Open Access

Association of diabetic vascular complications with poor sleep complaints

  • Ling-Ling Meng1, 2,
  • Ying Liu1,
  • Rui-Na Geng1,
  • Yun-Zhao Tang1 and
  • Dai-Qing Li1Email author
Diabetology & Metabolic Syndrome20168:80

DOI: 10.1186/s13098-016-0195-8

Received: 29 July 2016

Accepted: 29 November 2016

Published: 8 December 2016

Abstract

Background

Literatures reported that poor sleep complaints were associated with a great deal of health outcomes. However, there are few studies on the association of poor sleep complaints with diabetic vascular complications.

Methods

Aiming on the association, a cross-sectional survey was conducted among 1220 diabetic patients in this study. Poor sleep complaints were composed of difficulty falling asleep, early final awakening, short sleep and long sleep. The diabetic vascular complications involved in the study were diagnosed according to the Standards of Medical Care in Diabetes (ADA 2016).

Results

Our findings indicated that short sleep remained independently associated with diabetic kidney disease (DKD) (OR > 1, P < 0.05) after the adjustments; long sleep independently associated with diabetic retinopathy (DR) (OR > 1, P < 0.05); early final awakening and short sleep independently associated with cardiovascular disease (OR > 1, P < 0.05); short sleep independently associated with peripheral arterial disease (OR > 1, P < 0.05); there was no association between poor sleep complaints and neuropathy (P > 0.05).

Conclusions

The study suggests that the poor sleep complaints were distinguishably associated with diabetic vascular complications. Clinicians should take poor sleep complaints into account in diabetes treatment.

Keywords

Poor sleep complaints Diabetic kidney disease (DKD) Neuropathy Diabetic retinopathy (DR) Cardiovascular disease (CVD) Peripheral arterial disease (PAD)

Background

In recent years, evidences from experimental and epidemiologic studies have demonstrated that poor sleep quality is associated with a great deal of health outcomes such as diabetes, cardiovascular disease, hypertension and obesity [14]. Poor sleep or sleep disturbances are well-known symptoms in type 2 diabetes, which have been noted by many researchers [57]. Diabetic vascular complications covered macrovascular complications including cardiovascular disease (CVD), peripheral arterial disease (PAD) and stroke, and microvascular complications such as diabetic kidney diseases (DKD), neuropathy and retinopathy [8]. Some literatures reported that sleep disturbances or obstructive sleep apnea is one of the risk factors causing CVD [911]. One study demonstrated that abnormal sleep patterns could influence the diabetic microvascular complications, in particular diabetic neuropathy [12]. Another study described a novel independent association between diabetic peripheral neuropathy and obstructive sleep apnea (OSA) [13]. Some studies proposed that OSA may contribute to development of DKD [14, 15]. Nishimura et al. concluded that there was an independent relationship between severity of sleep disordered breathing and retinopathy in patients with diabetes [16]. In addition, diabetic vascular complications were considered to have important impact on sleep quality, especially retinopathy and neuropathy [17].

So far, most studies related to sleep disorders and diabetic vascular complications have focused mainly on OSA. There are few studies on various poor sleep complaints with the complications systematically. The aim of the present study was to investigate the association between poor sleep complaints with the diabetic vascular complications in a population-based cross-sectional study.

Methods

Materials and subjects

We conducted a population-based cross-sectional study in Chinese adults with type 2 diabetes. Patients were recruited between January 2013 and January 2016 from Metabolic Diseases Hospital of Tianjin Medical University. Inclusion criterion was those patients who were diagnosed with type 2 diabetes according to the 1999 WHO diagnostic criteria for diabetes. Exclusion criteria included type 1 diabetes mellitus, pre-diabetes, diabetes with snoring, acute complications, severe kidney dysfunction, decompensated liver cirrhosis, heart failure with an ejection fraction <30% or NYHA classification >II. The diseases affecting sleep quality were also excluded, including restless leg syndrome, pruritic skin disorders, mental illness and thyroid disease. Consent was obtained and this study design was approved by the local ethics committee and was in accordance with the Declaration of Helsinki. Demographic data such as age and gender were collected and physical examinations including body mass index (BMI) and blood pressure were performed in the subjects. Glycosylated hemoglobin (HbA1C) was measured using standard high-performance liquid chromatography.

Definitions

The poor sleep complaints included difficulty falling asleep, early final awakening, short sleep and long sleep in this study. The frequency of difficulty falling asleep more than three times a week was defined difficulty falling asleep. The definition of early final awakening was consistent with the above. Sleep duration <6 h/night was defined as short sleep, and sleep duration >9 h/night was defined as long sleep.

