0% found this document useful (0 votes)
19 views11 pages

The Global Prevalence of Methicillin-Resistant of Elderly Care Centers: A Systematic Review and Meta-Analysis

Uploaded by

Ach Ri Fa I
Copyright
© © All Rights Reserved
We take content rights seriously. If you suspect this is your content, claim it here.
Available Formats
Download as PDF, TXT or read online on Scribd
0% found this document useful (0 votes)
19 views11 pages

The Global Prevalence of Methicillin-Resistant of Elderly Care Centers: A Systematic Review and Meta-Analysis

Uploaded by

Ach Ri Fa I
Copyright
© © All Rights Reserved
We take content rights seriously. If you suspect this is your content, claim it here.
Available Formats
Download as PDF, TXT or read online on Scribd
You are on page 1/ 11

Hasanpour et al.

Antimicrobial Resistance
Antimicrobial Resistance & Infection Control (2023) 12:4
https://doi.org/10.1186/s13756-023-01210-6 and Infection Control

REVIEW Open Access

The global prevalence of methicillin‑resistant


Staphylococcus aureus colonization in residents
of elderly care centers: a systematic review
and meta‑analysis
Amir Hossein Hasanpour1, Mahdi Sepidarkish2, Abolfazl Mollalo3, Ali Ardekani4, Mustafa Almukhtar5,
Amal Mechaal6, Seyed Reza Hosseini7, Masoumeh Bayani7, Mostafa Javanian8 and Ali Rostami8*

