Implementation of infection prevention and control in acute care hospitals in Mainland China – a systematic review

Background Healthcare-associated infections (HAIs) and antimicrobial resistance (AMR) affect patients in acute-care hospitals worldwide. No systematic review has been published on adoption and implementation of the infection prevention and control (IPC) key components. The objective of this systematic review was to assess adoption and implementation of the three areas issued by the “National Health Commission of the People’s Republic of China” in acute-care hospitals in Mainland China, and to compare the findings with the key and core components on effective IPC, issued by the European Centre for Disease Prevention and Control (ECDC) and the World Health Organization (WHO). Methods We searched PubMed and the Chinese National Knowledge Infrastructure for reports on the areas “structure, organisation and management of IPC”, “education and training in IPC”, and “surveillance of outcome and process indicators in IPC” in acute-care facilities in Mainland China, published between January 2012 and October 2017. Results were stratified into primary care hospitals and secondary/tertiary care hospitals. Results A total of 6580 publications were retrieved, of which 56 were eligible for final analysis. Most of them were survey reports (n = 27), followed by observational studies (n = 17), and interventional studies (n = 12), either on hand hygiene promotion and best practice interventions (n = 7), or by applying education and training programmes (n = 5). More elements on IPC were reported by secondary/tertiary care hospitals than by primary care hospitals. Gaps were identified in the lack of detailing on organisation and management of IPC, education and training activities, and targets of surveillance such as central line-associated bloodstream infections, ventilator associated pneumonia, catheter-associated urinary tract infections, and Clostridium difficile infections. Information was available on adoption and implementation of 7 out of the 10 ECDC key components, and 7 out of the 8 WHO core components. Conclusion To variable degrees, there is evidence on implementation of all NHCPRC areas and of most of the ECDC key components and the WHO core components in acute care hospitals in Mainland China. The results are encouraging, but gaps in effective IPC were identified that may be used to guide future national policy-making in Mainland China. Electronic supplementary material The online version of this article (10.1186/s13756-019-0481-y) contains supplementary material, which is available to authorized users.


Introduction
The prevention of healthcare-associated infections (HAIs) is a first priority for patient safety in acute-care hospitals worldwide [1][2][3][4][5]. Adherence to the key and core components of infection prevention and control (IPC) issued by the European Centre for Disease Prevention and Control (ECDC)-funded "Systematic Review and Evidence-based Guidance on Organisation of Hospital Infection Control" (SIGHT) group and the World Health Organization (WHO), respectively, contributes to prevent HAI and the spread of antimicrobial resistance [6,7]. The United Nations Sustainable Development Goals highlighted the importance of IPC as a contributor to safe and effective high-quality health service delivery [7]. Furthermore, WHO intends to support countries in the development of their own national IPC programmes [7].
The Asia-Pacific region has been described as a geographic source for emerging infectious diseases, including multidrug-resistant organisms and pathogens with pandemic potential [8]. The People's Republic of China is the largest economic body in the region and faces similar global health challenges towards HAI and emerging antimicrobial resistance, as other countries in the region [2,3,8]. Little is known on how hospitals prevent HAIs and control the spread of multidrug-resistant microorganisms in Mainland China; in particular, there is lack of information on the availability and the implementation of the ECDC key components for effective IPC.
In 2006, the National Health Commission of the People's Republic of China (NHCPRC) published the "Nosocomial Infection Management Methods" (Decree No. 48), which are guidelines defining elements on the organisation of IPC at hospital level [9]. In 2018, hospital accreditation was linked to the NHCPRC elements by the "Accreditation regulation of control and prevention of healthcareassociated infection in hospitals" (WS/T 592-2018) [10]. The NHCPRC decree embraces three broad areas of IPC: 1) structure, organization and management of IPC; 2) education and training in IPC; and 3) outcome and process indicator surveillance in IPC.
The aim of this systematic review was to assess adoption and implementation of elements of the three NHCPRC areas by acute care hospitals in Mainland China, and to compare the findings with the ECDC key components and the WHO core components in IPC.

