morphometric study of the equine navicular bone: variations with breeds and types of horse and...

J. Anat. (1998), 193, pp. 535–549, with 10 figures Printed in the United Kingdom 535

Morphometric study of the equine navicular bone: variations

with breeds and types of horse and influence of exercise

ANNICK GABRIEL1, SANDRA JOLLY1, JOHANN DETILLEUX2, CE; CILE DESSY-DOIZE3

BERNARD COLLIN1 AND JEAN-YVES REGINSTER4

"Departments of Anatomy, #Biostatistics and $Histology, Faculty of Veterinary Medicine, and %Bone and Cartilage

Metabolism Unit, University of Lie[ ge, Belgium

(Accepted 14 July 1998)

Navicular bones from the 4 limbs of 95 horses, classified in 9 categories, were studied. The anatomical bases

were established for the morphometry of the navicular bone and its variations according to the category of

horse, after corrections were made for front or rear limb, sex, weight, size and age. In ponies, navicular

bone measurements were smallest for light ponies and regularly increased with body size, but in horses,

navicular bone dimensions were smallest for the athletic halfbred, intermediate for draft horse,

thoroughbreds and sedentary halfbreds and largest for heavy halfbreds. The athletic halfbred thus showed

reduced bone dimensions when compared with other horse types. Navicular bones from 61 horses were

studied histomorphometrically. Light horses and ponies possessed larger amounts of cancellous bone and

less cortical bone. Draft horses and heavy ponies showed marked thickening of cortical bone with minimum

intracortical porosity, and a decrease in marrow spaces associated with more trabecular bone. Two distinct

zones were observed for the flexor surface cortex: an external zone composed mainly of poorly remodelled

lamellar bone, disposed in a distoproximal oblique direction, and an internal zone composed mainly of

secondary bone, with a lateromedial direction for haversian canals. Flexor cortex external zone tended to be

smaller for heavy ponies than for the light ponies. It was the opposite for horses, with the largest amount

of external zone registered for draft horses. In athletic horses, we observed an increase in the amount of

cortical bone at the expense of cancellous bone which could be the result of reduced resorption and

increased formation at the corticoendosteal junction. Cancellous bone was reduced for the athletic horses

but the number of trabeculae and their specific surfaces were larger. Increased bone formation and reduced

resorption could also account for these differences.

Key words : Bone remodelling; navicular disease.

Knowledge the histological architecture of the nav-

icular bone is an important basis for understanding

the reason why some breeds and types of horse are

more susceptible to develop navicular disease (Gabriel

et al. 1994). Navicular disease represents a chronic

forelimb lameness in horses. This condition is a

painful degenerative disease which may include the

navicular bone, the navicular bursa and adjacent

surface of the deep digital flexor tendon in one, or

more often both front feet. The disease is considered

to be responsible for one third of chronic forelimb

Correspondence to Dr Annick Gabriel, Service d’Anatomie, Faculte! de Me!dicine Ve! te! rinaire, Universite! de Lie' ge, Bd de Colonster, B43,

4000 Lie' ge (Sart Tilman), Belgium. Fax: 32 43 66 41 22.

lameness in all horses (Colles, 1982). The disease

occurs most frequently in performance horses and is

seldom seen in Arabians, ponies and heavy breeds

(Hickman, 1989). American Quarter horses and

warmbloods appear particularly susceptible (Rose,

1996). Despite the high incidence of the disease and

the numerous research studies that have focused on it,

the disease still remains the cause of much controversy

and confusion, not only with regard to its nomencla-

ture, aetiology and pathogenesis, but also to its

radiological features and treatment (Wright &

Douglas, 1993). The 2 major theories concerning its

pathogenesis are circulatory disturbances (Colles &

Hickman, 1977; Rijkenhuizen, 1989) and alterations

in the biomechanics of the digit. According to the

mechanical theory, the pathogenesis of the navicular

syndrome is due to a disproportion between the

anatomical conformation and the mechanical load.

Mechanical factors, such as concussion, compression,

friction and tension from ligaments associated with

the size, shape and balance of the foot and the shape

of the navicular bone, have an aetiological role in the

syndrome (Rooney, 1969; Østblom et al. 1982, 1989;

MacGregor, 1986; Pool et al. 1989; Ratzlaff & White,

1989; Wright & Douglas, 1993; Dik & Van Den

Broeck, 1995). Nevertheless, little information is

available on normal navicular bone measurements,

although several authors have postulated changes in

bone dimensions in cases of navicular disease (Wintzer

& Da$ mmrich, 1971; Verschooten et al. 1989).

Qualitative variations at the tissue or cellular levels

may easily be studied by microscopic examination,

but quantitative variations generally escape this kind

of research. Morphometry uses stereological methods

to obtain quantitative information on cellular or

tissue structure and its modification in normal or

pathological states (Weibel, 1967, 1992; Cruz-Orive &

Weibel, 1990). A useful estimate of mechanical

strength of the bone may be gained by determining the

amount and structure of cortical and cancellous bone

histomorphometrically (Savage et al. 1991).

