Hydrodynamic mechanism of syringomyelia: its relationship ... · hindbrain hernia....

J. Neurol. Neurosurg. Psychiat., 1965, 28, 247

Hydrodynamic mechanism of syringomyelia:its relationship to myelocele

W. JAMES GARDNER'

From Cleveland, Ohio, U.S.A.

'Syringomyelia found in an adult is a rest of acongenital hydromyelia ... which cuts itself off fromthe central canal posteriorly.' (Leyden, 1876).

The thesis of this present communication is thatsyringomyelia originates in embryonal life as a resultof overdistension of the neural tube. In its simpleform the syrinx consists merely of a dilated centralcanal of the cord. More commonly, it is a ramifyingdiverticulum originating in the central canal orfloor of the fourth ventricle and dissecting along apath of least resistance paralleling fibre tracts. Ineither event the syrinx is not 'cut off' but during lifeis kept distended with ventricular fluid that enters itwith each pulse beat because the outlets of thefourth ventricle did not develop properly.The above concept evolved quite serendipitously

because of an inadequacy in radiological equipmentat the Cleveland Clinic Hospital in the 1930s. Inthose days pneumoencephalography could be per-formed quite effectively in a room of the surgicalpavilion equipped to make films in the uprightposture. For ventriculography requiring the hori-zontal posture, it was necessary to move the patientsome distance from the surgical pavilion whereresuscitative measures were inadequate. For thesereasons, in cases of suspected brain tumour withoutpapilloedema, pneumoencephalography was pre-ferred to ventriculography and was employed even inposterior fossa cases. Because of this practice thepneumoencephalographic picture of the cerebellartumour gradually unfolded (Gardner and Nosik,1942). It was found to consist of an absence of airin the ventricles, a midline position of the supra-callosal sulcus, and a filling defect in the cisternamagna outlining a cerebellar hernia. In operatingupon such patients, the anticipated tumour some-times proved to be a congenital hernia of thehindbrain resembling that seen in the infant withmyelocele, and below this hernia was a cystic spinalcord. As a result of such experiences the light gradu-ally dawned that this was symptomatic syringo-'Present address: 930 Hanna Building, Cleveland, Ohio.

bulbia with asymptomatic syringomyelia. Then came

a patient with classic symptoms of syringomyeliawithout posterior fossa signs. Pneumoencephalo-graphy revealed the same picture and operationagain disclosed a congenital hernia of the hindbrainand a cystic cord distended with clear, colourlesscerebrospinal fluid. Separation of the impactedcerebellar tonsils allowed the ventricular fluid topulsate freely through the previously impacted fora-men of Magendie. After this decompression, thepatient's symptoms improved.A case of particular significance to the present

discussion was encountered in October 1955(Gardner, Abdullah, and McCormack, 1957). Thispatient had classic symptoms of syringomyelia andsyringobulbia. Instead of the anticipated hernia ofthe hindbrain, operation revealed a dilated fourthventricle enclosed by a membrane representing an

unperforated rhombic roof. This so-called Dandy-Walker malformation is a recognized cause ofcongenital hydrocephalus, that, along with hydro-myelia, has been reported in infants with myelocele(Benda, 1952; Dandy, 1921). This further evidence ofa relationship between adult syringomyelia and in-fantile myelocele led to a careful search for indicationof failure of perforation of the rhombic roof incases of congenital hernia of the hindbrain. In thiscondition also, a similar membrane frequently was

found enclosing the foramens.During the past 25 years the cerebellum has been

exposed in 74 patients with syringomyelia. In eachcase there was a congenital deformity ofthe hindbrainresembling that found in the infant with myelocele.In many instances the foramen of Magendie was

closed by a membrane. Fluid aspirated from thedistended syrinx always was clear and colourlesssuggesting an origin in the choroid plexus. When dyeor radiographic medium was injected into theventricles it passed into the syrinx. These observa-tions indicate that the syrinx communicates with thefourth ventricle and is distended with fluid entering itbecause of failure of the foramens to open adequatelyin prenatal life. A brief review of the embryological

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development of the cerebrospinal fluid spaces ispertinent to the present discussion.

EMBRYOLOGY

The neural tube is a single cavity consisting of theventricles and central canal of the cord. In 1917Weed showed that by the sixth week of embryonallife this tube is distended with fluid that has begun tofilter through attenuating areas in the membranousroof of the primitive fourth ventricle. By the eighthweek the pressure of this filtrate has dissected openthe entire subarachnoid space. During this criticalperiod the filtration pressure causes a further dilata-tion of the primitive ventricles and central canal(Fig. 1). This embryonal hydrocephalus and hydro-myelia, better termed 'hydrocephalomyelia' since itis a single cavity, becomes compensated long beforeattenuating areas in the roof of the fourth ventricleperforate to form the foramens. Weed postulatedthat if attenuation had not rendered the rhombic roofadequately permeable during this critical sixth toeighth week period, a sufficient quantity of fluidcould not escape from within the distended lumen(obstructive hydrocephalus) to complete the dissec-tion of the subarachnoid spaces. Then communicat-ing hydrocephalus would prevail regardless ofwhether the foramens subsequently opened. Thus,almost a half century ago, Weed offered a logicalexplanation as to why congenital hydrocephalus is socommon, and why it may be either obstructive orcommunicating, or more commonly a combinationof both; also, although he failed to mention it,why hydromyelia so often is associated with con-

a b

genital hydrocephalus (Cameron, 1957). That Weed'sviews are not more widely accepted today is a strik-ing example of the time lag that so frequently in-tervenes between laboratory demonstration andclinical acceptance.

