Abstract Irritable bowel syndrome is the most frequentlydiagnosed disorder in gastroenterology. It has been dem-onstrated with specialized motility studies that these pa-tients compared to healthy subjects show changes in rec-toanal electrical and mechanical activity and in rectoanalsensitivity. However, until now no report has been pub-lished on morphological alterations in the rectum or theinternal anal sphincter. Twenty-five consecutive patientswith irritable bowel syndrome (mean age 32, range 17–47years; 24 females) were evaluated prospectively by trans-rectal ultrasonography, rectal sensitivity studies, and re-cordings of both electrical and mechanical activity of thedistal rectum and internal anal sphincter during a 2-h inter-digestive period. Ten healthy volunteers (mean age 34.5,range 19–50 years) served as a control group. Paired andnon-paired Student’s two-tailed t test and linear regressionanalysis were used. It was shown that muscle thickness ofthe rectum during rest (4.7±0.1 mm) was correlated nei-ther with its rectal spike amplitude (0.73±0.1 mV) nor withrectal spike frequency (17.06±3.6 spike/2 h). In addition,the diameter of the internal anal sphincter (1.2±0.1 mm)was correlated neither with its resting pressure, nor withfrequency (17.1±3.2/2 h), duration (14.9±1.5 s), or ampli-tude (14.1±1.9 mmHg), of inhibition of the spontaneousrectoanal inhibitory reflex. No correlation was foundbetween ultrasonographic parameters and rectal distensionvariables (r=0.03). This study demonstrates for the firsttime morphological anorectal changes in patients with ir-ritable bowel syndrome compared to healthy subjects, inaddition to showing that morphological changes are inde-pendent of physiological ones. Therefore both transrectalultrasonography to determine anorectal morphology andelectromanometry to assess anorectal function are impor-tant measures in the evaluation of patients with irritablebowel syndrome.

Key words Ultrasound · Manometry · Electromyo-graphy · Rectum · Anus · Internal anal sphincter ·Irritable bowel syndrome · Rectal sensitivity ·Rectoanal physiology

Résumé Le syndrome du côlon irritable constitue letrouble fonctionnel le plus fréquemment diagnostiqué engastroentérologie. Des études spécialisées de la motilité in-testinale ont démontré que ces patients, comparativementà des sujets sains, présentent des modifications dans l’ac-tivité électrique et mécanique recto-anale et dans la sensi-bilité anorectale. Jusqu’à présent, aucune publication ne faitmention d’altérations morphologiques du rectum ou dusphincter interne. Méthode: Vingt-cinq patients consécutifssouffrant de côlon irritable (âge moyen 32 ans, 14 à 47 ans;24 femmes) ont été évalués prospectivement avec une écho-graphie transrectale des études de la sensibilité rectale etdes enregistrements à la fois de l’activité électrique et mé-canique du rectum distal et du sphincter interne au coursd’une période inter-digestif de deux heures. Dix volon-taires sains (âge moyen 34,5 ans; 19 à 50 ans) ont servi degroupes-contrôles (moyenne±déviation standard; test T deStudent bilatéral apparié ou non apparié et une analyse derégression linéaire). Résultats: (1) Il a pu être démontré quel’épaisseur de la musculature rectale au repos (4,7±0,1 mm)n’est pas corrélée avec l’amplitude (0,73±0,1 mV) et la fré-quence (17,06±3,6 pics/2 heures) et que le diamètre dusphincter interne (1,2±0,1 mm) n’est pas corrélé avec lapression de repos, avec la fréquence (17,1±3,2/2 heures),la durée (14,9±1,5 sec.) et l’amplitude (14,1±1,9 mmHg)d’inhibition du réflexe recto-anal inhibiteur spontané. (2) Aucune corrélation n’a été trouvée entre les paramètresultra-sonographiques et la distension rectale (r=0,03). Conclusion: Les résultats de cette étude démontrent pourla première fois les modifications dans la morphologie ano-rectale survenant chez des patients porteurs d’un côlonirritable en comparaison aux observations faites chez dessujets sains en dehors du fait que ces modifications mor-phologiques sont indépendantes des données physiologi-ques. On en conclut que à la fois l’échographie transrectalepermettant d’étudier la morphologie anorectale et l’élec-

