Prevalence and risk factors for multidrug-resistant organisms colonization in long-term care facilities around the world: a review

antibiotics Review Prevalence and Risk Factors for Multidrug-Resistant Organisms Colonization in Long-Term Care Facilities Around the World: A Review Ángel Rodríguez-Villodres 1,† , Cecilia Martín-Gandul 1,† , Germán Peñalva 1, Ana Belén Guisado-Gil 1,2 , Juan Carlos Crespo-Rivas 1, María Eugenia Pachón-Ibáñez 1, JoséAntonio Lepe 1and JoséMiguel Cisneros 1,*   Citation: Rodríguez-Villodres, Á.; Martín-Gandul, C.; Peñalva, G.; Guisado-Gil, A.B.; Crespo-Rivas, J.C.; Pachón-Ibáñez, M.E.; Lepe, J.A.; Cisneros, J.M. Prevalence and Risk Factors for Multidrug-Resistant Organisms Colonization in Long-Term Care Facilities Around the World: A Review. Antibiotics 2021,10, 680. https://doi.org/10.3390/ antibiotics10060680 Academic Editor: Mamoon Aldeyab Received: 26 April 2021 Accepted: 2 June 2021 Published: 7 June 2021 Publisher’s Note: MDPI stays neutral with regard to jurisdictional claims in published maps and institutional affiliations. Copyright: © 2021 by the authors. Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (https:// creativecommons.org/licenses/by/ 4.0/). 1Clinical Unit of Infectious Diseases, Microbiology and Preventive Medicine, Institute of Biomedicine of Seville (IBiS), University of Seville/CSIC/University Hospital Virgen del Rocío, 41013 Seville, Spain; [email protected] (Á.R.-V.); [email protected] (C.M.-G.); [email protected] (G.P.); [email protected] (A.B.G.-G.); [email protected] (J.C.C.-R.); [email protected] (M.E.P.-I.); [email protected] (J.A.L.) 2Department of Pharmacy, University Hospital Virgen del Rocío, 41013 Seville, Spain *Correspondence: jmcisner[email protected]; Tel.: +34-697-958-658 † Both authors contributed equally to this work. Abstract: Elderly people confined to chronic care facilities face an increased risk of acquiring infections by multidrug-resistant organisms (MDROs). This review presents the current knowledge of the prevalence and risk factors for colonization by MDROs in long-term care facilities (LTCF), thereby providing a useful reference to establish objectives for implementing successful antimicrobial stewardship programs (ASPs). We searched in PubMed and Scopus for studies examining the prevalence of MDROs and/or risk factors for the acquisition of MDROs in LTCF. One hundred and thirty-four studies published from 1987 to 2020 were included. The prevalence of MDROs in LTCF varies between the different continents, where Asia reported the highest prevalence of extended-spectrum ß-lactamase (ESBL) Enterobacterales (71.6%), carbapenem resistant (CR) Enterobacterales (6.9%) and methicillin-resistant Staphylococcus aureus (MRSA) (25.6%) and North America the highest prevalence to MDR Pseudomonas aeruginosa (5.4%), MDR Acinetobacter baumannii (15.0%), vancomycin-resistant Enterococcus spp. (VRE) (4.0%), and Clostridioides difficile (26.1%). Furthermore, MDRO prevalence has experienced changes over time, with increases in MDR P. aeruginosa and extended spectrum ß-lactamase producing Enterobacterales observed starting in 2015 and decreases of CR Enterobacterales, MDR A. baumannii, VRE, MRSA and C. difficile. Several risk factors have been found, such as male sex, chronic wounds, the use of medical devices, and previous antibiotic use. The last of these aspects represents one of the most important modifiable factors for reducing colonization with MDROs through implementing ASPs in LTCF. Keywords: multidrug-resistant organism; long term care facilities; nursing homes; prevalence; risk factors; antimicrobial stewardship 1. Introduction Older adults confined to chronic care facilities are known to have an increased risk of acquiring infections, most commonly those of the skin, soft tissues, respiratory and urinary tracts, as well as gastroenteritis [ 1 ]. The recent COVID-19 outbreak has underlined the vulnerability of this group around the world [ 2 ], and the condition of frailty is gaining international attention. According to the Organization for Economic Co-operation and Development (OECD), it is expected that the population aged from 65 to 79 years will rise from about 10% in 2010 to about 15% in 2050 (https://www.oecd.org/els/healthsystems/47884543.pdf; accessed on 14 December 2020). Thus, current trends in the world’s demographic structure indicate increasing requirements in long-term care settings. Antibiotics 2021,10, 680. https://doi.org/10.3390/antibiotics10060680 https://www.mdpi.com/journal/antibiotics Antibiotics 2021,10, 680 2 of 22 The emergence of multidrug-resistant organisms (MDROs) is a major public health concern [ 3 ]. Bacteria such as extended-spectrum ß-lactamase (ESBL) Escherichia coli, ESBL Klebsiella pneumoniae, carbapenem-resistant (CR) Enterobacterales, methicillin-resistant Staphylococcus aureus (MRSA), vancomycin-resistant Enterococcus spp. (VRE), and multidrugresistant (MDR) non-fermenting species such as Pseudomonas aeruginosa and Acinetobacter baumannii are increasing in prevalence [ 4 – 7 ]. Although it is not an MDRO, Clostridioides difficile represents a worldwide public health concern, as it is one of the major causes of antibiotic-associated infections in healthcare settings, especially among older people living in nursing homes (NH) [8,9]. Polypharmacy and inappropriate prescriptions are well-known risk factors for adverse drug reactions, which commonly cause poor clinical outcomes in older people. Antimicrobial resistance is a major negative event resulting from inappropriate prescriptions of antimicrobials [10]. Antimicrobial stewardship programs (ASPs) have been widely implemented in hospitals, with considerable evidence of their impacts on prescription rates and some evidence that they reduce antibiotic-resistant infections [ 11 ]. Elderly care facilities and NH could also benefit from these programs. Knowledge of the epidemiology of MDROs at a local and global level is key to implementing successful antimicrobial stewardship intervention. The purpose of this narrative review is to present current knowledge on the prevalence and risk factors for colonization by MDROs in long-term care facilities (LTCF), along with epidemiological data to facilitate the establishment of objectives for implementing successful ASPs in this setting. 2. Results and Discussion 2.1. Studies Included Initially, 182 references were selected. Among these references, 48 were excluded as follows: (i) studies that did not include MDROs, NH, or LTCF (n= 18); (ii) studies reporting infections by MDROs instead of colonization (n= 17); (iii) limited information about the prevalence of or risk factors for colonization by MDROs (n= 9); and (iv) study population duplicated in included studies (n= 4). Ultimately, 134 references were included ( Figure 1 ). Studies included in this review were published from 1987 to 2020). The most frequent MDRO analyzed was MRSA (n= 88, 65.6%) [ 1 , 12 – 98 ] followed by ESBL Enterobacterales ( n= 51 , 38.0%) [ 1 , 14 , 16 , 18 – 23 , 25 , 31 , 33 , 34 , 39 , 57 , 62 , 73 , 75 , 76 , 82 , 83 , 85 , 89 , 97 , 99 – 125 ] (E. coli and K. pneumoniae), VRE (n= 36, 26.8%) [ 1 , 13 , 14 , 18 , 20 – 23 , 25 , 28 , 31 , 33 , 34 , 37 – 39 , 57 – 60 , 64 – 66 , 73 , 74 , 76 , 82 , 83 , 89 , 97 , 106 , 109 , 126 – 129 ], CR Enterobacterales (n= 27, 20.1%) [ 1 , 13 , 18 – 22 , 34 , 60 , 67 , 73 , 82 , 83 , 97 , 100 , 103 , 104 , 108 – 110 , 113 , 118 , 130 – 134 ], C. difficile (n= 11, 8.2%) [ 19 , 37 , 106 , 109 , 131 , 135 – 140 ], MDR A. baumannii (n= 11, 8.2%) [ 13 , 20 , 28 , 37 , 60 , 64 , 67 , 74 , 82 , 85 , 141 ], and MDR P. aeruginosa (n= 8, 5.9%) [ 13 , 20 , 34 , 37 , 64 , 67 , 85 , 142 ]. The types of studies were as follows: 99 (73.8%) cross-sectional studies [ 1 , 15 – 17 , 19 , 26 , 28 – 32 , 34 , 35 , 37 , 39 , 40 , 42 – 44 , 46 , 47 , 50 , 52 , 54 , 55 , 57 , 59 – 62 , 65 , 68 – 73 , 75 , 77 – 85 , 87 – 89 , 91 – 93 , 96 – 109 , 111 , 113 , 116 – 126 , 128 , 129 , 131 – 135 , 137 , 138 , 140 , 141 , 143 ], 28 (20.9%) observational prospective studies [ 12 – 14 , 18 , 27 , 33 , 36 , 38 , 41 , 45 , 48 , 51 , 53 , 56 , 58 , 66 , 67 , 76 , 90 , 94 , 95 , 110 , 112 , 115 , 127 , 136 , 139 , 144 ], 3 (2.2%) observational retrospective studies [ 63 , 64 , 114 ], and 4 (2.9%) case-control studies [ 74 , 86 , 130 , 142 ]. The MDRO samples were isolated from various sources: nasal (n= 79, 58.9%) [ 12 , 14 – 16 , 18 , 34 , 36 , 38 , 40 – 43 , 45 – 75 , 77 – 88 , 90 – 97 , 99 ], perianal (n= 