In syringomyelia of adult life as in myelocele ofinfancy one may find the combination ofhydrocepha-lus, hydromyelia, and an unperforated rhombicroof (Gardner, 1959a). Both disorders, therefore,appear to represent the postnatal persistence ofconditions that are physiological in the embryo.The unperforated rhombic roof is usually concealedin the impaction of a congenital hernia of the hind-brain (Fig. 2) but occasionally it is quite obviousin an expanded Dandy-Walker malformation(Gardner, 1959b).

Chiari, in 1891, attributed congenital hernia of thehindbrain to 'hydrocephalus of the cerebrum'.His type 1 (Fig. 3), consisting chiefly of a herniationof the tonsils, he described in an adult with hydro-cephalus and hydromyelia; his more severe type 2,since then unjustly labelled (Daniel and Strich, 1958;Greenfield, Blackwood, McMenemey, Meyer, andNorman, 1958) the 'Arnold'-Chiari malformation,he described in an infant with hydrocephalus,hydromyelia, and myelocele. In his extraordinarily ucomplete descriptions (Chiari, 1895), like most sub-sequent authors, he failed to note that in many cases,membranes enclosing the foramens of the fourthventricle bear mute evidence of the fact that therhombic roof has failed to perforate (Gardner,1959b). This oversight is due to the fact that thesemembranes are concealed in the impacted hernia.That they frequently remain intact is rather surpris-

c

FIG. 1. The physiological hydrocephalus and hydromyelia ofembryonal life.

a. An 18 mm. pig embryocorresponding to the sixth weekin the human, with the cerebrospinalfluid spaces outlined by precipitatedcrystals ofPrussian blue. Theventricular fluid is just beginning topush through two permeable areas inthe rhombic roof. Arrows indicate thearea membranacea superior andinferior.b. A 26 mm. pig embryocorresponding to the eighth week inthe human reduced to the same sizeas a, to depict the increasingdistension of the neural tube. Thesubarachnoid spaces have expandedand precipitated crystals ofPrussianblue were found in the venous duralsinuses.c. A six-week human embryophotographed by transillumination inits amniotic sac. The lighter areascorrespond to the darker areas in a.

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FIG. 2a. Diagram showing the outline of the embryonal neural tube superimposed upon the configuration of the maturecentral nervous system. The outlet ofthefourth ventricle is bridged by apermeable membrane thatfunnels the pulsations ofthe ventricularfluid into the central canal ofthe cord (arrow). Despite its vulnerable position, persistence ofthis membrane(area membranacea inferior of Weed) may be demonstrated not only in every Dandy- Walker malformation but also inmany Arnold-Chiari malformations.b. After the foramens open, the pulsations escape freely into the subarachnoid space (arrow) onto the outer surfaceofthe spinal cord. As a result ofthis bypass the central canal is compressed and becomes a vestigial structure. The ventricu-larfluidpulse pressure is progressively damped as it descends in the expansible dural sac. The pulse pressure recordings arefrom Bering (1955).c. Diagram of the neural tube in syringomyelia. The ventricles frequently are enlarged but the intracranial pressureis normal (compensated hydrocephalus). The foramens of the fourth ventricle are compressed by impaction in a congenitalhindbrain hernia. The central canal at the level of the hernia is usually patent but cannot dilate because of the impaction.Below the impaction the central canal is enormously dilated with loss of its ependymal lining except for small areas on thewall adjacent to the anterior commissure. Dilatation is greatest in the cervical region where the transmitted ventricularfluidpulse pressure is widest. A false diverticulum of the neural tube, as shown below the cut, may develop at any level toform a 'true syrinx' that parallels the central canal and is entirely lacking in ependyma. It may originatefrom thefloor ofthe fourth ventricle (syringobulbia) and by its downward extension, collapse the central canal.d. Diagram of the neural tube in myelocele. The severe hindbrain hernia has telescoped the cervico-medullaryjunction and closed the communication between fourth ventricle and dilated central canal. The ependyma lining the canalis much better preserved than in the adult form. The intracranial pressure is increased, the ventricles are greatly dilated(uncompensated hydrocephalus), and in certain cases their ependymal lining may be lacking. False diverticuli of the dilatedventricles or central canal may be present.

ing since their position renders them liable to ruptureas the hydrocephalic head is squeezed in its passagethrough the birth canal. Chiari's demonstration ofthe presence of hydromyelia and hydrocephalus withboth this adult type 1 and his infantile type 2 hernia-tions supports the present theory that syringomyeliain adults is the result of a mild degree of overdisten-sion of the neural tube compensated in utero, whilethe hydrocephalus and hydromyelia that accom-pany myelocele result from a severe degree thatfailed to become compensated (Gardner, 1961).Chiari, however, did not attribute the hindbrainhernia to extrusion resulting from growth of thehindbrain in a posterior fossa too small to accom-modate it. Apparently he failed to recognize the

abnormally low position of the transverse sinus(Cameron, 1957; Daniel and Strich, 1958) that hadseriously reduced the size of the posterior fossa.

