PRACA ORYGINALNA

ORIGINAL ARTICLE

FEATURES OF ANGIOARCHITECTURE OF THE ALBINO RATS STOMACH AND SMALL INTESTINE

CHARAKTERYSTKA UNACZYNIENIA ŻOŁĄDKA I JELITA CIENKIEGO U SZCZURÓW ALBINOSÓW

Volodymyr H. Hryn, Yuriy P. Kostylenko, Valentyna P. Bilash, Yana A. Tarasenko

Ukrainian Medical Stomatological Academy, Poltava, Ukraine

ABSTRACT

Introduction: The stomach and small intestine are important organs of the digestive system and, to date, they are the subject of research by morphologists, endocrinologists, immunologists, gastroenterologists, and other researchers.

The aim: The paper is aimed at the study and systematization of the features of angioarchitecture of the albino rats stomach and small intestine.

Materials and methods: The study based on the injection of the blood vasculature of abdominal organs of 20 albino male rats with 5% gelatin solution, colored with filtered black ink, was performed. The specimens were subject to photographing from different aspect angles in their original state, and then, after dehydration in alcohols with the transition to pure acetone, they were embedded in the epoxy. Photographing of the obtained specimens was made by a digital camera, as well as a binocular magnifier MBS-9, equipped with a digital photoattachment Sigeta DCM-900 9.0MP.

Results and conclusions: The results of injecting of blood vasculature of albino rats’ gastrointestinal tract with ink mass clearly demonstrate the specific difference in the intraorganic angioarchitecture of its different regions, which depends entirely on their functional purpose in the digestive process. In the stomach, the highest concentration of blood microvessels is in its glandular part, which is explained by the increased nutrient needs of the secretory process of the gastric glands, while the mucous membrane of its fundus (pre-stomach) contains a scattered network of exchange microvessels that only promote the process of regeneration of the stratified squamous (partially keratinized) covering epithelium.

In the small intestine, the typical principle of the organization of the microvasculature of its mucous membrane is somewhat modified in the duodenum, which is associated with the presence of mucous (Brunner’s) glands in it, as well as in those sites (starting from the duodenum) where the group lymph nodes (Peyer’s patches) are localized.

KEY WORDS: stomach, small intestine, angioarchitecture, albino rats

Wiad Lek 2019, 72, 3, 311-317

INTRODUCTION

The data on the anatomical and physiological features of the gastrointestinal tract of albino rats are reported in the publications of many authors who are engaged in experimental modeling of the pathological states of the digestive system [1, 2]. According to the publications, generally, the digestive tract of humans and the laboratory animals have more similarities than differences. The latter include the absence of tonsils and the appendix in albino rats, though they have a relatively more developed cecal part of the large intestine, which is extremely extensive compared to the human one [3, 4, 5, 6, 7, 8, 9, 10, 11 ].

However, all the data available in the literature on the morphological features of the gastrointestinal tract of albino rats cannot be considered sufficient, as the authors underestimate issues related to the peculiarities of its vascularization, and the available scarce data are not systematized, which determined the purpose of our studies.

THE AIM

The paper was aimed at the study and systematization of the features of the angioarchitecture of the albino rats stomach and small intestine.

MATERIALS AND METHODS

The study based on the injection of the blood vasculature of abdominal organs of 20 albino male rats with 5% gelatin solution, colored with filtered black ink, was performed in the mode of maintaining the temperature of the solution in the range of 37-40°C. Euthanasia of rats was made under thiopentone anesthesia overdose (75 mg / kg animal body weight intramuscularly in the upper third of the hip of the hind paw) [12, 13].

Before the experiment, all animals were kept in standard conditions of the experimental biological clinic (vivarium) at the Ukrainian Medical Stomatological Academy in compliance to the regulations on keeping experimental animals adopted by the European Parliament and Council Directive (2010/63 / EU), the Order of the Ministry of Education and Science, Youth and Sports of Ukraine as of 01.03.2012, No. 249 “On approval of the procedure for conducting tests, experiments on animals by research institutions” and “General ethical principles of experiments on animals”, adopted by the V National Congress on Bioethics (Kiev, 2013) (Minutes No. 155 as of 26.04.2017 of meeting the Commission on Biomedical Ethics at Ukrainian Medical Stomatological Academy) [14, 15, 16].

