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Journal of Hospital Infection xxx (2016) 1e9

Available online at www.sciencedirect.com

Journal of Hospital Infection


journal homepage: www.elsevierhealth.com/journals/jhin

Point-prevalence survey of healthcare-associated


infections in Beijing, China: a survey and analysis in
2014
J.Y. Liu a, Y.H. Wu b, *, M. Cai a, C.L. Zhou c
a
Division of Hospital Infection Control and Prevention, Beijing Hospital, Beijing, China
b
Division of Hospital Infection Control and Prevention, Peking University People’s Hospital, Beijing, China
c
Division of Hospital Infection Control and Prevention, Beijing Friendship Hospital, Capital Medical University, Beijing, China

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

Article history: Background: Point-prevalence studies can identify priorities for infection control.
Received 1 October 2015 Aim: In May 2014, the Beijing Nosocomial Infection Control and Quality Improvement
Accepted 16 March 2016 Centre organized a point-prevalence survey in 124 acute care hospitals in Beijing province.
Available online xxx By analysing the survey results and factors affecting the point prevalence of healthcare-
associated infections (HCAIs) in secondary and tertiary acute care hospitals in a certain
Keywords: area of China, this study provides evidence and reference to monitor HCAIs in a wide
Healthcare-associated variety of hospitals.
infections Methods: An epidemiological cross-sectional survey conducted by infection control
Monitoring practitioners was used to assess the point-prevalence rate of HCAIs by reviewing cases and
Point-prevalence survey performing bedside surveys.
Findings: In total, 124 hospitals and 61,990 patients were surveyed, and 1389 (2.2%) HCAIs
were diagnosed in 1294 (2.1%) patients. Respiratory tract infections were the most com-
mon HCAIs (54.4%, 51.7e56.9%), followed by urinary tract infections (15.0%, 13.2e16.9%),
gastrointestinal tract infections (7.7%, 6.3e9.1%), surgical site infections (6.3%, 5.1e7.6%)
and bloodstream infections (5.5%, 4.3e6.8%). In this survey, the top three pathogens were
Pseudomonas aeruginosa, Acinetobacter baumannii and Escherichia coli. Rates of central
vein catheter insertion, urethral catheterization and mechanical ventilation were 9.9%,
12.4% and 3.8%, respectively. Overall, 23.7% of the patients underwent surgery on or
before the date of the survey. HCAIs were present in 14.5% of intensive care unit patients,
2.3% of medical patients and 2% of surgical patients. Diarrhoea was found in 0.8% of the
assessed cases; however, tests for Clostridium difficile are not routinely available in
China.
Conclusion: In areas with limited personnel and resources, regular investigation of the
point prevalence of HCAIs can be performed in lieu of comprehensive monitoring to
elucidate risk factors and disease burdens of HCAIs.
ª 2016 Published by Elsevier Ltd on behalf of The Healthcare Infection Society.

* Corresponding author. Address: No. 11 Xizhimen South Street,


Xicheng District, Beijing 100044, China. Tel.: þ86 10 88325504.
E-mail address: 593857975@qq.com (Y.H. Wu).

http://dx.doi.org/10.1016/j.jhin.2016.03.019
0195-6701/ª 2016 Published by Elsevier Ltd on behalf of The Healthcare Infection Society.

Please cite this article in press as: Liu JY, et al., Point-prevalence survey of healthcare-associated infections in Beijing, China: a survey and
analysis in 2014, Journal of Hospital Infection (2016), http://dx.doi.org/10.1016/j.jhin.2016.03.019
2 J.Y. Liu et al. / Journal of Hospital Infection xxx (2016) 1e9