Padget (1957) has shown that the anlage of thetransverse sinus and tentorium arises far anteriorlyand is pushed posteriorly by the expanding forebrain(Fig. 4). This excursion is almost completed by thetwelfth week, at which stage the brain still is littlemore than a thin-walled bag of water containing arelatively enormous choroid plexus. In view of thisfact, it follows that the excursion of the primitivetransverse sinus is the result of fluid expansion of theforebrain rather than the growth of solid tissue aswas suggested by Barry, Patten, and Stewart (1957).Furthermore, since the pressure of fluid in a closed

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FIG. 3. Surgical exposure in a patient with syringomyelia.The cerebellar tonsils are protruding through the foramenmagnum as in Chiari's type I malformation. The secondcervical nerve roots slant upward and the cervico-medullaryjunction bulges posteriorly as in Chiari's type 2 malforma-tion. Below this the cystic cord, tethered laterally by thedentate ligaments, has collapsed in the antero-posteriorplane as a result of the pre-operative encephalogram (seeFig. 6).

FIG. 4. The transverse sinus with itsattached tentorium originates farforward and is pushed posteriorly bythe expanding forebrain. If it is pushedtoo far, the developing posterior fossawill be too small, as in the Chiarimalformation. If it is not pushedfarenough, this fossa will be too large, as inthe Dandy- Walker malformation. Themigration of the primitive straight sinusrather than the transverse sinus is shown,since the former is identifiable at anearlier stage than is the latter. Therelatively large size of the choroidplexus indicates its functional significance(redrawn from Padget, 1957).

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system is exerted equally in all directions, this ex-

pansion of the forebrain at the expense of the hind-brain can be explained only on the basis of greateryielding qualities inherent in the coverings of theforebrain. In other words, the migration of the primi-tive transverse sinus is the result of hydrodynamicforces in which the expansion of the forebraincompetes with that of the hindbrain.

If, due to inadequate permeability of the rhombicroof, the physiological hydrocephalus of the fore-brain attains a pathological degree, it will push themovable partition too far caudally. This will result ina posterior fossa too small to accommodate thelater growth of the hindbrain so that its posteriorportion will be extruded through the foramenmagnum. Chiari's hypothesis that hernia of thehindbrain is due to 'hydrocephalus of the cere-brum', therefore, still will apply. If the size of theposterior fossa is severely reduced by this process,the cerebellar portion of the resulting hernia willconsist of the earlier developing vermis (Chiari'stype 2); if its size is reduced to a lesser degree, thecerebellar hernia will consist of the later developingtonsils (Chiari's type 1). In the severe herniations thedilated central canal is kinked and cut off from thefourth ventricle by the telescoping of the uppercervical cord. The accompanying operative photo-graphs illustrate that gradations exist betweenChiari's types 1 and 2.

Contrariwise, if the coverings of the hindbrain ofthe hydrocephalic embryo are relatively more yield-ing than those of the forebrain, the resulting over-

expansion in the primitive hindbrain area will inter-fere with the posterior migration of the transversesinus and result in an abnormally large posteriorfossa. The developing hindbrain then will be in-adequate to fill this large fossa and the remainingspace will be occupied by a dilated fourth ventricleconstituting the Dandy-Walker malformation. Thus,inadequate permeability of the rhombic roof, as

proposed by Weed (1917), will explain not onlycongenital hydrocephalus with its hydromyelia butalso the accompanying hindbrain malformations ofChiari and of Dandy and Walker (Gardner, 1964).All these features are encountered in the adultwith syringomyelia as well as in the infant withmyelocele (Gardner, 1959a).

Clinicians and pathologists recognize that ob-

struction of the ventricular system at any level re-

sults in uniform dilatation of that part of the systemabove the obstruction. This observation, quite truein cases developing in postnatal life, led to the promptacceptance of foramenal obstruction as the cause ofthe dilated fourth ventricle in the Dandy-Walkermalformation. By the same token, it has seriouslydelayed our recognition that this foramenal obstruc-

tion is the cause of the compressed fourth ventriclein the Chiari malformation.

THE HYDRODYNAMIC THEORY

Every living membrane, of necessity, is permeableto fluid. The difference between a perforated and apermeable membrane is merely the size and numberof its holes (Gardner, McCormack, and Dohn,1960). In the rhombic roof such holes,whether macroscopic or ultramicroscopic, may becompetent to allow passage of ventricular fluid at thesame rate as it is formed, but incompetent to allowpassage of the sudden spurt imparted to it by eachpulse beat of the choroid plexus. This may be com-pared to a window screen readily permeable to abreeze but which bulges in response to a sudden gust.In syringomyelia the intracranial pressure is normalalthough the foramens of the fourth ventricle mayappear to be 'sealed' by such membranes. This fact,together with observations during surgery, indicatethat it is not an increase in mean pressure of the ven-tricular fluid which drives it down into the spinalcord, but rather the gentle, oft repeated water ham-mer effect of its pulse pressure. In other words,although the foramens of the fourth ventricle arecompetent to equalize the mean pressures within andwithout the lumen, they may not be competent toequalize the pulse pressures. According to this theorythe formation of a syrinx is a process of hydrodis-section comparable to that which is responsible fordeveloping the subarachnoid space in the embryo. Itdiffers in that the hydrodynamic force is purelypulsatile and is misdirected. Apropos at this point isGreenfield's (1958) description of the syrinx: 'Wherethere is a recent extension . . . the appearancessuggest tearing of the tissues and transudation ofserous fluid into them.'Bering (1962) pointed out that the beating of the

