MIS-C and Cardiac

Conduction Abnormalities
Nak Hyun Choi, MD, Michael Fremed, MD, Thomas Starc, MD, Rachel Weller, MD, Eva Cheung, MD, Anne Ferris, MBBS,
Eric S. Silver, MD, Leonardo Liberman, MD

Multisystem inflammatory syndrome in children (MIS-C) has spread through the

OBJECTIVES: abstract
pediatric population during the coronavirus disease 2019 pandemic. Our objective for the
study was to report the prevalence of conduction anomalies in MIS-C and identify predictive
factors for the conduction abnormalities.
METHODS: We performed a single-center retrospective cohort study of pediatric patients
,21 years of age presenting with MIS-C over a 1-month period. We collected clinical
outcomes, laboratory findings, and diagnostic studies, including serial electrocardiograms, in
all patients with MIS-C to identify those with first-degree atrioventricular block (AVB) during
the acute phase and assess for predictive factors.
RESULTS: Thirty-two patients met inclusion criteria. Median age at admission was 9 years. Six of
32 patients (19%) were found to have first-degree AVB, with a median longest PR interval of
225 milliseconds (interquartile range 200–302), compared with 140 milliseconds
(interquartile range 80–178) in patients without first-degree AVB. The onset of AVB occurred
at a median of 8 days after the initial symptoms and returned to normal 3 days thereafter. No
patients developed advanced AVB, although 1 patient developed a PR interval .300
milliseconds. Another patient developed new-onset right bundle branch block, which resolved
during hospitalization. Cardiac enzymes, inflammatory markers, and cardiac function were not
associated with AVB development.
CONCLUSIONS: In our population, there is a 19% prevalence of first-degree AVB in patients with
MIS-C. All patients with a prolonged PR interval recovered without progression to high-degree
AVB. Patients admitted with MIS-C require close electrocardiogram monitoring during the
acute phase.

Division of Pediatric Cardiology, NewYork-Presbyterian Morgan Stanley Children’s Hospital, Columbia University WHAT’S KNOWN ON THIS SUBJECT: A novel disease
Irving Medical Center, New York, New York known as multisystem inflammatory syndrome in
children (MIS-C) has been increasingly prevalent in
Drs Choi and Liberman conceptualized and designed the study, drafted the initial manuscript, and pediatric patients with coronavirus disease 2019. Few
reviewed and revised the manuscript; Drs Fremed, Starc, Weller, Cheung, Ferris, and Silver critically data are available on the incidence of arrhythmia and
reviewed and revised the manuscript for important intellectual content; and all authors approved
cardiac involvement in children with MIS-C.
the final manuscript as submitted.
DOI: https://doi.org/10.1542/peds.2020-009738 WHAT THIS STUDY ADDS: Pediatric patients with MIS-C
may develop conduction anomalies, particularly first-
Accepted for publication Sep 4, 2020 degree atrioventricular block. Patients have elevated
Address correspondence to Leonardo Liberman, MD, Division of Pediatric Cardiology, NewYork- levels of cardiac and inflammatory markers, which are
Presbyterian Morgan Stanley Children’s Hospital, Columbia University Irving Medical Center, 3959 not associated with development of conduction
Broadway, CHN 2-255, New York, NY 10032. E-mail: ll202@cumc.columbia.edu abnormalities. First-degree atrioventricular block
PEDIATRICS (ISSN Numbers: Print, 0031-4005; Online, 1098-4275). typically returns to normal after the acute illness phase.
