Claerhoudt Et Al-2012-Equine Veterinary Journal

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Differences in the morphology of distal border synovialinvaginations of the distal sesamoid bone in the horse as evaluatedby computed tomography compared with radiography

S. CLAERHOUDT†, H. J. BERGMAN‡, H. VAN DER VEEN‡, L. DUCHATEAU§, E. V. RAES† and J. H. SAUNDERS*†

†VeterinaryMedical Imaging and Small AnimalOrthopaedics, Faculty of Veterinary Medicine, GhentUniversity, Merelbeke, Belgium‡LingehoeveDiergeneeskunde/VetCT, Lienden, The Netherlands§Department of Physiologyand Biometry, Faculty of VeterinaryMedicine, GhentUniversity, Merelbeke,Belgium.

*Correspondenceemail: [email protected]; Received:04.05.11;Accepted:17.12.11

Summary

Reasons forperformingstudy:Distalbordersynovial invaginationsof thedistal sesamoidbone areradiographicallyassessed duringthe selectionprocessof horses admittedas breedingstallions or in purchaseexaminations. Nowadays, manymoderatelyor somedeeply penetrating proximally enlargedsynovialinvaginationsare considered as moderate or severe radiographicfindings.Objective: To measure the difference between and agreement of the morphology of distal border synovial invaginations on radiography vs. computedtomography (CT). It was hypothesised that the morphology of distal border synovial invaginations would be better evaluable on CT comparedwith radiography.Methods: Computed tomography scans and 3 dorsoproximal–palmarodistal oblique (DPr-PaDiO) radiographs were obtained on 50 cadaver forefeet

from 25 Warmblood horses. Computed tomography was assumed to be the gold standard. The number, shape and depth of penetration of distalborder synovial invaginations into the distal sesamoid bone were evaluated with both methods, and the comparison of their measurements wasstatistically described.Results: A statistically significant meandifferencefor number of distal synovialinvaginations between CTand all 3 DPr-PaDiO projections wasfound andwasapproximatelyequal to 2, meaningthat CTpermits visualisationof an averageof 2 moreinvaginations thanradiography. In noneof the casesdid radiographyhave a higher number observedthan CT. A large variationin the difference of measurements for depthof penetration against theirmean difference betweenCTand the3 radiographicprojections was seen. Radiographyunderestimated thedepthof invaginations, andmore so when these were deeper. There wasno statistically significant meandifference found between the techniquesfor depth. A moderate to goodagreement between measurements on CT and thethree DPr-PaDiO projections for shape was seen, in which the D55°Pr-PaDiO projection showed the best agreement. A high specificity (90–99%) and lowsensitivity (65%)for all projections for shape were found.Conclusions and potential relevance: Radiography differs considerably from CT concerning the morphology of distal navicular border synovialinvaginations. For the evaluation of the number, depth and shape of distal synovial invaginations in the distal sesamoid bone, radiography shows onlypartially the morphologyseen on CT.

Keywords: horse; distal sesamoid bone;Warmblood horse; synovial invagination; radiography; computed tomography

Abbreviations

CT:ComputedtomographyDPr-PaDiO: Dorsoproximal-palmarodistal obliqueDSB:Distal sesamoid bone

Introduction

The terms podotrochleosis, navicular syndrome or navicular diseasedenote a chronic, progressive uni- or bilateral forelimb lameness typicallyaffectingridinghorsesof middle age[1,2].Radiographic evaluationplaysanessential rolein the diagnosisof naviculardisease;however, radiographyislimited to changes of the bony component of the distal sesamoid bone

(DSB, also called the navicularbone).During the selection process of horses admitted as breeding stallionsor in purchase examinations, the synovial invaginations of the distalborder of the DSB are often graded according to radiographicclassification systems, using a dorso45°–70°proximal-palmarodistaloblique (D45°-70°Pr-PaDiO) radiographic projection. Although opinion isdivided, some clinicians consider many moderately or some deeplypenetrating rounded or inverted flask-shaped synovial invaginations asmoderate or severe radiographic findings. These changes have beensuggested by some authors to be associated with joint pain andlameness, and would impair a horse’s future sport career [3,4].Consequently, abnormal synovial invaginations are responsible fornegative advice in purchase examinations and may therefore have majorfinancial consequences for horse owners. Although many authors

describe these findings related to navicular disease, there is stilldiscussion about their significance [1,5–8].

