Stethoscopes or Maybe “Bacterioscopes” – Is hand Hygiene Solely Capable of Preventing Hospital-Associated Infections?

The World Health Organization (WHO) recognizes the phenomenon of healthcare-associated infections (HAIs) as a global public health problem still at the forefront of the challenges facing healthcare nowadays (Álvarez et al. 2016; Napolitani et al. 2020). These infections pose a risk primarily to hospitalized patients, most often affect people with impaired immunity, and are usually caused by multidrug-resistant organisms (MDRO) with a high spread potential (Álvarez et al. 2016; Knecht et al. 2019; Napolitani et al. 2020). Many cross-infections are mainly transmitted by healthcare workers’ (HCWs) hands, which actively contribute to transferring pathogens from one patient to another and within the healthcare institutions, thus, contributing to many HAIs (Álvarez et al. 2016; Kalra et al. 2021). Besides HCW hands, critical or invasive devices are also responsible for HAIs (Arora et al. 2020). Moreover, it is worthwhile to mention that non-critical medical devices, such as stethoscopes, white coats, masks, and latex gloves, can significantly contribute to HAIs, too, and have been taken into account in many outbreaks of HAIs (Datta et al. 2018; Messina et al. 2018; Millán-Lou et al. 2022).

Despite the continuous development of medical equipment used in diagnostic methods, the stethoscope poses an inseparable attribute of HCWs, including medical students, in their daily practice, and it is the primary clinical tool for patient care (Álvarez et al. 2016; Datta et al. 2018; Napolitani et al. 2020). The familiar sight of a doctor with a stethoscope significantly impacts the patient’s confidence when in contact with the physician (Knecht et al. 2019; Kalra et al. 2021). On the other hand, contaminated stethoscopes often enable the transmission of MDRO (Raksha et al. 2014; Gazibara et al. 2015; Haddad et al. 2019). Scientific studies carried out worldwide confirm a very high degree, on average 85% (range 66–100%) of the HCW stethoscopes contamination with a multitude of various bacteria, including dangerous pathogens such as methicillin-resistant Staphylococcus aureus (MRSA) (Datta et al. 2018; Kalra et al. 2021).

Medical students are going to become HCWs when they finish their medical studies. The period of their studies is the time for education and developing good habits and practices, including hand and stethoscope hygiene. Therefore, their hygiene habits are only fully developed, established, or sometimes correct once they finish their education (Uneke et al. 2008; Saunders et al. 2013).

Disinfecting procedures are applied to control the decrease in the microbial population in medical devices (CDC 2016). The cleaning and disinfection status of the stethoscope is an essential factor in considering the possibility of environmental influences on the spread and transmission of bacterial pathogens (Álvarez et al. 2016). Although the Centers for Disease Control and Prevention (CDC) recommend cleaning the stethoscope, the guidance is vastly different from for hand hygiene. The CDC recommends cleaning the stethoscope with alcohol only once a week or if it is visibly soiled (CDC 2016). Alternatively, it recommends using disposable stethoscopes (Whittington et al. 2009). In Poland, stethoscope disinfection procedures and practices barely exist or are unknown. At the same time, WHO recommendations in the form of “the five moments for hand hygiene” are commonly known. WHO rules precisely define the frequency and situations in which hand hygiene should be performed (WHO 2004). The CDC and the Food and Drug Administration (FDA) guidelines for hand hygiene are also known (Pittet et al. 2001; CDC 2016). This lack of rules for stethoscope hygiene and well-known recommendations for hand hygiene might be confusing, especially for students.

Given this context, the objective of this study was to evaluate the hygiene habits of medical students, including the examination of disinfection practices, confronted with the cleanliness of the stethoscopes they use. Therefore, the main aim of our study was to investigate the contamination of stethoscopes employed by medical students. It involved isolation, identification, testing of antibiotic resistance, and the clonality of the isolated bacterial pathogens.

