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Trends in prevalence of healthcare-associated infections and antimicrobial use in hospitals in the Netherlands: 10 years of national point-prevalence surveys
Journal Pre-proof Trends in prevalence of healthcare-associated infections and antimicrobial use in hospitals in the Netherlands: 10 years of national point-prevalence surveys T.E.M. Hopmans, E.A. Smid, J.C. Wille, T.I.I. van der Kooi, M.B.G. Koek, M.C. Vos, S.E. Geerlings, S.C. de Greeff PII:
S0195-6701(19)30433-5
DOI:
https://doi.org/10.1016/j.jhin.2019.10.005
Reference:
YJHIN 5821
To appear in:
Journal of Hospital Infection
Received Date: 6 August 2019 Revised Date:
2 October 2019
Accepted Date: 3 October 2019
Please cite this article as: Hopmans TEM, Smid EA, Wille JC, van der Kooi TII, Koek MBG, Vos MC, Geerlings SE, de Greeff SC, Trends in prevalence of healthcare-associated infections and antimicrobial use in hospitals in the Netherlands: 10 years of national point-prevalence surveys, Journal of Hospital Infection, https://doi.org/10.1016/j.jhin.2019.10.005. This is a PDF file of an article that has undergone enhancements after acceptance, such as the addition of a cover page and metadata, and formatting for readability, but it is not yet the definitive version of record. This version will undergo additional copyediting, typesetting and review before it is published in its final form, but we are providing this version to give early visibility of the article. Please note that, during the production process, errors may be discovered which could affect the content, and all legal disclaimers that apply to the journal pertain. © 2019 The Healthcare Infection Society. Published by Elsevier Ltd. All rights reserved.
T.E.M. Hopmans et al. Trends in prevalence of healthcare-associated infections and antimicrobial use in hospitals in the Netherlands: 10 years of national point-prevalence surveys T.E.M. Hopmansa,*, E.A. Smida, J.C. Willea, T.I.I. van der Kooia, M.B.G. Koeka, M.C. Vosb, S.E. Geerlingsc, S.C. de Greeffa a
Department of Epidemiology and Surveillance, National Institute for Public Health and the
Environment (RIVM), Bilthoven, The Netherlands b
Department of Medical Microbiology and Infectious Diseases, Erasmus MC, University
Medical Centre Rotterdam, Rotterdam, The Netherlands c
Department of Infectious Diseases, University Medical Centre Amsterdam, Amsterdam, The
Netherlands ______________________ *
Corresponding author. Address: National Institute for Public Health and the Environment,
Department of Epidemiology and Surveillance, A. van Leeuwenhoeklaan 9, Bilthoven, 3721MA, The Netherlands. Tel.: +31 621112694. E-mail address: [email protected] (T.E.M. Hopmans). SUMMARY Background: Prevalence of healthcare-associated infections (HCAIs) and antimicrobial use in hospitals in the Netherlands has been measured using voluntary biannual national pointprevalence surveys (PPSs). Aim: To describe trends in the prevalence of patients with HCAI, risk factors, and antimicrobial use in 2007–2016. Methods: In the PPS, patient characteristics, use of medical devices and antimicrobials, and presence of HCAI on the survey day are reported for all hospitalized patients, excluding patients in the day-care unit and psychiatric wards. Analyses were performed using linear and (multivariate) logistic regression, accounting for clustering of patients within hospitals. Findings: PPS data were reported for 171,116 patients. Annual prevalence of patients with HCAI with onset during hospitalization decreased from 6.1% in 2007 to 3.6% in 2016. The adjusted odds ratio (OR) for trend was 0.97 (95% confidence interval: 0.96–0.98). Most prominent trends were seen for surgical site infections (1.6% to 0.7%; OR: 0.31 (0.26–0.38)) and urinary tract infections (2.1% to 0.6%; OR: 0.18 (0.15–0.22)). From 2014 on, HCAIs at admission were also registered with a stable prevalence of approximately 1.5%. The mean length of stay decreased from 10 to 7 days. The percentage of patients treated with antibiotics increased from 31% to 36% (OR: 1.03 (1.02–1.03)). 1
Conclusion: Repeated PPS data from 2007 to 2016 show a decrease in the prevalence of patients with HCAI with onset during hospitalization, and a stable prevalence of patients with HCAI at admission. The adjusted OR of 0.97 for HCAI during hospitalization indicates a true reduction in prevalence of approximately 3% per year. Keywords: Healthcare-associated infection Repeated prevalence Antimicrobial use Infection prevention and control Length of stay Surveillance Introduction Healthcare-associated infections (HCAIs) contribute substantially to morbidity and mortality and are therefore recognized as a public health problem. A meta-analysis from studies in mixed patient populations revealed a pooled prevalence of 7.1% (95% confidence interval (CI): 6.5–7.8) in high-income countries [1]. Cassini et al. estimated that in the European Union and European Economic Area (EU/EEA) each year more than 91,000 deaths were attributable to the most frequent HCAIs [2]. As a proportion of the HCAIs are preventable, they are considered a marker of the quality of patient care [3]. To measure the frequency and burden of HCAIs, incidence surveillance of HCAIs is considered the reference standard. However, hospital-wide incidence surveillance for all HCAI types is very timeconsuming and hence not feasible. As such, the results of incidence surveillance mostly do not allow estimation of the burden of all HCAIs combined. Therefore, to gain insight into nationwide trends and burden of HCAI, repeated point-prevalence surveys of all HCAIs are a helpful tool. In the Netherlands, the national surveillance network PREZIES (PREvention of HCAIs (‘ZIEkenhuisinfecties’) through Surveillance) has coordinated a bi-annual PPS since 2007. This article provides a descriptive epidemiological presentation of the 10 years of national surveillance data, determining long-term trends in HCAIs and risk factors for HCAIs, such as use of medical devices and antimicrobial use. Methods PPS: population, inclusion, protocol, and HCAI definitions Dutch acute care hospitals participate voluntarily in the national PPSs, which are yearly performed in March and October following a standardized protocol [4,5]. Due to frequent hospital mergers in the Netherlands, the total number of hospitals decreased from 95 in 2007 to 77 in 2016 [6,7]. In 2016, 43 of them (56%) were primary hospitals (general 2
