the clinical signihcance of nerve of the cervical … · way of the anterior motor nerve root and...

J. Neurol. Neurosurg. Psychiat., 1960, 23, 321.

THE CLINICAL SIGNIHCANCE OF THE SINU-VERTEBRALNERVE OF THE CERVICAL SPINE IN RELATION

TO THE CERVICAL DISK SYNDROMEBY

RALPH B. CLOWARDHonolulu, Hawaii

The increasing frequency of injuries to the neckhas focused attention on the nature of pain resultingfrom trauma to the cervical spine. The origin andmechanism of pain in the neck, shoulder, and upperextremities resulting from such injury are not wellunderstood. It is assumed that these pains have theirorigin in the ligaments and joints of the cervicalspine including the intervertebral disks. Thesensory nerve which supplies these anatomicalstructures is the sinu-vertebral nerve. Recently,investigations have been made in patients withpainful neck injuries to determine the source of thepain (Cloward, 1959). From the results of thesestudies it has been possible to ascertain the courseand distribution of the sensory nerve which suppliesthese structures, and the referred pain resulting fromits stimulation.The importance of the sinu-vertebral nerve in

cases of rupture of lumbar intervertebral disk hasbeen described by Falconer, McGeorge, and Berg,(1948) and Wiberg (1949). These investigatorshave determined that reflex rigidity and scoliosisresulting from rupture of the lumbar intervertebraldisks are probably produced by irritation of thenerve endings of the sinu-vertebral nerve. Wiberginvestigated the anatomical structures about thelower lumbar spinal canal in conscious patientsunder local anaesthesia. Pressure applied to theligamentum flavum caused no pain except whenthe pressure was too great and was transmitted to theadjacent disk. Pressure on the posterior surfaceof the disk and longitudinal ligament resulted in apain in the lumbosacral area in all cases. Thepatients complained of a deep pain within the backlateralized to the side stimulated. Direct pressure tothe nerve root caused severe root pain over a derma-tome distribution. After anaesthetizing the nerveroot the lumbosacral pain could still be producedwhen pressure was applied to the disk. These ex-periments have all been carried out by the writerand the findings of Wiberg verified.

One may conclude from these investigations thatlow back pain with radiation into the sacro-iliacregion, hip joint, and upper thigh is not due to com-pression of the spinal nerve root by the rupturedlumbar disk but is the result of irritation of thesinu-vertebral nerve which supplies the peripheralfibres of the disk and ligaments which surround it.This has been called a diskogenic pain in contra-distinction to neurogenic or sciatic pain whichresults from impingement of the prolapsed diskupon the spinal nerve root. Valuable objectivediagnostic information as to the origin of the disko-genic pains has been obtained from the procedureof lumbar diskography. By inserting a fine needleinto a ruptured disk (posterior midline) and injectingan opaque fluid into it, pressure is applied to theperiphery of the disk through its torn recesses,producing pain. The patient will recognize thecharacter and location of this induced pain as beingthe same as his clinical symptom if it is caused bythe ruptured disk. Lumbar diskography has beenused for nearly a decade to determine the cause oflow back pain (Cloward and Buzaid, 1952).

All reported anatomical studies of the sinu-vertebral nerve have been made on the lumbar spinewhere the nerve is larger and more easily followed.The procedure of cervical diskography was developedin the hope that diagnostic information could beobtained to determine the origin and causeof pain from cervical disk pathology (Cloward,1958a).In 1956, the method was worked out by inserting

a needle into the antero-lateral surface of the disk,injecting an opaque solution, and obtaining aradiograph. As had been found with lumbar disko-graphy (Cloward and Buzaid, 1952), the injection ofa fluid medium into the interior of the cervical diskproved to be a painful procedure when the disk wasruptured, and the pain as a rule was described bythe patient as being identical with his clinicalsymptoms. It was also found that the antero-lateral