Histomorphometric analyses have only recently

been reported in the investigation of navicular bone

disease in the horse (Østblom et al. 1989). The

importance of normal reference material as a basis for

comparison when diagnosing disease in an individual

is well known, but such material is currently not

readily available for the horse. Information on the

effects of exercise on cortical bone in horses exists but

no reports on these effects on short bones or on

cancellous bone have been published (Jeffcott, 1992).

The aim of this investigation was thus to study the

anatomical and the microscopic appearances of the

navicular bone from various morphological types of

horse, using quantitative methods (morphometry and

histomorphometry) and to determine the variations

induced by exercise.

Anatomical considerations

The navicular bone (Os sesamoideum phalangis

distalis) is located between the deep digital flexor

tendon and the distal interphalangeal joint. Its distal

border is broad and convex and united to the distal

phalanx by the distal impar ligament (Ligamentum

sesamoideum distale). The articular surface (Facies

Fig. 1. Navicular bone: sagittal section. 1, Articular surface ; 2,

hyaline cartilage ; 3, cortical bone; 4, collateral sesamoidean

ligament; 5, proximal border ; 6, flexor surface; 7, internal cortical

bone; 8, external cortical bone; 9, fibrocartilage; 10, sagittal ridge;

11, distal impar ligament; 12, distal border ; 13, articular surface for

the distal phalanx; 14, medulla : cancellous bone.

articularis) is directed by dorsoproximally. The nav-

icular bone and distal phalanx are joined together by

a narrow articular surface (palmar facet). The flexor

surface (Facies flexoria) is directed palmodistally and

forms the scutum distale (Scutum distale) which

provide a gliding surface for the deep digital flexor

tendon. The flexor surface is divided by the sagittal

ridge. The navicular bursa (Podotrochlear bursa) lies

between the tendon and the navicular bone. The

elastic suspensory ligament of the navicular bone

comprising the medial and lateral collateral sesa-

moidean ligaments (Ligamenta sesasmoidea-

collateralia), arises dorsal to the collateral ligament of

the pastern joint. It then passes in a distopalmar

direction and curves axially to be inserted on the

navicular bone wing tips and roughened proximal

border (Barone, 1996; Nickel et al. 1986; Collin,

1993). The 2 articular surfaces of the navicular bone,

for the middle and distal phalanges, are covered by

hyaline cartilage while the flexor surface is covered by

fibrocartilage. Each has a subchondral bone plate and

the intervening medulla consists of trabeculae with

a regular dorsoproximal}palmarodistal arrangement

(Fig. 1).

Animals

A total of 121 horses were initially included in the

study but following macroscopic and radiographic

536 A. Gabriel and others

Table 1. Categories of horses

Number of horses

Morphometric study Histomorphometric study

Horse categories

(with their compactness index)

Draft horse (5±06³0±86) 13 7

Heavy halfbred (3±99³0±32) 5 2

Type I halfbred (3±14³0±19) 10 4

Type II halfbred (3±18³0±4) 15 14

Thoroughbred (2±76³0±29) 5 5

Fjord (3±78³0±32) 9 6

Heavy pony (3±3³0±23) 8 4

Pony (2±99³0±24) 8 7

Light pony (2±42³0±2) 22 12

evaluation of their feet and navicular bones, only 95

perfectly normal individuals were kept. The macro-

scopic and radiographic criteria used to separate

normal from diseased navicular bones have been

described previously (Gabriel, 1997) and were based

on the studies of MacGregor (1986), Denoix et al.

(1988), Verschooten et al. (1989), Kazer-Hotz &

Ueltschi (1992), Pleasant et al. (1993) and Dik & van

den Broeck (1995). Age was estimated by examination

of the incisor teeth according to the tables developed

by Barone (1966). The withers height was measured

with a metric tape for each horse and their weights

were recorded.

Nine categories of horses were defined according to

their breed and type (Table 1). An initial distinction

was made between young (! 2 y) and adult horses

(" 2 y). Horses with a withers height less than 1±45 m

were indexed as ponies. To classify the young horses

in the same way, their adult height was calculated

from growth tables (Martin-Rosset, 1983). The

compactness index (weight}height) was used to

further classify the ponies and horses.

Although their compactness index was similar, the

horses classified as halfbred type 1 and 2 were

separated. Indeed, type 2 horses were sound per-

formance horses from the Large Animals Surgery

department of the Faculty of Veterinary Medicine,

who died suddenly because of serious surgical gastro-

intestinal complications.