Diabetic vascular complications covered microangiopathy such as DKD, DR and diabetic neuropathy, and macroangiopathy such as CVD and lower extremity PAD. DKD was defined as the presence of albuminuria [urinary levels of 24-h microalbumin (UMA) >30 mg/24 h] and/or an estimated glomerular filtration rate (eGFR) <60 mL/min/1.73 m2 [15]. eGFR was calculated using the four-variable Modification of Diet in Renal Disease equation (MDRD). Diabetic neuropathy diagnosis based on the results of nerve conduction study, which is a reliable, accurate and sensitive method to evaluate peripheral nerve function [18]. Patients’ clinical symptoms included hyperesthesia, paresthesia, motor weakness or polyradiculopathy [17]. DR was determined by experienced ophthalmologists using dilated indirect ophthalmoscopy or retinal photographs. Retinopathy was defined as at least two microaneurysms and/or retinal hemorrhage and/or other signs of retinal damage [19]. In this study, CVD includes coronary artery disease, hypertensive heart disease, and congestive heart failure (an ejection fraction ≥30% or NYHA classification ≤II) [9]. PAD was diagnosed according to the four typical clinical staging of symptoms, including lower extremity arterial pulses weakening or disappearing found in physical examination and change in lower extremity nutrition disorder or pale, combined with related risk factors such as diabetes, dyslipidemia, hypertension, age and so on. Patients with PAD were confirmed to have different degree of lower extremity artery occlusion using Vascular Ultrasonography. Dyslipidemia was defined that TG, LDL or VLDL was higher than the upper limit of normal or HDL was lower than the lower limit of normal.

Statistical analysis

All parametrically distributed date are expressed as mean ± standard deviation (SD). Categorical variables are shown as frequencies; Chi square test was used to analyze these variables. Two-sided values of P < 0.05 were considered as statistically significant. Multivariate logistic regression analysis was performed to assess the association between poor sleep complaints with vascular complications using odds ratio (OR) and 95% confidence intervals (CI). We adjusted for major confounding factors expected to affect these relationships (i.e. gender, age, smoking history, BMI, SBP, duration of diabetes, HbA1C and dyslipidemia). SPSS (Statistical Package for Social Sciences) for Windows 18.0 program was used for statistical analysis.

Results

Table 1 shows the association of poor sleep complaints and baseline characteristics with complications in participants with diabetes. The frequency of early final awakening and short sleep were higher in patients with DKD (56.7 vs. 47.7%, P = 0.005; 51.7 vs. 45.3%, P = 0.043). The frequency of early final awakening and long sleep were higher in patients with DR (55.6 vs. 47.7%, P = 0.011; 6.0 vs.2.2%, P = 0.002). Subjects with diabetic neuropathy had higher prevalence of difficulty falling asleep (30.3 vs. 24.0%, P = 0.020), early final awakening (54.3 vs. 43.7%, P = 0.000) and short sleep (49.5 vs. 43.2%, P = 0.037), respectively. The frequency of early final awakening and short sleep were higher in the diabetic patients with CVD (56.4 vs. 41.5%, P = 0.000; 53.0 vs. 38.6%, P = 0.000, respectively). The frequency of early final awakening and short sleep were higher in the diabetic patients with PAD (52.5 vs. 46.0%, P = 0.043; 49.5 vs. 40.9%, P = 0.007). The patients with DKD had higher BMI, SBP, DBP and HbA1C (P < 0.05), longer diabetes duration (P < 0.05), and higher rate of male (60.9 vs. 51.9%, P < 0.05) compared to those without DKD. The patients with DR were older than those without DR, and had higher rate of female (51.7 vs. 42.0%, P < 0.05), longer diabetes duration (P < 0.05), higher SBP (P < 0.05). The patients with neuropathy were older (P < 0.05), and had longer diabetes duration (P < 0.05), higher SBP (P < 0.05) and lower HbA1C (P < 0.05), compared to those without neuropathy. The patients with CVD were older (P < 0.05), and had higher BMI, SBP (P < 0.05), lower HbA1C (P < 0.05), longer diabetes duration (P < 0.05) compared to those without CVD. The patients with PAD were older (P < 0.05), and higher rate of male (56.2 vs. 48.4%, P < 0.05), longer diabetes duration (P < 0.05), lower HbA1C (P < 0.05) compared to those without PAD.
Table 1

Associations of poor sleep complaints and baseline characteristics with complications in subjects with type 2 diabetes mellitus

Microangiopathies

DKD

Retinopathy

Neuropathy

Absent

Present

P value

Absent

Present

P value

Absent

Present

P value

Complaints of poor sleep

 Difficulty fall asleep

232 (28.1)

98 (27.2)

0.778

208 (26.8)

124 (30.0)

0.250

110 (24.0)

224 (30.3)

0.020

 Early awake

394 (47.7)

204 (56.7)

0.005

370 (47.7)

230 (55.6)

0.011

200 (43.7)

402 (54.3)

0.000

 Short sleep <6 h

374 (45.3)

186 (51.7)

0.043

372 (47.9)

186 (44.9)

0.330

198 (43.2)

366 (49.5)

0.037

 Long sleep >9 h

22 (2.8)

18 (5.2)

0.057

16 (2.2)

24 (6.0)