Characteristics of the student population and survey analysis. Twenty-five students from the 3^rd year, twenty-eight from the 4^th year, and thirteen from the ^5th year, with mean ages of 22.8 vs. 22.8 vs. 24.0, respectively, participated in the study. Among the 3^rd year students, there were more men than women (15/10), while among the 4^th and 5^th-year students, there were almost the same numbers of women and men (13/15 vs. 6/7).

Based on the results of the survey, it was found that 32% (n = 8) of the 3^rd, 35.7% (n = 10) of the 4^th, and 15.4% (n = 2) of the 5^th year students claimed to have cleaned their stethoscopes after every patient (Table I). Actually, 16% (n = 4), 35.7% (n = 10), and 23.1% (n = 3) of them declared to have cleaned their stethoscopes several times a day (details in Table I). The most frequently used method of stethoscope disinfection was swabbing with hand disinfectant gel. It was the case for 91.7% (n = 22) of 3^rd-year students, 100% (n = 28) of 4^th-year students, and 84.6% (n = 11) of 5^th-year students (Table I).

Students claimed to have predominantly cleaned their stethoscope diaphragms and bells (66.2% vs. 61.5%). As many as 78.4% of the respondents were never instructed on stethoscope hygiene, and 64.6)% had not searched for such information on their own. The students looked for different sources of knowledge about stethoscope disinfection techniques. For most of them, clinical classes inside and outside the university were the most popular source of proper hygiene practices (46.9% vs. 28.1%). Almost everyone used a chemical hand sanitizer to disinfect his or her stethoscope (93.8%; p = 0.022). Almost equal numbers of students used stethoscopes themselves, and at the same time, many of them rarely lent their stethoscopes to friends during clinical classes (43.5% vs. 46.8%). Almost everyone cleaned their hands after examining each patient (95.5%) and declared that almost everyone was taught the correct hand hygiene technique during classes (92.3%).

Most of the students admitted that they would disinfect their stethoscopes more frequently (answer 4 was given more often than the others on the Likert scale) if teachers emphasized stethoscope hygiene (Table II). Students declared that disinfectants were not available in adequate numbers in places where they had classes and contact with patients (answer 2 was given more often than the others on the Likert scale). Most students declared that they would disinfect the stethoscope more often if disinfectants were available in adequate amounts (answer 4 was more frequent). At the same time, the respondents believed that disinfectants might cause damage to the stethoscopes, which was statistically significant (p = 0.0037) when comparing declarations of the 4^th and 5^th-year students.

Most respondents strongly believed that the stethoscope might be a vector for microorganisms (answer 5 was more frequent) regardless of the year of study. For most of them, it was important to keep their stethoscopes and hands clean (answer 5 was more frequent). The participants also declared that they did not see their friends cleaning their stethoscopes regularly (answer 2 was given more often than the others on the Likert scale; details in Table II). There was a positive correlation between the frequency of stethoscope disinfection and individuals who believed that maintaining good hygiene of the stethoscope is important (p = 0.003; details in Table III). The correlation between students’ observations concerning disinfecting stethoscopes by other students and the declared frequency of stethoscope disinfection was also positive (p < 0.001).

Profile of bacteria recovered from stethoscope surfaces. Out of 66 stethoscopes cultured, all (100%) were found to be contaminated with at least one bacterial species. In total, 277 strains (including nine genera, 19 species) of bacteria were isolated. A bacteriological overview of the microorganisms isolated from the contaminated stethoscopes belonging to medical students with a particular emphasis on the Staphylococcus species is summarized in Fig. 1. Concerning other bacterial strains, Corynebacterium spp. (n = 3; 1.1%), Kocuria rhizophila (n = 3; 1.1%), Chryseomonas spp. (n = 1; 0.36%), Enterococcus faecalis (n = 1; 0.36%), and Neisseria mucosa (n = 1; 0.36%) were isolated. All collected Micrococcus spp. (n = 48; 17.3%) were identified as Micrococcus luteus. Among the ten species belonging to the genus Streptococcus, six S. equisimilis (2.17%), three S. sanguinis (1.08%) and one S. mitis (0.36%) were identified.

Fig. 1.

