Antibiotic susceptibility of Cronobacter spp. isolated from clinical samples

• Autorzy: Holy O. , Alsonosi A. , Hochel I. , Roderova M. , Zatloukalova S. , Mlynarcik P. , Kolar M. , Petrzelova J. , Alazraq A. , Chmelar D. , Forsythe S.
• Języki publikacji: EN

Abstrakty

EN

Cronobacter spp. have been recognized as causative agents of various severe infections in pre-term or full-term infants as well as elderly adults suffering from serious underlying disease or malignancy. A surveillance study was designed to identify antibiotic resistance among clinical Cronobacter spp. strains, which were isolated from patients of two hospitals between May 2007 and August 2013. Altogether, 52 Cronobacter spp. isolates were analyzed. Although MALDI-TOF mass spectrometry recognized all Cronobacter sakazakii and Crono­bacter malonaticus strains, it could not identify Cronobacter muytjensii strain. Nevertheless, all strains were identified as Cronobacter spp. using multilocus sequence typing (MLST). Strains were tested against 17 types of antibiotics, using the standard microdilution method according to the 2018 European Committee on Antimicrobial Susceptibility Testing criteria. Three Cronobacter species were identified as C. sakazakii (n = 33), C. malonaticus (n = 18), and C. muytjensii (n = 1); all isolates were susceptible to all tested antibiotics. All strains were PCR-negative for blaTEM, blaSHV, and blaCTX-M β-lactamase genes, as well. Even though the results of this study showed that Cronobacter spp. isolates were pan-susceptible, continued antibiotic resistance surveillance is warranted.

• Wydawca: -
• Czasopismo: Polish Journal of Microbiology
• Rocznik: 2019
• Tom: 68
• Numer: 1
• Opis fizyczny: p.5-14,ref.

Twórcy

autor

Holy O.

• Department of Public Health, Faculty of Medicine and Dentistry, Palacky University Olomouc, Olomouc, Czech Republic

autor

Alsonosi A.

• Microbiology Department, Faculty of Biomedical Sciences, Sabha University, Sabha, Libya

autor

Hochel I.

• Department of Biochemistry and Microbiology, University of Chemistry and Technology, Prague, Czech Republic

autor

Roderova M.

• Department of Microbiology, Faculty of Medicine and Dentistry, Palacky University Olomouc, Olomouc, Czech Republic

autor

Zatloukalova S.

• Department of Public Health, Faculty of Medicine and Dentistry, Palacky University Olomouc, Olomouc, Czech Republic

autor

Mlynarcik P.

• Department of Microbiology, Faculty of Medicine and Dentistry, Palacky University Olomouc, Olomouc, Czech Republic

autor

Kolar M.

• Department of Microbiology, Faculty of Medicine and Dentistry, Palacky University Olomouc, Olomouc, Czech Republic

autor

Petrzelova J.

• Department of Microbiology, Faculty of Medicine and Dentistry, Palacky University Olomouc, Olomouc, Czech Republic

autor

Alazraq A.

• Department of Pharmacology, Faculty of Pharmacy, Sabha University, Sabha, Libya

autor

Chmelar D.

• Department of Biomedical Sciences, Institute of Microbiology and Immunology, Faculty of Medicine, University of Ostrava, Ostrava, Czech Republic

autor

Forsythe S.

• foodmicrobe.com, Adams Hill, Keyworth, Nottinghamshire, U.K.

