Dynamic somatosensory evoked potential and magnetic resonance imaging in pudendal neuropathy: A comparative study with respect to the clinical diagnostic criteria

Burcu Ormeci; Handan Uzunçakmak Uyanık; Neslihan Taşdelen; Elif Çiğdem Keleş; Tibet Erdoğru; Ali Emre Öge

doi:10.4103/nsn.nsn_239_21

ORIGINAL ARTICLE

Year : 2022 | Volume : 39 | Issue : 3 | Page : 119-125

Dynamic somatosensory evoked potential and magnetic resonance imaging in pudendal neuropathy: A comparative study with respect to the clinical diagnostic criteria

Burcu Ormeci¹, Handan Uzunçakmak Uyanık², Neslihan Taşdelen³, Elif Çiğdem Keleş⁴, Tibet Erdoğru¹, Ali Emre Öge⁵
¹ Private Practice, İstanbul, Turkey
² Hacettepe University, Institute of Neurosciences and Psychiatry, Ankara, Turkey
³ Department of Radiology, Yeditepe University, Faculty of Medicine, İstanbul, Turkey
⁴ Department of Biostatistics and Medical Informatics, Yeditepe University, Faculty of Medicine, İstanbul, Turkey
⁵ Department of Neurology and Clinical Neurophysiology, Istanbul University, Faculty of Medicine, İstanbul, Turkey

Date of Submission	25-Dec-2021
Date of Decision	06-Feb-2022
Date of Acceptance	18-Mar-2022
Date of Web Publication	30-Sep-2022

Correspondence Address:
Handan Uzunçakmak Uyanık
Institute of Neurosciences and Psychiatry, Hacettepe University, Ankara 06230, Altindag
Turkey

Source of Support: None, Conflict of Interest: None

DOI: 10.4103/nsn.nsn_239_21

Abstract

Aim: Pudendal neuropathy (PN) is a common cause of chronic perineal pain and usually diagnosed long after the onset of symptoms. Diagnostic work-up of PN mainly includes radiologic and neurophysiological studies. However, there is no established diagnostic test to confirm the clinical diagnosis. This study aims to evaluate the correlation between the dynamic pudendal somatosensory evoked potential (SEP) and pudendal magnetic resonance imaging (MRI) in patients with PN diagnosed clinically based on Nantes criteria as the gold standard for comparison. Methods: Forty-three patients (25 females, 18 males) were included in the study. Dynamic pudendal SEP as a novel method, which includes both provocative positioning and stimulation of each side separately, and pudendal MRI were performed in each patient. Results: Dynamic pudendal SEPs were found to be abnormal in 42, normal in 12 of the 54 clinically symptomatic nerves and abnormal in 2, normal in 30 of the 32 clinically asymptomatic nerves. Pudendal MRI was abnormal in 19, normal in 35 of the 54 clinically symptomatic nerves and abnormal in 8 and normal in 24 of the 32 clinically asymptomatic nerves. There was 84% agreement between clinical diagnosis and dynamic pudendal SEP (high sensitivity and specificity), 49% agreement between clinical diagnosis and pudendal MRI (low sensitivity and acceptable specificity), 53% agreement between dynamic pudendal SEP and pudendal MRI. Conclusions: The novel dynamic pudendal SEP method seems to be useful in supporting the clinical diagnosis of PN, while pudendal MRI lacks sufficient sensitivity to be used alone in diagnosis of PN.

Keywords: Dynamic somatosensory evoked potential, magnetic resonance imaging, neurography, pudendal neuropathy

How to cite this article:
Ormeci B, Uyanık HU, Taşdelen N, Keleş E&, Erdoğru T, Öge AE. Dynamic somatosensory evoked potential and magnetic resonance imaging in pudendal neuropathy: A comparative study with respect to the clinical diagnostic criteria. Neurol Sci Neurophysiol 2022;39:119-25

How to cite this URL:
Ormeci B, Uyanık HU, Taşdelen N, Keleş E&, Erdoğru T, Öge AE. Dynamic somatosensory evoked potential and magnetic resonance imaging in pudendal neuropathy: A comparative study with respect to the clinical diagnostic criteria. Neurol Sci Neurophysiol [serial online] 2022 [cited 2023 Jun 9];39:119-25. Available from: http://www.nsnjournal.org/text.asp?2022/39/3/119/357500

