1887

Abstract

Recent reports have hypothesized that colonization of the maternal genital tract with non-capsulated could result in neonatal invasive disease. In this study, genital carriage of the genus was investigated in 510 pregnant women attending an Italian hospital for routine controls. Overall, vaginal carriage of the genus was 9.0 % (46/510). A high colonization rate with (37/510, 7.3 %) was found; other species, such as (7/510, 1.4 %) and (2/510, 0.4 %), were detected for the first time in the genital flora by 16S rRNA gene sequencing. Notably, no was identified, in agreement with previous investigations indicating that this species is rarely isolated from the genito-urinary tract of pregnant women. No antibiotic resistance was detected in and , but quite a high degree of ampicillin (10/37, 27 %) and ciprofloxacin (3/37, 8.1 %) resistance was observed in . Five ampicillin-resistant isolates were β-lactamase producers, whereas five isolates exhibited a β-lactamase-negative ampicillin-resistant (BLNAR) phenotype. Sequencing of penicillin-binding protein 3 revealed that Val511Ala, Asn526Ser, Ala530Ser and Thr574Ala changes were associated with BLNAR phenotypes. Two ciprofloxacin-resistant isolates carried substitutions in both GyrA (Ser84Phe and Asp88Tyr) and ParC (Ser84Tyr and Met198Leu); the other ciprofloxacin-resistant isolate had substitutions in ParC, only (Ser138Thr and Met198Leu). In conclusion, ∼10 % of pregnant women carried a species of in their genital tract. The emergence of non-β-lactamase-mediated resistance in genital is a matter of concern because of the risk of mother-to-baby transmission.

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2015-07-01
2020-01-22
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References

  1. Albritton W.L., Brunton J.L., Meier M., Bowman M.N., Slaney L.A.. ( 1982;). Haemophilus influenzae: comparison of respiratory tract isolates with genitourinary tract isolates. J Clin Microbiol 16: 826–831 Medline.
    [Google Scholar]
  2. Bäckman A., Lantz P., Rådström P., Olcén P.. ( 1999;). Evaluation of an extended diagnostic PCR assay for detection and verification of the common causes of bacterial meningitis in CSF and other biological samples. Mol Cell Probes 13: 49–600 [CrossRef]
    [Google Scholar]
  3. Barbosa A.R., Giufrè M., Cerquetti M., Bajanca-Lavado M.P.. ( 2011;). Polymorphism in ftsI gene and β-lactam susceptibility in Portuguese Haemophilus influenzae strains: clonal dissemination of β-lactamase-positive isolates with decreased susceptibility to amoxicillin/clavulanic acid. J Antimicrob Chemother 66: 788–796 [CrossRef].
    [Google Scholar]
  4. Barcaite E., Bartusevicius A., Tameliene R., Kliucinskas M., Maleckiene L., Nadisauskiene R.. ( 2008;). Prevalence of maternal group B streptococcal colonisation in European countries. Acta Obstet Gynecol Scand 87: 260–271 [CrossRef]
    [Google Scholar]
  5. Berndsen M.R., Erlendsdóttir H., Gottfredsson M.. ( 2012;). Evolving epidemiology of invasive Haemophilus infections in the post-vaccination era: results from a long-term population-based study. Clin Microbiol Infect 18: 918–923 [CrossRef]
    [Google Scholar]
  6. Cardines R., Giufrè M., Ciofi degli Atti M.L., Accogli M., Mastrantonio P., Cerquetti M.. ( 2009;). Haemophilus parainfluenzae meningitis in an adult associated with acute otitis media. New Microbiol 32: 213–215 Medline.
    [Google Scholar]
  7. Clarridge J.E. III. ( 2004;). Impact of 16S rRNA gene sequence analysis for identification of bacteria on clinical microbiology and infectious diseases. Clin Microbiol Rev 17: 840–862 [CrossRef].
    [Google Scholar]
  8. Collins S., Ramsay M., Slack M.P., Campbell H., Flynn S., Litt D., Ladhani S.N.. ( 2014;). Risk of invasive Haemophilus influenzae infection during pregnancy and association with adverse fetal outcomes. JAMA 311: 1125–1132 [CrossRef].
    [Google Scholar]
  9. Frankard J., Rodriguez-Villalobos H., Struelens M.J., Jacobs F.. ( 2004;). Haemophilus parainfluenzae: an underdiagnosed pathogen of biliary tract infections?. Eur J Clin Microbiol Infect Dis 23: 46–48 [CrossRef].
    [Google Scholar]
  10. García-Cobos S., Campos J., Lázaro E., Román F., Cercenado E., García-Rey C., Pérez-Vázquez M., Oteo J., de Abajo F.. ( 2007;). Ampicillin-resistant non-beta-lactamase-producing Haemophilus influenzae in Spain: recent emergence of clonal isolates with increased resistance to cefotaxime and cefixime. Antimicrob Agents Chemother 51: 2564–2573 [CrossRef].
