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The global prevalence of methicillin-resistant Staphylococcus aureus colonization in residents of elderly care centers: a systematic review and meta-analysis

The global prevalence of methicillin-resistant Staphylococcus aureus colonization in residents of... Background Methicillin-resistant Staphylococcus aureus (MRSA) is a difficult to treat infection, particularly in residents of elderly care centers (ECCs). Despite the substantial burden of MRSA, an inadequate number of studies have ana- lyzed MRSA prevalence in ECCs. Objectives We conducted a worldwide systematic review and meta-analysis on the prevalence and risk factors of MRSA in ECCs. Methods We searched MEDLINE/PubMed, EMBASE, Web of Science, and Scopus databases and the gray literature sources for all studies published between January 1980 and December 2022 on the prevalence of MRSA in ECCs. A random-effects model was utilized to estimate pooled prevalence rates at 95% confidence intervals (CI). Moreover, the data were analyzed based on World Health Organization-defined regions, income, and human development index levels. Results In total, 119 studies, including 164,717 participants from 29 countries, were found eligible for meta-analysis. The pooled global prevalence of MRSA was 14.69% (95% CI 12.39–17.15%; 16,793/164,717). Male gender [prevalence ratio (PR) = 1.55; 95% CI 1.47–1.64], previous MRSA infection (PR = 3.71; 95% CI 3.44–4.01), prior use of antibiotics (PR = 1.97; 95% CI 1.83–2.12), hospitalized within the previous year (PR = 1.32; 95% CI 1.20–1.45), have had any wound (PR = 2.38; 95% CI 2.23–2.55), have used urinary catheter (PR = 2.24; 95% CI 2.06–2.43), have used any medical device (PR = 1.78; 95% CI 1.66–1.91), and those with diabetes (PR = 1.55; CI 1.43–1.67) were more likely to be colonized by MRSA than other patients. Conclusion Screening programs and preventive measures should target MRSA in ECCs due to the high global preva- lence rates. Keywords Methicillin-resistant Staphylococcus aureus, Residential facilities, Nursing homes, Long-term care, Systematic review *Correspondence: Ali Rostami alirostami1984@gmail.com Full list of author information is available at the end of the article © The Author(s) 2023. Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article’s Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http:// creat iveco mmons. org/ licen ses/ by/4. 0/. The Creative Commons Public Domain Dedication waiver (http:// creat iveco mmons. org/ publi cdoma in/ zero/1. 0/) applies to the data made available in this article, unless otherwise stated in a credit line to the data. Hasanpour et al. Antimicrobial Resistance & Infection Control (2023) 12:4 Page 2 of 11 determinants of MRSA colonization in the elderly living Background in ECCs. The improvement of lifestyle and medical care, and declining birth rates in recent decades, have led to a rapid Methods increase in life expectancy and the mean age of the popu- We followed the Preferred Reporting Items for Systematic lation, especially in developed countries [1]. According Reviews and Meta-analyses (PRISMA) guidelines to per- to the World Health Organization (WHO) report, by form and report this systematic review and meta-analysis 2050, it is estimated that almost more than a quarter of [20] and registered it in PROSPERO (CRD42021291492). the world’s population will be over 60  years old [2]. The number of elderly is expected to reach 1.4 billion by 2030 Data source and searching strategies and 2.1 billion by 2050 [3, 4]. It is evident that a consid- Two authors (A.H.H and A.A.) independently searched erable portion of seniors will need intensive care, while MEDLINE/PubMed, EMBASE, Web of Science col- the majority of them merely need daycare facilities [5, 6]. lection, and Scopus databases on December 20, 2021, Therefore, the exponential need for institutions providing for articles published since January 1, 1980. The search long-term care facilities, nursing homes, and residential was updated for twice; first, on February 15, 2022, and care homes (all defined as elderly care centers (ECCs) in second, on December 15, 2022. Moreover, grey litera- this study) is anticipated [7]. ture was searched through manual inspections of bibli- Multidrug-resistant organisms (MDROs) are among ographies of retrieved studies and internet searches of the leading causes of morbidity and mortality in ECCs Google and Google Scholar. We applied the following [8, 9]. Elderly at ECCs are prone to colonization/infec- search terms: [(“Staphylococcus aureus” OR "methicil- tion with MDROs mainly due to age-associated mor- lin resistant Staphylococcus aureus" OR "MRSA" OR bidities (i.e., cognitive disorders), perpetual living in a "multidrug-resistant organisms" OR "methicillin resist- confined and crowded area, prolonged and recurrent use ance" OR “antibiotic-resistant infections” OR “antibiotic- of broad-spectrum antibiotics, and frequent referral to resistant bacteria”) AND ("old age homes" OR "Nursing and from acute-care hospitals [10–12]. One of the most Homes" OR "homes for the aged" OR "residential facili- prevalent MDROs in ECCs is methicillin-resistant Staph- ties" OR “Residential Care Homes” OR "housing for the ylococcus aureus (MRSA) [8, 13, 14]. MRSA is a global elderly" OR "Long term care facility") AND (“preva- health-threatening organism in healthcare settings, as lence” OR “epidemiology” OR “incidence”)] (Additional it is resistant to antibiotics making the treatment more file  1: Fig. S1). The search syntax was modified accord - complex [15]. MRSA infection could be responsible for ing to the properties of each database. We included stud- fatal sepsis, pneumonia, and higher rates of myocardial ies in all languages, and those with languages unknown infarction and heart failure in patients with bacteremia to the study team were translated into English using the [16]. A national cohort study conducted in the United “Google Translate” online tool. All articles were imported States indicated that MRSA colonization among commu- into EndNote reference manager software X8 (Thomp - nity adults aged 40–85 is associated with a significantly son and Reuters, Philadelphia, USA), and duplicates were increased mortality risk (hazard ratio, 1.75; 95% CI 1.12– removed. 2.73) [17]. Additionally, the attributable cost of MRSA among hospitalized individuals (≥ 65  years) is estimated Inclusion and exclusion criteria to be 22,293 $ per patient (95% CI 19,101–24,485$) in Two authors (A.H.H. and M.A.) independently screened the United States [18]. Another cohort study in Chinese titles and abstracts of retrieved citations to identify eli- nursing homes showed that MRSA colonization was an gible studies that met the following inclusion criteria: independent risk factor for 2 year infection-related mor- (i) presented data on prevalence or incidence of MRSA tality (hazard ratio, 1.96; 95% CI 1.01–3.78) [19]. in ECCs; (ii) reported data on the elderly (minimum age Considering the significant toll of MRSA, monitor - wasn’t specified, we accepted definition of the included ing the extent of colonization, and identifying the key studies for elderlies in ECCs); (iii) included at least 30 risk factors of MRSA acquisition in ECCs is essential tested elderlies. Only the last report was included in for controlling and reducing the burden of this disease multiple sequential articles that were generated from in ECCs residents. In the past years, a growing body of the same data set (e.g., cohort studies). In clinical trials, epidemiological literature evaluated the prevalence rate we only extracted baseline data. Articles were excluded of MRSA colonization in ECCs from various countries; if they were (i) performed only on MRSA patients; (ii) nevertheless, there is no comprehensive study to estimate performed on elderly in community or hospitals; (iii) global and regional prevalence rates. To