Effects of fatigue and load variation on metatarsal deformation measured in vivo during barefoot walking

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Abstract

This in vivo study presents information to assist in the understanding of metatarsal stress fracture etiology. The aims were (a) to provide a fundamental description of loading patterns of the second metatarsal (MTII) during barefoot walking, and (b) to investigate the hypothesis that MTII dorsal strain increases with fatigue and external carrying load. Dorsal MTII strain was measured in vivo under local anaesthetic with an instrumented staple in eight subjects. Experimental conditions were external loading with a 20 kg backpack and pre- and post-fatigue. M. flexor digitorum longus electromyography tentatively indicated fatigue after an extended walking treatment. A reproducible, cyclic temporal pattern of dorsal MTII surface deformation was described. Mean peak compression and tension strains in unloaded barefoot walking were −1534±636 and 363±359 με, respectively. Mean peak compression strain rate (SR) was −4165±1233 με/s. Compression strain increased significantly (α=0.05) both with the addition of the backpack and post-fatigue while maximum tension decreased significantly post-fatigue. SR increased significantly with the addition of the backpack. The highest plantar force time integrals were recorded underneath the heads of metatarsals II–V for all conditions (1561 N s pre-fatigue, without backpack; 2123 N s post, with). EMG and plantar pressure data presented a comprehensive description of biomechanical parameters influencing dorsal MTII deformation and alterations in strain following two experimental conditions were suggested as contributing factors in the pathogenesis of metatarsal stress fractures.

Introduction

Stress fractures are fractures that occur in the absence of a specific acute precipitating event (Buckwalter and Brandser, 1997) and are commonly reported in normal bones of young adults during periods of increased physical activity such as military or sports training. In a prospective study of 295 soldiers Milgrom et al. (1985) reported 184 stress fractures of the lower extremity of which 14 (7.6%) were of the metatarsals. A study of 169 stress fractures by Ha et al. (1991) showed 12 located at the second metatarsal (MTII). Up to 20% (11% MTII) of stress fractures in athletes and 23% in military recruits are located in the metatarsals (McBryde, 1985; Matheson et al., 1987; Hulkko, 1988). One hypothesis describing the occurrence of stress fractures is that insufficient remodeling of stressed bone results in fatigue related trabecular microfractures (Carter et al., 1981; McBryde, 1985; Fazzalari, 1993; Buckwalter and Brandser, 1997). Stress fractures may be initiated by excessive repetitive muscular forces (Stanitski et al., 1978; Orava et al., 1995).

Local bone deformation is regarded as an indicator of stress fracture risk and the measurement of local bone deformation using strain gauges has been performed for many years (Fries, 1972). This method is, however, not free of difficulties. There are disadvantages involved in the in vivo application of strain gauges directly onto osseous surfaces. It is difficult to provide a completely dry, chemically clean bone surface for the strain gauge bond and the effects of the bonding between the bone and the strain gauge are unknown and uncontrolled. Until recently cyanoacrylate adhesives were used for strain gauge application to the bone surface but this is not approved for human experimentation due to carcinogenic risks. Good results were reported by Hoshaw et al. (1997) for polymethylmethacrylate (PMMA) bonding, which is now being applied in human in vivo experiments. This technique is, however, quite invasive as the periosteum must be removed for strain gauge application and the bone is ‘roughened’ with a metal punch for optimal bonding surface preparation.

The insertion of instrumented staples involves less traumatic surgery and is thus more appropriate for human in vivo application. Strain on the human tibia has previously been measured in vivo with rosette strain gauges (Lanyon et al., 1975), transcutaneous extensometers (Fyhrie et al., 1998) and inserted staples (Burr et al., 1996; Ekenman et al., 1998a). Excellent linearity and good long-term results have been reported in measurements of in vivo loading of the canine lumbar spine with instrumented staples (Butterman et al., 1994). No such investigation has, however, been performed on metatarsals or bones of corresponding size and previous values for human metatarsal loading have been limited to theoretical biomechanical models (Stokes et al., 1979; Gross and Bunch, 1989) and in vitro investigations of human cadaver specimens (Lease and Evans, 1959; Sharkey et al., 1995; Courtney et al., 1997; Donahue and Sharkey, 1999).

