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Original Research |
1 Department of Radiology, Academic Medical Center, Meibergdreef 9, Amsterdam,
The Netherlands 1105 AZ.
2 Department of Radiology, University Hospital Maastricht, Maastricht, The
Netherlands.
3 Department of Radiology, Onze Lieve Vrouwe Gasthuis, Amsterdam, The
Netherlands.
4 Department of Clinical Epidemiology and Biostatistics, Academic Medical
Center, Amsterdam, The Netherlands.
5 Department of Surgery, University Hospital Maastricht, Maastricht, The
Netherlands.
Received March 4, 2005;
accepted after revision May 9, 2005.
Address correspondence to M. P. Terra
(m.p.terra{at}amc.uva.nl).
Abstract
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SUBJECTS AND METHODS. Thirty patients with fecal incontinence (23 women, seven men; mean age, 58.7 years; age range, 37-78 years) underwent both endoanal and external phased-array MRI. Images were evaluated for external anal sphincter atrophy by three radiologists. Measures of differences and agreement between both MRI techniques and of interobserver and intraobserver agreement of both techniques were calculated.
RESULTS. The MRI techniques did not significantly differ in their
ability to depict external anal sphincter atrophy (p = 0.63) with
good agreement (
= 0.72). Interobserver agreement was moderate (
= 0.53-0.56) for endoanal MRI and moderate to good ( = 0.55-0.8) for
external phased-array MRI. Intraobserver agreement was moderate to very good
( = 0.57-0.86) for endoanal MRI and fair to very good ( =
0.31-0.86) for external phased-array MRI.
CONCLUSION. External phased-array MRI is comparable to endoanal MRI in depicting external anal sphincter atrophy and, thereby, in selecting patients for anal sphincter repair. Because results among interpreters varied considerably depending on the experience level, both techniques can be recommended in the diagnostic workup of fecal incontinence only if sufficient experience is available.
Keywords: anus • atrophy • external anal sphincter • gastrointestinal radiology • incontinence • MRI • pelvic imaging • pelvis
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Many authors have evaluated tests for predicting deterioration of function in the long term after anterior anal sphincter repair. The reported results of these studies are conflicting [11]. A study [12] with MRI found, in concordance with some physiologic studies [13-15], that atrophy of the EAS caused by pudendal nerve damage is associated with a poor outcome of anterior anal sphincter repair.
Imaging has a central position in the diagnostic workup of patients with fecal incontinence. Endoanal sonography and endoanal MRI both accurately showed anal sphincter defects [16-23]. Of the two techniques, only endoanal MRI accurately depicted EAS atrophy [12, 22-29], making it a likely tool for predicting functional outcome after anterior anal sphincter repair. Unfortunately, endoanal MRI is restricted to specialized centers because a dedicated device is needed and the introduction of the endoanal coil leads to discomfort. These two disadvantages of endoanal MRI might be overcome with the use of external phased-array coils. Previous studies have shown that MRI with external phased-array coils is accurate in revealing anal anatomy [30, 31] and the presence and extent of anorectal disease [32-34]. A recent study showed external phased-array MRI to be comparable to endoanal MRI in the depiction of IAS and EAS defects [35].
To our knowledge, no study has evaluated the diagnostic accuracy and reproducibility of MRI with external phased-array coils in depicting atrophy of the EAS in patients with fecal incontinence. If external phased-array MRI would be comparable to endoanal MRI in the depiction of EAS atrophy, as it is for the depiction of anal sphincter defects, external phased-array MRI would be preferable to use for selecting patients for anterior anal repair because this technique is more widely available and is less invasive.
The purposes of this prospective study were to compare external phased-array MRI to endoanal MRI for depicting atrophy of the EAS in patients with fecal incontinence and to evaluate observer reproducibility for the detection of EAS atrophy using both MRI techniques.
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Inclusion criteria were fecal incontinence for at least 6 months and failure of conservative treatment (including dietary measurements or medication). Excluded were patients younger than 18 and those who were diagnosed with an anorectal tumor or with a previous ileoanal or coloanal anastomosis. As these patients also participated in a clinical cohort study investigating the effects of physiotherapy, we also excluded those with soiling (leakage of fecal material out of the anus after normal defecation leading to perineal eczema), chronic diarrhea (always fluid stools, three or more times a day), overflow incontinence, proctitis, rectal prolapse, and patients who had received pelvic floor physiotherapy in the previous 6 months.
