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Original article

Impact of rapid diagnostic tests on the management of patients presenting

with Enterobacteriaceae bacteremia
Évaluation de l’apport des tests rapides sur la prise en charge des bactériémies à entérobactéries
E. Farfour a,∗ , A.G. Si Larbi b , E. Cardot a , L. Limousin a ,
D. Mathonnet a , P. Cahen a , M. Vasse a , P. Lesprit a
a Service de biologie clinique, hôpital Foch, 40, rue Worth, 92150 Suresnes, France
b Service de réanimation, hôpital Foch, 40, rue Worth, 92150 Suresnes, France

Received 1st November 2017; accepted 29 November 2018

Abstract
Objective. – Pathogens are usually identified from blood cultures using a two-step procedure: Gram staining on the day of bacterial growth (D0),
followed by identification and susceptibility testing the following day (D1). We aimed to evaluate the use of rapid tests performed on D0 in patients
presenting with Enterobacteriaceae bacteremia.
Patients and methods. – Patients with ≥ 1 positive monomicrobial blood culture with Gram staining suggestive of an Enterobacteriaceae were
prospectively included. Two successive strategies were evaluated: i) conventional strategy (CS), ii) combination of a rapid identification test and
third-generation cephalosporin susceptibility testing (rapid strategy, e.g. RS).
Results. – Eighty-three patients were included (CS = 42; RS = 41). Compared with CS, the median delay of identification was significantly shorter
with RS (22 hours [20–27] vs. 47 hours [42–53]; P < 0.001). Patients in the RS group more frequently received an effective (82.9% vs. 73.8%,
P = 0.43) and appropriate (70.7% vs. 54.7%, P = 0.17) antibiotic therapy on D1. Moreover, all five RS patients infected with a non-susceptible
strain received an effective therapy on D1 versus only three of eight CS patients.
Conclusions. – Use of rapid testing was associated with a reduced time to result availability. This strategy should be useful to initiate an early
effective and appropriate therapy and to improve the care of patients.
© 2018 Elsevier Masson SAS. All rights reserved.

Keywords: Blood culture; Enterobacteriaceae; Bacteremia; Cephalosporins; Antibacterial agents

Résumé
Objectifs. – Le rendu des hémocultures positives est habituellement réalisé en 2 temps : examen direct le jour de la positivité du flacon (j0),
identification et antibiogramme le lendemain (j1). L’objectif de ce travail était d’évaluer l’apport des tests rapides réalisés à J0 sur les hémocultures
positives à entérobactéries.
Matériel et méthodes. – Les patients ayant au moins un flacon d’hémoculture positif monomicrobien à entérobactérie à l’examen direct ont été
prospectivement inclus. Deux stratégies successives ont été comparées : i) stratégie habituelle : groupe témoin (GT); ii) stratégie associant une
identification rapide et une évaluation de la sensibilité aux céphalosporines de troisième génération (C3G) : groupe test rapide (GR).
Résultats. – Quatre-vingt-trois patients ont été inclus (GT = 42; GR = 41). Comparé au GT, le délai médian d’identification était plus court dans
le GR (22 heures [20–27] vs 47 heures [42–53]; p < 0,001) avec une tendance à une antibiothérapie plus efficace (82,9 % vs 73,8 %, p = 0,43) et
plus appropriée (70,7 % vs 54,7 %, p = 0,17) à j1. Les cinq patients du GR infectés par une souche résistante aux C3G ont reçu une antibiothérapie
efficace à j1 contre seulement trois des huit patients du GT.

∗ Corresponding author.
E-mail addresses: e.farfour@hopital-foch.org, ericf6598@yahoo.fr (E. Farfour).

https://doi.org/10.1016/j.medmal.2018.11.015
0399-077X/© 2018 Elsevier Masson SAS. All rights reserved.

