RESEARCH ARTICLE
Transfer and Decontamination of S. aureus in Transmission Routes Regarding Hands and Contact Surfaces Pernilla Arinder1, Pär Johannesson2, Ingela Karlsson3, Elisabeth Borch1* 1 Food and Bioscience, SP Technical Research Institute of Sweden, Lund, Sweden, 2 Mechanics Research, SP Technical Research Institute of Sweden, Borås, Sweden, 3 Food and Bioscience, SP Technical Research Institute of Sweden, Göteborg, Sweden * [email protected]
a11111
OPEN ACCESS Citation: Arinder P, Johannesson P, Karlsson I, Borch E (2016) Transfer and Decontamination of S. aureus in Transmission Routes Regarding Hands and Contact Surfaces. PLoS ONE 11(6): e0156390. doi:10.1371/journal.pone.0156390 Editor: George-John Nychas, Agricultural University of Athens, GREECE Received: February 15, 2016 Accepted: May 15, 2016 Published: June 9, 2016 Copyright: © 2016 Arinder et al. This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
Abstract Hand hygiene, cleaning and disinfection are pre-requirements for hygiene management in hospital settings and the food industry. In order to facilitate risk management, different contamination scenarios and interventions need to be evaluated. In the present study data on transfer rates and reductions of Staphylococcus aureus were provided in an experimental set-up using artificial skin. Using this methodology, test persons were not exposed with pathogenic bacteria. An exposure assessment model was developed and applied to evaluate different contamination routes and hygiene interventions. The transfer rates of S. aureus from inoculated VITRO-SKIN1 to fomites were calculated from blotting series. The VITROSKIN1 was more prone to spread bacteria than fomites. When different surfaces were cleaned, the reduction of S. aureus varied between 6.7
3.5±0.3
3.1±0.7
4.5±1.3
5.0±0.4
White, low humidity
3.3±0.1
5.5±0.7
1.1±0.2
0.5±0.2
3.5±0.2
2.0±1.5
Virkon Blue, high humidity
2.2±0.5
6.7±0.0
5.3±0.3
3.6±0.4
5.2±0.6
5.1±1.0
Blue, low humidity
2.2±0.4
2.0±1.4
5.0±1.6
2.1±0.2
5.3±0.5
1.5±2.0
White, high humidity
3.1
6.1±0.3
4.9±1.0
5.4±0.3
5.9±0.3
4.6±1.2
White, low humidity
2.6±1.1
4.8±0.6
3.2±0.4
0.5±0.4
3.8±1.9
2.1±1.3
Dax 70 Blue, high humidity
2.8±0.8
6.6±1.0
4.3±1.0
7.1±1.0
6.1±1.1
2.1±1.0
Blue, low humidity
5.2±1.1
0.3±0.3
2.5±0.4
7.1±0.3
6.1±1.9
0.2±0.2
White, high humidity
3.4±1.0
4.1±1.0
4.7±1.0
1.4±1.0
6.6±1.0
4.5±1.0
White, low humidity
4.7±1.1
0.7±0.3
1.3±0.7
0.5±0.2
6.6±1.0
1.3±0.5
doi:10.1371/journal.pone.0156390.t002
contaminated door handle was able to spread a high level of S. aureus to uncontaminated hands. Scenario 2. Hand 1 touched a door handle that was subsequently touched by Hand 2. Hand 2 touched a laminate bench top. Hand 3 touched the same spot on the bench. All hands became contaminated. The laminate was contaminated with the bacteria that Hand 2 transferred from the door handle. The S. aureus level of Hand 3 was lower than of Hand 2 since it touched laminate that was contaminated by the bacteria transferred from Hand 2. Scenario 3. Hand 1 touched stainless steel door handle. Hand 2 touched the same door handle and then touched a laminate bench top. Hand 3 touched the bench top touched by Hand 2 and then touched the door handle. Hand 4 touched the door handle that had been touched by Hand 1 and Hand 3. The S. aureus level of Hand 3 was lower than of Hand 2 since it came later in the contamination chain. However, the level of S. aureus on Hand 4 was higher since it has been contaminated from the door handle to which the bacteria were transferred from both Hand 1 and Hand 3. Table 3. Analysis of Variance Table for reduction (log CFU) of S. aureus on different surface materials inoculated with two types of soiling using two types of cleaning wipes, three cleaning agents and two humidity levels. Factor
Sum of Squares
df
Mean Squares
F-value
p-value
Coupon material
58.06
2
29.03
16.50
2.23E-07
Soiling
56.65
1
56.65
32.20
1.30
