key: cord-0726830-505iraz6
authors: Brito, Daniel; Meester, Scott; Yanamala, Naveena; Patel, Heenaben B.; Balcik, Brenden J.; Casaclang-Verzosa, Grace; Seetharam, Karthik; Riveros, Diego; Beto, Robert James; Balla, Sudarshan; Monseau, Aaron J.; Sengupta, Partho P.
title: High Prevalence of Pericardial Involvement in College Student-Athletes Recovering From COVID-19
date: 2020-11-04
journal: JACC Cardiovasc Imaging
DOI: 10.1016/j.jcmg.2020.10.023
sha: a00ba580d4cd29bdd0ddd900bfaa095fa1dca7b6
doc_id: 726830
cord_uid: 505iraz6

Objectives We sought to explore the spectrum of cardiac abnormalities in student-athletes who returned to university campus in July 2020 with an uncomplicated Coronavirus disease 2019 (COVID-19). Background There is limited information regarding cardiovascular involvement in young individuals with mild or asymptomatic COVID-19. Methods Screening echocardiograms were performed in 54 consecutive student-athletes (mean age: 19 years, 85% males) who tested positive on reverse transcription–polymerase chain reaction nasal swab testing of the upper respiratory tract or IgG antibodies against SARS-CoV-2. A sequential cardiac magnetic resonance (CMR) imaging was performed in 48 (89%) subjects. Results A total of 16 (30%) athletes were asymptomatic while 36 (66%) and 2 (4%) reported mild and moderate COVID-19 related symptoms, respectively. For the 48 athletes completing both imaging studies, abnormal findings were identified in 27 (56.3%) individuals. This included 19 (39.5%) showing pericardial late enhancements with associated pericardial effusion. Of the individuals with pericardial enhancements, 6 (12.5%) had reduced global longitudinal strain (GLS) and/or an increased native T1. One patient showed myocardial enhancement and reduced left ventricular ejection fraction or reduced GLS with or without increased native T1 were also identified in additional 7 (14.6%) individuals. Native T2 were normal in all subjects and no specific imaging features of myocardial inflammation were identified. Hierarchical clustering of LV regional strain identified three unique myopericardial phenotypes that showed significant association with the CMR findings (P=0.03). Conclusion Over one in three previously healthy college-athletes recovering from COVID-19 infection showed imaging features of a resolving pericardial inflammation. Although subtle changes in myocardial structure and function were identified, no athlete showed specific imaging features to suggest an ongoing myocarditis. Further studies are needed to understand the clinical implications and long-term evolution of these abnormalities in uncomplicated COVID-19.

Myocardial injury with an elevated troponin level may occur in 7-17% of patients hospitalized with Coronavirus disease 2019 and is present in 22-31% of those admitted to the intensive care unit (1) (2) (3) . While the mechanisms of myocardial injury are diverse, the clinical differentiation of Coronavirus-2 (SARS-CoV-2) related myocarditis from other forms of myocardial dysfunction caused by hypoxia, inflammatory storm or a stress-cardiomyopathy like presentation remains challenging. More recently, imaging studies have found changes in left and right ventricular structure and function in COVID-19 that can persist beyond the acute stage into several weeks and months of recovery (4) . The immediate and long-term effects of these findings are unknown and warrant immediate scientific scrutiny.

With the infection's rapid spread throughout the community and the recent upsurge in COVID-19 in younger individuals, there is a potential need to understand the prevalence of any undiagnosed COVID-19 related cardiovascular involvement. Specifically, there is limited information regarding cardiac involvement amongst student-athletes with mild or asymptomatic COVID-19 infection (5) . This may be relevant for young college students and athletes who may be at a higher risk for sports and exercise related arrhythmias and cardiac dysfunction in the presence of underlying COVID-19 related myocardial injury. Therefore, our study aimed to investigate and determine the range of cardiac abnormalities seen in young athletes who were diagnosed with mild or asymptomatic COVID-19 infection after returning to college campus in July 2020. Using comprehensive echocardiography and cardiac magnetic resonance (CMR) imaging, we further investigated if the pattern of echocardiographic involvement, including strain, could be associated with the COVID-19 related cardiac involvement observed on CMR.