Copyright © 2020 by the American Academy of Pediatrics
To cite: Choi NH, Fremed M, Starc T, et al. MIS-C and
FINANCIAL DISCLOSURE: The authors have indicated they have no financial relationships relevant to Cardiac Conduction Abnormalities. Pediatrics. 2020;146(6):
this article to disclose. e2020009738

Downloaded from www.aappublications.org/news at Indonesia:AAP Sponsored on December 4, 2020

PEDIATRICS Volume 146, number 6, December 2020:e2020009738 ARTICLE
Since the first report of coronavirus
disease 2019 (COVID-19) on
December 31, 2019, new disease
manifestations and complications are
continuing to appear in pediatric
patients. Early studies in China
revealed that children of all ages were
susceptible to severe acute
respiratory syndrome coronavirus 2
(SARS-CoV-2), the viral etiology of
COVID-19.1 Compared with adults,
pediatric patients were more
commonly asymptomatic or had
benign respiratory and
gastrointestinal symptoms.1 Recently,
a new study revealed an emergence
of Kawasaki disease–like
presentations in pediatric patients
with an active or recent diagnosis of
COVID-19.2 The new syndrome, now
known as multisystem inflammatory
syndrome in children (MIS-C), has
been most prevalent in regions highly
burdened with COVID-19.2–4
As a large academic institution in
New York City at the epicenter of the
COVID-19 pandemic, our institution
has cared for multiple patients with
MIS-C. During the clinical assessment
and treatment of patients with MIS-C,
a subset of pediatric patients with PR
prolongation on the
electrocardiogram (ECG), consistent
with first-degree atrioventricular
block (AVB), emerged. Although
a recent case report described an
adult with a high-degree AVB and
a confirmed diagnosis of COVID-19 in
the absence of MIS-C symptoms, to
our knowledge there has not been
a similar report in pediatric patients.5
Our primary aim for this study was to
report the frequency of conduction
anomalies in MIS-C and to characterize
the presentation and clinical course for
the subset of patients who develop these
abnormalities. We also sought to identify
predictive factors for conduction
abnormalities in patients with MIS-C.
METHODS
The study was approved by the
Columbia University Irving Medical
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2 CHOI et al
Center Institutional Review Board.
We conducted a retrospective cohort
study of all patients ,21 years of age
presenting to NewYork-Presbyterian
Morgan Stanley Children’s Hospital in
New York City, New York, with
a clinical diagnosis of MIS-C between
April 15, 2020, and May 15, 2020. A
diagnosis of MIS-C was made by using
the case definition per the US Centers
for Disease Control and Prevention
guidelines.3,4 The diagnosis of MIS-C
was made in patients ,21 years old
presenting with fever ($38.0°C for
$24 hours or report of subjective
fever lasting $24 hours), laboratory
evidence of inflammation ($1 of the
following: elevated C-reactive protein
level, erythrocyte sedimentation rate,
fibrinogen level, procalcitonin level,
d-dimer level, ferritin level, lactic acid
dehydrogenase level, or interleukin 6
level or elevated neutrophil count),
and clinical severity requiring
hospitalization. Patients had
multisystem ($2) organ involvement,
including the cardiac, renal,
respiratory, hematologic,
gastrointestinal, dermatologic, or
neurologic system. Patients did not
have a plausible alternative diagnosis
and had to have tested positive for
current or recent SARS-CoV-2
infection by reverse transcription
polymerase chain reaction (PCR),
serology, or an antigen test.3,4 At our
institution, the serology testing does
not differentiate between
immunoglobulin M and
immunoglobulin G; thus, a positive
serology test result does not clearly
define a resolved infection. ECGs were
routinely obtained after admission
according to our institution’s
guidelines for workup of all patients
with MIS-C.6 First-degree AVB on the
ECG was defined as a PR interval on
a surface ECG .200 milliseconds
without associated disruption of
atrial-to-ventricular conduction.7 All
ECGs were read by a pediatric
cardiologist using electronic calipers.
All patients suspected of having MIS-
C were placed on continuous
telemetry monitoring during
admission, which was reviewed daily
by a pediatric cardiologist. All
statistical analyses were conducted in
Stata software version 16 (Stata Corp,
College Station, TX). Clinical and
demographic variables were
described by using summary
statistics. All continuous data were
presented as medians with ranges or
interquartile ranges (IQRs).
