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Application of pudendal evoked potentials in diagnosis of erectile dysfunction

Guang-You ZHU, Yan SHEN

Institute of Forensic Sciences, Ministry of Justice, Shanghai 200063, China

Asian J Androl  1999 Sep; 1: 145-150


Keywords: erectile dysfunction; pudendal evoked potential; pelvic fracture; spinal injury; diabetes; masturbation
Abstract
Aim: Extensive neurophysiological investigations were carried out in 100 healthysubjects and 84 patients with penile erectile dysfunction. Methods: Following examinations were performed, spinal and scalp somatosensory evoked potentials (SEPs) to stimulation of the dorsal nerve of penis, motor evoked potentials (MEPs) from bulbocavernosus (BC) in response to scalp and spinal root stimulation, and measurement of sacral reflex latency (SRL) from anal sphincter (AS). Results: In the healthy subjects, the mean sensory total conduction time (sensory TCT),as measured at the peak of the scalp P1 (P40) wave was 39.73 ms. The mean sensory central conduction time (sensory CCT=spinal-to-scalp conduction time) was 28.98 ms. The mean peripheral conduction time (PCP) was 9.40 ms. Transcranial brain stimulation was performed by using a magnetic stimulator during voluntary contraction of the examined muscle. Spinal root stimulation was performed at rest. Motor total conduction time (motor TCT) to BC muscles was 20.48 ms. Motor central conduction time (motor CCT) to sacral cord segments controlling BC muscles was 14.42 ms at rest. The mean  SRL was 35.13 ms. Conclusion: Combined or isolated abnormalities of SEPs, MEPs, and SRL were found in patients with erectile dysfunction.

1 Introduction

Some objective tools have recently been developed in order to differentiate the nature of erectile dysfunction, i.e., nocturnal penile tumescence (NPT)[1,2], electrically induced bulbocavernosus(BC) reflex[3], penile blood pressure, Doppler sonography, and plethysmography of penis[4,5]. These new objective aids will probably reveal increasing cases of erectile dysfunction due to organic causes, especially those of neurological origin. Recent trends indeed, have shown that erectile dysfunction is not uncommon in male patients with diseases of the nervous system[6,7].

In order to improve the evaluation of the erectile dysfunction, somatosensory evoked potentials (SEPs), motor evoked potentials (MEPs) from bulbocavernosus (BC) and the measurement of sacral reflex latency (SRL) from anal sphincter (AS) have been investigated in erectile dysfunction patients and in healthy subjects.

2 Materials and methods

2.1 Subjects

One hundred adult healthy males (Han race, mean age=38 years old) without any known neurological disorder and 84 patients (Han race) having erectile dysfunction alone or in conjunction with various diseases, were investigated. Of these patients, 31 cases developed erectile dysfunction after pelvic fracture(mean age=31 years old),10 after spinal injury (mean age=42 years old),16 with diabetes(mean age=50 years old) and 27 have a history of masturbation more than 5 years(mean age=31 years old).

2.2 SEPs: stimulating and recording methods[8]

The dorsal nerves of the penis were stimulated via 2 ring electrodes, 1.5 cm apart, wrapped around the penile shaft, with the cathode placed proximally. The response was bipolarly recorded at the spinal level (Th12-L1) and from the scalp, roughly overlying the sensorimotor cortex for the genital region (2 cm behind Cz, referred to Fz of the international 10-20 system). The subject was asked to relaxedly lie down on a bed at a supine position. Stimuli consisted of rectangular pulses 0.1 ms in duration, 3-4 times above the subjective threshold and a 2.77/s repetition rate. The subjective threshold was defined as the lowest perceivable intensity. The tracing represented the final average of 250 artifact-free responses. This gave reproducible SEPs in a reasonable time. The latency of the spinal response was measured at the peak of the initial negative deflection(sensory peripheral conduction time=sensory PCT). The latency of the scalp SEP was taken at the first reliable positive peak(wave P40=sensory total conduction time=sensory TCT). By subtracting the former from the latter, the sensory central conduction time (sensory CCT) was obtained.

