Resistance Rates of Streptococcus agalactiae Strains Isolated from Urine Samples to Various Antibiotics

Abstract

Aim: Group B Streptococcus (GBS), also known as Streptococcus agalactiae, are Gram-positive, encapsulated bacteria found in the normal human gastrointestinal and urogenital flora. A wide variety of infectious diseases can cause urogenital system infections in newborns, elderly people, immunocompromised people, pregnant women, and adults. In this study, we aimed to inform clinicians about the agents that can be used in intrapartum antibiotic prophylaxis by examining the antibiotic susceptibility of GBS strains isolated from urine samples from the Gynecology and Obstetrics Clinic in our laboratory. Material and Methods: Isolates of the S. agalactiae isolated from a total of 222 urine samples from the Gynecology and Obstetrics Clinic that came to our Medical Microbiology laboratory between January 2022 and December 2022 were included and the data of these isolates were evaluated retrospectively. The clinical samples that came to our laboratory were inoculated on Sheep blood agar medium and incubated at 37°C for 18-24 hours. Quantitatively seeded urine culture ≥104 CFU/ml grown bacteria was considered a uropathogenic. Urogenital skin flora element or three and more different types of bacteria growing cultures as contamination evaluated. Results: Due to the group selected as the sample, 100% of the patients were female. The age range of the patients ranged from 12 to 72, and the mean age was calculated as 30.16. All GBS isolates were susceptible to penicillin, linezolid, trimethoprim-sulfamethoxazole, tigecycline, teicoplanin, and vancomycin. Conclusion: Penicillin resistance was not found in our study. However, resistant strains were detected in erythromycin, clindamycin, and levofloxacin, which stand out as other options in cases where penicillin cannot be used.

Keywords

• Group B streptococcus
• penicillin
• antimicrobial susceptibility

İdrar Örneklerinden İzole Edilen Streptococcus agalactiae suşlarının Çeşitli Antibiyotiklere Direnç Oranları

Abstract

Amaç: Streptococcus agalactiae olarak da bilinen Grup B Streptokoklar (GBS) insan normal gastrointestinal ve ürogenital florasında bulunan Gram pozitif, kapsüllü bakterilerdir. Yenidoğanlarda, yaşlılarda, bağışıklığı baskılanmış kişilerde çok çeşitli bulaşıcı hastalıklar kişilerde, gebelerde ve erişkinlerde ürogenital sistem enfeksiyonlarına neden olabilirler. Bu çalışmada Kadın Hastalıkları ve Doğum Kliniği'nden laboratuvarımıza gelen idrar örneklerinden izole edilen GBS suşlarının antibiyotik duyarlılıklarını inceleyerek intrapartum antibiyotik profilaksisinde kullanılabilecek ajanlar hakkında klinisyenleri bilgilendirmek amaçlandı. Gereç ve Yöntemler: Ocak 2022- Aralık 2022 yılları arasında Kadın Hastalıkları ve Doğum Kliniği'nden Tıbbi Mikrobiyoloji laboratuvarımıza gönderilen toplam 222 klinik idrar örneğinden izole edilen S. agalactiae izolatları dahil edildi ve bu izolatlara ait veriler retrospektif olarak değerlendirildi. Laboratuvarımıza gelen klinik örnekler Koyun kanlı agar besiyerine ekildi ve 37°C'de 18-24 saat inkübe edildi. Kantitatif olarak ekim yapılan idrar kültüründe ≥104 CFU/ml üremesi olan bakteriler üropatojen olarak kabul edilirken ürogenital cilt flora elemanı veya üç ve daha fazla farklı tipte bakteri üreyen kültürler kontaminasyon olarak değerlendirildi. Bulgular: Seçilen hasta grubu nedeniyle hastaların %100’ü kadındı. Hastaların yaşları 12 ile 72 arasında değişirken yaş ortalaması ise 30,16’ydı. GBS izolatlarının tümü penisilin, linezolid, trimetoprim sulfametoksazol, tigesiklin, teikoplanin ve vankomisine duyarlıydı. Sonuç: Çalışmamızda penisilin direnci saptanmamıştır. Ancak penisilinin kullanılamadığı durumlarda diğer seçenekler olarak öne çıkan eritromisin, klindamisin ve levofloksasine dirençli suşlar tespit edilmiştir.

