Determination of pilus-islands profile and antibiotic susceptibility of Streptococcus agalactiae isolated from urine of pregnant women
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Abstract
Background and Objectives: Group B Streptococcus (GBS) is one of the most important causes of neonatal diseases and postpartum fever. GBS infection can be transmitted from the infected mother to her baby during delivery. This bacterium is also involved in causing urinary tract infections and asymptomatic bacteriuria, pyelonephritis, cystitis and urethritis. In addition to capsule, Pilus is known as a virulence factor of GBS. The aim of this study was to evaluate the frequency of pilus islands and antibiotic resistance in GBS isolated from urine of pregnant women in Yazd, Iran.
Materials and Methods: In this cross-sectional study, 33 GBS samples isolated from the urine of pregnant women were studied by the multiplex polymerase chain reaction (PCR) method for the presence of pilus islands PI-1, PI-2a and PI-2b. Antibiotic resistance phenotype of tetracycline, penicillin, gentamicin, erythromycin, levofloxacin and clindamycin was determined by disk diffusion method. Data were analyzed using SPSS, version 16.
Results: PI-1+PI-2a was the most frequent pilus island in the GBS isolates 28 (84.8%) and the frequency of PI-2b was 5 (15.2%). The frequency of PI-1+PI-2a was 50% in serotype III and 25%, 14.3%, 7.1% and 3.6% in serotypes Ia, II, Ib and V respectively (P=0.492). The sensitivity of all GBS isolates to penicillin was 93.9% and highest resistance to tetracycline (97%), clindamycin (24.2%) and erythromycin (21.2%).
Conclusion: Most of the GBS urine isolates examined carried the PI-1+PI-2a gene, which increases bacterial potency in colonization and resistance to the immune system. Penicillin was best choice for prevention.
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3. Ali MM, Woldeamanuel Y, Asrat D, Fenta DA, Beall B, Schrag S, et al. Features of Streptococcus agalactiae strains recovered from pregnant women and newborns attending different hospitals in Ethiopia. BMC Infect Dis 2020; 20: 848.
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7. Shadbad MA, Kafil HS, Rezaee MA, Farzami MR, Dehkharghani AD, Sadeghi J, et al. Filament genes and biofilm formation in Streptococcus agalactiae. Rev Med Microbiol 2020; 31: 17-25.
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10. Martins ER, Melo-Cristino J, Ramirez M. Evidence for rare capsular switching in Streptococcus agalactiae. J Bacteriol 2010; 192: 1361-1369.
11. Clinical, Institute LS. Performance standards for antimicrobial susceptibility testing. Clinical and Laboratory Standards Institute Wayne, PA; 2018.
12. Desai D, Goh KGK, Sullivan MJ, Chattopadhyay D, Ulett GC. Hemolytic activity and biofilm-formation among clinical isolates of group B streptococcus causing acute urinary tract infection and asymptomatic bacteriuria. Int J Med Microbiol 2021; 311: 151520.
13. Springman AC, Lacher DW, Waymire EA, Wengert SL, Singh P, Zadoks RN, et al. Pilus distribution among lineages of group b streptococcus: an evolutionary and clinical perspective. BMC Microbiol 2014; 14: 159.
14. Shadbad MA, Kafil HS, Rezaee MA, Farzami MR, Dehkharghani AD, Sadeghi J, et al. Streptococcus agalactiae clinical isolates in Northwest Iran: antibiotic susceptibility, molecular typing, and biofilm formation. GMS Hyg Infect Control 2020; 15: Doc23.
15. Madzivhandila M, Adrian PV, Cutland CL, Kuwanda L, Madhi SA, Team PT. Distribution of pilus islands of group B streptococcus associated with maternal colonization and invasive disease in South Africa. J Med Microbiol 2013; 62: 249-253.
16. Motallebirad T, Fazeli H, Jalalifar S, Shokri D, Moghim S, Nasr Esfahani B. Molecular Characterization of Hospital- and community-acquired Streptococcus agalactiae isolates among nonpregnant adults in Isfahan, Iran. Adv Biomed Res 2020; 9: 44.
17. Zhang L, Ma L, Zhu L, Zhou X-H, Xu L-J, Guo C, et al. Molecular characterization of pathogenic group B streptococcus from a tertiary hospital in Shanxi, China: High incidence of sequence type 10 strains in infants/pregnant women. J Microbiol Immunol Infect 2021; 54: 1094-1100.
18. Lin E, Zou S, Wang Y, Lee C-C, Chiu C-H, Feng Y. Phylogeny, recombination, and invasiveness of group B Streptococcus revealed by genomic comparisons of its global strains. Eur J Clin Microbiol Infect Dis 2021; 40: 581-590.
19. Moliva MV, Cerioli F, Reinoso EB. Evaluation of environmental and nutritional factors and sua gene on in vitro biofilm formation of Streptococcus uberis isolates. Microb Pathog 2017; 107: 144-148.
