Macrolide and lincosamide resistance of Streptococcus agalactiae in pregnant women in Poland.

Antimicrobial susceptibility patterns Group B Streptococcus Lincosamide resistance Macrolide resistance Serotyping Streptogramin resistance Virulence factors

Journal

Scientific reports
ISSN: 2045-2322
Titre abrégé: Sci Rep
Pays: England
ID NLM: 101563288

Informations de publication

Date de publication:
16 Feb 2024
Historique:
received: 11 11 2022
accepted: 13 02 2024
medline: 17 2 2024
pubmed: 17 2 2024
entrez: 17 2 2024
Statut: epublish

Résumé

Knowing about the antibiotic resistance, serotypes, and virulence-associated genes of Group B Streptococcus for epidemiological and vaccine development is very important. We have determined antimicrobial susceptibility patterns, serotype, and virulence profiles. The antibiotic susceptibility was assessed for a total of 421 Streptococcus agalactiae strains, isolated from pregnant women and neonates. Then, 89 erythromycin and/or clindamycin-resistant strains (82 isolates obtained from pregnant women and seven isolates derived from neonates) were assessed in detail. PCR techniques were used to identify the studied strains, perform serotyping, and assess genes encoding selected virulence factors. Phenotypic and genotypic methods determined the mechanisms of resistance. All tested strains were sensitive to penicillin and levofloxacin. The constitutive MLS

Identifiants

pubmed: 38366099
doi: 10.1038/s41598-024-54521-y
pii: 10.1038/s41598-024-54521-y
doi:

Types de publication

Journal Article

Langues

eng

Sous-ensembles de citation

IM

Pagination

3877

Informations de copyright

© 2024. The Author(s).

