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Article

MRSA Colonization in Workers from Different Occupational Environments—A One Health Approach Perspective

by
Ketlyn Oliveira
1,
Carla Viegas
1,2,3,* and
Edna Ribeiro
1
1
Health & Technology Research Center (H&TRC), Escola Superior de Tecnologia da Saúde de Lisboa (ESTeSL), Instituto Politécnico de Lisboa, 1990-096 Lisbon, Portugal
2
Public Health Research Centre, NOVA National School of Public Health, Universidade NOVA de Lisboa, 1099-085 Lisboa, Portugal
3
Comprehensive Health Research Center (CHRC), NOVA Medical School, Universidade NOVA de Lisboa, 1169-056 Lisboa, Portugal
*
Author to whom correspondence should be addressed.
Atmosphere 2022, 13(5), 658; https://doi.org/10.3390/atmos13050658
Submission received: 24 March 2022 / Revised: 13 April 2022 / Accepted: 19 April 2022 / Published: 21 April 2022
(This article belongs to the Special Issue Occupational Exposure Biological Agents: Focus on a Growing Concern)
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Abstract

:
Staphylococcus aureus and particularly methicillin-resistant S. aureus (MRSA) infections are currently associated with extremely high morbidity and mortality rates worldwide. The global escalation in the development of antibiotic-resistant human pathogens and S. aureus ability in developing new clones with the capacity to invade community settings, leads to an urgent need to develop accurate and efficient assessments of S. aureus colonization in occupational settings, particularly those with increased risk of human and animal colonization and food contamination. Here we present cross-sectional studies with the aim to assemble crucial information regarding MRSA prevalence in workers from five different Portuguese occupational environments (bakeries, swineries (humans and animals), ambulance crews, veterinary clinics and healthcare facilities). Our data demonstrated high prevalence of S. aureus asymptomatic carriers among bakery workers (40%; 75% MSSA and 25% MRSA), swinery workers (54%; 8% MSSA and 46% MRSA), firefighters (48.5%; 24% MSSA and 21% MRSA) and healthcare workers (Study 1: 42.2%; 18.4% MSSA and 23.7% MRSA, Study 2: 43.3% MRSA). S. aureus prevalence in veterinary staff was 7.1% (MSSA), lower than the results obtained in control groups (33.3% S. aureus; MRSA 4% to 10%). The present study sustains the urge to develop accurate and efficient assessment of S. aureus human and animal colonization, particularly in high risk occupational settings, with proper guidelines and validated procedures in order to avoid potential hazardous health outcomes associated with bioaerosol exposure and associated infectious diseases.

1. Introduction

It is estimated that 20% of the human population are persistent carriers of Staphylococcus aureus, and nearly 30% are intermittent carriers [1]. Because it is both a commensal bacterium and a pathogen, colonization can be dangerous, working as a reservoir and leading to the spread of the bacteria or future infections in the colonized individuum [2]. Additionally, S. aureus is the main agent of nosocomial and community-acquired infections, with high percentages of strains resistant to various antibiotics, antiseptics and disinfectants. It is a common cause of bacteremia and endocarditis, as well as osteoarticular, skin and soft tissue, pulmonary and device related infections [1,2,3].
Methicillin resistance is a prevalent antibiotic resistance associated with S. aureus and healthcare worldwide. MRSA strains produce an altered penicillin-binding protein (PBP2a) that is encoded by an acquired gene (mecA) associated with decreased affinity for most semisynthetic penicillins [1]. The emergence of MRSA is due to the acquisition and insertion of a mobile genetic element, designated staphylococcal cassette chromosome mec (SCCmec), that carry the mecA gene into the chromosomes of susceptible strains [1].
MRSA strains were previously more limited to the hospital environment, but are now showing rising degrees of linkage with community-acquired infections, as well as the emergence of multidrug-resistance [1,3,4]. MRSA has a persistently high mortality rate and may infect nearly any anatomical regions -. The infecting strains match the colonizing strains in 50–80% of MRSA infections, and it is estimated that colonization may increase infection risk by up to 25% [1]. Any item in contact with the skin can serve as a fomite in MRSA transmission, and the bacteria can remain for long periods of time in hosts or the environment, complicating attempts at eradication [1,3]. The spread of resistant strains can make common infectious diseases difficult, sometimes impossible, to treat, and leads to increased medical costs, prolonged hospitalizations and increased mortality [1,5].
Portugal is one of the countries with the highest prevalence of MRSA. Despite a decrease of 8.2 percentage points from 2014 to 2017, the percentage in 2017 was still at 39.2%, and MRSA continues to be defined as a public health priority [6]. The decrease in the prevalence of MRSA is due to the implementation of national recommendations and guidelines, prudent use of antibiotics, and prevention and control of infections [7].
Apart from humans, MRSA colonization and infection has also been reported in companion, livestock and wild animals [1]. In fact, dust is suspected to have an important role in transmission of livestock-associated MRSA between pigs, farmers and farmers’ families (Feld et al., 2018). Additionally, the indiscriminate use of antibiotics in animal husbandry and other agricultural activities, along with poor infection control measures, has largely contributed to an increase in the emergence of resistant strains and dissemination among livestock [1]. LA-MRSA has recently attracted considerable attention as a zoonotic risk, especially for people who interact closely with farm animals. The detection and geographic spread of LA-MRSA in the EU/EEA population increased between 2007 and 2013, according to an ECDC survey, highlighting the veterinary and public health relevance of LA-MRSA as a “One Health” problem [8].
Comprehensive MRSA strategies targeting all healthcare settings remain essential to slow the spread of MRSA in Europe. Surveillance for MRSA in animals and food is currently voluntary and only carried out in a limited number of countries [9]. Insufficient infection control and prevention contributes to the rapid progression of antibiotic resistance. As a response, all barriers to the spread of resistance must be determined [10].
To obtain information regarding MRSA prevalence in workers from five different Portuguese occupational environments (bakeries, swineries, ambulance crews, veterinary clinics and healthcare facilities), cross-sectional studies were performed. The studies were integrated into larger studies comprising also the assessment of MRSA contamination in the environment (ambulances) or, in the case of swineries, animals.

