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Chapter 34 Functional Asymmetry of Pelvic Floor Innervation
477
lengths, number of fibers and innervation zone positions (IZ1 and IZ2) are depicted as an example.c Sample epoch, 500 ms long,of multichannel single dif-
ic representation of anal probe position with respect to the external anal sphincter muscle; two motor units (MU#1 and MU#2), characterized by different
ferential EMG signals, detected with the probe shown in B1 on external anal sphincter muscle at maximum contraction level. Some MUs seem to be inner-
Fig. 34.2a–c. Principles of multichannel surface EMG detection with circular arrays from anal sphincter muscles (a–c). a 16-channel anal probe.b Schemat-
vated at one extremity
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Paul Enck, Fernando Azpiroz, Roberto Merletti
by a PC equipped with an analog-to-digital (A/D) conversion board and with a purposely designed acquisition and display software.Galvanic insulation through optical
coupling is present between the probe and the acquisition system,providing a high degree of safety to the patient and protection from electrical shocks.
Figure 34.2 also shows example signals detected with the system described above.
Similar signal features as in the case of other muscles can be recognized. In particular,
the action potentials propagating from the innervation zone and terminating at the fiber endings can be detected from the multichannel recordings.
A similar probe carrying 3 ×12 electrodes was developed for recording of MUAP
from the urethral sphincter; however, due to technical difficulties and challenges (limited size, hygiene requirements, etc.) during development we are not able to report
systematic data at this point.
34.2.5 Signal Interpretation and Development
of Sphincter Models
The multichannel recordings are the summation of the action potentials of the active
MUs. The decomposition of surface EMG signals is the procedure for the detection
and extraction of the contributions of the single MUs. The ability to track the activity
of single MUs allows the study of central and peripheral properties of the neuromuscular system such as motor control strategies and MU anatomical and physiological
properties. For the purpose of the decomposition, double differential signals (obtained by subtraction of two consecutive bipolar recordings) are often used to enhance the selectivity of the detection.
A software tool for the analysis of single MU properties developed by Gazzoni et al.
(2004) was applied to signals detected from the EAS using the probe described in the
previous section. The method is automatic, without interaction with the operator,and
involves a segmentation phase and a classification procedure (to detect action potentials and identify the MUs to which they belong), which adapts to slow changes of the
MU action potential shapes.
Surface EMG signals detected with electrode arrays provide more information with
respect to each signal considered independently.The partial redundancy (i.e., the observation of the same phenomena from different detection points) of the information
provided by multichannel detection can be advantageously used by the decomposition
technique for MU action potential identification, making it possible to identify discriminative information for the classification. At this moment, the method is not able
to resolve superpositions of MU action potentials; for this reason, the detection of almost all the activation instants of the MUs significantly contributing to the signal is
possible only in specific cases.In general, an incomplete firing pattern is extracted.
34.2.5.1 Models
A model is a set of equations describing a physical system which predicts,to a certain
extent,the changes in the system as a consequence of modifications in the parameters.
One of the greatest problems when studying a mathematical model of a physiological
system is biological complexity, which requires using substantial approximations in
the model. It is of fundamental importance to tackle the difficulties with a gradual approach, testing the hypothesis, fitting simulations with experiments, critically analyz-
Chapter 34 Functional Asymmetry of Pelvic Floor Innervation
ing the improvements in the prediction and interpretation capabilities of the models.
Indeed, the detailed geometry and parameters are usually unknown, so that a precise
model is usually not available. Furthermore, the parameters change among subjects,
so that a set of parameters properly selected for a subject may be useless when studying another individual. Besides these limitations, modeling has an important role in
the interpretation of experimental results since it provides (a) indications on the sensitivity of signal features to the physiological mechanisms under study and (b) an estimation of system parameters that cannot be measured directly. For example,starting
from a simple mathematical model of a sphincter as a perfect cylindrical muscle (Farina et al. 2004a,b),as shown in Fig. 34.3, numerical experiments can be performed to
generate the surface EMG detected in different conditions, varying anatomical or
physiological parameters such as fiber length or position. Such simulations can be
useful to compare detection system performance in different conditions, to improve
their design or select the best way to use them. Moreover, comparing experimental
data with the simulations,it is possible to infer the value of unknown parameters or of
the actual geometrical configuration.