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surface of the disk, either normal or pathological,when stimulated by inserting a needle into it,invariably produced pain. This presented anopportunity to study the sensory nerve supply of thecervical disk. Accordingly, various methods wereemployed to stimulate the disk, each of which willbe described. The referred pains resulting fromstimulation of cervical disks were carefully docu-mented according to the disk stimulated and to theexact location of referred pain which resulted. Thisinformation has been reported elsewhere (Cloward,1959).The anatomical regions to which pain was referred

were obtained from the patient when the anteriorand posterior surfaces of the intervertebral disk andthe corresponding longitudinal ligaments werestimulated. Several methods of stimulation wereused including three blind procedures: (1) Needlingthe anterior surface of the disk for diskography;(2) injection of the disk with a fluid medium fordiskography; (3) insertion of fine insulated wiresinto the disk through the diskogram needle forelectrical stimulation. At operation under localanaesthesia, using the anterior approach (Cloward,1958b), the anterior and posterior surfaces of thedisk were also stimulated under direct vision.

Blind Stimulation(1) The first patient subjected to a cervical disko-

gram complained of pain when the diskogramneedle made contact with the anterior surface of thedisk. When asked to localize the pain, she stated," In my right shoulder blade." Repeated jabs withthe needle into the bone (anterior surface of thevertebral body), above and below the disk, causedno pain. But when the disk was touched, the patientreported a rather sharp, aching type of pain locatedalong the vertebral border of the ipsolateral scapula.The pain referred from the upper cervical disks waslocalized more cephalad on the scapula and fromthe lower disks more caudad. In over 120 patients,upon whom a cervical diskogram of one or moredisks has been performed, this has been a constantfinding. This, together with other stimulationexperiments, has verified the fact that the anteriorouter fibres of the annulus fibrosis of the cervicalintervertebral disk are richly supplied with sensorynerves. When these nerves are stimulated or irritatedon one side of the disk, pain is referred to the regionof the vertebral border of the scapula on the sameside.The second method of investigation was analysis

of pain which resulted when the disk was injected

FIG. 1.-Cervical diskogram.

A. Lateral radiographs: opaque solution (" hypaque " 50%) injected in the centre of the disk has passed into the spinalcanal through a defect (rupture) in the posterior annulus, outlined the protruding disk fragment (arrow).

B. Antero-posterior projection: needles inserted into the centre of the nucleus pulposus from the antero-lateral surfaceof the disk. Injected " hypaque " has collected postero-laterally visualizing the herniated disk (arrow).

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for diskography (Fig. 1). In the case of a normaldisk, that is, one in which fibres of the annulusare not ruptured and the nucleus pulposus is intact,injection of 0-2 to 0 3 ml. of radio-opaque liquidcauses no pain. If the fibres of the annulus aretorn, permitting the opaque solution, injected underpressure, to reach the periphery of the disk, painresults. The location, character, and intensityof the pain will depend upon the location andextent of the rupture or fissure tract in the disk.Anterior or antero-lateral ruptures cause painsimilar to that produced by insertion of the disko-gram needle, i.e., along the medial border of thescapula.

If the disk is ruptured in a posterior or postero-lateral direction, pains which result from diskinjection are of three types: (a) diskogenic, (b) neuro-genic, and (c) myelogenic.The first is by far the most common. If the rupture

in the annulus extends to, but not through itsperipheral fibres, the pain caused by the injection isdescribed by the patient as beginning in the "shoulderblade" (medial scapular border), spreading over theback of the shoulder or on top of the shoulder in a

broad area and then down the posterior surfaceof the upper arm as far as the elbow. This painalso is described as a " deep, dull, aching sensation "which may be quite severe. It subsides about fiveto 10 minutes after the injection. This is the " disko-genic" pain.When the peripheral fibres of the posterior

annulus are lacerated, with or without herniation ofdisk fragments into the spinal canal, as demon-strated by the diskogram, the injected solution canpass through the defect, transmitting the pressureto the spinal nerve root and/or the spinal cord.This " neurogenic" pain resulting from nerve rootirritation has a sharper, more intense quality oftendescribed by the patient as an electric shock or a

hot, burning sensation. It shoots into the arm,forearm, and hand along a dermatome distribution.

