Rev Bras Fisiol Exerc 2022;21(3):204-16

doi: 10.33233/rbfex.v21i3.5282

REVIEW

Diaphragmatic ultrasonography as a predictor of ventilatory weaning: a systematic review

Ultrassonografia diafragmática como preditora de desmame ventilatório: uma revisão sistemática

 

André Luiz Lisboa Cordeiro1,2, Lucas Oliveira Soares2, Késsia Morgana Vital Oliveira2, Amanda Maria Garcez de Oliveira de Jesus2

 

1Escola Bahiana de Medicina e Saúde Pública, Salvador, BA, Brazil

2Centro Universitário Nobre, Feira de Santana, BA, Brazil

 

Received: September 12, 2022; Accepted: September 13, 2022.

Correspondence: André Luiz Lisboa Cordeiro, Faculdade Nobre, Avenida Maria Quitéria, Kalilândia, Feira de Santana, BA

 

André Luiz Lisboa Cordeiro: andrelisboacordeiro@gmail.com

Lucas Oliveira Soares: lucassoaresft@gmail.com

Késsia Morgana Vital Oliveira: kessiamorganav@gmail.com

Amanda Maria Garcez de Oliveira de Jesus: amanda_garcez21@outlook.com

 

Abstract

Objective: To review the evidence on diaphragmatic ultrasonography as a predictor of success in ventilatory weaning, using the PICO methodology and keywords: Ultrasound, Diagnostic imaging, Diaphragm, Weaning, Intensive Care Unit, Artificial Respiration, Mechanical Ventilation, Ventilator Weaning. Methods: Published cohort studies were used without language and year restrictions that addressed the use of ultrasound to predict success in weaning and ventilatory extubation. Studies with patients under 18 years of age, case reports, literature reviews, results that do not bring a cutoff value for thickness and diaphragmatic excursion and the definition of failure in the weaning and extubation process were excluded. Results: 459 were found, and after exclusion due to duplication and reading of titles and abstract, only 11 were selected by the inclusion criteria. The samples ranged from 34 to 193 individuals. Conclusion: We can evidence that the use of USG to assess the thickness and excursion of the diaphragm in patients undergoing invasive ventilatory support is effective in predicting success in the weaning and extubation process. The Diaphragmatic Ultrasonography has great applicability to assess the ability to predict success or failure in removing invasive ventilatory support.

Keywords: diaphragmatic ultrasound; mechanical ventilation; weaning; airway extubation.

 

Resumo

Objetivo: Revisar as evidências sobre a ultrassonografia diafragmática como preditor de sucesso no desmame ventilatório, usando a metodologia PICO e palavras-chave: Ultrassom, Diagnóstico por imagem, Diafragma, Desmame, Unidade de Terapia Intensiva, Respiração Artificial, Ventilação Mecânica, Desmame do Ventilador. Métodos: Estudos de coorte publicados foram usados sem restrições de idioma e ano que abordaram o uso de ultrassom para prever o sucesso no desmame e extubação ventilatória. Foram excluídos estudos com pacientes menores de 18 anos, relatos de casos, revisões de literatura, resultados que não trouxessem valor de corte para espessura e excursão diafragmática e definição de falha no processo de desmame e extubação. Resultados: Foram encontrados 459 estudos; após exclusão por duplicação e leitura de títulos e resumo, apenas 11 foram selecionados pelos critérios de inclusão. As amostras variaram de 34 a 193 indivíduos. Conclusão: Podemos evidenciar que o uso da USG para avaliar a espessura e excursão do diafragma em pacientes submetidos a suporte ventilatório invasivo é eficaz em predizer o sucesso no processo de desmame e extubação. A ultrassonografia diafragmática tem grande aplicabilidade para avaliar a capacidade de predizer sucesso ou falha na remoção do suporte ventilatório invasivo.

Palavras-chave: ultrassom diafragmático; ventilação mecânica; desmame, extubação.