choroid plexus transmits to the ventricular fluid acompression wave, absorbed in part by the spurtingof fluid from the fourth ventricle into the distensiblespinal subarachnoid space. He found symmetrichydrocephalus did not develop if the choroid plexuswas removed from one ventricle, and the animal wasmade hydrocephalic by the injection of kaolin intothe cisterna magna. In the ventricle lacking a choroidplexus the pulse wave was feeble. This ventricleremained small while the other dilated, even thoughthe foramens of Monro were patent. If unilateralchoroid plexectomy was done in animals with estab-lished hydrocephalus, that ventricle shrank whilethe opposite one continued to enlarge by virtue ofthe force of the compression wave generated by itschoroid plexus. In this fashion, Bering demon-strated that dilatation of the mature neural tube is a

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FIG. 5. In experimental hydrocephalus, injection ofPantopaque into the obstructed fourth ventricle shows thatit communicates with a dilated central canal. Thisconstitutes acquired hydrocephalomyelia. (By courtesyof McLaurin et al., 1954; with permission of thepublisher).

function of the ventricular fluid pulse pressure ratherthan of its mean pressure.

Previous experimental studies by McLaurin,Bailey, Schurr, and Ingraham (1954) had shown thatdilatation affecting the entire neural tube, that is, thecentral canal of the cord as well as the cerebralventricles, followed intracisternal injection ofkaolin. When a radiopaque medium was injected intothe ventricles of their animals, it did not escapefrom the foramens into the subarachnoid spacebut passed from the fourth ventricle into a dilatedcentral canal. Thus, hydromyelia developed when theforamens of the fourth ventricle were rendered in-competent. This demonstration supports the presenthydrodynamic theory of the mechanism of syringo-myelia (Fig. 5).

RADIOLOGICAL AND SURGICAL FINDINGS

The diagnosis of syringomyelia may be confirmedby air study. With proper technique (Greenwald,Eugenio, Hughes, and Gardner, 1958) the pneu-moencephalogram characteristically will disclose afilling defect in the cisterna magna as well as failureof air to enter the ventricles. Below the filling defectthe films may show a collapse of the cystic cord (Fig.6). Collapse occurs because withdrawal of the sup-porting fluid from the subarachnoid space permitsthe fluid within the syrinx to gravitate downwardand to filter through its attenuated walls so that theupper portion is empty. This collapse can take place

FIG. 6. A pneumoencephalogram with thepatient in the sitting position is reproduceddiagrammatically. Air has failed to enter theventricles.a. A film made immediately after thecomplete exchange disclosed herniatedtonsils outlined by air in the cisterna magnaand a distended cord below.b. A later film showed that the removal ofthe subarachnoid fluid had allowed the fluidin the syrinx to gravitate downward and tofilter through its attenuated walls so that theupper portion collapsed. This drainage offluidfrom the syrinx created a negativepressure within the ventricles which suckedthe cerebellar hernia up throuigh the foramenmagnum.

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only in the antero-posterior direction because thedistended cord is anchored laterally by the dentateligaments. Pneumoencephalography was done pre-operatively in 46 of 74 cases that constitute the basisof this report. The films disclosed no air in the ven-

tricles in 24 cases. In 22 cases some air gained en-trance to the lateral ventricles indicating that theywere dilated in 14 and normal in eight. These radio-logical findings constitute further evidence of in-competence of the foramens of the fourth ventricle.

Proper surgical treatment of syringomyeliaconsists not in incising the syrinx but in dissectingopen the foramen of Magendie to permit the escapeof the confined ventricular fluid pulsations pre-viously funneled into the syrinx. These pulsationsthen will be shunted past the central canal into thecisterna magna, restoring the dynamics of the cere-brospinal fluid to normal. Through a midline in-cision and with the patient in the sitting position,the foramen magnum is enlarged posteriorly, thelamina of the upper cervical vertebrae are removed,and the dura is opened widely. The cerebellar tonsilswill be found elongated and herniated into theforamen magnum so that the passageway betweenthem and the medulla is squeezed shut by theimpaction (Fig. 7). Furthermore, the surgeon willobserve that this impaction is accentuated momen-tarily by a downward excursion of the tonsils thatoccurs with each pulse systole. The cerebellar herniain syringomyelia not only interferes with the escapeof the ventricular fluid pulse wave from the lumenof the neural tube, but the impaction of this herniaalso creates a mild subarachnoid block at the fora-men magnum. These two hydrodynamic factorsserve to exaggerate the ventricular fluid pulse waveand to funnel it toward the take-off of the centralcanal beneath the obex. The surgeon may relievethe subarachnoid block by enlarging the foramenmagnum and the ventricular block by dissectingopen the passageway between the cerebellar tonsilsand the medulla.