79, 58.9%) [ 12 , 14 , 17 – 23 , 25 , 28 , 29 , 31 – 34 , 38 , 41 , 46 , 47 , 51 , 56 – 60 , 64 – 67 , 73 – 76 , 78 , 82 , 83 , 85 , 93 , 94 , 99 , 100 , 102 – 106 , 108 – 113 , 115 – 122 , 124 , 126 – 140 , 142 , 144 ], skin (n = 33, 24.6%) [ 12 , 20 – 24 , 28 , 29 , 32 , 33 , 39 , 41 , 43 , 50 , 54 , 60 , 64 – 66 , 69 , 71 – 74 , 79 , 86 , 87 , 92 , 97 , 99 , 105 , 127 , 139 ], oropharynx (n= 24, 17.9%) [ 15 , 20 , 21 , 24 , 25 , 29 – 33 , 41 , 47 , 57 , 62 , 64 – 66 , 74 , 83 – 85 , 93 , 113 , 125 ], ulcers (n= 28, 20.9%) [ 12 , 14 , 23 , 29 – 33 , 36 , 41 , 43 , 47 , 51 , 56 , 57 , 63 – 66 , 71 , 74 , 78 , 80 , 81 , 83 , 93 , 102 ], urine (n= 15, 11.2%) [ 12 , 14 , 16 , 20 – 22 , 32 , 43 , 80 , 101 , 102 , 104 , 114 , 123 , 124 ], devices (n= 14, 10.4%) [12,18,23,29,30,33,41,64–66,68,80,93,102], and sputum (n= 3, 2.2%) [43,78,141]. The studies were conducted in several continents, mainly Europe (n= 70, 52.2%) [ 1 , 13 , 15 – 22 , 25 , 30 – 32 , 34 , 36 , 37 , 39 , 40 , 46 – 50 , 52 , 53 , 55 , 57 , 62 , 63 , 68 , 70 – 72 , 75 – 77 , 79 , 80 , 83 – 86 , 88 , 91 – 93 , 98 , 99 , 101 , 103 – 105 , 107 – 110 , 114 – 121 , 123 , 124 , 136 , 140 ], North America (n= 41, 30.6%) [ 12 , 14 , 23 , 24 , 27 , Antibiotics 2021,10, 680 3 of 22 29 , 33 , 38 , 41 – 45 , 51 , 58 , 59 , 64 – 66 , 73 , 74 , 78 , 89 , 90 , 94 , 97 , 102 , 109 , 122 , 127 , 129 – 131 , 133 , 134 , 137 – 139 , 141 – 144 ], and Asia (n= 15, 11.2%) [ 26 , 28 , 35 , 54 , 60 , 67 , 69 , 87 , 95 , 96 , 100 , 111 , 112 , 126 , 132 ]. Seven studies reported data from Oceania (5.2%) [ 56 , 81 , 82 , 106 , 113 , 125 , 128 ] and only one from South America (0.7%) [61]. None of the studies were performed in Africa. Antibiotics 2021, 10, x FOR PEER REVIEW 3 of 23 (n = 24, 17.9%) [15,20,21,24,25,29–33,41,47,57,62,64–66,74,83–85,93,113,125], ulcers (n = 28, 20.9%) [12,14,23,29–33,36,41,43,47,51,56,57,63–66,71,74,78,80,81,83,93,102], urine (n = 15, 11.2%) [12,14,16,20–22,32,43,80,101,102,104,114,123,124], devices (n = 14, 10.4%) [12,18,23,29,30,33,41,64–66,68,80,93,102], and sputum (n = 3, 2.2%) [43,78,141]. The studies were conducted in several continents, mainly Europe (n = 70, 52.2%) [1,13,15–22,25,30–32,34,36,37,39,40,46–50,52,53,55,57,62,63,68,70–72,75–77,79,80,83– 86,88,91–93,98,99,101,103–105,107–110,114–121,123,124,136,140], North America (n = 41, 30.6%) [12,14,23,24,27,29,33,38,41–45,51,58,59,64– 66,73,74,78,89,90,94,97,102,109,122,127,129–131,133,134,137–139,141–144], and Asia (n = 15, 11.2%) [26,28,35,54,60,67,69,87,95,96,100,111,112,126,132]. Seven studies reported data from Oceania (5.2%) [56,81,82,106,113,125,128] and only one from South America (0.7%) [61]. None of the studies were performed in Africa. Figure 1. Flowchart search strategy. IQR, interquartile range. 2.2. MDRO Prevalence The overall prevalence of colonization with MDROs around the world varies between the different pathogens studied. For ESBL Enterobacterales, the median prevalence reported was 11.6%, which increased to 15.0% in the case of ESBL E.coli and decreased to 2.9% for ESBL K. pneumoniae. The overall prevalence of CR Enterobacterales was 0.8%. Among other MDR Gram-negative bacteria, such as P. aeruginosa and A. baumannii, the prevalences reported globally were 1.3% and 5.8%, respectively. In the case of Gram-pos- itive bacteria, MRSA showed the highest prevalence at 13.2%, followed by C. difficile 5.1% and VRE 1.5% (Table 1). This prevalence appears to vary between continents. Asia reported the highest prevalence of ESBL Enterobacterales [100,111,112], CR Enterobacterales [60,67,100,132] and MRSA [26,28,35,54,60,67,69,87,95,96]. In contrast, the lowest prevalence of ESBL Enterobacterales, CR Enterobacterales and MRSA have been reported in Oceania [82,106,113,125], Europe [1,13,18–22,34,83,103,104,108–110,118] and South America [61]. With respect to MDR P. aeruginosa [64,142], A. baumannii [64,74,141], VRE [14,23,33,38,58,59,64– 66,73,74,89,97,127,129] and C. difficile [131,137–139], North America reported the highest Figure 1. Flowchart search strategy. IQR, interquartile range. 2.2. MDRO Prevalence The overall prevalence of colonization with MDROs around the world varies between the different pathogens studied. For ESBL Enterobacterales, the median prevalence reported was 11.6%, which increased to 15.0% in the case of ESBL E. coli and decreased to 2.9% for ESBL K. pneumoniae. The overall prevalence of CR Enterobacterales was 0.8%. Among other MDR Gram-negative bacteria, such as P. aeruginosa and A. baumannii, the prevalences reported globally were 1.3% and 5.8%, respectively. In the case of Gram-positive bacteria, MRSA showed the highest prevalence at 13.2%, followed by C. difficile 5.1% and VRE 1.5% (Table 1). This prevalence appears to vary between continents. Asia reported the highest prevalence of ESBL Enterobacterales [ 100 , 111 , 112 ], CR Enterobacterales [ 60 , 67 , 100 , 132 ] and MRSA [ 26 , 28 , 35 , 54 , 60 , 67 , 69 , 87 , 95 , 96 ]. In contrast, the lowest prevalence of ESBL Enterobacterales, CR Enterobacterales and MRSA have been reported in Oceania [ 82 , 106 , 113 , 125 ], Europe [ 1 , 13 , 18 – 22 , 34 , 83 , 103 , 104 , 108 – 110 , 118 ] and South America [ 61 ]. With respect to MDR P. aeruginosa [ 64 , 142 ], A. baumannii [ 64 , 74 , 141 ], VRE [ 14 , 23 , 33 , 38 , 58 , 59 , 64 – 66 , 73 , 74 , 89 , 97 , 127 , 129 ] and C. difficile [ 131 , 137 – 139 ], North America reported the highest prevalence. However, remarkably, Asia has the lowest prevalence of VRE [ 28 , 60 , 126 ] (Table 1, Figure 2 ). Antibiotics 2021,10, 680 4 of 22 Table 1. Prevalence of multidrug-resistant organisms in long term care facilities. Multidrug-Resistant Organism No. of Articles n= 134 Percentage of Articles n= 134 (%) Microorganism Global Prevalence n= 134 (Median, IQR) Prevalence in Europe n= 70 (Median %, IQR) Prevalence in North America n= 41 (Median %, IQR) Prevalence in South America n= 1 (Median %, IQR) Prevalence in Asia n= 15 (median %, IQR) Prevalence in Oceania n= 7 (Median %, IQR) Prevalence in Africa n= 0 (Median %, IQR) ESBL Enterobacterales 51 38.0 11.6 (5.5–24.5) 12.9 (6.3–21.4) 9 (3.4–33) - 71.6 (46.6–74) 6.0 (1.4–10.8) - ESBL Escherichia coli 33 24.6 15.0 (7.7–41.4) 15.3 (7.8–41.2) 15 (2.9–30.3) - 82.7 (50.4–86.1) 10.4 (5.6–11.2) - ESBL Klebsiella pneumoniae 22 16.4 2.9 (0.4–7.1) 4.2 (0.6–6.5) 0.2 (0.0–4.8) - 9.1 (8.8–9.4) 1.7 - Carbapenem resistant Enterobacterales 27 20.1 0.8 (0.0–4.2) 0.2 (0.0–0.9) 5.0 (2.0–7.9) - 6.9 (1.4–14.6) 0.4 (0.3–0.5) - MDR Pseudomonas aeruginosa 8 5.9 1.3 (0.2–5.3) 0.2 (0.08–1.6) 5.4 (3.2–7.6) - 3.9 - - MDR Acinetobacter baumannii 11 8.2 5.8 (2.2–13.5) 1.9 (0–4.3) 15.0 (13.5–16.0) - 5.2 (2.9–12.3) 6.0 - Meticillin-resistant Staphylococcus aureus 88 65.6 13.2 (6.6–25) 9.1 (4.4–19.6) 22.0 (12.0–30.0) 3.7 25.6 (13–36.8) 10 (6.5–13) - Vancomycin-resistant Enterococcus spp. 36 26.8 1.5 (0.06–6.9) 0.4 (0.0–1.8) 4.0 (0.9–20.7) - 0.0 (0.0–4.8) 3.1 (2.5–4.5) - Clostridioides difficile 11 8.2 5.1 (1.9–24.8) 3.7 (1.1–4.9) 26.1 (16.2–37.5) - - 1.0 - ESBL, extended-spectrum ß-lactamase; MDR, multidrug resistant; IQR, interquartile range. Antibiotics 2021,10, 680 5 of 22 Antibiotics 2021, 10, x FOR PEER REVIEW 6 of 23 Figure 2. Prevalence of different MDRO in LTCF around the world. Maps were created through the online tool Mapchart.net (https://mapchart.net/world.html, accessed on 23 November 2020). ESBL, extended-spectrum ß-lactamase; MDR, multidrug-resistant. 2.3. MDRO Co-Colonization Co-colonization with multiple MDROs seems variable among LTCF. For example, Jans et al. [31] reported a low rate of co-colonization (0.8%) with ESBL Enterobacterales and MRSA among 2791 residents from 60 LTCF. On the other hand, Ludden et al. [18] found that the prevalence of co-colonization with MRSA and ESBL Enterobacterales increased to 39%, although the authors only analyzed one LTCF with 64 residents. Heinze et al. [66] Figure 2. Prevalence of different MDRO in LTCF around the world. Maps were created through the online tool Mapchart.net (https://mapchart.net/world.html, accessed on 23 November 2020). ESBL, extended-spectrum ß-lactamase; MDR, multidrug-resistant. 