Streptococcus pneumoniae: The evolution of antimicrobial resistance to beta-lactams, fluoroquinolones and macrolides

Microbes and Infection

Volumn 14, Issue 7-8, 2012, Pages 573-583

  Cornick, J E ^a,b   Bentley, S D ^c  

^a MALAWI LIVERPOOL WELLCOME TRUST CLINICAL RESEARCH PROGRAMME   (Malawi)

^b UNIVERSITY OF LIVERPOOL   (United Kingdom)

^c WELLCOME TRUST SANGER INSTITUTE   (United Kingdom)

Author keywords

Antimicrobial resistance; Beta lactams; Evolution; Fluoroquinolones; Macrolides; Streptococcus pneumoniae

Indexed keywords

AMOXICILLIN; BACTERIAL PROTEIN; BETA LACTAM ANTIBIOTIC; CIPROFLOXACIN; DNA TOPOISOMERASE (ATP HYDROLYSING) A; DNA TOPOISOMERASE (ATP HYDROLYSING) B; DNA TOPOISOMERASE IV; GATIFLOXACIN; KANAMYCIN; LEVOFLOXACIN; MACROLIDE; MOXIFLOXACIN; PENICILLIN BINDING PROTEIN 2A; PENICILLIN BINDING PROTEIN 2X; PENICILLIN G; PNEUMOCOCCUS VACCINE; QUINOLINE DERIVED ANTIINFECTIVE AGENT; RNA 23S;

ANTIBIOTIC RESISTANCE; BACTERIAL GENE; DNA SYNTHESIS; EVOLUTION; GENE EXPRESSION; GENE MUTATION; MINIMUM INHIBITORY CONCENTRATION; NONHUMAN; PNEUMOCOCCAL INFECTION; PRIORITY JOURNAL; SEROTYPE; SHORT SURVEY; STREPTOCOCCUS MITIS; STREPTOCOCCUS ORALIS; STREPTOCOCCUS PNEUMONIAE;

ANTI-BACTERIAL AGENTS; ANTI-INFECTIVE AGENTS; BETA-LACTAMS; DRUG RESISTANCE, MULTIPLE, BACTERIAL; FLUOROQUINOLONES; HUMANS; MACROLIDES; PNEUMOCOCCAL INFECTIONS; PNEUMOCOCCAL VACCINES; STREPTOCOCCUS PNEUMONIAE;

STREPTOCOCCUS PNEUMONIAE;

EID: 84862244127     PISSN: 12864579     EISSN: 1769714X     Source Type: Journal    
DOI: 10.1016/j.micinf.2012.01.012     Document Type: Short Survey

References (97)

