Evaluation of Antibiotic Resistance in Bacterial Strains Isolated from Sewage of Slaughterhouses Located in Sicily (Italy)
Abstract
:1. Introduction
2. Materials and Methods
2.1. Sampling Area
2.2. Samples Collection and Treatment
2.3. Isolation and Selection of Bacteria
2.4. Phenotypic Identification of Bacteria
2.5. Antibiotic Susceptibility
- (1)
- Beta-lactams, including penicillins (ampicillin (AMP, 10 μg), carbenicillin (CAR, 100 μg), mezlocillin (MEZ, 75 μg), piperacillin (PRL, 100 μg)), monobactams (aztreonam (ATM, 30 μg)), cephalosporins (cefazolin (KZ, 30 μg), cefoxitin (FOX, 30 μg), cefuroxime (CXM, 30 μg), cefotaxime (CTX, 30 μg), ceftazidime (CAZ, 30 μg), ceftriaxone (CRO, 30 μg)), carbapenems (imipinem (IMI,10 μg);
- (2)
- Fosfomycin (FOS, 50 μg);
- (3)
- Polymyxin (colistin sulphate (CS, 10 μg)).
- (1)
- Quinolones (nalidixic acid (NA, 30 μg), pipemidic acid (PI, 20 μg)); fluoroquinolones (ciprofloxacin (CIP, 5 μg), levofloxacin (LEV, 5 μg), norfloxacin (NOR, 10 μg) ofloxacin (OFX, 5 μg));
- (2)
- DNA inhibitors (nitrofurantoin (F, 300 μg));
- (3)
- RNA synthesis inhibitors: rifampicins (rifampicin (RD, 30 μg)).
- (1)
- Aminoglycosides (amikacin (AK, 30 μg), gentamycin (CN, 10 μg), netilmicin (NET, 30 μg), tobramycin (TOB, 10 μg));
- (2)
- Glicilglicines (tigecycline (TGC, 15 μg));
- (3)
- Macrolides (azithromycin (AZM, 15 μg));
- (4)
- Phenicol derivatives (chloramphenicol (C, 30 μg));
- (5)
- Tetracyclines (tetracycline (TE, 30 μg, CT0054B)).
3. Results
3.1. Bacteriological Monitoring
3.2. Evaluation of Antibiotic Resistance
4. Discussion
5. Conclusions
6. Limits of the Study
Supplementary Materials
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Conflicts of Interest
References
- De Kraker, M.E.A.; Stewardson, A.J.; Harbarth, S. Will 10 million people die a year due to antimicrobial resistance by 2050? PLoS Med. 2016, 13, e1002184. [Google Scholar] [CrossRef] [Green Version]
- O’Neill, J. Tackling Drug-Resistant Infections Globally: Final Report and Recommendations the Review on Antimicrobial Resistance. 2016. Available online: https://www.biomerieuxconnection.com/wp-content/uploads/2018/04/Tackling-Drug-Resistant-Infections-Globally_-Final-Report-and-Recommendations.pdf (accessed on 2 September 2021).
- Tacconelli, E.; Magrini, N. Global Priority List of Antibiotic-Resistant Bacteria to Guide Research, Discovery, and Development of New Antibiotics. 2017. Available online: https://www.who.int/medicines/publications/WHO-PPL-Short_Summary_25Feb-ET_NM_WHO.pdf (accessed on 2 September 2021).
