CHA

L.C. Weaver and C. Polosa (Eds.)

Progress in Brain Research, Vol. 152

ISSN 0079-6123

Copyright r 2006 Elsevier B.V. All rights reserved

PTER 21

Gastrointestinal symptoms related to autonomicdysfunction following spinal cord injury

Eric A.L. Chung and Anton V. Emmanuel�

St Mark’s Hospital, Northwick Park, Watford Road, Harrow, Middlesex, HA1 3UJ, UK

Abstract: The impact of spinal cord injury on an individual’s gastrointestinal tract function is often poorlyunderstood by the general public and also by those involved with persons with spinal cord injury. Thischapter reviews the anatomy, physiology and function of the gastrointestinal tract, with particular em-phasis on neurological control mechanisms. In turn, it relates the effect that spinal cord injury has on theneurological control of the gastrointestinal tract. The symptoms that are encountered by patients in theacute phase following injury, and by individuals in the months/years after injury, with particular referenceto the effect of altered autonomic nervous system control of the gastrointestinal tract, are discussed.Together with a following summary of current bowel management regimens and techniques, this chapteraims to provide an overall view of the effect that autonomic dysfunction due to spinal cord injury has ongastrointestinal function.

Introduction

Among the general population, the perceived im-pact that spinal cord injury has on people is oftenlimited to the noticeable effects of impaired mo-bility. Less well appreciated by the general popu-lation is the impact that spinal cord injury has onpelvic function, resulting in bladder, bowel andsexual dysfunction.

Control of the gastrointestinal system involvescomplex interactions between autonomic and so-matic innervation acting ultimately at the level ofthe intrinsic enteric nervous system. Followingspinal cord injury, this fine control mechanism isinterrupted to varying degrees, dependent uponthe level and extent of the spinal cord injury. Theresult is a spectrum of possible gastrointestinalsymptoms. To date, the effects of spinal cord in-jury on bowel function and management havebeen poorly understood. A much larger volume of

�Corresponding author. Tel.: +020-8235-4084;

Fax: +020-8235-4162; E-mail: a.emmanuel@imperial.ac.uk

DOI: 10.1016/S0079-6123(05)52021-1 317

published work has been dedicated to the urolog-ical sequelae of spinal cord injury, compared to theeffects on the gastrointestinal system. However, inrecent years this has begun to be researched. Thishas been fuelled by work that has shown that aconsiderable proportion of cord-injured peoplerate bowel dysfunction as a greater source ofdistress than bladder and sexual problems (Stoneet al., 1990a; Glickman and Kamm, 1996; De Loozeet al., 1998; Han et al., 1998).

In both the acute and long-term phases of spinalcord injury, patients report high levels of gastroin-testinal morbidity (Cosman et al., 1991; Kroghet al., 1997; De Looze et al., 1998; Miller et al.,2001). Gastrointestinal problems are a large cause ofrehospitalization among people with spinal cord in-jury, accounting for 11% of readmissions in a recentAustralian study (Middleton et al., 2004). This mor-bidity has significant cost implications to healthcaresystems in the acute hospital and community setting(Harvey et al., 1992; Johnson et al., 1996).

In the acute spinal cord injury setting, symp-toms can affect any region of the gastrointestinal

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tract. At the upper end of the gut, problems in-clude gastric dilatation, ileus, superior mesentericartery syndrome, peptic ulceration and pan-creatitis. Chronic gastrointestinal symptoms en-countered by people with spinal cord injuryinclude poorly localized abdominal pain, bloating,upper gastrointestinal symptoms such as nauseaand vomiting, incontinence and constipation. Thislist of symptoms which is partially attributable toautonomic dysfunction, exists alongside the po-tential for any other acute abdominal pathology,the diagnosis and treatment of which may often becomplicated by the reduction of visceral sensitivity(Bar-On and Ohry, 1995; Miller et al., 2001). Thesymptoms of lower gastrointestinal tract dysfunc-tion following spinal cord injury are more appar-ent to clinicians, typically presenting later withconstipation and fecal incontinence.

This chapter aims to give an overview of neuro-logical control within the gastrointestinal tract andalso to review the current understanding of thesymptoms and pathology behind the effect that spi-nal cord injury has on the gastrointestinal system.

Background

Bowel anatomy and innervation

The gastrointestinal tract from the oesophagus tothe rectum follows a similar structural pattern of atube whose lumen is formed by concentric layersof mucosa, submucosa, circular and longitudinalmuscle layers, and an outer serosal covering layer(Fig. 1). Between the muscular layers and beneaththe mucosa are collections of nerve cells that formplexuses (the submucosal Meissner’s and muscularAuerbach’s plexuses) that participate in the con-trol of gut peristalsis and secretion. Dependentupon the position in the gastrointestinal tract theselayers vary in thickness and complexity. This pat-tern is consistent between the gastrointestinaltracts of most vertebrates.

