Received: 31 May 2021 Revised: 15 November 2021 Accepted: 10 December 2021 DOI: 10.1002/ca.23828 ORIGINAL COMMUNICATION Sciatic nerve movement in the deep gluteal space during hip rotations maneuvers Ramon Balius1,2 | Montse Pujol1,3 | Dolores Pérez-Cuenca4 | Carles Morros4,5 | Antonio Susín6 | Hèctor Corominas7 | Xavier Sala-Blanch5,8 1 Consell Català de l'Esport, Generalitat de Catalunya, Barcelona, Spain Abstract 2 Sports Medicine Department, Clínica We hypothesize that the sciatic nerve in the subgluteal space has a specific behavior Diagonal, Barcelona, Spain during internal and external coxofemoral rotation and during isometric contraction of 3 Facultad de Fisioteràpia, Universitat Internacional de Catalunya, Sant Cugat del the internal and external rotator muscles of the hip. In 58 healthy volunteers, sciatic Vallés, Spain nerve behavior was studied by ultrasound during passive internal and external hip 4 Anesthesiology, Reanimation and Pain rotation movements and during isometric contraction of internal and external rota- Therapy, Clínica Diagonal, Barcelona, Spain 5 Anatomy and Embryology Unit, Faculty of tors. Using MATLAB software, changes in nerve curvature at the beginning and end Medicine, Universitat of Barcelona, Barcelona, of each exercise were evaluated for longitudinal catches and axial movement for Spain 6 transverse catches. In the long axis, it was observed that during the passive internal Math Department, UPC-BarcelonaTech, Barcelona, Spain rotation and during the isometric contraction of external rotators, the shape of the 7 Rheumatology Department, Hospital of the curve increased significantly while during the passive external rotation and the iso- Holy Cross and Saint Paul, Barcelona, Spain metric contraction of the internal rotators the curvature flattened out. During passive 8 Department of Anesthesiology, Hospital Clínic, Barcelona, Spain movements in internal rotation, on the short axis, the nerve tended to move laterally and forward, while during external rotation the tendency of the nerve was to move Correspondence Xavier Sala-Blanch, Department of toward a medial and backward position. During the isometric exercises, this displace- Anesthesiology, Hospital Clínic, University of ment was less in the passive movements. Passive movements of hip rotation and iso- Barcelona, 170, Villarroel Street, 08036 Barcelona, Spain. metric contraction of the muscles affect the sciatic nerve in the subgluteal space. Email: xsala@clinic.cat, xavi.sala.blanch@ Retrotrochanteric pain may be related to both the shear effect of the subgluteus gmail.com muscles and the endoneural and mechanosensitive aggression to which the sciatic nerve is subjected. KEYWORDS hip joint, isometric contraction, pain, rotation, sciatic nerve, ultrasonography 1 | INTRODUCTION Retrotrochanteric or deep gluteal pain has conventionally been related to the sciatic nerve. This nerve can be compromised by pathologies of the piriformis muscle (Barton, 1991; Güvençer et al., 2008; Location where the research was performed: Consell Català de l'Esport, Generalitat de Catalunya, Barcelona, Spain. Smoll, 2010; Steiner et al., 1987), the internal gemelli-obturator This is an open access article under the terms of the Creative Commons Attribution-NonCommercial-NoDerivs License, which permits use and distribution in any medium, provided the original work is properly cited, the use is non-commercial and no modifications or adaptations are made. © 2021 The Authors. Clinical Anatomy published by Wiley Periodicals LLC on behalf of American Association for Clinical Anatomists and the British Association for Clinical Anatomists. 482 wileyonlinelibrary.com/journal/ca Clinical Anatomy. 2022;35:482–491. 10982353, 2022, 4, Downloaded from https://onlinelibrary.wiley.com/doi/10.1002/ca.23828 by Readcube (Labtiva Inc.), Wiley Online Library on [06/06/2023]. See the Terms and Conditions (https://onlinelibrary.wiley.com/terms-and-conditions) on Wiley Online Library for rules of use; OA articles are governed by the applicable Creative Commons License BALIUS ET AL. 483 internus complex (Balius et al., 2018; Filler & Gilmer-Hill, 2009; The high ultrasound machine (TUS-A500 “Aplio 500” 5.0 Plati- Meknas et al., 2003, 2009, 2011; Murata et al., 2009), ischio-femoral num; Canon Medical Systems Corporation; Nasu, Japan) was fitted impingement (Fernández-Hernando et al., 2015; Taneja et al., 2013) with a high-frequency linear array probe (PLT-1005BT linear array, and injuries to the hamstring insertion (Bucknor et al., 2014; frequency range 5–14 MHz). Preset characteristics were a depth of Fernández-Hernando et al., 2015). Since the beginning of the century, 5 cm, with single focus at 1.8 cm and dynamic range of 69%. A video neurodynamics has emerged as a tool for therapeutic and health pur- of the nerve movement was recorded for each exercise trial. The poses. Nowadays, neurodynamic tests and treatments are suitable for video sequence had a capture rate of 30 frames per second. Two rep- all major nerves (Shacklock et al., 2007). The neurodynamic character- resentative frames (beginning and end of the exercise) were manually istics of the sciatic nerve have been evaluated, especially regarding its selected for analysis in each video. A different senior analyst seg- displacement during flexion-extension movements of the hip mented the sciatic nerve manually on the images. (Coppieters