Computedtomography(CT)is themost appropriate imagingmodalityfordetailed imaging of normal bone and detection of bony disorders [9–11].This imaging modality wasassumedby theauthors to be thegoldstandardforevaluationof theDSB in thepresentstudy.

We hypothesised that the morphology of distal border synovialinvaginations of the DSB would be better evaluable on CT than onradiography. The purpose of the study was to demonstrate thishypothesisby measuringthe difference between andagreement of the morphology ofsynovial invaginationsof the DSB on radiography vs. CT.

Materials and methods

Material

The material used in this study consisted of 50 forefeet of 25 Warmbloodhorses (mean age 7 years). All horses were subjected to euthanasia forreasons unrelated to this study. All feet were severed at the level of thefetlock joint immediately after euthanasia. The shoe and loose horn in thesole, if present, were removed, and the frog was cleaned. The feet werenot selected by any particular criteria, and both forefeet of each horsewere included.

Computed tomography examination

The CT scans were performed with a 4-detector row spiral CT scannera, inwhich the feet were placed in the gantry with the longitudinal axis of the

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Equine Veterinary Journal ISSN 0425-1644

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foot oriented parallel to the CT table andperpendicular to the plane of theCTgantry. Themedialside of thefootwas marked. Thelimbs were scannedin a distal-to-proximal direction. The output parameters were 120 kV and250 mA s per slice. The slice thickness was 0.6 mm, pitch of 0.875 cm, 0.3increment and 1 s rotation time. Transverse CT scans were reconstructedfrom the level of the distal aspect to the level of the proximal aspect of theDSB using a bone window setting (window level, 200–600 H.U.; windowwidth, 1000–2000 H.U.), 250 mm field of view and 512 ¥ 512 pixel matrix.

Theaveragetotal timerequired forscanning of eachfoot was46.25 s. Fromthe transverse images, sagittal and dorsal reconstructions, with a slicethicknessof 0.6 mm, werereformatted using of softwareb.

Radiographic examination

Radiographic examination was performed after the CT examination. Thesulci of the frog were packed with modelling compoundc. Threedorsoproximal-palmarodistal oblique (DPr-PaDiO) radiographic projectionswith differenthoof angles (D45°Pr-PaDiO, D55°Pr-PaDiO and D65°Pr-PaDiO)wereperformed onall feet. Thex-raybeamof thetubed waskept horizontalandcentred 2 cm proximalto thecoronary band at themidline of thefoot.Thefootwasplacedonawoodenblockwithaslopeof45°tothehorizontal.Using wedges (slope 5°),D55°Pr-PaDiOand D65°Pr-PaDiOprojectionsweremade of all feet. Thefeet were radiographed using 60 kV and12.5 mA s, agrid(6:1 ratio, 103 lines/cm)and a 100 cm focus–filmdistance.

Image analysis

Two observers, one board-certified radiologist (J.H.S.)and one PhDstudent(S.C.), interpreted all images together and a diagnosis was made byconsensus. The radiographic images of a particular foot and hoof anglewere reviewedin a randomised orderat thesame workstation, on the samediagnostic imaging screense and using a similar evaluationf, to determinethe number of distal border synovial invaginations. Furthermore, for eachsynovial invagination, thedepthand shape were determined. Next, theCTimages of a particular foot were reviewed in a random order to determinethe number of distal border synovial invaginations using transverse slicesand dorsal reconstructions, and for each synovial invagination the depthand shape were determined.

In a second step, the corresponding radiographic and CT images wereconsidered together. To compare depth and shape assessments on the 2imaging modalities, only synovial invaginations for which an assessment

was available on both radiography and CT were used (some invaginationsseen with CTwerenot seen with radiography).

