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Effect of Disease Severity on Respiratory Impedance in Parkinson’s Disease

Effect of Disease Severity on Respiratory Impedance in Parkinson’s Disease Background: Parkinson’s disease (PD) is a progressive neurodegenerative disorder. PD has been traditionally perceived as a motor disorder. However, it is frequently associated with pulmonary dysfunction which has been assessed by Spirometry, an effort-dependent technique. Purpose: To evaluate in patients with PD the effect of disease severity on respiratory impedance using Impulse Oscillometry (IOS) and to correlate with Spirometry. Methods: The study was conducted on 30 patients diagnosed with PD. Pulmonary function was assessed by IOS and spirometer. IOS is an effort-independent technique that uses sound waves of different frequencies to measure airway resistance. Spirometer measures the lung volume and generates flow–volume and volume–time relationship. Results: The mean age of patients was 60.1±9.45. Resistance at 5 Hz (R5) was found to be negatively correlated with forced expiratory volume in the first second of the FVC manoeuver (FEV ) (r = –0.628, P = .002), FEV /FVC (forced 1 1 vital capacity) (r = –0.487, P = .025), and PEF (r = –0.599, P = .004), and resistance at 20 Hz (R20) with FEV (r = –0.474, P = .029) and PEF (r = –0.522, P = .015). There was significant increase in R5 (0.32(0.36–0.28) vs 0.47(0.60–0.36); P = .04) and R20 (0.25(0.28–0.20) vs 0.30(0.40–0.25); P = .04) in stage II as compared to stage I of Hoehn–Yahr scale. Conclusion: IOS might be a promising tool for diagnosis of respiratory dysfunction in addition to Spirometry, especially in cases where patients are not able to perform forced manoeuvers. Keywords Airway resistance, Impulse Oscillometry, motor disorder, Parkinson’s disease, pulmonary function, spirometry This study, thus, aims to assess the effect of disease Introduction severity on pulmonary function using an effort-independent Parkinson’s disease (PD) is a progressive neurodegenerative technique, that is, Impulse Oscillometry (IOS) and correlate disorder. It is one of the most important movement disorders. with GOLD standard Spirometry to analyze if IOS is better at Around 6.3 million people worldwide suffer from PD. The detecting pulmonary dysfunction in patients with PD. age of onset is in the 60s (range: 35–85 years), and the course of the illness ranges between 10 and 25 years encompassing Methods both motor and non-motor symptoms. Study Design PD has been traditionally perceived as a motor disorder. However, several non-motor symptoms have gained attention This was a cross-sectional observational study assessing in recent years, including autonomic, sensory, neuropsychiatric respiratory dysfunction in PD. Consecutive patients visiting 3,4 and cognitive dysfunction. However, any impairment in the Neurology outpatient department after clinical diagnosis pulmonary function has not been generally manifested due were selected based on inclusion and exclusion criteria from to the sedentary lifestyle of the patients, though studies have been reported where pneumologic problems were found to be 1 Department of Physiology, All India Institute of Medical Sciences, the most common cause of death, but these studies have used New Delhi, India Department of Neurology, All India Institute of Medical Sciences, effort-dependent technique to assess pulmonary function. New Delhi, India Though obstructive patterns have been observed by Spirometry Corresponding author: and increased resistance by body plethysmography, it is not Anjana Talwar, 6003, 6th floor, Convergence Block, Department of Physiology, clear whether it is due to a motor disability or due to changes All India Institute of Medical Sciences, New Delhi 110029, India. in the airway resistance or both. E-mail: anjanatalwar@gmail.com Creative Commons CC BY: This article is distributed under the terms of the Creative Commons Attribution 4.0 License (http://www. creativecommons.org/licenses/by/4.0/) which permits any use, reproduction and distribution of the work without further permission provided the original work is attributed as specified on the SAGE and Open Access pages (https://us.sagepub.com/en-us/nam/open-access-at-sage). 