Next-generation sequencing combined with specific PCR assays to determine the bacterial 16S rRNA gene profiles of middle ear fluid collected from children with acute otitis media

mSphere

Volumn 2, Issue 2, 2017, Pages

  Sillanpää, Saara ^a   Kramna, Lenka ^b   Oikarinen, Sami ^c   Sipilä, Markku ^a   Rautiainen, Markus ^a   Aittoniemi, Janne ^d   Laranne, Jussi ^a   Hyöty, Heikki ^c,d   Cinek, Ondrej ^b  

^a TAMPERE UNIVERSITY HOSPITAL   (Finland)

^b CHARLES UNIVERSITY   (Czech Republic)

^c TAMPERE UNIVERSITY OF TECHNOLOGY   (Finland)

^d FIMLAB LABORATORIES   (Finland)

Author keywords

16S profiling; Acute otitis media; Bacteriome profiling; Mass sequencing; Next generation sequencing

Indexed keywords

EID: 85031916751     PISSN: None     EISSN: 23795042     Source Type: Journal    
DOI: 10.1128/mSphere.00006-17     Document Type: Article

References (44)

1. Ruohola A, Meurman O, Nikkari S, Skottman T, Salmi A, Waris M, österback R, Eerola E, Allander T, Niesters H, Heikkinen T, Ruuskanen O. 2006. Microbiology of acute otitis media in children with tympanostomy tubes: prevalences of bacteria and viruses. Clin Infect Dis 43:1417-1422. https://doi.org/10.1086/509332
2. Casselbrant ML, Mandel EM, Kurs-Lasky M, Rockette HE, Bluestone CD. 1995. Otitis media in a population of black American and white American infants, 0-2 years of age. Int J Pediatr Otorhinolaryngol 33:1-16. https://doi.org/10.1016/0165-5876(95)01184-D
3. Harimaya A, Takada R, Hendolin PH, Fujii N, Ylikoski J, Himi T. 2006. High incidence of Alloiococcus otitidis in children with otitis media, despite treatment with antibiotics. J Clin Microbiol 44:946-949. https://doi.org/ 10.1128/JCM.44.3.946-949.2006
4. Kaur R, Adlowitz DG, Casey JR, Zeng M, Pichichero ME. 2010. Simultaneous assay for four bacterial species including Alloiococcus otitidis using multiplex-PCR in children with culture negative acute otitis media. Pediatr Infect Dis J 29:741-745. https://doi.org/10.1097/INF.0b013 e3181d9e639
5. Marsh RL, Binks MJ, Beissbarth J, Christensen P, Morris PS, Leach AJ, Smith-Vaughan HC. 2012. Quantitative PCR of ear discharge from Indigenous Australian children with acute otitis media with perforation supports a role for Alloiococcus otitidis as a secondary pathogen. BMC Ear Nose Throat Disord 12:11. https://doi.org/10.1186/1472-6815-12-11
6. Palmu AAI, Saukkoriipi PA, Lahdenkari MI, Kuisma LK, Makela PH, Kilpi TM, Leinonen M. 2004. Does the presence of pneumococcal DNA in middle-ear fluid indicate pneumococcal etiology in acute otitis media? J Infect Dis 189:775-784. https://doi.org/10.1086/381765
7. Smith-Vaughan HC, Binks MJ, Marsh RL, Kaestli M, Ward L, Hare KM, Pizzutto SJ, Thornton RB, Morris PS, Leach AJ. 2013. Dominance of Haemophilus influenzae in ear discharge from Indigenous Australian children with acute otitis media with tympanic membrane perforation. BMC Ear Nose Throat Disord 13:12. https://doi.org/10.1186/1472-6815-13-12
8. Stol K, Verhaegh SJC, Graamans K, Engel JAM, Sturm PDJ, Melchers WJG, Meis JF, Warris A, Hays JP, Hermans PWM. 2013. Microbial profiling does not differentiate between childhood recurrent acute otitis media and chronic otitis media with effusion. Int J Pediatr Otorhinolaryngol 77: 488-493. https://doi.org/10.1016/j.ijporl.2012.12.016
