Pulmonary Function Tests Post-Stroke. Correlation between Lung Function, Severity of Stroke, and Improvement after Respiratory Muscle Training
Abstract
:1. Introduction
2. Materials and Methods
3. Results
Author/Date | Study Population/Mean Age/Gender (M/F) | Type of Study | Type of Stroke | Follow-Up Time | Scale of Stroke Severity | Study Aim | Results |
---|---|---|---|---|---|---|---|
Annoni J.M. et al. 1990 [11] | 23 non-smoking hemiplegic patients in the acute phase (53, 12/11) | Case–control | Any type | - | - | Correlation of PFTs with proximal arm function | FIVC and FEVC were reduced with time, independent of motor impairment but related to duration of illness. Patients exhibited a restrictive respiratory pattern. PEF and MEF were reduced by 75%. |
De Almeida I.C. et al. [16] 2011 | 8 patients with right side hemiplegia (51.25 ± 13.8, 4/4), 12 patients with left side hemiplegia (55.33 ± 9.57, 4/8) and 8 controls (52.12 ± 7.28, 5/3) | Case–control | Any type | - | Motor Assessment Scale | Comparison of PFTs and diaphragmatic excursion between groups | MIP significantly better in controls compared to patients with hemiplegia. FEF25–75% and PEF significantly correlated to left diaphragmatic excursion. IC was not changed. No difference of FVC%, FEV1%, FEV1/FVC (small number of patients able to perform these PFT maneuvers) |
Ezeugwu et al. 2013 [12] | 35 patients with stroke (55.8 ± 8.99, 21/14) and 35 healthy controls (55.6 ± 9.03, 21/14) | Case–control, cross-sectional | Any type | - | - | Comparison of PFTs between stroke patients and controls, correlation with chest excursion | Lower FEV1, FVC and PEF in stroke patients. Obstructive and restrictive pattern in stroke patients. Lower chest excursion in stroke patients. No correlation between chest excursion and PFTs. |
Fugl-Meyer et al. [17] 1983 | 54 patients with stroke and hemiplegia or hemiparesis | Cross-sectional | Any type | - | - | Correlation of PFTs with stroke severity | PFTs, MIP, MEP, lung compliance and resistance related to the degree of motor impairment and to the interval between stroke and investigation. Lower IC six months after stroke, more evident restrictive disturbance. |
Jandt S.R. et al. 2011 [18] | 21 patients with stroke (58.9 ± 13.5, 12/9) | Observative, descriptive | Any type | - | - | Correlation of PFTs with trunk impairment scale (TIS) | Significant correlation between TIS and PEF and between TIS and MEF. No correlation of TIS with FEV1, FVC, FEV1/FVC and MIF. |
Jeong Y. et al. 2020 [13] | 52 patients with stroke within six months of onset (34/18) | Prospective | Any type | 4 weeks | NIHSS score, Berg Balance Scale | Correlation of PFTs at baseline and 4 weeks after rehabilitation with TIS, Berg Balance Scale and functional independence measure | Baseline FVC, FEV1 and PEF correlated with initial TIS. Initial PEF significantly associated with Berg Balance Scale and Functional Independence Measure. No correlation with MIP and MEP. |
Jung et al. 2014 [19] | 10 stroke patients (59.7 ± 12.9, 8/2) and 16 healthy controls (56.1 ± 9.3, 6/10) | Case–control | Any type | - | Korean Modified Barthel Index | Correlation of diaphragmatic excursion with PFTs | Restrictive PFTs in stroke patients. Left diaphragmatic excursion reduction correlated with reduced FEV1 and FVC in stroke patients. |
Khedr et al. 2000 [20] | 34 acute stroke patients (57.23 ± 13.26, 24/10) and 25 healthy volunteers (47.2 ± 22, 17/8) | Case–control, cross-sectional | Ischemic stroke | - | Scandinavian Stroke Scale | Comparison of diaphragmatic excursion and PFTs between groups; no PFTs in healthy controls | 41% of the stroke group had decreased diaphragmatic excursion and 70% decreased magnetic evoked potentials. Hemiplegic patients with restrictive PFTs. Negative correlation of FEV1, FVC and FEV1/FVC with motor mobility and excitability threshold of affected hemisphere. |
Kimura Y et al. 2013 [21] | 20 stroke patients without dysphagia (65.7 ± 8.1), 10 stroke patients with dysphagia (74.1 ± 10.2) and 10 healthy controls (68.2 ± 7.2) all male | Case–control, cross-sectional | Any type | - | Brunnstrom’s recovery stage | Comparison of peak cough flow and spirometry between groups | Lower peak cough flow and IRV in stroke patients with dysphagia compared to healthy controls. Lower peak cough flow in stroke patients with dysphagia vs. without dysphagia. No differences in ERV or TV between groups. |
Kulnik S.T. et al. 2016 [22] | 72 patients with stroke (64.6 ± 14.4, 42/30) | Single blind randomised control trial | Any type | 4 weeks | NIHSS score | Comparison of peak cough flow in voluntary and reflex cough | Weaker flow in patients’ aspiration pneumonia. |
Liaw M.Y. et al. 2016 [23] | 47 stroke patients with congestive heart failure (65.9 ± 11.5, 24/23) | Cohort | Any type | - | Brunnstrom stage, Barthel Index | Correlation of PFTs with Brunnstrom change | MIP negatively associated with Brunnstrom stage of the proximal and distal parts of the upper extremities and lower extremities, FVC, predicted FVC% and FEV1%. MEP positively associated with average Brunnstrom stage of the distal area of the upper extremities, FVC, FEV1, and FEV1/FVC. FEV1/FVC negatively associated with the average Brunnstrom stage. Stroke patients had restrictive lung disorder and respiratory muscle weakness, associated with the neurological status of the affected limbs. |
