Radiology Department: A Potential Source of Multidrug-Resistant Microorganisms: A Cross-Sectional Study at Tertiary Hospital, Palestine

Introduction Globally, healthcare facilities face a great challenge in the form of hospital-acquired infections (HAIs). Aside from the morbidity and mortality they cause, these illnesses are also extremely costly. Research on infection transmission in the medical field has been considerable, but not so much in the radiology department. Aim This study aims to identify the presence of multidrug-resistant (MDR) microbes on surfaces that are frequently touched in computed tomography (CT), magnetic resonance imaging (MRI), ultrasound (US), plain X-ray examination rooms, and portable radiography that are susceptible to contamination as well as to investigate the potential dangers of contracting MDR organisms to patients and healthcare providers. Materials and Method. In this study, 160 swab samples were collected from the radiology department during May and June 2022. Samples were obtained from 80 predefined surfaces twice within and outside of CT and MRI examination rooms as well as from US and plain X-ray machines and portable X-ray machines. Samples were taken at 7:00 a.m. using cotton swabs following the regular cleaning procedure. Bacterial colony-forming units (CFUs) per square centimeter were calculated after swabbing a 100 cm2 surface. Results Nearly all of the surfaces tested had bacterial CFUs. The highest contamination rate was found on keyboards ranging from (1.2–8) CFU/cm2, the sides of patient tables (1.2–20) CFU/cm2, knee coil (2.4–3) CFU/cm2, and patient leg supports (1.2–8) CFU/cm2. A noticeable increase in the contamination was noticed in June compared to May, and this was consistent with the increase in the number of isolated patients in the hospital, the workload in the radiology department, and the number of patients referred to the hospital. In our study, none of the examined sites showed contamination with MDR Gram-negative bacteria such as extended-spectrum beta-lactamases producing Enterobacterales (ESPL) or Carbapenemase-producing Enterobacterales (CPE). On the other hand, methicillin-resistant Staphylococcus (MRS), vancomycin-resistant Staphylococcus (VRS), and vancomycin-resistant Enterococcus (VRE) were detected. Conclusion All of the radiology department equipment and sites could be a source of bacterial infection including MDR, so the obligatory and committed disinfection protocol must be revised and implemented in the morning and between patients.


Introduction
Tese days, the importance of infection control and prevention in health care centers cannot be overstated.Hospitals and health care centres often have surfaces contaminated with microorganisms, which can lead to serious healthcare-associated infections (HAIs) afecting both patients and health care workers.While it is well established that HAIa can cause serious diseases, there are still gaps in our understanding of how these bacteria are transmitted to patients.Tis gap underscores the critical importance of strict hygiene protocols and infection control measures within hospital and health care centre settings to reduce the risk of HAIs [1].
Te radiology department and the use of diferent radiological equipment, including computed tomography (CT), magnetic resonance imaging (MRI), ultrasound (US), plain Xrays, and portable X-ray machines, have a vital role in diagnosing and monitoring diferent conditions [2,3].Crosscontamination is a critical concern in this area since patients are transferred to the radiology department from various clinics and departments with a wide spectrum of medical conditions.Tese patients' susceptibility to illness is already high due to their underlying medical conditions.Because these patients may come into direct or indirect contact with health care workers (HCWs) and contaminated surfaces and equipment, the risk of nosocomial infection transmission among them increases, making them vulnerable to HAIs [3,4].
In recent years, the incidence of HAIs in radiology departments has witnessed a concerning increase.Tese infections jeopardize the safety of both HCWs and patients, further complicating radiographic investigation or intervention [5,6].
HAIs are commonly referred to as nosocomial infections, which are defned as infections acquired within 48 hours of admission to a healthcare facility [6,7].In contrast to community-acquired infections (CAIs), these infections usually occur as a result of pathogens taking advantage of patients whose normal defenses against infection are compromised [3].Extensive literature has highlighted the Centres for Disease Control and Prevention's (CDC) classifcation of nosocomial infection sites into 13 types with up to 50 infection sites [8].Tese infections put hospitalized patients at a big risk, leading to signifcant morbidity and mortality, particularly in lowincome countries rather than in high-income countries around the world [4,7,9].
High-touch surfaces in patient rooms, such as bed controls, bed rallies, call buttons, and bedside tray tables, represent a critically important multidrug-resistant organism (MDRO) reservoir and increase the risk of acquisition by other patients, visitors, and hospital staf who are exposed to them.Te presence of MDR bacteria within hospital settings poses a signifcant threat that extends to the selection of empiric antibiotics that target MDR bacteria.Tis can perpetuate a vicious cycle of increasing antimicrobial resistance [2,10,11].
Several studies have demonstrated that disinfection plays a signifcant role in controlling microbial carriage in people who are not harboring MDROs.Beyond disinfection, there are several essential infection prevention methods, such as environmental cleaning, hand hygiene, contact precautions, and active screening.Disinfection ofers a universal solution by safeguarding both MDRO carriers and noncarriers [12].
Disinfection is becoming increasingly signifcant in most hospitals because the number of patients harboring MDROs asymptomatically is growing over time [13].Increased research on MDROs persistence in the hospital environment and subsequent transmission has recently resulted in a greater emphasis on hospital environmental hygiene [14][15][16].
In a recent study, cleaning surfaces by using a sodium lauryl sulfate-based detergent can prevent MRSA transmission in health-care settings and reduce the risk of surface contamination at hospitals in general and radiology departments in particular [18].In a previous investigation involving bacterial detection, samples were obtained from CT equipment, and the results indicated that the CT wrap was the most contaminated with germs, prompting the development of a novel cleaning procedure [6].
Te real pandemic outbreak of COVID-19, which killed several million people and had major global economic consequences, is an indication that much more work is necessary to tackle infectious diseases and the growing global issue of antibiotic resistance [19].In the case of hospitalized patients, the case-fatality rate linked with bacteremia ranges from 35% to 50% and is usually associated with MDR Gramnegative bacteria such as ESBL and CRE [20].
Globally, prevalent carbapenemases are found in Enterobacteriaceae, including Klebsiella pneumoniae carbapenemases (KPC) [21].K. pneumoniae, which produces KPC, is a worldwide threat [22].In a recent study, bacterial contamination was found in almost all selected areas in the radiology department, including MRI and CT equipment; fortunately, no MDROs such as MRSA, ESPL, or CPE were detected [7].
Te spread of MDROs and HAIs presents a major challenge to the global healthcare community especially developing countries, as they have much higher risks of HCAIs with a ratio of 20 : 1 as compared to developed countries [23].
Tis cross-sectional study was conducted at a tertiary hospital in Palestine, where we investigated the presence of multidrug-resistant organisms on highly touched surfaces in the radiology department as well as the potential danger of patients and healthcare workers contracting multidrugresistant organisms.Swab samples were taken from the commonly hand-touched sites in the department of radiology and cultured at a microbiology lab.Antimicrobial resistance was tested.

