Journal of Pédiatrie Infectious Diseases 7 (2012) 151-157 151

DOI IO,3233/JPI-12O364
IOS Pr'ess

Applicability of the modified Duke criteria for

the diagnosis of infective endocarditis in
children with and without heart disease
Anjali Chelliaha, Lisa Saiman'»'''''^ and Stéphanie M,
''Morgan Stanley Children's Hospital ofNewYork-Presbyterian, New York, NY, USA
^'Department of Pediatrics, Columbia University Medical Center, New York, NY, USA
''Department of Infection Prevention and Control, NewYork-Presbyterian Hospital, New York, NY, USA

Received 26 February 2012

Revised 18 May 2012
Accepted 28 June 2012

Abstract. We sought to assess whether children with pre-existing heart disease treated for infective endocarditis (IE) were less
likely to fulfill the tnodified Duke criteria for definite IE than those without heart disease. While the modified Duke criteria are
widely accepted in research and clinical diagnosis, their applicability in diagnosing IE in children is not as well studied. We
performed a retrospective single-center study of children treated for IE from January 1999-December 2009 and compared the
proportion of children with and without heart disease who fulfilled modified Duke criteria for definite IE, We also examined
these criteria in children with cyanotic heart disease, hospital-acquired IE, or recent cardiac surgery. Fifty (60%) of 84 children
treated for IE met modified Duke criteria for definite IE, The proportion of children with and without heart disease who fulfilled
modified Duke criteria for definite IE was not significantly different (38/68, 56%, versus 12/16, 75%, respectively, p = 0,26),
Patients with cyanotic heart disease or hospital-associated IE were as likely to meet definite criteria as those without. However,
children with early postoperative IE were less likely than those with late postoperative or without cardiac surgery to meet definite
IE criteria (12/31, 39%, versus 38/53, 72%, p = 0,005), Only 60% of children treated for IE met modified Duke criteria for
definite IE, Children with early postoperative IE were least likely to fulfill these criteria. Future studies should evaluate potential
strategies to improve the diagnosis of IE in children.

Keywords: Infectious endocarditis, modified Duke criteria, congenital heart disease, postoperative endocarditis

1. Introduction tion of the critical role of echocardiography and the

Despite advances in diagnostic strategies, the di-
agnosis of infective endocarditis (IE) remains chal-
lenging as it relies on a combination of signs, symp-
toms, and tests rather than a single definitive test. The
Duke criteria and the modified Duke criteria were
developed to improve the diagnosis of IE, in recogni-
*Conrespondence: Stéphanie M, Levasseur, MD, Division of
Pédiatrie Cardiology, 3959 Broadway, CHONY 2 North, New
York-Presbyterian Hospital, New York, NY 10032, USA. Tel,: -Hi
212 305 2359; Fax: +1 212 305 4429; E-mail: sl2363@columbia,
edu.
evolving spectrum of pathogens [1,2], Although the
Duke and the modified Duke criteria were initially
intended to be used in clinical research and epidemi-
ology, many groups have studied their applicability
for clinical practice among adult populations [3-9],
Studies of the criteria among pédiatrie populations
have been few [10-14],
The changing demographics of the at-risk pédiatrie
population can further complicate the diagnosis of IE,
We and others have found that children with IE are
younger, more likely to have underlying heart disease,
and more likely to develop hospital-acquired or post-

