Original Article

Effect of Intrapartum Antibiotic Prophylaxis Against Group B Streptococcal Infection on Comparisons of Rates of Endometritis and Urinary Tract Infection in Multicenter Surveillance

Anne‐Marie Dumas, MD; Raphaëlle Girard, MD; Louis Ayzac, MD; Geneviève Beaumont, MWc; Emmanuelle Caillat‐Vallet, MSc; Florence Depaix, RNc; Chantal Gignoux, MWc; Catherine Haond, MD; Noelle Pral, MWc; Jacqueline Robert, MWc; Françoise Tissot‐Guerraz, MD; Agnès Vincent‐Bouletreau, MD; Michel Berland, MD; Jacques Fabry, MD  

From the Service de Gynécologie Obstétrique (A.M.D., M.B.) and the Service d'Hygiène et Épidémiologie (R.G.), Centre Hospitalier Lyon Sud, Pierre Bénite, and the Centre de Coordination de la Lutte Contre les Infections Nosocomiales Sud‐Est (L.A., G.B., E.C.‐V., F.D., C.G., C.H., N.P., J.R., F.T.‐G., A.V.‐B., J.F.), Saint Genis Laval, France.

Address reprint requests to Anne‐Marie Dumas, MD, Centre Hospitalier Lyon Sud, Service de Gynécologie Obstétrique, Batiment 3B, Pierre Bénite Cedex, 69495 Pierre Bénite, France (anne‐marie.dumas@chu‐lyon.fr).

Objective. To establish whether antibiotic prophylaxis against group B streptococcal infection may be a confounding factor in comparisons of rates of endometritis and urinary tract infection after vaginal delivery.

Design. Prospective study.

Setting. Maternity units at 48 hospitals in a regional surveillance network in France during 2001‐2004.

Methods. The maternity units used a common protocol to establish whether antibiotic prophylaxis was indicated. Risk factors for endometritis and urinary tract infections were evaluated using multiple logistic regression.

Results. We analyzed 49,786 vaginal deliveries. The percentage of women receiving antibiotic prophylaxis varied widely and significantly among the maternity units (range, 4.4%‐26.0%; median, 15.8%; 25th percentile, 12.1%; 75th percentile, 19.0%) ( , by Mantel‐Haenszel χ2 test). The incidence rate of endometritis was significantly reduced from 0.25% to 0.11% by antibiotic prophylaxis ( ). There was a decrease in the incidence of urinary tract infection from 0.37% to 0.32%, but it was not statistically significant ( ).

Conclusions. A reduction in the incidence of endometritis was observed when intrapartum antibiotic prophylaxis against group B streptococcal infection was used. However, the proportion of women considered to be at risk of infection varied widely among institutions. Comparisons of rates of endometritis among maternity units, but not urinary tract infection rates, should take into account antibiotic prophylaxis as a significant confounding factor.

Received August 10, 2007; accepted December 10, 2007; electronically published March 3, 2008.

Surveillance networks have been developed to help maternity units perform local quality assessments. This development is partly in response to patients’ increasing demands for nosocomial infection prevention.1‐6 However, patient heterogeneity is considerable among maternity units. Comparisons of nosocomial infection rates must therefore take account of all known confounding factors, such as maternal age and parity, and type of delivery, as well as any new factors that appear significantly associated with changes in nosocomial infection rates.4,7‐13 One such confounding factor might be antibiotic prophylaxis.

Streptococcus agalactiae (group B streptococcus [GBS]), which is the primary cause of neonatal infection, is also a leading cause of maternal infections, such as clinical chorioamnionitis,14 urinary tract infection (UTI), and endometritis.15,16 Several bodies, including the Centers for Disease Control and Prevention (CDC), have developed guidelines for the prevention of GBS infection, which have been adopted by the health authorities of many countries.17‐19

Since the implementation of intrapartum antibiotic prophylaxis in women carrying GBS (in the ninth month of pregnancy) or in women at high risk of GBS infection, the neonatal infection rate has decreased by approximately 70%.20‐24 However, the incidence of maternal nosocomial infections—in particular, endometritis and UTIs—has received less attention.25,26 A decrease in maternal infection rates has been noted as a result of surveillance programs,27 screening for risk factors for infection,7,8 and prevention strategies.28 In our surveillance network in southeastern France,29 which was established in 1995, the nosocomial infection rate for women who underwent vaginal deliveries decreased from 1.6% (0.47% for endometritis and 0.52% for UTIs) in 1997‐1998 to 0.99% (0.18% for endometritis and 0.34% for UTIs) in 2004.2 A retrospective analysis of 1,131 vaginal deliveries at a level 3 maternity unit (Centre Hospitalier Lyon Sud) in the surveillance network in the year 2000 indicated that the infection rate was 0.4% for women who received GBS antibiotic prophylaxis and that it was 1.2% for women who did not. However, the difference was not statistically significant ( ).30

Since 1999, our surveillance network includes confounding factors when calculating the number of expected nosocomial infections for each participating maternity unit. If there is a discrepancy between numbers of expected and observed cases, the maternity unit is asked to revise its surveillance program. We conducted a prospective study to find out whether the decreases we have observed in the rates of endometritis and UTI are in part caused by GBS antibiotic prophylaxis and, consequently, whether GBS antibiotic prophylaxis is a confounding factor in our surveillance data.

