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. 1988 Apr;1(2):218–227. doi: 10.1128/cmr.1.2.218

Haemophilus influenzae: antibiotic susceptibility.

C A Needham 1
PMCID: PMC358043  PMID: 3069197

Abstract

Ampicillin resistance was first reported among clinical isolates of Haemophilus influenzae in 1972. Reports of chloramphenicol resistance followed shortly thereafter. The principal mechanism of resistance to these two antibiotics is enzymatic. Although other mechanisms have been described, they are found in comparatively few strains. The genetic information for the inactivating enzymes is plasmid mediated and therefore readily transmissible to susceptible strains. Consequently, effective therapy for invasive disease caused by this pathogen has been seriously compromised. As antibiotic susceptibility became less predictable, in vitro testing became increasingly important. Unfortunately, the standardization of methods for laboratory testing has been slow and complicated by the fastidious nature of the organisms. This review traces the development of antibiotic resistance in H. influenzae, discusses the mechanisms which appear to be important in mediating resistance, explores newer antimicrobial agents which might be useful in the treatment of infection, and analyzes the various approaches to in vitro testing.

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Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Albritton W. L., Bendler J. W., Setlow J. K. Plasmid transformation in Haemophilus influenzae. J Bacteriol. 1981 Feb;145(2):1099–1101. doi: 10.1128/jb.145.2.1099-1101.1981. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Albritton W. L., Brunton J. L., Meier M., Bowman M. N., Slaney L. A. Haemophilus influenzae: comparison of respiratory tract isolates with genitourinary tract isolates. J Clin Microbiol. 1982 Nov;16(5):826–831. doi: 10.1128/jcm.16.5.826-831.1982. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Arpi M., Hønberg P. Z., Frimodt-Møller N. Antibiotic susceptibility of Haemophilus influenzae isolated from cerebrospinal fluid and blood. Acta Pathol Microbiol Immunol Scand B. 1986 Jun;94(3):167–171. doi: 10.1111/j.1699-0463.1986.tb03037.x. [DOI] [PubMed] [Google Scholar]
  4. Azemun P., Stull T., Roberts M., Smith A. L. Rapid detection of chloramphenicol resistance in Haemophilus influenzae. Antimicrob Agents Chemother. 1981 Aug;20(2):168–170. doi: 10.1128/aac.20.2.168. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Azimi P. H., Chase P. A. The role of cefamandole in the treatment of Haemophilus influenzae infections in infants and children. J Pediatr. 1981 Jun;98(6):995–1000. doi: 10.1016/s0022-3476(81)80616-6. [DOI] [PubMed] [Google Scholar]
  6. Bannatyne R. M., Cheung R. Susceptibility of Haemophilus influenzae type b to rifampin and sulfisoxazole. Antimicrob Agents Chemother. 1978 Jun;13(6):969–970. doi: 10.1128/aac.13.6.969. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Bannatyne R. M., Toma S., Cheung R., Hodge D. Antibiotic susceptibility of blood and cerebrospinal fluid isolates of Haemophilus influenzae. J Antimicrob Chemother. 1985 Feb;15(2):187–191. doi: 10.1093/jac/15.2.187. [DOI] [PubMed] [Google Scholar]
  8. Barkin R. M., Todd J. K., Roe M. H. Rapid ampicillin susceptibility testing for Haemophilus influenzae. Am J Clin Pathol. 1977 Jan;67(1):100–103. doi: 10.1093/ajcp/67.1.100. [DOI] [PubMed] [Google Scholar]
