Original Article

Changes in Early-Onset Group B Beta Hemolytic Streptococcus Disease With Changing Recommendations For Prophylaxis

¹Department of Pediatrics, Division of Neonatology, Golisano Children's Hospital at Strong, University of Rochester School of Medicine and Dentistry, Rochester, NY, USA

²Department of Microbiology, Golisano Children's Hospital at Strong, University of Rochester School of Medicine and Dentistry, Rochester, NY, USA

Correspondence to: Ronnie Guillet, MD, PhD, Department of Pediatrics, Division of Neonatology, Box 651, University of Rochester School of Medicine, 601 Elmwood Avenue, Rochester, NY 14642, USA

^aCurrent address: Pediatrix Medical Group of South Carolina, Spartanburg Regional Medical Center, 101 East Wood Street, Spartanburg, SC 29303, USA.

Abstract

OBJECTIVE: To determine the incidence of early-onset group B beta hemolytic streptococcal (EOGBS) infection and the association between changes in the incidence and intrapartum antibiotic prophylaxis (IAP).

STUDY DESIGN: A retrospective population survey of infants with GBS at <7 days of age with a nested case-control study of non-GBS infants over the same time period, January 1985 to December 1998. The incidence of GBS and maternal antibiotic treatment during labor was analyzed as a function of time period: prior to publication of guidelines for prevention of EOGBS (1985-1992), following AAP/ACOG guidelines (1993-1995), and following CDC consensus guidelines (1996-1998).

RESULTS: Fifty-six cases of EOGBS infection occurred among 53,088 live births. The incidence declined from 1.5/1000 before any guidelines to 0.67/1000 after AAP/ACOG guidelines (p=0.004), and continued to decline after the CDC consensus statement (0.28/1000) (p=0.38). IAP remained stable (33% of at risk mothers) until after introduction of the CDC consensus guidelines (59%, p=0.02).

CONCLUSION: IAP did not fully explain the decline in EOGBS incidence in our center. Journal of Perinatology (2002) 22, 516-522 doi:10.1038/sj.jp.7210798

BACKGROUND

Group B streptococcal (GBS) disease is a leading cause of neonatal bacterial morbidity and mortality. Mortality from the disease has progressively declined over the past three decades as a result of early recognition of infection and improved neonatal intensive care.¹ Among the strategies for the prevention of early-onset group B streptococcus (EOGBS) infection, the use of selective maternal intrapartum chemoprophylaxis in at-risk mothers is widely accepted to be the most efficacious.^2,3,4 This prompted the American Academy of Pediatrics (AAP) and American College of Obstetricians and Gynecologists (ACOG) in 1992 to recommend guidelines for intrapartum prophylaxis. The AAP advocated universal prenatal screening at 26 to 28 weeks of gestation with prophylaxis for carriers with obstetrical risk factors.⁵ The ACOG did not recommend prenatal screening, but rather prophylaxis was recommended for women with obstetrical risk factors.⁶ However, there was inconsistent implementation of these prophylaxis guidelines and a survey in 1994 revealed that practices varied widely.⁷ In 1996, the Centers for Disease Control and Prevention (CDC) published a set of consensus guidelines.⁸ These guidelines were supported by ACOG and AAP. The consensus guidelines gave practitioners a choice between two equally acceptable strategies. One strategy was based on a late prenatal screening culture at 35 to 37 weeks of gestation and the other was based only on maternal risk factors as enumerated in the 1992 AAP recommendations.

We present a 14-year observation of EOGBS incidence and antibiotic usage in a tertiary care center. Our primary objectives were to determine the incidence of EOGBS from 1985 to 1998 and the temporal association of any changes in incidence with the publication of the 1992 AAP/ACOG and 1996 CDC consensus guidelines. We measured the use of maternal antibiotics as a marker for implementation of these guidelines. The secondary objective was to determine the potential preventability of EOGBS infection in infants whose mothers met the criteria for preventive chemoprophylaxis in the CDC consensus guidelines.

