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Bacterial contamination of the smartphones of healthcare workers in a German tertiary-care hospital before and during the COVID-19 pandemic

  • Author Footnotes
    These authors contributed equally to this work.
    Romy Tannhäuser
    Footnotes
    † These authors contributed equally to this work.
    Affiliations
    Department of Medical Microbiology and Molecular Diagnostics, Central Medical Laboratory, Hospital St. Georg, Leipzig, Germany

    Department of Infectious Diseases/Tropical Medicine, Nephrology and Rheumatology, Hospital St. Georg, Leipzig, Germany
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  • Author Footnotes
    These authors contributed equally to this work.
    Olaf Nickel
    Footnotes
    † These authors contributed equally to this work.
    Affiliations
    Department of Medical Microbiology and Molecular Diagnostics, Central Medical Laboratory, Hospital St. Georg, Leipzig, Germany
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  • Margareta Lindner
    Affiliations
    Department of Medical Microbiology and Molecular Diagnostics, Central Medical Laboratory, Hospital St. Georg, Leipzig, Germany
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  • Angela Bethge
    Affiliations
    Department of Medical Microbiology and Molecular Diagnostics, Central Medical Laboratory, Hospital St. Georg, Leipzig, Germany
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  • Johannes Wolf
    Affiliations
    Department of Medical Microbiology and Molecular Diagnostics, Central Medical Laboratory, Hospital St. Georg, Leipzig, Germany

    Jeffrey Modell Diagnostic and Research Center for Primary Immunodeficiency Diseases, Immuno Deficiency Center Leipzig (IDCL) at Hospital St. Georg, Leipzig, Germany
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  • Stephan Borte
    Affiliations
    Department of Medical Microbiology and Molecular Diagnostics, Central Medical Laboratory, Hospital St. Georg, Leipzig, Germany

    Jeffrey Modell Diagnostic and Research Center for Primary Immunodeficiency Diseases, Immuno Deficiency Center Leipzig (IDCL) at Hospital St. Georg, Leipzig, Germany

    Department of Laboratory Medicine, Division of Clinical Immunology, Karolinska Institutet, Stockholm, Sweden
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  • Christoph Lübbert
    Correspondence
    Address correspondence to Christoph Lübbert, MD, PhD, DTM&H, Division of Infectious Diseases and Tropical Medicine, Department of Medicine II, Leipzig University Hospital, Liebigstr. 20, D-04103 Leipzig, Germany.
    Affiliations
    Department of Infectious Diseases/Tropical Medicine, Nephrology and Rheumatology, Hospital St. Georg, Leipzig, Germany

    Division of Infectious Diseases and Tropical Medicine, Department of Medicine II, Leipzig University Hospital, Leipzig, Germany

    Interdisciplinary Center for Infectious Diseases, Leipzig University Hospital, Leipzig, Germany
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  • Author Footnotes
    These authors contributed equally to this work.
Published:October 16, 2021DOI:https://doi.org/10.1016/j.ajic.2021.09.025

      Highlights

      • Bacterial contamination was present on 99.3% of the smartphone screens of HCWs.
      • The proportion of bacterial pathogens ranged from 21.2% in 2012 to 39.8% in 2021.
      • Multidrug-resistant bacteria such as MRSA and VRE accounted for less than 2%.
      • Hence, smartphones must be carefully disinfected after handling in healthcare.
      • Cleaning intensity increased over time, probably due to the COVID-19 pandemic.

      Abstract

      Background

      Assuming that hygiene measures have improved significantly due to COVID-19, we aimed to investigate bacterial colonization on smartphones (SPs) owned by healthcare workers (HCWs) before and during the pandemic.

      Methods

      Employing a before-and-after study design, randomly selected HCWs were included. Devices underwent sampling under real-life conditions, without prior manipulation. Swabs were collected in 2012 (pre-pandemic) and 2021 to determine microbial colonization. Isolates were identified by MALDI-TOF mass spectrometry and underwent microbiological susceptibility testing.

