Special Issue:

Emerging and Re-Emerging Animal Health Challenges in Low and Middle-Income Countries

Ontogenesis of Rectum in Local Awassi Sheep Fetuses (Ovis aris) During Prenatal Periods

Ali Mobder Niyf*, Jafar Ghazi Abbas Al-Jebori

College of Veterinary Medicine, Al-Qassim Green University, 51013 Babylon, Iraq

Received | July 14, 2024; Accepted | September 14, 2024; Published | October 30, 2024

*Correspondence | Ali Mobder Niyf, College of Veterinary Medicine, Al-Qassim Green University, 51013 Babylon, Iraq; Email: alimobderabdalhasan@vet.uoqasim.edu.iq

Citation | Niyf AM, Al-Jebori JGA (2024). Ontogenesis of rectum in local Awassi sheep fetuses (Ovis aris) during prenatal periods. J. Anim. Health Prod. 12(s1): 45-54.

DOI | http://dx.doi.org/10.17582/journal.jahp/2024/12.s1.45.54

ISSN (Online) | 2308-2801

 

 

Copyright: 2024 by the authors. Licensee ResearchersLinks Ltd, England, UK.

This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (https://creativecommons.org/licenses/by/4.0/).

Introduction

The intestinal development is related to morphological variations, an increasing manufacture of mucus, and the digestive system is adapted to different nutrients and new immunological microorganisms and nutrition antigens (Tano et al., 2014). From an embryological perspective, the large intestinal tube develops during the development of the endoderm in sheep, and it shares precursor tissues with the organs of the digestive system. Later, during embryogenesis, it includes tissue from all three layers of the trilaminar embryonic disk’s germ cells (Franco et al., 2017). In general, the mesoderm layer gives rise to the epithelium and associated glands, whereas the ectoderm layer gives rise to the mesenteric layer, connective tissues, smooth muscle, and blood vessels, and the extrinsic and intrinsic innervation.

During the large intestine’s growth, dazzling molecular tissue interaction is necessary to maintain structural and functional conformism (Kostouros et al., 2020). Early in the embryonic development of ruminants, the cloaca, the chamber that connects the digestive, urinary, and genital systems, is where the hindgut tube ends. It continues in adult reptiles, birds, and amphibians, but in ruminants, it reflects a temporary structural organ. It ends when the urorectal septum (mesenchyme partition) divides the cloaca into the dorsal cavity, which is endless from the end of the hindgut to the creation of the rectum at the end of the first trimester of pregnancy. In contrast, the urogenital sinus and ventral cavity are infinitely large. The top portion of the allantois and urogenital sinus give rise to the urethra and bladder of urine (Fletcher and Weber, 2004).

Currently, there are not sufficient studies on the rectum histogenesis in prenatal developmental stages of sheep’s fetuses. Therefore, this study attempts to analyze histomorphological description and the timing of first anlage of the components and parts of rectum at prenatal periods.

MATERIALS AND METHODS

Experimental animals

The purpose of this work was to describe the histomorphological developmental of rectum in prenatal periods of local awassi sheep’s fetuses (Ovis aris) where experimental samples are gathered from September to November 2024. The study was conducted on sheep fetuses from pregnant ewes that were slaughtered in Najaf’s and Babylon abattoirs for prenatal research. The sheep fetuses at prenatal stages distributed into three groups: first, second and third trimester of gestation according to the gestational age which determined depending on the crown rump length (CRL) by using of following formula (Hejazi et al., 2013; Al-Jebori and Salih, 2022).

Y= (2.74X+30.15)

Sample collection and light microscope technique

The sheep fetus’s cecum was preserved in buffered formalin (10%), dried out using a sequence of increasing alcohol concentrations, cleaned in xylene, and then embedded in paraffin wax. Using a rotary microtome, the blocks were sectioned at 5-6 μm thickness of slice. According to Al-Khakani et al. (2019) and Al-Janabi et al. (2022), histological sections were stained with trichrome mason’s stain, periodic acid schiff (PAS), and Hematoxyline and Eosin (H and E). Olympus light microscope with USB digital camera attached to computer slides and various magnification settings was used to study the sections (Abbas, 2014).

