Chinchilla as a robust, reproducible and polymicrobial model of otitis media and its prevention

Expert Review of Vaccines

Volumn 8, Issue 8, 2009, Pages 1063-1082

  Bakaletz, Lauren O ^a  

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

Author keywords

Biofilm; Coinfection superinfection; Eustachian tube; Middle ear; Moraxella catarrhalis; Nasopharyngeal colonization; Nontypeable Haemophilus influenzae; Streptococcus pneumoniae; Tubotympanum; Upper respiratory tract virus

Indexed keywords

PNEUMOCOCCUS VACCINE; VACCINE;

BACTERIAL INFECTION; BIOFILM; CHINCHILLA; CLINICAL TRIAL; CORRELATION ANALYSIS; DISEASE MODEL; GOLD STANDARD; HUMAN; IMMUNE RESPONSE; IN VITRO STUDY; MICROORGANISM; MIXED INFECTION; NONHUMAN; OTITIS MEDIA; PEDIATRICS; PRIORITY JOURNAL; REVIEW; SUPERINFECTION; VIRUS INFECTION;

ANIMALS; BACTERIAL INFECTIONS; CHINCHILLA; DISEASE MODELS, ANIMAL; HUMANS; OTITIS MEDIA;

EID: 68049132805     PISSN: 14760584     EISSN: 17448395     Source Type: Journal    
DOI: 10.1586/erv.09.63     Document Type: Review

References (144)

1. Jakab GJ. Viral-bacterial interactions in pulmonary infection. Adv. Vet. Sci. Comp. Med. 26, 155-171 (1982).
2. McIntosh K, Halonen P, Ruuskanen O. Report of a workshop on respiratory viral infections: epidemiology, diagnosis, treatment, and prevention. Clin. Infect. Dis. 16(1), 151-164 (1993).
3. Mackowiak PA. Microbial synergism in human infections (first of two parts). N. Engl. J. Med. 298(1), 21-26 (1978).
4. Paap CM. Management of otitis media with effusion in young children. Ann. Pharmacother. 30(11), 1291-1297 (1996).
5. Auinger P, Lanphear BP, Kalkwarf HJ, Mansour ME. Trends in otitis media among children in the United States. Pediatrics 112(3 Pt 1), 514-520 (2003).
6. 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. 8, 23 (2008).
7. Woodfield G, Dugdale A. Evidence behind the WHO guidelines: hospital care for children: what is the most effective antibiotic regime for chronic suppurative otitis media in children? J. Trop. Pediatr. 54(3), 151-156 (2008).
8. Baldwin RL. Effects of otitis media on child development. Am. J. Otol. 14(6), 601-604 (1993).
9. Hunter LL, Margolis RH, Giebink GS. Identification of hearing loss in children with otitis media. Ann. Otol. Rhinol. Laryngol. Suppl. 163, 59-61 (1994).
10. Infante-Rivard C, Fernandez A. Otitis media in children: frequency, risk factors, and research avenues. Epidemiol. Rev. 15(2), 444-465 (1993).
11. Teele DW, Klein JO, Chase C, Menyuk P, Rosner BA. 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(3), 685-694 (1990).
12. Alsarraf R, Jung CJ, Perkins J, Crowley C, Alsarraf NW, Gates GA. Measuring the indirect and direct costs of acute otitis media. Arch. Otolaryngol. Head Neck Surg. 125(1), 12-18 (1999).
13. Cassell GH. New and reemerging infectious diseases: a global crisis and immediate threat to the nation's health: the role of research. American Society for Microbiology, Washington, DC, USA (1997).
14. Kaplan B, Wandstrat TL, Cunningham JR. Overall cost in the treatment of otitis media. Pediatr. Infect. Dis. J. 16(2 Suppl.), S9-S11 (1997).
15. Stool SE, Berg AO, Berman S et al. Otitis Media with Effusion in Young Children. Clinical Practice Guideline. Agency for Health Care Policy and Research, Public Health Service, US Department of Health and Human Services, Rockville, MD, USA (1994).
16. Giebink GS. The microbiology of otitis media. Pediatr. Infect. Dis. J. 8(1 Suppl.), S18-S20 (1989).
17. Hament JM, Kimpen JL, Fleer A, Wolfs TF. Respiratory viral infection predisposing for bacterial disease: a concise review. FEMS Immunol. Med. Microbiol. 26(3-4), 189-195 (1999).
