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Okajimas Folia Anat. Jpn., 72(1): 29-36, May, 1995

An Anatomical Analysis of the Dorsoventral Relationship between the and the Pudendal in Man by Use of Computer Aided Three-Dimensional Reconstruction

By

Keiichi AKITA and Hitoshi YAMAMOTO

Department of Anatomy, School of Medicine, Tokyo Medical and Dental University, 1-5-45 Yushima, Bunkyo-ku, Tokyo, 113, Japan

-Received for Publication, January 30, 1995-

Key Words: , Sacral Plexus, 3-D reconstruction, Human gross anatomy

Summary: In order to investigate the dorsoventral relationship between the sacral plexus and the pudendal nerve in man, morphological examination was performed on one pelvic half of a male cadaver. The second and third spinal were removed en bloc and sectioned serially for three-dimensional reconstruction imaging of the selected sections. Comparison of the sequential images revealed that the root of the pudendal nerve is first situated ventral to the caudal root of the sacral plexus, and that the former and the latter are shifted cranialward and caudalward, respectively, at the point of exit from the second anterior sacral .

Abbreviation (Macaw mulatta) in order to determine the detailed relationships between the innervation of the pelvic Bis nerveto the short head of the bicepsfemoris limb and the pelvic outlet muscles. These findings Br (ex. Br1) branchof the spinalnerve revealed that the origins of the pudendal nerves Cfp posteriorfemoral cutaneous nerve were situated ventrocaudal to the sacral plexus. Co nerveto the coccygeus D dorsalprimary rami The present study was undertaken to confirm the Fx femoralflexor nerve dorsoventral relationship between the sacral plexus Gi inferiorgluteal nerve and the pudendal nerve in man by using computer Gs superiorgluteal nerve aided three-dimensional reconstruction imaging of La nerveto the levatorani serial sections of the second sacral nerve. Oi nerveto the obturatorinternus Per commonperoneal nerve Pud pudendalnerve Qf nerveto the quadratusfemoris Materials and Methods Sx rootof the sacralplexus Tib tibialnerve The right pelvic half of a male cadaver, typically fixed and preserved for dissection practice (10% formalin and 30% alcohol), was used for this study. The nerves innervating the muscles of the pelvic In this specimen, 24 presacral vertebrae (C7, Th12, outlet in man principally arise from the pudendal L5) were found. In the dissection procedure, in plexus. Although the pudendal plexus has close con- order to obtain detailed data of the segmental com- nections with the sacral plexus which sends primary position of the sacral and pudendal plexuses, the nerves to the pelvic limb, the stratificational relation- bony elements were completely removed. After ship (Akita et al. 1992a) between the sacral plexus identification of the main branches of both plexuses, and pudendal plexus in man remains unclear. In the plexuses were removed for detailed examination. previous studies (Akita 1992a ,b; Akita et al. , 1992b, The second and third sacral spinal nerves (Fig. 1) 1995), minute dissection was performed on Lacertilia were embedded en bloc in paraffin, and then serially (Iguanidae Iguana iguana and Varanus dumerillii), sectioned into 10 lim thick sections. The sections Urodele (Cryptobranchidae Megalobatrachus japo- were stained with hematoxylin-eosin. All sections nicus), Ayes (Gallus gallus domesticus) and mammals were photographed and traced; the branches of each