et al., 2015), the knee (Coppieters et al., 2015; Ellis In longitudinal captures, the nerve appeared as a band in the et al., 2012), and even the cervical spine (Ellis et al., 2012), but only in ultrasound images (Figure 1a). MATLAB (The MathWorks Inc, Natick, one publication have they been related to coxofemoral rotations MA) software was used first to compute the medial axis of this band (Balius et al., 2018). The behavior of the sciatic nerve at this level has as the representative curve of the nerve and then to calculate its cur- not been studied sufficiently. vature (Alex et al., 2008). The curvature κ of a point P ¼ ðxðtÞ, yðtÞÞ on The objective of the present study was to examine the normal a curve is defined as the inverse of the radius of the circle tangent to longitudinal and transverse behavior of the sciatic nerve in the deep the curve at that Point (A). It can be computed from the coordinate gluteal space during internal and external rotations of the hip and dur- derivatives using the formula ing isometric contractions of both the internal and external rotators, using high-resolution ultrasound. x0 y00  x00 y0 κ ¼ qffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffi  3 , ðAÞ x02 þ y0 2 The curvature of a curve is a good descriptor of its local shape 2 | MATERIAL AND METHOD and allows us to compare the shape of the sciatic nerve between the beginning and end of the motion. A curvature value κ ¼ 0 is associated 2.1 | Participants to indicate a flat curve (a straight line) and nonzero values correspond to proper curves. Positive and negative curvature values correspond A total of 58 healthy volunteers, mainly young athletes, were included to convex or concave parts of the curve, respectively. in the study: 30 men and 28 women, mean age 20.4 ± 7.7 years (range 18–54), height 176.4 ± 8.6 cm, weight 66.6 ± 9.8 kg, body mass index In transverse image capture, the sciatic nerve appeared as an elliptical 21.4 ± 2.4 kg/m2. The participants met the inclusion criteria: they were closed loop in the ultrasound images. MATLAB software was used to seg- healthy, over 18 years old, and had no previous pelvic and/or hip disor- ment it, and its centroid was determined as a representative point on the ders or symptoms suggestive of sciatic nerve dysfunction. Participants nerve in each image. Owing to possible misalignments during movement were excluded if they had a history of major trauma or surgery in the recording, a bone reference point was marked on the ischium lumbar, hip, gluteal, or hamstring enthesis, a negative straight leg raise corresponding to the most lateral edge of the acetabulum (Figure 1b). test, or sciatic nerve impairment. They were also excluded if they had As a result of this segmentation process, a closed elliptical loop any disorder that could alter nervous system functions. represented the cross-section of the nerve, and the centroid of these points was taken as the representative point for the nerve. The initial relative position of the centroid was compared with that at the end of 2.2 | Imaging each rotation movement. The previously acquired bone reference was placed at the origin of the coordinates, enabling the movement Movements of the sciatic nerve were assessed by ultrasound at the between the initial and final positions to be estimated. deep gluteal space. Shape changes between the beginning and end of different neural mobilization exercises were quantified in terms of: (a) the degree of curvature of the nerve in longitudinal view, (b) axial 2.3 | Hip mobilization exercises and evaluation motion in transverse view. An initial short-axis imaging test on the posterior buttock was used to locate the sciatic nerve precisely along Participant set-up. The volunteer was stretched on the examination the obturator internus tendon. Once the nerve was identified, the table in the prone position and their pelvis was secured by straps, leav- probe was rotated until it was located on the long axis. The slice was ing the buttocks free, in order to fix the lumbar area and the pelvis dur- from the point at which the nerve exited below the piriformis muscle ing hip mobilization. The knee was placed at 90 of flexion. Each toward the distal area, covering the gemelli-obturator internus com- participant made a total of four different movements. First, a passive plex and the proximal section of the quadratus femoris. A single exam- external and internal coxofemoral rotation was performed and the angle iner with 25 years' experience in ultrasound conducted all the of rotation was measured using a pendulum goniometer (Basson ultrasound tests. et al., 2015; Vila-Viñas et al., 2014). Subsequently, with an assistant 10982353, 2022, 4, Downloaded from https://onlinelibrary.wiley.com/doi/10.1002/ca.23828 by Readcube (Labtiva Inc.), Wiley Online Library on [06/06/2023]. See the Terms and Conditions (https://onlinelibrary.wiley.com/terms-and-conditions) on Wiley Online Library for rules of use; OA articles are governed by the applicable Creative Commons License 484 BALIUS ET AL. F I G U R E 1 Ultrasound study of the sciatic nerve in the deep gluteal space in the neutral position. (A) Long axis slice distal to the exit of the sciatic nerve below the piriformis muscle. (B) Short-axis slice just above the obturator internus muscle tendon. The images on the left are not processed. The images on the right show the segmented sciatic