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Research article

Median nerve fascicular anatomy as a basis for distal neural prostheses Uwe Planitzer a,b,∗,1 , Hanno Steinke a,1 , Jürgen Meixensberger b , Ingo Bechmann a , Niels Hammer a , Dirk Winkler b a b

Institute of Anatomy, University of Leipzig, Liebigstraße 13, D-04103 Leipzig, Germany Department of Neurosurgery, University of Leipzig, Liebigstraße 20a, D-04103 Leipzig, Germany

a r t i c l e

i n f o

Article history: Received 24 July 2013 Received in revised form 6 November 2013 Accepted 22 November 2013 Available online xxx Keywords: Anatomy Electrical stimulation Median nerve fascicles Prosthesis Rehabilitation

a b s t r a c t Introduction: Functional electrical stimulation (FES) serves as a possible therapy to restore missing motor functions of peripheral nerves by means of cuff electrodes. FES is established for improving lower limb function. Transferring this method to the upper extremity is complex, due to a lack of anatomical data on the physiological configuration of nerve fascicles. Our study’s aim was to provide an anatomical basis for FES of the median nerve in the distal forearm and hand. Methods: We investigated 21 distal median nerves from 12 body donors. The peripheral fascicles were traced back by removing the external and interfascicular epineurium and then assigned to 4 quadrants. Results: A distinct motor and sensory distribution was observed. The fascicles innervating the thenar eminence and the first lumbrical muscle originated from the nerves’ radial parts in 82%. The fascicle supplying the second lumbrical muscle originated from the ulnar side in 78%. No macroscopically visible plexus formation was observed for the distal median nerve in the forearm. Conclusions: The findings on the distribution of the motor branches of the median nerve and the missing plexus formation may likely serve as an anatomical basis for FES of the distal forearm. However, due to the considerable variability of the motor branches, cuff electrodes will need to be adapted individually in FES. Taking into account the sensory distribution of the median nerve, FES may also possibly be applied in the treatment of regional pain syndromes. © 2013 Elsevier GmbH. All rights reserved.

1. Introduction Functional electrical stimulation (FES) serves as a possible therapy for restoring missing functions of peripheral motor nerves by means of cuff electrodes (Hart et al., 2006; Kottink et al., 2007; Mangold et al., 2009; Mann et al., 2011; O’Halloran et al., 2003; Thrasher et al., 2008). Functional deficits can partially be restored by means of FES, supporting the neurologically impaired to regain their independence in everyday activities (Chan et al., 2009; Kottink et al., 2007). A fundamental prerequisite for accomplishing successful FES is the profound anatomical knowledge of the peripheral

Abbreviations: d, dorsal; FES, functional electrical stimulation; FM, flexor muscles of the forearm; FR, flexor retinaculum; MN, median nerve; MTE, muscles of the thenar eminence; n, sample size; p, palmar; PCB, palmar cutaneous branch; r, radial; S, skin; SPA, superficial palmar arch; TE, motor fascicle to the thenar eminence; u, ulnar. ∗ Corresponding author at: Institute of Anatomy, University of Leipzig, Liebigstraße 13, D-04103 Leipzig, Germany. Tel.: +49 341 97 22086; fax: +49 341 97 22009. E-mail address: [email protected] (U. Planitzer). 1 These authors contributed equally to this work.

architecture of the nerve of interest. The reliability of FES depends on this knowledge (Gustafson et al., 2005, 2009, 2012). One possible target of FES is the distal forearm and the palmar aspect of the hand. This region is supplied by the median nerve, which controls the ability to grasp an object and the major function of the thumb (Mumenthaler et al., 2007). The median nerve arises from the ventral roots of the fifth cervical to the first thoracic spinal nerve, originating from the brachial plexus. In the hand, the median nerve has efferent (motor) branches to the muscles of the thenar eminence and to the 2 radial lumbrical muscles. With its sensory branches on the palmar side of the hand, the common or proper palmar digital branches, the median nerve supplies digits 1–3 and the radial side of the fourth: dorsally and distally, the median nerve supplies digits 2–4. The palmar cutaneous branch (PCB) of the median nerve does not run through the carpal tunnel, and is therefore not affected in carpal tunnel syndromes (Mumenthaler et al., 2007). The above-mentioned distribution corresponds to the norm of the median nerve innervation area. There are many variations in the anatomical course of the median nerve in the region of the carpal tunnel and the hand (Davlin et al., 1992; Lanz, 1977). However, the internal structure of the median nerve has been insufficiently described with conflicting results in present

