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Ann Thorac Surg 2001;71:1572-1579
© 2001 The Society of Thoracic Surgeons
a Department of Cardiac Surgery, Wilkes-Barre General Hospital, Wilkes-Barre, Pennsylvania, USA
Address reprint requests to Dr Cimochowski, 35 West Linden St, Suite 340, Wilkes-Barre, PA 18702
Presented at the Thirty-Sixth Annual Meeting of The Society of Thoracic Surgeons, Fort Lauderdale, FL, Jan 31–Feb 2, 2000.
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Abstract |
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Methods. We prospectively followed 992 consecutive open heart surgery (OHS) patients who did not receive MPN prophylaxis (group I) from January 1, 1995 to October 31, 1996. Group II consisted of 854 consecutive patients followed prospectively from December 1, 1997 to March 31, 1999 treated with intranasal MPN given on the evening before, the morning of OHS, and twice daily for 5 days postoperatively.
Results. There was a significant difference in the rate of overall sternal wound infections between the untreated (group I) and the treated group (group II): 2.7% (27 of 992) versus 0.9% (8 of 854) (p = 0.005). The difference was also significant in the diabetic subgroup: 5.1% (14 of 277) (group I) versus 1.9% (5 of 266) (group II) (p = 0.04) and the nondiabetic group: 1.8% (13 of 715) (group I) versus 0.5% (3 of 588) (group II) (p = 0.03). The cost of MPN treatment was $12.47 per patient compared with $81,018 ± $41,567 for a deep wound infection with no antibiotic-related complications recorded.
Conclusions. Prophylactic intranasal MPN is safe, inexpensive, and very effective in reducing the overall sternal wound infections by 66.6%.
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Introduction |
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TopAbstractIntroductionMaterial and methodsResultsCommentDiscussionReferences |
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Material and methods |
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TopAbstractIntroductionMaterial and methodsResultsCommentDiscussionReferences |
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Group I, the control group, was comprised of 992 consecutive patients who received no specific prophylaxis other than pre- and postoperative intravenous antibiotics. Group II, the intervention group, consisted of 854 patients who received intranasal Mupirocin prophylaxis both preoperatively and postoperatively in addition to the routine intravenous antibiotics. There were 136 patients who underwent open heart surgery during the intervention period who were excluded from the study. They were excluded for the following reasons: (1) Mupirocin was not given, or (2) emergency surgery precluded following the protocol, thus leaving 854 patients in the intervention group II.
Surgical and perioperative procedures
Before surgery, all patients received a Chlorhexidine shower either the evening before or the morning of surgery. Hair removal was performed in the pre-op room at the surgical suite approximately 1 hour before the procedure using a safety razor. All patients were prepped with an alcoholic/betadine solution and finally were covered with a betadine-impregnated steridrape. Antibiotics were started 1 hour before induction and continued for 48 hours in the postoperative period using Cefuroxime 1.5 g, intravenously, every 12 hours. In case of allergy to the forementioned drug, the patient was given Clindamycin 60 mg intravenously preoperatively and 600 mg every 6 hours for 48 hours postoperatively. All incisions were painted with betadine starting 8 hours after surgery and continuing each shift until discharge.
Surgical methods
All patients underwent cardiopulmonary bypass using a membrane oxygenator. The surgery itself was performed by six different surgeons; however, the surgical technique was standardized throughout the study. Patients were not cooled but were allowed to drift to 35°C. Systemic cooling was performed only in those patients who underwent an arch aneurysm repair, as these patients underwent selective antegrade cerebral perfusion at 22 to 26°C with associated circulatory arrest. This was a relatively small group of 26 patients in whom no superficial or deep wound infection occurred.
All wounds were closed with a subcuticular technique. The chest tubes were routinely removed 36 hours postoperatively. Fastidious care was taken not to cauterize any part of the sternal bone edges and no bone wax was ever used. The cardiothoracic surgeons were responsible for the opening and closure of the chest in the vast majority of patients. In a small number of cases, the sternum was closed by the physician assistant. The above-noted techniques were consistent throughout the entire period for both the control and intervention groups.
Intervention
In the treated group, Mupirocin calcium ointment (Bactroban Nasal; SmithKline and Beecham Pharmaceuticals, Philadelphia, PA) was applied via a Q-tip swab to each nostril per the manufacturer’s instructions. The first dose was applied the night before surgery, and the second preoperative dose was given the morning of surgery 1 hour before entering the operating room suite. Treatment was continued twice a day for 5 consecutive days postoperatively. If the patient was an elective admission on the day of surgery, they were instructed on the application of the Mupirocin ointment at home and were counseled regarding its administration. Signs and symptoms of allergic reactions were be noted by the nursing staff as well as the patient.
