Pediatric myocarditis: presenting clinical characteristics
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American Journal of Emergency Medicine (2009) 27, 942–947
www.elsevier.com/locate/ajem
Original Contribution
Pediatric myocarditis: presenting clinical characteristics
Yamini Durani MD a,⁎, Matthew Egan MD b , Jeanne Baffa MD c ,
Steven M. Selbst MD a , Alan L. Nager MD d,e
a
Division of Emergency Medicine, Department of Pediatrics, Alfred I. duPont Hospital for Children,
Thomas Jefferson University, Wilmington, DE 19899, USA
b
Division of Pediatric Cardiology, Columbus Children's Hospital, Columbus, OH 43205, USA
c
Division of Pediatric Cardiology, Alfred I. duPont Hospital for Children, Thomas Jefferson University,
Wilmington, DE 19899, USA
d
Division of Emergency Medicine and Transport Medicine, Department of Pediatrics, Childrens Hospital Los Angeles,
Los Angeles, CA 90027, USA
e
Keck School of Medicine of the University of Southern California, Los Angeles, CA 90089, USA
Received 23 June 2008; revised 23 July 2008; accepted 24 July 2008
Abstract
Objective: The objective of the study was to characterize the clinical profiles of pediatric patients with
acute myocarditis and dilated cardiomyopathy (DCM) before diagnosis.
Methods: A retrospective cross-sectional study was conducted to identify patients with myocarditis and
DCM who presented over a 10-year span at 2 tertiary care pediatric hospitals. Patients were identified
based on the International Classification of Diseases, Ninth Revision, diagnostic codes.
Results: A total of 693 charts were reviewed. Sixty-two patients were enrolled in the study. Twenty-four
(39%) patients had a final diagnosis of myocarditis, and 38 (61%) had DCM. Of the 62 patients initially
evaluated, 10 were diagnosed with myocarditis or DCM immediately, leaving 52 patients who required
subsequent evaluation before a diagnosis was determined. Study patients had a mean age of 3.5 years,
47% were male, and 53% were female. Common primary complaints were shortness of breath,
vomiting, poor feeding, upper respiratory infection (URI), and fever. Common examination findings
were tachypnea, hepatomegaly, respiratory distress, fever, and abnormal lung examination result. Sixty-
three percent had cardiomegaly on chest x-ray, and all had an abnormal electrocardiogram results.
Conclusions: These data suggest children with acute myocarditis and DCM most commonly present
with difficulty breathing. Myocarditis and DCM may mimic other respiratory or viral illnesses, but
hepatomegaly or the finding of cardiomegaly and an abnormal electrocardiogram result may help
distinguish these diagnoses from other more common pediatric illnesses.
© 2009 Elsevier Inc. All rights reserved.
1. Background
Myocarditis, the inflammation of the muscular walls of
This article was presented, in part, at the Pediatric Academic Societies
Meeting in San Francisco, April 2006.
the heart, remains a diagnostic challenge in the clinical
⁎ Corresponding author. Tel.: +1 302 651 4296; fax: +1 302 651 4227. setting because of the variability of presentations in the
E-mail address: ydurani@nemours.org (Y. Durani). pediatric population. It is nonetheless an important
0735-6757/$ – see front matter © 2009 Elsevier Inc. All rights reserved.
doi:10.1016/j.ajem.2008.07.032Pediatric myocarditis: presenting clinical characteristics 943
diagnosis, as it is the most common etiology of heart failure The institutional review boards of both participating
in previously healthy pediatric patients [1]. The initial hospitals approved the study.
diagnosis of myocarditis is highly dependent upon clinical Children up to 18 years old who were identified as having
suspicion because diagnosis based on endomyocardial myocarditis or DCM based on the International Classifica-
biopsy has many inherent risks and is therefore not tion of Diseases, Ninth Revision, codes were eligible for the
performed routinely. Unless a high index of suspicion is study. Only patients diagnosed with DCM secondary to acute
maintained, acute myocarditis may easily be missed; and the myocarditis were included in the study. Patients with DCM
diagnosis may only be obvious in cases when fulminant secondary to other causes such as cardiotoxic drugs, inborn
disease is present. errors of metabolism, malformation syndromes, neuromus-
Patients often present with prodromal symptoms that cular disorders, or other familial syndromes were excluded.
are not recognized to be associated with myocarditis In all cases, the final diagnosis was based upon expert
initially. In a study of 90 patients younger than 16 years opinion of a pediatric cardiologist.