2. Materials and Methods

2.1. Workplaces and Workers Assessed

Biological samples were collected from 5 swineries assessing a total of 68 samples; 26 from workers (including veterinarians, engineers and workers) and 42 from animals. Regarding the animals, we selected 42 pigs from the maternities in 3 swineries, and 30 pigs from the stalls (3 weeks old) from 2 swineries, following the procedures published in [11,12]. Moreover, from a veterinary clinic, we collected samples from 14 volunteers (all day shift workers, including veterinarians and auxiliary workers) [13].
Regarding the ambulance crew, we collected 98 environmental samples from the ambulances and 33 from workers (ambulance crew), as previous reported [14].
From healthcare workers (including doctors, nurses, laboratory technicians and auxiliary workers), biological samples were taken in two central hospitals in Lisbon, assessing a total of 68 biological samples; 38 from Hospital 1 and 30 from Hospital 2 [15]. Additionally, 25 biological samples were collected in 10 Primary Health Care Centers (PHCC).
Furthermore, we collected 74 biological samples from workers (including supervisors, bakers and auxiliary workers) in 13 bakeries.
A control group with 55 biological samples was collected from volunteers (mostly from the academic environment, including teachers, students, auxiliary and administrative workers) with no occupational contact with healthcare or animal facilities.
All studies mentioned above were carried out in Portugal. Additional information about the sample collection procedure can be found in Table 1. All volunteers enrolled in the studies were healthy individuals (with no previously diagnosed pathologies). Inclusion criteria considered were adult voluntaries (older than 18 years old and younger than 65 years old) with no acknowledged previously diagnosed pathology of any type, no gender criteria were utilized. Exclusion criteria applied included viral and bacterial infections.

2.2. Samples Collection

All the biological samples were obtained through nasopharyngeal swab procedure for S. aureus identification, using transport swabs with Stuart media, and immediately transported to the laboratory. The swab was inserted into the nostrils (one at a time), and moved straight back along the floor of the nasal passage until it reached the posterior wall of the nasopharynx (about 4 to 6 cm or 1.6–2.5 inches), was gently rotated for a few seconds and carefully removed without touching the sides of the nostrils. All workers provided a signed written informed consent before enrolment in the study, making sure all the inherent ethical principles were properly safeguarded.
The projects were submitted and approved by Escola Superior de Tecnologia da Saúde de Lisboa Ethical Council (Lisboa, Portugal) (Re: CE-ESTeSL-Nº 63-2019; CE-ESTeSL-Nº.18-2019). The studies are in accordance with the Helsinki Declaration and Oviedo Convention and in Agreement with the Portuguese law nº 58/2019 of 8 of August regarding data protection.
Surface samples were collected by swabbing the surfaces using a 10 × 10 cm square stencil, which was disinfected with a 70% alcohol solution between each sampling (ISO 18593, 2004). Following inoculation, each swab was later extracted with 1 mL of 0.1% Tween™ 80 saline solution (NaCl 0.9%) for 30 min at 250 rpm in an orbital laboratory shaker (Edmund Bühler SM-30, Hechingen, Germany) [14].

2.3. Staphylococcus Aureus Identification

For S. aureus identification, the biological (N = 337) and environmental swab samples (N = 98) were inoculated in Columbia agar, with 5% sheep blood and CHROMID® MRSA, then incubated for 24 and 48 h at 37 °C. Suspicious colonies were isolated and identification performed through a catalase test, using a Slidex Staph Kit (Biomerieux ref #73115) and Slidex MRSA detection Test Kit (Biomerieux ref #73117). In this work, positive (MRSA laboratory collection) and negative (S. aureus ATCC 25923) control strains were included as positive and negative controls.

3. Results

3.1. Swineries

S. aureus was detected in 54% of the 26 workers selected from 5 swineries, 8% of the workers were colonized with MSSA and 46% with MRSA. The prevalence of MRSA was 34% in the 42 pigs selected from maternities in 3 swineries and 66% in 30 pigs selected from stalls in 2 swineries. Swineries where the colonization by MRSA in animals was higher also demonstrated higher colonization in workers (Figure 1).

3.2. Veterinary Clinic

The prevalence of S. aureus in the 14 workers from the veterinary staff was 7.1% (1). The identified S. aureus strain was susceptible to methicillin (MSSA) (Figure 2).

3.3. Ambulances

The prevalence of S. aureus detected in the 98 environmental samples swabs collected in 12 ambulances from two fire stations was 3%, with only one colonized with MRSA. Of the 33 firefighters who participated in the study, 48.5% were colonized with S. aureus, 24% MSSA and 21% MRSA (Figure 3).

3.4. Healthcare Environment

In the study carried out at Hospital 1, 42.2% of the 38 healthcare workers were colonized with S. aureus, of which 18.4% were MSSA and 23.7% MRSA. The prevalence of MRSA at Hospital 2 was 43.3% in a population of 30 healthcare workers. In the study carried out at Primary Health Care Centers, no MRSA was detected from the nasal swabs of the 25 workers that participated (Figure 4).

3.5. Bakeries

In the assessed bakeries, we identified a 40% prevalence of asymptomatic S. aureus carriers among the workers, of which 75% were sensible to methicillin (MSSA) and 25% presented a resistance phenotype (MRSA). Overall MRSA was found in 10% of the analyzed samples (Figure 5).

3.6. Control Group

From 55 healthy volunteers without regular contact with the healthcare setting analyzed in the two studies, the prevalence of MRSA was 7%. Study 1, with 25 samples collected, had one MRSA strain (4%). Study 2, with 30 samples collected, identified 33.3% volunteers colonized with S. aureus, 23.3% were MSSA and 10% MRSA (Figure 6).

