Modern Theories of Pelvic Floor Support

Current Urology Reports (2018) 19:9 https://doi.org/10.1007/s11934-018-0752-9

FEMALE UROLOGY (L COX, SECTION EDITOR)

Modern Theories of Pelvic Floor Support A Topical Review of Modern Studies on Structural and Functional Pelvic Floor Support from Medical Imaging, Computational Modeling, and Electromyographic Perspectives Yun Peng 1 & Brandi D. Miller 2 & Timothy B. Boone 2 & Yingchun Zhang 1

# Springer Science+Business Media, LLC, part of Springer Nature 2018

Abstract Purpose of Review Weakened pelvic floor support is believed to be the main cause of various pelvic floor disorders. Modern theories of pelvic floor support stress on the structural and functional integrity of multiple structures and their interplay to maintain normal pelvic floor functions. Connective tissues provide passive pelvic floor support while pelvic floor muscles provide active support through voluntary contraction. Advanced modern medical technologies allow us to comprehensively and thoroughly evaluate the interaction of supporting structures and assess both active and passive support functions. The pathophysiology of various pelvic floor disorders associated with pelvic floor weakness is now under scrutiny from the combination of (1) morphological, (2) dynamic (through computational modeling), and (3) neurophysiological perspectives. This topical review aims to update newly emerged studies assessing pelvic floor support function among these three categories. Recent Findings A literature search was performed with emphasis on (1) medical imaging studies that assess pelvic floor muscle architecture, (2) subject-specific computational modeling studies that address new topics such as modeling muscle contractions, and (3) pelvic floor neurophysiology studies that report novel devices or findings such as high-density surface electromyography techniques. We found that recent computational modeling studies are featured with more realistic soft tissue constitutive models (e.g., active muscle contraction) as well as an increasing interest in simulating surgical interventions (e.g., artificial sphincter). Diffusion tensor imaging provides a useful non-invasive tool to characterize pelvic floor muscles at the microstructural level, which can be potentially used to improve the accuracy of the simulation of muscle contraction. Studies using high-density surface electromyography anal and vaginal probes on large patient cohorts have been recently reported. Influences of vaginal delivery on the distribution of innervation zones of pelvic floor muscles are clarified, providing useful guidance for a better protection of women during delivery. Summary We are now in a period of transition to advanced diagnostic and predictive pelvic floor medicine. Our findings highlight the application of diffusion tensor imaging, computational models with consideration of active pelvic floor muscle contraction, high-density surface electromyography, and their potential integration, as tools to push the boundary of our knowledge in pelvic floor support and better shape current clinical practice. Keywords Pelvic floor support . Biomechanics . Finite element method . Electromyography

Introduction This article is part of the Topical Collection on Female Urology * Yingchun Zhang [email protected] 1

Department of Biomedical Engineering, Cullen College of Engineering, University of Houston, 360 HBS Building, 4811 Calhoun Rd., Houston, TX 77004, USA

2

Department of Urology, Houston Methodist Hospital, Houston, TX 77030, USA

Pelvic floor disorders include urinary incontinence (UI), pelvic organ prolapse (POP), fecal incontinence (FI), and other abnormalities of lower urinary and gastrointestinal tracts. A 2008 survey in the USA of 1961 non-pregnant women reported a 23.7% prevalence of at least one pelvic floor disorder, with 15.7% of women experiencing UI, 9.0% of women experiencing FI and 2.9% of women experiencing POP [1]. Similarly, a Turkish study that assessed 4002 non-pregnant women reported an overall prevalence of 67.5% of women

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experiencing at least one pelvic floor disorder [2]. By estimation, in the USA alone, from 2010 to 2050, the total number of women who will undergo surgery will increase by 47.2% for stress urinary incontinence (SUI) (from 210,700 to 310,050) and by 48.2% for POP (from 166,000 to 245,970) [3]. The high prevalence of pelvic floor disorders and the increasing number of surgical procedures is creating a profound economic burden on the healthcare system, which leads to an estimated direct annual cost of $412 million dollars in ambulatory care in the USA [4]. A better understanding of the pathophysiology of pelvic floor disorders is critical to the optimum utilization of medical resources. It has been well accepted that weakness in pelvic floor support is a key factor leading to pelvic floor disorders. Newer theories of pelvic floor disorders have been proposed [5••, 6••, 7–9], following the inception of two most popular and well-accepted theories: the Hammock Hypothesis by DeLancey [8] and the Integral Theory by Petros, Ulmsten [9]. Although these theories have some differences regarding the role played by each pelvic floor structure in specific disorders [10••], they all agree to some extent that normal pelvic floor functions are maintained by a well-coordinated interplay of multiple supporting structures including muscles, ligaments, tendons, and fascia residing in the female pelvis and that disturbance to their coordination would lead to functional disorders. It becomes clearer that the pelvic floor support is comprised of both passive and active components. The passive support function is mainly contributed by connective tissues (ligaments, fascia), while the active support function is mainly contributed by pelvic floor muscles, which can be contracted voluntarily to elevate the pelvic floor thereby counterbalancing increased abdominal pressure and maintaining the normal position of pelvic organs. Traditional pelvic floor assessments rely heavily on physical examination, which has many limitations, e.g., it focuses on surface anatomy instead of true structural abnormalities [11], tends to underestimate pelvic floor defects [12], produces results that are difficult to quantify [13•], and is subject to the examiners experience and interpretation. These limitations prevent a comprehensive and in-depth analysis of the aforementioned complex interplay of various key structures. Owing to the development of advanced medical techniques, modern research on pelvic floor support has been in a transition from single-mode empirical physical examination to a more comprehensive multimodal analysis utilizing highresolution imaging and advanced electrodiagnostic techniques. For example, high-resolution magnetic resonance (MR) imaging can provide detailed pelvic floor morphology for enhanced understanding of the passive pelvic floor support. Electrodiagnostic approaches, such as electromyography (EMG), provide the most suitable approach to assess the neurophysiologic aspect of pelvic floor muscle contractions. In addition, computational modeling, either passive or active,

Curr Urol Rep (2018) 19:9

offers a valuable tool to validate existing theories and also test new hypotheses that are difficult or impossible to investigate because of ethical or budgetary constraints. With these advanced approaches, we are gaining a better understanding of the multifactorial nature of pelvic floor support mechanisms. The pathophysiology of pelvic floor disorders is now under scrutiny utilizing the combination of anatomic, biomechanical, and neurophysiological instrumentation. This topical review aims to update newly emerged studies utilizing these approaches to study pelvic floor support.

