ARTERIAL SUPPLY OF THE CERVICAL SPINAL CORD AND ITS

ARTERIAL SUPPLY OF THE CERVICAL SPINAL CORD AND ITSRELATION TO THE CERVICAL MYELOPATHY IN SPONDYLOSIS

Arris and Gale Lecture delivered at the Royal College of Surgeons of Englandon

8th February 1967by

B. G. Chakravorty, M.S., Ph.D., F.R.C.S.Eng., F.R.C.S.Ed., F.A.C.S.Consultant Neurosurgeon and Lecturer, Department of Surgery, Sir Nilratan SircarMedical College, Calcutta; Teacher, Department of Surgery, Postgraduate College of

Medicine, University of Calcutta

CERVICAL SPONDYLOTIC MYELOPATHY is now known to be a commonneurological disorder affecting elderly people. In fact it is one of thecommonest, if not the commonest, diseases of the spinal cord after middlelife (Brain, 1954). This condition is the effect of cervical spondylosis,which is a slowly progressive degenerative condition affecting the inter-vertebral discs.The material presented in this lecture is partly anatomical and partly

clinical. An attempt has been made to define the arterial supply of thespinal cord in the cervical region, and to correlate the anatomical findingswith the clinical features of cervical myelopathy in spondylosis. Operativetreatment is based on this vascular concept, and the results so far havebeen satisfactory.PathologyThe basic pathology of cervical spondylosis is the protrusion of de-

generated disc material into the spinal canal. The primary factor in discdegeneration is still uncertain. It is thought to be a process of degenera-tion associated with ageing when the nucleus pulposus suffers a progressivereduction in its fluid content which results in a diminution in its sizetogether with a loss of elasticity (Puschel, 1930; Saunders and Inman,1940). This process of degeneration may occur at an earlier age in as-sociation with trauma or with pre-existing congenital maldevelopmenteither in the bony spine (fusion, spina bifida, hemivertebra) or in the discitself.Once the disc shrinks and loses its resilience the vertebral bodies tend to

approximate. The mobility of the cervical spine puts more strain on thedegenerated annulus, and the disc matter bulges out. Nuclear materialmay prolapse through a tear in the annulus (nuclear herniation) or theannulus itself may bulge out (annular protrusion). The prolapsed discmatter lifts the periosteum, and the subjacent bone proliferates to formosteophytes; these with time grow from above and below to enclose theprolapsed material. Excepting the condition of massive prolapse, whenthe spinal canal and the intervertebral foramina may all be equally in-volved, the localized form of the disc protrusions usually take threeanatomical positions, median, dorsilateral and intraforaminal (Fig. 1).Although intervertebral disc lesions in the cervical region as a cause of

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ARTERIAL SUPPLY OF THE CERVICAL SPINAL CORD

acute cord lesion had been recognized as early as 1892 by Victor Horsley,who treated the condition surgically, it was not until 1926 that Elliottfound that radicular symptoms involving the cervical nerve roots may becaused by the narrowing of the intervertebral foramina due to arthriticchanges in the vertebral column. Since then many others have workedon the clinical and pathological aspect of cervical disc lesions (Mixter andAyer, 1935; Stookey, 1940; Spurling and Scoville, 1944), and direct pres-sure on the cord or nerve root by the prolapsed disc substance was heldmainly responsible for myelopathy. Spillane and Lloyd (1951) in areport of 12 cases reviewed the literature and concluded that multipledisc degeneration leads to bulging of the discs; these ridges compress thecord, and produce abrasive effects on it by constant friction. Brainet al. (1952), in their post-mortem study of cases of cervical spondylosis,observed adhesions of dura to the posterior longitudinal ligament, and ofthe dural sleeves to the margins of the intervertebral foramina. They

Fig. 1. Digram showing the position of a median (I), dorsilateral (II) and intra-foraminal (III) cervical disc protrusion. There may be occasionally in-between

positions such as paramedian and lateral.

stressed that the cord was rendered more susceptible to injury by theseadhesions. They also suggested that the interference with the vascularsupply was an important subsidiary factor. Bedford et al. (1952) sup-ported the above workers, and commented that abnormal fixation of thecord may render it vulnerable to normal neck movements. At autopsythey observed unusual tension on the thickened denticulate ligaments andfibrous nerve roots; in addition, the theca was adherent to the posteriorlongitudinal ligament. Taylor (1953) suggested a compression effect onthe cord by the ligamenta flava during each extension movement of theneck against the anterior spondylotic elevations, thus producing gradualchanges of an uncertain nature in the vasculature of the spinal cord.Clinical featuresOn analysis of the clinical features of cervical spondylotic myelopathy

it has generally been agreed that the dominating feature of the condition isweakness and spasticity of limbs, usually starting in the legs (Tablea).