All (100%) of the 11 S. aureus and 31.9% (n = 15) of the 47 S. epidermidis strains showed methicillin resistance. All MRSA and MRSE strains also had the MLS_B phenotype (resistance to erythromycin and resistance to clindamycin). All isolates tested harbored the mecA gene. None of the Streptococcus strains showed the presence of the MLS_B phenotype. Furthermore, none of the Enterococcus strains displayed either the HLAR or VRE phenotypes. Neither HLAR nor VRE was detected in the Enterococcus strains.

The diaphragms were more contaminated than bells as they included one hundred and fifty-eight (57%) vs. one hundred and nineteen (43%) bacterial strains (Fig. 2). The stethoscopes of 3^rd-year students gave rise to the isolation of one hundred and twelve bacterial strains, including sixty-three (56.25%) from diaphragms and forty-nine (43.75%) from bells. Whereas 112 strains were isolated (including 66 strains from diaphragms and 46 from bells) in the group of the 4^th year students. The stethoscopes of 5^th-year students carried 55 strains (n = 31 from diaphragms and n = 24 from bells).

Fig. 2.

Molecular typing of MRSA and MRSE. MRSA and MRSE strains were subjected to molecular typing. Generally, among 11 MRSA isolates, four different PFGE (A-D) clusters were identified (Fig. 3 and S1). Ten MRSA isolates came from 5^th-year students’ stethoscopes assigned to one exercise group 11. One strain, number 124, was isolated from a 3^rd-year students’ stethoscope assigned to the same exercise group 11. Clone A gathered four strains with identical genetic profiles from 5^th and 3^rd-year students’ stethoscopes assigned to group 11, including two strains (no. 188 and 189) from one student, derived from the bell and diaphragm of the same stethoscope. Three strains of identical pulsotype from 5^th-year students’ stethoscopes belonging to the same group 11 were classified into clone B. All strains representing clone B were from the bell. Clones C and D were formed by two MRSA strains with identical pulsotypes within the clone, also isolated from the 5^th-year and group 11 students’ stethoscopes, where the C clone included bell-derived strains and clone D formed strains isolated from the diaphragm.

Fig. 3.

In the molecular analysis of 15 MRSE strains, three clones (A-C) were distinguished. In addition, ten strains representing unique restriction patterns (singletons) (D-L) were detected (Fig. 4). Clone A consisted of two strains with identical pulsotype derived from the diaphragm of stethoscopes of students belonging to the same 3^rd-year and the same group 11. Similarly, clone B was created by two strains from stethoscopes from students from the same 3^rd year and the group 12, also isolated from the diaphragm. Clone C gathered two strains derived from stethoscope bells of 5^th-year students classified to group 11. The remaining MRSE strains (D-L) were not related to each other.

Fig. 4.

We observed that the stethoscopes of three students were contaminated with MRSA and MRSE strains simultaneously (Fig. 3 and 4).

The hands, and in particular the fingers of physicians, are a source of bacteria that can be transmitted to the patient during a medical examination, so compliance with hand hygiene guidelines is an essential aspect of HAI prevention (Napolitani et al. 2020). However, as scientists from around the world prove, the source of infections with bacteria, including HAIs, can also be medical stethoscopes, which, when used many times a day, come into direct contact with the patients’ skin (Tschopp et al. 2016; Knecht et al. 2019). Since these instruments are frequently used on multiple patients, they can quickly become a source of transmission of many microorganisms, including the most dangerous pathogens, for example, MRSA (Torres-Ballesteros et al. 2017; Datta et al. 2018). Contaminated hands of HCWs can also be the source of stethoscope contamination. It is a possible way of transmitting bacterial strains because compliance rates of HCWs with hand hygiene principles before the COVID-19 pandemic were known to be around 50% (Vasudevan et al. 2019). The vast majority of JUMC students pay appropriate attention to proper hand hygiene. However, the risk associated with contaminated stethoscopes cannot be overlooked. Recent studies show that many stethoscopes are contaminated with numerous pathogenic bacteria (Campos-Murguía et al. 2014; Haddad et al. 2019). Various authors estimate the degree of stethoscope colonization to be very high: 85–87.3% (Álvarez et al. 2016), 66–100% (Datta et al. 2018), and 30–97% (Fafliora et al. 2014). Our study confirms this phenomenon by demonstrating that 100% of students’ stethoscopes gave rise to a positive bacterial culture, including commensal microbiota and potentially pathogenic microorganisms. These findings align with the other studies, which recorded that 100% of the 62 stethoscopes tested showed bacterial growth (Bansal et al. 2019). Analysis of our survey results demonstrated that only 30.3% of the JUMC students cleaned their stethoscopes properly. Moreover, some students declared that they had never cleaned the stethoscope. Other studies showed that 33.33–36% of students never cleaned their stethoscopes (Bukharie et al. 2004; Raksha et al. 2014;). As a comparison, in Serbia, the survey data showed that 40% of 4^th-year students cleaned their stethoscopes at least once a day compared with 30% for 6^th year students (Gazibara et al. 2015). In Poland, only 15.18% of the students disinfect the stethoscope before examining the patient, but 9.82% do not do it at all (Kawalec et al. 2014).

