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Ultrasonography |
1 From the Intestinal Imaging Centre (A.F., S.H., C.I.B.), Department of Cellular Pathology (A.B.P.), and Physiology Unit (A.F., M.A.K.), St Mark’s Hospital, Level 4V, Northwick Park, Watford Rd, Harrow, London HA1 3UJ, England; and Department of Obstetrics and Gynecology, University Graz, Austria (A.F., R.W.). Received May 31, 2001; revision requested June 18; revision received August 27; accepted October 10. Address correspondence to S.H. (e-mail: s.halligan@ic.ac.uk)
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ABSTRACT |
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 TOP ABSTRACT INTRODUCTIONMATERIALS AND METHODS RESULTSDISCUSSIONREFERENCES |
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MATERIALS AND METHODS: One hundred fifty asymptomatic nulliparous women (mean age, 31 years; range, 19–80 years) underwent endoanal US with a high-frequency 10-MHz transducer. Anal canal structures were measured at high, middle, and low levels and were correlated with age by using the Pearson simple linear correlation coefficient.
RESULTS: Internal sphincter thickness showed a highly significant positive correlation with age at both sites at which it was measured (high anal canal, r = 0.34, P < .001; middle anal canal, r = 0.33, P < .001). External sphincter thickness showed a highly significant negative correlation with age at all sites measured (high anal canal, r = -0.65, P < .001; middle anal canal, r = -0.49, P < .001; low anal canal, r = -0.21, P = .012). There was no significant correlation between age and thickness of subepithelial tissue, longitudinal muscle, or puborectalis muscle. Subjects whose internal sphincter showed mixed echogenicity were significantly older than those whose internal sphincter was uniformly hypoechoic (mean, 47.4 vs 34.6 years; P < .001). Subjects with mixed internal sphincter echogenicity also had a significantly thinner external sphincter at high (mean thickness, 3.8 vs 4.6 mm; P < .001) and middle (mean thickness, 3.7 vs 4.1 mm; P = .03) anal canal levels.
CONCLUSION: At older ages there are increased internal anal sphincter thickness and decreased external anal sphincter thickness. Diagnosis of external sphincter atrophy on the basis of sphincter thinning requires that one distinguish between abnormal thinning and age-related differences.
© RSNA, 2002
Index terms: Aging • Anus, abnormalities, 757.79 • Anus, US, 757.12981
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODS RESULTSDISCUSSIONREFERENCES |
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Anal sphincter atrophy or degeneration is an increasingly common diagnosis (5,6). Internal sphincter degeneration was first described by using endoanal US, and diagnosis hinges on US demonstration of a sphincter that is intact but thinner than expected (5). External sphincter atrophy was first described by using endoanal magnetic resonance (MR) imaging (6) and also depends on finding a thinner sphincter than expected. Although the internal sphincter is well visualized at US, external sphincter boundaries are more difficult to define, resulting in the suggestion that only endoanal MR imaging can demonstrate the changes in external sphincter morphology that accompany atrophy (7). However, the findings of a recent study (8) suggest that US diagnosis may be possible because inability to define the outer border of the external sphincter correlates with subsequent physiologic and MR imaging-based diagnosis of atrophy.
No matter which modality is used, measurements of sphincter thickness are central to diagnosis of atrophy or degeneration. However, these measurements are likely to be confounded by age-related changes in sphincter morphology. Findings of small US studies suggest that the internal sphincter thickens with age (9), but to our knowledge, there is little work relating to the external sphincter. Furthermore, there are few endoanal US studies dealing specifically with asymptomatic women, and, in addition, patients studied have been from a relatively young and narrow age range. Moreover, at the time the current article was written, all studies had involved the use of a 7-MHz transducer (10–12). The introduction of a 10-MHz transducer (model 6004; B&K Medical, Gentofte, Denmark) with near-field focusing (5–45 mm) has enabled individual sphincter components to be resolved with higher spatial resolution. The aim of this study was to evaluate endoanal US anatomy in a large group of nulliparous women (to eliminate any effect of childbirth) by using a high-frequency 10-MHz transducer to define normal age-related differences in sphincter morphology.