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literature. In the past, the internal anatomy of the peripheral nerves of the upper limb was investigated by means of micro-dissection by some authors (Jabaley et al., 1980; Sunderland, 1945). The focus of these studies was to understand the internal structure to obtain an anatomical basis for improving the outcome of nerve transplantations. The internal plexus formation of peripheral nerves was described, showing that its internal structure is incomparable to the previous conception of a simple cable structure. The fascicle configuration in the median nerve is not parallel as the fascicles change their location within the course of the nerve (Sunderland, 1945). These observations might influence the feasibility of FES at the distal arm by complicating the predictability of the stimulation, which has to be taken into account. The aim of our study has been to describe motor and sensory fascicular topography of the median nerve in the distal forearm to provide an anatomical basis for median nerve stimulation. The following issues were addressed: (A) Where does fascicular plexus formation end for the median nerve and which location of the median nerve is consequently most suitable for selective peripheral nerve stimulation? (B) Can median nerve fascicles be distinguished by macroscopic dissection? (C) How reliable is fascicular distribution, considering the median nerve’s cross-section in the distal forearm? 2. Materials and methods Twenty-one median nerves from 12 body donors (11 left arms and 10 right arms) were investigated at the Institute of Anatomy, University of Leipzig. While alive, all donors had given their informed consent to the donation of their bodies for teaching and research purposes. The mean age of the body donors was 84 (mean) ± 6.32 (standard deviation) years (range 76–95 years). Eight donors (7 left arms, 6 right arms) were female and 4 donors (4 left arms, 4 right arms) were male. Parts of the arms were already dissected in the gross anatomy course. All but one subject was examined in an ethanol–glycerin-fixed state (Hammer et al., 2012), the remaining one in a fresh unfixed condition.

Fig. 1. Depiction of the median nerve fascicles in the forearm in the unfixed condition. (a) In the distal forearm, amounting to the retinaculum, no plexus formation was macroscopically visible and (b) in the antecubital fossa a marked plexus formation (*) was seen.

branches of the median nerve were dissected under magnification. After complete dissection of the distal median nerve branches, we traced back each branch proximally and removed their covering external epineurium. The interfascicular epineurium of the median nerve could now be removed. Tracing back the peripheral fascicles, we then attributed each fascicle to the quadrants (Fig. 2). Doing so, the distal insertion sites of the motor and sensory fascicles could be assigned to the nerves’ cross-sections. 2.3. Statistics

2.1. Specimens in the unfixed condition For determining the location at which plexus formation starts in the median nerve, one right forearm was investigated in the unfixed condition. The external and interfascicular epineurium was removed from the nerve, beginning in the antecubital fossa and then dissecting distally along the nerve toward the carpal tunnel (Fig. 1).

Pearson’s chi-squared test for independent variables was used to investigate equal distribution of the nerve fascicles between the assigned quadrants. P values of 5% or less were considered as statistically significant. 3. Results 3.1. Location of median nerve plexus formation

2.2. Ethanol–glycerin-fixed specimens After removing the arms (n = 20) from the trunk, the PCB of the median nerve was visualized as a landmark. Then, the branching of the median nerve was dissected according to the approach of Bezerra et al. (1986), starting at the branching of the PCB and proximal to the rascetta. The distal forearm and the hand were removed from the arm, proximal to the site where the PCB originates. This complied with a distance of approximately 80 mm from the distal wrist crease (own unpublished results). We then incised the proximal part of the median nerve at the removed distal forearm with a scalpel under 2.3× magnification (C 2.3® binocular loupe, Heine Optotechnik, Herrsching, Germany) to determine its cross-section. The cross-sections were sub-divided into 4 quadrants: palmar radial, palmar ulnar, dorsal ulnar and dorsal radial, respectively. The proximal ending of each branch was fixed with a clamp, representing each of the 4 quadrants. Then the peripheral

In the forearm that was dissected in the anatomically unfixed condition, the median nerve fascicles showed no macroscopically visible plexus formation distal to the antecubital fossa (Fig. 1a). In contrast, a marked plexus formation was observed proximal to the antecubital fossa (Fig. 1b). 3.2. Separation of motor and sensory fascicles The distance between the separation of the PCB and the most distal wrist crease averaged 45 mm (range 16–69 mm). Distinguishing motor from sensory fascicles was possible by determining the insertion sites of the nerve. When assigning the fascicles to the 4 quadrants, all of them originated from 1 quadrant or from 2 adjacent quadrants. Eight combinations of fascicle origin were seen: (1) radial palmar, (2) radial dorsal, (3) ulnar palmar, (4) ulnar dorsal, (5) radial and ulnar palmar, (6) radial and ulnar dorsal, (7) radial

