Journal Pre-proof

How Long do Nosocomial Pathogens Persist on Inanimate Surfaces? A Scoping

Review

Lucy Porter, Ola Sultan, Brett G. Mitchell, Adam Jenney, Martin Kiernan, David J.
Brewster, Philip L. Russo

PII: S0195-6701(24)00072-0
DOI: https://doi.org/10.1016/j.jhin.2024.01.023
Reference: YJHIN 7168

To appear in: Journal of Hospital Infection

Received Date: 12 December 2023

Revised Date: 18 January 2024
Accepted Date: 31 January 2024

Please cite this article as: Porter L, Sultan O, Mitchell BG, Jenney A, Kiernan M, Brewster DJ, Russo
PL, How Long do Nosocomial Pathogens Persist on Inanimate Surfaces? A Scoping Review, Journal of
Hospital Infection, https://doi.org/10.1016/j.jhin.2024.01.023.

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© 2024 The Author(s). Published by Elsevier Ltd on behalf of The Healthcare Infection Society.
 1 How Long do Nosocomial Pathogens Persist on Inanimate Surfaces? A

2 Scoping Review

3 Lucy Porter*1,2 Ola Sultan*1,2 Brett G Mitchell3,6,9 Adam Jenney4 Martin Kiernan5 David J Brewster7,8

4 Philip L Russo1,2,3

5 *Authors Porter and Sultan contributed equally to this manuscript

6 1) Department of Nursing Research, Cabrini Health, Malvern, Australia

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7 2) School of Medicine, Monash University, Clayton, Australia

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8 3) School of Nursing, Avondale University, Wahroonga, Australia

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4) Microbiology Unit, Alfred Health, Prahran, Australia
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10 5) Richard Wells Research Centre, University of West London, London, UK
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11 6) School of Nursing and Midwifery, Monash University, Clayton, Australia

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12 7) Central Clinical School, Monash University, Clayton, Australia

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13 8) Intensive Care Unit, Cabrini Health, Malvern, Australia

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14 9) School of Nursing and Midwifery, University of Newcastle, Callaghan, Australia

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15

16

17 Corresponding author

18 Philip L Russo, Nursing and Midwifery, Building E, Peninsula Campus, 47 – 49 Moorooduc Highway

19 Frankston, Victoria, 3199 Australia. [email protected]

20

21

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22 How Long do Nosocomial Pathogens Persist on Inanimate Surfaces? A

23 Scoping Review

24

25 SUMMARY

26 Healthcare hygiene plays a crucial role in the prevention of healthcare associated infections. Patients

27 admitted to a room where the previous occupant had a multidrug resistant bacterial infection are at

28 an increased risk of colonisation and infection with the same organism. A 2006 systematic review by

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29 Kramer et al found that certain pathogens can survive for months on dry surfaces. The aim of this

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30 review is to update Kramer et al’s previous review and provide contemporary data on the survival of

31
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pathogens relevant to the healthcare environment. We systematically searched Ovid MEDLINE,
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32 CINAHL and Scopus databases for studies that described the survival time of common nosocomial
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33 pathogens in the environment. Pathogens included in the review were bacterial, viral, and fungal.
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34 Studies were independently screened against predetermined inclusion/exclusion criteria by two

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35 researchers. Conflicts were resolved by one of two senior researchers. A spreadsheet was developed
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36 for the data extraction. The search identified 1,735 studies. Following removal of duplicates and
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37 application of the search criteria, the synthesis of results from 62 included studies were included.

38 117 organisms were reported. The longest surviving organism reported was Klebsiella

39 pneumoniae which was found to have persisted for 600 days. Common pathogens of concern to

40 infection prevention and control, can survive or persist on inanimate surfaces for months. This data

41 supports the need for a risk based approach to cleaning and disinfection practices, accompanied by

42 appropriate training, audit and feedback which are proven to be effective when adopted in a ‘bundle’

43 approach.

44

45

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46 INTRODUCTION

47 The hospital environment provides a reservoir for pathogens to be transmitted to patients. Patients

48 admitted to a room where the previous occupant had a multidrug resistant bacterial infection are at

49 an increased risk of colonisation and infection with the same organism. 1 However it has been

50 demonstrated that improvements in routine hospital cleaning result in reduced healthcare

51 associated infection (HAI) rates.2 Shared medical equipment also pose additional HAI risks as

52 contaminated equipment may promote the spread of pathogens between patients on the ward. 3

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53 A 2006 systematic review by Kramer et al4 described the survival times, and factors affecting this

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54 survival, for many human pathogens including bacteria, fungi and viruses. Kramer et al found that

