Among the various problems to deal with in medicalized environment, healthcare-associated infections (HAI) currently represent one of the biggest threats for resident and hospitalized persons all around the world. A prevalence survey estimated the number of HAI in the United States as around 772,000 cases during the year 2011, corresponding to a prevalence of 4% [1
]. In 2012, in Europe, the HAI prevalence was around 6%, ranging from 2% to 11% for overall European countries [2
]. In the healthcare environment, microorganisms can easily spread from resident to resident [3
] and from resident to staff through different pathways. Direct contact between people is the most obvious factor of microbial cross-contamination. The hands of a healthcare worker can have a high risk of being contaminated following a direct skin contact with infected patient [4
], and hand hygiene is the first strategy for preventing healthcare-associated infections [7
]. However, pathogens can also spread through contact between people and touch surfaces. Indeed, by multiple surface-skin transfer, a contamination on a primary surface can somehow very quickly spread across an entire service or care unit [8
]. This observation highlights the role of the surfaces in the dissemination of microorganisms and it suggests that surfaces may represent sources of microbial contamination for the users [8
]. Furthermore, most of the microorganisms, and more specifically bacteria, can persist on these surfaces for an extremely long time [11
]. To hamper this situation, the main action against bacteria persistence remains the regular cleaning and disinfection of touch surfaces [12
]. However, as observed, bacteria can rapidly recolonize the surfaces after disinfection. For example, 24 h after decontamination with hydrogen peroxide vapor, methicillin-resistant Staphylococcus aureus
(MRSA) have been detected on surfaces in an intensive care unit [13
Nowadays, many approaches other than cleaning and disinfection are proposed to reduce the ability of microorganisms to adhere, survive, and grow on surfaces. Among them, the addition of active compounds at the surface of different materials and equipment takes a large part. One other approach is to work with inorganic materials having inherent antimicrobial properties, such as silver [14
], and copper. The capacity of copper surface to kill a wide range of bacterial, viral, and fungal species was highlighted through in vitro tests, demonstrating the antimicrobial activity of copper ions [18
], oxides [19
], and solid copper surfaces [20
] under specific conditions. The key of copper antimicrobial activity is ions releasing from the surface [29
]. On dry metallic copper surfaces, copper ions are released from the surface due to environmental humidity. Nevertheless, the contact between copper surface and bacterial cell wall components seems to be sufficient to trigger a release of copper ions from the surface [30
]. Copper ions will then induce damages to bacterial cell wall and membranes, production of reactive oxygen species, and degradation of DNA, resulting in rapid cell death [29
Nevertheless, the persistence of the antibacterial activity of metallic copper surfaces is still in debate. In this study, the ability of in situ copper alloys door handles and handrails to reduce the bacterial burden in five French long-term care facilities was investigated over a three years period of time. In addition, in vitro tests with MRSA were done on copper door handles that were collected in these long-term care facilities at different moments.
The spread of infections in healthcare facilities is an accurate problem, notably through inanimate surfaces contamination [8
]. A simple gesture such as “holding a door handle” can participate to a wide and fast dispersion of pathogens and favor the cross-contamination between inanimate surfaces and patients. Indeed, inanimate surfaces play an important role as a microbial beholder, despite hand-washing, which currently remains the primordial step against pathogens dissemination. To fight against microbial dissemination, new disinfection methods are being developed. Nevertheless, bacteria can still rapidly recolonize touch surfaces, especially multidrug resistant bacteria that are frequently found in healthcare facilities [13
]. Given this context, the use of copper surfaces brings a new perspective for constant and inherent disinfection. In this study, we investigated the antimicrobial properties of door handles and handrails containing copper that have been used on a daily base in five long-term care facilities.
Independently of the type, size, or localization of the establishments (city, countryside), the median contaminations levels observed were always lower on copper surfaces than on the control surfaces (Figure 2
). The estimate average bacterial burden reduction on copper was 59% for door handles and 33% for handrails. When compared to similar in situ investigations [34
], these reduction levels may seem lower than those that were observed in several other studies [34
] reaching, for some types of furniture, 90% of reduction [41
], but obviously, several different experimental points between these studies and ours can potentially explain these differences.
First, those studies mainly focused on hospital wards, while our study focused on five long-term care facilities, where different types of peoples are moving and meeting (patients-residents/staff/visitors). Different human populations can convey different microbiomes and bacterial burdens, directly impacting bacterial contamination on touch surfaces.
Second, the sampling protocols are quite different. The difference in sampling protocols may induce performance variations in the bacterial recovery. To collect bacteria from touch surfaces, we used a moistened cotton swab. Among others techniques, such as contact agar plates or wipes [35
], swabbing is preferred to perform samplings on small area and non-flat surfaces [34
], like the door handles and handrails of this study. Due to the size and form of the copper door handles, the area of 10 cm2
was used here as the standard area to sample, which is a smaller surface than in several other studies where sampled areas were frequently up to 100 cm2
or more [35
]. Also, peptone water was used as resuspension medium for bacteria, while other studies used media like saline water (0.9%) [34
] or neutralizing buffers [35
]. All of these experimental factors combined can lead to differences in the results.
