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Surgical Site Infections in Orthopedic Surgery: The Effect of Mupirocin Nasal Ointment in a Double-Blind, Randomized, Placebo-Controlled Study

  1. M. D Kalmeijer1,
  2. H Coertjens2,
  3. P. M van Nieuwland-Bollen2,
  4. D Bogaers-Hofman2,
  5. G. A. J de Baere3,
  6. A Stuurman1,
  7. A van Belkum4, and
  8. J. A. J. W Kluytmans2
  1. 1Departments of Pharmacy, Amphia Hospital, Breda
  2. 2Departments of Clinical Microbiology and Infection Prevention, Amphia Hospital, Breda
  3. 3Departments of Orthopedic Surgery, Amphia Hospital, Breda
  4. 4Departments of Department of Medical Microbiology and Infectious Diseases, Erasmus University Medical Center Rotterdam, The Netherlands
  1. Reprints or correspondence: M. D. Kalmeijer, Dept. of Pharmacy, Academic Medical Center, University of Amsterdam, Postbus 22660, 1100 DD Amsterdam, The Netherlands (m.d.kalmeijer{at}amc.uva.nl)
 
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Abstract

The objective of this study was to determine whether use of mupirocin nasal ointment for perioperative eradication of Staphylococcus aureus nasal carriage is effective in preventing the development of surgical site infections (SSIs). A randomized, double-blind, placebo-controlled design was used. Either mupirocin or placebo nasal ointment was applied twice daily to 614 assessable patients from the day of admission to the hospital until the day of surgery. A total of 315 and 299 patients were randomized to receive mupirocin and placebo, respectively. Eradication of nasal carriage was significantly more effective in the mupirocin group (eradication rate, 83.5% versus 27.8%). In the mupirocin group, the rate of endogenous S. aureus infections was 5 times lower than in the placebo group (0.3% and 1.7%, respectively; relative risk, 0.19; 95% confidence interval, 0.02–1.62). Mupirocin nasal ointment did not reduce the SSI rate (by S. aureus) or the duration of hospital stay

Surgical site infections (SSIs) are important complications of orthopedic procedures that involve prosthetic implants. A recent national surveillance study showed that, in The Netherlands, the mean rates of infection in orthopedic surgery that involved artificial implants ranged from 1.5% for total knee implantation to 6.8% for femur head replacement [1]. These infections are associated with discomfort for the patient and with considerable prolongation of hospital stay and increased cost of care [2–7]. When a deep SSI of a prosthetic implant develops, removal of the prosthesis is often required

Several risk factors for the development of SSIs have been identified. The 1999 guidelines of the Centers for Disease Control and Prevention (CDC) for the prevention of SSI included, for the first time, preoperative nasal carriage of Staphylococcus aureus as a risk factor for SSI [8]. The first studies to have suggested a relationship between nasal carriage of S. aureus and SSI were performed in the late 1950s and early 1960s. These observations were further confirmed by several more recent studies [9]. These studies showed that preoperative nasal carriage of S. aureus is associated with an increased risk of developing an SSI with the same strain. In a study of patients undergoing orthopedic surgery with prosthetic implants, nasal carriage of S. aureus was the most important independent risk factor for developing SSI [10]. Compared with persons who did not have nasal carriage, those with carriage had an RR of developing an SSI of 8.9 (95% CI, 1.7–45.5)

These findings led to the hypothesis that perioperative elimination of nasal carriage could lower the infection rate. Mupirocin nasal ointment is highly effective in eliminating S. aureus [11, 12]. In a study involving cardiothoracic surgery [13], perioperative elimination of nasal carriage with this ointment resulted in a significantly lower SSI rate. However, this study used a historical control group. In the present randomized, double-blind, placebo-controlled study, we evaluated the effectiveness of perioperative mupirocin nasal ointment in the prevention of SSI in orthopedic surgery with artificial implant material

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Methods

Selection of patients. The study was performed from January 1997 through July 1999 at the Department of Orthopedic Surgery at the Ignatius Hospital, Breda, The Netherlands. All patients undergoing elective orthopedic surgery during which prosthetic implant material was used (i.e., hip, knee, or back surgery) were eligible for the study, as were patients undergoing a revision operation of the same type. Every patient was included only once. Patients with an active infection at the moment of inclusion and who had received antibiotic treatment in the previous 24 h were excluded. The ethics committee of the hospital approved the study protocol, and appropriate written informed consent was obtained from all patients

Study medication. Mupirocin nasal ointment (GlaxoSmithKline; lot 550150/96G04) contains 2.15% weight/weight mupirocin calcium in a soft, white ointment base consisting of paraffin and a mixture of glycerin esters (Softisan 649). The placebo ointment was produced in the hospital pharmacy from paraffin (Bufa; lot 96H16GR) and Softisan (GlaxoSmithKline; lot 5051293), according to the GlaxoSmithKline protocol. Both active and placebo ointment were placed in 5-g tubes and numbered according to an individual randomization list by an independent pharmacist. The appearance of both ointments was identical

