Computer tomographic analysis of organ motion caused by respiration and intraoperative pneumoperitoneum in a porcine model for navigated minimally invasive esophagectomy

  • Felix Nickel
  • Hannes G. Kenngott
  • Jochen Neuhaus
  • Nathanael Andrews
  • Carly Garrow
  • Johannes Kast
  • Christof M. Sommer
  • Tobias Gehrig
  • Carsten N. Gutt
  • Hans-Peter Meinzer
  • Beat P. Müller-Stich
Article
  • 31 Downloads

Abstract

Background

Navigation systems have the potential to facilitate intraoperative orientation and recognition of anatomical structures. Intraoperative accuracy of navigation in thoracoabdominal surgery depends on soft tissue deformation. We evaluated esophageal motion caused by respiration and pneumoperitoneum in a porcine model for minimally invasive esophagectomy.

Methods

In ten pigs (20–34 kg) under general anesthesia, gastroscopic hemoclips were applied to the cervical (CE), high (T1), middle (T2), and lower thoracic (T3) level, and to the gastroesophageal junction (GEJ) of the esophagus. Furthermore, skin markers were applied. Three-dimensional (3D) and four-dimensional (4D) computed tomography (CT) scans were acquired before and after creation of pneumoperitoneum. Marker positions and lung volumes were analyzed with open source image segmentation software.

Results

Respiratory motion of the esophagus was higher at T3 (7.0 ± 3.3 mm, mean ± SD) and GEJ (6.9 ± 2.8 mm) than on T2 (4.5 ± 1.8 mm), T1 (3.1 ± 1.8 mm), and CE (1.3 ± 1.1 mm). There was significant motion correlation in between the esophageal levels. T1 motion correlated with all other esophagus levels (r = 0.51, p = 0.003). Esophageal motion correlated with ventilation volume (419 ± 148 ml) on T1 (r = 0.29), T2 (r = 0.44), T3 (r = 0.54), and GEJ (r = 0.58) but not on CE (r = − 0.04). Motion correlation of the esophagus with skin markers was moderate to high for T1, T2, T3, GEJ, but not evident for CE. Pneumoperitoneum led to considerable displacement of the esophagus (8.2 ± 3.4 mm) and had a level-specific influence on respiratory motion.

Conclusions

The position and motion of the esophagus was considerably influenced by respiration and creation of pneumoperitoneum. Esophageal motion correlated with respiration and skin motion. Possible compensation mechanisms for soft tissue deformation were successfully identified. The porcine model is similar to humans for respiratory esophageal motion and can thus help to develop navigation systems with compensation for soft tissue deformation.

Keywords

Esophagectomy Minimally invasive surgery Navigation Soft tissue deformation Respiratory motion 

Abbreviations

2D

Two-dimensional

3D

Three-dimensional

4D

Four-dimensional

ABDskin

Abdominal skin level

CE

Cervical esophagus level

CT

Computed tomography scan

GEJ

Gastroesophageal junction

MIE

Minimally invasive esophagectomy

MITK

Medical Imaging Interaction Toolkit

NS

Navigation system

OR

Operating room

T1

High thoracic esophagus level

T2

Middle thoracic esophagus level

T3

Low thoracic esophagus level

T1skin

High thoracic skin level

T2skin

Middle thoracic skin level

T3skin

Low thoracic skin level

Notes

Acknowledgements

The current study was conducted within the setting of the Collaborative Research Center 125: “Cognition Guided Surgery,” supported by the German Research Foundation (DFG). We thank Ms. Sarah Trent for proofreading of the manuscript.

Author contributions

BPM, FN, HGK, CNG, JN, H-PM: study conception and design, FN, TG, CMS, JN, NA, HGK, JK: acquisition of data, FN, JN, JK: statistical analysis, FN, BPM, H-PM, HGK, JN, JK, TG, CG: analysis and interpretation of data, FN, HGK, JN, CG: drafting of manuscripta, and BPM, H-PM, CNG, TG, CMS: critical revision.

Compliance with ethical standards

Disclosure

Felix Nickel reports receiving travel support for conference participation as well as equipment provided for laparoscopic surgery courses by Karl Storz, Johnson & Johnson, and Covidien/Medtronic. Hannes G. Kenngott, Jochen Neuhaus, Nathanael Andrews, Carly Garrow, Johannes Kast, Christof M. Sommer, Tobias Gehrig, Carsten N Gutt, Hans-Peter Meinzer, and Beat Peter Müller-Stich have no conflict of interest or financial ties to disclose.

