Vaccine development for non-typeable Haemophilus influenzae and Moraxella catarrhalis: progress and challenges

References

• Stenfors LE, Raisanen S. Quantitative analysis of the bacterial findings in otitis media. J. Laryngol. Otol. 104, 749–757 (1990).
   PubMed Web of Science ®Google Scholar
• Gan VN, Kusmiesz H, Shelton S, Nelson JD. Comparative evaluation of loracarbef and amoxicillin-clavulanate for acute otitis media. Antimicrob. Agents Chemother. 35, 967–971 (1991).
   PubMed Web of Science ®Google Scholar
• Johnson CE, Carlin SA, Super DM et al. Cefixime compared with amoxicillin for treatment of acute otitis media. J. Pediatr. 119, 117–122 (1991).
   PubMedGoogle Scholar
• Faden H, Bernstein J, Stanievich J, Brodsky L, Ogra PL. Effect of prior antibiotic treatment on middle ear disease in children. Ann. Otol. Rhinol. Laryngol. 101, 87–91 (1992).
   PubMed Web of Science ®Google Scholar
• Del Beccaro MA, Mendelman PM, Inglis AF et al. Bacteriology of acute otitis media: a new perspective. J. Pediatr. 120, 81–84 (1992).
   PubMed Web of Science ®Google Scholar
• Chonmaitree T, Owen MJ, Patel JA, Hedgpeth D, Horlick D, Howie VM. Effect of viral respiratory tract infection on outcome of acute otitis media. J. Pediatr. 120,586–862 (1992).
   Google Scholar
• Owen MJ, Anwar R, Nguyen HK, Swank PR, Bannister ER, Howie VM. Efficacy of cefixime in the treatment of acute otitis media in children. Am. J. Dis. Child. 147, 81–86 (1993).
   PubMedGoogle Scholar
• Aspin MM, Hoberman A, McCarty J et al. Comparative study of the safety and efficacy of clarithromycin and amoxicillin–clavulanate in the treatment of acute otitis media in children. J. Pediatr. 125, 135–141 (1994).
   Google Scholar
• Gehanno P, Lenoir G, Barry B, Bons J, Boucot I, Berche P. Evaluation of nasopharyngeal cultures for bacteriologic assessment of acute otitis media in children. Pediatr. Infect. Dis. J. 15, 329–332 (1996).
   PubMedGoogle Scholar
• Dagan R, Leibovitz E, Greenberg D, Yagupsky P, Fliss DM, Leiberman A. Early eradication of pathogens from middle ear fluid during antibiotic treatment of acute otitis media is associated with improved clinical outcome. Pediatr. Infect. Dis. J. 17, 776–782 (1998).
   PubMed Web of Science ®Google Scholar
• Block SL, Hedrick JA, Kratzer J, Nemeth MA, Tack KJ. Five-day twice daily cefdinir therapy for acute otitis media: microbiologic and clinical efficacy. Pediatr. Infect. Dis. J. 19(S12), S153–S158 (2000).
   PubMed Web of Science ®Google Scholar
• Block SL, McCarty JM, Hedrick JA et al. Comparative safety and efficacy of cefdinir vs amoxicillin/clavulanate for treatment of suppurative acute otitis media in children. Pediatr. Infect. Dis. J. 19, S159–S165 (2000).
   PubMed Web of Science ®Google Scholar
• Kilpi T, Herva E, Kaijalainen T, Syrjanen R, Takala AK. Bacteriology of acute otitis media in a cohort of Finnish children followed for the first two years of life. Pediatr. Infect. Dis. J. 20(7), 654–662 (2001).
   PubMed Web of Science ®Google Scholar
• Casey JR, Pichichero ME. Changes in frequency and pathogens causing acute otitis media in 1995–2003. Pediatr. Infect. Dis. J. 23(9), 824–828 (2004).