This cross-sectional observational study analyzed the data collected from college studentathletes who returned to West Virginia University, Morgantown campus for the fall 2020 semester and were found to have COVID-19. A total of 160 athletes were tested between June 12 and August 4, 2020 ( Figure 1 ). Initially, screening for COVID-19 by serum IgG antibody and nasopharyngeal (NP) swab testing for SARS-CoV-2 by real-time polymerase chain reaction (PCR) was performed on all athletes. IgG antibody testing was performed using a high throughput chemiluminescent microparticle immunoassay (CMIA) with an ARCHITECT i2000SR immunoassay analyzer (6) . The Sports Medicine Team at West Virginia University installed a monitoring protocol for the athletes using a smartphone-developed application for recognizing COVID-19 related symptoms as defined by CDC (7) . This questionnaire included the following symptoms: fever or chills, cough, shortness of breath, new onset of anosmia, fatigue, muscle or body aches, headache, sore throat, nasal congestion, nausea, vomiting and/or diarrhea. In addition, athletes who initially tested negative were re-tested on a weekly basis by NP swab for SARS-CoV-2 by real-time PCR. Troponin-I was added to the panel of screening test on all COVID-19 positive athletes and additional tests like CRP, ESR and BNP were evaluated as needed during individualized clinical assessments.

Following appropriate quarantine period, ECG and comprehensive echocardiography were recommended in all subjects of whom 54 underwent the tests. In addition, all subjects who had symptomatic COVID-19 (n=38) (Figure 1 ), and any asymptomatic (n=16) subject with an abnormal ECG, or an abnormal echocardiogram (i.e., abnormal GLS<16% or LV ejection fraction <50% or diagnostic uncertainty with echocardiographic features of RV dilation and/or RV dysfunction) underwent CMR imaging. We received exemption status from the Institutional J o u r n a l P r e -p r o o f Review Board of the West Virginia School of Medicine and followed guidelines issued by the Health Insurance Portability and Accountability Act Regulations, with all information collected from the electronic medical records (EMR) after the patient's visit. Our research was performed within the ethical guidelines by the declaration of Helsinki of 1975 (8).

Two-dimensional and Doppler echocardiographic examinations were performed using GE Vivid E9 or Philips Epiq 7 imaging systems equipped with 2.5MHz and non-imaging transducers. Standard views were acquired, and right and left cardiac chamber quantification was performed according to the American Society of Echocardiography (ASE) guidelines (9,10). The cutoff values for LV dysfunction (<50%) and right ventricle (RV) dysfunction (RV fractional shortening < 35%) were based upon recommended guidelines (11,12).

Speckle tracking analysis was performed in accordance with the ASE recommendations using offline vendor-free software (ImageArena, TomTec Inc.). Longitudinal strain was measured in all three views: apical four-, three-and two-chamber views. The peak global longitudinal strain (GLS) and regional longitudinal systolic strain were described using the 16segment model. For LV GLS, an absolute magnitude lower than 16% was considered abnormal (12). The free wall of the RV was separated into 3 segments which included the basal, mid, and apical regions. The strain value was calculated as the mean of the strain values present in the 3 segments and an absolute value lower than 20% was considered abnormal (9,13).