The patients of this study also participated in a large clinical cohort study evaluating the effects of pelvic floor physiotherapy. Patients underwent several diagnostic tests as part of the diagnostic cohort study. After testing, all patients underwent physiotherapy of the pelvic floor. Patients with failure of physiotherapy and an EAS defect without severe EAS atrophy were referred to the surgery department for anterior anal sphincter repair.
Medical History—Pudendal Nerve Terminal Motor Latency Testing
Data on medical history obtained from all patients included degree of fecal
incontinence and possible risk factors for pudendal nerve damage. The degree
of fecal incontinence was assessed according to the grading system of Vaizey
et al. [36]. This grading
system contains several incontinence-specific items and ranges from zero
(complete continence) to 24 (complete incontinence).
Possible risk factors for pudendal nerve damage are obstetric injuries in women (because of high-birth-weight infant, long second stage of labor, forceps delivery), neurologic disorders (cerebral, spinal, local), and diabetes mellitus [37].
Pudendal nerve terminal motor latency testing measures the time needed for the EAS to contract after stimulation of the pudendal nerve. Pudendal nerve terminal motor latencies were assessed in both hospitals, according to a standard procedure [38], on both the right and left sides using a St. Mark's Hospital electrode (Dantec Dynamics). Pudendal nerve terminal motor latency testing was performed in hospital 1 by residents of the gastroenterology department and in hospital 2 by a neurologist and residents of the neurology department. They were all experienced in performing and evaluating pudendal nerve terminal motor latency testing. Latencies were classified as pathologic when they were longer than 2.2 milliseconds.
MRI
Endoanal MRI and external phased-array MRI were performed according to
standard procedures on the same system on the same day. In hospital 1,
endoanal MRI was performed first, followed by external phased-array MRI. In
hospital 2, the order was reversed. Scan parameters were optimized for each
MRI system and coil based on extensive previous experience
[39,
40].
Endoanal MRI
Endoanal MRI was performed in both hospitals with a 1.5-T MR unit (hospital
1: Horizon Echo-Speed, GE Healthcare; hospital 2: Gyroscan ACS-NT, Philips
Medical Systems) and a dedicated 19-mm-diameter endoanal coil. All patients
were asked to fast 4 hours before the MRI examinations to reduce artifacts
from bowel peristalsis. Bowel relaxants were used in hospital 1 (1 mL of
butylscopolamine bromide [Buscopan, 20 mg/mL (Boehringer Ingelheim)] or 1 mg
of glucagon hydrochloride [GlucaGen (Novo Nordisk)]). In both hospitals, the
endoanal coil was covered with a condom, lubricated, and inserted in the anal
canal with the patient in a left lateral position. After positioning of the
endoanal coil, the patients turned in the supine position, and supportive pads
were used.
In hospital 1, the following T2-weighted fast spin-echo sequences were used for endoanal MRI: TR/TE 2,500/70; echo-train length, 10; field of view, 10 x 10 cm (axial) and 16 x 16 cm (coronal); imaging matrix, 256 x 512, slice thickness, 3 mm; interslice gap, 0.3 mm; excitations, 2. In hospital 2, imaging was performed by using the following T2-weighted fast spin-echo scan parameters: 3,000/80; echo-train length, 25; field of view, 20 x 20 cm (axial and coronal); imaging matrix, 256 x 512 (reconstruction matrix, 512 x 512); slice thickness, 3 mm; interslice gap, 0.3 mm; excitations, 4. Axial images and coronal images with slice orientation perpendicular and parallel to the anal sphincter and endoanal coil were obtained. All of the 15 patients within a hospital underwent an identical MRI protocol. The total imaging time was 15 minutes.
External Phased-Array MRI
In hospital 1, both the external phased-array coil and the endoanal coil
were positioned at the beginning of the procedure. External phased-array MRI
was performed after removal of the endoanal coil. In hospital 2, external
phased-array MRI was performed before endoanal MRI, with the endoanal coil
positioned after completion of the external phasedarray MRI sequences. All
patients were placed in the supine position with the pelvis centered at the
proximal end of a posterior phased-array spine coil in the feet-first
position. A body phased-array coil (hospital 2) or a quadrature phased-array
coil (hospital 1) was placed anteriorly.