64 Annals of Neurosciences 27(2) a tertiary care hospital. The study protocol was approved by IOS System is a non-invasive and effort-independent the Institute Ethics committee (Ref no: RT-3/22.07.2015). technique, unlike Spirometry which requires active Written informed consent was taken from all the subjects. participation by the patient. Dubois et al., in 1956 first described the forced oscillation technique (FOT) as a tool to measure respiratory impedance using the application of Participants external pressure waves of single or multiple frequencies 6,7 (2–35 Hz) to the spontaneous tidal breathing of patient. IOS The study was conducted on 30 patients with PD. The is a form of FOT which uses pressure oscillations at a fixed disease was diagnosed according to the United Kingdom frequency (square wave). Inspiratory and expiratory pressure Brain Bank criteria. Clinically diagnosed PD patients having and flow measured by the respective transducers are separated Hoehn–Yahr (H-Y) stage from I to IV and age ranging from from breathing pattern by “signal filtering.” Respiratory 40 to 70 years; both male and female were included in the impedance (Zrs) includes both respiratory resistance (Rrs) study. Patients with a history of lung or cardiovascular and respiratory reactance (Xrs) which are calculated by Fast disease affecting pulmonary function and those unable to Fourier Transformation (FFT) over a range of frequencies. perform pulmonary function test (PFT) due to anatomical Higher frequencies (>20 Hz) travel deeper into the lung abnormalities were excluded. All patients were non-smokers. and distal airways, whereas lower frequencies (<15 Hz) reflect Demographic features such as age, sex, height, and weight from proximal airways. Resistance and reactance at 5 Hz and were noted. Disease characteristics such as time since onset 20 Hz are denoted as R5, R20, and X5, X20 respectively. of symptoms and severity (evaluated by H-Y scale) were Therefore, resistance at lower frequency, that is, 5 Hz recorded. Patients were divided into two groups based on the (R5) gives information about the total respiratory system, H-Y scale (stage I and stage II) (Table 1). resistance at higher frequency, that is, 20 Hz (R20) provides information about central airways, and the difference between Study Procedure R5 and R20 reflects peripheral/small airways. Either central or peripheral airway obstruction results in increased R5. PFT was conducted using Spirometry (Medisoft Spiroair) and Central obstruction elevates resistance evenly; therefore, it IOS System (IOS-Jaeger). Patients were given instructions is independent of frequency. Peripheral obstruction elevates and demonstrations before the test. Trial sessions were held resistance at a lower frequency; therefore, resistance is to get the patients familiarized with the instrument. IOS frequency dependent. Resistance is the in-phase component was performed before Spirometry on the same day. Volume of respiratory impedance that reflects forward pressure of calibration for Spirometry and IOS was done using a 3 L conducting airways, whereas reactance is the out-of-phase syringe, and pressure calibration for IOS was performed with a component reflecting capacitive and inertive properties of reference resistance (0.2 kPa/L/s) daily. After the explanation airways. Capacitance represents the elastic properties of the of the procedure, patients were asked to sit comfortably lung and inertance represents the mass inertia of the moving without legs crossed and with a nose clip. Besides, during IOS air column. Reactance can be thought of rebound resistance maneuvers patients were asked to support their cheeks with giving information about the small airways. Conventionally, hands to prevent shunting of impulses, followed by normal capacitance is denoted by negative value and inertance by a tidal breathing in a relaxed state for at least 30–45 s during positive value. At lower frequency, capacitive pressure loss which around 120–150 sound impulses/pressure oscillations dominates; therefore, reactance at 5 Hz (X5) gives information were pushed into the lungs from which different parameters about tissue elastance and distal airways, whereas at higher were calculated. frequency, inertive pressure loss dominates. As the elasticity of the lung decreases, capacitance becomes more negative. Table 1. Demographic Data of Patients The frequency at which the total reactance is zero, that is, the magnitude of capacitance and inertance are the same, is Patients known as resonant frequency (Fres). Area of reactance (Ax) Pooled Patients Stage I Stage II represents total reactance at all frequencies between 5Hz and N = 30 N = 7 N = 7 Fres and provides information about the distal/peripheral Severity of PD H-Y Stage I, II, H-Y Stage I H-Y Stage II 6,8 airways. Normal value of Ax is <0.33 kPa/l. Coherence III, IV has a value between 0 and 1 reflecting reproducibility of Age 60.1±9.45 55.2±8.15 59.71±9.89 measurements. For accurate testing, at 5 Hz coherence should Height (cm) 164.5±6.80 166±3.91 163±5.85 be >0.8 cm H O and at 20 Hz, it should be between 0.9 and Weight (kg) 64.34±12.29 67±14.3 60.57±11.70 8 1. Average of 3–4 technically acceptable