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Perinatal Antibiotic Usage and Changes in Colonization and Resistance Rates of Group B Streptococcus and Other Pathogens

From the Department of Microbiology and Infectious Disease, Department of Pediatrics, Community Health Sciences, and Child Health Research Unit, Alberta Children’s Hospital, University of Calgary, Calgary, Alberta, Canada.

Address reprint requests to: H. Dele Davies, MD, Alberta Children’s Hospital, Division of Infectious Diseases, Child Health Research Unit, 1820 Richmond Road, SW, Calgary, AB T2T-5C7, Canada; E-mail: dele.davies{at}calgaryhealthregion.ca.

	ABSTRACT

TOP ABSTRACT MATERIALS AND METHODS RESULTS DISCUSSION REFERENCES

 
OBJECTIVE: To quantify current antibiotic usage during the perinatal period and impact on vaginal-rectal colonizing organism resistance rates.

METHODS: Swabs were obtained for culture of group B streptococcus and other bacteria from a cohort of 1207 pregnant women in Calgary, Alberta, at 36 weeks’ gestation. Those women who received antibiotics during labor or after pregnancy and a 10% subset who received no antibiotics had repeat cultures at 6 weeks postpartum. Cultured organisms were tested for sensitivity to several antibiotics.

RESULTS: Group B streptococcus was identified in 235 women (19.5%) in the antepartum period. Fifty-one percent of all participants received antibiotics (31.4% intrapartum). Group B streptococcus prophylaxis was given to 215 (17.8%), whereas 83 (6.9%) group B streptococcus-negative women without fever during labor received antibiotics. Ampicillin (49%), cefazolin (28%), and penicillin (18%) were the most frequently used antibiotics. Resistance rates among group B streptococcus to erythromycin and clindamycin were 5.6% and 3.0%, respectively, whereas 20.6% of Escherichia coli were ampicillin resistant. Among antibiotic recipients, 6.3% of all bacteria that were initially sensitive on prenatal cultures to a specific antibiotic became resistant in the postnatal period, whereas 6.5% that were initially resistant became sensitive.

CONCLUSION: Current prevention practices in our region were associated with perinatal antibiotic administration in over half of pregnant women. Ampicillin was the most common antibiotic administered. Some physicians are treating women who are group B streptococcus culture negative at term, a practice that is of no proven value. However, this was not associated with increased resistance for group B streptococcus or other organisms identified from maternal vaginal-rectal tracts.

Group B streptococcus has traditionally been the most significant cause of bacterial sepsis in newborn infants and the leading cause of death attributable to infection in newborn infants.^1–3 Group B streptococcus colonizes 12–40% of pregnant mothers and is transmitted to 40–70% of their infants.^2,4,5 Group B streptococcus is transmitted vertically into the amniotic fluid during labor, and is then aspirated by the infant or is acquired by passage through the birth canal. Infection with group B streptococcus most commonly manifests as septicemia, pneumonia, or meningitis, and is usually evident within the first few days of life with an associated mortality rate of 6–20%.^1,5,6

A number of risk factors have been correlated with the occurrence of group B streptococcus disease in neonates. Group B streptococcus colonization of the vaginal-rectal tract is obligatory for transmission of bacteria from mother to infant. Among colonized women, a major factor that increases the risk of transmission of group B streptococcus is the onset of labor and preterm delivery before 37 weeks’ gestation.⁷ Other significant risk factors, which are associated with higher incidence of group B streptococcus disease, are chorioamnionitis, intrapartum maternal fever higher than 37.5C, and prolonged rupture of membranes (greater than 12 hours).^7,8

Given the high morbidity and mortality of group B streptococcus disease in infants, effective methods for prevention have been sought. The Centers for Disease Control and Prevention (CDC) published consensus guidelines for the prevention of neonatal group B streptococcus disease in 1996 in an attempt to consolidate the previous recommendations of the ACOG and the American Academy of Pediatrics.⁹ These guidelines recommend the use of either a risk-based or screening-based approach to identify candidates for intrapartum prophylaxis. According to the risk-based approach, women who present at the time of labor with risk factors for disease transmission (fever, prolonged rupture of membranes, imminent preterm delivery) are offered intrapartum antibiotic prophylaxis. Using the screening-based approach, all women are screened for carriage of group B streptococcus between 35 and 37 weeks’ gestation, and intrapartum antibiotic prophylaxis is offered to all carriers and preterm deliveries. Late gestation screening is preferred because it substantially improves the predictive accuracy for positive results at delivery.¹⁰