- Santajit, S.; Indrawattana, N. Mechanisms of antimicrobial resistance in ESKAPE pathogens. BioMed Res. Int. 2016, 2016, 2475067. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Stilo, A.; Troiano, G.; Melcarne, L.; Gioffrè, M.E.; Nante, N.; Messina, G.; Laganà, P. Hand washing in operating room: A procedural comparison. Epidemiol. Biostat. Public Health 2016, 13, e11734-1–e11734-7. [Google Scholar] [CrossRef]
- Facciolà, A.; Pellicano, G.F.; Visalli, G.; Paolucci, I.A.; Rullo, E.V.; Ceccarelli, M.; D’Aleo, F.; Di Pietro, A.; Squeri, R.; Nunnari, G.; et al. The role of the hospital environment in the healthcare-associated infections: A general review of the literature. Eur. Rev. Med. Pharmacol. Sci. 2019, 23, 1266–1278. [Google Scholar] [PubMed]
- De Oliveira, D.M.P.; Forde, B.M.; Kidd, T.J.; Harris, P.N.A.; Schembri, M.A.; Beatson, S.A.; Paterson, D.L.; Walker, M.J. Antimicrobial Resistance in ESKAPE pathogens. Clin. Microbiol. Rev. 2020, 33, e00181–e00219. [Google Scholar] [CrossRef]
- Collignon, P.J.; McEwen, S.A. One health—Its importance in helping to better control antimicrobial resistance. Trop. Med. Infect. Dis. 2019, 4, 22. [Google Scholar] [CrossRef] [Green Version]
- Laganà, P.; Delia, S.; Di Pietro, A.; Costa, A.; Coniglio, M.A. Antibiotic resistance in bacteria strains isolated from foods and correlated environments. Prog. Nutr. 2020, 22, e2020041. [Google Scholar] [CrossRef]
- Marshall, B.M.; Levy, S.B. Food animals and antimicrobials: Impacts on human health. Clin. Microbiol. Rev. 2011, 24, 718–733. [Google Scholar] [CrossRef] [Green Version]
- Resistance WAGoISoAO. Critically Important Antimicrobials for Human Medicine: Ranking of Antimicrobial Agents for Risk Management of Antimicrobial Resistance Due to Non-Human Use, 5th ed.; World Health Organization: Geneva, Switzerland, 2017. [Google Scholar]
- Tang, K.L.; Caffrey, N.P.; Nóbrega, D.; Cork, S.C.; Ronksley, P.E.; Barkema, H.; Polachek, A.J.; Ganshorn, H.; Sharma, N.; Kellner, J.; et al. Restricting the use of antibiotics in food-producing animals and its associations with antibiotic resistance in food-producing animals and human beings: A systematic review and meta-analysis. Lancet Planet. Health 2017, 1, e316–e327. [Google Scholar] [CrossRef]
- Tang, K.L.; Caffrey, N.P.; Nóbrega, D.; Cork, S.C.; Ronksley, P.E.; Barkema, H.; Polachek, A.J.; Ganshorn, H.; Sharma, N.; Kellner, J.; et al. Comparison of different approaches to antibiotic restriction in food-producing animals: Stratified results from a systematic review and meta-analysis. BMJ Glob. Health 2019, 4, e001710. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Mancuso, M.; Catalfamo, M.; Laganà, P.; Rappazzo, A.C.; Raymo, V.; Zampino, D.; Zaccone, R. Screening of antimicrobial activity of citrus essential oils against pathogenic bacteria and Candida strains. Flavour Fragr. J. 2019, 34, 187–200. [Google Scholar] [CrossRef]
- Laganà, P.; Anastasi, G.; Marano, F.; Piccione, S.; Singla, R.K.; Dubey, A.K.; Delia, S.; Coniglio, M.; Facciolà, A.; Di Pietro, A.; et al. Phenolic substances in foods: Health effects as anti-inflammatory and antimicrobial agents. J. AOAC Int. 2019, 102, 1378–1387. [Google Scholar] [CrossRef]
- Coniglio, M.A.; Laganà, P.; Faro, G.; Marranzano, M. Antimicrobial potential of Sicilian honeys against Staphylococcus aureus and pseudomonas aeruginosa. J. AOAC Int. 2018, 101, 956–959. [Google Scholar] [CrossRef] [PubMed]
- Leistner, R.; Meyer, E.; Gastmeier, P.; Pfeifer, Y.; Eller, C.; Dem, P.; Schwab, F. Risk factors associated with the community-acquired colonization of extended-spectrum beta-lactamase (ESBL) positive escherichia coli. An exploratory case-control study. PLoS ONE 2013, 8, e74323. [Google Scholar] [CrossRef] [PubMed]