Methods

Morphometric study of the navicular bone

Navicular bones were extracted from the 4 hooves of

95 horses. Navicular bone morphometry was

evaluated by means of different measurements as

Fig. 2. Distal and palmar aspects of the navicular bone. 1, Articular

surface width; 2, length of the bone; 3, flexor surface width; 4,

medial width of the flexor surface; 5, lateral width of the flexor

surface; 6, flexor surface thickness.

illustrated in Figure 2. The largest width was measured

for the articular surface and the flexor surface. The

largest thickness was measured at the level of the

distal sagittal ridge. The width of the flexor surface

was also divided into medial and lateral widths. The

greatest length of the bone was determined at the level

of the sagittal ridge. Navicular bone volume was

calculated as described by Gabriel et al. (1997b).

Histomorphometric study of the navicular bone

Navicular bones from 61 horses were studied (Table

1). They were extracted as soon as possible after death

(maximum 10 h postmortem), fixed and dehydrated in

absolute methanol, immersed in chloroform for

defatting, cleared in toluol and embedded without

Equine navicular bone 537

Fig. 3. Test system used for estimating Vv

and Sv.

previous decalcification in methyl methacrylate

(Dhem, 1965). The embedded navicular bones were

cut into 120 µm thick serial sections with a vertical

diamond wire saw (Well, type 3241, Switzerland). The

axis of the sections was vertical with an arbitrary

rotation (Baddeley et al. 1986; Gundersen & Jensen,

1987; Michel & Cruz-Orive, 1988; Mathiasen et al.

1991; Gabriel et al. 1997b). Sections were ground

manually to a uniform thickness of 70–80 µm. Surface

staining of the sections was performed either with

methylene blue or with Goldner’s trichrome (Schenk

et al. 1984) and the sections were then mounted for

study. The microscope (Olympus, BH-2, Germany)

was provided with an objective allowing projection of

microscopic fields on a test system that consisted of

staggered cycloids (Fig. 3). Three to 5 sections per

bone were studied to evaluate navicular bone histo-

morphometry. For each section the following

parameters (Fig. 3) were measured by point counting

to determinate volumes (Vv%): Articular cortex:

mineralised cartilage, cortical bone, porosity ; Flexor

cortex: mineralised cartilage, cortical bone, external

cortical bone, internal cortical bone, porosity ; Distal

border ; Proximal border ; Mineralised part of the

distal impar ligament ; Mineralised part of the col-

lateral ligaments ; Cancellous bone: trabeculae and

marrow spaces.

Sv(Trabeculae, Cancellous Bone) (trabeculae density

surface) was determined by intercept counting with

the cycloids. Vv(Trabeculae, Cancellous Bone) (tra-

becular bone volume); total trabecular bone surface

(S ) and volume (V ), and the ratio S}V or trabeculae

specific surface (Parfitt et al. 1983) were then calcu-

lated.

Statistical tests

To estimate effects of breed and type of horse on

navicular bone morphometry and histomorphometry,

an analysis of variance was conducted with procedure

GLM (SAS, 1990). Horse category estimates were

adjusted to a common effect of front and rear limb,

sex, weight, size and age. A logarithmic transform-

ation was applied to navicular bone volume and

trabecular surface and volume, a ‘rank’ transform-

ation (SAS, 1990) was applied to flexor cortex internal

zone, and a square root transformation was applied to

the mineralised part for the distal impar ligament to


obtain data more normally distributed than the

original measurements.

Morphometric study of the navicular bone

All navicular bone measurements varied significantly

(P! 0±0001) with horse type. Within the horse

categories, navicular bone measurements were the

smallest for type 2 halfbred, except for the flexor

surface largest thickness. Draft horses, thoroughbred

and halfbred type 1 had similar bone measurements,

whereas heavy halfbred possessed the biggest nav-

icular bones. As for the ponies, bone measurements

were the smallest for light ponies, intermediate for

ponies, and significantly larger for heavy ponies and

the Fjord type. Table 2 gives the main results.


All navicular bone histomorphometric data varied

significantly with horse type, except for Vv for

proximal border and trabecular specific surface

(Table 3).

Comparisons between horses and ponies

The main results are listed in Table 4.

Articular surface (Fig. 4). The Vv

for articular

surface cortex, mineralised cartilage and cortical bone

was generally smaller for light horses and ponies and

larger for heavy horses and ponies. On the other hand,

porosity was more important for the lighter animals.

Flexor surface. The Vvfor flexor surface cortex and

cortical bone was generally larger for light horses and

ponies and smaller for heavy horses and ponies.