The term ‘neurogenic bowel’ relates to colonicdysfunction (constipation, fecal incontinence anddisordered defecation) following disruption ofnormal control, and is the largest contributor togastrointestinal symptoms following spinal cordinjury. The adult human large intestine consists of

a compliant tubular sac, approximately 1.5m inlength (Sinnatamby, 1999), which can be dividedanatomically into five parts; appendix, cecum,colon, rectum and anus (Fig. 2). Embryologically,the large bowel develops from two separate sourc-es: the proximal colon up to the transverse colonarising from the mid-gut, and the colon distal tothe mid-transverse colon, arising from the embry-onic hindgut. Proximally it commences at theileocecal valve and distally it ends with the analsphincter. The former is of little functional signif-icance, whereas the latter has obvious major phys-iological importance. The colon follows thegeneral structure of the gastrointestinal tract, withan inner circular smooth muscle layer and a thinouter longitudinal muscle layer that is gathered upinto thickened cords forming the taenia coli. Atthe distal rectum is the anal canal formed fromanal mucosa overlying two layers of muscle, theinternal and external anal sphincters. The internalanal sphincter is formed from a condensation ofthe inner circular smooth muscle and hence is notunder voluntary control. The external anal sphinc-ter is made up of a circumferential ‘voluntary’striated muscle band, which is continuous with thepelvic floor. These sphincters work in conjunctionwith the puborectalis muscle, which forms a slingaround the distal rectum and is tethered to thepubic symphysis to maintain the puborectal angle,a minor contributor to the maintenance of fecalcontinence. Tonic contraction of the internal analsphincter provides 80% of resting anal pressure(Schweiger, 1979). When the urge to defecateoccurs with rectal distension and puborectalisstretch, contraction of the external anal sphincterand puborectalis helps to maintain continence un-til there is a suitable moment to void. In additionto the voluntary control of external anal sphincterfunction, there is a reflex component, which can beexperimentally triggered by a cough or Valsalvamanoeuvre, and which serves physiologically tomaintain continence during episodes of raisedintra-abdominal pressure.

The enteric nervous system

The enteric nervous system controls the gastroin-testinal tract, via a network of sensory neurones

Fig. 1. The layers of the gastrointestinal tract. From Feldman’s GastroAtlas Online, with permission.

Fig. 2. Colon anatomy. From Feldman’s GastroAtlas Online, with permission.

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relaying information from the gut which in turncommunicates with a network of interneuronesand effector neurones to produce an effect on gutsecretion, blood flow and motor function. It hasbeen estimated that the enteric nervous systemcontains 80–100 million neurones (Furness andCosta, 1987) a similar number to that in the spinalcord itself (Goyal and Hirano, 1996). The entericnervous system can function independently of thecentral nervous system but the central nervoussystem plays a large role in coordinating gut func-tion. This has led to the concept of the brain gutaxis, with the ‘larger brain’ in the cranium and the‘mini brain’ in the abdomen. The central nervoussystem exerts its effect on the bowel via afferentand efferent sympathetic, parasympathetic and so-matic innervation (Sarna, 1991), which interactswith the intrinsic nervous system. An analogywould be of the enteric nervous system being likeconstant traffic running through a town, while thecentral nervous system is the system of trafficlights and roundabouts that controls the smoothflow of that traffic.

Nerve cell bodies in the enteric nervous systemare grouped into small ganglia that are connectedto each other by nerve processes, producing twomain plexuses that constitute this intrinsic nervoussystem. The myenteric (Auerbach’s) plexus is welldeveloped, made up of unmyelinated fibres andpostganglionic parasympathetic cell bodies andlies between the longitudinal and circular musclesof the gut and coordinates peristalsis. It suppliesthe mucosa with secretomotor innervation and hasconnections with the sympathetic ganglia (Fig. 3).The submucosal (Meissner’s) plexus lies on theluminal side of the circular muscle in the submu-cosa together with connective tissue, glands andsmall vessels. It conveys local sensory and motorresponses to Auerbach’s plexus and to the centralnervous system (Stiens et al., 1997). It also has arole in the control of secretions, endocrine cellsand the submucosal vasculature. The exact signal-ling controls between gut neurones have yet to befully elucidated. Neurones have been shown tocontain the classical adrenergic and cholinergicneurotransmitters, together with putative trans-mitters such as peptides (e.g., substance P), aminoacids [e.g., glutamate, g amino-butyric acid

(GABA)] and smaller molecules (e.g., nitric oxide)(Olsson and Holmgren, 2001). The role of eachtransmitter varies, in each region of the gut, de-pendent upon the interaction with other localtransmitters and receptor density on target cells(Schemann and Neunlist, 2004). A functional prin-ciple states that neuropeptides often act asneuromodulators, as opposed to direct neuro-transmitters, in the gut. Enteric nervous systemneurones can be broadly classed into intrinsic af-ferents, interneurones and motor neurones (Lynchet al., 2001). The intrinsic afferents form the sen-sory limb of motor and secretory reflexes, project-ing into the interneurones of both plexuses.Excitatory motor and secretory neurones projectto circular muscle locally or rostrally, whereas in-hibitory neurones project caudally. This pattern ofproximal relaxation with local and distal contrac-tion helps coordinate churning and peristaltic gutcontractions. The afferent and motor neurones arelinked by interneurones, forming multi-synapticpathways that fine-tune gut secretion and gut mo-tility. While the enteric nervous system coordinatessegmental motility and some peristaltic movement,global colonic movements are triggered by spinalcord-mediated reflexes, acting via pelvic nerves.