Références

Jamrozy, D. et al. Increasing incidence of group B streptococcus neonatal infections in the Netherlands is associated with clonal expansion of CC17 and CC23. Sci. Rep. 10, 9539. https://doi.org/10.1038/s41598-020-66214-3 (2020).
doi: 10.1038/s41598-020-66214-3 pubmed: 32533007 pmcid: 7293262
Lim, S., Rajagopal, S., Jeong, Y. R., Nzegwu, D. & Wright, M. L. Group B Streptococcus and the vaginal microbiome among pregnant women: a systematic review. Peer J. 9, e11437. https://doi.org/10.7717/peerj.11437 (2021).
doi: 10.7717/peerj.11437 pubmed: 34046261 pmcid: 8136278
Maeda, T. et al. Comparison between Invasive and Non-Invasive Streptococcus agalactiae isolates from human adults, Based on virulence gene profiles, capsular genotypes, sequence types, and antimicrobial resistance patterns. Jpn J. Infect. Dis. 74, 316–324 (2021).
doi: 10.7883/yoken.JJID.2020.761 pubmed: 33390429
Bianchi-Jassir, F. et al. Systematic review of Group B Streptococcal capsular types, sequence types and surface proteins as potential vaccine candidates. Vaccine. 38, 6682–6694 (2020).
doi: 10.1016/j.vaccine.2020.08.052 pubmed: 32888741 pmcid: 7526974
Humphries, R. M. Group B Streptococcus dynamics in the United States. Clin. Infect. Dis. 72, 1014–1015 (2021).
doi: 10.1093/cid/ciaa155 pubmed: 32060524
Genovese, C., D’Angeli, F., Di Salvatore, V., Tempera, G. & Nicolosi, D. Streptococcus agalactiae in pregnant women: serotype and antimicrobial susceptibility patterns over five years in Eastern Sicily (Italy). Eur. J. Clin. Microbiol. Infect. Dis. 39, 2387–2396 (2020).
doi: 10.1007/s10096-020-03992-8 pubmed: 32700131 pmcid: 7669783
Kaminska, D. et al. Increasing resistance and changes in distribution of serotypes of Streptococcus agalactiae in Poland. Pathogens. 9, 526 (2020).
doi: 10.3390/pathogens9070526 pubmed: 32610654 pmcid: 7400139
Nanduri, S. A. et al. Epidemiology of invasive early-onset and late-onset group B Streptococcal disease in the United States, 2006 to 2015: Multistate laboratory and population-based surveillance. JAMA Pediatr. 173, 224–233 (2019).
doi: 10.1001/jamapediatrics.2018.4826 pubmed: 30640366 pmcid: 6439883
Takahashi, T., Maeda, T., Lee, S., Lee, D. H. & Kim, S. Clonal distribution of clindamycin-resistant erythromycin-susceptible (CRES) Streptococcus agalactiae in Korea based on whole genome sequences. Ann. Lab. Med. 40, 370–381 (2020).
doi: 10.3343/alm.2020.40.5.370 pubmed: 32311850 pmcid: 7169627
Motallebirad, T. et al. Prevalence, population structure, distribution of serotypes, pilus islands and resistance genes among erythromycin-resistant colonizing and invasive Streptococcus agalactiae isolates recovered from pregnant and non-pregnant women in Isfahan Iran. BMC Microbiol. 21, 139 (2021).
doi: 10.1186/s12866-021-02186-2 pubmed: 33947330 pmcid: 8096152
Hawkins, P. A. et al. Cross-resistance to lincosamides, streptogramins A and pleuromutilins in Streptococcus agalactiae isolates from the USA. J. Antimicrob. Chemother. 72, 1886–1892 (2017).
doi: 10.1093/jac/dkx077 pubmed: 28333320
Center for Disease Control and Prevention. Antibiotic Resistance Threat in the United States, 2019; U.S. Department of Health and Human Services, CDC: Atlanta, GA, USA (2019).
Creti, R., Fabretti, F., Orefici, G. & von Hunolstein, C. Multiplex PCR assay for direct identification of group B streptococcal alpha-protein-like protein genes. J. Clin. Microbiol. 42, 1326–1329 (2004).
doi: 10.1128/JCM.42.3.1326-1329.2004 pubmed: 15004110 pmcid: 356896
Chan, J. M., Gori, A., Nobbs, A. H. & Heyderman, R. S. Streptococcal serine-rich repeat proteins in colonization and disease. Front. Microbiol. 11, 593356 (2020).
doi: 10.3389/fmicb.2020.593356 pubmed: 33193266 pmcid: 7661464
Russell, N.J. et al. GBS Maternal Colonization Investigator Group. Maternal colonization with group B Streptococcus and serotype distribution worldwide: Systematic review and meta-analyses. Clin. Infect. Dis. 65, 100–111 (2017).
Berner, R. Group B streptococcus vaccines: One step further. Lancet Infect. Dis. 21, 158–160 (2021).
doi: 10.1016/S1473-3099(20)30451-5 pubmed: 32891192
Perme, T. et al. Genomic and phenotypic characterisation of invasive neonatal and colonising group B Streptococcus isolates from Slovenia, 2001–2018. BMC Infect. Dis. 20, 958 (2020).
