Journal of Orthopaedic Research 8604-611 Raven Press, Ltd., New York 0 1990 Orthopaedic Research Society
Fatigue Fractures in Thoroughbred Racehorses: Relationships with Age, Peak Bone Strain, and Training D. M. Nunamaker, D. M. Butterweck, and M. T. Provost Comparative Orthopaedic Research Laboratory, University of Pennsylvania School of Veterinary Medicine, Kennett Square, Pennsylvania, U.S.A.
Summary: The North American Thoroughbred racehorse was chosen as a model to study the pathogenesis of fatigue failure of bone. This species has a high incidence of spontaneous fatigue failure of bone (bucked shins) during its early training. In vivo strain gauge studies of the third metacarpal bone of four young racehorses running at racing speeds showed high principal compressive strains [-4,841 f 572 (SD) microstrain] while two older horses had lower principal compressive strains ( - 3,317 microstrain measured at racing speed, - 3,250 microstrain extrapolated from a slower speed run). Previously reported inertial property measurements of the third metacarpal bone were related to the difference in bone strains seen in young and older horses. The high strains on the surface of the third metacarpal bone associated with young horses in training may lead to high strain, low cycle fatigue. The changing shape of the third metacarpal bone during maturation may be consistent with the lower strains recorded during high speed exercise in the older animals. This phenomenon may allow for the accumulation of additional strain cycles in older animals before failure occurs. Key Words: Thoroughbred racehorsesFatigue fractures-Third metacarpal.
The problem of spontaneous or fatigue fracture of cortical bone has a long clinical history. Meyerding and Pollock (28) in their review stated that Breithupt (2) first reported this condition in 1855. More recently, this fracture has come to be known as a “march” fracture due to its relatively high incidence in bones of the lower limbs of military recruits during initial (basic) training (26). This type of fracture is also seen frequently in athletes, especially runners (9,18,19,27,40). Fatigue fractures occur when the use of implants changes the functional use of the body part (42) and when drugs are used
that inhibit bone remodeling (12,13,21,25) and in response to injury (38). Fatigue fractures all have the following characteristics: (a) They are not associated with a single event or overt trauma (5). (b) They are associated with activities that produce repetitive loading of the involved bone (8). (c) They are frequently preceded by signs of impending fracture in the form of swelling and point tenderness without radiographic evidence of fracture (8,34,40). (d) Radiographic signs when they are seen may show evidence of a fracture line or may be just associated with callus formation (43). (e) The fractures, when they do occur, display blunt, brittle fracture planes, remarkably reminiscent of fatigue failure in engineering materials (1 1). It is the combination of points (b) and (e) above
Received July 1 1 , 1987; accepted December 28, 1989. Address correspondence and reprint requests to Dr. D. M. Nunamaker at New Bolton Center, 382 West Street Road, Kennett Square, PA 19348, U.S.A.
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FRACTURES IN RACEHORSES that has led to the overall characterization of these bony injuries as fatigue fractures. In vitro testing of fatigue in bone is well documented (3-8,22) and has been reported in the horse (31). To study fatigue fractures, it would be helpful to have an animal model that conforms to the above criteria. Additionally, it would be nice to use an in vivo model in which one could manipulate the stress and cyclic history to study their effects (44). The goal of the studies reported here was to explore further the mechanistic etiology of fatigue failure in cortical bone, using the racehorse as an experimental subject. FATIGUE FRACTURE ANIMAL MODEL The modern North American thoroughbred racehorse was used in this study. Fatigue fractures of the third metacarpal bone have a reported incidence of 70% in young Thoroughbred racehorses (29). The condition may occur bilaterally and is referred to as “bucked shins” in the racing industry. This condition occurs during the first year of training (usually the 2-year-old year) but will occur in older horses if the introduction of training is delayed beyond this time (30). It is of interest to note that this type of injury is not seen in older horses that have raced successfully and, once the condition is diagnosed and the animal successfully recovers, rarely recurs. Clinically, the condition is diagnosed by palpation, revealing heat, pain, and swelling over the dorsal surface of the third metacarpal bone. Radiographic diagnosis may be delayed but is evidenced by periosteal new bone formation over the dorsal or dorsomedial aspect of this bone (29). Some animals that “buck their shins” will develop a radiographically visible stress fracture on the dorsolateral surface of the third metacarpal bone up to 1 year after the original injury. Clinically, this injury is seen as a fracture line first with periosteal callus formation during the healing phase. The relationship of these two separate injuries to each other has been discussed elsewhere (29,30). Bucked shins are very uncommon in young Standardbred racehorses (29). Since these animals race at a slower speed than the Thoroughbred (48 vs. 64 k d h ) and in a different gait (trot or pace vs. gallop), the strains on the third metacarpal bone would be expected to be less in the standardbred than in the Thoroughbred.
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MATERIALS AND METHODS In Vivo Bone Strain
Rosette strain gauges (Micro Measurements CEA-13-125UR-350, Measurements Group, Raleigh, NC, U.S.A.) were bonded (isobutal cyanoacrylate, 3M Company, Animal Care Products, St. Paul, MN, U.S.A.) to the middorsolateral surface of the left and/or right third metacarpal bone between the lateral and common digital extensor tendons of five Thoroughbred racehorses after appropriate waterproofing (3 145RTV silicone rubber, Measurements Group Inc.). The rosette strain gauges were placed so that gauge 3 was aligned with the long axis of the bone, gauge 2 was applied at a 45” angle, and gauge 1 was orientated transversely. The site of gauge placement was chosen to coincide with the region affected by bone fatigue (Fig. 1). The gauges were applied with the horse under general anesthesia in lateral recumbancy. A 3 cm incision was made between the common and lateral digital extensor tendons and the skin was retracted. The periosteum was incised and elevated from the bone. Hemostasis was provided with electric cautery and the surface of the bone was degreased with ether before gauge placement. The lead wires from the strain gauges were placed under the lateral extensor tendon and exited the skin laterally and proximally by a separate incision. The skin was closed in a routine manner. Bandaging of the leg was accomplished and the animal was recovered from anesthesia. All animals used in this portion of the study were in training and all but one had raced prior to placement of the strain gauges. The wires from the strain gauges were exteriorized above the attachment of the gauge to the bone and were connected to a full bridge signal conditioner designed and built by one of us (D.M.B.). Output was recorded with a tape recorder (TEAC R71, TEAC Corporation, Montebello, CA, U.S.A.) that the jockey carried in a backpack. The combination carried by the jockey weighed 27 pounds, Bridge excitation was set at 5 V. The bridge amplifiers were balanced and shunt calibration determined the performance of the circuit while the animal’s leg was held off the ground, holding the leg by the radius, the bone above the area gauged. Data were collected within the first 3 days following surgery. All horses were sound at the time of their exercise session. Phenylbutazone (Butazolidin
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R -
C-
MC3
distance markers. One channel of the tape was used €or a voice overlay that the jockey used during the workout to assure gait patterns with the bone strain measurements. Strain determinations were made of each horse continuously throughout the workout. The track conditions varied considerably from horse to horse as did the performance times. All horses were urged to their maximum effort during the workout. Strains reported in this study were for their maximum effort. The recorded strains from the rosette gauges were resolved where possible using Mohr circle analysis to give maximal and minimal principal directions and strains. The principal strain directions were based on the long axis of the bone, i.e., gauge #3. No horse was included in this study if gauge #3 was not working. In Vivo Fatigue Studies
FIG. 1. The anatomical drawing of the bony anatomy of the horse’s distal limb shows R = radius, C = carpus, MC3 = third metacarpal bone, MC4 = fourth metacarpal bone, S = proximal sesamoid bone. The three phalangeal bones are shown distally. The strain gauge was placed directly on the bone where indicated by MC3.