Please cite this article in press as: Farfour E, et al. Impact of rapid diagnostic tests on the management of patients presenting with Enterobac-
teriaceae bacteremia. Med Mal Infect (2018), https://doi.org/10.1016/j.medmal.2018.11.015
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Conclusions. – L’utilisation des tests rapides a permis de réduire les délais de rendu des résultats. Cette stratégie devrait favoriser une
antibiothérapie rapidement efficace et appropriée et améliorer la prise en charge des patients.
© 2018 Elsevier Masson SAS. Tous droits réservés.
Mots clés : Hémoculture ; Entérobactérie ; Bactériémie ; Céphalosporines ; Agents antibactériens
1. Introduction
Time to bacteremia management has a direct impact on the
survival of patients [1–4]. Results (identification and antimicro-
bial susceptibility tests) are usually obtained after a two-stage
process:
• direct examination on the day of bacterial growth detection
(day 0);
• identification and antimicrobial susceptibility testing the fol-
lowing day (day 1).
Technological advances contributed to reducing the time to
result availability: compared with the usual phenotypic method,
the MALDI-TOF technique (Matrix-Assisted Laser Desorption
Ionization–Time Of Flight) reduces the time to identification
of microorganism colonies on agar media by approximately
20 hours [1]. The MALDI-TOF test is performed on day 1 from
subcultures of blood culture broths, and helps reduce the time
to prescription of an effective and adapted antibiotic therapy.
The case fatality is thus reduced (odds ratio = 0.55; P = 0.075).
To reduce this time frame by an additional 18–24 hours, the
MALDI-TOF technique has been adapted for the direct iden-
tification of micro-organisms in blood culture broths [5]. This
method allows for microorganism identification in less than one
hour, but requires several manipulations to isolate the bacteria
from the blood culture broth. Zabbe et al. more recently sug-
gested performing a three- to four-hour subculture on cooked
blood agar incubated at 35◦◦ C in aerobic conditions, from a
drop of blood culture broth. Identification with MALDI-TOF is
performed by collecting the initial bacterial culture phase on the
agar medium [6,7]. This easier-to-use and less expensive method
is associated with similar performances.
Molecular biology methods have also been developed. These
methods rely on specific PCR tests of groups of pathogens such
as multiplex PCR tests developed to identify Staphylococcus
aureus and resistance to methicillin [8,9], or PCR tests target-
ing more pathogens and enabling the identification of groups,
genera, or bacterial species as well as resistance genes [10,11].
None of these methods are designed to assess the susceptibility
to third-generation cephalosporins (3GC) because of the great
diversity of resistance mechanisms and their genetic origin.
However, rapid colorimetric assays are available and are able
to detect all types (extended-spectrum beta-lactamase [ESBL]
or hyperexpressed cephalosporinase) of enzyme resistance to
3GCs. Just like the MALDI-TOF technique, they can also
be performed directly from the blood culture broth following
several steps of manipulations to isolate the bacteria from the
Please cite this article in press as: Farfour E, et al. Impact of rapid diagnostic tests on the management of patients presenting with Enterobac-
teriaceae bacteremia. Med Mal Infect (2018), https://doi.org/10.1016/j.medmal.2018.11.015
broth. Several authors suggested performing this test on bacte-
rial subcultures of less than four hours to simplify the process
[6,12].
These techniques are associated with a rapid time to result
availability because of the associated rapid time to execution
without any subculture prolonged for 18–24 hours [13,14]. They
may thus contribute to a better management of patients and
improve the prognosis of bacteremia.
We aimed to assess a strategy combining two rapid tests
performed on blood cultures positive for Gram-negative bacilli
such as Enterobacteriaceae for identification and 3GC suscep-
tibility purposes. We thus compared the impact of this strategy
with that of the usual identification strategy and conventional
antimicrobial susceptibility testing.
2. Material and methods
2.1. Study design
We performed a prospective study from May 1 to October
30, 2016. All patients aged above 18 years who had been hospi-
talized on the day of bacterial growth detection in blood culture
(day 0) were included in the study. For the emergency depart-
ment, only hospitalized patients were included in the study. Only
monomicrobial episodes were included.
2.2. Assessed strategies
Two strategies were successively assessed over two periods
and in two groups of patients:
• an observational period (“control period”), during which we
used the usual strategy of the microbiology laboratory without
any rapid test: on day 0 the direct examination was performed
and interpreted, and results were transmitted as soon as bacte-
rial growth was detected in blood cultures. The medium was
then inoculated for antimicrobial susceptibility test, followed
by inoculation on a Columbia blood agar. On the follow-
ing day (day 1) the antimicrobial susceptibility test results
were interpreted and identification was performed with the
MALDI-TOF technique using the 18–24-hour subculture;
• an interventional period (“rapid period”), during which the
direct examination was performed on day 0 and which
results were transmitted to the prescriber, followed by rapid
identification of the microorganism by multiplex PCR (Fil-
®
mArray BCID , BioMérieux) or MALDI-TOF (Microflex
®
LT , Bruker Daltonic) and an anti-microbial susceptibility
®
test to 3GCs (␤-lacta , Bio-Rad). Results of these tests were
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then transmitted to the prescriber within four hours following
bacterial growth detection in blood culture. Similarly to the