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Fig. 2. Fascicular organization of the median nerve in the distal forearm and hand. (a) An overview of the forearm and hand is shown from the ventral and palmar aspect after removing the skin. The flexor muscles of the forearm can be seen prior to the dissection of the median nerve. FM, flexor muscles of the forearm; FR, flexor retinaculum; MTE, muscles of the thenar eminence; S, skin; asterisks, sensory branches of the median nerve, (b) peripheral fascicles were traced back by removing external and interfascicular epineurium and assigned to one or two of the four quadrants. MN, median nerve; MTE, muscles of the thenar eminence; PCB, palmar cutaneous branch; SPA, superficial palmar arch; black arrow, motor fascicle supplying the thenar eminence; asterisks, sensory branches, and (c) the median nerve cross-section was sub-divided into 4 quadrants, illustrated in different colors. Yellow, radial palmar; green, ulnar palmar; red, ulnar dorsal; blue, radial dorsal. (For interpretation of the references to color in this figure legend, the reader is referred to the web version of the article.)

palmar and dorsal as well as (8) ulnar palmar and dorsal. In the 2 hands that had been dissected previously, several of the median nerve fascicles could not be shown. Only the fascicles of the index and ring finger could be depicted in all 20 donors. 3.3. Distribution of motor fascicles The branch of the thenar eminence was shown in 17 of 20 hands, including the motor fascicles of the opponens pollicis muscle, the abductor pollicis brevis muscle and the superficial head of the flexor pollicis brevis muscle. Fascicular distribution was not equally distributed (p < 0.05). The majority originated from the nerves’ radial quadrants. In 35% (6/17) of the hands studied, the fascicle originated from radial dorsal, in 29% (5/17) of the hands from radial palmar and dorsal and in 18% (3/17) of the hands from radial palmar (Fig. 3). In the other cases, the fascicular location was ulnar dorsal (12%; 2/17) or radial and ulnar palmar (6%; 1/17). The first lumbrical muscle, with its supplying nerve fascicle, was dissected in 17 of the 20 hands and the second lumbrical muscle in 18 of the 20 hands. The locations of these fascicles were also not equally distributed (p < 0.001). The fascicle supplying the first

lumbrical muscle originated most frequently from the radial dorsal quadrant (53%; 9/17) and from the radial palmar quadrant (29%; 5/17). In 12% (2/17) of the hands, the fascicle supplying the first lumbrical muscle originated from the ulnar dorsal quadrant and, in 6% (1/17), from radial and ulnar dorsal (Fig. 3). The origin of the second lumbrical fascicle was mostly located on the ulnar dorsal side (56%; 10/18). The ulnar palmar (17%; 3/18) or radial dorsal (17%; 3/18), ulnar palmar and dorsal (5%; 1/18), and the radial palmar (5%; 1/18) origins were less frequent (Fig. 3). In 9 of the 17 hands (45%), the third lumbrical muscle was also innervated by median nerve fascicles, which then always originated from ulnar palmar. No gender- or side-related differences were observed. 3.4. Distribution of sensory fascicles All sensory fascicles could be depicted in 16 of the 20 hands in the ethanol–glycerin-fixed condition. The locations of the sensory fascicles were also not equally distributed (p < 0.01). A detailed distribution of all sensory fascicles is shown in Fig. 4 and the supplementary material. The assignment of the PCB was described as an example of a sensory fascicle. The fascicle originated mostly from

Fig. 3. Pattern of topographic distribution of median nerve motor fascicles. The median nerve was sectioned in 2 palmar (radial and ulnar) and 2 dorsal (radial and ulnar) quadrants each, according to black lines in the oval. The motor fascicles were assigned to the quadrants. The size of the squares represents the frequency of the observed fascicles’ locations and their ratios are given [%]. d, dorsal; n, sample size; p, palmar; r, radial; u, ulnar.

