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. 2020 Feb 16;237(1):166–175. doi: 10.1111/joa.13174

Three‐dimensional morphogenesis of the omental bursa from four recesses in staged human embryos

Tatsuro Nakamura 1, Shigehito Yamada 2,3,✉, Takuya Funatomi 4, Tetsuya Takakuwa 3, Hisashi Shinohara 5, Yoshiharu Sakai 1
PMCID: PMC7309287  PMID: 32064626

Abstract

The omental bursa (OB) is a complex upper abdominal structure in adults. Its morphological complexity stems from embryonic development. Approximately 200 years ago, the first theory regarding OB development was reported, describing that the OB developed from changes in the position of the stomach and its dorsal mesentery. Thereafter, the second theory reported that the OB originated from three recesses: the right pneumato‐enteric recess (rPER), hepato‐enteric recess (HER), and pancreatico‐enteric recess (PaER). However, the first theory, focusing on the rotation of the stomach, is still described in certain modern embryology textbooks. These two coexisting embryological theories deter the understanding of the anatomical complexity of the OB. This study aimed to unify these two theories into realistic illustrations. Approximately 10 samples per stage among Carnegie stage (CS) 13 and CS21 were microscopically observed and histological serial sections of the representative samples were aligned using the new automatic alignment method. The aligned images were segmented computationally and reconstructed into 3D models. The rPER and the HER encompassed the right half circumference of the esophagus and the stomach at CS13 and CS14, the PaER spread dorsal to the stomach and formed a discoid shape at CS15 and CS16, the infracardiac bursa (ICB) was separated by the diaphragm at CS17 and CS18, and the fourth recess, which we called the greater omental recess (GOR), extended caudally from the PaER among CS19 and CS21. The present results indicate that the fourth recess is also the origin of the OB. These two theories over 200 years can be generally unified into one embryological description indicating a new recess as the origin of the OB.

Keywords: automatic alignment, embryology, omental bursa, three‐dimensional morphogenesis

We visualized the 3D morphogenesis of the OB from four recesses in staged human embryos through automatic alignment of serial sections. Our results potentially unify the previous theories into one modern embryological description considering the new recess.

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1. INTRODUCTION

The omental bursa (OB) is the cavity lying dorsal to the stomach and communicates with the primary peritoneal cavity through the epiploic foramen of Winslow (Liebermann‐Meffert et al., 1983). Clinically, it serves as an essential anatomical landmark in gastrointestinal surgery (Brenkman et al., 2017) and is rarely a cause of internal hernia (Basu and Jacobs, 2009). This complex structure has remained challenging to understand because the OB comprises several regions including the superior recess (SuR), splenic recess (SpR), inferior recess (IR), and vestibule (Schulte et al., 2016). This anatomical complexity develops ‘during the prenatal period’, described in Larsen’s Human Embryology (Schoenwolf and Larsen, 2015).

The first theory of OB development was proposed by Müller (1830). According to this study on human embryos, the OB is a recess of the peritoneal cavity that results from changes in the position of the stomach, liver, and gastric mesenteries (Figure 1A). This theory had been generally accepted for 50 years. Thereafter, several studies investigated the origin of the OB in more detail (Brachet, 1895; His, 1880; Hochstetter, 1888; Mall, 1891; Ravn, 1887; Stoss 1890; 1892; Swaen, 1896; 1897) and it gradually became apparent that the OB results from the growth of a peritoneal recess already present before rotation of the stomach. Gastric rotation is said to contribute only to modifying the spatial configuration of the growing OB. Broman (1904) confirmed the development of the OB through a 3D reconstruction of detailed serial sections from human embryos and fetuses. He demonstrated that the enlargement of the recess isolated the organs from the mesenchymal mass, and the developing diaphragm separated the infracardiac bursa (ICB). Afterward, he named the three recesses: the right pneumato‐enteric recess (rPER), the hepato‐enteric recess (HER), and the pancreatico‐enteric recess (PaER) (Figure 2) (Broman, 1938). To date, several mechanistic concepts have been proposed to explain the formation of the rPER and the HER as follows: (1) invagination of the peritoneal mesothelium into the mesenchyme of the ‘mesenteries’ (Stoss, 1890; Brachet, 1895; Swaen, 1897; Broman, 1904; Bryden et al., 1973); (2) downgrowth of a sagittally oriented peritoneal fold, which places the vena cava, leading to separation of the recess from the rest of the main peritoneal cavity (Hochstetter, 1888; Mathes, 1895; Pernkopf, 1922; Clara, 1955; Boenig and Bertoloni, 1965); (3) de novo formation of small cavities within the mesenchyme of the ‘mesenteries’, which fuses to form the recess that later becomes connected to the peritoneal cavity (Kanagasuntheram, 1957). The second theory of OB development has been accepted in some embryology textbooks (Arey, 1934; Frazer, 1947; Hamilton, Boyd and Mossman, 1952; Patten, 1953; Hinrichsen, 1990).