- Ye, Q.; Wu, Q.; Zhang, S.; Zhang, J.; Yang, G.; Wang, J.; Xue, L.; Chen, M. Characterization of extended-spectrum β-lactamase-producing enterobacteriaceae from retail food in China. Front. Microbiol. 2018, 9, 1709. [Google Scholar] [CrossRef] [PubMed]
- Du, L.; Liu, W. Occurrence, fate, and ecotoxicity of antibiotics in agro-ecosystems. A review. Agron. Sustain. Dev. 2011, 32, 309–327. [Google Scholar] [CrossRef] [Green Version]
- Rousham, E.K.; Unicomb, L.; Islam, M.A. Human, animal and environmental contributors to antibiotic resistance in low-resource settings: Integrating behavioural, epidemiological and One Health approaches. Proc. R. Soc. B Biol. Sci. 2018, 285, 20180332. [Google Scholar] [CrossRef]
- Savin, M.; Bierbaum, G.; Hammerl, J.A.; Heinemann, C.; Parcina, M.; Sib, E.; Voigt, A.; Kreyenschmidt, J. Antibiotic-resistant bacteria and antimicrobial residues in wastewater and process water from German pig slaughterhouses and their receiving municipal wastewater treatment plants. Sci. Total Environ. 2020, 727, 138788. [Google Scholar] [CrossRef]
- Savin, M.; Bierbaum, G.; Hammerl, J.A.; Heinemann, C.; Parcina, M.; Sib, E.; Voigt, A.; Kreyenschmidt, J. ESKAPE bacteria and extended-spectrum-β-lactamase-producing Escherichia coli isolated from wastewater and process water from German poultry slaughterhouses. Appl. Environ. Microbiol. 2020, 86, e02748-19. [Google Scholar] [CrossRef] [Green Version]
- Blaak, H.; Van Hoek, A.H.A.M.; Hamidjaja, R.; Van Der Plaats, R.Q.J.; Heer, L.K.-D.; Husman, A.M.D.R.; Schets, F.M. Distribution, numbers, and diversity of ESBL-producing E. coli in the poultry farm environment. PLoS ONE 2015, 10, e0135402. [Google Scholar] [CrossRef]
- Müller, H.; Sib, E.; Gajdiss, M.; Klanke, U.; Lenz-Plet, F.; Barabasch, V.; Albert, C.; Schallenberg, A.; Timm, C.; Zacharias, N.; et al. Dissemination of multi-resistant Gram-negative bacteria into German wastewater and surface waters. FEMS Microbiol. Ecol. 2018, 94, fiy057. [Google Scholar] [CrossRef]
- Kaesbohrer, A.; Bakran-Lebl, K.; Irrgang, A.; Fischer, J.; Kämpf, P.; Schiffmann, A.; Werckenthin, C.; Busch, M.; Kreienbrock, L.; Hille, K. Diversity in prevalence and characteristics of ESBL/pAmpC producing E. coli in food in Germany. Veter. Microbiol. 2019, 233, 52–60. [Google Scholar] [CrossRef]
- Dohmen, W.; Van Gompel, L.; Schmitt, H.; Liakopoulos, A.; Heres, L.; Urlings, B.A.; Mevius, D.; Bonten, M.J.M.; Heederik, D.J.J. ESBL carriage in pig slaughterhouse workers is associated with occupational exposure. Epidemiol. Infect. 2017, 145, 2003–2010. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Fischer, J.; Hille, K.; Ruddat, I.; Mellmann, A.; Köck, R.; Kreienbrock, L. Simultaneous occurrence of MRSA and ESBL-producing Enterobacteriaceae on pig farms and in nasal and stool samples from farmers. Vet. Microbiol. 2017, 200, 107–113. [Google Scholar] [CrossRef]
- Wadepohl, K.; Müller, A.; Seinige, D.; Rohn, K.; Blaha, T.; Meemken, D.; Kehrenberg, C. Association of intestinal colonization of ESBL-producing Enterobacteriaceae in poultry slaughterhouse workers with occupational exposure—A German pilot study. PLoS ONE 2020, 15, e0232326. [Google Scholar] [CrossRef] [PubMed]
- Centro di Referenza Nazionale per l’Antibioticoresistenza (CRAB). Piano di Monitoraggio Armonizzato sulla Resistenza Agli Antimicrobici di Batteri Zoonotici e Commensali. 2021. Available online: https://www.izslt.it/crab/wp-content/uploads/sites/8/2020/12/Piano-AMR_2021.pdf (accessed on 2 September 2021).
- European Commission. Rapid Alert System for Food and Feed (RASFF). 2021. Available online: https://ec.europa.eu/food/safety/rasff-food-and-feed-safety-alerts/rasff-portal_en (accessed on 2 September 2021).
