Journal Article

Pudendal nerve involvement in patients with hereditary motor and sensory neuropathy
by D.B. Vodusek and J. Zidar, Institute of Clinical Neurophysiology, University Medical Centre, Ljubljana, Yugoslavia
published Acta Neurol Scand., 1987:76:457-460

Key words
peroneal muscular atrophy; hereditary motor and sensory neuropathy; pudendal nerve; urinary incontinence.

Abstract
Pudendal nerve involvement was demonstrated by electromyography of perineal muscles and by recordings of their direct and reflex responses on perineal electrical stimulation in 10 patients with hereditary motor and sensory neuropathy. Patients reported no defecation disturbances and the 6 men had good erections. Urinary stress incontinence was seen in those 2 (of 4) female patients who had delivered.

The so-called sphincter disturbances are described in very few patients with hereditary neuropathy (1,2). In our experience (with ca.140 patients with hereditary motor and sensory neuropathy – HMSN) we have encountered micturition problems in patients only rarely. In fact they had never been actively sought until now and no data about their true incidence exist. On the other hand there is growing awareness of possible neurogenic causation of "idiopathic" urinary and faecal incontinence. Incontinent patients (without other neurological symptoms) are increasingly referred for electrophysiological investigations for assessment of a possible neurogenic sphincter lesion. As neuropathic changes in HMSN patients are expected to be more or less generalized it was felt that electrophysiological investigations of incontinent HMSN patients are useless before more is learnt about the sacral neuromuscular system in continent HMSN patients.

Patients and method
Ten consecutive patients with HMSN (14-40 years old) were seen at their annual follow-up visit. The typical clinical picture, a positive family history, the EMG findings, sural nerve biopsy (Patient 9, Table 1), as well as ruling out other causes of neuropathy had been the basis for diagnosis. They were diagnosed as HMSN Type I (6 patients: 4 men, 2 females: all with motor conduction velocity of the median nerve below 33 m/s), HMSN Type II (3 patients, 1 man, 2 females) and HMSN Type III (1 male patient). Patients agreed to an additional EMG examination of the perineal muscles.
Patients were questioned about their micturition, defecation and erection. The female patients were gynecologically examined. The electrophysiological examination of perineal muscles consisted of a concentric needle EMG and the detection of direct [R1] and reflex [R3] responses (3). In short, the muscle responses are recorded by a concentric needle electrode: the direct [R1] response is elicited by electrical stimulation in the perineum posteriorly to the location of the recording electrode: the reflex [R3] response is elicited by electrical stimulation of the dorsal penile (clitoral) nerve. The bulbocavernosus muscle and the external anal sphincter were examined in the male: the periurethral sphincter and the external anal sphincter in the female. Due to the large variability of amplitudes of electrically elicited muscle responses (as recorded by a needle electrode) only the latencies were systematically analysed. The median nerve (motor and sensory fibres) as well as the peroneal nerve were also examined. All stimulations were performed with bi-polar surface disc electrodes (Disa 13L22). M-waves from limb muscles were recorded with bi-polar surface disc electrodes. The sensory action potential of the median nerve was recorded antidromically on the index finger with ring electrodes (Medelec E/DS-K53052).

Micturition disorders and pudendal nerve involvement in 10 patients with hereditary motor and sensory neuropathy

Patient Sex Age HMSN Type Symptoms Perineal Muscles EMG R1 (ms) R3 (ms)
1 J.M. M 32 I none increased No. of polyphasic MUPs" 6.9 80
2 M.M. M 22 I none – 9.8 40
3 S.A. M 37 I none – 6.8 36
4 S.B. M 14 I none – 7.4 62
5 S.M. F 40 I frequency & stress incont. reduction of MUPs 8.6 63
6.D.A. F 29 I none increased No. of polyphasic MUPs 5.2 52
7. B.K. F 40 II stress incont. – 4.8 47
8. S.B. F 21 II none – 5.5 43
9. M.L. M 30 II none pronounced polyphasia 8.0 40
10. V.J. M 19 III none increased No. of polyphasic MUPs 8.0 100

Any micturition or defecation dysfunction
" Motor unit potentials
Direct response in external urethral sphincter muscle
"Bulbocavernosus reflex" response in external urethral sphincter muscle

Results
All patients denied faecal incontinence and soiling of underwear. All 6 men claimed good erections. All men denied any micturition dysfunction. The 4 female patients were gynecologically unremarkable (2 of them had delivered children). Two female patients denied urinary incontinence (these were the 2 female patients who did not deliver children). Two female patients had stress incontinence which was in one of them combined with frequency of micturition (both of them were troubled enough to seek medical help because of incontinence).
Electrophysiological findings in perineal muscles were abnormal in all patients. The needle EMG was abnormal in all of them: it did not detect any abnormal spontaneous activity, there was however an increased incidence of polyphasic motor unit potentials (between 20 and 40% in 8 patients, 75% in one patient). The number of motor units was significantly reduced in only one patient.
The mean latency of the patients' direct responses [R1] was 7.1 ms, which is prolonged compared to the mean latency of this response in the normal population (4.9 plus or minus1.13 ms) (3). Nevertheless, the individual values were abnormal (i.e. longer than 7.7 ms) only in 5 patients.
The latency of the reflex response [R3] was abnormally prolonged in 7 patients (i.e. longer than 42.5 ms - the mean value in normal control being 32.3 plus or minus 3.94 (3)). The diagnosis, the urinary symptoms and the electrophysiological findings are listed in Table 1.
Electrophysiological findings in limb nerves were abnormal (Table 2). Sensory potentials were detected in only of the patients with HMSN Type 1. No M wave of the short toe extensor could be obtained in patients with HMSN Types II and III.
Relative involvement of median, peroneal and pudendal nerves can be seen by comparison of distal motor latencies (Table 2): the values for pudendal nerves are relatively less different from normal values than those for the limb nerves.