18. Hayden FG. Influenza virus and rhinovirus-related otitis media: potential for antiviral intervention. Vaccine 19(Suppl. 1), S66-S70 (2000).
19. Heikkinen T. The role of respiratory viruses in otitis media. Vaccine 19(Suppl. 1), S51-S55 (2000).
20. Heikkinen T. Role of viruses in the pathogenesis of acute otitis media. Pediatr. Infect. Dis. J. 19(5 Suppl.), S17-S22; discussion S22-S23 (2000).
21. Heikkinen T, Chonmaitree T. Viral-bacterial synergy in otitis media: implications for management. Curr. Infect. Dis. Rep. 2(2), 154-159 (2000). • Discusses how the viral-bacterial synergy operational in the pathogenesis of otitis media (OM) has implications for how this highly prevalent pediatric disease is managed medically.
22. Ruuskanen O, Arola M, Putto-Laurila A et al. Acute otitis media and respiratory virus infections. Pediatr. Infect. Dis. J. 8(2), 94-99 (1989).
23. Ruuskanen O, Heikkinen T. Viral-bacterial interaction in acute otitis media. Pediatr. Infect. Dis. J. 13(11), 1047-1049 (1994).
24. Kvaerner KJ, Nafstad P, Hagen J, Mair IW, Jaakkola JJ. Early acute otitis media: determined by exposure to respiratory pathogens. Acta. Otolaryngol. Suppl. 529, 14-18 (1997).
25. Paradise JL, Rockette HE, Colborn DK et al. Otitis media in 2253 Pittsburgh-area infants: prevalence and risk factors during the first two years of life. Pediatrics 99(3), 318-333 (1997).
26. Daly KA, Brown JE, Lindgren BR, Meland MH, Le CT, Giebink GS. Epidemiology of otitis media onset by six months of age. Pediatrics 103(6 Pt 1), 1158-1166 (1999).
27. Borriello G, Richards L, Ehrlich GD, Stewart PS. Arginine or nitrate enhances antibiotic susceptibility of Pseudomonas aeruginosa in biofilms. Antimicrob. Agents Chemother. 50(1), 382-384 (2006).
28. Borriello G, Werner E, Roe F, Kim AM, Ehrlich GD, Stewart PS. Oxygen limitation contributes to antibiotic tolerance of Pseudomonas aeruginosa in biofilms. Antimicrob. Agents Chemother. 48(7), 2659-2664 (2004).
29. Walters MC 3rd, Roe F, Bugnicourt A, Franklin MJ, Stewart PS. Contributions of antibiotic penetration, oxygen limitation, and low metabolic activity to tolerance of Pseudomonas aeruginosa biofilms to ciprofloxacin and tobramycin. Antimicrob. Agents Chemother. 47(1), 317-323 (2003).
30. Izano EA, Shah SM, Kaplan JB. Intercellular adhesion and biocide resistance in nontypeable Haemophilus influenzae biofilms. Microb. Pathog. 46(4), 207-213 (2009).
31. Rayner MG, Zhang Y, Gorry MC, Chen Y, Post JC, Ehrlich GD. Evidence of bacterial metabolic activity in culture-negative otitis media with effusion. JAMA 279(4), 296-299 (1998). •• Provided the first evidence of bacterial life within 'sterile' middle ear fluids, as opposed to simply residual bacterial by-products or antigens, when these investigators demonstrated the presence of short half-lived bacterial mRNA within these fluids. This study launched the novel paradigm that OM could include a biofilm component within the disease course.
32. Allegrucci M, Hu FZ, Shen K et al. Phenotypic characterization of Streptococcus pneumoniae biofilm development. J. Bacteriol. 188(7), 2325-2335 (2006).
33. Gallaher TK, Wu S, Webster P, Aguilera R. Identification of biofilm proteins in non-typeable Haemophilus influenzae. BMC Microbiol. 6, 65 (2006).
34. Murphy TF, Kirkham C. Biofilm formation by nontypeable Haemophilus influenzae: strain variability, outer membrane antigen expression and role of pili. BMC Microbiol. 2, 7 (2002).
35. Pearson MM, Laurence CA, Guinn SE, Hansen EJ. Biofilm formation by Moraxella catarrhalis in vitro: roles of the UspA1 adhesin and the Hag hemagglutinin. Infect. Immun. 74(3), 1588-1596 (2006).
