|
|
ORIGINAL ARTICLE |
|
Year : 2022 | Volume
: 16
| Issue : 2 | Page : 54-59 |
|
Association of respiratory muscle strength with glycosylated hemoglobin (HbA1c) levels, duration of disease, and physical activity levels in patients with type 2 diabetes: A cross-sectional study
Shrikant Ramkrishna Sahu1, Shreya Rahul Dhake2
1 Department of Physiotherapy, Manipal College of Health Professions, MAHE, Manipal, Karnataka, India 2 Department of Cardiovascular and Respiratory Physiotherapy, DES's Brijlal Jindal College of Physiotherapy, Pune, Maharashtra, India
Date of Submission | 17-Jun-2022 |
Date of Decision | 21-Oct-2022 |
Date of Acceptance | 30-Oct-2022 |
Date of Web Publication | 31-Jan-2023 |
Correspondence Address: Dr. Shrikant Ramkrishna Sahu C-78, Vineet Nagar, MBPT Staff Quarters, Near Cotton Green Railway Station, Kalachowky, Mumbai - 400 033, Maharashtra India
 Source of Support: None, Conflict of Interest: None  | Check |
DOI: 10.4103/pjiap.pjiap_27_22
CONTEXT: Type 2 diabetes is a systemic disorder that propagates several pathological processes leading to a plethora of complications including those on skeletal muscle strength and lung function. AIMS: This study aims to evaluate the association of glycemic control, duration of disease, and physical activity level on respiratory muscle strength (RMS). SETTINGS AND DESIGN: A cross-sectional study was conducted in the outpatient department setting after approval from the institutional ethics committee. SUBJECTS AND METHODS: The Hemoglobin A1c (HbA1c) level of recruited participants was recorded from a recent laboratory test and they were interviewed with the Rapid Assessment of Physical Activity (RAPA) tool to obtain their current physical activity levels. The evaluation of maximal inspiratory pressure (MIP) and maximal expiratory pressure (MEP) was performed using the MicroRespiratory Pressure Meter (MicroRPM) device. STATISTICAL ANALYSIS USED: Pearson's correlation coefficient (r) was calculated for the RMS variables (MIP and MEP) against HbA1c, duration of disease, and RAPA Score. RESULTS: Twenty-six participants were evaluated. Significant correlations were found HbA1c with MIP (r = −0.45, P = 0.02) and RAPA Score with MIP (r = 0.42, P = 0.03) at P < 0.05. CONCLUSIONS: Inspiratory muscle strength is well associated with glycemic control and physical activity of the individual.
Keywords: Chronic hyperglycemia, duration of diabetes, glycosylated hemoglobin, maximal respiratory pressures, physical activity, respiratory muscle strength, type 2 diabetes
How to cite this article: Sahu SR, Dhake SR. Association of respiratory muscle strength with glycosylated hemoglobin (HbA1c) levels, duration of disease, and physical activity levels in patients with type 2 diabetes: A cross-sectional study. Physiother - J Indian Assoc Physiother 2022;16:54-9 |
How to cite this URL: Sahu SR, Dhake SR. Association of respiratory muscle strength with glycosylated hemoglobin (HbA1c) levels, duration of disease, and physical activity levels in patients with type 2 diabetes: A cross-sectional study. Physiother - J Indian Assoc Physiother [serial online] 2022 [cited 2023 Jun 5];16:54-9. Available from: https://www.pjiap.org/text.asp?2022/16/2/54/368876 |
Introduction | |  |
Diabetes mellitus is defined as a group of metabolic diseases characterized by hyperglycemia resulting from defects in insulin secretion, insulin action, or both.[1]
Chronic hyperglycemia is intricately related to most complications of type 2 diabetes. In the past decade, glycosylated hemoglobin A1c (HbA1c) has taken over regular blood sugar level monitoring as a measure of glycemic control.[2]
Diabetic myopathy, a complication of diabetes, is the failure to preserve muscle mass and function. The occurrence of fatty infiltration of skeletal muscles has been proved in type 2 diabetes, leading to impaired mitochondrial function and oxidative stress.[3] Oxidative stress is an independent factor causing structural alterations in the mitochondria.[4]
The duration of diabetes is a strong predictor of a majority of the complications of diabetes.[5],[6],[7],[8] However, conflicting evidence exists regarding the association of respiratory muscle strength (RMS) with the duration of diabetes.[9],[10],[11],[12]
The presence of cardiac autonomic neuropathy impairs exercise tolerance and lowers maximal heart rate. Exercise training results in a shift in the cardiac sympathovagal balance in favor of parasympathetic dominance in individuals with diabetes.[13]
Lung function in type 2 diabetics has been repeatedly evaluated and proved to be clinically reduced primarily due to microangiopathies of the pulmonary vasculature and phrenic neuropathy.[12],[14],[15],[16],[17],[18],[19],[20] However, there is a lack of literature that clinically evaluates the RMS in patients with type 2 diabetes. India has shown a high prevalence,[20] low awareness, and poor attitude[21],[22] concerning diabetes. Hence, it is important to identify and evaluate additional factors that are prone to be overlooked. Maximal Inspiratory Pressure (MIP) and Maximal Expiratory Pressure (MEP) are valid clinical measures of RMS.[23] Hence, we propose a two-tailed hypothesis that RMS has some correlation with glycosylated hemoglobin, duration of disease, and physical activity in patients with type 2 diabetes.