bridge this gap, included only a specific group of elderly with a specific we performed a systematic review and meta-analysis to disease or situation; (iv) used datasets that overlapped evaluate the worldwide prevalence and identify potential Hasanpour  et al. Antimicrobial Resistance & Infection Control (2023) 12:4 Page 3 of 11 with other articles; (v) studies following the MRSA out- were no group comparisons or hypothesis tests of “treat- breaks in ECCs; (vi) case series, case reports, and arti- ment effect” [30]. cles without original data such as reviews or systematic We performed subgroup and meta-regression analysis reviews, comments, editorials, and corresponding letters. to identify sources of heterogeneity, determine the risk factors and the effects of socio-demographic factors on Data extraction and quality assessment prevalence rates. Subgroup analyses were undertaken After screening the articles, the required data from each according to WHO-defined regions, income and HDI eligible study were extracted and imported into a stand- levels, type of diagnostic methods, risk of bias, and key ardized Microsoft Excel spreadsheet (version 2016; determinants. Corresponding prevalence ratios (PRs) Microsoft Corporation, Redmond, USA). The follow - were estimated for variables subjected to subgroup analy- ing data were extracted from each study: name of the sis. Meta-regressions were performed on publication first author, year of publication, start and end year of year, sample size, income and HDI levels. study, country, type of ECCs, study design, body sam- pling sites, diagnostic methods for MRSA detection, age Results (mean and range) of tested elderlies, the total number Characteristics of the included studies of tested participants, the total number of participants As outlined in Fig. 1, a total of 4472 articles were identi- tested positive for Staphylococcus aureus, methicillin- fied in our initial literature search, of these 118 articles sensitive Staphylococcus aureus (MSSA), and MRSA. We (119 studies) involving 164,717 participants from 29 stratified countries according to WHO-defined regions countries were included in the meta-analysis. The main [17], World Bank’s income category [21], gross national characteristics of the included studies are shown in Addi- income per capita [22], and the human development tional file  1: Table  S1. Studies included were published index (HDI) [23]. Furthermore, to evaluate the main risk between 1990 and 2022. Twenty-six studies had data to factors of MRSA prevalence, we extracted data (if avail- determine the proportion of MRSA and MSSA. Over- able in individual studies) of gender, prior antibiotics use, all, eligible studies were available for five WHO-defined prior MRSA infection, prior hospitalization, having any regions; 65 studies were from European region, 34 from wound, urinary catheter, use of any medical device, dia- the region of the Americas, 18 studies from the Western betes, antacid use, and dementia. To conduct the quality Pacific region, and one study for each of the Eastern Med - assessment and the risk of bias in included studies, we iterranean and African regions. Countries with the most used the Joanna Briggs Institute (JBI) Critical Appraisal eligible studies were the United States (31 studies), China Checklist for studies that reported prevalence data [24]. (12 studies), Germany (10 studies), the United Kingdom The detailed items of JBI tools are presented in Addi - (eight studies), and Italy (six studies). Regarding study tional file 1: Table S1. designs, 88 studies were cross-sectional, 21 studies were prospective cohort, seven studies were randomized con- Data synthesis and statistical analysis trolled trial (RCT), and three studies were case control. Stata software version 16.0 (STATA Corp., College Sta- Regarding the location of studies, 71, 41, and 7 studies tion, Texas, USA) was used to perform the meta-analyses. were performed in nursing homes, long-term care facili- Before pooling prevalence estimates, the variance of the ties, and residential care homes, respectively. Consider- raw prevalence from each included study was stabilized ing the risk of bias, 68 and 51 studies were determined by using the Freeman-Tukey double arc-sine transforma- as the low and moderate risk of biases. All studies used tion [25]. The Cochran’s Q test and I index were used to culture-based methods to determine the MRSA preva- calculate the between-studies heterogeneity [23, 26]. A lence, and 54 performed further analyses using molecular P-value < 0.01 for the Cochran’s Q test and an I of > 75% methods. Additional information is presented in Tables 1 are considered as significant and high heterogeneity, and 2. respectively [23, 26, 27]. DerSimonian and Laird random- effects model (REM) was used in case of high heteroge - Prevalence of MRSA colonization in ECCs neity, to conservatively estimate the pooled prevalence Table  2 presents the national and regional pooled of MRSA at 95% confidence intervals (CIs) [25, 28]. We prevalence of MRSA in residents of ECCs. The pooled estimated the prevalence in individual countries by syn- global prevalence was 14.69% (95% CI 12.39–17.15%; thesizing the prevalence rates of all studies from the same 16,793/164,717) by using REM, with high heterogeneity country. Further, we calculated the prevalence rates of across 119 studies (χ2 = 18,637.54, P < 0.001, I = 99.3%). MRSA for the WHO-defined regions by synthesizing the According to WHO-defined regions, pooled prevalence data for countries within the same region [29]. We did rates (at 95% CI) were: 22.27% (15.56–29.79%) in the not assess publication bias, as in prevalence studies, there region of the Americas, 16.57% (11.70–22.10%) in the Hasanpour et al. Antimicrobial Resistance & Infection Control (2023) 12:4 Page 4 of 11 Fig. 1 The PRISMA diagram of the study selection Western Pacific, 10.93% (8.56–13.55%) in Europe. Only prevalence rates of MRSA were 16.29% (12.29–20.71%), one study was available for each of the Eastern Mediter- 14.35% (11.50–17.44%), and 9.85% (3.62–17.93%) for the ranean and African regions, indicating prevalence rates elderly living in long-term care facilities, nursing homes, of 8.55% (4.63–14.18%) and 9.04% (5.36–14.08%), respec- and residential care homes, respectively. Considering tively. For countries with two or more available stud- study designs, the lowest and highest prevalence rates ies, United States (23.78%), Singapore (22.72%), Poland were observed in studies with cross-sectional (13.37%, (22.18%), United Kingdom (18.66%), China (18.07%), 10.68–16.30%) and RCT (20.15%, 12.55–29.01%) designs, Italy (16.34%), Spain (15.45%), Israel (14.82%), France respectively. Studies published after year of 2000 showed (13.89%) and Switzerland (13.15%) exhibited almost the non-significant increasing prevalence rates (C = 0.001; highest prevalence rates (Fig.  2). Analyzing the data on P = 0.547) (Table  2 and Fig.  3C). Studies with low risk of the proportion of MRSA and MSSA in 26 studies using bias (13.06%, 10.26–16.15%) showed lower prevalence REM showed that 26% (18–36%) of all S. aureus isolates rates than those with moderate risk of bias (17.11%, were MRSA (Additional file 1: Fig. S2A). 