The Utility of Pudendal Nerve Terminal Motor Latencies in Idiopathic Incontinence Rocco Ricciardi, M.D., Anders F. Mellgren, M.D., Ph.D., Robert D. Madoff, M.D., Nancy N. Baxter, M.D., Ph.D., Richard E. Karulf, M.D., Susan C. Parker, M.D. Division of Colon & Rectal Surgery, University of Minnesota, Minneapolis, Minnesota and 2.4-ms thresholds. 4) Unilaterally prolonged pudendal nerve terminal motor latency was not associated with maximum mean resting pressure, maximum mean squeeze pressure, or fecal incontinence score at either threshold. CONCLUSIONS: The majority of incontinent patients with intact sphincters have normal pudendal nerve terminal motor latency. Bilaterally but not unilaterally prolonged pudendal nerve terminal motor latency is associated with poorer function and physiology in the incontinent patient with an intact sphincter. [Key words: Pudendal latency; Pudendal nerve terminal motor latency; Incontinence; Anal sphincter; Neuropathic]
PURPOSE: Pudendal nerve terminal motor latency testing has been used to test for pudendal neuropathy, but its value remains controversial. We sought to clarify the relationship of pudendal nerve terminal motor latency to sphincter pressure and level of continence in a cohort of patients with intact anal sphincters and normal pelvic floor anatomy. METHODS: We reviewed 1,404 consecutive patients who were evaluated at our pelvic floor laboratory for fecal incontinence. From this group, 83 patients had intact anal sphincters on ultrasound and did not have internal or external rectal prolapse during defecography. These patients were evaluated by pudendal nerve terminal motor latency testing, a standardized questionnaire, and anorectal manometry, which measured resting and squeeze anal pressures. Incontinence scores were calculated by using the American Medical Systems Fecal Incontinence Score. Values were compared by using the Fisher’s exact test and Wilcoxon’s rank-sum test; and significance was assigned at the P < 0.05 level. RESULTS: 1) Using a 2.2-ms threshold, 28 percent of patients had prolonged pudendal nerve terminal motor latency unilaterally and 12 percent bilaterally. 2) At a 2.4-ms threshold, 18 percent of patients had prolonged pudendal nerve terminal motor latency unilaterally and 8 percent bilaterally. 3) Bilaterally prolonged pudendal nerve terminal motor latency was significantly associated with decreased maximum mean resting pressure and increased Fecal Incontinence Score, but not decreased maximum mean squeeze pressure, at both 2.2-ms
F
ecal incontinence is an incapacitating condition, which often leads to social isolation.1 The causes of fecal incontinence are numerous, and physiologic evaluation is widely used for diagnosis and treatment planning. In addition to medical conditions that can lead to fecal incontinence, other etiologies can be divided into improper muscle function and/or improper neural function.2 Structural pelvic floor muscle abnormalities are common after obstetric injuries or after perineal or pelvic surgery. Evaluation of muscular structure and function is most often accomplished by endoanal ultrasound and anal manometry. At evaluation a number of patients are found to have weak anal sphincters that are intact on examination with endoanal ultrasonography. It is widely presumed that these patients have poor function because of idiopathic causes.3 Although single-fiber electromyography (EMG) is the most sensitive measure of pudendal nerve dysfunction,4 the discomfort and lack of familiarity of single-fiber EMG limit its clinical use.5 In addition, EMG is dependent on age,
Presented at the meeting of The American Society of Colon and Rectal Surgeons, Dallas, Texas, May 8 to 13, 2004. Reprints are not available. Correspondence to: Rocco Ricciardi, M.D., Division of Colon & Rectal Surgery, Department of Surgery, University of Minnesota Medical School, MMC 450, 420 Delaware Street, SE, Minneapolis, Minnesota 55455 Dis Colon Rectum 2006; 49: 852–857 DOI: 10.1007/s10350-006-0529-y * The American Society of Colon and Rectal Surgeons Published online: 10 April 2006
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gender, temperature and muscle fiber composition, length, fiber diameter, and firing frequency.5 Given that the relationship between EMG recording and physiologic variables is not confirmed,5 alternative methods have been evaluated. One alternative to diagnose pudendal neuropathy is to use a glovemounted (St. Mark’s) electrode to measure pudendal nerve conduction time (pudendal nerve terminal motor latency). Prolonged pudendal nerve terminal motor latency is associated with pudendal neuropathy,6 but the sensitivity and specificity of the test have not been clearly established. The relative ease and simplicity of pudendal nerve terminal motor latency recordings have popularized the role of this test at anorectal physiology testing facilities throughout North America and Europe. Yet, the value of pudendal nerve terminal motor latency determinations in defining pudendal neuropathy remains controversial. We sought to clarify the value of pudendal nerve terminal motor latency determinations in patients with intact anal sphincters and normal pelvic floor anatomy. These incontinent patients, presumed to have neuropathic fecal incontinence, should theoretically manifest elevated pudendal nerve terminal motor latency recordings. We also compared pudendal nerve terminal motor latency determinations to sphincter pressures and degree of incontinence to evaluate presumed relationships. This study was designed to assess the value of pudendal nerve terminal motor latency in the workup of patients with fecal incontinence.
