Energy expenditure and perceived effort during uphill and downhill walking in people with multiple sclerosis

Itai HAR-NIR; Lior FRID; Alon KALRON

doi:10.23736/S1973-9087.22.07682-1

. 2022 Dec 2;59(1):25–31. doi: 10.23736/S1973-9087.22.07682-1

Energy expenditure and perceived effort during uphill and downhill walking in people with multiple sclerosis

Itai HAR-NIR ¹, Lior FRID ², Alon KALRON ^{1, 2, 3,}^*

PMCID: PMC10035443 PMID: 36458477

Abstract

BACKGROUND

Walking on different slopes is a common daily activity for many ambulatory people with multiple sclerosis (pwMS)

AIM

Investigate energy expenditure measures of walking on level, uphill and downhill slopes in pwMS.

DESIGN

Observational case-control study.

SETTING

Sheba Multiple Sclerosis Center, Tel-Hashomer, Israel.

POPULATION

Eighteen pwMS; 10 women and 8 men, aged 39.7 (SD=6.8), mean EDSS was 2.9 (SD=1.2) and 23 healthy adults; 8 women and 15 men, aged 37.1 (S.D.=5.3).

METHODS

Energy expenditure values were obtained via a metabolic device during four conditions: sitting, comfortable walking, uphill and downhill walking. Each walking trial, obtained on a treadmill, lasted 6-min and were separated by10-min recovery intervals.

RESULTS

For both pwMS and healthy controls, the O2 rate and O2 cost was higher during uphill walking compared to level walking and lower during downhill walking compared with level walking. O2 rate and net O2 cost during uphill walking was lower in pwMS compared with the healthy controls. The most demanding effort was during uphill walking, with pwMS rating it more demanding compared with the healthy controls.

CONCLUSIONS

Perceived effort of walking on different slopes is not consistent with changes in the energy expenditure values in pwMS.

CLINICAL REHABILITATION IMPACT

pwMS describe the effort of walking on different slopes higher than normal, regardless of the energy expenditure values.

Key words: Multiple sclerosis, Oxygen consumption, Gait, Neurological rehabilitation

Mobility impairment is one of the most serious and frequent concerns of people with multiple sclerosis (pwMS).¹ Based on a survey which included 1011 patients, 70% specified that mobility impairment was the most challenging aspect of multiple sclerosis (MS).² Moreover, walking deficits in pwMS occur at the early disease stage, even when patients are classified as minimally impaired.^{3, 4}

The ability to successfully negotiate slopes is an important aspect of community mobility, as these gradients are encountered in 65% of community settings.⁵ Several studies have examined the effect of slope surfaces on gait in people with central nervous system damage, mainly stroke survivors.^6-9 Phan et al. found that when walking downhill, stroke survivors reduce their walking speed and length of steps, relative to walking on normal and uphill slopes.⁶ Furthermore, previous studies performed on stroke survivors demonstrated that the heart rate⁸ and angles of the major lower limb joints⁹ increase when walking uphill, indicating that an elevated workload is required when walking on different types of slopes.

To the best of our knowledge, walking performance on different types of slope surfaces has never been investigated in pwMS. However, Samaei et al. compared the efficacy of two intervention programs based on uphill and downhill treadmill walking in a sample of pwMS.¹⁰ The authors reported improvements in measures of fatigue and mobility metrics, post intervention, specifically, in the downhill walking group, indicating its rehabilitative potential in pwMS.

Measurement of the metabolic energy expenditure during gait is a key metric providing global information on overall walking performance. Moreover, energy expenditure measures can be used to quantify the overall physiological “penalty” resulting from pathological gait. Recently, it was reported in a systematic review and meta-analysis, that the energy cost of normal walking is 2-3 times higher in mildly-moderately pwMS compared to healthy controls.¹¹ However, to date, no information is available as to whether the differences in energy expenditure during normal walking between pwMS and healthy adults are similar during uphill or downhill walking conditions. Potentially, this information can be utilized in exercise rehabilitative programs aimed at improving aerobic capacity and/or lower limb muscle strength in the MS population. Therefore, the aim of this study was to investigate energy expenditure measures of walking on level, uphill and downhill conditions in pwMS compared with healthy adults. Our hypothesis was that pwMS would demonstrate a higher energy cost of walking than the healthy controls in all walking levels, but, to a higher extent during slope conditions.

