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Bulk compressive properties of the heel fat pad during walking: A pilot investigation in plantar heel pain
Clinical Biomechanics 24 (2009) 397–402
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Clinical Biomechanics journal homepage: www.elsevier.com/locate/clinbiomech
Bulk compressive properties of the heel fat pad during walking: A pilot investigation in plantar heel pain Scott C. Wearing a,*, James E. Smeathers b, Bede Yates c, Stephen R. Urry b,d, Philip Dubois c a
Health QWest and Bioengineering Unit, University of Strathclyde, 106 Rottenrow, Glasgow, Scotland G4 0NW, UK Institute of Health and Biomedical Innovation, Queensland University of Technology, Queensland, Australia c Queensland X-ray, Mater Private Hospital, South Brisbane, Queensland, Australia d Centre of Excellence for Applied Sports Science Research, Queensland Academy of Sport, Queensland, Australia b
a r t i c l e
i n f o
Article history: Received 20 August 2008 Accepted 13 January 2009
Keywords: Heel pad Compression Soft tissue properties Fluoroscopy Plantar fasciitis Gait
a b s t r a c t Background: Altered mechanical properties of the heel pad have been implicated in the development of plantar heel pain. However, the in vivo properties of the heel pad during gait remain largely unexplored in this cohort. The aim of the current study was to characterise the bulk compressive properties of the heel pad in individuals with and without plantar heel pain while walking. Methods: The sagittal thickness and axial compressive strain of the heel pad were estimated in vivo from dynamic lateral foot radiographs acquired from nine subjects with unilateral plantar heel pain and an equivalent number of matched controls, while walking at their preferred speed. Compressive stress was derived from simultaneously acquired plantar pressure data. Principal viscoelastic parameters of the heel pad, including peak strain, secant modulus and energy dissipation (hysteresis), were estimated from subsequent stress–strain curves. Findings: There was no significant difference in loaded and unloaded heel pad thickness, peak stress, peak strain, or secant and tangent modulus in subjects with and without heel pain. However, the fat pad of symptomatic feet had a significantly lower energy dissipation ratio (0.55 ± 0.17 vs. 0.69 ± 0.08) when compared to asymptomatic feet (P < .05). Interpretation: Plantar heel pain is characterised by reduced energy dissipation ratio of the heel pad when measured in vivo and under physiologically relevant strain rates. Ó 2009 Elsevier Ltd. All rights reserved.
1. Introduction Plantar heel pain is a poorly understood condition, which is characterised by pain localised to the medial calcaneal tubercle that is exacerbated with the onset of weight-bearing. While numerous aetiological factors have been hypothesised within the literature, the largely idiopathic condition has been classically viewed as an ‘overuse injury’ in which mechanical overload arising from repeated heel strike is thought to invoke an inflammatory response at the fascial enthesis (Riddle et al., 2003). However, inflammatory infiltrate has been rarely reported to involve the plantar fascia in chronic cases of plantar heel pain (Lemont et al., 2003; Tountas and Fornasier, 1996), despite evidence of diffuse fluid accumulation in perientheseal soft tissue structures, such as the heel pad, with medical imaging (Grasel et al., 1999). With the advent of the ‘‘enthesis organ” concept, in which the classical view of the enthesis has been expanded to include a complex of adjacent tissues that jointly serve to dissipate stress (Benjamin et al., 2004), * Corresponding author. E-mail address: [email protected] (S.C. Wearing). 0268-0033/$ - see front matter Ó 2009 Elsevier Ltd. All rights reserved. doi:10.1016/j.clinbiomech.2009.01.002
interest in perientheseal structures, such as the heel pad, in the development of chronic plantar heel pain, has been renewed. The heel pad has long been recognised as an important structure in dissipating the impulsive transients associated with heel strike (Jørgensen, 1985). However, the effect of plantar heel pain on the morphology and mechanical properties of the heel pad remains unclear. While some studies have observed a thicker heel pad, in both loaded and unloaded states, when compared to asymptomatic heels (Rome et al., 2002), the majority of studies have found heel pad thickness to remain unchanged in plantar heel pain (Turgut et al., 1999; Kanatli et al., 2001; Tsai et al., 2000). Similarly, the ‘elasticity’ of the heel pad has been reported to be either lower (Jørgensen, 1985; Prichasuk, 1994) or no different (Turgut et al., 1999; Tsai et al., 2000) to that of asymptomatic heels when a quasi-static measure, the compressibility index (the ratio of unloaded to loaded heel pad thickness), is used to characterise the properties of the heel pad. Although insightful, such quasi-static measures do not adequately replicate the loading conditions experienced by the heel pad during the dynamics of gait, which is critical when evaluating the mechanical properties of viscoelastic structures.
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Although studies employing more dynamic, sonograph-based indentation systems, have reported stiffness values of the heel pad to be lowered, heightened or unchanged in plantar heel pain (Rome et al., 2001; Tsai et al., 1999), they have typically employed either slow loading rates or have restricted their evaluation to the elastic properties of heel pad during loading, thus largely neglecting unloading and viscous factors. Characterisation of the timedependent behaviour of the heel pad is of particular importance in plantar heel pain, as it has long been regarded to contribute to the dissipation of the shock associated with heel strike (Jørgensen, 1985). Moreover, recent research in diabetes has shown that the viscous properties of soft tissues may be more sensitive to disease states than commonly measured properties, such as tissue stiffness (Hsu et al., 2002). While several approaches to studying the dynamic properties of the heel pad are available, including in vitro testing of cadaveric heels (Aerts et al., 1995, 1996; Ker, 1996; Bennett and Ker, 1990) and in vivo testing using impact and ballistic pendulum approaches (Kinoshita et al., 1993; Aerts and De Clercq, 1993), to date, research specifically directed toward evaluating the viscoelastic properties of the heel pad in plantar heel pain during the dynamics of gait is lacking. Promising early work in which fluoroscopy (cine-radiography) was used to evaluate the in vivo compressive strain of the heel pad during running (De Clercq et al., 1994), has been recently expanded to include simultaneous measures of the contact pressure beneath the foot during gait (Gefen et al., 2001). By incorporating measures of heel contact stress, the modified technique affords the ability to estimate geometrically-independent, material properties of the heel pad under the dynamic conditions of gait, thus overcoming the limitations of many of the previous techniques. The aim of the current investigation, therefore, was to employ a digital fluoroscope integrated with a capacitance mat transducer system to estimate the bulk compressive properties of heel pad in individuals with and without unilateral plantar heel pain while walking at their preferred speed.
