Review of Respiratory Medicine - Volumen 24, Número 4 - December 24

Review Article

Respiratory Muscle Training in Patients With Mechanical Ventilation: A Narrative Review

Entrenamiento de músculos respiratorios en pacientes con ventilación mecánica: una revisión narrativa

ABSTRACT

Background: Prolonged weaning, characterized by a delayed separation from me­chanical ventilation, is associated with significant complications and high mortality rates. Diaphragmatic weakness emerges as a common cause of weaning failure, affecting a large percentage of patients. In response to this challenge, respiratory muscle training presents a promising strategy.

Objective: To present the available evidence on the implementation of respiratory muscle training in patients undergoing mechanical ventilation and its impact on various clinical variables.

Material and Methods: A literature search was conducted for articles published up to December 2023 using various MeSH (Medical Subject Headings) terms and keywords. After applying filters, 25 articles were selected. The search was completed manually by reviewing the reference lists of the selected articles.

Development: Approaches vary between strength training programs and resistance training methods. All of them impact mechanical ventilation weaning time, maximal inspiratory strength, and quality of life as assessed by questionnaires such as EQ-5D and SF-36.

Conclusions: Despite the variability of studies regarding training methods and the optimal load, respiratory muscle training in adult patients under mechanical ventilation can result in improved respiratory muscle strength, reduce the duration of mechanical ventilation in specific patients, and improve quality of life.

Key words: Artificial respirator, Respiratory muscles, Respiratory muscle training, Mechanical ventilation, Weaning, intensive care

RESUMEN

Introducción: El destete prolongado, caracterizado por una separación tardía de la ventilación mecánica, conlleva significativas complicaciones y una alta mortalidad. La debilidad diafragmática emerge como una causa común de fracaso en el destete, afectando a un gran porcentaje de pacientes. Frente a este desafío, el entrenamiento de los músculos respiratorios se presenta como una estrategia prometedora.

Objetivo: Exponer la evidencia disponible sobre la implementación del entrenamiento de los músculos respiratorios en los pacientes bajo ventilación mecánica y el impacto en diversas variables clínicas.

Materiales y Métodos: Se realizó una búsqueda bibliográfica de artículos publicados hasta diciembre de 2023 con diversos términos MeSH y palabras claves combinadas. Se seleccionaron 25 artículos posterior a la colocación de filtros. La búsqueda se completó manualmente con la revisión de referencias bibliográficas de los artículos seleccionados.

Desarrollo: Los enfoques varían entre programas de entrenamiento de fuerza y métodos de entrenamiento de resistencia. Todos estos impactan sobre el tiempo de destete de la ventilación mecánica, fuerza inspiratoria máxima y calidad de vida evaluada mediante cuestionarios como EQ5D y SF-36.

Conclusiones: A pesar de la variabilidad de los estudios en cuanto a los métodos de entrenamiento y cuál es la carga óptima, el entrenamiento de los músculos respiratorios en pacientes adultos bajo ventilación mecánica puede resultar en una mejoría de la fuerza de los músculos respiratorios, reducir la duración de la ventilación mecánica en pacientes específicos y mejorar la calidad de vida.

Palabras claves: Respirador artificial, Músculos respiratorios, Entrenamiento de músculos respiratorios, Ventilación mecánica, Destete, cuidados intensivos

Received:07/26/2024

Accepted:12/11/2024

INTRODUCTION

Weaning is the process of liberating a patient from mechanical ventilation (MV) and begins with the first attempt to separate them from it, whether through a spontaneous breathing trial (SBT) in any of its modalities or through extubation without SBT in patients under orotracheal intubation (OTI). For tracheostomized patients, it starts after completing at least 24 hours without requiring MV.^1,2

Weaning can be classified as simple (Group 1), where separation from MV occurs within 24 hours of initiating the process; difficult (Group 2), where liberation occurs between 24 hours and 7 days af­ter starting weaning; prolonged (Group 3) where separation is not completed within one week of starting the weaning, and the patient either suc­cessfully weans (3a) or never weans off MV (3b); no weaning (Group 0), which includes patients who never attempted liberation from MV.¹