1
1.30
0.74
Cleaning wipe Cleaning agent
4.63E-08 0.3904
99.01
2
49.50
28.14
1.53E-11
Humidity
197.95
1
197.95
112.51
< 2.2e-16
Residuals
365.98
208
1.76
doi:10.1371/journal.pone.0156390.t003
PLOS ONE | DOI:10.1371/journal.pone.0156390 June 9, 2016
12 / 20
S. aureus Modelling Transmission Routes
Fig 3. Boxplots with notches to indicate significant differences, illustrating the reduction of S. aureus for the parameters; material, soiling, cleaning agent, cleaning cloth and humidity. doi:10.1371/journal.pone.0156390.g003
PLOS ONE | DOI:10.1371/journal.pone.0156390 June 9, 2016
13 / 20
S. aureus Modelling Transmission Routes
Fig 4. Illustrations of different contamination scenarios where bacteria are transferred between hands and surfaces. The count on Hand 1 is assumed to be 5 log CFU at the beginning of the scenario and the final count after each scenario is shown. The order of events in the scenario is indicated in the circles. The standard deviation is a result of the variation in the transfer rates for VITRO-SKIN1, stainless steel and laminate. doi:10.1371/journal.pone.0156390.g004
PLOS ONE | DOI:10.1371/journal.pone.0156390 June 9, 2016
14 / 20
S. aureus Modelling Transmission Routes
The scenario simulation shows that one contaminated hand can spread harmful bacteria to surfaces that spread the contamination further to new hands. It illustrates that it is easy for an entire environment to become infected.
Simulation of Interventions If interventions like hand washing and cleaning of surfaces are introduced, the amount of S. aureus on the hands will be different at the end of the above scenarios. Scenario 2 was used to study the effect of interventions (Tables 4, 5 and 6). Table 4. Predicted count of S. aureus on hands in scenario 2 with and without multiple interventions. Interventions
S. aureus transferred and remaining on hands (log CFU) Hand 1
Hand 2
Hand 3
No intervention
4.8±0.0
3.1±0.2
1.6±0.2
Washing Hand 1 1)
2.8±0.4
1.1±0.4
Transfer and Decontamination of S. aureus in Transmission Routes Regarding Hands and Contact Surfaces Pernilla Arinder1, Pär Johannesson2, Ingela Karlsson3, Elisabeth Borch1* 1 Food and Bioscience, SP Technical Research Institute of Sweden, Lund, Sweden, 2 Mechanics Research, SP Technical Research Institute of Sweden, Borås, Sweden, 3 Food and Bioscience, SP Technical Research Institute of Sweden, Göteborg, Sweden * [email protected]
a11111
OPEN ACCESS Citation: Arinder P, Johannesson P, Karlsson I, Borch E (2016) Transfer and Decontamination of S. aureus in Transmission Routes Regarding Hands and Contact Surfaces. PLoS ONE 11(6): e0156390. doi:10.1371/journal.pone.0156390 Editor: George-John Nychas, Agricultural University of Athens, GREECE Received: February 15, 2016 Accepted: May 15, 2016 Published: June 9, 2016 Copyright: © 2016 Arinder et al. This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
Abstract Hand hygiene, cleaning and disinfection are pre-requirements for hygiene management in hospital settings and the food industry. In order to facilitate risk management, different contamination scenarios and interventions need to be evaluated. In the present study data on transfer rates and reductions of Staphylococcus aureus were provided in an experimental set-up using artificial skin. Using this methodology, test persons were not exposed with pathogenic bacteria. An exposure assessment model was developed and applied to evaluate different contamination routes and hygiene interventions. The transfer rates of S. aureus from inoculated VITRO-SKIN1 to fomites were calculated from blotting series. The VITROSKIN1 was more prone to spread bacteria than fomites. When different surfaces were cleaned, the reduction of S. aureus varied between 6.7
3.5±0.3
3.1±0.7
4.5±1.3
5.0±0.4
White, low humidity
3.3±0.1
5.5±0.7
1.1±0.2
0.5±0.2
3.5±0.2
2.0±1.5
Virkon Blue, high humidity
2.2±0.5
6.7±0.0
5.3±0.3
3.6±0.4
5.2±0.6
5.1±1.0