Int J Colorect Dis (1998) 13: 82–87 © Springer-Verlag 1998

Accepted: 21 November 1997

R. A. Awad · J. Martin · M. Cal y MajorJ. L. Noguera · R. Ramos · C. Amezcua · S. CamachoR. Santiago · J. L. Ramirez · J. Castro

Transrectal ultrasonography: relationship with anorectal manometry, electromyography and sensitivity tests in irritable bowel syndrome

ORIGINAL ARTICLE

R. A. Awad (½) · J. Martin · M. Cal y Major · J. L. NogueraR. Ramos · C. Amezcua · S. Camacho · R. Santiago · J. L. RamirezJ. CastroExperimental Medicine and Motility Unit U-404-B, Ministry of Health, Mexico City General Hospital, D.F. 06726, Mexico

tromanométrie visant à déterminer la fonction ano-rectalesont des techniques importantes dans l’évaluation des pa-tients porteurs d’un côlon irritable.

Introduction

Irritable bowel syndrome (IBS) is the most frequently di-agnosed disorder in gastroenterology [1, 2]. It usually leadsto a chronic condition that has a negative impact on thepatient’s quality of life. Although controversial [3], spe-cialized motility studies have demonstrated changes in rec-toanal electrical and mechanical activity [4–6] and sensi-tivity [6, 7] in patients with IBS. However, until now noreport has been published on morphological alterations ofthe rectum or the internal anal sphincter.

Transrectal ultrasonography (TU) is currently the onlytechnique that provides clear and measurable images ofthe rectal wall and the complete anal sphincter [8]. It isquick and easy to carry out, causes little discomfort [9],and emits no radiation. In addition, it is relatively inex-pensive, easy to analyze by experienced personnel, and isthe most accessible radiological test [10]. TU is more re-liable than computed tomography, which usually producespoor-quality images of the rectoanal wall [11]. TU is cur-rently employed to evaluate prostate disorders [12], rec-tal and perirectal pathology [13], staging [14], and detec-tion of recurrent rectoanal cancer [15], pararectal fistules,fissures, and abscesses in Crohn’s disease [9]. It is alsoused in fecal incontinence [8], in the elderly [16], and inconstipation [17].

This report studied the rectoanal region by means of TU,manometry, and electromyography in 25 consecutive pa-tients with IBS and 10 healthy volunteers. We examinedthe possible correlation between morphological and phys-iological findings, which could be useful in producing anearly diagnosis of IBS by means of a readily accessibletechnique such as TU. This would obviate the need toundergo rectoanal motility tests which are complicated [6,18], not easily available [3], expensive, and time consum-ing to carry out and to analyze. This correlation would alsoyield new knowledge on the physiopathology of this so-called functional disease, since there is little understand-ing about what “functional” means.

Materials and methods

Setting

The study was conducted at the Experimental Medicine and Motil-ity Unit, U-404-B, Ministry of Health, Mexico City General Hospi-tal. This is a tertiary referred unit that carries out basic research withclinical applications in motility, physiology, pharmacology, gastroin-testinal hormones, and biofeedback. The study was also conductedat the Ultrasound Department of the Radiology Service. The patientsstudied were referred to our unit from the general hospital, which isone of the largest in Latin America and receives patients from all social strata and from all regions of Mexico.

