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Vascular Anatomy Defines Sites of Indomethacin Induced Jejunal Ulceration Along the Mesenteric Margin

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Vascular Anatomy Defines Sites of Indomethacin Induced Jejunal Ulceration Along the Mesenteric Margin Gut 1997; 41: 763–770 763 Vascular anatomy defines sites of indomethacin induced jejunal ulceration along the mesenteric Gut: first published as 10.1136/gut.41.6.763 on 1 December 1997. Downloaded from margin A Anthony, R E Pounder, A P Dhillon, A J Wakefield Abstract margin of the jejunum2–6 and more specifically, Background—Indomethacin induces ul- at sites supplied by short feeding vessels (vasa ceration in the rat jejunum with sparing of brevia, VB) located between the long feeding the ileum. The ulcers localise between vessels (vasa recta, VR).3 It is of interest that in vasa recta along the mesenteric margin of Crohn’s disease small intestinal ulcers also the bowel, observations that have not been tend to arise along the mesenteric margin fully explained. where blood vessels pass through the muscula- Aim—To examine the relationship be- ris propria, an acknowledged, but largely tween the localisation of experimental ignored observation.7 ulcers and the vascular anatomy of the rat Early anatomical studies of the human small intestine. gastrointestinal tract identified the existence of Methods—The normal vascular anatomy long (VR) and short (VB) feeding vessels that of the rat jejunum and ileum was studied supplied the antimesenteric and mesenteric and compared using arterial carbon ink margins of the bowel wall respectively.89While perfusion. The anatomical localisation of the mesenteric margin is known to be preferen- early and advanced lesions induced by tially ulcerated in the indomethacin/rat model indomethacin was examined with particu- this predilection still lacks an explanation. lar reference to the vasculature. Mucosal In this paper we have compared the normal injury induced by feeding vessel ligation vascular anatomy of the rat jejunum with the for 24 hours or brief ischaemia- ileum (sensitive and resistant sites of in- reperfusion injury was examined. The domethacin induced ulceration respectively) existence of anatomically sensitive sites to and examined the anatomical relationship indomethacin was tested in a two dose between the localisation of lesions and the vas- study. cular anatomy. We also tested the hypothesis Results—In the rat jejunum, poorly vascu- that the predilection for such lesions to arise at http://gut.bmj.com/ larised sites along the mesenteric margin anatomically susceptible sites is explained by were highly susceptible to indomethacin the existence of critically perfused areas in the induced injury, such sites being absent bowel wall which would be more prone to from the ileum. Villous contraction was a ischaemic injury. feature of both early indomethacin injury and ischaemia-reperfusion injury in the Materials and Methods rat jejunum. Twenty four hour ligation of MATERIALS on September 28, 2021 by guest. Protected copyright. jejunal vasa brevia selectively induced Male Sprague-Dawley rats (240–270 g) were ischaemic injury along the mesenteric kept under standard laboratory conditions and margin. Two doses of indomethacin to rats had free access to food at all times. Indometh- did not induce greater injury than a single acin was purchased from the Sigma Chemical dose. Company (St Louis, Missouri, USA) and black University Conclusions—Results support the hypoth- carbon ink from Pelikan (Hanover, Germany). Department of esis that the rat jejunum possesses vascu- Histopathology, Royal Experiments were performed under a project Free Hospital School larly compromised sites along the licence approved by the Home OYce (UK). of Medicine, London, mesenteric margin that are susceptible to UK indomethacin induced injury. Indometh- A Anthony acin may cause ischaemia-reperfusion METHODS A P Dhillon injury selectively at these sites. Vascular anatomy of the normal rat small A J Wakefield (Gut 1997; 41: 763–770) intestine After terminal anaesthesia (2% halothane and University Keywords: indomethacin; blood supply; small intestine; fentanyl 0.15 mg/kg intraperitoneally) rats un- Department of ulcers; rat; vascular anatomy; ischaemia derwent midline laparotomy. Heparin (100 U) Medicine R E Pounder was injected into the inferior vena cava and the rats were killed by cardiac exanguination. The Correspondence to: Jejunal ulceration induced by a single oral dose gastrointestinal tract was then arterially perfused Dr A Anthony, University of the non-steroidal anti-inflammatory drug with carbon ink for visualisation of the vascular Department of Histopathology, Royal Free (NSAID) indomethacin to rats is one of several anatomy. Briefly, the abdominal aorta was Hospital School of Medicine, chemically induced experimental models of cannulated with 5 gauge (French) polyethylene Rowland Hill Street, London inflammatory bowel disease.1 It has been noted intravenous tubing and the portal vein ruptured NW3 2PF, UK. that a most interesting and consistent feature of to permit perfusate outflow. The aorta was per- Accepted for publication these NSAID induced experimental lesions is fused with heparin-saline followed by carbon 15 July 1997 their propensity to occur along the mesenteric ink until the entire bowel had turned black. 