Categorical variables were presented
as number (%). The Wilcoxon rank
test was used for univariable
analyses. Variables with a P value
,.05 were considered statistically
significant.
RESULTS
Patient Characteristics
Thirty-two patients were diagnosed
with MIS-C. Demographic details of
the study population are listed in
Table 1. The median age was 9 years
(range 1–20), and there were 17
(53%) male patients. A majority of
patients (n = 22; 69%) were found to
have negative results on the SARS-
CoV-2 PCR testing but positive results
on the COVID-19 serology testing. The
remaining patients (n = 10; 31%) had
positive results on PCR testing. The
majority of patients received both
glucocorticoid (n = 30; 94%) and
intravenous immunoglobulin (IVIg)
therapy (n = 29; 91%) during
hospitalization, whereas 13% (n = 4)
of patients received anakinra,
a recombinant human interleukin-1
receptor antagonist.
ECG Findings
Of the 32 total patients, 6 had first-
degree AVB (19%) during
hospitalization, including 2 patients
with PR prolongation on the initial
ECG at presentation. None of the 6
patients progressed to advanced AVB
while on telemetry monitoring. The
median of the longest PR interval for
patients who did not develop first-
degree AVB versus the patients who
developed first-degree block, was 140
milliseconds (range: 80–178) vs 225
TABLE 1 Patient Characteristics
Total No. patients
Age, y, median (range)
Male sex, n (%)
COVID-19 laboratory testing, n (%)
PCR negative result and serology positive result
PCR positive result and serology positive result
PCR positive result and serology result unknown
Treatment, n (%)
IVIg
Glucocorticoids
Anakinra
Initial ECG intervals, median (IQR)
HR, beats per minute
PR, ms
QRS, ms
QTc, ms
HR, heart rate.
milliseconds (range: 200–302),
respectively (P # .01). No patients
developed tachyarrhythmias during
hospitalization. None of the patients
with first-degree AVB received
medications that prolonged the PR
interval, including b-blockers,
calcium channel blockers, or other
antiarrhythmic medications.
Figure 1 reveals chronological PR
changes for the 6 patients with MIS-C
FIGURE 1
PR interval changes on serial ECGs during MIS-C from onset of illness.
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PEDIATRICS Volume 146, number 6, December 2020
findings in patients with first-degree
Patient Characteristics AVB included a prolonged QTc
32
interval (n = 2), ectopic atrial rhythm
9 (1–20) (n = 2), ST elevation in inferior leads
17 (53) (n = 2), and nonspecific ST and T
wave abnormalities (n = 5). Notably, 1
22 (69) patient developed a new-onset right
7 (22)
3 (9)
bundle branch block (RBBB) along
with first-degree AVB on day 3 of
29 (91) hospitalization, both of which
30 (94) subsequently resolved by day 5
4 (13) (Fig 2). There was 1 patient who was
128 (102–143)
found to have profound PR
135 (121–160) prolongation of 302 milliseconds
77 (72–86) (Fig 3). Two of the 6 patients with PR
421 (398–434) prolongation had an initial QTc
interval of 476 milliseconds and
a QTc interval of 473 milliseconds in
the absence of medications
who developed first-degree AVB. All prolonging the QTc interval. At the
patients underwent an ECG every 24 conclusion of the study, both patients’
to 48 hours until discharge. The onset QTc values became normal.
of first-degree AVB occurred at
Additionally, abnormal ECG findings
a median of 8 days after the initial
in patients without first-degree AVB
onset of symptoms (range: 5–10). The
included a prolonged QTc interval
time to resolution of PR prolongation
(n = 4), ectopic atrial rhythm (n = 1),
occurred at a median of 3 days after
ST elevation or depression (n = 3), T
the initial first-degree AVB (range:
wave inversions (n = 5), nonspecific
1–5). One patient’s prolonged PR
ST and/or T wave abnormalities (n =
interval did not resolve by the
14), nonspecific intraventricular
conclusion of the study. Other ECG
conduction delay or right ventricular
conduction delay (n = 5), right axis
deviation (n = 5), and intermittent
premature ventricular complexes (n =
1). Four patients without first-degree
heart block had QTc intervals of 474,
486, 488, and 494 milliseconds,
which all normalized by the
conclusion of the study.
