Abstract
Objective:
To evaluate group B streptococcus (GBS) colonization prevalence and feasibility of intrapartum GBS screening/antibiotic prophylaxis (IAP) in Cameroon, Africa.
Methods:
Prospective cohort in the Cameroon Baptist Convention Health Services network. Maternity providers collected anogenital swabs from consenting term women in labor for testing by a rapid GBS-polymerase chain reaction (PCR) system. Positive tests (GBS+) resulted in initiation of intravenous ampicillin until delivery. Primary outcomes were GBS prevalence and proportion of GBS+ women receiving ampicillin before delivery and more than 4 hours before delivery.
Results:
A total of 219 women were enrolled from January 10 to April 27, 2017. GBS prevalence was 12.3% (95% confidence interval [CI] 7.9–16.7) with GBS+ women more likely to reside in urban areas (19.6% vs 9.7%, P=0.004). Of 27 GBS+ women, 19 (70.4%) received ampicillin before delivery and 14 (51.9%) 4 hours or longer before delivery. A median two doses of ampicillin (interquartile range [IQR] 1–5) were given and started at a median of 105 minutes (IQR 90–155) after swab collection and 20 minutes (IQR 10–45) after GBS result. Of the 8 women who did not receive ampicillin, 7 (87.5%) delivered before test results.
Conclusion:
A GBS IAP protocol is feasible in Cameroon and should be evaluated for widespread implementation in Cameroon and other low-income countries to decrease GBS-related morbidity.
Keywords: Antibiotic prophylaxis, Cameroon, Feasibility, Group B streptococcus, Intrapartum screening, Low-income countries, Prevalence
1 ∣. INTRODUCTION
Group B streptococcus (GBS) is a major infectious cause of neonatal morbidity and mortality with 10%-30% of pregnant women being colonized in the USA.1-5 Universal GBS screening at 35-37 weeks of gestation by anogenital culture followed by intrapartum antibiotic prophylaxis (IAP) for colonized women has been recommended in the USA since 2002, resulting in decreased neonatal morbidity and mortality.6
Cameroon, Africa has the 12th highest maternal mortality rate worldwide with 590 deaths/100 000 live births.7 It also has significant perinatal and infant mortality, with approximately one-third of infant deaths related to perinatal care and more than half to infectious disease.7 The 2015 WHO guidelines on peripartum infections recommend routine GBS screening and IAP even in low-income countries (LIC) such as Cameroon. While some developed nations do not incorporate GBS screening into pregnancy care, in LICs with high perinatal mortality, the impact of GBS screening and IAP may be greater. There is no standardized screening protocol in LICs with financial and technical barriers to performing culture for GBS. To our knowledge, there have been few published reports from sub-Saharan Africa (SSA), and none from Cameroon, regarding the prevalence of maternal GBS colonization, risk factors for colonization, and neonatal effects of invasive disease.
The Cameroon Baptist Convention Health Services (CBCHS) is one of the largest non-profit providers of medical care and education throughout Cameroon, with more than 10 000 deliveries each year. The CBCHS utilizes rapid molecular testing for tuberculosis (TB) with the use of the Cepheid GeneXpert system, which also has GBS testing capability by a rapid (<1 hour) nucleic acid amplification test with more than 85% sensitivity for GBS.8-12 As the GeneXpert system is already deployed across CBCHS centers for TB testing, this may offer the opportunity to screen women for GBS colonization in the intrapartum period as many patients present only for delivery without prenatal care. Therefore, it is crucial to demonstrate that intrapartum GBS screening and IAP can be accomplished locally and that anogenital GBS colonization is prevalent before introducing large-scale antenatal screening programs to decrease GBS-related morbidity and mortality in LICs.
The aims of the present study were to describe the prevalence of and risk factors for GBS anogenital colonization and to evaluate the feasibility of a rapid intrapartum GBS screening and IAP protocol in Cameroon.