479
Fig. 34.3. a Geometry of a mathematical model of a sphincter as a circular cylinder (Farina et al.
2004b). b Example of simulation of single differential surface EMG signals detected with 16
channels. The muscle fiber is 1 mm deep within the muscle. The innervation zone is at –90°,the
tendons at –140°,60° (0° corresponding to the dorsal side and to electrode E1). The relative short
duration of the simulated action potential is due to the generation of a single fiber potential, to
the small fiber depth, and to the specific selection of geometry and conductivity of the muscle
tissues
480
Paul Enck, Fernando Azpiroz, Roberto Merletti
34.3 First Results of the OASIS Technique
to Study Healthy, Continent Subjects
In the following we will present representative applications of the multichannel surface EMG detection system and processing techniques presented in the previous sections, applied to signals from the anal sphincter in healthy,continent subjects.
34.3.1 EMG Signal Amplitude
Surface EMG amplitude may be indicative of the exerted force (Bigland-Ritchie 1981);
thus it has been used for this purpose in many clinical studies.However, amplitude indicators (such as the average rectified or the root mean square value) are very sensitive
to factors other than the relative degree of muscle activation. The detection of signals
in many points over the muscle makes it possible to analyze the sensitivity of signal
features to electrode location.Figure 34.4 shows signals detected by the anal probe described above.The 16 signals obtained by the bipolar systems show significantly different amplitudes.As expected and demonstrated elsewhere (Roy et al. 1986), the signals
detected in proximity of the innervation zones or tendon endings have a lower amplitude than the others. Different electrode configurations provide signals with different
amplitude and spectral characteristics. As an example,Fig. 34.4 reports the signals detected by three bipolar systems with electrodes symmetrically placed. The figure also
shows how the orientation of the electrode may affect the signal amplitude.
The variability of amplitude measurements is significantly reduced if the proper
electrode location is selected specifically in each recording condition. A possible criterion is to estimate signal amplitude from bipolar arrangements located between the
innervation zone and the tendon endings. In this case, the maximum amplitude is obtained.A multichannel measurement is required to identify the optimal position.
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34.3.2 Noninvasive Assessment of Muscle Anatomical Properties
Multichannel EMG signals can obtain important information about anatomical properties of the muscle under study (Masuda et al. 1983, 1985;Roy et al.1986; Merletti et al.
1999b,2003; Roeleveld and Stegeman 2002;Rainoldi et al. 2004).According to the concepts described in ”The Project OASIS” (see also Fig. 34.2),visual analysis of the multichannel recordings estimates the length of the muscle fibers, the location of the innervation zones and the tendon regions. Figure 34.5 shows signals detected from the
EAS with the visual identification of the MU anatomical features (innervation zones
and fiber length). The MUs are innervated at different locations. The potentials propagate from the innervation zone,towards the fiber endings, with a specific CV.
34.3.3 Detection of Single Motor Unit Activities
The application of the decomposition technique to signals acquired from the sphincter muscle showed that it is possible to noninvasively identify MUs at low and high
contraction levels (Merletti et al. 2004). In many cases it was possible to detect the
Chapter 34 Functional Asymmetry of Pelvic Floor Innervation
Fig. 34.4A,B. Examples of surface EMG detection from the anal sphincter muscle using different
detection systems. A Schematic representation of the rectal probe (circles), shown from cable
side (see also Fig. 34.2A and corresponding caption). Multichannel EMG detection is obtained
with a series of differential amplifiers (쐃). Conventional bipolar EMG recording is instead obtained detecting a single signal as the difference between two opposite electrodes (쐇), from
which only amplitude-based information can be extracted (쐋). Effect of rotation of a bipolar
probe by a one-electrode step (22.5 degrees) in counter-clockwise direction. B Sample epoch,
100 ms long, of multichannel single differential EMG signals detected from external anal sphincter muscle during maximal contraction, using the probe shown in Fig. 34.2A, B1,and the detection method schematized in (쐏). C Sample epoch of conventional bipolar EMG signals,calculat-
ed from opposite electrodes on the same signal shown in B,in three different probe orientations:
electrodes aligned to left-right direction (BIP 0°, solid line), rotated by 22.5 degrees counterclockwise (BIP –22.5°), and clockwise (BIP +22.5°). In this specific case, a slight (–22.5 degrees)
rotation of the probe in counter-clockwise direction would not produce a significant effect,while
a rotation in the other direction would greatly affect both the amplitude (by roughly a twofold
factor) and shape of the potentials
481
same MUs at different contraction levels as well as the progressive and the recruitment
of new ones with increasing effort.
