Journal of Hospital Infection 135 (2023) 37e49

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Journal of Hospital Infection

journal homepage: www.elsevier.com/locate/jhin

Review

A systematic review and meta-analysis of risk factors

associated with healthcare-associated infections
among hospitalized patients in Chinese general
hospitals from 2001 to2022
X. Liu a, *, Y. Long b, C. Greenhalgh a, S. Steeg c, J. Wilkinson a, H. Li b, A. Verma a,
A. Spencer a
a
Division of Population Health, Health Services Research and Primary Care, School of Health Sciences, University of Manchester,
Manchester Academic Health Sciences Centre, Manchester, UK
b
Global Health Institute/School of Health Sciences, Wuhan University, Wuhan, China
c
Division of Psychology and Mental Health, School of Health Sciences, University of Manchester, Manchester Academic Health
Sciences Centre, Manchester, UK

A R T I C L E I N F O S U M M A R Y

Article history: Background: Healthcare-associated infections (HAIs) are a serious global public health
Received 15 September 2022 issue. However, a comprehensive analysis of risk factors for HAIs has yet been undertaken
Accepted 26 February 2023 at a large scale among general hospitals in China. The aim of this review was to assess risk
Available online 11 March 2023 factors associated with HAIs in Chinese general hospitals.
Methods: Medline, EMBASE and Chinese Journals Online databases were searched to find
Keywords: studies published from 1st January 2001 to 31st May 2022. The random-effects model was
Healthcare-associated used to estimate odds ratio (OR). Heterogeneity was assessed based on the b s2 and I2
infections statistics.
Risk factors Results: A total of 5037 published papers were identified from the initial search and 58
General hospitals studies were included in the quantitative meta-analysis; 1,211,117 hospitalized patients
China were incorporated covering 41 regions in 23 provinces of China and 29,737 were identified
Systematic review and meta- as having HAIs. Our review showed that HAIs were significantly associated with socio-
analysis demographic characteristics including age older than 60 years (OR: 1.74 (1.38e2.19)) and
male sex (1.33 (1.20e1.47)); invasive procedures (3.54 (1.50e8.34)); health conditions
such as chronic diseases (1.49 (1.22e1.82)), coma (OR: 5.12 (1.70e15.38)) and immuno-
suppression (2.45 (1.55e3.87)). Other risk factors included long-term bed (5.84 (5.12
e6.66)), and healthcare-related risk factors such as chemotherapy (1.96 (1.28e3.01)),
haemodialysis (3.12 (1.80e5.39)), hormone therapy (2.96(1.96e4.45)), immunosup-
pression (2.45 (1.55e3.87)) and use of antibiotics (6.64 (3.16e13.96)), and longer than 15
hospitalization days (13.36 (6.80e26.26)).
Conclusions: Being male and aged over 60 years, invasive procedure, health conditions,
healthcare-related risk factors, and longer than 15 hospitalization days were the main risk

* Corresponding author. Address: Division of Population Health, Health Services Research and Primary Care, School of Health Sciences, Faculty of
Biology, Medicine and Health, University of Manchester, Oxford Road, Manchester, M13 9PL, UK.
E-mail address: xinliang.liu@postgrad.manchester.ac.uk (X. Liu).

