Comparative evaluation of commercially available manual and automated nucleic acid extraction methods for rotavirus RNA detection in stools

Journal of Virological Methods

Volumn 194, Issue 1-2, 2013, Pages 242-249

  Esona, Mathew D ^a   McDonald, Sharla ^a   Kamili, Shifaq ^a,b   Kerin, Tara ^a   Gautam, Rashi ^a,b   Bowen, Michael D ^a  

^a NATIONAL CENTER FOR IMMUNIZATION AND RESPIRATORY DISEASES   (United States)

^b ATLANTA RESEARCH AND EDUCATION FOUNDATION   (United States)

Author keywords

Extraction methods; Quantitative real time RT PCR; Rotavirus; Stool

Indexed keywords

NUCLEIC ACID; VIRUS RNA;

ARTICLE; AUTOMATION; CONTROLLED STUDY; DILUTION; ENZYME IMMUNOASSAY; FECES ANALYSIS; INTERMETHOD COMPARISON; MEDICAL DEVICE; NONHUMAN; PRIORITY JOURNAL; QUANTITATIVE ANALYSIS; REFERENCE VALUE; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; RNA ANALYSIS; RNA EXTRACTION; RNA PURIFICATION; ROTAVIRUS; SEPARATION TECHNIQUE;

EXTRACTION METHODS; QUANTITATIVE REAL-TIME RT-PCR; ROTAVIRUS; STOOL;

AUTOMATION, LABORATORY; FECES; GASTROENTERITIS; HUMANS; MOLECULAR DIAGNOSTIC TECHNIQUES; RNA, VIRAL; ROTAVIRUS; ROTAVIRUS INFECTIONS; SPECIMEN HANDLING; VIROLOGY;

EID: 84884925845     PISSN: 01660934     EISSN: 18790984     Source Type: Journal    
DOI: 10.1016/j.jviromet.2013.08.023     Document Type: Article

References (54)

