Next Article in Journal
Deformation Analysis of the Rock Surrounding a Tunnel Excavated through a Gently Dipping Bed
Next Article in Special Issue
The Effect of Students, Computers, and Air Purifiers on Classroom Air Quality
Previous Article in Journal
Application of Deep Learning to Construct Breast Cancer Diagnosis Model
 
 
Search for Articles:
Title / Keyword
Author / Affiliation / Email
Journal
Article Type
 
 
Advanced Search
 
Section
Special Issue
Volume
Issue
Number
Page
 
Journals
Applied Sciences
Volume 12
Issue 4
10.3390/app12041958
applsci-logo
Submit to this Journal Review for this Journal Propose a Special Issue
► Article Menu

Article Menu

share Share announcement Help format_quote Cite question_answer Discuss in SciProfiles thumb_up
...
Endorse textsms
...
Comment
first_page
settings
Order Article Reprints
Font Type:
Arial Georgia Verdana
Font Size:
Aa Aa Aa
Line Spacing:
Column Width:
Background:
Review

Exposure and Health Effects of Bacteria in Healthcare Units: An Overview

by
Ana Monteiro
1,2,3,*,
Jéssica Cardoso
4,
Nuno Guerra
4,
Edna Ribeiro
1,
Carla Viegas
1,5,
Sandra Cabo Verde
3 and
António Sousa-Uva
2,5
1
H&TRC—Health & Technology Research Center, ESTeSL—Escola Superior de Tecnologia da Saúde, Instituto Politécnico de Lisboa, 1600-560 Lisbon, Portugal
2
Escola Nacional de Saúde Pública, Universidade NOVA de Lisboa, 1600-560 Lisbon, Portugal
3
Centro de Ciências e Tecnologias Nucleares (C2TN), Instituto Superior Técnico, Universidade de Lisboa, 1600-560 Lisbon, Portugal
4
Escola Superior de Tecnologia da Saúde de Lisboa, Instituto Politécnico de Lisboa, 1600-560 Lisbon, Portugal
5
Centro de Investigação em Saúde Pública, Universidade NOVA de Lisboa, 1600-560 Lisbon, Portugal
*
Author to whom correspondence should be addressed.
Appl. Sci. 2022, 12(4), 1958; https://doi.org/10.3390/app12041958
Submission received: 11 January 2022 / Revised: 9 February 2022 / Accepted: 10 February 2022 / Published: 13 February 2022
(This article belongs to the Special Issue Air Quality in Indoor Environments)
Browse Figure
Versions Notes

Abstract

:
Healthcare units consist of numerous people circulating daily, such as workers, patients, and companions, and these people are vehicles for the transmission of microorganisms, such as bacteria. Bacteria species may have different allergenic, pathogenic, infectious, or toxic properties that can affect humans. Hospital settings foment the proliferation of bacteria due to characteristics present in the indoor hospital environment. This review article aims to identify the potential health effects caused by bacterial contamination in the context of healthcare units, both in patients and in workers. A search was carried out for articles published in PubMed, Web of Science and Scopus, between 1 January 2000 and 31 October 2021, using the descriptor hospital exposure assessment bacteria. This bibliographic research found a total of 13 articles. Bacteria transmission occurs mainly due to the contact between healthcare workers and patients or through the handling of/contact with contaminated instruments or surfaces. The most common bacterial contaminants are Escherichia coli, Pseudomonas aeruginosa, Staphylococcus spp., Staphylococcus aureus and Micrococcus luteus, and the principal health effects of these contaminants are hospital-acquired infections and infections in immunocompromised people. A tight control of the disinfection methods is thus required, and its frequency must be increased to remove the microbial contamination of wards, surfaces and equipment. A better understanding of seasonal variations is important to prevent peaks of contamination.

1. Introduction

Infections associated with healthcare units are a major public health problem that concerns patients, the public, and politicians, since they impact society’s development [1]. These infections lead to significant mortality and financial losses for health systems each year. Therefore, the rate of infection associated with healthcare units is not only an indicator of patient safety but also of the global healthcare quality provided in hospitals [2,3,4]. According to the World Health Organization (WHO), for every 100 hospitalized patients at any given time, 7 in developed countries and 10 in developing countries will acquire at least one healthcare-associated infection [2]. Another survey indicated that 1 in 17 hospitalized patients who received healthcare-associated infections (while being treated for other health issues) died as a result [5].
Healthcare units such as hospitals, maternity centers, blood banks, clinics, medical offices, urgent care centers, or healthcare centers consist of countless people circulating daily, such as workers, patients and their companions, the healthy and the sick. These people are vehicles for transmitting microorganisms, such as bacteria, that can cause infections that are transmitted very easily in this setting due to its population of sick or immunocompromised people [6].
Additionally, bacterial contamination in hospitals is heavily affected by the following important factors: construction characteristics, levels of water and nutrients in the interior environment necessary for the growth and survival of bacteria, people that occupy the space, and the outdoor environment [7]. Medical activities, cleaning procedures and their frequency are crucial factors for the increase in bacterial load [8,9].
Bacterial species have different allergenic, pathogenic, infectious, or toxic properties that can affect humans [10]. Allergenic bacteria, mainly thermophilic bacteria, may generate a hypersensitivity response (hypersensitivity pneumonitis) in the host [10]. A pathogenic bacterium causes disease in a host and is determined by virulence factors, enabling the replication and dissemination of bacteria in the host organism [11,12]. Bacteria infect a host, usually from another host/reservoir, through direct contact, airborne transmission, a vector, or a common vehicle [10]. In addition, bacteria can produce toxins, which trigger a harmful process in the host organism, inhibiting protein synthesis, activating immune responses, and damaging cell membranes [13]. Bacterial cell wall constituents, such as endotoxins and peptidoglycans, are referred to as agents with pro-inflammatory properties causative of respiratory symptoms (asthma, bronchitis and byssinosis) [10].
The transmission of bacteria can be promoted because healthcare workers interact physically with different patients, unaware that they are transmitting potentially pathogenic agents. Additionally, the handling/contact with contaminated instruments or surfaces [14,15] can cause a risk of infection in both workers [16] and patients. In fact, the isolation of microorganisms from the surfaces suggests that some patients acquire bacterial infections in the hospital [17,18,19,20].
Hospital-acquired (nosocomial) infections are a concern in terms of patient safety, as they may have a high impact on patient morbidity and mortality [21,22].
Commonly, most bacteria do not cause adverse health effects and can even benefit us and the environment. The problem arises when the concentration of certain potentially pathogenic bacteria is higher than the infective dose, which varies dramatically across pathogen species [23]. The scale of the severity of the effects on human health depends on many factors such as toxicity, exposure time and microbial load, and even one’s age and nutritional status [24]. For example, bacteria such as Acinetobacter baumannii, Pseudomonas aeruginosa and Stenotrophomonas maltophiliam, which are non-fermenting Gram-negative bacilli, can cause infections and severe health problems. These bacteria have been recognized as multidrug-resistant (MDR) and are associated with higher rates of mortality, increased service costs, and a poorer clinical outcome [25,26,27,28]. Additionally, Burkholderia cepacia complex (Bcc), which are a non-fermenting Gram-negative bacillus, consist of 20 species that are similar in phenotype and genetically different [29]. During the last two decades, Bcc were considered the most common bacteria in intensive care units, and recognized as a nosocomial pathogen, associated with several outbreaks in immunocompromised patients [28], such as bloodstream infections, pneumonia, urinary tract infections, septic arthritis, and peritonitis [30,31].
For the healthcare sector, the priority is to reduce, prevent and monitor infections to provide a high-quality service with the fewest number of health conditions. Therefore, healthcare units must adopt strategies and systems of epidemiologic surveillance to control infections.
In order to improve public health, this article intends to describe prevalent bacteria and identify their potential health effects in the context of healthcare units, both in patients and in workers. For these, it is important to assess the factors that influence bacterial contamination in this setting. This will ultimately contribute to the prioritization of actions to establish procedures for evaluating occupational exposure, protocols, and guidelines adaptable to healthcare units, which have an increased risk of the transmission of infections due to prolonged exposure periods and the high density of people.

2. Materials and Methods

2.1. Systematic Review Registration

The protocol of this systematic review was submitted for registration in PROSPERO (https://www.crd.york.ac.uk/prospero/, accessed on 18 December 2021 ) (Registration Number: 291564). Moreover, the Preferred Reporting Items for Systematic Reviews (PRISMA) checklist was completed (Table S1—Supplementary Material).