Pelvic Floor Imaging Owing to the advance of modern medical imaging modalities, e.g., high-resolution MR imaging, evidence-based key insights have been discovered with regard to the relation between various pelvic floor disorders and morphological abnormalities in pelvic floor support structures. Earlier MR imaging studies of DeLancey and co-workers showed a higher incidence of major levator ani defects in women who had POP [14] or experienced vaginal delivery [15]. By combining MR imaging and threedimensional (3D) modeling, the same group reported aberrant displacement patterns of the posterior vaginal wall in women with posterior vaginal prolapse [16] and high excursion of the lateral anterior wall in women with anterior prolapse [17]. A more recent study compared the mid-sagittal MR imaging features among 30 controls, 30 anterior prolapse, and 30 posterior prolapse women and revealed a significantly larger levator area, a greater protrusion area and longer levator hiatus length in the two prolapse groups compared to controls during Valsalva [18•]. Pontbriand-Drolet et al. compared the morphology of pelvic floor musculature, bladder neck, and urethral sphincter position among mixed urinary incontinence, stress UI, and continent women. They found a lower pelvic floor muscle resting position and lower urethrovesical junction height in women with mixed urinary incontinence, and a higher likelihood of bladder neck funneling and larger posterior urethrovesical angle at rest in stress UI women [19•]. In addition to structural MR imaging, dynamic MR imaging offers useful information concerning the four compartments of the pelvis and allows a direct visualization of the pelvis during functional tasks, e.g., defecography, and has been frequently used in studies of anorectal dysfunctions [20, 21]. However, its correlation with symptoms (e.g., degree of prolapse) appears low [21]. The utility in the diagnosis and surgical management of pelvic floor disorders remain to be further explored. There has been an increasing interest in the utility of diffusion tensor imaging (DTI) in characterizing fiber orientation of the pelvic floor musculature [22•]. Muscle tissues are known to exhibit fiber-direction dependent anisotropic behavior (as opposed to isotopic behavior). By capturing the principle directions of water diffusion, DTI provides indirect


information about the tissue architecture and therefore enables a non-invasive characterization of muscle fibers at the microstructural level. In a feasibility study by Zijta et al., the authors successfully captured multiple pelvic floor muscular structures in five young nulliparous females [23]. Another study by Betschart et al. found statistically different muscle fascicle direction among three subdivisions of the levator ani muscle in 14 healthy women [24••]. DTI has also been successfully applied in characterizing the neurography of pelvic floor musculature [25], which is intimately relevant to the contraction of pelvic floor muscles and therefore active pelvic floor support. However, current DTI studies in pelvic floor research remain largely in a pioneering phase. There is a lack of case-control studies to further investigate the neuromuscular origins of disrupted pelvic floor support, despite its successful application in other skeletal muscle injuries [26]. Future studies are therefore required to reveal possible links between neuromuscular abnormalities at the microstructural level and pelvic floor disorders. It is worth noting that, owing to the capability in capturing muscle fiber orientation, DTI has recently been utilized in computational modeling studies to provide a more realistic biomechanical behavior of pelvic floor muscles [27•]. This aspect is further detailed in the next section.

Computational Modeling of Pelvic Floor Support Computational modeling using finite element (FE) method provide approximated solutions to complex physical biomechanical problems under prescribed assumptions [28••]. It offers substantial convenience not only in studying the mechanism of asymptomatic pelvic floor support functions, but also in simulating various conditions with impairment that are otherwise challenging or impossible to investigate because of ethical or budgetary constraints. The application of the FE method to pelvic floor studies only started emerging in the early last decade [29–32]. The current decade has witnessed a burgeoning growth of both the number and the quality of pelvic floor FE studies. Modern models are featured with more realistic material properties including visco-hyperelasticity [33–35], a more complete inclusion of critical anatomical structures [36••, 37••, 38], better biphasic modeling of the fluid-structure interactions [31, 39•, 40•], attention to more specific risk factors or causes of pelvic floor disorders such as prolonged second stage of labor [34], ligamentous injury [36••], or episiotomy [41••, 42], and increasing recognition of previously under-reported groups like incontinent athletes [43, 44]. These models provide the chance to appraise existing theories. Using a biomechanical model of the anterior vaginal wall and its support system (pubovisceral muscle, cardinal and/or uterosacral ligaments), Chen et al.

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demonstrated that the magnitude of the anterior vaginal wall prolapse was a combined function of both pubovisceral muscle and apical impairment. The genital hiatus opened and a prolapse developed, once a certain degree of pubovisceral impairment was reached. The size of prolapse further increased with an increasing degree of apical impairment [45]. Larger cystoceles formed in the presence of combined impairment of levator and apical support, in contrast to single impairment condition [29]. In the continued work by Luo et al. [37••], a multi-compartmental 3D model was developed to evaluate the occurrence of rectocele (Fig. 1a). The authors found the dependence of rectocele and cystocele on the presence of combined impairments in the anterior, posterior, levator, and/or apical support established an interaction between the anterior and posterior compartments. In the work by Brandão et al. [36••], a 3D model was created from a young healthy female to investigate the effect of ligamentous impairment on urethral mobility during Valsalva maneuver (Fig. 1b). They observed an increased alpha-angle from rest to 124.28° and a bladder neck displacement of 12 mm under maximal simulated impairment. In another study by Peng et al. [38••], a 3D model that incorporated 44 anatomical structures in the female pelvis was created (Fig. 1c). The influence of weakness of the pelvic muscles and anterior vaginal on the urethral support function was assessed. Urethral hypermobility was observed when all three subdivisions of the levator ani group were weakened. It was further demonstrated that the weakening effect was greater under combined impairment condition (levator ani group and anterior vaginal wall) than the sum of weakening effects caused by weakening each component individually, suggesting an interaction between para-urethral support structures. Owing to the findings revealed by computational models, we have now firmly recognized that a wellorchestrated interaction among pelvic floor structures is crucial to maintaining the normal pelvic floor support function. Going forward, it is expected that computer models could facilitate the formation and validation of new hypotheses in territories that are more challenging and/or little known. One example would be the application of computational models in the evaluation and optimization of treatment solutions [46•]. Concurrent with efforts to evaluate the performance of pelvic prosthetics under in vitro conditions or animal models [47•, 48••, 49••, 50], exciting treatmentoriented computational models simulating in vivo conditions are emerging. By simulating the surgical insertion of a mini-sling at various locations along the posterior urethral wall, Peng et al. confirmed that the mid-distal location offered the best restoration of native urethral excursion under increased intra-abdominal pressure and minimized urethral retention force [51•]. In an attempt to evaluate the effect of mesh stiffness on the outcome of surgical correction of urethral hypermobility, Brandão et al. found that both lower and higher stiffness allowed the correction of normal

