doi:10.1111/jog.13082
J. Obstet. Gynaecol. Res. 2016
Group B streptococcus antimicrobial resistance in neonates born to group B streptococcus-colonized mothers: Singlecenter survey Yi-Ping Li1, Chi-Man Kuok2, Shin-Yu Lin1, Wu-Shiun Hsieh2 and Ming-Kwang Shyu1 1
Departments of Obstetrics and Gynecology, 2Pediatrics, National Taiwan University Hospital and National Taiwan University College of Medicine, Taipei, Taiwan
Abstract Aim: In this study, we collected group B streptococcus (GBS) screening data and analyzed screening rate, antimicrobial resistance rate, and neonatal observation room (NOR) admission rate due to inadequate chemoprophylaxis. Methods: The GBS screening data for January 2006–December 2013 were retrospectively collected and analyzed. We also collected data for neonates admitted to NOR due to inadequate chemoprophylaxis during the period 1 April 2010–31 December 2013. Results: A total of 12 200 pregnant women received rectovaginal culture during the 8-year study period. The overall screening rate was 53.8% and maternal colonization rate was 20.7%. The GBS screening rate increased remarkably, from 23.2% in 2006 to 70% in 2013. Antimicrobial resistance was common. The resistance rates for each antimicrobial used in pregnancy were as follows: clindamycin, 49.51%; erythromycin, 49.51%. A total of 297 neonates were admitted to NOR due to inadequate antibiotic prophylaxis during 1 April 2010–31 December 2013. The overall NOR admission rate due to inadequate chemoprophylaxis was 2.67%, and the inadequate chemoprophylaxis rate for those GBS colonized mothers was 19.6%. None of these 297 infants had positive blood culture for GBS sepsis. Conclusion: The GBS screening rate increased remarkably, reaching 70% in 2013. The NOR admission rate due to inadequate chemoprophylaxis was 2.67% and there was no early onset GBS disease in a total of 11123 deliveries in this 4-year cohort study. Key words: colonization, drug resistance, group B streptococcus, rectovaginal culture.
Introduction Streptococcus agalactiae, also known as group B streptococcus (GBS), is a Gram-positive bacterium that colonizes the vagina or rectum of 10–30% women.1–3 GBS is a common pathogen that causes perinatal infections through vertical transmission from a GBScolonized mother to the newborn during labor.4 GBS infection causes neonatal bacteremia, pneumonia, and meningitis, with a high mortality rate.5
Since the 1980s, intrapartum antibiotic prophylaxis has been used to reduce neonatal GBS disease within 7 days of birth (early onset disease).6,7 Incidence of early onset neonatal GBS disease has declined dramatically from 1.7 cases per 1000 live births in the 1990s to 0.34–0.37 cases per 1000 live births in the 2010s after consensus on screening and intrapartum antibiotic prophylaxis.8 GBS prophylaxis with beta-lactam antibiotics for >4 h is highly effective at preventing early onset GBS disease,9 and shorter durations (≥2 h)
Received: December 2 2015. Accepted: May 13 2016. Correspondence: Dr. Ming-Kwang Shyu, Department of Obstetrics and Gynecology, National Taiwan University Hospital. No. 8, Chung-Shan South Road, Taipei, Taiwan. Email:
[email protected]
© 2016 Japan Society of Obstetrics and Gynecology
1
Y.-P. Li et al.
of appropriate antibiotics might also provide some protection.10 In 2002 several guidelines were established for prevention of perinatal GBS disease. Many countries worldwide have routine screening of all pregnant women for antenatal GBS carriage, such as the USA, Australia, Canada, Spain, France, Belgium, Germany, and Switzerland but not the UK, Holland or Norway, which opted for the risk-based approach.11–17 Taiwan joined the ranks of universal screening of all pregnant women for prevention of neonatal GBS infection in April 2012 as part of a national policy. In Taiwan, there have been several reports of neonatal GBS infection from regional single institutes18–22; and, in a multi-center prospective study, the incidence of early onset GBS disease was reported as 0.64 per 1000 live births.23 In Taiwan GBS has higher resistance to tetracycline and erythromycin, than in other regions of the world.24 In this study, we collected the GBS screening data from 2006 to 2013, and analyzed screening rate, maternal colonization rate, and antimicrobial resistance rate at National Taiwan University Hospital (NTUH), a tertiary center in Taiwan. We also retrospectively reviewed the neonates admitted to the neonatal observation room (NOR) due indications for inadequate antibiotic prophylaxis ( 75%); 10.0%, elevated C-reactive protein (CRP; >1 mg/dL); 13.3%, clinically respiratory distress; and the other 30.0% were non-specified.
