Considerations on the pathogenesis of navicular disease

CONSIDERATIONSON THE PATHOGENESISOF NAVICULARDISEASE K. N. Thompson, PhD; J. R. Rooney, DVM; M. B. Petrites-Murphy, DVM, PhD

SUMMARY

A mechanical hypothesis for this induction of damage to the fibrocartilage of the navicular bone and the deep flexor tendon is presented. In vitro experiments were consistent with the hypothesis.

INTRODUCTION

The causes and pathogenesis of navicular disease remain an enigma despite the recent resurgence of interest in this age-old problemJ -9 This report is intended to contribute to the on-going investigation of this condition. The report is based on observations from postmortem experience, mechanical theory, and in vitro experimental investigations. Navicular disease is defined, here, as a condition in which pathological changes occur in the fibrocartilage of the navicular bone and the deep flexor tendon within the confines of the navicular bursa. Secondary changes, also, occur in the synovial membrane and the navicular bone proper.

POSTMORTEM OBSERVATIONS

Based on alarge experienceofpostmortem examination (approximately 10,000 cases) of the relevant area, often but not always including histological examinations, the following statements are believed to be true (JRR). While Authors' addresses: Maxwell H. Gluck Equine Research Center, Department of Veterinary Science. Published as paper #88-4-193 with approval of the Director, Kentucky Agricultural Experiment Station.

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I must apologize for a lack of proper epidemiological data, such data cannot be generated in retrospect, and it is hoped the reader will accept experience for what it is. 1. The palmar/plantar fibrocartilage of the navicular bone is white in the young horse, becoming slightly grayer with age. In many older horses a tannish-yellow, translucent change appears in certain areas of the cartilage, specifically the distal and proximal ridges of the palmar surface of the navicular bone, as will be discussed later. This change is characterized microscopically by fraying of the superficial surface of the fibrocartilage and eosinophilia of the cartilage itself together with depletion and cloning of chondrocytes. Mirror image changes occur in the fibrocartilaginous surface of the deep flexor tendon?3 These aging changes occur in the absence of any pathological changes in the underlying subchondral bone? 3 2. The subchondral bone in the young horse is cancellous in character and becomes denser, more bone per unit volume, with age and work. This is comparable to the increases in density which occur in other small bones, i.e., carpal and tarsal bones. 13There is no evidence to separate age and work effects. The pathological evidence is that erosive, ulcerative damage of the navicular fibrocartilage (and deep flexor surface) occurs with~and without underlying subchondral bony change. Subchondral bony change has not been seen in the absence of the fibrocartilage damage and, indeed, frank ulceration of that fibrocartilage. The process appears no different than that of the classical descriptions of arthrosis of any joint? ° Subchondral changes of focal sclerosis and "cyst" formation follow on ulceration of the overlying cartilage with presumed intrusion of synovial fluid into the underlying bone space. 3. The so-called vascular channels of the distal border of the navicular bone are, in fact, outcroppings of the coffin joint cavity, lined with synovial membrane which carries microscopic vessels to that membrane andinto the navicular bone. The shape and number of these pouches is variable EQUINE VETERINARYSCI ENCE

Table 1. The influence of toe elevation (TE) on the mean scores of lesions for the navicular bone and deep flexor tendon in Experiment 1. Rotation of fetlock, ¢ounter~ockwille

/

Rotation of hoof and P3 Gounterclockwil~

~J ,

Figure 1. Rotations of the coffin and fetlock joints with flatfoot or heal-first impact. between horses and between legs in the same horse. There is no scientific evidence that the shape or number of these pouches is correlated with the occurrence of pathological change either within the navicular bone or in the navicular fibrocartilage. 4. While it cannot be established with certainty that the aging changes described in 1 are early changes of navicular disease, that is believed to be the case. In that light, naviculardisease may be thought of as an accelerated aging process, at least in part. These aging changes are most frequent on the distal ridge of the navicular surface, followed by the proximal ridge. A number of cases of early, frank erosion of the fibrocartilage found at postmortem were in the same areas. As the erosive lesions proceed to ulceration and confluence, the process is always most severe on and between these two ridges near the center of the palmar articular surface. 6. Horses with obvious, gross lesions of navicular disease at postmortem have had clinical signs. The less severe lesions, grading down to those described as aging changes usually did not have a relevant history, or the history was equivocal or unavailable. By far the greatest majority of horses with obvious lesions were, in my experience, animals that had been used for jumping or had worked on hard surfaces for prolonged periods (carriage, police. 13) Most of these animals were over five years of

