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PERSPECTIVE
Year : 2016  |  Volume : 1  |  Issue : 2  |  Page : 86-90

A new integrative approach to evaluate pathological gait: locomotor rehabilitation index


1 Exercise Research Laboratory, Escola de Educação Física, Fisioterapia e Dança, Universidade Federal do Rio Grande do Sul, Porto Alegre, Rio Grande do Sul, Brazil
2 Exercise Research Laboratory, Escola de Educação Física, Fisioterapia e Dança, Universidade Federal do Rio Grande do Sul, Porto Alegre, Rio Grande do Sul; Neurosciences and Rehabilitation Laboratory, Universidade Federal de Ciências da Saúde de Porto Alegre, Porto Alegre, Rio Grande do Sul, Brazil

Date of Web Publication7-Jul-2016

Correspondence Address:
Leonardo Alexandre Peyré-Tartaruga
Exercise Research Laboratory, Escola de Educação Física, Fisioterapia e Dança, Universidade Federal do Rio Grande do Sul, Porto Alegre, Rio Grande do Sul
Brazil
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Source of Support: This work was supported by LAPEX (No. 06/2015), CAPES, CNPq and FIPE-HCPA (No. 140051)., Conflict of Interest: None


DOI: 10.4103/2468-5658.184750

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  Abstract 

This article reviews the concept of locomotor rehabilitation index (LRI) from the principle of dynamical similarities and the theory of mechanism minimizing the energy expenditure in pathological walking. This index is defined as the percentage ratio between self-selected speed and optimum speed (algebraically LRI = 100 × self-selected speed/optimum walking speed). First, we analyze the mechanical foundations of human walking especially focusing on general size effects. Then, we discuss the descriptive physiology of pendular mechanism, evidencing the path that leads to the view of reductionist and extremely descriptive view of pathological gait. Integrative models, generated by the first evidence presented in our previous papers around the LRI, represent a crucial change of perspective. This model is discussed in details and criticized concerning the ensuing experimental findings. Finally, we discuss the case of Parkinson's disease using the Nordic walking as a neat example of application of LRI on pathological locomotion. To conclude , the concept of LRI is reinforced by the substantial evidence, showing that this new proposal for assessing the gait functionality is extremely promising and should be stimulated in studies that examine the effects of therapies on gait functionality in degenerative diseases.

Keywords: rehabilitation assessment; human walking; physical health; Parkinson′s disease


How to cite this article:
Peyré-Tartaruga LA, Monteiro EP. A new integrative approach to evaluate pathological gait: locomotor rehabilitation index. Clin Trials Degener Dis 2016;1:86-90

How to cite this URL:
Peyré-Tartaruga LA, Monteiro EP. A new integrative approach to evaluate pathological gait: locomotor rehabilitation index. Clin Trials Degener Dis [serial online] 2016 [cited 2020 Sep 28];1:86-90. Available from: http://www.clinicaltdd.com/text.asp?2016/1/2/86/184750

Acknowledgements
We are grateful to the Locomotion Group of the Federal University of Rio Grande do Sul, Brazil for discussions and comments. L.A. Peyré-Tartaruga is an established investigator of the Brazilian Research Council (CNPq), Brasília, Brazil.
Author statements
We state that the manuscript has been read and approved by all the authors, that the requirements for authorship as stated in the journal′s instruction to the authors have been met, and that each author believes that the manuscript represents honest work.



  Introduction Top


The physical impairment is one of the most prevalent age-related conditions and the primary cause of institutionalization in aging. Several studies have shown that the deteriorated gait is one of the most important physical impairments (Hennessy et al., 2015). Although crucial to evaluate the functionality of patients, the gait tests often used in clinical studies do not consider fundamental aspects of the walking performance as the size effects. Here, we propose a new approach including the lower limb length (LLL, vertical distance from the great trochanter to the ground), the self-selected walking speed (SSWS) and using model equations commonly used in the field of experimental biology. The theoretical basis for the present proposal rests (i) on the premise of the dynamical similarities principle, and (ii) on the theory of integrative mechanisms that minimize the muscle work and the metabolic cost of locomotion, particularly the pendulum-like mechanism. This perspective aims to analyze theoretical aspects and potential application of locomotor rehabilitation index (LRI) on gait rehabilitation and physical activity. Also, we will explore the mechanisms underlie the human gait mechanics, especially for physically impaired people, and the possible contributions of LRI to physical rehabilitation are shown by an example applied to Parkinson's disease (PD) individuals.


  Fundamental concepts of human walkin Top


Firstly studied by Alexander (2005), the principle of dynamic similarity is based on the premise that the optimal walking speeds of geometrically similar organisms are independent of size when speed is relativized to the dimensionless Froude number (Fr). The Fr is defined as:



where v is horizontal speed (m/s), g is the gravitational acceleration equal to 9.81 m/s 2 , and LLL is the lower limb length (m).

