Emergence of clonally related multidrug resistant Haemophilus influenzae with penicillin-binding protein 3-mediated resistance to extended-spectrum cephalosporins, Norway, 2006 to 2013

Eurosurveillance

Volumn 19, Issue 49, 2014, Pages

  Skaare, D ^a,b   Anthonisen, I L ^a   Kahlmeter, G ^c   Matuschek, E ^c   Natas O B ^d   Steinbakk, M ^e   Sundsfjord, A ^b,f   Kristiansen, B E ^b  

^a VESTFOLD HOSPITAL TRUST   (Norway)

^b UNIVERSITY OF TROMSØ   (Norway)

^c EUCAST Development Laboratory   (Sweden)

^d STAVANGER UNIVERSITY HOSPITAL   (Norway)

^e NORWEGIAN INSTITUTE OF PUBLIC HEALTH   (Norway)

^f UNIVERSITY HOSPITAL OF NORTH NORWAY   (Norway)

Author keywords

[No Author keywords available]

Indexed keywords

AMOXICILLIN; AMPICILLIN; BETA LACTAMASE; CEFEPIME; CEFIXIME; CEFOTAXIME; CEFTAROLINE; CEFTRIAXONE; CEFUROXIME; CEPHALOSPORIN; CHLORAMPHENICOL; CIPROFLOXACIN; CLARITHROMYCIN; COTRIMOXAZOLE; DNA TOPOISOMERASE (ATP HYDROLYSING) A; DOXYCYCLINE; IMIPENEM; LEVOFLOXACIN; MEROPENEM; MINOCYCLINE; PENICILLIN BINDING PROTEIN; PENICILLIN BINDING PROTEIN 3; PENICILLIN G; PIPERACILLIN PLUS TAZOBACTAM; PROTEIN PARC; RIFAMPICIN; TETRACYCLINE; UNCLASSIFIED DRUG;

ACUTE OTITIS MEDIA; ADOLESCENT; ADULT; AGED; ANTIBIOTIC RESISTANCE; ANTIBIOTIC SENSITIVITY; ANTIMICROBIAL THERAPY; ARTICLE; CHILD; CHRONIC OBSTRUCTIVE LUNG DISEASE; CLINICAL ARTICLE; FEMALE; HAEMOPHILUS INFLUENZAE; HUMAN; IMMUNOGLOBULIN DEFICIENCY; LYMPHATIC LEUKEMIA; MALE; MINIMUM INHIBITORY CONCENTRATION; MULTIDRUG RESISTANCE; MYASTHENIA GRAVIS; NUCLEOTIDE SEQUENCE; PNEUMONIA; PRESCHOOL CHILD; PULSED FIELD GEL ELECTROPHORESIS; SCHOOL CHILD; SEQUENCE ALIGNMENT; SEQUENCE HOMOLOGY; TREATMENT OUTCOME; X RAY;

EID: 84919725524     PISSN: 1025496X     EISSN: 15607917     Source Type: Journal    
DOI: 10.2807/1560-7917.ES2014.19.49.20986     Document Type: Article

References (38)