Lista Paz A. et al. 2016 [24] | 30 chronic stroke patients with a diagnosis of hemiplegia/hemiparesis who were able to walk (55.60 ± 15.84, 22/8) and 30 healthy controls (55.33 ± 14.61, 22/8) | Observational, cross-sectional | Any type | - | Scale Impact of Stroke version 16.0 | Comparison of MIP and MEP between groups | Significantly lower MIP and MEP in patients with stroke, <60%. Other spirometry parameters not measured. |
Lista-Paz A. et al. 2023 [25] | 33 patients with stroke (56.9 ± 15.7, 24/9) and 33 healthy controls (56.2 ± 15.2, 24/9) | Observational, cross-sectional | Any type | - | Stroke Impact Scale version 16.0 | Comparison of PFTs and 6MWT between groups | Stroke patients had significantly lower lung volumes and capacities (VC, FVC, FEV1, ERV, IC), than controls. Median FVC was 79% and PEF 64% of the reference value. The weak correlation of 6MWD with inspiratory reserve volume and PIF. |
Luvizutto G.J. et al. 2017 [26] | 32 patients with acute stroke (14/18) | Cross-sectional | Ischemic stroke | - | NIHSS score, mRS score | Correlation of MIP and MEP with anthropometric data and neurologic severity | Lower MIP and MEP than predicted. No association with neurologic severity, positive association with BMI. Other spirometry parameters not measured. |
Min S.W. et al. 2018 [27] | 57 patients with stroke (69.58 ± 10.29, 34/23) | Cross-sectional | Ischemic stroke | - | - | Correlation of PFTs with dysphagia and aspiration pneumonia | Increased dysphagia associated with worse PCF, FVC and FEV1 values and aspiration pneumonia. |
Nunez Filha M.C. et al. 2020 [28] | 53 patients with stroke (55 ± 13.43, 27/26) | Cross-sectional | Any type | - | NIHSS, Modified Barthel Index | Correlation of MIP and MEP and stroke severity with functional mobility | MIP, but not MEP, was independently associated with functional mobility in multivariate analysis. No other spirometry parameters were measured. |
Pinheiro M.B. et al. 2014 [29] | 89 patients with stroke (56.2 ± 12.0, 48/41) | Cross-sectional, observational | Any type | 2 days | - | Correlation of MIP and MEP with stroke population (community vs. non-community ambulators) | Stroke subjects demonstrated decreases of 26.5 and 20% in the MIP and MEP. Significantly worse MIP values seen in non-community ambulators but not statistical significance of MEP, FEV1 and FVC between community and non-community ambulators. |
Santos R.S.D. et al. 2019 [30] | 44 patients with stroke (59.4 ± 12.2, 19/25) | Cross-sectional | Any type | - | Functional Independence Measure scale | Correlation of PFTs, MIP and MEP with TIS and Functional Independence Measure | Lower PFTs, MIP and MEP of predicted values, correlation of TIS with FVC, FEV1 and MIP but not with MEP |
Sezer N. et al. 2004 [31] | 20 patients with stroke (54.25 ± 11.42, 9/11) and 15 controls (9/6) | Cross-sectional | Any type | - | Brunnstrom classification stage, Barthel Index, Massachusetts General Hospital Functional Ambulation Classification | Comparison of cardiopulmonary response between groups | FEV1, FVC, VC, PEF and MVV reduced in patients with stroke compared with controls but no correlation with motor disability. FEF25–75% and FEV1/FVC no different between groups. Significant respiratory dysfunction in hemiplegic patients. |
Teixeira-Salmela L.F. et al. 2005 [32] | 16 community-dwelling stroke survivors (58.37 ± 15.47, 8/8) and 19 age-matched healthy subjects (60.21 ± 4.47, 9/10) | Descriptive case–control | Any type | - | - | Comparison of PFTs, MIP and MEP between stroke patients and controls | Significantly lower MIP and MEP in stroke patients compared to controls and decreased abdominal contribution to tidal volume. Dynamic lung volumes not measured. |
Voyvoda et al. 2011 [33] | 23 hemiplegic patients (60.5 ± 10.7, 13/10) and 20 controls (61.2 ± 12.1, 13/7) | Descriptive case–control | Ischemic stroke | - | - | Comparison of diaphragm motility with ultrasonography and PFTs between groups | Significantly worse PFTs (FEV1, FVC, FEV1/FVC, MIP and MEP) in hemiplegic patients compared to control. No evidence of obstructive disturbance. No significance in diaphragmatic excursion between groups. |
Xiao L.J. et al. 2020 [34] | 30 patients with stroke and dysphagia (53 ± 11, 20/10), 30 with stroke without dysphagia (59 ± 11, 17/13) and 30 healthy controls (55 ± 18, 18/12) | Descriptive case–control | Any type | - | - | Comparison PFTs between patients with dysphagia after stroke, patients without dysphagia and normal people. Correlation between swallowing function and pulmonary function. | Patients with dysphagia had significantly lower PEF, MIP, MEP FVC, FEF25–75% and FIV but not FEV1 compared to those without dysphagia. |
3.1. Baseline PFTs in Stroke Survivors
3.2. Lung Volumes and Flows in Stroke Patients
3.3. MIP and MEP in Stroke Patients
3.4. Correlation of PFTs with Functional Impairment
3.5. Correlation of PFTs with Dysphagia and Risk of Aspiration
3.6. Correlation of PFTs with Diaphragmatic Dysfunction
Author/Date | Study Population/MEAN Age/Gender (M/F) | Type of Study | Type of Stroke | Follow-Up Time | Scale of Stroke Severity | Study Aim | Results |
---|---|---|---|---|---|---|---|
Aydogan A.S. et al. 2022 [35] | 21 stroke patients: 11 in the treatment group (61.72 ± 10.77, 5/6) and 10 in the control group (66.10 ± 8.87, 2/8) | Single blinded randomised controlled trial | Any type | 6 weeks | - | PFTs, stroke severity scores before and after a neurodevelopmental treatment program and IMT in the treatment arm | Significantly better PEF and MIP in the treatment group |
