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Infection Control Program and WHO Collaborating Centre on Patient Safety, University of Geneva Hospitals, Geneva, SwitzerlandFaculty of Medicine, University of Geneva, Geneva, Switzerland
Infection Control Program and WHO Collaborating Centre on Patient Safety, University of Geneva Hospitals, Geneva, SwitzerlandFaculty of Medicine, University of Geneva, Geneva, Switzerland
Infection Control Program and WHO Collaborating Centre on Patient Safety, University of Geneva Hospitals, Geneva, SwitzerlandFaculty of Medicine, University of Geneva, Geneva, Switzerland
Infection Control Program and WHO Collaborating Centre on Patient Safety, University of Geneva Hospitals, Geneva, SwitzerlandFaculty of Medicine, University of Geneva, Geneva, Switzerland
Correspondence: Address to Didier Pittet, MD, MS, Infection Control Program and WHO Collaborating Centre on Patient Safety, University of Geneva Hospitals, 4 Rue Gabrielle-Perret-Gentil, 1211 Geneva 14, Switzerland.
Infection Control Program and WHO Collaborating Centre on Patient Safety, University of Geneva Hospitals, Geneva, SwitzerlandFaculty of Medicine, University of Geneva, Geneva, Switzerland
To compare the contamination level of physicians’ hands and stethoscopes and to explore the risk of cross-transmission of microorganisms through the use of stethoscopes.
Patients and Methods
We conducted a structured prospective study between January 1, 2009, and May 31, 2009, involving 83 inpatients at a Swiss university teaching hospital. After a standardized physical examination, 4 regions of the physician’s gloved or ungloved dominant hand and 2 sections of the stethoscopes were pressed onto selective and nonselective media; 489 surfaces were sampled. Total aerobic colony counts (ACCs) and total methicillin-resistant Staphylococcus aureus (MRSA) colony-forming unit (CFU) counts were assessed.
Results
Median total ACCs (interquartile range) for fingertips, thenar eminence, hypothenar eminence, hand dorsum, stethoscope diaphragm, and tube were 467, 37, 34, 8, 89, and 18, respectively. The contamination level of the diaphragm was lower than the contamination level of the fingertips (P<.001) but higher than the contamination level of the thenar eminence (P=.004). The MRSA contamination level of the diaphragm was higher than the MRSA contamination level of the thenar eminence (7 CFUs/25 cm2 vs 4 CFUs/25 cm2; P=.004). The correlation analysis for both total ACCs and MRSA CFU counts revealed that the contamination level of the diaphragm was associated with the contamination level of the fingertips (Spearman’s rank correlation coefficient, ρ=0.80; P<.001 and ρ=0.76; P<.001, respectively). Similarly, the contamination level of the stethoscope tube increased with the increase in the contamination level of the fingertips for both total ACCs and MRSA CFU counts (ρ=0.56; P<.001 and ρ=.59; P<.001, respectively).
Conclusion
These results suggest that the contamination level of the stethoscope is substantial after a single physical examination and comparable to the contamination of parts of the physician’s dominant hand.
The patient-to-patient transmission of microorganisms is a major threat to hospitalized patients and causes significant morbidity and mortality. The present evidence indicates that health care workers’ hands are the main route of cross-transmission.
Small medical equipment, such as stethoscopes, may also contribute to the dissemination of microorganisms, but the evidence supporting this hypothesis is less robust and their role in microorganism propagation is poorly understood. Similar to any piece of medical equipment, stethoscopes have the theoretical capacity to be vectors of pathogens through a multistep process. First, stethoscopes must acquire microorganisms after contact with a source patient.
Second, these organisms must then survive on the object for at least several minutes and be transferred to the skin of a second patient during subsequent use. Numerous factors may affect the risk of transmission at each of these steps,
and assessing transmissibility is better achieved by studying 1 step at a time.
Many factors must be considered when conducting such studies. For example, as no piece of noncritical equipment used on patient wards is meant to be sterile, most objects in the health care environment will yield microorganisms when sampled. However, the clinical significance of detecting low levels of contamination is uncertain. One way to solve this difficulty and better understand the relative contribution of stethoscopes in the transmission of microorganisms is to place their levels of contamination into perspective with those of a universally recognized vector of dissemination, that is, the physician’s own hands. If the number of bacteria recovered from stethoscopes is much lower than the number recovered from the examiner’s hands, their role in the transmission of pathogens would be deemed more negligible. In contrast, if their contamination level is reported to be comparable with that of the examiner’s hands, their capacity to transmit pathogens would be more significant and transmission mitigation measures would be more urgently needed.
