Phalangeal and Navicular Bone Hypoplasia andHoof Malformation in the Hind Limbs of a Foal

D.R.K. SMITH, D.H. LEACH AND R.J. BELL

8420 - 101 Street, Edmonton, Alberta T6E 3Z3 (Smith), Department ofVeterinary Anatomy (Leach) and Department ofHerd Medicine andTheriogenology (Bell), Western College of Veterinary Medicine, University ofSaskatchewan, Saskatoon, Saskatchewan S7N 0 WO

ABSTRACT

Anatomical anomalies in the hind feetof a seven month old Appaloosa foalwere identified and investigatedthrough the use of gross anatomicaldissection, radiography and angio-graphy. Abnormalities were restrictedto the distal aspect of both hind legs,the right hind leg being more severelyaffected. Anatomically the right footresembled that of an equine fetus ofapproximately 120 days gestationalage. Disruption of vascular perfusionto hoof structures was evident in bothhind legs and was related to areas ofabnormal bone conformation as wellas to areas of abnormal ossificationand calcification. Phalangeal andnavicular bone hypoplasia wereapparent as were soft tissue and jointanomalies. Although the etiology ofthe defects identified remains obscure,several theories are suggested, namelyheritability, acquired defects and thepossible teratogenic effects ofclenbuterol.

Key words: Hind limb digits, hoof,foal, pathology.

R tSU M tHypoplasie phalangienne et sesa-moide, associee a la malformation dessabots des membres posterieurs d'unpoulainLa dissection macroscopique, la radio-graphie et l'angiographie ont permisaux auteurs de proceder a l'identifica-tion et a l'investigation d'anomaliesanatomiques des membres posterieursd'une pouliche Appaloosa. Elles n'enaffectaient que l'extremite distale et le

droit etait le plus gravement atteint;son anatomie ressemblait a celle d'unfoetus equin d'environ 120 jours.L'arret de la perfusion vasculaire desstructures du sabot de chacun des deuxmembres posterieurs etait evident etrelie a des regions de conformationosseuse anormale ou d'ossificationanormale et de calcification. L'hypo-plasie de la troisieme phalange et dupetit sesamoide etait apparente, toutcomme le tissu mou et les anomaliesarticulaires. Meme si l'etiologie desanomalies precitees demeure obscure,elles pourraient etre hereditaires, con-genitales ou imputables aux effetsteratogenes possibles du clenbuterol.

Mots cles: phalanges des membres pos-terieurs, sabot, poulain, pathologie.

I N T R O D U C T IO N

Congenital defects in development ofthe digit are rare in horses (1). Poly-dactylism is the defect with the highestreported incidence in equines (2,3,4,5,6). Leipold and Macdonald (5) de-scribed a case of right forelimb adact-yly and left forelimb polydactyly in aWelsh foal. Absence of the navicularbone (7) and distal phalangeal hypo-plasia or agenesis have been reportedfor the hind limbs in a total of fourhorse or mule foals (8,9). These pre-vious studies described mainly radio-graphic and external gross anatomicalfindings but did not include a detailedexamination of the digit. The presentreport describes a detailed study ofphalangeal and navicular bone hypo-plasia and hoof malformation in anAppaloosa foal.

HistoryOn July 6, 1984 the Western College

of Veterinary Medicine (WCVM),Saskatoon, Saskatchewan admitted aten year old Appaloosa mare with afilly at side. The presenting complaintwas gastrointestinal stasis subsequentto atropine administration for chronicobstructive pulmonary disease(COPD). Treatment for the respira-tory disorder had been undertakenfrom September 27 to October 19,1983. This consisted of clenbuterol(Boehringer Ingelheim (Canada) Ltd.,Burlington, Ontario) (10 mL IV b.i.d.the first day followed by 500 mgper osTID for one week reduced to b.i.d.treatment thereafter). The medicationwas discontinued when the owners,fearing possible teratogenic effects,felt capable of controlling the mare'srespiratory disease through changes inhusbandry. The mare, bred daily fromMay 21 through May 23, 1983 to anunrelated registered stallion, foaled onMay 3, 1984. Other than the COPDpreviously mentioned, both gestationand parturition were uneventful. Thegastrointestinal stasis had beenresolved by July 7 and both the mareand filly were released from WCVM.Though medical attention at

