Published online April 3, 2006
PEDIATRICS Vol. 117 No. 4 April 2006, pp. 1055-1066 (doi:10.1542/10.1542/peds.2005-1114)
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Rapid Tests for Group B Streptococcus Colonization in Laboring Women: A Systematic Review

Honest Honest, MBChB, Sushma Sharma, MRCOG and Khalid S. Khan, MRCOG

Department of Obstetrics and Gynecology, University of Birmingham, Birmingham Women's Hospital, Birmingham, United Kingdom


   ABSTRACT
TOP
 ABSTRACT
METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
OBJECTIVES. We set out to determine the accuracy and rapidity of various intrapartum group B Streptococcus (GBS) colonization tests.

STUDY DESIGN. We performed a systematic review of test-accuracy studies, which were identified without language restriction from Medline and Cochrane databases; bibliographies of known primary and review articles; and contact with authors, experts, and manufacturers. Studies were selected if they tested pregnant women intrapartum for GBS colonization and confirmed by "gold-standard" laboratory cultures. Two reviewers independently selected studies and extracted data on their characteristics, quality, and results. Accuracy data were used to form 2 x 2 contingency tables. Heterogeneity was assessed, and LRs for positive and negative test results were pooled in subgroups of studies of various tests.

RESULTS. There were 29 test-accuracy studies in 15691 women, evaluating 6 different tests: polymerase chain reaction (PCR), optical immunoassay (OIA), DNA hybridization, enzyme immunoassay, latex agglutination, and Islam starch medium tests. The methodologic quality of the studies was generally poor. The most accurate was the real-time PCR test, but it was less rapid than OIA test. Real-time PCR took 40 minutes to complete, whereas the OIA took 30 minutes.

CONCLUSIONS. Real-time PCR and OIA are candidates for rapid near patient intrapartum GBS testing to determine the need for antibiotic prophylaxis to prevent neonatal GBS disease. Before implementation in practice, a robust technology assessment of their accuracy, acceptability, and cost-effectiveness is required.

Key Words: group B Streptococcus • rapid intrapartum test • systematic review

Abbreviations: GBS—group B Streptococcus • LR—likelihood ratio • CI—confidence interval • PCR—polymerase chain reaction • OIA—optical immunoassay

Group B Streptococcus (GBS) is a frequent cause of severe early-onset infection in newborn infants, afflicting 1 to 2 per 2000 births.1–4 It is associated with up to 50% neonatal mortality4 and significant long-term morbidity, including impaired psychomotor development, in up to 30% of survivors of early GBS infection.5 Administration of intrapartum antibiotic prophylaxis to mothers who are colonized with GBS (asymptomatic carriage of GBS in the rectum or vagina)6 may prevent early-onset neonatal GBS disease.7,8 However, there is worldwide variation in practice concerning strategies to identify women for targeted intrapartum antibiotic prophylaxis.

There are 2 main approaches to the screening strategies. One approach is based on universal maternal testing at weeks 35 to 37 of gestation with culture of a high vaginal swab,1,4,7,9 which has been the standard of care in the United States. Another approach uses assessment based on clinical risk factors,10–12 which has been recommended in the United Kingdom recently and has been added to the culture-based screening in the revised US guidelines of 2002. Currently, most cases of early-onset neonatal GBS disease occur in newborns of mothers negative for antenatal GBS cultures and risk factors. Cultures at weeks 35 to 37 of gestation miss the preterm pregnancies that, though only 7% to 11% of births,13 are at the highest risk of serious neonatal GBS infection and account for 32% to 38% of early-onset GBS disease.14,15 Furthermore, there is a poor correlation between antenatal test results and intrapartum maternal GBS colonization after 1 to 2 weeks of test.16 The risk-based approach is inherently crude, with 1 recent study reporting that up to 65% of early-onset neonatal GBS cases did not have any risk factors.17 Thus, in the United States, despite combining the 2 screening strategies as advocated by the revised guidelines,4 invasive early-onset disease incidence has declined only by 34%.18 There is a need for new screening strategies to prevent cases of early-onset GBS disease over and above the disease reduction already achieved by antenatal culture, risk-based screening, and selective chemoprophylaxis. Could a rapid intrapartum test replace existing screening strategies or could it be used in conjunction with them? A key element in addressing these questions relates to the accuracy with which the rapid test identifies mothers with GBS colonization.

