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Administration of cefazolin prior to skin incision is superior to cefazolin at cord clamping in preventing postcesarean infectious morbidity: a randomized, controlled trial

      Objective

      The objective of the study was to determine whether the administration of cefazolin prior to skin incision was superior to administration at the time of umbilical cord clamping for the prevention of postcesarean infectious morbidity.

      Study Design

      This was a prospective, randomized, double-blind, placebo-controlled trial. Study subjects received cefazolin 15-60 minutes prior to incision and controls received cefazolin at the time of cord clamping. The occurrence of endomyometritis, wound infection, total infectious morbidity, and neonatal complications were compared.

      Results

      There were 357 subjects enrolled. No demographic differences were observed between groups. There were decreased total infectious morbidity in the study group (relative risk [RR] = 0.4, 95% confidence interval [CI] 0.18 to 0.87), decreased endometritis (RR = 0.2, 95% CI 0.15 to 0.94). No increase in neonatal sepsis (P = .99), sepsis workups (P = .96), or length of stay (P = .17) was observed.

      Conclusion

      Administration of prophylactic cefazolin prior to skin incision resulted in a decrease in both endomyometritis and total postcesarean infectious morbidity, compared with administration at the time of cord clamping. This dosing did not result in increased neonatal septic workups or complications.

      Key words

      Cesarean delivery is the most commonly performed surgery in the United States, with nearly 1.2 million procedures performed in 2004.
      National Institutes of Health State of the Science Conference Statement—cesarean delivery on maternal request.
      Infectious morbidity, consisting primarily of endomyometritis and wound infection, remains a leading cause of postoperative complications.
      • Henderson E.
      • Love E.J.
      Incidence of hospital-acquired infections associated with caesarean section.
      Estimates of postcesarean infection rates range from 7% to 20%, depending on demographic and obstetric variables.
      • Yokoe D.S.
      • Christiansen C.L.
      • Johnson R.
      • et al.
      Epidemiology of and surveillance for postpartum infections.
      • Ramsey P.S.
      • White A.M.
      • Guinn D.A.
      • et al.
      Subcutaneous tissue reapproximation, alone or in combination with drain, in obese women undergoing cesarean delivery.
      Infection following cesarean delivery results in not only increased hospital stay but also increases the cost of care. For example, diagnosing and treating a single case of endometritis is estimated to cost $815.
      • Chelmow D.
      • Hennesy M.
      • Evantash E.
      Prophylactic antibiotics for non-laboring patients with intact membranes undergoing cesarean delivery: an economic analysis.
      Prophylactic antibiotics can reduce the incidence of postcesarean infectious morbidity by as much as 75%.
      • Chelmow D.
      • Ruehli M.S.
      • Huang E.
      Prophylactic use of antibiotics for nonlaboring patients undergoing cesarean delivery with intact membranes: a meta-analysis.
      This risk reduction is observed in both planned and emergent cesareans.
      • Mohamed K.
      A double-blind randomized controlled trial on the use of prophylactic antibiotics in patients undergoing elective cesarean section.
      • Noyes N.
      • Berkeley A.S.
      • Freedman K.
      • Ledger W.
      Incidence of postpartum endomyometritis following single-dose antibiotic prophylaxis with either ampicillin/sulbactam, cefazolin, or cefotetan in high-risk cesarean section patients.
      First-generation cephalosporin antibiotics are the most commonly used agents and are usually administered following delivery of the infant after the cord is clamped.
      • Smaill F.
      • Hofmeyr G.J.
      Antibiotic prophylaxis for cesarean section.