Eosinophilic Tendon TE, cm Fibrillation deposits involvement .8 a 1,1 1.1 0.0 1.25 .2a .7 .7 3.8 1.9b .5 1.7 a'bMeansin the samecolumnwith unlikesuperscriptsdiffer(P<.05).

age. An exception is made for a number of Quarter Horses which had lesions earlier if used for the types of work described. Thoroughbred and Standardbred racehorses rarely had significant lesions of the navicular area unless they had been turned to jumping or hard-road work after retirement from racing. It is of course possible, though unanswerable, that navicular disease would be more frequent in racehorses if their careers were prolonged and comparable in duration to the careers of carriage, police and jumping horses. Navicular disease is considered a significant clinical problem in horses of the warmblood type and in draft horses. There have been too few such horses in my postmortem population for any useful comment. No surveys of the postmortem incidence of disease in these horses has been found in the literature.

THEORETICAL The first hypothesis of this report is that the damage of navicular disease occurs first on the opposing articular surfaces of the navicular bone and deep flexor tendon. This is based on the observations given above and the absence of any report in the literature clearly demonstrating the primacy of subchondral bone lesions or vascular lesions in spontaneous disease. It may be noted that such putative

Rotation of fetlock, counterclockwise

(

. . . . . . . . . . . . . . . . . . .

,011'! :o:::::°

Figure 2 . Rotations of the coffin and fetlock joints with toefirst impact.

Volume 11, Number 1, 1991

Figure 3. Sagittal section of the digit showing the proximal and distal ridges of the palmar surface of the navicular bone with the valley between. 5

Table 2. The influence, of toe elevat.ion (TE) on the mean scores of lesions for the navicular bone and deep flexor tendon in Experiment 2.

6

TE, cm

Fibrillation

0.0 1.25

0.0"

Eosinophilic Tendon deposits involvement .8 ~

.3

Table 3. The influence 9 f cy,cling frequency (CF) on the mean scores of lesions Tor me navicular bone and deep flexor tendon in Experiment 2. CF, Hz .2 1.0

Fibrillation .7 a .8 a

Eosinophilic Tendon deposits involvement 1.0 1.3

.6 .5

1.P .5" .5 3.8 1.7~ 2.3b 1.1 a.bMeansin the samecolumnwith unlikesuperscriptsdiffer (P<,05).

a'"Means in the same column with unlike superscripts differ (P<.05).

primary changes have been postulated many times in the history of arthrology and have never been substantiated.~° Given that hypothesis, a second, mechanical, hypothesis was developed to describe the cause and localization of the aging changes and early erosive changes on the surface of the navicular bone. That hypothesis was, then, tested by in vitro experiments. The horse's foot usually impacts flat footed with the ground at slower speeds (walk, trot) and heel first at the faster speeds (extended trot, canter, gallop). With flat or heel first impact, the coffin joint rotates clockwise (as seen in Fig. 1), tending to decrease tension in the deep flexor tendon. Simultaneously,or nearly so, the counter-clockwise rotation of the metacarpophalangealjointcauses an increase of tension in the deep flexor tendon. The net tension in the deep flexor tendon during impact, then is a function of the out-of-phase rotations of the coffin and fetlockjoints. !fthe toe impacts first, the foot rotating toe-heel to the surface rather than heel-toe, the coffin joint rotates counterclockwise, Figure 2, as the fedock is rotating counterclockwise. The tension in the deep flexor tendon, in this case, is the sum of the tension induced by the rotations of the two joints. These differences in deep flexor tension between heel first/flatfoot and toe first impact apply as the foot is rotating into full bearing contact with the surface. The localization of early degenerative changes and

aging changes on the palmar articular surface of the navicular bone is explained as follows: There are two transverse"ridges" on the surface, a proximal ridge with a lesser elevation than the distal ridge, Figure 3, with a "valley" between. The elevations of the two ridges above the surface are greatest axially and decrease abaxially. The tensile force in the deep flexor tendon causes a normal (perpendicular) force to be exerted by the tendon on the palmar articular surface of the navicular bone. The amount of this normal force is inversely related to the curvature of the surface. ~2That is, N= T/r where T is the tensile force, N is the normal force, and r is the radius of curvature of the surface. As the radius of curvature decreases, the normal force increases for a given value of T. Therefore, the normal force is greater on the distal ridge, with a smaller radius of curvature, than on the proximal ridge. As well, the normal force is greater on the ridges than in the valleys. As noted above the ridges have a smaller radius of curvature axially, decreasing abaxially, and, so the normal force is greater axially than abaxially. Aging changes and early degenerative changes appear first on those regions of least radius of curvature. These considerations implicate increased normal force generated by the deep flexor tendon as a cause of damage to the articular surface. It is proposed that this force acts by increasing friction on the surfaces. That is, the friction at

Figure 4. Fibrillation of the superficial part of the fibrocartilage of the navicular bone. H&E. 125x.

