A Functional and Clinical Reinterpretation of Human Perineal Neuromuscular Anatomy: Application to Sexual Function and Continence

Transcription

1 Clinical Anatomy 29: (2016) ORIGINAL COMMUNICATION A Functional and Clinical Reinterpretation of Human Perineal Neuromuscular Anatomy: Application to Sexual Function and Continence JEFFREY H. PLOCHOCKI, 1 JOSE R. RODRIGUEZ-SOSA, 1,2 BRENT ADRIAN, 1 SAUL A. RUIZ, 1 AND MARGARET I. HALL 1,2 * 1 Department of Anatomy, Arizona College of Osteopathic Medicine, Midwestern, University, N 59th Ave, Glendale, Arizona Department of Anatomy, College of Veterinary Medicine, Midwestern, University, N 59th Ave, Glendale, Arizona Modern anatomical and surgical references illustrate perineal muscles all innervated by branches of the pudendal nerve but still organized into anatomically distinct urogenital and anal triangles with muscles inserting onto a central perineal body. However, these conflict with the anatomy commonly encountered during dissection. We used dissections of 43 human cadavers to characterize the anatomical organization of the human perineum and compare our findings to standard references. We found bulbospongiosus and the superficial portion of the external anal sphincter (EAS) were continuous anatomically with a common innervation in 92.3% of specimens. The superficial transverse perineal muscle inserted anterior and lateral to the midline, interdigitating with bulbospongiosus. The three EAS subdivisions were anatomically discontinuous. Additionally, in 89.2% of our sample the inferior rectal nerve emerged as a branch of S3 and S4 distinct from the pudendal nerve and innervated only the subcutaneous EAS. Branches of the perineal nerve innervated bulbospongiosus and the superficial EAS and nerve to levator ani innervated the deep EAS. In conclusion, we empirically demonstrate important and clinically relevant differences with perineal anatomy commonly described in standard texts. First, independent innervation to the three portions of EAS suggests the potential for functional independence. Second, neuromuscular continuity between bulbospongiosus and superficial EAS suggests the possibility of shared or overlapping function of the urogenital and anal triangles. Clin. Anat. 29: , VC 2016 Wiley Periodicals, Inc. Key words: perineum; external anal sphincter; perineal body; bulbospongiosus; innervation INTRODUCTION Human perineal neuromuscular anatomy has confused anatomists and clinicians since at least the mid- 19 th century when French anatomist and physician Marie Sappey observed that this heavily studied region remained poorly understood (Sappey, 1877). Recently, there has been an effort to accurately describe the anatomical organization of perineal musculature and role of the perineal body (Bogduk, 1996; Myers, 2001; Fritsch et al., 2002; Shafik et al., 2007) and the innervation pattern of perineal muscles (Schraffordt et al., 2004; Vodusek, 2004; Wallner et al., 2007; Grigorescu et al., 2008). Consideration of perineal dysfunction and surgical approaches to this *Correspondence to: Margaret I. Hall; Department of Anatomy, Arizona College of Osteopathic Medicine, Midwestern University, N 59th Ave, Glendale, AZ 85308, USA. mhallx1@ midwestern.edu Received 17 August 2016; Accepted 24 August 2016 Published online 21 September 2016 in Wiley Online Library (wileyonlinelibrary.com). DOI: /ca VC 2016 Wiley Periodicals, Inc.

