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Microbiology of otitis media in Indigenous Australian children: review

Published online by Cambridge University Press:  16 January 2017

J Jervis-Bardy ,
A S Carney ,
R Duguid  and
A J Leach
J Jervis-Bardy*
Affiliation:
Child Health Division, Menzies School of Health Research, Charles Darwin University, Darwin
A S Carney
Affiliation:
Department of Otolaryngology – Head and Neck Surgery, Flinders University, Adelaide, Australia
R Duguid
Affiliation:
Child Health Division, Menzies School of Health Research, Charles Darwin University, Darwin
A J Leach
Affiliation:
Child Health Division, Menzies School of Health Research, Charles Darwin University, Darwin
*
Address for correspondence: Dr Jake Jervis-Bardy, Child Health Division, Menzies School of Health Research, Charles Darwin University, Darwin, Northern Territory, Australia E-mail: [email protected]
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Abstract

Objectives:

To review research addressing the polymicrobial aetiology of otitis media in Indigenous Australian children in order to identify research gaps and inform best practice in effective prevention strategies and therapeutic interventions.

Methods:

Literature review.

Results:

Studies of aspirated middle-ear fluid represented a minor component of the literature reviewed. Most studies relied upon specimens from middle-ear discharge or the nasopharynx. Culture-based middle-ear discharge studies have found that non-typeable Haemophilus influenzae and Streptococcus pneumoniae predominate, with Moraxella catarrhalis, Staphylococcus aureus and Streptococcus pyogenes isolated in a lower proportion of samples. Alloiococcus otitidis was detected in a number of studies; however, its role in otitis media pathogenesis remains controversial. Nasopharyngeal colonisation is a risk factor for otitis media in Indigenous infants, and bacterial load of otopathogens in the nasopharynx can predict the ear state of Indigenous children.

Conclusion:

Most studies have used culture-based methods and specimens from middle-ear discharge or the nasopharynx. Findings from these studies are consistent with international literature, but reliance on culture may incorrectly characterise the microbiology of this condition. Advances in genomic technologies are now providing microbiologists with the ability to analyse the entire mixed bacterial communities (‘microbiomes’) of samples obtained from Indigenous children with otitis media.

Keywords

Otitis MediaIndigenous PopulationMicrobiologyReviewMiddle Ear
Type
Review Articles
Information
The Journal of Laryngology & Otology , Volume 131 , Supplement S2: ASOHNS Supplement , July 2017 , pp. S2 - S11
Copyright
Copyright © JLO (1984) Limited 2017 