1. Van Eldere J, Slack MP, Ladhani S, Cripps AW. Non-typeable Haemophilus influenzae, an under-recognised pathogen. Lancet Infect Dis. 2014; 14(12): 1281-92. http://dx. doi. org/10. 1016/S1473-3099(14)70734-0 PMID: 25012226.
2. Resman F, Ristovski M, Forsgren A, Kaijser B, Kronvall G, Medstrand P, et al. Increase of β-lactam-resistant invasive Haemophilus influenzae in Sweden, 1997 to 2010. Antimicrob Agents Chemother. 2012; 56(8): 4408-15. http://dx. doi. org/10. 1128/AAC. 00415-12 PMID: 22687505.
3. Garcia-Cobos S, Arroyo M, Perez-Vazquez M, Aracil B, Lara N, Oteo J, et al. Isolates of β-lactamase-negative ampicillinresistant Haemophilus influenzae causing invasive infections in Spain remain susceptible to cefotaxime and imipenem. J Antimicrob Chemother. 2014; 69(1): 111-6. http://dx. doi. org/10. 1093/jac/dkt324 PMID: 23943391.
4. Tristram S, Jacobs MR, Appelbaum PC. Antimicrobial resistance in Haemophilus influenzae. Clin Microbiol Rev. 2007; 20(2): 368-89. http://dx. doi. org/10. 1128/CMR. 00040-06 PMID: 17428889.
5. Leclercq R, Canton R, Brown DF, Giske CG, Heisig P, MacGowan AP, et al. EUCAST expert rules in antimicrobial susceptibility testing. Clin Microbiol Infect. 2013; 19(2): 141-60. http://dx. doi. org/10. 1111/j. 1469-0691. 2011. 03703. x PMID: 22117544.
6. The European Committee on Antimicrobial Susceptibility Testing (EUCAST). Breakpoint tables for interpretation of MICs and zone diameters. Version 4. 0, 2014. Vaxjo: EUCAST; 2014. Available from: http://www. eucast. org.
7. Clinical and Laboratory Standards Institute (CSLI). Performance standards for antimicrobial susceptibility testing, twentythird informational supplement. Wayne, PA: CLSI; 2013. CLSI document M100-S23.
8. Skaare D, Anthonisen IL, Caugant DA, Jenkins A, Steinbakk M, Strand L, et al. Multilocus sequence typing and ftsI sequencing: a powerful tool for surveillance of penicillinbinding protein 3-mediated beta-lactam resistance in nontypeable Haemophilus influenzae. BMC Microbiol. 2014; 14(1): 131. http://dx. doi. org/10. 1186/1471-2180-14-131 PMID: 24884375.
9. Ubukata K, Shibasaki Y, Yamamoto K, Chiba N, Hasegawa K, Takeuchi Y, et al. 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. 2001; 45(6): 1693-9. http://dx. doi. org/10. 1128/AAC. 45. 6. 1693-1699. 2001 PMID: 11353613.
10. Hotomi M, Fujihara K, Billal DS, Suzuki K, Nishimura T, Baba S, et al. Genetic characteristics and clonal dissemination of beta-lactamase-negative ampicillin-resistant Haemophilus influenzae strains isolated from the upper respiratory tract of patients in Japan. Antimicrob Agents Chemother. 2007; 51(11): 3969-76. http://dx. doi. org/10. 1128/AAC. 00422-07 PMID: 17698631.
11. Garcia-Cobos S, Campos J, Lazaro E, Roman F, Cercenado E, Garcia-Rey C, et al. Ampicillin-resistant non-beta-lactamaseproducing Haemophilus influenzae in Spain: recent emergence of clonal isolates with increased resistance to cefotaxime and cefixime. Antimicrob Agents Chemother. 2007; 51(7): 2564-73. http://dx. doi. org/10. 1128/AAC. 00354-07 PMID: 17470649.
12. Hasegawa K, Chiba N, Kobayashi R, Murayama SY, Iwata S, Sunakawa K, et al. Rapidly increasing prevalence of betalactamase-nonproducing, ampicillin-resistant Haemophilus influenzae type b in patients with meningitis. Antimicrob Agents Chemother. 2004; 48(5): 1509-14. http://dx. doi. org/10. 1128/AAC. 48. 5. 1509-1514. 2004 PMID: 15105098.