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

Background determinants of MRSA colonization in the elderly living


The improvement of lifestyle and medical care, and in ECCs.
declining birth rates in recent decades, have led to a rapid
increase in life expectancy and the mean age of the popu- Methods
lation, especially in developed countries [1]. According We followed the Preferred Reporting Items for Systematic
to the World Health Organization (WHO) report, by Reviews and Meta-analyses (PRISMA) guidelines to per-
2050, it is estimated that almost more than a quarter of form and report this systematic review and meta-analysis
the world’s population will be over 60 years old [2]. The [20] and registered it in PROSPERO (CRD42021291492).
number of elderly is expected to reach 1.4 billion by 2030
and 2.1 billion by 2050 [3, 4]. It is evident that a consid- Data source and searching strategies
erable portion of seniors will need intensive care, while Two authors (A.H.H and A.A.) independently searched
the majority of them merely need daycare facilities [5, 6]. MEDLINE/PubMed, EMBASE, Web of Science col-
Therefore, the exponential need for institutions providing lection, and Scopus databases on December 20, 2021,
long-term care facilities, nursing homes, and residential for articles published since January 1, 1980. The search
care homes (all defined as elderly care centers (ECCs) in was updated for twice; first, on February 15, 2022, and
this study) is anticipated [7]. second, on December 15, 2022. Moreover, grey litera-
Multidrug-resistant organisms (MDROs) are among ture was searched through manual inspections of bibli-
the leading causes of morbidity and mortality in ECCs ographies of retrieved studies and internet searches of
[8, 9]. Elderly at ECCs are prone to colonization/infec- Google and Google Scholar. We applied the following
tion with MDROs mainly due to age-associated mor- search terms: [(“Staphylococcus aureus” OR "methicil-
bidities (i.e., cognitive disorders), perpetual living in a lin resistant Staphylococcus aureus" OR "MRSA" OR
confined and crowded area, prolonged and recurrent use "multidrug-resistant organisms" OR "methicillin resist-
of broad-spectrum antibiotics, and frequent referral to ance" OR “antibiotic-resistant infections” OR “antibiotic-
and from acute-care hospitals [10–12]. One of the most resistant bacteria”) AND ("old age homes" OR "Nursing
prevalent MDROs in ECCs is methicillin-resistant Staph- Homes" OR "homes for the aged" OR "residential facili-
ylococcus aureus (MRSA) [8, 13, 14]. MRSA is a global ties" OR “Residential Care Homes” OR "housing for the
health-threatening organism in healthcare settings, as elderly" OR "Long term care facility") AND (“preva-
it is resistant to antibiotics making the treatment more lence” OR “epidemiology” OR “incidence”)] (Additional
complex [15]. MRSA infection could be responsible for file 1: Fig. S1). The search syntax was modified accord-
fatal sepsis, pneumonia, and higher rates of myocardial ing to the properties of each database. We included stud-
infarction and heart failure in patients with bacteremia ies in all languages, and those with languages unknown
[16]. A national cohort study conducted in the United to the study team were translated into English using the
States indicated that MRSA colonization among commu- “Google Translate” online tool. All articles were imported
nity adults aged 40–85 is associated with a significantly into EndNote reference manager software X8 (Thomp-
increased mortality risk (hazard ratio, 1.75; 95% CI 1.12– son and Reuters, Philadelphia, USA), and duplicates were
2.73) [17]. Additionally, the attributable cost of MRSA removed.
among hospitalized individuals (≥ 65 years) is estimated
to be 22,293 $ per patient (95% CI 19,101–24,485$) in Inclusion and exclusion criteria
the United States [18]. Another cohort study in Chinese Two authors (A.H.H. and M.A.) independently screened
nursing homes showed that MRSA colonization was an titles and abstracts of retrieved citations to identify eli-
independent risk factor for 2 year infection-related mor- gible studies that met the following inclusion criteria:
tality (hazard ratio, 1.96; 95% CI 1.01–3.78) [19]. (i) presented data on prevalence or incidence of MRSA
Considering the significant toll of MRSA, monitor- in ECCs; (ii) reported data on the elderly (minimum age
ing the extent of colonization, and identifying the key wasn’t specified, we accepted definition of the included
risk factors of MRSA acquisition in ECCs is essential studies for elderlies in ECCs); (iii) included at least 30
for controlling and reducing the burden of this disease tested elderlies. Only the last report was included in
in ECCs residents. In the past years, a growing body of multiple sequential articles that were generated from
epidemiological literature evaluated the prevalence rate the same data set (e.g., cohort studies). In clinical trials,
of MRSA colonization in ECCs from various countries; we only extracted baseline data. Articles were excluded
nevertheless, there is no comprehensive study to estimate if they were (i) performed only on MRSA patients; (ii)
global and regional prevalence rates. To bridge this gap, performed on elderly in community or hospitals; (iii)
we performed a systematic review and meta-analysis to included only a specific group of elderly with a specific
evaluate the worldwide prevalence and identify potential disease or situation; (iv) used datasets that overlapped
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 I2 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 I2 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, I2 = 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

(PR = 1.97; 95% CI 1.83–2.12), history of hospitalization colonization (P-value > 0.05). More information is pre-
within the previous year (PR = 1.32; 95% CI 1.20–1.45), sented in Table 3.
those with any wound (PR = 2.38; 95% CI 2.23–2.55),
those who have used urinary catheter (PR = 2.24; 95%
CI 2.06–2.43), those who have used any medical device
Discussion
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

