Tolerance for Rectosigmoid Distention in Irritable Bowel Syndrome

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1 GASTROENTEROLOGY 199;98: Tlerance fr Rectsigmid Distentin in Irritable Bwel Syndrme WILLIAM E. WHITEHEAD, BEATE HOLTKOTTER, PAUL ENCK, RUPERT HOELZL, KIM D. HOLMES, JAMES ANTHONY, HARRY S. SHABSIN, and MARVIN M. SCHUSTER The Jhns Hpkins University Schl f Medicine and The Francis Sctt Key Medical Center, Baltimre, Maryland; Harvard University Schl f Medicine and Children's Hspital, Bstn, Massachusetts; University f Dusseldrf Department f Medicine, Dusseldrf, West Germany; and Max-Planck Institute, Munich, West Germany. Tw hyptheses were tested: (a) lwered tlerance fr balln distentin f the rectsigmid in patients with irritable bwel syndrme is caused by a psychlgical tendency t exaggerate the painfulness f any aversive stimulus, and (b) cntractins elicited by balln distentin are respnsible fr pain reprts. Tlerance fr stepwise distentin f a balln in the rectsigmid was cmpared with tlerance fr hlding ne hand in ice water in 16 irritable bwel patients, 1 patients with functinal bwel disrder wh did nt satisfy restrictive criteria fr irritable bwel, 25 lactse malabsrbers, and 18 asymptmatic cntrls. Cntractile activity was measured 5 cm abve and 5 cm belw the distending balln. Psychmetric tests were used t assess neurticism, anxiety, and depressin, and a standardized psychiatric interview was administered. Patients with irritable bwel syndrme had significantly lwer tlerance fr balln distentin but nt ice water, and balln tlerance was nt crrelated with neurticism r ther psychlgical traits measured. Rectsigmid and rectal mtility were als nt related t tlerance fr balln distentin. Bth hyptheses were rejected. A peripheral mechanism such as altered receptr sensitivity may be the cause f distentin pain in irritable bwel syndrme. Ritchie (1,2) first reprted that patients with irritable bwel syndrme (IBS) are mre likely than nrmal cntrls t reprt pain when a balln is inflated in the distal cln. His bservatins were replicated by mst ther investigatrs (3,4), but nt by Latimer et al. (5). Fielding (6) verified experimentally the cmmn clinical bservatin that patients with IBS are als mre likely than cntrls t reprt tenderness ver the distributin f the cln when the abdmen is palpated during physical examinatin. These bservatins suggest that IBS may be assciated with altered pain sensitivity at receptr sites in the cln. Hwever, the fllwing alternative hyptheses have been ffered t explain these data. 1. Latimer et al. (5) suggested that patients with IBS may have nrmal receptr sensitivity but may have a neurtic tendency t label as painful many smatic sensatins ther peple d nt call painful. One implicatin f this hypthesis is that IBS patients may reprt a lwer pain threshld r a lwer tlerance fr pain when ther types f aversive stimuli are presented. Ck et al. (7) tested this hypthesis by cmparing IBS patients with nrmal cntrls in an experiment in which electrical shcks f varius intensities were applied t the skin. Cntrary t the hypthesis f Latimer et ai., IBS patients had higher pain threshlds than nrmal cntrls. In the experiment described here, we sught t extend the bservatins f Ck et al. (7) by cmparing tlerance fr balln distentin f the cln with tlerance fr hlding a hand in ice water in patients with IBS and in cntrl grups f nrmal subjects and patients with lactse malabsrptin (LMA). 2. Ritchie (2) nted that inflatin f a balln in the cln may induce a cntractin that migrates dwn the cln; he suggested that the pain reprted by patients with IBS may be caused by cntractins at a site distal t the site f balln distentin. T test Abbreviatins used in this paper: DIS, Diagnstic Interview Schedule; FBD, functinal bwel disrder; IBS, irritable bwel syndrme; LMA, lactse malabsrptin. 199 by the American Gastrenterlgical Assciatin /9/$3.

