Research in Developmental Disabilities 35 (2014) 2527–2533
Contents lists available at ScienceDirect
Research in Developmental Disabilities
Physical fitness assessment in multiple sclerosis patients: A controlled study E. Guerra a,*, A. di Cagno a, P. Mancini a, F. Sperandii a, F. Quaranta a, E. Ciminelli a, F. Fagnani a, A. Giombini b, F. Pigozzi a a b
Department of Health, Movement and Human Sciences University of Rome ‘‘Foro Italico’’, Piazza Lauro de Bosis 15, Rome, Italy Department of Medicine and Health Sciences, University of Molise, V. De Sanctis, Campobasso, Italy
A R T I C L E I N F O
A B S T R A C T
Article history: Received 25 February 2014 Received in revised form 10 June 2014 Accepted 12 June 2014 Available online 5 July 2014
There is growing evidence to show the effectiveness of physical exercise for multiple sclerosis (MS) patients. Aim of this study was to evaluate aerobic capacity, strength, balance, and the rate of perceived exertion (RPE) after exercise, in ambulatory patients with mild MS and matched control healthy participants. Seventeen MS patients aged 48.09 10.0 years, with mild MS disability (Expanded Disability Status Scale: EDSS 1.5 to 4.5) and 10 healthy sedentary age matched (41.9 11.2 years) subjects volunteered for the study. MS patients underwent medical examination with resting electrocardiogram, arterial blood pressure, EDSS, and Modified Fatigue Impact Scale-MFIS. Both groups also underwent physical assessment with the Berg Balance Scale, test (Berg), Six Minutes Walking Test (6MWT), maximal isometric voluntary contraction (MIVC) of forearm, lower limb, shoulder strength test, and the Borg 10-point scale test. The one-way ANOVA showed significant differences for MFIS (F1.19 = 9.420; p < 0.01), Berg (F1.19 = 13.125; p < 0.01), handgrip MIVC (F1.19 = 4.567; p < 0.05), lower limbs MIVC (F1.19 = 7.429; p < 0.01), and 6MWT (F1.19 = 28.061; p < 0.01) between groups. EDSS, Berg test and Borg scores explained 80% of 6MWT variation. Mild grade EDSS patients exhibited impaired balance, muscle strength, and low self pace-6MWT scores, whereas RPE response after the exercise was similar to that of sedentary individuals. Both groups showed similar global physiological adjustments to exercise. ß 2014 Elsevier Ltd. All rights reserved.
Keywords: Aerobic capacity Balance Strength Fatigue Disability
1. Introduction Multiple sclerosis (MS) is a chronic autoimmune demyelinating disease of the central nervous system. Evidence indicates that MS is more prevalent in females than males (Ahlgren, Ode´n, & Lycke, 2011; Compston & Coles, 2002). The disease results in an alteration of the myelin, thus reducing the speed of transmission of the nerve impulses, up to conduction block (Ng, Dao, Miller, Gelinas, & Kent-Brau, 2000). This alteration may result in severe symptoms, particularly muscle fatigue and locomotor impairment. Several studies have shown that MS patients have lower values of maximal aerobic power, when compared to healthy adults matched for age and gender and a significant reduction in muscle strength (Smith, Adeney-Steel,
* Corresponding author. Tel.: +39 06 36733338; fax: +39 06 36733344. E-mail addresses: [email protected] (E. Guerra), [email protected] (A. di Cagno), [email protected] (P. Mancini), [email protected] (F. Sperandii), [email protected] (F. Quaranta), [email protected] (E. Ciminelli), [email protected] (F. Fagnani), [email protected] (A. Giombini), [email protected] (F. Pigozzi). http://dx.doi.org/10.1016/j.ridd.2014.06.013 0891-4222/ß 2014 Elsevier Ltd. All rights reserved.
