Nasal Carriage of Staphylococcus aureus among Surgeons and Surgical Residents: A Nationwide Prevalence Study

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.

Surgical 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 non-surgical patients and for developing SSI in particular in surgical patients [3,5 –11]. Screening patients and decolonizing nasal 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.

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 35°C. The broths were streaked onto selective chromogenic agar (S. aureus ID, bioMérieux, Marcy-l'Étoile, France) by use of a fully automated inoculator (Previ Isola, bioMérieux, Marcy-l'Étoile, France). Suspected green colonies were identified further by a positive catalase and slide coagulation reaction (Slidex^® Staph-kit, bioMérieux). Antimicrobial susceptibility testing was not performed on any of the isolates. Sample processing was performed in the exact same way for both groups.

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% α (two-sided).

Data were presented by absolute numbers and percentages. Differences between groups were analyzed with the Pearson χ² 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).

Table 1.

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

Characteristic	Physicians n=366 value (%)	Controls n=950 value (%)	p
Gender
Male	256 (69.9)	350 (36.8)	<0.001
Female	110 (30.1)	600 (63.2)
Residents	150 (41.0)	—
Surgeons	216 (59.0)	—
Experience (years)		—
<5	60 (27.8)	—
5–10	48 (22.2)	—
10–15	43 (19.9)	—
15–20	21 (9.7)	—
≥20	44 (20.4)	—

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 (p=0.187), the difference in proportion of carriage between physicians and control patients was significant for males (OR 1.89, 95% CI 1.36–2.63, p<0.001), whereas it was not significant for females (OR 1.31, 95% CI 0.85–2.02, p=0.215). In the control group a non-significant difference in carriage was found in males compared with females (p=0.058).

Table 2.

Logistic Regression Analysis of Staphylococcus aureus Nasal Carriage in Control Group and Physicians

	Control group n=950 (%)	Physicians n=366 (%)	OR [95% CI]	p
SA carrier	293 (30.8)	166 (45.4)	1.86 [1.45–2.38]	<0.001
Males	121 (34.6)^a	128 (50.0)	1.89 [1.36–2.63]	<0.001
Females	172 (28.7)	38 (34.5)	1.31 [0.85–2.02]	0.215

Gender was not a significant effect modifier (p=0.187).

A non-significant difference compared with female controls (p=0.058).

OR=odds ratio; CI=confidence interval; SA=Staphylococcus aureus.

The influence of gender and surgical practice experience in physicians

Logistic regression analysis for risk factors of S. aureus carriage in physicians showed that male gender was an independent risk factor for S. aureus nasal carriage among physicians (OR 1.90, 95% CI 1.19–3·01, p=0.007), whereas carriage was not significantly different between surgeons and residents (OR 1.15, 95% CI 0.76–1.75, p=0.517; Table 3). Similar results were observed if years of experience was used instead of surgeons versus residents, i.e., years of surgical practice experience was not significantly related to S. aureus nasal carriage.

Table 3.

Logistic Regression Analysis for Risk Factors of Staphylococcus aureus Nasal Carriage in Physicians

		Univariate analysis
	SA carriage rate (%)	OR [95% CI]	p
Gender
Female	34.5	1 (reference)
Male	50.0	1.90 [1.19–3.01]	0.007
Experience (years)
Resident	43.3	1 (reference)
Surgeon	46.8	1.15 [0.76–1.75]	0.517
<5	51.7	1.40 [0.77–2.55]	0.274
5–10	56.2	1.68 [0.87–3.24]	0.129
10–15	41.9	0.94 [0.47–1.87]	0.863
15–20	42.9	0.98 [0.39–2.47]	0.967
≥20	36.4	0.75 [0.37–1.50]	0.411

SA=Staphylococcus aureus; OR=odds ratio; CI=confidence interval.

