Muscle training in patients with pulmonary hypertension. a narrative review

Vicente Benavides-Cordoba; Martijn A Spruit

doi:10.25100/cm.v52i4.5163

. 2021 Dec 30;52(4):e2015163. doi: 10.25100/cm.v52i4.5163

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Muscle training in patients with pulmonary hypertension. a narrative review

Vicente Benavides-Cordoba ^1,^2,^✉, Martijn A Spruit ^3,^4,⁵

PMCID: PMC9067910 PMID: 35571592

Abstract

Patients with pulmonary hypertension present limited tolerance to exercise and aerobic capacity; which is reflected in the reduction in peak oxygen consumption and their functional performance. This intolerance to exercise has traditionally been attributed to cardiac and respiratory dysfunction. However, as it happens in other chronic diseases, lower-limb and respiratory muscle alterations are also involved in patients with pulmonary hypertension.

Increasing evidence suggests that physical exercise training is an efficient and safe strategy. The recommendation for light and moderate-intensity exercise is made within the framework of pulmonary rehabilitation, and its benefits have been previously described.

In diseases such as COPD, lower-limb muscle function, exercise tolerance and quality of life improve following exercise training. And just as with COPD, it is necessary to promote evidence-based interventions with pulmonary hypertension. This narrative review focuses on the evaluation, safety and efficacy of training the respiratory muscles and the muscles of upper and lower extremities in patients with pulmonary hypertension.

Keywords: Hypertension pulmonary, muscle strength, respiratory muscles, exercise.

Remark

1) Why was this study conducted?

Pulmonary hypertension is a disease that generates functional limitations from mild to severe, these limitations are a consequence not only of cardiovascular-pulmonary but also muscular compromise. For this reason, a narrative review was carried out in which it was intended to establish the safety, evaluation and training strategies of the respiratory and limb muscles according to the existing literature.

2) What were the most relevant results of the study?

According to the literature reviewed, limb and respiratory muscle training is safe and offers favorable results in aerobic capacity and health-related quality of life. The procedures must be correctly prescribed and it is recommended that they be part of a pulmonary rehabilitation program.

3) What do these results contribute?

These results synthesize the evaluation tools and safe training of respiratory muscles and upper and lower extremities according to the existing literature. As well as, it promotes the referral of patients with pulmonary hypertension to pulmonary rehabilitation programs according to the inclusion criteria.

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Introduction

Pulmonary hypertension is defined as an increase in pulmonary artery pressure ≥25 mm Hg at rest ¹ . Pulmonary hypertension is a pathophysiological disorder that involves different clinical conditions; it can be a complication of most respiratory and cardiovascular disorders ² .

Patients with pulmonary hypertension present limited tolerance to exercise and aerobic capacity ³ , which is reflected in the reduction in peak oxygen consumption (VO2peak), as well as in their functional performance evaluated with the six-minute walk test (6MWT) ⁴ . This intolerance to exercise has traditionally been attributed to cardiac and respiratory dysfunction ⁵ . However, as it happens in other chronic diseases ⁶ , lower-limb and respiratory muscle alterations are also involved in patients with pulmonary hypertension ⁵ ^, ⁷ ^, ⁸ .

Increasing evidence and recommendations from the American Thoracic Society and the European Respiratory Society suggest that physical exercise training is an efficient and safe strategy. The recommendation for light and moderate-intensity exercise is made within the framework of pulmonary rehabilitation. Its benefits have been previously described ⁹ .

In diseases such as COPD, lower-limb muscle function, exercise tolerance, and quality of life improve following exercise training ¹⁰ ^, ¹¹ . Moreover, just as with COPD, pulmonary hypertension,it is necessary to promote evidence-based interventions with pulmonary hypertension. This narrative review focuses on the safety and efficacy of training the respiratory muscles and the muscles of the upper and lower extremities in patients with pulmonary hypertension.

Lower-limb muscle dysfunction

Lower-limb muscle weakness occurs in patients with pulmonary hypertension ⁵ . This weakness is associated with dyspnea, angina, and syncope, inducing physical activity restriction. Furthermore, as the disease progresses, Health-related quality of life decreases, and functional limitations increase, causing alterations in physical health that restrict the social function of patients ¹² ^, ¹³ .

In COPD ¹⁴ , there is a shift from type I fibers, which have a high mitochondrial intensity and oxidative capacity, to type II fibers, which are faster fibers with less resistance to fatigue and completely depend on anaerobic metabolism ¹⁵ . It has been suggested that these changes also occur in pulmonary hypertension due to the finding that type IIx fibers displace type I fibers, which have an inverse correlation with the duration of the disease ¹⁶ . Also, in pulmonary hypertension, the decrease in AKT and p70S6 with an increase in atrogin-1 has been identified as a relevant factor in muscle proteolysis with depression of networks that mediate hypertrophy. In addition to the phosphorylation of the ryanodine 1 receptor, which suggests the alteration of the sarcoplasmic reticulum directly involved in the production of Ca ++ ¹⁶ . At a molecular level, there have also been identified a decrease in the extracellular signal-regulated kinase ERK, microRNA 126, and an increase in sprout-related EVH1 ¹⁷ .

The changes produced in the muscle may affect tropism, contractility, capillarity, and oxidative capacity. However, these alterations are not yet evident and defined ¹⁸ . An increase in the expression of E3 ligases MAFbx/atrogin-1 and MURF-1 has been found, which are considered markers of activating the ubiquitin-proteasome pathway in muscles; causing reduction of transverse fibers and degradation of myofibrillar proteins ¹⁹ .

Contractility is possibly altered by an increase in ryanodine receptor one phosphorylation, which alters the integration of muscle excitation-contraction ¹⁶ . Likewise, mitochondrial density and its oxidative capacity ¹⁸ and reduced capillarity secondary to endothelial dysfunction are critical in the reduction in muscle performance present in patients with pulmonary hypertension, a situation that widely compromises their functionality and, therefore, their health-related quality of life.