Figure 1.

Figure 1

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First theory of the development of the omental bursa (OB) based on the stomach rotation. (A) Schema from Muller’s study (1830) with slight modification. (B) Schema in modern embryology textbooks. The tissue linking the liver and the posterior abdominal wall is omitted. Dm, dorsal mesogastrium; Li, liver; Pa, pancreas; Sp, spleen; St, stomach

Figure 2.

Figure 2

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Second theory of the development of the omental bursa (OB) from three recesses during embryogenesis (adapted from Broman (1938) with slight modification). (A) Organs are isolated by three recesses: the right pneumato‐enteric recess (rPER), the hepato‐enteric recess (HER), and the pancreatico‐enteric recess (PaER) in the frontal view. (B) The infracardiac bursa (ICB) is separated during diaphragm (Di) development and the OB is formed from the abdominal recesses. (C) The liver is linked to the posterior abdominal wall through the caval mesentery during early embryogenesis in the horizontal view. Li, liver; lL, left lung; rL, right lung; Pa, pancreas; Pe, pericardium; Sp, spleen; St, stomach

However, the first theory, focused on the rotation of the stomach, is still described in modern prominent embryology textbooks (Moore et al., 2008; Schoenwolf and Larsen, 2015; Sadler and Langman, 2019) (Figure 1B), although more recent studies disagreed with the first theory (Viikari, 1950; Liebermann‐Meffert, 1969; Heckl, 1979; Brummer, 1982). The two coexisting theories complicate understanding of the anatomical complexity of the OB and the ICB. Actually, these two theories are illustrated in Gray’s Anatomy (Standring, 2016), and the topographic anatomy of the ICB has not been known among most surgeons until recently (Nakamura et al., 2019).

In the present study, the 3D morphogenesis of the OB from the recesses was revisited by reconstructing serial sections from the Kyoto Collection of Human Embryos (http://bird.cac.med.kyoto-u.ac.jp), using the new automatic alignment method (Kajihara et al., 2019). We attempted to unify these two theories in realistic illustrations.

2. MATERIALS AND METHODS

2.1. Human embryo specimens

The Kyoto Collection is composed of approximately 44 000 human embryos, which are preserved at the Congenital Anomaly Research Center of Kyoto University (Nishimura et al., 1968; Shiota, 1991; Yamaguchi and Yamada, 2018). In most cases, pregnancy was terminated during the first trimester owing to socioeconomic reasons under the Maternity Protection Law of Japan. After the aborted embryos were transported to the laboratory, they were measured and categorized in accordance with the Carnegie stage (CS), as described by O’Rahilly and Müller (O’Rahilly et al., 1987). The 547 well‐preserved specimens diagnosed as normal, were fixed in Bouin’s fluid for a day, transferred to 10% formalin, dehydrated, embedded in paraffin through standard methods, and serially sectioned at 10‐µm thickness.

2.2. Histological observations

We observed 10 samples per stage among CS13 and CS21 and confirmed that following structures were well‐preserved in each serial section: rPER, HER, PaER, ICB, stomach, mesentery, lung, liver, pancreas, and spleen. Thereafter, we selected the most appropriate sample for 3D model per stage (Table 1).