https://doi.org/10.1016/j.jhin.2023.02.013
0195-6701/ª 2023 The Author(s). Published by Elsevier Ltd on behalf of The Healthcare Infection Society. This is an open access article
under the CC BY-NC-ND license (http://creativecommons.org/licenses/by-nc-nd/4.0/).
38 X. Liu et al. / Journal of Hospital Infection 135 (2023) 37e49
factors associated with HAIs in Chinese general hospitals. This supports the evidence base
to inform the relevant cost-effective prevention and control strategies.
on behalf of The Healthcare Infection Society. This is an open access article
under the CC BY-NC-ND license (http://creativecommons.org/licenses/by-nc-nd/4.0/).
Introduction
Healthcare-associated infections (HAIs) are defined as
infections acquired by patients after admittance to a hospital
or other healthcare facility for more than 48 h, which were not
present or incubating at the time of admission. HAIs can appear
during hospital stay or after discharge. They include occupa-
tional infections among health professionals [1]. HAIs are a
serious global public health issue, having a great impact on
patient safety and disease burden [2e6]. HAIs are associated
with increased risks of mortality and morbidity, longer length
of hospitalization and high economic burden [7e10]. In the
USA, 9000 deaths attributable to HAIs were estimated from
1990 to 2002, resulting in a cost of US$ 28 to US$ 45 billion per
year [11]. In addition, HAIs are one of the key drivers of the
increase in occurrence of antimicrobial resistance (AMR)
making infections more complex to treat [12].
The HAI prevalence of hospitalized patients at any given
time in developing countries is 10%, while it is less at 7% in
developed countries reported by the World Health Organ-
ization (WHO) [1]. The risk of HAIs in developing countries is
reported to be between two and 20 times higher than that in
developed countries [1]. China is one of the developing coun-
tries seriously affected by HAIs. Our previous systematic review
and meta-analysis reported that the additional direct eco-
nomic burden attributable to HAIs estimated by the total
medical expenditure, the medicine expenditure and hospital-
ization days per inpatient was U24,881.37, U9,438.46 and
13.89 days in Chinese general hospitals [13].
Risk factors analysis is one way to help health professionals
understand the factors associated with the development of
HAIs and inform the creation of effective infection control
programmes, guidelines and regulations. A risk factor in our
study is defined as an aspect of individual behaviour or life-
style, environmental exposure, inborn or inherited character-
istics associated with an increased occurrence of a disease.
Risk factors including age over 85 years, hospitalization in
intensive care units (ICUs) and indwelling devices are asso-
ciated with an increase in the occurrence of HAIs [14]. Also,
patients who have received antimicrobials or experienced
central vascular catheters are also shown to be more likely to
acquire HAIs [15]. It is essential to identify risk factors for HAIs,
so as to inform the policy makers and hospital managers to
make effective prevention and control measures to reduce the
occurrence of HAIs, thereby reducing mortality, morbidity, and
economic burden, and allocation of the relevant medical
resources to protect vulnerable patients from acquiring HAIs.
Wang et al. conducted a systematic review and meta-
analysis and reported the pooled prevalence of HAIs in main-
land China was 3.12% in 2018 [16]. In the same year, the total
population of China was 1.4 billion [17] and the national hos-
pitalization rate among people presenting at hospital was
18.2% [18]. Therefore, the total number of hospitalized
patients with HAIs was estimated to be 7.95 million.
ª 2023 The Author(s). Published by Elsevier Ltd
Understanding the risk factors for HAIs is especially important
in China for corresponding prevention and control measures,
because the number of hospitalized patients with HAIs is large
and 35e55% of HAIs can be prevented [19]. Several risk-factor
analyses for HAIs studies have been conducted in China. How-
ever, all of them were single-centre studies. Only one sys-
tematic review and meta-analysis on risk factors associated
with HAIs among tuberculosis hospitalized patients has been
undertaken in Chinese hospitals [20]. A comprehensive analysis
of risk factors for HAIs has yet to be undertaken at a large scale
in China. The types of hospitals are categorized into general
hospitals, speciality hospitals, traditional Chinese medicine
hospitals, hospitals of integrated traditional Chinese and
western medicine, ethnic medical hospitals, and nursing care
hospitals. By the end of 2021, the number of general hospitals
was 20,307, accounting for 55.3% of the overall hospitals [21].
Therefore, the aim of this systematic review and meta-analysis
was to assess the risk factors associated with HAIs between
hospitalized patients with HAIs and those without HAIs in Chi-
nese general hospitals. General hospitals refer to large hospi-
tals with a resident medical staff which provide continuous
care to maternity, surgical and medical patients. They are
different from the specialty hospitals, such as maternity hos-
pitals, and are classified into three levels, including primary,
secondary and tertiary hospitals [13].
Methods
Systematic search strategy
The PICO/S (Population, Intervention, Comparison, Out-
come/Study type) tool was deployed and modified to define the
scope of the literature, as follows. Population: hospitalized
patients admitted to Chinese general hospitals for more than
48 h. Exposure: any potential risk factor which many have an
impact on HAIs, defined by the Ministry of Health, China in 2001
[22]. Comparison: hospitalized patients without HAIs. Out-
come: HAIs. Study type: cross-sectional, caseecontrol, or
cohort study.
The Preferred Reporting Items for Systematic Reviews and
Meta-analysis (PRISMA) guidelines were applied to guide our
systematic review and meta-analysis. We selected Medline,
EMBASE and Chinese Journals Online databases (China National
Knowledge Infrastructure (CNKI), Chinese Wan Fang digital
database and Chinese Science and Technique Journals Data-
base (VIP)) as our main databases to search the relevant arti-
cles. The studies published were limited to between 1st
January 2001 and 31st May 2022.
Medical subject heading (MeSH) terms were used as the
keywords in Medline and EMBASE databases to search the
studies published in English. The MeSH terms were “cross
infection/healthcare-associated infections/hospital acquired
infections” AND “risk factors” AND “China”. Terms searched in
the title, abstract and keywords included “healthcare-
 X. Liu et al. / Journal of Hospital Infection 135 (2023) 37e49 39

Identification Medline + Embase VIP database CNKI + WanFang databases

242 4481 352

5037 records after removing duplicated records

185 records excluded because of:

Screening

4794 records excluded which were irrelevant

of risk factors for HAIs among hospitalised Conference abstracts=1
patients in Chinese general hospitals after
screening the titles, abstracts, and keywords Not general hospital or not stating the type of the
study hospitals (N=24)

243 records screened by reading full texts Only description on the landscape of HAIs or
appropriate statistical analysis (N=99)
Eligibility

Repeated data published in different journals or

used in both journal articles and thesis (N=2)
58 full-text articles
Studies on specific units, diseases, or pathogens
assessed for eligibility
etc. (N=3)
No access to full texts (N=4)
Summary of risk factors based on authors’
Included

58 studies included in perspective (N=18)

the meta-analysis
Risk factors summarized by a logistic regression
analysis or chi squire test without specific data or
with inconsistent data for patients with and
without HAIs (N=26)
Diagnosis of HAIs not according to the definition
proposed by Ministry of China in 2001 (N=8)

Figure 1. Flow diagram of literature search. CNKI, China National Knowledge Infrastructure; HAI, healthcare-associated infection; VIP,
Chinese Science and Technique Journals Database; Wangfang database, Chinese Wan Fang digital database.