nerve in yellow; the red cross indicates a reference point on the lateral margin of the acetabulum. (*), sciatic nerve; (+), obturator internus tendon; FH, femoral head; IG, inferior gemellus muscle; ISC, ischium bone; QF, quadratus femoris muscle; ace, acetabulum; SG, superior gemellus muscle; arrow, connective anchor between the sciatic nerve and the obturator internus tendon holding the studied limb at 90 of knee flexion, an external and internal 3 | RE SU LT S coxofemoral isometric strength test was performed, quantifying the force with a “Commander Muscle Tester” (JTECH-Medical; Midvale, When the initial and final measurements for the two curves were USA) and selecting the highest value obtained (Thorborg et al., 2010). compared (Table 1), there were significant differences While these various actions were performed, the behavior of the (p < 0.050e-2) in the amplitude and mean values of each sciatic nerve was assessed by ultrasound in both long and short-axis (Figure 2). The largest difference was for passive internal rotation views. Passive maneuvers were performed at least twice, while iso- (PAS INT ROT), both left and right (Figure 3), and isometric exter- metric maneuvers were performed three times each. The replicate nal rotation (ISO EXT ROT), both left and right, with similar curve with the best ultrasound record was chosen. behaviors (Figure 4). Instead of studying craniocaudal displacement of the sciatic There was no statistically significant relationship between the nerve, we focused on describing the nerve shape during an internal or degree of deformation of the curve and the angle of internal or exter- external rotation of the hip or an isometric contraction of the internal nal rotation of the hip (p = 0.15). In addition, there was no statistical or external rotators. Movements were recorded on the long and short correlation between the deformity of the curve and the isometric con- axes in order to elucidate the conditioning of the overall movement traction strength of the rotators (p = 0.25). and shape of the nerve by surrounding anatomical structures. Initial The transverse movement of the sciatic nerve was studied curve measurements for all participants were compared with the final through short-axis ultrasound imaging tests. Owing to technical prob- measurements on both the long and short axes, after the four specific lems, only 51 of the 58 participants recruited were recorded and movements performed were chosen. finally included. All volunteers showed relative symmetry between the movements of the two hips along both the abscissa and the ordinate (Figure 5). Thus, internal rotation dynamic movements showed that 2.4 | Statistics the sciatic nerve tended to move laterally and forwards, while during external rotation its tendency was to move medially and backward The significances of the curve and movement measurements were (Figure 6). Neural translation movements during isometry (Figure 7) assessed using the Wilcoxon signed-rank test and MATLAB R2018a showed a smaller displacement than during dynamic movements Update 2 software. (Table 2). 10982353, 2022, 4, Downloaded from https://onlinelibrary.wiley.com/doi/10.1002/ca.23828 by Readcube (Labtiva Inc.), Wiley Online Library on [06/06/2023]. See the Terms and Conditions (https://onlinelibrary.wiley.com/terms-and-conditions) on Wiley Online Library for rules of use; OA articles are governed by the applicable Creative Commons License BALIUS ET AL. 485 TABLE 1 Mean and standard deviation (Std) values of the curvature for the initial and final curves (Kappa) corresponding to each movement κ -initial (103) κ -final (103) κ -variation (103) Type of motion Mean Std Mean Std Mean Std R_PAS_EXT_ROT 3.03 1.36 2.17 1.12 0.86 1.53 R_PAS_INT_ROT 3.14 1.45 6.2 2.45 3.06 2.33 R_ISO_EXT_ROT 3.08 1.27 6.3 1.68 3.22 1.98 R_ISO_INT_ROT 2.73 0.93 2.65 1.14 0.08 1.24 L_PAS_EXT_ROT 2.74 1.26 2.17 1.01 0.57 1.57 L_PAS_INT_ROT 2.46 0.83 5.3 1.66 2.84 1.90 L_ISO_EXT_ROT 3.16 1.41 6.02 1.88 2.86 2.37 L_ISO_INT_ROT 2.78 1.22 2.91 2.14 0.13 2.52 Abbreviations: L ISO EXT ROT, left isometric internal rotators; L ISO INT ROT, left isometric internal rotators; L PAS EXT ROT, left passive external rotation; L PAS INT ROT, left passive internal rotation; R ISO EXT ROT, right isometric internal rotators; R ISO INT ROT, right isometric internal rotators; R PAS EXT ROT, right passive external rotation; R PAS INT ROT, right passive internal rotation. F I G U R E 2 Statistical boxplot representation of the curvatures values of the sciatic nerve in all the participants. The curvatures of the initial and final shapes of the nerve are shown for each type of motion. In each box, the central mark (red line) is the median, the edges are the 25th and 75th percentiles, and the whiskers extend to the most extreme data points. Outliers are not considered and are plotted individually (red cross). Significant differences in mean values between the starting and final positions, mainly for the second and third columns. L ISO EXT ROT, left isometric internal rotators; L ISO INT ROT, left isometric internal rotators; L PAS EXT ROT, left passive external rotation; L PAS INT ROT, left passive internal rotation; R ISO EXT ROT, right isometric internal rotators; R ISO INT ROT, right isometric internal rotators; R PAS EXT ROT, right passive external rotation; R PAS INT ROT, right passive internal rotation 10982353, 