- Email: [email protected]
Automated teller machines (ATMs) and pedestrian crossing controls adjacent to major university teaching hospitals exhibit an exclusively Gram-positive flora
Accepted Manuscript Automated Teller Machines (ATMs) and Pedestrian Crossing Controls adjacent to major University Teaching hospitals exhibit an exclusively Gram-positive flora Medani Elshibly, Kaori Sudo, Jonathan Stirling, B. Cherie Millar, Naoaki Misawa, Colin E. Goldsmith, John E. Moore, Professor PII:
S0195-6701(16)30402-9
DOI:
10.1016/j.jhin.2016.09.014
Reference:
YJHIN 4925
To appear in:
Journal of Hospital Infection
Received Date: 14 September 2016 Accepted Date: 15 September 2016
Please cite this article as: Elshibly M, Sudo K, Stirling J, Millar BC, Misawa N, Goldsmith CE, Moore JE, Automated Teller Machines (ATMs) and Pedestrian Crossing Controls adjacent to major University Teaching hospitals exhibit an exclusively Gram-positive flora, Journal of Hospital Infection (2016), doi: 10.1016/j.jhin.2016.09.014. This is a PDF file of an unedited manuscript that has been accepted for publication. As a service to our customers we are providing this early version of the manuscript. The manuscript will undergo copyediting, typesetting, and review of the resulting proof before it is published in its final form. Please note that during the production process errors may be discovered which could affect the content, and all legal disclaimers that apply to the journal pertain.
ACCEPTEDLetter MANUSCRIPT
1 2 3 4 5 6
Automated Teller Machines (ATMs) and Pedestrian Crossing Controls adjacent to major University Teaching hospitals exhibit an exclusively Gram-positive flora
RI PT
7 8 9
Northern Ireland Public Health Laboratory, Department of Bacteriology, Belfast City Hospital, Lisburn Road, Belfast, BT9 7AD, Northern Ireland, UK,
M AN U
1.
Grosvenor Grammar School, Marina Park, Belfast, BT5 6BA, Northern Ireland, UK.,
3
Center for Animal Disease Control (CADIC), Laboratory of Veterinary Public Health, Department of Veterinary Science, Faculty of Agriculture, University of Miyazaki, 1-1 Gakuenkibanadai-nishi, Miyazaki 889-2192, Japan, 4.
TE D
2
School of Dentistry, Queen’s University of Belfast, Royal Group of Hospitals, Grosvenor Road, Belfast, BT12 6BP Northern Ireland, UK, School of Biomedical Sciences, University of Ulster, Cromore Road, Coleraine, BT52 1SA, Northern Ireland, UK.
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5
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11 12 13 14 15 16 17 18 19 20 21 22 23 24 25 26 27 28 29 30 31 32 33 34 35 36 37 38 39 40 41 42 43 44 45
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Medani Elshibly1,2, Kaori Sudo1,3, Jonathan Stirling1, B. Cherie Millar1, Naoaki Misawa3, Colin E. Goldsmith1 and John E. Moore1,3,4*
10
--------------------------------------------------------------------------------------------------------------*corresponding author
Professor John E. Moore, Northern Ireland Public Health Laboratory, Department of Bacteriology, Belfast City Hospital, Belfast, BT9 7AD, Northern Ireland, United Kingdom. Tel: Fax: E-mail:
+44 (28) 9026 3554 +44 (28) 9026 3991 [email protected] 1
48
ACCEPTED MANUSCRIPT
Sir,
49 Antimicrobial resistance (AMR) has emerged as a global public health problem, largely due to the
51
development of acquired antibiotic resistance in hitherto susceptible organisms, coupled with the
52
transmissibility of such organisms from patient-to-patient, as well as from the environment-to-patient.1
53
In order to help combat AMR, additional evidence is required regarding the potential occurrence,
54
persistence and transmission of AMR organisms within and outside the healthcare environment. Whilst
55
relatively well understood within the healthcare setting, there remains a relative paucity of evidence
56
regarding these three attributes for organisms outside the healthcare environment. To date, there have
57
been few reports on the total numbers, identities or antibiotic susceptibilities of culturable bacteria from
58
common utilities, including automated teller machines (ATMs) and the metal control buttons (MCBs) of
59
pedestrian crossings. Given the emerging importance of highly resistant Gram-negative organisms, in
60
particular, extended spectrum beta-lactamase (ESBL)-producing organisms and carbapenemase-
61
producing organisms, we wished to investigate whether such organisms are associated with these
62
utilities.