2. Methods 2.1. Subjects Nine subjects (3 male and 6 female) with unilateral plantar heel pain (age, 48 ± 13 yrs; height, 1.68 ± 0.11 m; weight, 81.6 ± 10.7 kg) and nine asymptomatic control subjects, individually matched for age, sex and body weight (age, 46 ± 12 yrs; height, 1.67 ± 0.11 m; weight, 80.1 ± 10.4 kg) participated in the study. Subjects with heel pain presented to a university foot and ankle clinic with focal tenderness localised to the calcaneal insertion of the plantar fascia, which was exacerbated with weight-bearing following periods of unloaded rest. Subjects were excluded if they presented with diffuse or bilateral pain, evidence of inflammatory arthropathy or a history of trauma or foot surgery. The mean duration of heel pain was 9 ± 6 months, with the average ‘first step’ pain rated as 4 ± 2 cm on a standard 10-cm visual analogue pain scale. All subjects gave written informed consent prior to participation in the study, which received approval from the institutional review board. 2.2. Equipment Dynamic lateral radiographs of each foot were acquired using a C-Vision multifunction fluoroscopy unit (Shimadzu, Kyoto, Japan) configured with a 405 mm four-field image intensifier. Radiographs were acquired at an exposure equivalent to 1.2 mA s 1 and an intensity of 50 kV. The imaging system incorporated a single 1024 1024 pixel array CCD camera with a sampling rate of
15 Hz. Spatial distortion within the fluoroscopic field of view was corrected using a rectilinear calibration grid (32 32 cm) positioned within the object plane and perpendicular to the central ray (Wearing et al., 2005), in combination with a previously outlined distortion correction procedure (Baltzopoulos, 1995). The RMS error for repeated linear measures of a calibration foot phantom using this method is 0.1 mm (Wearing et al., 2005). An EMED-SF capacitance mat transducer system (Novel GmbH, Munich, Germany), mounted within the field of view was used to simultaneously record pressure and temporal data at a sampling rate of 50 Hz. The 23 34-cm platform had a matrix of 2736 sensors, with an effective spatial resolution of four sensors per cm2. 2.3. Procedures Data collection was preceded by a familiarisation period in which the starting position of each subject was iteratively modified to ensure placement of the foot within the field of view, without obvious gait adjustments or targeting. Barefoot pressure and fluoroscopic data were collected following a preamble of at least three steps, while subjects walked at a self-selected speed. Walking speed was not monitored. Rather, consistency between trials was ensured by monitoring the stance phase duration of each footstep; which differed by less than 5% between trials. Trials were omitted if footsteps did not fall entirely within the boundaries of the fluoroscopic field of view, or if the investigators observed gait adjustments secondary to visual targeting of the platform. Three trials were recorded for each limb. 2.4. Data analysis Fluoroscopic images were post-processed using Matlab software (MathWorks Inc, Natick, Massachusetts, USA). Following the application of a global distortion correction procedure (Baltzopoulos, 1995; Wearing et al., 2005), convolution and edge detection algorithms were used to enhance the bone–soft-tissue interface. The inferior aspect of the lateral projection of the calcaneus and fifth metatarsal head were manually digitized from initial heel contact to the onset of heel lift. The foot–ground contact angle, defined as the axis intersecting the plantar surface of the metatarsal head and the calcaneal tuberosity relative to the support surface, was subsequently calculated. The sagittal thickness and deformation of the heel pad throughout the contact and midstance phase was calculated as the minimum gap between the inferior aspect of the calcaneus and the support surface (Fig. 1). Maximum sagittal deformation of the heel pad was used to calculate the loaded heel pad thickness (LHPT), while the unloaded thickness of the heel pad (ULHPT) was measured immediately prior to initial contact and provided the reference value for the computation of true compressive strain. True compressive strain was calculated as the ratio of deformation of the heel pad relative to the instantaneous heel pad thickness. For the purposes of the current study, compression is reflected by positive stress and strain values. Pressure data were analysed using proprietary software (Novel GmbH, Munich, Germany). The stance phase duration for the entire foot and temporal and peak pressure data beneath the heel, including the force–time integral, were calculated using a standardised masking procedure, in which the length of the footprint, excluding the toes, was divided into equal thirds. The initial stress rate during heel loading was determined by calculating the slope of the linear section of the peak pressure–time loading curve using a linear regression approach. Peak pressure data were subsequently resampled to 15 Hz to match strain data and employed as a measure of true compressive stress. Stress–strain data for each subject were interpolated using a cubic spline procedure and peak compressive stress and strain values
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S.C. Wearing et al. / Clinical Biomechanics 24 (2009) 397–402 Table 1 Mean (SD) principal gait parameters.
n Stance phase duration (ms) Foot–ground contact angle (°) Onset of heel lift (% stance phase duration) Peak stress (kPa) Instant of peak stress (% heel contact time) Stress rate during heel loading (kPa s
1
Force–time integral beneath heel (N s)
)
Control
Heel pain
9 921 (82) 12.9 (2.3) 58 (7) 246 (41) 32 (4) 1193 (125) 147 (37)
9 991 (128) 12.1 (3.0) 61 (10) 244 (22) 30 (5) 1242 (326) 158 (62)
Note: No statistically significant difference between groups (P > .05).
