Trans-Serosal Multimodal Optical Coherence Tomography for Visualization of Microstructure and Blood Circulation of the Small Intestine Wall

Abstract

The aim of the study was to evaluate the performance of trans-serosal multimodal OCT (MM OCT) in in vivo detecting of changes in microstructure and blood circulation of the small intestine wall caused by arteriovenous ischemia resulted from intestine strangulation. Materials and Methods. In experiments on Wistar rats (n=22), we examined the small intestine wall in vivo using MM OCT; the access to the intestine was reached through laparotomy. The microvasculature and microstructure of the wall were studied before and after acute arteriovenous ischemia created by ligation of a small bowel segment. The results were then added with data obtained from histological and intravital microscopic examination. Results. Trans-serous MM OCT allowed us to visualize the bowel wall to its entire thickness, distinguish between the serous-muscular and mucous-submucosal layers, and detect the villi and functioning blood vessels. The structures were best seen after a fat emulsion had been administered into the bowel lumen. In OCT images made in the optical coherent angiography (OCA) mode, large paired vessels (arteries and veins) and micro-vessels with a diameter of >15 μm could be seen. Most of the blood vessels were imaged in the depth range of 80-300 μm from the surface. Capillaries with a diameter of 7-10 μm were not seen, but they produced an overall bright background. In the OCA images reconstructed from a volume of 2.4×2.4×1.8 mm, the total length of the vascular bed before ischemia was 18.3 [16.6; 19.8] mm. Strangulation of the intestinal loop was associated with changes in the CP OCT picture: the villi-associated vertical pattern and shadows of blood vessels disappeared and the depth of tissue visualization in the cross-channel decreased. The optical equivalents of the serous-muscular layer were preserved; after 180±12 min of ischemia, their proportion in the intestinal wall thickness increased from 25 [18; 32] to 42 [31; 55]% (p=0.031). At that time-point, OCA images of the strangulated bowel loop looked all similar: a uniform dark background with isolated fragmentary large vessels and no signs of blood flow in the microvascular network. Conclusion. Trans-serous MM OCT provides for in vivo visualization of microstructures critical for surgical gastroenterology: the intestinal wall layers including villi and blood vessels of each layer, as confirmed by histological analysis. Destructive processes in the intestinal wall resulting from bowel ligation bring about optical changes, which can be detected using real-time MM OCT.

Prospects of Intraoperative Multimodal OCT Application in Patients with Acute Mesenteric Ischemia

“…During surgery, LDF, FI, SDF, IDF, LSCI, HIS, and OCTA can be helpful to determine the intestine viability and clarify the exact border of bowel resection [ 43 , 44 , 45 , 69 ]. LDF, FI, SDF, IDF, LSCI, HIS techniques obtain information about perfusion/blood flow and only OCTA assesses bowel microvessels and microstructure simultaneously [ 49 ].…”

“…Our experience of experimental and clinical research has shown that the data obtained on the AMI model in laboratory animals could only partially be extrapolated to clinical diagnosis in patients. OCTA of the small intestine of patients has shown both similarities and differences from the data obtained in experiment on laboratory animals (rats, miniature pigs) [ 49 , 59 ]. Apparently, the differences in the OCTA picture of the small intestine (both in the norm and in ischemia) between laboratory animals and humans are due to the anatomical and physiological parameters of the vascular system of the small intestine, namely, the thickness and optical density of the serous membrane, the depth of the location of large vessels, their diameter and the blood flow rate.…”

“…Apparently, the differences in the OCTA picture of the small intestine (both in the norm and in ischemia) between laboratory animals and humans are due to the anatomical and physiological parameters of the vascular system of the small intestine, namely, the thickness and optical density of the serous membrane, the depth of the location of large vessels, their diameter and the blood flow rate. In an experiment on animals [ 49 ], we have previously identified diagnostically significant criteria for the preservation of intramural intestinal blood flow: 1—the presence of large “treelike”, often paired, vessels with a diameter of 50–200 μm; 2—a uniformly light background to the OCTA image, the presence of which depends on the functioning of the arterioles, venules, and capillaries of the submucosa and mucosa. In the OCTA images of an ischemic but viable human intestine, these criteria were met in no more than 70% of observations.…”

“…Thus, it is a promising tool for the complex assessment of the intestinal wall damage caused by AMI. The experience of experimental and clinical application of OCT in gastroenterology indicates the possibility of the label-free imaging of the gut wall stratification with the resolution of 25 microns or less to the depth of 2 mm [ 47 , 48 , 49 ]. In the overwhelming majority of clinical studies using OCT, the gastrointestinal tract visualization has been carried out by endoscopic access, which has facilitated the assessment of mucous membranes of esophagus [ 50 ], stomach [ 51 ], and the initial part of small intestine and colon [ 52 , 53 ].…”

“…An OCT picture of ischemic damage to the wall of the small intestine in humans with AMI has not been previously obtained or assessed. We set out to test whether multimodal (MM) OCT, which has proven its effectiveness in studies of AMI models in laboratory animals [ 49 , 59 ], is effective here. This would enable us to obtain objective data on the state of the human intestinal wall with AMI in a clinical situation.…”