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Staphylococcus aureus bacteraemia (SAB) is the second most common source of positive blood cultures, after Escherichia coli, reported within NHS Scotland. Laboratory surveillance has been mandatory in Scotland for SAB since 2001.
Aim
To gain an understanding of the epidemiology of SAB cases and associated risk factors for healthcare and true community onset. Identification of these factors and the patient populations at greatest risk enables the development of focused improvement plans.
Methods
All NHS boards within NHS Scotland take part in the mandatory enhanced surveillance, with data collected by trained data collectors using nationally agreed definitions.
Findings
Between 1st October 2014 and 31st March 2016, 2256 episodes of SAB in adults were identified. The blood cultures were taken in 58 hospitals and across all 15 Scottish health boards. The data demonstrated that approximately one-third of all SAB cases are true community cases. Vascular access devices continue to be the most reported entry point (25.7%) in individuals who receive health care, whereas skin and soft tissue risk factors are present in all origins. A significant risk factor unique to community cases is illicit drug injection.
Conclusion
Improvement plans for reduction of SAB should be targeted more widely than hospital care settings alone.
Staphylococcus aureus bacteraemia (SAB) is the second most common source of positive blood cultures, after Escherichia coli, reported within NHS Scotland [
]. Despite a decrease in the number of meticillin-resistant Staphylococcus aureus (MRSA) bacteraemias in recent years across the UK, there has not been a matching decrease in meticillin-sensitive S. aureus (MSSA) [
Reducing Staphylococcus aureus bloodstream infections associated with peripheral intravenous cannulae: successful implementation of a care bundle at a large Australian health service.
]. Health boards have been set targets to reduce SAB, but these have not been achieved in most years. In response, many infection prevention and control teams (IPCTs) within the health boards collected data on each SAB episode to be used locally for improvement [
]. However, with no agreed definitions, the enhanced data collected were not comparable across health boards. In 2013, IPCTs from the Scottish health boards and HPS agreed to standardize the data collected in Scotland, and develop an enhanced data set to be collected for every SAB episode.
This paper aims to provide analysis of the surveillance data, and the difference between SAB cases associated with health care and true community cases across NHS Scotland. Identification of risk factors and patient populations at greatest risk enables the development of focused improvement plans.
Methods
Data were collected between 1st October 2014 and 31st March 2016 through the mandatory SAB surveillance programme [
]. An episode of SAB was defined in the HPS SAB surveillance protocol as a positive blood culture for S. aureus with no positive S. aureus blood culture in the previous 14 days (rolling 14 days from previous positive sample), excluding post-mortem blood cultures [
], and collated information in an Excel (Microsoft Corp, Redmond, WA, USA) spreadsheet that was exported to the surveillance team at HPS at the end of each quarter.
The enhanced data collected included demographics, origin of infection, source of bacteraemia and risk factors. The origin of infection was divided into hospital-acquired (HAI), healthcare-associated (HCAI), community-acquired and not known using definitions modified from Morris and Russell [
]. In summary, HAI patients included patients who were in hospital for more than 48 h, patients discharged in the previous 48 h, renal dialysis patients, or patients in whom the positive blood culture was considered a contaminant. HCAI patients met one of the criteria of health care in the previous 30 days. Full details of the definitions are provided in HPS Protocol of Enhanced SAB surveillance [
The source field was a generic field that contained both entry point and sources of deep-seated/metastatic infection which was mapped to provide breakdown required for the analysis, and was recorded as undefined when this was not possible. Risk factors for invasive S. aureus infection were recorded. Data were collected on all in-situ devices at the time of the first positive blood aspirate, or in the 30 days prior, but not including devices inserted to treat SAB. Details were collected about skin integrity plus other risk factors including illicit intravenous drug use and immunosuppression [
]. More than one risk factor could be selected in any of the risk categories. A number of validation checks are carried out by HPS every quarter to cross-check the definitions and risk factors selected. However, it is recognized – particularly in community-acquired infections – that an entry point may never be determined.
All-cause 30-day mortality was calculated through linkage of the enhanced SAB data to National Records Scotland death records and SMR01 (Scottish Morbidity Recording) acute hospital episodes. Data were linked using the Community Health Index number.