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Fulcher, & Longley, 2006). Based upon these findings, for many years, patients affected by MS were advised to avoid sessions of exercise and training, since most of them experienced excessive fatigue during and after exercise, coupled with a rise in body temperature (White, Wilson, Davis, & Petajan, 2000). In critical conducting axons, such as those that are demyelinated, impulse conduction may be affected by heating. Raising the body temperature by as little as 0.5 8C may be sufficient to precipitate conduction in critically conducting axons (Vucic, Burke, & Kiernan, 2010). During the last decade, it has become popular to prescribe physical exercise to MS patients, as long as it is well tolerated and induces relevant improvements in both physical and mental functioning (Dalgas, Stenager, & IngemannHansen, 2008; White & Dressendorfer, 2004). It is thought that much of the reduced efficiency in MS patients could be the result of increased ‘‘inactive life,’’ secondary to the disease, rather than the impairments caused by the disease per se (Ng, Miller, Gelinas, & Kent-Braun, 2004). Indeed, it is clearly necessary to prescribe and individualize physical exercise in order to achieve significant improvement in quality of life for MS patients and reduce the economic burden. In fact a significant increase in costs is associated with an increase in disease severity as measured by Expanded Disability Status Scale (EDSS) scores. Physical activity is a non-pharmaceutical intervention and act delaying the progression of disease (Naci, Fleurence, Birt, & Duhig, 2010). In light of this, the collection of fitness parameters such as aerobic capacity, strength levels and balance and may represent the basis from which training protocols can be planned. The current standard for testing aerobic capacity is a maximal cardiopulmonary exercise test which determines Maximum oxygen consumption (VO2peak). VO2peak reflects the maximum capacity of a person to absorb, carry and consume O2 (Albouaini, Egred, Alahmar, & Wright, 2007). However, VO2peak is a prerogative of specialized laboratory settings with low feasibility. On the contrary, submaximal tests are more functional and have been considered as good predictors of exercise capacity, especially in MS patients who show marked reductions in exercise capacity (Kuspinar, Andersen, Teng, Asano, & Mayo, 2010). Several studies have investigated upper and lower extremity muscle strength in MS subjects, using different methodologies (Citaker et al., 2013; Kuspinar et al., 2010). Indeed, it is thought that properly designed strength training of the weakest muscle groups should improve MS patients’ management of their everyday activity, whilst simultaneously improving autonomy and reducing the risk of falls (Cattaneo, Jonsdottir, & Repetti, 2007). Changes in balance, coordination, postural control, and gait are other features reported in MS subjects, due to a compromised neural functioning, which leads to both sensory and motor dysfunction (Coote, Finlayson, & Sosnoff, 2013). Proper evaluation of the balance deficit allows for the correct prescription of balance interventions. Over recent years, the quantification of these parameters and the analysis of their correlations have changed the way in which these patients are managed. Our primary objective was to compare aerobic capacity, strength, balance, and the rate of perceived exertion (RPE) after exercise between ambulatory patients with mild MS and matched control healthy participants. The second objective was to study the correlations between fitness and clinical parameters with the goal of sharpening the focus of the rehabilitation protocols used to tackle this disease.
2. Materials and methods We screened 17 subjects (13 females, 4 males) aged 48.09 10, affected by MS disability (EDSS 1.5 to 4.5). All patients were ambulatory type, whereas one used a cane. Inclusion criteria were: patients with confirmed diagnosis of clinically definite MS. Personal and clinical information such as age, sex, height, weight, duration of the disease and type of MS were determined by examination of medical charts. We also screened subjects’ BMI, heart rate, baseline electrocardiogram (ECG) and blood pressure. Quantification of disability in MS patients was determined by the EDSS (Sharrack & Hughes, 1996). The EDSS measure was administered by a consultant neurologist. No subject had undergone EDSS evaluation previously, and no EDSS score was reported in the medical charts. This basic scale quantifies disability by evaluating and assessing a score in eight neurological functional systems, namely pyramidal, cerebellar, brainstem, sensory, bowel and bladder, visual and cerebral. The EDSS score ranges from 0, which represents absence of clinical impairment to 10, which is the highest grade. An EDSS level of 3 represents a fully ambulatory patient with moderate disability, a score of 6 represents necessity for unilateral assistance with canes, crutches, or braces when required to walk 100 meters, and a score of 8 represents patients restricted to bed or chair or perambulated in a wheelchair. A total of 10 age and sex matched healthy and sedentary subjects (41.9 11.2 years) were included as a control group. Exclusion criteria for both the study groups included: pregnancy, morbid obesity as defined by BMI of 40 kg/m2 or more, cognitive impairment, cardiopulmonary disease, and orthopedic conditions prohibiting participation in safe exercise testing. The subjects’ characteristics are shown in Table 1. The perceived difficulty in carrying out daily living activities was assessed in all subjects, MS and Controls, using the Modified Fatigue Impact Scale (MFIS; Tellez et al., 2005). This approach is based on 21 items derived from interviews concerning how fatigue had impacted their lives over the preceding month. Administration time was approximately 5– 10 min for the full-length version. We administered the MFIS once before the testing sessions, and summary scores as well as physical, cognitive and psychosocial subscale scores were calculated. All examinations and tests were performed in a public rehabilitation facility. The study was designed in agreement with the Declaration of Helsinki, and was approved by the local Ethical Committee. All subjects volunteered for the study and informed written consent was obtained from all participants before the experimental set-up.
E. Guerra et al. / Research in Developmental Disabilities 35 (2014) 2527–2533
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Table 1 Subjects characteristics (mean SD).