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anorectal surgery or other trauma without an obvious sphincter defect on ultrasound remained in our study. The exclusions left 83 patients with intact sphincters and normal pelvic floor anatomy suffering from persistent fecal incontinence despite alterations in diet and medication. These 83 patients returned for several evaluations and consultations regarding incontinence treatment and represent our study population.
Incontinence Scores Incontinence scores were calculated by using the Fecal Incontinence Score developed by American Medical Systems. This index addresses the leakage of gas, mucous, liquid, or solid stool at varying frequencies (see Appendix).8 Cumulative scores for questionnaires were calculated for each patient.
Anorectal Manometry Anorectal manometry was performed by using a water-perfused manometry system and Duet software (Medtronic Diagnostics, Minneapolis, MN). A stationary pull-through technique with an eightchannel water-perfused catheter was used. Anal resting and squeeze pressures were recorded at each centimeter starting at 6 cm from the anal verge. The mean pressures of four channels were calculated at each level and thereafter the highest mean pressure was chosen as the maximal mean resting pressure and the maximal mean squeeze pressure.
METHODS A retrospective review was performed of the 1,404 patients evaluated for fecal incontinence from January 1999 to June 2003 at the Center for Pelvic Floor Disorders in Minneapolis, Minnesota. The protocol was approved by the Institutional Review Board at the University of Minnesota. Patients were evaluated with a standardized questionnaire and physiologic evaluation. All patients with internal or external rectal prolapse at defecography or sphincter injuries on endoanal ultrasound were excluded. Rectal prolapse patients were excluded because of previous work demonstrating elevated pudendal latencies in this group of patients.7 Given that rectoceles are thought to represent a normal variant unless associated with symptoms, we did not exclude rectoceles, enteroceles, or those patients with increased pelvic floor descent. In addition, those patients who had
Pudendal Nerve Terminal Motor Latency Pudendal nerve terminal motor latency examinations were performed with patients in the right lateral position on both the left and right sides of the external anal sphincter as described by Rogers et al.9 Pudendal nerve terminal motor latency was stimulated via a St. Mark’s electrode (Dantec-Medtronics, Minneapolis, MN) and recorded (Medtronic Diagnostics). Two latencies were recorded on each side and the shorter latency was used for analyses. The technicians who perform pudendal nerve terminal motor latency testing repeat recordings until a satisfactory waveform is obtained. Several recordings are at times taken before a satisfactory waveform is accepted. In addition, all tracings were reviewed by study authors (AFM and SCP) before pudendal nerve terminal motor latency value acceptance.
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Statistics Comparisons of data were made by using Fisher’s exact test and Wilcoxon’s rank-sum test. P < 0.05 was considered statistically significant.