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Fig. 4. Pattern of topographic distribution of median nerve sensory fascicles. The median nerve was sectioned in 2 palmar (radial and ulnar) and 2 dorsal (radial and ulnar) quadrants each, according to black lines in the oval. The sensory fascicles were assigned to the quadrants. The size of the squares represents the frequency of the observed fascicles’ locations and their ratios are given [%]. The numeric values are rounded to one decimal with the result that the numeric values partially vary from 100. (a) Palmar cutaneous branch (PCB) and thumb, (b) index finger, (c) middle finger, (d) ring finger and communicating branch of median nerve with ulnar nerve. d, dorsal; n, sample size; p, palmar; r, radial; u, ulnar; asterisk, the missing sample was supplied by the ulnar nerve.

the radial palmar side (83%; 15/18), followed by the radial palmar and dorsal side, the radial and ulnar palmar side and the ulnar dorsal side (each 6%; 1/18). 4. Discussion This macroscopic study investigated the fascicular anatomy of the human median nerve in the distal forearm and the hand. The aim has been to describe the location of both motor and sensory fascicles as a basis for possible neural prostheses in the upper extremity. 4.1. The absence of fascicular plexus formation in the distal median nerve suggests its suitability for FES An internal plexus formation is a major limitation to reliable prediction of the transmission of an electrical impulse along the nerve. A marked plexus formation was observed in the forearm previously, but the distances without fascicular branching were discrepant in these studies, likely due to methodological problems

(Mumenthaler et al., 2007). Mumenthaler and coworkers describe a distinct plexus formation using a surgical microscope in the forearm, which can be confirmed with our data. In the unfixed specimen that was investigated in our study, plexus formation ends in the antecubital fossa. Further distally, the fascicles are organized in a parallel manner. It can therefore be concluded that the region distal to the antecubital fossa is suitable for median nerve stimulation by means of FES. 4.2. Median nerve fascicles can be distinguished by macroscopic dissection The fascicles that arise from the median nerve can likely be distinguished by macroscopic dissection. After preparing the different fascicles peripherally, it is possible to trace them back to any level of the forearm and to assign them to the previously described quadrants. A macroscopic distinction can be made for the motor and sensory fascicles, starting the preparation as distally as possible. An exclusive stimulation of the particular motor fascicles without affecting the sensory ones is the goal of the stimulation

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procedure to selectively improve motor function. One issue is the surgical accessibility of the median nerve here. The division of the motor branch from the median nerve toward the thenar eminence is very distal (Lanz, 1977). Also, it is often located next to the superficial palmar arch (Fig. 2b). As a consequence, the risk of a nerve lesion would be disproportional. It is therefore of principal interest to know the fascicular distribution as accurately as possible in the most approachable area, which was the issue of our study on 20 forearms. 4.3. Median nerve fascicle distribution follows a regular pattern in the distal forearm The cross-section of the median nerve was separated into four quadrants to provide a geometrical basis for investigating its fascicles and their variations. This concept was successfully used to describe the fascicle distribution of the motor and sensory branches by means of statistical analyses. The results of our study confirm that fascicle distribution of the median nerve in the distal forearm is reliable, providing the anatomical basis for FES of the distal median nerve. Former studies investigated the course and position of the median nerve in the carpal tunnel (Lanz, 1977; Mackinnon and Dellon, 1988) and reported that the motor fascicles are mostly located radially. Mackinnon and Dellon found out that the motor fascicle is located palmar radial in 78% and centrally in 22% of all patient cases investigated by them (Mackinnon and Dellon, 1988). Their findings can be partially confirmed by our findings in body donors (Fig. 3): in 82% of our cases, the thenar branch originated from the radial parts of the nerve. We additionally observed dorsal palmar and ulnar origins of the motor fascicles, which complies with the findings of Lanz (1977). Mackinnon and Dellon reported that the “fascicles directly under the site of compression would be more likely to suffer a greater degree of change than located away” (Mackinnon and Dellon, 1988). They therefore concluded that if the motor fascicles are located palmar, they will more likely be predisposed to compression by the carpal ligaments, as compared to the dorsal location. In our findings, the motor branches of the median nerve tended to be located radially, which should be taken into account when planning FES. 4.4. Clinical implications Our findings provide an anatomical basis for median nerve stimulation. We can confirm that the distal branches of the median nerve are represented by distinct fascicles, as previously described for the nerves of the lower limb (Gustafson et al., 2005). The best location for nerve stimulation by means of cuff electrodes on the median nerve is the result of the identification of the fascicles of interest and their surgical accessibility. For the distal part of the median nerve, the most suitable anatomical location can be found in the region between the distal wrist crease and the antecubital fossa. Knowing the topographic distribution of sensory fascicles in more detail may also be useful for the treatment of chronic regional pain syndromes (Mirone et al., 2009). Furthermore, the interaction of motor and sensory function of the hand is another important issue with respect to its functionality (Mumenthaler et al., 2007). Our study has several limitations. First, the median nerve quadrants were defined artificially by incising the cross-sections with a scalpel under magnification, which complicated the attribution of the fascicle of interest to 1 of the 4 quadrants in some cases. By means of this definition, the distribution to the adjacent quadrants is explainable. Second, our data was exclusively derived from macroscopic dissections and does not provide histological validation for our findings. Third, a larger sample size would help to

