DOI 10.2478/pjvs-2013-0001

Original article

Bone mineral density (BMD) and computertomographic measurements of the equine

proximal phalanx in correlation with breakingstrength

P. Tóth1, C. Horvath2, V. Ferencz2, B. Tóth3, A. Varadi4, O. Szenci1, G. Bodó5

1 Clinic for Large Animals, Faculty of Veterinary Science, Szent Istvan University,2225 Ullo, Dóra major, Hungary

2 First Department of Medicine, Semmelweis University of Medicine, Budapest, Hungary3 Department of Veterinary Clinical Sciences, Purdue University, West Lafayette, IN, USA4 Faculty of Veterinary Science, Szent Istvan University, Budapest, Hungary, senior student5 University of Bern, Department of Clinical Veterinary Science, Equine Clinic, Switzerland

Abstract

Despite the fact that bone mineral density (BMD) is an important fracture risk predictor inhuman medicine, studies in equine orthopedic research are still lacking. We hypothesized that BMDcorrelates with bone failure and fatigue fractures of this bone. Thus, the objectives of this study wereto measure the structural and mechanical properties of the proximal phalanx with dual energy X-rayabsorptiometry (DXA), to correlate the data obtained from DXA and computer tomography (CT)measurements to those obtained by loading pressure examination and to establish representativeregion of interest (ROI) for in vitro BMD measurements of the equine proximal phalanx for predic-ting bone failure force.

DXA was used to measure the whole bone BMD and additional three ROI sites in 14 equineproximal phalanges. Following evaluation of the bone density, whole bone, cortical width and area inthe mid-diaphyseal plane were measured on CT images. Bones were broken using a manually control-led universal bone crusher to measure bone failure force and reevaluated for the site of fractures onfollow-up CT images. Compressive load was applied at a constant displacement rate of 2 mm/minuntil failure, defined as the first clear drop in the load measurement.

The lowest BMD was measured at the trabecular region (mean ± SD: 1.52 ± 0.12 g/cm2; median:1.48 g/cm2; range: 1.38-1.83 g/cm2). There was a significant positive linear correlation between trabel-cular BMD and the breaking strength (P=0.023, r=0.62). The trabecular region of the proximalphalanx appears to be the only significant indicator of failure of strength in vitro. This finding shouldbe reassessed to further reveal the prognostic value of trabecular BMD in an in vivo fracture riskmodel.

Key words: bone mineral density, DXA, CT, breaking strength, first phalanx, horse

Correspondence to: P. Tóth, email: Toth.Peter@aotk.szie.hu, tel.: +36 306 070 537

Polish Journal of Veterinary Sciences Vol. 16, No. 1 (2013), 3–8

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Introduction

Stress fractures are considered as one of the mostsignificant causes of economic losses in race horseindustry. According to large retrospective studies,80% of musculoskeletal injuries in the US (Johnsonet al. 1994) and 60% in the UK (Vaughan et al. 1975)are fatal in racehorses. Fractures of the proximalphalanx are one of the most common incidences dur-ing training (Vaughan et al. 1975) and during thedaily fracture repair at equine clinics as well (Smith2010). The most severe longitudinal and comminutedfractures are also observed in the first phalanx(Rooney 1969). Most fractures appear “sponta-neous” despite that they are the summation of com-plex processes with numerous factors involved (Bax-ter and Turner 2002).

The density of bony structures correlate to skel-etal strength and stiffness, which can be estimated byDXA (dual energy X-ray absorptiometry) in people(Genant et al. 1994, Genant et al. 1996, Grier et al.1996). Further, as a quantitative method, DXA alsohas the ability to reveal and monitor changes in bonestructural properties in humans and in various in vivoanimal models (Griffin et al. 1993, Turner et al.1995, Grier et al. 1996). Previous research in horsesfocused on the structural and mechanical propertiesof the third metacarpal bone (Bynum et al. 1971, ElShorafa et al. 1979, Nunamaker et al. 1989) and theproximal sesamoid bones (Young et al. 1991), al-though little is known about the biomechanical prop-erties of the first phalanx (Thompson et al. 1996,Dzierzęcka and Charuta 2012).

Thus, the objectives of this study were to corre-late the data obtained from DXA and CT (computertomography) measurements to those obtained byloading pressure examination. Further, this experi-ment aimed to establish representative ROI (regionof interest) of the equine proximal phalanx for pre-dicting bone failure force. We hypothesized thatbone failure force correlates to bone mineral density(whole bone; medial, lateral and trabecular region)and to the morphometric parameters of the proximalphalanx (cortical width, cortical area, total bonewidth).