In many cases the foramen of Magendie will bebridged by a membrane representing an unperforatedrhombic roof (Fig. 8). Incision of this membranewill disclose the floor of the fourth ventricle, and a

funnel-shaped upper end of the central canal thenmay be demonstrated beneath the obex (Fig. 7b).Frequently, there is an unusually deep median rapheleading into it. This funnel-shaped entrance shouldbe plugged with a bit of muscle or a wisp of cottonin order to close off the central canal from the fourthventricle. This plugging procedure, initiated in 1957,has been accomplished in each of the last 33 cases.A syrinx opening on to the floor of the fourthventricle was not described in any of the operativenotes. However, such a diverticulum could readily

be overlooked, particularly if it originated in a deepmedian raphe, which in reality constitutes an exten-sion of the central canal. In concluding the operationit is essential that the dura be left open, for if it isclosed the foramen of Magendie once more will besqueezed shut and the partial subarachnoid obstruc-tion at the foramen magnum re-established. Inrecent cases, the insertion of a patch of plastic duralsubstitute has permitted a relaxed closure of the durawhich does not re-impact the hindbrain hernia. Thisimportant step improves convalescence by prevent-ing access to the subarachnoid space of protein-laden interstitial fluid escaping from the raw surfaceof the nuchal muscles. Such access is indicated byspinal fluid protein levels up to 300 mg. per 100 ml.persisting in some cases for weeks after operation.The presence of excessive amounts of protein hasbeen shown to interfere with the absorption ofcerebrospinal fluid (Gardner, Spitler, and Whitten,1954). -

It is not only unnecessary but it may be inadvisableto carry the laminectomy low enough to expose thesyrinx, for the reason that extensive laminectomysometimes has been followed by a severe flexiondeformity of the cervical spine. In this series of 74cases, however, the syrinx was disclosed in 62, thusconfirming the diagnosis. In most of these 62 casesthe correct diagnosis was indicated pre-operativelyby the clinical findings and/or the pneumoencephalo-graphic picture. In the 12 remaining cases, althoughthe syrinx was not seen, the diagnosis was arrived atbecause of a characteristic dissociated sensory loss,a typical pneumoencephalographic picture, or acombination of both. In some instances, indigocarmine, previously injected into a lateral ventricle,was aspirated from the syrinx at operation. In onepatient indigo carmine was injected into the exposedsyrinx, after which manual compression of the cysticcord caused the dye to appear on the floor of thefourth ventricle. In one early case in which a highcervical cord tumour was suspected a cisternalmyelogram was attempted. The films showed thatthe lipiodol had been injected into a caudally dis-placed fourth ventricle. Twenty-four hours later,most of the lipiodol remained in the fourth ventricle,but a drop of it was observed in the centre of thespinal canal at the level of the first thoracic vertebra,presumably in the syrinx. In a later case, Pantopaqueinjected into a lateral ventricle also did not escapefrom the fourth ventricle into the subarachnoidspace but gradually trickled in a fine stream throughthe upper end of the central canal into the syrinx(Fig. 9).Because the syrinx is distended during life the

surgeon has an opportunity, seldom afforded thepathologist, to aspirate fluid from it. In each of 26

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FIG. 7. Surgical exposure in a patient with syringomyelia.

FIG. 7a. Impaction of the cerebellar hernia has squeezedshut the foramen of Magendie and has caused a partialsubarachnoid block at the foramen magnum. The posteriorinferior cerebellar arteries are redundant.FIG. 7b. The cerebellar tonsils have been retracted and anerve hook introduced to demonstrate the entrance to thecentral canal. The operative results are improved if thisfunnel-shaped communication is closed off by impacting init a tiny muscle plug or wisp of cotton.

FIG. 8. Surgical exposure in a patient with syringomyelia.Retraction of the herniated cerebellar tonsils in this casediscloses a membrane (arrow) entirely enclosing the fora-men ofMagendie. Its attachments indicate that it representsa persistent portion of the embryonic rhombic roof.

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FIG. 9. Pantopaque ventriculogram in a patient withsyringomyelia, made with the head erect. The medium hasnot escaped into the subarachnoid space but is held in thefourth ventricle and in a caudal diverticulum between thecerebellar tonsils. At operation this diverticulum was foundto be caused by dense pia-arachnoidal adhesions that boundthe external surface of the tonsils to each other and to thecervical cord, thus forming the pocket. On the originalfilma fine trickle ofPantopaque could be plainly seen extendingdownwardfrom the region ofthe obexfrom where apparent-ly it droppedfreely into the syrinx to come to rest oppositethe tenth thoracic vertebra (compare with Fig. 5).

TABLE ICOMPARISON OF TOTAL PROTEIN CONTENT OF CEREBRO-

SPINAL FLUID IN SYRINX AND LUMBAR FLUID

Protein Content of Cerebrospinal Fluid (mg./100 ml.)