2.2. Search Strategy and Inclusion and Exclusion Criteria

In this study, available data on the exposure assessment of bacteria, including hospitals and healthcare units, published between 1 January 2000 and 31 October 2021, were searched following the Preferred Reporting Items for Systematic Reviews and Meta-Analysis methodology. The databases chosen were PubMed, Web of Science, and Scopus. Searches were carried out in English. The search terms were “Exposure assessment bacteria” and “Hospital” and “Health Care Units”. Articles that did not meet the inclusion criteria and duplicates were excluded from further analysis (Table 1).

2.3. Studies Selection and Data Extraction

Initially, all titles and abstracts were selected, and then only the full texts of all potentially relevant studies were reviewed, considering the inclusion and exclusion criteria. The following information was manually selected: (1) title, (2) analyzed country, (3) analyzed environment, (4) collected data, (5) results, (6) bacteria found, (7) health effects and (8) affected population.

2.4. Quality Assessment

In each study, we assessed the bacterial results, type of bacteria found, and health effects in order to eliminate the risk of bias and ensure that each study was complying with the inclusion criteria focused on bacterial contamination, health effects and the fact that the study was performed in a clinical environment.

3. Results

Figure 1 illustrates the process used to identify and select the articles for analysis. The primary search on the databases returned 1049 studies from which 1003 abstracts were screened, and 125 full texts were assessed for eligibility. After considering the inclusion and exclusion criteria, we were able to select 44 articles. This review is centered on 13 articles about the context of exposure assessment bacteria in hospital and healthcare units.

3.1. Characteristics of the Selected Studies

The selected articles (13) were studied in terms of reference values of bacteria and health effects that could be caused by bacteria. The obtained data can be found in Table 2. These studies were conducted in several countries such as Italy, Poland, The United States of America, Korea, Pakistan, Greece, Uganda, Iran, Brazil, and Tehran. For the assessment of bacteria, more than half of the studies used air samples (7 out of 13), others used settle plates and swab methods, and some did not disclose the method used to assess bacteria.

3.1.1. Reference Values for Bacteria

Regarding the reference values for bacteria, the median level of colony forming units (CFU) in the wards of hospital 1 was 129.87 (87.46–268.97) CFU/m3 and, for hospital 2, was 297.97 (217.66–431.85) CFU/m3 [32], both part of a teaching hospital in Tehran. A study conducted in a Brazilian hospital reported median bacterial loads of 345.25 CFU/m3 in the post-surgical restroom and 566 CFU/m3 in operating theatres [33]. Another study in a hospital from Poland reported a median bacterial load of 347.4 CFU/m3 (257.1–436.3 CFU/m3) [34]. In a university hospital from Greece, the highest mean total microbial load (689 CFU/m3) and the highest Gram-negative bacteria load (4.16 CFU/m3) were observed in the intensive medicine ward [35]. A study dedicated to hospitals in the USA observed a mean bacterial load of 720 CFU/m3 [36]. Some of the analyzed articles did not quantify the bacterial contamination found (5 out of 13).

3.1.2. Seasonal Variation

Peak values of airborne bacteria occurred in November and May, and the lowest values were recorded between December and February [34], not specifying the month. Park et al. [36] concluded that winter was shown to have a lower bacterial concentration (mean) 230 CFU/m3 (14 samples), while summer had the highest, 970 CFU/m3 (25 samples). Considering the effect of the time of day, studies suggested that the concentrations in the morning (9 h) ranged between 267.1–505.6 CFU/m3 and in the afternoon (13 h), 213.6–410.9 CFU/m3 [34]. In another hospital the main concentration of bacteria was found during service hours (8 h–18 h) with an average of 930 CFU/m3 [36].
In the waiting rooms of primary healthcare units and hospital wards [37], mesophilic bacteria were the highest at 297 CFU/m3 in autumn. Airborne Staphylococci peaked at 96 CFU/m3 in winter (cardiology ward and intensive care room). The concentration of airborne actinomycetes was 231 CFU/m3 in winter (children’s ward).

3.1.3. Prevalent Bacteria

Several studies reported the variability of prevalent bacteria in hospital settings. For example, a gynecology theatre from a hospital in Italy [38] presented the highest bacterial load of 261.3 ± 131.3 CFU/dm2/h, with a prevalence of Pseudomonas spp. (25.8%), and the ophthalmology theatre had the highest concentration of microbial pathogens (38.9%), being 22% of Pseudomonas species and 18.7% of Bacillus spp. [38]. In other hospital wards and operating theatres [39], the bacterial concentration ranged from 1.27 × 104 to 17.83 × 104 CFU/dm2/h.
In an Italian hospital [40], the group of workers with the highest number of infections by H. pylori were physicians (16 out of 47) and nurses (18 out of 45). Both groups worked in the endoscopy unit; nurses (30 out of 75) worked in direct contact with patients but did not work in the endoscopy unit.
In terms of prevalent bacteria found in the air, the most mentioned was Escherichia coli, found in patients on a ward [34] in a Pakistan hospital [41] and in operating beds in Uganda [38]. Additionally, Pseudomonas aeruginosa was reported in the air of a hospital ward [34] in a Tehran teaching hospital [32], and in patients from a Pakistan hospital [41], in the gynecology theatre, main operating theatre, and on the instrument trolley. Pseudomonas spp. showed a higher prevalence, even though the species were not specified [38]. S. aureus were another common bacteria species found in patients from a Pakistan hospital [41], on the door handles of a Ugandan operating theatre [38], and in several wards in a Tehran hospital [32]. Staphylococcus spp. was detected in the air from a university hospital in Greece [35], in a Ugandan operating theatre [38] and in primary healthcare units and hospital wards in Poland [37]. Micrococcus luteus was found in the female surgery and male surgery wards in an Iranian hospital [39] and in a Brazilian hospital [33]. Other bacteria were mentioned, such as H. pylori [40], Staphylococcus epidermidis, Micrococcus, Streptococcus Flavobacterium spp., Acinetobacter calcoaceticus, Pantoea agglomerans, Enterobacter spp., Klebsiella oxytoca, Branhamella catarrhalis and Neisseria flavescens, Arthrobacter spp., Brevibacterium spp [34], Clostridium difficile [42], Gram-negative bacilli (XDR-GNB) [43], Haemophilus influenzae [41], Bacillus spp. [38], Staphylococcus epidermidis, Streptococcus spp., Diphtheroid spp., Micrococcus roseus, Bacillus subtilis. [39], mesophilic bacteria, airborne actinomycetes, S. saprophyticus, S. warneri [37], S. haemolyticus and S. hominis [33], Acinetobacter lwoffii, Salmonella typhimuriu and Klebsiella pneumonia [32].