2 ∣. MATERIALS AND METHODS
After receiving Institutional Review Board (IRB) approval at the University of Alabama (UAB) and the CBCHS (Cameroon IRB number 2016-20, approved in October 2016; UAB IRB number X161026005, approved in January 2017), a prospective cohort study (from 10 January to 27 April, 2017) was performed at three CBCHS facilities: Mboppi, Mbingo, and Banso, where Cepheid GeneXpert systems are used for TB testing. All women at more than 28 weeks of pregnancy (including multiple gestations) were approached for study participation upon admission for spontaneous labor or induction of labor (IOL). Patients were excluded for prenatally known fetal anomalies, penicillin allergy, planned cesarean delivery, or inability/unwillingness to pay for antibiotic prophylaxis which costs up to US$2/dose (given the ethical consideration of known positive test result without the ability to receive intervention).
After admission, trained maternity providers carried out anogenital swab collection on consenting patients. The double-headed polymerase chain reaction (PCR) swab from the collection kit was used to swab the anogenital region (the lower third of the vagina followed by the rectum), with both swab-heads twirled around each other (to minimize swab-to-swab variation), and placed into a single-use GBS cartridge.6 The GBS Xpert rapid test (Cepheid Inc., Sunnyvale, CA, USA) utilizes PCR amplification to detect the 3’-DNA region adjacent to the cfb gene. Sample preparation, amplification, internal controls, and detection are automated and integrated into the testing cartridge. The cartridge was taken to the lab, analyzed in the GeneXpert system, and results were reported to the maternity unit. Testing was only performed during routine lab hours. Positive tests (GBS+) led to the initiation of 1 g of intravenous ampicillin every 4 hours until delivery. GBS equivocal/indeterminate tests were considered negative for clinical purposes and repeat testing was not performed. A self-administered 15-question survey was given to participating trained providers regarding their attitudes to the screening and IAP protocol. Cepheid, Inc. donated the GBS cartridges for this study.
The primary outcome for the first objective was GBS prevalence. Secondary outcomes included GBS colonization risk factors, maternal outcomes (fever, infection, intrapartum stillbirth), and neonatal outcomes (need for additional care, infection/sepsis, death). It should be noted that there are no neonatal intensive care services available at these sites. To assess the feasibility of a screening and IAP protocol, the primary outcome was the proportion of GBS+ women receiving ampicillin before delivery and for longer than 4 hours (established time to achieve minimum inhibitory concentration).
Patient demographics (maternal age, location of residence [per self-report], site of care, medical co-morbidities), intrapartum/postpartum characteristics, and timing information (time of swab collection, reporting of lab results, initiation of ampicillin, and delivery) were collected by locally trained Cameroonian data abstractors and entered into a REDCap database. Data were verified by UAB biostatisticians with any inconsistencies sent back to Cameroon for review, confirmation, and editing. The maternity provider survey was self-administered via a web-based server and incorporated into the relational database. For this survey, respondent demographics (age, gender, practicing CBCHS site, provider type, and years in practice) were assessed.
Descriptive analyses were used to calculate GBS prevalence (with 95% confidence interval [CI]), proportions of GBS+ women receiving antibiotics at specific time points, median dosages of ampicillin received, and time interval data. Differences in baseline characteristics between GBS+ and GBS-negative (GBS−) women were used to assess for GBS colonization risk factors. Maternal and neonatal outcomes were compared between these groups. To evaluate feasibility, time interval data between GBS+ women who did and did not receive ampicillin were compared. Student t-test or Wilcoxon rank-sum test for continuous variables and χ2 or Fisher exact test for categorical variables were utilized as appropriate. Kruskal-Wallis was used to analyze responses in our provider survey. All analyses were completed with SAS version 9.4 (Cary, NC, USA) at a significance level of 0.05. No adjustments were made for multiple comparisons. It was estimated that a sample size of 200 screened patients would provide more than 80% power to estimate a GBS prevalence rate of 20% (approximately USA prevalence) with a 95% confidence level (Δ ± 5%).
