What Does Electromyography Tell Us About Dyspareunia?

What Does Electromyography Tell Us About Dyspareunia? Linda McLean, PhD,1 and Kaylee Brooks, MSc(c), BSc(Psych)2

ABSTRACT

Introduction: Emergent evidence suggests that pelvic floor muscle (PFM) dysfunction contributes to dyspareunia, the experience of pain on vaginal penetration. Electromyography (EMG) is a valuable tool for the assessment of neuromuscular control and could be very useful in enhancing our understanding of PFM involvement in sexual function and in conditions such as dyspareunia. However, PFM EMG must be interpreted within the context of the many factors that can influence findings. Aim: To outline the main factors to consider when evaluating PFM EMG for female sexual function and dyspareunia and to synthesize the literature in which EMG has been acquired and interpreted appropriately in this context. Methods: Standards for the acquisition and interpretation of EMG were retrieved and consulted. An exhaustive search of four electronic databases (Embase, CINAHL, PubMed, and PsycLit) and hand searching references from relevant articles were performed to locate articles relevant to PFM involvement in sexual function and in dyspareunia in which EMG was used as a primary outcome. Study outcomes were evaluated within the context of the appropriate application and interpretation of EMG and their contribution to knowledge. Main Outcome Measures: A synthesis of the evidence was used to present the current state of knowledge on PFM involvement in sexual function and in dyspareunia. Results: Few standards documents and no practice guidelines for the acquisition and interpretation of PFM EMG are available. Some cohort studies with small samples of women have described the role of the PFMs in female sexual function. The literature on PFM involvement in dyspareunia also is limited, with outcomes suggesting that higher than normal tonic activation and higher than normal reflex responses might be present in the superficial PFM layer and might be characteristic features of dyspareunia. The data are less clear on the involvement of the deep layer of the PFMs in dyspareunia. Conclusion: Guidelines for the application and interpretation of PFM EMG in the context of sexual function and dyspareunia are needed. When interpreted within the context of their strengths and limitations, EMG data have contributed valuable information to our understanding of PFM involvement in dyspareunia. The literature to date suggests that the superficial PFMs might have higher than normal tone and exaggerated responses to tactile or penetrative provocation in at least some women with dyspareunia. McLean L, Brooks K. What Does Electromyography Tell Us About Dyspareunia? Sex Med Rev 2017;X:XXeXX. Crown Copyright
2017, Published by Elsevier Inc. on behalf of the International Society for Sexual Medicine.

Key Words: Dyspareunia; Pelvic Floor Muscles; Electromyography; Muscle Tone

INTRODUCTION Dyspareunia—pain during sexual intercourse—affects 10% to 28% of women.1 This disorder, described as genito-pelvic pain/penetration disorder in the Diagnostic and Statistical Received August 20, 2016. Accepted February 14, 2017. 1

School of Rehabilitation Science, Faculty of Health Sciences, University of Ottawa, Ottawa, ON, Canada;

2

School of Kinesiology, Faculty of Health Sciences, University of Ottawa, Ottawa, ON, Canada

Crown Copyright ª 2017, Published by Elsevier Inc. on behalf of the International Society for Sexual Medicine. http://dx.doi.org/10.1016/j.sxmr.2017.02.001

Sex Med Rev 2017;-:1e13

Manual of Mental Disorders, is defined as “difficulties experienced with vaginal penetration during intercourse, marked vulvovaginal or pelvic pain during vaginal intercourse or penetration attempts, marked fear or anxiety about vulvovaginal or pelvic pain in anticipation of, during, or as a result of vaginal penetration, and marked tensing or tightening of the pelvic floor muscles (PFMs) during vaginal penetration.”2 Specific disorders, such as infection,3 inflammation,4 trauma, genetic factors,5,6 and hormone changes7 can result in vulvar pain. However, in a large proportion of women with vulvar pain, there is no clear, identifiable cause.8 Alterations in peripheral or central pain processing8e10 also have been identified and could be key factors in the persistence and/or recurrence of dyspareunia and could result in 1

2

heightened behavioral responses that result in contraction of the PFMs.11,12 Clinical reports of higher than normal PFM tone or unwanted contraction of the PFMs during attempts at penetration activities have suggested that the PFMs are implicated in dyspareunia,13 but we do not fully understand the context of such PFM involvement, often vaguely described as “hypertonicity or other dysregulations.”14 This lack of precision for the description of PFM involvement in dyspareunia is a reflection of how poorly understood the nature of this involvement is, although PFMs have been recognized as contributing to this disorder for quite some time.15 As recently noted by Reissing et al,15 the first published description of vaginismus did not distinguish between a contraction of the PFMs and pain, referring to “spasmodic closure of the vagina,” whereby the “slightest touch . at the reduplication of the hymeneal band produced . severe suffering.”16 In the contemporary literature, descriptions of PFM involvement in dyspareunia have included “heightened tone,”17,18 “hypertonicity,”17,19,20 “hypertonic dysfunction,”1 “hyperactivity,”21 “tension myalgia,”22 “non-relaxing,”23 “overactive,”24 and “short,”25 whereby investigators’ beliefs about the underlying mechanisms can be presumed based on their choice of terminology, and whereby the predominant opinion appears to be that women who report dyspareunia have higher than normal neural excitation of their PFMs. A recent consensus document by the International Continence Society refers to dyspareunia as one presentation among several clinical sequelae of “high-tone pelvic floor dysfunction,” in which symptoms also can manifest as muscle pain in the groin, low back, or gluteal regions, urinary or bowel dysfunction, and/or elimination difficulties.26 Some investigators have suggested that the PFM dysfunction in dyspareunia goes beyond changes in muscle tone and that affected women also present with difficulties in the neuromuscular control of the PFMs including poor ability to achieve18 and sustain27e29 a PFM contraction and to relax the PFMs after activation.11 With the plethora of terms used to describe the PFM involvement in dyspareunia and conflicting findings on the nature of this involvement,30 it is not surprising that the clinical evaluation and effective management31 of PFM dysfunction in dyspareunia have remained somewhat elusive. When applied and interpreted properly, electromyography (EMG) can be useful to provide insight into the mechanisms underlying PFM dysfunction in women with dyspareunia. Although EMG is relatively simple to apply, and many commercial systems are available to clinicians and researchers, there are no established guidelines for the application and interpretation of PFM EMG in the context of dyspareunia. Because many commercial systems use intravaginal electrodes that are inappropriately configured,32 the EMG outcomes from studies in which these systems have been used should be interpreted with caution. The objectives of this review were (i) to search for standards or guidelines for EMG acquisition and interpretation

McLean and Brooks

that are relevant to the PFMs and (ii) to review and synthesize the results of studies that have appropriately incorporated EMG as an outcome measurement when studying sexual function in general and dyspareunia more specifically.

METHODS Two literature searches were performed. The Embase, CINAHL, and PubMed databases were searched from May 3 to 10, 2016 for English-language publications using key words electromyography OR EMG AND standards OR guidelines, with no limits placed on year or type of publication. The search yielded only three articles, with one article being relevant to neurophysiologic investigations33 and no articles being relevant to surface EMG (SEMG). Therefore, the search was expanded to the Google database using the search terms EMG standards and EMG guidelines. A subsequent search of the Embase, CINAHL, PubMed, and PsycLit databases was performed from June 3 to August 10, 2016, using key words electromyography OR EMG AND pelvic floor muscles OR levator ani AND dyspareunia OR sexual pain OR vaginismus OR provoked vestibulodynia OR vulvar vaginitis OR sex. Only English-language articles were retrieved and no limits were set on the date of publication, type of article, or publication status. Study abstracts were screened for relevance, and reference lists were hand searched to ensure that all relevant articles were reviewed and included where appropriate. Data were extracted after thoroughly reviewing each article for relevance and for scientific rigor. Clear distinctions were made between theory and empirical evidence, because there were many narrative reviews and opinion pieces among the articles retrieved.