1. Brugger S.D., Hathaway L.J., Muhlemann K. Streptococcus pneumoniae strain co-colonization in the nasopharynx. J. Clin. Microbiol. 2009, 1750-1756.
2. Greenwood B. The epidemiology of pneumococcal infection in children in the developing world. Philos. Trans. R. Soc. Lond. B. Biol. Sci. 1999, 354:777-785.
3. Scott J.A.G. The preventable burden of pneumococcal disease in the developing world. Vaccine 2007, 25:2398-2405.
4. Levine O.S., O'Brien K.L., Knoll M., Adegbola R.A., Black S., Cherian T., Dagan R., Goldblatt D., Grange A., Greenwood B., Hennessy T., Klugman K.P., Madhi S.A., Mulholland K., Nohynek H., Santosham M., Saha S.K., Scott J.A., Sow S., Whitney C.G., Cutts F. Pneumococcal vaccination in developing countries. Lancet 2006, 367:1880-1882.
5. Hansman D., Bullen M.M. A resistant pneumococcus. Lancet 1967, 2:264-265.
6. Richter S.S., Heilmann K.P., Dohrn C.L., Riahi F., Beekmann S.E., Doern G.V. Changing epidemiology of antimicrobial-resistant Streptococcus pneumoniae in the United States, 2004-2005. Clin. Infect. Dis. 2009, 48:e23-e33.
7. Kyaw M.H., Lynfield R., Schaffner W., Craig A.S., Hadler J., Reingold A., Thomas A.R., Harrison L.H., Bennett N.M., Farley M.M., Facklam R.R., Jorgensen J.H., Besser J., Zell E.R., Schuchat A., Whitney C.G. Effect of introduction of the pneumococcal conjugate vaccine on drug-resistant Streptococcus pneumoniae. N. Engl. J. Med. 2006, 354:1455-1463.
8. Appelbaum P.C., Bhamjee A., Scragg J.N., Hallett A.F., Bowen A.J., Cooper R.C. Streptococcus pneumoniae resistant to penicillin and chloramphenicol. Lancet 1977, 2:995-997.
9. McGee L., McDougal L., Zhou J., Spratt B.G., Tenover F.C., George R., Hakenbeck R., Hryniewicz W., Lefevre J.C., Tomasz A., Klugman K.P. Nomenclature of major antimicrobial-resistant clones of Streptococcus pneumoniae defined by the pneumococcal molecular epidemiology network. J. Clin. Microbiol. 2001, 39:2565-2571.
10. Corso A., Severina E.P., Petruk V.F., Mauriz Y.R., Tomasz A. Molecular characterization of penicillin-resistant Streptococcus pneumoniae isolates causing respiratory disease in the United States. Microb. Drug Resist. 1998, 4:325-337.
11. Imai S., Ito Y., Ishida T., Hirai T., Ito I., Maekawa K., Takakura S., Iinuma Y., Ichiyama S., Mishima M. High prevalence of multidrug-resistant Pneumococcal molecular epidemiology network clones among Streptococcus pneumoniae isolates from adult patients with community-acquired pneumonia in Japan. Clin. Microb. Infect. 2009, 15:1039-1045.
12. Sadowy E., Kuch A., Gniadkowski M., Hryniewicz W. Expansion and evolution of the Streptococcus pneumoniae Spain9V-ST156 clonal complex in Poland. Antimicrob. Agents Chemother. 2010, 54:1720-1727.
13. Bergman M., Huikko S., Huovinen P., Paakkari P., Seppala H. Macrolide and azithromycin use are linked to increased macrolide resistance in Streptococcus pneumoniae. Antimicrob. Agents Chemother. 2006, 50:3646-3650.
14. Vanderkooi O.G., Low D.E., Green K., Powis J.E., McGeer A. Predicting antimicrobial resistance in invasive pneumococcal infections. Clin. Infect. Dis. 2005, 40:1288-1297.
15. Beekmann S.E., Diekema D.J., Heilmann K.P., Richter S.S., Doern G.V. Macrolide use identified as risk factor for macrolide-resistant Streptococcus pneumoniae in a 17-center case-control study. Eur. J. Clin. Microbiol. Infect. Dis. 2006, 25:335-339.