20. Lazzarin M, Mu R, Fabbrini M, Ghezzo C, Rinaudo CD, Doran KS, et al. Contribution of pilus type 2b to invasive disease caused by a Streptococcus agalactiae ST-17 strain. BMC Microbiol 2017; 17: 148.
21. 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. Microb Pathog 2018; 116: 189-194.
22. Martins ER, Pedroso-Roussado C, Melo-Cristino J, Ramirez M. Streptococcus agalactiae causing neonatal infections in portugal (2005–2015): Diversification and emergence of a CC17/PI-2b multidrug resistant sublineage. Front Microbiol 2017; 8: 499.
23. Gizachew M, Tiruneh M, Moges F, Tessema B. Streptococcus agalactiae maternal colonization, antibiotic resistance and serotype profiles in Africa: a meta-analysis. Ann Clin Microbiol Antimicrob 2019; 18: 14.
24. Bolukaoto JY, Monyama CM, Chukwu MO, Lekala SM, Nchabeleng M, Maloba MR, et al. Antibiotic resistance of Streptococcus agalactiae isolated from pregnant women in Garankuwa, South Africa. BMC Res Notes 2015; 8: 364.
25. Dhudasia MB, Flannery DD, Pfeifer MR, Puopolo KM. Updated guidance: prevention and management of perinatal Group B Streptococcus infection. Neoreviews 2021; 22(3): e177-e188.
26. Otaguiri ES, Morguette AE, Tavares ER, dos Santos PM, Morey AT, Cardoso JD, et al. Commensal Streptococcus agalactiae isolated from patients seen at University Hospital of Londrina, Paraná, Brazil: capsular types, genotyping, antimicrobial susceptibility and virulence determinants. BMC Microbiol 2013; 13: 297.
27. Hayes K, O’Halloran F, Cotter L. A review of antibiotic resistance in Group B Streptococcus: the story so far. Crit Rev Microbiol 2020; 46: 253-269.
28. van der Linden M, Mamede R, Levina N, Helwig P, Vila-Cerqueira P, Carriço JA, et al. Heterogeneity of penicillin-non-susceptible group B streptococci isolated from a single patient in Germany. J Antimicrob Chemother 2020; 75: 296-299.
2. 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 2020; 39: 2387-2396.
3. Ali MM, Woldeamanuel Y, Asrat D, Fenta DA, Beall B, Schrag S, et al. Features of Streptococcus agalactiae strains recovered from pregnant women and newborns attending different hospitals in Ethiopia. BMC Infect Dis 2020; 20: 848.
4. Bobadilla FJ, Novosak MG, Cortese IJ, Delgado OD, Laczeski ME. Prevalence, serotypes and virulence genes of Streptococcus agalactiae isolated from pregnant women with 35–37 weeks of gestation. BMC Infect Dis 2021; 21: 73.
5. Jalalifar S, Havaei SA, Motallebirad T, Moghim S, Fazeli H, Esfahani BN. 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 2019; 12:437.
6. Sadeh M, Firouzi R, Derakhshandeh A, Khalili MB, Kong F, Kudinha T. Molecular characterization of Streptococcus agalactiae isolates from pregnant and non-pregnant women at Yazd University Hospital, Iran. Jundishapur J Microbiol 2016; 9(2): e30412.
7. Shadbad MA, Kafil HS, Rezaee MA, Farzami MR, Dehkharghani AD, Sadeghi J, et al. Filament genes and biofilm formation in Streptococcus agalactiae. Rev Med Microbiol 2020; 31: 17-25.
8. Nabavinia M, Bagher Khalili M, Sadeh M, Eslami G, Vakili M, Azartoos N, et al. Distribution of Pilus island and antibiotic resistance genes in Streptococcus agalactiae obtained from vagina of pregnant women in Yazd, Iran. Iran J Microbiol 2020; 12: 411-416.
9. Emaneini M, Mirsalehian A, Beigvierdi R, Fooladi AAI, Asadi F, Jabalameli F, et al. High incidence of macrolide and tetracycline resistance among Streptococcus agalactiae strains isolated from clinical samples in Tehran, Iran. Maedica (Bucur) 2014; 9: 157-161.
10. Martins ER, Melo-Cristino J, Ramirez M. Evidence for rare capsular switching in Streptococcus agalactiae. J Bacteriol 2010; 192: 1361-1369.
11. Clinical, Institute LS. Performance standards for antimicrobial susceptibility testing. Clinical and Laboratory Standards Institute Wayne, PA; 2018.
12. Desai D, Goh KGK, Sullivan MJ, Chattopadhyay D, Ulett GC. Hemolytic activity and biofilm-formation among clinical isolates of group B streptococcus causing acute urinary tract infection and asymptomatic bacteriuria. Int J Med Microbiol 2021; 311: 151520.
