Objectives Congenital absence of the pericardium (CAP) is often confused with other conditions presenting with right ventricular dilatation and usually warrants CT or cardiac MR (CMR) to confirm. It would be desirable to have more specific echocardiographic criteria to provide a conclusive diagnosis.
Methods 11 patients who were diagnosed with CAP (four patients with total CAP) based on CT/CMR were consecutively enrolled. Thirteen patients with atrial septal defect (ASD) and 16 normal subjects served as controls. To investigate spatial changes of heart in the thoracic cavity in CAP, following echocardiographic measurements were made in the left and right decubitus positions: the angle between the ultrasound beam and the left ventricular posterior wall (Angle-PW) in end-diastole at the parasternal long axis, and the distance between the chest wall and the most distal part of the left ventricular posterior wall (Distance-PW) at the parasternal mid-ventricular short axis.
Results Angle-PW in patients with CAP were significantly greater than in those with ASD (100.1±12.5° vs 74.5±8.6°, p<0.017) or in normal subjects (100.1±12.5° vs 69.9±7.6°, p<0.017) at the left decubitus, and the difference in Angle-PW according to posture (left vs right) was significantly greater in CAP compared with the other groups (CAP 20.7±12.7°, ASD 0.31±1.80°, normal 0.31±1.40°, all p<0.017). The differences in Distance-PW according to patient position (CAP 2.43±0.77°, ASD 0.42±0.45°, normal 0.26±0.55°) or cardiac cycle in each position (left: CAP 1.60±0.76°, ASD 0.41±0.27°, normal 0.17±0.12°; right: CAP 0.70±0.32°, ASD 0.22±0.19°, normal 0.22±0.13°) were significantly higher in the CAP group than in the other groups (all p<0.017).
Conclusions Patients with CAP have dynamic alteration in cardiac position depending on posture, which is not observed in ASD or in normal controls. Hence, total or left-sided CAP can be reliably diagnosed with positional changes during routine echocardiography.
- congenital pericardial absence
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Congenital absence of the pericardium (CAP) is a well-described but rare clinical condition with fewer than 400 reported cases worldwide.1 Although most patients with CAP are asymptomatic, some experience chest pain, dyspnoea, palpitations, syncope, arrhythmia and even sudden death due to fatal myocardial strangulation or herniation.2 3 Early suspicion of CAP may be possible by demonstrating right ventricular (RV) dilation, cardiac hypermobility and/or a ‘teardrop’ appearance;1 4 however, these findings are not unique to CAP and can also be seen in patients with atrial septal defect (ASD).1 4–8 In addition, ASD shares many clinical and ECG findings with CAP, such as systolic ejection murmur, wide split of S2 and a right bundle branch block ECG pattern,5 8 so that this condition is frequently mistaken as ASD.9 For confirmation, therefore, cardiac MR (CMR) or cardiac CT imaging (CCT) is usually required to directly demonstrate the absence of the pericardium.1 6 9 10 With an additional expense of CMR and CCT and a risk of radiation exposure with CCT, a novel diagnostic and confirmatory technique for this rare disease using echocardiography is desirable. Approximately 40 years ago, Payvandi and Kerber suggested, using M-mode echocardiography, that abnormal findings like RV enlargement may disappear with the patient in the supine or right lateral position.8 ,11 also reported similar findings. Although positional change is a simple, promising intervention, there has been no systematic data supporting its usefulness for CAP diagnosis in the contemporary echocardiographic imaging era. Therefore, we attempted to demonstrate the usefulness and accuracy of this simple intervention for CAP diagnosis using two-dimensional echocardiography.
From January 2010 to April 2016, 13 consecutive patients who were suspected of having CAP based on RV enlargement on echocardiography were initially selected, two of whom declined to undergo CCT and/or CMR owing to economic or radiation concerns. Thus, 11 patients who had diagnostically confirmed CAP by CMR or CCT were finally enrolled. A diagnosis of CAP was confirmed by an independent second radiology specialist with expertise in the cardiovascular field. Patients with ASD with no history of coronary disease and no history of significant valve diseases were enrolled for comparison, who paid a first visit to echocardiographic laboratory for clinical evaluation and were scheduled to undergo surgical repair. Patients with ASD were selected for comparison because patients with CAP are frequently misdiagnosed with ASD due to its similar echocardiographic (eg, RV enlargement), clinical (eg, systolic ejection murmur and wide split S2) and/or ECG (eg, right bundle branch block pattern) features suggestive of RV enlargement.1 4 8 9 Also, 16 normal subjects were recruited for controls from the healthcare centre of our hospital, all of whom were confirmed to be normal in clinical, ECG and echocardiographic terms at the general check-up service. All subjects enrolled in this study had no history of cardiac surgery. Therefore, three different groups were included for this study: (1) patients with CAP; (2) patients with ASD and (3) normal subjects. Each member of the study population completed a chest X-ray, 12-lead ECG and comprehensive echocardiography.