2022, 4, Downloaded from https://onlinelibrary.wiley.com/doi/10.1002/ca.23828 by Readcube (Labtiva Inc.), Wiley Online Library on [06/06/2023]. See the Terms and Conditions (https://onlinelibrary.wiley.com/terms-and-conditions) on Wiley Online Library for rules of use; OA articles are governed by the applicable Creative Commons License 486 BALIUS ET AL. F I G U R E 3 Long axis study of right sciatic nerve during passive external and internal rotation maneuvers. (A) Initial (left) and final (right) frames for the external hip rotation (R PAS EXT ROT). (B) Sciatic nerve is segmented in yellow. (C) Initial (left) and final (right) frames for the external hip rotation. (R PAS INT ROT) (D) Sciatic nerve is segmented in yellow. (E) Curvature values for the sciatic nerve; red dots are associated with the starting position of the nerve and blue ones with the final position after the motion. Curvature values for both curves over all participants. In the R PAS INT ROT (E-right), it can be seen that the red dots are concentrated near-zero values while the blue ones reach higher values. R PAS EXT ROT, right passive external rotation; R PAS INT ROT, right passive internal rotation F I G U R E 4 Long axis study of the right sciatic nerve during isometric contraction of the external and internal rotators. (A) Initial (left) and end (right) frames for isometric contraction of the external rotators (R ISO EXT ROT). (B) Sciatic nerve is segmented in yellow. (C) Initial (left) and end (right) frames for isometric contraction of the internal rotators (R ISO INT ROT) (D) Sciatic nerve is segmented in yellow. (E) Curvature values for the sciatic nerve. Red dots are associated with the starting position of the nerve and blue ones with the final position after the motion. R ISO EXT ROT, right isometric internal rotators; R ISO INT ROT, right isometric internal rotators There was no statistical correlation between the neural transla- the external rotators (Video S1). Similarly, small displacements of the tion movements and the isometric contraction strength of the rotators sciatic nerve were observed on the axial axis. (p = 0.25). Until recent years, pseudo-sciatica or localized pain in the but- tock, with or without radiation to the thigh, has been related to sciatic entrapment at the level of the piriformis muscle (Piriformis syndrome) 4 | DISCUSSION (Hopayian et al., 2010), especially when the sciatic nerve has a variant anatomy (Poutoglidou et al., 2020). Pecina (1979) found that in 6.15% This study demonstrates that the sciatic nerve is deformed in the of cases the nervus peroneus communis passes between the tendi- deep gluteal space, especially during dynamic coxofemoral internal nous parts of the piriformis, and they considered this variation of rotation movements and even more during isometric contraction of practical significance for the development of “piriformis syndrome.” 10982353, 2022, 4, Downloaded from https://onlinelibrary.wiley.com/doi/10.1002/ca.23828 by Readcube (Labtiva Inc.), Wiley Online Library on [06/06/2023]. See the Terms and Conditions (https://onlinelibrary.wiley.com/terms-and-conditions) on Wiley Online Library for rules of use; OA articles are governed by the applicable Creative Commons License BALIUS ET AL. 487 F I G U R E 5 Short-axis study of the right sciatic nerve during all movements. Each point represents the relative motion between the centroid of the transverse section of the nerve and the anchor point for each participant. The big red marker is the median value of these points. The scale (X, Y) is in millimeters. The movements of the two hips are relatively symmetrical (first row images compared with the corresponding ones in the second row) L ISO EXT ROT, left isometric internal rotators; L ISO INT ROT, left isometric internal rotators; L PAS EXT ROT, left passive external rotation; L PAS INT ROT, left passive internal rotation; R ISO EXT ROT, right isometric internal rotators; R ISO INT ROT, right isometric internal rotators; R PAS EXT ROT, right passive external rotation; R PAS INT ROT, right passive internal rotation F I G U R E 6 Short-axis study of the right sciatic nerve during passive external and internal rotation maneuvers. (A) Initial (left) and end (right) frames for external hip rotation (R PAS EXT ROT). (B) Sciatic nerve is segmented in yellow and the anchor point in red. (C) Initial (left) and final (right) frames for external hip rotation (R PAS INT ROT) (D) Sciatic nerve is segmented in yellow and the anchor point in red. (E) Recorded transverse motion of the sciatic nerve during the different rotation exercises. Each point represents the relative motion between the centroid of the transverse section of the nerve and the anchor point for each participant. The big red marker is the median value of these points. The scales (X, Y) of the plots are in millimeters. R PAS EXT ROT, right passive external rotation; R PAS INT ROT, right passive internal rotation 10982353, 2022, 4, Downloaded from https://onlinelibrary.wiley.com/doi/10.1002/ca.23828 by Readcube (Labtiva Inc.), Wiley Online Library on [06/06/2023]. See the Terms and Conditions (https://onlinelibrary.wiley.com/terms-and-conditions) on Wiley Online Library for rules of use; OA articles are governed by the applicable Creative Commons License 488 BALIUS ET AL. F I G U R E 7 Long axis study of the right sciatic nerve during isometric contraction of