SURGICAL INFECTIONS Volume 16, Number 2, 2015 ª Mary Ann Liebert, Inc. DOI: 10.1089/sur.2014.022

Nasal Carriage of Staphylococcus aureus among Surgeons and Surgical Residents: A Nationwide Prevalence Study Jeroen L.A. van Vugt,1,* Robert J.S. Coelen,1,* Dirk W. van Dam,2 Bjorn Winkens,3 Joep P.M. Derikx,4 Edou R. Heddema,2 and Jan H.M.B. Stoot1

Abstract

Background: Staphylococcus aureus nasal carriage is an independent risk factor for developing nosocomial infections and for developing surgical site infection (SSI) in particular. The number of post-operative nosocomial S. aureus infections can be reduced by screening patients and decolonizing nasal carriers. In addition to patients, health care workers may also be S. aureus nasal carriers. The aim of this study was to explore S. aureus nasal carriage rates among surgeons. Methods: Nasal swabs were collected from surgeons and surgical residents during a national surgical congress. The control group consisted of non-hospitalized patients. Staphylococcus aureus carriage was detected using selective chromogenic agars by use of a fully automated inoculator. Suspected colonies were identified further by positive catalase and slide coagulation reactions. Results: Samples were collected from 366 surgeons and surgical residents and 950 control patients. The S. aureus nasal carriage rate among surgeons and residents was significantly greater compared with the control group (45.4% versus 30.8%, odds ratio [OR] 1.86 [1.45–2.38], p < 0.001). No significant difference in carriage rate was found between surgeons and residents (46.8% versus 43.3%, p = 0.769) and years of experience as a surgeon was not associated with a greater carriage rate. Male gender was an independent risk factor for carriage among physicians odds ratio ([OR] 1.90 [95% confidence interval 1.19–3.01], p = 0.007). Conclusions: The nationwide rate of S. aureus nasal carriage among surgeons and surgical residents proved to be significantly greater compared with a non-hospitalized patient control group. Male gender is an independent risk factor for carriage among physicians. Future studies are needed to investigate the possible relation with nosocomial post-operative S. aureus infections.

S

urgical site infection (SSI) is a frequently occurring nosocomial infection in surgical patients with Staphylococcus aureus as the most common pathogen [1]. Surgical site infection is defined as infection of the surgical site within 30 d after surgery [1]. Up to 20% of surgical patients acquire at least one health care related infection in the post-operative period and 2% to 5% of patients undergoing surgery develop an SSI [2–4]. Surgical site infections double the length of hospital stay and are related to greater comorbidity and mortality rates [2].

Furthermore, SSIs comprise 42% of all extra costs due to nosocomial infections; the increased costs in the United States are estimated as $5 to $10 billion annually [2]. The nose is the most frequent ecological niche for S. aureus in human beings [3]. Nasal carriage of S. aureus in the general population is approximately 30% and is an independent risk factor for developing nosocomial infections in both surgical and nonsurgical patients and for developing SSI in particular in surgical patients [3,5–11]. Screening patients and decolonizing nasal

1 Department of Surgery, 2Department of Medical Microbiology and Infection Control, Orbis Medical Center, Sittard-Geleen, The Netherlands. 3 Department of Methodology and Statistics, Maastricht University, Maastricht, The Netherlands. 4 Department of Surgery, Maastricht University Medical Center, Maastricht, The Netherlands. *Both of these authors have contributed equally to this work. Presented at the Annual Dutch Surgical Society meeting 2013, Veldhoven, The Netherlands and the International Surgical Week 2013, Helsinki, Finland.