Comprehensive, standard echocardiography was first performed with subjects lying in the left lateral decubitus position. After completion of standard echocardiography, subjects were asked to lie down in the right lateral decubitus position. For this study, focus was placed on the parasternal long-axis (PLAX) and parasternal short-axis (PSAX) images at the papillary muscle level obtained in both the left and right lateral decubitus positions, images of which were taken with end-expiratory breath-holding (figure 1). The following measurements were made for quantitative comparison in each subjects: (1) the end-diastolic angle between the longitudinal direction of left ventricular posterior wall and the transducer position (Angle-PW) on PLAX view (figure 2A) and (2) the end-systolic and end-diastolic distance between the starting point of the ultrasound beam and the most distal part of the left ventricular posterior wall (Distance-PW) at the papillary muscle level on PSAX view in centimetres (figure 2B). All measurements were made by an experienced, independent cardiologist at both end-systole and end-diastole and averaged from three consecutive beats.
Data are expressed as mean±SD for continuous variables and as numbers (%) for categorical variables. Differences in continuous variables between groups were compared using the Mann-Whitney U test. Because of the possibility of an inflation of type I error that may come from multiple comparisons, a probability value of <0.017 was adopted for statistical significance in this particular analysis. In the remaining statistical analyses, a value of <0.05 was considered to indicate statistical significance. For comparison of categorical variables, Fisher’s exact test was used. Intraobserver and interobserver variabilities were assessed using intraclass correlation coefficient analysis by two different blinded evaluations in 11 patients with CAP at least 3 months apart. All statistical analysis was conducted using SPSS version 22.0 for Windows.
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Baseline characteristics and standard echocardiographic measurements are summarised in tables 1 and 2. The mean age of patients with CAP was 43±19 years old, with male predominance (n=8, 72.7%). Left ventricle (LV) end-diastolic and end-systolic dimensions were both significantly smaller in patients with ASD, as compared with patients with CAP and normal subjects; however, the values of LV dimensions in all patients and normal subjects were within normal ranges.12 As expected, RV enlargement was observed in all patients with CAP and ASD. Moderate or severe tricuspid regurgitation was not found in any of study subjects. End-diastolic Angle-PW measured in the left lateral decubitus position was significantly higher (100.1±12.5°) in patients with CAP than in patients with ASD (74.5±8.6°) or in normal subjects (69.9±7.6°) (both p<0.017), but this statistical differences were lost when Angle-PW was measured in the right lateral decubitus position (all p>0.05). As a result, the difference in Angle-PW measurements between the left and the right decubitus at end-diastole was significantly higher in patients with CAP, as compared with patients with ASD or normal subjects (all p<0.017) (figure 3A). In terms of Distance-PW, similar trends were noted: end-diastolic Distance-PW in the left lateral decubitus position was significantly greater in patients with CAP (12.7±1.3) than in ASD (10.9±1.0) and normal controls (9.8±0.7) (both p<0.017), and the difference disappeared when the measurements were made in the right lateral decubitus position (all p>0.05). As a consequence, the difference in Distance-PW measurements between the left and right decubitus positions at end-diastole was significantly greater in patients with CAP, as compared with ASD or normal subjects (both p<0.017) (figure 3B). With regard to the difference in Distance-PW depending on cardiac cycle, the extent of the difference in patients with CAP was decreased by half in the right lateral decubitus position (right: 0.70±0.32 vs left: 1.60±0.76) (figure 3C). All of these findings imply that the heart in patients with CAP is displaced more dorsally than in patients with ASD or in normal controls, which phenomenon appears augmented in the left lateral decubitus posture and is partially normalised in the right lateral decubitus position.
The clinical features and the echocardiographic parameters at two decubitus positions of patients with CAP are summarised in table 3. A total absence of pericardium was found in four patients (36.4%), and the remaining seven patients (63.6%) had left pericardial absence. Transthoracic echocardiography showed RV enlargement in all 11 patients (100%) and apical hypermobility or apical swinging motion in six patients (54.5%). However, there was no normal subject showing RV enlargement and/or apical hypermobility. As expected, all patients with ASD showed an RV volume overload pattern on echocardiography, highlighting that this feature cannot be used to differentiate between ASD and CAP. At the individual patient level, there was a clear change in the difference of Angle-PW and the difference of Distance-PW according to patient posture and cardiac cycle, as shown in table 3, implying the usefulness of these two parameters for diagnostic confirmation of CAP. Echocardiographic images obtained from one patient with CAP are displayed in the online supplementary movie 1–4.