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a

b

c Fig. 1 Illustration of computational model studies of a Luo et al. [37••], b Brandão et al. [36••], and c Peng et al. [38••] that showed (upper panel) mid-sagittal plane deformation under loading condition (e.g., Valsalva maneuver) from simulation results and (lower panel) comparison with mid-sagittal plane MR imaging

urethral position but raised concerns regarding the increased sling force and possibility of tissue erosion associated with a mesh higher stiffness [52]. Male urinary incontinence, especially post-prostatectomy stress urinary incontinence, has been previously overlooked in computational modeling [53]. In the recent work by Natali et al. [54••], a 3D male urethral model was developed to evaluate the effect of imposed constant or parabolic cuff pressure on urethral occlusion in the context of artificial urethral sphincter for the treatment of male stress incontinence. Urethral occlusion was observed in the presence of a constant loading along the overall length of the cuff,


while marginal opening was observed in the presence of parabolic cuff conformation. Another example would be the attempt to model pelvic floor muscle contractions. Undoubtedly, muscle contraction plays a critical role in supporting pelvic organs, but there has been a paucity of relevant modeling studies investigating its role in pelvic organ support. Recent work by Brandão et al. adopted an established muscle contraction model by adding an anisotropic fiber-dependent active component to an isotopic hyperelastic constitutive model of muscle tissues and applied it to the simulation of pelvic floor muscle contraction [55••]. In this initial attempt, the fiber orientation was determined as the maximal principal stress lines when the pelvic floor muscle was subjected to a trial uniform pressure. In a follow up study, the authors evaluated the consistency of fiber orientations obtained from the initial attempt and from DTI and reported non-significant difference in the angles obtained from these two modalities [27•]. Simulation results of active contraction using DTI muscle fiber model had not been reported by the time of this review. Their model currently represents the most advanced active contraction model and potentially enables the exploration of pathophysiology of pelvic floor disorders associated with impaired muscle contraction. For example, a more obtuse anorectal angle has been associated with fecal incontinence and is directly influenced by the contraction of the puborectalis muscle [56]. Active contraction models would potentially allow better understanding of the etiology of fecal incontinence and provide a useful adjunct to the evaluation of puborectal sling treatment [57], which has only been recently approved by the Food and Drug Administration of the USA since February 2016. Despite the increasing popularity of computational models in pelvic floor studies, the simulation results should always be interpreted in light of the modeling assumptions and inputs [28••]. Verification and validation of existing pelvic models are often simple, such as comparison of simulation outcome with dynamic MR images in single anatomical plane [29, 36••, 38••] (Fig. 1) The bio-fidelity of computational models should always be established before they can be further applied to address clinical questions.

Pelvic Muscle Function Assessment with High-Density Surface EMG Techniques Pelvic floor muscle contraction is crucial to providing strong pelvic floor support and maintaining normal pelvic floor function. A well-coordinated contraction of pelvic floor muscles relies on the integrity of the neuromuscular pathway, which allows uninterrupted descending activation signals from the nervous system to alpha motor neurons driving axonal input to the neuromuscular junction. A motor neuron and the muscle fibers it innervates constitute the smallest functional unit of the muscle, namely the motor unit (MU). The pool of


neuromuscular junctions of fibers belonging to the same MU is distributed in a territory termed innervation zone (IZ). Electromyography is a technique commonly used in neurophysiologic diagnosis. By recording the bioelectrical activities associated with action potentials during muscle fiber activation, EMG provides useful information regarding many aspects of the neurophysiology of the neuromuscular system. Surface EMG signals obtained with intra-vaginal or intrarectal probes represent the gross spatial superposition of motor unit action potentials from multiple MUs at the recording electrode. Therefore, most clinical studies directly interpret the signal amplitude (e.g., averaged rectified value or root mean square of EMG signals over a short period of time) as the strength of pelvic floor muscle contractions. A moderate to high test-retest reliability in pelvic floor muscle EMG measurement has been previously reported in healthy subjects [58–60] and patients with pelvic floor muscle weakness [60]. A strong correlation of EMG amplitude to digital palpation in assessing pelvic floor strength has also been reported [61]. Using an intra-vaginal EMG probe, Botelho et al. compared the impact of three distinct modes of delivery (mediolateral episiotomy, cesarean section, and emergency cesarean section) on pelvic floor muscle in 75 primiparous women and identified a significant reduction in maximum contraction of the pelvic floor after mediolateral episiotomy [62]. EMG measurement at maximal voluntary contractions is found to be significantly higher in non-pregnant women than pregnant women [63]. In studies of neurological anorectal dysfunction, intramuscular needle EMG remains the standard diagnostic tool [64]. However, needle EMG is very invasive and undesired by patients. Surface EMG is often preferred. In a series of studies, Stafford and co-workers reported a catheter-based striated urethral sphincter EMG probe, which included four wire electrodes at equally placed intervals around a 6Fr 30 mm catheter with pairs separated by the two urine ports, allowing two differential recordings. Their pilot study indicated high data quality and detection of MU action potential (MUAP) with gentle contractions [65]. In a continued study on five healthy male subjects, the authors measured intra-abdominal pressure and sphincter EMG during dynamic activities and reported a linear relation between IAP amplitude and sphincter activity. An EMG onset preceding IAP increase was also observed during stepping [66]. In the most recent work, the authors identified strong dependence of activation patterns of several pelvic floor muscles on the type of verbal instructions given and therefore suggested the necessity to give instructions selectively during pelvic floor muscle training for optimized outcome [67••]. The main limitation of EMG probes containing only one single or a small number of EMG electrodes is the lack of spatiotemporal information obtained from the muscle of interest. As surface EMG signal recording is the superposition of