9. Virolainen A, Salo P, Jero J, Karma P, Eskola J, Leinonen M. 1994. Comparison of PCR assay with bacterial culture for detecting Streptococcus pneumoniae in middle ear fluid of children with acute otitis media. J Clin Microbiol 32:2667-2670
10. Xu Q, Kaur R, Casey JR, Adlowitz DG, Pichichero ME, Zeng M. 2011. Identification of Streptococcus pneumoniae and Haemophilus influenzae in culture-negative middle ear fluids from children with acute otitis media by combination of multiplex PCR and multi-locus sequencing typing. Int J Pediatr Otorhinolaryngol 75:239-244. https://doi.org/10 .1016/j.ijporl.2010.11.008
11. Yatsyshina S, Mayanskiy N, Shipulina O, Kulichenko T, Alyabieva N, Katosova L, Lazareva A, Skachkova T, Elkina M, Matosova S, Shipulin G. 2016. Detection of respiratory pathogens in pediatric acute otitis media by PCR and comparison of findings in the middle ear and nasopharynx. Diagn Microbiol Infect Dis 85:125-130. https://doi.org/ 10.1016/j.diagmicrobio.2016.02.010
12. Sillanpää S, Oikarinen S, Sipilä M, Kramna L, Rautiainen M, Huhtala H, Aittoniemi J, Laranne J, Hyöty H, Cinek O. 2016. Moraxella catarrhalis might be more common than expected in acute otitis media in young Finnish children. J Clin Microbiol 54:2373-2379. https://doi.org/10.1128/ JCM.01146-16
13. Liu CM, Cosetti MK, Aziz M, Buchhagen JL, ContenteCuomo TL, Price LB, Keim PS, Lalwani AK. 2011. The otologic microbiome: a study of the bacterial microbiota in a pediatric patient with chronic serous otitis media using 16SrRNA gene-based pyrosequencing. Arch Otolaryngol Head Neck Surg 137:664-668. https://doi.org/10.1001/archoto.2011.116
14. Jervis-Bardy J, Rogers GB, Morris PS, Smith-Vaughan HC, Nosworthy E, Leong LEX, Smith RJ, Weyrich LS, De Haan J, Carney AS, Leach AJ, O'Leary S, Marsh RL. 2015. The microbiome of otitis media with effusion in Indigenous Australian children. Int J Pediatr Otorhinolaryngol 79: 1548-1555. https://doi.org/10.1016/j.ijporl.2015.07.013
15. Neeff M, Biswas K, Hoggard M, Taylor MW, Douglas R. 2016. Molecular microbiological profile of chronic suppurative otitis media. J Clin Microbiol 54:2538-2546. https://doi.org/10.1128/JCM.01068-16
16. von Graevenitz A, Funke G. 2014. Turicella otitidis and Corynebacterium auris: 20 years on. Infection 42:1-4. https://doi.org/10.1007/s15010-013-0488-x
17. Kloos WE, Schleifer KH. 1983. Staphylococcus auricularis sp. nov.: an inhabitant of the human external ear. Int J Syst Bacteriol 33:9-14. https://doi.org/10.1099/00207713-33-1-9
18. Lew SQ, Saez J, Whyte R, Stephenson Y. 2004. Peritoneal dialysisassociated peritonitis caused by Staphylococcus auricularis. Perit Dial Int 24:195-196
19. Hoffman DJ, Brown GD, Lombardo FA. 2007. Early-onset sepsis with Staphylococcus auricularis in an extremely low-birth weight infant-an uncommon pathogen. J Perinatol 27:519-520. https://doi.org/10.1038/ sj.jp.7211773
20. Roland PS, Stroman DW. 2002. Microbiology of acute otitis externa. Laryngoscope 112:1166-1177. https://doi.org/10.1097/00005537-20020 7000-00005