Methods

 

We invited all maternity units in the surveillance network to take part in a multicenter study on the rates of endometritis and UTI after vaginal delivery. The study covered the years 2001‐2004. All women who underwent vaginal delivery at participating maternity units were included in the study. Women hospitalized in the units after giving birth elsewhere were excluded.

The surveillance protocol was a slightly modified version of the monitoring program used by all maternity units belonging to the Mater Sud‐Est Network: an additional item (ie, intrapartum administration of antibiotic prophylaxis against GBS) was added to the usual criteria, but no items that related to screening or risk of GBS infection were included. Full details of the surveillance protocol and definitions (in French) can be found on the network’s Web site.29 Data on the following variables were recorded: maternal age and parity, receipt of epidural analgesia, requirement for instrumental delivery (with forceps or vacuum extractor), blood loss of more than 800 mL, requirement for more than 5 vaginal digital examinations after rupture of membranes, induction of labor, premature rupture of the membranes, UTI during pregnancy, intrapartum fever, requirement for urinary drainage, and nosocomial infection. Variables were selected by the network on the basis of a literature review. GBS antibiotic prophylaxis was considered to have been given if it was prescribed and administered exactly according to the national guidelines, which specify administration of antibiotic intravenous ampicillin (2 g at the beginning of labor, then 1 g every 4 hours until delivery, and 1 g during placental expulsion) or, if the patient is allergic, clindamycin or erythromycin to women who have a GBS‐positive perineal sample at term or at 35 weeks, prepartum bacteriuria or GBS carriage, a previous child with GBS infection, a temperature above 38°C, chorioamnionitis, a preterm delivery, or premature rupture of the membranes (more than 18 hours), or who were not screened for GBS.

In line with the CDC clinical definition,31 endometritis was suspected on the basis of clinical signs (purulent cervical discharge and/or pelvic pain and/or late uterine involution associated with fever) and was diagnosed clinically by the physician or midwife who administered the antibiotics. Although endometritis can be confirmed by culture of intrauterine samples obtained with protected swabs, such sampling requires high operator skills to limit the risk of uterine perforation and thus cannot be used routinely.32 In any case, the endometrial flora in patients with endometritis tends to be relatively standard. Data on vaginal samples are not an appropriate substitute for microbiological data. UTI was diagnosed on the basis of a leukocyte count of more than 103 leukocytes/mL, a pathogen concentration of more than 105 cfu/mL in urine culture, and clinical symptoms in women who, according to a dipstick test, had no UTI on admission to the hospital.

Nosocomial infections were recorded during a patient’s hospital stay and during the first 30 days after delivery. Each maternity unit was free to use their method of choice to organize the postdischarge survey. Incidence of endometritis was the principal outcome measure, and incidence of UTI was the secondary outcome measure. On the basis of assumptions from earlier studies (24% of patients receive antibiotics, 0.8% develop endometritis, and administration of antibiotics reduces the incidence rate by half), an adequately powered study needed to include 15,780 vaginal deliveries (α = .05 and β = .20).30

The maternity units used Epi Info software, version 6 (Epidemiology Program Office; CDC), for data entry. Data were sent to one of us (R.G.) at the Centre Hospitalier Lyon Sud for validation, consolidation, and analysis using Epi Info, version 6, and SPSS statistical software, version 11.0 (SPSS). Infection rates for mothers who did and who did not receive antibiotic prophylaxis were compared by the Fisher exact test. Univariate analysis of potential risk factors was performed using the Mantel‐Haenszel χ2 test for categorical variables and the Student t test or Mann‐Whitney U test for continuous variables. Stepwise logistic regression was used for a multivariate analysis of selected variables (cutoff level, ).

Results

 

Overall, 48 maternity units took part in the study for 1‐12 periods lasting 4 months each. A total of 49,830 vaginal deliveries occurred during these periods, and full data were available for 49,786 deliveries. The number of deliveries ranged from 219 to 4,436 per maternity unit.