0.002

16 (3.6)

24 (3.5)

1.000

 Male (%)

402 (51.9%)

212 (60.9%)

0.005

420 (58.0%)

194 (48.3%)

0.002

362 (52.5%)

258 (58.1%)

0.067

 Age (years)

56.13 ± 11.20

57.21 ± 11.63

0.149

55.75 ± 11.72

57.78 ± 10.41

0.004

52.64 ± 12.63

58.91 ± 9.63

0.000

 BMI (kg/m2)

26.17 ± 3.95

27.34 ± 3.71

0.000

26.53 ± 4.01

26.43 ± 3.77

0.690

26.59 ± 4.06

26.47 ± 3.83

0.639

 Diabetes duration (years)

8.18 ± 7.26

10.68 ± 7.38

0.000

7.19 ± 6.75

12.13 ± 7.54

0.000

5.48 ± 6.27

11.20 ± 7.23

0.000

 SBP (mmHg)

130.63 ± 14.01

136.06 ± 17.57

0.000

131.29 ± 14.8

134.65 ± 16.2

0.005

130.94 ± 15.4

133.15 ± 15.27

0.019

 DBP (mmHg)

80.01 ± 8.51

81.57 ± 9.75

0.007

80.42 ± 8.70

80.52 ± 9.32

0.870

80.90 ± 9.23

80.22 ± 8.19

0.212

 HbA1C (%)

8.96 ± 1.79

9.23 ± 1.70

0.021

9.05 ± 1.89

9.06 ± 1.51

0.927

9.29 ± 1.94

8.88 ± 1.62

0.000

Macroangiopathies

CVD

PAD

Absent

Present

P value

Absent

Present

P value

Complaints of poor sleep

 Difficulty fall asleep

132 (26.8)

202 (28.8)

0.472

90 (25.6)

256 (29.5)

0.183

 Early awake

204 (41.5)

396 (56.4)

0.000

162 (46.0)

456 (52.5)

0.043

 Short sleep <6 h

190 (38.6)

372 (53.0)

0.000

144 (40.9)

430 (49.5)

0.007

 Long sleep >9 h

18 (3.9)

22 (3.3)

0.624

10 (4.1)

30 (3.4)

0.562

 Male (%)

264 (57.6%)

354 (52.7%)

0.101

118 (48.4%)

496 (56.2%)

0.030

 Age (years)

52.20 ± 11.96

59.33 ± 9.90

0.000

51.71 ± 12.95

57.79 ± 10.43

0.000

 BMI (kg/m2)

25.99 ± 3.87

26.87 ± 3.91

0.000

26.44 ± 4.12

26.51 ± 3.85

0.828

 Diabetes duration (years)

7.27 ± 6.99

10.07 ± 7.49

0.000

6.61 ± 6.40

9.61 ± 7.56

0.000

 SBP (mmHg)

129.80 ± 14.3

133.93 ± 15.5

0.000

131.93 ± 16.4

132.38 ± 15.1

0.699

 SBP (mmHg)

80.65 ± 8.52

80.35 ± 9.18

0.589

80.76 ± 9.52

80.38 ± 8.76

0.572

 HbA1C (%)

9.42 ± 1.99

8.80 ± 1.55

0.000

9.48 ± 1.98

8.93 ± 1.69

0.000

Italics values are statistically significant

DKD diabetic kidney disease; CVD cardiovascular disease; PAD peripheral arterial disease; BMI body mass index; SBP systolic blood pressure; DBP diastolic blood pressure; PSQI Pittsburgh Sleep Quality Index; HbAlc glycosylated hemoglobin type A1c

Table 2 describes the effect of the demographics (gender, age and BMI) on the poor sleep complaints. The complaints were individually saved as dependent variable, and the demographics were saved as independent variables. Older patients were more likely to have these complaints, difficulty fall asleep [OR 1.015, 95% CI (1.002–1.027) P = 0.020], early awake [OR 1.045, 95% CI (1.032–1.057) P = 0.000] and short sleep [OR 1.015, 95% CI (1.004–1.026) P = 0.006]. The female were more vulnerable to have difficulty fall asleep [OR 1.764, 95% CI (1.350–2.307) P = 0.000]. The fatter participants were less trouble in falling asleep [OR 0.955, 95% CI (0.922–0.990) P = 0.012].
Table 2

Effect of the demographics on the poor sleep complaints

Demographics

Difficulty fall asleep

Early awake

Short sleep

Long sleep

OR (95% of CI)

P value

OR (95% of CI)

P value

OR (95% of CI)

P value

OR (95% of CI)

P value

Gender

1.764 (1.350–2.307)

0.000

1.079 (0.844–1.378)

0.545

1.199 (0.943–1.523)

0.138

1.559 (0.807–3.013)

0.186

Age

1.015 (1.002–1.027)

0.020

1.045 (1.032–1.057)

0.000

1.015 (1.004–1.026)

0.006

0.965 (0.940–0.991)