Keywords

• Grup B streptokok
• penisilin
• antimikrobiyal duyarlılık

References

1. 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, Parana,Brazil: Capsular types, genotyping, antimicrobial susceptibility and virulence determinants. BMC Microbiol. 2013; 13: 297. https://doi.org/10.1186/1471-2180-13-297
2. Hays C, Louis M, Plainvert C, et al. Changing epidemiology of Group B Streptococcus susceptibility to fluoroquinolones and aminoglycosides in France. Antimicrob Agents Chemother. 2016; 60(12): 7424-30. https://doi.org/10.1128/AAC.01374-16
3. Wang YH, Chen HM, Yang YH, Yang TH, Teng CH, Chen CL, et al. Clinical and microbiological characteristics of recurrent group B streptococcal infection among non-pregnant adults. Int J Infect Dis. 2014; 26: 140-5. https://doi.org/10.1016/j.ijid.2014.05.026
4. Aracil B, Minambres M, Oteo J, De La Rosa M, GomezGarces JL, Alos AJ. Susceptibility of strains of Streptococcus agalactiae to macrolides and lincosamides, phenotype patterns and resistance genes. Clin Microbiol Infect. 2002; 8(11): 745-8. https://doi.org/10.1046/j.1469-0691.2002.00450.x
5. 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. https://doi.org/10.1186/s12879-020-05581-8
6. El Aila NA, Tency I, Claeys G, Saerens B, Cools P, Verstraelen H, et al. Comparison of different sampling techniques and of different culture methods for detection of group B streptococcus carriage inpregnant women. BMC Infect. Dis. 2010; 10: 285. https://doi.org/10.1186/1471-2334-10-285
7. Joachim A, Matee MI, Massawe FA, Lyamuya EF. Maternal and neonatal colonisation of group B streptococcus at Muhimbili National Hospital in Dar es Salaam, Tanzania: Prevalence, risk factors and antimicrobial resistance. BMC Public Health. 2009; 9: 437. https://doi.org/10.1186/1471-2458-9-437
8. Dipersio LP, Dipersio JR. Identification of an erm(T) gene in strains of inducibly clindamycin-resistant group B Streptococcus. Diagn. Microbiol. Infect. Dis. 2007; 57,: 189-93. https://doi.org/10.1016/j.diagmicrobio.2006.07.013

