Advertisement

Annals of Biomedical Engineering

, Volume 46, Issue 5, pp 705–716 | Cite as

The Turning Point for Morphomechanical Remodeling During Complete Intestinal Obstruction in Rats Occurs After 12–24 h

  • Daming Sun
  • Jingbo Zhao
  • Donghua Liao
  • Zhiyong Huang
  • Hans Gregersen
Article

Abstract

Intestinal obstruction prompts luminal dilation and wall remodeling proximal to the site of obstruction. Studies on temporal and spatial morphomechanical remodeling are needed for comprehending the pathophysiology of acute intestinal obstruction. The aim was to estimate the no-load and zero-stress morphomechanical properties in circumferential and longitudinal direction at 0, 6, 12, 24, 36, and 48 h after complete intestinal obstruction. Obstruction of the distal ileum was created surgically by placement of a polyethylene ring for up to 48 h in 30 rats. Sham and normal groups were also studied (n = 12). Five 6 cm-long intestinal segments proximal to the obstruction site were used for histological, morphometric and mechanical analysis at the designated times. Morphomechanical changes were huge but only subtle changes were observed between the 5 segments during the obstruction period. Due to dilation, the serosal length and mucosal length increased continuously from 6 to 48 h (p < 0.001). The wall area increased at 24 h and beyond (p < 0.001), demonstrating tissue growth. The opening and bending angle decreased to minimum values at 24 h where after the opening angle increased and the bending angle returned to pre-obstruction levels. For the residual stretch ratios and the position of the neutral axis the turning point was found after 24 h. Histologically, the thickness and area of most wall layers were quite stable for the first 12 h but with an increase at the 24 h time point that continued to the 48 h time point. The most pronounced change was found for the circumferential muscle layer (p < 0.05). Analysis of picrosirius red stained slides showed that submucosal type 3 collagen fraction increased significantly (p < 0.001), whereas the fraction of type 1 collagen decreased (p < 0.001). In conclusion, pronounced time-dependent morphomechanical remodeling was found. The obstructed intestine went from dilation remodeling to growth remodeling during the interval 12–24 h after creating the obstruction.

Keywords

Complete obstruction Histomorphometry Morphomechanical Rat intestine Residual stretch 

Notes

Acknowledgments

This study was partially supported by a grant from Chongqing Science and Technology Commission (cstc2013kjrc-ljrccj10003) and National “111 Plan” Base (B06023) and Karen Elise Jensen foundation. These contributions did not constitute any conflict of interest.