In midline disk protrusions, with spinal cordcompression, a " myelogenic" pain results fromdisk injection. This pain, originally described byL'Hermitte, is a shock-like sensation down themiddle of the spine and may spread into one or allextremities. It is of only momentary duration.The third stimulation method consisted of im-

planting insulated wires into the anterior surfaceof the disk through the diskogram needle. Electricalstimulus applied to the implanted wire resulted inpain similar to that obtained by needling the diskfor diskography, that is, it was referred to thevertebral border of the scapula. Weddell, Feinstein,and Pattle (1943) investigated the scapula pain,which is present in almost every patient with

cervical disk disease, by doing electromyograms onthe scapula muscles. They demonstrated abnormalaction potentials suggesting that this pain is a motorphenomenon which originates in the muscles of thescapula as a myalgia. Accordingly, electromyogramstudies were made on the scapular muscles bystimulating the wire implanted in the anterior surfaceof the C5-6 disk. These demonstrated a consistentlyincreased irritability of these muscles. Continuousinvoluntary muscle spasm could be initiated byanterior cervical disk stimulation. Novocaine in-jected into the area of the implanted stimulatingwires abolished the action potentials in the scapulamuscles.

If the pain located in the muscles of the vertebralborder of the scapula is a motor phenomenon, thenerve impulse must pass from the spinal cord byway of the anterior motor nerve root and theperipheral motor nerve. Stimulation of the ventralcervical nerve root has been shown to produce adeep, boring, myalgic type of pain in the musclesof the shoulder girdle, similar in quality and dis-tribution to that resulting from stimulation of theintervertebral disk. Frykholm (1947) appliedmechanical stimuli intradurally to the lower cervicalnerve roots under local anaesthesia. He demon-strated conclusively that nerve root pain could beelicited by stimulating the ventral or anterior rootas well as the sensory root.

Direct StimulationThe recent development of a new anterior surgical

approach (Cloward, 1958b) for removal of rupturedcervical disks offered an opportunity to stimulatethe disk under direct vision. The operation is per-formed under local anaesthesia with the patientconscious and alert. A 3 cm. transverse skin incisionis made on the antero-lateral surface of the neck,and by blunt dissection of the cervical muscles andcareful retraction, nearly the entire half of the diskis easily exposed. Pressure with a blunt instrument,a sharp needle, and stimulation by electric currenthas been applied to each of the cervical disksfrom C3 to C7 in a large series of patients. Thereferred pain to the scapular region found bythe other methods of stimulation was verified. Adrill hole 14 mm. in diameter is made completelythrough the vertebral bodies at the interspace,exposing the posterior surface of the disk and theposterior longitudinal ligament overlying the duramater of the spinal cord and nerve roots. The in-formation accumulated on the distribution of painproduced when the posterior disk ruptures wereinjected for diskography was generally verified bydirect stimulation of these elements at the bottomof the drill " hole ".

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DiscussionFrom the results of our stimulation studies on the

cervical disks, together with those of Frykholm(1947) on the motor roots, a theory may be formu-lated as to the location and distribution of the sinu-vertebral nerve in the cervical spine. While thenerve in this area is so small as to defy ordinaryanatomical methods, the formulation is consistentwith the known anatomy of the sinu-vertebral nerve

in the lumbar region.The original anatomical description of the nerve

supply to the vertebral column and its ligaments wasmade by Luschka in 1850. The nerve, called thesinu-vertebral nerve of Luschka, has been studiedsince that time, though as has been noted, ana-

tomical studies of it have been limited to the lumbarspine. While there is some disagreement as to itsactual course, the origin and distribution of itsterminal branches have been well established.The most accurate description of the origin of the

