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Diaphragmatic Motion Studied by M-mode Ultrasonography in Combined Pulmonary Fibrosis and Emphysema

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Abstract

Background

The coexistence of emphysema and pulmonary fibrosis is known as combined pulmonary fibrosis and emphysema (CPFE). The aim of this study was to compare diaphragmatic motion measured by M-mode ultrasonography of patients with CPFE, idiopathic pulmonary fibrosis (IPF), and chronic obstructive pulmonary disease (COPD).

Methods

Pulmonary function, high-resolution computed tomography (HRCT), and diaphragmatic motion were examined in patients with CPFE (n = 25), IPF (n = 18), and COPD (n = 60), and in healthy controls (n = 21). Diaphragmatic motions were measured on M-mode ultrasonographic images during quiet breathing and deep breathing.

Results

There were no significant differences in right or left diaphragmatic motion during quiet breathing among the four groups, whereas differences were significant in right and left motion during deep breathing. Diaphragmatic motion in CPFE patients was the lowest among the four groups. COPD patients, especially those with severe COPD, showed significantly lower diaphragmatic motion than IPF patients or healthy controls. There were no differences in diaphragmatic motion between IPF patients and healthy controls. Right diaphragmatic motions during deep breathing were negatively correlated with emphysema scores (r = −0.606, p < 0.001), but were not correlated with fibrosis scores on HRCT.

Conclusions

Diaphragmatic weakness was found in CPFE patients. Emphysema but not fibrosis may be one cause of limited diaphragmatic motion in patients with CPFE. M-mode ultrasonographic evaluation of diaphragmatic motion during deep breathing may be a useful tool in diagnosing CPFE and in discriminating CPFE patients from IPF or COPD patients.

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References

  1. Donaldson AV, Maddocks M, Martolini D, Polkey MI, Man WD (2012) Muscle function in COPD: a complex interplay. Int J Chron Obstruct Pulmon Dis 7:523–535. doi:10.2147/COPD.S28247

    PubMed Central  PubMed  Google Scholar 

  2. Glerant JC, Mustfa N, Man WD, Luo YM, Rafferty G, Polkey MI, Moxham J (2006) Diaphragm electromyograms recorded from multiple surface electrodes following magnetic stimulation. Eur Respir J 27(2):334–342

    Article  CAS  PubMed  Google Scholar 

  3. Mageras GS, Yorke E, Rosenzweig K, Braban L, Keatley E, Ford E, Leibel SA, Ling CC (2001) Fluoroscopic evaluation of diaphragmatic motion reduction with a respiratory gated radiotherapy system. J Appl Clin Med Phys 2(4):191–200

    Article  CAS  PubMed  Google Scholar 

  4. Boussuges A, Gole Y, Blanc P (2009) Diaphragmatic motion studied by m-mode ultrasonography: methods, reproducibility, and normal values. Chest 135(2):391–400. doi:10.1378/chest.08-1541

    Article  PubMed  Google Scholar 

  5. Paulin E, Yamaguti WP, Chammas MC, Shibao S, Stelmach R, Cukier A, Carvalho CR (2007) Influence of diaphragmatic mobility on exercise tolerance and dyspnea in patients with COPD. Respir Med 101(10):2113–2118

    Article  CAS  PubMed  Google Scholar 

  6. Papiris SA, Triantafillidou C, Manali ED, Kolilekas L, Baou K, Kagouridis K, Bouros D (2013) Combined pulmonary fibrosis and emphysema. Expert Rev Respir Med 7(1):19–31; quiz 32. doi:10.1586/ers.12.80

  7. Qaseem A, Wilt TJ, Weinberger SE et al (2011) Diagnosis and management of stable chronic obstructive pulmonary disease: a clinical practice guideline update from the American College of Physicians, American College of Chest Physicians, American Thoracic Society, and European Respiratory Society. Ann Intern Med 155(3):179–191. doi:10.7326/0003-4819-155-3-201108020-00008

    Article  PubMed  Google Scholar 

  8. Raghu G, Collard HR, Egan JJ et al (2011) ATS/ERS/JRS/ALAT Committee on Idiopathic Pulmonary Fibrosis. An official ATS/ERS/JRS/ALAT statement: idiopathic pulmonary fibrosis: evidence-based guidelines for diagnosis and management. Am J Respir Crit Care Med 15;183(6):788–824. doi:10.1164/rccm

