Distribution of Pilus island and antibiotic resistance genes in Streptococcus agalactiae obtained from vagina of pregnant women in Yazd, Iran
-
Mahdieh Nabavinia
,
Mohammad Bagher Khalili
,
Maryam sadeh
,
Gilda Eslami
,
Mahmood Vakili
,
Nastaran Azartoos
,
Mahdiye Mojibiyan
Abstract
Background and Objectives: Due to important role of Streptococcus agalactiae, Group B streptococci (GBS), in production of invasive disease in neonates, investigation regarding the pathogenicity and antibiotic resistance factors is necessary in selecting the appropriate therapeutic agents. Beside capsule, the pilus has been currently recognized as an important factor in enhancing the pathogenicity of GBS. Resistance of GBS to selected antibiotics is noticeably increasing which is mainly due to the anomalous use of these drugs for treatment. The aim of this study was to determine the prevalence of pili genes followed by antibiotic susceptibility of GBS, previously serotyped, isolated from pregnant women in the city of Yazd, Iran.
Materials and Methods: Fifty seven GBS from pregnant women were subjected to multiplex PCR for determination of PI-1, PI-2a and PI-2b pilus-islands and simultaneously, the phenotype of antibiotic resistance to penicillin, tetracycline, erythromycin, clindamycin, gentamycin and levofloxacin was determined. Antibiotic resistance genes (ermA, ermB, mefA, tetM, int-Tn) were further diagnosed using PCR and multiplex PCR.
Results: PI-1+PI-2a with 71.9%; followed by PI-2a (21.1%) and PI-2b (7%) were observed. PI-1+PI-2a in serotype III was (73.2%), serotype II, Ia, Ib and V were 12.2%, 9.8%, 2.4% and 2.4% respectively. GBS penicillin sensitive was 89.5% and 96.5% resistance to Tetracycline. The frequency of resistance genes were as follows: tetM (93%), ermA (33.3%), ermB (8.8%), int-Tn (80.7%) and mefA (0).
Conclusion: Majority of GBS contained PI-1+PI-2a. Hence presence of this pilus stabilizes the colonization, therefore designing a program for diagnosing and treatment of infected pregnant women seems to be necessary.
1. 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.
2. 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.
3. Manshadi SAD, Alizadeh R, Salehi M, Seifi A, Seifi M. Bilateral septic arthritis of the knee caused by group B streptococci: a case report. Iran J Microbiol 2019;11:187-190.
4. Najarian N, Khalili MB, Astani A, Vakili M, Sadeh M. Serotype determination of Streptococcus agalactiae detected from vagina and urine of pregnant women in Yazd, Iran-2015. IJML 2018;5:49-57.
5. Nazari A, Khalili MB, Astani A, Vakili M, Sadeh M, Mojibiyan M, et al. Determination of genotypes of Streptococcus agalactiae isolated from both urine and vagina of pregnant women referred to gynecology clinics of Yazd, Iran-2015. IJML 2017;4:180-188.
6. Dehbashi S, Pourmand MR, Mashhadi R. Characterization of Afb, a novel bifunctional protein in Streptococcus agalactiae. Iran J Microbiol 2016;8:73-79.
7. Heath PT, Balfour GF, Tighe H, Verlander NQ, Lamagni TL, Efstratiou A, et al. Group B streptococcal disease in infants: a case control study. Arch Dis Child 2009;94:674-680.
8. Tamura G, Kuypers J, Smith S, Raff H, Rubens C. Adherence of group B streptococci to cultured epithelial cells: roles of environmental factors and bacterial surface components. Infect Immun 1994;62:2450-2458.
9. Wessels MR, Rubens CE, Benedi VJ, Kasper DL. Definition of a bacterial virulence factor: sialylation of the group B streptococcal capsule. Proc Natl Acad Sci U S A 1989;86:8983-8987.
10. Imperi M, Pataracchia M, Alfarone G, Baldassarri L, Orefici G, Creti R. A multiplex PCR assay for the direct identification of the capsular type (Ia to IX) of Streptococcus agalactiae. J Microbiol Methods 2010;80:212-214.
