Journal of Respiratory Medicine

Journal of Respiratory Medicine / 2014 / Article

Research Article | Open Access

Volume 2014 |Article ID 683852 | 6 pages | https://doi.org/10.1155/2014/683852

Explorations of Unilateral Diaphragmatic Paralysis

Academic Editor: Norman R. Morris
Received19 May 2013
Revised02 Feb 2014
Accepted10 Feb 2014
Published01 Apr 2014

Abstract

Objective. The aim of the present study was to evaluate sniff test, maximal inspiratory pressure, and presence of paradoxical inspiratory diaphragmatic movements and their diagnostic value in patients referred for suspicion of diaphragmatic dysfunction. Methods. Twenty-two patients (8 men and 14 women, years) with suspected diaphragmatic dysfunction were included. Pulmonary function test was evaluated by spirometry. Diaphragm dysfunction was diagnosed with unilateral phrenic nerve stimulation. Esophageal pressure was recorded during sniff test and maximal static inspiratory movements. Detection of paradoxical diaphragmatic movement was performed with anteroposterior projection of chest X-ray fluoroscopic video. Results. Phrenic nerve stimulation enabled diagnosis of diaphragmatic paralysis in 15 of the 22 patients. The remaining 7 patients had normal explorations. Lung volumes were significantly lower in patients with diaphragmatic paralysis than in control subjects, as maximal inspiratory pressure. No patient with normal diaphragmatic exploration had paradoxical inspiratory movement. The combined diagnostic value of reduced esophageal pressure during sniff test, reduced esophageal pressure during maximal static inspiratory movements, and presence of paradoxical inspiratory movement had a sensitivity of 87% and a specificity of 71%. Conclusion. Our results suggest that, in most cases, a combination of sniff test, maximal inspiratory pressure, and paradoxical inspiratory movement could help to diagnose diaphragmatic dysfunction. Nevertheless, phrenic nerve stimulation remains the best test for assessing diaphragmatic dysfunction.

1. Introduction

Diaphragmatic paralysis is common and may be due to infectious, iatrogenic, or malignant causes, although the most common is frigore paralysis. Damage to the diaphragm or the phrenic nerve decreases inspiratory pressure, leading to diaphragmatic weakness and reduction in inspiratory muscle capacity [1] and lung volume, which in turn impair respiratory muscle endurance [2] and produce dyspnea [3]. Diaphragmatic dysfunction should thus be considered as a differential diagnosis of unexplained dyspnea, but its definitive diagnosis is difficult to assert. Definitive diagnosis can be obtained by phrenic nerve stimulation combined with measurement of twitch transdiaphragmatic pressure [4, 5], but the technique may be difficult in some patients. In clinical practice, suspicion of diaphragmatic paralysis is usually based on diaphragmatic curse during diaphragmatic fluoroscopic examination [6], inspiratory muscle strength evaluated by sniff test and maximal inspiratory pressure, and phrenic nerve stimulation [7]. Nevertheless, the relative value of the different explorations, as well as their place in the diagnosis of diaphragmatic paralysis, has not yet been clearly established. Therefore, the aim of the present study was to evaluate their diagnostic value in patients with diaphragmatic paralysis diagnosed by phrenic nerve stimulation.

2. Methods

2.1. Patients

Twenty-two patients with suspicion of diaphragmatic dysfunction (8 men and 14 women, 58 ± 13 years) were retrospectively included in the study, from 2008 to 2012. Criteria for inclusion were suspicion of diaphragmatic dysfunction due to phrenic nerve paralysis. The patients did not suffer from other muscular or neurologic disorders and had no contraindication to undergoing magnetic stimulation.

2.2. Measurements

Lung volume, spirometry, and flow-volume curves were measured according to standard guidelines and expressed as percentages of published values [8] (MasterScreen Body Plethysmograph, Carefusion, San Diego, CA).