Statistical analysis

A computerized program (SPSS) version 21 was used to the statistical analysis of data had done by descriptive statistics

RESULTS and Discussion

Observation during first trimester of gestation (50-55) days

The body weight of sheep embryos was about 41.6± 0.927 grams, gastrointestinal tract weighted about 2.17±0.050 gram and crown rump length were observed to be 10.4 ± 0.509 cm (Table 1 and Figure 1).

 

Morphologically

The rectum appeared translucent and white in color tube located at the lower portion of the pelvic cavity. The visual diameter of the rectum was slightly larger than the descending part of the colon containing small amounts of feces green in color and consists of a single cavity, and it was not divided into two potions within thin wall and no sacculation was observed.

Histologically

Rectum would be undergoing development along with the rest of the intestinal tract and the histological structure would be similar to that of other parts of the large intestine and more development including on several layers from inner to outer: mucosa, undifferential mesenchymal tissue (pluripotential blastemic tissue), muscularis externa, and tunica serosa or adventitia (Figure 2).

 

Table 1: Body weight, gastrointestinal tract weights and grown rump length of sheep’s embryo in different ages of embryonic life.

Crown rump length (cm)	GIT weight (gram)	Body weight (gram)	Parameter age
10.4±0.509A	2.17±0.050	41.6±0.927 A	50-55 day pregnant
19.6±0.678B	67±1.760	266.6±2.088B	70-75 day pregnant
31±0.707C	98.6±3.31	860.2±5.571C	100-105 day pregnant
42.6±0.927D	208.4±4.69	1361.6±6.046D	135-140 day pregnant

Values represent mean ±S.E Different capital letters mean significant differences (P≤0.05) between different age prenatally.

 

Table 3: Height of rectal villi in sheep fetuses during prenatal periods (µm).

Long villi hieght	Middle villi hieght	Short villi hieght	Parameter age
-	-	18±06 µm	50-55 day pregnant
178±93 µm	76±0.81 µm	51±0.66	70-75 day pregnant
Disappear	Disappear	Disappear	100-105 day pregnant
Disappear	Disappear	Disappear	130-140 day pregnant

Values represent mean±S.E. Different capital letters mean significant differences (P≤0.05) between different age prenatally.

 

Table 4: Thickness of rectum wall layers in sheep fetuses during prenatal periods (µm).

Serosa	Tunica muscularis	Submucosa	Mucosa	Parameter age
11.60±0.493A	3.54±0.189A	14.1±0.181A	10.64±0.180A	50-55 day pregnant
27.74±0.224B	25.92±0.615B	12.50±0.158B	14.4±0.156B	70-75 day pregnant
29.24±0.348C	34.60±0.481C	25.72±0.659C	11.52±0.149C	100-105 day pregnant
38.58±0.506D	46.88±0.628D	25.20±0.663C	16.22±0.234D	135-140 day pregnant

Values represent mean ±S.E. Different capital letters mean significant differences (P≤0.05) between different age.

 

The mucosa of the rectum consist of several columnar epithelium cells with different high with distributed of few goblet cell which appeared blue in color with PAS and Alician blue which appear high affinitive with this stain and lumen of rectum star shape like in appearance with premordium of relatively short villi where the thickness of epithelium from the apex of villi to basement membrane about (18±06) µm (Table 3). The thickness of epithelium wall about 10.64±0.180 µm (Table 4) and this may show a slightly thicker epithelial layer in rectum wall compared to the colon. This may be attributed to the rectum’s role in temporary fecal storage and fecal continence. Goblet cells, which secrete mucus, was more abundant in the rectum compared to the other parts of colon (Figure 3).

 

The submucosal layer (also called mesenchymal layer) was measured to be 14.1±0.181 µm in thickness which appear consists of undifferential mesenchymal cell which gives arise to epithelium and muscularis and of contain blood vessels, lymphatics, nerves. This converts gradually to connective tissue elements (Figure 4). The differences in submucosal thickness of the rectum were minimal at this stage of development.

