{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,10,19]],"date-time":"2026-10-19T07:46:29Z","timestamp":1792395989656,"version":"4.4.0"},"reference-count":49,"publisher":"MDPI AG","issue":"6","license":[{"start":{"date-parts":[[2023,12,1]],"date-time":"2023-12-01T00:00:00Z","timestamp":1701388800000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":["ARM"],"abstract":"<jats:p>This study aimed to investigate the relationship between pulmonary function and cardiac autonomic function parameters in clinically stable myasthenia gravis (MG) patients. A total of 22 MG patients and 22 healthy controls (HCs) were evaluated. Pulmonary function test parameters, heart rate variability (HRV), baroreflex sensitivity (BRS), and cardiovascular autonomic function test parameters (the Valsalva ratio, expiration\/inspiration (E\/I) ratio) were assessed. Compared with the HCs, the patients demonstrated a similar diffusion capacity for carbon monoxide (DLCO); a lower forced vital capacity (FVC%pred); a lower forced expiratory volume in 1 s (FEV1%pred); lower BRS and HRV, including high-frequency and total power spectral density; and a higher percentage of abnormal cardiovagal function test results (p &lt; 0.05). A lower BRS in the patient group was associated with worse clinical disease outcomes and reduced pulmonary function (DLCO%pred, R = 0.59; TLC%pred, R = 0.48). Age, forced vital capacity, and total lung capacity predicted the E\/I ratio (R2 values ranging from 0.48 to 0.49). Our study demonstrated a significant relationship between a reduced pulmonary ventilation function and respiratory mechanics with cardiovascular autonomic parameters, including the E\/I ratio, BRS, and HRV measures at rest, as shown in the MG group. Future studies should focus on the interplay between respiratory and autonomic function testing, as well as pulmonary rehabilitation, to mitigate cardiovascular risk in these patients.<\/jats:p>","DOI":"10.3390\/arm91060040","type":"journal-article","created":{"date-parts":[[2023,12,1]],"date-time":"2023-12-01T08:36:59Z","timestamp":1701419819000},"page":"546-559","update-policy":"https:\/\/doi.org\/10.3390\/mdpi_crossmark_policy","source":"Crossref","is-referenced-by-count":4,"title":["Correlation between Cardiovascular Autonomic and Pulmonary Ventilation Functions in Myasthenia Gravis Patients"],"prefix":"10.3390","volume":"91","author":[{"ORCID":"https:\/\/orcid.org\/0000-0003-3861-7113","authenticated-orcid":false,"given":"Monika","family":"Zawadka-Kunikowska","sequence":"first","affiliation":[{"name":"Department of Human Physiology, Nicolaus Copernicus University in Torun, Ludwik Rydygier Collegium Medicum in Bydgoszcz, Kar\u0142owicza 24, 85-092 Bydgoszcz, Poland"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0003-2995-6148","authenticated-orcid":false,"given":"\u0141ukasz","family":"Rzepi\u0144ski","sequence":"additional","affiliation":[{"name":"Sanitas\u2014Neurology Outpatient Clinic, Dworcowa 110, 85-010 Bydgoszcz, Poland"},{"name":"Department of Neurology, 10th Military Research Hospital and Polyclinic, 85-681 Bydgoszcz, Poland"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-0407-2592","authenticated-orcid":false,"given":"Miros\u0142awa","family":"Cie\u015blicka","sequence":"additional","affiliation":[{"name":"Department of Human Physiology, Nicolaus Copernicus University in Torun, Ludwik Rydygier Collegium Medicum in Bydgoszcz, Kar\u0142owicza 24, 85-092 Bydgoszcz, Poland"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Joanna","family":"Fanslau","sequence":"additional","affiliation":[{"name":"Department of Human Physiology, Nicolaus Copernicus University in Torun, Ludwik Rydygier Collegium Medicum in Bydgoszcz, Kar\u0142owicza 24, 85-092 Bydgoszcz, Poland"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Jacek J.","family":"Klawe","sequence":"additional","affiliation":[{"name":"Department of Hygiene, Epidemiology, Ergonomy and Postgraduate Education, Nicolaus Copernicus University in Torun, Ludwik Rydygier Collegium Medicum in Bydgoszcz, M. Sklodowskiej-Curie 9, 