Prevalence of Staphylococcus aureus Colonization in Orthopaedic Surgeons and Their Patients: A Prospective Cohort Controlled Study

Schwarzkopf, Ran MD, MS; Takemoto, Richelle C. MD; Immerman, Igor MD; Slover, James D. MD, MS; Bosco, Joseph A. MD

Journal of Bone & Joint Surgery - American Volume:
doi: 10.2106/JBJS.I.00991
Scientific Articles
Abstract

Background: Methicillin-resistant Staphylococcus aureus and methicillin-sensitive Staphylococcus aureus surgical site infections are an increasing health problem in the United States. To date, no study, as far as we know, has evaluated the prevalence of Staphylococcus aureus colonization in orthopaedic surgeons. The purpose of our study was to assess the prevalence of methicillin-resistant Staphylococcus aureus and methicillin-sensitive Staphylococcus aureus colonization in orthopaedic surgery attending surgeons and residents at our institution compared with that in our high-risk patients.

Methods: We performed nasal swab cultures in seventy-four orthopaedic attending surgeons and sixty-one orthopaedic surgery residents at our institution, screening for methicillin-resistant Staphylococcus aureus and methicillin-sensitive Staphylococcus aureus. We compared these results with a prospective database of nasal cultures of patients undergoing joint replacement and spine surgery.

Results: A total of 135 physicians were screened. Of those physicians, 1.5% were positive for methicillin-resistant Staphylococcus aureus and 35.7% were positive for methicillin-sensitive Staphylococcus aureus. None of the sixty-one residents were positive for methicillin-resistant Staphylococcus aureus. However, 59% were positive for methicillin-sensitive Staphylococcus aureus. Of the seventy-four attending surgeons, 2.7% were positive for methicillin-resistant Staphylococcus aureus and 23.3%, for methicillin-sensitive Staphylococcus aureus. Previous studies at our institution have demonstrated a 2.17% prevalence of nasal carriage of methicillin-resistant Staphylococcus aureus and an 18% rate of methicillin-sensitive Staphylococcus aureus in high-risk patients. Thus, no difference was found between the prevalence of methicillin-resistant Staphylococcus aureus in residents or attending surgeons and that in the high-risk patients. However, the prevalence of methicillin-sensitive Staphylococcus aureus colonization in the surgeons (35.7%) was significantly higher than that in the high-risk patient group (18%) (p < 0.01).

Conclusions: At a major teaching hospital, a higher prevalence of methicillin-sensitive Staphylococcus aureus colonization was found among attending and resident orthopaedic surgeons compared with a high-risk patient group, but the prevalence of methicillin-resistant Staphylococcus aureus colonization was similar.

Author Information

1Department of Orthopaedic Surgery, NYU Hospital for Joint Diseases, 301 East 17th Street, Suite 1500, New York, NY 10003. E-mail address for R. Schwarzkopf: schwarzk@gmail.com

A commentary by Bassam A. Masri, MD, FRCSC, is available at www.jbjs.org/commentary and as supplemental material to the online version of this article.

Article Outline

According to the Centers for Disease Control and Prevention’s National Nosocomial Infections Surveillance System, which monitors the rate of hospital-acquired infections in the United States, surgical site infections represent the third most commonly reported type of nosocomial infection, accounting for 14% to 16% of all nosocomial infections1. Staphylococcus aureus is the most commonly encountered etiologic pathogen in surgical site infections2. Methicillin-resistant Staphylococcus aureus was first described, as far as we know, in 1961 and is believed to have emerged because of the increasing use of antibiotics in hospitals3. Currently, about 57% of nosocomial infections with Staphylococcus aureus are resistant to methicillin4. Methicillin-resistant Staphylococcus aureus surgical site infection is an increasing health problem in the United States5. The increase in costs for treatment is estimated to be between $2000 and $4500 per infected patient and as much as $35,000 to $90,000 for high-risk patients, i.e., those managed with arthroplasty and spine surgery. The postoperative stay in the hospital is lengthened by seven to ten days, on the average, and additional surgeries are often needed, resulting in substantial morbidity6-8. In addition, compared with patients with methicillin-sensitive Staphylococcus aureus infection, patients with methicillin-resistant Staphylococcus aureus bacteremia have shown an increased mortality9,10. Recently, evidence has demonstrated an increased risk of bacteremia with Staphylococcus aureus colonization and a decreased surgical site infection rate with decolonization11.

Few studies have looked at the prevalence of methicillin-resistant Staphylococcus aureus and methicillin-sensitive Staphylococcus aureus colonization in health-care workers, and we know of none that have examined the prevalence in orthopaedic surgeons. A recent study by Johnston et al.12 at Johns Hopkins Hospital in Baltimore, Maryland, found that the prevalence of methicillin-sensitive Staphylococcus aureus and methicillin-resistant Staphylococcus aureus-positive nasal carriage was 28% and 2%, respectively, in the health-care staff. This is comparable with the prevalences of methicillin-sensitive Staphylococcus aureus and methicillin-resistant Staphylococcus aureus infection of 32% and 0.8%, respectively, found in the noninstitutionalized U.S. population13. However, Vonberg et al. showed that approximately 3% of methicillin-resistant Staphylococcus aureus outbreaks were caused by asymptomatic colonized health-care workers, and the authors demonstrated that health-care workers are capable of transmitting methicillin-resistant Staphylococcus aureus to others14, making colonization a potential concern. The aims of this study were to determine the prevalence of nasal colonization of methicillin-resistant Staphylococcus aureus and methicillin-sensitive Staphylococcus aureus in our high-risk patients and in orthopaedic resident and attending surgeons and to identify risk factors that may contribute to a positive nasal carriage in the orthopaedic attending and resident surgeons at our institution.

