JCLB-03794; No of Pages 6 Clinical Biomechanics xxx (2014) xxx–xxx

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Obese children experience higher plantar pressure and lower foot sensitivity than non-obese Emmanuel Souza da Rocha a, Denise Tiane Klein Bratz a, Larissa Colaço Gubert a, Ana de David b, Felipe P Carpes a,⁎ a b

Laboratory of Neuromechanics, Federal University of Pampa, Uruguaiana, RS, Brazil Laboratory of Biomechanics, University of Brasilia, Brasília, DF, Brazil

a r t i c l e

i n f o

Article history: Received 23 December 2013 Accepted 20 May 2014 Available online xxxx Keywords: Obesity Kinetics Posture Biomechanics Body mass index Correlating factors

a b s t r a c t Background: Children obesity is a risk factor for several dysfunctions and diseases, with negative effects on the morphology of the locomotor system, plantar pressure and body stability. A relationship between postural control and sensorimotor information has been assumed. However, there is few data on the effects of children obesity on the availability of sensorial information from the foot during standing. Methods: Twenty obese and twenty non-obese children were evaluated for foot sensitivity and plantar pressure during unipedal and bipedal stance. Data were compared between obese and non-obese participants, between foot regions and between legs. Findings: Obese children experiences higher plantar pressure and have lower foot sensitivity than non-obese. Additionally, obese children had similar sensitivity for different foot regions, as compared to the non-obese. Interpretation: Children obesity negatively influences foot sensitivity. Bipedal stance seemed more sensitive to differentiate between obese and non-obese. Higher plantar pressure and lower foot sensitivity in obese children may affect performance of weight bearing activities, contribute to higher risk of foot injuries and have potential implication for children footwear design and clinical physical examination. © 2014 Elsevier Ltd. All rights reserved.

1. Introduction Obesity is defined by a high percentage of body weight associated with adipose tissue deposit (Krebs et al., 2007). It affects several physiological systems leading to higher chance of premature death (Flegal et al., 2005). Childhood obesity increases mortality rates during adulthood (Whitlock et al., 2005), and an obese child has higher probabilities to become an obese adult (Krebs et al., 2007). Additionally, childhood obesity has negative effects on the anthropometric structure of the prepubescent foot (Morrison et al., 2007), most likely due to the continuous loading due to excessive mass (Adoracion Villarroya et al., 2008). The foot is a functional unit of human body with fundamental role for balance (Humphrey and Hemami, 2010; Zhang and Li, 2013) and locomotion (Arnold et al. 2014; Bosch and Rosenbaum, 2010; Zhang and Li, 2013). Additionally, foot works for attenuation of impact forces (Whittle, 1999) and stability (Humphrey and Hemami, 2010) as well provides important sensorial information for balance and gait (Zhang and Li, 2013). The sensorimotor system uses information from receptors in the ligaments of foot arches, joint capsules, intrinsic muscles and cutaneous mechanoreceptors in the plantar surface to regulate motor ⁎ Corresponding author at: Laboratory of Neuromechanics, Federal University of Pampa, BR 472 km 592, PO Box 118, Uruguaiana, RS 97500-970, Brazil. E-mail address: [email protected] (F.P. Carpes).

actions (Wright et al., 2012). However, there are conditions that impair the use of such information and can negatively influence the sensorimotor organization. Obesity influences plantar pressure distribution (Dowling et al., 2004; Gravante et al., 2003; Mickle et al., 2006; Phethean and Nester, 2012). In non-obese children aged 4 to 7 years, body mass or body mass index was not a factor of influence on plantar pressure under different foot regions (Phethean and Nester, 2012). However, among obese children, the proportional relationship between the development of musculoskeletal system and the increase of body mass is impaired. It leads to significant higher loading in soft tissues in the foot and increase chances of stress fractures and skin ulcerations due to increased pressures on small bones (Dowling et al., 2004). The changes in foot contact area (Gravante et al., 2003; Phethean and Nester, 2012) may also affect availability of sensorial information to the central nervous system (Gravante et al., 2003; Phethean and Nester, 2012; Teasdale et al., 2007). Together, these adaptations can influence foot biomechanics function (Shultz et al., 2012). The higher plantar pressure experienced by obese children (Dowling et al., 2004; Mickle et al., 2006; Phethean and Nester, 2012) apparently happens for both girls and boys (Phethean and Nester, 2012). Several studies addressed the anatomical (Shultz et al., 2012) and postural (D'Hondt et al., 2008) adaptation in obese children feet, concluding that pes planus and fallen arch are the more common (Shultz et al.,