The depth of penetration of the synovial invaginations was assessed onthe dorsal CT and radiographic images. Each synovial invagination wascalculatedby an imaging software programb, using the following equation:depth (R) = A/B, where A is thedistance(in centimetres)between themostdistal basis and the proximal top of the synovial invagination and B thedistance (in centimetres) between the distal and proximal flexor bordersof the DSB. Data on depth were classified into the following 3 categories:1 = R 0.33, 2 = 0.330.5.

The shape of the synovial invaginations was assessed on dorsal CT andradiographic images. The shape could be categorised as ‘conical’, ‘linear’,‘lollipop’ or ‘branched’ (4 categories, further described as shape4), with1 = normal (conicalor linear shaped)and 2 = abnormal(lollipop or branchedshaped; further described as shape2).

Data analysisTo compare the observed number of invaginations and the depth of theinvagination between CT and the DPr-PaDiO projections, Student’s pairedt test wasusedwith foot as block variable forthe number andinvaginationas block factor forthe depth.The results were summarised by the averagedifference and corresponding 95% confidence interval (CI) and 95%reference interval. The 95% reference interval is given by the meandifference 2 s.d., which contains 95% of the actual differences if thenormal distribution assumption holds. Bland-Altman plots are provided(Figs S1 and S2) for CT vs. the different DPr-PaDiO projections, toinvestigate a possible relationship between the difference and themagnitude of the measurement. A global significance level of 0.05 wasused, but each of the 3 pairwise comparisons was tested at a

comparisonwise significance level equal to 0.0125 (Bonferroniadjustment).

Thedegree of agreementbetween CTand theDPr-PaDiOprojections fornumber anddepth (taken as categorical variables) was quantifiedusing theweighted k statistic. The degree of agreement for shape was quantifiedusing the unweighted k statistic. The guidelines for strength of agreementbased on the values of k were as follows:


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thanradiography. The D45°Pr-PaDiO projectionshowedthe smallest meandifference. The corresponding 95% reference intervals, as well as the 95%CIs, were verywide forall 3 comparisons,reflectinga greatvariation in the

differences (Table 1). The Bland-Altmanplots of the differences for numberbetween themethods against their meansare shown inFigure S1.The weighted k valuesfor all3 projectionswerevery low, specifically for

the D55°Pr-PaDiO and D65°Pr-PaDiO projections, meaning that a greaterdisagreement with CT for number was calculated for these 2 projections(Table 2).

Depth

The linear measurements of depthof synovialinvaginations (measurement A of the equation) and distance between the distal and proximal flexorborders (measurement B) increased with radiographic angle in 25 of 50(50%) DSBs. There were no significant mean differences fordepthbetweenCT and the 3 radiographic projections, and the confidence intervals werealso narrow, meaning that there seems to be little or no bias. The meandifferences of measurements for depthbetweenCT and the 3 radiographicprojections were all positive and small, with the D45°Pr-PaDiO projection

showing the smallest mean difference. By evaluating reference intervals, itis possible to see how precise the individual estimates are. Consequently,the reference intervals for all 3 DPr-PaDiO projections showed quite wide,comparable ranges (Table 1). Ninety-five per cent of differences betweenCTand the differentDPr-PaDiOprojectionsfor depth lie between thelimits-0.28and0.32oftheinterval(0.28belowor0.32abovezero-level).Also,theBland-Altmanplots showed a large variationin the differences against theirmeans (see Fig S2). It is illustrated that as the mean measurements of CTand radiography increase (larger equations; deeper invaginations), thedifferences (measurements CT minus radiography) also seem to increase,meaning that the underestimation by radiography was greater in the caseof deeper invaginations(Fig 2).

The k statistics also revealed quite poor agreement between thetechniques (average k value of 0.21 and low weights to disagreements, assummarised in Table 2).

ShapeInonly3 of11(27%),4 of7 (57%)and3 of6 (50%)feetwithanequalnumberofsynovial invaginations on both the CT scans and D45°Pr-PaDiO,D55°Pr-PaDiO and D65°Pr-PaDiO projections, respectively, was the shapecomparable by both methods. The agreementfor shape4 ranged between0.42k 0.50,representing a moderateagreement, whereas the k valueforshape2 was higher (range 0.55k 0.71), representinga moderate togood agreement. Weighted k for shape was higher for the D55°Pr-PaDiOprojection, meaning that, relative to the other projections, a betteragreement with the gold standard for shape was calculated forthis projection.

