#PAGE_PARAMS# #ADS_HEAD_SCRIPTS# #MICRODATA#

Determinants of Group B streptococcal virulence potential amongst vaginal clinical isolates from pregnant women


Autoři: Lindsey R. Burcham aff001;  Brady L. Spencer aff001;  Lauryn R. Keeler aff002;  Donna L. Runft aff003;  Kathryn A. Patras aff002;  Melody N. Neely aff003;  Kelly S. Doran aff001
Působiště autorů: Department of Immunology and Microbiology, University of Colorado, Aurora, CO, United States of America aff001;  Department of Biology, San Diego State University, San Diego, CA, United States of America aff002;  Department of Molecular & Biomedical Sciences, University of Maine, Orono, ME, United States of America aff003
Vyšlo v časopise: PLoS ONE 14(12)
Kategorie: Research Article
doi: https://doi.org/10.1371/journal.pone.0226699

Souhrn

Streptococcus agalactiae, also known as Group B Streptococcus (GBS), is a Gram-positive bacterium isolated from the vaginal tract of approximately 25% of women. GBS colonization of the female reproductive tract is of particular concern during pregnancy as the bacteria can invade gestational tissues or be transmitted to the newborn during passage through the birth canal. Infection of the neonate can result in life-threatening pneumonia, sepsis and meningitis. Thus, surveillance of GBS strains and corresponding virulence potential during colonization is warranted. Here we describe a panel of GBS isolates from the vaginal tracts of a cohort of pregnant women in Michigan, USA. We determined that capsular serotypes III and V were the most abundant across the strain panel, with only one isolate belonging to serotype IV. Further, 12.8% of strains belonged to the hyper-virulent serotype III, sequence type 17 (ST-17) and 15.4% expressed the serine rich repeat glycoprotein-encoding gene srr2. Functional assessment of the colonizing isolates revealed that almost all strains exhibited some level of β-hemolytic activity and that ST-17 strains, which express Srr2, exhibited increased bacterial adherence to vaginal epithelium. Finally, analysis of strain antibiotic susceptibility revealed the presence of antibiotic resistance to penicillin (15.4%), clindamycin (30.8%), erythromycin (43.6%), vancomycin (30.8%), and tetracycline (94.9%), which has significant implications for treatment options. Collectively, these data provide important information on vaginal GBS carriage isolate virulence potential and highlight the value of continued surveillance.

Klíčová slova:

Antibiotic resistance – Antibiotics – Epithelial cells – Erythromycin – Penicillin – Tetracyclines – Vancomycin – Clindamycin


Zdroje

1. Verani JR, McGee L, Schrag SJJM, Mortality Weekly Report RGfC, Recommendations, Reports. Prevention of perinatal group B streptococcal disease. 2010;59(RR10):1–32.

2. Melin P. Neonatal group B streptococcal disease: from pathogenesis to preventive strategies. Clinical Microbiology and Infection. 2011;17(9):1294–303. doi: 10.1111/j.1469-0691.2011.03576.x 21672083

3. Doran KS, Nizet V. Molecular pathogenesis of neonatal group B streptococcal infection: no longer in its infancy. Molecular microbiology. 2004;54(1):23–31. doi: 10.1111/j.1365-2958.2004.04266.x 15458402

4. Baker C, Edwards M. Group B Streptococcal infections, p. 1091–1156. Infectious diseases of the fetus and newborn infant, 5th ed WB Saunders, Philadelphia, Pa. 2001.

5. Schrag S, Gorwitz RJ, Fultz-Butts K, Schuchat A. Prevention of perinatal group B streptococcal disease; revised guidelines from CDC. MMWR Recomm Rep. 2002;51(RR11):1–22.

6. Phares CR, Lynfield R, Farley MM, Mohle-Boetani J, Harrison LH, Petit S, et al. Epidemiology of invasive group B streptococcal disease in the United States, 1999–2005. Jama. 2008;299(17):2056–65. doi: 10.1001/jama.299.17.2056 18460666

7. CDC. Active Bacterial Core Surveillance Report, Emerging Infections Program Network, Group B Streptococcus, 2017. 2017.