1. Abu Al-Soud W., Radstrom P. Capacity of nine thermostable DNA polymerases to mediate DNA amplification in the presence of PCR-Inhibiting samples. Appl. Environ. Microbiol. 1998, 64:3748-3753.
2. Baert L., Uyttendaele M., Debevere J. Evaluation of two viral extraction methods for the detection of human noroviruses in shellfish with conventional and real-time reverse transcriptase PCR. Lett. Appl. Microbiol. 2007, 44:106-111.
3. Banyai K., Mijatovic-Rustempasic S., Hull J.J., Esona M.D., Freeman M.M., Frace A.M., Bowen M.D., Gentsch J.R. Sequencing and phylogenetic analysis of the coding region of six common rotavirus strains: evidence for intragenogroup reassortment among co-circulating G1P[8] and G2P[4] strains from the United States. J. Med. Virol. 2011, 83:532-539.
4. Chiu C.H., Ou J.T. Rapid identification of Salmonella serovars in feces by specific detection of virulence genes, invA and spvC, by an enrichment broth culture-multiplex PCR combination assay. J. Clin. Microbiol. 1996, 34:2619-2622.
5. Dalesio N., Marsiglia V., Quinn A., Quinn T., Gaydos Charlotte A. Performance of the MagNA pure LC robot for extraction of Chlamydia trachomatis and Neisseria gonorrhoeae DNA from urine and swab specimens. J. Clin. Microbiol. 2004, 42:3300-3302.
6. Das B.K., Gentsch J.R., Cicirello H.G., Woods P.A., Gupta A., Ramachandran M., Kumar R., Bhan M.K., Glass R.I. Characterization of rotavirus strains from newborns in New Delhi, India. J. Clin. Microbiol. 1994, 32:1820-1822.
7. Doan Y.H., Nakagomi T., Cunliffe N.A., Pandey B.D., Sherchand J.B., Nakagomi O. The occurrence of amino acid substitutions D96N and S242N in VP7 of emergent G2P[4] rotaviruses in Nepal in 2004-2005: a global and evolutionary perspective. Arch. Virol. 2011, 156:1969-1978.
8. Donato C.M., Ch'ng L.S., Boniface K.F., Crawford N.W., Buttery J.P., Lyon M., Bishop R.F., Kirkwood C.D. Identification of strains of RotaTeq rotavirus vaccine in infants with gastroenteritis following routine vaccination. J. Infect. Dis. 2012, 206:377-383.
9. Dundas N., Leos N., Mitui M., Revell P., Rogers B.B. Comparison of automated nucleic acid extraction methods with manual extraction. J. Mol. Diagn. 2008, 10:311-316.
10. Dundas N., Leos N.K., Mitui M., Revell P., Rogers B.B. Comparison of automated nucleic acid extraction methods with manual extraction. J. Mol. Diagn. 2008, 10:311-316.
11. Esona M.D., Foytich K., Wang Y., Shin G., Wei G., Gentsch J.R., Glass R.I., Jiang B. Molecular characterization of human rotavirus vaccine strain CDC-9 during sequential passages in Vero cells. Hum. Vaccine 2010, 6:247-253.
12. Esona M.D., Mijatovic-Rustempasic S., Conrardy C., Tong S., Kuzmin I.V., Agwanda B., Breiman R.F., Banyai K., Niezgoda M., Rupprecht C.E., Gentsch J.R., Bowen M.D. Reassortant group A rotavirus from straw-colored fruit bat (Eidolon helvum). Emerg. Infect. Dis. 2010, 16:1844-1852.
13. Estes M., Kapikian A. Rotaviruses. Fields Virology 2007, 1917-1974. Kluwer/Lippincott, Williams and Wilkins, Philadelphia, PA. 5th ed. D.M. Knipe, P.M. Howley, D.E. Griffin, R.A. Lamb, M.A. Martin, B. Roizman, S.E. Straus (Eds.).
14. Freeman M.M., Kerin T., Hull J., McCaustland K., Gentsch J. Enhancement of detection and quantification of rotavirus in stool using a modified real-time RT-PCR assay. J. Med. Virol. 2008, 80:1489-1496.
15. Gentsch J.R., Glass R.I., Woods P., Gouvea V., Gorziglia M., Flores J., Das B.K., Bhan M.K. Identification of group A rotavirus gene 4 types by polymerase chain reaction. J. Clin. Microbiol. 1992, 30:1365-1373.
16. Gentsch J.R., Laird A.R., Bielfelt B., Griffin D.D., Banyai K., Ramachandran M., Jain V., Cunliffe N.A., Nakagomi O., Kirkwood C.D., Fischer T.K., Parashar U.D., Bresee J.S., Jiang B., Glass R.I. Serotype diversity and reassortment between human and animal rotavirus strains: Implications for rotavirus vaccine programs. J. Infect. Dis. 2005, 192:S146-S159.
17. Glass R.I., Parashar U.D., Bresee J.S., Turcios R., Fischer T.K., Widdowson M.A., Jiang B., Gentsch J.R. Rotavirus vaccines: current prospects and future challenges. Lancet 2006, 368:323-332.
18. Gouvea V., Glass R.I., Woods P., Taniguchi K., Clark H.F., Forrester B., Fang Z.Y. Polymerase chain reaction amplification and typing of rotavirus nucleic acid from stool specimens. J. Clin. Microbiol. 1990, 28:276-282.
19. Grant L., Esona M., Gentsch J., Watt J., Reid R., Weatherholtz R., Santosham M., Parashar U., O'Brien K. Detection of G3P[3] and G3P[9] rotavirus strains in American Indian children with evidence of gene reassortment between human and animal rotaviruses. J. Med. Virol. 2011, 83:1288-1299.