Ethical approval

The study protocol was approved by the German Committee on Animal Care, Regierungspräsidium Karlsruhe, and the Ethics Committee at Heidelberg University Medical School, and written permission to conduct the experiments consistent with official guidelines was obtained for the research protocol (A-19/08). Appropriate care was administered to all the animals according to the National Research Council’s criteria for humane care, covered in the guide for the care and use of laboratory animals prepared by the National Institute of Health (NIH Publication 86–23, revised 1985). All animals were anesthetised during the entirety of the procedure. Once the procedures were complete, each animal was euthenized according to the official protocol with a lethal dose of potassium chloride (KCl) [10].

References

  1. 1.
    Perry KA, Enestvedt CK, Pham T, Welker M, Jobe BA, Hunter JG, Sheppard BC (2009) Comparison of laparoscopic inversion esophagectomy and open transhiatal esophagectomy for high-grade dysplasia and stage I esophageal adenocarcinoma. Arch Surg 144:679–684.  https://doi.org/10.1001/archsurg.2009.113 CrossRefPubMedGoogle Scholar
  2. 2.
    Verhage RJ, Hazebroek EJ, Boone J, Van Hillegersberg R (2009) Minimally invasive surgery compared to open procedures in esophagectomy for cancer: a systematic review of the literature. Minerva Chir 64:135–146PubMedGoogle Scholar
  3. 3.
    Bottger T, Terzic A, Muller M, Rodehorst A (2007) Minimally invasive transhiatal and transthoracic esophagectomy. Surg Endosc 21:1695–1700.  https://doi.org/10.1007/s00464-006-9178-4 CrossRefPubMedGoogle Scholar
  4. 4.
    Smithers BM (2010) Minimally invasive esophagectomy: an overview. Expert Rev Gastroenterol Hepatol 4:91–99.  https://doi.org/10.1586/egh.09.62 CrossRefPubMedGoogle Scholar
  5. 5.
    Nagpal K, Ahmed K, Vats A, Yakoub D, James D, Ashrafian H, Darzi A, Moorthy K, Athanasiou T (2010) Is minimally invasive surgery beneficial in the management of esophageal cancer? A meta-analysis. Surg Endosc.  https://doi.org/10.1007/s00464-009-0822-7 Google Scholar
  6. 6.
    Gutt CN, Bintintan VV, Koninger J, Muller-Stich BP, Reiter M, Buchler MW (2006) Robotic-assisted transhiatal esophagectomy. Langenbecks Arch Surg 391:428–434.  https://doi.org/10.1007/s00423-006-0055-3 CrossRefPubMedGoogle Scholar
  7. 7.
    Kenngott HG, Neuhaus J, Muller-Stich BP, Wolf I, Vetter M, Meinzer HP, Koninger J, Buchler MW, Gutt CN (2008) Development of a navigation system for minimally invasive esophagectomy. Surg Endosc 22:1858–1865.  https://doi.org/10.1007/s00464-007-9723-9 CrossRefPubMedGoogle Scholar
  8. 8.
    Zhang H, Banovac F, Lin R, Glossop N, Wood BJ, Lindisch D, Levy E, Cleary K (2006) Electromagnetic tracking for abdominal interventions in computer aided surgery. Comput Aided Surg 11:127–136.  https://doi.org/10.3109/10929080600751399 CrossRefPubMedCentralPubMedGoogle Scholar
  9. 9.
    Banovac F, Cheng P, Campos-Nanez E, Kallakury B, Popa T, Wilson E, Abeledo H, Cleary K (2010) Radiofrequency ablation of lung tumors in swine assisted by a navigation device with preprocedural volumetric planning. J Vasc Interv Radiol 21:122–129.  https://doi.org/10.1016/j.jvir.2009.09.012 CrossRefPubMedGoogle Scholar
  10. 10.
    Nickel F (2014) Accuracy assessment of a navigation system and analysis of soft tissue deformation in an experimental model for minimally invasive esophagectomy. Doctoral thesis, Heidelberg UniversityGoogle Scholar
  11. 11.
    Nickel F, Kenngott HG, Neuhaus J, Sommer CM, Gehrig T, Kolb A, Gondan M, Radeleff BA, Schaible A, Meinzer HP, Gutt CN, Muller-Stich BP (2013) Navigation system for minimally invasive esophagectomy: experimental study in a porcine model. Surg Endosc 27:3663–3670.  https://doi.org/10.1007/s00464-013-2941-4 CrossRefPubMedGoogle Scholar
  12. 12.