8. Armistead B, Oler E, Waldorf KA, Rajagopal L. The Double Life of Group B Streptococcus: Asymptomatic Colonizer and Potent Pathogen. Journal of molecular biology. 2019.

9. Edmond KM, Kortsalioudaki C, Scott S, Schrag SJ, Zaidi AK, Cousens S, et al. Group B streptococcal disease in infants aged younger than 3 months: systematic review and meta-analysis. The Lancet. 2012;379(9815):547–56.

10. Jones N, Bohnsack JF, Takahashi S, Oliver KA, Chan M-S, Kunst F, et al. Multilocus sequence typing system for group B streptococcus. Journal of clinical microbiology. 2003;41(6):2530–6. doi: 10.1128/JCM.41.6.2530-2536.2003 12791877

11. Tazi A, Disson O, Bellais S, Bouaboud A, Dmytruk N, Dramsi S, et al. The surface protein HvgA mediates group B streptococcus hypervirulence and meningeal tropism in neonates. Journal of experimental medicine. 2010;207(11):2313–22. doi: 10.1084/jem.20092594 20956545

12. Nizet V, Gibson RL, Chi EY, Framson PE, Hulse M, Rubens CEJI, et al. Group B streptococcal beta-hemolysin expression is associated with injury of lung epithelial cells. 1996;64(9):3818–26. 8751934

13. Doran KS, Chang JC, Benoit VM, Eckmann L, Nizet VJTJoid. Group B streptococcal β-hemolysin/cytolysin promotes invasion of human lung epithelial cells and the release of interleukin-8. 2002;185(2):196–203. doi: 10.1086/338475 11807693

14. Doran KS, Liu GY, Nizet VJTJoci. Group B streptococcal β-hemolysin/cytolysin activates neutrophil signaling pathways in brain endothelium and contributes to development of meningitis. 2003;112(5):736–44. doi: 10.1172/JCI17335 12952922

15. Seifert KN, Adderson EE, Whiting AA, Bohnsack JF, Crowley PJ, Brady LJJM. A unique serine-rich repeat protein (Srr-2) and novel surface antigen (ε) associated with a virulent lineage of serotype III Streptococcus agalactiae. 2006;152(4):1029–40.

16. Samen U, Eikmanns BJ, Reinscheid DJ, Borges FJI, immunity. The surface protein Srr-1 of Streptococcus agalactiae binds human keratin 4 and promotes adherence to epithelial HEp-2 cells. 2007;75(11):5405–14.

17. Sheen TR, Jimenez A, Wang N-Y, Banerjee A, van Sorge NM, Doran KS. Serine-Rich Repeat Proteins and Pili Promote Streptococcus agalactiae Colonization of the Vaginal Tract. 2011;193(24):6834–42. doi: 10.1128/JB.00094-11 21984789

18. Seo HS, Mu R, Kim BJ, Doran KS, Sullam PMJPp. Binding of glycoprotein Srr1 of Streptococcus agalactiae to fibrinogen promotes attachment to brain endothelium and the development of meningitis. 2012;8(10):e1002947. doi: 10.1371/journal.ppat.1002947 23055927

19. Wang N-Y, Patras KA, Seo HS, Cavaco CK, Rösler B, Neely MN, et al. Group B streptococcal serine-rich repeat proteins promote interaction with fibrinogen and vaginal colonization. 2014;210(6):982–91. doi: 10.1093/infdis/jiu151 24620021

20. Maisey HC, Hensler M, Nizet V, Doran KSJJob. Group B streptococcal pilus proteins contribute to adherence to and invasion of brain microvascular endothelial cells. 2007;189(4):1464–7. doi: 10.1128/JB.01153-06 17041051

