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Are bearded doctors dangerous? Are smartphones and credit cards safe? The importance of hygiene and object disinfection around hospital and private practice settings as well as the public environment.


Wiktor Kostecki1, Kuba Kupniewski1, Vanessa Crain1, Mitchell Raymond Mann1, Marta Płońska1, Lingjuan Zeng1, Edyta Golińska2, Agata Pietrzyk3, Piotr Kochan4



Introduction

Proper hand hygiene in a healthcare setting is essential in preventing the spread of infections from patient to patient. Although maintaining adequate hand hygiene is a simple, cost-effective way to limit the spread of hospital infections, it is difficult for healthcare personnel to achieve sufficient compliance with hand hygiene guidelines to be effective at decreasing the transmission of diseases [1]. According to the European Centre for Disease Prevention and Control (ECDC), 30% of the annual hospital infections can be prevented if medical personnel follows hand hygiene guidelines [2]. According to Centers for Disease Control and Prevention (CDC) data, about one out of 25 patients becomes afflicted with a healthcare-associated infection (HAI) during his or her hospital stay. The CDC data shows that there are about 722,000 HAIs a year and 75,000 patients die. Although infectious diseases have stepped down from the most common cause of death for many years now, especially in developed countries, HAIs still account for a significant amount of burden to the healthcare system. It is reported that at any given time, the prevalence of HAIs is 3.5% to 12% in developed countries and 5.7% to 19.1% in low- and middle-income countries [3].

Predictably, bacteria have been found on the hands of healthcare workers after patient interaction, including wound care, intravascular catheter care, respiratory tract care and handling patient secretions. However, bacteria have also been found on the hands of workers after surface contact, including taking a patient’s pulse, temperature, and blood pressure. Bacteria transmitted by physical contact with patients include Klebsiella spp., Staphylococcus aureus including methicillin-resistant S. aureus (MRSA), Clostridium difficile, and gram-negative bacteria. Indirect patient contact, such as handling of objects in the patient environment (e.g. patient beds) or objects carried around the hospital (e.g. patient charts) can also serve as sources of pathogen transmission [4].

Nowadays, with the prevalence of touch screen cell phones, with over 5 billion people owning cell phones (over 50% of which being smartphones) and the fact that people on average touch their cell phones 2,617 times a day, information regarding the hygienic risk that cell phones pose is of significant clinical importance [5, 6]. Cell phones have been found to be carriers of bacteria (including multi-drug resistant bacteria) [7]. Of all of the Staphylococcus species, S. aureus is the most dangerous. It has been reported to be present in the nose of about 30% of healthy adults and on the skin of about 20% of people, although this number is likely higher in hospital workers [8]. Other Staphylococcus species that can be found on the skin and often contaminate prosthetics and catheters include coagulase negative species such as Staphylococcus warneri and Staphylococcus epidermidis [9].

With the current situation of the COVID-19 pandemic, the importance of hand hygiene has become pertinent to not only the healthcare setting but also the general population. This study was done before the 2019/2020 COVID-19 pandemic, with the purpose of finding out whether medical students ̶ the future healthcare personnel may bring bacteria to patients not only from hands but also other personal use items. By demonstrating the findings of the study, we would like to raise awareness of hygiene in the health care setting and facilitate compliance to hand hygiene and other HAI preventative guidelines.

Materials and methods

The article originates from the microbiology laboratory exercise entitled "Disinfection, sterilization, and hand hygiene". Third-year medical and third-year dental surgery students from Jagiellonian University Medical College, School of Medicine in English performed experiments which would allow them to see whether everyday objects and their hands harboured potential biohazards for their future patients. Trypticase soy agar (TSA) Petri dishes were distributed among students with the purpose of making imprints of fingers and other objects.

Handprints. Students began by marking the Petri dishes with their names and initials and were then asked to make imprints of one selected unwashed finger. Students then washed their hands according to standard, non-medical hand hygiene protocol. After air-drying their hands, students were again asked to make a print on the Petri dish with the same finger, but on a different field, marked as washed. Afterwards, the students rubbed a handful of alcohol-based fluid (Skinman Soft Protect, EcoLab, Germany) into their hands and made the last print once their fingers were dry, on a separate field of the same Petri dish marked as disinfected. DDS-3 students made two different versions of prints: involving the dirty finger and nonmedically washed finger or involving the dirty finger and alcohol solution (Skinman Soft Protect, EcoLab, Germany) treated finger. The Petri dishes were then placed in incubators at 37 °C overnight and then photographed.