who died suddenly and unexpectedly, myocarditis was A standardized data collection form was used to abstract
found to be a major cause of death in 17%; and 60% of data from hospital medical records. Data were abstracted by
these patients had prodromal symptoms [2]. In another 3 investigators. Data collected included demographics,
study by Freedman et al of 14 patients seen by a clinical history, physical examination, and results of
physician before the diagnosis of myocarditis, 57% were laboratory evaluation.
originally diagnosed as having pneumonia or asthma. In The clinical history and physical examination data were
addition, 32% of patients presented with respiratory obtained from the first documented encounter at our
symptoms, 29% had cardiac symptoms, and 6% had institutions' EDs. If patients were transferred to our facilities
gastrointestinal symptoms. from an outside institution and did not have an ED
Previous research has shown that acute myocarditis may evaluation, the historical and clinical data were collected
progress to dilated cardiomyopathy (DCM). This occurs as from intensive care unit records or the referring hospital's
myocytes are injured by both direct viral injury and by the initial medical evaluation.
inflammatory response of the host via the effects of The presence or absence of the following clinical features
cytokines, autoantibodies, macrophages, natural killer cells, was collected: fever, diaphoresis, lethargy, fatigue, change in
and lymphocytic cells [3,4]. Although DCM may result from exercise tolerance, syncope, seizures, difficulty breathing,
other etiologies, such as neuromuscular disorders, inborn rapid breathing, cyanosis, wheezing, apnea, cough, rhinor-
errors of metabolism, or other familial syndromes, a recent rhea, chest pain, palpitations, poor feeding, vomiting,
study demonstrated that 27% of cases of DCM were diarrhea, abdominal pain, and decreased urination. Physical
secondary to viral myocarditis [5]. In this study, we have examination findings collected included triage or initial vital
selected cases of myocarditis and DCM that are only signs and the presence or absence of the following:
presumed to be viral in etiology. We also chose to group respiratory distress, evidence of upper respiratory tract
the spectrums together because ultimately the support and infection, abnormal lung examination results (wheezing,
treatment are the same for both. retractions, rales, decreased air exchange), gallop, murmur,
Characterizing signs and symptoms of patients with hepatomegaly, perfusion/pulses, and cyanosis. If no doc-
acute myocarditis and DCM could possibly facilitate umentation existed regarding a specific sign, symptom,
earlier diagnosis of the disease and help prevent medications, or other aspects of the history, it was recorded
misdiagnosis. The primary objective of this study is to as “not documented.”
characterize the clinical profiles of pediatric patients with Initial laboratory findings that were abstracted included
acute myocarditis and DCM at the time of presentation to complete blood count, C-reactive protein (CRP), erythrocyte
the hospital. A secondary objective is to review these sedimentation rate (ESR), troponin, and creatinine kinase
patients' initial diagnoses early in the course of their (CK). Microbiology results were also abstracted, such as
disease and to analyze cases that were initially diagnosed blood cultures, tracheal aspirate, nasal swab cultures, urine
as some other condition before myocarditis or DCM cultures, endomyocardial biopsy results, and more specific
was considered. viral testing. The findings of the initial chest x-ray (CXR),
electrocardiogram (EKG), and echocardiogram were
abstracted. The results of these tests were based on reported
data in the medical record.
2. Materials and methods If patients had medical evaluations by a physician in the
14 days preceding final diagnosis of myocarditis or DCM,
A retrospective cross-sectional study was conducted to the diagnoses given at these encounters were abstracted.
identify patients with myocarditis and DCM who presented SPSS for Windows version 14.0 (SPSS Inc, Chicago, IL)
over a 10-year span from January 1, 1994, to December 31, [6] was used for data analysis. Descriptive statistics were
2003, at 2 tertiary care pediatric centers with annual used to describe patient characteristics and frequencies of
emergency department (ED) visits of 35 000 and 62 000. signs, symptoms, and diagnoses.944 Y. Durani et al.
