Can amyotrophic lateral sclerosis patients with respiratory insufficiency exercise?
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1 Journal of the Neurological Sciences 169 (1999) locate/ jns Can amyotrophic lateral sclerosis patients with respiratory insufficiency exercise? a, b a b a Anabela C. Pinto *, Manuela Alves, Antonio Nogueira, Teresinha Evangelista, Joao Carvalho, a b b Antonio Coelho, Mamede de Carvalho, Maria Lurdes Sales-Luıs a Department of Medical Rehabilitation, Hospital de Santa Maria, Av. Prof. Egas Moniz, 1600 Lisboa, Portugal b Department of Neurology, Centro de Estudos Egas Moniz, Faculty of Medicine, Hospital de Santa Maria, Lisboa, Portugal Abstract The authors have shown in a recent paper that survival with amyotrophic lateral sclerosis (ALS) can be increased by the use of non-invasive methods of assisted ventilation (Bipap ). However, the progression of muscle weakness was not affected and the quality of life was not positively enhanced. In ALS, reduced physical activity may partially be secondary to alveolar hypoventilation syndrome. This leads to deconditioning of ALS/ motor neuron disease (ALS/ MND) patients. The authors decided to investigate the possibility of reducing motor decline by exercising these patients to the anaerobic threshold, but simultaneously compensating the respiratory insufficiency with the Bipap STD. We conducted a controlled single blind study, exercising eight consecutive ALS/ MND patients and used a control group of 12 ALS/ MND patients. The patients were all evaluated during a 1 year period. Respiratory function tests (RFT) were performed at entry and then at 6 month intervals. Barthel, Functional Independent Mobility scale (FIM) and Spinal and Bulbar Norris scores were recorded every 3 months. There was a significant difference between the two groups with respect to FIM scores (P, 0.03), but not Barthel scores (P, 0.8). A slower clinical course (Spinal Norris score P, 0.02) and a significant difference in the slope of the RFT (P, 0.008) were observed in the treated group, suggesting that exercise may be beneficial in ALS patients once Bipap is used to control peripheral and muscle oxygenation Elsevier Science B.V. All rights reserved. Keywords: Amyotrophic lateral sclerosis/ motor neuron disease; Respiratory insufficiency; Non-invasive ventilation (NIV); Respiratory function tests; Endurance exercise under non-invasive ventilation; Anaerobic threshold; Quality of life; Functional Independent Mobility scale (FIM) 1. Introduction the hypoventilation syndrome and responsible for the deconditioning of MND/ALS patients. We decided to Amyotrophic lateral sclerosis/ motor neuron disease investigate the possibility of reducing motor decline by (ALS/ MND) is a progressive and fatal disease in which the most common terminal event is respiratory insufficiency. Treatment of this terminal phase using various with the Bipap STD. methods of non-invasive ventilation is advised by many different authors [1 3], and has finally been accepted as exercising these patients to the anaerobic threshold, while at the same time compensating the respiratory insufficiency standard care for ALS/ MND patients [4,5]. However, all 2. Material and methods patients progress to quadriplegia with substantially reduced quality of life. Prolonging survival with independence in To test the effects of an exercise program on ALS/ activities of daily living is certainly a major goal in the MND patients, we conducted a prospective, single blind rehabilitation setting of ALS/ MND patients. controlled clinical trial of 20 consecutive patients. All Reduced physical activity may partially be secondary to patients gave their formal informed consent. Group 1 (treated group) included eight patients, six male and two female, with a mean age of years (mean6sd). *Corresponding author. Tel.: ; fax: address: jsanches.apinto@mail.telepac.pt (A.C. Pinto) Group 2 included 12 patients, four female and eight male, aged years (mean6sd). All patients were evalu X/ 99/ $ see front matter PII: S X(99)00218-X 1999 Elsevier Science B.V. All rights reserved.