Table 2
Electrophysiological findings in 10 patients with hereditary motor and sensory neuropathy

DL
MCV Median nerve SCV
A
DL Peroneal n. MCV
R1 Pudendal n. R3
1. J.M. 11.4 16 0 not done 6.9 80
2. M.M. 10.0 18 0 14.2 20 9.8 40
3. S.A. 6.2 32 0 10.5 18 6.8 36
4. S.B. 12.9 22 0 16.8 27 7.4 62
5. S.M. 9.3 18 0 15.5 22 8.6 63
6. D.A. 6.6 33 30 25 10.3 24 5.2 52
7. B.K. 3.8 56 46 10 0 4.8 47
8. S.B. 3.6 54 0 0 5.5 43
9. M.L. 4.4 58 46 30 0 8.0 40
10. V.J. 15.0 1.0 0 0 8.0 100

DL R1 : Distal motor latency (R1: upper limit of normal 7.7 ms)
MCV : Maximal motor conduction velocity
SCV : Maximal sensory conduction velocity
A : Amplitude of the sensory action potential
R3 : Bulbocavernosus reflex latency
0 : No response

Comment
All patients examined had electrophysiological abnormalities in their sacral neuromuscular system which were, however, less pronounced than the abnormalities detected in their limbs. Differences in electrophysiological findings in the sacral neuromuscular system between the groups HMSN I, II and III cannot be evaluated due to the small number of patients examined. Although evident electrophysiological abnormalities in sphincter muscles had been present in all patients only in 2 female patients micturition problems developed. Clinically and neurophysiologically they did not seem to differ obviously from other patients. The one distinguishing feature was the fact that of the 4 female patients in our group these 2 had had children. Therefore, childbirth can be regarded as an important factor in the development of incompetence of the urethral closure mechanism in these patients. Further, urodynamic evaluation for such patients would seem helpful.
Our study shows the pathologic process in patients with HMSN to be widespread, involving also the pudendal nerves. Abnormal EMG of perineal muscles (increased incidence of polyphasic potentials, reduction of motor unit potentials) was found in all patients examined. In addition, the distal latency for the pudendal nerve was abnormally prolonged in 5 of the bulbocavernosus reflex latency in 7 of the 10 patients examined. However functional disturbances due to the neuropathic process are not mandatory at the observed degree of involvement. In patients who do develop micturition problems other causative factors are probably involved.
We would like to stress this relative lack of correlation between electrophysiologic abnormalities and clinical dysfunction, which however is not a finding typical for the sacral nervous system. Lack of correlation between slowing of conduction in limb nerves and disturbances of function has been reported in patients with HMSN (4). In HMSN families some asymptomatic members have marked electrophysiologic abnormalities (5).
Whether such lack of correlation between an "abnormal sphincter EMG" and disturbance of function can be generalized to other groups of patients remains to be seen. It is claimed that idiopathic faecal incontinence (6,7) as well as idiopathic urinary stress incontinence (8) are neurogenic, as histological and electrophysiological investigations showed (minor) abnormalities in groups of such patients. We feel, however, that the correlation between the neuropathic abnormalities and functional deficiency is rather complex and that in an individual patient no micturition, defecation or erectile disorder should be "dismissed" as "neurogenic" by demonstration of minor electrophysiologic abnormalities alone.

Acknowledgement
This study was supported by the Research Community of SR Slovenia.

References
1. Holmes G. Family spastic paralysis associated with amyotrophy. Rev Neurol Psychia 1905;3;257-263.
2. Roussy G, Levy G.Sept cas d'une maladie familiale paticulière: troubles de la marche, pieds bots et areflexie tendineuse generalisé avec accessment, legère maladresse des mains. Rev Neurol (Paris) 1926:1:427-450.
3. Vodusek DB, Janko M, Lokar J. Direct and reflex resopnses in perineal muscles on electrical stimulation. J Neurol Neurosurg Psychiat 1983:46:67-71.
4. Buchthal F, Behse F. Peroneal muscular atrophy (PMA) and related disorders. 1. Clinical manifestations as related to biopsy findings, nerve conduction and electromyography. Brain 1977:100:41-66.
5. Harding AE, Thomas PK. The clinical features of hereditary motor and sensory neuropathy Types I and II. Brain 1980:103:259-280.
6. Parks AG. Anorectal incontinence. Proc R Soc Med 1975:68:681-690.
7. Beersiek F, Parks AG, Swash M. Pathogenesis of anorectal incontinence: a histometric study of the anal sphincter musculature. J Neurol Sci 1979:42:111-127.
8. Snooks SJ, Badenoch D, Tipfat R, Swash M. Perineal nerve damage in genuine stress incontinence of urine: an electrophysiological study. Br J Urol 1985:57:422-426.