The CDC screening-based recommendations include using combined vaginal-rectal swab cultures to determine colonization status with intrapartum antibiotic prophylaxis being given to group B streptococcus culture-positive women and those with unknown group B streptococcus status who demonstrate signs of or risk factors for infection during labor (fever, prolonged rupture of membranes, and preterm labor). In addition, any woman with a previous group B streptococcus-infected neonate or group B streptococcus bacteriuria should also receive empiric prophylaxis. The guidelines recommend the use of penicillin as the antibiotic of choice for prophylaxis because it is universally effective against group B streptococcus and has a narrow spectrum of action. In situations where a penicillin allergy exists, clindamycin and erythromycin are the recommended antibiotics. A decision analysis on prevention strategies for group B streptococcus has indicated that this approach should result in an 86% reduction in the occurrence of neonatal sepsis, at the cost of treating 27% of pregnant women with antibiotics.¹¹

Although the benefits of antibiotics are gratifying and have proven very successful in reducing the incidence of group B streptococcus disease in neonates,^6,12 adverse effects of widespread antibiotic usage cannot be dismissed. In addition to allergic reactions and direct organ toxicity, another hazard of antibiotic use is the potential selection of resistant strains of bacteria (McGavin M, McGeer A, DeAzavedo JC, Trpeski L, Pong-Porter S, Duncan C, et al. Emergence of erythromycin and clindamycin resistance in group B streptococci [GBS] associated with neonatal disease in Toronto, Canada [abstract number 1224]. In: 39th Interscience Conference on Antimicrobial Agents and Chemotherapy [ICAAC]. San Francisco, CA: American Society for Microbiology, 1999).^13–16 With a predicted 27% of pregnant women receiving antibiotics during labor,¹¹ it becomes very important to ensure that the possible harms of such antibiotic use do not outweigh the benefits. In their policy statement, the CDC indicated that "Investigations . . . are needed urgently to assess outcomes, including the incidence of neonatal group B streptococcus disease, occurrence of adverse reactions to antimicrobial prophylaxis, and the emergence of perinatal infections attributable to penicillin-resistant organisms."⁹

To evaluate the implications of antibiotic prophylaxis for group B streptococcus in Calgary women, we prospectively enrolled a cohort of pregnant women from the Calgary Health Region. We then compared those who received group B streptococcus prophylaxis or antibiotics for other reasons during the perinatal period with a control group (a subset who did not receive antibiotics during this same period). With this comparison, we were able to characterize and evaluate: 1) the variation in colonization status, and 2) microbial antibiotic resistance in both groups of women; that is, those who received perinatal antibiotics and those who did not. Furthermore, this study was performed not only to evaluate the incidence of group B streptococcus colonization but also to observe some positive and negative outcomes from the currently recommended CDC guidelines.

	MATERIALS AND METHODS

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The study was approved by the Ethics Board of the University of Calgary. The study population consisted of pregnant women in the Calgary Health Region. The city of Calgary in Alberta, population 933,700, has three hospitals that recorded 11,931 deliveries in 1999. Women were enrolled voluntarily from obstetric care practitioners (both family doctors and obstetricians), with a mix of low, medium, and high-risk deliveries, at the time of their most recent prenatal office visit (usually at 32–33 weeks). Two vaginal-rectal swabs were collected at 36 (35–37) weeks’ gestation. One swab was inoculated into Todd-Hewitt broth supplemented with colistin and gentamicin and processed for isolation of group B streptococcus using standard laboratory procedures,¹⁷ and the second swab was used to determine the presence of Escherichia coli (E coli), Staphylococcus aureus, group D enterococcus, group D non-enterococcus, and -haemolytic streptococcus using standard laboratory procedures for these organisms.^17–19 All cultured organisms were tested for sensitivity to several antibiotics.