SC
M AN U
TE D
EP
63
RI PT
50
Twelve sites were sampled in the geographical area between two hospitals in Belfast, Northern Ireland
65
that are located approximately 1.5 km apart: Belfast City Hospital and the Royal Group of Hospitals.
66
Environmental sampling occurred over a two week period during August 2015. We sampled were six
67
ATMs, all of which had a continuous consecutive flow of customers, and six MCBs at bust pedestrian
68
crossings. Swabs moistened in 0.1% [w/v] peptone saline diluent were used to sample the “Enter”
69
button on ATM keypads (most transactions require the use of this key) and the entire surface of MCBs.
70
Swabs were subsequently placed in Amies transport medium (Sterilin Ltd., Newport, UK), transported
71
to the laboratory at ambient temperature and inoculated onto Columbia blood agar (CM0331 Oxoid Ltd.,
AC C
64
3
ACCEPTED MANUSCRIPT Basingstoke, UK). Cultures were examined after incubation for 48h at 37oC under aerobic conditions.
73
Following this, further incubation was extended up to three weeks at ambient temperature, to promote
74
the proliferation of slow-growing environmental organisms. Total numbers of colonies were ascertained,
75
and expressed as colony forming units/cm2 (cfu/cm2). Isolates were identified using MALDI-TOF
76
technology (Biomerieux Ltd., Basingstoke, UK), and the antibiotic susceptibilities determined by
77
standard disk diffusion; antibiotics tested were vancomycin, mupirocin, penicillin, erythromycin,
78
clindamycin, fusidic acid, gentamicin, teicoplanin, oxacillin and cefoxitin.
SC
RI PT
72
79
All ATMs and pedestrian controls harboured culturable bacteria in the range of 2.0-9.5 cfu/cm2 (mean
81
4.25 cfu/cm2) and 0.3-4.3 cfu/cm2 (mean 2.9cm2), respectively. An exclusively Gram-positive flora was
82
isolated from both ATMs and MCBs, comprising five genera: Bacillus, Micrococcus, Mycobacterium,
83
Staphylococcus and Streptococcus. ATM machines harboured multiple replicates of seven species:
84
Micrococcus luteus was most frequent, followed by Staphylococcus haemolyticus, Bacillus simplex,
85
Staphylococcus hominis, Staphylococcus warneri and Bacillus pumilus; a single isolate of
86
Mycobacterium kansasii was isolated from one ATM machine. MCBs also harboured multiple
87
replicates of seven species: Micrococcus luteus followed by Staphylococcus epidermidis, Bacillus
88
subtilis, Staphylococcus equorum, Staphylococcus hominis, Streptococcus salivarius and Bacillus
89
licheniformis. All isolates were susceptible to all antibiotics tested, with the exception of Micrococcus
90
luteus (all resistant to mupirocin) and one isolate of Staphylococcus haemolyticus that was resistant to
91
cefoxitin.
92 93
This study generated large numbers of Gram-positive organisms, many of which were replicates of the
94
same recurring species, none of which were unequivocal pathogens. We were unable to isolate any
95
Gram-negative organisms from any ATM or MCB. These findings concur with our previously reported
AC C
EP
TE D
M AN U
80
4
ACCEPTED MANUSCRIPT
finding that Gram-negative bacteria could not be isolated from several currency coinages.2 The metal
97
surface of ATM keypads and MCBs appear to be a hostile environment for the survival of Gram-
98
negative bacteria. This may be due to the relative dryness or high polish of surfaces, high ambient
99
temperatures and/or the high incidence of ambient light . As it was not the design of our study, we are
100
unable to extrapolate evidence as to the potential for transmissibility of organism from keypad/control
101
units to fingertip, which requires further investigation.
