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The Journal of Bone and Joint Surgery 81:1236-44 (1999)
© 1999 The Journal of Bone and Joint Surgery, Inc.

Strains in the Metatarsals During the Stance Phase of Gait: Implications for Stress Fractures*

SETH W. DONAHUE, PH.D.{dagger} and NEIL A. SHARKEY, PH.D.{ddagger}, SACRAMENTO, CALIFORNIA

Investigation performed at Orthopaedic Research Laboratories, University of California, Davis, Sacramento


   Abstract
Top
 Abstract
Introduction
 Materials and Methods
 Results
 Discussion
 References
 
Background: Stress fractures of the metatarsals are common overuse injuries in athletes and military cadets, yet their etiology remains unclear. In vitro, high bone strains have been associated with the accumulation of microdamage and shortened fatigue life. It is therefore postulated that stress fractures in vivo are caused by elevated strains, which lead to the accumulation of excessive damage. We used a cadaver model to test the hypothesis that strains in the metatarsals increase with simulated muscle fatigue and plantar fasciotomy. Methods: A dynamic gait simulator was used to load fifteen cadaveric feet during the entire stance phase of gait under conditions simulating normal walking, walking with fatigue of the auxiliary plantar flexors, and walking after a plantar fasciotomy. Strains were measured, with use of axial strain-gauges, in the dorsal, medial, and lateral aspects of the diaphysis of the second and fifth metatarsals as well as in the proximal metaphysis of the fifth metatarsal. Results: When the feet were loaded under normal walking conditions, the mean peak strain in the dorsal aspect of the second metatarsal (-1897 microstrain) was more than twice that in the medial aspect of the fifth metatarsal (-908 microstrain). Simulated muscle fatigue significantly increased peak strain in the second metatarsal and decreased peak strain in the fifth metatarsal. Release of the plantar fascia caused significant alterations in strain in both metatarsal bones; these alterations were greater than those caused by muscle fatigue. After the plantar fasciotomy, the mean peak strain in the dorsal aspect of the second metatarsal (-3797 microstrain) was twice that under normal walking conditions. Conclusions: The peak axial strain in the diaphysis of the second metatarsal is significantly (p < 0.0001) higher than that in the diaphysis of the fifth metatarsal during normal gait. The plantar fascia and the auxiliary plantar flexors are important for maintaining normal strains in the metatarsals during gait. Clinical Relevance: Higher strains in the diaphysis of the second metatarsal may explain why stress fractures are more common in this region than they are in the fifth metatarsal. Elevated strains in the metatarsals due to muscle fatigue or loss of function of the plantar fascia may contribute to the development of metatarsalgia and stress fractures.


   Introduction
Top
 Abstract
 Introduction
Materials and Methods
 Results
 Discussion
 References
 
Stress fractures of the metatarsals are common overuse injuries in athletes and military cadets. It has been suggested that muscle fatigue contributes to the development of these fractures by increasing metatarsal bending40. Muscle fatigue in dogs has been shown to increase peak principal and shear strains in the tibia46. In a static cadaver model, one of us (N. A. S.) and colleagues37 demonstrated that reduced digital flexor force significantly (p < 0.02) increased strain in the second metatarsal and plantar-to-dorsal bending at the instant of heel-lift.

The plantar fascia is a strong mechanical linkage between the calcaneus and the toes, and it plays an integral role in maintaining the normal biomechanics of the foot18,19,42. Like stress fractures, the pathogenesis of plantar fasciitis is attributed to repetitive mechanical overload21,36. When nonoperative therapy for this condition fails, a plantar fasciotomy may be performed14,32. However, postoperative metatarsalgia3,40 and stress fractures of the metatarsals33 have been reported after this procedure. Stress fractures of the second and third metatarsals have also occurred following rupture of the plantar fascia1. These findings suggest that muscle forces and forces transmitted through the plantar fascia play important roles in maintaining normal loading of the metatarsals.

