Infection (2019) 47:45–50
The DENOVA score eﬃciently identiﬁes patients withmonomicrobial
Enterococcus faecalis bacteremia whereechocardiography
AndreasBerge1,2· AndreaKrantz3· HelenaÖstlund1· PontusNauclér1,2· MagnusRasmussen3,4
Received: 13 June 2018 / Accepted: 27 August 2018 / Published online: 3 September 2018
© The Author(s) 2018
Objectives Enterococcal bacteremia can be complicated by infective endocarditis (IE) and when suspected, transesophageal
echocardiography (TEE) should be performed. The previously published NOVA score can identify patients with enterococcal
bacteremia at risk for IE and we aimed to improve the score.
Methods Factors associated with IE were studied retrospectively in a population-based cohort of patients with monomicro-
bial Enterococcus faecalis bacteremia (MEFsB). Factors associated with IE in multivariable analysis were included in a new
score system which was compared to the NOVA score and validated in a cohort of patients with MEFsB from another region.
Results Among 397 episodes of MEFsB, 44 episodes with IE were compared to those without IE. Long Duration of symp-
toms (≥ 7 days) and Embolization were associated with IE in the multivariate analysis and hence were added to the NOVA
variables (Number of positive cultures, Origin of infection unknown, Valve disease, and Auscultation of murmur) to generate
a novel score; DENOVA. The area under the curve in ROC analyses was higher for DENOVA (0.95) compared to NOVA
(0.91) (p = 0.001). With a cutoﬀ at ≥ 3 positive variables the DENOVA score has a sensitivity of 100% and speciﬁcity of
83% which is superior to the NOVA score (speciﬁcity 29%). The DENOVA score was applied to the validation cohort (26IE
episodes and 256 non-IE episodes) and the resulting sensitivity was 100% and the speciﬁcity was 85% compared to 35%
Conclusions The DENOVA score is a useful tool to identify patients with MEFsB where TEE is not needed.
Keywords Endocarditis· Enterococcus faecalis· Bacteremia· Echocardiography· Management score
Enterococci are part of the normal human gut ﬂora and can
cause severe infections including urinary tract infections,
gastrointestinal infections, catheter-related infections, and
infective endocarditis (IE). IE is deﬁned by the modiﬁed
Duke criteria  in which the identiﬁcation of a causative
bacterium and echocardiographic evidence of endocardial
infection are major criteria.
Enterococcal bacteremia is a relatively common condi-
tion and has a mortality rate of around 20% [2, 3]. A sub-
stantial proportion of patients with enterococcal bacteremia
are diagnosed with IE [2, 4–6], and recent population-based
studies suggest that up to 25% of patients with community-
acquired Enterococcus faecalis bacteremia (EFsB) have this
condition [5, 6]. A number of factors have been associated
with the presence of IE in enterococcal bacteremia including
the species E. faecalis compared to other enterococci [3, 4,
Electronic supplementary material The online version of this
article (https ://doi.org/10.1007/s1501 0-018-1208-3) contains
supplementary material, which is available to authorized users.
* Magnus Rasmussen
1 Unit ofInfectious Diseases, Department ofMedicine, Solna,
Karolinska Institutet, Stockholm, Sweden
2 Department ofInfectious Diseases, Karolinska University
Hospital, Stockholm, Sweden
3 Department ofClinical Sciences Lund, Division ofInfection
Medicine, Lund University, BMC B14, Tornavägen 10,
4 Division forInfectious Diseases, Skåne University Hospital,
46 A.Berge et al.
6, 7], prosthetic heart valves [3, 5, 7], heart murmur [2, 4],
previous endocarditis , other valve disease [2–5], emboli-
zation , monomicrobial bacteremia [2, 3, 5], a high num-
ber of positive cultures [3, 4], an unknown focus of infection
[2, 4, 5], community acquisition, subacute syndrome ,
age [2, 3], and male sex [2, 5]. It is important to detect all
cases of IE since the condition has a high mortality, and
cure necessitates a long treatment course with a combination
of antibiotics and sometimes surgery. Therefore, a scoring
system to identify which patients with enterococcal bacte-
remia that have IE has to have a sensitivity close to 100%.
Transesophageal echocardiography (TEE) is the method
of choice to diagnose IE and identiﬁes changes compatible
with IE with a higher sensitivity than transthoracic echo-
cardiography (TTE) . However, TEE is a semi-invasive,
resource-demanding procedure which is not readily available
at all sites and it is not without discomfort for the patient.
