Sensitivity of intrapartum group B streptococcal screening and in vitro comparison of four rapid antigen tests

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European Journal of Obstetrics & Gynecology and Reproductive Biology 56 (1994) 21-26

ELSEVIER

Sensitivity of intrapartum group B streptococcal screening and in vitro comparison of four rapid antigen tests Albert H. Adriaanse*a, Harry L. Muytjensb, Louis A.A. KollCe”, Jan G. Nijhuis”, Tom K.A.B. Eskesa “Department

of Obstetrics

and Gynecology,

bDepartment

SI Radboud,

of Medical

Microbiology.

‘Department

P.O. Box 9101, 6500 HB Nijmegen.

of Pediatrics,

University

Hospital

Nijmegen

The Netherlands

Accepted 8 April 1994

Abstract Objectives:

To

evaluate the sensitivity of intrapartum

screening for group B streptococcal (GBS) colonization and to compare

4 rapid GBS antigen tests in vitro. Design: Two swabs of the lower vagina of 769 parturients were taken; one swab was cultured, the other was frozen at -70°C until antigen testing with the Group B Strep Test (Quidel) of the culture positive samples was performed. The Quidel test was then compared with 3 other rapid GBS antigen tests in vitro: Wellcogen Strep B (Wellcome Diagnostics), Slidex mtningite Strepto B (bioMCrieux) and ICON Strep B (Hybritech). The supernatant of 29 GBS cultures in Todd-Hewitt broth was tested in bacterial concentrations of 106, lo’, and lo* Colony-Forming Units (CFU)/ml, respectively. Results: Lower vagina GBS carrier rate was 13.4% (103/769) and heavy colonization (growth density 3 and 4 on blood agar plates) was found in 5.2% (40/769). The Group B Strep Test detected 11% (1 l/103) of GBS carriers, with a sensitivity for heavy colonization of 25% (10/40). In vitro none of the tests scored positively with a concentration of lo6 CFU/ml, while with 10’ CFU/ml the enzyme immunoassay tests (Quidel, Hybritech) were more sensitive (McNemar test, P < 0.05) than the latex agglutination tests (Wellcome Diagnostics, bioMerieux). Conclusions: Although in vitro the enzyme immunoassay tests are more sensitive than the latex agglutination tests, sensitivity in vivo is too low to recommend the use of rapid antigen tests for general screening. Keywords:

Group B streptococcus; Screening; Rapid detection; Latex agglutination;

1. Introduction

Group B beta-hemolytic streptococcus (GBS, Streptococcus agalactiae) is recognized as a major cause of neonatal sepsis and accounts for lo-25% of postpartum maternal bacteremia [1,2]. Invasive neonatal group B streptococcal infections present themselves either as early (usually within 24 h) or late (after 7 days) onset disease. Two thirds of cases are early onset infections, usually acquired by vertical transmission from the mother’s genital tract. Asymptomatic vaginal colonization with GBS occurs in 4-40% (usually about 20%) of pregnant women, depending on the population studied and culture technique used. The highest genital tract iso* Corresponding author. 0028-2243/94/$07.00 SSDI

0

0028-2243(94)01865-5

1994 Elsevier

Science Ireland

Enzyme immunoassay

lation rates are reported from the lower vagina (introitus) and lowest from the cervix [ 1,2]. In infants born to colonized mothers vertical transmission has been shown to range from 40%--70% (mean, 50%), the risk being greater in the presence of a high genital inoculum. Despite high prevalence rates for vertical transmission, the incidence of early onset GBS infection is only l-10 per 1000 live births. However, mortality is significant, ranging from 50%-70% in older studies and from 13%-37% more recently [l]. About half of the infants who survive GBS meningitis are left with permanent neurologic sequelae. There is no consensus on the best approach to prevent early onset GBS infection. Although conflicting results have been reported, single-dose penicillin prophylaxis in infants cannot be recommended [3-51. Several studies

