Otology/Neurotology

Microbiomes of the normal middle ear and ears with chronic otitis media

Corresponding Author

Shujiro B. Minami MD

[email protected]

orcid.org/0000-0002-7992-4868

National Hospital Organization Tokyo Medical Center, National Institute of Sensory Organs, Tokyo, Japan

Send correspondence to Shujiro B. Minami, MD, PhD, Department of Otolaryngology National Tokyo Medical Center, 2-5-1 Higashigaoka, Meguro, Tokyo 152-8902, Japan. E-mail: [email protected]Search for more papers by this author

Hideki Mutai PhD,

Hideki Mutai PhD

National Hospital Organization Tokyo Medical Center, National Institute of Sensory Organs, Tokyo, Japan

Search for more papers by this author

Tomoko Suzuki,

Tomoko Suzuki

National Hospital Organization Tokyo Medical Center, National Institute of Sensory Organs, Tokyo, Japan

Search for more papers by this author

Arata Horii MD,

Arata Horii MD

Niigata University, Department of Otolaryngology Head and Neck Surgery, Nigata, Japan

Search for more papers by this author

Naoki Oishi MD,

Naoki Oishi MD

Keio University, School of Medicine, Department of Otolaryngology, Keio, Japan

Search for more papers by this author

Koichiro Wasano MD,

Koichiro Wasano MD

Japanese Red Cross Shizuoka Hospital, Department of Otolaryngology, Shizuoka, Japan

Search for more papers by this author

Motoyasu Katsura MD,

Motoyasu Katsura MD

National Hospital Organization Ureshino Medical Center, Department of Otolaryngology, Ureshino, Japan

Search for more papers by this author

Fujinobu Tanaka MD,

Fujinobu Tanaka MD

National Hospital Organization Nagasaki Medical Center, Department of Otolaryngology, Nagasaki, Japan

Search for more papers by this author

Tetsuya Takiguchi MD,

Tetsuya Takiguchi MD

National Hospital Organization Kanazawa Medical Center, Department of Otolaryngology, Kanazawa, Japan

Search for more papers by this author

Masato Fujii MD,

Masato Fujii MD

National Hospital Organization Tokyo Medical Center, National Institute of Sensory Organs, Tokyo, Japan

Search for more papers by this author

Kimitaka Kaga MD,

Kimitaka Kaga MD

National Hospital Organization Tokyo Medical Center, National Institute of Sensory Organs, Tokyo, Japan

International University of Health and Welfare, Center for Speech and Hearing Disorders, Tochigi, Japan

Search for more papers by this author

Shujiro B. Minami MD,

Corresponding Author

Shujiro B. Minami MD

[email protected]

orcid.org/0000-0002-7992-4868

National Hospital Organization Tokyo Medical Center, National Institute of Sensory Organs, Tokyo, Japan

Hideki Mutai PhD,

Hideki Mutai PhD

National Hospital Organization Tokyo Medical Center, National Institute of Sensory Organs, Tokyo, Japan

Search for more papers by this author

Tomoko Suzuki,

Tomoko Suzuki

National Hospital Organization Tokyo Medical Center, National Institute of Sensory Organs, Tokyo, Japan

Search for more papers by this author

Arata Horii MD,

Arata Horii MD

Niigata University, Department of Otolaryngology Head and Neck Surgery, Nigata, Japan

Search for more papers by this author

Naoki Oishi MD,

Naoki Oishi MD

Keio University, School of Medicine, Department of Otolaryngology, Keio, Japan

Search for more papers by this author

Koichiro Wasano MD,

Koichiro Wasano MD

Japanese Red Cross Shizuoka Hospital, Department of Otolaryngology, Shizuoka, Japan

Search for more papers by this author

Motoyasu Katsura MD,

Motoyasu Katsura MD

National Hospital Organization Ureshino Medical Center, Department of Otolaryngology, Ureshino, Japan

Search for more papers by this author

Fujinobu Tanaka MD,

Fujinobu Tanaka MD

National Hospital Organization Nagasaki Medical Center, Department of Otolaryngology, Nagasaki, Japan

Search for more papers by this author

Tetsuya Takiguchi MD,

Tetsuya Takiguchi MD

National Hospital Organization Kanazawa Medical Center, Department of Otolaryngology, Kanazawa, Japan

Search for more papers by this author

Masato Fujii MD,

Masato Fujii MD

National Hospital Organization Tokyo Medical Center, National Institute of Sensory Organs, Tokyo, Japan

Search for more papers by this author

Kimitaka Kaga MD,

Kimitaka Kaga MD

National Hospital Organization Tokyo Medical Center, National Institute of Sensory Organs, Tokyo, Japan

International University of Health and Welfare, Center for Speech and Hearing Disorders, Tochigi, Japan

Search for more papers by this author

First published: 11 April 2017

https://doi.org/10.1002/lary.26579

Citations: 53

Financial Disclosure: Supported by a Grant-in-Aid for Clinical Research from the National Hospital Organization (Japan) and JSPS KAKENHI (grant number 16K11205). The authors have no other funding, financial relationships, or conflicts of interest to disclose.