Subjects and Methods | |  |
The sample size calculation was done using power calculation with a confidence interval of 90%, an effect size of 0.11 (prevalence of diabetes in Indian urban population),[20] and power of 90%. Twenty-six participants in the age group of 40–65 years diagnosed with type 2 diabetes by a registered diabetologist for more than or equal to 5 years were recruited for evaluation of maximal respiratory pressures. If any of such participants had a history of or was currently suffering from cardiopulmonary diseases, had a musculoskeletal deformity of the rib cage, was a smoker, was diagnosed with any other endocrinological disorder other than type 2 diabetes mellitus, or was diagnosed with a neurological disorder affecting cognition, they were excluded from the study.
The maximal inspiratory and expiratory pressures were measured using the Care Fusion Micro RPM device (San Diego, California, United States) according to the American Thoracic Society (ATS) guidelines for respiratory muscle assessment.[23]
The institutional ethics committee approval was obtained. Participants were explained the nature and purpose of the study and informed consent was taken. After screening according to the inclusion and exclusion criteria, participants were recruited. History evaluation was performed to obtain the duration of diabetes and the participants were interviewed with the Rapid Assessment of Physical Activity (RAPA) Scale. The RAPA tool is a self-administered scale to assess the level of physical activity. HbA1c was recorded from the most recent laboratory report at most 12 weeks' old.[24] If such a report was not available, the same was conducted and the result recorded. The cost of the test was borne by the researchers. The maximal inspiratory and expiratory pressures were evaluated as per the ATS guidelines for respiratory muscle assessment.[23]
Data management and analysis
The duration of disease (in years), glycosylated hemoglobin levels (in %), RAPA scores, MIP, and MEP (in cmH2O) scores were entered in the excel sheet and SPSS software, version 16 (SPSS Statistics, SPSS Inc., IBM, Chicago, Illinois, United States of America.) for analysis. Pearson's correlation coefficient ® was calculated to evaluate the correlation between the MIP and MEP score with the duration of disease, HbA1C levels, and RAPA score. A correlation with a test of significance P < 0.05 was considered statistically significant.
Results | |  |
The current study assessed 26 individuals in the age group of 40–65 years for MIP and MEP. The independent variables were, HbA1c, duration of disease, and RAPA Score. The Kolmogorov–Smirnov Z-test for normality produced insignificant results (P > 0.05) for all the independent and dependent variables proving that the variables were normally distributed [Table 1]. As the data were normally distributed, Pearson's correlation coefficient was used to analyze the correlation between the dependent and independent variables. The dependent variables are MIP and MEP while the independent variables are HbA1c, duration of disease, and RAPA score. | Table 1: Descriptive statistics of the variables analysed with normality test values
Click here to view |
The data showed a significant correlation of HbA1c with MIP (P < 0.05) but an insignificant correlation with MEP [P > 0.05, [Table 2]]. The current study produced results that show a significant correlation between Physical activity measured through the RAPA scale and MIP (P < 0.05). However, the correlation was not significant with MEP [P > 0.05, [Table 2]]. | Table 2: Correlation of glycosylated hemoglobin, duration of disease and rapid assessment of physical activity score with maximal inspiratory pressure and maximal expiratory pressure
Click here to view |
Discussion | |  |
This study evaluated the RMSs of type 2 diabetics aged 40–65 years. The inspiratory and expiratory muscle strengths, measured as MIP and MEP were evaluated for their association with HbA1c, duration of disease, and physical activity to establish their clinical importance in predicting significant subclinical respiratory muscle weakness in the absence of other conditions that negatively affect RMS; this isolates the significant effects of diabetic pathology on RMS. MIP was found to be significantly correlated with glycosylated hemoglobin and RAPA score.
