Transmission and Long-Term Colonization Patterns of Staphylococcus aureus in a Nursing Home
Abstract
:1. Introduction
2. Materials and Methods
2.1. Study Design and Sample Collection
2.2. S. aureus Identification and Detection of Methicillin-resistance
2.3. Multi-Locus Variable Number of Tandem Repeats Fingerprinting (MLVF)
2.4. Statistical Analysis
2.5. Ethical Statement
3. Results
3.1. S. aureus Carriage among the Residents and Personnel of a Nursing Home
3.2. MRSA Colonization among the Residents and Personnel of a Nursing Home
3.3. Risk Factors for S. aureus Carriage among the Residents and Personnel of a Nursing Home
3.4. Risk Factors for MRSA Colonization
3.5. Genotyping of S. aureus by Multi-Locus Variable Number of Tandem Repeats Fingerprinting
4. Discussion
5. Conclusions
Supplementary Materials
Author Contributions
Funding
Conflicts of Interest
References
- Zhang, J.; Gu, F.F.; Zhao, S.Y.; Xiao, S.Z.; Wang, Y.C.; Guo, X.K.; Ni, Y.X.; Han, L.Z. Prevalence and molecular epidemiology of Staphylococcus aureus among residents of seven nursing homes in Shanghai. PLoS ONE 2015, 10, e0137593. [Google Scholar] [CrossRef]
- Kline, K.A.; Bowdish, D.M. Infection in an aging population. Curr. Opin. Microbiol. 2016, 29, 63–67. [Google Scholar] [CrossRef] [PubMed]
- Harrison, E.M.; Ludden, C.; Brodrick, H.J.; Blane, B.; Brennan, G.; Morris, D.; Coll, F.; Reuter, S.; Brown, N.M.; Holmes, M.A.; et al. Transmission of methicillin-resistant Staphylococcus aureus in long-term care facilities and their related healthcare networks. Genome Med. 2016, 8. [Google Scholar] [CrossRef] [Green Version]
- Pathare, N.A.; Asogan, H.; Tejani, S.; Al Mahruqi, G.; Al Fakhri, S.; Zafarulla, R.; Pathare, A.V. Prevalence of methicillin resistant Staphylococcus aureus [MRSA] colonization or carriage among health-care workers. J. Infect. Public Health 2016, 9, 571–576. [Google Scholar] [CrossRef] [Green Version]
- Roghmann, M.C.; Johnson, J.K.; Sorkin, J.D.; Langenberg, P.; Lydecker, A.; Sorace, B.; Levy, L.; Mody, L. Transmission of methicillin-resistant Staphylococcus aureus (MRSA) to healthcare worker gowns and gloves during care of nursing home residents. Infect. Control Hosp. Epidemiol. 2015, 36, 1050–1057. [Google Scholar] [CrossRef] [Green Version]
- Senn, L.; Clerc, O.; Zanetti, G.; Basset, P.; Prod’hom, G.; Gordon, N.C.; Sheppard, A.E.; Crook, D.W.; James, R.; Thorpe, H.A.; et al. The stealthy superbug: The role of asymptomatic enteric carriage in maintaining a long-term hospital outbreak of ST228 methicillin-resistant Staphylococcus aureus. mBio 2016, 7, e02039-15. [Google Scholar] [CrossRef] [Green Version]
- Votintseva, A.A.; Miller, R.R.; Fung, R.; Knox, K.; Godwin, H.; Peto, T.E.; Crook, D.W.; Bowden, R.; Walker, A.S. Multiple-strain colonization in nasal carriers of Staphylococcus aureus. J. Clin. Microbiol. 2014, 52, 1192–1200. [Google Scholar] [CrossRef] [Green Version]