      Neither the use of broad-spectrum antimicrobials nor the administration of additional doses postoperatively has been shown to be superior to a single-dose cephalosporin regimen.
      • Gall S.
      • Hill G.
      Single-dose versus multiple-dose piperacillin prophylaxis in primary cesarean operation.
      • Hager W.D.
      • Rapp R.P.
      • Billeter M.
      • Bradley B.B.
      Choice of antibiotic in nonelective cesarean section.
      Optimal timing for prophylactic antibiotic administration is based on animal studies that demonstrate a maximum protective effect when adequate tissue antibiotic levels are present prior to bacterial contamination.
      • Burke J.F.
      The effective period of preventive antibiotic action in experimental incisions and dermal lesions.
      However, concerns about neonatal exposure to antibiotics and the potential effect on a neonatal sepsis workup prompted obstetricians to delay the administration until the time of umbilical cord clamping.
      • Hopkins L.
      • Smaill F.
      In addition, there is concern regarding the potential selection of resistant pathogens, especially Escherichia coli.
      • Edwards R.K.
      • Clark P.
      • Sistrom C.L.
      • Duff P.
      Intrapartum antibiotic prophylaxis I: relative effects of recommended antibiotics on gram-negative pathogens.
      There is no prospective evidence to support these concerns. A recent randomized trial found no difference in neonatal sepsis, sepsis workups, or neonatal intensive care unit (NICU) admissions between groups administered prophylactic antibiotics preoperatively or at cord clamping.
      • Thigpen B.
      • Hood W.A.
      • Chauhan S.
      • et al.
      Timing of prophylactic antibiotic administration in the uninfected gravida: a randomized clinical trial.
      In the majority of surgical procedures that require prophylaxis, antibiotics are usually administered prior to the skin incision.
      • Page C.P.
      • Bohnen J.M.
      • Fletcher J.R.
      • McManus A.T.
      • Solomkin J.S.
      • Wittman D.H.
      Antimicrobial prophylaxis for surgical wounds.
      Delay in administration has been associated with increased surgical site infection risk.
      • Classen D.C.
      • Evans R.S.
      • Pestotnik S.L.
      • Horn S.D.
      • Menlove R.L.
      • Burke J.P.
      The timing of prophylactic administration of antibiotics and the risk of surgical-wound infection.
      Such data suggest a potential benefit of preoperative antibiotic dosing with cesarean procedures.
      There are limited data to address the timing of cesarean antibiotic prophylaxis. In a small randomized trial [n = 90], Wax et al
      • Wax J.R.
      • Hersey K.
      • Philput C.
      • et al.
      Single dose cefazolin prophylaxis for postcesarean infections: before vs. after cord clamping.
      concluded that there was no difference in infectious morbidity between preoperative antibiotics and those given at cord-clamp. Fejgin et al
      • Fejgin M.D.
      • Markov S.
      • Goshen S.
      • Segal J.
      • Arbel Y.
      • Lang R.
      Antibiotic for cesarean section: the case for true prophylaxis.
      reported decreased wound infections (P = .008) in a prospective trial (n = 435) with use of preoperative antibiotic prophylaxis. More recently Thigpen et al
      • Thigpen B.
      • Hood W.A.
      • Chauhan S.
      • et al.
      Timing of prophylactic antibiotic administration in the uninfected gravida: a randomized clinical trial.
      demonstrated a decrease in total infectious morbidity with preoperative antibiotics but not specifically with the outcomes of endomyometritis or wound infection.
      A Cochrane database review from 2002 concluded that an adequately powered randomized trial was needed to address this issue.
      • Smaill F.
      • Hofmeyr G.J.
      Antibiotic prophylaxis for cesarean section.
      To this end, we performed a prospective, double-blinded, randomized clinical trial to determine whether antibiotic prophylaxis administered preoperatively was more effective in preventing infectious morbidity following cesarean delivery than administration following cord clamp.