The k and weighted k values for agreementof number, depthand shapeare presented in Table 2. The sensitivity, specificity (both calculated for

shape2) and corresponding 95% CIs for all 3 DPr-PaDiO projections forshape,withCT as gold standard,are summarised in Table 3.

Discussion

The morphological features of the distal navicular border synovialinvaginationsof the present population were describedin a previousstudy[13] using CT. The present investigation was carried out to assess thevariability and agreement between the appearance of distal bordersynovial invaginations of the DSB on radiographs vs. CT examinations.

Histology is regarded as the gold standard for the diagnosis of tissueabnormalities [14]. In the present study, no histological examination was

TABLE 2: Agreement between computed tomographic and 3

radiographic projections for number, depth and shape (*: only

unweighted k was calculated for shape2)

Radiographicprojection Categorical variable k Weighted k

D45°Pr-PaDiO Number 0.12 0.24

D55°Pr-PaDiO Number 0.02 0.17

D65°Pr-PaDiO Number 0.01 0.15D45°Pr-PaDiO Depth 0.23 0.30

D55°Pr-PaDiO Depth 0.19 0.26

D65°Pr-PaDiO Depth 0.23 0.29

D45°Pr-PaDiO Shape4 0.49 0.57



D45°Pr-PaDiO Shape2 0.68* –



Fig 2: Dorsally reconstructed CT image (a) and corresponding D65°Pr-PaDiOradiographic image (b) of a distal sesamoid bone, showing a deeply penetratinginvagination on the CT image (arrow), which is mildly penetrating on the radiographic

image (arrow). Lateral is on the left side and medial on the right side of the image. Anexampleof a false-negativeresult isshownin Fig3.

Fig 3: Dorsally reconstructed CT image (a) and corresponding D55°Pr-PaDiOradiographic image (b) of a distal sesamoid bone, showing 2 abnormally shapedinvaginations on the CT image (arrows), which were normally shaped on the

radiographic image (arrows). Lateral is on the left side and medial on the right side ofthe image.

S. Claerhoudt et al. Evaluation of distal navicularborder synovial invaginations



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performed; however, owing to the possibility of reconstruction ofmultiplanar, high-resolution images without superimposition, CT providesdetailed anatomical information on the synovial invaginations [11].Therefore, CTwas assumed by theauthorsto be thegoldstandard.

The total number of synovial invaginations counted on CT was muchhigher than with radiography. The differences between CT and the 3DPr-PaDiO projections for the number of synovial invaginations were allstatistically positive, with the D45°Pr-PaDiO projection showing thesmallest mean difference. In fact, CT permitted visualisation of an averageof 2 more invaginations per navicular bone than with radiography,indicating a better visibility of invaginations on CT than with radiography.Similar conclusions were reported earlier [10,11]. The synovialinvaginations that were ill defined or undetectable on radiography were

mostlysmalland located at thedistal sloping borders of theDSB on theCTimages. It has been described that the presence of small synovialinvaginations at the sloping borders on CT may be observed in normalDSBs, owing to lack of superimposition of surrounding bone and the highsensitivity of CT for detecting bone in detail [11]. However, the clinicalsignificance of thesesubtle CT findings remains questionable.

Inapproximately 80%of thecases inour study, a DSBwith7 invaginationson radiography had more than 7 distal border invaginations on CT.According to the literature, up to 7 radiographically detectable distalborder synovial invaginations are considered normal, and more than 7significant [15,16], although an overlap between sound andlame horsesisdescribed [5]. However, the clinical relevance of this increased number ofinvaginationson CT remains unclear, and further researchis required.

