Inspiratory Muscle Training on Glucose Control in Diabetes: A Randomized Clinical Trial

in International Journal of Sport Nutrition and Exercise Metabolism
View More View Less
  • 1 Universidade Federal do Rio Grande do Sul
  • 2 Hospital de Clínicas de Porto Alegre
  • 3 Faculdades Integradas de Taquara
  • 4 National Institute of Science and Technology for Health Technology Assessment (IATS)—CNPq/Brazil
Restricted access

Purchase article

USD  $24.95

Student 1 year online subscription

USD  $88.00

1 year online subscription

USD  $118.00

Student 2 year online subscription

USD  $168.00

2 year online subscription

USD  $224.00

This study evaluated the effects of inspiratory muscle training (IMT) in glucose control and respiratory muscle function in patients with diabetes. It was a randomized clinical trial conducted at the Physiopathology Laboratory of the Hospital de Clínicas de Porto Alegre. Patients with Type 2 diabetes were randomly assigned to IMT or placebo-IMT (P-IMT), performed at 30% and 2% of maximal inspiratory pressure, respectively, every day for 12 weeks. The main outcome measures were HbA1c, glycemia, and respiratory muscle function. Thirty patients were included: 73.3% women, 59.6 ± 10.7 years old, HbA1c 8.7 ± 0.9% (71.6 ± 9.8 mmol/mol), and glycemia 181.8 ± 57.8 mg/dl (10.5 ± 3.2 mmol/L). At the end of the training, HbA1c was 8.2 ±0.3% (66.1 ± 3.3 mmol/mol) and 8.7 ± 0.3% (71.6 ± 3.3 mmol/mol) for the IMT and P-IMT groups, respectively (p = .8). Fasting glycemia decreased in both groups with no difference after training although it was lower in IMT at 8 weeks: 170.0 ± 11.4 mg/dl(9.4 ± 0.6 mmol/L) and 184.4 ± 15.0 mg/dl (10.2 ± 0.8 mmol/L) for IMT and P-IMT, respectively (p < .05). Respiratory endurance time improved in the IMT group (baseline = 325.9 ± 51.1 s and 305.0 ± 37.8 s; after 12 weeks = 441.1 ± 61.7 s and 250.7 ± 39.0 s for the IMT and P-IMT groups, respectively; p < .05). Considering that glucose control did not improve, IMT should not be used as an alternative to other types of exercise in diabetes. Higher exercise intensities or longer training periods might produce better results. The clinical trials identifier is NCT 03191435.

Pinto and Schaan are with the Cardiology Program, Universidade Federal do Rio Grande do Sul, Porto Alegre, Brazil. Pinto, Bock, Schein, Portes, Monteiro, and Schaan are with the Exercise Pathophysiology Research Laboratory, Hospital de Clínicas de Porto Alegre, Porto Alegre, Brazil. Bock is with the Faculdades Integradas de Taquara, Taquara, Rio Grande do Sul, Brazil. Bock and Schaan are with the National Institute of Science and Technology for Health Technology Assessment (IATS)—CNPq/Brazil, Hospital de Clínicas de Porto Alegre, Porto Alegre, Brazil. Schaan is also with the Department of Internal Medicine, Universidade Federal do Rio Grande do Sul, Porto Alegre, Brazil.

Pinto (maribpinto@yahoo.com.br) is corresponding author.
  • Ahmad, A.M., Abdelsalam, H.M., & Lotfy, A.O. (2017). Effect of inspiratory muscle training on blood glucose levels and serum lipids in female patients with type 2 diabetes. International Journal of ChemTech Research, 10(4), 703709.

