The dynamics of methicillin-resistant Staphylococcus aureus exposure in a hospital model and the potential for environmental intervention

Background Methicillin-resistant Staphylococcus aureus (MRSA) is a major cause of healthcare-associated infections. An important control strategy is hand hygiene; however, non-compliance has been a major problem in healthcare settings. Furthermore, modeling studies have suggested that the law of diminishing return applies to hand hygiene. Other additional control strategies such as environmental cleaning may be warranted, given that MRSA-positive individuals constantly shed contaminated desquamated skin particles to the environment. Methods We constructed and analyzed a deterministic environmental compartmental model of MRSA fate, transport, and exposure between two hypothetical hospital rooms: one with a colonized patient, shedding MRSA; another with an uncolonized patient, susceptible to exposure. Healthcare workers (HCWs), acting solely as vectors, spread MRSA from one patient room to the other. Results Although porous surfaces became highly contaminated, their low transfer efficiency limited the exposure dose to HCWs and the uncolonized patient. Conversely, the high transfer efficiency of nonporous surfaces allows greater MRSA transfer when touched. In the colonized patient’s room, HCW exposure occurred more predominantly through the indirect (patient to surfaces to HCW) mode compared to the direct (patient to HCW) mode. In contrast, in the uncolonized patient’s room, patient exposure was more predominant in the direct (HCW to patient) mode compared to the indirect (HCW to surfaces to patient) mode. Surface wiping decreased MRSA exposure to the uncolonized patient more than daily surface decontamination. This was because wiping allowed higher cleaning frequency and cleaned more total surface area per day. Conclusions Environmental cleaning should be considered as an integral component of MRSA infection control in hospitals. Given the previously under-appreciated role of surface contamination in MRSA transmission, this intervention mode can contribute to an effective multiple barrier approach in concert with hand hygiene.

. Submodel for a direct contact event between a healthcare worker (HCW) and the uncolonized patient (PTu). HCW represents the concentration of MRSA cfu on the HCW (MRSA cfu/2000 sq.cm.). PTu represents the concentration of MRSA cfu on the uncolonized patient (MRSA cfu/2000 sq.cm.). The transfer efficiency of MRSA from the HCW's hands to the uncolonized patient's skin was assumed to be the same as transfer efficiency from the uncolonized patient's skin to the HCWs' hands.

Differential equations
A diagram depicting the compartmental model is shown in Figure 1 in the main text. The definitions of the parameters are presented in Table 1 and also in the main text. The following are the differential equations for the ten compartments.

1) The colonized patient (PT c )
We assumed that the colonized patient maintains a steady MRSA concentration on the exposed skin and hands (PT c ). This balance was achieved by the gain and loss of MRSA. The colonized patient gained MRSA from the replenishment of the skin epithelial cells and from touching the nose. The replenishing rate was assumed to be the same as the dispersal rate.
Concentration of MRSA in the nose (PT cn ) was assumed constant (1000 cfu/4 cm 2 ). The colonized patient, on the other hand, lost MRSA from the natural die-off and from pathogen flows to surfaces and HCWs due to touching events. The HCWs touched the colonized patient only during the first 20 minutes of the hour.
The change in MRSA concentration on the skin and hand of the colonized patient (PT c ) are given by the following: where, m∈Ζ+, and The function f(t) is a time indicator function for a HCW's visit in the colonized patient's room. f(t) was equal to one during the first 20 minutes, allowing HCW touching events to occur and equal to 0 during other times.
PT c was initialized at the equilibrium MRSA level of 6,000 cfu/2000 cm 2 .

2) The porous surface in the colonized patient's room (P c )
Changes in MRSA concentration on the porous surface in the colonized patient's room (P c ), as described in Equation 3, were driven by the deposition of MRSA on the surface, surface touches by the colonized patient, surface touches by the HCWs during the first 20 minutes of the hour, natural die-off, and daily surface decontamination.
where, m∈Ζ+, and The function h(t) is a time indicator function that regulates decontamination to every 24 hours.

3) The nonporous surface in the colonized patient's room (NP c )
Changes in MRSA concentration on the nonporous surface in the colonized patient's room (NP c ), as described in Equation 5, were driven by the deposition of MRSA dispersal on the surface, surface touches by the colonized patient, surface touches by the HCWs during the first 20 minutes of the hour, the natural die-off, and the daily surface decontamination. Structurally, the nonporous surface is similar to the porous surface, except that only the nonporous surfaces can be wiped off following a HCW touch. The wiping rate is as frequent as the rate at which HCWs touch the nonporous surface. The efficacy of the wipes and the wiping rate is denoted by ε w and ω hcw-np , respectively.

4) The uncolonized patient (PT u )
Changes in MRSA concentration on the skin and hands of the uncolonized patient (PT u ), as described in Equation 6, were driven by contacts with HCWs during the second 20 minutes of the hour, contacts with the two room surfaces, contact with one's own nose, and the natural dieoff on the skin and hand.
The function g(t) is a time indicator function regulating the HCW's visit in the uncolonized patient's room. g(t) was equal to one during the second 20 minutes of the hour, allowing the HCW's touching events to occur and equals 0 during other times.

5) The porous surface in the uncolonized patient's room (P u )
Changes in MRSA concentration on the porous surface in the uncolonized patient's room, as described in Equation 8, were similar to those in the porous surface in the colonized patient's room, except that there was no MRSA dispersal and deposition in the uncolonized patient's room. Surface touches by the HCW occurred during the second 20 minutes of the hour.

6) The nonporous surface in the uncolonized patient's room (NP u )
Changes in MRSA concentration on the nonporous surface in the uncolonized patient's room, as described in Equation 9, were similar to those in the nonporous surface in the colonized patient's room, except that there was no MRSA dispersal and deposition in the uncolonized patient's room. Surface touches by the HCW occurred during the second 20 minutes of the hour.

7) The healthcare workers (HCWs)
Changes in MRSA concentration on the exposed skin and hands of HCWs, as described in Equation 10, were driven by all HCW activities and natural die-off on skin and hands.
Activities of HCWs included touching the colonized patient and the room surfaces during the first 20 minutes while in the colonized patient's room, touching the uncolonized patient and the room surfaces during the second 20 minutes while in the uncolonized patient's room, and touching one's own noses. HCWs may also wipe the nonporous surfaces after a nonporous surface touch. HCWs were assumed to have clean skin and hands at the beginning of each 8-hour shift. The time indicator for the beginning of the shift is s(t).
where, m∈Ζ+ and The other two compartments in the model are MRSA accumulated in the uncolonized patient's nose and HCW's nose. They are given by the following equations: