International Journal of Infectious Diseases 104 (2021) 45–49

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International Journal of Infectious Diseases

journal homepage: www.elsevier.com/locate/ijid

Staphylococcus aureus bloodstream infection: Secular changes

associated with the implementation of a de novo clinical infectious
diseases service in a Canadian population
Kevin B. Lauplanda,b,c,* , Lisa Steeled, Kelsey Pasquilld, Elizabeth C. Parfittc
a
Faculty of Health, Queensland University of Technology (QUT), Brisbane, Queensland, Australia
b
Department of Intensive Care Services, Royal Brisbane and Women’s Hospital, Brisbane, Queensland, Australia
c
Department of Medicine, Royal Inland Hospital, Kamloops, British Columbia, Canada
d
Department of Pathology and Laboratory Medicine, Royal Inland Hospital, Kamloops, British Columbia, Canada

A R T I C L E I N F O A B S T R A C T

Objective: To investigate the epidemiology of Staphylococcus aureus bloodstream infections (BSI) in a

Keywords: mixed rural to small city population and examine secular changes associated with the implementation of
Bloodstream infections
a regional clinical infectious diseases program.
BSI
Methods: Population-based surveillance for incident S. aureus BSI was conducted in the western interior
Staphylococcus aureus
of British Columbia, Canada between April 2010 and March 2020. An infectious diseases service was
progressively implemented starting in 2013.
Results: 581 incident S. aureus BSI were identified. There was an increasing incidence during the study and
the overall age- and gender-adjusted annual rate was 32.9 per 100,000 population. Implementation of
the infectious diseases program was associated with an increase in rates of blood culture sampling,
documentation of persistent bacteremia, use of transthoracic and transesophageal echocardiography,
and a reduction in cases of relapsed BSI. Infectious diseases consultation was independently associated
with a reduced risk for death (odds ratio 0.5; 95% CI 0.3–0.9).
Conclusions: Although the implementation of a clinical infectious diseases service was associated with
changes in management and improved outcome, S. aureus BSI still causes a major burden of illness.
© 2020 The Author(s). Published by Elsevier Ltd on behalf of International Society for Infectious Diseases.
This is an open access article under the CC BY-NC-ND license (http://creativecommons.org/licenses/by-nc-
nd/4.0/).

Introduction repeat blood cultures, and detailed clinical decision-making

Population-based studies conducted in many jurisdictions
globally have identified Staphylococcus aureus as the second most
common cause of bloodstream infection (BSI) occurring with an
annual incidence of approximately 30–40 per 100,000 population
and an associated case-fatality rate of 20% (El Atrouni et al., 2009;
Huggan et al., 2010; Lam et al., 2019; Laupland et al., 2013; Laupland
et al., 2008; Opintan and Newman, 2017). Due in part to a propensity
for complications related to metastatic foci, anti-microbial resis-
tance, and risk for relapse, S. aureus BSI is associated with high
morbidity and mortality (Choi et al., 2020). To reduce this burden,
guidelines and algorithms that involve use of echocardiography,
* Corresponding author at: Intensive Care Services, Level 3 Ned Hanlon Building,
Royal Brisbane and Women’s Hospital, Butterfield Street, Herston, Queensland,
4029 Australia.
E-mail address: Kevin.laupland@qut.edu.au (K.B. Laupland).
including antimicrobial source and route and duration of adminis-
tration have been developed (Chong et al., 2013; Holland et al., 2018;
Liu et al., 2011). This complexity in management has led to S. aureus
BSI being a common indication to request infectious diseases
consultation, which a growing body of literature indicates is
associated with improved outcome (Kawasuji et al., 2020; Sherbuk
et al., 2019; Suzuki et al., 2020; Vogel et al., 2016).
Clinical infectious diseases expertise and consultative services
are widely available in major academic centres worldwide.
However, access to infectious diseases specialist consultation is
less available in many smaller communities and non-academic
institutions including those not primarily affiliated with, or staffed
by, a medical school. We recently described our experience in
developing and implementing a novel comprehensive clinical
infectious diseases consultation service in a traditionally non-
academic tertiary care centre in a small city and surrounding
region in Canada (Parfitt et al., 2020). The objective of this study
was to examine the population-based epidemiology and outcome

https://doi.org/10.1016/j.ijid.2020.12.064
1201-9712/© 2020 The Author(s). Published by Elsevier Ltd on behalf of International Society for Infectious Diseases. This is an open access article under the CC BY-NC-ND
license (http://creativecommons.org/licenses/by-nc-nd/4.0/).
K.B. Laupland, L. Steele, K. Pasquill et al.
of S. aureus BSI in our region and examine secular changes
associated with the implementation of a novel clinical infectious
diseases service.
Methods
Surveillance population
Population-based surveillance for all S. aureus BSI occurring
among individuals residing in the western interior of British
Columbia, Canada was conducted between April 1, 2010 and March
31, 2020 (Laupland et al., 2019a). The western interior region (total
population in 2019  191,000) encompasses the city of Kamloops
(population in 2019  123,000) and a large and geographically
diverse area inclusive of 6 local health areas (Cariboo–Chilcotin,
100 Mile House, Lillooet, South Cariboo, Merritt, and North
Thompson) within the southern interior of the province of British
Columbia. Within this region, tertiary care is provided at the Royal
Inland Hospital in Kamloops with care also provided in 5 smaller
hospitals in the region. The Interior Health Research Ethics Board
granted a waiver of individual informed consent (201314052-I).
Study protocol
S. aureus BSI cases were initially identified by the regional
laboratory based in Kamloops. Once positive blood cultures were
identified, a case-by-case review of the electronic medical charts
was conducted by one investigator (a senior infectious diseases
consultant) to further classify cases as incident episodes, apply
definitions, and obtain clinical details.
Residency status was established based on town/postal code of
primary residence and non-residents of the surveillance area were
excluded. For the purposes of this study methicillin-sensitive
(MSSA) and methicillin-resistant (MRSA) strains were deemed to
be separate. The first isolate of S. aureus per episode of disease was
deemed to be the incident isolate and all positive cultures within
the following 30-days were considered as part of that episode even
if there was a period of culture negativity within that time frame.
The total number of isolations, as well as the time (in days) from
index positive culture draw to last positive isolate from that
episode, were recorded.
A most likely diagnosis/source of infection related to the S.
aureus BSI was assigned based on an overall assessment of all
available microbiology, clinical, laboratory, and diagnostic imaging
information. Comorbidities were recorded as per Charlson et al
(Charlson et al., 1987), and episodes were classified as community-
associated, healthcare-associated, and hospital-onset as per Fried-
man et al (Friedman et al., 2002). Death at 30-days post index
infection was determined using provincial vital statistics informa-
tion (Laupland et al., 2019b). Echocardiography was recorded as
not done, transthoracic only, or transesophageal  transthoracic
related to the BSI episode. An infectious diseases consult was
evidenced by a full consultation note although in some cases this
was deemed to be present where clear written evidence of an
assessment and recommended plan as established with a specific
named infectious diseases consultant was included in the
electronic chart. Management at the tertiary centre was docu-
mented by some or all of the admission to hospital at the Royal
Inland Hospital in Kamloops. Length of stay in hospital was
calculated as an inclusive sum of all hospital admissions (including
interhospital transfer) associated with the BSI episode.
Analysis
All data were analysed using Stata 16.0 (StataCorp, College
Station, USA). Prior to analysis, all continuous data were examined
46
International Journal of Infectious Diseases 104 (2021) 45–49
using histograms to assess their underlying distribution. Medians
with interquartile ranges (IQR) were used to describe skewed
variables and groups were compared using the k-medians
(Wilcoxon–Mann–Whitney) test. Categorical variables were com-
pared using Fisher’s exact test.
Incidence data were expressed as annual rates per 100,000
population using regional population data. Direct age- and sex-
standardized of incidence rates against the 2019 western interior
population was performed using 5-year age strata through to age
89 years and then 90 years and older. This was calculated for the
Kamloops area specifically whereas the data for the other local
health areas were pooled.
A logistic regression model was developed to investigate factors
associated with 30-day all-cause case-fatality. We a priori selected
variables of infectious diseases consultation: age, gender, Charlson
comorbidity index, infection onset category, diagnostic group,
residency in Kamloops versus other area, MSSA vs MRSA,
admission to tertiary care, and echocardiography in the initial
model. Stepwise variable elimination and grouping of categorical
variables was then performed to develop the most parsimonious
model. After the putative model was developed we re-inserted
eliminated variables one-by-one to test for effect in the final
model. The final model discrimination and calibration were
assessed using the area under the receiver operator characteristic
and Hosmer-Lemeshow test, respectively. In all statistical testing
we deemed a P-value of <0.05 to represent significance.
Results
Population incidence
During the decade of surveillance, 581 incident S. aureus BSI
were identified among 540 individuals for an overall crude annual
incidence of 31.9 per 100,000. Of these, 460 (79.2%) and 121 (20.8%)
were MSSA and MRSA, respectively. While both MSSA and MRSA
BSI were most commonly healthcare-associated (227; 49.4% and
66; 54.6%. respectively), MSSA were more likely to be community-
associated (161; 35% vs 22; 18.2%; P < 0.001) and less likely to be of
hospital-onset (72; 15.7% vs. 33; 27.3%; P = 0.005) as compared to
MRSA BSI.
Two-thirds of S. aureus BSI episodes were in males (363/581;
62.5%) and the median age was 64.7 (IQR, 53.3–76.6). The overall
age- and gender-adjusted annual incidence rate was 32.9 per
100,000 population and was 34.0 and 30.9 per 100,000 among
residents of Kamloops and the other areas, respectively. There was
an annual increase in the incidence of S. aureus BSI during the study
Figure 1. Blood culture sampling rate and incidence of Staphylococcus aureus
bloodstream infection during a decade of surveillance in the western interior of
British Columbia, Canada (culture rate refers to all blood cultures performed in the
study region).
K.B. Laupland, L. Steele, K. Pasquill et al. International Journal of Infectious Diseases 104 (2021) 45–49

