Brain Injury, July 2010; 24(7–8): 988–994

ORIGINAL ARTICLE

A case-control study of cerebellar tonsillar ectopia (Chiari) andhead/neck trauma (whiplash)

MICHAEL D. FREEMAN1,2, SCOTT ROSA3, DAVID HARSHFIELD3,FRANCIS SMITH4, ROBERT BENNETT5, CHRISTOPHER J. CENTENO6,EZRIEL KORNEL7, AKE NYSTROM8, DAN HEFFEZ9, & SEAN S. KOHLES10,11

1Department of Public Health and Preventive Medicine, Oregon Health and Science University School of Medicine,OR, USA, 2Institute of Forensic Medicine, Faculty of Health Sciences, University of Aarhus, Aarhus, Denmark,3Private practice, 4Department of Diagnostic Imaging, University of Aberdeen, Aberdeen, Scotland, UK,5Oregon Health and Science University School of Nursing, OR, USA, 6Spinal Injury Foundation,

Westminster, CO, USA, 7Department of Neurological Surgery, Columbia University, USA,8Division of Plastic and Reconstructive Surgery and Orthopaedic Surgery and Rehabilitation, University of Nebraska

Medical Center, USA, 9Wisconsin Chiari Center, USA, 10Department of Mechanical & Materials Engineering,

Portland State University, OR, USA, and 11Department of Surgery, Oregon Health & Science University School

of Medicine, OR, USA

(Received 22 November 2009; revised 21 March 2010; accepted 26 April 2010)

AbstractPrimary objective: Chiari malformation is defined as herniation of the cerebellar tonsils through the foramen magnum, alsoknown as cerebellar tonsillar ectopia (CTE). CTE may become symptomatic following whiplash trauma. The purpose ofthe present study was to assess the frequency of CTE in traumatic vs non-traumatic populations.Study design: Case-control.Methods and procedures: Cervical MRI scans for 1200 neck pain patients were reviewed; 600 trauma (cases) and 600non-trauma (controls). Half of the groups were scanned in a recumbent position and half were scanned in an uprightposition. Two radiologists interpreted the scans for the level of the cerebellar tonsils.Main outcomes and results: A total of 1195 of 1200 scans were read. CTE was found in 5.7% and 5.3% in the recumbent andupright non-trauma groups vs 9.8% and 23.3% in the recumbent and upright trauma groups ( p! 0.0001).Conclusions: The results described in the present investigation are first to demonstrate a neuroradiographic differencebetween neck pain patients with and without a recent history of whiplash trauma. The results of prior research onpsychosocial causes of chronic pain following whiplash are likely confounded because of a failure to account for a possibleneuropathologic basis for the symptoms.

Keywords: Whiplash trauma, Chiari, cerebellar tonsillar ectopia, upright MRI

Introduction

Chiari Type I malformation is traditionally definedas caudal herniation of the cerebellar tonsils throughthe foramen magnum or tonsillar ectopia. Thecondition may be associated with syringomyelia

and osseous abnormalities at the craniovertebraljunction, but may occur in the absence of bothas well. Chiari Type II, also known as Arnold-Chiarimalformation, is differentiated from Chiari I in asmuch as it is present at birth, nearly always

Correspondence: Michael D. Freeman, PhD, MPh, 1234 SW 18th Ave, Suite 102, Portland, OR 97205, USA. Tel: 971-255-1088. Fax: 971-255-1046.E-mail: forensictrauma@gmail.com

ISSN 0269–9052 print/ISSN 1362–301X online ! 2010 Informa Healthcare Ltd.DOI: 10.3109/02699052.2010.490512

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associated with myelomeningocele (spina bifida) andincludes downward displacement of the medulla,fourth ventricle and vermis of the cerebellum intothe cervical spinal canal [1].Symptoms that are most often associated with

Chiari type I malformation are occipital headache,neck pain, upper extremity numbness and paresthe-sias and weakness [2, 3]. In a few cases there can alsobe lower extremity weakness and signs of cerebellardysfunction [4]. The criterion for diagnosis of aChiari Type I malformation is most frequently givenas magnetic resonance imaging (MRI) evidence oflow cerebellar tonsils relative to the foramenmagnum [5, 6]. The threshold for diagnosis isvariable; most authors have suggested that to beconsidered pathologic the cerebellar tonsils must be5mm or more below an imaginary line that runsfrom the basion (the most anterior point of theforamen magnum) to the opisthion (the posteriorpoint of the foramen magnum) [7]. Other authorshave suggested that the range of normal tonsilposition ends at 2mm below the basion-opisthionline (B-OL) [8]. The term tonsillar ‘ectopia’ is usedto characterize any condition in which the cerebellartonsils are found to be below the B-OL, regardless ofsymptom presence [8].Several authors have suggested that previously

quiescent Chiari Type I malformations can becomesymptomatic as a result of exposure to traumaticinjury. In their seminal paper describing 364 casesof symptomatic Chiari Type I cases, Milhorat et al.[2] noted that 24% of their subjects described atraumatic event that precipitated their symptoms.Wan et al. [9] described a symptomatic ‘conversion’of previously asymptomatic Chiari Type I followingminor head and neck trauma. Other authors havedescribed the discovery of symptomatic Chiari TypeI following motor vehicle crashes and what istypically described as ‘whiplash’ trauma [10, 11],in which the injury mechanism is a result of inertialloading of the spine and skull [12].There is no clear consensus regarding how trauma

may play a role in the activation of symptoms thatare attributed to a Chiari Type I or a lesser degree ofcerebellar tonsillar ectopia (CTE). Are the symp-toms coincidental to the trauma? Is the conditionsymptomatically ‘awakened’ by the trauma? Couldthe downward displacement of the tonsils be causedby the trauma? This last question is important, sincequite often the presence of tonsillar ectopia is notdiscovered until imaging is performed following heador neck trauma and acquired tonsillar herniation isradiographically indistinguishable from a pre-exist-ing CTE [3].In order to address some of these questions,

the present study describes an evaluation of theprevalence of CTE in two sub-populations

(trauma and non-trauma) of neck pain patientsreferred for MR imaging of the cervical spine usinga case-control study design. Further, the effect ofgravity dependence on tonsil level and its interactionwith a history of trauma was assessed by performingthe MRI scan in a traditional horizontal position ina recumbent scanner or in a vertical position in anupright scanner.

Methods

MR imaging films of the cervical spine and base ofthe skull from 1200 consecutive neck pain patients15 years and older presenting to four differentoutpatient radiology centres over a 3-year periodwere acquired and reviewed. Half of the scans (600)were from patients with neck pain resulting froma motor vehicle crash (cases) and half were frompatients without a recent history of trauma (con-trols). Further, half of the cases and half of thecontrols were scanned in a 0.6T Fonar upright openarchitecture MRI scanner (Fonar Corporation,Melville, NY) and the remaining half were obtainedfrom a facility with a 0.7T recumbent open archi-tecture Hitachi Altaire MRI scanner (HitachiMedical Systems, Tokyo, Japan). The resultingfour study groups had 300 scans each inthem—Recumbent Non-trauma (RNT), UprightNon-trauma (UNT), Recumbent Trauma (RT),and Upright Trauma (UT). Subject anonymity wasmaintained by the removal of all personal identifiersfrom the scans and patient histories and IRBapproval was sought and received from the SpinalInjury Foundation (Westminster, CO).

Traditional MR imaging sequences were used andincluded parasagittal to midsagittal slices. Sagittalsequences selected for measurement were those thatshowed the cerebellar tonsils at their lowest pointrelative to the B-OL. Sequences used on the uprightscanner were T2 fast spin-echo TR 1011, TE 160with slice thickness of 3.5mm, interval 4; and T1fast spin-echo TR 366, TE 17, with slice thickness of3.5mm, interval 4. Sequences used on the recum-bent scanner were T2 fast spin-echo sagittal TR3500, TE 120, with a slice thickness of 3mm,interval 4; and T1 SE sagittal TR 400, TE 16, witha slice thickness of 3mm and interval 4.