RESULTS Standards for Acquisition and Recording of EMG Only one relevant article on EMG standards was found through Embase,33 which focused on standards for neurophysiologic testing using EMG (ie, needle EMG recordings and evoked potential studies). One article31 and one book chapter11 on SEMG standards specifically with reference to PFMs, and co-written by one of the present authors, was retrieved through PubMed. Through the Google search engine using the search term surface EMG standards, three key resources that were not associated with commercial interests were found: (i) the standards for reporting EMG data,34 endorsed by the International Society of Electrophysiology and Kinesiology; (ii) recommendations by the Surface Electromyography for the Non-Invasive Assessment of Muscles (SENIAM) project,35 which are European standards published in the Journal of Electromyography and Kinesiology; and (iii) a keynote address published as an article by De Luca36 on the use of SEMG in biomechanics that was published in the Journal of Applied Biomechanics. Key factors associated with the fidelity and interpretation of EMG data relevant to the PFMs were synthesized from these sources and categorized into three headings: type of electrode, electrode Sex Med Rev 2017;-:1e13

Electromyography and Dyspareunia

configuration, and type of EMG activity being recorded. The reviews by Stålberg et al,33 Keshwani and McLean,32 and Gentilcore-Saulnier et al30 provide excellent detail on the acquisition and interpretation of EMG data and are recommended to readers who wish for more information. Type of Electrode EMG signals are generated through action potentials propagating along muscle fibers. These signals can be recorded through needle electrodes, where the tip of the needle is located within the muscle and records EMG signals from single muscle fibers or small groups of nearby muscle fibers; through fine wire electrodes that record motor unit potentials within a small region of the muscle; or through surface electrodes, which, depending on electrode size and spacing, record EMG signals from large numbers of motor units within a given muscle and are most representative of global activation of the muscle of interest.32 Needle EMG recordings are normally studied in the context of clinical neuromuscular assessment—where the size, shape, firing frequency, and sometimes propagation velocity of muscle fiber action potentials are recorded during low-level contractions and are of interest in diagnosing myopathic or neuropathic processes.33 Needle electrodes are sometimes used for other purposes, such as to record EMG signals during more intense contractions to evaluate global activation and/or to shed light on neuromuscular control37e42 when the muscle of interest is small or located deep beneath other muscle layers. Fine wire EMG recordings are generally used for research applications. Like needle electrodes, they are useful when recording activation from small muscles and/or muscles that run deep to the skin surface, where distinct EMG signals are difficult to obtain because other muscles lie adjacent or superficial to the muscle of interest. Fine wire EMG signals are particularly useful in studying neuromuscular activation in the context of understanding biomechanics or motor control.36,43 Unlike needle electrodes, fine wire electrodes are normally painless after insertion and therefore studies of normative muscle activation are not influenced by pain induced by the recording technique. SEMG recordings are the most commonly used form of EMG for biomechanics and motor control studies36 because they are easy to acquire and are noninvasive. They can provide useful information about global muscle activation patterns in large and/or superficial muscles and can be used to provide biofeedback on task performance.30 In studying the PFMs during sexual activities, the muscles are very small and, as such, needle or fine wire electrodes are of value because they are more likely to be resistant to crosstalk contamination (the recording of neuromuscular activation from nearby muscles that is indistinguishable from the activation of the muscle of interest), but the use of needle or fine wire electrodes is not practical for large-scale studies because the methods are invasive and unlikely to be acceptable to many women—especially given that the site of insertion is the perineum or through the vaginal wall.

Sex Med Rev 2017;-:1e13

3

Electrode Size and Spacing In modern EMG systems, differential recordings are the norm, in which two electrodes are placed over or within a muscle of interest and the resulting signal is recorded as the difference between the signals seen by each electrode at each point in time.32,35 In needle and fine wire EMG, the electrode configurations are more or less fixed, other than when monopolar needle electrodes are used (eg, Ambu Neuroline monopolar electrodes; http://www.Ambu.com), which are often referenced relative to a site where there is presumed to be no electrophysiologic activity. In contrast, for SEMG, electrode size and configuration can be discretionary, because adhesive electrodes are commonly used, allowing the clinician or researcher to decide on the precise size of and separation between pairs of electrodes (eg, http://www. noraxon.com; http://www.btsbiomedical.com; http://www. cadwell.com). Some commercial EMG systems come with proprietary, reusable surface electrode units with built-in preamplifiers (eg, http://www.Delsys.com; http://www.biopac.com) that fix the electrode size and spacing. In general, small, closely spaced electrodes are recommended to avoid the recording of excess physiologic (eg, heart signals) or electrical (eg, from the local environment) noise and crosstalk.35 Keshwani and McLean32 provided a thorough review of commercial electrodes used to evaluate PFM activation and found that most commercial intravaginal probes have embedded electrodes that are larger and separated farther than what is recommended in international standards,34,35 which suggest that roughly 10 mm of interelectrode spacing is optimal to minimize crosstalk contamination.44 Further, the electrode configurations on intravaginal probes are often inappropriate, because the two electrodes from a given pair are not properly aligned with respect to the direction of EMG signal propagation or are not located on the same muscle; Keshwani and McLean32 referred to the latter as a “faux-differential” configuration. These design flaws can lead to uncertainty in interpretation, limiting the value of most commercially available intravaginal probes as an outcome measurement in clinical or research applications. Type of EMG Activity Recorded The context of the EMG recordings is another important factor in interpreting PFM findings. Muscle activity recorded when the muscle is not contracting voluntarily or reflexively is sometimes referred to as tonic activation30 and reflects the functional demands placed on the muscle and the excitability of associated motor neurons or muscle fibers.33,45 Most muscles have no detectable SEMG signals when at rest,46 but this is not the case for the PFMs,47 which are constantly involved in postural support48,49 and continence control.50 The PFMs are under voluntary and automatic control. When contracted voluntarily, the resultant EMG activation patterns can be used to evaluate neuromuscular control.36 Although positively correlated, there is no linear relation between the EMG activation amplitude and the force generated51; a relation has yet to be

