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Gastrointestinal Imaging |
1 From the Departments of Radiology (R.G.H.B.T., E.L., J.M.A.v.E.), Surgery (G.L.M., G.L.B., K.e.N., C.G.M.I.B.), and Clinical Epidemiology (A.G.H.K.), University Hospital of Maastricht, P. Debyelaan 25, 6202 AZ Maastricht, the Netherlands. Received April 24, 2000; revision requested May 25; final revision received October 10; accepted November 1. Address correspondence to R.G.H.B.T. (e-mail: rbe@rdia.azm.nl).
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ABSTRACT |
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 TOP ABSTRACT INTRODUCTIONMATERIALS AND METHODSRESULTS DISCUSSION REFERENCES |
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MATERIALS AND METHODS: Sixty healthy volunteers underwent 1.5-T phased-array MR, endoanal MR, and endoanal US examinations. Sphincter muscle thicknesses were measured. Measurement reliability was analyzed, and correlations among the imaging methods were calculated. Multivariate analysis was performed to assess the influence of age, weight, height, sex, parity, and obstetric trauma on sphincter dimensions.
RESULTS: Both MR methods had good reliability for measurements of all sphincter components, whereas endoanal US was reliable for internal sphincter measurement only. There was little correlation between the techniques, except between the two MR techniques, with a strong correlation for total sphincter and perineal body thickness. The internal sphincter thickened significantly (P = .002) with age at endoanal US and endoanal MR imaging but not at phased-array MR imaging. There were small sex-based differences in sphincter muscle measurements at phased-array MR imaging only.
CONCLUSION: Endoanal US enables reliable measurement of only internal sphincter thickness, whereas both MR imaging methods enable reliable measurement of all sphincter components. Sphincter measurement with phased-array MR imaging is as reliable as that with endoanal MR imaging.
Index terms: Anus, 757.92 • Anus, MR, 757.121411, 757.121412, 757.121416 • Anus, US, 757.12989 • Magnetic resonance (MR), comparative studies, 757.121411, 757.121416
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTS DISCUSSION REFERENCES |
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Several imaging modalities can be used to evaluate the anal sphincter muscles. The advantage of endoanal US is that it is inexpensive and widely available. A major disadvantage is that it is difficult to visualize the external sphincter muscles with this modality owing to the inherent low soft-tissue contrast resolution (14,15). Similar to all US methods, endoanal US is operator dependent, with substantial interobserver variability (16,17).
Magnetic resonance (MR) imaging with an endoanal coil has been introduced as a complementary modality to endoanal US (10,18,19), especially for the evaluation of the external sphincter complex (20–22). A disadvantage of this modality is that its use has been restricted to specialized centers, because the required endoanal coil is not yet available with every MR machine. Although MR imaging with a body coil is more widely available, it provides insufficient spatial resolution for differentiating the individual small muscles of the anal sphincter (23–25). A high-spatial-resolution MR technique with a quadrature phased-array spine coil has shown promising results for the evaluation of the anal sphincter (26).
At present, it is unclear which imaging method is best for anal sphincter measurements. Anal sphincter components are small and are measured in millimeters. To detect subtle changes in thickness, an imaging technique with accurate discriminatory capability and accurate reproducibility is required. The available data on sphincter measurements indicate conflicting results. For example, in some studies (9,27–30), investigators have found a correlation between internal sphincter thickness and age, whereas in others, these findings could not be confirmed (24,31, 32). Some investigators have found a correlation between sphincter morphologic features and manometric results (5,27), whereas others have not (6,28,31,33). These conflicting results may reflect the inherent inaccuracies of the imaging techniques. To our knowledge, only one study so far, with eight volunteers, has involved a comparison of anal sphincter dimension measurements obtained with different imaging modalities (25). The authors concluded that endoanal US was superior to conventional MR imaging with a body coil, but the MR technique that was used is no longer considered up to date. The aim of the present study was to compare endoanal US, endoanal MR imaging, and phased-array MR imaging for the measurement of anal sphincter muscles in healthy volunteers.
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MATERIALS AND METHODS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTS DISCUSSION REFERENCES |
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After giving informed consent, the volunteers underwent MR imaging with a quadrature phased-array spine coil, endoanal MR imaging, and endoanal US. The three examinations always were performed in this order, and the whole procedure was complete within 1 hour. After the three examinations, each volunteer was asked to give a subjective score of discomfort with each of the procedures on a visual analog scale. A score of 0 represented not uncomfortable, excellently tolerated, and a score of 10 represented very uncomfortable, hardly tolerable.