Injectable, 20%, Jensen-Salasbery Laboratories, Kansas City, MO, U.S.A.). 2 mg/kg was used to assure comfort. Four 2-year-old horses that had been in training for approximately 6 months and a veteran 12-year-old Thoroughbred racehorse that had raced more than 40 times were used in this study. The horses were exercised in a counterclockwise direction on the dirt racecourse. The animals were warmed up to speed (approximately 0.75 mile) and clocked for 0.25 mile at full effort. Comparisons were made to a 4-year-old horse that had been strain-gauged previously (30). All data were recorded on the dirt racecourse at Delaware Park (Stanton, DE, U.S.A.). All animals were exercised at work, i.e., their racing speed. Speed was monitered with a stopwatch using the furlong poles as
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Six 2-year-old Thoroughbred racehorses in training had their records reviewed following the diagnosis of fatigue fractures of their third metacarpal bone. These records documented the distances, gait, and speed that the animals trained. By analyzing mileage and speed-gait, a monthly determination of the number of cycles incurred during training was made for each horse. The total number of cycles that occurred during training was recorded. Gait cycles at a walk and trot were not included in the totals. To determine the number of cycles involved in this training period, six 3-year-old Thoroughbred racehorses of varying size were exercised at a canter, gallop, and at work (racing speed) to determine the length of stride in each of the three gaits. These stride lengths were divided into 1 mile to determine the number of gait cycles/mile. The stride lengths were then divided into the distances trained by each horse in each gait that developed these fatigue fractures to determine the approximate number of cycles the animals experienced during training before the clinical signs became evident. RESULTS In Vivo Bone Strain
In vivo bone strains were measured in four 2year-old Thoroughbred racehorses. All horses ap-
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peared sound, without noticeable lameness, at the time of the trial. Individual speeds varied according to the ability of the horse and the condition of the track surface. Times ranged from 22 s for a talented horse on a fast trace (horse 1) to a low of 34 s for a talented horse on a sloppy (submerged) track during a downpour (horse 4). The average peak compressive strain taken from 10 consecutive gait cycles of each horse was -4,761 microstrain for horse 1, - 4,533 microstrain for horse 2, -5,670 microstrain for horse 3, and -4,400 microstrain for horse 4. All peak strain measurements taken at full effort showed the largest principal strain to be compression (Fig. 2). Horses 2 and 3 did not have all three gauges working during the fast exercise periods. The longitudinal strains from gauge #3 are reported. For comparison, horse 1 had a longitudinal strain of - 4,286 microstrain while horse 4 had a longitudinal strain of - 4,400 microstrain. Failure of some strain gauge rosettes occurred when the wires broke, were pulled off the gauge, or when the gauge became loose. Wild strain fluctuations, no strain recordings, or open circuits resulted and were easily recognized. Horse 3 developed pain and tenderness over the dorsal surface of the middiaphysis of the third metacarpal bone following his second race and prior to strain gauge placement. This finding was compatible with a diagnosis of early bucked shin. The condition was bilateral. At the time of strain gauge placement, woven bone (periosteal new bone formation) was found over the area of proposed gauge placement. This bone was scraped away with a peri-
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osteal elevator to obtain a reasonable surface on which to secure the gauge. One 12-year-old horse that was instrumented in the same manner had an average peak principal strain of - 3,317 microstrain (longitudinal microstrain = - 3,230) when running at high speed over the same surface with the track listed in good condition. A previously described 4-year-old Thoroughbred was instrumented in a similar manner except that telemetry was used to obtain the strain signals (30). This animal had previously raced and was retired because of exercise-induced pulmonary hemorrhage (33). The animal was being exercised every day and was in a pulmonary study. This animal was galloped over a grass field at a maximum rate of 9 d s . This would be equivalent to running the quarter mile in 45 s. The average peak principal strain in this horse was - 1,800 microstrain. Extrapolation of that data via regression analysis to the speeds used in this study (16 m/s) would produce similar results (-3,250 microstrain) to the 12year-old studied here (30). The principal directions of strain in the third metacarpal bone rotated -40" when the speed was increased from a trot (20 k d h ) to racing speed (60 k d h ) (Fig. 3). A change of axis of the principal strains was seen in all animals studied. In Vivo Fatigue Studies The total number of gait cycles of six 2-year-old Thoroughbred horses in race training was estimated based on the distances covered in a canter, gallop, or at work (racing speed). The majority of horses were being trained between 10,000 and 12,000 cycledmonth. The six horses were diagnosed with bucked shins between 35,284 and 53,299 total training cycles. DISCUSSION
FIG. 2. The strain tracing from a running Thoroughbred is shown with (A) gauge 3 vertical; (B) gauge 2 at 45", and (C) gauge 1 showing horizontal strain output from the rosette gauge. The rosette gauge was mounted to allow gauge 3 to approximate the anatomical longitudinal axis of the bone.