The films were interpreted by two board certifiedradiologists (authors DH and FS) who were blindedwith regard to the injury or scan position status. Themetric of interest was the level of the cerebellartonsils relative to the level of the foramen magnum,defined by a line drawn from the basion to theopisthion, the basion-opisthion line or B-OL(Figure 1).

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The scans were classified by the level of the lowestpoint of the cerebellar tonsils relative to the B-OL.The level of agreement between the two radiologistswas assessed, and in cases where there was disagree-ment the more conservative (more cephalad) assess-ment of tonsil station was used for the statistical tests.The results were described in terms of average

tonsil level as well as the relative proportion of scanswith tonsils 1mm or more below the level of theforamen magnum for each group and by gender.Three-way analysis of variance (ANOVA) with aTukey pairwise comparison was used to evaluate forsignificant differences in average tonsil level amongthe sub-groups (cases to controls, upright to recum-bent, male-to-female) and Chi-square goodness of fittest was used for evaluation of the proportionaldifferences between the groups. Comparisonswere statistically significant when p" 0.05.A Kappa statistic was used to assess the level ofagreement between the two radiologists (Analyse-It,Leeds, UK).

Results

Of the 1200 scans, five were considered uninterpre-table for tonsil station by one of the radiologists andall five of these studies were in the recumbent traumagroup. Amongst the remaining 1195 subjects theaverage age was 41.5 and 39.7 years in the cases and57.4 and 54.0 years in the controls (recumbent and

upright, respectively). A majority of subjects werefemale in all groups (Table I).

There was excellent agreement between the tworeaders regarding tonsil station (kappa range0.85–0.95). Both injury status and scan type (recum-bent vs upright) were associated with significantdifferences in the average level of the tonsils( p" 0.0001). The highest (most cephalad) meantonsil level was found in the recumbent non-traumagroup at 2.2mm above the B-OL, followed by thenon-trauma upright group at 1.7mm. The recum-bent trauma group average tonsil level was some-what lower at 1.3mm above the B-OL and thelowest station by far was observed in the uprighttrauma group at 0.1mm (or nearly even with theB-O line). The pairwise comparison indicated thatthe trauma cases had significantly lower averagetonsil levels than controls for both upright andrecumbent scan groups. There were also significantdifferences observed in tonsil level between the maleand female groups among the recumbent traumaand upright non-trauma groups, with the averagelevel in all of the female groups lower than those ofthe male groups ( p" 0.0001) (Table II).

Tonsillar herniation of 5mm and more was rarein all of the groups; there were a total of only sixcases in all groups, with three in the trauma groups(two upright and one recumbent) and three in thenon-trauma groups (one upright and two recum-bent). In contrast, there were quite substantialdifferences between the groups in the frequency ofscans with tonsils at 1mm or more below the B-OL;in the two non-trauma groups the tonsils were belowthe B-OL in 5.7% and 5.3% of cases in therecumbent and upright groups, respectively, whereasin the trauma groups 9.3% and 23.3% of cases in therecumbent and upright groups were 1mm or morebelow the B-OL (!2! 0.0001) (Table II). Similardifferences were observed when the groups werestratified by gender, with a significantly larger effectseen among the females (!2! 0.0001). An exemplarof a case with CTE observed in a vertically scannedtrauma group patient is depicted in Figure 2.

Discussion

This study reports that patients with a history ofmotor vehicle crash-associated neck pain have asubstantially higher frequency of cerebellar tonsillarectopia of 1mm or more than non-traumatic sub-jects; #4-times greater when evaluated with anupright MRI scanner. These data represent thefirst large series of patients scanned in both uprightand recumbent MR scanners with the intent ofevaluating CTE frequency.

Figure 1. The Basion-Opisthion Line (double arrow).

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The mean level of the tonsils in the non-traumagroups was relatively close and the frequency ofCTE was also nearly the same. This was not the casewith the trauma groups; the recumbent mean tonsillevel was substantially more cephalad than theupright. Notably, CTE was found 2.5-times moreoften in the upright trauma vs the recumbent traumagroup and #4-times more often than in either of thenon-trauma groups. Unless the difference betweentrauma and non-trauma cases was a result ofunforeseen variability, it is reasonable to concludethat these results reflect a degree of gravity depen-dent instability in the trauma group that was notobserved in the non-trauma group.

It is probable that the differences observedbetween the study groups were due to the indepen-dent variables of interest (scan type and injurystatus) rather than some unforeseen bias betweenthe groups. One possible source of bias is the factthat the scans were acquired at four differentoutpatient imaging centres (two upright and tworecumbent), raising the possibility of differing refer-ral criteria. A comparison of the demographics of thepatients indicates that the recumbent scan popula-tions were quite similar in age and gender mix to theupright scan populations, once trauma status wastaken into account and, thus, the type of facility(upright vs recumbent) did not appear to influencethe patient type seen at the facility. The traumapatients were substantially younger than thenon-trauma patients, but this was expected as thetrauma cases were representative of the mean ageof the general population that travels in a motorvehicle, whereas the non-trauma cases were morelikely to have neck symptoms associated withage-related degenerative joint and disc disease ofthe spine [13].

It has been suggested that, relative to a scanperformed in a recumbent MR scanner, a scanperformed in an upright scanner may demonstrateincreased caudal tonsillar ectopia [14]. Mechanicallythis makes sense; in an upright position the brain willtend to sit lower in the skull than when in a supineposition because of a combination of gravitationalforces and the configuration of the occiput. Whenvertical the base of the brain and the spinal cord tendto act as ‘cork stopper’ in the foramen magnum tothe extent allowed by the supporting tissues, andwhen horizontal the occipital lobe and cerebellumtend to slide in a cephalad direction along the

Figure 2. Exemplar of Chiari observed in a subject from theupright trauma group. The double arrow indicates the BO-L.

Table II. Mean tonsil level (mm above B-OL), 95% confidence interval (mm above B-OL), percentage of cases$ 1mm below B-OL.

All Female Male

M 95% CI % CTE M 95% CI % CTE M 95% CI % CTE

Recumbent non-trauma 2.2 2.0–2.4 5.7 2.1 1.8–2.4 7.2 2.3 2.0–2.7 5.0Upright non-trauma 1.7 1.5–1.9 5.3 1.4 1.2–1.7 7.5 2.2 1.9–2.5 2.4Recumbent trauma 1.3 1.1–1.5 9.3 1.0 0.7–1.3 11.4 1.8 1.4–2.2 6.7Upright trauma 0.1 %0.1–0.3 23.3 0.0 %0.2–0.3 24.6 0.4 0.0–0.8 19.5

Table I. Age (mean, SD), gender (F/M%).

Recumbent non-trauma Upright non-trauma Recumbent trauma Upright trauma

Number of subjects 300 300 295 300Age in years 57.4, 14.47 54.0, 17.74 41.5, 12.90 39.7, 14.37Gender 60.3/39.7 57.3/42.7 64.8/35.2 62.3/37.7