References

  1. 1.
    Bertoni, S., and G. Gabella. Hypertrophy of mucosa and serosa in the obstructed intestine of rats. J. Anat. 199:725–734, 2001.CrossRefPubMedPubMedCentralGoogle Scholar
  2. 2.
    Bertoni, S., G. Gabella, P. Ghizzardi, V. Ballabeni, M. Impicciatore, C. Lagrasta, M. L. Arcari, and E. Barocelli. Motor responses of rat hypertrophic intestine following chronic obstruction. Neurogastr. Motil. 16:365–374, 2004.CrossRefGoogle Scholar
  3. 3.
    Chang, I. Y., N. J. Glasgow, I. Takayama, K. Horiguchi, K. M. Sanders, and S. M. Ward. Loss of interstitial cells of Cajal and development of electrical dysfunction in murine small bowel obstruction. J. Physiol. 536:555–568, 2001.CrossRefPubMedPubMedCentralGoogle Scholar
  4. 4.
    De Giorgio, R., R. F. Cogliandro, G. Barbara, R. Corinaldesi, and V. Stanghellini. Chronic intestinal pseudo-obstruction: clinical features, diagnosis, and therapy. Gastroenterol. Clin. N. Am. 40:787–807, 2011.CrossRefGoogle Scholar
  5. 5.
    DiBaise, J. K., and E. M. Quigley. Tumor-related dysmotility: gastrointestinal dysmotility syndromes associated with tumors. Dig. Dis. Sci. 43:1369–1401, 1998.CrossRefPubMedGoogle Scholar
  6. 6.
    Díte, P., J. Lata, and I. Novotný. Intestinal obstruction and perforation—the role of the gastroenterologist. Dig. Dis. 21:63–67, 2003.CrossRefPubMedGoogle Scholar
  7. 7.
    Ekblad, E., R. Sjuve, A. Arner, and F. Sundler. Enteric neuronal plasticity and a reduced number of interstitial cells of Cajal in hypertrophic rat ileum. Gut 42:836–844, 1998.CrossRefPubMedPubMedCentralGoogle Scholar
  8. 8.
    Fung, Y. C. Biomechaincs. Properties of Living Tissues. Berlin: Springer, 1993.CrossRefGoogle Scholar
  9. 9.
    Gabella, G. Development and ageing of intestinal musculature and nerves: the guinea-pig taenia coli. J. Neurocytol. 30:733–766, 2001.CrossRefPubMedGoogle Scholar
  10. 10.
    Geuna, S., S. Cardillo, and M. G. Giacobini-Robecchi. Smooth muscle cell hypertrophy and hyperplasia in the partially obstructed gut of the rat: a quantitative evaluation. Cells Tissues Organs 163:69–74, 1998.CrossRefGoogle Scholar
  11. 11.
    Gregersen, H. Biomechanics of the Gastrointestinal Tract. London: Springer, 2002.Google Scholar
  12. 12.
    Gregersen, H., J. L. Emery, and A. D. McCulloch. History-dependent mechanical behavior of guinea-pig small intestine. Ann. Biomed. Eng. 26:850–858, 1998.CrossRefPubMedGoogle Scholar
  13. 13.
    Holzapfel, G. A., T. C. Gasser, and R. W. Ogden. A new constitutive framework for arterial wall mechanics and a comparative study of material models. J. Elast. 61:1–48, 2000.CrossRefGoogle Scholar
  14. 14.
    Katis, P. G., and S. M. Dias. Volvulus: a rare twist on small-bowel obstruction. Can. Med. Assoc. J. 171:728, 2004.CrossRefGoogle Scholar
  15. 15.
    Lattouf, R., R. Younes, D. Lutomski, N. Naaman, G. Godeau, K. Senni, and S. Changotade. Picrosirius red staining: a useful tool to appraise collagen networks in normal and pathological tissues. J. Histochem. Cytochem. 62:751–758, 2014.CrossRefPubMedGoogle Scholar
  16. 16.
    Lawrance, I. C., G. Rogler, G. Bamias, C. Breynaert, J. Florholmen, G. Pellino, S. Reif, S. Speca, and G. Latella. Cellular and molecular mediators of intestinal fibrosis. J. Crohns Colitis 11(12):1491–1503, 2015.PubMedCentralGoogle Scholar
  17. 17.
    Liao, D., J. Zhao, and H. Gregersen. 3d Mechanical properties of the partially obstructed guinea pig small intestine. J. Biomech. 43:2079–2086, 2010.CrossRefPubMedGoogle Scholar
  18. 18.
    Liu, D. H., X. Huang, X. Guo, X. M. Meng, Y. S. Wu, H. L. Lu, C. M. Zhang, Y. C. Kim, and W. X. Xu. Voltage dependent potassium channel remodeling in murine intestinal smooth muscle hypertrophy induced by partial obstruction. PLoS ONE 9:e86109, 2014.CrossRefPubMedPubMedCentralGoogle Scholar
  19. 19.
    Markogiannakis, H., E. Messaris, D. Dardamanis, N. Pararas, D. Tzertzemelis, P. Giannopoulos, A. Larentzakis, E. Lagoudianakis, A. Manouras, and I. Bramis. Acute mechanical bowel obstruction: clinical presentation, etiology, management and outcome. World J. Gastroenterol. 13:432–437, 2007.CrossRefPubMedPubMedCentralGoogle Scholar