20. Griffin D.D., Kirkwood C.D., Parashar U.D., Woods P.A., Bresee J.S., Glass R.I., Gentsch J.R. Surveillance of rotavirus strains in the United States: identification of unusual strains. The National Rotavirus Strain Surveillance System collaborating laboratories. J. Clin. Microbiol. 2000, 38:2784-2787.
21. Hale A.D., Green J., Brown D.W.G. Comparison of four RNA extraction methods for the detection of small round structured viruses in faecal specimens. J. Virol. Methods 1996, 57:195-201.
22. Hull J.J., Teel E.N., Kerin T.K., Freeman M.M., Esona M.D., Gentsch J.R., Cortese M.M., Parashar U.D., Glass R.I., Bowen M.D. United States rotavirus strain surveillance from 2005-2008: genotype prevalence before and after vaccine introduction. Pediatr. Infect. Dis. J. 2011, 30:S42-S47.
23. Iturriza Gomara M., Wong C., Blome S., Desselberger U., Gray J. Rotavirus subgroup characterisation by restriction endonuclease digestion of a cDNA fragment of the VP6 gene. J. Virol. Methods 2002, 105:99-103.
24. Jothikumar N., Kang G., Hill V.R. Broadly reactive TaqMan assay for real-time RT-PCR detection of rotavirus in clinical and environmental samples. J. Virol. Methods 2009, 155:126-131.
25. Kok T., Wati S., Bayly B., Devonshire-Gill D., Higgins G. Comparison of six nucleic acid extraction methods for detection of viral DNA or RNA sequences in four different non-serum specimen types. J. Clin. Virol. 2000, 16:59-63.
26. Kreader C.A. Relief of amplification inhibition in PCR with bovine serum albumin or T4 gene 32 protein. Appl. Environ. Microbiol. 1996, 62:1102-1106.
27. Lantz P.G., Matsson M., Wadstrom T., Radstrom P. Removal of PCR inhibitors from human faecal samples through the use of an aqueous two-phase system for sample preparation prior to PCR. J. Microbiol. Methods 1997, 28:159-167.
28. Lim D.V., Simpson J.M., Kearns E.A., Kramer M.F. Current and developing technologies for monitoring agents of bioterrorism and biowarfare. Clin. Microbiol. Rev. 2005, 18:583-607.
29. Loens K., Ursi D., Goossens H., Ieven M. Evaluation of the NucliSens miniMAG RNA extraction and real-time NASBA applications for the detection of Mycoplasma pneumoniae and Chlamydophila pneumoniae in throat swabs. J. Microbiol. Methods 2008, 72:217-219.
30. Makristathis A., Pasching E., Schutze K., Wimmer M., Rotter M.L., Hirschl A.M. Detection of Helicobacter pylori in stool specimens by PCR and antigen enzyme immunoassay. J. Clin. Microbiol. 1998, 36:2772-2774.
31. Matthijnssens J., Ciarlet M., McDonald S.M., Attoui H., Banyai K., Brister J.R., Buesa J., Esona M.D., Estes M.K., Gentsch J.R., Iturriza-Gomara M., Johne R., Kirkwood C.D., Martella V., Mertens P.P., Nakagomi O., Parreno V., Rahman M., Ruggeri F.M., Saif L.J., Santos N., Steyer A., Taniguchi K., Patton J.T., Desselberger U., Van Ranst M. Uniformity of rotavirus strain nomenclature proposed by the Rotavirus Classification Working Group (RCWG). Arch. Virol. 2011, 156:1397-1413.
32. Matthijnssens J., Rahman M., Yang X., Delbeke T., Arijs I., Kabue J.P., Muyembe J.J., Van Ranst M. G8 rotavirus strains isolated in the Democratic Republic of Congo belong to the DS-1-like genogroup. J. Clin. Microbiol. 2006, 44:1801-1809.
33. Monteiro L., Bonnemaison D., Vekris A., Petry K.G., Bonnet J., Vidal R., Cabrita J., Megraud F. Complex polysaccharides as PCR inhibitors in feces: Helicobacter pylori model. J. Clin. Microbiol. 1997, 35:995-998.
34. Pandey R.N., Adams R.P., Flournoy L.E. Inhibition of random amplified polymorphic DNAs (RAPDs) by plant polysaccharides. Plant Mol. Biol. Rep. 1996, 14:17-22.
35. Payne D.C., Edwards K.M., Bowen M.D., Keckley E., Peters J., Esona M.D., Teel E.N., Kent D., Parashar U.D., Gentsch J.R. Sibling transmission of vaccine-derived rotavirus (RotaTeq) associated with rotavirus gastroenteritis. Pediatrics 2010, 125:e438-e441.
36. Payne D.C., Staat M.A., Edwards K.M., Szilagyi P.G., Gentsch J.R., Stockman L.J., Curns A.T., Griffin M., Weinberg G.A., Hall C.B., Fairbrother G., Alexander J., Parashar U.D. Active, population-based surveillance for severe rotavirus gastroenteritis in children in the United States. Pediatrics 2008, 122:1235-1243.
37. Perelle S., Cavellini L., Burger C., Blaise-Boisseau S., Hennechart-Collette C., Merle G., Fach P. Use of a robotic RNA purification protocol based on the NucliSens easyMAG for real-time RT-PCR detection of hepatitis A virus in bottled water. J. Virol. Methods 2009, 157:80-83.
