analysis but occurred frequently in samples processed outside of the Aids Reference Laboratory. Although these laboratories were all accredited and the personnel was well-trained, the technicians may be less aware of the potential consequences associated with small traces of blood cells in the plasma. We believe that well-meant attempts to recuperate a maximum volume of plasma were the most likely cause of the contamination. The impact of cellular contamination on the viral load results will depend on the amount of contaminating cells, but also on the number of HIV-infected cells. DNA contamination will, therefore, not always result in a detectable viral load and this may complicate identification of the problem. The Abbott RealTime HIV-1 assay uses a RNA specific magnetic microparticle extraction technology that proved to be insensitive to the DNA contamination in PPT tubes [1]. We showed that all samples with detected DNA contamination and a false viral load result in the Roche assay, indeed tested negative with Abbott. The slightly higher number of undetectable viral loads found with Abbott most probably results from the lower sensitivity of this assay compared to the Roche test [7 10], although one may question to what extent DNA contamination may have impacted the results of the studies that compared the sensitivity of both assays. We present observations from a routine clinical laboratory that are, by definition, retrospective in nature and limited by sample availability. Nevertheless, the results clearly reveal that Roche viral load assays are prone to spurious results. A viral load resulting from unintentional plasma contamination with blood cells may even exceed the limit of 200 c/ml that is generally considered as clinically relevant [11,12]. Additional centrifugation of plasma before advancing to Roche HIV-1 viral load analysis must be recommended. Acknowledgements The Aids Reference Laboratories in Belgium are supported by the Belgian Ministry of Social Affairs through a fund within the Health Insurance System. Disclosures The authors declare that they do not have any commercial or other associations that might pose a conflict of interest to the work presented.
7 References 1. Salimnia H, Moore EC, Crane LR, Macarthur RD, Fairfax MR. Discordance between viral loads determined by Roche COBAS AMPLICOR human immunodeficiency virus type 1 monitor (version 1.5) standard and ultrasensitive assays caused by freezing patient plasma in centrifuged Becton-Dickinson vacutainer brand plasma preparation tubes. J Clin Microbiol 2005; 43: Stosor V, Palella FJ, Berzins B, et al. Transient viremia in HIV-infected patients and use of plasma preparation tubes. Clin Infect Dis 2005; 41: Wan H, Seth A, Rainen L, Fernandes H. Coamplification of HIV-1 proviral DNA and viral RNA in assays used for quantification of HIV-1 RNA. J Clin Microbiol 2010; 48: Cloherty G, Swanson P, Lucic D, et al. Clinical implications of elevated HIV-1 viral load results obtained from samples stored frozen in vacutainer plasma preparation tubes. J Virol Methods 2014; 204: Kran AM, Jonassen TO, Sannes M, et al. Overestimation of human immunodeficiency virus type 1 load caused by the presence of cells in plasma from plasma preparation tubes. J Clin Microbiol 2009; 47: Gault E, Michel Y, Dehee A, Belabani C, Nicolas JC, Garbarg-Chenon A. Quantification of human cytomegalovirus DNA by real-time PCR. J Clin Microbiol 2001; 224: Amendola A, Marsella P, Bloisi M, Forbici F, Angeletti C, Capobianchi MR. Ability of two commercially available assays (Abbott RealTime HIV-1 and Roche Cobas AmpliPrep/Cobas TaqMan HIV-1 Version 2.0) to quantify low HIV-1 RNA Levels (<1,000 copies/milliliter): comparison with clinical samples and NIBSC working reagent for nucleic acid testing assays. J Clin Microbiol 2014; 52: Naeth G, Ehret R, Wiesmann F, Braun P, Knechten H, Berger A. Comparison of HIV-1 viral load assay performance in immunological stable patients with low or undetectable viremia. Med Microbiol Immunol (Berl) 2013; 202: Adachi D, Benedet M, Tang JW, Taylor GD. Comparative evaluation of Roche s COBAS Ampliprep/COBAS TaqMan HIV-1 Test v2.0 and Abbott s RealTime m2000sp/rt HIV-1 assay on PPTs and EDTA samples. J Clin Virol 2014; 60: Leierer G, Grabmeier-Pfistershammer K, Steuer A, et al. Factors associated with low-level viraemia and virological failure: Results from the Austrian HIV Cohort Study. PLoS One 2015; 10:e Duncan Churchill LW, Ahmed N, Angus B, et al. British HIV Association guidelines for the treatment of HIV-1-positive adults with antiretroviral therapy Available at: Accessed 17 July Leierer G, Grabmeier-Pfistershammer K, Steuer A, et al. A single quantifiable viral load is predictive of virological failure in Human Immunodeficiency Virus (HIV)- infected patients on combination antiretroviral therapy: The Austrian HIV Cohort Study. Open Forum Infect Dis 2016; 3:ofw089. Figures Figure 1. Influence of the sample processing laboratory on the human albumin DNA concentration of Cobas 4800 RNA extracts. ARL: Aids Reference Laboratory; CL: Hospital Core Laboratory; PL: Peripheral laboratory; open circles: viral load <20 c/ml; grey circles: viral load between 20 and 1000 c/ml; black circles: viral load >1000 c/ml.
8 Figure 2. Effect of extra plasma centrifugation on the human albumin DNA concentration of Cobas 4800 RNA extracts. Open circles: samples with low pre-centrifugation DNA content (albumin qpcr Cq >30.0); closed circles:samples with high pre-centrifugation DNA content (albumin qpcr Cq <30.0). Figure 3. Impact of an additional plasma centrifugation on the viral load results obtained with the test of Roche and Abbott. Figure 3A, samples with high pre-centrifugation DNA content (albumin qpcr Cq <30.0) Figure 3B, samples with low pre-centrifugation DNA content (albumin qpcr Cq >30.0) Open circles: samples with undetectable viral load (Roche, <20 c/ml; Abbott, <40 c/ml); closed circles: samples with detectable viral load.
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