Parasympathetic innervation

Parasympathetic autonomic innervation from thevagus (10th cranial nerve), originating from thebrainstem, supplies the gastrointestinal tract fromthe esophagus up to the colonic splenic flexure(Devroede and Lamarche, 1974) (Fig. 4). Para-sympathetic innervation to the splenic flexure, de-scending colon and rectum arises from the sacral(S) spinal roots S2–S4 that form the pelvic plexusand give rise to the nervi erigentes. In man, theprecise point at which the vagal innervation to thebowel stops and pelvic innervation starts is asource of controversy with some authors describ-ing vagal innervation down to the rectum, andothers reporting pelvic nerve branches travellingproximally to innervate the entire colon (Stienset al., 1997). The parasympathetic supply to theinternal anal sphincter is derived from the sacralspinal cord and joins the pelvic nerves. It relaxes

Fig. 3. Layers of the submucosal and myenteric plexuses. From Feldman’s GastroAtlas Online, with permission.

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the sphincter by the effect of pre-ganglioniccholinergic neurones exciting nicotinic and mu-scarinic receptors.

Sympathetic innervation

Preganglionic axons from thoracic (T) nerve rootsT6–T12 pass via rami communicantes to the sym-pathetic chain and travel via thoracic splanchnicnerves, synapsing at the celiac and superior mes-enteric plexus, supplying small bowel and the as-cending colon. Sympathetic innervation distal tothe splenic flexure to the upper rectum arises fromlumbar (L) nerve roots L1–L3. The nerves travelto the sympathetic chain and via the lumbarsplanchnic nerves, synapse at the inferior mesen-teric ganglia. The supply then follows the arterialblood supply to the left colon. The lower rectumand anal canal sympathetic supply is derived fromthe aortic and lumbar splanchnics which unite toform the hypogastric plexus, giving off the pre-sacral branches to form the sacral plexus, whose

postganglionic fibres innervate the rectum andanus. The internal anal sphincter has sympatheticsupply from the inferior mesenteric ganglion viathe hypogastric nerves. Sympathetic tone is exci-tatory to the internal sphincter musculature andhelps to maintain continence.

Colonic function, reflexes and control

The colon serves several functions: stool storage;stool propulsion when socially appropriate; theprovision of an environment for symbiotic bacte-rial growth; and even absorption of amino acids,short chain fatty acids and fluid. Following thedisruption of supraspinal control systems, thedominant autonomic tone is inhibitory to colonicpropulsion, which contributes towards constipa-tion. The understanding of these neural mecha-nisms and their aberrant behaviour after spinalcord injury may provide a basis to treat symptoms.

Normal patterns of colonic contraction can beclassified into three groups: (i) individual phasic

Fig. 4. Autonomic innervation of the colon. From Feldman’s GastroAtlas Online, with permission.

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contractions (of long or short duration), whichhave the effect of kneading and mixing stool; (ii)organized groups (migratory and non-migratorymotor complexes), which are propulsive in smallregions of colon; (iii) giant migratory contractions,which produce movements of content and expelstool during defecation (Christensen, 1991; Sarna,1993). In addition, distension of the wall of thecolon causes proximal muscle contraction anddistal relaxation, resulting in caudal propagation.

The colon has intrinsic rhythmic slow waveactivity that is thought to be important in encour-aging fluid reabsorption from the colonic mucosa.The origin of this activity varies and the

mechanisms controlling it are inadequately under-stood. Enteric reflexes, with serotonin as theneurotransmitter, stimulate peristalsis (Hansen,2003), as demonstrated by its continuation afterthe gut is removed from the body. These entericreflexes also contribute to the colonic slow waveactivity (Olsson and Holmgren, 2001). Recentstudies have suggested that interstitial cells ofCajal, found in the submucosa, intra- and inter-muscle layers of the gut, especially in the right co-lon, generate spontaneously active pacemakercurrents (Horowitz et al., 1999; Takaki, 2003).These ‘pacemaker’ cells in the colon are likely tohave profound effects on colonic smooth muscles.

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One of the specialized aspects of gastrointestinalmotility is the gastrocolic reflex. This reflex causesincreased small bowel and colonic propulsive mo-tility, and is mediated by neural and endocrinemechanisms. The neural substrates comprise cho-linergic motor neurones which are activated by theingestion of a meal (Connell et al., 1963). Thestomach is not the source of the stimulus as theresponse is triggered if food bypasses the stomach(by a feeding tube) and enters the duodenum di-rectly (Snape, Jr. et al., 1979; Christensen, 1991)and even by the psychological anticipation orsmell of food. The proposed mechanisms for thereflex include a role for central vagal mediation,possibly long enteric reflexes via the enteric nerv-ous system and humoral components related torelease of cholecystokinin, gastrin and motilin(Christensen, 1991; Saltzstein et al., 1995). Studiesin spinal cord-injured subjects have demonstrateddiffering recorded responses of the reflex, eithershowing it to be intact or absent (Glick et al.,1984). The reasons for this discrepancy may simplybe methodological, and in the clinical setting atleast the reflex is frequently used as a managementtool for treating constipation in cord-injured peo-ple. By ingesting food or a calorific drink approx-imately 30min before bowel management isplanned, reflex colonic contractions can aid stoolemptying (Longo et al., 1989). Fatty foods tend tohave larger and longer action on the reflex com-pared to protein or carbohydrate-dominant foods(Spiller, 2000).