We aimed to compare prospectively the contamination level of stethoscopes and physicians’ hands after a single, standardized, physical examination by using quantitative cultures and 2 different markers of contamination.
Patients and Methods
Setting
We conducted a structured prospective study between January 1, 2009, and May 31, 2009, at the University of Geneva Hospitals (HUG), Geneva, Switzerland. HUG is a 2200-bed primary and tertiary teaching hospital admitting 47,000 patients annually with a long-standing experience in hand hygiene promotion.
Patients were recruited from internal medicine and orthopedic operating wards by using a convenience-based recruitment strategy. Eligibility criteria included stable medical condition, absence of a life-threatening condition, absence of active skin infection, and age 18 years or more. Eligible patients colonized with methicillin-resistant Staphylococcus aureus (MRSA) were identified by reviewing infection control databases and ongoing surveillance activities. Screening for MRSA colonization after patient admission by sampling of the anterior nares and the perineal region with a sterile premoistened swab is a standard operating procedure at HUG in specified acute care wards.
The present study was approved by the institutional review board of HUG.
Standardized Physical Examination
After patient enrollment, 1 of 3 physicians (Y.L., C.T., or A.S.) was randomly selected to perform a physical examination at the patient bedside. The examination was standardized to ensure reproducibility (Table 1). Physicians were allowed to adapt to unforeseen events (such as unbuttoning the patient’s gown or moving the bedside table) as long as the action was commonly encountered in routine clinical practice. An external observer ensured adherence to the standardized physical examination by using a checklist. A sterile stethoscope (Littmann Cardiology II, 3M) was used for each physical examination. Sterilization was conducted by using hydrogen peroxide gas plasma technology to preserve the integrity of the material (STERRAD 100NX Sterilizer, Advanced Sterilization Products).
The present study was divided into 2 phases. Phase 1 aimed to assess the total aerobic colony count (ACC). Sterile gloves (Protegrity Micro SMT PF, Cardinal Health) were worn by the examiner before the physical examination to ensure that the initial count would be zero. Phase 2 of the study focused solely on MRSA transmission, and the examiner conducted the physical examination with bare hands. The physician performed 2 consecutive hand hygiene procedures by using an alcohol-based hand rub formulation (Hopirub, B. Braun Medical AG) before the examination to ensure that hands were MRSA free. Each hand hygiene action strictly followed the World Health Organization–recommended technique and lasted at least 30 seconds.
To confirm the absence of MRSA, cultures of 4 regions of the examiners’ hands were performed after hand hygiene and before the beginning of the physical examination by using agar impression on selective chromogenic plates (MRSA-ID, Count-tact, bioMérieux SA).
After the completion of the physical examination, 4 regions of the physician’s dominant gloved (phase 1, ACC study) or ungloved (phase 2, MRSA study) hand (ie, fingertips, thenar eminence, hypothenar eminence, and dorsum) were sampled in addition to 2 sections of the stethoscope (diaphragm and tube). Sampling of the hand and stethoscope diaphragm was conducted by gently pressing the region under study on contact plates for 5 seconds.
The sampled section was located 10 cm from the head of the stethoscope.
Nonselective media were used to determine the total ACC (Count-Tact, bioMérieux SA), and selective chromogenic media were used to determine the MRSA colony-forming unit (CFU) count (MRSA-ID). After sampling, contact plates were incubated aerobically at 37°C for 18 to 24 hours. All colonies that grew on nonselective media were counted to assess the total ACC. Green colonies on MRSA-selective plates were considered presumptive MRSA isolates, and 1 colony per sample was subcultured onto Columbia blood agar for formal identification. The confirmation of MRSA isolates was achieved by a combination of tests, including a duplex quantitative polymerase chain reaction assay to evaluate the presence of the mecA gene and femA gene specific for S. aureus.
The total ACC and the MRSA CFU count per 25 cm2 were assessed using the following strategy developed in our laboratory: contact plates were digitally photographed, and the number of colonies was determined using a manual counting tool (Adobe Photoshop CS4 Extended). This strategy allows the precise measurement of CFU counts of up to 5000 CFUs/25 cm2. Interrater reliability was evaluated in a pilot study during which 3 independent observers measured CFU counts on 34 digital photographs with a wide range of bacterial growth (range, 2-4805 CFUs/25 cm2). The agreement between observers was high (intraclass correlation coefficient, 0.987; 95% CI, 0.977-0.993; P<.001; data not reported). The maximum colony count was fixed at 5000 CFUs; beyond this, colonies formed a confluent surface.
