Skip directly to site content Skip directly to page options Skip directly to A-Z link Skip directly to A-Z link Skip directly to A-Z link
Volume 28, Number 1—January 2022
Research

High-Level Quinolone-Resistant Haemophilus haemolyticus in Pediatric Patient with No History of Quinolone Exposure

Emi Tanaka1, Yuji Hirai1, Takeaki WajimaComments to Author , Yu Ishida, Yoshiaki Kawamura, and Hidemasa Nakaminami
Author affiliations: Tokyo University of Pharmacy and Life Sciences, Tokyo, Japan (E. Tanaka, T. Wajima, H. Nakaminami); Meijo University, Nagoya, Japan (E. Tanaka, T. Wajima); Tokyo Medical University Hachioji Medical Centre, Tokyo (Y. Hirai, Y. Ishida); Aichi Gakuin University, Nagoya, Japan (Y. Kawamura)

Main Article

Figure

Genomic analysis of Haemophilus haemolyticus strain 2019-19 from a 9-year-old girl in Japan. A) Circular map of the whole-genome sequence. The outermost circle shows the number of nucleotides, the second circle shows coding sequences on the plus strand, and the third circle shows coding sequences on the minus strand. The innermost circle represents the G+C skew (%) and second innermost circle, G+C content (%); green zones show the locations of gyrA and parC, and blue and light blue zones show CRISPR-Cas–associated genes. Map drawn using Artemis DNA Plotter (Wellcome Sanger institute, Hinxton, UK). G+C, guanine + cytosine. B, C) Comparison between the whole genomes of 2019-19 and H. haemolyticus NCTC 10839 (B) and H. influenzae ATCC 33391T (C), created using Easyfig version 2.2.2 (19). Red indicates matches in the same direction; blue indicates inverted matches; white areas indicate nonmatches.

Figure. Genomic analysis of Haemophilus haemolyticus strain 2019-19 from a 9-year-old girl in Japan. A) Circular map of the whole-genome sequence. The outermost circle shows the number of nucleotides, the second circle shows coding sequences on the plus strand, and the third circle shows coding sequences on the minus strand. The innermost circle represents the G+C skew (%) and second innermost circle, G+C content (%); green zones show the locations of gyrA and parC, and blue and light blue zones show CRISPR-Cas–associated genes. Map drawn using Artemis DNA Plotter (Wellcome Sanger institute, Hinxton, UK). G+C, guanine + cytosine. B, C) Comparison between the whole genomes of 2019-19 and H. haemolyticus NCTC 10839 (B) and H. influenzae ATCC 33391T (C), created using Easyfig version 2.2.2 (19). Red indicates matches in the same direction; blue indicates inverted matches; white areas indicate nonmatches.