Search strategy
This systematic review followed the "Preferred Reporting Items for Systematic Review and Meta Analysis" (PRISMA) guidelines [11]. We searched PubMed, the "Chinese National Knowledge Infrastructure" database, and the Cochrane library for any relevant document. In addition, we looked for guidelines on the official websites of the NHCPRC and the regional Ministries of Health in Mainland China.
Primary outcomes were: reporting on adopting, implementing (having) or analysing elements of the three NHCPRC areas. Secondary outcomes were: reporting on change of indicators (e.g. HAI or hand hygiene) by applying IPC practices. The search terms addressed the three IPC areas specified by the NHCPRC for acute care hospitals: 1) structure, organization and management of IPC; 2) education and training of IPC; and 3) surveillance of process and outcome indicators relevant to IPC. Search terms and key words for PubMed and the "Chinese National Knowledge Infrastructure" are summarized in Additional file 1: Tables S1A and S1B.

Inclusion/exclusion criteria
Any article was eligible for inclusion when all of the following criteria were met: 1) use of a quantitative, qualitative or combined (mixed-methods) method; 2) reporting on one of the primary and/or secondary outcomes; 3) publication between January 2012 and October 2017; and 4) publication either in English or Chinese. Articles were excluded if they met one of the following criteria: 1) conference papers, editorials, or letters; 2) duplicated results; 3) risk factor analysis without information on the use of any IPC practice; 4) non-acute healthcare setting; or 5) outbreak investigations.

Data extraction
Title, abstract and full text review were performed by two individual researchers (JW, FL). Disagreements were resolved by consensus, and, when necessary, discussed with a third researcher (WZ). Data extraction was stratified by two hospital categories (primary care and secondary/tertiary care hospitals). Definitions on hospital categories are provided in Additional file 1: Table S2. Articles were further categorised as survey reports, observational studies or interventional studies. The following data were extracted from survey reports: title, authors, publication year, province, total number of hospitals, and the number of hospitals applying specific elements of the three NHCPRC areas. The following data were extracted from observational studies: title, author, publication year, province, study aim, setting, surveillance protocol, sample size, study duration, methodology, and outcome. The following data were extracted from interventional studies: title, authors, publication year, province, study aim, population, intervention, comparison, study design and outcome. Data extraction for interventional studies followed the "PICO" (population interventioncomparisonoutcome) concept [11]. Data were verified by cross-checking (JW, FL and JBXT). Survey reports and observational studies were quality assessed by using the "Strengthening the Reporting of Observational Studies in Epidemiology" (STROBE) checklist (Additional file 1: Tables S3A and S3B) [12]. Interventional studies were quality assessed by using the "Integrated quality Criteria for the Review Of Multiple Study designs" (ICROMS) checklist (Additional file 1: Tables S3C and S3D) [13]. Findings were stratified by the three NHCPRC areas, and compared with the ECDC key components [6], and the WHO core components [7].

Statistical analysis
Frequencies of elements mentioned in the survey reports were calculated on hospital level (with the corresponding 95% confidence interval), and stratified by hospital category. The difference of each identified element between hospital categories was tested by Pearson's Chi-Square test. Statistical analysis was performed using STATA version 14.0 (Stata Corporation, College Station, Texas, USA). Results of observational and interventional studies were summarized descriptively.

Results
From a total of 6580 titles and abstracts, 56 articles were eligible for data extraction and analysis ( Fig. 1): 27 survey reports on structure, organisation and management of IPC (Table 1); 17 observational studies (8 single and 9 multicentre studies) measuring outcome and process indicators (Table 2); 5 interventional studies (5 single centre studies) applying education and training (Table 3); and 7 interventional studies (6 single-and 1 multicentre centre studies) testing the effectiveness of IPC strategies, mostly applying a multimodal strategy (n = 5) (Table 4).
NHCPRC area "structure, organisation and management of IPC" The search terms addressing the NHCPRC area on "structure, organisation and management of IPC" identified 27 survey reports summarizing the results of 1634 hospitals: 8 (29.6%) reports on 440 primary care hospitals, 17 (63.0%) reports on 1127 secondary/tertiary care hospitals, and 2 (7.4%) reports on 26 primary-and 41 secondary/tertiary care hospitals combined ( Table 1). The results of this area were divided into six elements (Table 1). Quality was moderate and low in eight and two of the 10 survey reports from primary care hospitals, respectively (Additional file 1: Table S4A). Quality was high, moderate and low in 1, 14, and 4 of the 19 survey reports from secondary/tertiary care hospitals, respectively (Additional file 1: Table S4B). Table 1, Additional file 1: Table S4A and Table S4B summarize the details on the reported elements, stratified by hospital types.