4. Discussion

Direct contact with pigs in swine occupational environment is a recognized risk factor for LA-MRSA colonization and swine workers, due to their daily work activities, are expected to be particularly highly exposed. In addition, veterinarians also have a significantly elevated risk of becoming LA-MRSA carriers [13,16,17]. In our study a higher prevalence was found in swine workers, but not in the veterinarians studied. This could be due to the fact that besides direct contact with infected animals occurring in both occupational environments, exposure to bioaerosols has also been suggested as a determinant for nasal carriage of LA-MRSA in swine workers [18], due to the dust present in swine [13,19]. In fact, during pig’s activity, emission of LA-MRSA may occur from mucus or by abscess of skin particles, and therefore bioaerosols can be released and disseminated in the stable air [20]. In addition, bioaerosols and dust may also constitute a source of transmission to humans outside the swine, due to emissions outside the swine or indirectly by contamination of workers cloths, tools, etc., which are brought out from swine facilities [21]. This could justify the increasing number of people without direct contact to livestock being registered as LA-MRSA positive [22,23,24,25], and also the results of our control groups.
To the best of our knowledge, this study is the first one reporting data concerning MRSA nasal carriage in bakery workers. As in the animal production setting, this occupational environment is prone increased exposure to flour dust and bioaerosols [26,27] and, consequently, the carriage of S. aureus and MRSA. Indeed, the dust can serve as a vehicle for microorganisms to workers respiratory airways, boosting workers exposure [13].
Data analysis revealed that healthcare occupational exposure, including ambulance crews, is concerningly high, following the trend already reported [6]. Previous studies carried out in Portugal emphasize that the main mode of transmission of MRSA is through the hands, with the absence of proper hand hygiene being the most common mode of transmission [28]. Thus, since health professionals are in direct contact with patients who may be contaminated, non-compliance with hygiene rules can be a way of spreading MRSA inside and outside the hospital environment, and in the community [29]. As previously mentioned, S. aureus has the ability to colonize different areas of the human body, with a preference for the nasopharynx [30] and the ability to spread as well as being transmitted by direct contact (mainly by hands) or indirect (contaminated surfaces) [31,32,33]. Indeed, one of its fundamental biological characteristics is the ability to colonize the healthy population asymptomatically (asymptomatic carrier), thus assuming an important role in spreading to other areas of the body, to other people and even contaminating food and surfaces during handling [31,32,33]. This colonization is considered a risk factor for the onset of infections by S. aureus, often combined with methicillin resistance-MRSA, increasing the risk of clinical disease [33,34].
The contrasting prevalence of MRSA colonization reported in each of the occupational environments assessed might be attributed to differences in hygiene practices and workers health education, both of which have a role in reducing MRSA contamination [35,36,37]. Another aspect to consider is S. aureus host-specificity, as companion animals treated at veterinary clinics are not frequently colonized by S. aureus, in contrast to meat-producing animals [38]. Thus, our results sustain the prerogative that exposure to bioaerosols at workplaces can represent a health hazard and potentially result in infectious disease [39], which is concerning both for workers and for the spread of these microorganisms in the community.
Staphylococcus aureus is reported as being a very robust species, which is highly resistant to environmental stress (e.g., desiccation) [40]. On surfaces, a persistence of 7 days to 7 months was reported [41] justifying the surface swabs as a sampling method to assess this species distribution, as was done for the ambulances´ surfaces. In the performed studies, environmental sampling was not in the aim and objectives of bakeries, swineries or healthcare facilities studied; however, the prevalence of S. aureus, including in the isolation of MRSA, reveals that dust is, in fact, a source of contamination and therefore, environmental sampling must be further included in colonization assessments. Furthermore, other sampling methods such as air and settled dust were already employed in different studies [16,18,21,42,43] corroborating the need to increase the protocol concerning the sampling approach to assess MRSA contamination in workplaces.
In order to provide more information regarding S. aureus colonization levels among workers from high risk occupational settings (of both human and animal colonization as well as food contamination), further studies should increase the sample number of assessed locations should be increased in future studies as well as different locations regarding the same occupational setting, and carry out continuous assessment over time. Furthermore, molecular biology methods could also be performed to assess clone origin (HA-MRSA; CA-MRSA; LA-MRSA) and enhance information regarding colonization origin.

5. Conclusions

Our results clearly sustain the need to develop accurate and efficient assessments of S. aureus for both human and animal colonization, particularly regarding MRSA, with proper guidelines and validated procedures. Considering S. aureus dissemination in the community, and the fact that it has the capacity to colonize asymptomatically (asymptomatic carrier) and spread to different areas of the body, other individuals and even food and surfaces during handling, the assessment of S. aureus in high risk occupational settings (including healthcare settings, animal productions and food handling) is crucial to avoid potential hazardous health outcomes associated with bioaerosols exposure including associated infectious diseases.

Author Contributions

Conceptualization, C.V. and E.R.; methodology, C.V. and E.R.; formal analysis, K.O., C.V. and E.R.; investigation, K.O., C.V. and E.R.; resources, C.V. and E.R.; writing—original draft preparation, K.O., C.V. and E.R.; writing—review and editing, K.O., C.V. and E.R.; supervision, C.V. and E.R.; project administration, C.V. and E.R.; funding acquisition, C.V. and E.R. All authors have read and agreed to the published version of the manuscript.

Funding

This research was supported by Instituto Politécnico de Lisboa, Lisbon, Portugal, by funding the Projects “Occupational exposure of ambulance drivers to bioburden” (IPL/2020/BIO-AmbuDrivers_ESTeSL) and “Bacterial Bioburden assessment in the context of occupational exposure and animal health of swine productions” (IPL/2016/BBIOR-Health).

Institutional Review Board Statement

The study was conducted according to the guidelines of the Declaration of Helsinki, and approved by the Ethics Committee of Escola Superior de Tecnologia da Saúde de Lisboa (Re: CE-ESTeSL-Nº 63-2019; CE-ESTeSL-Nº.18-2019).

Informed Consent Statement

Informed consent was obtained from all subjects involved in the study.

Data Availability Statement

Through the UIDB/05608/2020 and UIDP/05608/2020.