Mineralised cartilage volume was larger for the

heavier animals and porosity was larger for the lighter

ones. In ponies, the external zone of the flexor cortex

tended to be more developed for light ponies whereas

Table 2. Variation of navicular bone measurements within horse categories

Draft horse Type 1 halfbred Type 2 halfbred Fjord Light pony

Articular surface largest breadth (cm) 0±62 (***) 0±64 (***) ®0±02 0±38 (**) 5±33

Largest length of the bone (cm) 0±23 (***) 0±2 (***) 0±1 0±09 (*) 1±57

Flexor surface largest breadth (cm) 1 (***) 0±72 (***) 0±17 0±57 (***) 5±02

Flexor surface lateral breadth (cm) 0±59 (***) 0±5 (***) 0±17 0±32 (***) 2±52

Flexor surface medial breadth (cm) 0±43 (***) 0±24 (*) 0±005 0±28 (***) 2±48

Flexor surface largest thickness (cm) 0±08 0±22 (**) 0±13 0±12 1±96

Ln (Navicular bone volume) (cm$) 0±21 (***) 0±27 (***) 0±09 0±12 (*) 1±79

Statistical significance is expressed with respect to the light pony: *P! 0±05; **P! 0±010; ***P! 0±001.

Table 3. Statistical significance of the variation of histo-

morphometric data with horse type

Horse type

Volume (%)

1. Articular surface cortex 0±0001

Mineralised cartilage 0±001

Cortical bone 0±0001

Porosity 0±003

2. Flexor surface cortex 0±0008

Mineralised cartilage 0±005

Cortical bone 0±002

Porosity 0±0001

External zone 0±014

Rank of internal zone 0±008

3. Distal border cortical bone 0±0005

4. Proximal border cortical bone 0±11

5. o (Mineralised part for impar lig.) 0±003

6. Mineralised part for collateral lig. 0±01

7. Cancellous bone 0±002

Trabeculae 0±0001

Marrow spaces 0±0004

Cancellous bone characteristics

TBV (%) 0±0001

S (trabeculae, cancellous bone) (mm#}mm$) 0±0006

Ln (V (trabeculae)) (mm$) 0±0001

Ln (S (trabeculae)) (mm#) 0±0001

S (trabeculae)}V (trabeculae)) (mm#}mm$) 0±08

in horses it was larger for heavy horses (Fig. 5). The

internal zone of the flexor surface tended to be more

developed in light horses. Thus in horses, the internal

and external zones of the flexor cortex varied in an

opposite way, as light horses tended to have a larger

portion of internal zone and less external zone while it

was the opposite for heavy horses. The external zone

mainly consisted of some remodelled circumferential

lamellar bone disposed in a distoproximal oblique

direction, with few secondary osteons. External zone

porosity seemed to be more important than that of the

internal zone. The internal zone was highly remodelled

and consisted mainly of secondary osteons. The

haversian canals had a lateromedial oblique orien-

tation.


Table 4. Variation of histomorphometric data within horse category

Draft horse Type 1 halfbred Type 2 halfbred Heavy pony Light pony

Volume (%)

1. Articular surface cortex 1±19 ®0±64 4±93 (*) 7±86 (***) 13±35

Mineralised cartilage 0±61 0±53 1±14 (**) 1±18 (***) 1±43

Cortical bone 2±32 ®0±25 4±77 (**) 7±53 (***) 9±88

Porosity ®1±69 (***) ®0±81 ®0±9 (*) ®0±76 (*) 1±92

2. Flexor surface cortex ®3±14 ®1±33 4±15 (*) ®0±06 23±36

Mineralised cartilage 2±52 (***) 1±46 (**) 1±75 (***) 1±22 (**) 0±37

Cortical bone ®2±84 ®0±94 4±86 (*) 0±82 19±33

Porosity ®2±58 (***) ®1±44 (**) ®2±11 (***) ®1±69 (***) 3±1External zone ®7±64 (***) ®8±17 (***) ®6±19 (***) ®1±17 12±87

Rank of internal zone ®0±52 0±14 1±12 (*) 0±36 ®1±28

3. Distal border cortical bone 2±22 (***) 0±29 1±23 (*) 0±44 1±27

4. Proximal border cortical bone 1±26 (*) 0±47 1±02 (*) 1±1 (*) 1±47

5. o (Mineralised part for impar lig.) 0±37 ®0±3 0±06 ®0±27 0±58

6. Mineralised part for collateral lig. ®0±05 0±009 0±002 0±34 (***) 0±03

7. Cancellous bone ®1±39 1±64 ®11±8 (**) ®9±7 (**) 59±82

Trabeculae 2±79 2±36 ®1±97 1±33 21±19

Marrow spaces ®4±17 ®0±72 ®9±82 (**) ®11±03 (***) 38±62

Cancellous bone characteristics

TBV (%) 4±34 1±8 3±54 11±92 (***) 37±04

S (trabeculae, cancellous bone) (mm#}mm$) 0±2 0±06 0±27 ®0±08 3±5Ln (V (trabeculae)) (mm$) 0±47 (***) 0±38 (**) 0±09 0±26 (*) 0±12

Ln (S (trabeculae)) (mm#) 0±4 (*) 0±33 (*) 0±05 ®0±05 2±39

S (trabeculae)}V (trabeculae)) (mm#}mm$) ®0±77 ®0±52 ®0±49 ®2±58 (**) 9±85

Statistical significance is expressed with respect to the light pony: *P! 0±05; **P! 0±01; ***P! 0±001.