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curvature of the posterior skull interior. Ideally, allof the patients would have been scanned first inthe recumbent position and then in an uprightposition, in order to assess tonsillar shift withposition change.These findings beg the question of whether a

condition of a previously unknown CTE has beensymptomatically awakened by the motor vehiclecrash trauma or if the CTE was caused by thetrauma. There is some evidence in favour of thelatter; the fact that there was a substantial differenceobserved in the frequency of CTE in the upright vsthe recumbent trauma groups that was not presentin the non-trauma groups suggests instability of thebrain in the trauma group that is gravity dependent.It is well established that Chiari can be acquired;lumbar shunting performed to reduce CSF in casesof hydrocephalus can allow the brain to drop in theskull to the point that the cerebellar tonsils herniatethrough the foramen magnum. This phenomenon isdue to the fact that the flotation level of the brain isdependent on the amount of CSF within the duralcovering of the spine and brain [15, 16].Hypothetically, it then follows that if a dural leakcould result from crash trauma then a CSF leak andlowered pressure could explain the findings of lowertonsils in the upright trauma group vs the recumbentgroup.There is clinical evidence that dural leaks are

associated with whiplash trauma and chronic symp-toms; using radioisotope cisternography, Ishikawaet al. [17] described the identification of CSF leaks,primarily in the lumbar spine at the dural sleeves, in37 of 66 (56%) chronic whiplash patients withheadache, memory loss, dizziness and neck pain,inter alia. The authors described substantialimprovement in chronic symptoms in 32 of the 36(88%) patients who agreed to epidural blood patch(EBP) therapy. Huntoon and Watson [18] presenteda case study in which a 60 year-old woman wasexposed to a whiplash trauma and complained ofsubsequent headache and upper cervical pain.Subsequent MRI examination revealed CTE andfinding suggestive of extradural CSF, indicative ofa non-specific dural leak. The patient respondedpositively to EBP therapy.Although a possible mechanism of dural trauma

associated with whiplash trauma is only hypothetical,biomechanical study of a porcine spine modeldemonstrates substantial pressure changes in theCSF during simulated whiplash trauma; first thepressure drops by #75mm Hg and then it increasesby more than 150mm Hg over a period of #100ms[19]. Whether this is a sufficient pressure gradientchange to cause dural injury in some cases isunknown.

The identification of a here-to-fore unrecognizedcondition or possible injury to the central nervoussystem that may be causally associated with motorvehicle crash trauma raises potential concernsregarding the conclusions of prior authorswho have studied whiplash injuries as a primarilynon-pathologic chronic pain condition. A numberof recent papers have evaluated the relationshipbetween psychosocial factors such as litigationstatus, depression and coping strategies on symp-toms associated with whiplash-related neck pain,concluding that all are important and predictivefactors in injury outcome [20–22]. These and otherprior research efforts have been based on theassumption that there is no definable pathologyassociated with the chronic pain complaints amongthe injured subjects. Although this study did notevaluate the relationship between various symptompatterns and the presence or absence of CTE in the595 whiplash-injured patients, the fact remains thatneuroradiographic abnormality was found in approx-imately one-in-four upright trauma cases in thepresent study. Thus, while it cannot be concludedthat a patient with CTE is more likely to bedepressed, have difficulty coping and seek compen-sation for his injury than one without CTE, it cannotbe denied that the condition may have served as ahidden source of confounding in the aforementionedstudies and others with similar designs and intent,calling into question the validity of the conclusionsof the authors.

Irrespective of whether the radiographic findingsof CTE observed in the trauma groups resulted fromthe crash trauma or was pre-existing, the currentstudy indicates that cerebellar tonsillar ectopia issubstantially more prevalent in whiplash-injuredneck pain patients than in neck pain patients withno recent history of trauma. Of incidental note is thefact that the proportion of upright scans with CTEin the present study is approximately the same as theproportion of whiplash-injured patients who go on toreport chronic pain symptoms from their injuryreported by some authors [23].

A limitation of the present study is the lack ofdetail in the differentiation between the traumaticand non-traumatic subjects regarding a recent his-tory of whiplash trauma. Further informationregarding the prevalence of a remote history oftrauma among the non-traumatic subjects wouldhave been informative for further comparisonbetween the groups. Several authors have reportedthat nearly half of the population with chronic neckpain attribute the onset of their pain to a whiplashtrauma-associated injury [24, 25]. Accordingly, it isreasonable to assume that some proportion of thesubjects in the non-trauma groups did have a priorhistory of whiplash injury. As a source of error,

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this assumption would have minimized rather thanincreased the differences between the groups, result-ing in the probable under-estimation of the ratios ofCTE reported herein.A second limitation is the lack of detailed infor-

mation regarding the symptoms of the study sub-jects. Previous authors have described a myriad ofneurological complaints associated with a diagnosisof a symptomatic Chiari malformation followinghead and neck trauma [26, 27]; however, virtually allpatients complain of headache and many complainof neck pain, the two symptoms most commonlyassociated with whiplash injury [28]. The difficultyof evaluating the causal relationship between whip-lash injury-related symptoms and the finding of CTEis further complicated by the fact that a causalassociation has been described in the literaturebetween whiplash injury and fibromyalgia syndrome(FMS) [29, 30]. Further, Heffez et al. [31] havedescribed a higher than expected frequency of ChiariI malformations among a group of 270 patients withFMS (20%), with the lead author noting that morethan 70% were observed to have some degree ofCTE (personal communication with D. Heffez, 15October 2008). Thus, CTE has been found to beassociated with both a history of whiplash traumaand FMS. Although there are more questions thananswers generated by this observation, an appealinghypothesis is one that links FMS to whiplash injuryvia an acquired CTE resulting from the whiplashtrauma, possibly secondary to the type of dural leakdescribed by Ishikawa et al. [17].Future study that would advance the understand-

ing of the relationship between CTE and whiplashtrauma should include a detailed neurologic evalu-ation and elicited pre- and post-injury history ofChiari-unique headache symptoms (e.g. cough exac-erbation) as well as recumbent and upright MRIassessment of CTE status.

Conclusions

The results reported herein are the first to demon-strate a substantial neuroradiographic differencebetween neck pain patients with and without arecent history of motor vehicle crash trauma.Upright position MR imaging appears to increasethe sensitivity to CTE over recumbent MR imagingby 2.5-times. Future research should include effortsto confirm these results as well as biomechanicalresearch into whether injury-related mechanismscould result in dural injury and subsequent leaking.A prospective long-term follow-up of whiplash injurycases by cerebellar tonsillar ectopia status wouldprovide useful information in understanding post-traumatic neck pain and related syndromes.

Clinicians may want to consider evaluatingpatients for CTE (i.e. upright MRI of the neck andhead) when there is a history of whiplash trauma andpersisting suboccipital headache in combination withheadache worsened by cough or bilateral sensory ormotor deficits in the upper extremities. In CTEpatients with headache that is relieved when supineit also may be appropriate to consider radionuclidecisternography to evaluate for the presence of adural leak.

Declaration of interest: Dr Harshfield has afinancial interest in an imaging centre with anupright MRI. The authors report no further conflictsof interest. The authors alone are responsible for thecontent and writing of the paper.

References

1. Stevenson KL. Chiari Type II malformation: Past, present,and future. Neurosurgery Focus 2004;16:5.

2. Milhorat TH, Chou MW, Trinidad EM, Kula RW,Mandell M, Wolpert C, Speer MC. Chiari 1 malformationredefined: Clinical and radiographic findings for 364 symp-tomatic patients. Neurosurgery 1999;44:1005–1017.

3. Payner TD, Prenger E, Berger TS, Crone KR. AcquiredChiari malformations: Incidence, diagnosis, and manage-ment. Neurosurgery 1994;34:429–434.

4. Wolf DA, Veasey DA, Wilson SK, Adame J,Korndorffer WE. Death following minor head trauma intwo adult individuals with the Chiari I deformity. Journal ofForensic Science 1998;43:1241–1243.

5. Ball WS, Krone KR. Chiari malformation from Dr. Chiarito MR imaging. Radiology 1995;195:602–604.

6. Elster AD, Chen MY. Chiari 1 malformations: Clinical andradiological reappraisal. Radiology 1992;183:347–353.

7. Meadows J, Kraut M, Guarnieri M, Haroun RI, Carson BS.Asymptomatic Chiari type I malformations identified onmagnetic resonance imaging. Journal of Neurosurgery2000;92:920–926.

8. Barkovich AJ, Wippold FJ, Sherman JL, Citrin CM.Significance of cerebellar tonsillar position on MR. AJNR:American Journal of Neuroradiology 1986;7:795–799.

9. Wan MJ, Nomura H, Tator CH. Conversion to symptomaticChiari I malformation after minor head or neck trauma.Neurosurgery 2008;63:748–753.