3 ∣. RESULTS
Of the 1207 deliveries in the study period, 219 (18.1%) women were screened, consented, and enrolled at the three sites from January to April 2017 (Banso 85/372, Mboppi 95/647, Mbingo 39/188). Of these, 27 women screened positive for GBS for a prevalence of 12.3% (95% CI 7.9-16.7). Five women had indeterminate testing (2.3%) and 187 (85.3%) screened negative for GBS (total GBS− n = 192). Baseline characteristics of women by GBS status are presented in Table 1. GBS+ patients were similar to GBS− patients in terms of maternal age, marital status, parity, and gestational age at delivery, but GBS+ women were more likely to reside in urban areas (19.6% vs 9.7%, P=0.004) and deliver in urban facilities (22.1% vs 11.2%, P<0.001). Women with co-morbidities were less likely to be GBS+ than women without co-morbidities (0% vs 14.2%, P=0.03).
TABLE 1.
Maternal baseline characteristics by GBS colonization in Cameroon.
| GBS+ (n=27) | GBS− (n=192) | P value | |
|---|---|---|---|
| Maternal age (years) | 26.6 + 5.2 | 27.0 + 5.3 | 0.67 |
| Marital status | 0.65 | ||
| Single | 5 (18.5) | 43 (22.4) | |
| Married | 22 (81.5) | 149 (77.6) | |
| Location of residence | 0.004 | ||
| Urban | 22 (81.5) | 90 (47.4) | |
| Suburban | 1 (3.7) | 19 (10.0) | |
| Rural | 4 (14.8) | 81 (42.6) | |
| Maternal education level | 0.34 | ||
| None/Primary school | 11 (40.7) | 58 (31.5) | |
| Secondary/High school | 16 (59.3) | 126 (68.5) | |
| Maternal medical co-morbidities | 0.030 | ||
| Yes | 0 (0.0) | 28 (14.7) | |
| No | 27 (100.0) | 163 (85.3) | |
| HIV | 0 (0.0) | 17 (8.9) | 0.14 |
| Hypertension | 0 (0.0) | 3 (1.6) | >0.99 |
| Hepatitis B | 0 (0.0) | 4 (2.1) | >0.99 |
| Syphilis | 0 (0.0) | 2 (1.0) | >0.99 |
| Previous preterm birth | 0.60 | ||
| Yes | 0 (0.0) | 7 (3.6) | |
| No | 27 (100.0) | 185 (96.4) | |
| Parity | 0.20 | ||
| Nulliparous | 11 (40.7) | 55 (28.6) | |
| Multiparous | 16 (59.3) | 137 (71.4) | |
| Number of gestations | >0.99 | ||
| Singleton | 27 (100.0) | 190 (99.0) | |
| Multiple gestation | 0 (0.0) | 2 (1.0) | |
| Delivery hospital | <0.001 | ||
| Banso Baptist Hospital | 3 (11.1) | 82 (42.7) | |
| Mbingo Baptist Hospital | 3 (11.1) | 36 (18.8) | |
| Mboppi Baptist Hospital Douala | 21 (77.8) | 74 (38.5) | |
| Type of labor | 0.34 | ||
| Spontaneous | 23 (85.2) | 148 (77.1) | |
| Induced | 4 (14.8) | 44 (22.9) | |
| Mode of delivery (Baby A) | >0.99 | ||
| Vaginal | 24 (88.9) | 168 (88.0) | |
| Cesarean | 3 (11.1) | 23 (12.0) | |
| Gestational age at delivery (weeks), mean ± SD | 39.9 ± 1.6 | 39.5 ± 2.2 | 0.56 |
Values are given as number (percentage) unless otherwise specified. Individual columns may not add up to group ‘n’ given missing data.
Swab collection took a median of 7 minutes (interquartile range [IQR] 5.0-10.0), with 1.3 hours (IQR 1.0-2.3) from the time the specimen arrived in the lab to the reporting of results (Table 2). Overall, the median time from specimen collection to GBS result was 1.4 hours (IQR 1.1-3.0); time from specimen collection to delivery was 10.3 hours (IQR 3.8-21.5).
TABLE 2.
