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Shin, Kim, Sung, Yang, Choi, Roh, Kim, Huh, Lee, Oh, and Kim: Group B Streptococcus Detection Rate and Clindamycin Resistance Among Reproductive-Age Women in Korea During 2003–2022
Original Article
Obstetrics & Gynecology

Journal of Korean Medical Science 2025; 40(15): e29.

Published online: 7 November 2024

DOI: https://doi.org/10.3346/jkms.2025.40.e29

Group B Streptococcus Detection Rate and Clindamycin Resistance Among Reproductive-Age Women in Korea During 2003–2022

Areum Shin1, Doo Ri Kim1, Ji-Hee Sung2, Jinyoung Yang3, Suk-Joo Choi2, Cheong-Rae Roh2, Tae Yeul Kim4, Hee Jae Huh4, Nam Yong Lee4, Soo-young Oh2, Yae-Jean Kim1

1Department of Pediatrics, Samsung Medical Center, Sungkyunkwan University School of Medicine, Seoul, Korea.

2Department of Obstetrics and Gynecology, Samsung Medical Center, Sungkyunkwan University School of Medicine, Seoul, Korea.

3Division of Infectious Diseases, Department of Medicine, Samsung Medical Center, Sungkyunkwan University School of Medicine, Seoul, Korea.

4Department of Laboratory Medicine and Genetics, Samsung Medical Center, Sungkyunkwan University School of Medicine, Seoul, Korea.

Address for Correspondence: Yae-Jean Kim, MD, PhD. Department of Pediatrics, Samsung Medical Center, Sungkyunkwan University School of Medicine, 81 Irwon-ro, Gangnam-gu, Seoul 06351, Korea. yaejeankim@skku.edu

Address for Correspondence: Soo-young Oh, MD, PhD. Department of Obstetrics and Gynecology, Samsung Medical Center, Sungkyunkwan University School of Medicine, 81 Irwon-ro, Gangnam-gu, Seoul 06351, Korea. ohsymd@skku.edu

Received 14 September 2024       Accepted 25 October 2024

© 2025 The Korean Academy of Medical Sciences.

The Korean Academy of Medical Sciences

https://creativecommons.org/licenses/by-nc/4.0/
This is an Open Access article distributed under the terms of the Creative Commons Attribution Non-Commercial License (https://creativecommons.org/licenses/by-nc/4.0/) which permits unrestricted non-commercial use, distribution, and reproduction in any medium, provided the original work is properly cited.

Abstract

Background

Group B Streptococcus (GBS) is one of the leading causes of neonatal early-onset sepsis, resulting in high mortality and significant comorbidity. Intrapartum penicillin prophylaxis is recommended for pregnant women with GBS colonization to prevent vertical transmission. For pregnant women at high risk of anaphylaxis to penicillin, clindamycin is recommended only if the susceptibility of GBS isolates has been identified. We retrospectively examined the GBS detection rate and clindamycin resistance among Korean women of reproductive age over the last 20 years.

Methods

Microbiologic studies using vaginal, vaginal–rectal or vaginal–perianal swabs from female patients 15–49 years of age during 2003–2022 were reviewed. Annual GBS detection rates and clindamycin resistance rates were calculated. The study period was divided into two periods (period 1, 2003–2015; period 2, 2016–2022) based on the introduction of universal culture-based GBS screening in our center in 2016. GBS detection rates and clindamycin resistance rates were compared between the periods using χ2 tests.

Results

A total of 14,571 women were tested 16,879 times and GBS was isolated in 1,054 tests (6.2%), with 423 clindamycin-resistant isolates (40.1%). The GBS detection rate increased from 3.4% (301/8,869) in period 1 to 9.4% (2,753/8,010) in period 2 (P < 0.001). Even during period 1, the GBS detection rate was higher in 2009–2015 compared to 2003–2008 (P < 0.001). Clindamycin resistance rates have remained at similar levels since 2009, which were 39.5% (199/301) in period 1 and 40.2% (303/753) in period 2 (P = 0.833).

Conclusion

This study demonstrated that GBS detection rates in Korean women of reproductive age significantly increased almost three times during the twenty years of the study period, with a persistently high clindamycin resistance rate of up to 40%.