  9. Bergeron M. G., Claveau S., Simard P. Limited in vitro activity of cefamandole against 100 beta-lactamase- and non-beta-lactamase-producing Haemophilus influenzae strains: comparison of moxalactam, chloramphenicol, and ampicillin. Antimicrob Agents Chemother. 1981 Jan;19(1):101–105. doi: 10.1128/aac.19.1.101. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Bergeron M. G., Simard P., Provencher P. Influence of growth medium and supplement on growth of Haemophilus influenzae and on antibacterial activity of several antibiotics. J Clin Microbiol. 1987 Apr;25(4):650–655. doi: 10.1128/jcm.25.4.650-655.1987. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Bill N. J., Washington J. A., 2nd Comparison of in vitro activity of cephalexin, cephradine, and cefaclor. Antimicrob Agents Chemother. 1977 Mar;11(3):470–474. doi: 10.1128/aac.11.3.470. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Bottone E. J., Brandman Z., Schneierson S. S. Spheroplasts of Haemophilus influenzae induced by cell wall-active antibiotics and their effect upon the interpretation of susceptibility tests. Antimicrob Agents Chemother. 1976 Feb;9(2):327–333. doi: 10.1128/aac.9.2.327. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Boughton W. H. Rapid detection in spinal fluid of beta-lactamase produced by ampicillin-resistant Haemophilus influenzae. J Clin Microbiol. 1982 Jun;15(6):1167–1168. doi: 10.1128/jcm.15.6.1167-1168.1982. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Brunton J. L., Clare D., Ehrman N., Meier M. A. Evolution of antibiotic resistance plasmids in Neisseria gonorrhoeae and Haemophilus species. Clin Invest Med. 1983;6(3):221–228. [PubMed] [Google Scholar]
  15. Bulger R. R., Washington J. A., 2nd Effect of inoculum size and beta-lactamase production on in vitro activity of new cephalosporins against Haemophilus species. Antimicrob Agents Chemother. 1980 Mar;17(3):393–396. doi: 10.1128/aac.17.3.393. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Burns J. L., Mendelman P. M., Levy J., Stull T. L., Smith A. L. A permeability barrier as a mechanism of chloramphenicol resistance in Haemophilus influenzae. Antimicrob Agents Chemother. 1985 Jan;27(1):46–54. doi: 10.1128/aac.27.1.46. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Burns J. L., Smith A. L. Chloramphenicol accumulation by Haemophilus influenzae. Antimicrob Agents Chemother. 1987 May;31(5):686–690. doi: 10.1128/aac.31.5.686. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Campos Marqués J., García-Tornel S., Galvi Tahull J. M. Invasive infections caused by multiply resistant Haemophilus influenzae type b. J Pediatr. 1984 Jan;104(1):162–163. doi: 10.1016/s0022-3476(84)80626-5. [DOI] [PubMed] [Google Scholar]
  19. Campos J., Garcia-Tornel S., Sanfeliu I. Susceptibility studies of multiply resistant Haemophilus influenzae isolated from pediatric patients and contacts. Antimicrob Agents Chemother. 1984 Jun;25(6):706–709. doi: 10.1128/aac.25.6.706. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Campos J., García-Tornel S., Gairí J. M., Fábregues I. Multiply resistant Haemophilus influenzae type b causing meningitis: comparative clinical and laboratory study. J Pediatr. 1986 Jun;108(6):897–902. doi: 10.1016/s0022-3476(86)80923-4. [DOI] [PubMed] [Google Scholar]
  21. Catlin B. W. Iodometric detection of Haemophilus influenzae beta-lactamase: rapid presumptive test for ampicillin resistance. Antimicrob Agents Chemother. 1975 Mar;7(3):265–270. doi: 10.1128/aac.7.3.265. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Coulton J. W., Mason P., Dorrance D. The permeability barrier of Haemophilus influenzae type b against beta-lactam antibiotics. J Antimicrob Chemother. 1983 Nov;12(5):435–449. doi: 10.1093/jac/12.5.435. [DOI] [PubMed] [Google Scholar]
  23. D'Agostino R. L., Tilton R. C. Quantitative antibiotic susceptibility testing: Haemophilus influenzae type B. Ann Clin Lab Sci. 1976 Jan-Feb;6(1):104–109. [PubMed] [Google Scholar]
  24. De Graaff J., Elwell L. P., Falkow S. Molecular nature of two beta-lactamase-specifying plasmids isolated from Haemophilus influenzae type b. J Bacteriol. 1976 Apr;126(1):439–446. doi: 10.1128/jb.126.1.439-446.1976. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Deneer H. G., Slaney L., Maclean I. W., Albritton W. L. Mobilization of nonconjugative antibiotic resistance plasmids in Haemophilus ducreyi. J Bacteriol. 1982 Feb;149(2):726–732. doi: 10.1128/jb.149.2.726-732.1982. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Doern G. V., Chapin K. C. Susceptibility of Haemophilus influenzae to amoxicillin/clavulanic acid, erythromycin, cefaclor, and trimethoprim/sulfamethoxazole. Diagn Microbiol Infect Dis. 1986 Jan;4(1):37–41. doi: 10.1016/0732-8893(86)90054-4. [DOI] [PubMed] [Google Scholar]