10. Prattico F, Perfetti P, Gabrieli A, Longo D, Caroselli C,Ricci G. Chiari I malformation with syrinx: An unexpecteddiagnosis in the emergency department. European Journalof Emergergency Medicine 2008;15:342–343.

11. Bunc G, Vorsic M. Presentation of a previously asympto-matic Chiari I malformation by a flexion injury to the neck.Journal of Neurotrauma 2001;18:645–648.

12. Stemper BD, Yoganandan N, Gennarelli TA, Pintar FA.Localized cervical facet joint kinematics under physiologicaland whiplash loading. Journal of Neurosurgery Spine 2005;3:471–476.

13. Matsumoto M, Fujimura Y, Suzuki N, Nishi Y,Nakamura M, Yabe Y, Shiga H. MRI of cervical inter-vertebral discs in asymptomatic subjects. British Journal ofBone Joint Surgery 1998;80:19–24.

Chiari and whiplash injury 993

Brai

n In

j Dow

nloa

ded

from

info

rmah

ealth

care

.com

by

Ore

gon

Hea

lth S

ci C

ente

r on

06/1

7/10

For p

erso

nal u

se o

nly.

14. Elsig JP, Kaech DL. Imaging-based planning for spinesurgery. Minimally Invasive Therapy Allied Technology2006;15:260–266.

15. Caldarelli M, Novegno F, Di Rocco C. A late complicationof CSF shunting: Acquired Chiari I malformation. ChildsNervous System 2009;25:443–452.

16. Chumas PD, Armstrong DC, Drake JM, Kulkarni AV,Hoffman HJ, Humphreys RP, Rutka JT, Hendrick EB.Tonsillar herniation: The rule rather than the exception afterlumboperitoneal shunting in the pediatric population.Journal of Neurosurgery 1993;78:568–573.

17. Ishikawa S, Yokoyama M, Mizobuchi S, Hashimoto H,Moriyama E, Morita K. Epidural blood patch therapy forchronic whiplash-associated disorder. Anesthesia andAnalgesia 2007;105:809–814.

18. Huntoon MA, Watson JC. Intracranial hypotension followingmotor vehicle accident: An overlooked cause ofpost-traumatic head and neck pain? Pain Practice 2007;7:47–52.

19. Siegmund GP, Winkelstein BA, Ivancic PC, Svensson MY,Vasavada A. The anatomy and biomechanics of acute andchronic whiplash injury. Traffic Injury Prevention 2009;10:101–112.

20. Cassidy JD, Carroll LJ, Cote P, Lemstra M, Berglund A,Nygren A. Effect of eliminating compensation for pain andsuffering on the outcome of insurance claims for whiplashinjury. New England Journal of Medicine 2000;342:1179–1186.

21. Cote P, Hogg-Johnson S, Cassidy JD, Carroll L, Frank JW.The association between neck pain intensity, physicalfunctioning, depressive symptomatology and time-to-claim-closure after whiplash. Journal of Clinical Epidemiol2001;54:275–286.

22. Carroll LJ, Cassidy JD, Cote P. The role of pain copingstrategies in prognosis after whiplash injury: Passive copingpredicts slowed recovery. Pain 2006;124:18–26.

23. Freeman MD, Croft AC, Rossignol AM, Weaver DS,Reiser M. A review and methodologic critique of theliterature refuting whiplash syndrome. Spine 1999;24:86–98.

24. Freeman MD, Croft AC, Rossignol AC, Centeno CJ,Elkins W. Chronic neck pain and whiplash: A case/controlstudy of the relationship between acute whiplash injuries andchronic neck pain. Pain Research Management 2006;11:79–83.

25. Cote P, Cassidy JD, Carroll L. Is a lifetime history of neckinjury in a traffic collision associated with prevalent neckpain, headache and depressive symptomatology? AccidentAnalysis and Prevention 2000;32:151–159.

26. Murano T, Rella J. Incidental finding of Chiari I malforma-tion with progression of symptoms after head trauma:Case report. Journal of Emergency Medicine 2006;30:295–298.

27. Uzoigwe CE, Shabani F, Chami G, El-Tayeb M. Simplewhiplash? British Journal of Bone Joint Surgery 2009;91:1103–1104.

28. Obermann M, Nebel K, Riegel A, Thiemann D, YoonMS, Keidel M, Stude P, Diener HC, Katsarava Z.Incidence and predictors of chronic headache attributedto whiplash injury. Cephalalgia 2009; [Epub aheadof print]. PMID: 19673910.

29. Buskila D, Neumann L, Vaisberg G, Alkalaly D, Wolfe F.Increased rates of fibromyalgia following cervical spine injury.A controlled study of 161 cases of traumatic injury. Arthritisand Rheumatism 1997;40:446–452.

30. McLean SA, William DA, Clauw DJ. Fibromyalgia aftermotor vehicle collision: Evidence and implications. TrafficInjury Prevention 2005;6:97–104.

31. Heffez DS, Ross RE, Shade-Zeldow Y, Kostas K, Shah S,Gottschalk R, Elias DA, Shepard A, Leurgans SE,Moore CG. Clinical evidence for cervical myelopathy dueto Chiari malformation and spinal stenosis in anon-randomized group of patients with the diagnosis offibromyalgia. European Spine Journal 2004;13:516–523.

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Journal of Spine

ISSN: 2165-7939

Journal of SpineHenderson Sr and Henderson Jr, J Spine 2017, 6:2

DOI: 10.4172/2165-7939.1000364

Mini Review OMICS International

Volume 6 • Issue 2 • 1000364J Spine, an open access journalISSN: 2165-7939

Diagnosis of Atlantoaxial Instability Requires Clinical Suspicion to Drive the Radiological InvestigationFraser C Henderson Sr.1,2* and Fraser C Henderson Jr.3

1Doctors Community Hospital, Lanham, MD, USA2The Metropolitan Neurosurgery Group, LLC, Chevy Chase, MD, USA3Medical University of South Carolina, Charleston, SC, USA

*Corresponding author: Fraser Cummins Henderson Sr., M.D., 8401 Connecticut Avenue, Suite 220, Chevy Chase, MD 20815, USA, Tel: 301-654-9390; Fax: 301-654-9394; E-mail: Henderson@FraserHendersonMD.com

Received March 25, 2017; Accepted March 30, 2017; Published April 01, 2017

Citation: Henderson Sr. FC, Henderson Jr. FC (2017) Diagnosis of Atlantoaxial Instability Requires Clinical Suspicion to Drive the Radiological Investigation. J Spine 6: 364. doi: 10.4172/2165-7939.1000364

Copyright: © 2017 Henderson Sr. FC, et al. This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.

IntroductionAtlantoaxial instability (AAI) occurs as a result of trauma,

congenital conditions such as os odontoideum, neoplasm, infection and degenerative connective tissue disorders such as rheumatoid arthritis, genetic conditions such as HOX-D3 and Down syndrome, and heritable connective tissue disorders, emblematic of which are the Ehlers Danlos syndromes (EDS). Prototypical of disorders in which AAI is diagnosed, is rheumatoid arthritis (RA). Prior to the development of effective disease-modifying pharmacotherapies, 88% of RA patients exhibited radiographic evidence of C1-C2 involvement, in whom 49% were symptomatic and 20% myelopathic; ultimately, 10% may have suffered atlantoaxial dislocation and death [1-3].

In their report on pediatric patients undergoing C1-C2 transarticular screw fixation Gluf and Brockmeyer noted approximately one third of the cases of AAI resulted from trauma, one third from os odontoideum, and one third from congenital conditions such as Down syndrome, Stihl disease, dwarfism, Morquio syndrome, Klippel-Feil and others. Three patients were thought to have chronic instability, most likely to have resulted from ligamentous laxity, possibly EDS [4,5].

The diagnosis of AAI is not difficult in the presence of an abnormal ADI (Figure 1), but may be elusive in those cases where the transverse ligament is intact, and where there is incompetence of one or both the alar ligaments. In these cases, the diagnosis may require dynamic imaging and concordant clinical findings.