doi: 10.1186/s12879-020-05599-y pubmed: 33327946 pmcid: 7739447
Chaguza, C. et al. Population genomics of Group B Streptococcus reveals the genetics of neonatal disease onset and meningeal invasion. Nat. Commun. 13, 4215. https://doi.org/10.1038/s41467-022-31858-4 (2022).
doi: 10.1038/s41467-022-31858-4 pubmed: 35864107 pmcid: 9304382
Lamy, M. C. et al. Rapid detection of the “highly virulent” group B Streptococcus ST-17 clone. Microbes Infect. 8, 1714–1722 (2006).
doi: 10.1016/j.micinf.2006.02.008 pubmed: 16822689
Creti, R., Imperi, M., Berardi, A., Lindh, E., Alfarone, G., Pataracchia, M. & Recchia, S. The Italian Network On Neonatal And Infant Gbs Infections. Invasive Group B Streptococcal Disease in Neonates and Infants, Italy, Years 2015–2019. Microorganisms. 9, 2579. https://doi.org/10.3390/microorganisms9122579 (2021).
Matani, C., Trezzi, M., Matteini, A., Messeri, D. & Catalani, C. Streptococcus agalactiae: prevalence of antimicrobial resistance in vaginal and rectal swabs in Italian pregnant women. Infez. Med. 24, 217–221 (2016).
pubmed: 27668902
Capanna, F. et al. Antibiotic resistance patterns among group B Streptococcus isolates: implications for antibiotic prophylaxis for early-onset neonatal sepsis. Swiss. Med. Wkly. 143, w13778 (2013).
pubmed: 23572445
Fröhlicher, S. et al. Serotype distribution and antimicrobial susceptibility of group B streptococci in pregnant women: results from a Swiss tertiary centre. Swiss Med. Wkly. 144, w13935 (2014).
pubmed: 24652673
Dogan, B., Schukken, Y. H., Santisteban, C. & Boor, K. J. Distribution of serotypes and antimicrobial resistance genes among Streptococcus agalactiae isolates from bovine and human hosts. J. Clin. Microbiol. 43, 5899–5906 (2005).
doi: 10.1128/JCM.43.12.5899-5906.2005 pubmed: 16333073 pmcid: 1317170
Phares, C. R. et al. Epidemiology of invasive group B streptococcal disease in the United States, 1999–2005. JAMA. 299, 2056–2065 (2008).
doi: 10.1001/jama.299.17.2056 pubmed: 18460666
Wang, P. et al. Serotypes, antibiotic susceptibilities, and multilocus sequence type profiles of Streptococcus agalactiae isolates circulating in Beijing China. PLoS One. 10, e0120035 (2015).
doi: 10.1371/journal.pone.0120035 pubmed: 25781346 pmcid: 4363692
Wang, P. et al. Serotype distribution, antimicrobial resistance, and molecular characterization of invasive group B Streptococcus isolates recovered from Chinese neonates. Int. J. Infect. Dis. 37, 115–118 (2015).
doi: 10.1016/j.ijid.2015.06.019 pubmed: 26141418
Kekic, D. et al. Trends in molecular characteristics and antimicrobial resistance of group B streptococci: A multicenter study in Serbia, 2015–2020. Sci. Rep. 11, 540. https://doi.org/10.1038/s41598-020-79354-3 (2021).
doi: 10.1038/s41598-020-79354-3 pubmed: 33436658 pmcid: 7804007
European Committee on Antimicrobial Susceptibility Testing. Breakpoint Tables for Interpretation of MICs and Zone Diameters Version 11.0, Valid from 1 January 2021. Available online: https://www.eucast.org (accessed on 12 April 2021).
Arana, D., Rojo-Bezares, B., Torres, C. & Alós, J. I. First clinical isolate in Europe of clindamycin-resistant group B Streptococcus mediated by the lnu(B) gene. Rev. Esp. Quimioter. 27, 106–109 (2014).
pubmed: 24940891
Faccone, D. et al. Multiple-clones of Streptococcus agalactiae harbouringlnu B gene. J. Infect. Dev. Ctries. 4, 580–582 (2010).
doi: 10.3855/jidc.941 pubmed: 21045372
Compain, F. et al. Molecular characterization of Streptococcus agalactiae isolates harboring small erm(T)-carrying plasmids. Antimicrob. Agents Chemother. 58, 6928–6930 (2014).
doi: 10.1128/AAC.03855-14 pubmed: 25136004 pmcid: 4249376
De Azavedo, J., McGavin, M., Duncan, C. & Low, D. E. McGeer, APrevelence and mechanisms of macrolide resistance in invasive and noninvasive Group B Streptococcus isolates from Ontario Canada. Antimicrob. Agents Chemother. 45, 3504–3508 (2001).
doi: 10.1128/AAC.45.12.3504-3508.2001 pubmed: 11709331 pmcid: 90860
Santana, F. A. F. et al. Streptococcus agalactiae: Identification methods, antimicrobial susceptibility, and resistance genes in pregnant women. World J. Clin. Cases. 8, 3988–3998 (2020).
doi: 10.12998/wjcc.v8.i18.3988 pubmed: 33024755 pmcid: 7520794