Study Design.
A cross-sectional study design was carried over at the radiology department at Tertiary Hospital, Palestine.

Study Population.
Te commonly hand-touched sites were assessed according to the previous studies [7], and an adapted fow chart was created.Briefy, swab samples Antibiotics used in this study were purchased from Sigma Aldrich, while the media were purchased from Oxoid.Media with antibiotics were prepared as described in the Clinical and Laboratory Standard Institute (CLSI) 2021 and as described in the literature [24,25].
All plates were incubated at 37 degree/24 hours aerobically, while chocolate agar plates were incubated in 5% CO 2.
American Type Culture Collection (ATCC) strains (E. coli ATCC 25922 and S. aureus ATCC 25923) and clinically confrmed strains (MRSA, ESBL, CRE and VRE) were used as controls for the prepared media in each preparation.
Finally, all the identifed multidrug-resistant isolates were confrmed as such through antibiotic susceptibility testing, following the CLSI protocols.

Vancomycin Resistance.
Te screening method was used to detect vancomycin resistance.In short, bile esculin media was prepared with a concentration of 6 µg/ml; further confrmation was approached through E-test.E test was applied for those strains that needed to be screened for vancomycin sensitivity: MRS detected using MSA + oxacillin and colonies grown on bile esculin agar with vancomycin.

Contamination Rate Calculation.
Simply put each commonly encountered site in our study was swabbed with a sterile, premoistened PBS swab, targeting a 100 cm 2 (10 cm * 10 cm) area.After swabbing, the swab was placed in an already prepared falcon tube containing 2 ml sterile PBS, vortexed well, and 100 µl was transferred and cultivated on the prepared media's surface.
Following the incubation period, colonies on each plate were counted, and the fndings were given as CFU/cm 2 , taking the swabbed area and volume of PBS bufer in the tubes into account (calculation CFU/cm 2 : counted colonies number * 0.2), as shown in Table S3.

Ethical Approval. Ethical approval was taken from the institutional review board (IRB) at An-Najah National
University and An-Najah National University Hospital.

