Genotyping of Influenza Viruses Using Nucleic Acid Sequencing (code 40513) Notice of Assessment
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1 Genotyping of Influenza Viruses Using Nucleic Acid Sequencing (code 40513) Notice of Assessment June 2013 DISCLAIMER: This document was originally drafted in French by the Institut national d'ecellence en santé et en services sociau (INESSS), and that version can be consulted at It was translated into English by the Canadian Agency for Drugs and Technologies in Health (CADTH) with INESSS s permission. INESSS assumes no responsibility with regard to the quality or accuracy of the translation. While CADTH has taken care in the translation of the document to ensure it accurately represents the content of the original document, CADTH does not make any guarantee to that effect. CADTH is not responsible for any errors or omissions or injury, loss, or damage arising from or relating to the use (or misuse) of any information, statements, or conclusions contained in or implied by the information in this document, the original document, or in any of the source documentation.
2 1 GENERAL INFORMATION 1.1 Requestor: CHUQ - Centre hospitalier de l Université Laval. 1.2 Application Submitted: July 30, Notice Issued: April 12, Note: This notice is based on the scientific and commercial information (submitted by the requestor[s]) and on a complementary review of the literature according to the data available at the time that this test was assessed by INESSS. 2 TECHNOLOGY, COMPANY, AND LICENCE(S) 2.1 Name of the Technology Nucleic acid sequencing 1 of influenza viruses 2 using the traditional Sanger sequencing method (Sanger et al., 1977), also referred to as the dideoy procedure. 2.2 Brief Description of the Technology Sanger sequencing, which has been the most common sequencing method since 1977 (Shendure et al., 2011), is well established, namely for the characterization of the influenza A virus (Shinde et al., 2009; Hiromoto et al., 2000; Lindstrom et al., 1998). It comprises the following steps: a) selection of a specific primer complementary to a single strand of an amplified DNA template (through PCR or RT-PCR); b) incubation of the template, the primer and the DNA polymerase in the presence of unlabelled deoynucleotides (dntps) and dideoynucleotides (ddntps) labelled with a single fluorophore; c) polymerization of the molecules continues until the integration of a ddntp stops the chain (random termination for each molecule); d) the sequencing products of different sizes are purified based on their molecular weight through capillary electrophoresis; 1 Sequencing is used to determine the order of the nitrogenous bases that make up nucleic acids. 2 Three types of influenza virus (A, B, and C) are known, including two main types (A and B). There are several sub-types of the influenza A virus and they are named based on two proteins found at the surface: hemagglutinin (H) and neuraminidase (N). Unlike the influenza A virus, which infects several species, the influenza B virus infects mostly humans (Sheu et al., 2010). 1
3 e) a laser scans the capillary and stimulates the fluorescent dye of the terminal ddntp of each size-separated fragment; f) the sequence of the fluorescent signals sent is analyzed, which in turn allows deduction of the nucleotide sequence. Figure 1: Schematic Representation of Dideoy Sequencing Image courtesy of the National Forensic Science Technology Center, from NIJ s DNA analyst training program (figure from the NFSTC website, available at: Company or Developer: No information provided in the application. 2.4 Licence(s): No information provided in the application. 2.5 Patent, If Any: No information provided in the application. 2.6 Approval Status (Health Canada, FDA): No information provided in the application. 2.7 Weighted Value: 54.0, according to the information provided in the application. 3 CLINICAL INDICATIONS, PRACTICE SETTINGS, AND TESTING PROCEDURES 3.1 Targeted Patient Group According to the information provided in the application, the target patient population consists of patients with positive RT-PCR results for the influenza virus and for whom the antiviral treatment has failed (after five days). When a first-line procedure used to detect common mutations (e.g., pyrosequencing) fails, the Sanger sequencing method could be used for sequencing the entire viral genome. 