Patients with pulmonary hypertension demonstrated a decreased type I/type II muscle fiber ratio and a smaller cross-sectional area of myofibres type I compared to healthy subjects ¹⁶ . As well as an increase in RyR1 phosphorylation, which functions as a channel in which calcium is released from the sarcoplasmic reticulum towards the cytosol, in order to induce muscle contraction; hyperphosphorylation induces leakage, suggesting impaired sequestration ¹⁶ . It has also been found that the increase in the expression of the MuRF1 protein is not only due to physical inactivity (as it happens in healthy subjects) but also as a consequence of the increase in pulmonary vascular resistance ²⁰ .

Lower-limb muscle atrophy leads to weakness, this increases the structural degradation of myofibrils and some proteins ²¹ . All these structural changes cause functional alterations and consequently the compromise of the performance of daily activities associated with symptoms ²² and quality of life of patients ¹⁶ with respiratory and limb muscle damage ¹⁹ . Consequently, muscle training emerges as a strategy to implement pulmonary rehabilitation programs. Physical exercise appears to be safe and effective, which is why there is a need to establish specialized programs for patients with pulmonary hypertension ²³ ^- ²⁵ .

Patients with pulmonary hypertension are physically inactive, associated with a higher risk of hospitalization ²⁶ . Moreover, as physical inactivity may be one of the main drivers of lower-limb muscle weakness in patients with pulmonary hypertension, measuring physical activity levels seems of clinical importance ²⁷ ^, ²⁸ . This also provides a clear rationale for why exercise-based interventions are effective in patients with pulmonary hypertension to increase muscle function and exercise tolerance and quality of life.

Respiratory muscle dysfunction

Patients with stage II-IV pulmonary hypertension reduce muscle strength compared to healthy individuals (25% less) ²⁹ . For being progressive, pulmonary hypertension results in a reduction in aerobic capacity and the strength of respiratory muscles ³⁰ . It has been identified that functional aerobic capacity is directly related to muscle strength in patients with pulmonary hypertension; diaphragmatic dysfunction has been reported in animal models and patients who suffer from exercise intolerance; in rats with pulmonary hypertension by the monocrotaline model, the contraction and the generation of the maximum tetanic force of the diaphragm were lower. The transverse fiber of the diaphragm was significantly smaller in pulmonary hypertension rats ³¹ ^, ³² . In addition, histologically, there have been reported weakness and atrophy in the respiratory muscles of patients with pulmonary hypertension; a situation that strengthens the concept that this respiratory muscle dysfunction contributes to dyspnea and fatigue while exercising ³³ .

The maximum inspiratory and expiratory pressure values have been related to the distance in the 6-minutes walk test ⁸ . Furthermore, pulmonary hypertension patients have been shown to experience hyperventilation both at rest and during exercise ³⁴ ^, ³⁵ . Continuous muscle activity increases energy demand and reduces force-generating capacity; therefore, it is possible to infer that this direct relationship should promote the training of the respiratory muscles, and thus, indirectly, there will be an improvement in the aerobic capacity and in the functionality of the patients.

Evaluation

The evaluation of the patients should include a complete review of the medical history, including sociodemographic and clinical aspects such as dyspnea on exercise ⁽ ³⁶ and health-related quality of life ³⁷ . Furthermore, the evaluation of functional aerobic capacity has been included in various studies of patients with pulmonary hypertension ³⁸ ^, ³⁹ . It is recommended that the same physical therapist perform the evaluations weekly.

Muscle evaluation involves instrumental strategies with mostly objective results; the alternatives are described in Figure 1. For the evaluation of the extremities, the arm ergometer, the 6-minute pegboard and ring test, and the one-repetition maximum have been used in the upper limbs. In lower limbs, the contractile leg fatigue, the one-maximum repetition and for deep analysis the quadriceps tomography and the biopsy for molecular tests. The evaluation of respiratory muscles is carried out mainly with a manovacuometer in which maximum inspiratory pressure and maximum expiratory pressure are obtained. Each of the tools described are described in detail below.

Lower and upper-limb muscle function

For evaluating lower-limb strength, simple strategies such as one repetition maximum test are used, up to measurements that require specialized equipment such as computed tomography. The one-repetition maximum test is defined as the maximum weight that can be lifted with proper technique; in patients with COPD and other comorbidities, it is considered the gold standard in situations where laboratory tests cannot be performed. It is a well-tolerated and easily accessible test ⁴⁰ ^, ⁴¹ . The test consists of a warm-up with ten reps at a lightweight, followed by a 2-minutes rest period prior to the one-repetition maximum test. The initial weight is calculated according to the body weight and is progressively increased until reaching the maximum. A 60 second rest period is recommended between measurements ⁴² ^, ⁴³ .

Regarding specific assessments of lower-limb muscle strength, contractile leg fatigue after cycling has been used to assess nonvolitional and volitional strength in the quadriceps ⁴⁴ . During maximal voluntary contraction, patients sustain isometric force to the maximum possible for three seconds; signals are amplified and recorded in software ⁴⁵ .

Quadriceps function in pulmonary hypertension has also been assessed with hydraulic dynamometry ⁴⁶ ; patients are positioned in hip flexion at 90°, knee flexion at 70°; the transducer is located approximately 10 cm above the medial malleolus. A maximum voluntary contraction is measured by making five attempts with a 1-minute pause between each attempt ⁴⁷ .

Assessment by computed tomography, especially in the quadriceps, has also been included. In addition, a muscle biopsy has been used from the non-dominant side to identify muscle capillarity and the enzymatic activity of the quadriceps ⁴⁴ . Nevertheless; These measurements are more related to research, and their clinical applicability is reduced significantly in countries with difficult access to diagnostic tools.

For upper limbs, in addition to the evaluation of a maximum repetition, the 6-minute pegboard and ring test has been used, in which the subjects must move rings ranging from 14 to 50 grams, as far as possible in 6 minutes, and the score was the number of rings moved during this time period.

