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Original communication| Volume 139, ISSUE 3, P395-406, March 2006

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Induction and recovery of colonic motility/defecatory disorders after extrinsic denervation of the colon and rectum in rats

      Background

      Anterior resection for rectal disease is associated with extrinsic autonomic denervation of the neorectum, which may influence the myenteric plexus, and subsequently the motility/defecatory status after operation.

      Methods

      A rat model with denervated neorectum was constructed. Colonic contractile activity in vivo, the amount of generic neuron marker (PGP 9.5) and nitric oxide synthase (NOS) were measured periodically. The responses of the muscle strip in each period to electrical field stimulation were evaluated using various neurotransmitters.

      Results

      In rats with denervated neorectum, giant migrating contractions (GMCs) of the distal colon, the number of fecal lumps per day and their small size, significantly increased in the early phase postoperatively, although both recovered in the late-phase period. The contractile response of the muscle strip of the denervated colon to acetylcholine was reduced throughout the period; however, contraction of the denervated colon under the addition of NO inhibitor (l-NAME) was enhanced significantly in the late-phase period, and recovered to the control level by atropine. Neuronal NOS, but not PGP 9.5 concentration, in the myenteric plexus at the distal denervated colon, significantly increased in the late-phase period. None of the above items differed from the control at other colonic portions throughout the period.

      Conclusions

      Extrinsic autonomic denervation causes abnormal hyper-motility in the neorectum, which may be associated with multiple evacuations in the early phase postoperatively. Increased acetylcholine and the subsequent increase of neuronal NOS in the myenteric plexus may be an adaptive mechanism to compensate for such abnormal colonic motility after extrinsic denervation.
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      References

