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Ultrastructural anomalies in the fetal small intestine indicate that fetal swallowing is important for normal development: an experimental study

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Summary

Fetal swallowing is established early in development and if fetal ingestion is prevented, the gastrointestinal (GI) tract fails to grow normally. In this article we describe the ultrastructural features of GI tissues developing in the absence of swallowing, in the fetal sheep. We have noted a number of defects in enterocyte morphology. These include abnormal or absence of microvilli, inappropriate cell extrusion, glycogen accumulation and altered lysosomal morphology. Many of these changes resemble those seen in malnourished infants. It is possible that fetal ingestion provides a significant source of nutrients, ensuring adequate GI tract growth in utero, in addition to specific growth factors which may be present in ingested fluid.

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References

  • Avila CG, Harding R (1991) The development of the gastrointestinal system in fetal sheep in the absence of ingestion. J Pediatr Gastroenterol Nutr 12:96–104

    Google Scholar 

  • Brunser O, Castillo C, Araya M (1976) Fine structure of the small intestinal mucosa in infantile marasmic malnutrition. Gastroenterology 70:495–507

    Google Scholar 

  • Calvert R (1981) Effect of amniotic fluid and fetal bovine serum on the morphogenesis of mouse duodenal villi in organ culture. Experientia 37:417–418

    Google Scholar 

  • Calvert R, Lehoux J-G, Arsenault P, Menard D (1983) Extracts of rat amniotic fluid contain a potent inducer of intestinal crypt formation. Anat Rec 205:27–37

    Google Scholar 

  • Campos JVM, Neto UF, Patricio FRS, Wehba J, Carvalho AA, Shiner M (1979) Jejunal mucosa in marasmic children. Clinical, pathological, and fine structural evaluation of the effect of protein-energy malnutrition and environmental contamination. Am J Clin Nutr 32:1575–1591

    Google Scholar 

  • Dunger A, Lucke S, Reiher H, Hahn HJ (1990) Human amniotic fluid stimulates DNA synthesis of rat pancreatic islets. Acta Histochem (Jena) 34:297–302

    Google Scholar 

  • Gitlin D, Kumate J, Morales C, Noriega L, Arvelo N (1972) The turnover of amniotic fluid protein in the human conceptus. Am J Obstet Gynecol 113:632–645

    Google Scholar 

  • Gonnella PA, Siminoski K, Murphy RA, Neutra M (1987) Transepithelial transport of epidermal growth factor by absorptive cells of suckling rat ileum. J Clin Invest 80:22–32

    Google Scholar 

  • Gonnella P, Harmatz P, Walker WA (1989) Prolactin is transported across the epithelium of the jejunum and ileum of the suckling rat. J Cell Physiol 140:138–149

    Google Scholar 

  • Harding R, Booking AD, Sigger JN, Wickham PJD (1984) Composition and volume of fluid swallowed by fetal sheep. Q J Exp Physiol 69:487–495

    Google Scholar 

  • Herbst JJ (1981) Development of sucking and swallowing. In: Lebenthal E (ed) Textbook of gastroenterology and nutrition in infancy. Raven Press, New York, p 102

    Google Scholar 

  • Jacobs DG, Wesson DE, Mago-Cao H, Muraji T, Konuma K, Mancer K, Kent G, Heim T (1989) Effect of esophageal ligation on the growth of fetal rabbits. J Pediatr Gastroenterol Nutr 8:245–251

    Google Scholar 

  • Krishnamurti CR, Schaefer AL, Kitts DD (1987) Amino acid and protein metabolism in the fetus. In: Nathanliesz PW (ed) Animal models in fetal medicine (VI). Perinatalogy Press, Ithaca, p 210

    Google Scholar 

  • Morikawa Y, Shimonaka H, Okada T (1988) Evidence for stimulative effect of amniotic fluid on the development of colonic goblet cells in fetal rats. Jpn J Vet Sci 50:1109–1111

    Google Scholar 

  • Mulvihill SJ, Stone MN, Debas HT, Fonkalsrud EW (1985) The role of amniotic fluid in fetal nutrition. J Pediatr Surg 20:668–672