In studies of the dynamics of human walking, a walking LLL is frequently modeled as an inverted pendulum, where the trunk or center of mass goes through a circular arc centered at the foot. One of the most crucial messages from this principle is the finding that humans and others animals have optimum walking speed (OWS, the speed that the metabolic cost of walking is lowest; [Figure 1]) that corresponds to the same Fr, 0.25 (Alexander, 2005). In other words, the optimal speed is dependent on body size, especially from the LLL. From here, we can estimate the OWS as:
Figure 1: Cost of transport and metabolic power as a function of horizontal speed in normal humans.
Note: The descending and ascending limbs of the cost-speed relationship demonstrate the velocities where the metabolic cost is greater than the optimum walking speed (OWS). The patients walk in the descending limb (see text). Data from Ardigò et al. (2003).


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The equation 2 is a modification from Froude equation (equation 1) where Fr is replaced by 0.25 and v is replaced by OWS. Moreover, predictive models of walking capacity have been determined using the height as a crucial predictor (Salbach et al., 2015).

The function of walking is often evaluated in clinical studies determining the SSWS (also known as preferred walking speed). While the LLL is easily measured taking the vertical distance from the great trochanter of the femur to the ground, the SSWS is assessed by asking subjects to walk at a velocity most comfortable and natural in a short distance (3-40 m) (Salbach et al., 2015). In individuals without restrictions, the SSWS coincides with the OWS (close to 4.5 km/h for adults). On the other hand, in many pathological conditions (cardiovascular, respiratory, neurological and orthopedic disorders) the SSWS is lower than the OWS (attaining 2-3 km/h depending of level and type of disorder) (Salbach et al., 2015).

It has been well documented that under different constraints, due to neural, orthopedic, respiratory and cardiac disorders, the preferred walking speed is reduced. In general, these patients execute locomotor movements at relatively low speeds, during their daily life activities (Salbach et al., 2015).

Our recent works in transfemoral amputees, chronic heart failure and chronic obstructive pulmonary disease patients have demonstrated that the metabolic cost of walking is greater at the SSWS than at speeds above the SSWS for these patients indicating that the choice of SSWS is not directly related to metabolic profile (Cavagna et al., 1977; Mitoma et al., 2000; Hausdorff et al., 2003; Crompton et al., 2008; Figueiredo et al., 2013; Wild et al., 2013; Gomenuka et al., 2016). For example, in chronic heart failure subjects, the SSWS seems to be related to ventilatory efficiency (Figueiredo et al., 2013). In all patients studied for us and in the literature it is noticed that the walking is performed in the descending limb of the cost-speed curve ([Figure 1]). It means that at low speeds (at which impaired people walk), although the metabolic power increases with increasing speeds ([Figure 1]B), the cost of transport decreases with increasing speeds ([Figure 1]A) (Gomenuka et al., 2016).

Another fundamental feature of terrestrial locomotion observed here is directly related to metabolic cost of walking. The energy-saving mechanism of walking is defined as pendulum-like mechanism. During level walking, the exchange between gravitational potential and kinetic energies minimizes the fluctuations in the total mechanical energy of the body center of mass (Cavagna et al., 1977; Gomenuka et al., 2016). Substantial evidence has shown that the U-shaped curve of metabolic cost in function of speed ([Figure 1]) is mainly explained by optimization of pendular mechanism in humans. Evolutional pressures in humans seem to be related to bipedalism (Crompton et al., 2008). In pathological conditions, the fact that patients reduce their SSWS, moving away from the OWS, may explain the major cost of locomotion where the pendular mechanism is not optimized (Bona, 2011).


  Assessing the impaired physical function: the lri Top


Based on these findings, we proposed a new parameter of gait evaluation so-called, LRI. The present index defines the locomotor capacity, as before mentioned, taking into account the fundamental concepts of terrestrial locomotion strictly related to walking functionality. Conceptually the LRI determines how close the SSWS is to OWS, or how close the impaired gait is to the normal gait. The LRI is defined as:



Also, the LRI may be useful to evaluate the rehabilitation level not just related to increasing speed but also concerned with the metabolic impact and mechanics of walking during the rehabilitation program. In other words, lower values of LRI should indicate a larger potential of rehabilitation where indirectly the integrative index shows that the individual walk with a substantial metabolic cost (cost of transport; [Figure 1]) due to deteriorated pendular mechanism.


  An example application of lri: nordic walking for training pd subjects Top


This section presents one interesting example application of LRI before and after a training program of Nordic walking reported by Monteiro et al. (2016). PD patients suffer from motor disturbances such as stiffness, postural and balance alterations that provoke instability and a greater variability of spatial and temporal locomotion parameters (for example, more significant time of double support) (Hausdorff et al., 2003). Besides, PD gait is also altered on neuromuscular aspects, as a greater cocontraction of the distal muscles (Mitoma et al., 2000). Such alterations make the Parkinsonian SSWS smaller with increased energy expenditure when compared to healthy people (Wild et al., 2013).