After insertion of an esophageal balloon catheter and a gastric balloon catheter (70 cm long catheter; 1.4 mm external diameter; Marquat, Boissy Saint Léger, France), esophageal and gastric pressures [9] were measured in cmH2O with differential pressure transducer (DA 100C, Biopac Systems Inc., Santa Barbara, CA) [10]. Sniff maneuvers were performed at end of expiration with the patient in seated position. Patients were asked to perform sharp and maximal sniff maneuvers until peak esophageal pressure no longer increased. Maneuvers were only retained if sniff inspiratory time was under 0.5 seconds. Maximum sniff efforts were encouraged verbally and patients performed three series of five to ten sniffs, separated by at least 30 seconds [10]. Maximal static inspiratory pressure was measured from functional residual capacity (FRC) while seated and wearing a nose clip. Maximum inspiratory efforts were also encouraged verbally. Three maneuvers were performed separated by at least 30-second rest and continued until no further increase in pressure could be obtained [11].

Sniff test was considered as pathological if under 70 cmH2O for men and 60 cmH2O for women [1113]. Maximal static inspiratory pressure (MIF) was measured from FRC while seated and wearing a nose clip [14]. MIF was considered as pathological if under 80 cmH2O for men and 70 cmH2O for women [11, 1315]. Sniff maneuvers and maximal inspiratory pressure were performed before phrenic nerve stimulations with a 10-minute delay to avoid potentiation [16]. Diaphragm stimulations were performed using magnetic stimulation as previously described [17]. Briefly, bilateral phrenic nerve magnetic stimulations were performed at end expiratory time using a Magstim 200 stimulator powering a 90 mm circular coil (2.5 Tesla maximal output) (Magstim Ltd., Whitland, UK). The coil was placed at C7 level and three supramaximal reproducible stimulations were retained. Unilateral magnetic phrenic nerve stimulations (right and left phrenic nerve stimulations) were performed with a 43 mm branding iron type figure eight coil (Magstim Ltd., Whitland, UK), according to the technique described by Mills et al. [18]. A diagnosis of unilateral diaphragmatic paralysis was defined as a decrease of under 10 cmH2O in transdiaphragmatic pressure (Pdi) in response to unilateral phrenic nerve stimulation (ums) [13].

Anteroposterior projection fluoroscopic images were acquired with a radio amplifier (Flexiview 8800, General Electric, United Medical Technologies Corp., Fort Myers, FL) and recorded on a computer at 12 frames per second for later analysis (MMS, Tubingen, The Netherlands). Two sequences were recorded for each hemidiaphragm and two sequences were performed with the entire diaphragm in the field. The patients were in an upright position during testing and were asked to perform sharp and strong sniffs as previously learned during sniff test. A paradoxical inspiratory movement was defined as an inspiratory elevation of one hemidiaphragm during normal movement of the other hemidiaphragm, that is, a descent during the sharp sniff [19].

2.3. Data Analysis

Esophageal pressure amplitudes were measured from baseline to peak. Maximal sniff esophageal pressures (Pes, sniff) and maximal static inspiratory pressure (Pes, mip) were retained for analysis. Maximal esophageal and gastric pressures induced by phrenic nerve cervical magnetic stimulation were measured to calculate transdiaphragmatic pressure (Pdi) during cervical magnetic stimulation (CMS) or unilateral cervical stimulation (UMS) (resp., Pdi, cms and Pdi, ums). Presence or absence of paradoxical diaphragmatic inspiratory movements was noted.

2.4. Statistics

Statistical analyses were performed using StatView 5.0 software (SAS Institute Inc.). All results are expressed as means ± standard error (SE). Differences between the two groups of patients were analyzed with nonparametric Mann-Whitney test and were considered significant when the probability of a type I error was 0.05 or less. Sensitivity and specificity were calculated for each test, with diaphragmatic dysfunction being defined by a pathological Pdi measurement in response to unilateral phrenic nerve stimulation.

3. Results

The results of transdiaphragmatic pressure (Pdi) measurement in response to unilateral phrenic nerve stimulation enabled diagnosis of 15 diaphragmatic paralyses and 7 normal explorations. Ten of the 15 diaphragmatic paralyses had right diaphragmatic dysfunction and five had left diaphragmatic dysfunction. Vital capacity (VC), forced expiratory volume in one second (FEV1), FRC, Pes, mip, Pes, sniff, Pdi, ums, Pdi, cms, and videofluoroscopy results are summarized in Table 1.