Materials and Methods

Samples

Proximal phalanges of the frontlimbs were in-volved in the study. The horses were euthanised un-related to muscolosceletal injuries at Szent IstvanUniversity, Faculty of Veterinary Science, Clinic for

Large Animals, Ullo, Hungary. After dissection andmanual removal of all soft tissue, the bones werestored in ethyl-alcohol at room temperature untilmeasurements as previously validated (Beaupied et al.2006). The horses were: 5 ± 3 years old (mean ± SD,median: 5.29 years). There were 4 Lipizzaners, 1 Hun-garian half-blood, 1 Hungarian sporthorse, 1 Arabian.Gender distribution was the following: 5 mares, 1 stal-lion and 1 gelding. Horses were used for either pleas-ure (n=3. 42%), carriage-driving (n=2. 29%) orbreeding (n=2. 29%) purposes.

Bone mineral density (BMD) measurement

Bones were examined post mortem with a den-sitometer (Norland XR-26a) at the First Departmentof Medicine, Semmelweis University of Medicine,Budapest, Hungary. Imitation of soft tissue aroundthe bone was required for the software algorithm usedto measure the BMD. Therefore, a 20 mm plexiglasswas used as a substitution for soft tissue as describedin detail elsewhere (Tóth et al. 2010). Bones weremeasured once from dorsopalmar direction (Tóth etal. 2010). As the first step, the BMD of the wholebone was measured followed by selection of three 1x1cm ROIs. The ROIs were the entire bone; the medialcortex (CM), the lateral cortex (CL) at the level of thehorizontal axis of the mid-third of the bones and thetrabecular region of the sagittal plane of the proximalthird, 3 mm under the level of the deepest point of themetacarpophalangeal joint surface of the proximalphalanges (T) as shown in Fig. 1.

Fig. 1. DXA image of a proximal phalanx from dorsopalmardirection. Region of interests (ROIs) of the first phalanx.T: trabecular or cancellous bone, MC: medial cortex, LC:lateral cortex.

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Computer tomographic (CT) measurements

Bones were scanned with a commercially availablecomputer tomography unit (Siemens Somaton Emo-tion 6 Multislice CTb) using the following settings: 130kV, 20 mAs, slides: 2 mm; at Kaposvar University,Institute of Diagnostic Imaging and Radiation Oncol-ogy, Kaposvar, Hungary. Morphometric parametersof the proximal phalanx were taken at mid-diaphysealplane using a Siemens SIENETb software. Cortexwidth was measured from dorsal, lateral, medial andpalmar sides, then the bone total width in either dor-sopalmar and lateromedial directions (Fig. 2). Corti-cal area was calculated from these data using an equa-tion described by Sherman et al (1995). CT imageswere repeated after loading test to reveal the fracturesites.

Fig. 2. Transverse CT image at the level of the mid-dia-physeal region of a proximal phalanx. DT: diameter trans-versa; DS: diameter saggittalis; CM: cortex palmaris;CL: cortex lateralis; CD: cortex dorsalis; CM: cortex me-dialis.

Loading test

Biomechanical properties of proximal phalangeswere assessed at Budapest University of Technologyand Economics, Laboratory of Biomechanical Re-search. For loading pressure examination a universalbone crusher (ZD-20c universal testing machine) wasused. Due to the lack of previous ex vivo data regard-ing the first phalanx’s breaking force measurements,the machine was arbitrarly set for human lumbar spi-nal preset due to the similar cuboid shape. In order toposition the bone properly during measurements, theproximal and distal articular rimms of the P1 boneswere removed at the level of the deepest point of themetacarpophalangeal (proximal) and proximal inter-

phalangeal joint (distal) articular surfaces of theproximal phalanges by a bandsaw (Fig. 3). The boneswere subjected to loading pressure from a proximodis-tal direction, due to the convex shape of thelatero-medial site, which would have prevented accu-rate pressure loading. Bone failure strength was cal-culated from loading pressure values.

Fig. 3. ZD-20 universal testing machine. The bones weresubjected to loading pressure from a proximodistal direc-tion. The proximal and distal articular rimms of the P1bones were removed at the level of the deepest point of themetacarpophalangeal (proximal) and proximal interphalan-geal joint (distal) articular surfaces of the proximalphalanges by a bandsaw.