that was associated with an increased population culturing rate as
shown in Figure 1.
Clinical determinants and secular changes
Demographic and clinical determinants across the 3 eras of
infectious diseases program pre-implementation (2010–2012),
development (2013–2016), and full service (2017–2019) are
displayed in Table 1. Age, sex, hospital admission details, and
the proportion of MRSA versus MSSA infections did not vary among
the 3 eras (Table 1). Ninety-five per cent of patients (554/581) were
admitted for management and this did not vary among the 3 eras
(P = 0.6). However, later eras were associated with increased
echocardiography performance, demonstration of persistent
positive blood cultures, and diagnosis of fewer non-focal infections
(Table 1).
The overall median follow-up time was 429 (IQR 43–1141) days.
Thirty-eight (6.5%) patients had a second episode, 2 a third (<1%),
and 1 patient a fourth episode of S. aureus BSI. The median time
between subsequent episodes was 132 (IQR, 50.8–393.8) days.
Recurrence within 1 year was less likely in the later eras as shown
in Table 1.
As compared to other areas of the western interior, residents of
the Kamloops area were more likely to have an MRSA BSI (90/366;
24.6% vs. 31/215; 14.4; P = 0.004) and to have an infectious diseases
consultation (211/366; 57.7% vs. 91/215; 42.3%; P < 0.001).
However, no difference was observed for age, gender, Charlson
comorbidity index, onset of infection, diagnosis, or case-fatality
among Kamloops and other area residents.
Infectious diseases consultation
Overall 302/581 (52.0%) of episodes had a documented
infectious diseases consultation. Patients who received infectious
diseases consultation were twice as likely to have an echocardio-
gram (281/302; 93.0% vs. 133/279; 47.7%; P < 0.0001), and 3 times
more likely (69/302; 22.8% vs. 20/279; 7.2%; P < 0.0001) a
transesophageal echocardiogram, than patients who did not have
an infectious diseases consultation. Those managed with infec-
tious diseases consultation were more than twice as likely (128/
302; 42.4% vs 48/279; 17.2%; P < 0.0001) to have >2 positive blood
cultures.
The overall 30-day case-fatality per episode was significantly
lower in association with infectious diseases consultation (43/302;
14.2% vs. 85/279; 30.4%; P < 0.0001). A logistic regression model
limited to the 540 first episodes of S. aureus BSI had good
discrimination (area under receiver operator characteristic =
0.8180) and calibration (goodness of fit P = 0.9) and found

Table 1
Characteristics among during pre-, development and full service implementation of a clinical infectious diseases service.