In hospital 1, external phased-array MRI was performed by using the following T2-weighted fast spin-echo sequences: TR/TE, 2,500/70; echo-train length, 10; field of view, 30 x 30 cm; imaging matrix, 256 x 256 (axial) and 256 x 512 (coronal); slice thickness, 3 mm; interslice gap, 0.3; excitations, 2. In hospital 2, scan parameters were 3,000/80; echotrain length, 25; field of view, 20 x 20 cm; imaging matrix, 256 x 512 (reconstruction matrix 512 x 512; axial and coronal); slice thickness, 3 mm; interslice gap, 0.3; excitations, 6. Axial images and coronal images were obtained with slice orientation perpendicular and parallel to the long axis of the anal canal. All of the 15 patients within a hospital underwent an identical MRI protocol. The total imaging time was 15 minutes.
Image Analysis
Three radiologists (observers A, B, and C) with considerable abdominal MRI
experience, working in different hospitals, interpreted the MR images. Each
observer had a different level of experience in evaluating the anorectum,
pelvis, and pelvic floor with both MRI techniques. Observer A was more
experienced with external phased-array MRI (at least 600 examinations) than
with endoanal MRI (approximately 50 examinations). Observer B was familiar
with external phased-array MRI (approximately 500 examinations) but was more
experienced in evaluating endoanal MRI (approximately 1,000 examinations). The
experience level of observer C was similar for both MRI techniques
(approximately 200 examinations in each technique).
To compare both MRI techniques and to evaluate interobserver agreement, all observers evaluated separately the endoanal MRI and the external phased-array MRI examinations of all patients. The observers evaluated both techniques with at least 6 weeks in between to avoid recall bias.
To evaluate the intraobserver agreement of both techniques, all observers reevaluated 15 examinations of each MRI technique. The examinations for reinterpreting were randomly presented to the radiologists and were representative for the disease spectrum of the interobserver study. All observers performed the second interpretation after an interval of at least 4 weeks to avoid recall bias.
All observers were blinded to their own and to each other's results. They were unaware of any findings of pudendal nerve motor latency testing and of the medical history of the patients, except for age, sex, and the presence of fecal incontinence.
The MRI examinations were reviewed using workstation viewing software (IMPAX SP4 SU4 DS3000, Agfa HealthCare; Easy Vision Workstation, Philips Medical Systems; or eFilm Workstation 1.5.3, Merge eMed).
The radiologists evaluated and recorded the quality of the images as either adequate (moderate to good) or inadequate (poor) for interpretation, based on the presence of artifacts and identification of the EAS. Artifacts were classified as absent, motion artifacts (blurriness involving the complete image), peristalsis artifacts (blurriness in the phase-encoding direction), susceptibility artifacts, and artifacts related to the inner structure of the coil or suboptimal positioning of the coil. Identification of the EAS was scored as adequate (moderate to good) or inadequate (poor), based on the ability to evaluate the internal structure of the EAS.
The radiologists noted the presence of EAS atrophy, defined as thinning of the EAS muscle or diffuse replacement of EAS muscle by fat [23]. EAS atrophy was graded as none (no thinning of EAS and no replacement of EAS muscle by fat), mild (< 50% thinning of EAS or replacement of EAS muscle by fat), or severe (3 50% thinning of EAS or replacement of EAS muscle by fat). Atrophy was scored only when it comprised the whole circumference and length of the EAS.
In addition to evaluating the presence of EAS atrophy, a quantitative assessment of the EAS was performed by measuring the EAS thickness in millimeters at two points on a transverse image. Thickness was measured 1 cm cephalad to the lower border of the EAS at the 9-o'clock position of the right lateral side of the EAS. We arbitrarily chose the 9-o'clock position because we wanted to avoid interference from EAS defects, which are often located anteriorly [3, 6, 7]. The EAS was also measured at the point where it had the thickest volume. All three radiologists separately made both EAS thickness measurements.
The radiologists also evaluated the presence of an EAS defect, defined as discontinuity of the muscle ring (anatomic defect) and recognized by a hypointense deformation of the normal pattern of the muscle layer caused by replacement of muscle cells by fibrous tissue (functional defect, scar tissue) [23].