Bacterial Detection.
Bacterial growth was nearly detected in all targeted sites.Regarding samples collected in May, bacterial growth was detected in 49/80 sites.Samples collected in June showed growth in 52/80 sites.Interestingly, in total, 60/80 sites showed bacterial growth as shown in Tables S1 and S2.
In the radiology department as well as all other inanimate objects, Gram-positive bacteria are predominant in and out of CT, MRI, plain X-ray, US rooms, and portable Xray, while Gram-negative was only detected in four sites, as shown in Tables S1 and S2.

3.3.
Gram-Positive: Staphylococcus (MSA-Growth).Concerning contamination with bacteria that can grow on MSA which is mainly Staphylococcus, in May, out of 80 sites examined, 9 sites had a contamination rate of ≥1 CFUs/cm 2 , while in June, 18 sites were considered contaminated.In total, 19 sites showed contamination of ≥1 CFUs/cm 2 , as shown in Table 3.

Gram-Positive: MRS.
Regarding the surface contamination with MRS, six sites in May and 13 sites in June showed growth on MSA + oxacillin, which means MRS is suspected to be present.Later on, all suspected colonies were Canadian Journal of Infectious Diseases and Medical Microbiology   Canadian Journal of Infectious Diseases and Medical Microbiology confrmed as MRS after subculture, and cefoxitin resistance was demonstrated by the disk difusion method.Out of 13 sites, only one site had a contamination rate ≥1 CFUs/cm 2 in June and none in May.However, the site with a contamination rate ≥1 CFUs/cm 2 is the centre of the patient table of the CT Canon with 1.4 CFUs/cm 2 , as shown in Table 4.

Gram-Positive: Vancomycin-Resistant Staphylococcus (VRS).
After MRS detected and confrmed, all MRS isolates were tested for vancomycin sensitivity using E-test.In May, no VRS was detected, and all isolates were found to be vancomycin sensitive Staphylococcus.Surprisingly, in June, 7 out of 13 detected MRS were confrmed as VRS, namely,  and S2.
3.9.Contamination Rate.Because of the increasing number of patients and an increased number of referred patients in June, the contamination rate average of 1.3 CFUs/cm 2 is greater than in May 0.79 CFUs/cm 2 , as shown in S1 and S2 Tables, while for the study period (May and June), no differences were noticed in the disinfectant materials used to disinfect the surfaces, the time, and frequency at which the surfaces were cleaned.
Growth conditions afect the contamination rate, as the data shown in Table S3, the contamination rate on chocolate agar was higher than the contamination rate on blood agar for almost all sites during the two cohorts.Chocolate agar has a higher contamination rate than blood agar mostly because chocolate agar contains lysed red blood cells with better growth for fastidious organisms and due to the fact that chocolate agar plates were incubated in an anaerobic environment [26].
Te results showed a contamination median value greater than 3 CFU/cm 2 from seven common surface sites tested in the CT, MRI, US, and plain X-ray; centre and sides of the examination table X-ray patient's tables, knee coils, MRI patient's leg support, and all of the radiology machine keyboards.
Alarming fndings reveal that the highest contamination rate was found in the CT Canon's core of the patient table and the large touch screen of the US for general use, with 10 CFUs/cm 2 and 12.8 CFUs/cm 2 , respectively.Another alarming piece of data shows the high contamination rate on the right and left side of MRI patient (Table 2) MRI patient leg support 2, keyboard in the X-ray control room, left side of patient table of CT Canon, CT Siemen's keyboard in the control room, and keyboard and table of US for general use; in both cohorts, as shown in Table S3.