Graphical Abstract

jkms-40-e29-abf001.jpg

Keywords: Streptococcus agalactiae, Clindamycin Resistance, Women, Reproductive Age, Epidemiology, Korea

INTRODUCTION

Early-onset sepsis (EOS) caused by group B Streptococcus (GBS) in neonates, which develops within 72 hours after birth, is causing a significant disease burden even in the 21st century. The global incidence rate of GBS EOS from a meta-analysis in 2017 was 0.41 per 1,000 live births, with a substantial difference between countries.1 It has a high fatality rate of over 5%, and continuous monitoring is needed among survivors for long-term neurodevelopmental impairments in cognitive, motor, vision, or hearing function.12 A GBS maternal vaccine currently in active development seems promising, but its wide commercialization will need time.3
Intrapartum antibiotic prophylaxis (IAP), with penicillin as the first choice, in pregnant women colonized in the genitourinary or gastrointestinal tract with GBS has been shown to prevent vertical transmission and significantly reduce GBS EOS.45 For women at high risk for anaphylaxis due to penicillin, clindamycin has been recommended. However, its use is strictly limited to susceptible isolates, considering the high clindamycin resistance reported as a concerning threat by the U.S. Centers for Disease Control and Prevention (CDC) in 2019.678
Maternal candidates for GBS IAP can be determined using either a clinical risk factor-based approach or a universal culture-based approach. For the latter, antepartum screening at 35 0/7 weeks to 37 6/7 weeks of gestation was initially recommended in 1996 by the U.S. CDC, while screening at 36 0/7 weeks to 37 6/7 weeks of gestation has been recommended since 2020 by the American College of Obstetricians and Gynecologists.89
Currently, there is no consensus for either approach among countries.10111213 Screening pregnant women and prescribing intrapartum antibiotics need consideration on both the economic impacts and the effects of perinatal antibiotic exposure in neonates, such as antibiotic resistance or changes in the normal microflora.1415161718
In Korea, universal screening for GBS colonization in pregnant women has not been recommended at the national level because of insufficient data on the domestic epidemiology of EOS by GBS in the past.1920 However, a recent multi-center study revealed that GBS was the most common pathogen of EOS in Korean neonates born at 35 0/7 weeks of gestation or more during 2009–2018.21 In addition, the increasing trend of GBS maternal colonization with relatively high clindamycin resistance in Korea may require greater attention.22232425 In this study, we retrospectively examined the GBS detection rate and clindamycin resistance rate among Korean women of reproductive age during the last 20 years in one of the tertiary hospitals in Seoul, Korea.

METHODS

Study population

From the Clinical Data Warehouse DARWIN-C of Samsung Medical Center, female genital tract culture data from reproductive-age women of 15–49 years were retrieved from January 1, 2003, to December 31, 2022. According to the search criteria, study subjects were not limited to pregnant women. The subjects underwent vaginal, vaginal–rectal, or vaginal–perianal culture. If a person was tested multiple times within a year, only the first result of that year was included. Information on the residential region was also collected.

Sample collection and GBS identification

At our institution, procedures for GBS collection, identification, and antibiotic resistance tests are as follows.22 Using a rayon swab, specimens were obtained from the lower third of the vagina without using a speculum and then the rectal or perianal area. The swab is inserted into a liquid Stuart transport medium (Copan Venturi Transystem collection device; Copan Innovation, Corona, CA, USA) and transported to the laboratory. After sample inoculation onto a blood agar plate (Shinyang Chemical, Seoul, Korea), MacConkey agar plate, or Thayer–Martin agar plate (Hanilkomed, Seongnam, Korea), it is incubated at 35°C with 5% CO2 for 18–24 hours. Colonies with beta-hemolysis and gram-stained morphology for GBS are confirmed by VITEK-2 (bioMérieux, Marcy-l'Étoile, France) (before May 2017) or matrix-assisted laser desorption ionization-time of flight mass spectrometry (MALDI-TOF MS) (VITEK MS; bioMérieux) (after May 2017). Antimicrobial resistance testing, including inducible clindamycin resistance, is performed using VITEK-2. The CLSI M100-Ed32 breakpoints are used to interpret the results.

Analysis of GBS detection rate and clindamycin resistance rate

Annual GBS detection rates and clindamycin resistance rates were calculated. In addition, each rate was compared between two periods (period 1, 2003–2015; period 2, 2016–2022). During 2003–2015, a risk-based approach was adopted, and pregnant women received IAP when risk factors were identified; a GBS sepsis history in a previous child, GBS bacteriuria during the current pregnancy, preterm labor, preterm premature rupture of membranes, prolonged rupture of membranes for more than 18 hours, or intrapartum fever.22 During 2016–2022, universal culture-based screening was conducted in all pregnant women at 35–37 weeks of gestation.22 Women with positive GBS culture received IAP based on culture results, except those with a scheduled elective cesarean section.