Introduction

Pudendal nerves derive from S2-S4 sacral roots and give three major branches on either side: Inferior anal, perineal, and dorsal nerves of the penis or clitoris.^[1] The pudendal nerve is a mixed nerve composed of sensory, motor, and autonomic fibers. It innervates the perineum, rectum, and genitalia.^[1]

Pudendal neuropathy (PN) is a common cause of chronic resistant perineal pain that generally increases with hip flexion.^[2],[3] Most frequent locations of PN are its lesions at the common entrapment sites.^[4],[5] Estimated incidence of PN is 1/100–1/100,000^[6] and chronic pelvic pain is estimated to affect 7%–24% of the general population.^[7]

PN is generally diagnosed long after the initial onset of symptoms.^[8] There are several reasons for this situation. First, gynecologists and urologists often focus on the end-organs and the investigations necessary to decide that the problem is not residing in those organs take time to perform. Second, attempts for the treatment of each false diagnosis cause additional delays.^[9] The third obstacle is the lack of a good diagnostic test to confirm the clinical diagnosis of PN. Most of the current diagnostic tests are confined to the exclusion of alternative diagnoses, even though they are very valuable in this respect.^[10],[11] The fourth difficulty is that the pudendal nerve can be entrapped in four different regions and the tests directed to all of these regions are quite difficult.^[5],[12] In recent years, studies on the diagnosis and treatment of PN have been increased, but clear and confirmative knowledge has not yet been established, and success rate in the treatment is still limited.^{[3],[13],[14]}

The tests that can be used for the diagnosis of PN are mainly radiological^{[14],[15],[16],[17],[18]} and neurophysiological studies.^{[10],[11],[19],[20],[21]} Pudendal nerve block is also helpful in the diagnosis.^[15],[21] The success rate of the conventional neurophysiological studies (motor latency, bulbocavernosus reflex, somatosensory evoked potentials [SEP], needle EMG) to support the diagnosis is quite low.^{[20],[21],[22],[23]} However, in the new dynamic pudendal SEP method introduced in 2016, more than 45% decrease in the SEP amplitude at the end of the sitting period seems to be useful in supporting the diagnosis of neuropathy with 70.4% sensitivity and 96.9% specificity.^[23] In this method, right and left pudendal nerves are stimulated individually to obtain the responses. Thus, the possible diluting effect of normal side on the abnormal findings of the symptomatic side can be prevented in unilateral neuropathies. Dynamic SEP recordings are also obtained in the sitting position when the symptoms are more prevalent, and the electrodiagnostic criteria are described depending on these positional changes.^[23]

Radiological imaging methods to support the clinical diagnosis of PN are emerging in recent years, but pudendal magnetic resonance imaging (pudendal MRI) studies are scarce in the literature, possibly due to the difficulties caused by small caliber of the nerve and its location in the vicinity of intense vascular structures.^{[14],[15],[16],[17],[18]} Therefore, the radiological diagnosis is almost always based on asymmetry between the two sides, and the results need to be interpreted together with the clinical findings. MRI studies for the intra-pelvic region provide valuable additional information for differential diagnosis.^[15],[24]

In this study, we planned to evaluate the agreement between the dynamic pudendal SEP and pudendal MRI studies in patients with PN and the conformity of these methods to the clinically based Nantes criteria, which were accepted as the gold standard for comparison.^[13]

Methods

The study was performed at a University Clinical Neurophysiology Laboratory and Radiology Departments between March 2012 and March 2018, following approval by the local ethics committee, and informed consent was obtained from each patient.

All of the patients were referred for electrophysiological examination by the same urologist who treated them because of their complaints of chronic pelvic pain. Forty-three patients (25 females, 18 males) who were diagnosed with PN by using Nantes criteria were included in the study. Nantes criteria are summarized as follows: Pain in the anatomical territory of the pudendal nerve (1), predominantly experienced while sitting (2), does not wake the patient at night (3), with no objective sensory impairment (4), and relieved by diagnostic pudendal nerve block (5). The mean age of the patients was 42.4 ± 10.42 for females and 37.16 ± 10.17 for males.