Structure, organisation and management, guideline provision
Most primary care hospitals had an IPC committee (71.1%), a formal IPC programme (61.9%), and provided IPC guidelines (57.7%). Most secondary/tertiary care hospitals had an IPC committee (98.1%), performed feedback on IPC indicators (93.6%), and provided IPC guidelines (85.8%). No information on feedback, allocated

Education and training in IPC
Significantly more secondary/tertiary care hospitals offered regular, postgraduate IPC training compared to primary care hospitals (Table 1). However, the survey reports did not describe details on target population, training content, or frequency of training activities.

Indicator and outcome surveillance in IPC
The results of this area were stratified by "surveillance" and "auditing" and divided into 10 elements (  Table 1). The most frequently audited NHCPRC element in secondary/tertiary care hospitals was environmental culturing (92.5%), followed by waste management (57.6%), and sterilization and medical device decontamination (55.3%) ( Table 1).

NHCPRC area "Education and training in IPC"
In addition to the above-mentioned survey reports, the search terms addressing the NHCPRC area on "Education and training in IPC" identified 5 single centre interventional studies: two non-controlled before-after studies, two controlled before-after studies, and one non-controlled interrupted time-series study. The quality of all five interventional studies was high (Additional file 1: Table S3C). Table 3 summarizes the details of the studies. Education and training in IPC was delivered via lectures, problem-based learning, (focus) group discussion, video scenarios, and simulation training. Two studies targeted new staff, whereas one focused on nursing students. Training activities were associated with improvement of IPC knowledge, increase of hand hygiene compliance, and reduction of HAIs.

NHCPRC area "outcome and process indicator surveillance"
The search terms addressing the NHCPRC area on "outcome and process indicator surveillance" identified 17 observational studies (Table 2) and 7 interventional studies (Table 4). Of the 17 observational studies, 7 and 10 were of high and moderate quality, respectively ( Table 2). All seven interventional studies were of high quality (Additional file 1: Table S3C). Five of the interventional studies applied a multimodal strategy, and measured either outcome indicators (n = 3) or process indicators (n = 2) ( Table 4).
Observational studies on outcome-and process indicator surveillance Table 2 summarizes the findings of the 17 observational studies: five measured device-associated HAIs, three allcause HAIs, three Clostridium difficile infections (CDI), two ventilator-associated pneumonias (VAPs), two central line-associated bloodstream infections (CLABSIs), one SSIs, and one hospital acquired pneumonia. Twelve studies applied the standard Chinese surveillance protocol, four applied a network protocol other than the official document, and one applied a research protocol.
Interventional studies on outcome and process indicator surveillance Table 4 summarizes the details of the 7 interventional studies: six non-controlled before-after studies and one randomized controlled trial. Due to variation in intervention and outcome measurement, no meta-analysis was performed. Five studies used a multimodal strategy addressing hand hygiene improvement, CLABSI prevention, and VAP prevention. One study successfully tested pre-operative chlorhexidine mouthwash on VAP reduction, whereas another study reported MRSA reduction in the environment by improved cleaning practices.

Mapping to key/core components in IPC
This systematic review found information on all three NHCPRC areas, which are directly linked to the three ECDC key components on structure and organisation of IPC programmes, education and training in IPC, and performing surveillance (in a network) with timely feedback [6,7]. However, many of the survey reports also reported on elements linked to other ECDC key components such as provision and appropriate promotion of (locally adapted) guidelines, and performing audits. Furthermore, some of the interventional studies improved the provision of alcohol-based handrub at the point of care, or used new catheter insertion kits and trolleys, which are elements linked to the "materials and ergonomics" ECDC key component. Most of the interventional studies applied a multimodal strategy. Together, this systematic review identified information on 7 of the 10 ECDC key components, and 7 of the 8 WHO core components, respectively (Table 5).