Bibliografia

• Alsonosi A, Hariri S, Kajsík M, Oriešková M, Hanulík V, Röderová M, Petrželová J, Kollárová H, Drahovská H, For-sythe S, et al. The speciation and genotyping of Cronobacter iso-lates from hospitalised patients. Eur J Clin Microbiol Infect Dis. 2015;34(10):1979–1988. doi:10.1007/s10096-015-2440-8 Medline
• Alsonosi AM, Holy O, Forsythe SJ. Characterization of the patho-genicity of clinical Cronobacter malonaticus strains based on the tissue culture investigations. Antonie van Leeuwenhoek. 2018. doi:10.1007/s10482-018-1178-6 Medline
• Arlet G, Brami G, Décrè D, Flippo A, Gaillot O, Lagrange PH, Philippon A. Molecular characterisation by PCR-restriction frag-ment length polymorphism of TEM beta-lactamases. FEMS Micro-biol Lett. 1995;134(2–3):203–208. Medline
• Asato VC, Vilches VE, Pineda MG, Casanueva E, Cane A, Moroni MP, Brengi SP, Pichel MG. First clinical isolates of Crono­bacter spp. (Enterobacter sakazakii) in Argentina: characteriza-tion and subtyping by pulsed-field gel electrophoresis. Rev Argent Microbiol. 2013;45(3):160–164. doi:10.1016/S0325-7541(13)70018-X Medline
• Baldwin A, Loughlin M, Caubilla-Barron J, Kucerova E, Man-ning G, Dowson C, Forsythe S. Multilocus sequence typing of Cronobacter sakazakii and Cronobacter malonaticus reveals stable clonal structures with clinical significance which do not correlate with biotypes. BMC Microbiol. 2009;9(1):223. doi:10.1186/1471-2180-9-223 Medline
• Barbuddhe SB, Maier T, Schwarz G, Kostrzewa M, Hof H, Domann E, Chakraborty T, Hain T. Rapid identification and typing of Listeria species by matrix-assisted laser desorption ioni-zation-time of flight mass spectrometry. Appl Environ Microbiol. 2008;74(17):5402–5407. doi:10.1128/AEM.02689-07 Medline
• Bar-Oz B, Preminger A, Peleg O, Block C, Arad I.Enterobac­ter sakazakii infection in the newborn. Acta Paediatr. 2001; 90(3):356–358. doi:10.1111/j.1651-2227.2001.tb00319.x Medline
• Biering G, Karlsson S, Clark NC, Jónsdóttir KE, Lúdvígsson P, Steingrímsson O. Three cases of neonatal meningitis caused by Enterobacter sakazakii in powdered milk. J Clin Microbiol. 1989; 27(9):2054–2056. Medline
• Block C, Peleg O, Minster N, Bar-Oz B, Simhon A, Arad I,Shapiro M. Cluster of neonatal infections in Jerusalem due to unusual biochemical variant of Enterobacter sakazakii. Eur J Clin Microbiol Infect Dis. 2002;21(8):613–616. doi:10.1007/s10096-002-0774-5 Medline
• Bowen AB, Braden CR. Invasive Enterobacter sakazakii disease in infants. Emerg Infect Dis. 2006;12(8):1185–1189. doi:10.3201/eid1208.051509 Medline
• Brandão MLL, Umeda NS, Jackson E, Forsythe SJ, de Filippis I.Isolation, molecular and phenotypic characterization, and antibiotic susceptibility of Cronobacter spp. from Brazilian retail foods. Food Microbiol. 2017;63:129–138. doi:10.1016/j.fm.2016.11.011 Medline
• Caubilla-Barron J, Hurrell E, Townsend S, Cheetham P, Loc-Car-rillo C, Fayet O, Prère MF, Forsythe SJ. Genotypic and phenotypic analysis of Enterobacter sakazakii strains from an outbreak resulting in fatalities in a neonatal intensive care unit in France. J Clin Micro-biol. 2007;45(12):3979–3985. doi:10.1128/JCM.01075-07 Medline
• Chanawong A, M’Zali FH, Heritage J, Lulitanond A, Hawkey PM.Characterisation of extended-spectrum beta-lactamases of theSHV family using a combination of PCR-single strand conforma-tional polymorphism (PCR-SSCP) and PCR-restriction fragmentlength polymorphism (PCR-RFLP). FEMS Microbiol Lett. 2000;184(1):85–89. Medline