Statistical Analysis
The external phased-array MRI interpretations were compared with the
endoanal MRI interpretations. Because of the varying levels of experience in
evaluating the anorectum, pelvis, and pelvic floor, majority rule (at least
two of three observers) was used for the following parameters of interest:
image quality, artifacts, EAS identification, presence and grading of EAS
atrophy, and presence of EAS defects. For grading atrophy, a conservative rule
was used: if only two of three observers scored atrophy as present and these
observers disagreed about the level (mild or severe), then atrophy was noted
as mild. A mean value derived from all three observers' interpretations for
both of the EAS thickness measurements was calculated.
A McNemar test was used to test for differences between MRI techniques in the depiction of EAS atrophy. Cohen's kappa statistics with 95% CI were used to express agreement between both MRI techniques for the depiction of EAS atrophy and to express interobserver and intraobserver agreement of both techniques. Corresponding and discrepant diagnoses for grading EAS atrophy were noted.
To explore clinical associations of EAS atrophy, the MRI findings were related to available data from medical history and pudendal nerve terminal motor latency testing.
With a Student's t test for independent samples, we investigated whether a significant difference in EAS thickness measurements between patients with and without EAS atrophy occurred. A Student's t test for paired samples was used to evaluate whether a significant difference existed in EAS thickness measurements between both MRI techniques.
To assess the interobserver and intraobserver agreement in the EAS measurements, intraclass correlation coefficients with 95% CI were calculated.
For all statistical tests, p values below 0.05 were considered to show a statistically significant difference. The kappa values and intraclass correlation coefficients were interpreted as follows: < 0.20, poor agreement; 0.20-0.40, fair agreement; 0.41-0.60, moderate agreement; 0.61-0.80, good agreement; 0.81-1.00, very good agreement [41]. We used SPSS version 11.5 (Statistical Package for the Social Sciences) for Windows (Microsoft) and StatXact version 3.0 (Cytel Statistical Software) for Windows to perform statistical analysis of our data.
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In some patients, pudendal nerve terminal motor latencies could not be assessed on the right (n = 1) or left (n = 2) side. Pathologic pudendal nerve terminal motor latencies and possible risk factors for pudendal nerve damage are summarized in Tables 1 and 2.
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Image Quality
Endoanal MRI—The image quality of endoanal MRI and the EAS
identification was scored as adequate in all patients. Motion artifacts were
present in 11 patients, and artifacts related to the inner structure of the
endoanal coil and suboptimal positioning of the endoanal coil were shown in
four patients. These artifacts did not lead to an inadequate identification of
the EAS.
External phased-array MRI—Image quality of external phased-array MRI and the EAS identification was judged adequate in all patients. Artifacts were not shown.
Detection of EAS Atrophy
Endoanal MRI—With endoanal MRI, EAS atrophy was depicted in
11 patients. EAS atrophy was graded as none in 19 patients, mild in five
patients, and severe in six patients. The median EAS thickness was 3.5 mm
(range, 1.7-5 mm) at the right lateral side and 5 mm (range, 2.7-8.3 mm) at
the point where the EAS had the thickest volume.
Table 1 shows the findings from medical history and pudendal nerve terminal motor latency testing in patients with and without EAS atrophy at endoanal MRI. This table also shows the EAS thickness measurements and the number of EAS defects in patients with and without EAS atrophy.
We found a significant difference in EAS thickness at the point where the EAS had the thickest volume between patients with and those without EAS atrophy (p = 0.046). No such significant difference was seen for the EAS thickness at the right lateral side (p = 0.18).
External phased-array MRI—With external phased-array MRI, EAS atrophy was found in 13 patients. EAS atrophy was graded as none in 17 patients, mild in five patients, and severe in eight patients. The median EAS thickness was 4.1 mm (range, 1.9-7.7 mm) at the right lateral side and 5.7 mm (range, 2.9-8.3 mm) at the point where the EAS had the thickest volume.
Table 2 shows the findings from medical history and pudendal nerve terminal motor latency testing in patients with and without EAS atrophy at external phased-array MRI. This table also shows the EAS thickness measurements and the number of EAS defects in patients with and without EAS atrophy.
We found a significant difference in EAS thickness at the right lateral side between patients with and those without the presence of EAS atrophy (p = 0.02). No such significant difference could be seen for the EAS thickness at the point where the EAS had the thickest volume (p = 0.11).
