322 Article

Authors

H. Huang, Q. Guo, L. Li, S. Lin, Y. Lin, X. Gong, J. Yao, J. Liang, L. Lin, J. Wen, G. Chen

Affiliation

Department of Endocrinology, Fujian Provincial Hospital Key Laboratory of Endocrinology, Fujian Medical University, Fuzhou, China

Key words ▶ blood glucose ● ▶ pulmonary function ● ▶ type 2 diabetes mellitus ●

Abstract

received 09.12.2013 first decision 26.02.2014 accepted 17.03.2014 Bibliography DOI http://dx.doi.org/ 10.1055/s-0034-1372579 Exp Clin Endocrinol Diabetes 2014; 122: 322–326 © J. A. Barth Verlag in Georg Thieme Verlag KG Stuttgart · New York ISSN 0947-7349 Correspondence G. Chen, MD, PhD Postdoctor of Washington University School of Medicine in St. Louis Department of Endocrinology Fujian Provincial Hospital Fujian medical University Postal address: Box 4-704 92 Huqian Road Fuzhou Fujian China Tel.: + 86/135/09337 027 Fax: + 86/0591/87738 569 [email protected] H. Huang, MD, MS Department of Endocrinology Fujian Provincial Hospital Fujian medical University Postal address: 134 Dongjie Road Fuzhou Fujian China Tel.: + 86/136/96899 067 Fax: + 86/0591/87805 625 [email protected]



Background: Type 2 diabetes mellitus (T2DM) is a metabolic disease with debilitating effects on multiple organs. The alveolar-capillary network in the lung is a large microvascular unit which may be affected by T2DM-associated microangiopathy. Methods: This retrospective study investigated whether type 2 diabetes mellitus (T2DM) affected pulmonary function. Of the 584 patients enrolled in the study, 292 had T2DM and 292 did not. Forced expiratory volume in one second (FEV₁), forced vital capacity (FVC), maximum voluntary ventilation (MVV) and total lung capacity (TLC) are values as percent of predicted, as well as FEV₁/FVC ratio which were values measured. Results: FEV₁, FVC, FEV₁/FVC ratio, MVV, and TLC were significantly lower in T2DM than in non-T2DM (P-values < 0.010). Multiple linear regression analysis found that for the entire

Introduction



Type 2 diabetes mellitus (T2DM) effects multiple organs. Chronic hyperglycemia and microvascular lesions are the main cause of chronic complications in T2DM patients [1]. The alveolar-capillary network in the lung is a large microvascular unit which may be negatively affected by T2DM-associated microangiopathy [1, 2] possibly resulting from non-enzymatic glycosylation of collagen and elastin resulting in reduced lung [3]. A number of studies found that adults with T2DM have decreased lung function [4–14]; however, the findings have been inconsistent [15]. The association of T2DM with impaired lung function may be inversely related to blood glucose levels, length and severity of the disease, and obesity * The first 2 authors contributed equally to the study.

Huang H et al. Effect of Type 2 … Exp Clin Endocrinol Diabetes 2014; 122: 322–326

study population fasting plasma glucose levels was negatively associated with FEV₁, FVC, FEV₁/ FVC ratio and maximum voluntary ventilation (P-values < 0.030). Patients with T2DM were negatively associated with total lung capacity (P-values = 0.025). Multiple linear regression analysis found for patients with T2DM that fasting plasma glucose was negatively associated with FEV₁, FVC, FEV₁/FVC ratio and maximum voluntary ventilation (P-values < 0.020). In T2DM patient, height was negatively correlated with FEV₁ and FVC (all P-values < 0.020), triglycerides were negatively correlated with FEV₁/FVC ratio (P-values = 0.048), and creatinine was negatively correlated with total lung capacity (P-values = 0.017). Conclusions: In summary, T2DM is associated with impaired pulmonary function consistent with obstructive ventilation pattern and fasting plasma glucose is an independent risk factor of reduced pulmonary function.