   PubMed Web of Science ®Google Scholar
• Leibovitz E, Jacobs MR, Dagan R. Haemophilus influenzae: a significant pathogen in acute otitis media. Pediatr. Infect. Dis. J. 23(12), 1142–1152 (2004).
   PubMed Web of Science ®Google Scholar
• 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. 35, 2854–2858 (1997).
   PubMed Web of Science ®Google Scholar
• Hendolin PH, Paulin L, Ylikoski J. Clinically applicable multiplex PCR for four middle ear pathogens. J. Clin. Microbiol. 38, 125–132 (2000).
   PubMed Web of Science ®Google Scholar
• Post JC, Preston RA, Aul JJ et al. Molecular analysis of bacterial pathogens in otitis media with effusion. JAMA 273, 1598–1604 (1995).
   PubMed Web of Science ®Google Scholar
• Faden H. The microbiologic and immunologic basis for recurrent otitis media in children. Eur. J. Pediatr. 160(7), 407–413 (2001).
   PubMed Web of Science ®Google Scholar
• Sethi S, Murphy TF. Bacterial infection in chronic obstructive pulmonary disease in 2000. A state of the art review. Clin. Microbiol. Rev. 14(2), 336–363 (2001).
   PubMed Web of Science ®Google Scholar
• Wilson R. The role of infection in COPD. Chest 113, S242–S248 (1998).
   PubMed Web of Science ®Google Scholar
• Wilson R. Evidence of bacterial infection in acute exacerbations of chronic bronchitis. Respir. Infect. 15(3), 208–215 (2000).
   PubMedGoogle Scholar
• Christensen JJ. Moraxella (Branhamella) catarrhalis: clinical, microbiological and immunological features in lower respiratory tract infections. APMIS 107(Suppl.), 1–36 (1999).
   Google Scholar
• Enright MC, McKenzie H. Moraxella (Branhamella) catarrhalis – clinical and molecular aspects of a rediscovered pathogen. J. Med. Microbiol. 46, 360–371 (1997).
   PubMed Web of Science ®Google Scholar
• Fagon JY, Chastre J, Trouillet JL et al. Characterization of distal bronchial microflora during acute exacerbation of chronic bronchitis. Am. Rev. Respir. Dis. 142, 1004–1008 (1990).
   PubMed Web of Science ®Google Scholar
• Monso E, Ruiz J, Rosell A et al. Bacterial infection in chronic obstructive pulmonary disease. A study of stable and exacerbated out-patients using the protected specimen brush. Am. J. Respir. Crit. Care Med. 152, 1316–1320 (1995).
   PubMed Web of Science ®Google Scholar
• Ninane G, Joly J, Kraytman M. Bronchopulmonary infection due to Branhamella catarrhalis: 11 cases assessed by transtracheal puncture. BMJ 1, 276–278 (1978).
   PubMed Web of Science ®Google Scholar
• Pela R, Marchesani F, Agostinelli C et al. Airways microbial flora in COPD patients in stable clinical conditions and during exacerbations: a bronchoscopic investigation. Monaldi Arch. Chest. Dis. 53, 262–267 (1998).
   PubMedGoogle Scholar
• Soler N, Torres A, Ewig S et al. Bronchial microbial patterns in severe exacerbations of chronic obstructive pulmonary disease (COPD) requiring mechanical ventilation. Am. J. Respir. Crit. Care Med. 157, 1498–1505 (1998).
   PubMed Web of Science ®Google Scholar
• Musher DM, Kubitschek KR, Crennan J, Baughn RE. Pneumonia and acute febrile tracheobronchitis due to Haemophilus influenzae. Ann. Intern. Med. 99, 444–450 (1983).
   PubMed Web of Science ®Google Scholar
• Sethi S, Wrona C, Grant BJ, Murphy TF. Strain-specific immune response to Haemophilus influenzae in chronic obstructive pulmonary disease. Am. J. Respir. Crit. Care Med. 169, 448–453 (2004).
