Chapter 7 : Competitive and Cooperative Interactions in the Respiratory Microflora

MyBook is a cheap paperback edition of the original book and will be sold at uniform, low price.

Preview this chapter:
Zoom in

Competitive and Cooperative Interactions in the Respiratory Microflora, Page 1 of 2

| /docserver/preview/fulltext/10.1128/9781555817619/9781555813239_Chap07-1.gif /docserver/preview/fulltext/10.1128/9781555817619/9781555813239_Chap07-2.gif


This chapter reviews aspects of interaction among the members of the respiratory microflora by considering relevant laboratory models and examples of both cooperation and competition. In general, the author focuses on the anatomic area between the nasal mucosa and the epiglottis, where several bacterial species coexist and may cocolonize for extended periods. The lower airway, below the epiglottis, is a sterile environment under normal conditions. In contrast, another neighbor of the nasopharynx, the oral cavity, is home to literally hundreds of distinct species of bacteria. Specific data regarding the anatomic localization of colonizing bacteria in the nasopharynx and the relative burdens of each species are limited; however, evolving concepts of interaction among the members of the commensal flora are furthering one's understanding of carriage. Evidence from colonization rates of children transferred from other nurseries suggested that the latter was the more likely possibility, so the investigators took the striking approach of directly testing the phenomenon of bacterial interference. In addition, many of the members of the upper respiratory flora are auxotrophs. Competition for nutrients among members of mixed bacterial populations has been proposed. Artificial alteration of colonization through vaccination or antibiotic therapy may disrupt the ecological balance in this microenvironment and have unintended consequences. Further research in this area, especially if relevant in vivo models are employed, will contribute to one's evolving understanding of the ecology of the upper respiratory tract.

Citation: Ratner A. 2005. Competitive and Cooperative Interactions in the Respiratory Microflora, p 87-96. In Nataro J, Cohen P, Mobley H, Weiser J (ed), Colonization of Mucosal Surfaces. ASM Press, Washington, DC. doi: 10.1128/9781555817619.ch7

Key Concept Ranking

Tumor Necrosis Factor alpha
Highlighted Text: Show | Hide
Loading full text...

Full text loading...