Age (years) Years of disease Height (cm) Weight (kg) Body Mass index (BMI)
MS patients (n = 17)
Control group (n = 10)
Mean SD
Mean SD
47.8 10.6 6.8 5.1 164.5 10.7 65.1 15.8 24.1 3.3
41.9 11.3 – 165.7 10.9 64.9 13.4 23.6 4.2
2.1. Procedures All subjects attended two successive fitness evaluation sessions. In the first fitness testing session subjects underwent the Berg Balance Scale (Berg, Wood-Dauphinee, Williams, & Maki, 1992) and Six Minute Walking test (6MWT) whereas in the second session a strength test were performed. The Berg test consists of a 14 item scale, according to functional tasks deficits. The test duration is approximately 15 min, with 14 balance-related tasks including unsupported sitting, change of position, standing on one foot, standing with eyes closed. The Berg score ranges from 0, representing no balance capacity with high fall risk, to 4 (normal performance), with a maximum score of 56. In order to perform this test, a ruler, two standard chairs (one with arm rests, one without), a footstool or step, and a stopwatch are required. The Intraclass Correlation Coefficients (ICCs) for test–retest reliability range between 0.85 and 0.96, whilst the validity (r = 0.71) of the Berg scale has been assessed using a population of subjects with MS (Cattaneo et al., 2007; Cattaneo, Regola, & Meotti, 2006). Functional aerobic capacity (cardiovascular fitness) was measured by using the 6MWT. This test measures the distance that a patient can quickly walk on a flat, hard surface in a period of 6 min. It evaluates the global and integrated responses of all the systems involved during exercise, including the pulmonary and cardiovascular systems, systemic circulation, peripheral circulation, blood, neuromuscular units, and muscle metabolism. With this said however, it does not provide specific information on the function of each of the different organs and systems involved in exercise or the mechanism of exercise limitation. The self-paced 6MWT assesses the submaximal level of functional capacity, even if it involves a ‘‘maximal’’ request; the subjects are in fact invited to walk as many meters as they can. This test was performed in an enclosed 20 m corridor (Veloso-Guedes et al., 2011). Each meter was marked on the floor and a chair was present every 5 meters. Individuals were instructed to walk, back and forth, exerting maximal effort within the 6-min period at their own pace, but were continuously encouraged during this test (Broekmans et al., 2013). They could rest at any time during the test, but were encouraged to resume walking as soon as they were ready. The 6MVT has high reliability (ICC ranged between 0.80 and 0.90) and moderate validity (r = 0.56 to 0.88; Finch, Brooks, Stratford, & Mayo, 2002). Subjective perception of fatigue in this test was evaluated using the Borg 10-item scale (Borg, 1982). Maximum Isometric Voluntary Contraction (MIVC) was measured for the forearm muscles, shoulders elevators muscles and quadriceps muscles, in order to minimize the testing time (Gutierrez et al., 2005). Grip strength was measured using a programmed handgrip dynamometer (IBX H-101, MD Systems INC., Westerville, OH, USA). Standardized instruction and position were used, whilst 3 consecutive trials for each hand were recorded. Grip strength had excellent reliability with a measurement error of approximately 2 kg (Schreuders et al., 2003). The MIVC of the knee extensor muscles in both limbs was performed during the leg extension tests. Participants sat on a chair, with arms folded across the chest. A sitting iron support was prepared to adapt the sit to the length of the femur, in order to obtain a standard sit position. The trunk was erected and fastened using two crossing belts. Participants were instructed to exert maximal extension torque and to maintain it for 5 s. For extension the knee angle was positioned at 1108 (1808 refers to full extension), and the hip angle at 908. MIVC was calculated as the largest 1-s average reached within any single force recording. A total of 3 attempts were measured for both legs, with 2 min of rest between. Extension isometric torque was measured using a commercially available load cell (AEP elettronica, Italy) connected to a computerized system unit. Under the same sitting position but with arms hanging on their side, MIVC of the shoulder elevators was obtained by pulling a 20 cm iron bar connected in a series with the load cell. A target line was always set on the computer screen at a value 20% higher than the best performance. The participants were able to follow their performance on the computer screen. 3. Calculation Data were expressed as mean (SD). Descriptive statistics were used to characterize the participants and verify the distribution of variables. A one-way ANOVA was performed to assess significant differences between MS patients and the control group. If significant main effects were found, a Fisher’s LSD post hoc was performed. The relationship between investigated MS