METHODS

Golisano Children's Hospital at Strong is a division of Strong Memorial Hospital (SMH), a large university hospital with 3400 to 4300 live births a year that also serves as a major referral center for high-risk perinatal patients for the Finger Lakes region of New York state. All infants delivered at SMH from January 1, 1985 to December 31, 1998 with GBS isolated from blood and/or CSF at less than 7 days of age were included in this retrospective study. The protocol was approved by the Research Subjects Review Board of the University of Rochester.

Cases of EOGBS infection were identified from hospital microbiology laboratory records. Infant and maternal data were collected by chart review and from a computerized neonatal database. Demographic data were obtained and the presence or absence of the following was ascertained: chorioamnionitis (maternal fever, uterine tenderness, foul vaginal discharge, or as per the obstetrician's documentation of maternal chorioamnionitis), maternal GBS screening cultures, intrapartum maternal antibiotic use, and any one of the established risk factors for EOGBS (preterm rupture of membranes at <37 weeks of gestation, preterm delivery at <37 weeks of gestation, prolonged rupture of membranes >18 hours, intrapartum maternal fever 38°C, history of previous infant with GBS disease, GBS bacteriuria, or positive maternal GBS screening culture). Specific preestablished definitions were used in the chart review (Table 1). For maternal information, both inpatient and outpatient prenatal charts were reviewed. The year-to-year incidence of EOGBS was calculated based on the number of inborn EOGBS cases identified in each year and the number of live born infants at our institution for that particular year.

The 14-year study period was classified into three periods. The years 1985 to 1992 constituted the period before the publication of any guidelines (preguidelines period). The years 1993 to 1995 followed the introduction of the AAP/ACOG guidelines ("AAP/ACOG period"), and 1996 to 1998 followed the publication of the CDC consensus guidelines ("CDC consensus period"). Beginning in 1996, there was a recommendation from the Division of Fetal-Maternal Medicine at SMH to adhere to the CDC risk-based guidelines for EOGBS prophylaxis; however, prescription of intrapartum antibiotics was left to the individual practitioner. To assess actual practice, data on the use of antibiotics were collected. Our analysis was based on documented receipt of medication.

A sample of non-EOGBS infected infants was chosen to act as a control group for maternal intrapartum antibiotic use in the three periods under study. Six hundred twenty mothers were included in this control group, all taken from the first 40 deliveries of each year from 1985 to 1992 and the first 50 deliveries of each year from 1993 to 1998. They were chosen systematically after preliminary investigation showed no consistent seasonal variation in EOGBS incidence at our institution. Information on specific maternal antibiotic usage, timing, and doses received was gathered. The number for this group was derived from a sample size calculation based on the ability, with a power of 0.80 and of 0.05, to show a difference in antibiotic administration rates between case and control groups, assuming that 30% of controls would be risk factor- and/or GBS screening culture-positive and that 10% of cases, but 50% of risk factor-positive controls, would have received prophylactic antibiotics.

In addition, this control group, with the addition of any cases born during the same time period in early January of each year, served as a sample population from which to calculate the overall prevalence of intrapartum antibiotic use during the study period. Both the rate of total antibiotic use and the rate of antibiotic use among women with risk factors for EOGBS were calculated.

To determine the possible preventability of EOGBS infection among cases, the currently recommended CDC consensus guidelines were applied retrospectively to the mothers of EOGBS-infected infants to determine who would have been considered a candidate for antibiotic prophylaxis based on either the screening culture or risk factor-based protocols.

For statistical analysis, categorical variables were compared using chi-square with correction for multiple comparisons by requiring p<0.05 per number of comparisons. Continuous variables were compared using ANOVA followed by the Student's t-test with correction for multiple comparisons.

RESULTS

There were 56 cases of EOGBS identified from among 53,088 live births at Golisano Children's Hospital at Strong during the 14-year period from January 1, 1985 to December 31, 1998. The annual incidence of EOGBS at our center declined from 1.5/1000 live births (45 cases) in the preguidelines period (1985-1992) to 0.67/1000 live births (eight cases) in the AAP/ACOG guidelines period (1993-1995) (p=0.004). Although there was a further decline to 0.29/1000 live births (three cases) in the CDC consensus guidelines period (1996-1998), the incidence in these two periods did not reach statistical significance (p=0.38), likely due to the very small number of cases during the latter two time periods (Table 2, Figure 1).