3.2 Targeted Disease(s) Influenza viruses are major respiratory pathogens that cause the hospitalization of more than 200,000 persons annually in the United States (Monto, 2009) and that are responsible for the death of approimately half a million individuals worldwide (Englund, 2002). The genome of these viruses is made up of single-stranded RNA and their mutation is caused by the fact that their RNA polymerase makes a large number of mistakes during replication (Lauring and Andino, 2010; De la Torre and Holland 1990; Parvin et al., 1986). Several virus populations are thereby created when infection occurs and, in the presence of antiviral drugs, the only viruses that survive are those that have mutations conferring drug resistance (Mas et al., 2010; Lackenby et al., 2008). According to the information provided in the application, approimately 1% to 2% of influenza virus strains are resistant to oseltamivir and most are resistant to amantadine. During the flu season in Canada, up to 26% of influenza A H1N1 virus isolates were resistant to oseltamivir (Eshaghi et al., 2
4 2009). There do not appear to be any significant differences, in symptoms or severity, between infections caused by viruses that are resistant to oseltamivir and those that are susceptible (Ciancio et al., 2009; Dharan et al., 2009). 3.3 Number of Patients Targeted The annual provincial volume is undetermined, according to the information provided in the application. 3.4 Medical Specialties Involved (and Other Professions, If Any) Microbiology and infectious diseases. 3.5 Testing Procedure According to the information provided in the application, the sequencing procedure will involve patients with positive NAAT (RT-PCR) results for any influenza virus after five days of antiviral treatment. The analyses will be conducted at the requestor s laboratory once a week, upon which there will be a 96-hour delay in communicating results. 4 TECHNOLOGY BACKGROUND 4.1 Nature of the Diagnostic Technology Unique or complementary to phenotypic testing. 4.2 Brief Description of the Current Technological Contet According to the ISIRV 3, genotyping 4 of the influenza virus is an accepted method for monitoring susceptibility to amantadine, whether it is through sequencing of the M gene using Sanger sequencing or through pyrosequencing of the region coding for the transmembrane domain where the five known mutations of the M2 protein are located. Phenotypic assays (e.g., lytic plaque reduction assay on cultured cells) can also be used. For susceptibility to oseltamivir, the traditional phenotypic (or functional, to be precise) method is the neuraminidase inhibition test; this test uses chemiluminescence or fluorescence. For genotyping, this method would not allow for the conclusive determination of susceptibility to neuraminidase inhibitors, as the resistance of these antiviral treatments is specific to the drug itself, as well as to the type and sub-type of influenza virus 5. The best precautionary approach to assessing susceptibility to neuraminidase inhibitors consists of using phenotypic assays 6 and confirming results using genotypic assays 7 such as Sanger sequencing or pyrosequencing (Deyde et al., 2010). Furthermore, several other methods, including RT-PCR for the H275Y mutation (Nakauchi et al., 2011; Mahony et al., 2010), are being developed in order to better address the needs of hospital laboratories (speed, simplicity, etc.). 3 International Society for Influenza and other Respiratory Virus Diseases (ISIRV). Frequently Asked Questions Methodology (website). Available at: 4 A PCR-based nucleic acid amplification step precedes genotyping per se (Sanger sequencing or pyrosequencing) (Okomo-Adhiambo et al., 2013). 5 Although we are aware of certain neuraminidase mutations that lead to resistance or lower susceptibility (H275Y for seasonal influenza A H1N1 or 2009 (pandemic); E119V, I222V, or R292K for influenza A H3N2; R152K, D198E or I222T for influenza B), such resistance mechanisms are not fully known and other mutations, which have not been defined yet, could emerge. 6 Phenotypic assays can detect resistance that is the result of known or unknown mutations (Okomo-Adhiambo et al., 2013). 7 Unlike phenotypic assays, genotypic assays can detect only known mutations (Okomo-Adhiambo et al., 2013). 3