16. Riedel S., Beekmann S.E., Heilmann K.P., Richter S.S., Garcia-de-Lomas J., Ferech M., Goosens H., Doern G.V. Antimicrobial use in Europe and antimicrobial resistance in Streptococcus pneumoniae. Eur. J. Clin. Microbiol. Infect. Dis. 2007, 26:485-490.
17. Vilhelmsson S.E., Tomasz A., Kristinsson K.G. Molecular evolution in a multidrug-resistant lineage of Streptococcus pneumoniae: emergence of strains belonging to the serotype 6B Icelandic clone that lost antibiotic resistance traits. J. Clin. Micro 2000, 38:1375-1381.
18. Arason V.A., Gunnlaugsson A., Sigurdsson J.A., Erlendsdottir H., Gudmundsson S., Kristinsson K.G. Clonal spread of resistant pneumococci despite diminished antimicrobial use. Microb. Drug Resist. 2002, 8:187-192.
19. Henderson-Begg S.K., Livermore D.M., Hall L.M. Effect of subinhibitory concentrations of antibiotics on mutation frequency in Streptococcus pneumoniae. J. Antimicrob. Chemother. 2006, 57:849-854.
20. Prudhomme M., Attaiech L., Sanchez G., Martin B., Claverys J.P. Antibiotic stress induces genetic transformability in the human pathogen Streptococcus pneumoniae. Science 2006, 313:89-92.
21. Hicks L.A., Harrison L.H., Flannery B., Hadler J.L., Schaffner W., Craig A.S., Jackson D., Thomas A., Beall B., Lynfield R., Reingold A., Farley M.M., Whitney C.G. Incidence of pneumococcal disease due to non-pneumococcal conjugate vaccine (PCV7) serotypes in the United States during the era of widespread PCV7 vaccination, 1998-2004. J. Infect. Dis. 2007, 196:1346-1354.
22. Stephens D.S., Zughaier S.M., Whitney C.G., Baughman W.S., Barker L., Gay K., Jackson D., Orenstein W.A., Arnold K., Schuchat A., Farley M.M. Incidence of macrolide resistance in Streptococcus pneumoniae after introduction of the pneumococcal conjugate vaccine: population-based assessment. Lancet 2005, 365:855-863.
23. Kaplan S.L., Mason E.O., Wald E.R., Schutze G.E., Bradley J.S., Tan T.Q., Hoffman J.A., Givner L.B., Yogev R., Barson W.J. Decrease of invasive pneumococcal infections in children among 8 children's hospitals in the United States after the introduction of the 7-valent pneumococcal conjugate vaccine. Pediatrics 2004, 113:443-449.
24. Talbot T.R., Poehling K.A., Hartert T.V., Arbogast P.G., Halasa N.B., Mitchel E., Schaffner W., Craig A.S., Edwards K.M., Griffin M.R. Reduction in high rates of antibiotic-nonsusceptible invasive pneumococcal disease in tennessee after introduction of the pneumococcal conjugate vaccine. Clin. Infect. Dis. 2004, 39:641-648.
25. Beall B., McEllistrem M.C., Gertz R.E., Wedel S., Boxrud D.J., Gonzalez A.L., Medina M.J., Pai R., Thompson T.A., Harrison L.H., McGee L., Whitney C.G. Pre- and postvaccination clonal compositions of invasive pneumococcal serotypes for isolates collected in the United States in 1999, 2001, and 2002. J. Clin. Microbiol. 2006, 44:999-1017.
26. Moore M.R., Gertz R.E., Woodbury R.L., Barkocy-Gallagher G.A., Schaffner W., Lexau C., Gershman K., Reingold A., Farley M., Harrison L.H., Hadler J.L., Bennett N.M., Thomas A.R., McGee L., Pilishvili T., Brueggemann A.B., Whitney C.G., Jorgensen J.H., Beall B. Population snapshot of emergent Streptococcus pneumoniae serotype 19A in the United States, 2005. J. Infect. Dis. 2008, 197:1016-1027.
27. Huang S.S., Platt R., Rifas-Shiman S.L., Pelton S.I., Goldmann D., Finkelstein J.A. Post-PCV7 changes in colonizing pneumococcal serotypes in 16 Massachusetts communities, 2001 and 2004. Pediatrics 2005, 116:e408-e413.