  9. Miller MR, Hankinson J, Brusasco V et al (2005) ATS/ERS Task Force. Standardisation of spirometry. Eur Respir J 26(2):319–338

    Article  CAS  PubMed  Google Scholar 

  10. Ginghină C, Muraru D, Vlădaia A et al (2009) Doppler flow patterns in the evaluation of pulmonary hypertension. Rom J Intern Med 47(2):109–121

    PubMed  Google Scholar 

  11. Mori K, Shirai T, Mikamo M, Shishido Y, Akita T, Morita S, Asada K, Fujii M, Hozumi H, Suda T, Chida K (2013) Respiratory mechanics measured by forced oscillation technique in combined pulmonary fibrosis and emphysema. Respir Physiol Neurobiol 185(2):235–240. doi:10.1016/j.resp.2012.10.009

    Article  PubMed  Google Scholar 

  12. Hozumi H, Nakamura Y, Johkoh T, Sumikawa H, Colby TV, Karayama M, Hayakawa H, Yokomura K, Imokawa S, Yasuda K, Toyoshima M, Suganuma H, Shirai T, Inui N, Suda T, Nakamura H, Chida K (2011) Nonspecific interstitial pneumonia: prognostic significance of high-resolution computed tomography in 59 patients. J Comput Assist Tomogr 35(5):583–589. doi:10.1097/RCT.0b013e31822a5883

    Article  PubMed  Google Scholar 

  13. Kitaguchi Y, Fujimoto K, Hanaoka M, Kawakami S, Honda T, Kubo K (2010) Clinical characteristics of combined pulmonary fibrosis and emphysema. Respirology 15(2):265–271. doi:10.1111/j.1440-1843.2009.01676.x

    Article  PubMed  Google Scholar 

  14. Kantarci F, Mihmanli I, Demirel MK, Harmanci K, Akman C, Aydogan F, Mihmanli A, Uysal O (2004) Normal diaphragmatic motion and the effects of body composition: determination with M-mode sonography. J Ultrasound Med 23(2):255–260

    PubMed  Google Scholar 

  15. Nason LK, Walker CM, McNeeley MF, Burivong W, Fligner CL, Godwin JD (2012) Imaging of the diaphragm: anatomy and function. Radiographics 32(2):E51–E70. doi:10.1148/rg.322115127

    Article  PubMed  Google Scholar 

  16. Brennan NJ, Morris AJ, Green M (1983) Thoracoabdominal mechanics during tidal breathing in normal subjects and in emphysema and fibrosing alveolitis. Thorax 38(1):62–66

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  17. Green M, Mead J, Sears TA (1978) Muscle activity during chest wall restriction and positive pressure breathing in man. Respir Physiol 35(3):283–300

    Article  CAS  PubMed  Google Scholar 

  18. McKenzie DK, Butler JE, Gandevia SC (2009) Respiratory muscle function and activation in chronic obstructive pulmonary disease. J Appl Physiol 107(2):621–629. doi:10.1152/japplphysiol.00163

    Article  PubMed  Google Scholar 

  19. Kawamoto H, Kambe M, Kuraoka T (2008) Evaluation of the diaphragm in patients with COPD (emphysema dominant type) by abdominal ultrasonography. Nihon Kokyuki Gakkai Zasshi 46(4):271–277

    PubMed  Google Scholar 

  20. Finucane KE, Singh B (2012) Diaphragm efficiency estimated as power output relative to activation in chronic obstructive pulmonary disease. J Appl Physiol 113(10):1567–1575. doi:10.1152/japplphysiol.01453.2011

    Article  PubMed  Google Scholar 

  21. Dos Santos Yamaguti WP, Paulin E, Shibao S, Chammas MC, Salge JM, Ribeiro M, Cukier A, Carvalho CR (2008) Air trapping: The major factor limiting diaphragm mobility in chronic obstructive pulmonary disease patients. Respirology 13(1):138–144. doi:10.1111/j.1440-1843.2007.01194.x

    Article  PubMed  Google Scholar 

  22. Kang HW, Kim TO, Lee BR, Yu JY, Chi SY, Ban HJ, Oh IJ, Kim KS, Kwon YS, Kim YI, Kim YC, Lim SC (2011) Influence of diaphragmatic mobility on hypercapnia in patients with chronic obstructive pulmonary disease. J Korean Med Sci 26(9):1209–1213. doi:10.3346/jkms.2011.26.9.1209