3.1.4. Health Effects

Regarding health effects, the most prevalent bacteria-associated effects were hospital-acquired infections caused by Gram-positive bacteria and antibiotic-resistant Gram-negative bacteria [34,43], followed by nosocomial diarrhea caused by Clostridium difficile [42,44], nosocomial infections, and infections in immunocompromised people [33,37]. The other infections reported were bloodstream infections [33]; osteoarticular infections [41]; respiratory and infection diseases [36]; allergenic properties [34]; chronic active gastritis; gastric and duodenal ulcers [40]; osteomyelitis [41]; bacteremia; infections of skin, bones and joints; endocarditis; and central venous catheter infection [33].
Table
Table 2. Information obtained from the articles selected.
Table 2. Information obtained from the articles selected.
TitleCountryAnalyzed
Environment		Collected DataResultsBacteria FoundHealth EffectsAffected PopulationReferences
PubMedDoes Hospital Work Constitute a Risk Factor for Helicobacter Pylori Infection?ItalyHospitalA questionnaire was completed by participants before collection of fecal specimens.249 workers tested positive for H. pylori.: 16 out of 47 physicians (endoscopy unit); 18 out of 45 nurses (endoscopy unit); 5 out of 30 physicians (only contact with patients); 30 out of 75 nurses (only contact with patients); 9 out of 52 healthcare personnel (no patient contact).H. pyloriHelicobacter pyloriinfection likely represents the most common bacterial infection of the human species, with a prevalence of 25–50% in developed countries and up to 90% in developing countries. A vast body of evidence now indicates that H.pylori is the principal etiological agent of chronic active gastritis, as well as gastric and duodenal ulcers, and represents a major risk factor for the development of gastric cancer.Workers[40]
PubMedVariability of Airborne Microflora in a Hospital Ward Within a Period of One YearPolandHospital (ward)Air samplesConcentrations of airborne bacteria: 257.1–436.3 CFU/m3, peak values—November and May, lowest values—December to February; Gram-positive cocci: 31.4–46.4% of the total count and 37.2–49.6% of the respirable fraction; Gram-negative bacteria: 11.8–27.5% of the total count and 5.6–30.2% of the respirable fraction.Staphylococcus epidermidis, Micrococcus, Streptococcus Flavobacterium spp., Acinetobacter calcoaceticus, Pantoea agglomerans, Escherichia coli, Enterobacter spp., Klebsiella oxytoca, Pseudomonas aeruginosa, Branhamella catarrhalis and Neisseria flavescens, Arthrobacter spp., Brevibacterium spp.The risk of exposure to Staphylococci was diminished by the fact that the isolated strains were coagulase-negative and unlikely to cause infections. Gram-negative bacteria found in the air of the hospital ward could be a source of adverse endotoxin, and Acinetobacter strains may be a potential cause of hospital infections transmitted by air. Some of the Gram-positive isolates belonging to corynebacteria and actinomycetes (Arthrobacter spp., Brevibacterium spp., Streptomyces albus) show allergenic properties.Patients[34]
PubMedClostridium Difficile Infection in Hospitalized Children in the United StatesUnited StatesHospitalData were obtained from the triennial Healthcare Cost and Utilization Project Kids’ Inpatient Database (HCUP-KID) Clostridium difficile infections increased from 3.565 in 1997 to 7.779 in 2006; Clostridium difficile infections had an increased risk of death with an adjusted odds ratio (95% confidence interval); 1.20 (1.01–1.43), colectomy; 1.36 (1.04–1.79), longer length of stay; 4.34 (3.97–4.83) and higher charges; 2.12 (1.98–2.26).Clostridium difficileClostridium difficile is a Gram-positive, spore-forming, anaerobic bacillus that can colonize the gastrointestinal tract and can lead to C difficile infection (CDI). CDI has a wide variation of severity, ranging from asymptomatic colonization to severe diarrhea, pseudomembranous colitis, toxic megacolon, bowel perforation, and death.Patients (children)[42]
PubMedTrends in Clostridium Difficile Infection and Risk Factors for Hospital Acquisition of Clostridium Difficile Among Children With CancerUnited StatesHospital Clostridium difficile infection (CDI) is the most common cause of nosocomial diarrhea and can lead to a range of complications from colitis to toxic megacolon, bowel perforation, and death. CDI is a significant cause of nosocomial and antibiotic-associated diarrhea in adults, with increasing frequency and severity.Patients (children)[44]
PubmedAssessment of the Levels of Airborne Bacteria, Gram- Negative Bacteria, and Fungi in Hospital LobbiesKoreaHospital LobbiesAir samplesMean level of airborne bacteria: 7.2 × 102 CFU/m3; service hours (08 h–18 h): 9.3 × 102 CFU/m3 (mean); after service hours (18 h–24 h): 4.4 × 102 CFU/m3; winter: 2.3 × 102 CFU/m3 (mean); summer: 9.7 × 102 CFU/m3 (mean); Gram- negative bacteria mean: 1.7 × 10 CFU/m3. All occupants[36]
PubMedRisk Factors and Outcomes of Infections Caused by Extremely Drug-Resistant Gram-Negative Bacilli in Patients Hospitalized in Intensive Care UnitsUnited StatesICUsA matched case–control (1:2) study was conducted from February 2007 to January 2010 in 16 ICUs. An immunocompromised state (OR = 1.55, p = 0.047) and exposure to amikacin (OR = 13.81, p < 0.001), levofloxacin (OR = 2.05, p = 0.005), or trimethoprim-sulfamethoxazole (OR = 3.42, p = 0.009) were factors associated with XDR-GNB HAIs.Extremely drug-resistant Gram-negative bacilli (XDR-GNB)Antibiotic-resistant, Gram-negative bacilli (GNB) are increasingly common causes of healthcare-associated infections (HAIs) in intensive care units (ICUs) and are associated with higher mortality rates, longer hospitalizations, and increased healthcare expenditures. Effective treatment for extremely drug-resistant (XDR) GNB infections is challenging because of limited therapeutic options.Patients[43]
Web of ScienceStaph Aureus as the most common cause of osteoarticular infection in Dost-1 Mayo Hospital, LahorePakistanHospitalPatients were followed up in OPD for 24 weeks post operatively to assess the outcome of the procedureCausative organism (200 patients): Staph Aureus in 96% of the patients, Haemophilus influenzae 1.2%, Escherichia Coli was 2% and Pseudomonas Aeruginosa was 0.8%.Staph Aureus, Haemophilus influenzae, Escherichia Coli, Pseudomonas AeruginosaStaph Aureus was the organism which caused osteoarticular infection in 96% of patients.Patients[41]
PubmedAir Contamination in Different Departments of a Tertiary Hospital. Assessment of Microbial Load and of Antimicrobial SusceptibilityGreeceUniversity hospitalAir samplesThe highest mean total microbial load was observed in the IMW (689/m3), followed by the SW (596 CFU/m3), the NU (509 CFU/m3) and, finally, the ICU (353 CFU/m3). The load of GN, the highest load, was observed in the IMW (4.16 CFU/m3), followed by the ICU (1.14 CFU/m3), the SW (0.83 CFU/m3), and the NU (0.81 CFU/m3). In total, 101 samples were collected, from which 158 Gram-positive (GP) and 44 Gram-negative (GN) strains were isolated. The majority of GP isolates were Staphylococcus spp. (n = 100). The highest total microbial load was reported in the IMW (p = 0.005), while the highest Staphylococcus load was observed in the ICU (p = 0.018). All occupants[35]
PubMedContamination of Microbial Pathogens and Their Antimicrobial Pattern in Operating Theatres of Peri- Urban Eastern Uganda: A Cross-Sectional StudyUgandaOperating theatre109 samples (n  =  31 air samples and n  =  78 swabs)Gynecology theatre—261.3 ± 131.3 CFU/dm2/h (Pseudomonas spp.—25.8%); main OT—69.5 ± 78.7–38.9% microbial pathogens (Pseudomonas spp.—22%; Bacillus spp.—18.7%); operating bed (E. coli –77.8%), instrument trolley (Pseudomonas spp.—28.6%), door handles (100% of S. aureus)Pseudomonas spp., coagulase negative staphylococcus, Bacillus spp., E. coli, Staphylococcus aureus Patients[38]
Web of ScienceAssessment of bioaerosol particle characteristics at different hospital wards and operating theatres: A case study in TehranIranHospital (CCU, GICU, ICU, NICU, OT, NS)Passive sampling method (252 plates)Concentration of bacterial: 127 to 1783 CFUm-2 h-1; Micrococcus luteus: NS (41.5%), WS (72.3%), MS (70.0%), ICU (66.2%); Staphylococcus epidermidis: GICU (46.6%, NICU (50.0%); CCU: Streptococcus spp. (53.8%), Micrococcus luteus (46.2%).Micrococcus luteus, Staphylococcus epidermidis, Streptococcus spp., Diphtheroid spp., Micrococcus roseus, Bacillus subtilis. All occupants[39]
PubMedAssessment of Microbiological Aerosol Concentration in Selected Healthcare Facilities in Southern PolandPolandPrimary healthcare units and hospital wardsAir samplesMesophilic bacteria ranged 5 CFU/m3 in winter (No. IV)–297 CFU/m3 in autumn (No. V); airborne Staphylococci ranged 1 CFU/m3 in spring–96 CFU/m3 in winter (both No. IX); airborne actinomycetes ranged 7 CFU/m3 in spring and autumn (No. IV)–231 CFU/m3 in winter (No. VII); 55 isolates strains of Staphylococcus spp.: S. saprophyticus 25% (14), S. warneri 24% (13).Mesophilic Bacteria, Airborne staphylococci, Airborne actinomycetes, Staphylococcus spp., S. saprophyticus, S. warneriNosocomial infections and infections in immunocompromised people.All occupants[37]
web of SiencePotentially pathogenic bacteria isolated from neglected air and surfaces in hospitalsBrazilHospital Air samples, surfaces and uniforms samplesThe highest microbial load was found in the PSRR (566 CFU/m3, Hospital B) and the lowest in the ORT (124.5 CFU/m3, Hospital B).In the aerial microbiota of the sampled areas of both hospitals, M. luteus, S. haemolyticus and S. hominis spp hominis were the prevalent microorganisms, with a percentage greater than 30%. On the surfaces and uniforms, there was a prevalence of M. luteus (40%) and S. hominis spp hominis (20%).S. hominis subsp. hominis is reported as a potential pathogen isolated in generalized infections. M. luteus, found in several sampled environments, is described as the causative agent in endocarditis and central venous catheter infection. Some microorganisms, isolated in low percentages in this study, are described in some cases of nosocomial infections, as is the case of E. ludwigii, reported as an agent causing an outbreak of bloodstream infection. Bacillus cereus causes bacteremia, infection of skin, bones and joints; S. lugdunensis causes bacteremia. S. warneri causes endocarditis and S. cohnii subsp. urealyticus causes bacteremia.All occupants[33]
PubmedAssessment of Bacterial Pathogens and their Antibiotic Resistance in the Air of Different Wards of Selected Teaching Hospitals in TehranTehranWards of selected two teaching hospitals Air samplesThe median level of colonies in the wards of hospital 1 was 129.87 (87.46–268.97) CFU/m3 and 297.97 (217.66–431.85) CFU/m3 for hospital 2.Staphylococcus aureus was identified in most wards of the tow hospital. Acinetobacterlwoffii and Salmonella typhimuriu were the most abundant and least Gram-negative bacteria in hospital 1, respectively. In hospital 2, Pseudomonas aeuringos and Klebsiella pneumonia were the most abundant Gram-negative bacteria in the sampling stations. All occupants[32]