External phased-array MRI compared with endoanal MRI—With
both imaging techniques, image quality and EAS identification were scored as
adequate in all patients. External phased-array MRI and endoanal MRI were not
significantly different in assessing EAS atrophy (p = 0.63). In
depicting EAS atrophy, both techniques agreed in 26 of 30 patients (87%)
( = 0.72; 95% CI = 0.48-0.97) (Figs.
1A,
1B,
1C,
1D,
2A,
2B,
3A, and
3B). Both techniques agreed in
23 of 30 patients (77%) in grading EAS atrophy
(Table 3).
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Patients with EAS atrophy at endoanal MRI were not significantly different from patients with EAS atrophy at external phasedarray MRI with respect to relevant medical history and pathologic pudendal nerve terminal motor latencies (data not shown).
Significant differences occurred between the two techniques in the EAS thickness measurements at the right lateral side (p = 0.004) and at the point where the EAS had the thickest volume (p = 0.005).
EAS atrophy in combination with an EAS defect was seen with endoanal MRI in two patients and with external phased-array MRI in five patients.
Reproducibility
Interobserver agreement in endoanal MRI— In the detection of
EAS atrophy, observers A and B agreed in 23 of 30 patients (77%), observers A
and C agreed in 24 of 30 (80%) patients, and observers B and C agreed in 23 of
30 patients (77%).
Table 4 shows the kappa values, with 95% CI, for interobserver agreement for detecting EAS atrophy and the reliability of EAS measurements with endoanal MRI.
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Interobserver agreement in external phasedarray MRI—In the detection of EAS atrophy, observers A and B agreed in 25 of 30 patients (83%), observers A and C agreed in 24 of 30 (80%) patients, and observers B and C agreed in 27 of 30 patients (90%).
Table 4 shows the kappa values, with 95% CI, for interobserver agreement for detecting EAS atrophy and the reliability of EAS measurements with external phased-array MRI.
Intraobserver agreement in endoanal MRI— In the detection of EAS atrophy with endoanal MRI, agreement occurred between the first and second interpretations in 14 of 15 patients (93%), 14 of 15 patients (93%), and 12 of 15 patients (80%) for observers A, B, and C, respectively.
Table 5 shows the kappa values, with 95% CI, for intraobserver agreement for detecting EAS atrophy and the reliability of the EAS measurements with endoanal MRI.
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Intraobserver agreement in external phased-array MRI—In the detection of EAS atrophy with external phased-array MRI, agreement occurred between the first and second interpretations in 14 of 15 patients (93%), nine of 15 patients (60%), and 12 of 15 patients (80%) for observers A, B, and C, respectively.
Table 5 shows the kappa values, with 95% CI, for intraobserver agreement for detecting EAS atrophy and the reliability of the EAS measurements with external phased-array MRI.
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=0.72) for the depiction of EAS atrophy. We found that the interobserver
agreement was moderate ( = 0.53-0.56) for endoanal MRI and moderate to
good ( = 0.55-0.8) for external phased-array MRI. The intraobserver
agreement was moderate to very good ( = 0.57-0.86) for endoanal MRI and
fair to very good ( = 0.31-0.86) for external phased-array MRI. A
number of potential limitations should be taken into account. The power of
this study is limited because the sample size of this study was relatively
small. We depicted EAS atrophy in approximately one third of patients. This
reflects daily clinical practice because EAS atrophy is not seen in all
patients with fecal incontinence
[9]. The patients of this study participated in a large clinical cohort study investigating the effects of physiotherapy, and some groups of patients were excluded for the cohort study. As a result, the group of patients participating in our study does not represent the full spectrum of fecal incontinence complaints and, therefore, our results cannot be unconditionally generalized to all patients with fecal incontinence.
Histology, obtained during surgery (anal sphincter repair), is the gold standard for demonstrating EAS atrophy. We did not use histology as the reference standard in this study because not all patients would have been eligible for anal sphincter repair. In this patient group, endoanal MRI found an EAS defect in 11 patients and external phased-array MRI found an EAS defect in 10 patients [35]. Further, EAS atrophy at endoanal MRI is an indicator for poor outcome of an anterior anal sphincter repair [12]. Although previous studies reported the diagnostic value of endoanal MRI and showed its superiority over endoanal sonography for demonstrating EAS atrophy [12, 22-29], we do not believe that endoanal MRI has been validated as a reference standard because only a single study has compared endoanal MRI findings with histology [28]. As no gold standard was available, we performed a comparative study between an experimental technique (i.e., external phased-array MRI) and an imaging technique accepted in daily practice (endoanal MRI) for the depiction of EAS atrophy.