Discussion

In this nationwide study, a significantly greater nasal carriage rate of S. aureus among surgeons and surgical residents compared with an outpatient population was found (45.4% versus 30.8%) with male gender as an independent risk factor for physicians. This carriage rate is relatively high compared with previous studies. In the one study performed among physicians only (orthopedic surgeons) by Schwarzkopf et al. [22], the nasal carriage rate was approximately 35%. Furthermore, two similar studies evaluating S. aureus nasal carriage in physicians at two national microbiology and infectious disease congresses found carriage rates of 31.4% and 34.2% [19,26]. However, the current study can hardly be compared herewith, as surgeons and microbiologists or infectious disease specialists are greatly different groups. Moreover, health care workers with direct patient contact seem to be at increased risk for nasal carriage of S. aureus compared with health care workers without direct patient contacts [17,19,27]. The discrepancy with the current literature could also be attributed to differences in sample processing and culture techniques. In the current study, samples were inoculated overnight in a selective aztreonam enrichment broth before applying onto a selective chromogenic agar. Overnight enrichment of culture swabs results in a 9% to 25% increased sensitivity of detection [28,29]. Boisseau et al. [26] used polymerase chain reaction (PCR), whereas the study by Schwarzkopf et al. [22] did not report the performed sample processing method and culture technique used. In contrast to the latter study, no significant difference between surgeons and surgical residents was found [22]. Furthermore, surgical practice experience was not found to be a risk factor for S. aureus nasal carriage. This is in line with a study among health care workers in which no differences in years of health care service were found [30]. Different carriage rates in males and females have not been shown in all previous studies [19,21,30]. The relatively small female cohort may explain the difference found in the current study. Moreover, reproductive hormones are believed to influence the interaction between pathogen and host [31].

The estimated prevalence of S. aureus nasal carriage in the general population is reported to be approximately 30% [3 –5,10 –12,23 –25]. Approximately 20% of the general population is colonized permanently, 60% colonized intermittently, and 20% are non-carriers [23]. In some studies, carriage rates were greater among hospitalized patients compared with patients on admission. However, a wide range in carriage rates among hospitalized patients and health care workers is reported [17 –21,23,30]. This may partly be due to differences in study population, sampling quality, time of sampling, and culture techniques [23]. Colonization patterns of hospitalized patients and health care workers are not well known. Similar colonization patterns in health care workers compared with those in population studies have been reported. However, data are limited [20]. Because the present study is a cross-sectional study, the group of positively tested participants is a mix of permanent and intermittent carriers and both positive and negative tested participants might in fact be intermittent carriers. A longitudinal study should be performed to specify carriage patterns among hospitalized patients and physicians.

Controversy remains about the role of health care workers in transmission. It is believed that most nosocomial S. aureus infections are endogenous in origin [3,7]. However, multiple outbreaks due to nasal or hand carriage of S. aureus by health care workers have been reported [6,32]. Moreover, an endogenous origin could not be demonstrated in most cases in a study on the origin of orthopedic S. aureus SSIs [8]. These patients were either intermittent carriers and tested negative preoperatively or the pathogen originated from an exogenous source. Although the nares are the most common site of colonization, other body sites could have been colonized in these patients.

Despite the fact that vigilance to prevent nosocomial infections has always been of great importance, compliance of disinfecting hands is only 32% among physicians [33]. Moreover, there is an association between hand and nasal carriage of S. aureus [34]. A single treatment of intranasal mupirocin in health care workers was effective in reducing S. aureus nasal carriage up to 1 y and eradication of S. aureus nasal carrying health care workers led to a significant decrease of hand carriage up to 6 mo [35]. Hence, nasal decolonization of physicians might reduce the risk of transmission through hand contact. Nevertheless, this might be unsuccessful in the long term, as resistance to mupirocin could be developed [12].

It could be argued that the control group was not a well-balanced representation of the general population. Nevertheless, its carriage rate (30.8%) is in line with the accepted prevalence in many studies [3,23]. One of the limitations of the study is the lack of proof of demographic dispersal in the physician group. Although participants were randomly included at the entrance of the congress center, selection bias might have occurred. A limitation of the present study is that gender and surgical experience were the only recorded variables. After all, male gender, obesity and history of cerebrovascular event are associated with an increased likelihood and greater age, current smoking and use of antibiotics in the month before surgery with a decreased likelihood of S. aureus nasal carriage in general surgical patients [5]. Validation of the current results in a larger cohort with controlling for abovementioned factors influencing likelihood of carriage is recommended.

In conclusion, a significantly greater nationwide nasal carriage rate of S. aureus among surgeons and surgical residents compared with an outpatient control group is demonstrated in the present study. Further research on transmission and colonization patterns is needed. Moreover, future studies are recommended to investigate the impact of greater carriage rates among physicians on S. aureus-related nosocomial infections and whether decolonization of physicians could aid in preventing the burden of these hospital-related events.