Ltd. All rights reserved

22

A.H. Adriaanse et al. /Eur. J. Obstet. Gynecol. Reprod. Biol. 56 (1994) 21-26

have demonstrated that intrapartum antibiotic therapy (ampicillin, penicillin G) reduced vertical transmission of GBS [6-91. An alternative approach to chemoprophylaxis is vaginal chlorhexidine disinfection during labor [lo- 121.Infants of mothers with low levels of antibodies against GBS are at risk and a program of active immunization aimed at pregnant women would probably be most efficacious in controlling perinatal GBS disease. However, an effective vaccine is not available at present [13]. For the time being, intrapartum chemoprophylaxis in selected high risk parturients is the method of choice for preventing GBS infections. Apart from other risk factors, GBS carrier state in pregnant women plays a crucial role. A selective culture is the ‘gold standard’ for intrapartum screening but the results usually take too long to be of clinical importance. Therefore, several ‘rapid’ GBS screening methods have been developed and evaluated in the last two decades. Most techniques have been shown to be either insensitive or complicated to perform and take too long for implementation. Among the really rapid tests (result within 2 h) are latex agglutination and enzyme immunoassay. These rapid antigen detection tests appear to be quite specific but the question still remains whether they are sensitive enough to be instituted as the keystone of a large-scale preventive protocol. The purpose of this study was to evaluate the sensitivity of intrapartum GBS screening and to compare four rapid group B streptococcal antigen tests in vitro. 2. Materials and methods 2.1. Collection of material The study took place at two hospitals in the city of Nijmegen, The Netherlands. The protocol, which was part of a bigger study, was approved by the ethics committees of both hospitals and informed consent was obtained from the participating women. Two swabs of the lower vagina of 769 parturient women whose GBS carrier state was unknown were taken in a fixed order. The first, rayon tipped plastic swab, was stored at 4°C and frozen at -70°C within 24 h. The second, cotton tipped wooden swab, was put in Todd-Hewitt broth, stored at 4°C and plated semiquantitatively on 5% defibrinated sheep blood agar within 24 h. The blood agar plates were incubated for 48 h at 37°C. After plating, the swabs were put in a selective enrichment broth consisting of Todd-Hewitt broth with 15 pg nalidixic acid per ml and 8 pg gentamicin per ml, inhibiting the growth of Gram-negative Enterobacteriaceae and other bacteria in the normal genital tract flora that could interfere with the recovery and identification of GBS. After overnight incubation at 37°C the swabs were plated on blood agar and incubated at 37°C for

another 24 h. Confirmation of identified GBS was done by the CAMP-reaction and resistance to bacitracin on Casman medium base with 5% delibrinated sheep blood and, if necessary, agglutination with Streptex latex suspension (Wellcome Diagnostics). After 48 h incubation the growth density (1, 2, 3, or 4) on the directly plated blood agar plates was determined. If GBS were only isolated from the enrichment broth, this was scored as growth density 0. 2.2. Determination of sensitivity When all culture results were available, the frozen swabs of parturients with positive GBS culture were defrosted and tested with the Group B Strep Test (Quidel), an enzyme immunoassay. The tests were always performed by the same technician in accordance with the manufacturer’s instructions. The swab samples were extracted with extraction reagents and the extracted fluid samples transferred to a test cartridge containing a filtration membrane coated with rabbit polyclonal antibodies to GBS. Filtration occurred by gravity and GBS antigen present in the sample bound to the antibodies on the surface of the membrane. Antibody-enzyme conjugate, wash solution, and an enzyme substrate solution were added to develop and stabilize the test result. A positive result was indicated by a distinct blue circle on the test cartridge membrane, a negative result by a negative sign without a blue circle. A positive GBS control was included in the kit. The entire test could be performed in less than 10 min. Refrigeration of the samples does not affect test results because the enzyme immunoassay test identifies bacterial antigens regardless of the presence of live organisms. Moreover, the GBS is resistant to freezing and survives well [ 141. Nevertheless, to detect any possible loss of antigen-expressivity by freezing the swab, we compared freshly obtained and prefrozen specimens. For this purpose 3 identical rayon tipped swabs were taken from the lower vagina in 10 known GBS carrier women. One swab was cultured as mentioned above, one was tested immediately, the third being frozen at -70°C and tested later. 2.3. In vitro comparison of the antigen tests To compare 4 different rapid group B streptococcal antigen tests we tested the supernatant of 29 GBS cultures in Todd-Hewitt broth in 3 different bacterial concentrations with each of the tests. The strains used were 28 randomly chosen patient strains from our frozen stock and 1 American Type Culture Collection strain (ATCC 13813). The three concentrations tested contained 106, 107, and lo8 Colony-Forming Units per ml (CFU/ml). For each test 50 ~1 of the solutions was used. A growth density 2 on the blood agar plate corresponded to lo6 CFU/ml, while growth densities 3 and 4 cor-

A.H. Adriaanse et al. /Eur. Table 1 Results of lower vaginal culture 103 GBS carrier parturients

and Group

No. of swabs positive

‘Growth density on blood agar

Culture

B Strep Test (Quidel)

Quidel

(%)”

positive Quidel

1

21 (2.7) 15 (2.0)