Acknowledgments

H&TRC authors gratefully acknowledge the FCT/MCTES national support through the UIDB/05608/2020 and UIDP/05608/2020.

Conflicts of Interest

The authors declare no conflict of interest.

References

  1. Lakhundi, S.; Zhang, K. Methicillin-Resistant Staphylococcus aureus: Molecular Characterization, Evolution, and Epidemiology. Clin. Microbiol. Rev. 2018, 31, e00020-18. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  2. Tong, S.Y.C.; Davis, J.S.; Eichenberger, E.; Holland, T.L.; Fowler, V.G., Jr. Staphylococcus aureus Infections: Epidemiology, Pathophysiology, Clinical Manifestations, and Management. Clin. Microbiol. Rev. 2015, 28, 603–661. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  3. Turner, N.A.; Sharma-Kuinkel, B.K.; Maskarinec, S.A.; Eichenberger, E.M.; Shah, P.P.; Carugati, M.; Holland, T.L.; Fowler, V.G., Jr. Methicillin-resistant Staphylococcus aureus: An overview of basic and clinical research. Nat. Rev. Microbiol. 2019, 17, 203–218. [Google Scholar] [CrossRef] [PubMed]
  4. European Centre for Disease Prevention and Control Surveillance of Antimicrobial Resistance in Europe—Annual Report of the European Antimicrobial Resistance Surveillance Network (EARS-Net) 2017; European Centre for Disease Prevention and Control (ECDC): Stockholm, Sweden, 2018; ISBN 978-2-85653-642-1.
  5. World Health Organisation WHO. What Is Antibiotic Resistance? Available online: https://sites.wpro.who.int/antibiotic_awareness/?page_id=96 (accessed on 22 January 2019).
  6. Programa de Prevenção e Controlo de Infeções e de Resistência Aos Antimicrobianos. Direção Geral Saúde 2017, 8, 24.
  7. Norma No 018/2014, atualizada a 27/04/2015; Prevenção e Controlo de Colonização e Infeção Por Staphylococcus aureus Resistente à Meticilina (MRSA) Nos Hospitais e Unidades de Internamento de Cuidados Continuados Integrados 2015; Direção Geral de Saúde: Lisbon, Portugal, 2015.
  8. Kinross, P.; Petersen, A.; Skov, R.; Van Hauwermeiren, E.; Pantosti, A.; Laurent, F.; Voss, A.; Kluytmans, J.; Struelens, M.J.; Heuer, O.; et al. Livestock-associated meticillin-resistant Staphylococcus aureus (MRSA) among human MRSA isolates, European Union/European Economic Area countries, 2013. Eurosurveillance 2017, 22, 16-00696. [Google Scholar] [CrossRef] [Green Version]
  9. European Food Safety Authority (EFSA); European Centre for Disease Prevention and Control (ECDC). The European Union summary report on antimicrobial resistance in zoonotic and indicator bacteria from humans, animals and food in 2017. EFSA J. 2019, 17, e05598. [Google Scholar] [CrossRef]
  10. Nair, R.; Perencevich, E.N.; Blevins, A.E.; Goto, M.; Nelson, R.E.; Schweizer, M.L. Clinical Effectiveness of Mupirocin for Preventing Staphylococcus aureus Infections in Nonsurgical Settings: A Meta-analysis. Clin. Infect. Dis. 2016, 62, 618–630. [Google Scholar] [CrossRef] [Green Version]
  11. Ribeiro, E.; Pereira, A.; Vieira, C.; Paulos, I.; Marques, M.; Swart, T.; Monteiro, A. Bacteria Bioburden Assessment and MRSA Colonization of Workers and Animals from a Portuguese Swine Production: A Case Report. In Occupational Safety and Hygiene VI; CRC Press: London, UK, 2018; pp. 351–354. [Google Scholar] [CrossRef]
  12. Ribeiro, E.; Monteiro, A. Bacterial Contamination Assessment and MRSA Colonization in the Context of Occupational Exposure in Portuguese Swine Productions. Int. Symp. Occup. Saf. Hyg. Proc. B. SHO 2020, 2020, 257–261. [Google Scholar]
  13. Viegas, C.; Monteiro, A.; Ribeiro, E.; Caetano, L.A.; Carolino, E.; Assunção, R.; Viegas, S. Organic dust exposure in veterinary clinics: A case study of a small-animal practice in Portugal. Arch. Ind. Hyg. Toxicol. 2018, 69, 309–316. [Google Scholar] [CrossRef] [Green Version]