 

Introduction

 

One of the main causes of referral to the intensive care unit (ICU) is the need for invasive mechanical ventilation (IMV) [1,2]. Patients need IMV when they lose the ability to perform spontaneous ventilation due to respiratory failure or are unable to protect the airways by lowering the level of consciousness [3,4].

IMV can cause deleterious effects for the patient and diaphragmatic dysfunction (DD) is among the most important, causing weakness and atrophy due to disuse, prolonging the time spent on mechanical ventilation, risk of tracheostomy, complications up to one year after discharge from the ICU and impact on the mortality rate [3,4,5,6,7].

Weaning is a transitory process between the support of mechanical ventilation and spontaneous ventilation; it is also classified in categories according to the time of MV. Within intensive care units, and especially in patients on invasive ventilatory support, weaning becomes one of the main objectives of the multidisciplinary team. There are several causes for failure in the weaning process, in this scenario it is important to use accurate methods to predict success and avoid complications for the patient [8].

Several diagnostic techniques are used to assess diaphragmatic functions [9,10]. Among them, diaphragmatic ultrasonography (USG) has become increasingly used, proving to be very important in the intensive care environment and in the assessment of the critical patient. This method is accessible and can evaluate in real time the function and structure of the diaphragm, being able to detect changes that may difficult the weaning [1,3,4,11,12].

Parameters such as excursion and thickness are some of the findings that guide us to identify atrophy, paralysis and other diaphragmatic dysfunctions [1]. In this sense, Carrie et al. [13] assessed the performance of diaphragmatic USG to predict failure in weaning in patients under IMV using the maximum diaphragmatic excursion measurement, confirmed the ventilator-induced diaphragmatic dysfunction (VIDD) and suggests that the diaphragm is very sensitive to the absence of activity.

Llamas-Álvarez et al. [14] performed a review and suggest that diaphragmatic USG is a predictor in ventilatory weaning in critically ill patients. Therefore, the objective of this study was to review the evidence on diaphragmatic ultrasonography as a predictor of success in ventilatory weaning.

 

Methods

 

This is a systematic review and the guiding question of this study was: "What is the current evidence on diaphragmatic ultrasonography to predict success in weaning?"

The following databases were systematically searched: Pubmed, Scielo (Scientific Electronic Library Online), Lilacs (Latin American and Caribbean Literature in Health Sciences), VHL (Virtual Health Library) and Science Direct. The keywords used were: Ultrasound, Diagnostic imaging, Diaphragm, Weaning, Intensive Care Unit, Artificial Respiration, Mechanical Ventilation, Ventilator Weaning; synonyms and related words added by the Boolean operators "AND" and "OR", according to the Health Sciences Descriptors (DeCS). The survey was conducted in April 2020.

 

Eligibility criteria

 

We selected cohort studies without language and year restrictions which used the ultrasound to predict success in weaning and ventilatory extubation. Studies with patients under 18 years of age, case reports, literature reviews, results that do not bring a cutoff value for thickness and diaphragmatic excursion and the definition of failure in the weaning and extubation process were excluded and due to difficulty in translation we also excluded articles in Chinese.

 

Data extraction

 

The articles collected through the searches in the databases were selected by tracking the titles (first stage), abstracts (second stage) and complete reading (third stage). Then, an exploratory reading of the selected studies was carried out and, later, selective and analytical reading. The data extracted from the articles were systematized: authors, title, journal, year, summary and conclusions, in order to enable the obtaining of relevant information for the research.

The selection process, data extraction from articles and identification of methodological aspects was carried out by two independent reviewers. When there was any disagreement between them, the reviewers read the entire article again for reassessment. If the disagreement persists, a third independent reviewer assessed and made the final decision. The research followed the items of the PRISMA [15] protocol for systematic reviews.

 

Results

 

Four hundred and fifty-nine articles were found, and after exclusion due to duplication and reading of titles and abstracts, only eleven were selected according to the inclusion criteria. Those studies that did not make clear the values found with ultrasound to predict success in weaning / extubation (59) or articles with a literature review design or case reports (54) were also excluded from the study. The flowchart in Figure 1 shows all the criteria and databases used to select the articles.