28. Miller E., Andrews N.J., Waight P.A., Slack M.P., George R.C. Herd immunity and serotype replacement 4 years after seven-valent pneumococcal conjugate vaccination in England and Wales: an observational cohort study. Lancet Infect. Dis. 2011, 11:760-768.
29. Hausdorff W.P., Bryant J., Paradiso P.R., Siber G.R. Which pneumococcal serogroups cause the most invasive disease: implications for conjugate vaccine formulation and use, Part I. Clin. Infect. Dis. 2000, 30:100-121.
30. Paradiso P.R. Advances in pneumococcal disease Prevention: 13-valent pneumococcal conjugate vaccine for infants and children. Clin. Infect. Dis. 2011, 52:1241-1247.
31. Wroe P.C., Lee G.M., Finkelstein J.A., Pelton S.I., Hanage W.P., Lipsitch M., Stevenson A.E., Rifas-Shiman S.L., Kleinman K., Dutta-Linn M.M., Hinrichsen V.L., Lakoma M., Huang S.S. Pneumococcal carriage and antibiotic resistance in young children before 13-valent conjugate vaccine. Ped. Infect. Dis. J. 2011.
32. Avery O.T., Macleod C.M., McCarty M. Studies on the chemical nature of the substance inducing transformation of pneumococcal types: induction of transformation by a desoxyribonucleic acid fraction isolated from pneumococcus type III. J. Exp. Med. 1944, 79:137-158.
33. Croucher N.J., Harris S.R., Fraser C., Quail M.A., Burton J., van der Linden M., McGee L., von Gottberg A., Song J.H., Ko K.S., Pichon B., Baker S., Parry C.M., Lambertsen L.M., Shahinas D., Pillai D.R., Mitchell T.J., Dougan G., Tomasz A., Klugman K.P., Parkhill J., Hanage W.P., Bentley S.D. Rapid pneumococcal evolution in response to clinical interventions. Science 2011, 331:430-434.
34. Feil E.J., Holmes E.C., Bessen D.E., Chan M.S., Day N.P., Enright M.C., Goldstein R., Hood D.W., Kalia A., Moore C.E., Zhou J., Spratt B.G. Recombination within natural populations of pathogenic bacteria: short-term empirical estimates and long-term phylogenetic consequences. Proc. Nat. Acad. Sci. U.S.A. 2001, 98:182-187.
35. Ehrlich G.D., Hu F.Z., Shen K., Stoodley P., Post J.C. Bacterial plurality as a general mechanism driving persistence in chronic infections. Clin. Orthop. Relat. Res. 2005, 20-24.
36. Hiller N.L., Janto B., Hogg J.S., Boissy R., Yu S., Powell E., Keefe R., Ehrlich N.E., Shen K., Hayes J., Barbadora K., Klimke W., Dernovoy D., Tatusova T., Parkhill J., Bentley S.D., Post J.C., Ehrlich G.D., Hu F.Z. Comparative genomic analyses of seventeen Streptococcus pneumoniae strains: insights into the pneumococcal supragenome. J. Bacteriol. 2007, 189:8186-8195.
37. Donati C., Hiller N.L., Tettelin H., Muzzi A., Croucher N.J., Angiuoli S.V., Oggioni M., Dunning Hotopp J.C., Hu F.Z., Riley D.R., Covacci A., Mitchell T.J., Bentley S.D., Kilian M., Ehrlich G.D., Rappuoli R., Moxon E.R., Masignani V. Structure and dynamics of the pan-genome of Streptococcus pneumoniae and closely related species. Genome Biol. 2010, 11:R107.
38. Ardanuy C., Tubau F., Pallares R., Calatayud L., Dominguez M.A., Rolo D., Grau I., Martin R., Linares J. Epidemiology of invasive pneumococcal disease among adult patients in barcelona before and after pediatric 7-valent pneumococcal conjugate vaccine introduction, 1997-2007. Clin. Infect. Dis. 2009, 48:57-64.
39. Mera R.M., Miller L.A., Amrine-Madsen H., Sahm D.F. Impact of new clinical laboratory standards institute Streptococcus pneumoniae penicillin susceptibility testing breakpoints on reported resistance changes over time. Microb. Drug Res. 2011, 17:47-52.