    Troidl H, Bäcker B, Langer B, Winkler-Wilfurth A (1993) Fehleranalyse — Evaluierung und Verhütung von Komplikationen; ihre juristische Implikation. In: Hartel W (eds) Wandel der Chirurgie in unserer Zeit. Langenbecks Archiv für Chirurgie (Gegründet 1860, Kongreßorgan der Deutschen Gesellschaft für Chirurgie), vol 1993. Springer, Berlin, Heidelberg.  https://doi.org/10.1007/978-3-642-78145-2_12
  13. 13.
    Boselova L, Meitner ER (1977) Comparative morphology of the esophagus in various vertebrates II. Mammals. Gegenbaurs Morphol Jahrb 123:311–326PubMedGoogle Scholar
  14. 14.
    Bower AL, Ponsky JL, Brody FJ (2001) Physiology of intra-abdominal and intrathoracic Nissen fundoplications in a porcine model. J Laparoendosc Adv Surg Tech A 11:5–8.  https://doi.org/10.1089/10926420150502869 CrossRefPubMedGoogle Scholar
  15. 15.
    Green EM, Forrest LJ, Adams WM (2003) A vacuum-formable mattress for veterinary radiotherapy positioning: comparison with conventional methods. Vet Radiol Ultrasound 44:476–479CrossRefPubMedGoogle Scholar
  16. 16.
    Mallmann C, Wolf KJ, Wacker FK, Meyer BC (2012) Assessment of patient movement in interventional procedures using electromagnetic detection: comparison between conventional fixation and vacuum mattress. Rofo 184:37–41.  https://doi.org/10.1055/s-0031-1281633 CrossRefPubMedGoogle Scholar
  17. 17.
    Wolf I, Vetter M, Wegner I, Bottger T, Nolden M, Schobinger M, Hastenteufel M, Kunert T, Meinzer HP (2005) The medical imaging interaction toolkit. Med Image Anal 9:594–604.  https://doi.org/10.1016/j.media.2005.04.005 CrossRefPubMedGoogle Scholar
  18. 18.
    Bitter I, Van Uitert R, Wolf I, Ibanez L, Kuhnigk JM (2007) Comparison of four freely available frameworks for image processing and visualization that use ITK. IEEE Trans Vis Comput Graph 13:483–493.  https://doi.org/10.1109/TVCG.2007.1001 CrossRefPubMedGoogle Scholar
  19. 19.
    Maleike D, Nolden M, Meinzer HP, Wolf I (2009) Interactive segmentation framework of the Medical Imaging Interaction Toolkit. Comput Methods Progr Biomed 96:72–83.  https://doi.org/10.1016/j.cmpb.2009.04.004 CrossRefGoogle Scholar
  20. 20.
    Seitel A, Yung K, Mersmann S, Kilgus T, Groch A, Dos Santos TR, Franz AM, Nolden M, Meinzer HP, Maier-Hein L (2011) MITK-ToF-range data within MITK. Int J Comput Assist Radiol Surg.  https://doi.org/10.1007/s11548-011-0617-x PubMedGoogle Scholar
  21. 21.
    Wang ZY (1991) The length of the esophagus measured by SND-1 esophagus detector. Report of 197 cases. Zhonghua Wai Ke Za Zhi 29:566, 590PubMedGoogle Scholar
  22. 22.
    Wei XH (1989) Measurement of the length of the adult esophagus using a fiberogastroscope: 104 cases. Zhonghua Wai Ke Za Zhi 27:407–408, 444–405PubMedGoogle Scholar
  23. 23.
    Li Q, Castell JA, Castell DO (1994) Manometric determination of esophageal length. Am J Gastroenterol 89:722–725PubMedGoogle Scholar
  24. 24.
    Zhao KL, Liao Z, Bucci MK, Komaki R, Cox JD, Yu ZH, Zhang L, Mohan R, Dong L (2007) Evaluation of respiratory-induced target motion for esophageal tumors at the gastroesophageal junction. Radiother Oncol 84:283–289.  https://doi.org/10.1016/j.radonc.2007.07.008 CrossRefPubMedGoogle Scholar
  25. 25.
    Maier-Hein L, Muller SA, Pianka F, Worz S, Muller-Stich BP, Seitel A, Rohr K, Meinzer HP, Schmied BM, Wolf I (2008) Respiratory motion compensation for CT-guided interventions in the liver. Comput Aided Surg 13:125–138.  https://doi.org/10.3109/10929080802091099 CrossRefPubMedGoogle Scholar
  26. 26.
    Banovac F, Tang J, Xu S, Lindisch D, Chung HY, Levy EB, Chang T, McCullough MF, Yaniv Z, Wood BJ, Cleary K (2005) Precision targeting of liver lesions using a novel electromagnetic navigation device in physiologic phantom and swine. Med Phys 32:2698–2705CrossRefPubMedGoogle Scholar
  27. 27.
