1. Introduction
In the last few decades hospitals had to face several difficult challenges: an increasing proportion of immunologically vulnerable patients, rapidly evolving medical technologies and healthcare models, budget restrictions, and new health emergencies [
1]. All these features interfere with healthcare and can also modify the risk of acquiring healthcare-associated infections (HCAIs).
Among hospital’s wards, intensive care units (ICU) are one of the areas more involved in these challenges, since they are specialized divisions, which provide close monitoring and support to threatened or failing vital functions in critically ill patients who suffer from illnesses with the potential to endanger life, and perform adequate diagnostic measures and medical or surgical therapies to improve outcome [
2]. These units include several categories: neonatal ICUs, cardiac ICUs, neurological ICUs, surgical ICUs, medical ICUs, etc. Each of them has different characteristics and requirements, depending on the type of patient and disease.
The ICUs in hospitals have been the subject of many studies in the last two decades. Particular attention has been devoted to the role of infection control, but also to the built environment requirements, and also considering the increased demand emerging from the recent COVID-19 global pandemic.
Depending on the underlying disease, duration of stay and treatment, patients admitted to these units may show higher susceptibility to HAIs than healthy individuals. Some peculiar risk factors are the frequency of contact with healthcare workers (in particular with their hands), the number of colonized or infected patients in the same ward and the lack of compliance with infection prevention guidelines [
3]. ICUs’ rooms layout can also affect the risk of infection [
3], and the patient’s safety in a broad sense [
4]. A recent review [
5], analyzing the role of rooms design, shows that although several studies report a protective effect of single-bed ICU rooms versus patients’ antibiotic-resistant infections during their stay [
6,
7], or to nosocomial infection rate compared to a multibed unit [
8], other studies demonstrated no association [
9] or weaker associations [
10], suggesting that the main benefit of the unit design is to facilitate appropriate personnel behavior and that, consequently, design features are subordinate to more primary drivers of infection control, such as personnel behaviors [
11].
Regardless, ICUs’ environments are considered potential reservoirs for (opportunistic) pathogenic microbial strains [
12] able to survive and multiply on the medical equipment and in the surrounding environment [
13,
14]. In fact, several vehicles (i.e., surfaces, equipment, hospital textiles, air, etc.) can be a source of microorganisms and infections [
15,
16,
17,
18]. For example, some non-invasive devices, such as electrical equipment and devices that are difficult to clean due to their irregular shape, have been reported as a source for infection [
12]. Soiled or contaminated bed linen and pajamas, or privacy curtains, can also spread microorganisms during their handling [
19]. The same infected patients can act as a source of microorganisms and, in some studies, the surfaces close to the patient, frequently touched by them, resulted in being heavily contaminated [
20,
21]. It has been reported that the risk of acquiring a nosocomial infection increased significantly when the total microbial burden of the surface exceeded 500 CFU/100 cm
2 [
18]. For these reasons ICUs are included among the hospital environments at high risk and classified as ISO class 8 [
22], comparable to a grade C–D clean room following EU Guidelines to Good Manufacturing Practice Medical Products for Human and Veterinary Use [
23]. For these environments a heating, ventilation and air conditioning (HVAC) system is recommended, equipped with positive or neutral pressure and different level of air filtration depending on the type of ICU (general, burn, neonate, etc.) and the Country [
24].
In the ICUs, microbial concentrations in air and on surfaces must meet specific requirements to guarantee the safety of patients, medical staff and visitors [
4].
In particular, national and international guidelines and regulations report standards on the level of contamination of air and surfaces [
11,
25,
26,
27,
28].
Different strategies have been adopted to evaluate the environmental biocontamination. The US Centers for Disease Control and Prevention recommend environmental sampling only to support an investigation of an outbreak of disease or infections where environmental reservoirs or fomites are epidemiologically implicated in disease transmission [
29]. Other researchers recommend a periodic monitoring of high-risk environments to verify the absence of anomalies in the air treatment systems and the level of application of all the cleaning procedures, especially for protected areas [
30,
31]. Regarding the sampling method, several researchers prefer the sampling of surfaces rather than active air sampling, due to the higher reliability of results and the lower costs of investigations [
31]. The active sampling provides information about the concentration of viable particles in the air [
30], whereas surface sampling may be more sensitive for some microorganisms (e.g., molds), because they may settle on surfaces and remain for a long time, especially on electric devices [
32]. However, which microbiological environmental sampling approach to prefer is an unresolved issue; the lack of standardized protocols and reference values for environmental surveillance, recognized at national and international level, leave the choice to each hospital in terms of where, when, why and how to detect environmental microorganisms.
In this paper we describe the trend of environmental bacterial pollution observed in some ICUs of hospital buildings of the city of Rome (Italy), considering their activities, layout and structural characteristics, to evaluate changes in bacterial pollution among and within ICUs over time and to suggest preventive actions and design solutions to improve the hygienic standards and the safety of patients and healthcare workers.
4. Discussion and Conclusions
The investigated ICUs show different size (rooms), functional layout and assistance targets. The ICUs 2, 3 and 4 are all single multi-bed rooms, while ICU 1 includes single-bed and multi-bed rooms. ICU 5 has baby-incubators distributed in four rooms.
These characteristics are coherent with Italian regulations [
25,
26], following which the ICUs rooms can be single-bed or multiple-bed. In general, the guidelines support the option that single rooms are superior to multi-bed rooms in terms of patient safety [
8,
16,
39,
40,
41,
42], of privacy and sleeping quality [
43]. In the literature there is not agreement about the protective effect of single-bed ICU rooms from nosocomial infection rate if compared to a multibed unit. Many studies consider the design features subordinate to other drivers of infection control, such as, for example, ICU management. The functional layout is mainly finalized to favor appropriate personnel behavior and its efficiency, rather than to contain the infection risk [
11].
