• 1.

    Raabe VN, Shane AL, Group B, 2019. Streptococcus (Streptococcus agalactiae). Microbiol Spectr 7: 718.

  • 2.

    Björnsdóttir ES et al., 2016. Changing epidemiology of group B streptococcal infections among adults in Iceland: 1975–2014. Clin Microbiol Infect 22: 379.e9379.e16.

    • Search Google Scholar
    • Export Citation
  • 3.

    Lee CC, Hsu JF, Janapatla RP, Chen C, Zhou YL, Lien R, Chiu CH, 2019. Clinical and microbiological characteristics of group B Streptococcus from pregnant women and diseased infants in intrapartum antibiotic prophylaxis era in Taiwan. Sci Rep 9: 13525.

    • Search Google Scholar
    • Export Citation
  • 4.

    Gizachew M, Tiruneh M, Moges F, Tessema B, 2019. Streptococcus agalactiae maternal colonization, antibiotic resistance and serotype profile in Africa: a metanalysis. Ann Clin Microbiol Antimicrob 18: 14.

    • Search Google Scholar
    • Export Citation
  • 5.

    Batista RP, Ferreira CR, 2015. Streptococcus agalactiae septicemia in a patient with diabetes. Autops Case Rep 5: 3543.

  • 6.

    Kwatra G, Adrian PV, Shiri T, Buchmann EJ, Cutland CL, Madhi SA, 2015. Natural acquired humoral immunity against serotype-specific group B Streptococcus rectovaginal colonization acquisition in pregnant women. Clin Microbiol Infect 21: 568.e13e568.e21.

    • Search Google Scholar
    • Export Citation
  • 7.

    Medugu N et al., 2017. Group B streptococcal colonization and transmission dynamics in pregnant women and their newborns in Nigeria: implications for prevention strategies. Clin Microbiol Infect 23: 673.e9673.e16.

    • Search Google Scholar
    • Export Citation
  • 8.

    Metcalf BJ et al., 2017. Short-read whole genome sequencing for determination of antimicrobial resistance mechanisms and capsular serotypes of current invasive Streptococcus agalactiae recovered in the USA. Clin Microbiol Infect 23: 574.e7574.e14.

    • Search Google Scholar
    • Export Citation
  • 9.

    American Diabetes Association , 2019. Standard of medical care in diabetes 2019. Diabetes Care 42: S4S6.

  • 10.

    Clinical and Laboratory Standards Institute , 2015. Performance Standards for Antimicrobial Susceptibility Testing: Twenty-fifth Informational Supplement. CLSI document M100-S25, vol. 35. Wayne, PA: Clinical and Laboratory Standards Institute.

    • Search Google Scholar
    • Export Citation
  • 11.

    Teatero S, Ferrieri P, Martin I, Demczuk W, McGeer A, Fittipaldi N, 2017. Serotype distribution, population structure, and antimicrobial resistance of group B Streptococcus strains recovered from colonized pregnant women. J Clin Microbiol 55: 412422.

    • Search Google Scholar
    • Export Citation
  • 12.

    Slotved HC, Kong F, Lambertsen L, Sauer S, Gilbert GL, 2007. Serotype IX, a proposed new Streptococcus agalactiae serotype. J Clin Microbiol 45: 29292936.

    • Search Google Scholar
    • Export Citation
  • 13.

    Yao K, Poulsen K, Maione D, Rinaudo CD, Baldassarri L, Telford JL, Sorensen UB, Kilian M, 2013. Capsular gene typing of Streptococcus agalactiae compared to serotyping by latex agglutination. J Clin Microbiol 51: 503507.

    • Search Google Scholar
    • Export Citation
  • 14.

    Shabayek S, Abdalla S, Abouzeid AM, 2014. Serotype and surface protein gene distribution of colonizing group B Streptococcus in women in Egypt. Epidemiol Infect 142: 208210.

    • Search Google Scholar
    • Export Citation
  • 15.

    Boswihi SS, Udo EE, Al-Sweih N, 2012. Serotypes and antibiotic resistance in group B Streptococcus isolated from patients at the Maternity Hospital, Kuwait. J Med Microbiol 61: 126131.

    • Search Google Scholar
    • Export Citation
  • 16.

    Ippolito DL et al., 2010. Group B Streptococcus serotype prevalence in reproductive-age women at a tertiary care military medical center relative to global serotype distribution. BMC Infect Dis 10: 336.

    • Search Google Scholar
    • Export Citation
  • 17.

    Lamagni TL et al., 2013. Emerging trends in the epidemiology of invasive group B streptococcal disease in England and Wales, 1991–2010. Clin Infect Dis 57: 682688.