      Results

      The final analysis included 295 HCWs (67% female, mean age 34 years) from 26 wards. Bacterial contamination was present on 293 of 295 SP screens (99.3%). The proportion of clinically relevant bacterial pathogens (eg Staphylococcus aureus, enterococci, Enterobacterales, non-fermenting bacteria) ranged from 21.2% in 2012 to 39.8% in 2021. Resistance profiles revealed a proportion of multidrug-resistant bacteria such as MRSA and VRE of less than 2%. The comparison of before-and-after sampling showed a significant increase in smartphone use during work from 2012 to 2021 with a simultaneous increase in cleaning intensity, probably as a result of the COVID-19 pandemic.

      Conclusions

      Bacterial contamination of SPs within the hospital is of concern and can serve as a source of cross-contamination. Hence, in addition to excellent hand hygiene, SPs must be carefully disinfected after handling in healthcare. Behavioral changes related to the COVID-19 pandemic could have a significant impact if implemented sustainably in everyday clinical practice.

      Key Words

      Introduction

      Mobile communication devices, especially smartphones (SPs), have become an essential part of everyday life. The number of SP users in Germany exceeded 60 million in 2020.

      Koptyug E. Number of smartphone users in Germany 2009-2020. Available at: https://www.statista.com/statistics/461801/number-of-smartphone-users-in-germany/. Accessed May 8, 2021.

      Despite their frequent usage, most people, even healthcare workers (HCWs), often ignore the possibility of these devices accumulating and transmitting a variety of microorganisms, in particular during and after patient care.
      • Simmonds R
      • Lee D
      • Hayhurst E
      Mobile phones as fomites for potential pathogens in hospitals: microbiome analysis reveals hidden contaminants.
      ,
      • Huffman S
      • Webb C
      • Spina SP
      Investigation into the cleaning methods of smartphones and wearables from infectious contamination in a patient care environment (I-SWIPE).
      In German hospitals, about 400,000 to 600,000 nosocomial infections occur annually, of which, according to large independent epidemiological studies, approximately 80,000 to 180,000 could be avoided every year.
      • Gastmeier P
      • Brunkhorst F
      • Schrappe M
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      [How many nosocomial infections are avoidable?].
      Awareness of well-described risk factors such as the use of catheters and other invasive equipment
      • Vincent JL
      Nosocomial infections in adult intensive-care units.
      and adherence to simple preventive measures, especially adequate hand hygiene,
      • Allegranzi B
      • Pittet D
      Role of hand hygiene in healthcare-associated infection prevention.
      ,
      • Pittet D
      • Allegranzi B
      • Boyce J
      The world health organization guidelines on hand hygiene in health care and their consensus recommendations.
      can significantly limit the burden of disease. Given the importance that hospital surfaces play in the transmission of emerging pathogens in healthcare,
      • Wolfensberger A
      • Clack L
      • Kuster SP
      • et al.
      Transfer of pathogens to and from patients, healthcare providers, and medical devices during care activity-a systematic review and meta-analysis.
      • Muller MP
      • MacDougall C
      • Lim M
      • et al.
      Antimicrobial surfaces to prevent healthcare-associated infections: a systematic review.
      • Weber DJ
      • Rutala WA
      • Miller MB
      • et al.
      Role of hospital surfaces in the transmission of emerging health care-associated pathogens: norovirus, clostridium difficile, and acinetobacter species.
      this underlines the role of SPs as a potential source of cross-contamination.
      The ongoing coronavirus disease 2019 (COVID-19) pandemic has drawn tremendous public attention to improving basic hygiene.
      • Kampf G
      • Brüggemann Y
      • Kaba HEJ
      • et al.
      Potential sources, modes of transmission and effectiveness of prevention measures against SARS-CoV-2.
      General hygiene rules in the population in Germany have been established by the Robert Koch Institute and the Federal Ministry of Labor and Social Affairs.

      Robert Koch Institute. Empfehlungen des RKI zu Hygienemaßnahmen im Rahmen der Behandlung und Pflege von Patienten mit einer Infektion durch SARS-CoV-2. Available at: https://www.rki.de/DE/Content/InfAZ/N/Neuartiges_Coronavirus/Hygiene.html. Accessed May 11, 2021.

      ,

      German Federal Ministry of Labor and Social Affairs. SARS-CoV-2-Arbeitsschutzstandard. Available at: https://www.bmas.de/SharedDocs/Downloads/DE/Arbeitsschutz/sars-cov-2-arbeitsschutzstandard.pdf. Accessed May 11, 2021.