Treatment. Generally, patients were admitted to the hospital the day before surgery was performed. On that day, if necessary, depilatory cream was used to remove hair. A nasal swab was done of both nares for culture. Thereafter, therapy with mupirocin or placebo nasal ointment was administered according to the next number on the randomization list. The ointment was applied to both nares twice per day. The first dose of ointment was applied by one of the investigators. Treatment was continued by the nursing staff until the day of surgery. Before surgery, ⩾2 doses of nasal ointment were administered. In persons with nasal carriage, a posttreatment sample was obtained for culture 3–5 days after surgery

Cefamandole was given as perioperative antibiotic prophylaxis to all patients according to the following schedule: 2 g at 30–60 min before surgery, followed by 2 more doses of 1 g each at 8 h and 16 h after surgery. If patients were allergic to cephalosporins, clindamycin was given according to the following schedule: 600 mg at 30–60 min before surgery, followed by 2 more doses of 600 mg each at 8 h and 16 h after surgery

Nasal culture. Swabs of both nares were obtained with a Dacron swab. The swab was inoculated on a blood agar plate and on a mannitol salt agar plate. The material was spread into quadrants with a sterile loop [14]. The amount of growth was scored semiquantitatively. Growth of S. aureus limited to the first sector on the blood agar plate was scored as level 1 colonization. Growth up to the second, third, and fourth sector were scored as level 2, 3, and 4 colonization, respectively. The S. aureus strains isolated from nose swabs and wound specimens were typed by means of pulsed-field gel electrophoresis (PFGE) according to a protocol that has been described elsewhere [15]. DNA was embedded in agarose blocks and digested with the restriction enzyme SmaI (Boehringer Mannheim). PFGE was performed in 1% Seakem agarose gels (FMC Bioproducts) buffered in 0.5× Tris-borate-EDTA at 14°C. Electrophoresis (BioRad CHEF Mapper) was performed for 22 h (ramping, 2.16–44.69 s) at an angle of 120° at 6 V/cm. Banding patterns were scored and interpreted according to the criteria of Tenover et al. [16]

Variables and infection surveillance. The following variables were recorded: age, sex, body mass index (weight/[length]2; in kg/m2), kind of procedure performed, date of the admission to the hospital, date of surgery, date of discharge, total length of hospital stay, postoperative length of hospital stay, duration of the operation, surgeon (numbered 1 to 7), underlying disease (malignancy or diabetes mellitus), use of immunosuppressive drugs, American Society of Anesthesiologists score, method of anesthesia (general or spinal/epidural), level of growth for the first nasal swab, and level of growth for the posttreatment nasal swab. The medical records of all patients were studied for the development of SSI on the bases of criteria of the CDC [17]. The development of SSI was observed until 1 month after surgery. After discharge from the hospital, follow-up studies were performed over the phone by use of a standardized questionnaire that was based on CDC criteria. Patients were asked whether they had experienced any of the following symptoms: purulent drainage from the incision, pain and tenderness, and redness or heat; in addition, they were asked whether an antibiotic had been prescribed and whether a specimen of the wound had been obtained for culture. If one of the answers indicated an infection, the patient was seen at the outpatient department by an orthopedic surgeon for further evaluation. We checked all patients to see whether they were readmitted to the hospital and whether this readmission was for wound infection. For SSI, the date of onset and pathogens involved were recorded

Outcome. The primary outcome was the SSI rate. Secondary outcomes were the rate of SSIs due to S. aureus, the rate of endogenous S. aureus SSIs, and the duration of hospital stay. An endogenous SSI was defined as an SSI with a S. aureus isolate that was identical on PFGE analysis to the nasal isolate of that patient

Statistical analysis. The sample size was calculated by using the results of a previous surveillance study conducted in this department [10]. On the basis of an incidence of SSI of 6.6%, a reduction of 75%, and a power of 80%, with a significance level of 95%, ∼300 patients were needed for each treatment group

An intent-to-treat analysis was performed. Results were analyzed using SPSS software (SPSS). Differences between groups were tested by use of Student's t test, Fisher's exact test, or Wilcoxon rank sum test, as appropriate. P <.05 was considered to be statistically significant

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Results

During the study period, 692 patients were eligible for inclusion in the study; 65 patients (9.4%) were unwilling to participate. Of the 627 included patients, 13 could not be evaluated. Seven of these 13 patients did not undergo surgery, and 6 patients had to be excluded for the following reasons: 2 patients had an active infection that was detected after inclusion, 2 patients were included for the second time, and, in 2 patients, the respective study medications were possibly mixed up. None of these patients developed an SSI