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B. G. CHAKRAVORTY

This, in combination with extensor plantar responses and exaggerateddeep tendon reflexes, is attributable to lesions in the pyramidal tracts.Sensory depression, loss of reaction to pain and temperature, with pre-servation of light touch and tactile discrimination, are caused by lesionsin the spinothalamic tracts. The sphincter disturbances are also attribut-able to spinothalamic depression when lack of cortical appreciation ofvisceral sensation occurs. Anatonmically both these tracts occupy thelateral white column of the spinal cord.

Pain radiating down the arm, and zones of anaesthesia in dermatomedistribution are due to damage to roots rather than to the cord. Thecommon involvement of the first three fingers is due to the frequentlyaffected C5 and C6 nerve roots. Loss of vibration sense and tactilediscrimination, and a positive Rhomberg's sign, relate to damage of theposterior columns; these signs are occasional and rarely complete,

TABLE IANALYSIS OF CLINICAL FEATURES (31 PATIENTS)

No. Symptonms and signs No. ofpatienits

1. Weakness and spasticity of lower limbs .. .. 202. Simultaneous involvemeait of all limbs with weak-

ness and spasticity .. .. .. .. 143. Clumsiness of finger movements .. .. .. 164. Spinothalamic (pain and temperature) depression,

and paraesthesia .. .. .. .. .. 145. Sphincter disturbances .. .. .. 76. Pain in the neck with radiation into the arms .. 67. Limitation of neck move:ments .. .. .. 78. Exaggeration of deep je.-ks .. .. .. 259. Babinski's sign positive .. .. .. 21

10. Increase of tone in all limbs .. .. . 1611. Inversion of supinator j(,rks .. .. . 1512. Atrophy of intrinsic muscles of hand .. .. 8

signifying a partial involvement. Recently Crandall and Batzdorf (1966)in an analysis of 199 cases have shown pyramidal and spinothalamicinvolvement in all cases, whereas posterior columns were affected only in16 per cent.Muscular atrophy and depression of reflexes can be explained by

damage to the anterior horn cells. The inversion of the radial reflex,which was observed in 15 patients, is characteristic of this syndrome.It indicated interruption of the reflex arc and associated involvement of thepyramidal tract, resulting in exaggeration of the flexor movements of thefingers (Spillane and Lloyd, 1951). Loss of anterior horn cells may alsobe responsible for the disturbance of the reflex arc. Rigidity and weak-ness, a common finding, may indicate some damage to the extra-pyramidal corticospinal pathways; the rubrospinal tract occupies theateral column just anterior to the main pyramidal tract (pre-pyramidaltract).

Clinically the lesion is widespread. Compression and traction factorsseem inadequate to explain the extent and order of the damage. There issometimes little correlation between clinical findings in cervical myelo-

234


pathy, and the segmental level of radiological changes. The extent ofneurological damage is too great to be explained by the level ofcompression.The small muscles of the hand are often involved and this can be

attributed to the loss of anterior horn cells in the first thoracic segment,and cannot be explained by compression or traction factors. In largeprotrusions, or when the spinal canal has been greatly narrowed (10 mm.or less compared with 17 mm. normal (Wolf et al. 1956)), direct compres-sion of the cord against the laminae can cause myelopathy, but such adegree of narrowing is rare (Brain, 1948), although the extent of narrowingin spondylosis may be as little as 14 mm., still leaving enough room for thecord (Payne and Spillane, 1957).

A vascular factorIt is agreed that if the direct anteroposterior cord compression is the

basis of myelopathy then the signs and symptoms will be related mainlyto the lesions of anterior horn cells and anterior and posterior columns.Moreover, the level of the lesion will be localized, or remain localized fora long time, corresponding to the compressing agent. This fails to ex-plain widespread myelopathy in those cases where the compressing agentis very small or non-existent.

Recently various workers have laid emphasis on a vascular factor in thepathogenesis of cervical myelopathy. The theory of vascular insufficiencyin cervical myelopathy postulated by Morton (1950) and Allen (1952)has also been supported by Mair and Druckman (1953), Girard et al.(1954) and Clarke (1955). These workers, although putting forward acommon vascular hypothesis, differ in their explanation of the mechanism.Brain (1948), Frykholm (1951) and Taylor (1964) have also suggestedthe possibility of a vascular factor.

This suggestion of a vascular theory is not altogether a new concept.As early as 1875 Braun thought that osteophytic compression of the peri-radicular vessels was an essential factor in the production of root symp-toms. After a long lapse of time, Greenwood in 1942, while investigatingthe pathogenesis of amyotrophic lateral sclerosis, considered it to be theeffect of chronic anoxaemia of the cord resulting from a slowly developingreduction in the blood flow such as would occur in anterior spinal arterythrombosis affecting firstly the motor tracts. It might very well be thatmany of Greenwood's cases were actually patients suffering from cervicalspondylotic myelopathy.Although several workers have suggested the hypothesis of anterior

spinal ischaemia in the pathogenesis of cervical myelopathy, the exactmechanism remains controversial. This led us to find out more aboutthe vascular factors in cervical myelopathy from anatomical and com-parative anatomical studies of the arterial supply of the cervical cordin cadavers and in laboratory animals.