The occurrence of fatigue fractures in North American thoroughbred racehorses is common (29). This breed may thus serve as a model for further study of fatigue failure of bone (10). The fractures occur during a vigorous training program superimposed on growth and development of the individual horse. The equine third metacarpal bone has been reported to be primarily axially loaded (1,41). The in
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“LCI
=
---_
Ra x
Max
FIG. 3. The strains on the dorsal surface of the third metacarpal bone are plotted showing the principal directions of the strain in (A) a trotting 2-year old Thoroughbred (rnicrostrain: E l = - 1,039, E2 = - 1,685, E3 = 1,600, E(max) = 2,648, E(min) = -2,087. Angle of principal direction = -61.9’) and (B)in the same animal galloping (microstrain: El = 779, E2 = -3,377, E3 = -4,286, E(rnax) = 1,255, E(min) = -4,762. Angle of principal direction = -16.3”). The axis of strain gauge 3 represents the longitudinal axis of the bone.
+
vivo strains previously reported together with those of this study show that the bone is subjected to bending and torsion as well (16). Torsion would appear to play a significant role when the animal is trotting (Fig. 3). The change in principal directions of Em,, and Eminto a more longitudinal direction when the animal is running shows a decrease in this torsional strain. The magnitudes of strain recorded on the horses’ third metacarpal bone in this study are greater than those previously reported (1). Two reasons for this greater strain magnitude relate to the speed at which the animals exercised and the age of the individuals. Previous studies have used ponies rather than horses (1,36). Bucked shin injuries do not occur in ponies. Biewener’s ponies were run at 5.9 m/s while the horses reported here were running 16-17 m / s (1). Similarly, Rubin and Lanyon’s ponies ran at only 6.94 m/s while they measured the strain in the radius and tibia of their animals (36). The animals in previous studies were adult. The relationships of bone shape to induced strain were not noted in these individuals. Previously reported in vitro fatigue studies of equine third metacarpal bone showed that there was no difference in the fatigue properties between the Standardbred and Thoroughbred breeds (3 1). Al-
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though one might not expect a difference in in vivo fatigue properties, the difference in the incidence of fatigue fractures between these two breeds is remarkable. Fatigue fractures are rarely seen in Standardbreds (29). Data taken from a prior study on some geometric properties of the third metacarpal bone of Thoroughbred and Standardbred racehorses (32) were reviewed to help interpret the in vivo strain data generated in this study. This previous study examined 30 pairs of second, third, and fourth metacarpal bones of racehorses (10 standardbred and 20 thoroughbred horses). Data on the thoroughbred bones were grouped equally by age into four groups: yearlings; 2-year-olds; 3- and 4-year-olds; and “aged” (horses older than 5 years of age). The standardbred data were divided into two groups (five pairs in each group), yearlings, and “aged” horses. Comparisons were made between breeds of a particular age group and between age groups of a particular breed. Mean section properties were then plotted against percent of bone length in order to observe patterns proximal to distal for each property. The results of this previously reported study showed that age and breed were the only factors affecting section properties, i.e., there were no right-left differences. In the Thoroughbred group, all section properties were calculated to be much lower for yearlings than for any other age group. Little differences were seen in cross-sectional area between age groups 2 years and older. Changes in the second moments of area that relate to bending stiffness in a particular direction did show significant differences. The second moments related to bending in the dorsopalmar direction and the mediolateral direction were used to determine the principal moments Zmin and Zmm. All of the results indicate that the most significant changes in the bone occur at the midsections between the ages of 1 and 2 years. This is most obvious when examining the and x-directed moments of inertia. minimum (Imin) Most of the change occurs during the first 2 years while continued change occurs to age 3 or 4 years. No observable changes take place after age 4 years. When comparing the Standardbred and Thoroughbred, it can be seen that Zd,, is smaller in the yearling Thoroughbred than the yearling Standardbred but is larger in the adult Thoroughbred than in the adult Standardbred (Fig. 4); therefore, the Thoroughbred changes this property to a greater extent
FRACTURES IN RACEHORSES
4
Imin (
cm4 1 4.00
i----‘-------
i c
A ,-
I
2.50 20
30
40
50
60
70
80
% Length
FIG. 4. The minimum moment of the equine third metacarpal bones is shown comparing the Standardbred and Thoroughbred horse between the ages of 1 and 4 years. lmi, demonstrates the change in inertial properties in the dorsopalmar aspect of this bone. The percent length measures the bone from proximal to distal. Note the large change in this parameter in the Thoroughbred horse as opposed to the Standardbred horse. 0, 1 year Thoroughbreds; A,aged Thoroughbreds; . , 1 year Standardbreds; A,aged Standardbreds.