RESULTS Demographics and Pudendal Nerve Terminal Motor Latency Demographics of our study group are detailed in Table 1. Mean pudendal nerve terminal motor latency was 2.12 T 0.36 (range, 1.50–3.70) ms on the left and 2.13 T 0.30 (range, 1.58–2.90) ms on the right. At least one pudendal nerve terminal motor latency determination of e2.2 ms was noted in 88 percent of patients. At a threshold of >2.2 ms, 28 percent of patients had prolonged pudendal nerve terminal motor latency unilaterally and 12 percent had bilaterally prolonged pudendal nerve terminal motor latency. At a 2.4-ms threshold, 18 percent of patients had prolonged pudendal nerve terminal motor latency unilaterally and 8 percent had bilaterally prolonged pudendal nerve terminal motor latency bilaterally.
Anal Manometry The range of maximum mean resting pressures was 13 to 105 and averaged 45.9 T 21.7. The range of maximum mean squeeze pressures was 11 to 149 and averaged 42.8 T 31.1.
Fecal Incontinence Score The American Medical Systems Fecal Incontinence Score ranged from 31 to 115 and averaged 77.8 T 24.8, reflecting severe disease. Review of the data demonstrates that at least 84 percent of all patients experienced at least several daily episodes of ‘‘minor bowel soilage or seepage’’ (Fecal Incontinence Score >55). All patients experienced at a minimum several episodes of ‘‘accidental bowel leakage of gas’’ (Fecal Incontinence Score >25).
Table 1. Demographics Age (yr) Female No. of vaginal deliveries Hysterectomy rate
58 T 11 90.4% 3 T 1.2 52%
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Unilaterally Prolonged Pudendal Nerve Terminal Motor Latency Unilaterally prolonged pudendal nerve terminal motor latency >2.2 ms was present in 23 of 83 patients (28 percent; Table 2). There was no difference in maximum mean resting pressures or maximum mean squeeze pressures in patients with unilaterally prolonged pudendal nerve terminal motor latency >2.2 ms compared with patients with pudendal nerve terminal motor latency e2.2 ms. Also, Fecal Incontinence Scores of patients with unilaterally prolonged pudendal nerve terminal motor latency >2.2 ms was similar to the Fecal Incontinence Scores of patients with normal pudendal nerve terminal motor latency. Unilaterally prolonged pudendal nerve terminal motor latency >2.4 ms was present in 15 of 83 patients (18 percent). There was no difference in maximum mean resting pressures or maximum mean squeeze pressures in patients with unilaterally prolonged pudendal nerve terminal motor latency >2.4 ms compared with patients with pudendal nerve terminal motor latency e2.4 ms. Also, Fecal Incontinence Scores of patients with unilaterally prolonged pudendal nerve terminal motor latency >2.4 ms was similar to the Fecal Incontinence Scores of patients with normal pudendal nerve terminal motor latency.
Bilaterally Prolonged Pudendal Nerve Terminal Motor Latency Bilaterally prolonged pudendal nerve terminal motor latency was associated with decreased maximum mean resting pressure and increased Fecal Incontinence Scores, but not decreased maximum mean squeeze pressure, at both 2.2-ms and 2.4-ms thresholds. Bilaterally prolonged pudendal nerve terminal motor latency >2.2 ms was present in 10 of 83 patients (12 percent). Maximum mean resting pressure in patients with bilaterally prolonged pudendal nerve terminal motor latency >2.2 ms was
Table 2. PNTML Values One or two normal PNTML Unilateral PNTML >2.2 ms Unilateral PNTML >2.4 ms Bilateral PNTML >2.2 ms Bilateral PNTML >2.4 ms
73 23 15 10 7
(88) (28) (18) (12) (8)
PNTML = pudendal nerve terminal motor latency. Values at 2.2-ms and 2.4-ms threshold for the study group.
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Figure 1. Maximum mean resting pressure (MMRP), maximum mean squeeze pressure (MMSP), and Fecal Incontinence Scores (FIS) for bilateral pudendal nerve terminal motor latency (PNTML) recordings e 2.2 ms compared with >2.2 ms.