The present results show that when the mean measurements for depthon CT and radiography increase, the differences (measurements CT minusradiography) alsoseem to increase,resultingin a larger underestimationby

radiography in case of deeper invaginations. As described above, CTappeared better in evaluating synovial invaginations than radiography,owing to the better visibility of subtle changes on CT [9–11]. On CT, mostdeepinvaginations ended proximally as very tiny, deeply penetrating lines,which were undetectable on radiography. Therefore, care should be takenin judging the depth of distal border invaginations on radiographs duringpurchase examinations,because deeply penetrating invaginationsmay bemissed on DPr-PaDiO projections. It is reported that deeply penetratingdistal border invaginations are significant radiographic findings that couldbe responsible forfuture joint painand lameness [3,4]; however, the clinicalsignificance of subtle CT findings remains unclear. Further investigationwithclinicalassociation is necessary to determine the importance of thesedeeply penetrating, tinysynovialinvaginations.

In thepresent study, thesensitivity andspecificity forshapeof thedistalnavicular border synovialinvaginations werecalculated on the3 DPr-PaDiOprojections using CT as the gold standard. For radiography as diagnostic

modality, both a high sensitivity (i.e. high number of correctly identifiedabnormal shaped invaginations) and a high specificity (i.e. correctlyidentified absence of abnormally shaped invaginations) are desired.False-positive diagnosis (poor specificity) of abnormally shapedinvaginations can have major consequences, because the literaturedescribes these findings to be related to navicular disease [1,5–8].However, ourresults show an almost 100% specificity forall projectionsforshape, meaning that almost no false-positive results were seen. On thecontrary, more false-negative results were present, resulting in a muchlower sensitivityof 65% forshape.In otherwords,an abnormalinvaginationon radiography is effectively abnormal, but a normal one can in factbe abnormal.

The present results show a variable degree of agreement (k values)between measurements on CT and the DPr-PaDiO projections for the 3

variables. Alldatafor shape were groupedinto 2 categories (2 ¥ 2 table)forshape2 and4 categories(4 ¥ 4 table)for shape4, resultingin variablevaluesof k . For theresulting2 ¥ 2 tablea betteraveragek value of 0.65was found,compared with k = 0.47 for the 4 ¥ 4 table. In contrast, data on numberswere classified into 12 categories (0 being the lowest number ofinvaginations found and 11 the highest), logically resulting in very lowk values. In theory, any value of k much below 0.5 will indicate pooragreement.However, despite thesepublishedguidelines [12],no value of k

can be regarded universally as indicating some degree of agreement [17].In fact, the value of k depends on the number of categories and uponcircumstances, as demonstrated in our results. For multiple categories onan ordinal scale, weighted k hasthe advantagethat it ‘weights’the degreeof disagreements. Greater disagreement is penalised more, resulting inlower weighted k values.

Theresults of the present study showedthat the variability of theactualdifferences between CT and radiography is high for number and depth ofpenetration of distal navicular border synovial invaginations. This can beexplained by 3 factors. A first factor is the variable orientation of thesynovialinvaginations in theDSB. Indeed, a recent study hasdemonstratedthat theorientation of thedistal bordersynovial invaginations into theDSBcan vary from a straight, dorsoproximal to a palmaroproximal direction[13]. A second factor is the variable height of the heels. Pearce et al. [18]demonstrated that the degree of distal interphalangeal joint angulationincreases (increased joint flexion) with heel elevation, and van Dixhoorn

et al. [19] reportedthatthe DSBfollows thecoffin bone in vitro duringdistalinterphalangeal joint flexion. Thus, elevation of the heels results in at leastan increasedupright motionof theDSB in thesagittalplane. Finally, a thirdfactor is the superimposition of the DSB over other structures on aDPr-PaDiOprojection,preventingvisualisation of theexact pointof origin ofthesynovial invaginations [10]. Thedistal contour of theDSB on DPr-PaDiOprojections is visualised as 2 lines, one representing the articular borderand the second the flexor border, with the distal border synovialinvaginationsbeing situated in the groove between theseborders [16,20].