   PubMed Web of Science ®Google Scholar
• Bakri F, Brauer AL, Sethi S, Murphy TF. Systemic and mucosal antibody response to Moraxella catarrhalis following exacerbations of chronic obstructive pulmonary disease. J. Infect. Dis. 185, 632–640 (2002).
   PubMed Web of Science ®Google Scholar
• Murphy TF, Brauer AL, Grant BJ, Sethi S. Moraxella catarrhalis in chronic obstructive pulmonary disease. Burden of disease and immune response. Am. J. Respir. Crit. Care Med. 172, 195–199 (2005).
   PubMed Web of Science ®Google Scholar
• Murphy TF, Brauer AL, Aebi C, Sethi S. Identification of surface antigens of Moraxella catarrhalis as targets of human serum antibody responses in chronic obstructive pulmonary disease. Infect. Immun. 73, 3471–3478 (2005).
   PubMed Web of Science ®Google Scholar
• Chapman AJ, Musher DM, Jonsson S, Clarridge JE, Wallace RJ. Development of bactericidal antibody during Branhamella catarrhalis infection. J. Infect. Dis. 151, 878–882 (1985).
   PubMed Web of Science ®Google Scholar
• Sethi S, Evans N, Grant BJB, Murphy TF. New strains of bacteria and exacerbations of chronic obstructive pulmonary disease. N. Engl. J. Med. 347, 465–471 (2002).
   PubMed Web of Science ®Google Scholar
• Sethi S, Muscarella K, Evans N, Klingman KL, Grant BJB, Murphy TF. Airway inflammation and etiology of acute exacerbations of chronic bronchitis. Chest 118, 1557–1565 (2000).
   PubMed Web of Science ®Google Scholar
• White AJ, Gompertz S, Bayley DL et al. Resolution of bronchial inflammation is related to bacterial eradication following treatment of exacerbations of chronic bronchitis. Thorax 58(8), 680–685 (2003).
   PubMed Web of Science ®Google Scholar
• Pentilla M, Savolainen S, Kuikaanniemi H, Forsblom B, Jousimies-Somer H. Bacterial findings in acute maxillary sinusitis – European study. Acta Otolaryngol. S529, 165–168 (1997).
   Google Scholar
• Talbot GH, Kennedy DW, Scheld WM, Granito K. Rigid nasal endoscopy versus sinus puncture and aspiration for microbiologic documentation of acute bacterial maxillary sinusitis. Clin. Infect. Dis. 33(10), 1668–1675 (2001).
   PubMed Web of Science ®Google Scholar
• Wald ER, Milmoe GJ, Bowen A, Ledesma-Medina J, Salamon N, Bluestone CD. Acute maxillary sinusitis in children. N. Engl. J. Med. 304, 749–754 (1981).
   PubMed Web of Science ®Google Scholar
• Wald ER. Microbiology of acute and chronic sinusitis in children and adults. Am. J. Med. Sci. 316(1), 13–20 (1998).
   PubMedGoogle Scholar
• Ghaffar F, Muniz LS, Katz K et al. Effects of large dosages of amoxicillin/clavulanate or azithromycin on nasopharyngeal carriage of Streptococcus pneumoniae, Haemophilus influenzae, nonpneumococcal α-hemolytic streptococci, and Staphylococcus aureus in children with acute otitis media. Clin. Infect. Dis. 34(10), 1301–1309 (2002).
   PubMed Web of Science ®Google Scholar
• Berkovitch M, Bulkowstein M, Zhovtis D et al. Colonization rate of bacteria in the throat of healthy infants. Int. J. Pediatr. Otorhinolaryngol. 63(1), 19–24 (2002).
   PubMedGoogle Scholar
• Marchisio P, Gironi S, Esposito S, Schito GC, Mannelli S, Principi N. Seasonal variations in nasopharyngeal carriage of respiratory pathogens in healthy Italian children attending day-care centres or schools. J. Med. Microbiol. 50(12), 1095–1099 (2001).