the external and internal rotators. (A) Initial (left) and final (right) frames for isometric contraction of the external rotators (R ISO EXT ROT). (B) Sciatic nerve is segmented in yellow. (C) Initial (left) and final (right) frames for isometric contraction of the internal rotators (R ISO INT ROT) (D) Sciatic nerve is segmented in yellow. (E) Recorded transverse motion of the sciatic nerve during the different rotation exercises. Each point represents the relative motion between the centroid of the transverse section of the nerve and the anchor point for each participant. The big red marker is the median value of these points. The scales (X, Y) of the plots are in millimeters. R ISO EXT ROT, right isometric internal rotators; R ISO INT ROT, right isometric internal rotators During internal rotation of the thigh, the piriformis is extended, and Balius et al. (2018) revealed a specific connective anchorage from the tendons of the divided muscle are tightly pressed together, pin- the sciatic nerve to the obturator internus tendon in a cadaver. This ching the nerve between them. This variant was absent in our series, anchorage constrains the behavior of the nerve during passive internal but the sciatic nerve shows a consistent bending behavior that could and external rotation movements of the hip. In the cadaver, and in also, in certain situations, contribute to the appearance of symptoms. 31 healthy volunteers, the sciatic nerve traced a downward curve fol- Nowadays, the origin of pain in the deep gluteal space is more broadly lowing the obturator internus tendon during internal rotation. In con- identified, implicating other hip rotator muscles. Thus, the concept of trast, external hip rotation caused the nerve to stretch. The same the deep gluteal syndrome was proposed (Hu et al., 2021). This behavior was observed in the 58 healthy volunteers in our study increasingly recognized syndrome has changed the classical concept (Figure 8). In addition, high-resolution ultrasound demonstrated the of pyramidal syndrome, elucidating its pathophysiological mechanism. internal sciatic-obturator connective anchorage described by Balius The present article provides a dynamic perspective on the behavior of et al. (2018) in many of our young healthy subjects (Figure 1a). This the normal sciatic nerve during rotation maneuvers of the study also assessed short-axis sciatic nerve behavior and showed that coxofemoral joint, indicating that in future years its evaluation will during internal rotation the obturator tendon anchorage pulls the sci- facilitate the assessment of its possible significance for diagnosing atic nerve outwards and forwards while the external rotation move- pain in the buttock (Hu et al., 2021). ment pulls it in the opposite direction. The neurodynamic characteristics of the sciatic nerve have been A dynamic body movement entails the involvement of several studied mainly at the level of the thigh. Ellis et al. (2012) assessed joints and leads to specific muscle movements, but passive stabiliza- knee extension along with cervical flexion-extension and detected a tion can also be involved. The nervous system is usually ignored. Thus, craniocaudal movement of 2.6 ± 1.4 mm, whereas Coppieters a nerve moves to adapt to body movement and maintains its own et al. (2015) reported displacements of between 3.2 ± 2.1 mm and transmission function (Munne & Pedret, 2018). During daily activities, 17.0 ± 5.2 mm in combined flexion and extension hip or knee move- movements and postures that our body adopts generate tension, ments. Sciatic nerve behavior has also been studied during the compression, and shear forces on the nervous system. Under normal Straight Leg Raise Test (Ridehalgh et al., 2015), resulting in a dis- circumstances, the nervous system has the biomechanical ability to placement of 12.5 ± 1.4 mm. To date, all research has focused on adapt to those forces and continue to perform its functions (Silva joint flexion-extension movements at different levels, but never dur- et al., 2014). The structural organization of the peripheral nerves ing rotation movements. The effect of passive hip rotation on the allows axons to conduct nerve impulses that will facilitate a person's sciatic nerve has only been researched by Balius et al. (2018), who interactions with the environment while directing and tolerating thou- showed that during passive internal rotation the sciatic nerve trans- sands of torso, head, and limb postures (Munne & Pedret, 2018). formed from a straight to a curved structure. In addition, normal sci- The present study shows normal and specific sciatic nerve behav- atic nerve behavior has never been assessed during contraction of ior during isometric contraction of the external and internal rotator the hip rotator muscles. Our study goal was primarily focused on muscles of the hip. External rotators increase their volume by con- those muscles. tracting (specifically the gemelli, the internal obturator, and the 10982353, 2022, 4, Downloaded from https://onlinelibrary.wiley.com/doi/10.1002/ca.23828 by Readcube (Labtiva Inc.), Wiley Online Library on [06/06/2023]. See the Terms and Conditions (https://onlinelibrary.wiley.com/terms-and-conditions) on Wiley Online Library for rules of use; OA articles are governed by the applicable Creative Commons License BALIUS ET AL. 489 TABLE 2 Mean relative displacements values for the initial