Elevated strain magnitude has been implicated in the accelerated accumulation of fatigue damage in bone and in the pathogenesis of stress fractures25,26. Substantial creep damage occurred when cortical bone specimens were cyclically loaded with an average strain value other than zero9,13. Therefore, peak and average strains are useful parameters with which to evaluate the influence of muscle fatigue and plantar fasciotomy on metatarsal loading and the potential risk of metatarsalgia and stress fractures of the metatarsals. We used a dynamic simulator of the stance phase of gait39 to study the influence of simulated muscle fatigue and plantar fasciotomy on strains in the second and fifth metatarsals at sites where fractures are common. The second metatarsal was chosen because it frequently sustains stress fractures of the diaphysis4,15,23 and may be difficult to treat if there is a delayed union or nonunion5. The fifth metatarsal was studied because it is subjected to a different mechanical loading milieu during gait40, which may explain why stress fractures are less common in the fifth metatarsal23,29,41 and why they occur more frequently in the proximal metaphysis than in the diaphysis22.


   Materials and Methods
Top
 Abstract
 Introduction
 Materials and Methods
Results
 Discussion
 References
 

Specimens
Fifteen nonpaired feet were obtained by osteotomy through the middle of the tibial and fibular shafts of fresh-frozen cadavera. The individuals had been an average of seventy-two years old (range, forty-one to eighty-six years old) at the time of death. All soft tissue proximal to the malleoli was removed except for the tendons of the ankle plantar flexors. Tibial intramedullary rods were secured with polymethylmethacrylate and transverse Steinmann pins so that the feet could be interfaced with the gait simulator. The second and fifth metatarsals were exposed through dorsal incisions, and the surrounding soft tissue was resected. The periosteum was removed from the mid-part of the metatarsal shaft with a periosteal elevator and acetone. The mid-part of the second metatarsal shaft is roughly triangular in cross section, with the sides oriented approximately in the dorsal, medial, and lateral directions. An axial strain-gauge (Measurements Group, Raleigh, North Carolina) with a gauge length of three millimeters, mounted on a five-by-ten-millimeter backing, was fastened to each of the three sides of the bone with cyanoacrylate adhesive. Three gauges were also attached to the mid-part of the fifth metatarsal shaft, which has a more oval cross section. Consistent with bone geometry, we attempted to space these gauges uniformly around the perimeter of the cross section of the mid-part of the shaft on approximately the dorsal, medial, and lateral aspects of the bone. Since stress fractures of the fifth metatarsal usually occur at the base22, an additional gauge was attached on the dorsolateral aspect of the proximal metaphysis. All gauges were protected with a latex coating, and the metatarsals were wrapped in gauze soaked in saline solution for the duration of the experiment.

Gait Simulator
The specimens were tested in a dynamic gait simulator (Fig. 1) that loaded the cadaveric foot as it would be loaded in life39. The simulator generated plantar pressures and ground-reaction force profiles similar to those seen in healthy human subjects during the entire stance phase of gait. The simulator was designed to reproduce the kinematics of the proximal end of the tibia in the sagittal plane while applying physiological loads to the tendons of the ankle plantar flexors, inducing the foot to walk across a force-plate (Advanced Mechanical Technology, Newton, Massachusetts). Gait was simulated from heel-strike to toe-off; however, technical constraints required the simulations to occur over a time-period that was twenty times longer than what occurs in life. The frame of the simulator contains guide-slots that are machined to match the kinematics of the proximal end of the tibia in the sagittal plane for walking at normal speed45. A carriage, which holds the muscle actuators, was driven along these guide-slots during the gait simulation. An aluminum shaft, which represented the tibia, connected the carriage to the tibial intramedullary rod in the foot specimen. Independent contraction of five separate muscle groups was simulated by stepper-motor-driven linear actuators attached to the plantar flexor tendons with freeze clamps38. The actuated muscle groups were the gastrocnemius-soleus complex, the tibialis posterior, the flexor hallucis longus, the flexor digitorum longus, and the peroneus longus and brevis together. Muscle load profiles were based on electromyographic data from healthy human subjects31 and cross-sectional-area data from cadavera16,44. The peak muscle loads (mean and standard deviation) were 1658 ± 359 newtons for the gastrocnemius-soleus complex, 169 ± 48 newtons for the flexor hallucis longus, 87 ± 23 newtons for the flexor digitorum longus, 150 ± 40 newtons for the tibialis posterior, and 105 ± 27 newtons for the peroneus longus and brevis. The average muscle loads were 943 ± 243 newtons for the gastrocnemius-soleus complex, 45 ± 11 newtons for the flexor hallucis longus, 34 ± 9 newtons for the flexor digitorum longus, 77 ± 20 newtons for the tibialis posterior, and 41 ± 10 newtons for the peroneus longus and brevis. Relative muscle tensions were adjusted to attain a normal vertical ground-reaction force profile45, which was scaled to the body weight of each cadaver. The peak vertical ground-reaction forces were 110 percent of body weight. The mean body weight of the individuals at the time of death was 668 ± 166 newtons, and the peak vertical ground-reaction force during gait simulation was 735 ± 155 newtons.