hospital without teaching function), 26 (34%) secondary hospitals (general hospital with teaching function) and eight (10%) tertiary (university) hospitals. A hospital participating in the PPS, in short, includes all inpatients admitted to the hospital before the day of the survey, and determines the presence of an HCAI on the day of survey by the local infection control team (i.e. infection control professionals and medical microbiologists). Per ward, the surveillance is performed on a single day. The hospital-wide surveillance can be performed within one month, but each patient may be enrolled only once. Patients admitted in psychiatric and day-care units, such as dialysis, are excluded. The following data are collected: (i) the presence of and category of HCAIs on the survey day, their causative micro-organisms, and their resistance patterns [8]; (ii) presence of infection on the day of hospital admission (not HCAI); (iii) treating specialty; (iv) demographics (age, gender); (v) risk factors for HCAI (surgery since admission, presence of medical devices on the survey day, McCabe score (i.e. classification of the severity of underlying medical conditions in three categories: non-fatal disease; ultimately fatal disease; rapidly fatal disease or unknown [9]); (vi) antimicrobial use including indication; and (vii) time to infection for those with HCAI (defined as time from admission to onset of HCAI, optionally). The latter three were reported from 2011 onwards. HCAIs have been defined following the European Centre for Disease Prevention and Control (ECDC) definitions [9,10]. An infection is considered an HCAI if it occurs during or after hospitalization, without any evidence that the infection was present or had been incubating on admission [11]. An HCAI is considered to be present or active as long as the patient is symptomatic or receiving treatment for the infection on the day of the survey. From 2014 onwards, the registration was changed; HCAIs already present at the day of (re)admission were also included in the survey. To identify HCAIs at admission, a specific time-interval (length depending on the type of HCAI) between first admission (in the same or another hospital) and readmission had to be met [9]. The ECDC definitions for surgical site infection (SSI) following vaginal surgery and central line-associated bloodstream infection (CLABSI) are adapted to the Dutch situation as described elsewhere [11,12]. Medical devices (urinary catheter, central lines, and intubation) are recorded on the survey day and retrospectively for the previous six days, allowing the calculation of catheter-associated urinary tract infection (CAUTI), CLABSI, and ventilator-associated pneumonia (VAP). Asymptomatic UTIs are not reported. Data analyses
3
The yearly HCAI prevalence was calculated as the total number of patients with at least one HCAI per year (surveys of March and October combined) divided by the total number of included patients per year. Trends over time in prevalence and patient characteristics were analysed with linear and logistic regression methods, while accounting for clustering of patients within hospitals. Calendar year was recoded to year of surveillance (1 to 10) to calculate the trend per year with 95% confidence intervals (CIs). Multivariate regression analysis was performed to calculate trend in HCAI prevalence, while adjusting for gender, age categories, length of stay until survey day, previous surgery, and hospital type. Trend analyses were performed for all hospitals and for hospitals that participated for at least three calendar years. All analyses were conducted using SAS 9.4 (SAS Institute, Carey, NC, USA). Results Participation The number of hospitals participating each year varied from 30 in 2007 to 42 in 2016. Seventy-three hospitals (95%, using the 2016 number of hospitals as denominator) participated for at least three years and 45 hospitals (58%) participated for at least five years (range: 1–10). The distribution of the participating hospitals is included in Supplementary Table S1. Prevalence of patients with HCAI Annual prevalence of patients with HCAI with onset during current hospitalization decreased from 6.1% in 2007 to 3.6% in 2016 (Figure 1) and this decrease was observed in all types of hospitals [13]. The crude OR for trend for all hospitals was 0.92 (95% CI: 0.91– 0.93), and the OR adjusted for available confounders was 0.97 (95% CI: 0.96–0.98), indicating a 3% reduction in prevalence per year. When including only the hospitals that participated for at least three years the crude OR for trend was 0.93 (0.92–0.94), and the adjusted OR was 0.97 (0.96–0.98). The most prevalent HCAIs were lower respiratory tract infections and SSIs (Table I). The percentage of patients with more than one HCAI decreased from 0.8% in 2007 to 0.2% in 2016. The prevalence of patients with HCAI already present at admission was approximately 1.5% in 2014–2016 (Figure 1). Of these, 19% were related to a previous admission in a hospital other than the one reporting the HCAI. Of all HCAIs present at admission, 68% were SSIs, with a stable prevalence of approximately 1.2%. Although prevalence decreased significantly over time for all types of HCAI with onset during current hospitalization, crude ORs for trend were highest for SSI, UTI, and ‘other types of HCAI’ (e.g. skin, central nervous system infection; eye, ear, nose throat or mouth infection) (Table I and Supplementary Figure S1). 4
