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Streptococcus agalactiae strains isolated from cancer patients in Rio de Janeiro, Brazil

  • Clinical Microbiology - Short Communication
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Abstract

Streptococcus agalactiae is a recognized pathogen associated with infections in neonates, elderly, and immunocompromised adults, particularly those with cancer. In the present investigation, clinical-epidemiological features, multidrug resistance profiles, and virulence genes of S. agalactiae strains isolated from cancer patients were investigated. S. agalactiae capsular distribution assays demonstrated that Ia (43.6%) and V (23.6%) types were predominantly detected among 55 clinical isolates tested; only one strain (GBS1428) was capsular type III/ST-17. The fbsB and hylB genes were detected in all isolates, while the iag, lmb, and fbsA genes were detected in 94.5%, 91%, and 91% of oncological isolates, respectively. The combination of PI-1 and PI-2a was the most common (60%) among S. agalactiae strains isolated from oncologic patients. S. agalactiae strains were resistant to tetracycline (85.5%), erythromycin (9%), and clindamycin (5.5%). Norfloxacin non-susceptible was detected in 7.3% of S. agalactiae strains. Our findings reinforce the need for S. agalactiae control measures in Brazil, including cancer patients.

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References

  1. Shabayek S, Spellerberg B (2018) Group B Streptococcal colonization, molecular characteristics, and epidemiology. Front Microbiol 9:437. https://doi.org/10.3389/fmicb.2018.00437

    Article  PubMed  PubMed Central  Google Scholar 

  2. Crespo-Ortiz MP, Castañeda-Ramirez CR, Recalde-Bolaños M, Vélez-Londoño JD (2014) Emerging trends in invasive and non invasive isolates of Streptococcus agalactiae in a Latin American hospital: a 17-year study. BMC Infect Dis 14:428–439. https://doi.org/10.1186/1471-2334-14-428

    Article  PubMed Central  Google Scholar 

  3. Pimentel BAS, Martins CAS, Mendonça JC, Miranda PSD, Sanches GF, Mattos-Guaraldi AL, Nagao PE (2016) Streptococcus agalactiae infection in cancer patient: a five-year study. Eur J. Clin Microbiol Infect Dis 35(6):927–933. https://doi.org/10.1007/s10096-016-2617-9

    Article  CAS  PubMed  Google Scholar 

  4. Pietrocola G, Arciola CR, Rindi S, Montanaro L (2018) Speziale P (2018) Streptococcus agalactiae Non-pilus, cell wall-anchored proteins: involvement in colonization and pathogenesis and potential as vaccine candidates. Front Immunol 9:602. https://doi.org/10.3389/fimmu.2018.00602

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  5. Burcham LR, Spencer BL, Keeler LR, Donna L, Runft DL, Kathryn AP, Melody NN, Kelly SD (2019) Determinants of Group B streptococcal virulence potential amongst vaginal clinical isolates from pregnant women. PLoS One 14:e0226699. https://doi.org/10.1371/journal.pone.0226699

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  6. Madrid L, Seale AC, Kohli-Lynch M et al (2017) Infant GBS disease investigator group. Infant group B Streptococcal disease incidence and serotypes worldwide: systematic review and meta-analyses. Clin Infect Dis 65(suppl-2):S160–S172. https://doi.org/10.1093/cid/cix656

    Article  PubMed  PubMed Central  Google Scholar 

  7. Kao Y, Tsai MH, Lai MY, Chu SM, Huang HR, Chiang MC, Fu RH, Lu JJ, Hsu JF (2019) Emerging serotype III sequence type 17 group B streptococcus invasive infection in infants: the clinical characteristics and impacts on outcomes. BMC Infect Dis 19:538. https://doi.org/10.1186/s12879-019-4177-y

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  8. Vuillemin X, Hays C, Plainvert C, Dmytruk N, Louis M, Touak G, Saint-Pierre B, Adoux L, Letourneur F, Frigo A, Poyart C, Tazi A (2020) Invasive group B Streptococcus infections in non-pregnant adults: a retrospective study, France, 2007-2019. Clin Microbiol Infect 29:S1198-743X(20)30590-5. https://doi.org/10.1016/j.cmi.2020.09.037