Introduction (1e100 beds), secondary or second class hospitals (101e500


beds), and tertiary or third class hospitals (>500 beds). Primary
Healthcare-associated infections (HCAIs) are a major public and secondary hospitals mainly provide basic services, whereas
health issue due to their association with significant morbidity tertiary hospitals are referral centres for specialist care with
and mortality, prolongation of hospital stays and increased medical teaching and research. On 21st May 2014, the BNICC
costs of care. For example, in the USA, there are 2e3 million conducted point-prevalence surveys in tertiary and secondary
HCAIs each year, resulting in approximately 88,000 deaths and hospitals (rehabilitation hospitals, gerontological centres,
an economic loss of approximately $4.5 billion.1 The preva- community and township hospitals were not included) that
lence of HCAIs is closely associated with the regional economic applied for the Management System for Healthcare-Associated
level, the level of medical services, race, diet, lifestyle and Infections Monitoring programme.
behaviours.2e9 In addition, HCAI surveillance standards and The survey included all patients at the hospital at 0:00 h on
control measures affect their prevalence. Surveys conducted 21st May 2014 and patients who were discharged on the same
worldwide2e9 have demonstrated an inverse relationship be- day. Patients who were admitted to the hospital after 0:00 h on
tween HCAIs and national prosperity, although the diagnostic 21st May 2014 were not included.
criteria vary between countries. The surveillance standards in
most countries incorporate the definitions and diagnostic Data collection and definitions
criteria for healthcare-associated surveillance established by
the US Centers for Disease Control and Prevention (CDC).10 The definition of HCAIs used in this study is widely used in
The gold standard for HCAI surveillance is a large, pro- China, and was established by the Ministry of Health in 2001
spective, continuous, hospital-wide, incidence survey. How- [issued by the Hospital Infection Diagnostic Criteria (Trial)].20
ever, few hospitals opt for this approach because incidence Medical records were reviewed for HCAIs according to the
surveys require a significant amount of manpower, material abovementioned definition, modified from the case definitions
resources and a greater number of trained personnel.11,12 of the US CDC (1988). The main differences involve the cate-
Point-prevalence surveys are simple, fast and relatively inex- gorization of respiratory tract infection (RTI) and the definition
pensive compared with incidence surveys. Performing targeted of infection in patients aged 12 months. In China, the case
and sustained active surveillance helps explore the root causes definition of RTI includes the CDC categories of ‘pneumonia’,
of HCAIs in order to improve management and prevention.12e16 ‘lower respiratory tract infection other than pneumonia’ and
In addition, point-prevalence surveys of HCAIs are an important ‘upper respiratory tract infection’. In addition, patients aged
method for inter-regional and international monitoring and 12 months are listed independently in the CDC definitions
comparison. In China, the Healthcare-associated Infections from 1988, whereas in China, they are included in the overall
Surveillance Network of the Ministry of Health has conducted population numbers, except for cardiovascular and central
six nationwide point-prevalence surveys.17e19 The point prev- nervous system infections.
alence of HCAIs was 5.22% in 2001 (107,466 inpatients were
surveyed, 5614 HCAIs were found), 4.81% in 2003 (89,539 in- Survey
patients were surveyed, 4309 HCAIs were found), 4.77% in 2005
(115,143 inpatients were surveyed, 5492 HCAIs were found), An epidemiological, cross-sectional design was used. The
3.60% in 2010 (407,208 inpatients were surveyed, 14,674 HCAIs medical institutions participating in the point-prevalence sur-
were found), and 3.22% in 2012 (786,028 inpatients were sur- vey on the survey date (21st May 2014) used the Point-
veyed, 25,273 HCAIs were found); the prevalence in 2014 has prevalence Survey Form of Healthcare-associated Infections
not yet been published. This indicates a downward trend, issued by the BNICC to survey the hospitalized patients. Ac-
which may indirectly reflect the effect of surveillance and cording to Staff Responsibilities of Data Collection in the Survey
national infection control efforts that have been in place for Program of Prevalence of Healthcare-Associated Infections,
more than 10 years. Point-prevalence studies of HCAIs can also 2014 by the BNICC, staff in all positions were responsible for
provide a basis for health administrators to understand na- the organization, implementation and quality control of the
tional HCAI trends and design appropriate policies and regu- entire survey process.
lations. To enhance current understanding of these trends and There were three trained physicians in the team of vali-
evaluate infection control efforts in Beijing, the Beijing Noso- dators. All team members had been trained for over 8 h at the
comial Infection Control and Quality Improvement Centre BNICC. All face-to-face and case surveys were combined, and
(BNICC) initiated a point-prevalence survey of HCAIs in 2014. the use of antibiotics and test results were verified. The case
survey focused on temperature records, diagnosis at admis-
sion, imaging and laboratory test results. In compliance with
Methods the Hospital Management Assessment Guide, 2008 by the Min-
istry of Health and the Point-prevalence Survey Questionnaire
Study design and hospital selection of Healthcare-Associated Infections issued by the BNICC,
infection control practitioners (ICPs) completed a supple-
Hospitals in China are classified into the following four mental questionnaire using medical notes for patients under-
categories: hospitals within the public health system; hospitals going surgery at the time of the survey or patients who had
affiliated with medical education and research institutes; been discharged. In each ward, completed survey question-
military hospitals; and ‘other’, which includes private hospi- naires were checked individually to ensure completion of
tals. The first two types are the most common in China as well missing items and to avoid errors. The collected data were
as in Beijing province. In 1993, the Chinese Ministry of Health reported to the HCAI control department, where the staff
subdivided hospitals according to size into primary hospitals checked, completed and corrected the data.