 

The muscularis externa of rectum was approximatelly13.54±0.189 µm (Table 4) in thickness and consists of premordium of inner circular and outer longitudinal smooth muscle fibers where inner layer was more developed than the other outer layers (Figure 5).

The tunica serosa, the outermost layer of the intestine, provides a protective covering, serosal thickness of rectum was noticed to be about 11.60±0.493 µm (Table 4). There were potentially subtle histological differences between the parts of rectum layers at this stage of fetal development, however, they were not as pronounced as in adult animals. As the fetus continues to develop, regional differences in the structure and function of the intestine may become more evident. The differences between species were due to variation in the gestation period between the different species including ovine 150 days, bovine 280 days, camel 390 days, buffaloes 330 days and human 266 days.

Rectal patch in rectum wall was not developed where few light stained mesenchymal cells which were responsible for meshwork formation around the lymphocytes. Few collagen fibers and blood capillaries were also observed (Figure 4).

Observations at second trimester of gestation (70-75) days

The body weight of sheep embryos in current stage (at 70-75 days of gestation) was about 266.6±2.088 g, gastrointestinal tract weighted about 67±1.760 gram (Table 1) and crown rump length was approximately 19.6±0.678 cm.

Morphological observations

Rectum was identified from descending colon and was noticed to be slightly larger in diameter and contain small content of feces. Located in the distal part of pelvic cavity with dark green color, it was different from the previous stage where more medio-caudally to both kidneys were noticed. It continues to descend towards the external opening of the body along with the kidney ureters (Figure 6).

 

Histological observations

We noticed that the rectal wall at this age was composed of tunica mucosa, tunica submucosa, tunica muscularis and tunica serosa (adventitia) (Figure 7). The tunica mucosa of rectum was approximately 14.4±0.156 µm and was composed of layer of epithelial cells which were simple layer and were columnar in shape with rounded or elongated nuclei slightly located near to the base of epithelial cells. This covered the tips of the intestinal villi and more toward the layer at the base of villi due to these cells undergo to differentiated but still developed. The goblet cells were distributed among the epithelial cells, taking bright blue color by PAS-Alician blue staining and an increase in number of goblet cell along the rectal villi were observed. At their base, from the other parts of large intestine due to playing critical role by secreted the mucin substance to lubricated the dehydrated feces, constituted a barrier against harmful substance and pathogen (Figure 8).

 

Rectal villi at this age were different from the rest of the large intestine and can be classified into three type depending on their height: long villi (178±93µm), middle villi (76±0.81µm) and short villi (51±0.66µm) (Table 3). The shape of villi was wider and the long type villi contained side branches, forming short villi on the sides like branched tree. The core of these villi was composed of connective tissue cells and elastic and collagen fiber of lamina propria and measurement of the thickness of this layer with about 4.3 µm size. Thin layer of smooth muscle fiber (lamina muscularis) was observed to be about 1.4 µm and slight amount of connective tissue substance of tunica submucosa gave arise to the shape of villi as long, wider with several branched on the side of rectal villi (Figure 9).

 

Lamina propria and lamina were two layers that were observed at this age of gestation by a thin demarcation line between mucosal and mesenchymal tissue layer (submucosa) (about 14.1±0.181 µm) and the cells of the last were more differentiated and taken spindle-shape near to mucosal layer or tunica muscularis to forming smooth muscle fiber (Figure 10).

 

The tunica muscularis of the rectum at this age was clearly distinct because it played an important role in excreting waste. It consisted of two layers, the inner one being circular layer with a thickness of both about 25.92±0.615µm (Table 4). The outer one being longitudinal layer that appear more developed and growth than other parts of large intestine at same layer where inner circular layer (Stratum circulare) of tunica muscularis in rectum compose of developing immature smooth muscle fibers arranged circularly around the rectum not fully distinctly yet but more development than the other layer. The outer longitudinal layer (Stratum longitudinale) which appeared at early stages of development and growth composed of mature and immature longitudinal muscle fibers but are not fully developed. They were arranged longitudinally along the length of the rectum where the differentiation of smooth muscle layers is progressing, marking the initial stages of the development of the tunica muscularis of the rectum in sheep fetuses (Figure 10).