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Materials and Methods

We conducted a prospective observational study of the physicians and patients in our institution.

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Patient Screening

Our hospital instituted a policy of screening for methicillin-resistant Staphylococcus aureus and methicillin-sensitive Staphylococcus aureus nasal colonization in high-risk patients undergoing total hip or total knee arthroplasty or major spine surgery, with decolonization prior to surgery. Over a period of one year, all patients undergoing one of these operations who were seen at preadmission testing had their anterior nasal nares cultured for methicillin-resistant Staphylococcus aureus and methicillin-sensitive Staphylococcus aureus colonization. Only initial screenings were included; patients who were seen multiple times during the study period were included in the dataset only once, on the basis of the results of the first screening. These results were used as the control group for comparison between physician and patient rates of nasal colonization.

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Physician Screening and Data Collection

All attending and resident surgeons in the Department of Orthopaedic Surgery at New York University Hospital for Joint Diseases were invited to take part in the study. We included only physicians who had current surgical privileges in the department. Nasal swab samples were collected from consenting physicians. At the time of sample collection, the physicians were asked to fill out a questionnaire that included information regarding yearly case volume, recent antibiotic use, number of hospitals where the surgeon performed surgery, and exposure to patients who were positive for methicillin-resistant Staphylococcus aureus surgical site infections.

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Specimen Processing

All physician and patient specimen swabs were coded and transported within six hours to the microbiology laboratory at New York University Langone Medical Center. Analysis consisted of bacterial culture with use of standardized methods in the same microbiology laboratory.

The cultures of the patients and the physicians were obtained over the same time period to avoid potential temporal variations in colonization rates.

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Statistical Analysis

The Fisher exact test was used to compare the rates of colonization between different groups of subjects. The Pearson chi-square test was used to compare the rates of patient colonization by months. Spearman correlation analysis was used to investigate the relationship between the number of yearly cases, the number of hospitals attended, and colonization. Categorical regression analysis was performed to control for possible confounders in determining the correlations between colonization and the number of hospitals, yearly cases, and seniority level of residents. A p value of <0.05 was considered to be significant.

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Source of Funding

There was no external funding source for this study.

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Results

Screening Results

A total of 2256 patients, seventy-four attending surgeons, and sixty-one resident surgeons were included in the study. All of the patients were screened for both methicillin-resistant Staphylococcus aureus and methicillin-sensitive Staphylococcus aureus. All residents, with the exception of one who was on an off-site rotation, and all teaching attending surgeons participated in this study. No resident or attending surgeon declined participation. All surgeons were screened for methicillin-resistant Staphylococcus aureus, whereas only seventy-three attending surgeons and thirty-nine residents were screened for methicillin-sensitive Staphylococcus aureus. While the rates of methicillin-resistant Staphylococcus aureus colonization were similar between the high-risk patients (2.17%) and surgeons (1.5%) (p > 0.05), the rate of methicillin-sensitive Staphylococcus aureus colonization was significantly higher among the surgeons (35.7%) than among the patients (18%) (p < 0.01), and this difference was primarily accounted for by a higher rate of methicillin-sensitive Staphylococcus aureus colonization among the residents (59%) (Table I). With the numbers studied, there were no significant differences in the proportion of patients who tested positive in each of the twelve months of the testing period (p = 0.657).

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History of Antibiotic Use in the Previous Month

Among the attending surgeons, there was a higher rate of methicillin-sensitive Staphylococcus aureus colonization associated with a recent history of antibiotic usage, although significance was not reached. Two of the three attending surgeons who reported antibiotic use in the previous month tested positive for methicillin-sensitive Staphylococcus aureus compared with 21.4% of those who had not reported any antibiotic use (p = 0.133). Among the residents who were screened for methicillin-sensitive Staphylococcus aureus, none reported recent use of antibiotics.

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Recollection of Treating a Methicillin-Resistant Staphylococcus aureus-Positive Surgical Site Infection

Attending surgeons were asked if they could recall having treated any methicillin-resistant Staphylococcus aureus-positive surgical site infections during the past year. Fourteen attending surgeons (18.9%) reported that they had treated a methicillin-resistant Staphylococcus aureus-positive patient in the previous month; twenty-one (28.4%), that they had treated such a patient in the previous three months; thirty (40.5%), that they had done so in the previous six months; and thirty-six (48.6%), that they had done so in the previous twelve months. However, none of these attending surgeons screened positive for methicillin-resistant Staphylococcus aureus. Moreover, the two attending surgeons who tested positive for methicillin-resistant Staphylococcus aureus carriage did not recall having treated methicillin-resistant Staphylococcus aureus-positive patients within the past year. No resident in our sample tested positive for methicillin-resistant Staphylococcus aureus, so this analysis was not performed for the residents.