1. Adams, W. G.,, K. A. Deaver,, S. L. Cochi,, B. D. Plikaytis,, E. R. Zell,, C. V. Broome,, and J. D. Wenger. 1993. Decline of childhood Haemophilus influenzae type b (Hib) disease in the Hib vaccine era. JAMA 269:221226.
2. Aly, R.,, and H. R. Shinefield. 1982. Bacterial Interference. CRC Press, Inc., Boca Raton, Fla..
3. Aniansson, G.,, B. Alm,, B. Andersson,, P. Larsson,, O. Nylen,, H. Peterson,, P. Rigner,, M. Svanborg,, and C. Svanborg. 1992. Nasopharyngeal colonization during the first year of life. J. Infect. Dis. 165(Suppl. 1):S38S42.
4. Bakaletz, L. O.,, R. L. Daniels,, and D. J. Lim. 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. 168:865872.
5. Bakir, M.,, A. Yagci,, N. Ulger,, C. Akbenlioglu,, A. Ilki,, and G. Soyletir. 2001. Asymtomatic carriage of Neisseria meningitidis and Neisseria lactamica in relation to Streptococcus pneumoniae and Haemophilus influenzae colonization in healthy children: apropos of 1400 children sampled. Eur. J. Epidemiol. 17: 10151018.
6. Berkovitch, M.,, M. Bulkowstein,, D. Zhovtis,, R. Greenberg,, Y. Nitzan,, B. Barzilay,, and I. Boldur. 2002. Colonization rate of bacteria in the throat of healthy infants. Int. J. Pediatr. Otorhinolaryngol. 63:1924.
7. Blair, E. B.,, and A. H. Tull. 1969. Multiple infections among newborns resulting from colonization with Staphylococcus aureus 502A. Am. J. Clin. Pathol. 52:4249.
8. Brogden, K. A., 2002. Polymicrobial diseases of animals and humans, p. 320. In K. A. Brogden, and J. M. Guthmiller (ed.), Polymicrobial Infections. ASM Press, Washington, D.C..
9. Brook, I. 1999. Bacterial interference. Crit. Rev. Microbiol. 25:155172.
10. Colebrook, L. 1915. Bacterial antagonism, with particular reference to meningococcus. Lancet ii:11361138.
11. Cossart, P. 2000. Cellular Microbiology. ASM Press, Washington, D.C..
12. Cundell, D. R.,, N. P. Gerard,, C. Gerard,, I. Idanpaan-Heikkila,, and E. I. Tuomanen. 1995. Streptococcus pneumoniae anchor to activated human cells by the receptor for platelet-activating factor. Nature 377:435438.
13. Dagan, R.,, D. Fraser,, N. Givon,, and P. Yagupsky. 1999. Carriage of resistant pneumococci by children in southern Israel and impact of conjugate vaccines on carriage. Clin. Microbiol. Infect. 5(Suppl. 4):S29-–S37.
14. Dagan, R.,, N. Givon-Lavi,, O. Zamir,, and D. Fraser. 2003. Effect of a nonavalent conjugate vaccine on carriage of antibiotic- resistant Streptococcus pneumoniae in day-care centers. Pediatr. Infect. Dis. J. 22:532540.
15. Dagan, R.,, N. Givon-Lavi,, O. Zamir,, M. Sikuler-Cohen,, L. Guy,, J. Janco,, P. Yagupsky,, and D. Fraser. 2002. Reduction of nasopharyngeal carriage of Streptococcus pneumoniae after administration of a 9-valent pneumococcal conjugate vaccine to toddlers attending day care centers. J. Infect. Dis. 185:927936.
16. Dagan, R.,, R. Melamed,, M. Muallem,, L. Piglansky,, and P. Yagupsky. 1996. Nasopharyngeal colonization in southern Israel with antibiotic-resistant pneumococci during the first 2 years of life: relation to serotypes likely to be included in pneumococcal conjugate vaccines. J. Infect. Dis. 174:13521355.
17. Dagan, R.,, M. Muallem,, R. Melamed,, O. Leroy,, and P. Yagupsky. 1997. Reduction of pneumococcal nasopharyngeal carriage in early infancy after immunization with tetravalent pneumococcal vaccines conjugated to either tetanus toxoid or diphtheria toxoid. Pediatr. Infect. Dis. J. 16:10601064.
18. Davis, N. A.,, and G. H. Davis. 1965. Ecology of nasal staphylococci. J. Bacteriol. 89:11631168.
19. Drake, D. R.,, and K. A. Brogden,. 2002. Continuous-culture chemostat systems and flowcells as methods to investigate microbial interactions, p. 2130. In K. A. Brogden, and J. M. Guthmiller (ed.), Polymicrobial Infections. ASM Press, Washington, D.C..
20. Dykhuizen, R. S.,, D. Golder,, T. M. Reid,, and I. M. Gould. 1996. Phenoxymethyl penicillin versus co-amoxiclav in the treatment of acute streptococcal pharyngitis, and the role of beta-lactamase activity in saliva. J. Antimicrob. Chemother. 37:133138.