- European Committee on Antimicrobial Susceptibility Testing (EUCAST). Development and Validation of EUCAST Disk Diffusion Breakpoints. 2021. Available online: https://www.eucast.org/ast_of_bacteria/calibration_and_validation/ (accessed on 2 September 2021).
- Laganà, P.; Votano, L.; Caruso, G.; Azzaro, M.; Giudice, A.L.; Delia, S. Bacterial isolates from the Arctic region (Pasvik River, Norway): Assessment of biofilm production and antibiotic susceptibility profiles. Environ. Sci. Pollut. Res. 2017, 25, 1089–1102. [Google Scholar] [CrossRef] [PubMed]
- Savin, M.; Bierbaum, G.; Blau, K.; Parcina, M.; Sib, E.; Smalla, K.; Schmithausen, R.; Heinemann, C.; Hammerl, J.A.; Kreyenschmidt, J. Colistin-resistant enterobacteriaceae isolated from process waters and wastewater from German poultry and pig slaughterhouses. Front. Microbiol. 2020, 11, 575391. [Google Scholar] [CrossRef] [PubMed]
- Olawale, S.I.; Busayo, O.-O.M.; Olatunji, O.I.; Mariam, M.; Olayinka, O.S. Plasmid profiles and antibiotic susceptibility patterns of bacteria isolated from abattoirs wastewater within Ilorin, Kwara, Nigeria. Iran. J. Microbiol. 2020, 12, 547–555. [Google Scholar] [CrossRef] [PubMed]
- European Food Safety Authority (EFSA). Role Played by the Environment in the Emergence and Spread of Antimicrobial Resistance (AMR) Through the Food Chain. 2021. Available online: https://www.efsa.europa.eu/en/efsajournal/pub/6651 (accessed on 2 September 2021).
- Pacholewicz, E.; Swart, A.; Schipper, M.; Gortemaker, B.G.; Wagenaar, J.A.; Havelaar, A.H.; Lipman, L.J. A comparison of fluctuations of Campylobacter and Escherichia coli concentrations on broiler chicken carcasses during processing in two slaughterhouses. Int. J. Food Microbiol. 2015, 205, 119–127. [Google Scholar] [CrossRef]
- Van Gompel, L.; Dohmen, W.; Luiken, R.E.C.; Bouwknegt, M.; Heres, L.; Van Heijnsbergen, E.; Jongerius-Gortemaker, B.G.M.; Scherpenisse, P.; Greve, G.D.; Tersteeg-Zijderveld, M.H.G.; et al. Occupational exposure and carriage of antimicrobial resistance genes (tetW, ermB) in pig slaughterhouse workers. Ann. Work. Expo. Health 2019, 64, 125–137. [Google Scholar] [CrossRef] [Green Version]
- Schmithausen, R.M.; Schulze-Geisthoevel, S.V.; Stemmer, F.; El-Jade, M.; Reif, M.; Hack, S.; Meilaender, A.; Montabauer, G.; Fimmers, R.; Parčina, M.; et al. Analysis of transmission of MRSA and ESBL-E among pigs and farm personnel. PLoS ONE 2015, 10, e0138173. [Google Scholar] [CrossRef]
- Zurfluh, K.; Hächler, H.; Nüesch-Inderbinen, M.; Stephan, R. Characteristics of extended-spectrum β-lactamase- and carbapenemase-producing enterobacteriaceae isolates from rivers and lakes in Switzerland. Appl. Environ. Microbiol. 2013, 79, 3021–3026. [Google Scholar] [CrossRef] [Green Version]
- Ben Said, L.; Jouini, A.; Klibi, N.; Dziri, R.; Alonso, C.A.; Boudabous, A.; Ben Slama, K.; Torres, C. Detection of extended-spectrum beta-lactamase (ESBL)-producing Enterobacteriaceae in vegetables, soil and water of the farm environment in Tunisia. Int. J. Food Microbiol. 2015, 203, 86–92. [Google Scholar] [CrossRef]
