Hostname: page-component-76fb5796d-vvkck Total loading time: 0 Render date: 2024-04-27T04:18:04.243Z Has data issue: false hasContentIssue false

Nosocomial Outbreak of Upper Respiratory Tract Infection With β-Lactamase-Negative Ampicillin-Resistant Nontypeable Haemophilus influenzae

Published online by Cambridge University Press:  03 April 2018

Reiko Miyahara
Affiliation:
Department of Clinical Medicine, Institute of Tropical Medicine, Nagasaki University, Nagasaki, Japan Department of Human Genetics, Graduate School of Medicine, The University of Tokyo, Tokyo, Japan
Motoi Suzuki*
Affiliation:
Department of Clinical Medicine, Institute of Tropical Medicine, Nagasaki University, Nagasaki, Japan
Konosuke Morimoto
Affiliation:
Department of Clinical Medicine, Institute of Tropical Medicine, Nagasaki University, Nagasaki, Japan
Bin Chang
Affiliation:
National Institute of Infectious Diseases, Tokyo, Japan
Sayaka Yoshida
Affiliation:
Chikamori Hospital, Kochi, Japan
Shiori Yoshinaga
Affiliation:
Chikamori Hospital, Kochi, Japan
Miki Kitamura
Affiliation:
Chikamori Hospital, Kochi, Japan
Mikiko Chikamori
Affiliation:
Chikamori Hospital, Kochi, Japan
Kazunori Oishi
Affiliation:
National Institute of Infectious Diseases, Tokyo, Japan
Tatsuhiko Kitamura
Affiliation:
Chikamori Hospital, Kochi, Japan
Masayuki Ishida
Affiliation:
Chikamori Hospital, Kochi, Japan
*
Address correspondence to Motoi Suzuki, MD, PhD, Department of Clinical Medicine, Institute of Tropical Medicine, Nagasaki University, 1-12-4 Sakamoto, Nagasaki, Japan, 852-852 (mosuzuki@nagasaki-u.ac.jp).

Abstract

OBJECTIVE

To describe the epidemiologic features of an outbreak of an acute respiratory tract infection (ARI) caused by β-lactamase-negative ampicillin-resistant (BLNAR) nontypeable Haemophilus influenzae (NTHi) in an acute-care ward.

DESIGN

Cross-sectional case-control study.

SETTING

An acute-care ward (ward A) in a general hospital of Kochi in western Japan.

METHODS

Patients who shared a room with an index patient and all staff in ward A were screened and followed from July 1 to August 31, 2015. Sputum or throat swab samples were collected from participants and tested by culture and polymerase chain reaction (PCR). The association between detected pathogens and ARI development among all participants was examined. A case-control study was conducted to identify risk factors for disease.

RESULTS

In total, 78 participants, including the index patient, were enrolled. Of all participants, 27 (34.6%) developed mild respiratory symptoms during a 3-week period: 24 were diagnosed as upper respiratory tract infections, and 3 were diagnosed as lower respiratory tract infections. The presence of BLNAR NTHi was confirmed in 13 participants, and multilocus sequence typing demonstrated that these isolates belonged to sequence type 159. All isolates showed identical pulsed-field gel electrophoresis patterns. The presence of BLNAR NTHi was strongly associated with ARI development, whereas viruses were not associated with the disease. Multivariate analyses demonstrated that a history of contact with the index patient was independently associated with ARI caused by BLNAR NTHi.

CONCLUSIONS

BLNAR NTHi has the potential to cause upper respiratory tract infections among adults and to spread rapidly in hospital settings.

Infect Control Hosp Epidemiol 2018;39:652–659

Type
Original Articles
Copyright
© 2018 by The Society for Healthcare Epidemiology of America. All rights reserved 