Positive results were obtained only after preliminary washing of the entire blood vasculature with warm saline solution (with the addition of heparin injection solution of 5000 IU / ml) through the cannulated distal abdominal aorta with the intersection of the common iliac vein, through which outflow of the displaced blood occurred until a colorless liquid appeared. Only after this procedure, the vessels were filled with a gelatinous mass through the same cannula until it outflowed from the iliac vein. Immediately after that, in order to prevent the injection mass from leaking out, a ligature was applied on the distal aorta and caudal vena cava, after which the animal’s corpse was embedded first into cold water and then fixed in 10% formalin solution for two days [17].

Subsequently, after washing in running water, the whole complex of internal organs was removed from the abdominal cavity of the animal and partitioned into sections, with the selection of those that corresponded to the objectives of the study. Initially, they were photographed from different aspect angles in their original state, and then, after dehydration in alcohols with the transition to pure acetone, they were embedded in epoxy resin [18, 19, 20], facilitating the clearing of tissues and more expressive contrasting of injected blood vessels against their background. Photographing of the obtained specimens was made by a digital camera, as well as a binocular magnifier MBS-9, equipped with a digital photoattachment Sigeta DCM-900 9.0MP.

RESULTS

Out of all organs of the gastrointestinal tract of albino rats, the stomach is distinguished by the pronounced specificity of angioarchitecture, although, according to the general principle of the distribution of vessels, delivering the arterial and outflowing the venous blood, it is similar to the human stomach, which is supplied with blood ( if not taking into account the short fundal arteries) with two pairs of branches (mainly) of the celiac trunk, of which one pair of oppositely directed arteries mutually anastomose along the small curvature, and the other pair along the large curvature. Thus, these longitudinal, oppositely located arterial arches mutually anastomose along the two external surfaces of the stomach through the encircling branches. At the same time, these inter-arterial anastomoses are accompanied by corresponding venous vessels, from which blood flows into the portal vein. In contrast, our findings show, that the stomach of albino rats is supplied with blood only by one arterial arch from its small curvature, from which the encircling branches are fan-shaped bifurcated, anastomosing mutually along the large curvature (Fig. 1). But the most remarkable feature of angioarchitecture of the albino rats stomach is the intramural (intraparietal) distribution of blood vessels, which are generally organized in stratification in the form of three networks, one of which, occupying an intermediate position in the submucosa, plays the role of blood distribution between two other blood networks. At the same time, one of them is represented by the microvasculature of the muscular layer, and the other belongs to the mucous membrane. Obviously, both of them are represented by a complex association of resistive (arterial), exchange (capillary) and capacitive (venous) microvessels, which are organized depending on the nature of tissue structures according to a modular principle, which implies the presence of bypass (preferred) blood flow in the microvascular modules [ 21, 22]. Due to the fact that the muscle membrane is more uniform in structural organization in the stomach wall, when filling its microvasculature, we get a homogeneous total density of its coloring on macropreparations, while the density of the injection mass in the blood vasculature of the mucous membrane is different depending on corresponding three sections of the stomach of albino rats (Fig. 2). These preparations clearly demonstrate that the greatest intensity of the total coloring of the injected blood vessels is shown in the middle part of the stomach wall, which belongs to its gastric region. It is quite obvious that it entirely depends on the dense concentration of the gastric glands in its mucous membrane, which require a more abundant network of exchange microvessels for their secretory activity. Compared to this, the two other regions of the stomach (pyloric and fundal) markedly show less density of injection coloring, and the fundus or the pre-stomach is the lightest.

