Return of the intestinal loop to the abdominal coelom after physiological umbilical herniation in the early fetal period

Abstract

The intestine elongates during the early fetal period, herniates into the extraembryonic coelom, and subsequently returns to the abdominal coelom. The manner of herniation is well‐known; however, the process by which the intestinal loop returns to the abdomen is not clear. Thus, the present study was designed to document and measure intestinal movements in the early fetal period in three dimensions to elucidate the intestinal loop return process. Magnetic resonance images from human fetuses whose intestinal loops herniated (herniated phase; n = 5) while returning to the abdominal coelom [transition phase; n = 3, crown–rump length (CRL)] 37, 41, and 43 mm] and those whose intestinal loops returned to the abdominal coelom normally (return phase; n = 12) were selected from the Kyoto Collection. Intestinal return began from proximal to distal in samples with CRL of 37 mm. Only the ileum ends were observed in the extraembryonic coelom in samples with CRLs of 41 and 43 mm, whereas the ceca were already located in the abdominal coeloms. The entire intestinal tract had returned to the abdominal coelom in samples with CRL > 43 mm. The intestinal length increased almost linearly with fetal growth irrespective of the phase (R2 = 0.90). The ratio of the intestinal length in the extraembryonic coelom to the entire intestinal length was maximal in samples with CRLs of 32 mm (77%). This ratio rapidly decreased in three of the samples that were in the transition phase. The abdominal volumes increased exponentially (to the third power) during development. The intestinal volumes accounted for 33–41% of the abdominal volumes among samples in the herniated phase. The proportion of the intestine in the abdominal cavity increased, whereas that in the liver decreased, both without any break or plateau. The amount of space available for the intestine by the end of the transition phase was approximately 200 mm3. The amount of space available for the intestine in the abdominal coelom appeared to be sufficient at the beginning of the return phase in samples with CRLs of approximately 43 mm compared with the maximum intestinal volume available for the extraembryonic coelom in the herniated phase, which was 25.8 mm3 in samples with CRLs of 32 mm. A rapid increase in the space available for the intestine in the abdominal coelom that exceeded the intestinal volume in the extraembryonic coelom generated an inward force, leading to a ‘sucked back’ mechanism acting as the driving force. The height of the hernia tip increased to 8.9 mm at a maximum fetal CRL of 37 mm. The height of the umbilical ring increased in a stepwise manner between the transition and return phases and its height in the return phase was comparable to or higher than that of the hernia tip during the herniation phase. We surmised that the space was generated in the aforementioned manner to accommodate the herniated portion of the intestine, much like the intestine wrapping into the abdominal coelom as the height of the umbilical ring increased.

Midgut development in rat embryos using microcomputed tomography

“…Soffers et al (2015) addressed the development of the whole intestine and concluded that the intestine does not "rotate" but "slides" from the umbilical coelom into the abdominal cavity 7 . Recently, Nagata et al (2019) studied the return of intestinal loops after PUH, proposing an alternative "wrapped model" instead of the classical "rope model" 8 .…”

Relationship between rectal abdominis muscle position and physiological umbilical herniation and return: A morphological and morphometric study

“…Such growth proceeded regardless of the phases of herniation. In our previous study, the ventral‐dorsal height of the abdomen (abdominal height) was an exception, as there was increased abdominal height between the transition phase and return phase (Nagata et al, 2019).…”

“…Drastic and dynamic change occurs between the herniation phase and return phase of IL. The elongated IL herniated in the extraembryonic coelom, which promptly returns in the abdominal coelom in the fetal stage at approximately 40 mm (Kim et al, 2003; Mall, 1899; Nagata et al, 2019; Snyder Jr & Chaffin, 1952). Prompt changes in both the abdominal and umbilical compositions as well as volume should occur.…”

“…The intestine elongates considerably during the embryonic period, involving two drastic phenomena, namely, herniation into the extraembryonic coelom from the Carnegie stage (CS17) (herniation phase) and return into the abdominal coelom (return phase) (Kim, Kim, Ahn, Kim, & Park, 2003; Mall, 1898; Meckel, 1817; Ueda, Yamada, Uwabe, Kose, & Takakuwa, 2016). There is some consensus regarding the timing of its return into the abdominal coelom (Kim et al, 2003; Mall, 1899; Nagata et al, 2019; Snyder Jr & Chaffin, 1952), which has been reported to occur when the crown‐rump length (CRL) of the fetus is approximately 40 mm.…”

Development of extrinsic innervation in the abdominal intestines of human embryos

“…The delay in innervation may correspond with the rapid growth of the midgut resulting in the formation of loops (Soffers et al ., 2015; Ueda et al ., 2016). In agreement, the ganglionic cells of the intrinsic ENS begin to form the myenteric plexus at ~CS22 (Okamoto and Ueda, 1967, Fu et al ., 2004, Wallace and Burns, 2005), just prior to intestinal return and resolution of the hernia (Soffers et al ., 2015; Nagata et al ., 2019). Furthermore, it has been reported, however, that the mitotic index in the ileocaecal region of 11–12 weeks old foetuses was still ~2‐fold higher than in the oesophagus or hindgut (Vaos, 1989), while enteric neurons were less developed in the ileum than in adjacent parts of the gut (Tam, 1986).…”