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multiple MUs activated at different time instances, the neuromuscular function of MUs and their alterations may not always be fully explored by single channel recording. Recent advances in non-invasive high-density (HD) surface EMG recording and signal processing techniques have brought forth a promising tool for monitoring the neuromuscular functions of pelvic floor muscles [68]. High-density surface EMG can provide unique information that is not available using existing techniques [69]. In the pioneering work conducted by Merletti and co-workers in 2004 [69, 70], the authors successfully captured the propagation of MUAP of external anal sphincter (EAS) at different depths using an intra-rectal EMG probe with 16-channel circumferential electrodes (Fig. 2a, b) and derived the location of the innervation zones, where the propagation of MUAP is started to yield a contraction. Since asymmetric innervation patterns have been suggested as a possible cause of fecal incontinence [71], using this probe, Merletti and and coworkers conducted a series of studies to investigate the innervation pattern of the EAS and risk factors for fecal incontinence associated with childbirth [72••, 73–78]. In one study, EMG signals from 478 pregnant women were acquired with the IZ position along the sphincter circumference extracted for each identified MU [73••]. On average, 9 and 7 MUs were identified for rest and maximal voluntary contraction, respectively. The authors identified two distinct types of MUs, with 43% of total MUs classified as unidirectional MU (IZ at one end of MU) and the remaining bidirectional (IZ in the middle of MU length). Distribution of IZ also differed between these two types of MUs, with IZs of unidirectional MUs concentrated in the dorsal portion of the sphincter, while IZs of bidirectional MUs distributed more symmetrically between the left-right portions of the EAS (Fig. 2c). Potentially, this kind of information might be used to plan episiotomies and minimize risks of EAS denervation. In another multi-center study, pre-partum EMG measurements were performed on 511 women and post-partum EMG measurements were performed on 331 who returned for the second test [72••]. The number of IZs before and after delivery was compared between four delivery modes including cesarean section, vaginal delivery with no evident damage, spontaneous laceration, and episiotomy. No significant change was observed in women who had cesarean section, spontaneous laceration, or lack of evident damage, while significant reduction of IZ was observed in 82 women who received right mediolateral episiotomy. New knowledge obtained from these studies has the great potential to better shape our current clinical practice. For example, despite the fact that episiotomies are rarely performed in the USA, it remains a prevalent surgical maneuver in many other countries. A recent review article in 2015 reported that current episiotomy has significant practice variance in

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Fig. 2 a Merletti’s 16-channel anal EMG probe, schematic representation of anal probe position with respect to the external anal sphincter muscle, and illustration of two identified MUs with length. b Sample epoch of multichannel single differential EMG signals. c Cescon’s study of 478 pregnant women: distribution of the IZs of the EAS for unidirectional and bidirectional MUs during rest and maximal voluntary contractions. The size of the circles represents the range of MUAP amplitude. V-ventral, Ddorsal, R-right, L-left.

terms of technique and practice guideline [79]. The information obtained from intra-rectal probe EMG studies could enable obstetricians to take into account


predelivery analysis of innervation and perform the episiotomy, when deemed necessary, on the side of minimal or absent innervation of the EAS. [80]. As a result, the integrity of the EAS would be maximally preserved and the occurrence of postpartum FI could be reduced. Other groups have also reported novel multiple electrode EMG probes to study the innervation of different pelvic floor muscles and evaluate pelvic support function (Table 1) [81••, 82••, 83•]. Another probe with four circumferential electrodes at six different depths (4 by 6) was reported by Voorham-van der Zalm et al. [81], who measured the intra-vaginal and intrarectal EMG amplitudes (root mean square) of 229 healthy subjects with no pelvic floor disorders at rest, maximal contraction, endurance, cough, and Valsalva. Significant differences were found in EMG amplitude between genders and based on parity and menopausal status. High-density intravaginal (8 by 8) and intra-rectal (8 by 8) probes were reported by Peng et al. [83•] to measure the EMG signal of pelvic floor muscles and EAS from ten healthy female subjects. In addition, the authors also implemented an EMG decomposition algorithm to detect MUs (5.1 ± 3.0 MUs from intra-vaginal probe and 9.5 ± 2.4 MUs from intra-rectal probe). Heesakkers et al. reported a novel catheter-based minimally invasive circumferential sphincter surface EMG probe (three arrays, 12 electrodes each array) [82••]. EMG measurement was taken on 44 women with SUI or intrinsic sphincter deficiency. The authors identified the EMG measurement in the ventral quadrant during maximal contraction as a significant indicator for intrinsic sphincter deficiency. Multi-electrode EMG probes provide a great advantage in assessing MU behavior. Information obtained by recent highdensity surface EMG studies, in adjunct to other clinical diagnostic modulus, has greatly advanced our understanding of the underlying neurophysiology and its relation to active pelvic floor support. However, a major obstacle preventing the broad extension of these HD-EMG based probes is the dependence on advanced mathematical algorithms to isolate single MUs from the surface recording interferential pattern [77, 84–87], making the application of HD EMG to clinical practice difficult. This limitation has been partially solved as some of the algorithms have become commercially available. Another obstacle challenging all EMG measurements in the pelvic floor region is crosstalk, defined as EMG recording originating from neighboring muscles, rather than the muscle of interest. A recent review in 2017 of 49 studies investigating the phenomenon of crosstalk in pelvic floor muscle EMG signals identified intra-vaginal probe, electrode configuration, electrode size, and location as the main influencing factors [88•]. Future studies are expected to further elucidate this phenomenon and develop practical coping strategies. Additionally, the Authors of this review believe that EMG measurement could also provide useful inputs to computational modeling approaches, by allowing a more realistic

Curr Urol Rep (2018) 19:9 Table 1

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Summary of contemporary high-density EMG probes for pelvic floor muscles

Probe Dimension

Electrode Configuration

Electrode Size (mm)

Application

Diameter 14mm

1 × 16

L5 × Ø0.8

Anal

Diameter 14mm Inter-array Distance 15mm

3 × 16

L10 × Ø1

Anal

Appearance of probe

References

Multichannel surface EMG probe

Merletti et al. [69]

Multichannel surface EMG probe Enck et al. [75]

The Multiple Array Probe Leiden (MAPLe) Diameter 15mm Inter-array Distance 10mm Diameter 22.7mm Inter-array Distance 8.8mm Diameter 14.4mm Inter-array Distance 8mm 16 Fr catheter Inter-array Distance 1.75

6×4

NA

Vaginal or rectal

8×8

Ø4.0

Vaginal

Voorham van der Zalm et al. [81]

High-Density Surface EMG Probes Peng et al. [83]

High-Density Surface EMG Probes 8×8

L4.0 × W2.4

Rectal

3×12

L2.0 × Ø1.0

Urethral

Peng et al. [83]

Circumferential urinary sphincter surface EMG probe

definition of the contraction of pelvic floor muscles. Such an “active” model, upon validation, could potentially enable new areas to be explored, such as the development of fecal incontinence associated with impaired motor control of external anal sphincter and levator ani muscle.

Heesakkers et al. [82]

References Papers of particular interest, published recently, have been highlighted as: • Of importance •• Of major importance 1.

Conclusions In this review, we report on literature published over the past few years that provided new insight into pelvic floor support function through imaging, computational modeling, and advanced surface EMG methodology. Advanced imaging or high-density EMG techniques have proven useful for an improved understanding of the underlying principles of pelvic floor support, while computational models have provided useful tools for testing hypotheses that are difficult to accomplish using other modalities. Compliance with Ethical Standards

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5.

Conflict of Interest Yun Peng, Brandi D. Miller, Timothy B. Boone, and Yingchun Zhang each declare that they have no conflicts of interest.

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Human and Animal Rights and Informed Consent This article does not contain any studies with human or animal subjects performed by any of the authors.