   PubMedGoogle Scholar
• Harabuchi Y, Kodama H, Faden H. Outcome of acute otitis media and its relation to clinical features and nasopharyngeal colonization at the time of diagnosis. Acta. Otolaryngol. 121(8), 908–914 (2001).
   PubMedGoogle Scholar
• Smith-Vaughan HC, McBroom J, Mathews JD. Modelling of endemic carriage of Haemophilus influenzae in Aboriginal infants in Northern Australia. FEMS Immunol. Med. Microbiol. 31(2), 137–143 (2001).
   PubMedGoogle Scholar
• Farjo RS, Foxman B, Patel MJ et al. Diversity and sharing of Haemophilus influenzae strains colonizing healthy children attending day-care centers. Pediatr. Infect. Dis. J. 23(1), 41–46 (2004).
   PubMedGoogle Scholar
• St Sauver J, Marrs CF, Foxman B, Somsel P, Madera R, Gilsdorf JR. Risk factors for otitis media and carriage of multiple strains of Haemophilus influenzae and Streptococcus pneumoniae. Emerg. Infect. Dis. 6(6), 622–630 (2000).
   PubMedGoogle Scholar
• Peerbooms PG, Engelen MN, Stokman DA et al. Nasopharyngeal carriage of potential bacterial pathogens related to day care attendance, with special reference to the molecular epidemiology of Haemophilus influenzae. J. Clin. Microbiol. 40(8), 2832–2836 (2002).
   PubMedGoogle Scholar
• Aniansson G, Alm B, Andersson B et al. Nasopharyngeal colonization during the first year of life. J. Infect. Dis. 165(S1), S38–S42 (1992).
   PubMed Web of Science ®Google Scholar
• Faden H, Harabuchi Y, Hong JJ. Epidemiology of Moraxella catarrhalis in children during the first 2 years of life: relationship to otitis media. J. Infect. Dis. 169, 1312–1317 (1994).
   PubMed Web of Science ®Google Scholar
• Vaneechoutte M, Verschraegen G, Claeys G, Weise B, Van Den Abeele AM. Respiratory tract carrier rates of Moraxella (Branhamella) catarrhalis in adults and children and interpretation of the isolation of M. catarrhalis from sputum. J. Clin. Microbiol. 28, 2674–2680 (1990).
   PubMed Web of Science ®Google Scholar
• Leach AJ, Boswell JB, Asche V, Nienhuys TG, Mathews JD. Bacterial colonization of the nasopharynx predicts very early onset and persistence of otitis media in Australian Aboriginal infants. Pediatr. Infect. Dis. J. 13, 983–989 (1994).
   PubMed Web of Science ®Google Scholar
• Faden H, Brodsky L, Waz MJ, Stanievich J, Bernstein J, Ogra PL. Nasopharyngeal flora in the first three years of life in normal and otitis-prone children. Ann. Otol. Rhinol. Laryngol. 100, 612–615 (1991).
   PubMed Web of Science ®Google Scholar
• Faden H, Duffy L, Wasielewski R et al. Relationship between nasopharyngeal colonization and the development of otitis media in children. J. Infect. Dis. 175, 1440–1445 (1997).
   PubMed Web of Science ®Google Scholar
• Harabuchi Y, Faden H, Yamanaka N et al. Nasopharyngeal colonization with nontypeable Haemophilus influenzae and recurrent otitis media. J. Infect. Dis. 170, 862–866 (1994).
   PubMed Web of Science ®Google Scholar
• Abe Y, Murphy TF, Sethi S et al. Lymphocyte proliferative response to P6 of Haemophilus influenzae is associated with relative protection from exacerbations of chronic obstructive pulmonary disease. Am. J. Respir. Crit. Care Med. 165(7), 967–971 (2002).
   PubMed Web of Science ®Google Scholar
• Murphy TF, Brauer AL, Schiffmacher AT, Sethi S. Persistent colonization by Haemophilus influenzae in chronic obstructive pulmonary disease. Am. J. Respir. Crit. Care Med. 170, 266–272 (2004).