• Cui JH, Du XL, Wei RJ, Zhou HJ, Li W, Forsythe S, Cui ZG. Multi-locus sequence typing analysis of Cronobacter spp. isolated from China. Arch Microbiol. 2015;197(5):665–672. doi:10.1007/s00203-015-1097-0 Medline
• Davies AP, Reid M, Hadfield SJ, Johnston S, Mikhail J, Harris LG, Jenkinson HF, Berry N, Lewis AM, El-Bouri K, et al. Identifica-tion of clinical isolates of α-hemolytic streptococci by 16S rRNA gene sequencing, matrix-assisted laser desorption ionization-time of flight mass spectrometry using MALDI Biotyper, and conventional phenotypic methods: a comparison. J Clin Microbiol. 2012;50(12): 4087–4090. doi:10.1128/JCM.02387-12 Medline
• Dennison SK, Morris J. Multiresistant Enterobacter sakazakii wound infection in an adult. Infect Med. 2002;19(11):533–535.
• EUCAST. Breakpoint tables for interpretation of MICs and zone diameters. Version 8.0. The European Committee on Antimicrobial Susceptibility Testing. 2018.
• Farmer JJ 3rd, Asbury MA, Hickman FW, Brenner DJ. The Entero­bacteriacae Study Group. Enterobacter sakazakii: a new species of “Enterobacteriaceae” isolated from clinical specimens. Int J Syst Bac-teriol. 1980;30(3):569–584. doi:10.1099/00207713-30-3-569
• Forsythe SJ. Updates on the Cronobacter Genus. Annu Rev FoodSci Technol. 2018;9(1):23–44. doi:10.1146/annurev-food-030117- 012246 Medline
• Friedemann M. Epidemiology of invasive neonatal Cronobacter(Enterobacter sakazakii) infections. Eur J Clin Microbiol Infect Dis. 2009;28(11):1297–1304. doi:10.1007/s10096-009-0779-4 Medline
• Hariri S, Joseph S, Forsythe SJ.Cronobacter sakazakii ST4 strains and neonatal meningitis, United States. Emerg Infect Dis. 2013; 19(1):175–177. doi:10.3201/eid1901.120649 Medline
• Healy B, Cooney S, O’Brien S, Iversen C, Whyte P, Nally J, Calla-nan JJ, Fanning S.Cronobacter (Enterobacter sakazakii): an oppor-tunistic foodborne pathogen. Foodborne Pathog Dis. 2010;7(4):339–350. doi:10.1089/fpd.2009.0379 Medline
• Hochel I, Růžičková H, Krásný L, Demnerová K. Occurrence of Cronobacter spp. in retail foods. J Appl Microbiol. 2012;112(6):1257–1265. doi:10.1111/j.1365-2672.2012.05292.x Medline
• Holý O, Forsythe S.Cronobacter spp. as emerging causes of healthcare-associated infection. J Hosp Infect. 2014;86(3):169–177. doi:10.1016/j.jhin.2013.09.011 Medline
• Holý O, Matousková I, Holý V, Koukalová D, Chmelar D. Isolation of Cronobacter spp. (formerly Enterobacter sakazakii) from nostrils of healthy stable horse – short communication. Epidemiol Mikrobiol Imunol. 2011;60(4):167–169. Medline
• Holý O, Matoušková I, Raida L. [The incidence of gram-negative bacteria in the environment of the Transplant Unit, Department of Hemato-oncology, University Hospital - Olomouc]. (in Czech). Epidemiol Mikrobiol Imunol. 2012;61(4):103–109. Medline
• Holý O, Petrželová J, Hanulík V, Chromá M, Matoušková I, Forsythe SJ. Epidemiology of Cronobacter spp. isolates from patients admitted to the Olomouc University Hospital (Czech Republic). Epidemiol Mikrobiol Imunol. 2014;63(1):69–72. Medline
• Iversen C, Lehner A, Mullane N, Bidlas E, Cleenwerck I, Marugg J, Fanning S, Stephan R, Joosten H. The taxonomy of Enterobacter sakazakii: proposal of a new genus Cronobacter gen. nov. and descriptions of Cronobacter sakazakii comb. nov. Cronobacter saka­zakii subsp. sakazakii, comb. nov., Cronobacter sakazakii subsp. mal­onaticus subsp. nov., Cronobacter turicensis sp. nov., Cronobacter muytjensii sp. nov., Cronobacter dublinensis sp. nov. and Cronobactergenomospecies 1. BMC Evol Biol. 2007;7(1):64. doi:10.1186/1471-2148-7-64 Medline