3. Results Table 2 Identified viral pathogens
Specific viral pathogens No. of patients
A total of 693 charts were reviewed at the 2 participating
(n = 62)
institutions. Six hundred twenty-eight patients were
excluded because their heart disease was not myocarditis No pathogens identified 42 (68%)
or DCM, their heart disease was secondary to another Parainfluenza 8 (13%)
Coxsackie 4 (6%)
primary diagnosis (eg, muscular dystrophy, metabolic
Adenovirus 2 (3%)
disorder), or their heart disease was caused by medications. Influenza A 2 (3%)
Three patients were excluded secondary to incomplete Parvovirus 1 (2%)
medical records, resulting in 62 patients available for data Coinfections 3 (5%)
analysis: 24 patients from one institution (AI duPont) and 38 Echovirus, coxsackie B 1 (2%)
patients from the second institution (Childrens Hospital Los Influenza A and B, adenovirus 1 (2%)
Angeles). Twenty-four (38%) patients had a final diagnosis Coxsackie A, adenovirus 1 (2%)
of myocarditis, and 38 (61%) had DCM. Patients with known pathogen (%) 32%
As depicted on Table 1, study patients had a mean age of
3.5 years and a range from 6 days to 17 years. Forty-seven
percent were male, and 53% were female. Regarding race,
29% were African American; 29%, Hispanic; 14%, white; (32%) patients had 2 or 3 evaluations (18 with 2 visits, and
10%, Asian/Pacific Islander; 8%, other; and 10%, not 2 with 3 visits) before myocarditis or DCM was diagnosed.
documented. The mean duration of symptoms, before final Table 3 shows data regarding diagnoses for the 52 patients
diagnosis, was 7.6 days (SD ± 13 days). Thirty-nine percent at their first evaluation by a physician. A respiratory tract
of patients were diagnosed with myocarditis, and 61% were infection was diagnosed in 13 (25%) patients, including
diagnosed with DCM. In total, 8 (13%) patients died; and 54 pneumonia, bronchiolitis, and upper respiratory tract
(87%) survived. As shown on Table 2, a documented viral infection. Cardiac disease was diagnosed in 8 (15%)
pathogen was found in 20 (32%) of study patients, with patients, including cardiomegaly, arrhythmia, myocardial
parainfluenza being the most common pathogen found. infarction, and myocarditis. Four patients had combined
Sixty-two patients were initially evaluated during this diagnoses, with pneumonia/cardiomegaly in 3 patients and
analysis. Ten patients were diagnosed with myocarditis or congenital heart disease/cardiomegaly in 1 patient. Other
DCM at the first encounter at our respective institutions, diagnoses were given to 21 (40%) patients, and data were
resulting in 52 patients who required subsequent evalua- missing or not available for 6 (12%) patients. All patients
tions by a physician before a definitive diagnosis was who were suspected of having cardiac disease at the first
determined. Of these 52 patients, 32 (52%) patients had 1 visit were either diagnosed in our EDs or referred to our
additional evaluation within 14 days of symptoms. Twenty ED the first day the diagnosis was suspected, and all were
admitted to the hospital.
Table 4 lists the diagnoses of patients evaluated during the
Table 1 Characteristics of study patients second visit to a physician. A respiratory tract infection was
Patient characteristics No. of patients diagnosed in 5 (25%) patients, all of whom had pneumonia.
(n = 62)
Sex Table 3 Diagnoses at first medical evaluation
Male 29 (47%)
Specific diagnosis No. of patients
Female 33 (53%)
(n = 52)
Mean age (y) 3.5 y (SD ± 5.0)
Race Respiratory infection 13 (25%)
African American 18 (29%) Pneumonia 3 (6%)
Hispanic 18 (29%) Bronchiolitis 5 (10%)
White 9 (14%) Upper respiratory tract infection 5 (10%)
Asian/Pacific Islander 6 (10%) Cardiac disease 8 (15%)
Other 5 (8%) Cardiomegaly 4 (8%)
Not documented 6 (10%) Arrhythmia 2 (4%)
Mean duration of symptoms (d) 7.6 d (SD ± 13.0) Myocardial infarction 1 (2%)
Final diagnosis Myocarditis 1 (2%)
Myocarditis 24 (39%) Combined diagnoses 4 (8%)
DCM 38 (61%) Pneumonia/cardiomegaly 3 (6%)
Outcome Congenital heart disease/cardiomegaly 1 (2%)
Died 8 (13%) Other diagnoses 21 (40%)
Survived 54 (87%) Diagnosis not documented 6 (12%)Pediatric myocarditis: presenting clinical characteristics 945
Table 4 Diagnoses at second medical evaluation Table 6 Major findings on laboratory and radiographic
analysis
Specific diagnosis No. of patients
(n = 20) Mean WBC count ([×1000]/mm3) 11.4 (SD ± 5.4)
Respiratory infection 5 (25%) Elevated troponin 7/13 (54%)
Pneumonia 5 (25%) Elevated CK 16/22 (73%)
Cardiac disease 4 (20%) Elevated ESR 6/16 (38%)
Cardiomegaly 2 (10%) Elevated CRP 4/15 (27%)
Myocarditis 1 (5%) Abnormal EKG 59/59 (100%)
Congenital heart disease 1 (5%) Sinus tachycardia 27 (46%)
Combined diagnoses 2 (10%) Ventricular hypertrophy 24 (41%)
Pneumonia/DCM 1 (5%) ST wave abnormality 19 (32%)
T wave abnormality 18 (31%)
Pneumonia/cardiomegaly 1 (5%)
Other diagnoses 5 (25%) Bundle-branch block 6 (10%)
Diagnosis not documented 4 (20%) Arrhythmia 4 (7%)
AV block 3 (5%)
Prolonged QT interval 3 (5%)
Abnormal CXR 53/59 (90%)
Cardiac disease was diagnosed in 4 (20%) patients. Two Cardiomegaly 37 (63%)
patients had combined diagnoses, with pneumonia/DCM in 1 Pulmonary edema 9 (15%)
patient and pneumonia/cardiomegaly in 1 patient. Other Pulmonary infiltrate 3 (5%)
diagnoses were given to 5 (25%) patients, and data were Pleural effusions 1 (2%)
missing or not available for 4 (20%) patients. Other abnormality 3 (5%)
Of the 52 patients who were seen for their first medical Abnormal echo 60/61 (98%)
evaluation before a final diagnosis, 21 (40%) patients were WBC indicates white blood cell; AV, atrioventricular.