38. Petrich A., Mahony J., Chong S., Broukhanski G., Gharabaghi F., Johnson G., Louie L., Luinstra K., Willey B., Akhaven P., Chui L., Jamieson F., Louie M., Mazzulli T., Tellier R., Smieja M., Cai W., Chernesky M., Richardson S.E. Multicenter comparison of nucleic acid extraction methods for detection of severe acute respiratory syndrome coronavirus RNA in stool specimens. J. Clin. Microbiol. 2006, 44:2681-2688.
39. Rahman M., Matthijnssens J., Saiada F., Hassan Z., Heylen E., Azim T., Van Ranst M. Complete genomic analysis of a Bangladeshi G1P[8] rotavirus strain detected in 2003 reveals a close evolutionary relationship with contemporary human Wa-like strains. Infect. Genet. Evol. 2010, 10:746-754.
40. Rahman M., Matthijnssens J., Yang X., Delbeke T., Arijs I., Taniguchi K., Iturriza-Gomara M., Iftekharuddin N., Azim T., Van Ranst M. Evolutionary history and global spread of the emerging G12 human rotaviruses. J. Virol. 2007, 81:2382-2390.
41. Rahman M., Sultana R., Ahmed G., Nahar S., Hassan Z.M., Saiada F., Podder G., Faruque A.S., Siddique A.K., Sack D.A., Matthijnssens J., Van Ranst M., Azim T. Prevalence of G2P[4] and G12P[6] rotavirus, Bangladesh. Emerg. Infect. Dis. 2007, 13:18-24.
42. Ramachandran M., Gentsch J.R., Parashar U.D., Jin S., Woods P.A., Holmes J.L., Kirkwood C.D., Bishop R.F., Greenberg H.B., Urasawa S., Gerna G., Coulson B.S., Taniguchi K., Bresee J.S., Glass R.I. Detection and characterization of novel rotavirus strains in the United States. J. Clin. Microbiol. 1998, 36:3223-3229.
43. Rasool N.B., Monroe S.S., Glass R.I. Determination of a universal nucleic acid extraction procedure for PCR detection of gastroenteritis viruses in faecal specimens. J. Virol. Methods 2002, 100:1-16.
44. Ray P., Fenaux M., Sharma S., Malik J., Subodh S., Bhatnagar S., Greenberg H., Glass R.I., Gentsch J., Bhan M.K. Quantitative evaluation of rotaviral antigenemia in children with acute rotaviral diarrhea. J. Infect. Dis. 2006, 194:588-593.
45. Rivera L., Pena L.M., Stainier I., Gillard P., Cheuvart B., Smolenov I., Ortega-Barria E., Han H.H. Horizontal transmission of a human rotavirus vaccine strain - a randomized, placebo-controlled study in twins. Vaccine 2011, 29:9508-9513.
46. Schmid M., Oehme R., Schalasta G., Brockmann S., Kimmig P., Enders G. Fast detection of Noroviruses using a real-time PCR assay and automated sample preparation. BMC Infect. Dis. 2004, 4:1-8.
47. Schuurman T., de Boer R., Patty R., Kooistra-Smid M., van Zwet A. Comparative evaluation of in-house manual, and commercial semi-automated and automated DNA extraction platforms in the sample preparation of human stool specimens for a Salmonella enterica 5'-nuclease assay. J. Microbiol. Methods 2007, 71:238-245.
48. Tang Y.W., Sefers S.E., Li H.J., Kohn D.J., Procop G.W. Comparative evaluation of three commercial systems for nucleic acid extraction from urine specimens. J. Clin. Microbiol. 2005, 43:4830-4833.
49. Tang Y.W., Sefers S.E., Li H.J., Kohn D.J., Procop G.W. Comparative evaluation of three commercial systems for nucleic acid extraction from urine specimens. J. Clin. Microbiol. 2005, 43:5833.
50. Wolk D., Schneider S.K., Wengenack N.L., Sloan L.M., Rosenblatt J.E. Real-time PCR method for detection of Encephalitozoon intestinalis from stool specimens. J. Clin. Microbiol. 2002, 40:3922-3928.
51. Wu F.T., Banyai K., Huang J.C., Wu H.S., Chang F.Y., Yang J.Y., Hsiung C.A., Huang Y.C., Lin J.S., Hwang K.P., Jiang B., Gentsch J.R. Diverse origin of P[19] rotaviruses in children with acute diarrhea in Taiwan: detection of novel lineages of the G3, G5, and G9 VP7 genes. J. Med. Virol. 2011, 83:1279-1287.
52. Yang G., Erdman D.E., Kodani M., Kools J., Bowen M.D., Fields B.S. Comparison of commercial systems for extraction of nucleic acids from DNA/RNA respiratory pathogens. J. Virol. Methods 2011, 171:195-199.
53. Yen C., Jakob K., Esona M.D., Peckham X., Rausch J., Hull J.J., Whittier S., Gentsch J.R., LaRussa P. Detection of fecal shedding of rotavirus vaccine in infants following their first dose of pentavalent rotavirus vaccine. Vaccine 2011, 29:4151-4155.
54. Zeller M., Rahman M., Heylen E., De Coster S., De Vos S., Arijs I., Novo L., Verstappen N., Van Ranst M., Matthijnssens J. Rotavirus incidence and genotype distribution before and after national rotavirus vaccine introduction in Belgium. Vaccine 2010, 28:7507-7513.