A consequence of the variable orientation of the invaginations into thebone andof thelarge individual variationof heel height is that thedepthofthe distal navicular border synovial invaginations relative to the horizontalx-ray beam varies individually when the front of the hoof wall is angledforward at approximately 45,55 and65°. In fact, when elevating theheels,the depth of dorso- and palmaroproximal oriented synovial invaginationson DPr-PaDiO radiographic projections respectively shortens and enlarges

relative to the degree of heel elevation. The opposite effects are obtainedby loweringthe heels.A potential limitation of this study could be the absence of a

palmaroproximal-palmarodistal oblique projection, which permitsevaluation of the DSB without superimposition. However, this projectiononly allows evaluation of the number and width of the distal borderinvaginations[5]. Therefore, it was not included in our study.

In conclusion, the results of the present study indicate that radiographydiffers significantly from CT concerning the morphology of distal navicularborder synovial invaginations. CT is a much more sensitive method for thedetection of these invaginations; therefore, regardless of the exact clinicalmeaning of the synovial invaginations, thecriteria as used forradiographycan absolutely not be used unchanged in case of CT examination.Prospective epidemiological studies are necessary to assess the clinicalsignificance of CT-detected abnormalities in thisarea.

Authors’ declaration of interestsNo conflicts of interesthavebeen declared.

Source of funding

This study was financed by the ‘Bijzonder Onderzoeksfonds’, GhentUniversity.

Acknowledgements

The authors would like to thank Kim Claus and Marnix Verdonck fortechnical assistance. We thank Katrien Vanderperren for constructivecriticismof the manuscript.

TABLE 3: Sensitivity and specificity for all 3 radiographic projections

for shape with computed tomography as gold standard

Radiographic

projection

Sensitivity

(95% confidence

interval)

Specificity

(95% confidence

interval)

D45°Pr-PaDiO 0.65 (0.51–0.78) 0.97 (0.92–0.99)

D55°Pr-PaDiO 0.65 (0.51–0.78) 0.99 (0.95–1)D65°Pr-PaDiO 0.63 (0.48–0.76) 0.90 (0.84–0.95)

Evaluation of distal navicular border synovial invaginations S. Claerhoudt et al.

682 Equine Veterinary Journal 44 (2012)679–683© 2012 EVJ Ltd


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Manufacturers’ addresses

aMx8000, Philips Medical Systems, AE Eindhoven, The Netherlands.bOsirixImage processingSoftware,Geneva, Switzerland.cPlaydoh®:Rainbow Crafts, Cincinnati,Ohio, USA.dMobilux, X-rayEquipmentVerachtert, Antwerpen, Belgium.eTotokumonochromeLCD display, Lewisville, Texas,USA.fMicrosoft Excel, Microsoft Corp.,Redmond, Washington, USA.

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Supporting Information

Additional Supporting Information may be found in the online version ofthis article:

Fig S1: Bland–Altmanplots: differences of counted numbers (readings) oncomputed tomographic and radiographic images (A: D45°Pr-PaDiO; B:D55°Pr-PaDiO and C: D65°Pr-PaDiO) against their means. The numericalcoderepresentsthe number of distal sesamoidbones (totalsum of 50)withthe same difference in number against mean. Dashed line representszero-level (no difference), upper line = mean + 2s.d., middle line = mean,lower line = mean – 2s.d. s.d. = standard deviation; 95%RI = 95% referenceinterval;95%CI = 95% confidence interval.Fig S2: Bland–Altman plots: differences of the equations of depth(readings) on computed tomographic and radiographic images (A:D45°Pr-PaDiO; B: D55°Pr-PaDiO and C: D65°Pr-PaDiO)against their means.Each individual plot (O) represents a synovial invagination (total of 295plots). Dashed line represents zero-level (no difference), upper line = mean+ 2s.d., middle line = mean, lower line = mean – 2s.d. s.d. = standarddeviation;95%RI = 95% reference interval;95%CI = 95% confidenceinterval.

Please note: Wiley-Blackwell are not responsible for the content orfunctionality of any supporting materials supplied by the authors. Anyqueries (other than missing material) should be directed to thecorrespondingauthor for the article.

S. Claerhoudt et al. Evaluation of distal navicularborder synovial invaginations


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Claerhoudt Et Al-2012-Equine Veterinary Journal