Britto R.R. et al. 2011 [36] | 18 patients with chronic stroke: 9 in the experimental group (56.66 ± 5.56, 5/4) and 9 in the control group (51.44 ± 15.98, 4/5) | Randomised controlled trial | Any type | 8 weeks | - | Comparison of MIP, inspiratory muscular resistance before and after IMT | Significantly better values for MIP and inspiratory muscular resistance in the intervention group compared to baseline |
Chen P.C. et al. 2016 [37] | 21 patients with stroke and congestive heart failure: 11 in the IMT group (63.73 ± 14.64, 4/7) and 10 in the control group (67.50 ± 10.35, 4/6) | Randomised controlled trial | Any type | 10 weeks | Barthel Index | Comparison of spirometry, MIP and MEP between IMT group and control | Significant better values of FEV1, FVC, MIP and Barthel Index in the intervention group compared to baseline and in MIP compared to the control group |
Cho J.E. et al. 2018 [38] | 25 patients with stroke: 12 in the experimental group (47.58 ± 13.00, 7/5) and 13 in the control group (52.53 ± 9.06, 6/7) | Randomised controlled trial | Any type | 6 weeks | - | Comparison of diaphragm thickness ratio, MIP and inspiratory muscle endurance between IMT group and control | Increased diaphragm thickness, MIP and inspiratory muscle endurance in the IMP group |
Guillen-Sola A. et al. 2017 [39] | 62 patients with dysphagia and stroke (69.0 ± 8.7, 38/24) | Randomised controlled trial | Ischemic stroke | 3 months | NIHSS score on admission, mRS score, Barthel Index on admission at Rehabilitation | Comparison of dysphagia score, MIP and MEP after a 3-week rehabilitation program and in 3 months between standard shallow therapy group, standard shallow therapy with IEMS and standard shallow therapy and neuromuscular electric simulation | MIP and MEP significantly improved in the standard shallow therapy with IEMS, compared to the other groups |
Jung K.M. et al. 2017 [40] | 12 patients with hemiparesis due to stroke: 6 in the experimental group (61.2 ± 4.2, 2/4) and 6 in the control group (62.2 ± 5.3, 3/3) | Randomised controlled trial | Any type | 4 weeks | - | Comparison of PFTs and walking ability between IMT group vs. aerobic exercise group | Significant improvement of FEV1, FVC in both groups, significantly better FEV1, FVC in the IMT group |
Kilicoglou M.S. et al. 2022 [41] | 41 patients with stroke: 20 in the treatment group (64.6 ± 12.4, 10/10) and 21 in the control group (66.0 ± 10.3, 8/13) | Randomised-controlled trial | Any type | 6 weeks | - | Effect of respiratory exercise program on PFTs and diaphragm ultrasound parameters | FVC, FEV1, FEV1/FVC and diaphragm ultrasound parameters were improved after treatment in the intervention group |
Kim C.Y. et al. 2015 [42] | 37 patients with post-stroke hemiplegia: 12 in the integrated training group (57.53 ± 7.73, 7/5), 13 in the respiratory muscle training group (59.20 ± 6.12, 6/7) and 12 in the control group (60.53 ± 0.38, 4/8) | Randomised controlled trial | Any type | 6 weeks | - | Comparison of PFTs between controls, RMT and RMT plus abdominal drawing-in maneuver groups | Significantly better FEV1, FVC and EMG diaphragm activation in the RMT and abdominal drawing-in maneuver group |
Kim J. et al. 2014 [43] | 20 stroke patients: 10 in the exercise group (54.10 ± 11.69) and 10 in the control group (53.90 ± 5.82) | Randomised-controlled trial | Any type | 4 weeks | - | Effects of respiratory muscle and endurance training using an individualized training device for respiratory muscle training on PFTs and exercise capacity in stroke patients | FVC, FEV1, PEF and 6MWT significantly better in the intervention group |
Kulnik et al. 2015 [44] | 82 patients with stroke within two weeks of stroke onset (64 ± 14, 49/33) | Single-blind randomized placebo-controlled trial | Any type | 4 weeks | NIHSS score | Change in peak expiratory cough flow in patients with IMT, EMT and no respiratory muscle training | Significantly better values compared to baseline in all groups with no effect of training |
Lee K. et al. 2019 [45] | 25 chronic stroke patients, able to sit independently: 13 in the RMT group (58.62 ± 12.38, 7/6) and 12 in the TSE group (59.75 ± 13.38, 5/7) | Pilot randomised controlled trial | Any type | 6 weeks | mRS score | Comparison of PFTs between patients with progressive RMT with and without trunk stabilisation exercise | The MEP, PEF, MIP and PIF were significantly increased in the RMT group than in the control group |
Lee D.K et al. 2018 [46] | 24 chronic stroke patients: 12 in the experimental group (61.7 ± 6.2, 6/6) and 12 the control group (59.2 ± 4.6, 6/6) | Randomised controlled trials | Any type | 4 weeks | - | Comparison of PFTs, TIS and muscle activity of the trunk in patients who received neurodevelopmental treatment alone or with respiratory exercise | Significant better FVC, FEV1, TIS, Rectus Abdominis, internal oblique and external oblique in the respiratory exercise group |
Liaw M.Y. et al. 2020 [47] | 21 patients with stroke within six months of unilateral stroke, dysphagia, dysarthria and respiratory muscle weakness (63.86 ± 11.16, 12/9) | Randomised controlled trial | Any type | 6 weeks | mRS score, Barthel Index | Comparison of PFTs after IERMT and control group | FVC, FEV1 and MIP were significantly better in the intervention group |
Messagi-Sartor M. et al. 2015 [48] | 109 patients with subacute stroke (66.5 ± 11.2, 63/46) | Randomised controlled trial | Ischemic stroke | 6 months | NIHSS score, Barthel Index, mRS score | Comparison of MIP and MEP in the IEMT and the control group | Improved respiratory muscle strength in the intervention and control group. In IEMT group significantly improved MIP and MEP. Respiratory complications at 6 months more often in the control group, risk reduction of 14%. |
