screening pregnant women for group b streptococcus infection between 30 and 32Â weeks of pregnancy...

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CLINICAL ARTICLE

Screening pregnant women for group B streptococcus infection between30 and 32 weeks of pregnancy in a population at high riskfor premature birth

Boldizsar Horvth a,b,, Magdolna Grasselly b, Tams Bdecs a, Imre Boncz a, Jzsef Bdis a

a Faculty of Health Sciences, University of Pcs, Szombathely, Hungaryb Markusovszky Teaching Hospital, Szombathely, Hungary

a b s t r a c ta r t i c l e i n f o

Article history:

Received 6 September 2012Received in revised form 9 January 2013

Accepted 11 March 2013

Keywords:

Neonatal group B streptococcal infection

Screening for group B streptococcus

3032 weeks of pregnancy

Objective: To assess the benets of a chemoprophylaxis program based on screening women for group B

streptococcus (GBS) infection between 30 and 32 weeks of pregnancy in a population with a high rate of pre-mature births. Methods: From 1995 to 2011, 24 950 women were screened for GBS infection between 30

and 32 weeks of pregnancy at Markusovszky Teaching Hospital, Szombathely, Hungary. Those who tested

positive, and those who tested negative but were at risk of infecting their newborns, underwent intrapartum

prophylaxis. Neonatal outcomes were compared with those ofa historical cohortthat underwent no screening

or treatment, and with those published in CDC/ACOG guidelines recommending screening closer to term.

Results: There were 63 infected newborns (0.2%) in the study cohort, and 1 of 8 with sepsis died. There

were 149 infected newborns (0.7%) in the historical cohort, and 29 of 31 with sepsis died.Conclusion:Screening

women early in a population with a high rate of premature births may simplify preterm labor management.

It results, however, in a higher incidence of early onset neonatal GBS disease than when screening is done

closer to term.

2013 International Federation of Gynecology and Obstetrics. Published by Elsevier Ireland Ltd. All rights reserved.

1. Introduction

Over the last 3 decades, infection with group B Streptococcus

(GBS) species has been among the most common causes of neonatal

morbidity and mortality in the high-income countries. Since 90% of

early cases of GBS infection occur within the rst 24 hours postpar-

tum, the bacteria are probably transmitted in utero[115].The bacte-

ria are present in the lower digestive tract of 15% to 35% of humans,

but the incidence and distribution of GBS infection show ethnic

and geographic variations[1,2,8,11,13]. The incidence of GBS infec-

tion is higher among women who have multiple sexual partners

and also among women of lower socioeconomic backgrounds, and it

seems to be associated with Chlamydia, Trichomonas, Ureaplasma, or

Mycoplasma infection[1,2,11]. Vaginal GBS infection is intermittent

whereas anorectal infection is more constant [1619]. The rate of

mother-to-infant transmission is generally low, as only 1% to 2% of

the newborns of infected women develop GBS infection. The risk

factors for perinatal infection are well documented [2022]. The

most important ones are premature birth and premature rupture of

membranes (PROM).

In response to the continuing burden of perinatal disease due to

GBS and the inconsistent implementation of prevention practices,

the US Centers for Disease Control and Prevention (CDC) and the

American College of Obstetrics and Gynecology (ACOG) publishedconsensus guidelines in 2002 and revised them in 2010 [1221].

The revised guidelines recommend screening all women between

35 and 37 weeks, and administering intrapartum prophylaxis in

those found to be infected.

Until 1995, there had been no screening or prophylactic protocols

at the authorsinstitution. The factors taken into consideration, when

a screening strategy was developed that year, included not only cost

and feasibility but also Hungarys high rate of premature births. As a

result, an earlier time range, between 30 and 32 weeks, was chosen

for GBS screening.