 


 

Figure 1 - Flowchart demonstrating how the studies of cohorts that used ultrasound to assess diaphragmatic thickness and excursion were obtained

 

Table I shows the general characteristics of the other studies. We can observe that some studies were carried out in more than one unit, among which are wards, general ICU and specialized ICU.

 

Table I - General characteristics of the studies

 

It is possible to verify that the authors used very similar criteria to determine the failure in the weaning / extubation process, showing that they all started from the same point to define the failure of the removal of artificial ventilation, such as reconnection in the mechanical ventilator, reintubation, use of NIV and tracheostomy within 48 hours after extubation. Table II shows the definitions of each author for failure in weaning / extubation.

 

Table II - Characteristics of the included studies and definition of failure in weaning / extubation

 

The data presented below in Table III show the objectives and results found in each study using ultrasound to assess thickness and diaphragmatic excursion as a predictor of success in the weaning / extubation process. The authors identified that patients with thickness values < 1 cm, 20 < 2.20 + 0.69 mm [21] and < 10 mm [24] were associated with complications, prolonged MV and failure in weaning and extubation. Yoo et al. [26] found values of diaphragmatic thickness < 4 cm and 1.53 cm respectively are related to failure in weaning and extubation. These low values were also related to prolonged weaning, increased length of stay in the ICU, hospital mortality and after discharge from the unit.

 

Table III - General data from cohort studies using diaphragmatic USG as a predictor of success in weaning and extubation

 

Discussion

 

Based on the findings of this review, we can evidence that the use of diaphragmatic ultrasound to assess the thickness and excursion of the diaphragm in patients undergoing invasive ventilatory support is effective in predicting success in the weaning and extubation process.

It is essential to evaluate and identify patients able to remove invasive ventilatory support. Some studies indicate that failure in this process increases the chance of mortality by 50%. Diaphragmatic USG is able to identify the result of this process through anatomical and biomechanical measurements such as thickness and its excursion during normal operation, with the result of this assessment it is possible to develop therapeutic strategies to minimize these risks.

After evaluating Tdi, Sklar et al. [16] found that patients with values < 2.3 mm were associated with prolonged weaning, longer on invasive ventilatory support and had a significantly greater difference in hospital mortality, especially after discharge from the ICU. It was identified with the USG that the Tdi obtained on the beginning of MV was independently associated with prolonged MV and higher mortality regardless of the severity of the underlying disease [16].

Corroborating with Sklar [16], Dres et al. [21] found that patients with higher DTF and ED values proved to be efficient as a predictor independently associated with failure in weaning and extubation. They found that in an unelected population of mechanically ventilated patients considered ready to perform an ERT, the prevalence of DD was twice as high as the prevalence of ICU-AW, and that DD, not ICU-AW, influenced the outcome, being present in almost all patients who had failed weaning. This study served to highlight that DD should be the object of prevention and possible specific interventions [21].

Khan et al. [22] defined an IRRS cutoff point of 59 is 79% sensitive and 64% specific and 1.35 cm from DE, observed with ultrasound, a sensitivity of 74% and specificity of 75% to predict success in weaning, the greater the DE value the higher the success rate. In this study, they observed that IRRS better predicts the outcome of weaning, but that when associating the ND to the IRRS they are optimized in the classification of the outcome of weaning in guaranteeing extubation and prevention of reintubation [22].

In the intensive care setting, it becomes necessary to identify patients who are able to leave invasive ventilatory support and USG for diagnosing the patient's condition in real time, being low-cost, non-invasive and not emitting radiation is a useful tool and essential to evaluate these patients, its applicability is increasingly evident.