This differentiation on the density of the injection mass in the stomach blood vasculature of the albino rats becomes more pronounced when the preparations are embedded into epoxy resin. Figure 3 shows two images of one half of the stomach, one of which (upper) shows its inside view, and the other (lower) shows it from the outside. It is noteworthy that its gastric (glandular) region is separated from the other two (pyloric and fundal regions) by two intensely colored transverse stripes, which are interconnected by strands of similar color intensity, the increased coloring density of which is caused by the folding of the mucous membrane.

Thus, on the basis of the above results of filling the blood vasculature of albino rats stomach with coloring mass, it can be concluded that, consequently, the highest activity of the metabolic processes is noted in its glandular region, and the lowest is in the mucous membrane of the fundal region, in which the scarce network of exchange microvessels provides only the process of regeneration of the stratified squamous epithelium.

More uniform and stereotypically organized angioarchitecture is characteristic of the small intestine, which is due to the ordered cluster principle of distribution in their mucous membrane of uniform structures, which are the intestinal villi and crypts. In their common blood vasculature, marked superficial vessels are noted that carry out blood delivery and distribution throughout the intestinal tube, and intramural networks, represented mainly by microvascular communications of the muscular and mucous membranes. Apparently, the superficial blood vasculature of the small intestine originated mainly from the branches of the superior mesenteric artery that are paired with the corresponding inflows of the portal vein, which arc-anastomosing in the mesentery. In albino rats, similar to humans, these paired arcade chains are located along the line of attachment to the small intestine mesentery loops, from which, on a regular basis, along the whole length of the small intestine, the branches of the small intestine are divided into two surrounding ones, directed toward each other on the perimeter of the intestinal tube. The latter, meeting on the line opposite to the site of attachment to the small intestine mesentery, anastomose mutually. Considering this form of segmental loopback of blood delivery vessels (arteries) and its outflow (veins) in the small intestine, during preparation we dissect its individual segments along the mesentery line, after which they were spread out between two slide plates. Figure 4 shows the preparations of the duodenum, as well as the rest of the small intestine in the intermediate zone between Peyer’s patches and in the site of localization of the latter. It is noteworthy that the most rigorous segmental order of distribution of encircling (circular) blood vessels is noted in the wall of the small intestine in its intermediate zones between the Peyer’s patches, which is explained by the uniform nature of its structural organization. The above image clearly shows that the encircling arteries, accompanied by the venous vessels, having an opposite direction, gradually become thinner as a result of stepped branching, and their terminal branches in the zone opposite to the mesentery attachment site form extensive cross-anastomoses, which are seen more clearly after preparations embedment into the epoxy resin (Fig. 5). This image shows the extensive microvascular communications against the background of intestinal villi, which are formed by anastomoses between the arterial and venous vessels separately, among which the bypass blood flow pathways in the form of arteriole-venous anastomoses are found. This example shows the most typical picture of the formation of a common network of the blood vasculature of the mucous membrane over the entire surface of the small intestine, to which blood is supplied by multiple, segmentary alternating along its entire length encircling arteries, which are accompanied by the venous vessels. It should be noted that at the level of the formation of the blood microvasculature between the arterial and venous vessels disintegration occurs.

This strictly ordered principle of the organization of the blood vasculature of the small intestine is somewhat disturbed in the duodenal wall and in those sites of the small intestine where Peyer’s plaques are located. Figure 4A shows that in the duodenal wall the encircling arteries paired with the corresponding veins do not have strict segmental regularity in their distribution along the length of the intestinal tube. In addition, more significantly, they give out more branches, which, in turn, form denser microvascular networks compared to the rest of the small intestine. This is due to the fact that, as we established, in the wall of the duodenum between the mucous and muscular membranes the acini of the mucous (Brunner’s) glands are located.

As for those parts of the rest of the small intestine where Peyer’s patches are located, their common angioarchitecture is subject to variability due to the inclusion of microvascular associations into the common blood vasculature, ensuring the trophism of these lymphoid masses.