4. Discussion

Numerous studies presented divergent points of view on how bacterial contamination can be observed in different locations within hospital facilities, how seasonal variations affect the concentration, and even how data regarding the most prevalent genera that can be found in healthcare environments and staff due to occupational activities.
In the first presented study [34], concentrations of airborne bacteria reached a peak in November (436.3 CFU/m3), and the lowest value was identified in December (257.1 CFU/m3). However, the authors did not explain the decrease between these two months or between the other months of the year that were assessed. Another study, conducted in Portugal [45], described that most of the departments analyzed presented a high level of bacterial concentration (ranging from 12 to 170 CFU/m3) and concluded that the indoor bacterial concentration was not influenced by outdoor concentration but by indoor air. A higher bacterial concentration was identified in the mornings (267.1–505.6 CFU/m3), and even though the authors did not provide an explanation, we hypothesize that this could be due to increased human activity from visitors or workers [36,46].
In another analyzed study [37], winter and autumn had the highest concentration levels of bacteria with the increased bioburden associated with the waiting room in autumn and children’s ward in the winter. A possible explanation for the higher load in the waiting room can be attributed to an increase in the number of occupants (200 per day or more). The same hypothesis is suggested in the children’s ward, with the additional factor of the increased number of infections in children during the wintertime. The fact that the rooms in that ward are small, and that more than one parent can accompany the child, is another factor that increases the concentration of bacteria such as airborne actinomycetes, which were the most prevalent in the children’s ward [37].
The data from Portuguese studies revealed that Staphylococcus epidermidis [45] and Micrococcus spp. [45,46,47] were the most prevalent bacteria identified. However, S. epidermidis is not considered to be a relevant risk of exposure due to its lower infections rates [34]. On the other hand, Acinetobacter (species not identified) was found in two studies [32,34] as a prevalent genus in a university hospital from Ethiopia, justifying its persistence due to its great survival ability in the indoor environment [47], which can be a potential cause for hospital infections transmitted via the air [48]. Another relevant microorganism is Pantoea agglomerants, which is able to infect hospitalized individuals, particularly immunodeficient patients, through contaminated medical instruments [49].
A bacteria genus described in several studies considered of great interest is Staphylococcus spp., which was identified at the highest concentration in a cardiology ward/intensive care room (hospital 5). Once the strains were analyzed, S. saprophyticus was the most predominant, followed by S. warneri, being reported as an important opportunistic pathogen and associated with healthcare-acquired infections [37]. Cabo Verde et al. [45] also found S. warneri to be a prevalent species in the hospital, but no data were reported regarding S. saprophyticus in contrast to the findings of Sivagnanasundaram et al. [50]. S. saprophyticus can infect an individual’s blood through catheters, surgical prostheses, pneumonia, urinary tract infections and more [51,52,53]; therefore, this species is of particular relevance. Moreover, Staphylococcus aureus is one of the most relevant nosocomial pathogens, described as one of the main pathogenic bacteria that cause osteomyelitis (including in children)[54,55,56,57,58,59] septic arthritis [60,61,62,63], and prosthetic joint infections [64,65,66,67]. S. aureus is a commensal bacterium and a human pathogen; about 30% of all humans are colonized with S. aureus [68]. Osteoarticular infections can occur by the direct inoculation of microorganisms into tissues due to penetrating or open trauma [69]. In limited settings, infections complicate as many as 44% of open fractures [69]. Trauma-related osteoarticular infections among patients with punctures wounds seeking medical care varied from 2–60% depending on the type of the injury [70,71,72]. S. aureus was also prevalent in the studies by Matinyi et al. [38] and Thomas et al. [73], being detected on door handles, which could be considered a possible source of nosocomial infection [38]. Additionally, Staphylococcus epidermidis, as well as Micrococcus luteus and Bacillus subtilis, were common in the studies by Sivagnanasundaram et al. [50], Bielawska-Drózd et al. [74], and Bolookat et al. [39]. The reason for these results could be related to the presence of these bacteria in the skin, mucous membranes, hair of human beings and animals [75,76,77,78].
Considering health effects, the identification of Clostridium difficile, a Gram-positive, anaerobic, spore-forming bacillus, must be considered, as it is the principal agent of pseudomembranous colitis in humans [79]. In the hospital setting, C. difficile infection is the main cause of healthcare-associated diarrhea [80]. Symptoms arise when C. difficile spores germinate in the intestine, and the bacteria start to produce toxins, Toxin A (TcdA) and Toxin B (TcdB), causing the inflammation of the large intestine [81]. The clinical presentation can range from mild diarrhea to lethal toxic megacolon [81]. Nonetheless, the ingestion of C. difficile spores does not always lead to the development of symptomatic disease, since this bacterium can be silently present in the intestine without manifesting any symptoms, denominated as asymptomatic C. difficile colonization [82]. However, the patients with this condition act as a reservoir for further transmissions [83,84], and they can progress to the infection themselves, especially if they are affected by an underlying illness [85]. The infection is transmitted by spores that are environmentally resistant [86].
Another microorganism of interest is H. pylori, which is associated with occupational exposure among endoscopy personnel [87]. The study by Mastromarino et al. [40] aimed to determine if different staff groups of healthcare workers, either with or without direct patient contact, were at equal risk of acquiring H. pylori infection. The authors concluded that direct contact with patients is an important factor for becoming infected, as opposed to simply working in the endoscopy unit. Another study highlighted [87] that 24% (9 out of 37) of gastrointestinal endoscopy personnel, and 47% (33 out of 70) of workers in a hospital who care for disabled individuals, tested positive for H. pylori. In this case, direct contact with patients and working in a hospital where disabled individuals reside was associated with H. pylori infections, but the exposure to gastrointestinal secretions of the patients was not [87]. This study supports the previous study’s idea that direct contact with patients is a factor to take into consideration.
Among Gram-negative bacteria, the most frequently identified pathogens are Escherichia coli, Klebsiella pneumoniae, Pseudomonas aeruginosa, and Acinetobacter baumannii. E.coli was described to be prevalent in operating beds due to fecal contamination and the lack of efficiency in the cleaning process [88,89]. Pseudomonas spp., one of the most significant genera of nosocomial pathogens, was the most prevalent bacteria in all operating theatres in the Matinyi et al. study [38], and was identified in other studies [73,90] that referred to antiseptic solutions as a possible source of this contamination [56,57,91,92]. Other bacteria, Bacillus spp., can be related to dusty environments, the type commonly found in Uganda [38]. This contamination might occur in indoor areas if the windows are open for natural ventilation and could then be transferred to the operating theatres [73]. Furthermore, A. baumannii was associated with a vast number of infections, such as those of the bloodstream, respiratory tract, surgical sites, and urinary tract [93]. Transmission between patients in hospital settings is difficult to prevent because of the bacterium’s capacity to persist in the environment, particularly in intensive care units [93]. These Gram-negative pathogens are associated with the etiology of numerous and severe hospital-acquired infections in humans and have the capacity to resist antimicrobial agents, which has become an increasingly relevant problem [94]. Currently, antimicrobial-resistant Gram-negative bacteria are expanding worldwide and are considered a significant threat to human health [3].

