Upsala J Med Sci 81: 97-102, 1976 Gastric Evacuation and Propulsive Intestinal Motility in Acute Afferent Loop Syndrome in the Rat SVEN DAHLGREN From the Department of Surgery, University Hospital, U p p s a l a , Sweden ABSTRACT The acute afferent loop syndrome, i.e. occlusion of the afferent loop after partial gastrectomy by the Billroth I1 method, was produced in the rat. In a primary session a gastrojejunostomy with division of the pylorus was performed. 2-3 months later the afferent loop was ligated.. The gastric evacuation and the propulsive motility of the intestine were studied quantitatively, using an inert radio- isotope. Both the gastric evacuation and the propulsive in- testinal motility were considerably delayed in ALS, both in relation to the laparotomized controls and in relation to previous findings in mechanical intestinal obstruction and paralytic ileus due to retroperitoneal irritation or bacterial peritonitis. INTRODUCTION The gastric evacuation and propulsive intestinal motility in different pathological conditions of the abdomen and after different intra-abdominal oper- ations have been described by several authors (7-1 1, 13, 14). Both gastric evacuation and intestinal propulsion thus appear to be easily affected by different forms of trauma to the abdomen and abdominal organs. The stomach evacuates, however, even in the pres- ence of a low small bowel obstruction ( I I ) . Similar- ly, according to t h e same authors, a slow propulsion of the intestinal contents takes place above the obstruction. It was considered of interest to find out how the gastrointestinal propulsive motility is af- fected by an even more violent acute abdominal catastrophe than obstructive ileus. For this purpose the acute afferent loop syndrome (ALS) was used. This condition comprises a total obstruction of the pressure in the occluded loop, and in dog experi- ments the pressure increased in some cases up to 100 mmHg. Within 24 hours the occluded loop shows signs of necrosis, there is evidence of hepatocellular degeneration in the liver, and a fully developed pancreatitis is observed (3). Death may follow within a few days, both in man and in ex- perimental animals ( 2 ) . The syndrome thus ful- fils the criteria of an acute severe abdominal catastrophe. The present study was considered of importance also for understanding of the acute af- ferent loop syndrome. MATERIAL 112 male rats of the same strain (Sprague-Dawley) were used. The animals were part of two series of a study of the pathophysiology in the acute afferent loop syndrome (1). The distribution of the animals into groups, and their body weights, are given in Table I. METHODS Operative technique. In a primary session a gastroenteros- tomy with division of the pylorus was performed. Two months later the main experiment was carried out, whereby the afferent loop was ligated with a 3-0 silk liga- ture close to the gastroenterostomy (ALS series) (Fig. 1). The abdomen was closed with single silk sutures in two layers. Further details of the operation have been given in (1). The control rats (laparotomized c o n t r o l s L C ) also underwent gastroenterostomy 2 months prior to the main experiment; this comprised the same dissection in the abdomen, the afferent loop being brought forward and a silk ligature being placed around it close to the gastro- enterostomy, but without tying of the ligature. afferent loop a partial gastrectomy by the The gastric evacuarion and propu~sive intestinal motility 'I method. In ALS, which may appear in were analysed by a method previously described in detail the immediately Postoperative stage after a ( 5 ) . A standardized test meal containing a radioactive gastrectomy or much later ( 2 ) , there is a rise in substance (NalS1Cr04) was deposited in the stomach im- Upsala J M e d Sci 81 7 -162852 98 S . Dahlgren Fig. 1 . Acute afferent loop syndrome in the rat. mediately after the afferent loop had been ligated or, in the control experiments, after the dissection of the afferent loop. After 0 . 