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Nygaard I, Barber MD, Burgio KL, Kenton K, Meikle S, Schaffer J, et al. Prevalence of symptomatic pelvic floor disorders in US women. JAMA. 2008;300(11):1311–6. https://doi.org/10.1001/jama. 300.11.1311. Kepenekci I, Keskinkilic B, Akinsu F, Cakir P, Elhan AH, Erkek AB, et al. Prevalence of pelvic floor disorders in the female population and the impact of age, mode of delivery, and parity. Dis Colon Rectum. 2011;54(1):85–94. https://doi.org/10.1007/DCR. 0b013e3181fd2356. Wu JM, Kawasaki A, Hundley AF, Dieter AA, Myers ER, Sung VW. Predicting the number of women who will undergo incontinence and prolapse surgery, 2010 to 2050. Am J Obstet Gynecol. 2011;205(3):230. e1–5. Sung VW, Washington B, Raker CA. Costs of ambulatory care related to female pelvic floor disorders in the United States. Am J Obstet Gynecol. 2010;202(5):483. e1–4. Bergström BS. Urethral hanging theory. Neurourol Urodyn. 2017;36(3):826–7. https://doi.org/10.1002/nau.23018. Hoyte L, Damaser M. Biomechanics of the female pelvic floor. Academic Press; 2016. This book provides an overview of pelvic floor anatomy, pathology, basic concepts of pelvic floor biomechanics and a review of previous work. Tansatit T, Apinuntrum P, Phetudom T, Phanchart P. New insights into the pelvic organ support framework. Eur J Obstet Gynecol

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Page 8 of 10

Reprod Biol. 2013;166(2):221–5. https://doi.org/10.1016/j.ejogrb. 2012.10.038. 8. DeLancey JO. Structural support of the urethra as it relates to stress urinary incontinence: the hammock hypothesis. Am J Obstet Gynecol. 1994;170(5):1713–23. https://doi.org/10.1016/S00029378(12)91840-2. 9. Petros PEP, Ulmsten UI. An integral theory of female urinary incontinence. Acta Obstet Gynecol Scand. 1990;69(S153):7–31. https://doi.org/10.1111/j.1600-0412.1990.tb08027.x. 10.•• Lamblin G, Delorme E, Cosson M, Rubod C. Cystocele and functional anatomy of the pelvic floor: review and update of the various theories. Int Urogynecol J. 2016;27(9):1297–305. This recent review article provides a thorough summary of key anatomical structures and evaluated their roles in DeLancey’s and Petro’s theories. 11. Dietz HP. Pelvic floor ultrasound: a review. Clin Obstet Gynecol. 2017;60(1):58–81. https://doi.org/10.1097/grf. 0000000000000264. 12. Kearney R, Miller JM, DeLancey JO. Interrater reliability and physical examination of the pubovisceral portion of the levator ani muscle, validity comparisons using MR imaging. Neurourol Urodyn. 2006;25(1):50–4. https://doi.org/10.1002/nau.20181. 13.• Ahmad AN, Hainsworth A, Williams AB, Schizas AM. A review of functional pelvic floor imaging modalities and their effectiveness. Clin imaging. 2015;39(4):559–65. This review compares the utility of three pelvic floor imaging modalities: ultrasound imaging, magnetic resonance imaging, and dynamic defecating proctography. 14. DeLancey JO, Morgan DM, Fenner DE, Kearney R, Guire K, Miller JM, et al. Comparison of levator ani muscle defects and function in women with and without pelvic organ prolapse. Obstet Gynecol. 2007;109(2, Part 1):295–302. https://doi.org/10. 1097/01.AOG.0000250901.57095.ba. 15. JO DL, Kearney R, Chou Q, Speights S, Binno S. The appearance of levator ani muscle abnormalities in magnetic resonance images after vaginal delivery. Obstet Gynecol. 2003;101(1):46. 16. Luo J, Larson KA, Fenner DE, Ashton-Miller JA, DeLancey JO. Posterior vaginal prolapse shape and position changes at maximal Valsalva seen in 3-D MRI-based models. Int Urogynecol J. 2012;23(9):1301–6. https://doi.org/10.1007/s00192-012-1760-9. 17. Larson KA, Luo J, Guire KE, Chen L, Ashton-Miller JA, DeLancey JO. 3D analysis of cystoceles using magnetic resonance imaging assessing midline, paravaginal, and apical defects. Int Urogynecol J. 2012;23(3):285–93. https://doi.org/10.1007/s00192-011-1586-x. 18.• Sammarco AG, Nandikanti L, Kobernik EK, Xie B, Jankowski A, Swenson CW et al. Interactions among pelvic organ protrusion, levator ani descent, and hiatal enlargement in women with and without prolapse. Am J Obstet Gynecol. 2017. This MR imaging study compares the dynamic pelvic floor morphology between women with and without prolapse and identifies key features that are associated with prolapse. 19.• Pontbriand-Drolet S, Tang A, Madill SJ, Tannenbaum C, Lemieux MC, Corcos J, et al. Differences in pelvic floor morphology between continent, stress urinary incontinent, and mixed urinary incontinent elderly women: an MRI study. Neurourol Urodyn. 2016;35(4):515–21. This article highlighted the difference of morphological defects at rest between women with SUI and MUI symptoms and calls for special consideration during surgical intervention. 20. Alapati S, Jambhekar K, editors. Dynamic magnetic resonance imaging of the pelvic floor. Seminars in Ultrasound, CT and MRI; 2017: Elsevier. 21. Pizzoferrato A-C, Timoh KN, Fritel X, Zareski E, Bader G, Fauconnier A. Dynamic magnetic resonance imaging and pelvic floor disorders: how and when? Eur J Obstet Gynecol Reprod