Respiratory muscle function

Regarding the evaluation of respiratory musculature, the measurement of maximum inspiratory pressure and maximum expiratory pressure has been used in studies that include patients with pulmonary hypertension ²⁹ ^, ⁴⁸ ^, ⁴⁹ .

These evaluations are carried out with pressure devices that contain mouthpieces to make the measurements; the maximum inspiratory pressure maneuver is performed from a maximum expiration close to residual volume and the maximum expiratory pressure after a maximum inspiration. The maximum inspiratory pressure and maximum expiratory pressure values are calculated from the maximum sustained effort for one second; the tests are repeated until higher values are achieved with a difference of 10%; however, other authors consider performing three to five repetitions and taking the highest value of the tests performed ³⁰ ^, ³³ . The sniff nasal pressure measurement has also been used by performing it from the residual functional capacity ⁴⁹ ^, ⁵⁰ (Figure 1).

Training

Limb muscle training

Low to moderate intensity exercises have shown safety in patients with pulmonary hypertension. It has been identified that training can improve exercise capacity and health-related quality of life. To start with the training protocols, patients are receiving their pharmacological therapies and are supervised, minimizing complications ⁴ . Step climbing unsupported arm/leg exercises with and without dumbbells; use of circuits that involve large muscle groups using specific equipment for strengthening, such as leg and bench press, leg extension, lateral pulldown, and abdominal crunches ⁵¹ . It has also been reported that strength training in the quadriceps should be progressive, and it depends on what was obtained in the initial evaluations, starting in the first week with three sets of 12 repetitions at 50% of the one-repetition maximum test and progressing to 75% at week 7, until reaching week 12 with the same series and repetitions. Regarding resistance, the number of repetitions is increased to 30, also three series, but starting in week one at 30% of the one-repetition maximum test and progressing to 40% in week 7, also until reaching week 12 ⁴⁶ .

For the upper extremities, dumbbell workouts with low weight (500-1000 g) have been reported, focused on muscles independently ⁵¹ ^, ⁵² ; for 30 minutes, five times a week during 12 weeks; this could be due to the intention of carrying out safe activities that avoid as much as possible the appearance of complications related to musculoskeletal alterations and also to the heart-lung interaction ⁵³ .

One of the most reported results is the relative decrease in type IIx fibers after muscular training in pulmonary rehabilitation. This result is strongly correlated with the decrease in CO₂ production ⁴⁴ ; results that have been identified not only in pulmonary arterial hypertension patients but also in chronic thromboembolic pulmonary hypertension patients who also improved their functional aerobic capacity and quality of life ⁵² .

It has been reported that after training, there is an improvement in the distribution of muscle fibers ²³ , Activities as bicycle ergometer with continuous (30 min 50% peak workload) and interval training (1 min high/30 slow; 10-25 min; 10-60 W; with intensity 60-80% peakVO2); progressive increase during program ⁵⁴ ^, ⁵⁵ . The specific training of the quadriceps has caused improvement in the performance and muscular function, this improvement consequence of morphological changes through the increase in the capillarization and the oxidative enzymatic activity evaluated with vastus lateralis biopsy ⁴⁶ ^, ⁵⁶ .

Neuromuscular electrical stimulation has been used as an intervention in patients with chronic pulmonary disorders and is an alternative for those who do not have enough capacity to participate in moderate to high-intensity exercise programs ⁵⁷ . This method is passive and more tolerable for patients with severe symptoms resulting from a low metabolic load on the cardiorespiratory system ⁵⁸ ^, ⁵⁹ .

In pulmonary hypertension, although there is little evidence to support its use; An 8-week study used Neuromuscular electrical stimulation on quadriceps and delts with 50 Hz frequency in 350 μs pulses over an on: off duty cycle, which was increased weekly from 2:15 s to 5:20 s to 10:15 s. The intensity was increasing according to the tolerance of the patient. The protocol was scheduled for 40 minutes a day three days a week. The intervention improved peripheral muscle strength, muscle cross-sectional area and thickness, arterial stiffness, exercise capacity, functional mobility, balance, balance confidence, physical activity level, and quality of life in patients with pulmonary arterial hypertension ⁵⁹ .

In general, muscle training promotes the increase of the maximum and peak oxygen consumption; as well the reduction of symptoms during exercise measured with the Borg scale; likewise, at the hemodynamic level, changes in heart rate and systolic and diastolic pressures demonstrate benefits that range from functional to structural, with molecular and clinical changes ⁴³ ^, ⁵⁵ .

When the results obtained are integrated, it has been found that strength training improves Health-related quality of life when evaluated with questionnaires such as CAMPHOR and SF36; changes generally occur in physical, mental, health perception, bodily pain, and vitality functions ⁴³ ^, ⁵⁵ ^, ⁶⁰ .

When training patients with a disease such as pulmonary hypertension, which has a high compromise in the cardiovascular and pulmonary system, with a high risk of complications, adverse effects are a risk. There have been reports of patients with syncope that can generally appear hours after training and episodes of tachycardia in patients with a history of arrhythmia; however, these adverse events did not transform into clinical worsening of heart failure resolved quickly. Continuous monitoring and training by highly trained personnel is the best way to mitigate these risks.

Respiratory muscle training

The patients that have been reported to benefit from respiratory muscle training are those with moderate ⁴⁸ and even with severe pulmonary hypertension ⁶¹ ; due to the severity and cardiovascular compromise of the patients, the prescription must be carried out safely and effectively.

According to the evidence reviewed, the threshold inspiratory muscle training device is the most used to train muscles involved in inspiration, using loads of 30% of maximum inspiratory pressure for 30 minutes 7 days a week for six weeks ³⁰ . The threshold inspiratory muscle training allows training in a range from 9 cm H₂O to 41 cm H₂O. the loads generally start at 30% of the maximum inspiratory pressure; 15-minute workouts are reported twice a day for eight weeks, five days a week ⁴⁸ .

