Introduction

The diaphragm is the main respiratory muscle, and impairment can result in severe problems with respiration. Infants are much more significantly affected by unilateral and bilateral diaphragmatic paralysis than adults, which results in increased morbidity and mortality [1, 2]. Therefore, an early and accurate diagnosis is of the utmost importance.

M-mode sonography (M-US) has been used to assess diaphragmatic motion, but its use has been reported only in small series of children suspected of having diaphragmatic paralysis [3, 4]. Furthermore, its use is not widespread among pediatric radiologists. The purpose of this retrospective study is to describe our experience with M-US for the evaluation of diaphragmatic motion in a large series of children suspected of having diaphragmatic paralysis and to describe the sonographic technique used. In addition, we correlated the sonographic results with the findings on chest radiographs and the clinical outcome.

Materials and methods

After obtaining approval from the Research Ethics Board of our hospital, we retrospectively analyzed 371 consecutive M-US studies performed in 278 children to assess diaphragmatic motion. The studies had been performed between September 1999 and December 2003. There were 163 boys and 115 girls whose ages ranged from 3 days to 17 years (mean age: 1 year and 10 months). The examinations were performed with an Acuson Sequoia (Acuson, Mountain View, Calif., USA), an ATL HDI 5000 (Philips, Bothell, Wash., USA) or a GE Logic 900 (GE, Milwaukee, Wis., USA) scanner with M-mode option using a sector transducer at a MHz range that provided optimal imaging of the diaphragmatic interface in each patient. The examinations were performed according to the technique described below. All other relevant imaging studies, including chest radiographs and abdominal sonograms, were reviewed, and the interpretation of the findings was made by consensus. Medical records were also reviewed to correlate imaging findings with the patients’ clinical course.

Description of M-US technique

Initially, conventional B-mode sonography is performed with a sector transducer to evaluate the upper quadrants of the abdomen and the lower chest to exclude adjacent pathology. Subsequently, both hemidiaphragms are evaluated with B-mode sonography. This includes scanning in an oblique transverse subxiphoid plane in the midline to obtain comparative imaging of both hemidiaphragms; then the transducer is positioned in each subcostal area, and each hemidiaphragm is interrogated separately in the coronal plane. This is followed by M-US evaluation of each hemidiaphragm, which is performed using the technique described by Urvoas et al. [3].

During inspiration, the normal diaphragm contracts and moves caudally toward the transducer. This is recorded as an upward motion of the M-US tracing (Fig.1). During expiration, the diaphragm moves cephalad, away from the transducer, resulting in a downward inflexion of the M-US tracing (Fig.1). In the M-US tracing, two parameters are analyzed: direction of motion and amplitude of excursion (Fig.2).

Fig. 1
figure 1

Schematic drawing shows the US beam incidence on the diaphragm at the end of expiration and at the end of inspiration with the resulting M-mode tracing (Tins time of inspiration, Texp time of expiration). Adapted from Ayoub et al. [5]

Fig. 2
figure 2

Child with left diaphragmatic paralysis shown on B-mode and M-mode sonography. a, b Oblique transverse B-mode scans in the subxiphoid plane. In inspiration (a) the right hemidiaphragm moves toward the transducer, and the left hemidiaphragm moves away from the transducer (arrows). In expiration (b) the right hemidiaphragm moves away from the transducer, and the left hemidiaphragm moves toward the transducer (arrows). c, d M-mode sonography. The normal right hemidiaphragm (c) shows inspiratory peak (arrows) above the baseline. The paralyzed left hemidiaphragm (d) shows small paradoxical inspiratory peak below the baseline (arrows)

It is essential to correlate the phases of the M-US tracing to the correct phases of the respiratory cycle in order to determine the direction of motion of each hemidiaphragm. With some experience, this is easily achieved: normal inspiration occurs after a respiratory pause that represents the end of expiration. In addition, expiration can be identified during a cry or speech (Fig.3). In difficult cases, one can place a free hand on the patient’s chest and correlate movement with the M-US tracing, or an assistant can do this and call out the time of inspiration.