13.64–20.87%) (Table 2). Subgroup analyses of income and HDI levels yielded relatively similar results; prevalence rate for countries Risk factors associated with MRSA colonization in residents with upper-middle income and high HDI levels was of ECCs 16.5%, and for countries with high income and very high The analyses of key determinants of MRSA coloniza - HDI levels was 14.4% (see Table 2). Meta-regression anal- tion in elderly living in ECCs showed that MRSA is yses indicated a non-significant increasing trend in prev - more colonized in males than females (PR = 1.55; 95% CI alence with higher income [coefficient (C) = 0.000001; 1.47–1.64). With regard to other risk factors, we found P = 0.259], and HDI values (C = -0.117; P = 0.573) that elderly with a previous history of MRSA infection (Fig.  3A, B). According to the type of ECCs, pooled (PR = 3.71; 95% CI 3.44–4.01), prior use of antibiotics Hasanpour  et al. Antimicrobial Resistance & Infection Control (2023) 12:4 Page 5 of 11 Table 1 Global and regional pooled prevalence rates of MRSA among elderly living in ECCs; results from 119 studies performed in 30 countries WHO regions*/country Number of Number of individuals Number of individuals Pooled prevalence % (95% CI) datasets screened (total) with MRSA Global 119 164,717 16,793 14.69 (12.39–17.15) Americas 34 86,065 7508 22.27 (15.56–29.79) United States 31 21,457 5517 23.78 (19.12–28.77) Brazil 2 526 71 13.11 (10.34–16.14) Canada 1 64,082 1920 3.01 (2.87–3.13) Western Pacific Region 18 15,419 2936 16.57 (11.70–22.10) China 12 11,337 2101 18.07 (11.18–26.17) Japan 3 354 32 8.81 (5.99–12.08) Singapore 2 3613 785 21.72 (20.39–23.08) Australia 1 115 18 15.65 (9.55–23.60) European region 65 62,893 6319 10.93 (8.56–13.55) Germany 10 10,857 432 4.67 (2.59–7.29) United Kingdom 8 8633 2037 18.66 (12.07–26.28) Belgium 7 13,508 1403 8.97 (4.94–14.03) Italy 6 1710 246 16.34 (10.23–23.52) Spain 5 2700 460 15.45 (9.50–22.52) Sweden 4 1122 139 4.52 (0.01–33.07) Netherlands 3 5841 261 6.63 (0.01–35.64) France 3 1500 121 13.89 (3.70–29.01) Israel 3 545 68 14.82 (5.28–27.95) Switzerland 3 12,128 805 13.15 (7.08–20.70) Finland 1 213 2 0.94 (0.11–3.35) Ireland 2 818 82 9.46 (7.51–11.61) Poland 2 248 61 22.18 (17.16–27.62) Slovenia 2 209 22 10.50 (6.62–15.09) Greece 1 227 33 14.54 (10.22–19.81) Croatia 1 877 62 7.07 (5.46–8.97) Georgia 1 56 8 14.29 (6.38–26.22) Austria 1 500 0 0.01 (0.00–0.74) Luxembourg 1 954 69 7.23 (5.67–9.06) Turkey 1 247 8 3.24 (1.41–6.28) African region 1 152 13 8.55 (4.63–14.18) South Africa 1 152 13 8.55 (4.63–14.18) Eastern Mediterranean 1 188 17 9.04 (5.36–14.08) Saudi Arabia 1 188 17 9.04 (5.36–14.08) *The WHO regions are sorted based on prevalence rates, and countries are sorted based on the number of datasets colonization (P-value > 0.05). More information is pre- (PR = 1.97; 95% CI 1.83–2.12), history of hospitalization sented in Table 3. within the previous year (PR = 1.32; 95% CI 1.20–1.45), those with any wound (PR = 2.38; 95% CI 2.23–2.55), those who have used urinary catheter (PR = 2.24; 95% Discussion CI 2.06–2.43), those who have used any medical device MRSA infection continues to sustain as a major public (PR = 1.78; 95% CI 1.66–1.91), and those with diabe- health threat worldwide, especially in the elderly. In the tes (PR = 1.55; 95% CI 1.43–1.67) were more likely to be present study, for the first time, we assembled data from colonized by MRSA than other patients (Table  3). Other all available studies (over 40 years) that had reported the risk factors such as antacid use and dementia were not prevalence of MRSA in ECCs. Among the key findings significantly associated with an increased risk of MRSA was the high pooled prevalence of MRSA colonization Hasanpour et al. Antimicrobial Resistance & Infection Control (2023) 12:4 Page 6 of 11 Table 2 Prevalence estimates for the MRSA in the elderly, according to the study characteristics and socio-demographic factors Variable subgroup Number of Number of elderlies Number of elderlies Pooled prevalence % (95% CI) datasets screened (total) with MRSA Income Upper middle 16 12,071 2193 16.46 (10.79–23.05) High 103 152,646 14,600 14.42 (11.98–17.04) HDI High 15 12,015 2185 16.60 (10.74–23.42) Very high 104 152,702 14,608 14.42 (11.99–17.02) Type of setting Long-term care facilities 41 88,088 5069 16.29 (12.29–20.71) Nursing homes 71 69,652 10,730 14.35 (11.50–17.44) Residential care homes 7 6977 994 9.58 (3.62–17.93) Study design Cross-sectional 88 135,275 12,969 13.37 (10.68–16.30) Prospective cohort 21 23,022 2756 17.90 (12.66–23.82) Case–control 3 312 73 21.03 (3.67–46.99) RCT 7 6108 995 20.15 (12.55–29.01) Publication year Before 2000 14 3505 441 12.84 (9.24–16.93) 2001–2010 27 33,541 4365 16.12 (11.43–21.44) 2011–2022 78 127,671 11,987 14.53 (11.58–17.75) Risk of bias Low 68 151,473 14,489 13.06 (10.26–16.15) Moderate 51 13,244 2304 17.11 (13.64–20.87) Fig. 2 Worldwide distribution of MRSA colonization in ECCs Hasanpour  et al. Antimicrobial Resistance & Infection Control (2023) 12:4 Page 7 of 11 Fig. 3 Meta-regression analyses of MRSA prevalence among elderly living in ECCs concerning A Country’s gross national income per capita, B HDI level and C Publication year Table 3 Risk factors associated with MRSA colonization in elderly living in ECCs Variable subgroup Number of Number of elderlies Number of Pooled prevalence % (95% CI) Prevalence ratio (95% CI) datasets screened (total) elderlies with MRSA Gender Male 32 9149 2164 18.41 (13.14–24.30) 1.55 (1.47–1.64) Female 32 15,572 2387 15.18 (10.81–20.12) 1 Prior antibiotics use Yes 21 6746 1450 24.59 (17.82–32.03) 1.97 (1.83–2.12) No 21 9492 1031 13.61 (9.67–18.09) 1 Prior MRSA infection Yes 11 1430 669 49.86 (35.87–63.86) 3.71 (3.44–4.01) No 11 10,044 1264 17.76 (11.25–25.37) 1 Hospitalization in past year Yes 19 3149 559 21.34 (14.30–29.29) 1.32 (1.20–1.45) No 18 6907 926 16.90 (10.99–23.76) 1 Any wound Yes 24 4003 1056 27.03 (19.62–35.10) 2.38 (2.23–2.55) No 24 15,439 1706 12.41 (9.01–16.27) 1 Urinary catheter Yes 20 2949 661 19.59 (14.72–24.93) 2.24 (2.06–2.43) No 20 15,656 1565 10.86 (7.44–14.83) 1 Any device Yes 16 5413 1274 30.09 (19.43–41.85) 1.78 (1.66–1.91) No 16 9715 1279 16.07 (10.97–21.91) 1 Diabetes Yes 19 4990 870 17.11 (11.48–23.52) 1.55 (1.43–1.67) No 19 13,734 1543 14.74 (9.69–20.60) 1 Antacid use Yes 3 1364 72 8.95 (1.98–19.36) 1.02 (0.76–1.38) No 3 1966 101 5.01 (4.06–6.03) 1 Dementia Yes 5 1792 325 15.93 (7.93–25.97) 1.04 (0.93–1.17) No 5 5243 994 15.08 (9.36–21.84) 1 in the residents of ECCs (14.69%, 12.39–17.15%); which Furthermore, the estimated colonization rate in our is over tenfold higher than the MRSA colonization rate study is higher than those reported from other high- among the general community (1.3%, 1.04–1.53%) [31]. risk groups such as HIV + patients (7.0%, 5.0–9.0%) [32], Hasanpour et al. Antimicrobial Resistance & Infection Control (2023) 12:4 Page 8 of 11 hemodialysis patients (6.2%, 4.2–8.5%) [33], and patients environment are scarce [9]. Excessive use of antibiotics admitted to intensive care units (7.0%, 5.8–8.3%) [34]. is one contributing factor to the increase in antibiotic This highlights that elderly residents of ECCs are at very resistance and the growth in the emergence of MDROs, high risk for MRSA colonization, maybe due to cross- which should be addressed in ECCs. transmission between the elderlies in the crowded situa- Our findings identified several risk factors for MRSA tion of ECCs or introduction of infection when admitting colonization in residents of ECCs, such as being male, new elders from outside of ECCs (i.e., hospitals or com- prior antibiotics use, previous MRSA infection, hospitali- munity) [35]. Other possible explanations for this high zation in the past 12 months, presence of any wound, uri- prevalence of MRSA could be frailty, impaired immune nary catheter, usage of any invasive medical device, and system function, frequent hospitalization, and overuse diabetes. Our findings are consistent with several studies of antibiotics [36, 37]. All the above-mentioned reasons about the MRSA prevalence in the community or high- underline the significance of recognizing contributing risk populations such as HIV + and hemodialysis patients factors, and treating MRSA to reduce and prevent the [2, 31–33, 45, 46]. Although there is no consensus on the spread of the disease. role of gender in the prevalence of MRSA, it has been Our results showed that the geographic distribution asserted that elderly males are more prone to the other of MRSA colonization is heterogeneous, with the high- predisposing factors of being infected with MRSA namely est and lowest