Table 1.

Characteristics of embryos for the three‐dimensinal (3D) reconstruction model

Specimen Number of automatic aligned sections Number of manual segmented sections 3D reconstructed structures
CS ID Gut rPER HER PaER ICB GOR Mesentery dp vp Lung Dia Spleen Liver
13 4,953 211 126 ○ ○ ○ － － － ○ ○ ○ ○ － － ○
14 16,701 148 87 ○ ○ ○ － － － － － － － － － －
15 7,105 195 169 ○ ○ ○ ○ － － ○ ○ ○ ○ － － －
16 10,313 192 131 ○ ○ ○ ○ － － － － － － － － －
17 4,485 360 122 ○ ○ ○ ○ － － － － － － － － －
18 24,992 272 128 ○ － ○ ○ ○ － ○ － － ○ ○ － －
19 7,711 312 157 ○ － ○ ○ ○ ○ － － － － － － －
20 4,330 276 173 ○ － ○ ○ ○ ○ － － － － － ○ －
21 11,235 404 251 ○ － ○ ○ ○ ○ ○ － － － ○ ○ －
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Abbreviations: CS, Carnegie stage; dia, diaphragm; dp, dorsal pancreas; GOR, greater omental recess; gut, esophagus, stomach and duodenum; HER, hepato‐enteric recess; ICB, infracardiac bursa; PaER, pancreatico‐enteric recess; rPER, right pneumato‐enteric recess; vp, ventral pancreas.

2.3. 3D reconstruction using the feature‐based non‐rigid registration

Serial transverse sections with minimal deformations in each CS were scanned, digitized, and saved as Microsoft Windows Bitmap Images (.bmp files) with an Olympus virtual slide system (VS120‐S5‐J; Olympus), and tissue sections on each slide were divided into individual images (Figure 3A). Thereafter, the automatic alignment method of Kajihara et al. (2019) was used for each sample. In brief, this method has been developed for the 3D reconstruction from histological serial section images and comprises two modules: non‐rigid registration for an image pair and accumulation of serial images. The module of non‐rigid registration reveals a complex deformation with a smaller number of control points by estimating the rigid transformation in local regions and integrating them to interpolate the transformations at every pixel. Further, module of accumulation accurately selects the target image for registration to prevent discontinuity and adopts scale adjustment to prevent scale changes caused by non‐rigid registration. This method enables 3D reconstruction from hundreds of serial section images automatically (Figure 3B). Finally, completely aligned serial sections were segmented and computationally reconstructed into 3D models, using the amira software, version 6.4.0 (Thermo Fisher Scientific, Bordeaux, France) (Figure 3D). We evaluated morphological changes in each recess and adjacent organs sequentially among CS13 and CS21.

Figure 3.

Figure 3

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Procedure of three‐dimensional reconstruction from serial histological sections. (A) Tissue sections on a scanned slide were divided individually (red dotted square). (B) The images were aligned automatically through feature‐based non‐rigid registration. (C) The images were conventionally stacked using imagej software and manually aligned using amira software. (D) Target structures were segmented manually (blue area) and reconstructed using amira software

2.4. Validation of the automatic alignment

Serial sections at CS13, CS15, CS18, and CS21 were manually aligned and conventionally reconstructed to validate the accuracy of automatically aligned 3D models. Tissue images were stacked using software imagej™ (version 1.42q, National Institutes of Health, Bethesda, MD, USA; https://imagej.nih.gov/ij/). Thereafter, they were manually aligned and segmented using the amira software (Figure 3C). The representative view of the 3D model in each CS was compared for visual assessment (Pichat et al., 2018). The alignment duration was examined in both procedures.

2.5. Ethics

The present study was approved by the Ethics Committee of Kyoto University Graduate School and Faculty of Medicine (R0316).

3. RESULTS

3.1. Assessment of automatic alignment

The 3D models from automatic alignment were contrasted with those of manual alignment. Figure 4 shows the visual assessment of the models at CS13, CS15, CS18, and CS21. Models were evaluated from the ventral side. In each CS, both models displayed similar morphology for the stomach and the recesses.

