Добавил:
Sekretar
kiopkiopkiop18@yandex.ru
t.me/Prokururor I Вовсе не секретарь, но почту проверяю
Опубликованный материал нарушает ваши авторские права? Сообщите нам.
Вуз:
Предмет:
Файл:Ординатура / Хирургия / @xirurgi_2025 / @xirurgi_2025 - 1010 - файл
.pdf
Part X
On Asymmetry in Sphincters
X
Chapter 34
Chapter 34 Functional Asymmetry of Pelvic Floor Innerva-
469
Functional Asymmetry of Pelvic Floor
Innervation and Its Potential Role in the
34
Pathogenesis of Fecal and Urinary Incontinence –
Report from the EU-sponsored Research Project
OASIS (On Asymmetry In Sphincters)
Paul Enck,Fernando Azpiroz,Roberto Merletti
Contents
34.1 Assessment of Pelvic Floor Innervation
by Conventional Neurophysiological Techniques . . . . 470
34.1.1 Neurophysiology of the Pelvic Floor . . . . . . . . . . . 470
34.1.2 Unilateral Pudendal Neuropathy – Fact or Fiction? . . . 470
34.1.3 Evidence for Functional Asymmetry
of Pelvic Floor Innervation . . . . . . . . . . . . . . . . 471
34.1.3.1 Intraoperative Monitoring of Pudendal Sensory
and Motor Pathways . . . . . . . . . . . . . . . . . . . . 471
34.1.3.2 Central (Cortical) Representation of Motor
and Sensory Functions of the Pelvic Floor . . . . . . . . 472
34.1.3.3 Peripheral Nerve Stimulation and Recording . . . . . . 472
34.1.4 Clinical Relevance of Asymmetry in Patients
with Incontinence . . . . . . . . . . . . . . . . . . . . . . 473
34.2 The Project OASIS . . . . . . . . . . . . . . . . . . . . . 474
34.2.1 Multiple-Electrode Array Surface EMG
to Study Sphincter Innervation . . . . . . . . . . . . . . 474
34.2.2 Background of Surface EMG Technology . . . . . . . . . 474
34.2.3 Muscle Anatomy and Concepts Behind
the Array Detection . . . . . . . . . . . . . . . . . . . . . 475
34.2.4 An Anal Probe with Multiple Electrode Arrays . . . . . . 476
34.2.5 Signal Interpretation and Development
of Sphincter Models . . . . . . . . . . . . . . . . . . . . 478
34.2.5.1 Models . . . . . . . . . . . . . . . . . . . . . . . . . . . . 478
34.3 First Results of the OASIS Technique to Study Healthy,
Continent Subjects . . . . . . . . . . . . . . . . . . . . . 480
34.3.1 EMG Signal Amplitude . . . . . . . . . . . . . . . . . . . 480
34.3.2 Noninvasive Assessment
of Muscle Anatomical Properties . . . . . . . . . . . . . 480
34.3.3 Detection of Single Motor Unit Activities . . . . . . . . . 480
34.3.4 Estimation of Muscle Fiber Conduction Velocity . . . . 482
34.3.5 Differences in Sphincter Innervation
Between Men and Women . . . . . . . . . . . . . . . . . 484
References . . . . . . . . . . . . . . . . . . . . . . . . . . 488
34
470
Paul Enck, Fernando Azpiroz, Roberto Merletti
34.1 Assessment of Pelvic Floor Innervation
by Conventional Neurophysiological Techniques
34.1.1 Neurophysiology of the Pelvic Floor
Incontinence to urine and/or stool can derive from a variety of clinical conditions,
some of which are primary events where incontinence is an unavoidable consequence
of the disease such as bladder and/or anal/rectal cancer or inflammation of the respective storage organs. In many systemic disorders, incontinence occurs as the consequence of direct involvement of neural pathways to and from the bladder and anorectum such as in multiple sclerosis,diabetes mellitus, and other diseases.Finally,if injury of the continence organs occurs with surgery (e.g., episiotomy) or trauma (e.g.,delivery), incontinence may be the consequence (Hinninghofen and Enck 2003).In many
cases, however, incontinence appears to be idiopathic, that is without an immediate
preceding event, and is usually attributed to age-related degeneration of the neuromuscular apparatus maintaining continence or to traumatic events in the past (e.g.,
childbirth). As neurophysiological diagnostic testing has revealed pathological findings in many of these patients, idiopathic incontinence is frequently also labeled neurogenic (Kiff and Swash 1984).