40. Zapun A., Contreras-Martel C., Vernet T. Penicillin-binding proteins and beta-lactam resistance. FEMS Microbiol. Rev. 2008, 32:361-385.
41. Smith A.M., Klugman K.P. Alterations in PBP 1A essential-for high-level penicillin resistance in Streptococcus pneumoniae. Antimicrob. Agents Chemother. 1998, 42:1329-1333.
42. Laible G., Spratt B.G., Hakenbeck R. Interspecies recombinational events during the evolution of altered PBP 2x genes in penicillin-resistant clinical isolates of Streptococcus pneumoniae. Mol. Microbiol. 1991, 5:1993-2002.
43. Chi F., Nolte O., Bergmann C., Ip M., Hakenbeck R. Crossing the barrier: evolution and spread of a major class of mosaic pbp2x in Streptococcus pneumoniae, S. mitis and S. oralis. Int. J. Med. Microbiol. 2007, 297:503-512.
44. Stanhope M.J., Walsh S.L., Becker J.A., Miller L.A., Lefebure T., Lang P., Bitar P.D., Amrine-Madsen H. The relative frequency of intraspecific lateral gene transfer of penicillin binding proteins 1a, 2b, and 2x, in amoxicillin resistant Streptococcus pneumoniae. Infect. Genet. Evol. 2007, 7:520-534.
45. del Campo R., Cafini F., Morosini M.I., Fenoll A., Linares J., Alou L., Sevillano D., Canton R., Prieto J., Baquero F. Combinations of PBPs and MurM protein variants in early and contemporary high-level penicillin-resistant Streptococcus pneumoniae isolates in Spain. J. Antimicrob. Chemother. 2006, 57:983-986.
46. Chesnel L., Carapito R., Croize J., Dideberg O., Vernet T., Zapun A. Identical penicillin-binding domains in penicillin-binding proteins of Streptococcus pneumoniae clinical isolates with different levels of beta-lactam resistance. Antimicrob. Agents Chemother. 2005, 49:2895-2902.
47. Ohsaki Y., Tachibana M., Awaya T., Kuroki M., Itoh Y. Recovery of susceptibility to penicillin G in clinical isolates of Streptococcus pneumoniae despite increased accumulation of pbp gene alterations. Int. J. Antimicrob. Agents 2008, 32:427-431.
48. Rogers P.D., Liu T.T., Barker K.S., Hilliard G.M., English B.K., Thornton J., Swiatlo E., McDaniel L.S. Gene expression profiling of the response of Streptococcus pneumoniae to penicillin. J. Antimicrob. Chemother. 2007, 59:616-626.
49. Mascher T., Heintz M., Zahner D., Merai M., Hakenbeck R. The CiaRH system of Streptococcus pneumoniae prevents lysis during stress induced by treatment with cell wall inhibitors and by mutations in pbp2x involved in beta-lactam resistance. J. Bacteriol. 2006, 188:1959-1968.
50. Albarracin Orio A.G., Pinas G.E., Cortes P.R., Cian M.B., Echenique J. Compensatory evolution of pbp mutations restores the fitness cost imposed by beta-lactam resistance in Streptococcus pneumoniae. PLoS Path 2011, 7:e1002000.
51. Morand B., Muhlemann K. Heteroresistance to penicillin in Streptococcus pneumoniae. Proc. Nat. Acad. Sci. U.S.A. 2007, 104:14098-14103.
52. Klugman K.P. The successful clone: the vector of dissemination of resistance in Streptococcus pneumoniae. J. Antimicrob. Chemother. 2002, 50(Suppl. S2):1-5.
53. Zechiedrich E.L., Cozzarelli N.R. Roles of topoisomerase IV and DNA gyrase in DNA unlinking during replication in Escherichia coli. Genes. Dev. 1995, 9:2859-2869.
54. Li X., Zhao X., Drlica K. Selection of Streptococcus pneumoniae mutants having reduced susceptibility to moxifloxacin and levofloxacin. Antimicrob. Agents Chemother. 2002, 46:522-524.