Footnotes

Acknowledgments

The authors thank Marieke C.R. Alders, technician medical microbiology, Orbis Medical Center, Sittard, for performing laboratory analysis; Idserd D.G. Klop, medical student at Maastricht University, for helping with collecting samples; Yvette J. Kraat, clinical microbiologist, and Ruben G.J. Visschers, resident in surgery, Orbis Medical Center, Sittard, for their advice, help and support; bioMérieux (Marcy-l'Étoile, France) for providing the S. aureus ID chrome agar plates and Isola applicator cartridges; and the NVvH Chirurgendagen 2012 (Annual Dutch Surgical Society Meeting) and its participants for the possibility to collect samples.

Author Disclosure Statement

No competing financial interests exist.

References

Mangram

, Horan

, Pearson

, et al. Guideline for prevention of surgical site infection, 1999. Centers for Disease Control and Prevention (CDC) Hospital Infection Control Practices Advisory Committee. Am J Infect Control, 1999; 27:97–132.

Perl

. Prevention of Staphylococcus aureus infections among surgical patients: Beyond traditional perioperative prophylaxis. Surgery, 2003; 134:S10–17.

Wertheim

, Melles

, Vos

, et al. The role of nasal carriage in Staphylococcus aureus infections. Lancet Infect Dis, 2005; 5:751–762.

Saadatian-Elahi

, Teyssou

, Vanhems

. Staphylococcus aureus, the major pathogen in orthopaedic and cardiac surgical site infections: A literature review. Int J Surg, 2008; 6:238–245.

Herwaldt

, Cullen

, French

, et al. Preoperative risk factors for nasal carriage of Staphylococcus aureus. Infect Control Hosp Epidemiol, 2004; 25:481–484.

Herwaldt

. Staphylococcus aureus nasal carriage and surgical-site infections. Surgery, 2003; 134:S2–9.

Kluytmans

, Wertheim

. Nasal carriage of Staphylococcus aureus and prevention of nosocomial infections. Infection, 2005; 33:3–8.

Berthelot

, Grattard

, Cazorla

, et al. Is nasal carriage of Staphylococcus aureus the main acquisition pathway for surgical-site infection in orthopaedic surgery?. Eur J Clin Microbiol Infect Dis, 2010; 29:373–382.

Donker

, van der Laan

, Hendriks

, Kluytmans

. Evaluation of Staphylococcus aureus nasal carriage screening before vascular surgery. PloS One, 2012; 7:e38127.

10.

Munoz

, Hortal

, Giannella

, et al. Nasal carriage of S. aureus increases the risk of surgical site infection after major heart surgery. J Hosp Infect, 2008; 68:25–31.

11.

Kalmeijer

, van Nieuwland-Bollen

, Bogaers-Hofman

, de Baere

. Nasal carriage of Staphylococcus aureus is a major risk factor for surgical-site infections in orthopedic surgery. Infect Control Hosp Epidemiol, 2000; 21:319–323.

12.

Simor

. Staphylococcal decolonisation: An effective strategy for prevention of infection?. Lancet Infect Dis, 2011; 11:952–962.

13.

Perl

, Cullen

, Wenzel

, et al. Intranasal mupirocin to prevent postoperative Staphylococcus aureus infections. N Engl J Med, 2002; 346:1871–1877.

14.

van Rijen

, Bonten

, Wenzel

, Kluytmans

. Mupirocin ointment for preventing Staphylococcus aureus infections in nasal carriers. Cochrane Database Syst Rev, 2008:CD006216.

15.

Bode

, Kluytmans

, Wertheim

, et al. Preventing surgical-site infections in nasal carriers of Staphylococcus aureus. N Engl J Med, 2010; 362:9–17.

16.

Wertheim

, Vos

, Ott

, et al. Risk and outcome of nosocomial Staphylococcus aureus bacteraemia in nasal carriers versus non-carriers. Lancet, 2004; 364:703–705.

17.

Rashid

, Farzana

, Sattar

, Murtaza

. Prevalence of nasal Staphylococcus aureus and methicillin-resistant Staphylococcus aureus in hospital personnel and associated risk factors. Acta Pol Pharm, 2012; 69:985–991.

18.

Farzana

, Rashid

, Akhtar

, et al. Nasal carriage of staphylococci in health care workers: Antimicrobial susceptibility profile. Pak J Pharm Sci, 2008; 21:290–294.