The maternal group B streptococcus risk factor status, colonization status, doses of intrapartum antibiotics for group B streptococcus prophylaxis, and other antibiotics used (as prescribed by attending physicians) during the pregnancy or in the postpartum period up to 6 weeks as well as adverse events were recorded. At the 6-week postpartum visit, repeat vaginal-rectal swabs were performed on all mothers who received either intrapartum or postpartum antibiotics to define a change in the proportion and susceptibility patterns of the organisms identified at the 35–37 week prenatal visit. A control group of women comprising approximately 10% of the overall cohort of women and who received no antibiotics during or after their pregnancy also received this second swab. We determined the group B streptococcus prophylaxis group based on either a prenatal group B streptococcus-positive swab or preterm labor between 36 and 37 weeks because our study population was recruited at 36 weeks. Information on group B streptococcus bacteriuria or previous infant with group B streptococcus infection was not collected.

The controls were selected consecutively. An a priori decision was to enroll approximately 10% of participants as controls to give a sample size of no less than 120. Because we could not anticipate who was going to get antibiotics except those who were group B streptococcus positive, and the swabs needed to be done at the 6-week visit, we had to alert the participants and physicians involved. For this reason, all consecutive patients, whether or not they received antibiotics, were enrolled and informed they would receive the follow-up swabs until we had hit our target control enrollment of 120 (plus seven extras who were enrolled as a result of overshooting of target). Because the study period was short, we did not feel that consecutive enrollment occurring at multiple clinics would introduce any bias that would influence results based on the type of information collected.

Data were analyzed using Statistica 5.0 (StatSoft Inc., Tulsa, OK) and Excel 2000 (Microsoft Inc., Redmond, WA). Group proportions were compared using the ² test. The rates of antibiotic resistance in the study and control groups were also compared for each study organism using the ² test. McNemar ² for paired proportions was used for comparisons of change in colonization status before and after antibiotic therapy in colonized women. A P value < .05 was considered statistically significant.

	RESULTS

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During the 2-year study period, 1207 women were enrolled and followed (enrollment occurred over 17 months, November 1998 to April 2000). Of these subjects, 235 (19.5%, 95% confidence interval 17.2, 21.7) were colonized with group B streptococcus at the time of the prenatal vaginal-rectal swab (swab 1). Subject characteristics and colonization status for five other selected organisms are listed in Table 1. We found that 51.2% (618) of subjects were given antibiotics at some point during or immediately after their pregnancy. Antibiotic usage was further subdivided according to the perinatal period during which antibiotics were given (antepartum, intrapartum, postpartum, and postdischarge). The greatest proportion of antibiotic therapy was given during the intrapartum period, with 31.4% of the study population receiving antibiotics during this time. Ampicillin, cefazolin, and penicillin were the most frequently used antibiotics during this time, accounting for 49% (186), 28% (106), and 18% (68) of intrapartum antibiotics, respectively. The most common indication for giving intrapartum antibiotic was 57% (215 of 379) for group B streptococcus prophylaxis. Of the women who received cefazolin, 81.3% (87 of 107) were delivered by cesarean, suggesting that prophylaxis of postcesarean wound infection was the most common indication for this antibiotic. During the postpartum period, cefazolin was also the most commonly used antibiotic, accounting for 80% (140) of postpartum antibiotics. This was also used primarily as prolonged prophylaxis against cesarean-related wound infections. In the antepartum and postdis-charge periods, there were a wide variety of antibiotics used, probably reflecting the wide variety of reasons for which antibiotics were given. No allergic reaction either immediate or delayed was recorded.

Intrapartum antibiotics were also given to many women without clear indications for group B streptococcus prophylaxis. Forty-three (3.6%) women who were group B streptococcus negative and had no risk factors received intrapartum antibiotics, whereas in four women, there was inadequate information available on risk factors. We were unable to determine the indication for the antibiotics given in these cases. Of the indications for the 117 (9.7%) additional group B streptococcus-negative women receiving intrapartum antibiotics, 40 (3.3%) had prolonged rupture of membranes only. However, 32 (2.7%) had intrapartum fever, and 45 (3.7%) had both intrapartum fever and prolonged rupture of membranes.

Among all group B streptococcus-colonized mothers, 201 (85.5%) received intrapartum antibiotics. Thirty-four women cultured positive for group B streptococcus at the prenatal swab but did not receive any intrapartum antibiotics. In three of these women, there was no apparent reason for having not received antibiotics. Among the remaining 31 women, 15 had precipitous labor and delivery, three delivered at home, 12 had cesareans (elective or emergency), and one refused antibiotic therapy because of a prior anaphylactic reaction.