Etiology of Atlantoaxial Instability

Traumatic flexion of the neck may result in injury to the transverse odontoid ligaments and alar ligaments. An atlanto-dental interval (ADI) over 3 mm suggests possible instability in adults; an ADI exceeding 5 mm suggests instability in children. An ADI of 7 mm suggests rupture or incompetence of the transverse ligament, and/or of the cruciate ligament, and an ADI of 10 mm suggests loss or incompetence of the alar ligaments as well [6]. However, if the transverse ligament is intact, the ADI is normal despite the presence of alar ligament incompetence.

A proclivity to ligamentous incompetence renders the atlantoaxial joint at higher risk for instability. The atlantoaxial junction (AAJ) is the most mobile joint of the body. Held together by ligaments that allow a great degree of freedom of rotation, the AAJ is responsible for 50% of all neck rotation, 5° of lateral tilt, and 10° to 20° of flexion/extension [7]. It is not surprising therefore, that connective tissue disorders, such as Down syndrome and EDS, are more frequently visited by AAI. Motor delay [8,9], headache associated with “connective tissue pathological relaxation” and quadriparesis are attributed to ligamentous laxity and instability at the atlanto-occipital and atlantoaxial joints [10,11]. While the epidemiology of AAI in EDS-hypermobile type is unknown, AAI was seen in two thirds of patients with EDS-Vascular type [11]. A high risk of AAI is apparent in other connective tissue disorders, including 11% of Down syndrome patients [12].

The AAJ mechanical properties are determined by ligamentous structures [13,14], most prominent of which are the transverse and alar ligaments [15]. The alar ligaments limit axial rotation and lateral

bending to the contralateral side, are often injured in motor vehicle collisions, and could be implicated in whiplash-associated disorders [15]. Failure of the alar ligament allows a 30% increased rotation to the opposite side [16]. The atlantoaxial joint is ill-equipped to handle the required multi-axial movements in the presence of ligamentous laxity or disruption [17]. Weakness of the muscles and ligaments, hormonal changes, infection, immunological problems, and congenital dysmorphism may contribute to the overall mechanical dysfunction at the C1-C2 motion segment.

Hypermobility of the AAJ is common in children, and up to 45° of rotation may be observed in each direction. However, in the adult there is substantially less than 40° of rotation [17-20]: at 35° of rotation of C1 upon C2 there is stretching and kinking of the contralateral vertebral artery [20]; at 45°, both vertebral arteries become occluded [21].

Diagnostic FindingsDiagnosis of AAI is based upon careful history, a detailed

neurological exam and imaging of the upper cervical spine. The most common clinical features are neck pain and suboccipital headache, with the caveats that headache is present in 50% of patients with EDS [22], and that moderate pain is a common occurrence for most EDS patients. There may be symptoms referable to the vertebral artery blood flow, including visual changes, as well as headache associated with the vertebral artery itself. Syncopal and presyncopal events are frequent. Other symptoms include dizziness, nausea, sometimes facial pain, dysphagia, choking, and respiratory issues. There is usually improvement with a neck brace. Examination often demonstrates tenderness over C1-C2, altered mechanics of neck rotation, hyperreflexia, dysdiadochokinesia, hypoesthesia to pinprick. Weakness is not a constant feature of AAI [4,23-27].

Radiological features may show atlanto-dental interval (ADI) >2.5 mm in an adult, or 5 mm in a child, on lateral flexion x-rays (Figure 1) or rotation of C1 upon C2 >41° [4,28] (Figure 2). Excessive rotation occurs opposite to the side of an incompetent alar ligament. Alar ligament incompetence is the most frequent cause of AAI in the population of patients with hypermobility connective tissue disorders [4]. Thus diagnosis of AAI in EDS, or related connective tissue disorders, is best made with supine computerized tomography (CT), from occiput to C2, with full neck rotation (90° if possible) to left and to right. (Figure 2) The difficulty of recognizing rotary instability on standard x-ray, CT and MRI images has resulted in failure to diagnose [29].

Citation: Henderson Sr. FC, Henderson Jr. FC (2017) Diagnosis of Atlantoaxial Instability Requires Clinical Suspicion to Drive the Radiological Investigation. J Spine 6: 364. doi: 10.4172/2165-7939.1000364

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Volume 6 • Issue 2 • 1000364J Spine, an open access journalISSN: 2165-7939

Figure 1: ADI >3 mm in an adult.

Figure 2: Excessive (>41°) rotation between C1 and C2. Axial CT views through (a) C1 and (b) C2 on full neck rotation demonstrate that the angle between C1 and C2 is (85°-40°) = 45°, and therefore unstable.

In the hypermobility disorders, there may be abnormal facet overlap on full neck rotation<20% [30,31] (Figure 3); lateral translation of the facet joints: translation in aggregate >7 mm on coronal imaging as seen on open mouth odontoid views. Open mouth odontoid views are very effective in identifying AAI [32] (Figure 4).

Dvorak showed in cadavers that the mean axial rotation between the axis and the second cervical vertebra was 31.1°, increasing to 35° after contralateral rupture of the alar ligament; CT imaging thus demonstrated increased angular rotation of 4° to the side opposite the alar ligament injury [16].

The diagnosis of AAI can sometimes be seen on three dimensional CT, where there may be a clear demonstration of subluxation [31]. Increased ligament signal intensity on high-resolution proton density-weighted MRI may be seen, with the caveats that alar ligaments of asymptomatic patients may show high signal intensity, and that there is variable inter-examiner reliability of MRI evaluation [33]. Other radiological indiations of AAI include compromise of the vertebral arteries based upon abnormal mechanics at the C1-C2 junction; anomalous joints; retro-odontoid pannus [23,27,34] (Table 1).

Criteria for SurgeryThe decision to proceed to surgery rests upon the presence of severe

neck or suboccipital pain, the presence of cervical medullary syndrome or syncopal (or pre-syncopal) episodes, demonstrable neurological findings and radiological evidence of instability or compression of the neuraxis.

Figure 3: Axial CT scan through C1-C2 showing loss of facet overlap on full neck rotation, consistent with AAI.

Figure 4: AP open-mouth radiograph of the C1-C2 levels showing pathological loss of overlap.

TreatmentFor milder form of instability, the patient should be considered for

treatment with neck brace, physical therapy and avoidance of activities that provoke exacerbation of the AAI symptoms. If the non-operative treatment fails, fusion-stabilization at C1-C2 is required. Failure of any of the components of the atlantoaxial ligament complex requires dorsal surgical fusion [35]. This is most often accomplished with posterior screw constructs, transarticular screw fixation [24], or C1-C2 lateral mass/pedicle screws and interposed graft [4,25,26] (Figure 5). Aberrant vertebral artery anatomy may preclude the desired screw placement in 18% to 23% of patients [36,37], and the surgery may be complicated in EDS by small bone architecture.

Citation: Henderson Sr. FC, Henderson Jr. FC (2017) Diagnosis of Atlantoaxial Instability Requires Clinical Suspicion to Drive the Radiological Investigation. J Spine 6: 364. doi: 10.4172/2165-7939.1000364

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Volume 6 • Issue 2 • 1000364J Spine, an open access journalISSN: 2165-7939

Neurological and spinal manifestations of the Ehlers–Danlos syndromes. Am J Med Genet C Semin Med Genet 175: 195-211.

5. Gluf WM, Brockmeyer DL (2005) Atlantoaxial transarticular screw fixation: A review of surgical indications, fusion rate, complications, and lessons learned in 67 pediatric patients. J Neurosurg Spine 2: 164-169.

6. Fielding JW, Cochran G, Lawsing JF, Hohl M (1974) Tears of the transverse ligament of the atlas. A clinical and biomechanical study. J Bone Joint Surg Am 56(8): 1683-1691.

7. White AA, Panjabi MM (1990) Clinical biomechanics of the spine (2ndedn), JB Lippincott Company. Philadelphia.

8. Kirby A, Davies R (2007) Developmental coordination disorder and joint hypermobility syndrome–overlapping disorders? Implications for research and clinical practice. Child Care Health Dev 33: 513-519.