Except for the determination of the terminal motor latency of the pudendal nerve
(PNTML) by a less invasive technique (Kiff and Swash 1984), where a glove-mounted
surface electrode is used to stimulate the pudendal nerve through the rectal wall, and
evoked responses are recorded from the anal sphincter by another pair of electrodes at
the finger base, the neurophysiology of pelvic floor functions (Vodusek 2004) has never been a clinical routine tool used by many investigators and in many patients. This is
because needle EMG is an invasive and painful procedure for the patient and requires
a great deal of experience on the side of the clinician.
Besides PNTML recording, surface EMG has only been used for assessment of the
latencies of corticoanal afferent and efferent pathways – for the whole pathway as well
as for fractions thereof – via recordings of somatosensory and motor evoked potentials (Enck et al. 1992),and mainly for research purposes only.
Consequently, very little is known about the normal neurophysiology of pelvic
floor innervation in healthy volunteers,and contribution of its neuropathology to the
pathogenesis of fecal and or urinary incontinence. This is especially true for the question of whether innervation of the pelvic floor sphincters is symmetrical or asymmetrical in nature even in healthy volunteers, and whether this can be a contributing factor to the occurrence of incontinence symptoms.
34.1.2 Unilateral Pudendal Neuropathy – Fact or Fiction?
Routine clinical experience with recording of PNTML (Kiff and Swash 1984) will occasionally result in differences in potential amplitudes and latencies, which have been attributed by some authors to unilateral pudendal neuropathy but were assumed to be
due to technical difficulties to achieve a good electrode-to-pudendal nerve contact on
both sides during rectal digital examination by others.
Of all patients with pelvic floor problems undergoing PNTML in a study by Sangwan et al. (1996),8% had no response on both sides and 14% responses from one side
only. In the remaining patients, 61% had normal and 39% had abnormal PNTML; of all
Chapter 34 Functional Asymmetry of Pelvic Floor Innervation
patients with abnormal PNTML, 28% were delayed on both sides,and 71% on one side
only. In total, one-quarter of patients had what the authors called unilateral pudendal
neuropathy.In a similar but larger report from another group (Lubowski et al. 1988),
15% of PNTML investigations showed delayed or missing response on one side only.
However, another explanation for this phenomenon would be that despite its anatomical symmetry, pudendal nerve function may also be asymmetrical in some subjects, as is the case with other bilaterally innervated organs (e.g., the esophagus)
(Hamdy et al.1997). If this holds true,is may carry significant clinical implications specifically in those subjects with asymmetry of innervation, e.g., in case of unilateral
trauma (Enck et al. 1996).A research hypothesis based on this assumption is illustrated in Fig. 34.1 and was the basis of subsequently conducted research.
34.1.3 Evidence for Functional Asymmetry
of Pelvic Floor Innervation
Three approaches have been taken to evaluate functional asymmetry of pelvic floor
innervation in healthy subjects and in patients.