recordings were BMI 23.5±3.93 24.40±5.39 22.48±3.73 considered for calculations. Spirometry maneuver was performed according Source: The authors. Note: Data has been represented as mean±SD. to the guidelines given by Miller et al. Best of three Sampath et al. 65 Table 2. Correlation of Spirometry and IOS Parameters in PD Results Patients (n = 21) A total of 30 patients participated in the study (Table 1). All R5 (kPa/l/s) R20 (kPa/l/s) patients were on medication during the recording. Spirometry FEV % pred –0.628** –0.474* maneuver could not be performed in 9 out of 30 patients due FEV /FVC –0.487* – to a high rate of tremors; so, data for remaining patients have PEF% pred –0.599** –0.522* been presented. R5 was found to be negatively correlated with Source: The authors. FEV (P = .002), FEV /FVC (P = .025), and PEF (P = .004) 1 1 and R20 with FEV (P = .029) and PEF (P = .015) (Table 2). Note: Level of significance is denoted by asterisk (*) and (**) at 5% and 1% respectively. Data was stratified based on disease severity. There was a significant increase in R5 (P = 0.04) and R20 (P = 0.04) Table 3. Parameters of IOS and Spirometry in Stage I and Stage II in stage II as compared to stage I. However, we could not observe any significant differences in Spirometric parameters Stage I (n = 7) Stage II (n = 7) P Value (Table 3). R5 (kPa/l/s) 0.32(0.36-0.28) 0.47(0.60-0.36) 0.04* X5 (kPa/l/s) –0.13(–0.10) –0.13(–0.11) 0.94 Discussion – (–0.16) – (–0.29) R20 (kPa/l/s) 0.25(0.28-0.20) 0.30(0.40-0.25) 0.04* Despite recognition of pulmonary involvement in PD quite Ax (kPa/l) 0.67(0.84-0.22) 0.66(2.50-0.41) 0.70 early, little is known about the existing respiratory dysfunction. Fres (Hz) 17.27 17.41(24.04-16.39) 0.43 This study elucidates the respiratory abnormalities in PD (19.49-16.10) using IOS and Spirometer. There was not much difference Z5 (kPa/l/s) 0.35(0.38-0.32) 0.49(0.66-0.38) 0.07 in the mean percentage predicted values of Spirometric FEV % pred 95(100.5-76.30) 76.8(88.7-38.7) 0.10 parameters in those who were able to perform the tests, except for a consistent dip in the PEF among all patients. On FVC% pred 99.9(107.9-78.5) 80.8(98.6-59.8) 0.26 analyzing individual records, we observed three restrictive, FEV /FVC 76.08 70.99(78.79-45.09) 0.38 three obstructive, and four mixed patterns. (76.97-74.83) Lower FEV , FEV /FVC ratio, and PEF has been a frequent 1 1 PEF% pred 55.20 41.20967.40- 0.34 10,11,12 observation in PD patients. The reduction in the force (85.40-37.60) 16.20) exerted by expiratory muscles is discernible in the huge dip in Source: The authors. the PEF. The underlying motor disability, eventually results in Note: Data has been represented as median (inter quartile range). Level of low chest wall compliance and increased chest wall rigidity significance is denoted by asterisk (*) at 5%. leading to disordered respiratory mechanics, significantly contributing to increased morbidity and mortality in PD. technically accepted tests were obtained and forced vital The negative correlation of total and proximal airway capacity (FVC), forced expiratory volume in the first resistance R5 and R20, respectively, with FVC, FEV , and PEF second of the FVC manoeuver (FEV ), a ratio of FEV has been established in few studies. Qi et al. suggested that 1 1 to FVC (FEV % FVC), and peak expiratory flow (PEF) R5 might be used as a tool to investigate airway obstruction were calculated. All lung volumes were expressed as a in asthmatics, whereas Kolsum et al. found reactance values percentage of predicted values. to be more significantly correlated to Spirometric parameters in COPD patients. The total airway resistance, that is, R5 was found to be Statistical Analysis elevated with increasing severity of the (higher H-Y stage Each parameter was tested for distribution of the data based versus lower H-Y stage) disease. To the best of our knowledge on standard normality tests (D’ Agostino–Pearson omnibus there is no study to corroborate the current findings as this is normality test and Shapiro–Wilk test). The independent the first study to assess pulmonary function with increasing variable was stage I and stage II. Dependent variables were disease severity using the effort independent technique. parameters of IOS and parameters of Spirometry. Two group However, Spirometric parameters could not pick up any comparisons were done using unpaired t-test and Mann– significant difference with increasing disease severity. Whitney U test, as appropriate. To study the relationship We performed both the techniques in our study, between IOS and Spirometry techniques, Spearman’s one requiring effort (Spirometer) and the other which correlation was used. The level of statistical significance is independent of effort (IOS) to rule out the muscular was set at P < .05. All statistical analyses were performed component which is the underlying disability of patients with using GraphPad Prism version 5.00 for Windows (GraphPad PD. We have found that in spite of the decreased muscular Software, Inc., USA). force, these patients have high resistance as measured by 66 Annals of Neurosciences 27(2) IOS. So, the pulmonary dysfunction reported in these patients Co-relation with severity of disease and non-motor symptom might not be completely because of motor disability. scale score. J Clin Diagn Res 2014; 8(7): BC01– BC03. 