Curr Urol Rep (2018) 19:9 Biol. 2014;181:259–66. https://doi.org/10.1016/j.ejogrb.2014.07. 025. 22.• Zijta FM, Froeling M, Nederveen AJ, Stoker J. Diffusion tensor imaging and fiber tractography for the visualization of the female pelvic floor. Clin Anat. 2013;26(1):110–4. This review discusses the current state of diffusion tensor imaging and tractography in the evalatuion of female pelvic floor. 23. Zijta F, Froeling M, Van Der Paardt M, Lakeman M, Bipat S, van Swijndregt AM, et al. Feasibility of diffusion tensor imaging (DTI) with fibre tractography of the normal female pelvic floor. Eur Radiol. 2011;21(6):1243–9. https://doi.org/10.1007/s00330-0102044-8. 24.•• Betschart C, Kim J, Miller JM, Ashton-Miller JA, DeLancey JO. Comparison of muscle fiber directions between different levator ani muscle subdivisions: in vivo MRI measurements in women. Int Urogynecol J. 2014;25(9):1263–8. In this article, the normal pudendal nerve anatomy and its variations are discussed and abnormal appearances of the pudendal nerve and its branches are illustrated and highlighted. 25. Wadhwa V, Hamid AS, Kumar Y, Scott KM, Chhabra A. Pudendal nerve and branch neuropathy: magnetic resonance neurography evaluation. Acta Radiol. 2017;58(6):726–33. https://doi.org/10. 1177/0284185116668213. 26. Zaraiskaya T, Kumbhare D, Noseworthy MD. Diffusion tensor imaging in evaluation of human skeletal muscle injury. J Magn Reson Imaging. 2006;24(2):402–8. https://doi.org/10.1002/jmri.20651. 27.• Brandão S, Parente M, Silva E, Da Roza T, Mascarenhas T, Leitão J, et al. Pubovisceralis muscle fiber architecture determination: comparison between biomechanical modeling and diffusion tensor imaging. Ann Biomed Eng. 2017;45(5):1255–65. This article compares the pelvic floor muscle fiber directions between biomechanical modeling and diffusion tensor imaging methods, providing ground to the application of muscle fiber orientation in computer models. 28.•• Easley DC, Abramowitch SD, Moalli PA. Female pelvic floor biomechanics: bridging the gap. Curr Opin Urol. 2017;27(3):262–7. This topical review highlights recent contributions in mechanical testing and computational modeling to understand the pelvic floor biomechanics. 29. Chen L, Ashton-Miller JA, DeLancey JO. A 3D finite element model of anterior vaginal wall support to evaluate mechanisms underlying cystocele formation. J Biomech. 2009;42(10):1371–7. https://doi.org/10.1016/j.jbiomech.2009.04.043. 30. Noakes KF, Bissett IP, Pullan AJ, Cheng LK. Anatomically realistic three-dimensional meshes of the pelvic floor & anal canal for finite element analysis. Ann Biomed Eng. 2008;36(6):1060–71. https:// doi.org/10.1007/s10439-008-9471-6. 31. Zhang Y, Kim S, Erdman AG, Roberts KP, Timm GW. Feasibility of using a computer modeling approach to study SUI induced by landing a jump. Ann Biomed Eng. 2009;37(7):1425–33. https://doi. org/10.1007/s10439-009-9705-2. 32. Martins J, Pato M, Pires E, Jorge RN, Parente M, Mascarenhas T. Finite element studies of the deformation of the pelvic floor. Ann N Y Acad Sci. 2007;1101(1):316–34. https://doi.org/10.1196/annals. 1389.019. 33. Chen Z-W, Joli P, Feng Z-Q, Rahim M, Pirró N, Bellemare M-E. Female patient-specific finite element modeling of pelvic organ prolapse (POP). J Biomech. 2015;48(2):238–45. https://doi.org/ 10.1016/j.jbiomech.2014.11.039. 34. Jing D, Ashton-Miller JA, DeLancey JO. A subject-specific anisotropic visco-hyperelastic finite element model of female pelvic floor stress and strain during the second stage of labor. J Biomech. 2012;45(3):455–60. https://doi.org/10.1016/j.jbiomech.2011.12. 002. 35. Vila Pouca M, Ferreira J, Oliveira D, Parente M, Natal Jorge R. Viscous effects in pelvic floor muscles during childbirth: a

Curr Urol Rep (2018) 19:9 numerical study. Int J Numer Methods in Biomed Eng. 2017. doi: https://doi.org/10.1002/cnm.2927. 36.•• Brandão S, Parente M, Mascarenhas T, da Silva ARG, Ramos I, Jorge RN. Biomechanical study on the bladder neck and urethral positions: simulation of impairment of the pelvic ligaments. J Biomech. 2015;48(2):217–23. This finite element modeling study assesses the bladder neck position under different degrees of pelvic floor ligament impairment. 37.•• Luo J, Chen L, Fenner DE, Ashton-Miller JA, DeLancey JO. A multi-compartment 3-D finite element model of rectocele and its interaction with cystocele. J Biomech. 2015;48(9):1580–6. This finite element modeling study evaluated the impact of particular impairments of the anterior and posterior pelvic compartment structural support systems on the development of cystocele and rectocele. 38.•• Peng Y, Khavari R, Nakib NA, Boone TB, Zhang Y. Assessment of urethral support using MRI-derived computational modeling of the female pelvis. Int Urogynecol J. 2016;27(2):205–12. This finite element modeling study evaluates the individual contributions of muscle groups in providing urethral support during Valsalva maneuver. The model contains a most complete pelvic floor anatomy. 39. Spirka T, Kenton K, Brubaker L, Damaser MS. Effect of material properties on predicted vesical pressure during a cough in a simplified computational model of the bladder and urethra. Ann Biomed Eng. 2013;41(1):185–94. https://doi.org/10.1007/s10439-0120637-x. 40.• Peng Y, Neshatian L, Khavari R, Boone T, Zhang Y. PD01–12 a fluid-structure interaction simulation of fecal incontinence. J Urol. 2016;195(4):e50. This study introduces a realistic fluid-structure interaction model, namely the smoothed particle hydrodynamics (SPH), to simulate the motion of the stool to understand the interaction between sphincters and stools. 41.•• Oliveira DA, Parente MP, Calvo B, Mascarenhas T, Jorge RMN. A biomechanical analysis on the impact of episiotomy during childbirth. Biomech Model Mechanobiol. 2016;15(6):1523–34. This article explored how the episiotomy procedure impacts the pelvic floor during simulated childbirth using a finite element model. 42. Oliveira DA, Parente MP, Calvo B, Mascarenhas T, Jorge RMN. The management of episiotomy technique and its effect on pelvic floor muscles during a malposition childbirth. Comput Methods Biomech Biomed Eng. 2017;20(11):1249–59. https://doi.org/10. 1080/10255842.2017.1349762. 43. Dias N, Peng Y, Khavari R, Nakib NA, Sweet RM, Timm GW, et al. Pelvic floor dynamics during high-impact athletic activities: a computational modeling study. Clin Biomech. 2017;41:20–7. https:// doi.org/10.1016/j.clinbiomech.2016.11.003. 44. Da Roza T, Brandão S, Oliveira D, Mascarenhas T, Parente M, Duarte JA, et al. Football practice and urinary incontinence: relation between morphology, function and biomechanics. J Biomech. 2015;48(9):1587–92. https://doi.org/10.1016/j.jbiomech.2015.03. 013. 45. Chen L, Ashton-Miller JA, Hsu Y, DeLancey J. Interaction among apical support, levator ani impairment, and anterior vaginal wall prolapse. Obstet Gynecol. 2006;108(2):324–32. https://doi.org/10. 1097/01.AOG.0000227786.69257.a8. 46.• Todros S, Pavan P, Natali A. Biomechanical properties of synthetic surgical meshes for pelvic prolapse repair. J Mech Behav Biomed Mater. 2016;55:271–85. This review provides a comprehensive summary of mechanical properties of current synthetic surgical meshes for prolapse and relevant computational modelling studies. 47.• Barone WR, Moalli PA, Abramowitch SD. Textile properties of synthetic prolapse mesh in response to uniaxial loading. Am J Obstet Gynecol. 2016;215(3):326. e1–9. This study investigates the effect of tensile loading and pore orientation on mesh