13. Osaki Y, Sanbongi Y, Ishikawa M, Kataoka H, Suzuki T, Maeda K, et al. Genetic approach to study the relationship between penicillin-binding protein 3 mutations and Haemophilus influenzae beta-lactam resistance by using site-directed mutagenesis and gene recombinants. Antimicrob Agents Chemother. 2005; 49(7): 2834-9. http://dx. doi. org/10. 1128/AAC. 49. 7. 2834-2839. 2005 PMID: 15980357.
14. Ubukata K. Problems associated with high prevalence of multidrug-resistant bacteria in patients with communityacquired infections. J Infect Chemother. 2003; 9(4): 285-91. http://dx. doi. org/10. 1007/s10156-003-0278-Y PMID: 14691647.
15. Park C, Kim KH, Shin NY, Byun JH, Kwon EY, Lee JW, et al. Genetic diversity of the ftsI gene in β-lactamase-nonproducing ampicillin-resistant and β-lactamase-producing amoxicillin-/clavulanic acid-resistant nasopharyngeal Haemophilus influenzae strains isolated from children in South Korea. Microb Drug Resist. 2013; 19(3): 224-30. http://dx. doi. org/10. 1089/mdr. 2012. 0116 PMID: 23308379.
16. Dabernat H, Delmas C. Epidemiology and evolution of antibiotic resistance of Haemophilus influenzae in children 5 years of age or less in France, 2001-2008: a retrospective database analysis. Eur J Clin Microbiol Infect Dis. 2012; 31(10): 2745-53. http://dx. doi. org/10. 1007/s10096-012-1623-9 PMID: 22538797.
17. Skaare D, Allum AG, Anthonisen IL, Jenkins A, Lia A, Strand L, et al. Mutant ftsI genes in the emergence of penicillin-binding protein-mediated beta-lactam resistance in Haemophilus influenzae in Norway. Clin Microbiol Infect. 2010; 16(8): 1117-24. http://dx. doi. org/10. 1111/j. 1469-0691. 2009. 03052. x PMID: 19737286.
18. Barbosa AR, Giufre M, Cerquetti M, Bajanca-Lavado MP. Polymorphism in ftsI gene and beta-lactam susceptibility in Portuguese Haemophilus influenzae strains: clonal dissemination of beta-lactamase-positive isolates with decreased susceptibility to amoxicillin/clavulanic acid. J Antimicrob Chemother. 2011; 66(4): 788-96. http://dx. doi. org/10. 1093/jac/dkq533 PMID: 21393206.
19. Shuel M, Hoang L, Law DKS, Tsang R. Invasive Haemophilus influenzae in British Columbia: non-Hib and non-typeable strains causing disease in children and adults. Int J Infect Dis. 2011; 15(3): e167-73. http://dx. doi. org/10. 1016/j. ijid. 2010. 10. 005 PMID: 21134777.
20. Kilian M. A taxonomic study of the genus Haemophilus, with the proposal of a new species. J Gen Microbiol. 1976; 93(1): 9-62. http://dx. doi. org/10. 1099/00221287-93-1-9 PMID: 772168.
21. 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): 2382-6. PMID: 7814470.
22. Meats E, Feil EJ, Stringer S, Cody AJ, Goldstein R, Kroll JS, et al. Characterization of encapsulated and noncapsulated Haemophilus influenzae and determination of phylogenetic relationships by multilocus sequence typing. J Clin Microbiol. 2003; 41(4): 1623-36. http://dx. doi. org/10. 1128/JCM. 41. 4. 1623-1636. 2003 PMID: 12682154.
23. Tenover FC, Arbeit RD, Goering RV, Mickelsen PA, Murray BE, Persing DH, et al. Interpreting chromosomal DNA restriction patterns produced by pulsed-field gel electrophoresis: criteria for bacterial strain typing. J Clin Microbiol. 1995; 33(9): 2233-9. PMID: 7494007.
24. Livermore DM, Brown DFJ. Detection of beta-lactamasemediated resistance. J Antimicrob Chemother. 2001; 48(Suppl 1): 59-64. http://dx. doi. org/10. 1093/jac/48. suppl_1. 59 PMID: 11420337.
