Heel fat pad dynamics during loading cycles: an in-vivo study ―Effect of height and weight on heel fat pad movements between microchamber and macrochamber layers in loading and unloading cycles

doi:10.21203/rs.3.rs-2063700/v1

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Heel fat pad dynamics during loading cycles: an in-vivo study ―Effect of height and weight on heel fat pad movements between microchamber and macrochamber layers in loading and unloading cycles

https://doi.org/10.21203/rs.3.rs-2063700/v1

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Background

This study aimed to determine the effect of height and weight on heel fat pad thickness between microchamber and macrochamber layers during loading-unloading cycles.

Methods

The subjects performed loading-unloading movements, and the thickness change of the heel fat pad was measured. We examined the relationship between height and weight and the rate of change in the thickness of the microchamber and macrochamber layers of the heel fat pad when 0–100% load was applied.

Results

Significant changes were observed in the macrochamber layer. The thicknesses of the microchamber and macrochamber layers of the heel fat pad increased with increasing height and weight.

Conclusions

Function may differ between the microchamber and macrochamber layers of the heel fat pad. With increasing height and weight, the thickness of the microchamber and macrochamber layers increased, but the thickness change of the macrochamber layers decreased.

heel

heel fat pad

microchamber layer

macrochamber layer

ultrasound

The heel is the first point of contact with the ground during walking and other daily activities (heel strike), and the heel is frequently in a loaded and unloaded state. Anatomical studies have shown that pressure stress applied to the heel during ground contact can induce plantar heel pain[1, 2]. Plantar heel pain is a pain in the plantar region and occurs during walking and running. This may lead to resistance to daily activities, which may have various adverse effects on the body.

One factor associated with plantar heel pain is the presence of fatty bodies in the heel (hereafter referred to as heel fat pad). The main role of the heel fat pad is to absorb and disperse shock during walking and running. It has been suggested that degeneration or failure of the heel fat pad due to continuous pressure loading may reduce its shock absorption and dispersion functions and increase the risk of inducing plantar heel pain [3, 4]. Since function depends on tissue structure[5, 6], many studies have focused on the morphology of the heel fat pad and evaluated its function. However, reports in patients with plantar heel pain have shown that the heel fat pad is thicker during loading and unloading compared to the asymptomatic heel fat pad[7] and that the thickness does not change [8, 9]. There is currently no agreement on the relationship between heel fat pad morphology and plantar heel pain. There are also reports of functional evaluation of the heel fat pad by in vitro testing, but no certain view has been obtained, and to some extent, there are limitations in evaluating the function of soft tissues with dynamics using static indices[10]. Therefore, we believe that it is important to evaluate changes in heel fat pad loading in living subjects to clarify the function of the heel fat pad. Hsu et al. [11] explained the importance of evaluating dynamic changes in clarifying soft tissue function. They also reported that tissue behavior provides information about the tissue and suggests the presence of disease.

Studies reporting load changes in the heel fat pad have been undertaken using X-ray [12, 13], CT [14], MRI [15], and ultrasound imaging systems [16–18]. However, it has been difficult to depict the internal structures in detail. Furthermore, the heel fat pad is divided into two major layers, the microchamber layer (microchambers (MICs)) and the macrochamber layer (macrochambers (MACs)), bounded by the fibrous septum. The microchamber layer is composed of elastic fibers and the macrochamber layer is composed of collagen and elastic fibers. Since the adipose tissue morphology differs between the two layers [4, 10, 19–22], it is expected to exhibit different dynamic changes during loading. However, limited studies have focused on the functional differences between the two layers, and there have been various limitations, such as the limitation of the loading capacity (20 kg) [22], although the differences between the two layers have been focused on. To solve these problems, we developed an evaluation apparatus using polymethylpentene resin plate (PMP) [23]. The PMP device has a 5-mm polymethylpentene resin plate protecting the acoustic lens of the transducer, enabling the measurement of morphological changes in the heel fat body when full load is applied (Takiron Polymer Co., Ltd., Fukuoka, Japan). In addition, the resin plate used in this device is close to the acoustic impedance of the human body, which may enable a clear and highly accurate measurement of the internal structure.