observational period, an antimicrobial susceptibility test and
an identification test were then performed on day 1;
• the FilmArray BCID assay was directly performed on blood
cultures according to the manufacturer’s recommendations.
®
For the MALDI-TOF and ␤-lacta tests, a subculture on
Columbia agar medium with 5% sheep blood was incubated
at 35◦◦ C + −2◦◦ C for four hours in aerobic conditions. Both
tests were performed after collecting the initial culture phase
as per the manufacturer’s recommendations.
2.3. Data collection
The following data was collected:
• demographic data: identity, age, sex, hospitalization ward of
patients;
• microbiological data: results of rapid and final tests and
respective hours;
• clinical data: portal of entry of the bacteremia, infection sever-
ity, Charlson and McCabe scores;
• treatment data: date and hour of antibiotic therapy initiation,
adaptation or lack of adaptation following bacterial growth
detection in blood cultures and rapid and final test result
availability, infectious disease specialist’s advice.
2.4. Assessing the impact of each strategy
We assessed the time to identification of the microorganism
responsible for bacteremia from the blood culture collection.
The antibiotic therapy prescribed on day 1, eg. following trans-
mission of the direct examination results and rapid test results
to the prescriber, was retrospectively assessed based on the final
antimicrobial susceptibility test results. The antibiotic therapy
was considered effective if at least one of the antibiotics pre-
scribed was active against the isolated bacterium in vitro. The
antibiotic therapy was considered appropriate if effective with
an adequate spectrum of activity considering the isolated bac-
terium, and if it complied with the facility’s guidelines. This
evaluation was performed by an infectious disease specialist and
a microbiologist.
2.5. Statistical analyses
Quantitative variables were expressed as median and
interquartile range, and compared using the Mann-Whitney test
(SPSS software). Qualitative variables expressed as percentages
were compared using Fisher’s exact test.
3. Results
A total of 83 patients were included: 42 during the “con-
trol period” and 41 during the “rapid period”. No significant
difference was observed between both groups in terms of
demography and clinical presentation (Table 1). Overall, 25%
Please cite this article in press as: Farfour E, et al. Impact of rapid diagnostic tests on the management of patients presenting with Enterobac-
teriaceae bacteremia. Med Mal Infect (2018), https://doi.org/10.1016/j.medmal.2018.11.015
3
of patients presented with severe sepsis or septic shock and
16% of them were hospitalized in the intensive care unit. Bac-
teremia episodes were healthcare-associated in 40% of cases
and nosocomial in 24% of cases. The main portal of entries
were the urinary tract (54%) and the digestive tract (25%). A
total of 13 patients (15.6%) were infected with a strain resis-
tant to 3GCs: nine strains were ESBL-producing, three were
high-level cephalosporinase-producing, and one was OXA-48
carbapenemase-producing. All Enterobacteriaceae strains were
correctly identified by both rapid tests (MALDI-TOF, n = 23;
FilmArray, n = 18) following correlation with the reference iden-
®
tification. The ␤-lacta test was correlated with the antimicrobial
susceptibility test in all but one cases: a Klebsiella oxytoca strain
®
generated a positive ␤-lacta test result while the strain was sus-
ceptible to 3GCs. This result was not transmitted to the physician
because of the high frequency of false positive results with this
bacterial species [15].
The use of rapid tests led to significantly reducing
the time to identification of Enterobacteriaceae: median of
47 hours (42–53 hours) for the control period versus 22 hours
(20–27 hours) for the rapid period (P < 0.001) (Table 2). On day 1
the antibiotic therapy was overall more effective and more appro-
priate in the rapid test group. Among the 13 patients infected with
a 3GC-resistant strain, the five patients of the rapid test group
all received an effective antibiotic therapy on day 1 versus only
three of the eight control patients. In-hospital case fatality and
length of stay were also lower in the rapid test group, although
non significantly. No difference was observed in terms of impact
between both rapid identification tests.
4. Discussion
The use of rapid tests on four-hour subcultures led to signifi-
cantly reducing the time to identification of Enterobacteriaceae,
thus confirming the benefit of these techniques [8–10,13,14].
Our study only focused on Enterobacteriaceae. Enterobacteri-
aceae are responsible for a third of bacteremia cases diagnosed
in hospital settings [16] and the proportion of 3GC-resistant
strains is increasing (13.1% and 30.3% of Escherichia coli and
Klebsiella pneumoniae strains in 2015, respectively) [17]. How-
ever, no test is currently available to concomitantly identify
the microorganism and to assess the 3GC susceptibility. To
our knowledge, this strategy has not been extensively studied
[6].
No difference was observed between the performance of
the MALDI-TOF and FilmArray tests, which are both easy
to perform. However, the MALDI-TOF test has the advantage
of having a more comprehensive database and of being less
expensive (less than 5 Euros per test for MALDI-TOF versus
approximately 200 Euros for FilmArray). Besides, many labo-
ratories are now using mass spectrometers. FilmArray can only
be used in very specific situations (bacteremia, respiratory tract
infections or meningitis, etc.), and thus requires specific labo-
ratory equipment. However, it can be used with polymicrobial
blood cultures while MALDI-TOF cannot [10].
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Table 1
Demographic and clinical characteristics of patients.
Caractéristiques démographiques et cliniques des patients.
Control period Rapid period P
(n = 42) (n = 41)