than does the Standardbred during the first 3-4 years of life. Studies involving the inertial properties of bone showing the effect of exercise in other species have been reported (20,44). The inertial property measurement changes between the two breeds of horses in this previous study may help to explain the incidence of fatigue fractures as related to the exercise each breed does during training. The inertial properties of the third metacarpal bone change dramatically between the first and fourth year of age (32). It should be noted that all thoroughbred and standardbred racehorses have their birthday on January 1 of each year. Thus, an animal born on December 20 becomes 1 year old on the first of January. This distinction is important in examining the data from this previously reported study. Some of the 2year-old animals may have already been in training for 1 year (being almost 3-year-olds) while others may only be starting training. The differences between the reported ages of 1- and 2-year-old individuals are the greatest but the training history of these individuals is incomplete. The greatest changes in inertial property measurement occur while the animal undergoes training during growth and development. The second moment of inertia
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with respect to the dorsopalmar direction (I,) that was used to determine the principle moment (Imin) increased significantly as the animal’s age increased to 3-4 years (Fig. 4). This change in geometry of the bone correlates well with the decrease in strain noted in the in vivo strain data in this study. It would appear that the bone modelshemodels in order to reduce strain to some “physiological” level (14,15,23,24,37). In this study, the strains recorded in the 2-year-old racehorses are far higher than any strains recorded for similar activities in other species (36), whereas the strains recorded for the 12year-old racehorse working at similar speeds and a previously reported 4-year-old (30) racehorse whose strain recordings were extrapolated to high speeds are similar to those recorded in other species (36). It is interesting to note that horse 3, which had clinical signs compatible with “bucked shins” had the largest measured strain magnitudes ( - 5,670 microstrain) on its metacarpal bone when running. Horse 3 was approximately six standard deviations above the average of horses 1, 2, and 4 [ -4,565 2 182.6 (SD) microstrain]. The loss in bone stiffness that is seen in in vitro fatigue tests prior to bone failure (6) could provide an explanation for this individual deviation. If the horse’s bone lost stiffness in vivo as it neared its fatigue limits, then the same stresses of running should increase the deformation (strain) on the bone. If the stiffness decrease of the bone then triggered changes in the formation of lamellar or woven bone on the surface of the third metacarpal bone, then this could explain the animal’s response to high strain cyclic fatigue. As stated above, periosteal new bone formation over the dorsal surface of the third metacarpal bone is the classical radiographical sign seen with “bucked shins. ” It is not known if this phenomenon may be at work in horse 3 or perhaps in all of the young horses. The cause-and-effect relationships between inertial property changes, induced bone strain (including magnitude, direction, and strain rate), and bone fatigue in these young developing racehorses represents an enigma that deserves further study. Although bone may not have an absolute endurance limit in vivo (39), it seems plausible that the constant remodeling activity of the bone cortex would allow for a “biological” or operative endurance limit, reflecting a balance between fatigue damage and remodeling. This remodeling would repair local damage as concurrent modeling changes the shape of the third metacarpal bone, resulting in
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a decrease in peak strain when the horse gallops. The final shape of the bone would be related to the strain that is considered to be optimal (14,15,23,37). The timing of this remodeling should allow older horses to develop lower peak strains to complete this cycle without incurring fatigue fractures. Changes in the principal strain directions up to 16“ have been reported in the tibia of the dog throughout the animal’s speed range (36). No significant changes in principal strain directions on the dorsal surface of the metacarpus were reported for the metacarpus of ponies throughout their gait cycle up to 5.9 m/s (1). The differences may be explained by the speed that the animal travels and/or the influence of having a rider on the animal’s back. Different shoeing of the individual animal might also affect the principal strains and their direction as well. The dramatic changes in the principal directions of strain reported in this study that occurred on the dorsolateral surface of the third metacarpal bone as the animal changed its gait or velocity lead to a hypothesis that may help to explain the differences in the incidence of fatigue fractures between the Thoroughbred and Standardbred racehorse. Since the bone remodels according to the strain input (14,15,35,37), the magnitude and direction of the principal strains may precisely define the modeling and remodeling process. The Standardbred trains in its racing gait over relatively long distances; thus, the bone remodels to the strains that occur while racing. The Thoroughbred, however, trains mostly at a gait that is different from (or slower than) its racing gait. The average Thoroughbred trains at racing speed only once every 7 to 10 days. While accumulation of the high strain cycles (in racing) may lead to bone modeling/remodeling, the major input may come from the lower strain cycles of daily training, which may be very different in principal direction and magnitude. Hence, the Standardbred remodels its bone for racing while the Thoroughbred remodels its bone for training. The cyclic loading of training would induce bone fatigue (loss of stiffness) over time, but the infrequent high speed work that loads the bone in a different orientation could induce the signs of high strain cyclic fatigue. Recently, a report published showed that the peak incidence of stress fractures occurred in the first week of training in a group of U.S. Marines (17). The timing of the changed exercise regime in this group would correlate with the experience in the Thoroughbred racehorse. Classically, Thorough-
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bred racehorses “buck their shins” at or about the time of high speed works or early racing. Consequently, the Thoroughbred’s metacarpal bone may not be well adapted to the high strains and strain directions that occur in racing, ultimately leaving it more vulnerable to high strain cyclic fatigue. The training histories of the animals that developed bucked shins reported in this study averaged about 10,000 cycles of galloping including fast racing speed work per month. The high speed work accounted for less than 5% of these cycles, but seems to be very important in the development of this condition. Acknowledgment: This study was supported by the United States Department of Agriculture (#5-27637), the Horsemens Benevolent and Protective Association, New York Division (#5-21054), The Beech Fund via The New York Community Trust, and the Equine Orthopedic Research Fund, Kennett Square, PA.
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in thoroughbred racehorses: relationship with age and strain. Trans Orthop Res SOC 12:72, 1987 32. Nunamaker DM, Butterweck DM, Provost MT: Some geometric properties of the third metacarpal bone: a comparison between the standardbred and thoroughbred racehorse. J Biomech 22:129-134, 1989 33. Pascoe JR, Ferraro GL, Cannon JH, Arthur RM, Wheat JD: Exercise-induced pulmonary hemorrhage in racing thoroughbreds: a preliminary survey. Am J Vet Res 42:703-707, 1981 34. Pavlov H,Torg JS, Frieberger RH: Tarsal navicular stress fracture: radiographic evaluation. Radiology 148:64145, 1983 35. Rubin CT: Skeletal strain and the functional significance of bone architecture. Calcif Tissue Znt 36 (Supp I):Sll-S18, 1984 36. Rubin CT, Lanyon LE: Limb mechanics as a function of speed and gait: a study of functional strains in the radius and tibia of horse and dog. J Exp Biol 101:187-211, 1982 37. Rubin CT, Lanyon LE: Regulation of bone mass by mechanical strain magnitude. Calcif Tissue Znt 37:411-417,1985 38. Rupani HD, Holder LE, Espinola DA, Engin SI: Threephase radionuclide bone imaging in sports medicine. Radiology 156~187-196,1985 39. Seireg A, Kempke W: Behavior of in vivo bone under cyclic loading. J Biomech 2:455-461, 1969 40. Sullivan D, Warren RF, Pavlov H, Kelman G: Stress fractures in 51 runners. Clin Orthop Ref Res 187:188-192, 1984 41. Turner AS, Mills EJ, Gabel AA: In vivo measurements of bone strain in the horse. A m J Vet Res 36:1573-1579, 1975 42. Uhthoff HK, DuBuc FL: Bone structure changes in the dog under rigid internal fixation. Clin Orthop Re1 Res 81:165170, 1971 43. Uhthotf HK,Jaworski ZFG: Periosteal stress-induced reactions resembling stress fractures. Clin Orthop Re/ Res 199: 294-291, 1985 44. Woo SLY, Kvei SC, Amiel D, Gomez MA, Hayes WC, White FC, Akeson WH: The effect of prolonged physical training on the properties of long bone: a study of Wolff s Law. J Bone Joint Surg [Am] 63:780-786, 1981
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Fatigue Fractures in Thoroughbred Racehorses: Relationships with Age, Peak Bone Strain, and Training D. M. Nunamaker, D. M. Butterweck, and M. T. Provost Comparative Orthopaedic Research Laboratory, University of Pennsylvania School of Veterinary Medicine, Kennett Square, Pennsylvania, U.S.A.