2 1054 Plochocki et al. TABLE 1. Neuromuscular Patterns of the Human Perineum Females Males Total Deep transverse perineal muscle present 2/12 (16.7%) 18/18 (100%) 20/30(66.7%) Superficial pouch muscles form a continuous sheet 15/16 (93.8%) 24/26 (92.3%) 39/32 (92.9%) Perineal body is the primary attachment 2/15 (13.3%) 1/24 (4.2%) 3/39 (7.7%) site of perineal musculature Inferior rectal nerve not a branch of pudendal nerve 13/14 (92.9%) 20/23 (87.0%) 33/37 (89.2%) Inferior rectal nerve innervates only subcutaneous EAS 13/14 (92.9%) 21/22 (95.5%) 34/36 (94.4%) important anatomical region require accurate descriptions of neuromuscular structure. Despite published attempts to clarify perineal anatomy, incomplete and conflicting descriptions persist in medical texts and clinical references (e.g., Clemente, 2010; Moore et al., 2013; Drake et al., 2014; Netter, 2014; Rohen et al., 2015). In this study, we utilize human cadaveric dissection to fully describe the muscles and nerves of the superficial pouch and anal triangle of the perineum and address conflicting findings of perineal anatomy. We also compare our dissections to basic convention assumed in both health-care dissection teaching laboratories and the assumptions used for surgical and comparative anatomy of the perineum. MATERIALS AND METHODS Donated human cadavers (n 5 43) with a mean age of years at death (SD 12.2; range 49 95) were obtained from the National Body Donor Program (St. Louis, MO, USA) including 27 male and 16 female specimens. The specimens were embalmed through the internal jugular vein with six gallons of fluid, composed of 3% formaldehyde, 4% phenol, 31% glycerin, and 31% water. Cadavers were stored for a minimum of one month before being delivered to be utilized in one of several gross anatomy dissection or prosection courses for medical, Master s, or allied health students. All cadavers were treated in accordance with local and national laws and regulations and their use was approved by Midwestern University. Cadavers with pathologies or other abnormalities that may have affected perineal anatomy were excluded from the study. Dissection of perineal musculature initially followed the protocol set forth by Hall and Walters (2013). In short, with the cadaver supine, the suspensory ligament of the phallus was identified at its attachment to the pubic symphysis and followed to locate the body of the clitoris or the penis. From there, blunt dissection was used to expose the bulbospongiosus, ischiocavernosus, and superficial transverse perineal muscles, along with perineal nerves. Cadavers were then turned prone and fat was dissected from the ischioanal fossa to observe the external anal sphincter (EAS) and the levator ani portion of the pelvic diaphragm and relevant nerve supply. At this point we fully exposed and defined the perineal membrane and its relationship to the perineal muscles and the perineal body. We then transected the perineal membrane to observe the deep transverse perineal muscle. To observe the origin of the nerves supplying the perineum, we removed all abdominopelvic organs and transected the os coxa on one side at the ischial and pubic rami anteriorly and sacroiliac joint posteriorly with a hacksaw to expose the contralateral internal pelvic surface. We defined the anterior sacral rami (S1 S4) exiting from the anterior sacral foramina with blunt dissection and traced and defined the formation of the sacral nerves, including the superior and inferior gluteal nerves, sciatic nerve, posterior femoral cutaneous nerve, pudendal nerve, inferior rectal nerve, nerve to levator ani, nerve to piriformis, nerve to coccygeus, nerve to quadratus femoris, and the distal branches of the plexus including the perineal nerves and the dorsal nerve of the phallus. With the cadaver prone, we identified branches of the pudendal nerve coursing between the sacrotuberous and sacrospinous ligaments at the level of the ischial spine. We then removed the sacrotuberous ligament using small scissors to directly observe any nerves crossing the sacrospinous ligament and traced their course posteriorly to the sacral plexus and anteriorly to their muscular targets. RESULTS Muscles We observed and defined the ischiocavernosus, bulbospongiosus, and superficial transverse perineal muscles in all specimens. Deep transverse perineal muscle was identified in 16.7% of females and 100% of males (Table 1). When muscle fibers were not present in the female, there was a fibrous structure in its place. In 92.9% of cadavers (93.8% of females, 92.3% of males), bulbospongiosus, ischiocavernosus and superficial transverse perineal muscles formed a single, continuous sheet, the medial portion of which enclosed the bulbs of the vestibule or penis and the lateral portion of which enclosed the crura of the phallus (Figure 1). In females, muscles fibers enclosing the bulbs of the vestibule uniformly coursed posteriorly to form the superficial EAS (Figure 1B, right), while in males the anterior-most fibers fanned medially to cover the bulb of the penis, adjoining at a midline raphe, and posterior fibers extended to form the superficial EAS (Figure 1B, left). The lateral portion of the muscle sheet, superficial transverse perineal, originated at the ischial tuberosity and extended medially, its fibers forming a raised bundle that fanned as they approached the midline. These fibers interdigitated with those of bulbospongiosus just lateral to their medial attachments in both males and females.