85-094 Bydgoszcz, Poland"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Ma\u0142gorzata","family":"Tafil-Klawe","sequence":"additional","affiliation":[{"name":"Department of Human Physiology, Nicolaus Copernicus University in Torun, Ludwik Rydygier Collegium Medicum in Bydgoszcz, Kar\u0142owicza 24, 85-092 Bydgoszcz, Poland"}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"1968","published-online":{"date-parts":[[2023,12,1]]},"reference":[{"key":"ref_1","doi-asserted-by":"crossref","first-page":"30","DOI":"10.1038\/s41572-019-0079-y","article-title":"Myasthenia gravis","volume":"5","author":"Gilhus","year":"2019","journal-title":"Nat. Rev. Dis. Prim."},{"key":"ref_2","doi-asserted-by":"crossref","unstructured":"Di Stefano, V., Tubiolo, C., Gagliardo, A., Presti, R.L., Montana, M., Todisco, M., Lupica, A., Caimi, G., Tassorelli, C., and Fierro, B. (2022). Metalloproteinases and Tissue Inhibitors in Generalized Myasthenia Gravis. A Preliminary Study. Brain Sci., 12.","DOI":"10.3390\/brainsci12111439"},{"key":"ref_3","doi-asserted-by":"crossref","first-page":"3329","DOI":"10.1007\/s00415-023-11733-y","article-title":"Myasthenia gravis, respiratory function, and respiratory tract disease","volume":"270","author":"Gilhus","year":"2023","journal-title":"J. Neurol."},{"key":"ref_4","doi-asserted-by":"crossref","first-page":"406","DOI":"10.3390\/neurolint14020033","article-title":"Impact of COVID-19 in AChR Myasthenia Gravis and the Safety of Vaccines: Data from an Italian Cohort","volume":"14","author":"Lupica","year":"2022","journal-title":"Neurol. Int."},{"key":"ref_5","doi-asserted-by":"crossref","first-page":"1130","DOI":"10.1183\/09031936.95.08071130","article-title":"Ventilatory muscle strength and endurance in myasthenia gravis","volume":"8","author":"Keenan","year":"1995","journal-title":"Eur. Respir. J."},{"key":"ref_6","doi-asserted-by":"crossref","first-page":"120","DOI":"10.1016\/j.nmd.2016.11.015","article-title":"Sleep, lung function, and quality of life in patients with myasthenia gravis: A cross-sectional study","volume":"27","author":"Oliveira","year":"2017","journal-title":"Neuromuscul. Disord."},{"key":"ref_7","doi-asserted-by":"crossref","first-page":"517","DOI":"10.1111\/1759-7714.14774","article-title":"Analysis of influencing factors of postoperative myasthenic crisis in 564 patients with myasthenia gravis in a single center","volume":"14","author":"Jiao","year":"2023","journal-title":"Thorac. Cancer"},{"key":"ref_8","doi-asserted-by":"crossref","first-page":"12","DOI":"10.1111\/j.1600-0404.2010.01369.x","article-title":"Airway limitation and exercise intolerance in well-regulated myasthenia gravis patients","volume":"122","author":"Elsais","year":"2010","journal-title":"Acta Neurol. Scand."},{"key":"ref_9","doi-asserted-by":"crossref","first-page":"95","DOI":"10.17712\/nsj.2019.2.20180024","article-title":"Expiratory muscle strength as a pre-dictor of functional exercise capacity in generalized myasthenia gravis","volume":"24","author":"Salci","year":"2019","journal-title":"Neurosciences"},{"key":"ref_10","doi-asserted-by":"crossref","first-page":"98","DOI":"10.1002\/acn3.51706","article-title":"The systemic inflammation markers as possible indices for predicting respiratory failure and outcome in patients with myasthenia gravis","volume":"10","author":"Huang","year":"2023","journal-title":"Ann. Clin. Transl. Neurol."},{"key":"ref_11","doi-asserted-by":"crossref","first-page":"504","DOI":"10.1186\/s13075-014-0504-2","article-title":"The sympathetic nervous response in inflammation","volume":"16","author":"Pongratz","year":"2014","journal-title":"Arthritis Res. Ther."},{"key":"ref_12","doi-asserted-by":"crossref","first-page":"3","DOI":"10.1016\/j.ijcme.2014.08.003","article-title":"Cardiac manifestations of myasthenia gravis: A systematic review","volume":"5","author":"Shivamurthy","year":"2014","journal-title":"IJC Metab. Endocr."