Statistical analysis

The χ2 test was used to analyze categorical variables. The Pearson correlation was used to describe time-dependent change in the annual GBS detection rate, and the coefficient of determination (R2) was calculated. P value less than 0.001 was considered statistically significant. The statistical analysis was performed using the IBM SPSS Statistics (Version 27; IBM Corp., Armonk, NY, USA).

Ethics statement

This study was approved by the Institutional Review Board of Samsung Medical Center and the requirement for informed consent was waived (SMC 2024-10-070).

RESULTS

During the study period, a total of 14,571 women were tested 16,879 times. The median age was 33 (interquartile range, 30–37). Residential information was available in 14,343 subjects, and the majority (89.8%) were Seoul (56.3%) and Gyeonggi province (33.5%) residents. GBS was isolated in 6.2% of tests (1,054/16,879), and clindamycin resistance was detected in 40.1% of isolates (423/1,054).
Annual GBS detection rates and clindamycin resistance rates are shown in Figs. 1 and 2. The median number of swab tests per year increased from 594 per year in period 1 to 1,222 per year in period 2 (Fig. 1). Although the total number of swabs was similar in the two periods, the GBS detection rate increased significantly from period 1 to period 2 (Fig. 3). In period 1, 301 isolates were detected from 8,869 tests (3.4%); in period 2, 753 isolates were detected from 8,010 tests (9.4%) (P < 0.001).
Fig. 1

Annual detection rates of GBS from genital tract cultures of reproductive-age women.

GBS = group B Streptococcus, R2 = the coefficient of determination.
aVaginal, vaginal-rectal or vaginal-perianal swabs.
jkms-40-e29-g001
Fig. 2

Annual clindamycin resistance rates of GBS from genital tract cultures of reproductive-age women.

GBS = group B Streptococcus.
jkms-40-e29-g002
Fig. 3

Differences in the detection rates of GBS colonization and the clindamycin resistance rates by periods.

GBS = group B streptococcus.
***P < 0.001.
jkms-40-e29-g003
It is of note that the significant increase in the GBS detection rate already started during the pre-universal screening period (Fig. 1). During period 1, the GBS detection rate was higher in 2009–2015 (5.3%) compared to 2003–2008 (0.2%) (P < 0.001). GBS detection rate started to increase in 2009, which paralleled the increase in total swab numbers during 2009–2010. However, GBS detection continued to increase during 2013–2014, although annual total swab numbers stagnated. The GBS detection rate eventually entered a plateau in 2014–2015, prior to the introduction of universal screening. During the total study period, a time-dependent linear increase in the GBS detection rate was observed by the Pearson correlation coefficient of 0.93 (P < 0.001) with the R2 of 0.86.
According to our investigation, annual clindamycin resistance rates of GBS isolates have been maintained at similar levels since 2009 (Fig. 2). Although clindamycin resistance rates could not be estimated properly before 2009 due to the low number of positive culture cases, there was no difference in clindamycin resistance rates between the two periods (Fig. 3); in period 1, 199 of 301 isolates (39.5%) were resistant, while 303 of 753 isolates (40.2%) were resistant in period 2 (P = 0.833).