colonization rates reported in countries in more complicated diabetes and wounds, frequent use of regions of the Americas (22.27%) and Europe (10.93%), medical devices, and catheterization which may lead to a respectively. This finding is in accordance with previ - higher prevalence MRSA [47, 48]. Furthermore, frequent ous meta-analysis studies in other high-risk populations use of antibiotics is one of the main cause for the devel- [32–34]. Spatial variations of MRSA prevalence could opment of antimicrobial resistance in staphylococci and be explained by differences in numerous demographic other bacteria [46, 49]. A previous MRSA infection could information among the countries studied and different lead to re-infection secondary to a lack of proper eradi- ECCs in a country such as policies for prescription of cation or stable colonization [45]. The constant presence antibiotics, various infection prevention programs, dif- of high-risk individuals in hospitals and routine antibiot- ferent education and training of staff and elderly for per - ics use justify the higher prevalence of MRSA in elders sonal hygiene, different structure of health care systems, who were hospitalized in the last 12 months [34]. Medi- and facilities for MRSA diagnosis [32, 38–41]. Our study cal devices make patients susceptible to MRSA through also highlighted a significant data gap in less developed the mechanism of biofilm formation on the devices and countries, most strikingly in Latin America, Africa, East- subsequent detachment, which may contribute to bac- ern Mediterranean, Central Asia, and South-East of Asia teremia or sepsis [50]. A wide range of chronic diseases regions, where more data are required to obtain accu- like diabetes renders the patients prone to MRSA given rate estimates of the prevalence of MRSA colonization in the state of immunosuppression and more complicated elderly residents of ECCs. It should be noted that under- wounds [51, 52]. Similar to our findings, chronic illnesses, developed or developing countries may not have well- intravenous drug use, and contact with infected individu- established elderly care systems or antibiotic stewardship als are reported as risk factors for community-acquired programs. Due to the increasing number of ECCs in MRSA [31]. These findings have implications for policy - developing countries [42], these information gaps should makers in identifying high-risk groups to reduce the dis- be addressed through future representative epidemiolog- ease burden by employing targeted interventions. ical studies. Our findings in this comprehensive systematic Our findings suggested different prevalence rates of review and meta-analysis have implications for future MRSA colonization in nursing homes (14.35%), long- research and clinical practices. However, this study has term care facilities (16.29%), and residential care homes identified several shortcomings of the current data on (9.58%). The discrepancies in prevalence rates between MRSA colonization among the elderly in ECCs. First, different types of ECCs may stem from the differences our study contains reports from only 30 of ~ 200 coun- in services rendered by each type of center. In nursing tries globally; there were no country-level estimates for homes, patients usually receive daily or constant profes- some countries, and no prevalence data were available sional nursing care, and antibiotics can be prescribed from many countries. In addition, most of the available with the consultation of a physician [43], therefore, studies had a paucity of data on critical variables such antimicrobial overuse/abuse is prevalent [43]. In con- as gender, age, ethnicity, and risk factors associated trast, residential care centers are mostly restricted to with MRSA colonization. Therefore, some non-signif - personal care [44]. Despite monitoring schemes in hos- icant results considering risk factors might be due to pitals for antibiotic use, records for the nursing homes the low number of studies. For example, while among Hasanpour  et al. Antimicrobial Resistance & Infection Control (2023) 12:4 Page 9 of 11 Author contributions those who took antacids (as shown in Table  3) almost AHH and AR conceived the study. AHH, AR, MA, AA, AM and SRH conducted double MRSA (8.95%) has been estimated, the preva- the searches, and collected data. AHH, MS, MA, AM and MJ analysed the data lence ratio was non-significant. Second, the studies sets and interpreted the results. AHH, AM, AA, MB and AR drafted and edited the manuscript. All authors commented on, or edited, drafts and approved included had different qualities and studies with lower the final version of the manuscript. qualities (17.11%) showed higher colonization rates than high quality studies (13.06%) which highlight the Funding No funding. need for more robust surveys of MRSA colonization in residents of ECCs. Third, as expected in meta-anal - Availability of data and materials yses on prevalence studies [25, 29, 53–55], a substan- The data that support the findings of this study are available from the cor - responding author upon reasonable request. tial heterogeneity was found in our analyses that could not be explained by subgroup analyses. The sources of Declarations heterogeneity are likely related to study characteris- tics, including differences in geographical distribution, Ethics approval and consent to participate study design, sample size, diagnostic methods, leading Not applicable. to differences in the quality and performance of these Consent for publication methods. Moreover, this heterogeneity suggests that Not applicable. local risk factors and transmission routes of MRSA are Competing interests varied in different geographical regions, countries, or The authors declare that they have no competing interests. even in individual ECCs. Author details Student Research Committee, Babol University of Medical Sciences, Babol, Iran. Department of Biostatistics and Epidemiology, School of Public Health, Conclusion Babol University of Medical Sciences, Babol, Iran. Department of Public In conclusion, this study found that the prevalence of Health and Prevention Science, School of Health Sciences, Baldwin Wallace University, Berea, OH, USA. School of Medicine, Shiraz University of Medical MRSA colonization in residents of ECCs is high across 5 6 Sciences, Shiraz, Iran. Harlem Medical Center, Bridgeview, IL, USA. Depar t- the world and varies by gender and geographic location. ment of Hematopoietic Biology and Malignancy, The University of Texas Md Moreover, elders with previous MRSA infection, hospi- Anderson Cancer Center, Houston, TX, USA. Social Determinants of Health Research Center, Health Research Institute, Babol University of Medical Sci- talization, antibiotics and diabetes, and those that used ences, Babol, Iran. Infectious Diseases and Tropical Medicine Research Center, medical devices are more prone to MRSA colonization. Health Research Institute, Babol University of Medical Sciences, Babol, Iran. This sheds significant light on the essence of targeted Received: 12 April 2022 Accepted: 21 January 2023 interventions and screening programs to locate infected people, control risk factors, and reduce the transmis- sion of MRSA and other MDROs to elderlies living in ECCs. Given the aging trend of the populations, there References is an urgent need for studies, particularly in developing 1. Suzman R, Beard JR, Boerma T, Chatterji S. Health in an ageing world— and underdeveloped countries to better estimate the what do we know? Lancet. 2015;385(9967):484–6. 2. Wong JW, Ip M, Tang A, Wei VW, Wong SY, Riley S, Read JM, Kwok KO. risk of disease. We recommend several interventions Prevalence and risk factors of community-associated methicillin- to reduce the MRSA burden in ECCS. 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The global prevalence of methicillin-resistant Staphylococcus aureus colonization in residents of elderly care centers: a systematic review and meta-analysis