Body parts, inanimate and animate objects. In the next experiment, during the same lab exercise, students were allowed to make imprints of objects or body parts of their choice on the TSA Petri dishes. The selection included: keys, credit cards, wallets, cell phones, watches, jewellery (especially rings, wedding rings, earrings, and necklaces), hair bands, shoes, casino chips (sic!), doorknobs, faucets, coins and lab seats. Some students went to the washroom and made swabs and imprints of the toilet seat and flushing mechanism, as well as their genitals. Very interestingly, some students decided to test their beards, noses, and chest hair by making such imprints and swabs as well. Making an imprint was based on touching the surface of the agar with the given object for 5-10 seconds. After labelling, the Petri dishes were incubated in the same manner as described above and photographed.

Identification of selected specimens. This time, unlike Holstad et al. [2], we decided not only to show if there is visible growth of bacteria on the Petri dishes and how many colonies there are, but we wanted to roughly know what bacteria were present on hands and objects. We have therefore selected three cultures derived from: 1. fingerprints, 2. a credit card, and 3. an iPhone (Figure 1).

The colonies growing on these Petri dishes were not only stained with Gram stain but were also identified further using API kits (bioMérieux, France).


figure1
Figure 1. Petri dishes with cultures from (L to R): credit card, iPhone, and fingers ("D" stands for dirty, "W" stands for washed with soap and water, "DW" stands for washed & disinfected).
[please click on the image to enlarge]


Materials and methods

After incubation, we noted growth of microorganisms on virtually all Petri dishes. Many of the Petri dishes showed abundant growth, which would be significant quantitatively. The Gram staining showed interesting results (Figures 1-3), which was then confirmed by API testing:

1. The following microbes were isolated from the fingerprints culture:


a) Dirty hands (fingerprint): - Bacillus spp. (Bacillus subtilis)
- Staphylococcus aureus
- Staphylococcus epidermidis
- Staphylococcus warneri

b) Washed hands (fingerprint):
- Staphylococcus aureus
- Staphylococcus epidermidis
- Staphylococcus warneri

2. On the credit card the following were isolated:
- Bacillus spp. (Bacillus subtilis)
- Staphylococcus capitis
- Staphylococcus lentus
- Staphylococcus epidermidis

3. iPhone harboured the following strains:
- Gram+ bacilli (other than B. subtilis)
- Micrococcus spp.
- Staphylococcus warneri

figure2
Figure 2. Gram positive Bacillus spp. from the credit card. A photograph of the Gram-stained specimen (1000×).
[please click on the image to enlarge]


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Figure 3. Gram-stained sample from the iPhone (1000×).
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After analyzing the photographs, we made a selection of the most interesting Petri dishes showing bacterial colonies, which are now featured in Figures 4-16.

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Figure 4. Screenshot of the recording made from the specimens to be seen on the official WJOMI YouTube channel: https://youtu.be/9R9Q5SI8uos
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figure5
Figure 5. Petri dish with cultures made from the dirty, soap washed and alcohol-treated finger. Please note the difference in size and colour of colonies probably from the natural flora on the washed field.
[please click on the image to enlarge]


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Figure 6. Petri dish with cultures made from the dirty, soap washed and washed and alcohol-treated finger. Alcohol-based fluid is currently recommended to be used without previous washing of hands.
[please click on the image to enlarge]


figure7
Figure 7. Petri dish with cultures made from a credit card and a hair tie.
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Figure 8. Petri dish with colonies from cultures taken off an iPhone.
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Discussion

Below, you may find brief descriptions of the few species of bacteria we identified from the credit card, iPhone, and fingers.