Discussion
To our best knowledge, this is the first systematic review summarizing adoption and implementation of IPC in acute care hospitals in Mainland China. This review fills a research gap on the adoption and implementation of IPC in Mainland China (Table 6), highlighting, which of the key/core components recommended by ECDC/ WHO have been adopted and implemented, and which need further attention. It also offers an overview on the distribution of strategies and elements available in primary care hospitals compared to secondary/tertiary care hospitals. The observational and interventional studies complete the findings of the survey reports, offering a more granular picture on IPC activities in acute care hospitals in Mainland China. To various degrees, there is evidence that seven of the ECDC key components have been adopted and implemented in acute care hospitals in Mainland China.

Structure, organisation and management of infection prevention and control
Effective IPC in an acute care hospital needs an IPC programme with sufficient staffing and an allocated budget, support from the hospital management, and well defined duties and targets. The official structure requirements for IPC in Chinese hospitals (Additional file 1: Figure S1) are often not met. Only two-thirds of primary care hospitals have an IPC programme and an IPC committee. No information was found for any of the other elements of this NHCPRC area. The majority of secondary/tertiary care hospitals have an IPC programme, but only a third has an allocated budget. It is difficult to estimate the challenges on the proper functioning of IPC, but it has been shown that competing resources may have a negative impact on effective IPC [14]. Staffing, as identified in several reports is at minimal level [6,7,15], comparable to other surveys [16,17]. However, high staff turnover, particularly among IPC doctors [18][19][20], is even of more concern than understaffing. This is partially explained by low salaries and limited career tracks [19]. Only 4.4% of IPC doctors were satisfied with their position in one survey [19]. They were assigned to that position by hospital management, often against their will [19]. As a result, most IPC departments are managed by junior IPC doctors and IPC nurses. Due to the hierarchical gap between doctors and nurses, as well as between junior and senior doctors, IPC professionals face structural challenges, and struggle in influencing behaviour change [21]. Almost all secondary/tertiary care hospitals have an IPC committee in place. However, the importance of IPC is not always recognized by hospital management, and IPC committee members do not always participate actively in the committees [19,20]. Most secondary/tertiary care hospitals indicated to have a feedback mechanism in place. This is positive given the various IPC activities in surveillance and auditing. However, no details are available about format, target population, and frequency of feedbacks. Too often, information is conveyed to the hospital management only, and data reach healthcare workers too late, if at all, to be meaningful and impactful [22,23].
A low proportion of primary care hospitals indicated to have IPC guidelines. This is surprising given that various national IPC documents are available (n = 30), and that implementation is mandatory for many of them (n = 17) (Additional file 1: Table S5).

Education and training in infection prevention and control
Half of primary-and three-quarters of secondary/tertiary care hospitals indicated to have postgraduate IPC education and training in place. Education and training should be team-and task-oriented, frontline workers should take part in the preparation and execution process (ideally peerto-peer teaching), the content should follow local guidelines, and implementation should be multimodal [6]. Unfortunately, survey reports lack details on the target population, contents, delivery methods, and frequency. Thus, it is difficult to assess the available resources for education and training and whether they are adequate. The use of multimodal strategies was identified in five interventional studies that successfully reduced HAIs by improving IPC knowledge and increasing hand hygiene compliance [24][25][26][27][28]. Professionals working in IPC need knowledge and skills on management and implementation research [29]. With the "European Certificate for Infection Control", the European Society for Clinical Microbiology and Infectious Diseases has created a platform to offer comprehensive IPC training beyond hygiene to doctors [29,30]. Implementation research and management are not part of IPC training in Mainland China. The basic and intermediate skill levels focus on legal aspects, mandatory surveillance, definitions, diagnosis, HAI classification, HAI prevention, and hand hygiene (Additional file 1: Tables S6A and S6B) [31]. The contents of the advanced level were not sufficiently specified in the documents to allow conclusions on delivering skills regarding on the topic of project management and implementation research [31].
Not even two thirds of the hospitals perform surveillance on antimicrobial resistance and antimicrobial use, although this is mandatory since 2011 (Additional file 1: Table S5) [47,48]. This is of concern given the challenge of emerging resistance in the Asia Pacific region [1,3]. In addition, no information was identified on antimicrobial stewardship, which, at least according to some reports, is not yet established in primary care hospitals [3,49]. In 2016, the CHINET surveillance programme reported 7.0% of Enterobacteriaceae being resistant to carbapenems, 38.4% of Staphylococcus aureus being resistant to methicillin, and 45.2% of Enterobacteriaceae expressing extended-spectrum beta-lactamases [50]. These numbers are alarming, and IPC should be empowered both in recognition and resources to prevent cross-transmission of multidrug-resistant microorganisms in acute care hospitals.