http://dx.doi.org/10.1016/j.clinbiomech.2014.05.006 0268-0033/© 2014 Elsevier Ltd. All rights reserved.

Please cite this article as: da Rocha, E.S., et al., Obese children experience higher plantar pressure and lower foot sensitivity than non-obese, Clin. Biomech. (2014), http://dx.doi.org/10.1016/j.clinbiomech.2014.05.006

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E.S. da Rocha et al. / Clinical Biomechanics xxx (2014) xxx–xxx

2012). The higher compression and impact experienced by obese children may have implications for sensorimotor function as elicited by altered foot sensitivity. Of note, no previous studies aimed at quantifying plantar pressure and foot sensitivity for different foot regions in obese children. The goal of our study was to evaluate foot sensitivity and plantar pressure in obese and non-obese able-bodied children during unipedal and bipedal stance. We discuss the altered foot sensitivity and plantar pressure observed among obese children as playing a key role for adaptation in the foot anatomy such as the fallen arch and flat feet. 2. Methods 2.1. Participants Forty children participated in this research. According to their individual body mass index (BMI) (Conde and Monteiro, 2006), twenty children (13 female) were assigned to the obese group [mean (standard deviation) age 9.05 (1.20) years old; body mass 41.07 (7.41) kg; height 1.41 (0.09) m; BMI 20.67 (1.78) kg/m2] and twenty children (10 female) composed the non-obese group [mean (standard deviation) age 8.80 (1.36) years old; body mass 29.85 (7.90) kg; height 1.34 (0.11) m; BMI 16.27 (1.61) kg/m2]. A consent form approved by the institutional ethics committee (IRB #0062009) was signed by the parents or the legal guardian responsible of each child. Exclusion criteria involved presence of any musculoskeletal or neurologic alteration, lesion of lower limbs, use of correctives lenses, controlled medication or any impossibility to complete the trials. 2.2. Study design Children had leg preference and foot sensitivity assessed before completing unipedal and bipedal trials of upright quiet standing with eyes open while plantar pressure under each foot was recorded. Data were averaged for 3 trials completed for each stance condition and then compared between legs, groups and foot regions. All tests were performed in one day, always in the afternoon period. 2.3. Body mass and BMI determination Body mass was evaluated using a digital body mass scale (Welmy Co.) with resolution of 100 g. For all the anthropometric, sensitivity and plantar pressure measurements the participants were barefoot. The BMI was computed according to age (Conde and Monteiro, 2006). Children were included in the obese group if BMI presented between 20.10 kg/m2 and 24.89 kg/m2.

