Hostname: page-component-848d4c4894-x24gv Total loading time: 0 Render date: 2024-06-02T23:39:37.928Z Has data issue: false hasContentIssue false
  • English
  • Français

Gut lumen formation defect can cause intestinal atresia: evidence from histological studies of human embryos and intestinal atresia septum

Published online by Cambridge University Press:  12 April 2021

Xuelai Liu ,
Peiyu Hao ,
Vincent Chi Hang Lui Open the ORCID record for Vincent Chi Hang Lui [Opens in a new window] ,
Xianghui Xie ,
Yingchao Li ,
Yanbiao Song ,
Long Li  and
Zhe-Wu Jin
Xuelai Liu
Affiliation:
Department of Surgery, Capital Institute of Pediatrics affiliated Children Hospital, Beijing 100020, China
Peiyu Hao
Affiliation:
Department of Anatomy, Wuxi School of Medicine, Jiangnan University, WuXi, Jiangsu 214122, China
Vincent Chi Hang Lui
Affiliation:
Department of Surgery, Li Ka Shing Faculty of Medicine, The University of Hong Kong, HKSAR, Hong Kong
Xianghui Xie
Affiliation:
Department of Surgery, Capital Institute of Pediatrics affiliated Children Hospital, Beijing 100020, China
Yingchao Li
Affiliation:
Department of Pediatric Surgery, HeBei Medical University affiliated 2nd Hospital, ShiJiaZhuang, Hebei 050000, China
Yanbiao Song
Affiliation:
Central Laboratory, HeBei Medical University affiliated 2nd Hospital, ShiJiaZhuang, Hebei 050000, China
Long Li*
Affiliation:
Department of Surgery, Capital Institute of Pediatrics affiliated Children Hospital, Beijing 100020, China
Zhe-Wu Jin*
Affiliation:
Department of Anatomy, Wuxi School of Medicine, Jiangnan University, WuXi, Jiangsu 214122, China
*
Address for correspondence: Long Li, Department of Surgery, Capital Institute of Pediatrics affiliated Children Hospital, No.2, Yabao Rd, Chaoyang district, Beijing, 100020 China. Email: lilong23@126.com; Zhe-Wu Jin, Department of Anatomy, Wuxi School of Medicine, Jiangnan University, WuXi, 214122 China. Email: zwjin@jiangnan.edu.cn
Address for correspondence: Long Li, Department of Surgery, Capital Institute of Pediatrics affiliated Children Hospital, No.2, Yabao Rd, Chaoyang district, Beijing, 100020 China. Email: lilong23@126.com; Zhe-Wu Jin, Department of Anatomy, Wuxi School of Medicine, Jiangnan University, WuXi, 214122 China. Email: zwjin@jiangnan.edu.cn
Get access Rights & Permissions [Opens in a new window]

Abstract

Intestinal atresia (IA), a common cause of neonatal intestinal obstruction, is a developmental defect, which disrupts the luminal continuity of the intestine. Here, we investigated (i) the process of lumen formation in human embryos; and (ii) how a defective lumen formation led to IA. We performed histological and histochemical study on 6–10 gestation week human embryos and on IA septal regions. To investigate the topology of embryonic intestine development, we conducted 3D reconstruction. We showed that a 6–7th gestation week embryonic gut has no lumen, but filled with mesenchyme cells and vacuoles of a monolayer of epithelial cells. A narrow gut lumen was formed by gestation week-9, the gut was filled with numerous vacuoles of different sizes, some vacuoles were merging with the developing embryonic gut wall. At gestation week-10, a prominent lumen was developed, only few vacuoles were present and were merging with the intestine wall. At IA septal regions, vacuoles were located in the submucous layer, covered by a single layer of epithelium without glandular structure, and surrounded with fibrous tissue. The mucosal epithelium was developed with lamina propria and basement membrane, but the submucosa and the longitudinal smooth muscle layers were not properly developed. Hence, the vacuoles in IA septum could represent a remnant of vacuoles of embryonic gut. In conclusion, the fusion of vacuoles with the developing intestine wall associates with the disappearance of vacuoles and gut lumen formation in human embryos, and perturbation of these developmental events could lead to IA.