Fig. 1. A representative fluoroscopic image of the posterior aspect of the calcaneus and enveloping soft tissue during the stance phase of walking. Note the rectilinear array of calibration markers placed in the field of view used to correct for image distortion and as a reference of known distance to the support surface allow the thickness (t) of the heel pad relative to the support surface to be calculated.
created irregular stress–strain curves. The ensemble stress–strain curve for subjects with and without heel pain is shown in Fig. 3. No statistically significant differences were observed in the loaded and unloaded thickness, peak strain or secant modulus of heel pad in individuals with and without heel pain (Table 2). However, the heel pad was characterised by a significantly lower EDR (20%) in plantar heel pain when compared to healthy counterparts (P < .05). 4. Discussion
were calculated. The secant modulus was defined as the stress– strain ratio at the point of peak stress, while the tangent modulus was calculated over 50% of the loading curve using a linear regression approach in which the least square error was minimised. The area beneath each loading and unloading curve was estimated by numerical integration based on the trapezoid rule and the difference represented the area of the hysteretic loop. The energy dissipation ratio (EDR) was calculated as the area of the hysteretic loop relative to the area under the loading curve. 2.5. Statistical analysis The Statistical Package for the Social Sciences (SPSS Inc, Chicago, IL, USA) was used for all statistical procedures. Kolmogorov–Smirnov tests were used to evaluate data for underlying assumptions of normality. Since all outcome variables were normally distributed, means and standard deviations have been used as summary statistics. Differences in each of the dependent variables of interest (stance phase duration, ULHPT, LHPT, peak stress, peak strain, secant and tangent modulii and the EDR) were assessed using paired t-tests. An alpha level of 0.05 was used for all tests of significance. 3. Results There was no statistically significant difference in the mean stance phase duration between symptomatic and control limbs (P > .05). Similarly, there was no significant difference in the initial foot–ground contact angle between symptomatic and control limbs (P > .05). The duration of loading beneath the heel was comparable across groups, with no significant difference in the onset of heel lift observed in symptomatic and control heels (P > .05). No statistically significant differences were noted in the average stress rate during heel loading, the peak stress, time to peak stress and the force–time integral (impulse) beneath the heel between heel pain and control groups (Table 1). Real in vivo transient loading profiles associated with walking induced rapidly changing strain rates in the heel pad (Fig. 2) and
Absolute deformation of the fat pad in the current investigation was similar to that reported during barefoot running (9 ± 0.5 mm) and approximately twice that reported for shod running (De Clercq et al., 1994). The tangent modulus is comparable to those obtained from in vitro tests on excised plantar soft tissues following quasilinear statistical modelling of triangular wave stress–strain data (Ledoux and Blevins, 2007). The energy dissipated by heel pads in the current investigation (0.55 and 0.69), however, was greater than that reported for cyclic loading in cadaveric specimens (0.29–0.37) (Aerts et al., 1995; Ker, 1996; Ledoux and Blevins, 2007) and for previous in vivo measures of asymptomatic heels (0.24–0.40) using sonograph based quasi-static loading methods (Hsu et al., 1998; Tsai et al., 2000). While the energy dissipation ratios are lower than mean values reported for impact tests (0.73– 0.78) performed on healthy young adults and the elderly in vivo (Kinoshita et al., 1993), they fall between those reported for impact tests on isolated heel pads in vitro (0.65–0.86) and for ‘first loop’ energy loss values (0.39–0.67) reported for isolated cadaveric heels (Aerts et al., 1995; Ker, 1996). While methodological differences hamper cross-study comparisons, the energy dissipation ratio of heel pads in the current study is approximately 3-fold greater than those cited by Gefen et al. (2001) in which a similar fluoroscopic technique was employed (0.18). Although the latter study was restricted by low subject numbers (n = 2), peak stress values reported for the heel (60– 70 kPa) were substantially lower (3–4 fold) than those of the current and previous studies in which peak plantar pressures for the heel were recorded during barefoot walking (Cavanagh et al., 1997). The kinetic energy dissipated at heel strike largely depends on the contact velocity of the heel and effective mass of the lower limb (De Clercq et al., 1994). While the present study did not monitor the knee contact angle, it is possible that individuals with heel pain may have adopted a less energetic gait pattern, thereby reducing the energy damping requirement of the heel fat pad. However, we observed no significant difference in the average foot–ground
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Fig. 2. Ensemble average strain rate of the heel fat pad as a function of heel contact duration in subjects with unilateral plantar heel pain (n = 9) and individually matched control subjects (n = 9). Fine solid and dashed lines represent standard deviations for control and symptomatic heel pads, respectively.
contact angle, stance duration, or onset of heel lift between control and heel pain groups, suggesting subjects with heel pain adopted a similar foot roll-over pattern. Moreover, we observed no significant difference in the peak stress, time to peak stress or average initial stress rate during heel loading, suggesting that initial contact conditions between heel pain and control groups were comparable.
In the absence of demonstrable fluid flow between the compartments of the fat pad, Ker (1999) proposed that, the heel functions as a hydrostat, in which adipocytes act as a fluid of fixed volume, confined within connective tissue walls that distort with weightbearing. On the basis that changes in the apparent consistency of fat had little effect on the strain behaviour of the heel pad when
Fig. 3. Ensemble stress–strain curves for the heel fat pad in subjects with unilateral plantar heel pain (n = 9) and individually matched control subjects (n = 9). Arrows indicate direction of loading and unloading.
S.C. Wearing et al. / Clinical Biomechanics 24 (2009) 397–402 Table 2 Mean (SD) principal viscoelastic parameters of the heel pad.
n ULHPT (mm) LHPT (mm) Peak strain Tangent modulus (kPa) Secant modulus (kPa) EDR
Control
Heel pain
9 19.1 (1.9) 8.8 (1.5) 0.43 (0.05) 637 (124) 580 (145) 0.69 (0.08)
9 19.3 (1.7) 10.0 (2.1) 0.39 (0.09) 600 (81) 647 (128) 0.55a (0.17)
ULHPT: Unloaded heel pad thickness. LHPT: Minimum heel pad thickness during gait. EDR: Energy dissipation ratio. a Indicates statistically significant difference between groups (P < .05).