Teatero, S. et al. Clonal Complex 17 Group B Streptococcus strains causing invasive disease in neonates and adults originate from the same genetic pool. Sci. Rep. 6, 20047. https://doi.org/10.1038/srep20047 (2016).
doi: 10.1038/srep20047 pubmed: 26843175 pmcid: 4740736
Campisi, E. et al. Genomic analysis reveals multi-drug resistance clusters in group B Streptococcus CC17 hypervirulent isolates causing neonatal invasive disease in Southern Mainland China. Front. Microbiol. 7, 1265. https://doi.org/10.3389/fmicb.2016.01265 (2016).
doi: 10.3389/fmicb.2016.01265 pubmed: 27574519 pmcid: 4983569
Plainvert, C. et al. Multidrug-resistant hypervirulent group B Streptococcus in neonatal invasive infections, France, 2007–2019. Emerg. Infect. Dis. 26, 2721–2724 (2020).
doi: 10.3201/eid2611.201669 pubmed: 33079049 pmcid: 7588536
Martins, E.R., Pedroso-Roussado, C., Melo-Cristino, J. & Ramirez, M. Portuguese Group for the Study of Streptococcal Infections. Streptococcus agalactiae Causing Neonatal Infections in Portugal (2005–2015): Diversification and Emergence of a CC17/PI-2b Multidrug Resistant Sublineage. Front Microbiol. 8, 499. https://doi.org/10.3389/fmicb.2017.00499 (2017).
Martins, E. R., Nascimento, Ó. D., Marques Costa, A. L., Melo-Cristino, J. & Ramirez, M. Characteristics of Streptococcus agalactiae colonizing nonpregnant adults support the opportunistic nature of invasive infections. Microbiol. Spectr. 10, e0108222. https://doi.org/10.1128/spectrum.01082-22 (2022).
doi: 10.1128/spectrum.01082-22 pubmed: 35604173
Uh, Y., Kim, H. Y., Jang, I. H., Hwang, G. Y. & Yoon, K. J. Correlation of serotypes and genotype of macrolide-resistant Streptococcus agalactiae. Yonsei Med. J. 46, 480–483 (2005).
doi: 10.3349/ymj.2005.46.4.480 pubmed: 16127771 pmcid: 2815831
Gherardi, G. et al. Molecular epidemiology and distribution of serotypes, surface proteins and antibiotic resistance among group B streptococci in Italy. J. Clin. Microbiol. 45, 2909–2916 (2007).
doi: 10.1128/JCM.00999-07 pubmed: 17634303 pmcid: 2045288
Brzychczy-Włoch, M. et al. Genetic characterization and diversity of Streptococcus agalactiae isolates with macrolide resistance. J. Med. Microbiol. 59, 780–786 (2010).
doi: 10.1099/jmm.0.018176-0 pubmed: 20339021
Bobadilla, F. J., Novosak, M. G., Cortese, I. J., Delgado, O. D. & Laczeski, M. E. Prevalence, serotypes and virulence genes of Streptococcus agalactiae isolated from pregnant women with 35–37 weeks of gestation. BMC Infect. Dis. 21, 73 (2021).
doi: 10.1186/s12879-020-05603-5 pubmed: 33446117 pmcid: 7807883
Eskandarian, N. et al. Antimicrobial susceptibility profiles, serotype distribution and virulence determinants among invasive, non-invasive and colonizing Streptococcus agalactiae (group B streptococcus) from Malaysian patients. Eur. J. Clin. Microbiol. Infect. Dis. 34, 579–584 (2014).
doi: 10.1007/s10096-014-2265-x pubmed: 25359580 pmcid: 4356882
Beigverdi, R. et al. Virulence factors, antimicrobial susceptibility and molecular characterization of Streptococcus agalactiae isolated from pregnant women. Acta Microbiol. Immunol. Hung. 61, 425–434 (2014).
doi: 10.1556/amicr.61.2014.4.4 pubmed: 25496971
Rosenau, A. et al. Evaluation of the ability of Streptococcus agalactiae strains isolated from genital and neonatal specimens to bind to human fibrinogen and correlation with characteristics of the fbsA and fbsB genes. Infect. Immun. 75, 1310–1317 (2007).
doi: 10.1128/IAI.00996-06 pubmed: 17158903
Furfaro, L. L., Chang, B. J., Kahler, C. M. & Payne, M. S. Genomic characterisation of perinatal Western Australian Streptococcus agalactiae isolates. PLoS One. 14, e0223256. https://doi.org/10.1371/journal.pone.0223256 (2019).
doi: 10.1371/journal.pone.0223256 pubmed: 31577825 pmcid: 6774530
Verani, J.R., McGee, L., & Schrag, S.J. Prevention of Perinatal Group B Streptococcal Disease. Revised Guidelines from CDC, 2010. MMWR Recomm Rep. 59, No. RR-10 (2010).
Heczko, P. B. et al. Rekomendations for the detection of group B streptococcus (GBS) carriage in pregnant women and for prevention of neonatal infections caused by this pathogen. Zakazenia. 2, 87–96 (2008).
Kong, F., Ma, L. & Gilbert, G. L. Simultaneous detection and serotype identification of Streptococcus agalactiae using multiplex PCR and reverse line blot hybridization. J. Med. Microbiol. 54, 1133–1138 (2005).
doi: 10.1099/jmm.0.46244-0 pubmed: 16278425