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Number of Hospitals Where the Physician Performs Operative Procedures

The attending surgeons surveyed reported that they had treated patients in one to eight hospitals, with two hospitals being the most common response (37.8% of attending surgeons). The residents reported that they had worked in one to seven hospitals, with five being the most common response (47.5% of the residents). For the attending surgeons, we could not identify a significant correlation between the number of hospitals and colonization rates for methicillin-resistant Staphylococcus aureus (r = –0.092, p = 0.434) or methicillin-sensitive Staphylococcus aureus (r = –0.012, p = 0.919). For the residents, there was a significant negative correlation between the number of hospitals and methicillin-sensitive Staphylococcus aureus colonization (r = –0.391, p = 0.014). When the junior residents (≤200 cases) and senior residents (≥250 cases) were analyzed separately, no correlation was seen among the junior residents (r = 0.189, p = 0.411), whereas the negative correlation persisted among the senior residents (r = –0.595, p = 0.009).

Linear logistic regression analysis was performed to control for possible confounders. The number of hospitals appeared to be independently associated with methicillin-sensitive Staphylococcus aureus colonization rates, as residents who operated in fewer hospitals were more likely to be colonized with methicillin-sensitive Staphylococcus aureus (Table II).

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Discussion

The prevalence of Staphylococcus aureus in surgical site infections is an increasing problem in the United States, and colonization by providers may be one risk factor2,5. Our study indicates that nasal colonization with methicillin-resistant Staphylococcus aureus among attending and resident orthopaedic surgeons in one institution was similar to the prevalence found in that institution’s high-risk patients. In addition, the prevalences of colonization among surgeons were 1.5% for methicillin-resistant Staphylococcus aureus and 35.7% for methicillin-sensitive Staphylococcus aureus, which were similar to the prevalences of 2% and 28%, respectively, for health-care workers shown in a study by Johnston et al.12 at Johns Hopkins Hospital in Baltimore. The rates in both studies are comparable with the prevalences of colonization with methicillin-resistant Staphylococcus aureus and methicillin-sensitive Staphylococcus aureus of 0.8% and 32%, respectively, found in the noninstitutionalized U.S. population13.

The prevalence of methicillin-sensitive Staphylococcus aureus colonization among our physicians was higher than that among our high-risk patients, and the prevalence of methicillin-sensitive Staphylococcus aureus colonization among our orthopaedic residents was similar to the higher prevalence observed among institutionalized patients15. While the vast majority of our residents reside in geographic proximity to the population described, a markedly higher rate of colonization (59%) was observed, suggesting that residency, or the activities demanded of residents, may represent a risk factor for methicillin-sensitive Staphylococcus aureus colonization. Junior residents spend a substantial amount of time administering day-to-day care and performing daily dressing changes on orthopaedic inpatients. This may explain why junior residents exhibit the same prevalence of methicillin-sensitive Staphylococcus aureus colonization as institutionalized patients, and we recommend high vigilance for hand and equipment hygiene during daily patient and wound care.

Most individuals are intermittent carriers of Staphylococcus aureus, but only about 20% are persistent carriers16. Eradication of nasal colonization is easy and efficient in the short term with the help of topical agents such as mupirocin and antiseptic body washes. Long-term eradication is less successful. Because of this intermittent colonization pattern, routine long-term decolonization of health-care workers is not successful. Furthermore, prolonged use of mupirocin is associated with the development of mupirocin resistance17. On the basis of these findings, the Centers for Disease Control and Prevention (CDC) advises against routine methicillin-resistant Staphylococcus aureus surveillance of health-care workers, and both the Society for Healthcare Epidemiology of America and the CDC recommend decolonization of health-care workers only when they are implicated in outbreaks of methicillin-resistant Staphylococcus aureus infection. Hand hygiene is strongly recommended by the CDC and the Society for Healthcare Epidemiology of America for the prevention of methicillin-resistant Staphylococcus aureus transmission18.

At our institution, we currently have a protocol of universal decolonization of patients with mupirocin, regardless of colonization results, prior to total joint arthroplasty and spine surgery. We adopted this strategy because of the complexity of our medical environment and our desire to ensure that all patients are decolonized prior to these high-risk procedures and because of the growing evidence of decreased surgical site infection with decolonization of Staphylococcus aureus from patients’ nares11. Larger, well-designed studies are needed to determine whether routine decolonization has an impact on infection rates for orthopaedic procedures. Preoperative nasal cultures have been most useful in our center to help to guide the appropriate perioperative antibiotic choice.

Investigation performed at the Department of Orthopaedic Surgery, New York University Hospital for Joint Diseases, New York, NY

Disclosure: The authors did not receive any outside funding or grants in support of their research for or preparation of this work. Neither they nor a member of their immediate families received payments or other benefits or a commitment or agreement to provide such benefits from a commercial entity.

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