Arteriolar, capillary, and shunt flow gradients along the intestine in relation to the weight distribution of the mucosa, submucosa, and muscularis—a microsphere study

Abstract

The objective of this study was to establish the basal arteriolar (ART), capillary (CAP), and shunt (SH) flow of the three anatomical layers of the gut wall (mucosa, submucosa, and muscularis) along the intestinal tract of the dog employing a microsphere technique. We also examined whether a gradient of blood flow (BF) exists along the intestine, and if so, how this is related to the blood flow and weight distribution of the three anatomical layers along the intestine. We found the following. (i) In all locations of the intestine a higher proportion of the ART inflow passed through the capillaries of the layers with higher metabolic need, i.e., mucosa (68-79%) and the muscularis (50-79%), than through the capillaries of the submucosa (34-46%). Thus, the distribution between CAP and SH flow in the three anatomic layers of the gut wall, as measured by the microsphere technique, appears to correspond to the functional requirements of these tissue layers. (ii) From the duodenum to the ascending colon (but not along the colon), there was a significant decreasing gradient of ART flow (R2 = 50.6%) and a small and barely significant gradient of CAP (R2 = 11.6%) and SH flow (R2 = 9.7%) of the whole gut wall. (iii) All these gradients were present in the mucosa, but their slopes were higher than those in the whole gut wall; the R2 for the mucosal ART, CAP, and the SH flow was 60.5, 52.7, and 21.6%, respectively. (iv) The ART, CAP, or the SH flow of the submucosa and the muscularis showed no such decreasing gradient. Thus, the gradient of blood flow of the whole gut wall appears to be a reflection of a more prominent gradient of ART and CAP flow of the mucosa. (v) Similar to the mucosal blood flow, the weight distribution of the mucosa showed a craniocaudal gradient (R2 = 69.3%). The latter was found to be directly related to the mucosal blood flow of all locations from the duodenum to the ascending colon, except for the duodenum, which had a higher ART and SH flow than those of several, but not all, distal locations. This higher blood flow of the duodenum could be due to a functional difference of this location.

Enteral Feeding Reduces Endothelial Nitric Oxide Synthase in the Caudal Intestinal Microvasculature of Preterm Piglets

“…Based on our data, we suggest that blood flow gradients along the small intestine are related to the cranial-to-caudal decreasing gradients in mucosal vWF and/or eNOS, an endothelial enzyme responsible for the production of the main vasodilator NO in neonatal and premature animals (5,7,9). Furthermore, this blood flow gradient was prominent in the mucosal layer only (11), which is in agreement with the absence of an eNOS-or vWF gradient in the submucosal and muscle layer.…”

“…This is supported by the observed negative correlation between mucosal vWF density and surface density, although we cannot exclude the presence of wider capillaries in the caudal small intestine. A cranial-to-caudal decrease in intestinal blood flow has been reported in dogs (11), pigs (12,13), and humans (14). Based on our data, we suggest that blood flow gradients along the small intestine are related to the cranial-to-caudal decreasing gradients in mucosal vWF and/or eNOS, an endothelial enzyme responsible for the production of the main vasodilator NO in neonatal and premature animals (5,7,9).…”

“…Although eNOS is constitutively expressed in the endothelium, both eNOS mRNA and protein expression can be modulated (10), including by nutrient intake (7). Furthermore, intestinal blood flow shows a cranial-tocaudal decrease along the small intestine in neonatal and adult dogs (11), pigs (12,13), and humans (14). It is, however, unknown whether this functional gradient in the small intestine is associated with a similar gradient in microvessel distribution and/or eNOS protein expression.…”

Evolution of a detailed physiological model to simulate the gastrointestinal transit and absorption process in humans, Part 1: Oral solutions

“…The mucosa is composed of a simple columnar epithelium, which is in direct contact with the luminal contents, an underlying lamina propria (a connective tissue containing many blood and lymphatic vessels) and a thin layer of smooth muscle fibres (muscularis mucosae). Because of the high metabolic requirements of the mucosa, most of the arteriolar blood perfusing the intestine is distributed to this layer 31–34…”

Gastric digestion of protein through pancreozyme action optimizes intestinal forms for absorption, mucin formation and villus integrity

“…Total mesenteric arterial flow is dominated in use by the mucosa and submucosa vessels in a manner that decreases from duodenum to ileum to accommodate overall reduction of digestive intensity and villi dimension as nutrients absorbed from the lumen dissipate. In a converse manner, returning blood within the portal system is low distally and increases toward the duodenum in order to accommodate the progressive amounts of absorbed nutrients to the liver (Mailman, 1982;Shepard, 1982;Dinda and Beck, 1986). Overall control of blood flow within the small intestinal system revolves around the array of gastrointestinal hormones, extent of motility, and neural integration (Fondacaro, 1984;Premen et al, 1985;Holzer, 2006).…”