  9. Tazi A, Disson O, Bellais S, Bouaboud A, Dmytruk N, Dramsi S, Mistou MY, Khun H, Mechler C, Tardieux I, Trieu-Cuot P, Lecuit M, Poyart C (2010) The surface protein HvgA mediates group B streptococcus hypervirulence and meningeal tropism in neonates. J Exp Med 207:2313–2322. https://doi.org/10.1084/jem.20092594

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  10. Doran KS, Engelson EJ, Khosravi A, Maisey HC, Fedtke I, Equils O, Michelsen KS, Arditi M, Peschel A, Nizet V (2005) Blood-brain barrier invasion by Group B Streptococcus depends upon proper cell-surface anchoring of lipoteichoic acid. J Clin Invest 115:2499–2507. https://doi.org/10.1172/JCI23829

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  11. Centers for Disease Control and Prevention – CDC (2020) Guidelines for the Detection and Identification of Group B Streptococcus. https://www.cdc.gov/groupbstrep/. Accessed 24 Oct 2020

  12. Raabe VN, Shane AL (2019) Group B Streptococcus (Streptococcus agalactiae). Microbiol spect 7. https://doi.org/10.1128/microbiolspec.GPP3-0007-2018. https://doi.org/10.1128/microbiolspec.GPP3-0007-2018

  13. Gizachew M, Tiruneh M, Moges F, Tessema B (2019) Streptococcus agalactiae maternal colonization, antibiotic resistance and serotype profiles in Africa: a meta-analysis. Ann Clin Microbiol Antimicrob 18:14. https://doi.org/10.1186/s12941-019-0313-1

    Article  PubMed  PubMed Central  Google Scholar 

  14. Nanduri SA, Petit S, Smelser C, Apostol M, Alden NB, Harrison LH, Lynfield R, Vagnone PS, Burzlaff K, Spina NL, Dufort EM, Schaffner W, Thomas AR, Farley MM, Jain JH, Pondo T, McGee L, Beall BW, Schrag SJ (2019) 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. https://doi.org/10.1001/jamapediatrics.2018.4826

    Article  PubMed  PubMed Central  Google Scholar 

  15. Jalalifar S, Havaei SA, Motallebirad T, Moghim S, Fazeli H, Esfahani BN (2019) Determination of surface proteins profile, capsular genotyping, and antibiotic susceptibility patterns of group B Streptococcus isolated from urinary tract infection of Iranian patients. BMC Res Notes 12:437. https://doi.org/10.1186/s13104-019-4428-4

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  16. Cometto MA, Gasparotto AM, Navarro M, Rocchi M, Monterisi A, Soliani MI, Arce Romero S, Ocaña Carrizo AV (2018) Streptococcus agalactiae in non-pregnant adults. Analysis of 10 years in a University Hospital. Rev Fac Cien Med Univ Nac Cordoba 75:255–260. https://doi.org/10.31053/1853.0605.v75.n4.20569

    Article  PubMed  Google Scholar 

  17. Poyart C, Tazi A, Réglier-Poupet H, Billoët A, Tavares N, Raymond J, Trieu-Cuot P (2007) Multiplex PCR assay for rapid and accurate capsular typing of group B streptococci. J Clin Microbiol. 45(6):1985–1988. https://doi.org/10.1128/JCM.00159-07

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  18. Kayansamruaj P, Pirarat N, Katagiri T, Hirono I, Rodkhum C (2014) Molecular characterization and virulence gene profiling of pathogenic Streptococcus agalactiae populations from tilapia (Oreochromis sp.) farms in Thailand. J Vet Diagn Invest. 26(4):488–495. https://doi.org/10.1177/1040638714534237

    Article  CAS  PubMed  Google Scholar 

  19. Li L, Wang R, Huang Y, Huang T, Luo F, Huang W, Yang X, Lei A, Chen M, Gan X (2018) High incidence of pathogenic Streptococcus agalactiae ST485 strain in pregnant/puerperal women and isolation of hypervirulent human CC67 strain. Front Microbiol 9:50. https://doi.org/10.3389/fmicb.2018.00050