Monitoring/auditing
Standard and isolation precaution measures, waste management, sterilization and medical device decontamination, and environmental cultures are audited. Interestingly, there is no difference in the frequencies between the hospital types except for environmental cultures. Almost all secondary/tertiary care hospitals perform routine environmental cultures (in intensive care, operating theatres, central sterile services departments, endoscopy suites, haemodialysis centres, and dentistry departments), which is of questionable value outside of outbreaks [51]. These resources could be better directed towards targeted screening of patients at risk of carrying multidrug-resistant microorganisms [52].

Bundles and multimodal interventions
Consistent with the ECDC key components [6], five of the seven interventional studies used a multimodal 2. Education and training in infection prevention and control -Limited resources for IPC education and training; -Little experience with team-and task-oriented learning, or peer-to-peer teaching education; -Little experience with implementation strategies; 3. Surveillance of outcome and process indicators -Few prospective incidence surveillance programmes -Little antimicrobial stewardship programmes in primary-care hospitals; -Little effort towards targeted MDRO screening of patients on admission IPC infection prevention and control, NHCPRC National Health Commission of the People's Republic, MDRO multidrug-resistant microorganism strategy to improve hand hygiene, and reduce CLABSI and VAP [53][54][55][56][57]. Two studies on hand hygiene combined leadership engagement, provision of alcohol-based handrub at the point of care, feedback, and reminders at the workplace [53,54]. One study on CLABSI prevention [55] and two studies on VAP prevention [56,57] applied "bundles", and partially followed the recommendations from SHEA/IDSA [58,59]. These studies were performed in Eastern China, where the socioeconomic status is high, and therefore more resources might be available for implementing IPC measures and conducting studies (Additional file 1: Table S7) [3].

Limitations
This review has limitations. First, the data on the first NHCPRC area about IPC structure, organisation and management came from survey reports using questionnaires. This limits detailing, and the proportion of hospitals correctly implementing IPC elements may be overestimated. Second, the survey reports and studies in the final analysis originated mainly from regions with higher socioeconomic status, and thus, may not be representative for Mainland China as a whole. Third, publication bias may have occurred by the fact that we checked only scientific data sources and confined search on one English and one Chinese database. Fourth, there is no mandatory reporting system for HAI incidence in Mainland China. Studies on incidence surveillance are mainly retrospective. Thus, data on outcome indicators are limited. Fifth, methodological heterogeneity of the observational and interventional studies limited comparability; and thus, conducting a formal meta-analysis was not possible. However, the aim of this systematic review on describing adoption and implementation of elements of the three NHCPRC areas was still met. Sixth, the search terms of this systematic review were based on the three NHCPRC areas. We considered the concept of the ECDC key components too new to serve as a starting point for a search based on scientific literature. The search strategy based on recommendations by the Chinese healthcare authorities was a more pragmatic approach. However, the results still covered 7 of the 10 ECDC key components, and 7 of the 8 WHO core components. The only lacking key components were about frontline staffing, integrating champions in the implementation of IPC strategies, and fostering a positive organisational culture.

Conclusion
To variable degrees, there is evidence on implementation of all NHCPRC areas and of most of the ECDC key components and the WHO core components in acute care hospitals in Mainland China. The results are encouraging, but gaps in effective IPC were identified that may be used to guide future national policy-making in Mainland China.

Additional file
Additional file 1: Table S1A and S1B. Search terms for PubMed and the China National Knowledge Infrastructure (Chinese database). Table S2. Definition of hospital types.  Table S7. Geographical distribution of survey reports, observational studies and interventional studies in the final analysis. Figure S1.