Respiratory muscle strength
Both MIP and MEP were considerably lower than the normative data established earlier in the Indian population of the same age group.[25] The mean MIP obtained in this study (76.46 + 23.92 cm H2O) and the one obtained from the normative data for a higher age group (61–70 years → 76.10 + 10.10) were similar. This was not true for MEP (79.81 + 22.78 in this study vs. 67.18 + 14.0 in the normative study), which was higher when compared to the older age group. This finding points toward an experimental finding that says that diabetic processes contribute to accelerated loss of skeletal muscle strength.[26],[27],[28] The oxidative stress and molecular inflammation following extended hyperglycemia have been identified as the culprit for these changes.[3]
Zineldin et al. which had a comparable mean age of the patient population, got lower scores for both MIP and MEP when compared to the control population.[12] Fuso et al. got similar MIP values, with a significant difference between the patient and control population. The MEP values, however, were considerably higher, enough that the authors did not find any significant difference between the performances of the patient and control population.[10]
There is a decrease in overall pulmonary function with age.[29] To differentiate this physiological phenomenon in normal people from those occurring in patients with type 2 diabetes, Litonjua et al. conducted a longitudinal observational study.[30] The cases produced a lower lung function compared to the controls; this difference was due to a lower baseline lung function rather than the diabetic pathology. This study assessed the lung function and not the RMS, hence the applicability of its conclusions to the current study is restricted. It should be noted though that such a study is lacking for RMS in diabetics. RMS is closely related to lung function and until a similar conclusive study is conducted for RMS, the influence of preexisting physiology and a lower baseline RMS should not be discarded.
Hemoglobin A1c and respiratory muscle strength
HbA1c showed a significant association with MIP but not with MEP (r = −0.23, P > 0.05). Experimental findings evidence the fiber composition of the diaphragm and abdominal muscles to be primarily of type 1 fibers.[31],[32] Thus the microvascular complications of type 2 diabetes should produce similar effects on both muscles. This discrepancy in the obtained results can be explained by the results of the RCT performed by Kamsniski et al. The study group in their RCT which included patients with Diabetic Autonomic Neuropathy (DAN) had significantly lower MIP than the control group that consisted of type 2 diabetes patients without DAN; this was not true for MEP. Interestingly, the HbA1c showed no significant difference between the groups. Thus, independent of glycaemic control, DAN can negatively influence the inspiratory pressure while expiratory pressure is spared. Furthermore, the results of this study are in line with the results of Zineldin et al. who found similar inconsistencies in correlations.[13]
There is strong evidence that diabetic neuropathy can cause phrenic nerve neuropathy that contributes to impaired respiratory muscle function and reduced RMS. The occurrence and extent of phrenic neuropathy are similar to peripheral neuropathy in diabetes, but respiratory symptoms usually do not manifest themselves like peripheral symptoms. Reduced RMS is much more difficult to diagnose as the symptoms usually do not manifest until another primary cardiac or respiratory disease worsens the pulmonary function. Emerging evidence suggests considering phrenic neuropathy as the culprit for new onset, unexplained respiratory failure in type 2 diabetes and prediabetes. Hence, RMS impairment in type 2 diabetes, which in itself is subtle as found in this study, can easily go unnoticed until the clinical situation gets serious enough.
Other pathologies should be considered that negatively influence RMS as there are cases of type 2 diabetes without neuropathy that have reduced RMS.[33] These pathologies include downregulation of GLUT-4 protein, impaired glucose and fat metabolism, mitochondrial damage, endothelial damage, etc., The respiratory diaphragm is a skeletal muscle that is prone to suffer from these pathologies. Endothelial damage can impair the vascular supply to the muscle which is majorly composed of type 1 fibers furthering the deterioration of its function.