Fig. 3
figure 3

M-mode tracing while the patient is crying. Inspiration represents the first peak in the tracing after the long pause of expiration. Two cursors have been placed on the tracing to measure inspiratory excursion. The cursor at the peak of the inspiration is correctly placed. However, the second cursor is incorrectly placed after the inspiratory peak and should be placed at the end of expiration just prior to the inspiration (arrow). As shown here, the measurement taken underestimates the diaphragmatic excursion

The amplitude of excursion of the hemidiaphragm is measured on the vertical axis of the M-US tracing from the baseline to the point of maximum height of inspiration on the graph (Fig.4). It is important to pay meticulous attention to the measurement technique. The initial cursor should be placed at the end of expiration and the second cursor at the maximum height of the peak of inspiration. Both cursors must be placed either above or below the line of the tracing so that an accurate measurement of the excursion is obtained (Fig.4). This measurement is used to compare movement of the two hemidiaphragms and is essential for follow-up.

Fig. 4
figure 4

Measurements of right diaphragmatic excursion in the same patient. a The cursors have been correctly placed; they both should be either just below or just above the line of tracing. b There is erroneous placement of the cursors. The cursor that measures the maximum height of the peak of inspiration is above the tracing, while the cursor placed on the expiratory phase is below the tracing. This falsely exaggerates diaphragmatic excursion by approximately 20% in this case. Note also the erroneous placement of the second cursor in b, which should be at the end of the expiration before the inspiratory peak as in a

According to the parameters described by Urvoas et al. [3], diaphragmatic motion can be classified as normal, decreased, absent or paradoxical. It is considered normal if the diaphragmatic motion is toward the transducer in inspiration, the excursion is greater than 4 mm, and the difference of excursion between the hemidiaphragms is less than 50%. Decreased excursion is considered when the amplitude is less or equal to 4 mm and the difference of amplitude between the hemidiaphragms is greater than 50%. Absent motion is considered when the tracing shows a flat line (Fig.5). Paradoxical motion is considered when diaphragmatic motion is away from the transducer in inspiration (Fig.1). Absent motion and paradoxical motion indicate diaphragmatic paralysis.

Fig. 5
figure 5

Initial and follow-up M-US in a 3-month-old infant post-Glenn shunt procedure with left diaphragmatic paralysis. a First M-US shows a flat line indicative of absent motion of the left hemidiaphragm. b Follow-up M-US a few days later shows early signs of recovery with some movement of the diaphragm during inspiration. Note that the scales are different (0–90 in a, and 0–120 in b). This might make comparison difficult and could lead to the wrong conclusion that the line is still flat. When close attention is paid, the mild difference between these two lines is appreciated. c Complete recovery is seen 3 months later with return of normal inspiratory peak

Patients are examined during spontaneous respiration. In patients who have mechanically assisted ventilation, the ventilator is temporarily disconnected, and tracings are obtained during spontaneous breathing. In the latter instance, the disconnection of the ventilator and monitoring of the patient are performed by the intensive care nurse or respiratory therapist.

Results

There were 278 children and 742 hemidiaphragms evaluated. There was a wide variety of associated clinical conditions in these patients with suspected diaphragmatic impairment (Table 1).

Table 1 Associated clinical conditions in 278 patients with suspected diaphragmatic paralysis

Normal movement was detected in 238 right hemidiaphragms and in 232 left hemidiaphragms. Abnormal movement was detected in 131 right hemidiaphragms (84 had decreased excursion, 33 had absent motion, 14 had paradoxical motion) and in 135 left hemidiaphragms (63 had decreased excursion, 44 had absent motion, 28 had paradoxical motion). In two patients (0.71%), the left hemidiaphragm could not be visualized as a result of interposition of gas in the stomach and bowel. In two other patients (0.71%), the recorded images of both hemidiaphragms were not diagnostic because of poor technique.

Only one M-US examination was performed in 222 of the patients. Follow-up examinations were obtained in the remaining 56 patients. In the latter group, the number of follow-up examinations ranged from one to six. These follow-up studies showed improvement in diaphragmatic motion in 26, no change in 23 and deterioration of motion in 7. Plication of the hemidiaphragm was performed in the latter seven.