55. Fernandez-Moreira E., Balas D., Gonzalez I., de la Campa A.G. Fluoroquinolones inhibit preferentially Streptococcus pneumoniae DNA topoisomerase IV than DNA gyrase native proteins. Microb. Drug Resist. 2000, 6:259-267.
56. Lim S., Bast D., McGeer A., de Azavedo J., Low D.E. Antimicrobial susceptibility breakpoints and first-step parC mutations in Streptococcus pneumoniae: redefining fluoroquinolone resistance. Emerg. Infect. Dis. 2003, 9:833-837.
57. Brueggemann A.B., Coffman S.L., Rhomberg P., Huynh H., Almer L., Nilius A., Flamm R., Doern G.V. Fluoroquinolone resistance in Streptococcus pneumoniae in United States since 1994-1995. Antimicrob. Agents Chemother. 2002, 46:680-688.
58. Pletz M.W., McGee L., Jorgensen J., Beall B., Facklam R.R., Whitney C.G., Klugman K.P. Levofloxacin-resistant invasive Streptococcus pneumoniae in the United States: evidence for clonal spread and the impact of conjugate pneumococcal vaccine. Antimicrob. Agents Chemother. 2004, 48:3491-3497.
59. Janoir C., Zeller V., Kitzis M.D., Moreau N.J., Gutmann L. High-level fluoroquinolone resistance in Streptococcus pneumoniae requires mutations in parC and gyrA. Antimicrob. Agents Chemother. 1996, 40:2760-2764.
60. Pan X.S., Fisher L.M. Cloning and characterization of the parC and parE genes of Streptococcus pneumoniae encoding DNA topoisomerase IV: role in fluoroquinolone resistance. J. Bacteriol. 1996, 178:4060-4069.
61. Canton R., Morosini M., Enright M.C., Morrissey I. Worldwide incidence, molecular epidemiology and mutations implicated in fluoroquinolone-resistant Streptococcus pneumoniae: data from the global PROTEKT surveillance programme. J. Antimicrob. Chemother. 2003, 52:944-952.
62. Weigel L.M., Anderson G.J., Facklam R.R., Tenover F.C. Genetic analyses of mutations contributing to fluoroquinolone resistance in clinical isolates of Streptococcus pneumoniae. Antimicrob. Agents Chemother. 2001, 45:3517-3523.
63. Jumbe N.L., Louie A., Miller M.H., Liu W., Deziel M.R., Tam V.H., Bachhawat R., Drusano G.L. Quinolone efflux pumps play a central role in emergence of fluoroquinolone resistance in Streptococcus pneumoniae. Antimicrob. Agents Chemother. 2006, 50:310-317.
64. Bast D.J., de Azavedo J.C., Tam T.Y., Kilburn L., Duncan C., Mandell L.A., Davidson R.J., Low D.E. Interspecies recombination contributes minimally to fluoroquinolone resistance in Streptococcus pneumoniae. Antimicrob. Agents Chemother. 2001, 45:2631-2634.
65. Balsalobre L., Ferrandiz M.J., Linares J., Tubau F., de la Campa A.G. Viridans group streptococci are donors in horizontal transfer of topoisomerase IV genes to Streptococcus pneumoniae. Antimicrob. Agents Chemother. 2003, 47:2072-2081.
66. Tankovic J., Perichon B., Duval J., Courvalin P. Contribution of mutations in gyrA and parC genes to fluoroquinolone resistance of mutants of Streptococcus pneumoniae obtained in vivo and in vitro. Antimicrob. Agents Chemother. 1996, 40:2505-2510.
67. de la Campa A.G., Balsalobre L., Ardanuy C., Fenoll A., Perez-Trallero E., Linares J. Fluoroquinolone resistance in penicillin-resistant Streptococcus pneumoniae clones, Spain. Emerg. Infect. Dis. 2004, 10:1751-1759.
68. Hsueh P.R., Teng L.J., Lee C.M., Huang W.K., Wu T.L., Wan J.H., Yang D., Shyr J.M., Chuang Y.C., Yan J.J., Lu J.J., Wu J.J., Ko W.C., Chang F.Y., Yang Y.C., Lau Y.J., Liu Y.C., Leu H.S., Liu C.Y., Luh K.T. Telithromycin and quinupristin-dalfopristin resistance in clinical isolates of Streptococcus pyogenes: SMART Program 2001 Data. Antimicrob. Agents Chemother. 2003, 47:2152-2157.