Resistant micro-organisms isolated in HCAIs Annually, for 70–75% of HCAIs the causative micro-organisms were documented. The most reported pathogens each year were Staphylococcus aureus and Escherichia coli. From 2014 on, resistance patterns of micro-organisms were reported. In 2687 HCAI, 2057 cultures were reported positive. Carbapenem resistance was reported in 0.5% (N = 11) of Enterobacterales and in 0.8% (N = 17) of Pseudomonas aeruginosa, resistance to thirdgeneration cephalosporins in 5.8% (N = 120) of Enterobacterales, glycopeptide resistance in 0.2% (N = 4) of Enterococcus faecium, and oxacillin resistance in 0.7% (N = 14) of S. aureus. Due to the low numbers of resistant micro-organisms per year, trends could not be calculated. Patient characteristics Patient characteristics remained stable over the years and the percentage of patients with surgery significantly decreased from 37% in 2007 to 30% in 2016 (Supplementary Table S2). The mean length of stay (LOS) from admission to the day of the PPS decreased significantly from 10 to seven days for all patients, and from 26 to 18 days for patients with HCAI (P = 0.003; Figure 2). The mean time to infection remained stable (15 days) over the years. The proportion of patients with at least one medical device increased from 52% to 61% caused by a significant increase in the use of peripheral vascular catheters, from 43% in 2007 to 53% in 2016 (OR: 1.06 (1.05–1.06)) (Figure 3). The percentage of patients with antimicrobials on the day of survey increased from 31% to 36% (OR: 1.03 (1.02–1.03)). From 2011 onwards, 65% of the participating hospitals also reported the indication for antimicrobial use. The indication ‘treatment of communityassociated infection’ increased from 21% in 2011, to 33% in 2016 (OR: 1.42 (1.41–1.44)). The indication ‘treatment of HCAI’ remained stable, approximately 8% (Supplementary Table S2). Discussion From 2007 to 2016 the reported prevalence of HCAIs with onset during the current hospitalization decreased by 40% in the Netherlands. The prevalence of HCAI at admission (measured from 2014 onwards) remained stable at approximately 1.5%. The crude decrease in prevalence of HCAI with onset during current hospitalization may in theory be explained by several reasons, such as the simultaneous decline in LOS or the decrease in the proportion of patients with surgery. However, after correction for these and other potential confounders, the analyses of trend of HCAI prevalence over time still resulted in a significantly decreased odds of 0.97 per year, indicating a real reduction of approximately 3% per year. This is in line with 5
the hypothesis that repeated PPSs and feedback of the results may have increased awareness to prevent HCAI [14–16]. As the reduced chance to acquire and find an HCAI during admission (due to the shorter LOS) partly explained the observed crude decrease in HCAI, one could hypothesize that an increasing number of infections only manifests after discharge. It is unknown how many patients with HCAIs are treated in the outpatient department or by their general practitioner, but for the last three years HCAIs at admission are also included in the Dutch PPS. Although this is a short period, there does not seem to be an increase over time in HCAIs, including SSIs, at admission. Another explanation for the reduction in HCAI prevalence may be the Dutch Hospital Patient Safety Program which was initiated in 2008, introducing among others an SSI prevention bundle [17]. Compliance with this bundle resulted in a decrease in SSI incidence for specific procedures [18]. Likewise, from 2009 onwards, ‘surveillance of (in)appropriate use of urinary catheters (UCs)’ was integrated (optionally) into our prevalence survey [19]. Both interventions have probably successfully affected trends in HCAI, similar to that reported by other countries following the introduction of infection prevention programmes [20,21]. For instance, the proportion of patients with a UC remained around 20% in the period under study, while the prevalence of CAUTI decreased significantly from 1.4% to 0.4%. It is known that reduction of UC duration prevents the onset of CAUTI [20–22]. Unfortunately data regarding the number of UC-days in our surveillance were lacking, but it might be hypothesized that the increased awareness caused by the optional surveillance of (in)appropriate use of UC and the decrease in LOS has contributed to a decrease of CAUTI either directly or through a probable reduction of UCdays over the years. Finally, it is also possible that the periodic mandatory onsite validation visits, and the yearly workshops organized by the PREZIES team, may have improved use of case definitions and registration procedures, leading to a more strict application of the HCAI criteria [23]. The validations, at least once per hospital during the period under study, revealed overall discordant results in 6.7% of the data sample, mainly caused by HCAIs that were reported but did not meet the surveillance definitions (false positives). Remarkably, the proportion of patients with at least one medical device in our study increased significantly during the 10 years, which was mainly attributed to the use of peripheral catheters. This could reflect a more seriously ill hospital population. However, distribution of the McCabe score, which was reported from 2011 onwards, remained stable. It is questionable whether the McCabe score is adequately sensitive for this purpose. 6