When using USG to assess DTF and DE in patients with abdominal sepsis Eltrabili et al. [17] found some results similar to Khan et al. [22], and they noticed a significant difference in patients who failed and those who were successful. The diaphragmatic parameters obtained with the USG, a DTF of 30.7%, with sensitivity of 94.1% and specificity of 100% and DE of 10.4 mm, with a sensitivity of 94% and specificity of 84% were values to predict successful withdrawal of mechanical ventilation. They observed that the best cutoff value to predict the success of weaning was 30.7%, because in other studies it varies from 20 to 36%, depending on the ventilatory support offered during the measurement [17].

ED has become a very relevant variable for the assessment of extubation. With that in mind, Zhang et al. [19] assessed DE with USG and found that patients who had extubation success had a higher value compared to those who failed, this value was significantly statistical. In the study, a cutoff value of DE of 1.72 cm was associated with success in extubation and observed that the combination of DE 30 and ΔDE 30-5 was more accurate in predicting extubation. Even if patients are successful in the ERT, they are still at risk of failing extubation, further proving the importance of looking for another indicator to predict the outcome of extubation and improve the survival of patients admitted to the ICU [19].

Many authors report the importance of an accurate evaluation of the diaphragm, especially of DE, which often appears as the main variable to be analyzed. Palkar et al. [20] were emphatic and said that DE is an imperfect predictor. Although the successful extubation group was significantly larger than the ones that failed, many complexity factors can interfere with the extubation result. They also observed that when measured between A / C and TRE they obtained a better result than only during the TRE.

Soliman et al. [23] found in patients with successful weaning a DTF significantly higher than in the group that failed, with a cutoff value ≥ 29.5, which can predict the success of weaning with a sensitivity of 88.0% and specificity of 80.0 %. The authors conclude the study by saying that they support the use of USG to predict weaning failure, to assess the lung and diaphragm, helping to understand the pathophysiological effects of weaning and to optimize the clinical condition, increasing the chances of successful weaning [23].

Using USG to assess the diaphragm of the elderly and the relationship between diaphragmatic dystrophy and weaning, Huang et al. [24] defined a cutoff value below 10 mm and used the M mode. They observed a 75% prevalence of DD in ventilated elderly people mechanically and 70% of weaning failure, having complex factors as reasons behind these weaning failures [24].

With similar results, Pirompanich and Romsaiyt [25] found a higher DTF in the successful group compared to the group that failed. The authors suggest that the right DTF greater than or equal to 26% is more accurate to predict success in weaning, being the best and most efficient predictor of success in ventilatory weaning. The reason the right side is more effective than the left can be a higher lung volume [25].

According to Yoo et al. [26] DE values are higher than Tdi in predicting extubation success, suggesting that DE may be more accurate than Tdi to predict weaning success. It is noteworthy that the values of the analyzed variables differ between studies, our findings demonstrate that regardless of the cutoff value established by the authors, the most relevant to be analyzed is the amount of loss of DTF, Tdi and DE from the beginning of mechanical ventilation.

 

Conclusion

 

Based on the data found, we can conclude that diaphragmatic ultrasonography has great applicability to assess the ability to predict success or failure in removing invasive ventilatory support. Values of thickened fraction, excursion and diaphragmatic thickness differ between studies according to the authors and the population studied, but the main point of this review is to show that the loss of diaphragmatic function revealed by a decrease in the thickening, excursion and thickness fraction diaphragm in mechanically ventilated patients can predict success or failure in the weaning and extubation process.

 

Potential conflict of interest

No conflicts of interests have been reported for this article.

 

Funding source

The present study was carried out without funding.

