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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.
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
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
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
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 (%)
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,
study showed that infections associated with invasive devices 2005. J Hosp Infect 2008;69:288e294.
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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-
factors for HCAIs. In addition, few data on antibiotic usage
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
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15. Xue J, Li-hui M, Bao-kun D. Changing trends in nosocomial infec-
tion: cross section investigation. Chin J Nosocomiol
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regular investigation of the point prevalence of HCAIs can be 16. Huang DX, Zhou H, Sun J, Sheng HB, Huang QM. Hospital infection
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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
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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