  14. Viegas, C.; Sousa, P.; Dias, M.; Caetano, L.A.; Ribeiro, E.; Carolino, E.; Twarużek, M.; Kosicki, R.; Viegas, S. Bioburden contamination and Staphylococcus aureus colonization associated with firefighter’s ambulances. Environ. Res. 2021, 197, 111125. [Google Scholar] [CrossRef]
  15. Negrinho, A.; Serrano, D.; Shone, S.; Ribeiro, E.; Ferreira, B. Prevalência Da Colonização Nasal Por MRSA Nos Técnicos de ACSP Num Hospital Do Distrito de Lisboa: Estudo-Caso. In Proceedings of the III Congresso Nacional de Ciências Biomédicas Laboratoriais, Lisbon, Portugal, 25–27 October 2019. [Google Scholar]
  16. Dahms, C.; Hübner, N.-O.; Cuny, C.; Kramer, A. Occurrence of methicillin-resistant Staphylococcus aureus in farm workers and the livestock environment in Mecklenburg-Western Pomerania, Germany. Acta Vet. Scand. 2014, 56, 53. [Google Scholar] [CrossRef] [PubMed]
  17. Van Cleef, B.A.G.L.; Van Benthem, B.H.B.; Verkade, E.J.M.; Van Rijen, M.M.L.; Kluytmans-van den Bergh, M.F.Q.; Graveland, H.; Bosch, T.; Verstappen, K.M.H.W.; Wagenaar, J.A.; Bos, M.E.H.; et al. Livestock-Associated MRSA in Household Members of Pig Farmers: Transmission and Dynamics of Carriage, A Prospective Cohort Study. PLoS ONE 2015, 10, e0127190. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  18. Bos, M.E.H.; Verstappen, K.M.; van Cleef, B.A.G.L.; Dohmen, W.; Dorado-García, A.; Graveland, H.; Duim, B.; Wagenaar, J.A.; Kluytmans, J.A.J.W.; Heederik, D.J.J. Transmission through air as a possible route of exposure for MRSA. J. Expo. Sci. Environ. Epidemiol. 2016, 26, 263–269. [Google Scholar] [CrossRef] [PubMed]
  19. Viegas, C.; Faria, T.; Monteiro, A.; Caetano, L.A.; Carolino, E.; Gomes, A.Q.; Viegas, S. A Novel Multi-Approach Protocol for the Characterization of Occupational Exposure to Organic Dust—Swine Production Case Study. Toxics 2017, 6, 5. [Google Scholar] [CrossRef] [Green Version]
  20. Zhao, Y.; Aarnink, A.J.A.; de Jong, M.C.M.; Groot Koerkamp, P.W.G. Airborne Microorganisms from Livestock Production Systems and Their Relation to Dust. Crit. Rev. Environ. Sci. Technol. 2014, 44, 1071–1128. [Google Scholar] [CrossRef]
  21. Feld, L.; Bay, H.; Angen, Ø.; Larsen, A.R.; Madsen, A.M. Survival of LA-MRSA in Dust from Swine Farms. Ann. Work Expo. Health 2018, 62, 147–156. [Google Scholar] [CrossRef] [Green Version]
  22. van Rijen, M.M.L.; Bosch, T.; Verkade, E.J.M.; Schouls, L.; Kluytmans, J.A.J.W.; on behalf of the CAM Study Group. Livestock-Associated MRSA Carriage in Patients without Direct Contact with Livestock. PLoS ONE 2014, 9, e100294. [Google Scholar] [CrossRef] [Green Version]
  23. Larsen, J.; Petersen, A.; Sørum, M.; Stegger, M.; Van Alphen, L.; Valentiner-Branth, P.; Knudsen, L.K.; Larsen, L.S.; Feingold, B.; Price, L.B.; et al. Meticillin-resistant Staphylococcus aureus CC398 is an increasing cause of disease in people with no livestock contact in Denmark, 1999 to 2011. Eurosurveillance 2015, 20, 30021. [Google Scholar] [CrossRef] [Green Version]
  24. Deiters, C.; Günnewig, V.; Friedrich, A.W.; Mellmann, A.; Köck, R. Are cases of Methicillin-resistant Staphylococcus aureus clonal complex (CC) 398 among humans still livestock-associated? Int. J. Med. Microbiol. 2015, 305, 110–113. [Google Scholar] [CrossRef]
  25. Nielsen, R.T.; Kemp, M.; Holm, A.; Skov, M.N.; Detlefsen, M.; Hasman, H.; Aarestrup, F.M.; Kaas, R.S.; Nielsen, J.B.; Westh, H.; et al. Fatal Septicemia Linked to Transmission of MRSA Clonal Complex 398 in Hospital and Nursing Home, Denmark. Emerg. Infect. Dis. 2016, 22, 900–902. [Google Scholar] [CrossRef] [Green Version]