Blue, low humidity
2.2±0.4
2.0±1.4
5.0±1.6
2.1±0.2
5.3±0.5
1.5±2.0
White, high humidity
3.1
6.1±0.3
4.9±1.0
5.4±0.3
5.9±0.3
4.6±1.2
White, low humidity
2.6±1.1
4.8±0.6
3.2±0.4
0.5±0.4
3.8±1.9
2.1±1.3
Dax 70 Blue, high humidity
2.8±0.8
6.6±1.0
4.3±1.0
7.1±1.0
6.1±1.1
2.1±1.0
Blue, low humidity
5.2±1.1
0.3±0.3
2.5±0.4
7.1±0.3
6.1±1.9
0.2±0.2
White, high humidity
3.4±1.0
4.1±1.0
4.7±1.0
1.4±1.0
6.6±1.0
4.5±1.0
White, low humidity
4.7±1.1
0.7±0.3
1.3±0.7
0.5±0.2
6.6±1.0
1.3±0.5
doi:10.1371/journal.pone.0156390.t002
contaminated door handle was able to spread a high level of S. aureus to uncontaminated hands. Scenario 2. Hand 1 touched a door handle that was subsequently touched by Hand 2. Hand 2 touched a laminate bench top. Hand 3 touched the same spot on the bench. All hands became contaminated. The laminate was contaminated with the bacteria that Hand 2 transferred from the door handle. The S. aureus level of Hand 3 was lower than of Hand 2 since it touched laminate that was contaminated by the bacteria transferred from Hand 2. Scenario 3. Hand 1 touched stainless steel door handle. Hand 2 touched the same door handle and then touched a laminate bench top. Hand 3 touched the bench top touched by Hand 2 and then touched the door handle. Hand 4 touched the door handle that had been touched by Hand 1 and Hand 3. The S. aureus level of Hand 3 was lower than of Hand 2 since it came later in the contamination chain. However, the level of S. aureus on Hand 4 was higher since it has been contaminated from the door handle to which the bacteria were transferred from both Hand 1 and Hand 3. Table 3. Analysis of Variance Table for reduction (log CFU) of S. aureus on different surface materials inoculated with two types of soiling using two types of cleaning wipes, three cleaning agents and two humidity levels. Factor
Sum of Squares
df
Mean Squares
F-value
p-value
Coupon material
58.06
2
29.03
16.50
2.23E-07
Soiling
56.65
1
56.65
32.20
1.30
1
1.30
0.74
Cleaning wipe Cleaning agent
4.63E-08 0.3904
99.01
2
49.50
28.14
1.53E-11
Humidity
197.95
1
197.95
112.51
< 2.2e-16
Residuals
365.98
208
1.76
doi:10.1371/journal.pone.0156390.t003
PLOS ONE | DOI:10.1371/journal.pone.0156390 June 9, 2016
12 / 20
S. aureus Modelling Transmission Routes
Fig 3. Boxplots with notches to indicate significant differences, illustrating the reduction of S. aureus for the parameters; material, soiling, cleaning agent, cleaning cloth and humidity. doi:10.1371/journal.pone.0156390.g003
PLOS ONE | DOI:10.1371/journal.pone.0156390 June 9, 2016
13 / 20
S. aureus Modelling Transmission Routes
Fig 4. Illustrations of different contamination scenarios where bacteria are transferred between hands and surfaces. The count on Hand 1 is assumed to be 5 log CFU at the beginning of the scenario and the final count after each scenario is shown. The order of events in the scenario is indicated in the circles. The standard deviation is a result of the variation in the transfer rates for VITRO-SKIN1, stainless steel and laminate. doi:10.1371/journal.pone.0156390.g004
PLOS ONE | DOI:10.1371/journal.pone.0156390 June 9, 2016
14 / 20
S. aureus Modelling Transmission Routes
The scenario simulation shows that one contaminated hand can spread harmful bacteria to surfaces that spread the contamination further to new hands. It illustrates that it is easy for an entire environment to become infected.
Simulation of Interventions If interventions like hand washing and cleaning of surfaces are introduced, the amount of S. aureus on the hands will be different at the end of the above scenarios. Scenario 2 was used to study the effect of interventions (Tables 4, 5 and 6). Table 4. Predicted count of S. aureus on hands in scenario 2 with and without multiple interventions. Interventions
S. aureus transferred and remaining on hands (log CFU) Hand 1
Hand 2
Hand 3
No intervention
4.8±0.0
3.1±0.2
1.6±0.2
Washing Hand 1 1)
2.8±0.4
1.1±0.4