Multicenter and international studies^1,2 report a prevalence of prolonged weaning of 8.7-9.6%, associated with a mortality rate of 29.8% in this subgroup of patients. An article published in an European journal found a prevalence of prolonged weaning of 15%.³ In Argentina, the prevalence of prolonged weaning was 14.9%, with a mortality rate of 36.1% in this group. Prolonged weaning is therefore associated with worse patient outcomes, including increased mortality, longer stays in the Intensive Care Unit (ICU), and extended hospital stays. Furthermore, alongside age, the duration of MV is the strongest predictor of functionality one year after hospital discharge.⁴

One of the reasons why patients fail to wean is diaphragmatic dysfunction or weakness.⁵ This condition is diagnosed when the maximal dia­phragmatic pressure (Pdi max), measured through esophageal and gastric manometry, is less than 60 cmH₂O.⁶ Approximately 63% to 80% of patients ex­hibit diaphragmatic weakness at the time of wean­ing, and 80% of patients undergoing prolonged weaning experience this dysfunction.⁷

Diaphragmatic weakness is not always associ­ated with Intensive Care Unit-Acquired Weakness (ICUAW), which is diagnosed by evaluating the strength of the upper and lower limbs. During weaning, diaphragmatic weakness is twice as common as weakness in limb muscles, making these two conditions completely different enti­ties.⁸

For this reason, inspiratory muscle training (IMT) has been proposed as a treatment strategy for patients with diaphragmatic weakness as­sociated with prolonged weaning. IMT focuses on strengthening the diaphragm and accessory inspiratory muscles to improve muscle strength and endurance.⁹

Respiratory muscles respond to the same train­ing principles as other skeletal muscles: overload, specificity, and reversibility. These principles are important in designing IMT protocols, which include threshold loading, resistive loading, and full-body mobilization.⁹

To achieve a training response, it is necessary to overload the muscle fibers with a stimulus of intensity and duration that exceeds the training threshold. Additionally, specific loading leads to specific training responses (principle of specific­ity), and the physiological adaptations achieved through training are reversible, meaning they are lost during periods of inactivity.¹⁰

A survey among French physiotherapists revealed that 83% considered controlled dia­phragmatic breathing (without resistance) as a form of inspiratory muscle training, while only 16% measured the strength of the inspiratory muscles.¹¹

The primary objective of this narrative review is to present the available evidence on the implemen­tation of IMT in mechanically ventilated patients, the devices used, the existing application methods, and the impact on weaning variables, respiratory muscle strength, and quality of life.

MATERIALS AND METHODS

A bibliographic search was conducted in the database of PubMed, Virtual Health Library (VHL), and Cochrane for articles published up to December 2023 using the fo­llowing MeSH terms and combined keywords: “Ventilator Weaning” OR “Respirator Weaning” OR “Mechanical Ventilator Weaning” AND “Respiratory Muscle Training” OR “Respiratory Muscle” OR “Ventilatory Muscles.” After applying filters (full text, age over 18 years, studies in humans), 22 articles were selected from 1,088 results. The selection included multicenter studies, observational stu­dies, randomized controlled trials, and systematic reviews. The search was manually supplemented by reviewing the references of the selected articles, resulting in a total of 27 studies. Figure 1.