In previous study of 1226 Japanese subjects, the thickness of the microchamber and macrochamber layers of the heel fat pad at non-weight bearing increased with increasing body weight and height [24]. This suggests that the structure of the heel fat pad may have changed as an adaptation to the increased loading caused by increased height and weight. However, it is not yet clear how function changes in response to load.

This study aimed to clarify the differences in the movement of the microchamber and macrochamber layers of the heel fat pad using an evaluation device with a PMP, and clarify the effects of height and weight on the behavior of the microchamber and macrochamber layers in healthy subjects during load-extraction movements.

2.1 Participants

A total of 21 healthy participants (twelve males and nine females) were enrolled in this study. The study was sampled by simple random sampling. Participant characteristics are described in Table 1.

In this experiment, participants were excluded if they met any of the following exclusion criteria: (1) engaging in intense physical activity or consuming alcohol in the previous 48 hours; (2) a history of foot or ankle surgery or major trauma; (3) a history of ankle or foot orthopaedic injuries such as tendinopathy, bursitis, plantar fasciitis, or ligament injuries; (4) a history of rheumatic diseases, such as osteoarthritis, gout, or rheumatoid arthritis; (5) a history of a systemic disease, such as diabetes or connective tissue disorders.

All participants received a detailed explanation of the experimental procedures and risks of the research before the recordings were taken. Written informed consent was obtained from all participants and their guardians. This study was approved by the Ethics Committee and conducted according to the principles of the Declaration of Helsinki (Approval No. 2020 − 228).

2.2 Protocol

2.2.1 Load measuring instruments

The load measuring instruments consisted of two steel quadruped frames, each 400 mm high, 350 mm long and 350 mm wide, one with a 20 mm-thick polycarbonate resin top plate on the steel frame and the other with a scale on which the load was measured. The polycarbonate resin tabletop had a cross-hole to allow the ultrasound probe to image from the bottom [23].

In a preliminary experiment measurement of fast movements such as load-extraction movements, would be difficult to observe with ultrasound using the same technique as in the previous study because the PMP and the heel would separate at the time of ground release. Therefore, we created an original water tank using the PMP to enable the measurement of fast movements such as load-unloading movements. A water tank, 90 mm high, 350 mm long, and 155 mm wide, made of 5-mm-thick PMP plates was fixed at the position cut out for the cross-hole in the top panel, and water was filled to a height of 10 mm in the tank. Since the average foot axis angle during walking is considered to be approximately 7 degrees to the sagittal plane, the two evaluation platforms were placed so that they were open 7 degrees to the sagittal plane (Fig. 1).

2.2.2 Loading-unloading movement

The right foot, used as the measurement foot, was placed in the tank so that the second metatarsal and calcaneal ridge aligned with the straight line drawn on the PMP load measuring instrument. The subjects were made to stand shoulder-width apart, and the amount of load applied to the right foot was checked based on the scale readings. To prevent the heel from floating, the subjects were placed at eye level in the standing posture and kept their eyes on the marker during the measurement.

The loading and unloading movements were performed in accordance with previous studies [22]. The subject performed the loading and unloading movements on the PMP load measuring instrument at a frequency of 0.5 Hz on a metronome. The subject started with the toes grounded to a straight line drawn on a PMP tabletop to prevent the load axis from shifting, and the movements were performed three times in succession.

2.2.3 Thickness measurement of heel fat pad using ultrasonic method

The measurements were performed by a person with more than 6 years of experience observing heel fat pads. Measurements were taken using an ultrasound imaging system (ApplioαVerifia, Canon, JPN) with a 10 MHz high-frequency linear probe with the screen inverted vertically. The macrochamber layer was defined as the area from the inferior margin of the calcaneal ridge to the base of the fibroseptum, and the microchamber layer was defined as the area from the base of the fibroseptum to the skin. The macrochamber layer included the plantar tendon membrane, MASs, and fibroseptum, while the microchamber layer included the MICs and skin.

A set of three consecutive loading-unloading movements was performed, and changes in the microchamber and macrochamber layers of the heel fat pad were continuously imaged for a total of 6 seconds. The frame rate of the ultrasound imaging system was set at 30 images/second, which allowed clear observation of the internal structure of the heel fat pad. Six-second imaging was performed because the loading-unloading movements were performed at a frequency of 0.5 Hz, which required 1 second (30 fps) for loading, 1 second (30 fps) for unloading, and 2 seconds (60 fps) for loading-unloading movement. This is because the load was performed three times.