34.1.3.1 Intraoperative Monitoring of Pudendal Sensory
and Motor Pathways
Deletis et al. (1992) investigated children in whom individual dorsal root action potentials from the S1–S3 roots were recorded intraoperatively after electrical stimulation of
the dorsal penile or clitoral nerves, in preparation for surgery within the cauda equina. In most patients, pudendal afferent activity was present in S2 and S3 bilaterally; in
some, the afferent activity was confined to a single root bilaterally, and in one,to a single root on one side. No lesion of the roots or rootlets carrying significant afferent activity was created during the rhizotomy, and no dysfunction in micturition resulted.In
a replication study by the same groups (Huang et al. 1997), the pudendal afferent distribution was often confined to a single level in 18% of the patients or even to a single
root in 7.6%. None of the patients thus mapped developed long-term bowel or bladder
complications when the dominant root was saved from rhizotomy. Recently, Deletis
and co-workers (Krzan et al.1999) compared the radicular distribution of anal and pe-
471
Fig. 34.1. A research hypothesis of the clinical relevance of functional pudendal nerve asymmetry in case of unilateral trauma, i.e.,the same trauma can have entirely different consequences
34
472
Paul Enck, Fernando Azpiroz, Roberto Merletti
nile/clitoral afferents in 22 of these children and found that in more than half of the
patients,the main carrier was identical,while in 41% the main carrier of anal afferents
was caudal to that of penile/clitoral afferents. In 9% the main and only carrier of anal
afferents was a single root.Dissociation of fecal and urinary incontinence could be explained by different primary sacral carrier roots for anal and penile/clitoral afferents.
Sacral spinal root pacemaker implantation is a new technique in treatment of fecal
incontinence but requires intraoperative decision as to which two of the six potentially functional sacral spinal nerves should carry the electrodes. Matzel et al. (1999) investigated incontinent patients undergoing evaluation for chronic sacral spinal nerve
stimulation and continent patients undergoing testing for treatment of neurogenic
bladder.Both in continent as well as in incontinent patients,the dominant level was often not symmetrical, and in many cases,the highest responses obtained from left- and
right-side root stimulation were not on the same level.
34.1.3.2 Central (Cortical) Representation of Motor
and Sensory Functions of the Pelvic Floor
Topographic cortical mapping of both cerebral hemispheres was performed by Turnbull et al. (1999) in healthy subjects by applying suprathreshold transcranial magnetic
stimulation (TMS) to individual points on a scalp grid centered over the vertex and
then recording the electromyographic responses from the external anal sphincter, rectum, and tibialis anterior muscles. Cortical mapping showed that the anal responses
were bilaterally represented on the superior motor cortex of both cerebral hemispheres; a similar topography was found for the rectal responses. A similar study by
another group that was undertaken (Witscher et al. 1998) in healthy volunteers showed
latencies and motor thresholds to be similar between the dominant and the nondominant hemisphere, but the area over the nondominant hemisphere was significantly
larger compared to the dominant one. In two out of ten cases, the intraindividual left :
right area of activation was asymmetric (>30% difference), in one case each the left or
the right side was dominant. This distribution was not related to handedness.
To compare cortical responses following electrical stimulation of the human anal
canal to responses after stimulation of median and tibial nerves, Stottrop et al. (1998)
employed magnetoencephalography (MEG). Electrical stimuli were applied to the
anal canal, and to median and tibial nerves at different repetition rates,using belowpain-threshold intensities.Magnetic brain responses were averaged time-locked to the
stimuli. Magnetic responses to stimulation of the anal canal were explained by unilateral (five subjects) or bilateral (two subjects) sources; at least in a subgroup of volunteers this representation is asymmetrical.
34.1.3.3 Peripheral Nerve Stimulation and Recording
As outlined above, individual differences between the left and right pudendal nerve
terminal motor latency (PNTML) can occasionally be found in healthy humans. This
was first described as normal in healthy subjects by Hamdy et al.(1998).When they investigated healthy subjects following transcranial magnetic stimulation (TMS) conditioning of the motor pathway before applying PNTML stimuli, right or left pudendal
nerve stimulation evoked anal responses of similar latencies but with significant
asymmetric amplitudes in six of eight subjects (Hamdy et al.1999).
Chapter 34 Functional Asymmetry of Pelvic Floor Innervation
To explore whether muscular function of the external anal sphincter (EAS) is symmetrical or asymmetrical in healthy volunteers, healthy volunteers were investigated
by needle EMG of the anal sphincter muscle (Middelsdorf et al. 1998),and significant
intraindividual asymmetries of EMAP amplitudes were found in approximately onethird of cases. None of the differences found were directly related to gender and age of
the subjects.