There are several factors to consider when deter­mining if IMT is appropriate for a patient in the ICU. Since the training requires active participa­tion from the patients, their level of alertness and cooperation is essential. Patients must be sufficiently awake to understand the purpose of intermittent loading and perceive it as a temporary training stimulus. Therefore, minimizing sedation is a crucial component of the multidisciplinary ap­proach of IMT in the ICU.¹²

Training is feasible in patients with a trache­ostomy or endotracheal tube. Because it relies on threshold loads, IMT requires disconnection from mechanical ventilation. Consequently, pa­tients should not depend on high levels of positive end-expiratory pressure (PEEP), as disconnec­tion could lead to derecruitment and atelectasis. However, for clinically stable patients with PEEP levels < 10 cmH₂O and FiO₂ < 0.60, IMT does not result in changes to clinical parameters. Addition­ally, hemodynamic parameters must be stable at the time of training.¹² IMT can be beneficial in the process of weaning from mechanical ventilation for certain patients. It is particularly useful for those who, after 7 days of connection have not succeeded with standard methods such as progressive T-tube trials. Furthermore, it may be effective in patients with Pimax (maximal inspiratory pressure) values greater than -30 cmH₂O, as this criterion is consid­ered an indicator of successful weaning.¹³

There are several conditions in which IMT wouldn’t be appropriate, such as patients in the acute phase, experiencing severe pain, dyspnea, or those for whom palliative care has been proposed.¹² Table 1.

IMT devices

There is a wide range of techniques used for respiratory muscle training, including external resistive loading devices, external threshold pres­sure loading devices, adjustments to the trigger sensitivity of mechanical ventilators, and training with abdominal weights.^14-16

First, resistive loading devices involve placing a resistor in the patient’s airway, which increases airflow resistance during inspiration. This in­creased resistance requires the respiratory muscles to generate greater pressure to achieve the neces­sary airflow. Therefore, the pressure generated depends directly on the inspiratory flow that the patient can achieve.¹⁷

Secondly, threshold loading devices use a valve in the airway, set to a specific pressure level. To open this valve and allow airflow, the patient’s respira­tory muscles must generate the required pressure. Unlike resistive loading devices, the effect of train­ing with threshold loading devices is independent of the patient’s individual respiratory mechanics and respiratory drive, simplifying standardization.^9,11,17

Trigger sensitivity is determined by the pres­sure threshold in the circuit that the patient must reduce to open the inspiratory valve and achieve inspiratory gas flow.¹⁸

On the other hand, training with abdomi­nal weights increases intra-abdominal pressure, which stimulates diaphragm contraction, thereby strengthening the respiratory muscles.

Finally, there is no evidence to support the idea that deep breathing exercises without resistance result in significant improvements in respiratory muscle strength or enhance the weaning process in ICU patients.¹¹

Training methods

Inspiratory muscle training targets the diaphragm and accessory inspiratory muscles to improve muscle strength and endurance. Two treatment approaches can be distinguished: strength training program with moderate to high loads and low rep­etitions,¹⁹ or an endurance training method which uses low-intensity loads with many repetitions sustained over a set work period.²⁰ Although respi­ratory muscles are primarily endurance muscles, with the diaphragm composed of 80% fatigue-resistant fibers (55% type I and 25% type IIa),²¹ a recent systematic review that separately analyzed strength and endurance training regimens found that both approaches benefit respiratory muscle training compared to control groups.⁹

Based on the experience of some authors,¹¹ a strength training regimen is more feasible for ICU patients. This is partly because it involves less time of disconnection from mechanical ventilation, reducing alveolar derecruitment. Additionally, it requires less time of collaboration from the patient, who is often affected by fatigue, lack of attention, delirium, and other factors.¹¹

The duration of respiratory muscle training varies significantly across studies. Ibrahiem et al²² propose conducting training twice daily for three days. Conversely, in the study by Bissett et al,²³ training continued until patients were successfully weaned from mechanical ventilation.

The various training approaches are distin­guished in Table 2.

Impact on mechanical ventilation weaning

The findings from studies regarding the impact on the duration of weaning from mechanical ventilation are contradictory. Four studies^{15, 24-26} examining various forms of training (Threshold, trigger sensitivity, and Powerbreath) don’t show significant differences in weaning time. In con­trast, five other studies^{27, 28, 30–32} reported a reduc­tion in weaning time, with two of them^{31, 32} showing a significant decrease when the Threshold device was implemented. This aligns with the review conducted by Vorona et al⁹, which associated IMT with a significant reduction in weaning duration, even when studies with a high risk of bias were excluded (3.2 days; 95% CI 0.6-5.8).