   PubMed Web of Science ®Google Scholar
• Bandi V, Apicella MA, Mason E et al. Nontypeable Haemophilus influenzae in the lower respiratory tract of patients with chronic bronchitis. Am. J. Respir. Crit. Care Med. 164(11), 2114–2119 (2001).
   PubMed Web of Science ®Google Scholar
• Craig JE, Cliffe A, Garnett K, High NJ. Survival of nontypeable Haemophilus influenzae in macrophages. FEMS Microbiol. Lett. 203(1), 55–61 (2001).
   PubMed Web of Science ®Google Scholar
• Ketterer MR, Shao JQ, Hornick DB, Buscher B, Bandi VK, Apicella MA. Infection of primary human bronchial epithelial cells by Haemophilus influenzae: macropinocytosis as a mechanism of airway epithelial cell entry. Infect. Immun. 67, 4161–4170 (1999).
   PubMed Web of Science ®Google Scholar
• Forsgren J, Samuelson A, Ahlin A, Jonasson J, Rynnel-Dagoo B, Lindberg A. Haemophilus influenzae resides and multiplies intracellularly in human adenoid tissue as demonstrated by in situ hybridization and bacterial viability assay. Infect. Immunol. 62, 673–679 (1994).
   PubMed Web of Science ®Google Scholar
• Bakaletz LO, Kennedy B-J, 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, 2746–2762 (1999).
   PubMed Web of Science ®Google Scholar
• Bakaletz LO, Leake ER, Billy JM, Kaumaya PTP. Relative immunogenicity and efficacy of two synthetic chimeric peptides of fimbrin as vaccinogens against nasopharyngeal colonization by nontypeable Haemophilus influenzae in the chinchilla. Vaccine 15, 955–961 (1997).
   PubMed Web of Science ®Google Scholar
• Kyd JM, Cripps AW, Novotny LA, Bakaletz LO. 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. Immunol. 71(8), 4691–4699 (2003).
   PubMed Web of Science ®Google Scholar
• Morton DJ, Bakaletz LO, Jurcisek JA et al. 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(1), 25–33 (2004).
   PubMed Web of Science ®Google Scholar
• Suzuki K, Bakaletz LO. Synergistic effect of adenovirus Type 1 and nontypeable Haemophilus influenzae in a chinchilla model of experimental otitis media. Infect. Immunol. 62, 1710–1718 (1994).
   PubMedGoogle Scholar
• Barenkamp SJ. Immunization with high-molecular-weight adhesion proteins of nontypeable Haemophilus influenzae modifies experimental otitis media in chinchillas. Infect. Immunol. 64, 1246–1251 (1996).
   PubMed Web of Science ®Google Scholar
• 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. Immunol. 63, 4188–4190 (1995).
   PubMed Web of Science ®Google Scholar
• Doyle WJ. Animal models of otitis media: other pathogens. Pediatr. Infect. Dis. J. 8, S45–S47 (1989).
   Google Scholar
• Kyd J, John A, Cripps A, Murphy TF. Investigation of mucosal immunisation in pulmonary clearance of Moraxella (Branhamella) catarrhalis. Vaccine 18, 398–406 (2000).
   Google Scholar
• Kyd JM, Cripps AW. Potential of a novel protein, OMP26, from nontypeable Haemophilus influenzae to enhance pulmonary clearance in a rat model. Infect. Immunol. 66, 2272–2278 (1998).
   PubMed Web of Science ®Google Scholar
• Kyd JM, Dunkley ML, Cripps AW. Enhanced respiratory clearance of nontypeable Haemophilus influenzae following mucosal immunization with P6 in a rat model. Infect. Immunol. 63, 2931–2940 (1995).