associated infections/hospital acquired infections/hospital Data abstraction

infections/nosocomial infections”, “risk factors/influencing
factors”, and “China” for the Chinese databases with corre-
sponding Chinese, and the logic word “AND” was used with
these search terms.
Inclusion and exclusion criteria
The inclusion criteria included: (1) observational studies
including a caseecontrol, cohort study, or cross-sectional
design; (2) a multi-centre or a single-centre study; (3) studies
published in either English or Chinese; (4) studies conducted in
a general hospital rather than a specialty hospital; (5) any
studies published between 1st January 2001 and 31st May 2022;
(6) studies conducted in China.
The exclusion criteria included: (1) conference papers,
editorials, or letters; (2) studies using repeated data; (3)
studies conducted in specific hospitals (e.g., maternal and
paediatric hospitals), or units (e.g., neurosurgery), or disease
(e.g., pneumonia), or patients (e.g., old patients or infants), or
infection type (e.g., ventilator-associated pneumonia); (4)
studies only describing the prevalence of HAIs; (5) studies only
describing the characteristics of risk factors from the per-
spectives of health professionals; (6) studies which did not
define HAIs corresponding to the definition developed by Min-
istry of Health, China in 2001 [22]); (7) studies not providing the
specific data and only providing the statistical conclusion.
X.L. and Y.L., the two independent reviewers, each first
searched the relevant literature on risk factors associated
with HAIs from the databases through keywords, titles
and abstracts. Then, both of the reviewers independently
screened the eligibility of the searched literature based on
the inclusion and exclusion criteria. Both reviewers checked
10% of the studies included by the other reviewer to deter-
mine the eligibility. Disagreement on the included studies was
resolved by discussion between the two independent
reviewers.
Quality assessment
Two independent researchers (X.L. and Y.L.) conducted the
quality assessment of the included studies according to the
criteria proposed by the Joanna Briggs Institute (JBI) critical
appraisal tools for cross-section, caseecontrol and cohort
study checklist [23]. Eight questions for a cross-sectional study,
10 questions for a caseecontrol study, and 11 questions for a
cohort study were used to assess the quality. For each ques-
tion, four options (Yes, Unclear, No and Not applicable) were
provided for singe choice. A value was assigned to each answer,
including a range from 0 to 2 points. For example, 2 points were
assigned if the answer was “Yes”. Therefore, the full points
were 16 for a cross-sectional study, while 16, 20 and 22 points
were full for a cross-sectional study, a caseecontrol study and
 40
Table I
Characteristics of the studies included conducted in Chinese general hospitals from 2001 to 2022
Study ID Author (year) [ref. no.] Study design City (province) Study setting Year begun and Number of participants
duration (years) HAIs Non-HAIs
An et al. (2002) [44] Retrospective cross-sectional Zunyi (Guizhou)-0 One tertiary hospital 2001, 1 day 31 481
1 Chen et al. (2002) [45] Retrospective cross-sectional Guiyang (Guizhou)-1 One tertiary hospital 2001, 1 day 53 643
2 Dai et al. (2002) [46] Retrospective cross-sectional Taizhou (Zhejiang)-0 One tertiary hospital 2001, 1 day 66 844
3 Shu et al. (2005) [47] Retrospective cross-sectional Chengdu (Sichuan)-1 One tertiary hospital 2003, 1 month 258 4358
4 Xu et al. (2005) [25] Retrospective case-control Fuzhou (Fujian)-1 One tertiary hospital 2002, 1 72 144
5 Yang (2005) [48] Retrospective cross-sectional Tangshan (Hebei)e One secondary hospital 2002, 2 164 3779
6 Zhang et al. (2005) [49] Retrospective cross-sectional Urumchi (Xinjiang) One tertiary hospital 2004, 1 343 13,775
7 Wang et al. (2006) [50] Retrospective cross-sectional Shaoguan (Guangdong) One tertiary hospital 2002e2005, 3 days 173 2170