The following three points were identified during each loading movement (60 fps): the point where the heel contacted the PMP (initial contact), the point where the heel reached maximum load (the point where the thickness of the microchamber and macrochamber layers of heel fat pad no longer changed compared to the previous value) (maximal load), and the point where the heel left the PMP plate (unloading). The differences between the microchamber and macrochamber layers were compared. We also extracted 10 images from each of the 30 images measured between initial contact and maximal load and between maximal load and unloading, each of which was a multiple of 3, and evaluated the changes in the loading-unloading processes of the microchamber and macrochamber layers of the heel fat pad for each layer. The thicknesses of the microchamber and macrochamber layers of the heel fat pad between initial contact and maximal load and between maximal load and unloading were calculated, and the (1) amount of thickness change, (2) rate of thickness change, (3) ratio of thickness change of the microchamber and macrochamber layers to the entire heel fat body were calculated (Fig. 2). The calculation formulas are as follows.

Amount of change (mic) = Initial contact (mic) – Maximal load (mic)

or Amount of change (mac) = Initial contact (mac) – Maximal load (mac)・・(1)

Rate of change (mic) = \(\frac{Amount of change \left(mic\right)}{Initial contact \left(mic\right)}\)×100

or Rate of change (mic) = \(\frac{Amount of change \left(mac\right)}{Initial contact \left(mac\right)}\)×100・・(2)

Deformation proportion×100 (mic) = \(\frac{Amount of change \left(mic\right)}{Amount of change \left(mic\right)+Amount of change \left(mac\right)}\)×100

or Deformation proportion×100 (mic) = \(\frac{Amount of change \left(mic\right)}{Amount of change \left(mic\right)+Amount of change \left(mac\right)}\)×100・・(3)

One set of three loading-unloading movements was performed, and the average of the three was used as the measured value in this study.

2.3 Statistical Analysis

Statistical analysis was performed using SPSS software (SPSS Statistics28, IBM, USA). Sample size estimation was performed for each item.

A two-way analysis of variance was performed because normality was assumed after a Shapiro-Wilk test before performing a three-point comparison in the microchamber and macrochamber layers of the heel fat pad. If the test result of the difference in measurements was significant, the Bonferroni method was performed as a posteriori test.

The Shapiro-Wilk test was performed before comparing the loading-unloading processes in the microchamber and macrochamber layers of the heel fat pad at 10% intervals, and since normality was assumed, a corresponding t-test was performed. If the test result of the difference in measurements was significant, the Bonferroni method was performed as a posteriori test.

Before comparing the thickness change of the microchamber and macrochamber layers of the heel fat pad during the loading-unloading processes, the Shapiro-Wilk test was performed, and since normality was assumed, a paired t-test was used.

Pearson's correlation coefficients were used for the association between the thickness of the microchamber and macrochamber layers of heel fat pad and height and weight and the association between the percentage change in thickness of the microchamber and macrochamber layers of heel fat pad and height and weight. Multiple regression analysis was also performed using a stepwise method. The thickness and rate of thickness change of the microchamber and macrochamber layers of the heel fat pad were used as dependent variables, and height and weight were used as independent variables. Correlation results were categorized as follows: [0.00-0.20/-0.00–0.20 (poor correlation) / 0.21–0.40/-0.21–0.40 (fair correlation) / 0.41–0.60/-0.41–0.60 (moderate correlation) / 0.61–0.80/-0.61–0.80 (good correlation)/ 0.81-1.00/-0.81–1.00 (very good correlation)]. The significance level was set at less than 5%.

Comparison between the three points in the microchamber and macrochamber layers of the heel fat pad showed significant differences between initial contact and maximal load and between maximal load and unloading in the macrochamber layer. On the other hand, there was no significant difference between the three points in the microchamber layer. In addition, significant differences were found between the microchamber and macrochamber layers at all points (Fig. 3).

