Being the most important respiratory muscle, thus the diaphragm had gained special concern for its anatomical and functional disorders by both physical examination and imaging workup [1].
Despite that they might be asymptomatic, the unilateral diaphragmatic disorders had been described as more common than the usually symptomatic bilateral affection [2,3,4].
In the present study, the accuracy measures of the TAUS had been done in comparison to the CT examinations regarding the diaphragmatic defects and the elevated diaphragmatic copula as reported in the CT.
The diaphragmatic defects, in our study, had included hernias and post-traumatic defects (present in 7 patients 19.4%, 5 on the left side and 2 on the right side) with hernia being seen in 5 cases (3 congenital cases and 2 adult cases), and the traumatic defects were present in two cases: a left side predominance for hernia and defects was noted in this study (Fig. 2, 3, and 4); this had an agreement with the literature, where the congenital posterior hernias are commonly left-sided and more common than the anterior ones [10, 11], and this was explained by the relative protective effect of the liver for the right hemidiaphragm.
Post-traumatic defects can occur either by blunt or penetrating injuries; the blunt injuries are usually under diagnosed at the initial presentation probably due to overshadowing by other associated injuries. CT was considered as the reference standard for both types of injury, and many CT signs had been described as clues for the diagnosis by Desir and Ghaye; they also had reported that the left hemidiaphragm was more liable to injury than the right one and explained this by a multifactorial issues, including the liver support to the right hemi diaphragm. Additionally, it had an inherent resistance greater than the left one. Moreover, the congenital embryonic weakness of the postero-lateral aspect of the left hemidiaphragm might further weaken the left one [12]. We had a great match with such data and thus we used the CT as the reference standard in hemidiaphragmatic defects and hernias; however, in our study, TAUS showed a great sensitivity and specificity {100% (95% CI = 59.04 to100.00%) and 100% (95% CI = 88.06 to 100.00%), respectively} in this regard as compared to CT (the reference standard), but actually the number of cases in the present study was considerably lower and thus considered as a limitation despite the high accuracy measures and the matched data of the lesion location.
Although there is no consensus on the TAUS sensitivity and specificity in diagnosis of diaphragmatic rupture, there had been many reports in the literature that aided in the diagnosis including direct visualization of the diaphragmatic defects (this was also seen in our cases Fig. 3 and 4), visualization of some abdominal viscera above the diaphragm, and by M-mode; abnormal diaphragmatic excursion was readily seen [13], and this also had been seen in our study (Figs 2, 3, and 4).
In our limited experience, TAUS could be considered as a beneficial initial diagnostic tool for diaphragmatic injury especially if the motion assessment by M-mode was added to the anatomical scan; this was also supported by Bothwell et al. who documented the additional advantage of the dynamic assessment of the diaphragm over the plain radiography in this concern [13].
An elevated diaphragmatic copula in CT is considered as a sign of diaphragmatic dysfunction and could be a diaphragmatic weakness, paralysis, or due to subdiaphragmatic collection, and this was relevant—by TAUS—to abnormal diaphragmatic thickness (measured by B-mode and the thickening fraction), diaphragmatic weakness or paralysis (measured by M-mode in quiet and deep respiration as well as in sniffing), or if there were subphrenic collections or ascites underneath the affected copula.
Goligher and his co-workers stated that diaphragm thickness depends mainly on the muscle mass; thus, a reduced diaphragm thickness might indicate its atrophy. Measurement of the diaphragm thickness is feasible by using TAUS, where the hepatic window can facilitate the measurement of the right hemidiaphragm than the less accessible left one. They had estimated the normal diaphragm thickness in ventilated patients (2.4 ± 0.8 mm), and diaphragmatic atrophy had been identified as values below 2 mm [14]. A rather similar study by McCool et al., stated that the average thickness of the diaphragm is 2.2–2.8 mm in healthy volunteers and 1.3–1.9 mm in a paralyzed diaphragm. They also had reported the same issue as a diaphragm thickness less than 2 mm had been suggested as a cut-off value to define diaphragmatic atrophy [15]. A thinned out diaphragm as measured by TAUS was present in 9 of our cases (8 with paralysis and 1 with weakness out of 19 cases with paralysis and weakness). The mean thickness for cases with thinned out diaphragm was 1.8 mm; however, missing 10 cases out of 19 cases were a considerable issue. Kantarci et al. had explained this as the thickness could vary according to the site of measurement and the phase of the respiratory cycle (start of inspiration or end of expiration), thereby, a thickness as the sole parameter could miss a recently paralyzed diaphragm that could attain a normal thickness for a while, and on the other hand, it could identify an atrophic one in individuals with low body weight [16], this was also matching our study, where some patients with diaphragmatic weakness ( not yet paralyzed) that might preserve some muscle mass and action could have a thickness a little bit more than the lower limit value of 1.9 mm. Therefore, there is an agreement between our study and many literatures that the degree of diaphragm thickening (thickening fraction) had been assumed to be a more sensitive method than the measurement of thickness alone [4, 8, 16, 17].