Our survey results indicate that students from different years of study most often used hand sanitizer containing ethyl alcohol to disinfect stethoscopes. Research carried out by Grandiere-Perez et al. (2015) confirmed that disinfection of stethoscopes by ethanol-based hand sanitizer (gel or foam) was effective also at reducing MRSA colonies. Parmar et al. (2004) found that 66% ethyl alcohol was an effective disinfectant for stethoscope cleaning. In our study, students believed that disinfectants could damage the stethoscope. What is also interesting, students gave contradicting answers stating that they would disinfect the stethoscopes more often if sanitizers were easily accessible. At the same time, they claimed that they had broad access to the disinfectant agents. Neither of these responses was statistically significant. Our study showed that MRSA and MRSE strains survived the disinfection. Bacteria that survive disinfection can quickly become resistant to subsequent disinfection attempts; therefore, it is recommended to strictly observe the operating time of disinfectants, which is indicated on the packaging (Knecht et al. 2019).

Generally, the analysis of the survey results revealed that the students needed to have adequate knowledge about the hygiene of stethoscopes. Such a conclusion was presented earlier in the study by Gazibara et al. (2015). It is disturbing that many JUMC students felt that teachers and tutors supervising their classes in medical facilities did not give them the knowledge and proper cleaning techniques to apply stethoscope hygiene. Elsewhere, studies showed that students and other HCWs did not follow the standard protocol set to prevent infections by using stethoscopes (Arora et al. 2020). Altogether, these results prove a need for essential knowledge about stethoscope hygiene. In their colleagues’ opinion, observation of each other’s hygiene practices among the students showed that they do not clean their stethoscopes frequently enough. We asked students to answer this question because observation practices are often used in hospitals as one of the HAI surveillance tools (Vasudevan et al. 2019). This type of supervision may positively affect students’ stethoscopes and hand hygiene.

On the other hand, it is comforting that the students in our study declared their willingness to learn proper techniques for disinfecting stethoscopes, and they feel at ease when they know that their stethoscopes are clean. Therefore, medical students should be educated and motivated to practice not only hand hygiene but also current and correct disinfecting procedures for stethoscopes as important parts in preventing HAIs. Other researchers also believe that educating students about stethoscope hygiene is crucial to developing good practices in the future and essential to reduce the number of HAIs (Gaisser et al. 2021).

For our research, we had chosen the bell and the diaphragm as they come in direct contact with the fingers of HCWs and are applied directly to the patient’s body to receive vibrations from a selected skin surface area and transmit them to the inside of the waveguide. According to the literature data, bacterial colonization of the diaphragm is much more frequent than the colonization of the bell (Dutra et al. 2013; Campos-Murguía et al. 2014; Queiroz Júnior et al. 2021). It is also confirmed by our results from all tested stethoscopes, regardless of the year of a student’s education. Generally, it is known that, in Polish conditions, the bell is used less frequently than the diaphragm, which is in line with our results. As declared by the students, the frequency of cleaning individual elements of the stethoscopes also varied. Both in our study and the one by Gazibara et al. (2015), students cleaned the diaphragm more often (48.5% vs. 84% vs. 89.9%) than the bell (33.3% vs. 42% vs. 51%). Similarly, in the Indian study conducted by Datta et al. (2018), 60% of medical interns cleaned the diaphragm more frequently, while 40% cleaned both the diaphragm and the bell.