Interobserver and intraobserver measurement agreement were excellent, as shown in table 4.
CAP is a well-defined but rare cardiac malformation. It reportedly occurs in 1:10 000 to 14 000 people, with male predominance as shown in the current study.13 Although it is rare and usually takes a benign course, it can result in serious consequences like sudden death due to fatal myocardial strangulation or herniation.2 3 To date, CCT and CMR have been accepted as gold standard imaging modalities to diagnose CAP. Both imaging techniques can provide direct evidence of the absence of pericardium and/or fat and, furthermore, can demonstrate changes in the position of the heart within the thorax. In particular, CMR is very useful because of its high sensitivity to detection of pericardial fat and the absence of the preaortic recess that is almost always present in normal hearts.14 Although both modalities are reliable for the diagnostic confirmation of CAP, there are concerns over radiation exposure during CCT and over the high cost of CMR. In addition, it has been reported that reduced pericardial fat may be misdiagnosed as pericardial absence on CMR in about 10% of normal subjects.4 15 Therefore, it is important to establish specific echocardiographic diagnostic criteria to firmly identify CAP. In contrast to CCT or CMR, echocardiography cannot directly image the presence or absence of the pericardium itself. Although echocardiography shows some indirect clues of CAP such as pseudo RV volume overload, cardiac hypermobility, abnormal swinging motion of the apex and paradoxical septal motion, these findings are non-specific, are not always observed in patients with CAP (as demonstrated in our series) and can be observed in patients with other diseases such as ASD.4–6 8 13 15 16 In fact, RV volume overload pattern was observed in all patients with ASD and CAP without exception in the current study. In addition, cardiac hypermobility or a swinging motion was visually reported in only six patients with CAP (54.5%). As demonstrated in this study, however, echocardiography was able to provide additional strong evidence for CAP simply by changes in posture of the patient. Despite the small number of patients with CAP enrolled in this study, the difference in Angle-PW and the difference in Distance-PW according to patient posture were significantly greater in all patients with CAP as compared with ASD or healthy subjects without any exception (100%), suggesting that the heart was posteriorly displaced in patients with CAP lying in the left lateral decubitus position, possibly due to loss of pericardial constraint, which moved anteriorly when patients were on their right side.
Because a change in posture can significantly alter cardiac haemodynamics without causing serious concerns, it has been be considered best physiological as well as the safest intervention. For example, cardiac output in the standing or sitting position is lower than that in the lying position,17 and even a simple leg elevation can significantly increase LV preload due to an increase in venous return.18 In the current study, a simple change in lying position was adopted to modify the location of the heart in the thorax, and no patient reported any discomfort during examination.
One important function of pericardium is maintenance of cardiac position in the thorax in relation to the lungs. In the presence of pericardium, the apex shows a systolic twisting motion with the cardiac base as the fulcrum in combination with pericardial support.19 20 In the absence of pericardium, however, the anchoring role of the pericardium is not fulfilled, and the cardiac apex is dorsally displaced, as seen in figure 4A. In this situation, this anatomic alteration is accompanied by a functional change in cardiac systolic movement; that is, the unique twisting motion of the cardiac base is no longer observed, as clearly shown earlier.21 22 In other words, LV shows only an apical counterclockwise rotation without effective clockwise rotation of the cardiac base and, as a result, the LV only shows the anterior swinging motion during the systolic period (figure 4B).21 22 With the onset of diastole, the energy accumulated by twisting during systole is released and, at the same time, the cardiac apex moves back to the left, posterior side of the thorax (figure 4A) because normal pericardial support is absent.