X. Liu et al. / Journal of Hospital Infection 135 (2023) 37e49

8 Huang et al. (2007) [29] Retrospective cohort Xiamen (Fujian) One tertiary hospital 2005, 1 88 962
9 Huang (2007) [51] Retrospective cross-sectional Wenling (Zhejiang) One tertiary hospital 2005, 1 day 67 898
10 Chen et al. (2008) [52] Retrospective cross-sectional Jingzhou (Hunan) One tertiary hospital 2007, 6 months 369 13,151
11 Hong et al. (2009) [53] Retrospective cross-sectional Baoji (Shaanxi) One tertiary hospital 2008, 1 day 15 712
12 Fan et al. (2010) [54] Retrospective cross-sectional Xi’an (Shaanxi) One tertiary hospital 2009, 1 day 74 1691
13 He (2011) [55] Retrospective cross-sectional Zhangjiagang (Jiangsu) One secondary hospital 2008, 1 124 1156
14 Zhang et al. (2011) [56] Retrospective cross-sectional Suzhou (Jiangsu) One tertiary hospital 2009e2010, 2 days 81 1790
15 Gao et al. (2011) [26] Retrospective case-control Changchun (Jilin) One tertiary hospital 2009, 3 769 13,768
16 Tan (2012) [57] Retrospective cross-sectional Guangzhou (Guangdong) One tertiary hospital 2009e2011, 3 days 255 5176
17 Yu et al. (2013) [58] Retrospective cross-sectional Shanghai One tertiary hospital 2012, 1 day 31 1343
18 Fu & Yuan (2013) [27] Retrospective case-control Shaoxing (Zhejiang) One tertiary hospital 2011, 1 276 6051
19 Hu (2013) [59] Retrospective cross-sectional Zhangjiajie (Hunan) One tertiary hospital 2010e2012, 3 days 57 2288
20 Tang et al. (2014) [60] Retrospective cross-sectional Yibin (Sichuan) One tertiary hospital 2013, 1 day 55 1760
21 Peng et al. (2014) [61] Retrospective cross-sectional Changzhou (Jiangsu) One tertiary hospital 2013, 1 day 99 2029
22 Li et al. (2014) [62] Retrospective cross-sectional Xi’an (Shaanxi) One tertiary hospital 2013, 1 day 104 2134
23 Wang (2014) [63] Retrospective and prospective Hefei (Anhui) One tertiary hospital 2011, 3 2611 97,114
cross-sectional
24 Zhao & Xuan (2014) [64] Retrospective cross-sectional Luohe (Hebei) One tertiary hospital 2012, 1 day 42 990
25 Hu (2014) [65] Retrospective cross-sectional Nanning (Guangxi) One tertiary hospital 2011e2013, 3 days 135 2877
26 Li et al.-1 (2014) [66] Retrospective cross-sectional Wenzhou (Zhejiang) One tertiary hospital 2013,1 day 193 1805
27 Zhu (2014) [67] Retrospective cross-sectional Tianjin One tertiary hospital 2012, 1 699 44,669
28 Wu (2014) [68] Retrospective cross-sectional Zhengzhou (Henan) One tertiary hospital 2008, 5 2189 98,885
29 Xiao (2014) [69] Retrospective cross-sectional Guangzhou (Guangdong) One tertiary hospital 2010, 3 4302 169,909
30 Liu et al. (2015) [70] Retrospective cross-sectional Langfang (Hebei) One tertiary hospital 2013, 1 day 34 718
31 Liang et al. (2015) [71] Retrospective cross-sectional Xiangyang (Hubei) One tertiary hospital 2012, 1 78 822
32 Jia et al. (2015) [72] Retrospective cross-sectional Jiaxing (Zhejiang) One tertiary hospital 2010
2013, 4 days 160 4786
33 Niu & Yi (2015) [73] Retrospective cross-sectional Chongqing One tertiary hospital 2012, 2 811 20,458
34 Zhang et al. (2015) [74] Retrospective and prospective Tianjin One tertiary hospital 2014, 1 498 45,437
cross-sectional
35 Li (2015) [28] Retrospective case-control Guangzhou (Guangdong) One tertiary hospital 2013, 1 486 485
36 Fu et al. (2016) [30] Retrospective cross-sectional Sanya (Haiman) Four tertiary hospitals 2015, 1 day 170 2952
37 Zhang et al. (2016) [75] Retrospective cross-sectional Beijing One tertiary hospital 2015, 1 day 34 1043
38 Zhang et al.-1 (2016) [14] Retrospective cross-sectional Beijing One tertiary hospital 2012e2014, 3 days 147 3882
39 Maimaiti (2016) [76] Retrospective cross-sectional Urumchi (Xinjiang) One tertiary hospital 2012, 4 2503 126,893
 X. Liu et al. / Journal of Hospital Infection 135 (2023) 37e49 41
a cohort study, respectively. Higher-quality studies, therefore,
204,116 scored more highly.
170,747

12,684

32,729

10,668
4518

1150

6610
6245
2339

4875

4633

5583

7152
560

398

701

844
Statistical analysis

STATA 14.0 software was employed to estimate the pooled

37 unadjusted odds ratios (OR) of the potential risk factors asso-

16
207

156
18
274
147

242
278
165

391
367

516
217
332
200
3934
3524

ciated with HAIs with 95% confidence intervals (95% CIs) by

extracting the portions of potential risk factors between
patients with HAIs and patients without HAIs from the included
2010, 2012, 2014, 3 days

studies. Heterogeneity among studies was assessed based on

the bs2 and I2 statistics and results with a bs2 (P<0.05) and/or I2
2012e2015, 4 days

2014e2016, 3 days

2015e2017, 3 days

2015e2020, 6 days
>50% were considered as heterogeneity existing among stud-
2017, 6 months

ies. A random-effects model and a Forest plot were used to

2015, 4 days
2015, 1 day

2017, 1 day

2018, 1 day

estimate the pooled OR values. The statistical significance

level was set at P<0.05. A funnel plot was presented to show
2013, 4
2015, 2

2015, 1

2014, 3

2018, 2
2014, 6
2013, 6
2018, 1

the publication bias among the included studies. Subgroup

analyses were undertaken to investigate whether year of study
(before and after 2013, when considerable changes to the
medical care system in China occurred) and location of setting
hospital
hospital
hospital
hospital
hospital
hospital
hospital
hospital
hospital
hospital
hospital
hospital
hospital
hospital
hospital
hospital
hospital
hospital

(non-provincial and provincial capitals) had an impact on

potential risk factors associated with HAIs.
tertiary
tertiary
tertiary
tertiary
tertiary
tertiary
tertiary
tertiary
tertiary
tertiary
tertiary
tertiary
tertiary
tertiary
tertiary
tertiary
tertiary
tertiary

Results

Characteristics of eligible studies

One
One
One
One
One
One
One
One
One
One
One
One
One
One
One
One
One
One

Figure 1 shows that a total of 5037 published papers were

Guangzhou (Guangdong)

Hohhot (Inner Mongolia)

Hohhot (Inner Mongolia)

identified from the database search. After screening the full

Changzhou (Jiangsu)

text with the inclusion and exclusion criteria, 58 publications

Zhengzhou (Henan)
Chengdu (Sichuan)

Chengdu (Sichuan)
Guiyang (Guizhou)

Nanning (Guangxi)
Hengyang (Hunan)
Yantai (Shandong)
Shaoyang (Hunan)

Ganzhou (Jiangxi)
Jinan (Shandong)

were included in the quantitative synthesis and meta-analysis

Haikou (Hainan)

Xi’an (Shaanxi)

for the potential risk factors associated with HAIs.