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patient variables was analyzed using Pearson product-moment correlations (r). Forward stepwise linear regression (R2) was performed to identify the best predictive model of exercise capacity. All statistics were calculated using SPSS (SPSS version 20.0 Chicago). A significance level of p < 0.05 was adopted. 4. Results Seventeen patients with MS were evaluated. MS patients and controls were homogeneous at baseline for age and BMI. Of the patients, 10 showed Relapsing Remitting MS (RRMS), 6 had Secondary Progressive Course (SPMS), and 1 had only laboratory diagnosis of MS. A total of 6 subjects declined to perform the isometric strength tests, whereas 11 patients with MS underwent the strength testing sessions. Considering each dependent variable, the one-way ANOVA revealed significant differences between the two groups, for systolic blood pressure at baseline (F1.19 = 6.478; p < 0.05), diastolic blood pressure at baseline (F1.19 = 7.372; p < 0.05), MFIS (F1.19 = 9.420; p < 0.01), Berg (F1.19 = 13.125; p < 0.01), handgrip MIVC (F1.19 = 4.567; p < 0.05), lower limb MIVC (F1.19 = 7.429; p < 0.01), and 6MWT (F1.19 = 28.061; p < 0.01). No significant differences between groups were found for heart rate at baseline, heart rate at the end of exercise, delta of heart rate, or systolic and diastolic blood pressure at the end. Considering the strength tests for only the 11 MS patients who gave consent to perform MIVC, the following results were found: MICV leg extension(right-left) 29.2 18.9, MICV leg extension(dominant limb) 30.6 19.7 kg, range 4.87–78 kg, delta strength of lower limbs 23 16%, MICV handgrip(right-left) 24.2 10.7 kg, MICV handgrip(dominant limb) 25.07 12.8 kg, range 4.8–47.37 kg. MICV shoulder elevators(right-left) 30.3 17.3 kg, MICV shoulder elevators(dominant limb) 32.5 17.3 kg, range 10.5–66.88 kg. In comparison with controls, significant differences were found in handgrip and lower limb strength, whereas no significance was found for shoulder strength. The Fisher’s LSD post hoc results are shown in Table 2. Significant and large correlations were found between EDSS and HR at baseline (r = 0.620; p < 0.05), EDSS and 6MWT (r = 0.843; p < 0.01), as well as EDSS and Borg scores (r = 0.609; p < 0.05, and between 6MWT and Borg scores (r = 0.596; p = 0.053), and 6MWT and Berg (r = 0.716; p < 0.05). Handgrip, shoulder and lower limb MIVC were significantly correlated with each other (p < 0.01), and with the systolic blood pressure at the baseline (r = 0.806; r = 0.728; r = 0.653; p < 0.01, respectively). Results of linear regression analysis revealed a predictive model from the EDSS for Borg scores (R2 = 0.371, R2adj = 0.301; p < 0.05), for HR at baseline (R2 = 0.384, R2adj = 0.316; p < 0.05) and EDSS, for the cardiovascular fitness, assessed by 6MWT (R2 = 0. 711, R2adj = 0.679; p < 0.01); from 6MWT for Berg (R2 = 0.512, R2adj = 0.458; p < 0.05), and for Borg near the significance (R2 = 0.356, R2adj = 0.284; p = 0.053). The Delta MIVC of lower limbs was predictive of reduced balance evaluated by Berg test (R2 = 0.51, R2adj = 0.481; p < 0.05). The relationship between 6MWT scores and the other variables was further examined by multiple linear regressions, with adjustment for other covariates. EDSS, Berg test and Borg scores explained 80% 6MWT variation (R2 = 0.856, R2adj = 0.795; p < 0.01) whilst EDSS, 6MWT and Berg test 50%-Borg score variation (R2 = 0.657, R2adj = 0.511; p < 0.05). The results are shown in Fig. 1.
Table 2 Significant differences between MS patients, completing physical testing sessions, and Controls, according to ANOVA One-way test (*p < 0.05; ** p < 0.01). Variables