Duration of disease and respiratory muscle strength
The insignificant association of the duration of diabetes with RMS complications found in this study does not fit well along with its association with other complications of diabetes. Duration of diabetes is a significant determinant for the incidence and impact of various complications of diabetes including diabetic neuropathy,[8] nephropathy.[7] retinopathy[6] and autonomic neuropathy[9] However, conflicting evidence exists regarding the association of RMS with the duration of diabetes. Some studies concluded an insignificant correlation between the two parameters[10],[11] while other studies pointed out a weak negative significant correlation.[12],[13] The insignificant correlations were achieved with different measures of RMS including the maximal respiratory pressures, sniff oesophageal pressure, and trans-diaphragmatic pressure. The current study lines with the majority of evidence (r = −0.18, P > 0.05 for MIP and r = −0.04, P > 0.05 for MEP), however, not without its own caveats where it falls short on statistical aspects.
Scientifically, there is little to explore further. Duration of disease is a population-dependent variable and its controllable determinants are scarce. Hence, a close inspection of the descriptive analysis reveals a greater spread of data in this variable compared to other independent variables. The standard deviation for the duration of the disease is as much as 37% of the mean. The range extends from 5 to 20 (15) with a sample size of 26. This could serve as a significant limiting factor for the indiscriminate interpretation of the attained results. Resultantly, the samples assessed can be deemed as inadequate for this particular independent variable which allows for a greater spread of data. However, it should be noted that such data is still scarce in the current literature as it stands, and any concrete understanding of the subject should be put on hold until the confounding factors can be satisfactorily dealt with. Hence, for this subtopic, it would be more appropriate to say that the results were inconclusive rather than insignificant.
Physical activity and respiratory muscle strength
The assessment in the current study, which was carried out using a reliable and valid tool for Physical activity level assessment, the RAPA score, produced significantly positive results with MIP (r = 0.42, P < 0.05).
These findings are in line with the current evidence of positive effects of Physical activity on the aerobic capacity of the individual and now can be extended to RMS.[14],[34] Physical Activity has a global effect on various systems of the body. Right from accelerating hepatic glucose production, modifying GLUT-4 metabolism, and regulating lipid metabolism to increasing insulin sensitivity in the absence of insulin and improving glycogen re-synthesis in the muscle, physical activity can help alleviate the hyperglycaemic state in diabetes by creating a hyperinsulinemia-like state and sustain it for hours postexercise. These changes are primarily seen in the muscles that exercise, i.e., peripheral muscles.
There is limited evidence regarding the association of RMS and peripheral muscle strength in normal individuals without any respiratory pathology. One study that affirms such a correlation in athletes found that knee extensor and flexor strengths are significantly correlated to RMS.[35] The effects of regular, moderate physical activity on skeletal muscle strength can thus be translated to RMS as found in the current study.
Another study assessed the association of MEP with Physical Activity which was obtained with an interview. There was convincing evidence that patients without any regular exercise in daily life have been found to score a significantly lower MEP than those that perform regular exercise.[36] These bits of evidence expand the understanding of the cycle of low physical activity, obesity, cardiovascular disease (CVD), reduced RMS, and various other accompanying and preceding complications of these disorders seen in type 2 diabetes.
The participants reported their physical activities to be ranging from "under-active-regular" to "active" physical activity on the RAPA scale with no "sedentary" individuals. Higher levels of physical activity through immediate and chronic metabolic effects help in improving glycaemic control in type 2 diabetics. This is reflected in the HbA1c data. Although the highest recorded value of HbA1c was 10.3, the data were found to be skewed to the left, or lower side, indicating a greater aggregation of data in the lower values of HbA1c ([Mean + SD [6.93 + 1.21], Skewness [1.67]).
Glycaemic control in type 2 diabetes is the most important parameter under continuous monitoring and is also well correlated with RMS. In acute settings, glycaemic control usually worsens due to disturbed metabolism triggered by the primary pathology of the acute disorder. In such conditions, the long-acting pathologies of diabetes may act as a base for the rapid deterioration of RMS which can prove as a major limiting factor for encouraging early mobilization and reducing hospital stay. In ventilated patients, this rapid deterioration can potentially prolong dependency on the ventilator and further worsen the RMS, thereby worsening weaning of the patient. This study provides evidence regarding the importance of good glycaemic control and regular physical activity that may contribute to preventing deterioration of RMS which the individual may not notice at first, but may prove critical in acute settings.