36. Starner TD, Zhang N, Kim G, Apicella MA, McCray PB Jr. Haemophilus influenzae forms biofilms on airway epithelia: implications in cystic fibrosis. Am. J. Respir. Crit. Care Med. 174(2), 213-220 (2006).
37. West-Barnette S, Rockel A, Swords WE. Biofilm growth increases phosphorylcholine content and decreases potency of nontypeable Haemophilus influenzae endotoxins. Infect. Immun. 74(3), 1828-1836 (2006).
38. Bouchet V, Hood DW, Li J et al. Host-derived sialic acid is incorporated into Haemophilus influenzae lipopolysaccharide and is a major virulence factor in experimental otitis media. Proc. Natl Acad. Sci. USA 100(15), 8898-8903 (2003).
39. Daines DA, Bothwell M, Furrer J et al. Haemophilus influenzae luxS mutants form a biofilm and have increased virulence. Microb. Pathog. 39(3), 87-96 (2005).
40. Ehrlich GD, Veeh R, Wang X et al. Mucosal biofilm formation on middle-ear mucosa in the chinchilla model of otitis media. JAMA 287(13), 1710-1715 (2002). • First publication to show that when bacteria were inoculated into the middle-ear cavity of the chinchilla, they induced the formation of mucosal biofilms.
41. Hall-Stoodley L, Hu FZ, Gieseke A et al. Direct detection of bacterial biofilms on the middle-ear mucosa of children with chronic otitis media. JAMA 296(2), 202-211 (2006). •• Provided the first evidence of bacteria residing within biofilm-like structures in association with respiratory epithelial cells recovered from the middle ears of children with chronic or recurrent OM. These epithelial cells with associated biofilms were recovered from middle ears that were culture negative but nonetheless PCR positive for one or more of the three predominant bacterial pathogens of OM.
42. Hong W, Mason K, Jurcisek J, Novotny L, Bakaletz LO, Swords WE. 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(2), 958-965 (2007).
43. Jurcisek J, Greiner L, Watanabe H, Zaleski A, Apicella MA, Bakaletz LO. Role of sialic acid and complex carbohydrate biosynthesis in biofilm formation by nontypeable Haemophilus influenzae in the chinchilla middle ear. Infect. Immun. 73(6), 3210-3218 (2005).
44. Swords WE, Moore ML, Godzicki L, Bukofzer G, Mitten MJ, VonCannon J. Sialylation of lipooligosaccharides promotes biofilm formation by nontypeable Haemophilus influenzae. Infect. Immun. 72(1), 106-113 (2004).
45. Hong W, Juneau RA, Pang B, Swords WE. Survival of bacterial biofilms within neutrophil extracellular traps promotes nontypeable Haemophilus influenzae persistence in the chinchilla model for otitis media. J. Innate Immun. 1(3), 215-224 (2009).
46. Reid SD, Hong W, Dew KE et al. Streptococcus pneumoniae forms surfaceattached communities in the middle ear of experimentally infected chinchillas. J. Infect. Dis. 199(6), 786-794 (2009).
47. Webster P, Wu S, Gomez G, Apicella M, Plaut AG, St Geme JW 3rd. Distribution of bacterial proteins in biofilms formed by non-typeable Haemophilus influenzae. J. Histochem. Cytochem. 54(7), 829-842 (2006).
48. Jurcisek JA, Bakaletz LO. Biofilms formed by nontypeable Haemophilus influenzae in vivo contain both double-stranded DNA and type IV pilin protein. J. Bacteriol. 189(10), 3868-3875 (2007).
49. Hong W, Pang B, West-Barnette S, Swords WE. Phosphorylcholine expression by nontypeable Haemophilus influenzae correlates with maturation of biofilm communities in vitro and in vivo. J. Bacteriol. 189(22), 8300-8307 (2007).
50. Greiner LL, Watanabe H, Phillips NJ et al. Nontypeable Haemophilus influenzae strain 2019 produces a biofilm containing N-acetylneuraminic acid that may mimic sialylated O-linked glycans. Infect. Immun. 72(7), 4249-4260 (2004).
51. Pang B, Winn D, Johnson R et al. Lipooligosaccharides containing phosphorylcholine delay pulmonary clearance of nontypeable Haemophilus influenzae. Infect. Immun. 76(5), 2037-2043 (2008).