J o u r n a l P r e -p r o o f Cardiac Magnetic Resonance Imaging CMR was acquired on a 1.5 T magnet (Magnetom Aera, Siemens Medical Systems, Erlangen, Germany). Conventional sequences were obtained for imaging of cardiothoracic anatomy with axial stack of black blood using fast spin echo (FSE). Imaging for cardiac function, mass, and volume was performed using balanced steady state free precession (SSFP) cine imaging. Tissue characterization of LV was performed with edema imaging, T1 mapping, T2 mapping and late Gadolinium enhancement imaging. Edema imaging was performed using T2-weighted dark blood short tau inversion recovery sequence (STIR). The acquired T1 mapping was performed using the Shortened Modified Look Lockers Inversion (ShMOLLI) recovery sequence pre-contrast on three short axis slices at the base, mid and apical LV, the same location as STIR images. T2 map was performed using steady-state free-precession imaging with three different T2 preparation times at the same locations as STIR images and T1 maps (14) . Late Gadolinium imaging was performed 8-12 minutes after administration of contrast agent (0.1 mmol/kg of Gadavist™ Gadobutrol, Bayer Healthcare, USA) (15) .

Image analysis for LV volumes and function was performed using Vitrea software (Vital Images Inc. Minnetonka, Minnesota). Analysis of the short axis images of T1 map, T2 map and T2 weighted images was performed as detailed below. T2 weighted images were visually assessed for hyperintense areas. Analysis was performed to diagnose edema when myocardial T2 SI (signal intensity) ratio was ≥2:1 compared to that of skeletal muscle. Motion corrected native T1 images were post processed using Vitrea software. To assess diffuse disease, a region of interest (ROI) was drawn in the septum at the mid or basal cavity (if mid cavity images were technically J o u r n a l P r e -p r o o f inadequate) in a short-axis image of the LV in all patients for myocardial T1 assessments (16) .

Previously published native T2 value of over 52 ms was considered abnormal (17) . The estimated normal reference range and cut-off values for normal native T1 was determined by using an age-matched group of 16 healthy individuals (Supplementary Table 1 ). Based on this data, a T1 value of ≥ 990 ms was considered abnormal. Previous studies have suggested that the native T1 values in age-matched healthy controls are slightly higher than in athletes (30) and therefore any values higher than those obtained in age-matched healthy controls can be considered as abnormal.

In addition to the above, parametric maps and segmental native T1 relaxation times for the 16 myocardial segments were obtained by post processing the three short axis slices to assess regional pathology (cvi42, Circle Cardiovascular Imaging, Canada). Care was taken to avoid blood pool contamination when contouring the epicardial and endocardial borders. For T2 mapping, the endocardium and epicardial contouring was performed for the basal and mid ventricular short axis slices. Apical slice was disregarded and segments with artifacts were also excluded. NativeT2 relaxation time per segment was quantitated on the motion corrected images using cvi42 software (Circle Cardiovascular Imaging, Canada). Imaging for myocardial scar and pericardial involvement was performed using late gadolinium enhancement technique at the same location as cine images. Late enhancement was qualitatively assessed visually. Pericardial enhancement was considered if there was involvement of the pericardial layers and was confirmed by two observers. T1 map and SSSP cine images were used to carefully differentiate fat tissue from pericardial enhancement (Supplemental videos 1 -3).

J o u r n a l P r e -p r o o f CMR features specific to myocardial inflammation required the presence of at least one T2 criteria (global or regional increase of myocardial T2 relaxation time or an increased signal intensity in T2-weighted CMR images) and one T1 criteria (an increased myocardial T1, or late gadolinium enhancement) (18) . In addition, the abnormalities seen on echocardiography and CMR were integrated and adjudicated as: 1) pericardial: defined as the presence of late enhancement with pericardial effusion on CMR, 2) myocardial: presence of any of the following criteria in isolation or in a combination: (a) LV EF % less than 50%, (b) presence of regional wall motion abnormality, (c) GLS < 16% and (d) native T1 increase ≥ 990 ms, and 3) myopericardial: a combination of 1 and 2.

