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* From the Research Centre (Dr. Bellemare) and Departments of Anesthesiology (Dr. Couture), Radiology (Dr. Cordeau), Pneumology (Dr. Leblanc), and Surgery (Dr. Lafontaine), Centre hospitalier de l’Université de Montréal, Hôtel-Dieu, Montréal, Québec, Canada.
Correspondence to: François Bellemare, PhD, Centre de recherche, Centre hospitalier de l’Université de Montréal, Hôtel-Dieu, 3850 rue St-Urbain, Montréal, Québec, Canada H2W 1T8; e-mail: francois.bellemare{at}umontreal.ca
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Abstract |
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Design: Prospective clinical trial with a parallel group design.
Setting: Laboratory investigations in normal volunteers recruited by advertisement and in emphysema outpatients being evaluated for elective bilateral lung volume reduction surgery (LVRS).
Patients: Twenty-six normal subjects classified into young and older age groups, with a third group of 13 emphysema patients matched for age and sex with the older group.
Measurements: Identification and between-group comparisons were made of anatomic landmarks on anteroposterior and lateral chest radiographs obtained at total lung capacity. Predicted landmarks were generated from normal subjects. Within-subject and between-group comparisons were made of diaphragm length index (DLI) based on observed anatomic landmarks (DLIobs) and diaphragm length index based on predicted anatomic landmarks (DLIpred) at functional residual capacity.
Results: Anatomic landmarks were not different between the three groups or between male and female subjects, and were not different before and after LVRS in emphysema patients. No difference was found between DLIobs and DLIpred in normal subjects and emphysema patients, but both were smaller in emphysema patients than in normal subjects and increased after LVRS in emphysema patients.
Conclusion: This study validates the use of anatomic landmarks to estimate DLI. Using these landmarks simplifies the determination of diaphragmatic lengths and could be a useful tool for the evaluation of the functional capacity of the diaphragm, and possibly as a prognostic indicator of patients who are candidates for LVRS.
Key Words: chest radiograph • diaphragm length • emphysema • lung volume reduction surgery
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Introduction |
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TOPAbstractIntroductionMaterials and MethodsResultsDiscussionConclusionReferences |
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While several imaging techniques, including CT4 5 and MRI,6 7 can measure diaphragm length, the method of Braun et al8 using chest radiographs is the only method that can be applied to subjects in an upright position. This is important, as diaphragm strength is usually evaluated in this position and both diaphragm length and shape change markedly from the upright position to the supine position, both factors that are known to affect its pressure-generating capacity.
The method of Braun et al8 has been shown to provide reproducible measures of diaphragm length that are comparable to those of excised diaphragms measured at necropsy. Furthermore, the relationship between maximal transdiaphragmatic pressure measured during voluntary8 or artificially excited contractions9 and diaphragm length measured this way closely approximates the classic length-tension relationship of diaphragm muscles studied in vitro. Therefore, the method is reliable. However, because it is based on the identification of diaphragmatic insertions on radiographs exposed at full, active lung inflation, it requires that subjects or patients be able to maximally inflate their lungs to a volume close to normal total lung capacity (TLC). Given this premise, the technique of Braun et al8 is not applicable in its present form to patients whose TLC is reduced by restrictive lung or chest wall diseases. In these patients, intersections of diaphragm silhouette with the chest wall on radiographs obtained at active TLC are unlikely to correspond to anatomic insertions of the diaphragm. As a consequence, diaphragm length could be systematically underestimated. The recent findings of Singh and colleagues,10 using the technique of shorter-than-normal diaphragm length in patients with asbestos-related pleural fibrosis and reduced TLC, support this suggestion.
The major objective of the present study was to determine whether anatomic landmarks can be defined to predict the points of insertions of the diaphragm on chest radiographs independently of the capacity of subjects to inflate their lungs to TLC, and to evaluate the error introduced by this procedure. Anatomic landmarks were defined and compared in a group of normal subjects and a group of patients presenting with severe emphysema and a low, flat diaphragm, some of whom also underwent lung volume reduction surgery (LVRS), the hypothesis being that diaphragmatic insertions and, hence, anatomic landmarks should be unaffected by severe lung hyperinflation or surgery.
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Materials and Methods |
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TOPAbstractIntroductionMaterials and MethodsResultsDiscussionConclusionReferences |
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45 years of age comprised the older
age group. The physical and pulmonary function characteristics
of the three groups are given in Table 1 .11
12
13
The older group and the emphysema group were
comparable for age and sex. Six of the emphysema patients underwent
elective bilateral LVRS via a median sternotomy approach as described
by Cooper et al.14
These six patients were reevaluated 3
months postoperatively, and five of these patients were reevaluated
again at 6 months and 12 months postoperatively, thus allowing
assessment of the reproducibility of our measurements.
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Determination of Anatomic Landmarks
Using the anteroposterior and lateral views obtained at TLC, we
first identified the points of intersection of the diaphragm silhouette
with the chest wall. The anterior and posterior points of intersection
were identified on the lateral views. The point of intersection of the
diaphragm silhouette with the lateral chest wall on the right side was
identified on anteroposterior views. These three points will be
referred to as the anterior, posterior, and lateral points of insertion
of the diaphragm on the chest wall. The following landmarks were then
defined for the anterior, posterior, and lateral insertions (Fig 1
, top).