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MATERIALS AND METHODS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODS RESULTSDISCUSSIONREFERENCES |
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All women were nulliparous. Their ages were 19–80 years (mean age, 31 years ± 15.2 [SD]; median age, 36 years). All subjects verbally completed an anal continence (13) and constipation (14) questionnaire and were excluded if there were any symptoms of passive or urge fecal incontinence or any other anorectal dysfunction (mild constipation and/or laxatives at low doses were allowed in women 65 years of age or older). Women were also excluded if there was a history of previous pelvic floor surgery, irritable bowel syndrome, diabetes mellitus, or neurologic disorder. Women were attending the clinic for conditions unrelated to bowel dysfunction, such an abnormal cervical smear test results, infertility, ovarian cysts, or postmenopausal bleeding.
Scanning and Data Collection
Endoanal US was performed by using a dedicated unit (model 3535 scanner, with model 1850 endoprobe and model 6004 10-MHz transducer; B&K Medical, Gentofte, Denmark). The transducer was covered with a hard plastic sonolucent cone with an outer diameter of 1.7 cm. The transducer has a focal range of 5–45 mm, a transverse resolution of less than 0.05 mm, and a lateral resolution of 0.5–1.0 mm. The assembly was filled with degassed water for acoustic coupling and was covered with a lubricated condom for insertion. Endoanal US was well tolerated by all volunteers.
Subjects underwent scanning in the prone position to avoid perineal asymmetry (15), with the image oriented so that anterior was uppermost. All volunteers underwent scanning by the same examiner (A.F.) at both sites. The endoprobe was gently inserted into the anus to the level of the anorectal verge. During slow withdrawal of the probe, images were obtained high, in the middle of, and low in the anal canal. The high anal canal was defined as the level midway between the inferior border of the puborectalis muscle and complete formation of the external sphincter ring anteriorly (Fig 1a). The middle canal level was defined by the completion of the external sphincter ring anteriorly in combination with maximum internal sphincter thickness (Fig 1b). The low canal level was defined as that immediately caudal to the termination of the internal sphincter and comprised the subcutaneous external sphincter (Fig 1c). External anal sphincter thickness was measured at all three anal canal levels. Internal sphincter and longitudinal muscle thickness was measured at high and middle anal canal levels only, because of their termination within the low anal canal. If a separate intersphincteric fat plane was distinguished lateral to the longitudinal muscle, it was incorporated into the measurement of longitudinal muscle thickness. The subepithelium (defined as the layer between the external cone surface and the inner border of the internal sphincter) was measured at all three levels. All measurements were obtained at the 3 o’clock position (Fig 2). In addition, the thickness of the anterior ring (the anterior condensation of the external sphincter and longitudinal muscle) was measured at the 12 o’clock position at the level of the middle anal canal, and it was determined whether the external sphincter could be distinguished from the longitudinal muscle at this site. Any muscle slips related to the external sphincter that would result in anterior perineal asymmetry were noted.
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At Northwick Park Hospital, measurements were obtained at the time of examination by using electronic calipers that were accurate to 0.1 mm. At University Graz, images were digitally stored by using a personal computer with a picture acquisition and communication system (Medimage; Vepro, MHS Medizintechnik Vienna, Austria) and measurements obtained subsequently by the same investigator by using software calipers accurate to 0.01 mm.
Data Analysis
The mean and SD of structural anal canal measurements were calculated and any relationship with age and body mass index determined by using the Pearson simple linear correlation coefficient, with statistical significance assigned to a probability level of less than .05. Calculations were performed with Arcus Quickstat Biomedical software, version 1.2 (Research Solutions, Cambridge, England).