Fig. 4. Articular surface cortex volume in some horses and ponies. Statistical significance is expressed with respect to the light pony.

*P! 0±05; **P! 0±01; ***P! 0±001.

Cancellous bone (Fig. 6). The Vv

for cancellous

bone was generally larger for light horses and ponies

and smaller for the heaviest animals. Heavy horses

and ponies possessed more trabeculae with a larger

trabecular bone volume (TBV) and total trabeculae

surface and volume, whereas light horses and ponies

had more marrow spaces and a larger trabeculae

specific surface.

Distal and proximal borders. The Vv

for distal and

proximal borders was generally smaller for light

horses and ponies and larger for heavy horses and

ponies.

Mineralised parts of ligaments. The Vv

for the

mineralised part of the distal impar ligament was

smaller for light horses and ponies and larger for the

heavier animals. The mineralised part of the collateral


Fig. 5. Composition of flexor surface cortex in some horses and ponies.

ligaments varied differently in horses and ponies : it

was larger for heavy ponies but smaller for draft

horses.

Differences between type 1 (sedentary) and type 2

(athletic) halfbred

The results are listed in Table 4 and illustrated in

Figures 7 and 8. In type 2 halfbred horses, the

navicular bone possessed larger Vvfor articular surface

cortex (mineralised cartilage and cortical bone), flexor

surface cortex (mineralised cartilage, cortical bone,

external and internal cortical bone), distal and

proximal borders and the mineralised part of the

distal impar ligament. On the other hand, smaller Vv

were observed for articular and flexor surface cortex

porosities, cancellous bone (trabeculae and marrow

spaces), and the mineralised part of the collateral

ligaments. The type 2 halfbred horses also possessed

larger TBV, Sv(Trabeculae, Cancellous Bone) and a


Fig. 6. Cancellous bone volume and trabecular bone volume in some horses and ponies. Statistical significance is expressed with respect to

the light pony. *P! 0±05; **P! 0±01; ***P! 0±001.

Fig. 7. Volume (%) of articular surface cortex for type 1 and 2 halfbreds. Statistical significance is expressed with respect to the light pony.

*P! 0±05; **P! 0±01; ***P! 0±001.

larger trabeculae specific surface, whereas total tra-

becular surface and volume were smaller than for the

type 1 halfbred.

Navicular bone morphometry

Navicular bone measurements were smaller for the

light ponies and increased progressively with pony

size with maximal dimensions for the Fjord type.

Different observations were noted in horses. Navicular

bone dimensions were smallest for athletic halfbred

horses, intermediate for draft horse, thoroughbred

and sedentary halfbred and largest for the heavy

halfbred.

After excluding technical errors and individual

variation, we considered that smaller navicular bone

dimensions could be related to the reduction in hoof

measurements we had observed in a previous study


Fig. 8. Cancellous bone volume and trabecular bone volume (%) for type 1 and 2 halfbreds. Statistical signification is expressed with respect

to the light pony. *P! 0±05; **P! 0±01; ***P! 0±001.

(Gabriel et al. 1997a). Indeed, athletic halfbred hooves

were smaller than in the other horse categories, and

this situation did not improve when the horse aged.

Athletic horses are often shod as early as at 2 y of age,

and we speculate that early shoeing might slow hoof

growth and result in hoof atrophy. The horseshoe

restricted horn deformation, especially in the caudal

region, precluding the hoof normal shock absorber

role.

The differences observed between athletic and

sedentary horses could also be related to the growth

period, the intensity of sporting activity and the time

this activity had begun. The primary role of the

appendicular skeleton is to provide rigid structures to

withstand and transmit loads involved in locomotion.

The overall shape and anatomical relationships of a

bone are genetically determined but its final form,

mass and detailed architecture are influenced by

mechanical activity and are therefore a unique

achievement for each animal (Lanyon et al. 1982). The

bone’s ability to withstand loads depends on 2 main

factors : (1) its structural geometry, encompassing

mass and 3-dimensional shape, and (2) the mechanical

properties of the materials of which it is composed.

The shape and size of a bone are in large part

determined during growth (Martin, 1991).