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Landmark for Posterior Insertion:
The vertical distance
between this point of insertion and the base of T1 was measured as the
anatomic landmark for posterior insertion of the diaphragm. When the
level of T1 could not be identified on lateral views, its position was
transposed from the anteroposterior view using a midthoracic vertebra.
The landmark for posterior insertion was expressed as a ratio of the
vertical distance between the base of T1 and the base of T12.
Landmark for Lateral Insertion:
On anteroposterior
projections obtained at TLC, the diaphragm silhouette intersected the
chest wall on the right side at the level of the ninth or the 10th rib
laterally. As a landmark for this point of insertion, we measured its
vertical distance from the point at which the ninth and 10th ribs cross
over each other. This landmark was selected because it could always be
defined precisely.
Diaphragm Length Measurements
In all subjects, diaphragm length at functional residual
capacity (FRC) was first measured as described by Braun et
al,8
using the anatomic landmarks identified for each
subject on radiographs obtained at TLC and transposed to radiographs
obtained at FRC. The lengths of the diaphragm contours between the
anterior and posterior points of insertions on lateral projections and
between the lateral point of insertion to the center of the spine on
anteroposterior views films were then measured with a digitizing tablet
(Fig 1 , bottom). A diaphragmatic length index (DLI) of
observed anatomic landmarks (DLIobs) was then calculated as the sum of
the lengths of the diaphragm contours on the anteroposterior and
lateral projections divided by height.8
Diaphragm Length at FRC Using Predictors of Diaphragmatic
Insertions:
Predicted points of insertion were then calculated for
each subject using the average value of the anterior, posterior, and
lateral landmarks found in normal subjects. These average values in
normal subjects were referred to as the predictors of anterior,
posterior, and lateral insertions of the diaphragm. The predicted
points thus calculated were marked on radiographs obtained at FRC. The
distance along the chest wall between these predicted points of
insertion and the anatomic landmarks identified on radiographs obtained
at TLC was then measured and either added or subtracted from the
lengths of the diaphragm contours determined by observed landmarks,
thus yielding a new set of lengths for anteroposterior and lateral
projections obtained at FRC. This new set of lengths for diaphragm
contours then served to compute a DLI at FRC based on these predictors
(DLI based on predicted anatomic landmarks [DLIpred]). For comparison
with other studies using similar techniques, a correction factor of 0.9
for the magnification of the thoracic structures was applied to the
measured lengths.
Reproducibility of Measurements:
Interobserver and
intraobserver reproducibility was evaluated in the following way. For
interobserver reproducibility, 10 sets of radiographs from 10
consecutive subjects were evaluated once by two independent observers.
Each observer analyzed five sets of radiographs as the first observer,
erased all markings, and then analyzed the other five sets. For each
set of radiographs, each observer reported the anatomic landmarks on
radiographs obtained at TLC and the DLIpred measured on radiographs
obtained at FRC. For intraobserver reproducibility, the same sets of
radiographs were evaluated twice by the same observer at an interval of
1 week.
Statistical Analysis:
Descriptive statistics and a general
linear model analysis of variance (ANOVA) were used in between-group
comparisons of anatomic landmarks and of DLIs. Linear regressions and a
paired t test were employed in within-subject
comparisons of DLIobs and DLIpred. A paired t test was
used for interobserver and intraobserver reproducibility assessment.
The effects of LVRS on these variables were evaluated with ANOVA for
repeated measures. In all comparisons, a p value < 0.05 was
considered statistically significant. The average bias and limits of
agreement between the two methods of measuring diaphragm length were
determined by the method of Bland and Altman.16
Bias was
established as the difference between DLIobs and DLIpred and related to
the mean of the two measures. The upper and lower limits of agreement
between these two methods were assessed as ± 2 SD of the differences
between DLIobs and DLIpred. All statistical computations were performed
with commercially available software (SPSS Advanced Statistics v. 10
for Windows; SPSS; Chicago, IL).
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Results |
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TOPAbstractIntroductionMaterials and MethodsResultsDiscussionConclusionReferences |
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Discussion |
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Anatomic Landmarks and Diaphragmatic Insertions
As pointed out by Braun et al,8
the points of
intersection of the diaphragm silhouette with the chest wall on
radiographs obtained at active TLC appear to correspond to known
insertions of the diaphragm as determined at necropsy.17
Our finding of similar anatomic landmarks in normal subjects and
patients with severe emphysema that are not modified after LVRS gives
additional support to this assumption, since anatomic insertions of the
diaphragm clearly should not be modified by emphysema or surgery.
Because these anatomic landmarks appear to correspond to known anatomic
insertions of the diaphragm, they can be employed to estimate diaphragm
length from chest radiographs.