Regarding the studies by Sandoval Moreno et al²⁴ and Caruso et al,¹⁵ the lack of significant dif­ferences in weaning times between groups can be explained by the short duration of IMT in these studies. This is because training began within 48 to 72 hours of initiating MV, respectively, and patients were extubated early, suggesting an ab­sence of respiratory muscle dysfunction associated with MV.²⁴ In a randomized clinical trial (RCT),¹⁵ IMT was performed by reducing the sensitivity of the ventilator’s trigger, which provided initial resistance to opening the ventilator valve. On the other hand, IMT with the Threshold device offers resistance throughout the entire inspiratory phase, as reported by Cader et al.²⁷

Four studies^9,14,16,26 examined the impact of IMT on the duration of mechanical ventilation, and only the study by Elbouhy et al¹⁴ reported a significant reduction in MV duration (11.67 days ±1.95 vs. 14.12 days ±1.73). In a study conducted in Eng­land, patients were divided into two intervention groups: one subjected to abdominal weights and the other combining abdominal weights with the use of a cough machine. This device applies positive inspiratory pressure, which instantly converts into high-flow negative expiratory pressure, increasing peak cough flow and effectively clearing respira­tory tract secretions.¹⁶ While a reduction in MV days was observed, statistical significance was not achieved. However, the study highlighted limita­tions, including a lack of scientific rigor due to dif­ferences in training loads and durations, as well as a small sample size. Although the review by Vorona et al⁹ initially associated IMT with a reduction in MV duration, by excluding studies with a high risk of bias, this difference was non-significant, consistent with the findings of Shimizu et al.²⁶

Regarding weaning success, two RCTs imple­menting the Threshold device^19,31 and one ad­justing trigger sensitivity for training¹⁴ reported significant differences in the experimental group. Similarly, the study by Bissett et al³³ reported a lower rate of orotracheal reintubation in this group (45% vs. 76%; OR 0.603).

In one study³⁴ including patients with cervical spinal cord injuries who underwent a rehabilita­tion program including IMT, 70% of the patients were successfully weaned and decannulated, ex­cept for three patients with spinal cord injuries category A according to the ASIA (American Spinal Injury Association) at the C1 level. Two other stud­ies reported no significant differences in weaning success: Sandoval Moreno et al²⁴ found no differ­ences in weaning failure. Hung TY et al¹⁶ observed no differences in reintubation rates.

Effects on respiratory muscle strength

The effects of IMT on respiratory muscle strength were investigated in eighteen studies.^{9,15-19,22,24-32,35-37} Four studies^17,22,30,35 demonstrated that this train­ing correlated with a significant increase in maxi­mal inspiratory pressure (Pimax) from the begin­ning in patients undergoing training compared to the control group. Three studies^24,26,29 reported differences in muscle strength that did not reach statistical significance.

Several studies^{19,22,24,27,28,35-37} showed a sig­nificant improvement in the final Pimax com­pared to baseline exclusively in patients who received daily IMT with a threshold load. In contrast, four studies^25,26,29,31 observed a signifi­cant increase in Pimax in both the experimental and control groups.

Dixit et al³² evaluated 30 patients with pro­longed MV and divided them into two groups. Group A underwent conventional physiotherapy. Group B received conventional physiotherapy combined with IMT using a Threshold device. As a result, a Pimax increase was observed in both study groups, but it was significantly greater in Group B compared to Group A (-43.87 ± 8.01 vs. -35.68 ± 4.48; p = 0.0009).

In a 2022 study16, thirty patients with similar clinical and demographic characteristics were randomly assigned to two groups. One group un­derwent IMT with abdominal weights. The other combined abdominal weights with the use of a cough machine. Results revealed a significant im­provement in both Pimax and maximal expiratory pressure (Pemax) in both groups.