Hospitalization Findings
There was no statistical difference in
the rate of ICU admission during
hospitalization between those with
first-degree AVB and those without (4
of 6 [67%] and 21 of 26 [81%],
respectively; P = .46).
All patients diagnosed with MIS-C
underwent echocardiography during
hospitalization, and the left
ventricular ejection fraction (LVEF)
was measured. Univariable analyses
were completed by using the lowest
ejection fraction during the patient’s
3

FIGURE 2
ECG findings in a 9-year-old boy. A, Initial 12-lead ECG on presentation revealing normal sinus rhythm
with narrow QRS complexes. B, Twelve-lead ECG on day 3 of hospitalization revealing first-degree AVB
(PR of 200 milliseconds) with RBBB.
hospitalization (Table 2). There were
2 patients with a significantly
decreased LVEF (30% and 35%) in
the group without conduction
anomalies and none in the group with
PR prolongation. Despite these
outliers, the median LVEF for patients
who had first-degree AVB, compared
with patients without, was not
FIGURE 3
Twelve-lead ECG revealing significant first-degree AVB with a PR interval of 302 milliseconds and
nonspecific T wave abnormalities in a 12-year-old boy.
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4 CHOI et al
significantly different (53.5% [IQR:
45–57] and 56.5% [IQR: 48–59],
respectively; P = .32).
Cardiac and inflammatory markers
were also obtained for all patients
during hospitalization, illustrated in
Table 2. No laboratory variable was
significantly associated with the
development of first-degree AVB. At
the time of the initial first-degree AVB
development, all patients had normal
electrolyte levels.
DISCUSSION
Since the initial report of COVID-19 in
December 2019, children with severe
complications requiring
hospitalization were relatively rare
during the first several months of the
pandemic. A recent surge in pediatric
patients with significant systemic
inflammatory response and
multiorgan dysfunction, with
symptoms overlapping with
Kawasaki disease, has shifted the
diagnostic and treatment paradigm
for the pediatric population.8,9 At our
institution, .30 patients were
admitted with a diagnosis of MIS-C
during the study period. From
a cardiovascular perspective, some
patients were noted to have
decreased cardiac function and
conduction abnormalities.
Early reports in adult patients
revealed direct cardiac complications
of COVID-19, including arrhythmias,
acute myocardial injury, and
myocarditis with circulatory
failure.10,11 In a recent study, an adult
patient was found to have high-
degree AVB in the setting of COVID-
19 illness in the absence of MIS-C
symptoms.5 In our study, we analyzed
pediatric patients with a COVID-
19–related inflammatory disease; our
patients with MIS-C exhibited
conduction abnormalities, including
first-degree AVB and RBBB.
AVB has been associated with
multiple infectious and inflammatory
diseases, such as Lyme disease, acute
rheumatic fever, and myocarditis.12–14
Occurring in 15% to 20% of patients,
a prolonged PR interval is a minor
criteria for diagnosis of acute
rheumatic fever.13,15 Our study
revealed a similar 19% incidence of
a prolonged PR interval in pediatric
patients with MIS-C. Previous studies
revealed that patients with a PR
TABLE 2 Laboratory and Diagnostic Findings
Total patients, n
Age, y, median (range)
Male sex, n (%)
ICU admission, n (%)
Progression to advanced AVB, n
(%)
Longest PR interval, ms
Lowest LVEF percentile, median
(IQR)
High-sensitive troponin T, ng/L,
median (IQR)
NT-proBNP, pg/mL, median (IQR)
CRP, mg/dL, median (IQR)
ESR, mm/h, median (IQR)
Procalcitonin, ng/mL, median
(IQR)
Ferritin, ng/mL, median (IQR)
IL-6, pg/mL, median (IQR)
Manual absolute band count
percentile, median (IQR)
D-dimer, mg/mL, median (IQR)
Fibrin, mg/dL, median (IQR)
LDH, U/L, median (IQR)
Albumin, g/dL, median (IQR)
CRP, C-reactive protein; ESR, erythrocyte sedimentation rate; IL-6, interleukin 6; LDH, lactate dehydrogenase; NT-proBNP,
N-terminal pro–brain natriuretic peptide; —, not applicable.