Antibiotic prophylaxis carries disadvantages for the mother and infant, for example, potentially fatal anaphylaxis,19 medicalization of labor and neonatal period, and infection with resistant organisms.9,20–23 Thus, because of poor accuracy, there is controversy concerning these screening strategies in the United Kingdom.1,24

There are a number of considerations in developing rapid intrapartum tests for maternal colonization. The intermittent nature of maternal GBS colonization practically means that mothers should be tested for carriage at the onset of labor. However, standard microbiologic cultures take >24 hours for their results to become available, a time scale too long to inform the decision concerning intrapartum antibiotic prophylaxis. For a rapid test to be useful in practice, it would have to be accurate compared with the standard culture. Should a rapid and accurate test exist, timely and targeted antibiotic prophylaxis could then be implemented. Thus far, the lack of a GBS test, accurate and rapid enough in early labor, has been considered an impediment.4 However, there has not been a systematic review to assess intrapartum feasibility and the performance of purportedly rapid commercially available25–29 GBS tests. This background prompted us to undertake such a review using appropriate quality assessments and meta-analysis to obtain valid and reliable estimates of the accuracy of various intrapartum tests for maternal GBS colonization.


   METHODS
TOP
 ABSTRACT
 METHODS
RESULTS
 DISCUSSION
 REFERENCES
 
Our review was based on a prospective protocol developed using widely recommended methodology.30–33

Data Sources and Study Selection
Our search strategy included searches of Medline (1966 to August 2005) and the Cochrane Central Register of Controlled Trials, Cochrane Library (Issue 1, 2005). The databases were searched using relevant text words, Medical Subject Headings including all subheadings and their word variants. A total of 44 terms representing the concept (pregnancy OR labor) AND (GBS) AND (tests OR investigations OR diagnosis OR accuracy) were used. The terms for diagnosis and accuracy were adapted from existing search filters.34–36 In addition, we checked the reference lists of known reviews and primary articles to identify cited articles not captured by electronic searches and made contact with authors, experts, and manufacturers.

Articles were selected if the following criteria were met: (1) population of pregnant women in labor, (2) GBS test, and (3) confirmation of GBS status by "gold-standard" method of laboratory culture. Articles were selected in 2 stages. Initially, 1 reviewer (SS) scrutinized the electronic searches to obtain full articles of all citations that were likely to meet the predefined selection criteria. Secondly, the final inclusion or exclusion decisions were made on assessment of these articles independently by another reviewer (H.H.). No language restrictions were applied. English-language articles were assessed independently by 2 reviewers (H.H. and S.S.) and other language articles by people who had command of the language to allow data extraction from the articles. Disagreements were resolved either by consensus or arbitration with a third reviewer (K.S.K.). A full list of excluded articles is available from the authors.

Data Extraction and Its Rationale
Information was extracted from each selected study on population and test characteristics including the time taken to perform the tests, methodologic quality, and accuracy results. Information on time gave us an indication of the feasibility of a test in the intrapartum setting for guiding decisions concerning antibiotic prophylaxis. It is reported that antibiotic should be used for 2 hours before birth.6 We were interested in intrapartum setting, because the fetus acquires GBS infection from colonized birth canal at this time.16,37 We sought information on anorectal specimen in addition to vaginal specimen, because intestinal tract is a common reservoir and a source of spread to the vagina.16,37 Anorectal carriage of GBS is also an independent predictor of neonatal GBS.16,37,38 We defined the gold standard for verification of rapid tests as appropriate microbiologic culture of GBS (see below). Where accuracy data were not extractable, we contacted the corresponding author, by letter or email, to seek his or her assistance in data extraction. In cases of multiple publications, complete information on characteristics and quality was extracted using all sources, but only the most recent and complete results were included in meta-analysis.