1305-7707/12/$27.5O © 2012 - IOS Press and the authors. All rights reserved
152 A. CheUialt et al. /Modified Duke ciiieria in children with heart disease
Operative IE when compared to previous eras [15-18].
The original and modified Duke criteria include heart
disease as a minor diagnostic criterion, which may
increase the frequency of the diagnosis of possible IE
in such children. Cardiac interventions that include
foreign graft material can increase the rate of IE and
vegetations or abscesses may be more difficult to
visualize by echocardiography in structurally abnor-
mal hearts and following cardiac surgery [19]. As
cyanotic heart disease and residual shunts after in-
tervention may confer a higher risk of mortality from
IE, clinicians may be more likely to treat for IE in such
children [20]. We hypothesized that children with
heart disease treated for IE would be less likely to
fulfill the modified Duke criteria for definite IE than
those without heart disease. We also examined the
fulfillment of these criteria in those treated for IE with
cyanotic heart disease, hospital-acquired IE, or recent
cardiac surgery. Finally, we evaluated which diag-
nostic criteria were most commonly met in those with
definite versus possible IE.
2. Materials and methods
2. /. Study design and population
We performed a retrospective review of pédiatrie
patients treated for IE from January 1, 1999 to De-
cember 31, 2009 at the Morgan Stanley Children's
Hospital of NewYork-Presbyterian, Columbia Uni-
versity Medical Center. Patients less than 21 years of
age who were diagnosed with and treated for IE,
which we used as the 'gold standard' for IE, were
eligible for inclusion. Potential study subjects were
identified from International Classification of Dis-
eases-9 (ICD-9) discharge codes for endocarditis,
echocardiogram reports, and cardiology and infec-
tious diseases consultation records. The Institutional
Review Board at Columbia University Medical Center
approved this study and granted a waiver of informed
consent.
2.2. Case definitions
A patient was classified with heart disease if they
were previously diagnosed with congenital heart dis-
ease, rheumatic heart disease, cardiomyopathy, pul-
monary hypertension, or had undergone a cardiac
transplant. Patients were considered to have cyanotic
heart disease if they had a right to left intracardiac
shunt with a baseline oxygen saturation < 95% on
room air when IE was diagnosed. Early postoperative
IE was defined as IE within six months of cardiac
surgery and late postoperative IE was defined as IE
more than six months after surgery. Hospital-acquired
IE was defined as IE presenting 72 hours or more after
hospital admission and/or within eight weeks of car-
diac surgery [21,22].
2.3. Data collection and analysis
Demographic and clinical characteristics (e.g.,
underlying cardiac diagnosis, clinical signs and
symptoms, microbiology results, and echocardio-
graphy Undings) and duration of hospital stay were
obtained by reviewing the electronic medical records
of eligible patients. Patients were retrospectively
classified with definite, possible, or rejected IE by the
modified Duke criteria. The proportion of children
with and without heart disease; with and without cy-
anotic heart disease; with early versus late or non-
postoperative IE; and with community- versus hospi-
tal-acquired IE who met the modified Duke criteria for
definite IE were compared. The diagnostic criteria
fulfilled in those with definite versus possible IE were
also assessed. Characteristics of different subgroups
of patients were compared using Student's t-test for
continuous variables and the Chi-square test or Fish-
er's exact test, as appropriate, for categorical vari-
ables.
3. Results
3.1. Study population
Eighty-four patients met inclusion criteria for this
study, of whom 68 (81%) had underlying heart dis-
ease. Among those with heart disease, 18 (26%) of 68
had cyanotic heart disease when diagnosed with IE.
The demographic and clinical characteristics of chil-
dren with and without underlying heart disease were
similar, as shown in Table I. However, children with
cyanotic heart disease were younger than those with
acyanotic heart disease (median age 0.3 years versus
8.4 years, p = O.OOl), more likely to have undergone
cardiac surgery (94% versus 56%, p = 0.003), and had
a longer duration of hospitalization (median 46 days
versus 18.5 days, p = 0.055).
 A, Chelliah et al, /Modified Duke criteria in children with heart disease 153

Table 1
Characteristics of children with and without heart disease diagnosed with IE
Characteristic Heart disease No heart disease p-value
;i = 68 n = 16
Number of males (%) 38(56) 6(38) 0.38
Median age in years (IQR)" 3.4(0.1, 12.3) 7.8(1.5, 15.9) 0.15
Number hospitalized in neonatal
15(22) 2(13) 0.51
intensive care unit (%)
Hospital-acquired IE (%) 33 (49) 8(50) 0.92
Median hospitalizaron in days (IQR) 25(10.8,44.3) 29(14.8,34.8) 0.50
"IQR = interquartile range; IE: Infective endocarditis.