Statistical Analysis

Statistical analysis of the data was performed witha commercially available program (Minitab 16d).Mean, standard deviation, median and range werecalculated for bone mineral density, cortical area, cor-tex width, bone width, loading pressure, and breakingforce. Distribution of the data was assesed with theShapiro-Wilk test. Pearson’s linear correlation wasused to reveal any association between bone mineraldensity values (whole bone BMD, traecular BMD, lat-eral cortical BMD, medial, cortical BMD), corticalarea, cortical width (lateral, medial, dorsal, and pal-mar regions), bone width (saggittal, transversal) andbone breaking strength and loading pressure. Statisti-cal significance was set at P«0.05 and an adequatelinear correlation was assumed if regression coeffi-cient was greater than 0.6 (r>0.6).

Bone mineral density (BMD)... 5

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Results

Samples

14 proximal phalanges from 7 cadavers were usedin the study. 1 phalanx was excluded from the statisti-cal evaluation because following loading test examin-ations the fracture site could not be located on the CTimages.

Bone mineral density (BMD) measurement

Total bone BMD (g/cm2), lateral cortex BMD,medial cortex BMD, trabecular BMD were as shownin Table 1.

Table 1. Descriptive statistical data of the variables meas-ured across the 13 proximal phalanges in this study.

Variable N Mean SD Median Range

Whole BMD (g/cm2) 13 1.91 0.14 1.96 1.68-2.13

CL BMD (g/cm2) 13 2.19 0.15 2.2 1.95-2.51

CM BMD (g/cm2) 13 2.1 0.13 2.05 1.93-2.35

T BMD (g/cm2) 13 1.52 0.12 1.48 1.38-1.73

Compression strength(MPa) 13 74 15.56 72.56 49.96-100

Breaking force (kN) 13 72 13.36 74 45-92

CM (cm) 13 0.97 0.47 1.09 0.22-1.44

CL (cm) 13 0.83 0.45 1 0.15-1.34

CD (cm) 13 0.39 0.13 0.43 0.15-0.59

CP (cm) 13 0.53 0.23 0.63 0.09-0.8

DT (cm) 13 4.66 0.299 4.75 4.17-5.18

DS (cm) 13 2.8 0.55 2.6 2.28-3.78

Area (cm2) 13 5.4 1.90 6.06 2.47-8.1

BMD – bone mineral density, DT – diameter transversa,DS – diameter saggittalis, CM – cortex palmaris, CL – cortexlateralis, CD – cortex dorsalis, CM – cortex medialis,T – trabecular or cancellous bone, SD – standard deviation).

Computer tomographic morphometricmeasurements

Data are summarized in Table 1 as means of threeconsecutive measurements of each parameter. Frac-ture lines were identified in the sagittal plane in 13(92.86%) of 14 specimens. In 5 of 13 (38.46%) casesthe fracture lines were located in the proximal andmid-third, in 6 of 13 (46.15%) cases the fracture lineswere located in the mid and distal-third and in 2 of 13(15.38%) cases fracture lines were located in themid-third in the sagittal plane.

Loading test

Values of compression force and failure force aresummarized in Table 1.

Correlations

Significant positive linear correlation was foundbetween trabelcular BMD and the breaking force(P=0.023, r=0.62). Other parameters did not signifi-cantly correlate with the breaking force or compres-sion force as shown in Table 2.

Table 2. Pearson’s linear correlations.

Breaking Compressionforce [kN] strength [MPa]Variable

Whole bone BMD [g/cm2] P=0.068 n/a P=0.224 n/a

CM BMD [g/cm2] P=0.055 n/a P=0.377 n/a

LC BMD [g/cm2] P=0.479 n/a P=0.267 n/a

T BMD [g/cm2] P=0.023 r=0.62 P=0.514 n/a

CL width [cm] P=0.533 n/a P=0.746 n/a

CM width [cm] P=0.576 n/a P=0.921 n/a

CD width [cm] P=0.681 n/a P=0.587 n/a

CP width [cm] P=0.787 n/a P=0.564 n/a

DS [cm] P=0.482 n/a P=0.611 n/a

DT [cm] P=0.690 n/a P=0.1 n/a

Area [cm2] P=0.581 n/a P=0.868 n/a

r value is only indicated if P<0.05).BMD – bone mineral density, DT – diameter transversa,DS – diameter saggittalis, CM – cortex palmaris, CL – cortexlateralis, CD – cortex dorsalis, CM – cortex medialis,T – trabecular or cancellous bone, n/a – not applicable).

Discussion

The lowest BMD was observed in the trabecularROI. Both the anatomy and physiology of thetrabecular region differs from cortical region (Good-ship and Smith 2004). It is composed of smalltrabeculae with a lower mineral content. Unlike thecortical region, the trabecular region is not only underthe regulation of vitamin D, calcitonin or parathyroidhormone, but local forces can also induce marked re-modeling (Lawrence 2005) enabling this region to re-spond to mechanical forces directly. Loss of trabecu-lar bone induced by immobilization has been welldocumented in people (Kazarian and von Gierke1969) and is characterized by a complete loss or thinn-ing of trabeculae (Ijiri et al. 1995).