Please cite this article in press as: Liu JY, et al., Point-prevalence survey of healthcare-associated infections in Beijing, China: a survey and
analysis in 2014, Journal of Hospital Infection (2016), http://dx.doi.org/10.1016/j.jhin.2016.03.019
J.Y. Liu et al. / Journal of Hospital Infection xxx (2016) 1e9 3
The survey content included HCAI status, use of invasive ICPs collected survey questionnaires on each ward and
devices and surgical procedure details (venous catheter, uri- checked if questionnaires were fully completed. Data were
nary catheter, ventilator, surgical and peri-operative entered on to the HCAI control management system, and ICPs
medication). verified the information once again to avoid bias from typo-
graphical errors.
Quality control
Data analysis
To improve the authenticity of information, the results
needed to reflect the prevalence of HCAIs in Beijing objec- After data collection, the data analysis staff of the BNICC
tively. Therefore, the measures described below were taken to exported the data to a spreadsheet and established a data-
control possible biases and to ensure effective quality control base. Statistical analyses were performed using Statistical
for the survey. Package for the Social Sciences Version 21.0 (IBM Corp.,
Armonk, NY, USA). The prevalence of HCAIs and the prevalence
Selection bias control of HCAI patients were calculated, together with 95% confi-
dence intervals (CIs). Categorical differences were calculated
A census survey of all patients hospitalized on the survey using Chi-squared test. When P<0.1 was observed under uni-
date was obtained to avoid sampling errors and to control for variate analysis of risk factors, logistic regression was entered
selection bias. to check for possible interaction or confounding variable ef-
fects. Correlation among variables was examined using Pear-
son’s correlation model. All P-values calculated were two-
Information bias control tailed, and P<0.05 was considered to indicate statistical
significance.
Staff from medical institutions taking part in the survey
underwent training to understand the purpose and procedures
correctly, including diagnostic criteria and survey methods. Results
This resulted in greater awareness and better standardization
during questionnaire completion. The questionnaires collected Actual survey rate
from each ward were checked for missed entries, errors and
incorrect information. To ensure that every diagnosed case was All secondary and tertiary hospitals that met the inclusion
recorded accurately, proofreading was undertaken and HCAI criteria participated in this survey (N¼124 medical in-
cases detected in this survey were rechecked to avoid errors. stitutions). The participation rate was 100%. Of the 124

18

16 ICU

14
Patients with HCAIs (%)

12

10
Medicine Surgery
8

6 Other
Paediatrics
Gynaecology Ophthalmology &
4 & obstetrics otorhinolaryngology

Figure 1. Prevalence of healthcare-associated infections (HCAIs) in different departments. Note: (1) Within Medicine, the groups are
listed, in the order of lowest to highest percentage of HCAIs, as follows: Internal secretion group, Angiocarpy group, Respiratory group,
Digestion group, Traditional Chinese medicine group, Neurology group, Infectious disease group, Other (medicine), Oncology group,
Nephropathy group and Haemopathy group. (2) Within Surgery, the groups are listed as follows: Plastic surgery, Orthopaedics depart-
ment, Other (surgery department), General surgery department, Urinary surgery, Burns department, Cardiac surgery, Chest surgery and
Neurosurgery. (3) Within Gynaecology and Obstetrics, the groups are listed as follows: Obstetrics-neonatal group, Gynaecology and
Obstetrics-adult group. Within Paediatrics, the groups are listed as follows: Paediatrics-non-infant group, Paediatrics department
intensive care unit (ICU) and Paediatrics department-infant group. (4) Within Ophthalmology and Otorhinolaryngology, the groups are
listed as follows: Other (ENT), ENT department, Ophthalmology and Stomatology department. (5) Within ICU, the groups are listed as
follows: Medicine ICU, Surgery ICU and Comprehensive ICU. Within Other, the groups are listed as follows: Psychiatry and Other. Grey bars
indicate the percentage of departments (e.g. Medicine, Surgery, etc.); black bars indicate the percentage of groups.

Please cite this article in press as: Liu JY, et al., Point-prevalence survey of healthcare-associated infections in Beijing, China: a survey and
analysis in 2014, Journal of Hospital Infection (2016), http://dx.doi.org/10.1016/j.jhin.2016.03.019
4 J.Y. Liu et al. / Journal of Hospital Infection xxx (2016) 1e9
surveyed medical institutions, 25 were excluded because of a 61,908), and the ICU rate was 49.6% (479/965). The overall
very low questionnaire completion rate (<5%), a higher number urinary tract catheterization rate was 12.4% (7684/61,908),
of completed questionnaires compared with the number of and the ICU rate was 67.3% (649/965). In total, 23.7% of the
patients in hospital, and failure to reveal the total number of patients underwent surgery prior to the survey date, and 0.8%
patients present in the hospital. Of the remaining 99 medical of patients had experienced more than three episodes of
institutions, 95 had a questionnaire completion rate of >95% diarrhoea in the 24 h preceding the survey date.
which is in line with the requirements for prevalence surveys in Table III shows several risk factors for HCAIs by univariate
China and Beijing. The total survey completion rate was 97.8% and multi-variate analyses. In the overall logistic regression
(50,554/51,674), which meets the compliance requirement model, the following risk factors were independently associ-
(95%) of the Beijing Municipal Health Bureau. ated with HCAI: male sex, 65 years of age, 28 days of age,
ICU admission, tertiary hospital admission, non-traditional
Prevalence and infection sites Chinese medicine hospital admission, invasive device use