Pelvic sacral reflexes are excitatory, with the re-flex arc conveyed from the sacral spinal cord seg-ments in the conus, to and from the colon via pelvicnerves. Parasympathetic stimulation of splanchnicnerves leads to a significant propulsive colonic re-sponse. From the colon, enteric nerves trigger thisreflex in response to stretch or dilation, reinforcinginherent colonic enteric-mediated peristalsis. Therectocolic reflex is another pelvic reflex that is trig-gered by mechanical or chemical stimulation in therectum or anus. It also produces colonic peristalsis,which brings stool down to the rectum. Stoolentering the rectum can then trigger the recto-analinhibitory reflex, a reflex relaxation of the internalanal sphincter in response to rectal distensionallowing expulsion of stool from the rectum. The

properties of these two reflexes are exploited inbowel management, to aid defecation, as long asthe spinal cord lesion is above the level of the conus.

Spinal cord injury results in disruption of theinteraction that normally occurs between the in-trinsic and extrinsic nervous system. Studies look-ing at the effect of spinal cord and peripheral nervelesions on the enteric nervous system have shownganglion cell loss and secondary Schwanncell proliferation in the colon (Devroede andLamarche, 1974; Devroede et al., 1979). Onceestablished, recovery of this disruption is restrict-ed. However, recent work with enteric glia cells hasshown that they have the potential to aid axonalgrowth (Jiang et al., 2003) and may be a source offuture regenerative therapies.

Gastrointestinal dysfunction with acute spinal

cord injury

In the acute phase of spinal cord injury, tonic ex-citatory input to ganglionic and enteric neurones islost and the neurones are less excitable, resulting inoverall lack of neural input to the gut. Commonlyencountered complications in this acute period of‘spinal shock’ include ileus, gastric dilatation, pep-tic ulcer disease, pancreatitis and superior mesen-teric artery syndrome (Tibbs et al., 1979; Goreet al., 1981; Berlly and Wilmot, 1984). The lattercomplication, which is compression of the thirdpart of the duodenum by the superior mesentericartery, tends to occur due to alterations of vasculartone to the viscera. This spectrum of ‘spinal shock’abnormalities tends to settle over a varying periodof days to weeks after the initial injury (Ditunnoet al., 2004). Peptic ulceration in the acute settingis thought to occur as a result of unopposed para-sympathetic activity from the vagus and transientloss of sympathetic innervation, resulting in raisedgastrin levels and a reduced pH (Pollock andFinkelman, 1954; Bowen et al., 1974; Tanakaet al., 1979). Analgesic and corticosteroid admin-istration following spinal injury may exacerbatethe condition. These drugs have also been impli-cated in the prevalence of pancreatitis in acute spi-nal cord injury. Other causes of pancreatitis whichhave been described include autonomic imbalance

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causing over stimulation of the sphincter of Oddi,hypercalcaemia due to immobilization and thick-ened pancreatic secretions (Hyman et al., 1972;Carey et al., 1977; Maynard and Imai, 1977).

With regard to lower gut function, animalstudies have shown decreased colonic motilityimmediately after thoracic cord transection(Meshkinpour et al., 1985). Inhibitory reflexesbelow the lesion are lost and there is a loss offacilitation from above. This loss of supra-lesionalinput to the bowel in large part explains thereduced transit through the bowel that is found.Ileus occurs almost immediately in patients withthoracolumbar cord injury but can be delayed inhigh thoracic and cervical nerve injuries. However,it is most commonly seen in patients with higherlesions when cord injury occurs at or above thelevel of visceral innervation, namely T5.

Gastrointestinal dysfunction with chronic spinal

cord injury

Upper gastrointestinal symptoms

Little work has been published on the extent andmechanisms of upper gastrointestinal dysfunctionaffecting cord-injured people, and much of it iscontradictory. Mild upper gastrointestinal symp-toms have been reported to affect a third of cord-injured people (Lu et al., 1998). Heartburn anddysphagia have been reported in 61 and 30%,respectively, of injured individuals, which is ofgreater prevalence than in matched controls. Thissymptom-burden is associated with high levelsof endoscopic and histological evidence of es-ophagitis (Stinneford et al., 1993). Oesophagealmotility studies also show abnormal slow waveperistaltic propagation, the equivalent of theslowed motor abnormalities seen further downthe gastrointestinal tract. The cause and relevanceof these findings remains unknown.

A high prevalence of hiatus hernia is found afterspinal cord injury, which appears to be related to areduction of diaphragmatic motion, muscle atro-phy and weakening of fibrous tissue at the gastro-oesophageal junction due to chronically raisedintra-abdominal pressures. Treatment of hiatushernia and other reflux type symptoms is along the

same lines as in able-bodied patients. The focus ison antacids (alginates), acid suppressants (hista-mine (H)2-receptor antagonists and proton pumpinhibitors) and motility stimulating agents (dom-peridone, metoclopramide).

Nausea and vomiting related to gastric dilata-tion and ileus are common symptoms in the acutespinal cord injury setting. Both tend to improve asspinal shock resolves. Nausea, however, can alsobe a persistent and troublesome symptom in thelonger term (Stone et al., 1990a; Glickman andKamm, 1996). There are a number of possiblecauses for these symptoms: gastric stasis (second-ary to denervation), gallstone disease (which ismore prevalent in spinal cord injury patients) andconstipation (Camilleri, 1990; Pfeifer et al., 1996;Tola et al., 2000; Cubeddu, 2003).