    Article  PubMed Central  PubMed  Google Scholar 

  23. Ponçot-Mongars R, Zysman M, Regent D, Gomez E, Chaouat A, Chabot F (2013) Combined pulmonary fibrosis and emphysema: the natural history of the disease. The chronological evolution of clinical features, respiratory function and the CT scan. Rev Mal Respir 30(3):222–226. doi:10.1016/j.rmr.2012.06.002

    Article  PubMed  Google Scholar 

  24. McCool FD, Tzelepis GE (2012) Dysfunction of the diaphragm. N Engl J Med 366(10):932–942. doi:10.1056/NEJMra1007236

    Article  CAS  PubMed  Google Scholar 

  25. Cottin V, Nunes H, Brillet PY et al (2005) Combined pulmonary fibrosis and emphysema: a distinct underrecognised entity. Eur Respir J 26(4):586–593

    Article  CAS  PubMed  Google Scholar 

  26. de Man FS, van Hees HW, Handoko ML, Niessen HW, Schalij I, Humbert M, Dorfmüller P, Mercier O, Bogaard HJ, Postmus PE, Westerhof N, Stienen GJ, van der Laarse WJ, Vonk-Noordegraaf A, Ottenheijm CA (2011) Diaphragm muscle fiber weakness in pulmonary hypertension. Am J Respir Crit Care Med 183(10):1411–1418. doi:10.1164/rccm.201003-0354OC

    Article  PubMed  Google Scholar 

  27. Ahn B, Empinado HM, Al-Rajhi M, Judge AR, Ferreira LF (2013) Diaphragm atrophy and contractile dysfunction in a murine model of pulmonary hypertension. PLoS One 8(4):e62702. doi:10.1371/journal.pone.0062702

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  28. Manders E, de Man FS, Handoko ML, Westerhof N, van Hees HW, Stienen GJ, Vonk-Noordegraaf A, Ottenheijm CA (2012) Diaphragm weakness in pulmonary arterial hypertension: role of sarcomeric dysfunction. Am J Physiol Lung Cell Mol Physiol 303(12):L1070–L1078. doi:10.1152/ajplung.00135.2012

    Article  CAS  PubMed  Google Scholar 

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Acknowledgments

This work was supported by grants from the National Natural Science Foundation of China (No. 30500224) and Science and Technology Bureau of Jingzhou, Hubei, China (No. [2009]13).

Conflict of interest

The authors have no conflicts of interest or financial ties to disclose.

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Authors and Affiliations

  1. Department of Respiratory Medicine, Jingzhou Hospital of Tongji Medical College, Huazhong University of Science and Technology, No. 1, Ren Min Road, JingZhou District, JingZhou, 434020, Hu Bei Province, China

    Li He, Jiahong Zhang, Jingping Ma, He Huang, Jinwu Zeng, Chuanbin Zhu & Jianhua Gong

  2. Department of Surgery, Tongji Hospital of Tongji Medical College, Huazhong University of Science and Technology, No. 1095, Jie Fang Road, Han Kou District, Wu Han, 430030, Hu Bei Province, China

    Wanguang Zhang

  3. Ultrasonographic Medicine, Jingzhou Hospital of Tongji Medical College, Huazhong University of Science and Technology, No. 1, Ren Min Road, JingZhou District, JingZhou, 434020, Hu Bei Province, China

    Le Cao & Lan Gong

  4. Department of Respiratory Medicine, Tongji Hospital of Tongji Medical College, Huazhong University of Science and Technology, No. 1095, Jie Fang Road, Han Kou District, Wu Han, 430030, Hu Bei Province, China

    Yongjian Xu, Zhenxiang Zhang, Jianping Zhao & Huilan Zhang

Authors
  1. Li He
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  2. Wanguang Zhang
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  3. Jiahong Zhang
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  5. Lan Gong
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  7. He Huang
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  9. Chuanbin Zhu
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  10. Jianhua Gong
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  11. Yongjian Xu
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  12. Zhenxiang Zhang
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  14. Huilan Zhang
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Corresponding author

Correspondence to Huilan Zhang.

Additional information

Li He and Wanguang Zhang contributed equally to this work.

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He, L., Zhang, W., Zhang, J. et al. Diaphragmatic Motion Studied by M-mode Ultrasonography in Combined Pulmonary Fibrosis and Emphysema. Lung 192, 553–561 (2014). https://doi.org/10.1007/s00408-014-9594-5

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  • DOI: https://doi.org/10.1007/s00408-014-9594-5

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