 

Tunica serosa (adventitia) consists of irregular connective tissue made of fibroblast cells and some types of fibers such as collagen and elastic, which give elasticity and support to the rectal wall with a clear number of adipose cells, which give more thickness to this layer at this age and the measurement of the thickness of this layer was about 27.74±0.224 µm (Table 4), in addition to the presence of blood and lymphatic vessels (Figure 11).

At the starting of third trimester of gestation (100-105) days

The body weight of sheep embryos in current stage at 100-105 days of gestation was about 860.2±5.571 gram and the weight of gastrointestinal tract was about 98.6±3.31 gram (Table 1) and crown rump was measured to be 31±0.707cm.

Morphological characteristics

The rectum was straighter and larger in diameter than the rest of the large intestine. The wall of the rectum was thicker, and it course in the middle of the pelvic cavity, connected to the anal canal, which ends with the external opening of the body (Figure 12).

At the ending of third trimester (130-140) days of gestation

The body weight of sheep embryos in current stage at 135-140 days of gestation was about 1361.6±6.046-gram, gastrointestinal tract weight was about 208.4±4.69-gram (Table 1) and crown rump length was about (42.6±0.927 cm).

Morphological characterization

At this stage of gestation, rectum in sheep fetuses was beginning to take shape within the pelvic region. It was located posteriorly to the urinary bladder and anterior to the sacrum and coccyx. The rectum was a part of the lower gastrointestinal tract, connecting the colon to the anus, and it plays a crucial role in the storage and elimination of feces. As it enters the pelvis, the descending colon becomes the rectum which passes caudally as the most dorsal part of the pelvic viscera. Most of the rectum was suspended by the meso-rectum, the retroperitoneal space was full of soft tissue rich in fat.

 

Histologically on 100-105 and 130-140 days of gestation

The rectal wall consisted of four layers: tunica mucosa, tunica submucosa, tunica muscularis and adventitial layer. Tunica mucosa was clearly observed to be developed with 11.52±0.149 µm, and 16.22±0.234 µm, respectively. At both ages, it was formed of layer of epithelial cells, lamina propria and mucosa muscularis (Figure 13).

 

The layer of epithelium forming by simple, columnar epithelial cells, the nuclei of these cells be rounded and located near to the basement membrane with large number of goblet cells distributes among the epithelial layers. This can be detected histologically as being bright blue in colour with PAS-Alician blue staining technique, and its nucleus was close to the base of these cells, leaving a void at its cytoplasmic apexes filled with mucin (Figure 14).

The intestinal (rectal) villi slightly disappeared at this age of gestation due to progressive development of tunica mucosa and as a result of growth of the rectal wall, which led to increased tension of the mucosal layer and the disappearance of the villi.

At the gestational age of 100-105 days of age in sheep fetuses, the lamina propria of the rectum exhibited characteristics typical of early fetal development which were consist of loose connective tissue made by fibroblast cells, collagen and elastic fibers, which provides structural support to the overlying epithelial layer, blood vessels, including capillaries and small veins, would be present within the lamina propria. These vessels supply nutrients and oxygen to the mucosal cells and help remove waste products.

 

Intestinal glands development, the number of glands within the lamina propria may be relatively highly and these glands, which were present in the mucosa, contribute to mucous secretion and play a role in lubricating the rectal epithelium, the immune cells, such as lymphocytes and macrophages, may be scattered throughout the lamina propria and these cells help defend against pathogens and maintain immune surveillance in the mucosal tissue (Figure 15).