Information on GBS antibiotic prophylaxis was missing for only 0.6% of the deliveries. Of 49,786 women, 7,883 (15.9%) who were considered to be at risk of GBS infection received antibiotics. However, the percentage of at‐risk women varied widely and significantly among maternity units (range, 4.4%‐26.0%; median, 15.8%; 25th percentile, 12.1%; and 75th percentile, 19.0%) ( , by Mantel‐Haenszel χ2 test). The lower percentages were observed in the maternity units of local hospitals, and the higher percentages in those of teaching hospitals, as expected from recruitment differences.

The number and rates of nosocomial infection (endometritis and UTI) are given in Table 1 for women who did and did not receive GBS antibiotic prophylaxis. Only the rate of endometritis was significantly reduced with GBS antibiotic prophylaxis (0.11% vs 0.25% [ ]). The rate of UTIs decreased from 0.37% to 0.32%, but this difference was not statistically significant ( ).

Table 1. 
Table 1.  Incidence of Endometritis and/or Urinary Tract Infection (UTI) for Women Who Did and Did Not Receive GBS Antibiotic Prophylaxis After Vaginal Delivery

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The results of univariate analyses of potential risk factors (categorical variables) for endometritis and UTI are given in Table 2. Endometritis was associated with primiparity ( , vs multiparity) and instrumental delivery ( , vs noninstrumental delivery). With respect to continuous variables, the group of women who developed postpartum endometritis were younger than the group who did not (mean age, 27.8 vs 29.4 years; ) and had a greater number urinary catheterizations during labor (mean, 0.86 vs 0.68 procedures per patient; median, 1 procedure per patient for both groups; ). Postpartum UTI was associated with UTI during pregnancy ( , vs no UTI during pregnancy), premature rupture of membranes ( , vs no premature rupture of membranes), blood loss of more than 800 mL ( , vs less blood loss), receipt of epidural analgesia ( , vs. no epidural analgesia), instrumental delivery ( , vs noninstrumental delivery), and receipt of more than 5 digital vaginal examinations after rupture of the membranes ( , vs receipt of fewer digital vaginal examinations). With respect to continuous variables, the group of women who developed postpartum UTI had a greater number of urinary catheterizations during labor than the group who did not (mean, 1.01 vs 0.68 procedures per patient; median, 1 procedure per patient for both groups; ); however, no difference in age was observed (mean, 29.4 vs 29.4 years, ).

Table 2. 
Table 2.  Univariate Analysis of Categorical Variables Possibly Associated With Endometritis and/or Urinary Tract Infection (UTI) After Vaginal Delivery

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Stepwise logistic regression analysis that included all the variables for which the P value was less than or equal to .1 in the univariate analyses confirmed that age and instrumental delivery were risk factors for endometritis, and that UTI during pregnancy, instrumental delivery, receipt of epidural analgesia, and receipt of more than 1 urinary catheterization during labor were risk factors for postpartum UTI (Table 3). The incidence of endometritis was significantly reduced in women who received antibiotic prophylaxis. However, the reduction in the incidence of UTI did not reach statistical significance.

Table 3. 
Table 3.  Risk Factors Significantly Associated With Endometritis or Urinary Tract Infection (UTI) in Logistic Regression Analysis

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Discussion

 

Our prospective study of 49,786 vaginal deliveries in 48 maternity units revealed that antibiotic prophylaxis against GBS appears to be a significant confounding factor for endometritis. The incidence of endometritis decreased significantly (from 0.25% to 0.11%) after administration of GBS antibiotic prophylaxis was implemented in accordance with national guidelines.33 The decrease in the UTI rate (from 0.37% to 0.32%) was not statistically significant ( ). Reasons for confidence in these results are the large number of women included in the study, the surveillance network’s control over factors that influence data comprehensiveness and validity, and the use of a multivariate analysis that accounted for potential confounding factors.

UTI is the most common postpartum infection.5 Since our surveillance network was set up, the rate of UTIs has decreased from 0.6% of deliveries in 1997‐1998 to 0.5% in 2001 to 0.4% in 2004. Our study has confirmed that UTI during pregnancy and the number of urinary catheterizations during labor are risk factors for postpartum infection.6 Screening for UTI during a woman's 9‐month pregnancy checkup has been recommended.34

The postpartum endometritis incidence rate that we found among patients who did not receive GBS prophylaxis was 0.25%, which is lower than the rate of approximately 1%‐4% reported elsewhere and is decreasing with time (0.3% in 2001 vs 0.5% in 1997‐1998).8,13,14 This decrease could be attributed to the requirements of the surveillance network, in the same way that decreases have been attributed to the requirements of the CDC nosocomial infection surveillance networks. If endometritis is not diagnosed and treated early, complications such as pelviperitonitis, peritonitis, pelvic thrombophlebitis, septicemia, and even meningitis (which accounts for less than 1% of cases of meningitis in adults) may occur.35 The reduced rate of endometritis that we found among patients who received GBS prophylaxis was 0.03%, which is similar to the reduced rate observed in a comparative study of 3 prevention protocols.26 It is also in line with earlier conclusions by Krohn et al.36 that 157 [2.0%] of 7,922 women had postpartum endometritis and a published review by Thinkhamrop et al.37 that found that prophylaxis during the second or third trimester of pregnancy reduces risk of endometritis (odds ratio, 0.48 [95% confidence interval, 0.29‐0.78]).