2.3. MDRO Co-Colonization Co-colonization with multiple MDROs seems variable among LTCF. For example, Jans et al. [ 31 ] reported a low rate of co-colonization (0.8%) with ESBL Enterobacterales and MRSA among 2791 residents from 60 LTCF. On the other hand, Ludden et al. [ 18 ] found that the prevalence of co-colonization with MRSA and ESBL Enterobacterales increased to 39%, although the authors only analyzed one LTCF with 64 residents. Heinze et al. [ 66 ] reported that 13.2% of the residents were co-colonized with both MRSA and VRE. When MDROs were considered, the prevalence of co-colonization ranged from 5.5% to 21% for at Antibiotics 2021,10, 680 6 of 22 least two MDROs [ 57 , 85 , 142 ]. All of these studies suggest that LTCF may act as reservoirs for MDROs, through which transmission may occur via resident–resident interactions or resident–healthcare worker interactions. 2.4. Changes in MDRO Prevalence Over Time In the last decade, there has been a remarkable increase in the number of publications on MDR prevalence and LTCF. Figure 3shows a representation of the median prevalence of MDROs within 5-year periods from 1985 to 2020. In order to be able to observe if there have been changes in the prevalence of MDROs over time, we established a cut-off point in 2015 and compared two time periods (until 2015, including and after 2015). Thus, we had a balanced number of publications on both groups, for each MDRO ( Table 2 ). The ESBL Enterobacterales prevalence increased from 10.5% [ 14 , 18 , 22 , 23 , 25 , 31 , 33 , 39 , 57 , 75 , 76 , 82 , 85 , 89 , 99 , 101 , 102 , 104 , 106 , 107 , 111 , 112 , 116 , 119 , 121 – 125 , 143 ] to 15.1% [ 1 , 16 , 19 – 21 , 34 , 62 , 73 , 83 , 97 , 100 , 103 , 105 , 108 – 110 , 113 – 115 , 117 , 118 , 120 ], but this increase seems to be due to ESBL K. pneumoniae (0.7% vs. 4.2%) rather than ESBL E. coli (18.0% vs. 14.4%). In contrast, the prevalence of CR Enterobacterales decreased from 2015 onward (2.9% vs. 0.8%) [ 18 , 22 , 82 , 104 , 132 , 133 ] vs. [ 1 , 13 , 19 – 21 , 34 , 60 , 67 , 73 , 83 , 97 , 100 , 103 , 108 – 110 , 113 , 118 , 130 , 131 , 134 ], as did that of MDR A. baumannii, from 10.5% to 5.2% [ 74 , 82 , 85 , 141 ] vs. [ 13 , 20 , 28 , 37 , 60 , 64 , 67 ]; that of VRE, from 2.8% to 0.6% [ 14 , 18 , 22 , 23 , 25 , 31 , 33 , 38 , 39 , 57 – 59 , 65 , 74 , 76 , 82 , 89 , 106 , 126 – 129 ] vs. [ 1 , 13 , 20 , 21 , 28 , 34 , 37 , 60 , 64 , 66 , 73 , 83 , 97 , 109 ] ; that of MRSA, from 16.0% to 9.6% [ 14 , 17 , 18 , 22 , 23 , 25 – 27 , 29 – 33 , 35 , 36 , 38 – 48 , 50 , 54 , 56 – 59 , 63 , 65 , 68 , 69 , 71 , 72 , 75 – 81 , 84 – 86 , 89 – 91 , 93 – 96 , 98 ] vs. [ 1 , 13 , 15 , 16 , 19 – 21 , 24 , 28 , 34 , 37 , 49 , 55 , 60 – 62 , 64 , 66 , 67 , 70 , 73 , 83 , 87 , 88 , 92 , 97 ]; and that of C. difficile, from 7.1% to 3.9% [ 106 , 137 – 140 ] vs. [ 19 , 37 , 109 , 131 , 135 , 136 ]. Conversely, the prevalence of MDR P. aeruginosa experienced a slight increase in recent years (0.5% vs. 2.75%) [ 85 , 142 ] vs. [ 13 , 20 , 34 , 37 , 64 , 67 ] (Table 2). At a more individual level, Kohler et al. [ 13 ] analyzed changes in the prevalence of MDROs between 2007 and 2017 in NH from Switzerland. The authors reported an increase from 1.6% to 7.8% in ESBL K. pneumoniae and from 2% to 8% in MDR P. aeruginosa. Furthermore, a decrease from 34.3% to 25.9% was observed in MRSA prevalence. However, in contrast with the global data from this review, ESBL E. coli showed an increase from 5.4% in 2007 to 21.6% in 2017. Min et al. [ 33 ], in a one-year period of study, also reported an increase in the prevalence of ESBL-Enterobacterales from 36% to 39% and of VRE, from 10% to 13%. However, in contrast with the previous study, they observed an increase in the prevalence of MRSA, from 23% to 43%. Table 2. Changes in the prevalence of multidrug-resistant organisms, before and after 2015. Multidrug-Resistant Organism No. of Articles (2015 or Before) n= 90 No. of Articles (After 2015) n= 44 Prevalence of MDR (2015 or Before) Median (IQR) Prevalence of MDR (After 2015) Median (IQR) Difference (%) ESBL Enterobacterales 30 22 10.5 (3.5–31.4) 15.1 (9.1–19.9) 4.6 ESBL Escherichia coli 19 14 18.0 (5.5–40.9) 14.4 (8.1–41.4) −3.6 ESBL Klebsiella pneumoniae 10 12 0.7 (0.2–9.2) 4.2 (0.7–6.3) 3.5 Carbapenem resistant Enterobacterales 6 21 2.9 (0.1–7.5) 0.8 (0–1.9) −2.1 MDR Pseudomonas aeruginosa 2 6 0.5 (0.25–0.75) 2.75 (0.5–8.2) 2.25 MDR Acinetobacter baumannii 4 7 10.5 (5.4–15.5) 5.2 (0.3–8.9) −5.3 Meticillin-resistant Staphylococcus aureus 61 26 16.0 (7.8–23.3) 9.6 (3.9–25.5) −6.4 Vancomycin-resistant Enterococcus spp. 22 14 2.8 (0.5–5.5) 0.6 (0.001–13.0) −2.2 Clostridioides difficile 5 6 7.1 (4.6–33.0) 3.9 (1.1–15.7) −3.2 IQR, interquartile range; ESBL, extended-spectrum ß-lactamase; MDR, multidrug resistant. Antibiotics 2021,10, 680 7 of 22 Antibiotics 2021, 10, x FOR PEER REVIEW 8 of 23 Figure 3. Prevalence of different MDRO in LTCF in 5-year periods. ESBL, extended-spectrum ß-lactamase; MDR, multidrug-resistant; MRSA, methicillin-resistant Staphylococcus aureus. Figure 3. Prevalence of different MDRO in LTCF in 5-year periods. ESBL, extended-spectrum ß-lactamase; MDR, multidrugresistant; MRSA, methicillin-resistant Staphylococcus aureus. 2.5. Risk Factors for Colonization 2.5.1. Reside in Nursing Homes Residing in NH and other LTCF was reported in many studies to be a risk factor for MDRO colonization [ 28 , 37 , 99 ]. A point-prevalence study analyzing MDRO prevalence in Antibiotics 2021,10, 680 8 of 22 LTCF, rehabilitation clinics, and homecare facilities found that LTCF and homecare services correlated with a much higher prevalence of MDROs and C. difficile than rehabilitation clinics [ 37 ]. In a prospective study performed in France to identify and compare residents of NH or LTCF colonized with bacteria (defined as exposure to the risk of carrying MDROs) with those living at home (defined as non-exposed), the rate of MDRO carriage was found to be three times higher among institutionalized patients [99]. In a cross-sectional study conducted in a 342-bed hospital and 4 LTCF in Spain, at hospital admission, the prevalence of MRSA colonization was found to be around five times more likely (odds ratio (OR) 4.84 95% CI 1.00–23.51) among patients referred from an LTCF or residential center than among patients from the community [ 72 ]. In Singapore, the admission prevalence of MRSA colonization was 41% (78/190) for those from NH and 6.0% (885/14,849) among non-nursing home residents (relative risk (RR) 6.89 95% CI 5.74–8.26). In this study, the fraction of the MRSA burden upon admission attributable to NH residency was 6.92% [ 35 ]. In a German study, the prevalence of intestinal colonization by C. difficile among 240 NH residents was higher than that among 249 volunteers living outside the LTCF (4.6% vs. 0.8%, p= 0.02) [140]. Thus, residing in LTCF seems by itself to be a risk factor for colonization by MDROs. However, differences in NH infrastructure need to be considered. Specifically, the presence of communal areas and multi-bed resident rooms could impact the transmission risk inside such areas [109]. 2.5.2. Age Older age was also established in many studies as a risk factor for MRSA colonization based on bivariate analysis [ 13 , 20 , 26 , 61 , 79 , 98 ]. In most studies, age was analyzed as a categorical variable. An analysis of national surveillance data over an 11-year period between 2007 and 2017 in Swiss NH, including a total of 9940 residents, established three categories (<70, 70–85, and >85) that increased the colonization risk from age 70 onward [ 13 ]. Similar results were obtained in Ireland for residents >80 years [ 98 ] and in four Italian LTCF fixing the cut-off at >86 years [ 20 ]. However, in these studies, the rates reported as an increased risk of MDRO colonization were two-fold lower and lacked statistical significance in the multivariate analysis. Somestudies reportedageasanindependent riskfactorviamultivariate analysis [22,26,80] . In Northern Ireland, a point-prevalence study of 45 NH including 1111 residents, based on a reference age of <60 years, found that those aged ≥ 90 were around nine times more likely to be colonized in the adjusted analysis (OR 8.77 95% CI 2.86–26.86; p< 0.001) [ 80 ]. An Italian study reported OR 4.63 (95% CI 1.12–19.1; p= 0.034) in residents with age ≥ 86 years to be colonized by ESBL producers [ 22 ], and in Taiwan, MRSA colonization was more frequent in residents aged ≥60 years (OR 2.164 95% CI1.168–4.001; p= 0.013) [26]. No difference was established by age as a continuous variable in a study including 14 NH in Taiwan; however, an age >60 years was significantly associated with MRSA colonization (OR 2.164 95% CI 1.168–4.011) [ 26 ]. An age ≥ 86 years was related to ESBL colonization, but not to MRSA colonization in a point-prevalence study of MRSA, VRE, ESBL Enterobacterales, CR, and