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RESULTS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODS RESULTSDISCUSSIONREFERENCES |
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Internal Sphincter
Internal sphincter thickness showed a highly significant positive correlation with age at both sites at which it was measured (Table, Fig 3). The internal sphincter was homogenously hypoechoic in 76 (76%) of the 100 subjects in whom this characteristic was noted (Fig 4). The internal sphincter border with adjacent structures (subepithelium medially and longitudinal muscle laterally) was ill defined to a variable degree in 28 (28%) subjects, 20 of whom also showed the internal sphincter as somewhat hyperechoic (Fig 4). Another four subjects showed some internal sphincter hyperechogenicity, so that this feature was present in 24 (24%) subjects overall. Subjects whose internal sphincter showed mixed echogenicity were significantly older than those whose internal sphincter was uniformly hypoechoic (mean age, 47.4 vs 34.6 years; P < .001, unpaired t test). These patients also had a significantly thinner external sphincter at high (mean thickness, 3.8 vs 4.6 mm; P < .001) and middle anal canal levels (mean thickness, 3.7 vs 4.1 mm; P = .03). No other comparison was significant.
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External Sphincter
The mean external sphincter thickness is given in the Table. The outer border of the external sphincter was difficult to define in three (2%) subjects at all three levels and in five (3%) subjects at the subcutaneous level only. Measurements were not obtained at these levels in these subjects. In contrast with that of the internal sphincter, the thickness of this muscle showed a highly significant negative correlation with age at all levels measured (Table, Fig 5).
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Body Mass Index
Longitudinal muscle thickness correlated positively with body mass index at both high (r = 0.22, P = .03) and middle (r = 0.23, P = .02) anal canal levels. Internal sphincter thickness also positively correlated with body mass index at the level of the middle anal canal (r = 0.23, P = .02) but not at the level of the high anal canal (r = 0.09, P = .35). External sphincter thickness negatively correlated with body mass index at high (r = -0.25, P = .01) and middle (r = -0.21, P = .04) anal canal levels but did not correlate at the subcutaneous level (r = -0.01, P = .95). Neither puborectalis muscle (r = 0.06, P = .53) nor anterior ring (r = -0.14, P = .16) thickness showed any correlation with body mass index.
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DISCUSSION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODS RESULTSDISCUSSIONREFERENCES |
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Several endoanal US studies have included asymptomatic subjects as controls, but at the time this article was written, very few investigators (1,10) had focused on normal anatomy, and even fewer (9,11) had specifically sought age-related differences in sphincter morphology. Burnett and Bartram (9) were the first to investigate age-related changes and studied 42 asymptomatic volunteers, 24 of whom were women. Using a 7-MHz transducer, they found a significant tendency for the internal sphincter to be thicker at older ages, but technical developments at that time restricted sphincter measurements to 1-mm increments—a serious limitation when measuring such a small structure. They also found that internal sphincter echogenicity was greater at older ages, but there was no external sphincter measurement (9). Nielsen and colleagues (11) also used a 7-MHz transducer to examine 20 asymptomatic women and related differences to age, also finding a tendency for the internal sphincter to be thicker at older ages. The external sphincter was measured, but no significant relationship was found, possibly because of small numbers, caliper limitations, or inclusion of the longitudinal muscle and intersphincteric plane in external sphincter measurements (11). Sultan and colleagues (12) examined 93 nulliparous volunteers as part of a study of the effects of subsequent vaginal delivery on the anal sphincter; consequently, all volunteers were pregnant at the time of examination, with a median age of 27 years. Because the oldest subject was only 41 years of age, the authors were unable to determine age-related sphincter differences.
Measurements of muscle thickness are clinically important because they are central to diagnosis of sphincter atrophy (5,7). Atrophy has been best characterized in the internal sphincter, for which a new and discrete clinicopathologic entity, idiopathic internal anal sphincter degeneration, has been described (5). Investigators in a study of 45 patients with intact sphincters and passive anal incontinence (5) found a thin and hyperechoic internal sphincter, often with indistinct borders, in all 38 subjects in whom US findings were available for review. Furthermore, all patients had low resting anal canal pressures in combination with normal squeeze pressures and no evidence of pudendal neuropathy (5). Idiopathic internal anal sphincter degeneration has subsequently become a common diagnosis in our practice and affects primarily patients older than those with obstetric sphincter trauma. Because of this, a large study of age-related US changes in asymptomatic individuals is central to defining atrophy. We found a highly significant tendency for the internal sphincter to be thicker at older ages at both levels at which it was measured. Measurements for day-to-day clinical diagnosis would usually be obtained at the level of the middle anal canal. Furthermore, the internal sphincter showed some evidence of mixed echogenicity in 24% of our volunteers who were significantly older than others, suggesting that this is also an age-related difference.