  27. Doern G. V., Daum G. S., Tubert T. A. Ampicillin disk diffusion susceptibility testing of Haemophilus influenzae. J Clin Microbiol. 1987 Sep;25(9):1675–1678. doi: 10.1128/jcm.25.9.1675-1678.1987. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. Doern G. V., Daum G. S., Tubert T. A. In vitro chloramphenicol susceptibility testing of Haemophilus influenzae: disk diffusion procedures and assays for chloramphenicol acetyltransferase. J Clin Microbiol. 1987 Aug;25(8):1453–1455. doi: 10.1128/jcm.25.8.1453-1455.1987. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. Doern G. V., Jorgensen J. H., Thornsberry C., Preston D. A. Prevalence of antimicrobial resistance among clinical isolates of Haemophilus influenzae: a collaborative study. Diagn Microbiol Infect Dis. 1986 Feb;4(2):95–107. doi: 10.1016/0732-8893(86)90143-4. [DOI] [PubMed] [Google Scholar]
  30. Eickhoff T. C., Ehret J. M., Baines R. D. Characterization of an ampicillin-resistant Haemophilus influenzae type B. Antimicrob Agents Chemother. 1976 Jun;9(6):889–892. doi: 10.1128/aac.9.6.889. [DOI] [PMC free article] [PubMed] [Google Scholar]
  31. Elwell L. P., De Graaff J., Seibert D., Falkow S. Plasmid-linked ampicillin resistance in haempohilus influenza type b. Infect Immun. 1975 Aug;12(2):404–410. doi: 10.1128/iai.12.2.404-410.1975. [DOI] [PMC free article] [PubMed] [Google Scholar]
  32. Elwell L. P., Saunders J. R., Richmond M. H., Falkow S. Relationships among some R plasmids found in Haemophilus influenzae. J Bacteriol. 1977 Jul;131(1):356–362. doi: 10.1128/jb.131.1.356-362.1977. [DOI] [PMC free article] [PubMed] [Google Scholar]
  33. Escamilla J. Susceptibility of Haemophilus influenza to ampicillin as determined by use of a modified, one-minute beta-lactamase test. Antimicrob Agents Chemother. 1976 Jan;9(1):196–198. doi: 10.1128/aac.9.1.196. [DOI] [PMC free article] [PubMed] [Google Scholar]
  34. Farooki Z. Q., Henry J. G., Green E. W. Hemophilus influenzae pericarditis associated with meningitis. Clin Pediatr (Phila) 1974 Jul;13(7):609–610. doi: 10.1177/000992287401300712. [DOI] [PubMed] [Google Scholar]
  35. Feldman W. E. Concentrations of bacteria in cerebrospinal fluid of patients with bacterial meningitis. J Pediatr. 1976 Apr;88(4 Pt 1):549–552. doi: 10.1016/s0022-3476(76)80003-0. [DOI] [PubMed] [Google Scholar]
  36. Gordon R. C., Thompson T. R., Stevens L. I., Carlson W. H. In vitro susceptibility of Haemophilus influenzae to eight antibiotics. Antimicrob Agents Chemother. 1974 Jul;6(1):114–115. doi: 10.1128/aac.6.1.114. [DOI] [PMC free article] [PubMed] [Google Scholar]
  37. Granoff D. M., Sargent E., Jolivette D. Haemophilus influenzae type b osteomyelitis. Am J Dis Child. 1978 May;132(5):488–490. doi: 10.1001/archpedi.1978.02120300048009. [DOI] [PubMed] [Google Scholar]
  38. Gray B. M., Hubbell C. A., Dillon H. C., Jr Manner and meaning of susceptibility testing of ampicillin-resistant Haemophilus influenzae. Antimicrob Agents Chemother. 1977 Jun;11(6):1021–1026. doi: 10.1128/aac.11.6.1021. [DOI] [PMC free article] [PubMed] [Google Scholar]
  39. Grunberg E., Cleeland R., Beskid G., DeLorenzo W. F. In vivo synergy between 6 beta-amidinopenicillanic acid derivatives and other antibiotics. Antimicrob Agents Chemother. 1976 Apr;9(4):589–594. doi: 10.1128/aac.9.4.589. [DOI] [PMC free article] [PubMed] [Google Scholar]
  40. Heffron F., Sublett R., Hedges R. W., Jacob A., Falkow S. Origin of the TEM-beta-lactamase gene found on plasmids. J Bacteriol. 1975 Apr;122(1):250–256. doi: 10.1128/jb.122.1.250-256.1975. [DOI] [PMC free article] [PubMed] [Google Scholar]
  41. Howard A. J., Hince C. J. The activity of N-formimidoyl thienamycin (MK0787) against Haemophilus influenzae and Streptococcus pneumoniae. J Antimicrob Chemother. 1982 Nov;10(5):383–390. doi: 10.1093/jac/10.5.383. [DOI] [PubMed] [Google Scholar]