0.008

BMI

0.955 (0.922–0.990)

0.012

0.997 (0.966–1.028)

0.832

1.022 (0.992–1.054)

0.153

1.029 (0.952–1.113)

0.471

The poor sleep complaints were individually saved as dependent variable, and the demographics were saved as independent variable

Italics values are statistically significant

BMI body mass index

Table 3 shows the multivariate analysis for impact of poor sleep complaints on diabetic complications in the populations (model 1). In this model, diabetic vascular complications were individually put into dependent variables, and poor sleep complaints were individually put into independent variables. We adjusted for possible factors (age, gender, duration of diabetes, BMI, SBP, HbA1C, smoking history and dyslipidemia) in the regression analysis. Subjects with short sleep had a higher risk of developing DKD [OR 1.317, 95% CI (1.006–1.723) P = 0.045]; participants with long sleep had a higher risk of developing DR [OR 3.409, 95% CI (1.671–6.995) P = 0.001]; the risk of CVD was higher among the subjects with final early awakening [OR 1.348,95% CI (1.042–1.745) P = 0.023] and/or short sleep [OR 1.589, 95% CI (1.232–2.049) P = 0.000); the risk of PAD was higher among the subjects with short sleep [OR 1.343, 95% CI (1.024–1.762) P = 0.033); after adjustment of potential confounders, poor sleep complaints have no association with the development of neuropathy (P > 0.05).
Table 3

Multiple logistic regression analysis for impact of poor sleep complaints on vascular complications in subjects with type 2 diabetes mellitus (model 1)

Microangiopathies

DKD

Retinopathy

Neuropathy

OR (95% of CI)

P value

OR (95% of CI)

P value

OR (95% of CI)

P value

Poor sleep complaints

 Difficulty fall asleep

1.015 (0.749–1.376)

0.924

0.970 (0.726–1.296)

0.835

1.134 (0.841–1.529)

0.410

 Early wake

1.275 (0.966–1.682)

0.086

1.084 (0.831–1.413)

0.554

1.009 (0.771–1.320)

0.948

 Short sleep <6 h

1.317 (1.006–1.723)

0.045

0.774 (0.597–1.004)

0.054

1.152 (0.886–1.499)

0.291

 Long sleep >9 h

1.829 (0.893–3.746)

0.099

3.409 (1.671–6.995)

0.001

1.342 (0.636–2.828)

0.440

Macroangiopathies

CVD

PAD

OR (95% of CI)

P value

OR (95% of CI)

P value

Poor sleep complaints

 Difficulty fall asleep

0.901 (0.678–1.197)

0.472

1.091 (0.803–1.483)

0.577

 Early wake

1.348 (1.042–1.745)

0.023

0.967 (0.733–1.277)

0.815

 Short sleep <6 h

1.589 (1.232–2.049)

0.000

1.343 (1.024–1.762)

0.033

 Long sleep >9 h

0.947 (0.438–1.976)

0.947

1.034 (0.466–2.294)

0.934

The complications of diabetes were individually put into dependent variables, poor sleep complaints were individually put into independent variables, logistic regression analysis was adjusted for gender, age, duration of diabetes, smoking history, BMI (body mass index), SBP (systolic blood pressure), HbA1C (glycosylated hemoglobin type A1c) and dyslipidemia

Italics values are statistically significant

DKD diabetic kidney disease; CVD cardiovascular disease; PAD peripheral arterial disease

Table 4 shows the multivariate analysis for impact of diabetic complications on poor sleep complaints in the studied-populations (model 2). In the model, poor sleep complaints were individually put into dependent variables, and diabetic vascular complications were individually put into independent variables. We also adjusted for possible factors (age, gender, duration of diabetes, BMI, SBP, HbA1C, smoking history and dyslipidemia) in the regression analysis. CVD (OR 1.364, 95% CI 1.055–1.765, P = 0.018) was independent variable for early final awakening; DKD (OR 1.322, 95% CI 1.011–1.730, P = 0.042), CVD (OR 1.599, 95% CI 1.239–2.063, P = 0.000) and PAD (OR 1.365, 95% CI 1.041–1.790, P = 0.025) were independent variables for short sleep; DR (OR 3.660, 95% CI 1.762–7.601, P = 0.001) was independent variable for long sleep.
Table 4

Multiple logistic regression analysis for impact of vascular complications on poor sleep complaints in subjects with type 2 diabetes mellitus (model 2)

Variables

Difficulty fall asleep

Early wake

Short sleep

Long sleep

OR (95% of CI)

P value

OR (95% of CI)

P value

OR (95% of CI)

P value

OR (95% of CI)

P value

DKD

1.052 (0.778–1.422)

0.741

1.300 (0.986–1.713)

0.063

1.322 (1.011–1.730)

0.042

1.892 (0.945–3.788)

0.072

Retinopathy

0.983 (0.738–1.310)

0.909

1.073 (0.822–1.399)

0.605

0.780 (0.601–1.011)