[5, 8, 16]. It is not clear whether impaired pulmonary function associated with T2DM is due to restrictive or obstructive lung disease [10, 17–19]. In general, prior studies were limited by the small sample size (< 100 patients) and were case reports, survey based, or cross-sectional in design [12, 16, 20–22]. No prior studies have evaluated total lung capacity (TLC) in patients with T2DM. In the present study, we retrospectively collected pulmonary function of 584 patients (292 with T2DM and 292 non-T2DM controls), who had undergone elective surgery for routine preoperative preparation, to explore whether impaired pulmonary function was associated with T2DM. We evaluated pulmonary function by measuring forced expiratory volume in one second (FEV₁), forced vital capacity (FVC), FEV₁/ FVC, maximal voluntary ventilation (MVV) and total lung capacity (TLC).

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Effect of Type 2 Diabetes Mellitus on Pulmonary Function

Article 323 Materials and Methods



This was a retrospective study of patients who received pulmonary function testing for routine preoperative evaluation prior to elective surgery at Fujian Provincial Hospital from January 2011 to January 2012. Routine pulmonary function tests before elective surgery are required for all patients in our hospital. The protocol was approved by the hospital’s Institutional Review Board and was performed in accordance with the Declaration of Helsinki.

models. The independent variables with P < 0.05 in the descriptive analysis were included in the multiple linear regression models. The variance inflation factor (VIF) test was performed to verify the severity of multicollinearity in the multiple linear regression models. The weight coefficient β and 95 % confidence intervals (CIs) in multiple linear regression analysis were performed. All statistical assessments were 2-sided and evaluated at the 0.05 level of significant difference. Statistical analyses were performed with SPSS software version 18.0 (SPSS Inc., Chicago, IL, USA).

Study population

Data collection Data were collected retrospectively from patient’s hospital records and included pulmonary function (i. e., FEV₁, FVC, FEV₁/ FVC ratio, MVV and TLC), fasting plasma glucose, age, body weight, body height, systolic blood pressure, diastolic blood pressure, urea nitrogen, uric acid, creatinine, serum total cholesterol, triglyceride, and low- and high-density lipoprotein. For T2DM patients, information on duration of T2DM was also collected. Pulmonary function testing was performed in accordance with the criteria of the American Thoracic Society (ATS) [23] using American MedGraphics CPX pulmonary function measuring instrument (MedGraphics, St. Paul, MN, USA). Patients were asked to rest sufficiently before testing, and pulmonary function was performed while the patient was sitting in accordance with the hospital’s standard protocol. If a test was not adequate/successful, the test was repeated. The maximal value of an ideal curve was obtained, and the results were expressed as percent predicted. All calculations required for evaluating pulmonary function were determined using MedGraphics CPX pulmonary function device (Medical Graphics Corp.).

Statistical analysis Continuous variables were presented by mean and standard deviation (SD). Categorical variables were presented by count and percentage. Difference between the T2DM and the nonT2DM groups were compared using independent 2-sample t-test for the continuous variables, and Chi-square test or Fisher’s exact test with Yate’s correction if any cell number was < 5 or close to zero for the categorical variables. Multiple linear regression was used to analyze any association between pulmonary function and independent variables. All 5 pulmonary function results, (FEV₁, FVC, FEV₁/FVC ratio, MVV, and TLC), were separately considered as dependent variable in 5 different regression