In total, 61,990 patients and 62,087 cases were surveyed,


and 61,908 and 62,003 met the inclusion criteria, respectively. Table I
Patients were considered to be ineligible if data were missing Infection site distribution in the Beijing 2014 point-prevalence
from the survey questionnaire. In the 61,908 cases, 1389 (2.2%, study of healthcare-associated infections
2.1e2.4%) HCAIs were reported from 1294 (2.1%, 2.0e2.2%)
Type of infection No. of Proportion of all healthcare-
patients. There was a significant difference in the prevalence
infections associated infections (N¼1389)
of HCAIs between secondary and tertiary hospitals (P<0.05).
(%) (95% CI)
Across the range of hospital departments, the prevalence of
HCAIs in intensive care units (ICUs) was 14.5%, which was Respiratory system 755 54.4 (51.7e56.9)
greater than the prevalence of HCAIs in internal medicine Lower respiratory 649 46.7 (44.1e49.4)
(2.3%) and surgical (2.0%) departments. The prevalence of tract
HCAIs was lowest in the ophthalmology and otorhinolaryn- Upper respiratory 95 6.8 (5.5e8.2)
gology departments (0.3%) (Figure 1). tract
RTI was the most prevalent HCAI (54.4%, 51.7e56.9%), fol- Pleural cavity 11 0.8 (0.3e1.3)
lowed by urinary tract infection (15.0%, 13.2e16.9%), gastro- Urinary tract 209 15.0 (13.2e16.9)
intestinal infection (7.7%, 6.3e9.1%), surgical site infection Gastrointestinal 107 7.7 (6.3e9.1)
(6.3%, 5.1e7.6%) and bloodstream infection (5.5%, 4.3e6.8%) system
(Table I). In patients with lower respiratory infection, chest Gastrointestinal 55 4.0 (2.9e5.0)
radiography indicated that only 47.9% (311 patients) had tract
radiological evidence of pneumonia. Intra-abdominal 52 3.7 (2.8e4.7)
Surgical site 88 6.3 (5.1e7.6)
Micro-organisms Superficial 56 4.0 (3.0e5.1)
incisional
Most HCAIs were diagnosed by physical symptoms and radi- Deep incisional 20 1.4 (0.8e2.1)
ography, and 85% (1187/1389) of infections were confirmed Organ/space 12 0.9 (0.4e1.4)
microbiologically; from these, 745 taxa of pathogenic bacteria Bloodstream 77 5.5 (4.3e6.8)
were isolated. The top five pathogens isolated were Pseudo- Primary 63 4.5 (3.4e5.6)
monas aeruginosa, Acinetobacter baumannii, Escherichia coli, bloodstream
Klebsiella pneumoniae and Staphylococcus aureus (Table II). infection
P. aeruginosa was most frequently detected from infections Catheter-related 14 1.0 (0.5e1.5)
involving the lower respiratory tract (73.1%, 68/93), urinary bloodstream
tract (8.6%, 8/93) and abdomen (3.2%, 3/93). A. baumannii was infection
most frequently detected from infections involving the lower Central nervous 52 3.7 (2.8e4.7)
respiratory tract (86.2%, 75/87), abdomen (3.4%, 3/87) and system
urinary tract (3.4%, 3/87). E. coli was most frequently detected Skin and soft tissue 39 2.8 (1.9e3.7)
from infections involving the urinary tract (47.2%, 42/89), Skin or soft tissue 38 2.7 (1.9e3.6)
surgical wounds (11.2%, 10/89) and lower respiratory tract infection
(11.2%, 10/89). Burn infection 1 0.1 (0.0e0.2)
System infection 30 2.2 (1.4e2.9)
Baseline and factor distribution Eye, ear, nose, 12 0.9 (0.4e1.4)
throat and mouth
Among the 61,908 patients surveyed, there were more men Reproductive tract 8 0.6 (0.2e1.0)
than women, and the mean age was 53.90 (standard deviation Cardiovascular 7 0.5 (0.1e0.6)
22.12) years. Individuals aged 45e64 years represented the system
largest set of patients. Of the surveyed hospitals, 13.1% were Endocarditis 4 0.3 (0.0e0.6)
traditional Chinese medicine hospitals. In this survey, the Myocarditis or 3 0.2 (0.0e0.5)
overall invasive ventilation rate was 3.8% (2374/61,908), and pericarditis
the ICU invasive ventilation rate was 44.2% (427/965). The Bone and joint 5 0.4 (0.1e0.7)
overall central venous catheter insertion rate was 9.9% (6149/ CI, confidence interval.