Factor Pre Development (2013–2016) Full service(2017–2019)N = 223 p-value

(2010–2012)N N = 229
= 129
Median age 64.2 (53.0–74.3) 63.4 (53.3–76.2) 66.2 (53.8–78.1) 0.3
Male 75 (58.1%) 147 (64.2%) 141 (63.2%) 0.5
Recurrence within 1 year 13 (10.1%) 8 (3.5%) 6/143 (4.2%)* 0.035
Infectious diseases consultation 7 (5.4%) 129 (56.6%) 166 (74.8%) <0.001
Number positive cultures per episode 0.003
1 40 (31.0%) 57 (24.9%) 55 (24.7%)
2 73 (56.6%) 98 (42.8%) 82 (36.8%)
3 6 (4.7%) 18 (7.9%) 22 (9.9%)
4 8 (6.2%) 25 (10.9%) 30 (13.5%)
5 1 (1%) 9 (3.9%) 6 (2.7%)
6 0 6 (2.6%) 11 (4.9%)
7 0 5 (2.2%) 4 (1.8%)
>7 1 (1%) 11 (4.8%) 13 (5.8%)
Days of positive cultures 0.001
1 116 (89.9%) 161 (70.3%) 144 (54.6%)
2 6 (4.7%) 14 (6.1%) 26 (11.7%)
3 2 (1.6%) 12 (5.2%) 17 (7.6%)
4 1 (0.8%) 11 (4.8%) 11 (4.9%)
5 0 6 (2.6%) 3 (1.4%)
6 0 7 (3.1%) 3 (1.4%)
7 1 (0.8%) 3 (1.3%) 3 (1.4%)
>7 3 (2.3%) 15 (6.6%) 16 (7.2%)
Echocardiogram <0.001
Not done 60 (46.5%) 59 (25.8%) 48 (21.5%)
TTE only 54 (41.9%) 145 (63.3%) 126 (56.5%)
TEE 15 (11.6%) 25 (10.9%) 49 (22.0%)
Median Charlson comorbidity index (IQR) 1 (0–3) 2 (1–3) 2 (0–4) 0.002
Diagnosis group 0.013
No focus 37 (28.9%) 59 25.8%) 41 (18.4%)
Bone/joint 29 (22.7%) 60 (26.2%) 61 (27.4%)
Soft tissue 17 (13.3%) 31 (13.5%) 18 (8.1%)
Respiratory 20 (15.6%) 22 (9.6%) 38 (17.0%)
Cardiovascular 15 (11.7%) 49 (21.4%) 50 (22.4%)
Other 10 (7.8%) 8 (3.5%) 15 (6.7%)
MSSA 96 (74.4%) 183 (79.9%) 181 (81.2%) 0.3
MRSA 33 (25.6%) 46 (20.0%) 42 (18.8%)
Management or part thereof at tertiary centre 104 (80.6%) 189 (82.5%) 187 (83.9%) 0.7
Kamloops residency 86 (66.7%) 146 (63.8%) 134 (60.1%) 0.4
30-day case-fatality 24 (18.6%) 51 (22.3%) 53 (23.8%) 0.5
Median hospital length of stay (IQR) 16 (8-36) 15 (8-30)N = 217 14 (8-32)N = 215 0.7
N = 122
*
Number of cases limited to 2017/2018 study years due to limited duration of follow-up in the final study year.