Hefei (Anhui)

Characteristics: synthesis of the included studies

Beijing

Table I shows that a total of 1,211,117 hospitalized patients

were incorporated in the 58 included studies, which covered 41
cross-sectional
cross-sectional
cross-sectional
cross-sectional
cross-sectional
cross-sectional
cross-sectional
cross-sectional
cross-sectional

cross-sectional
cross-sectional
cross-sectional
cross-sectional
cross-sectional
cross-sectional
cross-sectional
cross-sectional

regions in 23 provinces (34 provincial administrative regions in

case-control

total) in China. Of them, 29,737 hospitalized patients were

identified as having HAIs, and 1,181,380 hospitalized patients
were without HAIs. Most of the included studies (52 out of 58)
were cross-sectional studies, while just five studies adopted a
caseecontrol design [24e28]. Only one study was a cohort
Retrospective
Retrospective
Retrospective
Retrospective
Retrospective
Retrospective
Retrospective
Retrospective
Retrospective
Retrospective
Retrospective
Retrospective
Retrospective
Retrospective
Retrospective
Retrospective
Retrospective
Retrospective

study [29]. The majority of the studies (56 of 58) were con-
ducted in tertiary hospitals and all of the general hospitals
were located in cities. Only one study was a multi-centre study
[30].
Zhang et al.-2 (2016) [78]

Description of the potential risk factors among the

Yang & Chen (2021) [92]
Zhong et al. (2018) [84]
Zhang et al. (2017) [82]

Zhang et al. (2019) [88]

Yang et al. (2019) [87]

included studies
Han et al. (2017) [81]

Fan et al. (2020) [91]

Yin et al. (2017) [80]

Wu et al. (2022) [93]

Liu et al. (2017) [79]

Liu et al. (2018) [85]

Liu et al. (2019) [86]

Chen (2020) [89]

Table II shows that a total of 58 potential risk factors were

Wu (2016) [77]

Yin (2018) [24]

Fu (2020) [90]
Lv (2017) [83]

identified from the included studies. The most frequent

potential risk factors studied were age (48 of 58), indwelling
urinary catheter (46 of 58), surgery (42 of 58), gender (41 of
58), ventilator (41 of 58), and arteriovenous cannula (34 of 58).
Potential risk factors of which the frequency was less than 2
were not included in the following meta-analyses. In addition,
because the classification of season confirming HAIs and hos-
pital wards was not consistent in the included studies, neither
40
41
42
43
44
45
46
47
48
49
50
51
52
53
54
55
56
57

were included in the meta-analyses. Although the classification

 42
Table II
Frequency of the potential risk factors identified among the included studies from 2010 to 2022
Potential risk factors/Study ID 1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20 21 22 23 24 25 26 27 28 29 30
1 Age O O O O O O O O O O O O O O O O O O O O O O O
2 Alcohol
3 Arteriovenous cannula O O O O O O O O O O O O O O O O O O
4 Artificial devices
5 Blood transfusion
6 Body Mass Index (BMI)
7 Cardiovascular and cerebrovascular diseases
8 Central/Peripheral arteriovenous catheter
9 Chemotherapy O O O O O O O O O O O O

X. Liu et al. / Journal of Hospital Infection 135 (2023) 37e49

10 Chronic diseases
11 Chronic diseases or low immunity
12 Clinical diagnosis
13 Coma O O
14 Deep vein catheterization O
15 Diabetes mellitus O O O O
16 Disease of blood system O
17 Drainage O O
18 Endoscope
19 Foreign matter implantation O
20 Gastric tube
21 Gender O O O O O O O O O O O O O O O O O O O O O
22 General anaesthesia
23 Glucocorticoids O O
24 Haemodialysis O O O O O O O
25 Health expenses
26 Hormone O O O O O O O O
27 Hypertension
28 Immunosuppression O O O O O O O O O O O
29 Impaired consciousness
30 Indwelling central catheter O O O
31 Indwelling urinary catheter O O O O O O O O O O O O O O O O O O O O O O
32 Infection when admitted O O
33 Intravenous catheterization
34 Intravenous infusion O
35 Invasive procedures O O O O
36 Length of hospitalization O O O O O O O O O O O O
37 Liver cirrhosis O
38 Long-term bed O
39 Malignant tumour O O O O
40 Marriage O
41 Mechanical ventilation
42 Nephropathy
43 Organ transplantation
44 Paracentesis
45 Parenteral nutrition
46 Personality
47 Previous disease history
48 Radiotherapy O O O O O O O O O O
49 Season of confirming HAIs O
50 Smoking
51 Sulks
52 Surgery O O O O O O O O O O O O O O O O O O O O O
53 Tracheal cannula O O
54 Tracheotomy O O O O O O O O O O O O O

X. Liu et al. / Journal of Hospital Infection 135 (2023) 37e49

55 Underlying diseases O O O O
56 Use of antibiotics O O O O O O O
57 Ventilator O O O O O O O O O O O O O O O O O O O O O
58 Wards O O O O

31 32 33 34 35 36 37 38 39 40 41 42 43 44 45 46 47 48 49 50 51 52 53 54 55 56 57 58 Total
O O O O O O O O O O O O O O O O O O O O O O O O O 48
O 1
O O O O O O O O O O O O O O O O 34
O 1
O 1
O 1
O 1
O 1
O O O O O O O 19
O O 2
1
O 1
O O O 5
O O 3
O O O O 8
O 2
O O 3
O 1
1
O 1
O O O O O O O O O O O O O O O O O O O O 41
O 1
O O 4
O O O O O 12
O 1
O O O O 12
O 1
O O O O O O O O O 20

43
(continued on next page)
 44
Table II (continued )
31 32 33 34 35 36 37 38 39 40 41 42 43 44 45 46 47 48 49 50 51 52 53 54 55 56 57 58 Total
O 1
O O O O 7
O O O O O O O O O O O O O O O O O O O O O O O O 46
O 3
O 1
O 2
O O O O O 9
O O O O O O O O O O O O O 25
O O 3
O 2