Nasal cultures were taken on 472 patients in the control group to determine the predominant organisms and more specifically the presence of S aureus in the nares. Nasal cultures, including Mupirocin sensitivity, were also done poststudy in a smaller sample (100 patients) 22 months after the study commenced and 6 months after it was concluded to evaluate Mupirocin resistance. All S aureus-positive patients in this group were then recultured at 2 to 3 months to determine the incidence of recolonization of S aureus in the nose. SmithKline Beecham provided no funding for this study.
Surveillance method
The identification and confirmation of a sternal wound infection was done by the infection control staff, the cardiac surgeons, or an infectious disease consultant. Besides the daily rounds of the cardiac surgeons, surveillance was done by the nurse epidemiologists. This included rounds on the patient floors at least three times per week, chart review, discussions with nursing staff and physicians, review and correlation of culture results, and direct wound observations. Determination of a superficial or deep wound infection was made in conjunction with the cardiac surgeons and/or the infectious disease specialists using modified criteria from The Center for Disease Control and Prevention (see Appendix). The date of onset of the infection was recorded as well as the specific organisms obtained from the microbiology laboratory. All data were prospectively analyzed. The data for the nasal cultures were taken from reports generated by the microbiology laboratory, as was the sensitivity to Mupirocin testing that was done in the subcategory of patients in the poststudy group.
The calculation of cost of a deep sternal wound infection and a superficial wound infection was done in conjunction with the finance department at the Hospital using criteria that stated that 62% of the Medicare charge was a reasonable figure for the cost of the hospitalization [10].
The postoperative length of hospital stay was derived directly from the hospital record. The cost of Mupirocin Calcium was provided by the pharmacy department.
Statistical analysis
The results were analyzed using BMDP (Bio Medical Package) Software (Statistical Solutions, Saugus, MA). Categorical variables were analyzed using 
2 tests. Nonparameter Wilcoxon rank-sum tests (equivalent to Mann-Whitney tests) were used for the length-of-stay data.
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Comment |
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Eradication of S aureus in the nose is not a new concept [9, 14]. It has been attempted both by topical and systemic antibiotics as well as topical antiseptics for several decades but with unpredictable and inconsistent results. With the introduction of Mupirocin Calcium in the late 1980s, a topical antibiotic was at hand that was highly effective in eradicating nasal S aureus [15]. Because of a special composition using paraffin, the drug was also nonirritable to the tissues of the nose. Mupirocin is produced by a fermentation of Pseudomonas bacteria, resulting in a naturally occurring antibiotic that is very active against Staphylococcus, including methicillin-resistant strains and streptococcus. According to the review by Hudson and associates in 1993, the antibiotic Mupirocin is structurally unrelated to any other clinically used antibiotic and, in addition, can only be used topically [15]. The emergence of Vancomycin-resistant S aureus, which was recently reported by Smith and associates in the New England Journal of Medicine, highlights the problem of systemic antibiotics in eradicating S aureus because of the eventual tendency to develop resistance [16]. Intranasal Mupirocin Calcium has been reported to be extremely effective in the short-term eradication of S aureus in the nasal reservoir with eradication persisting up to 1 year. The short-term effectiveness has been reported anywhere from 91% to 100% [17]. Subsequently, there is a regrowth of S aureus in the patients’ nasal reservoir. However, the time frame reported in the literature is variable, up to 22 weeks in 56% of the patients after a simple short-term course of treatment [11]. Furthermore, its benefit is not only the reduction of nasal S aureus reservoirs but also in eliminating positive hand cultures, which has been reported by Reagan and associates [11]. They also noted in their study that 97% of Staphylococcus hand cultures exactly matched the patients’ current nasal phage type [11]. One possibility of the etiology of wound infection points to the patient’s own nasal reservoir with subsequent spread to the hands or skin and thus to the wound [14]. No one knows the exact means by which nares S aureus is transmitted to wounds, but it is postulated that one or more of the following explanations are applicable. (1) The trauma from the endotracheal tube spreads S aureus from the nose hematogenously to the wound. (2) S aureus from the nose is transmitted into the operating air and thus the wound. (3) The S aureus from the nose is transmitted to the patient’s own skin and is not eradicated completely by the preoperative techniques used to sterilize the operative site [18].