69. Montanari M.P., Tili E., Cochetti I., Mingoia M., Manzin A., Varaldo P.E. Molecular characterization of clinical Streptococcus pneumoniae isolates with reduced susceptibility to fluoroquinolones emerging in Italy. Microb. Drug Resist. 2004, 10:209-217.
70. Schito G.C., Felmingham D. Susceptibility of Streptococcus pneumoniae to penicillin, azithromycin and telithromycin (PROTEKT 1999-2003). Int. J. Antimicrob. Agents 2005, 26:479-485.
71. Wolter N., von Gottberg A., du Plessis M., de Gouveia L., Klugman K.P. Molecular basis and clonal nature of increasing pneumococcal macrolide resistance in South Africa, 2000-2005. Int. J. Antimicrob. Agents 2008, 32:62-67.
72. Edelstein P.H. Pneumococcal resistance to macrolides, lincosamides, ketolides, and streptogramin B agents: molecular mechanisms and resistance phenotypes. Clin. Infect. Dis. 2004, 38(Suppl. 4):S322-S327.
73. Seppala H., Skurnik M., Soini H., Roberts M.C., Huovinen P. A novel erythromycin resistance methylase gene (ermTR) in Streptococcus pyogenes. Antimicrob. Agents Chemother. 1998, 42:257-262.
74. Cochetti I., Tili E., Vecchi M., Manzin A., Mingoia M., Varaldo P.E., Montanari M.P. New Tn916-related elements causing erm(B)-mediated erythromycin resistance in tetracycline-susceptible pneumococci. J. Antimicrob. Chemother. 2007, 60:127-131.
75. McDougal L.K., Tenover F.C., Lee L.N., Rasheed J.K., Patterson J.E., Jorgensen J.H., LeBlanc D.J. Detection of Tn917-like sequences within a Tn916-like conjugative transposon (Tn3872) in erythromycin-resistant isolates of Streptococcus pneumoniae. Antimicrob. Agents Chemother. 1998, 42:2312-2318.
76. Brenciani A., Bacciaglia A., Vecchi M., Vitali L.A., Varaldo P.E., Giovanetti E. Genetic elements carrying erm(B) in Streptococcus pyogenes and association with tet(M) tetracycline resistance gene. Antimicrob. Agents Chemother. 2007, 51:1209-1216.
77. Courvalin P., Carlier C. Tn1545: a conjugative shuttle transposon. Mol. Gen. Genet. 1987, 206:259-264.
78. Cochetti I., Tili E., Mingoia M., Varaldo P.E., Montanari M.P. erm(B)-carrying elements in tetracycline-resistant pneumococci and correspondence between Tn1545 and Tn6003. Antimicrob. Agents Chemother. 2008, 52:1285-1290.
79. Syrogiannopoulos G.A., Grivea I.N., Ednie L.M., Bozdogan B., Katopodis G.D., Beratis N.G., Davies T.A., Appelbaum P.C. Antimicrobial susceptibility and macrolide resistance inducibility of Streptococcus pneumoniae carrying erm(A), erm(B), or mef(A). Antimicrob. Agents Chemother. 2003, 47:2699-2702.
80. Farrell D.J., Morrissey I., Bakker S., Felmingham D. Molecular characterization of macrolide resistance mechanisms among Streptococcus pneumoniae and Streptococcus pyogenes isolated from the PROTEKT 1999-2000 study. J. Antimicrob. Chemother. 2002, 50(Suppl. S1):39-47.
81. Robinson W.G., Old L.A., Shah D.S., Russell R.R. Chromosomal insertions and deletions in Streptococcus mutans. Caries. Res. 2003, 37:148-156.
82. Camilli R., Del Grosso M., Iannelli F., Pantosti A. New genetic element carrying the erythromycin resistance determinant erm(TR) in Streptococcus pneumoniae. Antimicrob. Agents Chemother. 2008, 52:619-625.
83. Calatayud L., Ardanuy C., Cercenado E., Fenoll A., Bouza E., Pallares R., Martin R., Linares J. Serotypes, clones, and mechanisms of resistance of erythromycin-resistant Streptococcus pneumoniae isolates collected in Spain. Antimicrob. Agents Chemother. 2007, 51:3240-3246.