Page 9 of 10 9 porosity and pore dimension and provides useful guidance towards a better mesh design and improved surgical techniques. 48.•• Liang R, Knight K, Abramowitch S, Moalli PA. Exploring the basic science of prolapse meshes. Curr Opin Obstet Gynecol. 2016;28(5): 413. This review article provides an update of current understanding of the impact of mesh texile properties and mechanical behavior on vaginal structure, function and immune responses. 49.•• Jallah Z, Liang R, Feola A, Barone W, Palcsey S, Abramowitch S, et al. The impact of prolapse mesh on vaginal smooth muscle structure and function. BJOG Int J Obstet Gynaecol. 2016;123(7):1076– 85. This animal study (Macaques) investigates the impact of prolapse mesh properties on the strucutre and function of vaginal smooth muscles. 50. Barone WR, Amini R, Maiti S, Moalli PA, Abramowitch SD. The impact of boundary conditions on surface curvature of polypropylene mesh in response to uniaxial loading. J Biomech. 2015;48(9): 1566–74. https://doi.org/10.1016/j.jbiomech.2015.02.061. 51.• Peng Y, Khavari R, Nakib NA, Stewart JN, Boone TB, Zhang Y. The single-incision sling to treat female stress urinary incontinence: a dynamic computational study of outcomes and risk factors. J Biomech Eng. 2015;137(9):091007. This is the first finite element modeling study to implement a sub-urethral sling in the pelvic floor region. Optimal sling implantation location was recommended based on simulation results that minimized the retention force and maximized the recovery of natural urethral mobility. 52. Brandão S, Parente M, Da Roza TH, Silva E, Ramos IM, Mascarenhas T, et al. On the stiffness of the mesh and urethral mobility: a finite element analysis. J Biomech Eng. 2017;139(8): 081002. https://doi.org/10.1115/1.4036606. 53. Dias N, Peng Y, Miles B, Khavari R, MacDonnell V, Boone T, et al. PD49-07 urethral mobility study with a computational model of the male pelvis. J Urol. 2016;195((4):e1182-e3. 54.•• Natali AN, Carniel EL, Fontanella CG, Todros S, De Benedictis GM, Cerruto MA, et al. Urethral lumen occlusion by artificial sphincteric devices: a computational biomechanics approach. Biomech Model Mechanobiol. 2017:1–8. This finite element modeling study pioneers the computational modeling of artificial sphincter devices. 55.•• Brandão FSQDS, Parente MPL, Rocha PAGG, Saraiva MTDQECDM, Ramos IMAP, Natal Jorge RM. Modeling the contraction of the pelvic floor muscles. Comput Methods Biomech Biomed Eng. 2016;19(4):347–56. This is the first finite element modeling study that considers active pelvic floor muscle contractions by including an active term in the constitutive model of muscle tissues. 56. Stokes WE, Jayne DG, Alazmani A, Culmer PR, editors. A physical simulation to investigate the effect of anorectal angle on continence. Biomedical Engineering (BioMed), 2017 13th IASTED International Conference on; IEEE; 2017. 57. Mellgren A, Zutshi M, Lucente VR, Culligan P, Fenner DE, Group TS. A posterior anal sling for fecal incontinence: results of a 152patient prospective multicenter study. Am J Obstet Gynecol. 2016;214(3):349. e1–8. 58. Grape HH, Dedering Å, Jonasson AF. Retest reliability of surface electromyography on the pelvic floor muscles. Neurourol Urodyn. 2009;28(5):395–9. https://doi.org/10.1002/nau.20648. 59. Auchincloss CC, McLean L. The reliability of surface EMG recorded from the pelvic floor muscles. J Neurosci Methods. 2009;182(1): 85–96. https://doi.org/10.1016/j.jneumeth.2009.05.027. 60. Koenig I, Luginbuehl H, Radlinger L. Reliability of pelvic floor muscle electromyography tested on healthy women and women with pelvic floor muscle dysfunction. Ann Phys Rehabil Med. 2017;60(6):382–6. https://doi.org/10.1016/j.rehab.2017.04.002. 61. Botelho S, Pereira LC, Marques J, Lanza AH, Amorim CF, Palma P, et al. Is there correlation between electromyography and digital

