Healthcare-associated infections in intensive care units in Taiwan, South Korea, and Japan: recent trends based on national surveillance reports

The European Healthcare-associated Infections Surveillance Network (HAI-net) is one of the most coordinated and comprehensive surveillance systems that monitors healthcare-associated infections (HAI). By centralizing data on antimicrobial use, HAI incidence, and HAI point prevalence, HAI-net builds a regional landscape that allows inter-country comparison and provides feedback for implementation of regional infection prevention and control (IPC) guidelines [1].

With its high burden of HAI, Asia stands to benefit by learning from such a surveillance network. A recent meta-analysis reported a pooled HAI incidence density of 20 cases per 1000 intensive care unit-days in Southeast Asia [2]; studies in India and China found pooled ventilator-associated pneumonia of 9.4 and 20.8 cases per 1000 ventilator-days, respectively [3, 4]. Establishing surveillance in Asian countries, either as national or regional collaborations, might help relevant stakeholders to identify systemic gaps and establish improvements in IPC.

The current understanding of HAI surveillance in Asia remains limited despite the relatively large numbers of IPC conducted in Asia [2, 5]. Likewise, national scale data documenting the regional HAI epidemiology in Asia is scarce [2]. To better understand the current state of HAI surveillance and IPC programs in Asia, we searched for data on existing national HAI surveillance programs. Three Asian countries: Taiwan [6, 7], South Korea [8‐10], and Japan [11] were found to conduct nationwide HAI surveillance systems. The present study is based on data derived from open access reports from the surveillance systems of these countries. They include temporal trends of HAI in intensive care units (ICUs), the major causative pathogens and antimicrobial resistance (AMR). Nationally implemented IPC policies were also reviewed to gain insights on important interventions instituted in these three countries.

In the current study, we described the surveillance and IPC programs of Taiwan, South Korea and Japan. A variation in surveillance protocol, such as HAI case definition and surveillance items was found among the three countries although these protocols were similar to those employed by the HAI-net and NHSN. There were also common IPC strategies shared by the three countries, but each with special emphasis on different aspects of IPC. We also compared the rates of HAI and the most common causative pathogens as reported by the three surveillance systems. There was a 53% decline in overall HAI in the surveyed ICUs of all three countries over the 8-year period. The overall incidence densities of HAI in Taiwan, Korea, and Japan in 2015 were 5.0, 2.8, and 2.7 per 1000 patient-days, respectively. These rates are comparable to HAI-net (2.6 per 1000 patient-days), and substantially lower than those of developing countries, as shown in Table 3 [2, 12‐15].

We believe that essential elements that contributed to the sustained decrease in the incidence of HAI in Taiwan, Korea and Japan were the national surveillance programs combined with improvement in IPC practices [16]. In Korea, there was a significant decline in device-associated HAI in association with the implementation of the KONIS program [17]. National IPC programs such as hand hygiene, care bundles, antimicrobial stewardships, and environmental hygiene have been shown to effectively reduce HAI and infections caused by AMR pathogens [7, 18‐20]. In Taiwan, hand hygiene program over a 4-year period were found to reduce HAI in ICU by 17.2% and BSI by 12.7% [20], and care bundles to further reduce CAUTI and CLABSI by 22.7 and 12.2%, respectively [21, 22]. In Korea, a multicentre study found that VAP rate decreased from 4.08 to 1.16 cases per 1000 ventilator-days following 3 months of bundle intervention [23]. Evidence-based IPC practices have been shown to be cost-saving and effective in preventing HAI [20, 24]. Adoption of these practices to reduce HAI burden might be helpful for many Asian countries, which are facing problems such as rising healthcare costs and inefficient healthcare insurance systems [25].

Appointment of infection control professionals or infection control committees is a common strategy across the three countries (Fig. 1, Additional file 2: Table S2). In Japan, one serious fundamental obstacle before 2010 was the lack of personnel dedicated to IPC. In 2010, Japan revised medical reimbursement system and provided 10 USD per patient per admission if a hospital payed the annual cost for the designated work hours for infection control personnel which included certificated nurse, doctor, pharmacist and medical technician/microbiologist. IPC incentives through reimbursement policies were revised in 2012 and 2018, as described in Additional file 2: Table S2. Such a scheme encourages hospitals dedicated certificated personnel to participate in IPC (Table 1). Other than manpower, personnel training and resource infrastructure are essential for surveillance and prevention of HAI [26, 27]. During the study period, financial incentives to support IPC programs were employed by Korea and Japan. Japan switched its reimbursement system to a penalty system in 2000, and then changed it back to the current reward system in 2010. This suggests that a supportive environment that encourages IPC practices might be better than one that punishes for wrongdoing, and should be fostered by national authorities for effective prevention of HAI [27]. Correspondingly, such a difference in reimbursement may have well influenced the outcomes of HAI in Taiwan, Korea and Japan.