Although there was year-to-year variation, overall maternal intrapartum antibiotic use was 10% in 1985 to 1992, 7% in 1993 to 1995 (p=0.34 for difference from 1985 to 1992), and 21% in 1996 to 1998 (p=0.0008 for difference from 1993 to 1995). One hundred thirty-four women (22% of total women surveyed) had either clinical risk factors for EOGBS infection or positive screening cultures for GBS. If antibiotic use among only these women was considered, 33% received antibiotic treatment in 1985 to 1992, whereas 33% received antibiotic treatment in 1993 to 1995 (p=0.96 for difference from preceding period), and 59% received antibiotic treatment in 1996 to 1998 (p=0.04 for difference from preceding period) (Table 2, Figure 1). There was no change in the rate of treatment of chorioamnionitis in surveyed women over the 14-year period (10/300 in 1985-1992, 3.3%; 4/150 in 1993-1995, 2.7%; 6/150 in 1996-1998, 4.0%). Intrapartum antibiotics consisted primarily of ampicillin either with or without added gentamicin, with smaller numbers of patients receiving penicillin, clindamycin, erythromycin, and cephalosporins. Among surveyed women who received intrapartum antibiotics, there was no change between periods in the proportion who received "adequate" intrapartum prophylaxis (2 doses of antibiotics beginning at least 4 hours before delivery) (35% in 1985-1992, 20% in 1993-1995, 32% in 1995-1998; p=0.66).

A significant decline in the incidence of EOGBS in our institution occurred at a time when there was no change in maternal antibiotic use (from the preguidelines period to the AAP/ACOG guidelines period). The significant increase in prescription of maternal intrapartum antibiotics occurred later. To further assess the relationship between intrapartum antibiotic prophylaxis (IAP) and risk of EOGBS, cases were compared to the control group of women with healthy infants. When compared, there was no difference in the antibiotic use among women with risk factors between the case and control groups (p=0.47) (Table 3).

As shown in Table 4, there were no significant race or gender differences observed between the EOGBS cases and the control group. However, as expected, babies born at less than 37 weeks of gestation and those with low birth weight were significantly overrepresented among the cases with EOGBS disease (p<0.001).

Among case mothers identified, the majority (43/56, 77%) had risk factors, including either maternal culture positive for GBS and/or clinical risk factors associated with EOGBS (Table 5). Although 28 of the case mothers (50%) had urogenital cultures sent, the majority of cultures (n=24, 43%) were performed intrapartum and it was thus unlikely that the results of the cultures were known prior to delivery. Only four case mothers (9%) had cultures performed at least a week prior to delivery, all of which were positive for GBS. Twenty five percent of case mothers had a single risk factor identified, whereas half had two or more risk factors present. Intrapartum maternal fever, rupture of membranes 18 hours, and preterm rupture of membranes each were seen in about 50% of the EOGBS cases. Of the women with clinical risk factors (Table 5), 20 received at least one dose of antibiotics prior to delivery. In the control group, 364 women (59%) did not have cultures done, 168 (27%) had prenatal cultures, 82 (13%) had cultures intrapartum, and 6 (1%) had cultures postpartum.

In 95% (n=53) of EOGBS cases identified, GBS was isolated from the blood alone, whereas 4% (n=2) had GBS isolated from both blood and CSF. One infant developed meningitis with a negative blood culture. The overall mortality rate was 9% (5/56). This decreased to 6% (3/54) if twins born before 24 weeks were excluded. Duration of survival varied from less than 30 minutes to 7 days. All deaths occurred in babies born at less than 30 weeks of gestation and all had one or more identifiable maternal clinical risk factors present at the time of delivery. None of the mothers of the babies who died had maternal screening cultures sent. Only two of the four mothers received intrapartum antibiotics. One mother received two doses of ampicillin beginning over 4 hours prior to delivery. The mother of the 23-week-gestational-age twins received one dose each of ampicillin, gentamicin, and clindamycin, all less than 4 hours prior to delivery.