Figure 4.

Figure 4

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Visualization of automatic alignment at CS13, C15, CS18, and CS21 from the ventral side. Upon automatic alignment (light blue), the recesses displayed the same form as manually aligned ones (green). Stomach (st) rotations were similar during both phenomena

Furthermore, the alignment duration was estimated in both procedures. At CS13, manual alignment was faster than automatic alignment. However, at other stages, automatic alignment was faster than manual alignment. At CS21, it took 2.2 min per 100 images during automatic alignment (Table 2).

Table 2.

Comparison of the duration between automatic and manual alignment

Specimen Number of sections (n) Required time (min) A/M × 100 (%) A/n × 100 (min)
CS ID automatic (A) manual (M)
13 4,953 211 67 38 176 32
15 7,105 195 35 36 97 18
18 24,992 272 27 49 55 10
21 11,235 404 9 77 12 2.2
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Abbreviation: CS, Carnegie stage.

3.2. A series of the right pneumato‐enteric recess and the hepato‐enteric recess (CS13 and CS14)

The rPER and the HER were microscopically observed as a series of recesses at CS13 and CS14. The consecutive recess isolated the esophagus and stomach from the lung and liver. The 3D model at CS13 showed that the stomach had not rotated yet, and the recess covered the right half circumference of the esophagus and the stomach (Figure 5A). The cranial edge of the rPER was located between the right lung and the esophagus (Figure 5B), and the HER spread between the liver and the esophagus (Figure 5B) and broadly connected to the peritoneal cavity on the caudal side.

Figure 5.

Figure 5

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Histological sections with segmentation and a ventral view of the three‐dimensional model at Carnegie stage (CS) 13 (A–C) and CS15 (D‐F). (A) The right pneumato‐enteric recess (rPER) and the hepato‐enteric recess (HER) were consecutively observed along the right side of the esophagus (es) and stomach (st). (B) The transverse section at the level of line (a). The rPER (light blue segmentation) was located between the esophagus (pink segmentation) and the right lung (rl, blue segmentation). (C) A transverse section at the level of line (b). The HER (light blue segmentation) isolated the stomach (pink segmentation) and the liver (li). (D) The pancreatico‐enteric recess (PaER) extended to the left lateral side from the HER. The PaER has a discoid morphology. (E) The transverse section at the level of line (c). The HER and the PaER (light blue segmentation) were surrounded by the liver, the stomach, and the caval mesentery (CM). (F) The transverse section at the level of line (d). The PaER narrowly spread into the dorsal mesogastrium. dp, dorsal pancreas (yellow segmentation); gc, gastric corpus; vp, ventral pancreas (green segmentation)

3.3. Spreading of the pancreatico‐enteric recess (CS15 and CS16)

As the stomach gradually rotated and the gastric corpus developed at CS15 and CS16, the PaER was observed between the stomach and the dorsal pancreas. In the 3D model at CS15, the PaER spread dorsal to the stomach as a narrow split into the dorsal mesogastrium and developed a discoid morphology (Figure 5D–F). The rPER and the HER extended in the rostro‐caudal direction during embryonic development.

3.4. Separation of the infracardiac bursa (CS17 and CS18)

After spreading of the PaER, the diaphragm developed, and the esophageal hiatus was closed at CS17 and CS18. The 3D model of CS18 showed that rPER was almost separated by the diaphragm and the ICB was retained in the lower mediastinum as the closed space (Figure 6A,B). Simultaneously, the SuR was established on the abdominal side immediately below the diaphragm. The PaER broadened in comparison with the previous model at CS15. The passage between the HER and the main peritoneal cavity was narrowed owing to stomach rotation.

Figure 6.