PREZIES participated in the two European-wide PPSs of HCAIs and antimicrobial use in acute care hospitals, which were coordinated by the ECDC [9,10,24–26]. Despite uniform case definitions, the prevalence of HCAIs is difficult to compare between countries due to differences in representativeness of hospitals, heterogeneous study populations, and differences in capacity for diagnostic testing [24]. Repeated PPSs within countries are, however, useful for detecting trends in HCAI, medical device, and antimicrobial use. Traditionally, prudent use of antimicrobials is advocated in the Netherlands and the Dutch working party on Antibiotic Policy introduced antimicrobial stewardship as part of the national action plan against antimicrobial resistance in 2012 [27,28]. Despite this policy, the overall percentage of in-hospital patients on antimicrobial treatment on the survey day increased significantly in the 10 years of the PPS. The increase might be the result of a shorter LOS, resulting in a higher proportion of patients in an acute stage of care, and not of an increased administration of antimicrobial per individual patient. This is confirmed by the observation that the proportion of patients on antimicrobial treatment during the first days of admission did not increase (data not shown). Whereas in the European PPS of 2011–2012 on average 95% of the patients with HCAIs received antimicrobials, and in the USA antimicrobial treatment is considered as the most sensitive proxy indicator for the presence of HCAIs, in the Netherlands only 80% of the patients with HCAIs are treated with antimicrobials [24,29,30]. This is probably explained by other effective treatment of HCAIs such as removal of medical devices, irrigation of wounds or that – in line with the Dutch guidelines – treatment with antimicrobials was not indicated. To the best of our knowledge, this is one of the few national PPSs that has been repeated (bi)annually for 10 years, enabling interpretation of national trends in HCAIs and antimicrobial use. The strength of this survey is the use of standardized definitions following the ECDC definitions and registration of all types of HCAI. Other countries performed PPSs less frequently, selected only specific HCAIs, or were not patient-based [24,31]. Despite surveillance of HCAIs not being mandatory in the Netherlands, 95% of hospitals have participated in the PPS for at least three years and 58% of hospitals participated for more than five years. In addition, the participation of primary, secondary, and tertiary hospitals in the PPSs fluctuated over the years but fairly represented the distribution of hospital types. It should be stressed, however, that repeated PPSs can never replace surveillance of HCAIs at hospital level, because HCAIs are rare and 95% CIs are wide, due to which no detection of short- or medium-term trends at hospital level is possible. Due to this limitation and considering that performing a PPS brings a substantial workload, the frequency of the Dutch PPS is currently being discussed. Nevertheless, the PPS enhances awareness and 7
thus warrants continued measurements, but perhaps at a lower frequency. The annual training of hospital infection control teams resulted in a positive predictive value for diagnosis of HCAI of 81.5% and a negative predictive value of 97.2% (data not shown). Therefore, PPSs are considered a useful tool to monitor trends in the prevalence and distribution of HCAIs at national level. Despite the use of standardized definitions, assessment of the presence of HCAIs based on patient records is influenced by personal experience and training of the surveyor. It is therefore important to offer easily accessible support, yearly workshops, and enhanced training of infection control teams to minimize the risk of misclassification. In conclusion, although prevalence rates may not be suitable for direct comparison within and between hospitals, at national level repeated PPSs are useful to analyse trends in HCAIs. As such, repeated national PPSs can be used in addition to targeted incidence surveillance (e.g. device-associated and surgery-related HCAIs) [32]. In the Netherlands, the repeated PPSs revealed a significant decline in the prevalence of patients with SSI and UTI with onset during current hospitalization. To reduce the workload of PPSs and improve standardization for all hospital registrations we should explore the possibility of (semi)automated surveillance using electronic data elements and algorithms [33–35]. Acknowledgements The surveys would not have been possible without the participation and contribution of infection control departments, microbiologists, and other staff from the participating hospitals. We thank them for their invaluable work. Conflict of interest statement None declared. Funding sources None. Supplementary Appendix Supplementary data related to this article can be found at …
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Table I Prevalence (%) of patients with HCAI and device-associated HCAI with onset during current hospitalization and crude OR for trend HCAI
2007
2008
2009
2010
2011
2012
2013
2014
2015
2016
OR
95% CI
SSI
1.6
1.8
1.5
1.2
1.1
1.0
0.7
0.8
0.8
0.8
0.91
0.90–0.93
UTI
2.1
1.7
1.4
1.3
0.9
0.8
0.5
0.7
0.6
0.6
0.85
0.83–0.87
CAUTI
1.4
1.2
0.9
0.8
0.6
0.5
0.3
0.4
0.4
0.4
0.85
0.83–0.87
LRTI
1.4
1.5
1.2
1.1
1.0
0.9
0.9
1.0
1.0
1.2
0.97
0.95–0.99
VAP
0.5
0.4
0.3
0.3
0.3
0.2
0.2
0.2
0.2
0.2
0.93
0.89–0.97
BSI
0.9
1.0
0.9
0.8
0.7
0.7
0.6
0.7
0.6
0.7
0.96
0.94–0.98
CLABSI
0.3
0.3
0.2
0.3
0.1
0.2
0.2
0.2
0.1
0.1
0.90
0.87–0.94
GI
0.3
0.4
0.2
0.4
0.2
0.2
0.2
0.2
0.3
0.2
0.92
0.89–0.96
Other
0.7
0.8
0.6
0.5
0.4
0.3
0.3
0.3
0.3
0.4
0.88
0.86–0.92
All HCAI
6.1
6.1
5.1
4.8
4.1
3.5
3.0
3.4
3.4
3.6
0.92
0.91–0.93
HCAI, healthcare-associated infection; OR, odds ratio; CI, confidence interval; SSI, surgical site infection; UTI, urinary tract infection; CAUTI, urinary catheter-associated UTI; LRTI, lower respiratory tract infection; VAP, ventilator-associated pneumonia; BSI, bloodstream infection; CLABSI, central line-associated BSI; GI, gastrointestinal infection; Other, group of other infections.
13
Figure 1. Overall prevalence of patients with healthcare-associated infection (HCAI) with onset during current hospitalization and of patients with HCAI already present at admission. 95% confidence intervals around the prevalence estimates were calculated with the Wilson score [13].
Overall prevalence 7 6
Prevalence (%)
5 4 3 2 1 0 2007
2008
2009
2010
2011
2012
2013
2014
2015
2016
Prevalence of patients with HAI with onset during current hospitalization Prevalence of patients with HAI at admission
14
Figure 2. Length of stay of patients with and without healthcare-associated infection (HCAI) until the survey day and time to infection.
30 25
Days
20 15 10 5 0 2007
2008
2009
Patients with HAI
2010
2011
2012
2013
patients without HAI
2014
2015
2016
Time to infection
15
Figure 3. Proportion of patients with medical device use.