Gastric emptying is delayed after spinal cordinjury (Lu et al., 1998; Kao et al., 1999). Vagalparasympathetic innervation to the upper gastro-intestinal tract originates from the brainstem andits control tends to be preserved in spinal cord in-jury. However, the sympathetic outflow arisesfrom the thoracic lumbar cord (T5–T12) and itsloss with a lesion about this level results in exces-sive splanchnic sympathetic activity from the tho-racic cord, and hence gastroparesis (decreasedgastric emptying). After lower level injuries, thereis no loss of supra-spinal influence and the auto-nomic hyper-reflexia and delayed gastric emptyingis not seen (Fealey et al., 1984; Nino-Murcia andFriedland, 1992). There is some evidence to sug-gest that gastric emptying tends to return towardsnormal over time as a degree of autonomic nerv-ous system-mediated homeostasis and regulationreturns in long-term spinal cord-injured individu-als (Segal et al., 1987).

Orocecal transit times are delayed after spinalcord injury (Chen et al., 2004). Using a non-invasive hydrogen breath test method, these au-thors have shown that cord-injured subjects haveoverall mean orocecal transit times of 180min com-pared to 98min in controls. The net result of thisprolonged small bowel transit time, is to predisposeto disturbance of digestion and bacterial over-growth which can exacerbate nausea. Nausea hasalso been attributed, in part, to the higher incidenceof gallstone disease found in cord-injured patients

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(Ketover et al., 1996). Studies looking at the gall-bladder following spinal cord injury, have shownreduced contractility and this has been postulatedas possible reason for the increase in incidence(Fong et al., 2003). Gallstones have been implicatedin causing non-specific symptoms such as nauseaand bloating in cord-injured people (Moonka et al.,1999). However, given the prevalence of gallstonesafter spinal cord injury, the presence of vague ab-dominal symptoms that occur should not be putdown to the presence of gallstones alone (Moonkaet al., 2000). Gastric or colonic pathology should beconsidered in the diagnostic workup.

Pain

Abdominal pain experienced by people after spinalcord injury needs to be carefully investigated toexclude common abdominal pathology (such asneoplasm, peptic ulceration and ischemia), as di-agnosis in this population can be fraught with dif-ficulty (Ingersoll, 1985; Bar-On and Ohry, 1995).Chronic neurological visceral pain does affectcord-injured people but the extent of this problemis poorly documented and understood partly as aresult of poor classification (Beric, 2003). Studiesquote the prevalence of chronic visceral pain asbetween 3 and 10% (Cardenas et al., 2002). Al-though not as common as musculoskeletal or ne-uropathic pain, visceral pain is perceived as beingof higher intensity (severe/excruciating) comparedto musculoskeletal pain. Visceral pain tends to de-velop months or years after injury, compared withother pain types that more likely have an earlyonset. This probably results following the devel-opment of visceral organ problems associated withspinal cord injury such as constipation, bladderinfection and renal calculi. Visceral pain may bedue to normal afferent sensation via the sympa-thetic and vagus nerves in paraplegics, or vagalinnervation alone in tetraplegics (Richards, 1992;Siddall and Loeser, 2001).

Lower gastrointestinal symptoms and pathology

Colorectal dysfunction following spinal cordinjury is the major source of gastrointestinal

symptoms in these patients. Constipation, fecalincontinence and incoordinated defecation are themost frequently reported symptoms. The incidenceof constipation reported in the literature rangesfrom 20 to 58%. This discrepancy in the reportedfigures can be attributed to a disparity betweendefinitions of constipation and bowel managementpractices used between spinal injury units. Incon-tinence to feces and flatus is reported to affect upto 75% of the spinal cord injury population al-though the percentage of cord-injured people inwhom this occurs on a regular basis (more thanmonthly) is only approximately 15% (Krogh et al.,1997). However, the threat of episodes of fecal in-continence causes psychological stresses to cord-injured people and their carers and can result insocial isolation.

Colonic diverticulae are found more frequentlyand at younger ages in the spinal cord injury pop-ulation compared with controls (Gore et al., 1981).This may be due to the contribution of the highpressures that uncoordinated segmental peristalsiscan produce and of chronic intraluminal disten-sion (Gore et al., 1981). Hemorrhoids are alsocommon with up to three-quarters of cord-injured people having the problem (Stone et al.,1990a).

Upper versus lower motor neurone lesions: effect onthe bowel

When describing symptoms attributable to boweldysfunction after spinal cord injury, an under-standing of the effect that the level of injury has onthe bowel is necessary, as this determines the pat-tern of colonic motility. Upper motor neuronespinal cord injury lesions occur above the level ofthe conus medullaris, which in adults lies at thelumbar (L)1,2 level. The colon in these cases isdescribed as ‘spastic’ with increased colonic walland striated external anal sphincter muscle tone.Baseline colonic activity is higher in this groupcompared to controls (Aaronson et al., 1985).Rectal tone is high (Krogh et al., 2002), resultingin a reduced capacity to hold stool and thereforeincreasing the risk of fecal incontinence episodes.This gives rise to poorly coordinated peristalsis,with excessive segmental and reduced propulsive

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peristalsis. The resulting slow whole gut transitresults in constipation that is often exacerbated bychanges in puborectalis muscle function. Evacua-tion of feces is achieved by triggering reflex def-ecation either by mechanical (digitation) orchemical means (suppositories or enemas).