Subjects and study design

From August 1993 to February 1995 we examined 127 outpatientsconsecutively referred to our tertiary unit. Among these there were25 (mean age 32, range 17–47 years; 24 females) who were symp-tomatic for at least 2 years and fulfilled at least seven of the follow-ing ten criteria for IBS [19–21] (Rome criteria, 22): abdominal pain,pain relieved by defecation, more frequent stools when pain begins,looser stools when pain begins, abdominal distention, mucus per rec-tum, feeling of incomplete evacuation, altered stool frequency, al-tered stool form (hard or loose), and altered stool passage (straining,urgency). Ten healthy volunteers (mean age 34.5, range 19–50 years;4 females) served as a control group. Both sexes were included be-cause although, almost all our patients were women, we do have malepatients [6, 23]. Subjects who had previously undergone abdominalor anorectal surgery were excluded. None had taken any kind of drugsfor at least 7 days. None of the women were pregnant. For inclusionin the protocol the IBS patients could have no concomitant disease,including, for the women, previous obstetric injuries that would af-fect the appearance of the internal anal sphincter. All subjects under-went clinical history recording, standard laboratory tests, rectosig-moidoscopy (Welch Allyn 32823 sigmoidoscope, Skaneateles Falls,NY, USA) and TU. IBS patients were also given manometric andelectromyographic tests of the distal rectum and the internal analsphincter.

The protocol was approved by the Ethics and Research Commit-tee of the Ministry of Health, Mexico City General Hospital in Au-gust 1993. Signed informed consent was obtained from all subjects.

Transrectal ultrasonography

Examinations were carried out based on techniques described else-where [8, 9, 13, 21, 24, 25] using endorectal sonographic equipment(model 1850 Bruel and Kjaer Copenhagen, Denmark) consisting ofa rigid device, 24 cm in length, with 7-Mhz radial transducer, 2 cmin diameter, and a focal point of 2–5 cm. The transducer spins at afrequency of two or three cycles and covers 360°. It is covered by alatex balloon that is itself covered with a latex condom for protec-tion. The balloon is coated with gel and introduced into the patient’srectum while lying on the left side with knees at a 90° angle to thebody. The balloon is then filled with 60 ml water. The proceduretakes 15 min to carry out.

Images 8 cm from the anal margin were obtained in examiningthe rectum [9, 13]. We measured the following layers: mucosa (hy-poechoic layer nearest to the balloon), muscularis mucosae (secondhypoechoic layer), submucosa (third echogenic layer), and muscu-laris propria (outermost hypoechoic layer). To evaluate the internalanal sphincter, the transducer was introduced 2.5 cm from the analmargin [15]. Total and muscle thickness was measured, the latter tak-en as a hypoechoic layer next to the submucosa [10, 24–27].

Measurements of both rectum and internal anal sphincter weretaken three times in the area that provided maximum clarity, and byelectronic indicators built into the equipment’s program. Because theequipment does not register measurements of less than 1 mm, min-imum thickness was given a value of 0.5 mm. The dimensions weremeasured in resting state, during defecation movement (straining),and during voluntary contraction of the sphincter (squeezing).

Manometric and electromyographic recording technique

Intraluminal pressure and electrical activity were recorded by meansof the same probe: (Honeywell MP-3 motility probe, Honeywell,Denver, CO, USA), which contains three miniature pressure trans-ducers within a surgical grade silicone rubber tube 5 mm in diame-ter. The transducers were staggered at 120° intervals around theprobe. Myoelectrical activity was recorded by means of two bipolarAgAgCl ring electrodes positioned around the probe alongside thepressure transducers.

One pressure transducer was positioned in the internal analsphincter. The second transducer and a ring electrode were positioned

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in the rectum 5 cm from the pressure transducer in the internal analsphincter, and the third transducer with a ring electrode was posi-tioned a further 5 cm away. Care was always taken to ensure the prop-er position of the probe throughout the 2-h duration of the study; ourexperience with this probe (>300 studies [6, 23, 28, 29, 30]) showsthat folding or movement from the high-pressure sphincter zone isvery rare and easily detectable. A period of 30 min was allowed forthe patient to become accustomed to the presence of the probe. Thestudy was performed with the subject in the left lateral position.