Phased-Array MR Imaging
MR imaging was performed with a 1.5-T unit (Gyroscan Powertrak 6000, NT release 6.2.1; Philips Medical Systems, Best, the Netherlands) (gradient echo strength, 23.0 mT/m; rise time, 0.2 msec; slew rate, 105 T/m/sec). All subjects were placed in the supine position with the pelvis centered at the proximal end of a quadrature phased-array spine coil in the feet-first position. T1-weighted two-dimensional turbo spin-echo (656/10 [repetition time msec/echo time msec], echo train length of five, 8-mm section thickness, 0.8-mm intersection gap, four signals acquired, 166 x 256 matrix, 25-cm field of view, acquisition time of 1 minute 4 seconds) and T2-weighted two-dimensional turbo spin-echo (3,427/150, echo train length of 25, 3-mm section thickness, 0.3-mm intersection gap, eight signals acquired, 175 x 256 matrix, 20-cm field of view, voxel size of 2.64 mm3, acquisition time of 6 minutes 5 seconds) sequences were used.
The T1-weighted sequences were performed in the transverse plane, and the T2-weighted sequences were performed in the sagittal, coronal, and transverse planes. The T1-weighted and sagittal and coronal T2-weighted sequences served for accurate planning of the transverse T2-weighted sequences, because it was important to angle these planes exactly perpendicular to the long axis of the anal canal. The subjects did not receive bowel preparation, and no catheters were inserted in the anal canal during the procedure. The total imaging time for phased-array MR imaging was 20 minutes.
Endoanal MR Imaging
Endoanal MR imaging was performed with the MR unit used for phased-array MR imaging. All subjects were repositioned in the head-first position after the phased-array spine coil was removed. The endoanal coil is designed for imaging the anal canal. It is a rigid coil with a length of 10 cm and a diameter of 19 mm. The device was covered with a condom, and after application of a lubricant, it was positioned in the anal canal in a left lateral decubitus position, after which the volunteers were carefully turned in the supine position. On the coronal and sagittal survey images, a transverse plane perpendicular to the long axis of the anal canal was identified, and T2-weighted two-dimensional turbo spin-echo sequences (3,427/150, echo train length of 25, 3-mm section thickness, 0.3-mm intersection gap, eight signals acquired, 175 x 256 matrix, 12-cm field of view, voxel size of 0.96 mm3, acquisition time of 6 minutes) were performed. The total imaging time for endoanal MR imaging was 7 minutes.
Endoanal US
Endoanal US was performed, by a colorectal surgeon (G.L.M.) experienced in performing endoanal US, by using a US scanner (SSD-2000 MultiView; Aloka, Tokyo, Japan) with a radial endoscopic probe and a 7.5-MHz transducer. A plastic cone with a diameter of 17 mm covered the transducer head, which was then covered by a latex balloon filled with degassed water. A lubricated condom was placed over the balloon. Subjects were examined in the supine left lateral position with their knees bent at 90°. The probe was introduced into the anal canal, positioned at the upper aspect of the puborectalis sling, and rotated so that the 12 o’clock was anterior, as in a normal orientation for cross-sectional imaging. (3 o’clock represents the patient’s left side; and 9 o’clock, the patient’s right side.) A personal computer with a video frame grabber was used to capture the series of US images taken from the video output of the scanner. When a "frozen image" was acquired, the probe was withdrawn one increment and the new position was scanned and acquired. This process was repeated until all levels perpendicular to the anal canal were scanned, and each study was saved for subsequent review. The total examination time for endoanal US was 10 minutes.
Image Evaluation
MR images.—All MR images were evaluated independently by a radiologist (R.G.H.B.T.) and a colorectal surgeon (G.L.M.), both of whom were experienced in reading pelvic MR images. The presence of motion artifacts was evaluated by only the radiologist. The MR measurements were performed by using a workstation (Easy Vision; Philips Medical Systems) at least 2 months after data acquisition to avoid bias from the other imaging techniques. Each observer was unaware of the other’s findings at all times. To assess intraobserver agreement of the MR measurements, the radiologist, blinded with regard to previous measurements, performed two separate assessments of each MR study, which were separated by at least 2 weeks.
The internal sphincter, longitudinal muscle, external sphincter, and total sphincter thickness were measured on the transverse images. All measurements were taken at the 4 o’clock left lateral aspect at the midanal level of the anal canal by using software callipers accurate to 0.1 mm. The 4 o’clock site was chosen somewhat arbitrarily on the posterior aspect to avoid interference with occult sphincter lesions that often are located anteriorly.