5. Conclusions

The bacterial contamination of healthcare units was found to be diverse and causative of several hazardous health effects. The reported contamination in this setting was divergent depending mostly on the sampling site. Nevertheless, Pseudomonas spp. and Staphylococcus spp., two of the greatest nosocomial pathogens, were the most prevalent bacteria identified in healthcare units. Hospital-acquired infection caused by Gram-positive bacteria and antibiotic-resistance, Gram-negative bacteria were the most frequent and relevant associated health effects. The necessity for tight control in the cleaning process was made clear in order to improve disinfection efficiency in wards, surfaces, equipment, and uniforms and prevent direct contact transmission. A better understanding of seasonal variations is essential, allowing hospitals to avoid contamination peaks.

Supplementary Materials

The following supporting information can be downloaded at: https://www.mdpi.com/article/10.3390/app12041958/s1, Table S1: PRISMA Checklist (Adopted from Moher et al. 2009 *).

Author Contributions

Conceptualization, A.M. Data curation, A.M., J.C., N.G.; Formal analysis, A.M., J.C. N.G., C.V., S.C.V., A.S.-U.; Investigation, A.M., J.C., N.G.; Methodology, A.M., S.C.V., A.S.-U.; Supervision, A.M; Validation, A.M., C.V., S.C.V., A.S.-U.; Writing—original draft, A.M., J.C., N.G.; Writing—review and editing, A.M., E.R., C.V., S.C.V., A.S.-U. All authors have read and agreed to the published version of the manuscript.

Funding

This work was supported of FCT/MCTES through UIDB/05608/2020 and UIDP/05608/2020. And by C2TN/IST (UIDB/04349/2020þUIDP/04349/2020).

Institutional Review Board Statement

Not applicable.

Informed Consent Statement

Not applicable.

Data Availability Statement

Not applicable.

Acknowledgments

H&TRC authors gratefully acknowledge the national support of FCT/MCTES through UIDB/05608/2020 and UIDP/05608/2020. The support of FCT is also acknowledged by C2TN/IST (UIDB/04349/2020þUIDP/04349/2020).

Conflicts of Interest

The authors declare no conflict of interest.