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References

1 Morris, PS, Leach, AJ, Silberberg, P, Mellon, G, Wilson, C, Hamilton, E et al. Otitis media in young Aboriginal children from remote communities in Northern and Central Australia: a cross-sectional survey. BMC Pediatr 2005;5:27 CrossRefGoogle ScholarPubMed
2 Lehmann, D, Weeks, S, Jacoby, P, Elsbury, D, Finucane, J, Stokes, A et al. Absent otoacoustic emissions predict otitis media in young Aboriginal children: a birth cohort study in Aboriginal and non-Aboriginal children in an arid zone of Western Australia. BMC Pediatr 2008;8:32 CrossRefGoogle Scholar
3 Williams, CJ, Jacobs, AM. The impact of otitis media on cognitive and educational outcomes. Med J Aust 2009;191:S69–72CrossRefGoogle ScholarPubMed
4 Smith-Vaughan, H, Marsh, R, Leach, A. Otitis media: an ongoing microbial challenge. Microbiology Australia 2009;165:181–4CrossRefGoogle Scholar
5 Satzke, C, Turner, P, Virolainen-Julkunen, A, Adrian, PV, Antonio, M, Hare, KM et al. Standard method for detecting upper respiratory carriage of Streptococcus pneumoniae: updated recommendations from the World Health Organization Pneumococcal Carriage Working Group. Vaccine 2013;32:165–79CrossRefGoogle ScholarPubMed
6 Jervis-Bardy, J, Sanchez, L, Carney, A. Otitis media in Indigenous Australian children: review of epidemiology and risk factors. J Laryngol Otol 2014;128:S16–27CrossRefGoogle ScholarPubMed
7 Jacobs, MR, Dagan, R, Appelbaum, PC, Burch, DJ. Prevalence of antimicrobial-resistant pathogens in middle ear fluid: multinational study of 917 children with acute otitis media. Antimicrob Agents Chemother 1998;42:589–95CrossRefGoogle ScholarPubMed
8 Bluestone, CD, Stephenson, JS, Martin, LM. Ten-year review of otitis media pathogens. Pediatr Infect Dis J 1992;11:S7–11CrossRefGoogle ScholarPubMed
9 Segal, N, Givon-Lavi, N, Leibovitz, E, Yagupsky, P, Leiberman, A, Dagan, R. Acute otitis media caused by Streptococcus pyogenes in children. Clin Infect Dis 2005;41:35–41 CrossRefGoogle ScholarPubMed
10 Leach, AJ. Prospective Studies of Respiratory Pathogens, Particularly Streptococcus Pneumoniae, in Aboriginal and Non-Aboriginal Infants: Impact of Antibiotic Use and Implications for Otitis Media. Darwin: University of Sydney, 1996 Google Scholar
11 Leach, A, MacKenzie, G, Hare, K, Stubbs, E, Beissbarth, J, Kennedy, M et al. Microbiology of acute otitis media with perforation (AOMwiP) in Aboriginal children living in remote communities—monitoring the impact of 7-valent pneumococcal conjugate vaccine (7vPCV). International Congress Series 2006;1289:89–92 CrossRefGoogle Scholar
12 Mackenzie, GA, Carapetis, JR, Leach, AJ, Morris, PS. Pneumococcal vaccination and otitis media in Australian Aboriginal infants: comparison of two birth cohorts before and after introduction of vaccination. BMC Pediatr 2009;9:14 CrossRefGoogle ScholarPubMed
13 Marchisio, P, Bianchini, S, Baggi, E, Fattizzo, M, Galeone, C, Torretta, S et al. A retrospective evaluation of microbiology of acute otitis media complicated by spontaneous otorrhea in children living in Milan, Italy. Infection 2013;41:629–35CrossRefGoogle ScholarPubMed
14 Bluestone, CD. Epidemiology and pathogenesis of chronic suppurative otitis media: implications for prevention and treatment. Int J Pediatr Otorhinolaryngol 1998;42:207–23CrossRefGoogle ScholarPubMed
15 Wiertsema, SP, Leach, AJ. Theories of otitis media pathogenesis, with a focus on Indigenous children. Med J Aust 2009;191:50–4CrossRefGoogle ScholarPubMed
16 Leach, A, Wood, Y, Gadil, E, Stubbs, E, Morris, P. Topical ciprofloxin versus topical framycetin-gramicidin-dexamethasone in Australian aboriginal children with recently treated chronic suppurative otitis media: a randomized controlled trial. Pediatr Infect Dis J 2008;27:692–8CrossRefGoogle ScholarPubMed