WCVM in July was directed primarilytowards the mare, a subtle hind limbconformational abnormality in thefoal had been detected. At the time, itwas believed to be correctable throughproper hoof trimming. A local farrierwas contacted and all four hooveswer.e trimmed biweekly throughoutthe summer. The conformationalabnormality did not improve and thefarrier elected to try corrective shoe-

Reprint requests to Dr. D.H. Leach.

Can Vet J 1986; 27: 28-34.28

ing. He requested radiographs of thehind limbs for an accurate assessmentof the situation prior to this undertak-ing. Subsequently, the filly was exam-ined and radiographed by WCVMfield service personnel on September12, 1984. She was noted to be verylame on the right hind limb. Slightmuscle atrophy had occurred over theright hip. Both hind hooves weresmaller than normal and the right hindhoof was slightly worn on the lateralwall. Based on the radiographicresults, a diagnosis of malformation ofthe distal phalanx (PIIl) of both hindlimbs was made and a poor prognosisgiven. The foal was euthanized onDecember 10, 1984. One forelimb digitand both hind limb digits wereretained for further study.

MATERIALS AND METHODS

For each hoof the external anatomyand hoof wear were evaluated andphotographs were taken of the lateral,medial, dorsal and weightbearingaspects.Angiography was performed on the

hind limbs. A teat cannula wasinserted into the tibial artery of eachhind limb and barium sulphate(Liquid Polibar, E-Z-EM CanadaLtd., Whitby, Ontario) was injected bymeans of a 10 mL syringe until sub-stantial back pressure and adequateperfusion were obtained. Subsequentto angiography the barium sulphatewas flushed out with normal physio-logical saline and the limbs cut in amidsagittal plane. A detailed dissec-tion of the remainder of each digit wasthen performed.The terminology suggested by

Mishra (10) for blood vessels of theequine digit will be used in this paper.Nomina Anatomica Veterinaria(1983) terminology will also be used,when applicable.

RESULTS

Right Hind LimbExternally, the right hind limb

appeared more normal than the left.No external bruising was evident onthe hoof. The Stratum (S.) externum("S. tectorium") was normal.On sagittal section a number of

abnormalities were seen (Figure 1).Some hoof tubules of the S. mediumwere wavey rather than straight; the S.

FIGURE 1. Midsagittal section of the right hind limb digit. Note that the distal extremity of the distalphalanx (Plll) is missing and that the navicular bone (n) is hypoplastic. The deep digital flexortendon (ddft) is fused with the navicular bone. The coronary border, stratum medium (sm) and sole(s) are abnormally wide. Hemorrhage is evident in the sole and white line (arrowheads). Arrow-wavy pattern of hoof tubules; Pll- middle phalanx.

internum ("S. lamellatum") was unus-ually wide; hemorrhage extended intothe interior part of the coronaryborder; the sole was approximatelyfour times thicker than normal. Inaddition, there was extensive hemor-rhage into the white zone ("whiteline"), sole and a small area of the frogdirectly underneath a rudimentaryPIll. The proliferating zones of thecoronary border and the sole werecontinuous with one another. Thecoronary border and the spacebetween it and Plll were wider thannormal.The proximal third of Plll was nor-

mal in appearance and the extensor

process, though small, accommodatedthe tendon of insertion of the long digi-tal extensor muscle (Figure 1). How-ever, the distal two thirds of PIll, thatpart vascularized by the terminal archand circumflex artery (10), was absent(Figures 2 and 3). The remaining bonewas totally dissociated from the S.internum of the hoof wall. Radio-graphy revealed a number of radiolu-cent areas, one of which appeared to bea lateral fragment from PIll (Figure 3).On gross dissection a very firm digitalcushion was detected and several piecesof cartilage and ossified areas were dis-covered in the craniolateral and cranio-medial edges of the digital cushion.