52. Fujita K, Hirano T, Kodama S, Suzuki M. Prognostic impact of phosphorylcholine expression in nontypeable Haemophilus influenzae in otitis media with effusion. Acta Otolaryngol. 1-7 (2008) (Epub ahead of print).
53. Janson H, Carl n B, Cervin A et al. Effects on the ciliated epithelium of protein D-producing and -nonproducing nontypeable Haemophilus influenzae in nasopharyngeal tissue cultures. J. Infect. Dis. 180(3), 737-746 (1999).
54. Weiser JN, Shchepetov M, Chong ST. Decoration of lipopolysaccharide with phosphorylcholine: a phase-variable characteristic of Haemophilus influenzae. Infect. Immun. 65(3), 943-950 (1997).
55. Fan X, Pericone CD, Lysenko E, Goldfine H, Weiser JN. Multiple mechanisms for choline transport and utilization in Haemophilus influenzae. Mol. Microbiol. 50(2), 537-548 (2003).
56. Fox KL, Li J, Schweda EK et al. Duplicate copies of lic1 direct the addition of multiple phosphocholine residues in the lipopolysaccharide of Haemophilus influenzae. Infect. Immun. 76(2), 588-600 (2008).
57. Swords WE, Ketterer MR, Shao J, Campbell CA, Weiser JN, Apicella MA. Binding of the non-typeable Haemophilus influenzae lipooligosaccharide to the PAF receptor initiates host cell signalling. Cell Microbiol. 3(8), 525-536 (2001).
58. Moxon ER, Sweetman WA, Deadman ME, Ferguson DJ, Hood DW. Haemophilus influenzae biofilms: hypothesis or fact? Trends Microbiol. 16(3), 95-100 (2008).
59. Apicella MA. Bacterial otitis media, the chinchilla middle ear, and biofilms. J. Infect. Dis. 199(6), 774-775 (2009).
60. Slinger R, Chan F, Ferris W et al. Multiple combination antibiotic susceptibility testing of nontypeable Haemophilus influenzae biofilms. Diagn. Microbiol. Infect. Dis, 56(3), 247-253 (2006).
61. DeMaria TF. Animal models for nontypable Haemophilus influenzae otitis media. Pediatr. Infect. Dis. J. 8(1 Suppl.), S40-S42 (1989).
62. Doyle WJ. Animal models of otitis media: other pathogens. Pediatr. Infect. Dis. J. 8(1 Suppl.), S45-S47 (1989).
63. Lim DJ, Hermansson A, Hellstrom SO et al. Recent advances in otitis media. 3. Animal models; anatomy and pathology; pathogenesis; cell biology and genetics. Ann. Otol. Rhinol. Laryngol. Suppl. 194, 31-41 (2005).
64. Juhn SK, Tolan CJ, Antonelli PJ, Giebink GS, Goycoolea MV. The significance of experimental animal studies in otitis media. Otolaryngol. Clin. North Am. 24(4), 813-827 (1991).
65. Giebink GS. Otitis media: the chinchilla model. Microb. Drug Resist. 5(1), 57-72 (1999).
66. Harrison JM, Irving R. Visual and nonvisual auditory systems in mammals. Anatomical evidence indicates two kinds of auditory pathways and suggests two kinds of hearing in mammals. Science 154(750), 738-743 (1966).
67. Henderson D. Temporal summation of acoustic signals by the chinchilla. J. Acoust. Soc. Am. 46(2), 474-475 (1969).
68. Miller JD. Audibility curve of the chinchilla. J. Acoust. Soc. Am. 48(2), 513-523 (1970).
69. Margolis RH, Schachern PL, Hunter LL, Sutherland C. Multifrequency tympanometry in chinchillas. Audiology 34(5), 232-247 (1995).
70. Giebink GS, Payne EE, Mills EL, Juhn SK, Quie PG. Experimental otitis media due to Streptococcus pneumoniae: immunopathogenic response in the chinchilla. J. Infect. Dis. 134(6), 595-604 (1976).
71. Giebink GS. The pathogenesis of pneumococcal otitis media in chinchillas and the efficacy of vaccination in prophylaxis. Rev. Infect. Dis. 3(2), 342-353 (1981). • Discusses how the conduct of preclinical trials in the chinchilla host supported development and licensure of a pediatric vaccine for the prevention of OM.