Training activities that are accompanied by respiratory therapy performed five times a week have also been included. Other activities, including exercises to stretch the muscles related to breathing and trunk muscles, techniques such as pursed lips and conscious modulation of breathing patterns ⁴⁹ , and yoga techniques (Ujjayi breathing), which have been shown to improve baroreflex sensitivity in a healthy population ⁶² .

Continuous monitoring of hemodynamic variables is required to perform the procedures while the intervention is being performed. The cut-off point is suggested at ≤130/min in heart rate. Regarding the peripheral oxygen saturation, a saturation value ≤85% is considered to decide to reduce the intensity; in cases where saturation decreases, the patients can receive supplemental oxygen during the performance of the procedures, which can be delivered utilizing low or high flow ⁶³ .

It has been reported that the addition of respiratory muscle training to the functional treatment of the upper and lower extremities offers more significant benefits to the improvement in the function of the muscles that are involved, also the positive benefits in the cardiocirculatory system, quality of life and the reduction of dyspnea during exercise ⁶¹ . However, another study showed that performing muscle training with a threshold inspiratory muscle training device five days a week for 15 minutes, twice a day, only managed to improve the strength of the respiratory muscles, but no other parameters (quality of life and symptoms). This result may reinforce the idea that muscle training should be carried out in both respiratory muscles and limb muscles; and that the benefits are obtained with localized training accompanied by global training ⁴⁸ (Table 1).

Table 1. Strategies and observations for muscle training in patients with pulmonary hypertension.

Region	Strategy	Observations
Respiratory Muscles	Threshold inspiratory muscle training device	Allows training in a range from 9 cm H₂O to 41 cm H₂O. the loads generally start at 30% of the maximum inspiratory pressure ⁸ ^, ³⁰
Lower Limbs	Specific equipment for strengthening	Leg and bench press, leg extension, and lateral pulldown; starting in the first week with 3 sets of 12 repetitions at 50% of the one repetition maximum test and progressing to 75% at week 7 for strength ⁴⁶ ^, ⁵¹
Lower Limbs	For resistance, the number of repetitions is increased to 30, also 3 series, but starting in week 1 at 30% of the one repetition maximum test and progressing to 40% in week 7 ⁴⁶ .
Upper Limbs	Dumbbell workouts	Low weight (500 - 1000 gr) have been reported, focused on muscles independently for 30 minutes, five times a week during 12 weeks. Making increments according to the patient's response ⁴ ^, ⁵¹ ^, ⁵³

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Conclusion

There are several alternatives for muscle testing and training in pulmonary hypertension. Muscle training in patients with pulmonary hypertension has been shown to be safe and effective; the selection of the appropriate patient, based on the severity of the disease, taking into account the values obtained in the right heart catheterization, imaging, biomarkers, and functional classification of patients; promoting early inclusion in training programs, which may be within the framework of pulmonary rehabilitation; is essential to choose forms of assessment and intervention.

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Colomb Med (Cali). 2021 Dec 30;52(4):e2015163. [Article in Spanish]

Entrenamiento muscular en pacientes con hipertensión pulmonar, una revision narrativa

Contribución del estudio

1) ¿Por qué se realizó este estudio?

La hipertensión pulmonar es una enfermedad que genera limitaciones funcionales que van desde leves a severas, estas limitaciones son consecuencia no solamente por el compromiso cardiovascular-pulmonar sino también muscular. Por esto, se realizó una revisión narrativa en la que se pretendió establecer la seguridad, las estrategias de evaluación y de entrenamiento de los músculos respiratorios y de extremidades de acuerdo a la literatura existente.

2) ¿Cuáles fueron los resultados más relevantes del estudio?

De acuerdo a la literatura revisada, el entrenamiento muscular de extremidades y de músculos respiratorios es seguro y ofrece resultados favorables en la capacidad aeróbica y la calidad de vida relacionada con la salud. Los procedimientos deben ser prescritos correctamente y se recomienda se enmarquen dentro de un programa de rehabilitación pulmonar.

3)¿Qué aportan estos resultados?

Estos resultados sintetizan las herramientas de evaluación y entrenamiento seguro de los músculos respiratorios y de extremidades superiores e inferiores de acuerdo a la literatura existente. Así como también, promueve la remisión de los pacientes con hipertensión pulmonar a los programas de rehabilitación pulmonar de acuerdo al cumplimiento de los criterios de inclusión.

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Introducción

La hipertensión pulmonar se define como un aumento de la presión de la arteria pulmonar ≥25 mm Hg en reposo¹. Es un trastorno fisiopatológico que involucra diferentes condiciones clínicas; y puede ser una complicación de la mayoría de los trastornos respiratorios y cardiovasculares².

Los pacientes con hipertensión pulmonar presentan limitada tolerancia al ejercicio ³, lo que se refleja en la reducción del consumo pico de oxígeno (VO2pico), así como en su desempeño funcional evaluado con el test de caminata de seis minutos (6MWT)^{(4 )}. Esta intolerancia al ejercicio, ha sido tradicionalmente atribuida a disfunciones cardíacas y respiratorias⁵. Sin embargo, como sucede con otras enfermedades pulmonares crónicas⁶, las alteraciones de los músculos respiratorios y de los músculos de extremidades superiores e inferiores también están involucradas ⁵^,⁷^,⁸.

La creciente evidencia y recomendaciones de la American Thoracic Society y la European Respiratory Society, sugieren que el entrenamiento físico es una estrategia eficiente y segura. La recomendación de ejercicio de intensidad ligera y moderada se realiza en el marco de la rehabilitación pulmonar. Sus beneficios han sido descritos previamente⁹.

En enfermedades como la EPOC, la función muscular de las extremidades inferiores, la tolerancia al ejercicio y la calidad de vida mejoran después del entrenamiento físico ⁽¹⁰^,¹¹⁾. Además, al igual que con la EPOC, en hipertensión pulmonar, es necesario promover intervenciones basadas en la evidencia. Esta revisión narrativa se centra en la seguridad y eficacia del entrenamiento de los músculos respiratorios y de las extremidades superiores e inferiores en pacientes con hipertensión pulmonar.