In a systematic review,⁹ the Pimax increased by 40% in patients exposed to IMT, compared to an 18% increase in the control group. Differences were also observed in the Pemax, which increased by 63% in the IMT group versus 17% in the control group. The Pimax tended to increase with strength training compared to endurance training and when using the Threshold device. But the difference between subgroups was small and did not reach statistical significance. Figure 2.

Impact on pulmonary function

Respiratory muscle training can generate changes in the strength (as reflected in the Pimax and Pemax), and it can also lead to changes in pul­monary function. Several studies have described variations in parameters such as the rapid shallow breathing index, tidal volume, respiratory rate, and inspiratory flow, among others.

Some studies^16,30,31,36 demonstrated improve­ments in the rapid shallow breathing index after patients participated in a respiratory muscle train­ing program. Conversely, Tonella et al²⁸ reported no significant changes in this index. In a RCT²⁷ where the IMT was performed with a threshold-loading device versus standard care, an increase was observed in the mentioned index in both study groups. However, this increase was smaller in the intervention group (mean difference -8.3; 95% CI -13.7 to -2.9). Despite the observed increase, both groups remained below the cutoff value pro­posed as predictor of successful weaning, which is less than 105 breaths/min/L and corresponds to breaths per minute divided by the tidal volume (TV) in liters.³⁸

Changes in TV were considered in some studies. In the study by Condessa et al³⁰, the TV increased in the intervention group undergoing IMT, while a decline was observed in the control group (mean difference 72; 95% CI 17 to 128). This improvement in TV could explain the improvement in the rapid shallow breathing index in the intervention group. Similar results were found in three articles^16,29,36 which reported increased volumes following respiratory muscle training.

Hung TY et al¹⁶ observed a significant improve­ment in vital capacity, Pimax, Pemax, and peak cough flow with respect to baseline values in the experimental group, compared to the control group. In the study of Lee CY et al,³⁶ an improve­ment was observed in respiratory rate, minute volume, and breathing pattern after IMT. Holle­beke et al²⁹ documented increases in inspiratory flow and in the oxygenation of respiratory muscles following an IMT program, along with a significant reduction in the work of breathing (WOB) in this group.

Pascotiniet al³⁹ found that patients treated with conventional physiotherapy experienced an increase in respiratory rate. In contrast, patients who received IMT with the Threshold device in addition to conventional therapy showed a reduc­tion in respiratory rate.

Impact on survival rate and quality of life

A 2017 study⁴⁰ reported that patients undergoing IMT had a higher survival rate 30 days post-intervention compared to the control group, of 79% and 44%, respectively, and those values turned out to be statistically significant.

Bissetet al³⁵ assessed quality of life using the EQ-5D and SF-36 scales. Both measures showed statistically significant improvements from base­line in the IMT group only. The difference regard­ing the EQ-5D scores between groups was greater in the IMT group (mean difference 12; 95% CI 1–23; p = 0.034). No significant differences were observed in SF-36 scores between groups, although point estimates suggested potential benefits. While the results did not reach statistical significance, data suggest a trend towards improved quality of life in relation to health, defined as the well-being level derived from an assessment made by an individual of various life domains, considering the impact of their health status,⁴³ which could indicate a potential benefit of the treatment. On the other hand, a significant increase in mortality was reported in the IMT group, though none of the deaths were linked to respiratory complications from IMT. So, this increased mortality may be at­tributed to patient comorbidities and the severity of their condition upon hospital admission.

CONCLUSION

Despite the variability of studies regarding train­ing methods and the optimal load, respiratory muscle training in adult patients under MV can result in improved respiratory muscle strength, reduce the duration of mechanical ventilation in specific patients, and improve quality of life. Given the fact that the weakness of these muscles has a clear impact in the outcomes both in and out of the ICU, incorporating personalized, targeted respira­tory muscle training into conventional respiratory therapy could help maximize patient recovery.