84. Lynch J.P., Zhanel G.G. Escalation of antimicrobial resistance among Streptococcus pneumoniae: implications for therapy. Semin. Respir. Crit. Care Med. 2005, 26:575-616.
85. Cochetti I., Vecchi M., Mingoia M., Tili E., Catania M.R., Manzin A., Varaldo P.E., Montanari M.P. Molecular characterization of pneumococci with efflux-mediated erythromycin resistance and identification of a novel mef gene subclass, mef(I). Antimicrob. Agents Chemother. 2005, 49:4999-5006.
86. Daly M.M., Doktor S., Flamm R., Shortridge D. Characterization and prevalence of MefA, MefE, and the associated msr(D) gene in Streptococcus pneumoniae clinical isolates. J. Clin. Microbiol. 2004, 42:3570-3574.
87. Santagati M., Iannelli F., Cascone C., Campanile F., Oggioni M.R., Stefani S., Pozzi G. The novel conjugative transposon tn1207.3 carries the macrolide efflux gene mef(A) in Streptococcus pyogenes. Microb. Drug Resist. 2003, 9:243-247.
88. Del Grosso M., Iannelli F., Messina C., Santagati M., Petrosillo N., Stefani S., Pozzi G., Pantosti A. Macrolide efflux genes mef(A) and mef(E) are carried by different genetic elements in Streptococcus pneumoniae. J. Clin. Microbiol. 2002, 40:774-778.
89. Gay K., Stephens D.S. Structure and dissemination of a chromosomal insertion element encoding macrolide efflux in Streptococcus pneumoniae. J. Infect. Dis. 2001, 184:56-65.
90. Del Grosso M., Scotto d'Abusco A., Iannelli F., Pozzi G., Pantosti A. Tn2009, a Tn916-like element containing mef(E) in Streptococcus pneumoniae. Antimicrob. Agents Chemother. 2004, 48:2037-2042.
91. Del Grosso M., Northwood J.G., Farrell D.J., Pantosti A. The macrolide resistance genes erm(B) and mef(E) are carried by Tn2010 in dual-gene Streptococcus pneumoniae isolates belonging to clonal complex CC271. Antimicrob. Agents Chemother. 2007, 51:4184-4186.
92. Del Grosso M., Camilli R., Libisch B., Fuzi M., Pantosti A. New composite genetic element of the Tn916 family with dual macrolide resistance genes in a Streptococcus pneumoniae isolate belonging to clonal complex 271. Antimicrob. Agents Chemother. 2009, 53:1293-1294.
93. Mingoia M., Vecchi M., Cochetti I., Tili E., Vitali L.A., Manzin A., Varaldo P.E., Montanari M.P. Composite structure of Streptococcus pneumoniae containing the erythromycin efflux resistance gene mefI and the chloramphenicol resistance gene catQ. Antimicrob. Agents Chemother. 2007, 51:3983-3987.
94. Bae S., Lee K. Distribution of capsular serotypes and macrolide resistance mechanisms among macrolide-resistant Streptococcus pneumoniae isolates in Korea. Diagn. Microbiol. Infect. Dis. 2009, 63:213-216.
95. de la Pedrosa E.G., Morosini M.I., van der Linden M., Ruiz-Garbajosa P., Galan J.C., Baquero F., Reinert R.R., Canton R. Polyclonal population structure of Streptococcus pneumoniae isolates in Spain carrying mef and mef plus erm(B). Antimicrob. Agents Chemother. 2008, 52:1964-1969.
96. Reinert R.R., Filimonova O.Y., Al-Lahham A., Grudinina S.A., Ilina E.N., Weigel L.M., Sidorenko S.V. Mechanisms of macrolide resistance among Streptococcus pneumoniae isolates from Russia, Antimicrob. Agents Chemother. 2008, 52:2260-2262.
97. Farrell D.J., Jenkins S.G., Brown S.D., Patel M., Lavin B.S., Klugman K.P. Emergence and spread of Streptococcus pneumoniae with erm(B) and mef(A) resistance. Emerg. Infect. Dis. 2005, 11:851-858.