|Year : 2015 | Volume
| Issue : 1 | Page : 27-31
Study of Prevalence of Microbial Contamination with its Antibiotic Resistance Pattern in Automated Teller Machine in and around Puducherry, India
J Nagajothi1, D Jeyakumari1, S Vigneshwaran2, R Praveen Kumar2, RS Bharatwaj3, R Bagyalakshmi1
1 Department of Microbiology, Sri Lakshmi Narayana Institute of Medical Sciences, Ossudu, Puducherry, India
2 Department of Internees, Sri Lakshmi Narayana Institute of Medical Sciences, Ossudu, Puducherry, India
3 Department of Community Medicine, Sri Lakshmi Narayana Institute of Medical Sciences, Ossudu, Puducherry, India
|Date of Web Publication||3-Jul-2015|
Department of Microbiology, Sri Lakshmi Narayana Institute of Medical Sciences, Ossudu, Koodapakkam Post, Villianur Commune, Puducherry - 605 502
Source of Support: None, Conflict of Interest: None
Objective: To determine the prevalence of microbial contamination in automated teller machine (ATM) centers and report on its antibiotic susceptibility pattern. Materials and Methods: Ninety-two samples were collected from different ATM centers in and around Puducherry, India during summer (n = 50) and winter (n = 42). Sterile swabs soaked in sterile saline were used to swab the door handles, ATM monitors, keyboards, card swiping machines, and money outlets. The swabs were transported to the laboratory within 30 min from the time of collection and processed according to standard microbiological methods. Results: Of the 92 swabs collected from ATM centers, microbial growth was observed in 88 (95.7%) swabs. One hundred and sixty micro-organisms comprising 157 bacteria and 3 fungi were isolated. Klebsiella species (42.5%) was the predominant isolate followed by coagulase-negative Staphylococcus (CoNS) 20.62% and Pseudomonas aeruginosa (15%), Escherichia coli (10.6%), Staphylococcus aureus (3.75%). All the isolates of Klebsiella, P. aeruginosa, and E. coli were susceptible to amikacin, imipenem, ceftazidime-clavulanic acid, and piperacillin-tazobactam. Variable susceptibility patterns were obtained with amoxyclav, ceftazidime, ciprofloxacin, gentamycin. In the summer study, 82% Klebsiella species were extended-spectrum beta-lactamase (ESBL) producers and 40% S. aureus were resistant to methicillin. CoNS exhibited sensitivity to amoxyclav, penicillin, ceftazidime, erythromycin, linezolid, vancomycin. Conclusion: The study revealed heavy bacterial contamination of ATM centers. Significantly ESBL producing Klebsiella species and Methicillin resistant S. aureus were colonizing the ATM machines. This finding necessitates the need for frequent disinfection of ATM machines and its accessories along with periodical microbiological surveillance.
Keywords: Automated teller machine, coagulase-negative Staphylococcus, extended-spectrum beta-lactamase, Klebsiella species, Methicillin resistant Staphylococcus aureus
|How to cite this article:|
Nagajothi J, Jeyakumari D, Vigneshwaran S, Kumar R P, Bharatwaj R S, Bagyalakshmi R. Study of Prevalence of Microbial Contamination with its Antibiotic Resistance Pattern in Automated Teller Machine in and around Puducherry, India. J Earth Environ Health Sci 2015;1:27-31
|How to cite this URL:|
Nagajothi J, Jeyakumari D, Vigneshwaran S, Kumar R P, Bharatwaj R S, Bagyalakshmi R. Study of Prevalence of Microbial Contamination with its Antibiotic Resistance Pattern in Automated Teller Machine in and around Puducherry, India. J Earth Environ Health Sci [serial online] 2015 [cited 2020 Mar 31];1:27-31. Available from: http://www.ijeehs.org/text.asp?2015/1/1/27/159924
| Introduction|| |
Pathogens spread among people with direct or indirect contact on hands or on inanimate objects.  Bank automated teller machine (ATM) are mainly localized in city centers, trade areas, and around the hospitals. Hundreds of people whose socioeconomic levels and hygienic status are quite different with each other use ATMs daily. The point of contact is the customer's hands to the surfaces of keypad and/or screen of these devices. However, there is limited data about their potential for microbial colonization. Therefore, investigation of the bacterial load of these devices may be valuable to increase our awareness about the possible ways of transmission of these pathogens.  Many epidemiological studies have confirmed that many contaminated surfaces played a major role in the spread of infectious diseases. Most people do not realize that microbes are found on many common outdoor objects, in their offices, and even in their homes viz; playground equipments, ATM keyboards, kitchen sinks, office desks, computer keyboards, escalator handrails, elevator buttons, shopping carts handles in supermarkets. ,
One of the most commonly touched surfaces today is the computer keyboard. Twenty-five percent of keyboards carry pathogens at any given time which is more than double that of other commonly touched surfaces. , Many factors have been shown to influence the bacterial transfers between surfaces, including the source and destination surface features, bacterial species involved, moisture levels, pressure and friction between the contact surfaces, and inoculum size on surfaces. It has also been shown that food eaten without proper washing of the fingers can easily be cross-contaminated by bacteria from the hands after handling dirty currency notes. It has also been shown that microbes once attached to hands and to some surfaces may survive for a while and may be difficult to remove. 