Table 2 IE were not predictive of fulfilling definite criteria for

Characteristics associated with fulfilling modified Duke criteria for IE (Table 2). In contrast, children diagnosed with
definite IE
early postoperative IE were less likely to meet criteria
Characteristics Definite IE Not Definite IE" p-value for definite IE (12 out of 31) than children with either
n = 50 n = 34
n (%) « (%) late postoperative IE or without postoperative IE (38
Gender
out of53)(p = 0.005).
Male 26 (59%) 18(41%)
>0.99 3.3. Fulfillment of major and minor criteria
Female 24 (60%) 16(40%)
Age
<2yrs 21 (57%) 16(43%) The major and minor criteria fulfilled by children
0.66
í2yrs 29 (62%) 18(38%) with definite versus possible IE are compared in Table 3.
Known heart disease Patients with definite and with possible IE were
Yes 38 (56%) 30 (44%) equally likely to fulfill individual criteria with two
0.26
No 12(75%) 4 (25%) exceptions. Those with definite IE were more likely to
Cyanotic heart disease have positive findings on echocardiogram (94% ver-
Yes 10(56%) 8 (44%) sus 24%, p < 0.0001) and to have vascular or embolie
0.70
No 40(61%) 26 (39%)
phenomena (40% versus 12%, p - 0.01). Most pa-
Early postoperative IE
tients (62%) classified with definite IE fulfilled two
Yes 12(39%) 19(61%)
0.005 major criteria and most patients (82%) classified with
No 38 (72%) 15(28%)
possible IE fulfilled one major and one minor crite-
Hospital-acquired
Yes 22 (54%) 19(46%)
rion. Children without heart disease were more likely
0.28 to experience vascular or embolie phenomena than
No 28 (65%) 15(35%)
those with heart disease (67% versus 32%, p = 0.04).
"Includes possible and rejected IE; IE: Infective endocarditis.
Only 14 (17%) patients had transesophageal echo-
cardiograms (TEE) performed. Eight of these patients
3.2. Characteristics associated with definite IE had non-diagnostic transthoracic echocardiograms
(TTE) and none had findings consistent with IE on
Among the 84 patients, 50 (60%) met criteria for TEE. Six had TTEs consistent with IE and underwent
definite IE, 33 (39%) met criteria for possible IE, and TEE to identify suspected local complications; of
one (1 %) patient was classified as rejected for IE. This these, two were found to have an abscess.
patient presented with persistent fevers following
prosthetic mitral valve placement and was treated for
IE despite negative cultures and no transthoracic 4. Discussion
echocardiographic findings consistent with IE. The
proportion of children with and without heart disease To our knowledge, this study represents the first
who fulfilled the modified Duke criteria for definite IE systematic evaluation of children with and without
was not significantly different (56% versus 75%, heart disease to determine the factors associated with
respectively, p = 0.26), as shown in Table 2. Age, failure to meet the modified Duke criteria for definite
gender, cyanotic heart disease, and hospital-acquired IE. We did not confirm our hypothesis that children
154 A. Chelliah ei ai /Modified Duke criteria in children with heart di.sea.se