Time intervals (medians with interquartile range) in a GBS screening and antibiotic prophylaxis protocol in Cameroon, Africa.
| GBS+ (n=27) |
||||
|---|---|---|---|---|
| Time intervals | All participants (n=219) | Antibiotics (ABX) (n=19) | No ABX (n=8) | P value |
| Swab collection to in lab time (min) | 7.0 (5.0-10.0) | 10 (5.0-11.0) | 5.5 (5.0-25.5) | 0.77 |
| Swab collection to test result reported (h) | 1.4 (1.1-3.0) | 1.3 (1.1-1.6) | 2.0 (1.3-7.8) | 0.09 |
| In lab time to result reported (h) | 1.3 (1.0-2.3) | 1.2 (0.9-1.5) | 1.7 (1.2-7.6) | 0.06 |
| Swab collection to delivery (h) | 10.3 (3.8-21.5) | 11.6 (5.4-22.8) | 1.8 (1.1-5.9) | <0.001 |
| Result reported to delivery (h) | 7.7 (0.0-19.4) | 10.5 (4.1-21.8) | −0.3 (−336.0 to 0.05)a | 0.002 |
| Swab collection to 1st dose of ABX (min) | 105.0 (90.0-155.0) | |||
| Result reported to 1st dose of ABX (min) | 20.0 (10.0-45.0) | |||
| 1st dose ABX to delivery (h) | 9.7 (3.8-21.0) | |||
Negative time values indicate that delivery occurred before result reported.
Of the 27 GBS+ women, 19 (70.4%) received IAP before delivery, with 14 (51.9%) receiving antibiotics for longer than 4 hours before delivery. Of the 8 women who did not receive IAP, 7 (87.5%) delivered before the reporting of test results. In 1 (3.7%) woman, the protocol was not followed and IAP was not started after a GBS+ result was reported. For GBS+ women who received antibiotics (n=27), a median of two doses (IQR 1-5) were administered and started at a median of 105 minutes after swab collection (IQR 90-155) and 20 minutes (IQR 10-45) after a GBS+ result (Table 2). For women receiving IAP, the first dose of antibiotics was started a median of 9.7 hours (IQR 3.8–21.0) before delivery. Comparison of time points demonstrated that women not receiving IAP had significantly shorter time intervals between delivery and both swab collection and GBS result reporting than those who received IAP (Table 2).
Perinatal outcomes are presented in Table 3. While selected maternal outcomes were similar for GBS+ and GBS− women, neonates born to GBS+ mothers were significantly more likely to be diagnosed with infection/sepsis (18.5% vs 2.6%, P=0.003). Of the five neonates of GBS+ mothers diagnosed with infection/sepsis, one delivered before antibiotic initiation, one delivered with less than 4 hours of antibiotics, and two of these women had extended labor courses longer than 18 hours.
TABLE 3.
Perinatal outcomes associated with GBS colonization in Cameroon, Africa.
| GBS+ (n=27) | GBS− (n=192) | P value | |
|---|---|---|---|
| Maternal fever | 3 (11.1) | 9 (4.7) | 0.17 |
| Maternal infection | 1 (3.7) | 4 (2.1) | 0.49 |
| Fetal death before delivery | 0 (0.0) | 1 (0.5) | >0.99 |
| Neonatal death (baby death) | 0 (0.0) | 2 (1.0) | >0.99 |
| NICU/special care admission | 3 (11.1) | 5 (2.6) | 0.06 |
| Baby diagnosed with infection/sepsis | 5 (18.5) | 5 (2.6) | 0.003 |
Values are given as number (percentage).