sinu-vertebral nerve was made by Hovelacque (1925)and recently studied by Kinney (quoted by Herlihy1949). According to Kinney, the nerve is formedby a junction of two roots, spinal and sympathetic.The spinal root takes origin from the ventral surfaceof the "spinal nerve" within the spinal canal. Theanterior and posterior spinal nerve roots meet,decussate, and divide into the anterior and posteriorprimary rami, the short area of decussation beingthe "spinal nerve". The spinal root of the sinu-vertebral nerve is immediately joined by a sym-pathetic fibre which passes medially from thesympathetic chain. Both groups of fibres constitutethe sinu-vertebral nerve. The main trunk of the nervethen passes medially behind the vertebral body andafter a short course divides into its terminal branches.The distribution of the terminal branches of the

sinu-vertebral nerve has been described by Lazorthes,Poulhes, and Espagno (1948) who disagree with an

earlier description by Van Buskirk (1941) as totheir course. Van Buskirk refers to the origin ofthe nerve as the " recurrent nerve " which, on

gaining the intervertebral canal, divides into an

ascending and descending branch, and forms a

longitudinal strand of nerve fibres which he callsthe sinu-vertebral nerve. The longitudinal strand,he states, extends the length of the vertebral canalanastamosing with its fellow above and below fromthe opposite side. Lazorthes et al., on the otherhand, insist " that the distribution of the branchesis purely segmental; that the branches may be shortor long and all are ascendent with one exception;that the nerve never divides into ascending or des-cending branches; and that the nerve anastamoses;the branches may pass anterior or posterior to theanterior longitudinal ligaments and venous sinuses."

According to Lazorthes et al., the branches of thesinu-vertebral nerve are distributed as follows:-

(1) To the vertebral body from the posteriorsurface by a few twigs which pass medially anteriorto the posterior common ligament and enter thebone along with the basi-vertebral veins; (2) to theneuro-laminae from their anterior surface; (3) tothe intervertebral disk above this vertebral body bymore numerous twigs; (4) to the intervertebral diskbelow this vertebral body by fine inconstant fila-ments which are the only descending elements; (5) tothe posterior common ligament; (6) to the internalvertebral plexus; (7) to the epidural tissue; (8) tothe dura mater by one or two twigs.The terminal nerve endings of the sinu-vertebral

nerve have been studied by Jung and Brunschwig(1932) who described nerve fibres in the anteriorspinal ligament, in the posterior longitudinal liga-ment, and between the annulus fibrosus and thespinal ligaments. They found no nerve endingswithin the intervertebral disk, but more recentlyRoofe (1940) observed numerous nerve endings inthe posterior annulus fibrosus and posterior longi-tudinal ligament.The sinu-vertebral nerve supplies the vertebral

column, the intervertebral disks, "the longitudinalvenous sinuses", the ligaments within the vertebralcanal, the epidural tissue of the vertebral canal,and the dura mater. The nerve is largely sensoryand according to Roofe it subserves the functionof pain. Van Buskirk indicates that the nerve con-tains both myelinated and non-myelinated fibres,the majority being the latter. The sympatheticfibres have an arterio-vasomotor function since thelongitudinal veins of the internal vertebral plexusdo not contain muscle tissue.From our stimulation experiments and the known

anatomical distribution of the sinu-vertebral nervein the lumbar region, the nerve supply to the cervicalintervertebral disks, its course and distribution, maybe postulated (Fig. 2). The receptors of this sensorynerve are located throughout the peripheral fibresof the annulus fibrosus of the intervertebral disk,including the attachment of these fibres to the mar-gins of the adjacent vertebral bodies (Sharpey'sfibres). The findings suggest that the nerve fromeach side passes around the disk, supplying one-half of it. The terminal fibres must extend a shortdistance across the midline and decussate with thosefrom the opposite side, since anterior stimulationof the centre of the disk produces bilateral shoulderpain. The terminal branches probably enter theanterior longitudinal ligament. It is questionablewhether the entire length of the long ligament issupplied by filaments from the nerve or just the areaof the ligament which passes over the disk. As

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FIG. 2.-Drawing to demonstrate the proposed anatomy of the sinu-vertebral nerve in the cervical region and the pathwayover which pain impulses originating in the periphery of the intervertebral disk are referred to the region of thescapula, shoulder, and upper arm.

