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Abstract:

OBJECTIVE: 

Morning blood pressure surge (MBPS) is an independent predictor of cardiovascular events. However, little is known about the association between glycemic control and MBPS, and its effect on vascular injury in patients with type 2 diabetes mellitus (T2DM). The current study examined the association between glycemic control and MBPS, and the involvement of MBPS in the development of vascular dysfunction in Type 2 DM patients.
MATERIAL AND METHODS

122 consecutive Type 2DM out-patients from the department of Cardiology and endocrinology were enrolled in this study. We did MBPS in Type 2DM patients 85 male (69.7%) and 37 female (30.3%) ; mean age  60.1� 9.39; (n = 122) using 24-h ambulatory blood pressure monitoring, and assessed vascular function by brachial artery flow-mediated dilation (FMD) and nitroglycerin-mediated dilation (NMD).
RESULTS The correlation between MBPS and various clinical variables were examined by single regression analysis in all subjects. MBPS showed significant and positive correlation with Pulse Rate (p= 0.01), FBS (p=0.002), PPBS (p=0.05) .To further confirm the association of insulin resistance with MBPS in Type2DM patients, we examined the correlation between HOMA-IR, and MBPS in patients who were not taking insulin, no significant association of MBPS (p value 0.41) HOMA-IR ,ACE/ARB (p=0.07) was observed. We examined the relationship between MBPS and vascular injury by measuring endothelium-dependent FMD and endothelium independent NMD in T2DM patients. Among the various traditional risk factors for atherosclerosis like DM duration (p=0.04), FMD (p=0.036) emerged as significant factors. HOMA-IR was negative correlation with FMD. ROC curve was constructed for the best cut off value of MBPS, at 19.67 mmhg, which has sensitivity 43.5%, Specificity 90%, Positive Predictive value 85.71%, Negative Predictive value 62%.

CONCLUSIONS

The current study demonstrated that poor glycemic control and insulin resistance have predictive value for the occurrence of MBPS in Type 2 DM patients, which is  significantly associated with endothelial dysfunction.
























Introduction:
Many studies in the past decade have demonstrated diurnal variation in the onset of acute cardiovascular disorders in hypertensive patients, such as acute coronary syndrome, and ischemic and hemorrhagic stroke occurring in the morning (6:00 AM to noon) after a nadir in these events during the night. Blood pressure (BP) falls during the night because of the reduction of sympathetic activity in sleep and then increases steeply in the morning when the subject awakes and resumes his/her daily activities. This increase occurs together with a peak incidence of cerebral and cardiac events in the morning hours. Moreover, a recent prospective study suggests that higher morning BP surge (MBPS) might be an independent risk factor of atherosclerotic events beyond ambulatory BP and nocturnal BP falls. The molecular mechanisms associating MBPS peak and vulnerable atherosclerotic plaque are not clear, although inflammation, which plays a central role in the cascade of events that result in plaque erosion and fissuring also were related to MBPS. 
 
Patients with diabetes mellitus (DM) tend to exhibit accelerated arteriosclerosis and are consequently at higher risk of cardiovascular disease (CVD), including stroke and coronary heart disease. DM is often complicated with other co-morbidities that contribute to increased risk of CVD (i.e., hypertension, chronic kidney disease, and dyslipidemia).