2. Materials and methods

From January 1, 1995, through December 31, 2011, a prospective

study based on a modied screening-based protocol was carried out

at Markusovszky Teaching Hospital, Szombathely, Hungary, with

24950 women and their newborns. All pregnant women attending

the hospitals prenatal clinic were asked to participate and none re-

fused. Most were middle- to low-income and all had received some

prenatal care. Approval from the institutional ethics committee and

written consent from the participants were obtained.

Physicians collected samples from the participants distal vagina

(without speculum placement) and rectum approximately between

30 and 32 weeks. Swabs (Transwab for Aerobes and Anaerobes; Medi-

cal Wire and Equipment Company, Corsham, UK) were used for collec-

tion, and the samples were then placed in Stuart transport medium and

International Journal of Gynecology and Obstetrics 122 (2013) 912

Corresponding author at: Faculty of Health Sciences, University of Pcs, 9700,

Szombathely, Jkai ut 14. Hungary. Tel.: +36 94 311 650; fax: +36 94 0327 873.

E-mail address:[email protected](B. Horvth).

0020-7292/$ see front matter 2013 International Federation of Gynecology and Obstetrics. Published by Elsevier Ireland Ltd. All rights reserved.

http://dx.doi.org/10.1016/j.ijgo.2013.01.027

Contents lists available at SciVerse ScienceDirect

International Journal of Gynecology and Obstetrics

j o u r n a l h o m e p a g e : w w w . e l s e v i e r . c o m / l o c a t e / i j g o

19/08/2014
http://dx.doi.org/10.1016/j.ijgo.2013.01.027http://dx.doi.org/10.1016/j.ijgo.2013.01.027http://dx.doi.org/10.1016/j.ijgo.2013.01.027mailto:[email protected]://dx.doi.org/10.1016/j.ijgo.2013.01.027http://www.sciencedirect.com/science/journal/00207292http://crossmark.crossref.org/dialog/?doi=10.1016/j.ijgo.2013.01.027&domain=pdfhttp://www.sciencedirect.com/science/journal/00207292http://dx.doi.org/10.1016/j.ijgo.2013.01.027mailto:[email protected]://dx.doi.org/10.1016/j.ijgo.2013.01.027


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sent to the laboratory for culture. A red label markedGBS positive was

afxed to the prenatal records of infected participants to notify labor

and delivery personnel[23].

The protocol was designed so that both GBS-positive women

and women with risk factors for the transmission of early onset

GBS disease would automatically receive intrapartum antibiotic

prophylaxis. Moreover, special attention was paid to women who

seemed likely to undergo a premature delivery. The intravenous

prophylactic regimen administered during labor was 2 g of ampicillin,followed by 1 g of ampicillin every 4 hours until delivery. Patients aller-

gic to penicillin received erythromycin or clindamycin intravenously

in equivalent dosage.

Neonatal GBS infection was recorded as denite or probable. It

was considered denite if there were clinical signs of GBS disease

and/or if blood, cerebrospinal uid, urine, tracheal aspirate, or lung

tissue were found positive for GBS. It was considered probable if

there were clinical signs of GBS disease and at least 1 of the following:

increased or decreased blood neutrophil count; high count of immature

neutrophils; high immature-to-total neutrophil ratio; and abnormal

cerebrospinal uidndings, such as increased protein or decreased glu-

cose levels or pleocytosis[20].

Only infections deemed denitive were included in the analysis.

For binary variables, statistical evaluations were performed using

the 2 test or the Fisher exact test. To test associations among multi-

ple variables, logistic regression was performed. All analyses were

performed using SPSS version 11 (IBM, Armonk, NY, USA). P b0.05

was considered signicant.

3. Results

Data from a historical cohort of 19722 womenand 19722newborns

were collected prospectively from February 1, 1984, through December

31, 1994. These women did not undergo GBS screening and received no

intrapartum prophylaxis. Over the decade of data collection, 149 new-

borns (0.76%) were found to be infected with GBS, approximately 15

peryear. Of the97 bornprematurely, 31 incurred sepsis(approximately

3 per year), 29 died, and 21 lived with lasting sequelae ( Table 1).