21. Maisey HC, Quach D, Hensler ME, Liu GY, Gallo RL, Nizet V, et al. A group B streptococcal pilus protein promotes phagocyte resistance and systemic virulence. 2008;22(6):1715–24. doi: 10.1096/fj.07-093963 18198218

22. Banerjee A, Kim BJ, Carmona EM, Cutting AS, Gurney MA, Carlos C, et al. Bacterial Pili exploit integrin machinery to promote immune activation and efficient blood-brain barrier penetration. 2011;2:462. doi: 10.1038/ncomms1474 21897373

23. Lauer P, Rinaudo CD, Soriani M, Margarit I, Maione D, Rosini R, et al. Genome analysis reveals pili in Group B Streptococcus. 2005;309(5731):105–. doi: 10.1126/science.1111563 15994549

24. Dramsi S, Caliot E, Bonne I, Guadagnini S, Prévost MC, Kojadinovic M, et al. Assembly and role of pili in group B streptococci. 2006;60(6):1401–13. doi: 10.1111/j.1365-2958.2006.05190.x 16796677

25. Jacobsson KJVm. A novel family of fibrinogen-binding proteins in Streptococcus agalactiae. 2003;96(1):103–13. doi: 10.1016/s0378-1135(03)00206-2 14516712

26. Madoff LC, Michel JL, Kasper DL. A monoclonal antibody identifies a protective C-protein alpha-antigen epitope in group B streptococci. 1991;59(1):204–10. 1702759

27. Faralla C, Metruccio MM, De Chiara M, Mu R, Patras KA, Muzzi A, et al. Analysis of Two-Component Systems in Group B Streptococcus Shows That RgfAC and the Novel FspSR Modulate Virulence and Bacterial Fitness. mBio. 2014;5(3):e00870–14. doi: 10.1128/mBio.00870-14 24846378

28. Wilkinson HW. Nontypable group B streptococci isolated from human sources. 1977;6(2):183–4. 408376

29. Wilson CB, Weaver WMJJoID. Comparative susceptibility of group B streptococci and Staphylococcus aureus to killing by oxygen metabolites. 1985;152(2):323–9. doi: 10.1093/infdis/152.2.323 2993435

30. Hayano S, Tanaka A. Repetitive counterelectrophoresis on agar gel for the immunological identification of esterases produced by strains of Lancefield's group A, B, and C streptococci. Infect Immun. 1977;15(1):295–9. 319062

31. Poyart C, Tazi A, Réglier-Poupet H, Billoët A, Tavares N, Raymond J, et al. Multiplex PCR assay for rapid and accurate capsular typing of group B streptococci. Journal of clinical microbiology. 2007;45(6):1985–8. doi: 10.1128/JCM.00159-07 17376884

32. Geno KA, Saad JS, Nahm MH. Discovery of Novel Pneumococcal Serotype 35D, a Natural WciG-Deficient Variant of Serotype 35B. J Clin Microbiol. 2017;55(5):1416–25. doi: 10.1128/JCM.00054-17 28202800

33. Wharton RE, Stefanov EK, King RG, Kearney JF. Antibodies generated against Streptococci protect in a mouse model of disseminated aspergillosis. J Immunol. 2015;194(9):4387–96. doi: 10.4049/jimmunol.1401940 25821219

34. Pritchard DG, Gray BM, Egan ML. Murine monoclonal antibodies to type Ib polysaccharide of group B streptococci bind to human milk oligosaccharides. Infection and immunity. 1992;60(4):1598–602. 1548081

35. Gray BM, Egan ML, Pritchard DGJPr. Specificity of monoclonal antibodies against group B streptococcus type II and inhibition of their binding by human secretions. 1988;24(1):68. doi: 10.1203/00006450-198807000-00017 2457865

36. Egan ML, Pritchard DG, Dillon H, Gray BJJoEM. Protection of mice from experimental infection with type III Group B Streptococcus using monoclonal antibodies. 1983;158(3):1006–11. doi: 10.1084/jem.158.3.1006 6193228