The three participating centers surveyed a total of 88 obstetric providers, of which 80 completed the self-administered 15-question survey (response rate 91%). Mean age ± standard deviation of the respondents was 32.2 years ± 9.0 with a median of 2 (range 0.5-23) years in practice. The majority of providers were women (n=66, 82.5%) and trained midwives (n=53, 67.1%); the remainder were nurses (n=17, 21.5%), physicians (n=4, 5.1%), or other provider types (n=5, 6.3%). Overall, providers were satisfied with the ease of GBS specimen collection, rapidity of test results, and ability to begin antibiotics in a timely fashion (Table 4). Most respondents reported that the protocol did not take longer than expected (n=68, 85%) or delay patient care (n=74, 92.5%). Not only would they perform this test again (n=73, 91.3%), they would incorporate it into practice (n=69, 86.3%). Providers universally found GBS testing to be beneficial (100%), with benefit to both mother and baby (n=67, 84.8%). Provider type was significantly associated with responses, as midwives were more satisfied with the protocol and more likely to perform the test again (P=0.044) and in general practice (P=0.027) compared to other provider types.
TABLE 4.
Obstetric provider attitudes towards a rapid intrapartum GBS screening and antibiotic prophylaxis protocol.
| Satisfaction with ease of collection of GBS specimen (mean ± SD on Likert scale of 1-7, 7=very satisfied) | 5.7 ± 1.2 |
| Satisfaction with ease of collection of GBS specimen | |
| Satisfied | 68 (86.1) |
| Neutral | 7 (8.9) |
| Dissatisfied | 4 (5.1) |
| Satisfaction with rapidness of test results (Likert mean ± SD) | 5.8 ± 1.2 |
| Satisfaction with rapidness of test results | |
| Satisfied | 70 (88.6) |
| Neutral | 4 (5.1) |
| Dissatisfied | 5 (6.3) |
| Satisfaction with ability to begin antibiotics with positive test results (Likert mean ± SD) | 6.2 ± 1.1 |
| Satisfaction with ability to begin antibiotics with positive test results | |
| Satisfied | 73 (91.3) |
| Neutral | 4 (5.0) |
| Dissatisfied | 3 (3.8) |
Values are given as number (percentage) unless otherwise specified.
4 ∣. DISCUSSION
A prevalence of at least 12.3% (approximately 20% in urban areas) of maternal GBS colonization by an intrapartum PCR-based rapid GBS test in Cameroon has been demonstrated. The feasibility of a rapid GBS screening and IAP protocol in Cameroon, with more than 70% of GBS+ women receiving antibiotics before delivery (>50% for >4 hours), with obstetric providers satisfied with the protocol and willing to incorporate it into practice, has also been shown. In addition, test results were available in less than 1.5 hours. Given this feasibility, acceptability, and equivalent disease risk to developed countries (such as the USA), a GBS screening and IAP protocol should strongly be considered for more widespread implementation in Cameroon and other LICs. In fact, two sites participating in this pilot study (Mboppi and Mbingo) have started discussions to implement this protocol into their standard care. Efforts are underway to determine the additional cost this would introduce in these LICs.
Although PCR-based (molecular) testing is not the current standard for maternal GBS colonization assessment, the screening characteristics of rapid intrapartum GBS testing have been well-studied. Using the GeneXpert rapid GBS test, Tejada et al. found that intrapartum GBS screening with rapid PCR performed by non-laboratory personnel was at least as accurate as standard antepartum culturing techniques, with a sensitivity of 85%.8 Other studies, most using the GeneXpert system, have demonstrated even higher sensitivities in the range of 90.8%-98.5% with positive predictive values of 87.8%-99.6%.9-15 These studies also demonstrated that PCR-based testing was superior as a screening test to standard culture and often more predictive of neonatal GBS disease.8-17 Results can often be obtained within 1 hour, while GBS culturing takes an average of 48 hours.12 As such, it has been proposed as a rapid point-of-care test to identify women with GBS colonization in situations when GBS culture is unavailable.6 Thus, it is an attractive option for GBS screening in parts of the world where culture is not feasible, trained laboratory personnel are not always available, and uptake of routine prenatal care is not standard. As these limitations are present in Cameroon, rapid GBS intrapartum testing is an excellent option.