Thus, TEE should only be performed when there is a risk
of IE. For this purpose, a diagnostic score termed NOVA
[Number of positive blood cultures ≥ 3 (5 points), Origin of
infection unknown (4 points), Valve disease (2 points) and
Auscultation of heart murmur (1 point)] was developed by
Bouza etal. meant to guide the use of TEE in enterococcal
bacteremia . The authors set the cutoﬀ at 4 points, mean-
ing that TEE is recommended in patients with three or more
positive cultures (N) or unknown origin of infection (O). The
NOVA score was later validated in an adapted form and was
found to have a high sensitivity (97%) but limited speciﬁcity
(23%) . The majority of cases with enterococcal IE is due
to E. faecalis and have a monomicrobial blood culture and
in such cases IE should be considered [2, 4, 5]. We therefore
aimed to improve the NOVA score using easy accessible
clinical parameters in a population-based cohort of patients
with monomicrobial E. faecalis bacteremia (MEFsB) from
southern Sweden and to externally validate the NOVA score
and the improved score in another cohort of patients from a
tertiary referral center in another part of Sweden.
All consecutive blood cultures positive for E. faecalis from
January 2012 through December 2016 were obtained from
the database of the Laboratory for Clinical Microbiology in
Skåne County, in southern Sweden. This is the only labo-
ratory in the region and has a catchment area of 1.3mil-
lion inhabitants and nine hospitals. The medical records of
patients with MEFsB were studied retrospectively. Data col-
lection was carried out from 90days prior to an episode until
1year after the episode. Patients under the age of 18years or
where medical records could not be retrieved were excluded.
Ethical approval was obtained from the Ethics Committee of
Lund University (2013/31).
A detailed description of data collection and deﬁnitions is
given in supplementary material 1. An episode was deﬁned
as a clinical situation in which a patient had MEFsB and the
episode was ended after 7 days of eﬀective treatment. IE was
deﬁned using the modiﬁed Dukes criteria considering deﬁ-
nite cases only as IE . Scoring of patients was performed
using the information available to the clinician at the time
of the receipt of the positive blood culture results. NOVA
score parameters were deﬁned as described by Bouza etal.
 with modiﬁcations of number of cultures as described by
Dahl etal. . The origin of infection (O in NOVA, deﬁni-
tion not detailed by Bouza etal. ) was deﬁned as a focal
infection (fulﬁllment of at least two of the following criteria
(a) typical signs or symptoms of infection, (b) isolation of
E. faecalis at the site of infection, and (c) imaging results
compatible with focal infection which was likely to be the
point of entry for the bacteria. Valve disease in NOVA (V)
was deﬁned as a history of any of the predisposing heart
conditions that constitute a high or moderate risk of devel-
oping IE, including (1) native valve disease, (2) previous
IE, or (3) the presence of a valve prosthesis [8, 9]. Auscul-
tation of murmur (A in NOVA) included those with any
murmur reported. Duration of symptoms was deﬁned as the
number of days before the ﬁrst positive blood culture was
taken with any symptom compatible with IE. Embolization
was deﬁned by signs on clinical examination or by ﬁndings
using imaging techniques. A previous EFsB was deﬁned as a
blood culture with growth of E. faecalis, within the previous
90 days preceding an episode. Community and health-care
site of acquisition was deﬁned as previously described ,
whereas nosocomial acquisition was deﬁned as a blood cul-
ture drawn after 48 or more hours of hospitalization .
Comorbidities were classiﬁed according to the Charlson
The validation cohort was from Karolinska University Hos-
pital, Stockholm, Sweden, a tertiary referral center serv-
ing the Stockholm County with a population of 2.3million
inhabitants. All blood culture data for patients with growth
of enterococci were retrieved from January 2012 through
December 2016 from the Department of Clinical Microbiol-
ogy, Karolinska University Hospital. Records from patients
with MEFsB were studied retrospectively and data were col-
lected as described for the calibration cohort above. Ethical
approval was obtained from the ethics committee review
board in Stockholm (Dnr 2015/1184-31).
The DENOVA score eﬃciently identiﬁes patients withmonomicrobial Enterococcus faecalis…
For the results to be valid in the clinical setting, all episodes
of MEFsB were included in the analyses. Hence, each patient
could have more than one episode. To account for repeated
events, we applied the statistical method generalized esti-
mation equations (GEE). This method takes into account
clustering and was used both in univariate and multivariate
analyses . P values are based on GEE estimates with a
signiﬁcance level of < 0.05. For the multivariate model, we
were limited by the number of IE outcomes in the calibration
test set (n = 44). We ﬁrst performed a multivariate model that
included all variables signiﬁcantly associated with IE in uni-
variate analyses. We then removed variables from the model
that were not signiﬁcantly associated with the outcome.