Disfunción muscular de miembros inferiores

La debilidad de los músculos de las extremidades inferiores se presenta en pacientes con hipertensión pulmonar⁵. Esta debilidad se asocia con disnea, angina y síncope, lo que induce a la restricción de la actividad física. Además, a medida que la enfermedad progresa, la calidad de vida relacionada con la salud disminuye y aumentan las limitaciones funcionales, provocando alteraciones en la salud física que restringen la función social de los pacientes¹²^,¹³.

En la EPOC¹⁴, las fibras tipo I, que tienen una alta intensidad mitocondrial y capacidad oxidativa, se convierten en fibras tipo II, que son fibras más rápidas, con menor resistencia a la fatiga y totalmente dependientes del metabolismo anaeróbico¹⁵. Se ha sugerido que estos cambios también ocurren en la hipertensión pulmonar, con el desplazamiento de fibras tipo I por fibras tipo IIx, con una correlación inversa con la duración de la enfermedad¹⁶. Además, en la hipertensión pulmonar, la disminución de AKT y p70S6 con aumento de atrogina-1 se ha identificado como un factor relevante en la proteólisis muscular con depresión de las redes que median la hipertrofia. Además de la fosforilación del receptor de rianodina 1, lo que sugiere la alteración del retículo sarcoplásmico directamente involucrado en la producción de Ca++¹⁶. A nivel molecular, también se ha identificado una disminución de la quinasa regulada por señal extracelular ERK y microRNA 126¹⁷.

Los cambios producidos en el músculo pueden afectar el trofismo, la contractilidad, la capilaridad y la capacidad oxidativa. Sin embargo, esas alteraciones aún no son evidentes y definidas¹⁸. Se ha encontrado un aumento en la expresión de las ligasas E3 MAFbx/atrogin-1 y MURF-1, que se consideran marcadores de activación de la vía ubiquitina-proteosoma en los músculos; provocando la reducción de las fibras transversales y la degradación de las proteínas miofibrilares¹⁹.

La contractilidad es posiblemente alterada por un aumento en la fosforilación del receptor de rianodina, lo que cambia la integración de la excitación-contracción muscular¹⁶. Asimismo, la densidad mitocondrial y su capacidad oxidativa¹⁸⁾y la capilaridad reducida secundaria a la disfunción endotelial son fundamentales en la reducción del rendimiento muscular que presentan los pacientes con hipertensión pulmonar, situación que compromete su funcionalidad y, por tanto, su calidad de vida relacionada con la salud.

Los pacientes con hipertensión pulmonar presentan disminución de la proporción de fibras musculares tipo I/tipo II y un área transversal más pequeña de miofibras tipo I en comparación con sujetos sanos¹⁶. También, el aumento en la fosforilación de RyR1, que funciona como un canal en el que se libera calcio desde el retículo sarcoplasmático hacia el citosol, con el fin de inducir la contracción muscular; la hiperfosforilación induce fugas, lo que sugiere un secuestro alterado¹⁶. También se ha encontrado que el aumento en la expresión de la proteína MuRF1 no solo se debe a la inactividad física (como ocurre en sujetos sanos) sino también como consecuencia del aumento de la resistencia vascular pulmonar²⁰.

La atrofia de los músculos de los miembros inferiores conduce a la debilidad, lo que aumenta la degradación estructural de las miofibrillas y algunas proteínas²¹. Todos estos cambios estructurales provocan alteraciones funcionales y consecuentemente el compromiso de la realización de las actividades diarias asociadas a los síntomas²²⁾y la calidad de vida de los pacientes¹⁶⁾con daño muscular respiratorio y de las extremidades¹⁹. En consecuencia, el entrenamiento muscular surge como una estrategia para implementar en programas de rehabilitación pulmonar. El ejercicio físico parece ser seguro y eficaz, por lo que existe la necesidad de establecer programas especializados para pacientes con hipertensión pulmonar²³^-²⁵.

Los pacientes con hipertensión pulmonar son físicamente inactivos, asociados a un mayor riesgo de hospitalización²⁶. Además, dado que la inactividad física puede ser uno de los principales impulsores de la debilidad de los músculos de las extremidades inferiores en pacientes con hipertensión pulmonar, medir los niveles de fuerza parece tener importancia clínica²⁷^,²⁸. Esto también proporciona una justificación clara de por qué las intervenciones basadas en el ejercicio son efectivas en pacientes con hipertensión pulmonar para aumentar la función muscular, la tolerancia al ejercicio y la calidad de vida.

Disfunción de los músculos respiratorios

Los pacientes con hipertensión pulmonar estadio II-IV tienen reducción de la fuerza muscular en comparación con individuos sanos (25% menos)²⁹⁾Por ser progresiva, la hipertensión pulmonar resulta en una reducción de la capacidad aeróbica y de la fuerza de los músculos respiratorios³⁰⁾. Se ha identificado que la capacidad aeróbica funcional está directamente relacionada con la fuerza muscular en pacientes con hipertensión pulmonar; se ha documentado disfunción diafragmática en modelos animales y pacientes que padecen intolerancia al ejercicio; en ratas con hipertensión pulmonar por el modelo de monocrotalina, la contracción y la generación de la fuerza tetánica máxima del diafragma fueron menores. La fibra transversal del diafragma fue significativamente más pequeña en ratas con hipertensión pulmonar ³¹^,³². Además, se han reportado debilidad y atrofia en los músculos respiratorios de pacientes con hipertensión pulmonar; situación que refuerza el concepto de que esa disfunción de los músculos respiratorios, contribuye a la disnea y la fatiga durante el ejercicio³³.