2 3 4

27 (3.5) 22 (2.9) 18 (2.3)

5 5

4 23b 28b

103 (13.4)

11

11c

0

Total “Percentage bSensitivity

I

of total cultures. for heavy colonization

(growth

Group B Strep Test (Quidel). The cultures of 103 of the 769 laboring women revealed GBS, the GBS carrier rate in the lower vagina being 13.4%. Growth densities (0, 1, 2, 3, and 4) on blood agar plates among carriers were distributed as shown in the table. Heavy colonization (growth density 3 and 4) was found in 5.2% (40/769) of the women. Overall, 11 of the 103 GBS carriers (11%; 95% confidence interval, 5-19%) were detected by the Group B Strep Test (Quidel); when restricted to heavily colonized carriers only (10/40), the sensitivity of the test was 25% (95% confidence interval, 12-42%). The swabs of 10 known GBS carriers showed identical results in the Group B Strep Test when tested immediately and after having been frozen. No loss of antigen-expressivity was found. Table 2 shows the results of the in vitro comparison of 4 rapid group B streptococcal antigen tests. With a bacterial concentration of lo6 CFU/ml, each test scored negatively for all 29 strains. With a concentration of IO’ CFU/ml both latex agglutination tests were negative for all 29 strains. The Group B Strep Test (Quidel) was positive for 7 strains (4 slightly positive and 3 positive). The results of the ICON Strep B (Hybritech) were: 20 positive (5 slightly positive, 14 positive and 1 clearly positive). The concentration of 10’ CFU/ml seems to be distinctive: the enzyme immunoassay tests are more sensitive than the latex agglutination tests and the ICON Strep B is more sensitive than the Group B Strep Test (McNemar test, P < 0.05). When testing with a concentration of lo8 CFU/ml the ICON Strep B resulted in most positive results (29 strains), followed by the Group B Strep Test (27 strains), Slidex meningite Strepto B (27 strains) and Wellcogen Strep B (20 strains), respectively.

in

Sensitivity (“XI)of

by:

density

3 and 4): 25%,

95% confidence interval 12-42%. c95”h confidence interval 5- 19%.

responded to 10’ and 10’ CFU/ml, respectively. Two latex agglutination tests were performed, namely the Wellcogen Strep B (Wellcome Diagnostics) and the Slidex meningite Strepto B (bioMCrieux) and two enzyme immunoassays, the Group B Strep Test (Quidel) and the ICON Strep B (Hybritech). Tests were performed following the manufacturer’s instructions by the same technician. A positive control was included in all test kits. Test results were scored as negative, slightly positive, positive, or clearly positive. 2.4. Statistical method The McNemar test for paired samples was used to compare the results of the tests.

4. Discussion

3. Results

A program of disease prevention requires reliable identification of persons at risk and availability of effec-

Table 1 shows the results of vaginal cultures and the

Table 2 In vitro results of 4 rapid antigen Test

tests for 29 CBS strains

Latex agglutination Wellcome

(CFU/ml)

23

J. Obster. Gynecol. Reprod. Biol. 56 (1994) 21-26

IO6

+++

Enzyme immunoassay bioMCrieux

10s

106

10’6

10s

29

29

10’”

10s

29

3 4 7 22

23 3 1 27 2

23 4

29

29

27 2

Hybritech

106

1 20 9

tests

Quidel

14 5

++ + Total +

concentrations

tests

Diagnostics 10’a

in 3 bacterial

106

10’a

108 26 3

29

1 14 5 20 9

+++, ++, +, and - denote a clearly positive, a positive, a slightly positive, and a negative result, respectively (degree of color reaction). aAt a concentration of 10’ CFU/ml the enzyme immunoassay tests are more sensitive than the latex agglutination tests and the Hybritech more sensitive than the Quidel test (McNemar

test, P < 0.05).

29 0

test is

A. H. Adriaanse et al. /Eur. J. Obstet. Gynecol. Reprod. Biol. 56 (1994) 21-26

24

tive preventive treatment. Effective therapy for prevention of early onset neonatal GBS sepsis is available, but identification of parturients at risk of transmiting the disease still poses a problem. Risk factors such as low birthweight, preterm labor, prolonged rupture of membranes, intrapartum fever, prolonged labor and others should be recognized [2,15], while intrapartum screening for GBS carriership would be ideal. Screening is generally defined as the presumptive identification of a disease or defect by the use of an examination or test procedure that can be applied rapidly, easily, and relatively inexpensively. The GBS antigen kits can be performed within 10 min and are easy to use, although it is questionable whether this counts for a busy clinician at night-time hours as well as for a trained laboratory technician. The costs are relative, depending on the prevalence of GBS, management protocols and prevention of morbidity in a specific clinical setting. A test searching for a serious process in which nontreatment would have greater consequences than treatment would need to be quite sensitive, to avoid placing patients at risk because of non-treatment. We found a disappointing overall sensitivity of 11% (25% for heavy

