The isolated bowel segment (Iowa model II); Motility across the anastomosis with or without mesenteric division

The Isolated Bowel Segment (Iowa Model II): Motility Across the A n a s t o m o s i s With or Without M e s e n t e r i c Division By Masahito Yamazato, Ken Kimura, Hiroaki Yoshino, Michel Murr, Dan EIIsbury, and Robert T. Soper Iowa City, Iowa 9 In previous reports, anastomosis has been shown to disrupt the myoelectric activity of the bowel. However, these studies have failed to delineate the role of the extrinsic nerves. Using an isolated bowel segment (IBS) and an amesenteric bowel segment (ABS), motility was evaluated by myoelectric recording across a bowel anastomosis. Ten rats were divided equally into the experimental group with the IBS and the control group with the ABS. In the IBS group, an 8-cm segment of jejunum was divided, reanastomosed, and coapted to the liver margin (Iowa model II). In the ABS group, an 8-cm segment of jejunum was coapted to the liver margin without disruption of bowel continuity (Iowa model II variant). Two weeks later, bipolar electrodes were implanted in the IBS and ABS, and normal jejunum in both groups. Mesenteric division (MD) was performed 4 weeks later to eliminate extrinsic innervation. Myoelectrical recordings were taken 2 weeks before and after MD. In the control group with IBS, incoordination in the propagation of the migrating motor complex (MMC) and reduction in the frequency of slow waves (FSW) were observed across the anastomosis and were unchanged by MD. In the control group with the ABS, the MMC and FSW were identical to that in the normal jejunum and were unaffected by MD. In both groups postprandial inhibition of the MMC was the same as in the normal jejunum and was unaffected by MD. This study confirms that incoordination in propagation of the MMC and reduction in FSW occur across a bowel anastomosis, and elimination of extrinsic innervation does not affect the autonomy of these changes. Postprandial inhibition of the MMC does not appear to be affected by intramural discontinuity or elimination of extrinsic innervation. Copyright 9 1992 by W.B. Saunders Company INDEX WORDS: Isolated bowel segment (Iowa model), motility, myoelectrical activity.

REPORTS show that there is incoorp REVIOUS dination in the propagation of the migrating motor complex (MMC) and reduced frequency of slow waves (FSW) across bowel anastomoses, suggesting that motility is autonomously controlled in each segment of bowel. 1 However, these studies have failed to eliminate the influence of extrinsic innervation carried through the mesentery. We developed a technique to create an isolated bowel segment (IBS) that is totally devoid of its mesentery yet with its viability, motility, and absorption preservedY In this study, we evaluated motility by myoelectrical recordings taken across a bowel anastomosis between normal jejunum and the IBS which is devoid of a mesentery, and thereby lacking any extrinsic innervation that might come through its mesenteric attachment.

Journal of Pediatric Surgery, Vol 27, No 6 (June), 1992: pp 691-695

MATERIALS AND METHODS

Initial Operation Ten male Spraque-Dawley rats (weighing 300 to 350 g) were equally divided into experimental and control groups. The rats were anesthetized by intraperitoneal injection of chloral hydrate (300 mg/kg) and the abdomen was entered through a median incision. In the experimental group, the jejunum was divided at 10 and 18 cm from the ligament of Treitz and both ends of the IBS were immediately reanastomosed to reconstruct bowel continuity. Hepatoenteropexy was established by denuding the serosa of the antimesenteric border of the 8-cm jejunal loop and the anterior liver margin and then coapting these two surfaces by running sutures of 5-0 Vicryl (Iowa model II). In the control group, a jejunal loop of identical site and length to the experimental group was also coapted to the liver to form a hepatoenteropexy, however bowel continuity was retained. At the end of the procedure, aminobenzyl penicillin (100 mg/kg) was administered intraperitoneally; lactated Ringer's solution (20 mg/kg) was given intravenously, and then discontinued. Purina rat chow feedings were begun 24 hours after operation.

Second Operation Two weeks later, six sets of bipolar electrodes were constructed using 30-cm-long Teflon-coated stainless steel wire of 79-t~m diameter (AS631 Cooner Wire Co, Chatsworth, CA). These electrodes were implanted in both groups of animals intramurally 2 mm apart from each other in the hepatoenteropexy (3), proximal jejunum (2), and distal jejunum (1), at intervals of 2 cm. The wires were assembled into a silicon tube that was passed through a subcutaneous tunnel and then connected to a socket that was secured to the posterior neck skin and muscles of the animals by wire sutures. 6 Perioperative management was identical to the first operation.

Third Operation Four weeks after the second operation, the abdomen was again entered in both groups of animals. The mesentery to the bowel loop coapted to the liver margin (the hepatoenteropexy bowel) was completely severed to create an IBS and an amesenteric bowel segment (ABS) in the experimental and control group, respectively. The IBS and ABS retain their viability by collateral circulation from the liver which develops after hepatoenteropexy (Figs 1A and 1B).