X. Liu et al. / Journal of Hospital Infection 135 (2023) 37e49

O O O 7
1
O O O O 4
O 1
O 1
O O 1
O 1
O 1
O 1
O O O O O O 16
O O 3
O 1
O 1
O O O O O O O O O O O O O O O O O O O O O 42
O O O O O 7
O O O O O O O O O O O O O O 27
O O O 7
O O O O O O O O O O 17
O O O O O O O O O O O O O O O O O O O O 41
O O O O O 9
Long-term bed refers to a patient who is on bed for a long period. Personality refers to a characteristic of a person. In our review, the personality was classified into three types, including
extrovert, introvert, and neutral. Sulks mean that a person is silent and bad-tempered due to depression or being upset.
 X. Liu et al. / Journal of Hospital Infection 135 (2023) 37e49 45

Table III
The pooled odds ratios (ORs) of the potential risk factors estimated in the meta-analyses between patients with healthcare-associated
infections (HAIs) and patients without HAIs
Risk factors OR [95% CI] bs2(P) I2 (%) P
Age (60 years vs. <60 years) 1.74 [1.38e2.19] 0.2858 (<0.001) 96.2 <0.001*
Arteriovenous cannula 3.73 [2.79e4.99] 0.6374 (<0.001) 97.4 <0.001*
Chemotherapy 1.96 [1.28e3.01] 0.5559 (<0.001) 98.1 0.002*
Chronic diseases 1.49 [1.22e1.82] 0.0000 (0.582) 0.0 <0.001*
Coma 5.12 [1.70e15.38] 1.5127 (<0.001) 98.3 0.004*
Deep vein catheterization 7.57 [1.03e55.91] 2.7531 ((<0.001) 90.4 0.047*
Diabetes mellitus 2.29 [1.21e4.32] 0.7683 (<0.001) 97.2 0.011*
Disease of blood system 12.91 [0.20e849.53] 9.0882 (<0.001) 99.6 0.231
Drainage 2.84 [1.93e4.20] 0.0918 (0.003) 79.0 <0.001*
Gender (Male vs. Female) 1.33 [1.20,1.47] 0.0724 (<0.001) 82.5 <0.001*
Glucocorticoids 2.00 [0.96e4.14] 0.3683 (0.014) 71.6 0.063
Haemodialysis 3.12 [1.80e5.39] 0.4825 (<0.001) 74.2 <0.001*
Hormone 2.96 [1.96e4.45] 0.3357 (<0.001) 91.3 <0.001*
Immunosuppression 2.45 [1.55e3.87] 0.7765 (<0.001) 97.5 <0.001*
Indwelling central catheter 6.79 [4.78e9.65] 0.1520 (<0.001) 84.2 <0.001*
Indwelling urinary catheter 3.58 [2.75e4.66] 0.7620 (<0.001) 98.4 <0.001*
Infection when admitted 1.67 [1.19e2.35] 0.0000 (0.634) 0.0 0.003*
Intravenous infusion 2.84 [1.72e4.67] 0.0000 (0.761) 0.0 <0.001*
Invasive procedures 3.54 [1.50e8.34] 1.2942 (<0.001) 98.2 0.004*
Length of hospitalization (15 days vs <15 days) 13.36 [6.80e26.26] 0.9830 (<0.001) 97.9 <0.001*
Liver cirrhosis 1.28 [1.34e1.45] 0.0000 (0.930) 0.0 <0.001*
Long-term bed 5.84 [5.12e6.66] 0.0075 (0.016) 82.8 <0.001*
Malignant tumour 1.95 [1.02e3.73] 0.7274 (<0.001) 97.5 0.044*
Mechanical ventilation 4.59 [2.08e10.16] 0.6076 (<0.001) 92.8 <0.001*
Radiotherapy 1.50 [0.81e2.78] 0.7311 (<0.001) 89.6 0.203
Surgery 1.64 [1.39e1.94] 0.2326 (<0.001) 93.7 <0.001*
Tracheal cannula 5.35 [3.53e8.11] 0.1927 (<0.001) 91.2 <0.001*
Tracheotomy 10.44 [7.50e14.53] 0.5144 (<0.001) 95.9 <0.001*
Number of underlying diseases (3 vs <3) 2.63 [1.71e4.06] 0.0969 (0.103) 51.5 <0.001*
Use of antibiotics 6.64 [3.16e13.96] 1.6512 (<0.001) 97.3 <0.001*
Ventilator 6.63 [5.41e8.11] 0.3229 (<0.001) 93.3 <0.001*
*Statistical significance at P<0.05.