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  		Fig. 1 Photographs and illustrations of the dynamic gait simulator that was used to produce lifelike loading of fresh cadaveric limbs. The apparatus mimics the normal kinetics and kinematics of the tibia, ankle, and foot that occur during the stance phase of gait. The foot is placed on a pedobarograph (Baltimore Therapeutic Equipment, Hanover, Maryland) in series with a force-plate (Advanced Mechanical Technology, Newton, Massachusetts). The proximal end of the tibia is connected to an actuator carriage. Motion of the carriage in the sagittal plane is controlled by kinematic guide-plates designed to produce anatomically correct stance-phase trajectories45. The actions of the extrinsic muscles controlling the foot and ankle are based on electromyographic data31 and are simulated with force-feedback-controlled linear actuators that are interfaced to the tendons of five separate muscle groups with freeze clamps38. The behavior of the foot depends on motion of the tibia, interactions between the foot and the ground, and simulated muscle activity.

 

Simulations
Each foot was tested under five conditions: normal muscle forces (normal walking), simulated moderate fatigue of the flexor hallucis longus and flexor digitorum longus, simulated severe fatigue of the flexor hallucis longus and flexor digitorum longus, simulated severe fatigue of all muscle groups except the gastrocnemius-soleus complex (Achilles tendon only), and plantar fasciotomy with normal muscle forces. The tendon forces were reduced by 50 percent from the normal condition to simulate moderate fatigue and were eliminated to simulate severe fatigue. After the muscle-fatigue simulations, the plantar fascia was released from the calcaneus. The order of testing for the muscle-fatigue simulations was randomized; the plantar fasciotomy condition was always tested last because of the associated destruction involved.

Statistical Design
Peak and average strains (during the entire stance phase) were determined for each gauge under each simulated condition. Repeated measures analyses of variance were performed with Statview statistical software (SAS Institute, Cary, North Carolina) to individually assess the effects of simulated muscle fatigue and plantar fasciotomy on peak and average strains in the metatarsals. A significance level of 0.05 was used for all analyses of variance. Significant analyses of variance were followed up with Bonferroni-Dunn tests for multiple-means comparisons. Because the Bonferroni-Dunn test adjusts the significance level for the number of comparisons being made, post hoc comparisons of simulated muscle fatigue were not significant unless the p values were less than 0.0083. Analyses of variance were also used to verify that there were no significant differences in the peak ground-reaction forces between conditions.


   Results
Top
 Abstract
 Introduction
 Materials and Methods
 Results
Discussion
 References
 
There were no significant differences in the mediolateral (p = 0.0853), anteroposterior (p = 0.1043), or vertical (p = 0.1910) ground-reaction forces between the normal walking condition and all other conditions. All feet appeared to function normally when loaded with simulated normal muscle conditions and all levels of simulated fatigue. There was a visible lengthening of the foot and collapse of the longitudinal arch on loading after the plantar fasciotomy. There was also a one to two-centimeter gap visible in the plantar fascia at the site of the incision when the foot was fully loaded. The peak tension in the Achilles tendon that was necessary to reproduce ground-reaction forces was affected by the simulated condition. Simulated severe fatigue of all muscle groups except the gastrocnemius-soleus complex, which loaded only the Achilles tendon, required significantly (p < 0.0001) greater tension in the Achilles tendon (1717 ± 349 newtons) to reproduce ground-reaction forces compared with that required in the normal walking group (1658 ± 359 newtons). Peak tension in the Achilles tendon was significantly (p < 0.0001) reduced to 1541 ± 361 newtons after the plantar fasciotomy.