21. Ehrenkranz, N. J. 1970. Bacterial colonization of newborn infants and subsequent acquisition of hospital bacteria. J. Pediatr. 76:839847.
22. El Ahmer, O. R.,, M. W. Raza,, M. M. Ogilvie,, D. M. Weir,, and C. C. Blackwell. 1999. Binding of bacteria to HEp-2 cells infected with influenza A virus. FEMS Immunol. Med. Microbiol. 23:331341.
23. Eskola, J.,, T. Kilpi,, A. Palmu,, J. Jokinen,, J. Haapakoski,, E. Herva,, A. Takala,, H. Kayhty,, P. Karma,, R. Kohberger,, G. Siber,, and P. H. Makela. 2001. Efficacy of a pneumococcal conjugate vaccine against acute otitis media. N. Engl. J. Med. 344:403409.
24. Flak, T. A.,, L. N. Heiss,, J. T. Engle,, and W. E. Goldman. 2000. Synergistic epithelial responses to endotoxin and a naturally occurring muramyl peptide. Infect. Immun. 68:12351242.
25. Florey, H. W. 1946. The use of micro-organisms for therapeutic purposes. Yale J. Biol. Med. 19:101117.
26. Garcia-Rodriguez, J. A.,, and M. J. Fresnadillo Martinez. 2002. Dynamics of nasopharyngeal colonization by potential respiratory pathogens. J. Antimicrob. Chemother. 50 Suppl. S2):5973.
27. Gerber, M. A.,, R. R. Tanz,, W. Kabat,, G. L. Bell,, B. Siddiqui,, T. J. Lerer,, M. L. Lepow,, E. L. Kaplan,, and S. T. Shulman. 1999. Potential mechanisms for failure to eradicate group A streptococci from the pharynx. Pediatrics 104:911917.
28. Graham, N. M.,, R. M. Douglas,, and P. Ryan. 1986. Stress and acute respiratory infection. Am. J. Epidemiol. 124:389401.
29. Gwaltney, J. M., Jr., M. A. Sande, R. Austrian, and J. O. Hendley. 1975. Spread of Streptococcus pneumoniae in families. II. Relation of transfer of S. pneumoniae to incidence of colds and serum antibody. J. Infect. Dis. 132:6268.
30. Hakansson, A.,, A. Kidd,, G. Wadell,, H. Sabharwal,, and C. Svanborg. 1994. Adenovirus infection enhances in vitro adherence of Streptococcus pneumoniae. Infect. Immun. 62:27072714.
31. Hament, J. M.,, J. L. Kimpen,, A. Fleer,, and T. F. Wolfs. 1999. Respiratory viral infection predisposing for bacterial disease: a concise review. FEMS Immunol. Med. Microbiol. 26:189195.
32. Harder, W.,, and L. Dijkhuizen. 1982. Strategies of mixed substrate utilization in microorganisms. Philos. Trans. R. Soc. Lond. Ser. B 297:459480.
33. Hood, D. W.,, K. Makepeace,, M. E. Deadman,, R. F. Rest,, P. Thibault,, A. Martin,, J. C. Richards,, and E. R. Moxon. 1999. Sialic acid in the lipopolysaccharide of Haemophilus influenzae: strain distribution, influence on serum resistance and structural characterization. Mol. Microbiol. 33:679692.
34. Houck, P. W.,, J. D. Nelson,, and J. L. Kay. 1972. Fatal septicemia due to Staphylococcus aureus 502A. Report of a case and review of the infectious complications of bacterial interference programs. Am. J. Dis. Child. 123:4548.
35. Ishizuka, S.,, M. Yamaya,, T. Suzuki,, H. Takahashi,, S. Ida,, T. Sasaki,, D. Inoue,, K. Sekizawa,, H. Nishimura,, and H. Sasaki. 2003. Effects of rhinovirus infection on the adherence of Streptococcus pneumoniae to cultured human airway epithelial cells. J. Infect. Dis. 188:19291940.
36. Johanson, W. G., Jr., R. Blackstock, A. K. Pierce, and J. P. Sanford. 1970. The role of bacterial antagonism in pneumococcal colonization of the human pharynx. J. Lab. Clin. Med. 75:946952.
37. Krivan, H. C.,, D. D. Roberts,, and V. Ginsburg. 1988. Many pulmonary pathogenic bacteria bind specifically to the carbohydrate sequence GalNAc beta 1-4Gal found in some glycolipids. Proc. Natl. Acad. Sci. USA 85:61576161.
38. Lakshman, R.,, C. Murdoch,, G. Race,, R. Burkinshaw,, L. Shaw,, and A. Finn. 2003. Pneumococcal nasopharyngeal carriage in children following heptavalent pneumococcal conjugate vaccination in infancy. Arch. Dis. Child. 88:211214.