2 70 A.C. Pinto et al. / Journal of the Neurological Sciences 169 (1999) ated at their visit following diagnosis and followed-up without the Bipap, and also weekly to evaluate the during 1 year. Respiratory Function Tests (RFT) were possibility of increasing the resistance of the treadmill. performed three times at 6 month intervals and Functional Exercise was applied with the goal of attaining an- Independent Mobility scale (FIM), Barthel, and Spinal and aerobic threshold in min. Exercise ceased when Bulbar Norris scores were each recorded at 3 month there was subjective fatigue using the clinical scale of intervals. Borg [6], leg pain, HR above 75% of rest values or Patients in group 1 were submitted to an exercise desaturation not correctable with increased Ipap parameter. program according to a ramp protocol in a treadmill, with The slopes of the different clinical evolution parameters the Bruce or Naughton protocol [6 8] according to their were evaluated (the ratio of the initial score minus the final initial endurance tests. All the patients in this group score by the number of months of evolution). Data were breathed with the assistance of a Bipap STD, with analysed to assess differences in clinical parameters becontinuous monitoring of end-tidal volumes, heart rate tween the two groups using the T-test, assuming unequal (HR) and oxygen saturation using a pulse oximeter (sp ) (Figs. 1 and 2). Exercise continued with increased inspiratory variances with a confidence interval of positive air pressure (I pap) when necessary and limited by lowering of end-tidal volumes or sustained drops of sp below 90%. All patients in group 1, with partial or 3. Results global respiratory insufficiency, started exercise after a period of about 0.5 h of non-invasive ventilation with the Clinical data, including respiratory function parameters, Bipap STD at rest, in order to re-establish normality of are presented in Tables 1 4, and the respective means, blood gases. standard deviations and t-tests with the P values are The assessed clinical parameters were as follows. Previ- presented in Table 5. Data from Barthel scores and ous evolution (time between onset of symptoms and first respective slopes are omitted because they were not found referral); RFT at initial observation and at 6 and 12 to be relevant, in fact we did not find any statistical months, including evaluation of volumes, output, input, significance between the two groups during the period of and blood gases; FIM and Barthel scales at 3 month this study (Table 6). intervals; Norris Spinal and Bulbar scores also at 3 month In group 1, at initial observation, two patients (2 and 4) intervals; spo at rest, during exercise and during the had global respiratory insufficiency (RI) at rest with P 2 CO2 recovery period for the initial endurance test with and over 50 mmhg and P below 80 mmhg. The remaining Fig. 1. A graphical representation of patient No. 4 with global respiratory insufficiency, starting with a period of rest under non-invasive ventilation with Bipap STD. Exercise started at 12:35 h and ended at 12:38 h, with substantially reduced sp.
3 A.C. Pinto et al. / Journal of the Neurological Sciences 169 (1999) Fig. 2. A graphical representation of the same patient, 2 months later, exercising for a longer period of 12 min without any substantial reduced sp course, under non-invasive ventilation with Bipap STD. and, of Table 1 Demographic characteristics and clinical evolution data for patients in group 1: Pre Ev, previous evolution time in months; FVC i, 2, 3, forced vital capacity at the initial observation and at 6 and 12 months; ScB i, 3, 6, 9, 12, Bulbar Norris scores at the initial observation and at 3 month intervals during a 1 year period; SlB 6, 9 and 12, Norris Bulbar slope at 6, 9 and 12 months Pat. Sex Pre FVC (%) Sl ScB SlB No. Ev FVC i 2 3 i M M M M F F M M Table 2 Clinical evolution data for patients in group 1: Sp i, 3, 6, 9, 12, Norris Spinal scores at initial observation and at 3 month intervals; FIM i, 3, 6, 9, 12, initial Functional Independent Mobility Scale and at 3 month interval observations; SlSp and SlFIM i, 3, 6, 9, 12, Norris Spinal and FIM slopes at initial observation and at 3 month intervals during a 1 year period Pat. Sp SlSp FIM SlFIM No. i i