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

REFERENCES

1. Van Eldere, J, Slack, MPE, Ladhani, S, Cripps, AW. Non-typeable Haemophilus influenzae, an under-recognised pathogen. Lancet Infect Dis 2014;14:12811292.Google Scholar
2. Cilveti, R, Olmo, M, Pérez-Jove, J, et al. Epidemiology of otitis media with spontaneous perforation of the tympanic membrane in young children and association with bacterial nasopharyngeal carriage, recurrences and pneumococcal vaccination in Catalonia, Spain—the prospective HERMES study. PLoS One 2017;12:e0170316.CrossRefGoogle Scholar
3. Wilkinson, TMA, Aris, E, Bourne, S, et al. A prospective, observational cohort study of the seasonal dynamics of airway pathogens in the aetiology of exacerbations in COPD. Thorax 2017;72:919927.Google Scholar
4. Agrawal, A, Murphy, TF. Haemophilus influenzae infections in the H. influenzae type B conjugate vaccine era. J Clin Microbiol 2011;49:37283732.Google Scholar
5. Dworkin, MS, Park, L, Borchardt, SM. The changing epidemiology of invasive Haemophilus influenzae disease, especially in persons. Clin Infect Dis 2007;44:17.CrossRefGoogle ScholarPubMed
6. Puig, C, Grau, I, Marti, S, Tubau, F, Calatayud, L. Clinical and molecular epidemiology of Haemophilus influenzae causing invasive disease in adult patients. PLoS One. 9(11):e112711. doi: 10.1371/journal.pone.0112711.CrossRefGoogle Scholar
7. Van Wessel, K, Rodenburg, GD, Veenhoven, RH, Spanjaard, L, van der Ende, A, Sanders, EAM. Nontypeable Haemophilus influenzae invasive disease in the Netherlands: a retrospective surveillance study 2001–2008. Clin Infect Dis 2011;53:e1e7.Google Scholar
8. Yanagihara, K, Kadota, J, Aoki, N, et al. Nationwide surveillance of bacterial respiratory pathogens conducted by the surveillance committee of Japanese Society of Chemotherapy, the Japanese Association for Infectious Diseases, and the Japanese Society for Clinical Microbiology in 2010: general view of the pathogens’ antibacterial susceptibility. J Infect Chemother 2015;21:410420.Google Scholar
9. Oikawa, J, Ishiwada, N, Takahashi, Y, et al. Changes in nasopharyngeal carriage of Streptococcus pneumoniae, Haemophilus influenzae and Moraxella catarrhalis among healthy children attending a day-care centre before and after official financial support for the 7-valent pneumococcal conjugate vaccine and H. influenzae type B vaccine in Japan. J Infect Chemother 2014;20:146149.Google Scholar
10. Ito, M, Hotomi, M, Maruyama, Y, et al. Clonal spread of beta-lactamase-producing amoxicillin-clavulanate-resistant (BLPACR) strains of non-typeable Haemophilus influenzae among young children attending a day care in Japan. Int J Pediatr Otorhinolaryngol 2010;74:901906.CrossRefGoogle Scholar
11. Navne, JE, Borresen, ML, Slotved, HC, et al. Nasopharyngeal bacterial carriage in young children in Greenland: a population at high risk of respiratory infections. Epidemiol Infect 2016;144:32263236.Google Scholar
12. Smith-Vaughan, HC, Beissbarth, J, Bowman, J, et al. Geographic consistency in dominant, non-typeable Haemophilus influenzae genotypes colonising four distinct Australian paediatric groups: a cohort study. Pneumonia (Nathan) 2016;8:13.Google Scholar
13. Mackenzie, GA, Leach, AJ, Carapetis, JR, Fisher, J, Morris, PS. Epidemiology of nasopharyngeal carriage of respiratory bacterial pathogens in children and adults: cross-sectional surveys in a population with high rates of pneumococcal disease. BMC Infect Dis 2010;10:304.Google Scholar
14. Bosch, AATM, van Houten, MA, Bruin, JP, et al. Nasopharyngeal carriage of Streptococcus pneumoniae and other bacteria in the 7th year after implementation of the pneumococcal conjugate vaccine in the Netherlands. Vaccine 2016;34:531539.Google Scholar
15. Hammitt, LL, Akech, DO, Morpeth, SC, et al. Population effect of 10-valent pneumococcal conjugate vaccine on nasopharyngeal carriage of Streptococcus pneumoniae and non-typeable Haemophilus influenzae in Kilifi, Kenya: findings from cross-sectional carriage studies. Lancet Global Health 2014;2:e397e405.Google Scholar
16. Winokur, PL, Chaloner, K, Doern, GV, Ferreira, J, Apicella, MA. Safety and immunological outcomes following human inoculation with nontypeable Haemophilus influenzae . J Infect Dis 2013;208:728738.Google Scholar
17. Yoshida, L-M, Suzuki, M, Yamamoto, T, et al. Viral pathogens associated with acute respiratory infections in central Vietnamese children. Pediatr Infect Dis J 2010;29:7577.Google Scholar