Pressure waves and electrical signals were recorded simultane-ously on a Hewlett-Packard 8-channel polygraph model 4574A(Waltham, MA, USA) with lower and upper cutoff frequencies set at 5–30 Hz for electrical recordings, an amplifier gain of 12.5 mmHg/cm for motor recordings, and a paper speed of 0.5 mm/s.A band pass filter of 5–30 Hz removed all slow wave activity andallowed only spike activity to be recorded. Only spike potentialsgreater than 0.02 mV were considered. A reference electrode wasfixed to the right leg skin with electrode paste.

Each transducer used a diaphragm-type sensor and was refer-enced to atmospheric pressure. Calibration was performed before andafter each experiment. Pressure changes of less than 5 mmHg andidentifiable artifacts were excluded from analysis. Two forms of me-chanical activity were assessed: (a) basal anal pressure and (b) nat-urally occurring rectoanal inhibitory reflex. There was a 2-h basalperiod, with the sensors static in the internal anal sphincter and therectum. The naturally occurring rectoanal inhibitory reflex can bedefined as the association of spontaneous increase in rectal pressureassociated with inhibition of the internal anal sphincter [6, 28, 29].Rectal sensitivity was measured as described previously [6, 7, 29].

Statistical analysis

Data are presented as mean±SEM. Statistical significance was as-sessed using paired and nonpaired Student’s two-tailed t test. Line-ar regression analysis was used to evaluate correlations between mor-phological and physiological rectoanal variables. An α level of 0.05was used. Sonography was performed by members of the radiolog-ical team experienced in the interpretation of ultrasound images whowere blinded to the results of manometric and myoelectrical evalu-ations. The copyright on the computer program used in the electro-manometry for this study has been registered with the Ministry of

Public Education, United States of México (Awad Reyes R, LunaTrillo VM, 1995, certificate #68958).

Results

Subjects

Of the 127 prospects interviewed, 45 fulfilled the necessaryrequirements. Twenty declined to participate because theyrefused to allow a TU study, and finally 25 were enrolled.TU was carried out on IBS patients and healthy volunteersalike. IBS patients were also given electromyography andrecto-anal manometry tests to compare procedures. All la-boratory and rectosigmoidoscopic parameters were normal.

Transrectal ultrasonography

Rectal wall

In all studied subjects the four layers of the rectal wall wereidentified and measured clearly. In healthy subjects thethickness of the total rectal wall and submucosa was sig-nificantly reduced during strain and squeeze (P<0.05),while in patients with IBS the thickness of submucosa andmuscularis mucosae was significantly diminished duringstrain (P<0.05; Table 1). Total rectal thickness at rest wasless in IBS patients than in healthy subjects (4.7±0.1 vs.6.1±0.1 mm; P<0.001).

Internal anal sphincter

The internal anal sphincter was clearly defined and meas-ured in both healthy volunteers and patients with IBS. Inhealthy subjects both the total thickness of the anal sphinc-ter and the muscle thickness of the internal anal sphincter atrest (Fig. 1) were significantly diminished during strain andsqueeze (P<0.05; Fig. 2, Table 1). In patients with IBS therewas the opposite, with total thickness at rest (Fig. 3) beingsignificantly increased during strain and squeeze (P<0.05;

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Fig. 1 Muscle thickness of the internal anal sphincter at rest in ahealthy subject (TU)

Fig. 2 Muscle thickness of the internal anal sphincter during strainin a healthy subject (TU)

Fig. 3 Muscle thickness of the internal anal sphincter at rest in anirritable bowel syndrome patient (TU)

Fig. 4), and muscle thickness increased during squeeze(P=0.02; Table 1). Muscle thickness of the internal analsphincter at rest was less in IBS patients than in healthy sub-jects (1.2±0.1 vs 1.8±0.1 mm; P=0.01); however, it in-creased during strain (P=0.0001) and squeeze (P=0.0001).