With the exception of smoking and good perioperative glucose control, as noted by others, most of the risk factors for sternal wound infection in cardiac surgery cannot be significantly altered preoperatively, intraoperatively or postoperatively [19]. On the other hand, prophylaxis with intranasal antibiotic could be done in all patients except in the most dire of circumstances, and even those who are taken emergently to the operating room could get a preoperative dose in the operating room and the subsequent postoperative 5-day dosage.
Our results, as noted in Table 2, show that the sternal wound infection rate in the Mupirocin Calcium-treated group was significantly reduced 66.6% as compared with the control group (2.7% vs 0.9%) (p = 0.005). In addition, the subgroups of superficial and deep wound infection and diabetes, likewise, had across-the-board reduction in their wound infection rates in the Mupirocin-treated group as compared with the control group. The group of patients who were eliminated from the intervention group because of failure to receive Mupirocin had a similar wound infection rate of 2.9% as compared with the control group of 2.7%, which clearly indicates that there was no bias in eliminating this particular group of patients from the intervention group. The population characteristics were nearly identical in both groups with reference to gender, use of internal mammary artery, previous open heart surgery, obesity, diabetes, and saphenous vein graft, with the solitary exception being that the treated group was a significantly older group of 66.6 years versus 64.7 (p = 0.006). This would favor a higher sternal wound infection rate in the treated group, which did not occur. As noted in Table 5, there was a statistically significant reduction in the sternal wound infection length of stay cases from 31.7 days to 12.7 days (p = 0.004) in the control versus intervention group, as well as the deep and superficial sternal wounds in the two groups. While mortality was reduced from 11.1% in the control group to 0% in the treated group, this did not achieve statistical significance (p = 0.32), and selection bias may play a role due to the nonrandomization of the groups.
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Review of the literature reveals only one other paper related to the specific use of intranasal Mupirocin prophylactically to reduce surgical wound infections in cardiac surgery. This was published by Kluytmans and associates in 1996, in whose report 928 patients were compared with an intervention group of 752 patients. The surgical site infection was significantly reduced from 7.3% to 2.8% [13]. They likewise reported no resistance to Mupirocin during the study. They did not, however, determine whether the reduction was due to deep sternal infections, superficial wound infections, diabetics, or nondiabetics. Nevertheless, their reduction of surgical site infection from 7.3% to 2.8% (61.1%) was remarkably close to our 66% reduction.
Our final discussion point is the potential abuse of this antibiotic. In light of antibiotics abuse since their introduction to medicine in the 1940s, cardiac surgeons should be concerned about resistance of S aureus infection to antibiotics in general as well as potential abuse of Mupirocin. As reported in the New England Journal of Medicine last year, there are now two documented cases of Vancomycin resistance to S aureus in the United States, and one can only project the number will increase [16]. The incidence of Mupirocin resistance has essentially been reported when there has been abuse based on the length of treatment, the type of wound it has been used for, and in the type of patient that it has been used on [21–23]. An editorial by John Boyce in 1996 stated that the development of Mupirocin resistance to S aureus has not been observed by using a single 5-day course, but he does go on to state that the widespread use of Mupirocin for the purpose of controlling methicillin-resistant S aureus (MRSA) has been associated with Mupirocin resistance to S aureus in the United Kingdom [24]. Furthermore, he states the "usage patterns that appear to have promoted the emergence of Mupirocin resistance include frequent or continuous application for periods of weeks or months, especially when applied to large wounds or areas of dermatitis, and widespread use within an institution" [24]. A letter to the editor in the New Zealand Medical Journal clearly points out the risk of having an over-the-counter drug of this nature [23]. This was approved for over-the-counter use in New Zealand in the early 1990s, and the incidence of Mupirocin resistance has steadily increased over the 5-year period from 3.7% to 16%. Mupirocin alone will not eradicate MRSA infections, although it has been used as a serious adjunct in the treatment of MRSA epidemics [25]. We further emphasize the point that it is important to advocate associated technical factors such as not cauterizing the sternum or using bone wax as part of the armenterium of the cardiac surgeon in preventing sternal wound infections. Finally, in our study, we did not show any significant Mupirocin resistance. It was still 96.2% effective after 2.5 years of continual usage on our service. But we are the only service who uses it at the present time on a regular basis, we only use it intranasally, and we avoid repeated applications.
Limitation of study
This paper suffers from lack of randomizing and blinding, but this is countered by the inclusion of large population groups in each study arm, all of whom were entered prospectively over a relatively short period of time. In addition, while there were multiple surgeons in the study, which could lead to surgical technical bias, the philosophy of the group was to perform all procedures in a standardized fashion over the period and this was adhered to. A selection bias cannot be ruled out conclusively due to lack of randomization, but because this is only the second paper in the literature concerning the use of Mupirocin in cardiac surgery patients, a study of this type certainly was warranted at the time while future studies could be randomized prospectively.