Please cite this article in press as: Liu JY, et al., Point-prevalence survey of healthcare-associated infections in Beijing, China: a survey and
analysis in 2014, Journal of Hospital Infection (2016), http://dx.doi.org/10.1016/j.jhin.2016.03.019
J.Y. Liu et al. / Journal of Hospital Infection xxx (2016) 1e9 5

Table II
Healthcare-associated infection (HCAI) pathogen composition in the Beijing 2014 point-prevalence study of HCAIs
Pathogen All HCAI patients Lower Urinary Upper Primary bloodstream Surgical site (superficial
(N¼1389) respiratory tract respiratory infection (N¼63) incisional) (N¼56)
N (%) tract (N¼209) tract N (%) N (%)
(N¼649) N (%) (N¼95)
N (%) N (%)
Pathogen Rank 745 (53.6) 380 (67.5) 121 (57.9) 18 (27.7) 56 (88.9) 32 (0.6)
detected
Pseudomonas 1 103 (13.8) 76 (20.0) 8 (6.6) 1 (5.6) 2 (3.6) 3 (9.4)
aeruginosa
Acinetobacter 2 96 (12.9) 81 (21.3) 3 (2.5) 2 (11.1) 2 (3.6) 1 (3.1)
baumannii
Escherichia coli 3 94 (12.6) 13 (3.4) 39 (32.2) 1 (5.6) 11 (19.6) 10 (31.3)
Klebsiella 4 71 (9.5) 47 (12.4) 5 (4.1) 2 (11.1) 3 (5.4) 1 (3.1)
pneumoniae
Staphylococcus 5 66 (8.9) 30 (7.9) 1 (0.8) 2 (11.1) 9 (16.1) 7 (21.9)
aureus
Candida albicans 6 39 (5.2) 13 (3.4) 14 (11.6) 0 (0.0) 2 (3.6) 0 (0.0)
Enterococcus 7 38 (5.1) 2 (0.5) 18 (14.9) 0 (0.0) 4 (7.1) 0 (0.0)
Enterobacter 8 26 (3.5) 11 (2.9) 4 (3.3) 0 (0.0) 3 (5.4) 3 (9.4)
cloacae
Other fungi 9 22 (3.0) 9 (2.4) 4 (3.3) 0 (0.0) 1 (1.8) 0 (0.0)
Staphycoccus 10 14 (1.9) 2 (0.5) 1 (0.8) 0 (0.0) 4 (7.1) 2 (6.3)
epidermidis
Others 11 176 (23.6) 96 (25.3) 24 (19.8) 10 (55.6) 15 (26.8) 5 (15.6)
No pathogenic 440 (31.7) 183 (32.5) 55 (26.3) 49 (75.4) 6 (9.5) 12 (0.2)
bacteria
detected
No samples 204 (14.7) 86 (15.3) 33 (15.8) 28 (43.1) 1 (1.6) 12 (0.2)
submitted