Auteurs

Dorota Kamińska (D)

Chair and Department of Genetics and Pharmaceutical Microbiology, Collegium Pharmaceuticum, Poznan University of Medical Sciences, Rokietnicka 3, 60-806, Poznan, Poland.

Magdalena Ratajczak (M)

Chair and Department of Genetics and Pharmaceutical Microbiology, Collegium Pharmaceuticum, Poznan University of Medical Sciences, Rokietnicka 3, 60-806, Poznan, Poland.

Dorota M Nowak-Malczewska (DM)

Chair and Department of Genetics and Pharmaceutical Microbiology, Collegium Pharmaceuticum, Poznan University of Medical Sciences, Rokietnicka 3, 60-806, Poznan, Poland.

Justyna A Karolak (JA)

Chair and Department of Genetics and Pharmaceutical Microbiology, Collegium Pharmaceuticum, Poznan University of Medical Sciences, Rokietnicka 3, 60-806, Poznan, Poland.

Marek Kwaśniewski (M)

Chair and Department of Genetics and Pharmaceutical Microbiology, Collegium Pharmaceuticum, Poznan University of Medical Sciences, Rokietnicka 3, 60-806, Poznan, Poland.

Anna Szumala-Kakol (A)

Unit of Microbiology, Gynecological and Obstetric Clinical Hospital, Poznan University of Medical Sciences, Polna 33, 60-535, Poznan, Poland.

Jolanta Dlugaszewska (J)

Chair and Department of Genetics and Pharmaceutical Microbiology, Collegium Pharmaceuticum, Poznan University of Medical Sciences, Rokietnicka 3, 60-806, Poznan, Poland.

Marzena Gajecka (M)

Chair and Department of Genetics and Pharmaceutical Microbiology, Collegium Pharmaceuticum, Poznan University of Medical Sciences, Rokietnicka 3, 60-806, Poznan, Poland. gamar@man.poznan.pl.
Institute of Human Genetics, Polish Academy of Sciences, Strzeszynska 32, 60-479, Poznan, Poland. gamar@man.poznan.pl.

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