653 patients with EFsB were identiﬁed, of whom 36 were
excluded since they were < 18years old, 6 due to lack of
access to medical ﬁles, and 249 because they had polymi-
crobial bacteremia. The 362 included patients had 397 epi-
sodes of MEFsB, of which 44 episodes in 44 patients (11%)
fulﬁlled the Duke criteria for IE (Supplementary material 2).
Four episodes, in which the Dukes criteria were not fulﬁlled,
were treated as possible IE by the physician.
Most patients (336) had only one episode of MEFsB.
However, 26 patients had at least one more episode of
MEFsB (in total, 35 additional episodes). The ﬁrst episode
was a non-IE in all these patients, but six of these patients
later had an episode with IE. 153 patients died within the
study period of 360 days for reasons presumed to be unre-
lated to IE based on comorbidities, clinical presentation, and
absence of positive blood culture for EFs.
Diﬀerences in distribution of variables between episodes
of IE and non-IE that could tentatively be included in a score
are given in Table1 with odds ratios and signiﬁcance lev-
els. Additional information on the treatment, investigations,
and outcome is given in Supplementary material 3. In the
univariate analysis, the number of positive blood cultures,
unknown origin of infection, valve disease, heart murmur,
a long duration of symptoms, embolization, age, commu-
nity acquisition, and previous EFsB were associated with
IE. These variables were included in a multivariate model.
Community acquisition, previous EFsB, and valve disease
were not signiﬁcantly associated with IE in the multivariate
analysis and were thus removed from the model. Further-
more, we removed age from the model since this variable
resulted in very large standard errors of other estimates indi-
cating a numerical problem.
In the ﬁnal multivariate model, symptom duration, embo-
lization, number of positive blood cultures, unknown ori-
gin of infection, and heart murmur were associated with IE
(Table2). These variables were included in a novel score,
and despite not being signiﬁcantly correlated with IE in mul-
tivariate analysis, we chose to include also the valve disease
criterion of NOVA in our new score to conform with earlier
studies [4, 5]. The novel score was termed DENOVA and
each variable was given one point to make it easy to use
The DENOVA score was tested for its ability to separate
episodes with IE from episodes without IE and the resulting
receiver operator characteristics (ROC) curve had an area
under the curve (AUC) of 0.95 (95% CI, 0.94–0.97) com-
pared to the adapted NOVA score which had a signiﬁcantly
lower AUC of 0.91 (95% CI, 0.89–0.95) (p = 0.001 for dif-
ference) (Fig.1). With a cutoﬀ at ≥ 3 points DENOVA had
a sensitivity of 100% and a speciﬁcity of 83% to identify
episodes of IE in MEFsB, while at the suggested cutoﬀ of 4
points , the NOVA score had a sensitivity of 100% and a
speciﬁcity of 29%.
The NOVA and the DENOVA score were validated in a
separate cohort of 485 patients with EFsB, 233 patients
were excluded due to polymicrobial bacteremia (n = 168),
age under 18years (n = 42), or unavailable records (n = 23).
Finally, 268 episodes in 252 patients were included in the
analyses, 26 classiﬁed as IE and 242 as non-IE.
The majority (238 patients) had only one episode of
MEFsB. Sixteen episodes, 4 with IE and 12 non-IE, were
followed by a new episode within 360 days. The episodes
that followed an IE were always another episode of IE. Six
non-IE episodes were followed by a new non-IE and six
were followed by an episode of IE. Two patients had three
episodes. 62 patients died within 360 days because of rea-
sons presumed to be unrelated to IE.
The characteristics of patients in the validation cohort
were similar to that of the calibration cohort, though some
diﬀerences were noted (Supplementary material 4).
When the DENOVA score was applied to the valida-
tion cohort, the resulting ROC curve had an AUC of 0.95
(95% CI, 0.93–0.98) which was signiﬁcantly higher than
that of the adapted NOVA (AUC 0.92 (95% CI 0.88–0.95),
p = 0.007). At the predeﬁned cutoﬀ of three points, DEN-
OVA had a sensitivity of 100% and a speciﬁcity of 85%
compared to the NOVA score (with cutoﬀ 4 ) with a sen-
sitivity of 100% and a speciﬁcity of 35%.