4 72 A.C. Pinto et al. / Journal of the Neurological Sciences 169 (1999) Table 3 Demographic characteristics and clinical evolution data for patients in group 2. See Table 1 for abbreviations Pat. Sex Pre FVC (%) Sl ScB SlB No. Ev FVC i 2 3 i M M M M F F F M M F M M patients had normal blood gases or partial RI with P due to fatigue, with an inadequate response to exercise, lower than 90 mmhg and normal, or even lower than with desaturation (sp ) below 90% because of a small normal, P C. Patient 5 had completely normal RFT and inspiratory reserve with lowering of end-tidal volumes, but blood gases. All the patients in group 1 had a decreased other reasons were also noted (Table 7). tolerance to exercise on the treadmill compared with the Patients in group 2 were not submitted to the endurance established tolerance limits in an otherwise normal popula- test on the treadmill. Concerning inspiratory volumes (vital tion matched for age and sex. These patients, in the capacity) the two groups showed a significant difference beginning, could not exercise within the Bruce or Naugh- (P, 0.001) in the same direction to that observed for ton protocols. Only one patient attained stage 3, two FVC. patients attained stage 2 in the Naughton protocol and patients 2, 4, and 7 could not go beyond stage 1 (1.4 km/h with a ramp of 58). After adapting the Bipap STD, the latter patients attained stage 2 (2 km/h with a ramp of 108) 4. Discussion offering the possibility of being independent in daily activities. Six months later these three patients could work Non-invasive ventilation in neuromuscular diseases and in the Bruce protocol. The remaining patients improved in in MND/ALS patients is a well established technique the Naughton protocol with the exception of patient 8 [9 14]. There are many advantages of Bipap over because of an uncontrolled spasticity in the legs. Twelve invasive methods: it is less expensive, prolongs survival, months later the same patients in the Bruce and in the and improves quality of life, sleep and exercise tolerance. Naughton protocol remained stable and patient 8 was But some questions about non-invasive ventilation remain; wheelchair-bound, for the same reasons. The limiting particularly, when should this therapy be started? It is factors for progress in exercise resistance were essentially accepted that non-invasive ventilation should be started Table 4 Clinical evolution data for patients in group 2. See Table 2 for abbreviations Pat. Sp SlSp FIM SlFIM No. i i
5 A.C. Pinto et al. / Journal of the Neurological Sciences 169 (1999) Table 5 when its advantages are clear to the patient. This usually Differences between the two groups occurs when diurnal gas exchange is clearly disturbed. Group 1 Group 2 t-test Some authors [15 17] believe that nocturnal desatura- Mean 6SD Mean 6SD P values tion is the first sign of RI and has to be carefully evaluated to implement compensation when detected. Nevertheless, a Age controlled clinical trial with survival rates has not yet been Pre Ev reported. Gay and Daube, in 1991 [18], showed that only FVC i 76% % * FVC 6 66% % two-thirds of these patients had nocturnal desaturation and FVC 12 60% % only one-third RI. They also found that the best correlation Sl FVC * with survival was involvement of the inspiratory muscles, ScB i * evaluated by inspiratory and expiratory maximal pressures. ScSp i However, these are unreliable respiratory function parame- FIM i ScB ters since they are dependent on patient collaboration. ScSp We observed that, in five of eight patients in group 1, FIM * the limiting factor for exercising, when first tested (Table ScB ), was a definite desaturation with substantially reduced ScSp end-tidal volumes. Progressively increasing the Ipap param- FIM * ScB eter allowed patients to continue exercising to secondary ScSp * limiting factors such as leg pain, heart rate or generalised FIM * fatigue. The poor exercise tolerance at the beginning of SlSp this study, improved by the Bipap STD, implies that SlB non-invasive ventilation can be useful even sooner that SlFIM SlSp once believed. SlB As far as exercise in ALS/MND patients is concerned, it SlFIM is accepted [19 21] that exercise is useful when the SlSp * muscle strength is above 3 (MRC scale). We consider that SlB part of the rate of motor decline is due to deconditioning SlFIM and diminished respiratory reserve and have tested this hypothesis through exercise with simultaneous compensa- tion of respiratory symptoms using the Bipap STD. This Table 6 device monitors the end-tidal volumes allowing us to Differences between groups with