29 30 K. Akita and H. Yamamoto section were then identified. In order to obtain the The nerve trunk was divided into a few branches reconstruction image, sections at about every 1000inn (Fig. 2a). In this section, the dorsal primary ramus were selected and scanned by a Sharp JX-220 color was not divided. The nerve to the coccygeus arose image scanner on a NEC PC-9801RXmicrocomputer from the caudal surface of the branch designated and an Astrodesign VP-1125 video CG system. here as number 5 (Br5). The dorsal primary rami Sequences of the selected 36 sections were recon- arose from the dorsal region of Br5 (Fig. 2b). After structed using Ratoc System Engineering TRI/P soft- the primary dorsal ramus was given off, the nerve ware. Compiled images were photographed directly trunk was composed of four large branches and two from a Sony PVM-1442Q color video monitor. small branches (Fig. 2c). Brl and Br3 were united forming Brl + 3. Brl + 3, Br2 and Br4 moved caudal- ward, and Br4 shifted dorsalward. Br6 as well arose Results from the dorsal region of Br5. As seen in Figure 2d, Brl + 3, Br2 and Br4 became divided into small Segmental composition of the nerves from the sacral branches and shifted more caudalward. Br6 ran and pudendal plexuses caraniodorsalward, and was craniocaudally divided In the examination of the ventral primary rami of into two branches. The nerves to the L4 to 54, the sacral plexus was found to extend arose from S3 and ran on the ventral surfaces of the between L4 and 52, and the pudendal plexus between branches of S2; Br5 was then divided into three S2 and S4. branches (Fig. 2e). The branches from S3 ran cranial- The superior gluteal nerve arose from the dorsal ward and fused with the branches from S2. surface of L4, L5 and 51 as their proximalmost dorsal branches. The roots of the inferior gluteal Three-dimensionalreconstruction (Fig. 3) nerve arose from the dorsal surfaces of the union of In order to elucidate the spatial course of the L4 and L5 and Si. The nerves to the piriformis arose main branches of the second , three- from the caudalmostroots of the superior and inferior dimensional reconstruction images of the nerve were gluteal nerves. The was obtained. Sections from approximatelyevery 1000 formed by the union of the dorsal trunks of L4 and interval were selected from the union of the ventral L5 and the dorsal trunk of Si. The ventral divisions and dorsal roots of the spinal nerve. The branches of L4 to 52 united to form the . Muscular are colored according to their final destinations. branches to the posterior muscles of the thigh [the The dorsal primary rami (blue) branched off femoral flexor nerve (Eisler, 1891, 1892)1 arose from dorsalward. The pudendal nerve (yellow) arose from the ventral surface of the tibial nerve. The nerve to the ventral surface of the main trunk of the second the quadratus femoris arose from the ventral surfaces spinal nerve, and ran caudalward. Br5 (red) gave off of the union of L4 and L5, and Si. The nerve to the some branches, ran slightlycranialward, and formed obturator internus, which arose from the ventral the caudal root of the sacral plexus. Br6 (sky blue) surfaces of Si and S2, was situated more caudal than ran craniodorsalward and became branches of the the quadratus femoris nerve. posterior femoral cutaneous nerve. At the point of The pudendal nerve was formed by S2, S3 and S4; exit from the anterior sacral foramen (Fig. 3d), the the dorsal nerve of arose from S2 and 53 as a pudendal nerve (yellow) was situated caudal to the ventral branch of the pudendal nerve. The perinea] sacral plexus (red). nerve and the inferior rectal nerve did not appear to be divided. The nerves to the levator ani arose from the ventral surfaces of S3 and 54, and those to the Discussion coccygeus arose from the dorsal surfaces of S2 and S3. The pelvic splanchnic nerve arose as the ventral- The sacral plexus and the pudendal plexus are most nerve of S3. The roots of the posterior femoral generally regarded as the nerve complexes which cutaneous nerve arose from the dorsal roots of the innervate the muscles of the primary inferior limb , the common peroneal nerve and the muscles of the pelvic outlet, respectively. and the tibial nerve. Although numerous reports have discussed the seg- mental composition of the sacral and pudendal Serial sections of the trunk of the second sacral nerve plexuses in man (e.g. Eisler 1891, 1892; Bardeen and As the second sacral nerve is involved in both the Elting 1901a,b; Nakanishi 1967a,b; Takahashi 1980; sacral and pudendal plexuses, this nerve was chosen Sato 1980), few have included a description of the for the three-dimensional analysis. Figure 2 shows dorsoventral relationship between these two plexuses. sequential sections of the second sacral nerve. The In previous comparative anatomical studies (Akita points of sectioning are indicated in Figure 1. 1992a,b; Akita et al. 1992b, 1995), we reported that 3-D Reconstruction of Second Sacral Nerve 31 the pudendal nerve (or the nerve which is -homolo- could be schematicallydemonstrated (Fig. 4). Based gous to the pudendal nerve) is situated caudoventral on the present three-dimensionalreconstruction (Fig. within the sacral plexus. Akita eta!. (1992a)proposed 4a), the root of the pudendal nerve (yellow in Fig. 3) that the stratificational relationship within the limb is first situated ventral to the caudal root of the sacral plexus is one of the most fundamental features in plexus (red in Fig. 3). Gradually, the former shifts limb formation, and this relationship is common dorsocaudalward and the latter shifts ventrocranial- to each species. Kida (1990) speculated that nerve ward (Fig. 4b). The roots of the sacral plexus and the branching pattern is, at least, well associated with a pudendal nerve shift cranialward and caudalward, certain relationship between innervation and muscle respectively, at the point of exit from the second phylogeny on the basis of findingsobtained by typo- anterior sacral foramen (Fig. 4c). Therefore, both logical anatomy. And Kida and Ishida (1988) called roots changed their relative positions within the trunk the relationship "corrected nerve-musclespecificity". of the second spinal nerve in the . The dorso- Tani et al. (1994) reported that the ramification ventral relationship of these two roots is similar in pattern of the intercostal nerve appears to correspond various species (Akita 1992a,b; Akita et al. 1992b, with the arrangement of motoneuron pool in the 1995). ventral horn of the thoracic and lumbar . Kida (1987) performed a minute investigation of Therefore, the dorsoventral ramificationpatterns of the third and fourth cervical nerves (C3 and C4) the spinal nerves is one of the most fundamental using a macroscopical fiber analysis method. He elements in trunk and limb formation. reported that the cutaneous nerves in C3 and C4 In this study, the positional relationships between display at least two kinds of torsion before and after the roots of the sacral plexus and the pudendal nerve the , and that it is necessary to inves- tigate the whole length of the spinal nerve in order to explain the true dorsoventral relationships among the branches of a spinal nerve. Although the torsions of the nerve fibersof the second sacral nerve remain unclear, the positional relationships of the main branches can be revealed easily by using three- dimensional reconstruction of serial sections. Figure 5 shows the schematic representation of