As a first step, we performed the Shapiro-Wilk test to check if the data were normally distributed across different groups. We found that most of the variables were not normally distributed; therefore, we employed non-parametric methods for all statistical analysis. Continuous data were expressed as the median (interquartile ranges, IQRs). Categorical data are presented as counts (percentages). Comparisons of continuous variables of demographics, echocardiography and CMR between different groups (i.e., controls, symptomatic-and asymptomatic COVID-19 positive student-athletes) were performed either using Kruskal-Wallis test with Dunn-Bonferroni correction or Mann-Whitney U test. A chi-square was used for categorical variable with an expected value for each cell to be 5 or greater. If this assumption was not met, a Fischer's test was used. To investigate the relationship between regional strain and CMR, hierarchical cluster analysis (HCA) was performed to identify relationships among the sixteen segmental longitudinal strains that might otherwise remain undiscovered (additional details are presented in J o u r n a l P r e -p r o o f supplementary methods section). All statistical analysis were performed using Medcalc for Windows, version 19.5.2 (MedCalc Software, Ostend, Belgium) and RStudio version 3.1.3 (Vienna, Austria). Statistical significance less than <0.05 was used for all tests.

A total of 160 student-athletes were screened for COVID-19 of whom fifty-three (33.1%) tested positive on PCR, while a total of 7 (4.3%) athletes tested positive for IgG antibodies against SARS-CoV-2 ( Figure 1 ). A total of 4 (2.5%) individuals were positive by both PCR and IgG antibodies. By August 9, 2020, a total of 54 college level athletes with COVID-19 had undergone imaging studies ( Table 1 ). The median time-interval from tests performed to the imaging assessment was 27 (22 to 33) days. Overall, the median age was 19 years (range: 19 -21 years) and more than 85% of the cohort were male. A total 36 (66%) and 2 (4%) individuals experienced mild and moderate COVID-19 related symptoms respectively; however, the illness was self-limited, and none of the participant required hospitalization (19) . The remaining 16 (30%) athletes reported no symptoms at the time of COVID-19 screening.

Nearly a quarter of the symptomatic COVID-19 patients also experienced cardiac symptoms (shortness of breath, fatigue, chest pain, or lightheadedness) while only 1 (6%) of the patients with no specific COVID-19 symptoms as defined by the CDC guideline (7) subsequently reported a single episode of chest pain during the quarantine period. Cardiac Troponin-I levels were normal except in one symptomatic patient (Table 1) .

Cardiac wall and cavity dimensions, volume, LV mass index, and LVEF were similar in asymptomatic and symptomatic groups ( Table 2) . Symptomatic COVID-19 student-athletes had J o u r n a l P r e -p r o o f significantly lower septal e' (P=0.008 vs asymptomatic) and average e' (P=0.014 vs asymptomatic) but not significantly lower lateral e' velocities (P=0.07). However, despite the significant group differences, it is important to note that these values are mostly within normal range for athletes and the general population. One symptomatic patient had EF < 50% with global hypokinesis (11). A total of four (11%) and two (13%) patients from the symptomatic and asymptomatic groups had reduced GLS respectively. There were no significant differences in the GLS or RV strain ( Table 2 ). Small pericardial effusions (≥5mm) were detected in three individuals. The importance of the described echocardiographic findings in COVID-19 infected student-athletes is underlined by the comparison of age-matched athletic controls (n = 20)

showing normal findings of LV structure/function in otherwise healthy non-infected athletes ( Table 2) .

A total of 48 subjects underwent CMR. This included all symptomatic COVID-19 except one subject who could not complete CMR due to claustrophobia (n=37, Figure 1 ). A total of 11 asymptomatic subjects underwent CMR, this included one subject with abnormal ECG (inappropriate sinus tachycardia with ST&T-wave changes), and two with echocardiographic impaired LV function (abnormal GLS <16% or EF < 50%); and eight with borderline RV dilation/ dysfunction on echocardiography (n=8) necessitating CMR for overcoming diagnostic uncertainty.