11. Hanh TQ, Van Du V, Hien PT, Chinh DD, Loi CB, Dung NM, et al. Prevalence and capsular type distribution of group B Streptococcus isolated from vagina of pregnant women in Nghe An province, Vietnam. Iran J Microbiol 2020;12:11-17.
12. Vengadesan K, Ma X, Dwivedi P, Ton-That H, Narayana SV. A model for group B Streptococcus pilus type 1: the structure of a 35-kDa C-terminal fragment of the major pilin GBS80. J Mol Biol 2011;407:731-743.
13. Sharma P, Lata H, Arya DK, Kashyap AK, Kumar H, Dua M, et al. Role of pilus proteins in adherence and invasion of Streptococcus agalactiae to the lung and cervical epithelial cells. J Biol Chem 2013;288:4023-4034.
14. 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.
15. Martins ER, Melo-Cristino J, Ramirez M. Evidence for rare capsular switching in Streptococcus agalactiae. J Bacteriol 2010;192:1361-1369.
16. Phares C, Lynfield R, Farley M, Mohle-Boetani J, Harrison L, Petit S, et al. Epidemiology of invasive group B streptococcal disease in the United States, 1999-2005. JAMA 2008;299:2056-2065.
17. Wang YH, Su LH, Hou JN, Yang TH, Lin TY, Chu C, et al. Group B streptococcal disease in nonpregnant patients: emergence of highly resistant strains of serotype Ib in Taiwan in 2006 to 2008. J Clin Microbiol 2010;48:2571-2574.
18. Gherardi G, Imperi M, Baldassarri L, Pataracchia M, Alfarone G, Recchia S, et al. Molecular epidemiology and distribution of serotypes, surface proteins, and antibiotic resistance among Group B streptococci in Italy. J Clin Microbiol 2007;45:2909-2916.
19. Sadowy E, Matynia B, Hryniewicz W. Population structure, virulence factors and resistance determinants of invasive, non-invasive and colonizing Streptococcus agalactiae in Poland. J Antimicrob Chemother 2010;65:1907-1914.
20. Daramroodi AK, Keshavarzi F, Raissi F. The investigation of antibiotic resistance and rapid detection of group B Streptococcus (Bca) from vaginal specimens of pregnant women by colony PCR method. J Bas Res Med Sci 2018; 5:27-32.
21. Clinical and Laboratory Standards Institute (CLSI). Performance Standards for Antimicrobial Susceptibility Testing: Approved Twenty-: Document M100-S28. Wayne, PA, USA: CLSI 2018.
22. Poyart C, Jardy L, Quesne G, Berche P, Trieu-Cuot P. Genetic basis of antibiotic resistance in Streptococcus agalactiae strains isolated in a French hospital. Antimicrob Agents Chemother 2003;47:794-797.
23. Lu B, Chen X, Wang J, Wang D, Zeng J, Li Y, et al. Molecular characteristics and antimicrobial resistance in invasive and noninvasive Group B Streptococcus between 2008 and 2015 in China. Diagn Microbiol Infect Dis 2016;86:351-357.
24. Margarit I, Rinaudo CD, Galeotti CL, Maione D, Ghezzo C, Buttazzoni E, et al. Preventing bacterial infections with pilus-based vaccines: the group B streptococcus paradigm. J Infect Dis 2009;199:108-115.
25. Xia FD, Mallet A, Caliot E, Gao C, Trieu-Cuot P, Dramsi S. Capsular polysaccharide of Group B Streptococcus mediates biofilm formation in the presence of human plasma. Microbes Infect 2015;17:71-76.
26. DeLeo FR, Rinaudo CD, Rosini R, Galeotti CL, Berti F, Necchi F, et al. Specific involvement of Pilus type 2a in biofilm formation in Group B Streptococcus. PLoS One 2010;5(2): e9216.
27. Martins E, Andreu A, Melo-Cristino J, Ramirez M. Distribution of Pilus Islands in Streptococcus agalactiae that cause human infections: insights into evolution and implication for vaccine development. Clin Vaccine Immunol 2013;20:313-316.