The current CDC consensus guidelines were applied retrospectively to determine preventability of the EOGBS cases identified (Table 5). Twenty of the case mothers (36%) received intrapartum antibiotics. Among this group of women, three received the recommended course of prophylactic antibiotics (two or more doses of prophylactic antibiotics for the presence of either clinical or culture risk factors, starting at least 4 hours before delivery ¾ "adequate prophylaxis"). Two of these case mothers received two doses of ampicillin and the third received two doses of clindamycin. We considered these cases to be nonpreventable. One of the three infants born to these women died due to GBS infection, despite the intrapartum maternal antibiotics received. Multiple⁴ maternal risk factors were found in this particular case and the mother was sick enough to warrant continued treatment postpartum. The remaining 17 case mothers in this group received a single dose of antibiotics less than 4 hours prior to delivery ("inadequate prophylaxis"). Twelve of these 17 women received their antibiotics less than an hour prior to delivery, whereas the remaining five received antibiotics 1 to 3 hours prior to delivery. EOGBS infection in this group of infants was considered possibly preventable had their mothers received the recommended course of antibiotic prophylaxis.

An additional 23 case mothers with clinical risk factors and/or positive maternal cultures for GBS, who would have been eligible for prophylaxis, did not receive intrapartum antibiotics. These cases were judged to be possibly preventable.

The remaining 13 cases had no identifiable maternal clinical risk factors present nor were any maternal cultures sent. If the preventability of these cases were based on the risk factor strategy of the current guidelines, these cases would be nonpreventable because their mothers would not have been identified as eligible for intrapartum prophylaxis. In the absence of culture data, preventability based on the screening culture strategy cannot be determined.

DISCUSSION

The significant decline in the incidence of EOGBS disease observed in this study appeared to be coincident with the publication of the guidelines for the prevention of EOGBS infection. However, use of maternal antibiotics did not appear to explain this decline in the incidence. The fall in infection rate began before there was a significant rise in maternal IAP in our population.

Guidelines for IAP were in place during the period of most rapid fall in EOGBS rates. However, neither the rate of antibiotic use among control mothers, the use of antibiotics in mothers with risk factors, nor the proportion of treated women who received "adequate" antibiotic prophylaxis increased in the period during which EOGBS incidence was decreasing most dramatically. There were also no significant changes in the numbers of women with risk factors for EOGBS among any of the periods studied. It appears that neither the quantity nor the quality of IAP fully explained the lowered EOGBS incidence seen in our institution in 1993 to 1995.

Several approaches have been taken to estimate the efficacy of IAP in the prevention of EOGBS infection. Decision analysis models^9,10 have the advantages of allowing extrapolation to large populations and manipulation of underlying assumptions. However, they are heavily dependent on the accuracy of the assumptions used. Analysis of national databases is a powerful tool for determining trends in EOGBS infection. However, the analysis is constrained by the availability and reliability of specific data fields.

Randomized, controlled clinical trials and case-control studies have suggested the efficacy of intrapartum maternal antibiotic prophylaxis in the prevention of EOGBS disease.^{3,11,12,13,14} There have been observational, population-based studies of the incidence of EOGBS spanning the periods before and after the publication of guidelines for IAP. The majority of these studies have inferred a correlation between the fall in EOGBS and the increase in IAP based on institutional adoption of policies for intrapartum antibiotic use.^15,16,17 However, other reports have challenged the efficacy of IAP. A critical literature review by Ohlsson and Myhr¹⁸ concluded that many studies showed evidence of lowered neonatal GBS colonization following intrapartum prophylaxis, but most lacked the power to provide compelling evidence of reduction in EOGBS infection. Due to methodologic differences among studies, these authors declined to perform a meta-analysis of the studies they surveyed.¹⁸ Katz et al.,¹⁹ in a more recent study, showed that despite a significant increase in the use of maternal antibiotics during labor, there was no change in the rate of EOGBS sepsis at their institution. However, only about half of their study patients was screened and received prophylaxis appropriately. In perhaps the most comprehensive study, Brozanski et al.²⁰ determined not only the incidence of EOGBS in their population, but also the frequency of administration of intrapartum antibiotics as recommended in the CDC consensus guidelines. They documented an 86% compliance with IAP and an 88% reduction in EOGBS from 1.16 per 1000 live births in the pre-CDC period (1992-1995) to 0.14 per 1000 live births in the CDC guidelines period (1995-1999). There was no change in maternal colonization rate that might have accounted for the decrease in infection. Brozanski et al.'s findings differ from ours in that their rate of EOGBS remained relatively high during the time at which our rate had begun to fall. The differing timing of the fall in EOGBS between the studies raises the question of whether the association seen between IAP and change in EOGBS rate was causal, unrelated, or some combination of the two. Observational studies cannot answer this question fully.