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Abstract

Background Methicillin-resistant Staphylococcus aureus (MRSA) is a difficult to treat infection, particularly in residents of elderly care centers (ECCs). Despite the substantial burden of MRSA, an inadequate number of studies have ana- lyzed MRSA prevalence in ECCs. Objectives We conducted a worldwide systematic review and meta-analysis on the prevalence and risk factors of MRSA in ECCs. Methods We searched MEDLINE/PubMed, EMBASE, Web of Science, and Scopus databases and the gray literature sources for all studies published between January 1980 and December 2022 on the prevalence of MRSA in ECCs. A random-effects model was utilized to estimate pooled prevalence rates at 95% confidence intervals (CI). Moreover, the data were analyzed based on World Health Organization-defined regions, income, and human development index levels. Results In total, 119 studies, including 164,717 participants from 29 countries, were found eligible for meta-analysis. The pooled global prevalence of MRSA was 14.69% (95% CI 12.39–17.15%; 16,793/164,717). Male gender [prevalence ratio (PR) = 1.55; 95% CI 1.47–1.64], previous MRSA infection (PR = 3.71; 95% CI 3.44–4.01), prior use of antibiotics (PR = 1.97; 95% CI 1.83–2.12), hospitalized within the previous year (PR = 1.32; 95% CI 1.20–1.45), have had any wound (PR = 2.38; 95% CI 2.23–2.55), have used urinary catheter (PR = 2.24; 95% CI 2.06–2.43), have used any medical device (PR = 1.78; 95% CI 1.66–1.91), and those with diabetes (PR = 1.55; CI 1.43–1.67) were more likely to be colonized by MRSA than other patients. Conclusion Screening programs and preventive measures should target MRSA in ECCs due to the high global preva- lence rates. Keywords Methicillin-resistant Staphylococcus aureus, Residential facilities, Nursing homes, Long-term care, Systematic review *Correspondence: Ali Rostami alirostami1984@gmail.com Full list of author information is available at the end of the article © The Author(s) 2023. Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article’s Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http:// creat iveco mmons. org/ licen ses/ by/4. 0/. The Creative Commons Public Domain Dedication waiver (http:// creat iveco mmons. org/ publi cdoma in/ zero/1. 0/) applies to the data made available in this article, unless otherwise stated in a credit line to the data. Hasanpour et al. Antimicrobial Resistance & Infection Control (2023) 12:4 Page 2 of 11 determinants of MRSA colonization in the elderly living Background in ECCs. The improvement of lifestyle and medical care, and declining birth rates in recent decades, have led to a rapid Methods increase in life expectancy and the mean age of the popu- We followed the Preferred Reporting Items for Systematic lation, especially in developed countries [1]. According Reviews and Meta-analyses (PRISMA) guidelines to per- to the World Health Organization (WHO) report, by form and report this systematic review and meta-analysis 2050, it is estimated that almost more than a quarter of [20] and registered it in PROSPERO (CRD42021291492). the world’s population will be over 60  years old [2]. The number of elderly is expected to reach 1.4 billion by 2030 Data source and searching strategies and 2.1 billion by 2050 [3, 4]. It is evident that a consid- Two authors (A.H.H and A.A.) independently searched erable portion of seniors will need intensive care, while MEDLINE/PubMed, EMBASE, Web of Science col- the majority of them merely need daycare facilities [5, 6]. lection, and Scopus databases on December 20, 2021, Therefore, the exponential need for institutions providing for articles published since January 1, 1980. The search long-term care facilities, nursing homes, and residential was updated for twice; first, on February 15, 2022, and care homes (all defined as elderly care centers (ECCs) in second, on December 15, 2022. Moreover, grey litera- this study) is anticipated [7]. ture was searched through manual inspections of bibli- Multidrug-resistant organisms (MDROs) are among ographies of retrieved studies and internet searches of the leading causes of morbidity and mortality in ECCs Google and Google Scholar. We applied the following [8, 9]. Elderly at ECCs are prone to colonization/infec- search terms: [(“Staphylococcus aureus” OR "methicil- tion with MDROs mainly due to age-associated mor- lin resistant Staphylococcus aureus" OR "MRSA" OR bidities (i.e., cognitive disorders), perpetual living in a "multidrug-resistant organisms" OR "methicillin resist- confined and crowded area, prolonged and recurrent use ance" OR “antibiotic-resistant infections” OR “antibiotic- of broad-spectrum antibiotics, and frequent referral to resistant bacteria”) AND ("old age homes" OR "Nursing and from acute-care hospitals [10–12]. One of the most Homes" OR "homes for the aged" OR "residential facili- prevalent MDROs in ECCs is methicillin-resistant Staph- ties" OR “Residential Care Homes” OR "housing for the ylococcus aureus (MRSA) [8, 13, 14]. MRSA is a global elderly" OR "Long term care facility") AND (“preva- health-threatening organism in healthcare settings, as lence” OR “epidemiology” OR “incidence”)] (Additional it is resistant to antibiotics making the treatment more file  1: Fig. S1). The search syntax was modified accord - complex [15]. MRSA infection could be responsible for ing to the properties of each database. We included stud- fatal sepsis, pneumonia, and higher rates of myocardial ies in all languages, and those with languages unknown infarction and heart failure in patients with bacteremia to the study team were translated into English using the [16]. A national cohort study conducted in the United “Google Translate” online tool. All articles were imported States indicated that MRSA colonization among commu- into EndNote reference manager software X8 (Thomp - nity adults aged 40–85 is associated with a significantly son and Reuters, Philadelphia, USA), and duplicates were increased mortality risk (hazard ratio, 1.75; 95% CI 1.12– removed. 2.73) [17]. Additionally, the attributable cost of MRSA among hospitalized individuals (≥ 65  years) is estimated Inclusion and exclusion criteria to be 22,293 $ per patient (95% CI 19,101–24,485$) in Two authors (A.H.H. and M.A.) independently screened the United States [18]. Another cohort study in Chinese titles and abstracts of retrieved citations to identify eli- nursing homes showed that MRSA colonization was an gible studies that met the following inclusion criteria: independent risk factor for 2 year infection-related mor- (i) presented data on prevalence or incidence of MRSA tality (hazard ratio, 1.96; 95% CI 1.01–3.78) [19]. in ECCs; (ii) reported data on the elderly (minimum age Considering the significant toll of MRSA, monitor - wasn’t specified, we accepted definition of the included ing the extent of colonization, and identifying the key studies for elderlies in ECCs); (iii) included at least 30 risk factors of MRSA acquisition in ECCs is essential tested elderlies. Only the last report was included in for controlling and reducing the burden of this disease multiple sequential articles that were generated from in ECCs residents. In the past years, a growing body of the same data set (e.g., cohort studies). In clinical trials, epidemiological literature evaluated the prevalence rate we only extracted baseline data. Articles were excluded of MRSA colonization in ECCs from various countries; if they were (i) performed only on MRSA patients; (ii) nevertheless, there is no comprehensive study to estimate performed on elderly in community or hospitals; (iii) global and regional prevalence rates. To bridge this gap, included only a specific group of elderly with a specific we performed a systematic review and meta-analysis to disease or situation; (iv) used datasets that overlapped