respect to initial Barthel scores and at 3, increase the Ipap parameter as necessary to the limit of 6, 9 and 12 months pressure and patient comfort. Group 1 Group 2 t-test Reconditioning exercise up to anaerobic threshold in a P values Mean 6SD Mean 6SD normal population as well as in athletes, cardiac patients, COPD patients, paediatric patients and even in some Barthel i neuromuscular diseases is well tried [22 24]. The use of Barthel Barthel this protocol in ALS patients has not previously been Barthel described. Exercising patients to anaerobic threshold Barthel means exercising to the point of the exponential increase of blood lactate concentration [7,25] or to the point of Table 7 Clinical evolution data for patients in group 1 exercising on a treadmill. Progression in stages of the Bruce (B) or Naughton (N) protocol, without and with Bipap STD assistance initially and at 3, 6 and 12 months later. sp is the percentage oxygen saturation measured with a pulse oximeter at the end of the first exercising test (ET) without non-invasive assistance. 18 and 28Lim are the limiting factors to exercise without and with non-invasive ventilation Pat. Initial observation and exercise without Bipap Exercise with Bipap No. PaO P sp 2 aco2 O2 ET 18Lim ET i 28Lim ET 3 ET 6 ET (N) HR 3(N) HR 3(B) 4(B) 4(B) (N) Dessat 2(N) RI 3(N) 4(N) 4(N) (N) Dessat 3(N) Leg pain 4(N) 3(B) 3(B) (N) Dessat 2(N) RI 3(N) 3(N) 2(N) (N) Dessat 2(N) Dessat 3(N) 3(N) 3(N) (N) Fatigue 3(N) HR 4(N) 3(B) 3(B) (N) Dessat 2(N) Fatigue 4(N) 4(N) 3(N) (N) HR 2(N) Spastic 3(N) 2(N)
6 74 A.C. Pinto et al. / Journal of the Neurological Sciences 169 (1999) maximal oxygen uptake (V max.). The relationship of confirm this possibility. This may be particularly important this point to fatigue and the beginning of muscle overuse is in bulbar forms of ALS patients, where it is often said that also known. Froelicher [6] demonstrated a linear correla- non-invasive ventilation is less efficient because of the tion between V max. and heart rate. excessive amount of secretions in advanced stages of the Since VO max. is equal to the product HR 3 A 2V diff., disease [3,26]. 2 we considered it to be safe working within these limits, controlling simultaneously the pulse rate and the percentage of saturated O 2 (sp O ) with a simple pulse 2 oximeter (Vitalograph, Respironics). Exercising up to Acknowledgements anaerobic threshold is also the most efficient and least time The authors are indebted to Gasin Co, Medical Division consuming way of reconditioning, which we considered of Portugal, for cooperating with us with patient assiscritical in these patients. tance, and to Margarida Fernandes for secretarial support. When considering our results and the differences between the two groups (Table 5) significant differences between groups at initial observation in Norris Bulbar score (P, 0.004) and FVC (P, 0.01) were found. There References was far more bulbar involvement in group 1 patients than [1] Pinto AC, Evangelista T, de Carvalho M, Alves MR, Sales Luıs in group 2. For this reason we did not analyse survival ML. Respiratory assistance with a non-invasive ventilator (Bipap) in between the groups. Nevertheless, at the end of the trial MND/ALS patients: survival rates in a controlled trial. J Neurol Sci there was a positive trend towards reduced bulbar slope 1995;129: (P, 0.18) and a significant reduction in the rate of decline [2] Bach JR, Wang T. Non-invasive long term ventilatory support for of the FVC (P, 0.002) These results also suggest that individuals with spinal muscular atrophy and functional bulbar musculature. Arch Phys Med Rehabil 1995;76(3): exercise under non-invasive ventilation does not cause [3] Cazolli PA. Oppenheimer home mechanical ventilation for amyodeleterious effects in respiratory muscle function. The trophic lateral sclerosis: nasal compared to tracheotomy intermittent progressive decline in Bulbar Norris scores, related to positive pressure ventilation. J Neurol Sci 1996;129: neuronal loss, may be modulated, in part, by the progresrespiratory [4] Hopkins LC, Tatarian GT, Pianta TF. Management of ALS: sive disturbance of gas exchange in ALS patients. care. Neurology 1996;47(2):S When considering the parameters related to muscle force [5] Strong MJ. Discussion. In: Management of ALS: respiratory care. Neurology 1996;47(Suppl 2):S (Spinal Norris score) and quality of life (Barthel scores [6] Froelicher VF, Quaglietti S. In: Little, Brown and Co., editors, and FIM scores), both groups did not show significant Handbook of exercise testing, 1st ed., Boston, MA: Brown Co, differences at initial observation. Spinal Norris score 1996, pp detected significant differences at the end of the period of [7] Morris CK, Myers J, Froelicher VF. Kawagushi Normogram for observation (12 months), both in absolute values and in the exercise capacity using METS and age. J Am Coll Cardiol 1993;22: rate of decline (P, 0.02 and P, 0.02, respectively). [8] Myers J, Buchanan N, Smith D, Neutel J, Bowes E, Froelicher VF. The FIM scale was the first to detect changes with Individual ramp protocol in a treadmill. Observation on a new significance in absolute values at 6, 9 and 12 months protocol. Chest 1992;101: (P, 0.03, P, 0.02 and P, 0.03, respectively). The [9] Carey Z, Gottfried SB, Levy R. Ventilatory muscle support in poorer statistical meaning of this scale at the slopes (rate of respiratory failure with nasal positive pressure ventilation. Chest 1990;97: decline) might be due to its reduced specificity, but if one [10] Hechmatt JZ, Loh L, Dubowitz V. Night-time ventilation in neurocompares the percentage of the number of patients in- muscular disease. Lancet 1990;335: dependent in activities of daily living at the end of the [11] Rigault JY, Leroy F, Poncey C, Brun J, Mallet JF. Ventilation study in both groups we can clearly see that, in group 1, mecanique prolongee par voi nasale. Rev Mal Respir 1991;8:479 only 25% of the patients lost independence (FIM score 85. [12] Bach JR, Intintola P, Alba A, Holland IE. The ventilator assisted,90) and, in group 2, 43% of the patients lost indepen- individual: cost analyses of institutionalisation versus rehabilitation dence in activities of daily living during the same period of and home management. Chest 1992;101: observation. [13] Unterborn JN, Hill NS. Options for mechanical ventilation in In summary, in this small sample of ALS patients our neuromuscular diseases. Clin Chest Med 1994;15(4): results suggest that exercise should be recommended, even [14] Hill N. Long term nasal ventilation. Thorax 1995;50(6): [15] Evangelista T, de Carvalho M, Pinto AC, Sales Luıs ML. Phrenic when there is respiratory insufficiency, using Bipap assis- nerve conduction in amyotrophic lateral sclerosis. J Neurol Sci tance to control tissue oxygenation. Exercise testing is 1996;129:35 7. apparently a provocative method to anticipate disturbed [16] Piper AJ, Sullivan CE. Effects of long term nasal ventilation on gas exchanges that otherwise would only be apparent at the spontaneous breathing during sleep in neuromuscular and chest wall end stage of the disease [3]. We believe this signifies that disorders. Eur Respir J 1996;9(7): [17] Carvalho M, Matias T, Coelho F, Evangelista T, Pinto AC, Sales the prescription of non-invasive ventilation should be made Luıs ML. Motor neuron disease presenting with respiratory failure. J at an earlier stage. However, exercise testing was not Neurol Sci 1996;139: applied to patients in group 2 and further studies should [18] Gay PC, Daube JR, Litchy R. Effects of alteration in pulmonary
7 A.C. Pinto et al. / Journal of the Neurological Sciences 169 (1999) function and sleep variables on survival in ALS patients. Mayo Clin [23] Wolfson MR, Shaffer TH. Respiratory muscle: physiology, evalua- Proc 1991;66: tion and treatment. In: Cardiopulmonary physical therapy, Vol. 17, [19] Norris FH, Smith RA, Denys EH. The treatment of amyotrophic Mosby: Scott Irwin, 1996, pp lateral sclerosis. In: Cosi V, editor, ALS therapeutic, psychological [24] Leith DE, Bradley M. Ventilatory muscle strength and endurance and research aspects, New York: Plenum Press, training. J Appl Physiol 1976;41:508. [20] Muller EA. Influence of training and of inactivity on muscle [25] Brooks GA. The lactate shuttle during exercise and recovery. Med strength. Arch Phys Med Rehabil 1970;51: Sci Sports Exerc 1986;18: [21] Caroscio JT. Amyotrophic lateral sclerosis: the disease. In: Caroscio [26] Bach JR. Management of neuromuscular ventilatory failure by 24 JT, editor, ALS, New York: Thieme Medical Publishers, hours non-invasive intermittent positive pressure ventilation. Eur [22] Darbee J, Cerny F. Exercise testing and exercise conditioning for Respir Rev 1993;3: children with lung dysfunction. In: Pulmonary physical therapy and rehabilitation, 1996, pp
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