A significant risk factor for endometritis in our multivariate analysis was intrumental delivery ( ). The risk of maternal infections is known to be higher after endouterine procedures (use of forceps and artificial rupture of membranes or uterine revision [ie, manual exploration of the uterine cavity]), even when proper aseptic measures are taken. Routine administration of antibiotic prophylaxis has been proposed for women who undergo such procedures, but its efficacy is not proven.38

Findings that there is a possible relationship between endometritis and GBS infection are conflicting.32,39 We do not know the percentage of women with endometritis who had GBS‐positive culture results in this study, because data on other additional variables were not recorded by the network. The preferred antibiotic for GBS prophylaxis in the United States is penicillin G, to which 0.001% of patients are allergic. The French maternity units in our network use ampicillin, because the rate of resistance to this agent is low, it is available in oral form (for neonates), it is not expensive, and it provides a highly satisfactory drug concentration in the blood, urinary tract, and placenta. The present study was not designed to compare antibiotic protocols. The issues of antibiotic choice, dosage, potential for emergence of resistance, and cost are still being debated and need to be studied in similar studies that included more cases because of the very low incidence of endometritis.6,14,40 Administration of antibiotics other than ampicillin in the intrapartum period—for instance, after endouterine procedures—for UTIs at admission, or for prophylaxis against endocarditis, could influence rates of endometritis and UTI rates, but this was not documented in our study.

Overall, 14.7% of the women in our study received GBS antibiotic prophylaxis. The percentage varied widely according to hospital (2.6%‐26.3%), indicating that the proportion of women at risk of GBS infection probably depends on the maternity unit: women with a previous history of GBS infection and at high risk of premature delivery were admitted to level 3 maternity units. Our multivariate analysis demonstrates the relationship between GBS antibiotic prophylaxis and nosocomial infections with regard to individual risks. However, for comparison of nosocomial infection rates among maternity units, it is important to include in standardization methods all significant factors that are unequally distributed among maternity units, such as administration of GBS antibiotic prophylaxis.

Our observation that administration of GBS prophylaxis is a significant factor in the incidence of endometritis has 3 important repercussions. First, the conclusions of our study cannot be automatically generalized beyond maternity units with patient profiles and practices similar to those of the our surveillance network. Second, antibiotic prophylaxis needs to be taken into account in any study that compares the effect of administration of prophylaxis on the incidence of endometritis in different maternity units. Third and most importantly, administration of antibiotic prophylaxis must be taken into account in any calculation of the number of expected cases. Collating data on antibiotic prophylaxis has become mandatory in our network surveillance program since 2003 and has been included in the calculation of expected cases of endometritis since 2005.

Acknowledgments

 

The following members of the participating maternity units of the Mater Sud‐Est Network played an integral role in this study: S. Henry, MD, and M. Meiffre (Ales Hospital); M. Pier, MD, and E. Charignon (Annonay Hospital); T. Perez, MD, and N. Prost (Aubagne‐Casamance); I. Savelli, MD, and P.Y. Attali, MD (Aubagne Hospital); P. Mille, MD, and C. Durif (Aurillac Hospital); D. Lepreux, MD, and R. Martin (Avignon Hospital); A. Vialet, MD, and M. H. Hours (Bourgoin Jallieu Hospital); L. Serve, MD, C. Ghizzoni, and M. Basso (Brignoles Hospital); A. Cherasse, MD, V. Chaix, and F. Pospisil (Carpentras Hospital); C. Barbier, MD, and S. Lamard (Dole Hospital); P. C. Brochery, MD, and F. Blesius (Fréjus Hospital); A. Mansoor, MD, and C. Mayer (Issoire Hospital); B. de Pury, MD, and Y. Frikh (L’Arbresle Hospital and Perinatal Center); R.C. Rudigoz, MD, and F. Tissot‐Guerraz, MD (Lyon‐Cx Rousse); D. Disant, MD, and F. Vacca (Lyon‐St. Joseph/St. Luc); B. Gres, MD, and A. Poncet, MD (Montelimar Hospital); M. Beytout, MD, and J. Vincent (Moulins Hospital); P. Mares, MD, and C. Bremond (Nimes University Hospital Carémeau); M. Galli, MD, and M. Klein (Orange Hospital).

Potential conflicts of interest. All authors report no conflicts of interest relevant to this article.

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