    Article  PubMed  PubMed Central  Google Scholar 

  20. CLSI (2018) Performance Standards for Antimicrobial Susceptibility Testing CLSI supplement M100-S28. Wayne, PA. Clin Lab Stand Instit 28:1–296

    Google Scholar 

  21. Magiorakos AP, Srinivasan A, Carey RB, Carmeli Y, Falagas ME, Giske CG, Harbarth S, Hindler JF, Kahlmeter G, Olsson-Liljequist B, Paterson DL, Rice LB, Stelling J, Struelens MJ, Vatopoulos A, Weber JT, Monnet DL (2012) Multidrug-resistant, extensively drug-resistant and pandrug-resistant bacteria: an international expert proposal for interim standard definitions for acquired resistance. Clin Microbiol and Infect Dis 18:268–281. https://doi.org/10.1111/j.1469-0691.2011.03570.x

    Article  CAS  Google Scholar 

  22. Miranda PSD, Lannes-Costa PS, Pimentel BAS, Silva LG, Ferreira-Carvalho BT, Menezes GC, Mattos-Guaraldi AL, Hirata RJ, Mota RA, Nagao PE (2018) Biofilm formation on different pH condition by Streptococcus agalactiae isolated from bovine mastitic milk. Lett Appl Microbiol 67(3):235–243. https://doi.org/10.1111/lam.13015

    Article  CAS  PubMed  Google Scholar 

  23. Furfaro LL, Nathan EA, Chang BJ, Payne MS (2019) Group B streptococcus prevalence, serotype distribution and colonization dynamics in Western Australian pregnant women. J Med Microbiol 68:728–740. https://doi.org/10.1099/jmm.0.000980

    Article  CAS  PubMed  Google Scholar 

  24. Russell NJ, Seale AC, O’Driscoll M et al (2017) GBS maternal colonization investigator group. Maternal colonization with Group B Streptococcus and serotype distribution worldwide: systematic review and meta-analyses. Clin Infect Dis 65(suppl_2):S100–S111. https://doi.org/10.1093/cid/cix658

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  25. Gori A, Harrison OB, Mlia E et al (2020) Pan-GWAS of Streptococcus agalactiae highlights lineage-specific genes associated with virulence and niche adaptation. mBio 11:e00728–e00720. https://doi.org/10.1128/mBio.00728-20

    Article  PubMed  PubMed Central  Google Scholar 

  26. Dutra VG, Alves VM, Olendzki AN, Dias CA, de Bastos AF, Santos GO et al (2014) Streptococcus agalactiae in Brazil: serotype distribution, virulence determinants and antimicrobial susceptibility. BMC Infect Dis. 14:323–332. https://doi.org/10.1186/1471-2334-14-323

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  27. Botelho ACN, Oliveira JG, Damasco AP, Santos KTB, Ferreira AFM, Rocha GT, Marinho PS, Bornia RBG, Pinto TCA, Américo MA, Fracalanzza SEL, Teixeira LM (2018) Streptococcus agalactiae carriage among pregnant women living in Rio de Janeiro, Brazil, over a period of eight years. PLoS One 13(5):e0196925. https://doi.org/10.1371/journal.pone.0196925

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  28. Do Nascimento CS, Dos Santos NFB, Ferreira RCC, Taddei CR (2019) Streptococcus agalactiae in pregnant women in Brazil: prevalence, serotypes, and antibiotic resistance. Braz J Microbiol 1:1–10. https://doi.org/10.1007/s42770-019-00129-8

    Article  CAS  Google Scholar 

  29. Kernéis S, Plainvert C, Barnier JP, Tazi A, Dmytruk N, Gislain B, Loubinoux J, El Sayed F, Cattoir V, Desplaces N, Vernet V, Morand P, Poyart C (2017) Clinical and microbiological features associated with group B Streptococcus bone and joint infections, France 2004-2014. Eur J Clin Microbiol Infect Dis. 36(9):1679–1684. https://doi.org/10.1007/s10096-017-2983-y

    Article  PubMed  Google Scholar 

  30. Palmeiro JK, Dalla-Costa LM, Fracalanzza SE, Botelho AC, da Silva NK, Scheffer MC, de Almeida Torres RS, de Carvalho NS, Cogo LL, Madeira HM (2010) Phenotypic and genotypic characterization of group B streptococcal isolates in southern Brazil. J Clin Microbiol l48(12):4397–4403. https://doi.org/10.1128/JCM.00419-10