0.061

3.660 (1.762–7.601)

0.001

Neuropathy

1.149 (0.854–1.545)

0.359

1.022 (0.782–1.338)

0.871

1.160 (0.893–1.509)

0.267

1.511 (0.694–3.289)

0.298

CVD

0.896 (0.675–1.190)

0.450

1.364 (1.055–1.765)

0.018

1.599 (1.239–2.063)

0.000

1.008 (0.486–2.089)

0.948

PAD

1.110 (0.816–1.509)

0.507

0.982 (0.746–1.294)

0.899

1.365 (1.041–1.790)

0.025

1.063 (0.478–2.361)

0.881

Poor sleep complaints were individually put into dependent variables, the complications of diabetes were individually put into independent variables, logistic regression analysis was adjusted for gender, age, duration of diabetes, smoking history, BMI (body mass index), SBP (systolic blood pressure), HbA1C (glycosylated hemoglobin type A1c) and dyslipidemia

Italics values are statistically significant

DKD diabetic kidney disease; CVD cardiovascular disease; PAD peripheral arterial disease

Discussion

Sleep disturbances, a condition with important for hypertension, diabetes and cardiovascular disease [2022], has been less researched for diabetes-associated vascular diseases. In addition, current studies related to sleep and diabetic vascular complications have focused mainly on OSA [15, 2325]. Our work differs from previous studies by offering exploration of the association between various poor sleep complaints and vascular complications in diabetes. Such research is particularly important, which are showing rapidly increasing prevalence of poor sleep complaints and diabetes in populations.

In this study, we described the effect of demographics on sleep complaints of the recruited participants. As expected, older patients were more likely to have these sleep complaints, difficulty fall asleep, early awake and short sleep; the female have a harder time falling asleep; the fatter participants were less trouble in falling asleep. From our data (Table 1), we found that age, gender, BMI, SBP, DBP, diabetes duration and HbA1C have impact on vascular disease distinguishably. Therefore, these factors were all adjusted in logistic regressions.

Interestingly, we demonstrated that early final awakening and short sleep both were risk factors for DKD from Chi square test. However, only short sleep persisted after the adjustment for a wide range of demographic and clinically relevant confounders in logistic regression analysis (model 1). Even though sleep disturbances or OSA has been proved as risk factor for development and progression of DKD [15, 26], short sleep may play great role in pathogenesis of DKD from this research. Meanwhile, we found that diabetic patients with DKD had shorter sleep duration in logistic regression (model 2), demonstrating that DKD and short sleep were interrelated closely.

Our data revealed early final awakening and long sleep were risk factors for DR from Chi square test. But only long sleep still was risk factors for DR after the adjustment in logistic regression (model 1). There was a literature reporting that short and long sleep was associated with high prevalence of DR in men and they speculated sleep deprivation may be involved in the pathogenesis of DR development [27]. In model 2, we found that DR patients had longer sleep; however, one report said the presence of diabetic retinopathy impairs the sleep quality, sleep latency, sleep duration and diurnal function in diabetic patients [17]. The proportion of participants with long sleep was significantly minor in the study, so we did not consider that long sleep was related to DR.

Tahrani et al. provided evidence that OSA is independently associated with diabetic peripheral neuropathy [13]. There are literatures also reporting that pain due to peripheral neuropathy causes nighttime awakening and this leads to disturbed sleep [17, 28, 29]. But there was no association between poor sleep complaints and diabetic neuropathy from the above regression analysis.

From the previous studies, sleep disturbances and/or short sleep were risk factors for CVD [9, 3032]. One report proposed that frequent awakenings and early morning awakening were not associated with a significantly increased risk of CVD mortality in older populations [33]. Nevertheless, the prevalence of early final awakening was more in patients with CVD than those without CVD; similar was the trend with short sleep in this study. In the regression analysis model 1, early final awakening and short sleep remained independently associated with CVD after adjustment. In addition, association of CVD with early final awakening and short sleep was showed in the model 2, which have not been reported in diabetes patients to the best of our knowledge.

We tried to assess the association between poor sleep complaints with lower extremity PAD in the type 2 diabetes patients. There was great difference between the patients with and without PAD in the prevalence of early final wakening and short sleep from Chi square test. In the model 1, only short sleep was risk factor for PAD after the adjustment. Diabetic patients with PAD had shorter sleep duration in logistic regression model 2 after adjustment. Even though a few current literatures revealed that prevalence of OSA is high in patients with PAD [34, 35], there is little literature reporting the association between poor sleep complaints and PAD.

Mechanisms of poor sleep complaints impacting morbidity of diabetic vascular complications have been speculated. Pathogenesis of vascular diseases in diabetes ascribe to oxidative stress, low-grade inflammation, endothelial dysfunction and so on [36]. First, poor sleep complaints could activate the autonomic nervous system and elevate the secretion of catecholamine, which can stimulate production of inflammatory mediators and could lead to metabolic imbalance [37]. Second, sleep disturbances and sleep fragmentation could activate pro-inflammatory transcription factors such as nuclear factor kappa B (NF-κ B), which is a key player in inflammatory and innate immune responses and a master regulator of inflammatory gene expression, and genes such as TNF-α or IL-8 that are important to the atherosclerotic process. Sleep disturbances may also aggravate oxidative stress which could sharpen endothelial dysfunction and increase insulin resistance [38].