Age Paralysis side VC FEV1 FRC Pes, sniff Pes, mip Pdi, cms Pdi, ums (left) Pdi, ums (right)Paradox
(years)Left/right/no (% pred) (% pred) (% pred) (cmH2O) (cmH2O) (cmH2O) (cmH2O)(cmH2O)(y/n)

Patients with diaphragmatic paralysis
#158Right 28.5 25.1 # 42 32 8.0 6.0 5.0 y
#266Right 84.4 76.8 72.8 71 47 13.0 12.0 4.0 y
#365Right 100.0 100.0 100.0 54 69 10.6 7.4 4.0 y
#467Right 34.1 40.5 83.5 53 70 5.0 10.0 4.0 y
#571Right 71.3 60.5 143.8 60 44 10.0 5.0 0.0 n
#664Right 57.3 58.9 54.0 57 61 3.0 6.0 3.0 y
#746Left 106.6 93.8 88.8 100 85 13.0 8.0 20.0 n
#868Right 88.8 61.7 64.8 48 # 6.0 8.0 4.0 y
#962Left 85.1 86.0 68.2 65 69 18.0 9.0 19.0 n
#1072Left 115.8 117.3 93.5 110 82 20.0 6.0 6.0 n
#1175Right 106.7 89.7 95.0 71 63 20.0 11.0 8.0 n
#1274Right 92.5 75.3 109.5 72 72 17.7 9.6 7.1 n
#1359Left 70.7 75.9 50.1 70 74 18.0 4.0 5.0 y
#1452Right 79.6 80.2 67.4 71 89 13.0 6.0 8.0 y
#1556Left 73.0 70.1 178.8 91 69 21.0 8 8.0 n
Mean ± SE

Patients without diaphragmatic paralysis
#1651 No 107.2 97.3 106.0 92 90 34.0 19.0 15.0 n
#1738 No 95.5 90.0 104.2 75 75 32.0 18.3 19.9 n
#1832 No 96.4 93.8 88.7 116 91 25.0 25.0 23.0 n
#1974 No 92.3 95.8 98.0 67 53 23.0 13.0 12.0 n
#2041 No 107.8 102.3 92.5 80 122 36.0 19.0 16.0 n
#2142 No 99.3 100.0 114.1 84 # 29.0 18.0 13.0 n
#2244 No 87.4 89.6 115.4 61 73 18.0 15.0 16.0 n
Mean ± SE
value<0,010,050,010,10,080,05<0,01<0,01<0,01

VC: vital capacity.
FEV1: forced expiratory volume in one second.
FRC: functional residual capacity.
Pes, sniff: esophageal pressure during strong sniff.
Pes, mip: maximal esophageal inspiratory pressure.
Pdi, cms: transdiaphragmatic pressure induced by cervical bilateral phrenic nerve magnetic stimulation.
Pdi, ums: transdiaphragmatic pressure induced by unilateral phrenic nerve magnetic stimulation.

3.1. Pulmonary Function Tests

Results are presented in Table 1. There was a significant difference between the two groups for FEV1 () and VC (). FRC tended to be lower in patients with diaphragmatic paralysis, but difference was not statistically significant ().

3.2. Diaphragmatic Strength

Pes, sniff was not statistically lower in patients with diaphragmatic paralysis (resp., 82.1 ± 6.8 cmH2O versus 69 ± 4.9 cmH2O, ). Pes, mip and Pdi, cms were higher in patients with no diaphragmatic paralysis than in patients with diaphragmatic paralysis (resp., 84.0 ± 9.5 cmH2O versus 66.1 ± 4.3 cmH2O, , and 28.1 ± 2.4 cmH2O versus 13.1 ± 1,5 cmH2O, (Figure 1)). Two patients did not correctly perform the maneuver to obtain maximal inspiratory pressure. Pdi, ums was not different between right and left side in patients with normal explorations (right: 16.4 ± 1.5 cmH2O, left: 18.2 ± 1.4 cmH2O, ). Pdi, ums was significantly lower in patients with diaphragmatic paralysis, for both sides (Figure 2). Sensitivity and specificity were, respectively, 53% and 100% for Pes, sniff, 67% and 71% for Pes, mip, and 93% and 86% for Pdi, cms.