  42. Istre G. R., Conner J. S., Glode M. P., Hopkins R. S. Increasing ampicillin-resistance rates in Hemophilus influenzae meningitis. Am J Dis Child. 1984 Apr;138(4):366–369. doi: 10.1001/archpedi.1984.02140420032012. [DOI] [PubMed] [Google Scholar]
  43. Jokipii L., Jokipii A. M. Emergence and prevalence of beta-lactamase producing Haemophilus influenzae in Finland and susceptibility of 102 respiratory isolates to eight antibiotics. J Antimicrob Chemother. 1980 Sep;6(5):623–631. doi: 10.1093/jac/6.5.623. [DOI] [PubMed] [Google Scholar]
  44. Jorgensen J. H., Alexander G. A. Comparative activities of selected beta-lactam antibiotics against Haemophilus influenzae. Antimicrob Agents Chemother. 1978 Feb;13(2):342–343. doi: 10.1128/aac.13.2.342. [DOI] [PMC free article] [PubMed] [Google Scholar]
  45. Jorgensen J. H., Jones P. M. Simplified medium for ampicillin susceptibility testing of Haemophilus influenzae. Antimicrob Agents Chemother. 1975 Feb;7(2):186–190. doi: 10.1128/aac.7.2.186. [DOI] [PMC free article] [PubMed] [Google Scholar]
  46. Jorgensen J. H., Lee J. C. Microdilution technique for antimicrobial susceptibility testing of Haemophilus influenzae. Antimicrob Agents Chemother. 1975 Nov;8(5):610–611. doi: 10.1128/aac.8.5.610. [DOI] [PMC free article] [PubMed] [Google Scholar]
  47. Jorgensen J. H., Lee J. C. Standardized disk-diffusion susceptibility test for Haemophilus influenzae. Am J Clin Pathol. 1977 Mar;67(3):264–268. doi: 10.1093/ajcp/67.3.264. [DOI] [PubMed] [Google Scholar]
  48. Jorgensen J. H., Redding J. S., Maher L. A., Howell A. W. Improved medium for antimicrobial susceptibility testing of Haemophilus influenzae. J Clin Microbiol. 1987 Nov;25(11):2105–2113. doi: 10.1128/jcm.25.11.2105-2113.1987. [DOI] [PMC free article] [PubMed] [Google Scholar]
  49. Kammer R. B., Preston D. A., Turner J. R., Hawley L. C. Rapid detection of ampicillin-resistant Haemophilus influenzae and their susceptibility to sixteen antibiotics. Antimicrob Agents Chemother. 1975 Jul;8(1):91–94. doi: 10.1128/aac.8.1.91. [DOI] [PMC free article] [PubMed] [Google Scholar]
  50. Kaplan S. L., Mason E. O., Kvernland S. J. Effect of prior antibiotics on the susceptibility of Haemophilus influenzae type b to ampicillin. Pediatrics. 1981 Feb;67(2):269–271. [PubMed] [Google Scholar]
  51. Khan W., Ross S., Rodriguez W., Controni G., Saz A. K. Haemophilus influenzae type B resistant to ampicillin. A report of two cases. JAMA. 1974 Jul 15;229(3):298–301. [PubMed] [Google Scholar]
  52. Kinmonth A. L., Storrs C. N., Mitchell R. G. Meningitis due to chloramphenicol-resistant Haemophilus influenzae type b. Br Med J. 1978 Mar 18;1(6114):694–694. doi: 10.1136/bmj.1.6114.694. [DOI] [PMC free article] [PubMed] [Google Scholar]
  53. Kirven L. A., Thornsberry C. In vitro susceptibility of Haemophilus influenzae to trimethoprim-sulfamethoxazole. Antimicrob Agents Chemother. 1974 Dec;6(6):869–870. doi: 10.1128/aac.6.6.869. [DOI] [PMC free article] [PubMed] [Google Scholar]
  54. Laufs R., Kaulfers P. M., Jahn G., Teschner U. Molecular characterization of a small Haemophilus influenzae plasmid specifying beta-lactamase and its relationship to R factors from Neisseria gonorrhoeae. J Gen Microbiol. 1979 Mar;111(1):223–231. doi: 10.1099/00221287-111-1-223. [DOI] [PubMed] [Google Scholar]
  55. Laufs R., Riess F. C., Jahn G., Fock R., Kaulfers P. M. Origin of Haemophilus influenzae R factors. J Bacteriol. 1981 Aug;147(2):563–568. doi: 10.1128/jb.147.2.563-568.1981. [DOI] [PMC free article] [PubMed] [Google Scholar]
  56. Lee W. S., Komarmy L. Iodometric spot test for detection of beta-lactamase in Haemophilus influenzae. J Clin Microbiol. 1981 Jan;13(1):224–225. doi: 10.1128/jcm.13.1.224-225.1981. [DOI] [PMC free article] [PubMed] [Google Scholar]