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S. AUREUS NASAL CARRIAGE AMONG SURGEONS

carriers on admission reduces the number of nosocomial S. aureus infections and SSI in particular [2,12–15]. One could speculate whether either patients or physicians are the main source of S. aureus in hospitals, how carriage in both groups is influenced by each other, and finally, whether a greater carriage rate among surgeons and surgical residents is associated with developing S. aureus-related infections in patients. After all, S. aureus-related death is four times more likely in non-carrying patients compared with carrying patients who develop an S. aureus infection [16]. Previously conducted prevalence studies showed high S. aureus nasal carriage rates among health care workers [17–21]. Just one study among physicians only and none among general surgeons have been conducted so far [22]. Therefore, a nationwide observational study was designed to explore the prevalence of S. aureus nasal carriage among general surgeons and surgical residents and the influence of gender and surgical experience. Participants and Methods Sample collection in physicians

Participants of a Dutch surgical congress (May 11–12, 2012) were asked to participate in the study. Only surgeons and surgical residents working in The Netherlands were included. At the congress center entrance, congress participants were randomly invited to take part in the study by three researchers. Participants were only included once. Participation in the study was anonymous. By use of a questionnaire, data regarding being either surgeon or surgical resident, the number of years of surgical practice (as a surgeon), and gender were recorded. A nasal swab (Transwab, MWE, Wiltshire, England) was taken by the participant him- or herself using one nasal swab for both anterior nares. Ethical approval was obtained from the Medical Ethics Committee. Sample collection in control group

For the control group, representing a non-hospitalized population, we included all unique and consecutive S. aureus screened patients undergoing elective knee or hip surgery in the outpatient clinic of our center from June 16, 2012 until June 16, 2013. Screening was performed routinely in this patient group in our center. Only the initial sample was included if patients were seen more than once during the study period. Sample collection was performed in the exact same way as in the physicians group at the congress.

179 Statistical analysis

A sample size calculation was performed using Open Epi (Version 2.3.1, www.openepi.com/Menu/OpenEpiMenu.htm). Given the prevalence of S. aureus nasal carriage of approximately 30% in the general population in the literature [3–5,10– 12,23–25], and a hypothesized prevalence of at least 40% in physicians [22], a minimum of 356 participants per group was required to detect a significant difference in prevalence with 80% power at 5% a (two-sided). Data were presented by absolute numbers and percentages. Differences between groups were analyzed with the Pearson w2 test for dichotomous parameters. The effect of group (physician versus control) or surgical practice experience (surgeon versus surgical residents, or categorical: 0 for residents and 1–5 for surgeons with < 5, 5–10, 10–15, 15–20, > 20 y of surgical practice) on S. aureus nasal carriage was assessed using logistic regression analysis, where gender was included as covariate and tested for effect-modification. Odds ratio (OR) and 95% confidence interval (95% CI) were presented. Two-tailed p values < 0.05 were considered significant. All statistical analyses were performed using the Statistical Package for the Social Science (version 19, SPSS Inc., IBM, Armonk, NY). Results Sampling

A total of 366 physicians and 950 consecutive controls were included (Table 1). Within the physicians group, there were significantly more males (n = 256, 69.9%) than within the control group (n = 350, 36.8%, p < 0.001). The physicians group consisted of 150 (41.0%) residents and 216 (59.0%) surgeons. There were significantly more male surgeons (n = 256, 69.9%) than female surgeons (n = 110, 30.1%, p < 0.001). Physicians versus control group

An overview of the results is provided in Table 2. The prevalence of S. aureus nasal carriage among physicians was significantly greater compared with the control group (45.4% versus 30.8%, OR 1.86, 95% CI 1.45–2.38, p < 0.001). Although gender was not a significant effect modifier

Table 1. Characteristics of the Three Hundred Sixty-Six Physicians and Nine Hundred Fifty Control Patients

Sample processing

Nasal swabs collected at the congress were all marked with a unique code and stored at room temperature. Within 24 h the nasal swabs were transported and processed by the Laboratory of Medical Microbiology of Orbis Medical Center. Swabs were inoculated overnight in a selective aztreonam enrichment broth at 35C. The broths were streaked onto selective chromogenic agar (S. aureus ID, bioMe´rieux, Marcy-l’E´toile, France) by use of a fully automated inoculator (Previ Isola, bioMe´rieux, Marcy-l’E´toile, France). Suspected green colonies were identified further by a positive catalase and slide coagulation reaction (Slidex Staph-kit, bioMe´rieux). Antimicrobial susceptibility testing was not performed on any of the isolates. Sample processing was performed in the exact same way for both groups.

Characteristic Gender Male Female Residents Surgeons Experience (years)