        • Sarna S.K.
        Physiology and pathophysiology of colonic motor activity (1).
        Dig Dis Sci. 1991; 36: 827-862
        • Sarna S.K.
        Physiology and pathophysiology of colonic motor activity (2).
        Dig Dis Sci. 1991; 36: 998-1018
        • Netter F.H.
        Innervation of small and large intestine.
        in: Oppenheimer E. The Netter collection of medical illustrations. Vol. 3. Part II: lower digestive tract. Icon Learning Systems, New Jersey2000: 77-90
        • Iizuka I.
        • Koda K.
        • Seike K.
        • Shimizu K.
        • Takami Y.
        • Fukuda H.
        • Tsuchida D.
        • Oda K.
        • Takiguchi N.
        • Miyazaki M.
        Defecatory malfunction caused by motility disorder of the neorectum after anterior resection for rectal cancer.
        Am J Surg. 2004; 188: 176-180
        • Shibata C.
        • Sasaki I.
        • Matsuno S.
        • Mizumoto A.
        • Itoh Z.
        Colonic motility in innervated and extrinsically denervated loops in dogs.
        Gastroenterology. 1991; 101: 1571-1578
        • Ohta D.
        • Ozeki K.
        • Ura K.
        • Tsunoda T.
        • Kanematsu T.
        Effect of celiac and superior mesenteric ganglionectomy on fasted canine colonic motor activity.
        Surg Today. 1995; 25: 717-721
        • Ishikawa M.
        • Mibu R.
        • Iwamoto T.
        • Konomi H.
        • Oohata Y.
        • Tanaka M.
        Change in colonic motility after extrinsic autonomic denervation in dogs.
        Dig Dis Sci. 1997; 42: 1950-1956
        • Irie M.
        • Kajiyama Y.
        • Enjoji A.
        • Ozeki K.
        • Ura K.
        • Kanematsu T.
        Changes in colonic motility in dogs after a resection of the inferior mesenteric ganglion and plexus.
        Surg Today. 1998; 28: 626-632
        • Tanabe Y.
        • Hotokezaka M.
        • Mibu R.
        • Tanaka M.
        Effects of extrinsic autonomic denervation and myenteric plexus transection on colonic motility in conscious dogs.
        Surgery. 2002; 132: 471-479
        • Koda Keiji
        • Saito Norio
        • Seike Kazuhiro
        • Shimizu Kimio
        • Kosugi Chihiro
        • Miyazaki Masaru
        Denervation of the neorectum as a potential cause of defecatory disorder following low anterior resection for rectal cancer Dis Col Rectum. 2005; 48: 210-217
        • Li M.
        • Johnson C.P.
        • Adams M.B.
        • Sarna S.K.
        Cholinergic and nitrergic regulation of in vivo giant migrating contractions in rat colon.
        Am J Physiol Gastrointest Liver Physiol. 2002; 283: G544-G552
        • Sethi A.K.
        • Sarna S.K.
        Contractile mechanisms of colonic propulsion.
        Am J Physiol Gastrointest Liver Physiol. 1995; 268: G530-G538
        • Oya M.
        • Sugamata Y.
        • Komatsu J.
        • Ishikawa H.
        • Nozaki M.
        Poor neorectal evacuation as a cause of impaired defecatory function after low anterior resection.
        Surg Today. 2002; 32: 111-117
        • Yagyu T.
        • Yamamoto T.
        • Mochizuki H.
        New predictor for the defecatory function after sphincter-preserving operation.
        World J Surg. 2002; 26: 54-58
        • Nakahara S.
        • Itoh H.
        • Mibu R.
        • Ikeda S.
        • Oohata Y.
        • Kitamo K.
        • Nakamura Y.
        Clinical and manometric evaluation of anorectal function following low anterior resection with low anastomotic line using an EEA stapler for rectal cancer.
        Dis Colon Rectum. 1988; 31: 762-766
        • Horgan P.G.
        • O’Connel P.R.
        • Shinkwin C.A.
        • Kirwan W.O.
        Effect of anterior resection on anal sphincter function.
        Br J Surg. 1989; 76: 783-786
        • Hida J.
        • Yasutomi M.
        • Fujimoto K.
        • Okuno K.
        • Ieda S.
        • Machidera N.
        • Kubo R.
        • Shindo K.
        • Koh K.
        Functional outcome after low anterior resection with low anastomosis for rectal cancer using the colonic J-pouch.Prospective randomized study for determination of optimum pouch size.
        Dis Colon Rectum. 1996; 39: 986-991
        • Otto I.C.
        • Ito K.
        • Ye C.
        • Hibi K.
        • Kasai Y.
        • Akiyama S.
        • Takagi H.
        Causes of rectal incontinence after sphincter-preserving operations for rectal cancer.
        Dis Colon Rectum. 1996; 39: 1423-1427
        • Tomaru A.
        • Ishii A.
        • Kishibayashi N.
        • Karasawa A.
        Colonic giant migrating contractions induced by glycerol enema in anesthetized rats.
        Jpn J Pharmacol. 1993; 63: 525-528
        • Sethi A.K.
        • Sarna S.K.
        Colonic motor activity in acute colitis in conscious dogs.
        Gastroenterology. 1991; 100: 954-963
        • Takahashi T.
        • Nakamura K.
        • Itoh H.
        • Sima A.A.
        • Owyang C.
        Impaired expression of nitric oxide synthase in the gastric myenteric plexus of spontaneously diabetic rats.
        Gastroenterology. 1997; 113: 1535-1544
        • Nakamura K.
        • Takahashi T.
        • Taniuchi M.
        • Hsu C.X.
        • Owyang C.
        Nicotinic receptor mediates nitric oxide synthase expression in the rat gastric myenteric plexus.
        J Clin Invest. 1998; 101: 1479-1489
        • Hasler W.L.
        • Kurosawa S.
        • Chung O.Y.
        Regional cholinergic differences between distal and proximal colonic myenteric plexus.
        Am J Physiol. 1990; 258: G404-G410
        • Takahashi T.
        • Owyang C.
        Regional differences in the nitrergic innervation between the proximal and the distal colon in rats.
        Gastroenterology. 1998; 115: 1504-1512
        • Mizuta Y.
        • Takahashi T.
        • Owyang C.
        Nitrergic regulation of colonic transit in rats.
        Am J Physiol. 1999; 277: G275-G279
        • Gonzalez A.
        • Sarna S.K.
        Neural regulation of in vitro giant contractions in the rat colon.
        Am J Physiol Gastrointest Liver Physiol. 2001; 281: G275-G282
        • Yunker A.M.
        • Galligan J.J.
        Extrinsic denervation increases NADPH diaphorase staining in myenteric nerves of guinea pig ileum.
        Neurosci Lett. 1994; 167: 51-54
        • Nakao K.
        • Takahashi T.
        • Utsunomiya J.
        • Owyang C.
        Extrinsic neural control of nitric oxide synthase expression in the myenteric plexus of rat jejunum.
        J Physiol. 1998; 507: 549-560
        • Leelakusolvong S.
        • Sarr M.G.
        • Miller S.M.
        • Phillips S.F.
        • Bharucha A.E.
        Role of extrinsic innervation in modulating nitrergic transmission in the canine ileocolonic region.
        Am J Physiol Gastrointest Liver Physiol. 2002; 283: G230-G239