  57. Malouin F., Schryvers A. B., Bryan L. E. Cloning and expression of genes responsible for altered penicillin-binding proteins 3a and 3b in Haemophilus influenzae. Antimicrob Agents Chemother. 1987 Feb;31(2):286–291. doi: 10.1128/aac.31.2.286. [DOI] [PMC free article] [PubMed] [Google Scholar]
  58. Markowitz S. M. Isolation of an ampicillin-resistant, non-beta-lactamase-producing strain of Haemophilus influenzae. Antimicrob Agents Chemother. 1980 Jan;17(1):80–83. doi: 10.1128/aac.17.1.80. [DOI] [PMC free article] [PubMed] [Google Scholar]
  59. Marks M. I. In vitro activity of clindamycin and other antimicrobials against gram-positive bacteria and Hemophilus influenzae. Can Med Assoc J. 1975 Jan 25;112(2):170–173. [PMC free article] [PubMed] [Google Scholar]
  60. Mason E. O., Jr, Kaplan S. L., Anderson D. C., Hinds D. B., Feigin R. D. In vitro susceptibility of 104 clinical isolates of Haemophilus influenzae to moxalactam (LY127935), ampicillin, chloramphenicol, and ticarcillin. Antimicrob Agents Chemother. 1980 Mar;17(3):470–473. doi: 10.1128/aac.17.3.470. [DOI] [PMC free article] [PubMed] [Google Scholar]
  61. Mathies A. W., Jr Penicillins in the treatment of bacterial meningitis. J R Coll Physicians Lond. 1972 Jan;6(2):139–146. [PMC free article] [PubMed] [Google Scholar]
  62. May J. R., Roberts D. E., Ingold A., Want S. V. Osmotically stable L forms of Haemophilus influenzae and their significance in testing sensitivity to penicillins. J Clin Pathol. 1974 Jul;27(7):560–564. doi: 10.1136/jcp.27.7.560. [DOI] [PMC free article] [PubMed] [Google Scholar]
  63. McCracken G. H., Jr, Nelson J. D., Kaplan S. L., Overturf G. D., Rodriguez W. J., Steele R. W. Consensus report: antimicrobial therapy for bacterial meningitis in infants and children. Pediatr Infect Dis J. 1987 Jun;6(6):501–505. [PubMed] [Google Scholar]
  64. McGowan J. E., Jr, Terry P. M., Nahmias A. J. Susceptibility of Haemophilus influenzae isolates from blood and cerebrospinal fluid to ampicillin, chloramphenicol, and trimethoprim-sulfamethoxazole. Antimicrob Agents Chemother. 1976 Jan;9(1):137–139. doi: 10.1128/aac.9.1.137. [DOI] [PMC free article] [PubMed] [Google Scholar]
  65. McLinn S. E., Nelson J. D., Haltalin K. C. Antimicrobial susceptibility of Hemophilus influenzae. Pediatrics. 1970 May;45(5):827–838. [PubMed] [Google Scholar]
  66. Medeiros A. A., O'Brien T. F. Ampicillin-resistant Haemophilus influenzae type B possessing a TEM-type beta-lactamase but little permeability barrier to ampicillin. Lancet. 1975 Mar 29;1(7909):716–719. doi: 10.1016/s0140-6736(75)91630-x. [DOI] [PubMed] [Google Scholar]
  67. Mendelman P. M., Chaffin D. O., Clausen C., Stull T. L., Needham C., Williams J. D., Smith A. L. Failure to detect ampicillin-resistant, non-beta-lactamase-producing Haemophilus influenzae by standard disk susceptibility testing. Antimicrob Agents Chemother. 1986 Aug;30(2):274–280. doi: 10.1128/aac.30.2.274. [DOI] [PMC free article] [PubMed] [Google Scholar]
  68. Mendelman P. M., Chaffin D. O., Stull T. L., Rubens C. E., Mack K. D., Smith A. L. Characterization of non-beta-lactamase-mediated ampicillin resistance in Haemophilus influenzae. Antimicrob Agents Chemother. 1984 Aug;26(2):235–244. doi: 10.1128/aac.26.2.235. [DOI] [PMC free article] [PubMed] [Google Scholar]
  69. Mendelman P. M., Doroshow C. A., Gandy S. L., Syriopoulou V., Weigen C. P., Smith A. L. Plasmid-mediated resistance in multiply resistant Haemophilus influenzae type b causing meningitis: molecular characterization of one strain and review of the literature. J Infect Dis. 1984 Jul;150(1):30–39. doi: 10.1093/infdis/150.1.30. [DOI] [PubMed] [Google Scholar]
  70. Montgomery K., Raymundo L., Jr, Drew W. L. Chromogenic cephalosporin spot test to detect beta-lactamase in clinically significant bacteria. J Clin Microbiol. 1979 Feb;9(2):205–207. doi: 10.1128/jcm.9.2.205-207.1979. [DOI] [PMC free article] [PubMed] [Google Scholar]
  71. Norrby R., Brorsson J. E., Seeberg S. Comparative study of the in vitro antibacterial activity of cefoxitin, cefuroxine, and cephaloridine. Antimicrob Agents Chemother. 1976 Mar;9(3):506–510. doi: 10.1128/aac.9.3.506. [DOI] [PMC free article] [PubMed] [Google Scholar]