      Materials and Methods

      The Institutional Review Board at the Medical University of South Carolina (MUSC) and the research division of the Department of Obstetrics and Gynecology approved this project (approval #11120, January 2003). In addition, the trial was registered with the federal government and posted on the Clinical Trials.gov (Clinical Trials.gov) clearinghouse (NCT00330278).
      This was a randomized, double-blinded, placebo-controlled trial. Total postcesarean infectious morbidity was the primary outcome. Power was calculated a priori using MUSC infection control data, which indicated a historical postcesarean infection incidence of 17%. Using a power of 0.80 and an alpha of 0.05, 174 subjects per arm were calculated to be necessary to detect a 50% decrease in overall infectious morbidity for subjects given preoperative antibiotic prophylaxis. Primary and secondary outcomes were defined prior to the beginning of enrollment.
      Subjects were eligible for the trial if they were older than 24 weeks estimated gestational age and required cesarean delivery. Exclusion criteria included cephalosporin allergy, age less than 18 weeks, exposure to any antibiotic agent within 1 week of delivery, or the need for emergent cesarean delivery. Following informed consent, simple randomization using a random number table was performed by the investigational pharmacy staff. Consolidated Standard of Reporting Trials (CONSORT) standards for randomization were followed.
      Infusion bags were prepared in accordance with randomization and the bags labeled as A or B. One bag contained 1 g of cefazolin mixed with 50 cc of normal saline. The other bag contained only 50 cc of normal saline. Bag A was administered at least 15 minutes prior to skin incision but no more than 60 minutes before. This interval was chosen based on previously published maternal pharmacokinetics of cefazolin.
      • Fiore Mitchell T.
      • Pearlman M.D.
      • Chapman R.L.
      • Bhatt-Mehta V.
      • Faix R.G.
      Maternal and transplacental pharmacokinetics of cefazolin.
      Bag B was administered at the time of cord clamping by the anesthesia staff present for the procedure. Providers and patients were blinded to the contents of the bags until the conclusion of the study.
      Subjects were followed through their hospital course and up to the 6-week postpartum visit. Infectious morbidity was documented using established clinical criteria.
      • Faro S.
      • Soper D.E.
      Endomyometritis was diagnosed if maternal fever greater than 100.4°F on 2 separate occasions along with uterine fundal tenderness, tachycardia, or leukocytosis. Wound infection was diagnosed if there was purulent discharge, erythema, and induration of the incision site. Hematomas, seromas, or wound breakdowns in the absence of previously discussed signs were not considered wound infections. Pyelonephritis was diagnosed by maternal temperature, flank pain, and urine culture showing more than 100,000 colonies of a gram negative uropathogen.
      Neonatal sepsis was diagnosed by a positive blood culture. Organism, antibiotic resistances, and clinical course data were recorded. Length of stay, admission status, and decision to undertake a sepsis workup were determined by the staff neonatologists who were also blinded to group assignment.
      Study data were analyzed using SPSS version 12.0 (Chicago, IL). Normality of the data was tested with Kolmogorov-Smirnov and χ2 goodness-of-fit tests when appropriate. χ2 comparisons were performed for categorical variables and relative risks (RR) with 95% confidence interval were calculated. Analysis of variance testing was performed when multiple groups of categorical variables were encountered. Student t tests were used for continuous variable analysis. A logistic regression was also performed to obtain adjusted relative risk values. A P value of less than .05 was considered statistically significant.

