British Journal of Radiology 74 (2001),701-708 © 2001 The British Institute of Radiology
Breath-hold MRI in evaluating patients with pectus excavatum
N Raichura, BSc
1
J Entwisle, MRCP, FRCR
2
J Leverment, FRCS
3 and
C S Beardsmore, BSc, PhD
1
1Department of Child Health, University of Leicester, Clinical Sciences Building, Leicester Royal Infirmary, PO Box 65, Leicester LE2 7LX, and Departments of 2Radiology and 3Cardiothoracic Surgery, University Hospitals of Leicester NHS Trust, Glenfield Hospital, Groby Road, Leicester LE3 9QP, UK
Correspondence: Dr L S Beardsmore. Mr N Raichura was supported by a grant from the Wolfson Foundation. Additional support came from the Glenfield Hospital Cardiothoracic Trust.
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Abstract
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Pectus excavatum (PE) is a congenital condition in which the sternum is displaced posteriorly with associated changes in the adjacent costal cartilages. The aetiology of PE is uncertain although various underlying abnormalities of the diaphragm have been implicated. There is sparse information regarding the use of fast MRI in evaluating the deformity. Our aims were to use fast MRI to evaluate static and respiratory-related dynamic chest wall characteristics, the extent of cardiac displacement and diaphragmatic excursion in patients. FLASH and TurboFLASH MR sequences in axial and coronal planes were performed on the thoraces of six young patients with PE and six individually matched healthy controls during full inspiratory and full expiratory breath-holds. The Pectus Index was derived from chest wall measurements using axial images. The distances of the left and right cardiac borders from the midline were measured using axial images, and excursion of the dome of each hemidiaphragm was measured using coronal images. The degree of sternal depression worsened substantially in expiration. Anterior chest wall movement was similar in the two groups. Patients had significantly flatter chests than the controls. There was a trend towards leftward cardiac displacement in the patients (maximum distance between left heart border and midline during full expiration 99.5 mm in patients and 91.8 mm in controls). The right diaphragmatic dome excursion was greater than the left in the controls (53.6 mm and 47.4 mm, respectively), but this was not seen in the patients (50.2 mm and 50.4 mm, respectively). It is concluded that fast MRI is very informative in evaluating skeletal abnormalities, chest wall motion, and cardiac and diaphragmatic changes seen in PE.
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Introduction
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Pectus excavatum (PE), a congenital condition occurring in approximately 8 per 1000 live births [1, 2], is the most common chest wall deformity seen by paediatricians and general practitioners [3]. It is characterized by a posteriorly displaced sternum with associated abnormalities of the costal cartilages. The aetiology of PE is uncertain but several theories have been suggested, including overgrowth of the ribs and costal cartilages [4] and underlying defects of the diaphragm [5]. The condition often results in symptoms [6, 7] and psychological problems may predominate in younger patients [8]. The pathophysiological effects of PE are variable and in severe forms the heart, lungs and other intrathoracic structures are structurally deranged or displaced [6, 9, 10]. Corrective surgery usually provides excellent cosmetic results and significant subjective improvement [11–13].
The extent of deformity is generally assessed radiologically by means of chest radiographs and CT. Although these imaging modalities provide useful information on abnormal thoracic anatomy for clinical purposes, they may lack the ability to detect other, more subtle, structural changes. Moreover, there are limitations associated with the multislice high resolution CT techniques, including exposure to significant levels of ionizing radiation.
There is sparse published information relating to the value of MRI in the assessment of patients with PE. Although numerous authors have implicated the diaphragm as the underlying cause, movement patterns of the diaphragm have not been extensively studied in patients. Similarly, the degree of cardiac displacement and anterior chest wall movement have not been documented in these patients. With conventional spin echo imaging, long imaging times as well as cardiac and respiratory motion artifacts result in inadequate temporal resolution for dynamic assessment of diaphragmatic motion and cardiac position. The use of fast TurboFLASH and FLASH sequences greatly reduces these problems and allows more accurate positional measurements to be made. We aimed to evaluate anterior chest wall movement, diaphragmatic excursion and cardiac displacement in six patients with PE and six healthy, individually matched controls using fast MRI sequences.