2 1188 WHITEHEAD ET AL. GASTROENTEROLOGY Vl. 98, N.5 this hypthesis, we recrded cntractins at sites 5 cm abve and 5 cm belw the distending balln. Methd Participants included 16 patients with IBS, 1 patients with functinal bwel disrder (FBD), 25 patients with LMA, and 18 nrmal cntrls. Diagnstic criteria were as fllws. All subj ects were tested fr LMA by hydrgen breath test, and anyne whse hydrgen breath cncentratin increased by 22 ppm r mre within 3 h after ingesting a 5-g lactse meal was classified as LMA, regardless f presenting bwel symptms. Irritable. bwel syndrme was defined by self-reprt f pain that is relieved by a bwel mvement plus at least tw f the fllwing five symptms in the absence f a psitive lactse tlerance test r ther indicatin f a different disrder: lse stls at the nset f pain, mre frequent bwel mvements with the nset f pain, distentin f the abdmen, mucus passed by rectum, and frequent feeling f incmplete evacuatin. These criteria were adpted frm Manning et al. (8). Functinal bwel disrder was defined by a self-reprt f abdminal pain plus either cnstipatin r diarrhea in patients wh did nt satisfy the criteria fr IBS and wh als had negative lactse tlerance tests and n indicatin f ther disrders. This study was reviewed and apprved by the Francis Sctt Key Medical Center's Institutinal Review Bard. The cln prbe used in this study was built by R. Helzl's labratry. It cnsisted f a silicn rubber tube 1.4 cm in diameter with plastic segments situated at the tip and 15 cm belw the tip. Each plastic segment cntained a perfusin prt thrugh which cntractile activity culd be measured. The cln prbe als cntained a latex balln 4 cm in length attached circumferentially midway between the perfusin prts. Pressure waves in the cln were recrded n a Sensrmedics (Anaheim, Calif.) R611 plygraph at an amplifier gain f 5 mmhg/cm and a paper speed f 5 mm/s. The plygraph amplifier utput was digitized by a Tecmar (Cleveland, Ohi) analg-t-digital bard in an IBM-XT cmputer in 4-min blcks at a sampling rate f 4.27 Hz. Participants were asked t discntinue all medicatins fr at least 24 h befre the study, t fast fr 12 h, and t take a phsphate enema (Fleet's; Fleet Pharmaceuticals, Lynchburg,V A.) 2 h befre the test prcedure. After btaining infrmed cnsent, the cln prbe was lubricated with surgical lubricant and passed blindly t a depth f 25-3 cm. The psitin f the tube was nt checked radilgically fllwing insertin f the prbe, and it is pssible fr the tube t fld n itself in the rectum. Hwever, extensive experience with this large-diameter prbe shws that flding is rare and is detectable by extrusin f the prbe tip frm the rectum r the appearance f identical pressure tracings at bth perfusin prts. Twenty-five minutes were allwed fr the subject t becme habituated t the presence f the cln prbe. Tw 4-min baseline samples were then cllected. Ice Water Tlerance Subjects were asked t insert their right hands int a mixture f ice and water t the wrist jint and t hld them there fr as lng as pssible, and time befre withdrawing the hand frm the water was measured with a stp watch fr each subject. If the hand was nt withdrawn befre 4 min, the subj ect was instructed t withdraw the hand, and a value f 24 s was assigned. Balln Distentin Tlerance After the subj ect withdrew the hand frm the ice water, a 5-min recvery perid was allwed. The balln was then distended in a stepwise fashin by adding 2 ml f air every 3 min. Mtility was recrded fr 4 min after infusing 1 ml f air r the maximum vlume the subj ect tlerated if this was <1 mi. Unless this represented the subject's maximum tlerable vlume, additina12-ml increments f air were added at 3-min intervals up t a maximum f 2 mi. The maximum tlerable vlume