At phased-array MR imaging, the internal anal sphincter is depicted as an isointense to hypointense circular band, whereas at endoanal MR imaging, it appears as a hyperintense circular band. At the midanal level, the external sphincter appears as a typical teardrop, with the tip of the drop pointing to the coccyx. The hypointense longitudinal muscle can be found in the hyperintense fat tissue of the intersphincteric space between the internal and external sphincter muscles (Figs 1, 2). The total sphincter thickness was defined as the distance between the inner border of the internal sphincter and the outer border of the external sphincter. The perineal body is formed by the fibers of the external sphincter and transverse perineal muscle (Fig 1). It is much more developed in women and provides anterior support of the anal canal. The thickness of the perineal body was measured in the midline and defined as the distance between the inner surface of the internal sphincter and the outer surface of the anterior muscle complex. It was measured in women only, and the internal sphincter was included in the measurement, because of the practical difficulty at phased-array MR imaging in defining the border between the hypointense internal sphincter and the hypointense perineal body.
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The results of the different imaging modalities were compared by using the Pearson correlation coefficient, and orthogonal regression curves were constructed for significant correlations. To assess the influence of clinical variables, a multivariate analysis was performed with a regression model that included age, weight, height, sex, parity, and obstetric trauma simultaneously. The multivariate analysis was performed on only those sphincter dimensions that could be measured with reasonable reliability. The statistical analyses were performed by using a software package (SPSS for Windows, release 8.0; SPSS, Chicago, Ill). A P value of less than .05 was considered to indicate a statistically significant difference.
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RESULTS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTS DISCUSSION REFERENCES |
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The volunteers considered the phased-array MR imaging examination to be the least uncomfortable and the endoanal MR imaging examination to be the most uncomfortable. The mean (± SD) visual analog scale scores for discomfort at imaging were 1.4 ± 1.8 for endoanal US, 2.6 ± 2.3 for endoanal MR imaging, and 0.6 ± 0.9 for phased-array MR imaging. A pairwise comparison between the three methods showed that the differences were statistically significant (P < .001 for all three examinations). The fixed order of the examinations, however, could have been a source of bias.
The men found the insertion of an endoanal probe, at both US and MR imaging, more unpleasant than did the women (mean difference in visual analog scale score of 1), but the difference was not statistically significant.
Normal Values
The sphincter measurements in the healthy volunteers obtained with the three imaging methods are listed in Table 1. All values obtained with both MR techniques, except those for the internal sphincter and the perineal body, were within the same range. The internal sphincter and perineal body measurements with phased-array MR imaging were thicker than those with endoanal MR imaging. There was a marked difference in mean external sphincter thickness between endoanal US—7.2 mm for women and 6.1 mm for men—and both MR techniques: 1.2 and 1.3 mm for men and women, respectively, at endoanal MR imaging and 1.3 and 1.4 mm for men and women, respectively, at phased-array MR imaging.
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Correlations among Imaging Techniques and Regression Curves
Correlations among the three imaging techniques are shown in Table 3. There was a moderate but significant (Pearson) correlation between endoanal US and endoanal MR imaging for internal sphincter (r = 0.33) and total sphincter thickness (r = 0.38) measurements. The orthogonal regression formulas (curves not shown) were as follows: endoanal US internal sphincter thickness = -13.3 + (8.8 x endoanal MR internal sphincter thickness), and endoanal US total sphincter thickness = -17.4 + (5.1 x endoanal MR total sphincter thickness). There was no correlation between endoanal US and phased-array MR imaging for measurement of any sphincter component. Phased-array MR imaging and endoanal MR imaging showed a strong correlation for measurement of total sphincter thickness (r = 0.61) and the perineal body (r = 0.82). The orthogonal regression curves and coefficients are shown in Figure 4. Although there was a strong correlation, the regression curve in Figure 4b shows that the measured thickness varied according to MR imaging technique; this suggests that the two MR techniques provide measurements in a different way. When the correlations were recalculated for readings of the other observer, only the correlation between the two MR techniques for measurements of total sphincter thickness and the perineal body remained significant (P < .01).
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DISCUSSION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTS DISCUSSION REFERENCES |
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Our study results show that with endoanal US, only internal anal sphincter thickness can be reliably measured, whereas with MR imaging—especially phased-array MR imaging—reliable measurements of all the sphincter components can be made. It is important to realize that this limitation of endoanal US applies to only subtle variations in sphincter thickness, in the same order of variation among a normal population. Reliability is likely to improve when the pathologic changes are more obvious (ie, tripling of thickness). Thus, it is even more obvious that this limitation of endoanal US does not apply in the detection of localized sphincter defects, where its benefit has been proved (5,7,8).