Keywords

Vacuolesrecanalizationintestinal atresiaembryos
Type
Original Article
Information
Journal of Developmental Origins of Health and Disease , Volume 13 , Issue 1 , February 2022 , pp. 61 - 67
Check for updates
Copyright
© The Author(s), 2021. Published by Cambridge University Press in association with International Society for Developmental Origins of Health and Disease

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Grosfeld, J, O’Neill, J, Coran, A, Fonkalsrud, E. Duodenal Atresia and Stenosis– Annular Pancreas, 2006. Mosby.Google Scholar
Tandler, J. Zur Entwicklungsgeschichte des menschlichen Duodenum in fruhen Embryonalstadien. Morphol Jahrb. 1900; 29, 187.Google Scholar
Cheng, W, Tam, PK. Murine duodenum does not go through a “solid core” stage in its embryological development. Eur J Pediatr Surg. 1998; 8(4), 212–215.CrossRefGoogle Scholar
Kanard, RC, Fairbanks, TJ, De Langhe, SP, et al. Fibroblast growth factor-10 serves a regulatory role in duodenal development. J Pediatr Surg. 2005; 40(2), 313–316.CrossRefGoogle ScholarPubMed
Fairbanks, TJ, Kanard, R, Del Moral, PM, et al. Fibroblast growth factor receptor 2 IIIb invalidation—a potential cause of familial duodenal atresia. J Pediatr Surg. 2004; 39(6), 872–874.CrossRefGoogle ScholarPubMed
Louw, JH, Barnard, CN. Congenital intestinal atresia; observations on its origin. Lancet. 1955; 269(6899), 1065–1067.CrossRefGoogle ScholarPubMed
Barnard, CN, Louw, JH. The genesis of intestinal atresia. Minn Med. 1956; 39(11), 745; passim.Google ScholarPubMed
Barnard, CN. The genesis of intestinal atresia. Surg Forum. 1957; 7, 393–396.Google Scholar
Morris, G, Kennedy, A Jr, Cochran, W. Small bowel congenital anomalies: a review and update. Curr Gastroenterol Rep. 2016; 18(4), 16.CrossRefGoogle ScholarPubMed
Zhang, S, Liu, X, Wang, H, Peng, J, Wong, KK. Silver nanoparticle-coated suture effectively reduces inflammation and improves mechanical strength at intestinal anastomosis in mice. J Pediatr Surg. 2014; 49(4), 606–613.CrossRefGoogle ScholarPubMed
Liu, X, Hao, W, Lok, CN, Wang, YC, Zhang, R, Wong, KK. Dendrimer encapsulation enhances anti-inflammatory efficacy of silver nanoparticles. J Pediatr Surg. 2014; 49(12), 1846–1851.CrossRefGoogle ScholarPubMed
Liu, X, Gao, P, Du, J, Zhao, X, Wong, KKY. Long-term anti-inflammatory efficacy in intestinal anastomosis in mice using silver nanoparticle-coated suture. J Pediatr Surg. 2017; 52(12), 2083–2087.CrossRefGoogle ScholarPubMed
Rodriguez, AM, Downs, KM. Visceral endoderm and the primitive streak interact to build the fetal-placental interface of the mouse gastrula. Dev Biol. 2017; 432(1), 98–124.CrossRefGoogle ScholarPubMed
Ki, EY, Jang, DG, Jeong, DJ, Kim, CJ, Lee, SJ. Rare case of complete colon structure in a mature cystic teratoma of the ovary in menopausal woman: a case report. BMC Womens Health. 2016; 16(1), 70.CrossRefGoogle Scholar
Bourret, A, Chauvet, N, de Santa Barbara, P, Faure, S. Colonic mesenchyme differentiates into smooth muscle before its colonization by vagal enteric neural crest-derived cells in the chick embryo. Cell Tissue Res. 2017; 368(3), 503–511.CrossRefGoogle ScholarPubMed
Micchelli, CA. The origin of intestinal stem cells in Drosophila. Dev Dyn. 2012; 241(1), 85–91.CrossRefGoogle ScholarPubMed
Bely, AE. Early events in annelid regeneration: a cellular perspective. Integr Comp Biol. 2014; 54(4), 688–699.CrossRefGoogle ScholarPubMed
Kimes, PK, Liu, Y, Neil Hayes, D, Marron, JS. Statistical significance for hierarchical clustering. Biometrics. 2017; 73(3), 811–821.CrossRefGoogle ScholarPubMed
Kern, M, Lex, A, Gehlenborg, N, Johnson, CR. Interactive visual exploration and refinement of cluster assignments. BMC Bioinf. 2017; 18(1), 406.CrossRefGoogle ScholarPubMed
Heileman, KL, Tabrizian, M. Dielectric spectroscopy platform to measure MCF10A epithelial cell aggregation as a model for spheroidal cell cluster analysis. Analyst. 2017; 142(9), 1601–1607.CrossRefGoogle ScholarPubMed
Agnew, DJ, Green, JE, Brown, TM, Simpson, MJ, Binder, BJ. Distinguishing between mechanisms of cell aggregation using pair-correlation functions. J Theor Biol. 2014; 352, 16–23.CrossRefGoogle ScholarPubMed
Liu, X, Song, Y, Hao, P, et al. Delayed development of vacuoles and recanalization in the duodenum: a study in human fetuses to understand susceptibility to duodenal atresia/stenosis. Fetal Pediatr Pathol. 2021; doi: 10.1080/15513815.2021.1876191, 1–7.Google ScholarPubMed