those who took antacids (as shown in Table 3) almost Author contributions
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
included had different qualities and studies with lower the manuscript. All authors commented on, or edited, drafts and approved
the final version of the manuscript.
qualities (17.11%) showed higher colonization rates
than high quality studies (13.06%) which highlight the Funding
need for more robust surveys of MRSA colonization No funding.
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-
tial heterogeneity was found in our analyses that could responding author upon reasonable request.
not be explained by subgroup analyses. The sources of
heterogeneity are likely related to study characteris- Declarations
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
varied in different geographical regions, countries, or Competing interests
The authors declare that they have no competing interests.
even in individual ECCs.
Author details
1
Student Research Committee, Babol University of Medical Sciences, Babol,
Iran. 2 Department of Biostatistics and Epidemiology, School of Public Health,
Conclusion Babol University of Medical Sciences, Babol, Iran. 3 Department of Public
In conclusion, this study found that the prevalence of Health and Prevention Science, School of Health Sciences, Baldwin Wallace
MRSA colonization in residents of ECCs is high across University, Berea, OH, USA. 4 School of Medicine, Shiraz University of Medical
Sciences, Shiraz, Iran. 5 Harlem Medical Center, Bridgeview, IL, USA. 6 Depart-
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. 7 Social Determinants of Health
talization, antibiotics and diabetes, and those that used Research Center, Health Research Institute, Babol University of Medical Sci-
ences, Babol, Iran. 8 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
interventions and screening programs to locate infected Received: 12 April 2022 Accepted: 21 January 2023
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.
risk of disease. We recommend several interventions 2. Wong JW, Ip M, Tang A, Wei VW, Wong SY, Riley S, Read JM, Kwok KO.
Prevalence and risk factors of community-associated methicillin-
to reduce the MRSA burden in ECCS. For instance,
resistant Staphylococcus aureus carriage in Asia-Pacific region from
reducing the consumptions of antibiotics (especially 2000 to 2016: a systematic review and meta-analysis. Clin Epidemiol.
fluoroquinolones and third generation cephalosporins), 2018;10:1489–501.
3. Naja S, Din Makhlouf MME, Chehab MAH. An ageing world of the
enhanced barrier precautions, chlorhexidine bathing,
21st century: a literature review. Int J Community Med Public Health.
routine MDROs surveillance, and isolation of MRSA- 2017;4(12):4363–9.
infected patients in single rooms. Additionally, edu- 4. Tarakcı E, Zenginler Y, Kaya Mutlu E. Chronic pain, depression symptoms
and daily living independency level among geriatrics in nursing home.
cating and training the elderly and health workers in
Agri. 2015;27(1):35–41.
personal hygiene should be promoted. 5. McClean P, Hughes C, Tunney M, Goossens H, Jans B, Group obotESoAC-
NHP, Jans B, Stroobants R, Goossens H, Budimir A, et al. Antimicrobial
prescribing in European nursing homes. J Antimicrob Chemother.
Supplementary Information 2011;66(7):1609–16.
The online version contains supplementary material available at https://​doi.​ 6. Christensen K, Doblhammer G, Rau R, Vaupel JW. Ageing populations: the
org/​10.​1186/​s13756-​023-​01210-6. challenges ahead. Lancet. 2009;374(9696):1196–208.
7. Aschbacher R, Pagani E, Confalonieri M, Farina C, Fazii P, Luzzaro F,
Additional file 1. Supplematary tables and figures. Montanera PG, Piazza A, Pagani L. Review on colonization of residents
and staff in Italian long-term care facilities by multidrug-resistant bacteria
compared with other European countries. Antimicrob Resist Infect Con-
Acknowledgements trol. 2016;5:33.
The authors would like to thank to Health Research Institute of Babol Univer-
sity of Medical Sciences for their supports.
Hasanpour et al. Antimicrobial Resistance & Infection Control (2023) 12:4 Page 10 of 11