Shape and size changes are located on bone surfaces

(periosteal and endosteal) and, during growth, there

is more modelling than remodelling. Adults have little

capacity for changing their bone shape and size,

because modelling is reduced in rate and extent, but

on the other hand remodelling can be increased by

changes in mechanical loading. The effects of exercise

loading on the skeletal system can vary because of

many factors, such as exercise intensity, skeletal

maturity, type of bone (trabecular or cortical) and

anatomical location (weight-bearing vs non weight-

bearing regions) (Raub et al. 1989). Rapidly growing

bone is more sensitive to mechanical loading than

mature bone. Low intensity training may stimulate

long-bone length and girth increase (Raub et al. 1989),

whereas high-intensity training may inhibit bone

growth (Matsuda et al. 1986; Carter, 1987). In long

bones, both an absence or an excess of physical

activity can delay normal growth and we believe it

could be the same for the navicular bone. To explain

adequately the difference in bone morphometry we

had observed between type 1 and 2 halfbreds, it would

have been useful to have known the horse’s history.

It can be concluded that the athletic halfbred, when

compared with other horse categories, shows a

reduction in navicular bone dimensions, which

involves an increase in the total applied mechanical

load for similar work.


Comparisons between horses and ponies

Navicular bone architecture. Light horses and ponies

possessed larger amounts of cancellous bone but less

cortical bone (articular cortical bone, distal and


Fig. 9. Architecture of the navicular bone in some horses and ponies.

proximal border cortical bone) (Fig. 9). Bone is able

to adjust its architecture in relation to its functional

strain environment, the objective of which is assumed

to be an appropriate compromise between form,

mass, strength and need for tissue economy (Carter,

1987). It has long been recognised that a relationship

exists between the severity of mechanical loading to

which the skeleton is exposed during daily activities

and the mass and strength of bones (Lanyon, 1990).

Large heavy individuals who are physically active

tend to have denser and stronger bones than frail

sedentary individuals (Carter et al. 1987). Skeletal

morphology interacts with physical activity to gen-

erate a certain type and range of strain in the

locomotor system (Rubin & Lanyon, 1982; Rubin,

1984; Rubin et al. 1990). Two main kinds of

adaptation for bone morphology are possible : either

heavy animals possess larger bones, or heavy animals

possess stronger bones. As the strength of bone

decreases in an exponential way as porosity increases

(Currey, 1988), it is reasonable to expect that

cancellous bone, of which the volume fraction of

solids is less than 70%, is less strong than cortical

bone. Light horses and ponies possess more cancellous

bone and less cortical bone, which could thus be

related to their smaller body weights and, for the light

pony, also probably to a lesser level of physical

activity. On the other hand, the opposite situation

exists for draft horses and heavy ponies whose

skeleton is submitted to greater loads in relation to

their larger body weights. Heavy horses and ponies

thus seem to possess larger and stronger navicular

bones than light animals.

Cortical bone porosity. Other compositional factors

of bone strength such as cortical bone porosity were

different for light and heavy horses. Porosity may be

defined as the fraction of a bone volume occupied by

voids filled with soft tissues (cavities, including blood

channels such as haversian canals, and erosion

cavities). Bone strength decreases in an exponential

fashion as porosity increases (Currey, 1988; Riggs &

Evans, 1990). Young’s modulus of bone is strongly

dependent on the mineral content of the bone material

(Currey, 1988). The mineral content of bone tissue is,

other things being equal, inversely proportional to

porosity. Bone stiffness rapidly falls with small

changes in porosity when the material is mostly solid

(compact bone). Thus heavy horses and ponies possess

more stiff cortical bone than lighter animals.

Mineralised cartilage and mineralised parts of

ligaments. The mineralised parts of articular and

flexor surface cartilage were larger for heavy horses

and ponies. Mu$ ller-Gerbl et al. (1987) had established

that the thickness of the calcified layer of articular

cartilage corresponds closely to that of the total

cartilage. The value of the calcified layer expressed as

a percentage of the total cartilage volume varied in

human femoral heads from 3±72 to 8±8%. In horses,

Yousfi et al. (1997) observed higher values (20%) for

the talus. In humans, the volume of the calcified zone

is constant for all joints of a single individual and

depends upon mechanical factors. As we did not study

the full cartilage or fibrocartilage volume, we are not

able to relate the mineralised part to total volume, but

it can be speculated that the situation is no different

for horses than for man. Thus the larger amounts of


mineralised cartilage could be related to increased

mechanical load. On the other hand, as mineralised

cartilage exhibits a larger mineral density than cortical

bone, and reduced mineralisation is considered to

make bones weaker and more compliant, increased

amounts of mineralised cartilage and fibrocartilage

could also increase bone stiffness.