9. Jelsma LD, Geuze RH, Klerks MH, Niemeijer AS, Smits-Engelsman BC (2013) The relationship between joint mobility and motor performance in children with and without the diagnosis of developmental coordination disorder. BMC Pediatrics 13: 1.

10. Nagashima C, Tsuji R, Kubota S, Tajima K (1981) Atlanto-axial, atlanto-occipital dislocations, developmental cervical canal stenosis in the ehlers-danlos syndrome (author’s transl). No Shinkei Geka 9: 601-608.

11. Halko GJ, Cobb R, Abeles M (1995) Patients with type IV ehlers-danlos syndrome may be predisposed to atlantoaxial subluxation. J Rheumatol 22: 2152-2155.

12. El-Khouri M, Mourão MA, Tobo A, Battistella LR, Herrero CFP, et al. (2014) Prevalence of atlanto-occipital and atlantoaxial instability in adults with down syndrome. World Neurosurgery 82: 215-218.

Occiput to C1/C2 fusion should be considered in the presence of craniocervical instability, basilar invagination or complex Chiari malformation.

Conclusion AAI results from trauma, congenital conditions, neoplasm,

infection, degenerative connective tissue disorders, genetic conditions such as the HOX-D3 or Down syndrome, and heritable connective tissue disorders, emblematic of which are the Ehlers Danlos syndromes. AAI in the hypermobility disorders usually requires dynamic imaging to demonstrate ligamentous incompetence. Radiological findings which are concordant with clinical findings should prompt consideration of surgery.

References

1. Fehlings M, Cooper P, Errico T (1992) Rheumatoid arthritis of the cervical spine. In: Neurosurgical topics: Degenerative disease of the cervical spine. Rolling Meadows, IL, American Association of Neurological Surgeons 125-139.

2. Weissman BN, Aliabadi P, Weinfeld MS, Thomas WH, Sosman JL (1982) Prognostic features of atlantoaxial subluxation in rheumatoid arthritis patients. Radiology 144: 745-751.

3. Mikulowski P, Wollheim FA, Rotmil P, Olsen I (1975) Sudden death in rheumatoid arthritis with atlanto‐axial dislocation. Acta Med Scand 198: 445-451.

4. Henderson FC, Austin C, Benzel E, Bolognese P, Ellenbogen R, et al. (2017)

ADI (Atlanto-dental interval) >3 mm in an adult, or 5 mm in a child, on lateral flexion x-rays. Lateral translation of the facet joints: translation in aggregate >7 mm on coronal imaging as seen on open mouth odontoid views. Open mouth odontoid views are very effective in identifying AAI [32]. Rotation of C1 upon C2, >41° [4,28] (Figure 1).Facet overlap on full neck rotation <20% [30,31] (Figure 2). Greater than 8° difference between the left and right axial rotation, on axial CT with full neck rotation [37]. Three-dimensional CT demonstrating subluxation (Figure 3).Increased ligament signal intensity on high-resolution proton density-weighted MRI, with the caveats that alar ligaments of asymptomatic patients may show high signal intensity and that there is variable inter-examiner reliability of MRI evaluation [33]. Compromise of the vertebral arteries based upon abnormal mechanics at the C1-C2 junction.Anomalous joints.Retro-odontoid pannus [23,27,34].

Table 1: Radiological findings of AAI.

Figure 5: (a) Sagittal model of atlanto-axial rotary sub-luxation; (b) Treatment of AAI.

Citation: Henderson Sr. FC, Henderson Jr. FC (2017) Diagnosis of Atlantoaxial Instability Requires Clinical Suspicion to Drive the Radiological Investigation. J Spine 6: 364. doi: 10.4172/2165-7939.1000364

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13. Steinmetz MP, Mroz TE, Benzel EC (2010) Craniovertebral junction: Biomechanical considerations. Neurosurgery 66: 7-12.

14. Wolfla CE (2006) Anatomical, biomechanical, and practical considerations in posterior occipito-cervical instrumentation. Spine J 6: 225S-232S.

15. Tubbs RS, Hallock JD, Radcliff V, Naftel RP (2011) Ligaments of the craniocervical junction: A review. Journal of Neurosurgery: Spine 14: 697-709.

16. Dvorak J, Panjabi M, Gerber M, Wichmann W (1987) CT-functional diagnostics of the rotatory instability of upper cervical spine: An experimental study on cadavers. Spine 12: 197-205.

17. Martin M, Bruner H, Maiman D (2010) Anatomic and biomechanical considerations of the craniovertebral junction. Neurosurgery 66: 2-6.

18. Zhang H, Bai J (2007) Development and validation of a finite element model of the occipito-atlantoaxial complex under physiologic loads. Spine 32: 968-974.

19. Panjabi M, Dvorak J, Crisco JJ, Oda T, Wang P, et al. (1991) Effects of alar ligament transection on upper cervical spine rotation. J Orthop Res 9: 584-593.

20. Selecki BR (1969) The effects of rotation of the atlas on the axis: Experimental work. Med J Aust 1: 1012-1015.

21. Menezes AH, Traynelis VC (2008) Anatomy and biomechanics of normal craniovertebral junction (a) and biomechanics of stabilization (b). Child’s Nervous System 24: 1091-1100.

22. Sacheti A, Szemere J, Bernstein B, Tafas T, Schechter N, et al. (1997) Chronic pain is a manifestation of the ehlers-danlos syndrome. J Pain Symptom Manage 14: 88-93.

23. Isono M, Ishii K, Kamida T, Fujiki M, Goda M, et al. (2001) Retro-odontoid soft tissue mass associated with atlantoaxial sub-luxation in an elderly patient: A case report. Surg Neurol 55: 223-227.

24. Dickman C, Sonntag V (1998) Posterior C1-C2 transarticular screw fixation for atlantoaxial arthrodesis. Neurosurgery 43: 275-280.

25. Goel A, Desai KI, Muzumdar DP (2002) Atlantoaxial fixation using plate and screw method: A report of 160 treated patients. Neurosurgery 51: 1351-1356.

26. Aryan HE, Newman CB, Nottmeier EW, Acosta FL Jr, Wang VY, et al. (2008) Stabilization of the atlantoaxial complex via C-1 lateral mass and C-2 pedicle

screw fixation in a multicenter clinical experience in 102 patients: Modification of the harms and goel techniques. J Neurosurg Spine 8: 222-229.

27. Goel A, Phalke U, Cacciola F, Muzumdar D (2004) Atlantoaxial instability and retroodontoid mass-Two case reports. Neurol Med Chir (Tokyo) 44: 603-606.

28. Koby M (2014) The discordant report – pathological radiological findings: A peripatetic review of salient feature of neuropathology in the setting of an erstwhile standard ‘normal’ radiological assessment. In: Co-Morbidities that Complicate the Treatment and Outcomes of Chiari Malformation. Lulu. 50.

29. Kothari P, Freeman B, Grevitt M, Kerslake R (2000) Injury to the spinal cord without radiological abnormality (SCIWORA) in adults. J Bone Joint Surg Br 82: 1034-1037.

30. Fielding JW, Hawkins RJ (1977) Atlanto-axial rotatory fixation. (fixed rotatory subluxation of the atlanto-axial joint). J Bone Joint Surg Am 59: 37-44.

31. Fielding JW, Stillwell WT, Chynn K, Spyropoulos E (1978) Use of computed tomography for the diagnosis of atlanto-axial rotatory fixation. A case report. JBJS Case Connector 8: 1102-1104.

32. Taniguchi D, Tokunaga D, Hase H (2008) Evaluation of lateral instability of the atlanto-axial joint in rheumatoid arthritis using dynamic open-mouth view radiographs. Clin Rheumatol 27: 851-857.

33. Willauschus WG, Kladny B, Beyer WF, Gluckert K, Arnold H, et al. (1995) Lesions of the alar ligaments. In vivo and in vitro studies with magnetic resonance imaging. Spine 20: 2493-2498.