Los valores de presión inspiratoria y espiratoria máxima han sido relacionados con la distancia en la prueba de marcha de 6 minutos⁸. Además, se ha demostrado que los pacientes con hipertensión pulmonar experimentan hiperventilación tanto en reposo como durante el ejercicio³⁴^,³⁵. La actividad muscular continua aumenta la demanda de energía y reduce la capacidad de generación de fuerza; por lo tanto, es posible inferir que esta relación directa debe promover el entrenamiento de los músculos respiratorios, y así, indirectamente, habrá una mejora en la capacidad aeróbica y en la funcionalidad de los pacientes.

Evaluación

La evaluación de los pacientes debe incluir una revisión completa de la historia clínica, incluyendo aspectos sociodemográficos y clínicos como la disnea de ejercicio ³⁶ y la calidad de vida relacionada con la salud³⁷. Además, la evaluación de la capacidad aeróbica funcional ha sido incluida en varios estudios de pacientes con hipertensión pulmonar³⁸^,³⁹. Para mejores resultados, se recomienda que el mismo fisioterapeuta realice las evaluaciones semanalmente.

La evaluación muscular implica estrategias instrumentales con resultados mayoritariamente objetivos; las alternativas se describen en la Figura 1. Para la evaluación de las extremidades se han utilizado en los miembros superiores el ergómetro de brazos, el 6-minute pegboard and ring test y la repetición máxima. En miembros inferiores, la contráctil leg fatigue, la repetición máxima y para análisis profundos la tomografía de cuádriceps y la biopsia para pruebas moleculares. La evaluación de los músculos respiratorios se realiza principalmente con un manovacuómetro con el que se obtienen la presión inspiratoria máxima y la presión espiratoria máxima. Cada una de las herramientas se describen en detalle a continuación.

Función de los músculos de las extremidades inferiores y superiores

Para evaluar la fuerza de los miembros inferiores, se utilizan estrategias simples, como la prueba de una repetición máxima, hasta mediciones que requieren equipos especializados, como la tomografía computarizada. La prueba de una repetición máxima se define como el peso máximo que se puede levantar con la técnica adecuada; en pacientes con EPOC y otras comorbilidades, se considera el estándar de oro en situaciones en las que no se pueden realizar pruebas de laboratorio. Es una prueba bien tolerada y de fácil acceso⁴⁰^,⁴¹. La prueba consiste en un calentamiento con diez repeticiones en un peso ligero, seguido de un período de descanso de 2 minutos antes de la prueba máxima de una repetición. El peso inicial se calcula en función del peso corporal y se va aumentando progresivamente hasta alcanzar el máximo. Se recomienda un período de descanso de 60 segundos entre las mediciones⁴²^,⁴³.

Con respecto a las evaluaciones específicas de la fuerza de los músculos de las extremidades inferiores, la contractile leg fatigue after cycling se ha utilizado para evaluar la fuerza volitiva y no volitiva en los cuádriceps⁴⁴. Durante la contracción voluntaria máxima, los pacientes mantienen la fuerza isométrica al máximo posible durante tres segundos; las señales son amplificadas y registradas en software⁴⁵.

La función del cuádriceps en la hipertensión pulmonar también ha sido evaluada con dinamometría hidráulica⁴⁶; los pacientes se colocan en flexión de cadera a 90°, flexión de rodilla a 70°; el transductor se encuentra aproximadamente 10 cm por encima del maléolo medial. Una contracción voluntaria máxima se mide haciendo cinco intentos con una pausa de 1 minuto entre cada intento⁴⁷.

También se ha incluido la valoración por tomografía computarizada, especialmente en el cuádriceps. Además, se ha utilizado una biopsia muscular del lado no dominante para identificar la capilaridad muscular y la actividad enzimática del cuádriceps⁴⁴⁾. Sin embargo; Estas medidas están más relacionadas con la investigación y su aplicabilidad clínica se reduce significativamente en países con difícil acceso a herramientas de diagnóstico.

Para miembros superiores, además de la valoración de una repetición máxima, se ha usado el 6-minute pegboard and ring test, en el que los sujetos deben mover anillos que van desde 14 a 50 gramos, como fuera posible en 6 minutos, y la puntuación era el número de anillos movidos durante este período de tiempo.

Función de los músculos respiratorios

En cuanto a la evaluación de la musculatura respiratoria, la medición de la presión inspiratoria máxima y la presión espiratoria máxima ha sido utilizada en estudios que incluyen pacientes con hipertensión pulmonar²⁹^,⁴⁸^,⁴⁹.

Estas evaluaciones se realizan con dispositivos de presión que contienen boquillas para realizar las mediciones; la maniobra de presión inspiratoria máxima, se realiza a partir de una máxima espiración cercana al volumen residual y la presión espiratoria máxima tras una máxima inspiración. Los valores de presión inspiratoria máxima y presión espiratoria máxima se calculan a partir del esfuerzo máximo sostenido durante un segundo; se repiten las pruebas hasta alcanzar valores superiores con una diferencia del 10%; sin embargo, otros autores consideran realizar de tres a cinco repeticiones y tomar el mayor valor de las pruebas realizadas³⁰^,³³⁾. También se ha utilizado la medida de la presión inspiratoria nasal realizándola a partir de la capacidad funcional residual⁴⁹^,⁵⁰⁾(Figura 1).

Entrenamiento

Entrenamiento muscular de las extremidades

Los ejercicios de intensidad baja a moderada han demostrado seguridad en pacientes con hipertensión pulmonar. Se ha identificado que el entrenamiento puede mejorar la capacidad de ejercicio y la calidad de vida relacionada con la salud. Para iniciar con los protocolos de entrenamiento, los pacientes deben estar recibiendo sus terapias farmacológicas y deben ser supervisados, minimizando las complicaciones⁴. Ejercicios de escalón con extremidades sin apoyo con y sin mancuernas; uso de circuitos que involucran grandes grupos musculares utilizando equipos específicos para el fortalecimiento, como press de piernas, extensión de piernas, movimientos laterales y abdominales⁵¹. También se ha reportado que el entrenamiento de fuerza en cuádriceps debe ser progresivo, y depende de lo obtenido en las evaluaciones iniciales, comenzando en la primera semana con tres series de 12 repeticiones al 50% del test de una repetición máxima y progresando al 75% en la semana 7, hasta llegar a la semana 12 con las mismas series y repeticiones. En cuanto a la resistencia, se aumenta el número de repeticiones a 30, también tres series, pero comenzando en la semana uno al 30% de la prueba máxima de una repetición y progresando al 40% en la semana 7, también hasta llegar a la semana 12⁴⁶.