    Article  Google Scholar 

  31. Alhhazmi A, Hurteau D, Tyrrell GJ (2016) Epidemiology of invasive group B streptococcal disease in Alberta. Canada, from 2003 to 2013. J Clin Microbiol 54:1774–1781. https://doi.org/10.1128/jcm.00355-16

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  32. Campisi E, Rinaudo CD, Donati C, Barucco M, Torricelli G, Edwards MS, Baker CJ, Margarit I, Rosini R (2016) Serotype IV Streptococcus agalactiae ST-452 has arisen from large genomic recombination events between CC23 and the hypervirulent CC17 lineages. Sci Rep 6:29799. https://doi.org/10.1038/srep29799

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  33. Oviedo P, Pegels E, Laczeski M, Quiroga M, Vergara M (2013) Phenotypic and genotypic characterization of Streptococcus agalactiae in pregnant woman. First study in a province of Argentina. Braz J Microbiol 44:253–258. https://doi.org/10.1590/S1517-83822013005000030

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  34. Lu B, Wu J, Chen X, Gao C, Yang J, Li Y, Wang J, Zeng J, Fang Y, Wang D, Cui Y, Wang L (2018) Microbiological and clinical characteristics of Group B Streptococcus isolates causing materno-neonatal infections: high prevalence of CC17/PI-1 and PI-2b sublineage in neonatal infections. J Med Microbiol 67:1551–1559. https://doi.org/10.1099/jmm.0.000849

    Article  CAS  PubMed  Google Scholar 

  35. Hays C, Touak G, Bouaboud A, Fouet A, Guignot J, Poyart C, Tazi A (2019) Perinatal hormones favor CC17 group B Streptococcus intestinal translocation through M cells and hypervirulence in neonates. Elife 8:e48772. https://doi.org/10.7554/eLife.48772

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  36. Vigliarolo L, Arias B, Suárez M, Van Haute E, Kovacec V, Lopardo H, Bonofiglio L, Mollerach M (2019) Argentinian multicenter study on urinary tract infections due to Streptococcus agalactiae in adult patients. J Infect Dev Ctries 13:77–82. https://doi.org/10.3855/jidc.10503

    Article  CAS  PubMed  Google Scholar 

  37. Tazi A, Morand PC, Réglier-Poupet H, Dmytruk N, Billoët A, Antona D, Trieu-Cuot P, Poyart C (2011) Invasive group B streptococcal infections in adults, France (2007-2010). Clin Microbiol Infect 17:1587–1589. https://doi.org/10.1111/j.1469-0691.2011.03628.x

    Article  CAS  PubMed  Google Scholar 

  38. Beyar-Katz O, Dickstein Y, Borok S, Vidal L, Leibovici L, Paul M (2017) Empirical antibiotics targeting gram-positive bacteria for the treatment of febrile neutropenic patients with cancer. Cochrane Database Syst Rev 6:CD003914. https://doi.org/10.1002/14651858.CD003914

    Article  PubMed  Google Scholar 

  39. Guo H, Fu M, Peng Q, Chen Z, Liu J, Qiu Y, Huang Y (2019) Antimicrobial resistance and molecular characterization of Streptococcus agalactiae from pregnant women in southern China. J Infect Dev Ctries 13:802–809. https://doi.org/10.3855/jidc.11395

    Article  CAS  PubMed  Google Scholar 

  40. Hamed SM, Elkhatib WF, El-Mahallawy HA, Helmy MM, Ashour MS (2018) Aboshanab KMA (2018) Multiple mechanisms contributing to ciprofloxacin resistance among Gram negative bacteria causing infections to cancer patients. Sci Rep. 8:12268. https://doi.org/10.1038/s41598-018-30756-4

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  41. Arias B, Kovacec V, Vigliarolo L, Suárez M, Tersigni C, Müller L, Lopardo H, Bonofiglio L, Mollerach M (2019) Fluoroquinolone-resistant Streptococcus agalactiae invasive isolates recovered in Argentina. Microb Drug Resist 25(5):739–743. https://doi.org/10.1089/mdr.2018.0246