5 4.3 Brief Description of the Advantages Cited for the New Technology By comparing the sequence under investigation with a wild-type sequence, Sanger sequencing can identify all mutations, both known and unknown. First-generation sequencers allow sequencing up to 1,000 nucleotides while automating steps in Sanger sequencing steps that are too timeconsuming (separation of fragments, analysis, etc.) (Shendure et al., 2011). 4.4 Cost of Technology and Options: No analysis has been conducted to date. 5 EVIDENCE 5.1 Clinical Relevance Other Tests Replaced: Does not apply Diagnostic, Prognostic, or Therapeutic Value Sanger sequencing is the reference method for sequencing the viral genome and thereby detecting mutations that may or may not be related to antiviral drug resistance. However, the procedure may not be fast enough to be considered appropriate in a clinical contet, allowing for the treatment to be adjusted based on the results. 5.2 Clinical Validity The literature review did not identify any studies on the clinical validity of the analysis in terms of sensitivity, specificity, and predictive value. 5.3 Analytical (or Technical) Validity COMPONENT PRESENCE ABSENCE NOT APPLICABLE Repeatability Reproducibility Analytical Sensitivity Analytical Specificity Matri Effect Concordance Correlation Between Test and Indicator Others Based on Test Type 4
6 Sensitivity and Specificity Sanger sequencing is the reference method. However, as far as sensitivity is concerned, this method cannot detect a virus population representing less than 20% to 25% of any mi (Chen et al., 2011; Wang et al., 2007). 5.4 Recommendations for Listing in Other Jurisdictions No recommendation has been found. 6 ANTICIPATED OUTCOMES OF INTRODUCING THE TEST 6.1 Impact on Material and Human Resources: Not assessed. 6.2 Economic Consequences of Introducing Test Into Quebec s Health Care and Social Services System: Not assessed. 6.3 Main Organizational, Ethical, and Other (Social, Legal, Political) Issues: Ecept for the initial 30 to 50 base pairs (Pourmand et al., 2006), the sequencing of all genes by the Sanger method is accurate for the detection of alterations in the viral genome, which makes it the preferred method for identifying new or known alterations that may be associated with antiviral resistance. This is what distinguishes Sanger sequencing, as pyrosequencing, for instance, cannot sequence an entire genome, nor can it identify unknown mutations. However, it must be noted that Sanger sequencing is not a reliable method for discriminating mied virus populations, as it is unable to detect a virus population in amounts of less than 20% to 25% (Chen et al., 2011; Wang et al., 2007). On the other hand, pyrosequencing has the ability to detect population subsets of 5% (Deng et al., 2011). Moreover, rapid detection of antiviral resistance is paramount in a clinical setting in order to inform proper patient care (Bao et al., 2011). However, according to the narrative review conducted by Okomo-Adhiambo et al. (2013), Sanger sequencing is time-consuming, labor-intensive, and costly. Indeed, even when sequencing is automated, as is the case with the protocol used by Suppiah et al. (2011), there are still purification steps required to isolate viruses (e.g., by cell culture), RNA, and amplification products. Additionally, it has recently been recommended that the viruses analyzed be directly recovered from clinical samples rather than going through a purification process through cell culture in a laboratory setting, since in vitro replication may differ from the actual process that takes place within the human body leading to the selection of viral particles that do not reflect reality, etc.) (Okomo-Adhiambo et al., 2010; Hurt et al., 2009). 5
7 7 INESSS NOTICE IN BRIEF Genotyping of Influenza Viruses Using Nucleic Acid Sequencing (Code 40513) Status of the Diagnostic Technology: Established Innovative Eperimental (for research purposes only) Replacement for technology:, which becomes obsolete INESSS Recommendation: Keep test in the Inde Remove test from the Inde Reassess test Additional Recommendation: Draw connection with listing of drugs, if companion test Production of an optimal use manual Production of indicators, when monitoring is required 6
8 REFERENCES Bao JR, Huard TK, Piscitelli AE, Tummala PR, Aleemi VE, Coon SL, et al. Reverse-transcription polymerase chain reaction/pyrosequencing to characterize neuraminidase H275 residue of influenza A 2009 H1N1 virus for rapid and specific detection of the viral oseltamivir resistance marker in a clinical laboratory. Diagn Microbiol Infect Dis 2011;71(4): Chen LF, Dailey NJ, Rao AK, Fleischauer AT, Greenwald I, Deyde VM, et al. Cluster of oseltamivir-resistant 2009 pandemic influenza A (H1N1) virus infections on a hospital ward among immunocompromised patients North Carolina, J Infect Dis 2011;203(6): Ciancio BC, Meerhoff TJ, Kramarz P, Bonmarin I, Borgen K, Boucher CA, et al. Oseltamivir-resistant influenza A(H1N1) viruses detected in Europe during season had epidemiologic and clinical characteristics