      Assuming that hygiene measures have improved significantly due to COVID-19, we aimed to investigate the frequency and intensity of bacterial colonization on SPs owned by HCWs before and during the pandemic at our institution, employing a before-and-after study design.

      Methods

      Study design and participants

      This prospective before-and-after study included HCWs who used private SPs during their daily clinical practice. All HCWs from clinical departments qualified for the study. The years 2012 (pre-pandemic cohort) and 2021 (during the second wave of the COVID-19 pandemic in Germany) were set as sampling periods.

      Setting

      The Hospital St. Georg in Leipzig, Saxony, Germany, is a large tertiary-care hospital with 1,066 beds and 25 different specialist areas and clinics, embedded in the structure of a modern academic teaching hospital. The healthcare personnel comprises approximately 3,400 employees.

      Sampling and data collection

      Sampling followed a standardized procedure (Fig 1). First, participants received detailed information about the study. After providing voluntary written informed consent, privately owned SPs, which were also used during work in the hospital, were retrieved for microbiological testing. In particular, no purification procedures were performed. All sampling was done by the same investigator to ensure consistency. After hygienic hand disinfection, the investigator wiped the SP screen with a COPAN eSwab (COPAN, Brescia, Italy) which was moistened with the Amies transport medium from the swab tube before. After this procedure, the swab was immediately transferred to a Brain-Heart-Infusion (BHI) tube (Merck, Darmstadt, Germany). At the same time, participants filled out a detailed questionnaire with information on age, gender, affiliation, focus of activity, SP use, and further professional biography details.
      Fig 1
      Fig 1Flowchart for sample collection on SPs and microbiological processing of collected materials. First, the SP was swabbed with a COPAN brush. Second, a Brain-Heart-Infusion media tube was inoculated, followed by subculturing with a dilution spreading technique employing unselective and selective growth media. Species identification was performed by MALDI-TOF mass spectrometry, and multidrug-resistance was confirmed by specific PCR.

      Microbiological approach

      After transport to our microbiology laboratory on site, BHI tubes were incubated at 36°C for 24 hours. Clear BHI tubes were incubated for further 5 days. Aerobic and anaerobic subcultures were grown from turbid BHI tubes. Subculturing included media for aerobic bacteria, anaerobic spore formers, and fungi, comprising Columbia CNA agar (bioMérieux, Nürtingen, Germany), Gram-negative selective endo agar (Becton Dickinson, Heidelberg, Germany), Schaedler Kanamycin-Vancomycin (KV) anaerobic agar (Becton Dickinson), and Sabouraud Gentamicin-Chloramphenicol (SAB) agar (bioMérieux). In addition, selective plates were inoculated for the culturing of multidrug-resistant pathogens employing chromID MRSA/ESBL/VRE agars (bioMérieux) and Brilliance CRE agar (ThermoFisher Scientific, Waltham, Massachusetts, USA). Species were identified using VITEK Matrix Assisted Laser Desorption Ionization—Time of Flight Mass Spectrometry (MALDI-TOF-MS, bioMérieux) and VITEK 2 system (bioMérieux). For further typing, microscopic and biochemical methods (coagulase, catalase, and oxidase tests), an ESBL/AmpC test (MAST Diagnostica, Reinfeld, Germany), and specific polymerase chain reactions (PCR) for MRSA (Xpert MRSA NxG, detecting mecA and mecC genes) and VRE (Xpert van A/van B, detecting vanA and vanB genes) (both Cepheid, Sunnyvale, California, USA) were applied (Fig 1). All multidrug resistant isolates underwent semi-automated antimicrobial susceptibility testing using the VITEK 2 system (bioMérieux), with respect of the current breakpoints according to EUCAST (European Committee on Antimicrobial Susceptibility Testing, www.eucast.org).

      European Committee on Antimicrobial Susceptibility Testing (EUCAST). Breakpoint tables for interpretation of MICs and zone diameters. Available at: https://eucast.org/clinical_breakpoints/. Accessed May 22, 2021.

      Statistical analysis

      The statistical analysis was performed using SPSS for Windows (SPSS 23.0, IBM Corporation, Armonk, New York, USA). Numerical variables were summarized as mean, and categorical variables were given as frequencies or proportions. Categorical data became dichotomized in case of more than two expressions and were analyzed by the Fisher's exact test. P values (two-sided) <.05 were considered statistically significant.