      Results

      There were 367 subjects consented for this trial. Ten subjects did not complete randomization because of either medication delay, previously undiscovered exclusion criteria, or development of a need for emergent cesarean delivery. Three hundred fifty-seven subjects completed randomization and received the study medications. Eight subjects were lost to 6-week postpartum follow-up but were included in the final analysis because their hospital course data were available. The Figure illustrates the randomization scheme. Completion of the trial was accomplished in 26 months.
      Figure thumbnail gr1
      FigureSubject flow through the cefazolin trial
      Table 1 summarizes the demographic variables measured in the study and control groups. There were no significant differences observed between the study and control groups. Table 2 illustrates the clinical obstetric variables measured between the two groups. There were again no significant differences observed between the preoperative or cord-clamping groups. There were no cases of maternal anaphylaxis or other adverse events related to cefazolin use reported during the trial.
      Table 1Demographic variable comparison
      VariableStudy group (n = 175)Control group (n = 182)P value
      Maternal age28.3 ± 6.128.3 ± 6.01.0
      Maternal weight225.3 ± 144.5228.1 ± 152.9.85
      Parity1.41.2.07
      Race (C/AA/H/other)
      Caucasian, African American, Hispanic, other.
      72/77/21/582/65/31/4.45
      Medicaid>87 (49%)82 (45%).61
      Premature delivery (less than 37 wks)30 (17%)46 (25%).08
      low asterisk Caucasian, African American, Hispanic, other.
      Table 2Obstetric variable comparisons
      VariableStudy group (n = 175)Control group (n = 182)P value
      Indication for C/S (Arr, NRFS, NL, other)50/36/51/3854/39/44/45.68
      Diabetes17 (10%)29 (16%).10
      Multiple gestation12 (7%)19 (10%).31
      Preeclampsia18 (10.3%)25 (13.7%).4
      Estimated blood loss (cc)878 ± 112895 ± 127.18
      ROM time (h)6.1 ± 5.06.8 ± 5.4.20
      Internal monitors23 (13%)25 (13.7%).87
      Subcutaneous drain6 (3.4%)13 (7%).12
      Operative time (min)45.3 ± 13.648 ± 14.9.07
      Arr, arrest disorders; C/S, cesarean section; NRFS, nonreassuring fetal status; NL, not laboring; ROM, rupture of membranes.
      Infectious morbidity outcomes are summarized in Table 3. There were more cases of endomyometritis in the control group (n = 10) than in the study group (n = 2), and this difference was statistically significant (RR = 0.2, 95% confidence interval [CI] 0.15 to 0.94). There were also more cases of wound infection in the control group (n = 10) than in the study group (n = 5); however, this difference did not reach statistical significance (RR = 0.52, 95% CI 0.18 to 1.5). Seven cases of hematomas or seromas that did not meet criteria for wound infections were noted. There was 1 case of pyelonephritis in the control group and 1 case of pneumonia in the study group. Overall, total infectious morbidity in the control (n = 21) group was higher than in the study group (n = 8), and this difference was statistically significant (RR = 0.4, 95% CI 0.18 to 0.87). A logistic regression model was performed to adjust for 6 demographic and clinical variables that are associated with infectious risk and were noted to trend toward the control group. The adjusted odds ratios are reported in Table 3 and were not significantly different from the crude relative risks.
      Table 3Infectious morbidity
      Summary of postcesarean infectious morbidity observed
      OutcomeStudy group (n = 175)Control group (n = 182)Relative risk 95% CIAdjusted OR 95% CI
      Endomyometritis2 (1%)10 (5%)0.2 (0.2 to 0.94)0.22 (0.05 to 0.9)
      Wound infections5 (3%)10 (5%)0.52 (0.18 to 1.5)0.4 (0.1 to 1.3)
      Total infectious morbidity8 (4.5%)21 (11.5%)0.4 (0.18 to 0.87)0.35 (0.14 to 0.82)
      OR, odds ratio.
      The neonatal outcome variables are illustrated in Table 4. There were no significant differences observed between the 2 groups in neonatal sepsis (P = .99), NICU admission (P = .4), total length of stay (P = .17), metabolic acidosis (P = .88), or sepsis workups (P = .96). There were significantly fewer NICU admission days in the preoperative antibiotic group (P < .01).
      Table 4Neonatal outcomes
      VariableStudy group (n = 185)Control group (n = 194)P value
      Birthweight3034 ± 7322947 ± 989.35
      Gestational age37.5 ± 2.837 ± 3.1.11
      Sepsis6 (3%)7 (3.6%).99
      Septic workup35 (19%)36 (18.5%).96
      NICU admission25 (13.5%)33 (17%).40
      Intermediate admission35 (19%)32 (16.4%).65
      NICU days14.2 ± 15.819.7 ± 24.9.01
      Length of stay6.6 ± 9.98.5 ± 15.8.17
      pH less than 7.110 (5%)12 (6%).88
      In addition, the neonatal cases of sepsis did not demonstrate different causative organisms between groups or an increased incidence of antibiotic resistant organisms. Table 5 lists the causative organisms and their resistance profiles.
      Table 5Neonatal sepsis organisms
      SubjectTreatment groupCultured organismDay of lifeResistances
      11Staphylococcus aureus14None
      21Staphylococcus aureus24Methicillin
      32Enterobacter cloacae14None
      42Staphylococcus aureus3Methicillin
      52Enterobacter cloacae7None
      61Escherichia coli10Ampicillin
      72Pseudomonas aeriginosa35None
      82Staphylococcus aureus26Methicillin
      91Serratia marcesens3None
      102Staphylococcus aureus11Methicillin
      111Staphylococcus aureus11None
      122Staphylococcus aureus5None
      131Klebsiella pneumoniae23None
      Treatment groups: 1, study group; 2, control group.