    • Search Google Scholar
    • Export Citation
  • Ahmad, A.M., Heba, A.M., & Hala, A.M. (2018). Effect of inspiratory muscle training on health-related quality of life in patients with type 2 diabetes. International Journal of Diabetes Research, 1(1), 813. doi:10.17554/j.issn.2414-2409.2018.01.6

    • Search Google Scholar
    • Export Citation
  • American Thoracic Society and European Respiratory Society. (2002). Statement on respiratory muscle testing. American Journal of Respiratory and Critical Care Medicine, 166, 518624. PubMed ID: 12186831 doi:10.1164/rccm.166.4.518

    • Search Google Scholar
    • Export Citation
  • Awotidebe, T.O., Adedoyin, R.A., Oke, K.I., Ativie, R.N., Opiyo, R., Ikujeyisi, E.O., … Afolabi, M.A. (2017). Relationship between functional capacity and health-related quality of life of patients with type-2 diabetes. Diabetes & Metabolic Syndrome: Clinical Research & Reviews, 11(1), 15. PubMed ID: 27389077 doi:10.1016/j.dsx.2016.06.004

    • Crossref
    • Search Google Scholar
    • Export Citation
  • Bhandari, A., Xia, Y., Cortright, R., Dohm, G.L., & Bazzy, A.R. (2000). Effect of respiratory muscle training on GLUT-4 in the sheep diaphragm. Medicine & Science in Sports & Exercise, 32(8), 14061411. PubMed ID: 10949006 doi:10.1097/00005768-200008000-00008

    • Crossref
    • Search Google Scholar
    • Export Citation
  • Bolton, C.F, Grand’Maison, F., Parkes, A., & Shkrum, M. (1992). Needle electromyography of the diaphragm. Muscle & Nerve, 15(6), 678681. PubMed ID: 1508232 doi:10.1002/mus.880150608

    • Crossref
    • Search Google Scholar
    • Export Citation
  • Boniol, M., Dragomir, M., Autier, P., & Boyle, P. (2017). Physical activity and change in fasting glucose and HbA1c: A quantitative meta-analysis of randomized trials. Acta Diabetologica 54(11), 983991. PubMed ID: 28840356 doi:10.1007/s00592-017-1037-3

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • Bruells, C.S., Maes, K., Rossaint, R., Thomas, D., Cielen, N., Bleilevens, C., … Weis, J. (2013). Prolonged mechanical ventilation alters the expression pattern of angio-neogenetic factors in a pre-clinical rat model. PLoS One, 8(8), e70524. PubMed ID: 23950950 doi:10.1371/journal.pone.0070524

    • Crossref
    • Search Google Scholar
    • Export Citation
  • Cho, N.H., Shaw, J.E., Karuranga, S., Huang, Y., da Rocha Fernandes, J.D., Ohlrogge, A.W., & Malanda, B. (2018). IDF Diabetes Atlas: Global estimates of diabetes prevalence for 2017 and projections for 2045. Diabetes Research and Clinical Practice, 138, 271281. PubMed ID: 29496507 doi:10.1016/j.diabres.2018.02.023

    • Crossref
    • Search Google Scholar
    • Export Citation
  • Coppola, A., Sasso, L., Bagnasco, A., Giustina, A., & Gazzaruso, C. (2016). The role of patient education in the prevention and management of type 2 diabetes: An overview. Endocrine, 53(1), 1827. PubMed ID: 26494579 doi:10.1007/s12020-015-0775-7

    • Crossref
    • Search Google Scholar
    • Export Citation
  • Corrêa, A.P., Antunes, C.F., Figueira, F.R., de Castro, M.A., Ribeiro, J.P., & Schaan, B.D. (2015a) Effect of acute inspiratory muscle exercise on blood flow of resting and exercising limbs and glucose levels in type 2 diabetes. PLoS One, 10(3), e0121384. PubMed ID: 25803283 doi:10.1371/journal.pone.0121384

    • Crossref
    • Search Google Scholar
    • Export Citation
  • Corrêa, A.P., Figueira, F.R., Umpierre, D., Casali, K.R., & Schaan, B.D. (2015b). Inspiratory muscle loading: A new approach for lowering glucose levels and glucose variability in patients with Type 2 diabetes. Diabetic Medicine, 32(9), 12551257. PubMed ID: 25970646 doi:10.1111/dme.12798

    • Crossref
    • Search Google Scholar
    • Export Citation
  • Corrêa, A.P., Ribeiro, J.P., Balzan, F.M., Mundstock, L., Ferlin, E.L., & Moraes, R.S. (2011). Inspiratory muscle training in type 2 diabetes with inspiratory muscle weakness. Medicine & Science in Sports & Exercise, 43(7), 11351141. PubMed ID: 21200342 doi:10.1249/MSS.0b013e31820a7c12