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B. G. CHAKRAVORTY

Materials and methodsThe material upon which this present study has been made consists of

31 spinal cords obtained at autopsy, as soon as possible after death, fromadults of different ages, mostly the victims of accidental death who in allprobability during life had not suffered from any vascular or nervousdiseases. In order to study the comparative anatomy, in vivo injectionexperiments were carried out on four monkeys, three dogs, five rabbits andfour rats.The arterial supply of the cervical spinal cord was studied following

injection of radio-opaque barium, Indian ink, Monastral blue (I.C.I.),and coloured neoprene latex solutions. The apparatus for injectionconsisted of a small Woulfe's bottle, connected in series to the inlet tubewith a manometer in which pressure during injection was maintained at120-160 mm. Hg, i.e. at an average systolic blood pressure appropriateto the age of the specimen, by pumping in air.

In all cadavers, prior to injection, the brain was removed at the mid-brain level avoiding damage to the basilar artery and its branches. Theclavicle on the ipsilateral side was removed and the subclavian artery withits principal branches, i.e. vertebral, thyrocervical, costocervical and in-ternal mammary trunks, were isolated and injected with the media underpositive pressure.

Following injection, the spinal cords with intact dural coverings andnerve roots were dissected out from the medulla to the third thoraciclevel.

After fixation, the meninges were removed and the vessels were examinedmacroscopically, radiologically and histologically.Observations

In this series, complete absence of the right vertebral, the right anteriorspinal or of the main anterior spinal trunk (Duret, 1873; Spiller, 1908)has not been observed. In each case the vertebral artery entered into thecranium piercing the atlanto-occipital membrane. Never was it seen topass through the second or third cervical intervertebral foramen (Kadyi,1889), and the abnormality of incontinuous anterior spinal trunk(Romanes, 1962) has also not been noted.

It was noticed that when injections were carried through the anteriorand posterior spinal branches of the intracranial vertebral artery thesearterial trunks could be filled only in the highest cervical segments; therest of these trunks had very poor filling if any at all. The spinal branchesof the intracranial vertebral artery are probably important for the fillingof the upper cervical cord (Cl, C2, C3) only. In all specimens the wholeanterior and posterior arterial trunks had excellent filling when injectionswere carried out through isolated radicular arteries (Fig. 2a and b).The radicular arteries were inferred to be the main source of supply for thecervical spinal cord except for a few segments at the cranial end where the

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vertebral anterior and posterior spinal branches are important supply.Anterior spinal artery: The diameter of the anterior spinal trunk always

increases immediately below the junction with a radicular artery, indirect,evidence that the radicular arteries are feeding vessels, and bring bloodto the anterior spinal artery. In three cases only we noted the Y-shaped

I

..

I.T.'

ia b !

zM,r :'wx-1w.(a) (t) (C)

Fig. 2. (a) Shows filling of the anterior spinal artery (paired vessel in this specimen).Cranial end is not filled, injection was made through the isolated left C5 radicularartery which also shows Y-shaped bifurcation. (b) Shows the posterior spinalarterial chains of both sides and its relation to the posterior nerve roots. Injectionwas made through the isolated right C5 radicular artery. The cranial end is spar-ingly filled. (c) Showing the Y-shaped bifurcation of a solitary radicular arteryinto an ascending and descending branch to form the anterior spinal artery.

division of the anterior spinal artery, as though its branches were reallythe anterior spinal artery going up and down (Fig. 2c). In 19 specimensthe anterior spinal artery was a single trunk, but in 12 these were pairedvessels in the cervical region; such duplications were never noted belowC5/6 segments (Fig. 2a).

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B. G. CHAKRAVORTY

The anterior spinal artery, when a single trunk, was always contained inthe midline groove. Sometimes deflections occurred at the junction of theradicular arteries, but these were never more than 1 mm. from the midlineexcept in those cases where the anterior spinal artery appeared to be theY-shaped bifurcation of a major anterior radicular artery, which could beas much as 5 mm. from the midline (Fig. 2c). In duplications, the widervessel more often occupied the midline sulcus, and the other was usuallywithin 0.5-1.5 mm.; the distance was never more than 2 mm. Knowledgeregarding the position and duplication of the anterior spinal artery is ofgreat importance in operative procedures like cordotomy.

Posterior spinal arteries: In 17 specimens the origin of the posteriorspinal arteries were dissected free; in 11 they originated from the posteriorinferior cerebellar artery, and in six they were branches of the vertebralartery. The posterior spinal arteries appeared as anastomotic chains oneither side of the midline close to the line of attachment of the posteriornerve roots (Fig. 2b). This arterial system was not a continuous channelof uniform diameter but extremely irregular, and in parts found to beincomplete; a breach in continuity may occur at the junction of posteriorspinal with the first posterior radicular artery. Injection into the anteriorspinal artery only, never produced filling of the posterior spinal and viceversa; it is possible that the anastomoses between the anterior and posteriorarterial systems are very sparse and functionally ineffective.