Main Article

References
  1. Nørskov-Lauritsen  N. Classification, identification, and clinical significance of Haemophilus and Aggregatibacter species with host specificity for humans. Clin Microbiol Rev. 2014;27:214–40. DOIPubMedGoogle Scholar
  2. Adachi  Y, Ando  M, Morozumi  M, Ubukata  K, Iwata  S. Genotypic characterization of Haemophilus influenzae isolates from paediatric patients in Japan. J Med Microbiol. 2018;67:695–701. DOIPubMedGoogle Scholar
  3. Kilian  M. Genus III. Haemophilus. Winslow, Broadhurst, Buchanan, Rogers and Smith 1917. In: Brenner DJ, Krieg NR, Staley JT, Garrity GM, editors. Bergey’s manual of systematic bacteriology, 2nd ed., vol. 2. The proteobacteriaceae. Part B. The gammaproteobacteria. New York: Springer; 2005. p. 883–904.
  4. Murphy  TF, Brauer  AL, Sethi  S, Kilian  M, Cai  X, Lesse  AJ. Haemophilus haemolyticus: a human respiratory tract commensal to be distinguished from Haemophilus influenzae. J Infect Dis. 2007;195:81–9. DOIPubMedGoogle Scholar
  5. Kirkham  LA, Wiertsema  SP, Mowe  EN, Bowman  JM, Riley  TV, Richmond  PC. Nasopharyngeal carriage of Haemophilus haemolyticus in otitis-prone and healthy children. J Clin Microbiol. 2010;48:2557–9. DOIPubMedGoogle Scholar
  6. McCrea  KW, Xie  J, LaCross  N, Patel  M, Mukundan  D, Murphy  TF, et al. Relationships of nontypeable Haemophilus influenzae strains to hemolytic and nonhemolytic Haemophilus haemolyticus strains. J Clin Microbiol. 2008;46:406–16. DOIPubMedGoogle Scholar
  7. Mukundan  D, Ecevit  Z, Patel  M, Marrs  CF, Gilsdorf  JR. Pharyngeal colonization dynamics of Haemophilus influenzae and Haemophilus haemolyticus in healthy adult carriers. J Clin Microbiol. 2007;45:3207–17. DOIPubMedGoogle Scholar
  8. Hotomi  M, Kono  M, Togawa  A, Arai  J, Takei  S, Ikeda  Y, et al. Haemophilus influenzae and Haemophilus haemolyticus in tonsillar cultures of adults with acute pharyngotonsillitis. Auris Nasus Larynx. 2010;37:594–600. DOIPubMedGoogle Scholar
  9. Seyama  S, Wajima  T, Yanagisawa  Y, Nakaminami  H, Ushio  M, Fujii  T, et al. Rise in Haemophilus influenzae with reduced quinolone susceptibility and development of a simple screening method. Pediatr Infect Dis J. 2017;36:263–6. DOIPubMedGoogle Scholar
  10. Tanaka  E, Hara  N, Wajima  T, Ochiai  S, Seyama  S, Shirai  A, et al. Emergence of Haemophilus influenzae with low susceptibility to quinolones and persistence in tosufloxacin treatment. J Glob Antimicrob Resist. 2019;18:104–8. DOIPubMedGoogle Scholar
  11. Yokota  S, Ohkoshi  Y, Sato  K, Fujii  N. Emergence of fluoroquinolone-resistant Haemophilus influenzae strains among elderly patients but not among children. J Clin Microbiol. 2008;46:361–5. DOIPubMedGoogle Scholar
  12. Cherkaoui  A, Gaïa  N, Baud  D, Leo  S, Fischer  A, Ruppe  E, et al. Molecular characterization of fluoroquinolones, macrolides, and imipenem resistance in Haemophilus influenzae: analysis of the mutations in QRDRs and assessment of the extent of the AcrAB-TolC-mediated resistance. Eur J Clin Microbiol Infect Dis. 2018;37:2201–10. DOIPubMedGoogle Scholar
  13. Puig  C, Tirado-Vélez  JM, Calatayud  L, Tubau  F, Garmendia  J, Ardanuy  C, et al. Molecular characterization of fluoroquinolone resistance in nontypeable Haemophilus influenzae clinical isolates. Antimicrob Agents Chemother. 2015;59:461–6. DOIPubMedGoogle Scholar
  14. Tateda  K, Ohno  A, Ishii  Y, Murakami  H, Yamaguchi  K; Levofloxacin surveillance group. Investigation of the susceptibility trends in Japan to fluoroquinolones and other antimicrobial agents in a nationwide collection of clinical isolates: A longitudinal analysis from 1994 to 2016. J Infect Chemother. 2019;25:594–604. DOIPubMedGoogle Scholar
  15. Yamada  S, Seyama  S, Wajima  T, Yuzawa  Y, Saito  M, Tanaka  E, et al. β-Lactamase-non-producing ampicillin-resistant Haemophilus influenzae is acquiring multidrug resistance. J Infect Public Health. 2020;13:497–501. DOIPubMedGoogle Scholar
  16. Ishiwada  N, Fujimaki  K, Matsumoto  T, Kiyota  H, Tateda  K, Sato  J, et al. Nationwide surveillance of bacterial pathogens isolated from children conducted by the surveillance committee of Japanese Society of Chemotherapy, the Japanese Association for Infectious Diseases, and the Japanese Society for Clinical Microbiology in 2017: General overview of pathogenic antimicrobial susceptibility. J Infect Chemother. 2021;27:139–50. DOIPubMedGoogle Scholar
  17. Marti  S, Puig  C, de la Campa  AG, Tirado-Velez  JM, Tubau  F, Domenech  A, et al. Identification of Haemophilus haemolyticus in clinical samples and characterization of their mechanisms of antimicrobial resistance. J Antimicrob Chemother. 2016;71:80–4. DOIPubMedGoogle Scholar
  18. Clinical Laboratory and Standards Institute. Performance standards for antimicrobial susceptibility testing (M100). 29th ed. Wayne (PA): The Institute; 2019.
  19. Sullivan  MJ, Petty  NK, Beatson  SA. Easyfig: a genome comparison visualizer. Bioinformatics. 2011;27:1009–10. DOIPubMedGoogle Scholar
  20. Richter  M, Rosselló-Móra  R, Oliver Glöckner  F, Peplies  J. JSpeciesWS: a web server for prokaryotic species circumscription based on pairwise genome comparison. Bioinformatics. 2016;32:929–31. DOIPubMedGoogle Scholar