The mineralised part of the distal impar ligament

was larger for heavy horses and ponies, whereas the

mineralised part of the collateral ligament varied

differently in horses and ponies, being smallest for

draft horses and light ponies. The role of collateral

sesamoidean ligaments is to maintain the position of

the navicular bone relative to the middle phalanx and

to assist the extensor branches of the suspensory

ligament in resisting flexion at the proximal inter-

phalangeal joint. The navicular ligaments are tensed

in normal horses as the hoof breaks over at the end of

the stance phase, and because of positional changes of

the phalanges that occur during weightbearing. These

ligaments are also under excessive tension in horses

with a conformation where the wall-pastern axis of

the hoof is broken back or when the horse has a

low or underrun heel (Leach, 1993). These types of

conformation create a long-standing tension on the

ligaments. The importance of the mineralised part of

the ligaments could be related to the strain

encountered by the ligament and thus to hoof

conformation. Light ponies and draft horses possess a

peculiar hoof conformation, with a high ratio between

heel height and toe height (Gabriel et al. 1997a) that

could reduce the strain without the collateral

ligaments. This could explain the fact that the

mineralised part is less developed. The distal impar

ligament firmly anchors the distal navicular bone to

the distal phalanx (Ratzlaff & White, 1989). The

importance of its mineralised part could be related to

the size of the ligament, its bone attachment zone and

the strain to which it is submitted.

Flexor surface cortex. Flexor surface cortex tended

to be more developed in light horses and ponies

whereas it was the opposite for the articular surface

cortex. The external zone of the flexor cortex of the

navicular bone is more developed in light ponies and

heavy horses. The internal zone of the flexor surface is

particularly well developed for light horses. Heavy

horses thus show a larger amount of external zone but

less internal zone whereas it is the opposite for light

horses. The internal zone is more developed laterally

and medially and is relatively thin at the level of the

distal sagittal ridge whereas the external zone is

especially well developed at the level of the distal

sagittal ridge but its thickness diminishes medially and

laterally. To our knowledge, the existence of external

and internal zones of the flexor cortex has not been

reported in the literature before this study. We believe

that the flexor cortex develops in response to the

tension induced in the bone by the stretching of the

ligaments during activity. Berry et al. (1992) have also

postulated that the principal stress or strain are

directed in a proximodistal direction within the

navicular bone. Haversian canals of the internal zone

seem well adapted to resist these tensile strengths.

Heavy horses and light ponies tend to have the

same hoof conformation: a high ratio between heel

and toe height, which is the opposite for the Fjord

type and light horses (Gabriel et al. 1997a). This

conformation could diminish the tension within the

collateral sesamoidean ligaments and could thus

partly justify the fact that the internal zone is less

developed. It can be speculated that the technique of

treatment for navicular disease that consists in a

desmotomy of the navicular collateral ligaments

(Wright, 1993) could be a very effective means of

diminishing and normalising the strain within the

ligaments and the bone. Another speculation consists

in considering flexor cortex architecture in relation to

haversian remodelling. Remodelling could be less

important for light ponies and heavy horses as they

possess a larger amount of poorly remodelled flexor

cortex external zone but a smaller amount of internal

zone, which is mainly composed of secondary bone.

The reduced level of haversian remodelling could also

be related to a lesser level of functional strain within

the cortex in relation to physical activity : light ponies

are mainly used for juvenile riding or pleasure and

draft horses are currently less used for agricultural

works but instead are bred for pleasure. Different

purposes are proposed for remodelling: (1) a homeo-

static role, with quick release of significant quantities

of calcium, (2) a mechanism for repair of micro-

damage, (3) replacement of dead osteocytes, and (4)

an adaptation of bone to mechanical loading to

achieve better material properties. But haversian

remodelling weakens bone structure, causing primary

lamellar bone to have a larger tensile strength than

osteonal bone (Martin & Ishida, 1989). Thus draft

horses and light ponies possess thicker and stronger

flexor surface cortical bone and this finding could

partly explain their lower susceptibility to navicular

disease.

Cancellous bone. The amount of cancellous bone

and marrow spaces in the navicular bone volume was

more important for light horses and ponies, as well as

trabeculae specific surface. Heavy horses and ponies

possess larger amounts of trabeculae in cancellous


Fig. 10. Architecture of the navicular bone for type 1 and 2 halfbreds.

bone and in the navicular bone, and thus also possess

larger trabecular bone surface and volume. Cancellous

bone is found where the bone is loaded almost wholly

in compression. It provides effective, broad and

homogeneous support for transfer of compression

loads from one bone to another. Cancellous bone

increases flexibility and damping of a bone under load

(Frost, 1964). The symmetry of the structure in

cancellous bone depends on the direction of the

applied loads. If the stress pattern in cancellous bone

is complex, then the structure of the network of

trabeculae is also complex and highly asymmetric

(Mosekilde et al. 1987; Jensen et al. 1990; Goldstein

et al. 1991), but in bones where the loading is largely

uniaxial, as in the navicular bone, the trabeculae often

develop a columnar structure with cylindrical sym-

metry (Whitehouse et al. 1971; Gibson, 1985). Within

the navicular bone, the trabeculae are oriented in a

dorsoproximal}palmodistal direction. Trabeculae are

thus mainly adapted to resist compression exerted by

the deep digital flexor tendon and compression exerted

by the middle phalanx that transmits a portion of the

weight to the navicular bone during weight bearing.