Figure 34.6 shows an example of decomposition of two signals recorded at 100%
and 50% MVC from an incontinent subject. At 100% MVC four MUs are detected. By
decreasing the contraction level to 50% MVC, two MUs are de-recruited. The same two
MUs are active at both contraction levels.The firing pattern of MU 2 is rather well reconstructed for both contraction levels.Since the symptomatic subject was not able to
maintain the 50% MVC contraction, the activity gradually decreased from t = 2 s and
stopped at t = 7 s. This behavior is well described in the de-recruitment pattern shown
in the right column diagrams of Fig. 34.6.
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Paul Enck, Fernando Azpiroz, Roberto Merletti
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Fig. 34.5a, b. Examples of multichannel EMG signals detected from the external anal sphincter
muscle of a female subject. Signals were acquired from 1-cm depth in the anal canal. a Relaxed
condition, b maximal voluntary contraction. Note the different vertical scales in a and b
34.3.4 Estimation of Muscle Fiber Conduction Velocity
Muscle fiber CV is an important physiological parameter since it reflects muscle fiber
type and contractile properties (Andreassen and Arendt-Nielsen 1987). Conduction
velocity can be estimated from multichannel surface EMG signals by computing the
delay of propagation between signals detected by systems placed along the fiber direction (Farina and Merletti 2004). In case of sphincter muscles, the specific geometry of
the muscle makes the estimation of CV critical. Indeed,the observed delay of propagation depends not only on the velocity of propagation, but also on the location of the
muscle fibers within the muscle (Fig. 34.7). Methods for estimating CV from these
muscles should be based on the concomitant estimation of the source depth and of the
propagation delay. Results from limb muscles indicate that this goal is feasible from
two-dimensional surface EMG recordings (Roeleveld et al. 1997,1998).
Chapter 34 Functional Asymmetry of Pelvic Floor Innervation
Fig. 34.6. Example of the decomposition of signals recorded during 10-s-long contractions at the
contraction levels 100% MVC (on the left) and 50% MVC (on the right). Superposition of the MU
action potentials belonging to each of the four MUs. Note that the same MUs (#2 and #4) are
identified at the two contraction levels and new MUs (#1 and #3) are recruited at 100% MVC.In
particular, MU #2 firing pattern is quite well reconstructed
483
Fig. 34.7a–c. Simulation of EMG signals generated by three fibers at different depths within the
muscle.The model is a two-layer circular cylinder (Farina et al. 2004b) with muscle and mucosa
(1 mm thick). The innervation zone is at 0°, the fiber ends at –100°, 80° (0° corresponding to the
dorsal side and to electrode E1). The fibers are 1 mm,2.5 mm and 4 mm deep within the muscle.
The set of signals reported in a, b and c are normalized with respect to the maximum amplitude
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Paul Enck, Fernando Azpiroz, Roberto Merletti
34.3.5 Differences in Sphincter Innervation
Between Men and Women
Fifty-two healthy subjects with no history of neurological or pelvic floor problems (37
nulliparous females and 15 males, 20–55 years old) were recruited in three centers
(Dept. of General Surgery,University Hospitals Tübingen,Germany; Dept. of Gynecology,Vivantes Klinikum Neukölln Berlin, Germany; Division of Digestive Disease,University Hospital Val d’Hebron, Barcelona, Spain) and investigated as described above
(Enck et al. 2004a).