filaments and producing a standardized pressure force to the skin surface (Semmes–Weinstein monofilaments consider six values between 0.05 gf and 300 gf) according to the manufacturer calibration and recommendation for use (Holewski et al., 1988). Participants were tested while resting in a supine position in a quiet, distraction-free environment. They were blindfolded in order to avoid participants to observe their feet or probes during testing (Breger, 1987; Holewski et al., 1988; Nurse and Nigg, 1999). All children were assessed by the same experimenter. The first foot tested was alternated between the participants to avoid any leg effect. The filaments were pressed onto the plantar surface at nine specific sites of both feet (Fig. 1a). Tactile threshold was determined by applying thinner filaments until the subject could not be able to detect touch (Breger, 1987). The average sensitivity was computed for whole foot, forefoot, midfoot and rearfoot based on the gram-force values attributed for each filament (Fig. 1c and Table 1), which means that the higher the value in the filament testing, the worse is the sensitivity. 2.5. Plantar pressure measurement Plantar pressure for obese and non-obese participants was recorded at sampling rate of 100 Hz during barefoot unipedal and bipedal stance using a portable plantar pressure map system (Matscan, Tekscan Inc., Boston, USA) (Zammit et al., 2010). For each condition, three trials lasting 30 s with 30 s interval were performed and average values were computed. Participants placed their feet on the mat keeping their arms resting beside the body (Kellis, 2001). For unipedal condition, the contralateral limb was sustained with knee in flexion and therefore not in touch with any surface during the trials. Trials were performed with eyes open and conditions were randomized. The mean plantar pressure was computed considering the foot divided in forefoot, midfoot and rearfoot (Burns et al., 2005). 2.6. Statistical analysis Data normality was checked using Shapiro–Wilk test. Data from unipedal stance were compared between groups using the Mann– Whitney U test and between feet regions using the Friedman and Wilcoxon tests, and asymmetries were verified by the Wilcoxon test. Data from bipedal stance were compared between groups using an independent t-test and between feet regions using a one-way ANOVA with Bonferroni post hoc test, and asymmetries were tested using paired t-tests. An a priori significance level was set at 0.05 for all statistical procedures. 3. Results 3.1. Anthropometric and sensitivity results

2.4. Leg preference and foot sensitivity Leg preference was verified using the revised version of the Waterloo Inventory (Elias et al., 1998). Foot sensitivity was quantified using Semmes–Weinstein pressure aesthesiometry (Semmes–Weinstein Monofilaments, San Jose, USA) (Patel, 2011). The aesthesiometer comprised 6 nylon filaments of different colors (Table 1) and equal length (35 mm). Assessment was accomplished by varying diameter of the

Body mass and BMI were higher in the obese group (p b 0.001), while the groups were paired for age (p = 0.460) and height (p = 0.051). Foot sensitivity was similar between preferred and non-preferred foot in obese [whole foot (p = 0.727), forefoot (p = 0.732), midfoot (p = 0.147) and rearfoot (p = 0,931)] and non-obese participants [whole foot (p = 0.408), forefoot (p = 0.331), midfoot (p = 0.474) and rearfoot (p = 1.000)].

Table 1 Characteristics of the filament and respective clinical meanings are presented according to manufacturer information. mN = millinewtons; gf = gram-force; N = Newton. Filaments

What means

Green (0.05 gf or 0.49 mN) Blue (0.2 gf or 1.96 mN) Violet (2.0 gf or 19.6 mN) Red (4.0 gf or 39.2 mN) Orange (10.0 gf or 98.1 mN) Pink (300 gf or 2.94 N) No answer

Normal sensitivity to the hand and foot Decreased sensation for hand, with difficulty as fine discrimination; still within the “normal” to the foot Protective sensation diminished, leaving enough to prevent injuries; difficulty to discriminate shape and temperature Loss of protective sensation to the hand, and sometimes to the foot; vulnerable to injuries; loss of discrimination for temperature Loss of protective sensation to the foot, and may still feel deep pressure and pain Sensitivity to deep pressure maintained and can still feel pain Loss of sensitivity to deep pressure usually cannot feel pain

Please cite this article as: da Rocha, E.S., et al., Obese children experience higher plantar pressure and lower foot sensitivity than non-obese, Clin. Biomech. (2014), http://dx.doi.org/10.1016/j.clinbiomech.2014.05.006

E.S. da Rocha et al. / Clinical Biomechanics xxx (2014) xxx–xxx

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Fig. 1. (a) The nine specific sites in the foot tested for foot sensitivity; (b) illustration of the Semmes–Weinstein monofilaments; (c) determination of foot regions for further analyses: forefoot (50%), midfoot (19%) and rearfoot (31%) (Burns et al., 2005). Whole foot analyses involved the full contact of foot with the surface.