Results



Of the 7 175 eligible patients, 3 162 were excluded due to being smokers, having chronic respiratory disease, COPD, asthma, cardiovascular disease, chest wall disease, acute respiratory infection within 2 weeks of study enrollment or other diseases that ▶ Fig. 1). Of the remaining influenced pulmonary function (● 4 013 patients, 407 were T2DM patients. 30 additional patients were excluded for having T2DM for < 1 year or having fasting plasma glucose ≥ 7.0 mmol/L but not having diagnosed T2DM. 407 non-T2DM patients were randomly selected to match the T2DM patients. T2DM patients were significantly older than non-T2DM patients (68.56 ± 9.91 vs. 62.36 ± 11.44, P < 0.001). To control for this difference, subjects were matched for gender and age ( ± 1year). After matching, 292 T2DM and 292 non-T2DM patients with similar age and gender and were used in the analysis. T2DM patients compared with non-T2DM patients had higher BMI, height, blood pressure, triglyceride levels, and fasting ▶ Table 1). T2DM patients plasma glucose (all P-values < 0.040) (● had lower pulmonary function and levels of plasma uric acid, total cholesterol, and LDL- and HDL-cholesterol (all P-val▶ Table 1). The 2 groups were similar in respect to ues < 0.010) (● plasma levels of urea, nitrogen and creatinine (all P-val▶ Table 1). ues > 0.050) (● Multiple linear regression analysis of results from the 5 pulmonary function test results across all patients indicated that fasting plasma glucose levels significantly correlated with FEV₁, FVC, ▶ Table 2). Height was FEV₁/FVC, and MVV (all P-values < 0.030) (● negatively associated with FVC (P-values = 0.045). T2DM was ▶ Table 2). No negatively associated with TLC (P-values = 0.025) (● other independent variables were significantly associated with pulmonary function. Multiple linear regression analysis found that fasting plasma glucose levels was negatively correlated with FEV₁, FVC, FEV₁/ FVC, and MVV in patients with T2DM (all P-values < 0.020) ▶ Table 3). Height negatively correlated with FEV₁ and FVC (all (● P-values < 0.020), triglyceride levels negatively correlated with FEV₁/FVC (P-values = 0.048), and creatinine levels negatively cor▶ Table 3). related with total lung capacity (P-values = 0.017) (● Triglyceride levels negatively correlated with MVV (Coefficient: − 3.389; 95 % CI: − 6.604, − 0.175; P-values = 0.039; data not shown). Other independent variables were not significantly associated with pulmonary function.

Discussion and Conclusions



This retrospective study investigated the association of T2DM with pulmonary function. We found that T2DM patients comHuang H et al. Effect of Type 2 … Exp Clin Endocrinol Diabetes 2014; 122: 322–326

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Patients were included if they underwent elective surgery defined as non-emergency surgery and surgeries that did not affect pulmonary function (e. g., surgery of the heart, lungs, thorax, chest etc.). T2DM was diagnosed according to fasting plasma glucose of ≥ 7.0 mmol/l on 2 separate tests or treatment with insulin or other hypoglycemic agents. T2DM and non-T2DM patients were excluded if they had a history of smoking, chronic respiratory diseases, chronic obstructive pulmonary disease (COPD), asthma, cardiovascular disease, such as heart failure, myocardial infarction, or stroke. Patients with chest wall disease, acute respiratory infection within 2 weeks of study enrollment, or tumors or other diseases that influenced pulmonary function were also excluded. Patients with only one fasting plasma glucose ≥ 7.0 mmol/L measurement, or self-reported type 1 diabetes, or other secondary diabetes were also excluded.

324 Article

Fig. 1 Patient disposition. T2DM, Type 2 diabetes mellitus.

Patient with elective surgery from 2011/1 to 2012/1 (n= 7175) Excluded (n= 3162) ○ Patients who being smokers, having chronic respiratory disease, COPD, asthma, cardiovascular disease, chest wall disease, acute respiratory infection within 2 weeks of study enrollment or other diseases that influenced pulmonary function

There were 407 T2DM patients and randomly selected 407 non-T2DM patients

T2DM patients (n= 407)

Non-T2DM patients (n= 407)

Excluded (n= 30) ○ Patients who diagnosed with T2DM < 1 year or having fasting plasma glucuso≥7.0 mmol/L but not being diagnosed with T2DM

T2DM patients (n=377)

Matched for gender and age (± 1year)

T2DM patients for analysis (n=292)

T2DM patients for analysis (n= 292)

pared with non-T2DM patients had significantly impaired pulmonary function, and multiple linear regression analysis indicated that plasma blood glucose level negatively correlated with pulmonary function. The fact that multiple regression analysis found that fasting plasma glucose levels was negatively associated with FEV₁, FVC, FEV₁/FVC, and MVV, but not TLC, leads us to hypothesize that the reduced lung function in patients with T2DM results from obstructive pattern of respiratory abnormality. This idea is consistent with a prior case-control study which found in patients matched in age, body mass index, and waist circumference that T2DM patients had lower FEV₁ and higher residual volume [19]. They also found that fasting plasma glucose was negatively associated with FEV₁ but positively associated with residual volume, suggesting that the impaired pulmonary function was that of obstructive ventilator pattern [19]. Results from the Research Center in Framingham, USA showed that T2DM patients not on therapy for diabetes had a greater reduction in FEV₁ than reduction in FVC resulting in a reduced FEV₁/FVC again consistent with pulmonary obstruction. In contrast, a meta-analysis found T2DM patients had lower FEV₁ and FVC but comparable FEV₁/FVC compared with non-T2DM Huang H et al. Effect of Type 2 … Exp Clin Endocrinol Diabetes 2014; 122: 322–326