Rectal electrical activity

During the 2-h recording period there was no loss of electri-cal signal due to poor apposition between the electrodesand the rectal wall. The IBS rectal spike frequency was17.06±3.6 spike/2 h, and the amplitude was 0.73±0.1 mV(Fig. 5).

Rectoanal mechanical activity

In IBS patients basal anal pressure was 23.1±2.5 mmHg.The naturally occurring rectoanal inhibitory reflex showeda frequency of 17.1±3.2/2 h, an amplitude of inhibition of

the internal anal sphincter of 14.1±1.9 mmHg, and a du-ration of inhibition of the sphincter of 14.9±1.5 s (Fig. 5).

Sonography and electromyography

In IBS patients total rectal thickness and that of each layerwere nonsignificantly correlated with the frequency andamplitude of rectal spike (r=0.02).

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Table 1 Sonography: analsphincter and rectal thickness(mm) in 10 healthy individualsand 25 IBS patients

Internal sphincter Rectum

Total wall Muscular Total wall Mucosae Muscularis Submucosae Muscularismucosae propria

Healthy individuals

Rest 5.40±0.22 1.85±0.15 6.10±0.1 1.40±0.16 1.35±0.18 1.80±0.20 1.15±0.10Strain 4.64±0.28* 0.55±0.15* 4.65±0.23* 1.20±0.13 0.95±0.05 1.40±0.16* 1.10±0.12Squeeze 4.73±0.17** 0.55±0.05** 4.50±0.21** 1.15±0.15 1.10±0.06 1.35±0.15** 1.05±0.11

IBS patients

Rest 5.12±0.25 1.24±0.12 4.70±0.19 1.12±0.08 0.86±0.06 1.16±0.09 1.08±0.07Strain 5.72±0.20* 1.38±0.10 4.68±0.26 1.08±0.11 0.70±0.05* 0.94±0.07* 1.04±0.10Squeeze 5.72±0.19** 1.56±0.22* 4.56±0.24 1.06±0.10 0.74±0.07 0.98±0.08 1.08±0.10

* = P<0.05, rest vs. strain** = P<0.05, rest vs. squeeze

Fig. 4 Muscle thickness of the internal anal sphincter during strainin an irritable bowel syndrome patient (TU)

Fig. 5 A recording at the distal rectum and internal anal sphincterlevel in which the IBS patient’s rectal spike amplitude is accompa-nied by an increase in rectal mechanical activity and an inhibition ofinternal anal sphincter mechanical activity (spontaneous rectoanalinhibitory reflex)

Sonography and manometry

Total and muscle thickness of the internal anal sphincterwere nonsignificantly correlated with basal anal pressure(r=0.11) and with frequency, amplitude, and duration ofinternal anal sphincter inhibition during the naturally oc-curring rectoanal inhibitory reflex (r=0.02).

Sonography and rectoanal sensitivity

The rectal sensitivity values found in this study were sim-ilar to those in our previous report on 80 IBS patients [6].Patients felt a sensation with 15.3±1.3 ml and discomfortwith 55.9±8 ml, and the time to perceive the sensation was4.5±0.9 s. No significant correlation was found with anymorphological, sonographic, or physiological parameters(r=0.02).

Discussion

These results demonstrate for the first time morphologicalanorectal changes in patients with IBS compared to healthysubjects. They also show that morphological changes areindependent of physiological ones.

In our IBS patients the total thickness of rectal wall atrest was less than that in healthy subjects. The contrary hasbeen reported in inflammatory diseases such as Crohn’sdisease [9], where an increase in thickness of the rectalwall has been observed by TU in 40% of all patients andin 58% of those with active proctological lesions. Havingpreviously reported on excitatory rectal neurotransmissionin IBS [6, 22], we evaluated the possible correlationbetween thickness of the rectal wall measured by TU andexcitatory and inhibitory neurotransmission measured byrectal electromyography [6, 18]. However, since we didnot observe any significant correlation, it is suggested thatphysiological changes in rectal spike activity are indepen-dent of rectal wall morphological ones. Therefore we canassume that greater or lesser thickness of the wall is notrelated to higher or lower electrical activity.