Another critical aspect is the ICUs’ size. In the Italian regulation [
25,
26] their sizes vary between newly built ICUs or restructured, or between single-bed or multiple-bed ICUs. For newly built ICUs the minimum surface area for a single room is 20 and 16 m
2 per bed for a multiple-bed ICU, with a distance between beds of ≥ 2.5 m. For already existing ICUs, the minimum surface area for each single-bed room is 16 and 12 m
2 per bed for a multi-bed ICU, except for Neurovascular ICUs in which the minimum surface is 9 m
2 per bed. The importance of increasing the distance between beds is a basic recommendation in hospital environments mainly to reduce the spread of respiratory infections (e.g., tuberculosis), and it is currently the main preventive measure to counteract the spread of all indirectly transmitted infections, Covid-19 included, together with hand washing and the use of protective devices [
44,
45,
46]. Other countries (e.g., USA, Australia) define different size standards, generally larger [
27,
28]. The role of design should be to reduce travel distances for staff, placing frequently needed spaces, equipment or materials as close as possible to the site of use. On this topic, we agree with Thompson et al. [
39], who considers as efficient a unit small enough for care providers to be fully aware of all activities, yet large enough to permit safety and efficiency. It is not a matter of choosing a centralized or decentralized design, it is important that caregivers are allowed to observe patients from many points within the unit [
8].
The investigated ICUs were all equipped with HVAC systems, since they are specific requirements reported in the Italian regulation [
25,
26]. In particular, the regulation indicates the following standards: a temperature between 20 and 24°, a relative humidity between 40 and 60% and at least six air changes/hour (ACH). A higher temperature range is recommended for Neurovascular ICUs (20–26°) and Neonatal ICUs (20–28°). The high efficiency air filtration is required in all ICUs, excluding Neonatal ICUs. Absolute filtration (≥99.95%) is required for isolation rooms only. The positive pressure is required in neonatal ICUs, while in other types of ICUs (resuscitation, cardiology, neurovascular) the pressure can be positive or negative (+ or −10 Pa), according to needs. During the current COVID-19 pandemic, for example, some authors recommended to place intensive care rooms under negative or even normal pressure to protect the staff and patients’ health [
47], but it has been observed that this solution increased the risk of opportunistic infections in immunocompromised patients [
48].
In a relevant number of samplings the investigated ICUs showed microclimatic parameters levels that were not compliant with the regulations reported above [
25,
26]. This situation could depend on several factors. First of all, the opening of doors inside the ICUs environments; in fact, during sampling campaigns the doors were frequently found open. This habit, also observed in other investigations [
30,
49,
50,
51], is deleterious, since it modifies the microclimatic conditions and it hinders the ICUs’ pressurization. A limit of this investigation is that the number of air changes/hour (ACH) and the air pressurization were not measured; therefore it is difficult to try to make robust conclusions about the role of building and HVAC characteristics on the concentrations of air sampled microbes. These parameters will be included in future investigations regarding these ICUs.
Secondly, the periodic maintenance of HVAC systems could be insufficient, since it generally occurs once a year in these environments. In particular, the air velocity resulted as compliant in 56.1% of samplings only, resulting lower than 0.05 m/sec in the others; this condition could be related to a shortage of the filters maintenance (e.g., filters saturation). This is another aspect to investigate in the future.
Coming back to the bacterial pollution described in this study, while a general decreasing trend of air contamination during the years is observed, the surfaces contamination does not show a significant improvement. In particular, ICU 4 and ICU 5 have shown an average air contamination > 200 CFU/m
3, but a significant improvement has occurred in ICU 5 only. This Neonatal ICU is equipped with a decentralized HVAC system. The improvement could be related to a higher respect of a periodic filter’s maintenance. Contrariwise, in this ICU, as in the other ICUs investigated, the contamination of surfaces does not show a significant improvement. It could depend on the average acceptable level of CFU/plate observed in all ICUs. Regardless, 28% of samples were contaminated (>50 CFU/plate), supporting the need to review cleaning protocols and personnel’s behaviors. Actually, as already described in a previous study [
52,
53], the lack of knowledge is the major reason for non-adherence to procedures and education is an important factor to influence compliance with good practices. At the same time, an efficient service requires an adequate staff (e.g., nurses) in terms of competence and numerosity.
As reported in the literature [
14,
21], several frequently touched surfaces have shown a high level of contamination. Many of them exceeded the threshold level of infection risk, as indicated by Salgado et al. [
18]; in particular over-bed surfaces, infusion pumps and baby incubators. While in ICU 4 they were reduced along the years, a particular attention should be given to ICU 1, since all these over-threshold samples have been collected in the last years (after 2015). This ICU also shows the lowest percentage of compliant samples in terms of microclimatic conditions. It means that it will be necessary to focus attention on this issue to increase patients’ and healthcare workers’ safety and comfort. At the same time it is important to reduce the number of people and their movements inside the ICUs’ environments, since the direct correlation between microbial pollution and number of people is well documented (e.g., operating rooms) [
30,
49,
54,
55]. Unfortunately, the occupational density during the samplings was not measured in this investigation and it is a limit of the study, since the number of occupants had certainly impacted the concentration of microbes in air samples significantly and could have helped to better understand the causes of the observed problems. This aspect will also be taken into account in the future investigations.
In conclusion, the care for patients admitted to ICUs is very demanding and consists of a complex of medical procedures, whose complexity depends on the underlying disease. A fundamental part of intensive care is prevention of infection. This study dealt with microbial contamination in different types of ICUs, monitoring both air and surfaces contamination, but also considering their environmental characteristics and type of activity. Several criticalities have been observed that allowed us to identify priorities and areas with major intervention needs.