4

established for PFMs.30 As such, the amplitude of the PFM EMG signal should not be used as a proxy for muscle force. Activation amplitude also is affected by other characteristics of the contraction; for example, if the muscle remains the same length compared with when it shortens or lengthens, then the EMG amplitude can differ even when the force output does not.51e53 Because the amplitude of the recorded EMG signal also depends on the size, location, and configuration of the recording electrodes relative to the location and number of active muscle fibers54 and the excitability of the motor neuron pool,55 EMG activation amplitude recorded from the PFMs during voluntary activation is inherently highly variable between patients and between sessions,56,57 making it an undesirable outcome measurement in research or clinical applications. Further, synergistic action must be considered within the context of crosstalk32 and changes in the postural48,49 or continence50 demands. Evaluating the endurance of the PFMs during voluntary activation using EMG signal characteristics is quite complex, because muscle force output must be recorded concurrently to establish whether changes in EMG signal amplitude or frequency characteristics are the result of declines in muscle force-generating capacity, motivation, and/or motor control. Studies in which PFM endurance is reported using EMG and/or force outcomes in isolation must be interpreted with caution. The reflex activation of muscles can be determined using electrical stimuli to the nerve leading to that muscle, mechanical stimuli, such as a stretch to the muscle or provocation stimuli delivered to structures that have reflex associations with the muscle of interest, or stimulation of interneurons associated with interneurons at spinal or supraspinal levels.33 Muscle activation timing and amplitude in response to provocation stimuli show aspects of the morphology and excitability of the motoneuron pool.33 The nerves innervating the PFMs are difficult to access along their pathways deep within the pelvis and therefore electrically evoked reflexes are rarely studied. PFM motor-evoked potentials generated through transcranial magnetic stimulation have demonstrated high within-subject variability58e60—likely because the cortical motor area for the PFMs lies so deep within the central sulcus that very high stimulation levels are required. High levels of cortical stimulation lead to the activation of several nearby muscles, which in turn results in crosstalk contamination when recording PFM EMG and precludes interpretability. Studies retrieved when searching for PFM involvement in sexual function and dyspareunia must be interpreted within the context of the type of electrode used, the electrode size and spacing, and the type of EMG activity recorded.

EMG Recorded From PFMs to Understand Female Sexual Function and Dysfunction All results retrieved through the second search were categorized under two key headings: the role of the PFMs in normative sexual function and cohort studies comparing some aspect of

McLean and Brooks

PFM function in women with vs without dyspareunia. Cohort studies were further classified by the outcomes studied: (i) tonic activation, (ii) voluntary activation, and (iii) reflex or evoked activation. Overall, very few studies were retrieved, yet cohort studies were found describing impairments in all three of these areas in women with dyspareunia compared with women without any history of sexual pain. Role of PFMs in Female Sexual Function The PFMs are normally involved in sex, yet their exact function is not fully understood. This knowledge gap could explain why we understand so little about the role of the PFMs in dyspareunia. Because the bulbocavernosus muscle, the most superficial PFM, encircles the introitus, it is reasonable to assume that relaxation of this muscle is necessary for pain-free vaginal penetration, yet no study was retrieved that demonstrated this empirically. Seminal studies by Shafik et al provided some of the only research evidence for what can be considered normal in terms of the PFM contributions to sexual activities in women. Using needle EMG, the bulbocavernosus muscle was found to be active during sexual activity, and it was presumed to function to hold the penis (or other penetrative device) in place while providing penile stimulation during heterosexual sex.61,62 Reflex contractions of the levator ani and puborectalis muscles have been found on stimulation of the clitoris and cervix and it has been suggested that they enhance biological reproductive function by providing distal vaginal distention, elongation of the vagina, and proximal vaginal ballooning, presumably facilitating entry of the penis, moving the cervix more cranially to limit potentially painful contact, and providing a receptacle near the cervix to hold semen and thus facilitate conception, respectively.63,64 Contraction of the pubovisceral portion of the levator ani results in a shortening of the distance between the posterior rectum and the pubic symphysis,65 essentially compressing the vaginal opening. This anatomic feature could contribute to sexual satisfaction and could make this muscle relevant in dyspareunia. Some studies have suggested that strong PFMs are associated with better sexual function in women66e68; however, the evidence for PFM strengthening to enhance sexual function is currently limited. Differences in PFM Activation in Women With vs Without Dyspareunia The results of the different cohort studies investigating differences in muscle activation, as measured using EMG, in women with vs without dyspareunia are presented in Table 1.

Tonic PFM activation in dyspareunia. It appears that the PFMs of women with dyspareunia have higher levels of tonic activation than their pain-free counterparts. Using needle EMG, Shafik and El Sibai42 reported significantly higher tonic EMG activation in the bulbocavernosus, puborectalis, and levator ani muscles of women with vaginismus (n ¼ 7) compared with women without dyspareunia (n ¼ 7). Despite the limitations of Sex Med Rev 2017;-:1e13

5

Electromyography and Dyspareunia

Table 1. Results of different cohort studies investigating differences in muscle activation, as measured using electromyography G, in women with vs without dyspareunia Type of activation Tonic activation

Voluntary activation Maximum voluntary activation

Superficial PFMs Higher in women with vaginismus and PVD69 than in controls, but the samples were very small.

Possibly higher in women with vaginismus.42 Early suggestion that tone is higher in women with vulvodynia,27 yet much evidence suggests no difference between women with PVD compared with controls.71e74

No evidence

Postulated to be decreased,28,29,75 yet no difference in women with vs without dyspareunia71e74,76 in cohort studies. Postulated to be impaired,27,29 yet no difference in women with vs without dyspareunia71e74,76 in cohort studies. Impaired endurance has been postulated in women with PVD27; however, no studies have assessed EMG and force concurrently, which is essential to draw conclusions. Not higher in women with PVD when stimulus is pressure at the vulvar vestibule.73

Amplitude variance during sustained activation

No evidence

Endurance

No evidence

Evoked or reflex activation

Deep PFMs 42,69,70

Polysynaptic reflex amplitudes higher in women with vulvodynia than controls69 when evoked through clitoral stimulation. Might be higher in women with PVD when evoked through pressure at the vulvar vestibule73 or vaginal probe insertion.42

EMG ¼ electromyography; PFM ¼ pelvic floor muscle; PVD ¼ provoked vestibulodynia.

their study (ie, small sample, lack of blinding, lack of psychometric data on their approach), the result is quite compelling, because the women with vaginismus had almost double the tonic EMG activation amplitude compared with their control counterparts. Frasson et al69 found results consistent with higher tonic activation of the external anal sphincter, also considered a superficial PFM, in 10 women with idiopathic lifelong vaginismus and in 10 women with vulvar vestibulitis syndrome (ie, provoked vestibulodynia), but not in controls. Most recently, Gammoudi et al70 found, using needle EMG, higher than normal EMG responses in the bulbocavernosus and ischiocavernosus muscles in seven of nine women with a clinical diagnosis of vaginismus, whereas no such evidence was present in 11 controls. Further, four of the nine women with vaginismus demonstrated higher than normal tonic activation of the same muscles. However, it is difficult to define vaginismus14,15 and vaginismus is not present in all women with dyspareunia; therefore, these results might not be representative of PFM involvement in all subtypes of dyspareunia.15 Findings regarding tonic activity of the PFMs have been mixed when evaluating women with dyspareunia using SEMG. After having observed that women with vulvar vestibulitis syndrome decreased the amplitude of the tonic activation of their PFMs after a period of training using SEMG biofeedback,29 Glazer et al27 sought and found higher tonic PFM activation in women with dysesthetic vulvodynia (n ¼ 25) compared with healthy controls (n ¼ 25). Since that time, several separate cohort studies27,28,71e74 using various surface electrode Sex Med Rev 2017;-:1e13

configurations and protocols have reported no difference in tonic PFM EMG amplitudes in women with vs without vulvar pain. Because of the type of EMG electrodes used by Glazer et al, which were large and covered the circumference of an intravaginal probe, their SEMG signals might have represented the combined activation of the superficial and deep layers of the PFMs and other nearby muscles (eg, hip rotators), which could explain the differences in results. A recent cohort study by Gentilcore-Saulnier et al,73 using separate differential SEMG electrode pairs over the superficial (transperineal) and deep (intravaginal) PFM layers, demonstrated that women with provoked vestibulodynia (n ¼ 11) had significantly higher normalized tonic activity in their superficial but not their deep PFMs compared with controls (n ¼ 11). However, all cohort studies to date have been very small and lack assessor blinding as a feature of their experimental design. Taken together, the results from studies investigating tonic activation of the PFMs suggest that women with dyspareunia present with heightened tonic activation of the superficial layer of the PFMs. Because of the nature of these studies, a causal relation cannot be established and it is not clear whether this tonic activation is heightened because the women are anxious about the testing procedures or are in a state of perpetually heightened neuromuscular excitation. Further research is required to validate and standardize test scenarios and electrode configurations to clearly elucidate which, if any, muscles comprising the deep PFMs demonstrate heightened tonic activation in women with dyspareunia. Such studies should incorporate appropriate

6

McLean and Brooks

electrode size and configuration and use blinded assessors to strengthen the level of resulting evidence.