- Mody, L.; Flannery, E.; Bielaczyc, A.; Bradley, S.F. Molecular Epidemiology of Staphylococcus aureus Colonization in 2 Long-Term Care Facilities. Infect. Control Hosp. Epidemiol. 2006, 27, 212–214. [Google Scholar] [CrossRef]
- Livermore, D.M.; Pearson, A. Antibiotic resistance: Location, location, location. Clin. Microbiol. Infect. 2007, 13, 7–16. [Google Scholar] [CrossRef] [Green Version]
- Sabat, A.; Krzyszton-Russjan, J.; Strzalka, W.; Filipek, R.; Kosowska, K.; Hryniewicz, W.; Travis, J.; Potempa, J. New method for typing Staphylococcus aureus strains: Multiple-Locus Variable-Number Tandem Repeat Analysis of polymorphism and genetic relationships of clinical isolates. J. Clin. Microbiol. 2003, 41, 1801–1804. [Google Scholar] [CrossRef] [Green Version]
- Grzegorczyk, A.; Malm, A. Genotyping of Staphylococcus aureus strains isolated from healthy persistent carriers. Folia Microbiol. 2014, 59, 349–353. [Google Scholar] [CrossRef]
- Jakobsson, H.E.; Jernberg, C.; Andersson, A.F.; Sjölund-Karlsson, M.; Jansson, J.K.; Engstrand, L. Short-term antibiotic treatment has differing long-term impacts on the human throat and gut microbiome. PLoS ONE 2010, 5, e9836. [Google Scholar] [CrossRef] [Green Version]
- Keeney, K.M.; Yurist-Doutsch, S.; Arrieta, M.-C.; Finlay, B.B. Effects of antibiotics on human microbiota and subsequent disease. Annu. Rev. Microbiol. 2014, 68, 217–235. [Google Scholar] [CrossRef]
- Rondeau, C.; Chevet, G.; Blanc, D.S.; Gbaguidi-Haore, H.; Decalonne, M.; Dos Santos, S.; Quentin, R.; van der Mee-Marquet, N. Current molecular epidemiology of methicillin-resistant Staphylococcus aureus in elderly French people: Troublesome clones on the horizon. Front. Microbiol. 2016, 7, 31. [Google Scholar] [CrossRef] [PubMed]
- Aslam, B.; Wang, W.; Arshad, M.I.; Khurshid, M.; Muzammil, S.; Rasool, M.H.; Nisar, M.A.; Alvi, R.F.; Aslam, M.A.; Qamar, M.U.; et al. Antibiotic resistance: A rundown of a global crisis. Infect. Drug Resist. 2018, 11, 1645–1658. [Google Scholar] [CrossRef] [Green Version]
- Rogers, G.B.; Shaw, D.; Marsh, R.L.; Carroll, M.P.; Serisier, D.J.; Bruce, K.D. Respiratory microbiota: Addressing clinical questions, informing clinical practice. Thorax 2015, 70, 74–81. [Google Scholar] [CrossRef] [Green Version]
- Kang, C.-I.; Song, J.-H.; Ko, K.S.; Chung, D.R.; Peck, K.R. Clinical features and outcome of Staphylococcus aureus infection in elderly versus younger adult patients. Int. J. Infect. Dis. 2011, 15, e58–e62. [Google Scholar] [CrossRef] [Green Version]
- Jwa, H.; Beom, J.W.; Lee, J.H. Predictive factors of methicillin-resistant Staphylococcus aureus infection in elderly patients with community-onset pneumonia. Tuberc. Respir. Dis. 2017, 80, 201. [Google Scholar] [CrossRef]
- Kanwar, A.; Cadnum, J.L.; Thakur, M.; Jencson, A.L.; Donskey, C.J. Contaminated clothing of methicillin-resistant Staphylococcus aureus (MRSA) carriers is a potential source of transmission. Am. J. Infect. Control 2018, 46, 1414–1416. [Google Scholar] [CrossRef]