    • Crossref
    • Search Google Scholar
    • Export Citation
  • Davis, W.A., Knuiman, M, Kendall, P., Grange, V., Davis, T.M.E., & Fremantle Diabetes Study.(2004). Glycemic exposure is associated with reduced pulmonary function in type 2 diabetes: The Fremantle Diabetes Study. Diabetes Care. 27(3), 752757. PubMed ID: 14988297 doi:10.2337/diacare.27.3.752

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • Dos Santos Silva, M., Ramos, L.R., Tufik, S., Togeiro, S.M., & Lopes, G.S. (2015). Influence of inspiratory muscle training on Changes in Fasting Hyperglycemia in the Older Adult: The Epidoso Project. Journal of Diabetes Science and Technology, 9(6), 13521353. PubMed ID: 26251371 doi:10.1177/1932296815599006

    • Crossref
    • Search Google Scholar
    • Export Citation
  • Ewing, D.J., Martyn, C.N., Young, R.J., & Clarke, B.F. (1985). The value of cardiovascular autonomic function tests: 10 years experience in diabetes. Diabetes Care, 8(5), 491498. PubMed ID: 4053936 doi:10.2337/diacare.8.5.491

    • Crossref
    • Search Google Scholar
    • Export Citation
  • Folse, H.J., Mukherjee, J., Sheehan, J.J., Ward, A.J., Pelkey, R.L., Dinh, T.A., … Kim, J. (2017). Delays in treatment intensification with oral antidiabetic drugs and risk of microvascular and macrovascular events in patients with poor glycaemic control: An individual patient simulation study. Diabetes, Obesity & Metabolism, 19(7), 10061013. PubMed ID: 28211604 doi:10.1111/dom.12913

    • Crossref
    • Search Google Scholar
    • Export Citation
  • Hameed, U.A., Manzar, D., Raza, S., Shareef, M.Y., & Hussain, M.E. (2012). Resistance training leads to clinically meaningful improvements in control of glycemia and muscular strength in untrained middle-aged patients with type 2 diabetes mellitus. North American Journal of Medical Sciences, 4(8), 336343. PubMed ID: 22912941 doi:10.4103/1947-2714.99507

    • Crossref
    • Search Google Scholar
    • Export Citation
  • Inzucchi, S.E., Bergenstal, R.M., Buse, J.B., Diamant, M., Ferrannini, E., Nauck, M., … Matthews D.R. (2015). Management of hyperglycemia in type 2 diabetes, 2015: A patient-centered approach: Update to a position statement of the American Diabetes Association and the European Association for the Study of Diabetes. Diabetes Care, 38(1), 140149. PubMed ID: 25538310 doi:10.2337/dc14-2441

    • Crossref
    • Search Google Scholar
    • Export Citation
  • Kalyani, R.R., Saudek, C.D., Brancati, F.L., & Selvin, E. (2010). Association of diabetes, comorbidities, and A1C with functional disability in older adults: Results from the National Health and Nutrition Examination Survey (NHANES), 1999–2006. Diabetes Care, 33(5), 10551060. PubMed ID: 20185736 doi:10.2337/dc09-1597

    • Crossref
    • Search Google Scholar
    • Export Citation
  • Kaminski, D.M., Schaan, B.D., da Silva, A.M., Soares, P.P., & Dall’Ago, P. (2011). Inspiratory muscle weakness is associated with autonomic cardiovascular dysfunction in patients with type 2 diabetes mellitus. Clinical Autonomic Research, 21, 2935. PubMed ID: 21052769 doi:10.1007/s10286-010-0087-1

    • Crossref
    • Search Google Scholar
    • Export Citation
  • Kaminski, D.M., Schaan, B.D., da Silva, A.M., Soares, P.P., & Dall’Ago, P.D. (2015). Inspiratory muscle training in patients with diabetic autonomic neuropathy: A randomized clinical trial. Clinical Autonomic Research, 25(4), 263266. PubMed ID: 25982993 doi:10.1007/s10286-015-0291-0