Voluntary PFM activation and motor control. Although it has been postulated that women with dyspareunia have deficits in PFM strength and motor control,28,75,77 cohort studies have failed to demonstrate that maximal voluntary activation amplitudes are lower or that motor control is impaired in women with dyspareunia compared with pain-free counterparts.71e74,76 Therefore, it is not clear what, if any, differences exist in the activation capacity of the PFMs in women with vs without dyspareunia. Some have suggested that women with dyspareunia have impaired PFM endurance capacity.27 However, using EMG, muscle fatigue can be confirmed only if there is a concurrent measurement of force output—which has not been the case in any study to date, likely because there is no instrument on the market that can currently and validly measure PFM force and EMG. Glazer et al27 reported that women with vulvodynia have particular difficulty with the performance of steady contractions of their PFMs and, based on this discovery, developed an EMGbased PFM biofeedback program to address tonic activation and poor motor control. Conversely, Engman et al71 found no significant differences in women with vs without vaginismus in the variance of EMG amplitude during phasic contractions.

Reflex connections and PFM activation. The PFMs appear to be strongly influenced by reflex responses. The reflex activity of the superficial bulbocavernosus muscle can be electrophysiologically evaluated through non-painful stimulation of the clitoris or electrically through stimulation of the clitoral nerve, with multiphasic responses reflecting the complexity of neural inputs to these muscles.78 This evaluation is not commonly performed in clinical settings but could be of value in the assessment of spindle excitability when trying to understand the relative contributions of different excitation mechanisms related to dyspareunia. 69

Frasson et al demonstrated hyperreflexia of the bulbocavernosus muscle in response to clitoral stimulation in women with vulvodynia. Regardless of subtype, women with vulvodynia demonstrated polysynaptic reflex amplitudes that were approximately twice as high as those recorded from a control group, providing compelling evidence of a central nervous system involvement. These results could reflect the phenomenon reported by Shafik and El Shibai,42 whereby higher amplitude needle PFM EMG responses were observed during vaginal probe insertion in women with vaginismus, and the phenomenon reported by Gentilcore-Saulnier et al73 who observed higher normalized SEMG responses in the bulbocavernosus muscle in women with provoked vestibulodynia compared with those without vulvar pain when a pressure stimulus was applied to the vulvar vestibule.

DISCUSSION There are no guidelines or standards for the acquisition and reporting of PFM EMG data. Such standards would improve the quality and value of reported outcomes using PFM EMG to understand the pathophysiology of dyspareunia. Standards also would allow for between-study comparisons and meta-analyses. The PFMs have a complex multilevel, multiplanar anatomy79 but generally can be considered as having two functional layers: superficial and deep. In developing standards for PFM EMG, despite the synergies between the muscle layers, based on the results presented in Table 1, there is a clear need to separate the evaluation of the superficial and deep layers of the PFMs and for researchers to study the two muscle layers separately but concurrently when evaluating PFM function and dysfunction in terms of tonic, voluntary, reflex, and evoked activation. Although needle or fine wire electrodes are ideal because they are more specific for this purpose, it might be wise to develop and refine methods to study the muscle layers using SEMG electrode pairs or arrays. Despite their inherent limitations in crosstalk and motion artifact,32,80,81 surface electrodes are less invasive and more likely to be acceptable to women. Based on the EMG literature available at this time, it appears likely that women with dyspareunia present with higher than normal tonic activation and hyperreflexia of the superficial layer of the PFMs, particularly the bulbocavernosus muscle. This finding is consistent with the experience of pain when a finger, penis, or other device is inserted into the vagina—tonic activation or premature contraction of the bulbocavernosus muscle can narrow the introitus making penetrative activities difficult. If penetrative activities continue despite contraction of the superficial PFMs, then pain and tissue injury can ensue, and the deeper layer of the PFMs can respond as a protective response82 or synergistically. However, this theory is based on small-scale cohort comparisons; larger, confirmatory studies are required using protocols in which the assessor is blinded to group assignment. Most studies on women with dyspareunia report no significant differences in EMG findings within the deep PFM layers.27,28,71e74 Although intravaginal palpation showed restriction of the vaginal opening and higher tone (resistance to passive stretch) of the pubococcygeus muscle but not of the puborectalis muscle in women with vulvar vestibulitis syndrome,11 the same study found no differences in deep PFM tone in women with vs without dyspareunia when muscles were palpated anally. Although palpation findings should be interpreted with caution, because they are subjective and have questionable reliability,83 results suggest that the superficial PFMs in women with provoked vestibulodynia demonstrate increased tonic activation, which is consistent with the EMG findings discussed earlier.42,69,73 The EMG data imply that the tonic activation of the deeper layer of the PFMs is not higher than normal in women with dyspareunia,27,28,71e73 but this layer

Sex Med Rev 2017;-:1e13

Electromyography and Dyspareunia

7

Figure 1. Factors contributing to PFM tone in women. Beyond the usual neural input from sensory nerve endings within the muscle fibers, the PFMs receive neural input from several sources including the surrounding tissues and organs (especially the bowel and bladder) and the limbic system, which is linked to emotions such as pain and anxiety. Although myofascial TrPs are currently poorly understood, they also might contribute to alterations in PFM tone through mechanical or neural processes. GTOs ¼ Golgi tendon organs; PFM ¼ pelvic floor muscle; TrPs ¼ trigger points.

might still demonstrate heightened responses to vaginal penetration.69 The development of standardized approaches to study superficial and deep PFM tonic activation, voluntary activation, and reflex responses are needed to inform our understanding of PFM involvement in dyspareunia.