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FIGURE 2. Lateral-medial radiograph of the right hind limb digit. Note the abnormal shape and sizeof the distal phalanx (PIII) and the navicular bone (n).

FIGURE 3. Anterior-posterior radiograph of the right hind limb digit. Note the abnormal shape ofthe distal phalanx (PIII) and the areas of ossification within the digital cushion (arrowheads).Although PII appears to be asymmetrical, this could be due to poor radiographic positioning.

FIGURE4. Lateral-medial angiograph of theright hind limb digit. A reduced vascular supplyto the digital cushion is evident. The coronaryartery appears intact (arrow).

FIGURE 5. Anterior-posterior radiograph of theright hind limb digit. Note the underdevelopedterminal arch (t) and circumflex artery (c), aswell as the reduced vascular supply to the ossi-fied and partially ossified areas of the digitalcushion (arrowheads).

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Angiography (Figures 4 and 5) showeda compromised vascular supply to theseareas of the digital cushion.The coronary artery which supplies

blood to the coronary borderappeared to be intact on the angio-grams (Figure 4). Branches from thisvessel anastomosed with remnants ofthe terminal arch to form a meshworkof vessels in the parietal corium. Thecircumflex artery, which is locatedinterior to the white zone, was alsounderdeveloped (Figure 5).The deep digital flexor tendon

(DDFT) did not have a tendon sheathand was fused to the distal sesamoid(navicular bone), in addition to insert-ing on PIll. The navicular bone was ofnormal shape but greatly reduced insize (Figure 1). A navicular bursa wasnot present. The extension of the distalinterphalangeal joint space betweenPIll and the navicular bone wasabsent and the two bones were con-nected by ligamentous tissue and smallamounts of cartilage. The articularcartilage of the distal interphalangealjoint appeared thinner than normaland was absent between PllI and thenavicular bone. The middle phalanx(Pll) was abnormally shaped with thedistal one third notably smaller thanthe proximal two thirds (Figure 1).

Left Hind LimbExternally, the left hind limb exhi-

bited a valgus deformity distal to themetatarsophalangeal joint. Themedial hoof wall had grown under tocover part of the sole. The lateral hoofwall had grown out laterally andcurled up. The toe, which was longerthan normal, also curled up. Bruisingof the medial coronary border and S.medium of the medial quarter and heelwas observed.A sagittal section of the digit

revealed the following anomalies(Figure 6): the proximal coronaryborder was slightly wider than normal;the white zone of the hoof wall wasthree times wider than normal andbecame narrower distally; there washemorrhage into the white zone; dis-tally, PIII had rotated away from thewall and the resulting area was filledwith fibrous tissue. PIII was locatedfarther away from the sole than nor-mal. The midcranial aspect of PIll wasconcave and malformation of the dis-

FIGURE 6. Midsagittal section of the left hind limb digit. Note the partially rotated and hypoplasticdistal phalanx (PIll). Also note that the distal interphalangeal joint cavity fails to project betweenthe hypoplastic navicular bone (n) and Pill.

FIGURE 7. Lateral-medial radiograph of the left hind limb digit. Note the abnormal size and shape ofthe distal phalanx (PIll), particularly the concave cranial profile.

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tal two thirds of this bone was evident(Figures 6 and 7).A dense mass associated with the

lateral aspect of PIll was found in theanteriorposterior radiograph (Fig-ure 8). On gross dissection this wasfound to be an area of ossification ofparietal corium. This ossified coriumwas attached to the cranial aspect ofthe hoof and continued for approxi-mately 8.0 cm into the corium of thelateral quarter. Tough fibrocartila-genous and partially ossified tissueseparated this area of ossification fromthe rudimentary PIll. Angiographyrevealed areas of vascular compromiseon the lateral side of the hoof, includ-ing the area of parietal corium ossifica-tion, and the digital cushion (Figures 9and 10). As well, the medial portion ofthe terminal arch was almost completebut the lateral aspect was not, resultingin blood being diverted to more later-ally located vessels (Figure 10).On radiography the medial solar

FIGURE 9. Lateral-medial angiograph of the left hind digit. Note the reduced perfusion of the digitalcushion.