In the present study, we found good agreement between diaphragm length measured with observed and predicted landmarks. Both methods were equally sensitive in detecting differences in diaphragmatic length between normal subjects and emphysema patients as well as the change in DLI after LVRS. It therefore appears that the two methods can be used interchangeably in normal subjects and emphysema patients. This should not be the case in patients with restrictive lung or chest wall diseases, in whom the technique of Braun et al8 is likely to underestimate diaphragm length. For these patients, anatomic landmarks as reported in Table 2 could be used to define the insertions of the diaphragm and to measure its length. Comparison of DLIobs and DLIpred, as in Figure 3 , could also be employed to determine whether the measurements lie outside the predicted 95% confidence limits.
Although the use of anatomic landmarks was primarily intended for patients with restrictive lung or chest wall disorders, it need not be limited to this application. As our results show in patients undergoing LVRS, these anatomic landmarks are reproducible over time. Furthermore, because the technique does not rely on radiographs obtained at TLC, the determination of diaphragm length involves less radiation to the subject, more rapid performance, and lower cost. The technique may thus be useful when repeated DLI determinations in the same subjects are required.
Comparison With Other Studies
Our technique of obtaining chest radiographs differed somewhat
from earlier studies, in that our subjects stood on a platform with
their heads fixed to a backboard. Because of this constraint, an
anteroposterior projection was selected for the coronal view. We used
the platform as a way of standardizing the spinal attitude in all
subjects, as well as in the same subject on anteroposterior and lateral
projections. However, the effect of this constraint on DLI
determination was not evaluated. Comparison of DLI measurements with
published values obtained without this constraint suggests that the
effect, if any, is probably small. In their study of 22 normal
subjects, Braun et al8
reported a DLI at FRC of
0.25 ± 0.03 cm/cm. In four normal subjects investigated in the
seated posture, Prezant et al3
obtained a DLI at FRC of
0.26 ± 0.01 cm/cm. For 26 normal subjects, we recorded a DLI at FRC
of 0.27 ± 0.04 cm/cm, which is not significantly different from
previously published values.3
8
Furthermore, because the
diaphragm is not passively tensed at FRC in the upright posture, its
in situ length should be equal to the excised resting
length. The length of excised diaphragms has been measured by Braun et
al8
in 32 normal subjects at necropsy. The DLI of excised
diaphragms calculated using the greatest anteroposterior and
left-to-right diameters averaged 0.267 ± 0.024 cm/cm, a value almost
identical to that of our normal subjects at FRC. Our radiographic
technique, therefore, appears to provide reliable estimates of
diaphragm length.
It is also of interest to compare our length measurements with those obtained by other imaging techniques. Gauthier et al7 studied four normal subjects at different lung volumes by MRI. From their data, an average DLI at FRC of 0.37 cm/cm can be calculated. Cassart et al18 studied 10 normal subjects and 10 patients with severe emphysema by spiral CT. In their normal subjects, DLI at FRC was 0.41 cm/cm, which is only slightly greater than the value reported by Gauthier et al7 but 50% greater than in our normal subjects. For the emphysema patients examined by Cassart et al,18 a DLI at FRC of 0.32 cm/cm can be calculated, which is also about 50% greater than in the present study. The degree of pulmonary hyperinflation (ie, FRC) was comparable in the two investigations. The differences in DLI between our study and their study seem too large to be accounted for by the different imaging technique employed or by the characteristics of the subjects examined. We believe that most of this difference can be explained by the change in lung volume and diaphragm position that occurs in a gravitational field when a subject goes from the upright to the supine position. Our imaging technique, therefore, cannot be compared directly with their technique.
We confirmed the observation of Braun et al8 of comparable DLI in normal male and female subjects, thus supporting the normalization for height. We also confirmed earlier findings of shorter DLI in emphysema patients than in normal subjects at their respective lung volume.2 18 Because DLI increased after LVRS, the DLI difference between normal subjects and emphysema patients was reduced by this procedure, a factor that could explain the improvement in the pressure-generating capacity of the diaphragm reported after this type of surgery.19 Because the position of the diaphragm at active TLC was not modified by surgery, the longer initial length at FRC should also have increased the capacity of the diaphragm to shorten and to produce volume displacements. By improving the strength and shortening capacity of the diaphragm, the observed increase in DLI after LVRS could help explain the improved dyspnea seen after surgery in these patients.
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Conclusion |
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Acknowledgements |
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Footnotes |
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This study was supported by the Medical Research Council of Canada.
Received for publication July 17, 2000. Accepted for publication February 26, 2001.
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This article has been cited by other articles:
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  F. Bellemare, A. Jeanneret, and J. Couture Sex Differences in Thoracic Dimensions and Configuration Am. J. Respir. Crit. Care Med., August 1, 2003; 168(3): 305 - 312. [Abstract] [Full Text] [PDF]
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R. B. Gorman, D. K. McKenzie, N. B. Pride, J. F. Tolman, and S. C. Gandevia Diaphragm Length during Tidal Breathing in Patients with Chronic Obstructive Pulmonary Disease Am. J. Respir. Crit. Care Med., December 1, 2002; 166(11): 1461 - 1469. [Abstract] [Full Text] [PDF]
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