In comparing the loading-unloading processes in the microchamber and macrochamber layers of the heel fat pad at 10% intervals, significant changes were observed up to 30% in the loading process in the macrochamber layer, and significant changes were observed in all stages of the unloading process. On the other hand, no significant changes were observed in the microchamber layer during the loading and unloading processes (Fig. 4).

Significant differences were observed between the microchamber and macrochamber layers of the heel fat pad during the loading-unloading processes regarding the amount of thickness change, rate of thickness change, and percentage of thickness change in the microchamber and macrochamber layers relative to the total heel fat pad (Table 2).

In terms of the relationship between the thickness of the microchamber and macrochamber layers of heel fat pad and height and weight, there was a good positive correlation in the microchamber layer for height (r = 0.711, p < .05) and a very good positive correlation for weight (r = 0.805, p < .05). At the microchamber layer, good positive correlations were found for height (r = 0.672, p < .05) and weight (r = 0.682, p < .05). Multiple regression analysis revealed a significant variable, with body weight being the larger factor (microchamber layer: R² = 0.648, p < .001) (weight: β = 0.805) (macrochamber layer: R² = 0.465, p < .001) (weight: β = 0.682) (Fig. 5).

In the relationship between the rate of change in the thickness of the microchamber and macrochamber layers of the heel fat pad and height and weight, no significant correlation was found in the microchamber layer for height (r = 0.024, p > .05) and weight (r = 0.198, p > .05). In the macrochamber layers, a fair negative correlation was found for height (r=-0.383, p < .05) and a moderate negative correlation for weight (r=-0.571, p < .05) (macrochamber layer: R² = 0.327, p < .05) (weight: β=-0.572) (Fig. 6).

This study aimed to clarify the differences in the movement of the microchamber and macrochamber layers of the heel fat pad using an evaluation device with a PMP, and then to clarify the effects of height and weight on the behavior of the microchamber and macrochamber layers in healthy subjects during load-extraction movements.

The microchamber and macrochamber layers showed most of the difference during weight bearing, with the macrochamber layer accounting for about 98% of the total heel fat pad thickness, while the microchamber layer accounted for about 2% of the total thickness. It has been reported that anatomical findings indicate that the tissue morphology differs between the microchamber and macrochamber layers of the heel fat pad, with the macrochamber layer responsible for shock absorption and the microchamber layer for controlling excessive macrochamber layer deformation [25–29]. In addition, previous studies[26, 30] that investigated changes in microchamber and macrochamber layers of the human organism when pseudo-loading or 20 kg load was applied reported that the morphological changes were more pronounced in the macrochamber layers. The present study is the first to evaluate changes in microchamber and macrochamber layers by adding all body weights. As in previous studies, the macrochamber layers changed significantly at full load, and the changes increased with the load. On the other hand, the microchamber layer did not change with increasing load.

In the relationship between the thickness of the microchamber and macrochamber layers of the heel fat pad and height and weight, the thickness of the microchamber and macrochamber layers morphologically increases with height and weight, but the rate of change of the microchamber layer thickness remains the same, while the rate of change of the macrochamber layer thickness is low. Although it is difficult to say whether this change is due to adaptation to overload or a decline in functional characteristics, the results of this study suggest that a thicker heel fat pad does not necessarily imply superior functional characteristics.

It has been reported that the heel fat pad undergoes degenerative changes due to aging [31] and lesions [30] due to diseases such as diabetes mellitus. Heel adipose bodies become thinner with age, with degeneration and destruction of elastic fibers and reduction and loss of healthy adipose tissue [32]. Plantar heel pain is particularly common in patients in their 40s to 60s [33], and it has also been shown that only the macrochamber layers of the heel fat pad become thinner after this age group. In other words, changes in the morphology of the macrochamber layers may lead to decreased shock absorption capacity and increased pressure stress, which may lead to plantar heel pain, suggesting the importance of examining the two layers separately, rather than comprehensively examining the two layers as heel fat pad. In addition, patients with plantar heel pain are expected to reach maximum deformation (= maximum loading point) early in the loading phase because of the thinning of the heel fat pad and fibrosis of the septum as indicated above. Since repeated heel contact in the thinning state may be linked to the possibility of increasing the risk of inducing plantar heel pain, we believe it is crucial to focus on the loading changes.