- Sassmannshausen, R.; Deurenberg, R.H.; Köck, R.; Hendrix, R.; Jurke, A.; Rossen, J.W.; Friedrich, A.W. MRSA prevalence and associated risk factors among health-care workers in non-outbreak situations in the Dutch-German EUREGIO. Front. Microbiol. 2016, 7, 1273. [Google Scholar] [CrossRef] [Green Version]
- Peters, C.; Kleinmüller, O.; Nienhaus, A.; Schablon, A. Prevalence and risk factors of MRSA colonisations: A cross-sectional study among personnel in outpatient care settings in Hamburg, Germany. BMJ Open 2018, 8, e021204. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Lee, B.Y.; Bartsch, S.M.; Wong, K.F.; Singh, A.; Avery, T.R.; Kim, D.S.; Brown, S.T.; Murphy, C.R.; Yilmaz, S.L.; Potter, M.A.; et al. The importance of nursing homes in the spread of methicillin-resistant Staphylococcus aureus (MRSA) among hospitals. Med. Care 2013, 51, 205–215. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Jiménez-Truque, N.; Saye, E.J.; Soper, N.; Saville, B.R.; Thomsen, I.; Edwards, K.M.; Creech, C.B. Longitudinal assessment of colonization with Staphylococcus aureus in healthy collegiate athletes. J. Pediatr. Infect. Dis. Soc. 2016, 5, 105–113. [Google Scholar] [CrossRef] [Green Version]
- Horner, C.; Wilcox, M.; Barr, B.; Hall, D.; Hodgson, G.; Parnell, P.; Tompkins, D. The longitudinal prevalence of MRSA in care home residents and the effectiveness of improving infection prevention knowledge and practice on colonisation using a stepped wedge study design. BMJ Open 2012, 2, e000423. [Google Scholar] [CrossRef]
- Jans, B.; Schoevaerdts, D.; Huang, T.D.; Berhin, C.; Latour, K.; Bogaerts, P.; Nonhoff, C.; Denis, O.; Catry, B.; Glupczynski, Y. Epidemiology of multidrug-resistant microorganisms among nursing home residents in Belgium. PLoS ONE 2013, 8, e64908. [Google Scholar] [CrossRef] [Green Version]
- Peters, C.; Dulon, M.; Kleinmüller, O.; Nienhaus, A.; Schablon, A. MRSA prevalence and risk factors among health personnel and residents in nursing homes in Hamburg, Germany—A cross-sectional study. PLoS ONE 2017, 12, e0169425. [Google Scholar] [CrossRef]
- Knox, J.; Uhlemann, A.-C.; Miler, M.; Hafer, C.; Vasquez, G.; Vavagiakis, P.; Shi, Q.; Lowy, F.D. Environmental contamination as a risk factor for intra-household Staphylococcus aureus transmission. PLoS ONE 2012, 7, e49900. [Google Scholar] [CrossRef] [Green Version]
- Ye, Z.; Mukamel, D.B.; Huang, S.S.; Li, Y.; Temkin-Greener, H. Healthcare-associated pathogens and nursing home policies and practices: Results from a national survey. Infect. Control Hosp. Epidemiol. 2015, 36, 759–766. [Google Scholar] [CrossRef] [Green Version]
- Chamchod, F.; Ruan, S. Modeling the spread of methicillin-resistant Staphylococcus aureus in nursing homes for elderly. PLoS ONE 2012, 7, e29757. [Google Scholar] [CrossRef] [Green Version]
- Stark, L.; Olofsson, M.; Lofrgren, S.; Molstad, S.; Lindgren, P.-E.; Matussek, A. Prevalence and molecular epidemiology of Staphylococcus aureus in Swedish nursing homes—As revealed in the SHADES study. Epidemiol. Infect. 2014, 142, 1310–1316. [Google Scholar] [CrossRef] [Green Version]