    • Search Google Scholar
    • Export Citation
  • 18.

    Melin P, Efstratiou A, 2013. Group B streptococcal epidemiology and vaccine needs in developed countries. Vaccine 31: D31D42.

  • 19.

    Florindo C et al., 2014. Epidemiological surveillance of colonising group B Streptococcus epidemiology in the Lisbon and Tagus Valley regions, Portugal (2005 to 2012): emergence of a new epidemic type IV/clonal complex 17 clone. Euro Surveill 19: 20825.

    • Search Google Scholar
    • Export Citation
  • 20.

    Fabbrini M et al., 2016. The protective value of maternal group B Streptococcus antibodies: quantitative and functional analysis of naturally acquired responses to capsular polysaccharides and pilus proteins in European maternal sera. Clin Infect Dis 63: 746753.

    • Search Google Scholar
    • Export Citation
  • 21.

    Karunakaran R, Raja NS, Hafeez A, Puthucheary SD, 2009. Group B Streptococcus infection: epidemiology, serotypes, and antimicrobial susceptibility of selected isolates in the population beyond infancy (excluding females with genital tract- and pregnancy-related isolates) at the University Malaya Medical Centre, Kuala Lumpur. Jpn J Infect Dis 62: 192194.

    • Search Google Scholar
    • Export Citation
  • 22.

    Dhanoa A, Karunakaran R, Puthucheary SD, 2010. Serotype distribution and antibiotic susceptibility of group B streptococci in pregnant women. Epidemiol Infect 138: 979981.

    • Search Google Scholar
    • Export Citation
  • 23.

    Belard S et al., 2015. Streptococcus agalactiae serotype distribution and antimicrobial susceptibility in pregnant women in Gabon, Central Africa. Sci Rep 5: 17281.

    • Search Google Scholar
    • Export Citation
  • 24.

    Le Doare K, Jarju S, Darboe S, Warburton F, Gorringe A, Heath PT, Kampmann B, 2016. Risk factors for group B Streptococcus colonisation and disease in Gambian women and their infants. J Infect 72: 283294.

    • Search Google Scholar
    • Export Citation
  • 25.

    Tsai M, Hsu JF, Lai MY, Lin LC, Chu SM, Huang HR, Fu MR, Lu JJ, 2019. Molecular characteristics and antimicrobial resistance of group B Streptococcus strains causing invasive disease in neonates and adults. Front Microbiol 10: 264.

    • Search Google Scholar
    • Export Citation
  • 26.

    Matsubara K, Katayama K, Baba K, Nigami H, Harigaya H, Sugiyama M, 2002. Seroepidemiologic studies of serotype VIII group B Streptococcus. Jpn J Infect Dis 186: 855858.

    • Search Google Scholar
    • Export Citation
  • 27.

    Lin HC et al., 2016. Clonal dissemination of invasive and colonizing clonal complex 1 of serotype VI group B Streptococcus in central Taiwan. J Microbiol Immunol Infect 49: 902909.

    • Search Google Scholar
    • Export Citation
  • 28.

    Ji W et al., 2017. Colonization prevalence and antibiotic susceptibility of group B Streptococcus in pregnant women over a 6-year period in Dongguan, China. PLoS One 12: e0183083.

    • Search Google Scholar
    • Export Citation
  • 29.

    Lu B, Li D, Cui Y, Sui W, Huang L, Lu X, 2014. Epidemiology of group B Streptococcus isolated from pregnant women in Beijing, China. Clin Microbiol Infect 20: O370O373.

    • Search Google Scholar
    • Export Citation
  • 30.

    Kwatra G, Adrian PV, Shiri T, Buchmann EJ, Cutland CL, Madhi SA, 2014. Serotype-specific acquisition and loss of group B Streptococcus recto-vaginal colonization in late pregnancy. PLoS One 9: e98778.

    • Search Google Scholar
    • Export Citation
  • 31.

    Davies HD et al., 2001. Antibodies to capsular polysaccharides of group B Streptococcus in pregnant Canadian women: relationship to colonization status and infection in the neonate. J Infect Dis 184: 285291.

    • Search Google Scholar
    • Export Citation
  • 32.

    Kunze M, Ziegler A, Fluegge K, Hentschel R, Proempeler H, Berner R, 2011. Colonization, serotypes and transmission rates of group B streptococci in pregnant women and their infants born at a single university center in Germany. J Perinat Med 39: 417422.

    • Search Google Scholar
    • Export Citation
  • 33.