and final images corresponding to each type of movement Relative x-displacement Relative y-displacement Type of motion Mean Std Mean Std R_PAS_EXT_ROT 0.15 2.05 3.16 4.21 R_PAS_INT_ROT 0.52 2.61 3.12 5.34 R_ISO_EXT_ROT 1.15 2.76 1.34 4.84 R_ISO_INT_ROT 0.53 2.02 0.29 4.21 L_PAS_EXT_ROT 1.09 2.15 2.12 6.66 L_PAS_INT_ROT 0.004 2.04 1.42 3.96 L_ISO_EXT_ROT 1.09 2.37 1.35 5.58 L_ISO_INT_ROT 0.15 1.44 0.24 3.55 Abbreviations: L ISO EXT ROT, left isometric internal rotators; L ISO INT ROT, left isometric internal rotators; L PAS EXT ROT, left passive external rotation; L PAS INT ROT, left passive internal rotation; R ISO EXT ROT, right isometric internal rotators; R ISO INT ROT, right isometric internal rotators; R PAS EXT ROT, right passive external rotation; R PAS INT ROT, right passive internal rotation. F I G U R E 8 Neural translation during hip rotations. (A) Neutral position. (B) External rotation; the tendon of the obturator internus lacks tension and the sciatic nerve relaxes, becoming straighter. (C) Internal rotation; the tendon of the obturator internus and gemelli tightens, followed by the sciatic nerve, which becomes curved. IG, inferior gemellus muscle; OI, obturator internus muscle; P, piriformis muscle; QF, quadratus femoris muscle; SG, superior gemellus muscle; (*), sciatic nerve quadratus femoris), causing the sciatic nerve dorsal to them to bulge Lundborg, 1988; Lundborg & Dahlin, 1996). Keeping the nerve bed to a posterior direction to adapt to the muscle dynamics. In contrast, stretched at 6% for an hour causes a 70% reduction in nerve conduc- the obturator internus tendon, owing to its anatomical arrangement, is tion. The longer this stretch is maintained, the longer complete recov- tensioned in the opposite (anterior) direction. This combination of ery will take, and the more likely side effects are to appear increased volume of the gluteal muscles in the posterior direction with (Lundborg, 1988). It seems reasonable to propose that repeated the tension of the internal obturator tendon in the anterior direction deformation of the sciatic nerve beyond the behavior observed in this increases the sciatic nerve curvature significantly and repeatedly study could produce harmful mechanosensitivity and endoneural deforms it during isometric contraction movements. Conversely, dur- effects. ing isometric contraction of the hip internal rotator muscles, the nerve Most nerves are surrounded by adipose tissue and not in direct tends to stretch (Figure 9). contact with the epimysium of muscle. The microanatomy of succes- This alteration of behavior in response to both excess and deficit sive cross-sections allows those details to be seen. They are not visi- could change the mechanosensitivity and endoneural health of the ble with 8–12 MHz ultrasound probes, which misleadingly show the nerve. Intraneural tissue (axon, endoneurium, and blood vessels) does muscle in direct contact with nerves. This fat is necessary to preserve not have the same flexibility as its interfaces. Consequently, these the nerve's displacement between neighboring structures (muscle, structures have a retracting or rippling arrangement in the rest posi- bone, and joints) by decreasing the friction (Reina et al., 2020). Thus, tion. When a movement is initiated, the endoneurial tissue lengthens there are commonly adaptive changes in the structure of the nerve (Butler & Coppieters, 2007; Paillant, 2003). Sustaining the stretching covering to protect the axons following chronic injuries under normal of the nerve bed and/or exceeding its limits impairs nerve function. A and pathological conditions: increases in the thickness of the perineu- lengthening of 5%–10% impairs small vessel blood flow and 15% rium and epineurium and in the amount of adipose tissue inside and interrupts it (Butler & Coppieters, 2007; Coppieters et al., 2006; outside the nerve, and between the fascicles and within the 10982353, 2022, 4, Downloaded from https://onlinelibrary.wiley.com/doi/10.1002/ca.23828 by Readcube (Labtiva Inc.), Wiley Online Library on [06/06/2023]. See the Terms and Conditions (https://onlinelibrary.wiley.com/terms-and-conditions) on Wiley Online Library for rules of use; OA articles are governed by the applicable Creative Commons License 490 BALIUS ET AL. patients, a hypothesis about the association with retrotrochanteric pain or other pain conditions could be proposed. 5 | CONC LU SION To sum up, the present work reveals the normal behavior of the sci- atic nerve during rotational movements of the hip and (for the first time) during isometric contraction of the rotator muscles of the hip. The assessment of this behavior in pathological situations would allow the pathogenic basis of gluteal pain, which is currently uncertain, to be better understood. F I G U R E 9 Neural translation during isometry. (A) During an CONFLIC T OF INT ER E ST isometric contraction of the internal rotator muscles, the nerve is more tense but the external rotators are relaxed. (B) Conversely, The authors declare no potential conflict of interest. during an isometric contraction of the external rotator muscles, the nerve is highly curved because the muscle has increased in volume INFORMED CONS ENT and the obturator internus tendon is tense, pulling the nerve down Informed consent was obtained from all participants. (i.e., anteriorly) while the muscles push it upward (i.e., posteriorly) OR