21. Faden H, Dryja D. 1989. Recovery of a unique bacterial organism in human middle ear fluid and its possible role in chronic otitis media. J Clin Microbiol 27:2488-2491
22. Hendolin PH, Markkanen A, Ylikoski J, Wahlfors JJ. 1997. Use of multiplex PCR for simultaneous detection of four bacterial species in middle ear effusions. J Clin Microbiol 35:2854-2858
23. Hendolin PH, Paulin L, Ylikoski J. 2000. Clinically applicable multiplex PCR for four middle ear pathogens. J Clin Microbiol 38:125-132
24. Holder RC, Kirse DJ, Evans AK, Peters TR, Poehling KA, Swords WE, Reid SD. 2012. One third of middle ear effusions from children undergoing tympanostomy tube placement had multiple bacterial pathogens. BMC Pediatr 12:87. https://doi.org/10.1186/1471-2431-12-87
25. Aydin E, Taştan E, Yücel M, Aydogan F, Karakoç E, Arslan N, Kantekin Y, Demirci M. 2012. Concurrent assay for four bacterial species including Alloiococcus otitidis in middle ear, nasopharynx and tonsils of children with otitis media with effusion: a preliminary report. Clin Exp Otorhinolaryngol 5:81-85. https://doi.org/10.3342/ceo.2012.5.2.81
26. Harimaya A, Takada R, Somekawa Y, Fujii N, Himi T. 2006. High frequency of Alloiococcus otitidis in the nasopharynx and in the middle ear cavity of otitis-prone children. Int J Pediatr Otorhinolaryngol 70:1009-1014. https://doi.org/10.1016/j.ijporl.2005.10.012
27. Holder RC, Kirse DJ, Evans AK, Whigham AS, Peters TR, Poehling KA, Swords WE, Reid SD. 2015. Otopathogens detected in middle ear fluid obtained during tympanostomy tube insertion: contrasting purulent and non-purulent effusions. PLoS One 10:e0128606. https://doi.org/10 .1371/journal.pone.0128606
28. Post JC, Aul JJ, White GJ, Wadowsky RM, Zavoral T, Tabari R, Kerber B, Doyle WJ, Ehrlich GD. 1996. PCR-based detection of bacterial DNA after antimicrobial treatment is indicative of persistent, viable bacteria in the chinchilla model of otitis media. Am J Otolaryngol 17:106-111
29. Lupan I, Ianc MB, Ochis C, Popescu O. 2013. The evidence of contaminant bacterial DNA in several commercial Taq polymerases. Rom Biotechnol Lett 18:8007-8012
30. Niimi H, Mori M, Tabata H, Minami H, Ueno T, Hayashi S, Kitajima I. 2011. A novel eukaryote-made thermostable DNA polymerase which is free from bacterial DNA contamination. J Clin Microbiol 49:3316-3320. https://doi.org/10.1128/JCM.00584-11
31. Spangler R, Goddard NL, Thaler DS. 2009. Optimizing Taq polymerase concentration for improved signal-to-noise in the broad range detection of low abundance bacteria. PLoS One 4:e7010. https://doi.org/10.1371/ journal.pone.0007010
32. Westerberg BD, Kozak FK, Thomas EE, Blondel-Hill E, Brunstein JD, Patrick DM. 2009 Is the healthy middle ear a normally sterile site? Otol Neurotol 30:174-177. https://doi.org/10.1097/MAO.0b013e31819225a0
33. Nadkarni MA, Martin FE, Jacques NA, Hunter N. 2002. Determination of bacterial load by real-time PCR using a broad-range (universal) probe and primers set. Microbiology 148:257-266. https://doi.org/10.1099/ 00221287-148-1-257