Discussions
Te fndings of our study indicate that Gram-positive bacteria were more detected in the radiology department than Gram-negative ones, and this was expected.Tis result is consistent with previous investigations that have found that Gram-positive were more common than Gram-negative bacteria on inanimate surfaces in the radiology department [7].It was demonstrated that Gram-positive bacteria have a stronger potential for surviving on inanimate surfaces and environment [27].Furthermore, Gram-positive bacteria also make up a signifcant portion of the skin's microbiota [28].In short, the higher occurrence of Gram-positive bacteria in the radiology department can be attributed to their survival characteristics and their presence on the skin.
In our study, the MRSA contamination rate on the inert surface was relatively high 28/160 (17.5%).On the other hand, in Sweden, swabs were taken from the bore, table, and wrap of two quaternary care inpatient CT scanners; the wrap was the most contaminated item on a CT scanner, and the prevalence of MRSA was signifcantly low [29].However, in another study in Ireland, from 125 samples collected from the radiology department, MRSA was detected from one sample only, bore in the MRI gantry [30].Canadian Journal of Infectious Diseases and Medical Microbiology However, in earlier research on cassettes and lead aprons carried out in radiology departments across the United Kingdom, there was no evidence of MRSA [2].In our research, no MRS was detected from the MRI gantry, but the other 27 samples taken from diferent sites of the radiology department's equipment were positive for MRS.MRSA was present on an X-ray cassette that had been utilized in the operation room [31].In addition, our investigation showed no evidence of MRS and bacterial contamination on the Xray cassette.
In general, the sample area makes up only a small portion of the overall surfaces, which may reduce the sensitivity of the test when attempting to identify resistant bacteria that are present in low numbers.In addition, the purpose of this investigation was to identify any contamination on the surfaces inside and outside the radiology examination rooms and equipment and determine whether they were more likely to be contaminated.In the majority of the CT, X-ray, and US examination rooms both inside and outside, as well as on the patient tables of the MRI machines, the keyboards contained a noticeable bacterial contamination rate that ranged 1-8 CFU/cm 2 .
Tis has additionally been shown to be the case in other research, as they showed that work station sites in the radiology department are 64.3%(9 of 14) contaminated with S. aureus and 21.4% (3 of 14) are contaminated with enteric organisms [7,32].It is probable that this is because medical staf members do not adequately disinfect their hands after dealing with the patient within the examination room or that they do not regularly disinfect the keyboards and patient tables.Both of these factors contribute to the spread of infection.Tere has been a lot of research on how important it is to practice good hand hygiene in order to prevent the spread of infection [33].
Te simplest, most efective, and least expensive strategy to prevent the spread of microorganisms is to practice strict hand cleanliness.In our study, a large number of CFU/cm 2 was found in most cases on the LT side of MRI patient (Table 2) the centre of patient table CT CANON, and the large touch screen for US for general use with 8.4, 10, and 12.8 CFUs/cm 2 ; respectively.One possible explanation is that the patients' clothing had been in contact with their bodies for at least 15 minutes and HCWs hands when dealing with patients during examination.In addition, the examination tables' sides of MRI, CT, and X-ray had contamination rates ranging from 1-8.4 CFU/cm 2 .Tis may be due to the fact that patients sit on the examination table with their skin in close contact with the side of the examination table.Te examination table's sides and centre, as well as the MRI knee coil and patient legs support, are most likely not thoroughly disinfected.In general, a large number of surfaces showed bacterial contamination that was higher than the permissible limit of one CFU/cm 2 .Meanwhile, other studies showed low numbers of CFUs/cm 2 on the side of the tunnel of the MRI camera in the radiology department [7] and a decrease in bacterial growth presence in the magnetic feld [34,35].
Te surfaces may not have been cleaned thoroughly enough, and this may be a cause of the infection.Tis could be the result of, for instance, an insufcient amount of staf education on infection management, or it could be because the cleaning is not efective.When deciding on a cleaning procedure, there are many factors to take into consideration.It should be efcient, but at the same time, it should not have any negative efects on either humans or the environment, and it should not be too expensive [36].
Alterations to cleaning procedures and the kind of materials used have varying efects on certain infections.A cleaning solution containing hydrogen peroxide is excellent against bacteria and viruses, but it is harmful to humans and cannot be used for continuous cleaning [37].
Self-disinfecting surfaces covered with copper and silver have also been studied, and this has been demonstrated to minimize HAI.For the pathogen, efciency, the environment, and the economy to all beneft from disinfection procedures, further research is needed [38].
In the radiology department, fortunately, we detected a low number of CFU/cm 2 approximately near zero CFU/ cm 2 on the side of the Siemens CT gantry, patient table of Xray, head coil MRI, surface coils of MRI, and probes for interventional ultrasonography compared to other sites in the MRI examination room, the side of the X-ray patient table, and probes of US for general use.Since patients contact this location practically every time they use these machines, it is highly unlikely that it is disinfected more regularly than other parts of the apparatus.
Concerning the efect that magnetic felds have on the number of bacteria present, additional research needs to be A previous study investigated the potential efect of a rotating magnetic feld against bacteria through cell wall disruption and changes in morphology [39].We were able to detect substantial diferences in the contamination between months of May and June in the radiology department.In June, patient isolation, workload, and the number of referrals for patients were all higher than in May.As a refection of that, the average contamination rate from all sites in June was 1.3 CFUs/cm 2 , while in May, it was 0.79 CFUs/cm 2 .Moreover, six sites showed contamination with MRS in May compared to 13 sites in June, with only one site in June having a contamination rate of ≥1 CFUs/cm 2 .Surprisingly, 7 sites showed contamination with VRS, and all were in June.Regarding contamination with Gram-negative bacteria, a contamination rate of ≥1 CFUs/cm 2 was detected only at one site in June.In addition to that, VRE was detected at one site in May with a contamination rate of <1 CFUs/cm 2 , while it was detected at four sites in June, with a contamination rate of ≥1 CFUs/cm 2 .
Based on our results, we can say that reducing contamination efectively in a healthcare setting, such as a radiology department, requires a comprehensive approach involving staf education, proper cleaning and disinfection protocols, and ongoing monitoring.We emphasize that hospital staf must be educated and trained regularly on proper hand hygiene techniques.We also propose implementing a regular cleaning schedule for all surfaces within the radiology department to ensure that cleaning includes high-touch areas like doorknobs, keyboards, phones, and equipment surfaces [40][41][42][43].
Another technique for infection control is the use of disposable barriers (e.g., plastic covers) on equipment surfaces that come into direct contact with patients.Tese can be changed between each patient, reducing the risk of crosscontamination [44].
Because patients and family members are a signifcant part of the contamination equation, we encourage educating patients about the importance of hand hygiene and covering coughs and sneezes to reduce the risk of spreading infections within the department [45].
We also encourage conducting regular audits and assessments of cleaning and infection control practices to ensure that the whole team has a clear understanding of the hand hygiene importance and infection prevention precautions [46,47].