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Materials and methods
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Subjects
The study group comprised six consecutive patients (median age 18.5 years, range 15–38 years) with diagnosed PE referred to a consultant thoracic surgeon, and six healthy, individually matched controls (median age 24 years, range 16–31 years) (Table 1
). Controls were recruited by means of advertisements placed in two local hospitals and were individually matched in order of priority to gender, height, ethnicity, age and body mass index. Subjects with moderate or severe asthma, defined as requiring regular medication, and those with other cardiopulmonary problems were excluded. One patient had mild scoliosis. Informed written consent was obtained from each subject and, if appropriate, from a parent or guardian. This study was approved by the Leicestershire Area Health Authority Ethics Committee.
Imaging
Imaging of the thorax was performed on a 1.5 T Magnetom Vision unit (Siemens, Iselin, NJ) using the Numaris III software, version Vb33A (Siemens, Erlangen, Germany). Fast TurboFLASH and FLASH sequences were used. The short acquisition times produced images that were comparatively free of motional artefact from cardiac or respiratory movement. The fast acquisition times also enabled images of the entire thorax to be obtained during a single breath-hold. For axial images a TurboFLASH sequence was used with a body coil, 8° flip angle, 5.0 ms repetition time, 2.3 ms echo time, 10 mm slice thickness, 35–48 cm field of view and 96 x 256 matrix. Sequential slices were obtained in the axial plane at 10 mm increments from the lung apices to the bases during suspended full inspiration and again at full expiration. For coronal images a FLASH sequence was used with a 80° flip angle, 174.9 ms repetition time, 4.1 ms echo time, 7 mm slice thickness and 128 x 256 matrix. Coronal images were obtained during full inspiratory and full expiratory breath-holds and included the domes of each hemidiaphragm. Subjects were instructed by the radiographer to hyperventilate before imaging by taking two or three deep breaths to increase the duration of breath-holding, and then to inspire or expire fully before breath-holding during image acquisition. Breath-holds lasted between 19 s and 22 s. Subjects were verbally coached to emphasize the need for absolute maximum inspiratory and expiratory efforts during breath-holding. A video link enabled the radiographer to visualize subjects throughout the entire scanning duration.
Image analysis
The MR images were transferred to a workstation (Voxel Q; Picker, Highland Heights, OH) and were analysed by one person (NR). The following measurements were made from the axial scans taken during full inspiration and full expiration.
Chest wall measurements
The Pectus Index, defined previously as the ratio of the maximum internal transverse diameter of the thorax to the minimum sternovertebral distance [14–16], was determined as a measure of chest wall deformity. Chest wall flatness was determined according to the method of Nakahara et al [17]. Mean anteroposterior chest wall movement was calculated as the average percentage increase during respiration in the anteroposterior rib diameters on the left and right sides (Figure 1).
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Figure 1. Chest wall measurements. Fast TurboFLASH axial image with measurements of the skeletal extent of pectus excavatum deformity. Pectus Index=b/a; chest flatness=b/c; mean anteroposterior chest wall movement=100[(ci/ce)+(c'i/c'e)-2]/2, where the subscripts i and e are the full inspiratory and expiratory measurements, respectively. a, minimum sternovertebral distance (minimum anteroposterior diameter) at the level of greatest deformity; b, maximum internal transverse diameter of the thorax; c and c', maximum anteroposterior rib diameters on the right and left sides, respectively, at the level of greatest deformity.
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Cardiac displacement
The degree of cardiac displacement was determined from axial images taken during full inspiratory and full expiratory breath-holds (Figure 2). The most lateral distances of the left and right cardiac borders were measured from a fixed reference midline, which passed through the mid sternum anteriorly and the midpoint of the vertebral body posteriorly. All measurements were made perpendicular to the midline. The maximum left and right distances did not necessarily occur at the same level vertically.
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Figure 2. Cardiac displacement. Axial images of (a) full inspiration and (b) full expiration. HL, most lateral distance of the left cardiac border from midline; HR, most lateral distance of the right cardiac border from midline; ......., midline; i, full inspiratory measurement; e, full expiratory measurement.
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Diaphragmatic excursion
Diaphragmatic dome excursion of the left and right sides was measured from coronal images taken during full inspiration and full expiration (Figure 3). A fixed horizontal reference line from which the measurements were made, was defined above the lung apices. Given that the diaphragm lacks symmetry and undergoes substantial changes in position, shape and size during respiration, it was not possible to define specific anatomical locations or points of reference. The distances from the midline to the domes were kept constant when comparing inspiratory and expiratory images to ensure that similar points of the diaphragm were being analysed in each case. The highest point of the diaphragm was selected to represent the dome. Absolute excursions of the left and right hemidiaphragms were calculated as the difference between full inspiratory and full expiratory vertical distances of the domes from the reference line.