Lower motor neurone lesions occur with injuriesat the level of the conus, cauda equina or pelvicnerves resulting in the disruption of parasympa-thetic innervation to the bowel. Loss of parasym-pathetic control results in a flaccid bowel and lowinternal anal sphincter tone. There is also an ab-sence of spinal cord-mediated reflex peristalsis, andhence stool propulsion occurs with intrinsic my-enteric plexus-triggered segmental peristalsis. Withthe loss of external anal sphincter control and theabsence of internal anal sphincter parasympatheticsupply, the anal sphincter complex resting tone islow. This low pressure makes cord-injured peoplesusceptible to passive fecal leakage. This tendencyis exacerbated by the associated loss of rectal tone,resulting in a capacious rectum full of stool. Man-ual removal of stool, aided by increases in intra-abdominal pressure (such as with a Valsalva) is themainstays of management of such people.

Incoordinate anal sphincter function

There are a number of reports in the literature ofabnormal anorectal physiology in spinal cord-injured people. Resting sphincter tone (mainly areflection of internal anal sphincter function) isreduced in cord-injured people compared to con-trols, and is maintained mainly by internal analsphincter activity possibly due to tonic excitatorysympathetic discharge (Lynch et al., 2000). TheValsalva manoeuvre causes a rise in intra-abdom-inal pressure that is thought to stimulate pelvicfloor tension receptors into triggering reflex exter-nal anal sphincter contraction (MacDonagh et al.,1992). In able-bodied individuals, a cortically me-diated pathway relaxes the external anal sphincterduring straining to defecate. With upper motorneurone lesions where the reflex pathway is intactbut the supra-lesional input is absent, Valsalvamanoeuvres for bowel emptying may actuallyworsen attempts to evacuate stool, as the externalanal sphincter tone increases on straining. The

recto-anal inhibitory reflex described above ispresent after spinal cord injury but differs fromcontrols in that it can be triggered with lower vol-umes compared to controls. It has been hypoth-esized that the cause of this could be decreasedrectal compliance (a less distensible rectum) re-sulting in lower threshold for stimulating the reflex(Meshkinpour et al., 1983; Glick et al., 1984). Thiscombination of a less distensible rectum and reflexanal relaxation contributes towards triggering ep-isodes of fecal incontinence in spinal cord injury.

Constipation and incontinence

Constipation is common after spinal cord injury(Glickman and Kamm, 1996). The frequency ofconstipation is affected by the level of injury, withup to three-quarters of quadriplegics being affect-ed, falling to a third in paraplegics with lesionsbetween the T10 and L2 cord segments (De Loozeet al., 1998). This is due to delayed colonic transit,disordered evacuation and changes in visceral sen-sitivity. Investigating and researching constipationis difficult since imaging and measuring bowelmotility is not straightforward. However there aretechniques available: radionucleotide and radio-opaque marker studies (van der Sijp et al., 1993);solid state pressure catheters (Fajardo et al., 2003);balloon distension and Barostat recorders(Bruninga and Camilleri, 1997). Using these tech-niques, it is possible to understand the patient’sbowel motility pattern and allow therapeutic in-terventions to be directed appropriately. Moststudies show overall colonic transit times to beprolonged following spinal cord injury (Menardoet al., 1987). Some studies have suggested that thisdelay in colonic transit is segmental, most mark-edly in the distal colon and rectum (Menardoet al., 1987; Beuret-Blanquart et al., 1990). Bycontrast, others show a pan-colonic increase intransit times (Keshavarzian et al., 1995). In theclinical setting, groups of cord-injured patientsbenefit from oral laxatives in addition to rectalmedications and reflex stimulation, indicating areduction in whole colon motility. Poor coordina-tion of the anal sphincter complex described pre-viously, leading to outlet obstruction, can alsocontribute towards constipation. The importance

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of a good bowel care programme, to prevent con-stipation, is underlined by some studies that showhigh levels (73%) of megacolon (dilated colon sec-ondary to constipation) in people with spinal cordinjury (Harari and Minaker, 2000).

Incontinence is a threat to cord-injured peopledue to a combination of factors — lack of aware-ness of rectal fullness, overflow following poorevacuation management, and weak sphincter func-tion as described above (particularly in lower mo-tor neurone lesion patients). Poor control of flatusand fecal leakage can lead to physical, psycholog-ical, sexual and social problems (DeLisa andKirshblum, 1997). Effective bowel managementstrategies to prevent these symptoms are impor-tant for the well being of cord-injured people.Regular evacuation and preventing loose stoolformation by ensuring an adequate fibre intake,preventing gastrointestinal infections and regulat-ing diet are core techniques that will be discussedfurther later in this chapter.

Therapies that exacerbate symptoms

Spinal cord injuries cause dysfunction to manyorgan systems and the treatment of these can resultin adverse effects on the bowel. Side effects fromprescribed medications are very common. Anti-cholinergics used in the treatment of bladderdyssynergia, opiates and anti-spasmodics slowbowel transit and dry the stool thereby exacerbat-ing the constipation. Broad-spectrum antibioticscan cause diarrhea by altering the balance of com-mensal enteric flora in the gut. Additionally, ther-apies used in bowel management can exacerbatesymptoms. Anal digitation, evacuation and rectalmedication administration can cause local traumapotentially irritating hemorrhoids and predispos-ing towards anal fissure and solitary rectal ulcerformation. All treatments and therapies shouldtherefore be evaluated for side effects, and vigi-lance observed for their onset.

