Respiratory Syncytial virus promotes Moraxella catarrhalis-induced ascending experimental Otitis media

PLoS ONE

Volumn 7, Issue 6, 2012, Pages

  Brockson, M Elizabeth ^a   Novotny, Laura A ^a   Jurcisek, Joseph A ^a   McGillivary, Glen ^a   Bowers, Martha R ^a   Bakaletz, Lauren O ^a  

^a THE OHIO STATE UNIVERSITY COLLEGE OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BACTERIAL COLONIZATION; BACTERIUM CULTURE; BACTERIUM IDENTIFICATION; CHINCHILLA; DISEASE PREDISPOSITION; EARDRUM; HAEMOPHILUS INFECTION; HAEMOPHILUS INFLUENZAE; HUMAN; MIDDLE EAR EFFUSION; MIDDLE EAR MUCOSA; MIXED INFECTION; MORAXELLA CATARRHALIS; MORAXELLACEAE INFECTION; MUCOSAL BLEEDING; NASOPHARYNX; NONHUMAN; OTITIS MEDIA; OTOSCOPY; PATHOPHYSIOLOGY; PNEUMOVIRUS INFECTION; RAT; RESPIRATORY SYNCYTIAL PNEUMOVIRUS; SUPERINFECTION;

ACOUSTIC IMPEDANCE TESTS; ANIMALS; BACTERIAL ADHESION; BIOFILMS; CHINCHILLA; EAR, MIDDLE; HAEMOPHILUS INFLUENZAE; MORAXELLA (BRANHAMELLA) CATARRHALIS; MUCOUS MEMBRANE; NASOPHARYNX; OTITIS MEDIA; OTOSCOPY; RESPIRATORY SYNCYTIAL VIRUSES; VIDEO RECORDING;

ANIMALIA; BACTERIA (MICROORGANISMS); CHINCHILLIDAE; HAEMOPHILUS INFLUENZAE; MORAXELLA CATARRHALIS; RESPIRATORY SYNCYTIAL VIRUS; RICE STRIPE VIRUS;

EID: 84863100432     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0040088     Document Type: Article

References (70)