Cervical radicular arteries: The cervical radicular arteries, i.e. the arteriesaccompanying the nerve roots entering through the intervertebralforamina, are capable of filling both anterior and posterior arteries in thecervical cord when injections are carried through the isolated radiculararteries obliterating the intracranial vertebral branches (Fig. 2a and b).These radicular arteries may originate from any branch of the subclavianartery in the neck, i.e. from the vertebral, costocervical and thyrocervicaltrunks. In the upper six segments they can arise from the vertebralsor from the ascending cervical branch of the thyrocervical trunk, and thespinal branches of these two vessels always anastomosed (Fig. 3a). Itwas apparent that either the vertebral or the ascending cervical can main-tain the radicular supplies in the upper cervical region through theseanastomoses if either source is blocked. A radicular of the 7th or 8thsegment is always from the branches of the costocervical trunk. As a rule,a radicular artery accompanying the 8th root is rare; in only one specimenin this series was there a radicular artery accompanying the right 8throot.

Although there may be two branches (one from the vertebral and onefrom the ascending cervical) entering one intervertebral foramen, theradicular artery connecting the anterior spinal trunk is always singular forthat particular segment; it originates as a common radicular artery anddivides into an anterior and a posterior branch. The anterior radicularhas a range of diameter 100-750 p, and can be divided into major

238


(500-750 p), minor (250-500 p) and minimal (less than 250 ,u), accordingto the diameter. It appeared that vessels having a diameter greater than250 ,u were the only sources of blood supply to the spinal cord (exceptingthe highest segments), because only they joined the anterior spinal artery.

,." II,/

Fig. 3. (a) Latex corrosion specimen, showing the intervertebral branches fromthe ascending cervical artery. These anastomose with the radicular branches of thevertebral artery, or the radicular arteries may arise directly from the ascendingcervical artery. (b) Corrosion specimen of the vascular pattern in a rabbit. Theformation of the basilar artery is seen. Radicular branches of the right ascending

cervical and the vertebral artery anastomose.

The minimal vessels (i.e. having diameters less than 250 p) were seen inalmost every segment and they ended supplying the tissues around theroots.Radicular arteries in spondylosis

In the present series it was observed that, though the anterior radiculararteries may occur at any level, the significant vessels (i.e. more than 250 idiameter) were usually between C4 and C6 segments and very rarelyat C3, C7 and C8. In the 31 spinal cords investigated, eight radicular

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B. G. CHAKRAVORTY

arteries accompanied C4 nerve root, sixteen C5 and nine entered alongwith C6 nerves. The average number of radicular arteries (major andminor) in the cervical cord is two or three. This observation seems toagree with that of Kadyi (1889) and Suh and Alexander (1939), and therewas very little difference from other workers (Table II). In many casesthe anterior radicular artery may be solitary; in 20 of the 31 cords in-vestigated there was only one anterior radicular artery communicatingwith the anterior spinal trunk in the cervical region (Fig. 2c).

Spondylotic changes in the cervical vertebrae commonly affect thelower cervical region. In Morton's (1950) series of post-mortem exam-

TABLE IINUMBERS AND POSITIONS OF THE SIGNIFICANT RADICULAR ARTERIES IN THE CERVICAL

CORD AS NOTED BY DIFFERENT OBSERVERS

Adamkiewicz (1881)

Kadyi (1889)

Suh and Alexander(1939)

Bolton (1939)Zulch (1954)

Woollam and Millen(1958)

Gillilan (1958)

Perese and Fracasso(1959)

Present series

Anterior radiculararteries

Usually 3; at C4, C5and C8Usually 2; between C4to C7; most commonlyat C5 or C61 or 2 in lower and 1 inupper cervical region,usually between C3 toC6

1 or 2 usually at C6 orC7I major at C6 or C7; 3to 5 minor at segmentsabove C6At least 2; larger one atC5 or C6, the next oneat C3; almost never atC81 to 5 may occur at alllevels; maximum be-tween C3 to C72 or 3 may occur at anylevel, mostly betweenC4 to C6; very rarely atC8

Posterior radiculararteries

I or 2; at C6 or C7

I or 2; between C4 andC7

A large one at C4

1 at C2; I to 3 betweenC5 to C7

1 or 2 may occur at anylevel between C2 to C6;usually one at C4

inations, the commonest incidence was at C4/5 and C5/6 levels. InWilkinson's (1960) series of 17 autopsy examinations, all but one had adisc protrusion at C5/6 level, and the next common level was C4/5. Inthe large series of Crandall and Batzdorf (1966), comprising 199 cases,the same order of incidence is seen. We also confirm this with our clinicalexperience, autopsy findings, and during operative procedures in thisseries of 31 patients (Table lll). It is strongly felt that if the radicularartery (or arteries) is occluded the risk of ischaemia arises. The risk isgreater if there is but a single major radicular artery which is occluded,and the incidence of solitary radicular artery in the cervical cord, asalready stated, is frequent. By random clipping of C4, C5 and C6 nerveroots, including the radicular arteries (if any), it had been noticed that in