DISCUSSION

The stomach and small intestine are important organs of the digestive system, and to date, they are the subject of research by morphologists, endocrinologists, immunologists, gastroenterologists, and other researchers. Publications report about the two-cavity stomach in all rodents, unlike in human one. In rats, regardless of a mixed diet, though containing a large proportion of grain and solid foods, such division of the stomach into two regions is preserved. Consequently, the esophageal region or pre-stomach is distinguished as well as the rest of the major part, which is essentially comparable to the human stomach. These two regions are partially separated by a well-pronounced ridge. It is believed that the pre-stomach is intended mainly for bacterial digestion, whereas the rest of region performs an enzymatic digestion of foodstuff [1, 2, 23, 24, 25].

The small intestine is the longest part of the digestive tract, intended to perform the major functions in the process of the consumption of nutrients by the body, which are mainly products of enzymatic hydrolysis of proteins, fats and polysaccharides. The final phase of this process is the absorption of these nutrients into the internal environment of the body. The conveyor nature of digestion in the small intestine is generally expressed in the well-known anatomical distinguishing of such parts as the duodenum, jejunum and ileum, the length of which in a human is approximately (separately) is 30 cm – 2 m – 3 m, respectively. Evidently, the length of the rat small intestine is much smaller. However, the data reported in the literature are questionable. Thus, according to them, the length of the rat duodenum is comparable to that of a human one, and the rest of its small intestine is approximately equal to 1 meter. Consequently, the entire rat small intestine is only by 4-5 times shorter than that of a human one. Obviously, in a limited volume of the rat abdomen of such a length, the digestive tube can fit if it is sufficiently thin [23]. Unfortunately, no data on its thickness have been found in the literature to date. It is known, the transverse size of the human small intestine varies in length from 2 to 3 cm [2, 10].

Publications report [9, 24, 26] that the thickness of the gastric mucosa varies from 2-3 mm, dependent on its functional state. Its connective tissue lamina propria is covered with a simple high (columnar) secretory epithelium. Therefore, the entire epithelial layer of the gastric mucosa can normally be considered as a continuous glandular field, producing mucous secretion, with its thin layer covers the entire surface. This layer of mucus forms a protective barrier for the mucous membrane from the devastating effects of hydrochloric acid and pepsin.

The deepest layer of the gastric mucosa, bordering the submucosal layer, is myoplasty, consisting of bundles of smooth muscle cells located in all directions in the plane of the mucous membrane. Throughout its length, separate bundles are split off, which, penetrating the thickness of the mucous membrane, pass between the glands, ending in the basal membrane of their excretory ducts and covering epithelium. Due to the contractile activity of these smooth muscle structures, adaptive dynamic plasticity (change in thickness and shape) of the mucosa itself is carried out, as well as the enhanced secretion of the glands through the excretory ducts. Consequently, the gastric mucosa has its autonomous contractile system.

The mucous membrane of the human small intestine, preserving its general principle of the structure, has not only its own distinctive features, but also differs in certain morphological features in its various parts. A common anatomical feature for it is the presence of numerous transverse-ring folds throughout it, due to the loose submucosa and smooth muscle tone. But their number and degree of manifestation gradually decreases towards the distal part of the ileum. In the duodenum, the folding of the mucous membrane is somewhat different in that from the side of the medial wall of its descending part where a permanent longitudinal fold is located, which inferiorly becomes higher and ends with a large papilla. It opens with one common hole of the bile duct and pancreatic duct. A little superiorly, the second papilla of a smaller size is located, on which the accessory pancreatic duct opens.

The mucous membrane of the small intestine, in the straightened state, is distinguished by a dull, velvety appearance, due to the numerous tiny (about 1 mm long) finger- or foliate processes called the intestinal villi. [27].

The mucous membrane of the small intestine has a greatly developed local representation of the immune system in the form of intestinal lymphoepithelial clusters called lymphoid nodules. Mostly they are in the form of single nodules and their group clusters [28, 29].