HR baseline HR at the end Delta HR Systolic blood pressure at baseline Systolic blood pressure at end Diastolic blood pressure at baseline Diastolic blood pressure at baseline MFIS BORG BERG Handgrip test Shoulder elevator test Leg extension test Right leg extension test Left leg extension test 6MW test
MS patients (n.11)
Control (n.10)
Variance
Mean SD
Mean SD
F
p
75.1 5.3 96.1 2.4 21.0 18.9 121.8 13.3 145.5 19.8 80.0 8.9 77.3 9.8 29.7 16.7 4.6 1.7 45.7 8.9 22.5 11.6 30.3 17.3 29.2 18.9 27.8 20.7 26.2 18.2 384.0 119.6
72.8 11.6 98.0 17.2 25.2 15.9 107.0 13.4 131.0 17.3 70.0 7.8 72.5 5.9 10.9 10.2 4.4 1.1 56.0 0.0 34.3 13.7 40.2 16.2 52.8 19.8 53.0 19.0 53.1 21.2 614.2 70.6
0.348 0.0538 0.300 6.478 3.145 7.372 1.770 9.420 0.143 13.125 4.567 1.7524 7.429 8.373 9.821 28.061
0.562 0.198 0.590 0.020* 0.092 0.014* 0.199 0.006** 0.709 0.002** 0.045* 0.202 0.014* 0.009** 0.005**
Contents lists available at ScienceDirect
Research in Developmental Disabilities
Physical fitness assessment in multiple sclerosis patients: A controlled study E. Guerra a,*, A. di Cagno a, P. Mancini a, F. Sperandii a, F. Quaranta a, E. Ciminelli a, F. Fagnani a, A. Giombini b, F. Pigozzi a a b
Department of Health, Movement and Human Sciences University of Rome ‘‘Foro Italico’’, Piazza Lauro de Bosis 15, Rome, Italy Department of Medicine and Health Sciences, University of Molise, V. De Sanctis, Campobasso, Italy
A R T I C L E I N F O
A B S T R A C T
Article history: Received 25 February 2014 Received in revised form 10 June 2014 Accepted 12 June 2014 Available online 5 July 2014
There is growing evidence to show the effectiveness of physical exercise for multiple sclerosis (MS) patients. Aim of this study was to evaluate aerobic capacity, strength, balance, and the rate of perceived exertion (RPE) after exercise, in ambulatory patients with mild MS and matched control healthy participants. Seventeen MS patients aged 48.09 10.0 years, with mild MS disability (Expanded Disability Status Scale: EDSS 1.5 to 4.5) and 10 healthy sedentary age matched (41.9 11.2 years) subjects volunteered for the study. MS patients underwent medical examination with resting electrocardiogram, arterial blood pressure, EDSS, and Modified Fatigue Impact Scale-MFIS. Both groups also underwent physical assessment with the Berg Balance Scale, test (Berg), Six Minutes Walking Test (6MWT), maximal isometric voluntary contraction (MIVC) of forearm, lower limb, shoulder strength test, and the Borg 10-point scale test. The one-way ANOVA showed significant differences for MFIS (F1.19 = 9.420; p < 0.01), Berg (F1.19 = 13.125; p < 0.01), handgrip MIVC (F1.19 = 4.567; p < 0.05), lower limbs MIVC (F1.19 = 7.429; p < 0.01), and 6MWT (F1.19 = 28.061; p < 0.01) between groups. EDSS, Berg test and Borg scores explained 80% of 6MWT variation. Mild grade EDSS patients exhibited impaired balance, muscle strength, and low self pace-6MWT scores, whereas RPE response after the exercise was similar to that of sedentary individuals. Both groups showed similar global physiological adjustments to exercise. ß 2014 Elsevier Ltd. All rights reserved.
Keywords: Aerobic capacity Balance Strength Fatigue Disability
1. Introduction Multiple sclerosis (MS) is a chronic autoimmune demyelinating disease of the central nervous system. Evidence indicates that MS is more prevalent in females than males (Ahlgren, Ode´n, & Lycke, 2011; Compston & Coles, 2002). The disease results in an alteration of the myelin, thus reducing the speed of transmission of the nerve impulses, up to conduction block (Ng, Dao, Miller, Gelinas, & Kent-Brau, 2000). This alteration may result in severe symptoms, particularly muscle fatigue and locomotor impairment. Several studies have shown that MS patients have lower values of maximal aerobic power, when compared to healthy adults matched for age and gender and a significant reduction in muscle strength (Smith, Adeney-Steel,
* Corresponding author. Tel.: +39 06 36733338; fax: +39 06 36733344. E-mail addresses: [email protected] (E. Guerra), [email protected] (A. di Cagno), [email protected] (P. Mancini), [email protected] (F. Sperandii), [email protected] (F. Quaranta), [email protected] (E. Ciminelli), [email protected] (F. Fagnani), [email protected] (A. Giombini), [email protected] (F. Pigozzi). http://dx.doi.org/10.1016/j.ridd.2014.06.013 0891-4222/ß 2014 Elsevier Ltd. All rights reserved.