Psychophysiologic and Psychosocial Considerations When Interpreting EMG Findings From PFMs Beyond the standardization of EMG hardware and signal processing,30 the interpretation of EMG findings must consider and attempt to control concurrent biological, psychophysiologic, and psychosocial factors. Biological factors include the many reflex loops known to affect PFM excitability, mechanical factors including PFM and connective tissue stiffness characteristics, and the presence of myofascial trigger points (TrPs) and are presented in Figure 1. Psychological confounders are many and include the impact of alterations in pain processing that can occur in the absence of physiologic evidence of tissue damage and psychosocial factors including changes in emotional state related to cultural beliefs or experiences. These factors are not unique to PFM assessment using EMG; they also would influence other Sex Med Rev 2017;-:1e13

forms of PFM assessment such as palpation, dynamometry, and ultrasound imaging but are particularly relevant to the interpretation of PFM EMG outcomes. Biological Factors: Reflex Loops and Myofascial Trigger Points Shafik et al reported extensively on reflex loops that affect the excitability of the PFMs, including findings of a “straining cavernous reflex,”84 a “urethrovesical stimulation reflex,”85 a urethro-corporo-cavernosal reflex,38 a cavernoso-anal reflex,41 and a “vesicoperineal reflex,”39 whereby superficial PFM activation was found to be associated with increases in intraabdominal, bladder, urethral, and anal pressures. There is good evidence that tonic activation of the deep PFMs increases with increasing volumes of urine in the bladder.50,86,87 More research into the complex neural loops among the pelvic viscera and the PFMs could prove fruitful in our understanding of the influence of PFM tone on dyspareunia, but no studies have been reported in this area to date. A standardized approach to the investigation of tonic activation should include recommendations for limiting the influences of visceromotor reflexes on PFM EMG outcomes,

8

for example, no gas or stool in the bowel and standardized urine volumes and positioning. Despite the ample presence of sensory nerve endings to monitor muscle tension and position (ie, muscle spindles, Golgi tendon organs) and optimal conditions (eg, tonic activation), anecdotal evidence suggests that women have relatively poor kinesthetic awareness of their PFMs.88 Some reports have suggested that as many as 30% of healthy women cannot perform a voluntary PFM contraction.89e91 Others have commented on apparent alterations in kinesthetic awareness of the PFMs in women with urinary incontinence92,93; however, studies specifically designed to evaluate differences in kinesthetic awareness in women with vs without dyspareunia or other pelvic floor disorders have not been reported in the literature and future research should address this gap. The physiologic interpretation of more variable EMG activity recorded during a sustained PFM contraction is unclear because this phenomenon can result from many causes including pain, poor kinesthetic awareness, poor motor control, poor endurance, or poor motivation. Further, the many reflex loops within the genitourinary system can make the PFMs particularly susceptible to brainstem and limbic inputs,21,94,95 which in turn could affect tonic and phasic PFM activation from one moment to the next. Activation of the PFMs, generated through cutaneous, emotional,11,21,94,96 or visceral50,86,97,98 excitation, could make these muscles more excitable in women with dyspareunia, in turn causing impairments in motor control, yet there is currently no evidence to support this. Myofascial Trigger Points Can Confound the Assessment of PFM Tone Myofascial pain syndrome and myofascial TrPs have been the focus of many reported assessment20,99,100 and treatment approaches62e64 for dyspareunia.101,102 Despite this syndrome being extremely poorly understood, patients are diagnosed with myofascial pain syndrome if they have palpable nodules or bands (eg, TrPs) within their PFMs, and if palpation of the nodule or band causes a reproduction or exacerbation of the patient’s pain complaint, often leading to a localized twitch response.103,104 Based on the recent review by Shah et al104 and despite our limited understanding of myofascial TrPs, research suggests that the presence of a TrP causes an increase in stiffness of the muscle. Although TrPs are not associated with higher than normal tonic EMG activation,104 pressure on a TrP can result in a localized twitch response,103,104 which must be taken into account when interpreting EMG findings. Anticipation of pain, especially if a women has a TrP, can further confound interpretation of PFM tone. Psychophysiologic Factors: Alterations in Pain Processing and Behavioral Responses Can Occur in Dyspareunia and Can Confound EMG Findings Understanding PFM involvement in dyspareunia is complicated even further by the physiology of pain. The site of pain

McLean and Brooks

perception could be at the source of the tissue damage or far from it. Pain also can be present in the absence of any evidence of tissue damage at all. Through recent advances in pain science, we know that virtually any painful experience can lead to alterations in pain processing through changes in peripheral and central pain processing. Persistent pain induces changes in the peripheral and central nervous systems that lead to allodynia (eg, decreased pain threshold whereby stimuli that are not normally perceived as pain are found to be painful) and hypersensitivity (eg, decreased tactile threshold). In the peripheral nervous system, axonal sprouting, spontaneous firing, and increases in inflammatory neuropeptides occur locally, and these phenomena lead to a release of excitatory and inflammatory neuropeptides and an increase in upregulation of the pain signals to the brain. In cases of central sensitization, brain activity is increased in pain-related cortical regions (eg, cingulate, insular, and frontal cortices) in response to tactile and painful stimuli10,105 and the regions of the brain that receive sensory input from the affected area are enlarged.106 Such changes could explain dyspareunia that occurs after the resolution of known pathologies such as vaginal infection.107,108 There have been assumptions in the literature that prolonged or recurrent pain in the pelvic organs is accompanied by an increase in tonic or reflex PFM activity,88,109 and although there is no empirical evidence to confirm this, it can be explained through visceromotor reflexes as discussed earlier. The central nervous systems of women with dyspareunia exhibit evidence of augmented neural activity in areas of pain modulation in response to painful vestibular stimulation,10 and they have greater gray matter density in several brain areas,110 similar to what is seen in other chronic pain conditions. Pain processing is clearly impaired in women with some forms of dyspareunia.8 As such, alterations in peripheral and central pain processing can enhance any protective or withdrawal responses seen in the PFMs and could be a key area of focus for therapies.12 Psychosocial Factors Holstege96 recently described an “emotional motor system” in cats, which has connections to many bodily functions and regions including the muscles innervated by the sacral nerves and, hence, the PFMs. The emotional motor system represents diffuse pathways originating in the caudal brainstem and terminating on spinal gray matter, which can affect the tone or excitability of the PFMs under different physiologic conditions, such as voiding, sexual activity, or sleeping. The suggestion of such a direct influence between emotion and PFM activity is particularly interesting because the tonic activation of the PFMs has been found to be elevated in women who are experiencing states of high psychological stress.11,21,94 In women with and without dyspareunia, PFM and trapezius muscle activity is increased when watching sexually threatening film clips and anxiety-provoking film clips without sexual content,94,111 suggesting that the PFMs increase their Sex Med Rev 2017;-:1e13

9

Electromyography and Dyspareunia

Figure 2. A proposed systematic approach to using EMG in the assessment of pelvic floor muscle function in women with dyspareunia.

Based on the findings of this review, we recommend the development of standardized approaches to the evaluation of superficial and deep pelvic floor muscle layers. When evaluating tonic pelvic floor muscle activation, it is important to remember that biomechanical (position, posture), physiologic (bladder fullness), and emotional inputs will influence the EMG signal amplitude. It might be of value to assess tonic activation in the absence of impending provocation and separately before and after some provocation (eg, pressure, penetration). It also is important to remember that noise from the environment and from the EMG equipment will be embedded in recordings of tonic pelvic floor muscle EMG activation. No normative values exist. When evaluating voluntary pelvic floor muscle activation, it is important to remember that EMG amplitude is highly variable from day to day and does not directly reflect force output, meaning that comparisons among women or among days should be avoided. No normative data exist for voluntary pelvic floor muscle EMG activation. Standardized protocols for the evaluation of evoked and reflex activation of the pelvic floor muscle do not exist but could provide valuable information about central and peripheral neuronal excitability. Currently, no normative data are available for reflex latencies. EMG ¼ electromyography.

activation as part of a general defense mechanism. However, such defense mechanisms can be enhanced in women with a history of sexual abuse94 and this factor should be carefully considered when evaluating PFM tone in women with dyspareunia. The emotional state of women and their perceived threat of pain or discomfort with the assessment procedures must be taken into account when evaluating the tone of the PFMs in all women, which can be particularly relevant in women with dyspareunia. Emotions can increase the excitatory drive to the PFMs, enhancing tonic activation and excitability of the stretch reflexes. EMG could be of particular value in evaluating the impact of fear or anxiety provoked by the assessment procedures, and the corollary is also true in that fear or anxiety with the evaluation procedure must be considered when interpreting EMG data. Sex Med Rev 2017;-:1e13