3. Zesiewicz TA, Baker ML, Wahba M, et al. Autonomic nervous system dysfunction in Parkinson’s disease. Curr Treat Options Conclusion Neurol 2003; 5(2): 149–160. 4. Wang Y, Shao WB, Gao L, et al. Abnormal pulmonary function Resistance at 5 Hz and 20 Hz might be used as a diagnostic tool and respiratory muscle strength findings in Chinese patients with in conjunction with Spirometry in assessing the pulmonary Parkinson’s disease and multiple system atrophy-comparison dysfunction with increasing severity of the disease and with normal elderly. PloS One 2014; 9(12): e116123. also in cases where patients are not able to perform forced maneuvers. 5. Sabate M, Rodriguez M, Mendez E, et al. Obstructive and restrictive pulmonary dysfunction increases disability in Acknowledgments Parkinson disease. Arch Phys Med Rehabil 1996; 77: 29–34. The study was supported by Department of Physiology, All India 6. Bickel S, Popler J, Lesnick B, et al. Impulse oscillometry: Institute of Medical Sciences, New Delhi. Interpretation and practical applications. Chest 2014; 146(3): 841–847. Author Contributions 7. Nazeran H, Goldman MD, Nava P, et al. Forced oscillation: Patient recruitment, data acquisition, analysis and manuscript Neural networks can advance clinical utility of impulse preparation was performed by M. S. oscillometry in the assessment of lung function in asthmatic Concept and the intellectual content was proposed by A.T, A. K. J children. Int J Med Implants Devices 2007; 2: 89–107. and K. K. D. 8. Brashier B and Salvi S. Measuring lung function using sound Patients for data acquisition was provided by A. K. S and V.G. waves: role of the forced oscillation technique and impulse Manuscript was edited and reviewed by A. T, A. K. J, K. K. D, A. oscillometry system. Breathe 2015; 11(1): 57–65. K. S and V. G. 9. Miller MR, Hankinson J, Brusasco V, et al. Standardisation of spirometry. Eur Respir J 2005; 26(2): 319–338. Declaration of Conflicting Interests 10. Sabate M, Gonzalez I, Ruperez F, et al. Obstructive and The authors declared the following potential conflicts of interest with restrictive pulmonary dysfunctions in Parkinson’s disease. J respect to the research, authorship, and/or publication of this article: Neurol Sci 1996; 138(1–2): 114–119. The manuscript has not been presented elsewhere for consideration and complies with ICMJE guidelines. The authors declare no conflict 11. De Pandis MF, Starace A, Stefanelli F, et al. Modification of interest. of respiratory function parameters in patients with severe Parkinson’s disease. Neurol Sci 2002; 23: S69–S70. Ethical Statement 12. Izquierdo-Alonso JL, Jimenez-Jimenez FJ, Cabrera-Valdivia F, et al. Airway dysfunction in patients with Parkinson’s disease. The study protocol was discussed and approved by the ʻInstitute Ethics Committee for Post Graduate Research’, All India Institute of Lung 1994; 172(1): 47–55. Medical Sciences, New Delhi (Ref no: RT-3/22.07.2015). 13. Sathyaprabha TN, Kapavarapu PK, Pall PK, et al. Pulmonary functions in Parkinson’s disease. Indian J Chest Dis Allied Sci Funding 2005; 47(4): 251–257. The authors received no financial support for the research, 14. Owolabi LF, Nagoda M, and Babashani M. Pulmonary function authorship, and/or publication of this article. tests in patients with Parkinson’s disease: A case-control study. Niger J Clin Pract 2016 Feb; 19(1): 66–70. ORCID iD 15. Qi GS, Zhou ZC, Gu WC, et al. Detection of the airway Anjana Talwar https://orcid.org/0000-0001-7947-5209 obstruction stage in asthma using impulse oscillometry system. J Asthma 2013; 50(1): 45–51. References 16. Kolsum U, Borrill Z, Roy K, et al. Impulse oscillometry in 1. Gupta BM and Bala A. Parkinson’s disease in India: An analysis COPD: Identification of measurements related to airway of publications output during 2002–2011. Int J Nutr Pharmacol obstruction, airway conductance and lung volumes. Respir Neurol Dis 2013; 3(3): 254–262. Med 2009; 103(1): 136–143. 2. Bidikar MP, Jagtap GJ, and Chakor RT. Influence of deep breathing on heart rate variability in Parkinson’s disease: http://www.deepdyve.com/assets/images/DeepDyve-Logo-lg.png Annals of Neurosciences SAGE