was defined as the vlume at which the subject requested terminatin f the prcedure because f pain. If the subject did nt reprt pain, a value f 2 ml was assigned. At the cnclusin f the prcedure, the air was withdrawn frm the balln and measured t insure that n leak had ccurred t invalidate the test. Psychmetric Tests Subjects cmpleted a battery f psychmetric tests, including the NEG Persnality Inventry (9). This psychmetric test is scred fr three factrs-neurticism, extraversin, and penness t experience. The neurticism scale is described by the test develpers as measuring emtinal lability. Subjects als cmpleted the trait scale f the Spielberger State-Trait Anxiety Inventry (1) and the Beck Depressin Inventry (11). Psychiatric Diagnses The Diagnstic Interview Schedule (DIS) (12) was used t assign psychiatric diagnses in a ttal f 48 subjects wh cnsented t be interviewed. This included 1 nrmal cntrls, 13 IBS patients, 6 FBD patients, and 19 LMA patients. N subject wh was asked refused the DIS interview, but it was nt always pssible t arrange fr a separate 2-h appintment t.cnduct the DIS interview because sme patients lived lng distances frm the hspitai. Interviews were cnducted by fur lay interviewers wh had als administered the DIS interview in the East Baltimre Epidemilgy f Mental Illness study (13). They were trained and supervised by ne f the authrs (I.A.). Diagnses were assigned using the same cmputer algrithm used in the East Baltimre study. Data Analysis Parametric statistics culd nt be used t analyze tlerance fr balln distentin r tlerance fr ice water because the data were skewed (Figures 1 and 2). This ccurred because artificial ceilings were placed n the tlerance measures. Cnsequently, each patient grup was cmpared with the nrmal cntrl grup by Mann-Whitney

3 May 199 TOLERANCE FOR RECTOSIGMOID DISTENTION IN IBS 1189 DISTENTION (ml) 2 I- 15 -& 1 5 Figure 1. Tlerance fr bal- ln distentin f the rectsigmid cln in IDS, FDD, LMA, and asymptmatic cntrls (NOR). Bxes represent mean andse. IBS -1t O -B- {t- FBD LMA NOR U statistic, and Spearman rank rder crrelatins were used t examine the crrelatins between variables. Mtility tracings were first screened visually t exclude blcks f data cntaining mre than 1 s f mvement artifact. The digitized data were then scred by a cmputer pattern recgnitin prgram that emulates visual scring (14). This prgram yields a mtility index fr each 4-min segment f data. The mtility index is defined as the sum f the areas f all waves divided by recrding time in secnds. These mtility indices were transfrmed t lg values s that the assumptins f parametric statistical tests culd be satisfied and were then entered int a tw-way analysis f variance with diagnstic grups as a between-subjects factr and cnditins (baseline vs. balln distentin) as a withinsubjects factr. Between-grup differences in mtility were als tested by t-tests with Bnferrni crrectin fr multiple cmparisns fr each baseline perid and during balln distentin. The frequency f psychiatric diagnses were tested by Fisher's exact prbability tests, and between-grup differences in psychmetric inventry scres were tested by t-test with Bnferrni crrectin fr multiple cmparisns. An a level f.5 was used fr all statistical tests. COLD TOLERANCE (sec) tr 2 * 15 i 1 5 f- Figure 2. Tlerance fr hlding a hand in ice water in IDS, FDD, LMA, and asymptmatic O L ~ ~ cntrls - - -( N-O Bxes -R ~ - represent mean and ~ IBS FBD LMA NOR SE.