Fig. 4. Schematic representation of the shift of the main branches of the second spinal nerve. a) at first the main branches are dorsoventrally arranged, b) the root of the pudendal nerve shifts caudodorsally, and the root of the sacral plexus shifts Fig. 5 Schematic representation of the stratificational relation- cranioventrally, c) at the point of exit from the anterior ships among the branches of the sacral and pudendal sacral foramen, both roots are craniocaudally arranged. plexuses in this specimen (male. right) (ventral aspect). 32 K. Akita and H. Yamamoto the stratificational relationship of the sacral and among the main nerves from the dorsal division of the sacral pudendal plexuses of the present specimen. The plexus and the innervation of the piriformis. Anat Rec stratificational relationship of the dorsal division of 1992a;233:633-642. 4) Akita K, Sakamoto H, Sato T. Muscles of the pelvic outlet the sacral plexus was proposed in Akita et al. (1992a). ill the fowl (Gallus gallus domesticus) with special reference Sato (1980) proposed the positional relationship to their nerve supply. J. Morph 1992b;214:179-185. among the branches of the pudendal plexus; 1) the 5) Akita K, Sakamoto H, Sato T. Muscles of the pelvic outlet nerves to the levator ani, ventral, 2) the pudendal in the rhesus monkey (Macaca mulatta) with special refer- nerve, middle, and 3) the nerves to the coccygeus, ence to their nerve supply. Anat Rec 1995;241:273-283. 6) Bardeen CR, Elting AW A statistical study of the variation dorsal. In the present specimen, the nerve to the in the formation and position of the lumbo-sacral plexus in coccygeus in S2 arose from the caudal surface of Br5 man. Part 1. Anat Anz 1901a;19:124-135. (Fig. 2a). In this section (Fig. 2a) the dorsal primary 7) Bardeen CR, Elting AW. A statistical study of the variation ramus was not yet divided. Thus, the nerve to the in the formation and position of the lumbo-sacral plexus in coccygeus in S2 might be regarded as the dorsalmost man. Part 2. Anat Anz 1901b;19:209-238. 8) Eisler P. Der Plexus lumbosacralis des Menschen. Anat Anz branch of the ventral primary ramus. 1891;6:274-281. Although in man there are various patterns of 9) Eisler P. Der Plexus lumbosacralis des Menschen. Abh d segmental composition (e.g. Bardeen and Elting Naturf Ges Halle 1892;17:279-364. 1901a,b; Sato 1980), based on the present findings, it 10) Kida M. Study on the constitution of the human cervical plexus, with special reference to C3 and C4. Acta Anat could be confirmed that the stratificational pattern is Nippon 1987;62:109-148 (in Japanese with English abstract). common in man as in all species (Akita 1992a,b; 11) Kida M. Stratum-structure of the spinal nerves in the under- Akita et al. 1992b, 1995). standing of body structure. Acta Anat. Nippon. 1990;65 :75— 82 (in Japanese with English abstract). 12) Kida M, Ishida H. Gantzer's muscle-like variation inserted into the forearm flexor retinaculum. Okajimas Folia Anat. Acknowledgment Jpn. 1990;66:1-12. 13) Nakanishi T. Studies on the pudendal nerve. Part 1. A We thank Dr. Tatsuo Terashima of the Depart- macroscopical observation of the pudendal nerve in man. ment of Anatomy, School of Dentistry, Tokyo Acta Anat Nippon 1967a;42:223-239 (in Japanese with Medical and Dental University, for technical support. English abstract). 14) Nakanishi T. Macroscopical observations on the muscular branches of the pudendal nerve. Acta Anat Nippon 1967b;42:288-295 (in Japanese with English abstract). References 15) Sato K. A morphological analysis of the nerve supply of the sphincter ani externus, levator ani and coccygeus. Acta 1) AkitaK. An anatomicalinvestigation of the musclesof the Anat Nippon 1980;55:187-223 (in Japanese with English pelvicoutlet in iguanas(Iguanidae Iguana iguana) and abstract). Varanus(Varanidae Varanus (dumerillii)) with special ref- 16) Takahashi M. Morphological analysis of the pudendal nerve. erenceto theirnerve supply. Ann Anat 1992a;174:119— Acta Anat Nippon 1980;55:23-44 (in Japanese with English 129. abstract). 2) Akita K. An anatomicalinvestigation of the musclesof the 17) Tani M, Kida MY, Akita K. Relationship between the pelvicoutlet in japanese giant salamander (Cryptobranchidae arrangement of motoneuron pools in the ventral horn Megalobatrachusjaponicus) with special reference to their and ramification pattern of the spinal nerve innervating nervesupply. Ann Anat1992b;174:235-243. trunk muscles in the cat (Fells domestica). Exp. Neurol. 3) AkitaK. SakamotoH. Sato T. Stratificationalrelationship 1994;128:290-300. 3-D Reconstruction of Second Sacral Nerve 33 Plate I