},{"key":"ref_13","doi-asserted-by":"crossref","first-page":"193","DOI":"10.15420\/aer.2018.27.2","article-title":"Heart Rate Variability: An Old Metric with New Meaning in the Era of using mHealth Technologies for Health and Exercise Training Guidance. Part One: Physiology and Methods","volume":"7","author":"Singh","year":"2018","journal-title":"Arrhythm. Electrophysiol. Rev."},{"key":"ref_14","doi-asserted-by":"crossref","first-page":"51","DOI":"10.1161\/01.HYP.0000197613.47649.02","article-title":"Sympathetic neural outflow and chemoreflex sensitivity are related to spontaneous breathing rate in normal men","volume":"47","author":"Narkiewicz","year":"2006","journal-title":"Hypertension"},{"key":"ref_15","doi-asserted-by":"crossref","first-page":"262","DOI":"10.1161\/01.CIR.100.3.262","article-title":"Enhanced sympathetic and ventilatory responses to central chemoreflex activation in heart failure","volume":"100","author":"Narkiewicz","year":"1999","journal-title":"Circulation"},{"key":"ref_16","doi-asserted-by":"crossref","first-page":"2119","DOI":"10.1007\/s00415-014-7465-x","article-title":"The presence of dysautonomia in different subgroups of myasthenia gravis patients","volume":"261","year":"2014","journal-title":"J. Neurol."},{"key":"ref_17","doi-asserted-by":"crossref","unstructured":"Zawadka-Kunikowska, M., Rzepi\u0144ski, \u0141., Tafil-Klawe, M., Klawe, J.J., Zalewski, P., and S\u0142omko, J. (2022). Association of Cardiac Autonomic Responses with Clinical Outcomes of Myasthenia Gravis: Short-Term Analysis of the Heart-Rate and Blood Pressure Variability. J. Clin. Med., 11.","DOI":"10.3390\/jcm11133697"},{"key":"ref_18","doi-asserted-by":"crossref","first-page":"1777","DOI":"10.1007\/s00415-008-0049-x","article-title":"Left ventricular long-axis function in myasthenia gravis","volume":"255","author":"Owe","year":"2008","journal-title":"J. Neurol."},{"key":"ref_19","doi-asserted-by":"crossref","first-page":"102710","DOI":"10.1016\/j.autrev.2020.102710","article-title":"Efficacy of immunosuppressive therapy in myocarditis: A 30-year systematic review and meta analysis","volume":"20","author":"Cheng","year":"2021","journal-title":"Autoimmun. Rev."},{"key":"ref_20","doi-asserted-by":"crossref","first-page":"1140","DOI":"10.3390\/neurolint15030071","article-title":"Altered Cardiac Autonomic Regulation in Individuals with Myasthenia Gravis\u2014A Systematic Review and Meta-Analysis","volume":"15","author":"Veronese","year":"2023","journal-title":"Neurol. Int."},{"key":"ref_21","doi-asserted-by":"crossref","unstructured":"Ching, S.-M., Chia, Y.-C., Lentjes, M.A.H., Luben, R., Wareham, N., and Khaw, K.-T. (2019). FEV1 and total Cardiovascular mortality and morbidity over an 18 years follow-up Population-Based Prospective EPIC-NORFOLK Study. BMC Public Health, 19.","DOI":"10.1186\/s12889-019-6818-x"},{"key":"ref_22","doi-asserted-by":"crossref","first-page":"478","DOI":"10.1016\/S0140-6736(97)11144-8","article-title":"Baroreflex sensitivity and heart-rate variability in prediction of total cardiac mortality after myocardial infarction. ATRAMI (Autonomic Tone and Reflexes After Myocardial Infarction) Investigators","volume":"351","author":"Bigger","year":"1998","journal-title":"Lancet"},{"key":"ref_23","doi-asserted-by":"crossref","unstructured":"Tantucci, C., Bottone, D., Levi, G., Uccelli, S., Venturoli, N., Magri, R., Garrafa, E., and Pini, L. (2020). Respiratory function, autonomic dysfunction, and systemic inflammation are closely linked in patients with COPD and tidal flow limitation: An exploratory study. Respir. Physiol. Neurobiol., 284.","DOI":"10.1016\/j.resp.2020.103565"},{"key":"ref_24","doi-asserted-by":"crossref","first-page":"369","DOI":"10.1590\/S1807-59322010000400004","article-title":"Deep breathing heart rate variability is associated with respiratory muscle weakness in patients with chronic obstructive pulmonary disease","volume":"65","author":"Reis","year":"2010","journal-title":"Clinics"},{"key":"ref_25","doi-asserted-by":"crossref","first-page":"254","DOI":"10.1016\/j.ijcard.2017.06.047","article-title":"Integrated cardiovascular\/respiratory control in type 1 diabetes evidences functional imbalance: Possible role of hypoxia","volume":"244","author":"Bianchi","year":"2017","journal-title":"Int. J. Cardiol."