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Enterococcus spp. (including VRE), Staphylococcus aureus (including MRSA), Streptococcus pyogenes,
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56 and many Gram- negative species, such as Acinetobacter spp., Escherichia coli, Klebsiella spp.,
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57 Pseudomonas aeruginosa, Serratia marcescens, or Shigella spp., can survive for months on dry
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58 surfaces. Whereas most respiratory viruses such as corona, coxsackie, influenza, SARS or rhinovirus,
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59 can persist on surfaces for a few days. Factors such as humidity, temperature, and material
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60 composition of the surface can affect longevity of these pathogens.4

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61

62 Understanding the persistence of nosocomial pathogens is important to inform infection prevention

63 guidelines, particularly environmental cleaning. The aim of this review is to use a reproducible

64 approach to update Kramer et al’s 4 review and provide a complete and contemporaneous review of

65 the literature.

66

67 METHODS

68 Study Design

69 A scoping review was undertaken in preference to a systematic review, in line with the review’s

70 purpose of mapping the available literature, identifying knowledge gaps, and identifying novel

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71 infectious diseases publications in light of the COVID-19 pandemic. Moreover, the variability in

72 settings (both clinical and laboratory-based) posed challenges for the conduct of concise,

73 comparable, risk of bias assessments.5 We followed the Preferred Reporting Items for Systematic

74 Reviews and Meta-Analyses extension for Scoping Reviews (PRISMA-ScR).6

75 Search Strategy

76 A comprehensive search of the literature was performed using Ovid MEDLINE, CINAHL, and Scopus

77 databases. These databases were searched on the 5th of March 2023 with no year restrictions but

78 limited to English publications. The combination of keywords used were (“cross infection” OR

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79 “infection control”) AND (“survival” OR “persistence”), OR the organisms listed in supplementary

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80 Table S1.
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81 Study selection
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82 All identified publications were imported from Ovid MEDLINE, CINAHL, and Scopus into Covidence,
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83 (www.covidence.org) a systematic review software program, for title, abstract, and full-text
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84 screening. Following duplicate removal, titles and abstracts of the remaining citations were screened
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85 by LP and OS against the eligibility criteria (Table I)

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86 Any conflicts were reviewed by one of two senior researchers (PR and BM), who also checked a 20%

87 sample of the first authors’ title/abstract screening results. Relevant articles were then divided

88 equally between two researchers (LP and OS) for full text assessment against the inclusion/exclusion

89 criteria. With the support from the same two senior researchers (PR and BM) approximately 30% of

90 the first authors’ full text assessments were crossed-screened. Any conflicting opinions were

91 resolved through discussions held at regular meetings between four authors (OS, LP, BM, PR).

92 Data extraction

93 From the included studies, data were extracted into a spreadsheet. Extracted data included: title,

94 author, year of publication, location of study, setting, pathogens assessed, number/type of isolates,

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 95 organism type, temperature, humidity, wet/dry environment, porous/non-porous surface, types of

96 environments included in sampling, role of biofilm discussed, frequency of environmental sampling,

97 inoculation time (crude, minimum and maximum), sample survivability (viable/non-viable/not

98 discussed). In studies where they reported a range of survival times due to multiple tests, we used

99 the longest reported survival time. Where data was not available or could be clearly interpreted

100 from the study, we did not include those data.

101 RESULTS

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102 Our search identified 62 papers, in which the survival of 31 pathogens was undertaken in 572 tests.

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103 The studies spanned publications from 1963 to 2023 and were conducted in 14 different countries

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and are summarised in supplementary Table SII. The selection process and reasons for exclusion are
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105 demonstrated in the PRISMA flowchart (Figure 1).
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106 The environmental survival time for different pathogens from the included papers are presented in
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107 Table 2. We included all data reported from the included papers in this table. The longest survival
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108 time identified for a Gram negative bacterium was 600 days (Klebsiella pneumoniae) and for a Gram
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109 positive bacterium was 300 days (Staphylococcus aureus) respectively. The survival time for Candida
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110 spp. was 28 days.