interval .300 milliseconds were
more likely to progress to having
complete AVB from an infectious
etiology process, such as Lyme
disease.16 In our study, 1 patient
developed significant PR prolongation
of 302 milliseconds, which improved
without progression to advanced
AVB. Additionally, AVB in patients
with Lyme carditis and myocarditis
typically resolved within 7 and 5
days, respectively.17,18 In our study,
we found that most patients’ PR
intervals returned back to baseline in
a median of 3 days from the initial
diagnosis of first-degree AVB.
The exact pathogenic mechanism
underlying the development of
conduction abnormalities remains
unknown. In patients with rheumatic
carditis, there is evidence suggesting
molecular mimicry as the etiology of
myocardial injury.19 During an acute
infection (such as group A
Streptococcus), the immune response
leads to production of antibodies or
cytotoxic T cells directed against
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PEDIATRICS Volume 146, number 6, December 2020
which is not regularly seen in
MIS-C Without First- MIS-C With First- P Normal Kawasaki disease.21 More commonly,
Degree AVB Degree AVB Laboratory Values PR interval prolongation is seen in
26 6 — — infections such as Lyme disease.16 In
7.5 (1–20) 11.5 (9–17) — — addition to the first-degree AVB
12 (46) 5 (83) .11 — found in our cohort of patients with
21 (81) 4 (67) .46 — MIS-C, 1 patient developed a new-
0 0 — —
onset RBBB with PR prolongation
140 (80–178) 225 (200–302) ,.01 — during the acute illness phase.
56.5 (48–59) 53.5 (45–57) .32 — Although first-degree AVB is
commonly seen in patients with Lyme
44 (13–88) 89 (49–217) .11 ,14 disease and acute rheumatic fever,
7236 (3117–27 552) 5438 (1809–35 255) .90 10–242
involvement of the bundle branches is
201 (48–300) 211 (163–255) .77 ,0.9 uncommon.22
69 (47–79) 78 (58–90) .48 0–20
1.9 (0.7–16.3) 2.6 (0.8–2.8) .79 ,0.08 At our institution, patients with MIS-C
and first-degree AVB did not progress
595 (344–866) 559 (378–752) .96 13–150 to high-degree AVB. This may be
227 (80–315) 124 (102–315) .85 ,5 explained by the initiation of
4.5 (0–10) 4.5 (0–7) .71 0
immunosuppression, including
3.8 (2.5–8.1) 2.9 (2.2–3.9) .21 ,0.8 glucocorticoids and IVIg early in the
571 (426–680) 709 (660–750) .18 191–430 acute phase of illness. Previous data
373 (285–444) 308 (288–523) .99 140–280 regarding the efficacy of
2.9 (2.5–3.5) 2.6 (2.2–3.5) .50 3.9–5.2 immunosuppression for acquired
AVB are limited. In one study,
a review of the literature indicated
that complete heart block associated
with acute myocarditis resolved in all
human valvular endothelium because
3 children in whom steroids and IVIg
of the antigenic similarities of the
treatment were used.12 Literature has
infectious agent and the glycoproteins
also revealed that glucocorticoids
of cardiac valves.19 This process may
downregulate the activation of the
result in mitral or aortic valvulitis as
proinflammatory response and have
well as pancarditis. A similar
been used to treat congenital heart
pathophysiology of AVB has not yet
block in fetuses and neonates.23,24 We
been clearly established. Cristal
suspect that the early initiation of
et al20 showed that advanced AVB can
high-dose steroids and IVIg treatment
occur in the absence of rheumatic
may have curtailed the inflammatory
carditis, suggesting an alternative
effects on the myocardium and
mechanism of acquired AVB. In this
conduction system and, therefore, the
vein, conduction abnormalities of
progression of first-degree AVB to
MIS-C may be an isolated finding
advanced AVB.