high-level AmpC activity in a 120-bed LTCF attached to the regional hospital in Bolzano, Italy [22]. Therefore, older patients were generally around twice as likely to be colonized than younger patients across the studies; however, some studies found no differences up to 90 years of age based on multivariate analysis. In addition, the different categories used in the studies prevent us from establishing a cut-off or fixed age that is more likely to be colonized by MDROs (Table 3). Antibiotics 2021,10, 680 9 of 22 Table 3. Risk factors for multidrug-resistant organism colonization in long-term care facilities in the studies. Common characteristics and limitations. Risk Factors for MDRO Colonization Limitations and Common Characteristics Age An increase entails higher risk. There is not a cut-off established for colonization by MDROs. Male sex Confirmed in many studies by multivariate analysis Dementia An increase entails higher risk. There is not a cut-off established for colonization by MDROs. Diabetes Controversial results. Differences by MDRO type. Cancer Controversial results. Differences by MDRO type. Chronic wound Confirmed in many studies by multivariate analysis Dependence An increase entails higher risk. There is not a cut-off established for colonization by MDROs. Medical devices Confirmed in many studies by multivariate analysis Previous antibiotic use Confirmed in many studies by multivariate analysis Previous hospitalization Whether the risk could be increased by days of hospitalization is unknown. Previous MDRO colonization Controversial results. Differences by MDRO type. MDRO: multidrug-resistant organism. 2.5.3. Sex The risk of MDRO colonization was higher in males than in females across the studies [ 13 , 20 , 31 , 43 , 47 , 49 , 77 , 98 ] (Table 3). An Italian point-prevalence study of 340 residents in four LTCF found male sex to be an independent risk factor for MRSA colonization with an OR of 2.31 (95% CI 1.16–4.59); however, male sex was not found to be an independent risk factor for ESBL colonization in this study [ 20 ]. In Ireland, a study including 6 NH and 786 residents obtained similar results for MRSA colonization, with an OR 2.18 95% CI (1.28–3.73) [ 98 ]. Other studies reported male sex to be around 1.5 times more likely than the female sex to be colonized by MRSA [77,80]. In Belgium, a multilevel logistic regression analysis of individual risk factors for ESBL Enterobacterales carriage among 2457 residents of 60 NH determined an OR of 1.5 (95% CI 1.1–2.1) associated with the male sex [ 31 ]. Other authors found similar results for ESBL colonization in Switzerland [13]. The reason why male sex is a risk factor remains unknown. However, the higher frequencies of other risk factors among male residents, who have more co-morbidities compared to female residents, likely predisposed men to have around 1.5 times greater risk than women for MDRO acquisition in most studies. 2.5.4. Underlying Diseases: Dementia (Lower Cognitive Status), Diabetes, Cancer and Chronic Wound (Pressure/Decubitus Ulcer) Analyzing the impact of underlying diseases on MDRO colonization is not a straightforward task, since miscellaneous baseline diseases are included in many studies, which makes it challenging to draw conclusions. In some studies, underlying diseases were ranked using the Charlson index or co-morbidity score [ 74 , 79 ]. Residents with a Charlson index of ≥ 2 were 1.5 times more probable to be colonized by MRSA in a study performed on two communities in Spain, including nine LTCF with a total of 1586 beds [79]. In the same way, some studies analyzed diseases such as dementia as encased variables within chronic cerebral conditions to rank their Global Deterioration Score (ranging from 0—normal to 7—end-stage dementia) [ 28 , 58 , 96 ]. Two studies in Hong Kong found dementia, encased with other chronic cerebral conditions such as cerebrovascular accidents and Parkinson’s disease, to be independent risk factors for MRSA colonization based on multivariate analysis [ 28 , 96 ]. Other studies included the level of dementia, categorized Antibiotics 2021,10, 680 16 of 22 13. Kohler, P.; Fulchini, R.; Albrich, W.C.; Egli, A.; Balmelli, C.; Harbarth, S.; Héquet, D.; Kahlert, C.R.; Kuster, S.P.; Petignat, C.; et al. Antibiotic resistance in Swiss nursing homes: Analysis of National Surveillance Data over an 11-year period between 2007 and 2017. Antimicrob. Resist. Infect. Control. 2018,7, 88. [CrossRef] [PubMed] 14. Mylotte, J.M.; Goodnough, S.; Tayara, A. Antibiotic-resistant organisms among long-term care facility residents on admission to an inpatient geriatrics unit: Retrospective and prospective surveillance. Am. J. Infect. Control. 2001,29, 139–144. [CrossRef] 15. Drayß, M.; Claus, H.; Hubert, K.; Thiel, K.; Berger, A.; Sing, A.; Van Der Linden, M.; Vogel, U.; Lâm, T.-T. Asymptomatic carriage of Neisseria meningitidis, Haemophilus influenzae, Streptococcus pneumoniae, Group A Streptococcus and Staphylococcus aureus among adults aged 65 years and older. PLoS ONE 2019,14, e0212052. [CrossRef] [PubMed] 16. Verhoef, L.; Roukens, M.; De Greeff, S.; Meessen, N.; Natsch, S.; Stobberingh, E. Carriage of antimicrobial-resistant commensal bacteria in Dutch long-term-care facilities. J. Antimicrob. Chemother. 2016,71, 2586–2592. [CrossRef] 17. Brugnaro, P.; Fedeli, U.; Pellizzer, G.; Buonfrate, D.; Rassu, M.; Boldrin, C.; Parisi, S.G.; Grossato, A.; Palù, G.; Spolaore, P. Clustering and Risk Factors of Methicillin-Resistant Staphylococcus aureus Carriage in Two Italian Long-Term Care Facilities. Infection 2008,37, 216–221. [CrossRef] [PubMed] 18. Ludden, C.; Cormican, M.; Vellinga, A.; Johnson, J.R.; Austin, B.; Morris, D. Colonisation with ESBL-producing and carbapenemase-producing Enterobacteriaceae, vancomycin-resistant enterococci, and meticillin-resistant Staphylococcus aureus in a long-term care facility over one year. BMC Infect. Dis. 2015,15, 168. [CrossRef] 19. Giufrè, M.; Ricchizzi, E.; Accogli, M.; Barbanti, F.; Monaco, M.; De Araujo, F.P.; Farina, C.; Fazii, P.; Mattei, R.; Sarti, M.; et al. Colonization by multidrug-resistant organisms in long-term care facilities in Italy: A point-prevalence study. Clin. Microbiol. Infect. 2017,23, 961–967. [CrossRef] 20. Nucleo, E.; Caltagirone, M.; Marchetti, V.M.; D’Angelo, R.; Fogato, E.; Confalonieri, M.; Reboli, C.; March, A.; Sleghel, F.; Soelva, G.; et al. Colonization of long-term care facility residents in three Italian Provinces by multidrug-resistant bacteria. Antimicrob. Resist. Infect. Control. 2018,7, 33. [CrossRef] 21. March, A.; Aschbacher, R.; Sleghel, F.; Soelva, G.; Kaczor, M.; Migliavacca, R.; Piazza, A.; Mattioni Marchetti, V.; Pagani, L.; Scalzo, K.; et al. Colonization of residents and staff of an Italian long-term care facility and an adjacent acute care hospital geriatric unit by multidrug-resistant bacteria. New Microbiol. 2017,40, 258–263. [PubMed] 22. March, A.; Aschbacher, R.; Dhanji, H.; Livermore, D.M.; Böttcher, A.; Sleghel, F.; Maggi, S.; Noale, M.; Larcher, C.; Woodford, N. Colonization of residents and staff of a long-term-care facility and adjacent acute-care hospital geriatric unit by multiresistant bacteria. Clin. Microbiol. Infect. 2010,16, 934–944. [CrossRef] [PubMed] 23. Trick, W.E.; Weinstein, R.A.; DeMarais, P.L.; Kuehnert, M.J.; Tomaska, W.; Nathan, C.; Rice, T.W.; McAllister, S.K.; Carson, L.A.; Jarvis, W.R. Colonization of Skilled-Care Facility Residents with Antimicrobial-Resistant Pathogens. J. Am. Geriatr. Soc. 2001 ,49, 270–276. [CrossRef] 24. Roghmann, M.-C.; Lydecker, A.D.; Hittle, L.; DeBoy, R.T.; Nowak, R.G.; Johnson, J.K.; Mongodin, E.F. Comparison of the Microbiota of Older Adults Living in Nursing Homes and the Community. mSphere 2017,2, e00210-17. [CrossRef] 25. Hogardt, M.; Proba, P.; Mischler, D.; Cuny, C.; Kempf, V.A.; Heudorf, U. Current prevalence of multidrug-resistant organisms in long-term care facilities in the Rhine-Main district, Germany, 2013. Eurosurveillance 2015,20, 21171. [CrossRef] [PubMed] 26. Tsao, F.-Y.; Kou, H.-W.; Huang, Y.-C. Dissemination of methicillin-resistant Staphylococcus aureus sequence type 45 among nursing home residents and staff in Taiwan. Clin. Microbiol. Infect. 2015,21, 451–458. [CrossRef] [PubMed] 27. Hudson, L.O.; Reynolds, C.; Spratt, B.G.; Enright, M.C.; Quan, V.; Kim, D.; Hannah, P.; Mikhail, L.; Alexander, R.; Moore, D.F.; et al. Diversity of Methicillin-Resistant Staphylococcus aureus Strains Isolated from Residents of 26 Nursing Homes in Orange County, California. J. Clin. Microbiol. 