9. Verani JR, McGee L, Schrag SJ. Prevention of perinatal group B streptococcal disease–revised guidelines from CDC, MMWR Recommendations and reports: Morbidity and mortality weekly report Recommendations and reports. CDC Recomm. Rep. 2010; 59: 1-32.
10. Hays C, Louis M, Plainvert C, Dmytruk N, Touak G, Trieu-Cuot P, et al. Changing epidemiology of Group B Streptococcus susceptibility to fluoroquinolones and aminoglycosides in France. Antimicrob Agents Chemother. 2016; 60(12): 7424-30. https://doi.org/10.1128/AAC.01374-16
11. Kimura K, Suzuki S, Wachino J, Kurokawa H, Yamane K, Shibata N, et al. First molecular characterization of group B streptococci with reduced penicillin susceptibility. Antimicrob Agents Chemother. 2008; 52(8): 2890-7. https://doi.org/10.1128/AAC.00185-08
12. Nakamura PA, Schuab RB, Neves FP, Pereira CF, Paula GR, Barros RR. Antimicrobial resistance profiles and genetic characterisation of macrolide resistant isolates of Streptococcus agalactiae. Mem Inst Oswaldo Cruz. 2011; 106(2): 119-22. https://doi.org/10.1590/s0074-02762011000200001
13. Atalay A, Olcu M, Perçin D. Antibiotic susceptibilities and serotyping of clinical Streptococcus agalactiae isolates. Balkan Med J. 2010; 28: 362-5. https://doi.org/10.5174/tutfd.2010.03979.2
14. Otaguiri ES, Morguette AEB, Morey AT, Tavares ER, Kerbauy G, de Almeida Torres RSL, et al. Development of a melting-curve based multiplex realtime PCR assay for simultaneous detection of Streptococcus agalactiae and genes encoding resistance to macrolides and lincosamides. BMC Pregnancy Childbirth. 2018; 18(1): 126. https://doi.org/10.1186/s12884-018-1774-5
15. Gygax SE, Schuyler JA, Kimmel LE, Trama JP, Mordechai E, Adelson ME. Erythromycin and clindamycin resistance ingroup B streptococcal clinical isolates. Antimicrob. Agents Chemother. 2006; 50: 1875-7. https://doi.org/10.1128/AAC.50.5.1875-1877.2006
16. 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. https://doi.org/10.1186/s12941-019-0313-1.
17. Nkembe NM, Kamga HG, Baiye WA, Chafa AB, Njotang PN. Streptococcus agalactiae prevalence and antimicrobial susceptibility pattern in vaginal and anorectal swabs of pregnant women at a tertiary hospital in Cameroon. BMC Res. Notes. 2018; 11: 480. https://doi.org/10.1186/s13104-018-3589-x
18. Baba S, Aydin MD. İdrar örneklerinden izole edilen Grup B streptokokların serotip dağılımı, biyofilm üretimi ve antibiyotik duyarlılıklarının araştırılması. Mikrobiyol Bul. 2016; 50(3): 353-60. https://doi.org/10.5578/mb.26466
19. Longtin J, Vermeiren C, Shahinas D, Tamber GS, McGeer A, Low DE, et al. Novel mutations in a patient isolate of Streptococcus agalactiae with reduced penicillin susceptibility emerging after long-term oral suppressive therapy. Antimicrob Agents Chemother. 2011; 55(6): 2983-5. https://doi.org/10.1128/AAC.01243-10
20. Betriu C, Gomez M, Sanchez A, Cruceyra A, Romero J, Picazzo J. Antibiotic resistance and penicillin tolerance in clinical isolates of group B streptococci. Antimicrob Agents Chemother 1994; 38: 2183-6. https://doi.org/10.1128/aac.38.9.2183
21. Nagano N, Nagano Y, Kimura K, Tamai K, Yanaqisawa H, Arakawa Y. Genetic heterogeneity in pbp genes among clinically isolated group B streptococci with reduced penicillin susceptibility. Antimicrob Agents Chemother. 2008; 52: 4258-67. https://doi.org/10.1128/AAC.00596-08
22. 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): 219-24. https://doi.org/10.18502/ijm.v15i2.12473
23. 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: 189-94. https://doi.org/10.1016/j.micpath.2018.01.035