Syrinx Lumbar

16 17 23 23 23 29 29 33 33 42 33 19 45 45 41 41 41 41 41 5941 50 30 32 35 41 75 90 41 50 15 30 20 38 35 33

cases in which this was accomplished, the fluid ap-

peared to be normal cerebrospinal fluid. In 18 of thesecases the protein content of the syrinx fluid was com-

pared with that of the lumbar fluid. Protein rangedfrom 16 to 90 mg. per 100 ml. and that of the corre-

sponding lumbar fluid ranged from 15 to 59 mg. per

100 ml. (Table 1). In 10 cases the protein content ofthe syrinx fluid was lower than that of the cor-

responding lumbar fluid and thus resembled ven-

tricular fluid more closely than did the lumbar fluid.Contrariwise, in three cases of cystic tumours of thecervical cord with symptoms suggesting syringo-myelia, the fluid was thick and yellow with a totalprotein content of 2,500, 3,500, and 5,000 mg. per

100 ml., respectively. It has been shown that fluid

accumulating in cystic gliomas is the result of diffu-sion of plasma through the walls of the tumourcapillaries (Gardner, Collis, and Lewis, 1963). Ittherefore represents interstitial (intercellular) fluid,whereas cerebrospinal fluid is transcellular in origin,which accounts for its low protein content. Theinterstitial fluid escaping from an ependymomaoriginating in the closed adult central canal mayeither redistend this canal or create a false passagethat parallels it. Such tumours of the cervical cordmay account for the fact that occasionally a patientwith the clinical picture of syringomyelia will benefitby radiation therapy.Of these 74 patients with syringomyelia, the in-

competence of the foramen of Magendie was due toa Chiari malformation in 68, to a Dandy-Walkermalformation in three, and to a congenital cystobstructing the foramen of Magendie in three (Fig.10). Such hindbrain malformations may account forsome of the symptoms attributed to syringobulbia.

In all 68 cases of syringomyelia associated with theChiari malformation, the cerebellar portion of thehernia was constituted by the tonsils rather than bythe vermis as is usually the case with the severe in-fantile forms. The cerebellar tonsils were describedas protruding 'into' the foramen magnum in fivecases and 'through' it in 15. The tonsils reached thelevel of the first cervical lamina in 29 cases, the secondin 18, and the third in one. In 29 instances the herni-ated tonsils were cone-shaped and bound down to themedulla by a dense band of piarachnoid adhesions(Fig. 11). In 28 cases, the surgeon described a caudaldislocation of the obex, indicating a downwarddisplacement of the medulla (Fig. 12A). In 36 casesthe second cervical nerve roots pursued a cephaladcourse to their foramens of exit, indicating that thisportion of the cervical cord was dislocated down-ward (Fig. 3; Fig. 12B). A posterior bulging of themedulla was described in 17. In 24 cases the foramenof Magendie was enclosed by a membrane whoseattachments indicated that it represented the un-perforated rhombic roof. This membrane was linedby ependyma in two of the younger patients, and inone instance it contained choroid plexus. If these 24cases are added to the three with Dandy-Walkermalformation and to the three with cyst of the fora-men of Magendie, there was a total of 30 cases inwhich a membrane entirely closed the foramen. Asthe membrane was incised, fluid spurted through itwith each pulse beat. In addition there were eightcases in which a membrane partially enclosing theforamen was described. Such membranes surelycannot be considered merely incidental but a findingwhich would be anticipated if during embryonal lifethe rhombic roof were less permeable and cor-respondingly tougher than normal. At operation it

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FIG. 10. Surgical exposure in a patient with syringomyelia.a. A thin-walled cyst, entirely separatefrom the arachnoid,fills the cisterna magna. Its resemblance to the Dandy- Walkermalformation is obvious in this view.b. The cyst is blocking the foramen of Magendie. Although microscopically it resembled arachnoid, its position andattachments indicate that it represents an unperforated rhombic roofwhose inner and outer layers became separated by anaccumulation ofventricular fluid between them (Gardner et al., 1957). The containedfluid was clear and colourless with atotalprotein content of29 mg. per 100 ml. Fluid with such a low protein content cannot be ofpathological origin but mustcome from the choroidplexus.c. After evacuation the anterior wall of the cyst was found to have displaced the vermis upward and to have sealed theforamen of Magendie between the flattened tonsils.

is not feasible to examine the foramens of Luschka,but necropsy study in cases of imperforate foramenof Magendie (Gardner et al., 1957; Russell, 1949,cases 19 and 39) and of hydromyelia (Bezi, 1931)has disclosed similar membranes at the foramens ofLuschka. In this more protected locus these mem-

branes are apt to preserve the microscopic appearanceof the rhombic roof, whereas at the foramen ofMagendie the glial layer is usually missing and theyresemble pia arachnoid.The above figures do not indicate the true incidence

of these features inasmuch as the operations were

performed by several surgeons who, particularly inthe early cases, undoubtedly overlooked some ofthem. For example, the lower medulla must havebeen dislocated caudally in all cases in which theupper cervical cord was so dislocated. The trueincidence of unperforated rhombic roof undoubtedlywas higher than the figures indicate, since this delicatemembrane enclosing the foramen of Magendie maybe readily torn by the surgeon's attempts to expose

it. In some instances the tonsils were so adherent thatthe attempt to separate them had to be abandoned.In these cases the foramen of Magendie was notvisualized and the fourth ventricle was opened byincising the vermis. In one early case in which it was

stated that the cord was not cystic because it was notfluctuant, the operative photograph (reproduced inFig. 3) clearly shows a wide collapsed cord thatbefore encephalography must have been distendedwith fluid. When the herniated tonsils were retractedin this case, a membrane was not disclosed and thesurgeon therefore stated that the foramen ofMagendie was patent. However, it is apparent thatin this impacted hernia of the hindbrain the fora-men, though patent, could not have been competentto allow free passage of the ventricular fluid pulsewave.