5 , 4 , 8 and 12 hours (ALS series) and 0.5 and 4 hours (control series) the animals were anaesthetized with ether on an open mask and killed by cardiac puncture and exsanguination. The abdomen was opened by a large incision and ligatures were placxd around the cardia and around the efferent loop at the gastroenterostomy. Prior to this the entire afferent loop had been excised ( 1 ) . The whole gastrointestinal tract from the stomach to the anus was then taken out by careful dissection. The organs were then placed on a Plexiglas plate which was moved under a scintillation detector synchronously with an automatic linear recorder, connected to the re- cording unit of the scintillation detector. A quantitative study of the distribution of the radioactive test dose was then made, a planimetric analysis being performed on the area corresponding to the stomach and on each of 10 equal fractions into which the area of the small intestine had been divided. The caecum and colon were anlysed plani- metrically as one combined area. Each planimetrically determined area was expressed in percent of the total area of the curve, i.e. in per cent of the total amount of radioactivity in the gastrointestinal tract, corresponding to the radioactive dose. Further information was obtained by analysing the re- sults by the so-called quotient method described by Grev- sten, Johansson & Nylander ( 6 ) : X1 A=? v + z x, j = I where &=the propulsive quotient for intestinal fraction i xi=the radioactive content of fraction i V=the radioactive content of the stomach 2X,=the radioactive content of all fractions proximal to j = 1 fraction i i- I R E S U L T S T h e increase in weight in t h e different groups be- tween t h e primary operation and t h e main experi- ment is given in Table I . T h e s a m e table gives the haematocrit value a t t h e primary operation and at the main experiment and the number of animals in each group. Only a few animals in t h e group with 12 hours’ occlusion of t h e afferent loop died. T h e ani- mals were in surprisingly good condition a t the time of the main experiment, with t h e exception of the 12-hour group, which appeared extremely lethargic a n d ruffled and showed a very pale oral mucosa and a p o o r tendency t o bleeding from t h e tail, as signs of peripheral vascular contraction. Gastric evacuation T h e gastric evacuation is given as t h e proportion of t h e radioactive d o s e remaining in t h e stomach a t a given time point, expressed in p e r cent of t h e total d o s e administered. T h e mean values and the errors of the means for t h e percentage of t h e test d o s e recorded in t h e stomach and analysed plani- metrically are given f o r the different groups in Table 11. Figure 2 shows the corresponding values plotted in a coordinate system, where the radioac- tive gastric content is given o n t h e ordinate a n d t h e duration of occlusion of the loop o n the abscissa. It is seen that t h e gastric evacuation is exponential, a n d is markedly delayed in t h e afferent loop syndrome compared with t h e laparotomized con- trols. Since t h e comparison of importance was that be- tween laparotomized controls and A L S animals, t h e motility in intact controls with a gastroenterostomy alone w a s not studied in these experiments. T h e gastric evacuation in such animals h a s been shown b y Nylander & Wikstrom (lo), a n d their results a r e also included in Fig. 2 (IC). T h e difference be- tween t h e gastric evacuation in t h e control and A L S groups i s significant, both at experimental times of 0.5 and 4 hours (p<0.0005). JJpsala J M e d Sci 81 Gastro-intestinal motility in acute afferent loop syndrome 99 Table I . Data concerning the two series - No. of Initial Final Group animals Initial wt. Final wt. haematocrit haematocri t Control series 0.5 hr 16 233210.7 385k10.3 48f0.7 33k1.1 4 hrs 19 244f 7.9 400f 8.0 49f0.4 32+ 1.2 ALS series 0.5 hr 17 230f 4.8 394f 12.6 49f0.5 3651.6 4 hrs 24 244f 6.2 231f 7.5 5 0 f 0 . 7 35f1.5 8 hrs 18 238f 5.3 318k10.5 4 7 f 0 . 7 36f1.2 12 hrs 18 238f 5.7 406+ 7.8 4 9 f 0 . 4 31f1.0 Table 11. Planimetric analysis of the percentage distribution of the radioactive dose in the stomach, in fractions of the small intestine and in the colon Laparotomy controls Afferent loop syndrome 0.5 hr 4 hrs 0.5 hr 4 hrs 8 hrs 12 hrs Stomach Fraction 1 2 3 4 5 6 7 8 9 10 Caecumi -colon 67.8 k4.20 19.5f2.10 8 . 