Summary: The North American Thoroughbred racehorse was chosen as a model to study the pathogenesis of fatigue failure of bone. This species has a high incidence of spontaneous fatigue failure of bone (bucked shins) during its early training. In vivo strain gauge studies of the third metacarpal bone of four young racehorses running at racing speeds showed high principal compressive strains [-4,841 f 572 (SD) microstrain] while two older horses had lower principal compressive strains ( - 3,317 microstrain measured at racing speed, - 3,250 microstrain extrapolated from a slower speed run). Previously reported inertial property measurements of the third metacarpal bone were related to the difference in bone strains seen in young and older horses. The high strains on the surface of the third metacarpal bone associated with young horses in training may lead to high strain, low cycle fatigue. The changing shape of the third metacarpal bone during maturation may be consistent with the lower strains recorded during high speed exercise in the older animals. This phenomenon may allow for the accumulation of additional strain cycles in older animals before failure occurs. Key Words: Thoroughbred racehorsesFatigue fractures-Third metacarpal.
The problem of spontaneous or fatigue fracture of cortical bone has a long clinical history. Meyerding and Pollock (28) in their review stated that Breithupt (2) first reported this condition in 1855. More recently, this fracture has come to be known as a “march” fracture due to its relatively high incidence in bones of the lower limbs of military recruits during initial (basic) training (26). This type of fracture is also seen frequently in athletes, especially runners (9,18,19,27,40). Fatigue fractures occur when the use of implants changes the functional use of the body part (42) and when drugs are used
that inhibit bone remodeling (12,13,21,25) and in response to injury (38). Fatigue fractures all have the following characteristics: (a) They are not associated with a single event or overt trauma (5). (b) They are associated with activities that produce repetitive loading of the involved bone (8). (c) They are frequently preceded by signs of impending fracture in the form of swelling and point tenderness without radiographic evidence of fracture (8,34,40). (d) Radiographic signs when they are seen may show evidence of a fracture line or may be just associated with callus formation (43). (e) The fractures, when they do occur, display blunt, brittle fracture planes, remarkably reminiscent of fatigue failure in engineering materials (1 1). It is the combination of points (b) and (e) above
Received July 1 1 , 1987; accepted December 28, 1989. Address correspondence and reprint requests to Dr. D. M. Nunamaker at New Bolton Center, 382 West Street Road, Kennett Square, PA 19348, U.S.A.
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FRACTURES IN RACEHORSES that has led to the overall characterization of these bony injuries as fatigue fractures. In vitro testing of fatigue in bone is well documented (3-8,22) and has been reported in the horse (31). To study fatigue fractures, it would be helpful to have an animal model that conforms to the above criteria. Additionally, it would be nice to use an in vivo model in which one could manipulate the stress and cyclic history to study their effects (44). The goal of the studies reported here was to explore further the mechanistic etiology of fatigue failure in cortical bone, using the racehorse as an experimental subject. FATIGUE FRACTURE ANIMAL MODEL The modern North American thoroughbred racehorse was used in this study. Fatigue fractures of the third metacarpal bone have a reported incidence of 70% in young Thoroughbred racehorses (29). The condition may occur bilaterally and is referred to as “bucked shins” in the racing industry. This condition occurs during the first year of training (usually the 2-year-old year) but will occur in older horses if the introduction of training is delayed beyond this time (30). It is of interest to note that this type of injury is not seen in older horses that have raced successfully and, once the condition is diagnosed and the animal successfully recovers, rarely recurs. Clinically, the condition is diagnosed by palpation, revealing heat, pain, and swelling over the dorsal surface of the third metacarpal bone. Radiographic diagnosis may be delayed but is evidenced by periosteal new bone formation over the dorsal or dorsomedial aspect of this bone (29). Some animals that “buck their shins” will develop a radiographically visible stress fracture on the dorsolateral surface of the third metacarpal bone up to 1 year after the original injury. Clinically, this injury is seen as a fracture line first with periosteal callus formation during the healing phase. The relationship of these two separate injuries to each other has been discussed elsewhere (29,30). Bucked shins are very uncommon in young Standardbred racehorses (29). Since these animals race at a slower speed than the Thoroughbred (48 vs. 64 k d h ) and in a different gait (trot or pace vs. gallop), the strains on the third metacarpal bone would be expected to be less in the standardbred than in the Thoroughbred.
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MATERIALS AND METHODS In Vivo Bone Strain
Rosette strain gauges (Micro Measurements CEA-13-125UR-350, Measurements Group, Raleigh, NC, U.S.A.) were bonded (isobutal cyanoacrylate, 3M Company, Animal Care Products, St. Paul, MN, U.S.A.) to the middorsolateral surface of the left and/or right third metacarpal bone between the lateral and common digital extensor tendons of five Thoroughbred racehorses after appropriate waterproofing (3 145RTV silicone rubber, Measurements Group Inc.). The rosette strain gauges were placed so that gauge 3 was aligned with the long axis of the bone, gauge 2 was applied at a 45” angle, and gauge 1 was orientated transversely. The site of gauge placement was chosen to coincide with the region affected by bone fatigue (Fig. 1). The gauges were applied with the horse under general anesthesia in lateral recumbancy. A 3 cm incision was made between the common and lateral digital extensor tendons and the skin was retracted. The periosteum was incised and elevated from the bone. Hemostasis was provided with electric cautery and the surface of the bone was degreased with ether before gauge placement. The lead wires from the strain gauges were placed under the lateral extensor tendon and exited the skin laterally and proximally by a separate incision. The skin was closed in a routine manner. Bandaging of the leg was accomplished and the animal was recovered from anesthesia. All animals used in this portion of the study were in training and all but one had raced prior to placement of the strain gauges. The wires from the strain gauges were exteriorized above the attachment of the gauge to the bone and were connected to a full bridge signal conditioner designed and built by one of us (D.M.B.). Output was recorded with a tape recorder (TEAC R71, TEAC Corporation, Montebello, CA, U.S.A.) that the jockey carried in a backpack. The combination carried by the jockey weighed 27 pounds, Bridge excitation was set at 5 V. The bridge amplifiers were balanced and shunt calibration determined the performance of the circuit while the animal’s leg was held off the ground, holding the leg by the radius, the bone above the area gauged. Data were collected within the first 3 days following surgery. All horses were sound at the time of their exercise session. Phenylbutazone (Butazolidin
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R -
C-
MC3
distance markers. One channel of the tape was used €or a voice overlay that the jockey used during the workout to assure gait patterns with the bone strain measurements. Strain determinations were made of each horse continuously throughout the workout. The track conditions varied considerably from horse to horse as did the performance times. All horses were urged to their maximum effort during the workout. Strains reported in this study were for their maximum effort. The recorded strains from the rosette gauges were resolved where possible using Mohr circle analysis to give maximal and minimal principal directions and strains. The principal strain directions were based on the long axis of the bone, i.e., gauge #3. No horse was included in this study if gauge #3 was not working. In Vivo Fatigue Studies
FIG. 1. The anatomical drawing of the bony anatomy of the horse’s distal limb shows R = radius, C = carpus, MC3 = third metacarpal bone, MC4 = fourth metacarpal bone, S = proximal sesamoid bone. The three phalangeal bones are shown distally. The strain gauge was placed directly on the bone where indicated by MC3.