The remaining 614 patients were included in the intent-to-treat analysis. Of these 614 patients, 43 (7.0%) underwent surgery that did not involve the use of prosthetic material, which resulted in 571 patients (93.0%) fulfilling the inclusion criteria. In the intent-to-treat analysis, 315 patients were randomized to the mupirocin group and 299 to the placebo group. Both groups were comparable with respect to sex, age, body mass index, type of surgical procedure, duration of surgery, underlying disease, immunosuppressive therapy received, American Society of Anesthesiologists score, and surgeon (table 1). Also, no differences were found in the method of anesthesia and the distribution of operations among the surgeons (data not shown). All patients received ⩾2 doses of nasal ointment before undergoing surgery

Figure 1
Figure 1

Results of pulsed-field gel electrophoresis typing of Staphylococcus aureus strains

Table 1
Table 1

for surgical site infections after orthopedic surgery performed with artificial implant material

The mupirocin and placebo groups were also comparable with respect to the preoperative nasal carriage rates: 30.3% in the mupirocin group and 28.8% in the placebo group had nasal carriage of S. aureus (table 2). After treatment, 15 of the 95 patients who were initially carrying S. aureus in the mupirocin group and 61 of 86 in the placebo group were still carrying S. aureus (P <.05). In 12 patients, no nasal swab was taken to control for effectiveness of treatment. None of these patients developed an SSI or an SSI with S. aureus Typing with PFGE revealed that, of the posttreatment cultures that yielded S. aureus in the placebo group, 84% contained the original S. aureus strain. In the mupirocin group, this rate was 80%. Almost all patients (99.3%) received cefamandole as antibiotic prophylaxis. Three patients received clindamycin, and 1 patient did not receive perioperative prophylaxis. This patient did not develop an SSI. The SSI rates in the mupirocin and placebo groups were comparable (3.8% and 4.6%, respectively; table 3). Also the rates of SSI caused by S. aureus were not significantly different (mupirocin group, 1.6%; placebo group, 2.7%)

Table 2
Table 2

Baseline and posttreatment rates of nasal carriage of Staphylococcus aureus in 614 patients assessed for surgical site infections after orthopedic surgery performed with artificial implant material

Table 3
Table 3

Surgical site infection (SSI) rates for 614 patients assessed for SSIs after orthopedic surgery performed with artificial implant material

Overall, 13 infections with S. aureus occurred (5 infections in the mupirocin group and 8 in the placebo group). Of the 5 patients in the mupirocin group infected with S. aureus, 2 had nasal carriage (figure 1). On the basis of the outcome of the PFGE analysis of pre- and posttreatment S. aureus isolates, it was concluded that 1 of these persons with nasal carriage developed an endogenous infection. Of the 8 patients infected with S. aureus in the placebo group, 5 had nasal carriage. These 5 persons with nasal carriage all developed an endogenous infection. Endogenous S. aureus infections were 5 times less likely to occur in the mupirocin group, but this difference was not statistically significant (RR, 0.19; 95% CI, 0.02–1.62). No statistically significant differences were found between different types of surgery (data not shown). Each of the 7 exogenous strains was unique. All S. aureus strains in the study were susceptible to cefamandole and clindamycin, as was expected, because methicillin-resistant S. aureus is not endemic in The Netherlands. Also, all strains were susceptible to mupirocin

The mean (±SD) duration of hospital stay was comparable in both groups: 15.0 ± 6.3 days in the placebo group and 14.7 ± 7.3 days in the mupirocin group. Five patients were readmitted to the hospital: 2 patients in the mupirocin group (for repositioning) and 3 patients in the placebo group (1 for removing the prosthesis as a result of a deep infection and 2 for repositioning)

In addition to the intent-to-treat analysis, an analysis was performed of the 571 patients who complied with the inclusion criteria. The results of this analysis were not significantly different from the results of the intent-to-treat analysis. Also, all patients not included in the study during the study period underwent infection surveillance. No higher infection rate was found in this group of patients

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Discussion

The initial nasal carriage rate of S. aureus of ∼30% found in this study population falls within the range of nasal carriage rates reported in other studies [9]. Treatment resulted in an elimination rate of 83.5% among mupirocin recipients and 21.8% among placebo recipients. In an analysis of 6 clinical trials, Doebbeling et al. [11] reported a range of elimination rates of 68%–100% (mean, 91%) for patients who received mupirocin twice per day for 5 days, and they reported a range of elimination rates of 1%–13% (mean, 6%) for patients who received the same regimen with placebo. Compared with these results, the short treatment course in the present study was relatively effective. Because placebo is not effective in vitro against S. aureus, the reduction in the placebo group is most likely a naturally occurring phenomenon that is the result of intermittent carriage, not an effect of placebo cream on S. aureus [9]. As can be concluded from table 2, the effectiveness of mupirocin, on the basis of the elimination of the original strain, was 86.8%, compared with 34.6% for the placebo ointment (P <.05)