    [Google Scholar]
  11. García-Cobos S., Arroyo M., Campos J., Pérez-Vázquez M., Aracil B., Cercenado E., Orden B., Lara N., Oteo J.. ( 2013;). Novel mechanisms of resistance to β-lactam antibiotics in Haemophilus parainfluenzae: β-lactamase-negative ampicillin resistance and inhibitor-resistant TEM β-lactamases. J Antimicrob Chemother 68: 1054–1059 [CrossRef].
    [Google Scholar]
  12. Glover W.A., Suarez C.J., Clarridge J.E. III. ( 2011;). Genotypic and phenotypic characterization and clinical significance of ‘Haemophilus quentini’ isolated from the urinary tract of adult men. J Med Microbiol 60: 1689–1692 [CrossRef].
    [Google Scholar]
  13. Govind B., Veeraraghavan B., Anandan S., Thomas N.. ( 2012;). Haemophilus parainfluenzae: report of an unusual cause of neonatal sepsis and a literature review. J Infect Dev Ctries 6: 748–750 [CrossRef].
    [Google Scholar]
  14. Harper J.J., Tilse M.H.. ( 1991;). Biotypes of Haemophilus influenzae that are associated with noninvasive infections. J Clin Microbiol 29: 2539–2542 Medline.
    [Google Scholar]
  15. Heath P.T., Booy R., Azzopardi H.J., Slack M.P., Fogarty J., Moloney A.C., Ramsay M.E., Moxon E.R.. ( 2001;). Non-type b Haemophilus influenzae disease: clinical and epidemiologic characteristics in the Haemophilus influenzae type b vaccine era. Pediatr Infect Dis J 20: 300–305 [CrossRef].
    [Google Scholar]
  16. Houang E., Philippou M., Ahmet Z.. ( 1989;). Comparison of genital and respiratory carriage of Haemophilus parainfluenzae in men. J Med Microbiol 28: 119–123 [CrossRef].
    [Google Scholar]
  17. Jordens J.Z., Slack M.P.. ( 1995;). Haemophilus influenzae: then and now. Eur J Clin Microbiol Infect Dis 14: 935–948 [CrossRef].
    [Google Scholar]
  18. Kaczmarek F.S., Gootz T.D., Dib-Hajj F., Shang W., Hallowell S., Cronan M.. ( 2004;). Genetic and molecular characterization of beta-lactamase-negative ampicillin-resistant Haemophilus influenzae with unusually high resistance to ampicillin. Antimicrob Agents Chemother 48: 1630–1639 [CrossRef].
    [Google Scholar]
  19. Kishii K., Chiba N., Morozumi M., Hamano-Hasegawa K., Ubukata K., Kurokawa I., Masaki J.. ( 2010;). Diverse mutations in the ftsI gene in ampicillin-resistant Haemophilus influenzae isolates from pediatric patients with acute otitis media. J Infect Chemother 16: 87–93 [CrossRef].
    [Google Scholar]
  20. Ladhani S., Slack M.P., Heath P.T., von Gottberg A., Chandra M., Ramsay M.E., European Union Invasive Bacterial Infection Surveillance participants. ( 2010;). Invasive Haemophilus influenzae disease, Europe, 1996–2006. Emerg Infect Dis 16: 455–463 [CrossRef].
    [Google Scholar]
  21. Law D.K., Shuel M., Bekal S., Bryce E., Tsang R.S.. ( 2010;). Genetic detection of quinolone resistance in Haemophilus parainfluenzae: mutations in the quinolone resistance-determining regions of gyrA parC. Can J Infect Dis Med Microbiol 21: e20–e22 Medline.
    [Google Scholar]
  22. Mak G.C., Ho P.L., Tse C.W., Lau S.K., Wong S.S.. ( 2005;). Reduced levofloxacin susceptibility and tetracycline resistance in a clinical isolate of Haemophilus quentini identified by 16S rRNA sequencing. J Clin Microbiol 43: 5391–5392 [CrossRef].
    [Google Scholar]
  23. Markowitz S.M.. ( 1980;). Isolation of an ampicillin-resistant, non-beta-lactamase-producing strain of Haemophilus influenzae. Antimicrob Agents Chemother 17: 80–83 [CrossRef].
    [Google Scholar]
  24. Martel A.Y., St-Laurent G., Dansereau L.A., Bergeron M.G.. ( 1989;). Isolation and biochemical characterization of Haemophilus species isolated simultaneously from the oropharyngeal and anogenital areas. J Clin Microbiol 27: 1486–1489 Medline.
    [Google Scholar]
  25. Morton D.J., Hempel R.J., Whitby P.W., Seale T.W., Stull T.L.. ( 2012;). An invasive Haemophilus haemolyticus isolate. J Clin Microbiol 50: 1502–1503 [CrossRef].