References

  1. Humphreys, H.; Smyth, E.T.M. Prevalence surveys of healthcare-associated infections: What do they tell us, if anything? Clin. Microbiol. Infect. 2006, 12, 2–4. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  2. World Health Organization. Health Care-Associated Infections Fact Sheet. 2013. Available online: http://www.who.int/gpsc/country_work/gpsc_ccisc_ fact_sheet_en.pdf (accessed on 10 September 2021).
  3. National Nosocomial Infections Surveillance System. National Nosocomial Infections Surveillance (NNIS) system report, data summary from January 1992 through June 2004, issued October 2004. Am. J. Infect. Control 2004, 32, 470. [Google Scholar] [CrossRef]
  4. Menachemi, N.; Yeager, V.A.; Welty, E.; Manzella, B. Are physician productivity and quality of care related? J. Healthc. Qual. 2015, 37, 93–101. [Google Scholar] [CrossRef] [PubMed]
  5. Haque, M.; Sartelli, M.; McKimm, J.; Abu Bakar, M. Health care-associated infections—An overview. Infect. Drug Resist. 2018, 11, 2321–2333. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  6. Levy, S.B. Factors impacting on the problem of antibiotic resistance. J. Antimicrob. Chemother. 2002, 49, 25–30. [Google Scholar] [CrossRef] [PubMed]
  7. National Academies of Sciences, Engineering and Medicine. Microbiomes of the Built Environment: A Research Agenda for Indoor. Microbiology, Human Health, and Buildings; The National Academies Press: Washington, DC, USA, 2017; pp. 95–131. [Google Scholar]
  8. Qudiesat, K.; Abu-Elteen, K.H.; Elkarmi, A.Z.; Hamad, M.; Abussaud, M. Assessment of airborne pathogens in healthcare settings. Afr. J. Microbiol. Res. 2009, 3, 66–76. Available online: https://www.academicjournals.org/ajmr (accessed on 10 October 2021).
  9. Marchand, G.; Duchaine, C.; Lavoie, J.; Veillette, M.; Cloutier, Y. Bacteria emitted in ambient air during bronchoscopy—A risk to health care workers? Am. J. Infect. Control 2016, 44, 1634–1638. [Google Scholar] [CrossRef] [PubMed]
  10. Douwes, J.; Torne, P.; Pearce, N.; Heederik, D. Bioaerosol health effects and exposure assessment: Progress and prospects. Ann. Occup. Hyg. 2003, 47, 187–200. [Google Scholar] [CrossRef] [Green Version]
  11. Cross, A.S. What is a virulence factor? Crit. Care 2008, 12, 196. [Google Scholar] [CrossRef] [Green Version]
  12. Wu, H.J.; Wang, A.H.; Jennings, M.P. Discovery of virulence factors of pathogenic bacteria. Curr. Opin. Chem. Biol. 2008, 12, 93–101. [Google Scholar] [CrossRef]
  13. Actor, J.A.J. 11—Basic Bacteriology. Elsevier’s Integrated Review; Elsevier/Saunders: Philadelphia, PA, USA, 2012; pp. 93–103. [Google Scholar] [CrossRef]
  14. Huslage, K.; Rutala, W.; Sickbert-Bennett, E.; Weber, D. A quantitative approach to defining “high-touch” surfaces in hospitals. Infect. Control Hosp. Epidemiol. 2010, 31, 850–853. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  15. Weber, D.; Rutala, W.; Miller, M.; Huslage, K.; Sickbert-Bennett, E. Role of hospital surfaces in the transmission of emerging health care-associated pathogens: Norovirus, Clostridium difficile, and Acinetobacter species. Am. J. Infect. Control 2010, 38, S25–S33. [Google Scholar] [CrossRef] [PubMed]
  16. Luksamijarulkul, P.; Aiempradit, N.; Vatanasomboon, P. Microbial Contamination on Used Surgical Masks among Hospital Personnel and Microbial Air Quality in their Working Wards: A Hospital in Bangkok. Oman Med. J. 2014, 29, 346–350. [Google Scholar] [CrossRef] [PubMed]
  17. Drees, M.; Snydman, D.; Schmid, C.; Barefoot, L.; Hansjosten, K.; Vue, P.; Cronin, M.; Nasraway, S.; Golan, Y. Prior environmental contamination increases the risk of acquisition of vancomycin-resistant enterococci. Clin. Infect. Dis. 2008, 46, 678–685. [Google Scholar] [CrossRef]
  18. Malamou-Ladas, H.; O’Farrell, S.; Nash, J.; Tabaqchali, S. Isolation of Clostridium difficile from patients and the environment of hospital wards. J. Clin. Pathol. 1983, 36, 88–92. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  19. Neely, A.; Maley, M. Survival of enterococci and staphylococci on hospital fabrics and plastic. J. Clinic. Microbiol. 2000, 38, 724–726. [Google Scholar] [CrossRef] [Green Version]
  20. Shaughnessy, M.; Micielli, R.; DePestel, D.; Arndt, J.; Strachan, C.; Welch, K.; Chenoweth, C. Evaluation of hospital room assignment and acquisition of Clostridium difficile infection. Infect. Control Hosp. Epidemiol. 2011, 32, 201–206. [Google Scholar] [CrossRef]
  21. Allegranzi, B.; Bagheri Nejad, S.; Combescure, C.; Graafmans, W.; Attar, H.; Pittet, D.L.D. Burden of endemic health-care-associated infection in developing countries: Systematic review and meta-analysis. Lancet 2011, 377, 228–241. [Google Scholar] [CrossRef]
  22. Burke, J.P. Infection control—A problem for patient safety. N. Engl. J. Med. 2003, 348, 651–656. [Google Scholar] [CrossRef] [Green Version]
  23. Goyer, N.; Lavoie, J.; Lazure, L.; Marchand, G. Bioaerosols in the Workplace: Evaluation, Control and Prevention Guide; Institut de Reserche en Santé et en Sécurité du Travail du Québec: Quebéc, QC, Canada, 2001. [Google Scholar]
  24. Huff, W.; Kubena, L.; Harvey, R.; Doerr, J. Mycotoxin interactions in poultry and swine. J. Anim. Sci. 1988, 66, 2351–2355. [Google Scholar] [CrossRef] [Green Version]
  25. Dizbay, M.; Tunccan, O.; Sezer, B.; Aktas, F.; Arman, D. Nosocomial Burkholderia cepacia infections in a Turkish university hospital: A five-year surveillance. J. Infect. Dev. Ctries. 2009, 3, 273–277. [Google Scholar] [CrossRef] [Green Version]
  26. Gautam, V.; Singhal, L.; Ray, P. Burkholderia cepacia complex: Beyond pseudomonas and acinetobacter. Indian J. Med. Microbiol. 2011, 29, 4–12. [Google Scholar] [CrossRef]
  27. Gautam, V.; Patil, P.; Kumar, S.; Midha, S.; Kaur, M.; Kaur, S.; Singh, M.; Mali, S.; Shastri, J.; Arora, A.; et al. Multilocus sequence analysis reveals high genetic diversity in clinical isolates of Burkholderia cepacia complex from India. Sci. Rep. 2016, 6, 35769. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  28. Paul, L.; Hegde, A.; Pai, T.; Shetty, S.; Baliga, S.; Shenoy, S. An Outbreak of Burkholderia cepacia Bacteremia in a Neonatal Intensive Care Unit. Indian J. Pediatr. 2016, 83, 285–288. [Google Scholar] [CrossRef] [PubMed]
  29. Sousa, S.; Feliciano, J.; Pita, T.; Guerreiro, S.; Leitão, J.H. Burkholderia cepacia Complex Regulation of Virulence Gene Expression: A Review. Genes 2017, 8, 43. [Google Scholar] [CrossRef] [Green Version]
  30. Antony, B.; Cherian, E.; Boloor, R.S.K. A sporadic outbreak of Burkholderia cepacia complex bacteremia in pediatric inten-sive care unit of a tertiary care hospital in coastal Karnataka, South India. Indian J. Pathol. Microbiol. 2016, 59, 197–199. [Google Scholar] [CrossRef] [PubMed]
  31. Singhal, T.; Shah, S. Naik, R. Outbreak of Burkholderia cepacia complex bacteremia in a chemotherapy day care unit due to intrinsic contamination of an antiemetic drug. Indian J. Med. Microbiol. 2015, 33, 117–119. [Google Scholar] [CrossRef]
  32. Montazer, M.; Soleimani, N.; Vahabi, M.; Abtahi, M.; Etemad, K.; Zendehdel, R. Assessment of Bacterial Pathogens and their Antibiotic Resistance in the Air of Different Wards of Selected Teaching Hospitals in Tehran. Indian J. Occup. Environ. Med. 2011, 25, 78–83. [Google Scholar] [CrossRef]
  33. Oliveira, M.; Cunha, L.; Cruz, F.; Batista, N.; Gil, E.; Alves, V.; Bara, M.; Torres, I. Potentially pathogenic bacteria isolated from neglected air and surfaces in hospitals. J. Pharm. Sci. 2011, 57. [Google Scholar] [CrossRef]
  34. Augustowska, M.; Dutkiewicz, J. Variability of airborne micro-flora in a hospital ward within a period of one year. AAEM 2006, 13, 99–106. [Google Scholar]
  35. Tselebonis, A.; Nena, E.; Panopoulou, M.; Kontogiorgis, C.; Bezirtzoglou, E.; Constantinidis, T. Air Contamination in Different Departments of a Tertiary Hospital. Assessment of Microbial Load and of Antimicrobial Susceptibility. Biomedecines 2020, 8, 163. [Google Scholar] [CrossRef] [PubMed]
  36. Park, D.; Yeom, J.; Lee, W.; Lee, K. Assessment of the levels of airborne bacteria, Gram-negative bacteria, and fungi in hospital lobbies. Int. J. Environ. Res. Public Health 2013, 10, 541–555. [Google Scholar] [CrossRef] [PubMed]
  37. Stec, J.; Lenart-Boroń, A. Assessment of microbiological aerosol concentration in selected healthcare facilities in southern Poland. Cent. Eur. J. Public Health 2019, 27, 239–244. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  38. Matinyi, S.; Enoch, M.; Akia, D.; Byaruhanga, V.; Masereka, E.; Ekeu, I.; Atuheire, C. Contamination of microbial pathogens and their an-timicrobial pattern in operating theatres of peri-urban eastern Uganda: A cross-sectional study. BMC Infect. Dis. 2018, 18, 460. [Google Scholar] [CrossRef]
  39. Bolookat, F.; Hassanvand, M.S.; Faridi, S.; Hadei, M.; Rahmatinia, M.; Alimohammadi, M. Assessment of bioaerosol particle characteristics at different hospital wards and operating theaters: A case study in Tehran. MethodsX 2018, 5, 1588–1596. [Google Scholar] [CrossRef]
  40. Mastromarino, P.; Conti, C.; Donato, K.; Strappini, P.; Cattaruzza, M.; Orsi, G. Does hospital work constitute a risk factor for Helicobacter pylori infection? J. Hosp. Infect. 2005, 60, 261–268. [Google Scholar] [CrossRef]
  41. Chaudhry, A.; Rafiq, A.; Raza, J.; Gillani, S.-U.-H.; Malik, A.; Farqaleet, S.; Sami, A.; Awais, S. Staph Aureus as the most common cause of osteoarticular infection in dost †“1 Mayo Hospital, Lahore”. Ann. King Edw. Med. Univ. 2015, 21, 136. [Google Scholar] [CrossRef]
  42. Nylund, C.; Goudie, A.; Garza, J.; Fairbrother, G.; Cohen, M. Clostridium difficile infection in hospitalized children in the United States. Arch. Pediatr. Adolesc. Med. 2011, 165, 451–457. [Google Scholar] [CrossRef] [Green Version]
  43. Patel, S.J.; Oliveira, A.P.; Zhou, J.J.; Alba, L.; Furuya, E.Y.; Weisenberg, S.A.; Jia, H.; Clock, S.A.; Kubin, C.J.; Jenkins, S.G.; et al. Risk factors and outcomes of infections caused by extremely drug-resistant gram-negative bacilli in patients hospitalized in intensive care units. Am. J. Infect. Control 2014, 42, 626–631. [Google Scholar] [CrossRef] [Green Version]
  44. de Blank, P.; Zaoutis, T.; Fisher, B.; Troxel, A.; Aplenc, K.J.R. Trends in Clostridium difficile infection and risk factors for hospital acquisition of Clostridium difficile among children with cancer. J. Pediatr. 2013, 163, 699–705.e1. [Google Scholar] [CrossRef] [Green Version]
  45. Cabo Verde, S.; Almeida, S.; Matos, J.; Guerreiro, D.M.M.; Faria, T.; Botelho, D.; Santos, M.; Viegas, C. Microbiological assessment of indoor air quality at different hospital sites. Res. Microbiol. 2015, 166, 557–563. [Google Scholar] [CrossRef] [PubMed]
  46. Sivagnanasundaram, P.; Amarasekara, R.; Madegedara, R.; Magana-Arachchi, E.A.D. Assessment of Airborne Bacterial and Fungal Communities in Selected Areas of Teaching Hospital, Kandy, Sri Lanka. Biomed. Res. Int. 2019, 2019, 7393926. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  47. Monteiro, A.; Almeida, B.; Paciência, I.; Cavaleiro Rufo, J.; Ribeiro, E.; Carolino, E.; Viegas, C.; Uva, A.; Cabo Verde, S. Bacterial Contamination in Health Care Centers: Differences between Urban and Rural Settings. Atmosphere 2021, 12, 450. [Google Scholar] [CrossRef]
  48. Solomon, F.; Wadilo, F.; Arota, A.; Abraham, Y. Antibiotic resistant airborne bacteria and their multidrug resistance pattern at University teaching referral Hospital in South Ethiopia. Ann. Clin. Microbiol. Antimicrob. 2017, 16, 29. [Google Scholar] [CrossRef]
  49. Allen, K.D.; Green, H. Hospital outbreak of multi-resistant Acinetobacter anitratus: An airborne mode of spread? J. Hosp. Infect. 1987, 9, 110–119. [Google Scholar] [CrossRef]
  50. Dutkiewicz, J.; Mackiewicz, B.; Lemieszek, M.K.; Golec, M.; Milanowski, J. Pantoea agglomerans: A mysterious bacterium of evil and good. Part IV. Beneficial effects. Ann. Agric. Environ. Med. 2016, 23, 206–222. [Google Scholar] [CrossRef] [PubMed]