Figure 6

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Histological section with segmentation and a ventral view of the three‐dimensional model at Carnegie stage (CS) 18 (A, B) and CS21 (C, D). (A) The infracardiac bursa (ICB) was almost separated by the diaphragm (black arrows) from the right pneumato‐enteric recess (rPER). Simultaneously, the superior recess (SuR) was being formed from the hepato‐enteric recess (HER). (B) The section at the level of plane (a). The esophageal hiatus was almost closed during diaphragm development (black arrows). (C) The greater omental recess (GOR, light blue segmentation) caudally extended from the pancreatico‐enteric recess (PaER, light blue segmentation). (D) The section at the level of plane (b). The splenic recess (SpR, light blue segmentation) isolated the spleen (sp) from the stomach (st, pink segmentation). ca, cardia; di, diaphragm; es, esophagus (pink segmentation); fu, fundus; gc, gastric corpus; li, liver; rl, right lung

3.5. Extension of the greater omental recess (CS19, CS20 and CS21)

After CS19, the greater omental recess (GOR) was detected as a split in the dorsal mesogastrium. It extended caudally from the PaER and was enlarged during embryonic development (Figure 6C,D). The spleen was then observed in the dorsal mesogastrium at approximately CS20, and the SpR was identified as the extension of the PaER towards the hilum of the spleen. The stomach was enlarged; the fundus was clearly visible. The duodenum did not adhere to the posterior abdominal wall, and the foramen of Winslow was not yet established.

3.6. Morphological changes in the OB in accordance with the CS

Morphogenesis in the OB and stomach was continuously altered in the frontal view among CS13 and CS21 (Figure 7).

Figure 7.

Figure 7

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Ventral view of three‐dimensional morphological changes in the omental bursa and the stomach among Carnegie stage (CS) 13 and CS21. The right pneumato‐enteric recess (rPER) and the hepato‐enteric recess (HER) encompassed the right half circumference of the esophagus and the stomach (st) at CS13 and CS14. The pancreatico‐enteric recess (PaER) dorsally spread to the stomach and formed a discoid structure at CS15 and CS16. The infracardiac bursa (ICB) was separated at CS17 and CS18. The greater omental recess (GOR) caudally extended from the PaER at CS19 and CS21

4. DISCUSSION

This study examined morphogenesis of the OB from recesses in staged human embryos through 3D reconstructions of serial sections. The present results show that the rPER and the HER encompassed the right half circumference of the esophagus and the stomach at CS13 and CS14, the PaER spread dorsally to the stomach at CS15 and CS16, the ICB was separated by the diaphragm at CS17 and CS18, and the GOR extended into the dorsal mesogastrium from the PaER at CS19 and CS21. These results support the second theory, adding the observation that the GOR originated from the PaER as the fourth recess. The GOR clearly differed from the PaER and extended caudally with a mesenteric constriction.

To examine morphogenesis of various organs in the embryos, 3D reconstruction of serial sections is very useful and has long been used. Over several decades, the procedure has been drastically changed from Born’s wax plate method (Born, 1876) to the software‐based digital method (Yamada et al., 2007). However, it still takes great effort to reconstruct numerous serial sections (Bardol et al., 2018). This study is the first to apply the automatic alignment method to restore deformations and for accurate alignment of serial sections. When embryo sections were large, it required less time and effort to align the histological sections in comparison with conventional manual procedures (Table 2). In this study, the effect of non‐rigid registration was not significant because we selected sections with minor deformation. However, intrinsic attributes of the method can be effectively demonstrated upon reconstruction of numerous deformed samples, confirming that the automatic alignment method is functional on a sampling inspection. The present results indicate that the automatic alignment is better than the manual alignment method to ensure objectivity.