Normal Walking
The peak axial strains in the diaphyses of the second and fifth metatarsals tended to coincide with the peak tension in the Achilles tendon and the peak vertical ground-reaction force at approximately 80 percent of the stance phase (Figs. 2 and 3). When the feet were loaded under normal walking conditions, the mean peak axial strain ranged from -1897 ± 613 microstrain (which is a compressive strain) in the dorsal aspect of the second metatarsal (Fig. 4) to 802 ± 503 microstrain (which is a tensile strain) in the lateral aspect of the fifth metatarsal (Fig. 5). The mean peak axial strain in the dorsal aspect of the diaphysis of the second metatarsal (-1897 ± 613 microstrain) was significantly (p < 0.0001) higher than that in the medial aspect of the fifth metatarsal (-908 ± 503 microstrain) during normal gait.



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  		Fig. 2 Axial strain in the second metatarsal during the stance phase of the gait cycle with normal walking. * = peak strain.

 


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  		Fig. 3 Axial strain in the fifth metatarsal during the stance phase of the gait cycle with normal walking. * = peak strain.

 


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  		Fig. 4 Graph of the mean peak strain (and one standard deviation) in the second metatarsal for the fifteen specimens under each of the five conditions.* = significantly different from normal (p < 0.05).

 


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  		Fig. 5 Graph of the mean peak strain (and one standard deviation) in the fifth metatarsal for the fifteen specimens under each of the five conditions. * = significantly different from normal (p < 0.05).

 

Muscle Fatigue
Simulations of muscle fatigue tended to change the magnitude, but not the shape, of the strain curves for the second and fifth metatarsals. Severe flexor fatigue significantly increased the peak (p = 0.0002) and average (p = 0.0003) strains in the dorsal aspect of the second metatarsal and significantly decreased the peak (p = 0.0046) and average (p = 0.0008) strains in the medial aspect (Figs. 4 and 6). Loading of only the Achilles tendon significantly (p < 0.0001) increased the peak strain in the dorsal aspect of the second metatarsal.



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  		Fig. 6 Graph of the mean average strain (and one standard deviation) in the second metatarsal for the fifteen specimens under each of the five conditions. * = significantly different from normal (p < 0.05).

 
In the fifth metatarsal, all levels of simulated muscle fatigue significantly decreased the peak (p < 0.0077) and average (p < 0.0054) strains in the proximal metaphysis (Figs. 5 and 7). The peak and average strains in the medial aspect of the fifth metatarsal were significantly decreased by severe flexor fatigue (p = 0.0035 and p = 0.0006, respectively) and loading of only the Achilles tendon (p = 0.0002 and p < 0.0001). The peak and average strains in the lateral aspect of the fifth metatarsal were significantly decreased by severe flexor fatigue (p = 0.0003 and p = 0.0029, respectively) and loading of only the Achilles tendon (p < 0.0001 for both).



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  		Fig. 7 Graph of the mean average strain (and one standard deviation) in the fifth metatarsal for the fifteen specimens under each of the five conditions. * = significantly different from normal (p < 0.05).

 

Plantar Fasciotomy
After the plantar fasciotomy, the peak strain in the dorsal aspect of the second metatarsal (-3797 microstrain) was 100 percent higher than that under normal walking conditions (-1897 microstrain) (p < 0.0001), and the average strain in the dorsal aspect (-1829 microstrain) was 86 percent higher than that under normal walking conditions (-984 microstrain) (p < 0.0001) (Figs. 4 and 6). Both the peak (p = 0.0001) and the average (p < 0.0001) strain in the medial aspect of the second metatarsal increased in magnitude and reversed polarity, from compressive to tensile, after the plantar fasciotomy.

The peak strain in the lateral aspect of the fifth metatarsal increased significantly (p = 0.0284) after release of the plantar fascia (Fig. 5). The average strain in the dorsal aspect of the fifth metatarsal increased significantly (p = 0.0136) and the average strain in the proximal metaphysis decreased significantly (p = 0.0135) after the plantar fasciotomy (Fig. 7).