• Iversen C, Mullane N, McCardell B, Tall BD, Lehner A, Fanning S, Stephan R, Joosten H.Cronobacter gen. nov., a new genus to accom-modate the biogroups of Enterobacter sakazakii, and proposal of Cronobacter sakazakii gen. nov., comb. nov., Cronobacter malonati­cus sp. nov., Cronobacter turicensis sp. nov., Cronobacter muytjensiisp. nov., Cronobacter dublinensis sp. nov., Cronobacter genomo-species 1, and of three subspecies, Cronobacterdublinensis subsp. dublinensis subsp. nov., Cronobacterdublinensis subsp. lausannen­sis subsp. nov. and Cronobacterdublinensis subsp. lactaridi subsp. nov. Int J Syst Evol Microbiol. 2008;58(6):1442–1447. doi:10.1099/ijs.0.65577-0 Medline
• Joseph S, Cetinkaya E, Drahovska H, Levican A, Figueras MJ, Forsythe SJ.Cronobacter condimenti sp. nov., isolated from spiced meat, and Cronobacteruniversalis sp. nov., a species designation for Cronobacter sp. genomospecies 1, recovered from a leg infec-tion, water and food ingredients. Int J Syst Evol Microbiol. 2012;62(Pt 6):1277–1283. doi:10.1099/ijs.0.032292-0 Medline
• Joseph S, Forsythe SJ. Predominance of Cronobactersakaza­kii sequence type 4 in neonatal infections. Emerg Infect Dis. 2011;17(9):1713–1715. doi:10.3201/eid1709.110260 Medline
• Kadlicekova V, Kajsik M, Soltys K, Szemes T, Slobodnikova L, Janosikova L, Hubenakova Z, Ogrodzki P, Forsythe S, Turna J, et al.Characterisation of Cronobacter strains isolated from hospitalised adult patients. Antonie van Leeuwenhoek. 2018;111(7):1073–1085.doi:10.1007/s10482-017-1008-2 Medline
• Kucerova E, Clifton SW, Xia XQ, Long F, Porwollik S, Fulton L, Fronick C, Minx P, Kyung K, Warren W, et al. Genome sequence of Cronobactersakazakii BAA-894 and comparative genomic hybridization analysis with other Cronobacter species. PLoS One. 2010;5(3):e9556. doi:10.1371/journal.pone.0009556 Medline
• Kuhns M, Zautner AE, Rabsch W, Zimmermann O, Weig M, Bader O, Groß U. Rapid discrimination of Salmonellaentericaserovar Ty phi from other serovars by MALDI-TOF mass spectrome-try. PLoS One. 2012;7(6):e40004. doi:10.1371/journal.pone.0040004 Medline
• Lai KK.Enterobactersakazakii infections among neonates, infants, children, and adults. Case reports and a review of the literature. Medicine. 2001;80(2):113–122. doi:10.1097/00005792-200103000-00004 Medline
• Matoušková I, Holý O. [Bacterial contamination of the indoor air in a transplant unit]. (in Czech). Epidemiol Mikrobiol Imunol. 2013;62(4):153–159. Medline
• Matoušková I, Holy O. Monitoring of the environment at the trans-plant unit-hemato-oncology clinic. Int J Environ Res Public Health. 2014;11(9):9480–9490. doi:10.3390/ijerph110909480 Medline
• Matoušková I, Raida L, Holý O. [The incidence of nonfermenta-tive gram-negative bacilli in the environment of the transplant unit, department of hemato-oncology, university hospital Olomouc]. (in Czech). Epidemiol Mikrobiol Imunol. 2012;61(4):110–115. Medline
• Mellmann A, Cloud J, Maier T, Keckevoet U, Ramminger I, Iwen P, Dunn J, Hall G, Wilson D, LaSala P, et al. Evaluation of matrix-assisted laser desorption ionization-time-of-flight mass spectrometry in comparison to 16S rRNA gene sequencing for species identification of nonfermenting bacteria. J Clin Microbiol. 2008;46(6):1946–1954. doi:10.1128/JCM.00157-08 Medline
• Muytjens HL, van der Ros-van de Repe J. Comparative in vitro sus-ceptibilities of eight Enterobacter species, with special reference to Enterobactersakazakii. Antimicrob Agents Chemother. 1986;29(2):367–370. doi:10.1128/AAC.29.2.367 Medline