17 Brook, I. The role of anaerobic bacteria in chronic suppurative otitis media in children: implications for medical therapy. Anaerobe 2008;14:297–300 CrossRefGoogle ScholarPubMed
18 Daniel, SJ. Topical treatment of chronic suppurative otitis media. Curr Infect Dis Rep 2012;14:121–7CrossRefGoogle ScholarPubMed
19 Couzos, S, Lea, T, Mueller, R, Murray, R, Culbong, M. Effectiveness of ototopical antibiotics for chronic suppurative otitis media in Aboriginal children: a community-based, multicentre, double-blind randomised controlled trial. Med J Aust 2003;179:185–90CrossRefGoogle ScholarPubMed
20 Stuart, J, Butt, H, Walker, P. The microbiology of glue ear in Australian Aboriginal children. J Paediatr Child Health 2003;39:665–7CrossRefGoogle ScholarPubMed
21 Dawson, V, Coelen, R, Murphy, S, Graham, D, Dyer, H, Sunderman, J. Microbiology of chronic otitis media with effusion among Australian Aboriginal children: role of Chlamydia trachomatis. Aust J Exp Biol Med Sci 1985;63:99–107 CrossRefGoogle ScholarPubMed
22 Ashhurst-Smith, C, Hall, ST, Walker, P, Stuart, J, Hansbro, PM, Blackwell, CC. Isolation of Alloiococcus otitidis from Indigenous and non-Indigenous Australian children with chronic otitis media with effusion. FEMS Immunol Med Microbiol 2007;51:163–70CrossRefGoogle ScholarPubMed
23 Gibney, K, Morris, P, Carapetis, J, Skull, S, Smith-Vaughan, H, Stubbs, E et al. The clinical course of acute otitis media in high-risk Australian Aboriginal children: a longitudinal study. BMC Pediatr 2005;5:16 CrossRefGoogle ScholarPubMed
24 Marsh, RL, Binks, MJ, Beissbarth, J, Christensen, P, Morris, PS, Leach, AJ et al. 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 2012;12:11 CrossRefGoogle ScholarPubMed
25 Smith-Vaughan, HC, Binks, MJ, Marsh, RL, Kaestli, M, Ward, L, Hare, KM et al. Dominance of Haemophilus influenzae in ear discharge from Indigenous Australian children with acute otitis media with tympanic membrane perforation. BMC Ear Nose Throat Disord 2013;13:12 CrossRefGoogle ScholarPubMed
26 Stephen, AT, Leach, AJ, Morris, PS. Impact of swimming on chronic suppurative otitis media in Aboriginal children: a randomised controlled trial. Med J Aust 2013;199:51–5CrossRefGoogle ScholarPubMed
27 Ashhurst-Smith, C, Hall, ST, Burns, CJ, Stuart, J, Blackwell, CC. In vitro inflammatory responses elicited by isolates of Alloiococcus otitidis obtained from children with otitis media with effusion. Innate Immun 2014;20:320–6CrossRefGoogle ScholarPubMed
28 Tano, K, Von Essen, R, Eriksson, PO, Sjöstedt, A. Alloiococcus otitidis--otitis media pathogen or normal bacterial flora? APMIS 2008;116:785–90CrossRefGoogle ScholarPubMed
29 Takada, R, Harimaya, A, Yamazaki, N, Himi, T. Detection of Alloiococcus otitidis and three middle ear pathogens in the nasopharynx and the middle ear effusion of otitis-prone children. International Congress Series 2003;1257:213–15CrossRefGoogle Scholar
30 Child and Adolescent Health and Development, Prevention of Blindness and Deafness. Chronic Suppurative Otitis Media: Burden of Illness and Management Options. Geneva: World Health Organization, 2004 Google Scholar
31 Recommendations for Clinical Care Guidelines on the Management of Otitis Media in Aboriginal and Torres Strait Islander Populations (2010). In: http://www.healthinfonet.ecu.edu.au/other-health-conditions/ear/resources-and-equipment/otitis-media-guidelines#-about-the-guidelines [8 October 2016]Google Scholar
32 Leach, AJ, Boswell, JB, Asche, V, Nienhuys, TG, Mathews, JD. Bacterial colonisation of the nasopharynx predicts very early onset and persistence of otitis media in Australian aboriginal infants. Pediatr Infect Dis J 1994;13:983–9CrossRefGoogle ScholarPubMed