The 14-year span of our study offers several advantages. The study includes several epochs in the development of EOGBS prophylaxis measures. Several previous studies have analyzed EOGBS incidence in the pre- and postpublication periods for either the 1992 AAP/ACOG protocol or the 1996 CDC consensus guidelines, but not both.^21,22 We have presented observational data on individual cases derived from a large population base (53,088 live births). We were able to gather extensive information about each case identified. This allows us to draw reliable conclusions about the efficacy of prophylaxis. In addition, year-to-year variations in both antibiotic use and disease frequency were smoothed, allowing long-term trends during the introduction of new interventions to be more easily identified. Despite the large number of births surveyed, the incidence of EOGBS disease had fallen so dramatically by the AAP/ACOG period that further decreases during the CDC period would have been difficult to confirm statistically even with the 12,000 to 13,000 births in each of those periods. Larger regional and national samples have suggested that the incidence of EOGBS has continued to fall in the last several years, although again the association does not prove cause and effect.²³

A single institution study may not reflect national trends, especially with the reported geographic variation in the incidence of EOGBS infections.⁸ We therefore caution against extrapolating the information in this study to populations dissimilar to ours. Observational studies may also be subject to ascertainment bias. Identification of cases in our study, however, was based on preestablished definitions to minimize problems of inconsistent diagnostic criteria. In addition, reviewing both microbiology records and the NICU database allowed reasonable certainty that we were able to capture all EOGBS-infected babies during the three periods under study. In a retrospective study, it is also impossible to impute motives to the practitioners administering antibiotics. Although we specifically assessed antibiotic use in light of published guidelines, administration of antibiotics in the presence of risk factors implies, rather than guarantees, that the intention of the practitioner was to comply with recommended guidelines.

It was impossible to review accurately the medical records of all babies born during the study period; therefore, a sample of the more than 50,000 maternal-infant pairs was chosen for analysis to determine the rate of prescription of maternal antenatal antibiotics. The first 40 to 50 infants born in each calendar year were chosen as representative of the entire population after distribution of cases over the year was determined not to vary significantly from month to month. The number of cases diagnosed in January of each year represented both the mean and the mode for the entire year. January was also chosen in part because it was in the middle of the academic year, and thus, treatment with intrapartum antibiotics would likely not be influenced by the influx of new practitioners that occurs in the summer months. The number of doses of intrapartum antibiotics administered in January corresponded to the mean and median number of monthly doses over the course of the year. Other methods of choosing an appropriate control group (e.g., reviewing the records of the three infants born preceding and following each case infant) would also have been valid, but were logistically more cumbersome.

Three infants in our study developed EOGBS infection despite adequate antibiotic prophylaxis. Ampicillin was used as prophylaxis in two, whereas clindamycin was given in the third case. Most studies report that GBS remains susceptible to penicillin;²⁴ however, there are reports of GBS isolates resistant to erythromycin and clindamycin.²⁵ Because antibiotic susceptibility testing of GBS isolates is not a routine policy at our institution, no observation about the possibility of antibiotic resistance among the GBS isolates identified can be made.

A proportion of cases identified during the study period was possibly preventable by retrospective application of the current CDC guidelines. Most of the possibly preventable cases were identifiable by the risk factor arm of the CDC guidelines. However, the risk factor-based strategy failed to identify a substantial number of mothers whose infants developed EOGBS infection. Twenty-three percent of infants with EOGBS infection did not have any identifiable clinical risk factors. This is similar to the 25% to 50% reported in the literature.^11,26 The low rate of performance of maternal screening cultures in our EOGBS-infected subjects precludes conclusions regarding preventability using the screening arm of the protocol.