Data analysis
Although this study was primarily descriptive, numerical study data were analysed statistically using the SPSS version 10.0 package. Non-parametric tests that make fewer distributive assumptions were used because of the small sample size and uncertainty surrounding the normality of distribution of data. The Wilcoxon signed rank test was used to compare the two groups in terms of their respective median values. Unless otherwise stated, mean values were reported as ±standard deviations. A p-value of less than 0.05 was considered to be statistically significant. One patient who failed to co-operate during MRI breath-holds was excluded from the relevant section of the analysis, and this has been clearly identified.
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Results
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Patient and control demographics
All subjects were White caucasians and five of the matched pairs were male (Table 1
). In one matched pair the age difference was 14 years but in the remaining five pairs the age difference was 10 years or less. Patients and controls were closely matched for height with a maximum difference of 5 cm. The control subjects weighed more than the patients in all but one case, and this was reflected by the difference in body mass index (BMI) of 3.17±3.19 kg m-2.
Chest wall measurements
Measurements of chest wall features are summarized in Table 2. There was a noticeable difference in the minimum anteroposterior diameterand hence the Pectus Index between patients and controls, but this narrowly failed to achieve statistical significance (p=0.06). The maximum internal transverse diameter was not significantly different between the two groups. There was a significant reduction in the minimum anteroposterior diameter in full expiration comparedwith full inspiration in both the patient and control groups (p=0.03 for both groups). Similarly, significant reductions were found when comparing the maximum internal transverse diameter in full expiration with full inspiration (p=0.03 for both groups). The degree of sternal depression, as determined by the Pectus Index, increased substantially in full expiratory breath-holds and this change was typically greater in the patient group. However, there were no significant differences between the two groups when considering the mean anteroposterior chest wall movement during respiration on the left and right sides. The patient group had significantly flatter chests than the control group (p=0.03) on the basis of the Chest Flatness Index.
Cardiac displacement
Measurements of cardiac displacement in terms of the maximum distance of the left and right heart borders from the midline are given in Table 3.
The left heart border (HL) was clearly more laterally located in three patients compared with their controls, but there was no statistically significant difference in the distance from the most lateral border of the left side of the heart to the midline (HL) between groups in either full inspiratory and full expiratory positions (Figure 4). The three patients in whom the left heart border was clearly laterally displaced (Patients 1, 4 and 5) were those with the most marked deformity (Inspiratory Pectus Indices 5.28, 5.37 and 8.03, respectively). HL was significantly higher in expiration compared with inspiration in both the patient and control groups (p=0.03 for both groups). Moreover, this lateral shift of the left heart border showed a tendency towards being greater in the patient group relative to the control group. This observation was particularly marked in Patients 1, 2 and 4 who had movements of 26 mm, 20 mm and 34 mm, respectively. In contrast to HL, the distance from the most lateral border of the right side of the heart to the midline (HR) did not differ significantly between groups and there were no significant changes in HR between full inspiratory and full expiratory positions in either group.
Diaphragmatic excursion
A comparison of left and right hemidiaphragmatic excursion between the patient and control groups is illustrated in Figure 5. One subject pair has been omitted because the patient could not perform a technically satisfactory recording.
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Figure 5. Left and right hemidiaphragmatic excursion ( D) in patients and controls. Note the relatively greater movement of the left hemidiaphragm dome in the patient group compared with controls. In contrast, a comparatively reduced excursion of the right hemidiaphragm dome in the patients was seen.
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The mean left and right hemidiaphragmatic excursions were 50.4 mm and 50.2 mm, respectively, in the patient group. In the controls these were 47.4 mm and 53.6 mm, respectively. There was no statistically significant difference in left hemidiaphragmatic excursion between the patient and control groups (p=0.31). Similarly, no significant difference was noted in excursion of the right hemidiaphragm (p=0.25). However, there was a noticeable trend towards greater excursion of the left hemidiaphragm in the patient group compared with the control group. This was reflected by the 95% confidence interval for the difference in means in left hemidiaphragmatic excursion, which ranged from -8.76 mm to 2.76 mm. In contrast, there was a tendency towards a decreased excursion of the right hemidiaphragm in the patient group compared with the control group, with a 95% confidence interval for the difference in means ranging from -2.53 mm to 9.33 mm.