8. Cassone M, Mody L. Colonization with multidrug-resistant organisms in 30. Hunter JP, Saratzis A, Sutton AJ, Boucher RH, Sayers RD, Bown MJ. In
nursing homes: scope, importance, and management. Curr Geriatr Rep. meta-analyses of proportion studies, funnel plots were found to be
2015;4(1):87–95. an inaccurate method of assessing publication bias. J Clin Epidemiol.
9. Tinelli M, Tiseo G, Falcone M. Prevention of the spread of multidrug-resist- 2014;67(8):897–903.
ant organisms in nursing homes. Aging Clin Exp Res. 2021;33(3):679–87. 31. Salgado CD, Farr BM, Calfee DP. Community-acquired methicillin-
10. Gruber I, Heudorf U, Werner G, Pfeifer Y, Imirzalioglu C, Ackermann H, resistant Staphylococcus aureus: a meta-analysis of prevalence and risk
Brandt C, Besier S, Wichelhaus TA. Multidrug-resistant bacteria in geriatric factors. Clin Infect Dis. 2003;36(2):131–9.
clinics, nursing homes, and ambulant care–prevalence and risk factors. 32. Sabbagh P, Riahi SM, Gamble HR, Rostami A. The global and regional
Int J Med Microbiol. 2013;303(8):405–9. prevalence, burden, and risk factors for methicillin-resistant Staphylo-
11. Lim CJ, Cheng AC, Kennon J, Spelman D, Hale D, Melican G, Sidjabat HE, coccus aureus colonization in HIV-infected people: a systematic review
Paterson DL, Kong DC, Peleg AY. Prevalence of multidrug-resistant organ- and meta-analysis. Am J Infect Control. 2019;47(3):323–33.
isms and risk factors for carriage in long-term care facilities: a nested 33. Zacharioudakis IM, Zervou FN, Ziakas PD, Mylonakis E. Meta-analysis
case–control study. J Antimicrob Chemother. 2014;69(7):1972–80. of methicillin-resistant Staphylococcus aureus colonization and risk of
12. Dyar OJ, Pagani L, Pulcini C. Strategies and challenges of antimicro- infection in dialysis patients. J Am Soc Nephrol. 2014;25(9):2131–41.
bial stewardship in long-term care facilities. Clin Microbiol Infect. 34. Zervou FN, Zacharioudakis IM, Ziakas PD, Rich JD, Mylonakis E.
2015;21(1):10–9. Prevalence of and risk factors for methicillin-resistant Staphylococcus
13. Budimir A, Pal MP, Bošnjak Z, Mareković I, Vuković D, Križan IR, Milas aureus colonization in HIV infection: a meta-analysis. Clin Infect Dis.
J, Plečko V, Kalenić S. Prevalence and molecular characteristics of 2014;59(9):1302–11.
methicillin-resistant Staphylococcus aureus strains isolated in a multi- 35. Sasahara T, Ae R, Yoshimura A, Kosami K, Sasaki K, Kimura Y, Akine D,
center study of nursing home residents in Croatia. Am J Infect Control. Ogawa M, Hamabata K, Hatakeyama S, et al. Association between
2014;42(11):1197–202. length of residence and prevalence of MRSA colonization among resi-
14. Lasseter G, Charlett A, Lewis D, Donald I, Howell-Jones R, McNulty CAM. dents in geriatric long-term care facilities. BMC Geriatr. 2020;20(1):481.
Staphylococcus aureus carriage in care homes: identification of risk factors, 36. Denkinger CM, Grant AD, Denkinger M, Gautam S, D’Agata EM.
including the role of dementia. Epidemiol Infect. 2010;138(5):686–96. Increased multi-drug resistance among the elderly on admission
15. Tacconelli E, Carrara E, Savoldi A, Harbarth S, Mendelson M, Monnet DL, to the hospital–a 12-year surveillance study. Arch Gerontol Geriatr.
Pulcini C, Kahlmeter G, Kluytmans J, Carmeli Y. Discovery, research, and 2013;56(1):227–30.
development of new antibiotics: the WHO priority list of antibiotic-resist- 37. Yoshikawa TT. Epidemiology and unique aspects of aging and infectious
ant bacteria and tuberculosis. Lancet Infect Dis. 2018;18(3):318–27. diseases. Clin Infect Dis. 2000;30(6):931–3.
16. Inagaki K, Lucar J, Blackshear C, Hobbs CV. Methicillin-susceptible and 38. Kavanagh KT. Control of MSSA and MRSA in the United States: protocols,
methicillin-resistant Staphylococcus aureus bacteremia: nationwide policies, risk adjustment and excuses. Antimicrob Resist Infect Control.
estimates of 30-day readmission, in-hospital mortality, length of stay, and 2019;8(1):103.
cost in the United States. Clin Infect Dis. 2019;69(12):2112–8. 39. Piper Jenks N, Pardos de la Gandara M, D’Orazio BM, Correa da rosa J, Kost
17. Mainous AG, Rooks BJ, Carek PJ. Methicillin-resistant Staphylococcus RG, Khalida C, Vasquez KS, Coffran C, Pastagia M, Evering TH, et al. Differ-
aureus colonization and mortality risk among community adults aged ences in prevalence of community-associated MRSA and MSSA among
40–85. J Am Board Fam Med. 2021;34(2):439–41. U.S. and non-U.S. born populations in six New York Community Health