Bacillus subtilis

Bacillus subtilis is a Gram-positive, catalase-positive, rod-shaped, facultative anaerobic bacterium commonly found in the upper layers of soil and is a gut commensal in humans [10]. Like other Bacillus genus members, B. subtilis forms an endospore during times of nutritional stress, enabling for its long-term survival in extreme conditions of temperature, pH, salinity, radiation, and dehydration [10]. B. subtilis is highly flagellated, enabling for its rapid movements in liquids. B. subtilis readily takes up DNA from the environment and can be genetically manipulated in the laboratory setting [10]. For this reason, the species is a common model organism and is frequently used to assess sporulation and bacterial chromosome replication [11]. B. subtilis was historically used to stimulate the immune response to promote recovery from diseases of the gastrointestinal and urinary tracts [12] and has since been used in numerous bioindustrial applications, including radionucleotide waste disposal [13], the production of amylase and various proteases and as a soil inoculant [14, 15].

B. subtilis has been designated as safe by various health agencies, including the Food and Drug Administration [16] and the European Food Safety Authority [17]. Some strains cause ropiness in spoiled bread dough, leading to a sticky and stringy consistency, but is otherwise not harmful to humans [18].

Staphylococcus aureus

Staphylococcus aureus is a Gram-positive, catalase-positive, beta-haemolytic facultative anaerobe that grows in clusters [19, 20]. S. aureus is a common human gut commensal and is also found on the skin (e.g. the nares, axilla, groin, and ears), the upper respiratory tract, and the female reproductive tract [19, 21, 22]. While a common member of the body’s microbiota with 20-30% of the population being long-term carriers [21, 23], S. aureus is an opportunistic pathogen that produces several virulence factors, including protein A (used to bind the Fc-IgG to inhibit complement activation and phagocytosis) [24] exfoliative toxin [25], enterotoxin type B [25, 26], and toxic shock syndrome toxin [25, 26], causing inflammatory and toxin-mediated diseases. S. aureus can cause skin infections [23, 27, 28], organ abscesses, sinusitis, pneumonia, septic arthritis and endocarditis; it is a leading cause of osteomyelitis [23, 28, 29]. Additionally, it can cause scalded skin syndrome, rapid-onset food poisoning [30], and potentially fatal toxic-shock syndrome [25, 26]. S. aureus is one of the most common causes of nosocomial infections and commonly leads to post-surgical wound infections and prosthetic infections. S. aureus infections are treated with penicillin, but the emergence of MRSA is a global clinical problem [31]. One also has to pay special attention to the growing problem of community-associated MRSA (CA-MRSA), in majority causing skin and soft tissue infections, as well as other phenotypes of resistance, including vancomycin-intermediate S. aureus (VISA) and vancomycin-resistant S. aureus (VRSA).

Staphylococcus epidermidis

Staphylococcus epidermidis is a bacterium that normally colonizes human skin. It serves as a common cause of nosocomial infections, being able to attach to indwelling medical devices (e.g. catheters). Treatment for S. epidermidis infections amounts to an estimated $2 billion per year in the United States, alone. Although S. epidermidis rarely leads to life-threatening disease, it is a robust strain of bacteria, evolved to survive in harsh conditions on the skin, including extreme salt concentrations and osmotic pressures. The same factors that allow S. epidermidis to persist on human skin make it a difficult pathogen to treat clinically. S. epidermidis is resistant to treatment and forms biofilms, bacterial aggregations with strong resistance to antibiotics (e.g., MRSE), inside the body. Not only is it difficult to treat, but it is also easily spread during medical procedures such as catheter placement and care [32].

Staphylococcus warneri

Staphylococcus warneri makes up less than 1% of skin flora and is a catalase-positive, oxidase-negative, coagulase-negative bacterium [33]. These facultatively anaerobic bacteria produce several antimicrobial molecules such as bacteriocin nukacin ISK-1 and warnericin, the latter of which has been shown to have activity against Legionella [34]. Of note, it has been found that biofilm-forming strains of S. warneri carried more genes conferring beta-lactam, aminoglycoside and macrolide resistance than strains that did not produce biofilms. Tigecycline and rifampicin have been proven to be effective against such resistant strains [35]. S. warneri rarely may cause sepsis, mostly in immunocompromised individuals, and has also been linked to abscesses, septic arthritis and endocarditis [33]. As with all coagulase-negative staphylococcus species, S. warneri may lead to catheter-related bacteraemia, colonize prosthetic heart valves, prosthetic joints, neurosurgical shunts and can pose a problem in intensive care nurseries [36]. These infections are commonly resistant to penicillin as they have beta-lactamase activity but are susceptible to other antibiotics with gram-positive activity. Rarely S. warneri may cause urinary tract infections, which respond to fluroquinolones [33].