34. Jun B (1999) Complete reduction of retro-odontoid soft tissue mass in OS odontoideum following the posterior C1-C2 tranarticular screw fixation. Spine 24: 1961.

35. Menendez JA, Wright NM (2007) Techniques of posterior C1-C2 stabilization. Neurosurgery 60: S103-11.

36. Madawi A, Casey A, Solanki G, Tuite G, Veres R, et al. (1997) Radiological and anatomical evaluation of the atlantio-axial transarticular screw fixation technique. J Neurosurg 86: 961-968.

37. Dvorak J, Hayek J, Zehnder R (1987) CT-functional diagnostics of the rotatory instability of the upper cervical spine. Part-2. An evaluation on healthy adults and patients with suspected instability. Spine 12: 726-731.

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Citation: Henderson Sr. FC, Henderson Jr. FC (2017) Diagnosis of Atlantoaxial Instability Requires Clinical Suspicion to Drive the Radiological Investigation. J Spine 6: 364. doi: 10.4172/2165-7939.1000364

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Upright Magnetic Resonance Imaging of

the Craniocervical Junction Francis W. Smith MD FRCR FRCS FRCP FFSEM (UK) Clinical Director, Medserena Upright MRI Centre, London, UK Magnetic Resonance Imaging (MRI) is conventionally performed in the supine position, where no information about the effect of gravity on the patient in the upright position is possible. Humans spend the larger part of each day in the upright position, where most of their musculoskeletal ailments are experienced. This is especially so along the spinal axis and in the weight-bearing joints. With the capability of scanning patients in the upright position, so has come the ability to use MRI to examine the brain, spine, and major joints in the upright position under the effects of gravity. It is not only the alterations in the biomechanics of the body that can be observed, it is also alterations in blood flow, venous drainage and cerebral spinal fluid flow that are now amenable to the study under the effects of gravity.

This is especially so at the cranio-cervical junction and in the cervical spine, where the weight of the head on the neck can result in significant alteration in the MRI appearance between the supine and upright positions. An adult human head constitutes around 8% of the whole body mass and weighs somewhere between 4.5 and 5 kg (9–11 lb) [1]. This weight exerts significant pressure on the craniocervical junction and the cervical spine. The value of being able to image in the upright position is well demonstrated in the case of a 50-year-old woman who had been suffering for many years from neck pain. A prior supine MRI examination had shown a mild degenerative intervertebral disc bulge at the C5–C6 level with a moderate segmental kyphosis. (Fig. 1). Despite repeated attempts with conservative treatment, the patient's symptoms worsened and were marked by the onset of transient paraesthesia, transient loss of muscle tone in the legs and drop attacks, which could not be explained by the disc bulge seen in the MRI examination. An examination in the upright position shows the full extent of the posterior disc bulge at the C5–C6 level, with an increase in the segmental kyphosis. More importantly it shows the presence of downward herniation of the cerebellar tonsils with compression of the brainstem, the full extent of which is not appreciated in the supine examination (Fig. 2).

Fig. 1. Supine MRI examination. Fig. 2. Upright MRI examination.

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Downward herniation of the cerebellar tonsils, tonsillar ectopia, is graded as a Chiari type 1, traditionally defined as caudal herniation of the cerebellar tonsils through the foramen magnum. The criterion for diagnosis of a Chiari Type I malformation is most frequently given as MR evidence of cerebellar tonsils extending greater than 3–5mm below the foramen magnum. [2] Chiari type II also known as Arnold-Chiari malformation, is differentiated from a Chiari type I in as much as it is present at birth and nearly always associated with myelomeningocoel and includes downward displacement of the medulla, fourth ventricle and cerebellum into the cervical spinal canal [3].

The threshold for diagnosis is variable, some authors have suggested that to be considered pathologic the cerebellar tonsils must be 3–5 mm or more below an imaginary line that runs from the basion, or the most anterior point of the foramen magnum, to the opisthion, or the posterior point of the foramen magnum, the basion-opisthion line or McRae’s line (Figure 3) [4]. Others have suggested that the range of normal tonsil position ends at 2 mm below the basion-opisthion line [5].

Fig. 3. The basion-opisthion line or McRae’s line.

While this classification is still widely used today, research shows that the degree of tonsillar herniation is not related to severity of symptoms. In fact, some people with significant tonsillar herniation, greater than 3 mm, have no symptoms. In a study of over 12,000 MRI scans it was found that over 30% of the people who had herniation greater than 5 mm were symptom free [6].

On the other hand, some people exhibit classic Chiari-type symptoms where the tonsils lie at the level of the foramen magnum or just below. This observation is referred to as Chiari 0 malformation. This is a controversial topic especially since the term Chiari 0 was first used by a group of researchers led by Dr. Jerry Oakes, where they identified five patients with syringomyelia and no evidence of tonsillar herniation (i.e. no Chiari I malformation) [7]. Today, by common usage, the term is applied to low lying cerebellar tonsils, at or below the foramen magnum, regardless of the presence or absence of syringomyelia.

In the study of patients following hyperflexion/extension injury (whiplash injury) the question of symptomatic activation of previously quiescent Chiari Type I malformations as a result of exposure to traumatic injury has been reported (8–11). It is not clear how trauma plays a role in the activation of symptoms attributed to a Chiari Type I malformation. Are the symptoms merely coincidental to the trauma or is the condition symptomatically ‘awakened’ by the trauma?

Could the Chiari Appearances Be Caused by the Trauma?

This last question is important, since quite often the presence of tonsillar ectopia is not discovered until after trauma, and acquired tonsillar herniation is radiologically indistinguishable from a pre-

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existing Chiari Type I [12]. In an effort to assess the incidence of Chiari 0 in patients following whiplash injury and also to assess if this observation is better made with the patient scanned upright rather than recumbent (supine), the MRI studies of the cervical spine and base of the skull from 1,200 consecutive neck pain patients 18 years and older presenting to 4 different outpatient radiology centres over a 3-year period were reviewed. Half of the scans (600) were acquired from a facility with a 0.6-tesla upright open architecture MRI scanner. The other half (600) were obtained from a facility with a 0.7-tesla conventional recumbent open MRI scanner. Half were from patients with neck pain following a road traffic accident. Half were from patients with no recent history of trauma.

The resulting 4 groups comprise 300 scans each; recumbent nontrauma, upright nontrauma, recumbent trauma, and upright trauma. The images were interpreted by two radiologists, blinded with regard to the clinical history and scanner type. The scans were categorized by the level of the lowest point of the cerebellar tonsils relative to the basion-opisthion line. (Table 1.) Of the 1,200 scans 5 were considered uninterpretable for tonsil station by one or other of the radiologists. All 5 were in the recumbent trauma group.

Table 1. Grading criteria for tonsil station

Tonsil position

Position relative to the basion-opisthion line

+3 >5 mm above +2 3 to <5 mm above

+1 1 to <3 mm above

0 <1 mm above to <1 mm below

-1 1 to <3 mm below

-2 3 to <5 mm below -3 >5 mm below

Table 2. Age, gender, and average tonsil station.

RNT RT UNT UT

n 300 295 300 300 Mean age, years 57.4 41.5 54.0 39.7

Female/male, % 60/39 65/35 57/42 62/37

Mean tonsil station

Overall 1.1 0.7 0.9 0.1

Male 1.2 0.9 1.1 0.2 Female 1.2 0.6 0.8 0.0

RNT = recumbent nontrauma; UNT = upright nontrauma; RT = recumbent trauma; UT = upright trauma

Amongst the remaining 1,195 subjects the average age was 41.5 and 39.7 years in the trauma groups, and 57.4 and 54.0 years in the non-trauma groups (recumbent and upright, respectively). The majority of subjects were female in all groups. There was excellent agreement between the two readers regarding tonsil station (kappa range 0.85–0.95). Both injury status and scan type (recumbent vs. upright) were associated with significant differences in the average tonsil station (p = <0.0001;Table 2).