18. Nelson RE, Hyun D, Jezek A, Samore MH. Mortality, length of stay, and Centers. Travel Med Infect Dis. 2016;14(6):551–60.
healthcare costs associated with multidrug-resistant bacterial infections 40. Borg MA, Camilleri L, Waisfisz B. Understanding the epidemiology of
among elderly hospitalized patients in the United States. Clin Infect Dis. MRSA in Europe: Do we need to think outside the box? J Hosp Infect.
2021;74(6):1070–80. 2012;81(4):251–6.
19. Chan TC, Cheng VCC, Hung IFN, Chan FHW, Ng WC, Yuen KY. The associa- 41. Al-Orphaly M, Hadi HA, Eltayeb FK, Al-Hail H, Samuel BG, Sultan
tion between methicillin resistant Staphylococcus aureus colonization AA, Skariah S. Epidemiology of multidrug-resistant pseudomonas
and mortality in Chinese nursing home older adults: a 2-year prospective aeruginosa in the Middle East and North Africa Region. mSphere.
cohort. J Am Med Dir Assoc. 2015;9(16):796–7. 2021;6(3):e00202-00221.
20. Moher D, Shamseer L, Clarke M, Ghersi D, Liberati A, Petticrew M, Shekelle 42. Wang L, Qi N, Zhou Y, Zhang H. Prevention and infection control of
P, Stewart LA. Preferred reporting items for systematic review and meta- COVID-19 in nursing homes: experience from China, vol. 49. Oxford:
analysis protocols (PRISMA-P) 2015 statement. Syst Rev. 2015;4(1):1. Oxford University Press; 2020. p. 894–5.
21. Munn Z, Moola S, Riitano D, Lisy K. The development of a critical appraisal 43. Arnold SH, Jensen JN, Bjerrum L, Siersma V, Bang CW, Kousgaard MB,
tool for use in systematic reviews addressing questions of prevalence. Int Holm A. Effectiveness of a tailored intervention to reduce antibiotics for
J Health Policy Manag. 2014;3(3):123–8. urinary tract infections in nursing home residents: a cluster, randomised
22. DerSimonian R, Laird N. Meta-analysis in clinical trials. Control Clin Trials. controlled trial. Lancet Infect Dis. 2021;21(11):1549–56.
1986;7(3):177–88. 44. Netten A, Darton R, Bebbington A, Brown P. Residential or nursing
23. Higgins JP, Thompson SG, Deeks JJ, Altman DG. Measuring inconsistency home care? The appropriateness of placement decisions. Ageing Soc.
in meta-analyses. BMJ. 2003;327(7414):557–60. 2001;21(1):3–23.
24. Munn Z, Moola S, Lisy K, Riitano D, Tufanaru C. Methodological guidance 45. Huang SS, Platt R. Risk of methicillin-resistant Staphylococcus aureus
for systematic reviews of observational epidemiological studies reporting infection after previous infection or colonization. Clin Infect Dis.
prevalence and cumulative incidence data. Int J Evid Based Healthc. 2003;36(3):281–5.
2015;13(3):147–53. 46. Lowy FD. Antimicrobial resistance: the example of Staphylococcus aureus.
25. Barendregt JJ, Doi SA, Lee YY, Norman RE, Vos T. Meta-analysis of preva- J Clin Invest. 2003;111(9):1265–73.
lence. J Epidemiol Community Health. 2013;67(11):974–8. 47. Kupfer M, Jatzwauk L, Monecke S, Möbius J, Weusten A. MRSA in a large
26. Higgins JP, Thompson SG. Quantifying heterogeneity in a meta-analysis. German University Hospital: Male gender is a significant risk factor for
Stat Med. 2002;21(11):1539–58. MRSA acquisition. GMS Krankenhhyg Interdiszip 2010;5(2).
27. Higgins JP, Thomas J, Chandler J, Cumpston M, Li T, Pae MJ, Welch VA. 48. Walker JN, Flores-Mireles AL, Pinkner CL, Schreiber HLT, Joens MS, Park
Cochrane handbook for systematic reviews of interventions. New York: AM, Potretzke AM, Bauman TM, Pinkner JS, Fitzpatrick JAJ, et al. Catheteri-
John Wiley & Sons; 2019. zation alters bladder ecology to potentiate Staphylococcus aureus infec-
28. DerSimonian R, Laird N. Meta-analysis in clinical trials revisited. Contemp tion of the urinary tract. Proc Natl Acad Sci U S A. 2017;114(41):E8721–30.
Clin Trials. 2015;45:139–45. 49. Tenover FC. Mechanisms of antimicrobial resistance in bacteria. Am J
29. Rostami A, Sepidarkish M, Leeflang MM, Riahi SM, Shiadeh MN, Esfand- Med. 2006;119(6):S3–10.
yari S, Mokdad AH, Hotez PJ, Gasser RB. SARS-CoV-2 seroprevalence 50. Zheng Y, He L, Asiamah TK, Otto M. Colonization of medical devices by
worldwide: a systematic review and meta-analysis. Clin Microbiol Infect. staphylococci. Environ Microbiol. 2018;20(9):3141–53.
2021;27(3):331–40. 51. Berbudi A, Rahmadika N, Tjahjadi AI, Ruslami R. Type 2 diabetes and its
impact on the immune system. Curr Diabetes Rev. 2020;16(5):442–9.
Hasanpour et al. Antimicrobial Resistance & Infection Control (2023) 12:4 Page 11 of 11