3 Human Perineal Anatomy 1055 Fig. 1. (A) Traditionally understood human perineal anatomy at the level of superficial EAS, inferior view (left, male; right, female). (B) The results of our dissections (left, male; right, female; insets, corresponding dissections). Note: In both sexes, superficial perineal pouch musculature forms a single sheet and bulbospongiosus is Muscles of the superficial perineal pouch of the urogenital triangle were not continuous with the subcutaneous portion of the external anal sphincter. Fibers of the subcutaneous EAS were separate from those of the superficial EAS with a different fiber orientation. Superficial EAS exhibited fibers with an anteroposterior direction; however, each bundle of subcutaneous fibers originated every few millimeters laterally around the anal orifice to insert onto the skin medial to the orifice, creating a star shape (Figure 2). Likewise, deep EAS, also separated spatially from the superficial portion, displayed a unique fiber direction. Superiorly, the puborectalis portion of pubococcygeus, one of the three muscles that comprise the levator ani muscle, formed the deep EAS, with an anterosuperior-toposteroinferior fiber direction around the deepest part of the anal canal. Muscles of the superficial perineal pouch inserted onto the perineal body in only 7.7% of cadavers (13.3% of females, 4.2% of males). The remaining 92.3% of our sample had a broad posterior attachment that did not converge on the perineal body. continuous with the superficial EAS. ACL, anococcygeal ligament; BS, bulbospongiosus; IC, ischiocavernosus; IT, ischial tuberosity; MR, median raphe; PB, perineal body; PM, perineal membrane; STP, superficial transverse perineal. [Color figure can be viewed at wileyonlinelibrary. com] Instead, the majority of muscle fibers from the bulbospongiosus portion of the superficial perineal muscular sheet continued into the anal triangle to form the superficial EAS. These fibers created an incomplete ring from the anterior part of each bulb of the vestibule/penis to the posterior portion of the anal canal to insert on the anococcygeal ligament (Figures 1 and 2). Nerves In all specimens we identified S1 S4 anterior rami emerging from the anterior sacral foramina. We confirmed that the pudendal nerve is a branch of S2, S3, and S4 in all specimens. However, in 92.9% of females and 87.0% of males, the inferior rectal nerve emerged as a separate branch formed by S3 and S4 anterior rami independent from the pudendal nerve and the pudendal canal. Instead, the inferior rectal nerve passed between the sacrotuberous and sacrospinous ligaments lateral to the pudendal nerve to course medially to the subcutaneous EAS and

4 1056 Plochocki et al. branch of the perineal nerve that pierced the obturator fascia covering the pudendal canal and coursed medially to innervate the superficial portion of the external anal sphincter (Figure 3) and the most superficial portion of the deep layer of the external anal sphincter. A branch of nerve to levator ani pierced the puborectalis muscle to innervate the majority of the deep EAS. Fig. 2. Lateral view of the muscles that act upon the rectum and anal canal. The deep EAS and puborectalis form a continuous muscle. Posterior fibers of the bulbospongiosus portion of the superficial perineal muscle sheet contribute to the superficial EAS to form a sphincter superficial to the deep EAS. The subcutaneous EAS, anchored to the skin, has comparatively gracile muscle fibers perpendicular to the deeper sphincter muscles. ACL, anococcygeal ligament; BS, bulbospongiosus; EAS, external anal sphincter; PR, puborectalis; SF, superficial; Sub, subcutaneous. associated skin. In 94.4% of cadavers, the only portion of the external anal sphincter innervated by the inferior rectal nerve was the subcutaneous layer. In a small subset of our sample the interior rectal provided a minor contribution to the superficial EAS. We confirmed the perineal nerve and dorsal nerve of the phallus were both branches of the pudendal nerve in all cadavers. The dorsal nerve of the phallus emerged from the distal end of the pudendal canal and then traveled superiorly and anteriorly to pierce the perineal membrane and reach the dorsum of the phallus. After giving off the dorsal nerve of the phallus, the perineal nerve courses anteriorly and inferiorly to innervate superficial perineal pouch musculature (Figure 3). We did not find deep and superficial branches of the perineal nerve separating in the urogenital triangle. However, we did find a muscular DISCUSSION Our dissections of the human perineum, comprised of soft tissue spanning the pelvic outlet, conflict with widely utilized