    [Google Scholar]
  26. Murphy T.F., Brauer A.L., Sethi S., Kilian M., Cai X., Lesse A.J.. ( 2007;). Haemophilus haemolyticus: a human respiratory tract commensal to be distinguished from Haemophilus influenzae. J Infect Dis 195: 81–89 [CrossRef].
    [Google Scholar]
  27. Nørskov-Lauritsen N.. ( 2014;). Classification, identification, and clinical significance of Haemophilus Aggregatibacter species with host specificity for humans. Clin Microbiol Rev 27: 214–240 [CrossRef].
    [Google Scholar]
  28. Nørskov-Lauritsen N., Bruun B., Kilian M.. ( 2005;). Multilocus sequence phylogenetic study of the genus Haemophilus with description of Haemophilus pittmaniae sp. nov. Int J Syst Evol Microbiol 55: 449–456 [CrossRef].
    [Google Scholar]
  29. Quentin R., Musser J.M., Mellouet M., Sizaret P.Y., Selander R.K., Goudeau A.. ( 1989;). Typing of urogenital, maternal, and neonatal isolates of Haemophilus influenzae Haemophilus parainfluenzae in correlation with clinical source of isolation and evidence for a genital specificity of H. influenzae biotype IV. J Clin Microbiol 27: 2286–2294 Medline.
    [Google Scholar]
  30. Rele M., Giles M., Daley A.J.. ( 2006;). Invasive Haemophilus parainfluenzae maternal–infant infections: an Australasian perspective and case report. Aust N Z J Obstet Gynaecol 46: 258–260 [CrossRef].
    [Google Scholar]
  31. Rodríguez-Martínez J.M., López-Hernández I., Pascual A.. ( 2011;). Molecular characterization of high-level fluoroquinolone resistance in a clinical isolate of Haemophilus parainfluenzae. J Antimicrob Chemother 66: 673–675 [CrossRef].
    [Google Scholar]
  32. Scheifele D.W., Fussell S.J.. ( 1981;). Frequency of ampicillin-resistant Haemophilus parainfluenzae in children. J Infect Dis 143: 495–498 [CrossRef].
    [Google Scholar]
  33. Schösnheyder H., Ebbesen F., Grunnet N., Ejlertsen T.. ( 1991;). Non-capsulated Haemophilus influenzae in the genital flora of pregnant and post-puerperal women. Scand J Infect Dis 23: 183–187 [CrossRef].
    [Google Scholar]
  34. Sturm A.W.. ( 1986;). Isolation of Haemophilus influenzae Haemophilus parainfluenzae from genital-tract specimens with a selective culture medium. J Med Microbiol 21: 349–352 [CrossRef].
    [Google Scholar]
  35. Takala A.K., Pekkanen E., Eskola J.. ( 1991;). Neonatal Haemophilus influenzae infections. Arch Dis Child 66: 437–440 [CrossRef].
    [Google Scholar]
  36. Tinguely R., Seiffert S.N., Furrer H., Perreten V., Droz S., Endimiani A.. ( 2013;). Emergence of extensively drug-resistant Haemophilus parainfluenzae in Switzerland. Antimicrob Agents Chemother 57: 2867–2869 [CrossRef].
    [Google Scholar]
  37. Tristram S., Jacobs M.R., Appelbaum P.C.. ( 2007;). Antimicrobial resistance in Haemophilus influenzae. Clin Microbiol Rev 20: 368–389 [CrossRef].
    [Google Scholar]
  38. Tristram S.G., Pitout M.J., Forward K., Campbell S., Nichols S., Davidson R.J.. ( 2008;). Characterization of extended-spectrum beta-lactamase-producing isolates of Haemophilus parainfluenzae. J Antimicrob Chemother 61: 509–514 [CrossRef].
    [Google Scholar]
  39. Ubukata K., Shibasaki Y., Yamamoto K., Chiba N., Hasegawa K., Takeuchi Y., Sunakawa K., Inoue M., Konno M.. ( 2001;). Association of amino acid substitutions in penicillin-binding protein 3 with beta-lactam resistance in beta-lactamase-negative ampicillin-resistant Haemophilus influenzae. Antimicrob Agents Chemother 45: 1693–1699 [CrossRef].
    [Google Scholar]
  40. Van Eldere J., Slack M.P., Ladhani S., Cripps A.W.. ( 2014;). Non-typeable Haemophilus influenzae, an under-recognised pathogen. Lancet Infect Dis 14: 1281–1292 [CrossRef].
    [Google Scholar]
  41. Witherden E.A., Bajanca-Lavado M.P., Tristram S.G., Nunes A.. ( 2014;). Role of inter-species recombination of the ftsI gene in the dissemination of altered penicillin-binding-protein-3-mediated resistance in Haemophilus influenzae Haemophilus haemolyticus. J Antimicrob Chemother 69: 1501–1509 [CrossRef].
    [Google Scholar]
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