    Article  CAS  PubMed  Google Scholar 

  42. Guo Y, Deng X, Liang Y, Zhang L, Zhao GP, Zhou Y (2018) The draft genomes and investigation of serotype distribution, antimicrobial resistance of group B Streptococcus strains isolated from urine in Suzhou, China. Ann Clin Microbiol Antimicrob. 17(1):28. https://doi.org/10.1186/s12941-018-0280-y

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  43. Hays C, Louis M, Plainvert C, Dmytruk N, Touak G, Trieu-Cuot P, Poyart C, Tazi A (2016) Changing epidemiology of group B Streptococcus susceptibility to fluoroquinolones and aminoglycosides in France. Antimicrob Agents Chemother 60(12):7424–7430. https://doi.org/10.1128/AAC.01374-16

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  44. Simoni S, Vincenzi C, Brenciani A, Morroni G, Bagnarelli P, Giovanetti E, Mingoia M (2018) Molecular characterization of Italian isolates of fluoroquinolone-resistant Streptococcus agalactiae and relationships with chloramphenicol resistance. Microbial Drug Resist 24(3):225–231. https://doi.org/10.1089/mdr.2017.0139

    Article  CAS  Google Scholar 

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Acknowledgments

The authors acknowledge the Instituto Nacional do Câncer – INCA and Dr. Carlos Martins for providing the S. agalactiae strains.

Funding

This study was funded by the Fundação de Amparo à Pesquisa do Estado do Rio de Janeiro (FAPERJ) [award number E-26/010.000895/2015]. This study was also financed in part by the Coordenação de Aperfeiçoamento de Pessoal de Nível Superior - Brasil (CAPES) - Finance Code 001 and Sub Reitoria de Pós-Graduação e Pesquisa da Universidade do Estado do Rio de Janeiro (SR-2/UERJ) provided postgraduate scholarships. Finance code NIH/NINDS R01-NS051247 to KSD.

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Authors and Affiliations

  1. Laboratório de Biologia Molecular e Fisiologia de Estreptococos, Instituto de Biologia Roberto Alcantara Gomes, Rio de Janeiro State University, Rua São Francisco Xavier, 524 - PHLC 5º andar sala 501B-Maracanã, Rio de Janeiro, RJ, CEP 20550-013, Brazil

    Glenda de Figueiredo Sanches, Pamella Silva Lannes-Costa, Melissa Coimbra Cristoforêto & Prescilla Emy Nagao

  2. Department of Immunology and Microbiology, University of Colorado School of Medicine, Aurora, CO, USA

    Glenda de Figueiredo Sanches & Kelly S. Doran

  3. Faculdade de Ciências Médicas, Rio de Janeiro State University (UERJ), Rio de Janeiro, RJ, Brazil

    Ana Luíza Mattos-Guaraldi

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  1. Glenda de Figueiredo Sanches
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  2. Pamella Silva Lannes-Costa
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  3. Melissa Coimbra Cristoforêto
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Contributions

G.F.S. and P.E.N. participated in the design and discussion of the research. G.F.S. and P.S.L.C. carried out the experimental part of the work, wrote the original draft, carried out the analysis of the data, and wrote the final manuscript. M.C.C. carried antimicrobial susceptibility. G.F.S., P.S.L.C., K.S.D., A.L.M.G., and P.E.N. contributed to literature review and manuscript discussion. All authors have read and approved the final manuscript.

Corresponding author

Correspondence to Prescilla Emy Nagao.

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The authors declare that they have no conflict of interests.

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Ethical approval for the study was obtained from the Institutional Ethics Commission, Instituto Nacional do Cancer (INCA)/Rio de Janeiro Pedro Ernesto Hospital University (CONEP-CAAE: 04124313.0.0000.5259).

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Responsible Editor: Agnes M.S. Figueiredo

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de Figueiredo Sanches, G., Lannes-Costa, P.S., Cristoforêto, M.C. et al. Streptococcus agalactiae strains isolated from cancer patients in Rio de Janeiro, Brazil. Braz J Microbiol 52, 303–310 (2021). https://doi.org/10.1007/s42770-020-00419-6

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