The strength of this study was that it is the first time to assess the relationship between diabetic complications and poor sleep complaints using validated questionnaire roundly. Secondly, the studied-population was large and representative, so the results were worthy to be trusted and extrapolated. However, some limitations of this study should be taken attention. First, the adjusted-confounders were identical in the regression analysis, and this may lead to inaccurate adjustment for each diabetic complication. Second, it is difficult to draw an exact causal relationship between complications of diabetes and poor sleep complaints due to cross-sectional design of the study. In addition, some sleep complaints such as daytime sleepiness and frequent awakening were not assessed in the study, and we should perfect it in future study.

Conclusions

Poor sleep complaints were distinguishably associated with diabetic vascular complications. Larger prospective trails using the objective assessment by polysomnography are warranted to investigate the underlying mechanisms. Clinicians should pay more attention to poor sleep complaints for improving diabetes patients life quality.

Abbreviations

T2DM: 

type 2 diabetes mellitus

PSQI: 

Pittsburgh sleep quality index

DKD: 

diabetic kidney disease

DR: 

diabetic retinopathy

CVD: 

cardiovascular disease

PAD: 

peripheral arterial disease

Declarations

Authors’ contributions

LLM conceived of the study, analyzed the data, and drafted the manuscript. YL and RNG recruited the patients, collected the data, involved in the visiting of the patients. YZT and DQL conceived of the study, and participated in its design and coordination and helped to draft the manuscript. All authors read and approved the final manuscript.

Acknowledgements

We would like to thank Professor Jia-Rui Li for valuable suggestions to the study and revising the manuscript. We also thank Gang Wang for collecting part of the data.

Competing interests

We wish to confirm that there are no known competing interests associated with this publication and there has been no significant financial support for this work that could have influenced its outcome.

We confirm that the manuscript has been read and approved by all named authors and that there are no other persons who satisfied the criteria for authorship but are not listed. We further confirm that the order of authors listed in the manuscript has been approved by all of us.

We confirm that we have given due consideration to the protection of intellectual property associated with this work and that there are no impediments to publication, including the timing of publication, with respect to intellectual property. In so doing we confirm that we have followed the regulations of our institutions concerning intellectual property.

We further confirm that any aspect of the work covered in this manuscript that has involved human patients has been conducted with the ethical approval of all relevant bodies and that such approvals are acknowledged within the manuscript.

Availability of data and materials

This is just a part of our research, other research results have not been published, the data is not available to provide.

Consent for publication

Consents were obtained from theses participants to publish.

Ethics approval and consent to participate

Consent was obtained and this study design was approved by the local ethics committee and was in accordance with the Declaration of Helsinki.

Funding

Natural Science Foundation of China (Grant No. 81270891/H0713) and the foundation of Tianjin Science and Technology commission (Grant No. 15ZXHLSY00460, 15ZCZDSY00500, 16JCYBJC25700).

Open AccessThis article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated.

Authors’ Affiliations

(1)
Key Laboratory of Hormones and Development (Ministry of Health), Tianjin Key Laboratory of Metabolic Diseases, Metabolic Diseases Hospital and Tianjin Institute of Endocrinology, Tianjin Medical University
(2)
Third Division of Endocrinology Department, Hebei Cangzhou Central Hospital