4 k 1.66 3.4f1.12 1.0k0.70 0.1 k0.14 0.4f0.38 0.1 f0.09 30.8f7.75 5 . 9 f 1 . 3 8 5.2 f0.98 1.820.63 2.6 f 0.94 2 . 9 f 1.05 6.2f 1.67 12.5 f 3.70 1 l.Of3.60 6.823.30 8 .Of3.57 8.8k4.89 89.9f2.36 65.5 f 6 . 0 5 8.8f1.82 14.1k1.97 1.4f0.69 5.3f 1.10 0.2f0.20 3.3f0.97 3.1 f 1.08 3.0k1.20 3.4f1.50 I .4f0.74 1.3f0.24 1.1 k0.22 0.8f0.19 63.426.69 42.7k7.32 18.2 k2.49 15.3 f 2 . 4 3 10.823.03 9.122.36 4 . 3 f 1 . 4 8 6. I f 1.34 2 . 9 f 1.29 6 . 4 k 1.75 1.0f0.71 6.4k2.12 0.2f0.24 4.1f1.30 2.8+ 1.03 2.7+ I .95 1.7 + 1.09 0.7f0.48 2.622.15 Propulsive intestinal motility The percentage distribution of the test dose in the 10 equal, consecutive fractions of the small in- testine and the colonic fraction, as obtained by planimetry, is given in Table 11. The same values are illustrated graphically in Fig. 3 for control and ALS animals a t experimental times of 0.5 and 4 hours, and i n Fig. 4 for 4-hour control animals and for ALS animals a t 8 and 12 hours. Fractions con- taining less than 5 % of the total test dose were not included in the subsequent analysis. It was found that the propulsion in the distal direction after 0.5 hours had reached the second fraction in the control cases and the first fraction in the ALS group. After 4 hours the colonic fraction was reached i n the controls and the second fraction in the ALS group. After 8 and 12 hours the second and fifth fractions, respectively, had been reached in the ALS group. Thus the propulsion was considerably delayed in the acute afferent loop syndrome. The relationship between gastric evacuation and propulsive intesti- nal motility is evident from the propulsive quotients given numerically in Table 111 and diagrammatically in Fig. 5. In the acute afferent loop syndrome there is thus a strong inhibition of the intestinal propul- sion. % X-X L C 0-OALS A-A IC { N y l a n d e r B W i k s t r o m 1967) 2o 1 2 4 6 8 10 12 hrs Fig. 2 . Diagram illustrating gastric emptying. Upsala J Med Sci 81 100 S . Dahlgren Table 111. The propulsive quotient Fraction Groups 1 2 3 4 5 6 7 8 9 10 Colon LC 0.5 h r 0.29 0.10 LC 4 h r s 0.19 0.14 0.04 0.06 0.06 0.13 0.23 0.16 0.09 0.09 0.09 ALS 0.5 hr 0.10 ALS 4 hrs 0.22 0.08 ALS 8 hrs 0.29 0.13 ALS 12 hrs 0.36 0.16 0.09 0.09 0.08 DISCUSSION The inhibitory effect of laparotomy on the gastrointestinal motility has been pointed out previ- ously by Nylander & Wikstrom ( l o ) , Nylander & Svensson ( 1 I ) and Kylberg (8), among others. In the present control rats the laparotomy was combined with a dissection of the afferent loop corresponding to that required in order to place a ligature around the afferent loop and thereby produce an afferent loop syndrome. In this way the inhibitory effect was even more pronounced than in the previously de- scribed laparotomies. Despite the relatively strong inhibition of the intestinal motility after the laparo- tomy, there was a significantly more delayed gastric evacuation in the ALS groups and a delay of the propulsive motility. In ALS the entire small in- $ 100 1 n=17 0 . 5 hr ALS % 80 I testine is intact, since the pathological process lies in the blind portion which is occluded from the efferent intestinal segment leading from the stomach. Even though this efferent part is com- pletely intact, as well as the communication be- tween the stomach and the efferent loop, ALS leads to pronounced gastric and intestinal paralysis, which was found in these studies to be more marked than has been described in experimental intestinal obstruction in the rat ( 1 1). There are certainly sev- eral reasons for this. In ALS the pathological pro- cess is localized to the upper part of the abdomen in the vicinity of the stomach, while that in a low small bowel obstruction lies i n the lower part of the abdomen. ALS has, in addition, a direct effect on three organs, the duodenum, liver and pancreas. Of n=22 4 hrs A I S 1 2 3 4 5 6 I 8 9 10 z 1 0 0 1 as16 0.5 hr c o n t r o l s % 100 80 60 40 20 0 1 2 3 4 5 6 7 8 9 1 0 1 n=19 4 hrs controls h,, 1 2 3 4 5 6 7 8 9 1 0 colon F i g . 