Figure 5 . Deposition of eosinophilic debris on the surface of the fibrocartilage.

2.0

1.3b

1.3

.8

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the surfaces is primarily rolling in nature: F = mu(N/r) where F is the frictional force, mu is the coefficient of friction, N is the normal force, and r is the radius of curvature. Clearly, an increase of N acting on an area of small r, means more frictional force on that area. Thus, as the pathological experience suggests, the increase ofT, and N, in the deep flexor tendon, causes frictional damage first on the axial portion of the distal ridge, then the proximal ridge. With continuing erosion and ulceration, confluence occurs, and the major damage in the advanced case will involve the ridges and the valley between, as pathological observation show.

EXPERIMENTAL PROCEDURES Forelegs were collected from immature horses, between 6 months and one year of age, at postmortem. The legs were severed six inches above the radiocarpal joint, sealed in plastic bags and stored at -10°C. Before testing, the legs were thawed for 15 hours at 7°C. The proximal end of the leg was attached to a high strain rate servohydraulic testing machinea with the hoof resting on the machine actuator. Experiment 1. Twenty-four legs were assigned to treatments simulating toe first impact for differing trial times in a randomized block experiment. The toe was elevated by wedges to 0, 1.25 and 3.8 cm in trials of one, two and three hours duration. There were two observations per time period for the 0 and 1.25 cm treatments and four observations per time period for the 3.8 cm treatment. The legs were cycled at 0.1 Hz using a sinusoidal input. The 0 elevation legs were controls. At the conclusion of the trial, the navicular and deep flexor tendon were examined and specimens fixed in 10% buffered formalin. Three sections of the navicular and tendon were examined: axial midline and 0.64 cm abaxial to the midline, medial and lateral. The sections were strained with hematoxylin-eosin,Masson's trichrome,PASalcian blue, and safranin-O-fast green. Cartilage damage was graded on a 0 to 3 scale with 0 being no damage and 3 the maximum damage observed. The data was analyzed by variance procedures for a randomized block experiment. Experiment 2. Eighteen legs were tested at three frequencies (0.2, 1.0.2.0 Hz) and three toe elevations (0, 1.25, 3.8 cm) for one hour. A triangular waveform was substituted as input to simulate the "snapping" action of toe-first impact (JRR, personal observation). Again, the elevation was the control and the data analyzed for a randomized block experiment. alnstronCorporation,Canton,Mass.

Volume 11, Number 1, 1991

RESULTS Gross lesions were not produced in either experiment. In experiment 1 histological lesions were characterized by focal deposition of amorphous eosinophilic debris on the surface, focal increase of eosinophilia and fibrillation of the fibrocartilage. Figures 4, 5. The lesions were identical in the navicular fibrocartilage and deep flexor surface though somewhat less frequent in the latter. With the 3.8 cm toe elevation, the mean score was higher (P<.05) for cartilage fibrillation than in the controls (Table 1.) Greater values were found for eosinophilic deposits and tendon lesions, but these were not significant (P>.05). No difference (P>.05) were found among cycling times. In experiment 2 a larger number of lesions were found (Tables 1, 2, 3). In addition to the changes already described, safranin-O-fast green staining showed focal decreased staining of the fibrocartilage. In both experiments all lesions occurred in the axial midline section (P<.05) and were more frequent on the distal ridge.

DISCUSSION The experimental results and mechanical theory are consistent with pathological observations. Further, the histological changes observed are consistent with those reported in the literature.7 Obviously, such changes as cartilage cell cloning and vascular invasion of the tidemark would not be seen with in vitro preparations. The mechanisms for the increase of eosinophilia of the cartilage or the deposition of eosinophilic debris on the surface of the cartilage were not explained in this study as they have not been explained in other studies. 7 No case is made that navicular disease, per se, has been produced since this is not possible except in the live animal. What has been demonstrated is that changes in the appropilate areas and of appropriate type have been produced by increasing tension in the deep flexor tendon. One way, at least, of causing such an increase of tension is by toe-first impact, and that was simulated in these experiments. Changes simulating those of spontaneous disease have been produced in vitro, and mechanical factors need to be given due consideration in the evaluation of the pathogenesis of this condition.