33 Smith-Vaughan, H, Byun, R, Nadkarni, M, Jacques, NA, Hunter, N, Halpin, S et al. Measuring nasal bacterial load and its association with otitis media. BMC Ear Nose Throat Disord 2006;6:10 CrossRefGoogle ScholarPubMed
34 Watson, K, Carville, K, Bowman, J, Jacoby, P, Riley, T, Leach, AJ et al. Upper respiratory tract bacterial carriage in Aboriginal and non-Aboriginal children in a semi-arid area of Western Australia. Pediatr Infect Dis J 2006;25:782–90CrossRefGoogle Scholar
35 Pickering, J, Smith-Vaughan, H, Beissbarth, J, Bowman, JM, Wiertsema, S, Riley, TV et al. Diversity of nontypeable Haemophilus influenzae strains colonizing Australian Aboriginal and non-Aboriginal children. J Clin Microbiol 2014;52:1352–7CrossRefGoogle ScholarPubMed
36 Moore, HC, Jacoby, P, Taylor, A, Harnett, G, Bowman, J, Riley, TV et al. The interaction between respiratory viruses and pathogenic bacteria in the upper respiratory tract of asymptomatic Aboriginal and non-Aboriginal children. Pediatr Infect Dis J 2010;29:540–5CrossRefGoogle ScholarPubMed
37 Binks, MJ, Cheng, AC, Smith-Vaughan, H, Sloots, T, Nissen, M, Whiley, D et al. Viral-bacterial co-infection in Australian Indigenous children with acute otitis media. BMC Infect Dis 2011;11:161 CrossRefGoogle ScholarPubMed
38 Leach, A, Boswell, J, Asche, V, Nienhuys, T, Mathews, J. Moraxella (Branhamella) catarrhalis and early onset of otitis media in Aboriginal infants. In: Conference Proceedings: Medical Options for Prevention and Treatment of Otitis Media in Australian Aboriginal Infants. Darwin: Menzies School of Health Research and the Australian Doctors Fund, 1992 Google Scholar
39 Gibson, P, Stuart, J, Wlodarczyk, J, Olson, L, Hensley, M. Nasal inflammation and chronic ear disease in Australian Aboriginal children. J Paediatr Child Health 1996;32:143–7CrossRefGoogle ScholarPubMed
40 Smith-Vaughan, H, Leach, A, Shelby-James, T, Kemp, K, Kemp, D, Mathews, J. Carriage of multiple ribotypes of non-encapsulated Haemophilus influenzae in Aboriginal infants with otitis media. Epidemiol Infect 1996;116:177–84CrossRefGoogle ScholarPubMed
41 Leach, AJ, Morris, PS, Mathews, JD. Compared to placebo, long-term antibiotics resolve otitis media with effusion (OME) and prevent acute otitis media with perforation (AOMwiP) in a high-risk population: a randomized controlled trial. BMC Pediatr 2008;8:23 CrossRefGoogle Scholar
42 Massa, HM, Cripps, AW, Lehmann, D. Otitis media: viruses, bacteria, biofilms and vaccines. Med J Aust 2009;191:S44–9CrossRefGoogle ScholarPubMed
43 Vergison, A. Microbiology of otitis media: a moving target. Vaccine 2008;26(suppl 7):G5–10CrossRefGoogle ScholarPubMed
44 Short, KR, Diavatopoulos, DA, Thornton, R, Pedersen, J, Strugnell, RA, Wise, AK et al. Influenza virus induces bacterial and nonbacterial otitis media. J Infect Dis 2011;204:1857–65CrossRefGoogle ScholarPubMed
45 Heikkinen, T, Thint, M, Chonmaitree, T. Prevalence of various respiratory viruses in the middle ear during acute otitis media. N Engl J Med 1999;340:260–4CrossRefGoogle ScholarPubMed
46 Chonmaitree, T, Revai, K, Grady, JJ, Clos, A, Patel, JA, Nair, S et al. Viral upper respiratory tract infection and otitis media complication in young children. Clin Infect Dis 2008;46:815–23CrossRefGoogle ScholarPubMed
47 Ruohola, A, Pettigrew, MM, Lindholm, L, Jalava, J, Räisänen, KS, Vainionpää, R et al. Bacterial and viral interactions within the nasopharynx contribute to the risk of acute otitis media. J Infect 2013;66:247–54CrossRefGoogle Scholar
48 Cripps, AW, Otczyk, DC. Prospects for a vaccine against otitis media. Expert Rev Vaccines 2006;5:517–34CrossRefGoogle ScholarPubMed