Consistent with echocardiographic findings, no significant differences were noted between symptomatic and asymptomatic COVID-19 athletes (Table 3) 

The central illustration shows the overall prevalence of cardiac abnormalities as identified using echocardiography and CMR in 27 (56.3%) out of 48 individuals. The frequency of abnormalities seen in the individual modality are shown in Supplementary Table 2. In these 27 individuals, the most common involvement was pericardial disease with pericardial enhancement seen in 13 (48%) individuals. Specific CMR signs of myocardial inflammation (both T1 and T2 criteria) was not seen in any subject. A total of 6 (22.2%) subjects with pericardial enhancement also showed additional myocardial abnormalities (GLS < 16%, n=2 or native T1 increase ≥ 990 ms, n=3 or combination of both, n=1)). Isolated myocardial involvement was seen in 8 (29.6%) subjects (one with LV EF < 50%, two with GLS < 16%, four with raised T1, and one with GLS<16%, myocardial enhancement and raised T1, respectively).

To understand the association between echocardiography strain abnormalities and CMR we performed unsupervised hierarchical clustering. A model based on 16 segmental longitudinal strain grouped patients into three major clusters ( Figure 6 ). A phenotypic group on the left of the dendrogram (Group A: diffuse myopericardial involvement) clustered nine patients with widespread reduction in regional longitudinal strains. The phenotypic distribution of CMR J o u r n a l P r e -p r o o f findings in Group A was significantly different from the rest of the dendrogram (p=0.03). The phenotypic group on the right of the dendrogram clustered 27 patients of whom 9 (33%) had pericardial enhancement (Group B: mild myopericardial involvement) with reduction in their regional longitudinal strain but preserved overall LV GLS. The remaining patients in the center (Group C: mild pericardial involvement) included 11 patients with pericardial abnormalities seen in 4 (36%) cases. Supplementary Figure 2 shows the correlations between CMR derived segmental T1 and speckle-tracking echocardiography derived segmental longitudinal strain.

To the best of our knowledge, this is the first study to use comprehensive echocardiography with speckle tracking strain and CMR together to explore the spectrum of cardiac involvement in college student-athletes who recovered from uncomplicated COVID-19.

Abnormal findings on cardiac imaging was seen in over half of the patients with a majority (39.5%) having pericardial late enhancement with pockets of pericardial effusion and patchy or a diffuse pattern of myocardial segmental strain abnormalities. While the immediate and long-term clinical relevance of these findings remain unclear, our study underscores that a mild or asymptomatic COVID-19 is not a benign illness considering that over half of the younger individuals showed subclinical myocardial and pericardial disease.

Recent CMR studies performed in adults convalescing from COVID-19 indicated a high prevalence of myocardial inflammation (1, 4) . In a recent study of 26 competitive athletes with COVID-19 which included 12 with mild symptoms and 14 asymptomatic athletes, CMR findings consistent with myocarditis based on the presence of myocardial edema by elevated T2 signal J o u r n a l P r e -p r o o f and myocardial injury by presence of nonischemic delayed enhancements were reported in four (15%) athletes (5) . In contrast, we observed a high prevalence of late pericardial enhancement.

The normal pericardium is avascular, and hence gadolinium uptake indicates signs of increased vascularity with pericardial inflammation. However, in our cohort, none of the patients had classic signs of acute inflammation (edema on CMR T2 imaging or elevation of inflammatory biomarkers). Patients frequently showed residual pockets of pericardial effusion suggesting that this may represent subacute or convalescing phase of pericarditis. It remains unclear whether the pericardial involvement seen in our study represents a primary viral involvement or identifies a more generalized COVID-19 related multisystem inflammatory syndrome (20). During CMR imaging, we did not note additional involvement of serous surfaces like the lung pleura in our cases. Interestingly endothelial injury associated with intracellular SARS-CoV-2 has been described to cause new vessel growth -a unique mechanism referred to as intussusceptive angiogenesis (21) . A potential susceptibility of pericardial mesothelial cells to SARS-CoV2 virus due to increased angiotensin converting enzyme receptor activity coupled with inflammation and angiogenesis could explain the high prevalence of pericardial late enhancements and requires investigation (22) . COVID-19 can disrupt the cardiac contractile machinery causing unique patterns of LV segmental dysfunction (23) (24) (25) (26) . Although the significance of these abnormalities is currently unclear, it is important for us to understand whether the multimodality imaging can be grouped together to identify clusters/sub-groups of different pathophysiological phenotypes of COVID-19-induced cardiac involvement. Recent studies have used speckle tracking echocardiography derived GLS with CMR for diagnosing the extent of myocardial dysfunction in viral myocarditis J o u r n a l P r e -p r o o f (27) (28) (29) . Using a similar multimodality imaging along with hierarchical clustering -an approach used previously to risk stratify COVID-19 patients (30), we identified three distinct phenotypic clusters in student-athletes ( Figure 6 ). However, it should be noted that a presence of mere reduction in myocardial strain or an increase in native T1 does not imply myocarditis, since similar findings may result from inflammatory or a Takotsubo cardiomyopathy like stressinduced myocardial dysfunction (31) . More work would be needed to establish the prognostic relevance of these phenotypic patterns.