Table 2 shows the susceptibility of group B streptococcus, E coli, group D enterococcus, and -hemolytic streptococcus to selected antibiotics. Group B streptococcus was universally sensitive to both penicillin and ampicillin. Resistance rates among group B streptococcus strains in our population to erythromycin and clindamycin were 5.6% and 3.0%, respectively. Of the E coli cultured, 20.6% (152 of 738) were ampicillin resistant.

	DISCUSSION

TOP ABSTRACT MATERIALS AND METHODS RESULTS DISCUSSION REFERENCES

For guidelines to have the desired impact, they need to be implemented as prescribed, otherwise the underlying assumptions about cost-effectiveness and efficacy may be invalid. The components of the CDC guidelines⁹ were followed correctly in the majority of cases. However, we found that some physicians are giving prophylaxis based on risk factors in women who are group B streptococcus negative at term, a practice that is not recommended in any of the current guidelines, and whose cost-effectiveness has not been evaluated. The rationale for this is not clear, but may be due to fears about false-negative culture results or misinterpretation of the guidelines. Although few women who should have received group B streptococcus prophylaxis were missed (15% of group B streptococcus-positive women did not receive prophylaxis), 91% of these cases’ extenuating circumstances, such as precipitous labor or cesarean, accounted for the absence of treatment. These data suggest that, overall, compliance to CDC group B streptococcus guidelines continues to improve in our region compared with compliance documented for previous years, but there are areas where physician education needs to continue.^6,21

An area of concern identified by this study is the first-line choice of antibiotics for group B streptococcus prophylaxis. Current guidelines recommend the use of penicillin because of its high efficacy against group B streptococcus and its narrow spectrum of action. We found that ampicillin appears to be the antibiotic of choice among physicians in Calgary, used in 79.5% of participants requiring clear indications for group B streptococcus prophylaxis, with only 32.1% of participants receiving penicillin. Similar results were found in a study by Towers et al¹³ who postulated that this could be related to the cheaper cost of ampicillin and the greater familiarity of ampicillin to most physicians with respect to dosing regimens. Group B streptococcus strains are universally sensitive to ampicillin, so it is effective in preventing transmission; however, because it is a broad spectrum antibiotic, it has greater potential for the selection of resistant organisms.^22,23 There was limited use of erythromycin and clindamycin, which are the recommend antibiotics in cases where allergy to penicillin exists. Other deviations from the guidelines that warrant education include: 1) continuation of prophylaxis in the postpartum period resulting in an unnecessary use of antibiotics, and 2) administration of antibiotics to participants who cultured negative for group B streptococcus and had no fever (83, 6.9% of all women).

Potential adverse effects of increased antibiotic use are a major concern within the medical community and general population with a slight majority of pregnant women receiving antibiotics, whether it be for group B streptococcus prophylaxis or otherwise. The most significant proportion of antibiotics was given during the intrapartum period for group B streptococcus prophylaxis, accounting for more than half of antibiotics given to pregnant women. Another noteworthy indication for an antibiotic among our population was cesareans for which cefazolin was the most common antibiotic given. This use of antibiotics is also likely to have a significant impact on our population because about one in six pregnancies results in cesarean. In spite of the high percentage of women receiving antibiotics, we did not document any allergic adverse events. This may be partly due to the fact that the women were somewhat older (mean age 30 years), and likely had a clear history of whether or not they were allergic to penicillin that would have led to prescription of other antibiotics. However, we did not have a large enough sample to have detected anaphylaxis, were it to occur.

Despite the considerable rate of antibiotic therapy, we did not find any impact on the resistance rates among organisms commonly colonizing maternal vaginal-rectal tracts in women who received versus those who did not receive antibiotics. Our data, however, do not account for any women who became colonized with resistant strains of a different organism due to antibiotic usage because we looked at the development of resistance only in those women who were colonized by the same organism both at the prenatal and postnatal swab. Among those who carried sensitive bacterial strains that became resistant, there was no trend with respect to what antibiotic they received or when they received it. We identified 17 people who were colonized with E coli who developed ampicillin resistance after receiving antibiotics. However, an equivalent number of women colonized with resistant E coli became sensitive after antibiotic therapy. There was also an equivalent proportion of E coli transformations, both sensitive to resistant and resistant to sensitive, which occurred in the control group who did not receive any antibiotics. A major strength of our study and one that has not been previously investigated was that not only were the colonization rates with resistant organisms low but there was an equivalent number of strains converting from resistant to sensitive to those converting to resistant from sensitive. However, larger studies will be needed to further explore the relative frequency of these shifts in resistant and sensitive strains. Some previous reports^13,24–27 have noted increased neonatal infection with ampicillin resistant E coli in the setting of intrapartum ampicillin use for group B streptococcus prophylaxis. A large study involving 19 Connecticut hospitals was conducted to determine whether intrapartum antibiotic prophylaxis for neonatal group B streptococcus resulted in an increased rate of non-group B streptococcus or antibiotic-resistant early onset invasive neonatal disease. In this study, Baltimore et al²⁸ noted that although there was a rise in ampicillin-resistant E coli with implementation of group B streptococcus prophylaxis between 1996 and 1998, there was a drop in 1999. These data suggest that acquisition of resistance in vaginal-rectal flora is a complex and dynamic process that may not be wholly accounted for by presence or absence of antibiotics. Nonetheless, as a rule, ampicillin usage for prophylaxis should continue to be discouraged.