tested in vitro (Bennett and Ker, 1990; Ker, 1996), the mechanical properties of the heel pad were proposed to reflect those of the septal wall, which is composed of relatively inelastic collagen fibres surrounding a central core of highly deformable fibres that incorporate elastin (Buschmann et al., 1995). While the relationship between the structural components and viscoelastic properties of collagen rich tissue is complex, the finding that the heel pad had a reduced energy dissipation ratio in plantar heel pain suggests it behaves as a more elastic solid. The elastic mechanical responses of collagen, as well as the energy dissipation from proteoglycan–collagen and proteoglycan–proteoglycan interactions, are known to be influenced by the abundance and size of proteoglycans, the degree to which they form stable aggregates, and the integrity of the surrounding collagen network (Elliott et al., 2003). Thus, the reduction in the energy dissipation ratio of the heel pad in plantar heel pain may arise from a lower content, quality or aggregation state of proteoglycan or a relative increase in collagen organisation and cross-linking. While there is experimental evidence that degenerative change of the heel pad is characterised by a loss of water content (Kuhns, 1949), an increase in collagen organisation and cross-linking would, however, also increase the stiffness (elastic modulus) of the tissue, which was not observed in the current study. Similar reductions in viscosity, albeit with a concomitant rise in elastic modulus, have been reported in ovine cartilage exposed to elevated levels of nitric oxide (Cake et al., 2003), in rodent skin exposed to prednisilone acetate (Vogel, 1993) and more recently in a disuse model of rodent tendon (Eliasson et al., 2007). Irrespective of the underlying mechanism, reduced energy dissipation of the heel pad may increase the risk of fatigue and microinjury at sites of local stress concentration within the heel, and thus either initiate or exacerbate the condition. As with all crosssectional research, however, the current study cannot establish potential cause-and-effect relationships between plantar heel pain and reduced energy dissipation of the heel pad. It is unknown, therefore, whether plantar heel pain results in altered properties of the heel fat pad, or whether reduced energy dissipation of the heel pad contributes to the development of plantar heel pain. The present study employed fluoroscopy to evaluate deformation of the heel pad. Fluoroscopy is a transmission technique that creates two-dimensional (2-D) projections of what is undoubtedly a three-dimensional (3-D) deformation. The findings, therefore, are only applicable to the sagittal plane compressive properties of the heel pad. In addition, compression of the heel pad was viewed as an extension of Hertzian contact, in which the peak stress and
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strain were assumed to coincide with the point of contact between an homogenous elastic half space and a spherical calcaneal surface. Support for such an idealisation is provided by evidence that the properties of the heel pad are likely isotropic in nature (MillerYoung et al., 2002), and that the magnitude of tangential stress components of the heel are <10% of the peak vertical stress during barefoot walking (Lebar et al., 1996). A further limitation of the current study was that the temporal resolution of the imaging system resulted in a relatively low sampling rate (15 Hz) compared to modern motion analysis systems. Although theoretically sufficient to capture the majority of skeletal movements in gait, in which frequencies up to 5 or 6 Hz are typically reported (Winter et al., 1974), the method is not suitable for evaluating the specific response of the heel pad to impulsive transients associated with heel strike, in which frequencies as high as 100 Hz have been recorded (Simon et al., 1981). In addition, fluoroscopic imaging produces relatively low contrast between different types of soft tissue structures (Fig. 1). Hence, the technique does not permit the contribution of various internal structures, such as the superficial microchamber or the deep macrochamber (Hsu et al., 2007), to the bulk compressive behaviour of the heel pad to be ascertained. 5. Conclusions The findings of the present investigation indicate that plantar heel pain is associated with altered viscoelastic behaviour of the heel pad, which is characterised by a reduced energy dissipation ratio during walking when measured in vivo and under free living conditions. Acknowledgement The authors received no financial support for the preparation of this manuscript and have no competing interests that are directly related to its contents. References Aerts, P., De Clercq, D., 1993. Deformation characteristics of the heel region of the shod foot during a simulated heel strike: the effect of varying midsole hardness. J. Sports. Sci. 11, 449–461. Aerts, P., Ker, R.F., De Clercq, D., et al., 1995. The mechanical properties of the human heel pad: a paradox resolved. J. Biomech. 28, 1299–1308. Aerts, P., Ker, R.F., De Clercq, D., et al., 1996. The effects of isolation on the mechanics of the human heel pad. J. Anat. 188, 417–423. Baltzopoulos, V., 1995. A videofluoroscopy method for optical distortion correction and measurement of knee–joint kinematics. Clin. Biomech. 10, 85–92. Benjamin, M., Moriggl, B., Brenner, E., et al., 2004. The ‘‘enthesis organ” concept: why enthesopathies may not present as focal insertional disorders? Arthritis Rheum. 50, 3306–3313. Bennett, M.B., Ker, R.F., 1990. The mechanical properties of the human subcalcaneal fat pad in compression. J. Anat. 171, 131–138. Buschmann, W.R., Jahss, M.H., Kummer, F., et al., 1995. Histology and histomorphometric analysis of the normal and atrophic heel fat pad. Foot Ankle Int. 16, 254–258. Cake, M.A., Appleyard, R.C., Read, R.A., et al., 2003. Topical administration of the nitric oxide donor glyceryl trinitrate modifies the structural and biomechanical properties of ovine articular cartilage. Osteoarthritis Cartilage 11, 872–878. Cavanagh, P., Morag, E., Boulton, A.J.M., et al., 1997. The relationship of static foot structure to dynamic foot function. J. Biomech. 30, 243–250. De Clercq, D., Aerts, P., Kunnen, M., 1994. The mechanical characteristics of the human heel pad during foot strike in running: an in vivo cineradiographic study. J. Biomech. 27, 1213–1222. Eliasson, P., Fahlgren, A., Pasternak, B., et al., 2007. Unloaded rat Achilles tendons continue to grow, but lose viscoelasticity. J. Appl. Physiol. 103, 459–463. Elliott, D.M., Robinson, P.S., Gimbel, J.A., et al., 2003. Effect of altered matrix proteins on quasilinear viscoelastic properties in transgenic mouse tail tendons. Ann. Biomed. Eng. 31, 599–605. Gefen, A., Megido-Ravid, M., Itzchak, Y., 2001. In vivo biomechanical behavior of the human heel pad during the stance phase of gait. J. Biomech. 34, 1661–1665. Grasel, R.P., Schweitzer, M.E., Kovalovich, A.M., et al., 1999. MR imaging of plantar fasciitis: edema, tears, and occult marrow abnormalities correlated with outcome. Am. J. Roentgenol. 173, 699–701.