While direct myocardial or pericardial biopsy samples could establish these hypothesis, such investigative steps may be unreasonable for less symptomatic or asymptomatic individuals considering a majority of patients with isolated CMR pericardial late enhancement would likely experience a benign course (32) . A distinct 15-30% could be at a risk of developing recurrent pericarditis or constrictive pericarditis (33) . The presence of myocardial inflammation could have more severe consequences since chronic smoldering myocarditis could lead to development of heart failure (34) . In addition, the evidence of isolated nonischemic myocardial LGE at CMR can be a substrate for malignant arrhythmia and severe complications, such as sudden cardiac death (35) . Therefore, until we have more information about the true nature of COVID-19 related illness, careful surveillance with cardiac imaging will be of paramount importance for identifying successful resolution or disease progression.

Our study has several limitations. First, although a number of studies have described delayed myocardial enhancement within the LV myocardium in ostensibly healthy athletes, the conservative estimates suggest presence of a significant cardiac abnormalities to be encountered in a frequency of 1:200 (0.5%) (36) . The frequency and distribution of abnormalities in this confined population of young symptomatic and asymptomatic COVID-19 athletic students is J o u r n a l P r e -p r o o f therefore much higher than incidental findings reported in athletes from this age group. Second, as CMR was not clinically indicated in all asymptomatic COVID-19 subjects, this could bias our observations on the true prevalence of subclinical findings in asymptomatic COVID-19 subjects.

Third, although no subepicardial involvement was identified in LGE, the visceral pericardium is in extreme proximity and a direct extension (less than a few pixels involvement) into the epicardium cannot be resolved. Fourth, although we used a multiple step process to carefully differentiate fat from pericardial enhancements using T1 maps and B-SSFP cine images with confirmation offered by a second reader, a step using fat saturated late Gadolinium enhancement 

In a young, otherwise healthy cohort of college athletes recovering from COVID-19, myocardial and pericardial abnormalities were frequently identified using echocardiography and cardiac magnetic resonance imaging. Presence of an abnormal global and regional longitudinal strain identified the varying phenotypic patterns of myocardial involvement with a varying degree of regional myocardial dysfunction. These data will help developing future cardiac screening strategies and guide serial testing in symptomatic and asymptomatic COVID-19 patients.

Previously healthy college-athletes recovering from COVID-19 infection have a high prevalence of cardiac magnetic resonance (CMR) imaging findings that suggest resolving pericardial inflammation. CMR T1 mapping and speckle-tracking echocardiography also revealed subtle changes in myocardial structure and function.

While specific clinical features of ongoing myocardial inflammation were not frequently identified, future studies need to address the underlying pathophysiological process and longterm evolution of the myopericardial abnormalities seen in uncomplicated COVID-19. 

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Video 1. Accompanying Video for Figure 1A. SSFP CMR cine of mid-ventricular short axis view showing absence of pericardial fat during cardiac cycle

Accompanying Video for Figure 1B. SSFP CMR cine of long axis three-chamber view demonstrating absence of pericardial fat during cardiac cycle

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