separate from the myocardial injury
documented in patients actively This study is inherently limited by its
infected with SARS-CoV-2.10 retrospective design and small
sample size. Furthermore, the
Although the clinical presentation and diagnosis of MIS-C continues to
conduction abnormalities found in evolve, and the symptoms may also
patients with MIS-C share similarities overlap with other viral illnesses in
with other disease entities, there are pediatric patients, making the
a few notable distinctions. Despite diagnosis challenging.
similar presenting characteristics
with Kawasaki disease, including Although no patients in our study
limbic sparing conjunctivitis and oral progressed to advanced AVB, 1
mucosal changes, patients with MIS-C patient developed significant PR
exhibited a prolonged PR interval, prolongation and 1 patient had new-
5
onset RBBB. Previous studies have
revealed a progression of PR interval
prolongation to advanced AVB in
other infectious or inflammatory
conditions, such as Lyme disease.14,16
It is possible that disease in patients
with MIS-C may theoretically have
progressed to advanced AVB in the
absence of treatment. Given the
relative lack of knowledge and
prospective studies regarding the
MIS-C disease process, conclusions
about the natural history are
necessarily limited. In this vein, all
patients with MIS-C should be
monitored closely during
hospitalization with frequent ECGs
and telemetry monitoring, and follow-
FUNDING: No external funding.
POTENTIAL CONFLICT OF INTEREST: The authors have indicated they have no potential conflicts of interest to disclose.
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This study reveals a 19% prevalence
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associated with MIS-C improved
without progression to advanced
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ABBREVIATIONS
AVB: atrioventricular block
COVID-19: coronavirus disease
2019
ECG: electrocardiogram
IQR: interquartile range
IVIg: intravenous immunoglobulin
LVEF: left ventricular ejection
fraction
MIS-C: multisystem inflammatory
syndrome in children
PCR: polymerase chain reaction
RBBB: right bundle branch block
SARS-CoV-2: severe acute respira-
tory syndrome
coronavirus 2
heart block in children with acute
myocarditis. Pediatr Cardiol. 2003;24(5):
495–497
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with acute rheumatic fever. Pediatr
Cardiol. 2013;34(2):383–389
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7
 MIS-C and Cardiac Conduction Abnormalities
Nak Hyun Choi, Michael Fremed, Thomas Starc, Rachel Weller, Eva Cheung, Anne
Ferris, Eric S. Silver and Leonardo Liberman
Pediatrics 2020;146;
DOI: 10.1542/peds.2020-009738 originally published online November 12, 2020;

Updated Information & including high resolution figures, can be found at:
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References This article cites 21 articles, 3 of which you can access for free at:
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 MIS-C and Cardiac Conduction Abnormalities
Nak Hyun Choi, Michael Fremed, Thomas Starc, Rachel Weller, Eva Cheung, Anne
Ferris, Eric S. Silver and Leonardo Liberman
Pediatrics 2020;146;
DOI: 10.1542/peds.2020-009738 originally published online November 12, 2020;

The online version of this article, along with updated information and services, is
located on the World Wide Web at:
http://pediatrics.aappublications.org/content/146/6/e2020009738

Pediatrics is the official journal of the American Academy of Pediatrics. A monthly publication, it
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