- van Rijen, M.M.L.; Bosch, T.; Heck, M.E.O.C.; Kluytmans, J.A.J.W. Meticillin-resistant Staphylococcus aureus epidemiology and transmission in a Dutch hospital. J. Hosp. Infect. 2009, 72, 299–306. [Google Scholar] [CrossRef] [PubMed]
- van Belkum, A. Hidden Staphylococcus aureus carriage: Overrated or underappreciated? mBio 2016, 7, e00079-16. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Muenks, C.E.; Hogan, P.G.; Wang, J.W.; Eisenstein, K.A.; Burnham, C.A.D.; Fritz, S.A. Diversity of Staphylococcus aureus strains colonizing various niches of the human body. J. Infect. 2016, 72, 698–705. [Google Scholar] [CrossRef] [Green Version]
Variable | Total n = 92 | Residents n = 55 | Personnel n = 37 |
---|---|---|---|
Age (years), mean ± SD 1 | 65 ± 20.7 | 80 ± 9.8 | 42.7 ± 9.1 |
Female, n (%) | 69 (75) | 39 (70.9) | 30 (81.1) |
Male, n (%) | 23 (25) | 16 (29.1) | 7 (18.9) |
Smoking, n (%) | 13 (14.1) | 8 (14.5) | 5 (13.5) |
Recent antibiotic use, n (%) | |||
0 | 60 (65.2) | 36 (65.5) | 24 (64.9) |
1 | 22 (23.9) | 11 (20) | 11 (29.7) |
≥2 | 6 (6.5) | 8 (14.5) | 2 (5.4) |
Hospital in the past one year, n (%) | |||
0 | 75 (81.5) | 39 (70.9) | 36 (96.3) |
1 | 11 (12) | 10 (18.2) | 1 (2.7) |
≥2 | 6 (6.5) | 6 (10.9) | 0 |
Underlying diseases, n (%) | |||
Diabetes mellitus | 17 (18.5) | 14 (25.5) | 3 (8.1) |
Cancer | 4 (4.3) | 2 (3.6) | 2 (5.4) |
Renal disease | 7 (7.6) | 7 (12.7) | 0 |
Neurological disorders | 19 (20.7) | 19 (34.5) | 0 |
Gastrointestinal disease | 19 (20.7) | 17 (30.9) | 2 (5.4) |
Respiratory tract disorders | 10 (10.9) | 9 (16.4) | 1 (2.7) |
Cardiovascular disease | 53 (57.6) | 47 (85.5) | 6 (16.2) |
Immunosuppressive drugs | 7 (7.6) | 7 (12.7) | 0 |
Variable | Univariate Analysis | |||||
---|---|---|---|---|---|---|
Carriers (Persistent and Intermittent) (n = 38) | Noncarriers (n = 17) | p Value | Persistent Carriers (n = 19) | Intermittent Carriers (n = 19) | p Value | |
Age (years), mean ± SD | 80.3 ± 10.2 | 79.0 ± 9.3 | ||||
<85 | 22 (57.9) | 11 (64.7) | 0.77 | 7 (36.8) | 15 (78.9) | 0.02 |
> 85 | 16 (42.1) | 6 (35.3) | 12 (63.2) | 4 (21.1) | ||
Female, n (%) | 27 (71.1) | 12 (70.6) | 1.0 | 14 (73.7) | 13 (68.4) | 1.0 |
Male, n (%) | 11 (28.9) | 5 (29.4) | 5 (26.3) | 6 (31.6) | ||
Smoking, n (%) | 5 (13.2) | 3 (17.7) | 0.69 | 1 (5.3) | 7 (21.1) | 0.34 |
Recent antibiotic use, n (%) | ||||||
0 | 24 (63.2) | 12 (70.6) | 0.28 | 12 (63.2) | 12 (63.2) | 0.83 |
1 | 9 (23.7) | 2 (11.8) | 5 (26.3) | 4 (21.1) | ||
≥2 | 5 (13.2) | 3 (17.7) | 2 (10.5) | 3 (15.8) | ||
Hospitalization in past one year, n (%) | ||||||
0 | 27 (71.1) | 12 (70.6) | 0.22 | 14 (73.7) | 13 (68.4) | 0.39 |
1 | 5 (13.2) | 5 (29.4) | 3 (15.8) | 2 (10.5) | ||
≥2 | 6 (15.8) | 0 (0) | 2 (10.5) | 4 (21.1) | ||
Underlying diseases, n (%) | ||||||
Diabetes mellitus | 8 (21.1) | 6 (35.3) | 0.32 | 2 (10.5) | 6 (31.6) | 0.23 |
Cancer | 1 (2.6) | 1 (5.9) | 0.53 | 0 (0) | 1 (5.3) | 1.0 |
Renal disease | 4 (10.5) | 3 (17.7) | 0.66 | 3 (15.8) | 1 (5.3) | 0.60 |
