Limits...
The growth pattern of the human intestine and its mesentery.

Soffers JH, Hikspoors JP, Mekonen HK, Koehler SE, Lamers WH - BMC Dev. Biol. (2015)

Bottom Line: 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.

View Article: PubMed Central - PubMed

Affiliation: Department of Anatomy & Embryology, Maastricht University, P.O. Box 616, 6200 MD, Maastricht, The Netherlands. Jelly.soffers@maastrichtuniversity.nl.

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 1st secondary loop (duodenum, proximal jejunum) developed intraabdominally towards a left-sided position. The 2nd secondary loop (distal jejunum) assumed a left-sided position inside the hernia before returning, while the 3rd and 4th secondary loops retained near-midline positions. Intestinal return into the abdomen resembled a backward sliding movement. Only after return, the 4th 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.

Show MeSH

Related in: MedlinePlus

Tertiary loops arise from the 8th week onwards and exhibit variation in number and position. Panels a-d show caudal views of the progressive folding of the apex of the 2nd secondary loop (coded yellow) that results in tertiary loops. Panel a: CS20 (462); panel b: CS21 (4090); panel c: CS22 (H983); panel d: CS23 (s4141). The tip of the extending loops remains close to the mesenteric rod. Panels e-g show ventral views of three CS23 embryos of increasing size from left to right (s48, s4141, s9226). Note the variation in number and position of the tertiary loops and the fairly rapid movement of the 2nd secondary loop from right (e) to left (g). For color codes, see Figure Legends. The scale bars (units in μm) show the diameter of the intestines with their surrounding mesenchyme in that panel. An interactive 3D-PDF is available online (3D-PDF CS23)
© Copyright Policy - OpenAccess
Related In: Results  -  Collection

License 1 - License 2
getmorefigures.php?uid=PMC4546136&req=5

Fig6: Tertiary loops arise from the 8th week onwards and exhibit variation in number and position. Panels a-d show caudal views of the progressive folding of the apex of the 2nd secondary loop (coded yellow) that results in tertiary loops. Panel a: CS20 (462); panel b: CS21 (4090); panel c: CS22 (H983); panel d: CS23 (s4141). The tip of the extending loops remains close to the mesenteric rod. Panels e-g show ventral views of three CS23 embryos of increasing size from left to right (s48, s4141, s9226). Note the variation in number and position of the tertiary loops and the fairly rapid movement of the 2nd secondary loop from right (e) to left (g). For color codes, see Figure Legends. The scale bars (units in μm) show the diameter of the intestines with their surrounding mesenchyme in that panel. An interactive 3D-PDF is available online (3D-PDF CS23)

Mentions: The length of the small intestine increased ~6-fold during CS20-23 (Fig. 6) with all secondary loops lengthening evenly. In addition, the radial length of the mesenteric leaves of the secondary loops increased, so that each secondary loop now clearly had its own leaf (3D-PDF CS23; compare Fig. 5b,c). The 3rd and 4th loops remained separated by the central axis, formed by the mesenteric rod, right vitelline vein, SMA, and periductal mesenchyme. The mesenteric leaves associated with the secondary loops remained recognizable during subsequent development and, thus, formed landmarks for these loops. The continued longitudinal growth was further accompanied by the appearance of tertiary loops within the secondary loops (Fig. 6a-d). The tertiary loops differed from the secondary loops in that their deposition varied between different embryos of similar stage (Fig. 6e-g). Of note, tertiary loops only developed within secondary loops with a mesentery. Accordingly, the proximal (future duodenal) part of the 1st secondary loop (coded red) did not develop tertiary loops. Interestingly, the 2nd secondary loop (coded yellow) assumed a left-sided position inside the hernia during the formation of tertiary loops (Fig. 6e-g). Although this change in position is obviously important for its future position in the abdomen (see: “Resolution of the hernia”), we have not identified any external cause for it.Fig. 6


The growth pattern of the human intestine and its mesentery.