 

Authors’ contributions

Literature search, Data collection, Study design, Manuscript preparation and Review of manuscript: Cordeiro ALL, Soares LO, Oliveira KMV, Jesus AMGO

 

References

 

  1. Varón-Vega F, Hernández A, López M, Cáceres E, Giraldo-Cadavid LF, Uribe-Hernandez AM, Crevoisier S. Usefulness of diaphragmatic ultrasound in predicting extubation success. Med Intensiva (Engl Ed) 2021;45(4):226-33. doi: 10.1016/j.medin.2019.10.007 [Crossref]
  2. Girard TD, Alhazzani W, Kress JP, Ouellette DR, Schmidt GA, Truwit JD, et al. An Official American Thoracic Society/American College of Chest Physicians Clinical Practice Guideline: Liberation from mechanical ventilation in critically ill adult rehabilitation protocols, ventilator liberation protocols, and cuff leak tests. Am J Respir Crit Care Med 2017;195:120-33. doi: 10.1164/rccm.201610-2075ST [Crossref]
  3. Grasse A, Ferlicca D, Lupieri E, Calcinati S, Francesconi S, Sala V, et al. Assisted mechanical ventilation promotes recovery of diaphragmatic thickness in critically ill patients: a prospective observational study. Critical Care 2020;24:85. doi: 10.1186/s13054-020-2761-6 [Crossref]
  4. Goligher EC, Dres M, Fan E, Rubenfeld GD, Scales DC, Herridge MS, et al. Mechanical ventilation-induced diaphragm atrophy strongly impacts clinical outcomes. Am J Respir Crit Care Med 2018;197(2):204-13. doi: 10.1164/rccm.201703-0536OC [Crossref]
  5. Sklar MC, Dres M, Fan E, Rubenfeld GD, Scales DC, Herridge MS, et al. Association of low baseline diaphragm muscle mass with prolonged mechanical ventilation and mortality among critically ill adults. JAMA Network Open 2020;3(2):e1921520. doi: 10.1001/jamanetworkopen.2019.21520 [Crossref]
  6. Dres M, Dubé B-P, Mayaux J, Delemazure J, Reuter D, Brochard L, 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(1):57-66. doi: 10.1164/rccm.201602-0367OC [Crossref]
  7. Medrinal C, Prieur G, Frenoy E, Quesada AR, Poncet A, Bonnevie T, et al. Respiratory weakness after mechanical ventilation is associated with one-year mortality - a prospective study. Crit Care 2016;20(1):231. doi: 10.1186/s13054-016-1418-y [Crossref]
  8. Geiseler J, Kelbe C. Weaning from mechanical ventilation. Weaning categories and weaning concepts. Med Klin Intensivmed Notfmed 2016;111:208-14. doi: 10.1007/s00063-016-0147-y [Crossref]
  9. Goligher EC, Fan E, Herridge MS, Murray A, Vorona S, Brace D, et al. Evolution of diaphragm thickness during mechanical ventilation. Impact of inspiratory effort. Am J Respir Crit Care Med 2015;192(9):1080. doi: 10.1164/rccm.201503-0620OC [Crossref]
  10. Palkar A, Mayo P, Singh K, Koenig S, Narasimhan M, Singh A, et al. Serial diaphragm ultrasonography to predict successful discontinuation of mechanical ventilation. Lung 2018;196:363-8. doi: 10.1007/s00408-018-0106-x [Crossref]
  11. Öztürk E, Tanıdır İC, Yıldız O, Yükçü B, Ergün S, Haydın S, et al. Ultrasonographic postoperative evaluation of diaphragm function of patients with congenital heart defects. Turk Gogus Kalp Dama 2020;28(1):70-5. doi: 10.5606/tgkdc.dergisi.2020.18458 [Crossref]
  12. Abbas A, Embarak S, Walaa M, Lutfy SM. Role of diaphragmatic rapid shallow breathing index in predicting weaning outcome in patients with acute exacerbation of COPD. Int J COPD 2018;13:1655-61. doi: 10.2147/COPD.S161691 [Crossref]