      Ethics approval

      The study was conducted in accordance with the ethical guidelines of the 1964 Declaration of Helsinki and its later amendments and was approved by the local ethics committee (Saxonian Board of Physicians, Dresden, Germany, vote EK-BR-18/21-1).

      Results

      Sociodemographic data

      Two hundred and ninety-five HCWs (67% female; mean age 34 years) from 26 wards comprising 19 different specialties were included in the final analysis (Fig 2, Table 1).
      Table 1Baseline data of the participants and responses to questionnaires in 2012 and 2021
      20122021P value
      Number of investigated SPs101196
      Number of SPs from fully evaluable participants (%)99 (98)196 (100)
      Females (%)60 (60.6)138 (70.4).115
      Median age (range)30 (18-63)36 (18-63)
      18–25 ys (%)30 (30.3)39 (19.9).001
      26–35 ys (%)37 (37.4)51 (26)
      36–45 ys (%)17 (17.2)46 (23.5)
      46–55 ys (%)14 (14.1)38 (19.4)
      >55 ys (%)1 (1)22 (11.2)
      Peripheral ward (%)22 (22.2)83 (42.3).001
      ICU/IMC/stroke unit (%)43 (43.4)46 (23.5)
      Multiple locations (%)15 (15.2)29 (14.8)
      Other clinical areas (%)19 (19.2)38 (19.4)
      Nurse (%)60 (60.6)130 (66.3).488
      Physician (%)29 (29.3)45 (23)
      Other professions (%)10 (10.1)21 (10.7)
      Internal medicine (%)48 (48.5)93 (47.4).01
      Surgical disciplines (%)32 (32.3)38 (19.4)
      Interdisciplinary (%)19 (19.2)65 (33.2)
      SP cleaning at a fixed interval, daily or more frequently (%)23 (23.2)90 (45.9)<.001
      SP cleaning without a fixed interval (%)68 (68.7)99 (50.5)
      No SP cleaning (%)8 (8.1)7 (3.6)
      SP storage in a workwear pocket (%)39 (39.4)136 (69.4)<.001
      SP storage on the ward (%)50 (50.5)56 (28.6)
      SP storage not on the ward (%)10 (10.1)4 (2)
      The participation rate of 63.4% (196 of 309) in the pandemic year 2021 was significantly higher than in 2012 (101 of 624, 16.2%; P <.001).