102
RI PT
96
Changing societal practices, particularly relating to digital security, is making employment of touch
104
devices, such as access keypads, more common. Innovation is currently being developed by Google
105
called Project Soli, which will revolutionise a new generation of touchless finger activated controls
106
employing radar, which may have significant advantages for infection prevention.3
M AN U
SC
103
107
In conclusion, the study demonstrates that ATM machines and MCBs are not reservoirs of Gram-
109
negative organisms in the community, and thus are unlikely to be a communal source of ESBL or
110
carbapenem-producing organisms.
113 114
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112
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111
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108
5
115
ACCEPTED MANUSCRIPT
ACKNOWLEDGEMENT
116 KS was supported by a Japan Public-Private Partnership Student Study Abroad Program TOBITATE
118
Young Ambassador Program awarded by the Japan Society for the Promotion of Science (JSPS). JEM
119
was supported by a travel grant awarded by the Great Britain Sasakawa Foundation (GBSF #4731)
120
(www.gbsf.org.uk)., to examine aspects of antimicrobial resistance in Japan and the UK. The authors
121
wish to thank Mr. Alan Murphy, Northern Ireland Public Health Laboratory, Department of
122
Bacteriology, Belfast City Hospital, for advice regarding bacteriological culture media
SC
RI PT
117
123
M AN U
124
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125
6
126
ACCEPTED MANUSCRIPT
REFERENCES
127 128 129
1
130
Holmes AH, Moore LS, Sundsfjord A, et al. Understanding the mechanisms and drivers of antimicrobial resistance. Lancet 2016;387(10014):176-187.
132
2
133
RI PT
131 Xu J, Moore JE, Millar BC. Ribosomal DNA (rDNA) identification of the culturable bacterial flora on monetary coinage from 17 currencies. J Environ Health 2005;67:51-55.
134
136
3
Anon. Welcome to Project Soli. https://www.youtube.com/embed/0QNiZfSsPc0.
SC
135
Last accessed on 04 August 2016.
M AN U
137 138
AC C
EP
TE D
139
7
S0195-6701(16)30402-9
DOI:
10.1016/j.jhin.2016.09.014
Reference:
YJHIN 4925
To appear in:
Journal of Hospital Infection
Received Date: 14 September 2016 Accepted Date: 15 September 2016
Please cite this article as: Elshibly M, Sudo K, Stirling J, Millar BC, Misawa N, Goldsmith CE, Moore JE, Automated Teller Machines (ATMs) and Pedestrian Crossing Controls adjacent to major University Teaching hospitals exhibit an exclusively Gram-positive flora, Journal of Hospital Infection (2016), doi: 10.1016/j.jhin.2016.09.014. This is a PDF file of an unedited manuscript that has been accepted for publication. As a service to our customers we are providing this early version of the manuscript. The manuscript will undergo copyediting, typesetting, and review of the resulting proof before it is published in its final form. Please note that during the production process errors may be discovered which could affect the content, and all legal disclaimers that apply to the journal pertain.
ACCEPTEDLetter MANUSCRIPT
1 2 3 4 5 6
Automated Teller Machines (ATMs) and Pedestrian Crossing Controls adjacent to major University Teaching hospitals exhibit an exclusively Gram-positive flora
RI PT
7 8 9
Northern Ireland Public Health Laboratory, Department of Bacteriology, Belfast City Hospital, Lisburn Road, Belfast, BT9 7AD, Northern Ireland, UK,
M AN U
1.
Grosvenor Grammar School, Marina Park, Belfast, BT5 6BA, Northern Ireland, UK.,
3
Center for Animal Disease Control (CADIC), Laboratory of Veterinary Public Health, Department of Veterinary Science, Faculty of Agriculture, University of Miyazaki, 1-1 Gakuenkibanadai-nishi, Miyazaki 889-2192, Japan, 4.