72. Giebink GS, Berzins IK, Marker SC, Schiffman G. Experimental otitis media after nasal inoculation of Streptococcus pneumoniae and influenza A virus in chinchillas. Infect. Immun. 30(2), 445-450 (1980). •• First demonstration of a polymicrobial model of experimental OM developed in the chinchilla host. These investigators clearly showed that pre-existing infection of the upper respiratory tract by influenza A virus predisposed the middle ear to invasion by Streptococcus pneumoniae.
73. Giebink GS, Wright PF. Different virulence of influenza A virus strains and susceptibility to pneumococcal otitis media in chinchillas. Infect. Immun. 41(3), 913-920 (1983).
74. Bakaletz LO, Daniels RL, Lim DJ. 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(4), 865-872 (1993).
75. Gitiban N, Jurcisek JA, Harris RH et al. Chinchilla and murine models of upper respiratory tract infections with respiratory syncytial virus. J. Virol. 79(10), 6035-6042 (2005).
76. Giebink GS, Kurono Y, Bakaletz LO et al. Recent advances in otitis media. 6. Vaccine. Ann. Otol. Rhinol. Laryngol. Suppl. 194, 86-103 (2005).
77. Green BA, Vazquez ME, Zlotnick GW et al. Evaluation of mixtures of purified Haemophilus influenzae outer membrane proteins in protection against challenge with nontypeable H. influenzae in the chinchilla otitis media model. Infect. Immun. 61(5), 1950-1957 (1993).
78. Giebink GS, Ripley ML, Wright PF. Eustachian tube histopathology during experimental influenza A virus infection in the chinchilla. Ann. Otol. Rhinol. Laryngol. 96(2 Pt 1), 199-206 (1987).
79. Chung MH, Griffith SR, Park KH, Lim DJ, DeMaria TF. Cytological and histological changes in the middle ear after inoculation of influenza A virus. Acta Otolaryngol. 113(1), 81-87 (1993).
80. Giebink GS. Studies of Streptococcus pneumoniae and influenza virus vaccines in the chinchilla otitis media model. Pediatr. Infect. Dis. J. 8(1 Suppl.), S42-S44 (1989).
81. Sirakova T, Kolattukudy PE, Murwin D et al. 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(5), 2002-2020 (1994).
82. Suzuki K, Bakaletz LO. Synergistic effect of adenovirus type 1 and nontypeable Haemophilus influenzae in a chinchilla model of experimental otitis media. Infect. Immun. 62(5), 1710-1718 (1994).
83. Bakaletz LO. Otitis Media. Polymicrobial Diseases. Brogden KA, Guthmiller JM (Eds). ASM Press, Washington, DC, USA, 259-298 (2002).
84. Giebink GS. Vaccination against middle-ear bacterial and viral pathogens. Ann. NY Acad. Sci. 830, 330-352 (1997).
85. Miyamoto N, Bakaletz LO. Kinetics of the ascension of NTHi from the nasopharynx to the middle ear coincident with adenovirus-induced compromise in the chinchilla. Microb. Pathog. 23(2), 119-126 (1997).
86. Bakaletz LO, Murwin DM, Billy JM. Adenovirus serotype 1 does not act synergistically with Moraxella (Branhamella) catarrhalis to induce otitis media in the chinchilla. Infect. Immun. 63(10), 4188-4190 (1995).
87. Tong HH, Fisher LM, Kosunick GM, DeMaria TF. Effect of adenovirus type 1 and influenza A virus on Streptococcus pneumoniae nasopharyngeal colonization and otitis media in the chinchilla. Ann. Otol. Rhinol. Laryngol. 109(11), 1021-1027 (2000).
88. Peltola VT, Boyd KL, McAuley JL, Rehg JE, McCullers JA. Bacterial sinusitis and otitis media following influenza virus infection in ferrets. Infect. Immun. 74(5), 2562-2567 (2006).
89. Wadowsky RM, Mietzner SM, Skoner DP, Doyle WJ, Fireman P. Effect of experimental influenza A virus infection on isolation of Streptococcus pneumoniae and other aerobic bacteria from the oropharynges of allergic and nonallergic adult subjects. Infect. Immun. 63(4), 1153-1157 (1995).
90. Heikkinen T, Thint M, Chonmaitree T. Prevalence of various respiratory viruses in the middle ear during acute otitis media (see comments). N. Engl. J. Med. 340(4), 260-264 (1999).