   PubMed Web of Science ®Google Scholar
• Murphy TF, Kyd JM, John A, Kirkham C, Cripps AW. Enhancement of pulmonary clearance of Moraxella (Branhamella) catarrhalis following immunization with outer membrane protein CD in a mouse model. J. Infect. Dis. 178, 1667–1675 (1998).
   PubMed Web of Science ®Google Scholar
• Hou Y, Hu WG, Hirano T, Gu XX. A new intra-NALT route elicits mucosal and systemic immunity against Moraxella catarrhalis in a mouse challenge model. Vaccine 20(17–18), 2375–2381 (2002).
   PubMed Web of Science ®Google Scholar
• Hu WG, Chen J, Collins FM, Gu XX. An aerosol challenge mouse model for Moraxella catarrhalis. Vaccine 18, 799–804 (2000).
   Google Scholar
• Hu WG, Chen J, Battey JF, Gu XX. Enhancement of clearance of bacteria from murine lungs by immunization with detoxified lipooligosaccharide from Moraxella catarrhalis conjugated to proteins. Infect. Immunol. 68(9), 4980–4985 (2000).
   PubMed Web of Science ®Google Scholar
• Murphy TF. Branhamella catarrhalis: epidemiology, surface antigenic structure, and immune response. Microbiol. Rev. 60, 267–279 (1996).
   PubMedGoogle Scholar
• Murphy TF, Sethi S. Bacterial infection in chronic obstructive pulmonary disease. Am. Rev. Respir. Dis. 146, 1067–1083 (1992).
   PubMed Web of Science ®Google Scholar
• Faden H, Bernstein J, Brodsky L et al. Otitis media in children. I. The systemic immune response to nontypable Haemophilus influenzae. J. Infect. Dis. 160, 999–1004 (1989).
   PubMed Web of Science ®Google Scholar
• Faden H, Hong J, Murphy TF. Immune response to outer membrane antigens of Moraxella catarrhalis in children with otitis media. Infect. Immunol. 60, 3824–3829 (1992).
   PubMed Web of Science ®Google Scholar
• Meier PS, Freiburghaus S, Martin A, Heiniger N, Troller R, Aebi C. Mucosal immune response to specific outer membrane proteins of Moraxella catarrhalis in young children. Pediatr. Infect. Dis. J. 22(3), 256–262 (2003).
   PubMed Web of Science ®Google Scholar
• Hotomi M, Yamanaka N, Shimada J et al. Intranasal immunization with recombinant outer membrane protein P6 induces specific immune responses against nontypeable Haemophilus influenzae. Int. J. Pediatr. Otorhinolaryngol. 65(2), 109–116 (2002).
   PubMed Web of Science ®Google Scholar
• Hotomi M, Ikeda Y, Suzumoto M et al. A recombinant P4 protein of Haemophilus influenzae induces specific immune responses biologically active against nasopharyngeal colonization in mice after intranasal immunization. Vaccine 23(10), 1294–1300 (2005).
   PubMed Web of Science ®Google Scholar
• Stenfors L-E, Raisanen S. Secretory IgA-, IgG- and C3b-coated bacteria in the nasopharynx of otitis-prone and non-otitis-prone children. Acta. Otolaryngol. 113, 191–195 (1993).
   PubMed Web of Science ®Google Scholar
• Stutzmann Meier P, Heiniger N, Troller R, Aebi C. Salivary antibodies directed against outer membrane proteins of Moraxella catarrhalis in healthy adults. Infect. Immunol. 71(12), 6793–6798 (2003).
   PubMedGoogle Scholar
• Shurin PA, Pelton SI, Tazer IB, Kasper DL. Bactericidal antibody and susceptibility to otitis media caused by nontypeable strains of Haemophilus influenzae. J. Pediatr. 97, 364–369 (1980).
   PubMed Web of Science ®Google Scholar
• Murphy TF, Bakaletz LO, Kyd JM, Watson B, Klein DL. Vaccines for otitis media: proposals for overcoming obstacles to progress. Vaccine 23(21), 2696–2702 (2005).
   Google Scholar