Materials and methods

Study design and participants

After local ethical approval, 18 relapsing-remitting pwMS 10 women and 8 men, aged 39.7 (SD=6.8) from the Multiple Sclerosis Center, Sheba Medical Center, Tel Hashomer, Israel, were admitted to our observational case-control study. Participants (pwMS and healthy subjects) were recruited by direct contact of the study staff or via local advertising. Inclusion criteria included: 1) diagnosis of definite relapsing-remitting MS according to the revised McDonald criteria 2017;¹² 2) age range: 18-50 years; and (3) an EDSS Score <4.5.¹³ Exclusion criteria included: 1) orthopedic disorders that could negatively affect mobility; 2) major depression or cognitive decline and incapability of performing on a treadmill; 3) pregnancy; 4) blurred vision; 5) MS clinical relapse or treatment with corticosteroid therapy within a 6-month period prior to examination (6) and cardiovascular disorders. Twenty-three apparently healthy adults, 8 women and 15 men, aged 37.1 (S.D.=5.3), served as a control group. None of the healthy participants reported any medication intake or relevant health impairments (e.g. orthopedic, neurological, or internal diseases). The study was approved by the Sheba Institutional Review Board (Ref# SMC-4709-17). All subjects signed an informed consent form prior to participation.

Experimental protocol

Energy expenditure measures were obtained while walking on the Zebris FDM-T motor-driven treadmill (Zebris1 Medical GmbH, Germany).¹⁴ Prior to the measurement phase, the participant received an adaptation-familiarization trial in order to determine the individual’s comfortable walking speed. Starting at a fixed speed of 0.5 km/h, the speed of the belt was increased by 0.4 km/h every 15 sec in a stepwise manner. Once the participant informed the tester of his/her comfortable walking speed, it was determined as the comfort/normal walking speed. Following the adaptation phase, each participant completed a sequence, in the same order of four consecutive measurement trials while wearing a portable metabolic device:

sitting: considered the resting condition;
comfortable walking: wearing one’s usual walking shoes. The treadmill belt was positioned at surface level and the speed of the belt was set to the patient’s comfortable walking speed;
uphill walking: identical conditions as in (1); treadmill inclination was positioned at a 5-degree ascending slope;
downhill walking: identical conditions as in (2), treadmill inclination was positioned at a 5-degree descending slope.

Each walking trial lasted 6-min¹⁵ and were separated by10-min recovery intervals. Participants were supervised by an exercise physiologist during the experiment.

Energy expenditure measurement

Energy expenditure was measured separately for each trial. Gas exchange values were continuously acquired by open spirometry and indirect calorimetry during each measurement period. Measurements were collected via a portable metabolic device using breath-by-breath technology (COSMED K5, COSMED Srl, Rome, Italy). Participants breathed through a Hans Rudolph face mask (Kansas City, Missouri) equipped with inspiratory valves. Prior to each test, the oxygen and carbon dioxide analyzers and the flow turbine were calibrated according to the COSMED K5’s manufacturer’s instructions. The COSMED unit was placed in a comfortable harness and worn on the shoulders. Data from each subject were telemetrically transferred to a laptop and analyzed by the COSMED software. Furthermore, individual information (i.e., height, weight and age) were inputted into the unit’s software. Participants were asked to avoid eating 4 hours prior to measurements, nor consume alcohol or engage in exercise during the 24 hours prior to testing.

Oxygen consumption at rest was calculated by averaging 30 second VO₂ values (mL/ kg*min) over a 5-minute period of seated rest; higher values indicated a greater rate of resting energy expenditure. Subsequently, the subjects participated in three, 6-minute walking trials walking on a treadmill (surface, uphill, downhill). The treadmill speed was kept constant during all the trials. In the event that the participant felt unstable on the treadmill, slight reductions in speed were made during the first minute of each trial. Gas exchange values were calculated by averaging 30-second values over the final 3 minutes (minutes 4-6).

Research studies have confirmed that the last 3 minutes of a 6-minute period of walking on a treadmill at a predetermined speed, yields a steady-state of VO₂ in pwMS.¹⁶ Net VO₂ (VO_2walk-VO_2sit) was used to calculate the cost of walking (mL O₂ kg^-1 m^-1) during the preferred walking speed. Cost of walking = (VO_2walk-VO_2sit)/speed of walking (m/s).¹⁷ The Borg Category Ratio Scale (Borg CR₁₀) measured the rate of perceived exertion (RPE)¹⁸ for each walking trial. The scale ranges from 0 to 10, with 0 representing no exertion and 10 indicating maximum exertion. Each point on the scale correlates to the amount of exertion felt.