An effect of obesity was observed for foot sensitivity. Obese participants presented lower foot sensitivity at whole foot and midfoot compared to the non-obese. Additionally, the comparison of sensitivity among foot regions in obese children indicated hardly any effect of foot region on foot sensitivity, whereas non-obese participants presented differences in sensitivity between the foot regions (Table 2). 3.2. Plantar pressure—unipedal stance The mean plantar pressure of obese participants during unipedal stance was similar between preferred and non-preferred foot considering the whole foot area (p = 0.493), forefoot (p = 0.329), midfoot (p = 0.858) and rearfoot (p = 0.092). Non-obese participants showed asymmetric plantar pressure considering the average pressure for whole foot area (p = 0.001) and symmetric plantar pressure in the forefoot (p = 0.092), midfoot (p = 0.250) and rearfoot (p = 0.379). Obese participants had higher pressure for all foot regions when compared with non-obese, and the highest pressure was observed in the rearfoot (Fig. 2 and Table 3). Additionally, plantar pressure for obese participants differed between all foot regions (Fig. 2 and Table 3). Among non-obese children, pressure on forefoot was similar to the midfoot, and both regions were different from rearfoot (Fig. 2 and Table 3).

(p = 0.471). When groups were compared in the bipedal stance (Fig. 3), preferred and non-preferred legs were analyzed apart. In the preferred leg, plantar pressure in the whole foot (p = 0.352) and rearfoot (p = 0.249) were similar between the groups, but obese children presented higher plantar pressure in the forefoot (p b 0.01) and midfoot (p b 0.01). Considering the non-preferred leg, plantar pressure was higher in the obese children for whole foot and all foot regions (p b 0.01). Finally, comparing the foot regions within the groups, plantar pressure differed between all regions in the obese group for both the feet (p b 0.01; Table 4 and Fig. 3). In the non-obese, all regions differed significantly, except by the comparison between forefoot and

3.3. Plantar pressure—bipedal stance During bipedal stance (Fig. 3), obese children presented asymmetry in the plantar pressure for whole foot (p b 0.01) and rearfoot (p b 0.01). In the forefoot (p = 0.412) and midfoot (p = 0.630), plantar pressure was symmetric. As observed among obese children, the non-obese group presented asymmetry in the plantar pressure in the whole foot (p b 0.01). Non-obese had asymmetry in the forefoot (p b 0.01), while symmetry was observed in the midfoot (p = 0.418) and rearfoot

Table 2 Sensitivity scores (averaged for foot regions) and p-values found in the comparison of foot sensitivity between groups and between foot regions within the groups. gf = gram-force. Foot region

Obese (gf)

Non-obese (gf)

p-value between groups

Whole foot Forefoot Midfoot Rearfoot p-value between regions

0.380 0.337 0.346 0.703 0.378

0.228 0.261 0.080 0.328 0.008†

0.007⁎ 0.130 0.003⁎ 0.194

⁎ Statistical difference between groups (Mann–Whitney U test). † Statistical difference between foot regions (Friedman and Wilcoxon tests).

Fig. 2. Mean and standard deviation plantar pressure values (N/cm2) for the whole foot and different foot regions during the unipedal stance. In the top, comparison between the groups, with * indicating differences between the groups in the different foot regions (p b 0.05). In the bottom, considering each group, *, **, *** and **** indicate statistical difference (p b 0.05) between the foot regions within each group.

Please cite this article as: da Rocha, E.S., et al., Obese children experience higher plantar pressure and lower foot sensitivity than non-obese, Clin. Biomech. (2014), http://dx.doi.org/10.1016/j.clinbiomech.2014.05.006

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Table 3 Statistical outcomes found for comparison of plantar pressure between foot regions within each group during unipedal stance. Foot region comparison Whole foot

Forefoot

Midfoot

Rearfoot

Forefoot Midfoot Rearfoot Whole foot Midfoot Rearfoot Whole foot Forefoot Rearfoot Whole foot Forefoot Midfoot