3. Histograms representing the quantitative distribu- tion of the radioactive substance in the gastrointestinal Upsala J Med Sci 81 sample. Control groups 0.5 and 4 hours and ALS groups 0.5 and 4 hours. Gastro-intestinal motility in acute afferent loop syndrome 101 100 80 60 . Ic loO1 80 a. n=18 8 hrs ALS 0 - h ::L 20 1 2 3 4 5 6 7 8 9 10 n=19 4 hrs controls 1 2 3 4 5 6 7 8 9 1 0 E O l o n % 100 60 n=18 12 h r e ALS 4: 20 L 1 2 3 4 5 6 7 8 9 10 colon -19 4 hrs c o n t r o l s ::k 0 , , rc-h , , , 1 2 3 4 5 6 7 8 9lOealon F i g . 4 . Histograms representing the quantitative distribu- tion of the radioactive substance in the gastrointestinal sample. Control group 4 hours and ALS groups 8 and 12 hours. probable importance for the development is the di- lated, tense duodenal loop, i n which rnucosal necrosis gradually occurs (3). This necrosis gives a possibility of leakage into the peritoneum of both bacteria from the bacteriarich duodenal fluid (1) and toxins. Supporting this assumption are the signs of peritonitis with increased fluid in the peritoneum which were observed i n all cases. In ALS, pancreatitis occurs regularly (3, 4, 13). This also contributes both to peritonitis and t o paralytic ileus, which is a regular component in all cases of pancreatitis. Added to this is the fact that ALS also gives rise to biliary stasis and hepato- cellular degeneration (3), which can contribute to deterioration of the liver function and thereby re- duction of the capacity of general detoxification. Paralytic ileus has been produced previously in A-A LC L h r s 0 4 LC 0 5 " ._. A l S 1 2 " 0-0 ALS 8 " 04 A L S L '' A A l S 0 5 " I . . . . . . . . . . , 1 2 3 L 5 6 7 8 9 10 colon Froction Fig. 5. Diagram illustrating propulsive quotient values. the rat both by means of bacterial peritonitis (8) and through retroperitoneal irritation (9). The paralysis of the gastrointestinal tract occurring in the acute afferent loop syndromes seems to be more pro- nounced, however. Contributing to this is thus the combination of pancreatitis, intestinal necrosis, hepatocellular degeneration and peritonitis, and in the final phase the irreversible shock which de- velops. REFERENCES 1. 2 . 3. 4 . 5. 6. Bengtsson, S . , Dahlgren, S . & Hellsing, K.: The path- ophysiology of the acute afferent loop syndrome. Acta Chir Scand 1976. (In press.) Dahlgren, S . : The afferent loop syndrome. Acta Chir Scand, Suppl. 327, 1964. Dahlgren, S . & Thorell, J.: Histological changes in the duodenum, pancreas and liver in the acute affer- ent loop syndrome. In The Afferent Loop Syndrome (ed. S . Dahlgren). Acta Chir Scand, Suppl. 327: 65, 1964. Dahlgren, S . & Stenram, U . : Acute pancreatitis and hepatic necrosis in the acute afferent loop syndrome-a histopathological study in the rat. Up- sala J Med Sci 1976. (In press.) Derblom, H . , Johansson, H . & Nylander, G . : A sim- ple method of recording quantitatively certain gastro- intestinal motility functions in the rat. Acta Chir Scand 132: 154, 1966. Grevsten, S . , Johansson, H. & Nylander, G.: Analysis of a quantitative method of evaluation a s applied to the propulsive gastrointestinal motility in the rat. Acta Chir Scand 133: 563, 1967. Upsala J Med Sci 81 102 S. Dahlgren 7. Johansson, H. & Nylander, G.: Ileo-colic transit in rats subjected to ileocaecal resection. Acta Chir Scand 135: 455, 1969. 8. Kylberg, F.: Gastric evacuation and propulsive in- testinal motility in experimental perforation peri- tonitis. Scand J Gastroent5: 593, 1970. 9. Lindquist, B.: Propulsive gastrointestinal motility re- lated to retroperitoneal irritation. Acta Chir Scand, Suppl. 384, 1968. 10. Nylander, G. & Wikstrom, S.: Gastric emptying and propulsive intestinal motility following partial gastric resection, gastroenteroanastomosis, and abdominal “trunk” vagotomy in the rat. Acta Chir Scand 133: 41, 1967. 11. Nylander, G. & Svensson, A.: Gastric emptying and propulsive intestinal motility in experimental intestinal obstruction. Acta Chir Scand 134: 135, 1968. 12. Parkkulainen, K. V.: Simple low small bowel obstruc- tion. Acta Chir Scand, Suppl. 290, 1962. 13. Port, M . & Gelb, A.: Acute afferent loop syndrome simulating acute pancreatitis. Amer J Gastroent 53:36, 1970. 14. Wikstrom, S.: Propulsive gastrointestinal motility in regional and graded ischemia of the small bowel. Acta Chir Scand, Suppl. 386, 1%8. Received November I , 1975 Address for reprints: Sven Dahlgren Karnsjukhuset Skovde Fack S-54101 Skovde Sweden Upsulu J Med Sci 81