A total of 287 chest radiographs obtained within 48 h of the M-US examinations were available for our review. Of these, 23 were not optimal for evaluation of diaphragmatic position because of the presence of pleural effusion, focal diaphragmatic eventration, marked thoracic scoliosis or pneumothorax. Tables 2 and 3 describe the correlation between the radiographic and the M-US findings. Excluding the radiographs and M-US examinations that were not considered diagnostic (Table 3), the sensitivity, specificity, positive predictive value and negative predictive value of chest radiographs for detecting abnormal diaphragmatic motion were 34.4%, 86.3%, 84.9% and 36.9%, respectively.

Table 2 Correlation of the position of the diaphragm on 287 chest radiographs with the findings on the M-US examination
Table 3 Correlation of the findings on 260 chest radiographs with the corresponding M-US examinations (non-diagnostic radiographs and M-US examinations have been excluded)

Discussion

Many clinical situations result in abnormal motion of the diaphragm [3, 5, 610]. In children, diaphragmatic paralysis has been most commonly reported in association with birth trauma and following thoracotomy. In our series, cardiac surgery, including heart transplantation, was the most common cause of diaphragmatic dysfunction and paralysis, accounting for 75% of our cases. The incidence of phrenic nerve injury after cardiac surgery has been reported to range from 0.5 to 10% and might be the result of cooling, stretching, cauterizing and/or accidental severing [1, 11, 12].

In infants and young children, adequate ventilation is almost totally dependent on diaphragmatic function because of the poorly developed and weak intercostal muscles and the mobility of the mediastinum [1]. Therefore, the effect of diaphragmatic paralysis is more severe and poorly tolerated in children, making them particularly susceptible to atelectasis, pneumonia and ventilatory failure even in unilateral paralysis, and children virtually always suffer ventilatory failure when the paralysis is bilateral [13].

Diaphragmatic paralysis might well be underdiagnosed because of its varied and often non-specific presentation. Clinical findings that can suggest the presence of diaphragmatic impairment include unexplained difficulties in weaning the patient from mechanical ventilation, persistent elevated hemidiaphragm on chest radiographs, unexplained respiratory distress or dependence on oxygen supplementation, asymmetric breathing pattern, paradoxical movement of the epigastrium, recurrent pneumonia, recurrent unilateral lung collapse and tachypnea [2]. Early diagnosis is important because diaphragmatic paralysis can require adapted and prolonged ventilatory support that is often associated with complications. Surgical plication of the hemidiaphragm, when indicated, can help to reduce the duration of ventilatory assistance [11, 12, 14].

Several imaging modalities have been used in the evaluation of suspected diaphragmatic paralysis. The chest radiographs are of little utility in its early diagnosis, particularly during the neonatal period. Although a chest radiograph might show elevation of the affected hemidiaphragm, this is not a specific sign because of the wide normal range of the position of the hemidiaphragms [15]. In our series, a frontal chest radiograph had a low sensitivity (34%) to detect abnormal diaphragmatic motion (Tables 2, 3). Of the 187 radiographs that showed normal position of the hemidiaphragms, 118 (63%) had abnormal diaphragmatic motion on M-US. On the other hand, of the 73 showing elevation of one hemidiaphragm, 11 (15%) had normal diaphragmatic motion on M-US.

Traditionally, assessment of diaphragmatic motion has relied on fluoroscopic evaluation in the antero-posterior view with the patient in supine position or in the lateral view with the patient in decubitus position. However, this fluoroscopic evaluation, still in use in many institutions and formerly considered the gold standard method for evaluation of diaphragmatic motion, can provide conflicting information. In addition, it has many disadvantages, which include radiation exposure, the need for an assistant to summon the phases of respiration while the radiologist watches the image intensifier, the need to transport the patient to the fluoroscopy unit, visualization of only the least mobile anterior third of the diaphragm on the antero-posterior view [16, 17] and potential misinterpretation when there is bilateral diaphragmatic paralysis [3, 6].