240


all specimens but one there was no significant filling of the anterior spinalartery.The intravertebral part of the vertebral artery and the first six nerve

roots are embedded in one mass of connective tissue. The radiculararteries from vertebral or from ascending cervical originate and passthrough this connective tissue mass. This connective tissue is normallycomposed of loose areolar type, and its character does not change withage, i.e. it retains its areolar character whether it is from a still-born foetusor from a person over 75. In spondylosis, probably by the irritation ofosteophytes, this areolar tissue changes into mature fibrous tissue whichwith time becomes hyaline and sclerotic. It surrounds and envelopsthe perineural sheaths of the issuing nerves at the exit foramina producinga constricting effect on the contents of the i.v. foramina including thecervical nerves, and the radicular arteries. Although Frykholm (1951)noticed fibrosis of the dural sheaths, what he called ' root sleeve fibrosis ',we have found that the real thickening and hyalinization are in theperidural layer in which the radicular vessels run. The dura itself is

TABLE IIIINCIDENCE OF Disc PROTRUSIONS AND SIGNIFICANT RADICULAR

ARTERIES IN RELATION TO CERVICAL SEGMENTAL LEVELSLevels Morton Brain Wilkinson Stoops Present Levels of

(1950) et al. (1960) and series significant31 cases (1952) 17 cases King (1967) radicular

38 cases (1962) 31 cases arteries49 cases 31 specimens

C2/3 4 5 4 1 2C3/4 5 20 12 1 6 8C4/5 6 19 11 7 12 16C5/6 6 18 16 22 21 9C6/7 5 14 9 14 18 2C7/T1 1 1 2 6 - 1

little thickened, and at operation the sclerotic epidural tissue can bescraped off leaving a clear shining dural surface. This root sheathcompression can be pre-operatively confirmed by myelography; inmyelogram this is evidenced by the failure of entry of Myodil into theaffected nerve sheaths (Fig. 4).

It becomes apparent that should the blood supplying radicular artery(or arteries) be affected by lateral foraminal disc protrusion and/or thereactive fibrosis there will be a major cut-down in the vascular supply tothe anterior spinal trunk, and anterior spinal ischaemia will follow; therisk is maximal when the radicular artery is solitary and that too is in-volved in the osteophytic and fibrous strangulation.The histology of the cervical cord obtained at post-mortem examinations

from cases of spondylotic myelopathy shows widespread degeneration,extending both upwards and downwards for several segments. Mair andDruckman (1953) have shown that the lesion principally involved theanterior horns, lateral columns and the anterior part of the dorsal columns.The histological changes were similar to those of ischaemia, and they alsoshowed that the area of lesion following the zone of distribution of the

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B. G. CHAKRAVORTY

anterior spinal artery. We fully agree with Mair and Druckman. Theclinical features of the patients suffering from spondylotic myelopathycan be explained satisfactorily on the basis of lesions involving the anteriorspinal arterial zone. The anterior spinal artery supplies the anterior two-thirds of the spinal cord, i.e. anterior horns, anterolateral tracts (maintracts are anterior and lateral, pyramidal and spinothalamic tracts;rubrospinal tract), central grey matter, and the anterior part of the posteriorcolumns (Fig. 5a and b).The atrophy of the small muscles of the hand (lesion of Ti segment) in

cervical myelopathy can only be explained by the vascular hypothesis.In all specimens we noticed that, on injecting either through the intra-cranial branch or through the cervical radicular arteries, the filling of the

Fig. 4. Anteroposterior myelogram shows absence of bilateral root sleeve filling.At operation C6 roots on both sides were found to be compressed by fibrous tissue

only.anterior and posterior spinal trunks gradually tapered down to the lowercervical segments; at most it reached up to the second thoracic segmentand never below it. This may indicate a terminal zone of the cranio-cervical feeding vessels and would support the theory that segments of thehighest thoracic level, where the supply of blood from upper (cranio-cervical) and lower (thoracic radicular) sources meet, are likely to sufferfrom an insufficiency of blood from either source (Fig. 5c). Zulch (1954)in anatomical and clinical sudies has shown that an occluding lesion ofthe anterior spinal artery, or of a major cervical radicular artery, cancause necrosis of lower cervical and highest thoracic segments, as thisarea is the 'last field' zone where the supply of the cervical and thoracicradiculars come into contact.