Two studies have specifically addressed the problems of the reproducibility of endoanal US sphincter measurements (16, 17). Enck et al (16) examined a small group of healthy volunteers and concluded that endoanal US did not provide reliable measurements of internal and external sphincter thicknesses. Gold et al (17) examined 51 patients and found that measurements of the internal sphincter were more reproducible than those of the external sphincter. These findings are consistent with our results. At endoanal US, the internal sphincter is easy to define because it is a hypoechoic structure that is highlighted against hyperechoic adjacent tissues. In contrast to the internal sphincter, the more hyperechoic longitudinal and external sphincter muscles show less contrast with the surrounding hyperechoic fatty tissue. Both the inner and outer borders of the external sphincter are more difficult to define, leading to less reliable measurements (Fig 3).
The high inherent soft-tissue contrast makes MR a more reliable imaging method to measure anal sphincter components. The results of previous studies by Briel et al (14) and Rociu et al (22) showed that endoanal MR imaging is superior to endoanal US in assessing localized and diffuse sphincter lesions, especially those of the external sphincter. Our results support this finding.
MR Techniques
MR imaging with a body coil has insufficient spatial resolution for accurate delineation of the individual small muscle components of the anal sphincter (23–25). MR imaging with an endoanal coil, however, generates high-spatial-resolution images of the anal sphincter because of a very high signal-to-noise ratio near the coil (10,18,20,37). Reports (26,38) have shown that detailed images of the anal sphincter can be generated by also using a phased-array coil. The present study findings confirm that results that are at least as reliable as those obtained with an endoluminal coil can be obtained with this external coil. The multiple-coil arrangement in a phased-array coil increases the signal-to-noise ratio, and images with small voxels and high spatial resolution can be obtained. The specific coil used in our study was a quadrature phased-array spine coil. Unlike the linear arrangement of the coil components in a standard torso or pelvic phased-array coil, the components in a phased-array spine coil are arranged in quadrature. This further improves the signal-to-noise ratio, and, thus, even smaller voxels can be generated.
Correlations
There were no strong correlations between the measurements obtained with endoanal US and those obtained with the two MR techniques. This was no surprise, considering the low reliability of most of the US measurements. Because the measurements with the two MR techniques were more reliable for all muscle components, we expected a high correlation. However, there was a consistent and strong correlation between the two MR techniques for only the total sphincter and perineal body thickness measurements. The absence of correlation for internal and external sphincter muscle measurements, with a strong correlation for total sphincter thickness measurements, suggests a difference in distinguishing the individual muscle components between the two MR techniques.
In our experience, it was not always easy to distinguish the longitudinal muscle from the external sphincter at endoanal MR imaging. This was reflected also in the lower reliability of endoanal MR imaging, compared with that of phased-array MR imaging, in measuring the external sphincter and longitudinal muscle. These two muscles often lay close to each other, and the interface of these muscles with the hyperintense fat tissue of the intersphincteric space is more likely to fade when the sphincter complex is stretched by an endoluminal coil (Fig 5). The outer border of the total sphincter complex is less often influenced by the stretching effect of the coil; this explains the strong correlation between the two MR techniques for total sphincter thickness measurements.
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A striking observation was the large difference in external sphincter thickness between endoanal US and both MR techniques, with a much thicker external sphincter and greater variability at endoanal US than at MR imaging. Although the US values were within the range of values reported in literature, this large difference between the two imaging modalities again illustrates the inherent inaccuracy of endoanal US in defining and measuring the external sphincter muscle.
Normal values for sphincter dimensions differ between techniques, and the lack of strong correlation between the different imaging modalities suggests that values of anal sphincter muscle thickness obtained with different techniques are not interchangeable. The question of which of these imaging techniques reveals the true values of sphincter muscle thickness in healthy individuals can be asked, and it may be that none of the methods yields the correct measurement. This question, however, is not very relevant, because the purpose of measuring anal sphincters is to distinguish with consistency a normal versus abnormal measurement, regardless of the absolute values. Therefore, the practical consequence is that one needs to refer to normal sphincter values with each technique to decide whether a measured thickness is normal or abnormal. Even then, there can be differences.