Explanation of Figures

Plate I

Fig. 1. Dorsal aspect of a part of the second and third sacral nerves. Lines a—e correspond to the sections in Figures 2 and 3. 34 K. Akita and H. Yamamoto

Plate H

Plate II

Fig. 2. Sections of the trunk of the second sacral nerve as indicated in Figure 1. a) the trunk is divided into a few branches (Brl —5) ( x75), b) the dorsal primary rami arises from the dorsal portion of Br5 (X 160), c) after the dorsal primary rami is given off, Br6 arises from the dorsal portion of Br5, and Brl and Br3 fuse (x75), d) Brl + 3, Br2 and Br4 are divided into small branches, and run caudodorsalward ( x75), e) the branches from S2 adjoin the branches from S3 ( x37.5). 3-D Reconstruction of Second Sacral Nerve 35 Plate Ill

Plate III

Fig. 3. Three-dimensional reconstruction images of selected serial sections of the second sacral nerve. The directions of the figures arc correspondent to Figure 2. These figures (Figs. 3a—f) show the distal sectioning aspects of the nerve approximately every 5 mm from the beginning. The branches arc colored according to the final destinations: yellow, root of the pudendal nen c: red, root of the sacral plexus: blue, dorsal primary rami: sky blue, root of the posterior femoral cutaneous nerve: green. nerve to the coccygeus.