4 119 WHITEHEAD ET AL. GASTROENTEROLOGY Vl. 98, N.5 Table 1. Demgraphic Characteristics f Grups Nrmal IBS FBD LMA N. f subjects Age (yr)" 38.2 (9.3) 37.7 (13.) 46. (16.) 39.3 (13.7) / Male % White "Standard deviatin in parentheses. Results Characteristics f study grups are given in Table 1. There were n statistically significant differences amng grups in age, gender, r racial cmpsitin. Figure 1 shws grup differences in tlerance fr balln distentin. The IBS grup had significantly lwer tlerance fr balln distentin than the nrmal cntrl grup (Mann-Whitney U = 128, P <.5). Hwever, n ther grup was significantly different frm nrmal cntrls. Figure 2 shws grup differences in tlerance fr ice water. Cntrary t the hypthesis f Latimer et ai., paired cmparisns failed t shw any significant differences between patient grups and nrmal cntrls. The LMA patients tended t have lwer tlerances fr ice water than cntrls fr unknwn reasns. Psychmetric test scres are given in Table 2. Anxiety and depressin scres were significantly elevated in patients with IBS and patients with FBD cmpared with nrmal cntrls. Hwever, IBS patients were nt significantly different frm nrmal cntrls n the neurticism scale f the NEO Persnality Inventry (t(31) = 1.8, P >.5). When the DIS was used t assign psychiatric diagnses (Table 3), there was a tendency fr a larger prprtin f IBS patients (6 f 13) and FBD patients (3 f 6) t be assigned psychiatric diagnses (primarily depressin) cmpared with nrmal cntrls and with ppulatin estimates fr Baltimre (13). Hwever, these differences were nt statistically significant because f the small number wh were tested with the DIS. These trends are cnsistent with the psychmetric data shwing elevated levels f depressin and anxiety in IBS patients, and suggest that the elevated psychmetric test scres represent an excess incidence f diagnsable psychiatric disrder. Table 3. Psychiatric Diagnses Made by Diagnstic Interview Schedule IBS FBD LMA Nrmal Majr depressin r biplar disrder Generalized anxiety disrder Phbias Other psychiatric disrders ;,,; 1 psychiatric disrder 6/13 3/6 8/19 2/1 The effects f balln distentin n rectsigmid and rectal mtility are shwn in Table 4. Analysis f variance f the lg-transfrmed rectsigmid mtility data shwed that the main effect fr grups (F(3,64) = 2.77, P <.5) and the interactin between grups and experimental cnditins (F(6,128) = 4.4, P <.5) were significant, but the main effect fr cnditins was nt significant (F(2,128) = 1.86, P =.6). A similar analysis f the rectal mtility data shwed a significant main effect fr grups (F(3,56) = 2.92, P <.5) but nt fr experimental cnditins (F(2,112) = 2.86, P >.5) r fr the interactin between grups and cnditins (F(6,112) = 1.15, P >.1). Paired t-tests shwed fr bth rectsigmid and rectal mtility that the nrmal cntrl grup was significantly different frm all the ther diagnstic grups during balln distentin but nt during either baseline perid. The intercrrelatins amng dependent measures are given in Table 5 fr all subj ects cmbined and fr IBS patients separately. Cntrary t the hypthesis f Latimer et ai. (5), the crrelatin between psychmetric measures f psychlgical distress and tlerance fr balln distentin were nt statistically significant. Cntrary t the Ritchie hypthesis (2), tlerance fr balln distentin was nt crrelated with the mtility index either in the rectum r in the rectsigmid Discussin These data replicate previus studies shwing that tlerance fr balln distentin f the cln is significantly lwer in IBS patients than in nrmal cntrls. Hwever, these data are incmpatible with Table 2. Psychmetric Test Scres Spielberger Trait Anxiety Beck Depressin Inventry NEO Persnality Inventry-Neurticism b Nrmal (5.54) 2.22 (2.76) (6.84) IBS (1.53)" (1.34)" [11.6) FBD 49.1 [7.3)" 16.1 (1.64)" [5.97)" LMA [8.48) 6.5 [6.45)" 51.8 [8.17) Data presented as mean (SD). "Different frm nrmal grup at p <.5 using Bnferrni crrectin. bneo Persnality Inventry scres were transfrmed t T-scres t adjust fr gender differences.