37. Whidbey C, Harrell MI, Burnside K, Ngo L, Becraft AK, Iyer LM, et al. A hemolytic pigment of Group B Streptococcus allows bacterial penetration of human placenta. Journal of Experimental Medicine. 2013;210(6):1265–81. doi: 10.1084/jem.20122753 23712433

38. Lamy M-C, Dramsi S, Billoët A, Réglier-Poupet H, Tazi A, Raymond J, et al. Rapid detection of the “highly virulent” Group B Streptococcus ST-17 clone. Microbes and infection. 2006;8(7):1714–22. doi: 10.1016/j.micinf.2006.02.008 16822689

39. Patras KA, Rosler B, Thoman ML, Doran KS. Characterization of host immunity during persistent vaginal colonization by Group B Streptococcus. Mucosal immunology. 2015;8(6):1339–48. doi: 10.1038/mi.2015.23 25850655

40. Patras KA, Wang NY, Fletcher EM, Cavaco CK, Jimenez A, Garg M, et al. Group B Streptococcus CovR regulation modulates host immune signalling pathways to promote vaginal colonization. 2013;15(7):1154–67. doi: 10.1111/cmi.12105 23298320

41. Biemer JJ. Antimicrobial susceptibility testing by the Kirby-Bauer disc diffusion method. Annals of Clinical & Laboratory Science. 1973;3(2):135–40.

42. Seo HS, Minasov G, Seepersaud R, Doran KS, Dubrovska I, Shuvalova L, et al. Characterization of fibrinogen binding by glycoproteins Srr1 and Srr2 of Streptococcus agalactiae. Journal of Biological Chemistry. 2013;288(50):35982–96. doi: 10.1074/jbc.M113.513358 24165132

43. Six A, Bellais S, Bouaboud A, Fouet A, Gabriel C, Tazi A, et al. Srr2, a multifaceted adhesin expressed by ST‐17 hypervirulent G roup B Streptococcus involved in binding to both fibrinogen and plasminogen. Molecular microbiology. 2015;97(6):1209–22. doi: 10.1111/mmi.13097 26094503

44. Seifert KN, Adderson EE, Whiting AA, Bohnsack JF, Crowley PJ, Brady LJ. A unique serine-rich repeat protein (Srr-2) and novel surface antigen (epsilon) associated with a virulent lineage of serotype III Streptococcus agalactiae. Microbiology. 2006;152(Pt 4):1029–40. doi: 10.1099/mic.0.28516-0 16549667

45. Six A, Bellais S, Bouaboud A, Fouet A, Gabriel C, Tazi A, et al. Srr2, a multifaceted adhesin expressed by ST-17 hypervirulent Group B Streptococcus involved in binding to both fibrinogen and plasminogen. Mol Microbiol. 2015;97(6):1209–22. doi: 10.1111/mmi.13097 26094503

46. Anthony BF, Concepcion NF. Group B Streptococcus in a general hospital. J Infect Dis. 1975;132(5):561–7. doi: 10.1093/infdis/132.5.561 1102616

47. A'Hearn-Thomas B, Khatami A, Randis TM, Vurayai M, Mokomane M, Arscott-Mills T, et al. High Rate of Serotype V Streptococcus agalactiae Carriage in Pregnant Women in Botswana. The American journal of tropical medicine and hygiene. 2019.

48. Belard S, Toepfner N, Capan-Melser M, Mombo-Ngoma G, Zoleko-Manego R, Groger M, et al. Streptococcus agalactiae serotype distribution and antimicrobial susceptibility in pregnant women in Gabon, Central Africa. 2015;5:17281. doi: 10.1038/srep17281 26603208

49. Botelho ACN, Oliveira JG, Damasco AP, Santos KT, Ferreira AFM, Rocha GT, et al. Streptococcus agalactiae carriage among pregnant women living in Rio de Janeiro, Brazil, over a period of eight years. 2018;13(5):e0196925. doi: 10.1371/journal.pone.0196925 29750801