      Comment

      Postcesarean infectious morbidity is common and costly and rarely can lead to life-threatening conditions such as necrotizing fasciitis.
      • Goepfort A.R.
      • Guinn D.A.
      • Andrews W.W.
      • Hauth J.C.
      Necrotizing fasciitis after cesarean delivery.
      Cesarean infectious rates have been shown to be higher than in comparable surgical procedures.
      • Gaynes R.P.
      • Culver D.H.
      • Horan T.C.
      • Edwards J.R.
      • Richards C.
      • Tolson J.S.
      Surgical site infection (SSI) rates in the United States, 1992-98: the National Nosocomial Infections Surveillance System basic SSI risk index.
      Whereas it is impossible to compare outcomes across different procedures, 1 possible explanation for this difference is the common practice of delaying prophylactic antibiotics until cord clamping for neonatal concerns. The neonatal concerns often cited to justify this practice have not been validated by prospective trials. On the contrary, previous studies have demonstrated no increase in neonatal sepsis or sepsis workups when prophylactic antibiotic are given preoperatively.
      • Thigpen B.
      • Hood W.A.
      • Chauhan S.
      • et al.
      Timing of prophylactic antibiotic administration in the uninfected gravida: a randomized clinical trial.
      Our study confirms these findings and, in fact, revealed a trend toward decreased NICU admission and length of stay in the preoperative antibiotic group. We do not believe this is causative but merely more evidence of no neonatal harm.
      Our study confirms the findings in the animal models of antibiotic prophylaxis of Burke.
      • Burke J.F.
      The effective period of preventive antibiotic action in experimental incisions and dermal lesions.
      He demonstrated that the size of Staphylococcus-induced lesions were reduced when antibiotic tissue levels were present before bacterial contamination. It is probable that it is this mechanism that explains the benefit of preoperative antibiotics. Waiting until cord clamping to administer antibiotics allows bacterial contamination of the uterus and subcutaneous tissues well before adequate tissue levels can be achieved.
      Strengths of this study include its design as a randomized, double-blind, placebo trial. The a priori power was achieved, and the randomization scheme achieved its purpose of no major variable differences between groups. A weakness of the trial is the high-risk nature of the study population. This population was more obese, more likely to have diabetes, preterm delivery, multiple gestation, and be of minority ethnicity than the general population. This is not surprising, given that the location of the trial was in a tertiary care center. In addition, all cesareans in this study were performed by resident physicians as the primary surgeons. This resulted in a longer average surgery time, which is a risk factor for infectious morbidity.
      • Mangran A.J.
      • Horan T.C.
      • Pearlson M.L.
      • Silver L.C.
      • Jarvis W.R.
      Guideline for prevention of surgical site infection.
      The marked reduction of infectious morbidity with preoperative antibiotics seen in this trial may be less dramatic in a less obese, lower-risk population.
      Overall, given the significant reductions in both endomyometritis and total postcesarean infectious morbidity, we would recommend the routine administration of prophylactic antibiotics preoperatively for cesarean section. Exact timing would depend on the pharmacokinetics of the individual agent because we used 15-60 minutes prior to skin incision with cefazolin to achieve tissue levels.
      • Fiore Mitchell T.
      • Pearlman M.D.
      • Chapman R.L.
      • Bhatt-Mehta V.
      • Faix R.G.
      Maternal and transplacental pharmacokinetics of cefazolin.
      This recommendation would appear not to represent a neonatal risk for either sepsis or selection of resistant organisms based on our and previous studies findings. There is no known maternal risk to preoperative dosing of antibiotics as well. Given that there is no increase in cost associated with this recommendation and the expected reduction in infectious morbidity, it is likely to be cost effective as well. Future studies designed to confirm the potential cost savings of this recommendation are needed.

      Acknowledgments

      We thank Myla Ebeling, MS; Charles Rittenberg, MD; Kathryn Menard, MD, MPH; Kimberly Porter, PharmD; and the MUSC resident physicians.

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      • Correction
        American Journal of Obstetrics & GynecologyVol. 197Issue 3
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          The article, “Administration of cefazolin prior to skin incision is superior to cefazolin at cord clamping in preventing post-cesarean infectious morbidity: a randomized controlled trial,” by Sullivan et al, published in the May 2007 issue (volume 196, page 455.e1) contains an error.
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