We believe ours to be the first endoanal US study in which significant thinning of the external sphincter was demonstrated at older ages, a phenomenon present at all three levels measured. The anterior sphincter ring also was significantly thinner at older ages, probably because this measurement incorporated the external sphincter. We could not find any age-related differences for the subepithelial tissues, longitudinal muscle, or puborectalis muscle. As with the internal sphincter, atrophy also affects the external sphincter and has been identified by using endoanal MR imaging (6–8,18). Although not as well characterized as internal sphincter degeneration, there is good evidence that external sphincter atrophy is also a distinct clinicopathologic entity; in a study of 20 women undergoing sphincter repair after obstetric trauma (7), preoperative MR imaging-based diagnosis of external sphincter atrophy enabled prediction of poor symptomatic outcome. In a subsequent study in which endoanal MR imaging was used to quantify external sphincter bulk (18), and the proportion of muscle was replaced by fat (a process occurring during atrophy), it was possible to discriminate between incontinent subjects and control subjects.
In the largest study at the time this article was written in which endoanal MR imaging was performed in asymptomatic volunteers (19), there was a tendency for the external sphincter to be thinner at older ages in 50 men and 50 women. It has frequently been suggested that accurate external sphincter measurement is impossible at endoanal US, because the lateral borders of this muscle are not as well defined as at endoanal MR imaging. However, we found the lateral external sphincter border difficult to define in only three (2%) subjects at all three levels measured and in five (3%) subjects at the subcutaneous level only. Furthermore, interobserver agreement for external sphincter thickness measurement with US is good (17), suggesting that landmark identification is both possible and accurate when performed by experienced observers. This is likely a result of increasingly frequent application of both endoanal MR imaging and US in the same subject, a procedure likely to enhance familiarity with muscle boundaries. In a recent study in which endoanal MR imaging, endoanal US, and phased-array MR imaging were used (20), both MR imaging modalities were superior to endoanal US for measurement of the external anal sphincter but were equivalent for measurement of the internal anal sphincter. However, strength of agreement was determined with intraclass correlation rather than with calibration against a known measurement; the results may reflect a degree of unfamiliarity with endoanal US muscle boundaries (20). A limitation of our study was that a single observer performed all measurements, at the time of examination in 50 women and subsequently (approximately 6 months after recruitment had ended) in the remaining 100. There was no attempt to determine interobserver variation in the present study.
The internal sphincter is composed of smooth muscle; hence, the term degeneration has been used to describe wasting, whereas the external sphincter is composed of striated muscle, leading to adoption of the term atrophy. Increased echogenicity at US in patients with primary degeneration has been shown histologically to correlate with replacement of smooth muscle by fibrous tissue (5). External sphincter atrophy may be related to age or other unknown factors. Whether there are changes in addition to loss of striated muscle bulk is unknown. The external and internal sphincters are innervated differently. Many muscles degenerate to some degree with age, but it is unknown why a particular sphincter muscle is singled out in certain individuals.
Whether internal sphincter degeneration and external sphincter atrophy can occur in the same patient and share a common cause are currently unknown, but the possibilities seem likely. Because diagnosis of sphincter atrophy is increasingly common (5,7,8,18), it will be important to distinguish abnormal thinning from physiologic age-related sphincter differences. This should not be a problem in the internal sphincter, since degeneration thins the muscle against a background of age-related differences in thickness. The situation is very different for the external sphincter; atrophy thins the muscle, but the muscle is also thinner at older ages, and it may be difficult to distinguish sufficiently between the two. Further studies are required.
In conclusion, at older ages there are increased thickness of the internal sphincter and decreased thickness of the external sphincter. For diagnosis of anal sphincter atrophy, which depends on US demonstration of abnormally thin sphincters, abnormal thinning must be distinguished from normal physiologic age-related sphincter differences.
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FOOTNOTES |
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REFERENCES |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODS RESULTSDISCUSSIONREFERENCES |
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This article has been cited by other articles:
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