FIGURE 8. Anterior-posterior radiograph of the left hind limb digit. Note the abnormal shape ofthedistal phalanx (PIII), particularly the lack of development on its lateral aspect (L). Also note theossified portion of the parietal corium (arrows) and the presence of the medial solar foramen(arrowhead). The lateral solar foramen is not present.

FIGURE 10. Posterior-anterior radiograph o0the left hind digit. Note the reduced perfusion ofthe terminal arch (t), digital cushion and lateralsolar foramen (arrow). The vascular supply lat-eral to the terminal arch is apparent(arrowhead).

32

foramen of Plll was apparent but thelateral foramen was absent (Figure 8).Angiography revealed that the vesselthat normally passes through thelateral solar foramen was also absent(Figure 10). The circumflex artery wasonly partially developed with thelateral aspect being most affected(Figure 10). Grossly both the DDFTand long digital extensor tendon(LDET) were found to have normalinsertions onto PIll.The navicular bone was normal in

shape but reduced in size (Figure 6). Arudimentary navicular bursa existedlaterally but medially was absentbecause of a strong fibrous fusion tothe DDFT. The distal interphalangealjoint appeared normal except theextension from the joint space betweenthe navicular bone and Pll wasmarkedly reduced in size (Figure 6).

DISCUSSION

Disruptive alterations in embryogene-sis may produce anomalies in structureor function which are present at birth.Such congenital defects may be eithergenetic or environmental in origin.Many exist with no established cause(I) and may occur as part of multiplecongenital defects (8). In cattle,phalangeal reduction may be inheritedthrough a single recessive trait (I 1). Aswith other reported occurrences (8,9),the sporadic nature of this case makesit impossible to document it as aninherited or acquired defect. Regard-less of the cause, it is clear that a dis-ruption of blood vessels had occurredin the hooves of this foal and that thedevelopment of hoof structures wasabnormal.

Several variations from normal vas-cular perfusion were identified in bothhind limbs and these suggest a directrelationship between abnormal bloodflow and anatomical malformation.The medial hoof wall of the right limbwas thicker than normal and alsoappeared to have obtained preferentialblood flow. The distal aspect of theequine Plll receives its major arterialsupply via the terminal arch and cir-cumflex artery (10). It is thus interest-ing to note that the more hypoplasticPIll of the right hind limb also pos-sessed a rudimentary terminal archand circumflex artery (Figure 5).Furthermore, on the left hind limb,where PIll appears more normal on

the medial aspect than on the lateral,the medial aspect also possessed asolar foramen plus a more completeterminal arch and circumflex arterythan did the lateral (Figures 8 and 10).Angiography also revealed a verycompromised blood supply to the digi-tal cushions. Ossification and partialossification of the digital cushionappeared to be related to these sites ofpoor vascularization. A compromisedblood flow to the digital cushion couldproduce hypoxia, which, in turn, hasbeen found to induce ectopic ossifica-tion ( 12). The craniolateral aspect ofthe left hind limb corium also con-tained an area of ossification asso-ciated with reduced vascular supply.such ossification has been reportedpreviously in the bovine hoof (13).

Alternatively one might argue thatabnormal bone or soft tissue develop-ment may result in vascular compro-mise rather than vice versa. Theabnormal development may con-tribute to limb instability and alteredweightbearing. The area involved maythen be more susceptible to trauma, inturn causing inflammation, a disrup-tion of the vascular supply, and there-by promote ossification.