Effect of Disease Severity on Respiratory Impedance in Parkinson’s Disease

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Abstract

Background: Parkinson’s disease (PD) is a progressive neurodegenerative disorder. PD has been traditionally perceived as a motor disorder. However, it is frequently associated with pulmonary dysfunction which has been assessed by Spirometry, an effort-dependent technique. Purpose: To evaluate in patients with PD the effect of disease severity on respiratory impedance using Impulse Oscillometry (IOS) and to correlate with Spirometry. Methods: The study was conducted on 30 patients diagnosed with PD. Pulmonary function was assessed by IOS and spirometer. IOS is an effort-independent technique that uses sound waves of different frequencies to measure airway resistance. Spirometer measures the lung volume and generates flow–volume and volume–time relationship. Results: The mean age of patients was 60.1±9.45. Resistance at 5 Hz (R5) was found to be negatively correlated with forced expiratory volume in the first second of the FVC manoeuver (FEV ) (r = –0.628, P = .002), FEV /FVC (forced 1 1 vital capacity) (r = –0.487, P = .025), and PEF (r = –0.599, P = .004), and resistance at 20 Hz (R20) with FEV (r = –0.474, P = .029) and PEF (r = –0.522, P = .015). There was significant increase in R5 (0.32(0.36–0.28) vs 0.47(0.60–0.36); P = .04) and R20 (0.25(0.28–0.20) vs 0.30(0.40–0.25); P = .04) in stage II as compared to stage I of Hoehn–Yahr scale. Conclusion: IOS might be a promising tool for diagnosis of respiratory dysfunction in addition to Spirometry, especially in cases where patients are not able to perform forced manoeuvers. Keywords Airway resistance, Impulse Oscillometry, motor disorder, Parkinson’s disease, pulmonary function, spirometry This study, thus, aims to assess the effect of disease Introduction severity on pulmonary function using an effort-independent Parkinson’s disease (PD) is a progressive neurodegenerative technique, that is, Impulse Oscillometry (IOS) and correlate disorder. It is one of the most important movement disorders. with GOLD standard Spirometry to analyze if IOS is better at Around 6.3 million people worldwide suffer from PD. The detecting pulmonary dysfunction in patients with PD. age of onset is in the 60s (range: 35–85 years), and the course of the illness ranges between 10 and 25 years encompassing Methods both motor and non-motor symptoms. Study Design PD has been traditionally perceived as a motor disorder. However, several non-motor symptoms have gained attention This was a cross-sectional observational study assessing in recent years, including autonomic, sensory, neuropsychiatric respiratory dysfunction in PD. Consecutive patients visiting 3,4 and cognitive dysfunction. However, any impairment in the Neurology outpatient department after clinical diagnosis pulmonary function has not been generally manifested due were selected based on inclusion and exclusion criteria from to the sedentary lifestyle of the patients, though studies have been reported where pneumologic problems were found to be 1 Department of Physiology, All India Institute of Medical Sciences, the most common cause of death, but these studies have used New Delhi, India Department of Neurology, All India Institute of Medical Sciences, effort-dependent technique to assess pulmonary function. New Delhi, India Though obstructive patterns have been observed by Spirometry Corresponding author: and increased resistance by body plethysmography, it is not Anjana Talwar, 6003, 6th floor, Convergence Block, Department of Physiology, clear whether it is due to a motor disability or due to changes All India Institute of Medical Sciences, New Delhi 110029, India. in the airway resistance or both. E-mail: anjanatalwar@gmail.com Creative Commons CC BY: This article is distributed under the terms of the Creative Commons Attribution 4.0 License (http://www. creativecommons.org/licenses/by/4.0/) which permits any use, reproduction and distribution of the work without further permission provided the original work is attributed as specified on the SAGE and Open Access pages (https://us.sagepub.com/en-us/nam/open-access-at-sage). 