An important limitation of this study is its low sample size. It restricts the clear interpretation of some analyses. This study emphasizes that RMS evaluation should be done routinely in patients who have had type 2 diabetes for more than 5 years. In the future, a cross-sectional observational study can be performed on diabetics with chronic respiratory disease and compared with a control group.
Conclusions | |  |
The present study concludes that RMS has a moderately strong, but significant association with glycemic control and physical activity of the individual. Duration of the disease may not have such an association with the maximal respiratory pressures.
Acknowledgment
We extend our sincere gratitude toward Dr. Shreerang Godbole and Dr. Sanjay Gandhi for their support in sample collection.
Financial support and sponsorship
Nil.
Conflicts of interest
There are no conflicts of interest.
References | |  |
1. | American Diabetes Association. Diagnosis and classification of diabetes mellitus. Diabetes Care 2014;37 Suppl 1:S81-90. |
2. | |
3. | Bianchi L, Volpato S. Muscle dysfunction in type 2 diabetes: A major threat to patient's mobility and independence. Acta Diabetol 2016;53:879-89. |
4. | Kelley DE, He J, Menshikova EV, Ritov VB. Dysfunction of mitochondria in human skeletal muscle in type 2 diabetes. Diabetes 2002;51:2944-50. |
5. | Fong DS, Aiello L, Gardner TW, King GL, Blankenship G, Cavallerano JD, et al. Retinopathy in diabetes. Diabetes Care 2004;27 Suppl 1:S84-7. |
6. | Shahbazian H, Rezaii I. Diabetic kidney disease; review of the current knowledge. J Renal Inj Prev 2013;2:73-80. |
7. | Nisar MU, Asad A, Waqas A, Ali N, Nisar A, Qayyum MA, et al. Association of diabetic neuropathy with duration of type 2 diabetes and glycemic control. Cureus 2015;7:e302. |
8. | Moningi S, Nikhar S, Ramachandran G. Autonomic disturbances in diabetes: Assessment and anaesthetic implications. Indian J Anaesth 2018;62:575-83.  [ PUBMED] [Full text] |
9. | Fuso L, Pitocco D, Longobardi A, Zaccardi F, Contu C, Pozzuto C, et al. Reduced respiratory muscle strength and endurance in type 2 diabetes mellitus. Diabetes Metab Res Rev 2012;28:370-5. |
10. | Wanke T, Formanek D, Auinger M, Popp W, Zwick H, Irsigler K. Inspiratory muscle performance and pulmonary function changes in insulin-dependent diabetes mellitus. Am Rev Respir Dis 1991;143:97-100. |
11. | Zineldin MA, Hasan KA, Salama Al-Adl A. Respiratory function in type II diabetes mellitus. Egypt J Chest Dis Tuberc 2015;64:219-23. |
12. | Kaminski DM, Schaan BD, da Silva AM, Soares PP, Plentz RD, Dall'Ago P. Inspiratory muscle weakness is associated with autonomic cardiovascular dysfunction in patients with type 2 diabetes mellitus. Clin Auton Res 2011;21:29-35. |
13. | Peirce NS. Diabetes and exercise. Br J Sports Med 1999;33:161-72. |
14. | Kabitz HJ, Sonntag F, Walker D, Schwoerer A, Walterspacher S, Kaufmann S, et al. Diabetic polyneuropathy is associated with respiratory muscle impairment in type 2 diabetes. Diabetologia 2008;51:191-7. |
15. | El-Azeem AA, Hamdy G, Saraya M, Fawzy E, Anwar E, Abdulattif S. The role of procalcitonin as a guide for the diagnosis, prognosis, and decision of antibiotic therapy for lower respiratory tract infections. Egypt J Chest Dis Tuberc 2013;62:687-95. |
16. | Shah SH, Sonawane P, Nahar P, Vaidya S, Salvi S. Pulmonary function tests in type 2 diabetes mellitus and their association with glycemic control and duration of the disease. Lung India 2013;30:108-12.  [ PUBMED] [Full text] |
17. | Shravya Keerthi G, Bandi HK, Suresh M, Preetham JK, Mallikarjuna Reddy N, Singh MS. Role of duration of diabetes on ventilatory capacities and expiratory flow rates in type 2 diabetes mellitus. J Biol Agric Healthc 2012;2:77-82. |