There was no obvious difference for cancellous bone

architecture between light and heavy horses though

trabeculae seemed to be more transversely connected

in heavy horses and ponies. In cancellous bone, the

relative numbers and sizes of trabeculae, as well as

their orientation and spacing, influence the elastic

modulus: thus the stiffness of cancellous bone depends

both on its porosity and its trabecular orientations.

The fact that porosity was more important for light

horses and ponies, cancellous bone, with a tendency

for fewer transverse connections between trabeculae

and thinner trabeculae (larger trabecular specific

surface), can once more be related to the mechanical

load encountered by the bone.

Differences between type 1 (sedentary) and type 2

(athletic) halfbred

Bone architecture and cortical bone mass. Navicular

bones from athletic halfbreds showed larger amounts

of cortical bone (articular and flexor surfaces, distal

and proximal borders), but less cancellous bone

(trabeculae and marrow spaces) than sedentary half-

breds (Fig. 10).

Exercise has been shown in a number of studies to

increase the average mass, cortical thickness and

structural strength of bone (Schryver, 1978; Millis,

1983; Frost, 1987; Jeffcott et al. 1987, 1988;

McCarthy & Jeffcott, 1988; Raub et al., 1989;

Buckingham & Jeffcott, 1990). Increased mechanical

strain stimulates growth and modelling and depresses

bone resorption.

In our study, an increased level of physical activity

in a population of sound horses increased the

percentage of cortical bone but diminished medullary

bone volume. Woo et al. (1981) have also observed a

decrease of medullary area in swine femora after 1 y of

moderately intense training. But in their study, as well

as that performed by Matsuda et al. (1986) on rooster

tarsometatarsal bones, bone apposition mainly oc-

curred on longitudinally compressed concave bone


surfaces. In our study, thickening was observed at the

level of the distal and proximal borders, which are

mainly loaded in longitudinal compression, but also

at the level of the flexor cortex which is not loaded in

longitudinal compression. Pool et al. (1989) have

observed an increase in flexor cortex thickness for

athletic horses, which was more radiodense, and have

attributed this phenomenon to increased cortical bone

loading during racing and to degenerative disease of

the fibrocartilage with a decreased capacity of the

cartilage matrix to diffuse forces transmitted to the

subchondral bone. In our study, cortical thickening

induced by training was also apparent in the articular

cortex and occurred in the flexor cortex without

degenerative disease of the fibrocartilage. Therefore

flexor cortex thickening could be considered as a

response to increased tension in the ligaments that

involves adaptive remodelling of the cortex in re-

sponse to the functional strain.

Reduced articular and flexor cortical bone porosity

was observed for the navicular bones of athletic

horses. Exercise is well known to induce extensive

modelling with large amount of subperiosteal bone

formation and a trend towards reduced resorption

(Chen et al. 1994). McCarthy & Jeffcott (1992) have

studied the effects of exercise and relative inactivity on

cortical bone in young growing horses and have

observed marked decreases in cortical porosity in the

3rd metacarpal bone of exercised horses whereas bone

mineral content and cortical bone stiffness were

increased. As there is not much surface covered by

periosteum in the navicular bone, subperiosteal bone

formation does not seem to be implicated but reduced

endosteal bone resorption and endosteal bone for-

mation are certainly more important and leads to a

reduction in cancellous bone volume.

Cancellous bone. There is a paucity of information

concerning cancellous bone remodelling in horses

(Savage et al. 1991). Cancellous bone volume, es-

pecially marrow spaces, was reduced for the athletic

horses, but the amount of trabeculae and their specific

surface were larger, which could be related to a larger

number of trabeculae, with more transverse con-

nections between them. Yeh et al. (1993) have studied

the influence of exercise on cancellous bone of the

aged female rat and have observed reduced bone

resorption after 9 wk of training without effects on

bone formation, whereas after 16 wk of exercise there

was bone formation. Increased bone formation and

suppressed resorption could also account for the effect

of exercise on cancellous bone in the navicular. As

cancellous bone plays an important role in shock

absorbing and transfer of compression loads (Frost,

1964), a reduction in cancellous bone volume,

associated with the reduction in bone dimensions

could imply an unsuitable adaptation for the bone

when it is subjected to high compressive loads from

the deep digital flexor tendon.

The authors wish to thank Professor Simar Leon for

his continued support and interest in this work,

Professor Didier Serteyn for his scientific contri-

bution, Prevost Cecile for her invaluable help and Dr

A. Ruttens, General Inspector at the slaughter house

at Charleroi, for his help in providing distal horse

limbs. The authors are indebted to Ledoux Freddy

and Weyckmans Bruno for their dedicated laboratory

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