TE D
2
School of Dentistry, Queen’s University of Belfast, Royal Group of Hospitals, Grosvenor Road, Belfast, BT12 6BP Northern Ireland, UK, School of Biomedical Sciences, University of Ulster, Cromore Road, Coleraine, BT52 1SA, Northern Ireland, UK.
EP
5
AC C
11 12 13 14 15 16 17 18 19 20 21 22 23 24 25 26 27 28 29 30 31 32 33 34 35 36 37 38 39 40 41 42 43 44 45
SC
Medani Elshibly1,2, Kaori Sudo1,3, Jonathan Stirling1, B. Cherie Millar1, Naoaki Misawa3, Colin E. Goldsmith1 and John E. Moore1,3,4*
10
--------------------------------------------------------------------------------------------------------------*corresponding author
Professor John E. Moore, Northern Ireland Public Health Laboratory, Department of Bacteriology, Belfast City Hospital, Belfast, BT9 7AD, Northern Ireland, United Kingdom. Tel: Fax: E-mail:
+44 (28) 9026 3554 +44 (28) 9026 3991 [email protected] 1
48
ACCEPTED MANUSCRIPT
Sir,
49 Antimicrobial resistance (AMR) has emerged as a global public health problem, largely due to the
51
development of acquired antibiotic resistance in hitherto susceptible organisms, coupled with the
52
transmissibility of such organisms from patient-to-patient, as well as from the environment-to-patient.1
53
In order to help combat AMR, additional evidence is required regarding the potential occurrence,
54
persistence and transmission of AMR organisms within and outside the healthcare environment. Whilst
55
relatively well understood within the healthcare setting, there remains a relative paucity of evidence
56
regarding these three attributes for organisms outside the healthcare environment. To date, there have
57
been few reports on the total numbers, identities or antibiotic susceptibilities of culturable bacteria from
58
common utilities, including automated teller machines (ATMs) and the metal control buttons (MCBs) of
59
pedestrian crossings. Given the emerging importance of highly resistant Gram-negative organisms, in
60
particular, extended spectrum beta-lactamase (ESBL)-producing organisms and carbapenemase-
61
producing organisms, we wished to investigate whether such organisms are associated with these
62
utilities.
SC
M AN U
TE D
EP
63
RI PT
50
Twelve sites were sampled in the geographical area between two hospitals in Belfast, Northern Ireland
65
that are located approximately 1.5 km apart: Belfast City Hospital and the Royal Group of Hospitals.
66
Environmental sampling occurred over a two week period during August 2015. We sampled were six
67
ATMs, all of which had a continuous consecutive flow of customers, and six MCBs at bust pedestrian
68
crossings. Swabs moistened in 0.1% [w/v] peptone saline diluent were used to sample the “Enter”
69
button on ATM keypads (most transactions require the use of this key) and the entire surface of MCBs.
70
Swabs were subsequently placed in Amies transport medium (Sterilin Ltd., Newport, UK), transported
71
to the laboratory at ambient temperature and inoculated onto Columbia blood agar (CM0331 Oxoid Ltd.,
AC C
64
3
ACCEPTED MANUSCRIPT Basingstoke, UK). Cultures were examined after incubation for 48h at 37oC under aerobic conditions.
73
Following this, further incubation was extended up to three weeks at ambient temperature, to promote
74
the proliferation of slow-growing environmental organisms. Total numbers of colonies were ascertained,
75
and expressed as colony forming units/cm2 (cfu/cm2). Isolates were identified using MALDI-TOF
76
technology (Biomerieux Ltd., Basingstoke, UK), and the antibiotic susceptibilities determined by
77
standard disk diffusion; antibiotics tested were vancomycin, mupirocin, penicillin, erythromycin,
78
clindamycin, fusidic acid, gentamicin, teicoplanin, oxacillin and cefoxitin.