evaluate the worldwide prevalence and identify potential Hasanpour  et al. Antimicrobial Resistance & Infection Control (2023) 12:4 Page 3 of 11 with other articles; (v) studies following the MRSA out- were no group comparisons or hypothesis tests of “treat- breaks in ECCs; (vi) case series, case reports, and arti- ment effect” [30]. cles without original data such as reviews or systematic We performed subgroup and meta-regression analysis reviews, comments, editorials, and corresponding letters. to identify sources of heterogeneity, determine the risk factors and the effects of socio-demographic factors on Data extraction and quality assessment prevalence rates. Subgroup analyses were undertaken After screening the articles, the required data from each according to WHO-defined regions, income and HDI eligible study were extracted and imported into a stand- levels, type of diagnostic methods, risk of bias, and key ardized Microsoft Excel spreadsheet (version 2016; determinants. Corresponding prevalence ratios (PRs) Microsoft Corporation, Redmond, USA). The follow - were estimated for variables subjected to subgroup analy- ing data were extracted from each study: name of the sis. Meta-regressions were performed on publication first author, year of publication, start and end year of year, sample size, income and HDI levels. study, country, type of ECCs, study design, body sam- pling sites, diagnostic methods for MRSA detection, age Results (mean and range) of tested elderlies, the total number Characteristics of the included studies of tested participants, the total number of participants As outlined in Fig. 1, a total of 4472 articles were identi- tested positive for Staphylococcus aureus, methicillin- fied in our initial literature search, of these 118 articles sensitive Staphylococcus aureus (MSSA), and MRSA. We (119 studies) involving 164,717 participants from 29 stratified countries according to WHO-defined regions countries were included in the meta-analysis. The main [17], World Bank’s income category [21], gross national characteristics of the included studies are shown in Addi- income per capita [22], and the human development tional file  1: Table  S1. Studies included were published index (HDI) [23]. Furthermore, to evaluate the main risk between 1990 and 2022. Twenty-six studies had data to factors of MRSA prevalence, we extracted data (if avail- determine the proportion of MRSA and MSSA. Over- able in individual studies) of gender, prior antibiotics use, all, eligible studies were available for five WHO-defined prior MRSA infection, prior hospitalization, having any regions; 65 studies were from European region, 34 from wound, urinary catheter, use of any medical device, dia- the region of the Americas, 18 studies from the Western betes, antacid use, and dementia. To conduct the quality Pacific region, and one study for each of the Eastern Med - assessment and the risk of bias in included studies, we iterranean and African regions. Countries with the most used the Joanna Briggs Institute (JBI) Critical Appraisal eligible studies were the United States (31 studies), China Checklist for studies that reported prevalence data [24]. (12 studies), Germany (10 studies), the United Kingdom The detailed items of JBI tools are presented in Addi - (eight studies), and Italy (six studies). Regarding study tional file 1: Table S1. designs, 88 studies were cross-sectional, 21 studies were prospective cohort, seven studies were randomized con- Data synthesis and statistical analysis trolled trial (RCT), and three studies were case control. Stata software version 16.0 (STATA Corp., College Sta- Regarding the location of studies, 71, 41, and 7 studies tion, Texas, USA) was used to perform the meta-analyses. were performed in nursing homes, long-term care facili- Before pooling prevalence estimates, the variance of the ties, and residential care homes, respectively. Consider- raw prevalence from each included study was stabilized ing the risk of bias, 68 and 51 studies were determined by using the Freeman-Tukey double arc-sine transforma- as the low and moderate risk of biases. All studies used tion [25]. The Cochran’s Q test and I index were used to culture-based methods to determine the MRSA preva- calculate the between-studies heterogeneity [23, 26]. A lence, and 54 performed further analyses using molecular P-value < 0.01 for the Cochran’s Q test and an I of > 75% methods. Additional information is presented in Tables 1 are considered as significant and high heterogeneity, and 2. respectively [23, 26, 27]. DerSimonian and Laird random- effects model (REM) was used in case of high heteroge - Prevalence of MRSA colonization in ECCs neity, to conservatively estimate the pooled prevalence Table  2 presents the national and regional pooled of MRSA at 95% confidence intervals (CIs) [25, 28]. We prevalence of MRSA in residents of ECCs. The pooled estimated the prevalence in individual countries by syn- global prevalence was 14.69% (95% CI 12.39–17.15%; thesizing the prevalence rates of all studies from the same 16,793/164,717) by using REM, with high heterogeneity country. Further, we calculated the prevalence rates of across 119 studies (χ2 = 18,637.54, P < 0.001, I = 99.3%). MRSA for the WHO-defined regions by synthesizing the According to WHO-defined regions, pooled prevalence data for countries within the same region [29]. We did rates (at 95% CI) were: 22.27% (15.56–29.79%) in the not assess publication bias, as in prevalence studies, there region of the Americas, 16.57% (11.70–22.10%) in the Hasanpour et al. Antimicrobial Resistance & Infection Control (2023) 12:4 Page 4 of 11 Fig. 1 The PRISMA diagram of the study selection Western Pacific, 10.93% (8.56–13.55%) in Europe. Only prevalence rates of MRSA were 16.29% (12.29–20.71%), one study was available for each of the Eastern Mediter- 14.35% (11.50–17.44%), and 9.85% (3.62–17.93%) for the ranean and African regions, indicating prevalence rates elderly living in long-term care facilities, nursing homes, of 8.55% (4.63–14.18%) and 9.04% (5.36–14.08%), respec- and residential care homes, respectively. Considering tively. For countries with two or more available stud- study designs, the lowest and highest prevalence rates ies, United States (23.78%), Singapore (22.72%), Poland were observed in studies with cross-sectional (13.37%, (22.18%), United Kingdom (18.66%), China (18.07%), 10.68–16.30%) and RCT (20.15%, 12.55–29.01%) designs, Italy (16.34%), Spain (15.45%), Israel (14.82%), France respectively. Studies published after year of 2000 showed (13.89%) and Switzerland (13.15%) exhibited almost the non-significant increasing prevalence rates (C = 0.001; highest prevalence rates (Fig.  2). Analyzing the data on P = 0.547) (Table  2 and Fig.  3C). Studies with low risk of the proportion of MRSA and MSSA in 26 studies using bias (13.06%, 10.26–16.15%) showed lower prevalence REM showed that 26% (18–36%) of all S. aureus isolates rates than those with moderate risk of bias (17.11%, were MRSA (Additional file 1: Fig. S2A). 