To quantitatively demonstrate dynamic cardiac movement throughout the cardiac cycle in patients with CAP, we measured Angle-PW and Distance-PW and compared with those of ASD and healthy subjects. As expected, we found that loss of normal pericardial restraint in patients with CAP causes the heart to be displaced towards the left side and posteriorly at end-diastole while patients with CAP are in the left lateral position and, thus, the Distance-PW was significantly increased, but this was not true for patients with ASD or normal subjects. In addition, the difference in Distance-PW according to cardiac cycle was significantly increased in patients with CAP owing to the systolic anterior movement of the heart caused by the loss of normal pericardial restraint when patients with CAP were on their left sides. This excessive anterior movement of the heart in systole was not observed when the patients lay on their right, because lying on the right side makes the heart itself move anteriorly in the thorax and limits the anterior motion of the heart in systole (figure 4C and D). For this reason, the difference in Distance-PW according to patient posture was significantly greater in patients with CAP as compared with ASD or healthy subjects. In contrast, we did not find any significant change in Distance-PW in ASD or normal subjects when they changed position. The normalisation of Angle-PW in patients with CAP when in the right decubitus position can be well explained by a change in the anatomic position of the heart within the thorax (figure 4). This dynamic movement of the heart observed in patients with CAP is unique and was found in all patients with CAP with no exception and, thus, can be used for diagnostic confirmation of the left or total pericardial absence.
Based on the results presented here, we believe that echocardiography combined with simple postural change can be used to rule in or rule out the diagnosis of CAP in patients who show features of RV volume overload pattern with or without apical hypermobility or apical swinging motion. In contrast to the work published previously,8 we used 2D echocardiography of high quality, included large population of patients with CAP and provides quantitative evidence of dynamic changes in cardiac position according to postural change. In addition, the current work compared patients with CAP with patients with ASD as well as normal subjects, providing the diagnostic usefulness of this simple manoeuvre for confirmation of CAP. Although we presented quantitative data analyses to objectively prove our concept, a diagnosis of CAP could be easily made on a visual basis even without quantitative measurements of the parameters presented here.
Several limitations of the current study should be acknowledged. First, only a small number of patients with CAP were included, making the study susceptible to bias and low statistical power. However, CAP is a rare disease,23 and as far as we know, the current work includes the largest population of patients with CAP assessed by echocardiography. Furthermore, we found consistent changes in Angle-PW and Distance-PW according to cardiac cycle or patient position in all patients with CAP without an exception. Thus, we believe that the results can be practically adopted as the diagnostic criteria of CAP in the echocardiographic laboratory. Second, we did not enrol right-sided patients with CAP. Therefore, we cannot be sure that the diagnostic approach suggested here will be applicable to cases of right pericardial absence. Finally, we need to think about the concern that complete pericardial absence seems to be less vulnerable to serious complications like sudden death than partial defect does. Although this concern seems to be theoretically correct, there have been no systematic data on what proportion of each type of pericardial defect suffers from serious complications like sudden death. Thus, this information should be also re-evaluated in a multinational, multicentre study format.
In conclusion, the total or left-sided pericardial absence can be reliably diagnosed with a simple manoeuvre of changing a patient’s posture during routine echocardiography. We believe that this simple echocardiographic approach can pave the way for reliable diagnosis of total or left-sided pericardial absence without resorting to CCT or CMR in patients who have RV enlargement on routine echocardiography.
What is already known about this subject?
Congenital absence of the pericardium (CAP) is a rare but clinically relevant disease. Although asymptomatic in most patients, it may cause sudden death. Confirmatory diagnosis cannot be made only with clinical or echocardiographic findings. Thus, cardiac MR (CMR) or cardiac CT (CCT) imaging is required to confirm the CAP.
What might this study add?
This study provides simple, but practical, confirmatory echocardiographic diagnosis of CAP. With the simple positional change of the patient with pseudo right ventricular (RV) enlargement, CAP diagnosis can be reliably ruled in or ruled out without help of other imaging modalities.
How might this impact on clinical practice?
Patients with CAP have been required to undergo CCT or CMR to reveal the disorders causing RV enlargement, making them exposed to radiation or to additional cost. Using the simple positional change we suggested here, however, CAP can be reliably diagnosed without using other imaging modalities.
We acknowledge the sonographers who faithfully attempted to stick to the study protocol.
Contributors MJK and H-KK contributed to the conception and design, acquisition of data or analysis and interpretation of data. J-HJ, J-BP, Y-JK, G-YC and D-WS contributed to the conception and design, and acquisition of data. J-HJ, YEY, H-LK contributed to the analysis and interpretation of data. MJK and H-KK contributed to the drafting and finalising the article. J-HJ, YEY, S-PL, Y-JK, G-YC, D-WS and JKO contributed to the revision of the article critically for important intellectual content. All authors provided final approval of the version to be published.
Funding This study was partly supported by Chong Kun Dang Research Fund 2016.
Competing interests None declared.
Patient consent Study patients provided written informed consent to participate in the study.
Ethics approval The study protocol was approved by the Institutional Review Board of Seoul National University Hospital.
Provenance and peer review Not commissioned; externally peer reviewed.
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