seen by their primary care provider, 21 (40%) were evaluated
in a general ED, 2 (4%) were cared for in a pediatric ED, and
8 (15%) were seen in other settings (clinics, neonatal units, Many of the patients studied had frequent and overlapping
etc). Of the 20 patients who were seen at a second medical signs and symptoms at the time they were diagnosed with
evaluation (including 18 who had 2 evaluations and 2 myocarditis or DCM. For the 62 patients studied, Table 5
patients who had 3 evaluations) before final diagnosis, 7 lists various common symptoms and clinical findings. At the
(35%) were cared for by their primary care provider, 7 (35%) time of presentation to our institutions, 43 (69%) patients had
were seen in a general ED, 2 were evaluated in a pediatric a history of shortness of breath, 30 (48%) had vomiting, 25
ED, and 4 (20%) were seen in other areas. (40%) presented with poor feeding, 24 (39%) showed upper
respiratory symptoms, 22 (36%) had fever, and 22 (36%)
presented with lethargy. On physical examination, 37 (60%)
Table 5 Symptoms and physical examination findings patients had clinical evidence of tachypnea, 31 (50%) had
Specific symptoms and physical No. of patients
hepatomegaly, 29 (47%) patients had respiratory distress, 22
examination findings (n = 62) (36%) patients presented with fever, and 21 (34%) patients
had an abnormal lung examination result.
Most common presenting symptoms
A normal heart rate for age [7] was found in 41 (66%)
Shortness of breath 43 (69%)
patients studied. Of the 20 patients with tachycardia, 9 (45%)
Vomiting 30 (48%)
Poor feeding 25 (40%) were febrile and 11 (55%) were afebrile. In addition, 1
Upper respiratory symptoms 24 (39%) afebrile patient was bradycardic. Heart rates were based on a
Fever 22 (36%) single measurement in triage or the first available vital signs
Lethargy 22 (36%) at the time of encounter at our institution.
Most common physical examination findings Table 6 shows laboratory data, abnormalities found on
Tachypnea 37 (60%) CXR, EKG abnormalities, and results of echocardiography.
Hepatomegaly 31 (50%) The mean white blood cell count of patients was 11 400 (SD ±
Respiratory distress 29 (47%) 5.4; range, 4100-34 200). Only 13 patients had a troponin
Fever 22 (36%) level checked; and of these, 7 (54%) had an elevated level.
Abnormal lung exam 21 (34%)
Twenty-two patients had a CK checked; and of these, 16
Heart rate findings
(73%) were elevated. Six patients had an elevated ESR, and
Normal heart rate 41 (66%)
Tachycardia 20 (32%) 4 patients had an elevated CRP.
Febrile and tachycardic 9 (45%) An abnormal EKG was documented in 59 of 59
Afebrile and tachycardic 11 (55%) (100%) patients, with no EKG on 3 patients. The most
Bradycardia 1 (2%) common abnormal EKG finding was sinus tachycardia,
with the next most common EKG abnormality demon-946 Y. Durani et al.
strating evidence of ventricular hypertrophy followed by diagnoses in patients with mild respiratory symptoms,
ST-wave abnormality. An abnormal CXR was documen- respiratory distress, or unexplained shock.