Third and maybe the most important, copper alloys compositions are probably very different from one study to another. Even if the percentage of copper is known, minor elements can have a huge importance in the antimicrobial efficiency of the alloy [23
In our study, the cleaning protocols remained unchanged after the copper surfaces set-up in four of the five long-term care facilities and are different when compared to those that were used in other studies [34
]. Indeed, the regular use of classic disinfectants or cleaning solutions can somehow modify the copper surface and lead to a loss of the surface antibacterial activity. Such antagonist effects between cleaning solutions and copper surfaces have already been pointed out [39
]. Mikolay et al. [39
] observed low bacterial burden reductions by copper surface, ranging from 0% to 40%. They suggested that these values were due to the daily cleaning solution used in the hospital, proposing that the glucoprotamin, a bactericidal compound that is present in the solution, may form a thin layer on copper surface, thus protecting environmental bacteria from direct contact with copper. These results indicate that the use of an appropriate disinfectant or cleaning solution for copper surfaces and the application of a specific upkeep protocol could lead to an even better and stable copper antimicrobial activity.
Looking individually at the five establishments, singularities in the bacterial burden levels have been observed. Highest global contaminations were found in long-term care facilities E, on both control (median of door handles, 7 CFU/cm2; median of handrails, 7 CFU/cm2) and copper (median on door handles, 3 CFU/cm2; median on handrails, 4 CFU/cm2). Interestingly, it is, by far, the largest long-term care facility of the study, with a capacity of 347 residents and a number of 193 employees. Potentially, a higher number of people in an establishment may induce a more intensive use of surfaces, and then results in higher levels of surface contaminations, but also on a faster lowering of the antibacterial activity of copper by oxidation or dirt accumulation.
The values of bacterial burden were very variable between the establishments and inside each establishment, ranging from <1 CFU/cm2
to >2000 CFU/cm2
. High-level contaminations, depending on numerous parameters (humidity, temperature, time delay between contamination, and sampling) stochastically occurred on touch surfaces in long-term care facilities during the study. Our results showed that copper surfaces are less subject to these extreme contaminations, this frequency being reduced by 50% on copper handrail and by 79% on door handles. The average reductions of bacterial burden, as well as the 4,6 times decrease of high contaminations (>20 CFU/cm2
) on copper door handles as compared to control handles, (Figure 1
) suggest that door handles display a stronger antibacterial activity than handrails. These differences in activity between the door handles and handrails may depend in many factors, including the cleaning protocols that are different for door handle and handrail, the way the two types of items are used by the persons and most probably the difference in the percentage of copper, door handles having a higher copper percentage (90% vs. 70%) and being more active against bacteria than handrails.
No correlation was highlighted between contaminations levels and external temperature when sampling was carried out (data not shown). Nevertheless, it cannot be excluded that the period of the year has a slight effect on the global bacterial populations (temperature, humidity, wintry and summer infections, percentage of sick residents). In addition, statistical correlation indicates that the medians of bacterial burden on copper surfaces correlates with the medians that were observed on control, demonstrating that the global bacterial burden levels on touch surfaces are influenced by forces depending on the facility and the period of time. Taking all into account, the overall bacterial burden levels were lower on copper surfaces, and this was observed in the five establishments, one year and three years after copper set-up, for both door handle and handrails (Figure 3
). Thereby, regardless of the healthcare facilities, copper surfaces maintained their antibacterial activity.
To see if this antibacterial activity was still relevant against MRSA, in vitro contaminations were assayed (Figure 4
). MRSA is a pathogen that is frequently involved in healthcare-associated infections [2
] and is regularly found on healthcare touch surfaces [46
], where it can potentially persist under environmental conditions for months [12
]. Here, we highlighted that, after three years of normal use in healthcare facilities, the copper handles maintain their activity against this pathogen, with a reduction superior to 90% for most of the tested copper door handles, as compared to the residual burden on glass and stainless steel door handles. The efficiency of the copper surfaces, however, seems to slowly decrease with time. While new copper door handles allowed an average 3.2 logs reduction of number of MRSA within two hours, the reduction dropped to 2.7 logs after one year and 1.7 logs after three years of use. Still, copper surfaces remain an interesting long-term solution to fight against touch surface contaminations, especially if installed in the whole facility. Also, as mentioned before, the cleaning protocols remained identical than before the set-up of copper surfaces and other studies have already suggested that cleaning solutions may have an antagonist effect on copper antimicrobial activity [39
]. Yet, even if using these inadequate solutions for more than three years, copper surfaces still demonstrate a significant impact against MRSA.