Bowel management

Early implementation of a regulated-controlledbowel management program is held to be the bestpractice for patients after their injuries. During the

phase of spinal shock when peristalsis is reduced,digital or manual evacuation of stool is required(Halm, 1990). When bowel function stabilizes, aregular bowel care program can be initiated. Cur-rent programs vary between institutions, wheremanagement is often empirical, given the lack ofwell-designed controlled trials (Wiesel et al., 2001).There have been published proposed bowel pro-grams (Correa and Rotter, 2000) but none havebeen universally adopted and for many cord-in-jured people, bowel management regimens are farfrom ideal. One series reported 41% of cord-in-jured individuals spending more than 1 h on bowelevacuation (Harari et al., 1997) and some peoplereport having to spend 3 h or more a day on theirbowel care. It has been quoted that the ideal bowelmanagement regime should be self controlled andspontaneous, with or without oral medication,performed at least once every 2 days, and com-pleted within 30min to result in effective evacua-tion without complication and this was achievedby only 32% of subjects in one study (Han et al.,1998). In the clinical setting, it is accepted thatthere have been improvements in bowel care overthe last two decades although hard evidence toback this up is scarce.

The foundation of good bowel managementprogram involves the implementation of a regularroutine, which addresses the specific issues such asconstipation, incontinence and functional mobility,using the appropriate interventions. A bowel careroutine should be timed to coincide with colonicgiant migratory contractions, to take advantage ofany stool propulsion. Giant migratory contrac-tions tend to occur after meals and in the morning,on waking. This regime should take into accountthe person’s social, sexual, cultural and vocationalbeliefs. Also, the question of functional mobilityneeds to be addressed, ensuring carers and appro-priate equipment such as commode chairs areavailable. Logistical issues such as access to toiletfacilities, are fundamental but often overlooked.

Diet

Simple dietary measures can benefit bowel man-agement. Adequate fluid intake aids gut transit bysoftening stool. In people with spinal cord injury,

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fibre does not increase colonic transit time but actsto absorb excess water and to keep the stool softand formed, thereby reducing the problems of in-continence (Banwell et al., 1993).

Laxatives

There are several groups of medications that canbe taken orally to aid bowel movements or to re-lieve constipation. Lubricants and stool softeners(e.g., docusate sodium, liquid paraffin and mineraloils) ‘grease’ the stool and make passage throughthe bowel easier. Bulking agents (e.g., isogel gran-ules, ispaghula husk, methylcellulose, psyllium)are indicated if dietary fibre cannot be adequatelyingested. They act by absorbing water in the gutthereby softening and bulking stool. Fluid intakemust be adequate when on these treatments, al-though this can be difficult to achieve in peoplewith bladder management difficulties. Bloatingand flatulence can be problematic but tend to set-tle if people can persevere with the treatment.

Indigestible carbohydrates (lactitol, lactulose,polyethylene glycols) and salts [e.g., magnesium(Epsom) salts] act osmotically to draw fluid intothe colon. Stimulant laxatives (bisacodyl, da-nthron, senna) induce and augment peristalticmovement of the bowel, thus aiding stool progres-sion and reducing the time allowed for water andelectrolyte resorption. Senna is broken down inabsorbable anthraquinones which directly stimu-late the myenteric plexus. Oral stimulant laxativescan all cause the side effects of cramps, diarrheaand dehydration. Their chronic use can lead tocolonic mucosal staining due to macrophagephagocytosis of pigments derived from laxatives(melanosis coli) (Menter et al., 1997). There is noevidence in cord-injured people that their alreadyvery slow transit is further compromised by reg-ular use of these agents. The delay of onset forthese laxatives is 1–2 days, except for magnesiumsalts that have a faster onset of action of about 4 h(Frisbie, 1997; Amir et al., 1998). The attraction ofosmotic agents is their speed of action and theirability to be titrated, done according to stool con-sistency. Care must be taken however to avoid tooloose a stool, especially in people with sphinctercompromise, as they may lead frequent episodes of

fecal incontinence. Senna may be used as an oc-casional night-time dose to ‘prime’ the bowel for amorning evacuation. Combinations of the differ-ent classes of laxatives often deliver the desiredresults. For example, a regular bulking agent witha stimulant laxative can lead to the regular evac-uation of soft, formed stools.

Suppositories and enemas

Glycerine suppositories are used to stimulate rectalcontraction due to its irritant and hyperosmoticaction and result in bowel movements in15–30min. Bisacodyl can be administered in sup-pository form and it acts on sensory afferentnerves of the mucosa producing a parasympathet-ically mediated reflex peristaltic contraction of theentire colon (Stiens et al., 1998), which aids bowelemptying and reduces time spent on bowel man-agement (Frisbie, 1997). Saline, water or docusatesodium enemas can be used. These work by trig-gering reflex colonic peristalsis, lubricating and inthe case of docusate softening the stool. Auto-nomic dysreflexia is the condition of abrupt onset,potentially lethal hypertension in people with spi-nal cord injury above the level of T6 (see chaptersaddressing cardiovascular dysfunction, this vol-ume). It is caused by uncontrolled sympatheticdischarge triggered by any noxious stimulus andmany innocuous stimuli below the level of the le-sion. Common triggers of this condition relate tobladder and bowel distension or irritation (Adsitand Bishop, 1995). The maneuvers involved withbowel management such as digitation, use of en-emas and evacuation can trigger autonomicdysreflexia particularly if there is local pathologysuch as anal fissure or rectal ulceration. Use oflocal anesthetic agents, such as lidocaine gel canreduce the incidence of attacks of autonomicdysreflexia during bowel management.