28. 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.
29. Madzivhandila M, Adrian PV, Cutland CL, Kuwanda L, Madhi SA, The Po PSTT. 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.
30. 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.
31. Ghanbarzadeh N, Mehramiz M, Gannadkafi M, Namaei MH. The prevalence of group B streptococcus rectovaginal colonization and antimicrobial susceptibility pattern among pregnant women: a descriptive-analytical study. Mod Care J 2017;14(3):e66391.
32. 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.
33. Martins ER, Pedroso-Roussado C, Melo-Cristino J, Ramirez M, The 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 2017;8:499.
34. Heelan JS, Hasenbein ME, McAdam AJ. Resistance of group B Streptococcus to selected antibiotics, including erythromycin and clindamycin. J Clin Microbiol 2004;42:1263-1264.
2. 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.
3. Manshadi SAD, Alizadeh R, Salehi M, Seifi A, Seifi M. Bilateral septic arthritis of the knee caused by group B streptococci: a case report. Iran J Microbiol 2019;11:187-190.
4. Najarian N, Khalili MB, Astani A, Vakili M, Sadeh M. Serotype determination of Streptococcus agalactiae detected from vagina and urine of pregnant women in Yazd, Iran-2015. IJML 2018;5:49-57.
5. Nazari A, Khalili MB, Astani A, Vakili M, Sadeh M, Mojibiyan M, et al. Determination of genotypes of Streptococcus agalactiae isolated from both urine and vagina of pregnant women referred to gynecology clinics of Yazd, Iran-2015. IJML 2017;4:180-188.
6. Dehbashi S, Pourmand MR, Mashhadi R. Characterization of Afb, a novel bifunctional protein in Streptococcus agalactiae. Iran J Microbiol 2016;8:73-79.
7. Heath PT, Balfour GF, Tighe H, Verlander NQ, Lamagni TL, Efstratiou A, et al. Group B streptococcal disease in infants: a case control study. Arch Dis Child 2009;94:674-680.
8. Tamura G, Kuypers J, Smith S, Raff H, Rubens C. Adherence of group B streptococci to cultured epithelial cells: roles of environmental factors and bacterial surface components. Infect Immun 1994;62:2450-2458.
9. Wessels MR, Rubens CE, Benedi VJ, Kasper DL. Definition of a bacterial virulence factor: sialylation of the group B streptococcal capsule. Proc Natl Acad Sci U S A 1989;86:8983-8987.
10. Imperi M, Pataracchia M, Alfarone G, Baldassarri L, Orefici G, Creti R. A multiplex PCR assay for the direct identification of the capsular type (Ia to IX) of Streptococcus agalactiae. J Microbiol Methods 2010;80:212-214.
11. Hanh TQ, Van Du V, Hien PT, Chinh DD, Loi CB, Dung NM, et al. Prevalence and capsular type distribution of group B Streptococcus isolated from vagina of pregnant women in Nghe An province, Vietnam. Iran J Microbiol 2020;12:11-17.
12. Vengadesan K, Ma X, Dwivedi P, Ton-That H, Narayana SV. A model for group B Streptococcus pilus type 1: the structure of a 35-kDa C-terminal fragment of the major pilin GBS80. J Mol Biol 2011;407:731-743.
13. Sharma P, Lata H, Arya DK, Kashyap AK, Kumar H, Dua M, et al. Role of pilus proteins in adherence and invasion of Streptococcus agalactiae to the lung and cervical epithelial cells. J Biol Chem 2013;288:4023-4034.
14. 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.
15. Martins ER, Melo-Cristino J, Ramirez M. Evidence for rare capsular switching in Streptococcus agalactiae. J Bacteriol 2010;192:1361-1369.
16. Phares C, Lynfield R, Farley M, Mohle-Boetani J, Harrison L, Petit S, et al. Epidemiology of invasive group B streptococcal disease in the United States, 1999-2005. JAMA 2008;299:2056-2065.