30.7 T 11.5 but 47.9 T 22 in patients with pudendal nerve terminal motor latency e2.2 ms (P < 0.05). There was no difference in maximum mean squeeze pressure in patients with bilaterally prolonged pudendal nerve terminal motor latency >2.2 ms compared with patients with pudendal nerve terminal motor latency e2.2 ms. Fecal Incontinence Scores of patients with bilaterally prolonged pudendal nerve terminal motor latency >2.2 ms was 93.5 T 23.1 but 76.1 T 24.7 in patients with pudendal nerve terminal motor latency e2.2 ms (P < 0.05) (Fig. 1). Bilaterally prolonged pudendal nerve terminal motor latency >2.4 ms was present in 7 of 83 patients (8 percent; Table 2). Maximum mean resting pressure in patients with bilaterally prolonged pudendal nerve terminal motor latency >2.4 ms was 26.4 T 5.1 but 47.6 T 21.8 in patients with pudendal nerve terminal motor latency e2.4 ms (P < 0.05). There was no difference in maximum mean squeeze pressure in patients with bilaterally prolonged pudendal nerve terminal motor latency >2.4 ms compared with patients with pudendal nerve terminal motor latency e2.4 ms. Fecal Incontinence Scores of patients with bilaterally prolonged pudendal nerve terminal motor latency >2.4 ms was 104 T 7.2 but 75.8 T 24.7 in patients with pudendal nerve terminal motor latency e2.4 ms (P < 0.05; Fig. 2).
DISCUSSION ‘‘Idiopathic’’ fecal incontinence is diagnosed when patients have anatomically intact anal sphincters but poor sphincter function. The cause of idiopathic incontinence is widely believed to be a result of traction injury of the pudendal nerves, most fre-
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Figure 2. Maximum mean resting pressure (MMRP), maximum mean squeeze pressure (MMSP), and Fecal Incontinence Scores (FIS) for bilateral pudendal nerve terminal motor latency (PNTML) recordings e 2.4 ms compared with >2.4 ms.
quently caused by prolonged labor or chronic straining with defecation. Although histologic studies have shown evidence of external anal sphincter denervation in patients with idiopathic incontinence, and single-fiber EMG studies have shown evidence of muscle reinnervation, most laboratories now use pudendal nerve terminal motor latency determination by a glove-mounted St. Mark’s electrode to diagnose pudendal neuropathy. We found that the vast majority of our patients with idiopathic fecal incontinence had normal pudendal nerve terminal motor latency recordings. Only a small percentage of patients demonstrated abnormal pudendal nerve terminal motor latency recordings on one side and an even smaller number demonstrate bilaterally prolonged latencies. Patients with unilaterally prolonged pudendal nerve terminal motor latency values did not manifest any differences in manometric recordings or incontinence scores compared with patients with normal pudendal nerve terminal motor latency recordings. Those patients with bilaterally prolonged pudendal nerve terminal motor latency >2.2 ms had impaired sphincter function and more severe incontinence scores. These findings suggest that pudendal nerve terminal motor latency has poor sensitivity to detect pudendal nerve damage or that something other than pudendal nerve injury is the cause of idiopathic fecal incontinence. This study evaluated a cohort of incontinent patients with intact anal sphincters as documented by ultrasound and normal pelvic floors as defined by defecography. A recent Danish study attempted to perform a similar analysis, but the authors did not completely exclude pelvic floor abnormalities.10 In
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their study, the authors did not perform routine endoanal ultrasound, routine defecography, or ascertain complete obstetric history. The resultant effect may be the inclusion of patients with occult anal sphincter defects or pelvic floor prolapse. Sphincter defects and prolapse are associated with prolonged pudendal nerve latencies from muscle stretching or disruption.11,12 We elected to include only those patients with proven intact pelvic floors who are presumed to have fecal incontinence from neuropathy. Pudendal nerve terminal motor latency is a relatively simple modality to evaluate anal sphincter innervation. The reliability of pudendal nerve testing has been confirmed with relatively good reproducibility between observers.13 Yet, it is generally accepted that performance and interpretation of pudendal nerve terminal