A modality that seems to be useful for the rehabilitation of the pathological gait of PD is the walking training (Soares and Peyré-Tartaruga, 2010; Gallo et al., 2014). Recent systematic reviews have demonstrated the potential of Nordic walking, a walk with the use of two poles, as a rehabilitation modality for the Parkinsonian gait (Tschentscher et al., 2013). To execute the Nordic walking, a greater demand of the upper limbs is necessary, focusing on timing of the movements, dissociation of shoulder and pelvic girdles, and coordination of the swing of the arms alternated with the legs (Pellegrini et al., 2015). The utilization of the contralateral arm to support the pole for the propulsion allows the increase of the walking speed (Fritz et al., 2011; Reuter et al., 2011). In this way, it can be considered as a more efficient intervention model, when compared to free walking (without the use of the poles).

Monteiro et al. (2016) hypothesized that the motor complexity of the Nordic walking task involves neural mechanisms of the motor and non-motor areas, which promote adaptations beyond those related to the automatism of the gait. Besides, the utilization of the poles can attenuate the abnormal patterns of the Parkinsonian gait and increase the SSWS of the patients. They also suggested a higher LRI consequently improved walking metabolic economy after a period of Nordic walking training (Monteiro et al., 2016).

Therefore, the aim of our study was to assess the LRI of patients with PD before and after the Nordic walking and free walking training. Thirty-three patients with idiopathic PD in the stages between 1.5 and 2.5 of Hoehn and Yahr scale participated in this clinical trial, and were randomized in two training groups: Nordic walking (n = 16) and free walking (n = 17). Monteiro et al. (2016) proposed a training of two sessions weekly for 9 weeks, once for 1 hour with intensity between 60-80% of the maximal heart rate. The assessments of SSWS and LRI occurred in pre- and post-training periods, in which the patients walked on the treadmill at three different velocities to select SSWS (Figueiredo et al., 2013; Monteiro et al., 2016). The authors used Generalized Estimating Equations (GEE) as statistical analysis for comparison between groups and times, with Bonferroni post-hoc and α = 0.05.

The individuals were evaluated at pre-familiarization, pre-training and posttraining moments of evaluation (T1, T2 and T3, respectively). The LRI of Nordic walking and free walking groups showed a significant statistical difference between groups in T1, T2 and T3 assessments (P < 0.001, [Figure 2]). There was no time/group interaction (P = 0.695). An increase in LRI values could be observed from T1 to T3 in both groups. However, the LRI was greater for Nordic walking group at all times, indicating that the walking speed of patients from Nordic walking group is closer to the OWS ([Figure 2]).
Figure 2: Comparison of Locomotor rehabilitation index between the Nordic walking (black bars) and free walking (white bars) groups at pre-familiarization, pre-training and post-training moments of evaluation.
Note: "*" represents significant difference between the groups (P < 0.001), different capital letters represent statistical difference (A, B; P < 0.001) among the three evaluation moments (T1, T2, T3). T1: Before familiarization; T2: after familiarization and before training; T3: after training.walking speed (OWS). The patients walk in the descending limb (see text). Data from Ardigò et al. (2003).


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It is hard to precise how the plasticity of the central nervous system occurs after interventions with the use of physical exercise and how it directly or indirectly relates to functional improvements of the gait in PD patients undergoing both training programs. One of the hypotheses that can be highlighted is if the release of trophic factors can impact on dopaminergic neurons, glial cells or even different neurotransmitters are involved in locomotion (Fritz et al., 2011; Monteiro et al., 2016). Although our study does not reach the exact rationale about the mechanisms involved in these adaptations, we consider the present findings as a starting point to mechanistic studies.

Likewise, the clinical implications of gait change outcomes such as LRI need to be further investigated. For example, possible changes in stride frequency and length to explain the modifications in LRI will have a high clinical significance for PD's individuals.

Monteiro and collaborators (Monteiro et al., 2016) conclude that both Nordic walking and free walking training are effective in improving SSWS and LRI. Nordic walking comes up as a therapeutic intervention alternative that enhances LRI of PD patients. Therefore, Nordic walking is considered as an efficient rehabilitation modality for functional recovery of subjects with dopaminergic circuit loss, not only for PD patients, but also for other populations. Moreover, LRI shows to be a simple and low-cost tool with easy access, to evaluate gait rehabilitation of PD patients.