2013,51, 3788–3795. [CrossRef] 28. Cheng, V.C.C.; Chen, J.H.K.; Ng, W.C.; Wong, J.Y.H.; Chow, D.M.K.; Law, T.C.; So, S.Y.C.; Wong, S.C.Y.; Chan, T.C.; Chan, F.H.W.; et al. Emergence of Carbapenem-Resistant Acinetobacter baumannii in Nursing Homes With High Background Rates of MRSA Colonization. Infect. Control Hosp. Epidemiol. 2016,37, 983–986. [CrossRef] 29. Mody, L.; Kauffman, C.A.; Donabedian, S.; Zervos, M.; Bradley, S.F. Epidemiology of Staphylococcus aureus Colonization in Nursing Home Residents. Clin. Infect. Dis. 2008,46, 1368–1373. [CrossRef] 30. Denis, O.; Jans, B.; Deplano, A.; Nonhoff, C.; De Ryck, R.; Suetens, C.; Struelens, M.J. Epidemiology of methicillin-resistant Staphylococcus aureus (MRSA) among residents of nursing homes in Belgium. J. Antimicrob. Chemother. 2009 ,64, 1299–1306. [CrossRef] 31. 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. [CrossRef] 32. Kotilainen, P.; Routamaa, M.; Peltonen, R.; Evesti, P.; Eerola, E.; Salmenlinna, S.; Vuopio-Varkila, J.; Rossi, T. Eradication of methicillin-resistant Staphylococcus aureus from a health center ward and associated nursing home. Arch. Intern. Med. 2001 ,161, 859–863. [CrossRef] 33. Min, L.; Galecki, A.; Mody, L. Functional Disability and Nursing Resource Use Are Predictive of Antimicrobial Resistance in Nursing Homes. J. Am. Geriatr. Soc. 2015,63, 659–666. [CrossRef] [PubMed] 34. Van Dulm, E.; Tholen, A.T.R.; Pettersson, A.; Van Rooijen, M.S.; Willemsen, I.; Molenaar, P.; Damen, M.; Gruteke, P.; Oostvogel, P.; Kuijper, E.J.; et al. High prevalence of multidrug resistant Enterobacteriaceae among residents of long term care facilities in Amsterdam, the Netherlands. PLoS ONE 2019,14, e0222200. [CrossRef] [PubMed] Antibiotics 2021,10, 680 17 of 22 35. Verrall, A.; Merchant, R.; Dillon, J.; Ying, D.; Fisher, D. Impact of nursing home residence on hospital epidemiology of meticillinresistant Staphylococcus aureus: A perspective from Asia. J. Hosp. Infect. 2013,83, 250–252. [CrossRef] 36. Stone, N.D.; Lewis, D.R.; Lowery, H.K.; Darrow, L.A.; Kroll, C.M.; Gaynes, R.P.; Jernigan, J.A.; McGowan, J.E.; Tenover, F.C.; Richards, C.L. Importance of Bacterial Burden Among Methicillin-Resistant Staphylococcus aureus Carriers in a Long-Term Care Facility. Infect. Control Hosp. Epidemiol. 2008,29, 143–148. [CrossRef] 37. Hübner, N.; Dittmann, K.; Begunk, R.; Kramer, A. Infection control measures and prevalence of multidrug-resistant organisms in non-hospital care settings in northeastern Germany: Results from a one-day point prevalence study. J. Hosp. Infect. 2017 ,97, 234–240. [CrossRef] [PubMed] 38. Mitchell, S.L.; Shaffer, M.L.; Loeb, M.B.; Givens, J.L.; Habtemariam, D.; Kiely, D.K.; D’Agata, E. Infection Management and Multidrug-Resistant Organisms in Nursing Home Residents With Advanced Dementia. JAMA Intern. Med. 2014 ,174, 1660–1667. [CrossRef] 39. Ruscher, C.; Pfeifer, Y.; Layer, F.; Schaumann, R.; Levin, K.; Mielke, M. Inguinal skin colonization with multidrug-resistant bacteria among residents of elderly care facilities: Frequency, persistence, molecular analysis and clinical impact. Int. J. Med. Microbiol. 2014,304, 1123–1134. [CrossRef] 40. Greenland, K.; Rijnders, M.I.; Mulders, M.; Haenen, A.; Spalburg, E.; Van De Kassteele, J.; De Neeling, A.; Stobberingh, E. Low Prevalence of Methicillin-Resistant Staphylococcus Aureus in Dutch Nursing Homes. J. Am. Geriatr. Soc. 2011 ,59, 768–769. [CrossRef] [PubMed] 41. Gibson, K.E.; McNamara, S.E.; Cassone, M.; Perri, M.B.; Zervos, M.; Mody, L.; on behalf of the Targeted Infection Prevention (TIP) Study Team, Ann Arbor, Michigan. Methicillin-Resistant Staphylococcus aureus:Site of Acquisition and Strain Variation in High-Risk Nursing Home Residents with Indwelling Devices. Infect. Control Hosp. Epidemiol. 2014,35, 1458–1465. [CrossRef] 42. Reynolds, C.; Quan, V.; Kim, D.; Peterson, E.; Dunn, J.; Whealon, M.; Terpstra, L.; Meyers, H.; Cheung, M.; Lee, B.; et al. Methicillin-Resistant Staphylococcus aureus (MRSA) Carriage in 10 Nursing Homes in Orange County, California. Infect. Control Hosp. Epidemiol. 2011,32, 91–93. [CrossRef] 43. Murphy, S.; Denman, S.; Bennett, R.G.; Greenough, W.B.; Lindsay, J.; Zelesnick, L.B. Methicillin-ResistantStaphylococcus aureusColonization in a Long-Term-Care Facility. J. Am. Geriatr. Soc. 1992,40, 213–217. [CrossRef] 44. Storch, G.A.; Radcliff, J.L.; Meyer, P.L.; Hinrichs, J.H. Methicillin-Resistant Staphylococcus aureus in a Nursing Home. Infect. Control. 1987,8, 24–29. [CrossRef] 45. Muder, R.R.; Brennen, C.; Wagener, M.M.; Vickers, R.M.; Rihs, J.D.; Hancock, G.A.; Yee, Y.C.; Miller, J.M.; Yu, V.L. Methicillin- Resistant Staphylococcal Colonization and Infection in a Long-Term Care Facility. Ann. Intern. Med. 1991 ,114, 107–112. [CrossRef] 46. Eveillard, M.; Charru, P.; Rufat, P.; Hippeaux, M.-C.; Lancien, E.; Benselama, F.; Branger, C. Methicillin-resistant Staphylococcus aureus carriage in a long-term care facility: Hypothesis about selection and transmission. Age Ageing 2008 ,37, 294–299. [CrossRef] 47. Cox, R.; Bowie, P. Methicillin-resistant Staphylococcus aureus colonization in nursing home residents: A prevalence study in Northamptonshire. J. Hosp. Infect. 1999,43, 115–122. [CrossRef] [PubMed] 48. Suetens, C.; Niclaes, L.; Jans, B.; Verhaegen, J.; Schuermans, A.; Van Eldere, J.; Buntinx, F. Methicillin-Resistant Staphylococcus aureus Colonization Is Associated with Higher Mortality in Nursing Home Residents with Impaired Cognitive Status. J. Am. Geriatr. Soc. 2006,54, 1854–1860. [CrossRef] [PubMed] 49. Nillius, D.; Von Müller, L.; Wagenpfeil, S.; Klein, R.; Herrmann, M. Methicillin-Resistant Staphylococcus aureus in Saarland, Germany: The Long-Term Care Facility Study. PLoS ONE 2016,11, e0153030. [CrossRef] 50. Namnyak, S.; Adhami, Z.; Wilmore, M.; Keynes, H.; Hampton, K.; Mercieca, E.; Roker, K. Methicillin-resistant Staphylococcus aureus: A questionnaire and microbiological survey of nursing and residential homes in Barking, Havering and Brentwood. J. Infect. 1998,36, 67–72. [CrossRef] 51. Bradley, S.F.; Terpenning, M.S.; Ramsey, M.A.; Zarins, L.T.; Jorgensen, K.A.; Sottile, W.S.; Schaberg, D.R.; Kauffman, C.A. Methicillin-resistant Staphylococcus aureus: Colonization and Infection in a Long-term Care Facility. Ann. Intern. Med. 1991 ,115, 417–422. [CrossRef] [PubMed] 52. Monaco, M.; Bombana, E.; Trezzi, L.; Regattin, L.; Brusaferro, S.; Pantosti, A.; Goglio, A. Meticillin-resistant Staphylococcus aureus colonising residents and staff members in a nursing home in Northern Italy. J. Hosp. Infect. 2009 ,73, 182–184. [CrossRef] [PubMed] 53. Horner, C.; Parnell, P.; Hall, D.; Kearns, A.; Heritage, J.; Wilcox, M. Meticillin-resistant Staphylococcus aureus in elderly residents of care homes: Colonization rates and molecular epidemiology. J. Hosp. Infect. 2013,83, 212–218. [CrossRef] 54. Ho, P.-L.; Lai, E.L.; Chow, K.-H.; Chow, L.S.; Yuen, K.-Y.; Yung, R.W. Molecular epidemiology of methicillin-resistant Staphylococcus aureus in residential care homes for the elderly in Hong Kong. Diagn. Microbiol. Infect. Dis. 2008 ,61, 135–142. [CrossRef] [PubMed] 55. 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. [CrossRef] 56. Friedewald, M.; de Wit, D. MRSA screening of nursing home, residents admitted to hospital on the NSW Central Coast. Aust. Infect. Control. 2001,6, 119–121. [CrossRef] Antibiotics 2021,10, 680 18 of 22 57. Gruber, I.; Heudorf, U.; Werner, G.; Pfeifer, Y.; Imirzalioglu, C.; Ackermann, H.; Brandt, C.; Besier, S.; Wichelhaus, T.A. Multidrugresistant bacteria in geriatric clinics, nursing homes, and ambulant care—Prevalence and risk factors. Int. J. Med. Microbiol. 2013 , 303, 405–409. [CrossRef] [PubMed] 58. O’Fallon, E.; Schreiber, R.; Kandel, R.; D’Agata, E.M.C. Multidrug-Resistant Gram-Negative Bacteria at a Long-Term Care Facility: Assessment of Residents, Healthcare Workers, and Inanimate Surfaces. Infect. Control Hosp. Epidemiol. 2009 ,30, 1172–1179. [CrossRef] [PubMed] 59. Pop-Vicas, A.; Mitchell, S.L.; Kandel, R.; Schreiber, R.; D’Agata, E.M.C. Multidrug-Resistant Gram-Negative Bacteria in a Long-Term Care Facility: Prevalence and Risk Factors. J. Am. Geriatr. Soc. 2008,56, 1276–1280. [CrossRef] 60. Chen, H.; Au, K.M.; Hsu, K.E.; Lai, C.K.; Myint, J.; Mak, Y.F.; Lee, S.Y.; Wong, T.Y.; Tsang, N.C. Multidrug-resistant organism carriage among residents from residential care homes for the elderly in Hong Kong: A prevalence survey with stratified cluster sampling. Hong Kong Med. J. 2018,24, 350–360. [CrossRef] 61. Da Silveira, M.; Cunha, M.D.L.R.D.S.D.; De Souza, C.S.M.; Correa, A.A.F.; Fortaleza, C.M.C.B. Nasal colonization with methicillinresistant Staphylococcus aureus among elderly living in nursing homes in Brazil: Risk factors and molecular epidemiology. Ann. Clin. Microbiol. Antimicrob. 