Between January 1, 1995, and December 31, 2011, data were alsocollected prospectively for 24950 women and 25857 newborns

(there were 789 twins and 59 triplets). All women underwent GBS

screening and 5788 (23.2%) were found positive for GBS. Intrapartum

prophylaxis was provided selectively, according to the study protocol.

Infection with GBS was detected during delivery or in the early

neonatal period in 63 newborns (0.24%). Of 8 newborns (0.03%) who

incurred neonatalsepsis, the only onewho died wasmarkedlyprema-

ture, with a birth weight of 1200 g at a gestational age of 27 weeks.

Because delivery occurred before the prescribed screening period,

the mother had not been evaluated for GBS. Regarding late-onset GBS

infection, no case has occurred at Markusovszky Teaching Hospital in

the last 16 years (Table 1).

The differences in incidence of early onset GBS infection

(Pb0.001) and infection severity (P b0.001) noted in the historical

and the present studies are statistically signicant. For a more mean-

ingful result, however, the ndings of the present study were also

compared with ndings reported in the CDC/ACOG guidelines,

which recommend screening between 35 and 37 weeks. The 0.24%

rate of early onset infection in the present study was much higherthan the 0.034%0.037% in the CDC/ACOG reports [21], which was

probably due to the nonprovision of a prophylactic treatment to

women who became infected closer to term.

Of the 149 cases of neonatal GBS infection in the historical cohort,

97 occurred in preterm newborns. By contrast, only 1 premature new-

born was infected at birth in the present study, a result to which

maternal screening must have contributed. In the present study, 55

(87%) of the 63 women whose newborns were infected presented 2

or more factors predicting severe neonatal GBS disease, and these in-

cluded 23 women not found positive at screening (Table 2). Premature

labor and PROM were the 2 most important risk factors ( Table 2).

As was suggested by the higher incidence of neonatal infection in

the present study than in the reports that accompany the revised

2010 CDC/ACOG guidelines, there was a high rate of women falsely

categorized as not infected when they were admitted for delivery.

Since only 29 (46%) of the 63 women whose newborns had a GBS

infection were GBS positive between 30 and 32 weeks, the other 34

(54%) must have become infected closer to term. Again, not treating

this group no doubt accounts for the higher incidence of early onset

infection in the present study than in the CDC/ACOG reports.

Antibiotic prophylaxis was administered either not early enough

or too late (because of a very short labor and delivery duration) in

42 of the 63 mothers of newborns with GBS infection, and in 6 more

women the duration of antibiotic prophylaxis was also too short.

Thus, 48 (76.2%) of the 63 women who received prophylaxis had a

dose-to-delivery interval of less than 4 hours (Pby the 2 test, 0.43;

odds ratio, 1.58; condence interval, 0.505.0). There were only 5

cases of clinically observed GBS disease in the newborns of women

who received prophylaxis over more than 12 hours. There was notreatment failure in the penicillin-allergic women who received

erythromycin or clindamycin.

Table 1

Prevalence of neonatal GBS infection without (1984

1994) and with (1995

2011) pro-phylactic maternal treatment during labor and delivery.a

Study period Newborns

infectedbForm of GBS infection Newborn

deathsSepsisc Pneumoniad Othere

19841994

(N = 19722)

149 (0.75) 31 (0.16) 88 (0.45) 30 (0.15) 29

19952011

(N = 25857)

63 (0.24) 8 (0.03) 19 (0.07) 35 (0.14) 1f

Abbreviations: CI, condence interval; GBS, group B streptococcus; OR, odds ratio.a Pvalues were calculated by the 2 test; other values are given as number or num-

ber (percentage).b P= 0.001; OR, 0.36; 95% CI, 0.260.49.c P= 0.001; OR, 0.27; 95% CI, 0.120.58.d P= 0.001; OR, 0.19; 95% CI, 0.110.32.e P= 0.90; OR, 0.97; 95% CI, 0.581.62.f

Delivery occurred before screening for GBS infection could take place.