Staphylococcus lentus

Staphylococcus scirubi subspecies lentus is a gram-positive, oxidase-positive, coagulase-negative zoonotic bacterium which infrequently infects humans. It is a known animal pathogen, that has been isolated from multiple species of animals as well as farm soil and water [37]. In humans, S. lentus is known to colonize and cause multiple types of infections such as endocarditis, urinary tract infections, endophthalmitis, pelvic inflammatory disease, and peritonitis [38]. Unlike other members of the sciuri group, lentus lacks the Mac A gene and hence is more susceptible to antibiotics, especially β-lactams, to which other members of the group are resistant, but vancomycin remains the first-line treatment in case of an infection [39].

Staphylococcus capitis

Staphylococcus capitis is an aerobic, gram-positive, coagulase-negative, spherical bacterium which is a part of the normal flora of human skin, with an inclination towards the scalp and face. It is known for its ability to form a biofilm, which allows it to establish surface-associated communities and offers protection from antibiotics [40]. Although S. epidermidis is by far a more common pathogen in gram-positive, coagulase-negative infections, S. capitis accounts for 5% of pathogenic isolates from coagulate-negative infection sites and has been implicated in pneumonia, UTIs, catheter-related, bacteraemia, cellulitis, as well as prosthetic joint infections. When it comes to antibiotic sensitivity, S. capitis shows less resistance to antibiotic treatment than S. epidermidis, but vancomycin is the preferred treatment in case of coagulase-negative staphylococcal infection.

Micrococcus spp.

Micrococcus species are gram-positive, catalase-positive and strictly aerobic cocci, which usually form white to yellow colonies on blood agar. There are currently 16 species under the Micrococcus genus, such as M. luteus, and they are commonly found on human skins, mucosa and oropharynx [41]. Although micrococci rarely cause infectious disease in humans, cases like bacteraemia [42] endocarditis [43], keratitis [44], brain abscess [45], peritonitis [46] have been reported especially in immunocompromised patients [41]. In addition, micrococci are also one of the common blood contaminants that can interfere with the diagnostic procedure [47]. Micrococcus spp. are relatively susceptible to most antibiotics. Infections caused by Micrococcus have been treated by antibiotics like penicillin, gentamicin, clindamycin and vancomycin.

In this investigation, we sought to determine the different bacterial species which healthcare professionals may expose their patients to via passive contact with everyday objects or their own body parts. In doing so, we aimed to emphasise the importance of proper hand hygiene and sanitation in the clinical setting as to prevent the transmission of such bacterial species and protect patients from their potential mal effects. In assessing the bacterial cultures derived from over a dozen common objects, including jewellery, cell phones, credit cards, keys, wallets, and faucets, as well as body parts such as fingers, beards, and genitalia, we were able to isolate several bacterial species of varied prevalence within or on the human body and responsible for a diverse range of potential health risks.

We found it extremely interesting that one of the bacteria that was found on the credit card – S. lentus, a zoonotic bacterium, which normally lives on horse’s skin, was isolated and is an infrequent pathogen causing peritonitis. We could hypothesize the potential route it took from the person having contact with an animal, going through their daily business using a credit card, and finally having contact with a patient, possibly causing an infection. Another aspect of the study showed that facial and bodily hair may be reservoirs of certain bacterial species. One could think about many aspects of such results with respect to medical and psychological consequences in medical practices. Should some rules prohibit doctors from having facial hair? Should there be special guidelines provided to doctors with facial hair to use special hygiene protocols for facial hair? Would this be an infringement on their personal liberties? This poses a good question, why doctors have facial hair and how patients view doctors with and without facial hair.



















