• Muytjens HL, Zanen HC, Sonderkamp HJ, Kollée LA, Wachs-muth IK, Farmer JJ 3rd. Analysis of eight cases of neonatal men-ingitis and sepsis due to Enterobactersakazakii. J Clin Microbiol. 1983;18(1):115–120. Medline
• Pagani L, Dell’Amico E, Migliavacca R, D’Andrea MM, Giaco-bone E, Amicosante G, Romero E, Rossolini GM. Multiple CTX-M-type extended-spectrum beta-lactamases in nosocomial isolates of Enterobacteriaceae from a hospital in northern Italy. J Clin Micro-biol. 2003;41(9):4264–4269. doi:10.1128/JCM.41.9.4264-4269.2003 Medline
• Pan Z, Cui J, Lyu G, Du X, Qin L, Guo Y, Xu B, Li W, Cui Z, Zhao C. Isolation and molecular typing of Cronobacter spp. in com-mercial powdered infant formula and follow-up formula. Foodborne Pathog Dis. 2014;11(6):456–461. doi:10.1089/fpd.2013.1691 Medline
• Pitout JD, Moland ES, Sanders CC, Thomson KS, Fitzsim-mons SR. Beta-lactamases and detection of beta-lactam resistance in Enterobacter spp. Antimicrob Agents Chemother. 1997;41(1):35–39. doi:10.1128/AAC.41.1.35 Medline
• Sauer S, Freiwald A, Maier T, Kube M, Reinhardt R, Kostrzewa M, Geider K. Classification and identification of bacteria by mass spec-trometry and computational analysis. PLoS One. 2008;3(7):e2843. doi:10.1371/journal.pone.0002843 Medline
• Schulthess B, Bloemberg GV, Zbinden A, Mouttet F, Zbinden R, Böttger EC, Hombach M. Evaluation of the Bruker MALDI Bio-typer for identification of fastidious Gram-negative rods. J Clin Microbiol. 2016;54(3):543–548. doi:10.1128/JCM.03107-15 Medline
• See KC, Than HA, Tang T.Enterobacter sakazakii bacteraemia with multiple splenic abscesses in a 75-year-old woman: a case report. Age Ageing. 2007;36(5):595–596. doi:10.1093/ageing/afm092 Medline
• Shi C, Song K, Zhang X, Sun Y, Sui Y, Chen Y, Jia Z, Sun H, Sun Z, Xia X. Antimicrobial activity and possible mechanism of action of citral against Cronobactersakazakii. PLoS One. 2016;11(7):e0159006. doi:10.1371/journal.pone.0159006 Medline
• Stephan R, Grim CJ, Gopinath GR, Mammel MK, Sathyamoor-thy V, Trach LH, Chase HR, Fanning S, Tall BD. Re-examination of the taxonomic status of Enterobacterhelveticus, Enterobacter pulverisand Enterobacter turicensis as members of the genus Cronobacterand their reclassification in the genera Franconibacter gen. nov. and Siccibacter gen. nov. as Franconibacterhelveticus comb. nov., Fran­conibacterpulveris comb. nov. and Siccibacter turicensis comb. nov., respectively. Int J Syst Evol Microbiol. 2014;64(Pt10):3402–3410. doi:10.1099/ijs.0.059832-0 Medline
• Stock I, Wiedemann B. Natural antibiotic susceptibility of Entero­bacter amnigenus, Enterobacter cancerogenus, Enterobacter ger­goviae and Enterobacter sakazakii strains. Clin Microbiol Infect. 2002;8(9):564–578. doi:10.1046/j.1469-0691.2002.00413.x Medline
• Terragno R, Salve A, Pichel M, Epszteyn S, Brengi S, Binsztein N.Characterization and subtyping of Cronobacter spp. from imported powdered infant formulae in Argentina. Int J Food Microbiol. 2009;136(2):193–197. doi:10.1016/j.ijfoodmicro.2009.10.013 Medline
• Vojkovska H, Karpiskova R, Orieskova M, Drahovska H. Charac-terization of Cronobacter spp. isolated from food of plant origin and environmental samples collected from farms and from supermar-kets in the Czech Republic. Int J Food Microbiol. 2016;217:130–136. doi:10.1016/j.ijfoodmicro.2015.10.017 Medline
• Willis J, Robinson J.Enterobacter sakazakii meningitis in neonates. Pediatr Infect Dis J. 1988;7(3):196–199.doi:10.1097/00006454-198803000-00012 Medline

Identyfikatory

DOI

10.21307/pjm-2019-001