ted in 53 of 59 (90%) patients. In addition, 6 (10%) had a Although many clinicians believe resting tachycardia is a
normal CXR and 3 patients had no CXR. The most common finding in patients with myocarditis, this study
common abnormal CXR finding was cardiomegaly in 37 found that 66% of patients had a normal heart rate for age. In
(60%) patients, followed by pulmonary edema and addition, the heart rate did not appear to be related to fever. It
pulmonary infiltrate. An abnormal echocardiogram was is our speculation that sequential vital signs to measure
found in 60 of 61 (97%) patients. One patient had a trends in the heart rate may be more helpful in future studies.
normal echocardiogram, and 1 patient died in the ED and A single heart rate measurement, therefore, may not be a
had no echocardiogram performed. The patient with a useful objective marker of myocarditis.
normal echocardiogram result was diagnosed with Most cases of myocarditis or DCM were not initially
myocarditis by a cardiologist based on a clinical picture recognized by either a primary care provider or a general
of respiratory distress, upper respiratory tract infection, emergency medicine health care provider. Of the 62 patients
positive viral culture, and cardiac arrhythmia consisting initially analyzed, 52 (84%) required more than 1 visit to a
of premature atrial contractions. The patient who died and physician within 14 days before the diagnosis of myocarditis
had no echocardiogram performed was diagnosed with a or DCM was made. Overall, most patients were initially
probable myocarditis because of evidence of heart failure diagnosed with a respiratory illness.
on CXR and cardiac arrhythmia that progressed to cardiac Although myocarditis and DCM may mimic other
arrest. The patient's cardiac rhythm was obtained from a respiratory or viral illnesses, findings on physical
cardiorespiratory monitor tracing; and the patient initially examination such as hepatomegaly should not be over-
had a narrow QRS complex with peaked T waves that looked; and the finding of cardiomegaly on CXR should
changed to a widened QRS complex, resulting eventually help distinguish these diagnoses from other more common
in cardiac arrest. pediatric respiratory illnesses. In addition, although not
A myocardial biopsy was performed in 6 patients, and apparent in our study, several case reports have included
findings consistent with myocarditis were found in 5; 1 seizures as the inciting event, along with other cardiac
patient had an insufficient sample. signs and symptoms that led to the diagnosis of
myocarditis [10,11]. Therefore, this variability in signs
and symptoms, especially when they are associated with
cardiac or radiographic findings, should alert the clinician
4. Discussion to assess for myocarditis or DCM.
Our study is similar to a previously published study by
This study has identified prodromal symptoms and signs Freedman et al, who examined signs and symptoms along
associated with myocarditis and DCM in a diverse pediatric with CXR and EKG findings in patients with myocarditis.
population. Myocarditis and DCM may vary from mild to Although the 2 studies were similar with regard to the
fulminant disease. In milder cases, diagnosis at initial predominance of respiratory and gastrointestinal symptoms,
presentation may be challenging. However, because of the our study had a higher percentage of patients with
potential for severe and fatal disease, it is important to respiratory complaints. In addition, our study demonstrated
identify myocarditis and DCM early, so that monitoring and that 50% of patients at the time of diagnosis had
supportive treatment can be timely. hepatomegaly vs 36% in the study of Freedman et al.
Most patients in this study population presented with Regarding CXR evaluation, our study demonstrated that
complaints of shortness of breath and were found to have 60% of patients had evidence of cardiomegaly (vs 55%);
tachypnea with associated respiratory distress and an and 95% of patients with myocarditis in our study had an
abnormal lung examination result. This is consistent with abnormal EKG (vs 93%) [3].
a case series of 7 myocarditis patients who all presented Although the results of our studies differ to a small
with respiratory distress, including tachypnea and inter- degree regarding clinical signs and symptoms (respiratory
costal retractions. In this series of patients, initial and gastrointestinal), such symptoms along with CXR and
diagnoses included asthma, pneumonia, congestive heart EKG findings ultimately led to the same cardiac diagnosis
failure, rule-out sepsis, and shock [8]. Although all of the in both studies.
patients in the study progressed and developed worsening As demonstrated in our study, several laboratory tests
symptoms, they nonetheless all started out with respiratory were obtained in a relatively small proportion of patients.
symptoms, similar to most of the patients in our study It has been postulated that troponin levels may provide the
population. In another case series of 4 patients, all best evidence of myocyte injury in patients with
presented with the acute onset of severe respiratory myocarditis [12]. Our study, however, demonstrated that
distress, leading to shock; and all were subsequently only 7 of 13 patients tested had a positive result. This
diagnosed with myocarditis [9]. Therefore, a cardiac small sample size does not allow us to draw the conclusion
etiology should be considered among the differential that this should be a mandatory laboratory test in thePediatric myocarditis: presenting clinical characteristics 947
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