      Microbiological contamination of SPs

      A microbiological analysis was carried out on a total of 295 SPs from fully evaluable participants (99 in 2012, and 196 in 2021), supplemented by 4 negative controls which were freshly decontaminated before the analysis. Bacterial growth was detected on 293 out of 295 devices analyzed (99.3%). No microorganisms were detected on the 4 SPs serving as controls. Coagulase-negative staphylococci (CNS) were the most common isolate group detected in both study periods (Fig 3).
      Fig 3
      Fig 3Comparison of bacterial contamination of SPs in 2012 versus 2021 (during the second wave of the COVID-19 pandemic).
      In 2012, 80 of 99 SPs (80.8%), and in 2021, 147 of 196 SPs (75%) carried this group of bacteria (P = .307). Frequently detected representatives of this group were Staphylococcus (S.) lugdunensis, S. hominis, S. epidermidis, S. warneri, S. capitis, and S. haemolyticus. Spore-forming aerobic bacteria represented the second largest group of bacteria detected on SPs. Among them, Bacillus cereus was identified most frequently, followed by Lysinibacillus fusiformis and Lysinibacillus sphaericus. In contrast to CNS, significantly more spore-forming aerobic bacteria were detected in 2021 (130 of 196, 66.3%) than in 2012 (37 of 99, 37.4%; P <.001). Polymicrobial contamination was detected on 54 of 99 SPs (54.5%) in 2012, and on 155 of 196 SPs (79.1%) in 2021 (P =.003) (Table 2).
      Table 2Bacterial species detected on SP screens and their clinical relevance regarding nosocomial infections
      20122021P value
      Number of SPs from fully evaluable participants (%)99 (98)196 (100)
      Monomicrobial colonization (%)44 (44.4)40 (20.4)<.001
      Polymicrobial colonization, ≤3 species (%)53 (53.5)140 (71.5).003
      Polymicrobial colonization, >3 species (%)1 (1)15 (7.6).002
      No bacterial growth (%)1 (1)1 (0.5).0
      Gram-positive bacteria (%)97 (98)194 (99).6
      Gram-negative bacteria (%)12 (12.1)30 (15.3).6
      Staphylococcus aureus (%)8 (8.1)26 (13.3).247
      MSSA8 (8.123 (11.7)
      − MRSA0 (0)3 (1.5)
      Coagulase-negative staphylococci (CNS) (%)80 (80.8)147 (75).307
      Other Gram-positive cocci (%)6 (6.1)5 (2.6).19
      Lactococcus lactis0 (0)4 (2.0)
      − Micrococcus spp.6 (6.1)1 (0.5)
      Viridans streptococci (%)1 (1.0)34 (17.3)<.001
      S. sanguinis1 (1.0)12 (6.1)
      − S. parasanguinis0 (0)13 (6.6)
      − S. mitis0 (0)8 (4.1)
      − S. suis0 (0)1 (0.5)
      Streptococcus agalactiae (%)0 (0)1 (0.5).0
      Enterococcus spp. (%)3 (3)35 (17.8)<.001
      E. faecalis2 (2)27 (13.8)
      − E. durans1 (1)0 (0)
      − E. faecium0 (0)6 (3.1)
      − E. faecalis (VRE)0 (0)1 (0.5)
      − E. faecium (VRE)0 (0)1 (0.5)
      Spore-forming aerobic bacteria (%)37 (37.4)130 (66.3)<.001
      Enterobacterales (%)8 (8.1)25 (12.7).616
      − Enterobacter cloacae1 (1.0)4 (2.0)
      − Enterobacter spp.0 (0)2 (1.0)
      − Escherichia coli0 (0)4 (2)
      − Klebsiella oxytoca0 (0)2 (1)
      − Pantoea spp.4 (4)12 (8.1)
      − Leclercia adecarboxylata3 (3)1 (0.5)
      Non-fermenting bacteria (%)4 (4)8 (4.1).0
      Pseudomonas spp.0 (0)2 (1)
      − Acinetobacter baumannii3 (3)6 (3.1)
      − Sphingomonas paucimobilis1 (1)0 (0)
      SPs with detection of clinically relevant pathogens (%)21 (21.2)78 (39.8).002
      Staphylococcus aureus (MRSA/MSSA)8 (8.1)26 (13.3)
      Enterococci3 (3)35 (17.8)
      Enterobacterales8 (8.1)25 (12.7)
      Non-fermenting bacteria4 (4)8 (4.1)
      SPs with detection of commensal bacteria (%)94 (94.9)183 (93.4).8
      Coagulase-negative staphylococci (CNS)80 (80.8)147 (75)
      Spore-forming aerobic bacteria37 (37.4)130 (66.3)
      Corynebacterium spp.3 (3)0 (0)
      Viridans streptococci1 (0)34 (17.3)
      Streptococcus agalactiae0 (0)1 (0.5)
      Other Gram-positive cocci6 (6.1)5 (2.6)
      In principle, almost all bacteria detected can cause infections in critically ill patients, especially those with immunosuppression. As clinically relevant pathogens, we defined bacteria that are not expected to be detectable on SP screens and whose presence is likely due to smear infection, (eg enterococci, Enterobacterales, and non-fermenting bacteria), but also bacteria well known to cause severe infections in critically ill patients, such as S. aureus. In 2012, the proportion of SPs with detection of clinically relevant pathogens (21 of 99, 21.2%) was significantly lower than in 2021 (78 of 196, 39.8%; P =.002) (Fig 4).
      Fig 4
      Fig 4Detection of clinically relevant bacterial pathogens with high relevance for nosocomial infections on SPs.
      Methicillin-resistant S. aureus (MRSA) was not detected in 2012, but on 3 SPs (1.5%) in 2021. Also a higher rate of enterococci were detected on SPs in 2021 (35 out of 196, 17.8%) compared to 2012 (3 out of 99, 3.3%; P <.001). In the 2012 study period, no vancomycin-resistant enterococci (VRE) were detected either, but in 2 of 196 SPs (1%) in 2021. No yeasts were detected on Sabouraud agar plates in 2012 or 2021, respectively. Furthermore, there was no detection of anaerobically growing bacteria on Schaedler plates, as well as no microbiological evidence of Gram-negative bacteria producing extended spectrum beta-lactamases (ESBLs) in either period of study.