},{"key":"ref_26","first-page":"31","article-title":"Association between respiratory mechanics and autonomic function in morbid obesity","volume":"20","author":"Junior","year":"2014","journal-title":"Rev. Port. Pneumol."},{"key":"ref_27","doi-asserted-by":"crossref","first-page":"805925","DOI":"10.3389\/fphys.2021.805925","article-title":"Alternation of the Autonomic Nervous System Is Associated With Pulmonary Sequelae in Patients With COVID-19 After Six Months of Discharge","volume":"12","author":"Bai","year":"2022","journal-title":"Front. Physiol."},{"key":"ref_28","doi-asserted-by":"crossref","unstructured":"Rzepi\u0144ski, \u0141., Zawadka-Kunikowska, M., Newton, J.L., and Zalewski, P. (2021). Cardiac Autonomic Dysfunction in Myasthenia Gravis and Re-lapsing-Remitting Multiple Sclerosis-A Pilot Study. J. Clin. Med., 10.","DOI":"10.3390\/jcm10102173"},{"key":"ref_29","doi-asserted-by":"crossref","first-page":"16","DOI":"10.1212\/WNL.55.1.16","article-title":"Myasthenia gravis: Recommendations for clinical research standards. Task force of the medical scientific advisory board of the myasthenia gravis foundation of America","volume":"55","author":"Jaretzki","year":"2000","journal-title":"Neurology"},{"key":"ref_30","doi-asserted-by":"crossref","first-page":"e70","DOI":"10.1164\/rccm.201908-1590ST","article-title":"Standardization of spirometry 2019 update. An official American thoracic society and European respiratory society technical statement","volume":"200","author":"Graham","year":"2019","journal-title":"Am. J. Respir. Crit. Care Med."},{"key":"ref_31","doi-asserted-by":"crossref","first-page":"948","DOI":"10.1183\/09031936.05.00035205","article-title":"Interpretative strategies for lung function tests","volume":"26","author":"Pellegrino","year":"2005","journal-title":"Eur. Respir. J."},{"key":"ref_32","doi-asserted-by":"crossref","first-page":"2101499","DOI":"10.1183\/13993003.01499-2021","article-title":"ERS\/ATS technical standard on interpretive strategies for routine lung function tests","volume":"60","author":"Stanojevic","year":"2021","journal-title":"Eur. Respir. J."},{"key":"ref_33","doi-asserted-by":"crossref","first-page":"666","DOI":"10.1016\/j.clinph.2020.11.024","article-title":"Electrodiagnostic assessment of the autonomic nervous system: A consensus statement endorsed by the American Autonomic Society, American Academy of Neurology, and the International Federation of Clinical Neurophysiology","volume":"132","author":"Cheshire","year":"2020","journal-title":"Clin. Neurophysiol."},{"key":"ref_34","unstructured":"Therapeutics and Technology Assessment Subcommittee of the American Academy of Neurology (1996). Assessment clinical auto-nomic testing report of the therapeutics and technology subcommittee of the American Academy of Neurology. Neurology, 46, 873\u2013880."},{"key":"ref_35","doi-asserted-by":"crossref","first-page":"64","DOI":"10.1109\/51.620497","article-title":"Continuous monitoring of the sympatho-vagal balance through spectral analysis","volume":"16","author":"Bianchi","year":"1997","journal-title":"IEEE Eng. Med. Biol. Mag."},{"key":"ref_36","unstructured":"Fortin, J., Klinger, T., Wagner, C., Sterner, H., Madritsch, C., Gr\u00fcllenberger, R., Hacker, A., Habenbacher, W., and Skrabal, F. (1998, January 1). The task force monitor\u2014A non-invasive beat-to beat monitor for hemodynamic and autonomic function of the human body. Proceedings of the 20th Annual International Conference of the IEEE Engineering in Medicine and Biology Society, Hong Kong, China."},{"key":"ref_37","unstructured":"(2020, August 21). NIST\/SEMATECH e-Handbook of Statistical Methods, Available online: http:\/\/www.itl.nist.gov\/div898\/handbook\/.2012\/01\/20."},{"key":"ref_38","first-page":"405","article-title":"Peak expiratory flow and the single-breath count test as markers of respiratory function in patients with myasthenia gravis","volume":"38","author":"Aguirre","year":"2020","journal-title":"Neurol. Engl. Ed."