  72. O'Callaghan C. H., Morris A., Kirby S. M., Shingler A. H. Novel method for detection of beta-lactamases by using a chromogenic cephalosporin substrate. Antimicrob Agents Chemother. 1972 Apr;1(4):283–288. doi: 10.1128/aac.1.4.283. [DOI] [PMC free article] [PubMed] [Google Scholar]
  73. Overturf G. D., Steinberg E. A., Underman A. E., Wilkins J., Leedom J. M., Mathies A. W., Jr, Wehrle P. F. Comparative trial of carbenicillin and ampicillin therapy for purulent meningitis. Antimicrob Agents Chemother. 1977 Mar;11(3):420–426. doi: 10.1128/aac.11.3.420. [DOI] [PMC free article] [PubMed] [Google Scholar]
  74. Overturf G. D., Wilkins J., Leedom J. M., Ivler D., Mathies A. W. Susceptibility of Hemophilus influenzae, type b, to ampicillin at Los Angeles County/University of Southern California Medical Center. A reappraisal after ten years. J Pediatr. 1975 Aug;87(2):297–300. doi: 10.1016/s0022-3476(75)80606-8. [DOI] [PubMed] [Google Scholar]
  75. Parr T. R., Jr, Bryan L. E. Mechanism of resistance of an ampicillin-resistant, beta-lactamase-negative clinical isolate of Haemophilus influenzae type b to beta-lactam antibiotics. Antimicrob Agents Chemother. 1984 Jun;25(6):747–753. doi: 10.1128/aac.25.6.747. [DOI] [PMC free article] [PubMed] [Google Scholar]
  76. Parr T. R., Jr, Pai C. H., Bryan L. E. Simple screening method for beta-lactamase-positive and -negative ampicillin-resistant Haemophilus influenzae isolates. J Clin Microbiol. 1984 Jul;20(1):131–132. doi: 10.1128/jcm.20.1.131-132.1984. [DOI] [PMC free article] [PubMed] [Google Scholar]
  77. Philpott-Howard J., Williams J. D. Increase in antibiotic resistance in Haemophilus influenzae in the United Kingdom since 1977: report of study group. Br Med J (Clin Res Ed) 1982 May 29;284(6329):1597–1599. doi: 10.1136/bmj.284.6329.1597. [DOI] [PMC free article] [PubMed] [Google Scholar]
  78. Piffaretti J. C., Camponovo T., Borer-Bigliardi B., Arini A. A novel type of resistance plasmid in Haemophilus influenzae. Antimicrob Agents Chemother. 1986 Mar;29(3):511–514. doi: 10.1128/aac.29.3.511. [DOI] [PMC free article] [PubMed] [Google Scholar]
  79. Piot P., van DYCK E., Pattyn S. R. Sensibilitê d' "Haemophilus influenzae" ă 5 antibiotiques et dêtection rapide de sa rêsistance a l'ampicilline. Pathol Biol (Paris) 1977 Feb;25(2):83–87. [PubMed] [Google Scholar]
  80. Price E., Boswell P. A. Letter: Ampicillin-resistant Haemophilus influenzae. Lancet. 1974 May 11;1(7863):936–937. doi: 10.1016/s0140-6736(74)90397-3. [DOI] [PubMed] [Google Scholar]
  81. Richmond M. H., Sykes R. B. The beta-lactamases of gram-negative bacteria and their possible physiological role. Adv Microb Physiol. 1973;9:31–88. doi: 10.1016/s0065-2911(08)60376-8. [DOI] [PubMed] [Google Scholar]
  82. Roberts M. C., Swenson C. D., Owens L. M., Smith A. L. Characterization of chloramphenicol-resistant Haemophilus influenzae. Antimicrob Agents Chemother. 1980 Oct;18(4):610–615. doi: 10.1128/aac.18.4.610. [DOI] [PMC free article] [PubMed] [Google Scholar]
  83. Roberts M., Elwell L. P., Falkow S. Molecular characterization of two beta-lactamase-specifying plasmids isolated from Neisseria gonorrhoeae. J Bacteriol. 1977 Aug;131(2):557–563. doi: 10.1128/jb.131.2.557-563.1977. [DOI] [PMC free article] [PubMed] [Google Scholar]
  84. Rosen I. G., Jacobson J., Rudderman R. Rapid capillary tube method for detecting penicillin resistance in Staphylococcus aureus. Appl Microbiol. 1972 Mar;23(3):649–650. doi: 10.1128/am.23.3.649-650.1972. [DOI] [PMC free article] [PubMed] [Google Scholar]
  85. Rosenblatt J. E., Neumann A. M. A rapid slide test for penicillinase. Am J Clin Pathol. 1978 Mar;69(3):351–354. doi: 10.1093/ajcp/69.1.351. [DOI] [PubMed] [Google Scholar]
  86. Rubin L. G., Medeiros A. A., Yolken R. H., Moxon E. R. Ampicillin treatment failure of apparently beta-lactamase-negative Haemophilus influenzae type b meningitis due to novel beta-lactamase. Lancet. 1981 Nov 7;2(8254):1008–1010. doi: 10.1016/s0140-6736(81)91214-9. [DOI] [PubMed] [Google Scholar]