In summary, there is sufficient empirical evidence to assume that the left-to-right
ratio of pelvic floor functions is asymmetrical in a subgroup of volunteers and/or patients; based on the preliminary data cited above, this fraction may be about 20%,
while in the remaining, the function may be symmetrical. It is currently open to discussion whether this asymmetry is cortical in nature, or whether any cortical sign of
asymmetry only reflects peripheral dominance of pudendal pathway utilization. This
needs to be studied in more detail in the future.
34.1.4 Clinical Relevance of Asymmetry in Patients
with Incontinence
Left and right side anal surface EMG (S-EMG) recordings by means of a modified anal
plug electrode and a conventional S-EMG system was used to assess the innervation of
the external anal sphincter at both sides in the anal canal separately in Wietek et al.
(2002). Three cohorts were studied: nulliparous women in the third trimester (Study
1), primiparae within 6 months after nontraumatic vaginal delivery (Study 2), and
women after childbirth-related third- or fourth-degree perineal tear 6–12 months
postpartum (Study 3). Approximately 40% of nulliparous women reported signs of
mild fecal incontinence; however, relative asymmetry was neither correlated to symptom severity nor to manometric measures (Study 1).In Study 2, 40% of women had an
episiotomy performed, of which one-third developed severe incontinence.The association between asymmetry and incontinence did not reach significance level; however,
comparison of pre and postpartum measures of S-EMG showed high reproducibility
within subjects. In study 3,approximately 40% of women reported moderate to severe
incontinence. Asymmetry and symptom severity were significantly correlated. Manometry revealed a significant negative correlation between relative asymmetry and
squeeze pressure but not with resting pressure. It was concluded that functional asymmetry of anal sphincter innervation is associated with incontinence symptoms, but
only after childbirth-related injuries (trauma) (Wietek et al.2002).
With the same technique, a large series of consecutive patients with fecal incontinence were investigated during routine diagnostic work-up of an incontinence outpatient clinic (Hinninghofen et al. 2003) to assess the functional innervation of the leftand right-side external anal sphincter (EAS). Besides being investigated by mass surface EMG, all patients underwent conventional clinical diagnostic work-up including
anorectal manometry,endoanal ultrasound, defecography, and other routines.A symmetry index was computed (SI=mean(left-right)/max(left,right) of the EMG amplitude), defining the relative S-EMG amplitude symmetry between 0=symmetric and
1=asymmetric. A subgroup of 30% of the patients were regarded as asymmetric. More
women than men were identified as asymmetric, and the association between female
gender and asymmetry status was significant. Among the (female) patients with
asymmetric innervation, two out of three had a history of deliveries. The symmetry
status (SI) between women with childbirth was significantly higher than in those
without, but the degree of asymmetry was not related to the number of childbirths.
473
34
474
Paul Enck, Fernando Azpiroz, Roberto Merletti
Asymmetry degree was also correlated with the results of diagnostic work-up to
identify major determinants and consequences of relative asymmetry,but without the
clinical investigators knowing the results of symmetry assessment. In both men and
women, a significant and negative correlation of SI to the EAS squeeze pressure was
found,and a positive association with sphincter defects detected during endosonography. Association with EAS squeeze pressure was stronger in men than in women, but
in men, the SI was also correlated positively to resting pressure.
The symmetry status (SI) also correlated with the degree of incontinence, as assessed by the Wexner Score: patients with severe incontinence were significantly more
frequently asymmetric than those with mild incontinence.
Functional asymmetry of EAS innervation appears to vary from physiological to
pathophysiological grades, and in the latter case, results in decreased squeeze pressures of the EAS. However, overall moderate to weak correlations indicate other important factors contributing to symptom development and severity on the one hand
and asymmetry of sphincter innervation on the other.