50. Chukwu MO, Mavenyengwa RT, Monyama CM, Bolukaoto JY, Lebelo SL, Maloba MR, et al. Antigenic distribution of Streptococcus agalactiae isolates from pregnant women at Garankuwa hospital–South Africa. 2015;5(4):125. doi: 10.11599/germs.2015.1080 26716101

51. Corrêa ABdA, Silva LGd, Pinto TdCA, Oliveira ICMd, Fernandes FG, Costa NSd, et al. The genetic diversity and phenotypic characterisation of Streptococcus agalactiae isolates from Rio de Janeiro, Brazil. 2011;106(8):1002–6. doi: 10.1590/s0074-02762011000800017 22241124

52. Dutra VG, Alves VM, Olendzki AN, Dias CA, de Bastos AF, Santos GO, et al. Streptococcus agalactiae in Brazil: serotype distribution, virulence determinants and antimicrobial susceptibility. 2014;14(1):323.

53. El Aila NA, Tency I, Claeys G, Saerens B, De Backer E, Temmerman M, et al. Genotyping of Streptococcus agalactiae (group B streptococci) isolated from vaginal and rectal swabs of women at 35–37 weeks of pregnancy. 2009;9(1):153.

54. Eskandarian N, Ismail Z, Neela V, Van Belkum A, Desa M, Nordin SAJEJoCM, et al. Antimicrobial susceptibility profiles, serotype distribution and virulence determinants among invasive, non-invasive and colonizing Streptococcus agalactiae (group B streptococcus) from Malaysian patients. 2015;34(3):579–84. doi: 10.1007/s10096-014-2265-x 25359580

55. Florindo C, Viegas S, Paulino A, Rodrigues E, Gomes JP, Borrego MJJCM, et al. Molecular characterization and antimicrobial susceptibility profiles in Streptococcus agalactiae colonizing strains: association of erythromycin resistance with subtype III-1 genetic clone family. 2010;16(9):1458–63. doi: 10.1111/j.1469-0691.2009.03106.x 19886900

56. Hannoun A, Shehab M, Khairallah M-T, Sabra A, Abi-Rached R, Bazi T, et al. Correlation between group B streptococcal genotypes, their antimicrobial resistance profiles, and virulence genes among pregnant women in Lebanon. 2010;2009.

57. Ji W, Zhang L, Guo Z, Xie S, Yang W, Chen J, et al. Colonization prevalence and antibiotic susceptibility of Group B Streptococcus in pregnant women over a 6-year period in Dongguan, China. PloS one. 2017;12(8):e0183083. doi: 10.1371/journal.pone.0183083 28813477

58. Khatami A, Randis TM, Tavares L, Gegick M, Suzman E, Ratner AJ. Vaginal co-colonization with multiple Group B Streptococcus serotypes. Vaccine. 2019;37(3):409–11. doi: 10.1016/j.vaccine.2018.12.001 30528847

59. Khodaei F, Najafi M, Hasani A, Kalantar E, Sharifi E, Amini A, et al. Pilus–encoding islets in S. agalactiae and its association with antibacterial resistance and serotype distribution. 2018;116:189–94. doi: 10.1016/j.micpath.2018.01.035 29371153

60. Liakopoulos A, Mavroidi A, Vourli S, Panopoulou M, Zachariadou L, Chatzipanagiotou S, et al. Molecular characterization of Streptococcus agalactiae from vaginal colonization and neonatal infections: a 4-year multicenter study in Greece. 2014;78(4):487–90. doi: 10.1016/j.diagmicrobio.2013.12.017 24503505

61. Mavenyengwa R, Maeland J, Moyo SJIjomm. Serotype markers in a Streptococcus agalactiae strain collection from Zimbabwe. 2010;28(4):313. doi: 10.4103/0255-0857.71819 20966561