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Clinical Biomechanics journal homepage: www.elsevier.com/locate/clinbiomech
Bulk compressive properties of the heel fat pad during walking: A pilot investigation in plantar heel pain Scott C. Wearing a,*, James E. Smeathers b, Bede Yates c, Stephen R. Urry b,d, Philip Dubois c a
Health QWest and Bioengineering Unit, University of Strathclyde, 106 Rottenrow, Glasgow, Scotland G4 0NW, UK Institute of Health and Biomedical Innovation, Queensland University of Technology, Queensland, Australia c Queensland X-ray, Mater Private Hospital, South Brisbane, Queensland, Australia d Centre of Excellence for Applied Sports Science Research, Queensland Academy of Sport, Queensland, Australia b
a r t i c l e
i n f o
Article history: Received 20 August 2008 Accepted 13 January 2009
Keywords: Heel pad Compression Soft tissue properties Fluoroscopy Plantar fasciitis Gait
a b s t r a c t Background: Altered mechanical properties of the heel pad have been implicated in the development of plantar heel pain. However, the in vivo properties of the heel pad during gait remain largely unexplored in this cohort. The aim of the current study was to characterise the bulk compressive properties of the heel pad in individuals with and without plantar heel pain while walking. Methods: The sagittal thickness and axial compressive strain of the heel pad were estimated in vivo from dynamic lateral foot radiographs acquired from nine subjects with unilateral plantar heel pain and an equivalent number of matched controls, while walking at their preferred speed. Compressive stress was derived from simultaneously acquired plantar pressure data. Principal viscoelastic parameters of the heel pad, including peak strain, secant modulus and energy dissipation (hysteresis), were estimated from subsequent stress–strain curves. Findings: There was no significant difference in loaded and unloaded heel pad thickness, peak stress, peak strain, or secant and tangent modulus in subjects with and without heel pain. However, the fat pad of symptomatic feet had a significantly lower energy dissipation ratio (0.55 ± 0.17 vs. 0.69 ± 0.08) when compared to asymptomatic feet (P < .05). Interpretation: Plantar heel pain is characterised by reduced energy dissipation ratio of the heel pad when measured in vivo and under physiologically relevant strain rates. Ó 2009 Elsevier Ltd. All rights reserved.
1. Introduction Plantar heel pain is a poorly understood condition, which is characterised by pain localised to the medial calcaneal tubercle that is exacerbated with the onset of weight-bearing. While numerous aetiological factors have been hypothesised within the literature, the largely idiopathic condition has been classically viewed as an ‘overuse injury’ in which mechanical overload arising from repeated heel strike is thought to invoke an inflammatory response at the fascial enthesis (Riddle et al., 2003). However, inflammatory infiltrate has been rarely reported to involve the plantar fascia in chronic cases of plantar heel pain (Lemont et al., 2003; Tountas and Fornasier, 1996), despite evidence of diffuse fluid accumulation in perientheseal soft tissue structures, such as the heel pad, with medical imaging (Grasel et al., 1999). With the advent of the ‘‘enthesis organ” concept, in which the classical view of the enthesis has been expanded to include a complex of adjacent tissues that jointly serve to dissipate stress (Benjamin et al., 2004), * Corresponding author. E-mail address: [email protected] (S.C. Wearing). 0268-0033/$ - see front matter Ó 2009 Elsevier Ltd. All rights reserved. doi:10.1016/j.clinbiomech.2009.01.002
interest in perientheseal structures, such as the heel pad, in the development of chronic plantar heel pain, has been renewed. The heel pad has long been recognised as an important structure in dissipating the impulsive transients associated with heel strike (Jørgensen, 1985). However, the effect of plantar heel pain on the morphology and mechanical properties of the heel pad remains unclear. While some studies have observed a thicker heel pad, in both loaded and unloaded states, when compared to asymptomatic heels (Rome et al., 2002), the majority of studies have found heel pad thickness to remain unchanged in plantar heel pain (Turgut et al., 1999; Kanatli et al., 2001; Tsai et al., 2000). Similarly, the ‘elasticity’ of the heel pad has been reported to be either lower (Jørgensen, 1985; Prichasuk, 1994) or no different (Turgut et al., 1999; Tsai et al., 2000) to that of asymptomatic heels when a quasi-static measure, the compressibility index (the ratio of unloaded to loaded heel pad thickness), is used to characterise the properties of the heel pad. Although insightful, such quasi-static measures do not adequately replicate the loading conditions experienced by the heel pad during the dynamics of gait, which is critical when evaluating the mechanical properties of viscoelastic structures.
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Although studies employing more dynamic, sonograph-based indentation systems, have reported stiffness values of the heel pad to be lowered, heightened or unchanged in plantar heel pain (Rome et al., 2001; Tsai et al., 1999), they have typically employed either slow loading rates or have restricted their evaluation to the elastic properties of heel pad during loading, thus largely neglecting unloading and viscous factors. Characterisation of the timedependent behaviour of the heel pad is of particular importance in plantar heel pain, as it has long been regarded to contribute to the dissipation of the shock associated with heel strike (Jørgensen, 1985). Moreover, recent research in diabetes has shown that the viscous properties of soft tissues may be more sensitive to disease states than commonly measured properties, such as tissue stiffness (Hsu et al., 2002). While several approaches to studying the dynamic properties of the heel pad are available, including in vitro testing of cadaveric heels (Aerts et al., 1995, 1996; Ker, 1996; Bennett and Ker, 1990) and in vivo testing using impact and ballistic pendulum approaches (Kinoshita et al., 1993; Aerts and De Clercq, 1993), to date, research specifically directed toward evaluating the viscoelastic properties of the heel pad in plantar heel pain during the dynamics of gait is lacking. Promising early work in which fluoroscopy (cine-radiography) was used to evaluate the in vivo compressive strain of the heel pad during running (De Clercq et al., 1994), has been recently expanded to include simultaneous measures of the contact pressure beneath the foot during gait (Gefen et al., 2001). By incorporating measures of heel contact stress, the modified technique affords the ability to estimate geometrically-independent, material properties of the heel pad under the dynamic conditions of gait, thus overcoming the limitations of many of the previous techniques. The aim of the current investigation, therefore, was to employ a digital fluoroscope integrated with a capacitance mat transducer system to estimate the bulk compressive properties of heel pad in individuals with and without unilateral plantar heel pain while walking at their preferred speed.