Oh D. et al. 2016 [49] | 23 stroke patients: 11 in the experimental group (69.7 ± 6.8, 6/5) and 12 in the control group (71.6 ± 7.9, 7/5) | Randomised controlled trial | Any type | 6 weeks | - | Comparison of abdominal muscle thickness and PFTs of the IMT group vs. conventional therapy group | FVC, FEV1, deep abdominal muscle thickness and Berg Balance Scale scores significantly improved in the experimental group |
Parreiras de Menezes K.K. et al. 2019 [50] | 38 patients with stroke and respiratory muscle weakness: 19 in the experimental group (60 ± 14, 8/11), 19 in the control group (67 ± 11, 8/11) | Double-blind randomised trial | Any type | 8 weeks | - | Comparison of MIP, MEP, respiratory complications in the RMT group with high-intensity home-based program vs. control group | Significant increase in MIP, MEP, endurance of respiratory muscles and reduction of dyspnea in intervention group |
Ptaszkowska et al. 2019 [51] | 60 stroke patients: 30 PNF-treated (64 ± 5, 20/10), 30 PNF-untreated (64 ± 7, 22/8) | Randomised controlled trial | Ischemic stroke | - | Barthel Index | Comparison of PFTs after respiratory stimulation through Proprioceptive Neuromuscular Facilitation (PNF) and controls | FEV1/FVC% values in PNF-untreated group was substantially lower than in PNF-treated group |
Rattes C. et al. 2018 [52] | 10 stroke patients with right hemiparesis (60 ± 5.7, 8/2) | Randomised controlled trial | Any type | 3 days | Barthel Index | Comparison of PFTs between respiratory stretching group and control | MIF, MEF and VT increased in respiratory stretching group compared to control group |
Song G.B. et al. 2015 [53] | 40 patients with stroke: 20 in the CRE group (55.50 ± 11.43, 12/8) and 20 in the CEE group (58.30 ± 11.10, 11/9) | Randomised controlled trial | Any type | 8 weeks | - | Comparison of a chest resistance and a chest expansion intervention group regarding PFTs and TIS | Significantly better FVC, FEV1 and TIS in both groups, TIS significantly better in the chest resistance intervention group |
Sutbeyaz S.T. et al. 2010 [54] | 45 patients with stroke, randomised in three groups: 15 in IMT (62.8 ± 7.2, 8.7); 15 in breathing retraining, diaphragmatic breathing and pursed-lips breathing (60.8 ± 6.8, 8/7); 15 control group (61.9 ± 6.15, 8/7). | Randomised controlled trial | Any type | 6 weeks | Barthel Index | Effect of exercise--breathing retraining (BRT) and IMT--improve on cardiopulmonary functions | In IMT group significantly improved FEV1, FVC, VC and FEF25–75%, compared with the BRT and control groups. PEF was increased significantly in the BTR group compared with the IMT and control groups. MIP and MEP increased in the BRT group and MIP in the IMT group compared with baseline and the control group. |
Tovar-Alcaraz et al. 2021 [55] | 16 stroke survivors in the subacute phase: 8 in the experimental group (58 ± 12.9, 6/2) and 8 in the control group (56 ± 9.2, 6/2) | Randomised controlled trial | Any type | 8 weeks | Postural Scale for Stroke Patients (PASS), Berg scale | Comparison of MIP, PFTs, trunk and postural control in the IMT group vs. control | Significant increase in MIP compared to baseline in both groups, more significant in the IMT group |
Vaz L. et al. 2021 [56] | 50 patients with stroke with inspiratory muscle weakness (53 ± 11, 21/29) | Randomised controlled trial | Any type | 3 months | NIHSS score, Fugl-Meyer Assessment | Comparison of 6MWT, MIP, MEP in a group after IMT and without | Change in 6MWD in both groups but no difference in MIP, MEP after intervention |
Yoo H.J et al. 2018 [57] | 40 patients with stroke: 20 in the intervention group (14/6) and 20 in the control group (12/8) | Randomised controlled trial | Any type | 3 weeks | NIHSS score, Modified Barthel Index, Berg Balance Scale, Fugl-Meyer Assessment | Comparison of PFTs and stroke severity scores in two groups assigned either to bedside IEMT or no intervention | PFTs significantly improved in the intervention group after 3 weeks of IEMT independent of the improvement in stroke-related disabilities |
Zheng Y. et al. 2021 [58] | 60 patients within two months post-stroke: 30 in the experimental group (63.50 ± 10.36, 24/6) and 30 in the control group (67.23 ± 9.15, 19/11) | Randomised controlled trial | Any type | 3 weeks | Berg Balance Scale, Modified Barthel Index | Comparison of PFTs, stroke severity scores of the RMT group using Liuzijue Qigong vs. conventional respiratory training | Significant improvement in MIP, FVC and PEF in both groups, better MIP and MEP and TIS in the Liuzijue Qigong group |
3.7. Change in PFTs after Respiratory Muscle Training in Stroke Survivors
3.8. Stroke Population
3.9. Type of Respiratory Muscle Training Intervention
3.10. Outcomes Measured
4. Discussion
5. Limitations
6. Conclusions
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Conflicts of Interest
Abbreviations
References
- Gkantzios, A.; Tsiptsios, D.; Karatzetzou, S.; Kitmeridou, S.; Karapepera, V.; Giannakou, E.; Vlotinou, P.; Aggelousis, N.; Vadikolias, K. Stroke and Emerging Blood Biomarkers: A Clinical Prospective. Neurol. Int. 2022, 14, 784–803. [Google Scholar] [CrossRef] [PubMed]
- Gomes-Neto, M.; Saquetto, M.B.; Silva, C.M.; Carvalho, V.O.; Ribeiro, N.; Conceição, C.S. Effects of Respiratory Muscle Training on Respiratory Function, Respiratory Muscle Strength, and Exercise Tolerance in Patients Poststroke: A Systematic Review With Meta-Analysis. Arch. Phys. Med. Rehabil. 2016, 97, 1994–2001. [Google Scholar] [CrossRef] [PubMed]