Conflict of interest

Authors have no conflicts of interest to declare.

REFERENCES

1. Béduneau G, Pham T, Schortgen F, et al. Epidemiology of Weaning Outcome according to a New Definition. The WIND Study. Am J Respir Crit Care Med. 2017;195:772-83. https://doi.org/10.1164/rccm.201602-0320OC

2. Pham T, Heunks L, Bellani G, et al. Weaning from mechani­cal ventilation in intensive care units across 50 countries (WEAN SAFE): a multicentre, prospective, observational cohort study. Lancet Respir Med. 2023;11:465-76. https:// doi.org/10.1016/S2213-2600(22)00449-0

3. Boles JM, Bion J, Connors A, et al. from mechani­cal ventilation. Eur Respir J. 2007;29:1033-56. https://doi. org/10.1183/09031936.00010206

4. Plotnikow GA, Gogniat E, Accoce M, Navarro E, Dorado JH. Epidemiology of mechanical ventilation in Argentina. The EpVAr multicenter observational study. Med Inten­siva (Engl Ed). 2022;46:372-82. https://doi.org/10.1016/j. medin.2021.10.003

5. Heunks LM, van der Hoeven JG. Clinical review: the ABC of weaning failure-a structured approach. Crit Care. 2010;14:245. https://doi.org/10.1186/cc9296

6. American Thoracic Society/European Respiratory Soci­ety. ATS/ERS Statement on respiratory muscle testing. Am J Respir Crit Care Med. 2002;166:518-24. https://doi. org/10.1164/rccm.166.4.518

7. Dres M, Goligher EC, Heunks LMA, Brochard LJ. Critical illness-associated diaphragm weakness. Intensive Care Med. 2017;43:1441-52. https://doi.org/10.1007/s00134-017-4928-4

8. Dres M, Dubé BP, Mayaux J, et al. Coexistence and Impact of Limb Muscle and Diaphragm Weakness at Time of Libera­tion from Mechanical Ventilation in Medical Intensive Care Unit Patients. Am J Respir Crit Care Med. 2017;195:57-66. https://doi.org/10.1164/rccm.201602-0367OC

9. Vorona S, Sabatini U, Al-Maqbali S, et al. Inspiratory Muscle Rehabilitation in Critically Ill Adults. A Systematic Review and Meta-Analysis. Ann Am Thorac Soc. 2018;15:735-44. https://doi.org/10.1513/AnnalsATS.201712-961OC

10. McConnell AK, Romer LM, Weiner P. Inspiratory muscle training in obstructive lung disease. Breathe. 2005;2:38-49. https://doi.org/10.1183/18106838.0201.38

11. Bissett BM, Wang J, Neeman T, Leditschke IA, Boots R, Paratz J. Which ICU patients benefit most from inspiratory muscle training? Retrospective analysis of a randomized trial. Physiother Theory Pract. 2020;36:1316-21. https:// doi.org/10.1080/09593985.2019.1571144

12. Bissett B, Leditschke IA, Green M, Marzano V, Collins S, Van Haren F. Inspiratory muscle training for intensive care patients: A multidisciplinary practical guide for clinicians. Aust Crit Care. 2019;32:249-55. https://doi.org/10.1016/j. aucc.2018.06.001

13. Tobin MJ, Jubran A. Weaning from mechanical ventila­tion. En: Tobin MJ. Principles and Practice of Mechanical Ventilation. 3 ed. Chicago: American Journal of Respiratory and Critical Care Medicine; 2013. p. 1307-1351.