Our study did not include additional protection measures, such as disposable stethoscope diaphragm barriers. These kinds of solutions are still infrequent in Polish hospitals. Although many authors indicate them as having a more favorable protective effect than stethoscope disinfection (Vasudevan et al. 2020; Kalra et al. 2021; Peacock et al 2023), these studies are generally relatively new.

During our study (pre-COVID-19 era), there was a lack of information about the existence of disposable stethoscope diaphragm barriers in Poland. Considering the neglectful approach to disinfection and the protection of medical equipment in Poland, the emphasis on the disinfection of stethoscopes is more than justified. As disposable aseptic diaphragm barriers were shown to work as efficient solutions to reduce the transmission of pathogens via stethoscopes, it seems reasonable to change the attitude and practice concerning the hygiene of stethoscopes. Adequate procedures, the attitude of training, and practice of stethoscope hygiene should become an essential topic of discussion with people responsible for healthcare organizations in Poland and worldwide. There is a need to purchase special disinfectants for medical equipment and disposable stethoscope diaphragm barriers in Polish hospitals. Furthermore, there is a need to provide adequate knowledge, procedures, and practice of stethoscope hygiene to medical students during their studies.

According to literature data, the profile of bacteria contaminating the surfaces of stethoscopes represents an enormous species diversity with a predominance of Gram-positive organisms representing a regular part of the human skin and mucous membranes microbiota (Álvarez et al. 2016; Thapa and Sapkota 2017; Johani et al. 2018; Knecht et al. 2019). It is confirmed by the findings in our study, which showed that the dominant contaminant species were staphylococci (50.5%), headed by representatives of the CoNS group (46.5%), including 10.7% of MRSE isolates. As a comparison, observations carried out in Tunisia confirm the contamination of stethoscopes also mainly by the genus Staphylococcus, but to a lower degree (30.7%, including CoNS 17.9% and methicillin-resistant CoNS 5.1%) (Haddad et al. 2019). The isolation of S. epidermidis in our and other studies indicates that stethoscopes are easily contaminated with microbiota from the skin of patients who undergo physical examinations. Unfortunately, it is disturbing that we isolated strains of S. epidermidis resistant to antibiotics (MRSE) from the surface of the stethoscopes.

In our study, S. aureus strains accounted for 7.9% of all analyzed bacteria, and were methicillin-resistant (MRSA strains). It is worth noting that, for severe infections, the risk of death is approximately twofold higher with MRSA than with methicillin-susceptible S. aureus (MSSA) (Fenelon et al. 2009). Furthermore, MRSA strains can survive up to nine days on stethoscopes (Sahiledengle 2019). Other studies showed that contamination of stethoscopes with S. aureus was higher, but the percentage of strains resistant to beta-lactam antibiotics was lower than in our study. In a study by Uneke et al. (2008), S. aureus amounted to 41.6%. According to Queiroz Júnior et al. (2021), 80% to 100% of stethoscopes in use are contaminated with S. aureus, of which 20–40% are resistant to methicillin. As a comparison, in the study by Gazibara et al. (2015), S. aureus was most frequently isolated at 62.64%, of which 21.05% were MRSA isolates. In studies by Datta et al. (2018), S. aureus isolates accounted for 15% of all bacteria isolated, and MRSA strains accounted for 25%. Perhaps it is related to the type of disinfection agent and the response to exposure to the disinfectant (CDC 2016). In contrast, no S. aureus strain was detected in a study by a research team in Saudi Arabia (Bukharie et al. 2004).