DISCUSSION

In this study, GBS detection rates in Korean women of reproductive age increased almost three times over the last 20 years, from 3.4% in the pre-universal screening period to 9.4% in the universal screening period. The clindamycin resistance rate of GBS isolates could be estimated from 2009 onward and has remained around 40%.
Before 2005, the GBS detection rate among pregnant Korean women from single-center studies had been reported to be under 5%.2627 During 2006–2011, Yook et al.28 estimated a GBS detection rate of 8.0% among 5,095 pregnant women from tertiary hospitals, with a clindamycin resistance rate of 39.5%. Meanwhile, Choi et al.23 observed a temporal increase in maternal GBS detection at a single tertiary hospital, 19.8% among 379 women during 2017–2019, which was nearly double the previously reported rate of 11.5% among 234 women during 2008–2009.29 While these previous research predicted a recent increasing tendency in GBS detection rate based on studies from less than five-year periods, our study has the strength to prove a significant increase in the GBS detection rate, using 20-year longitudinal data.
Several factors can contribute to differences in GBS detection rate, such as variations in sample-collection methods by physicians or bacterial isolation techniques in microbiology laboratories. At our institution, there were no changes in vaginal–rectal or vaginal–perianal swab procedures or GBS isolation techniques except for the introduction of MALDI-TOF MS in 2017, which did not seem to influence the GBS detection rate significantly.
Therefore, we believe that the increase in the GBS detection rate, even before the introduction of universal screening, truly reflects an ongoing increase in GBS colonization rates among Korean women of reproductive age. Whether this increasing tendency of GBS colonization rates is a universal phenomenon among other East Asian countries would be an interesting topic since this area is traditionally known for the relatively low maternal GBS colonization rates.103031323334 A meta-analysis in 2017 reported that the maternal GBS colonization rate was 8.3% from studies published in Korea during 1997–2015, 11.3% in China during 1995–2016, and 16.2% in Japan during 2002–2015, with adjustment for sample collection and microbiological methods.10 A recent study in China reported a GBS colonization rate of 17.9% during 2021–2022.31
In the U.S., since the introduction of universal screening in 2002, more than 50% of GBS EOS cases have been reported from GBS culture-negative mothers, raising awareness of standardized detection methods.535 Therefore, the American Society of Microbiology (ASM) has strongly recommended several high-yield strategies in the 2021 guideline, such as vaginal–rectal specimen collection with a flocked swab transported to the testing laboratory within 24 hours; incubating the specimens in selective enrichment broth for 18–24 hours prior to agar plating; and the inclusion of potential non-hemolytic candidates, which compose about 5–6% of GBS isolates in screening specimens.36 On the other hand, unlike ASM’s recommendation of vaginal–rectal swabs over vaginal–perianal swabs, a recent meta-analysis from 2022 reported that vaginal–perianal swabs showed a comparable yield with less patient discomfort than vaginal–rectal swabs.37
Meta-analyses from international studies have revealed an enhanced GBS detection rate of 1.9-fold associated with selective enrichment broth compared to unselective agar only, and that of 1.4-fold associated with vaginal–rectal swabs compared to single vaginal swabs, respectively.10 Nevertheless, the maternal GBS colonization rate in the U.S. has remained around 20–25% since the 1980s and needs further monitoring in the future.1038
Many medical centers in Korea, including ours, have introduced the universal GBS screening approach at the institutional level; however, they have not strictly followed the recommended guidelines yet. Previous reports have documented a wide range of GBS colonization rates among Korean women in a recent 10-year period (6.4–19.8%), which may be partly attributed to the difference in GBS detection methods between institutions.22232425 For instance, the GBS detection rate of 10.6% reported from a multi-center study in 2018–2020 among 33,721 women might be undervalued, as the authors indicated, since the specimens were collected via only a single vaginal swab and direct agar plating was done without selective enrichment.24 In fact, our institution used rayon swabs until 2023. Based on this study’s results, we replaced them with flocked swabs and introduced a preincubation with selective Lim Broth in early 2024.
In Japan, national universal screening for GBS was introduced in 2008, with a relatively higher maternal GBS colonization rate than those of neighboring countries.10 However, unlike in the U.S., where the incidence of GBS EOS cases eventually decreased (from 1.8 per 1,000 live births in the 1990s to 0.23 per 1,000 live births in 2015), the incidence rate of GBS EOS in Japan remained unchanged over 10 years following the implementation of universal screening (0.08 per 1,000 live births in 2004–2010 vs. 0.09 per 1,000 live births in 2016–2020).53940 Aside from the intrinsically low incidence rate of GBS EOS in Japan compared to the U.S., poor adherence to standardized detection methods became an issue again. A recent national surveillance study in Japan revealed that 66% of institutions skipped the selective enrichment step and 60% collected the specimen from the vagina alone.3941 This study result may provide additional insights in other institutions and countries where GBS screening is being performed or considered.