Methodologic Quality Assessment
We defined quality as the confidence that the study design, conduct, and analysis minimized bias in the estimation of test accuracy. Existing checklists39,40 and empirical evidence41 relate bias to a number of items: case-control design, nonprospective data collection, nonconsecutive patient enrollment, inadequate description of participants and/or index tests, lack of blinding, partial or differential verification of index tests, and use of different gold standards.39,41 Items related to gold standards were critical to our review, as use of nonselective medium during incubation decreases its validity.42,43 Therefore, we considered a study to be of high quality if it reported a prospective design, consecutive patient enrollment, an adequate test description, blinding of the test results, and use of selective medium for incubation of specimen for gold-standard culture. In addition, we sought information on a priori estimation of sample size and its rationale. We also sought information on whether a study explored for spectrum variation44 considering predisposing factors, because test accuracy varies in relation to these. For GBS colonization, risk factors include prematurity, prelabor rupture of membranes, and intrapartum fever.1

Data Synthesis
Data from individual studies were synthesized separately for the various tests. For each test, sensitivity, specificity and likelihood ratios for positive (LR+) and negative (LR–) results with confidence intervals (CI) were calculated as measures of accuracy of individual studies. Heterogeneity was assessed graphically and statistically45,46 within subgroups of studies stratified by test type. For graphical exploration, we used plots of sensitivities versus 1– specificity in the receiver operating characteristic space and forest plots of LRs of the various rapid tests. Statistically, we used the {chi}2 test for heterogeneity to assess whether the differences between studies could be explained by chance alone. We also checked for correlation between sensitivity and specificity using Spearman's rank correlation test.32 These evaluations helped assess the feasibility of pooling individual results in a meta-analysis, where correlation indicates dependency of sensitivity and specificity to variation in cutoff point and would make pooling of these measures independently inadvisable. As in our previous publications,47,48 summary LRs were generated if pooling (using a random-effects model) was considered appropriate. LRs are useful in indicating by how much a given test result will raise (when positive, indicated by the value of LR+) or lower (ie, LR–) the probability of having GBS and would allow the determination of posttest probabilities (ie, posttest probability = LR x pretest probability/{1 + [pretest probability x (1 – LR)]}).47 We did not consider pooling sensitivities and specificities separately, because they are not independent values.49 For many tests, pooling could only be undertaken in subgroups according to the subtype of test and site of swabs. Furthermore, pooling was stratified according to type of gold-standard culture used. We took extreme care to avoid multiple counting of the same patients in the meta-analysis.

Where a sufficient number of studies with contrasting features (study quality items and site of swabs) was available within subgroups of tests, we planned to use metaregression analysis50,51 to examine the relation between these features and accuracy. Our metaregression models assessed the effect of study quality (high or low) and site of swabs (vaginal or anorectal) on diagnostic odds ratio (ratio of LR+/LR–), adjusting for test type. For quality evaluation, if 3 of the quality items outlined above were met, we arbitrarily classified the study as high quality. Where a quality item presence was not explicitly stated, it was treated as "no" in the metaregression analysis. We also undertook funnel plot (diagnostic odds ratio versus 1/SE) analysis to examine for publication and related biases.52 All of the statistical analyses were performed using statistical packages SPSS 10 (SPSS Inc, Chicago, IL) and Stata 8.0 (Stata Corp, College Station, TX).


   RESULTS
TOP
 ABSTRACT
 METHODS
 RESULTS
DISCUSSION
 REFERENCES
 
Literature Identification and Study Quality
On electronic literature search, 1296 citations were found, which were scrutinized as shown in Fig 1. Of these, 23 articles (29 studies) that met the predefined selection criteria were selected. Some articles contributed >1 study in our review, because they evaluated >1 test. There were 6 different types of tests for the diagnosis of GBS colonization: polymerase chain reaction (PCR) in 2 studies (914 women)25,53; optical immunoassay (OIA) in 5 studies (1970 women)27,54–57; DNA hybridization in 2 studies (268 women)58,59; enzyme immunoassay in 9 studies (3569 women; 1 study54 evaluated 2 different enzyme immunoassay tests)28,54,57,60–64; latex agglutination in 10 studies (8451 women)28,29,62–69; and Islam starch medium tests in 2 studies (519 women).26,70


Figure 1
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  		FIGURE 1 Study selection process for systematic review of tests for detecting GBS intrapartum maternal colonization. a List is available from the authors. b The total number of studies exceeded 23, because some articles evaluated multiple types of tests.