    Madhi SA et al., 2013. Considerations for a phase-III trial to evaluate a group B Streptococcus polysaccharide–protein conjugate vaccine in pregnant women for the prevention of early- and late-onset invasive disease in young infants. Vaccine 31: D52D57.

    • Search Google Scholar
    • Export Citation
  • 34.

    Ueno H, Yamamoto Y, Yamamichi A, Kikuchi K, Kobori S, Miyazaki M, 2012. Characterization of group B Streptococcus isolated from women in Saitama City, Japan. Jpn J Infect Dis 65: 516521.

    • Search Google Scholar
    • Export Citation
  • 35.

    Lee BK et al., 2010. Epidemiology of group B Streptococcus in Korean pregnant women. Epidemiol Infect 138: 292298.

  • 36.

    Castor ML et al., 2008. Antibiotic resistance patterns in invasive group B streptococcal isolates. Infect Dis Obstet Gynecol 2008: 727505.

  • 37.

    Dogan B, Schukken YH, Santisteban C, Boor KJ, 2005. Distribution of serotypes and antimicrobial resistance genes among Streptococcus agalactiae isolates from bovine and human hosts. J Clin Microbiol 43: 58995906.

    • Search Google Scholar
    • Export Citation
  • 38.

    Zhao Z, Kong F, Zeng X, Gidding HF, Morgan J, Gilbert GL, 2008. Distribution of genotypes and antibiotic resistance genes among invasive Streptococcus agalactiae (group B Streptococcus) isolates from Australasian patients belonging to different age groups. Clin Microbiol Infect 14: 260267.

    • Search Google Scholar
    • Export Citation
  • 39.

    Suara RO, Adegbola RA, Baker CJ, Secka O, Mulholland EK, Greenwood BM, 1994. Carriage of group B streptococci in pregnant Gambian mothers and their infants. J Infect Dis 170: 13161319.

    • Search Google Scholar
    • Export Citation
  • 40.

    Edmond KM et al., 2012. Group B streptococcal disease in infants aged younger than 3 months: systematic review and meta-analysis. Lancet 379: 547.

    • Search Google Scholar
    • Export Citation
  • 41.

    Meehan M, Cunney R, Cafferkey M, 2014. Molecular epidemiology of group B streptococci in Ireland reveals a diverse population with evidence of capsular switching. Eur J Clin Microbiol Infect Dis 33: 11551162.

    • Search Google Scholar
    • Export Citation
  • 42.

    Shabayek SA, Abdalla SM, Abouzeid AM, 2009. Vaginal carriage and antibiotic susceptibility profile of group B Streptococcus during late pregnancy in Ismailia. Egypt. J Infect Public Health 2: 8690.

    • Search Google Scholar
    • Export Citation
  • 43.

    Sadaka SM, Aly HA, Meheissen MA, Orief YI, Arafa BM, 2018. Group B streptococcal carriage, antimicrobial susceptibility, and virulence related genes among pregnant women in Alexandria, Egypt. Alex J Med 54: 6976.

    • Search Google Scholar
    • Export Citation
  • 44.

    Wali IE, Sorour AE, Abdalla MAH, 2007. Assessment of different methods for detection of group B streptococci carriage among pregnant females. Egypt J Med Microbiol 16: 593598.

    • Search Google Scholar
    • Export Citation
  • 45.

    Elbaradie SMY, Mahmoud M, Farid M, 2009. Maternal and neonatal screening for group B streptococci by SCP B gene based PCR: a preliminary study. Int J Med Microbiol 27: 1721.

    • Search Google Scholar
    • Export Citation
  • 46.

    Ulett KB, Benjamin WH, Zhuo F, Xiao M, Kong F, Gilbert GL, Schembri MA, Ulett GC, 2009. Diversity of group B Streptococcus serotypes causing urinary tract infection in adults. J Clin Microbiol 47:20552060.

    • Search Google Scholar
    • Export Citation
  • 47.

    Sendi P, Johansson L, Norrby-Teglund A, 2008. Invasive group B streptococcal disease in non-pregnant adults: a review with emphasis on skin and soft-tissue infections. Infection 36: 100111.

    • Search Google Scholar
    • Export Citation
  • 48.

    Madrid L et al., 2018. Maternal carriage of group B Streptococcus and Escherichia coli in a district hospital in Mozambique. Pediatr Infect Dis J 37: 11451153.

    • Search Google Scholar
    • Export Citation
  • 49.

    Foster-Nyarko E et al., 2016. Associations between nasopharyngeal carriage of group B Streptococcus and other respiratory pathogens during early infancy. BMC Microbiol 16: 97.