SC
RI PT
72
79
All ATMs and pedestrian controls harboured culturable bacteria in the range of 2.0-9.5 cfu/cm2 (mean
81
4.25 cfu/cm2) and 0.3-4.3 cfu/cm2 (mean 2.9cm2), respectively. An exclusively Gram-positive flora was
82
isolated from both ATMs and MCBs, comprising five genera: Bacillus, Micrococcus, Mycobacterium,
83
Staphylococcus and Streptococcus. ATM machines harboured multiple replicates of seven species:
84
Micrococcus luteus was most frequent, followed by Staphylococcus haemolyticus, Bacillus simplex,
85
Staphylococcus hominis, Staphylococcus warneri and Bacillus pumilus; a single isolate of
86
Mycobacterium kansasii was isolated from one ATM machine. MCBs also harboured multiple
87
replicates of seven species: Micrococcus luteus followed by Staphylococcus epidermidis, Bacillus
88
subtilis, Staphylococcus equorum, Staphylococcus hominis, Streptococcus salivarius and Bacillus
89
licheniformis. All isolates were susceptible to all antibiotics tested, with the exception of Micrococcus
90
luteus (all resistant to mupirocin) and one isolate of Staphylococcus haemolyticus that was resistant to
91
cefoxitin.
92 93
This study generated large numbers of Gram-positive organisms, many of which were replicates of the
94
same recurring species, none of which were unequivocal pathogens. We were unable to isolate any
95
Gram-negative organisms from any ATM or MCB. These findings concur with our previously reported
AC C
EP
TE D
M AN U
80
4
ACCEPTED MANUSCRIPT
finding that Gram-negative bacteria could not be isolated from several currency coinages.2 The metal
97
surface of ATM keypads and MCBs appear to be a hostile environment for the survival of Gram-
98
negative bacteria. This may be due to the relative dryness or high polish of surfaces, high ambient
99
temperatures and/or the high incidence of ambient light . As it was not the design of our study, we are
100
unable to extrapolate evidence as to the potential for transmissibility of organism from keypad/control
101
units to fingertip, which requires further investigation.
102
RI PT
96
Changing societal practices, particularly relating to digital security, is making employment of touch
104
devices, such as access keypads, more common. Innovation is currently being developed by Google
105
called Project Soli, which will revolutionise a new generation of touchless finger activated controls
106
employing radar, which may have significant advantages for infection prevention.3
M AN U
SC
103
107
In conclusion, the study demonstrates that ATM machines and MCBs are not reservoirs of Gram-
109
negative organisms in the community, and thus are unlikely to be a communal source of ESBL or
110
carbapenem-producing organisms.
113 114
EP
112
AC C
111
TE D
108
5
115
ACCEPTED MANUSCRIPT
ACKNOWLEDGEMENT
116 KS was supported by a Japan Public-Private Partnership Student Study Abroad Program TOBITATE
118
Young Ambassador Program awarded by the Japan Society for the Promotion of Science (JSPS). JEM
119
was supported by a travel grant awarded by the Great Britain Sasakawa Foundation (GBSF #4731)
120
(www.gbsf.org.uk)., to examine aspects of antimicrobial resistance in Japan and the UK. The authors
121
wish to thank Mr. Alan Murphy, Northern Ireland Public Health Laboratory, Department of
122
Bacteriology, Belfast City Hospital, for advice regarding bacteriological culture media
SC
RI PT
117
123
M AN U
124
AC C
EP
TE D
125
6
126
ACCEPTED MANUSCRIPT
REFERENCES
127 128 129
1
130
Holmes AH, Moore LS, Sundsfjord A, et al. Understanding the mechanisms and drivers of antimicrobial resistance. Lancet 2016;387(10014):176-187.
132
2
133
RI PT
131 Xu J, Moore JE, Millar BC. Ribosomal DNA (rDNA) identification of the culturable bacterial flora on monetary coinage from 17 currencies. J Environ Health 2005;67:51-55.
134
136
3
Anon. Welcome to Project Soli. https://www.youtube.com/embed/0QNiZfSsPc0.
SC
135
Last accessed on 04 August 2016.
M AN U
137 138
AC C
EP
TE D
139
7