The present study was undertaken to evaluate the microbial contamination with its antibiotic resistance in ATM centers in and around Puducherry.
| Materials and Methods|| |
Ninety-two samples were collected from different ATM centers during summer (n = 50: ATM Study I) and winter (n = 42: ATM Study II) in Puducherry. Sterile swabs soaked in sterile saline was used to swab the door handles, ATM monitors, keyboards, card swiping machines, and money outlets in ATM centers. The swabs were transported to the laboratory within 30 min. The swabs were inoculated on blood agar, MacConkey agar, and incubated at 37°C for 24-48 h. MacConkey agar supporting the growth of both Gram-positive and Gram-negative organisms was used in the study. MacConkey agar (HiMedia, M082A-500G) without crystal violet and with 0.5% bile salts was used for isolation. The bacterial growth was observed, and the colonies were identified based on standard biochemical tests. Kirby-Bauer disc diffusion test was performed as per CLSI guidelines  to determine the susceptibility pattern of the isolates recovered from ATM Study I. The antibiotics used in the study were amoxicillin/clavulanic acid (30 μg), amikacin (30 μg), ceftazidime (30 μg), ciprofloxacin (5 μg), piperacillin-tazobactam (100/10 μg), imipenem (10 μg), trimethoprim/sulfamethoxazole (1.25/23.75 μg), gentamicin (10 μg), penicillin (10 units), oxacillin (1 μg), clindamycin (2 μg), erythromycin (15 μg), linezolid (30 μg), vancomycin (30 μg).
The susceptibility and resistance pattern of the bacterial isolates were recorded based on the zone size that is, the diameter of the zone of inhibition. The diameter zones were recorded and compared with the standard chart (HiMedia). Accordingly, susceptibility and resistance pattern of the isolates were documented.
Extended-spectrum beta-lactamase (ESBL) producing bacterial isolates were identified by using EzyMIC™ (ESBL and AmpC detection Ezy MIC™ strip, Catalogue No EM081A, Himedia, India). The test was carried out on a Mueller-Hinton agar plate inoculated with a standardized bacterial inoculum (turbidity matched with McFarland 0.5) and EzyMIC™ was placed. The plates were incubated aerobically at 37°C. The value where the ellipse intersects the scale on the strip was noted and accordingly interpreted as ESBL or non-ESBL producing organisms.
For isolation of fungi, the swabs were inoculated on Sabouraud's dextrose agar (SDA) and incubated at 25°C for 10 days. The identification of filamentous fungi was carried out by slide culture technique. In brief, a small square agar block of SDA was placed on a clean glass slide. Growth from the colony was removed using an inoculating needle and placed on the four corners of the agar block. A cover slip was placed over the agar and gently pressed to seat it firmly on the agar. Ten milliliter of sterile distilled water was poured into the Petri dish, and incubated at room temperature 25°C for 48-72 h. When sufficient growth has occurred, the cover slip was removed with sterile forceps and transferred to a drop of lactophenol cotton blue mount on a microscopic slide. The fungi were identified based on the microscopic characters. 
| Results|| |
Of the 92 swabs collected from ATM centers, 88 (95.7%) showed microbial growth and 4 (4.3%) swabs revealed no microbial growth. One hundred and sixty microorganisms were recovered from 88 swabs, which comprised 157 bacteria and 3 fungi. The bacterial isolates were identified by standard biochemical tests [Table 1]. The distribution of microorganisms recovered from ATM I and ATM II is given in [Table 2]. Klebsiella species (42.5%) was the predominant isolate followed by coagulase-negative Staphylococci (CoNS) 20.62% and Pseudomonas aeruginosa (15%). In the summer season, Klebsiella species were the predominant isolate (61.72%) followed by P. aeruginosa (17.28%), Staphylococcus aureus and CoNS (7.40%) and E. coli (6.17%). In winter, CoNS (34.17%) were the predominant isolate followed by Klebsiella species (22.7%). Nonfermenters and fungal isolates were recovered from ATM center only in the winter season.
|Table 1: Results of biochemical tests performed to identify bacterial isolates recovered from ATM centers|
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The results that is, isolation of bacteria in the study were analyzed by Fisher exact test using SPSS software version 20. Fisher exact test was applied to find out whether the organisms isolated during the summer and winter were statistically significant or not.
