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

“Rotation” of the midgut relative to the superior mesenteric artery. The diagram shows the changes in position (“rotation”) of the indicated intestinal structures relative to the SMA as seen from ventral. Cranial relative to the SMA represents 0° and the gut “rotates” counterclockwise. The squares represent rotation associated with the primary loop. The diamonds show the degree of rotation between 5.5 and 8.5 weeks, while the circles show the degree of rotation during and immediately after intestinal return (9th week). Only rotation and not distance to the SMA are shown, so that rotation during intestinal return appears extensive, whereas the change in position is only minor. We conclude that the intestines do not “rotate” but “slide” from the umbilical orifice to the lower-right abdominal cavity
© Copyright Policy - OpenAccess
Related In: Results  -  Collection

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

Fig12: “Rotation” of the midgut relative to the superior mesenteric artery. The diagram shows the changes in position (“rotation”) of the indicated intestinal structures relative to the SMA as seen from ventral. Cranial relative to the SMA represents 0° and the gut “rotates” counterclockwise. The squares represent rotation associated with the primary loop. The diamonds show the degree of rotation between 5.5 and 8.5 weeks, while the circles show the degree of rotation during and immediately after intestinal return (9th week). Only rotation and not distance to the SMA are shown, so that rotation during intestinal return appears extensive, whereas the change in position is only minor. We conclude that the intestines do not “rotate” but “slide” from the umbilical orifice to the lower-right abdominal cavity

Mentions: We have, of course, asked ourselves the question whether the change in position of the duodenojejunal junction and the cecum relative to the axis of the SMA represented a 270° rotation. Rotation is usually described to occur in 2 phases, that is, during formation of the primary loop and upon intestinal return into the abdominal cavity [6, 16], but sometimes an intermediate stage that represents the growth of the secondary loops is included [8]. We also mapped the positions of the 4 secondary loops relative to the SMA as degrees of rotation when they first develop (5.5 weeks), during intrahernial growth (between 5.5 and 8 weeks), and after return (>9.0 weeks). Figure 12 shows that the rotation of the primary loop is experienced by all parts of the midgut. Although the outcome of our model does not differ from the “en-bloc” rotation model in this phase of development, it proposes for the first time a potential mechanism for the initiation of asymmetric gut development, namely the descent of the distal foregut and its derivatives in embryos with a still helical body axis. The subsequent topographical changes of the intestine relative to the SMA during late herniation are most pronounced in the proximal duodeno-jejunal loop (orange) which extends caudal to the SMA in a leftward direction over a 3-week period, suggesting it represents a period of local growth. Thereafter, the position of this segment hardly changes in position. In contrast, the distal ileal loop (blue) hardly changes in position relative to the SMA during late herniation, but does so within a few days after return in the abdominal cavity. As Fig. 9 shows, this latter change in position is due to a movement of this part of the gut from midsagittal and ventral to right-lateral and more dorsal. Even though the rotational change of this part of the intestine after intestinal return appears extensive, the linear change in position is only minor. If one insists on using the term rotation for this movement, it would be largely around a craniocaudal axis (in the transverse plane) rather than a dorsoventral axis (frontal plane). In view of the brief time window and orientation of the apparent rotational axis, we conclude that the distal ileum and cecum “slide” rather than “rotate” as from the umbilical orifice to the lower-right abdominal cavity. “En-bloc rotation” is a conceptually simple and, therefore, attractive model of intestinal development, but the very different degrees, rates, and developmental timing of the apparent rotation of different parts of the midgut shows that this model cannot be upheld. Our present study shows that hierarchical looping is a viable new model to describe key morphogenetic events in intestinal development (for a comparison of both models, see Fig. 13).Fig. 12


The growth pattern of the human intestine and its mesentery.

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

“Rotation” of the midgut relative to the superior mesenteric artery. The diagram shows the changes in position (“rotation”) of the indicated intestinal structures relative to the SMA as seen from ventral. Cranial relative to the SMA represents 0° and the gut “rotates” counterclockwise. The squares represent rotation associated with the primary loop. The diamonds show the degree of rotation between 5.5 and 8.5 weeks, while the circles show the degree of rotation during and immediately after intestinal return (9th week). Only rotation and not distance to the SMA are shown, so that rotation during intestinal return appears extensive, whereas the change in position is only minor. We conclude that the intestines do not “rotate” but “slide” from the umbilical orifice to the lower-right abdominal cavity
© Copyright Policy - OpenAccess
Related In: Results  -  Collection

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

Fig12: “Rotation” of the midgut relative to the superior mesenteric artery. The diagram shows the changes in position (“rotation”) of the indicated intestinal structures relative to the SMA as seen from ventral. Cranial relative to the SMA represents 0° and the gut “rotates” counterclockwise. The squares represent rotation associated with the primary loop. The diamonds show the degree of rotation between 5.5 and 8.5 weeks, while the circles show the degree of rotation during and immediately after intestinal return (9th week). Only rotation and not distance to the SMA are shown, so that rotation during intestinal return appears extensive, whereas the change in position is only minor. We conclude that the intestines do not “rotate” but “slide” from the umbilical orifice to the lower-right abdominal cavity
Mentions: We have, of course, asked ourselves the question whether the change in position of the duodenojejunal junction and the cecum relative to the axis of the SMA represented a 270° rotation. Rotation is usually described to occur in 2 phases, that is, during formation of the primary loop and upon intestinal return into the abdominal cavity [6, 16], but sometimes an intermediate stage that represents the growth of the secondary loops is included [8]. We also mapped the positions of the 4 secondary loops relative to the SMA as degrees of rotation when they first develop (5.5 weeks), during intrahernial growth (between 5.5 and 8 weeks), and after return (>9.0 weeks). Figure 12 shows that the rotation of the primary loop is experienced by all parts of the midgut. Although the outcome of our model does not differ from the “en-bloc” rotation model in this phase of development, it proposes for the first time a potential mechanism for the initiation of asymmetric gut development, namely the descent of the distal foregut and its derivatives in embryos with a still helical body axis. The subsequent topographical changes of the intestine relative to the SMA during late herniation are most pronounced in the proximal duodeno-jejunal loop (orange) which extends caudal to the SMA in a leftward direction over a 3-week period, suggesting it represents a period of local growth. Thereafter, the position of this segment hardly changes in position. In contrast, the distal ileal loop (blue) hardly changes in position relative to the SMA during late herniation, but does so within a few days after return in the abdominal cavity. As Fig. 9 shows, this latter change in position is due to a movement of this part of the gut from midsagittal and ventral to right-lateral and more dorsal. Even though the rotational change of this part of the intestine after intestinal return appears extensive, the linear change in position is only minor. If one insists on using the term rotation for this movement, it would be largely around a craniocaudal axis (in the transverse plane) rather than a dorsoventral axis (frontal plane). In view of the brief time window and orientation of the apparent rotational axis, we conclude that the distal ileum and cecum “slide” rather than “rotate” as from the umbilical orifice to the lower-right abdominal cavity. “En-bloc rotation” is a conceptually simple and, therefore, attractive model of intestinal development, but the very different degrees, rates, and developmental timing of the apparent rotation of different parts of the midgut shows that this model cannot be upheld. Our present study shows that hierarchical looping is a viable new model to describe key morphogenetic events in intestinal development (for a comparison of both models, see Fig. 13).Fig. 12

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