64 Annals of Neurosciences 27(2) a tertiary care hospital. The study protocol was approved by IOS System is a non-invasive and effort-independent the Institute Ethics committee (Ref no: RT-3/22.07.2015). technique, unlike Spirometry which requires active Written informed consent was taken from all the subjects. participation by the patient. Dubois et al., in 1956 first described the forced oscillation technique (FOT) as a tool to measure respiratory impedance using the application of Participants external pressure waves of single or multiple frequencies 6,7 (2–35 Hz) to the spontaneous tidal breathing of patient. IOS The study was conducted on 30 patients with PD. The is a form of FOT which uses pressure oscillations at a fixed disease was diagnosed according to the United Kingdom frequency (square wave). Inspiratory and expiratory pressure Brain Bank criteria. Clinically diagnosed PD patients having and flow measured by the respective transducers are separated Hoehn–Yahr (H-Y) stage from I to IV and age ranging from from breathing pattern by “signal filtering.” Respiratory 40 to 70 years; both male and female were included in the impedance (Zrs) includes both respiratory resistance (Rrs) study. Patients with a history of lung or cardiovascular and respiratory reactance (Xrs) which are calculated by Fast disease affecting pulmonary function and those unable to Fourier Transformation (FFT) over a range of frequencies. perform pulmonary function test (PFT) due to anatomical Higher frequencies (>20 Hz) travel deeper into the lung abnormalities were excluded. All patients were non-smokers. and distal airways, whereas lower frequencies (<15 Hz) reflect Demographic features such as age, sex, height, and weight from proximal airways. Resistance and reactance at 5 Hz and were noted. Disease characteristics such as time since onset 20 Hz are denoted as R5, R20, and X5, X20 respectively. of symptoms and severity (evaluated by H-Y scale) were Therefore, resistance at lower frequency, that is, 5 Hz recorded. Patients were divided into two groups based on the (R5) gives information about the total respiratory system, H-Y scale (stage I and stage II) (Table 1). resistance at higher frequency, that is, 20 Hz (R20) provides information about central airways, and the difference between Study Procedure R5 and R20 reflects peripheral/small airways. Either central or peripheral airway obstruction results in increased R5. PFT was conducted using Spirometry (Medisoft Spiroair) and Central obstruction elevates resistance evenly; therefore, it IOS System (IOS-Jaeger). Patients were given instructions is independent of frequency. Peripheral obstruction elevates and demonstrations before the test. Trial sessions were held resistance at a lower frequency; therefore, resistance is to get the patients familiarized with the instrument. IOS frequency dependent. Resistance is the in-phase component was performed before Spirometry on the same day. Volume of respiratory impedance that reflects forward pressure of calibration for Spirometry and IOS was done using a 3 L conducting airways, whereas reactance is the out-of-phase syringe, and pressure calibration for IOS was performed with a component reflecting capacitive and inertive properties of reference resistance (0.2 kPa/L/s) daily. After the explanation airways. Capacitance represents the elastic properties of the of the procedure, patients were asked to sit comfortably lung and inertance represents the mass inertia of the moving without legs crossed and with a nose clip. Besides, during IOS air column. Reactance can be thought of rebound resistance maneuvers patients were asked to support their cheeks with giving information about the small airways. Conventionally, hands to prevent shunting of impulses, followed by normal capacitance is denoted by negative value and inertance by a tidal breathing in a relaxed state for at least 30–45 s during positive value. At lower frequency, capacitive pressure loss which around 120–150 sound impulses/pressure oscillations dominates; therefore, reactance at 5 Hz (X5) gives information were pushed into the lungs from which different parameters about tissue elastance and distal airways, whereas at higher were calculated. frequency, inertive pressure loss dominates. As the elasticity of the lung decreases, capacitance becomes more negative. Table 1. Demographic Data of Patients The frequency at which the total reactance is zero, that is, the magnitude of capacitance and inertance are the same, is Patients known as resonant frequency (Fres). Area of reactance (Ax) Pooled Patients Stage I Stage II represents total reactance at all frequencies between 5Hz and N = 30 N = 7 N = 7 Fres and provides information about the distal/peripheral Severity of PD H-Y Stage I, II, H-Y Stage I H-Y Stage II 6,8 airways. Normal value of Ax is <0.33 kPa/l. Coherence III, IV has a value between 0 and 1 reflecting reproducibility of Age 60.1±9.45 55.2±8.15 59.71±9.89 measurements. For accurate testing, at 5 Hz coherence should Height (cm) 164.5±6.80 166±3.91 163±5.85 be >0.8 cm H O and at 20 Hz, it should be between 0.9 and Weight (kg) 64.34±12.29 67±14.3 60.57±11.70 8 1. Average of 3–4 technically acceptable recordings