  20. 20.
    Miyamoto, M., K. Egami, S. Maeda, K. Ohkawa, N. Tanaka, E. Uchida, and T. Tajiri. Hirschsprung’s disease in adults: report of a case and review of the literature. J. Nippon Med. Sch. 72:113–120, 2005.CrossRefPubMedGoogle Scholar
  21. 21.
    Nguyen, V. H. Intestinal obstruction due to tuberculosis. Asian J. Surg. 25:145–148, 2002.CrossRefPubMedGoogle Scholar
  22. 22.
    Prihoda, M., A. Flatt, and R. W. Summers. Mechanisms of motility changes during acute intestinal obstruction in the dog. Am. J. Physiol. 247:G37–G42, 1984.PubMedGoogle Scholar
  23. 23.
    Silva, A. C., M. Pimenta, and L. S. Guimaraes. Small bowel obstruction: what to look for. Radiographics 29:423–439, 2009.CrossRefPubMedGoogle Scholar
  24. 24.
    Storkholm, J. H., J. Zhao, G. E. Villadsen, and H. Gregersen. Spontaneous and bolus-induced motility in the chronically obstructed guinea-pig small intestine in vitro. Dig. Dis. Sci. 53:413–420, 2008.CrossRefPubMedGoogle Scholar
  25. 25.
    Storkholm, J. H., J. Zhao, G. E. Villadsen, H. Hager, S. L. Jensen, and H. Gregersen. Biomechanical remodeling of the chronically obstructed Guinea pig small intestine. Dig. Dis. Sci. 52:336–346, 2007.CrossRefPubMedGoogle Scholar
  26. 26.
    Sun, D., J. Zhao, D. Liao, P. Chen, and H. Gregersen. Shear modulus of the partially obstructed rat small intestine. Ann. Biomed. Eng. 45:1069–1082, 2017.CrossRefPubMedGoogle Scholar
  27. 27.
    Tuca, A., E. Guell, E. Martinez-Losada, and N. Codorniu. Malignant bowel obstruction in advanced cancer patients: epidemiology, management, and factors influencing spontaneous resolution. Cancer Manag. Res. 4:159–169, 2012.CrossRefPubMedPubMedCentralGoogle Scholar
  28. 28.
    Vilz, T. O., B. Stoffels, C. Strassburg, H. H. Schild, and J. C. Kalff. Ileus in Adults. Dtsch. Arztebl. Int. 114:508–518, 2017.PubMedGoogle Scholar
  29. 29.
    Wilkins, B. M., and L. Spitz. Incidence of postoperative adhesion obstruction following neonatal laparotomy. Br. J. Surg. 73:762–764, 1986.CrossRefPubMedGoogle Scholar
  30. 30.
    Wu, C. C., Y. M. Lin, J. Gao, J. H. Winston, L. K. Cheng, and X. Z. Shi. Are interstitial cells of Cajal involved in mechanical stress-induced gene expression and impairment of smooth muscle contractility in bowel obstruction? PLoS ONE 8:e76222, 2013.CrossRefPubMedPubMedCentralGoogle Scholar
  31. 31.
    Yamada, H., and F. G. Evans. Strength of Biological Materials. Baltimore: Williams & Wilkins, 1970.Google Scholar
  32. 32.
    Yang, J., J. Zhao, P. Chen, T. Nakaguchi, D. Grundy, and H. Gregersen. Interdependency between mechanical parameters and afferent nerve discharge in hypertrophic intestine of rats. Am. J. Physiol-Gastr. Liver Physiol. 310:G376–G386, 2016.Google Scholar
  33. 33.
    Zhao, J., D. Liao, J. Yang, and H. Gregersen. Biomechanical remodelling of obstructed guinea pig jejunum. J. Biomech. 43:1322–1329, 2010.CrossRefPubMedPubMedCentralGoogle Scholar
  34. 34.
    Zhao, J., D. Liao, J. Yang, and H. Gregersen. Phasic and tonic smooth muscle function of the partially obstructed guinea pig intestine. J. Biomed. Biotechnol. 2011:489720, 2011.PubMedPubMedCentralGoogle Scholar
  35. 35.
    Zhao, J., D. Liao, J. Yang, and H. Gregersen. Stress and strain analysis of contractions during ramp distension in partially obstructed guinea pig jejunal segments. J. Biomech. 44:2077–2082, 2011.CrossRefPubMedPubMedCentralGoogle Scholar
  36. 36.
    Zissin, R., M. Hertz, H. Paran, J. Bernheim, M. Shapiro-Feinberg, and G. Gayer. Small bowel obstruction secondary to Crohn disease: CT findings. Abdom. Imaging 29:320–325, 2004.CrossRefPubMedGoogle Scholar

Copyright information

© Biomedical Engineering Society 2018

Authors and Affiliations

  1. 1.GIOME and the Key Laboratory for Biorheological Science and Technology of Ministry of EducationBioengineering College of Chongqing UniversityChongqingChina
  2. 2.Department of Clinical MedicineAarhus UniversityAarhusDenmark
  3. 3.Communication EngineeringCollege of Chongqing UniversityChongqingChina
  4. 4.GIOME Center, College of BioengineeringChongqingChina

Personalised recommendations