      Data from questionnaires

      The responses to the questionnaires showed a statistically relevant difference between the surveys in 2012 and 2021 with regard to the storage behavior of SPs during working hours (Table 1). In 2012, 39 out of 99 respondents (39.4%) stated that they always carry the SP with them while working compared to 136 out of 196 (69.4%; P <.001) in 2021. In 2012, only 23 out of 99 respondents (23.2%) said they cleaned their SP on a daily or less frequent basis. In 2021, the number rose significantly to 90 of 196 (45.9%; P <.001). In 2012, 68 out of 99 participants (68.7%) stated to clean their SP only when it is obviously contaminated. In 2021, the respective number dropped to 99 from 196 (50.5%; P <.001). In 2012, 8 out of 99 respondents (8.1%) reported no cleaning procedures at all, and in 2021 the respective numbers were 7 out of 196 (3.6%; P <.001). No statistically relevant differences could be found within different subgroups.

      Discussion

      In this study among 295 HCWs from 26 different wards, we could show that 99.3% of SP screens were bacterially contaminated. The proportion of clinically relevant bacterial pathogens ranged from 21.2% in 2012 to 39.8% in 2021. The comparison of before-and-after sampling showed a significant increase in smartphone use during work from 2012 to 2021 with a simultaneous increase in cleaning intensity, probably as a result of the COVID-19 pandemic.
      Our study yielded data comparable to previous studies with regard to the contamination rate as well as the bacterial spectrum.
      • Brady RR
      • Verran J
      • Damani NN
      • et al.
      Review of mobile communication devices as potential reservoirs of nosocomial pathogens.
      The questionnaire evaluation regarding hand hygiene and specific SP hygiene showed that careful disinfecting cleaning of SPs in 2012 was internalized by two thirds of the study participants as not necessary if there was no visible contamination. By repeating sampling in the same cohort during the second wave of the COVID-19 pandemic, we were able to demonstrate the effects of improved general hygiene measures. The significantly increased participation rate during the pandemic (63.4% in 2021 vs 16.2% in 2012; P <.001) also fits in with this improved awareness.
      As predicted in 2012, the popularity of smartphones has increased massively over the past ten years.

      Koptyug E. Number of smartphone users in Germany 2009-2020. Available at: https://www.statista.com/statistics/461801/number-of-smartphone-users-in-germany/. Accessed May 8, 2021.

      The Bring-Your-Own-Device (BYOD) concept to hospitals illustrates the implementation of these devices in everyday clinical practice. A wide range of applications, also for clinical questions in the medical field, is available (eg medical risk score calculators, antibiotics and medication guides, digital reference works).
      • Payne KFB
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      Smartphone and medical related App use among medical students and junior doctors in the United Kingdom (UK): a regional survey.
      ,
      • Helou RI
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      Use of stewardship smartphone applications by physicians and prescribing of antimicrobials in hospitals: a systematic review.
      The increasing use of hospital-provided devices (Corporate Owned Personally Enabled [COPE] devices) connected to the hospital information system underscores their importance and shows that restricting the use of SPs and tablet computers would not work.
      • Khutsafalo K
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      ,
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      It is therefore not unexpected that a large number of our study participants stated that they also carry the SP with them at work, eg in pockets of their work clothing.
      Fifty percent of the study participants stated, even under the conditions of the COVID-19 pandemic, that they only clean the SP screen when it is clearly contaminated. This information from questionnaires indicates that SP hygiene is not sufficiently integrated into basic hygiene measures yet. Nevertheless, the rate of participants who stated that they did not clean their device at regular intervals in 2021 fell by more than 22% compared to 2012. At this time, according to manufacturer's recommendations, a dry microfiber fabric was often used to clean the SP surface, especially taking into account that electronic devices are subject to technical protection standards such as susceptibility to liquids. Since the liquid tightness of SPs has improved significantly since 2012, it is now less difficult to clean and disinfect a SP. Modern devices with special seals even withstand treatment with disinfectant solutions. In addition, special surface treatments, eg metal oxide solutions with antibacterial properties, are available. Smart alternative options, such as UV light for disinfection, however, are not generally in use.
      • Lisa M
      • Titus W
      • Emily R
      • et al.
      Evaluation of an ultraviolet C light–emitting device for disinfection of electronic devices.
      Bacterial contamination of SP surfaces is affected by various factors such as sebum, sweat, saliva, fat, food residues, and make-up.
      • Brady RR
      • Verran J
      • Damani NN
      • et al.
      Review of mobile communication devices as potential reservoirs of nosocomial pathogens.
      ,
      • Noumi E
      • Merghni A
      • Alreshidi M
      • et al.
      Phenotypic and genotypic characterization with MALDI-TOF-MS based identification of staphylococcus spp. isolated from mobile phones with their antibiotic susceptibility, biofilm formation, and adhesion properties.
      When comparing both study periods, the spectrum of bacteria was very similar. However, bacteria known for airborne transmission were detected more frequently in 2021, as well as polymicrobial contamination. In addition, the increased colonization rate with clinically relevant pathogens in 2021 may be attributed to different usage behavior and increased storage in a coat pocket during work itself. For instance, compared to the pre-pandemic study period, the rate of viridans streptococci was much higher in 2021. Taking into account that voice assistants have become a mega-trend in recent years,