Conclusions
This study comprises 1,846 patients over a 3-year period who were enrolled in two consecutive prospective groups involving the use and nonuse of intranasal Mupirocin.
The use of intranasal Mupirocin was extremely effective, easy to apply, had no complications, and reduced sternal wound infections in both diabetics and nondiabetic patients. The cost of this treatment was minimal but we strongly adhere to guidelines to avoid resistance to Mupirocin.
A randomized controlled study would be the ultimate verification of this modality and would appear to be warranted.
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Appendix |
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Deep surgical site infection
Infection occurs within 30 days after the operation if no implant is left in place or within 1 year if implant is in place and the infection appears to be related to the operation and infection involves any part of the anatomy (eg, organs or spaces), other than the incision, which was opened or manipulated during an operation and at least one of the following: 1. Purulent drainage from a drain that is placed through a stab wound into the organ/space. 2. Organisms isolated from an aseptically obtained culture of fluid or tissue in the organ/space. 3. An abscess or other evidence of infection involving the organ/space that is found on direct examination, during reoperation, or by histopathologic or radiologic examination. 4. Diagnosis of an organ/space SSI by a surgeon or infectious disease specialist.
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Discussion |
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Doctor Cimochowski and his colleagues have presented a nonrandomized, historically controlled study on the effect of nasal Mupirocin on the endpoint outcome of sternal wound infection. Through univariate analysis alone they have shown a decrease in their rate of sternal wound infection. This decrease is claimed to be solely the result of the Mupirocin treatment in the study group. I am afraid the authors have not conclusively proven their hypothesis.
Special situations demand special actions. The authors’ overall combined sternal infection rate in the control group of 2.7% is two times the 1998 published STS combined average of 1.3%. Both the deep and superficial infection rates are also two times higher than the published norms, while their diabetic cohort is three times higher. Whether or not the use of Mupirocin will reduce sternal infection rates below what the rest of us consider "normal" has yet to be proven. Dr Cimochowski, could you tell us why you believe the rate of infection in your control group was so high and speculate as to why length of stay was shorter in the infected patients in the study group.
Twenty percent of the control group was found on preoperative culture to have S aureus colonization of the nares. What were the relative rates of sternal infection in the colonized control patients versus the noncolonized control patients? Did colonization predict subsequent infection? Stated differently, was there a correlation between preoperative nasal colonization and postoperative sternal infection in your control group? Were the surgeons, nurses, PAs, scrub personnel, anesthesiologists cultured, and if found positive, similarly treated? Were any of these personnel involved during the control period and not during the study period?
It is very important to note for the audience that 146 patients were excluded from the study group, and I quote the paper, "because they failed to have the protocol followed in an exact manner." These excluded study patients had an overall infection rate of 2.9%. So, if we redo this analysis and base it on intent to treat, the results become much less spectacular. The univariate analyses presented on deep, superficial, diabetic, and nondiabetic infections are all just barely significant, and one more infection in any of those groups would have put that particular 2 analysis on the other side of the statistical tracks. In fact, there are actually four infections in the 136 treated but excluded patients. Were these deep or superficial? Were they diabetic or nondiabetic?
Only by combining the rates of deep sternal and superficial infection are the authors able to show a significant univariate effect of Mupirocin based on intent to treat. Does this mean that Mupirocin alone affected this change? In the absence of either a concomitantly randomized study or at least a multivariable analysis of the entire historical cohort with Mupirocin as one of the variables, we just cannot tell from the data presented. Dr Cimochowski, could you tell us, if this is a truly prospective study, why it was not randomized from the start?
A univariate analysis in a historically controlled study does not prove that Mupirocin alone prevents wound infections. Could you tell us if a multivariate analysis of sternal wound infection was done? And if so, did it implicate Mupirocin as protective against infection?
To claim a 66% reduction in infection rates due independently to Mupirocin requires a relative risk of 0.34 by multivariate analysis for that variable. In the absence of such an analysis, no such claim can be made. What were the relative incidences in both groups of the other previously published independent risk factors for infection, namely, bilateral IMA use, COPD, renal failure, body mass index (which is a more objective measure of obesity), chronic steroid use, bypass time, transfusions, and especially glucose levels.
Hyperglycemia, which is the true risk factor for infection in diabetics, is a strong independent predictor of wound infections, and continuous insulin drips in diabetics have been shown to significantly reduce wound infection by multivariable analyses. Was there a change in the management of hyperglycemia during the course of this study? Specifically, were insulin drips employed in the latter part of this study when the study group was being treated? What were the average perioperative glucose levels in the diabetic patients in both arms?