34.2 The Project OASIS
34.2.1 Multiple-Electrode Array Surface EMG
to Study Sphincter Innervation
While the above-cited literature gives preliminary evidence to the clinical relevance of
functional asymmetry of sphincter innervation, important questions remain, which
can only be resolved with a new technology that allows screening of pelvic floor innervation in large patient and volunteer cohorts.This in itself excludes conventional neurophysiological techniques based on needle EMG from this task. On the other hand,
surface EMG has so far only been used to evaluate within-subject changes of pelvic
floor function with therapy,e.g., after biofeedback training (Enck 1993), or latencies of
somatosensory and somatomotor responses following central, spinal, or peripheral
stimulation of the pathways (Kiff and Swash 1984; Sangwan et al. 1996; Swash 2002;
Vodusek 2004). It is not regarded as an appropriate technique to diagnose pelvic floor
innervation and its dysfunctions (Pullman et al. 2000).
A recently described new technology using multielectrode arrays (MEA) to study
individual motor unit action potentials (MUAP) from large muscles in the body’s periphery (Merletti et al. 1999a, b) was the starting point of a European Communitysponsored research project whose first results were reported recently (Hinninghofen
et al. 2002; Liu et al.2002; Merletti et al.2004). It was named OASIS (On Asymmetry in
Sphincters – The role of functional asymmetry in sphincter innervation for incontinence, QLRT-2001-00218) and included four clinical partners (from gastroenterology,
surgery,gynecology, and urology), a technical partner for biomedical engineering, and
two small industrial partners. It started working in January 2002 for a total of 3 years.
34.2.2 Background of Surface EMG Technology
Although the detection of surface EMG signals is relatively easy, the interpretation of
the signal features for understanding physiological mechanisms and monitoring pathological conditions is a complex task (Farina et al. 2004c).Surface EMG signals are in-
Chapter 34 Functional Asymmetry of Pelvic Floor Innervation
deed affected by many factors whose effect on the variables extracted from the signal
is often not intuitive. As an example, it has been only recently recognized that EMG
signals detected at different locations over the same muscle may have significantly different amplitudes (Roy et al.1986; Jensen et al.1993), which implies that electrode location is of primary importance for comparing results (Hermes and Freriks 1997). The
difficulties in interpreting results has led, in some cases, to rather strong critiques of
this noninvasive technique (Haig et al. 1996; Pullman et al. 2000).
The most frequently used montage for surface EMG signal detection is the bipolar
configuration, which consists in recording the difference between signals detected by
two electrodes placed over the same muscle at a certain distance from each other. This
detection modality has been used in many studies on the assessment of the external
anal sphincter (EAS) functions (e.g., Kiesswetter 1976; Nielsen et al. 1985; O’Donnell et
al. 1988; Binnie et al. 1991) with a variety of electrode shapes, sizes, and locations. Signals recorded by the bipolar configuration are affected by anatomical, geometrical,
physical and detection system parameters (Farina et al. 2002). Among these factors,
the most relevant are the thickness of the layers interposed between the electrodes and
the muscle,the tissue in-homogeneities, the length of the fibers, the interelectrode distance, the shape and size of the electrodes and the relative location and orientation of
the electrodes with respect to the muscle fibers. The relevance of these factors for the
interpretation of results depends on the specific muscle architecture.
In recent years,efforts have overcome the limitations of the classic bipolar EMG recording technique (Zwarts and Stegeman 2003). The followed approach has been
based on increasing the number of electrodes placed over the muscle in order to obtain a map of the potential distribution over the skin rather than a single local observation. The use of multichannel surface EMG makes it possible to concomitantly detect bipolar EMG derivations from a number of locations over the muscle. The availability of more than one detection point may be useful for the selection of the optimal
locations to reliably extract the descriptive variables of the signal. Moreover, it provides an insight into the mechanisms of generation of the signals, which may help in
understanding and reducing the sources of artifact in the detection.
In the research field, multichannel surface EMG is being recorded from muscles of
rather simple architecture. In the case of the EAS, the placement of many detection
systems over the muscle presents important technological limitations. Recently, these
limitations have been overcome, and systems for surface EMG detection from this
muscle with up to 48 electrodes have been presented (Merletti et al. 2002, 2004; Enck
et al. 2004a).