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palpation as means of measuring pelvic floor muscle contractility in nulliparous, pregnant, and postpartum women? Neurourol Urodyn. 2013;32(5):420–3. https://doi.org/10.1002/nau.22321. 62. Botelho S, Riccetto C, Herrmann V, Pereira LC, Amorim C, Palma P. Impact of delivery mode on electromyographic activity of pelvic floor: comparative prospective study. Neurourol Urodyn. 2010;29(7):1258–61. https://doi.org/10.1002/nau.20864. 63. Resende APM, Petricelli CD, Bernardes BT, Alexandre SM, Nakamura MU, Zanetti MRD. Electromyographic evaluation of pelvic floor muscles in pregnant and nonpregnant women. Int Urogynecol J. 2012;23(8):1041–5. https://doi.org/10.1007/ s00192-012-1702-6. 64. Bharucha AE, Dunivan G, Goode PS, Lukacz ES, Markland AD, Matthews CA, et al. Epidemiology, pathophysiology, and classification of fecal incontinence: state of the science summary for the National Institute of Diabetes and Digestive and Kidney Diseases (NIDDK) workshop. Am J Gastroenterol. 2015;110(1):127–36. https://doi.org/10.1038/ajg.2014.396. 65. Stafford RE, Sapsford R, Ashton-Miller J, Hodges PW. A novel transurethral surface electrode to record male striated urethral sphincter electromyographic activity. J Urol. 2010;183(1):378–85. https://doi.org/10.1016/j.juro.2009.08.105. 66. Stafford RE, Ashton-Miller JA, Sapsford R, Hodges PW. Activation of the striated urethral sphincter to maintain continence during dynamic tasks in healthy men. Neurourol Urodyn. 2012;31(1):36–43. https://doi.org/10.1002/nau.21178. 67.•• Stafford RE, Ashton-Miller JA, Constantinou C, Coughlin G, Lutton NJ, Hodges PW. Pattern of activation of pelvic floor muscles in men differs with verbal instructions. Neurourol Urodyn. 2016;35(4):457–63. This series of studies describes the pioneering application of transurethral surface EMG electrode to record the electromyography of male urethral sphincters. 68. Drost G, Stegeman DF, van Engelen BG, Zwarts MJ. Clinical applications of high-density surface EMG: a systematic review. J Electromyogr Kinesiol. 2006;16(6):586–602. https://doi.org/10. 1016/j.jelekin.2006.09.005. 69. Merletti R, Bottin A, Cescon C, Farina D, Gazzoni M, Martina S, et al. Multichannel surface EMG for the non-invasive assessment of the anal sphincter muscle. Digestion. 2004;69(2):112–22. https:// doi.org/10.1159/000077877. 70. Enck P, Franz H, Azpiroz F, Fernandez-Fraga X, Hinninghofen H, Kaske-Bretag K, et al. Innervation zones of the external anal sphincter in healthy male and female subjects. Digestion. 2004;69(2):123–30. https://doi.org/10.1159/000077878. 71. Wietek BM, Hinninghofen H, Jehle EC, Enck P, Franz HB. Asymmetric sphincter innervation is associated with fecal incontinence after anal sphincter trauma during childbirth. Neurourol Urodyn. 2007;26(1):134–9. https://doi.org/10.1002/nau.20307. 72.•• Cescon C, Riva D, Začesta V, Drusany-Starič K, Martsidis K, Protsepko O, et al. Effect of vaginal delivery on the external anal sphincter muscle innervation pattern evaluated by multichannel surface EMG: results of the multicentre study TASI-2. Int Urogynecol J. 2014;25(11):1491–9. This article summarizes the findings of a large multicenter study. The distribution of innervation zones was analyzed and compared before (511 prepartum women) and after (331 returned postpartum) delivery. 73.•• Cescon C, Raimondi EE, Začesta V, Drusany-Starič K, Martsidis K, Merletti R. Characterization of the motor units of the external anal sphincter in pregnant women with multichannel surface EMG. Int Urogynecol J. 2014;25(8):1097–103. In this article, the motor unit properties of the external anal sphincter during voluntary contraction were investigated in 478 pregnant women. The identified innervation zone distribution provided important pre-planning parameters for episiotomy. 74. Cescon C, Mesin L, Nowakowski M, Merletti R. Geometry assessment of anal sphincter muscle based on monopolar multichannel

Curr Urol Rep (2018) 19:9 surface EMG signals. J Electromyogr Kinesiol. 2011;21(2):394– 401. https://doi.org/10.1016/j.jelekin.2010.11.003. 75. Enck P, Franz H, Davico E, Mastrangelo F, Mesin L, Merletti R. Repeatability of innervation zone identification in the external anal sphincter muscle. Neurourol Urodyn. 2010;29(3):449–57. 76. Cescon C, Bottin A, Fraga XLF, Azpiroz F, Merletti R. Detection of individual motor units of the puborectalis muscle by non-invasive EMG electrode arrays. J Electromyogr Kinesiol. 2008;18(3):382–9. https://doi.org/10.1016/j.jelekin.2006.11.007. 77. Ullah K, Cescon C, Afsharipour B, Merletti R. Automatic detection of motor unit innervation zones of the external anal sphincter by multichannel surface EMG. J Electromyogr Kinesiol. 2014;24(6): 860–7. https://doi.org/10.1016/j.jelekin.2014.05.003. 78. Enck P, Hinninghofen H, Merletti R, Azpiroz F. The external anal sphincter and the role of surface electromyography. Neurogastroenterol Motil. 2005;17(s1):60–7. https://doi.org/10. 1111/j.1365-2982.2005.00660.x. 79. Sagi-Dain L, Sagi S. The correct episiotomy: does it exist? A crosssectional survey of four public Israeli hospitals and review of the literature. Int Urogynecol J. 2015;26(8):1213–9. https://doi.org/10. 1007/s00192-015-2680-2. 80. Merletti R, Riva D, Cescon C, Zacesta V. The correct episiotomy: does it exist? Int Urogynecol J. 2016;27(1):161–2. https://doi.org/ 10.1007/s00192-015-2879-2. 81.• Voorham-van der Zalm PJ, Voorham JC, van den Bos TW, Ouwerkerk TJ, Putter H, Wasser MN, et al. Reliability and differentiation of pelvic floor muscle electromyography measurements in healthy volunteers using a new device: the Multiple Array Probe Leiden (MAPLe). Neurourol Urodyn. 2013;32(4):341–8. This study describes a multi-channel EMG probe and its application in differentiation of EMG signals from a large group of healthy subjects (N=229). 82.•• Heesakkers J, Gerretsen R, Izeta A, Sievert KD, Farag F. Circumferential urinary sphincter surface electromyography: a novel diagnostic method for intrinsic sphincter deficiency. Neurourol Urodyn. 2016;35(2):186–91. This article describes the pioneering effort to apply a high-density surface EMG array to record the EMG activities from urinary sphincter muscles. 83.• Peng Y, He J, Khavari R, Boone TB, Zhang Y. Functional mapping of the pelvic floor and sphincter muscles from high-density surface EMG recordings. Int Urogynecol J. 2016;27(11):1689–96. This study describes the application of new intravaginal and intrarectal high-density surface EMG probes in detecting motor unit properties of multiple pelvic floor muscles. 84. Peng Y, He J, Yao B, Li S, Zhou P, Zhang Y. Motor unit number estimation based on high-density surface electromyography decomposition. Clin Neurophysiol. 2016;127(9):3059–65. https://doi.org/ 10.1016/j.clinph.2016.06.014. 85. Holobar A, Zazula D, editors. Gradient convolution kernel compensation applied to surface electromyograms. International Conference on Independent Component Analysis and Signal Separation: Springer; 2007. 86. Liu Y, Ning Y, Li S, Zhou P, Rymer WZ, Zhang Y. Threedimensional innervation zone imaging from multi-channel surface EMG recordings. Int J Neural Syst. 2015;25(06):1550024. https:// doi.org/10.1142/S0129065715500240. 87. Zhang C, Peng Y, Liu Y, Li S, Zhou P, Rymer WZ, et al. Imaging three-dimensional innervation zone distribution in muscles from Mwave recordings. J Neural Eng. 2017;14(3):036011. https://doi.org/ 10.1088/1741-2552/aa65dd. 88.• Flury N, Koenig I, Radlinger L. Crosstalk considerations in studies evaluating pelvic floor muscles using surface electromyography in women: a scoping review. Arch Gynecol Obstet. 2017:1–11. This review article highlights the topic concerning the problem of crosstalk in pelvic floor surface EMG studies.