Changes in case definition might have contributed to the observed HAI trends. For example, the newer definition for UTI established in 2009 would probably have excluded cases that might have been classified as HAI under the older definition [28]. Nevertheless, based on the consistent decline of HAI incidence across all infection categories, it is unlikely that modifications in case definition can explain the remarkable decrease in HAI trends.

Substantial variation exists for causative pathogens of HAI across the three countries. This variability could be due to a number of factors, including baseline characteristics of participating hospitals and ICUs, variation in diagnostic standards and case definitions, geography and climate, and IPC practices. For example, Japan’s BSI was dominated by staphylococci (39.9%) possibly because its reports were limited to device-associated modules in BSI. An interesting variation that is likely not attributable to systemic differences was noted for A. baumannii, which was isolated commonly from Taiwan and Korea but rarely from Japan. Results from HAI-net seem to support this notion, with higher proportions of HAI caused by Acinetobacter spp. in some countries [13].

Our study showed a general decrease in isolates of important AMR species: MRSA, CRPA and CRAB even though the number of participating ICUs has expanded from 2008 to 2015. This downward trend is likely due to hand hygiene to prevent cross-transmission of AMR pathogens, care bundles to prevent device- or procedure-associated infections, and antimicrobial stewardship programs to mitigate the selection pressure implemented in these countries [7, 18‐20, 29]. A recent meta-analysis reported that antimicrobial stewardship programs in Asia reduced overall antimicrobial consumption by 9.74% and incidence density of important AMR pathogens such as MRSA by 0.9 to 1.4 isolates per 1000 patient-days [19]. Expenditure associated with antimicrobial prescription and hospitalization were also found to decrease by a range of 9.7 to 58.1%. These findings highlight the efficacy and importance of antimicrobial stewardship programs in combating the rise of AMR pathogens.

While surveillance of HAI may provide important feedback for IPC efforts, the high costs in establishing and maintaining the system may preclude many countries from undertaking such an ordeal. Introducing information technology in surveillance systems may help reduce labor intensive and increase the efficiency of surveillance [30‐33]. In Asia, National Taiwan University Hospital has established a web-based real-time surveillance system based on algorithms for AMR pathogens, UTI and BSI. The surveillance system is sophisticated in its ability to integrate and analyse several data sources [32, 33]. Their studies and a recent systematic review of the literature demonstrated that adopting electronic surveillance software yields considerable time savings pertaining to case findings, data collection, case ascertainment and classification while maintaining high levels of sensitivity and specificity [31‐33]. Thus, information technology may represent an opportunity for countries seeking to establish HAI surveillance and overcome the gaps of human resources.

Our study provides a framework for other countries to establish or improve surveillance and IPC programs. Further studies on cost-effectiveness of these strategies will be helpful to relevant stakeholders as they allocate and prioritize budget for infection control. Our work also serves as the foundation for possible regional collaborations in East Asia or in greater Asia. Standardization of protocols will allow inter-country comparison and benchmarking. For Europe, the similarities and differences in HAI trends between our study and the HAI-net re-affirmed the need for continual surveillance and IPC efforts.

The strengths of this study were our ability to obtain an overview of the surveillance and IPC programs of Taiwan, Korea, and Japan that were seldom described in past reports. We were also able to obtain comprehensive HAI data from their surveillance systems and compare these data with Western developed countries and developing countries worldwide. The limitations were the need to use open access datasets. This restricted our ability to assess and compare HAI epidemiology comprehensively across the three countries. JANIS only releases data on UTI, CLABSI, and VAP in its surveillance reports. Information on the other infection modules: CAUTI, BSI, and HAP were unavailable. We were unable to comprehensively describe the complete pathogen rankings and AMR profiles for each country, because these data were unavailable on some surveillance systems. There are differences in protocols employed by each surveillance system, such as JANIS, which calculated device-associated infections differently. Standardization of protocols should allow for inter-country comparison. Furthermore, we need to include antibiotic use in future studies because of their critical impact on development of resistance. Finally, there were differences in the types of the hospitals enrolled in the three systems, wide variation of hospital participation rates (6.8% in Japan and 100% in Taiwan), and thus, discrepancies in hospital coverage rates (1.9% in Japan and 21.2% in Taiwan). Therefore, data presented here cannot be generalized to the entire 3 countries.

We found that national surveillance data obtained from Taiwan, South Korea, and Japan from 2008 to 2015 was associated with a 53.0% reduction in HAI in surveyed ICUs. There were differences among the countries in surveillance protocols, hospital coverage rates, national IPC programs, distribution of invading microorganisms and antibiotic resistance. The overall decrease in HAI appears to be due to improved surveillance coupled with a series of interventions in each country. We propose that a regional HAI network be established in East Asia similar to Europe’s HAI-net. Such a coordinated effort should enable greater regional collaborations and development of joint strategies as we learn from one another.