242


I wL- -i _~ Ir_A Cl.C iI_gl IP| I 11M I_a.pwnsl wAve'ytXa s s 1 Cl_ Q . WL.t -b4sr2;t1.3

s.i cs/I&/c-r

TI

(a)

atTS/t'9,,7 ~~~~~~~~~~~attqeta(b) (c)

Fig. 5. (a) Section of the spinal cord showing relative positions of the ascendingand descending tracts, and the areas of distribution of the anterior and posteriorspinal arteries. The leg fibres occupy the outermost position in the lateral cortico-spinal (main pyramidal) bundle. (1) Dorsal spinocerebellar; (2) lateral cortico-spinal (pyramidal); (3) ventral spinocerebellar; (4) lateral spinothalamic; (5) ventralspinothalamic; (6) central branch of anterior spinal artery; (7) posterior spinalartery; (8) peripheral pial network. (b) Micro-angiography of a C5 segmentshowing the joining of an anterior radicular artery to the anterior spinal artery,and the distribution of the central branch of the anterior spinal in the anterolateralaspect of the cord. (c) Shows the probable direction of blood flow in the anterior

spinal artery. The areas indicate the ' last field ' zones.

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B. G. CHAKRAVORTY

The vascular hypothesis can also explain why the legs are first affectedwith spasticity and weakness in so many cases and why in some casesparaesthesia is the first symptom. In the spinal cord, the leg fibresoccupy the outermost position in the main corticospinal bundle; thespinothalamic tracts are also located peripherally. The distal position ofthe leg fibres, and of the spinothalamic tracts, make them more susceptibleto even a minor degree of ischaemia; these zones are similar to a ' lastfield' on horizontal cross sections where the central branches of theanterior spinal artery and the penetrating branches of the pial networkmeet (Fig. 5a and b). In progressive ischaemia the area of supplygradually attains a concentric constriction, and the centre suffers last.The anterior part of the posterior columns, though supplied by the anteriorspinal artery, is usually spared in ischaemia; Gillilan (1958) has shownthat there is always a zone of overlapping in this area.Comparative anatomy

It was noticed that the arterial arrangements of the cervical cord inmonkeys and rats were very similar to those of man. In dogs, the branchfrom the vertebral artery accompanying the first cervical nerve root isvery small, the larger vertebral branch commonly enters through thethird intervertebral foramen. In none of the human specimens in ourseries was this anatomical variation noted, though such an anomaly in thehuman is on record (Kadyi, 1889; Sterzi, 1914). In rabbits, the arterialpattern is somewhat different as the right innominate and left commoncarotid leave the arch of the aorta as a single trunk, and the left subclavianis a separate aortic branch. In number and positions also, the anteriorradicular arteries in dogs and rabbits differed from those of monkeys,rats and men. The number of radicular arteries was greater in dogs andrabbits; almost every segment had a radicular artery of more or lessuniformly small diameter. The contribution from the ascending cervicalartery (Fig. 3b), the relationship with the vertebral artery and cervicalnerve roots and the ultimate distribution of vessels in the cord are similarin all these animals, including man (Sahs, 1942; Woollam and Millen,1958; Yoss, 1950).

In our animal experiments, interruption of bilateral C5 radiculararteries produced widespread vertical degeneration of the cord extendingfrom first cervical to first thoracic segments (Table IV). Necrosis wasmost marked at C5 and C6 segments, and the total area of the segmentswas involved. In the third and fourth segments, degeneration affectedboth anterior and posterior parts, while at distal segments it was relatedstrictly to the distribution of the anterior spinal artery (Fig. 6). The totalnecrosis at the level of the occlusion is due possibly to a secondary necrosisas a result of occlusion and haemorrhage in the anterior two-thirds of thesegments following the acute ischaemic experiment.Treatment

Every patient in the present series had a prior trial with non-operative244


conservative measures such as immobilization, traction and limitation ofactivity combined with analgesics and various drugs, ranging from weeksto several years. This regime of management afforded a varying degree ofsymptomatic relief for a temporary period in most of the patients. Theneurological deterioration remained progressive though the rate of worsen-ing varied and ultimately, when conservative measures were consideredinadequate, operative treatment was proposed.The operation procedure adopted in this series aims mainly at relieving

the compressed radicular arteries by decompression of the nerve roots atthose intervertebral foramina where they are affected, and it also freesthe cord from other possible compressing agents such as a big anteriorlyplaced bony spur or hypertrophied ligamenta flava.