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Fulcher, & Longley, 2006). Based upon these findings, for many years, patients affected by MS were advised to avoid sessions of exercise and training, since most of them experienced excessive fatigue during and after exercise, coupled with a rise in body temperature (White, Wilson, Davis, & Petajan, 2000). In critical conducting axons, such as those that are demyelinated, impulse conduction may be affected by heating. Raising the body temperature by as little as 0.5 8C may be sufficient to precipitate conduction in critically conducting axons (Vucic, Burke, & Kiernan, 2010). During the last decade, it has become popular to prescribe physical exercise to MS patients, as long as it is well tolerated and induces relevant improvements in both physical and mental functioning (Dalgas, Stenager, & IngemannHansen, 2008; White & Dressendorfer, 2004). It is thought that much of the reduced efficiency in MS patients could be the result of increased ‘‘inactive life,’’ secondary to the disease, rather than the impairments caused by the disease per se (Ng, Miller, Gelinas, & Kent-Braun, 2004). Indeed, it is clearly necessary to prescribe and individualize physical exercise in order to achieve significant improvement in quality of life for MS patients and reduce the economic burden. In fact a significant increase in costs is associated with an increase in disease severity as measured by Expanded Disability Status Scale (EDSS) scores. Physical activity is a non-pharmaceutical intervention and act delaying the progression of disease (Naci, Fleurence, Birt, & Duhig, 2010). In light of this, the collection of fitness parameters such as aerobic capacity, strength levels and balance and may represent the basis from which training protocols can be planned. The current standard for testing aerobic capacity is a maximal cardiopulmonary exercise test which determines Maximum oxygen consumption (VO2peak). VO2peak reflects the maximum capacity of a person to absorb, carry and consume O2 (Albouaini, Egred, Alahmar, & Wright, 2007). However, VO2peak is a prerogative of specialized laboratory settings with low feasibility. On the contrary, submaximal tests are more functional and have been considered as good predictors of exercise capacity, especially in MS patients who show marked reductions in exercise capacity (Kuspinar, Andersen, Teng, Asano, & Mayo, 2010). Several studies have investigated upper and lower extremity muscle strength in MS subjects, using different methodologies (Citaker et al., 2013; Kuspinar et al., 2010). Indeed, it is thought that properly designed strength training of the weakest muscle groups should improve MS patients’ management of their everyday activity, whilst simultaneously improving autonomy and reducing the risk of falls (Cattaneo, Jonsdottir, & Repetti, 2007). Changes in balance, coordination, postural control, and gait are other features reported in MS subjects, due to a compromised neural functioning, which leads to both sensory and motor dysfunction (Coote, Finlayson, & Sosnoff, 2013). Proper evaluation of the balance deficit allows for the correct prescription of balance interventions. Over recent years, the quantification of these parameters and the analysis of their correlations have changed the way in which these patients are managed. Our primary objective was to compare aerobic capacity, strength, balance, and the rate of perceived exertion (RPE) after exercise between ambulatory patients with mild MS and matched control healthy participants. The second objective was to study the correlations between fitness and clinical parameters with the goal of sharpening the focus of the rehabilitation protocols used to tackle this disease.
2. Materials and methods We screened 17 subjects (13 females, 4 males) aged 48.09 10, affected by MS disability (EDSS 1.5 to 4.5). All patients were ambulatory type, whereas one used a cane. Inclusion criteria were: patients with confirmed diagnosis of clinically definite MS. Personal and clinical information such as age, sex, height, weight, duration of the disease and type of MS were determined by examination of medical charts. We also screened subjects’ BMI, heart rate, baseline electrocardiogram (ECG) and blood pressure. Quantification of disability in MS patients was determined by the EDSS (Sharrack & Hughes, 1996). The EDSS measure was administered by a consultant neurologist. No subject had undergone EDSS evaluation previously, and no EDSS score was reported in the medical charts. This basic scale quantifies disability by evaluating and assessing a score in eight neurological functional systems, namely pyramidal, cerebellar, brainstem, sensory, bowel and bladder, visual and cerebral. The EDSS score ranges from 0, which represents absence of clinical impairment to 10, which is the highest grade. An EDSS level of 3 represents a fully ambulatory patient with moderate disability, a score of 6 represents necessity for unilateral assistance with canes, crutches, or braces when required to walk 100 meters, and a score of 8 represents patients restricted to bed or chair or perambulated in a wheelchair. A total of 10 age and sex matched healthy and sedentary subjects (41.9 11.2 years) were included as a control group. Exclusion criteria for both the study groups included: pregnancy, morbid obesity as defined by BMI of 40 kg/m2 or more, cognitive impairment, cardiopulmonary disease, and orthopedic conditions prohibiting participation in safe exercise testing. The subjects’ characteristics are shown in Table 1. The perceived difficulty in carrying out daily living activities was assessed in all subjects, MS and Controls, using the Modified Fatigue Impact Scale (MFIS; Tellez et al., 2005). This approach is based on 21 items derived from interviews concerning how fatigue had impacted their lives over the preceding month. Administration time was approximately 5– 10 min for the full-length version. We administered the MFIS once before the testing sessions, and summary scores as well as physical, cognitive and psychosocial subscale scores were calculated. All examinations and tests were performed in a public rehabilitation facility. The study was designed in agreement with the Declaration of Helsinki, and was approved by the local Ethical Committee. All subjects volunteered for the study and informed written consent was obtained from all participants before the experimental set-up.
E. Guerra et al. / Research in Developmental Disabilities 35 (2014) 2527–2533
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Table 1 Subjects characteristics (mean SD).