18. | Shravya Keerthi G, Singh MS, Bandi HK, Suresh M, Preetham JK, Mallikarjuna Reddy N. Deterioration of pulmonary functions in type 2 diabetes mellitus. IOSR J Pharm Biol Sci 2012;1:39-43. |
19. | Klein OL, Meltzer D, Carnethon M, Krishnan JA. Type II diabetes mellitus is associated with decreased measures of lung function in a clinical setting. Respir Med 2011;105:1095-8. |
20. | Anjana RM, Deepa M, Pradeepa R, Mahanta J, Narain K, Das HK, et al. Prevalence of diabetes and prediabetes in 15 states of India: Results from the ICMR-INDIAB population-based cross-sectional study. Lancet Diabetes Endocrinol 2017;5:585-96. |
21. | Kant R, Thapliyal V. Knowledge attitude and practice of type 2 diabetic patients in a tertiary care teaching hospital in India. Integr Food Nutr Metab 2015;2:131-5. [Doi: 10.15761/IFNM.1000115]. |
22. | Hussain R, Rajesh B, Giridhar A, Gopalakrishnan M, Sadasivan S, James J, et al. Knowledge and awareness about diabetes mellitus and diabetic retinopathy in suburban population of a South Indian state and its practice among the patients with diabetes mellitus: A population-based study. Indian J Ophthalmol 2016;64:272-6.  [ PUBMED] [Full text] |
23. | American Thoracic Society/European Respiratory Society. ATS/ERS Statement on respiratory muscle testing. Am J Respir Crit Care Med 2002;166:518-624. |
24. | Khan MI, Weinstock RS. Carbohydrates. In: McPherson RA, Pincus MR, editors. Henry's Clinical Diagnosis and Management by Laboratory Methods. 22 nd ed., Ch. 16. Philadelphia, PA: Saunders Elsevier; 2011. p. 210-25. |
25. | Nambiar VK, Ravindra S. Maximal respiratory pressures and their correlates in normal Indian adult population: A cross-sectional study. Int J Physiother Res 2015;3:1188-96. |
26. | Lee JS, Auyeung TW, Leung J, Kwok T, Leung PC, Woo J. The effect of diabetes mellitus on age-associated lean mass loss in 3153 older adults. Diabet Med 2010;27:1366-71. |
27. | Park SW, Goodpaster BH, Lee JS, Kuller LH, Boudreau R, de Rekeneire N, et al. Excessive loss of skeletal muscle mass in older adults with type 2 diabetes. Diabetes Care 2009;32:1993-7. |
28. | Park SW, Goodpaster BH, Strotmeyer ES, Kuller LH, Broudeau R, Kammerer C, et al. Accelerated loss of skeletal muscle strength in older adults with type 2 diabetes: The health, aging, and body composition study. Diabetes Care 2007;30:1507-12. |
29. | Sharma G, Goodwin J. Effect of aging on respiratory system physiology and immunology. Clin Interv Aging 2006;1:253-60. |
30. | Litonjua AA, Lazarus R, Sparrow D, Demolles D, Weiss ST. Lung function in type 2 diabetes: The Normative Aging Study. Respir Med 2005;99:1583-90. |
31. | Polla B, D'Antona G, Bottinelli R, Reggiani C. Respiratory muscle fibres: Specialisation and plasticity. Thorax 2004;59:808-17. |
32. | Häggmark T, Thorstensson A. Fibre types in human abdominal muscles. Acta Physiol Scand 1979;107:319-25. |
33. | Van Eetvelde BL, Cambier D, Vanden Wyngaert K, Celie B, Calders P. The influence of clinically diagnosed neuropathy on respiratory muscle strength in type 2 diabetes mellitus. J Diabetes Res 2018;2018:8065938. |
34. | Colberg SR, Sigal RJ, Yardley JE, Riddell MC, Dunstan DW, Dempsey PC, et al. Physical activity/exercise and diabetes: A position statement of the American Diabetes Association. Diabetes Care 2016;39:2065-79. |
35. | Akınoğlu B, Kocahan T, Özkan T. The relationship between peripheral muscle strength and respiratory function and respiratory muscle strength in athletes. J Exerc Rehabil 2019;15:44-9. |
36. | Ali IA, Elmutaz HT, Omer AM. Effect of diabetes mellitus on the respiratory muscle power in Sudanese diabetic patients. Int J Pulmonol Infect Dis 2018;1:1-5. |
[Table 1], [Table 2]
|