of the age and length of hospitalization was different among
the included studies, we adopted the most frequent classi-
fication of the age and length of hospitalization in the meta-
analyses.
Quality analysis of all the included studies
As to the 52 cross-sectional studies, the average points were
11.69  1.65, which indicated the quality of the included cross-
sectional studies was moderate (11.69 of 16). The five
caseecontrol studies were of high quality, scoring from 18 to
19. The cohort study was assessed as scoring 15, which indi-
cated moderate quality. This cohort study did not mention any
information about the follow-up design. Chi-squared test or
binary logistic regression was used to infer the statistical sig-
nificance. However, it was not always clear whether unad-
justed or adjusted ORs were reported from the binary logistic
regression, although most of the included studies appeared to
adopt the adjusted ORs according to the results. Quality
assessments of the included studies are exhibited in the sup-
plementary material (Supplementary Tables S1, S2 and S3).
Meta-analyses of all the potential risk factors
As shown in Table III, 31 potential risk factors were included
in the meta-analyses. Most of the potential risk factors (27 of
31), except chronic diseases, infection when admitted, intra-
venous infusion, and liver cirrhosis, had a high heterogeneity (I2
50%) among the studies. Our systematic review and meta-
analysis showed that HAIs in China were significantly asso-
ciated with age older than 60 years (OR: 1.74 (1.38e2.19)) and
male sex (OR: 1.33 (1.20, 1.47)), invasive procedure (OR: 3.54
(1.50e8.34)), including arteriovenous cannula (OR: 3.73
(2.79e4.99)), deep vein catheterization (OR: 7.57
(1.03e55.91)), drainage (OR: 2.84 (1.93e4.20)), indwelling
central catheter (OR: 6.79 (4.78e9.65)), indwelling urinary
catheter (OR: 3.58 (2.75e4.66)), intravenous infusion (OR: 2.84
(1.72e4.67)), mechanical ventilation (OR: 4.59 (2.08e10.16)),
surgery (OR: 1.64 (1.39e1.94)), tracheal cannula (OR: 5.35
(3.53e8.11)), tracheotomy (OR: 10.44 (7.50e14.53)) and ven-
tilator (OR: 6.63 (5.41e8.11)), health conditions such as
chronic diseases (OR: 1.49 (1.22e1.82)), coma (OR: 5.12
(1.70e15.38)), diabetes mellitus (OR: 2.29 (1.21e4.32)) and
46 X. Liu et al. / Journal of Hospital Infection 135 (2023) 37e49
long-term bed stay (OR: 5.84 (5.12e6.66)), healthcare-related
risk factors including chemotherapy (OR: 1.96 (1.28e3.01)),
haemodialysis (OR: 3.12 (1.80e5.39)), hormone therapy (OR:
2.96 (1.96e4.45)), immunosuppression (OR: 2.45 (1.55e3.87)),
more than three underlying diseases (OR: 2.63 (1.71e4.06))
and use of antibiotics (OR: 6.64 (3.16e13.96)), and longer than
15 hospitalization days (OR: 13.36 (6.80e26.26)). All the P-
values were less than 0.05. The specific information about the
Forest plots of the risk factors is presented in the Supple-
mentary data. Moreover, the publication bias with the funnel
plots is also shown in the Supplementary data and indicates
that publication bias was presented among all included studies
for each of the listed risk factors. Furthermore, the subgroup
analyses by year and capital cities were also shown in the
Supplementary data. Except for some risk factors, including
hormone therapy, invasive procedure (indwelling central
catheter, tracheotomy, ventilator), length of hospitalization,
and use of antibiotics, the OR values were similar.
Discussion
To our best knowledge, our systematic review and meta-
analysis was the first to comprehensively assess the risk fac-
tors associated with HAIs in Chinese general hospitals at a
national level. This review incorporated a total of 1,211,117
hospitalized patients, which were distributed in 41 regions in
23 provinces (34 provincial administrative regions in total) of
China. Our systematic review and meta-analysis showed that
HAIs in Chinese general hospitals are significantly associated
with socio-demographic, invasive procedure, health con-
ditions, healthcare-related risk factors, and longer hospital
stays.
Our review found that patients older than 60 years or male
patients were more likely to get HAIs. In line with our findings,
Iskender et al. undertook a prospective cross-sectional study in
a teaching hospital of Turkey and found the HAIs prevalence
was higher among elderly patients (aged over 65 years: 15.1)
than those patients aged under 65 years (2.9) [31].
Elderly patients are potentially an immune-comprised pop-
ulation. Moreover, elderly patients commonly have other
comorbidities, such as cardiovascular disease, cancer, and
chronic obstructive pulmonary disease [32], factors which
further reduce the immunity of the elderly. A three-year sur-
veillance study on HAIs among elderly patients in a large Chi-
nese tertiary hospital also confirmed that the higher incidence
of HAIs in the elderly may be attributable to the higher rates of
comorbidities [32]. Elderly patients should be prioritized in the
surveillance, prevention and management of HAIs. A cross-
sectional study undertaken among elderly hip fracture
patients also showed that male patients were more susceptible
to obtaining HAIs [33]. However, this study did not discuss
potential mechanisms for the impact of gender on the occur-
rence of HAIs. Therefore, further study is needed to investigate
any differential compliance to the HAIs prevention and control
measures or personal behaviour, such as hand washing using
alcohol-based rubs or smoking between males and females.
We also found that patients exposed to invasive procures
were more vulnerable to acquiring HAIs. This finding is con-
sistent with those studies conducted in Slovenia [34] and
Ethiopia [35]. The systematic review and meta-analysis con-
ducted by Rodrı́guez-Acelas et al. concluded that mechanical
ventilation was an independent risk factor associated with an
increased HAI rate (OR:12.95 (6.28e26.73)) [36], which is
higher than the OR of mechanical ventilation (4.59
(2.08e10.16)) in our review. Moreover, the systematic review
and meta-analysis conducted in Ethiopia found that patients
who had surgery were more likely to get HAIs (OR: 3.37
(1.85e4.89)) [35], which was higher than our OR of surgery in
the current review (1.64 (1.39e1.94)). Metsini et al. conducted
a point prevalence survey of HAIs in three large Swiss acute-
care hospitals and reported that having a medical device,
such as peripheral venous catheter, central venous catheter,
urinary catheter, endotracheal tube, was an independent risk
factor for HAIs (OR: 4.43 (3.49e5.63)) [37], which is similar to
the OR of invasive procedures (3.54 (1.50e8.34)) in our review.
These findings confirm that invasive procedures are a sig-
nificant hazard for hospitalized patients for acquiring an HAI.