Age (years) Years of disease Height (cm) Weight (kg) Body Mass index (BMI)
MS patients (n = 17)
Control group (n = 10)
Mean SD
Mean SD
47.8 10.6 6.8 5.1 164.5 10.7 65.1 15.8 24.1 3.3
41.9 11.3 – 165.7 10.9 64.9 13.4 23.6 4.2
2.1. Procedures All subjects attended two successive fitness evaluation sessions. In the first fitness testing session subjects underwent the Berg Balance Scale (Berg, Wood-Dauphinee, Williams, & Maki, 1992) and Six Minute Walking test (6MWT) whereas in the second session a strength test were performed. The Berg test consists of a 14 item scale, according to functional tasks deficits. The test duration is approximately 15 min, with 14 balance-related tasks including unsupported sitting, change of position, standing on one foot, standing with eyes closed. The Berg score ranges from 0, representing no balance capacity with high fall risk, to 4 (normal performance), with a maximum score of 56. In order to perform this test, a ruler, two standard chairs (one with arm rests, one without), a footstool or step, and a stopwatch are required. The Intraclass Correlation Coefficients (ICCs) for test–retest reliability range between 0.85 and 0.96, whilst the validity (r = 0.71) of the Berg scale has been assessed using a population of subjects with MS (Cattaneo et al., 2007; Cattaneo, Regola, & Meotti, 2006). Functional aerobic capacity (cardiovascular fitness) was measured by using the 6MWT. This test measures the distance that a patient can quickly walk on a flat, hard surface in a period of 6 min. It evaluates the global and integrated responses of all the systems involved during exercise, including the pulmonary and cardiovascular systems, systemic circulation, peripheral circulation, blood, neuromuscular units, and muscle metabolism. With this said however, it does not provide specific information on the function of each of the different organs and systems involved in exercise or the mechanism of exercise limitation. The self-paced 6MWT assesses the submaximal level of functional capacity, even if it involves a ‘‘maximal’’ request; the subjects are in fact invited to walk as many meters as they can. This test was performed in an enclosed 20 m corridor (Veloso-Guedes et al., 2011). Each meter was marked on the floor and a chair was present every 5 meters. Individuals were instructed to walk, back and forth, exerting maximal effort within the 6-min period at their own pace, but were continuously encouraged during this test (Broekmans et al., 2013). They could rest at any time during the test, but were encouraged to resume walking as soon as they were ready. The 6MVT has high reliability (ICC ranged between 0.80 and 0.90) and moderate validity (r = 0.56 to 0.88; Finch, Brooks, Stratford, & Mayo, 2002). Subjective perception of fatigue in this test was evaluated using the Borg 10-item scale (Borg, 1982). Maximum Isometric Voluntary Contraction (MIVC) was measured for the forearm muscles, shoulders elevators muscles and quadriceps muscles, in order to minimize the testing time (Gutierrez et al., 2005). Grip strength was measured using a programmed handgrip dynamometer (IBX H-101, MD Systems INC., Westerville, OH, USA). Standardized instruction and position were used, whilst 3 consecutive trials for each hand were recorded. Grip strength had excellent reliability with a measurement error of approximately 2 kg (Schreuders et al., 2003). The MIVC of the knee extensor muscles in both limbs was performed during the leg extension tests. Participants sat on a chair, with arms folded across the chest. A sitting iron support was prepared to adapt the sit to the length of the femur, in order to obtain a standard sit position. The trunk was erected and fastened using two crossing belts. Participants were instructed to exert maximal extension torque and to maintain it for 5 s. For extension the knee angle was positioned at 1108 (1808 refers to full extension), and the hip angle at 908. MIVC was calculated as the largest 1-s average reached within any single force recording. A total of 3 attempts were measured for both legs, with 2 min of rest between. Extension isometric torque was measured using a commercially available load cell (AEP elettronica, Italy) connected to a computerized system unit. Under the same sitting position but with arms hanging on their side, MIVC of the shoulder elevators was obtained by pulling a 20 cm iron bar connected in a series with the load cell. A target line was always set on the computer screen at a value 20% higher than the best performance. The participants were able to follow their performance on the computer screen. 3. Calculation Data were expressed as mean (SD). Descriptive statistics were used to characterize the participants and verify the distribution of variables. A one-way ANOVA was performed to assess significant differences between MS patients and the control group. If significant main effects were found, a Fisher’s LSD post hoc was performed. The relationship between investigated MS