  87. Sanders C. C., Sanders W. E., Jr In vitro activity of rosamicin against Neisseria and Haemophilus, including penicillinase-producing strains. Antimicrob Agents Chemother. 1977 Aug;12(2):293–294. doi: 10.1128/aac.12.2.293. [DOI] [PMC free article] [PubMed] [Google Scholar]
  88. Scheifele D. W., Syriopoulou V. P., Harding A. L., Emerson B. B., Smith A. L. Evaluation of a rapid beta-lactamase test for detecting ampicillin-resistant strains of Hemophilus influenzae type b. Pediatrics. 1976 Sep;58(3):382–387. [PubMed] [Google Scholar]
  89. Schwartz R., Rodriguez W., Khan W. N. Resistance of H. influenzae to ampicillin. J Pediatr. 1978 Feb;92(2):343–344. doi: 10.1016/s0022-3476(78)80049-3. [DOI] [PubMed] [Google Scholar]
  90. Simard P., Bergeron M. G. Inoculum size effect on the MIC of cefoperazone, moxalactam, cefotaxime, cefoxitin and cephalothin for 118 strains of Haemophilus influenzae including 'tolerant' micro-organisms. J Antimicrob Chemother. 1982 Nov;10(5):397–402. doi: 10.1093/jac/10.5.397. [DOI] [PubMed] [Google Scholar]
  91. Simasathien S., Duangmani C., Echeverria P. Haemophilus influenzae type B resistant to ampicillin and chloramphenicol in an orphanage in Thailand. Lancet. 1980 Dec 6;2(8206):1214–1217. doi: 10.1016/s0140-6736(80)92478-2. [DOI] [PubMed] [Google Scholar]
  92. Sinai R., Hammerberg S., Marks M. I., Pai C. H. In vitro susceptibility of Haemophilus influenzae to sulfamethoxazole-trimethoprim and cefaclor, cephalexin, and cephradine. Antimicrob Agents Chemother. 1978 May;13(5):861–864. doi: 10.1128/aac.13.5.861. [DOI] [PMC free article] [PubMed] [Google Scholar]
  93. Stephenson W. P., Doern G., Gantz N., Lipworth L., Chapin K. Pharyngeal carriage rates of Haemophilus influenzae, type b and non-b, and prevalence of ampicillin-resistant Haemophilus influenzae among healthy day-care children in central Massachusetts. Am J Epidemiol. 1985 Nov;122(5):868–875. doi: 10.1093/oxfordjournals.aje.a114169. [DOI] [PubMed] [Google Scholar]
  94. Strandberg D. A., Jorgensen J. H., Drutz D. J. Activities of newer beta-lactam antibiotics against ampicillin, chloramphenicol, or multiply-resistant Haemophilus influenzae. Diagn Microbiol Infect Dis. 1984 Sep;2(4):333–337. doi: 10.1016/0732-8893(84)90065-8. [DOI] [PubMed] [Google Scholar]
  95. Strausbaugh L. J., Mandaleris C. D., Sande M. A. Cefamandole and ampicillin therapy in experimental Haemophilus influenzae meningitis. J Infect Dis. 1977 Feb;135(2):210–216. doi: 10.1093/infdis/135.2.210. [DOI] [PubMed] [Google Scholar]
  96. Stuy J. H. Plasmid transfer in Haemophilus influenzae. J Bacteriol. 1979 Aug;139(2):520–529. doi: 10.1128/jb.139.2.520-529.1979. [DOI] [PMC free article] [PubMed] [Google Scholar]
  97. Sykes R. B., Griffiths A., Ryan D. M. Comparative acitivity of ampicillin and cefuroxime against three types of Haemophilus influenzae. Antimicrob Agents Chemother. 1977 Apr;11(4):599–604. doi: 10.1128/aac.11.4.599. [DOI] [PMC free article] [PubMed] [Google Scholar]
  98. Sykes R. B., Matthew M., O'Callaghan C. H. R-factor mediated beta-lactamase production by Haemophilus influenzae. J Med Microbiol. 1975 Aug;8(3):437–441. doi: 10.1099/00222615-8-3-437. [DOI] [PubMed] [Google Scholar]
  99. Syriopoulou V. P., Scheifele D. W., Sack C. M., Smith A. L. Effect of inoculum size on the susceptibility of Haemophilus influenzae b to beta-lactam antibiotics. Antimicrob Agents Chemother. 1979 Oct;16(4):510–513. doi: 10.1128/aac.16.4.510. [DOI] [PMC free article] [PubMed] [Google Scholar]
  100. Syriopoulou V., Scheifele D., Smith A. L., Perry P. M., Howie V. Increasing incidence of ampicillin resistance in Hemophilus influenzae. J Pediatr. 1978 Jun;92(6):889–892. doi: 10.1016/s0022-3476(78)80354-0. [DOI] [PubMed] [Google Scholar]