Para las extremidades superiores, se han reportado entrenamientos con mancuernas con bajo peso (500-1000g), enfocados en los músculos de forma independiente⁵¹^,⁵²; durante 30 minutos, cinco veces por semana durante 12 semanas; esto podría deberse a la intención de realizar actividades seguras que eviten en lo posible la aparición de complicaciones relacionadas con alteraciones musculoesqueléticas y también con la interacción corazón-pulmón⁵³.

Uno de los resultados más reportados es la disminución relativa de fibras tipo IIx luego del entrenamiento muscular en rehabilitación pulmonar. Este resultado está fuertemente correlacionado con la disminución en la producción de CO₂⁴⁴; resultados que han sido identificados no sólo en pacientes con hipertensión arterial pulmonar sino también en pacientes con hipertensión pulmonar tromboembólica crónica que además mejoraron su capacidad aeróbica funcional y calidad de vida⁵².

Se ha reportado que después del entrenamiento, hay una mejora en la distribución de las fibras musculares²³⁾, Actividades como bicicleta ergométrica con entrenamiento continuo (30 min 50% carga de trabajo pico) e interválico (1 min rápido/30 lento; 10-25 min; 10-60 W; con intensidad 60-80% del VO2 pico); aumento progresivo durante el programa⁵⁴^,⁵⁵. El entrenamiento específico del cuádriceps ha provocado una mejora en el rendimiento y función muscular, esta mejora es consecuencia de cambios morfológicos a través del aumento de la capilarización y de la actividad enzimática oxidativa evaluada con biopsia del vasto lateral⁴⁶^,⁵⁶.

La estimulación eléctrica neuromuscular se ha utilizado como intervención en pacientes con trastornos pulmonares crónicos y es una alternativa para aquellos que no tienen la capacidad suficiente para participar en programas de ejercicio de intensidad moderada a alta⁵⁷⁾. Este método es pasivo y más tolerable para pacientes con síntomas severos resultantes de una baja carga metabólica en el sistema cardiorrespiratorio⁵⁸^,⁵⁹.

En hipertensión pulmonar, aunque hay poca evidencia que apoye su uso; Un estudio de 8 semanas usó estimulación eléctrica neuromuscular en cuádriceps y deltoides con frecuencia de 50 Hz en pulsos de 350 µs durante un ciclo de encendido: apagado, que se incrementó semanalmente de 2:15 s a 5:20 s a 10:15 s. La intensidad fue aumentando según la tolerancia del paciente. El protocolo estaba programado para 40 minutos al día tres días a la semana. La intervención mejoró la fuerza de los músculos periféricos, el área transversal y el grosor de los músculos, la rigidez arterial, la capacidad de ejercicio, la movilidad funcional, el equilibrio, la confianza en el equilibrio, el nivel de actividad física y la calidad de vida en pacientes con hipertensión arterial pulmonar⁵⁹.

En general, el entrenamiento muscular promueve el aumento del consumo máximo y pico de oxígeno; así como la reducción de los síntomas durante el ejercicio medido con la escala de Borg; asimismo, a nivel hemodinámico, los cambios en la frecuencia cardíaca y las presiones sistólica y diastólica demuestran beneficios que van desde lo funcional hasta lo estructural, con cambios moleculares y clínicos⁴³^,⁵⁵.

Integrando los resultados obtenidos, se ha encontrado que el entrenamiento de fuerza mejora la calidad de vida relacionada con la Salud cuando se evalúa con cuestionarios como CAMPHOR y SF36; los cambios ocurren generalmente en las funciones físicas, mentales, de percepción de la salud, del dolor corporal y de la vitalidad⁴³^,⁵⁵^,⁶⁰.

Cuando se entrena a pacientes con una enfermedad como la hipertensión pulmonar, que tiene un alto compromiso en el sistema cardiovascular y pulmonar, con alto riesgo de complicaciones, los efectos adversos son un riesgo. Ha habido reportes de pacientes con síncope que generalmente puede aparecer horas después del entrenamiento y episodios de taquicardia en pacientes con antecedentes de arritmia; sin embargo, estos eventos adversos no se transformaron en un empeoramiento clínico de la insuficiencia cardíaca que se resolvió rápidamente. El monitoreo continuo y contar con personal altamente capacitado es la mejor manera de mitigar estos riesgos.

Entrenamiento de los músculos respiratorios

Los pacientes que se ha informado se benefician del entrenamiento de los músculos respiratorios son aquellos con hipertensión pulmonar moderada ⁴⁸ e incluso severa⁶¹⁾; debido a la gravedad y compromiso cardiovascular de los pacientes, la prescripción debe realizarse de forma segura y eficaz.

De acuerdo con la evidencia revisada, el dispositivo threshold es el más utilizado para entrenar los músculos involucrados en la inspiración, utilizando cargas del 30% de la presión inspiratoria máxima durante 30 minutos, los 7 días de la semana durante seis semanas³⁰.El entrenamiento muscular inspiratorio umbral permite entrenar en un rango de 9 cm H₂O a 41 cm H₂O. las cargas generalmente comienzan en el 30% de la presión inspiratoria máxima; Los entrenamientos de 15 minutos se pueden repetir dos veces al día durante ocho semanas, cinco días a la semana⁴⁸.