13. Springman AC, Lacher DW, Waymire EA, Wengert SL, Singh P, Zadoks RN, et al. Pilus distribution among lineages of group b streptococcus: an evolutionary and clinical perspective. BMC Microbiol 2014; 14: 159.
14. Shadbad MA, Kafil HS, Rezaee MA, Farzami MR, Dehkharghani AD, Sadeghi J, et al. Streptococcus agalactiae clinical isolates in Northwest Iran: antibiotic susceptibility, molecular typing, and biofilm formation. GMS Hyg Infect Control 2020; 15: Doc23.
15. Madzivhandila M, Adrian PV, Cutland CL, Kuwanda L, Madhi SA, Team PT. Distribution of pilus islands of group B streptococcus associated with maternal colonization and invasive disease in South Africa. J Med Microbiol 2013; 62: 249-253.
16. Motallebirad T, Fazeli H, Jalalifar S, Shokri D, Moghim S, Nasr Esfahani B. Molecular Characterization of Hospital- and community-acquired Streptococcus agalactiae isolates among nonpregnant adults in Isfahan, Iran. Adv Biomed Res 2020; 9: 44.
17. Zhang L, Ma L, Zhu L, Zhou X-H, Xu L-J, Guo C, et al. Molecular characterization of pathogenic group B streptococcus from a tertiary hospital in Shanxi, China: High incidence of sequence type 10 strains in infants/pregnant women. J Microbiol Immunol Infect 2021; 54: 1094-1100.
18. Lin E, Zou S, Wang Y, Lee C-C, Chiu C-H, Feng Y. Phylogeny, recombination, and invasiveness of group B Streptococcus revealed by genomic comparisons of its global strains. Eur J Clin Microbiol Infect Dis 2021; 40: 581-590.
19. Moliva MV, Cerioli F, Reinoso EB. Evaluation of environmental and nutritional factors and sua gene on in vitro biofilm formation of Streptococcus uberis isolates. Microb Pathog 2017; 107: 144-148.
20. Lazzarin M, Mu R, Fabbrini M, Ghezzo C, Rinaudo CD, Doran KS, et al. Contribution of pilus type 2b to invasive disease caused by a Streptococcus agalactiae ST-17 strain. BMC Microbiol 2017; 17: 148.
21. 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. Microb Pathog 2018; 116: 189-194.
22. Martins ER, Pedroso-Roussado C, Melo-Cristino J, Ramirez M. Streptococcus agalactiae causing neonatal infections in portugal (2005–2015): Diversification and emergence of a CC17/PI-2b multidrug resistant sublineage. Front Microbiol 2017; 8: 499.
23. Gizachew M, Tiruneh M, Moges F, Tessema B. Streptococcus agalactiae maternal colonization, antibiotic resistance and serotype profiles in Africa: a meta-analysis. Ann Clin Microbiol Antimicrob 2019; 18: 14.
24. Bolukaoto JY, Monyama CM, Chukwu MO, Lekala SM, Nchabeleng M, Maloba MR, et al. Antibiotic resistance of Streptococcus agalactiae isolated from pregnant women in Garankuwa, South Africa. BMC Res Notes 2015; 8: 364.
25. Dhudasia MB, Flannery DD, Pfeifer MR, Puopolo KM. Updated guidance: prevention and management of perinatal Group B Streptococcus infection. Neoreviews 2021; 22(3): e177-e188.
26. Otaguiri ES, Morguette AE, Tavares ER, dos Santos PM, Morey AT, Cardoso JD, et al. Commensal Streptococcus agalactiae isolated from patients seen at University Hospital of Londrina, Paraná, Brazil: capsular types, genotyping, antimicrobial susceptibility and virulence determinants. BMC Microbiol 2013; 13: 297.
27. Hayes K, O’Halloran F, Cotter L. A review of antibiotic resistance in Group B Streptococcus: the story so far. Crit Rev Microbiol 2020; 46: 253-269.
28. van der Linden M, Mamede R, Levina N, Helwig P, Vila-Cerqueira P, Carriço JA, et al. Heterogeneity of penicillin-non-susceptible group B streptococci isolated from a single patient in Germany. J Antimicrob Chemother 2020; 75: 296-299.
| Files | ||
| Issue | Vol 15 No 2 (2023) | |
| Section | Original Article(s) | |
| DOI | https://doi.org/10.18502/ijm.v15i2.12473 | |
| Keywords | ||
| Group B Streptococcus; Pregnant women; Bacterial pili; Antibiotic resistance; Urine; Streptococcus agalactiae | ||
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This work is licensed under a Creative Commons Attribution-NonCommercial 4.0 International License. |
How to Cite
1.
Panahi S, Khalili MB, Sadeh M, Vakili M. Determination of pilus-islands profile and antibiotic susceptibility of Streptococcus agalactiae isolated from urine of pregnant women. Iran J Microbiol. 2023;15(2):219-224.