Resistance to
Neonates admitted to NOR
LVX (%)
P (%)
TE (%)
TGC (%)
VA (%)
Because the antimicrobial resistance test panel changed every year at the present hospital, some antimicrobial resistance test data were not available. The GBS antimicrobial resistance spectrum at NTUH is summarized in Table 1. Antimicrobial resistance was very common. GBS strain had the highest resistance to tetracycline, with a nonsusceptibility rate of 87.5%. Resistance to clindamycin and erythromycin was also common, with a nonsusceptibility rate of 49.51% and 49.51%, respectively. The overall resistance rate to chloramphenicol was 9.18%, followed by levofloxacin, with a non-susceptibility rate of 3.14%. In contrast, the GBS isolates were highly susceptible to penicillin, vancomycin and tigecycline. The nonsusceptibility rates to these antibiotics were all below 1%. Only one strain was resistant to tigecycline, which was the most effective antibiotic agent.
0.00 NA 0.00 0.00 0.00 0.00 0.00 1.64 0.30 (n = 7/2321)
GBS survey at NTUH
3
Y.-P. Li et al.
Table 2 NOR admission neonates: Background data (n = 30) n (%) Para-1 Para-2 Para-3 Para-4 Early preterm ( 0) Left shift (Seg. > 75%) Elevated CRP (>1 mg/dL) Clinical respiratory distress Non-specified indication
5 (16.7) 5 (16.7) 4 (13.3) 3 (10.0) 4 (13.3) 9 (30.0)
CRP, C-reactive protein; NOR neonatal observation room.
or local clinics can receive a government grant of $NT500.00 ($US16.50) per GBS rectovaginal culture. In the present study, the GBS screen rate increased gradually from 23.2% in 2006 to 61.7% in 2011 at NTUH. Since 2002, we have followed the CDC guideline and started GBS screening in Taiwan. Obstetricians in Taiwan ensured that the benefit of GBS screening was publicized widely, and the screening rate reached 60% in 2009, although it plateaued in 2009–2011. This may be due to concern among unscreened women about the cost of GBS screening or poor accessibility in some rural areas. For these reasons universal GBS screening was considered and finally included in the national policy in 2012. After this time, the screen rates increased to 66% and 70% in 2012 and 2013, respectively. The screen rate was still below the surveillance rate (85%) in the USA during 2003–2004, and the 86.6% reported in Italy in 2005.26,27 The isolation rate of GBS from pregnant women was 18–22%, compatible with a previous report from Taiwan.23 Group B streptococcus is highly resistant to erythromycin, tetracycline, and clindamycin.28–31 In the present study, the resistance rate for erythromycin, tetracycline, and clindamycin was 49.5%, 87.5%, 49.5%, respectively. The non-susceptibility rate for erythromycin was close to the reported rate (50.7%) in the USA,28 and less than the rate in China (71.2%).30 The non-susceptibility rate for tetracycline was also high. The non-susceptibility rate for levofloxacin was 3.1% and the rate is lower than that reported in China (37.7%)30 and Japan (18.4%).31 The
4
present Taipei data are consistent with a previous study by Lee and Lai in Tainan.24 According to the 2010 CDC guideline,8 for penicillinallergic women at high risk for anaphylaxis, clindamycin or erythromycin may be used if their GBS isolate is susceptible. Vancomycin may be used if their isolate is resistant to clindamycin.8 Pending the sensitivity test results, however, clindamycin is not a good empirical antibiotic for penicillin-allergic women in Taiwan because the resistance rate is as high as 50%. Also, in the present study 21 and seven GBS strains were resistant to penicillin and vancomycin, respectively. Penicillin and vancomycin resistance is extremely rare. In this study the resistance detected was not confirmed by a reference laboratory and therefore further study is required to confirm this unusual finding. Since the national policy of universal GBS screening was implemented, the screening rate reached 70% in 2013. Berardi et al. reported that 93.1% women had indications for intrapartum antibiotic chemoprophylaxis, but only 52.0% of these women received this for ≥4 h.27 Prevalence of inadequate intrapartum antibiotics chemoprophylaxis (