Statistical Analyses
Descriptive analysis results are expressed as percentages for categorical variables and as median values and interquartile ranges (IQRs) or as mean ± SD for continuous variables, as appropriate. Because of skewed distributions, the levels of contamination of different parts of the hands and stethoscopes were described as medians with 25th and 75th percentiles (ie, IQR) and depicted in the form of box plots. The contamination of different regions of hands and stethoscopes was compared using Wilcoxon signed-rank tests for paired continuous variables. We generated scatter plots and used the Spearman’s rank correlation coefficient (ρ) to measure correlations between the contamination of different parts of hands and the contamination of stethoscopes. All tests were 2-sided, and a P value of less than .05 was considered to indicate statistical significance. Statistical analyses were performed using PASW statistics, version 18 (SPSS Inc).
Results
Baseline Characteristics
A total of 489 quantitative cultures were taken to evaluate bacterial contamination of 83 study participants (ACC study: 33; MRSA study: 50). Because MRSA was not recovered from the physicians’ dominant hand or the stethoscope after the examination of 12 of 50 patients colonized with MRSA (24%), these patients were excluded from the final analysis. The clinical characteristics of participants are listed in Table 2. Most participants were men (43 of 71 [60.6%]), with a mean age of 68±16 years. A total of 23 participants (32%) were undergoing antibiotic therapy, 8% had a central venous line, and one-fifth had an indwelling urinary catheter. Twenty-one of 71 patients (30%) had 1 or more skin wounds. The mean time since their last bath/shower was 10±6 hours. Half of the patients had last bathed themselves by using a sponge by the sink, one-third had taken a shower, and 14% had received a sponge bath in their bed. One patient colonized with MRSA was undergoing decolonization at the time of the study.
Table 2Characteristics of Patients Enrolled at the University of Geneva Hospitals, Geneva, Switzerland
Figure 1 depicts the levels of bacterial contamination of stethoscopes and physicians’ hands. After a single examination, the most heavily contaminated region in terms of the total ACC was the fingertips (median contamination [IQR], 467 [141-2239] CFUs/25 cm2), followed by the stethoscope diaphragm (median [IQR], 89 [27-691] CFUs/25 cm2). The contamination levels of the thenar and hypothenar eminences were comparable (median [IQR], 37 [11-117] and 34 [11-117] CFUs/25 cm2, respectively). The median level of stethoscope tube contamination was 18 [IQR 4-120] CFUs/25 cm2. The least heavily contaminated region was the dorsum of the hand (median [IQR], 8 [2-41] CFUs/25 cm2). When comparing these various regions, we found that the contamination level of the diaphragm was significantly lower (P<.001) than the contamination level of the fingertips but significantly higher than the contamination level of the thenar eminence, hypothenar eminence, and dorsum of the hand (P≤.004 for each comparison). The contamination level of the stethoscope tube was lower than that of the fingertip and thenar eminence (P≤.04), similar to that of the hypothenar eminence (P=.10), and higher than that of the dorsum of the hand (P=.04).
Figure 1Total aerobic colony count recovered from physicians’ gloved hands (orange boxes) and stethoscopes (blue boxes) after a single physical examination. Results are presented on a logarithmic scale. The top and bottom of the box plots represent the interquartile ranges, and the horizontal lines represent the median values. The error bars extend to the maximum and minimum values. Differences between levels of contamination were tested using Wilcoxon paired rank-sum tests. CFU = colony-forming unit. ∗P<.001 compared with stethoscope tube. ∗∗P=.04 compared with stethoscope tube.
After the examination of patients colonized with MRSA (Figure 2), the most heavily contaminated region was again the fingertips (median [IQR], 12 [3-113] CFUs/25 cm2), followed by the stethoscope diaphragm (median [IQR], 7 [0-71] CFUs/25 cm2), thenar eminence (median [IQR], 4 [0-13] CFUs/25 cm2), and hypothenar eminence (median [IQR], 2 [1-23] CFUs/25 cm2). The median levels of the contamination of the stethoscope tube and hand dorsum were 0. When comparing these various regions in terms of MRSA contamination, we found that diaphragm contamination was not significantly different from fingertip contamination (P=.54) and was higher than thenar eminence (P=.004), hypothenar eminence (P=.02), and hand dorsum (P<.001) contamination. Tube contamination was lower than the fingertip (P<.001), thenar eminence (P=.02), and hypothenar eminence (P=.008) contamination, but similar to hand dorsum contamination (P=.42).