From the Department of Surgery, The Universityof Iowa Collegeof Medicine, Iowa City, IA. Presented at the 24th Annual Meeting of the Pacific Association of Pediatric Surgeons, Hong Kong, May 20-24, 1991. Address reprint requests to Ken Kimura, MD, Department of Surgery, The University of Iowa Hospitals & Clinics, Iowa City, IA 52242. Copyright 9 1992 by W.B. Saunders Company 0022-3468/92/2706-0003503. 00/0

691

692

YAMAZATO ET AL

B

A Fig 1.

Bowel anatomy and location of electrodes in the (A) experimental and (B) control groups,

Myoelectrical Recording Myoelectrical recordings were carried out 2 weeks before and 2 weeks after mesenteric division. After 16 hours of fasting, rats were placed in a cage with minimal restraint. No sedatives were used. The electrode wires were connected to the lead selector coupler (type 9865; Beckman, Fullerton, CA) and an 8-channel Beckman recorder (Dynograph R611; Beckman). Fasting myoelectrical activity was recorded for 2 hours. Postprandial myoelectrical activity was recorded for 2 hours on separate occasions after 48 hours of fasting. In the restraint cage, rats were fed 3.0 to 5.0 g of rat chow when phase 3 activity of the MMC appeared in the tracing of the leads implanted in the proximal jejunum. The cut-off level was 5.3 to 30.0 Hz for recording MMC and postprandial myoelectrical activity. The speed of the tracing paper in each recording was varied as needed.

Analysis of Data Recordings in the tracing paper were visually inspected. The FSW per minute was counted on the recording paper and its mean value _+ SD was calculated to compare the two groups (experimental and control). The migration pattern of the MMC was visually analyzed. The cyclic period of the MMC (cMMC), which is represented by the time interval between the adjacent ends of phase 3 activity, was measured on the recording paper and expressed by mean value _+ SD (n = 5). In the postprandial recordings, inhibition of MMC by feeding was visually inspected.

All data were compared between the experimental and control groups. RESULTS

O f 10 rats, 2 d i e d o f o p e r a t i v e c o m p l i c a t i o n s , o n e f r o m e a c h g r o u p . T h e r e m a i n i n g 8 rats w e r e e n t e r e d i n t o t h e s t u d i e s . T h e s u r v i v o r s t o l e r a t e d r e g u l a r rat chow after these three operations.

MyoelectricaI Activities Slow waves. W e l l - r e c o g n i z e d slow w a v e s ( S W ) w e r e o b s e r v e d in b o t h g r o u p s . B e f o r e m e s e n t e r i c division, F S W in t h e p r o x i m a l j e j u n u m a n d t h e h e p a t o e n t e r o p e x y j e j u n u m w a s 34.8 __ 2.4 a n d 31.8 _+ 1.9, r e s p e c t i v e l y ( P < .01), in t h e e x p e r i m e n t a l g r o u p , w h e r e a s it w a s 33.3 -+ 1.6 a n d 33.2 _+ 1.6 ( N S ) , r e s p e c t i v e l y , in t h e c o n t r o l g r o u p . A f t e r m e s e n t e r i c division, F S W in t h e p r o x i m a l j e j u n u m a n d I B S (or A B S ) w a s 34.1 + 1.6 a n d 30.9 +- 1.4 ( P < .001), r e s p e c t i v e l y , in t h e e x p e r i m e n t a l g r o u p , w h e r e a s it w a s 32.8 + 0.9 a n d 32.5 _+ 0.8 ( N S ) , r e s p e c t i v e l y , in t h e c o n t r o l g r o u p . S t a t i s t i c a l l y significant d i f f e r e n c e in t h e F S W w a s o b s e r v e d a c r o s s t h e a n a s t o m o s i s , b u t

THE I S O L A T E D BOWEL S E G M E N T (IOWA M O D E L II)

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The MMC was clearly identified in both groups. In the experimental group, incoordinated propagation of the MMC was observed across the anastomosis between the proximal jejunum and the hepatoenteropexy bowel (IBS) (Fig 3). In the control group, coordinated propagation of the MMC from the proximal to distal jejunum via the hepatoenteropexy bowel (ABS) was observed. After mesen . . teric division, the pattern of propagation did not show a change in each group. Before mesenteric division, cMMC in the proximal jejunum and the hepatoenteropexy bowel was 16.1 _+ 4.0 and 14.2 + 4.5 minutes (NS), respectively, in the experimental group, whereas it was 17.2 _+ 5.3 and 17.5 _+ 5.9 minutes (NS), respectively, in the control group. After mesenteric division, cMMC in the upper jejunum and the hepatoenteropexy bowel (IBS or ABS) was 18.8 -+ 5.5 and 18.3 +-- 4.8 minutes (NS), respectively, in the experimental group, whereas it was 18.4 + 4.6 and 19.7 _+ 4.8 minutes (NS), respectively, in the control group (Fig 4). Postprandialpattern. Postprandial pattern showed no difference between the two groups, before and after mesenteric division. Postprandial inhibition of MMC was identically observed in both groups (Fig 5).