  26. Viegas, C.; Faria, T.; Caetano, L.A.; Carolino, E.; Quintal-Gomes, A.; Twarużek, M.; Kosicki, R.; Viegas, S. Characterization of Occupational Exposure To Fungal Burden in Portuguese Bakeries. Microorganisms 2019, 7, 234. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  27. Viegas, C.; Fleming, G.T.A.; Kadir, A.; Almeida, B.; Caetano, L.A.; Gomes, A.Q.; Twarużek, M.; Kosicki, R.; Viegas, S.; Coggins, A.M.; et al. Occupational Exposures to Organic Dust in Irish Bakeries and a Pizzeria Restaurant. Microorganisms 2020, 8, 118. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  28. Mondal, H.; Gupta, I.; Nandi, P.; Ghosh, P.; Chattopadhyay, S.; Mitra, G.D. Nasal Screening of Healthcare Workers for Nasal Carriage of Methicillin Resistance Staphylococcus aureus, Vancomycin Resistance Staphylococcus aureus and Prevalence of Nasal Colonization with Staphylococcus aureus in Burdwan Medical College and Hospital. Int. J. Contemp. Med. Res. 2016, 3, 3342–3346. [Google Scholar]
  29. Dulon, M.; Peters, C.; Schablon, A.; Nienhaus, A. MRSA carriage among healthcare workers in non-outbreak settings in Europe and the United States: A systematic review. BMC Infect. Dis. 2014, 14, 363. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  30. Mainous, A.G.; Hueston, W.J.; Everett, C.J.; Diaz, V.A. Nasal Carriage of Staphylococcus aureus and Methicillin-Resistant S aureus in the United States, 2001–2002. Ann. Fam. Med. 2006, 4, 132–137. [Google Scholar] [CrossRef] [Green Version]
  31. Touimi, G.B.; Bennani, L.; Berrada, S.; Moussa, B.; Bennani, B. Prevalence and antibiotic resistance profiles of Staphylococcus sp. isolated from food, food contact surfaces and food handlers in a Moroccan hospital kitchen. Lett. Appl. Microbiol. 2020, 70, 241–251. [Google Scholar] [CrossRef] [PubMed]
  32. Ahmed, O.B. Prevalence of Methicillin-Resistant Staphylococcus aureus and Classical Enterotoxin Genes among Sudanese Food Handlers. Cureus 2020, 12, e12289. [Google Scholar] [CrossRef]
  33. Ribeiro, E.; Clérigo, A. Assessment of Staphylococcus aureus Colonization in Bakery Workers: A Case Study. In Vertentes e Desafios da Segurança 2017;. Leiria, Portugal, 2017. In Vertentes e Desafios da Segurança 2017; Simões & Linhares: Leiria, Portugal.
  34. Ghasemzadeh-Moghaddam, H.; Neela, V.; van Wamel, W.; Hamat, R.A.; Shamsudin, M.N.; Hussin, N.S.C.; Aziz, M.N.; Haspani, M.S.M.; Johar, A.; Thevarajah, S.; et al. Nasal carriers are more likely to acquire exogenous Staphylococcus aureus strains than non-carriers. Clin. Microbiol. Infect. 2015, 21, 998.e1–998.e7. [Google Scholar] [CrossRef] [Green Version]
  35. Pittet, D.; Hugonnet, S.; Harbarth, S.; Mourouga, P.; Sauvan, V.; Touveneau, S.; Perneger, T.V. Effectiveness of a hospital-wide programme to improve compliance with hand hygiene. Lancet 2000, 356, 1307–1312. [Google Scholar] [CrossRef]
  36. Safdar, N.; Abad, C. Educational interventions for prevention of healthcare-associated infection: A systematic review. Crit. Care Med. 2008, 36, 933–940. [Google Scholar] [CrossRef]
  37. Rohde, R.E.; Ross-Gordon, J. MRSA model of learning and adaptation: A qualitative study among the general public. BMC Health Serv. Res. 2012, 12, 88. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  38. Haag, A.F.; Fitzgerald, J.R.; Penadés, J.R. Staphylococcus aureus in Animals. Microbiol. Spectr. 2019, 7. [Google Scholar] [CrossRef] [PubMed]
  39. Walser, S.M.; Gerstner, D.G.; Brenner, B.; Bünger, J.; Eikmann, T.; Janssen, B.; Kolb, S.; Kolk, A.; Nowak, D.; Raulf, M.; et al. Evaluation of exposure–response relationships for health effects of microbial bioaerosols–A systematic review. Int. J. Hyg. Environ. Health 2015, 218, 577–589. [Google Scholar] [CrossRef] [PubMed]
  40. Clements, M.O.; Foster, S.J. Stress resistance in Staphylococcus aureus. Trends Microbiol. 1999, 7, 458–462. [Google Scholar] [CrossRef]