13.64–20.87%) (Table 2). Subgroup analyses of income and HDI levels yielded relatively similar results; prevalence rate for countries Risk factors associated with MRSA colonization in residents with upper-middle income and high HDI levels was of ECCs 16.5%, and for countries with high income and very high The analyses of key determinants of MRSA coloniza - HDI levels was 14.4% (see Table 2). Meta-regression anal- tion in elderly living in ECCs showed that MRSA is yses indicated a non-significant increasing trend in prev - more colonized in males than females (PR = 1.55; 95% CI alence with higher income [coefficient (C) = 0.000001; 1.47–1.64). With regard to other risk factors, we found P = 0.259], and HDI values (C = -0.117; P = 0.573) that elderly with a previous history of MRSA infection (Fig.  3A, B). According to the type of ECCs, pooled (PR = 3.71; 95% CI 3.44–4.01), prior use of antibiotics Hasanpour  et al. Antimicrobial Resistance & Infection Control (2023) 12:4 Page 5 of 11 Table 1 Global and regional pooled prevalence rates of MRSA among elderly living in ECCs; results from 119 studies performed in 30 countries WHO regions*/country Number of Number of individuals Number of individuals Pooled prevalence % (95% CI) datasets screened (total) with MRSA Global 119 164,717 16,793 14.69 (12.39–17.15) Americas 34 86,065 7508 22.27 (15.56–29.79) United States 31 21,457 5517 23.78 (19.12–28.77) Brazil 2 526 71 13.11 (10.34–16.14) Canada 1 64,082 1920 3.01 (2.87–3.13) Western Pacific Region 18 15,419 2936 16.57 (11.70–22.10) China 12 11,337 2101 18.07 (11.18–26.17) Japan 3 354 32 8.81 (5.99–12.08) Singapore 2 3613 785 21.72 (20.39–23.08) Australia 1 115 18 15.65 (9.55–23.60) European region 65 62,893 6319 10.93 (8.56–13.55) Germany 10 10,857 432 4.67 (2.59–7.29) United Kingdom 8 8633 2037 18.66 (12.07–26.28) Belgium 7 13,508 1403 8.97 (4.94–14.03) Italy 6 1710 246 16.34 (10.23–23.52) Spain 5 2700 460 15.45 (9.50–22.52) Sweden 4 1122 139 4.52 (0.01–33.07) Netherlands 3 5841 261 6.63 (0.01–35.64) France 3 1500 121 13.89 (3.70–29.01) Israel 3 545 68 14.82 (5.28–27.95) Switzerland 3 12,128 805 13.15 (7.08–20.70) Finland 1 213 2 0.94 (0.11–3.35) Ireland 2 818 82 9.46 (7.51–11.61) Poland 2 248 61 22.18 (17.16–27.62) Slovenia 2 209 22 10.50 (6.62–15.09) Greece 1 227 33 14.54 (10.22–19.81) Croatia 1 877 62 7.07 (5.46–8.97) Georgia 1 56 8 14.29 (6.38–26.22) Austria 1 500 0 0.01 (0.00–0.74) Luxembourg 1 954 69 7.23 (5.67–9.06) Turkey 1 247 8 3.24 (1.41–6.28) African region 1 152 13 8.55 (4.63–14.18) South Africa 1 152 13 8.55 (4.63–14.18) Eastern Mediterranean 1 188 17 9.04 (5.36–14.08) Saudi Arabia 1 188 17 9.04 (5.36–14.08) *The WHO regions are sorted based on prevalence rates, and countries are sorted based on the number of datasets colonization (P-value > 0.05). More information is pre- (PR = 1.97; 95% CI 1.83–2.12), history of hospitalization sented in Table 3. within the previous year (PR = 1.32; 95% CI 1.20–1.45), those with any wound (PR = 2.38; 95% CI 2.23–2.55), those who have used urinary catheter (PR = 2.24; 95% Discussion CI 2.06–2.43), those who have used any medical device MRSA infection continues to sustain as a major public (PR = 1.78; 95% CI 1.66–1.91), and those with diabe- health threat worldwide, especially in the elderly. In the tes (PR = 1.55; 95% CI 1.43–1.67) were more likely to be present study, for the first time, we assembled data from colonized by MRSA than other patients (Table  3). Other all available studies (over 40 years) that had reported the risk factors such as antacid use and dementia were not prevalence of MRSA in ECCs. Among the key findings significantly associated with an increased risk of MRSA was the high pooled prevalence of MRSA colonization Hasanpour et al. Antimicrobial Resistance & Infection Control (2023) 12:4 Page 6 of 11 Table 2 Prevalence estimates for the MRSA in the elderly, according to the study characteristics and socio-demographic factors Variable subgroup Number of Number of elderlies Number of elderlies Pooled prevalence % (95% CI) datasets screened (total) with MRSA Income Upper middle 16 12,071 2193 16.46 (10.79–23.05) High 103 152,646 14,600 14.42 (11.98–17.04) HDI High 15 12,015 2185 16.60 (10.74–23.42) Very high 104 152,702 14,608 14.42 (11.99–17.02) Type of setting Long-term care facilities 41 88,088 5069 16.29 (12.29–20.71) Nursing homes 71 69,652 10,730 14.35 (11.50–17.44) Residential care homes 7 6977 994 9.58 (3.62–17.93) Study design Cross-sectional 88 135,275 12,969 13.37 (10.68–16.30) Prospective cohort 21 23,022 2756 17.90 (12.66–23.82) Case–control 3 312 73 21.03 (3.67–46.99) RCT 7 6108 995 20.15 (12.55–29.01) Publication year Before 2000 14 3505 441 12.84 (9.24–16.93) 2001–2010 27 33,541 4365 16.12 (11.43–21.44) 2011–2022 78 127,671 11,987 14.53 (11.58–17.75) Risk of bias Low 68 151,473 14,489 13.06 (10.26–16.15) Moderate 51 13,244 2304 17.11 (13.64–20.87) Fig. 2 Worldwide distribution of MRSA colonization in ECCs Hasanpour  et al. Antimicrobial Resistance & Infection Control (2023) 12:4 Page 7 of 11 Fig. 3 Meta-regression analyses of MRSA prevalence among elderly living in ECCs concerning A Country’s gross national income per capita, B HDI level and C Publication year Table 3 Risk factors associated with MRSA colonization in elderly living in ECCs Variable subgroup Number of Number of elderlies Number of Pooled prevalence % (95% CI) Prevalence ratio (95% CI) datasets screened (total) elderlies with MRSA Gender Male 32 9149 2164 18.41 (13.14–24.30) 1.55 (1.47–1.64) Female 32 15,572 2387 15.18 (10.81–20.12) 1 Prior antibiotics use Yes 21 6746 1450 24.59 (17.82–32.03) 1.97 (1.83–2.12) No 21 9492 1031 13.61 (9.67–18.09) 1 Prior MRSA infection Yes 11 1430 669 49.86 (35.87–63.86) 3.71 (3.44–4.01) No 11 10,044 1264 17.76 (11.25–25.37) 1 Hospitalization in past year Yes 19 3149 559 21.34 (14.30–29.29) 1.32 (1.20–1.45) No 18 6907 926 16.90 (10.99–23.76) 1 Any wound Yes 24 4003 1056 27.03 (19.62–35.10) 2.38 (2.23–2.55) No 24 15,439 1706 12.41 (9.01–16.27) 1 Urinary catheter Yes 20 2949 661 19.59 (14.72–24.93) 2.24 (2.06–2.43) No 20 15,656 1565 10.86 (7.44–14.83) 1 Any device Yes 16 5413 1274 30.09 (19.43–41.85) 1.78 (1.66–1.91) No 16 9715 1279 16.07 (10.97–21.91) 1 Diabetes Yes 19 4990 870 17.11 (11.48–23.52) 1.55 (1.43–1.67) No 19 13,734 1543 14.74 (9.69–20.60) 1 Antacid use Yes 3 1364 72 8.95 (1.98–19.36) 1.02 (0.76–1.38) No 3 1966 101 5.01 (4.06–6.03) 1 Dementia Yes 5 1792 325 15.93 (7.93–25.97) 1.04 (0.93–1.17) No 5 5243 994 15.08 (9.36–21.84) 1 in the residents of ECCs (14.69%, 12.39–17.15%); which Furthermore, the estimated colonization rate in our is over tenfold higher than the MRSA colonization rate study is higher than those reported from other high- among the general community (1.3%, 1.04–1.53%) [31]. risk groups such as HIV + patients (7.0%, 5.0–9.0%) [32], Hasanpour et al. Antimicrobial Resistance & Infection Control (2023) 12:4 Page 8 of 11 hemodialysis patients (6.2%, 4.2–8.5%) [33], and patients environment are scarce [9]. Excessive use of antibiotics admitted to intensive care units (7.0%, 5.8–8.3%) [34]. is one contributing factor to the increase in antibiotic This highlights that elderly residents of ECCs are at very resistance and the growth in the emergence of MDROs, high risk for MRSA colonization, maybe due to cross- which should be addressed in ECCs. transmission between the elderlies in the crowded situa- Our findings identified several risk factors for MRSA tion of ECCs or introduction of infection when admitting colonization in residents of ECCs, such as being male, new elders from outside of ECCs (i.e., hospitals or com- prior antibiotics use, previous MRSA infection, hospitali- munity) [35]. Other possible explanations for this high zation in the past 12 months, presence of any wound, uri- prevalence of MRSA could be frailty, impaired immune nary catheter, usage of any invasive medical device, and system function, frequent hospitalization, and overuse diabetes. Our findings are consistent with several studies of antibiotics [36, 37]. All the above-mentioned reasons about the MRSA prevalence in the community or high- underline the significance of recognizing contributing risk populations such as HIV + and hemodialysis patients factors, and treating MRSA to reduce and prevent the [2, 31–33, 45, 46]. Although there is no consensus on the spread of the disease. role of gender in the prevalence of MRSA, it has been Our results showed that the geographic distribution asserted that elderly males are more prone to the other of MRSA colonization is heterogeneous, with the high- predisposing factors of being infected with MRSA namely est and lowest colonization rates reported in countries in more complicated diabetes and wounds, frequent use of regions of the Americas (22.27%) and Europe (10.93%), medical devices, and catheterization