The absence of meaningful statistical analysis may be the Achilles heel of this very thoughtful study.
Having said all that, and now that sternal infection rates at this institution have been normalized, this would be a wonderful study to continue in a double-blinded, randomized fashion with nasal Vaseline as the control arm. And at a cost of only $12 per patient, the results would be most intriguing.
I would like to thank the Society for the privilege of discussing this paper.
DR CIMOCHOWSKI: Thank you, Dr Furnary, for your comments. I will need to present another paper to answer all your questions in the allotted time.
First of all, 2.7% is a combined superficial and deep wound infection rate, which I certainly do not consider to be excessive. The actual deep sternal wound infection rate when we started was 1.2% and decreased to 0.4%. If you look in the literature (and it is very hard to ascertain who is telling the truth and who is not), what I like to do is look at the papers that have been published by infectious disease departments about cardiac surgery patients and deep wound infection, and it has usually been reported to be between 2% to 3%. In March 2000, the Center for Disease Control (CDC) is sponsoring the Fourth Decentennial International Conference on nosocomial and health care infections in Atlanta, Georgia. Two of the abstracts concerning cardiac surgery patients from the University of Pittsburgh and Mercy Health Care System in Pittsburgh reported deep sternal wound infection rates of 4.6% and 4.3%, respectively. This is contemporary data, which will be presented in March 2000.
As Kluytmans’ data showed here, he did a similar study in cardiac surgery patients, and their combined superficial and deep wound infection was 7.8%, which was reduced to 2.8%.
Now, we did not randomize this study. It was prospective and it was consecutive, except for the patients that were eliminated, as we stated, in the treatment group. And they were eliminated mainly because if a patient comes from the cath lab to the OR, we still give them the Mupirocin, but most often they did not receive the nocturnal dose that should be given the day before. It defies logic to say that a group that did not receive the treatment should be considered a treatment group. When we looked at the wound infection rate in that group, it was 2.9%, but that is equivalent to the control group, and the control group was 2.7%. So I would beg to differ a little bit with you on that issue. It is customary in most scientific centers to first do small nonrandomized, noncomparison groups to study a new technique, followed by retrospective and prospective and nonrandomized comparison groups of larger studies, and then finally do a randomized study. Because this is only the second study in the literature applicable to cardiac surgery, it is well within the standard of care to perform this type of study, which was a large prospective consecutive series comparing two groups to confirm the only other study to determine if it is worth while in doing a randomized study.
We did not culture the Staphylococcal nares of the hospital personnel because this was not appropriate. Not only would it potentially leave the hospital personnel at risk for legal reasons, but the purpose of the study, as clearly stated, was to compare cardiac surgery patients who did and did not receive Mupirocin. I believe your question on that issue is mostly irrelevant. However, the reported incidence in the literature for medical personnel and in health care workers has been around a 40% carrier state.
I am well aware of the paper that came out of your group in comparing the effect of insulin drips and target glucose control of diabetic wound infections. First of all, this paper covered not just diabetics, but all consecutive open heart surgery patients. So that giving insulin drips to only diabetics and not to the rest of the patients would result in significant nonuniformity in both groups. In addition, we use glucose insulin potassium very liberally for inotropic support over the past few years. And we give intravenous insulin drips in that setting so many of these patients did have insulin drips but were given it to more in line with their glucose insulin potassium inotropic milieu than in trying to control the reduction of wound infection in diabetics. As noted in the paper, diabetic wound infections were remarkedly decreased from 5.1% to 1.9% with the use of intranasal Mupirocin.
I would like to say one last thing else if I could. In addition to the overwhelming number of questions that you have posed, many of them have referred to the fact that we did not do a multivariate analysis. I would like to point out that this study was not organized to analyze all the various risk factors in cardiac surgery for sternal wound infections, but to compare the infection rate in two groups: no nasal Mupirocin versus nasal Mupirocin, a comparative analysis that was clearly stated in the beginning of the paper and in the beginning of our study. It is totally appropriate to use a univariate analysis to compare the two groups, which is exactly what we did. Our goal of the paper was not to compare every single risk factor using a multivariate analysis. Finally, if you will be a little patient, just recently we were informed by the company (Smith-Kline Beecham) that there is a randomized prospective study that has been completed, has been verbally presented, but has not been published. However, the reduction of sternal wound infection rate was almost exactly the same as ours of approximately 60 some percent. This is to be published in the near future, which substantially confirms the results of our study. Thank you very much.
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