The U.K. reported a recent increase in the incidence of GBS EOS from 0.48 per 1,000 live births in 2000 to 0.57 per 1,000 live births in 2015.42 However, universal culture-based screening for GBS is not recommended in the U.K. as updated in 2017.14 They noted that most babies born from GBS carrier mothers do not develop EOS; it is generally suggested that up to 50% of babies born from GBS carrier mothers become colonized with GBS, and roughly 1% of them develop EOS. Consequently, giving IAP to all carrier mothers would only increase adverse outcomes from unnecessary antibiotic exposure in most cases. In addition, many severely affected babies of GBS EOS are preterm neonates, which is beyond the jurisdiction of universal screening. They also raised concerns about the accuracy of the GBS screening methods.
A meta-analysis of studies comparing the effect of the risk-based approach versus the screening approach suggested that the latter was associated with a lower incidence of GBS EOS without overuse of antibiotics than the former.12 Authors retrospectively found a higher number of missed cases of GBS EOS from the risk-based approach (41.3%) than the screening approach (24.2%), while similar rates of prophylactic antibiotics were used in both approaches. Further related studies are needed.
Clindamycin is an alternative option for women at high risk for penicillin anaphylaxis only if the susceptibility of GBS isolates has been identified, considering their high resistance rate. Our study observed the clindamycin resistance rate of GBS around 40% for longer than 10 years. In comparison to neighboring countries, it was reported as 34.2% from a single tertiary hospital in Japan during 2017–2021, 42.3% from a single tertiary hospital in Taiwan during 2012–2020, and 56.7–66.0% from China Antimicrobial Resistance Surveillance System during 2017–2021.303443
A recent multi-center study from the U.S. unexpectedly found that the occurrence of GBS EOS from GBS-colonized mothers was comparable between those who received non-penicillin prophylaxis, including clindamycin, and those who did not receive any antibiotic.44 Investigators pointed out the possibility of prescribing non-penicillin antibiotics based on physician preference rather than antibiotic susceptibility results.44 This confirms the importance of strict evidence-based decision-making for mothers at high risk for penicillin anaphylaxis and the continuous monitoring of clindamycin resistance dynamics of GBS isolates from pregnant women. Meanwhile, in the U.K., clindamycin is no longer recommended as IAP, based on a resistance rate of 16%.14
This study has a few limitations. First, it was a single-center study, and 89.8% of the subjects were from Seoul and Gyeonggi province, while 50.7% of the Koreans resided in Seoul and Gyeonggi province, according to the 2023 annual report from Statistics Korea.45 However, Bae et al.24 reported in a study using nationwide data in 2018–2020 that the overall GBS colonization rate in pregnant women was 10.6% and the clindamycin resistance rate was 34.5%. In their study, 45.8% of the samples were from Seoul and Gyeonggi province, and the resistance rate in this area was 38.0%. Therefore, although limited, the GBS detection rate in reproductive-age women of 9.4% with a clindamycin resistance rate of 40.2% in period 2 of this study may represent nationwide data to a certain extent. Second, study subjects were not restricted to pregnant women, specifically at 35–37 weeks of gestation, which would have provided the most relevant data for predicting vertical transmission. Third, longitudinal dynamics of maternal GBS isolates were not further stratified by serotype or genotype, which could support changes in the maternal colonization rate.46
In conclusion, this study demonstrated that GBS detection rates in Korean women of reproductive age have almost tripled from the pre-universal screening period to the universal screening period in the last 20 years and showed that almost one in ten women has been colonized with GBS in recent years with relatively high clindamycin resistance rate up to 40%. Universal GBS screening for IAP is the result of different team efforts and collaboration because every step is interrelated, contributing to the correct diagnosis of GBS colonization and the proper prophylaxis. Our observations provide evidence that it is time to discuss GBS universal screening at the national level in Korea, with additional considerations and preparations required before its effective implementation.

ACKNOWLEDGMENTS

The authors thank So-yeon Kim for assisting with the collection of data from the Clinical Data Warehouse DARWIN-C of Samsung Medical Center.

Notes

Disclosure: The authors have no potential conflicts of interest to disclose.

Data Availability Statement: The data that support the findings of this study are available from the corresponding authors upon reasonable request.

Author Contributions:

  • Conceptualization: Kim YJ.

  • Data curation: Shin A, Kim DR, Oh SY, Kim YJ.

  • Formal analysis: Shin A, Kim DR.

  • Investigation: Shin A, Kim DR, Sung JH, Yang J.

  • Methodology: Kim DR, Sung JH, Choi SJ, Roh CR, Kim TY, Huh HJ, Lee NY, Oh SY, Kim YJ.

  • Supervision: Choi SJ, Roh CR, Lee NY, Oh SY, Kim YJ.

  • Validation: Sung JH, Yang J, Kim TY, Huh HJ, Oh SY.

  • Visualization: Shin A, Kim YJ.

  • Writing - original draft: Shin A, Kim YJ.

  • Writing - review & editing: Yang J, Kim TY, Huh HJ, Oh SY, Kim YJ.

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