14. Elbouhy MS, AbdelHalim HA, Hashem AMA. Effect of respiratory muscles training in weaning of mechanically ventilated COPD patients. Egypt J Chest Dis Tuberc. 2014;63:679–87. https://doi.org/10.1016/j.ejcdt.2014.03.008

15. Caruso P, Denari SD, Ruiz SA, et al. Inspiratory muscle training is ineffective in mechanically ventilated critically ill patients. Clinics. 2005;60:479-84. https://doi.org/10.1590/ S1807-59322005000600009

16. Hung TY, Wu WL, Kuo HC, et al. Effect of abdominal weight training with and without cough machine assistance on lung function in the patients with prolonged mechanical ventilation: a randomized trial. Crit Care. 2022;26:153. https://doi.org/10.1186/s13054-022-04012-1

17. Volpe MS, Aleixo AA, Almeida PRMN. Influence of inspira­tory muscle training on weaning patients from mechanical ventilation: a systematic review. Fisioter Mov. 2016;29:173- 81. https://doi.org/10.1590/0103-5150.029.001.AR02

18. Setten M, Tiribelli N, Rodrigues La Moglie R. Modos ven­tilatorios. En: Chiappero G, Ríos F, Setten M. Ventilación Mecánica. 3 ed. Buenos Aires: Editorial Médica Panameri­cana; 2018. p. 99-118.

19. Martin D, Smith B, Davenport P, et al. Inspiratory muscle strength training improves weaning outcome in failure to wean patients: a randomized trial. Crit Care. 2011;15:R84. https://doi.org/10.1186/cc10081

20. Dall’Ago P, Chiappa GR, Guths H, Stein R, Ribeiro JP. Inspiratory muscle training in patients with heart failure and inspiratory muscle weakness: a randomized trial. J Am Coll Cardiol. 2006;47:757-63. https://doi.org/10.1016/j. jacc.2005.09.052

21. DeVito EL. Músculos respiratorios. En: Mazzei JA, Mazzei M, Barro A, Di Bartolo CG. Manual de Pruebas de Función Pulmonar. De la Fisiología a la Práctica. Buenos Aires: Fundación Argentina del Tórax; 2009. p. 149-156.

22. Ibrahiem AA, Mohamed AR, Saber HM. Effect of respira­tory muscles training in addition to standard chest phys­iotherapy on mechanically ventilated patients. J Med Res Prac. 2014;03:52-8.

23. Bissett B, Leditschke IA, Paratz JD, Boots RJ. Respiratory dysfunction in ventilated patients: can inspiratory muscle training help?. Anaesth Intensive Care. 2012;40:236-46. https://doi.org/10.1177/0310057X1204000205

24. Sandoval Moreno LM, Casas Quiroga IC, Wilches Luna EC, García AF. Efficacy of respiratory muscle training in wean­ing of mechanical ventilation in patients with mechanical ventilation for 48hours or more: A Randomized Controlled Clinical Trial. Med Intensiva. 2019;43:79-89. https://doi. org/10.1016/j.medin.2017.11.010

25. Roceto Ratti LDS, Marques Tonella R, Castilho de Figueir do L, Bredda Saad IA, Eiras Falcão AL, Martins de Oliveira PP. Inspiratory Muscle Training Strategies in Tracheosto­mized Critically Ill Individuals. Respir Care. 2022;67:939- 48. https://doi.org/10.4187/respcare.08733

26. Shimizu JM, Manzano RM, Quitério RJ, et al. Determinant factors for mortality of patients receiving mechanical ventilation and effects of a protocol muscle training in weaning. MtpRehab J. 2014;1-7. https://doi.org/10.17784/ mtprehabjournal.2014.12.180

27. Cader SA, Vale RG, Castro JC, et al. Inspiratory muscle training improves maximal inspiratory pressure and may assist weaning in older intubated patients: a randomised trial. J Physiother. 2010;56:171-7. https://doi.org/10.1016/ S1836-9553(10)70022-9

28. Tonella RM, Ratti LDSR, Delazari LEB, et al. Inspira­tory Muscle Training in the Intensive Care Unit: A New Perspective. J Clin Med Res. 2017;9:929-34. https://doi. org/10.14740/jocmr3169w

29. Hollebeke MV, Louvaris Z, Clerckx B, et al. Evolution of inspiratory muscle training in patients with weaning dif­ficulties. Eur Respir J. 2019;54(63):PA2202. https://doi. org/10.1183/13993003.congress-2019.PA2202