39. Light, I. J.,, J. M. Sutherland,, M. L. Cochran,, and J. Sutorius. 1968. Ecologic relation between Staphylococcus aureus and Pseudomonas in a nursery population. Another example of bacterial interference. N. Engl. J. Med. 278:12431247.
40. Light, I. J.,, R. L. Walton,, J. M. Sutherland,, H. R. Shinefield,, and V. Brackvogel. 1967. Use of bacterial interference to control a staphylococcal nursery outbreak. Deliberate colonization of all infants with the 502A strain of Staphylococcus aureus. Am. J. Dis. Child. 113:291300.
41. Lipsitch, M. 1999. Bacterial vaccines and serotype replacement: lessons from Haemophilus influenzae and prospects for Streptococcus pneumoniae. Emerg. Infect. Dis. 5:336345.
42. Lipsitch, M.,, J. K. Dykes,, S. E. Johnson,, E. W. Ades,, J. King,, D. E. Briles,, and G. M. Carlone. 2000. Competition among Streptococcus pneumoniae for intranasal colonization in a mouse model. Vaccine 18:28952901.
43. Luotonen, J. 1982. Streptococcus pneumoniae and Haemophilus influenzae in nasal cultures during acute otitis media. Acta Otolaryngol. 93:295299.
44. Macfarlane, G. T.,, and J. H. Cummings. 2002. Probiotics, infection and immunity. Curr. Opin. Infect. Dis. 15:501506.
45. Mackowiak, P. A. 1978. Microbial synergism in human infections (first of two parts). N. Engl. J. Med. 298:2126.
46. Mackowiak, P. A. 1978. Microbial synergism in human infections (second of two parts). N. Engl. J. Med. 298:8387.
47. Maibach, H. I.,, W. G. Strauss,, and H. R. Shinefield. 1969. Bacterial interference: relating to chronic furunculosis in man. Br. J. Dermatol. 81 Suppl. 1):6976.
48. May, J. R. 1954. Pathogenic bacteria in chronic bronchitis. Lancet 267:839842.
49. McCool, T. L.,, T. R. Cate,, G. Moy,, and J. N. Weiser. 2002. The immune response to pneumococcal proteins during experimental human carriage. J. Exp. Med. 195:359365.
50. McCool, T. L.,, T. R. Cate,, E. I. Tuomanen,, P. Adrian,, T. J. Mitchell,, and J. N. Weiser. 2003. Serum immunoglobulin G response to candidate vaccine antigens during experimental human pneumococcal colonization. Infect. Immun. 71:57245732.
51. McCullers, J. A.,, and J. E. Rehg. 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. 186:341350.
52. Mohle-Boetani, J. C.,, G. Ajello,, E. Breneman,, K. A. Deaver,, C. Harvey,, B. D. Plikaytis,, M. M. Farley,, D. S. Stephens,, and J. D. Wenger. 1993. Carriage of Haemophilus influenzae type b in children after widespread vaccination with conjugate Haemophilus influenzae type b vaccines. Pediatr. Infect. Dis. J.12:589593.
53. Mosse, J. R. 1852. Of the use of yeast in the treatment of boils. Lancet ii:113.
54. Murphy, T. V.,, P. Pastor,, F. Medley,, M. T. Osterholm,, and D. M. Granoff. 1993. Decreased Haemophilus colonization in children vaccinated with Haemophilus influenzae type b conjugate vaccine. J. Pediatr. 122:517523.
55. Nain, M.,, F. Hinder,, J. H. Gong,, A. Schmidt,, A. Bender,, H. Sprenger,, and D. Gemsa. 1990. Tumor necrosis factoralpha production of influenza A virus-infected macrophages and potentiating effect of lipopolysaccharides. J. Immunol.145:19211928.
56. Ohashi, Y.,, Y. Nakai,, Y. Esaki,, Y. Ohno,, Y. Sugiura,, and H. Okamoto. 1991. Influenza A virus-induced otitis media and mucociliary dysfunction in the guinea pig. Acta Otolaryngol. Suppl. 486:135148.
57. Paster, B. J.,, S. K. Boches,, J. L. Galvin,, R. E. Ericson,, C. N. Lau,, V. A. Levanos,, A. Sahasrabudhe,, and F. E. Dewhirst. 2001. Bacterial diversity in human subgingival plaque. J. Bacteriol. 183:37703783.
58. Pericone, C. D.,, K. Overweg,, P. W. Hermans,, and J. N. Weiser. 2000. Inhibitory and bactericidal effects of hydrogen peroxide production by Streptococcus pneumoniae on other inhabitants of the upper respiratory tract. Infect. Immun. 68:39903997.
59. Raza, M. W.,, C. C. Blackwell,, M. M. Ogilvie,, A. T. Saadi,, J. Stewart,, R. A. Elton,, and D. M. Weir. 1994. Evidence for the role of glycoprotein G of respiratory syncytial virus in binding of Neisseria meningitidis to HEp-2 cells. FEMS Immunol. Med. Microbiol. 10:2530.