References

  1. Grandner MA, Hale L, Moore M, Patel NP. Mortality associated with short sleep duration: the evidence, the possible mechanisms, and the future. Sleep Med Rev. 2010;14(3):191–203.View ArticlePubMedGoogle Scholar
  2. Lou P, Chen P, Zhang L, Zhang P, Chang G, Zhang N, Li T, Qiao C. Interaction of sleep quality and sleep duration on impaired fasting glucose: a population-based cross-sectional survey in China. BMJ Open. 2014;4(3):e004436.View ArticlePubMedPubMed CentralGoogle Scholar
  3. Cappuccio FP, Taggart FM, Kandala NB, Currie A, Peile E, Stranges S, Miller MA. Meta-analysis of short sleep duration and obesity in children and adults. Sleep. 2008;31(5):619–26.PubMedPubMed CentralGoogle Scholar
  4. Hoevenaar-Blom MP, Spijkerman AM, Kromhout D, van den Berg JF, Verschuren WM. Sleep duration and sleep quality in relation to 12-year cardiovascular disease incidence: the MORGEN study. Sleep. 2011;34(11):1487–92.PubMedPubMed CentralGoogle Scholar
  5. Sridhar GR, Madhu K. Prevalence of sleep disturbances in diabetes mellitus. Diabetes Res Clin Pract. 1994;23(3):183–6.View ArticlePubMedGoogle Scholar
  6. Chin K, Oga T, Takahashi K, Takegami M, Nakayama-Ashida Y, Wakamura T, Sumi K, Nakamura T, Horita S, Oka Y, et al. Associations between obstructive sleep apnea, metabolic syndrome, and sleep duration, as measured with an actigraph, in an urban male working population in Japan. Sleep. 2010;33(1):89–95.PubMedPubMed CentralGoogle Scholar
  7. Tang Y, Meng L, Li D, Yang M, Zhu Y, Li C, Jiang Z, Yu P, Li Z, Song H, et al. Interaction of sleep quality and sleep duration on glycemic control in patients with type 2 diabetes mellitus. Chin Med J. 2014;127(20):3543–7.PubMedGoogle Scholar
  8. Chiniwala N, Jabbour S. Management of diabetes mellitus in the elderly. Curr Opin Endocrinol Diabetes Obes. 2011;18(2):148–52.View ArticlePubMedGoogle Scholar
  9. Meng LL, Tang YZ, Ni CL, Yang M, Song HN, Wang G, Li YZ, Zhang M, Li DQ. Impact of inflammatory markers on the relationship between sleep quality and incident cardiovascular events in type 2 diabetes. J Diabetes Complications. 2015;29(7):882–6.View ArticlePubMedGoogle Scholar
  10. Seif F, Patel SR, Walia H, Rueschman M, Bhatt DL, Gottlieb DJ, Lewis EF, Patil SP, Punjabi NM, Babineau DC, et al. Association between obstructive sleep apnea severity and endothelial dysfunction in an increased background of cardiovascular burden. J Sleep Res. 2013;22(4):443–51.View ArticlePubMedPubMed CentralGoogle Scholar
  11. Seif F, Patel SR, Walia HK, Rueschman M, Bhatt DL, Blumenthal RS, Quan SF, Gottlieb DJ, Lewis EF, Patil SP, et al. Obstructive sleep apnea and diurnal nondipping hemodynamic indices in patients at increased cardiovascular risk. J Hypertens. 2014;32(2):267–75.View ArticlePubMedPubMed CentralGoogle Scholar
  12. Raman R, Gupta A, Venkatesh K, Kulothungan V, Sharma T. Abnormal sleep patterns in subjects with type II diabetes mellitus and its effect on diabetic microangiopathies: Sankara Nethralaya Diabetic Retinopathy Epidemiology and Molecular Genetic Study (SN-DREAMS, report 20). Acta Diabetol. 2012;49(4):255–61.View ArticlePubMedGoogle Scholar
  13. Tahrani AA, Ali A, Raymond NT, Begum S, Dubb K, Mughal S, Jose B, Piya MK, Barnett AH, Stevens MJ. Obstructive sleep apnea and diabetic neuropathy: a novel association in patients with type 2 diabetes. Am J Respir Crit Care Med. 2012;186(5):434–41.View ArticlePubMedPubMed CentralGoogle Scholar
  14. Nannapaneni S, Ramar K, Surani S. Effect of obstructive sleep apnea on type 2 diabetes mellitus: a comprehensive literature review. World J Diabetes. 2013;4(6):238–44.View ArticlePubMedPubMed CentralGoogle Scholar
  15. Tahrani AA, Ali A, Raymond NT, Begum S, Dubb K, Altaf QA, Piya MK, Barnett AH, Stevens MJ. Obstructive sleep apnea and diabetic nephropathy: a cohort study. Diabetes Care. 2013;36(11):3718–25.View ArticlePubMedPubMed CentralGoogle Scholar
  16. Nishimura A, Kasai T, Tamura H, Yamato A, Yasuda D, Nagasawa K, Okubo M, Narui K, Mori Y. Relationship between sleep disordered breathing and diabetic retinopathy: analysis of 136 patients with diabetes. Diabetes Res Clin Pract. 2015;109(2):306–11.View ArticlePubMedGoogle Scholar
  17. Ozturk ZA, Yesil Y, Kuyumcu ME, Savas E, Uygun O, Sayiner ZA, Kepekci Y. Association of depression and sleep quality with complications of type 2 diabetes in geriatric patients. Aging clinical and experimental Res. 2015;27(4):533–8.View ArticleGoogle Scholar