2. Methods 2.1. Subjects Nine subjects (3 male and 6 female) with unilateral plantar heel pain (age, 48 ± 13 yrs; height, 1.68 ± 0.11 m; weight, 81.6 ± 10.7 kg) and nine asymptomatic control subjects, individually matched for age, sex and body weight (age, 46 ± 12 yrs; height, 1.67 ± 0.11 m; weight, 80.1 ± 10.4 kg) participated in the study. Subjects with heel pain presented to a university foot and ankle clinic with focal tenderness localised to the calcaneal insertion of the plantar fascia, which was exacerbated with weight-bearing following periods of unloaded rest. Subjects were excluded if they presented with diffuse or bilateral pain, evidence of inflammatory arthropathy or a history of trauma or foot surgery. The mean duration of heel pain was 9 ± 6 months, with the average ‘first step’ pain rated as 4 ± 2 cm on a standard 10-cm visual analogue pain scale. All subjects gave written informed consent prior to participation in the study, which received approval from the institutional review board. 2.2. Equipment Dynamic lateral radiographs of each foot were acquired using a C-Vision multifunction fluoroscopy unit (Shimadzu, Kyoto, Japan) configured with a 405 mm four-field image intensifier. Radiographs were acquired at an exposure equivalent to 1.2 mA s 1 and an intensity of 50 kV. The imaging system incorporated a single 1024 1024 pixel array CCD camera with a sampling rate of
15 Hz. Spatial distortion within the fluoroscopic field of view was corrected using a rectilinear calibration grid (32 32 cm) positioned within the object plane and perpendicular to the central ray (Wearing et al., 2005), in combination with a previously outlined distortion correction procedure (Baltzopoulos, 1995). The RMS error for repeated linear measures of a calibration foot phantom using this method is 0.1 mm (Wearing et al., 2005). An EMED-SF capacitance mat transducer system (Novel GmbH, Munich, Germany), mounted within the field of view was used to simultaneously record pressure and temporal data at a sampling rate of 50 Hz. The 23 34-cm platform had a matrix of 2736 sensors, with an effective spatial resolution of four sensors per cm2. 2.3. Procedures Data collection was preceded by a familiarisation period in which the starting position of each subject was iteratively modified to ensure placement of the foot within the field of view, without obvious gait adjustments or targeting. Barefoot pressure and fluoroscopic data were collected following a preamble of at least three steps, while subjects walked at a self-selected speed. Walking speed was not monitored. Rather, consistency between trials was ensured by monitoring the stance phase duration of each footstep; which differed by less than 5% between trials. Trials were omitted if footsteps did not fall entirely within the boundaries of the fluoroscopic field of view, or if the investigators observed gait adjustments secondary to visual targeting of the platform. Three trials were recorded for each limb. 2.4. Data analysis Fluoroscopic images were post-processed using Matlab software (MathWorks Inc, Natick, Massachusetts, USA). Following the application of a global distortion correction procedure (Baltzopoulos, 1995; Wearing et al., 2005), convolution and edge detection algorithms were used to enhance the bone–soft-tissue interface. The inferior aspect of the lateral projection of the calcaneus and fifth metatarsal head were manually digitized from initial heel contact to the onset of heel lift. The foot–ground contact angle, defined as the axis intersecting the plantar surface of the metatarsal head and the calcaneal tuberosity relative to the support surface, was subsequently calculated. The sagittal thickness and deformation of the heel pad throughout the contact and midstance phase was calculated as the minimum gap between the inferior aspect of the calcaneus and the support surface (Fig. 1). Maximum sagittal deformation of the heel pad was used to calculate the loaded heel pad thickness (LHPT), while the unloaded thickness of the heel pad (ULHPT) was measured immediately prior to initial contact and provided the reference value for the computation of true compressive strain. True compressive strain was calculated as the ratio of deformation of the heel pad relative to the instantaneous heel pad thickness. For the purposes of the current study, compression is reflected by positive stress and strain values. Pressure data were analysed using proprietary software (Novel GmbH, Munich, Germany). The stance phase duration for the entire foot and temporal and peak pressure data beneath the heel, including the force–time integral, were calculated using a standardised masking procedure, in which the length of the footprint, excluding the toes, was divided into equal thirds. The initial stress rate during heel loading was determined by calculating the slope of the linear section of the peak pressure–time loading curve using a linear regression approach. Peak pressure data were subsequently resampled to 15 Hz to match strain data and employed as a measure of true compressive stress. Stress–strain data for each subject were interpolated using a cubic spline procedure and peak compressive stress and strain values
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S.C. Wearing et al. / Clinical Biomechanics 24 (2009) 397–402 Table 1 Mean (SD) principal gait parameters.
n Stance phase duration (ms) Foot–ground contact angle (°) Onset of heel lift (% stance phase duration) Peak stress (kPa) Instant of peak stress (% heel contact time) Stress rate during heel loading (kPa s
1
Force–time integral beneath heel (N s)
)
Control
Heel pain
9 921 (82) 12.9 (2.3) 58 (7) 246 (41) 32 (4) 1193 (125) 147 (37)
9 991 (128) 12.1 (3.0) 61 (10) 244 (22) 30 (5) 1242 (326) 158 (62)
Note: No statistically significant difference between groups (P > .05).