91. Morens DM, Taubenberger JK, Fauci AS. Predominant role of bacterial pneumonia as a cause of death in pandemic influenza: implications for pandemic influenza preparedness. J. Infect. Dis. 198(7), 962-970 (2008).
92. Bakaletz LO. Viral potentiation of bacterial superinfection of the respiratory tract. Trends Microbiol. 3(3), 110-114 (1995).
93. Avadhanula V, Rodriguez CA, Devincenzo JP et al. Respiratory viruses augment the adhesion of bacterial pathogens to respiratory epithelium in a viral species- and cell type-dependent manner. J. Virol. 80(4), 1629-1636 (2006).
94. Griffiths NJ, Bradley CJ, Heyderman RS, Virji M. IFN-g amplifies NFkB-dependent Neisseria meningitidis invasion of epithelial cells via specific upregulation of CEArelated cell adhesion molecule 1. Cell Microbiol. 9(12), 2968-2983 (2007).
95. Avadhanula V, Wang Y, Portner A, Adderson E. Nontypeable Haemophilus influenzae and Streptococcus pneumoniae bind respiratory syncytial virus glycoprotein. J. Med. Microbiol. 56(Pt 9), 1133-1137 (2007).
96. Proud D, Sanders SP, Wiehler S. Human rhinovirus infection induces airway epithelial cell production of human b-defensin 2 both in vitro and in vivo. J. Immunol. 172(7), 4637-4645 (2004).
97. McGillivary G, Ray WC, Bevins CL, Munson RS Jr, Bakaletz LO. A member of the cathelicidin family of antimicrobial peptides is produced in the upper airway of the chinchilla and its mRNA expression is altered by common viral and bacterial co-pathogens of otitis media. Mol. Immunol. 44(9), 2446-2458 (2007).
98. McGillivary G, Mason KM, Jurcisek JA, Peeples ME, Bakaletz LO. RSV-induced dysregulation of expression of a mucosal b-defensin augments colonization of the upper airway by nontypeable Haemophilus influenzae. Cell Microbiol. (2009) (In Press).
99. McCullers JA. Insights into the interaction between influenza virus and pneumococcus. Clin. Microbiol. Rev. 19(3), 571-582 (2006).
100. Novotny LA, Bakaletz LO. The fourth surface-exposed region of the outer membrane protein P5-homologous adhesin of nontypable Haemophilus influenzae is an immunodominant but nonprotective decoying epitope. J. Immunol. 171(4), 1978-1983 (2003).
101. Poolman JT, Bakaletz L, Cripps A et al. Developing a nontypeable Haemophilus influenzae (NTHi) vaccine. Vaccine 19(Suppl. 1), S108-S115 (2000).
102. Kyd J, Cripps A. Nontypeable Haemophilus influenzae: challenges in developing a vaccine. J. Biotechnol. 73(2-3), 103-108 (1999).
103. Bakaletz LO, Kennedy BJ, Novotny LA, Duquesne G, Cohen J, Lobet Y. 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(6), 2746-2762 (1999).
104. Kennedy BJ, Novotny LA, Jurcisek JA, Lobet Y, Bakaletz LO. 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(5), 2756-2765 (2000).
105. Braun LE, Sutter DE, Eichelberger MC et al. Co-infection of the cotton rat (Sigmodon hispidus) with Staphylococcus aureus and influenza A virus results in synergistic disease. Microb. Pathog. 43(5-6), 208-216 (2007).
106. Jurcisek JA, Durbin JE, Kusewitt DF, Bakaletz LO. Anatomy of the nasal cavity in the chinchilla. Cells Tissues Organs 174(3), 136-152 (2003).
107. Jossart GH, Erdmann GR, Levitt DG et al. An experimental model for measuring middle ear antimicrobial drug penetration in otitis media. Pharm. Res. 7(12), 1242-1247 (1990).
108. Hiraide F, Inouye T. The fine surface view of the human adult Eustachian tube. J. Laryngol. Otol. 97(2), 149-157 (1983).
109. Doyle WJ. Eustachian tube function in the chinchilla. Arch. Otolaryngol. 111(5), 305-308 (1985).
110. Matsune S, Sando I, Takahashi H. Distributions of Eustachian tube goblet cells and glands in children with and without otitis media. Ann. Otol. Rhinol. Laryngol. 101(9), 750-754 (1992).