The exclusion criteria were pure coccygeal or gluteal pain, paroxysmal pain, pruritus, having any systemic disease that could affect the peripheral or central nervous system, history of pelvic surgery or symptoms and/or physical signs indicating one of the manifest urological or neurological disorders (other than migraine and other chronic headaches).

Eleven patients (six females) had bilateral and 32 patients had unilateral complaints (17 right [11 females] and 15 left [eight females]). Asymptomatic sides of the patients who had unilateral symptoms were considered to be clinically normal. Thus, 86 (43 × 2) pudendal nerves were evaluated in the study. Fifty-four nerves (both pudendal nerves of the bilateral cases and symptomatic nerves of the unilateral cases) constituted the symptomatic group, and 32 nerves on the asymptomatic sides of unilateral cases formed the asymptomatic group.

Electrophysiological studies were performed by using a Keypoint-net (Natus Medical Inc., Middleton, USA) electrophysiology unit. Stimulation was performed by using bar electrodes with saline-soaked felt-pads (diameter: 4 mm, inter-electrode distance: 2.5 cm). In female subjects, the stimulator cathode was placed just laterally to the clitoris on either side, between the minor and major labia, and the anode was placed posteriorly. In the male subjects, the anode was placed just proximally to the corona of the glans on the most lateral side of the penis with the cathode pointing proximally. The stimulator bar was secured to the position by adhesive tapes. The ground electrode was placed on the ipsilateral iliac spine.

Square-wave electrical pulses of 0.2 ms duration were delivered at 2 Hz. The intensity of electrical stimulation was adjusted as 2 times the sensory threshold to avoid stimulating the nerve on the contralateral side. This intensity was well below the pain threshold and easily tolerated.

SEP responses were recorded using 9 mm cup electrodes placed on the points 2 cm behind the Cz and Fpz, according to the international 10-20 system.^[25] The bandpass filter was between 5 and 3000 Hz. Sensitivity was 5 μV/division and sweep speed was 10 ms/division.

Each subject was requested to close his/her eyes, open the mouth slightly and stay as relaxed as possible during the recordings. Recordings were performed by stimulating the right and left sides separately.

Three SEP recordings composed of at least 350 averaged responses were obtained in the supine position. Then, the subject was positioned to the sitting posture by hanging his/her legs down the lateral edge of the examination table without getting support from their arms, while the feet were not touching the ground and the hip and knee joints were flexed about 90°. In the control group, the duration of the sitting position was decided to be 20 min, which had been generally adequate to trigger the pain in most of the PNE patients.^[23] In the study group, this period was also 20 min if the patient was able to tolerate. If the patient was not able to maintain the position (due to severe pain or disappearance of the SEP responses), the study was terminated. In subjects who maintained the position for 20 min, up to 10–12 recordings composed of at least 350 averaged responses were achieved. If the subjects were unable to complete sitting period, fewer recordings could be obtained. Then, the subjects were moved into supine position again and four consecutive averaged recordings were made. The differences between the amplitudes of the responses elicited at the first lying position and those recorded at the end of the sitting position were calculated and expressed as percentage changes. The pudendal nerves with unobtainable responses at the first supine position and those suffering more than 45% decrease in the amplitude at the end of sitting position were coded as having abnormal SEP studies.^[23]

In pudendal MRI, the patients were imaged using an 8-channel anterior TORSO multitransmit coil on a 3T scanner (Ingenia, Philips, NL). The following sequences were obtained: Fat-saturated T2 W axial (T2 SPAIR; TR/TE, 6000/80; echo train length 17; slice thickness, 3; FOV 210; matrix 210 × 180), T1W axial (TR/TE, 595/10; echo train length 4; slice thickness, 3; FOV 190; matrix 240 × 200), fat-saturated proton-density coronal (TR/TE, 4200/30; echo train length 20; slice thickness, 3; FOV 250 matrix 256 × 200) and contrast-enhanced fat-saturated T1W axial and coronal (TR/TE, 520/10; echo train length 4; slice thickness, 3; FOV 210; matrix 264 × 228). Images were evaluated by the same radiologist blinded to the diagnoses of the patients. In accordance with the earlier reports, the main criteria for the presence of an abnormality in or around a pudendal nerve were increased T2 signal and/or the thickness of the nerve, prominence of the neighboring neurovascular bundle, contrast enhancement in any segment of the nerve and perineural scarring.^{[14],[15],[16],[17],[18]} Some other abnormal findings presented in [Table 1] were also included in this list due to their presence in or around the symptomatic pudendal nerve.