It has been increasingly recognized that the early morning blood pressure surge (MBPS) (i.e., the increase in blood pressure [BP] that occurs during the period from night to early morning), which can be detected by ambulatory BP monitoring (ABPM), provides a clinically relevant measure to predict CVD risk independent of age and 24-h systolic BP (SBP). This concept is supported by data indicating that cerebral and cardiac events occur most often in the morning. It is possible that inadequate glycemic control or the occurrence of insulin resistance activate sympathetic activity, which leads to MBPS in DM patients. Furthermore, hypertensive patients with exaggerated MBPS exhibit elevated levels of macrophages, T-lymphocytes, and tumor- necrosis factor alpha in atherosclerotic plaques obtained from the carotid artery compared with those without exaggerated MBPS, suggesting an association between MBPS and vascular injury in hypertensive patients. Taken together, these results suggest that poor glycemic control could accelerate vascular injury in DM patients by causing MBPS.
In recent years, flow mediated dilatation (FMD) has become a popular technique in cardiovascular medicine and clinical physiology, as evidence has occurred that depressed FMD is an independent prognostic index of incident and recurrent cardiovascular events which adds predictive value to the established risk factors. 
The FMD measurement has gained growing interest as several studies indicated that a decreased FMD response predicts arterial disease progression with intimal thickening and increased cardiovascular mortality. Several cardiovascular risk factors have been shown to lead to acute and chronic FMD impairment.
Insulin Resistance (IR) is defined as a disorder of insulin mediated glucose release. Although, hyperinsulinema itself is a marker for IR, it can also be determined using methods such as hyperglycemic-euglycemic clamp technique, intravenous glucose tolerance test, and insulin compression test. Since these techniques are complicated and difficult to utilize and there are some difficulties in the daily routine usage and application to wide populations, easier indexes which were depended on clinical measurements were improved. HOMA-IR is well correlated with hyperglycemic-euglycemic clamp technique which was accepted to determine the insulin sensitivity as a valuable standard. It has been shown that insulin has various vascular benefits, like increasing the nitric oxide (NO) activity, releasing NO synthesis gene expression, and causing vasodilatation. As it is known that insulin increases the endothelium dependent dilatation this effect is impaired with the presence of IR.                   
It is known that endothelial dysfunction has a close relation with hyperglycemia, hypertension, dyslipidemia, fibrinolysis, obesity, and insulin resistance (IR), has a major role in progression of micro-vascular complications. 
In this study, we evaluated 1) the association of insulin resistance and glycemic control with MBPS and 2) the association between MBPS and vascular endothelial dysfunction as assessed by endothelium-dependent flow-mediated dilation (FMD) and nitroglycerin mediated dilation (NMD) in type 2 DM (Type 2 DM) patients.
Material and Methods:
Study Patients:
One twenty two (122) consecutive out-patients from the Department of Cardiology and endocrinology were enrolled in this study during the period of March 2014 to November 2014. Ethical committee approval and informed consent from each patient were obtained. Exclusion criteria were  the presence of clinically evident micro/macro vascular complications of diabetes i.e., the clinical or ECG evidence of CAD, past or present episodes of stroke, and / or TIA, clinical evidence of peripheral vascular disease, features suggestive of diabetic retinopathy on fundus examination, presence of overt proteinuria or serum creatinine > 2mg/dl, clinical evidence of diabetic neuropathy, associated co-morbid illness which is likely to influence the endothelial function like congestive cardiac failure, liver diseases, chronic infections, renal diseases.

Procedural Protocol:

Clinical examination included blood pressure measurement, cardiovascular examination, and body-mass index (BMI) measurement. Biochemical assessment included fasting blood sugar (FBS), post-prandial blood sugar (PPBS) levels and comprehensive lipid profile. Plasma glucose, insulin and lipid estimation were done after an overnight fast of 12 h. Homeostasis model assessment ratio (HOMA-IR) which was calculated as fasting insulin (�U/ml) multiplied by fasting plasma glucose (FPG) (mg/dl) and divided by 405, was used to assess the insulin sensitivity in the subjects without insulin therapy. Diabetic Mellitus defined as per ADA criteria.
Determination of vascular function with ultrasound:
The ultrasound method for measuring endothelium dependent and endothelium independent arterial dilatation has been used as described previously. The brachial artery diameter was measured on B-mode ultrasound images, with the use of a 7.5 MHz linear array transducer with image point HX Ultra sound Equipment (iE33 2-D Echo, Philips Ultrasound Bothell, Washington USA). The right brachial artery was studied in all the subjects. Brachial artery endothelial function was studied after the subject had abstained from alcohol, caffeine, and smoking for 8 hours. Scans were obtained with the subject at rest, during reactive hyperaemia and again at rest. The subjects were asked to lie quietly for at least 10min before the first scan. The brachial artery was scanned in longitudinal section 2 cm above the elbow, the centre of the artery was identified when the clearest picture of the anterior and posterior intimal layers was obtained. The transmit (focus) zone was set to the depth of the near wall, because of the greater difficulty in evaluating the "M" line (the interface between the media and adventitia) of the near wall as compared with that of the far wall. Depth and gain settings were set to optimize images of the interface between the lumen and the arterial wall, and the images were magnified. Settings for operating the machine were not changed during the study.
When a satisfactory transducer position was found, the skin was marked and the arm was kept in the same position throughout the study. A resting scan was obtained. The arterial diameter was measured. Increased flow was then induced by the inflation of a sphygmomanometer cuff placed around the forearm (distal to the scanned part of the artery) to a pressure of 200 mmHg for 5 minutes followed by release. A second scan was performed continuously of 30 seconds, 60 seconds and 90 seconds after deflation of the cuff.  The diameter of the artery was measured at the peak of R wave (Corresponding to end diastole). 
Flow-mediated dilatation was calculated, and the average result of the three observations was recorded. Flow-mediated dilatation results are presented as the percent change diameter post ischemia (d2) � diameter baseline (d1) divided by diameter baseline (d1) multiplied by 100. Severe endothelial dysfunction was defined as FMD <5.5% as has been described. 15 minutes was allowed for vessel to recovery and then a further resting scan was taken, then sublingual glycerol tri nitrate (GTN-200mics puff) was administered and 4 minutes after, the last scan was done. ECG was monitored throughout the scans and artery diameter measured at the peak of R wave (corresponding to end diastole). An average of 3 values was taken for each measurement. None of these patients were treated with dietary therapy alone. BMI was calculated as body weight (in kilograms)/height (in square meters).