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figure8
Figure 9. One of the most interesting cultures made from facial and body hair. Material collected from the same person.
[please click on the image to enlarge]

Some articles point to the fact that doctors with facial hair may be perceived differently by patients. As observed by a psychiatry resident Nathan P. Morris, medical staff and patients alike treat him with more seniority when he goes a few days without a clean shave. What is more, senior physicians he works with no longer mistake him for a medical student [48]. When it comes to cleanliness of beards of medical staff, and whether it might be a safe harbour of common nosocomial pathogens, a study published in the Journal of Hospital Infections attempted to compare rates of facial bacterial colonization in clean shaven male staff and the ones who lack any form of facial hair. Although there were no differences in the colonization rates by gram-negative bacteria, surprisingly, S. aureus and coagulase-negative staphylococci were statistically less prevalent in staff who have facial hair when compared to shaven individuals [49]. One might wonder what the reason for such a discrepancy can be, is medical staff with any form of facial hair more likely to spend extra time in the bathroom each morning? Without a doubt it is difficult question to answer but it doesn’t look like medical staff will need to say goodbye to their facial hair for hygienic reasons anytime soon.

figure8
Figure 10. Culture of nasal swab and mobile phone showing abundant colony growth.
[please click on the image to enlarge]

Analysing Ong and Poljak’s paper entitled "Smartphones as mobile microbiological laboratories", we as medical professionals should remember that mobile devices are becoming more and more popular, not only as contact cell phones but also as fully-fledged medical devices [50]. Nowadays, more and more apps, as well as smartphone accessories, allow doctors to improve the point-of-care approach to medical procedures, such as using guidelines, making the smartphone a dermatoscope for visualizing skin cancer and melanomas, a potential device for reading the vital parameters and blood pressure of patients, as well as proposed in the article above, mobile microbiological lab of the future. Therefore, we must think of devising a proper smartphone disinfection algorithm to be available internationally or on a national level, as smartphones are devices which are being used constantly to contact patients, the family, friends, use social media, and also in any hospital setting, are known to serve a higher purpose, but at the same time harbour multiple species of pathogenic bacteria.

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Figure 11. Culture of toilet key imprint showing numerous colonies.
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figure8
Figure 12. Culture of a watch and glasses (temple with earpiece imprint).
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figure8
Figure 13. Yet another culture from a credit card.
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Figure 14. Colonies growing from an earring and nasal skin.
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Figure 15. Colonies grown from an armband culture.
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Figure 16. Credit card culture.
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The importance of washing hands has been linked to better healthcare outcomes for almost two centuries by Dr. Ignaz Semmelweis. However, studies have demonstrated the lack of proper hand hygiene knowledge in healthcare professionals [51], which still hinders the effort in HAI reduction. On the contrary, many studies showed encouraging results that education programs for hand hygiene successfully decreased the HAI, even including infection caused by MRSA [52-54]. With our study confirming the fact that healthcare workers can easily expose to and potentially carry pathogenic bacteria, it is never enough to underlie the importance of improving hand hygiene compliance and reducing HAI through education programs. According to Mathai et al., an effective education program should promote behaviour change, and address not only "why" but also "when" and "how" handwashing must be performed [54]. Besides, there are also studies evaluating the effectiveness of hand hygiene education in a community setting, which also provided a positive impact of education on the compliance of handwashing practice. For example, one study showed that hand hygiene education significantly increased the number of self-reported handwashing and hand sanitizer using during the period of the Middle East Respiratory Syndrome (MERS) outbreak in Korea [55]. Such results indicated that, in terms of control of infectious disease, hand hygiene education could potentially bring positive effects to healthcare settings but also community settings.