 
As shown in Fig 2, the quality of the studies was poor in many respects: only 4 recruited mothers consecutively27–29,53; only 4 blinded the test from the gold standard27,53,59,61; and only 12 used an adequate gold standard (selective enrichment culture).* None of the studies explored for spectrum variation. Although only 1 computed sample size a priori,53 3 studies had a sample of >1000 women.28,67,69


Figure 2
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  		FIGURE 2 Methodologic quality of studies included in the systematic review of intrapartum tests for maternal GBS colonization. Data are presented as 100% stacked bars. Figures in the stacks represent the number of studies (total = 29 studies).

 
Most studies obtained vaginal swabs for tests and gold standards without speculum examination. The technique for obtaining specimens with these swabs was poorly described, but in 12 it was clear that specimens were obtained from the lower third of the vagina.{dagger} Only 4 studies obtained high vaginal swabs using speculum examination,29,63,65,68 and only 4 studies also examined the accuracy of rectal swabs.25,27,62,70 The prevalence of GBS colonization in these studies varied from 5% to 32%.27,65

Rapidity of Intrapartum Tests for GBS Colonization
The time taken to undertake the tests is detailed in Table 1. For PCR it was 40 to 100 minutes, for OIA it was 30 minutes, for DNA hybridization it was 60 to 1440 minutes, for enzyme immunoassay it was 5 to 10 minutes, for latex agglutination it was 70 to 85 minutes, and for Islam starch medium tests it was 120 to 1400 minutes. The rapidity of PCR tests varied according to type, with real time taking 40 minutes and conventional taking 100 minutes. For enzyme immunoassay and latex agglutination, the rapidity varied with the heaviness of colonization, and the more heavily colonized specimens tested more quickly. DNA hybridization, Islam starch medium, and latex agglutination tests took too long to be feasible as rapid intrapartum tests. Enzyme immunoassay, although rapid, was less accurate than either PCR or OIA.


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  		TABLE 1 Characteristics of Studies on Accuracy of Various GBS Tests in Predicting Maternal Intrapartum Colonization

 
Accuracy of Various Intrapartum Tests for GBS Colonization
Because of multiplicity of test types, sites of swabs, and gold standards, there were forty-two 2 x 2 tables to compute test accuracy (Table 2). When examining studies with selective culture as the gold standard, the 2 most accurate tests were real-time PCR and OIA (Fig 3). Real-time PCR had a LR+ of 38.80 (95% CI: 6.05–248.72) and LR– of 0.06 (95% CI: 0.03–0.11); median sensitivity of 0.96 (95% CI: 0.88–0.99) and median specificity of 0.98 (95% CI: 0.96–0.99). Summary LR+ for OIA was 14.7 (95% CI: 10.6–20.3), summary LR– was 0.47 (95% CI: 0.31–0.73), median sensitivity was 0.48 (range: 0.37–0.72) and median specificity was 0.97 (range: 0.96–0.99). Metaregression analysis showed that test accuracy did not vary according to overall quality (P = .58) or the addition of anorectal swab (P = .064). Funnel plot analysis did not show any evidence of asymmetry to indicate the presence of publication or related bias for the largest subgroup of studies.


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  		TABLE 2 Results of Individual Studies on Various Rapid Maternal Intrapartum Tests for GBS Colonization

 

Figure 3
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  		FIGURE 3 Meta-analysis of subgroup studies using selective culture for gold standard showing summary LRs for intrapartum test of maternal GBS colonization. a Accuracy result was derived from reporting at 1 hour; the rest of the results, from 8, 16, and 25 hours, which were too long to be of use for intrapartum testing, were excluded. b Heterogeneity within meta-analysis. See Table 2 for details of individual results and their meta-analysis.