   Discussion
Top
 Abstract
 Introduction
 Materials and Methods
 Results
 Discussion
References
 
Stress fractures of the lower limbs are a major clinical problem in military recruits and in athletes2,4, 20,23,30,41. Clinical assessment can be difficult and depends on diagnostic techniques. The reported rates of stress fracture in military recruits range from 1.4 percent (295 of 20,422) with radiographic assessment4 to 31 percent (ninety-one of 295) with scintigraphy30. In one study of 295 military trainees with a total of 339 stress fractures, 28 percent (ninety-six) of the stress fractures occurred in the metatarsals4. Runners account for more stress fractures than all other athletes combined20. Sullivan et al.41 found that 14 percent (eight) of fifty-seven stress fractures of the lower limbs in runners occurred in the metatarsals. On the basis of his personal experience with more than 1000 stress fractures in runners, McBryde23 estimated that 20 percent of those fractures occur in the metatarsals, with 11 percent occurring in the second metatarsal. Stress fractures of the second metatarsal most often occur in the shaft and usually originate on the medial aspect of the bone. Stress fractures of the fifth metatarsal can also occur in the shaft, but they most often originate on the lateral aspect of the base15.

With use of cadaveric feet and a dynamic gait simulator, we were able to characterize strains in the second and fifth metatarsals during the entire stance phase of gait. Both simulated muscle fatigue and plantar fasciotomy significantly (p < 0.028) affected strain in the metatarsals. Peak strains were always higher in the second metatarsal than in the fifth. In addition, increases in strain after simulated muscle fatigue and plantar fasciotomy were greater in the second metatarsal than in the fifth. Simulated muscle fatigue generally increased peak strain in the second metatarsal, whereas it decreased peak strain in the fifth. After release of the plantar fascia, the peak strain in the dorsal aspect of the second metatarsal was 100 percent greater than it was under the normal walking condition (-3797 compared with -1897 microstrain), and it approached the extremes of physiological limits7. Since bone is viscoelastic and the simulations were performed at speeds that were slower than the speed of walking by live individuals, the model probably slightly overestimates the in vivo magnitude of the strains in the metatarsals; however, it is useful for the evaluation of the relative effects of muscle fatigue and plantar fasciotomy. On the basis of experimental work on the strain-rate sensitivity of bone24, we estimated that the strain values that we found in the metatarsals are approximately 15 percent greater than in vivo values.

It is also important to point out that the peak strains recorded by the axial gauges are not necessarily the peak strains in the cross section or in the bone as a whole. With use of finite element analysis and in vivo rosette-strain-gauge data to calculate peak strains in the mid-part of the third metacarpal shaft from a horse, Gross et al.17 found that the peak strains occurred away from the gauge sites. The peak strain at the gauge sites (-1900 microstrain) was almost 80 percent of the estimated peak strain in the cross section (-2400 microstrain). Burr et al.8 used rosette gauges to measure in vivo strains in human tibiae and found that the peak shear strains were greater than the peak principal strains. Although the axially directed strains reported in the present study provide a useful index for comparison, we readily acknowledge that they do not necessarily represent absolute peak values.

While the peak strain in the medial aspect of the second metatarsal was usually compressive during the gait simulations, it was tensile in six of the fifteen specimens, in part because of interspecimen variability in the cross-sectional geometry of the metatarsal and the loading behavior of the forefoot. Interestingly, stress fractures of the second metatarsal do not usually occur in the regions where we found the highest strains (the compressive strains in the dorsal aspect). Rather, they are more common in the medial aspect15, where we often recorded tensile strains. It is known that cortical bone has a longer fatigue life in compression than it does in tension9. Therefore, even though peak strains may occur in the dorsal aspect of the second metatarsal, stress fractures may be more common in the medial aspect because of inferior fatigue characteristics. In the fifth metatarsal, the peak strain in the base was tensile in thirteen of the fifteen specimens; however, the magnitude of the strain was lower than it was in the shaft, where stress fractures are less common. This finding corroborates the belief that stress fractures of the base of the fifth metatarsal are a consequence of activities, other than gait, that may induce excessive pronation or supination2, as opposed to march fractures, which are most common in the shaft and are caused by activities such as frequent marching during basic military training15.

Stress fractures are most commonly associated with intense training of athletes and military cadets, but they also occur in less active, healthy individuals as a result of normal daily activity that may not be any more vigorous than walking15. It is estimated that 35 percent of a recruit's training miles (seventy of 200 miles [113 of 322 kilometers]) entail marching and 65 percent (130 of 200 miles [209 of 322 kilometers]) entail running20. Substantial osseous microdamage probably accumulates in athletes and recruits during walking as well as running. In the present study, dynamic simulations of walking showed that muscle fatigue and plantar fasciotomy can increase strain in the metatarsals; it can therefore be hypothesized that muscle fatigue and plantar fasciotomy could also increase strain in the metatarsals during running and other vigorous activities.