On comparing the excursion of the left and right hemidiaphragms in each group, the right dome moved, on average, 6.2 mm more than the left dome in the control group. In the patient group, however, the left hemidiaphragm dome moved, on average, 0.2 mm more than the right dome. There was, therefore, a strong correlation between left and right diaphragmatic excursion in the patient group (r=0.92, p=0.03), but a weaker association was found in the control group (r=0.84, p=0.07). Essentially, our findings suggest that diaphragmatic movement in the patients is more symmetric than in the controls.
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Discussion
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PE is a relatively common condition that often causes subjective complaints [4, 6, 7, 13] and can be psychologically detrimental [6, 8, 16]. Although some authors have reported functional cardiopulmonary abnormalities in patients, no consensus has been established [7, 9, 11, 18]. Routine radiological assessment may lack the sensitivity required to detect more subtle anatomical changes. This case–control pilot study comprised six patients with diagnosed PE and six healthy controls. Most of the patients were symptomatic and the common complaints were chest tightness, dyspnoea on minimal exertion and pre-cordial pain. It is possible that these complaints were, at least in part, psychogenic in origin. Although patients had varying degrees of chest wall deformity, sternal depression became more apparent in expiration. Asymmetry of the chest was more common in patients but was generally mild. No significant difference was found in anterior chest wall movement between patients and controls. Lateral cardiac displacement tended to be greater in patients than controls, particularly during full expiration. Unusual patterns of diaphragmatic excursion occurred during respiration in the patient group, with tendencies towards increased excursion of the left dome and reduced excursion of the right dome compared with controls.
Although each patient–control pair was closely matched for height, gender and ethnic origin, precise matching for weight and age was not always obtained. Moreover, all but one control subject weighed more than their respective patient. This introduced a potential source of bias when applying statistical comparison tests between the two groups. Close matching of the past medical history and social history of each patient–control pair was not possible, but none of the patients or volunteers had a previous history of respiratory disease. There were no asthmatics on regular medication, and two patients and one control were mild smokers. A potential disadvantage of this study was its small sample size.
When assessing cardiac displacement, use of the TurboFLASH sequence might, in theory, have led to blurring of the cardiac border. ECG gated single slice scans would have been an alternative if more scanning time had been available. However, assessing cardiac borders was not difficult in the subject group.
Indices of deformity using MRI in PE patients have not previously been reported. In the present study, we established the MRI-derived Pectus Index, of which a CT-derived analogous index has been extensively reported in previous studies [14–16]. The wide spectrum of sternal deformity amongst the patients in our study was reflected by the large standard deviation of the Pectus Index. In contrast, the Pectus Index in the controls was considerably less variable. The mean values of the inspiratory Pectus Index were 4.41 and 2.37 in patients and controls, respectively. These findings, whilst being derived from small samples, were comparable with previous studies that reported the mean CT Pectus Severity Index to be 4.42 in patients [16] and 2.38 in normal young adults [14]. Small degrees of chest wall asymmetry were commoner in the patient group.
The minimum anteroposterior diameter of the chest decreased in full expiration compared with full inspiration in all subjects, with a corresponding increase in the Pectus Index. This change was generally more pronounced in the patient group. However, the sharp inward-directed angulation of the anterior ribs and costal cartilages was more apparent during full inspiration. This observation was consistent with the findings of Fonkalsrud and Bustorff-Silva [16] who noticed accentuation of sternal depression in deep inspiration. It has been suggested that patients with PE have diminished chest wall expansion [16], although no mechanisms have been suggested for this. The patients in the present study demonstrated movements of the anterior chest wall comparable with those of the healthy controls. These findings are in keeping with those of Mead et al [19] who concluded that rib cage mobility in patients was entirely normal. The present study confirms the findings of previous work [20] that demonstrated the value and reliability of MRI in evaluating local chest wall motion.
The chests of patients were generally flatter than those of controls, consistent with a previous study [17]. This may suggest possible underlying alterations in entire rib cage configuration independent of the abnormal position of the sternum.
Wada et al [21] considered cardiac displacement in PE patients using anteroposterior chest radiographs. In contrast to our methods they measured the distances from the right cardiac border to the right chest wall (R), and from the left heart border to the left chest wall (L). They concluded that the ratio R/L was increased in PE patients, and changed remarkably after operation. We measured the most lateral borders of the left and right sides of the heart from the midline (HL and HR) during full inspiration and full expiration from axial scans to give an indication of the degree of cardiac displacement. The left heart border had a tendency to be laterally displaced in some patients. The magnitude of the leftward displacement was directly related to the severity of chest wall deformity and was accentuated in expiration. It could be suggested that true lateral displacement of the heart would generally result in an increase in HL and a corresponding decrease in HR. However, given that a number of patients demonstrated relatively small positional changes of the right cardiac border compared with that of the left, the possibility of cardiac distortion, compression or rotation in these patients cannot be overlooked.