Table 2

Numbers of neonatal GBS infection according to maternal risk factors.

Risk factora Newborns

infected

(n = 63)

Mother tested

positive for GBS

at 32 wk (n = 35)

Mother tested

negative for GBS

at 32 wk (n = 28)

Premature deliveryb 13c 5 8

Multiple gestation 3 2 1

PROM 28d 16 12

PPROM 6e 1 5

Temperature duringlabor >37.5 C 3 0 3

Diabetes 8 5 3

Polyhydramnios 8 3 5

1 or no risk factor 8 3 5

2 or more risk factors 55f 30 25

Abbreviations: CI, condence interval; GBS, group B streptococcus; OR, odds ratio;

PPROM, preterm premature rupture of membranes (occurring 1218 h before onset

of labor); PROM, premature rupture of membranes (occurring 312 h before onset of

labor).a More than 1 risk factor was possible.b Maternal screening was not performed in 6 cases.c P= 0.18 by the 2 test; OR, 0.32; 95% CI, 0.061.83.d P = 0.10 by the 2 test; OR = 2.55; 95% CI, 0.837,80 (P = 0.16 by the Fisher

exact test).e P = 0.13 by the 2 test; OR = 0.20; 95% CI, 0.021.95 (P = 0.18 by the Fisher

exact test).f

P= 0.51 by the 2

test; OR = 2.30; 95% CI, 0.19

26.6.

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The risk stratication applied in the administration of antibiotics

had a benecial effect on the incidence and severity of neonatal GBS

infection. Serious neonatal sepsis developed in only 8 newborns, 5 of

whom were born at term and weighed more than 3000 grams at

birth. Only 1 of these 8 newborns was born prematurely, and its death

was the only neonatal death from GBS infection at Markusovszky

Teaching Hospital in the past 16 years. In the prior decade, 29 neonatal

deaths from GBS infection were reported.

Of the 8 women whose newborns incurred sepsis, only 2 testedpositive for GBS between 30 and 32 weeks, but 7 presented 2 or

more factors predicting GBS disease in their newborns. The prophy-

lactic antibiotic treatment could not be administered in 4 women

because of a very short labor and delivery duration. The only newborn

who died was severely premature, with a gestational age of only

27 weeks and a very low birth weight at delivery, and its mother

was probably heavily infected with GBS. All other affected newborns

recovered without lasting adverse effects. The mean recovery period

was 15.6 days (range, 1036 days).

4. Discussion

Most bacterial infections in newborns arise from maternal vaginal

colonization, and GBS causes most cases of neonatal morbidity and

mortality in high-income countries. Transmission probably occurs

during vaginal delivery or because an ascending infection eventually

affects the fetal membranes[2,5,7,17,21,24]. Risk factors for transmis-

sion include prematuredelivery; multiple gestation; PROM; long labor

duration, especially when PROM has occurred; maternal temperature

during labor; diabetes; and polyhydramnios[14]. The 2 most impor-

tant of these risk factors are premature delivery and PROM [15].

The present prospective study spanned 16 years. It was designed

to conrm the expected benet of instituting a GBS screening and

prophylaxis program at Markusovszky Teaching Hospital. It was also

designed to evaluate the effectiveness of early screeningbetween

30 and 32 rather than 35 and 37 weeks, as recommended by the

CDC/ACOG guidelinesin women from populations where premature

births are common.