Percentage of patients
60 50 40 30 20 10 0 2007 2008 2009 2010 2011 2012 2013 2014 2015 2016 Peripheral Venous catheter
Urinary catheter
Central Venous Catheter
Intubation
16
S0195-6701(19)30433-5
DOI:
https://doi.org/10.1016/j.jhin.2019.10.005
Reference:
YJHIN 5821
To appear in:
Journal of Hospital Infection
Received Date: 6 August 2019 Revised Date:
2 October 2019
Accepted Date: 3 October 2019
Please cite this article as: Hopmans TEM, Smid EA, Wille JC, van der Kooi TII, Koek MBG, Vos MC, Geerlings SE, de Greeff SC, Trends in prevalence of healthcare-associated infections and antimicrobial use in hospitals in the Netherlands: 10 years of national point-prevalence surveys, Journal of Hospital Infection, https://doi.org/10.1016/j.jhin.2019.10.005. This is a PDF file of an article that has undergone enhancements after acceptance, such as the addition of a cover page and metadata, and formatting for readability, but it is not yet the definitive version of record. This version will undergo additional copyediting, typesetting and review before it is published in its final form, but we are providing this version to give early visibility of the article. Please note that, during the production process, errors may be discovered which could affect the content, and all legal disclaimers that apply to the journal pertain. © 2019 The Healthcare Infection Society. Published by Elsevier Ltd. All rights reserved.
T.E.M. Hopmans et al. Trends in prevalence of healthcare-associated infections and antimicrobial use in hospitals in the Netherlands: 10 years of national point-prevalence surveys T.E.M. Hopmansa,*, E.A. Smida, J.C. Willea, T.I.I. van der Kooia, M.B.G. Koeka, M.C. Vosb, S.E. Geerlingsc, S.C. de Greeffa a
Department of Epidemiology and Surveillance, National Institute for Public Health and the
Environment (RIVM), Bilthoven, The Netherlands b
Department of Medical Microbiology and Infectious Diseases, Erasmus MC, University
Medical Centre Rotterdam, Rotterdam, The Netherlands c
Department of Infectious Diseases, University Medical Centre Amsterdam, Amsterdam, The
Netherlands ______________________ *
Corresponding author. Address: National Institute for Public Health and the Environment,
Department of Epidemiology and Surveillance, A. van Leeuwenhoeklaan 9, Bilthoven, 3721MA, The Netherlands. Tel.: +31 621112694. E-mail address: [email protected] (T.E.M. Hopmans). SUMMARY Background: Prevalence of healthcare-associated infections (HCAIs) and antimicrobial use in hospitals in the Netherlands has been measured using voluntary biannual national pointprevalence surveys (PPSs). Aim: To describe trends in the prevalence of patients with HCAI, risk factors, and antimicrobial use in 2007–2016. Methods: In the PPS, patient characteristics, use of medical devices and antimicrobials, and presence of HCAI on the survey day are reported for all hospitalized patients, excluding patients in the day-care unit and psychiatric wards. Analyses were performed using linear and (multivariate) logistic regression, accounting for clustering of patients within hospitals. Findings: PPS data were reported for 171,116 patients. Annual prevalence of patients with HCAI with onset during hospitalization decreased from 6.1% in 2007 to 3.6% in 2016. The adjusted odds ratio (OR) for trend was 0.97 (95% confidence interval: 0.96–0.98). Most prominent trends were seen for surgical site infections (1.6% to 0.7%; OR: 0.31 (0.26–0.38)) and urinary tract infections (2.1% to 0.6%; OR: 0.18 (0.15–0.22)). From 2014 on, HCAIs at admission were also registered with a stable prevalence of approximately 1.5%. The mean length of stay decreased from 10 to 7 days. The percentage of patients treated with antibiotics increased from 31% to 36% (OR: 1.03 (1.02–1.03)). 1
Conclusion: Repeated PPS data from 2007 to 2016 show a decrease in the prevalence of patients with HCAI with onset during hospitalization, and a stable prevalence of patients with HCAI at admission. The adjusted OR of 0.97 for HCAI during hospitalization indicates a true reduction in prevalence of approximately 3% per year. Keywords: Healthcare-associated infection Repeated prevalence Antimicrobial use Infection prevention and control Length of stay Surveillance Introduction Healthcare-associated infections (HCAIs) contribute substantially to morbidity and mortality and are therefore recognized as a public health problem. A meta-analysis from studies in mixed patient populations revealed a pooled prevalence of 7.1% (95% confidence interval (CI): 6.5–7.8) in high-income countries [1]. Cassini et al. estimated that in the European Union and European Economic Area (EU/EEA) each year more than 91,000 deaths were attributable to the most frequent HCAIs [2]. As a proportion of the HCAIs are preventable, they are considered a marker of the quality of patient care [3]. To measure the frequency and burden of HCAIs, incidence surveillance of HCAIs is considered the reference standard. However, hospital-wide incidence surveillance for all HCAI types is very timeconsuming and hence not feasible. As such, the results of incidence surveillance mostly do not allow estimation of the burden of all HCAIs combined. Therefore, to gain insight into nationwide trends and burden of HCAI, repeated point-prevalence surveys of all HCAIs are a helpful tool. In the Netherlands, the national surveillance network PREZIES (PREvention of HCAIs (‘ZIEkenhuisinfecties’) through Surveillance) has coordinated a bi-annual PPS since 2007. This article provides a descriptive epidemiological presentation of the 10 years of national surveillance data, determining long-term trends in HCAIs and risk factors for HCAIs, such as use of medical devices and antimicrobial use. Methods PPS: population, inclusion, protocol, and HCAI definitions Dutch acute care hospitals participate voluntarily in the national PPSs, which are yearly performed in March and October following a standardized protocol [4,5]. Due to frequent hospital mergers in the Netherlands, the total number of hospitals decreased from 95 in 2007 to 77 in 2016 [6,7]. In 2016, 43 of them (56%) were primary hospitals (general 2