Soffers JH, Hikspoors JP, Mekonen HK, Koehler SE, Lamers WH - BMC Dev. Biol. (2015)

Tertiary loops arise from the 8th week onwards and exhibit variation in number and position. Panels a-d show caudal views of the progressive folding of the apex of the 2nd secondary loop (coded yellow) that results in tertiary loops. Panel a: CS20 (462); panel b: CS21 (4090); panel c: CS22 (H983); panel d: CS23 (s4141). The tip of the extending loops remains close to the mesenteric rod. Panels e-g show ventral views of three CS23 embryos of increasing size from left to right (s48, s4141, s9226). Note the variation in number and position of the tertiary loops and the fairly rapid movement of the 2nd secondary loop from right (e) to left (g). For color codes, see Figure Legends. The scale bars (units in μm) show the diameter of the intestines with their surrounding mesenchyme in that panel. An interactive 3D-PDF is available online (3D-PDF CS23)
© Copyright Policy - OpenAccess
Related In: Results  -  Collection

License 1 - License 2
Show All Figures
getmorefigures.php?uid=PMC4546136&req=5

Fig6: Tertiary loops arise from the 8th week onwards and exhibit variation in number and position. Panels a-d show caudal views of the progressive folding of the apex of the 2nd secondary loop (coded yellow) that results in tertiary loops. Panel a: CS20 (462); panel b: CS21 (4090); panel c: CS22 (H983); panel d: CS23 (s4141). The tip of the extending loops remains close to the mesenteric rod. Panels e-g show ventral views of three CS23 embryos of increasing size from left to right (s48, s4141, s9226). Note the variation in number and position of the tertiary loops and the fairly rapid movement of the 2nd secondary loop from right (e) to left (g). For color codes, see Figure Legends. The scale bars (units in μm) show the diameter of the intestines with their surrounding mesenchyme in that panel. An interactive 3D-PDF is available online (3D-PDF CS23)
Mentions: The length of the small intestine increased ~6-fold during CS20-23 (Fig. 6) with all secondary loops lengthening evenly. In addition, the radial length of the mesenteric leaves of the secondary loops increased, so that each secondary loop now clearly had its own leaf (3D-PDF CS23; compare Fig. 5b,c). The 3rd and 4th loops remained separated by the central axis, formed by the mesenteric rod, right vitelline vein, SMA, and periductal mesenchyme. The mesenteric leaves associated with the secondary loops remained recognizable during subsequent development and, thus, formed landmarks for these loops. The continued longitudinal growth was further accompanied by the appearance of tertiary loops within the secondary loops (Fig. 6a-d). The tertiary loops differed from the secondary loops in that their deposition varied between different embryos of similar stage (Fig. 6e-g). Of note, tertiary loops only developed within secondary loops with a mesentery. Accordingly, the proximal (future duodenal) part of the 1st secondary loop (coded red) did not develop tertiary loops. Interestingly, the 2nd secondary loop (coded yellow) assumed a left-sided position inside the hernia during the formation of tertiary loops (Fig. 6e-g). Although this change in position is obviously important for its future position in the abdomen (see: “Resolution of the hernia”), we have not identified any external cause for it.Fig. 6

Bottom Line: 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.

View Article: PubMed Central - PubMed

Affiliation: Department of Anatomy & Embryology, Maastricht University, P.O. Box 616, 6200 MD, Maastricht, The Netherlands. Jelly.soffers@maastrichtuniversity.nl.

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 1st secondary loop (duodenum, proximal jejunum) developed intraabdominally towards a left-sided position. The 2nd secondary loop (distal jejunum) assumed a left-sided position inside the hernia before returning, while the 3rd and 4th secondary loops retained near-midline positions. Intestinal return into the abdomen resembled a backward sliding movement. Only after return, the 4th 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.

Show MeSH
Related in: MedlinePlus