2.3 MEPs: stimulating and recording methods[8]

Brain and sacral root stimulation was performed with simultaneous recording of the response in BC muscle with surface electrodes. Three different motor conduction times were determined: a motor total conduction time (motor TCT) which represents the transit time from brain to target muscle, a motor peripheral conduction time (motor PCT) which corresponds to the sacral roots to the target muscle transit time and, by subtracting the latter from the former,a motor central conduction time (motor CCT=brain to sacral roots conduction time) was obtained. Stimulation was performed via a magnetic stimulator (Cadwell MES-10) with a coil of 9 cm internal diameter applied in direct contact to the skin. The intensity of magnetic stimulation can  be expressed as a percentage of the maximum (=2.5 Tesla). The stimulation was performed with the posterior edge of the coil applied 2 cm behind Cz. First,the stimulation intensity was progressively increased until an MEP could be recorded in the muscles with the subjects at rest. The transcranial stimulation was then repeated with the same intensity during a transient and moderate voluntary contraction of the examined muscles (facilitation procedure). Spinal root stimulation was performed with the center of the coil applied 5 cm laterally to the spine at the level of the right iliac crest. MEPs were recorded only at rest. Latencies were measured at the onset of the first steady deflection from the baseline.

Both SEPs and MEPs were obtained with a poststimulus analysis time of 100 ms and 50 ms, respectively, and a filtering bandpass of 10-500 Hz. They were repeated several times and superimposed to facilitate discrimination of stimulus locked from random activity. A relative negativity in grid 1 of the amplifier provoked an upward deflection.

2.4 SRL: stimulating and recording methods[8]

The dorsal nerves of the penis were electrically stimulated while the reflex response was recorded in the anal sphincter. Stimulation and recording parameters were the same as for SEPs. The responses to single shocks at 0.15 c/s were recorded and the minimum latency of 50 reflex responses was measured. The latency was measured at the onset of the first repeatable deflection from the baseline.

3 Results

3.1 Healthy subjects

SEPs: The cortical response had a w-shaped wave form. The mean latency of the first positive peak (P1) measured as total sensory conduction time (TCT) was 39.73 ms (+3s=45.82 ms) (Table 1).

Table 1.Somatosensory evoked potentials (SEPs) and motor evoked potentials (MEPs) of 100 healthy adult males (latencies in ms)

Test

Latencies (mean)

s

mean+3s

Sensory EPs

TCT

39.73

2.03

45.82

PCT

9.40

1.46

13.78

CCT

28.98

2.83

37.47

SRL

35.13

3.52

45.69

Motor EPs

TCT

20.48

2.21

27.11

PCT

5.98

1.62

10.84

CCT

14.42

2.56

22.10

A spinal response of low voltage was recorded. This potential was seldom well defined, being initially negative and predominantly monophasic. The mean onset latency of the spinal response measured as PCT was 9.40 ms (+3s=13.78 ms). The CCT as measured from the onset of the spinal EP to the cortical P1 peak was 28.98 ms (+3s=37.`47 ms).

SRL: SRL was recorded in AS. The mean latency for the first deflection was 35\^13 ms (+3s=45.69 ms)in the anal sphincter (Table 1).

MEPs: Brain stimulation was performed with facilitation and spinal stimulation at rest. The scalp and spinal motor evoked potentials were recorded. In the BC, the TCT and  PCT were 20.48 ms (+3s=27.11 ms) and 5.98 ms (+3s=10.84 ms),

respectively. The Mean CCT was 14.42 ms (+3s=22.10 ms) (Table 2). The intensity of transcranial stimulation ranged between 60 %-90 % of the stimulator's output in the healthy subjects and 60%-100% of the output in the patients.

3.2 Patients

We briefly describe here the results of a few groups of patients with erectile dysfunction. Abnormalities were defined when SEPs, MEPs or SRL were absent or when latencies or conduction times were more than 3s from the control mean, provided the height was in the range of the healthy male group.

3.3 Patients with pelvic fracture

We have investigated 31 cases of the patients having erectile dysfunction after pelvic fracture. The results showed that 12 had abnormal pudendal EPs. The rate of abnormality was 38.70%. (Table 2)

Table 2.Pelvic fracture (latencies in ms, ?: absent, -: not tested).

Patients
()

Age
(years)

Sensory EPs

Motor EPs

SRL

TCT

PCT

CCT

TCT

PCT

CCT

020

47

?