Data analysis
Chi-squared tests were used to test for differences in the distributions of sex, age group, presence of device, skin or other risk factors, and entry point between the origin types. Logistic regression was used to estimate crude and adjusted odds ratios together with 95% confidence intervals for sex, age group, origin of infection, presence of device, skin or other risk factors, and entry point using SPSS Statistics Version 21.0 (ICM Corp., Armonk, NY, USA).
Results
Between 1st October 2014 and 31st March 2016, there were 2275 episodes of SAB in adults across 58 hospitals in Scotland. In 19 episodes, the data were incomplete so these cases were excluded from the study; in total, 2256 episodes were analysed. Of these, 186 (8%) were MRSA. SAB occurred more frequently in males (P<0.001) and the median age of cases was 66 years (Table I). HAIs accounted for 41.9% (N=945, 57 of these were contaminants), HCAIs accounted for 28.2% (N=636) and community-acquired infections accounted for 29.9% (N=675) of cases. Several variables were significantly associated with origin of infection, including age group, presence of a device, presence of other risk factors, entry point and type of deep-seated infection (Table I).
Table IPatient characteristics, presence of risk factors and source of entry point by origin of infection in 2256 episodes of Staphylococcus aureus bacteraemia
Includes, but not exclusively: indwelling VADs: (a) non-tunnelled central venous catheters (CVCs), tunnelled CVCs, dialysis lines, peripherally inserted central catheter lines, peripheral venous catheters and fistulas; (b) indwelling medical devices other than VADs such as chest drains, surgical drains, tracheostomy, epidural anaesthetic devices, spinal anaesthetic devices, nephrostomy, urethral catheter, suprapubic catheter, self catheterization, and percutaneous endoscopic gastrostomy tubes, inserted in the 30 days prior to the date when the positive blood culture was taken (applies to a and b).
Includes, but not exclusively: indwelling VADs: (a) non-tunnelled central venous catheters (CVCs), tunnelled CVCs, dialysis lines, peripherally inserted central catheter lines, peripheral venous catheters and fistulas; (b) indwelling medical devices other than VADs such as chest drains, surgical drains, tracheostomy, epidural anaesthetic devices, spinal anaesthetic devices, nephrostomy, urethral catheter, suprapubic catheter, self catheterization, and percutaneous endoscopic gastrostomy tubes, inserted in the 30 days prior to the date when the positive blood culture was taken (applies to a and b).
a Includes, but not exclusively: indwelling VADs: (a) non-tunnelled central venous catheters (CVCs), tunnelled CVCs, dialysis lines, peripherally inserted central catheter lines, peripheral venous catheters and fistulas; (b) indwelling medical devices other than VADs such as chest drains, surgical drains, tracheostomy, epidural anaesthetic devices, spinal anaesthetic devices, nephrostomy, urethral catheter, suprapubic catheter, self catheterization, and percutaneous endoscopic gastrostomy tubes, inserted in the 30 days prior to the date when the positive blood culture was taken (applies to a and b).
b Excluded cases with not known/undefined deep infection to test nature of infection alone.
In 69.2% (N=1562) of cases, the entry point was known; of these, 7.5% (N=117) also had a metastatic deep focus. In 30.8% (N=694) of cases, the entry point was not identified but a deep focus was present in 50.7% (N=352). The majority of SAB were related to an indwelling device, with vascular access devices (VADs) and devices other than VADs (non-VADs) being responsible for 21.4% (N=483) of the SABs in NHS Scotland. The most common VADs that resulted in SAB were peripheral venous catheters (PVCs) (7.6%, N=171), central venous catheters (CVCs) (4.2%, N=95) and dialysis lines (4.1%, N=93) (Figure 1). VADs and skin and soft tissue infections (SSTIs) together account for 36% (N=812) of the SAB entry points (Table I). Bone and joint infection was the most common deep-seated metastatic infection (8.4%; N=189), followed by cardiovascular infection (5.5%; N=123) and deep abscess/haematoma (4.5%; N=103) (Table I).
Figure 1Breakdown of device entry points. PVC, peripheral venous catheter; CVC, central venous catheter; PICC, peripherally inserted central catheter.
Table I shows the association found between the entry points recorded and the origin of infection (P<0.001). VADs accounted for 38.1% (N=360) of HAIs, SSTIs were the most common known entry point in HCAIs (23.9%; N=152), and illicit drug injection was the most common known entry point in community-acquired infections (27.9%; N=188). When the entry point was not known or not defined, 25.1% (N=174) of patients presented with a deep infection of bone or joint (Figure 2).