111. Sando I, Takahashi H, Aoki H, Matsune S. Mucosal folds in human Eustachian tube: a hypothesis regarding functional localization in the tube. Ann. Otol. Rhinol. Laryngol. 102(1 Pt 1), 47-51 (1993).
112. Sando I, Takahashi H, Matsune S, Aoki H. Localization of function in the Eustachian tube: a hypothesis. Ann. Otol. Rhinol. Laryngol. 103(4 Pt 1), 311-314 (1994).
113. Sabirov A, Metzger DW. Mouse models for the study of mucosal vaccination against otitis media. Vaccine 26(12), 1501-1524 (2008).
114. Means LW, Daniel HJ, Jordan LH, Loesche PJ. Nonsusceptibility to otitis media of the laboratory gerbil. Meriones unguiculatus. Physiol. Psychol. 3, 229-230 (1975).
115. Thompson TA, Gardner D, Fulghum RS et al. Indigenous nasopharyngeal, auditory canal, and middle ear bacterial flora of gerbils: animal model for otitis media. Infect. Immun. 32(3), 1113-1118 (1981).
116. Wells JR, Gernon WH, Ward G, Davis RK, Hays LL. Otosurgical model in the guinea pig (Cavia porcellus). Otolaryngol. Head Neck Surg. 95(4), 450-457 (1986).
117. Daniel HJ, Carmine FH, Cook RA. Otitis media in two strains of laboratory rats. J. Aud. Res. 11, 276-278 (1971).
118. Daniel HJ, Means LW, Dressel ME, Loesche PJ. Otitis media in laboratory rats. Physiol. Psychol. 1, 7-8 (1973).
119. Chung MH, Enrique R, Lim DJ, De Maria TF. Moraxella (Branhamella) catarrhalis-induced experimental otitis media in the chinchilla. Acta Otolaryngol. 114(4), 415-422 (1994).
120. Hu WG, Chen J, Collins FM, Gu XX. An aerosol challenge mouse model for Moraxella catarrhalis. Vaccine 18(9-10), 799-804 (1999).
121. Unhanand M, Maciver I, Ramilo O et al. Pulmonary clearance of Moraxella catarrhalis in an animal model. J. Infect. Dis. 165(4), 644-650 (1992).
122. Westman EB, Hermansson A, Prellner K, Melhus A, Hellstrom S. Moraxella catarrhalis-Induced Purulent Otitis Media In The Rat Middle Ear. Takasaka T (Ed.). Kugler Publications, Oita, Japan, 193-195 (1994).
123. Luke NR, Jurcisek JA, Bakaletz LO, Campagnari AA. Contribution of Moraxella catarrhalis type IV pili to nasopharyngeal colonization and biofilm formation. Infect. Immun. 75(12), 5559-5564 (2007).
124. Novotny LA, Partida-Sanchez S, Munson RS Jr, Bakaletz LO. Differential uptake and processing of a Haemophilus influenzae P5-derived immunogen by chinchilla dendritic cells. Infect. Immun. 76(3), 967-977 (2008).
125. Figueira MA, Ram S, Goldstein R, Hood DW, Moxon ER, Pelton SI. Role of complement in defense of the middle ear revealed by restoring the virulence of nontypeable Haemophilus influenzae siaB mutants. Infect. Immun. 75(1), 325-333 (2007).
126. Giebink GS, Koskela M, Vella PP, Harris M, Le CT. Pneumococcal capsular polysaccharide-meningococcal outer membrane protein complex conjugate vaccines: immunogenicity and efficacy in experimental pneumococcal otitis media. J. Infect. Dis. 167(2), 347-355 (1993).
127. Sato K, Quartey MK, Liebeler CL, Le CT, Giebink GS. Roles of autolysin and pneumolysin in middle ear inflammation caused by a type 3 Streptococcus pneumoniae strain in the chinchilla otitis media model. Infect. Immun. 64(4), 1140-1145 (1996).
128. Johnson MD, Fitzgerald JE, Leonard G, Burleson JA, Kreutzer DL. Cytokines in experimental otitis media with effusion. Laryngoscope 104(2), 191-196 (1994).