patients, suggesting the impaired pulmonary function was typical of a restrictive ventilatory pattern [17]. In addition, a small cross-sectional study (N = 60 patients) found decreased FVC and FEV₁ and normal FEV₁/FVC in T2DM patients compared with non-diabetic subjects suggesting an association of T2DM with restrictive respiratory pattern [18]. Further experiments are necessary to evaluate if diabetes results in restrictive or obstructive impairment of pulmonary function. Similar to our study, several prior studies found T2DM patients had lower FEV₁ compared with non-T2DM patients, and fasting plasma glucose was negatively correlated with FEV₁ and FVC [5, 12]. The Third National Health and Nutrition Examination Survey in the USA showed that pulmonary function in T2DM patients with good glucose control was better than that of their counterparts with poor glucose control [16]. A prospective study also indicated that, among patients with pulmonary cystic fibrosis, T2DM patients had significantly poorer pulmonary function when compared with non-T2DM patients [24]. There are several possible molecular mechanisms by which diabetes may affect pulmonary function, including loss of lung elasticity in T2DM patients possibly resulting from non-enzymatic

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Assessed for eligibility (n= 4013)

Article 325

Table 1 Basic characteristics of patients with and without type 2 diabetes.

age (years) 1 gender 2 male female BMI (kg/m2) 1 height (cm) 1 systolic blood pressure (mmHg) 1 diastolic blood pressure (mmHg) 1 urea nitrogen (mmol/l) 1 uric acid (umol/l) 1 ureatinine (umol/l) 1 TC (mmol/l) 1 TG (mmol/l) 1 LDL-cholesterol (mmol/l) 1 HDL-cholesterol (mmol/l) 1 FPG (mmol/l) 1 duration of diabetes (year) 1 FEV₁ ( %) 1† FVC ( %) 1† FEV₁/FVC ratio 1 MVV ( %) 1† TLC ( %) 1†

T2DM

Non-T2DM

(n = 292)

(n = 292)

P-value

66.85 ± 9.56

66.57 ± 9.43

181 (61.99) 111 (38.01) 23.94 ± 3.81 161.50 ± 8.98 136.00 ± 15.34 74.83 ± 9.39 5.64 ± 1.90 259.96 ± 113.78 73.69 ± 22.47 4.46 ± 1.12 1.62 ± 1.15 2.64 ± 0.87 1.05 ± 0.39 8.55 ± 2.85 5.23 ± 5.55 89.14 ± 17.65 85.02 ± 12.65 82.92 ± 9.13 83.72 ± 20.89 98.24 ± 11.55

181 (61.99) 111 (38.01) 22.10 ± 3.31 159.93 ± 8.51 123.79 ± 14.04 72.88 ± 8.26 6.15 ± 5.45 300.08 ± 105.42 79.07 ± 42.77 4.73 ± 1.18 1.34 ± 0.78 3.01 ± 1.02 1.18 ± 0.38 5.29 ± 0.71 NA 93.65 ± 13.34 88.33 ± 8.70 85.06 ± 8.22 90.63 ± 19.33 100.97 ± 10.33

0.724 1.000

< 0.001* 0.031* < 0.001* 0.008* 0.138 < 0.001* 0.058 0.005* 0.001* < 0.001* < 0.001* < 0.001* NA 0.001* < 0.001* 0.003* < 0.001* 0.003*

P < 0.05 indicates a significant difference between the 2 groups 1

Values are expressed as mean ± SD and P-values are based on independent 2 sample t-test

2

Values are expressed as n ( %) and P-values are based on Chi-square test



Values are expressed as a percentage of the predicted value

BMI, body mass index; FEV₁, forced expiratory volume in one second; FPG, fasting plasma glucose; FVC, forced vital capacity; HDL, high-density lipoprotein; LDL, low-density lipoprotein; MVV, maximum voluntary ventilation; NA, no data available; T2DM, type 2 diabetes mellitus; TC, total cholesterol; TG, triglyceride; TLC, total lung capacity