19.

Nulens

, Gould

, MacKenzie

, et al. Staphylococcus aureus carriage among participants at the 13th European Congress of Clinical Microbiology and Infectious Diseases. Eur J Clin Microbiol Infect Dis, 2005; 24:145–148.

20.

Johnston

, Stokes

, Ross

, et al. Staphylococcus aureus colonization among healthcare workers at a tertiary care hospital. Infect Control Hosp Epidemiol, 2007; 28:1404–1407.

21.

Rongpharpi

, Hazarika

, Kalita

. The prevalence of nasal carriage of Staphylococcus aureus among healthcare workers at a tertiary care hospital in Assam with special reference to MRSA. J Clin Diagn Res, 2013; 7:257–260.

22.

Schwarzkopf

, Takemoto

, Immerman

, et al. Prevalence of Staphylococcus aureus colonization in orthopaedic surgeons and their patients: A prospective cohort controlled study. J Bone Joint Surg Am, 2010; 92:1815–1819.

23.

Kluytmans

, van Belkum

, Verbrugh

. Nasal carriage of Staphylococcus aureus: Epidemiology, underlying mechanisms, and associated risks. Clin Microbiol Rev, 1997; 10:505–520.

24.

Kalmeijer

, Coertjens

, van Nieuwland-Bollen

, et al. Surgical site infections in orthopedic surgery: The effect of mupirocin nasal ointment in a double-blind, randomized, placebo-controlled study. Clin Infect Dis, 2002; 35:353–358.

25.

Wertheim

, Vos

, Ott

, et al. Mupirocin prophylaxis against nosocomial Staphylococcus aureus infections in nonsurgical patients: A randomized study. Ann Intern Med, 2004; 140:419–425.

26.

Boisseau

, Alfandari

, Gauzit

, et al. Staphylococcus aureus nasal carriage during the infectious diseases national congress in France. Med Mal Infect, 2012; 42:435–439.

27.

Guclu

, Yavuz

, Tokmak

, et al. Nasal carriage of pathogenic bacteria in medical students: Effects of clinic exposure on prevalence and antibiotic susceptibility. Eur Arch Otorhinolaryngol, 2007; 264:85–88.

28.

Grandin

, Deschamps

, Magdoud , et al. Evaluation of the impact of different lengths of pre-enrichment in a nutritive broth and prolonged incubation of MRSA-ID, a chromogenic agar medium, on its performances for identifying methicillin-resistant Staphylococcus aureus in screening samples. Pathol Biol (Paris), 2009; 57:e37–42.

29.

Safdar

, Narans

, Gordon

, Maki

. Comparison of culture screening methods for detection of nasal carriage of methicillin-resistant Staphylococcus aureus: A prospective study comparing 32 methods. J Clin Microbiol, 2003; 41:3163–3166.

30.

Askarian

, Zeinalzadeh

, Japoni

, et al. Prevalence of nasal carriage of methicillin-resistant Staphylococcus aureus and its antibiotic susceptibility pattern in healthcare workers at Namazi Hospital, Shiraz, Iran. Int J Infect Dis, 2009; 13:e241–247.

31.

Zanger

, Nurjadi

, Gaile

, et al. Hormonal contraceptive use and persistent Staphylococcus aureus nasal carriage. Clin Infect Dis, 2012; 55:1625–1632.

32.

Blok

, Troelstra

, Kamp-Hopmans

, et al. Role of healthcare workers in outbreaks of methicillin-resistant Staphylococcus aureus: A 10-year evaluation from a Dutch university hospital. Infect Contr Hosp Epidemiol, 2003; 24:679–685.

33.

Erasmus

, Daha

, Brug

, et al. Systematic review of studies on compliance with hand hygiene guidelines in hospital care. Infect Contr Hosp Epidemiol, 2010; 31:283–294.

34.

Tammelin

, Klotz

, Hambraeus

, et al. Nasal and hand carriage of Staphylococcus aureus in staff at a department for thoracic and cardiovascular surgery: Endogenous or exogenous source?. Inf Control Hosp Epidemiol, 2003; 24:686–689.

35.

Doebbeling

, Reagan

, Pfaller

, et al. Long-term efficacy of intranasal mupirocin ointment. A prospective cohort study of Staphylococcus aureus carriage. Arch Intern Med, 1994; 154:1505–1508.