Download PDF
J Pediatr Infect Dis 2020; 15(06): 283-287
DOI: 10.1055/s-0040-1715855
Original Article

Respiratory Carriage of Haemophilus influenzae Associated with Hib Vaccine in Jordanian Children

Fadia M. Abu Sailik
1   Department of Pathology and Microbiology and Forensic Medicine, School of Medicine, The University of Jordan, Amman, Jordan
,
Eman F. Badran
2   Department of Pediatrics, Jordan University Hospital, Amman, Jordan
,
Basma Marrar
3   Pediatric Division, Al-Bashir Hospital, Ministry of Health, Amman, Jordan
,
Asem A. Shehabi
1   Department of Pathology and Microbiology and Forensic Medicine, School of Medicine, The University of Jordan, Amman, Jordan
› Author Affiliations
› Further Information
    Permissions and Reprints

Abstract

Objective Haemophilus influenzae type b (Hib) is the most virulent serotype that colonizes the upper respiratory tract of children. After introducing Hib conjugate vaccine, Hib has become almost entirely replaced by nontypeable H. influenzae (NTHi) strains. This study investigated the incidence of NTHi, which may cause serious sporadic body infections.

Methods A total of 300 nasal and throat swab samples were obtained from children aged 6 to 60 months, who visited outpatient pediatric clinics of Jordan University Hospital and Al-Bashir Hospital, Amman, Jordan. Colonies resembling H. influenzae were tested by conventional laboratory tests including Gram staining and antibiotic susceptibility. The 16S rRNA and bexA (capsulation gene) were amplified from the extracted DNA. Swabs (n = 100) were delivered to the laboratory in transport media. After initial culture, DNA was extracted directly and tested by conventional polymerase chain reaction (PCR) employing actin beta primers for assessing the housekeeping gene, followed by quantitative PCR (qPCR) against Hib-specific primers.

Results A total of 31/300 (10.33%) of H. influenzae isolates were recovered by culture and confirmed by PCR for 16S rRNA; 96.77% (30/31) were NTHi, and only one isolate was Hib. This isolate was confirmed by detection region II of the cap locus of Hib gene by qualitative TaqMan real-time qPCR. Antibiotic resistance among NTHi to ampicillin and erythromycin was 50.0 and 20.0%, respectively.

Conclusion The conjugated Hib vaccine almost eliminated the occurrence of Hib in the upper respiratory tract of the Jordanian children, while NTHi colonization was found in 10% of them.

Keywords

Haemophilus influenza - nontypeable H. influenza - antimicrobial susceptibility - Jordanian children


Publication History

Received: 10 December 2019

Accepted: 13 July 2020

Article published online:
31 August 2020

Georg Thieme Verlag KG
Stuttgart · New York

 