More recently, sonography has been used in the assessment of diaphragmatic motion. This has more commonly been performed with real-time B-mode sonography by direct visualization of the hemidiaphragms on the parasagittal plane in addition to a comparative view on an oblique transverse plane through a subxiphoid approach [18, 19]. There are also reports of indirect assessment of diaphragmatic motion with B-mode sonography, by measuring renal excursion [20] or by assessment of cranio-caudal displacement of the left branches of the portal vein [21].

Sonography offers several advantages over fluoroscopy, which include visualization of all portions of each hemidiaphragm, the lack of radiation exposure, its portability and capability of evaluating for an underlying disease process in the base of the thorax, such as pleural effusion, and for pathology in the upper abdomen. In adults, diaphragmatic motion can also be easily assessed with real-time sonography with the use of special maneuvers such as coughing or the “sniff test” [22, 23]. These maneuvers require the patient’s cooperation and, therefore, cannot be performed in neonates and young infants and in children with a decreased level of consciousness who are in the intensive care unit post-operatively. Even in older children, who might try to cooperate, the findings can be difficult to appreciate and interpret because of their rapid respiratory rate.

In contrast to B-mode sonography, M-US traces the movement of structures along the sonographic beam and plots this against time, thereby enabling the quantification of motion (Fig.1). An initial study to evaluate diaphragmatic motion with M-US dates to 1975, when Haber et al. [24] attempted to use this technique in patients with pleural effusion and various abdominal pathologies. These authors pointed out the potential usefulness of M-US, but did not elaborate on the technique and reported no data. In the following decades, the description of the potential utility of M-US in diaphragmatic paralysis in children was limited to a few sporadic case reports [25]. Urvoas et al. [3] reported the usefulness of this technique in 27 children in 1994, and Riccabona et al. [4] did the same in 30 children in 1998. Until now, however, there has been no report of this technique in a large series of children, and its use is not widespread among pediatric radiologists.

Our study in a large number of children shows that M-US is an easy and reproducible technique that can be done at any age and can be used to follow the progress of diaphragmatic function at the bedside without the use of ionizing radiation. We were able to visualize and assess the motion of all of the right hemidiaphragms. In only a minority of our patients (0.71%) could the left hemidiaphragm not be visualized because of overlying bowel gas. This is in contrast to previous papers that have reported a much higher incidence of non-visualization of the left hemidiaphragm [5]. In addition to the advantages of B-mode sonography, the use of M-US permits one to obtain measurements of the amplitude, duration and velocity of the diaphragmatic excursion, and it allows one to maintain a permanent record of the diaphragmatic excursion. This quantification results in a more objective evaluation that is particularly helpful for follow-up studies in order to monitor improvement or deterioration. It might also allow some degree of prognostication; some authors have postulated that immobility of the affected hemidiaphragm carries a better prognosis than paradoxical motion [26].

Pitfalls of M-US are mainly related to the lack of a meticulous technique. We noted in our review some inconsistency in the way the measurements were obtained, which, although this only caused minimal and non-significant errors (Figs.3, 4), in selected cases could result in an erroneous diagnosis. Measurements should be obtained at the correct phases of the respiration, with the first cursor placed at the end of the expiration and the second cursor placed at the peak of the end of the inspiration. The placement of the cursors is also important in relation to the tracing as shown in Fig.4. It is also important to select an appropriate scale that allows enough depth of the field of view so the entire hemidiaphragm is included, but that also allows good visualization of the tracing; this scale should be repeated in follow-up studies to make serial comparison easier (Fig.5). The use of the 50% difference between the excursions of the hemidiaphragms might be useless in cases of bilateral paralysis or dysfunction, but in these cases the absolute numbers of the excursion of each hemidiaphragm are extremely useful. It is important to note, however, that the current parameters proposed by Urvoas et al. [3] do not discriminate between the ages of the patients and the cutoff point of 5 mm as the lower range of normal diaphragmatic excursion. More studies are probably needed to determine whether there is any correlation between the patient’s age and the range of normal diaphragmatic excursion.

In conclusion, sonography with B-mode and M-mode should be the modality of choice to assess diaphragmatic motion, as it can easily diagnose diaphragmatic dysfunction and allows comparison of changes in follow-up studies.