Table 3 Performance

specifications

Method

Reference

Latex agglutination tests Vaginal 8 Vaginal Vaginal Vaginal Cervical Cervical/vaginal High vaginal Vaginal Cervical/vaginal Vaginal Vaginal Cervical/vaginal Vaginal

17 21 25 26 27 28 29 31 32 32 33 34

Enzyme immunoassay tests Vaginal 17 Cervical I8 Cervical/vaginal 19 20 Vaginal Vaginal 21 Vaginal 22 Cervical/vaginal 23 Cervical 24 Cervical 24

from published

evaluations

colonization) using the Group B Strep Test (Quidel) compared with a selective GBS culture. The built-in positive control gives such a distinct degree of color reaction that it is only equalled by the samples of very heavily colonized parturients. We found quite a discrepancy between the performance of the Quidel test for heavy vaginal colonization compared with the in vitro results. Most probably the lower in vivo sensitivity is the result of interference factors that exist for vaginal swabs: contamination with blood, mucus, and amniotic fluid. These factors are likely to negatively influence the antigen-expressivity of a vaginal GBS population, compared with a more standardized population growing under optimal conditions in Todd-Hewitt broth. Moreover, it is known that rupture of the membranes in the in vivo situation may cause a ‘washout’ effect, reducing the bacterial concentration [ 161.Information from the literature on the discrepancy between rapid GBS antigen testing in vivo and in vitro is scant. A few authors reported results that seem to support our findings [ 17,181. Sensitivities of rapid GBS antigen tests reported in the literature show a wide variation (Table 3) [8,17-341. The

of rapid GBS antigen

tests Sensitivity (heavy colonisation)

Specificity

Remark

1585 I05 6 52 19 37 22 64 92 225 233 25 197

26% 15% 33% 40% 58% 62% 14% 19% 30% 20% 24% 88% 92%

100% 99% 95% 99% 93% 99% 93% 99% 93% 99% 99% 99% 98%

A

I05 50 20 30 6 98 19 18 I7

22% 24% 60% 33% 33% 9%

Trademark

No. women

No. culture

Streptolatex Streptex Bactigen Bactigen Bactigen Bactigen Wellcogen Streptex Directigen Bactigen Directigen Wellcogen Streptex

8977 1062 250 464 431 344 200 434 314 4251 4251 500 II00

Equate Equate Equate ICON Equate ICON Quidel ICON Quidel

1062 660 I31 300 250 424 331 180 189

Remarks: A: preincubation in enrichment moderate/heavy colonization.

broth

for 5-7

h; B: preincubation

pos.

(29%) (67%) (95%) (50%) (63%) (76%) (57%) (62%)

(37%) (80%) (lOO%)

( lOO%) (89%) I I% (100%) 24% ( 100%)

for 60 mitt; C: preincubation

B C

99% 95% 92% 95% 99% I 00% 99% 100% 100% for 8-12

h; D: study population:

A.H. Adriaanse et al. /Eur. J. Obstet. Gynecol. Reprod. Biol. 56 (1994) 21-26

highest overall sensitivities are found after a preincubation step, thereby limiting the rapid character of the test [33,34]. It should be noted that some of the studies mentioned used non-selective blood agar rather than selective medium to culture GBS. It is therefore possible that the actual prevalence of colonization is higher, making the true sensitivities of the rapid tests even lower. Furthermore, the prevalence of GBS carriership among parturients will turn out to be higher when more sites (cervix, rectum) are cultured. Some authors take the view that identification of heavily colonized parturients rather than all colonized parturients may be adequate while others point to the experience that, although heavy colonization definitely is a high risk factor, 20-50% of colonized women will be missed and even scant maternal colonization can result in transmission of GBS to the neonate [l&19,22,35,36]. Although our in vitro comparison of rapid GBS antigen tests shows that the enzyme immunoassay tests are more sensitive than the latex agglutination tests, we conclude that the sensitivity in vivo still is too low to recommend the use of rapid antigen tests for general screening. The search for a more sensitive test or method should continue. Acknowledgments

This study was supported by grant No. 28-2011 from the Dutch ‘Praeventiefonds’. The Group B Strep Test (Quidel) was kindly supplied on request by Tecnolab International BV, Alkmaar, The Netherlands.

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