 

Lamina muscularis of the rectum were composed of smooth muscle fiber and located at the base of the crypt thicker layer and were very clearly observed (Figure 16). Histological examination reveals the complex organization of smooth muscle fibers within the laminar muscles. The circular muscle layer forms a continuous thick band around the inner circumference of the rectal wall, while the longitudinal muscle layer extends parallel to the length of the rectum. This arrangement allows for the coordinated contraction and relaxation of muscle fibers, enabling peristaltic movement and propulsion of feces, while lamina propria also clearly observed at this age of gestation as loose connective tissue surrounding the rectal gland and be under the epithelial cells layer and separated from tunica submucosa by lamina muscularis (Figure 16).

Tunica submucosa of rectum during third trimester (100-105 and 135-140 days of gestation) undergoes important developmental changes and this tunica was developed and rich in connective tissue components, including collagen and elastic fibres (Figure 17). The thickness of this tunica was 25.72±0.659 µm at 100-105 days and about 35.20±0.663 µm at 130-140 days of gestation (Table 4). There was continuous deposition and organization of these fibers, which contribute to the structural integrity and elasticity of the rectal wall and the blood vessels within the tunica submucosa play a crucial role in supplying nutrients and oxygen to the rectal mucosa, histological examination reveals the presence of small arteries, veins and capillaries that become more developed as pregnancy progresses, ensuring adequate perfusion of the rectal tissues also this tunica contained lymphatic vessels responsible for draining excess interstitial fluid and immune surveillance (Figure 17).

 

The tunica muscularis of the rectum in sheep fetuses during the 100-105 and 135-140 days of gestation undergoes significant development and organization, and this layer is responsible for peristaltic contractions that push fecal material through the rectum and ultimately facilitate its expulsion during birth and after birth. It consists mainly of smooth muscle fibers arranged in two layers: an inner circular layer and an outer longitudinal layer. The thickness of this tunica was about 34.60±0.481 µm at 100-105 days and about 46.88±0.628 µm at 130-140 days of gestation (Table 4) (Figure 18).

 

Serosal layer of the rectum in sheep fetuses during the third trimester of gestation (100-105 and 135-145 days) with a thickness of about29.24±0.348 µm, 38.58±0.506 µm, respectively (Table 4). These features reveal several main features including the mesothelial cells primarily of a single layer of mesothelial cells be flattened in shape and specialized to produce a lubricating fluid that helps reduce friction between the rectum and surrounding structures within the peritoneal cavity also underneath the layer of mesothelial cells is a layer of loose connective tissue comprised by fibroblast cells, collagen and elastin fibers also large number of adipose cells be observed, small aggregation of lymphatic tissue and blood vessels all that are provided structural support for the serosa and helps anchor it to the underlying layers of the rectal wall (Figure 19).

 

The rectum at this age is a transparent and white-walled tube located at the lower portion of the pelvic cavity. The visual diameter of the rectum is slightly larger than the descending part of the colon. It contains very small amounts of feces, and its green color appearance as a result of the transparency of the rectal wall. It consists of a single cavity and is not divided into two parts (thin and sacculation), as is the case in camel embryos at same age. This study differs from Bello et al. (2015) who have described that the rectum is composed of two parts (thin and sacculation parts) in camel embryos at same age. The rectum would be undergoing development along with the rest of the intestinal tract and the histological structure would be similar to that of other parts of the large intestine and more development including on several layers from inner to outer: mucosa, undeferential mesenchymal tissue, muscularis externa, and serosa or (adventitia).The pervious study agreement with Bello et al. (2015) in camel fetuses at first stage of development which described the rectum like the other parts of intestinal tract forming from four general tunicae and consist of four layers namely: tunica mucosa, tunica submucosa (mesenchymal tissue), tunica muscularis and tunica serosa.

The mucosa of rectum lining by several layer of columnar epithelial cells with goblet cells distributed among them with short villi projected into the lumen. These results are compatible with Ram et al. (2022) in camel and in bovine. They have noticed that the goblet cell appears cleared at this stage of development.