111 In studies where the type of surface a pathogen was tested on could be easily identified and classified

112 into a porous or non-porous surface, we identified the reported range of survival times for various

113 pathogens (Table III). There are instances where surfaces could not be classified into porous or non-

114 porous and therefore, the data in Tables II and III at the pathogen level may appear inconsistent. From

115 the available data, the maximum survival time on porous surfaces was higher for Acinetobacter sp.,

116 E.coli, K.pneumoniae and S.aureus.

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118 DISCUSSION

119 This scoping review has provided updated data on the reported persistence of pathogens in the

120 healthcare environment, and adds to the growing evidence of the importance of healthcare

121 hygiene.1,4,68 Assadian and colleagues describe a risk based approach to healthcare hygiene based on

122 three interrelated risk profiles, that of the patient, the surface and the pathogen. Understanding the

123 relationship between these is crucial to informing cleaning and disinfection practices in the different

124 environments in healthcare. 68

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125 This review identified that clinically important pathogens have been found to persist for long periods

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126 of time; S.aureus 318 days, C.difficile 140 days, Acinetobacter sp 90 days, E.coli 56 days, Klebsiella

127 pneumoniae 600 days, and C.auris 14 days. New for this review is the finding that SARS-CoV2 had a

128
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reported maximum survival of 2 days. This however was limited to one study. Differences in survival
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129 times in our review, compared to other evidence synthesis or evidence summaries, may be explained
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130 by different search methods and different inclusion criteria, in particular conditions we were
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131 interested in papers representative of normal healthcare, residential aged care or social care settings.
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132 Pathogens surviving in the environment for varying points of time, potentially for long periods of
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133 time, emphasises the importance of routine and terminal room cleaning, in addition to the cleaning

134 of equipment between patients. The critical importance of cleaning is further supported by evidence

135 of an increased risk of pathogen acquisition from prior room occupants of S.aureus, C.difficile,

136 Acinetobacter sp and Klebsiella sp1 which we have found to survive between 90 and 600 days. A

137 multi-modal approach to environmental cleaning has been suggested as being the most beneficial

138 approach, inclusive of cleaning and care staff.69,70

139 This review identified some differences in survival times for several pathogens when compared to

140 Kramers review e.g E.coli, Serratia sp, Salmonella sp. It is uncertain why these differences were

141 identified, but one explanation may be differences in the search method and inclusion/exclusion

142 criteria.

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143 In alignment with Assadian’s emphasis on understanding the surface profile risk, this review found

144 that generally pathogens are reported to survive longer on porous surfaces. Whilst much of the

145 healthcare environment is comprised of non-porous surfaces, the opportunity for harbouring

146 persistent pathogens is facilitated through porous surfaces found with gowns, paper records,

147 bedding and clothing, all common features in a hospital environment.

148 There are limitations in this review. We were unable to replicate Kramer’s search methods from the

149 published review, this may explain a difference in the studies identified and reported survival times.

150 The decision to perform a scoping review was made once it became clear a systematic review was

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151 not feasible given the broad range of heterogenous studies identified, therefore we are unable to

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152 report on the strength or quality of the studies. Importantly differences in sampling,laboratory

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techniques and the number of different experiments per organisms in each study may also influence
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154 the data. Many of the studies were poorly described, revealed little data and there was inconsistent
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155 reporting of organism nomenclature. Another limitation is that the effect of survival micro-organisms
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156 in spore form or as a dry surface biofilm has not been reported in this review. Some studies have
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157 demonstrated survival times of greater than a year for MRSA,71 however initial conventional
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158 sampling methods showed no growth. The inability of conventional laboratory methods in the
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159 detection of viable but non-culturable environmental organisms has been demonstrated in other

160 studies.72-74 This means that our findings could be considered as a minimum potential survival time

161 for biofilm-forming organisms such as Candida auris.75

162 The importance of healthcare hygiene in the prevention of HAIs in undeniable. Inoculated, high-

163 touch surfaces represent an important reservoir in facilitating infection perpetuation within

164 healthcare facilities. Contamination of hands is a common method of transmission for nosocomial

165 pathogens.76-78 Contaminated surfaces can facilitate transmission of pathogens to hands and hands

166 similarly may transfer pathogens to surfaces.79-82 Cleaning and disinfection practices need to be

167 informed by a risk based approach, and also needs to include appropriate training, audit and

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168 feedback, proven to be effective when adopted in a ‘bundle’ approach.2 Further research is required

169 to identify more effective methods of detecting environmental contamination including biofilms,

170 efficient cleaning regimes and the efficacy of enhanced chemistries and ‘no-touch’ technologies to

171 eliminate persistent pathogens.