?

?

24.20

10.50

13.70

?

099

36

41.40

9.53

31.90

24.80

6.17

18.60

32.30

151

34

45.50

11.90

33.62

5.50

5.08

19.20

38.30

159

21

37.20

8.13

29.00

-

-

-

30.30

172

69

-

-

-

27.20

11.20

15.90

51.60

221

54

40.20

9.38

30.80

-

-

-

-

228

29

40.18

10.30

30.50

21.90

7.19

14.70

33.40

266

39

41.60

8.13

33.47

19.50

4.84

14.66

38.30

299

21

-

-

-

?

5.08

?

-

311

33

47.70

10.50

37.20

?

9.45

?

42.50

326

31

39.10

11.70

28.40

?

5.31

?

29.50

342

48

46.50

11.40

34.10

?

7.03

?

46.60

429

25

43.60

9.22

34.10

16.80

5.05

11.75

31.70

447

40

52.20

8.59

43.60

-

-

-

35.30

575

40

60.20

18.80

41.40

19.80

5.20

14.60

?

569

39

42.30

10.50

31.80

21.40

5.28

16.12

29.70

603

23

39.70

11.90

27.80

19.10

5.78

13.72

32.70

606

38

41.90

11.70

30.20

-

-

-

44.70

609

38

44.80

14.50

30.30

19.50

5.63

13.87

?

628

23

44.50

11.10

33.40

19.50

5.31

14.19

32.00

695

23

40.20

7.66

32.54

19.20

5.40

13.80

28.40

714

33

32.80

8.42

4.36

20.50

5.50

15.00

35.30

748

32

38.90

7.50

31.40

14.10

5.08

9.02

29.20

796

22

42.00

7.97

34.03

24.60

5.45

19.05

36.30

815

25

42.50

10.20

30.30

18.60

7.97

10.63

31.30

822

20

41.10

9.06

32.04

19.70

7.19

12.58

32.50

823

20

-

-

-

16.30

4.53

11.70

-

828

27

48.60

13.60

35.00

15.30

7.11

8.19

38.60

829

37

?

?

?

18.70

5.00

13.70

?

862

34

?

?

?

17.70

4.70

13.00

?

872

28

39.80

8.75

31.05

18.80

5.16

13.64

34.10

3.4 Spinal damage patients

There were 10 patients in this group. The results showed that 5 had abnormal pudendal EPs. The rate of abnormality was 50 %. (Table 3)

Table 3.  Spinal damage (latencies in ms, ?: absent, -: not tested).

Patients
()

Age
(years)

Sensory EPs

Motor EPs

SRL

TCT

PCT

CCT

TCT

PCT

CCT

001

53

41.60

?

?

-

-

-

30.90

084

43

44.10

14.40

29.70

-

-

-

43.10

098

45

43.00

11.10

31.90

-

-

-

37.50

122

27

41.40

9.38

32.02

-

-

-

39.40

311

33

47.70

10.50

37.20

?

9.45

?

42.50

423

43

39.80

8.13

31.67

21.20

5.18

16.02

71.90

474

47

?

?

?

20.20

5.78

14.42

?

548

32

44.10

?

?

14.90

5.39

9.51

39.40

697

45

41.90

8.59

33.31

17.00

5.08

11.92

31.40

852

56

46.70

14.20

32.50

-

-

-

51.30

3.5 Diabetes patients

We have investigated 16 cases of diabetes patients. The results showed that 8  had abnormal pudendal EPs. The rate of abnormality was 50%. (Table 4)

Table 4. Diabetes patients (latencies in ms, ?: absent, -: not tested).

Patients
()

Age
(years)

Sensory EPs

Motor EPs

SRL

TCT

PCT

CCT

TCT

PCT

CCT

025

53

55.10

16.20

38.90

-

-

-

56.00

055

34

43.10

18.20

25.10

19.40

5.06

14.34

37.30

092

66

42.30

10.50

31.60

-

-

-

56.10

109

33

41.40

9.53

30.80

22.50

5.50

17.00

43.60

206

63

-

-

-

22.40

6.20

16.20

36.60

283

63

43.00

11.60

31.40

21.40

5.08

16.30

36.10

353

49

40.40

10.30

30.10

-

-

-

40.60

363

41

39.10

8.91

30.20

26.30

5.70

20.60

34.20

549

60

46.70

?