CONCLUSION Although it should not be used in isolation, EMG is a useful clinical tool to evaluate PFM tone and function and could help to identify the specific mechanisms associated with dyspareunia. A systematic approach to the evaluation of PFM involvement in dyspareunia should take into account the functional anatomy of the female pelvic floor—where the superficial and deep muscle layers are considered separately—and should involve EMG methods that meet international standards (Figure 2). Further, the confounding influences of biological, psychophysiologic, and psychosocial factors should be considered and controlled where possible. Through the use of accepted standards for the recording and interpretation of PFM EMG, and through the use of a careful systematic approach to the assessment of PFM tone, we

10

McLean and Brooks

can improve clinical outcomes through the decrease of PFM tone in women with dyspareunia. Currently available literature implicates higher than normal tonic activation of the superficial PFMs in dyspareunia, and it appears that heightened excitability of the motoneuron pools of the superficial and deep PFMs also could be implicated. Corresponding Author: Linda McLean, PhD, School of Rehabilitation Science, Faculty of Health Sciences, University of Ottawa, Ottawa, ON, Canada; E-mail: [email protected] Conflicts of Interest: The authors report no conflicts of interest. Funding: None.

STATEMENT OF AUTHORSHIP Category 1 (a) Conception and Design Linda McLean (b) Acquisition of Data Linda McLean; Kaylee Brooks (c) Analysis and Interpretation of Data Linda McLean

7. Goldstein AT, Belkin ZR, Krapf JM, et al. Polymorphisms of the androgen receptor gene and hormonal contraceptive induced provoked vestibulodynia. J Sex Med 2014;11:27642771. 8. Hampson JP, Reed BD, Clauw DJ, et al. Augmented central pain processing in vulvodynia. J Pain 2013;14:579-589. 9. Zhang Z, Zolnoun D, Francisco EM, et al. Altered central sensitization in subgroups of women with vulvodynia. Clin J Pain 2011;27:755-763. 10. Pukall CF, Strigo IA, Binik YM, et al. Neural correlates of painful genital touch in women with vulvar vestibulitis syndrome. Pain 2005;115:118-127. 11. Reissing ED, Brown C, Lord MJ, et al. Pelvic floor muscle functioning in women with vulvar vestibulitis syndrome. J Psychosom Obstet Gynecol 2005;26:107-113. 12. Vandyken C, Hilton S. Physical therapy in the treatment of central pain mechanisms for female sexual pain. Sex Med Rev 2017;5:20-30. 13. Dargie E, Pukall CF. Women in “sexual” pain: exploring the manifestations of vulvodynia. J Sex Marital Ther 2016; 42:309-323.

Category 2

14. Bornstein J, Goldstein AT, Stockdale CK, et al. 2015 ISSVD, ISSWSH, and IPPS consensus terminology and classification of persistent vulvar pain and vulvodynia. J Sex Med 2016; 13:607-612.

(a) Drafting the Article Linda McLean; Kaylee Brooks (b) Revising It for Intellectual Content Linda McLean

15. Reissing ED, Borg C, Spoelstra SK, et al. “Throwing the baby out with the bathwater”: the demise of vaginismus in favor of genito-pelvic pain/penetration disorder. Arch Sex Behav 2014;43:1209-1213.

Category 3

16. Sims MJ. On vaginismus. Trans Obstet Soc London 1861; 3:356-367.

(a) Final Approval of the Completed Article Linda McLean; Kaylee Brooks

REFERENCES 1. Pukall CF, Goldstein AT, Bergeron S, et al. Vulvodynia: definition, prevalence, impact, and pathophysiological factors. J Sex Med 2016;13:291-304. 2. American Psychiatric Association. Diagnostic and statistical manual of mental disorders. 5th ed. Arlington, VA: American Psychiatric Publishing; 2013.

17. Thibault-Gagnon S, Morin M. Active and passive components of pelvic floor muscle tone in women with provoked vestibulodynia: a perspective based on a review of the literature. J Sex Med 2015;12:2178-2189. 18. Morin M, Bergeron S, Khalifé S, et al. Morphometry of the pelvic floor muscles in women with and without provoked vestibulodynia using 4D ultrasound. J Sex Med 2014;11:776785. 19. Butrick CW. Pathophysiology of pelvic floor hypertonic disorders. Obstet Gynecol Clin North Am 2009;36:699-705.

3. Bohm-Starke N. Medical and physical predictors of localized provoked vulvodynia. Acta Obstet Gynecol Scand 2010; 89:1504-1510.

20. Butrick CW. Pelvic floor hypertonic disorders: identification and management. Obstet Gynecol Clin North Am 2009; 36:707-722.

4. Gerber S, Witkin SS, Stucki D. Immunological and genetic characterization of women with vulvodynia. J Med Life 2008;1:432-438.

21. Van Lunsen RHW, Ramakers MJ. The hyperactive pelvic floor syndrome (HPFS): psychosomatic and psycho-sexual aspects of hyperactive pelvic floor disorders with co-morbidity of urogynaecological, gastrointestinal and sexual symptomatology. Acta Endosc 2002;32:275-285.

5. Babula O, Danielsson I, Sjoberg I, et al. Altered distribution of mannose-binding lectin alleles at exon I codon 54 in women with vulvar vestibulitis syndrome. Am J Obstet Gynecol 2004;191:762-766.

22. Sinaki M, Merritt JL, Stillwell GK. Tension myalgia of the pelvic floor. Mayo Clin Proc 1977;52:717-722.

6. Tympanidis P, Casula MA, Yiangou Y, et al. Increased vanilloid receptor VR1 innervation in vulvodynia. Eur J Pain 2004; 8:129-133.

23. Faubion SS, Shuster LT, Bharucha AE. Recognition and management of nonrelaxing pelvic floor dysfunction. Mayo Clin Proc 2012;87:187-193. Sex Med Rev 2017;-:1e13

Electromyography and Dyspareunia

11

24. Thibault-Gagnon S. Definitions and basic etiology of the overactive pelvic floor. In: Padoa A, Rosenbaum TY, eds. The overactive pelvic floor. 1st ed. New York: Springer; 2016.

42. Shafik A, El Sibai O. Study of the pelvic floor muscles in vaginismus: a concept of pathogenesis. Eur J Obstet Gynecol Reprod Biol 2002;105:67-70.

25. FitzGerald MP, Kotarinos R. Rehabilitation of the short pelvic floor. I: Background and patient evaluation. Int Urogynecol J Pelvic Floor Dysfunct 2003;14:261-268.

43. Auchincloss C, Thibault-Gagnon S, Graham R, et al. Validity of estimation of pelvic floor muscle activation through transperineal ultrasound imaging in women. Chicago: International Society of Electrophysiology and Kinesiology; 2016.