  51. Dakić, I.; Morrison, D.; Vuković, D.; Savić, B.; Shittu, A.; Jezek, P.; Hauschild, T.; Stepanović, S. Isolation and molecular characterization of Staphylococcus sciuri in the hospital environment. J. Clin. Microbiol. 2005, 43, 2782–2785. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  52. Drozenová, J.; Petrás, P. Vlastnosti koaguláza-negativních stafylokoků izolovaných z hemokultur [Characteristics of coagulase-negative staphylococci isolated from hemocultures]. Epidemiol. Mikrobiol. Imunol. 2000, 49, 51–58. [Google Scholar] [PubMed]
  53. Shittu, A.; Lin, J.; Morrison, D.; Kolawole, D. Isolation and molecular characterization of multiresistant Staphylococcus sciuri and Staphylococcus haemolyticus associated with skin and soft-tissue infec-tions. J. Med. Microbiol. 2004, 53, 51–55. [Google Scholar] [CrossRef]
  54. Castellazzi, L.; Mantero, M.; Esposito, S. Update on the Management of Pediatric Acute Osteomyelitis and Septic Arthritis. Int. J. Mol. Sci. 2016, 17, 855. [Google Scholar] [CrossRef] [Green Version]
  55. Taylor, T.A.; Unakal, C.G. Staphylococcus Aureus. [Updated 2021 Jul 21]. In StatPearls [Internet]; StatPearls Publishing: Treasure Island, FL, USA, 2021. [Google Scholar]
  56. Hodgson, S.H.; Atkins, B.; Bejon, P.; Byren, I.; Whyllic, D.; Athanason, N.A.; Berendt, A.; McNally, M. The microbiology of chronic osteomyelitis: Prevalence of resistance to common empirical anti-microbial regimens. J. Infect. 2010, 60, 338–343. [Google Scholar] [CrossRef]
  57. Inoue, S.; Moriyama, T.; Horinouchi, Y.; Tachibana, T.; Okada, F.; Maruo, K.; Yoshiya, S. Comparison of clinical features and outcomes of staphylococcus aureus vertebral osteomyelitis caused by methicillin-resistant and methicillin-sensitive strains. Springerplus 2013, 2, 283. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  58. Beronius, M.; Bergman, B.; Andersson, R. Vertebral osteomyelitis in Göteborg, Sweden: A retrospective study of patients during 1990–1995. Scand. J. Infect. Dis. 2001, 33, 527–532. [Google Scholar] [CrossRef]
  59. Corrah, T.W.; Enoch, D.A.; Aliyu, S.H.; Lever, A.M. Bacteraemia and subsequent vertebral osteomyelitis: A retrospective review of 125 patients. QJM 2011, 104, 201–207. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  60. Clerc, O.; Prod’hom, G.; Greub, G.; Zanetti, G.; Senn, L. Adult native septic arthritis: A review of 10 years of experience and lessons for empirical antibiotic therapy. J. Antimicrob. Chemother. 2011, 66, 1168–1173. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  61. Stoesser, N.; Pocock, J.; Moore, C.E.; Soeng, S.; Hor, P.; Sar, P.; Limmathurotsakul, D.; Day, N.; Kumar, V.; Khan, S.; et al. The epidemiology of pediatric bone and joint infections in Cambodia, 2007–2011. J. Trop. Pediatr. 2013, 59, 36–42. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  62. Howard-Jones, A.R.; Isaacs, D.; Gibbons, P.J. Twelve-month outcome following septic arthritis in children. J. Pediatr. Orthop. B 2013, 22, 486–490. [Google Scholar] [CrossRef]
  63. Khan, F.Y.; Abu-Khattab, M.; Baagar, K.; Mohamed, S.F.; Elgendy, I.; Anand, D.; Malallah, H.; Sanjay, D. Characteristics of patients with definite septic arthritis at Hamad General Hospital, Qatar: A hospital-based study from 2006 to 2011. Clin. Rheumatol. 2013, 32, 969–973. [Google Scholar] [CrossRef]
  64. Peel, T.N.; Cheng, A.C.; Choong, P.F.; Buising, K.L. Early onset prosthetic hip and knee joint infection: Treatment and outcomes in Victoria, Australia. J. Hosp. Infect. 2012, 82, 248–253. [Google Scholar] [CrossRef] [PubMed]
  65. Westberg, M.; Grøgaard, B.; Snorrason, F. Early prosthetic joint infections treated with debridement and implant retention: 38 primary hip arthroplasties prospectively recorded and followed for median 4 years. Acta Orthop. 2012, 83, 227–232. [Google Scholar] [CrossRef] [Green Version]
  66. Bejon, P.; Berendt, A.; Atkins, B.; Green, N.; Parry, H.; Masters, S.; McLardy-Smith, P.; Gundle, R.; Byren, I. Two-stage revision for prosthetic joint infection: Predictors of outcome and the role of reimplantation microbiology. J. Antimicrob. Chemother. 2010, 65, 569–575, Erratum in J. Antimicrob. Chemother. 2011, 66, 1204.. [Google Scholar] [CrossRef] [Green Version]
  67. Byren, I.; Bejon, P.; Atkins, B.L.; Angus, B.; Masters, S.; McLardy-Smith, P.; Gundle, R.; Berendt, A. One hundred and twelve infected arthroplasties treated with ‘DAIR’ (debridement, antibiotics and implant retention): Antibiotic duration and outcome. J. Antimicrob. Chemother. 2009, 63, 1264–1271, Erratum in: J. Antimicrob. Chemother. 2011, 66, 1203; Erratum in: J. Antimicrob. Chemother. 2013, 68, 2964–2965. [Google Scholar] [CrossRef] [Green Version]
  68. Wertheim, H.F.; Melles, D.C.; Vos, M.C.; van Leeuwen, W.; van Belkum, A.; Verbrugh, H.A.; Nouwen, J.L. The role of nasal carriage in Staphylococcus aureus infections. Lancet Infect. Dis. 2005, 5, 751–762. [Google Scholar] [CrossRef]
  69. Mathieu, L.; Mottier, F.; Bertani, A.; Danis, J.; Rongiéras, F.; Chauvin, F. Management of neglected open extremity fractures in low-resource settings: Experience of the French Army Medical Service in Chad. Orthop. Traumatol. Surg. Res. 2014, 100, 815–820. [Google Scholar] [CrossRef] [Green Version]
  70. Eidelman, M.; Bialik, V.; Miller, Y.; Kassis, I. Plantar puncture wounds in children: Analysis of 80 hospitalized patients and late sequelae. Isr. Med. Assoc. J. 2003, 5, 268–271. [Google Scholar] [PubMed]
  71. Laughlin, R.T.; Reeve, F.; Wright, D.G.; Mader, J.T.; Calhoun, J.H. Calcaneal osteomyelitis caused by nail puncture wounds. Foot Ankle Int. 1997, 18, 575–577. [Google Scholar] [CrossRef] [PubMed]
  72. Imoisili, M.A.; Bonwit, A.M.; Bulas, D.I. Toothpick puncture injuries of the foot in children. J. Pediatr. Infect. Dis. 2004, 23, 80–82. [Google Scholar] [CrossRef] [PubMed]
  73. Thomas, S.; Palmer, R.; Chipungu, P.E.G. Reducing bacterial con-tamination in an Orthopedic Theatre ventilated by natural ventilation in a Developing Country. J. Infect. Dev. Ctries. 2016, 10, 518–522. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  74. Bielawska-Drózd, A.; Cieślik, P.; Bohacz, J.; Korniłłowicz-Kowalska, T.; Żakowska, D.; Bartoszcze, M.; Kocik, J. Microbiological analysis of bioaerosols collected from Hospital Emergency Depart-ments and ambulances. Ann. Agric. Environ. Med. 2018, 25, 274–279. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  75. Azimi, F.; Nabizadeh, R.; Alimohammadi, M.; Naddafi, K. Bacterial Bioaerosols in the Operating Rooms: A Case Study in Tehran Shariati Hospital. J. Air Pollut. Health 2016, 1, 215–218. [Google Scholar]
  76. Mentese, S.; Rad, A.Y.; Arısoy, M.; Güllü, G. Seasonal and Spatial Variations of Bioaerosols in Indoor Urban Environments, Ankara, Turkey. Indoor Built Environ. 2012, 21, 797–810. [Google Scholar] [CrossRef]
  77. Polednik, B. Aerosol and bioaerosol particles in a dental office. Environ. Res. 2014, 134, 405–409. [Google Scholar] [CrossRef] [PubMed]
  78. Rendon, R.; Garcia, B.C.; Vital, P.G. Assessment of airborne bacteria in selected occupational environments in Quezon City, Philippines. Arch. Environ. Occup. Health 2017, 72, 178–183. [Google Scholar] [CrossRef]
  79. Bartlett, J.G. Antibiotic-associated pseudomembranous colitis. Rev. Infect. Dis. 1979, 1, 530–539. [Google Scholar] [CrossRef] [PubMed]
  80. Miller, B.A.; Chen, L.F.; Sexton, D.J.; Anderson, D.J. Comparison of the burdens of hospital-onset, healthcare facility-associated Clostridium difficile Infection and of healthcare-associated infection due to methicillin-resistant Staphylococcus aureus in community hospitals. Infect. Control Hosp. Epidemiol. 2011, 32, 387–390. [Google Scholar] [CrossRef]
  81. Smits, W.K.; Lyras, D.; Lacy, D.B.; Wilcox, M.H.; Kuijper, E.J. Clostridium difficile infection. Nat. Rev. 2016, 2, 16020. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  82. Crobach, M.J.T.; Vernon, J.J.; Loo, V.G.; Kong, L.Y.; Péchiné, S.; Wilcox, M.H.; Kuijper, E.J. Understanding Clostridium difficile Colonization. Clin. Microbiol. Rev. 2018, 31, e00021-17. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  83. Eyre, D.W.; Griffiths, D.; Vaughan, A.; Golubchik, T.; Acharya, M.; O’Connor, L.; Crook, D.W.; Walker, A.S.; Peto, T.E. Asymptomatic Clostridium difficile colonisation and onward transmission. PLoS ONE 2013, 8, e78445. [Google Scholar] [CrossRef]
  84. Kong, L.Y.; Eyre, D.W.; Corbeil, J.; Raymond, F.; Walker, A.S.; Wilcox, M.H.; Crook, D.W.; Michaud, S.; Toye, B.; Frost, E.; et al. Clostridium difficile: Investigating Transmission Patterns Between Infected and Colonized Patients Using Whole Genome Sequencing. Clin. Infect. Dis. Off. Publ. Infect. Dis. Soc. Am. 2019, 68, 204–209. [Google Scholar] [CrossRef]
  85. Zacharioudakis, I.M.; Zervou, F.N.; Pliakos, E.E.; Ziakas, P.D.; Mylonakis, E. Colonization with toxinogenic C. difficile upon hospital admission, and risk of infection: A systematic review and meta-analysis. Am. J. Gastroenterol. 2015, 110, 381–390. [Google Scholar] [CrossRef]
  86. Leffler, D.A.; Lamont, J.T. Clostridium difficile infection. N. Engl. J. Med. 2015, 372, 1539–1548. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  87. Angtuaco, T.; Sharma, V.; Corder, F.; Raufman, J.; Howden, C. Seroprevalence of H. pylori infection and symptoms of up-per gastrointestinal tract disease in two groups of healthcare workers. Dig. Dis. Sci. 2002, 47, 292–297. [Google Scholar] [CrossRef]
  88. Napoli, C.; Marcotrigiano, V.; Montagna, M. Air sampling procedures to evaluate microbial contamination: A comparison between active and passive methods in operating theatres. BMC Public Health 2012, 12, 594. [Google Scholar] [CrossRef] [Green Version]
  89. Nasser, A.; Zhang, X.; Yang, L.; Sawafta, F.; Salah, B. Assessment of Surgical Site Infections from Signs & Symptoms of the Wound and Associated Factors in Public Hospitals of Hodeidah City, Yemen. Int. J. Appl. Sci. 2013, 3, 101–110. [Google Scholar]
  90. Ensayef, S.; Al Shalchi, S.; Sabbar, M. Microbial contamination in the operating theatre: A study in a hospital in Baghdad. East. Mediterr. Health J. 2009, 15, 219–223. [Google Scholar] [CrossRef] [PubMed]
  91. Bellido, F.; Hancock, R. Susceptibility and Resistance of P. aeruginosa to Antimicrobial Agents em in Pseudomona aeruginosa as an Opportunistic Pathogen; Campa, M., Bendinelli, M.F.H., Eds.; Springer: Boston, MA, USA, 1993; pp. 321–348. [Google Scholar]
  92. Peña, C.; Dominguez, M.A.; Pujol, M.; Vardarguer, R.; Gudiol, F.; Ariza, J. An outbreak of carbapenem-resistant Pseudomonas aeruginosa in a urology ward. Clin. Microbiol. Infect. 2003, 9, 938–943. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  93. Peleg, A.; Seifert, H.; Paterson, D. Acinetobacter baumannii: Emergence of a successful pathogen. Clin. Microbiol. Rev. 2008, 21, 538–582. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  94. Paterson, D. Resistance in gram-negative bacteria: Enterobacteriaceae. Am. J. Med. 2006, 119, S20–S70. [Google Scholar] [CrossRef]
Applsci 12 01958 g001 550
Figure 1. PRISMA-based selection of articles.
Figure 1. PRISMA-based selection of articles.
Applsci 12 01958 g001
Table
Table 1. Inclusion and exclusion criteria in the articles selected.
Table 1. Inclusion and exclusion criteria in the articles selected.
Inclusion CriteriaExclusion Criteria
Articles in the English languageArticles in other languages (for articles)
Articles published from 1 January 2000 to 31 October 2021Articles published before 2000
Articles related to bacteria contamination in healthcare unitsArticles related to biological samples from patients or workers(exclusive)
Articles related to health effects of bacteria on humansAbstract of congress, reviews/state-of-the art, reports
Articles related exclusively to humansArticles related exclusively to animals
Bacterial identification to the genera level and if possible, to the species level.
Publisher’s Note: MDPI stays neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Share and Cite