Surgical site infection (SSI) is one of the most common HAIs
[38]. In order to control the occurrence of HAIs among patients
undergoing invasive procedures, it is essential to control the
duration of exposure to medical invasive devices, such as
arteriovenous cannula, central venous catheter, indwelling
urinary catheter, mechanical ventilation, and ventilator. Fur-
thermore, it is vital to comply with disinfection measures to
reduce the SSI rate.
Another finding in our review was that patients with
underlying diseases or comorbidities such as diabetes mellitus
and liver cirrhosis were at greater risk of HAIs. A systematic
review and meta-analysis conducted in Ethiopia also found that
underlying non-communicable diseases place patients at
greater risk of HAIs (OR: 2.81 (1.39e4.22)) [35]. This may be
due to underlying diseases weakening the immune system. Two
previous studies have described how Type 2 Diabetes and cir-
rhosis could cause dysfunction of the immune response,
therefore failing to prevent the invading pathogens [39,40].
Long-term bed stays were also found to be a significant risk
factor associated with HAIs, though this has not been well
studied in current literature, and it also indicated that the
sample size was not sufficient in our review. There is a need to
collect empirical data to explore the underlying mechanism,
and make corresponding prevention and control measures to
reduce the HAIs rate among these patients.
Healthcare-related risk factors including chemotherapy,
haemodialysis, hormone therapy, and use of antibiotics were
also found to significantly increase the risk of acquiring HAIs for
patients in our review. However, the effects of chemotherapy,
haemodialysis, and hormone therapy are not well investigated
in existing literature, and further empirical data are needed.
Some studies have found that use of antibiotics is related to an
increased HAIs rate, such as the long-time use of antibiotics
[41], the excessive volume of antibiotics use, and prophylactic
antimicrobial therapy [42]. These studies highlight the irra-
tional use of antibiotics, which ultimately results in anti-
microbial resistance (AMR), a well-known global health issue.
Therefore, antimicrobial stewardship programmes or cam-
paigns are pivotal to make appropriate use of antibiotics. It is
also essential to control and monitor the health professionals’
prescription behaviour to prevent irrational use of antibiotics.
Likewise, the public’s knowledge, attitudes, and practices
relating to the use of antibiotics are also important. It is nec-
essary to increase the awareness of the public and health
professionals to achieve the goal of prudent high-quality anti-
biotics use.
 X. Liu et al. / Journal of Hospital Infection 135 (2023) 37e49
Hospitalization stays longer than 15 days were recognized as
a significant risk factor associated with the increased occur-
rence of HAIs in our review and has been well investigated in
current literature [20,43]. It is possible for hospitalized
patients to be predisposed to HAIs for prolonged hospital-
ization. Consequently, patients are more susceptible to HAIs.
Therefore, it is important to place patients with long hospi-
talization under surveillance, especially those patients with
extremely long hospitalization, and prioritize safely shortening
hospitalization stays.
There are likely interactions between the risk factors
associated with HAIs in our review. For example, elderly
patients, underlying diseases or comorbidities, and therapy of
immunosuppression were the three significant risk factors
associated with HAIs according to our meta-analyses. Elderly
patients require long-term care and immunosuppressive ther-
apy, and they are more likely to have underlying disease or
comorbidities [31,32]. Therefore, comprehensive prevention
and control measures need to be taken according to the
evidence-based risk factors to reduce the burden attributable
to HAIs.
Our systematic review and meta-analysis has some limi-
tations. First, the included studies were mostly published in
Chinese journals, which constrain the large scale of research-
ers from other countries in sharing the knowledge. Second, we
also found that most of the included studies were single-centre
studies. Multi-centre studies are needed to provide more
robust findings. Third, our review shows that the publication
bias among the included studies for all the potential risk factors
existed, and the unadjusted ORs were calculated. Therefore,
the relationships between the potential risk factors and HAIs
might be overstated. It is better to estimate the adjusted ORs
by controlling the potential confounders.
In conclusion, age older than 60 years and male sex, invasive
procedure including arteriovenous cannula, deep vein cathe-
terization, drainage, indwelling central catheter, indwelling
urinary catheter, intravenous infusion, mechanical ventilation,
surgery, tracheal cannula, tracheotomy and ventilator, health
conditions as chronic diseases, coma, diabetes mellitus and
long-term bed stay, healthcare-related risk factors including
chemotherapy, haemodialysis, hormone therapy, immunosup-
pression, more than three underlying diseases and use of
antibiotics, and longer than 15 hospitalization days were
established as the main risk factors among hospitalized
patients with HAIs compared with those without HAIs in Chi-
nese general hospitals. Our review could help health pro-
fessionals and service managers to make corresponding
prevention and control measures to reduce the occurrence of
HAIs. It is necessary to conduct further empirical research to
confirm some risk factors for HAIs which are not well docu-
mented in current literature.
Author contributions
X.L. drafted and revised the systematic review and con-
ducted the meta-analyses. X.L. and Y.L. searched the tar-
geted databases to find the relevant articles and assessed
the quality of the included studies. A.S., A.V., C.G., and S.S.
commented on the systematic review. J.W. recommended
the methodology of the systematic review. H.L. commented
on the discussion of the systematic review. X.L. and A.S.
designed the systematic review framework. A.S. and C.G.
proofread the whole systematic review.
47
Conflict of interest statement
The authors declare no potential conflicts of interest with
respect to the research, authorship, and/or publication of
this article.
Funding sources
This research did not receive any specific grant from funding
agencies in the public, commercial, or not-for-profit
sectors.
Appendix A. Supplementary data
Supplementary data to this article can be found online at
https://doi.org/10.1016/j.jhin.2023.02.013.
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