REFERENCES 1. Colles CM, Hickman J: The arterial supply of the navicular 7

bone and its variation in navicular disease. Equine Vet J 9:150-154,1977. 2. Colles CM: Ischemic necrosis of the navicular bone and its treatment. Vet Rec 104:133-137,1979. 3. Fdcker OH, Riek W, Hugelshofer J: Occlusion of the digital arteries: A model for pathogenesis of navicular disease. Equine Vet J 14:203-207,1982. 4. Nemeth F: Arteriosclerosis and filariasis as possible etiological factors in the pathogenesis of sesamoiditis and navicular disease in horses. Neth J Vet Sci 5:56-71,1972. 5. Turner TA, Fessler JF: The anatomic, pathologic, and radiographic aspects of navicular disease. Corn Cont Ed Pract Vet 4:$350-$355,1982. 6. Ostblum L, Lund C, Melson F: Histological study of navicular bone disease. Equine VetJ 14:199-202,1982. 7. Svalostoga E, Reimann I, Nielson K: Changes of the fibrocartilage in navicular disease in horses. Nord Vet Med 35:372-378,1983. 8. Svalostoga E: Subchondral pressure in the navicular bone of the horse. Proceedings AAEP 29:257-263,1983. 9. Doige CE, Hoffer MA: Pathological changes in the navicular bone and associated structures of the horse. Can J Comp Med 47:387-394,1983. 10. Collins DH: The Pathology of Articular and Spinal Diseases. Williams and Wilkins, Baltimore, 1950.11. Gardner DL: General Pathology of the Peripheral Joints. In: Sokoloff L ed. The Joints and Synovial Fluid. Vol 11, Academic Press, New York, 1980. 12. Aleksandrev AD: Curves and surfaces. In: Aleksandrov AD, Kolmogorov AN, Lavrentev MA. Mathematics. Vol 11. MIT Press, Cambridge, 1963. 13. Rooney JR: Personal observations. 1960-1990.

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ERRATA

Warning: Not for use in horses intended for food.

In the paper "Navicular disease in the horse: the effect of coritrolled intrabursal corticoid injection." J.Eq. Vet. Science, 10:4, 316-320, on page 318 of the Sportsmedicine section, the following sentences were omitted: A spinal needle (88mm x 1.2mm! is introduced medially from the lateral cartilaae. Darallel to the median Diane and obliauely in the direction of the navicular bone. The position of the navicular bone is easily determined from outside. It lies in the middle of and just underneath the coronet border. Each intrabursal corticoid in!ection was preceded by an in!ection of 2 ml of positive contrasP and checked by instant and reversed fluoroscopy 1oto make sure that injection was truly intrabursal.

Dosage and Administration: The recommended dose of Adequan ® i.m. in horses is 500rag every 4 days for 28 days intramuscularly. The injection site must De thoroughly cleansed prior to injection Do not mix Adequan ~ i.m. with other drugs or solvents. Reproductive Safety: Studies have not been conducted to establish salety in breeding horses,

Caution: Federal Law restricts this drug 1o use by or on the order of a licensed veterinarian. Warning: Keep this and all medications out of the reach of children. HOW Supplied: Adequan ® i m solution. 5OOmg/SmL, is available in 5rnL glass ampules or vials, packaged in boxes of 4.

Storage Conditions: Store in a c00l place 8°-15°C (46°-59°F). Discard unused portion AHD-P1 REV. 10/89 [1] Data on file - Luitp01d Pharmaceuticals, Inc.

The authors note that the description of the injection technique is quite essential and the title of the paper can never be understood when omitted as it was. The editors apologize for this error. In the same paper, the alignment on Table 2 was not the best. We have, therefore, reprinted Table 2 below. Table

2.

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The effect of intrabursal corticoid injection (148 horses = 100%) No effect Effect-

: 19.5%

<<1 month " 14%

- 1 month and more • 66.2%

8

LUITPOLD PHARMACEUTICALS, Inc. Animal Health Division Shirley, N Y 11967 (516) 924-4000

4- 8 d a y s " 4.7% 10-14 days • 3.3% 21 days" 6.0% 1 month : 6.0% 2-12 months : 47.9% >>> 12 months : 6.7% several months : 5.4%

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