Injectable, 20%, Jensen-Salasbery Laboratories, Kansas City, MO, U.S.A.). 2 mg/kg was used to assure comfort. Four 2-year-old horses that had been in training for approximately 6 months and a veteran 12-year-old Thoroughbred racehorse that had raced more than 40 times were used in this study. The horses were exercised in a counterclockwise direction on the dirt racecourse. The animals were warmed up to speed (approximately 0.75 mile) and clocked for 0.25 mile at full effort. Comparisons were made to a 4-year-old horse that had been strain-gauged previously (30). All data were recorded on the dirt racecourse at Delaware Park (Stanton, DE, U.S.A.). All animals were exercised at work, i.e., their racing speed. Speed was monitered with a stopwatch using the furlong poles as
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Six 2-year-old Thoroughbred racehorses in training had their records reviewed following the diagnosis of fatigue fractures of their third metacarpal bone. These records documented the distances, gait, and speed that the animals trained. By analyzing mileage and speed-gait, a monthly determination of the number of cycles incurred during training was made for each horse. The total number of cycles that occurred during training was recorded. Gait cycles at a walk and trot were not included in the totals. To determine the number of cycles involved in this training period, six 3-year-old Thoroughbred racehorses of varying size were exercised at a canter, gallop, and at work (racing speed) to determine the length of stride in each of the three gaits. These stride lengths were divided into 1 mile to determine the number of gait cycles/mile. The stride lengths were then divided into the distances trained by each horse in each gait that developed these fatigue fractures to determine the approximate number of cycles the animals experienced during training before the clinical signs became evident. RESULTS In Vivo Bone Strain
In vivo bone strains were measured in four 2year-old Thoroughbred racehorses. All horses ap-
FRACTURES IN RACEHORSES
peared sound, without noticeable lameness, at the time of the trial. Individual speeds varied according to the ability of the horse and the condition of the track surface. Times ranged from 22 s for a talented horse on a fast trace (horse 1) to a low of 34 s for a talented horse on a sloppy (submerged) track during a downpour (horse 4). The average peak compressive strain taken from 10 consecutive gait cycles of each horse was -4,761 microstrain for horse 1, - 4,533 microstrain for horse 2, -5,670 microstrain for horse 3, and -4,400 microstrain for horse 4. All peak strain measurements taken at full effort showed the largest principal strain to be compression (Fig. 2). Horses 2 and 3 did not have all three gauges working during the fast exercise periods. The longitudinal strains from gauge #3 are reported. For comparison, horse 1 had a longitudinal strain of - 4,286 microstrain while horse 4 had a longitudinal strain of - 4,400 microstrain. Failure of some strain gauge rosettes occurred when the wires broke, were pulled off the gauge, or when the gauge became loose. Wild strain fluctuations, no strain recordings, or open circuits resulted and were easily recognized. Horse 3 developed pain and tenderness over the dorsal surface of the middiaphysis of the third metacarpal bone following his second race and prior to strain gauge placement. This finding was compatible with a diagnosis of early bucked shin. The condition was bilateral. At the time of strain gauge placement, woven bone (periosteal new bone formation) was found over the area of proposed gauge placement. This bone was scraped away with a peri-
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osteal elevator to obtain a reasonable surface on which to secure the gauge. One 12-year-old horse that was instrumented in the same manner had an average peak principal strain of - 3,317 microstrain (longitudinal microstrain = - 3,230) when running at high speed over the same surface with the track listed in good condition. A previously described 4-year-old Thoroughbred was instrumented in a similar manner except that telemetry was used to obtain the strain signals (30). This animal had previously raced and was retired because of exercise-induced pulmonary hemorrhage (33). The animal was being exercised every day and was in a pulmonary study. This animal was galloped over a grass field at a maximum rate of 9 d s . This would be equivalent to running the quarter mile in 45 s. The average peak principal strain in this horse was - 1,800 microstrain. Extrapolation of that data via regression analysis to the speeds used in this study (16 m/s) would produce similar results (-3,250 microstrain) to the 12year-old studied here (30). The principal directions of strain in the third metacarpal bone rotated -40" when the speed was increased from a trot (20 k d h ) to racing speed (60 k d h ) (Fig. 3). A change of axis of the principal strains was seen in all animals studied. In Vivo Fatigue Studies The total number of gait cycles of six 2-year-old Thoroughbred horses in race training was estimated based on the distances covered in a canter, gallop, or at work (racing speed). The majority of horses were being trained between 10,000 and 12,000 cycledmonth. The six horses were diagnosed with bucked shins between 35,284 and 53,299 total training cycles. DISCUSSION
FIG. 2. The strain tracing from a running Thoroughbred is shown with (A) gauge 3 vertical; (B) gauge 2 at 45", and (C) gauge 1 showing horizontal strain output from the rosette gauge. The rosette gauge was mounted to allow gauge 3 to approximate the anatomical longitudinal axis of the bone.