similar to co-circulating susceptible A(H1N1) viruses. Euro Surveill 2009;14(46). De la Torre JC et Holland JJ. RNA virus quasispecies populations can suppress vastly superior mutant progeny. J Virol 1990;64(12): Deng YM, Caldwell N, Hurt A, Shaw T, Kelso A, Chidlow G, et al. A comparison of pyrosequencing and neuraminidase inhibition assays for the detection of oseltamivir-resistant pandemic influenza A(H1N1) 2009 viruses. Antiviral Res 2011;90(1): Deyde VM, Sheu TG, Trujillo AA, Okomo-Adhiambo M, Garten R, Klimov AI, Gubareva LV. Detection of molecular markers of drug resistance in 2009 pandemic influenza A (H1N1) viruses by pyrosequencing. Antimicrob Agents Chemother 2010;54(3): Dharan NJ, Gubareva LV, Meyer JJ, Okomo-Adhiambo M, McClinton RC, Marshall SA, et al. Infections with oseltamivir-resistant influenza A(H1N1) virus in the United States. JAMA 2009;301(10): Englund JA. Antiviral therapy of influenza. Semin Pediatr Infect Dis 2002;13(2): Eshaghi A, Bolotin S, Burton L, Low DE, Mazzulli T, Drews SJ. Genetic microheterogeneity of emerging H275Y influenza virus A (H1N1) in Toronto, Ontario, Canada from the respiratory season. J Clin Virol 2009;45(2): Hiromoto Y, Yamazaki Y, Fukushima T, Saito T, Lindstrom SE, Omoe K, et al. Evolutionary characterization of the si internal genes of H5N1 human influenza A virus. J Gen Virol 2000;81(Pt 5): Hurt AC, Holien JK, Parker M, Kelso A, Barr IG. Zanamivir-resistant influenza viruses with a novel neuraminidase mutation. J Virol 2009;83(20): Lackenby A, Democratis J, Siqueira MM, Zambon MC. Rapid quantitation of neuraminidase inhibitor drug resistance in influenza virus quasispecies. Antivir Ther 2008;13(6): Lauring AS et Andino R. Quasispecies theory and the behavior of RNA viruses. PLoS Pathog 2010;6(7):e Lindstrom S, Endo A, Sugita S, Pecoraro M, Hiromoto Y, Kamada M, et al. Phylogenetic analyses of the matri and non-structural genes of equine influenza viruses. Arch Virol 1998;143(8): Mahony JB, Chong S, Luinstra K, Petrich A, Smieja M. Development of a novel bead-based multiple PCR assay for combined subtyping and oseltamivir resistance genotyping (H275Y) of seasonal and pandemic H1N1 influenza A viruses. J Clin Virol 2010;49(4): Mas A, Lopez-Galindez C, Cacho I, Gomez J, Martinez MA. Unfinished stories on viral quasispecies and Darwinian views of evolution. J Mol Biol 2010;397(4):
9 Monto AS. The risk of seasonal and pandemic influenza: Prospects for control. Clin Infect Dis 2009;48(Suppl 1):S20-5. Nakauchi M, Ujike M, Obuchi M, Takashita E, Takayama I, Ejima M, et al. Rapid discrimination of oseltamivir-resistant 275Y and -susceptible 275H substitutions in the neuraminidase gene of pandemic influenza A/H1N virus by duple one-step RT-PCR assay. J Med Virol 2011;83(7): Okomo-Adhiambo M, Sheu TG, Gubareva LV. Assays for monitoring susceptibility of influenza viruses to neuraminidase inhibitors. Influenza Other Respi Viruses 2013;7(Suppl 1):44-9. Okomo-Adhiambo M, Nguyen HT, Sleeman K, Sheu TG, Deyde VM, Garten RJ, et al. Host cell selection of influenza neuraminidase variants: Implications for drug resistance monitoring in A(H1N1) viruses. Antiviral Res 2010;85(2): Parvin JD, Moscona A, Pan WT, Leider JM, Palese P. Measurement of the mutation rates of animal viruses: Influenza A virus and poliovirus type 1. J Virol 1986;59(2): Pourmand N, Diamond L, Garten R, Erickson JP, Kumm J, Donis RO, Davis RW. Rapid and highly informative diagnostic assay for H5N1 influenza viruses. PLoS One 2006;1:e95. Sanger F, Nicklen S, Coulson AR. DNA sequencing with chain-terminating inhibitors. Proc Natl Acad Sci U S A 1977;74(12): Shendure JA, Porreca GJ, Church GM, Gardner AF, Hendrickson CL, Kieleczawa J, Slatko BE. Overview of DNA sequencing strategies. Curr Protoc Mol Biol 2011;Chapter 7:Unit7.1. Sheu TG, Deyde VM, Garten RJ, Klimov AI, Gubareva LV. Detection of antiviral resistance and genetic lineage markers in influenza B virus neuraminidase using pyrosequencing. Antiviral Res 2010;85(2): Shinde V, Bridges CB, Uyeki TM, Shu B, Balish A, Xu X, et al. Triple-reassortant swine influenza A (H1) in humans in the United States, N Engl J Med 2009;360(25): Suppiah J, Yusof MA, Othman KA, Saraswathy TS, Thayan R, Kasim FM, et al. Monitoring of the h275y mutation in pandemic influenza A(H1N1) 2009 strains isolated in Malaysia. Southeast Asian J Trop Med Public Health 2011;42(1): Wang C, Mitsuya Y, Gharizadeh B, Ronaghi M, Shafer RW. Characterization of mutation spectra with ultradeep pyrosequencing: Application to HIV-1 drug resistance. Genome Res 2007;17(8):
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