(central venous catheter insertion, urinary tract catheteriza- Infectious Disease (People’s Republic of China, Presidential
tion and invasive ventilation), surgery and presence of diar- Decree No.48), issued in 2004; Nosocomial Infection Manage-
rhoea (Figure 2). ment Method (Ministry of Health of People’s Republic of China,
Decree No.48), issued in 2006; Technique Standard for Isolation
Discussion in Hospital (WS/T 311-2009), issued in 2009; and Management
Standard for Hospital Sterilization and Supply Center (WS310-
Analysis of HCAIs 2009) and Technical Standard for Disinfection of Medical
Institution (WS 36-2012), issued in 2012. In addition, the Beijing
The prevalence survey results from 2014 were similar to Health Administration Department has also issued many doc-
those from 2012. The prevalence of HCAIs in Beijing from 2006 uments to regulate the management of nosocomial infections
to 2014 shows a downward trend, and the overall prevalence in and environmental health sanitation in Beijing City. These
2014 was lower than the national prevalence rate in 2012 include Rules for the Implementation of Nosocomial Infection
(3.2%).19 Compared with the prevalences of HCAIs in other Prevention and Control Plan (2013e2015), and Environmental
Chinese provinces and cities, the prevalence in Beijing was Health Technology and Management Standard of Beijing Medi-
close to the lower end of the range. Over the past 10 years, the cal Institution. These laws and regulations, as well as technical
prevalence of HCAIs in China and Beijing has been declining, for specifications, form the legal basis for infection control in
which there are several possible reasons. Although infection Chinese hospitals.
prevention and control in Chinese hospitals began only The highest prevalence of HCAIs was in ICUs, which is
recently, rapid development has been witnessed over the past consistent with other research performed in China and other
10 years. This has been driven by national legislation; hygiene countries.2,3,19 This is likely to be related to factors that pre-
standards and technical specifications issued by the Health dispose to HCAIs, including the critical condition of patients,
Administrative Department of State Council. Laws and regula- immune dysfunction, and invasive procedures such as ventila-
tions, as well as industry standards, have defined higher re- tion and catheterization.
quirements in order to prevent nosocomial infections. The lower respiratory tract was one of the main HCAI sites in
Standards and legislation include: Technical Standard for this survey; these infections were substantially more common
Disinfection (Health Administrative Department of People’s than surgical site infections. This is similar to the results of the
Republic of China No.27), issued in 2002; Law of the People’s prevalence study of HCAIs throughout China (2012).19 However,
Republic of China on the Prevention and Treatment of USA and European studies have generally reported that

Please cite this article in press as: Liu JY, et al., Point-prevalence survey of healthcare-associated infections in Beijing, China: a survey and
analysis in 2014, Journal of Hospital Infection (2016), http://dx.doi.org/10.1016/j.jhin.2016.03.019
6 J.Y. Liu et al. / Journal of Hospital Infection xxx (2016) 1e9

Table III
Intrinsic and extrinsic risk factors for healthcare-associated infections (HCAIs): univariate and multi-variate analysis (logistic regression)
Risk factors Patients with HCAIs, N (%) Univariate OR (95% CI) Multi-variate ORa (95% CI)
Sex
Male (N¼32,386) 791 (2.4) 1 1
Female (N¼29,522) 503 (1.7) 0.7 (0.6e0.8) 0.8 (0.7e0.9)
P¼0.00 P¼0.00
Age, N (%)
18 years (N¼4009) 66 (1.6) 1 1
19e24 years (N¼1775) 22 (1.2) 0.8 (0.5e1.2) 1.1 (0.7e1.9)
P¼0.25 P¼0.61
25e44 years (N¼2082) 136 (1.1) 0.7 (0.5e0.9) 1.0 (0.7e1.4)
P¼0.11 P¼0.87
45e64 years (N¼21,734) 370 (1.7) 1.0 (0.8e1.4) 1.2 (0.9e1.6)
P¼0.79 P¼0.20
65e84 years (N¼18,905) 553 (2.9) 1.8 (1.4e2.3) 1.9 (1.4e2.6)
P¼0.00 P¼0.00
85 years (N¼2826) 132 (4.7) 2.9 (2.2e3.9) 2.2 (1.6e3.2)
P¼0.00 P¼0.00
28 days (N¼577) 15 (2.6) 1.6 (0.9e2.8) 3.3 (1.7e6.3)
P¼0.11 P¼0.01
Department classification, N (%)
Medicine (N¼28,312) 641 (2.3) 1 1
Surgery (N¼18,459) 375 (2.0) 0.9 (0.8e1.0) 0.5 (0.5e0.6)
P¼0.09 P¼0.00
Gynaecology and obstetrics (N¼5220) 18 (0.3) 0.1 (0.1e0.2) 0.2 (0.1e0.3)
P¼0.00 P¼0.00
Paediatrics (N¼1302) 31 (2.4) 1.1 (0.7e1.5) 0.8 (0.5e1.4)
P¼0.78 P¼0.46
Ophthalmology and otorhinolaryngology (N¼2300) 6 (0.3) 0.1 (0.1e0.3) 0.1 (0.1e0.3)
P¼0.00 P¼0.00
ICUs (N¼965) 140 (14.5) 7.3 (6.0e8.9) 1.5 (1.2e1.9)
P¼0.00 P¼0.00
Otherb (N¼5350) 83 (1.6) 0.7 (0.5e0.9) 0.7 (0.6e0.9)
P¼0.00 P¼0.02
Hospital classification, N (%)
Second level (N¼21,069) 319 (1.5) 1 1
Tertiary (N¼40,839) 975 (2.4) 1.6 (1.4e1.8) 1.4 (1.2e1.6)
P¼0.00 P¼0.00
Traditional Chinese medicine hospital, N (%)
Yes (N¼8127) 95 (1.1) 1 1
No (N¼53,781) 1199 (2.2) 2.0 (1.6e2.5) 1.7 (1.4e2.1)
P¼0.00 P¼0.00
Central venous catheter in place on survey date, N (%)
No (N¼55,759) 819 (1.5) 1 1
Yes (N¼6149) 475 (7.7) 5.6 (5.0e6.3) 2.2 (1.9e2.5)
P¼0.00 P¼0.00
Urinary tract catheterization on survey date, N (%)
No (N¼54,224) 714 (1.3) 1 1
Yes (N¼7684) 580 (7.5) 6.1 (5.4e6.8) 3.6 (3.1e4.2)
P¼0.00 P¼0.00
Patient receiving invasive ventilation on survey date, N (%)
No (N¼59,534) 1035 (1.7) 1 1
Yes (N¼2374) 259 (10.9) 6.9 (6.0e8.0) 1.3 (1.1e1.6)
P¼0.00 P¼0.00
Surgery prior to survey date, N (%)
No (N¼47,253) 885 (1.9) 1
Yes (N¼14,655) 409 (2.8) 1.5 (1.3e1.7) 1.2 (1.1e1.5)
P¼0.00 P¼0.01