Obese

Non-obese

b0.001⁎ b0.001⁎ b0.001⁎ b0.001⁎ b0.001⁎ b0.001⁎ b0.001⁎ b0.001⁎ b0.001⁎ b0.001⁎ b0.001⁎ b0.001⁎

b0.001⁎ b0.001⁎ b0.001⁎ b0.001⁎ 0.528 b0.001⁎ b0.001⁎ 0.528 b0.001⁎ b0.001⁎ b0.001⁎ b0.001⁎

⁎ Statistical significance for both the feet (p b 0.05).

whole foot in the non-preferred leg (Table 4 and Fig. 3). Descriptive data of plantar pressure in the different conditions and foot regions are presented in the supplemental file 1. 4. Discussion The foot can be considered a functional unit providing support to the body weight and playing important role for attenuation of impact forces during locomotion (Whittle, 1999). Receptors in the ligaments, foot arches, joint capsules, intrinsic muscles and cutaneous mechanoreceptors from plantar surface provide the central nervous system with information that helps to control body position control during upright position (Wright et al., 2012). Such sensorial information is an important component of motor control for a range of daily activities as well as during physical exercise. Obese children are frequently requested to get involved in physical exercise programs as an attempt to reduce body weight and therefore to decrease individual body mass index.

However, alterations in the foot function may commit the physical exercise performance by increase of pain, discomforts and risk of injuries in the lower extremity. In this study, we compared foot sensitivity and plantar pressure between obese and non-obese children in attempt to identify the effects of obesity on foot sensorimotor function. We found increased plantar pressure and lower foot sensitivity in the obese children. The higher mechanical loading on the foot associated with lower sensitivity may account as a risk factor for foot injuries in the obese children (Dowling et al., 2004; Shultz et al., 2010). It suggests foot sensitivity should be included as a component of physical exam in the obese children. While foot sensitivity was similar between preferred and nonpreferred foot, there were differences in the sensitivity between foot regions in the non-obese children. Considering plantar pressure in the unipedal stance, which we used to illustrate a more challenging postural task, we observed that whole foot plantar pressure was asymmetric in the non-obese children. It suggests some leg specific adaptation for weight support that was not observed among the obese children. Additionally, it is possible that control of standing position in the non-obese children is not a challenging task as for obese and therefore non-obese children are able to successfully stand relying more on one leg. Previous studies did not find differences in plantar pressure when comparing right and left foot in the children, independent of their body mass (Bosch et al., 2007; Phethean and Nester, 2012). In our study, asymmetries in plantar pressure in non-obese group were evidenced due to a larger plantar pressure for whole foot average in preferred unipedal support than non-preferred one. We also found asymmetries in plantar pressure during bipedal stance for non-obese group in the whole foot area and forefoot regions, and for obese group in whole foot and rearfoot region. The influence of leg preference for stabilization tasks such as the standing considered here is not clear, as leg preference for stabilization tasks is known to be much more variable when compared with mobilization tasks (Teixeira and Teixeira, 2008). The symmetric foot sensitivity between the feet suggests that sensorial

Fig. 3. Mean and standard deviation plantar pressure values (N/cm2) for the whole foot and different foot regions during the bipedal stance. In the top, comparison between the groups, with * indicating differences between the groups in the different foot regions (p b 0.05). In the bottom, considering each group, *, **, *** and **** indicate statistical difference (p b 0.05) between the foot regions within each group.

Please cite this article as: da Rocha, E.S., et al., Obese children experience higher plantar pressure and lower foot sensitivity than non-obese, Clin. Biomech. (2014), http://dx.doi.org/10.1016/j.clinbiomech.2014.05.006

E.S. da Rocha et al. / Clinical Biomechanics xxx (2014) xxx–xxx Table 4 Statistical outcomes found for comparison of plantar pressure between foot regions within each group during bipedal stance. Foot region comparison Whole foot

Forefoot

Midfoot

Rearfoot

Forefoot Midfoot Rearfoot Whole foot Midfoot Rearfoot Whole foot Forefoot Rearfoot Whole foot Forefoot Midfoot

Obese

Non-obese

b0.001⁎ b0.001⁎ b0.001⁎ b0.001⁎ b0.001⁎ b0.001⁎ b0.001⁎ b0.001⁎ b0.001⁎ b0.001⁎ b0.001⁎ b0.001⁎

b0.01$; 0.743# b0.001⁎ b0.001⁎ b0.01⁎; 0.743# b0.001⁎ b0.001⁎ b0.001⁎ b0.001⁎ b0.001⁎ b0.001⁎ b0.001⁎ b0.001⁎

⁎ Statistical significance for both the feet (p b 0.05). $ Statistical significance only for preferred foot (p b 0.05). # No statistical significance for non-preferred foot.