Table 3
Modified Duke criteria in children with definite versus possible IE

Criteria Definite/I =50 Possible n = . /Í-va lue

n (%) n {%)
Major
Pathologic criteria 12 (24) n/a -
Culture criteria 34(68) 19(57) 0.36
Positive blood culture: typical" 25 (50) 11 OS) 0.18
Positive blood culture: persistent 9(18) 8(24) 0.58
One positive blood culture for Coxiella bumetti or IgG
0 0 0
antibody titer > 1 : 800
Echocardiography criteria 47(94) 8(24) < 0.0001
Minor
Predisposing heart disease or intravenous drug abuse** 35 (70) 28 (85) 0.19
Fever > 38" 47(94) .30(91) 0.68
Vascular/ embolie phenomena 20(40) 4(12) 0.01
Immunologie phenomena 3(6) 0 0.28
Single positive culture for atypical organism 13(26) 7(21) 0.79
Serologie evidence of infection 1(2) 0 1
Clinical criteria Definite Possible
2 major 31(62) n/a
I major + 3 minor 19(38) n/a
5 minor 0 n/a
I major + I minor n/a 27 (82)
3 minor n/a 6(18)

"Typical culture criteria include *: 2 positive cultures for viridians streptococci. Sireptococciis bovis. HACEK
group. S. aureus, or community-acquired enteroeoeei in the absence of a primary focus.
''One patient had a history of intravenous drug abuse. IE: Infective endocarditis.