Antimicrobial susceptibility testing was performed only on the bacterial isolates obtained from ATM 1 Study. ATM 2 Study was conducted to determine the seasonal variation in microbial flora. The results were analyzed statistically using SPSS software version 20. Fisher exact test was carried out to find out whether the organisms isolated during the summer and winter were statistically significant or not.
All the isolates of Klebsiella, P. aeruginosa, and E. coli were susceptible to Amikacin, ceftazidime-clavulanic acid, piperacillin-tazobactam, and imipenem. Variable susceptibility patterns were obtained with amoxyclav, ceftazidime, ciprofloxacin, and gentamycin [Table 3].
|Table 3: Table representing the susceptibility pattern of bacterial isolates|
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All the isolates of CoNS were susceptible (100%) to amoxyclav, penicillin, clindamycin, erythromycin, linezolid, and vancomycin whereas all the isolates of S. aureus were sensitive (100%) to linezolid and vancomycin. Varying susceptibility was obtained with amoxyclav, amikacin, ciprofloxacin, co-trimoxazole, penicillin, clindamycin, and erythromycin.
Among S. aureus, 40% were resistant to Methicillin, 55% to penicillin followed by resistance to co-trimoxazole (27%), gentamycin (25%), erythromycin (20%), amikacin (15%), ciprofloxacin (5%), and clindamycin (5%). Twenty percent of CoNS were resistant to gentamicin followed by co-trimoxazole (15%), amikacin (10%), and ciprofloxacin (2%). Methicillin resistance was not observed in CoNS. All the isolates of Klebsiella were resistant to amoxyclav and co-trimoxazole (100%) while 70% of E. coli were resistant to amoxyclav and 100% resistant to co-trimoxazole. Forty-one isolates (82%) of klebsiella species were ESBL producers while ESBL was not detected in P. aeruginosa and E. coli. The resistance profile of Gram-negative bacilli and Gram-positive cocci are shown in [Figure 1] and [Figure 2], respectively.
|Figure 1: Histogram representing the resistance profile of Gram-negative bacilli|
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|Figure 2: Histogram representing the resistance profile of Gram-positive cocci|
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| Discussion|| |
Today, ATMs are widely used by many people, and they tend to harbor the microorganisms on their surfaces. The hand borne transmission through ATM is one of the most important routes for the spread of infectious agents in the community.  To investigate whether ATMs can serve as potential vectors for transmission of infection, the study was carried out by collecting swabs from ATM centers in and around Puducherry. The results revealed the growth of micro-organisms in ATM machines particularly the pathogenic and antibiotic resistant organisms such as Klebsiella species, P. aeruginosa, E. coli, and S. aureus.
Microbial growth was detected in 95.7% swabs collected from ATMs, which is suggestive of heavy contamination of ATM machines. Apart from pathogenic organisms, microorganisms of low virulence such as CoNS and nonfermenters were also isolated. Presence of these organisms in ATM machines cannot be ignored as they can be potentially pathogenic in immunocompromised and hospitalized patients.
Klebsiella species were predominant in summer season as against CoNS in winter. The result of antimicrobial susceptibility testing revealed the presence of 40% Methicillin resistant S. aureus (MRSA) and 82% ESBL producing Klebsiella species. ATM machines harboring the resistant micro-organisms would serve as a potential hazard in the transmission of pathogenic bacteria.
Many bacterial, fungal, and viral pathogens could survive on the inanimate objects for several months, and such pathogens could cause epidemic infections as a result of direct or indirect transmission in "hand-object-susceptible patient" ring. Specifically, high rates of microbial accumulation were found on the mobile phones and computers' keypads, which had similar features with ATMs according to their physical and operational aspects.