hospital without teaching function), 26 (34%) secondary hospitals (general hospital with teaching function) and eight (10%) tertiary (university) hospitals. A hospital participating in the PPS, in short, includes all inpatients admitted to the hospital before the day of the survey, and determines the presence of an HCAI on the day of survey by the local infection control team (i.e. infection control professionals and medical microbiologists). Per ward, the surveillance is performed on a single day. The hospital-wide surveillance can be performed within one month, but each patient may be enrolled only once. Patients admitted in psychiatric and day-care units, such as dialysis, are excluded. The following data are collected: (i) the presence of and category of HCAIs on the survey day, their causative micro-organisms, and their resistance patterns [8]; (ii) presence of infection on the day of hospital admission (not HCAI); (iii) treating specialty; (iv) demographics (age, gender); (v) risk factors for HCAI (surgery since admission, presence of medical devices on the survey day, McCabe score (i.e. classification of the severity of underlying medical conditions in three categories: non-fatal disease; ultimately fatal disease; rapidly fatal disease or unknown [9]); (vi) antimicrobial use including indication; and (vii) time to infection for those with HCAI (defined as time from admission to onset of HCAI, optionally). The latter three were reported from 2011 onwards. HCAIs have been defined following the European Centre for Disease Prevention and Control (ECDC) definitions [9,10]. An infection is considered an HCAI if it occurs during or after hospitalization, without any evidence that the infection was present or had been incubating on admission [11]. An HCAI is considered to be present or active as long as the patient is symptomatic or receiving treatment for the infection on the day of the survey. From 2014 onwards, the registration was changed; HCAIs already present at the day of (re)admission were also included in the survey. To identify HCAIs at admission, a specific time-interval (length depending on the type of HCAI) between first admission (in the same or another hospital) and readmission had to be met [9]. The ECDC definitions for surgical site infection (SSI) following vaginal surgery and central line-associated bloodstream infection (CLABSI) are adapted to the Dutch situation as described elsewhere [11,12]. Medical devices (urinary catheter, central lines, and intubation) are recorded on the survey day and retrospectively for the previous six days, allowing the calculation of catheter-associated urinary tract infection (CAUTI), CLABSI, and ventilator-associated pneumonia (VAP). Asymptomatic UTIs are not reported. Data analyses
3
The yearly HCAI prevalence was calculated as the total number of patients with at least one HCAI per year (surveys of March and October combined) divided by the total number of included patients per year. Trends over time in prevalence and patient characteristics were analysed with linear and logistic regression methods, while accounting for clustering of patients within hospitals. Calendar year was recoded to year of surveillance (1 to 10) to calculate the trend per year with 95% confidence intervals (CIs). Multivariate regression analysis was performed to calculate trend in HCAI prevalence, while adjusting for gender, age categories, length of stay until survey day, previous surgery, and hospital type. Trend analyses were performed for all hospitals and for hospitals that participated for at least three calendar years. All analyses were conducted using SAS 9.4 (SAS Institute, Carey, NC, USA). Results Participation The number of hospitals participating each year varied from 30 in 2007 to 42 in 2016. Seventy-three hospitals (95%, using the 2016 number of hospitals as denominator) participated for at least three years and 45 hospitals (58%) participated for at least five years (range: 1–10). The distribution of the participating hospitals is included in Supplementary Table S1. Prevalence of patients with HCAI Annual prevalence of patients with HCAI with onset during current hospitalization decreased from 6.1% in 2007 to 3.6% in 2016 (Figure 1) and this decrease was observed in all types of hospitals [13]. The crude OR for trend for all hospitals was 0.92 (95% CI: 0.91– 0.93), and the OR adjusted for available confounders was 0.97 (95% CI: 0.96–0.98), indicating a 3% reduction in prevalence per year. When including only the hospitals that participated for at least three years the crude OR for trend was 0.93 (0.92–0.94), and the adjusted OR was 0.97 (0.96–0.98). The most prevalent HCAIs were lower respiratory tract infections and SSIs (Table I). The percentage of patients with more than one HCAI decreased from 0.8% in 2007 to 0.2% in 2016. The prevalence of patients with HCAI already present at admission was approximately 1.5% in 2014–2016 (Figure 1). Of these, 19% were related to a previous admission in a hospital other than the one reporting the HCAI. Of all HCAIs present at admission, 68% were SSIs, with a stable prevalence of approximately 1.2%. Although prevalence decreased significantly over time for all types of HCAI with onset during current hospitalization, crude ORs for trend were highest for SSI, UTI, and ‘other types of HCAI’ (e.g. skin, central nervous system infection; eye, ear, nose throat or mouth infection) (Table I and Supplementary Figure S1). 4