Statistical analysis

Data analysis was performed using the IBM SPSS Statistics for Windows (Version 27.0. Armonk, NY, USA). The data were initially examined for normality violations, outliers, typing errors and missing values. Descriptive statistics were employed for demographic, clinical characteristics, and energy expenditure measures (O₂ rate, O₂ cost, net O₂ cost, Respiratory Exchange Ratio [RER], Metabolic Equivalent of Task [MET], and RPE). The χ² test examined the differences between the healthy controls and the pwMS for gender. A one-way analysis of variance tests (ANOVA) examined age, height, weight and BMI. All outcome variables showed normal distribution. To test our hypothesis, we chose the repeated measure ANOVA with a between-subject factor at 2 levels: the pwMS group vs. the healthy control group and a within-subject factor at 3 levels of walking conditions (comfort, uphill and downhill). A P value of <0.05 was considered significant.

Results

Demographic and clinical data of the participating subjects are presented in Table I.

Table I. —Demographic and clinical data of the participating subjects.

Variables	Total (N.=41)	Healthy (N.=23)	MS (N.=18)	P value
Female	25	15	10	0.540
Males	16	8	8
Age (y)	38.6 (8.7)	37.1 (5.3)	39.7 (6.8)	0.461
Height (cm)	169.0 (8.5)	167.8 (7.9)	170.7 (9.1)	0.278
Weight (kg)	67.1 (13.6)	65.7 (11.1)	68.96 (16.4)	0.460
BMI	23.3 (3.2)	23.20 (2.3)	23.4 (4.2)	0.408
Disease duration (y)	---	---	11.0 (7.7)	---
Mean EDSS	---	---	2.9 (1.2)	---
Comfort walking speed (km/h)	3.6 (0.6)	3.7 (0.5)	3.4 (0.7)	0.180
Energy expenditure measures in sitting position (rest)
O₂ Rate (mL/kg min)	4.41 (1.44)	4.23 (1.00)	4.63 (1.87)	0.386
Metabolic equivalent	1.24 (0.42)	1.19 (0.29)	1.31 (0.54)	0.375
Respiratory exchange ratio	0.78 (0.04)	0.77 (0.03)	0.79 (0.04)	0.052

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Values presented as mean (SD).

The mean EDSS for the pwMS group was 2.9 (SD=1.2) indicating pwMS fully ambulatory without aid,¹³ mean disease duration of 11.0 (S.D.=7.7) years and mean age of 39.7 (S.D.=6.8). No significant differences were observed between pwMS and healthy controls in terms of age, gender distribution, height, weight, and BMI. Comfort walking speed was slightly slower in the pwMS group compared with the healthy controls; however, it did not meet a significant level (P value=0.180). No differences in the energy expenditure measures during sitting were observed between groups.

Energy expenditure measures according to the three walking conditions and groups is presented in Table II and illustrated in Figure 1, 2, 3, 4, 5, 6.

Table II. —Energy expenditure measures according to the three walking condition and study groups.

Variable	Healthy (N.=23)			F (P value) for condition	MS (N.=18)			F (P value) for condition	F (P value) for condition x group
Variable	Normal	Uphill	Downhill	F (P value) for condition	Normal	Uphill	Downhill	F (P value) for condition	F (P value) for condition x group
O₂ Rate [mL/kg min]	12.67 (2.2)^a	22.32 (3.5)^b	9.54 (2.0)^c	285.285 (<0.001)	13.04 (4.1)^a	18.29 (3.7)^b	10.54 (2.3)^c	61.663 (<0.001)	19.049 (<0.001)
C_wnet [mg/kg m]	0.13 (0.03)^a	0.29 (0.05)^b	0.08 (0.03)^c	303.490 (<0.001)	0.14 (0.06)^a	0.24 (0.05)^b	0.10 (0.04)^c	56.597 (<0.001)	13.060 (<0.001)
C_w [mg/kg m]	0.20 (0.04)^a	0.36 (0.06)^b	0.15 (0.04)^c	311.219 (<0.001)	0.23 (0.07)^a	0.32 (0.07)^b	0.19 (0.05)^c	60.414 (<0.001)	13.172 (<0.001)
RER [VO₂/VCO₂]	0.73 (0.03)^a	0.79 (0.04)^b	0.78 (0.04)^b	24.757 (<0.001)	0.75 (0.07)^a	0.81 (0.05)^b	0.81 (0.07)^b	8.402 (<0.050)	0.261 (0.771)
MET	3.61 (0.63)^a	6.38 (1.03)^b	2.71 (0.56)^c	285.646 (<0.001)	3.76 (1.20)^a	5.38 (1.34)^b	3.23 (1.36)^a	21.386 (<0.001)	10.067 (<0.001)
RPE [Score]	1.60 (0.40)^a	2.90 (0.40)^b	1.50 (0.50)^a	70.442 (<0.001)	2.60 (0.80)^a	4.10 (0.80)^b	3.60 (1.40)^b	11.861 (<0.001)	7.672 (<0.001)