DISCUSSION In the previous studies, we tested the motility of the IBS (Iowa model II), which was created in functioning jejunum of rat by hepatoenteropexy. Contrast material was propelled downstream and coordinated aborad propagation of MMC was observed in radiological and myoelectrical studies. 4 These preliminary studies did not include myoelectrical recordings in the IBS before mesenteric division and in the control normal jejunum

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bowel, and, therefore, did not allow us to evaluate the influence of extrinsic innervation on the myoelectrical changes in the IBS. This study was designed to cover these defects. Myoelectrical activity generated in the smooth muscle of the small bowel consists of two representative components; SW and electrical response activity (spike burst [SB]). 7'8 SW are generated in the longitudinal muscle cells in the proximal bowel and propagates distally through the enteric nervous system or special muscle structure. 9,1~ Each muscle cell in dif-

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694

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ferent locations may generate SW. SW are believed to be the pacesetter potential that controls the site, frequency, and direction of circular muscle contraction. H SB represents circular muscle contraction and M M C is one of the components in the SB that appears cyclically in the gastrointestinal tract of most mammals in fasted states, ~2,~3 Every SB is superimposed on the SW. 14,15Therefore, the frequency of SB (or MMC) does not exceed that of the SW. In previous reports, 16,a7 reduction in the FSW has been observed across the anastomosis as we observed in the experimental group before the mesentery was divided. No significant change in the FSW was in-

ET AL

duced by mesenteric division in this group, which supports the contention that the FSW may be regulated by an intrinsic conductive system such as the enteric nervous system or muscular continuity. Previous studies reported that incoordination in propagation of M M C occurs across bowel that has been divided and reanastomosedJ 8,19 In the experimental group, incoordinate propagation of M M C was observed between the upper normal jejunum and the IBS across the anastomosis regardless the attachment of its mesentery, which was identical to the result of other reports. 2~ However, coordinate propagation of M M C was observed in the IBS independent from the rest of the bowel. 1 These observations support the contention that coordination in propagation of M M C can be maintained as long as continuity of the bowel wall musculature including the enteric nervous system is intact. Coordination in propagation of M M C across an anastomosis has been observed to be reestablished 3 to 6 months as the enteric nervous system recovers its continuity. 7,18In the present experiment, the limited time interval between creation of the IBS and myoelectrical recordings (2 weeks) does not seem adequate for reconnection of the enteric nervous system across the anastomosis. Postprandial pattern of motility (PPM) is a prolonged irregular spike activity that interrupts periodic activity in which M M C propagates aborally. In this study, PPM was identical between the experimental and control groups regardless of the status of the mesenteric attachment. PPM appeared 3 to 5 minutes after the start of eating. Identical PPMs were recorded in the upper normal jejunum, IBS, and lower normal jejunum in the control group. This result differs from those in FSW and MMC, suggesting that PPM is not mediated over the enteric nervous system or extrinsic innervation. The overall results of this study suggest that elimination of extrinsic innervation of a bowel segment by dividing its mesentery does not influence autonomy of myoelectrical changes across the anastomosis.

REFERENCES

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6. Yamazato M, Kimura K, Yoshino H, et al: Improved technique of electrode implantation for myoelectrical recording of bowel. J Pediatr Surg 27:394-395,1992(abstr) 7. S{~rna SK: Gastrointestinal electrical activity. Terminology. Gastroenterology68:1631-1635,1975 8. Weibrodt NW: Motilityof the small intestine, in Johnson LR (ed): Physiologyof Gastrointestinal Tract, vol 2. New York, NY, Raven, 1981,pp 411-443 9. Sarna SK, Otterson MF: Small intestinal physiology and pathophysiology.Gastroenterol Clin North Am 18:375-404,1989 10. Wingate DL: The small intestine, in Christensen J, Wingate DL (eds): A Guide to Gastrointestinal Motility. Littleton, MA, Wright PSG, 1983,pp 101-127

THE ISOLATED BOWEL SEGMENT (IOWA MODEL II)

ll. Mathias JR, Sninsky CA: Motility of the small intestine: A look ahead. Am J Physiol 248:G495-500, 1985 12. Sarna S, Condon RE, Cowels V: Enteric mechanism of initiation of migrating myoelectric complexs in dogs. Gastroenterology 84:814-822, 1983 13. Ruckebusch M, Fioramonti J: Electrical spiking activity and propulsion in small intestine in fed and fasted rat. Gastroenteroloty 68:1500-1508, 1975 14. Bass P: In vivo electrical activity of the small bowel, in Code FC (ed): Hand Book of Physiology, section 6, vol 4: Motility. Baltimore, MD, Williams & Wilkins, 1968, pp 2051-2074 15. Conklin JL, Christensen J: Local specialization at ileocecal junction of the cat and opossum. Am J Physio1228:1075-1081, 1971

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