were BMI 23.5±3.93 24.40±5.39 22.48±3.73 considered for calculations. Spirometry maneuver was performed according Source: The authors. Note: Data has been represented as mean±SD. to the guidelines given by Miller et al. Best of three Sampath et al. 65 Table 2. Correlation of Spirometry and IOS Parameters in PD Results Patients (n = 21) A total of 30 patients participated in the study (Table 1). All R5 (kPa/l/s) R20 (kPa/l/s) patients were on medication during the recording. Spirometry FEV % pred –0.628** –0.474* maneuver could not be performed in 9 out of 30 patients due FEV /FVC –0.487* – to a high rate of tremors; so, data for remaining patients have PEF% pred –0.599** –0.522* been presented. R5 was found to be negatively correlated with Source: The authors. FEV (P = .002), FEV /FVC (P = .025), and PEF (P = .004) 1 1 and R20 with FEV (P = .029) and PEF (P = .015) (Table 2). Note: Level of significance is denoted by asterisk (*) and (**) at 5% and 1% respectively. Data was stratified based on disease severity. There was a significant increase in R5 (P = 0.04) and R20 (P = 0.04) Table 3. Parameters of IOS and Spirometry in Stage I and Stage II in stage II as compared to stage I. However, we could not observe any significant differences in Spirometric parameters Stage I (n = 7) Stage II (n = 7) P Value (Table 3). R5 (kPa/l/s) 0.32(0.36-0.28) 0.47(0.60-0.36) 0.04* X5 (kPa/l/s) –0.13(–0.10) –0.13(–0.11) 0.94 Discussion – (–0.16) – (–0.29) R20 (kPa/l/s) 0.25(0.28-0.20) 0.30(0.40-0.25) 0.04* Despite recognition of pulmonary involvement in PD quite Ax (kPa/l) 0.67(0.84-0.22) 0.66(2.50-0.41) 0.70 early, little is known about the existing respiratory dysfunction. Fres (Hz) 17.27 17.41(24.04-16.39) 0.43 This study elucidates the respiratory abnormalities in PD (19.49-16.10) using IOS and Spirometer. There was not much difference Z5 (kPa/l/s) 0.35(0.38-0.32) 0.49(0.66-0.38) 0.07 in the mean percentage predicted values of Spirometric FEV % pred 95(100.5-76.30) 76.8(88.7-38.7) 0.10 parameters in those who were able to perform the tests, except for a consistent dip in the PEF among all patients. On FVC% pred 99.9(107.9-78.5) 80.8(98.6-59.8) 0.26 analyzing individual records, we observed three restrictive, FEV /FVC 76.08 70.99(78.79-45.09) 0.38 three obstructive, and four mixed patterns. (76.97-74.83) Lower FEV , FEV /FVC ratio, and PEF has been a frequent 1 1 PEF% pred 55.20 41.20967.40- 0.34 10,11,12 observation in PD patients. The reduction in the force (85.40-37.60) 16.20) exerted by expiratory muscles is discernible in the huge dip in Source: The authors. the PEF. The underlying motor disability, eventually results in Note: Data has been represented as median (inter quartile range). Level of low chest wall compliance and increased chest wall rigidity significance is denoted by asterisk (*) at 5%. leading to disordered respiratory mechanics, significantly contributing to increased morbidity and mortality in PD. technically accepted tests were obtained and forced vital The negative correlation of total and proximal airway capacity (FVC), forced expiratory volume in the first resistance R5 and R20, respectively, with FVC, FEV , and PEF second of the FVC manoeuver (FEV ), a ratio of FEV has been established in few studies. Qi et al. suggested that 1 1 to FVC (FEV % FVC), and peak expiratory flow (PEF) R5 might be used as a tool to investigate airway obstruction were calculated. All lung volumes were expressed as a in asthmatics, whereas Kolsum et al. found reactance values percentage of predicted values. to be more significantly correlated to Spirometric parameters in COPD patients. The total airway resistance, that is, R5 was found to be Statistical Analysis elevated with increasing severity of the (higher H-Y stage Each parameter was tested for distribution of the data based versus lower H-Y stage) disease. To the best of our knowledge on standard normality tests (D’ Agostino–Pearson omnibus there is no study to corroborate the current findings as this is normality test and Shapiro–Wilk test). The independent the first study to assess pulmonary function with increasing variable was stage I and stage II. Dependent variables were disease severity using the effort independent technique. parameters of IOS and parameters of Spirometry. Two group However, Spirometric parameters could not pick up any comparisons were done using unpaired t-test and Mann– significant difference with increasing disease severity. Whitney U test, as appropriate. To study the relationship We performed both the techniques in our study, between IOS and Spirometry techniques, Spearman’s one requiring effort (Spirometer) and the other which correlation was used. The level of statistical significance is independent of effort (IOS) to rule out the muscular was set at P < .05. All statistical analyses were performed component which is the underlying disability of patients with using GraphPad Prism version 5.00 for Windows (GraphPad PD. We have found that in spite of the decreased muscular Software, Inc., USA). force, these patients have high resistance as measured by 66 Annals of Neurosciences 27(2) IOS. So, the pulmonary dysfunction reported in these patients Co-relation with severity of disease and non-motor symptom might not be completely because of motor disability. scale score. J Clin Diagn Res 2014; 8(7): BC01– BC03. 