      Petrock V. Voice assistant and smart speaker users 2020. Available at:https://www.emarketer.com/content/voice-assistant-and-smart-speaker-users-2020/. Accessed June 19, 2021.

      a growing detection rate for oral streptococci is not unexpected. However, wearing a mask while using the SP is a new condition under pandemic circumstances, suggesting that people are removing their face masks to make calls or record voice messages. Carrying the SP close to the body and high frequency of use lead to a possible increase in the temperature of the device, which is associated with an improvement in the replication conditions for bacteria. A recent study also analyzed the posterior surface of SPs. Interestingly, Kuriyama et al. found an even higher colonization rate on the posterior side of the SPs.
      • Kuriyama A
      • Fujii H
      • Hotta A
      • Asanuma R
      • Irie H
      Prevalence of bacterial contamination of touchscreens and posterior surfaces of smartphones owned by healthcare workers: a cross-sectional study.
      This underlines the immense importance of an adequate and complete cleaning at fixed intervals. This fact should be taken into account in future hygiene analyses of handheld devices.
      The fact that no yeasts could be detected in our study suggests that they are not part of the normal skin flora. Multidrug-resistant Gram-positive pathogens such as MRSA and VRE were detected in less than 2% of the isolates, and Gram-negative ESBL-producers were not detected at all. This could indicate that hygiene measures are particularly consistently adhered to when patients are known to be colonized with multidrug-resistant organisms.

      Limitations

      The main limitations of this study result from the monocentric design and the medium-sized cohort (n = 295) with limited statistical power. Due to the eight-year interval between the two study periods, there were changes in the baseline characteristics of the two cohorts analyzed. These differences mainly result from the fact that the majority of the study participants were the same in both study periods, but 8 years older. In addition, there was no control group outside the hospital. Thus, our findings are rather descriptive. Since only bacterial and fungal contamination was investigated, no statement can be made about the viral load on SP screens. Furthermore, compliance with hand hygiene in HCWs in the study cohort was only queried, but not systematically observed. Social desirability as a possible influencing factor has to be considered when questionnaires were filled out directly.
      Depending on the SP manufacturer, type of SP, material, software and usage behavior, there are differently frequented areas on SP touchscreens, which is why we opted for a semi-quantitative identification process by wiping the entire touchscreen and culturing in BHI. Due to the different growth behavior, suboptimal growth of anaerobic bacteria is possible and must be taken into account. A possible quantitative bias in the bacterial load is conceivable due to the enlarged surface structure of the COPAN brushes used in 2021. Improved routine usage of MALDI-TOF mass spectrometry for bacterial identification could have led to a qualitative bias in differentiation down to the species level in 2021. Only the front screens of SPs were analyzed. No statements can be made about hygienically relevant colonization rates on the posterior side of the SPs.

      Conclusion

      Bacterial contamination of SPs occurs before and after patient contact and can serve as a source of cross-contamination. Hence, in addition to excellent hand hygiene, SPs must be carefully disinfected after handling in healthcare. Behavioral changes related to the COVID-19 pandemic could have a significant impact if implemented sustainably in everyday clinical practice.

      Acknowledgments

      The authors gratefully acknowledge Thomas Grünewald for his valuable input and clinical support.

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