  Conclusions Top


The LRI is a new proposal for evaluating the gait impairments under different pathological conditions. The crucial positive feature of the LRI for the gait rehabilitation is that it is based on central and essential foundations of terrestrial locomotion: the principle of dynamic similarity and the pendular energy saving mechanism of walking. This assessment method is easy to be implemented in clinical conditions and only requires individuals to perform the preferred speed of walking and the measure of lower limb length (from the great trochanter to ground). Secondarily, we demonstrated the practical application of LRI in PD patients after a training program of Nordic walking, showing that the walking speed is improved concomitant with a more economical (metabolically) gait.[16]

 
  References Top

1.
Alexander RM (2005) Models and the scaling of energy costs for locomotion. J Exp Biol 208:1645-1652.  Back to cited text no. 1
    
2.
Cavagna GA, Heglund NC, Taylor CR (1977) Mechanical work in terrestrial locomotion: two basic mechanisms for minimizing energy expenditure. Am J Physiol 233:R243-261.  Back to cited text no. 2
    
3.
Crompton RH, Vereecke EE, Thorpe SK (2008) Locomotion and posture from the common hominoid ancestor to fully modern hominins, with special reference to the last common panin/hominin ancestor. J Anat 212:501-543.  Back to cited text no. 3
    
4.
Figueiredo P, Ribeiro PA, Bona RL, Peyre-Tartaruga LA, Ribeiro JP (2013) Ventilatory determinants of self-selected walking speed in chronic heart failure. Med Sci Sports Exerc 45:415-419.  Back to cited text no. 4
    
5.
Fritz B, Rombach S, Godau J, Berg D, Horstmann T, Grau S (2011) The influence of Nordic Walking training on sit-to-stand transfer in Parkinson patients. Gait Posture 34:234-238.  Back to cited text no. 5
    
6.
Gallo PM, McIsaac TL, Garber CE (2014) Walking economy during cued versus non-cued self-selected treadmill walking in persons with Parkinson′s disease. J Parkinsons Dis 4:705-716.  Back to cited text no. 6
    
7.
Gomenuka NA, Bona RL, da Rosa RG, Peyre-Tartaruga LA (2016) The pendular mechanism does not determine the optimal speed of loaded walking on gradients. Hum Mov Sci 47:175-185.  Back to cited text no. 7
    
8.
Hausdorff JM, Schaafsma JD, Balash Y, Bartels AL, Gurevich T, Giladi N (2003) Impaired regulation of stride variability in Parkinson′s disease subjects with freezing of gait. Exp Brain Res 149:187-194.  Back to cited text no. 8
    
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Hennessy S, Kurichi JE, Pan Q, Streim JE, Bogner HR, Xie D, Stineman MG (2015) Disability stage is an independent risk factor for mortality in medicare beneficiaries aged 65 years and older. PM R 7:1215-1225.  Back to cited text no. 9
    
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Mitoma H, Hayashi R, Yanagisawa N, Tsukagoshi H (2000) Characteristics of parkinsonian and ataxic gaits: a study using surface electromyograms, angular displacements and floor reaction forces. J Neurol Sci 174:22-39.  Back to cited text no. 10
    
11.
Monteiro EP, Franzoni LT, Cubillos DM, de Oliveira Fagundes A, Carvalho AR, Oliveira HB, Pantoja PD, Schuch FB, Rieder CR, Martinez FG, Peyre-Tartaruga LA (2016) Effects of Nordic walking training on functional parameters in Parkinson′s disease: a randomized controlled clinical trial. Scand J Med Sci Sports doi: 10.1111/sms.12652.  Back to cited text no. 11
    
12.
Pellegrini B, Peyre-Tartaruga LA, Zoppirolli C, Bortolan L, Bacchi E, Figard-Fabre H, Schena F (2015) Exploring muscle activation during nordic walking: a comparison between conventional and uphill walking. PLoS One 10:e0138906.  Back to cited text no. 12
    
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Reuter I, Mehnert S, Leone P, Kaps M, Oechsner M, Engelhardt M (2011) Effects of a flexibility and relaxation programme, walking, and nordic walking on Parkinson′s disease. J Aging Res 2011:232473.  Back to cited text no. 13
    
14.
Salbach NM, O′Brien KK, Brooks D, Irvin E, Martino R, Takhar P, Chan S, Howe JA (2015) Reference values for standardized tests of walking speed and distance: a systematic review. Gait Posture 41:341-360.  Back to cited text no. 14
    
15.
Tschentscher M, Niederseer D, Niebauer J (2013) Health benefits of Nordic walking: a systematic review. Am J Prev Med 44:76-84.  Back to cited text no. 15
    
16.
Wild LB, de Lima DB, Balardin JB, Rizzi L, Giacobbo BL, Oliveira HB, de Lima A, II, Peyre-Tartaruga LA, Rieder CR, Bromberg E (2013) Characterization of cognitive and motor performance during dual-tasking in healthy older adults and patients with Parkinson′s disease. J Neurol 260:580-589.  Back to cited text no. 16
    


    Figures

  [Figure 1], [Figure 2]


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