POST-OPERATIVE RESULTS

Immediately following operation there was improve-ment in some of the symptoms of 52 patients, nochange in 11, worsening of the pre-operativesymptoms in six, and five patients did not survivethe operation. Of the pre-operative symptoms, sub-jective numbness, dissociated sensory loss, and painwere most likely to be improved, although motorpower, astereognosis, ataxia, and bulbar palsies alsowere benefited in some patients. In several instancesbulbar or long-tract symptoms, non-existent before,were precipitated by the operation. This was attri-

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FIG. 11. Surgical exposure in syringomyelia. The cone-shaped cerebellar tonsils are bound down by a band ofthickened pia-arachnoid. The cystic cord has collapsedbecause ofa pre-operative encephalogram.

( I)

FIG. 12. Congenital hernias of the hindbrain in adults resembling those found in infants with myelocele.a. Separation of the herniated tonsils discloses the fourth ventricle whose lower end (arrow) reaches the level of C2.Below the 'obex there may be seen the posterior buckling ofthe cervico-medullary junction. The vermis is displaced caudallyalmost to the level of the foramen magnum.

b. Exposure in a similar case demonstrating a pronounced upward course of the second cervical nerve root. In neither ofthese sejere herniations did the clinical picture indicate syringomyelia nor was a syrinx disclosed at operation. This suggeststhat in kvere adult Chiari malformation, as is true in the infantile cases, the central canal may be squeezed shut at the levelof the impaction.

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W. James Gardner

buted to oedema resulting from the sudden relief ofthe life-long compression of the medulla. In onepatient, bulbar symptoms developed several daysafteroperation, and necropsy disclosed a delayed intra-medullary haemorrhage. In two patients the pre-operative compensated hydrocephalus became un-compensated post-operatively to a degree thatnecessitated a ventriculo-jugular shunt. This wasattributed to the entrance of blood and interstitialfluid into the subarachnoid space. Following dis-charge from the hospital one patient had twoepisodes of spontaneous subarachnoid haemorrhagefrom which he fortunately recovered. In three patientsquadriparesis developed during operation. It wasattributed to compression of the pyramidal decus-sation by a high odontoid process because of flexionof the head. (In one-third of the cases, radiographsdisclosed the tip of the odontoid to be more than 10mm. above a line drawn from the posterior end of thehard palate to the base of the skull. This degree ofbasilar impression in syringomyelia is believed due tohydrocephalus unrecognized at birth and compensa-ted in childhood.) This operation, therefore, entails adefinite risk and should be reserved for those patientsin whom total disability is threatened by progressionof the symptoms.

Seventeen of these patients were operated uponbefore 1950 and thus provided an adequate follow-up. Of these 17 patients, one died of respiratoryarrest 18 hours after operation. In two patients thesymptoms were unchanged by the operation, and inthree the symptoms were worse. In eight patients, orone-half the survivors of this group, the symptomswere improved when the patients were seen afterintervals of 23, 17, 16, 15, 14, nine, seven, and sixyears, respectively. The symptoms in the remainingthree patients, seen 24, 13, and six years afteroperation, had been improved for five years, sevenmonths, and one year, respectively, and then re-cuffed.

MICROSCOPIC FINDINGS

Post-mortem material from eight cases of syringo-myelia was available for study. Fifty-six cross sec-tions from varying levels of these spinal cords werefound to have included the syrinx. In 24 the syrinxwas adjacent to the anterior commissure. In each ofthese the wall was partly lined with ependyma, withno ependyma elsewhere. This finding is consistentwith a distension of the central canal. In 31 sectionsthe wall of the syrinx was naked of ependyma.In these a central canal was present in its normalposition and separate from the syrinx. This finding isconsistent with a false diverticulum arising from someportion of the central canal or from the floor of the

fourth ventricle. In the remaining slide no ependymawas present either in the wall of the syrinx or else-where.

CONCLUSIONS

In acquired pathological states the terms early andmild as opposed to late and severe are virtuallysynonymous; in congenital malformations the op-posite is true. In either case, effective investigation ofa disease process begins with the study of mild formsand progresses to the more severe. This principle,followed quite unintentionally in the study of con-genital malformations of the hindbrain, led to theconclusion that syringomyelia is the mild expressionof an embryonic defect which in its severe form re-sults in myelocele.

In syringomyelia as in myelocele one finds theneural tube distended and imperforate, thus repre-senting postnatal persistence of the embryonic state.In the embryo the degree of distension of the neuraltube is determined by the permeability of therhombic roof, and permeability in turn depends uponattenuation. The end stage of this attenuation isperforation. Therefore, an imperforate rhombicroof persisting into postnatal life is evidence ofdelayed attenuation and impaired permeability ofthe structure in embryonic life.

In syringomyelia as in myelocele one encountersthe Chiari or occasionally the Dandy-Walker mal-formation. Both malformations can be explained bya pathological degree of distension of the embryonicneural tube, in which overdistension of the fore-brain competes with that of the hindbrain. Suchoverdistension (hydrocephalomyelia) tends to be-come compensated by the same mechanism as doesthe normal distension. If compensation occurssufficiently early the infant may appear normal, butthe imprisoned hydrodynamic stresses will eventuatein syringomyelia. In brief the cause of syringomyleiashould be sought not in the spinal cord but in thehindbrain.The anatomical evidence accumulated in this study

suggests that myelocele is due not to failure ofclosure but rather to rupture of the neural tuberesulting from a degree of overdistension too severeto permit of compensation. This mechanistic theoryis not supported by the findings of the experimentalpathologists who, on the other hand, have notexplained how an unclosed neural tube can becomeoverdistended.