    • Search Google Scholar
    • Export Citation
  • 50.

    Deng J, Yang Y, 2008. Detection and molecular serotyping of group B Streptococcus in fatal neonatal pneumonia in China. Pediatrics 121 (Suppl 2): S127.

    • Search Google Scholar
    • Export Citation
  • 51.

    Quiroga M, Pegels E, Oviedo P, Pereyra E, Vergara M, 2008. Antibiotic susceptibility patterns and prevalence of group B Streptococcus isolated from pregnant women in Misiones, Argentina. Braz J Microbiol 39: 245250.

    • Search Google Scholar
    • Export Citation
  • 52.

    Allam AA, Bahgat MA, 2006. Phenotype and genotype of some clinical group B Streptococcus isolates resistant to erythromycin in Egypt. Egypt J Med Microbiol 15: 7177.

    • Search Google Scholar
    • Export Citation
  • 53.

    Abdelmoaty T, Wafaa Z, Kawthar M, 2009. Prevalence and antibiotic susceptibility of anogenital group B streptococci colonization in pregnant women. Egypt J Med Lab. 18: 105111.

    • Search Google Scholar
    • Export Citation
  • 54.

    Joachim A, Matee MI, Massawe FA, Lyamuya EF, 2009. Maternal and neonatal colonization of group B Streptococcus at Muhimbili National Hospital in Dares Salaam, Tanzania: prevalence, risk factors and antimicrobial resistance. BMC Public Health 9: 437.

    • Search Google Scholar
    • Export Citation
  • 55.

    Onipede A, Adefusi O, Adeyemi A, Adejuyigbe E, Oyelese A, Ogunniyi T, 2012. Group B Streptococcus carriage during late pregnancy in Ile-ife, Nigeria. Afr J Clin Exp Microbiol 13: 135143.

    • Search Google Scholar
    • Export Citation
  • 56.

    Dunia R, Kowatli K, Abutouk A, Rosa-Fraile M, 2006. Epidemiology of group B Streptococcus in pregnant women in Syria. Arab J Pharm Sci 3: 8188.

  • 57.

    Al-Sweih N, Hammoud M, Al-Shimmiri M, Jamal M, Neil L, Rotimi V, 2005. Serotype distribution and mother-to-baby transmission rate of Streptococcus agalactiae among expectant mothers in Kuwait. Arch Gynecol Obstet 272: 131135.

    • Search Google Scholar
    • Export Citation
  • 58.

    Foad MF, 2016. Urinary tract and vaginal infections caused by group B Streptococcus and the macrolide-inducible resistance to clindamycin in non-pregnant females. Int J Curr Microbiol Appl Sci 5: 486496.

    • Search Google Scholar
    • Export Citation
  • 59.

    Schrag S, Phil D, Zell ER, Stat M, Lynfield R, Roome A, 2002. A population based comparison of strategies to prevent early-onset group B streptococcal disease in neonates. N Engl J Med 347: 233239.

    • Search Google Scholar
    • Export Citation
  • 60.

    Verani JR, McGee L, Schrag SJ, 2010. Prevention of perinatal group B streptococcal disease: revised guidelines from CDC, 2010. MMWR Morbid Mortal Wkly Rep 19: 136.

    • Search Google Scholar
    • Export Citation
  • 61.

    Dunkelberg WE, 1981. Kirby-Bauer disk diffusion method. Am J Clin Path 75: 273.

 
 
 

 

 

 

 

 

 

Serotyping and Antibiotic Susceptibility of Invasive Streptococcus agalactiae in Egyptian Patients with or without Diabetes Mellitus

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  • 1 Department of Clinical Pathology, Al-Azhar University, Cairo, Egypt;
  • | 2 Al Borg Laboratory, Cairo, Egypt;
  • | 3 Centers for Disease Control and Prevention, Atlanta, Georgia;
  • | 4 Hepatology and Gastroenterology Department, National Liver Institute, Menoufia University, Shebeen El-Kom, Egypt;
  • | 5 Department of Tropical Medicine, Faculty of Medicine, AinShams University, Cairo, Egypt;
  • | 6 Hepatobiliary and Liver Transplant Surgery Department, National Liver Institute, Menoufia University, Shebeen El-Kom, Egypt;
  • | 7 Gastroenterology, Hepatology and Infectious Diseases Department, Faculty of Medicine, Kafrelsheikh University, Kafrelsheikh, Egypt;
  • | 8 Epidemiology and Preventive Medicine Department, National Liver Institute, Menoufia University, Shebeen El-Kom, Egypt;
  • | 9 Faculty of Medicine, Suez University, Suez, Egypt;
  • | 10 Department of Internal Medicine, Faculty of Medicine, Menoufia University, Shebeen El-Kom, Egypt;
  • | 11 Department of Clinical Pharmacology, Faculty of Medicine, Menoufia University, Shebeen El-Kom, Egypt

ABSTRACT.