- Javaheri, S.; Peker, Y.; Yaggi, H.K.; Bassetti, C.L.A. Obstructive sleep apnea and stroke: The mechanisms, the randomized trials, and the road ahead. Sleep Med. Rev. 2022, 61, 101568. [Google Scholar] [CrossRef]
- Kishore, A.K.; Vail, A.; Chamorro, A.; Garau, J.; Hopkins, S.J.; Di Napoli, M.; Kalra, L.; Langhorne, P.; Montaner, J.; Roffe, C.; et al. How is pneumonia diagnosed in clinical stroke research? A systematic review and meta-analysis. Stroke 2015, 46, 1202–1209. [Google Scholar] [CrossRef]
- Pelosi, P.; Severgnini, P.; Chiaranda, M. An integrated approach to prevent and treat respiratory failure in brain-injured patients. Curr. Opin. Crit. Care 2005, 11, 37–42. [Google Scholar] [CrossRef]
- Miller, M.R.; Crapo, R.; Hankinson, J.; Brusasco, V.; Burgos, F.; Casaburi, R.; Coates, A.; Enright, P.; van der Grinten, C.P.M.; Gustafsson, P.; et al. General considerations for lung function testing. Eur. Respir. J. 2005, 26, 153–161. [Google Scholar] [CrossRef]
- Hozawa, A.; Billings, J.L.; Shahar, E.; Ohira, T.; Rosamond, W.D.; Folsom, A.R. Lung function and ischemic stroke incidence: The Atherosclerosis Risk in Communities study. Chest 2006, 130, 1642–1649. [Google Scholar] [CrossRef] [PubMed]
- Truelsen, T.; Prescott, E.; Lange, P.; Schnohr, P.; Boysen, G. Lung function and risk of fatal and non-fatal stroke. The Copenhagen City Heart Study. Int. J. Epidemiol. 2001, 30, 145–151. [Google Scholar] [CrossRef]
- Wannamethee, S.G.; Shaper, A.G.; Ebrahim, S. Respiratory function and risk of stroke. Stroke 1995, 26, 2004–2010. [Google Scholar] [CrossRef]
- Duong, M.; Islam, S.; Rangarajan, S.; Leong, D.; Kurmi, O.; Teo, K.; Killian, K.; Dagenais, G.; Lear, S.; Wielgosz, A.; et al. Mortality and cardiovascular and respiratory morbidity in individuals with impaired FEV1 (PURE): An international, community-based cohort study. Lancet Glob. Health 2019, 7, e613–e623. [Google Scholar] [CrossRef]
- Annoni, J.-M.; Ackermann, D.; Kesselring, J. Respiratory function in chronic hemiplegia. Int. Disabil. Stud. 1990, 12, 78–80. [Google Scholar] [CrossRef] [PubMed]
- Ezeugwu, V.E.; Olaogun, M.; Mbada, C.E.; Adedoyin, R. Comparative lung function performance of stroke survivors and age-matched and sex-matched controls. Physiother. Res. Int. 2013, 18, 212–219. [Google Scholar] [CrossRef] [PubMed]
- Jeong, Y.J.; Kim, G.S.; Jeong, Y.G.; Moon, H.I. Can Pulmonary Function Testing Predict the Functional Outcomes of Poststroke Patients?: An Observational Study. Am. J. Phys. Med. Rehabil. 2020, 99, 1145–1149. [Google Scholar] [CrossRef] [PubMed]
- Van Criekinge, T.; Truijen, S.; Schröder, J.; Maebe, Z.; Blanckaert, K.; van der Waal, C.; Vink, M.; Saeys, W. The effectiveness of trunk training on trunk control, sitting and standing balance and mobility post-stroke: A systematic review and meta-analysis. Clin. Rehabil. 2019, 33, 992–1002. [Google Scholar] [CrossRef] [PubMed]
- Fabero-Garrido, R.; del Corral, T.; Angulo-Díaz-Parreño, S.; Plaza-Manzano, G.; Martín-Casas, P.; Cleland, J.A.; Fernández-de-Las-Peñas, C.; López-de-Uralde-Villanueva, I. Respiratory muscle training improves exercise tolerance and respiratory muscle function/structure post-stroke at short term: A systematic review and meta-analysis. Ann. Phys. Rehabil. Med. 2022, 65, 101596. [Google Scholar] [CrossRef]
- de Almeida, I.C.L.; Clementino, A.C.C.R.; Rocha, E.H.T.; Brandão, D.C.; de Andrade, A.D. Effects of hemiplegy on pulmonary function and diaphragmatic dome displacement. Respir. Physiol. Neurobiol. 2011, 178, 196–201. [Google Scholar] [CrossRef]
- Fugl-Meyer, A.R.; Linderholm, H.; Wilson, A.F. Restrictive ventilatory dysfunction in stroke: Its relation to locomotor function. Scand. J. Rehabil. Med. Suppl. 1983, 9, 118–124. [Google Scholar]
- Jandt, S.R.; Caballero, R.M.d.S.; Junior, L.A.F.; Dias, A.S. Correlation between trunk control, respiratory muscle strength and spirometry in patients with stroke: An observational study. Physiother. Res. Int. 2011, 16, 218–224. [Google Scholar] [CrossRef]
- Jung, K.-J.; Park, J.-Y.; Hwang, D.-W.; Kim, J.-H.; Kim, J.-H. Ultrasonographic diaphragmatic motion analysis and its correlation with pulmonary function in hemiplegic stroke patients. Ann. Rehabil. Med. 2014, 38, 29–37. [Google Scholar] [CrossRef]
- Khedr, E.M.; El Shinawy, O.; Khedr, T.; Abdel Aziz Ali, Y.; Awad, E.M. Assessment of corticodiaphragmatic pathway and pulmonary function in acute ischemic stroke patients. Eur. J. Neurol. 2000, 7, 509–516. [Google Scholar] [CrossRef]
- Kimura, Y.; Takahashi, M.; Wada, F.; Hachisuka, K. Differences in the peak cough flow among stroke patients with and without dysphagia. J. UOEH 2013, 35, 9–16. [Google Scholar] [CrossRef] [PubMed]
- Kulnik, S.T.; Birring, S.S.; Hodsoll, J.; Moxham, J.; Rafferty, G.F.; Kalra, L. Higher cough flow is associated with lower risk of pneumonia in acute stroke. Thorax 2016, 71, 474–475. [Google Scholar] [CrossRef]
- Liaw, M.-Y.; Wang, L.-Y.; Pong, Y.-P.; Tsai, Y.-C.; Huang, Y.-C.; Yang, T.-H.; Lin, M.-C. Preliminary investigation of cardiopulmonary function in stroke patients with stable heart failure and exertional dyspnea. Medicine 2016, 95, e5071. [Google Scholar] [CrossRef] [PubMed]
- Lista Paz, A.; Gonzalez Doniz, L.; Ortigueira Garcia, S.; Saleta Canosa, J.L.; Moreno Couto, C. Respiratory Muscle Strength in Chronic Stroke Survivors and Its Relation With the 6-Minute Walk Test. Arch. Phys. Med. Rehabil. 2016, 97, 266–272. [Google Scholar] [CrossRef]
- Lista-Paz, A.; Kuisma, R.; Canosa, J.L.S.; Sebio García, R.; Gonzalez Doniz, L. Pulmonary function in patients with chronic stroke compared with a control group of healthy people matched by age and sex. Physiother. Theory Pract. 2023, 39, 918–926. [Google Scholar] [CrossRef] [PubMed]