CID Xavier Sala-Blanch https://orcid.org/0000-0002-9126-0179 paraneural (circumneural) compartments (concentrical fat compart- ment surrounding the nerve). These structural changes undoubtedly RE FE RE NCE S occur along the studied portion of the nerve. It is well known that the Alex, S. M., Hussain, B. Z., & Prabhakaran, D. J. (2008). Engineering mathe- internal microstructure of a trapped nerve is disrupted (echogenicity matics. Pearson Education. Balius, R., Susín, A., Morros, C., Pujol, M., Pérez-Cuenca, D., & Sala- changes, increased sectional area proximal to entrapping areas, alter- Blanch, X. (2018). Gemelli-obturator complex in the deep gluteal ations in neurodynamics, etc.) (Gervasio et al., 2020). The new high- space: An anatomic and dynamic study. Skeletal Radiology, 47(6), resolution ultrasound machines can allow the sciatic nerve to be 763–770. examined accurately in the deep gluteal space. A skilled examiner can Barton, P. M. (1991). Piriformis syndrome: A rational approach to manage- ment. Pain, 47(3), 345–352. easily evaluate the nerve in gray scale, and the specificity can be Basson, A., Olivier, B., Ellis, R., Coppieters, M., Stewart, A., & Mudzi, W. improved by a dynamic evaluation with rotational movements of the (2015). The effectiveness of neural mobilizations in the treatment of hip, which could elucidate the pathogenesis of deep gluteal syndrome. musculoskeletal conditions: A systematic review protocol. JBI Data- On the other hand, the “scissor effect” is classically referenced as base of Systematic Reviews and Implementation Reports, 13(1), 65–75. the cause of sciatic nerve entrapment by passing under the piriformis Bucknor, M. D., Steinbach, L. S., Saloner, D., & Chin, C. T. (2014). Magnetic resonance neurography evaluation of chronic extraspinal sciatica after muscle belly and over the gemelli-obturator internus complex remote proximal hamstring injury: A preliminary retrospective analysis. (Ergun & Lakadamyali, 2010; Fernández-Hernando et al., 2015, 2016; Journal of Neurosurgery, 121(2), 408–414. Pérez-Carro et al., 2016). The present study shows that this effect is Butler, D. S., & Coppieters, M. W. (2007). Neurodynamics in a broader per- more complex than initially described. There is not only a shear effect spective. Manual Therapy, 12(1), 7–8. Coppieters, M. W., Alshami, A. M., Babri, A. S., Souvlis, T., Kippers, V., & between these muscles; the gemelli-obturator internus complex also Hodges, P. W. (2006). Strain and excursion of the sciatic, tibial, and pulls the nerve in the sagittal plane, moving it in the coronal plane, plantar nerves during a modified straight leg raising test. Journal of while the piriformis blocks this movement. Orthopaedic Research, 24(9), 1883–1889. Currently, pain at this level is classed as “deep gluteal pain” Coppieters, M. W., Andersen, L. S., Johansen, R., Giskegjerde, P. K., (Fernández-Hernando et al., 2015, 2016; Kizaki et al., 2020; Martin Høivik, M., Vestre, S., & Nee, R. J. (2015). Excursion of the sciatic nerve during nerve mobilization exercises: An in vivo cross-sectional et al., 2011; Pérez-Carro et al., 2016). This indicates the study using dynamic ultrasound imaging. The Journal of Orthopaedic etiopathogenic complexity of the process and therefore its symptoms and Sports Physical Therapy, 10(10), 731–737. and exploration. In daily clinical practice, it is uncommon for imaging Ellis, R. F., Hing, W. A., & McNair, P. J. (2012). Comparison of longitudinal to reveal any impairment at this level. Therefore, it is first essential to sciatic nerve movement with different mobilization exercises: An know that normal nerve behavior is related to the movements of the in vivo study utilizing ultrasound imaging. The Journal of Orthopaedic and Sports Physical Therapy, 42(8), 667–675. surrounding joints. Once the normal behavior of the sciatic nerve in Ergun, T., & Lakadamyali, H. (2010). CT and MRI in the evaluation of the deep gluteal space is known, we suggest that further studies on extraspinal sciatica. The British Journal of Radiology, 83(993), 791–803. patients with retrotrochanteric pain should be performed (Martin Fernández-Hernando, M., Cerezal, L., Pérez-Carro, L., Abascal, F., & et al., 2014). If nerve motion/shaping is found to differ in symptomatic Canga, A. (2015). Deep gluteal syndrome: Anatomy, imaging, and 10982353, 2022, 4, Downloaded from https://onlinelibrary.wiley.com/doi/10.1002/ca.23828 by Readcube (Labtiva Inc.), Wiley Online Library on [06/06/2023]. See the Terms and Conditions (https://onlinelibrary.wiley.com/terms-and-conditions) on Wiley Online Library for rules of use; OA articles are governed by the applicable Creative Commons License BALIUS ET AL. 491 management of sciatic nerve entrapments in the subgluteal space. Paillant, B. (2003). Etirementsneuroméningés: Etude  d'un cas. Kinésithér Skeletal Radiology, 44, 919–934. Scient, 437, 47–52. Fernández-Hernando, M., Cerezal, L., Pérez-Carro, L., Canga, A., & Prada- Pecina, M. (1979). Contribution to the etiological explanation of the González, R. (2016). Evaluation and management of ischiofemoral piriformis syndrome. Acta Anatomica, 105(2), 181–187. impingement: A pathophysiologic, radiologic, and therapeutic Pérez-Carro, L., Fernandez-Hernando, M., Cerezal, L., Saenz-Navarro, I., approach to a complex diagnosis. Skeletal Radiology, 45, 771–787. Alfonso-Fernández, A., & Ortiz-Castillo, A. (2016). Deep gluteal space Filler, A.