Resistant micro-organisms isolated in HCAIs Annually, for 70–75% of HCAIs the causative micro-organisms were documented. The most reported pathogens each year were Staphylococcus aureus and Escherichia coli. From 2014 on, resistance patterns of micro-organisms were reported. In 2687 HCAI, 2057 cultures were reported positive. Carbapenem resistance was reported in 0.5% (N = 11) of Enterobacterales and in 0.8% (N = 17) of Pseudomonas aeruginosa, resistance to thirdgeneration cephalosporins in 5.8% (N = 120) of Enterobacterales, glycopeptide resistance in 0.2% (N = 4) of Enterococcus faecium, and oxacillin resistance in 0.7% (N = 14) of S. aureus. Due to the low numbers of resistant micro-organisms per year, trends could not be calculated. Patient characteristics Patient characteristics remained stable over the years and the percentage of patients with surgery significantly decreased from 37% in 2007 to 30% in 2016 (Supplementary Table S2). The mean length of stay (LOS) from admission to the day of the PPS decreased significantly from 10 to seven days for all patients, and from 26 to 18 days for patients with HCAI (P = 0.003; Figure 2). The mean time to infection remained stable (15 days) over the years. The proportion of patients with at least one medical device increased from 52% to 61% caused by a significant increase in the use of peripheral vascular catheters, from 43% in 2007 to 53% in 2016 (OR: 1.06 (1.05–1.06)) (Figure 3). The percentage of patients with antimicrobials on the day of survey increased from 31% to 36% (OR: 1.03 (1.02–1.03)). From 2011 onwards, 65% of the participating hospitals also reported the indication for antimicrobial use. The indication ‘treatment of communityassociated infection’ increased from 21% in 2011, to 33% in 2016 (OR: 1.42 (1.41–1.44)). The indication ‘treatment of HCAI’ remained stable, approximately 8% (Supplementary Table S2). Discussion From 2007 to 2016 the reported prevalence of HCAIs with onset during the current hospitalization decreased by 40% in the Netherlands. The prevalence of HCAI at admission (measured from 2014 onwards) remained stable at approximately 1.5%. The crude decrease in prevalence of HCAI with onset during current hospitalization may in theory be explained by several reasons, such as the simultaneous decline in LOS or the decrease in the proportion of patients with surgery. However, after correction for these and other potential confounders, the analyses of trend of HCAI prevalence over time still resulted in a significantly decreased odds of 0.97 per year, indicating a real reduction of approximately 3% per year. This is in line with 5
the hypothesis that repeated PPSs and feedback of the results may have increased awareness to prevent HCAI [14–16]. As the reduced chance to acquire and find an HCAI during admission (due to the shorter LOS) partly explained the observed crude decrease in HCAI, one could hypothesize that an increasing number of infections only manifests after discharge. It is unknown how many patients with HCAIs are treated in the outpatient department or by their general practitioner, but for the last three years HCAIs at admission are also included in the Dutch PPS. Although this is a short period, there does not seem to be an increase over time in HCAIs, including SSIs, at admission. Another explanation for the reduction in HCAI prevalence may be the Dutch Hospital Patient Safety Program which was initiated in 2008, introducing among others an SSI prevention bundle [17]. Compliance with this bundle resulted in a decrease in SSI incidence for specific procedures [18]. Likewise, from 2009 onwards, ‘surveillance of (in)appropriate use of urinary catheters (UCs)’ was integrated (optionally) into our prevalence survey [19]. Both interventions have probably successfully affected trends in HCAI, similar to that reported by other countries following the introduction of infection prevention programmes [20,21]. For instance, the proportion of patients with a UC remained around 20% in the period under study, while the prevalence of CAUTI decreased significantly from 1.4% to 0.4%. It is known that reduction of UC duration prevents the onset of CAUTI [20–22]. Unfortunately data regarding the number of UC-days in our surveillance were lacking, but it might be hypothesized that the increased awareness caused by the optional surveillance of (in)appropriate use of UC and the decrease in LOS has contributed to a decrease of CAUTI either directly or through a probable reduction of UCdays over the years. Finally, it is also possible that the periodic mandatory onsite validation visits, and the yearly workshops organized by the PREZIES team, may have improved use of case definitions and registration procedures, leading to a more strict application of the HCAI criteria [23]. The validations, at least once per hospital during the period under study, revealed overall discordant results in 6.7% of the data sample, mainly caused by HCAIs that were reported but did not meet the surveillance definitions (false positives). Remarkably, the proportion of patients with at least one medical device in our study increased significantly during the 10 years, which was mainly attributed to the use of peripheral catheters. This could reflect a more seriously ill hospital population. However, distribution of the McCabe score, which was reported from 2011 onwards, remained stable. It is questionable whether the McCabe score is adequately sensitive for this purpose. 6
PREZIES participated in the two European-wide PPSs of HCAIs and antimicrobial use in acute care hospitals, which were coordinated by the ECDC [9,10,24–26]. Despite uniform case definitions, the prevalence of HCAIs is difficult to compare between countries due to differences in representativeness of hospitals, heterogeneous study populations, and differences in capacity for diagnostic testing [24]. Repeated PPSs within countries are, however, useful for detecting trends in HCAI, medical device, and antimicrobial use. Traditionally, prudent use of antimicrobials is advocated in the Netherlands and the Dutch working party on Antibiotic Policy introduced antimicrobial stewardship as part of the national action plan against antimicrobial resistance in 2012 [27,28]. Despite this policy, the overall percentage of in-hospital patients on antimicrobial treatment on the survey day increased significantly in the 10 years of the PPS. The increase might be the result of a shorter LOS, resulting in a higher proportion of patients in an acute stage of care, and not of an increased administration of