172

173

174

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175 Acknowledgements

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176 The authors acknowledge the assistance of Ms Di Horrigan from Cabrin Health library.
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177
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178 Conflict of interest

179 The authors report no conflicts of interest

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180
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181 Funding statement

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182 The authors wish to thank Cabrini Health for support through the Cabrini Medical Staff Student

183 Research Scholarship for LP and OS. PLR is a recipient of National Health and Medical Research

184 Council Early Career Fellowship (APP1156312), BGM is a recipient of National Health and Medical

185 Research Council Investigator grant (GNT2008392)

186

187 Author contributions

188 LP: methodology, data collection, data analysis, writing – original draft, review and editing

189 OS: methodology, data collection, data analysis, writing – original draft, review and editing

190 BGM: conceptualization, methodology, formal analysis, data curation, writing – review and editing,

191 supervision

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192 AJ: methodology, data curation, writing – review and editing

193 MK: conceptualization, methodology, data curation, writing – review and editing

194 DJB: conceptualization, methodology, writing – review and editing

195 PLR: conceptualization, methodology, formal analysis, data curation, writing – original draft, review

196 and editing, supervision

197

198 Ethics Statement

199 Not required

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431

432 Table I – Eligibility Criteria

Inclusion criteria Exclusion criteria

● English language ● Non-peer reviewed literature,
● All methods/designs available secondary and review articles,
● Primary research editorials, commentary articles
● Peer reviewed ● Grey literature
● Identifiable ‘inoculation’ time ● Non-English publications
● Identifiable environmental ● Conference proceedings
contamination of inanimate surfaces ● Text books

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● Normal ambient conditions - ● Abstracts not available
representative of normal

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healthcare/residential aged care/social
care settings
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435

436 Table II – Range of survival by pathogen

Pathogen Range of survival in Studies

days (unless (references)
otherwise indicated)
7-32
Gram positive Staphylococcus aureus <1min - 318
33-36 34-36
Clostridioides difficile 0.13-140
12,23,24,37
Coagulase negative <1 min - 28
Staphylococcus
12
Micrococcus sp. 10-10
21
Streptococcus mutans 0.13-0.2

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12,14,15,22,24,29,38-43
Gram negative Acinetobacter sp. 0.04-90
12,44
Burkholderia cepacia 0.13-8

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22,24
Bacillus sp. 1-28
45
Citrobacter freundii 0.06-0.11
Escherichia coli -p <1 min - 56 8,10,12-15,20-
24,43,45,46
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10,12,14,15,19,22,24,39,
Enterococcus sp. 0.02-287
43,45,47-49
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15,43,45,50,51
Klebsiella pneumoniae 0.57-600
43
Proteus mirabilis 0.16-0.16
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8,10,12,15,18,19,22,24,2
Pseudomonas sp 0.08-7
9,43,44,47,52 53
n

12
Salmonella sp 0.29-5
12,14,15,22,43
Serratia sp 0.29-20
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12
Stenotrophomonas maltophilia 0.29-1
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54
Fungi Candida auris 14-14
20-22,36,54,55
Candida sp. 0.13-28

56,57
Virus Animal virus 0.5-7
58-60
Coronavirus 0.04-20
61
Cytomegalovirus <1 min - 0.01
19
Haemophilus influenzae 1-1
57,62-66
Human virus <1min - 12
67
SARS-CoV 1-2
437 Human virus – Hepatitis A virus, Herpes simplex, Human immunodeficiency virus, Influenza, Parainfluenza,
438 Respiratory syncytial virus

439 Animal virus – Pseudorabies, Bovine viral diarrhoea virus, Feline calicivirus, Canine parvovirus

440

441

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442 Table III – Range of survival time by pathogen and surface

Surface Pathogens of interest ^ Range of survival Studies (references)

in days
(across studies)
12,14,15,22,24,29,41
Non-porous* Acinetobacter sp 0.29-60
33,35,36 35,36
Clostridioides difficile 0.13-140
8,12,14,15,20,22,24
Escherichia coli 0.25-11
15
Klebsiella pneumoniae 2-2
8,12,15,22,24,29,47,52
Pseudomonas sp 0.21-7
8,14,17,20,22,24,26,27,29,31,32
Staphylococcus aureus 0.04-60
12,40,42,43
Porous** Acinetobacter sp 1.5-90
35
Clostridioides difficile 0.25-3
12,13,22,43
Escherichia coli 0.29-25

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43,50
Klebsiella pneumoniae 4-600
12,18,43,47
Pseudomonas sp 0.08-7

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7,12,13,16-18,22,30-32
Staphylococcus aureus 1-168
443 * Examples of non-porous samples identified included: glass, vinyl, stainless steel, plastic, metal, ceramic,
444
445
copper, Formica, enamel. -p
** Examples of porous surfaces included: paper, linen, wood, sponge, cotton, polyester, wool, fabric.
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446 ^ Selected pathogens chosen, of important relevance to infection prevention. Full details of all papers and
447 results are provided in supplementary spreadsheet.
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Figure 1. PRISMA flow chart for included papers

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