5

5. Conclusion Obesity produces an excessive load in the children foot, which is most likely similar between preferred and non-preferred foot. The higher pressure experienced by obese children seems to negatively affect foot sensitivity resulting in lower foot sensitivity for all foot regions of the obese compared to the non-obese children. Lower foot sensitivity in obese children can be considered a risk factor for a variety of injuries related to foot loading as well as during long term exercises frequently recommended for obese to control the weight and should be included in physical examination of the obese children. Acknowledgment This study was partially funded by FAPERGS (grant number 1013100) provided to FPC. Appendix A. Supplementary data

information from both feet is available to central nervous system at same extent, without influence of lateral preference. Obese children showed lower foot sensitivity than non-obese. Additionally, obese children had similar sensitivity across all foot regions, whereas non-obese children were able to discriminate touch in different intensities for the different foot regions. Former study suggested that higher sensitivity to touch is related to higher density of receptors, which declines with age (Kozłowska, 1988). Therefore, it is hypothesized that lower sensitivity in obese children might be originated, among others causes, by a lower density of receptors for surface area unit (Kozłowska, 1988). Foot sensitivity has a determinant role for balance control during postural tasks (Hohne et al., 2009) and has an important role for plantar pressure (Meyer et al., 2004). Our results suggest that obese children have a greater risk of foot injuries like stress fractures in the forefoot or skin ulcerations (Dowling et al., 2004; Shultz et al., 2010). Indeed, different foot sensitivity in the foot regions is expected as different sites of the foot have different volumes of soft tissues as well as different capacities for muscle activation modulation. When such analysis was performed in aged and adults participants, it was found that foot sensitivity was related to postural control in elderly but not in adults and in elderly foot sensitivity was impaired compared to the adults (Ueda and Carpes, 2013). Additionally, foot sensitivity in forefoot of young adults was positively related with center of pressure displacement (Ueda and Carpes, 2013). Higher plantar pressure observed among obese children may result from the higher body mass. Our results suggest that higher loading may have long-term effects on the mechanoreceptors activities resulting in lower foot sensitivity, which is not observed in children with the expected body mass for the age. As mentioned before, one reason for such losses in sensitivity can be a lower density of receptors for surface are unit (Kozłowska, 1988). Reduction in the sensitivity of plantar mechanoreceptors impairs the function of sensorimotor system (Phethean and Nester, 2012; Teasdale et al., 2007). Alterations in sensitivity can be a relevant factor to changes in the plantar pressure during upright posture (Hohne et al., 2009) and could explain differences in plantar pressure between foot regions observed in our study. Finally, obese and non-obese children showed differences in plantar pressure between foot regions, with higher pressures observed among obese participants. Rearfoot was the foot region with highest pressure for obese and non-obese group. Pressure in the midfoot was the smallest between foot regions in both groups. Such results are in agreement with previous investigations (Dowling et al., 2004; Kellis, 2001), which reinforces the relevance of our outcomes for foot sensitivity as determinants for changes in plantar pressure in the obese children.

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Please cite this article as: da Rocha, E.S., et al., Obese children experience higher plantar pressure and lower foot sensitivity than non-obese, Clin. Biomech. (2014), http://dx.doi.org/10.1016/j.clinbiomech.2014.05.006

Obese children experience higher plantar pressure and lower foot sensitivity than non-obese.

Children obesity is a risk factor for several dysfunctions and diseases, with negative effects on the morphology of the locomotor system, plantar pres...
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