También se han incluido actividades de entrenamiento que van acompañadas de terapia respiratoria cinco veces por semana. Otras actividades, que incluyen ejercicios para estirar los músculos relacionados con la respiración y los músculos del tronco, técnicas como fruncir los labios y la modulación consciente de los patrones de respiración⁴⁹, y técnicas de yoga (respiración Ujjayi), que han demostrado mejorar la sensibilidad barorrefleja en población sana⁶².

Se requiere monitoreo continuo de las variables hemodinámicas para realizar los procedimientos. El punto de corte se sugiere en ≤130/min de frecuencia cardiaca. En cuanto a la saturación de oxígeno periférico, se considera un valor de saturación ≤85% para decidir disminuir la intensidad; en los casos en que la saturación disminuya, los pacientes pueden recibir oxígeno suplementario durante la realización de los procedimientos, que puede ser entregado utilizando bajo o alto flujo⁶³.

Se ha reportado que la adición del entrenamiento de los músculos respiratorios, al tratamiento funcional de las extremidades superiores e inferiores, ofrece beneficios más significativos a la mejora en la función de los músculos involucrados, también los beneficios en el sistema cardiocirculatorio, calidad de vida y reducción de la disnea durante el ejercicio ⁶¹. Sin embargo, otro estudio demostró que realizando entrenamiento muscular con threshold cinco días a la semana durante 15 minutos, dos veces al día, solo conseguía mejorar la fuerza de los músculos respiratorios, pero ningún otro parámetro (calidad de vida y síntomas). Este resultado puede reforzar la idea de que el entrenamiento muscular debe realizarse tanto en los músculos respiratorios como en los de las extremidades; y que los beneficios se obtienen con entrenamiento localizado acompañado de entrenamiento global⁴⁸(Tabla 1).

Tabla 1. Estrategias y observaciones para el entrenamiento muscular en pacientes con hipertensión pulmonar.

Región	Estrategia	Observaciones
Músculos Respiratorios	Dispositivo Threshold	Permite entrenar en un rango de 9 cm H₂O a 41 cm H₂O. Las cargas generalmente comienzan al 30% de la presión inspiratoria máxima⁸^,³⁰
Miembros inferiores	Equipos específicos para el fortalecimiento	Press de piernas, extensión de piernas y movimientos laterales; comenzando en la primera semana con tres series de 12 repeticiones al 50% de la prueba máxima de una repetición y progresando al 75% en la semana 7 para fuerza⁴⁶^,⁵¹
Miembros inferiores	Equipos específicos para el fortalecimiento	Para resistencia, se aumenta el número de repeticiones a 30, también tres series, pero comenzando en la semana 1 al 30% de la prueba máxima de una repetición y progresando al 40% en la semana 7⁴⁶
Miembros superiores	Entrenamiento con mancuernas	Se ha reportado uso de peso bajo (500-1,000 g), enfocados en los músculos de forma independiente durante 30 minutos, cinco veces a la semana durante 12 semanas. Realización de incrementos según la respuesta del paciente⁴^,⁵¹^,⁵³

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Conclusión

Existen varias alternativas para la evaluación y el entrenamiento muscular en hipertensión pulmonar. Se ha demostrado que el entrenamiento muscular en pacientes con hipertensión pulmonar es seguro y eficaz; la selección del paciente adecuado, en función de la gravedad de la enfermedad, teniendo en cuenta los valores obtenidos en el cateterismo cardíaco derecho, imágenes, biomarcadores y clasificación funcional de los pacientes. Se necesita promover la inclusión temprana en programas de entrenamiento, que pueden estar en el marco de la rehabilitación pulmonar. Es fundamental elegir formas de evaluación e intervención.

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PERMALINK

Muscle training in patients with pulmonary hypertension. a narrative review

Entrenamiento muscular en pacientes con hipertensión pulmonar, una revision narrativa

Vicente Benavides-Cordoba

Martijn A Spruit

Abstract

Resumen

Remark

Introduction

Lower-limb muscle dysfunction

Respiratory muscle dysfunction

Evaluation

Lower and upper-limb muscle function

Respiratory muscle function

Training

Limb muscle training

Respiratory muscle training

Table 1. Strategies and observations for muscle training in patients with pulmonary hypertension.

Conclusion

References

Entrenamiento muscular en pacientes con hipertensión pulmonar, una revision narrativa

Contribución del estudio

Introducción

Disfunción muscular de miembros inferiores

Disfunción de los músculos respiratorios

Evaluación

Función de los músculos de las extremidades inferiores y superiores

Función de los músculos respiratorios

Entrenamiento

Entrenamiento muscular de las extremidades

Entrenamiento de los músculos respiratorios

Tabla 1. Estrategias y observaciones para el entrenamiento muscular en pacientes con hipertensión pulmonar.

Conclusión

ACTIONS

PERMALINK

RESOURCES

Cite

Add to Collections

PERMALINK

Muscle training in patients with pulmonary hypertension. a narrative review

Entrenamiento muscular en pacientes con hipertensión pulmonar, una revision narrativa

Vicente Benavides-Cordoba

Martijn A Spruit

Abstract

Resumen

Remark

Introduction

Lower-limb muscle dysfunction

Respiratory muscle dysfunction

Evaluation

Lower and upper-limb muscle function

Respiratory muscle function

Training

Limb muscle training

Respiratory muscle training

Table 1. Strategies and observations for muscle training in patients with pulmonary hypertension.

Conclusion

References

Entrenamiento muscular en pacientes con hipertensión pulmonar, una revision narrativa

Contribución del estudio

Introducción

Disfunción muscular de miembros inferiores

Disfunción de los músculos respiratorios

Evaluación

Función de los músculos de las extremidades inferiores y superiores

Función de los músculos respiratorios

Entrenamiento

Entrenamiento muscular de las extremidades

Entrenamiento de los músculos respiratorios

Tabla 1. Estrategias y observaciones para el entrenamiento muscular en pacientes con hipertensión pulmonar.

Conclusión

ACTIONS

PERMALINK

RESOURCES

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