Combining the calibration and validation cohorts and
analyzing the subgroup of patients where echocardiography
had been performed, DENOVA had a sensitivity of 100%
and a speciﬁcity of 62%. The numbers needed to screen to
48 A.Berge et al.
ﬁnd one case of IE was 2.4 for DENOVA (≥ 3) and 7 for
NOVA (> 4).
Bacteremia with enterococci is a condition which can be
complicated by IE, and tools to aid clinicians, to decide
whether echocardiography should be performed, are poten-
tially very useful. We propose the use of the DENOVA scor-
ing system to guide the use of TEE in MEFsB. Importantly,
Table 1 Characteristics of
episodes of MEFsB with and
without IE at the time of scoring
a Consisting of any of previous IE, native valve disease, or valve prosthesis and is Valve disease (V) in
NOVA  and DENOVA
b Most common other infections were wound infections and intravascular infections
IE (n = 44) Non-IE (n = 353) Odds ratio (95% CI) p value
Age (years, median) 70 76 0.98 (0.95–1.00) 0.039
<55 7 (16) 18 (5) 1 (ref)
55–64 6 (14) 48 (14) 0.34 (0.10–1.2) 0.10
65–74 11 (25) 98 (28) 0.31 (0.10–0.97) 0.044
75–84 14 (32) 111 (31) 0.34 (0.11-1.0) 0.054
≥85 6 (14) 78 (22) 0.22 (0.06–0.76) 0.017
Sex (% women) 8 (18) 92 (26) 0.61 (0.27–1.4) 0.22
Charlson score (median) 2 3 0.89 (0.79–1.0) 0.052
0–1 16 (36) 99 (28) 1 (ref)
2–3 17 (39) 115 (33) 0.93 (0.45–1.9) 0.84
≥4 11 (25) 139 (39) 0.50 (0.22–1.1) 0.087
Predisposing heart conditiona26 (59) 65 (18) 6.2 (3.3–12) < 0.001
Previous IE (%) 7 (16) 5 (1) 13 (5.0–34) < 0.001
Native valve disease (%) 10 (23) 39 (11) 2.3 (1.0–5.0) 0.046
Valve prosthesis (%) 16 (36) 34 (10) 5.2 (2.5–11) < 0.001
Intracardiac device (%) 5 (11) 40 (11) 0.99 (0.37–2.7) 0.21
Previous EFsB (%) 9 (20) 27 (8) 3.0 (1.3–7.0) 0.01
Site of acquisition (%)
Community 22 (50) 90 (26) 2.9 (1.5–5.5) 0.001
Health care 21 (48) 181 (51) 0.87 (0.47–1.6) 0.66
Nosocomial 1 (2) 81 (23) 0.08 (0.01–0.57) 0.01
Fever (%) 36 (82) 288 (82) 1.0 (0.46–2.3) 0.94
Murmur (%) 36 (82) 49 (14) 28 (12–66) < 0.001
Embolization (%) 8 (18) 1 (0) 76 (9.4–610) < 0.001
Duration of symptoms ≥ 7 days 30 (68) 43 (12) 15 (7.6–31) < 0.001
≥2 positive cultures (%) 43 (98) 221 (62) 27 (3.4–210) 0.002
Origin of infection (%)
Urinary tract 1 (2) 159 (45) 0.03 (0.003–0.21) < 0.001
Gastrointestinal and biliary 0 52 (15) N/A
Otherb2 (5) 38 (11) 0.38 (0.09–1.6) 0.19
Unknown 41 (93) 104 (29) 34 (10–110) < 0.001
Table 2 Variables of the DENOVA score, each giving 1 point, and
their association with IE in multivariate analyses
Odds ratio (95% CI) p value
Duration of symptoms ≥ 7 days 9.7 (3.6–26) < 0.001
Embolization 50 (6.2–400) < 0.001
Number of positive cultures ≥ 2 6.8 (1.5–32) 0.01
Origin of infection unknown 7.3 (2.0–26) 0.003
Valve disease 1.7 (0.57–4.9) 0.35
Auscultation of murmur 13 (4.7–36) < 0.001
The DENOVA score eﬃciently identiﬁes patients withmonomicrobial Enterococcus faecalis…
DENOVA had a high sensitivity and speciﬁcity both in
the original cohort and in the separate validation cohort.
DENOVA had a higher speciﬁcity than the previously pro-
posed NOVA score and the number needed to screen to ﬁnd
one case of IE was 2.4 for DENOVA, as compared to 7 for
NOVA. Using DENOVA to guide the use of TEE could
reduce the number of procedures for patients at low risk
of IE and the costs for the health-care system. Moreover,
DENOVA is easy to use since each variable gives one point
as compared to the more diﬀerentiated NOVA score .