In the two non-trauma groups the tonsils were below the basion-opisthion line in 5.7 and 5.3% of cases in the recumbent and upright groups, respectively. In the trauma groups, the tonsils were

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below the basion-opisthion line in 9.5 and 23.7% of cases in the recumbent and upright groups, respectively (χ2=0.0001)

In this study of 1,200 patients, tonsillar ectopia was identified in 1 in 4 trauma patients versus 1 in 18 nontrauma patients. Upright MRI appears to increase the sensitivity of MRI diagnosis of tonsillar ectopia by more than double [13].

Whether or not tonsillar ectopia results from whiplash trauma is open to question. Chiari 0 was found to be approximately 4 times more prevalent in whiplash-injured neck-pain patients than neck pain patients with no recent history of trauma.

Interestingly, the proportion of upright scans with tonsillar ectopia is approximately the same as the proportion of whiplash-injured patients who go on to experience chronic pain symptoms from their injury [14]. In addition to assessing the degree of cerebellar tonsillar ectopia, MRI can be used to make measurement of the skull base and its relationship to the cerebellum and brainstem as well as its relationship to the cervical spine.

The clivoaxial angle also known as the clivovertebral angle is the angle made by a line drawn along the clivus to the basion and a line drawn down the posterior border of the odontoid peg. It should normally measure between 150 and 180°. (Fig. 4)

Fig. 4. The clivoaxial angle

This measurement is a good method for assessing the degree of basilar invagination. A decrease in the normal clivoaxial angle can kink the brainstem and cord, compress the contents of the foramen magnum and spinal canal, and cause Chiari malformations. In addition to the spinal cord, the contents of the foramen magnum also include: (1) the vertebral veins, which drain the brain during upright posture; (2) the vertebral arteries, which supply blood to the brainstem, cerebellum and inner aspects of the temporal and occipital lobes of the brain; and (3) the subarachnoid space of the cord, which contains cerebrospinal fluid (CSF) and is continuous with the cisterns of the brain.

The Grabb-Oakes measurement is also invaluable for the assessment of basilar invagination. On MRI, a line is drawn from the basion to the tip of the posterior inferior C2 vertebra. A perpendicular line is drawn from the b–pC2 line to the dura as shown in Figure 5. A value greater than or equal to 9 mm indicates ventral brainstem compression.

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Fig. 5. The Grabb-Oakes line is indicated in red.

To assess for indications of craniocervical instability, Harris’ lines, measuring the basion axial interval and the basion dental interval should be measured. To measure the basion axial interval, a line is drawn along the posterior aspect of the dens and a measurement between this line and the tip of the basion is made (Fig. 6). The basion dental interval is a distance measured between the tip of the basion and the tip of the dens. Both these measurements should be less than 12 mm. If they are greater than 12 mm then occipitoatlantal disassociation has occurred. These measurements are often referred to as the ‘rule of twelve’.

Fig. 6. Harris lines. The basion axial interval is shown in yellow and the basion dental interval is shown in red.

To determine if there is anterior occipitoatlantal disassociation, the Power’s ratio can be measured. This ratio is a distance between the basion and the posterior spinolaminar line of C1 (BC), divided by the distance between the anterior arch of C1 and the opisthion (AO; Fig. 7). If the Power’s ratio (BC/AO) is greater than 1, then anterior occipitoatlantal disassociation has occurred.

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Fig. 7 Power’s ratio

To assess if there is likely to be basilar invagination, Chamberlain’s line should be drawn between the posterior end of the hard palate to the posterior lip of the foramen magnum, the opisthion (Fig. 8). Basilar invagination is present if the tip of the odontoid peg is more than 3mm above this line.

Fig. 8 Chamberlain’s line

Another measure of possible basilar invagination is to draw a line from the posterior edge of the hard palate to the most caudal point of the occipital curve. This is referred to as McGregor's line (Fig. 9). Basilar invagination is likely if the tip of the odontoid process is more than 4.5 mm above this line.

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Fig. 9 McGregor’s line

The basal angle of the skull can also be measured when assessing for platybasia, which may occur in association with the Chiari malformation as well as other conditions such as osteogenesis imperfecta and craniocleidodysostosis. The basal angle is the angle formed by a line joining the basion with the centre of the pituitary fossa and a second line joining the anterior border of the foramen magnum with the centre of the pituitary fossa (Fig. 10). The normal range for the basal angle of the skull is between 125 and 145°. Angles of greater than 145° are classified as platybasia. Recently, a modified method for measuring the basal angle has been proposed using the angle formed by a line extending across the anterior cranial fossa to the tip of the dorsum sellae connecting to a line drawn along the posterior margin of the clivus (Fig. 11) [15]. This modified method of Koenigsberg et al, gives measurements that are lower than with the conventional method, in the range of 114 –134°

Fig. 10. Basal angle of the skull base. Fig. 11. Basal angle of the skull base. Koenigsberg modification.

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Acknowledgements

Figures 1 and 2: courtesy of Dr. Jean-Pierre Elsig, Zurich, Switzerland. Figures 3–11: courtesy of Medserena Upright MRI Centre, London, UK.

References

[1] http://danny.oz.au/anthropology/notes/human-head-weight . [2] Ball WS, Krone KR. Chiari malformation from Dr Chiari to MR imaging, Radiology 1995:195:602-604. [3] Stevenson KL. Chiari Type II malformation: past, present, and future. Neurosurg. Focus. Feb 15 2004;16(2):E5 [4] Meadows J, Kraut M, Guarnieri M, Haroun RI, Carson BS. Asymptomatic Chiari Type I malformations identified on magnetic resonance imaging. J Neurosurg. 2000 Jun;92(6):920-6. [5] Barkovich AJ, Wippold FJ, Sherman JL, Citrin CM. Significance of cerebellar tonsular position on MR, AJNR 1986;7:795-799. [6] Elster AD, Chen MYM: Chiari I malformations: clinical and radiologic reappraisal. Radiology 183:347–353, 1992. [7] Iskandar BI, Hedlund GL, Grabb PA, Oakes WJ. The resolution of syringomyelia without hindbrain herniation after posterior fossa decompression. J Neurosurg 1998;89: 212–216. [8] Milhorat TH, Chou MW, Trinidad EM, Kula RW, Mandell M, Wolpert C, Speer MC. Chiari 1 malformation redefined: clinical and radiographic findings for 364 symptomatic patients. Neurosurgery 1999, 44:1005-1017. [9] Wan MJ, Nomura H, Tator CH. Conversion to symptomatic Chiari I malformation after minor head or neck trauma. Neurosurgery. 2008 Oct;63(4):748-53; discussion 753. [10] Pratticò F, Perfetti P, Gabrieli A, Longo D, Caroselli C, Ricci G. Chiari I malformation with syrinx: an unexpected diagnosis in the emergency department. Eur J Emerg Med. 2008 Dec;15(6):342-3. [11] Bunc G, Vorsic M. Presentation of a previously asymptomatic Chiari I malformation by a flexion injury to the neck. J Neurotrauma. 2001 Jun;18(6):645-8. [12] Payner TD, Prenger E, Berger TS, Crone KR. Acquired Chiari malformations: incidence, diagnosis, and management. Neurosurgery. 1994 Mar;34(3):429-34. [13] Freeman M.D., Rosa S, Harshfield D, Smith F, Bennett R, Centeno C. J., Kornel E, Nystrom A, Heffez D & Kohles S.S. A case control study of cerebellar tonsillar ectopia (Chiari) and head/neck trauma (whiplash). Brian Injury, July 2010; 24(7-8): 988-994. [14] Freeman MD, Croft AC, Rossignol AM, Weaver DS, Reiser M. A review and methodological critique of the literature refuting whiplash syndrome. Spine 1999;24(1):86-98 [15] Koenigsberg R A, Vakila N, Honga TA, Htaik T, Faerber E, Maiorano T, Dua M, Farob S and Gonzales C Evaluation of Platybasia with MR Imaging AJR 2005 26: 89-92