5 May 199 TOLERANCE FOR RECTOSIGMOID DISTENTION IN IBS 1191 Table 4. Rectsigmid and Rectal Mtility at Baseline and Fllwing Distentin f the Rectsigmid With 1 ml f Air Nrmal IBS FBD LMA Sigmid Mtility Index Baseline [2.2).67 [1.48) 1.9 [1.32).71 [.87) Baseline 2.77 [1.1).53 [.64) 1.31 [1.5).67 [.6) Balln distentin.7 [.14).7 [1.27)".73 [.78)" 1.14 [1.59)" Rectal Mtility Index Baseline 1.56 [.8).83 [1.31) 1.49 [1.84).96 [1.21) Baseline 2.62 [.94).74 [.89) 1.99 [2.37).88 [1.1) Balln distentin.13 [.31) 1.85 [4.48)" 1.83 [2.62)" 1.14 [2.78)" Data presented as mean [SD). "Significantly different frm nrmal, p <.5. the hypthesis f Latimer et ai., which suggests that lwered tlerance fr balln distentin in IBS is a functin f neurtic persnality traits. In agreement with Ck et ai. (7), we did nt find that IBS patients had significantly lwer tlerance fr an exterceptive aversive stimulus, hlding a hand in ice water. Mrever, individual differences in tlerance fr balln distentin f the cln were unrelated t tlerance fr the exterceptive aversive stimulus (ice water) and unrelated t psychmetric test scres. Patients with FBD, wh wuld be classified as having IBS by cmmnly used clinical diagnstic criteria but nt by the mre restrictive diagnstic criteria used here (15), did nt shw reduced tlerance fr balln distentin f the cln; their tlerance fr rectsigmid distentin was similar t cntrls. This is cnsistent with the cnclusin f an earlier study (15) that the diagnstic criteria used t define IBS and FBD identify distinct grups f patients. Reduced tlerance fr distentin f the bwel may cntribute t the abdminal pain cmplaints f the IBS grup but appears nt t explain abdminal pain in the FBD grup. Psychmetric tests and the DIS fr psychpathlgy Table 5. Crrelatins Between Dependent Variables All subjects IBS patients Ice Ice Balln water Balln water Spielberger Trait Anxiety Index [52) [53) (13) (14) Beck Depressin Inventry [51) [55) (11) (12) NEO- Neurticism (48) [5) (13) (14) Rectal Mtility Index [51) (49) (12) (12) Sigmid Mtility Index [51) (49) (11) (11) Ice water tlerance (49) (12) Numbers in parentheses represent the number f pairs f bservatins used t cmpute the crrelatin. shwed that IBS patients seen in a medical clinic were mre depressed and anxius than nrmal cntrls. Hwever, such data btained frm medical clinic patients may verestimate the significance f psychpathlgy in IBS; we (15) and thers (16) have previusly shwn that the estimated 8% f individuals with symptms f IBS wh d nt cnsult a physician are n different frm asymptmatic cntrls n psychmetric tests such as these. Self-selectin fr treatment by mre psychlgically distressed individuals cntributes t the assciatin f psychlgical symptms with bwel symptms in medical clinic attenders. In previus studies (4) we have shwn that stepwise distentin f the rectsigmid cln with a balln elicited increased clnic mtility at the site f stimulatin, and the respnse was greater fr IBS patients than fr cntrls. In the present study, mtility was measured 5 em prximal and 5 em distal t the site f balln distentin. Balln distentin f the rectsigmid prduced decreased mtility at these sites in nrmal cntrls and caused n change r a slight increase in mtility in IBS patients. As in previus studies, nrmal cntrls had significantly less mtility than IBS patients during balln distentin but nt at baseline. These findings f greater rectsigmid mtility during balln distentin in IBS patients than in cntrls appears t favr the Ritchie hypthesis (2) that tlerance fr balln distentin is mediated by the elicitatin f cntractile activity. Hwever, cntrary t this hypthesis, there was n crrelatin between tlerance fr balln distentin and amunt f mtility in the rectum r rectsigmid cln during balln distentin. Helzl et ai. (17) have suggested an alternative explanatin fr lwer tlerance t distentin, namely that differences between IBS patients and nrmal cntrls in the cmpliance f the bwel wall culd accunt fr the differences in visceral pain threshld. Using test prcedures similar t thse used in the present study, they fund a significant negative crrelatin between tlerance fr distentin and clnic cmpliance as measured by the static pressure in-