Share a link

Email
Wechat
Bluesky

Abstract

Objective

The aim of this study was to profile and compare the middle ear microbiomes of human subjects with and without chronic otitis media.

Study Design

Prospective multicenter cohort study.

Methods

All consecutive patients undergoing tympanoplasty surgery for chronic otitis media or ear surgery for conditions other than otitis media were recruited. Sterile swab samples were collected from the middle ear mucosa during surgery. The variable region 4 of the 16S rRNA gene in each sample were amplified using region-specific primers adapted for the Illumina MiSeq sequencer (Illumina, CA, USA)). The sequences were subjected to local blast and classified using Metagenome@KIN (World Fusion, Tokyo, Japan).

Results

In total, 155 participants were recruited from seven medical centers. Of these, 88 and 67 had chronic otitis media and normal middle ears, respectively. The most abundant bacterial phyla on the mucosal surfaces of the normal middle ears were Proteobacteria, followed by Actinobacteria, Firmicutes, and Bacteroidetes. The children and adults with normal middle ears differed significantly in terms of middle ear microbiomes. Subjects with chronic otitis media without active inflammation (dry ear) had similar middle ear microbiomes as the normal middle ears group. Subjects with chronic otitis media with active inflammation (wet ear) had a lower prevalence of Proteobacteria and a higher prevalence of Firmicutes than the normal middle ears.

Conclusion

The human middle ear is inhabited by more diverse microbial communities than was previously thought. Alteration of the middle ear microbiome may contribute to the pathogenesis of chronic otitis media with active inflammation.