Neurological disorders | 12 (31.6) | 7 (41.2) | 0.55 | 5 (26.3) | 7 (36.8) | 0.73 |
Gastrointestinal disease | 9 (23.7) | 8 (47.1) | 0.12 | 5 (26.3) | 4 (21.1) | 1.0 |
Respiratory tract disorders | 6 (15.8) | 3 (17.7) | 1.0 | 2 (10.5) | 4 (21.1) | 0.66 |
Cardiovascular disease | 33 (86.8) | 14 (82.4) | 0.69 | 16 (84.2) | 17 (89.5) | 1.0 |
Immunosuppressive drugs | 3 (7.9) | 3 (17.7) | 0.36 | 3 (15.8) | 0 (0) | 0.23 |
Variable | Univariate Analysis | |||||
---|---|---|---|---|---|---|
Carriers (Persistent and Intermittent) (n = 31) | Noncarriers (n = 6) | p Value | Persistent Carriers (n = 15) | Intermittent Carriers (n = 16) | p Value | |
Age (years), mean ± SD | 42.6 ± 9.5 | 43.0 ± 7.7 | 0.93 | 43.3 ± 10.9 | 42.0 ± 8.2 | 0.70 |
Female, n (%) | 24 (77.4) | 6 (100) | 0.57 | 10 (66.7) | 14 (87.5) | 0.22 |
Male, n (%) | 7 (22.6) | 0 (0) | 5 (33.3) | 2 (12.5) | ||
Smoking, n (%) | 4 (12.9) | 1 (16.7) | 1.0 | 3 (20.0) | 1 (6.3) | 0.33 |
Close contact with residents, n (%) | 22 (71.0) | 4 (66.7) | 1.0 | 11 (73.3) | 11 (68.8) | 1.0 |
Duration of work (months), mean (range) | 84 (12–480) | 60 (24–420 | 0.77 | 60 (24–252) | 78 (12––480) | 0.72 |
Recent antibiotic use, n (%) | ||||||
0 | 19 (61.3) | 5 (83.3) | 0.46 | 7 (46.7) | 12 (75.0) | 0.019 |
1 | 10 (32.3) | 1 (16.7) | 8 (53.3) | 2 (12.5) | ||
≥2 | 2 (6.4) | 0 (0) | 0 (0) | 2 (12.5) | ||
Hospitalization in past one year, n (%) | ||||||
0 | 30 (96.8) | 6 (100) | 1.0 | 14 (93.3) | 16 (100) | 0.48 |
1 | 1 (3.2) | 0 (0) | 1 (6.7) | 0 (0) | ||
Underlying diseases, n (%) | ||||||
Diabetes mellitus | 3 (9.7) | 0 (0) | 1.0 | 0 (0) | 3 (18.8) | 0.22 |
Cancer | 2 (6.5) | 0 (0) | 1.0 | 1 (6.7) | 1 (6.3) | 1.0 |
Gastrointestinal disease | 2 (6.5) | 0 (0) | 1.0 | 1 (6.7) | 1 (6.3) | 1.0 |
Respiratory tract disorders | 1 (3.2) | 0 (0) | 1.0 | 0 (0) | 1 (6.3) | 1.0 |
Cardiovascular disease | 6 (19.4) | 0 (0) | 0.56 | 3 (20.0) | 3 (18.8) | 1.0 |
Variable | Univariate Analysis | |||
---|---|---|---|---|
Total (n = 92) | MRSA Carriers (n = 10) | Others/Noncarriers (n = 82) | p Value | |
Age (years), median (range) | 81 (56–97) | 45 (28–97) | 70 (26–94) | 0.17 |
Female, n (%) | 69 (75.0) | 10 (100) | 59 (72.0) | 0.061 |
Male, n (%) | 23 (25.0) | 0 (0) | 23 (28.0) | |
Smoking, n (%) | 13 (14.1) | 1 (10.0) | 12 (14.6) | 1.0 |
Nursing home residents, n (%) | 55 (59.8) | 3 (30.0) | 52 (63.4) | 0.083 |
Persistent carriage, n (%) | 34 (37.0) | 3 (30.0) | 31 (37.8) | 0.74 |
Recent antibiotic use, n (%) | ||||
0 | 60 (65.2) | 6 (60.0) | 54 (65.9) | 0.60 |
1 | 22 (23.9) | 2 (20.0) | 20 (24.4) | |
≥2 | 9 (9.8) | 2 (20.0) | 7 (8.5) | |
Hospitalization in past one year, n (%) | ||||
0 | 75 (81.5) | 10 (100) | 65 (79.3) | 0.23 |
1 | 11 (12.0) | 0 (0) | 11 (13.4) | |
≥2 | 6 (6.5) | 0 (0) | 6 (7.3) | |
Underlying diseases, n (%) | ||||
Diabetes mellitus | 17 (18.5) | 3 (30.0) | 14 (17.1) | 0.39 |
Cancer | 4 (4.4) | 0 (0) | 4 (4.9) | 1.0 |
Renal disease | 7 (7.6) | 1 (10.0) | 6 (7.3) | 0.57 |
Neurological disorders | 19 (20.7) | 1 (10.0) | 18 (22.0) | 0.68 |