Mechanical or electrical stimulation of:(a) Anterior surface of cervical disk refers pain to vertebral border of scapula.(b) Postero-lateral surface of the disk, pain referred to the scapula, shoulder, and radiation into upper arm.(c) Motor nerve root intradural; deep myalgic type of pain referred to muscles of vertebral border of the scapula.

Pathway of sinu-vertebral from periphery of cervical disk indicated by arrows. Pain impulse enters pasteriornerve root and/or to muscle of scapula as reflex arc through spinal cord, anterior root, and motor nerve. Branchfrom sympathetic chain has insignificant role in pain syndrome.

described above, the referred scapular pain is notproduced by stimulating this ligament over the bodyof the vertebra, but only as it crosses over the disk.It may be that inasmuch as the ligament is so closelyassociated with and often adherent to the anteriorsurface of the disk, the stimulus is transmittedthrough the ligament to the disk surface. This mayindicate that the anterior longitudinal ligament hasonly an insignificant nerve supply compared withthat of the disk itself, and therefore contributes verylittle to the overall pain syndrome.The nerve evidently courses around the disk to

the posterior surface where its fine branches andsensory receptors give evidence of being morenumerous. The flood of pain resulting from stimu-lation of these areas is more diffuse, that is, it spreadsover a wider area. It has been possible to map outby stimulation under direct vision the posterior areaof the disk and posterior longitudinal ligament, butthe information obtained is not so accurate as that

derived from the anterior surface. These posteriorstructures along with the overlying anterior duramater are so closely associated that a great manymore nerve endings of the sinu-vertebral nervewhich supply them are stimulated when the disk isinjected for diskography or at open operation. Thiswould account for the pain which is mere severe andextends over a wider area. Because of the extensiveoverlapping of the painful areas resulting fromstimulation of the posterior surface of the variouscervical disks, it is suggested that one sinu-vertebralnerve may contribute to the nerve supply of theposterior surface of more than one cervical disk,and that through its descending branches it may alsosupply the posterior surface of the intervertebraldisk below as suggested by Lazorthes et al. (1948).

In the lumbar region, according to anatomists,the various branches of the sinu-vertebral nerveconverge on the posterior surface of the spine toform the main trunk or " recurrent nerve " (Van

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Buskirk) which passes through the intervertebralforamen and enters the " spinal nerve " slightlydistal to the spinal root ganglion. The pathwayover which the sensory impulse travels after gainingentrance to the spinal cord by way of the posteriorhorn is unknown. It is likely that the sensoryimpulses pass through a segmental reflex arc to theshoulder muscles by way of the anterior horn cellsand motor root at the same or an adjacent levelof the spinal cord. Many of the muscles of thepectoral girdle are supplied by cervical motor nerveroots. Pain caused by pressure on the ventral roothas been ascribed to changes produced in the musclefibres with resultant activation of local sensoryendings in the muscle, after which the afferentimpulse travels centripetally by way of sensory path-ways, dorsal root ganglia, and dorsal roots to enterthe spinal cord. The impulse is then transmitted vianeurons of higher order to cerebral centres for pain.

It is understandable that pain from stimulationof the anterior surface of the disk would be selec-tively referred to muscles along the vertebral borderof the scapula. These muscles, i.e., the levatoresscapulae, the rhomboidus minor and major, receivetheir nerve supply from the anterior rami of thethird, fourth, and fifth cervical nerves. The explana-tion for a painful stimulus on the anterior surfaceof the spine being perceived in the middle of theback is to be found in the developmental originof the posterior muscles of the body wall. Em-bryologically the " ventrolateral " sheath of muscu-lature of the lower cervical region undergoessubsequent migration to obtain a secondary skeletalattachment to the vertebral column at a considerabledistance from its origin. Such " muscle migration "is most clearly seen in the diaphragm and latissimusdorsi muscles.A few patients were selected because they were