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Cw: Cost of walking; C_wnet: Net cost of walking (considering energy expenditure during rest); RER: Respiratory Exchange Ratio; MET: Metabolic Equivalent of Task; RPE: Rate Perceived Exertion. ^{a, b, c} define significant differences between walking conditions.

—O₂ rate according to the three walking conditions and groups.

—Cost of walking according to the three walking conditions and groups.

—Net cost of walking according to the three walking conditions and groups.

—Respiratory Exchange Rate (RER) according to the three walking conditions and groups.

—Metabolic Equivalent of Task (MET) according to the three walking conditions and groups.

—Rating of Perceived Exertion (RPE) according to the three walking conditions and groups.

O₂ rate and O₂ cost of walking was significantly different between the three walking conditions in both the pwMS and healthy controls. For both pwMS and healthy controls, the O₂ rate and O₂ cost was higher during uphill walking compared to level walking and lower during downhill walking compared with level walking. Moreover, the O₂ rate during uphill walking was lower in pwMS compared with the healthy controls (18.3 (S.D. 3.7 vs. 22.3 (S.D.=3.5; P value=0.001). Similarly, the O₂ cost (net) during uphill walking was lower in pwMS compared with the healthy controls (0.24 (S.D.=0.05) vs. 0.29 (S.D.=0.05; P value<0.05).

In each of the three walking conditions, the RPE was higher in pwMS compared with the healthy controls (Figure 6). The most demanding effort was reported during uphill walking compared with downhill and level walking for all subjects, with pwMS rating it more demanding compared with the healthy controls (4.1 (S.D.=0.8) vs. 2.9 (S.D.=0.4); P value<0.001).

Discussion

To the best of our knowledge, this study is the first to present energy expenditure values during treadmill walking on uphill and downhill slopes in pwMS. The motivation for this investigation was based on the recognition that walking on different types of slopes is a common daily activity for many ambulatory pwMS, thus, requiring different physiological requirements. We found that when comparing level walking with uphill walking, the uphill walking required higher oxygen consumption whereas, the downhill walking required less. Furthermore, pwMS reported higher RPE scores during level, uphill and downhill slopes compared with the healthy controls. However, the perceived effort score was not always related with changes in the energy expenditure values.

The present values of energy expenditure during level walking of pwMS are in accordance with the literature. According to a recent systematic review, the energy cost of treadmill walking in pwMS, with belt speed set between 0.43 and 1.48 m/s, lies between 0.16 and 0.44 mL O₂/kg/m.¹⁹ Therefore, we consider the value of 0.23 of the present MS cohort acceptable, mainly reflecting the condition of mildly disabled pwMS.

The higher energy expenditure values measured during uphill walking and the lower values found during downhill walking (each compared to level walking) match the literature, and was similar between pwMS and healthy adults.²⁰ We further clarify, that changes in energy expenditure during uphill and downhill walking occur when there are changes in the whole-body mechanics.²¹ Uphill walking leads to an increase in energy expenditure values since the legs have to perform more positive work²² to move the center of mass upward against gravity. Moderate downhill walking causes a decrease in energy expenditure.²¹ During downhill walking, the muscles produce more eccentric work than during level or uphill walking²² in order to prevent the center of mass from accelerating downward. Negative mechanical work is less metabolically costly than positive mechanical work, therefore, downhill walking is less metabolically costly than uphill walking. From this perspective, mildly disabled pwMS and healthy adults similarly perform.