Gastrointestinal disease | 19 (20.7) | 3 (30.0) | 16 (19.5) | 0.43 |
Respiratory tract disorders | 10 (10.9) | 2 (20.0) | 8 (9.8) | 0.30 |
Cardiovascular disease | 53 (57.6) | 5 (50.0) | 48 (58.5) | 0.74 |
Immunosuppressive drugs | 6 (6.5) | 1 (10.0) | 5 (6.1) | 0.51 |
Variable | Univariate Analysis | |||
---|---|---|---|---|
Total n = 69 | MRSA Carriers n = 10 | Non-MRSA Carriers n = 59 | p Value | |
Age (years), median (range) | 65 (26–97) | 45 (28–97) | 68 (26–97) | 0.25 |
Female, n (%) | 51 (73.9) | 10 (100) | 41 (69.5) | 0.053 |
Male, n (%) | 18 (26.1) | 0 (0) | 18 (30.5) | |
Smoking, n (%) | 9 (13.0) | 1 (10.0) | 8 (13.6) | 1.0 |
Nursing home residents, n (%) | 38 (55.1) | 3 (30.0) | 35 (59.3) | 0.10 |
Persistent carriage, n (%) | 34 (49.3) | 3 (30.0) | 31 (52.5) | 0.31 |
Recent antibiotic use, n (%) | ||||
0 | 43 (62.3) | 6 (60.0) | 37 (62.7) | 0.30 |
1 | 19 (27.5) | 2 (20.0) | 17 (28.8) | |
≥2 | 4 (5.8) | 2 (20.0) | 4 (6.8) | |
Hospitalization in past one year, n (%) | ||||
0 | 57 (82.6) | 10 (100) | 47 (79.7) | 0.24 |
1 | 6 (8.7) | 0 (0) | 6 (10.2) | |
≥2 | 6 (8.7) | 0 (0) | 6 (10.2) | |
Underlying diseases, n (%) | ||||
Diabetes mellitus | 11 (15.9) | 3 (30.0) | 8 (13.6) | 0.19 |
Cancer | 3 (4.4) | 0 (0) | 3 (5.1) | 1.0 |
Renal disease | 4 (5.8) | 1 (10.0) | 3 (5.1) | 0.47 |
Neurological disorders | 12 (17.4) | 1 (10.0) | 11 (18.6) | 0.68 |
Gastrointestinal disease | 11 (15.9) | 3 (30.0) | 8 (13.6) | 0.19 |
Respiratory tract disorders | 7 (10.1) | 2 (20.0) | 5 (8.5) | 0.27 |
Cardiovascular disease | 39 (56.5) | 5 (50.0) | 34 (57.6) | 0.74 |
Immunosuppressive drugs | 3 (4.4) | 1 (10.0) | 0 (0) | 0.38 |
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Kasela, M.; Grzegorczyk, A.; Korona-Głowniak, I.; Ossowski, M.; Nowakowicz-Dębek, B.; Malm, A. Transmission and Long-Term Colonization Patterns of Staphylococcus aureus in a Nursing Home. Int. J. Environ. Res. Public Health 2020, 17, 8073. https://doi.org/10.3390/ijerph17218073
Kasela M, Grzegorczyk A, Korona-Głowniak I, Ossowski M, Nowakowicz-Dębek B, Malm A. Transmission and Long-Term Colonization Patterns of Staphylococcus aureus in a Nursing Home. International Journal of Environmental Research and Public Health. 2020; 17(21):8073. https://doi.org/10.3390/ijerph17218073
Chicago/Turabian StyleKasela, Martyna, Agnieszka Grzegorczyk, Izabela Korona-Głowniak, Mateusz Ossowski, Bożena Nowakowicz-Dębek, and Anna Malm. 2020. "Transmission and Long-Term Colonization Patterns of Staphylococcus aureus in a Nursing Home" International Journal of Environmental Research and Public Health 17, no. 21: 8073. https://doi.org/10.3390/ijerph17218073
APA StyleKasela, M., Grzegorczyk, A., Korona-Głowniak, I., Ossowski, M., Nowakowicz-Dębek, B., & Malm, A. (2020). Transmission and Long-Term Colonization Patterns of Staphylococcus aureus in a Nursing Home. International Journal of Environmental Research and Public Health, 17(21), 8073. https://doi.org/10.3390/ijerph17218073