anatomical and clinical references that form the basis of medical education. Interestingly, our findings agree with limited descriptions available in the research and surgical literature, yet none of these studies have been incorporated in standard texts. Specifically, the role of the perineal body, the composition of the EAS and its relationship with other urogenital and pelvic floor muscles, and the innervation pattern of perineal musculature remain ambiguous. However, accurate descriptions of the anatomy are important for understanding surgical approaches, repair techniques, the anatomical bases of incontinence and many other clinical factors. The perineal body is traditionally described as a fibromuscular mass that acts as an insertion site for perineal muscles at the intersection of the urogenital and anal triangles. However, during development, fibers from the embryological bulbospongiosus muscle extend to form the superficial EAS (Arakawat et al., 2010). And indeed, most individuals in our sample reflected this embryological pattern, displaying a bulbospongiosus continuous with the superficial EAS, a finding also supported by Shafik et al. (2007). Additionally, septation of the cloaca, the event responsible for the formation of the perineal body, occurs prior to the migration of myogenic precursors that form these perineal muscles, making the perineal body an unlikely major site of attachment (Valasek et al., 2005). Fig. 3. (A) Nerves of the human male perineum, right side (anterior is to the right). (B) Schematic clarifying nerves seen in A. BS, bulbospongiosus; EAS, external anal sphincter; LA, levator ani; N, nerve; PB, perineal body; PM, perineal membrane; SF, superficial. [Color figure can be viewed at wileyonlinelibrary.com]

5 Human Perineal Anatomy 1057 Likewise, our dissections showed the perineal body is not a major attachment site of any perineal muscle. Nonetheless, we found a small number of individuals with perineal muscle attachment to the deepest part of the perineal body. This was more common in females than males, possibly due to the role of the perineal body in maintaining the topographical link between the vagina and the anus and pelvic floor (DeLancey, 1999). However, the clinical significance of sexual dimorphism in perineal body muscle attachment is unclear. For example, stretching of the perineal body during pregnancy does not substantially impact defecatory, urinary or reproductive muscle function (Meriwether et al., 2016). Similarly, surgical dissection through the perineal body does not adversely affect the functions of superficial perineal muscles in either males or females (Kraima et al., 2015). A few anatomical and surgical references, such as Hollinshead (1956), Agur and Moore (2009), and Clemente (2010), contain a range of figures that depict the perineal body in a manner similar to what we found in dissection. However, most represent the perineal body as either the nexus of attachment for the bulbospongiosus, transverse perinei and EAS or as a site of decussating muscle fibers of bulbospongiosus and the EAS (e.g., Standring, 2005; Moore et al., 2013; Drake et al., 2014; Netter and Frank, 2014; Rohen et al., 2015). Some anatomical atlases depict male and female perineal muscles differently, attempting to reflect sex differences found in dissection (Clemente, 2010; Agur and Dalley, 2015; Rohen et al., 2015). Considering the importance of accurate anatomical descriptions that capture the full range of normal anatomical variation for use in clinical settings, anatomical and surgical texts and atlases require revision to include updated information. Our dissections also revealed muscles of the superficial perineal pouch form a continuous sheet in most individuals. We also found these muscles share common innervation from branches of the pudendal nerve. Early anatomical descriptions similarly observed the arrangement of perineal musculature into continuous sheets that formed supportive and sphincteric diaphragms (Henle, 1873; Holl, 1897; Meyer, 1861). However, few modern texts or atlases represent the anatomy in this manner, likely due to regional differences in fiber orientation along with close anatomical relationships with erectile tissues. We agree these factors support the utility of conceptualizing the musculature into distinct muscles; however, the presence of the muscular continuities common in the normal range of human variation should not be overlooked. Conceptualizing the EAS as three layers of a single muscle dates back to at least Santorini (1775). Some modern descriptions also organize the EAS into three muscular portions, including a subcutaneous layer originating