?

-

-

-

35.90

599

52

45.50

9.41

35.09

27.80

6.80

21.00

41.80

699

56

44.40

12.30

32.10

27.30

5.70

20.60

34.20

713

67

-

-

-

24.20

6.25

17.95

39.50

729

52

39.50

8.44

31.06

18.80

6.95

11.85

33.90

730

52

46.30

10.60

35.70

21.60

5.39

16.21

44.70

767

33

46.10

9.84

35.46

16.50

6.17

10.33

29.10

769

56

-

-

-

19.10

8.52

10.58

30.20

3.6 Masturbation patients

We have tested 27 patients with a history of 5 or more years of consistent masturbation. Nine had abnormal pudendal EPs. The rate of the abnormality was 33.33%. (Table 5)

Table 5. Masturbation patients (latencies in ms, ?: absent, -: not tested).

Patients
()

Age
(years)

Sensory EPs

Motor EPs

SRL

TCT

PCT

CCT

TCT

PCT

CCT

028

28

38.90

9.22

29.00

-

-

-

51.40

095

21

53.30

9.00

44.30

18.70

7.81

10.90

27.50

141

24

?

?

?

-

-

-

31.60

169

28

42.50

10.50

32.00

-

-

-

36.45

196

51

40.20

9.06

31.10

-

-

-

40.20

216

24

40.90

10.50

30.40

-

-

-

38.80

231

27

39.10

9.80

30.20

19.30

5.23

14.07

55.00

285

23

43.00

10.20

32.80

20.50

5.92

14.50

33.30

347

20

46.10

15.23

0.90

-

-

-

62.20

363

41

39.10

8.90

30.20

25.30

7.80

18.50

29.40

374

34

41.70

8.10

33.60

-

-

-

33.10

375

43

44.70

10.50

34.20

-

-

-

37.30

379

29

40.20

11.10

29.10

-

-

-

43.40

390

30

39.70

8.80

30.90

19.80

6.72

13.10

47.00

396

28

43.40

8.70

34.70

23.20

6.95

14.10

37.80

407

25

42.50

19.70

22.80

-

-

-

48.00

440

25

49.80

10.20

39.60

18.40

9.45

9.00

33.10

498

52

41.30

10.00

31.30

19.50

6.09

13.41

35.90

583

35

38.90

7.34

31.56

-

-

-

30.20

560

30

41.90

10.30

31.60

17.80

5.63

12.17

45.80

584

37

39.20

7.81

31.39

-

-

-

30.20

698

36

42.00

7.19

34.81

-

-

-

33.00

703

34

-

-

-

22.10

9.45

12.65

28.00

786

32

43.20

9.53

34.76

-

-

-

36.10

801

26

39.20

8.28

30.92

16.20

6.64

9.56

40.00

814

31

39.10

7.50

31.60

-

-

-

26.70

838

32

36.60

8.59

28.01

-

-

-

29.80

4 Discussion

4.1 About healthy males

Electrophysiological techniques have opened new perspectives in the diagnosis of erectile dysfunction, providing an objective way to test afferent and efferent somatic pathways governing the erectile ability.

In agreement with other reports[9-11],we found that the pudendal EPs in healthy subjects on stimulation of the penile are relatively easy to elicit and demonstrate a consistent morphology and latency.

SEP examine the afferent pathways from the dorsal nerve of the penis to the sensorimotor cortex. Although the role of this nerve is not well understood in humans, its integrity is thought to be crucial in the maintenance of erection, transmitting sensory impulses from the glans penis to the brain. In agreement with the general results in the literature[8-10], we found that the latency of scalp evoked potential (P1) was 39.73 ms (+3s=45.82 ms) and that of PCT was 9.40 ms (+3s=13.78 ms).

Measurement of SRL is useful in the evaluation of the spinal and peripheral somatic innervation of the genito-urinary tract. The sacral reflex pathway consists of the dorsal nerve of the penis, the S2-S4 cord segments, and the motor branch of the pudendal nerve innervating the BC muscles, and anal and urethral sphincters. SRL is also a useful index to examine the integrity of parasympathetic nerves controlling penile erectile function. In the present study the latencies of reflex responses in healthy male are 35.13 ms (+3s=45.69), which are the same as those previously reported[9-11].