The OB is a basic anatomical structure in the upper abdomen in adults and is normally collapsed on computed tomography or magnetic resonance imaging; therefore, it is difficult to understand its precise 3D structure not only for medical students (Xu et al., 2015) but also for surgeons (Brenkman et al., 2017). During surgical treatment of gastrointestinal cancers, the concept of excising organ‐specific mesenteries has become increasingly important in recent years, namely, total for mesorectal excision (Heald et al., 1982; Heald and Ryall, 1986), complete mesocolic excision (Hohenberger et al., 2009), and systematic mesogastric excision (Shinohara et al., 2018). It is imperative for surgeons to understand the development of the mesenteries (Sakai, 2016). In particular, morphogenesis in the mesogastrium is complex and closely associated with that in the OB. Intensive discussions of morphological changes in the OB are urgently required. However, horizontal illustrations of the first theory may hinder the understanding of the anatomy of the OB because they unintentionally lead to the misunderstanding that the OB is formed through the fusion of the liver and the posterior abdominal wall after stomach rotation. Horizontal illustrations are limited in their lengthwise description of the OB. Thus, we provided 3D illustrations of OB development from four recesses (Figure 8). Moreover, we demonstrated the origin of the complex regions of the OB in adults (Figure 9). These illustrations potentially bridge the gap between embryological and anatomical knowledge regarding the OB.

Figure 8.

Figure 8

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Schematic ventral views of the development of the omental bursa from four recesses. The right pneumato‐enteric recess (rPER) and the hepato‐enteric recess (HER) were consecutive at the right side of the esophagus (es) and stomach (st) at CS13 and CS14. Thereafter, the pancreatico‐enteric recess (PaER) expanded toward the dorsal side of the stomach from the HER at CS15 and CS 16. Subsequently, the infracardiac bursa (ICB) was established through closure of the esophageal hiatus during diaphragm (di) development at CS17 and CS18. Furthermore, the greater omental recess (GOR) caudally extended from the PaER among CA19 and CS21. dp, dorsal pancreas; mpc, main peritoneal cavity; sp, spleen

Figure 9.

Figure 9

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Origin of the omental bursa in adults. The foramen of Winslow (FOW), vestibule (Ve), and Superior recess (SuR) originate from the hepato‐enteric recess (shown as a blue area). The infracardiac bursa (ICB) originates from the right pneumato‐enteric recess (shown as a green area). The splenic recess (SpR) originates from the pancreatico‐enteric recess (shown as a red area). The inferior recess (InR) originates from the greater omental recess (shown as a purple area)

This study has several limitations. First, the 3D images were reconstructed for only one sample per CS because segmentation of many structures was time‐consuming. Hence, a selection bias among samples may have influenced the results. To reduce this error, we macroscopically confirmed that approximately 10 cases at each CS were almost similar to the representative sample. A deep learning‐based automatic segmentation has been conducted using magnetic resonance imaging (Wang et al., 2018), which may be used for segmentation of numerous serial sections. Second, we could not examine the initiation of the rPER and the formation of the foramen of Winslow owing to a lack of well‐preserved histological sections. A large collection of early embryos and fetuses through international networks and collaborations may be required to investigate these aspects in the future.

5. CONCLUSIONS

We visualized the 3D morphogenesis of the OB from recesses in staged human embryos through automatic alignment of serial sections. The present results indicate that the fourth recess is also the origin of the OB, i.e. the GOR. Our results potentially unify the previous theories into one modern embryological description considering the new recess.

AUTHOR CONTRIBUTIONS

Study conception and design: Nakamura, Yamada, Sakai, Shinohara. Acquisition of data: Nakamura, Yamada, Funatomi. Analysis and interpretation of data: Nakamura, Yamada, Funatomi, Takakuwa. Drafting of manuscript: Nakamura, Yamada. Critical revision: Sakai, Shinohara, Takakuwa.

ACKNOWLEDGEMENTS

We thank Haruyuki Makishima and Tomoaki Okada from Kyoto University for helpful opinions and information, and Itsuro Kamimura from Maxnet Corporation for providing technical support for 3‐dimensional reconstructions. This work was supported by ISHIZUE 2019 of the Kyoto University Research Development Program. We would also like to thank Editage (www.editage.jp) for English language editing. The authors have no conflicts of interest to disclose.

Nakamura T, Yamada S, Funatomi T, Takakuwa T, Shinohara H, Sakai Y. Three‐dimensional morphogenesis of the omental bursa from four recesses in staged human embryos. J. Anat. 2020;237:166–175. 10.1111/joa.13174

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