This perioperative eradication, however, did not result in a significant difference in primary outcome, the overall rate of SSI. Also, in the secondary outcomes (rate of SSI due to S. aureus, rate of endogenous S. aureus infection, and the duration of hospital stay), no significant differences were found, although all were lower in the mupirocin group. Therefore, the conclusion could be that perioperative treatment with mupirocin nasal ointment is not effective in SSI prevention in orthopedic surgery with artificial implant material. This is not in accordance with the results of earlier intervention studies of nasally administered mupirocin. In another study involving orthopedic surgery, the rate of SSI was reduced significantly, from 2.7% to 1.3%. The rate of S. aureus SSI decreased nonsignificantly, from 1.1% to 0.7% [18]. In a study involving cardiothoracic surgery, the SSI rate was significantly reduced, from 7.3% to 2.8% [13]. In both studies, a historical control group was used. It is well known that the use of historical control groups may lead to false conclusions. This may explain the discrepancy with our present data

The preliminary analysis of a prospective, randomized, placebo-controlled clinical trial in cardiothoracic, general, and neurological procedures shows that application of nasal mupirocin is associated with a significant decrease in the risk of nosocomial S. aureus infection [19]. Several aspects should be taken into consideration when interpreting the results of the present study. First, several observations indicate an effect of mupirocin. The rate of SSI caused by S. aureus was 2.7% in the placebo group and 1.6% in the mupirocin group, and the rate of endogenous S. aureus infection was 5 times lower in the mupirocin group. Also, the RR of nasal carriage for the development of SSI was 2.6 (95% CI, 0.9–7.7) in the placebo group and 1.2 (95% CI, 0.3–3.9) in the mupirocin group. These differences were, however, not statistically significant

Colonization with S. aureus was found to be an independent risk factor for developing an SSI due to S. aureus [10]. On the bases of these results, we expected eradication of nasal carriage with mupirocin to lower the infection rate and, especially, to affect the rate of deep infection. In the present study, we found superficial SSI rates of 3.8% in the intervention group and 4.3% in the placebo group, which is comparable with the previous data (4.0%) [10]. Deep SSIs, however, almost disappeared: only 1 deep SSI was found in the placebo group (0.3%), compared with 2.6% in the surveillance study (P <.05). This unexpectedly strong decrease made it impossible to measure a difference between groups with the current number of patients

It is well known that the pathogenesis of SSI—and thereby the prevention of SSI—depends on many different factors. It has been reported several times that SSI surveillance and feedback of the results lead to lower SSI rates [20–25]. If surgical personnel and nursing staff are informed about (high) SSI rates, they will improve infection-control measures as well as surgical technique. The relative contribution of the individual measures to the decrease of SSIs is unknown. This intervention study should be considered as an intensive means of surveillance with a strong effect on the deep SSI rate. No specific measures had been taken to prevent SSI, and the surgical team was the same during the entire period

In many hospitals, SSIs remain important complications in clean surgical procedures. Nasal carriage of S. aureus is now definitely considered to be a risk factor for the development of SSI. One study showed that nasal carriage also plays an important role in the development of S. aureus bacteremia [26]. The role of perioperative eradication of nasal carriage, however, remains unclear. Studies with historical control groups have found that mupirocin has a statistically significant effect [13, 18]. However, in general, the use of historical control groups is not accepted as a reliable method of research

The results of this study emphasize the pitfalls of this methodology. The significant decrease in the rate of deep SSI in the placebo group compared with the control subjects of a previous surveillance study would have led to the unjustified conclusion that mupirocin is effective. Therefore, a randomized, double-blind, placebo-controlled study was performed. In this trial, the intervention did not result in a statistically significant reduction in SSI rate. However, this does not necessary mean that perioperative eradication of nasal carriage is useless. The unexpected decrease in the SSI rate observed in the placebo group resulted in insufficient power of the study, and, therefore, conclusions regarding the efficacy of mupirocin cannot be drawn

Although this study did not answer its initial question, 2 important lessons can be learned. First, paying serious attention to SSI by performing active surveillance—in this case, through performing an intervention study—is a highly effective way to prevent SSI. Considering the near disappearance of deep SSI, additional measures, such as the use of mupirocin nasal ointment, may have no additional effect. Second, future studies should seriously consider the effect of the study itself on the SSI rate in their power calculations. This effect may even be stronger than the effect of the intervention studied

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Footnotes

  • Mupirocin nasal ointment and the ingredients for the placebo nasal ointment were provided by GlaxoSmithKline

  • Received August 21, 2001.
  • Revision received February 1, 2002.
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  1. Clin Infect Dis. (2002) 35 (4): 353-358. doi: 10.1086/341025
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