Muscle thickness of the internal anal sphincter at restin this study was 1.85±0.15 mm. This agrees with the 2.09 mm reported by Gantke et al. [26], the 2 mm reportedby Nielsen et al. [10], and the 2.2 mm registered by Pa-pachrysostomou et al. [32]. Others have reported measure-ments in the range of 3–8 mm [9, 17, 25, 27]. The discrep-ancy in these figures could be explained by the variety ofmethods used. At the moment there is no standard tech-nique.

Muscle thickness of the internal anal sphincter was lessin patients with IBS at rest than in healthy subjects but be-came greater during strain and squeeze. We could find noexplanation for this because, to our knowledge, this is thefirst report on the use of TU in patients with IBS. Never-theless, a probable explanation is that IBS patients havechronic rectoanal excitatory activity [6], the muscle at rest

having a reduced thickness because it undergoes greaterexercise. Once excited, while working harder, its thicknessincreases during strain and squeeze.

Our values on basal anal pressure are lower than thosepreviously reported [26]. This is probably because mostresearchers use a stationary pull-through for their mea-surements; this is not very accurate because a number ofvariables can affect the data, such as movement and in-crease of spontaneous pressure when the patient feels thedevice being removed. Our data were based on figurestaken over an average time span of 2 h.

We found no significant correlation between morpho-logical data on the internal anal sphincter produced by TUand physiological data produced by manometry and elec-tromyography. This supports the findings of Nielsen et al.[33] and Gantke et al. [26] who also found no correlationbetween the internal anal sphincter diameter and pressureat rest in healthy subjects. On the other hand, Law et al.[8] reported a relationship between pressure at rest andinternal anal sphincter thickness in seven patients with neu-rogenic anal incontinence. Although there is a discrepancy,which shows that there may or may not be a correlation,Law et al. reported on a small number of patients in whoma relationship was observed only in those with intact ex-ternal anal sphincter. Therefore it seems that diameterchanges in the sphincter are not related to physiologicalfactors in IBS patients.

A technical limitation in this study was that the ultra-sound equipment was not able to measure more exactlythan 1 mm. This problem, however, is not unusual, havingbeen reported previously [33]. Another possible limitationis that we used a water-filled balloon rather than a plasticcone for the anal ultrasound assessments. However, analendosonography was performed by the same team of ra-diologists throughout the study. Care was always taken touse the same amount of water to prevent over inflation ofthe balloon that could squash the internal anal sphincterand give false images of the muscle thickness. Moreover,the same technique is currently used by Nielsen et al. [33]and by Tjandra et al. [25] who do not feel that the use of aplastic cone is necessary and routinely perform anal endo-luminal ultrasound in patients without it. Furthermore, theinternal anal sphincter was clearly defined and measuredin healthy volunteers and in patients with IBS, and our de-scription is correlated with that of other groups of investi-gators [10, 26, 32].

In conclusion, these ultrasound data provide for the firsttime valuable information about morphological rectoanalchanges in patients with IBS. These alterations are inde-pendent of rectoanal mechanical and electrical physiolog-ical changes. This suggests that there are different path-ways of neurotransmission in the received stimulus and itsconscious integration into the nervous system, and the pro-cess carried out by the effector organ.

The two methods – electromanometry to evaluate thefunctioning of the rectum and the internal anal sphincter,and TU to determine its morphology – constitute impor-tant techniques in evaluating the rectoanal segment. Thisinformation could well be useful in improving our under-

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standing of the physiopathology of such a common andcomplicated disorder as IBS. These findings will probablyalso lead to improved and more scientifically based treat-ment.

Acknowledgements With appreciation for the collaboration of J. G. de la Cruz, M. Castro, M. E. Martinez, M. C. Sandoval, andJohn Hertzberg for the English revision of the manuscript. A portionof this report was part of the postgraduate theses in radiology of J. M., J. L. N., and R. R.

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