129. Bookwalter JE, Jurcisek JA, Gray- Owen SD, Fernandez S, McGillivary G, Bakaletz LO. A carcinoembryonic antigen-related cell adhesion molecule 1 homologue plays a pivotal role in nontypeable Haemophilus influenzae colonization of the chinchilla nasopharynx via the outer membrane protein P5- homologous adhesin. Infect. Immun. 76(1), 48-55 (2008).
130. Harris RH, Wilk D, Bevins CL, Munson RS Jr, Bakaletz LO. Identification and characterization of a mucosal antimicrobial peptide expressed by the chinchilla (Chinchilla lanigera) airway. J. Biol. Chem. 279(19), 20250-20256 (2004).
131. Kerschner JE, Meyer TK, Burrows A, Ehrlich G, Post JC. Mucin gene cDNA sequence characterization in chinchilla middle ear epithelium. Int. J. Pediatr. Otorhinolaryngol. 70(8), 1449-1456 (2006).
132. Kerschner JE, Erdos G, Hu FZ et al. Characterization of normal and Haemophilus influenzae-infected mucosal cDNA libraries in chinchilla middle ear mucosa. Ann. Otol. Rhinol. Laryngol. (2008) (In Press).
133. Polasik D, Kmiec M, Liefers S, Terman A. Single nucleotide polymorphisms in exon 10 of the chinchilla growth hormone receptor (GHR) gene. J. Appl. Genet. 46(4), 403-406 (2005).
134. Bakaletz LO. Developing animal models for polymicrobial diseases. Nat. Rev. Microbiol. 2(7), 552-568 (2004).
135. Harrison A, Dyer DW, Gillaspy A et al. Genomic sequence of an otitis media isolate of nontypeable Haemophilus influenzae: comparative study with H. influenzae serotype D, strain KW20. J. Bacteriol. 187(13), 4627-4636 (2005).
136. Teele DW, Klein JO, Rosner BA. Epidemiology of otitis media in children. Ann. Otol. Rhinol. Laryngol. Suppl. 89(3 Pt 2), 5-6 (1980).
137. Novotny LA, Jurcisek JA, Godfroid F, Poolman JT, Denoel PA, Bakaletz LO. 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(22), 4804-4811 (2006).
138. Prymula R, Peeters P, Chrobok V et al. Pneumococcal capsular polysaccharides conjugated to protein D for prevention of acute otitis media caused by both Streptococcus pneumoniae and non-typable Haemophilus influenzae: a randomised double-blind efficacy study. Lancet 367(9512), 740-748 (2006). •• First study to demonstrate that one could immunize children parenterally with an antigen derived from nontypeable H. influenzae and prevent the development of OM due to H. influenzae. This study re-energized the field of vaccine development efforts for the prevention of NTHI-induced OM.
139. Prymula R, Peeters P, Chrobok V et al. An eleven-valent pneumococcal-protein D conjugate (11pn-PD) vaccine protects against otitis caused by both pneumococci or Haemophilus influenzae. Presented at: 23rd Annual Meeting of the European Society for Paediatric Infectious Diseases - ESPID. Valencia, Spain, 18-20 May 2005.
140. Forsgren A, Riesbeck K, Janson H. Protein D of Haemophilus influenzae: a protective nontypeable H. influenzae antigen and a carrier for pneumococcal conjugate vaccines. Clin. Infect. Dis. 46(5), 726-731 (2008).
141. Palmu A, Jokinen J, Kilpi T. Impact of different case definitions for acute otitis media on the efficacy estimates of a pneumococcal conjugate vaccine. Vaccine 26(20), 2466-2470 (2008).
142. Toropainen M, Raitolehto A, Henckaerts I et al. Pneumococcal Haemophilus influenzae protein D conjugate vaccine induces antibodies that inhibit glycerophosphodiester phosphodiesterase activity of protein D. Infect. Immun. 76(10), 4546-4553 (2008).
143. Novotny LA, Bakaletz LO, Poolman J, Denoel PA. 10-valent pneumococcal protein-D conjugate vaccine induces protection against NTHi-induced otitis media in a chinchilla model. Presented at: 1st International Workshop on Haemophilus influenzae and Moraxella catarrhalis. Rotterdam, The Netherlands, 16-17 May 2008.
144. Park K, Bakaletz, LO, Coticchia JM, Lim DJ. Effect of influenza A virus on ciliary activity and dye transport function in the chinchilla Eustachian tube. Ann. Otol. Rhinol. Laryngol. 102(7), 551-558 (1993).