  41. Kramer, A.; Schwebke, I.; Kampf, G. How long do nosocomial pathogens persist on inanimate surfaces? A systematic review. BMC Infect. Dis. 2006, 6, 130. [Google Scholar] [CrossRef] [Green Version]
  42. Schulz, J.; Friese, A.; Klees, S.; Tenhagen, B.A.; Fetsch, A.; Rösler, U.; Hartung, J. Longitudinal Study of the Contamination of Air and of Soil Surfaces in the Vicinity of Pig Barns by Livestock-Associated Methicillin-Resistant Staphylococcus aureus. Appl. Environ. Microbiol. 2012, 78, 5666–5671. [Google Scholar] [CrossRef] [Green Version]
  43. Agersø, Y.; Vigre, H.; Cavaco, L.M.; Josefsen, M.H. Comparison of air samples, nasal swabs, ear-skin swabs and environmental dust samples for detection of methicillin-resistant Staphylococcus aureus (MRSA) in pig herds. Epidemiol. Infect. 2014, 142, 1727–1736. [Google Scholar] [CrossRef]
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Figure 1. MRSA prevalence in the swinneries.
Figure 1. MRSA prevalence in the swinneries.
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Figure 2. MRSA prevalence in the veterinary clinic.
Figure 2. MRSA prevalence in the veterinary clinic.
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Figure 3. MRSA prevalence in the ambulances and crew.
Figure 3. MRSA prevalence in the ambulances and crew.
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Figure 4. MRSA prevalence in the healthcare workers.
Figure 4. MRSA prevalence in the healthcare workers.
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Figure 5. MRSA prevalence in the bakery workers.
Figure 5. MRSA prevalence in the bakery workers.
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Figure 6. MRSA distribution in the control groups.
Figure 6. MRSA distribution in the control groups.
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Table
Table 1. Environmental and biological samples collected in each workplace environment.
Table 1. Environmental and biological samples collected in each workplace environment.
Occupational Environment/Control GroupBiological SamplesEnvironmental SamplesReferences
Swineries
(N = 5)		Nasopharyngeal swabs
(N = 68; 26 humans and 42 animals)		Not performed[11,12]
Veterinary clinic (N = 1)Nasopharyngeal swabs
(N = 14)		Not performed[13]
Ambulance crew (N = 12) Nasopharyngeal swabs
(N = 33)		Surface swabs (N = 98) performed on floor, gurney handle, chairs, entrance and ceiling handle, washstand, shelves, driver’s cabin (wheel) and air exit of the medical cabin[14]
Healthcare
Environment
(N = 3)		Nasopharyngeal swabs
(N = 93; 38 from Hospital 1, 30 from Hospital 2, 25 from PHCC)		Not performed[15]
Bakeries
(N = 13)		Nasopharyngeal swabs
(N = 74)		Not performedData not published
Control group
(N = 2)		Nasopharyngeal swabs
(N = 55; 25 from Study 1, 30 from Study 2)		Not performedData not published
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Oliveira, K.; Viegas, C.; Ribeiro, E. MRSA Colonization in Workers from Different Occupational Environments—A One Health Approach Perspective. Atmosphere 2022, 13, 658. https://doi.org/10.3390/atmos13050658

AMA Style

Oliveira K, Viegas C, Ribeiro E. MRSA Colonization in Workers from Different Occupational Environments—A One Health Approach Perspective. Atmosphere. 2022; 13(5):658. https://doi.org/10.3390/atmos13050658

Chicago/Turabian Style

Oliveira, Ketlyn, Carla Viegas, and Edna Ribeiro. 2022. "MRSA Colonization in Workers from Different Occupational Environments—A One Health Approach Perspective" Atmosphere 13, no. 5: 658. https://doi.org/10.3390/atmos13050658

APA Style

Oliveira, K., Viegas, C., & Ribeiro, E. (2022). MRSA Colonization in Workers from Different Occupational Environments—A One Health Approach Perspective. Atmosphere, 13(5), 658. https://doi.org/10.3390/atmos13050658

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