},{"key":"ref_39","doi-asserted-by":"crossref","first-page":"2769","DOI":"10.1161\/01.CIR.91.11.2769","article-title":"Reduced alveolar\u2013capillary membrane diffusing capacity in chronic heart failure. Its pathophysiological relevance and relationship to exercise performance","volume":"91","author":"Puri","year":"1995","journal-title":"Circulation"},{"key":"ref_40","doi-asserted-by":"crossref","first-page":"101473","DOI":"10.1016\/j.eclinm.2022.101473","article-title":"Risk factors for impaired pulmonary diffusion function in convalescent COVID-19 patients: A systematic review and meta-analysis","volume":"49","author":"Zhi","year":"2022","journal-title":"EClinicalMedicine"},{"key":"ref_41","doi-asserted-by":"crossref","first-page":"791410","DOI":"10.3389\/fmed.2021.791410","article-title":"Impaired Spontaneous Baroreceptor Reflex Sensitivity in Patients With COPD Compared to Healthy Controls: The Role of Lung Hyperinflation","volume":"8","author":"Mayr","year":"2022","journal-title":"Front. Med."},{"key":"ref_42","doi-asserted-by":"crossref","first-page":"H6","DOI":"10.1152\/ajpheart.00701.2017","article-title":"Cardiorespiratory interactions in humans and animals: Rhythms for life","volume":"315","author":"Elstad","year":"2018","journal-title":"Am. J. Physiol. Heart Circ. Physiol."},{"key":"ref_43","first-page":"P2183","article-title":"Correlation between heart rate variability and pulmonary function in adults","volume":"44","author":"Sperandio","year":"2014","journal-title":"Eur. Respir. J."},{"key":"ref_44","doi-asserted-by":"crossref","unstructured":"Bianchim, M., Sperandio, E., Martinh\u00e3o, G., Matheus, A., Lauria, V., da Silva, R., Spadari, R., Gagliardi, A., Arantes, R., and Romiti, M. (2016). Correlation between heart rate variability and pulmonary function adjusted by confounding factors in healthy adults. Braz. J. Med. Biol. Res., 49.","DOI":"10.1590\/1414-431X20154435"},{"key":"ref_45","doi-asserted-by":"crossref","first-page":"88","DOI":"10.1111\/j.1542-474X.2005.10101.x","article-title":"Heart rate variability: Measurement and clinical utility","volume":"10","author":"Kleiger","year":"2005","journal-title":"Ann. Noninvasive Electrocardiol."},{"key":"ref_46","first-page":"S114","article-title":"Impaired lung transfer factor in fibromyalgia syndrome","volume":"34","author":"Rizzi","year":"2016","journal-title":"Clin Exp Rheumatol."},{"key":"ref_47","doi-asserted-by":"crossref","first-page":"145","DOI":"10.1159\/000026376","article-title":"Autonomic innervation of human airways: Structure, function, and pathophysiology in asthma","volume":"6","author":"Hulsmann","year":"1999","journal-title":"Neuroimmunomodulation"},{"key":"ref_48","doi-asserted-by":"crossref","unstructured":"Zannin, E., Pellegrino, R., Di Toro, A., Antonelli, A., Dellac\u00e0, R.L., and Bernardi, L. (2015). Parasympathetic Stimuli on Bronchial and Cardiovascular Systems in Humans. PLoS ONE, 10.","DOI":"10.1371\/journal.pone.0127697"},{"key":"ref_49","doi-asserted-by":"crossref","first-page":"17141","DOI":"10.1038\/s41598-021-96505-2","article-title":"Effects of chronic cholinergic stimulation associated with aerobic physical training on cardiac morphofunctional and autonomic parameters in spontaneously hypertensive rats","volume":"11","author":"Gardim","year":"2021","journal-title":"Sci. Rep."}],"container-title":["Advances in Respiratory Medicine"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/www.mdpi.com\/2543-6031\/91\/6\/40\/pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2025,10,10]],"date-time":"2025-10-10T21:36:16Z","timestamp":1760132176000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.mdpi.com\/2543-6031\/91\/6\/40"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2023,12,1]]},"references-count":49,"journal-issue":{"issue":"6","published-online":{"date-parts":[[2023,12]]}},"alternative-id":["arm91060040"],"URL":"https:\/\/doi.org\/10.3390\/arm91060040","relation":{},"ISSN":["2543-6031"],"issn-type":[{"value":"2543-6031","type":"electronic"}],"subject":[],"published":{"date-parts":[[2023,12,1]]}}}