antimicrobial per individual patient. This is confirmed by the observation that the proportion of patients on antimicrobial treatment during the first days of admission did not increase (data not shown). Whereas in the European PPS of 2011–2012 on average 95% of the patients with HCAIs received antimicrobials, and in the USA antimicrobial treatment is considered as the most sensitive proxy indicator for the presence of HCAIs, in the Netherlands only 80% of the patients with HCAIs are treated with antimicrobials [24,29,30]. This is probably explained by other effective treatment of HCAIs such as removal of medical devices, irrigation of wounds or that – in line with the Dutch guidelines – treatment with antimicrobials was not indicated. To the best of our knowledge, this is one of the few national PPSs that has been repeated (bi)annually for 10 years, enabling interpretation of national trends in HCAIs and antimicrobial use. The strength of this survey is the use of standardized definitions following the ECDC definitions and registration of all types of HCAI. Other countries performed PPSs less frequently, selected only specific HCAIs, or were not patient-based [24,31]. Despite surveillance of HCAIs not being mandatory in the Netherlands, 95% of hospitals have participated in the PPS for at least three years and 58% of hospitals participated for more than five years. In addition, the participation of primary, secondary, and tertiary hospitals in the PPSs fluctuated over the years but fairly represented the distribution of hospital types. It should be stressed, however, that repeated PPSs can never replace surveillance of HCAIs at hospital level, because HCAIs are rare and 95% CIs are wide, due to which no detection of short- or medium-term trends at hospital level is possible. Due to this limitation and considering that performing a PPS brings a substantial workload, the frequency of the Dutch PPS is currently being discussed. Nevertheless, the PPS enhances awareness and 7
thus warrants continued measurements, but perhaps at a lower frequency. The annual training of hospital infection control teams resulted in a positive predictive value for diagnosis of HCAI of 81.5% and a negative predictive value of 97.2% (data not shown). Therefore, PPSs are considered a useful tool to monitor trends in the prevalence and distribution of HCAIs at national level. Despite the use of standardized definitions, assessment of the presence of HCAIs based on patient records is influenced by personal experience and training of the surveyor. It is therefore important to offer easily accessible support, yearly workshops, and enhanced training of infection control teams to minimize the risk of misclassification. In conclusion, although prevalence rates may not be suitable for direct comparison within and between hospitals, at national level repeated PPSs are useful to analyse trends in HCAIs. As such, repeated national PPSs can be used in addition to targeted incidence surveillance (e.g. device-associated and surgery-related HCAIs) [32]. In the Netherlands, the repeated PPSs revealed a significant decline in the prevalence of patients with SSI and UTI with onset during current hospitalization. To reduce the workload of PPSs and improve standardization for all hospital registrations we should explore the possibility of (semi)automated surveillance using electronic data elements and algorithms [33–35]. Acknowledgements The surveys would not have been possible without the participation and contribution of infection control departments, microbiologists, and other staff from the participating hospitals. We thank them for their invaluable work. Conflict of interest statement None declared. Funding sources None. Supplementary Appendix Supplementary data related to this article can be found at …
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Table I Prevalence (%) of patients with HCAI and device-associated HCAI with onset during current hospitalization and crude OR for trend HCAI
2007
2008
2009
2010
2011
2012
2013
2014
2015
2016
OR
95% CI
SSI
1.6
1.8
1.5
1.2
1.1
1.0
0.7
0.8
0.8
0.8
0.91
0.90–0.93
UTI
2.1
1.7
1.4
1.3
0.9
0.8
0.5
0.7
0.6
0.6
0.85
0.83–0.87
CAUTI
1.4
1.2
0.9
0.8
0.6
0.5
0.3
0.4
0.4
0.4
0.85
0.83–0.87
LRTI
1.4
1.5
1.2
1.1
1.0
0.9
0.9
1.0
1.0
1.2
0.97
0.95–0.99
VAP
0.5
0.4
0.3
0.3
0.3
0.2
0.2
0.2
0.2
0.2
0.93
0.89–0.97
BSI
0.9
1.0
0.9
0.8
0.7
0.7
0.6
0.7
0.6
0.7
0.96
0.94–0.98
CLABSI
0.3
0.3
0.2
0.3
0.1
0.2
0.2
0.2
0.1
0.1
0.90
0.87–0.94
GI
0.3
0.4
0.2
0.4
0.2
0.2
0.2
0.2
0.3
0.2
0.92
0.89–0.96
Other
0.7
0.8
0.6
0.5
0.4
0.3
0.3
0.3
0.3
0.4
0.88
0.86–0.92
All HCAI
6.1
6.1
5.1
4.8
4.1
3.5
3.0
3.4
3.4
3.6
0.92
0.91–0.93
HCAI, healthcare-associated infection; OR, odds ratio; CI, confidence interval; SSI, surgical site infection; UTI, urinary tract infection; CAUTI, urinary catheter-associated UTI; LRTI, lower respiratory tract infection; VAP, ventilator-associated pneumonia; BSI, bloodstream infection; CLABSI, central line-associated BSI; GI, gastrointestinal infection; Other, group of other infections.
13
Figure 1. Overall prevalence of patients with healthcare-associated infection (HCAI) with onset during current hospitalization and of patients with HCAI already present at admission. 95% confidence intervals around the prevalence estimates were calculated with the Wilson score [13].
Overall prevalence 7 6
Prevalence (%)
5 4 3 2 1 0 2007
2008
2009
2010
2011
2012
2013
2014
2015
2016
Prevalence of patients with HAI with onset during current hospitalization Prevalence of patients with HAI at admission
14
Figure 2. Length of stay of patients with and without healthcare-associated infection (HCAI) until the survey day and time to infection.
30 25
Days
20 15 10 5 0 2007
2008
2009
Patients with HAI
2010
2011
2012
2013
patients without HAI
2014
2015
2016
Time to infection
15
Figure 3. Proportion of patients with medical device use.
Percentage of patients
60 50 40 30 20 10 0 2007 2008 2009 2010 2011 2012 2013 2014 2015 2016 Peripheral Venous catheter
Urinary catheter
Central Venous Catheter
Intubation
16