6 1192 WHITEHEAD ET AL. GASTROENTEROLOGY Vl. 98, N.5 crease t stepwise distentin. Higher wall tensin r muscle tne culd be respnsible fr reduced cmpliance and, thereby, increased sensitivity t distentin at the peripheral receptr site. In an analg test f this mdel, they shwed that when differences in bwel wall tensin were manipulated in nrmal subjects by tnically inflating a balln in the cln befre presenting brief distentin stimuli, theshlds fr lwest detectable vlume (nt pain) were inversely related t predistentin vlumes and pressures, that is, t wall tensin. The relevance f these perceptin threshld data frm nrmal cntrls t pain threshlds and pain tlerance in IBS patients has nt yet been tested directly. Hwever, sme frm f peripheral mechanism fr the reduced tlerance t distentin pain and its rle in the prductin f clinical pain symptms f IBS seems increasingly likely. Such a peripheral mechanism wuld be cnsistent with the reprt f Fielding (6) that IBS patients are mre likely than nrmal individuals t reprt tenderness n abdminal palpatin. This study extends the findings f Ck et al. (7) in three respects: (a) we directly cmpared tlerance fr balln distentin f the cln with tlerance fr a nnclnic stimulus such as that used by Ck et al. and cnfirmed that there is a reduced tlerance fr balln distentin which is specific t the cln; (b) we included a cntrl grup with LMA that did nt shw reduced tlerance fr balln distentin, suggesting that clnic hyperalgesia may be specific t IBS; and (c) we tested the Ritchie (2) hypthesis that pain tlerance is a cnsequence f elicited clnic mtility and fund it nt supprtable. References 1. Ritchie J. Pain frm distentin f the pelvic cln by inflating a balln in the irritable cln syndrme. Gut 1973;14: Ritchie I. Mechanisms f pain in the irritable bwel syndrme. In: Read NW, ed. Irritable bwel syndrme. Lndn: Grune & Strattn, 1985; Kullman G, Fielding IF. Rectal distensibility in the irritable bwel syndrme. Ir Med I 1981;74: Whitehead WE, Engel BT, Schuster MM. Irritable bwel syndrme: physilgical and psychlgical differences between diarrhea-predminant and cnstipatin-predminant patients. Dig Dis Sci 198;25: Latimer P, Campbell D, Latimer M, Sarna S, Daniel E, Waterfall W. Irritable bwel syndrme: a test f the clnic hyperalgesia hypthesis. I Behav Med 1979;2: Fielding IF. The diagnstic sensitivity f physical signs in the irritable bwel syndrme. Ir Med I 1981;74: Ck II, van Eeden A, Cllins SM. Patients with irritable bwel syndrme have greater pain tlerance than nrmal subjects. Gastrenterlgy 1987;93: Manning AP, Thmpsn WG, Heatn KW, Mrris AF. Twards psitive diagnsis f the irritable bwel. Br Med I 1978;2: Csta PT Ir, McCrae RR. The NEO persnality inventry manual. Odessa, Fla.: Psychlgical Assessment Resurces, Spielberger CD. State-trait anxiety inventry. Pal Alt, Calif.: Cnsulting Psychlgists, Beck AI. Ward CH, Mendelsn M, Mck I, Erbaugh I. An inventry fr measuring depressin. Arch Gen Psych 1961;4: Rbins LN, Helzer IE, Crughan I, Rathcliff AS. Natinal Institute f Mental Health Diagnstic Interview Schedule: its histry, characteristics, and validity. Arch Gen Psych 1981;38: Rbins LN, Helzer IE, Weissman MM, Orvaschel H, Gruenberg E, Burke ID Ir, Regier OA. Lifetime prevalence f specific psychiatric disrders in three sites. Arch Gen Psych 1984;41: Parker R, Whitehead WE, Schuster MM. Pattern recgnitin prgram fr analysis f cln myelectric and pressure data. Dig Dis Sci 1987;32: Whitehead WE, Bsmajian L, Znderman AD, Csta PT Ir, Schuster MM. Symptms f psychlgic distress assciated with irritable bwel syndrme: cmparisn f cmmunity and medical clinic samples. Gastrenterlgy 1988;95: Drssman DA, McKee DC, Sandler RS, Mitchell CM, Cramer EM, Lwman BC, Burger AL. Psychscial factrs in the irritable bwel syndrme. A multi-variate study f patients and nn patients with irritable bwel syndrme. Gastrenterlgy 1988;95: Helzl R, Erasmus L, Kratzmair M. Peripheral transductin mechanisms in viseral pain perceptin f irritable bwel patients. In: Singer MV, Gebell H, eds. Nerves and the gastrintestinal tract, Falk Sympsium 5 [abstr). Lancaster, U.K.: Kluwer Academic, 1989; Received lanuary 27, Accepted Octber 27, Address requests fr reprints t: William E. Whitehead, Ph.D., Francis Sctt Key Medical Center, 494 Eastern Avenue, Baltimre, Maryland Supprted by grants ROl AM31369, K5 MH133, RRO 2719, DFG H94/1, and by research fellwships frm The Deutschen Akademischen Austauschdienstes.

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