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      The growth pattern of the human intestine and its mesentery

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          Abstract

          Background

          It remains unclear to what extent midgut rotation determines human intestinal topography and pathology. We reinvestigated the midgut during its looping and herniation phases of development, using novel 3D visualization techniques.

          Results

          We distinguished 3 generations of midgut loops. The topography of primary and secondary loops was constant, but that of tertiary loops not. The orientation of the primary loop changed from sagittal to transverse due to the descent of ventral structures in a body with a still helical body axis. The 1 st secondary loop (duodenum, proximal jejunum) developed intraabdominally towards a left-sided position. The 2 nd secondary loop (distal jejunum) assumed a left-sided position inside the hernia before returning, while the 3 rd and 4 th secondary loops retained near-midline positions. Intestinal return into the abdomen resembled a backward sliding movement. Only after return, the 4 th secondary loop (distal ileum, cecum) rapidly “slid” into the right lower abdomen. The seemingly random position of the tertiary small-intestinal loops may have a biomechanical origin.

          Conclusions

          The interpretation of “intestinal rotation” as a mechanistic rather than a descriptive concept underlies much of the confusion accompanying the physiological herniation. We argue, instead, that the concept of “en-bloc rotation” of the developing midgut is a fallacy of schematic drawings. Primary, secondary and tertiary loops arise in a hierarchical fashion. The predictable position and growth of secondary loops is pre-patterned and determines adult intestinal topography. We hypothesize based on published accounts that malrotations result from stunted development of secondary loops.

          Electronic supplementary material

          The online version of this article (doi:10.1186/s12861-015-0081-x) contains supplementary material, which is available to authorized users.

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          Most cited references52

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          On the growth and form of the gut.

          The developing vertebrate gut tube forms a reproducible looped pattern as it grows into the body cavity. Here we use developmental experiments to eliminate alternative models and show that gut looping morphogenesis is driven by the homogeneous and isotropic forces that arise from the relative growth between the gut tube and the anchoring dorsal mesenteric sheet, tissues that grow at different rates. A simple physical mimic, using a differentially strained composite of a pliable rubber tube and a soft latex sheet is consistent with this mechanism and produces similar patterns. We devise a mathematical theory and a computational model for the number, size and shape of intestinal loops based solely on the measurable geometry, elasticity and relative growth of the tissues. The predictions of our theory are quantitatively consistent with observations of intestinal loops at different stages of development in the chick embryo. Our model also accounts for the qualitative and quantitative variation in the distinct gut looping patterns seen in a variety of species including quail, finch and mouse, illuminating how the simple macroscopic mechanics of differential growth drives the morphology of the developing gut.
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            Intestinal malrotation: varied clinical presentation from infancy through adulthood.

            The purpose of this study was to determine the incidence and clinical presentation of intestinal malrotation from infancy through adulthood by examining the experience of a single institution caring for patients of all ages with this condition. We conducted a retrospective review on all patients diagnosed with intestinal malrotation at Massachusetts General Hospital between 1992 and 2009. Patient demographics, clinical history, diagnostic tests, operative procedures, and outcome variables were recorded. Patients were divided into 3 age groups: infants (<1 year), children (1-18 years), and adults (18 years). We identified 170 patients, of whom 31% were infants, 21% were children, and 48% were adults. Infants nearly always presented with emesis (93%), whereas adults most commonly presented with abdominal pain (87%), and less often with emesis (37%) or nausea (31%). The incidence of volvulus declined with age, from 37% to 22% to 12%, in each of the 3 age groups, respectively. Although infants were most often diagnosed within hours or days of symptom onset, 59% of children and 32% of adults experienced symptoms for years before diagnosis. Upper gastrointestinal series was the most common imaging study performed in infants and children, but was replaced by abdominal computed tomography in adults. All infants and children underwent a Ladd's procedure, compared with only 61% of adults. The majority of patients experienced resolution of symptoms after operative intervention, although this decreased slightly with age. Intestinal malrotation can occur in patients of any age and, in contrast with traditional teaching, nearly half of these patients may present during adulthood. An increased awareness of this entity and an understanding of its varied presentation at different ages may reduce time to diagnosis and improve patient outcome. Copyright © 2011 Mosby, Inc. All rights reserved.
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              Congenital intestinal atresia; observations on its origin.

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                Author and article information

                Contributors
                Jelly.soffers@maastrichtuniversity.nl
                Jill.hikspoors@maastrichtuniversity.nl
                Hayelom.mekonen@maastrichtuniversity.nl
                Leo.koehler@maastrichtuniveristy.nl
                +31433881061 , WH.Lamers@maastrichtuniversity.nl
                Journal
                BMC Dev Biol
                BMC Dev. Biol
                BMC Developmental Biology
                BioMed Central (London )
                1471-213X
                22 August 2015
                22 August 2015
                2015
                : 15
                : 31
                Affiliations
                [ ]Department of Anatomy & Embryology, Maastricht University, P.O. Box 616, 6200 MD Maastricht, The Netherlands
                [ ]Tytgat Institute for Liver and Intestinal Research, Academic Medical Center, University of Amsterdam, Amsterdam, The Netherlands
                Article
                81
                10.1186/s12861-015-0081-x
                4546136
                26297675
                af3d76ca-5a93-4865-be93-1b265b963076
                © Soffers et al. 2015

                Open Access This article is distributed under the terms of the Creative Commons Attribution 4.0 International License ( http://creativecommons.org/licenses/by/4.0), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver ( http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated.

                History
                : 30 October 2014
                : 30 October 2014
                Categories
                Research Article
                Custom metadata
                © The Author(s) 2015

                Developmental biology
                Developmental biology

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