62. Pinto AM, Pereira TA, Alves V, Araújo A, Lage OM. Incidence and serotype characterisation of Streptococcus agalactiae in a Portuguese hospital. 2018;71(6):508–13. doi: 10.1136/jclinpath-2017-204646 29180508

63. Sadeh M, Firouzi R, Derakhshandeh A, Khalili MB, Kong F, Kudinha TJJjom. Molecular characterization of Streptococcus agalactiae isolates from pregnant and non-pregnant women at Yazd University Hospital, Iran. 2016;9(2). doi: 10.5812/jjm.30412 27127592

64. Seo YS, Srinivasan U, Oh KY, Shin JH, Chae JD, Kim MY, et al. Changing molecular epidemiology of group B streptococcus in Korea. J Korean Med Sci. 2010;25(6):817–23. doi: 10.3346/jkms.2010.25.6.817 20514299

65. Slotved H-C, Dayie NT, Banini JA, Frimodt-Møller NJBp, childbirth. Carriage and serotype distribution of Streptococcus agalactiae in third trimester pregnancy in southern Ghana. 2017;17(1):238. doi: 10.1186/s12884-017-1419-0 28732495

66. Smith T, Roehl S, Pillai P, Li S, Marrs C, Foxman BJE, et al. Distribution of novel and previously investigated virulence genes in colonizing and invasive isolates of Streptococcus agalactiae. 2007;135(6):1046–54. doi: 10.1017/S0950268806007515 17156495

67. Teatero S, Ferrieri P, Martin I, Demczuk W, McGeer A, Fittipaldi N. Serotype Distribution, Population Structure, and Antimicrobial Resistance of Group B Streptococcus Strains Recovered from Colonized Pregnant Women. J Clin Microbiol. 2017;55(2):412–22. doi: 10.1128/JCM.01615-16 27852675

68. Ueno H, Yamamoto Y, Yamamichi A, Kikuchi K, Kobori S, Miyazaki MJJjoid. Characterization of group B streptococcus isolated from women in Saitama city, Japan. 2012;65(6):516–21. doi: 10.7883/yoken.65.516 23183204

69. Usein C-R, Militaru M, Cristea V, Străuţ MJMdIOC. Genetic diversity and antimicrobial resistance in Streptococcus agalactiae strains recovered from female carriers in the Bucharest area. 2014;109(2):189–96. doi: 10.1590/0074-0276140431 24676662

70. Randis TM, Gelber SE, Hooven TA, Abellar RG, Akabas LH, Lewis EL, et al. Group B Streptococcus β-hemolysin/cytolysin breaches maternal-fetal barriers to cause preterm birth and intrauterine fetal demise in vivo. The Journal of infectious diseases. 2014;210(2):265–73. doi: 10.1093/infdis/jiu067 24474814

71. Carey AJ, Tan CK, Mirza S, Irving-Rodgers H, Webb RI, Lam A, et al. Infection and cellular defense dynamics in a novel 17β-estradiol murine model of chronic human group B streptococcus genital tract colonization reveal a role for hemolysin in persistence and neutrophil accumulation. The Journal of Immunology. 2014;192(4):1718–31. doi: 10.4049/jimmunol.1202811 24453257

72. Patras KA, Doran KS. A murine model of group B Streptococcus vaginal colonization. JoVE (Journal of Visualized Experiments). 2016(117):e54708.

73. Jiang S-M, Cieslewicz MJ, Kasper DL, Wessels MR. Regulation of virulence by a two-component system in group B streptococcus. Journal of Bacteriology. 2005;187(3):1105–13. doi: 10.1128/JB.187.3.1105-1113.2005 15659687

74. Park SE, Jiang S, Wessels MR. CsrRS and environmental pH regulate group B streptococcus adherence to human epithelial cells and extracellular matrix. Infection and immunity. 2012;80(11):3975–84. doi: 10.1128/IAI.00699-12 22949550

75. Jones N, Oliver KA, Barry J, Harding RM, Bisharat N, Spratt BG, et al. Enhanced invasiveness of bovine-derived neonatal sequence type 17 group B streptococcus is independent of capsular serotype. Clin Infect Dis. 2006;42(7):915–24. doi: 10.1086/500324 16511753