Table 2 Multiple linear regression analysis of 5 pulmonary functions among all patients (N = 584). Dependent variables (for an increase of 1 %)

Statistically significant independent variables†

FEV₁ FVC

FPG FPG height FPG FPG patients with T2DM

FEV₁/FVC ratio MVV TLC

Coefficient (95 % CI) − 0.914 ( − 1.555, − 0.572 ( − 1.018, − 0.106 ( − 0.210, − 0.484 ( − 0.841, − 0.961 ( − 1.793, − 2.907 ( − 5.449,

− 0.272) − 0.127) − 0.002) − 0.127) − 0.129) − 0.364)

P-value 0.005 0.012 0.045 0.008 0.024 0.025

† Independent variables include BMI, height, SBP, DBP, urea nitrogen, uric acid, creatinine, TC, TG, LDL-cholesterol, HDL-cholesterol, FPG, and T2DM status T2DM, type 2 diabetes; BMI, body mass index; CI, confidence interval; DBP, diastolic blood pressure; FPG, fasting plasma glucose; FEV₁, forced expiratory volume in one second; FVC, forced vital capacity; HDL, high-density lipoprotein; LDL, low-density lipoprotein; MVV, maximum voluntary ventilation; SBP, systolic blood pressure; TC, total cholesterol; TG, triglyceride; TLC, total lung capacity; NS, not significant

Table 3 Multiple linear regression analysis of 5 pulmonary functions among T2DM patients (n = 292). Dependent variables (for an increase of 1 %) FEV₁ FVC FEV₁/FVC ratio MVV TLC †

Statistically significant independent variables† FPG height FPG height FPG TG FPG creatinine

Coefficient (95 % CI) − 1.178 ( − 1.961, − 2.698 ( − 0.562, − 0.712 ( − 1.276, − 0.217 ( − 0.387, − 0.580 ( − 0.985, − 1.170 ( − 2.331, − 1.271 ( − 2.208, − 0.090 ( − 0.163,

− 0.395) − 0.088) − 0.149) − 0.046) − 0.175) − 0.009) − 0.334) − 0.016)

P-value 0.003 0.007 0.013 0.013 0.005 0.048 0.008 0.017

Independent variables include BMI, height, SBP, DBP, urea nitrogen, uric acid, creatinine, TC, TG, LDL-cholesterol, HDL-cholesterol, and FPG

BMI, body mass index; CI, confidence interval; DBP, diastolic blood pressure; FPG, fasting plasma glucose; FEV₁, forced expiratory volume in one second; FVC, forced vital capacity; HDL, high-density lipoprotein; LDL, low-density lipoprotein; MVV, maximum voluntary ventilation; SBP, systolic blood pressure; TC, total cholesterol; TG, triglyceride; TLC, total lung capacity

Huang H et al. Effect of Type 2 … Exp Clin Endocrinol Diabetes 2014; 122: 322–326

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Variables

glycosylation of the connective tissue [12]. In addition, T2DM patients have insufficient pulmonary surfactant, which may influence airflow stability and airway diameter, resulting in pulmonary function impairment [12]. T2DM patients also have reduced muscle function and polyneuropathy which can reduce pulmonary function [25, 26]. A limitation of this study was that it was retrospective in design. In addition, we did not evaluate the influence of other diabetesassociated complications such as retinopathy, nephropathy, or neuropathy with pulmonary function. In our study, the mean duration of T2DM was about 5 years, which is relatively short. Thus, we postulate that the proportion of severe complications of T2DM might be lower than that seen in other T2DM studies. We did not evaluate the influence of potential changes in pulmonary diffusion which can be reduced in T2DM patients [3]. In addition, patients required elective surgery to be considered for the study which may have biased the results. In summary, we found that T2DM correlated with impaired pulmonary function. Blood glucose was an independent risk factors of reduced pulmonary function. Our findings emphasize that more attention should be paid to pulmonary function in T2DM patients, especially in older patients. Epidemiological studies with a large sample size and long term follow-up are required to elucidate the mechanisms underlying impaired pulmonary function in T2DM patients.

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326 Article

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Effect of type 2 diabetes mellitus on pulmonary function.

Type 2 diabetes mellitus (T2DM) is a metabolic disease with debilitating effects on multiple organs. The alveolar-capillary network in the lung is a l...
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