3. Zesiewicz TA, Baker ML, Wahba M, et al. Autonomic nervous system dysfunction in Parkinson’s disease. Curr Treat Options Conclusion Neurol 2003; 5(2): 149–160. 4. Wang Y, Shao WB, Gao L, et al. Abnormal pulmonary function Resistance at 5 Hz and 20 Hz might be used as a diagnostic tool and respiratory muscle strength findings in Chinese patients with in conjunction with Spirometry in assessing the pulmonary Parkinson’s disease and multiple system atrophy-comparison dysfunction with increasing severity of the disease and with normal elderly. PloS One 2014; 9(12): e116123. also in cases where patients are not able to perform forced maneuvers. 5. Sabate M, Rodriguez M, Mendez E, et al. Obstructive and restrictive pulmonary dysfunction increases disability in Acknowledgments Parkinson disease. Arch Phys Med Rehabil 1996; 77: 29–34. The study was supported by Department of Physiology, All India 6. Bickel S, Popler J, Lesnick B, et al. Impulse oscillometry: Institute of Medical Sciences, New Delhi. Interpretation and practical applications. Chest 2014; 146(3): 841–847. Author Contributions 7. Nazeran H, Goldman MD, Nava P, et al. Forced oscillation: Patient recruitment, data acquisition, analysis and manuscript Neural networks can advance clinical utility of impulse preparation was performed by M. S. oscillometry in the assessment of lung function in asthmatic Concept and the intellectual content was proposed by A.T, A. K. J children. Int J Med Implants Devices 2007; 2: 89–107. and K. K. D. 8. Brashier B and Salvi S. Measuring lung function using sound Patients for data acquisition was provided by A. K. S and V.G. waves: role of the forced oscillation technique and impulse Manuscript was edited and reviewed by A. T, A. K. J, K. K. D, A. oscillometry system. Breathe 2015; 11(1): 57–65. K. S and V. G. 9. Miller MR, Hankinson J, Brusasco V, et al. Standardisation of spirometry. Eur Respir J 2005; 26(2): 319–338. Declaration of Conflicting Interests 10. Sabate M, Gonzalez I, Ruperez F, et al. Obstructive and The authors declared the following potential conflicts of interest with restrictive pulmonary dysfunctions in Parkinson’s disease. J respect to the research, authorship, and/or publication of this article: Neurol Sci 1996; 138(1–2): 114–119. The manuscript has not been presented elsewhere for consideration and complies with ICMJE guidelines. The authors declare no conflict 11. De Pandis MF, Starace A, Stefanelli F, et al. Modification of interest. of respiratory function parameters in patients with severe Parkinson’s disease. Neurol Sci 2002; 23: S69–S70. Ethical Statement 12. Izquierdo-Alonso JL, Jimenez-Jimenez FJ, Cabrera-Valdivia F, et al. Airway dysfunction in patients with Parkinson’s disease. The study protocol was discussed and approved by the ʻInstitute Ethics Committee for Post Graduate Research’, All India Institute of Lung 1994; 172(1): 47–55. Medical Sciences, New Delhi (Ref no: RT-3/22.07.2015). 13. Sathyaprabha TN, Kapavarapu PK, Pall PK, et al. Pulmonary functions in Parkinson’s disease. Indian J Chest Dis Allied Sci Funding 2005; 47(4): 251–257. The authors received no financial support for the research, 14. Owolabi LF, Nagoda M, and Babashani M. Pulmonary function authorship, and/or publication of this article. tests in patients with Parkinson’s disease: A case-control study. Niger J Clin Pract 2016 Feb; 19(1): 66–70. ORCID iD 15. Qi GS, Zhou ZC, Gu WC, et al. Detection of the airway Anjana Talwar https://orcid.org/0000-0001-7947-5209 obstruction stage in asthma using impulse oscillometry system. J Asthma 2013; 50(1): 45–51. References 16. Kolsum U, Borrill Z, Roy K, et al. Impulse oscillometry in 1. Gupta BM and Bala A. Parkinson’s disease in India: An analysis COPD: Identification of measurements related to airway of publications output during 2002–2011. Int J Nutr Pharmacol obstruction, airway conductance and lung volumes. Respir Neurol Dis 2013; 3(3): 254–262. Med 2009; 103(1): 136–143. 2. Bidikar MP, Jagtap GJ, and Chakor RT. Influence of deep breathing on heart rate variability in Parkinson’s disease:

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