Figure 2Methicillin-resistant Staphylococcus aureus CFU counts recovered from physicians’ hands (orange boxes) and stethoscopes (blue boxes) after a single physical examination. Results are presented on a logarithmic scale. The top and bottom of the box plots represent the interquartile ranges, and the horizontal lines represent the median values. The error bars extend to the maximum and minimum values. Differences between contamination levels were tested using Wilcoxon paired rank-sum tests. CFU = colony-forming unit. ∗P<.001 compared with stethoscope tube. ∗∗P=.02 compared with stethoscope tube. ∗∗∗P=.008 compared with stethoscope tube.
Correlation Between Hand and Stethoscope Contamination
For both total ACCs and MRSA CFU counts, the contamination level of stethoscopes was strongly associated with the contamination level of physicians’ hands. As illustrated in Figure 3, A-D, the total ACC contamination level of the diaphragm increased with the contamination level of the fingertips (ρ=.80; P<.001), thenar eminence (ρ=.47; P=.006), hypothenar eminence (ρ=.47; P=.006), and hand dorsum (ρ=.71; P=.001). Similar findings were found for tube contamination (Figure 3, E-H). The contamination level of the tube increased with the contamination levels of the fingertips (ρ=.56; P=.001), thenar eminence (ρ=.48; P=.005), hypothenar eminence (ρ=.56; P=.001), and hand dorsum (ρ=.61; P=.001).
Figure 3A-D, Relation between total ACC contamination of stethoscope diaphragm and physicians’ fingertips (panel A), thenar eminence (panel B), hypothenar eminence (panel C), and hand dorsum (panel D). E-H, Relation between total ACC contamination of stethoscope tube and physicians’ fingertips (panel E), thenar eminence (panel F), hypothenar eminence (panel G), and hand dorsum (panel H). Data are presented on a logarithmic scale. ACC = aerobic colony count; CFU = colony-forming unit.
Figure 4, A-D, illustrates the association between the MRSA contamination level of the stethoscope diaphragm and the MRSA contamination of examiners’ hands. The increased MRSA contamination level of the diaphragm was associated with the increased contamination level of the fingertips (ρ=.76; P<.001), thenar eminence (ρ=.76; P=.006), hypothenar eminence (ρ=.68; P<.001), and hand dorsum (ρ=.44; P=.005). Similarly, the MRSA contamination level of the stethoscope tube was associated with the contamination of each of the 4 regions of the hand (ρ>.59; P<.001 for all comparisons; Figure 4, E-H).
Figure 4A-D, Relation between methicillin-resistant Staphylococcus aureus contamination of stethoscope diaphragm and physicians’ fingertips (panel A), thenar eminence (panel B), hypothenar eminence (panel C), and hand dorsum (panel D). E-H, Relation between methicillin-resistant Staphylococcus aureus contamination of stethoscope tube and physicians’ fingertips (panel E), thenar eminence (panel F), hypothenar eminence (panel G), and hand dorsum (panel H). Data are presented on a logarithmic scale. CFU = colony-forming unit.
Despite a strong theoretical basis, cross-transmission through small medical equipment, such as stethoscopes, sphygmomanometers, and thermometers, is much less understood. The present study found that the contamination of stethoscopes is not negligible after a physical examination. In general, stethoscope diaphragms are contaminated as much as (or even more than) the physician’s own thenar eminence. Furthermore, we observed a direct relation between hand and stethoscope contamination, with higher levels of hand contamination associated with the increased levels of stethoscope contamination. This observation suggests that the patient’s skin and immediate surroundings are the common denominators and determinants of both physicians’ hands and stethoscope contamination. Why some patients apparently shed bacteria more readily than others remains to be elucidated and deserves further study.
Most studies have investigated the levels of stethoscope contamination by using a point prevalence methodology.
These studies have found considerable variation in stethoscope contamination, ranging from a few CFUs to several hundreds. This variation could be due to factors that are difficult to control in cross-sectional studies, such as the frequency of stethoscope use, the exact use of the instrument (eg, taking blood pressure, auscultation of the lungs, heart, abdomen, or great vessels), or the frequency of disinfection. In addition, the “opportunity for contamination” is often not considered in these studies.
This observation probably partly explains the wide discrepancy in the frequency of MRSA contamination of stethoscopes between cross-sectional studies, which ranges from 0% to 27%.