Age, median 70 (61–81) 74 (63–82) 0.57

Male sex (%) 26 (61.9%) 17 (41.5%) 0.08
McCabe Score 0.29
0 20 (47.6%) 16 (39.0%)
1 18 (42.9%) 16 (39.0%)
2 4 (9.5%) 9 (22%)
Charlson Score, median 2 (1–3) 2 (1–6) 0.36
Ward 0.28
Medicine 22 (52.4%) 22 (53.7%)
Surgery 11 (26.2%) 15 (36.6%)
Intensive care unit 9 (21.4%) 4 (9.7%)
3GC-resistant Enterobacteriaceae 8 (19.0%) 5 (12.2%) 0.54
Bacterial species
E. coli 25 (59.5%) 29 (70.6%)
K. pneumoniae 7 (16.6%) 4 (9.7%)
Proteus mirabilis 2 (4.8%) 2 (4.9%)
Enterobacter cloacae 2 (4.8%) 2 (4.9%)
Other Enterobacteriaceae 4 (9.5%) 0
Enterobacter aerogenes 0 2 (4.9%)
≥ 2 species of Enterobacteriaceae 2 (4.8%) 0
Origin of the infection 0.64
Community-acquired 13 (30.9%) 17 (41.5%)
Healthcare-associated 18 (42.9%) 15 (36.6%)
Nosocomial 11 (26.2%) 9 (21.9%)
Severity 0.51
Sepsis 29 (69.0%) 33 (80.6%)
Severe sepsis 7 (16.7%) 4 (9.7%)
Septic shock 6 (14.3%) 4 (9.7%)
Portal of entry 1
Urinary tract 22 (52.4%) 23 (56.1%)
Digestive tract 11 (26.2%) 10 (24.5%)
Primary 6 (14.2%) 4 (9.7%)
Genitals 2 (4.8%) 0
Catheter 1 (2.4%) 3 (7.3%)
Cutaneous 0 1 (2.4%)
Infectious disease specialist’s advice 25 (59.5%) 29 (70.7%) 0.36

Table 2
Impact of rapid tests on patient’s management.
Impact des tests rapides sur la prise en charge des patients.
Control period Rapid period P
(n = 42) (n = 41)

Time to identification, median (hours) 47 (42–53) 22 (20–27) < 0.001

Effective antibiotic therapy on day 1 31 (73.8%) 34 (82.9%) 0.43
Appropriate antibiotic therapy on day 1 23 (54.7%) 29 (70.7%) 0.17
Duration of antibiotic therapy, median (days) 12 (10–19) 10 (10–14.5) 0.57
Case fatality 4 (9.5%) 2 (4.9%) 0.67
Length of hospital stay, median (days) 10 (6–16) 7 (5–12) 0.27