Prokinetic agents

Metoclopramide and domperidone are dopamineantagonists that increase the rate of gastric emp-tying and of small gut transit. They have no effecton colonic peristalsis and are most commonly used

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in the acute setting of spinal cord injury when try-ing to overcome the gastric dilatation and ileus thataccompanies spinal shock (Miller and Fenzl, 1981;Segal et al., 1987). Erythromycin is a macrolideantibiotic with prokinetic effects which is also usedin the acute setting to enhance transit through theupper gut (Clanton and Bender, 1999).

The parasympathomimetic drugs neostigmine,bethanechol, distigmine and pyridostigmine, allenhance parasympathetic effects on the gut to in-crease motility but are rarely used in the clinicalsetting for this purpose, due to their side effects.They may have a role in treating the rare situationof acute pseudo-obstruction of the gut (Ogilvie’sSyndrome) which is seen in some cases after acuteinjury, related to sudden loss of autonomic tone tothe viscera (Delgado-Aros and Camilleri, 2003).Cisapride was used for its prokinetic properties onthe upper and lower gut and increased colonictransit speed (Binnie et al., 1988; Geders et al.,1995; Longo et al., 1995) but has been withdrawnfrom clinical use because of an association withfatal cardiac arrhythmias (Prescrire Int, 2000;Cubeddu, 2003).

Mechanical devices and surgical interventions

Anal plug devices can be utilized to prevent leak-age of flatus and feces (Kim et al., 2001) for cord-injured people with lower motor neurone lesions,who often have an atonic anal sphincter. They arebest tolerated by people who have no preservationof anal sensation, but tend to be inefficient if largevolumes of stool are being lost. Pulsed irrigationenemas have been used, in which a catheter withan inflatable retention cuff is passed into the rec-tum followed by a program of tap water pulses(Puet et al., 1997). This loosens and suspends stoolthat is removed via a conduit drain runningthrough the centre of the catheter. Antegrade con-tinence enemas require appendicocecostomies tobe surgically fashioned to deliver washout fluidinto the proximal colon to allow controlled dailyemptying. Water or saline is infused into thececum and passes through to produce bowel evac-uation minutes later (Malone, 2004). The tech-nique has been modified to allow radiological

(Chait et al., 1997) or endoscopic placement (DePeppo et al., 1999). These irrigation methods havebeen most studied in pediatric practice, especiallyin children with myelomeningocoele. While oftenefficient in the short term, infective and mechanicalcomplications around the tube entry site can beproblematic. Furthermore, there is evidence thatwith time, the irrigation method may become lessefficient, and indeed the antegrade continence en-ema openings in the abdominal wall frequentlystenose (McAndrew and Malone, 2002).

Severe refractory constipation, prolonged bowelcare time, fecal incontinence and chronic peri-analulcers are reasons for cord-injured people to con-sider stoma formation for their bowel care(Deshmukh et al., 1996; Pfeifer et al., 1996). How-ever, the decision to opt for surgery should not betaken lightly as there are issues of assessment ofthe current bowel care program, body image, life-style, and required nursing assistance to be takeninto account together with the high risks of surgeryin this group of patients. That said, the formationof a stoma (ileostomy or colostomy) has beenshown in several studies to improve the quality oflife for people who opt for this treatment option asit can simplify bowel management, reduce incon-tinence and bloating and increase independence(Stone et al., 1990b; Randell et al., 2001; Branaganet al., 2003). Choice of type and position of stomashould be assessed according to the person, de-pendent upon their colonic transit characteristicsand their mobility (Safadi et al., 2003).

Sacral anterior root stimulators have beenimplanted since 1977 (Brindley et al., 1986), orig-inally being used for functional electrical stimula-tion to control bladder emptying (Brindley andRushton, 1990; Binnie et al., 1991; Brindley, 1994).The implant consists of a subcutaneous radio-re-ceiver connected to S2, S3 and S4 nerve roots viatunnelled wires. Trains of high-frequency stimula-tion trigger complex, high pressure, phasic colonicand rectal contractions resembling peristalticmovements, which act to bring stool down distal-ly. Following stimulation, defecation may occur(Varma et al., 1986; MacDonagh et al., 1990;Varma, 1992) and indeed this procedure was foundto improve bowel management in addition tobladder care in some patients.

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Conclusion

Gastrointestinal symptoms and the required pro-cedures for management of the bowel in peoplewith spinal cord injury are very problematic anddistressing. Unlike the advances in limb and blad-der dysfunction, the understanding of the effects ofspinal cord injury on the bowel is still very poor.Improvement in the quality of life for this group ofpeople requires on-going basic clinical research inthis field. Greater understanding of the influenceof neural disconnection on the residual function ofthe gut (via the enteric nervous system) is needed.Specifically, the understanding of the role of pelvicreflexes in controlling evacuation and continence isrequired to offer the prospect of possible futureneuromodulation of these reflexes. Finally, under-standing of the quality of life implications of boweldysfunction and developments of simple means toremedy the socially isolating problems is required.The above necessitates a combination of labora-tory and clinical research, in addition to advancesin nursing care. All of this requires a greater pri-ority to be placed on the research and the clinicalagenda for spinally injured people.

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