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patient variables was analyzed using Pearson product-moment correlations (r). Forward stepwise linear regression (R2) was performed to identify the best predictive model of exercise capacity. All statistics were calculated using SPSS (SPSS version 20.0 Chicago). A significance level of p < 0.05 was adopted. 4. Results Seventeen patients with MS were evaluated. MS patients and controls were homogeneous at baseline for age and BMI. Of the patients, 10 showed Relapsing Remitting MS (RRMS), 6 had Secondary Progressive Course (SPMS), and 1 had only laboratory diagnosis of MS. A total of 6 subjects declined to perform the isometric strength tests, whereas 11 patients with MS underwent the strength testing sessions. Considering each dependent variable, the one-way ANOVA revealed significant differences between the two groups, for systolic blood pressure at baseline (F1.19 = 6.478; p < 0.05), diastolic blood pressure at baseline (F1.19 = 7.372; p < 0.05), MFIS (F1.19 = 9.420; p < 0.01), Berg (F1.19 = 13.125; p < 0.01), handgrip MIVC (F1.19 = 4.567; p < 0.05), lower limb MIVC (F1.19 = 7.429; p < 0.01), and 6MWT (F1.19 = 28.061; p < 0.01). No significant differences between groups were found for heart rate at baseline, heart rate at the end of exercise, delta of heart rate, or systolic and diastolic blood pressure at the end. Considering the strength tests for only the 11 MS patients who gave consent to perform MIVC, the following results were found: MICV leg extension(right-left) 29.2 18.9, MICV leg extension(dominant limb) 30.6 19.7 kg, range 4.87–78 kg, delta strength of lower limbs 23 16%, MICV handgrip(right-left) 24.2 10.7 kg, MICV handgrip(dominant limb) 25.07 12.8 kg, range 4.8–47.37 kg. MICV shoulder elevators(right-left) 30.3 17.3 kg, MICV shoulder elevators(dominant limb) 32.5 17.3 kg, range 10.5–66.88 kg. In comparison with controls, significant differences were found in handgrip and lower limb strength, whereas no significance was found for shoulder strength. The Fisher’s LSD post hoc results are shown in Table 2. Significant and large correlations were found between EDSS and HR at baseline (r = 0.620; p < 0.05), EDSS and 6MWT (r = 0.843; p < 0.01), as well as EDSS and Borg scores (r = 0.609; p < 0.05, and between 6MWT and Borg scores (r = 0.596; p = 0.053), and 6MWT and Berg (r = 0.716; p < 0.05). Handgrip, shoulder and lower limb MIVC were significantly correlated with each other (p < 0.01), and with the systolic blood pressure at the baseline (r = 0.806; r = 0.728; r = 0.653; p < 0.01, respectively). Results of linear regression analysis revealed a predictive model from the EDSS for Borg scores (R2 = 0.371, R2adj = 0.301; p < 0.05), for HR at baseline (R2 = 0.384, R2adj = 0.316; p < 0.05) and EDSS, for the cardiovascular fitness, assessed by 6MWT (R2 = 0. 711, R2adj = 0.679; p < 0.01); from 6MWT for Berg (R2 = 0.512, R2adj = 0.458; p < 0.05), and for Borg near the significance (R2 = 0.356, R2adj = 0.284; p = 0.053). The Delta MIVC of lower limbs was predictive of reduced balance evaluated by Berg test (R2 = 0.51, R2adj = 0.481; p < 0.05). The relationship between 6MWT scores and the other variables was further examined by multiple linear regressions, with adjustment for other covariates. EDSS, Berg test and Borg scores explained 80% 6MWT variation (R2 = 0.856, R2adj = 0.795; p < 0.01) whilst EDSS, 6MWT and Berg test 50%-Borg score variation (R2 = 0.657, R2adj = 0.511; p < 0.05). The results are shown in Fig. 1.
Table 2 Significant differences between MS patients, completing physical testing sessions, and Controls, according to ANOVA One-way test (*p < 0.05; ** p < 0.01). Variables
HR baseline HR at the end Delta HR Systolic blood pressure at baseline Systolic blood pressure at end Diastolic blood pressure at baseline Diastolic blood pressure at baseline MFIS BORG BERG Handgrip test Shoulder elevator test Leg extension test Right leg extension test Left leg extension test 6MW test
MS patients (n.11)
Control (n.10)
Variance
Mean SD
Mean SD
F
p
75.1 5.3 96.1 2.4 21.0 18.9 121.8 13.3 145.5 19.8 80.0 8.9 77.3 9.8 29.7 16.7 4.6 1.7 45.7 8.9 22.5 11.6 30.3 17.3 29.2 18.9 27.8 20.7 26.2 18.2 384.0 119.6
72.8 11.6 98.0 17.2 25.2 15.9 107.0 13.4 131.0 17.3 70.0 7.8 72.5 5.9 10.9 10.2 4.4 1.1 56.0 0.0 34.3 13.7 40.2 16.2 52.8 19.8 53.0 19.0 53.1 21.2 614.2 70.6
0.348 0.0538 0.300 6.478 3.145 7.372 1.770 9.420 0.143 13.125 4.567 1.7524 7.429 8.373 9.821 28.061
0.562 0.198 0.590 0.020* 0.092 0.014* 0.199 0.006** 0.709 0.002** 0.045* 0.202 0.014* 0.009** 0.005**