Streptococcus agalactiae serotype distribution and its antibiotic susceptibility affect disease prevention strategies, but the serotype distribution varies among patient groups. The objectives of this study were to establish the group B Streptococcus (GBS) serotype distribution in patients from Egypt and to assess antibiotic sensitivity of invasive GBS isolates. A total of 490 patients participated in this multicenter study; 160 had urinary tract infection, 115 complained of diabetic foot ulcers, 125 men had genital tract infections, and 30 women females had genital tract infections. Others had bronchopneumonia, otitis media, synovitis, or meningitis. Serotyping of the isolated GBS was performed at the CDC in the United States. Antibiotic sensitivity patterns were determined using the disk diffusion method. In men, the most common serotypes were II, III, and V, whereas types Ia, II, III, and V were isolated from women. Macrolides (erythromycin) resistance occurred in 4.1% of the isolates; 10.2% were resistant to both clindamycin and inducible resistance of macrolides, lincomycin, and streptogramin; 17.3% were resistant to quinolones; and 95.9% were resistant to tetracyclines. GBS primarily infected the urinary tract, skin, soft tissue, and genital tract in both genders. Isolates were sensitive to beta-lactam drugs, vancomycin, and linezolid; 14.0% were resistant to macrolides with or without clindamycin. Only 6.0% of the strains were sensitive to tetracyclines. Although GBS causes invasive infections in Egyptian adults, it rarely causes neonatal meningitis or sepsis. Future studies should determine whether GBS isolates are transmitted sexually, by performing a follow-up study of the partner of the infected patient.

Author Notes

Address correspondence to Abd-ElAleem A. El-Gendy, Faculty of Medicine, Al-Azhar University, Almokhayam Aldaaem St., 11884, Nasr City, Cairo, Egypt. E-mail: abdelaleemelgendy2000@gmail.com

Authors’ addresses: addresses: Abd-ElAleem A. El-Gendy and Mohamed El-Tonsy El-Sayed, Department of Clinical Pathology, Al-Azhar University, Cairo, Egypt, E-mail: abdelaleemelgendy2000@gmail.com. Sawsan El Tayeb Hassan, Department of Clinical Pathology, Al-Azhar University, Cairo, Egypt, and Al Borg Laboratory, Cairo, Egypt. Bob Gertz and Beal Bernard, Centers for Disease Control and Prevention, Atlanta, GA. Mohamed Meligy Ahmed, Hassan Ahmed Elzohry, and Mohamed Fathey Elgazzar, Hepatology and Gastroenterology Department, National Liver Institute, Menoufia University, Shebeen El-Kom, Egypt, E-mails: mmelegy2013@gmail.com and elzohry2002@yahoo.com. Ghada Abd El Tawab, Al Borg Laboratory, Egypt, E-mail: elgazzar_mohamed@yahoo.com. Shimaa Y. Kamel, Department of Tropical Medicine, Faculty of Medicine, AinShams University, Cairo, Egypt, E-mail: shimaayoussif81@gmail.com. Hazem Zakaria, Hepatobiliary and Liver Transplant Surgery Department, National Liver Institute, Menoufia University, Shebeen El-Kom, Egypt, E-mail: hazemlasheenn@yahoo.com. Aya Mohammed Mahros and Mohammed Hussien Ahmed, Gastroenterology, Hepatology and Infectious Diseases Department, Faculty of Medicine, Kafrelsheikh University, Kafrelsheikh, Egypt, E-mails: yoye_85@hotmail.com and dr.mm63@yahoo.com. Marwa Ali Tahoon, Epidemiology and Preventive Medicine Department, National Liver Institute, Menoufia University, Shebeen El-Kom, Egypt, E-mail: marwa.123ali@yahoo.com. Mohamed A. Sakr, Faculty of Medicine, Suez University, Suez, Egypt, E-mail: msakr.md@gmail.com. Abdelnaser Abdel-Atty Gadallah, Department of Internal Medicine, Faculty of Medicine, Menoufia University, Shebeen El-Kom, Egypt, E-mail: ahmed_naser2004@yahoo.com. Fatma Eldesoky Ahmed, Department of Clinical Pharmacology, Faculty of Medicine, Menoufia University, Shebeen El-Kom, Egypt, E-mail: fatma.shehata@med.menofia.edu.eg.

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