In the last several years, an emerging resistance of group B streptococcus to erythromycin and clindamycin has been reported.^14,15,29 The appearance of resistant strains of group B streptococcus to these antibiotics, which are recommended for treatment of group B streptococcus infection in those patients who are allergic to penicillin, has coincided with the introduction of routine group B streptococcus prophylaxis regimens. In this study, we did not find high rates of development of group B streptococcus resistant to erythromycin or clindamycin (5.6% and 3.0%, respectively). These findings are similar to those of a recent population-based study of invasive group B streptococcus isolates across Canada in which the rates of resistance to erythromycin and clindamycin were 6.7% and 4.4%, respectively.³⁰ In contrast, Morales et al²⁹ identified 18% erythromycin resistance, and 5% clindamycin resistance, whereas Pearlman et al¹⁴ identified rates of 16% and 15%, and Vermillion et al³¹ reported 8% and 19% resistance to the two drugs, respectively. The differences with our population may relate to differing antibiotic practices. Nonetheless, demonstration of increasing resistance of group B streptococcus to these antibiotics in other locales suggests a need for vigilant monitoring as increasing rates may necessitate a need for alternative second-line choices such as first-generation cephalosporins.²⁹ Despite the appearance of increasing numbers of resistant group B streptococcus strains, group B streptococcus remains universally sensitive to penicillin G (McGavin M, McGeer A, DeAzavedo JC, Trpeski L, Pong-Porter S, Duncan C, et al. Emergence of erythromycin and clindamycin resistance in group B streptococci [GBS] associated with neonatal disease in Toronto, Canada [abstract number 1224]. In: 39th Interscience Conference on Antimicrobial Agents and Chemotherapy [ICAAC]. San Francisco, CA: American Society for Microbiology, 1999).^14,29

In summary, this study investigated the impact of antibiotic usage for group B streptococcus prophylaxis. Among the pregnant population in Calgary, there is a substantial rate of antibiotic use and, in particular, antibiotic use for group B streptococcus prophylaxis. It appears that some physicians are giving antibiotics based on risk factors in women who are group B streptococcus negative at term and who do not have evidence for chorioamnionitis, a practice that is not recommended in any of the current guidelines, and that is of no proven value. We found no increase in the rates of colonizing organisms among women who were treated with antibiotics for group B streptococcus prophylaxis or any other indication. Furthermore, there was no change in resistance rates of organisms cultured regardless of whether antibiotics had been given. We did not identify any adverse allergic effects resulting from antibiotic therapy in the studied population. Ongoing surveillance and education are needed to evaluate and improve the impact and consequences of practices related to current guidelines and guide the implementation of revisions.

	Footnotes

 
Renee Spaetgens, MSc, and Kim DeBella, BSc, contributed equally to this paper.

H. Dele Davies, MD, is a Medical Scholar of the Alberta Heritage Foundation for Medical Research.

Grant and financial support: Canadian Institutes of Health Research (formerly Medical Research Council of Canada, Grant Number MT-15026).

PII S0029-7844(02)02068-9

Received January 22, 2002. Received in revised form March 14, 2002. Accepted April 4, 2002.

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6. Davies H, Adair C, Schuchat A, Low D, Sauve R, The Alberta Neonatal Group B Streptococcal and Toronto Invasive Bacterial Diseases Networks, et al. Physician prevention practices and incidence of neonatal GBS disease in two Canadian regions. Canadian Med Assoc J 2001;64:479–85.

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