Varying degrees in the severity anddistribution of hemorrhage wereobserved in both hind limbs. Thisrelated well to the amount and propor-tion of weight one would expect eachleg to bear. The left hind leg achievedthe more normal anatomical form,afforded the animal more support andthus was used preferentially. Theextensive bruising observed on themedial aspect of the hoof wall sug-gested that the medial wall was theprimary weight bearing surface. Theright hind was more abnormal andcontributed to the lameness observed.For comfort the filly apparentlyshifted weight off the right onto the leftand, in so doing, minimized theamount of bruising of the right limb.The hemorrhage observed in the righthind hoof indicates that weight, whenborne on this leg, was distributed tothe sole subjacent to Pill. It must bekept in mind, however, that the animalhad been subjected to extensive hooftrimming in an attempt to correct thefoot conformation. It is not knownhow much this affected limb weightbearing and hoof wear.

Several other anatomical abnormali-

ties are worth further comment. Forinstance the DDFT of the right hindlimb lacked a tendon sheath. Beckhamet al (14) attributed tendon sheathabsence and subsequent fusion to lackof limb movement in utero. It is inter-esting to note, however, that in thepresent study such fusion was apparentin only one of four limbs. The navicularbone is believed by some to be anembryological derivative of PIll (15).The fibrocartilagenous material identi-fied between the rudimentary Plll andnavicular bone of the right hind maypossibly be a remnant ofan embryologi-cal link between these two structureswhich is normally not seen.

Third phalanx hypoplasia involvingthe right hind limb of an Appaloosacolt has been reported previously (9).Based on radiographic evidence, astriking similarity exists between itand the condition observed in the lefthind limb of this Appaloosa filly. Thefact that two out of five cases reportedwith this condition were similar radio-graphically and occurred in the samebreed (Appaloosa) may warrantfurther investigation.

Finally, as it was of concern to theowner of the mare, one must considerthe possible teratogenic effects ofclenbuterol. It has been shown pre-viously that clenbuterol does not pro-duce teratological effects in foals ofmares treated with twice the recom-mended dose of this drug at 26, 130 or280 days of gestation ( 16). Teratogeniccompounds usually express them-selves in bilaterally symmetricalanomalies. Although both hind limbswere affected in this filly, these ano-malies were not symmetrical nor equi-valent in severity. It is interesting tonote, however, that the right hind legdevelopment appeared to have beenarrested at approximately 120 days ofgestation (17). This corresponds to thetime of treatment of the mare withclenbuterol.

ACKNOWLEDGMENTS

We thank Dr. F.W. Harris, managerof veterinary medical affairs of Boeh-ringer Ingelheim (Canada) Limited,for bringing to our attention theresearch report on the effect of clenbu-terol on pregnant mares. We alsothank Jim Gibbons for technical helpand Dave Powell, farrier, for informa-tion he provided about this foal.

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REFERENCES

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2. THEILE H. Polydactylism in a foal. Monat-shefte Veterinaermed 1958; 13: 342-343.

3. BLENAU B. KLOS z. A case of polydactylism ina foal. Med Weter 1969; 25: 545-547.

4. EVANS LH. JENNY J. RAKER CW. Surgical cor-

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5. LEIPOLD H. MACDONALD KR. Adactylia andpolydactylia in a Welsh foal. Vet Med SmallAnim Clin 1971; 66: 928-930.

6. McGAVIN MC, LEIPOLD HW. Attempted surgi-cal correction of equine polydactylism. JAm Vet Med Assoc 1975; 166: 63-64.

7. JOHNSON JH. The foot. ln: Mansman RAand McAlister ES, eds. Equine medicineand surgery. Santa Barbara, California:

American Veterinary Publications, 1982:1033-1054.

8. TAYLOR TS. MORRIS EL. Agenesis of the distalphalanx in a mule. Vet Radiol 1983; 24:63-65.

9. BERTONE AL. AANES WA. Congenital phalan-geal hypoplasia in Equidae. J Am Vet MedAssoc 1984; 185: 554-556.

10. MISHRA Pc. Extrinsic and intrinsic veins ofthe equine hoof wall. M.Sc. thesis, Univer-sity of Saskatchewan, 1982.

11 BLOOD DC. RADOSTITS OM, HENDERSON JA.

Veterinary medicine. 6th ed. London: Bail-liere Tindall, 1983.