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substantiate our findings and to determine possible statistical correlations. Unfortunately, it was impossible to get the same number of cases for all fascicles. However, we wanted to keep the number of specimens as high as possible. Furthermore, other factors influencing the stimulation effects were not considered in this study, such as proprioception, which may form the content of future studies. 4.5. Conclusions and outlook The aim of this study was to deepen the understanding of distal median nerve fascicular anatomy against the background of electrical nerve stimulation. FES may be applied to the distal forearm due to the missing plexus formation within the median nerve. However, our findings on the variation of median nerve fascicle locations indicate that every electrode should be tested and calibrated individually. A distinct fascicle distribution was found at the median nerve cross-section in both motor and sensory fascicles. These findings may be useful for FES to improve an impaired median nerve function. The use of nerve cuff electrodes in the distal forearm would minimize the danger of damaging the distal branches of the median nerve. Furthermore, unwanted side effects of the stimulation of sensory fascicles could be minimized, taking into account the most likely position. Conflicts of interest None to report. Acknowledgements St. Jude Medical provided financial support for this study. The authors would like to thank Maria Schaebs, Matthias Oehme, Philipp Pieroh and Thomas Wolfskämpf for supporting the authors in anatomical dissection related to this study. Christine Auste took the pictures. Andreas Hinz provided support in statistics and Gustav Preller in proofreading. Appendix A. Supplementary data Supplementary data associated with this article can be found, in the online version, at http://dx.doi.org/10.1016/j.aanat.2013. 11.002. References Bezerra, A.J., Carvalho, V.C., Nucci, A., 1986. An anatomical study of the palmar cutaneous branch of the median nerve. Surg. Radiol. Anat. 8, 183–188. Chan, M.K.-L., Tong, R.K.-Y., Chung, K.Y.-K., 2009. Bilateral upper limb training with functional electric stimulation in patients with chronic stroke. Neurorehabil. Neural Repair 23, 357–365. Davlin, L.B., Aulicino, P.L., Bergfield, T.L., 1992. Anatomical variations of the median nerve at the wrist. Orthop. Rev. 21, 955–959. Gustafson, K.J., Grinberg, Y., Joseph, S., Triolo, R.J., 2012. Human distal sciatic nerve fascicular anatomy: implications for ankle control using nerve-cuff electrodes. J. Rehabil. Res. Dev. 49, 309–321. Gustafson, K.J., Pinault, G.C.J., Neville, J.J., Syed, I., Davis, J.A., Jean-Claude, J., Triolo, R.J., 2009. Fascicular anatomy of human femoral nerve: implications for neural prostheses using nerve cuff electrodes. J. Rehabil. Res. Dev. 46, 973–984. Gustafson, K.J., Zelkovic, P.F., Feng, A.H., Draper, C.E., Bodner, D.R., Grill, W.M., 2005. Fascicular anatomy and surgical access of the human pudendal nerve. World J. Urol. 23, 411–418. Hammer, N., Löffler, S., Feja, C., Sandrock, M., Schmidt, W., Bechmann, I., Steinke, H., 2012. Ethanol–glycerin fixation with thymol conservation: a potential alternative to formaldehyde and phenol embalming. Anat. Sci. Educ. 5, 225–233. Hart, D.J., Taylor, P.N., Chappell, P.H., Wood, D.E., 2006. A microcontroller system for investigating the catch effect: functional electrical stimulation of the common peroneal nerve. Med. Eng. Phys. 28, 438–448. Jabaley, M.E., Wallace, W.H., Heckler, F.R., 1980. Internal topography of major nerves of the forearm and hand: a current view. J. Hand Surg. Am. 5, 1–18.

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Median nerve fascicular anatomy as a basis for distal neural prostheses.

Functional electrical stimulation (FES) serves as a possible therapy to restore missing motor functions of peripheral nerves by means of cuff electrod...
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