The occurrence of fatigue fractures in North American thoroughbred racehorses is common (29). This breed may thus serve as a model for further study of fatigue failure of bone (10). The fractures occur during a vigorous training program superimposed on growth and development of the individual horse. The equine third metacarpal bone has been reported to be primarily axially loaded (1,41). The in
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“LCI
=
---_
Ra x
Max
FIG. 3. The strains on the dorsal surface of the third metacarpal bone are plotted showing the principal directions of the strain in (A) a trotting 2-year old Thoroughbred (rnicrostrain: E l = - 1,039, E2 = - 1,685, E3 = 1,600, E(max) = 2,648, E(min) = -2,087. Angle of principal direction = -61.9’) and (B)in the same animal galloping (microstrain: El = 779, E2 = -3,377, E3 = -4,286, E(rnax) = 1,255, E(min) = -4,762. Angle of principal direction = -16.3”). The axis of strain gauge 3 represents the longitudinal axis of the bone.
+
vivo strains previously reported together with those of this study show that the bone is subjected to bending and torsion as well (16). Torsion would appear to play a significant role when the animal is trotting (Fig. 3). The change in principal directions of Em,, and Eminto a more longitudinal direction when the animal is running shows a decrease in this torsional strain. The magnitudes of strain recorded on the horses’ third metacarpal bone in this study are greater than those previously reported (1). Two reasons for this greater strain magnitude relate to the speed at which the animals exercised and the age of the individuals. Previous studies have used ponies rather than horses (1,36). Bucked shin injuries do not occur in ponies. Biewener’s ponies were run at 5.9 m/s while the horses reported here were running 16-17 m / s (1). Similarly, Rubin and Lanyon’s ponies ran at only 6.94 m/s while they measured the strain in the radius and tibia of their animals (36). The animals in previous studies were adult. The relationships of bone shape to induced strain were not noted in these individuals. Previously reported in vitro fatigue studies of equine third metacarpal bone showed that there was no difference in the fatigue properties between the Standardbred and Thoroughbred breeds (3 1). Al-
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though one might not expect a difference in in vivo fatigue properties, the difference in the incidence of fatigue fractures between these two breeds is remarkable. Fatigue fractures are rarely seen in Standardbreds (29). Data taken from a prior study on some geometric properties of the third metacarpal bone of Thoroughbred and Standardbred racehorses (32) were reviewed to help interpret the in vivo strain data generated in this study. This previous study examined 30 pairs of second, third, and fourth metacarpal bones of racehorses (10 standardbred and 20 thoroughbred horses). Data on the thoroughbred bones were grouped equally by age into four groups: yearlings; 2-year-olds; 3- and 4-year-olds; and “aged” (horses older than 5 years of age). The standardbred data were divided into two groups (five pairs in each group), yearlings, and “aged” horses. Comparisons were made between breeds of a particular age group and between age groups of a particular breed. Mean section properties were then plotted against percent of bone length in order to observe patterns proximal to distal for each property. The results of this previously reported study showed that age and breed were the only factors affecting section properties, i.e., there were no right-left differences. In the Thoroughbred group, all section properties were calculated to be much lower for yearlings than for any other age group. Little differences were seen in cross-sectional area between age groups 2 years and older. Changes in the second moments of area that relate to bending stiffness in a particular direction did show significant differences. The second moments related to bending in the dorsopalmar direction and the mediolateral direction were used to determine the principal moments Zmin and Zmm. All of the results indicate that the most significant changes in the bone occur at the midsections between the ages of 1 and 2 years. This is most obvious when examining the and x-directed moments of inertia. minimum (Imin) Most of the change occurs during the first 2 years while continued change occurs to age 3 or 4 years. No observable changes take place after age 4 years. When comparing the Standardbred and Thoroughbred, it can be seen that Zd,, is smaller in the yearling Thoroughbred than the yearling Standardbred but is larger in the adult Thoroughbred than in the adult Standardbred (Fig. 4); therefore, the Thoroughbred changes this property to a greater extent
FRACTURES IN RACEHORSES
4
Imin (
cm4 1 4.00
i----‘-------
i c
A ,-
I
2.50 20
30
40
50
60
70
80
% Length
FIG. 4. The minimum moment of the equine third metacarpal bones is shown comparing the Standardbred and Thoroughbred horse between the ages of 1 and 4 years. lmi, demonstrates the change in inertial properties in the dorsopalmar aspect of this bone. The percent length measures the bone from proximal to distal. Note the large change in this parameter in the Thoroughbred horse as opposed to the Standardbred horse. 0, 1 year Thoroughbreds; A,aged Thoroughbreds; . , 1 year Standardbreds; A,aged Standardbreds.