- Luvizutto, G.J.; Dos Santos, M.R.L.; Sartor, L.C.A.; da Silva Rodrigues, J.C.; da Costa, R.D.M.; Braga, G.P.; de Oliveira Antunes, L.C.; Souza, J.T.; de Carvalho Nunes, H.R.; Bazan, S.G.Z.; et al. Evaluation of Respiratory Muscle Strength in the Acute Phase of Stroke: The Role of Aging and Anthropometric Variables. J. Stroke Cerebrovasc. Dis. 2017, 26, 2300–2305. [Google Scholar] [CrossRef]
- Min, S.W.; Oh, S.H.; Kim, G.C.; Sim, Y.J.; Kim, D.K.; Jeong, H.J. Clinical Importance of Peak Cough Flow in Dysphagia Evaluation of Patients Diagnosed With Ischemic Stroke. Ann. Rehabil. Med. 2018, 42, 798–803. [Google Scholar] [CrossRef]
- Nunez Filha, M.C.; Mascarenhas, L.; Messias, D.; Furtado, C.; Dias, C.; Dantas, M.C.; Almeida, L.R.S.; Pinto, E.B. Stroke Severity and Maximum Inspiratory Pressure are Independently Associated with Functional Mobility in Individuals After Stroke. J. Stroke Cerebrovasc. Dis. 2020, 29, 105375. [Google Scholar] [CrossRef]
- Pinheiro, M.B.; Polese, J.C.; Faria, C.D.; Machado, G.C.; Parreira, V.F.; Britto, R.R.; Teixeira-Salmela, L.F. Inspiratory muscular weakness is most evident in chronic stroke survivors with lower walking speeds. Eur. J. Phys. Rehabil. Med. 2014, 50, 301–307. [Google Scholar]
- Santos, R.S.D.; Dall’alba, S.C.F.; Forgiarini, S.G.I.; Rossato, D.; Dias, A.S.; Forgiarini Junior, L.A. Relationship between pulmonary function, functional independence, and trunk control in patients with stroke. Arq. Neuropsiquiatr. 2019, 77, 387–392. [Google Scholar] [CrossRef]
- Sezer, N.; Ordu, N.K.; Sutbeyaz, S.T.; Koseoglu, B.F. Cardiopulmonary and metabolic responses to maximum exercise and aerobic capacity in hemiplegic patients. Funct. Neurol. 2004, 19, 233–238. [Google Scholar] [PubMed]
- Teixeira-Salmela, L.F.; Parreira, V.F.; Britto, R.R.; Brant, T.C.; Inácio, E.P.; Alcântara, T.O.; Carvalho, I.F. Respiratory pressures and thoracoabdominal motion in community-dwelling chronic stroke survivors. Arch. Phys. Med. Rehabil. 2005, 86, 1974–1978. [Google Scholar] [CrossRef] [PubMed]
- Voyvoda, N.; Yücel, C.; Karataş, G.; Oğuzülgen, I.; Oktar, S. An evaluation of diaphragmatic movements in hemiplegic patients. Br. J. Radiol. 2012, 85, 411–414. [Google Scholar] [CrossRef] [PubMed]
- Xiao, L.J.; Guo, Q.; Huang, F.Y.; Liao, M.X.; Zhang, L.L.; Yan, T.B. [Correlation between swallowing function and pulmonary ventilation function and respiratory muscles strength in patients with dysphagia after stroke]. Zhonghua Yi Xue Za Zhi 2020, 100, 504–508. [Google Scholar] [CrossRef]
- Aydoğan Arslan, S.; Uğurlu, K.; Sakizli Erdal, E.; Keskin, E.D.; Demirgüç, A. Effects of Inspiratory Muscle Training on Respiratory Muscle Strength, Trunk Control, Balance and Functional Capacity in Stroke Patients: A single-blinded randomized controlled study. Top. Stroke Rehabil. 2022, 29, 40–48. [Google Scholar] [CrossRef]
- Britto, R.R.; Rezende, N.R.; Marinho, K.C.; Torres, J.L.; Parreira, V.F.; Teixeira-Salmela, L.F. Inspiratory muscular training in chronic stroke survivors: A randomized controlled trial. Arch. Phys. Med. Rehabil. 2011, 92, 184–190. [Google Scholar] [CrossRef]
- Chen, P.-C.; Liaw, M.-Y.; Wang, L.-Y.; Tsai, Y.-C.; Hsin, Y.-J.; Chen, Y.-C.; Chen, S.-M.; Lin, M.-C. Inspiratory muscle training in stroke patients with congestive heart failure: A CONSORT-compliant prospective randomized single-blind controlled trial. Medicine 2016, 95, e4856. [Google Scholar] [CrossRef]
- Cho, J.-E.; Lee, H.-J.; Kim, M.-K.; Lee, W.-H. The improvement in respiratory function by inspiratory muscle training is due to structural muscle changes in patients with stroke: A randomized controlled pilot trial. Top. Stroke Rehabil. 2018, 25, 37–43. [Google Scholar] [CrossRef]
- Guillén-Solà, A.; Messagi Sartor, M.; Bofill Soler, N.; Duarte, E.; Barrera, M.C.; Marco, E. Respiratory muscle strength training and neuromuscular electrical stimulation in subacute dysphagic stroke patients: A randomized controlled trial. Clin. Rehabil. 2017, 31, 761–771. [Google Scholar] [CrossRef]
- Jung, K.-M.; Bang, D.-H. Effect of inspiratory muscle training on respiratory capacity and walking ability with subacute stroke patients: A randomized controlled pilot trial. J. Phys. Ther. Sci. 2017, 29, 336–339. [Google Scholar] [CrossRef]
- Kılıçoğlu, M.S.; Yurdakul, O.V.; Çelik, Y.; Aydın, T. Investigating the correlation between pulmonary function tests and ultrasonographic diaphragm measurements and the effects of respiratory exercises on these parameters in hemiplegic patients. Top. Stroke Rehabil. 2022, 29, 218–229. [Google Scholar] [CrossRef] [PubMed]
- Kim, C.-Y.; Lee, J.-S.; Kim, H.-D.; Kim, I.-S. Effects of the combination of respiratory muscle training and abdominal drawing-in maneuver on respiratory muscle activity in patients with post-stroke hemiplegia: A pilot randomized controlled trial. Top. Stroke Rehabil. 2015, 22, 262–270. [Google Scholar] [CrossRef]
- Kim, J.; Park, J.H.; Yim, J. Effects of respiratory muscle and endurance training using an individualized training device on the pulmonary function and exercise capacity in stroke patients. Med. Sci. Monit. 2014, 20, 2543–2549. [Google Scholar] [CrossRef] [PubMed]
- Kulnik, S.T.; Birring, S.S.; Moxham, J.; Rafferty, G.F.; Kalra, L. Does respiratory muscle training improve cough flow in acute stroke? Pilot randomized controlled trial. Stroke 2015, 46, 447–453. [Google Scholar] [CrossRef] [PubMed]