As mentioned, screening consisted of establishing the presence orabsence of GBS by growing cultures from samples obtained from the

rectum and distal vagina. The prevalence of infection between 30

and 32 weeks was 23.2%, a rate consistent with the rate reported

for the general population [112]. Premature delivery being known

as an important risk factor for neonatal GBS infection, the screening

protocol was tailored and implemented to account for the rate of

premature deliveries in Hungary, which by some accounts is as high

as 10%. Over the 16 years of the study, labor and delivery personnel

were helped greatly by being aware of each womans presumed GBS

status before delivery. They could initiate a prompt antibiotic inter-

vention as part of the preterm labor management protocol.

Markusovszky Teaching Hospital was an ideal setting to study the

benets of a screening and treatment protocol. The institution had no

screening or prophylactic program prior to 1995, and the historicalstudy showed that the rate of neonatal sepsis due to GBS was relatively

high, 1.6 per 1000 births, during the decade preceding the start of

the present study. Implementing simple strategies conrmed, not sur-

prisingly, the generally accepted tenet that GBS screening and selective

intrapartum prophylaxis signicantly improved neonatal outcomes.

The incidence of early onset infection and the severity of infection

were signicantly less in the study cohort than in the historical cohort.

The prevalence of early onset neonatal disease was 0.24% in the

present study and the range published with the CDC/ACOG guidelines

was 0.034% to 0.037% [21]. The higher rate in the present study is

not likely attributable to the high rate of prematurity in Hungary, as

screening was done earlier to compensate for this factor, a strategy

that perhaps succeeded because only 1 infected newborn was prema-

ture. The higher incidence is more likely due to the high rate of results

falsely considered negative because of early screening. As only 29 of

the women whose newborns were infected with GBS were GBS posi-

tive between 30 and 32 weeks, some of those who tested negative

must have become GBS carriers closer to term, as has been suspected

and reported in the literature[14,21].

The screening protocol may need to be reconsidered as a result

of the studys ndings. The earlier screening schedule may remain

in effect for women who are at increased risk for premature delivery

(the known risk factors being prior premature delivery, older mater-nal age, multiple gestation, maternal chronic conditions, and poor

prenatal care); and if the pregnancy proceeds further in these women,

rescreening may be performed between 35 and 37 weeks. For women

with no known risk factors for premature delivery, the standard, CDC/

ACOG-recommended schedule may be adopted.

The present study also assessed the benets of administering

intrapartum treatment to both GBS-positive women and women

who were risk-stratiedas being likelyto have a newborn with severe

GBSdisease. Of the63 women with infected newborns, 55 (87%) had2

or more risk factors for severe neonatal GBS disease and premature

labor and PROM were the 2 most important. Data analysis suggests

that completion of the intrapartum antibiotic regimen and time from

administration initiation to delivery were important factors for suc-

cessful treatment. Ineffectiveness in 48 of the 63 cases was probably

due to too short a treatment duration.

In summary, vaginal infection with CBS is an important risk factor

for neonatal infection that can largely be prevented by selective

intrapartum prophylaxis. Findings from the present study have led

to conclusions and recommendations that other institutions might

also want to consider. Consideration should be given to initiate a pro-

phylactic antibiotic protocol immediately after admission in infected

women, particularly those at risk of having severely infected new-

borns, so that a sufcient number of doses can be administered prior

to delivery.

Screening earlier than is recommended by the CDC/ACOG guide-

lines aims at meeting the needs of the estimated 10% of women

who go into premature labor in Hungary. However, it leads to catego-

rize as free of infection women who may become infected later in

their pregnancya situation that, in turn, leads to a higher rate ofearly onset neonatal GBS disease. On the other hand, screening closer

to term ignores the needs of this vulnerable group. Screening be-

tween 30 and 32 weeks could, therefore, be entered in the protocol

as an additional, rather than alternative, procedure for women with

known risk factors for premature delivery. This solution would ensure

a positive cost/benet ratio. To aid in CBS screening and prevention,

public health agencies might considerer supporting efforts toward

the development of both a rapid diagnostic test and a polyvalent

GBS vaccine[24].

Conict of interest

The authors have no conicts of interest.

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