Fig. 1. A representative fluoroscopic image of the posterior aspect of the calcaneus and enveloping soft tissue during the stance phase of walking. Note the rectilinear array of calibration markers placed in the field of view used to correct for image distortion and as a reference of known distance to the support surface allow the thickness (t) of the heel pad relative to the support surface to be calculated.
created irregular stress–strain curves. The ensemble stress–strain curve for subjects with and without heel pain is shown in Fig. 3. No statistically significant differences were observed in the loaded and unloaded thickness, peak strain or secant modulus of heel pad in individuals with and without heel pain (Table 2). However, the heel pad was characterised by a significantly lower EDR (20%) in plantar heel pain when compared to healthy counterparts (P < .05). 4. Discussion
were calculated. The secant modulus was defined as the stress– strain ratio at the point of peak stress, while the tangent modulus was calculated over 50% of the loading curve using a linear regression approach in which the least square error was minimised. The area beneath each loading and unloading curve was estimated by numerical integration based on the trapezoid rule and the difference represented the area of the hysteretic loop. The energy dissipation ratio (EDR) was calculated as the area of the hysteretic loop relative to the area under the loading curve. 2.5. Statistical analysis The Statistical Package for the Social Sciences (SPSS Inc, Chicago, IL, USA) was used for all statistical procedures. Kolmogorov–Smirnov tests were used to evaluate data for underlying assumptions of normality. Since all outcome variables were normally distributed, means and standard deviations have been used as summary statistics. Differences in each of the dependent variables of interest (stance phase duration, ULHPT, LHPT, peak stress, peak strain, secant and tangent modulii and the EDR) were assessed using paired t-tests. An alpha level of 0.05 was used for all tests of significance. 3. Results There was no statistically significant difference in the mean stance phase duration between symptomatic and control limbs (P > .05). Similarly, there was no significant difference in the initial foot–ground contact angle between symptomatic and control limbs (P > .05). The duration of loading beneath the heel was comparable across groups, with no significant difference in the onset of heel lift observed in symptomatic and control heels (P > .05). No statistically significant differences were noted in the average stress rate during heel loading, the peak stress, time to peak stress and the force–time integral (impulse) beneath the heel between heel pain and control groups (Table 1). Real in vivo transient loading profiles associated with walking induced rapidly changing strain rates in the heel pad (Fig. 2) and
Absolute deformation of the fat pad in the current investigation was similar to that reported during barefoot running (9 ± 0.5 mm) and approximately twice that reported for shod running (De Clercq et al., 1994). The tangent modulus is comparable to those obtained from in vitro tests on excised plantar soft tissues following quasilinear statistical modelling of triangular wave stress–strain data (Ledoux and Blevins, 2007). The energy dissipated by heel pads in the current investigation (0.55 and 0.69), however, was greater than that reported for cyclic loading in cadaveric specimens (0.29–0.37) (Aerts et al., 1995; Ker, 1996; Ledoux and Blevins, 2007) and for previous in vivo measures of asymptomatic heels (0.24–0.40) using sonograph based quasi-static loading methods (Hsu et al., 1998; Tsai et al., 2000). While the energy dissipation ratios are lower than mean values reported for impact tests (0.73– 0.78) performed on healthy young adults and the elderly in vivo (Kinoshita et al., 1993), they fall between those reported for impact tests on isolated heel pads in vitro (0.65–0.86) and for ‘first loop’ energy loss values (0.39–0.67) reported for isolated cadaveric heels (Aerts et al., 1995; Ker, 1996). While methodological differences hamper cross-study comparisons, the energy dissipation ratio of heel pads in the current study is approximately 3-fold greater than those cited by Gefen et al. (2001) in which a similar fluoroscopic technique was employed (0.18). Although the latter study was restricted by low subject numbers (n = 2), peak stress values reported for the heel (60– 70 kPa) were substantially lower (3–4 fold) than those of the current and previous studies in which peak plantar pressures for the heel were recorded during barefoot walking (Cavanagh et al., 1997). The kinetic energy dissipated at heel strike largely depends on the contact velocity of the heel and effective mass of the lower limb (De Clercq et al., 1994). While the present study did not monitor the knee contact angle, it is possible that individuals with heel pain may have adopted a less energetic gait pattern, thereby reducing the energy damping requirement of the heel fat pad. However, we observed no significant difference in the average foot–ground
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Fig. 2. Ensemble average strain rate of the heel fat pad as a function of heel contact duration in subjects with unilateral plantar heel pain (n = 9) and individually matched control subjects (n = 9). Fine solid and dashed lines represent standard deviations for control and symptomatic heel pads, respectively.
contact angle, stance duration, or onset of heel lift between control and heel pain groups, suggesting subjects with heel pain adopted a similar foot roll-over pattern. Moreover, we observed no significant difference in the peak stress, time to peak stress or average initial stress rate during heel loading, suggesting that initial contact conditions between heel pain and control groups were comparable.
In the absence of demonstrable fluid flow between the compartments of the fat pad, Ker (1999) proposed that, the heel functions as a hydrostat, in which adipocytes act as a fluid of fixed volume, confined within connective tissue walls that distort with weightbearing. On the basis that changes in the apparent consistency of fat had little effect on the strain behaviour of the heel pad when
Fig. 3. Ensemble stress–strain curves for the heel fat pad in subjects with unilateral plantar heel pain (n = 9) and individually matched control subjects (n = 9). Arrows indicate direction of loading and unloading.
S.C. Wearing et al. / Clinical Biomechanics 24 (2009) 397–402 Table 2 Mean (SD) principal viscoelastic parameters of the heel pad.
n ULHPT (mm) LHPT (mm) Peak strain Tangent modulus (kPa) Secant modulus (kPa) EDR
Control
Heel pain
9 19.1 (1.9) 8.8 (1.5) 0.43 (0.05) 637 (124) 580 (145) 0.69 (0.08)
9 19.3 (1.7) 10.0 (2.1) 0.39 (0.09) 600 (81) 647 (128) 0.55a (0.17)
ULHPT: Unloaded heel pad thickness. LHPT: Minimum heel pad thickness during gait. EDR: Energy dissipation ratio. a Indicates statistically significant difference between groups (P < .05).