    • Crossref
    • Search Google Scholar
    • Export Citation
  • Klein, O.L., Krishnan, J.A., Glick, S., & Smith, L.J. (2010). Systematic review of the association between lung function and Type 2 diabetes mellitus. Diabetic Medicine, 27(9), 977987. 20722670 doi:10.1111/j.1464-5491.2010.03073.x

    • Crossref
    • Search Google Scholar
    • Export Citation
  • Lee, J., Kim, D., & Kim, C. (2017). Resistance training for glycemic control, muscular strength, and lean body mass in old type 2 diabetic patients: A meta-analysis. Diabetes Therapy, 8(3), 459573. PubMed ID: 28382531 doi:10.1007/s13300-017-0258-3

    • Crossref
    • Search Google Scholar
    • Export Citation
  • Mavros, Y., Kay, S., Anderberg, K.A., Baker, M.K., Wang, Y., Zhao, R., … Singh, M.A.F. (2013). Changes in insulin resistance and HbA1c are related to exercise-mediated changes in body composition in older adults with type 2 diabetes: Interim outcomes from the GREAT2DO trial. Diabetes Care, 36(8), 23722379. PubMed ID: 23474589 doi:10.2337/dc12-2196

    • Crossref
    • Search Google Scholar
    • Export Citation
  • Meznaric, M., & Cvetko, E. (2016). Size and proportions of slow-twitch and fast-twitch muscle fibers in human costal diaphragm. Biomed Research International, 5946520. PubMed ID: 27891518 doi:10.1155/2016/5946520

    • Search Google Scholar
    • Export Citation
  • Neder, J.A., Andreoni, S., Lerario, M.C., & Nery, L.E. (1999). Reference values for lung function tests. II. Maximal respiratory pressures and voluntary ventilation. Brazilian Journal of Medical and Biological Research, 32(6), 719727. PubMed ID: 10412550 doi:10.1590/s0100-879x1999000600007

    • Crossref
    • Search Google Scholar
    • Export Citation
  • Neumann, C., & Schmid, H. (1997). Standardization of a computerized method for calculating autonomic function test responses in healthy subjects and patients with diabetes mellitus. Brazilian Journal of Medical and Biological Research, 30(2), 197205. PubMed ID: 9239305 doi:10.1590/s0100-879x1997000200007

    • Crossref
    • Search Google Scholar
    • Export Citation
  • O’Gorman, D.J., Karlsson, H.K., McQuaid, S., Yousif, O., Rahman, Y., Gasparro, D., … Nolan, J.J. (2006). Exercise training increases insulin-stimulated glucose disposal and GLUT4 (SLC2A4) protein content in patients with type 2 diabetes. Diabetologia, 49(12), 298392. PubMed ID: 17019595 doi:10.1007/s00125-006-0457-3

    • Crossref
    • Search Google Scholar
    • Export Citation
  • Podnar, S., & Resman-Gaspersic, A. (2008). Quantitative motor unit potential analysis in the diaphragm: A normative study. Muscle Nerve, 37(4), 518521. PubMed ID: 18067138 doi:10.1002/mus.20939

    • Crossref
    • Search Google Scholar
    • Export Citation
  • Richter, E.A., & Hargreaves, M. (2013). Exercise, GLUT4, and skeletal muscle glucose uptake. Physiological reviews, 93(3), 9931017. PubMed ID: 23899560 doi:10.1152/physrev.00038.2012

    • Crossref
    • Search Google Scholar
    • Export Citation
  • Sadek, Z., Salami, A., Joumaa, W.H., Awada, C., Ahmaidi, S., & Ramadan, W. (2018). Best mode of inspiratory muscle training in heart failure patients: A systematic review and meta-analysis. European Journal of Preventive Cardiology, 25(16), 16911701. PubMed ID: 30073849 doi:10.1177/2047487318792315

    • Crossref
    • Search Google Scholar
    • Export Citation
  • Schulz, K.F., Altman, D.G., & Moher, D. (2010). CONSORT 2010 statement: Updated guidelines for reporting parallel group randomised trials. British Medical Journal, 340, c332. PubMed ID: 20332509 doi:10.1136/bmj.c332