Our results confirm these risks and extend them to other items that may commonly be found in the medical setting and beyond: body parts of both medical personnel and patients, articles of clothing, jewellery, watches, smartwatches, doorknobs, faucets, credit cards, poker chips, shoes, keys, and nightclub tags. Beyond the duties at the hospital, one must keep in mind that medical staff show a variety of interests like any other members of society, having hobbies, relaxing, socializing, etc. [56]

It is of primary importance to follow the WHO worked-out algorithms for medical hand hygiene, but as the data below show, it may be a tough nut to crack. According to the Centers for Disease Control and Prevention (CDC), approximately 1.7 million hospital-associated infections lead to 99,000 deaths each year in the USA alone [57]. Other sources report that 2 million patients in the US are infected annually, racking up a cost ranging from $4.5 billion to $11 billion per year [58]. The most common types of hospital infections in the US include urinary tract infections (40%), followed by surgical site infections (5%-20%), and bloodstream infections and pneumonia (9-27%) [59]. It would be surprising to find that there is a huge discrepancy between European Union (EU) and US data, where the European Centres for Disease Control and Prevention (ECDC) lists approximately 4.1 million hospital infections annually in the EU, of which 30% could be prevented by adhering to strict hand-hygiene protocols [2]. We live in an era which was already predicted by Alexander Fleming, in his Nobel lecture, i.e. the era of antibiotic resistance. Thus far, we understood antimicrobial resistance mostly in terms of hospital settings. Unfortunately, as our research moved on, we started noticing resistant strains in community settings, too. This is mostly due to care-free approaches to food-production (animal production) and overuse of antibiotics in antibiotic growth promoters (AGPs) since most of the global antibiotic production is not used in healthcare settings but is rather spent on mass-scale animal production. Another aspect of antibiotic overuse may also be noted in some prescription-free and deregulated healthcare systems. The different phenotypes of resistance in microbes that may be very difficult to treat include MRSA, VISA, VRSA, ESBL, Amp-C, and many more. The transmission of such resistant strains may be propagated with poor hygiene standards [60].


Conclusions

Our results demonstrated that there are many potential hazards for a healthcare provider and patients to be exposed to possible pathogens. This further emphasizes the importance of proper hand hygiene, and more importantly, the necessity to educate healthcare providers when and how to wash their hands. Despite the fact that WHO hand hygiene guidelines are widely available, the data show non-adherence to hand hygiene protocols. In addition, the results proved that many personal objects can potentially harbour pathogens. Therefore, it indicates that conducting regular disinfection of personal objects, like cell phones, jewellery, should be mandatory, especially in medical settings, and highly considered in community settings, especially during the pandemic. Global health organizations must come together to work out a better system for convincing medical staff to follow proper hand hygiene protocols. Modern technology could be implemented to help “enforce” such algorithms by giving visual or acoustic signalling when the procedure of hand hygiene is completed or not done correctly.

Another reminder could be implemented with a smartphone app which would signal the need for hand hygiene when crossing, for example, patient zones.

As to the answers to the title questions: "Are bearded doctors dangerous?" and "Are smartphones and credit cards safe?", we must say it all depends on personal and object hygiene. As described in the discussion, facial hair may possibly also lower colonization with S. aureus and CNS. As to the credit cards - they may not necessarily be safer than money, especially when passed around there are many microorganisms on their surface. And phones are currently the most contaminated objects.

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Acknowledgements: Big words of thanks to all JUMC students who contributed to this article with their samples.

Conflict of interest: PK is the Editor-in-Chief of WJOMI.

Authors’ affiliations:
1 Jagiellonian University Medical College, School of Medicine in English, Cracow, Poland.
2 Jagiellonian University Medical College, Microbial Ecology Lab, Department of Bacteriology, Microbial Ecology and Parasitology, Cracow, Poland.
3 Jagiellonian University Medical College, Head of Parasitology Lab, Chair of Microbiology, Cracow, Poland.
4 Jagiellonian University Medical College, Chair of Microbiology, Cracow, Poland.

Corresponding author:
Wiktor Kostecki
62-71 60Th Street
Ridgewood, NY 11385
USA
Phone: +1 347-614-9741
e-mail: wikkos17@gmail.com

To cite this article: Kostecki W, Kupniewski K, Crain V, Mann MR, Płońska M, Zeng L, Golińska E, Pietrzyk A, Kochan P. Are bearded doctors dangerous? Are smartphones and credit cards safe? The importance of hygiene and object disinfection around hospital and private practice settings as well as the public environment. World J Med Images Videos Cases 2021; 7:e1-19.

Submitted for publication: 3 December 2020
Accepted for publication: 18 January 2021
Published on: 31 January 2021







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