3.3. Diaphragmatic Movements

On diaphragm radioscopy, no patient with normal diaphragmatic exploration had paradoxical inspiratory movement. In patients with diaphragmatic paralysis, eight experienced paradoxical inspiratory movement and seven normal diaphragmatic curse for the paralyzed hemidiaphragm. Sensitivity was therefore 53% and specificity 100%.

When Pes, sniff was abnormal, Pes, mip was abnormal and presence of a paradoxical inspiratory movement was noted; sensitivity was calculated at 87% and specificity at 71% for diaphragmatic dysfunction diagnosis.

4. Discussion

This study demonstrated that diaphragmatic paralysis induced respiratory muscle weakness and paradoxical inspiratory movements of the paralyzed hemidiaphragm in a majority of patients with good sensitivity. Nevertheless, phrenic nerve stimulation remains the gold standard method for diagnosis of diaphragmatic paralysis.

While numerous methods have been proposed for diagnosing diaphragmatic paralysis and diaphragmatic weakness, magnetic phrenic nerve stimulation [12], either unilateral [15] or bilateral [20, 21], is currently the most precise technique for diagnosing phrenic nerve paralysis [2, 12] or diaphragmatic weakness [12, 22]. The major difficulty in diaphragmatic explorations is that there are no cut-off values for clear separation of “normal” and “pathological” explorations. Hart et al. proposed a Pdi, ums of less than 3.5 cmH2O [2]. This cut-off was arbitrarily chosen, and the authors acknowledged that, with such a low value, only severe diaphragm weakness would be diagnosed as “diaphragm paralysis.” Luo et al. investigated the value of Pdi, cms on normal subjects and found it to be 28 ± 5 cmH2O [23]. From this study, Steier et al. [24] proposed as cut-off value 18 cmH2O for Pdi, cms, but did not mention Pdi, ums. Recently, a review [13], proposed a cut-off value of 10 cmH2O for Pdi, ums and 20 cmH2O for Pdi, cms to diagnose clinically significant diaphragmatic weakness, which we decided to take into account. Differences in diaphragmatic strengths obtained after bilateral phrenic nerve stimulation compared to unilateral phrenic nerve stimulation observed in our study have been previously described and can be explained by the stabilizing effect of cervical magnetic stimulations on the rib cage [25]. It should be noted that the relatively low number of patients included in the present study is due to the fact that inclusion criteria were difficult to achieve for many patients. In particular Pdi, cms and Pdi, ums were very often lacking, with patients not achieving test completion.

Our results confirm that mobilizable lung volumes are lower in cases of diaphragmatic dysfunction, in absence of any other pulmonary diseases. Consequently, pulmonary function tests are useful as a first approach and to ensure easily led follow-up of patients suffering from diaphragmatic dysfunction. Nevertheless, normal pulmonary function test is unable to rule out diaphragmatic dysfunction. In our study, Pes, sniff was the only test which allowed assessment of diaphragmatic dysfunction when abnormal with no false positive, but with subsequent false negatives [26]. It seems from the report that sniff transdiaphragmatic pressure can be higher than maximal static transdiaphragmatic pressure [27, 28], although conflicting results have been reported in controls [29] and in patients [30].