In our study, the isolation of bacteria considered to be permanent or transient skin microbiota resulted in the genera Bacillus (25.3%), Micrococcus (17.3%), and Streptococcus (3.6%), which altogether amounted to 46.2% of the detected bacteria. For most people, these bacteria are not etiologic agents of infections. However, for children, immunosuppressed patients, or patients undergoing invasive medical procedures during hospitalization, micrococci, and streptococci can cause severe invasive infections (Laupland et al. 2019; Martín Guerra et al. 2019; Neff et al. 2020; Zhu et al. 2021). Contrary to our findings, other studies showed a much lower percentage of contamination with bacilli, micrococci, and streptococci on the surfaces of stethoscopes. Other authors showed stethoscope contamination with Bacillus spp. at the rate of 2.6% to 16.48% (Raksha et al. 2014; Haddad et al. 2019). Also, Raksha et al. (2014) showed contamination of stethoscopes with Micrococcus spp. (4.40%). However, Haddad et el. (2019), did not detect micrococci. Others also showed that Streptococcus spp. contaminated 9% of stethoscopes or not at all (Johani et al. 2018; Haddad et al. 2019). In our study, E. faecalis was isolated only once. Contrary to our study, others showed a much higher contamination with enterococcal strains. For example, among bacteria isolated from stethoscopes of medical students in Nigeria, E. faecalis strains accounted for 16.1% and were identified as the HLAR phenotype (Uneke et al. 2008). Johani et al. (2018) revealed a relatively high percentage of vancomycin-resistant Enterococcus (VRE) at 7%. Numerous studies have shown that antibiotic-resistant strains of common healthcare pathogens (e.g., Enterococcus, P. aeruginosa, K. pneumoniae, and E. coli) were as sensitive to disinfectants as antibiotic-sensitive strains. It may explain the lack of detection of Gram-negative rods on the surfaces of the stethoscopes in our study. According to Arora et al. (2020), 12.7% of Gram-negative bacteria and 14.3% of enterococci were isolated from stethoscopes.

The aim of PFGE analysis was to assess the clonality and persistence of MRSA and MRSE isolates among JUMC students’ stethoscopes. The PFGE study of the tested MRSA and MRSE strains indicated a selection of resistant isolates of an epidemic nature and their transmission between students. Our study focused solely on evaluating the persistence of MRSA and MRSE strains on students’ stethoscopes. The obtained results are difficult to discuss due to the minimal number of studies on this subject or even the lack of studies on molecular analyzes of MRSA and MRSE isolates from stethoscopes used by medical students. We only found studies proving the involvement of stethoscopes in the spread of MDRO and HAIs involving Gram-negative bacteria (Crespo et al. 2004; Messina et al. 2018; Lee et al. 2021; Millán-Lou et al. 2022).

The main limitation of our study was the lack of nasal swabs (carrier assessment) from stethoscope owners and environmental samples. In the future, it will be important to extend the research that can prove the link between the possible transmission of strains contaminating stethoscopes of medical students and the hospital environment and newly hospitalized patients.

Training proper hygiene habits should be improved during classes in each year of studies. It is known that consolidating proper hygiene habits requires a correct example from teachers, knowledge of procedures, repeating activities, and the possibility of verifying the acquired skills. If students develop good hygiene habits during their studies, there is a high probability that they will apply them properly while practicing their profession.

Our study, together with many others, has asserted the need to elevate the priority of stethoscope hygiene in the daily practice of HCWs and to update the disinfection guidelines in care facilities. Therefore, medical students should be educated about hand and stethoscope hygiene as a collaborative effort to prevent HAIs (Fig. 5).

Fig. 5.

Based on the results of the questionnaires, the necessity of the validated procedures for cleaning the stethoscopes was demonstrated. The survey results show the supervisor’s key role in shaping students’ proper hygiene habits. This study highlights the fact that the stethoscopes of medical students are contaminated with numerous bacteria, including multidrug-resistant organisms. The clonal structure of the MRSA and MRSE populations derived from stethoscopes has been demonstrated. Our results confirm the possibility that these medical devices mediate the spread of hazardous pathogens in the hospital and non-hospital environments. Practical exercises are essential to forming the correct hygiene habits involving stethoscopes, which enable practicing and checking the correctness of the established skills.