25. Clinical and Laboratory Standards Institute (CSLI). M07-A9. Methods for dilution antimicrobial susceptibility tests for bacteria that grow aerobically; approved standard-ninth edition. Wayne, PA: CSLI;, 2012.
26. Perez-Vazquez M, Roman F, Aracil B, Canton R, Campos J. Laboratory detection of Haemophilus influenzae with decreased susceptibility to nalidixic acid, ciprofloxacin, levofloxacin, and moxifloxacin due to GyrA and ParC mutations. J Clin Microbiol. 2004; 42(3): 1185-91. http://dx. doi. org/10. 1128/JCM. 42. 3. 1185-1191. 2004 PMID: 15004073.
27. Hekker TA, van der Schee AC, Kempers J, Namavar F, van Alphen L. A nosocomial outbreak of amoxycillin-resistant non-typable Haemophilus influenzae in a respiratory ward. J Hosp Infect. 1991; 19(1): 25-31. http://dx. doi. org/10. 1016/0195-6701(91)90125-R PMID: 1684594.
28. Watanabe H, Hoshino K, Sugita R, Asoh N, Watanabe K, Oishi K, 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(1): 362-5. http://dx. doi. org/10. 1128/JCM. 42. 1. 362-365. 2004 PMID: 14715779.
29. 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(6): 1501-9. http://dx. doi. org/10. 1093/jac/dku022 PMID: 24562614.
30. Kaczmarek FS, Gootz TD, Dib-Hajj F, Shang W, Hallowell S, Cronan M. Genetic and molecular characterization of beta-lactamase-negative ampicillin-resistant Haemophilus influenzae with unusually high resistance to ampicillin. Antimicrob Agents Chemother. 2004; 48(5): 1630-9. http://dx. doi. org/10. 1128/AAC. 48. 5. 1630-1639. 2004 PMID: 15105114.
31. NORM/NORM-VET. Usage of Antimicrobial Agents and Occurrence of Antimicrobial Resistance in Norway. Tromso/Oslo, Norway. NORM/NORM-VET; 2011. Available from: http://www. unn. no/getfile. php/UNN%20INTER/Fagfolk/www. antibiotikaresistens. no/NORM_2012/NORM%20NORM-VET%202011. pdf.
32. Georgiou M, Munoz R, Roman F, Canton R, Gomez-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(7): 1741-4. PMID: 8807076.
33. Perez-Vazquez M, Roman F, Garcia-Cobos S, Campos J. Fluoroquinolone resistance in Haemophilus influenzae is associated with hypermutability. Antimicrob Agents Chemother. 2007; 51(4): 1566-9. http://dx. doi. org/10. 1128/AAC. 01437-06 PMID: 17283196.
34. Pfeifer Y, Meisinger I, Brechtel K, Grobner S. Emergence of a multidrug-resistant Haemophilus influenzae strain causing chronic pneumonia in a patient with common variable immunodeficiency. Microb Drug Resist. 2013; 19(1): 1-5. http://dx. doi. org/10. 1089/mdr. 2012. 0060 PMID: 23095085.
35. Leaves NI, Dimopoulou I, Hayes I, Kerridge S, Falla T, Secka O, et al. Epidemiological studies of large resistance plasmids in Haemophilus. J Antimicrob Chemother. 2000; 45(5): 599-604. http://dx. doi. org/10. 1093/jac/45. 5. 599 PMID: 10797080.
36. Mohd-Zain Z, Turner SL, Cerdeno-Tarraga AM, Lilley AK, Inzana TJ, Duncan AJ, et al. Transferable antibiotic resistance elements in Haemophilus influenzae share a common evolutionary origin with a diverse family of syntenic genomic islands. J Bacteriol. 2004; 186(23): 8114-22. http://dx. doi. org/10. 1128/JB. 186. 23. 8114-8122. 2004 PMID: 15547285.
37. Watson ME Jr, Burns JL, Smith AL. Hypermutable Haemophilus influenzae with mutations in mutS are found in cystic fibrosis sputum. Microbiology. 2004; 150(Pt 9): 2947-58. http://dx. doi. org/10. 1099/mic. 0. 27230-0 PMID: 15347753.
38. 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(10): e25923. http://dx. doi. org/10. 1371/journal. pone. 0025923 PMID: 21998721.