This in vitro study revealed a significant positivelinear correlation between the trabecular region BMDand failure strength. This result coincides with the cli-

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nical evidence that fracture of the trabecular region isthe most common in the proximal phalanx (Nixon2012). In this study post-fracture CT images revealedthat most fracture lines were located in the sagittalplane at the proximal or distal trabecular regions,similarly to an earlier retrospective study (Ellis et al.1987). Thus, it would be important to focus on thisregion in further studies, as the trabecular region ap-pears to be the key component in sagittal proximalphalanx fractures. Proximal phalanx fractures are cat-egorized as sagittal or transverse, the latter extendsacross the bone and does not involve articular surfaces(Ellis et al. 1987). Sagittal proximal phalanx fracturesare categorized as incomplete or complete. Although,the most common fracture of the proximal phalanx isthe sagittal fracture, breed and usage are importantpredisposing factors. Fractures of the palmar/plantarprocesses can occur in Standardbreds (Ruggles 2003),while dorso-frontal fractures can occur both in Stan-dardbreds (Ruggles 2003) and Throroughbreds(Stashak 2002) raced on hard surface. Despite the co-inciding results, it must be emphasized that sagittaltrabecular fractures are currently attributed to themechanical effect of the saggital ridge of the thirdmetacarpal bone (Nixon 2012), which was not part ofour in vitro model. Davies performed proximodistalloading of equine metacarpal bones with both endsembedded in fibreglass-impregnated resin (Davies2009), which also did not account for the mechanicalload of the proximal articular surface. Since neitherDavies’ nor our in vitro approaches are exact modelsof in vivo strains, the relationship between thetrabecular region of the proximal phalanx and the sag-ittal ridge of the metacarpus, and to evaluate thecharectiristics and effects of the subchondral bone un-der the proximal articular surface of the bone war-rants further investigation.

During training, microcracks may occur withoutevidence of lameness and with complete recovery tonormal function after a short period of rest (Baxterand Turner 2002). The bone may withstand a particu-lar strain until remodels or, less frequently, the micro-cracks progress to macroscopic stress fractures(Nunamaker et al. 1990). Light work (compared toregular training load) or immobilization (e.g. longerperoid of stall rest) will decrease BMD in horses,while intense training without transition increases theincidence of bone fractures (Nunamaker et al. 1990).The bone has a dynamic structure and remodels withexercise (Riggs 2002). BMD has been shown to de-crease with inactivity or increase with high level oftraining (Sherman et al. 1995). Due to the insidiousnature of stress fractures, there would be a need of anin vitro diagnostic tool that correlates or predictsfracure risk in performance horses. Since our resultsindicate that there is a significant correlation between

failure of strength and trabecular BMD, this hypoth-esis could be tested in vivo as well.

Correct positioning of the patient/subject is a criti-cal part of the densitometry. DXA machine convertsa three-dimensional structure into a two-dimensionalimage. Elliptical bones may have different BMD valuedepending on the position of the bone (Rozenberg etal. 1995). In this in vitro experiment bones were meas-ured once from dorsopalmar direction, as describedpreviously (Tóth et al. 2010). Nevertheless, in vivomeasurements would require careful limb positioningand deep sedation.

In conclusion, this study suggests that thetrabecular region is the sole ROI in predictingfailure of strength of the proximal phalanx. In futurestudies identification of the fracture lines andmeasurement of the BMD of those particular areasshould also be investigated. Further, in vivo experi-ments are also warranted to reveal whether or notthe trabecular BMD data are useful indicator of frac-ture risk evaluation of the proximal phalanx inhorses.

Acknowledgement

The authors would like to acknowledge the Sur-gery Department at the Large Animal Clinic, thedensitometry laboratory of the First Department ofMedicine at the Semmelweis University, the Labora-tory of Biomechanical Research of the BudapestUniversity of Technology and Economics and the In-stitute of Diagnostic Imaging and Radiation Oncol-ogy of the Kaposvhr University for contributing tothis study with their specialized equipment and ex-pertise.

Abbreviations

DXA – dual energy x-ray absorptiometryCT – computer tomographBMD – bone mineral densityP1 – proximal phalanxROI – region of interest

Manufacturers’ adresses

a – Norland XR-26, Norland Corporation, Fort Atkin-son, WI, USA

b – Siemens AG, Erlangen, Germanyc – ZD-20 Universal Testing Machine, Jyoti Ltd, East

Germany & FIB make (India)d – Minitab Inc., PA, USA

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