Interestingly, although the trend of energy expenditure values between walking conditions was similar between groups, the relative change (in %) between walking conditions varied. For example, in the healthy controls, the energy cost of walking was ~120% higher in the uphill walking condition compared with level walking, whereas, this value increased by only ~70% in pwMS. Moreover, during downhill walking the cost of walking was ~40% lower compared to level walking in healthy adults, yet lower by only ~30% in pwMS. These observations suggest that compared with healthy adults, pwMS tend to maintain the metabolic cost of walking (as much as possible) despite changes in slope level, probably by using different walking strategies. Unfortunately, in the present study, we did not capture definite measures of gait, besides speed, during the walking trials. Consequently, we can only speculate about the walking strategy that was used by pwMS during the uphill and downhill conditions and define whether it was different than observed in the healthy controls. Furthermore, it is possible that more than one walking strategy had been utilized, i.e. a previous study found that minimally impaired pwMS demonstrate different biomechanics of the lower limbs compared with healthy adults when instructed to transit from normal walking to jogging.²³ In order to clarify this issue, we encourage future research to investigate the associations between energy expenditure measures during walking on slopes with major kinematics and kinetics of the lower limbs in pwMS.

A novel finding of our study relates to the RPE. Despite similar energy expenditure values between pwMS and healthy controls, pwMS rated the effort significantly higher in all three walking conditions (especially, in the slope conditions), compared with healthy adults. This finding is not in accordance with the literature. Bollaert et al. demonstrated that pwMS reported similar RPE scores during an aerobic exercise test compared to healthy controls.²⁴ Similarly, Morrison et al. found that despite greater reported fatigue levels, pwMS showed similar RPE and physiologic responses during submaximal and maximal exercise tests compared with the healthy controls.²⁵ Furthermore, Kiselka et al. did not find differences in the perception of a muscular effort (elbow extension) between pwMS and age-matched healthy controls.²⁶

We speculate that the reason for the different findings of our study compared with previous studies relates to the testing design. In previous studies, the exercise testing condition was performed in a sitting position (i.e. cycle ergometer), a relatively safe and stable position. In contrast, our testing condition of walking on different types of slopes might have been a bit frightening for several of the pwMS, especially, those with a low confidence level in their dynamic balance capabilities. Worth noting, ambulating on a sloped treadmill surface (uphill or downhill) is more challenging compared to over-ground conditions, mainly, because walking on a treadmill requires the participant to adjust his/her speed according to the movement of the belt, if not, there is a danger of falling off the treadmill. We speculate that the increased RPE scores reported by the pwMS were due to the linkage of the perceived effort of the walking condition with fear of losing their balance and/or falling. Notably, all participants wore a harness during the walking conditions for safety, however, this element might not have been enough to lessen the fear of falling.

Limitations of the study

There are several limitations to our study design. Firstly, we assessed the oxygen cost of walking and energy equivalents during treadmill walking, which is less generalizable to real-life walking than over-ground walking. Secondly, we did not attempt to screen eligible pwMS for heat sensitivity, the presence or absence of which may have affected the study’s result. Additionally, the level of spasticity and fatigue related to our main outcome measures, was not controlled in the study, although, it is rarely significant in mild MS. Furthermore, our study was limited to patients with a relapsing-remitting form of the disease, relatively young (up to 50 years of age) with minimal and mild disability. Therefore, our conclusions cannot be confirmed in progressive MS, older patients or patients with moderate and severe disabilities and/or in the use of mobility aids. Finally, the present sample size was relatively small, however, our data should serve as sample size calculations for future trials.

Conclusions

Compared to walking on a level surface, pwMS demonstrated higher energy expenditure values during uphill walking and lower values during downhill walking. Furthermore, the pwMS rated the perceived effort of walking on slope conditions higher compared to the healthy adults. From a clinical perspective, these findings should aid professionals in the field of physical rehabilitation of pwMS. Walking on different types of slopes is essential for many outdoor daily life activities for ambulatory pwMS, we, therefore, confirm that it should be inserted as part of a training program. Importantly, the therapist/trainer should be aware that patients describe the effort higher, regardless of the actual energy expenditure value. Finally, future studies should clarify whether energy expenditure values, and rating of perceived effort during uphill and downhill walking, are similar between treadmill to over-ground walking conditions in the MS population.

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PERMALINK

Energy expenditure and perceived effort during uphill and downhill walking in people with multiple sclerosis

Itai HAR-NIR

Lior FRID

Alon KALRON