Table 1: Abnormal findings in pudendal magnetic resonance imaging

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Statistical analyses were performed using SPSS software version 25 and MedCalc Statistical Software version 18.6 (MedCalc Software bvba, Ostend, Belgium; http://www.medcalc.org; 2018). Descriptive analyses were presented using frequencies and percentages. McNemar test was used to compare the proportions between methods. The agreement between two different methods was investigated using the Kappa test. For the estimation of best cutoff points to discriminate the abnormal MRI and SEP findings elicited in the symptomatic group according to the clinical diagnosis, analysis receiver operating characteristics (ROC) was performed, and the area under the curve was calculated.

When a significant cut-off value was observed, the sensitivity, specificity, positive and negative predictive values were presented. While evaluating the area under the curve, a 5% type-I error level was used to accept a statistically significant predictive value of the test. A 5% type-I error level was used to infer a statistical significance.

Results

The abnormal pudendal MRI findings elicited in the present study are shown in [Table 1] and [Figure 1].

Figure 1: T1W (a) and fat saturated T2W (b) images demonstrate bilateral normal pudendal neurovascular bundles (arrows). Consecutive fat saturated gadolinium enhanced T1 W images (c and d) demonstrate enhancement (thin arrow) on left pudendal nerve and asymmetrical prominency (thick arrow) on left pudendal neurovascular bundle. T1W image (e) reveal mild thickening of right pudendal nerve and perineural scarring (thin arrow) with normal neurovascular bundles on fat saturated T2W images(f) on both sides at the level of Alcock's canal (thick arrows). T1 W (g) and fat saturated T2 W (h) images demonstrate mild prominency on left neurovascular bundle at the level of ischial spine

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By taking the clinical diagnosis as the gold standard, a comparison of the results of MRI and dynamic pudendal SEP studies can be summarized as follows:

Dynamic pudendal SEP studies: 8 patients (2 females) had bilaterally normal SEPs, 9 patients (5 females) had bilaterally abnormal SEPs, 13 patients (9 females) had abnormal SEPs on the right side, and 13 patients (8 females) had abnormal SEPs on the left side

[Figure 2]

Dynamic pudendal SEP studies were found to be abnormal in 42 and normal in 12 of the 54 clinically symptomatic nerves
Dynamic pudendal SEPs were abnormal in 2 and normal in 30 of the 32 clinically asymptomatic nerves.
Pudendal MRI results: 17 patients (8 females) had bilaterally normal pudendal MRI studies, 5 patients (3 females) had abnormal findings on the right side, and 21 patients (14 females) had abnormal findings on the left side [Figure 3]

Pudendal MRI was abnormal in 19 and normal in 35 of the 54 clinically symptomatic nerves
Pudendal MRI was abnormal in 8 and normal in 24 of the 32 clinically asymptomatic nerves.

When the results of dynamic pudendal SEP and MRI were compared [Figure 4]:

Pudendal MRI was normal in 31 and abnormal in 11 of 42 pudendal nerves, which had normal SEP findings
Pudendal MRI was normal in 29 and abnormal in 15 of 44 pudendal nerves, which had abnormal SEP findings.

When the ROC analyses were performed by accepting the clinical diagnoses based on Nantes criteria as a gold standard: Dynamic pudendal SEP studies had 77.78% sensitivity and 93.75% specificity with a Youden index of 0.7153. In the same analyses, pudendal MRI could not discriminate symptomatic and asymptomatic pudendal nerves by having the best cut-off that gave 33.3% sensitivity and 75% specificity with a Youden index of 0.0833 [Figure 5].

There was 84% agreement between clinical diagnosis and dynamic pudendal SEP
There was 49% agreement between clinical diagnosis and pudendal MRI
There was 53% agreement between dynamic pudendal SEP and pudendal MRI. Dynamic pudendal SEPs of all the patients who had abnormal pudendal MRI were also abnormal.