Please cite this article in press as: Liu JY, et al., Point-prevalence survey of healthcare-associated infections in Beijing, China: a survey and
analysis in 2014, Journal of Hospital Infection (2016), http://dx.doi.org/10.1016/j.jhin.2016.03.019
J.Y. Liu et al. / Journal of Hospital Infection xxx (2016) 1e9 7

Table III (continued )


Risk factors Patients with HCAIs, N (%) Univariate OR (95% CI) Multi-variate ORa (95% CI)
Diarrhoeac, N (%)
No (N¼61,417) 1231 (2.0) 1 1
Yes (N¼491) 63 (12.8) 7.2 (5.5e9.4) 4.5 (3.4e6.1)
P¼0.00 P¼0.00
OR, odds ratio; CI, confidence interval; ICUs, intensive care units.
a
Adjusted for all variables in the model.
b
Refers to all departments not included in the listed categories.
c
The definition of diarrhoea in the study was three or more loose stools in one day.

pneumonia and surgical site infections account for similar that detection rates in sputum cultures in community-acquired
proportions of all HCAIs.2,3 One reason for the difference in the pneumonia are very low.23e25 The detection rate of antibiotic-
present study may be that postdischarge surveillance for sur- resistant Gram-negative bacteria such as P. aeruginosa and
gical site infections was not undertaken. The 2013 Europe A. baumanii in respiratory samples is increased following
Nosocomial Infection and Infectious Disease and Epidemic antibiotic exposure.26 In addition, sputum is the most
Disease Report found that 50% of surgical site infections commonly submitted sample in Chinese hospitals, whereas
occurred after discharge.21 Secondly, differences in diagnostic samples from the lower airway (e.g. bronchoalveolar lavage)
criteria for respiratory tract infections in this study may also are more commonly collected in other countries.27
account for lower respiratory infection being more common in P. aeruginosa and A. baumannii are common pathogens in the
this study. In China, a wider range of symptoms are categorized hospital environment.28,29 Indeed, A. baumannii isolated from
as ‘lower respiratory infection’,20 including pneumonia, tra- patients and the ICU environment have been shown to be
chitis and bronchitis, while lower respiratory infection in the indistinguishable.30
USA is categorized separately from pneumonia.10 Thirdly, in Patients with diarrhoea accounted for 0.8% of all re-
China, microbiological diagnosis is often based on sputum spondents in this survey. Clostridium difficile is rarely detec-
culture, with little attempt to distinguish between colonization ted in China, which is inconsistent with research worldwide.
and infection. The latest US prevalence of HCAI survey reveals that gastro-
The most common pathogens in this survey were intestinal tract infections are important nosocomial infections,
P. aeruginosa and A. baumanii, as in a previous Chinese HCAI and C. difficile is the most common cause, accounting for 12.1%
prevalence survey19; this differs from the pathogen distribution of all diarrhoeal pathogens.2,3 In Beijing, only a few microbi-
of HCAIs in American and European countries.2,3 One possible ology laboratories can perform C. difficile testing, and it is not
explanation is that there is lower awareness among Chinese included in routine testing. Moreover, many clinicians are not
clinicians of the need to submit microbial samples for exami- aware of C. difficile. As such, the true picture of C. difficile
nation, especially before antimicrobials are administered. infection in China is not known.
Guoli et al. conducted a study on specimen culture in 841 cases
of ICU patients in 2014, and showed that only 33.5% of 269 Risk factors for healthcare-associated infections
patients on broad-spectrum antibiotics had samples collected
for microbiological examination.22 There are few specific data Advanced age (>65 years), ICU stay, invasive procedures
on HCAIs, but reports on community-acquired pneumonia show (central venous catheter insertion, urethral catheterization

12 Invasive ventilation
10.9%
10
Central venous catheter
Patients with HCAIs (%)

Urinary tract catheter


8 7.7% 7.5%

2 1.5% 1.7%
1.3%

0
No Yes No Yes No Yes

Figure 2. Prevalence of healthcare-associated infections (HCAIs) in relation to invasive devices on survey date.