52. Stacey HJ, Clements CS, Welburn SC, Jones JD. The prevalence of
methicillin-resistant Staphylococcus aureus among diabetic patients: a
meta-analysis. Acta Diabetol. 2019;56(8):907–21.
53. Kwatra G, Cunnington MC, Merrall E, Adrian PV, Ip M, Klugman KP,
Tam WH, Madhi SA. Prevalence of maternal colonisation with group B
streptococcus: a systematic review and meta-analysis. Lancet Infect Dis.
2016;16(9):1076–84.
54. Rostami A, Riahi S, Gamble H, Fakhri Y, Shiadeh MN, Danesh M, Behniafar
H, Paktinat S, Foroutan M, Mokdad A. Global prevalence of latent toxo-
plasmosis in pregnant women: a systematic review and meta-analysis.
Clin Microbiol Infect. 2020;26(6):673–83.
55. Rostami A, Sepidarkish M, Fazlzadeh A, Mokdad AH, Sattarnezhad A,
Esfandyari S, Riahi SM, Mollalo A, Dooki ME, Bayani M. Update on SARS-
CoV-2 seroprevalence: regional and worldwide. Clin Microbiol Infect.
2021;27(12):1762–71.

Publisher’s Note
Springer Nature remains neutral with regard to jurisdictional claims in pub-
lished maps and institutional affiliations.

Ready to submit your research ? Choose BMC and benefit from:

• fast, convenient online submission


• thorough peer review by experienced researchers in your field
• rapid publication on acceptance
• support for research data, including large and complex data types
• gold Open Access which fosters wider collaboration and increased citations
• maximum visibility for your research: over 100M website views per year

At BMC, research is always in progress.

Learn more biomedcentral.com/submissions

You might also like