with heart disease would be less likely to fulllll crite-
ria for definite IE. Additionally, neither cyanotic heart
disease nor hospital-acquired IE predicted failure to
fulfill the modified Duke criteria for definite IE.
However, those with early postoperative IE were less
likely to meet definite criteria than those with late
postoperative IE or those without previous cardiac
surgery. We speculate that in the early postoperative
period, patients with positive blood cultures were
more likely to be treated for IE with less robust evi-
dence as clinicians have justifiable concerns about
increased morbidity and mortality from IE in these
vulnerable patients.
4.1. Utility of Duke criteria in pédiatrie populations
Numerous investigators have assessed the sensi-
tivity of the Duke and the modified Duke criteria in
diagnosing IE [23]. To do so, most studies have as-
sessed the sensitivity of the Duke criteria against the
'gold standard' of clinical diagnosis of IE. Among
adult patients, the sensitivity of the Duke criteria
ranges from 49% to 86% [1,3-5,6-9,24-26,]. In
children, three single-center studies found that the
sensitivity of the Duke criteria ranged from 48% to
66%, as summarized in Table 4. Three additional
studies, including our study, assessed the sensitivity of
the modified Duke criteria in a total of 298 children.
Yoshinaga et al. found that 59% of pédiatrie patients
(unpublished data from author) met definite criteria
for IE [12]. Our finding that 60% of our patients met
definite criteria for IE is consistent with these obser-
vations. In contrast, Tissières et al. found that 88% of
their patients fulfilled the modified criteria for definite
IE, but their study population largely consisted of
children referred from Africa for congenital heart
surgery and their findings may not be generalizable.
Thus, the sensitivity of the Duke criteria and the
modified Duke criteria seem comparable in the pédi-
atrie population.
The modifications made to the Duke criteria were
intended to further improve the sensitivity of the di-
agnosis of IE. These modifications included new
major microbiologie criteria, i.e., positive serology or
blood cultures for Q fever (Coxiella bumetti) or two or
more blood cultures for Sraphylococcus aureus (either
 A. Chelliah et al. /Modified Duke criteria in children with heart disease
Table 4
Case series evaluating the Duke and modified Duke criteria in children
Author [Ref], Country Study years Study patients (n)
Del Pont [11], Argentina 1978-1994 38
Stockheim [13], USA 1978-1996 104
Liewetal. [14], Singapore 1997-2004 27
Tissieres [10], Switzerland 1985-2001 40
Yoshinaga [4444]°, Japan 1997-2001 174
This study, USA 1999-2009 84
"Additional data obtained from personal communication with the author; IE: Infective endocarditis.
community or nosocomial acquisition) and empha-
sized the use of TEE to improve visualization of le-
sions consistent with IE [2,9,27,28]. However, these
modifications may be less useful in pédiatrie popula-
tions than in adult populations. For example, Q fever
may cause 37% of cases of "culture-negative" endo-
carditis in adults, but it is rarely reported in children [28,
29]. In the three published studies assessing the mod-
ified Duke criteria (Table 4), only one of 298 children
had evidence of Coxiella burnetti [10]. Studies of 5.
aureus endocarditis suggest that many cases of right-
sided IE occur as a result of intravenous drug abuse, a
rare risk factor in children [30]. Furthermore, both
community- and hospital-acquired 5. aureus bacte-
remia in adults may be associated with IE in 10% to
40% of cases [31-34]. However, studies performed in
children suggest that the rates of IE associated with 5.
aureus bacteremia are generally lower than the rates
noted in adults. Valente et al. assessed 51 children
with 5. aureus bacteremia and no symptoms of IE and
found that 12% met modified Duke criteria for defi-
nite IE and 6% met criteria for possible IE [35]. No-
tably, 90% of those with IE had congenital heart dis-
ease. In contrast, Ross et al. found that only 3 (1%) of
298 children with at least one positive blood culture
for 5. aureus bacteremia were diagnosed with IE not
clinically suspected upon admission [36]. In different
pédiatrie populations, the rates of IE associated with 5.
aureus bacteremia have varied, ranging from 0% to
11% [37^0]. Our study population had only 5 pa-
tients with nosocomially- acquired 5. aureus; all of
these patients would be classified as having defmite IE
by the original Duke criteria as well as the modified
criteria. Thus, use of the modified Duke criteria did
not identify any additional patients as having definite
IE compared to the original criteria. Finally, as TTE is
highly sensitive for IE in pédiatrie populations [41,
42], additional benefit from TEE has not been shown
in children, although very few patients have been
155
Criteria Definite IE (%) Possible IE (%) Rejected IE (%)
Duke 66 34 0
Duke 66 34 0
Duke 48 52 0
Modified Duke 88 12 0
Modified Duke 59 32 9
Modified Duke 60 39 1
studied [41]. While TEE was performed in a minority
of our patients (14/84, 17%), this diagnostic modality
did not improve the diagnosis of IE, although it did
identify local complications in two patients. None-
theless, the low rate of utilization of TEE did not
permit us to conclusively assess its diagnostic utility.
4.2. Limitations
This study had limitations. Our relatively small
sample size may have lacked sufficient power to de-
tect chiiracteristics of patients that predicted fulfilling
definite IE criteria. Given our retrospective study
design, we lacked complete physical exam data in a
small number of patients from the earlier years of this
study (prior to implementing electronic medical rec-
ords) which may have led to us to underestimate
vascular and immunologie phenomena. As in many
other studies of the diagnostic utility of the modified
Duke criteria, clinical diagnosis was used as the 'gold
standard' for IE, and as these criteria have been widely
utilized for over a decade, they are likely to have
influenced physicians' clinical decision making.
5. Conclusion
Children with IE, particularly those with underly-
ing heart disease, represent a unique population with
different clinical characteristics compared to adult
patients with IE. While 60% of our cases met modi-
fied Duke criteria for definitive diagnosis, children
diagnosed with post-operative IE were least likely to
fulfill defmite criteria. This observation suggests that
clinicians have a lower threshold for treating patients
with positive blood cultures who are in the early post-
operative period for IE. We suggest that, when feasi-
ble, a multidisciplinary team of cardiologists, infec-
tious disease specialists, and clinical microbiologists
156 A. ClielUali et til. /Modified Duke criieriu in children willi heart di.sease
be assembled lo employ standardized diagnostic pro-
tocols, similar to those implemented by Botelho-
Neverset et al., to improve accurate diagnosis and
management of IE [43]. Potential strategies could
include increased use of TEE and improving central
line care to reduce catheter-associated bloodstream
infections in postoperative patients. Future studies
should include a multi-center study to confirm our
findings and should evaluate potential strategies to
improve the diagnosis of IE in children.
Acknowledgements
The authors would like to thank Luis R. Alba for
assistance with database design and Drs. Thomas
Stare and Welton Gersony for helpful discussions
about our findings.
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