Limitations.
In general, it is important to note that the sampled area in our study represents only a fraction of the entire surfaces being studied at a specifc period of time.Tis limitation could potentially reduce the test's sensitivity and may restrict the generalizability of our results, especially when trying to detect resistant bacteria that may be present in small quantities.
Our study observes signifcant variability in contamination rates between diferent months, which raises questions about the consistency of factors afecting contamination levels.Factors such as patient workload, isolation practices, and referral rates can fuctuate and complicate the interpretation of results.

Conclusion
Tere is an ongoing debate all around the world regarding whether or not the setting of a hospital contributes to the spread of HAIs.However, there is evidence from research that supports the concept that hospitals can operate as a crucial reservoir of numerous nosocomial infections in a variety of environments.Tese environments include surfaces, medical equipment, and water systems.
In this investigation, it was concluded that (1) Radiology department could be a source of healthcare-acquired infection.Gram-positive bacteria were the most present bacteria and multidrugresistant bacteria were detected from various sites with a contamination rate which exceeded the limit of 1 CFU/cm 2 for bacterial contamination.In summary, our research provides practical insights that can guide infection control practices in radiology departments.It highlights the need for rigorous cleaning and disinfection protocols, awareness of specifc bacterial strains like methicillin-resistant Staphylococcus, and further exploration of innovative solutions to minimize bacterial contamination and reduce the risk of infections in healthcare settings.work, analysis, and wrote the manuscript.SA revised and wrote the manuscript.All authors have read and approved the fnal version of the manuscript for submission.

( 2 )
Te relatively high methicillin-resistant Staphylococcus contamination rate observed in this study highlights the importance of regular monitoring for Staphylococcus contamination in radiology departments.It emphasizes the need for stringent infection control practices to prevent the spread of methicillin-resistant Staphylococcus within healthcare facilities.(3) Increase in the work load, referred and isolated patients which were proportional to the increase in the contamination rate, the presence of Gramnegative, and multidrug-resistant bacteria.(4) Surface cleaning and disinfecting must frequently focus on keyboards in the radiology department, examination patient table sides and centres, knee coil, US machine, and patient legs support in particular.Proper hand hygiene can also help reduce the risk of bacterial transmission within examination rooms.

Table 2 :
Sites with the contamination rate of ≥1 CFU/cm 2 , either on blood or on chocolate agar.

Table 3 :
Sites contaminated with bacteria that can grow on MSA agar during two months.
3.6.Gram-Positive: VRE.VRE were detected in fve of the examined sites, one site in May with a contamination rate <1 CFUs/cm 2 , while the other four times were in June, with a contamination rate of ≥1 CFUs/cm 2 , as shown in Table5.3.7.Gram-Negatives.Our results showed that only four Gram-negative bacteria were isolated from four diferent sites during the two cohorts done in May and June 2022.Tree of these contaminated sites have contamination rate of <1 CFUs/cm 2 during May, while the fourth contaminated site (centre of patient table-CT cannon) has a contamination rate of 1.4 CFUs/cm 2 and this contamination was detected in June, as shown in Tables S1, S2 and 6.3.8.Gram-Negative: ESBL and CRE.None of the equipment sites from the radiology department that were tested showed growth of ESBL and CRE, according to the data in TablesS1

Table 4 :
Sites contaminated with MRS on mannitol salt agar with oxacillin.

Table 5 :
Sites harbors VRE in the radiology department, on bile esculin agar with vancomycin.

Table 6 :
Samples with growth of Gram-negative bacteria.