MDPI and ACS Style

Monteiro, A.; Cardoso, J.; Guerra, N.; Ribeiro, E.; Viegas, C.; Cabo Verde, S.; Sousa-Uva, A. Exposure and Health Effects of Bacteria in Healthcare Units: An Overview. Appl. Sci. 2022, 12, 1958. https://doi.org/10.3390/app12041958

AMA Style

Monteiro A, Cardoso J, Guerra N, Ribeiro E, Viegas C, Cabo Verde S, Sousa-Uva A. Exposure and Health Effects of Bacteria in Healthcare Units: An Overview. Applied Sciences. 2022; 12(4):1958. https://doi.org/10.3390/app12041958

Chicago/Turabian Style

Monteiro, Ana, Jéssica Cardoso, Nuno Guerra, Edna Ribeiro, Carla Viegas, Sandra Cabo Verde, and António Sousa-Uva. 2022. "Exposure and Health Effects of Bacteria in Healthcare Units: An Overview" Applied Sciences 12, no. 4: 1958. https://doi.org/10.3390/app12041958

APA Style

Monteiro, A., Cardoso, J., Guerra, N., Ribeiro, E., Viegas, C., Cabo Verde, S., & Sousa-Uva, A. (2022). Exposure and Health Effects of Bacteria in Healthcare Units: An Overview. Applied Sciences, 12(4), 1958. https://doi.org/10.3390/app12041958

Note that from the first issue of 2016, this journal uses article numbers instead of page numbers. See further details here.

Article Metrics

Back to TopTop