26. Messelink B, Benson T, Berghmans B, et al. Standardization of terminology of pelvic floor muscle function and dysfunction: report from the Pelvic Floor Clinical Assessment Group of the International Continence Society. Neurourol Urodyn 2005;24:374-380. 27. Glazer HI, Jantos M, Hartmann EH, et al. Electromyographic comparisons of the pelvic floor in women with dysesthetic vulvodynia and asymptomatic women. J Reprod Med 1998; 43:959-962. 28. White G, Jantos M, Glazer H. Establishing the diagnosis of vulvar vestibulitis. J Reprod Med 1997;42:157-160. 29. Glazer HI, Rodke G, Swencionis C, et al. Treatment of vulvar vestibulitis syndrome with electromyographic biofeedback of pelvic floor musculature. J Reprod Med 1995;40:283-290. 30. Gentilcore-Saulnier E, Auchincloss C, McLean L. Electromyography. In: Padoa A, Rosenbaum TY, eds. The overactive pelvic floor. 1st ed. New York: Springer; 2016. p. 175-203. 31. Andrews JC. Vulvodynia interventions—systematic review and evidence grading. Obstet Gynecol Surv 2011;66:299-315. 32. Keshwani N, McLean L. State of the art review: Intravaginal probes for recording electromyography from the pelvic floor muscles. Neurourol Urodyn 2015;34:104-112. 33. Stålberg E, Falck B, Gilai A, et al. Standards for quantification of EMG and neurography. The International Federation of Clinical Neurophysiology. Electroencephalogr Clin Neurophysiol Suppl 1999;52:213-220. 34. Merletti R, Di Torino P. Standards for reporting EMG data. J Electromyogr Kinesiol 1997;7:I-II. 35. Group TS. SENIAM recommendations 2010. Available at: http://www.seniam.org. Accessed May 1, 2016. 36. De Luca CJ. The use of surface electromyography in biomechanics. J Appl Biomech 1997;13:135-163. 37. Shafik A, Doss S, Asaad S. Etiology of the resting myoelectric activity of the levator ani muscle: physioanatomic study with a new theory. World J Surg 2003;27:309-314. 38. Shafik A, Shafik AA, El Sibai O, et al. The response of the corporal tissue and cavernosus muscles to urethral stimulation: an effect of penile buffeting of the vaginal introitus. J Androl 2007;28:853-857.

44. De Luca CJ, Kuznetsov M, Gilmore LD, et al. Inter-electrode spacing of surface EMG sensors: reduction of crosstalk contamination during voluntary contractions. J Biomech 2012;45:555-561. 45. Enck P, Vodusek DB. Electromyography of pelvic floor muscles. J Electromyogr Kinesiol 2006;16:568-577. 46. Sherrington CS. Decerebrate rigidity, and reflex coordination of movements. J Physiol 1898;22:319-332. 47. Taverner D, Smiddy FG. An electromyographic study of the normal function of the external anal sphincter and pelvic diaphragm. Dis Colon Rectum 1959;2:153-160. 48. Capson AC, Nashed J, Mclean L. The role of lumbopelvic posture in pelvic floor muscle activation in continent women. J Electromyogr Kinesiol 2011;21:166-177. 49. Smith MD, Coppieters MW, Hodges PW. Postural activity of the pelvic floor muscles is delayed during rapid arm movements in women with stress urinary incontinence. Int Urogynecol J 2007;18:901-911. 50. McLean L, Normandeau C, Hodder J. The impact of state of bladder fullness on tonic and phasic activation of the pelvic floor muscles in women. J Electromyogr Kinesiol 2016; 27:60-65. 51. Weir JP, Wagner LL, Housh TJ. Linearity and reliability of the IEMG v torque relationship for the forearm flexors and leg extensors. Am J Phys Med Rehabil 1992;71:283-287. 52. Komi PV, Klissouras V, Karvinen E. Genetic variation in neuromuscular performance. Int Z Angew Physiol 1973; 31:289-304. 53. Komi PV, Kaneko M, Aura O. EMG activity of the leg extensor muscles with special reference to mechanical efficiency in concentric and eccentric exercise. Int J Sports Med 1987; 8:S22-S29. 54. Hermens HJ, Freriks B, Disselhorst-Klug C, et al. Development of recommendations for SEMG sensors and sensor placement procedures. J Electromyogr Kinesiol 2000; 10:361-374.

39. Shafik A, Shafik I, El Sibai O, et al. Role of the perineal muscles in micturition. J Pelvic Med Surg 2006;12:19-24.

55. Rainoldi A, Bullock-Saxton J, Cavarretta F, et al. Repeatability of maximal voluntary force and of surface EMG variables during voluntary isometric contraction of quadriceps muscles in healthy subjects. J Electromyogr Kinesiol 2001;11:425438.

40. Shafik A, Shafik I, El Sibai O, et al. Effect of external anal sphincter contraction on the ischiocavernosus muscle and its suggested role in the sexual act. J Androl 2006;27:40-44.

56. Auchincloss CC, McLean L. The reliability of surface EMG recorded from the pelvic floor muscles. J Neurosci Methods 2009;182:85-96.

41. Shafik A, Shafik I, Shafik AA, et al. The cavernoso-anal reflex: response of the anal sphincters to cavernosus muscles’ stimulation. Asian J Androl 2006;8:331-336.

57. Grape HH, Dedering Å, Jonasson AF. Retest reliability of surface electromyography on the pelvic floor muscles. Neurourol Urodyn 2009;28:395-399.

Sex Med Rev 2017;-:1e13

12

McLean and Brooks

58. Pelliccioni G, Scarpino O, Piloni V. Motor evoked potentials recorded from external anal sphincter by cortical and lumbosacral magnetic stimulation: normative data. J Neurol Sci 1997 Jul;149:69-72.

76. Polpeta NC, Giraldo PC, Juliato CRT, et al. Electromyography and vaginal pressure of the pelvic floor muscles in women with recurrent vulvovaginal candidiasis and vulvodynia. J Reprod Med 2012;57:141-147.

59. Brostrom S. Motor evoked potentials from the pelvic floor. Neurourol Urodyn 2003;22:620-637.

77. Van der Velde J, Everaerd W. Voluntary control over pelvic floor muscles in women with and without vaginistic reactions. Int Urogynecol J Pelvic Floor Dysfunct 1999;10:230-236.

60. Brostrom S, Jennum P, Lose G. Motor evoked potentials from the striated urethral sphincter and puborectal muscle: reproducibility of latencies. Clin Neurophysiol 2003;114:18911895.

78. Vodusek D, Janko M, Lokar J. Direct and reflex responses in perineal muscles on electrical stimulation. J Neurol Neurosurg Psychiatry 1983;46:67-71.

61. Shafik A, Shafik A. The “clitoromotor” reflex. Int Urogynecol J 1995;6:329-336.

79. Ashton-Miller JA, Delancey JOL. Functional anatomy of the female pelvic floor. Ann N Y Acad Sci 2007;1101:266-296.

62. Shafik A. Cervico-motor reflex: description of the reflex and role in sexual acts. J Sex Res 1996;33:153-157.

80. Keshwani N, McLean L. Development of a differential suction electrode for improved intravaginal recordings of pelvic floor muscle activity: reliability and motion artifact assessment. Neurourol Urodyn 2012;31:1272-1278.