24. Evren K, Yardibi Demir HA, Mutlu Sarıgüzel F, Dinç B. Klinik örneklerden izole edilen Streptococcus agalactiae izolatlarının antibiyotik duyarlılıkları. Türk Mikrobiyol Cemiy. Derg. (2021): 51(3); 239-44. https://doi.org/10.5222/TMCD.2021.71601
25. Yenişehirli G, Bulut Y, Demirtürk F, Çalışkan AC. Gebe kadınlardan izole edilen Streptococcus agalactiae suşlarının antimikrobiyal duyarlılıkları ve serotip dağılımı. Mikrobiyol Bül. 2006; 40: 155-60.
26. de Azavedo JC, M McGavin, C Duncan, D E Low, A McGeer. Prevalence and mechanisms of macrolide resistance in invasive and noninvasive group B streptococcus isolates from Ontario, Canada. Antimicrob Agents Chemother. 2001; 45: 3504-8.
27. Ko WC, Lee HC, Wang LR, Lee CT, Liu AJ, Wu JJ. Serotyping and antimicrobial susceptibility of group B streptococcus over an eight-year period in Southern Taiwan. Eur J Clin Microbiol Infect Dis. 2001; 20(5): 334-8.
28. Motlova J, Strakova L, Urbaskova P, Sak P, Sever T. Vaginal and rectal carriage of Streptococcus agalactiae in the Czech Republic: incidence, serotypes distribution and susceptibility to antibiotics. Indian J Med Res 2004; 119 suppl: 84-7.
29. Aracil B, Minambres M, Oteo J, De La Rosa M, GomezGarces JL, Alos AJ. Susceptibility of strains of Streptococcus agalactiae to macrolides and lincosamides, phenotype patterns and resistance genes. Clin Microbiol Infect. 2002; 8(11): 745-8. https://doi.org/10.1046/j.1469-0691.2002.00450.x
30. Leszczynski P, Sokol-Leszczynska B, Pietrzak B, SawickaGrzelak A, Wielgos M. Erythromycin or clindamycin - is it still an empirical therapy against Streptococcus agalactiae in patients allergic to penicillin? Pol J Microbiol. 2017; 66(2): 265-8. https://doi.org/10.5604/01.3001.0010.7878
31. Barros RR, de Souza AF, Luiz FBO. Polyclonal spread of Streptococcus agalactiae resistant to clindamycin among pregnant women in Brazil. J Antimicrob Chemother. 2016; 71(7): 2054-6. https://doi.org/10.1093/jac/dkw085
32. Berg BR, Houseman JL, terSteeg ZE, LeBar WD, Newton DW. Antimicrobial susceptibilities of group B streptococcus isolates from prenatal screening samples. J Clin Microbiol. 2014; 52(9): 3499-500. https://doi.org/10.1128/JCM.01781-14
33. Savcı Ü, Toprak S, Sungur M. Streptococcus agalactiae suşarının antimikrobiyal direnç paterni: beş yıllık tek merkez değerlendirmesi. J Health Sci Med. 2018; 1(2): 25-9.
34. Lee WT, Lai MC. High prevalence of Streptococcus agalactiae from vaginas of women in Taiwan and its mechanisms of macrolide and quinolone resistance. J Microbiol Immunol Infect. 2015; 48(5): 510-6. https://doi.org/10.1016/j.jmii.2014.03.002
35. Piccinelli G, Gargiulo F, Corbellini S, Ravizzola G, Bonfanti C, Caruso A, et al. Emergence of the first levofloxacin-resistant strains of Streptococcus agalactiae isolated in Italy. Antimicrob Agents Chemother. 2015; 59(4): 2466-9. https://doi.org/10.1128/AAC.05127-14
36. Ki M, Srinivasan U, Oh KY, Kim MY, Shin JH, Hong HL, Dang T, et al. Emerging fluoroquinolone resistance in Streptococcus agalactiae in South Korea. Eur J Clin Microbiol Infect Dis. 2012; 31(11): 3199-205. https://doi.org/10.1007/s10096-012-1685-8
37. Barros RR, Kegele FC, Paula GR, Brito MA, Duarte RS. Molecular characterization of the first fluoroquinolone resistant strains of Streptococcus agalactiae isolated in Brazil. Braz J Infect Dis. 2012; 16(5): 476-8. https://doi.org/10.1016/j.bjid.2012.05.003
38. Wang H, Zhao C, He W, Zhang F, Zhang L, Cao B, et al. High prevalence of fluoroquinolone-resistant group B streptococci among clinical isolates in China and predominance of sequence type 19 with serotype III. Antimicrob Agents Chemother. 2013; 57(3): 1538-41. https://doi.org/10.1128/AAC.02317-12