motor latency requires significant expertise and experience. It is the lack of expertise in pudendal nerve terminal motor latency technique that has limited the universal application of this technology among colorectal surgeons. A survey of The American Society of Colon and Rectal Surgeons membership revealed routine use of pudendal nerve terminal motor latency in only 15 percent of American anorectal physiology laboratories.14 Pudendal nerve terminal motor latency testing only reflects the conduction velocity of the fastest motor nerve fiber supplying the anal sphincter.15 Given that the pudendal nerve is made up of a number of nerve fibers, the accuracy of pudendal latencies remains unknown. The American Gastroenterological Association maintains that pudendal nerve terminal motor latency should not be recommended for the workup and evaluation of fecal incontinence.16 Our laboratory, as well as others, continues to use pudendal nerve terminal motor latency determinations as well as anorectal manometry to evaluate patients with fecal incontinence. These values should be directly associated given that the pudendal nerve directly effects voluntary contraction of the anal sphincter. Yet, no correlations have been noted between squeeze pressures and pudendal nerve latencies.10,17,18 In previous research, only fiber density but not pudendal nerve terminal motor latency was correlated with clinical and manometric variables.16 The authors questioned the routine use of pudendal nerve terminal motor latency in the assessment of patients with fecal incontinence. Similarly we found no correlation between bilaterally prolonged pudendal nerve terminal motor latency and anal squeeze pressures. We
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were, however, able to demonstrate an association between prolonged pudendal nerve terminal motor latency and anal resting pressures. Others have similarly found no correlation between pudendal nerve terminal motor latency values and anal squeeze pressures.17,19 However, the finding of a correlation between resting pressures and pudendal nerve terminal motor latency may be because of the relatively large contribution of the pudendal nerve to the resting tone of the anal sphincter. Although the internal anal sphincter is the major contributor to anal resting pressures, a significant component of the resting tone is from the external anal sphincter. Only a small number of patients (12 percent) in the present study demonstrated bilateral neuropraxia. Similarly, of 2,067 patients who underwent pudendal nerve testing only 11 percent manifested bilateral neuropraxia.20 Although the significance of bilaterally prolonged pudendal nerve terminal motor latency recordings is revealed by our data as well as others,10 no physiologic significance can be attributed to unilateral neuropathy. The present study revealed no correlation between unilateral neuropraxia and anorectal pressures and incontinence scores. The relative insignificance of unilateral neuropathy may be explained by the substantial anatomic overlap between opposite pudendal nerves.21 Preservation of one pudendal nerve may compensate for the slowed conduction of the other nerve and thereby maintain anal sphincter function.
CONCLUSIONS The patients in the present study were profoundly incontinent as evidenced by the high Fecal Incontinence Scores and low manometric recordings. Yet in this group of patients with intact anal sphincters and normal pelvic floors, only a small percentage of patients manifested prolonged pudendal nerve terminal motor latency determinations. These findings may indicate poor sensitivity of pudendal nerve terminal motor latency in detecting pudendal nerve damage or a nonpudendal–nerve-mediated etiology for idiopathic fecal incontinence. More sensitive investigative methods are needed to define the extent of pelvic floor damage in idiopathic fecal incontinence.
ACKNOWLEDGMENT The authors thank Ms. Susan Stagg whose technical assistance in data collection was indispensable.
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Appendix American Medical Systems Fecal Incontinence Score In the last four weeks, how often did you experience the following: Accidental bowel leakage of gas? Minor bowel soiling or seepage? Significant accidental leakage of liquid stool? Significant accidental leakage of solid stool? Does accidental leakage affect your lifestyle?