good witnesses to sensory stimuli. When thecervical disk were stimulated and the scapular painproduced, superficial sensation over the area wastested with light touch and pin prick. Although thefindings were often equivocal, one occasionallyencountered a patient who insisted that the skinover the painful scapular area was hypersensitiveto superficial stimuli. This was observed imme-diately following injection of the disk for disko-graphy. This finding suggested a sensory as well asa motor origin for the scapular pain and mayrepresent a retrograde impulse through the posteriorspinal root and sensory nerve as suggested by Kahrand Sheehan (1933).

In performing the cervical diskogram, inquiry isalways made to determine if the flood of pain whichfollows disk injection could be interpreted as havinga sympathetic character or distribution. There are

numerous reports in the literature in which symp-toms such as headache, facial pain, vertigo, pseudo-angina, etc., have been attributed to and describedas a part of the cervical disk syndrome (Neuwirthand Gayral, 1958). It has been our general im-pression clinically that ruptured cervical disks arenot directly responsible for these vague, unexplain-able symptoms. Furthermore, experimentally in-duced pain, resulting from disk injection, in ourexperience has not been referred to the head,face, ear, eye, or precordium. This suggests thatpain impulses having their origin in the disk do notspread through the sympathetic chain to theseremote areas. The function of the sympatheticbranch of the sinu-vertebral nerve is to supply, viavisceral motor fibres, the blood vessels of the spinalcanal and the spinal dura mater, as described byFrench anatomists. If pain of a sympatheticcharacter results from irritation of these structuresby a ruptured disk, it remains localized as part ofthe neck, shoulder, and arm pain and does notspread to other regions.

Summary and ConclusionsIn the investigation of the cause of neck, shoulder,

and arm pain in patients with lesions of cervicalintervertebral disks, the anatomical structure respons-ible for the major portion of these pains was foundto be the intervertebral disk itself and its surround-ing ligaments. Various methods were used tostimulate the disks in conscious subjects, and theexact location and distribution of the referred painswere determined. Objective information was alsoobtained by electromyographic studies of theshoulder and arm muscles resulting from stimulationof the lower cervical disks. From the informationthus accumulated, together with known anatomicalknowledge of the sinu-vertebral nerve in the lumbarregion, the course of this nerve in the cervical spinehas been proposed. Two possible routes for the painimpulse carried by this nerve after it enters the spinalcord are also suggested.

REFERENCESCloward, R. B. (1958a). Amer. J. Roentgenol., 79, 563.

(1958b). J. Neurosurg., 15, 602.(1959). Ann. Surg., 150, 1052.

, and Buzaid, L. L. (1952). Amer. J. Roentgenol., 68, 552.Falconer, M. A., McGeorge, M., and Berg, A. C. (1948). J. Netrol.

Neurosurg. Psychiat., 11, 13.Frykholm, R. (1947). J. Neurosurg., 4, 403.Herlihy, W. F. (1949). N.Z. med. J., 48, 214.Hovelacque, A. (1925). Ann. Anat. path., 2, 435.Jung, A., and Brunschwig, A. (1932). Presse med., 40, 316.Kahr, S., and Sheehan, D. (1933). Brain, 56, 265.Lazorthes, G., Poulhes, J., and Espagno, J. (1948). C. R. Ass. Anat.

34th Reunion, p. 317.Luschka, H. (1850). Die Nerven des menschlichen Wirbelkanales.

Laupp, Tubingen.Neuwirth, E., and Gayral, L. (1958). J. Lancet, 78, 197.Roofe, P. G. (1940). Arch. Neurol. Psychiat. (Chicago), 44, 100.Van Buskirk, C. (1941). Arch. Surg. (Chicago), 43, 427.Weddell, G., Feinstein, B., and Pattle, R. E. (1943). Lancet, 1, 236.Wiberg, G. (1949). Acta orthop. scand., 19, 211.

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