Reducing the time required for evaluating 3GC susceptibility
among Enterobacteriaceae is particularly interesting at a time
of antibiotic resistance and when last resort antibiotics such as
®
carbapenems should be spared. The ␤-lacta test has excellent
performance for E. coli and K. pneumoniae (> 96% susceptibility
and 100% specificity), but its susceptibility for group 3 Enter-
obacteriaceae is lower (67%) [15]. Resistance to 3GCs through
hyperexpression of chromosomal cephalosporinase may trigger
a false negative result [15]. In that case, the rapid identifica-
®
tion associated with a negative ␤-lacta test allows the use of
cefepime and avoids the excessive use of carbapenems. K. oxy-
toca strains with hyperexpression of chromosomal penicillinase,
although susceptible to 3GCs, may trigger a false positive result,
as observed in one patient.
The use of this strategy should positively impact the quality of
the antibiotic therapy and thus improve patient’s management.

Please cite this article in press as: Farfour E, et al. Impact of rapid diagnostic tests on the management of patients presenting with Enterobac-
teriaceae bacteremia. Med Mal Infect (2018), https://doi.org/10.1016/j.medmal.2018.11.015
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In our study, patients who benefited from this strategy had
a more effective and appropriate treatment on day 1; were
associated with a lower in-hospital case fatality and a lower
length of hospital stay compared with those benefiting from
the conventional identification method. These findings were
not significant, probably because of our sample size and
of the small proportion of 3GC-resistant Enterobacteriaceae
(15%), although already quite substantial. Several studies
reported the clinical impact of rapid tests, and mainly the early
adaptation of the antibiotic therapy [14,18–20]. For Gram-
negative bacilli, this adaptation was more frequent on day
1 for group 3 Enterobacteriaceae (59.3%) than for other
Enterobacteriaceae (35.1%) [18]. The time to de-escalation
was also reduced by at least 24 hours [21]. The impact
of rapid identification by MALDI-TOF test on the hospital
length of stay has also been demonstrated with a significant
reduction in the median length of stay from 14 to 9.5 days
[22].
Rapid tests may be optimized when combined with the sys-
tematic advice of an infectious disease specialist [23,24]. A
meta-analysis assessing the impact of rapid tests (PCR) reported
a significantly lower case fatality when the test was associated
with the infectious disease specialist’s advice (OR = 0.64; 95%
CI: 0.51–0.79). Results were not significant in the absence of
the infectious disease specialist’s advice when the molecular
test was used on its own [23]. The infectious disease special-
ist’s advice was not systematically sought in our study (65% of
episodes). Rapid tests should lead to a more rapid identification
of patients infected with a resistant strain and should contribute
to giving priority to the infectious disease specialist’s advice for
these patients.
Finally, new rapid tests are associated with additional costs
for health facilities. However, two American economic stud-
ies have demonstrated that the use of the FilmArray assay
led to reducing the cost associated with the patient’s manage-
ment by approximately 3000 $ per patient [14,20]. Economic
evaluations should be performed in Europe to confirm these
analyses.
Our study confirms the benefit of rapid tests combining the
identification of Enterobacteriaceae and the evaluation of sus-
ceptibility to 3GC in case of bacteremia. Using these tests on
blood cultures collected from patients presenting with a risk of
infection with a 3GC-resistant strain should confirm the added
value of this strategy.
Contribution of authors
E. Farfour and P. Lesprit wrote the study protocol, contributed
to inclusions, and wrote the article. A.G. Si Larbi performed
the statistical analysis and reviewed the article. E. Cardot, L.
Limousin, D. Mathonnet, P. Cahen, and M. Vasse contributed to
including patients and reviewed the article.
Disclosure of interest
The authors declare that they have no competing interest.
Please cite this article in press as: Farfour E, et al. Impact of rapid diagnostic tests on the management of patients presenting with Enterobac-
teriaceae bacteremia. Med Mal Infect (2018), https://doi.org/10.1016/j.medmal.2018.11.015
5
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Please cite this article in press as: Farfour E, et al. Impact of rapid diagnostic tests on the management of patients presenting with Enterobac-
teriaceae bacteremia. Med Mal Infect (2018), https://doi.org/10.1016/j.medmal.2018.11.015