REFERENCES

Barry, A., Patten, B. M., and Stewart, B. H. (1957). Possible factorsin the development of the Arnold-Chiari malformation. J.Neurosurg., 14, 285-301.

Benda, C. E. (1952). Developmental Disorders of Mentation andCerebral Palsies. Grune and Stratton, New York.

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Bering, E. A. Jr. (1955). Choroid plexus and arterial pulsation of cere-brospinal fluid; demonstration of the choroid plexuses as acerebrospinal fluid pump. Arch. Neurol. Psychiat. (Chic.), 73,165-172.

(1962). Circulation of the cerebrospinal fluid. Demonstration ofthe choroid plexuses as the generator of the force for flow offluid and ventricular enlargement. J. Neurosurg., 19, 405-413.

Bezi, 1. (1931). Assimilation of atlas and compression of medulla.Arch. Path., 12, 333-357.

Cameron, A. H. (1957). The Arnold-Chiari and other neuro-anatomi-cal malformations associated with spinal bifida. J. Path. Bact.,73, 195-211.

Chiari, H. (1891). Ober Veranderungen des Kleinhirns infolge vonHydrocephalie des Grosshirns. Dtsch. med. Wschr., 17,1172-1175.

(1895). Ueber die Veranderungen des Kleinhirns des Pons undder Medulla oblongata in Folge von congenitaler Hydro-cephalie des Grosshirns. Denkschr. Akad. Wissensch. Wiern.Mathnaturw. kl., 63, 71-116.

Dandy, W. E. (1921). The diagnosis and treatment of hydrocephalusdue to occlusions of the foramina of Magendie and Luschka.Surg. Gynec. Obstet., 32, 112-124.

Daniel, P. M., and Strich, S. J. (1958). Some observations on thecongenital deformity of the central nervous system known as

the Arnold-Chiari malformation. J. Neuropath. exp. Neurol.,17, 255-266.

Gardner, W. J. (1959a). Anatomic anomalies common to myelo-meningocele of infancy and syringomyelia of adulthoodsuggest a common origin. Cleveland Clin. Quart., 26, 118-133.

(1959b). Anatomic features common to the Arnold-Chiari andthe Dandy-Walker malformations suggest a common origin.Ibid., 26, 206-222.

(1961). Rupture of the neural tube: the cause of myelomeningo-cele. Arch. Neurol. (Chic.), 4, 1-7.

(1964). Diastematomyelia and Klippel-Feil syndrome; relation-ship to hydrocephalus, syringomyelia, meningocele, meningo-myelocele, and iniencephalus. Cleveland Clin. Quart., 31,19-44.

Abdullah, A. F., and McCormack, L. J. (1957). The varyingexpressions of embryonal atresia of fourth ventricle in adults.Arnold-Chiari malformation, Dandy-Walker syndrome,'arachnoid' cyst of cerebellum, and syringomyelia. J. Neuro-surg., 14, 591-607.Collis, J. S. Jr., and Lewis, L. A. (1963). Cystic brain tumoursand the blood-brain barrier. Arch. Neurol. (Chic.), 8, 291-298.McCormack, L. J., and Dohn, D. F. (1960). Embryonal atresiaof the fourth ventricle. The cause of 'arachnoid cyst' of cere-bellopontine angle. J. Neurosurg., 17, 226-237.and Nosik, W. A. (1942). Experiences with encephalography incerebellar tumor. Amer. J. Roentgenol., 47, 691-698.Spitler, D. K., and Whitten, C. (1954). Increased intracranialpressure caused by increased protein content in the cerebro-spinal fluid; an explanation of papilledema in certain cases ofsmall intracranial and intraspinal tumors, and in the Guillain-Barre syndrome. New Engl. J. Med., 250, 932-936.

Greenfield, J. G., Blackwood, W., McMenemey, W. H., Meyer, A.,and Norman, R. M. (1958). Neuropathology. Arnold, London.

Greenwald, C. M., Eugenio, M., Hughes, C. R., and Gardner, W. J.(1958). The importance of the air shadow of cisterna magna inencephalographic diagnosis. Radiology, 71, 695-701.

Leyden, E. (1876). Ueber Hydromyelus und Syringomyelie. VirchowsArch. path. Anat., 68, 1-26.

McLaurin, R. L., Bailey, 0. T., Schurr, P. H., and Ingraham, F. D.(1954). Myeolomalacia and multiple cavitations of spinal cordsecondary to adhesive arachnoiditis; experimental study.Arch. Path., 57, 138-146.

Padget, D. H. (1957). The Development of the cranial venous systemin man, from the viewpoint of comparative anatomy. Contr.Embryol. Carneg. Instn, 36, 79-140.

Russell, D. S. (1949). Observations on the pathology of hydrocephalus.Spec. Rep. Ser. med. Res. Coun. (Lond.), no. 265.

Weed, L. H. (1917). The development of the cerebro-spinal spaces inpig and in man. Contr. Embryol. Carneg. Instn, 5, 1-116.

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