Another strength of our study is that the DENOVA score was
generated in a population-based cohort avoiding the poten-
tial bias of single center studies and further it was validated
in a separate cohort, from a referral hospital with partly dif-
ferent epidemiology, with similar performance. Finally, our
design avoids the bias introduced when patients subjected to
TEE with a ﬁnding of IE are compared to patients subjected
to TEE without a ﬁnding of IE (a type of over-matching)
such as in the study behind the NOVA score . When
we applied the DENOVA score only to patients that had
undergone echocardiography, the sensitivity was still 100%,
whereas the speciﬁcity dropped to 62%. This was expected
since the decision by the treating physician to perform TEE
was likely based on a perceived increased risk for IE.
However, there are several limitations to this study. First,
the DENOVA score cannot be applied to E. faecium bac-
teremia and not to polymicrobial EFsB. In both these con-
ditions, IE is uncommon [2, 4, 6] and separate very large
studies would be needed to adapt the score to these condi-
tions. Secondly, the retrospective design of our study makes
it sensitive to misclassiﬁcation, potentially non-diﬀerential.
For example, a clinician who suspects IE might be more
prone to take additional blood cultures, make a more thor-
ough heart auscultation, or look for emboli, which will
potentially increase the DENOVA score. Further external
validation and most importantly prospective studies are
needed to address this concern.
Thirdly, a limited number of patients underwent TEE in
our study. This is a common problem in this type of studies
[4, 5, 14, 15] and a consequence of the retrospective design.
Even in prospective studies, however, a high frequency of
TEE in bacteremia is not always obtained  and, impor-
tantly, a negative TEE does not rule out the presence of IE
or that a visible vegetation can develop after TEE. To assess
the risk of misclassiﬁcation, we followed the patients for
360 days. Patients with a non-IE MEFsB were rarely treated
more than 14 days and it is thus unlikely that a misclassi-
ﬁed IE would have been without a relapse. However, a large
number of patients died within 360 days after a non-IE epi-
sode (142 and 62 in the calibration and validation cohorts,
respectively). We cannot rule out that some of these patients
died from a missed IE, yet the analysis of patient records did
not indicate that this was the cause of death. The proportion
of patients diagnosed with IE was very similar in our cohort
and a recent Danish cohort also indicating that we did not
miss a substantial number of IE cases .
In patients with multiple MEFsB episodes, the ﬁrst classi-
ﬁed as non-IE, in both the calibration and validation cohort
together, a new episode of IE was detected in 12 patients
during 360 days of follow-up. In eight of these, no TEE was
Fig. 1 Receiver operator charac-
teristics (ROC) curve for the
ability of the NOVA (blue) and
DENOVA (red) score to sepa-
rate episodes with IE from non-
IE episodes. The inset shows the
number of episodes of IE (black
bars) and non-IE (gray bars) in
relation to the score obtained
using DENOVA (data from the
50 A.Berge et al.
done during the ﬁrst episode. The initial episodes might thus
have been misclassiﬁed in these cases. However, DENOVA
score in these eight episodes was ≥ 3 in ﬁve cases, which
would have been subjected to TEE if DENOVA would have
In summary, the use of DENOVA in clinical decision-
making will help physicians to focus echocardiographic
investigations on persons at high risk for IE.
Acknowledgements This work was supported by the Swedish Govern-
ment Fund for Clinical Research (ALF), the Stockholm County Coun-
cil, the foundations of Marianne and Marcus Wallenberg, Crafoord,
Österlund. Lundgren, and the Royal Physiographic Society in Lund.
We acknowledge the advice by Dr Per Åkesson and the invaluable help
of Mrs. Lena Hyllebusk at the Department for Clinical Microbiology,
Lund. Part of this work has been presented at the ISCVID meeting in
Author contributions MR concieved the study and wrote the manu-
script together with AB. All authors contributed to the design of the
study. AK, AB and HÖ collected data and PN performed statistical
analyses. All authors contributed to the writing and gave their ﬁnal
Compliance with ethical standards
Conflict of interest On behalf of all authors, the corresponding author
states that there is no conﬂict of interest.
Open Access This article is distributed under the terms of the Crea-
tive Commons Attribution 4.0 International License (http://creat iveco
mmons .org/licen ses/by/4.0/), which permits unrestricted use, distribu-
tion, and reproduction in any medium, provided you give appropriate
credit to the original author(s) and the source, provide a link to the
Creative Commons license, and indicate if changes were made.
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