Cyclical mechanical loading of cortical bone at physiological or greater strain levels is associated with an increase in fatigue damage6,10,27,35 and a decrease in strength and stiffness11,12,34. Increases in bone strain exponentially decrease the fatigue life of compact bone25,26. The accumulation of damage and fractures also occur in compact bone loaded under constant stress9,13,28; this suggests that increasing the average strain in the metatarsals during the entire stance phase causes additional damage to accumulate in the metatarsals by a creep mechanism. We believe that increases in peak and average strains in the metatarsals cause localized areas of microdamage during repetitive loading and that this damage is manifested as pain in the area of the metatarsals and represents the initial stages of a stress fracture. With use of an empirically derived equation for the fatigue life of cortical bone12, we estimated that the increase in strain in the second metatarsal due to simulated muscle fatigue caused a fourfold reduction in the number of loading cycles that the second metatarsal can withstand before failure. This estimation does not account for in vivo repair processes but is useful for approximating the relative risk of fatigue failure. If the metatarsals are repetitively loaded at high strains, causing fatigue damage to accumulate faster than it can be repaired by bone-remodeling, stress fractures most likely will occur.

In the present study, plantar fasciotomy caused greater increases in strain in the metatarsals than simulated muscle fatigue did. There have been clinical reports of pain3,43 and, more recently, of stress fractures in the metatarsals1,33 subsequent to a loss of function of the plantar fascia. On the basis of data on bone fatigue measured in vitro12, we estimated that plantar fasciotomy reduces the fatigue life of the second metatarsal fortyfold. Since the metatarsals and the plantar fascia are mechanically linked and both plantar fasciitis and stress fractures of the metatarsals are overuse injuries, it seems likely that patients who have plantar fasciitis would also have a high degree of accumulated fatigue damage in the metatarsals. If this is the case, the accumulation would be exacerbated by increased strain in the metatarsals due to the plantar fasciotomy. Thus, plantar fasciotomy or rupture of the plantar fascia in endurance athletes and military recruits may increase the likelihood of stress fractures in individuals who are already at risk.

Our estimations of metatarsal fatigue life based on the strain values obtained with use of the gait simulator are consistent with clinical reports on the occurrence of stress fractures of the metatarsals15,22,23,29,41. During normal gait in the present study, the peak strain in the fifth metatarsal was 908 microstrain. Simulated muscle fatigue decreased the strain, and plantar fasciotomy increased the peak strain to only 976 microstrain. These relatively low strain values might explain why stress fractures of the fifth metatarsal are less common than those of the more gracile second and third metatarsals in runners and military cadets23,29,41. Comparison of the strain values obtained from the simulator with laboratory fatigue data12 suggests that the fatigue life of the fifth metatarsal is fifty-one times greater than that of the second metatarsal under normal walking conditions.

In summary, our data indicate that muscle fatigue may increase the risk of stress fractures of the second metatarsal by increasing the peak and average strains and that loss of function of the plantar fascia may be even more deleterious by causing greater increases in peak and average strains. Fatigue of the toe flexors does not appear to be involved in the pathomechanics of stress fractures of the fifth metatarsal, as strains were reduced by simulated muscle fatigue; however, loss of function of the plantar fascia may increase the risk of stress fractures by increasing peak tensile strains in the lateral aspect of the fifth metatarsal.


   Footnotes
 
*No benefits in any form have been received or will be received from a commercial party related directly or indirectly to the subject of this article. Funds were received in total or partial support of the research or clinical study presented in this article. The funding source was Grant RG 94-0681 from The Whitaker Foundation.

{dagger}Orthopaedic Research Laboratories, University of California, Davis, School of Medicine, 4635 Second Avenue, Sacramento, California 95817.

{ddagger}Center for Locomotion Studies, The Pennsylvania State University, 29 Recreation Building, University Park, Pennsylvania 16802. E-mail address: nas9@psu.edu.


   References
Top
 Abstract
 Introduction
 Materials and Methods
 Results
 Discussion
 References
 

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