764 Anthony, Pounder, Dhillon, Wakefield AM counting eyepiece graticule (25 µm intervals) was used to make vascular measurements. C Gut: first published as 10.1136/gut.41.6.763 on 1 December 1997. Downloaded from To quantify the vascularity of the mesenteric 12 and antimesenteric halves of the rat jejunum and ileum, segments of cleared tissues from 11 1 each rat were examined by light microscopy as described above. A line (AC) between two 10 2 B consecutive VR, not separated by a VB, passing from the mesenteric margin to the antime- 9 3 senteric margin was visualised using the MM eyepiece graduated scale (fig 1). The line was 8 4 bisected into mesenteric (AB) and antime- VR A senteric halves (BC). All arteries transecting VB VB the line in each half were scored 1, 2, or 3 VR 7 5 MP according to outer diameter (score 1 = 25–50 VB VR 6 µm; score 2 = 50–75 µm; score 3 = 75–100 PIMA µm). A total score for each half was determined by summating the scores. For each rat, five consecutive lines were assessed in this way and Figure 1: Schematic diagram of the rat small intestine indicating the arterial blood the mean score was calculated for the me- supply. Long (VR) and short (VB) feeding vessels arising from the peri-intestinal marginal senteric and antimesenteric halves. The mean artery (PIMA) supply the antimesenteric (AM) and mesenteric margins (MM) (SEM) score in each half was determined for respectively. The cross section of the bowel wall is considered to represent a clock face where the antimesenteric and mesenteric margins are located at 12 and 6 o’clock respectively. the group of rats (n=5). Indomethacin induced jejunal ulceration Two groups of rats (n=5) received an oral dose of indomethacin 10 mg/kg as a sodium bicarbonate 1.5% aqueous solution. In one group the rats were terminally anaes- thetised four hours after indomethacin and the entire small intestine was examined externally for early lesions. After terminal cardiac exan- guination, the small intestine was perfused arterially with carbon ink as described in the previous section. The jejunum (defined as the segment of small intestine beginning 10 cm distal to the pylorus and ending 20 cm from the http://gut.bmj.com/ ileocaecal valve) and terminal ileum (defined as the terminal 10 cm of intestine), were opened longitudinally along the antimesenteric mar- gin, pinned onto cork, immersion fixed over- night, and cleared to transparency using the method described earlier. The position of each Figure 2: The mesenteric margin of an unopened loop of normal rat jejunum that has indomethacin induced early mucosal lesion on September 28, 2021 by guest. Protected copyright. been cleared to reveal the carbon filled vasculature. Only the arterial system was filled with carbon ink. Arising from the large extramural peri-intestinal marginal artery are VR (large and its relationship with the vasculature was arrow) and the smaller VB (small arrow). Notice that the sites of penetration of the VB are noted by both dissection microscopic examin- closer to the mesenteric margin than the sites of VR penetration. The areas of the bowel ation and light microscopy. Smaller pieces of supplied by the VB correspond to sites of indomethacin ulceration. Bar = 0.2 cm. tissue from the main specimen were placed on Segments of mid-jejunum (20 cm) and termi- a glass slide and covered with a glass cover slip. nal ileum (10 cm) were removed and divided Areas of normal mucosa from antimesenteric into two, one half being opened longitudinally and mesenteric sites were also examined. along the mesenteric margin and the other Lesions and normal areas were examined opened along the antimesenteric margin. The histologically by trimming them from the main tissues were pinned onto cork and immersion specimen, washing in chloroform overnight, and fixed overnight. The tissues were then dehy- processing into paraYn wax for routine histol- drated in absolute ethanol and cleared to ogy. transparency in methylsalicylate using the In the other group the rats were killed 24 method of Spalteholtz.10 Small segments (2 hours later and the small intestine examined cm) of jejunum and ileum were left unopened externally for lesions followed by longitudinal for the examination of intact tissue. The vascu- opening along the mesenteric margin for lar anatomy was examined by dissection assessment of advanced mucosal ulceration. microscopy, focusing primarily on the feeding vessels of the bowel wall and the submucosal Ligation of vasa recta and vasa brevia plexus. Distances (mm) between feeding ves- Experiments involving extramural ligation of sels were measured using a ruler. It was possi- rat VR and VB feeding vessels were performed ble to trim away small sections of cleared tissue to establish which parts, if any, of the bowel from the main specimen for direct visualisation wall would ulcerate after prolonged (24 hours) under a light microscope by securing the piece ischaemia.
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