Mesenteric neovascularization with distraction-induced intestinal growth: enterogenesis - Pediatric Surgery International

Background

Distraction-induced enterogenesis, whereby the intestine lengthens with application of linear forces, is an emerging area which may provide a unique treatment for short bowel syndrome. With an increase in overall tissue mass, there is an increase in oxygen and nutrient demand. We hypothesized that a neovascularization within the mesentery is necessary to support the growing small bowel.

Methods

A curvilinear hydraulic device was used to induce growth within the small bowel of Yorkshire pigs, and the intestine was harvested after 14 days. High-resolution gross pictures were recorded of the mesentery at implantation and at harvest, and CT imaging of the bowel and mesentery was performed at harvest after dye injection.

Results

After 2 weeks of distraction, an average of 72.5 % (8.7 cm) bowel lengthening was achieved. Gross images of the mesentery between major vessels showed a blossoming of the microvasculature and this was confirmed by CT imaging with 3D reconstruction. Mesenteric sample taken from the distracted segment had a fourfold increase in the volume of microvasculature versus controls.

Conclusion

Enterogenesis results not only in increased bowel length, but also significant increase in the mesenteric microvascularity. Presumably, this sustains the lengthened segment after application of longitudinal forces.

1. Cole CR et al (2008) Very low birth weight preterm infants with surgical short bowel syndrome: incidence, morbidity and mortality, and growth outcomes at 18 to 22 months. Pediatrics 122(3):e573–e582

   Article  PubMed  Google Scholar 

2. Sigalet DL (2001) Short bowel syndrome in infants and children: an overview. Semin Pediatr Surg 10(2):49–55

   Article  PubMed  CAS  Google Scholar 

3. Hess RA et al (2011) Survival outcomes of pediatric intestinal failure patients: analysis of factors contributing to improved survival over the past two decades. J Surg Res 170(1):27–31

   Article  PubMed  Google Scholar 

4. Torres C et al (2007) Role of an intestinal rehabilitation program in the treatment of advanced intestinal failure. J Pediatr Gastroenterol Nutr 45(2):204–212

   Article  PubMed  Google Scholar 

5. Struijs MC et al (2009) Establishing norms for intestinal length in children. J Pediatr Surg 44(5):933–938

   Article  PubMed  Google Scholar 

6. Messing B et al (1999) Long-term survival and parenteral nutrition dependence in adult patients with the short bowel syndrome. Gastroenterology 117(5):1043–1050

   Article  PubMed  CAS  Google Scholar 

7. Turner JM et al (2011) Novel neonatal piglet models of surgical short bowel syndrome with intestinal failure. J Pediatr Gastroenterol Nutr 52(1):9–16

   Article  PubMed  Google Scholar 

8. Spencer AU et al (2005) Pediatric short bowel syndrome: redefining predictors of success. Ann Surg 242(3):403–409 (discussion 409–412)

   PubMed  Google Scholar 

9. Peretti N et al (2011) Growth hormone to improve short bowel syndrome intestinal autonomy: a pediatric randomized open-label clinical trial. J Parenter Enteral Nutr 35(6):723–731

   Article  CAS  Google Scholar 

10. Kim HB et al (2003) Serial transverse enteroplasty (STEP): a novel bowel lengthening procedure. J Pediatr Surg 38(3):425–429

    Article  PubMed  Google Scholar 

11. Bianchi A (1997) Longitudinal intestinal lengthening and tailoring: results in 20 children. J R Soc Med 90(8):429–432

    PubMed  CAS  Google Scholar 

12. O’Keefe SJ et al (2006) Short bowel syndrome and intestinal failure: consensus definitions and overview. Clin Gastroenterol Hepatol 4(1):6–10

    Article  PubMed  Google Scholar 

13. Hoffman BD, Grashoff C, Schwartz MA (2011) Dynamic molecular processes mediate cellular mechanotransduction. Nature 475(7356):316–323

    Article  PubMed  CAS  Google Scholar 

14. Codivilla A (1904) On the means of lengthening, in the lower limbs, the muscles and tissues which are shortened through deformity. Clin Orthop Relat Res 1994(301):4–9

    Google Scholar 

15. Nishisho T, Yukata K, Matsui Y, Matsuura T, Higashino K, Suganuma K, Nikawa T, Yasui N (2012) Angiogenesis and myogenesis in mouse tibialis anterior muscles during distraction osteogenesis: VEGF, its receptors, and myogenin genes expression. J Orthop Res 30(11):1767–1773. doi:10.1002/jor.22136

    Google Scholar 

16. Park J et al (2004) Enterogenesis by mechanical lengthening: morphology and function of the lengthened small intestine. J Pediatr Surg 39(12):1823–1827

    Article  PubMed  Google Scholar 

17. Koga H et al (2012) Distraction-induced intestinal enterogenesis: preservation of intestinal function and lengthening after reimplantation into normal jejunum. Ann Surg 255(2):302–310

    Article  PubMed  Google Scholar 

18. Okawada M, Maria HM, Teitelbaum DH (2011) Distraction induced enterogenesis: a unique mouse model using polyethylene glycol. J Surg Res 170(1):41–47

    Article  PubMed  Google Scholar 

19. Stark R et al (2011) Restoration of mechanically lengthened jejunum into intestinal continuity in rats. J Pediatr Surg 46(12):2321–2326

    Article  PubMed  Google Scholar 

20. Feng Y, McDunn JE, Teitelbaum DH (2010) Decreased phospho-Akt signaling in a mouse model of total parenteral nutrition: a potential mechanism for the development of intestinal mucosal atrophy. Am J Physiol Gastrointest Liver Physiol 298(6):G833–G841

    Article  PubMed  CAS  Google Scholar 

21. Johnston M et al (2005) Subarachnoid injection of Microfil reveals connections between cerebrospinal fluid and nasal lymphatics in the non-human primate. Neuropathol Appl Neurobiol 31(6):632–640

    Article  PubMed  CAS  Google Scholar 

22. Lin G et al (1984) Microvasculature architecture of small liver metastases in man. A correlation between microfil vascular preparations and histologic sections. Invest Radiol 19(4):296–302

    Article  PubMed  CAS  Google Scholar 

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Authors and Affiliations

1. Section of Pediatric Surgery, Department of Surgery, C.S. Mott Children’s Hospital F3970, University of Michigan, Ann Arbor, MI, 48109-0245, USA

   Matthew W. Ralls, Ryo Sueyoshi, Richard S. Herman, Nancy Si & Daniel H. Teitelbaum

2. Department of Mechanical Engineering, University of Michigan, Ann Arbor, MI, USA

   Brent Utter, Isabel Czarnocki, Jonathan Luntz & Diann Brei

Corresponding author

Correspondence to Daniel H. Teitelbaum.

Cite this article

Ralls, M.W., Sueyoshi, R., Herman, R.S. et al. Mesenteric neovascularization with distraction-induced intestinal growth: enterogenesis. Pediatr Surg Int 29, 33–39 (2013). https://doi.org/10.1007/s00383-012-3204-5

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• Published: 16 November 2012

• Issue Date: January 2013

• DOI: https://doi.org/10.1007/s00383-012-3204-5

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