The tunica muscularis forming by inner circular and outer longitudinal smooth muscle fiber and the outer layer was developed which was in agreement with Singh et al. (2012) who have noticed that the muscularis externa was developed at this stage of gestation from the other portion of large intestine in buffalo fetuses. Rectal patch in rectum wall was not development and this result disagree with the observation made by Indu et al. (2018) in goat fetuses. They also observed that the rectal patch was appearing at 60 days of gestation as continuous band small to medium-size lymphocyte in lamina propria. Few light-stained mesenchymal cells formed meshwork around the lymphocytes.

The location of rectum at second age was aligned to the observations made by Sadler (2006) which described hindgut portion entering posterio-caudally region of the cloaca (future anorectal canal), and the allantois enters the anterior region (future urogenital sinus). Breakdown of the cloacal membrane covering this area provides communication to the exterior for the anus and urogenital sinus.

At the same age, the mucosa of rectum lining by simple layer of columnar epithelial cells increased goblet cells appearance at this layer this observation was contradictive to Joubert (1956) who showed the goblet cells may not be observable at any age along the course of gestation in horse fetuses. Bello et al. (2015) have mentioned that the goblet cells be increased with advanced age and be more numerous in the rectum in the fetuses of goat.

Rectal villi appeared in different lengths projected into the rectal lumen and have several lateral branches as was observed. They have described that the villi developed at same age of gestation in bovine fetuses and showed the villi in rectum were shorter in length. Lamina propria and lamina muscularis were observed at this age of gestation by a thin demarcation line between mucosal and mesenchymal tissue layer (submucosa). These results are in agreement with observations made by Esrefoglu and Cetin (2017). They have mentioned that the musculature mucosa stays in differential progressive and be more developed after mid stage of gestation in mammals’ fetuses.

The serosal layer of the rectum several key features, including a single layer of mesothelial cells that are primarily flattened in shape and specialized to produce a lubricating fluid that helps reduce friction between the rectum and surrounding structures within the peritoneal cavity. Additionally, a layer of loose connective tissue beneath the layer of mesothelial cells is comprised of fibroblast cells, collagen, and elastin fibers. A large number of adipose cells can be observed, as well as a small aggregation of lymphatic tissue and blood vessels, all of which provide structural support for the serosa and help anchor it to the beneath. These results align with the observation of Franco et al. (2017) where they have described the structural components of serosal layer of abomasum in deer and sheep fetuses and mentioned the serosal layer formed by flatted mesothelial cells and high cellular connective tissue elements.

Conclusions and Recommendations

All gross biometrical parameters of rectum at prenatal development (length, width and thickness) increased with the advanced age of the fetus and there was significant variation in the gross biometry. The rectal wall was comprised of four layers: Epithelium, pluripotential blastemic tissue, premordium tunica muscularis and serosa (adventitia) in the first trimester and at the second and third trimester of gestation the rectum comprised four-layer: epithelium, submucosa, tunica muscularis and serosa. The epithelial layer of rectum be stratified columnar epithelium with goblet cells distributed in different part of this layer and increased also be more density by age of the rectum progressed. Therefore, the epithelial stratified layer transformed to simple layer of columnar epithelial cells. Rectal villi appeared as small elevation of mucosal layer into rectal lumen at first trimester and then exhibited several villi with different length at second trimester. These finding advanced several aspects of the rectum development and offer several markers to be considered during effective assess of animal health and production potential.

Novelty Statement

Present report and finding can advanced several aspects of the rectum development and offer several markers to be considered during effective assess of animal health and production potential.

Author’s Contribution

Ali Mobder Niyf and Jafar Ghazi Abbas Al-Jebori confirm contribution to the paper equally.

Funding

No funding was received.

Availability of data and materials

The datasets used and/or analyzed during the current study are available from the corresponding author on reasonable request.

Patient consent for publication

Not applicable.

Ethics approval and consent to participate

The experimental procedures were approved by the Institutional Animal Ethics Committee and conducted at Veterinary Medicine Collage, Al-Qasim Green University, Iraq. Ethical regulation of the present work was assinged by university research comitte and guidelines of American Veterinary Medical Association (https://www.avma.org/resources-tools/animal-health-and-welfare/animal-welfare).

Conflict of interest

The authors have declared no conflict of interest.

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