As the muscles generally thicken during contraction due to fiber shortening, thus, the increase in the diaphragmatic thickness during contraction (inspiration) could be used as an indirect indicator of the muscle fiber contraction, and this was described and measured by a general formula of Gottesman and McCool, a thickening fraction = (thickness at end-inspiration–thickness at end-expiration)/thickness at end-expiration [8], and it had reported in the literature to have a range from 22 to 78% with a mean thickening fraction = 38.4% [8, 18,19,20,21]. They concluded that diaphragmatic thickness and the thickening fraction could detect diaphragmatic paralysis and confirm diaphragmatic atrophy in long-standing paralysis with poor thickening on inspiration; Jung et al. had documented that a thickness variation of< 20% was a predictor for failure of weaning from mechanical ventilation due to diaphragmatic dysfunction [22]. In our study, the results had a concordance with the previous studies where the thickness and the thickening fraction were utilized as parameters for evaluation of the diaphragmatic dysfunction not only for assessment of the muscle mass but also emphasizing the value of the dynamic evaluation of the diaphragmatic contraction through assessment of the thickening fraction and actually, this was done even in cases with diaphragmatic defects and hernias as this—from our point of view—could give an idea about the restoration of the diaphragmatic function after surgical repair if it would be done; this is eventually considered as merit of the TAUS other than measuring the size of the defect.
It should be mentioned that TAUS had the advantage of an indirect assessment of the degree of diaphragmatic contraction (through the measurement of the thickening fraction) over other imaging modalities that can barely assess the diaphragmatic motion and its paradox.
Another role for the TAUS could be added in diaphragmatic function evaluation which was the diaphragmatic motion by M-mode and assessment of the degree of excursion where the diaphragm was assessed in quiet and deep breathing as well as with sniffing.
The diaphragmatic excursion should be done using the curvilinear probe, in M-mode, and measured from the point of the maximal excursion to the baseline, in quiet breathing and in the sniffing; in deep breathing, the measurement should be from the highest to the lowest point of excursion [23], and this was done in the present study as well.
Boussuges et al. had demonstrated that M-mode ultrasonography was a reproducible method for assessing hemidiaphragmatic movement [24].
Diaphragm weakness was indicated by decreased (less-than-normal) amplitudes of excursion on deep breathing with or without paradoxical motion upon sniffing, whereas a diaphragmatic paralysis was indicated by diminished (absence of) excursion with quiet and deep breathing and with absence of motion or paradoxical movement on sniffing (Figs. 5 and 6). The direction of diaphragmatic motion could be identified by the TAUS and correlated to the respiratory phases and paradoxical motion was identified when the diaphragm was moving away from the probe in the inspiratory phase (the reverse of the expected [24,25,26].
In our study, diaphragmatic weakness was present in 9 cases that was presented in CT with an elevated copula, and the TAUS revealed abnormal thickening fraction, in addition to the decreased excursion amplitudes; hereby, we had met an important term, which was the diaphragmatic eventration that was defined in the literature by a congenital focal weakness of the diaphragm and commonly occur in the anteromedial aspect of the right copula and radiographically forms a bulge known as hump that can be identified by either plain radiography or CT [23]. It was seen in one of our cases (Fig. 6), and a differentiation from hernia should be done where the eventration has a continuous but focally weak segment while hernia and defects had a usually discontinuity through protrusion of any abdominal viscera.
By definition, eventration should occur in a congenital weak focal segment in otherwise normal diaphragm [23], which was not the case in our patient where the entire diaphragm was weakened (Fig. 6). Our explanation was that, in reviewing the literature, it had been showed that the eventration increases with elevated abdominal pressure and could actually widen and increase with time and may involve the entire hemidiaphragm by conditions related to an increased abdominal pressure, like obesity, ascites, repeated childbirth, and in constipated individuals and heavy object lifters [23], and our patient had a relevant history that had supported this explanation.
In concordance with Boon et al. and Chavhan et al., our study had shown a high sensitivity and specificity (96.55% and 100% sensitivity and specificity, respectively, with an overall accuracy 97.2% compared to 93% and 100% sensitivity and specificity, respectively, in theirs) in evaluation of a hemidiaphragmatic dysfunction either due to neuromuscular causes (paralysis or weakness) or through the visualization of the infradiaphragmatic causes (ascites or collections) (Fig. 7). They considered the TAUS was superior to fluoroscopy in functional evaluation of the diaphragm [27, 28]; in our study, 10 cases were identified to have an infradiaphragmatic collections, where the TAUS had an excellent depiction of the subphrenic collections and could readily give an idea about its nature as a simple, septated, or complex particulate collections, like those in subphrenic abscesses (Fig. 7).
It should be mentioned that the measurement of excursion depends on maximal inspiratory and voluntary action of the patient and this should be considered for the interpretation of the cut-off values [25]; however, it had been reported that the normal side-to-side difference of excursion between both diaphragmatic copulas should be less than 50% [29]; a right-to-left ratio of excursion had been documented to be 0.5–2.5 in normal breathing and 0.5–1.6 in deep breathing [24]. We had obtained benefit at this point, as it had utilized the patient’s normal side as a reference standard for the affected copula, but this benefit had been lacking in cases with bilateral affection of the diaphragmatic copulas (those who were excluded from our study).
Ultrasound had been proved as a clinically valuable diagnostic modality, but it did have some limitations. The first one was being an examiner-dependent technique, and the second one was a relatively low number of cases presented by hernia and defects. In our study, which might be taken in consideration, in spite of the high obtained accuracy measures, thus, further research with a larger sample volume for hernia and defects should be proposed; the last one was that the measurement of the excursion depends on the maximum voluntary inspiration done by the patients, and this consequently had limited the interpretative data and the usage of general cut-off values of the amplitudes of excursion in a non-homogenous population sample; however, this factor was related to the patient compliance and general condition; thus, a conscious and cooperative patient can help to obtain a maximal inspiratory effort, and the left-right side comparison had provided good control in our study where only one side was a dysfunctional.