-G., & Gilmer-Hill, H. (2009). Piriformis syndrome.Obturator inter- problems: Piriformis syndrome, ischiofemoral impingement and sciatic nus syndrome.Pudendal nerve entrapment.And other pelvic entrap- nerve release. Muscle, Ligaments and Tendons Journal, 21, 384–396. ments. In H. R. Winn (Ed.), Youmans neurological surgery (6th ed., Poutoglidou, F., Piagkou, M., Totlis, T., Tzika, M., & Natsis, K. (2020). Sci- pp. 2447–2455). Saunders. atic nerve variants and the piriformis muscle: A systematic review and Gervasio, A., Stelitano, C., Bollani, P., Giardini, A., Vanzetti, E., & Ferrari, M. meta-analysis. Cureus, 12, e11531. (2020). Carpal tunnel sonography. Journal of Ultrasound, 23(3), Reina, M. A., Boezaart, A. P., Tubbs, R. S., Zasimovich, Y., Fernández- 337–347. Domínguez, M., Fernández, P., & Sala-Blanch, X. (2020). Another Güvençer, M., Akyer, P., Iyem, C., Tetik, S., & Naderi, S. (2008). Anatomic (internal) epineurium: Beyond the anatomical barriers of nerves. Clini- considerations and the relationship between the piriformis muscle cal Anatomy, 33, 199–206. and the sciatic nerve. Surgical and Radiologic Anatomy, 30(6), Ridehalgh, C., Moore, A., & Hough, A. (2015). Sciatic nerve excursion dur- 467–474. ing a modified passive straight leg raise test in asymptomatic partici- Hopayian, K., Song, F., Riera, R., & Sambandan, S. (2010). The clinical fea- pants and participants with spinally referred leg pain. Manual Therapy, tures of the piriformis syndrome: A systematic review. European Spine 20(4), 564–569. Journal, 19(12), 2095–2109. Shacklock, M., Donoso, C. G., & Lo  pez, M. L. (2007). Hacia un enfoque clí- Hu, Y. E., Ho, G. W. K., & Tortland, P. D. (2021). Deep gluteal syndrome: A nico-científico en el diagno  stico con test neurodinámicos (tensio n neu- pain in the buttock. Current Sports Medicine Reports, 20, 279–285. ral). Fisioterapia, 29, 288–297. Kizaki, K., Uchida, S., Shanmugaraj, A., Aquino, C. C., Duong, A., Silva, A., Manso, A., Andrade, R., Domingues, V., Brand~ ao, M. P., & Simunovic, N., Martin, H. D., & Ayeni, O. R. (2020). Deep gluteal syn- Silva, A. G. (2014). Quantitative in vivo longitudinal nerve excursion drome is defined as a non-discogenic sciatic nerve disorder with and strain in response to joint movement: A systematic literature entrapment in the deep gluteal space: A systematic review. Knee Sur- review. Clinical Biomechanics, 29, 839–847. gery, Sports Traumatology, Arthroscopy, 28, 3354–3364. Smoll, N. R. (2010). Variations of the piriformis and sciatic nerve with clini- Lundborg, G. (1988). Intraneural microcirculation. The Orthopedic Clinics of cal consequence: A review. Clinical Anatomy, 23(1), 8–17. North America, 19(1), 1–12. Steiner, C., Staubs, C., Ganon, M., & Buhlinger, C. (1987). Piriformis syn- Lundborg, G., & Dahlin, L. B. (1996). Anatomy, function, and pathophysiol- drome: Pathogenesis, diagnosis, and treatment. The Journal of the ogy of peripheral nerves and nerve compression. Hand Clinics, 12(2), American Osteopathic Association, 87(4), 318–323. 185–193. Taneja, A. K., Bredella, M. A., & Torriani, M. (2013). Ischiofemoral impinge- Martin, H. D., Kivlan, B. R., Palmer, I. J., & Martin, R. L. (2014). Diagnos- ment. Magnetic Resonance Imaging Clinics of North America, 21(1), tic accuracy of clinical tests for sciatic nerve entrapment in the glu- 65–73. teal regio  n. Knee Surgery, Sports Traumatology, Arthroscopy, 22, Thorborg, K., Petersen, J., Magnusson, S. P., & Hölmich, P. (2010). Clinical 882–888. assessment of hip strength using a hand-held dynamometer is reliable. Martin, H. D., Shears, S. A., Johnson, J. C., Smathers, A. M., & Palmer, I. J. Scandinavian Journal of Medicine & Science in Sports, 20(3), 493–501. (2011). The endoscopic treatment of sciatic nerve entrapment/deep Vila-Viñas, M., Bagur-Calafat, M. C., & Girabent-Farrés, M. (2014). gluteal syndrome. Arthroscopy, 27, 172–181. Fiabilidad del gonio  metro pendular para medir las rotaciones cox- Meknas, K., Christensen, A., & Johansen, O. (2003). The internal obturator ofemorales. Fisioterapia, 36, 247–254. muscle may cause sciatic pain. Pain, 104(1-2), 375–380. Meknas, K., Kartus, J., Letto, J. I., Christensen, A., & Johansen, O. (2009). Surgical release of the internal obturator tendon for the treatment of SUPPORTING INF ORMATION retro-trochanteric pain syndrome: A prospective randomized study, Additional supporting information may be found in the online version with long-term follow-up. Knee Surgery, Sports Traumatology, Arthros- of the article at the publisher's website. copy, 17, 1249–1256. Meknas, K., Oddmund, J., & Kartus, J. (2011). Retrotrochanteric sciatica- like pain: Current concept. Knee Surgery, Sports Traumatology, Arthros- copy, 19, 1971–1985. How to cite this article: Balius, R., Pujol, M., Pérez-Cuenca, D., Munne, C., & Pedret, C. (2018). Displacement of the nervous system Morros, C., Susín, A., Corominas, H., & Sala-Blanch, X. (2022). through articular movement by ultrasound. Bibliographic review. Sciatic nerve movement in the deep gluteal space during hip Apunts Medicine de l'Esport, 53, 75–83. rotations maneuvers. Clinical Anatomy, 35(4), 482–491. Murata, Y., Ogata, S., Ikeda, Y., & Yamagata, M. (2009). An unusual cause of sciatic pain as a result of the dynamic motion of the obturator inter- https://doi.org/10.1002/ca.23828 nus muscle. The Spine Journal, 9(6), e16–e18.