  18. Ko SH, Cha BY. Diabetic peripheral neuropathy in type 2 diabetes mellitus in Korea. Diabetes Metab J. 2012;36(1):6–12.View ArticlePubMedPubMed CentralGoogle Scholar
  19. Fong DS, Aiello L, Gardner TW, King GL, Blankenship G, Cavallerano JD, Ferris FL 3rd, Klein R. Diabetic retinopathy. Diabetes Care. 2003;26(1):226–9.View ArticlePubMedGoogle Scholar
  20. Cho EH, Lee H, Ryu OH, Choi MG, Kim SW. Sleep disturbances and glucoregulation in patients with type 2 diabetes. J Korean Med Sci. 2014;29(2):243–7.View ArticlePubMedPubMed CentralGoogle Scholar
  21. Calhoun DA, Harding SM. Sleep and hypertension. Chest. 2010;138(2):434–43.View ArticlePubMedPubMed CentralGoogle Scholar
  22. Redline S, Foody J. Sleep disturbances: time to join the top 10 potentially modifiable cardiovascular risk factors? Circulation. 2011;124(19):2049–51.View ArticlePubMedGoogle Scholar
  23. Buyukaydin B, Akkoyunlu ME, Kazancioglu R, Karakose F, Ozcelik HK, Erkoc R, Kart L. The effect of sleep apnea syndrome on the development of diabetic nephropathy in patients with type 2 diabetes. Diabetes Res Clin Pract. 2012;98(1):140–3.View ArticlePubMedGoogle Scholar
  24. Misra A, Shrivastava U. Obstructive sleep apnea and diabetic nephropathy. Diabetes Technol Ther. 2016;18(7):405–7.View ArticlePubMedGoogle Scholar
  25. Banerjee D, Leong WB, Arora T, Nolen M, Punamiya V, Grunstein R, Taheri S. The potential association between obstructive sleep apnea and diabetic retinopathy in severe obesity-the role of hypoxemia. PLoS ONE. 2013;8(11):e79521.View ArticlePubMedPubMed CentralGoogle Scholar
  26. Turek NF, Ricardo AC, Lash JP. Sleep disturbances as nontraditional risk factors for development and progression of CKD: review of the evidence. Am J Kidney Dis. 2012;60(5):823–33.View ArticlePubMedPubMed CentralGoogle Scholar
  27. Jee D, Keum N, Kang S, Arroyo JG. Sleep and diabetic retinopathy. Acta ophthalmologica. 2016. doi:10.1111/aos.13169.Google Scholar
  28. Luyster FS, Dunbar-Jacob J. Sleep quality and quality of life in adults with type 2 diabetes. Diabetes Educ. 2011;37(3):347–55.View ArticlePubMedPubMed CentralGoogle Scholar
  29. Zelman DC, Brandenburg NA, Gore M. Sleep impairment in patients with painful diabetic peripheral neuropathy. Clin J Pain. 2006;22(8):681–5.View ArticlePubMedGoogle Scholar
  30. Monahan K, Redline S. Role of obstructive sleep apnea in cardiovascular disease. Curr Opin Cardiol. 2011;26(6):541–7.View ArticlePubMedPubMed CentralGoogle Scholar
  31. Ryan S, Taylor CT, McNicholas WT. Systemic inflammation: a key factor in the pathogenesis of cardiovascular complications in obstructive sleep apnoea syndrome? Thorax. 2009;64(7):631–6.PubMedGoogle Scholar
  32. Nagai M, Hoshide S, Kario K. Sleep duration as a risk factor for cardiovascular disease- a review of the recent literature. Curr Cardiol Rev. 2010;6(1):54–61.View ArticlePubMedPubMed CentralGoogle Scholar
  33. Newman AB, Spiekerman CF, Enright P, Lefkowitz D, Manolio T, Reynolds CF, Robbins J. Daytime sleepiness predicts mortality and cardiovascular disease in older adults. The Cardiovascular Health Study Research Group. J Am Geriatr Soc. 2000;48(2):115–23.View ArticlePubMedGoogle Scholar
  34. Utriainen KT, Airaksinen JK, Polo O, Raitakari OT, Pietila MJ, Scheinin H, Helenius HY, Leino KA, Kentala ES, Jalonen JR, et al. Unrecognised obstructive sleep apnoea is common in severe peripheral arterial disease. Eur Respir J. 2013;41(3):616–20.View ArticlePubMedGoogle Scholar
  35. Pizarro C, Schaefer C, Kimeu I, Pingel S, Horlbeck F, Tuleta I, Nickenig G, Skowasch D. Underdiagnosis of obstructive sleep apnoea in peripheral arterial disease. Respiration. 2015;89:214–20.View ArticleGoogle Scholar
  36. Rask-Madsen C, King GL. Vascular complications of diabetes: mechanisms of injury and protective factors. Cell Metab. 2013;17(1):20–33.View ArticlePubMedPubMed CentralGoogle Scholar
  37. Hakim F, Gozal D, Kheirandish-Gozal L. Sympathetic and catecholaminergic alterations in sleep apnea with particular emphasis on children. Front Neurol. 2012;3:7.View ArticlePubMedPubMed CentralGoogle Scholar
  38. Dumitrascu R, Heitmann J, Seeger W, Weissmann N, Schulz R. Obstructive sleep apnea, oxidative stress and cardiovascular disease: lessons from animal studies. Oxid Med Cell Longev. 2013;2013:234631.View ArticlePubMedPubMed CentralGoogle Scholar

Copyright

© The Author(s) 2016

Advertisement