which may lead to a respectively. This finding is in accordance with previ - higher prevalence MRSA [47, 48]. Furthermore, frequent ous meta-analysis studies in other high-risk populations use of antibiotics is one of the main cause for the devel- [32–34]. Spatial variations of MRSA prevalence could opment of antimicrobial resistance in staphylococci and be explained by differences in numerous demographic other bacteria [46, 49]. A previous MRSA infection could information among the countries studied and different lead to re-infection secondary to a lack of proper eradi- ECCs in a country such as policies for prescription of cation or stable colonization [45]. The constant presence antibiotics, various infection prevention programs, dif- of high-risk individuals in hospitals and routine antibiot- ferent education and training of staff and elderly for per - ics use justify the higher prevalence of MRSA in elders sonal hygiene, different structure of health care systems, who were hospitalized in the last 12 months [34]. Medi- and facilities for MRSA diagnosis [32, 38–41]. Our study cal devices make patients susceptible to MRSA through also highlighted a significant data gap in less developed the mechanism of biofilm formation on the devices and countries, most strikingly in Latin America, Africa, East- subsequent detachment, which may contribute to bac- ern Mediterranean, Central Asia, and South-East of Asia teremia or sepsis [50]. A wide range of chronic diseases regions, where more data are required to obtain accu- like diabetes renders the patients prone to MRSA given rate estimates of the prevalence of MRSA colonization in the state of immunosuppression and more complicated elderly residents of ECCs. It should be noted that under- wounds [51, 52]. Similar to our findings, chronic illnesses, developed or developing countries may not have well- intravenous drug use, and contact with infected individu- established elderly care systems or antibiotic stewardship als are reported as risk factors for community-acquired programs. Due to the increasing number of ECCs in MRSA [31]. These findings have implications for policy - developing countries [42], these information gaps should makers in identifying high-risk groups to reduce the dis- be addressed through future representative epidemiolog- ease burden by employing targeted interventions. ical studies. Our findings in this comprehensive systematic Our findings suggested different prevalence rates of review and meta-analysis have implications for future MRSA colonization in nursing homes (14.35%), long- research and clinical practices. However, this study has term care facilities (16.29%), and residential care homes identified several shortcomings of the current data on (9.58%). The discrepancies in prevalence rates between MRSA colonization among the elderly in ECCs. First, different types of ECCs may stem from the differences our study contains reports from only 30 of ~ 200 coun- in services rendered by each type of center. In nursing tries globally; there were no country-level estimates for homes, patients usually receive daily or constant profes- some countries, and no prevalence data were available sional nursing care, and antibiotics can be prescribed from many countries. In addition, most of the available with the consultation of a physician [43], therefore, studies had a paucity of data on critical variables such antimicrobial overuse/abuse is prevalent [43]. In con- as gender, age, ethnicity, and risk factors associated trast, residential care centers are mostly restricted to with MRSA colonization. Therefore, some non-signif - personal care [44]. Despite monitoring schemes in hos- icant results considering risk factors might be due to pitals for antibiotic use, records for the nursing homes the low number of studies. For example, while among Hasanpour  et al. Antimicrobial Resistance & Infection Control (2023) 12:4 Page 9 of 11 Author contributions those who took antacids (as shown in Table  3) almost AHH and AR conceived the study. AHH, AR, MA, AA, AM and SRH conducted double MRSA (8.95%) has been estimated, the preva- the searches, and collected data. AHH, MS, MA, AM and MJ analysed the data lence ratio was non-significant. Second, the studies sets and interpreted the results. AHH, AM, AA, MB and AR drafted and edited the manuscript. All authors commented on, or edited, drafts and approved included had different qualities and studies with lower the final version of the manuscript. qualities (17.11%) showed higher colonization rates than high quality studies (13.06%) which highlight the Funding No funding. need for more robust surveys of MRSA colonization in residents of ECCs. Third, as expected in meta-anal - Availability of data and materials yses on prevalence studies [25, 29, 53–55], a substan- The data that support the findings of this study are available from the cor - responding author upon reasonable request. tial heterogeneity was found in our analyses that could not be explained by subgroup analyses. The sources of Declarations heterogeneity are likely related to study characteris- tics, including differences in geographical distribution, Ethics approval and consent to participate study design, sample size, diagnostic methods, leading Not applicable. to differences in the quality and performance of these Consent for publication methods. Moreover, this heterogeneity suggests that Not applicable. local risk factors and transmission routes of MRSA are Competing interests varied in different geographical regions, countries, or The authors declare that they have no competing interests. even in individual ECCs. Author details Student Research Committee, Babol University of Medical Sciences, Babol, Iran. Department of Biostatistics and Epidemiology, School of Public Health, Conclusion Babol University of Medical Sciences, Babol, Iran. Department of Public In conclusion, this study found that the prevalence of Health and Prevention Science, School of Health Sciences, Baldwin Wallace University, Berea, OH, USA. School of Medicine, Shiraz University of Medical MRSA colonization in residents of ECCs is high across 5 6 Sciences, Shiraz, Iran. Harlem Medical Center, Bridgeview, IL, USA. Depar t- the world and varies by gender and geographic location. ment of Hematopoietic Biology and Malignancy, The University of Texas Md Moreover, elders with previous MRSA infection, hospi- Anderson Cancer Center, Houston, TX, USA. Social Determinants of Health Research Center, Health Research Institute, Babol University of Medical Sci- talization, antibiotics and diabetes, and those that used ences, Babol, Iran. Infectious Diseases and Tropical Medicine Research Center, medical devices are more prone to MRSA colonization. Health Research Institute, Babol University of Medical Sciences, Babol, Iran. This sheds significant light on the essence of targeted Received: 12 April 2022 Accepted: 21 January 2023 interventions and screening programs to locate infected people, control risk factors, and reduce the transmis- sion of MRSA and other MDROs to elderlies living in ECCs. Given the aging trend of the populations, there References is an urgent need for studies, particularly in developing 1. Suzman R, Beard JR, Boerma T, Chatterji S. Health in an ageing world— and underdeveloped countries to better estimate the what do we know? Lancet. 2015;385(9967):484–6. 2. Wong JW, Ip M, Tang A, Wei VW, Wong SY, Riley S, Read JM, Kwok KO. risk of disease. We recommend several interventions Prevalence and risk factors of community-associated methicillin- to reduce the MRSA burden in ECCS. 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Journal

Antimicrobial Resistance & Infection Control – Springer Journals

Published: Jan 29, 2023

Keywords: Methicillin-resistant Staphylococcus aureus; Residential facilities; Nursing homes; Long-term care; Systematic review

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