2018,17, 1–5. [CrossRef] [PubMed] 62. Kwetkat, A.; Pfister, W.; Pansow, D.; Pletz, M.W.; Sieber, C.C.; Hoyer, H. Naso- and oropharyngeal bacterial carriage in nursing home residents: Impact of multimorbidity and functional impairment. PLoS ONE 2018,13, e0190716. [CrossRef] [PubMed] 63. Manzur, A.; Domínguez, M.A.; de Gopegui, E.R.; Mariscal, D.; Gavalda, L.; Segura, F.; Perez, J.; Pujol, M. Natural history of meticillin-resistant Staphylococcus aureus colonisation among residents in community long term care facilities in Spain. J. Hosp. Infect. 2010,76, 215–219. [CrossRef] [PubMed] 64. Wang, J.; Foxman, B.; Mody, L.; Snitkin, E.S. Network of microbial and antibiotic interactions drive colonization and infection with multidrug-resistant organisms. Proc. Natl. Acad. Sci. USA 2017,114, 10467–10472. [CrossRef] [PubMed] 65. Fisch, J.; Lansing, B.; Wang, L.; Symons, K.; Cherian, K.; McNamara, S.; Mody, L. New Acquisition of Antibiotic-Resistant Organisms in Skilled Nursing Facilities. J. Clin. Microbiol. 2012,50, 1698–1703. [CrossRef] [PubMed] 66. Heinze, K.; Kabeto, M.; Martin, E.T.; Cassone, M.; Hicks, L.; Mody, L. Predictors of methicillin-resistant Staphylococcus aureus and vancomycin-resistant enterococci co-colonization among nursing facility patients. Am. J. Infect. Control. 2019 ,47, 415–420. [CrossRef] 67. Lee, C.-M.; Lai, C.-C.; Chiang, H.-T.; Lu, M.-C.; Wang, L.-F.; Tsai, T.-L.; Kang, M.-Y.; Jan, Y.-N.; Lo, Y.-T.; Ko, W.-C.; et al. Presence of multidrug-resistant organisms in the residents and environments of long-term care facilities in Taiwan. J. Microbiol. Immunol. Infect. 2017,50, 133–144. [CrossRef] 68. Budimir, A.; Pal, M.P.; Bošnjak, Z.; Marekovi´c, I.; Vukovi´c, D.; Križan, I.R.; Milas, J.; Pleˇcko, V.; Kaleni´c, S. Prevalence and molecular characteristics of methicillin-resistant Staphylococcus aureus strains isolated in a multicenter study of nursing home residents in Croatia. Am. J. Infect. Control. 2014,42, 1197–1202. [CrossRef] 69. 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. [CrossRef] 70. Moschou, A.; Maraki, S.; Giormezis, N.; Moraitaki, H.; Stafylaki, D.; Militsopoulou, M.; Spiliopoulou, I.; Papadakis, J.; Samonis, G.; Kofteridis, D. Prevalence and molecular epidemiology of Staphylococcus aureus nasal colonization in four nursing home residents in Crete, Greece. J. Infect. Chemother. 2020,26, 199–204. [CrossRef] 71. Cretnik, T.Z.; Vovko, P.; Retelj, M.; Juteršek, B.; Harlander, T.; Kolman, J.; Gubina, M. Prevalence and Nosocomial Spread of Methicillin-ResistantStaphylococcus aureusin a Long-Term-Care Facility in Slovenia. Infect. Control Hosp. Epidemiol. 2005 ,26, 184–190. [CrossRef] 72. Barrufet, M.P.; Vendrell, E.; Force, L.; Sauca, G.; Rodríguez, S.; Martínez, E.; Palomera, E.; Serra-Prat, M.; Capdevila, J.A.; Cornudella, J.; et al. Prevalence and risk factors for meticillin-resistant Staphylococcus aureus in an acute care hospital and long-term care facilities located in the same geographic area. Rev. Esp. Quimioter. 2014,27, 190–195. [PubMed] 73. McKinnell, J.A.; Singh, R.D.; Miller, L.G.; Kleinman, K.; Gussin, G.; He, J.; Saavedra, R.; Dutciuc, T.D.; Estevez, M.; Chang, J.; et al. The SHIELD Orange County Project: Multidrug-resistant Organism Prevalence in 21 Nursing Homes and Long-term Acute Care Facilities in Southern California. Clin. Infect. Dis. 2019,69, 1566–1573. [CrossRef] 74. Mody, L.; Gibson, K.E.; Horcher, A.; Prenovost, K.; McNamara, S.E.; Foxman, B.; Kaye, K.S.; Bradley, S. Prevalence of and Risk Factors for Multidrug-Resistant Acinetobacter baumannii Colonization Among High-Risk Nursing Home Residents. Infect. Control Hosp. Epidemiol. 2015,36, 1155–1162. [CrossRef] [PubMed] 75. Hoogendoorn, M.; Smalbrugge, M.; Stobberingh, E.E.; van Rossum, S.V.; Vlaminckx, B.J.; Thijsen, S.F. Prevalence of Antibiotic Resistance of the Commensal Flora in Dutch Nursing Homes. J. Am. Med. Dir. Assoc. 2013,14, 336–339. [CrossRef] [PubMed] 76. Andersson, H.; Lindholm, C.; Iversen, A.; Giske, C.G.; Örtqvist, Å.; Kalin, M.; Fossum, B. Prevalence of antibiotic-resistant bacteria in residents of nursing homes in a Swedish municipality: Healthcare staff knowledge of and adherence to principles of basic infection prevention. Scand. J. Infect. Dis. 2012,44, 641–649. [CrossRef] [PubMed] 77. Barr, B.; Wilcox, M.H.; Brady, A.; Parnell, P.; Darby, B.; Tompkins, D. Prevalence of Methicillin-ResistantStaphylococcus aureusColonization Among Older Residents of Care Homes in the United Kingdom. Infect. Control Hosp. Epidemiol. 2007 ,28, 853–859. [CrossRef] Antibiotics 2021,10, 680 19 of 22 78. Furuno, J.P.; Hebden, J.N.; Standiford, H.C.; Perencevich, E.N.; Miller, R.R.; Moore, A.C.; Strauss, S.M.; Harris, A.D. Prevalence of methicillin-resistant Staphylococcus aureus and Acinetobacter baumannii in a long-term acute care facility. Am. J. Infect. Control. 2008,36, 468–471. [CrossRef] 79. Manzur, A.; Gavalda, L.; de Gopegui, E.R.; Mariscal, D.; Domínguez, M.A.; Perez, J.; Segura, F.; Pujol, M. Prevalence of methicillinresistant Staphylococcus aureus and factors associated with colonization among residents in community long-term-care facilities in Spain. Clin. Microbiol. Infect. 2008,14, 867–872. [CrossRef] 80. Baldwin, N.S.; Gilpin, D.; Hughes, C.M.; Kearney, M.P.; Gardiner, D.A.; Cardwell, C.; Tunney, M.M. Prevalence of Methicillin- Resistant Staphylococcus aureus Colonization in Residents and Staff in Nursing Homes in Northern Ireland. J. Am. Geriatr. Soc. 2009,57, 620–626. [CrossRef] 81. Flint, J.A.; Ryan, P.; Gordon, D.L. Prevalence of MRSA in South Australian nursing homes. Med. J. Aust. 1998 ,169, 559–560. [CrossRef] [PubMed] 82. Lim, C.J.; Cheng, A.; Kennon, J.; Spelman, D.; Hale, D.; Melican, G.; Sidjabat, H.E.; Paterson, D.L.; Kong, D.; Peleg, A.Y. Prevalence of multidrug-resistant organisms and risk factors for carriage in long-term care facilities: A nested case-control study. J. Antimicrob. Chemother. 2014,69, 1972–1980. [CrossRef] 83. Latour, K.; Huang, T.-D.; Jans, B.; Berhin, C.; Bogaerts, P.; Noel, A.; Nonhoff, C.; Dodémont, M.; Denis, O.; Ieven, M.; et al. Prevalence of multidrug-resistant organisms in nursing homes in Belgium in 2015. PLoS ONE 2019 ,14, e0214327. [CrossRef] [PubMed] 84. Mossong, J.; Gelhausen, E.; Decruyenaere, F.; Devaux, A.; Perrin, M.; Even, J.; Heisbourg, E. Prevalence, risk factors and molecular epidemiology of methicillin-resistantStaphylococcus aureus(MRSA) colonization in residents of long-term care facilities in Luxembourg, 2010. Epidemiol. Infect. 2012,141, 1199–1206. [CrossRef] [PubMed] 85. Del Rosario-Quintana, C.; Tosco-Núñez, T.; Lorenzo, L.; Martín-Sánchez, A.M.; Molina-Cabrillana, J. Prevalencia y factores asociados a la colonización de microorganismos multirresistentes en centros de larga estancia de Gran Canaria. Revista Española de Geriatría y Gerontología2015,50, 232–236. [CrossRef] 86. Vovko, P.; Retelj, M.; Cretnik, T.Z.; Jutersek, B.; Harlander, T.; Kolman, J.; Gubina, M. Risk Factors for Colonization With Methicillin-ResistantStaphylococcus aureusin a Long-Term-Care Facility in Slovenia. Infect. Control Hosp. Epidemiol. 2005 ,26, 191–195. [CrossRef] [PubMed] 87. Gu, F.-F.; Zhang, J.; Zhao, S.-Y.; Yang, Z.-R.; Zhang, Y.-L.; Xiao, S.-Z.; Wang, S.; Guo, X.-K.; Qu, J.-M.; Ni, Y.-X.; et al. Risk factors for methicillin-resistant Staphylococcus aureus carriage among residents in 7 nursing homes in Shanghai, China. Am. J. Infect. Control. 2016,44, 805–808. [CrossRef] 88. Becker, J.; Diel, R. Screening for Methicillin-resistant Staphylococcus aureus in a residence home for elderly in Germany. J. Occup. Med. Toxicol. 2017,12, 3. [CrossRef] 89. El Emam, K.; Arbuckle, L.; Essex, A.; Samet, S.; Eze, B.; Middleton, G.; Buckeridge, D.; Jonker, E.; Moher, E.; Earle, C. Secure Surveillance of Antimicrobial Resistant Organism Colonization or Infection in Ontario Long Term Care Homes. PLoS ONE 2014 , 9, e93285. [CrossRef] 90. Cederna, J.E.; Terpenning, M.S.; Ensberg, M.; Bradley, S.F.; Kauffman, C.A. StaphylococcusaureusNasal Colonization in a Nursing Home: Eradication With Mupirocin. Infect. Control Hosp. Epidemiol. 