TABLE IVEXPERIMENTAL ISCHAEMIA IN DOGS

Method Procedure Effects Histologicaladopted produced changes

1. Both vertebrals Nil Niland one commoncarotid ligated inneck

2. Both vertebrals Nil Niltied in neck withproduction of arti-ficial thrombosisin one vertebralartery

3. Intradural bi- Immediate dia- Oedema of cellslateral ligation of phragmatic and and loss of NisslC4 nerve roots intercostal respir- granules in theand accompanying atory paralysis anterolateral re-radicular arteries gions of C3, C4

and C54. Intradural bi- Spastic weakness Necrosis in antero-

lateral ligation of in limbs and lack lateral region of allC5 nerve roots of sensory and vis- segments (Cl toand accompanying ceral appreciation T2), except C5 andradicular arteries C6 in which

necrosis was totalInformation already obtained by the lateral and oblique X-rays, and

myelography showing encroachment of the intervertebral foramina andobliteration of root sheaths, helps to indicate the site of exposure (Fig. 4).Operation comprises of laminectomy and decompression of the nerve rootsby removing the compressing agent, bony or fibrous.Operative techniqueThe operation is carried out under general anaesthesia with the patient

in sitting position, which facilitates good respiration and minimizescongestion and bleeding from the extradural venous plexus. Laminaeof the contiguous vertebrae of the affected intervertebral foramina areremoved. The position of the affected roots, i.e. for the more commonlyinvolved C4, C5, C6 levels, C5 and C6 roots, are then determined. Theroot (or roots) may be swollen and tightly compressed by osteophytesor by dense fibrosis. A fine probe is passed very gently along the fora-

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B. G. CHAKRAVORTY

niina which helps to recognize the roots affected and the degree of com-pression; this is not attempted if inspection suggests a very high degreeof foraminal constriction. Using an electric dental burr, the affectedroot is now decompressed by unroofing its foramen. This involvesremoval of the posterior wall of the intervertebral foramen, i.e. contiguousarticular pillars with zygopophyseal joint (Figs. 7a and 8). The con-densed fibrous tissue surrounding the dural sheath of nerve root is thenremoved as far outwards as possible, leaving the roots free (Fig. 7b).This process is repeated with each affected nerve root. At the conclusion

Cl ®(8 C2

0 CCe~~~~~A

Fig. 6. The shaded areas in the diagram show the areas of necrosis as observedin the various segments of the spinal cord resulting from occlusion of bilateral C5

radicular vessels in dogs.

the roots should appear reasonably slack, and the probe should passsmoothly. The dura need not be opened unless some other pathologyin the cord is suspected, and no attempt should be made to remove anyanterior bony spurs.Results

Complications following the operation were fortunately rare. Nonesuffered from air embolism; probably meticulous care in haemostasis andliberal use of saline irrigation during the operation prevented this danger.There was no post-operative death.

All patients were allowed up on the sixth post-operative day, and re-

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ARTERLkL SUPPLY OF THE CERVICAL SPINAL CORD

(a) (b)Fig. 7. Photograph during operation. (a) Muscles have been separated andlaminae have been removed. Dura is not opened. The electric dental burr isbeing used to remove the posterior wall of the left C4/5 intervertebral foramen.The nerve root is protected with a fine dissector. (b) Shows that C5 roots on bothsides have been completely freed from compression. Posterior bony walls havebeen removed, and thickened epidural tissue has been stripped off leaving only

intact dural sheaths of the nerve roots.

II-tA'I

I'I'

-l II £il#

- .1 :1'. 1

'I

Fig. 8. Diagrammatic representation of operation on the right side.

247

B. G. CHAKRAVOR1 Y

ceived continued post-operative physiotherapy. They were allowed tocontinue their exercises at home after discharge. None needed anyexternal support.

These patients have been followed up for periods of six months to fiveand a half years. The age of the patients and duration of their symptomsseemed less important than the severity of the pre-operative neurologicalabnormalities in determining prognosis.

Post-operative results were assessed on the basis of neurological findingsand also on the degree of return of their power to carry out their normalactivities. Results were considered good when there was completerestoration of ability, and their normal interests. Of these 31 patients,19 have shown good results (Table V). In eight, improvement has beenpoor, i.e. they have shown marked improvement in muscle tone and power,but disability is still there although the improvement continued. In threepatients subjective improvement has been slight. Though one has re-gained sphincter control satisfactorily, and another can move about thehouse (this was difficult for him pre-operatively), they feel that there hasnot been any significant change in their muscle power.

TABLE VRESULTS OF FORAMINAL DECOMPRESSION

Authors Cases Degree of improvement DeathGood Fair Slight, no change

or worseScoville (1961) .. 6 3 3Stoops and King 49 28 15 1 post-op.

(1962) (2 untraced) complication3 other causes

Epstein et al. (1963) 14 5 6 3Present series (1967) 31 19 8 3

(1 untraced)Post-operative physiotherapy is considered very important, and at least

once a week or fortnight during the first year or two the patient shouldreceive the supervision and guidance of a trained physiotherapist.

DiscussionOther operative procedures designed to relieve cord compression have

not proved satisfactory. Simple cord decompression by laminectomyin different series of patients has not yielded such good results as in thepresent series where it was combined with root decompression (Table V).A recent recommendation of laminectomy and leaving the dura open hasalso not yielded such satisfactory results. Attempts to chisel off theventral bony spurs have proved uniformly disastrous, though it has beensuccessful in Allen's personal series (1952). Transdural approach to themedian protrusions is also hazardous. Laminectomy with or withoutsection of the ligamentum denticulatum as advised by Kahn (1947) didnot improve results in Scoville's series (1961), and sometimes severelyworsened the long tract signs. This procedure has also been abandonedby some workers (Mayfield, 1955; Bradshaw, 1957).