47
K.B. Laupland, L. Steele, K. Pasquill et al.
Table 2
Logistic regression of factors associated with 30-day all-cause case fatality among 540 first episodes of Staphylococcus aureus bloodstream infection.
Factor Odds ratio
Infectious diseases consultation 0.52
Age (per year) 1.04
Charlson (per point) 1.24
Hospital onset 3.68
Diagnosis
Other 1 (reference)
Respiratory 3.03
Cardiovascular 2.47
Echocardiography 0.38
infectious diseases consultation associated with reduced risk for
death as shown in Table 2.
Discussion
This study demonstrates the major burden of illness associated
S. aureus BSI and the benefit of the implementation of a novel
clinical infectious diseases service in mixed rural to small city
regional population. Our observation of an annual incidence rate of
33 per 100,000 is comparable to that observed in other studies
conducted in Australia, New Zealand, Europe, and North America
(El Atrouni et al., 2009; Huggan et al., 2010; Lam et al., 2019;
Laupland et al., 2013; Laupland et al., 2008; Opintan and Newman,
2017). It is noteworthy that we observed a similar rate of 30.9 per
100,000 in the areas of the western interior other than Kamloops.
This area is vast (91,000 km2), geographically diverse, and has a
very low population density (<1 resident/ km2) with the next
largest centre represented by the city of Williams Lake (city and
surrounding population 18,000 residents). Much of the previous
population-based study on S. aureus BSI has been reported from
academic centres primarily based in urban centres. It is an
important finding that we observed similar epidemiology of
S. aureus BSI in our mixed rural to small city population.
Several studies have investigated the role of infectious diseases
consultation on the outcome associated with S. aureus BSI
(Kawasuji et al., 2020; Sherbuk et al., 2019; Suzuki et al., 2020;
Vogel et al., 2016). Vogel et al conducted a systematic review of the
literature on this topic and included 18 reports inclusive of more
than 5,000 patients (Vogel et al., 2016). Infectious diseases
consultation was found to be associated with improved antimi-
crobial therapy, increased use of echocardiography and repeat
cultures, and a 30-day case fatality reduction (relative risk 0.53;
95% CI 0.43–0.65) (Vogel et al., 2016). We considered increased use
of repeat blood cultures (or documentation of persistent bacter-
emia), fewer cases without an identified focus of infection, and use
of echocardiography to be measures of improved care associated
with S. aureus BSI. While we do not have evidence of changes in
anti-microbial therapy, our study findings provide further evi-
dence in support of the value of infectious diseases consultation in
non-academic centres.
We observed several changes associated with the development
and implementation of the infectious diseases service in our
region, including increased blood culture sampling rates, docu-
mentation of persistent bacteremia, and use of both transthoracic
and transesophageal echocardiography (Laupland et al., 2018).
Before 2013, only telephone advice or transfer to a hospital
external to the region were available for infectious diseases
consultation (Parfitt et al., 2020). Starting in 2013, direct
consultation access increased and by 2017 full service was
available. However, it is important to note that infectious diseases
consultants were based only in Kamloops such that patients in
other areas of the western interior were required to either be
transferred to Kamloops or managed by telephone support (Parfitt
48
International Journal of Infectious Diseases 104 (2021) 45–49
95% confidence interval P-value
0.30–0.90 0.019
1.03–1.06 <0.001
1.12–1.37 <0.001
2.17–6.26 <0.001
–
1.63–5.64 <0.001
1.33–4.58 0.004
0.22–0.66 0.001
et al., 2020). Importantly, residents external to Kamloops were not
at increased risk for adverse outcome in our study (excluded from
the model; Table 2), as other studies have suggested that telephone
support alone may be inadequate (Forsblom et al., 2013). Although
we do not have the empiric data to demonstrate this, our
contention is that the improvements in management that have
occurred following infectious diseases service implementation
have been the result of direct consultation and the indirect effects
of increased awareness of the importance of S. aureus BSI.
While this study benefits from population-based design and
ability to stepwise measure the effect of the implementation of a
novel infectious diseases clinical service, some limitations merit
discussion. First, this is an observational study and unmeasured
variables could be confounding our assessment of the benefit of
infectious diseases consultation. The quality and availability of
electronic records have improved during the past decade and
changes over time in some variables (i.e., Charlson comorbidities)
may be influenced in part by the inclusion of more detailed data in
later years. Second, improvements in care may be at least
attributable to general improvements in service provision during
the past decade. Major recruitment and programmatic develop-
ment have occurred with an approximate doubling of medical
speciality services. Third, we did not record therapy details such as
the type, route, and duration of antimicrobial therapy nor
interventions for source control. While we suspect that these
changed with the implementation of the infectious diseases
service we do not have the actual evidence to support this claim.
Fourth, we did not record the date and time of consultation such
that timeliness could not be evaluated as an outcome determinant.
However, it is our standard practice to receive all consults by
physician-to-physician telephone request with initial immediate
discussion of management. Provision of comprehensive bedside
clinical consultation is performed same-day during weekdays and
next-day during the after-hours. Fifth, it is possible that early
deaths occurring prior to the opportunity to have infectious
diseases consultation could have influenced results. However, a
post hoc analysis of our logistic regression model limited to
survivors to at least 2 days showed no significant changes in the
parameters. Finally, data collection was retrospective and, as a
result, we were limited to an assessment of information that was
available in the chart. While variability was minimized by
assessment by a single expert reviewer, the possibility of
incomplete data remains.
In summary, this study reports results of a decade of
surveillance for S. aureus BSI in a mixed rural to small city
population and provides evidence to support the value of the
implementation of clinical infectious diseases programs in non-
academic centres.
Funding
This research did not receive any specific grant from funding
agencies in the public, commercial, or not-for-profit sectors.
K.B. Laupland, L. Steele, K. Pasquill et al.
Conflict of Interest
The authors declare they have no conflicts of interest.
Ethical Approval
The Interior Health Research Ethics Board granted a waiver of
individual informed consent (201314052-1). This waiver was
granted to the Royal Inland Hospital, Kamloops, British Columbia,
Canada.
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