Diaphragmatic video fluoroscopy can provide dynamic information on diaphragmatic movement. A study performed on inspiratory-expiratory radiographs obtained from 350 subjects aged between 30 and 80 years, during quiet tidal breathing in an erect position, and without evidence of respiratory disease, found mean tidal excursions of the domes of the right and left hemidiaphragms to be 3.3 and 3.5 cm, respectively [31]. Tidal diaphragmatic movement was on average 0.5 cm lower in women than in men. Despite similar mean values, unequal movement of the two hemidiaphragmatic domes in an individual subject is common, most commonly greater on the right [32, 33]. Unilateral diaphragm paralysis is easier to detect because there is paradoxical motion during tidal inspiration, with ascent of the paralyzed dome, contrasting with descent of the normal hemidiaphragm; this contrast can be amplified by sniff test, which induces a vigorous, short contraction in the normal hemidiaphragm [34]. In our study, paradoxical motion, such as Pes, Sniff, has excellent specificity, but lower sensitivity. Its presence can enable assessment of the existence of diaphragmatic dysfunction, but this exploration can be proved wrong for moderate dysfunction of a hemidiaphragm, or on the contrary for severe bilateral paralysis.

As seen above, no one single exploration (Pes, sniff, Pes, mip, search for paradoxical motion during sniff manoeuvre) is relevant in the diagnosis of diaphragmatic dysfunction, due to numerous false negatives, except Pdi, ums or Pdi cms measurements. Nevertheless, combining Pes, sniff, Pes, mip and paradoxical motion allows obtention of high sensitivity, at 87%. Consequently, a combination of easily performed, noninvasive explorations, confronted with clinical context, is very useful. Phrenic nerve stimulation should therefore be used for uncommon cases, when clinical argument is insufficient for diagnosis of diaphragmatic weakness, or when it is necessary to give the precise level of diaphragmatic paralysis.

In conclusion, our results suggest that, in most cases, combining Pes, sniff, Pes, mip measurements and diaphragmatic videofluoroscopy in search of an eventual paradoxical inspiratory diaphragmatic movement during sniff maneuvers is useful to manage suspicion of diaphragmatic dysfunction. However, phrenic nerve stimulation remains the best exploration to confirm diagnosis.

Disclosure

Neither funding nor grants nor equipment was provided for the project by any source; there was no financial profit for the authors. There has been no previous presentation of the research, paper, or abstract in any form.

Conflict of Interests

The authors declare that there is no conflict of interests.

Acknowledgment

The authors are grateful to Nikki Sabourin-Gibbs, Rouen University Hospital, for editing the paper.