Level of Evidence

2b. Laryngoscope, 127:E371–E377, 2017

BIBLIOGRAPHY

1Wilson M. Bacteriology of Humans: An Ecological Perspective. Malden, MA: Wiley-Blackwell; 2008.
Google Scholar
2 Human Microbiome Project C. Structure, function and diversity of the healthy human microbiome. Nature 2012; 486: 207–214.
10.1038/nature11234
CAS PubMed Web of Science® Google Scholar
3Hugenholtz P, Goebel BM, Pace NR. Impact of culture-independent studies on the emerging phylogenetic view of bacterial diversity. J Bacteriol 1998; 180: 4765–4774.
10.1128/JB.180.18.4765-4774.1998
CAS PubMed Web of Science® Google Scholar
4Costello EK, Lauber CL, Hamady M, Fierer N, Gordon JI, Knight R. Bacterial community variation in human body habitats across space and time. Science 2009; 326: 1694–1697.
10.1126/science.1177486
CAS PubMed Web of Science® Google Scholar
5 Human Microbiome Project C. A framework for human microbiome research. Nature 2012; 486: 215–221.
10.1038/nature11209
CAS PubMed Web of Science® Google Scholar
6Weinstock GM. Genomic approaches to studying the human microbiota. Nature 2012; 489: 250–256.
10.1038/nature11553
CAS PubMed Web of Science® Google Scholar
7Head IM, Saunders JR, Pickup RW. Microbial evolution, diversity, and ecology: a decade of ribosomal RNA analysis of uncultivated microorganisms. Microb Ecol 1998; 35: 1–21.
10.1007/s002489900056
CAS PubMed Web of Science® Google Scholar
8Parte AC. LPSN—list of prokaryotic names with standing in nomenclature. Nucleic Acids Res 2014; 42: D613–D616.
10.1093/nar/gkt1111
CAS PubMed Web of Science® Google Scholar
9Wallis S, Atkinson H, Coatesworth AP. Chronic otitis media. Postgrad Med 2015; 127: 391–395.
10.1080/00325481.2015.1027133
PubMed Web of Science® Google Scholar
10Kuo CL. Etiopathogenesis of acquired cholesteatoma: prominent theories and recent advances in biomolecular research. Laryngoscope 2015; 125: 234–240.
10.1002/lary.24890
PubMed Web of Science® Google Scholar
11Prasad SC, Shin SH, Russo A, Di Trapani G, Sanna M. Current trends in the management of the complications of chronic otitis media with cholesteatoma. Curr Opin Otolaryngol Head Neck Surg 2013; 21: 446–454.
10.1097/MOO.0b013e3283646467
PubMed Web of Science® Google Scholar
12Brook I. Role of anaerobic bacteria in chronic otitis media and cholesteatoma. Int J Pediatr Otorhinolaryngol 1995; 31: 153–157.
10.1016/0165-5876(94)01080-H
CAS PubMed Web of Science® Google Scholar
13Suzuki K, Kurono Y, Ikeda K, et al. Nationwide surveillance of 6 otorhinolaryngological infectious diseases and antimicrobial susceptibility pattern in the isolated pathogens in Japan. J Infect Chemother 2015; 21: 483–491.
10.1016/j.jiac.2015.03.005
PubMed Web of Science® Google Scholar
14Jervis-Bardy J, Rogers GB, Morris PS, et al. The microbiome of otitis media with effusion in Indigenous Australian children. Int J Pediatr Otorhinolaryngol 2015; 79: 1548–1555.
10.1016/j.ijporl.2015.07.013
PubMed Web of Science® Google Scholar
15Liu CM, Cosetti MK, Aziz M, et al. 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 2011; 137: 664–668.
10.1001/archoto.2011.116
PubMed Web of Science® Google Scholar
16Chan CL, Wabnitz D, Bardy JJ, et al. The microbiome of otitis media with effusion. Laryngoscope 2016; 126: 2844–2851.
10.1002/lary.26128
CAS PubMed Web of Science® Google Scholar
17Caporaso JG, Lauber CL, Walters WA, et al. Ultra-high-throughput microbial community analysis on the Illumina HiSeq and MiSeq platforms. ISME J 2012; 6: 1621–1624.
10.1038/ismej.2012.8
CAS PubMed Web of Science® Google Scholar
18Hammer O, Harper DAT, Ryan PD. Past: paleontological statistics software package for education and data analysis. Palaeontologia Electronica 2001; 4: 1.
Google Scholar
19Lax S, Smith DP, Hampton-Marcell J, et al. Longitudinal analysis of microbial interaction between humans and the indoor environment. Science 2014; 345: 1048–1052.
10.1126/science.1254529
CAS PubMed Web of Science® Google Scholar
20Wilson MT, Hamilos DL. The nasal and sinus microbiome in health and disease. Curr Allergy Asthma Rep 2014; 14: 485.
10.1007/s11882-014-0485-x
CAS PubMed Web of Science® Google Scholar
21Lu LJ, Liu J. Human microbiota and ophthalmic disease. Yale J Biol Med 2016; 89: 325–330.
CAS PubMed Google Scholar
22Salter SJ, Cox MJ, Turek EM, et al. Reagent and laboratory contamination can critically impact sequence-based microbiome analyses. BMC Biol 2014; 12: 87.
10.1186/s12915-014-0087-z
CAS PubMed Web of Science® Google Scholar
23Stroman DW, Roland PS, Dohar J, Burt W. Microbiology of normal external auditory canal. Laryngoscope 2001; 111: 2054–2059.
10.1097/00005537-200111000-00035
CAS PubMed Web of Science® Google Scholar
24Dibb WL. The normal microbial flora of the outer ear canal in healthy Norwegian individuals. NIPH Ann 1990; 13: 11–16.
CAS PubMed Google Scholar
25Arslan IB, Genc S, Kayhan BC, Gumussoy M, Ozel G, Cukurova I. Bacterial change in external auditory canal upon antisepsis with povidone-iodine during tympanoplasty. Eur Arch Otorhinolaryngol 2015; 272: 551–555.
10.1007/s00405-013-2864-7
PubMed Web of Science® Google Scholar
26Parha E, Alalade A, David K, Kaddour H, Degun P, Namnyak S. Brain abscess due to Trueperella bernardiae. Br J Neurosurg 2015; 29: 728–729.
10.3109/02688697.2015.1023776
PubMed Web of Science® Google Scholar
27Chole RA, Faddis BT. Evidence for microbial biofilms in cholesteatomas. Arch Otolaryngol Head Neck Surg 2002; 128: 1129–1133.
10.1001/archotol.128.10.1129
PubMed Web of Science® Google Scholar
28Funke G, Stubbs S, Altwegg M, Carlotti A, Collins MD. Turicella otitidis gen. nov., sp. nov., a coryneform bacterium isolated from patients with otitis media. Int J Syst Bacteriol 1994; 44: 270–273.
10.1099/00207713-44-2-270
CAS PubMed Web of Science® Google Scholar

Citing Literature

Volume127, Issue10

October 2017

Pages E371-E377

Microbiomes of the normal middle ear and ears with chronic otitis media

Abstract

Objective

Study Design

Methods

Results

Conclusion

Level of Evidence

BIBLIOGRAPHY

Citing Literature

References

Information

About Wiley Online Library

Help & Support

Opportunities

Connect with Wiley

Microbiomes of the normal middle ear and ears with chronic otitis media

Abstract

Objective

Study Design

Methods

Results

Conclusion

Level of Evidence

BIBLIOGRAPHY

Citing Literature

References

Related

Information