 

   DISCUSSION
TOP
 ABSTRACT
 METHODS
 RESULTS
 DISCUSSION
REFERENCES
 
Our review shows that many of the GBS tests, with the exception of real-time PCR and OIA, took either too long or were not of sufficient accuracy to be feasible for maternal intrapartum testing to aid decision making concerning antibiotic prophylaxis to prevent neonatal GBS disease. Although OIA seemed less accurate than real-time PCR, the latter was only evaluated in 2 small studies, 1 of which was a relatively small study. In light of the poor methodologic quality of the existing studies and the imprecision of the evidence for PCR, a robust technology assessment comparing the most promising tests (PCR and OIA) is needed before reaching recommendations for practice.

The strength of our inferences depends on the rigor of our methodology. We complied with existing guidelines for reviews of test-accuracy studies.30–33 We did limit our search to a couple of databases, but we did not apply language restrictions. In light of input from experts and manufacturers, we feel reasonably confident that relevant studies have not been missed.71 Cognizant that meta-analysis of test-accuracy studies are fraught with difficulty because of poor methodologic quality of the primary studies, we scrutinized the selected studies for their quality considering recent recommendations and checklists.39,40 Case-control design that may overestimate accuracy was not found in the selected studies. However, other quality criteria concerning tests and gold standards were commonly poorly adhered to. Our quality assessments were also affected by lack of reporting in some instances. Although assessment of heterogeneity on the receiver operating characteristic space and exploration for reasons behind heterogeneity were planned a priori, they were hampered because of the small number of studies in the review. In the presence of unexplained heterogeneity, we proceeded with caution, pooling data for summary LRs with a random effects model in line with the current recommendation but not sensitivity or specificity measures.46 Our inferences are supported by the most methodologically sound selected studies, particularly those with an appropriate gold standard.

Our systematic review informs the design of the technology assessment required to develop a strategy for administering antibiotic prophylaxis according to intrapartum maternal testing to prevent neonatal GBS. The assessment should be undertaken in a hierarchical fashion, based on methodologically robust frameworks for evaluation of tests,72,73 comparing tests based on real-time PCR and OIA. Initially, their accuracy in detecting GBS colonization among women in labor should be established, taking specimens from the lower vagina without the need for speculum examination. The role of rectal swabs, emphasized as an independent predictor of neonatal GBS,16,37 needs to be considered in this assessment, because it has been neglected by existing studies. The effect of prior risk categorization on test accuracy, that is, spectrum variation,44 should be examined using multivariable analysis.74,75 In addition, the acceptability of intrapartum testing for GBS colonization to different social and ethnic groups should be examined. Finally, cost-effectiveness of intrapartum testing and targeted prophylaxis for preventing neonatal GBS should be evaluated in light of the outcome of the accuracy comparison of real-time PCR vis-à-vis OIA, comparing it with others strategies,1,4 using either decision analytic modeling or a direct randomized, controlled trial. In fact, this terminal analysis would yield highly pertinent, potentially practice changing results for communities that had adopted a specific strategy (eg, the United States, Canada, or Australia). In light of the emerging evidence from our review, we believe that any screening recommendation for practice needs to be reevaluated.


   ACKNOWLEDGMENTS
 
We thank the United Kingdom National Health Service Health Technology Assessment program for funding a primary study (grant 02/38/04) on GBS intrapartum screening.

We thank Dr Jim Gray, consultant microbiologist at Birmingham Women's Hospital, for expert advice and contact with manufacturer. We also thank Mary Publicover, head librarian at Birmingham Women's Hospital Education Resource Centre, for assistance in on-line search and retrieval of articles.


   FOOTNOTES
 
Accepted Sep 20, 2005.

Address correspondence to Honest Honest, MBChB, Department of Obstetrics and Gynecology, Birmingham Women's Hospital, Edgbaston, Birmingham B15 2TG, United Kingdom. E-mail: honest.honest{at}bwhct.nhs.uk

The authors have indicated they have no financial relationships relevant to this article to disclose.

* Refs 8,25,26,53,54,56–60,62, and 69. Back

{dagger} Refs 25,26,28,53–56,58,59,62, and 69. Back


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PEDIATRICS (ISSN 1098-4275). ©2006 by the American Academy of Pediatrics

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