1990,11, 13–16. [CrossRef] 91. Lasseter, G.; Charlett, A.; Lewis, D.L.; Donald, I.P.; Howelljones, R.; McNulty, C.A.M. Staphylococcus aureus carriage in care homes: Identification of risk factors, including the role of dementia. Epidemiol. Infect. 2010,138, 686–696. [CrossRef] 92. Galán-Sánchez, F.; Pérez-Eslava, M.; Machuca, J.; Trujillo-Soto, T.; Arca-Suárez, J.; Rodríguez-Iglesias, M. Staphylococcus aureus carriage in older populations in community residential care homes: Prevalence and molecular characterization of MRSA isolates. Enfermedades Infecciosas y Microbiología Clínica 2019,37, 172–175. [CrossRef] 93. Kerttula, A.-M.; Lyytikäinen, O.; Virolainen, A.; Finne-Soveri, H.; Agthe, N.; Vuopio-Varkila, J. Staphylococcus aureus colonization among nursing home residents in a large Finnish nursing home. Scand. J. Infect. Dis. 2007,39, 996–1001. [CrossRef] [PubMed] 94. Lee, Y.-L.; Cesario, T.; Gupta, G.; Flionis, L.; Tran, C.; Decker, M.; Thrupp, L. Surveillance of colonization and infection with Staphylococcus aureus susceptible or resistant to methicillin in a community skilled-nursing facility. Am. J. Infect. Control. 1997, 25, 312–321. [CrossRef] 95. Chan, T.C.; Cheng, V.C.C.; Hung, I.F.N.; Chan, F.H.W.; Ng, W.C.; Yuen, K.Y. The Association between Methicillin Resistant Staphylococcus aureus Colonization and Mortality in Chinese Nursing Home Older Adults: A 2-Year Prospective Cohort. J. Am. Med. Dir. Assoc. 2015,16, 796–797. [CrossRef] [PubMed] 96. Cheng, V.C.; Tai, J.W.; Wong, Z.S.; Chen, J.H.; Pan, K.B.; Hai, Y.; Ng, W.-C.; Chow, D.M.; Yau, M.C.; Chan, J.F.; et al. Transmission of methicillin-resistant staphylococcus aureus in the long term care facilities in Hong Kong. BMC Infect. Dis. 2013 ,13, 1–205. [CrossRef] 97. McKinnell, J.A.; Miller, L.G.; Singh, R.; Kleinman, K.; Peterson, E.M.; Evans, K.D.; Dutciuc, T.D.; Heim, L.; Gombosev, A.; Estevez, M.; et al. Prevalence of and Factors Associated With Multidrug Resistant Organism (MDRO) Colonization in 3 Nursing Homes. Infect. Control Hosp. Epidemiol. 2016,37, 1485–1488. [CrossRef] [PubMed] 98. O’Sullivan, N.; Keane, C. Risk factors for colonization with methicillin-resistant Staphylococcus aureus among nursing home residents. J. Hosp. Infect. 2000,45, 206–210. [CrossRef] Antibiotics 2021,10, 680 20 of 22 99. Eveillard, M.; LaFargue, S.; Guet, L.; Mangeol, A.; Piquet, J.; Quenon, J.-L.; Fauvelle, F. Association between Institutionalization and Carriage of Multiresistant Bacteria in the Elderly at the Time of Admission to a General Hospital. Eur. J. Clin. Microbiol. Infect. Dis. 1999,18, 133–136. [CrossRef] 100. Dandachi, I.; Sokhn, E.S.; Najem, E.; Azar, E.; Daoud, Z. Carriage of beta-lactamase-producing Enterobacteriaceae among nursing home residents in north Lebanon. Int. J. Infect. Dis. 2016,45, 24–31. [CrossRef] 101. Van Der Donk, C.; Schols, J.; Driessen, C.; Hagenouw, R.; Meulendijks, A.; Stobberingh, E. Prevalence and Spread of Multidrug Resistant Escherichia coli Isolates Among Nursing Home Residents in the Southern Part of the Netherlands. J. Am. Med. Dir. Assoc. 2013,14, 199–203. [CrossRef] [PubMed] 102. Wiener, J.; Quinn, J.P.; Bradford, P.A.; Goering, R.; Nathan, C.; Bush, K.; Weinstein, R.A. Multiple Antibiotic–Resistant Klebsiella and Escherichia coli in Nursing Homes. JAMA 1999,281, 517–523. [CrossRef] [PubMed] 103. Birgand, G.; Hayatgheib, N.; Bémer, P.; Guilloteau, V.; Legeay, C.; Perron, S.; Chapelet, G.; Corvec, S.; Bourigault, C.; Batard, E.; et al. Multi-drug-resistant Enterobacteriacae carriage in highly exposed nursing homes: Prevalence in western France. J. Hosp. Infect. 2017,97, 258–259. [CrossRef] [PubMed] 104. Cochard, H.; Aubier, B.; Quentin, R.; Van Der Mee-Marquet, N.; Du Centre, R.D.H. Extended-Spectrum β -Lactamase–Producing Enterobacteriaceae in French Nursing Homes: An Association between High Carriage Rate among Residents, Environmental Contamination, Poor Conformity with Good Hygiene Practice, and Putative Resident-to-Resident Transmission. Infect. Control Hosp. Epidemiol. 2014,35, 384–389. [CrossRef] 105. Leitner, E.; Zechner, E.; Ullrich, E.; Zarfel, G.; Luxner, J.; Pux, C.; Pichler, G.; Schippinger, W.; Krause, R.; Zollner-Schwetz, I. Low prevalence of colonization with multidrug-resistant gram-negative bacteria in long-term care facilities in Graz, Austria. Am. J. Infect. Control. 2018,46, 76–80. [CrossRef] 106. Stuart, R.L.; Kotsanas, D.; Webb, B.; Vandergraaf, S.; Gillespie, E.E.; Hogg, G.G.; Korman, T. Prevalence of antimicrobial-resistant organisms in residential aged care facilities. Med. J. Aust. 2011,195, 530–533. [CrossRef] [PubMed] 107. Thibaut, S.; Caillon, J.; Marquet, A.; Grandjean, G.; Potel, G.; Ballereau, F.; Microbiology Laboratories of the MedQual Network. Epidemiology of third-generation cephalosporin-resistant community-acquired Enterobacteria isolated from elderly patients. Méd. Mal. Infect. 2014,44, 57–62. [CrossRef] [PubMed] 108. Rodrigues, C.; Machado, E.; Fernandes, S.; Peixe, L.; Novais, Â. Different Escherichia coli B2-ST131 clades (B and C) producing extended-spectrum β -lactamases (ESBL) colonizing residents of Portuguese nursing homes. Epidemiol. Infect. 2017 ,145, 3303–3306. [CrossRef] 109. Terveer, E.; Fallon, M.; Kraakman, M.; Ormond, A.; Fitzpatrick, M.; Caljouw, M.; Martin, A.; Van Dorp, S.; Wong, M.; Kuijper, E. Corrigendum to “Spread of ESBL-producing Escherichia coli in nursing home residents in Ireland and the Netherlands may reflect infrastructural differences” [J Hosp Infect 103 (2019) 160–164]. J. Hosp. Infect. 2020,103, 160–164. [CrossRef] 110. Valenza, G.; Nickel, S.; Pfeifer, Y.; Pietsch, M.; Voigtländer, E.; Lehner-Reindl, V.; Höller, C. Prevalence and genetic diversity of extended-spectrum β -lactamase (ESBL)-producing Escherichia coli in nursing homes in Bavaria, Germany. Veter- Microbiol. 2017 , 200, 138–141. [CrossRef] 111. Jallad, M.A.; Naoufal, R.; Irani, J.; Azar, E. Extended Spectrum Beta-Lactamase Carriage State among Elderly Nursing Home Residents in Beirut. Sci. World J. 2015,2015, 1–7. [CrossRef] 112. Yamamoto, Y.; Luvsansharav, U.-O.; Hirai, I.; Niki, M.; Nakata, A.; Yoshinaga, A.; Matsuura, N.; Kawakami, F. Fecal carriage of CTX-M β -lactamase-producing Enterobacteriaceae in nursing homes in the Kinki region of Japan. Infect. Drug Resist. 2013 ,6, 67–70. [CrossRef] [PubMed] 113. Gorrie, C.L.; Mirceta, M.; Wick, R.R.; Judd, L.M.; Wyres, K.L.; Thomson, N.R.; Strugnell, R.A.; Pratt, N.F.; Garlick, J.S.; Watson, K.M.; et al. Antimicrobial-Resistant Klebsiella pneumoniae Carriage and Infection in Specialized Geriatric Care Wards Linked to Acquisition in the Referring Hospital. Clin. Infect. Dis. 2018,67, 161–170. [CrossRef] 114. Pulcini, C.; Clerc-Urmes, I.; Attinsounon, C.A.; Fougnot, S.; Thilly, N. Antibiotic resistance of Enterobacteriaceae causing urinary tract infections in elderly patients living in the community and in the nursing home: A retrospective observational study. J. Antimicrob. Chemother. 2018,74, 775–781. [CrossRef] [PubMed] 115. Hagel, S.; Makarewicz, O.; Hartung, A.; Weiß, D.; Stein, C.; Brandt, C.; Schumacher, U.; Ehricht, R.; Patchev, V.; Pletz, M.W. ESBL colonization and acquisition in a hospital population: The molecular epidemiology and transmission of resistance genes. PLoS ONE 2019,14, e0208505. [CrossRef] 116. Rooney, P.J.; O’Leary, M.C.; Loughrey, A.C.; McCalmont, M.; Smyth, B.; Donaghy, P.; Badri, M.; Woodford, N.; Karisik, E.; Livermore, D.M. Nursing homes as a reservoir of extended-spectrum -lactamase (ESBL)-producing ciprofloxacin-resistant Escherichia coli. J. Antimicrob. Chemother. 2009,64, 635–641. [CrossRef] 117. Blom, A.; Ahl, J.; Månsson, F.; Resman, F.; Tham, J. The prevalence of ESBL-producing Enterobacteriaceae in a nursing home setting compared with elderly living at home: A cross-sectional comparison. BMC Infect. Dis. 2016 ,16, 111. [CrossRef] [PubMed] 118. Broussier, M.; Gbaguidi-Haoré, H.; Rachidi-Berjamy, F.; Bertrand, X.; Slekovec, C. Prevalence, genetic diversity of and factors associated with ESBL-producing Enterobacterales carriage in residents of French nursing homes. J. Hosp. Infect. 2020 ,104, 469–475. [CrossRef] 119. Willemsen, I.; Nelson, J.; Hendriks, Y.; Mulders, A.; Verhoeff, S.; Mulder, P.; Roosendaal, R.; Van Der Zwaluw, K.; Verhulst, C.; Bergh, M.K.-V.D.; et al. Extensive Dissemination of Extended Spectrum β -Lactamase–Producing Enterobacteriaceae in a Dutch Nursing Home. Infect. Control Hosp. Epidemiol. 