12. UHTHOFF HK. SARKER K. MAYNARD JA. Calci-

fying tendonitis. A new concept in itspathogenesis. Clin Orthop 1976; 118:164-168.

13. KUBICEK A. Inflammation of the corium ofthe bovine hoof associated with exostoses

on the third phalanx. Vet Med (Prague)1970; 15: 97-101.

14. BECKHAM C. DIMOND R. GREENLEE 1K. Therole of movement in the development of adigital flexor tendon. Am J Anat 1977; 150:443-460.

15. COLLES CM. The embryology of the navicu-lar bone. First international conference onnavicular disease. Newmarket, England,1984.

16. HAMM D. NAB 365 (Clenbuterol, Ventipul-min): evaluation of teratogenicity in theequine. Unpublished data generatedthrough contract research with BoehringerIngelheim to support FDA registration ofclenbuterol. 1981.

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LETTER TO THE EDITOR

Euthanasia of ReptilesDecapitation: An InhumaneMethod of Slaughter for theClass "Reptilia"

DEAR SIR:

It was previously thought thatdecapitation was a humane method ofeuthanasia for reptiles. This led torecommendations for its use in at leastthe following publications: Ball andBellairs (1), Cooper and Jackson (2),Frye (3) and Duphar VeterinaryLimited (4). However, recent discus-sions between veterinary surgeons andspecialists have resulted in the con-demnation of this practice (5,6).

Since the recent publications did notoffer a broad statement with theannouncement recommending discon-tinuation of decapitation, a briefexplanation of why this practiceshould be more widely condemned isas follows:The reptillian metabolism is

renowned for its ability to function at alow respiration and heart rate. It istherefore reasonable that nerve tissueis far more tolerant of a reduction inoxygen supply than, for example,mammals and can withstand compara-

tively long periods of induced hypo-tension and anoxia. One hears ofanecdotal accounts where snakes andlizards indicate consciousness follow-ing decapitation, as the head may beseen to react to an approach byattempting to defend itself, respond totouch with movement and respond tolight with pupil dilation and contrac-tion. Klauber (7) was one of the first todocument such reactions as much as59 minutes after decapitation. How-ever, he made no conclusions regard-ing the 13 rattlesnakes, used in hisexperiments, ability to feel pain.

It has been suggested that such ahigh transection of the spinal cordwould induce rapid and sufficient neu-rogenic shock to incapacitate normalcentral nervous system functions andreduce or eliminate sensitivity to pain.For various reasons it would be irre-sponsible for anyone to offer approvalon this point alone as the duration andtype of reactions suggest that the"shock" effect is insufficient to reduceawareness significantly.CLIFFORD WARWICK36 Beech A venueDrakes BroughtonPershore, Worcs WRIO 2JBEngland

References1. BAILL DJ. BELLAIRS Ad-A. The U.F.A.W. (Uni-

versities Federation for Animal Welfare)handbook on the care and management oflaboratory animals, 5th ed. Edinburgh:Churchill Livingstone, 1976.

2. COOPER JE. JACKSON OF. Diseases of the repti-lia. London: Academic Press, 1981.

3. FRYE FL. Biochemical and surgical aspects ofcaptive reptile husbandry. Kansas: Veteri-nary Medicine Publishing Company, 1981.

4. DUPHAR VET-ERINARY LIMITED. The manage-ment of exotic animals. Southampton:Duphar Veterinary Limited, 1982.

5. COOPERJEet al. Euthanasia of tortoises. VetRec 1984; 115: 635.

6. WARWICK C. Euthanasia of tortoises. Vet Rec1985; 1 16: 82.

7. KLAULBER IM. Rattesnakes. 2 vol. University ofCalifornia, 1956.

Editor's NoteMethods for humanely killing repti-

lia are being considered by the Scien-tific Advisory Panel of the WorldSociety for the Protection of Animals.Further information may be obtainedfrom Mr. Colin Platt, Coordinator,Scientific Advisory Panel, WSPA, 106Jermyn Street, London, SWIY 6EE,United Kingdom.

34 Can Vet J 1986; 27:34.