34. Carvalho Mda G, Tondella ML, McCaustland K, Weidlich L, McGee L, Mayer LW, Steigerwalt A, Whaley M, Facklam RR, Fields B, Carlone G, Ades EW, Dagan R, Sampson JS. 2007. Evaluation and improvement of real-time PCR assays targeting lytA, ply, and psaA genes for detection of pneumococcal DNA. J Clin Microbiol 45:2460-2466. https://doi.org/10 .1128/JCM.02498-06
35. De Vos D, Lim AJ, Pirnay JP, Struelens M, Vandenvelde C, Duinslaeger L, Vanderkelen A, Cornelis P. 1997. Direct detection and identification of Pseudomonas aeruginosa in clinical samples such as skin biopsy specimens and expectorations by multiplex PCR based on two outer membrane lipoprotein genes, oprI and oprL. J Clin Microbiol 35:1295-1299
36. Pichon B, Hill R, Laurent F, Larsen AR, Skov RL, Holmes M, Edwards GF, Teale C, Kearns AM. 2012. Development of a real-time quadruplex PCR assay for simultaneous detection of nuc, Panton-Valentine leucocidin (PVL), mecA and homologue mecALGA251. J Antimicrob Chemother 67:2338-2341. https://doi.org/10.1093/jac/dks221
37. Muyzer G, de Waal EC, Uitterlinden AG. 1993. Profiling of complex microbial populations by denaturing gradient gel electrophoresis analysis of polymerase chain reaction-amplified genes coding for 16S rRNA. Appl Environ Microbiol 59:695-700
38. Jaric M, Segal J, Silva-Herzog E, Schneper L, Mathee K, Narasimhan G. 2013. Better primer design for metagenomics applications by increasing taxonomic distinguishability. BMC Proc 7(Suppl 7):S4. https://doi.org/10 .1186/1753-6561-7-S7-S4
39. Kozich JJ, Westcott SL, Baxter NT, Highlander SK, Schloss PD. 2013. Development of a dual-index sequencing strategy and curation pipeline for analyzing amplicon sequence data on the MiSeq Illumina sequencing platform. Appl Environ Microbiol 79:5112-5120. https://doi.org/10.1128/ AEM.01043-13
40. Schloss PD, Westcott SL, Ryabin T, Hall JR, Hartmann M, Hollister EB, Lesniewski RA, Oakley BB, Parks DH, Robinson CJ, Sahl JW, Stres B, Thallinger GG, Van Horn DJ, Weber CF. 2009. Introducing mothur: opensource, platform-independent, community-supported software for describing and comparing microbial communities. Appl Environ Microbiol 75:7537-7541. https://doi.org/10.1128/AEM.01541-09
41. Caporaso JG, Kuczynski J, Stombaugh J, Bittinger K, Bushman FD, Costello EK, Fierer N, Peña AG, Goodrich JK, Gordon JI, Huttley GA, Kelley ST, Knights D, Koenig JE, Ley RE, Lozupone CA, McDonald D, Muegge BD, Pirrung M, Reeder J, Sevinsky JR, Turnbaugh PJ, Walters WA, Widmann J, Yatsunenko T, Zaneveld J, Knight R. 2010. QIIME allows analysis of high-throughput community sequencing data. Nat Methods 7:335-336. https://doi.org/10.1038/nmeth.f.303
42. Edgar RC. 2010. Search and clustering orders of magnitude faster than BLAST. Bioinformatics 26:2460-2461. https://doi.org/10.1093/ bioinformatics/btq461
43. Quast C, Pruesse E, Yilmaz P, Gerken J, Schweer T, Yarza P, Peplies J, Glöckner FO. 2013. The SILVA ribosomal RNA gene database project: improved data processing and web-based tools. Nucleic Acids Res 41: D590-D596. https://doi.org/10.1093/nar/gks1219
44. Klindworth A, Pruesse E, Schweer T, Peplies J, Quast C, Horn M, Glöckner FO. 2013. Evaluation of general 16S ribosomal RNA gene PCR primers for classical and next-generation sequencing-based diversity studies. Nucleic Acids Res 41:e1. https://doi.org/10.1093/nar/gks808