from the skin, a superficial layer that is continuous with bulbospongiosus and partially inserting or decussating at the perineal body, and a deep layer described as being formed by, or at least continuous with, puborectalis (Shafik, 1975; Ayoub, 1979; Bogduk, 1996). Our dissections yielded similar anatomical findings. We were able to organize the EAS into three separate muscles based on the relationship of the muscle fibers with skin around the anus in the case of the subcutaneous layer, continuities with bulbospongiosus in the case of the superficial layer, and continuities with levator ani in the case of the deep layer. This is in agreement with MRI and histological data that show only a subcutaneous and superficial portion are easily distinguishable and that the deep portion is continuous with puborectalis (Stoker et al., 2001; Fritsch et al., 2002). The EAS innervation pattern followed the same organization in most individuals in our sample. We observed the inferior rectal nerve entering the surface of the subcutaneous external anal sphincter, while a muscular branch of the perineal branch of the pudendal nerve distributed innervation to the superficial layer and sometimes to part of the deep EAS, and the deep portion formed by puborectalis was innervated by the nerve to levator ani. This innervation pattern is consistent with electromyographic data that distinguish only the subcutaneous and superficial layer during nerve stimulation of the external anal sphincter (Enck and Vodusek, 2006). Electromyographic recordings show stimulation of the nerve to levator ani elicits contraction of puborectalis (deep EAS) independent from the subcutaneous and superficial EAS (Percy et al., 1980). Most anatomical texts show the inferior rectal nerve as a branch of the pudendal nerve. However, in most of our sample, inferior rectal nerve originates independently from the sacral plexus (S3 S4). This common variation has previously been described in the research literature (Grigorescu et al., 2008). Additionally, in agreement with Soga et al. (2007) we regularly found a muscular branch of the perineal nerve coursing along the posterior margin of the perineal membrane to supply superficial EAS. Other investigators have identified similar patterns in the contributions of the nerve to levator ani, pudendal nerve and inferior rectal nerve to muscles of the external anal sphincter (Schraffordt et al., 2004; Wallner et al., 2007). Clinical interventions should strongly consider these variations in perineal nervous supply. Such variations should also be represented in anatomical references. In light of our findings, we suggest several modifications to the current anatomical cannon to include the variations described here. First, the perineal body is a robust, fibrous cutaneous structure that occupies an anatomical plane inferior to the perineal muscles and is not a major site of attachment for perineal muscles in many individuals. Second, the three named muscles of the superficial perineal pouch comprise a single muscle sheet with common innervation and function. Third, the medial portion of the perineal muscle sheet continues to the anal triangle to form the superficial EAS, suggesting these muscles act in concert for the somatic part of erection and fecal continence in males and females and urinary continence in males. Fourth, traditional conceptualization of the EAS as three parts of a single muscle requires revision; the deep EAS is the inferior-most portion of puborectalis (innervated by nerve to levator ani), the superficial EAS is part of the bulbospongiosus portion of the superficial perineal pouch muscle sheet (innervated by perineal nerve), and the subcutaneous EAS

6 1058 Plochocki et al. (innervated by inferior rectal nerve) that, due to its gracility and fiber orientation, plays a minor role in fecal continence. Lastly, S2 S4 anterior rami of the sacral plexus innervate the muscles of the perineum but not solely as branches of the pudendal nerve; inferior rectal is commonly an independent branch of S3 S4 not associated with the pudendal canal. ACKNOWLEDGMENTS The authors would like to thank the cadaveric donors and their families. The authors thank Ashley Bergeron and Edward Nawrocki for access to specimens. We thank Drs. Linda Walters, Christopher Heesy and Aryeh Grossman for useful discussions. We thank Drs. Kathleen Muldoon, Randall Nydam, and Heather Smith for accommodating our dissections. This work was funded by Midwestern University intramural funds. REFERENCES Agur AM, Dalley AF Grant s Atlas of Anatomy. 11th Ed. Philadelphia: Lippincott Williams & Wilkins. 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