The MTII is subject to disproportionally high external loads relative to its physical dimensions. Donahue and Sharkey (1999) measured metatarsal deformation on a cadaver lower leg model simulating walking and found the mean peak dorsal strain to be −1897 με, which was significantly higher than strain measured on the fifth metatarsal. A dorsal compressive strain of −6662 με was calculated by Gross and Bunch (1989) for the MTII which exceeded that of the first metatarsal by a factor of 6.9. Excessive bending moments resulting from inactivity or fatigue of the toe flexor muscles are commonly mentioned in the etiology of metatarsal overuse injuries (Tanaka, 1981; Sharkey et al., 1995; Voloshin et al., 1998; Donahue and Sharkey, 1999). Increased local bone deformation resulting from lacking soft tissue support can lead to forces responsible for stress fractures, metatarsalgia and flattening of the longitudinal arch of the foot. In military recruits vigorous marches at an early stage of military service provide the prerequisites for both repetitive external loading and muscular fatigue, which may explain the exceptionally high rate of stress fractures. In this study in vivo measurement of metatarsal strains was utilized to address these factors by comparing two experimental treatments: with and without external loading with a 20 kg backpack and the effect of fatigue.

Section snippets

Staple mounted strain gauge

The application of the staple technique to bones approximating the dimensions of MTII had been previously tested in an in vitro pilot study using chicken tibiae (Arndt et al., 1999). The results showed a linearity of strain measurements relative to a controlled input force of R2=0.992±0.006 and an intraclass correlation coefficient of 0.92.

Two strain gauges (types EA-06-031DE-350 and EA-06-031EC-350, Measurement Group Inc., USA) were mounted perpendicular to each other on the underneath bridge

Temporal description of MTII deformation

A repetitive cyclic pattern of local MTII deformation was seen (Fig. 2). The following fundamental temporal pattern describes the mean±standard deviation of all subjects for barefoot, pre-fatigue, no backpack treadmill walking. TD was followed by peak tension, which occurred at 8±7% stance phase followed by a transition to maximum compression during the majority of stance phase with peak compression at 65±15%. Immediately after peak compression local deformation decreased to ≈0 με around which

Discussion

There are obvious limitations involved when measuring strain at a single location in a single direction on a bone surface and attempting to apply the results to general behaviour of the bone during loading as different strains can of course be acting at other locations and in other directions. The dorsal MTII surface was, however, chosen as it is a relevant site in the discussion of stress fractures and was easily accessible for the in vivo technique used. No limitations in terms of

Conclusions

Maximum strains measured on the human second metatarsal during walking were in the range described in the literature for other bones during physiological loading. The direct in vivo method here described provided concrete information on the biomechanical loading of the human foot during gait.

The fatigue implications raised by the results of this study are treated with caution as the extent of fatigue experienced by long-distance athletes or military recruits greatly exceeds that produced in

Acknowledgements

Financial support for this study was provided by the Swedish Defense Material Administration and the Karolinska Institute, Sweden.

References (32)

  • G.R. Butterman et al.

    Description and application of instrumented staples for measuring in vivo bone strain

    Journal of Biomechanics

    (1994)
  • D.L. Carter et al.

    Fatigue behaviour of adult cortical bonethe influence of mean strain and strain range

    Acta Orthopaedica Scandinavica

    (1981)
  • A.C. Courtney et al.

    Effects of age, density, and geometry on the bending strength of human metatarsals

    Foot and Ankle International

    (1997)
  • S.E. Donahue et al.

    Strains on the metatarsals during the stance phase of gaitimplications for stress fractures

    Journal of Bone and Joint Surgery

    (1999)
  • I. Ekenman et al.

    Local bone deformation at two predominant sites for stress fracture of the tibia—an in vivo study

    Foot and Ankle International

    (1998)
  • I. Ekenman et al.

    The reliability and validity of an instrumented staple system for in vivo measurement of local bone deformation—an in vitro study

    Scandinavian Journal of Medicine and Science in Sports

    (1998)
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