Never
Rarely
Sometimes
Weekly
Daily
Several Times Daily
0 0 0 0 0
1 31 61 67 1
7 37 73 79 2
13 43 85 91 3
19 49 97 103 4
25 55 109 115 5
Several times daily (>1 episode/day) Daily (1 episode/day) Weekly (<1/day but >1/wk) Sometimes (>1 in the last 4 weeks but <1/wk) Rarely (1 in the last 4 weeks) Never (no episodes in the past 4 weeks) Score from ‘‘Does accidental leakage affect your lifestyle’’ is added to the highest score from the first four questions Maximal score = 120 Adapted from Vaizey et al.8
REFERENCES 1. Mavrantonis C, Wexner SD. A clinical approach to fecal incontinence. J Clin Gastroenterol 1998;27:108 – 21. 2. Toglia MR. Pathophysiology of anorectal dysfunction. Obstet Gynecol Clin North Am 1998;25:771 – 81. 3. Kiff ES, Swash M. Slowed conduction in the pudendal nerves in idiopathic (neurogenic) faecal incontinence. Br J Surg 1984;71:614 – 6. 4. Olsen AL, Rao SS. Clinical neurophysiology and electrodiagnostic testing of the pelvic floor. Gastroenterol Clin North Am 2001;30:33 – 54. 5. Arendt-Nielsen L, Zwarts M. Measurement of muscle fiber conduction velocity in humans: techniques and applications. J Clin Neurophysiol 1989;6:173 – 90. 6. Varma JS, Smith AN, McInnes A. Electrophysiological observations on the human pudendo-anal reflex. J Neurol Neurosurg Psychiatry 1986;49:1411 – 6. 7. Pfeifer J, Salanga VD, Agachan F, Weiss EG, Wexner SD. Variation in pudendal nerve terminal motor latency according to disease. Dis Colon Rectum 1997; 40:79 – 83. 8. Vaizey CJ, Carapeti E, Cahill JA, Kamm MA. Prospective comparison of faecal incontinence grading systems. Gut 1999;44:77 – 80. 9. Rogers J, Henry MM, Misiewicz JJ. Disposable pudendal nerve stimulator: evaluation of the standard instrument and new device. Gut 1988;29:1131 – 3. 10. Rasmussen OO, Christiansen J, Tetzschner T, Sorensen M. Pudendal nerve function in idiopathic fecal incontinence. Dis Colon Rectum 2000;43:633 – 6. 11. Vernava AM III, Longo WE, Daniel GL. Pudendal neuropathy and the importance of EMG evaluation of fecal incontinence. Dis Colon Rectum 1993;36:23 – 7.
12. Ho YH, Goh HS. The neurophysiological significance of perineal descent. Int J Colorectal Dis 1995;10:107 – 11. 13. Tetzschner T, Sorensen M, Rasmussen OO, Lose G, Christiansen J. Reliability of pudendal nerve terminal motor latency. Int J Colorectal Dis 1997;12:280 – 4. 14. Karulf RE, Coller JA, Bartolo DC, et al. Anorectal physiology testing: a survey of availability and use. Dis Colon Rectum 1991;34:464 – 8. 15. Lubowski DZ, Jones PN, Swash M, Henry MM. Asymmetrical pudendal nerve damage in pelvic floor disorders. Int J Colorectal Dis 1988;3:158 – 60. 16. Barnett JL, Hasler WL, Camilleri M. American Gastroenterological Association Medical Position Statement on Anorectal Testing Techniques. American Gastroenterological Association. Gastroenterology 1999; 116:732 – 60. 17. Suilleabhain CB, Horgan AF, McEnroe L, et al. The relationship of pudendal nerve terminal motor latency to squeeze pressure in patients with idiopathic fecal incontinence. Dis Colon Rectum 2001;44:666 – 71. 18. Osterberg A, Graf W, Edebol Eeg-Olofsson K, Hynninen P, Pahlman L. Results of neurophysiologic evaluation in fecal incontinence. Dis Colon Rectum 2000;43:1256 – 61. 19. Thomas C, Lefaucheur JP, Galula G, de Parades V, Bourguignon J, Atienza P. Respective value of pudendal nerve terminal motor latency and anal sphincter electromyography in neurogenic fecal incontinence. Neurophysiol Clin 2002;32:85 – 90. 20. Hill J, Hosker G, Kiff ES. Pudendal nerve terminal motor latency measurements: what they do and do not tell us. Br J Surg 2002;89:1268 – 9. 21. Wunderlich M, Swash M. The overlapping innervation of the two sides of the external anal sphincter by the pudendal nerve. J Neurol Sci 1983;59:97 – 109.