Figure 2Source of deep-seated/metastatic infection when entry point is not known/undefined.
The overall 30-day mortality rate was 20.7%. The rates in both HCAIs and HAIs were significantly higher than in community-acquired infections (22.9% and 23.3% vs 14.9%; P<0.001). However, when adjusting for risk factors in the multi-variable analysis, the difference became non-significant as a result of the higher proportion of younger people with lower mortality who had community-acquired infections. In the multi-variable analysis, only age group, and entry points of respiratory infection, SSTIs and not known/not defined remained significant factors for 30-day mortality, with borderline associations with origin (Table II).
Table IIUnivariable and multi-variable logistic regression results on 30-day mortality outcome
Looking at the risk factors recorded broken down by origin, it was found that SSTI risks were similar across the origin types (Table III). For HCAI cases, 46.6% (N=291) had a similar device risk. Previous hospital admission and medical instrumentation were commonly reported in both HAI and HCAI cases; 37.4% of HCAI patients had a previous hospital admission in the last 30 days (N=238). Patients being admitted from a long term care facility or another hospital only accounted for 5.9% (N=132) of the SAB cases. Of the 694 SAB cases where the entry point was not known or the only source recorded was a deep/metastatic infection, 81.9% of the HAIs had at least one device risk factor (Table IV). In contrast, approximately 50% of community-acquired cases with no known entry point did not have any recorded risk factors.
Table IIIRisk factors by origin of Staphylococcus aureus bacteraemia
Risk factors
Total, N=2256
CA, N=675
HCAI, N=636
HAI, N=945
N (%)
N (%)
N (%)
N (%)
Device risk factors
1103 (48.9%)
–
291 (45.8%)
812 (85.9%)
Skin and soft tissue risk factors
1079 (47.8%)
333 (49.3%)
319 (50.2%)
427 (45.2%)
Medical/surgical instrumentation within last 30 days
Includes, but not exclusively: indwelling vascular access devices (VADs): (a) non-tunnelled central venous catheters (CVCs), tunnelled CVCs, dialysis lines, peripherally inserted central catheter lines, peripheral venous catheters and fistulas; (b) indwelling medical devices other than VADs, such as chest drains, surgical drains, tracheostomy, epidural anaesthetic devices, spinal anaesthetic devices, nephrostomy, urethral catheter, suprapubic catheter, self catheterization, and percutaneous endoscopic gastrostomy tubes, inserted in the 30 days prior to the date when the positive blood culture was taken (applies to a and b).
Includes but not exclusively: infections of skin (pressure sores, trauma, ulcers, cuts, grazes, surgical incisions, burns and eczema), subcutaneous tissue, fascia and muscle (does not include deep-seated/metastatic soft tissue infection) that were present when the positive blood culture was taken.
Includes, but not exclusively: medical/surgical instrumentation, intramuscular, intravenous, subcutaneous, intra-articular medication, venepuncture, immunosuppression, diabetes mellitus, previous hospital admission or non-healthcare, cosmetic procedure breaking skin or mucous membranes in the 30 days prior to the positive blood culture being taken.
489 (70.5%)
96 (37.5%)
206 (90.4%)
187 (89.0%)
CA, community-acquired infection; HCAI, healthcare-associated infection; HAI, hospital-acquired infection.
a Includes, but not exclusively: indwelling vascular access devices (VADs): (a) non-tunnelled central venous catheters (CVCs), tunnelled CVCs, dialysis lines, peripherally inserted central catheter lines, peripheral venous catheters and fistulas; (b) indwelling medical devices other than VADs, such as chest drains, surgical drains, tracheostomy, epidural anaesthetic devices, spinal anaesthetic devices, nephrostomy, urethral catheter, suprapubic catheter, self catheterization, and percutaneous endoscopic gastrostomy tubes, inserted in the 30 days prior to the date when the positive blood culture was taken (applies to a and b).
b Includes but not exclusively: infections of skin (pressure sores, trauma, ulcers, cuts, grazes, surgical incisions, burns and eczema), subcutaneous tissue, fascia and muscle (does not include deep-seated/metastatic soft tissue infection) that were present when the positive blood culture was taken.
c Includes, but not exclusively: medical/surgical instrumentation, intramuscular, intravenous, subcutaneous, intra-articular medication, venepuncture, immunosuppression, diabetes mellitus, previous hospital admission or non-healthcare, cosmetic procedure breaking skin or mucous membranes in the 30 days prior to the positive blood culture being taken.