The diagnosis of EAS atrophy was primarily made by the radiologists based on a visual subjective qualitative interpretation of thinning of the EAS muscle fibers, the diffuse replacement of EAS muscle by fat, or both. In clinical practice there are no "hard" criteria available for the visual diagnosis of EAS atrophy at MRI. This may have led in some patients to disagreement between both MRI techniques in assessing and grading EAS atrophy.
Quantitative measurements of the area of remaining EAS and of the percentage of fat content of the EAS were found to play a role in diagnosing EAS atrophy [12, 24, 28]. We found that the EAS thickness measurements at both techniques were smaller in patients with EAS atrophy compared with those without EAS atrophy. We showed a significant difference between patients with and without EAS atrophy in the EAS thickness at the point where the EAS had the thickest volume at endoanal MRI and in the EAS thickness at the right lateral side at external phased-array MRI. It seems that diminished EAS measurements with both MRI techniques were associated with EAS atrophy.
The EAS thickness measurements at endoanal MRI were significantly smaller compared with the thickness measurements at external phased-array MRI. This could be explained by the introduction of the endoanal coil with endoanal MRI leading to stretching of the anal sphincter muscles, with subsequently smaller thickness measurements.
In the literature, opinions about the diagnostic value of pudendal nerve terminal motor latency in assessing EAS atrophy are conflicting [42]. Our study showed that most patients with EAS atrophy had at least a pathologic pudendal nerve terminal motor latency at one side. Yet, in some patients with EAS atrophy no pathologic pudendal nerve terminal motor latencies were seen. This can be explained by the fact that with pudendal nerve terminal motor latency testing only the conduction time of the fastest muscle fibers is measured [9].
Our group has shown that the spatial resolution of external phased-array MRI in this patient group, despite slight differences in spatial resolution between both hospitals for external phased-array MRI, was as effective as endoanal MRI for adequate image quality and identification of the anal sphincter muscles [35].
The demarcation of the EAS is sometimes unclear at the anterior part of the EAS, which may result in discrepancies in diagnosing EAS defects. In contrast, the delineation of the remaining major part of the EAS to the surrounding tissues is clearer. Further, fat results in a high signal at MRI and is therefore easily recognized within the EAS, which has relatively low signal intensity. These two arguments may be an explanation for the good agreement between both techniques for the depiction of EAS atrophy.
To our knowledge this is the first study evaluating observer reproducibility in assessing EAS atrophy with MRI. In line with the findings of a recent study of interobserver agreement for detecting EAS defects [35], we found weak interobserver agreement for the detection of EAS atrophy. The weak interobserver agreement is most likely explained by frame-of-reference differences among the observers. These differences might result from unfamiliarity with changes in sphincter morphology that occurs in EAS atrophy. The fact that, as described previously, no hard criteria are available for the visual diagnosis of EAS atrophy and that there is a relative scarcity of papers on EAS atrophy assessed at MRI may result in a higher contribution of personal experience in interpretation. This point of view is supported by the fact that intraobserver agreement was stronger for each observer when interpreting the specific MRI technique with which he or she was most familiar. We found, overall, a weak reproducibility among and within observers for EAS measurements for both MRI techniques.
Further studies evaluating MRI with histology are mandatory to develop criteria for assessing and grading atrophy based on either qualitative or quantitative interpretation. Radiologists can then be trained in interpreting endoanal MRI and external phased-array MRI to assess EAS atrophy. This process can be expected to increase reproducibility and to improve reviewer performance for both MRI techniques.
Based on the findings of this study, we conclude that external phased-array MRI is as suitable as endoanal MRI for depicting EAS atrophy in patients with fecal incontinence. Because interobserver agreement is weak and intraobserver agreement was found to be related to the experience level of the observer with each MRI technique, both external phased-array MRI and endoanal MRI can be used in the selection of patients who might benefit from anal sphincter repair in the diagnostic workup of fecal incontinence only if sufficient experience is available.
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