References

  1. C. M. Laroche, A. K. Mier, J. Moxham, and M. Green, “Diaphragm strength in patients with recent hemidiaphragm paralysis,” Thorax, vol. 43, no. 3, pp. 170–174, 1988. View at: Google Scholar
  2. N. Hart, A. H. Nickol, D. Cramer et al., “Effect of severe isolated unilateral and bilateral diaphragm weakness on exercise performance,” American Journal of Respiratory and Critical Care Medicine, vol. 165, no. 9, pp. 1265–1270, 2002. View at: Publisher Site | Google Scholar
  3. C. M. Laroche, N. Carroll, J. Moxham, and M. Green, “Clinical significance of severe isolated diaphragm weakness,” American Review of Respiratory Disease, vol. 138, no. 4, pp. 862–866, 1988. View at: Google Scholar
  4. M. Aubier, D. Murciano, Y. Lecocguic, N. Viires, and R. Pariente, “Bilateral phrenic stimulation: a simple technique to assess diaphragmatic fatigue in humans,” Journal of Applied Physiology, vol. 58, no. 1, pp. 58–64, 1985. View at: Google Scholar
  5. T. Similowsky, B. Fleury, S. Launois, H. P. Cathala, P. Bouche, and J.-P. Derenne, “Cervical magnetic stimulation (SMC). A new method of bilateral phrenic nerve stimulation usable in clinical practice,” Revue des Maladies Respiratoires, vol. 5, no. 6, pp. 609–614, 1988. View at: Google Scholar
  6. G. J. Gibson, “Diaphragmatic paresis: pathophysiology, clinical features, and investigation,” Thorax, vol. 44, no. 11, pp. 960–970, 1989. View at: Google Scholar
  7. E. Verin, J. Marie, C. Tardif, and P. Denis, “Spontaneous recovery of diaphragmatic strength in unilateral diaphragmatic paralysis,” Respiratory Medicine, vol. 100, no. 11, pp. 1944–1951, 2006. View at: Publisher Site | Google Scholar
  8. P. H. Quanjer, G. J. Tammeling, J. E. Cotes, O. F. Pedersen, R. Peslin, and J. C. Yernault, “Lung volumes and forced ventilatory flows. Report Working Party Standardization of Lung Function Tests, European Community for Steel and Coal. Official Statement of the European Respiratory Society,” The European Respiratory Journal. Supplement, vol. 16, pp. 5–40, 1993. View at: Google Scholar
  9. A. Baydur, P. K. Behrakis, and W. A. Zin, “A simple method for assessing the validity of the esophageal balloon technique,” American Review of Respiratory Disease, vol. 126, no. 5, pp. 788–791, 1982. View at: Google Scholar
  10. F. Héritier, F. Rahm, P. Pasche, and J. Fitting, “Sniff nasal inspiratory pressure: a noninvasive assessment of inspiratory muscle strength,” American Journal of Respiratory and Critical Care Medicine, vol. 150, no. 6, part 1, pp. 1678–1683, 1994. View at: Google Scholar
  11. N. Syabbalo, “Assessment of respiratory muscle function and strength,” Postgraduate Medical Journal, vol. 74, no. 870, pp. 208–215, 1998. View at: Google Scholar
  12. C. Uldry and J.-W. Fitting, “Maximal values of sniff nasal inspiratory pressure in healthy subjects,” Thorax, vol. 50, no. 4, pp. 371–375, 1995. View at: Google Scholar
  13. F. D. McCool and G. E. Tzelepis, “Dysfunction of the diaphragm,” The New England Journal of Medicine, vol. 366, no. 10, pp. 932–942, 2012. View at: Publisher Site | Google Scholar
  14. L. F. Black and R. E. Hyatt, “Maximal respiratory pressures: normal values and relationship to age and sex,” American Review of Respiratory Disease, vol. 99, no. 5, pp. 696–702, 1969. View at: Google Scholar
  15. C. Bruschi, I. Cerveri, M. C. Zoia et al., “Reference values of maximal respiratory mouth pressures: a population-based study,” American Review of Respiratory Disease, vol. 146, no. 3, pp. 790–793, 1992. View at: Google Scholar
  16. “ATS/ERS Statement on respiratory Muscle Testing,” American Journal of Respiratory and Critical Care Medicine, vol. 166, pp. 518–624, 2002. View at: Google Scholar
  17. T. Similowski, B. Fleury, S. Launois, H. P. Cathala, P. Bouche, and J. P. Derenne, “Cervical magnetic stimulation: a new painless method for bilateral phrenic nerve stimulation in conscious humans,” Journal of Applied Physiology, vol. 67, no. 4, pp. 1311–1318, 1989. View at: Google Scholar
  18. G. H. Mills, D. Kyroussis, C.-H. Hamnegard, S. Wragg, J. Moxham, and M. Green, “Unilateral magnetic stimulation of the phrenic nerve,” Thorax, vol. 50, no. 11, pp. 1162–1172, 1995. View at: Google Scholar
  19. M. J. Tobin, “Respiratory muscles in disease,” Clinics in Chest Medicine, vol. 9, no. 2, pp. 263–286, 1988. View at: Google Scholar