The introduction of enhanced SAB surveillance in 2014 has allowed the identification of sources of infection and the associated risk factors. Data analysis showed that the point of entry for SAB differed depending on the origin of the bacteraemia. This study found that 70.1% of SAB episodes were linked to health care (HAIs + HCAIs). The majority of these are preventable, and further work is required at clinical level to reduce this figure.
As reported in a number of other studies, VADs and other medical devices are a major source of entry point for SAB [
]. The programme has identified PVCs, dialysis lines and CVCs as major contributors to SAB in Scotland. Improved management of patients in hospital with VADs remains an important quality indicator. Reductions in VAD-related SAB can be achieved with insertion and maintenance care bundles [
Reducing Staphylococcus aureus bloodstream infections associated with peripheral intravenous cannulae: successful implementation of a care bundle at a large Australian health service.
]. However, for PVCs, there is debate regarding the length of time that a PVC should remain in situ before being replaced, and the risk for SAB if the dwell time exceeds 72 h [
]. Although the importance of bundles has been highlighted in these studies, bundles do not target specific patient populations where intrinsic risk for SAB may be present. One of the aims of the enhanced surveillance was to support these investigations at health board level, and identify those specific populations of patients to enable targeted work and further improvements.
SSTIs were identified either as the entry point or a risk factor in both healthcare and community cases (47.2% and 49.5%, respectively). This brings the focus to joint work of improvement teams and the need to concentrate on patient follow-up in the community. Tissue viability teams may play a leading role, and intelligence from enhanced surveillance is an essential start to facilitate this work.
Further detailed analysis is required in community-onset SAB cases with unknown origin as 50% of cases had no recorded risk factors. Risk factors in this protocol may need to be extended, and new categories may need to be added to enable identification of specific problems in the community. As 30% of SAB cases in Scotland are acquired in the community, the improvement workforce needs to include community teams and facilitate joint work to initiate targeted actions.
Septic episodes, including SABs, in injection drug users have been described in the literature [
]. The data from the present study show that approximately 10% of all SAB cases in Scotland were related to drug misuse. This is a large group of patients in whom reduction of infections may be most challenging; further support for the work of harm reduction teams is essential.
Recording contaminants as HAIs can focus improvements in blood culture aspiration technique. Review of blood culture sampling practice and education for acute areas is essential to reduce the number of contaminated samples. This contamination can be interpreted as infection, resulting in patients receiving additional treatment and extended stay, and over reporting of actual infection rates.
A limitation of this study was that entry point was originally collected as a generic source field, which contained both entry point and sources of deep-seated/metastatic infection. The source field was subsequently mapped to an entry point field to match the updated definitions [
], and this resulted in an increased number of undefined entries where entry point could not be determined. Enhanced surveillance programmes using blood culture isolates need to ensure that they identify the entry point which gave rise to the infection from complications that arise from metastatic or direct spread.
The national SAB surveillance in Scotland is being developed to allow hospital and speciality level analysis that will support NHS boards to evaluate the effect of local intervention strategies.
VADs continue to be a major contributing factor in the acquisition of SAB, and healthcare professionals should continue to use insertion and maintenance care bundles to optimize practice and reduce the risk of infection. Skin integrity assessments and symptom management of people with chronic skin conditions may reduce the risk of SAB in all adult age groups.
One-third of all SAB cases were identified as true community-acquired infections, and more interventions are required for populations identified as being at risk. Increased awareness of the risks associated with SSTIs should be encouraged through public health messages directed at health and social care staff and the general public.
Acknowledgements
The authors wish to thank the Enhanced Staphylococcus aureus Bacteraemia Short Life Working Group for the development of national definitions, protocols and implementation. In addition, the authors wish to thank local surveillance teams for supplying the data used in this analysis.
Reducing Staphylococcus aureus bloodstream infections associated with peripheral intravenous cannulae: successful implementation of a care bundle at a large Australian health service.
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