60. Raza, M. W.,, O. R. El Ahmer,, M. M. Ogilvie,, C. C. Blackwell,, A. T. Saadi,, R. A. Elton,, and D. M. Weir. 1999. Infection with respiratory syncytial virus enhances expression of native receptors for non-pilate Neisseria meningitidis on HEp-2 cells. FEMS Immunol. Med. Microbiol. 23:115124.
61. Reid, G.,, J. Howard,, and B. S. Gan. 2001. Can bacterial interference prevent infection? Trends Microbiol. 9:424428.
62. Rickard, A. H.,, P. Gilbert,, N. J. High,, P. E. Kolenbrander,, and P. S. Handley. 2003. Bacterial coaggregation: an integral process in the development of multi-species biofilms. Trends Microbiol. 11:94100.
63. Riley, M. A.,, and J. E. Wertz. 2002. Bacteriocins: evolution, ecology, and application. Annu. Rev. Microbiol. 56:117137.
64. Rosebury, T.,, D. Gale,, and D. F. Taylor. 1954. An approach to the study of interactive phenomena among microorganisms indigenous to man. J. Bacteriol. 67:135152.
65. Rotimi, V. O.,, and B. I. Duerden. 1981. The development of the bacterial flora in normal neonates. J. Med. Microbiol. 14:5162.
66. Sanders, E. 1969. Bacterial interference. I. Its occurrence among the respiratory tract flora and characterization of inhibition of group A streptococci by viridans streptococci. J. Infect. Dis. 120:698707.
67. Sanford, B. A.,, A. Shelokov,, and M. A. Ramsay. 1978. Bacterial adherence to virus-infected cells: a cell culture model of bacterial superinfection. J. Infect. Dis. 137:176181.
68. Shakhnovich, E. A.,, S. J. King,, and J. N. Weiser. 2002. Neuraminidase expressed by Streptococcus pneumoniae desialylates the lipopolysaccharide of Neisseria meningitidis and Haemophilus influenzae: a paradigm for interbacterial competition among pathogens of the human respiratory tract. Infect. Immun. 70:71617164.
69. Shinefield, H. R.,, M. Boris,, J. C. Ribble,, E. F. Cale,, and H. F. Eichenwald. 1963. Bacterial interference: its effect on nurseryacquired infection with Staphylococcus aureus. III. The Georgia epidemic. Am. J. Dis. Child. 105:663673.
70. Shinefield, H. R.,, J. C. Ribble,, M. Boris,, and H. F. Eichenwald. 1963. Bacterial interference: its effect on nursery-acquired infection with Staphylococcus aureus. I. Preliminary observations on artificial colonzation of newborns. Am. J. Dis. Child. 105:646654.
71. Smith, H. 1982. The role of microbial interactions in infectious disease. Philos. Trans. R. Soc. Lond. Ser. B 297:551561.
72. Speck, W. T.,, J. M. Driscoll,, R. A. Polin,, and H. S. Rosenkranz. 1978. Effect of bacterial flora on staphylococcal colonisation of the newborn. J. Clin. Pathol. 31:153155.
73. Sprunt, K.,, and G. Leidy. 1988. The use of bacterial interference to prevent infection. Can. J. Microbiol. 34:332338.
74. Sprunt, K.,, G. Leidy,, and W. Redman. 1980. Abnormal colonization of neonates in an ICU: conversion to normal colonization by pharyngeal implantation of alpha hemolytic streptococcus strain 215. Pediatr. Res. 14:308313.
75. Sprunt, K.,, G. A. Leidy,, and W. Redman. 1971. Prevention of bacterial overgrowth. J. Infect. Dis. 123:110.
76. Sprunt, K.,, and W. Redman. 1968. Evidence suggesting importance of role of interbacterial inhibition in maintaining balance of normal flora. Ann. Intern. Med. 68:579590.
77. Stemmons, E. D.,, and H. L. Smith. 2000. Competition in a chemostat with wall attachment. SIAM J. Appl. Math. 61:567595.
78. Strauss, W. G.,, H. I. Maibach,, and H. R. Shinefield. 1969. Bacterial interference treatment of recurrent furunculosis. 2. Demonstration of the relationship of strain to pathogeneicity. JAMA 208:861863.
79. Swords, W. E.,, B. A. Buscher,, K. Ver Steeg Ii,, A. Preston,, W. A. Nichols,, J. N. Weiser,, B. W. Gibson,, and M. A. Apicella. 2000. Non-typeable Haemophilus influenzae adhere to and invade human bronchial epithelial cells via an interaction of lipooligosaccharide with the PAF receptor. Mol. Microbiol. 37:1327.