It has been suggested that patients with PE often use more extensive diaphragmatic excursions during respiration, but no mechanism has been given [16] and there is a lack of information relating to diaphragmatic movement in PE patients. Gierada et al [22] used fast gradient recalled echo MRI to evaluate diaphragmatic excursion in 10 healthy subjects in the supine position during slow vital capacity breathing. The mean right and left dome excursions were 44 mm and 42 mm, respectively. In the present study, the mean right and left diaphragmatic excursion in healthy controls were 53.6 mm and 47.4 mm, respectively. Both studies, therefore, found greater movements of the right diaphragm compared with the left in healthy subjects. The variations seen in absolute values are likely to be owing to differing subject demographics, image sequences and procedure.
Measurements made in the tidal range may better reflect normal diaphragmatic motion, but we chose to measure diaphragmatic position at extremes as this was more likely to reveal significant differences between patients and controls, especially with a small sample. The MR navigator echo technique would have given a more detailed analysis of diaphragmatic motion [23, 24], but the necessary software was unavailable.
The mean right and left diaphragmatic excursion in patients were similar (50.2 mm and 50.4 mm, respectively) and there was a significant association between the movements of both sides (r=0.92, p=0.03). These findings suggest that the left diaphragm dome tended to move more in the patient group compared with the control group, and that the right diaphragm dome tended to move comparatively less. Essentially, these findings suggest that diaphragmatic movement was more symmetrical in the patients than in the controls. No significant relationship was found between diaphragmatic excursion and age, weight or height in either group. Differences in weight and body mass index between patients and controls may potentially have been a source of bias in the comparative analysis, resulting in errors in interpretation.
This is the first report on chest wall, cardiac and diaphragmatic characteristics using fast MRI in PE patients. It has shown that MRI can be extremely informative in evaluating these changes seen in PE. MR evaluation of the condition is seldom employed for clinical reasons, mainly owing to the high cost and limited availability of the technique. Moreover, other radiological methods, such as conventional radiographs and CT, are often considered adequate in evaluating the main features of the condition. The lack of ionizing radiation, excellent soft tissue contrast and multiplanar capabilities are the major advantages of MRI compared with other imaging modalities.
In conclusion, the degree of chest wall depression typically worsened during full expiration, although full inspiration had the effect of making the deformity visually more obvious. No differences were found in mean anterior chest wall movement in patients compared with healthy controls. Further work is needed to detect any subtle differences in chest wall dynamics not evaluated in the present study.
Lateral cardiac displacement was apparent in some of the patients, although the extent of this varied considerably. Expiration generally had the effect of causing further shift of the heart away from the midline. A possible explanation for these findings in the patients is the lack of space in the mediastinum. It is important to determine the extent of cardiac displacement, rotation and compression of the heart in these patients as they can potentially have detrimental effects on cardiac function. Cardiac rotation has been described in PE, but there has been a lack of information relating to its extent. This could be established by a number of non-invasive techniques, including electrocardiography, CT or MRI.
The present study found altered excursion patterns of the diaphragm in patients. Future studies could consider more detailed movements of the diaphragm at a number of different locations from coronal and sagittal images. There was a trend towards reduced excursion of the right hemidiaphragm and increased excursion of the left compared with controls. Only minimal differences in the excursion of right and left hemidiaphragms were found in patients. In contrast, the control group showed greater excursion of the right hemidiaphragm compared with the left. It may be suggested, therefore, that an underlying structural abnormality of the diaphragm may account for the differences seen in the movement patterns. Anecdotally, it has been suggested that the anterior attachments of the diaphragm are abnormal in PE patients. These attachments, together with other diaphragm characteristics including thickness, surface area, radius of curvature and the zone of apposition, are potential other areas that could be considered for future research.
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Acknowledgments
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We are indebted to Dr M Horsfield, MRI physicist, and the radiographers at Glenfield Hospital, Leicester, for their invaluable assistance.
Received for publication September 27, 2000.
Revision received February 19, 2001.
Accepted for publication March 16, 2001.
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Abstract
Introduction
) and full expiration (
) for each subject pair. In pairs 1, 4 and 5 (columns below the zero line), the left heart border of the patient is more laterally located than the control and becomes more marked on full expiration.