We do not dispute the effectiveness of intrapartum antibiotics in the reduction of EOGBS disease. However, the uncertain role of maternal intrapartum prophylaxis in the initial decline of EOGBS incidence seen at our institution suggests that there might be other variables involved in the change in the incidence of this disease. There are studies which suggest that changing population demographics may affect GBS colonization rate.^27,28 However, no racial or ethnic shifts were observed in our population (data not shown). Although previous studies have found a higher risk of EOGBS associated with black race, this was not statistically significant in our population, likely due to small numbers and lack of power. Change in the prevalence of GBS carriage among pregnant women is another potential explanation. The low rate of GBS screening cultures in our study prevents us from addressing this issue. Other potential explanations could be changes in GBS serotype and susceptibility distributions that led to virulence modification over time.^29,30,31

In conclusion, over the 14 years we examined, there was a significant decline in the incidence of EOGBS infection at our institution. However, we were unable to demonstrate clearly an association between this decrease and the use of maternal antibiotics. A proportion of the cases identified, both before and after publication of the AAP/ACOG and CDC consensus guidelines, were nonpreventable. No currently identified antibiotic strategy will prevent all EOGBS. Other strategies, perhaps including vaccines, may be necessary to reduce further or to eradicate the disease.

References

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4 Boyer KM, Gadzala CA, Kelly PD, Gotoff SP. Selective intrapartum chemoprophylaxis of neonatal group B streptococcal early onset disease: III. Interruption of mother to infant transmission. J Infect Dis 1983; 148: 810-6. MEDLINE

5 American Academy of Pediatrics. Guidelines for prevention of group B streptococcal infection by chemoprophylaxis. Pediatrics 1992; 90: 775-8.

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16 Factor SH, Whitney CG, Zywicki SS, Schuchat A. Effects of hospital policies based on 1996 group B streptococcal disease consensus guidelines. Obstet Gynecol 2000; 95: 377-82. MEDLINE

17 Schrag SJ, Zywicki S, Farley MM et al. Group B streptococcal disease in the era of intrapartum antibiotic prophylaxis. N Engl J Med 2000; 342: 15-20. MEDLINE

18 Ohlsson A, Myhr TL. Intrapartum chemoprophylaxis of perinatal group B streptococcal infections: a critical review of randomized controlled trials. Am J Obstet Gynecol 1994; 170: 910-7. MEDLINE

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20 Brozanski BS, Jones JG, Krohn MA, Sweet RL. Effect of a screening-based prevention policy on prevalence of early-onset group B streptococcal sepsis. Obstet Gynecol 2000; 95: 496-501. MEDLINE

21 Adriaanse AH, Lagendijk I, Muytjens HL, Nijhuis JG, Kollee LA. Neonatal early onset group B streptococcal infection. A nine-year retrospective study in a tertiary care hospital. J Perinat Med 1996; 24: 531-8. MEDLINE

22 Lieu TA, Mohle-Boetani JC, Ray GT et al. Perinatal group B streptococcal infection in a managed care population. Obstet Gynecol 1998; 92: 21-7. MEDLINE

23 Schrag SJ, Zywicki S, Farley MM et al. Group B streptococcal disease in the era of intrapartum antibiotic prophylaxis. N Engl J Med 2000; 342: 15-20. MEDLINE

24 Morales WJ, Dickey SS, Bornick P, Lim DV. Change in antibiotic resistance of group B streptococcus: impact on intrapartum management. Am J Obstet Gynecol 1999; 181: 310-4. MEDLINE

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Figures

Figure 1 EOGBS incidence and maternal antenatal antibiotic use. EOGBS incidence (closed triangles) showed a significant decline between the preguidelines period (1985-1992) and the AAP/ACOG guidelines period (1993-1995) (p=0.004). There was a further decline in the CDC consensus guidelines period (1996-1998) that was not statistically significant (p=0.38). Over the same time periods, maternal antibiotic use (open squares) remained stable between the preguidelines period and the AAP/ACOG period. A significant increase occurred during the CDC guidelines period (p=0.0008).

Tables

Table 1 Definition of Terms

Table 2 Summary Data for EOGBS Incidence and Antibiotic Use

Table 3 Antenatal Antibiotic Use Among Women with Risk Factors

Table 4 Patient Demographics

Table 5 EOGBS Cases, 1985-1998

October/November 2002, Volume 22, Number 7, Pages 516-522

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