1. Stool SE, Berg AO, Berman S, Carney CJ, Cooley JR, et al. (1994) Otitis Media with Effusion in Young Children. Clinical Practice Guideline. Rockville, MD: Agency for Health Care Policy and Research, Public Health Service, U.S. Department of Health and Human Services.
2. Infante-Rivard C, Fernandez A, (1993) Otitis media in children: frequency, risk factors, and research avenues. Epidemiol Rev 15: 444-465.
3. Hunter LL, Margolis RH, Giebink GS, (1994) Identification of hearing loss in children with otitis media. Ann Otol Rhinol Laryngol pp. 59-61.
4. Baldwin RL, (1993) Effects of otitis media on child development. Am J Otol 14: 601-604.
5. Teele DW, Klein JO, Chase C, Menyuk P, Rosner BA, (1990) Otitis media in infancy and intellectual ability, school achievement, speech, and language at age 7 years. Greater Boston Otitis Media Study Group. J Infect Dis 162: 685-694.
6. Alsarraf R, Jung CJ, Perkins J, Crowley C, Alsarraf NW, et al. (1999) Measuring the indirect and direct costs of acute otitis media. Arch Otolaryngol Head Neck Surg 125: 12-18.
7. Cassell GH, (1997) New and Reemerging Infectious Diseases: A Global Crisis and Immediate Threat to the Nation's Health: The Role of Research. Washington, D.C.: American Society for Microbiology. 1-11 p.
8. Kaplan B, Wandstrat TL, Cunningham JR, (1997) Overall cost in the treatment of otitis media. Pediatr Infect Dis J 16: S9-11.
9. El-Ahmer OR, Braun JM, Amyes SG, Weir DM, Beuth J, et al. (2003) Comparison of Moraxella catarrhalis isolates from children and adults for growth on modified New York City medium and potential virulence factors. J Med Microbiol 52: 853-859.
10. Sakkou Z, Stripeli F, Papadopoulos NG, Critselis E, Georgiou V, et al. (2011) Impact of influenza infection on children's hospital admissions during two seasons in Athens, Greece. Vaccine 29: 1167-1172.
11. Short KR, Diavatopoulos DA, Thornton R, Pedersen J, Strugnell RA, et al. (2011) Influenza Virus Induces Bacterial and Nonbacterial Otitis Media. J Infect Dis.
12. Skoner DP, (2010) Oseltamivir treatment for acute otitis media in children with influenza. Curr Allergy Asthma Rep 10: 389-390.
13. Bezerra PG, Britto MC, Correia JB, Duarte Mdo C, Fonceca AM, et al. (2011) Viral and atypical bacterial detection in acute respiratory infection in children under five years. PLoS One 6: e18928.
14. Moore HC, Jacoby P, Taylor A, Harnett G, Bowman J, et al. (2010) The interaction between respiratory viruses and pathogenic bacteria in the upper respiratory tract of asymptomatic Aboriginal and non-Aboriginal children. Pediatr Infect Dis J 29: 540-545.
15. Bakaletz LO, (2010) Immunopathogenesis of polymicrobial otitis media. J Leukoc Biol 87: 213-222.
16. McGillivary G, Mason KM, Jurcisek JA, Peeples ME, Bakaletz LO, (2009) Respiratory syncytial virus-induced dysregulation of expression of a mucosal beta-defensin augments colonization of the upper airway by non-typeable Haemophilus influenzae. Cell Microbiol 11: 1399-1408.
17. Heikkinen T, (2000) The role of respiratory viruses in otitis media. Vaccine 19: S51-55.
18. Krishnamurthy A, McGrath J, Cripps AW, Kyd JM, (2009) The incidence of Streptococcus pneumoniae otitis media is affected by the polymicrobial environment particularly Moraxella catarrhalis in a mouse nasal colonisation model. Microbes Infect 11: 545-553.
19. Binks MJ, Cheng AC, Smith-Vaughan H, Sloots T, Nissen M, et al. (2011) Viral-bacterial co-infection in Australian Indigenous children with acute otitis media. BMC Infect Dis 11: 161.
20. Karalus R, Campagnari A, (2000) Moraxella catarrhalis: a review of an important human mucosal pathogen. Microbes Infect 2: 547-559.
21. Luke NR, Jurcisek JA, Bakaletz LO, Campagnari AA, (2007) Contribution of Moraxella catarrhalis type IV pili to nasopharyngeal colonization and biofilm formation. Infect Immun 75: 5559-5564.
22. Novotny LA, Clements JD, Bakaletz LO, (2011) Transcutaneous immunization as preventative and therapeutic regimens to protect against experimental otitis media due to nontypeable Haemophilus influenzae. Mucosal Immunol 4: 456-467.
23. McCullers JA, Rehg JE, (2002) Lethal synergism between influenza virus and Streptococcus pneumoniae: characterization of a mouse model and the role of platelet-activating factor receptor. J Infect Dis 186: 341-350.
24. Bakaletz LO, Kennedy BJ, Novotny LA, Duquesne G, Cohen J, et al. (1999) Protection against development of otitis media induced by nontypeable Haemophilus influenzae by both active and passive immunization in a chinchilla model of virus-bacterium superinfection. Infect Immun 67: 2746-2762.
25. Armbruster CE, Hong W, Pang B, Weimer KE, Juneau RA, et al. (2010) Indirect pathogenicity of Haemophilus influenzae and Moraxella catarrhalis in polymicrobial otitis media occurs via interspecies quorum signaling. MBio 1.