Please cite this article in press as: Liu JY, et al., Point-prevalence survey of healthcare-associated infections in Beijing, China: a survey and
analysis in 2014, Journal of Hospital Infection (2016), http://dx.doi.org/10.1016/j.jhin.2016.03.019
8 J.Y. Liu et al. / Journal of Hospital Infection xxx (2016) 1e9
and mechanical ventilation) and use of antibiotics were among 5. Lyytikäinen O, Kanerva M, Agthe N, Möttönen T, Ruutu P, Finnish
other main risk factors, which is consistent with a US point- Prevalence Survey Study Group. Healthcare-associated infections
prevalence survey conducted in 2011.2 However, while the US in Finnish acute care hospitals: a national prevalence survey,
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6. Lee MK, Chiu CS, Chow VC, Lam RK, Lai RW. Prevalence of hospital
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9. Faria S, Sodano L, Gjata A, et al. The first prevalence survey of
nosocomial infections in the University Hospital Centre ‘Mother
Strengths and limitations Teresa’ of Tirana, Albania. J Hosp Infect 2007;65:244e250.
10. Garner JS, Jarvis WR, Emori TG, Horan TC, Hughes JM. CDC defi-
This survey was a census which significantly minimized nitions for nosocomial infections, 1988. Am J Infect Control
sampling error, meaning that the results are representative. In 1988;16:128e140.
addition, this is the first report of the prevalence of HCAIs in 11. Wu A, Yi X, Ren N, et al. The survey of hospital infection man-
China that includes the incidence of diarrhoea caused by agement. Chin J Nosocomiol 2001;11:342e343.
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The survey focused on a relatively small number of risk
13. World Health Organization. The guidelines of nosocomial infec-
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tion. Prevention and control. 2nd ed. Geneva: World Health Or-
were available. It is suggested that future Chinese surveys ganization; 2002.
should collect more data on antibiotic usage. 14. Yue W, Lu-tao Z, Li-ke S, Yan L. Nosocomial infection: a transverse
section survey on 1483 inpatients. Chin J Nosocomiol
Conclusion 2010;20:2566e2569.
15. Xue J, Li-hui M, Bao-kun D. Changing trends in nosocomial infec-
tion: cross section investigation. Chin J Nosocomiol
In countries like China with limited personnel and resources,
2009;19:1496e1498.
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performed in lieu of comprehensive monitoring to elucidate among inpatients: surveillance and analysis in grade-A hospital.
risk factors and disease burdens of HCAIs. However, limited use Chin J Nosocomiol 2009;19:1496e1498.
of microbiology laboratories in the diagnosis of HCAIs is an 17. Nan R, Wen XM, Wu AH. Study on the changing trends in national
important constraint to obtaining data that can be compared nosocomial infection transection investigation results. Chin J
with other countries. Infect Control 2007;6:16e18.
18. Wen XM, Ren N, Wu AH. Distribution of pathogens and antimi-
crobial resistance: an analysis of China healthcare-associated
Acknowledgements infection cross-sectional survey in 2010. Chin J Infect Control
2012;11:1e6.
The authors wish to thank all of the tertiary and secondary 19. Wu AH, Li CH, Wen XM, Ren N. China national point-prevalence
hospitals that participated in this survey. survey on healthcare-associated infection and antimicrobial use
in 2012. Chin J Infect Control 2014;13:8e15.
Conflict of interest statement 20. Ministry of Health. Health care-associated infection monitoring
None declared. specification (WS/ T312-2009). Available at: http://www.moh.
gov.cn/zwgkzt/s9496/200904/40117.shtml [last accessed June
2014].
Funding sources
21. European Centre for Disease Prevention and Control. Annual
None. epidemiological report reporting on 2011 surveillance data and
2012 epidemic intelligence data. Stockholm: ECDC; 2013. Available
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analysis in 2014, Journal of Hospital Infection (2016), http://dx.doi.org/10.1016/j.jhin.2016.03.019
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Please cite this article in press as: Liu JY, et al., Point-prevalence survey of healthcare-associated infections in Beijing, China: a survey and
analysis in 2014, Journal of Hospital Infection (2016), http://dx.doi.org/10.1016/j.jhin.2016.03.019

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