- Liu, X.; Thungrat, K.; Boothe, D.M. Occurrence of OXA-48 carbapenemase and other β-lactamase genes in ESBL-producing multidrug resistant Escherichia coli from dogs and cats in the United States, 2009–2013. Front. Microbiol. 2016, 7, 1057. [Google Scholar] [CrossRef] [Green Version]
- Hammerum, A.M.; Larsen, J.; Andersen, V.D.; Lester, C.H.; Skytte, T.S.S.; Hansen, F.; Olsen, S.S.; Mordhorst, H.; Skov, R.L.; Aarestrup, F.; et al. Characterization of extended-spectrum β-lactamase (ESBL)-producing Escherichia coli obtained from Danish pigs, pig farmers and their families from farms with high or no consumption of third- or fourth-generation cephalosporins. J. Antimicrob. Chemother. 2014, 69, 2650–2657. [Google Scholar] [CrossRef] [PubMed]
- Diallo, A.A.; Brugère, H.; Kérourédan, M.; Dupouy, V.; Toutain, P.-L.; Bousquet-Melou, A.; Oswald, E.; Bibbal, D. Persistence and prevalence of pathogenic and extended-spectrum beta-lactamase-producing Escherichia coli in municipal wastewater treatment plant receiving slaughterhouse wastewater. Water Res. 2013, 47, 4719–4729. [Google Scholar] [CrossRef]
- Wan, M.T.; Chou, C.C. Spreading of β -lactam resistance gene (mecA) and methicillin-resistant Staphylococcus aureus through municipal and swine slaughterhouse wastewaters. Water Res. 2014, 64, 288–295. [Google Scholar] [CrossRef]
- Wan, M.T.; Chou, C.C. Class 1 integrons and the antiseptic resistance gene (qacEΔ1) in municipal and swine slaughterhouse wastewater treatment plants and wastewater—Associated methicillin-resistant Staphylococcus aureus. Int. J. Environ. Res. Public Health 2015, 12, 6249–6260. [Google Scholar] [CrossRef]
- Pessoa, R.B.G.; de Oliveira, W.F.; Marques, D.S.C.; Correia, M.T.D.S.; de Carvalho, E.V.M.M.; Coelho, L.C.B.B. The genus Aeromonas: A general approach. Microb. Pathog. 2019, 130, 81–94. [Google Scholar] [CrossRef] [PubMed]
- Saavedra, M.; Guedes-Novais, S.; Alves, A.; Rema, P.; Tacao, M.; Correia, A.; Martínez-Murcia, A. Resistance to β-lactam antibiotics in Aeromonas hydrophila isolated from rainbow trout (Oncorhynchus mykiss). Int. Microbiol. 2004, 7, 207–211. [Google Scholar] [PubMed]
- Li, L.; Olsen, R.H.; Ye, L.; Yan, H.; Nie, Q.; Meng, H.; Shi, L. Antimicrobial resistance and resistance genes in aerobic bacteria isolated from pork at slaughter. J. Food Prot. 2016, 79, 589–597. [Google Scholar] [CrossRef] [PubMed]
- Stratev, D.; Odeyemi, O. Antimicrobial resistance of Aeromonas hydrophila isolated from different food sources: A mini-review. J. Infect. Public Health 2016, 9, 535–544. [Google Scholar] [CrossRef] [Green Version]
- Roth, N.; Käsbohrer, A.; Mayrhofer, S.; Zitz, U.; Hofacre, C.; Domig, K.J. The application of antibiotics in broiler production and the resulting antibiotic resistance in Escherichia coli: A global overview. Poult. Sci. 2019, 98, 1791–1804. [Google Scholar] [CrossRef] [PubMed]
- Poole, T.; Sheffield, C. Use and misuse of antimicrobial drugs in poultry and livestock: Mechanisms of antimicrobial resistance. Pak. Vet. J. 2013, 33, 266–271. [Google Scholar]
- United States Department of Agriculture. Economics of Antibiotic Use in US Livestock Production. 2015. Available online: https://www.ers.usda.gov/media/1950577/err200.pdf (accessed on 2 September 2021).