26. Suzuki K, Bakaletz LO, (1994) Synergistic effect of adenovirus type 1 and nontypeable Haemophilus influenzae in a chinchilla model of experimental otitis media. Infect Immun 62: 1710-1718.
27. Kennedy BJ, Novotny LA, Jurcisek JA, Lobet Y, Bakaletz LO, (2000) Passive transfer of antiserum specific for immunogens derived from a nontypeable Haemophilus influenzae adhesin and lipoprotein D prevents otitis media after heterologous challenge. Infect Immun 68: 2756-2765.
28. Novotny LA, Jurcisek JA, Godfroid F, Poolman JT, Denoel PA, et al. (2006) Passive immunization with human anti-protein D antibodies induced by polysaccharide protein D conjugates protects chinchillas against otitis media after intranasal challenge with Haemophilus influenzae. Vaccine 24: 4804-4811.
29. Kyd JM, Cripps AW, Novotny LA, Bakaletz LO, (2003) Efficacy of the 26-kilodalton outer membrane protein and two P5 fimbrin-derived immunogens to induce clearance of nontypeable Haemophilus influenzae from the rat middle ear and lungs as well as from the chinchilla middle ear and nasopharynx. Infect Immun 71: 4691-4699.
30. Morton DJ, Bakaletz LO, Jurcisek JA, VanWagoner TM, Seale TW, et al. (2004) Reduced severity of middle ear infection caused by nontypeable Haemophilus influenzae lacking the hemoglobin/hemoglobin-haptoglobin binding proteins (Hgp) in a chinchilla model of otitis media. Microb Pathog 36: 25-33.
31. Jurcisek JA, Bakaletz LO, (2007) Biofilms formed by nontypeable Haemophilus influenzae in vivo contain both double-stranded DNA and type IV pilin protein. J Bacteriol 189: 3868-3875.
32. Hong W, Mason K, Jurcisek J, Novotny L, Bakaletz LO, et al. (2007) Phosphorylcholine decreases early inflammation and promotes the establishment of stable biofilm communities of nontypeable Haemophilus influenzae strain 86-028NP in a chinchilla model of otitis media. Infect Immun 75: 958-965.
33. Martinez-Marin C, Huelves L, del Prado G, Garcia-Cia JI, Cenjor C, et al. (2005) Effect of erythromycin treatment delay on therapeutic outcome of experimental acute otitis media caused by Streptococcus pneumoniae. J Antimicrob Chemother 56: 783-786.
34. Ponte C, Cenjor C, Parra A, Nieto E, Garcia-Calvo G, et al. (1999) Antimicrobial treatment of an experimental otitis media caused by a beta-lactamase positive isolate of Haemophilus influenzae. J Antimicrob Chemother 44: 85-90.
35. Block SL, Hedrick J, Harrison CJ, Tyler R, Smith A, et al. (2004) Community-wide vaccination with the heptavalent pneumococcal conjugate significantly alters the microbiology of acute otitis media. Pediatr Infect Dis J 23: 829-833.
36. Revai K, McCormick DP, Patel J, Grady JJ, Saeed K, et al. (2006) Effect of pneumococcal conjugate vaccine on nasopharyngeal bacterial colonization during acute otitis media. Pediatrics 117: 1823-1829.
37. Aebi C, (2011) Moraxella catarrhalis- pathogen or commensal? Adv Exp Med Biol 697: 107-116.
38. Murphy TF, Parameswaran GI, (2009) Moraxella catarrhalis, a human respiratory tract pathogen. Clin Infect Dis 49: 124-131.
39. Watson K, Carville K, Bowman J, Jacoby P, Riley TV, et al. (2006) Upper respiratory tract bacterial carriage in Aboriginal and non-Aboriginal children in a semi-arid area of Western Australia. Pediatr Infect Dis J 25: 782-790.
40. Gibney KB, Morris PS, Carapetis JR, Skull SA, Smith-Vaughan HC, et al. (2005) The clinical course of acute otitis media in high-risk Australian Aboriginal children: a longitudinal study. BMC Pediatr 5: 16.
41. McCullers JA, Karlstrom A, Iverson AR, Loeffler JM, Fischetti VA, (2007) Novel strategy to prevent otitis media caused by colonizing Streptococcus pneumoniae. PLoS Pathog 3: e28.
42. Meek RB, 3rd, McGrew BM, Cuff CF, Berrebi AS, Spirou GA, et al (1999) Immunologic and histologic observations in reovirus-induced otitis media in the mouse. Ann Otol Rhinol Laryngol 108: 31-38.
43. Hirano T, Kurono Y, Ichimiya I, Suzuki M, Mogi G, (1999) Effects of influenza A virus on lectin-binding patterns in murine nasopharyngeal mucosa and on bacterial colonization. Otolaryngol Head Neck Surg 121: 616-621.
44. Gitiban N, Jurcisek JA, Harris RH, Mertz SE, Durbin RK, et al. (2005) Chinchilla and murine models of upper respiratory tract infections with respiratory syncytial virus. J Virol 79: 6035-6042.
45. Appell LH, Kovatch RM, Reddecliff JM, Gerone PJ, (1971) Pathogenesis of Sendai virus infection in mice. Am J Vet Res 32: 1835-1841.
46. Klemens JJ, Thompson K, Langerman A, Naclerio RM, (2006) Persistent inflammation and hyperresponsiveness following viral rhinosinusitis. Laryngoscope 116: 1236-1240.
47. Armengol CE, Hendley JO, Winther B, (2011) Occurrence of acute otitis media during colds in children younger than four years. Pediatr Infect Dis J 30: 518-520.