    Clifford MA, Banovac F, Levy E, Cleary K (2002) Assessment of hepatic motion secondary to respiration for computer assisted interventions. Comput Aided Surg 7:291–299.  https://doi.org/10.1002/igs.10049 CrossRefPubMedGoogle Scholar
  28. 28.
    Levy EB, Tang J, Lindisch D, Glossop N, Banovac F, Cleary K (2007) Implementation of an electromagnetic tracking system for accurate intrahepatic puncture needle guidance: accuracy results in an in vitro model. Acad Radiol 14:344–354.  https://doi.org/10.1016/j.acra.2006.12.004 CrossRefPubMedGoogle Scholar
  29. 29.
    Yaniv Z, Cheng P, Wilson E, Popa T, Lindisch D, Campos-Nanez E, Abeledo H, Watson V, Cleary K, Banovac F (2010) Needle-based interventions with the image-guided surgery toolkit (IGSTK): from phantoms to clinical trials. IEEE Trans Biomed Eng 57:922–933.  https://doi.org/10.1109/tbme.2009.2035688 CrossRefPubMedGoogle Scholar
  30. 30.
    Koch N, Liu HH, Starkschall G, Jacobson M, Forster K, Liao Z, Komaki R, Stevens CW (2004) Evaluation of internal lung motion for respiratory-gated radiotherapy using MRI: part I–correlating internal lung motion with skin fiducial motion. Int J Radiat Oncol Biol Phys 60:1459–1472CrossRefPubMedGoogle Scholar
  31. 31.
    Sra J, Krum D, Malloy A, Bhatia A, Cooley R, Blanck Z, Dhala A, Anderson AJ, Akhtar M (2006) Posterior left atrial-esophageal relationship throughout the cardiac cycle. J Interv Card Electrophysiol 16:73–80CrossRefPubMedGoogle Scholar
  32. 32.
    Plathow C, Zimmermann H, Fink C, Umathum R, Schobinger M, Huber P, Zuna I, Debus J, Schlegel W, Meinzer HP, Semmler W, Kauczor HU, Bock M (2005) Influence of different breathing maneuvers on internal and external organ motion: use of fiducial markers in dynamic MRI. Int J Radiat Oncol Biol Phys 62:238–245CrossRefPubMedGoogle Scholar
  33. 33.
    Birkfellner W, Watzinger F, Wanschitz F, Ewers R, Bergmann H (1998) Calibration of tracking systems in a surgical environment. IEEE Trans Med Imaging 17:737–742CrossRefPubMedGoogle Scholar
  34. 34.
    Muench RK, Blattmann H, Kaser-Hotz B, Bley CR, Seiler PG, Sumova A, Verwey J (2004) Combining magnetic and optical tracking for computer aided therapy. Z Med Phys 14:189–194CrossRefPubMedGoogle Scholar
  35. 35.
    Bintintan V, Gutt CN, Mehrabi A, Yazdi SF, Kashfi A, Funariu G, Ciuce C (2009) Gas-chamber mediastinoscopy for dissection of the upper esophagus. Chirurgia (Bucur) 104:67–72Google Scholar
  36. 36.
    Bintintan VV, Mehrabi A, Fonouni H, Esmaeilzadeh M, Muller-Stich BP, Funariu G, Ciuce C, Gutt CN (2009) Feasibility of a high intrathoracic esophagogastric anastomosis without thoracic access after laparoscopic-assisted transhiatal esophagectomy: a pilot experimental study. Surg Innov 16:228–236.  https://doi.org/10.1177/1553350609345852 CrossRefPubMedGoogle Scholar
  37. 37.
    Bintintan VV, Mehrabi A, Fonouni H, Golriz M, Koninger J, Kashfi A, Funariu G, Buechler MW, Ciuce C, Gutt CN (2009) Evaluation of the combined laparoscopic and mediastinoscopic esophagectomy technique. Chirurgia (Bucur) 104:187–194Google Scholar

Copyright information

© Springer Science+Business Media, LLC, part of Springer Nature 2018

Authors and Affiliations

  • Felix Nickel
    • 1
  • Hannes G. Kenngott
    • 1
  • Jochen Neuhaus
    • 2
  • Nathanael Andrews
    • 1
  • Carly Garrow
    • 1
  • Johannes Kast
    • 2
  • Christof M. Sommer
    • 3
  • Tobias Gehrig
    • 1
  • Carsten N. Gutt
    • 4
  • Hans-Peter Meinzer
    • 2
  • Beat P. Müller-Stich
    • 1
  1. 1.Department of General, Visceral and Transplantation SurgeryUniversity of HeidelbergHeidelbergGermany
  2. 2.Division of Medical and Biological InformaticsGerman Cancer Research CenterHeidelbergGermany
  3. 3.Department of Diagnostic and Interventional RadiologyUniversity of HeidelbergHeidelbergGermany
  4. 4.Department of SurgeryMemmingen HospitalMemmingenGermany

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