248


The anterior approach for removal of a cervical disc with subsequentfusion is commended for single space disc prolapse with or withoutsubluxation, and when the diagnosis of spondylosis is absolutely certain.However, Logue (1967) has encountered spinal cord angiomas, secondarydeposits, and syringomyelia cysts when the pre-operative diagnosis wasspondylotic myelopathy. These conditions would have been missed if ananterior approach had been made. In spondylosis, calcified protrusionsand osteophytes broaden the intervertebral surface, and the neck becomesmore stable; in these cases even careful laminectomy and excision of theposterior wall of the intervertebral foramina usually do not impart anymarked instability even when several roots are decompressed.Laminectomy with foraminal decompression in cases of spondylotic

myelopathy was occasionally practised as early as 1952 (Brain et al.).Since then the advantage of foraminotomy over other procedures has beennoted by various workers including ourselves (Table V), although the

TABLE VIRESULTS FOLLOWING LAMINECTOMY

Author Improvement Unchanged TotalGood Fair Slight or worse

Epstein and Davidoff (1951) 1 1 2 4Northfield (1955) .. .. 13 - 9 16 38Arnold (1955) .. .. 2 2 1 3 8Walsh and Mackenzie

(1956) .. .. .. 13 4 11 28Segerberg (1956) .. 3 4 - 7Taylor (1964) .. .. 3 2 6 4 15

Tota! .. .. .. 22 22 20 36 100

explanations are different. Most workers comment that this remarkableimprovement in the result is due to a release of the anchoring effect of thespinal root sleeves which permit a dorsal migration of the cord (Scoville,1961; Stoops and King, 1962; Epstein et al. 1963). We have no doubtthat foraminal decompression of roots and removal of the dense periduralfibrous tissue are responsible for this remarkable change in the results.It is felt that this is not due to the removal of the tethering effect and dorsalmigration of the cord from the bony spur (which in fact does not occur),but to release of the important radicular arteries so long compressed, witha resultant improvement in the blood supply of the cervical spinal cord.The foraminal compression may be by fibrous tissue only and in somecases it has been found that bony changes were minimal while fibrosiswas dense.The radicular arteries are the main feeders of the anterior spinal artery,

and their levels of origin usually correspond to the levels commonlyaffected with spondylosis (Table III). In myelopathy vascular occlusiveanoxia is slow and chronic, never acute and rarely complete. Thisprobably explains why operative radicular decompression brings aboutimprovement. It is true that if the necrosis and cavitation have already

249

B. G. CHAKRAVORTY

taken place in the cord substance (recognized clinically by features ofnearly complete transection), this operative foraminal decompression willbe of little value.Even extreme pressure on the nerves does not impede conduction of

nerve impulses. Grundfest (1936) exposed nerves to a range of pressure2,000-7,000 lb./sq. inch, and still there was no defect in nerve conduction.On the other hand, Causey (1955) pointed out that vascular obstructionwithout interfering with the fibres can block impulse conduction, and thatthis ischaemic block was reversible. This theory may explain why the rateof post-operative improvement is so high after the decompressionoperation.The question may arise that there may be many elderly persons with

gross radiological narrowing of the cervical intervertebral foramina whoare free from myelopathy. On the other hand, there are some patientswith minimal radiological evidence of one-space narrowing with grossmyelopathy. It is possible that the former group have at least one majorradicular artery spared which is sufficient to maintain the nutrition of thecervical cord, whereas in the latter it may well be that the solitary radicularartery has been involved.

It is possible that in the pathogenesis of this syndrome no single factoris responsible, as direct compression, traction, venous stasis and ischaemiamay all play a part. Clinically and histologically the majority of casesof cervical myelopathy resemble those of the anterior spinal arterysyndrome, but at operation or autopsy they do not show a sufficientdegree of cord compression or traction to explain the condition. As theoperation to release the strangled radicular vessels brings improvementto the patient, only the ischaemic hypothesis provides an adequateexplanation.

ACKNOWLEDGEMENTSMy sincere thanks are due to Professor H. W. Rodgers and Mr. A. R.

Taylor of the Queen's University of Belfast, who gave me all possibleguidance and co-operation during the anatomical and experimentalstudies in this connection. I am also grateful to Professor G. W. Causeyof the Royal College of Surgeons of England for his constructive criticismin the final preparation of this lecture. I am also indebted to my col-leagues in Belfast and in Calcutta for their valuable help, and to my wife,Dr. Jayanti Chakravorty, for her technical assistance throughout thisstudy.

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ARTERIAL SUPPLY OF THE CERVICAL SPINAL CORD AND ITS