Our values for internal sphincter thickness at endoanal US were slightly higher than those of other authors who used a probe with the same diameter, and our measurements for individual sphincter muscle thickness at endoanal MR imaging were slightly lower than those in other reports (30). This can be explained by differences in the equipment used, sequences, the manner of performing measurements, and definitions and subjective interpretations. To minimize the effect of these confounding variables, the imaging techniques should be standardized. At present, the most practical advice is that when one wants to compare sphincter dimensions with a set of normal values from the literature, an imaging technique that is as similar as possible to the referenced technique should be used.
Multivariate Analysis
Our study results show that with increasing age, the internal sphincter becomes slightly thicker, at least when measured with endoanal US and endoanal MR imaging. At endoanal US, the muscle thickness increases by 0.38 mm every 10 years; and at endoanal MR imaging, by 0.13 mm. This confirms the findings of many other reports (9,27–30, 39,40). The age-related increase in internal sphincter size most likely is the result of connective tissue infiltration rather than of true hypertrophy (29,41–43). It is surprising that this increase in thickness could not be demonstrated with phased-array MR imaging in our study.
There were small sex-related differences in internal sphincter, external sphincter, and longitudinal muscle measurements, but only at phased-array MR imaging: In men, the external sphincter was found to be thicker. Other authors have reported conflicting results for sex-related differences: Some have reported a thicker external sphincter in men (32,44); and others, no difference (29,35). In an endoanal MR study with 50 female and 50 male healthy volunteers, Rociu et al (30) generally did not find any sex-related differences, except in the younger age group, in which the male volunteers had a thicker external sphincter than did the female volunteers.
Parity had little effect on anal sphincter dimensions. This seems to be in contrast with the results of a study by Zetterstrom et al (36), who found thinner perineal bodies in multiparous women than in their nulliparous control counterparts. In that study, however, the multiparous women had symptomatic sphincter defects and no other variables such as obstetric trauma were taken into account. An interesting finding in our study was that in the women who had undergone episiotomy or had a perineal laceration during childbirth, the perineal body was thicker when measured with phased-array MR imaging. This can be explained by the fibrotic scar tissue after healing of the episiotomy wound or the perineal laceration.
It remains difficult to explain why some differences and correlations are apparent with one imaging method and not with the other and why many reports show divergent findings. Some of the apparent differences may be caused by a type 1 error (significant difference by chance when in reality there is no difference), especially when performing multiple analyses. Other inconsistencies may be caused by the poor reliability of the imaging method or by difficulties in comparing different imaging techniques and different investigators, as discussed earlier.
At present, endoanal US is the imaging method of choice for the work-up of patients with fecal incontinence. The majority of younger patients are found to have underlying structural sphincter damage. Endoanal US is performed to identify those patients with sphincter damage who may benefit from surgical repair (5,7,8). However, there is a small group of patients in whom endoanal US cannot depict any sphincter damage. It has been suggested that measuring sphincter thickness in this group may be important to exclude diffuse structural sphincter changes associated with idiopathic fecal incontinence, passive fecal incontinence, or obstructive defecation disorders (9,11–13).
Results of the present study show that with endoanal US, only internal anal sphincter thickness can be measured reliably, whereas with MR imaging, reliable measurements of all the sphincter components can be made. MR imaging with a phased-array spine coil is as reliable as the more established endoanal MR imaging. A disadvantage is that normal sphincter dimensions differ not only between the two imaging techniques but also between authors who apparently are using the same technique. When sphincter measurements are going to be used for clinical decision making or for further research, the imaging techniques should be standardized as much as possible.
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ACKNOWLEDGMENTS |
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FOOTNOTES |
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Author contributions: Guarantor of integrity of entire study, R.G.H.B.T.; study concepts, J.M.A.v.E., R.G.H.B.T., G.L.B., G.L.M., C.G.M.I.B.; study design, R.G.H.B.T., G.L.M., G.L.B., J.M.A.v.E.; literature research, R.G.H.B.T., G.L.M.; clinical studies, R.G.H.B.T., G.L.M., K.e.N., E.L.; data acquisition, R.G.H.B.T., G.L.M., K.e.N., E.L.; data analysis/interpretation, R.G.H.B.T., G.L.M.; statistical analysis, R.G.H.B.T., G.L.B., A.G.H.K.; manuscript preparation, R.G.H.B.T.; manuscript definition of intellectual content and editing, R.G.H.B.T., G.L.B., G.L.M., J.M.A.v.E.; manuscript revision/review, G.L.B., C.G.M.I.B., J.M.A.v.E.; manuscript final version approval, R.G.H.B.T., G.L.M., G.L.B., A.G.H.K., E.L., C.G.M.I.B., J.M.A.v.E.
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REFERENCES |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTS DISCUSSION REFERENCES |
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