BP Measurements and Analysis of ABPM Data

Non invasive ABPM was performed in a hospital setting with an automated system (BR-102 plus SCHILLER, Switzerland) that records BP using the auscultatoric and oscilliometric method and pulse rate every 1 hour for 24 h, as described previously. Awake and sleep time were defined on the basis of written diaries recorded by the patients during the ABPM. The morning BP was defined as the average of the four BP values obtained during the first 2 h after waking up. The lowest BP was defined as the average of the three BP readings centred around the lowest night time reading (i.e., the lowest night time reading plus the readings immediately before and after). The Morning Blood Pressure Surge (MBPS) was calculated as the morning Systolic Blood Pressure (SBP) minus the lowest SBP as reported previously. Smoothness Index is defined as the homogeneity of the blood pressure reduction induced by antihypertensive treatment over the 24 hours.
Statistical Analysis:
Statistical software: The Statistical software namely SAS 9.2, SPSS 15.0, Stata 10.1, Med Calc 9.0.1, Systat 12.0 and R environment ver. 2.11.1 were used.
Statistical Methods: Descriptive and inferential statistical analysis has been carried out in the present study. Results on continuous measurements are presented as mean ( SD (min-max), median (limits of observed values) was used for the DM duration, HOMA-IR, urine micro albumin (UMA), Urine Albumin to Creatinine ratio (UACR). Unpaired samples were analyzed nonparametrically using Mann Whitney U test. Correlation coefficients were calculated by simple and multiple regression analyses. Receiver-operating Characteristic (ROC) Curves was constructed to access the best MBPS for the identification of the presence of vascular dysfunction. P Values < 0.05 were considered statistically significant.  
Results: 

 The clinical characteristics of 122 patients were summarized in Table 1. Out of 122 patients, 85(69.7%) were male and  37(30.3%) were female patients. The duration of diabetes was 0.22 � 36 years, Smokers were 20 (16.39%), Alcoholics were 14(11.47%), 13 patients were hypothyroid (10.8%), Post Menopausal women were 34 (30.6%). Out of 122 patients 51 (41.8%) on insulin therapy, 111(91%) on Metformin, 47 (38.5%) on Glimipride, 6 (4.9%) on Vildagliptin and 26 (21.3%) on Voglibose, 17 (13.9%) on Saxagliptin. 81 (66.4%) were on �-blockers, 89 (73%) on ACE/ARB, 44 (36.1%) on Calcium Channel Blockers (CCB), 40 (32.8%) additionally using Diuretics along with other drugs. No significant difference existed in MBPS between patients receiving treatment and not receiving treatment with �-blockers (p value 0.23), ACE/ARBs (p value 0.63) or CCBs (p value 0.38), Diuretics (p value 0.51) and statins.
In this study out of 122 patients, Morning Surge was present in 108 (88.52%) absent in 14 (11.46%) patients, Smoothness Index was 0.73 � 0.10 (p=0.039), impaired HOMA-IR (3 and above) was observed in 37 (48.68%) patients. Severely impaired FMD i.e., < 5.5 was observed in 69 (57.02%) patients. MBPS was significantly lower in patients with normal FMD than in those with impaired FMD (p value 0.08),extreme dippers (pvalue0.00005). FMD was not significantly lower in , patients receiving �-blockers(p value 0.07), ACE/ARB (p value 0.75), CCB (p value 0.34), Diuritics (p value 0.62) and Statins (p=0.68) also did not show significant difference between normal and severely impaired FMD.
 Correlations of the Clinical Variables with MBPS in T2DM Patients
On Univariate Analysis MBPS shows significant and positive co relation with Pulse Rate (p value 0.001), FBS (p value 0.002), PBBS (p value 0.002), Negative dippers (p value 0.000) and FMD (p value 0.035) NMD(p value 0.17). All the variables which are statistically significant on univariate analysis further analysed by multivariate regression analysis ,(Table 2) showing negative co-relation with BMI (r = -0.12, B =0.88), HBA1c (r = -0.61, B =0.54), FMD (r = -0.12, B =0.88) and ACE/ARB (r = - 3.12, B =0.04). We next examined the relationship between MBPS and vascular injury by measuring endothelium-dependent FMD and endothelium independent NMD in T2DM patients. Duration of diabetes (p value 0.04), pulse rate (p value 0.04) and extreme dipper (p value 0.00005) were statistically significant. By regression Analysis there was a negative Co-relation with FMD and MBPS (p =0.03)    Figure 1. But there is no correlation with NMD(p value 0.28).
To further confirm the association of insulin resistance with MBPS in T2DM patients, we examined the correlation between HOMA-IR, an established marker of insulin resistance and MBPS in DM patients who were not on insulin, no stastically significant difference was found, there is also no correlation with cortisol levels and MBPS. 