Figure 2: Clinical diagnosis and somatosensory evoked potential agreement

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Figure 3: Clinical diagnosis and magnetic resonance imaging agreement

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Figure 4: Magnetic resonance imaging and somatosensory evoked potential agreement

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Figure 5: Dynamic pudendal somatosensory evoked potential studies had 77.78% sensitivity and 93.75% specificity with a Youden index of 0.7153 and pudendal magnetic resonance imaging had 33.3% sensitivity and 75% specificity with a Youden index of 0.0833 on the receiver operating characteristics analyses performed by accepting the clinical diagnoses based on Nantes criteria as a gold standard

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Discussion

PN is a common cause of chronic resistant perineal pain. The etiology of PN has not yet clearly understood.^[8],[9] Its clinical diagnosis primarily depends on clinical evidence, mostly on the typical patient history. Although clinical diagnosis, summarized in the Nantes criteria, has been recognized as the gold standard for PN, modern medical understanding needs objective tests to support and substantialize the diagnosis.^[13]

Electrodiagnostic studies have limited accomplishment in the evaluation of PN.^[20],[21] SEP is one of the most frequently used techniques due to its noninvasive and relatively painless methodology.^[21],[22] Although traditional SEP methods generally have not been successful to reveal pudendal nerve dysfunction, the novel dynamic pudendal SEP technique used in this study provided good cut-off values in discriminating the patients with the aid of provocation by positioning the patient and unilateral stimulation of each side.^[23]

While electrophysiological studies provide information about the function of the nerve, pudendal MRI is expected to provide information about normal and abnormal structural details throughout the pudendal nerve.^{[14],[15],[16],[17],[18]} Despite all the positive contributions of pudendal MRI, it also has some limitations. The pudendal nerve is thin, and therefore, its evaluation is frequently limited due to poor spatial resolution, even with a 3T scanner. Inhomogeneous fat suppression, nerve branching variations, and surrounding vessels, especially in the setting of pelvic venous congestion, may obscure the nerve.^{[14],[15],[16],[17],[18]} Therefore, the findings may be very subtle, and this can limit the objective radiological evaluation.

In pudendal MRI, asymmetrical appearances of the structures are the main features facilitating to decide about the presence of abnormal findings.^{[14],[15],[16],[17],[18]} However, asymmetrical findings may not be present in case of bilateral PN, and pudendal MRI can be misinterpreted as to be normal. In addition, PN can be categorized into four major types based on the location of the entrapment.^[14] In the patients who have type IV PN, where the distal branches are entrapped, pudendal MRI may not provide sufficient findings due to the fact that distal branches are too thin. Finally, pudendal MRI has low reliability due to the lack of established criteria for normality and abnormality of the nerve and adjacent structures. However, MRI is very helpful to find other confounding causes of pelvic pain, such as endometriosis and unsuspected pelvic mass lesions, which take place in the differential diagnosis.^[24]

Conclusions

In the present study, the dynamic pudendal SEP method provided good sensitivity and specificity in discriminating the symptomatic and asymptomatic pudendal nerves with a good agreement with the clinical diagnosis. Although MRI had some acceptable level of specificity, it could not make this discrimination with sufficient sensitivity. MRI's agreements with the clinical diagnosis and dynamic pudendal SEP were also poor. As a result, MRI of the pudendal nerve at least with the methods described herein is not satisfactory for to be used in substantiating the presence of pudendal entrapment neuropathies.

It seems that the best laboratory method for the diagnosis and follow-up of pudendal nerve dysfunction is currently the dynamic pudendal SEP study. On the other hand, although the dynamic SEP is good at supporting the diagnosis, its capability in localizing the lesion site and determining the nature of the lesion are limited. Therefore, it must be complemented by other methods, preferably by those coming from imaging grounds. MRI is expected to supplement the information gained from clinical and electrodiagnostic findings with its ability to detect the normal and abnormal appearance of the major nerves, as well as the surrounding soft tissue abnormalities.^{[14],[15],[16],[17],[18]} Although MRI is being increasingly used in the setting of suspected PN, the results of the present study imply that its current methodology used in the routine clinical settings is not sufficient for PN.^{[14],[15],[16],[17],[18]} Further refinement of the MRI methodology, more clear-cut description of the abnormal findings, and the probable help from the other imaging areas, such as diffusion tensor imaging, are awaited to fill the gap in this area.

Financial support and sponsorship

Nil.

Conflicts of interest

There are no conflicts of interest.

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