The need for GBS screening and IAP is supported by the GBS prevalence in Cameroon. While the overall prevalence was slightly lower (12.3%) than has traditionally been reported in Africa (approximately 20%), the Cameroonian urban prevalence was similar (19.6%).18 Studies have shown incidences of neonatal GBS disease in Africa as similar or higher than that observed in the USA before the 1970s 18,19 In fact, the burden of neonatal GBS in Africa is so high that there are multiple efforts to develop maternal vaccinations against GBS.18 As effective GBS vaccinations are currently unavailable, it is imperative to develop feasible protocols for GBS screening and IAP in these LICs.
The present study, one of the first to be performed in Cameroon, showed that testing can be accomplished using existing infrastructure and adopted with minimal difficulty into routine practice at these CBCHS clinical sites. While the time between testing and result was slightly longer in Cameroon than in other studies, it is important to note that most studies on the accuracy and screening potential of rapid GBS testing were performed in high-income nations. Furthermore, we showed that even given the limited resources in Cameroon, prophylactic antibiotics could be initiated in most women (approximately 70%) before delivery.
The limitations of the present study include the inability to assess the screening characteristics of rapid GBS testing compared to standard culture in the Cameroonian population. However, standard culture is less sensitive; it also cannot currently be performed at these sites and transporting swabs to labs capable of testing is cost-prohibitive. A second limitation is that, given the sample size, it was not possible to detect the incidence of maternal complications, neonatal GBS disease, or the impact of IAP on neonatal disease. Furthermore, this study did not include all women; some were excluded because they could not afford to pay for the cost of prophylaxis, were allergic to penicillin, or had planned cesarean deliveries. We acknowledge that these exclusion criteria may bias results with an actual prevalence rate higher than our results (especially excluding those who could not afford medication, as low socioeconomic status is a GBS risk factor). However, for ethical considerations (not treating a positive result or no alternative non-penicillin medications), these were excluded and should be considered in future studies of GBS prevalence in Cameroon. Another limitation was the lab's inability to perform testing outside routine hours, accounting for the long time intervals between swab collection and results and delaying or even inhibiting (delivery before result) initiation of IAP. The rate of IAP before delivery would certainly be increased if testing could be performed at all hours. In addition, there is the possibility of assignment bias in the assessment of maternal and neonatal infection/sepsis as providers were not blinded to the reception of IAP (i.e. increased neonatal infection/sepsis in the GBS+ group may be secondary to this bias as opposed to a true difference). Furthermore, as neonates were not tested for GBS or other micro-organisms, we cannot currently estimate neonatal GBS colonization or the etiology of infection in infected neonates.
A rapid intrapartum screening and IAP protocol is feasible in Cameroon, and necessary, given maternal GBS colonization rates. However, current costs of the GeneXpert cartridges (up to US$40/ unit) and lab personnel may be unaffordable for most Cameroonians; those costs will need to be subsidized to enable this intervention to have a public health impact. Consideration should also be given to screening at 34-38 weeks of gestation in antenatal clinics, so that 24-hour laboratory coverage is not required and IAP can begin earlier. As the participating CBCHS sites begin implementing this protocol into routine labor management, a larger study will provide additional data regarding maternal and neonatal colonization prevalence, the burden of neonatal disease, and impact of IAP.
ACKNOWLEDGMENTS
The authors acknowledge the donation of the GBS GeneXpert cartridges by Cepheid Inc. for the purposes of this study.
Footnotes
CONFLICTS OF INTEREST
The authors have no conflicts of interest.