Tekerekoglu et al. , reported that cell phones of patients, visitors, and health care workers carried multidrug-resistant hospital pathogens including Acinetobacter spp., S. aureus, and extended-spectrum β-lactamase ESBL-positive Enterobacteriaceae. Hence, they suggested frequent disinfection of mobile phones to reduce bacterial reservoir on these devices. Similarly, Dogan et al.,  2008 found many types of pathogens on the computers' mice and keypads which were used in hospitals and in education institutes. These findings necessitate the need for assessing the hygienic status of bank ATMs to develop preventive measures against the health risks caused by such devices. In the present study, 41 (82%) ESBL producing Klebsiella species and 40% MRSA were isolated from the swabs collected from ATM centers. Several research groups have conducted studies on microbiological surveillance of ATM and reported the presence of drug-resistant bacteria. Tekerekoglu et al.  reported MRSA; Methicillin resistant CoNS recovered from ATM. Antibiotic resistant E. coli was not reported in the study. Joshaline et al.,  reported about P. aeruginosa exhibiting resistance to amikacin, ampicillin, co-trimoxazole, chloramphenicol, nalidixic acid, and E. coli exhibiting resistance to amikacin, ampicillin, chloramphenicol, co-trimoxazole, nalidixic acid, Klesiella showed resistance to amikacin, ampicillin, co-trimoxazole, chloramphenicol, and nalidixic acid. Chairman et al.  reported on E. coli isolates, which were resistant to augmentin, imipenem, and S. aureus isolates which were resistant to clindamycin, cephalothin, and augmentin while K. pneumoniae showed resistance to augmentin and metronidazole. Cleaning regimen aimed at reducing the population and presence of these organisms on such surfaces should be developed using appropriate sanitizers and strictly adhered to by operators of such facilities. Frequent disinfection of the keyboards and screen parts, using antibacterial covers for the contact surfaces or using alcohol wipes before and after use may be a benefit for limiting the bacterial accumulation and transmission with cash machines. Further investigations are required to determine the status of ATMs according to viruses and parasites, which were not studied in this investigation. Antibiotic-resistant bacteria and seasonal variation of bacterial flora from ATM centers are being reported in the study emphasizing the need for continuous microbiological surveillance. To the best of our knowledge, this is the first study reporting the colonization of bacteria in ATM centers in Puducherry. Our results suggest that ATMs might be potential areas for pathogen accumulation, and they might have a role in microbial transmission in the community.
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Conflict of interest
There are no conflicts of interest.
| References|| |
Mathai E, Allegranzi B, Kilpatrick C, Pittet D. Prevention and control of health care-associated infections through improved hand hygiene. Indian J Med Microbiol 2010;28:100-6.
Tekerekoglu MS, Duman Y, Serindag A, Cuglan SS, Kaysadu H, Tunc E, et al.
Do mobile phones of patients, companions and visitors carry multidrug-resistant hospital pathogens? Am J Infect Control 2011;39:379-81.
Hartmann B, Benson M, Junger A, Quinzio L, Röhrig R, Fengler B, et al.
Computer keyboard and mouse as a reservoir of pathogens in an intensive care unit. J Clin Monit Comput 2004;18:7-12.
Noble J. Text Book of Primary Care Medicine. 3 rd
ed. St. Louis, Mo: Mosby; 2001. p. 8.
Bures S, Fishbain JT, Uyehara CF, Parker JM, Berg BW. Computer keyboards and faucet handles as reservoirs of nosocomial pathogens in the intensive care unit. Am J Infect Control 2000;28:465-71.
Hendley JO, Wenzel RP, Gwaltney JM Jr. Transmission of rhinovirus colds by self-inoculation. N Engl J Med 1973;288:1361-4.
Rusin P, Maxwell S, Gerba C. Comparative surface-to-hand and fingertip-to-mouth transfer efficiency of Gram-positive bacteria, Gram-negative bacteria, and phage. J Appl Microbiol 2002;93:585-92.
Jansen A, Kielstein JT. The new face of enterohaemorrhagic Escherichia coli
infections. Euro Surveill 2011;16:25.
National Committee for Clinical Laboratory Standards. Performance standards for antimicrobial disc susceptibility tests. Approved standard (M2-A8). Wayne, PA: NCCLS; 2003.
Forbes BA, Sahm DF, Weissfeld AS. Laboratory methods in basic mycology. Bailey and Scott′s - Diagnostic Microbiology. 12 th
ed., Ch. 50. Mosby Elsevier; p. 629-709.
Tekerekoðlu MS, Yakupogullari Y, Otlu B, Duman Y, Gucluer N. Bacteria found on banks′ automated teller machines (ATMs). Afr J Microbiol Res 2013;7:1619-21.
Dogan M, Feyzioglu B, Ozdemir M, Baysal B. Investigation of microbial colonization of computer keyboards used inside and outside hospital environments. Mikrobiyol Bul 2008;42:331-6.
Joshaline MC, Subathra M, Shyamala M, Padma S, Rekha. Clinical Laboratory Standard Institute. Performance standards for antimicrobial susceptibility testing. Fifteen informational supplement; M100-S15. Wayne, PA: CLSI; 2005.
Chairman K, Mathew KE, Padmalatha C, Ranjit AJ. Beware of pathogenic microbes in public utility devices. J Microbiol Biotechnol Res 2011;1:85-90.
[Figure 1], [Figure 2]
[Table 1], [Table 2], [Table 3]