  • References

  • 1 MacNeil JR, Cohn AC, Farley M. , et al Current epidemiology and trends in invasive Haemophilus influenzae disease--United States, 1989-2008. Clin Infect Dis 2011; 53 (12) 1230-1236
    CrossrefPubMedGoogle Scholar
  • 2 Whittaker R, Economopoulou A, Dias JG, Bancroft E, Ramliden M, Celentano LP. European Centre for Disease Prevention and Control Country Experts for Invasive Haemophilus influenzae Disease. Epidemiology of invasive Haemophilus influenzae disease, Europe, 2007-2014. Emerg Infect Dis 2017; 23 (03) 396-404
    CrossrefPubMedGoogle Scholar
  • 3 World Health Organization. Weekly epidemiological record. 2013; 88 (39) 413-428
    PubMedGoogle Scholar
  • 4 Watt J, Chen S, Santosham M. Haemophilus influenzae type B conjugate vaccine: review of observational data on long term vaccine impact to inform recommendations for vaccine schedules. Geneva: World Health Organization; 2012
    Google Scholar
  • 5 Morris SK, Moss WJ, Halsey N. Haemophilus influenzae type b conjugate vaccine use and effectiveness. Lancet Infect Dis 2008; 8 (07) 435-443
    CrossrefPubMedGoogle Scholar
  • 6 Duell BL, Su YC, Riesbeck K. Host-pathogen interactions of nontypeable Haemophilus influenzae: from commensal to pathogen. FEBS Lett 2016; 590 (21) 3840-3853
    CrossrefPubMedGoogle Scholar
  • 7 MacNeil JR, Cohn AC, Farley M. , et al Current epidemiology and trends in invasive Haemophilus influenzae disease--United States, 1989-2008. Clin Infect Dis 2011; 53 (12) 1230-1236
    CrossrefPubMedGoogle Scholar
  • 8 Resman F, Ristovski M, Ahl J. , et al Invasive disease caused by Haemophilus influenzae in Sweden 1997-2009; evidence of increasing incidence and clinical burden of non-type b strains. Clin Microbiol Infect 2011; 17 (11) 1638-1645
    CrossrefPubMedGoogle Scholar
  • 9 van Wessel K, Rodenburg G, Veenhoven R, Spanjaard L, van der Ende A, Sanders E. Non-typeable Haemophilus influenza invasive disease in The Netherlands: a retrospective surveillance study 2001–2008. Clin Infect Dis 2011; 53 (01) e1-e7 . Doi: 10.1093/cid/cir268
    CrossrefPubMedGoogle Scholar
  • 10 Clinical and Laboratory Standards Institute (CLSI). Performance Standards for Antimicrobial Disk Susceptibility Tests. CLSI Document M07–A10. Villanova, PA, United States: CLSI; 2015
    Google Scholar
  • 11 Tian GZ, Zhang LJ, Wang XL. , et al Rapid detection of Haemophilus influenzae and Haemophilus parainfluenzae in nasopharyngeal swabs by multiplex PCR. Biomed Environ Sci 2012; 25 (03) 367-371
    PubMedGoogle Scholar
  • 12 Falla TJ, Crook DW, Brophy LN, Maskell D, Kroll JS, Moxon ER. PCR for capsular typing of Haemophilus influenzae . J Clin Microbiol 1994; 32 (10) 2382-2386
    CrossrefPubMedGoogle Scholar
  • 13 WHO vaccine-preventable diseases: monitoring system. 2018 Global summary. Available at: http://apps.who.int/immunization_monitoring/globalsummary/estimates?c=JOR.
    Google Scholar
  • 14 Chandran A, Watt J, Santosham M. Haemophilus influenzae. In: Plotkin S, Orenstein W, Offit P. eds. Vaccines, 6th ed. Philadelphia: Elsevier; 2013: 167-182
    Google Scholar
  • 15 Purohit P, Al-Obaid IA, Omar NG. The first reported case of possible Haemophilus influenzae type b vaccine failure from Kuwait and literature-review. J Infect Public Health 2014; 7 (02) 99-105
    CrossrefPubMedGoogle Scholar
  • 16 Maaroufi Y, De Bruyne JM, Heymans C, Crokaert F. Real-time PCR for determining capsular serotypes of Haemophilus influenzae . J Clin Microbiol 2007; 45 (07) 2305-2308
    CrossrefPubMedGoogle Scholar
  • 17 Amin M, Ghaderpanah M, Navidifar T. Detection of Haemophilus influenzae type b, Streptococcus agalactiae, Streptococcus pneumoniae and Neisseria meningitidis in CSF specimens of children suspicious of meningitis in Ahvaz, Iran. Kaohsiung J Med Sci 2016; 32 (10) 501-506
    CrossrefPubMedGoogle Scholar
  • 18 Dunne EM, Murad C, Sudigdoadi S. , et al Carriage of Streptococcus pneumoniae, Haemophilus influenzae, Moraxella catarrhalis, and Staphylococcus aureus in Indonesian children: a cross-sectional study. PLoS One 2018; 13 (04) e0195098
    CrossrefPubMedGoogle Scholar
  • 19 Su YC, Jalalvand F, Thegerström J, Riesbeck K. The interplay between immune response and bacterial infection in COPD: focus upon non-typeable Haemophilus influenzae . Front Immunol 2018; 9: 2530
    CrossrefPubMedGoogle Scholar
  • 20 Romaneli MTDN, Tresoldi AT, Pereira RM, Garcia MT, Hofling CC, Resende MR. Invasive non-type b Haemophilus influenzae disease: report of eight cases. Rev Paul Pediatr 2019; 37 (02) 156-160
    CrossrefPubMedGoogle Scholar
  • 21 Collins S, Litt DJ, Flynn S, Ramsay ME, Slack MP, Ladhani SN. Neonatal invasive Haemophilus influenzae disease in England and Wales: epidemiology, clinical characteristics, and outcome. Clin Infect Dis 2015; 60 (12) 1786-1792
    CrossrefPubMedGoogle Scholar
  • 22 Puig C, Grau I, Marti S. , et al Clinical and molecular epidemiology of haemophilus influenzae causing invasive disease in adult patients. PLoS One 2014; 9 (11) e112711
    CrossrefPubMedGoogle Scholar
  • 23 Pan H, Cui B, Huang Y, Yang J, Ba-Thein W. Nasal carriage of common bacterial pathogens among healthy kindergarten children in Chaoshan region, southern China: a cross-sectional study. BMC Pediatr 2016; 16 (01) 161
    CrossrefPubMedGoogle Scholar
  • 24 World Health Organization. Antimicrobial Resistance Global Report on Surveillance. 2014; 20: 1211
    PubMedGoogle Scholar
  • 25 Frank DN, Feazel LM, Bessesen MT, Price CS, Janoff EN, Pace NR. The human nasal microbiota and Staphylococcus aureus carriage. PLoS One 2010; 5 (05) e10598
    CrossrefPubMedGoogle Scholar
  • 26 Jamsheer A, Rafay AM, Daoud Z, Morrissey I, Torumkuney D. Results from the survey of antibiotic resistance (SOAR) 2011-13 in the Gulf states. J Antimicrob Chemother 2016; 71 (01) (Suppl. 01) i45-i61
    CrossrefPubMedGoogle Scholar
  • 27 Haddadin RN, Alsous M, Wazaify M, Tahaineh L. Evaluation of antibiotic dispensing practice in community pharmacies in Jordan: a cross sectional study. PLoS One 2019; 14 (04) e0216115
    CrossrefPubMedGoogle Scholar