This study confirmed that PMP could be used to evaluate the internal structure of the heel fat pad during loading in detail. This can be further applied to various movement measurements. In particular, understanding the biomechanical behavior in daily activities, such as walking and running, is crucial to understanding various movements in the future. Moreover, although this study was conducted on healthy subjects, the actual measurement of loading-unloading movements in the heel fat pad, which has degenerated due to degenerative changes or lesions, may clarify of the relationship between plantar heel pain and the heel fat pad and the mechanism of plantar heel pain generation. Therefore, further investigation is needed based on this study.

4.1 Limitations

Since the loading-unloading operation was a continuous, it was impossible to control the adjustment of the amount of load applied. In addition, since foot pressure measurement was not performed, determining whether the load was applied to the heel or not was difficult, although it was certain that the full load was applied to the measured foot. Furthermore, the number of subjects was small; it is necessary to increase the number of subjects to obtain more reliable values. Finally, the load speed was set uniformly and was slower than the speed at which a person would normally walk, so the possibility that the change in load was different from the change in load when walking cannot be ruled out.

The results suggest that function may differ between the microchamber and macrochamber layers of the heel fat pad. In addition, with increasing height and weight, the thickness of the microchamber and macrochamber layers increased, but the thickness change of the macrochamber layer decreased. It is suggested that thickness increases with increasing load, but elasticity may decreased.

Ethics approval and consent to participate

Consent for publication

Not applicable.

Availability of data and material

Please contact author for data requests.

Competing interests

The authors declare that they have no competing interests.

Funding

This work was supported by Public Interest Incorporated Foundation Yamaha Motor Foundation for Sports.

Authors' contributions

TM was involved in the conception and design of the study, approval of the institutional review board of facilities, acquisition of data, data analysis, interpretation of data, and drafting and writing of the article. MM was involved in the conception and design of the study and revising it critically for important intellectual content. TT, SI, TO and ZL were responsible for the acquisition of data, data analysis, and interpretation of data. HT was responsible for revising the paper critically for important intellectual content. TK gave advice on all processes in preparation of the paper and was involved in the final approval of the version to be submitted. All authors read and approved the final manuscript.

Acknowledgements

The authors would like to thank all participants who participated in the measurements.

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Table 1. Physical characteristics of participants

	Age (years)		Height (cm)		Body mass (kg)		BMI (kg/m²)		Macrochamber layer thickness (mm)		Microchamber layer thickness (mm)
ALL	23.7	（1.9）	165.4	（7.1）	58.1	（8.7）	21.2	（2.0）	10.3	(1.3)	2.6	(0.3)
Male	24.6	(1.8)	170.6	(3.9)	63.4	(7.2)	21.8	(2.2)	11.0	(1.0)	2.9	(0.3)
Female	22.6	(1.4)	158.6	(3.8)	51.1	(4.4)	20.3	(1.4)	9.3	(1.0)	2.4	(0.1)

Data are shown as mean (SD)　

Abbreviation: BMI: body mass index

Table 2. Microchamber and macrochamber layer tissue properties.

	Microchamber layer		Macrochamber layer		p
*Loading cycle*
Amount of change (mm)	0.1	（0.1）	6.2	（0.9）	.001
Rate of change (%)	4.3	（2.0）	60.6	（11.1）	.001
Deformation proportion × 100 (%)	1.8	（0.8）	98.2	（0.8）	.001
*Unloading cycle*
Amount of change (mm)	0.1	(0.1)	5.2	(0.8)	.001
Rate of change (%)	4.1	(2.0)	56.6	(11.5)	.001
Deformation proportion × 100 (%)	2.1	(1.1)	97.9	(1.1)	.001

Data are shown as mean (SD)

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Heel fat pad dynamics during loading cycles: an in-vivo study ―Effect of height and weight on heel fat pad movements between microchamber and macrochamber layers in loading and unloading cycles

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Abstract

Background

Methods

Results

Conclusions

Figures

1 Introduction

2 Materials And Methods

2.1 Participants

2.2 Protocol

2.2.1 Load measuring instruments

2.2.2 Loading-unloading movement

2.2.3 Thickness measurement of heel fat pad using ultrasonic method

2.3 Statistical Analysis

3 Results

4 Discussion

4.1 Limitations

5 Conclusions

Declarations

References

tables

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