49 Hare, KM, Marsh, RL, Binks, MJ, Grimwood, K, Pizzutto, SJ, Leach, AJ et al. Quantitative PCR confirms culture as the gold standard for detection of lower airway infection by nontypeable Haemophilus influenzae in Australian Indigenous children with bronchiectasis. J Microbiol Methods 2013;92:270–2CrossRefGoogle ScholarPubMed
50 Feazel, LM, Frank, DN, Ramakrishnan, VR. Update on bacterial detection methods in chronic rhinosinusitis: implications for clinicians and research scientists. Int Forum Allergy Rhinol 2011;1:451–9CrossRefGoogle ScholarPubMed
51 Hall-Stoodley, L, Hu, FZ, Gieseke, A, Nistico, L, Nguyen, D, Hayes, J et al. Direct detection of bacterial biofilms on the middle-ear mucosa of children with chronic otitis media. JAMA 2006;296:202–11CrossRefGoogle ScholarPubMed
52 Saunders, J, Murray, M, Alleman, A. Biofilms in chronic suppurative otitis media and cholesteatoma: scanning electron microscopy findings. Am J Otolaryngol 2011;32:32–7CrossRefGoogle ScholarPubMed
53 Moriyama, S, Hotomi, M, Shimada, J, Billal, DS, Fujihara, K, Yamanaka, N. Formation of biofilm by Haemophilus influenzae isolated from pediatric intractable otitis media. Auris Nasus Larynx 2009;36:525–31CrossRefGoogle ScholarPubMed
54 Leskinen, K, Hendolin, P, Virolainen-Julkunen, A, Ylikoski, J, Jero, J. The clinical role of Alloiococcus otitidis in otitis media with effusion. Int J Pediatr Otorhinolaryngol 2002;66:41–8CrossRefGoogle ScholarPubMed
55 Post, JC, Preston, RA, Aul, JJ, Larkins-Pettigrew, M, Rydquist-White, J, Anderson, KW et al. Molecular analysis of bacterial pathogens in otitis media with effusion. JAMA 1995;273:1598–604CrossRefGoogle ScholarPubMed
56 Kaur, R, Adlowitz, DG, Casey, JR, Zeng, M, Pichichero, ME. Simultaneous assay for four bacterial species including Alloiococcus otitidis using multiplex-PCR in children with culture negative acute otitis media. Pediatr Infect Dis J 2010;29:741–5CrossRefGoogle ScholarPubMed
57 Post, JC, Aul, JJ, White, GJ, Wadowsky, RM, Zavoral, T, Tabari, R et al. 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 1996;17:106–11CrossRefGoogle ScholarPubMed
58 Hendolin, PH, Markkanen, A, Ylikoski, J, Wahlfors, JJ. Use of multiplex PCR for simultaneous detection of four bacterial species in middle ear effusions. J Clin Microbiol 1997;35:2854–8CrossRefGoogle ScholarPubMed
59 Lee, MR, Pawlowski, KS, Luong, A, Furze, AD, Roland, PS. Biofilm presence in humans with chronic suppurative otitis media. Otolaryngol Head Neck Surg 2009;141:567–71CrossRefGoogle ScholarPubMed
60 Thornton, R, Rigby, P, Wiertsema, S, Filion, P, Langlands, J, Coates, H et al. Multi-species bacterial biofilm and intracellular infection in otitis media. BMC Pediatr 2011;11:94 CrossRefGoogle ScholarPubMed
61 Hall-Stoodley, L, Nistico, L, Sambanthamoorthy, K, Dice, B, Nguyen, D, Mershon, WJ et al. Characterization of biofilm matrix, degradation by DNase treatment and evidence of capsule downregulation in Streptococcus pneumoniae clinical isolates. BMC Microbiol 2008;8:173 CrossRefGoogle ScholarPubMed
62 Kasenõmm, P, Štšepetova, J. Applicability of PCR-DGGE and 16S rDNA sequencing for microbiological analysis of otitis media with effusion. Int J Otolaryngol Head Neck Surg 2012;1:71–6CrossRefGoogle Scholar
63 Marsh, R. Culture-independent Analysis of the Bacteriology Associated with Acute Otitis Media in Indigenous Australian Children. Darwin: Charles Darwin University, 2013 Google Scholar
64 Jervis-Bardy, J, Rogers, GB, Morris, PS, Smith-Vaughan, HC, Nosworthy, E, Leong, LE et al. The microbiome of otitis media with effusion in Indigenous Australian children. Int J Pediatr Otorhinolaryngol 2015;79:1548–55CrossRefGoogle ScholarPubMed
65 Liu, CM, Cosetti, MK, Aziz, M, Buchhagen, JL, Contente-Cuomo, TL, Price, LB 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;137:664–8CrossRefGoogle Scholar