  101. Thirumoorthi M. C., Kobos D. M., Dajani A. S. Susceptibility of Haemophilus influenzae to chloramphenicol and eight beta-lactam antibiotics. Antimicrob Agents Chemother. 1981 Aug;20(2):208–213. doi: 10.1128/aac.20.2.208. [DOI] [PMC free article] [PubMed] [Google Scholar]
  102. Thomas W. J., McReynolds J. W., Mock C. R., Bailey D. W. Letter: Ampicillin-resistant Haemophilus influenzae meningitis. Lancet. 1974 Feb 23;1(7852):313–313. doi: 10.1016/s0140-6736(74)92617-8. [DOI] [PubMed] [Google Scholar]
  103. Thorne G. M., Farrar W. E., Jr Transfer of ampicillin resistance between strains of Haemophilus influenzae type B. J Infect Dis. 1975 Sep;132(3):276–281. doi: 10.1093/infdis/132.3.276. [DOI] [PubMed] [Google Scholar]
  104. Thornsberry C., Baker C. N., Jones R. N. In vitro antimicrobial activity of piperacillin and seven other beta-lactam antibiotics against Neisseria gonorrhoeae and Haemophilus influenzae, including beta-lactamase producing strains. J Antimicrob Chemother. 1979 Mar;5(2):137–142. doi: 10.1093/jac/5.2.137. [DOI] [PubMed] [Google Scholar]
  105. Thornsberry C., Baker C. N., Kirven L. A., Swenson J. M. Susceptibility of ampicillin-resistant Haemophilus influenzae to seven penicillins. Antimicrob Agents Chemother. 1976 Jan;9(1):70–73. doi: 10.1128/aac.9.1.70. [DOI] [PMC free article] [PubMed] [Google Scholar]
  106. Thornsberry C., Kirven L. A. Ampicillin resistance in Haemophilus influenzae as determined by a rapid test for beta-lactamase production. Antimicrob Agents Chemother. 1974 Nov;6(5):653–654. doi: 10.1128/aac.6.5.653. [DOI] [PMC free article] [PubMed] [Google Scholar]
  107. Tomeh M. O., Starr S. E., McGowan J. E., Jr, Terry P. M., Nahmias A. J. Ampicillin-resistant Haemophilus influenzae type B infection. JAMA. 1974 Jul 15;229(3):295–297. [PubMed] [Google Scholar]
  108. Turk D. C. A comparison of chloramphenicol and ampicillin as bactericidal agents for Haemophilus influenzae type B. J Med Microbiol. 1977 Feb;10(1):127–131. doi: 10.1099/00222615-10-1-127. [DOI] [PubMed] [Google Scholar]
  109. Uchiyama N., Greene G. R., Kitts D. B., Thrupp L. D. Meningitis due to Haemophilus influenzae type b resistant to ampicillin and chloramphenicol. J Pediatr. 1980 Sep;97(3):421–424. doi: 10.1016/s0022-3476(80)80193-4. [DOI] [PubMed] [Google Scholar]
  110. Washington J. A., 2nd, Snyder R. J., Kohner P. C. Spurious ampicillin resistance by testing Haemophilus influenzae with agar containing supplement C. Antimicrob Agents Chemother. 1976 Jan;9(1):199–200. doi: 10.1128/aac.9.1.199. [DOI] [PMC free article] [PubMed] [Google Scholar]
  111. Watanakunakorn C., Glotzbecker C. Evaluation of the capillary beta-lactamase test and antimicrobial susceptibility of Haemophilus influenzae. Am J Clin Pathol. 1977 Sep;68(3):351–354. doi: 10.1093/ajcp/68.3.351. [DOI] [PubMed] [Google Scholar]
  112. Williams J. D., Cavanagh P. Letter: Ampicillin-resistant Haemophilus influenzae meningitis. Lancet. 1974 May 4;1(7862):864–864. doi: 10.1016/s0140-6736(74)90508-x. [DOI] [PubMed] [Google Scholar]
  113. Williams J. D., Kattan S., Cavanagh P. Letter: Penicillinase production by Haemophilus influenzae. Lancet. 1974 Jul 13;2(7872):103–103. doi: 10.1016/s0140-6736(74)91663-8. [DOI] [PubMed] [Google Scholar]
  114. Yourassowsky E., Schoutens E. In vitro bacteriostatic and bactericidal activities of 7 cephalosporin antibiotics on Haemophilus influenzae. Int J Clin Pharmacol Biopharm. 1975 Dec;12(4):433–436. [PubMed] [Google Scholar]
  115. Yourassowsky E., van der Linden M. P., Schoutens E. Use and interpretation of Schlichter's test on Haemophilus influenzae: relation of in vitro to in vivo results for cefamandole. J Clin Pathol. 1979 Sep;32(9):956–959. doi: 10.1136/jcp.32.9.956. [DOI] [PMC free article] [PubMed] [Google Scholar]
  116. van Klingeren B., van Embden J. D., Dessens-Kroon M. Plasmid-mediated chloramphenicol resistance in Haemophilus influenzae. Antimicrob Agents Chemother. 1977 Mar;11(3):383–387. doi: 10.1128/aac.11.3.383. [DOI] [PMC free article] [PubMed] [Google Scholar]

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