The knowledge on the blood supply of the organs of abdominal cavity is crucial in the study of its state [30, 31, 32].

The features of the morphofunctional structure, the rheological properties of the blood, changes in the microvasculature in the vessels provide a comprehensive description of the effect of the chemical agent on the organ or system. The vascular bed is an important functional system that responds to various negative effects, both by the general reaction of its constituent structural components, and by the changes in the properties of the blood. This is explained by the fact that the vessels of the microvasculature are the first to be affected by the pathogenic agents and are the first to ensure the response of the organ or tissue to external influence [33].

The small intestine contains numerous vessels that form a large blood microvascular field, which is very sensitive to intoxication. It is also known that the endothelium, lining the blood capillaries of various organs, has its own characteristics, due to the specificity of the functioning of these organs. However, under the influence of various factors, the type of endothelium can locally change, which reflects a high level of adaptation processes [34].

CONCLUSIONS

The results of injecting of blood vasculature of albino rats gastrointestinal tract with ink mass clearly demonstrate the specific difference in the intraorganic angioarchitecture of its different regions, which depends entirely on their functional purpose in the digestive process.

In the stomach, the highest concentration of blood microvessels is in its glandular part, which is explained by the increased nutrient needs of the secretory process of the gastric glands, while the mucous membrane of its fundus (pre-stomach) contains a scattered network of exchange microvessels that only provides for the process of regeneration of the stratified squamous (partially keratinized) covering epithelium.

In the small intestine, the typical principle of the organization of the microvasculature of its mucous membrane is somewhat modified in the duodenum, which is associated with the presence of mucous (Brunner’s) glands in it, as well as in those sites (starting from the duodenum) where the group lymph nodes (Peyer’s patches) are localized. The latter, which are of primary interest in our research, will be discussed in detail in our subsequent publications.

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The paper has been written within the research scientific work, carried out at the Department of Human Anatomy of the Ukrainian Medical Stomatological Academy, entitled “Age-related aspects of the structural organization of the organs of the human immune system, glands of gastrointestinal and urogenital system in normal condition and pathology”; State registration number 0116U004192.

Authors’ contributions:

According to the order of the Authorship.

Conflict of interest:

The Authors declare no conflict of interest.

CORRESPONDING AUTHOR

Volodymyr Hryn

Department of Human Anatomy,

Ukrainian Medical Stomatological Academy

23 Shevchenko str., 36011 Poltava, Ukraine

tel.: +380(66)8126497

e-mail: vogrin034@gmail.com

Received: 15.11.2018

Accepted: 22.02.2019

Figire 1. The outer surface of the albino rat stomach after injection of blood vessels with ink and gelatin.

1 – the fundus (pre-stomach); 2 – gastric (glandular) region; 3 – pyloric region; 4 – pyloric sphincter; 5 – small curvature of the stomach; 6 – large curvature of the stomach; 7 – encircling blood vessels.

Figure 2. The inner surface of the albino rat stomach after injection of blood vessels with ink and gelatin.

1 – the fundus (pre-stomach); 2 – gastric (glandular) region; 3 – pyloric region; 4 – pyloric sphincter; 5 – folds of mucous membrane.

B

Figure 3. The albino rat stomach after injection of blood vessels with ink and gelatin, subsequently embedded into epoxy resin. А – inner surface; B – outer surface.

1 – the fundus (pre-stomach); 2 – gastric (glandular) region; 3 – pyloric region; 4 – pyloric sphincter; 5 – folds of mucous membrane.

Figure 4. Preparations of different parts of albino rat small intestine. А – duodenum; B – part of the small intestine between the Peyer’s patches; C – zone of localization of the Peyer’s patches.

1 – segmentary encircling blood vessels; 2 – vessels ensured blood supply to Peyer’s patch.

Figure 5. Blood vasculature of the small intestine in the intermediate zone between the Peyer’s patches.

1 – arterial and venous, segmentary encircling vessels; 2 – their branches and anastomoses between them; 3 – intestinal villi.

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