    Google Scholar 

  • Mulvihill SJ, Stone MD, Fonkalsrud EW, Debas HT (1986) Trophic effect of amniotic fluid on fetal gastrointestinal development. J Surg Res 40:291–296

    Google Scholar 

  • Mulvihill SJ, Hallden G, Debas HT (1989) Trophic effect of amniotic fluid on cultured fetal gastric mucosal cells. J Surg Res 46:327–329

    Google Scholar 

  • Owens JA, Owens PC, Robinson JS (1989) Experimental fetal growth retardation: metabolic aspects: In: Lebenthal E (ed) Research in fetal physiology, vol VIII. Advances in fetal physiology. Perinatology Press, Ithaca, pp 263–286

    Google Scholar 

  • Pierro A, Cozzi F, Colarossi G, Irving IM, Peirce AM, Lister J (1987) Does fetal gut obstruction cause hydramnios and growth retardation? J Pediatr Surg 22:454–457

    Google Scholar 

  • Schindler AE (1982) Hormones in amniotic fluid. Monogr Endocrinol 21:1–158

    Google Scholar 

  • Shiner M, Nichols VN, Barrish JP, Nichols BL (1990) Pathogenesis of small-intestinal mucosal lesions in chronic diarrhea of infancy. II. An electron microscopic study. J Pediatr Gastroenterol Nutr 11:464–480

    Google Scholar 

  • Siminoski K, Gonnella P, Bernanke P, Owen L, Neutra M (1986) Uptake and transepithelial transport of nerve growth factor in suckling rat ileum. J Cell Biol 103:1979–1990

    Google Scholar 

  • Spencer GS, Hill DJ, Garssen GJ, MacDonald AA, Colenbrander B (1983) Somatomedin activity and growth hormone levels in body fluids of the fetal pig: effect of chronic hyperinsulinaemia. J Endocrinol 96:107–114

    Google Scholar 

  • Stahlman MT, Orth DN, Gray ME (1989) Immunocytochemical localization of epidermal growth factors in the developing human respiratory system and in acute and chronic lung disease in the neonate. Lab Invest 60:539–547

    Google Scholar 

  • Trahair JF, Robinson PM (1986) Development of the ovine small intestine. Anat Rec 214:294–303

    Google Scholar 

  • Trahair JF, Avila CG, Robinson PM (1985) Growth of the fetal sheep small intestine. Growth 50:201–216

    Google Scholar 

  • Trahair JF, Harding R, Bocking AD, Silver M, Robinson PM (1986a) The role of ingestion in the development of the small intestine in fetal sheep. Q J Exp Physiol 71:99–104

    Google Scholar 

  • Trahair JF, Perry RA, Silver M, Robinson PM (1986b) The migration of enterocytes in the developing small intestine of the sheep. Biol Neonate 50:214–220

    Google Scholar 

  • Trahair JF, Perry RA, Silver M, Robinson PM (1987a) Studies on the maturation of the small intestine of the fetal sheep. I. The effects of bilateral adrenalectomy. Q J Exp Physiol 72:61–69

    Google Scholar 

  • Trahair JF, Perry RA, Silver M, Robinson PM (1987b) Studies on the maturation of the small intestine of the fetal sheep. II. The effects of exogenous cortisol. Q J Exp Physiol 72:71–79

    Google Scholar 

  • Weaver LT, Gonnella PA, Isreal EJ, Walker WA (1990) Uptake and transport of epidermal growth factor by the small intestinal epithelium of the fetal rat. Gastroenterology 98:828–837

    Google Scholar 

  • Wesson DE, Muraji T, Kent G, Filler RM, Almachi T (1984) The effect of intrauterine esophageal ligation on growth of fetal rabbits. J Pediatr Surg 19:398–399

    Google Scholar 

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Trahair, J.F., Harding, R. Ultrastructural anomalies in the fetal small intestine indicate that fetal swallowing is important for normal development: an experimental study. Vichows Archiv A Pathol Anat 420, 305–312 (1992). https://doi.org/10.1007/BF01600209

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  • DOI: https://doi.org/10.1007/BF01600209

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