The left column of Fig. 34.8 shows the histograms of the innervation zone (IZ) distributions at the three depths in the 15 male subjects. At all three levels the IZs are rather scattered, showing a large interindividual variability. If the three histograms are
added, the plot of Fig. 34.9 is obtained.An apparent predominance of right-left innervation with respect to ventral-dorsal innervation can be detected.
The right column of Fig. 34.8 shows the histograms of the IZ distributions at the
three depths in the 37 nulliparous female subjects. An innervation pattern similar to
that observed in males appears only at the 1 cm level.At the 2 cm level,the distribution
of IZs is more uniform around the circle and at the 3 cm level IZs are mostly in the dorsal and ventral regions with predominance on the ventral side.
A considerable amount of information can be extracted from the S-EMG of the
EAS. This study deals only with the location of the IZs detectable at 1-cm, 2-cm and
3-cm depth levels in the anal canal during maximal voluntary contractions. Except for
our recently reported work showing that it is possible to identify MUAPs of the EAS
and that there is large interindividual variability (Liu et al. 2002; Merletti et al. 2004),
no previous experience on this topic has been reported.Although IZ can be identified
from a single MUAP, at least ten MUAPs starting at the same location and showing bidirectional propagation were required in this study to identify such location as an IZ.
The MUAPs generated in this location could belong to different MUs. This criterion is
rather arbitrary and has the purpose of guaranteeing a positive identification of an IZ.
Relaxing it would increase the number of IZs by including those where fewer MUAPs
are generated,but would also increase the risk of erroneous detection due to artifacts;
this may be appropriate once more experience with this technique has been gathered.
This criterion therefore underestimates the total number of innervation zones observed in the EAS with the electrode array. Two additional limitations should be
considered: (a) the IZs of MUs that are far enough from the electrodes, so that their
MUAPs are near the noise level, are not detected, and (b) the MUAPs showing unidirectional propagation are not considered. For the reasons indicated above, these results should be considered preliminary.More solid evidence will come with the development of automatic procedures for detecting IZs and with a larger number of subjects.
These data may make it possible to close a missing link between different clinical
findings with respect to the pelvic floor.First, the incidence and prevalence of urinary
and fecal incontinence is known to be significantly higher in women than men, especially at higher age (Nelson 2004); this is usually attributed to specific risks for pelvic
floor trauma women undergo with pregnancy and childbirth.
The pathophysiology of incontinence recognized these gender-specific risk factors
(Snooks et al. 1986),as has the investigation of the role of asymmetry in incontinence
(Wietek et al. 2002). It is conceivable that the different probabilities of innervation of
the ventral region at different depths – as found in our study – may be a developmen-
Chapter 34 Functional Asymmetry of Pelvic Floor Innervation
485
Fig. 34.8a–f. Histograms of the number of innervation zones (IZ) found under each channel in 15
males (left column) and 37 females (right column) at the depth levels of 1 cm, 2 cm and 3 cm
486
Paul Enck, Fernando Azpiroz, Roberto Merletti
34
Fig. 34.9. Cumulative histogram of the number of innervation zones (IZ) found under each channel in 15 males and 37 females. The IZs at different depth levels are pooled together
tal consequence of higher risks for birth trauma in this region of the pelvic floor, and
is “aimed”at preventing or reducing the risk of incontinence in such case.
Second, pelvic anatomy has also shown significant differences between men and
women, especially since new imaging technologies (endoanal ultrasound, MRI) have
been applied to the study of pelvic floor anatomy (Schäfer et al. 1994; Eckardt et al.
2002).
Three anatomical concepts of the external anal sphincter and its innervation are
currently represented in the published literature: (a) a traditional concept claiming
that the EAS consists of three bundles of striated muscle fibers that are all three circular in nature,but with varying attachment, also varying between the genders. This concept has frequently been replicated in the anatomical textbooks and is the most widely used concept of sphincter anatomy (Cook and Mortensen 2002).Electrophysiologically, only two of the three parts of the EAS could be distinguished, a subcutaneous
part and a deep part (Podnar and Vodusek 1999). (b) A more recently developed con-
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