30. Condessa RL, Brauner JS, Saul AL, Baptista M, Silva AC, Vieira SR. Inspiratory muscle training did not accelerate weaning from mechanical ventilation but did improve tidal volume and maximal respiratory pressures: a randomised trial. J Physiother. 2013;59:101-7. https://doi.org/10.1016/ S1836-9553(13)70162-0

31. Khodabandeloo F, Abdi A, Heidari Gorji MA, Mohammadi A, Amri Maleh P, Karimi H. The effect of threshold inspiratory muscle training on the duration of weaning in intensive care unit-admitted patients: A randomized clinical trial. J Res Med Sci. 2023;28:44. https://doi.org/10.4103/jrms. jrms_757_22

32. Dixit A, Prakash S. Effects of threshold inspiratory muscle training versus conventional physiotherapy on the weaning period of mechanically ventilated patients: a comparative study. Int J Physiother Res. 2014;2:424-8.

33. Bissett BM, Leditschke IA, Neeman T, et al. Does mechani­cal threshold inspiratory muscle training promote recovery and improve outcomes in patients who are ventilator-dependent in the intensive care unit? The IMPROVE randomised trial. Aust Crit Care. 2023;36:613-21. https:// doi.org/10.1016/j.aucc.2022.07.002

34. Gundogdu I, Ozturk EA, Umay E, Karaahmet OZ, Unlu E, Cakci A. Implementation of a respiratory rehabilitation protocol: weaning from the ventilator and tracheostomy in difficult-to-wean patients with spinal cord injury. Disabil Rehabil. 2017;39:1162-70. https://doi.org/10.1080/096382 88.2016.1189607

35. Bissett BM, Leditschke IA, Neeman T, Boots R, Paratz J. In­spiratory muscle training to enhance recovery from mechan­ical ventilation: a randomised trial. Thorax. 2016;71:812-9. https://doi.org/10.1136/thoraxjnl-2016-208279

36. Lee CY, Tsa YC, Bien MY. The effect of inspiratory muscle exercise in patients with prolonged mechanical ventila­tion. Am J Respir Crit Care Med. 2012;185. https://doi. org/10.1164/ajrccm-conference.2012.185.1_MeetingAb­stracts.A3090

37. Saad IAB, Melo FX, Silva V, Oliveira LVF, Lima JRO. A new device for inspiratory muscle training in patients with tracheostomy tube in ICU: a randomized trial. Respir Care. 2014;59:1501-8.

38. Yang KL, Tobin MJ. A prospective study of indexes pre­dicting the outcome of trials of weaning from mechanical ventilation. N Engl J Med. 1991;324:1445-50. https://doi. org/10.1056/NEJM199105233242101

39. Pascotini FDS, Denardi C, Nunes GO, Trvisan ME, Antunes VDP. Treinamento muscular respiratório em pacientes em desmame da ventilação mecânica. ABCS Ciencias de la Salud. 2014;39:12-6. https://doi.org/10.7322/abcshs.v39i1.253

40. Guimarães BL, De souza L, Guimarães F, et al. Use of a new isokinetic device oriented by software for inspiratory muscle training in prolonged weaning. Critical Care. 2017;21:40.

41. Hoffman M, Van Hollebeke M, Clerckx B, et al. Can inspira­tory muscle training improve weaning outcomes in difficult to wean patients? A protocol for a randomised controlled trial (IMweanT study). BMJ Open. 2018;8:e021091. https:// doi.org/10.1136/bmjopen-2017-021091

42. Smith BK, Gabrielli A, Davenport PW, Martin AD. Effect of training on inspiratory load compensation in weaned and unweaned mechanically ventilated ICU patients. Respir Care. 2014;59:22-31. https://doi.org/10.4187/resp­care.02053

43. Urzúa MA. Health related quality of life: Conceptual ele­ments. RevMed Chil. 20