- Machalaba, C.; Raufman, J.; Anyamba, A.; Berrian, A.M.; Berthe, F.C.J.; Gray, G.C.; Jonas, O.; Karesh, W.B.; Larsen, M.H.; Laxminarayan, R.; et al. Applying a One Health approach in global health and medicine: Enhancing involvement of medical schools and global health centers. Ann. Glob. Health 2021, 87, 30. [Google Scholar] [CrossRef]
- European Union. Ban on Antibiotics as Growth Promoters in Animal Feed Enters into Effect. 2006. Available online: https://ec.europa.eu/commission/presscorner/detail/en/IP_05_1687 (accessed on 2 September 2021).
- AccessScience Editors. U.S. Bans Antibiotics Use for Enhancing Growth in Livestock; McGraw-Hill Education: New York, NY USA, 2017. [Google Scholar] [CrossRef] [Green Version]
- World Health Organization (WHO). Stop Using Antibiotics in Healthy Animals to Prevent the Spread of Antibiotic Resistance. 2017. Available online: https://www.who.int/news/item/07-11-2017-stop-using-antibiotics-in-healthy-animals-to-prevent-the-spread-of-antibiotic-resistance (accessed on 2 September 2021).
- World Health Organization. Critically Important Antimicrobials for Human Medicine; 6th rev.; World Health Organization: Geneva, Switzerland, 2018; Available online: https://apps.who.int/iris/bitstream/handle/10665/312266/9789241515528-eng.pdf (accessed on 2 September 2021).
Aeromonas spp. | Citrobacter spp. | Enterobacter spp. | E. coli | Proteus spp. | Pseudomonas spp. | |
---|---|---|---|---|---|---|
Aminoglycosides | 7.2 | 0.0 | 9.4 | 0.0 | 2.2 | 5.5 |
Carbapenems | 14.3 | 0.0 | 12.5 | 0.0 | 0.0 | 18.2 |
Cephalosporins | 28.6 | 33.3 | 75.0 | 50.0 | 48.1 | 60.6 |
Cloramphenicol | 0.0 | 0.0 | 12.5 | 0.0 | 33.3 | 45.5 |
Colistine | 28.6 | 33.3 | 0.0 | 50.0 | 33.3 | 9.1 |
Fosfomycin | 57.1 | 0.0 | 75.0 | 50.0 | 33.3 | 18.2 |
Macrolides | 71.4 | 100.0 | 87.5 | 100.0 | 88.9 | 63.6 |
Monobactams | 28.6 | 33.3 | 75.0 | 0.0 | 33.3 | 33.3 |
Nitrofurans | 57.1 | 66.7 | 87.5 | 100.0 | 66.7 | 63.6 |
Penicillins | 40.0 | 33.3 | 72.0 | 50.0 | 28.5 | 68.9 |
Quinolones | 11.4 | 6.7 | 32.5 | 12.5 | 22.2 | 19.2 |
Rifampicin | 42.9 | 100.0 | 87.5 | 100.0 | 33.3 | 54.5 |
Tetracyclines | 71.4 | 33.3 | 87.5 | 50.0 | 55.6 | 54.5 |
Tigecycline | 57.1 | 100.0 | 87.5 | 100.0 | 77.8 | 54.5 |
Mean resistance value | 41.0 | 42.7 | 60.1 | 50.8 | 43.8 | 45.4 |
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Facciolà, A.; Virga, A.; Gioffrè, M.E.; Laganà, P. Evaluation of Antibiotic Resistance in Bacterial Strains Isolated from Sewage of Slaughterhouses Located in Sicily (Italy). Int. J. Environ. Res. Public Health 2021, 18, 9611. https://0-doi-org.brum.beds.ac.uk/10.3390/ijerph18189611
Facciolà A, Virga A, Gioffrè ME, Laganà P. Evaluation of Antibiotic Resistance in Bacterial Strains Isolated from Sewage of Slaughterhouses Located in Sicily (Italy). International Journal of Environmental Research and Public Health. 2021; 18(18):9611. https://0-doi-org.brum.beds.ac.uk/10.3390/ijerph18189611
Chicago/Turabian StyleFacciolà, Alessio, Antonino Virga, Maria Eufemia Gioffrè, and Pasqualina Laganà. 2021. "Evaluation of Antibiotic Resistance in Bacterial Strains Isolated from Sewage of Slaughterhouses Located in Sicily (Italy)" International Journal of Environmental Research and Public Health 18, no. 18: 9611. https://0-doi-org.brum.beds.ac.uk/10.3390/ijerph18189611