than does the Standardbred during the first 3-4 years of life. Studies involving the inertial properties of bone showing the effect of exercise in other species have been reported (20,44). The inertial property measurement changes between the two breeds of horses in this previous study may help to explain the incidence of fatigue fractures as related to the exercise each breed does during training. The inertial properties of the third metacarpal bone change dramatically between the first and fourth year of age (32). It should be noted that all thoroughbred and standardbred racehorses have their birthday on January 1 of each year. Thus, an animal born on December 20 becomes 1 year old on the first of January. This distinction is important in examining the data from this previously reported study. Some of the 2year-old animals may have already been in training for 1 year (being almost 3-year-olds) while others may only be starting training. The differences between the reported ages of 1- and 2-year-old individuals are the greatest but the training history of these individuals is incomplete. The greatest changes in inertial property measurement occur while the animal undergoes training during growth and development. The second moment of inertia
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with respect to the dorsopalmar direction (I,) that was used to determine the principle moment (Imin) increased significantly as the animal’s age increased to 3-4 years (Fig. 4). This change in geometry of the bone correlates well with the decrease in strain noted in the in vivo strain data in this study. It would appear that the bone modelshemodels in order to reduce strain to some “physiological” level (14,15,23,24,37). In this study, the strains recorded in the 2-year-old racehorses are far higher than any strains recorded for similar activities in other species (36), whereas the strains recorded for the 12year-old racehorse working at similar speeds and a previously reported 4-year-old (30) racehorse whose strain recordings were extrapolated to high speeds are similar to those recorded in other species (36). It is interesting to note that horse 3, which had clinical signs compatible with “bucked shins” had the largest measured strain magnitudes ( - 5,670 microstrain) on its metacarpal bone when running. Horse 3 was approximately six standard deviations above the average of horses 1, 2, and 4 [ -4,565 2 182.6 (SD) microstrain]. The loss in bone stiffness that is seen in in vitro fatigue tests prior to bone failure (6) could provide an explanation for this individual deviation. If the horse’s bone lost stiffness in vivo as it neared its fatigue limits, then the same stresses of running should increase the deformation (strain) on the bone. If the stiffness decrease of the bone then triggered changes in the formation of lamellar or woven bone on the surface of the third metacarpal bone, then this could explain the animal’s response to high strain cyclic fatigue. As stated above, periosteal new bone formation over the dorsal surface of the third metacarpal bone is the classical radiographical sign seen with “bucked shins. ” It is not known if this phenomenon may be at work in horse 3 or perhaps in all of the young horses. The cause-and-effect relationships between inertial property changes, induced bone strain (including magnitude, direction, and strain rate), and bone fatigue in these young developing racehorses represents an enigma that deserves further study. Although bone may not have an absolute endurance limit in vivo (39), it seems plausible that the constant remodeling activity of the bone cortex would allow for a “biological” or operative endurance limit, reflecting a balance between fatigue damage and remodeling. This remodeling would repair local damage as concurrent modeling changes the shape of the third metacarpal bone, resulting in
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a decrease in peak strain when the horse gallops. The final shape of the bone would be related to the strain that is considered to be optimal (14,15,23,37). The timing of this remodeling should allow older horses to develop lower peak strains to complete this cycle without incurring fatigue fractures. Changes in the principal strain directions up to 16“ have been reported in the tibia of the dog throughout the animal’s speed range (36). No significant changes in principal strain directions on the dorsal surface of the metacarpus were reported for the metacarpus of ponies throughout their gait cycle up to 5.9 m/s (1). The differences may be explained by the speed that the animal travels and/or the influence of having a rider on the animal’s back. Different shoeing of the individual animal might also affect the principal strains and their direction as well. The dramatic changes in the principal directions of strain reported in this study that occurred on the dorsolateral surface of the third metacarpal bone as the animal changed its gait or velocity lead to a hypothesis that may help to explain the differences in the incidence of fatigue fractures between the Thoroughbred and Standardbred racehorse. Since the bone remodels according to the strain input (14,15,35,37), the magnitude and direction of the principal strains may precisely define the modeling and remodeling process. The Standardbred trains in its racing gait over relatively long distances; thus, the bone remodels to the strains that occur while racing. The Thoroughbred, however, trains mostly at a gait that is different from (or slower than) its racing gait. The average Thoroughbred trains at racing speed only once every 7 to 10 days. While accumulation of the high strain cycles (in racing) may lead to bone modeling/remodeling, the major input may come from the lower strain cycles of daily training, which may be very different in principal direction and magnitude. Hence, the Standardbred remodels its bone for racing while the Thoroughbred remodels its bone for training. The cyclic loading of training would induce bone fatigue (loss of stiffness) over time, but the infrequent high speed work that loads the bone in a different orientation could induce the signs of high strain cyclic fatigue. Recently, a report published showed that the peak incidence of stress fractures occurred in the first week of training in a group of U.S. Marines (17). The timing of the changed exercise regime in this group would correlate with the experience in the Thoroughbred racehorse. Classically, Thorough-
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bred racehorses “buck their shins” at or about the time of high speed works or early racing. Consequently, the Thoroughbred’s metacarpal bone may not be well adapted to the high strains and strain directions that occur in racing, ultimately leaving it more vulnerable to high strain cyclic fatigue. The training histories of the animals that developed bucked shins reported in this study averaged about 10,000 cycles of galloping including fast racing speed work per month. The high speed work accounted for less than 5% of these cycles, but seems to be very important in the development of this condition. Acknowledgment: This study was supported by the United States Department of Agriculture (#5-27637), the Horsemens Benevolent and Protective Association, New York Division (#5-21054), The Beech Fund via The New York Community Trust, and the Equine Orthopedic Research Fund, Kennett Square, PA.
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in thoroughbred racehorses: relationship with age and strain. Trans Orthop Res SOC 12:72, 1987 32. Nunamaker DM, Butterweck DM, Provost MT: Some geometric properties of the third metacarpal bone: a comparison between the standardbred and thoroughbred racehorse. J Biomech 22:129-134, 1989 33. Pascoe JR, Ferraro GL, Cannon JH, Arthur RM, Wheat JD: Exercise-induced pulmonary hemorrhage in racing thoroughbreds: a preliminary survey. Am J Vet Res 42:703-707, 1981 34. Pavlov H,Torg JS, Frieberger RH: Tarsal navicular stress fracture: radiographic evaluation. Radiology 148:64145, 1983 35. Rubin CT: Skeletal strain and the functional significance of bone architecture. Calcif Tissue Znt 36 (Supp I):Sll-S18, 1984 36. Rubin CT, Lanyon LE: Limb mechanics as a function of speed and gait: a study of functional strains in the radius and tibia of horse and dog. J Exp Biol 101:187-211, 1982 37. Rubin CT, Lanyon LE: Regulation of bone mass by mechanical strain magnitude. Calcif Tissue Znt 37:411-417,1985 38. Rupani HD, Holder LE, Espinola DA, Engin SI: Threephase radionuclide bone imaging in sports medicine. Radiology 156~187-196,1985 39. Seireg A, Kempke W: Behavior of in vivo bone under cyclic loading. J Biomech 2:455-461, 1969 40. Sullivan D, Warren RF, Pavlov H, Kelman G: Stress fractures in 51 runners. Clin Orthop Ref Res 187:188-192, 1984 41. Turner AS, Mills EJ, Gabel AA: In vivo measurements of bone strain in the horse. A m J Vet Res 36:1573-1579, 1975 42. Uhthoff HK, DuBuc FL: Bone structure changes in the dog under rigid internal fixation. Clin Orthop Re1 Res 81:165170, 1971 43. Uhthotf HK,Jaworski ZFG: Periosteal stress-induced reactions resembling stress fractures. Clin Orthop Re/ Res 199: 294-291, 1985 44. Woo SLY, Kvei SC, Amiel D, Gomez MA, Hayes WC, White FC, Akeson WH: The effect of prolonged physical training on the properties of long bone: a study of Wolff s Law. J Bone Joint Surg [Am] 63:780-786, 1981
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