48. Bakaletz LO, Murwin DM, Billy JM, (1995) Adenovirus serotype 1 does not act synergistically with Moraxella (Branhamella) catarrhalis to induce otitis media in the chinchilla. Infect Immun 63: 4188-4190.
49. Verhaegh SJ, Snippe ML, Levy F, Verbrugh HA, Jaddoe VW, et al. (2011) Colonization of healthy children by Moraxella catarrhalis is characterized by genotype heterogeneity, virulence gene diversity and co-colonization with Haemophilus influenzae. Microbiology 157: 169-178.
50. Jacoby P, Carville KS, Hall G, Riley TV, Bowman J, et al. (2011) Crowding and other strong predictors of upper respiratory tract carriage of otitis media-related bacteria in Australian Aboriginal and non-Aboriginal children. Pediatr Infect Dis J 30: 480-485.
51. Broides A, Dagan R, Greenberg D, Givon-Lavi N, Leibovitz E, (2009) Acute otitis media caused by Moraxella catarrhalis: epidemiologic and clinical characteristics. Clin Infect Dis 49: 1641-1647.
52. Grieves JL, Jurcisek JA, Quist B, Durbin RK, Peeples ME, et al. (2010) Mapping the anatomy of respiratory syncytial virus infection of the upper airways in chinchillas (Chinchilla lanigera). Comp Med 60: 225-232.
53. Pericone CD, Overweg K, Hermans PW, Weiser JN, (2000) Inhibitory and bactericidal effects of hydrogen peroxide production by Streptococcus pneumoniae on other inhabitants of the upper respiratory tract. Infect Immun 68: 3990-3997.
54. Kotikoski MJ, Palmu AA, Puhakka HJ, (2003) The symptoms and clinical course of acute bullous myringitis in children less than two years of age. Int J Pediatr Otorhinolaryngol 67: 165-172.
55. Luke NR, Russo TA, Luther N, Campagnari AA, (1999) Use of an isogenic mutant constructed in Moraxella catarrhalis to identify a protective epitope of outer membrane protein B1 defined by monoclonal antibody 11C6. Infect Immun 67: 681-687.
56. Bakaletz LO, Tallan BM, Hoepf T, DeMaria TF, Birck HG, et al. (1988) Frequency of fimbriation of nontypeable Haemophilus influenzae and its ability to adhere to chinchilla and human respiratory epithelium. Infect Immun 56: 331-335.
57. Sirakova T, Kolattukudy PE, Murwin D, Billy J, Leake E, et al. (1994) Role of fimbriae expressed by nontypeable Haemophilus influenzae in pathogenesis of and protection against otitis media and relatedness of the fimbrin subunit to outer membrane protein A. Infect Immun 62: 2002-2020.
58. Luke NR, Howlett AJ, Shao J, Campagnari AA, (2004) Expression of type IV pili by Moraxella catarrhalis is essential for natural competence and is affected by iron limitation. Infect Immun 72: 6262-6270.
59. Bakaletz LO, Daniels RL, Lim DJ, (1993) Modeling adenovirus type 1-induced otitis media in the chinchilla: effect on ciliary activity and fluid transport function of Eustachian tube mucosal epithelium. J Infect Dis 168: 865-872.
60. Miyamoto N, Bakaletz LO, (1997) Kinetics of the ascension of NTHi from the nasopharynx to the middle ear coincident with adenovirus-induced compromise in the chinchilla. Microb Pathog 23: 119-126.
61. Giebink GS, Berzins IK, Marker SC, Schiffman G, (1980) Experimental otitis media after nasal inoculation of Streptococcus pneumoniae and influenza A virus in chinchillas. Infect Immun 30: 445-450.
62. Giebink GS, (1999) Otitis media: the chinchilla model. Microb Drug Resist 5: 57-72.
63. Balder R, Krunkosky TM, Nguyen CQ, Feezel L, Lafontaine ER, (2009) Hag mediates adherence of Moraxella catarrhalis to ciliated human airway cells. Infect Immun 77: 4597-4608.
64. Labout JA, Duijts L, Lebon A, de Groot R, Hofman A, et al. (2011) Risk factors for otitis media in children with special emphasis on the role of colonization with bacterial airway pathogens: the Generation R study. Eur J Epidemiol 26: 61-66.
65. Casey JR, Pichichero ME, (2004) Changes in frequency and pathogens causing acute otitis media in 1995-2003. Pediatr Infect Dis J 23: 824-828.
66. Tan TT, Morgelin M, Forsgren A, Riesbeck K, (2007) Haemophilus influenzae survival during complement-mediated attacks is promoted by Moraxella catarrhalis outer membrane vesicles. J Infect Dis 195: 1661-1670.
67. Schaar V, Nordstrom T, Morgelin M, Riesbeck K, (2011) Moraxella catarrhalis outer membrane vesicles carry beta-lactamase and promote survival of Streptococcus pneumoniae and Haemophilus influenzae by inactivating amoxicillin. Antimicrob Agents Chemother 55: 3845-3853.
68. VandeWoude SJ, Luzarraga MB, (1991) The role of Branhamella catarrhalis in the "bloody-nose syndrome" of cynomolgus macaques. Lab Anim Sci 41: 401-406.
69. Embers ME, Doyle LA, Whitehouse CA, Selby EB, Chappell M, et al. (2011) Characterization of a Moraxella species that causes epistaxis in macaques. Vet Microbiol 147: 367-375.
70. Thornton RB, Rigby PJ, Wiertsema SP, Filion P, Langlands J, et al. (2011) Multi-species bacterial biofilm and intracellular infection in otitis media. BMC Pediatr 11: 94.