  21. Meier-Kolthoff  JP, Göker  M. TYGS is an automated high-throughput platform for state-of-the-art genome-based taxonomy. Nat Commun. 2019;10:2182. DOIPubMedGoogle Scholar
  22. Grissa  I, Vergnaud  G, Pourcel  C. CRISPRFinder: a web tool to identify clustered regularly interspaced short palindromic repeats. Nucleic Acids Res. 2007;35(Web Server issue):W52–7.
  23. Christensen  H, Kuhnert  P, Olsen  JE, Bisgaard  M. Comparative phylogenies of the housekeeping genes atpD, infB and rpoB and the 16S rRNA gene within the Pasteurellaceae. Int J Syst Evol Microbiol. 2004;54:1601–9. DOIPubMedGoogle Scholar
  24. Bruin  JP, Kostrzewa  M, van der Ende  A, Badoux  P, Jansen  R, Boers  SA, et al. Identification of Haemophilus influenzae and Haemophilus haemolyticus by matrix-assisted laser desorption ionization-time of flight mass spectrometry. Eur J Clin Microbiol Infect Dis. 2014;33:279–84. DOIPubMedGoogle Scholar
  25. Saffert  RT, Cunningham  SA, Ihde  SM, Jobe  KE, Mandrekar  J, Patel  R. Comparison of Bruker Biotyper matrix-assisted laser desorption ionization-time of flight mass spectrometer to BD Phoenix automated microbiology system for identification of gram-negative bacilli. J Clin Microbiol. 2011;49:887–92. DOIPubMedGoogle Scholar
  26. Collins  S, Vickers  A, Ladhani  SN, Flynn  S, Platt  S, Ramsay  ME, et al. Clinical and molecular epidemiology of childhood invasive nontypeable Haemophilus influenzae disease in England and Wales. Pediatr Infect Dis J. 2016;35:e76–84. DOIPubMedGoogle Scholar
  27. Lulitanond  A, Chanawong  A, Pienthaweechai  K, Sribenjalux  P, Tavichakorntrakool  R, Wilailuckana  C, et al. Prevalence of β-lactamase-negative ampicillin-resistant haemophilus influenzae isolated from patients of a teaching hospital in Thailand. Jpn J Infect Dis. 2012;65:122–5.PubMedGoogle Scholar
  28. Richter  M, Rosselló-Móra  R. Shifting the genomic gold standard for the prokaryotic species definition. Proc Natl Acad Sci U S A. 2009;106:19126–31. DOIPubMedGoogle Scholar
  29. Meier-Kolthoff  JP, Auch  AF, Klenk  HP, Göker  M. Genome sequence-based species delimitation with confidence intervals and improved distance functions. BMC Bioinformatics. 2013;14:60. DOIPubMedGoogle Scholar
  30. Harris  TM, Price  EP, Sarovich  DS, Nørskov-Lauritsen  N, Beissbarth  J, Chang  AB, et al. Comparative genomic analysis identifies X-factor (haemin)-independent Haemophilus haemolyticus: a formal re-classification of ‘Haemophilus intermedius’. Microb Genom. 2020;6:e000303. DOIPubMedGoogle Scholar
  31. Georgiou  M, Muñoz  R, Román  F, Cantón  R, Gómez-Lus  R, Campos  J, et al. Ciprofloxacin-resistant Haemophilus influenzae strains possess mutations in analogous positions of GyrA and ParC. Antimicrob Agents Chemother. 1996;40:1741–4. DOIPubMedGoogle Scholar
  32. Chang  CM, Tang  HJ, Wang  LR, Shih  HI, Huang  CC, Lee  NY, et al. Increasing resistance to fluoroquinolones among Haemophilus species in Southern Taiwan. J Microbiol Immunol Infect. 2017;50:258–60. DOIPubMedGoogle Scholar
  33. Rodríguez-Martínez  JM, López-Hernández  I, Pascual  A. Molecular characterization of high-level fluoroquinolone resistance in a clinical isolate of Haemophilus parainfluenzae. J Antimicrob Chemother. 2011;66:673–5. DOIPubMedGoogle Scholar
  34. Mikasa  K, Aoki  N, Aoki  Y, Abe  S, Iwata  S, Ouchi  K, et al. JAID/JSC guidelines for the treatment of respiratory infectious diseases: the Japanese Association for Infectious Diseases/Japanese Society of Chemotherapy—the JAID/JSC guide to clinical management of infectious disease/Guideline-preparing Committee Respiratory Infectious Disease WG. J Infect Chemother. 2016;22(Suppl):S1–65. DOIPubMedGoogle Scholar
  35. Wouters  I, Desmet  S, Van Heirstraeten  L, Herzog  SA, Beutels  P, Verhaegen  J, et al. NPcarriage Study Group. How nasopharyngeal pneumococcal carriage evolved during and after a PCV13-to-PCV10 vaccination programme switch in Belgium, 2016 to 2018. Euro Surveill. 2020;25:1900303. DOIGoogle Scholar
  36. Takahata  S, Ida  T, Senju  N, Sanbongi  Y, Miyata  A, Maebashi  K, et al. Horizontal gene transfer of ftsI, encoding penicillin-binding protein 3, in Haemophilus influenzae. Antimicrob Agents Chemother. 2007;51:1589–95. DOIPubMedGoogle Scholar
  37. Witherden  EA, Bajanca-Lavado  MP, Tristram  SG, Nunes  A. Role of inter-species recombination of the ftsI gene in the dissemination of altered penicillin-binding-protein-3-mediated resistance in Haemophilus influenzae and Haemophilus haemolyticus. J Antimicrob Chemother. 2014;69:1501–9. DOIPubMedGoogle Scholar

Main Article

1These authors contributed equally to this article.

Page created: November 10, 2021
Page updated: December 22, 2021
Page reviewed: December 22, 2021
The conclusions, findings, and opinions expressed by authors contributing to this journal do not necessarily reflect the official position of the U.S. Department of Health and Human Services, the Public Health Service, the Centers for Disease Control and Prevention, or the authors' affiliated institutions. Use of trade names is for identification only and does not imply endorsement by any of the groups named above.
file_external