2015,36, 394–400. [CrossRef] Antibiotics 2021,10, 680 21 of 22 120. Overdevest, I.; Haverkate, M.; Veenemans, J.; Hendriks, Y.; Verhulst, C.; Mulders, A.; Couprie, W.; Bootsma, M.; Johnson, J.; Kluytmans, J. Prolonged colonisation with Escherichia coli O25:ST131 versus other extended-spectrum beta-lactamase-producing E. coli in a long-term care facility with high endemic level of rectal colonisation, the Netherlands, 2013 to 2014. Eurosurveillance 2016,21, 30376. [CrossRef] 121. Arvand, M.; Moser, V.; Pfeifer, Y. Prevalence of extended-spectrum- β -lactamase-producing Escherichia coli and spread of the epidemic clonal lineage ST131 in nursing homes in Hesse, Germany. J. Antimicrob. Chemother. 2013,68, 2686–2688. [CrossRef] 122. Lautenbach, E.; Han, J.; Santana, E.; Tolomeo, P.; Bilker, W.B.; Maslow, J. Colonization with Extended-Spectrum β -Lactamase- ProducingEscherichia coliandKlebsiellaSpecies in Long-Term Care Facility Residents. Infect. Control Hosp. Epidemiol. 2012 ,33, 302–304. [CrossRef] 123. Van Der Mee-Marquet, N.; Savoyen, P.; Domelier-Valentin, A.-S.; Mourens, C.; Quentin, R.; Réseau des Hygiénistes du Centre Study Group. CTX-M–Type Fluoroquinolone-Resistant Escherichia coli: Analysis of the Colonization of Residents and Inanimate Surfaces 1 Year after a First Case of Urinary Tract Infection at a Nursing Home in France. Infect. Control Hosp. Epidemiol. 2010 ,31, 968–970. [CrossRef] 124. Bertrand, X.; Amara, M.; Sauget, M.; Clément, M.-C.; Talon, D.; Domelier-Valentin, A.-S.; Quentin, R.; van der Mee-Marquet, N. Extended-spectrum beta-lactamase-producing Enterobacteriacae: Unexpected low prevalence of carriage in elderly French residents. Age Ageing 2012,41, 233–237. [CrossRef] 125. Etherton-Beer, C.D.; Inglis, T.; Waterer, G. Prevalence of oropharyngeal antibiotic-resistant flora among residents of aged care facilities: A pilot study. Respirology 2015,20, 1139–1141. [CrossRef] [PubMed] 126. Benenson, S.; Cohen, M.J.; Block, C.; Stern, S.; Weiss, Y.; Moses, A.E.; JIRMI Group. Vancomycin-Resistant Enterococci in Long-Term Care Facilities. Infect. Control Hosp. Epidemiol. 2009,30, 786–789. [CrossRef] [PubMed] 127. Elizaga, M.L.; Weinstein, R.A.; Hayden, M.K. Patients in Long-Term Care Facilities: A Reservoir for Vancomycin-Resistant Enterococci. Clin. Infect. Dis. 2002,34, 441–446. [CrossRef] 128. Padiglione, A.A.; Grabsch, E.; Wolfe, R.; Gibson, K.; Grayson, M.L. The Prevalence of Fecal Colonization With VRE Among Residents of Long-Term—Care Facilities in Melbourne, Australia. Infect. Control Hosp. Epidemiol. 2001 ,22, 576–578. [CrossRef] [PubMed] 129. Silverblatt, F.J.; Tibert, C.; Mikolich, D.; Blazek-D’Arezzo, J.; Alves, J.; Tack, M.; Agatiello, P. Preventing the Spread of Vancomycin- Resistant Enterococci in a Long-Term Care Facility. J. Am. Geriatr. Soc. 2000,48, 1211–1215. [CrossRef] 130. Cunha, C.; Kassakian, S.Z.; Chan, R.; Tenover, F.C.; Ziakas, P.; Chapin, K.C.; Mermel, L.A. Screening of nursing home residents for colonization with carbapenem-resistant Enterobacteriaceae admitted to acute care hospitals: Incidence and risk factors. Am. J. Infect. Control. 2016,44, 126–130. [CrossRef] 131. Prasad, N.; Labaze, G.; Kopacz, J.; Chwa, S.; Platis, D.; Pan, C.X.; Russo, D.; LaBombardi, V.J.; Osorio, G.; Pollack, S.; et al. Asymptomatic rectal colonization with carbapenem-resistant Enterobacteriaceae and Clostridium difficile among residents of a long-term care facility in New York City. Am. J. Infect. Control. 2016,44, 525–532. [CrossRef] 132. Ben-David, D.; Masarwa, S.; Navon-Venezia, S.; Mishali, H.; Fridental, I.; Rubinovitch, B.; Smollan, G.; Carmeli, Y.; Schwaber, M.J.; Israel PACF CRKP (Post-Acute-Care Facility Carbapenem-Resistant Klebsiella pneumoniae) Working Group. Carbapenem- Resistant Klebsiella pneumoniaein Post-Acute-Care Facilities in Israel. Infect. Control Hosp. Epidemiol. 2011 ,32, 845–853. [CrossRef] [PubMed] 133. Prabaker, K.; Lin, M.Y.; McNally, M.; Cherabuddi, K.; Ahmed, S.; Norris, A.; Lolans, K.; Odeh, R.; Chundi, V.; Weinstein, R.A.; et al. Transfer from High-Acuity Long-Term Care Facilities Is Associated with Carriage ofKlebsiella pneumoniaeCarbapenemase– ProducingEnterobacteriaceae: A Multihospital Study. Infect. Control Hosp. Epidemiol. 2012,33, 1193–1199. [CrossRef] 134. Reuben, J.; Donegan, N.; Wortmann, G.; DeBiasi, R.; Song, X.; Kumar, P.; McFadden, M.; Clagon, S.; Mirdamadi, J.; White, D.; et al. Healthcare Antibiotic Resistance Prevalence—DC (HARP-DC): A Regional Prevalence Assessment of Carbapenem-Resistant Enterobacteriaceae (CRE) in Healthcare Facilities in Washington, District of Columbia. Infect. Control Hosp. Epidemiol. 2017 ,38, 921–929. [CrossRef] [PubMed] 135. Leitner, E.; Schreiner, E.; Neuhold, M.; Bozic, M.; Pux, C.; Pichler, G.; Schippinger, W.; Steinmetz, I.; Krause, R.; Zollner-Schwetz, I. Low prevalence of Clostridium difficile colonization in patients in long-term care facilities in Graz, Austria: A point-prevalence study. Am. J. Infect. Control. 2020,48, 1144–1147. [CrossRef] [PubMed] 136. Rodriguez, C.; Taminiau, B.; Korsak, N.; Avesani, V.; Van Broeck, J.; Brach, P.; Delmée, M.; Daube, G. Longitudinal survey of Clostridium difficile presence and gut microbiota composition in a Belgian nursing home. BMC Microbiol. 2016 ,16, 1–12. [CrossRef] [PubMed] 137. Walker, K.J.; Gilliland, S.S.; Vance-Bryan, K.; Moody, J.A.; Larsson, A.J.; Rotschafer, J.C.; Guay, D.R.P. Clostridium difficileColonization in Residents of Long-Term Care Facilities: Prevalence and Risk Factors. J. Am. Geriatr. Soc. 1993 ,41, 940–946. [CrossRef] [PubMed] 138. Thomas, D.R.; Bennett, R.G.; Laughon, B.E.; Iii, W.B.G.; Bartlett, J.G. Postantibiotic Colonization withClostridium difficilein Nursing Home Patients. J. Am. Geriatr. Soc. 1990,38, 415–420. [CrossRef] [PubMed] 139. Riggs, M.M.; Sethi, A.K.; Zabarsky, T.F.; Eckstein, E.C.; Jump, R.L.P.; Donskey, C.J. Asymptomatic Carriers Are a Potential Source for Transmission of Epidemic and Nonepidemic Clostridium difficile Strains among Long-Term Care Facility Residents. Clin. Infect. Dis. 2007,45, 992–998. [CrossRef] Antibiotics 2021,10, 680 22 of 22 140. Arvand, M.; Moser, V.; Schwehn, C.; Bettge-Weller, G.; Hensgens, M.P.; Kuijper, E.J. High Prevalence of Clostridium difficile Colonization among Nursing Home Residents in Hesse, Germany. PLoS ONE 2012,7, e30183. [CrossRef] 141. Mortensen, E.; Trivedi, K.K.; Rosenberg, J.; Cody, S.H.; Long, J.; Jensen, B.J.; Vugia, D.J. Multidrug-Resistant Acinetobacter baumannii Infection, Colonization, and Transmission Related to a Long-Term Care Facility Providing Subacute Care. Infect. Control Hosp. Epidemiol. 2014,35, 406–411. [CrossRef] [PubMed] 142. O’Fallon, E.; Kandell, R.; Schreiber, R.; D’Agata, E.M.C. Acquisition of Multidrug-Resistant Gram-Negative Bacteria: Incidence and Risk Factors within a Long-Term Care Population. Infect. Control Hosp. Epidemiol. 2010 ,31, 1148–1153. [CrossRef] [PubMed] 143. Kahvecioglu, D.; Ramiah, K.; Mcmaughan, D.; Garfinkel, S.; McSorley, V.; Nguyen, Q.N.; Yang, M.; Pugliese, C.; Mehr, D.; Phillips, C.D. Multidrug-Resistant Organism Infections in US Nursing Homes: A National Study of Prevalence, Onset, and Transmission across Care Settings, October 1, 2010-December 31, 2011. Infect. Control Hosp. Epidemiol. 2014 ,35, S48–S55. [CrossRef] [PubMed] 144. D’Agata, E.M.C.; Habtemariam, D.; Mitchell, S. Multidrug-Resistant Gram-Negative Bacteria: Inter- and Intradissemination Among Nursing Homes of Residents With Advanced Dementia. Infect. Control Hosp. Epidemiol. 2015,36, 930–935. [CrossRef] 145. Mody, L.; Krein, S.L.; Saint, S.K.; Min, L.C.; Montoya, A.; Lansing, B.; McNamara, S.E.; Symons, K.; Fisch, J.; Koo, E.; et al. A Targeted Infection Prevention Intervention in Nursing Home Residents With Indwelling Devices. JAMA Intern. Med. 2015 ,175, 714–723. [CrossRef] [PubMed] 146. Ziakas, P.D.; Zacharioudakis, I.M.; Zervou, F.N.; Grigoras, C.; Pliakos, E.E.; Mylonakis, E. Asymptomatic Carriers of Toxigenic C. difficile in Long-Term Care Facilities: A Meta-Analysis of Prevalence and Risk Factors. PLoS ONE 2015 ,10, e0117195. [CrossRef] 147. Donskey, C.J.; Kundrapu, S.; Deshpande, A. Colonization Versus Carriage of Clostridium difficile. Infect. Dis. Clin. N. Am. 2015 , 29, 13–28. [CrossRef] [PubMed] 148. Simor, A.E.; Bradley, S.F.; Strausbaugh, L.J.; Crossley, K.; Nicolle, L.E. SHEA Long-Term–Care Committee Clostridium difficilein Long-Term–Care Facilities for the Elderly. Infect. Control Hosp. Epidemiol. 2002,23, 696–703. [CrossRef] 149. Thompson, G.; Shindruk, C.L.; Adekoya, A.A.; Demczuk, L.; McClement, S. Meanings of ‘centredness’ in long-term care facilities: A scoping review protocol. BMJ Open 2018,8, e022498. [CrossRef]