tested in vitro (Bennett and Ker, 1990; Ker, 1996), the mechanical properties of the heel pad were proposed to reflect those of the septal wall, which is composed of relatively inelastic collagen fibres surrounding a central core of highly deformable fibres that incorporate elastin (Buschmann et al., 1995). While the relationship between the structural components and viscoelastic properties of collagen rich tissue is complex, the finding that the heel pad had a reduced energy dissipation ratio in plantar heel pain suggests it behaves as a more elastic solid. The elastic mechanical responses of collagen, as well as the energy dissipation from proteoglycan–collagen and proteoglycan–proteoglycan interactions, are known to be influenced by the abundance and size of proteoglycans, the degree to which they form stable aggregates, and the integrity of the surrounding collagen network (Elliott et al., 2003). Thus, the reduction in the energy dissipation ratio of the heel pad in plantar heel pain may arise from a lower content, quality or aggregation state of proteoglycan or a relative increase in collagen organisation and cross-linking. While there is experimental evidence that degenerative change of the heel pad is characterised by a loss of water content (Kuhns, 1949), an increase in collagen organisation and cross-linking would, however, also increase the stiffness (elastic modulus) of the tissue, which was not observed in the current study. Similar reductions in viscosity, albeit with a concomitant rise in elastic modulus, have been reported in ovine cartilage exposed to elevated levels of nitric oxide (Cake et al., 2003), in rodent skin exposed to prednisilone acetate (Vogel, 1993) and more recently in a disuse model of rodent tendon (Eliasson et al., 2007). Irrespective of the underlying mechanism, reduced energy dissipation of the heel pad may increase the risk of fatigue and microinjury at sites of local stress concentration within the heel, and thus either initiate or exacerbate the condition. As with all crosssectional research, however, the current study cannot establish potential cause-and-effect relationships between plantar heel pain and reduced energy dissipation of the heel pad. It is unknown, therefore, whether plantar heel pain results in altered properties of the heel fat pad, or whether reduced energy dissipation of the heel pad contributes to the development of plantar heel pain. The present study employed fluoroscopy to evaluate deformation of the heel pad. Fluoroscopy is a transmission technique that creates two-dimensional (2-D) projections of what is undoubtedly a three-dimensional (3-D) deformation. The findings, therefore, are only applicable to the sagittal plane compressive properties of the heel pad. In addition, compression of the heel pad was viewed as an extension of Hertzian contact, in which the peak stress and
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strain were assumed to coincide with the point of contact between an homogenous elastic half space and a spherical calcaneal surface. Support for such an idealisation is provided by evidence that the properties of the heel pad are likely isotropic in nature (MillerYoung et al., 2002), and that the magnitude of tangential stress components of the heel are <10% of the peak vertical stress during barefoot walking (Lebar et al., 1996). A further limitation of the current study was that the temporal resolution of the imaging system resulted in a relatively low sampling rate (15 Hz) compared to modern motion analysis systems. Although theoretically sufficient to capture the majority of skeletal movements in gait, in which frequencies up to 5 or 6 Hz are typically reported (Winter et al., 1974), the method is not suitable for evaluating the specific response of the heel pad to impulsive transients associated with heel strike, in which frequencies as high as 100 Hz have been recorded (Simon et al., 1981). In addition, fluoroscopic imaging produces relatively low contrast between different types of soft tissue structures (Fig. 1). Hence, the technique does not permit the contribution of various internal structures, such as the superficial microchamber or the deep macrochamber (Hsu et al., 2007), to the bulk compressive behaviour of the heel pad to be ascertained. 5. Conclusions The findings of the present investigation indicate that plantar heel pain is associated with altered viscoelastic behaviour of the heel pad, which is characterised by a reduced energy dissipation ratio during walking when measured in vivo and under free living conditions. Acknowledgement The authors received no financial support for the preparation of this manuscript and have no competing interests that are directly related to its contents. References Aerts, P., De Clercq, D., 1993. Deformation characteristics of the heel region of the shod foot during a simulated heel strike: the effect of varying midsole hardness. J. Sports. Sci. 11, 449–461. Aerts, P., Ker, R.F., De Clercq, D., et al., 1995. The mechanical properties of the human heel pad: a paradox resolved. J. Biomech. 28, 1299–1308. Aerts, P., Ker, R.F., De Clercq, D., et al., 1996. The effects of isolation on the mechanics of the human heel pad. J. Anat. 188, 417–423. Baltzopoulos, V., 1995. A videofluoroscopy method for optical distortion correction and measurement of knee–joint kinematics. Clin. Biomech. 10, 85–92. Benjamin, M., Moriggl, B., Brenner, E., et al., 2004. The ‘‘enthesis organ” concept: why enthesopathies may not present as focal insertional disorders? Arthritis Rheum. 50, 3306–3313. Bennett, M.B., Ker, R.F., 1990. The mechanical properties of the human subcalcaneal fat pad in compression. J. Anat. 171, 131–138. Buschmann, W.R., Jahss, M.H., Kummer, F., et al., 1995. Histology and histomorphometric analysis of the normal and atrophic heel fat pad. Foot Ankle Int. 16, 254–258. Cake, M.A., Appleyard, R.C., Read, R.A., et al., 2003. Topical administration of the nitric oxide donor glyceryl trinitrate modifies the structural and biomechanical properties of ovine articular cartilage. Osteoarthritis Cartilage 11, 872–878. Cavanagh, P., Morag, E., Boulton, A.J.M., et al., 1997. The relationship of static foot structure to dynamic foot function. J. Biomech. 30, 243–250. De Clercq, D., Aerts, P., Kunnen, M., 1994. The mechanical characteristics of the human heel pad during foot strike in running: an in vivo cineradiographic study. J. Biomech. 27, 1213–1222. Eliasson, P., Fahlgren, A., Pasternak, B., et al., 2007. Unloaded rat Achilles tendons continue to grow, but lose viscoelasticity. J. Appl. Physiol. 103, 459–463. Elliott, D.M., Robinson, P.S., Gimbel, J.A., et al., 2003. Effect of altered matrix proteins on quasilinear viscoelastic properties in transgenic mouse tail tendons. Ann. Biomed. Eng. 31, 599–605. Gefen, A., Megido-Ravid, M., Itzchak, Y., 2001. In vivo biomechanical behavior of the human heel pad during the stance phase of gait. J. Biomech. 34, 1661–1665. Grasel, R.P., Schweitzer, M.E., Kovalovich, A.M., et al., 1999. MR imaging of plantar fasciitis: edema, tears, and occult marrow abnormalities correlated with outcome. Am. J. Roentgenol. 173, 699–701.
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