Spinal and transcranial magnetic stimulation is a complementary method used to examine the central and peripheral motor pathways leading to the striated muscles of the urogenital system. It is known that the motor pathway has an important role in developing and maintaining the rigidity of penile erection. In general, 80% of patients with spinal cord injury experience erectile dysfunction. The crucial problem is the duration of the erection: tumescence and rigidity tend to fade away quickly and the patient is unable to perform intercourse. This is thought to be due to the injury of the central and/or peripheral motor pathway leading to the striated muscles of the urogenital system. In our study the MEPs in BC after transcranial stimulation have a latency of about 20.48 ms (+3s=27.11 ms) in the contracted state of pelvic floor muscles. Spinal root stimulation provokes a response with a latency of about 5.98 ms (+3s=10.84 ms). These latencies are slightly shorter than those reported previously[10]. The reason is perhaps due to the difference in the intensity of the stimulation used.

4.2 About patients

Abnormal SEPs, MEPS, and SRL were obtained in different ways and with variable frequencies due to varied locations of lesions in the peripheral and central nervous systems.

Although erectile dysfunction is known to occur in up to 50% of patients  with posterior urethral rupture after traumatic pelvic fracture[12],its exact mechanism has remained unclear. The origin is usually assumed to be neurovascular, without any differentiation between these 2 factors. Recent advances in pudendal evoked potentials have permitted a more accurate neurophysiologic evaluation of these injuries. Of our 31 patients with a history of  pelvic fracture together with  complete or incomplete urethral disruption, 12 (38.70%) demonstrated distinct abnormal pudendal evoked potentials. These results suggest that in these patients the causes of the erectile dysfunction may be in part the injury  of pudendal nerves.

In many cases of spinal cord lesions, there is no difficulty in explaining the cause of erectile dysfunction[13]. However, some patients may suffer from erectile dysfunction alone or together with urinary incontinence, especially those cases with mild cauda/conus traumatic lesions. The test of the pudendal EPs in spinal lesions unmasked clinical and subclinical involvement of the lower sacral and lower lumbar roots, respectively. In the higher level of spinal cord involvement, SRL had no practical value and was essentially normal, while both SEPs were more important in showing the degree of involvement in the afferent spinal tracts. In the present study we have investigated 10 patients, who developed erectile dysfunction after spinal traumatic injuries with sensory disturbances in the area of the pudendum and/or lower extremities. Six of them (50%) showed abnormal pudendal EPs. In these patients, there was a high incidence of the pudendal nerves injury.

Different types of erectile dysfunction were well documented in diabetes mellitus and it was believed that most cases had autonomic and somatosensory neuropathy. In our study we examined 10 cases of erectile dysfunction patients with diabetes and found that 3 of them have abnormal pudendal Eps (Table 3).

It is thought that masturbation is a bad habits but not harmful to the health. It is very interesting that we have encountered many young patients, who complained of erectile dysfunction without any apparent causes except a history of long continued masturbation. After careful examination we found 9 of 27 cases (33.33%) having abnormal pudendal EPs. We do not quite understand the relationship between erectile dysfunction and masturbation, which seems to be worthy of further investigation.

In conclusion, the pudendal EPs is a useful objective method to test afferent and efferent somatic pathways governing the erectile ability. The present study showed that in patients having erectile dysfunction after traumatic pelvic fracture, spinal injure, diabetes or with a history of consistent masturbation, there is a high incidence of  damage of the neural pathways involving the penile erection. From a practical point of view, pudendal EPs are recommended to be tested in all cases of erectile dysfunction.

References

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[11] Opsomer RJ, Caramia MD, Zarloa F, Pesce F, Rossini PM. Neurophysilogical evaluations of central-peripheralsensory and motor pudendal fibers. Elecltroencephal Clin Neurophysol 1989; 74: 260-70.
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Correspondence to Prof. Guang-You ZHU.
Fax: +86-21-6244 2691
E-mail: chendj@online.sh.cn
Received 1999-08-26     Accepted 1999-09-12