76. Brochet M, Couve E, Zouine M, Vallaeys T, Rusniok C, Lamy MC, et al. Genomic diversity and evolution within the species Streptococcus agalactiae. Microbes Infect. 2006;8(5):1227–43. doi: 10.1016/j.micinf.2005.11.010 16529966

77. Manning SD, Lewis MA, Springman AC, Lehotzky E, Whittam TS, Davies HD. Genotypic diversity and serotype distribution of group B streptococcus isolated from women before and after delivery. Clin Infect Dis. 2008;46(12):1829–37. doi: 10.1086/588296 18462173

78. Manning SD, Springman AC, Lehotzky E, Lewis MA, Whittam TS, Davies HD. Multilocus sequence types associated with neonatal group B streptococcal sepsis and meningitis in Canada. J Clin Microbiol. 2009;47(4):1143–8. doi: 10.1128/JCM.01424-08 19158264

79. Takahashi S, Adderson EE, Nagano Y, Nagano N, Briesacher MR, Bohnsack JF. Identification of a Highly Encapsulated, Genetically Related Group of Invasive Type III Group B Streptococci. The Journal of Infectious Diseases. 1998;177(4):1116–9. doi: 10.1086/517408 9534996

80. Lembo A, Gurney MA, Burnside K, Banerjee A, De Los Reyes M, Connelly JE, et al. Regulation of CovR expression in Group B Streptococcus impacts blood–brain barrier penetration. Molecular microbiology. 2010;77(2):431–43. doi: 10.1111/j.1365-2958.2010.07215.x 20497331

81. Kimura K, Suzuki S, Wachino J-i, Kurokawa H, Yamane K, Shibata N, et al. First molecular characterization of group B streptococci with reduced penicillin susceptibility. 2008;52(8):2890–7. doi: 10.1128/AAC.00185-08 18490507

82. Crespo-Ortiz MdP, Castañeda-Ramirez CR, Recalde-Bolaños M, Vélez-Londoño JDJBID. Emerging trends in invasive and noninvasive isolates of Streptococcus agalactiae in a Latin American hospital: a 17-year study. 2014;14(1):428.

83. Moroi H, Kimura K, Kotani T, Tsuda H, Banno H, Jin W, et al. Isolation of Group B Streptococcus with reduced β-lactam susceptibility from pregnant women. 2019;8(1):2–7. doi: 10.1080/22221751.2018.1557987 30866792

84. Gizachew M, Tiruneh M, Moges F, Tessema BJAocm, antimicrobials. Streptococcus agalactiae maternal colonization, antibiotic resistance and serotype profiles in Africa: a meta-analysis. 2019;18(1):14.


Článek vyšel v časopise

PLOS One


2019 Číslo 12
Nejčtenější tento týden
Nejčtenější v tomto čísle
Kurzy

Zvyšte si kvalifikaci online z pohodlí domova

Současné pohledy na riziko v parodontologii
nový kurz
Autoři: MUDr. Ladislav Korábek, CSc., MBA

Svět praktické medicíny 3/2024 (znalostní test z časopisu)

Kardiologické projevy hypereozinofilií
Autoři: prof. MUDr. Petr Němec, Ph.D.

Střevní příprava před kolonoskopií
Autoři: MUDr. Klára Kmochová, Ph.D.

Aktuální možnosti diagnostiky a léčby litiáz
Autoři: MUDr. Tomáš Ürge, PhD.

Všechny kurzy
Kurzy Podcasty Doporučená témata Časopisy
Přihlášení
Zapomenuté heslo

Zadejte e-mailovou adresu, se kterou jste vytvářel(a) účet, budou Vám na ni zaslány informace k nastavení nového hesla.

Přihlášení

Nemáte účet?  Registrujte se

#ADS_BOTTOM_SCRIPTS#