63. Shafik A. Vagino-levator reflex: description of a reflex and its role in sexual performance. Eur J Obstet Gynecol Reprod Biol 1995;60:161-164. 64. Shafik A. Vagino-puborectalis reflex. Int J Gynecol Obstet 1995;51:61-62. 65. Tuttle LJ, Nguyen OT, Cook MS, et al. Architectural design of the pelvic floor is consistent with muscle functional subspecialization. Int Urogynecol J 2014;25:205-212. 66. Martinez CS, Ferreira FV, Castro AAM, et al. Women with greater pelvic floor muscle strength have better sexual function. Acta Obstet Gynecol Scand 2014;93:497-502. 67. Kanter G, Rogers R, Pauls RN, et al. A strong pelvic floor is associated with higher rates of sexual activity and improved sexual function. J Minim Invasive Gynecol 2014;21:S19. 68. Lowenstein L, Gruenwald I, Gartman I, et al. Can stronger pelvic muscle floor improve sexual function? Int Urogynecol J 2010;21:553-556. 69. Frasson E, Graziottin A, Priori A, et al. Central nervous system abnormalities in vaginismus. Clin Neurophysiol 2009; 120:117-122. 70. Gammoudi N, Affes Z, Mellouli S, et al. The diagnosis value of needle electrode electromyography in vaginismus. Sexologies 2016;25:e57-e60. 71. Engman M, Lindehammar H, Wijma B. Surface electromyography diagnostics in women with partial vaginismus with or without vulvar vestibulitis and in asymptomatic women. J Psychosom Obstet Gynecol 2004;25:281-294. 72. Naess I, Bø K. Pelvic floor muscle function in women with provoked vestibulodynia and asymptomatic controls. Int Urogynecol J 2015;26:1467-1473. 73. Gentilcore-Saulnier E, McLean L, Goldfinger C, et al. Pelvic floor muscle assessment outcomes in women with and without provoked vestibulodynia and the impact of a physical therapy program. J Sex Med 2010;7:1003-1022. 74. Danielsson I, Torstensson T, Brodda-Jansen G, et al. EMG biofeedback versus topical lidocaine gel: a randomized study for the treatment of women with vulvar vestibulitis. Acta Obstet Gynecol Scand 2006;85:1360-1367. 75. Jantos M. Vulvodynia: a psychophysiological profile based on electromyographic assessment. Appl Psychophysiol Biofeedback 2008;33:29-38.

81. Keshwani N, McLean L. A differential suction electrode for recording electromyographic activity from the pelvic floor muscles: crosstalk evaluation. J Electromyogr Kinesiol 2013; 23:311-318. 82. Reissing ED, Binik YM, Khalifé S, et al. Vaginal spasm, pain, and behavior: an empirical investigation of the diagnosis of vaginismus. Arch Sex Behav 2004;33:5-17. 83. Bø K, Finckenhagen HB. Vaginal palpation of pelvic floor muscle strength: inter-test reproducibility and comparison between palpation and vaginal squeeze pressure. Acta Obstet Gynecol Scand 2001;80:883-887. 84. Shafik A, Shafik IA, El Sibai O, et al. A study of the effect of straining on the cavernosus muscles: identification of “straining-cavernosus reflex” and its clinical significance. Andrologia 2008;40:23-28. 85. Shafik A, Shafik IA, Shafik AA, et al. Effect of urethral stimulation on vesical contractile activity. Am J Med Sci 2007;334:240-243. 86. Deindl FM, Vodusek DB, Hesse U, et al. Activity patterns of pubococcygeal muscles in nulliparous continent women. Br J Urol 1993;72:46-51. 87. Vereecken RL, Verduyn H. The electrical activity of the paraurethral and perineal muscles in normal and pathological conditions. Br J Urol 1970;42:457-463. 88. Vodusec D. Neuroanatomy and neurophysiology of the pelvic floor muscles. In: Bø K, Berghmans B, Morkved S, et al., eds. Evidence-based physiotherapy. Pelvic floor. 2nd ed. New York: Elsevier Health Sciences; 2015. p. 40. 89. Kegel AH. Progressive resistance exercise in the functional restoration of the perineal muscles. Am J Obstet Gynecol 1948;56:238-248. 90. Bø K, Larsen S, Oseid S, et al. Knowledge about and ability to correct pelvic floor muscle exercises in women with urinary stress incontinence. Neurourol Urodyn 1988;7:261-262. 91. Bump RC, Hurt WG, Fantl JA, et al. Assessment of Kegel pelvic muscle exercise performance after brief verbal instruction. Am J Obstet Gynecol 1991;165:322-329. 92. Thompson JA, O’Sullivan PB, Briffa NK, et al. Altered muscle activation patterns in symptomatic women during pelvic floor Sex Med Rev 2017;-:1e13

Electromyography and Dyspareunia muscle contraction and Valsalva manouevre. Neurourol Urodyn 2006;25:268-276. 93. Devreese A, Staes F, De Weerdt W, et al. Clinical evaluation of pelvic floor muscle function in continent and incontinent women. Neurourol Urodyn 2004;23:190-197. 94. van der Velde J, Everaerd W. The relationship between involuntary pelvic floor muscle activity, muscle awareness and experienced threat in women with and without vaginismus. Behav Res Ther 2001;39:395-408. 95. Blok BFM, van Maarseveen JTP, Holstege G. Electrical stimulation of the sacral dorsal gray commissure evokes relaxation of the external urethral sphincter in the cat. Neurosci Lett 1998;249:68-70. 96. Holstege G. The emotional motor system in relation to the supraspinal control of micturition and mating behavior. Behav Brain Res 1998;92:103-109. 97. Floyd WF, Walls EW. Electromyography of the sphincter ani externus in man. J Physiol 1953;122:599-609. 98. Huynh HK, Willemsen ATM, Lovick TA, et al. Pontine control of ejaculation and female orgasm. J Sex Med 2013;10:30383048. 99. Prendergast SA, Weiss JM. Screening for musculoskeletal causes of pelvic pain. Clin Obstet Gynecol 2003;46:773782. 100. De Andres J, Sanchis-Lopez N, Asensio-Samper JM, et al. Vulvodynia—an evidence-based literature review and proposed treatment algorithm. Pain Pract 2016;16:204-236. 101. Weiss JM. Chronic pelvic pain and myofascial trigger points. Pain Clin 2000;2:13-18.

Sex Med Rev 2017;-:1e13

13 102. Zoorob D, South M, Karram M, et al. A pilot randomized trial of levator injections versus physical therapy for treatment of pelvic floor myalgia and sexual pain. Int Urogynecol J 2015; 26:845-852. 103. Simons DG, Travell JG, Simons LS. Travell & Simons’ myofascial pain and dysfunction: the trigger point manual. Baltimore: Williams & Wilkins; 1999. 104. Shah JP, Thaker N, Heimur J, et al. Myofascial trigger points then and now: a historical and scientific perspective. PM R 2015;7:746-761. 105. Moseley G. A pain neuromatrix approach to patients with chronic pain. Man Ther 2003;8:130-140. 106. Latremoliere A, Woolf CJ. Central sensitization: a generator of pain hypersensitivity by central neural plasticity. J Pain 2009; 10:895-926. 107. Nguyen RHN, Swanson D, Harlow BL. Urogenital infections in relation to the occurrence of vulvodynia. J Reprod Med 2009;54:385-392. 108. Edgardh K, Abdelnoor M. Vulvar vestibulitis and risk factors: a population-based case-control study in Oslo. Acta Derm Venereol 2007;87:350-354. 109. Prather H, Dugan S, Fitzgerald C, et al. Review of anatomy, evaluation, and treatment of musculoskeletal pelvic floor pain in women. PM R 2009;1:346-358. 110. Schweinhardt P, Kuchinad A, Pukall CF, et al. Increased gray matter density in young women with chronic vulvar pain. Pain 2008;140:411-419. 111. Blok BFM, Holstege G. The neuronal control of micturition and its relation to the emotional motor system. Prog Brain Res 1996;107:113-126.