We controlled for potential confounders by standardizing the physical examination, using sterile stethoscopes, assessing MRSA colonization in patients, and comparing stethoscope contamination with the contamination level of the examiner’s own dominant hand. Furthermore, although quantification of bacterial contamination has so far been hampered by the difficulty to count high numbers of CFU on relatively small culture plates, we developed a new strategy to precisely quantify high bacterial counts on these media.
To our knowledge, stethoscope tube contamination has not been studied so far, probably because it does not come into contact with the patient’s skin and is not perceived as a significant vector of transmission. The present study finds that the contamination level of the stethoscope tube is not only comparable to that of the examiner’s hand dorsum but also greater. Contamination probably occurs indirectly through its manipulation with contaminated hands, and these findings highlight the need to disinfect the stethoscope tube as well as the diaphragm.
It is generally recognized that most physicians and nurses do not disinfect their stethoscopes frequently (ie, less than once a month, if at all). Most surveys support this perception and reveal that 70% to 90% of the physicians do not disinfect systematically their stethoscope after every patient contact.
By considering that stethoscopes are used repeatedly over the course of a day, come directly into contact with patients’ skin, and may harbor several thousands of bacteria (including MRSA) collected during a previous physical examination, we consider them as potentially significant vectors of transmission. Thus, failing to disinfect stethoscopes could constitute a serious patient safety issue akin to omitting hand hygiene. Hence, from infection control and patient safety perspectives, the stethoscope should be regarded as an extension of the physician’s hands and be disinfected after every patient contact. However, the optimal method of disinfection remains to be determined. Alternatively, cross-transmission could be interrupted by assigning stethoscopes to individual patients. Clearly, there is an urgent need to identify effective transmission mitigation strategies.
This study has some limitations. It was conducted in a single hospital with the participation of a limited number of physicians and patients, thus limiting its generalizability to other settings. We used a convenience-based strategy to recruit patients. We assessed contamination of 4 regions of physicians’ dominant hands and 2 sections of stethoscopes, and our findings may not be generalizable to the nondominant hand. The contamination level of the entire surfaces of hands and stethoscopes was not assessed, because these are technically difficult to evaluate. It is possible that the overall contamination of both hands is quantitatively much higher than the overall contamination of stethoscopes, thereby reducing the relative transmission potential of stethoscopes. Subsequent studies are required to investigate the transmission potential of each part of hands and stethoscopes and better understand which ones are more likely to transmit pathogens. With the exception of MRSA, we did not distinguish pathogenic and nonpathogenic bacteria. The identification of all microorganisms recovered from hands and stethoscopes would require considerable resources. Whether a similar relation exists between hand and stethoscope contamination for other health care–associated pathogens such as Clostridium difficile remains to be determined. In addition, the exact source of contamination of stethoscopes and hands could not be identified. We hypothesize that most contamination originates from patients, but contamination with the physicians’ own hands also probably occurred. As mentioned initially, this study focused solely on the first step of the cross-transmission process. Transmission is affected by a multitude of other variables, such as a pathogen’s capacity to survive on the surface, the frequency of the use of the object, and the quality of disinfection.
Conclusion
Our findings provide strong evidence of the potential for stethoscope-mediated transmission of microorganisms and the need to systematically disinfect stethoscopes after each use. Consequently, our results may help convince physicians of the importance of proper and timely disinfection. Further studies will be required to better understand microorganism survival on stethoscopes as well as their transmissibility onto a recipient’s skin. Furthermore, additional studies are needed to better understand how stethoscopes can be efficiently and safely disinfected.
Acknowledgment
We thank Rosemary Sudan for expert editorial assistance.
Dr Longtin is now with the McGill University Faculty of Medicine and Jewish General Hospital, Montreal, Quebec, Canada.
Grant Support: This study was supported by an institutional grant from the University of Geneva Hospitals . The authors also acknowledge the recent funding for partial financial support for hand hygiene research activities by subsidy 3200BO-122324/1 from the Swiss National Science Foundation .
Although the article by Longtin et al1 published in the March 2014 issue of Mayo Clinic Proceedings is an important contribution, it does not offer a solution to the infectivity of stethoscopes. An article by my colleagues and me,2 which was cited by Longtin et al, documented that ethanol-based hand sanitizer effectively cleans stethoscope surfaces as well as the hands. The simple maneuver of concurrently wiping stethoscope surfaces and cleaning hands with sanitizer is proven to be effective in reducing colony counts of known pathogens and requires virtually no additional time.
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