18. Dice, LR. Measures of the amount of ecologic association between species. Ecology 1945;26:297302.CrossRefGoogle Scholar
19. Meats, E, Feil, EJ, Stringer, S, et al. Characterization of encapsulated and noncapsulated Haemophilus influenzae and determination of phylogenetic relationships by multilocus sequence typing. J Clin Microbiol 2003;41:16231636.Google Scholar
20. Andersson, M, Resman, F, Eitrem, R, et al. Outbreak of a beta-lactam resistant non-typeable Haemophilus influenzae sequence type 14 associated with severe clinical outcomes. BMC Infect Dis 2015;15:129.Google Scholar
21. Yang, C-J, Chen, T-C, Wang, C-S, et al. Nosocomial outbreak of biotype I, multidrug-resistant, serologically non-typeable Haemophilus influenzae in a respiratory care ward in Taiwan. J Hosp Infect 2010;74:406409.Google Scholar
22. Goetz, MB, O’Brien, H, Musser, JM, Ward, JI. Nosocomial transmission of disease caused by nontypeable strains of Haemophilus influenzae . Am J Med 1994;96:342347.Google Scholar
23. Van Dort, M, Walden, C, Walker, ES, Reynolds, SA. An outbreak of infections caused by non-typeable Haemophilus influenzae in an extended care facility. J Hosp Infect 2007;66:5964.CrossRefGoogle Scholar
24. Hekker, T, van der Schee, AC, Kempers, J. A nosocomial outbreak of amoxycillin-resistant non-typable Haemophilus influenzae in a respiratory ward. J Hosp Infect 1991;19:2531.Google Scholar
25. Niki, Y, Hanaki, H, Matsumoto, T, et al. Nationwide surveillance of bacterial respiratory pathogens conducted by the Japanese Society of Chemotherapy in 2008: general view of the pathogens’ antibacterial susceptibility. J Infect Chemother 2011;17:510523.Google Scholar
26. Watanabe, H, Hoshino, K, Sugita, R, et al. Possible high rate of transmission of nontypeable Haemophilus influenzae, including beta-lactamase-negative ampicillin-resistant strains, between children and their parents. J Clin Microbiol 2004;42:362365.Google Scholar
27. Murphy, TF, Lesse, AJ, Kirkham, C, Zhong, H, Sethi, S, Munson, RS Jr. A Clonal group of nontypeable Haemophilus influenzae with Two IgA proteases is adapted to infection in chronic obstructive pulmonary disease. PLoS One 2011;6:e25923.Google Scholar
28. Skaare, D, Anthonisen, IL, Caugant, DA, et al. Multilocus sequence typing and ftsI sequencing: a powerful tool for surveillance of penicillin-binding protein 3-mediated beta-lactam resistance in nontypeable Haemophilus influenzae . BMC Microbiol 2014;14:131.Google Scholar
29. Gough, J, Kraak, WA, Anderson, EC, Nichols, WW, Slack, MP, McGhie, D. Cross-infection by nonencapsulated Haemophilus influenzae . Lancet 1990;336:159160.Google Scholar
30. Sturm, AW, Mostert, R, Rouing, P, Van Klingeren, B. Outbreak of multiresistant non-encapsulated Haemophilus influenzae infections in a pulmonary rehabilitation centre. Lancet 1990;335:214216.Google Scholar
31. Kuster, SP, Shah, PS, Coleman, BL, et al. Incidence of influenza in healthy adults and healthcare workers: a systematic review and meta-analysis. PLoS One 2011;6:e26239.Google Scholar
32. Lu, Y, Tong, J, Pei, F, et al. Viral aetiology in adults with acute upper respiratory tract infection in Jinan, Northern China. Clin Dev Immunol 2013;2013:869521869527.Google ScholarPubMed
33. Thors, V, Christensen, H, Morales-Aza, B, Vipond, I, Muir, P, Finn, A. The effects of live attenuated influenza vaccine on nasopharyngeal bacteria in healthy 2 to 4 year olds: a randomized controlled trial. Am J Respir Crit Care Med 2016;193:14011409.Google Scholar
34. Klugman, KP, Chien, Y-W, Madhi, SA. Pneumococcal pneumonia and influenza: a deadly combination. Vaccine 2009;27(Suppl 3):C9C14.Google Scholar
35. Raina MacIntyre, C, Chughtai, AA, Zhang, Y, et al. Viral and bacterial upper respiratory tract infection in hospital health care workers over time and association with symptoms. BMC Infect Dis 2017;17:553.Google Scholar
36. Hassoun, A, Huff, MD, Weisman, D, et al. Seasonal variation of respiratory pathogen colonization in asymptomatic health care professionals: a single-center, cross-sectional, 2-season observational study. Am J Infect Control 2015;43:865870.Google Scholar
37. Murphy, TF. Vaccines for nontypeable Haemophilus influenzae: the future is now. Clin Vaccine Immunol 2015;22:459466.Google Scholar
Supplementary material: File

Miyahara et al. supplementary material

Table S1

Download Miyahara et al. supplementary material(File)
File 131.9 KB