  13. Carrie C, Gisbert-Morae C, Bonnardel E, Gauche B, Matthieu B, Vargas F, et al. Ultrasonographic diaphragmatic excursion is inaccurate and not better than the MRC score for predicting weaning-failure in mechanically ventilated patients. Anaesth Crit Care Pain Med 2016:1-27. doi: 10.1016/j.accpm.2016.05.009 [Crossref]
  14. Llamas-Álvarez AM, Tenza-Lozano EM, Latour-Pérez J. Diaphragm and lung ultrasound to predict weaning outcome: systematic review and meta-analysis. Chest 2017;52(6):1140-50. doi: 10.1016/j.chest.2017.08.028 [Crossref]
  15. Moher D, Liberati A, Tetzlaff J, Altman DG, The PRISMA Group. Preferred Reporting Items for Systematic Reviews and Meta-Analyses: The PRISMA Statement. PLoS Med.2009;6(7):e1000097
  16. Sklar MC, Dres M, Fan E, Rubenfeld GD, Scales DC, Herridge MS, et al. Association of low baseline diaphragm muscle mass with prolonged mechanical ventilation and mortality among critically Ill Adults. JAMA Network Open. 2020;3(2):e1921520. doi: 10.1001/jamanetworkopen.2019.21520 [Crossref]
  17. Viver E, Muller M, Putegnat Jean-Baptiste, Steyer J, Barrau S, Boissier F, et al. Inability of diaphragm ultrasound to predict extubation failure a multicenter study. Chest 2019;155(6):1131-9. doi: 10.1016/j.chest.2019.03.004 [Crossref]
  18. Eltrabili HH, Hasanin AM, Soliman MS, Lofty AM, Hamimy WI, Mukhtar AM. Evaluation of diaphragmatic ultrasound indices as predictors of successful liberation from mechanical ventilation in subjects with abdominal sepsis. Respir Care 2019;64(5):564-9. doi: 10.4187/respcare.06391 [Crossref]
  19. Zhang X, Yuan J, Zhan Y, Wu J, Liu B, Zhand P, Yu T, et al. Evaluation of diaphragm ultrasound in predicting extubation outcome in mechanically ventilated patients with COPD. Ir J Med Sci 2020;189(2):661-8. doi: 10.1007/s11845-019-02117-1 [Crossref]
  20. Palkar A, Mayo P, Singh K, Koenig S, Narasimhan, Singh A, et al. Serial diaphragm ultrasonography to predict successful discontinuation of mechanical ventilation. Lung 2018;196(3):363-8. doi: 10.1007/s00408-018-0106-x [Crossref]
  21. Dres M, Dube Bruno-Pierre, Mayaux J, Delemazure J, Reuter D, Brochard L, 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(1):57-66. doi: 10.1164/rccm.201602-0367OC [Crossref]
  22. Khan M, Munawar K, Hussain S, Qadeer A, Saeed ML, Shad ZS, et al. Comparing ultrasound-based diaphragmatic excursion with rapid shallow breathing index as a weaning predictor. Cureus 2018;10(12):3710. doi: 10.7759/cureus.3710 [Crossref]
  23. Soliman SB, Ragab F, Soliman RA, Gaber A, Kamal A. Chest Ultrasound in predication of weaning failure. Open Access Maced J Med Sci 2019;7(7):1143-47. doi: 10.3889/oamjms.2019.277 [Crossref]
  24. Huang D, Ma H, Zhong W, Wang X, Wu Y, Qin T, et al. Using M-mode ultrasonography to assess diaphragm dysfunction and predict the success of mechanical ventilation weaning in elderly patients. J Thorac Dis 2017;9(9):3177-86. doi: 10.21037/jtd.2017.08.16 [Crossref]
  25. Pirompanich P, Romsaiyut S. Use of diaphragm thickening fraction combined with rapid shallow breathing index for predicting success of weaning from mechanical ventilator in medical patients. J Intensive Care 2018;6:6. https://10.1186/s40560-018-0277-9 [Crossref]
  26. Yoo Jung-Wan, Lee SJ, Lee JD, Kim HC. Comparison of clinical utility between diaphragm excursion and thickening change using ultrasonography to predict extubation success. Korean J Intern Med 2018;33:331-9. doi: 10.3904/kjim.2016.152.e1 [Crossref]