17. Wang YH, Su LH, Hou JN, Yang TH, Lin TY, Chu C, et al. Group B streptococcal disease in nonpregnant patients: emergence of highly resistant strains of serotype Ib in Taiwan in 2006 to 2008. J Clin Microbiol 2010;48:2571-2574.
18. Gherardi G, Imperi M, Baldassarri L, Pataracchia M, Alfarone G, Recchia S, et al. Molecular epidemiology and distribution of serotypes, surface proteins, and antibiotic resistance among Group B streptococci in Italy. J Clin Microbiol 2007;45:2909-2916.
19. Sadowy E, Matynia B, Hryniewicz W. Population structure, virulence factors and resistance determinants of invasive, non-invasive and colonizing Streptococcus agalactiae in Poland. J Antimicrob Chemother 2010;65:1907-1914.
20. Daramroodi AK, Keshavarzi F, Raissi F. The investigation of antibiotic resistance and rapid detection of group B Streptococcus (Bca) from vaginal specimens of pregnant women by colony PCR method. J Bas Res Med Sci 2018; 5:27-32.
21. Clinical and Laboratory Standards Institute (CLSI). Performance Standards for Antimicrobial Susceptibility Testing: Approved Twenty-: Document M100-S28. Wayne, PA, USA: CLSI 2018.
22. Poyart C, Jardy L, Quesne G, Berche P, Trieu-Cuot P. Genetic basis of antibiotic resistance in Streptococcus agalactiae strains isolated in a French hospital. Antimicrob Agents Chemother 2003;47:794-797.
23. Lu B, Chen X, Wang J, Wang D, Zeng J, Li Y, et al. Molecular characteristics and antimicrobial resistance in invasive and noninvasive Group B Streptococcus between 2008 and 2015 in China. Diagn Microbiol Infect Dis 2016;86:351-357.
24. Margarit I, Rinaudo CD, Galeotti CL, Maione D, Ghezzo C, Buttazzoni E, et al. Preventing bacterial infections with pilus-based vaccines: the group B streptococcus paradigm. J Infect Dis 2009;199:108-115.
25. Xia FD, Mallet A, Caliot E, Gao C, Trieu-Cuot P, Dramsi S. Capsular polysaccharide of Group B Streptococcus mediates biofilm formation in the presence of human plasma. Microbes Infect 2015;17:71-76.
26. DeLeo FR, Rinaudo CD, Rosini R, Galeotti CL, Berti F, Necchi F, et al. Specific involvement of Pilus type 2a in biofilm formation in Group B Streptococcus. PLoS One 2010;5(2): e9216.
27. Martins E, Andreu A, Melo-Cristino J, Ramirez M. Distribution of Pilus Islands in Streptococcus agalactiae that cause human infections: insights into evolution and implication for vaccine development. Clin Vaccine Immunol 2013;20:313-316.
28. 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.
29. Madzivhandila M, Adrian PV, Cutland CL, Kuwanda L, Madhi SA, The Po PSTT. 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.
30. 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.
31. Ghanbarzadeh N, Mehramiz M, Gannadkafi M, Namaei MH. The prevalence of group B streptococcus rectovaginal colonization and antimicrobial susceptibility pattern among pregnant women: a descriptive-analytical study. Mod Care J 2017;14(3):e66391.
32. 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.
33. Martins ER, Pedroso-Roussado C, Melo-Cristino J, Ramirez M, The 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 2017;8:499.
34. Heelan JS, Hasenbein ME, McAdam AJ. Resistance of group B Streptococcus to selected antibiotics, including erythromycin and clindamycin. J Clin Microbiol 2004;42:1263-1264.
| Files | ||
| Issue | Vol 12 No 5 (2020) | |
| Section | Original Article(s) | |
| DOI | https://doi.org/10.18502/ijm.v12i5.4601 | |
| Keywords | ||
| Streptococcus agalactiae; Pili; Antibiogram; Women; Yazd | ||
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This work is licensed under a Creative Commons Attribution-NonCommercial 4.0 International License. |
How to Cite
1.
Nabavinia M, Khalili MB, sadeh M, Eslami G, Vakili M, Azartoos N, Mojibiyan M. 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(5):411-416.