80. Swords, W. E.,, M. L. Moore,, L. Godzicki,, G. Bukofzer,, M. J. Mitten,, and J. VonCannon. 2004. Sialylation of lipooligosaccharides promotes biofilm formation by nontypeable Haemophilus influenzae. Infect. Immun. 72:106113.
81. Tagg, J. R. 1984. Production of bacteriocin-like inhibitors by group A streptococci of nephritogenic M types. J. Clin. Microbiol. 19:884887.
82. Tagg, J. R.,, and K. P. Dierksen. 2003. Bacterial replacement therapy: adapting ‘germ warfare’ to infection prevention. Trends Biotechnol. 21:217223.
83. Takala, A. K.,, J. Eskola,, M. Leinonen,, H. Kayhty,, A. Nissinen,, E. Pekkanen,, and P. H. Makela. 1991. Reduction of oropharyngeal carriage of Haemophilus influenzae type b (Hib) in children immunized with an Hib conjugate vaccine. J. Infect. Dis. 164:982986.
84. Takala, A. K.,, M. Santosham,, J. Almeido-Hill,, M. Wolff,, W. Newcomer,, R. Reid,, H. Kayhty,, E. Esko,, and P. H. Makela. 1993. Vaccination with Haemophilus influenzae type b meningococcal protein conjugate vaccine reduces oropharyngeal carriage of Haemophilus influenzae type b among American Indian children. Pediatr. Infect. Dis. J. 12:593599.
85. Toleman, M.,, E. Aho,, and M. Virji. 2001. Expression of pathogen-like Opa adhesins in commensal Neisseria: genetic and functional analysis. Cell Microbiol. 3:3344.
86. Topley, W. W. C.,, and H. A. Fielden. 1922. The succession of dominant species in a mixed bacterial culture in a fluid medium. Lancet iii:11641165.
87. Tuomanen, E. 1986. Piracy of adhesins: attachment of superinfecting pathogens to respiratory cilia by secreted adhesins of Bordetella pertussis. Infect. Immun. 54:905908.
88. Unkmeir, A.,, U. Kammerer,, A. Stade,, C. Hubner,, S. Haller,, A. Kolb-Maurer,, M. Frosch,, and G. Dietrich. 2002. Lipooligosaccharide and polysaccharide capsule: virulence factors of Neisseria meningitidis that determine meningococcal interaction with human dendritic cells. Infect. Immun. 70:24542462.
89. Van Nhieu, G. T.,, and P. Sansonetti,. 2000. Cell adhesion molecules and bacterial pathogens, p. 97111. In P. Cossart,, P. Boquet,, S. Normark,, and R. Rappuoli (ed.), Cellular Microbiology. ASM Press, Washington, D.C..
90. Vernazza, T. R.,, and T. H. Melville. 1979. Inhibitory activity of Streptococcus mitis against oral bacteria. Microbios 26:95101.
91. Virji, M.,, D. Evans,, J. Griffith,, D. Hill,, L. Serino,, A. Hadfield,, and S. M. Watt. 2000. Carcinoembryonic antigens are targeted by diverse strains of typable and non-typable Haemophilus influenzae. Mol. Microbiol. 36:784795.
92. Walls, T.,, D. Power,, and J. Tagg. 2003. Bacteriocin-like inhibitory substance (BLIS) production by the normal flora of the nasopharynx: potential to protect against otitis media? J. Med. Microbiol. 52:829833.
93. Weiser, J. N.,, D. Bae,, C. Fasching,, R. W. Scamurra,, A. J. Ratner,, and E. N. Janoff. 2003. Antibody-enhanced pneumococcal adherence requires IgA1 protease. Proc. Natl. Acad. Sci. USA 100:42154220.
94. Whitney, C. G.,, M. M. Farley,, J. Hadler,, L. H. Harrison,, N. M. Bennett,, R. Lynfield,, A. Reingold,, P. R. Cieslak,, T. Pilishvili,, D. Jackson,, R. R. Facklam,, J. H. Jorgensen,, and A. Schuchat. 2003. Decline in invasive pneumococcal disease after the introduction of protein-polysaccharide conjugate vaccine. N. Engl. J. Med. 348:17371746.


Generic image for table
Table 1

Mechanisms of pathogenesis in polymicrobial disease

Citation: Ratner A. 2005. Competitive and Cooperative Interactions in the Respiratory Microflora, p 87-96. In Nataro J, Cohen P, Mobley H, Weiser J (ed), Colonization of Mucosal Surfaces. ASM Press, Washington, DC. doi: 10.1128/9781555817619.ch7

This is a required field
Please enter a valid email address
Please check the format of the address you have entered.
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error