REFERENCES
- 1.Franciosi RA, Knostman JD, Zimmerman RA. Group B streptococcal neonatal and infant infections. J Pediatr. 1973;82:707–718. [DOI] [PubMed] [Google Scholar]
- 2.McCracken GH Jr. Group B streptococci: The new challenge in neonatal infections. J Pediatr. 1973;82:703–706. [DOI] [PubMed] [Google Scholar]
- 3.Allardice JG, Baskett TF, Seshia MM, et al. Perinatal group B streptococcal colonization and infection. Am J Obstet Gynecol. 1982;142:617–620. [DOI] [PubMed] [Google Scholar]
- 4.Regan JA, Klebanoff MA, Nugent RP. The epidemiology of group B streptococcal colonization in pregnancy. Vaginal Infections and Prematurity Study Group. Obstet Gynecol. 1991;77:604–610. [PubMed] [Google Scholar]
- 5.Campbell JR, Hillier SL, Krohn MA, Ferrieri P, Zaleznik DF, Baker CJ. Group B streptococcal colonization and serotype-specific immunity in pregnant women at delivery. Obstet Gynecol. 2000;96:498–503. [DOI] [PubMed] [Google Scholar]
- 6.Centers for Disease Control and Prevention. Prevention of perinatal group B streptococcal disease. Morb Mortal Wkly Rep. 2010;59(RR10):1–32. [Google Scholar]
- 7.Trends in maternal mortality: 1990–2013. Estimates by WHO, UNICEF, UNFPA,The World Bankand the United Nations Population Division. http://www.who.int/reproductivehealth/publications/monitoring/maternal-mortality-2013/en/Accessed July 9, 2018 [Google Scholar]
- 8.De Tejada BM, Pfister RE, Renzi G, et al. Intrapartum group B streptococcus detection by rapid polymerase chain reaction assay for the prevention of neonatal sepsis. Clin Microbiol Infect. 2011;17:1786–1791. [DOI] [PubMed] [Google Scholar]
- 9.Gavino M, Wang E. A comparison of a new rapid real-time polymerase chain reaction system to traditional culture in determining group B streptococcus colonization. Am J Obstet Gynecol. 2007;197:388.e1–388.e4. [DOI] [PubMed] [Google Scholar]
- 10.Edwards RK, Novak-Weekley SM, Koty PP, Davis T, Leeds LJ, Jordan JA. Rapid group B streptococci screening using a real-time polymerase chain reaction assay. Obstet Gynecol 2008;111:1335–1341. [DOI] [PubMed] [Google Scholar]
- 11.El Helali N, Nguyen JC, Ly A, Giovangrandi Y, Trinquart L. Diagnostic accuracy of a rapid real-time polymerase chain reaction assay for universal intrapartum group B streptococcus screening. Clin Infect Dis. 2009;49:417–423. [DOI] [PubMed] [Google Scholar]
- 12.Young BC, Dodge LE, Gupta M, Rhee JS, Hacker MR. Evaluation of a rapid, real-time intrapartum group B Streptococcus assay. Am J Obstet Gynecol. 2011;205:372.e1–372.e6. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 13.Davies HD, Miller MA, Faro S, Gregson D, Kehl SC, Jordan JA. Multicenter study of a rapid molecular-based assay for the diagnosis of group B Streptococcus colonization in pregnancy women. Clin Infect Dis. 2004;39:1129–1135. [DOI] [PubMed] [Google Scholar]
- 14.Park JS, Cho D, Yang JH, et al. Usefulness of a rapid real-time PCR assay in prenatal screening for Group B streptococcus colonization. Ann Lab Med. 2013;33:39–44. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 15.Hakansson S, Kallen K, Bullarbo M, et al. Real-time PCR-assay in the delivery suite for determination of group B streptococcal colonization in a setting with risk-based antibiotic prophylaxis. J Matern Fetal Neonatal Med. 2014;27:328–332. [DOI] [PubMed] [Google Scholar]
- 16.Daniels JP, Gray J, Pattison HM, et al. Intrapartum tests for group B streptococcus: Accuracy and acceptability of screening. BJOG. 2011;118:257–265. [DOI] [PubMed] [Google Scholar]
- 17.Abdelazim IA. Intrapartum polymerase chain reaction for detection of group B streptococcus colonization. Aust N Z J Obstet Gynaecol. 2013;53:236–242. [DOI] [PubMed] [Google Scholar]
- 18.Sinha A, Russell LB, Tomczyk S, et al. Disease burden of group B Streptococcus among infants in Sub-Saharan Africa: A systematic literature review and meta-analysis. Pediatr Infect Dis J. 2016;35:933–942. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 19.Joachim A, Matee MI, Massawe FA, EF Lyamuy Maternal and neonatal colonization 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. [DOI] [PMC free article] [PubMed] [Google Scholar]