- Lee, K.; Park, D.; Lee, G. Progressive Respiratory Muscle Training for Improving Trunk Stability in Chronic Stroke Survivors: A Pilot Randomized Controlled Trial. J. Stroke Cerebrovasc. Dis. 2019, 28, 1200–1211. [Google Scholar] [CrossRef] [PubMed]
- Lee, D.-K.; Kim, S.-H. The effect of respiratory exercise on trunk control, pulmonary function, and trunk muscle activity in chronic stroke patients. J. Phys. Ther. Sci. 2018, 30, 700–703. [Google Scholar] [CrossRef] [PubMed]
- Liaw, M.-Y.; Hsu, C.-H.; Leong, C.-P.; Liao, C.-Y.S.; Wang, L.-Y.; Lu, C.-H.; Lin, M.-C. Respiratory muscle training in stroke patients with respiratory muscle weakness, dysphagia, and dysarthria—A prospective randomized trial. Medicine 2020, 99, e19337. [Google Scholar] [CrossRef] [PubMed]
- Messaggi-Sartor, M.; Guillen-Solà, A.; Depolo, M.; Duarte, E.; Rodríguez, D.A.; Barrera, M.-C.; Barreiro, E.; Escalada, F.; Orozco-Levi, M.; Marco, E. Inspiratory and expiratory muscle training in subacute stroke: A randomized clinical trial. Neurology 2015, 85, 564–572. [Google Scholar] [CrossRef]
- Oh, D.; Kim, G.; Lee, W.; Shin, M.M.S. Effects of inspiratory muscle training on balance ability and abdominal muscle thickness in chronic stroke patients. J. Phys. Ther. Sci. 2016, 28, 107–111. [Google Scholar] [CrossRef]
- Parreiras de Menezes, K.K.; Nascimento, L.R.; Ada, L.; Avelino, P.R.; Polese, J.C.; Mota Alvarenga, M.T.; Barbosa, M.H.; Teixeira-Salmela, L.F. High-Intensity Respiratory Muscle Training Improves Strength and Dyspnea Poststroke: A Double-Blind Randomized Trial. Arch. Phys. Med. Rehabil. 2019, 100, 205–212. [Google Scholar] [CrossRef]
- Ptaszkowska, L.; Ptaszkowski, K.; Halski, T.; Taradaj, J.; Dymarek, R.; Paprocka-Borowicz, M. Immediate effects of the respiratory stimulation on ventilation parameters in ischemic stroke survivors: A randomized interventional study (CONSORT). Medicine 2019, 98, e17128. [Google Scholar] [CrossRef] [PubMed]
- Rattes, C.; Campos, S.L.; Morais, C.; Gonçalves, T.; Sayão, L.B.; Galindo-Filho, V.C.; Parreira, V.; Aliverti, A.; de Andrade, A.D. Respiratory muscles stretching acutely increases expansion in hemiparetic chest wall. Respir. Physiol. Neurobiol. 2018, 254, 16–22. [Google Scholar] [CrossRef] [PubMed]
- Song, G.B.; Park, E.C. Effects of chest resistance exercise and chest expansion exercise on stroke patients’ respiratory function and trunk control ability. J. Phys. Ther. Sci. 2015, 27, 1655–1658. [Google Scholar] [CrossRef] [PubMed]
- Sutbeyaz, S.T.; Koseoglu, F.; Inan, L.; Coskun, O. Respiratory muscle training improves cardiopulmonary function and exercise tolerance in subjects with subacute stroke: A randomized controlled trial. Clin. Rehabil. 2010, 24, 240–250. [Google Scholar] [CrossRef] [PubMed]
- Tovar-Alcaraz, A.; de Oliveira-Sousa, S.L.; Leon-Garzon, M.C.; Gonzalez-Carrillo, M.J. Effects of inspiratory muscle training on respiratory function and balance in stroke survivors: A randomized controlled trial. Rev. Neurol. 2021, 72, 112–120. [Google Scholar] [CrossRef] [PubMed]
- Vaz, L.d.O.; Almeida, J.d.C.; Froes, K.S.d.S.O.; Dias, C.; Pinto, E.B.; Oliveira-Filho, J. Effects of inspiratory muscle training on walking capacity of individuals after stroke: A double-blind randomized trial. Clin. Rehabil. 2021, 35, 1247–1256. [Google Scholar] [CrossRef] [PubMed]
- Yoo, H.-J.; Pyun, S.-B. Efficacy of Bedside Respiratory Muscle Training in Patients With Stroke: A Randomized Controlled Trial. Am. J. Phys. Med. Rehabil. 2018, 97, 691–697. [Google Scholar] [CrossRef]
- Zheng, Y.; Zhang, Y.; Li, H.; Qiao, L.; Fu, W.; Yu, L.; Li, G.; Yang, J.; Ni, W.; Yong, Z.; et al. Comparative Effect of Liuzijue Qigong and Conventional Respiratory Training on Trunk Control Ability and Respiratory Muscle Function in Patients at an Early Recovery Stage From Stroke: A Randomized Controlled Trial. Arch. Phys. Med. Rehabil. 2021, 102, 423–430. [Google Scholar] [CrossRef]
- Mozaffarian, D.; Benjamin, E.J.; Go, A.S.; Arnett, D.K.; Blaha, M.J.; Cushman, M.; de Ferranti, S.; Després, J.-P.; Fullerton, H.J.; Howard, V.J.; et al. Heart disease and stroke statistics—2015 update: A report from the American Heart Association. Circulation 2015, 131, e29–e322. [Google Scholar] [CrossRef]
- Canning, C.G.; Ada, L.; Adams, R.; O’Dwyer, N.J. Loss of strength contributes more to physical disability after stroke than loss of dexterity. Clin. Rehabil. 2004, 18, 300–308. [Google Scholar] [CrossRef]
- Lanini, B.; Bianchi, R.; Romagnoli, I.; Coli, C.; Binazzi, B.; Gigliotti, F.; Pizzi, A.; Grippo, A.; Scano, G. Chest wall kinematics in patients with hemiplegia. Am. J. Respir. Crit. Care Med. 2003, 168, 109–113. [Google Scholar] [CrossRef] [PubMed]
- Lanini, B.; Gigliotti, F.; Coli, C.; Bianchi, R.; Pizzi, A.; Romagnoli, I.; Grazzini, M.; Stendardi, L.; Scano, G. Dissociation between respiratory effort and dyspnoea in a subset of patients with stroke. Clin. Sci. 2002, 103, 467–473. [Google Scholar] [CrossRef] [PubMed]
- Cohen, E.; Mier, A.; Heywood, P.; Murphy, K.; Boultbee, J.; Guz, A. Diaphragmatic movement in hemiplegic patients measured by ultrasonography. Thorax 1994, 49, 890–895. [Google Scholar] [CrossRef] [PubMed]
- Martino, R.; Foley, N.; Bhogal, S.; Diamant, N.; Speechley, M.; Teasell, R. Dysphagia after stroke: Incidence, diagnosis, and pulmonary complications. Stroke 2005, 36, 2756–2763. [Google Scholar] [CrossRef] [PubMed]
- Ramsburg, H.; Moriarty, H.J.; MacKenzie Greenle, M. End-of-Life Symptoms in Adult Patients With Stroke in the Last Two Years of Life: An Integrative Review. Am. J. Hosp. Palliat. Care 2023. [Google Scholar] [CrossRef]