475
34.2.3 Muscle Anatomy and Concepts Behind the Array Detection
Muscles are composed of nearly parallel fibers that constitute the contractile structural units. A motoneuron innervates a group of muscle fibers, which thus constitutes
the smallest functional unit of the muscle. The motoneuron and the fibers it innervates are called a motor unit (MU). Muscle fibers of a MU are randomly distributed in
the muscle (MU territory) and each axon reaches the fibers by the neuromuscular
junctions. The pool of neuromuscular junctions of the fibers belonging to a MU is distributed in a territory,termed innervation zone.
The electric impulse that propagates along the motoneuron and reaches the neuromuscular junction determines the excitation of the muscle fiber membranes and the
generation of propagating action potentials. A transmembrane current distribution
476
Paul Enck, Fernando Azpiroz, Roberto Merletti
(depolarization zone) corresponds to this potential distribution. The depolarization
zones propagate without attenuation along the muscle fibers from the neuromuscular
junctions to the two tendon endings (Fig. 34.2).The velocity with which the action potential propagates depends on the fiber diameter and type and is termed muscle fiber
conduction velocity (CV). The intracellular action potentials generate and extinguish
at the neuromuscular junctions and tendons, respectively. The summation of the action potentials generated by fibers innervated by a single motoneuron determines the
MU action potential.
Each depolarization zone can be seen as a moving source of electric field at some
depth below the skin. If the source moves along the fiber, the surface potential distribution will move with it. An electrode system placed on the skin will detect an interference signal due to the contributions of the action potential trains of all the active
MUs.Increasing contraction force results in activation (recruitment) of an increasing
number of progressively larger MUs and in an increase in the frequency of activation
(firing rate) of those already active (Henneman’s principle). The set of activation instants of a MU is termed firing pattern.
Figure 34.1a shows the characteristics of EMG signals detected at different locations
along the biceps brachii muscle. The detection is performed by a number of equally
spaced bipolar recordings, located along a line. This multichannel system is also
known as linear electrode array (Masuda et al. 1998; Merletti et al. 1999a,2003). The array detects signals with similar shape, which propagate in two opposite directions
starting from the innervation zone. The basic idea is to locate electrodes along the
muscle fiber orientation covering the entire muscle length.
34
34.2.4 An Anal Probe with Multiple Electrode Arrays
Following the concepts behind the design of a linear array,in the case of the EAS it is
necessary to locate electrodes around circumferences in order to follow the main muscle fiber orientation.As in the case of electrodes displaced longitudinally along rectilinear fibers (Fig. 34.2), the displacement of electrodes along a circumference allows
the detection of the MU action potentials from their generation at the innervation
zone to their extinction at the tendon endings. For this purpose, a specific probe was
designed (Merletti et al. 2003,2004; Enck et al. 2004b).
The anal probe (Fig. 34.2) is composed of a rounded-tip plastic cylinder, 150 mm in
length and 14 mm in diameter,holding a circumferential array of 16 equally spaced silver bar electrodes, located at a distance of 20 mm from the probe tip and aligned with
the probe axis.A flexible, multiwire cable encapsulated in silicone rubber is provided
at the bottom of the probe,and is used to connect the circular array to a multichannel
EMG amplifier.
A small plastic marking, encapsulated in the probe tip,indicates electrode 1 and the
direction of numbering. A plastic fin at the end of the probe, also aligned with electrode 1, helps the operator in checking the orientation of the probe with respect to a
fixed reference during and after insertion.
The probe is manufactured using a purposely designed machine, which injects
melted biocompatible plastic (polystyrene) at a temperature of 250°C into a metallic
mold, with a pressure of 120 atm and a variable injection speed. The probe can be sterilized chemically and is autoclavable.
By means of a multichannel electromyograph for surface EMG signals to which the
probe is connected, each bipolar signal is amplified, band-pass filtered and acquired
Соседние файлы в папке @xirurgi_2025