    • Crossref
    • Search Google Scholar
    • Export Citation
  • Shah, S.H., Sonawane, P., Nahar, P., Vaidya, S., Salvi, S. (2013). Pulmonary function tests in type 2 diabetes mellitus and their association with glycemic control and duration of the disease. Lung India, 30(2), 108112, PubMed ID: 23741090 doi:10.4103/0970-2113.110417

    • Crossref
    • Search Google Scholar
    • Export Citation
  • Sigal, R.J., Kenny, G.P., Boulé, N.G., Wells, G.A., Prud’homme, D., Fortier, M., & Jaffey, J. (2007). Effects of aerobic training, resistance training, or both on glycemic control in type 2 diabetes: A randomized trial. Annals of Internal Medicine 147(6), 357369. PubMed ID: 17876019 doi:10.7326/0003-4819-147-6-200709180-00005

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • Silva, M.S., Martins, A.C., Cipriano, G., Ramos, L.R., & Lopes, G.S. (2012). Inspiratory training increases insulin sensitivity in elderly patients. Geriatrics & Gerontology International. 12(2), 345351. PubMed ID: 21973074 doi:10.1111/j.1447-0594.2011.00755.x

    • Crossref
    • Search Google Scholar
    • Export Citation
  • Thomas, N., Alder, E., & Leese, G.P. (2004). Barriers to physical activity in patients with diabetes, Postgraduate Medical Journal. 80(943), 287291. PubMed ID: 15138320 doi:10.1136/pgmj.2003.010553

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • Umpierre, D., Ribeiro, P.A., Kramer, C.K., Leitão, C.B., Zucatti, A.T.N., Azevedo, M.J., … Schaan, B.D. (2011). Physical activity advice only or structured exercise training and association with HbA1c levels in type 2 diabetes: A systematic review and meta-analysis. Journal of the American Medical Association, 305(17), 17901799. PubMed ID: 21540423 doi:10.1001/jama.2011.576

    • Crossref
    • Search Google Scholar
    • Export Citation
  • Umpierre, D., Ribeiro, P.A., Schaan, B.D., & Ribeiro, J.P. (2013). Volume of supervised exercise training impacts glycaemic control in patients with type 2 diabetes: A systematic review with meta-regression analysis. Diabetologia, 56(2), 242251. PubMed ID: 23160642 doi:10.1007/s00125-012-2774-z

    • Crossref
    • Search Google Scholar
    • Export Citation
  • Yeh, H.C., Punjabi, N.M., Wang, N.Y., Pankow, J.S, Duncan, B.B., & Brancati, F.L. (2008). Cross-sectional and prospective study of lung function in adults with type 2 diabetes: The Atherosclerosis Risk in Communities (ARIC) study. Diabetes Care. 31(4),741746 PubMed ID: 18056886 doi:10.2337/dc07-1464

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • Zelmanovitz, T., Gross, J.L., Oliveira, J.R., Paggi, A., Tatsch, M., & Azevedo, M.J. (1997). The receiver operating characteristics curve in the evaluation of a random urine specimen as a screening test for diabetic nephropathy. Diabetes Care, 20(4), 516519. PubMed ID: 9096972 doi:10.2337/diacare.20.4.516

    • Crossref
    • Search Google Scholar
    • Export Citation
  • Zoungas, S., Arima, H., Gerstein, H.C., Holman, R.R., Woodward, M., Reaven, P., … Collaborators on Trials of Lowering Glucose (CONTROL) Group. (2017). Effects of intensive glucose control on microvascular outcomes in patients with type 2 diabetes: A meta-analysis of individual participant data from randomised controlled trials. Lancet Diabetes and Endocrinology, 5(6), 431437. PubMed ID: 28365411 doi:10.1016/S2213-8587(17)30104-3

    • Crossref
    • Search Google Scholar
    • Export Citation
All Time Past Year Past 30 Days
Abstract Views 438 438 252
Full Text Views 25 25 11
PDF Downloads 13 13 5