- Narain, S.; Puckree, T. Pulmonary function in hemiplegia. Int. J. Rehabil. Res. 2002, 25, 57–59. [Google Scholar] [CrossRef]
- Stanojevic, S.; Kaminsky, D.A.; Miller, M.R.; Thompson, B.; Aliverti, A.; Barjaktarevic, I.; Cooper, B.G.; Culver, B.; Derom, E.; Hall, G.L.; et al. ERS/ATS technical standard on interpretive strategies for routine lung function tests. Eur. Respir. J. 2022, 60, 2101499. [Google Scholar] [CrossRef]
- Pai, H.-C.; Li, C.-C. Relationship Between Trunk Control Ability and Respiratory Function in Stroke Patients: A Scoping Review and Meta-Analysis. Asian Nurs. Res. (Korean Soc. Nurs. Sci.) 2023, 17, 61–69. [Google Scholar] [CrossRef]
- Young, R.P.; Hopkins, R.; Eaton, T.E. Forced expiratory volume in one second: Not just a lung function test but a marker of premature death from all causes. Eur. Respir. J. 2007, 30, 616–622. [Google Scholar] [CrossRef]
- Kulbacka-Ortiz, K.; Triest, F.J.J.; Franssen, F.M.E.; Wouters, E.F.M.; Studnicka, M.; Vollmer, W.M.; Lamprecht, B.; Burney, P.G.J.; Amaral, A.F.S.; Vanfleteren, L.E.G.W. Restricted spirometry and cardiometabolic comorbidities: Results from the international population based BOLD study. Respir. Res. 2022, 23, 34. [Google Scholar] [CrossRef]
- Silvestre, O.M.; Nadruz, W., Jr.; Querejeta Roca, G.; Claggett, B.; Solomon, S.D.; Mirabelli, M.C.; London, S.J.; Loehr, L.R.; Shah, A.M. Declining Lung Function and Cardiovascular Risk: The ARIC Study. J. Am. Coll. Cardiol. 2018, 72, 1109–1122. [Google Scholar] [CrossRef] [PubMed]
- Corlateanu, A.; Covantev, S.; Mathioudakis, A.G.; Botnaru, V.; Cazzola, M.; Siafakas, N. Chronic Obstructive Pulmonary Disease and Stroke. COPD 2018, 15, 405–413. [Google Scholar] [CrossRef] [PubMed]
- Szylińska, A.; Kotfis, K.; Bott-Olejnik, M.; Wańkowicz, P.; Rotter, I. Post-Stroke Outcomes of Patients with Chronic Obstructive Pulmonary Disease. Brain Sci. 2022, 12, 106. [Google Scholar] [CrossRef] [PubMed]
- Pozuelo-Carrascosa, D.P.; Carmona-Torres, J.M.; Laredo-Aguilera, J.A.; Latorre-Román, P.; Párraga-Montilla, J.A.; Cobo-Cuenca, A.I. Effectiveness of Respiratory Muscle Training for Pulmonary Function and Walking Ability in Patients with Stroke: A Systematic Review with Meta-Analysis. Int. J. Environ. Res. Public Health 2020, 17, 5356. [Google Scholar] [CrossRef]
- Menezes, K.K.; Nascimento, L.R.; Ada, L.; Polese, J.C.; Avelino, P.R.; Teixeira-Salmela, L.F. Respiratory muscle training increases respiratory muscle strength and reduces respiratory complications after stroke: A systematic review. J. Physiother. 2016, 62, 138–144. [Google Scholar] [CrossRef]
- Menezes, K.K.; Nascimento, L.R.; Avelino, P.R.; Alvarenga, M.T.M.; Teixeira-Salmela, L.F. Efficacy of Interventions to Improve Respiratory Function After Stroke. Respir. Care 2018, 63, 920–933. [Google Scholar] [CrossRef]
Inclusion Criteria | Exclusion Criteria |
---|---|
Abstracts written in English language Patients with stroke Adult patient population PFTs performed post-stroke as baseline or RCTs after implementation of a respiratory muscle training program | Reviews, meta-analyses, editorials, case reports, Articles in pediatric population Articles in special populations (e.g., pregnancy) Articles with outcomes related exclusively to exercise testing PFTs performed in the setting of rehabilitation but not including a respiratory muscle training program |
Disclaimer/Publisher’s Note: The statements, opinions and data contained in all publications are solely those of the individual author(s) and contributor(s) and not of MDPI and/or the editor(s). MDPI and/or the editor(s) disclaim responsibility for any injury to people or property resulting from any ideas, methods, instructions or products referred to in the content. |
© 2024 by the authors. Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (https://creativecommons.org/licenses/by/4.0/).
Share and Cite
Drakopanagiotakis, F.; Bonelis, K.; Steiropoulos, P.; Tsiptsios, D.; Sousanidou, A.; Christidi, F.; Gkantzios, A.; Serdari, A.; Voutidou, S.; Takou, C.-M.; et al. Pulmonary Function Tests Post-Stroke. Correlation between Lung Function, Severity of Stroke, and Improvement after Respiratory Muscle Training. Neurol. Int. 2024, 16, 139-161. https://doi.org/10.3390/neurolint16010009
Drakopanagiotakis F, Bonelis K, Steiropoulos P, Tsiptsios D, Sousanidou A, Christidi F, Gkantzios A, Serdari A, Voutidou S, Takou C-M, et al. Pulmonary Function Tests Post-Stroke. Correlation between Lung Function, Severity of Stroke, and Improvement after Respiratory Muscle Training. Neurology International. 2024; 16(1):139-161. https://doi.org/10.3390/neurolint16010009
Chicago/Turabian StyleDrakopanagiotakis, Fotios, Konstantinos Bonelis, Paschalis Steiropoulos, Dimitrios Tsiptsios, Anastasia Sousanidou, Foteini Christidi, Aimilios Gkantzios, Aspasia Serdari, Styliani Voutidou, Chrysoula-Maria Takou, and et al. 2024. "Pulmonary Function Tests Post-Stroke. Correlation between Lung Function, Severity of Stroke, and Improvement after Respiratory Muscle Training" Neurology International 16, no. 1: 139-161. https://doi.org/10.3390/neurolint16010009
APA StyleDrakopanagiotakis, F., Bonelis, K., Steiropoulos, P., Tsiptsios, D., Sousanidou, A., Christidi, F., Gkantzios, A., Serdari, A., Voutidou, S., Takou, C. -M., Kokkotis, C., Aggelousis, N., & Vadikolias, K. (2024). Pulmonary Function Tests Post-Stroke. Correlation between Lung Function, Severity of Stroke, and Improvement after Respiratory Muscle Training. Neurology International, 16(1), 139-161. https://doi.org/10.3390/neurolint16010009