  20. G. H. Mills, D. Kyroussis, C. H. Hamnegard, M. I. Polkey, M. Green, and J. Moxham, “Bilateral magnetic stimulation of the phrenic nerves from an anterolateral approach,” American Journal of Respiratory and Critical Care Medicine, vol. 154, no. 4, part 1, pp. 1099–1105, 1996. View at: Google Scholar
  21. T. Similowski, C. Straus, V. Attali, A. Duguet, B. Jourdain, and J. Derenne, “Assessment of the motor pathway to the diaphragm using cortical and cervical magnetic stimulation in the decision-making process of phrenic pacing,” Chest, vol. 110, no. 6, pp. 1551–1557, 1996. View at: Google Scholar
  22. A. Teixeira, P. Cherin, A. Demoule et al., “Diaphragmatic dysfunction in patients with idiopathic inflammatory myopathies,” Neuromuscular Disorders, vol. 15, no. 1, pp. 32–39, 2005. View at: Publisher Site | Google Scholar
  23. Y. M. Luo, N. Hart, N. Mustfa et al., “Reproducibility of twitch and sniff transdiaphragmatic pressures,” Respiratory Physiology and Neurobiology, vol. 132, no. 3, pp. 301–306, 2002. View at: Publisher Site | Google Scholar
  24. J. Steier, S. Kaul, J. Seymour et al., “The value of multiple tests of respiratory muscle strength,” Thorax, vol. 44, pp. 990–996, 1989. View at: Google Scholar
  25. T. Similowski, C. Straus, V. Attali, A. Duguet, and J. Derenne, “Cervical magnetic stimulation as a method to discriminate between diaphragm and rib cage muscle fatigue,” Journal of Applied Physiology, vol. 84, no. 5, pp. 1692–1700, 1998. View at: Google Scholar
  26. G. H. Mills, D. Kyroussis, C. Hamnegard et al., “Cervical magnetic stimulation of the phrenic nerves in bilateral diaphragm paralysis,” American Journal of Respiratory and Critical Care Medicine, vol. 155, no. 5, pp. 1565–1569, 1997. View at: Google Scholar
  27. J. M. Miller, J. Moxham, and M. Green, “The maximal sniff in the assessment of diaphragm function in man,” Clinical Science, vol. 69, no. 1, pp. 91–96, 1985. View at: Google Scholar
  28. C. M. Laroche, A. K. Mier, J. Moxham, and M. Green, “The value of sniff esophageal pressures in the assessment of global inspiratory muscle strenght,” American Review of Respiratory Disease, vol. 138, no. 3, pp. 598–603, 1988. View at: Google Scholar
  29. Y. F. Heijdra, P. N. R. Dekhuijzen, C. L. A. van Herwaarden, and H. T. M. Folgering, “Differences between sniff mouth pressures and static maximal inspiratory mouth pressures,” European Respiratory Journal, vol. 6, no. 4, pp. 541–546, 1993. View at: Google Scholar
  30. F. Heritier, C. Perret, and J.-W. Fitting, “Maximal sniff mouth pressure compared with maximal inspiratory pressure in acute respiratory failure,” Chest, vol. 100, no. 1, pp. 175–178, 1991. View at: Google Scholar
  31. E. A. Lennon and G. Simon, “The height of the diaphragm in the chest radiograph of normal adults,” British Journal of Radiology, vol. 38, no. 456, pp. 937–943, 1965. View at: Google Scholar
  32. D. A. Young and G. Simon, “Certain movements measured on inspiration-expiration chest radiographs correlated with pulmonary function studies,” Clinical Radiology, vol. 23, no. 1, pp. 37–41, 1972. View at: Google Scholar
  33. I. Y. Ch'en and J. D. Armstrong II, “Value of fluoroscopy in patients with suspected bilateral hemidiaphragmatic paralysis,” American Journal of Roentgenology, vol. 160, no. 1, pp. 29–31, 1993. View at: Google Scholar
  34. J. G. Houston, M. Fleet, M. D. Cowan, and N. C. McMillan, “Comparison of ultrasound with fluoroscopy in the assessment of suspected hemidiaphragmatic movement abnormality,” Clinical Radiology, vol. 50, no. 2, pp. 95–98, 1995. View at: Google Scholar

Copyright © 2014 Alexandre Quesnel et al. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.


More related articles

2732 Views | 421 Downloads | 1 Citation
 PDF  Download Citation  Citation
 Download other formatsMore
 Order printed copiesOrder

Related articles

We are committed to sharing findings related to COVID-19 as quickly and safely as possible. Any author submitting a COVID-19 paper should notify us at help@hindawi.com to ensure their research is fast-tracked and made available on a preprint server as soon as possible. We will be providing unlimited waivers of publication charges for accepted articles related to COVID-19. Sign up here as a reviewer to help fast-track new submissions.