ROC curve was constructed for the best cut off value of morning blood pressure surge at 19.67 mm hg has sensitivity 43.5%, specificity 90%, positive predictive value 85.71%, negative predictive value 62%.(figure 2).
Discussion
In the current study, we demonstrated that MBPS was significantly and independently associated in a negative fashion with FMD, but not NMD. These data suggested that poor glycemic control or insulin resistance is associated with the occurrence of MBPS in Type 2 DM patients, which is associated with the development of endothelial dysfunction in these patients. It was suggested that triglyceride level might provide an index for insulin resistance, we did the correlations of the established markers of insulin resistance, HOMA-IR with MBPS, for diabetic patients not receiving insulin therapy. But statictically  significant correlation between HOMA-IR and MBPS was not observed in this study.
MBPS is considered to result from increased activities of the sympathetic nervous system, the renin angiotensin system, and the hypothalmic-adrenalpituitary (HPA) axis during the latter half of the sleep cycle. Because insulin resistance is known to stimulate sympathetic activity by affecting the metabolism of adipocytokines, such as leptin, the association of TG level and HOMA-R with MBPS might be explained through increased sympathetic activity by insulin resistance. Furthermore, it remains possible that insulin-stimulated re-absorption of sodium at the renal tubule might contribute to the development of MBPS. The activity of the HPA axis shows a clear circadian rhythm exhibiting a rapid rise during the latter half of the sleep cycle, with the highest levels occurring in the early morning in parallel with the time course change of BP, suggesting the involvement of a diurnal change in HPA axis in the generation of MBPS. It was reported that Type 2DM patients exhibit higher baseline levels of serum cortisol. Therefore, it is possible that insulin resistance might make the association with MBPS significant by its stimulatory effect on HPA axis early in the morning. Chronic hyperglycemia is reported to cause endothelial dysfunction by accumulating advanced glycosylation end products in the vascular wall, resulting in the development of vascular injury, hypertensive and diabetic patients exhibit higher levels of plasma advanced glycosylation end products than their non-hypertensive counterparts.
Impaired FMD of the brachial artery, which is mainly caused by the loss of endothelium-derived nitric oxide (NO), has been established as a relevant marker for endothelial dysfunction. MBPS appears to play the most important role in the development of endothelial dysfunction, as reflected by the strongest association of MBPS with CVD risk. Because MBPS might acutely increase mechanical stretch on endothelial cells, it augmented the production of endothelium-derived superoxide, resulting in the inactivation of NO. Indeed, it was reported that marked fluctuations in BP in sino aortic denervated rats significantly impaired endothelial function by reducing acetylcholine-induced NO release from aortic rings. In the current study, HbA1c level correlated significantly in a negative manner with FMD in multivariate regression analyses, including MBPS as an independent variable, suggesting the intimate involvement of MBPS in the association of HbA1c level and FMD. The previous study, demonstrating the association of a blunted dip in BP during sleep with endothelial dysfunction in Type 2DM patients, might support our data suggesting MBPS as an important factor to accelerate vascular damage in Type 2DM patients.
Our study showed that MBPS was associated with impaired FMD, a marker for endothelium injury, but not NMD, a marker of vascular smooth muscle function. Because it was reported   that DM patients showed vascular injury more predominantly in the endothelium   than on the arterial wall, the preferential association of MBPS with FMD, but not NMD, might validate    the importance of MBPS in the development of vascular injury in Type 2DM patients. In the early stage of DM, endothelial dysfunction, as reflected by impaired FMD, might predominately occur over arterial smooth muscle dysfunction as represented by impaired NMD. 
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[[[�[�[��G����������ٲ��٠ٲًٲٲٲًyweP(h<B,hTq>CJKHOJQJaJnH	@tH	@"h�E6CJKHOJQJaJnH	@tH	@U"hF,�CJKHOJQJaJnH	@tH	@(h<B,h�p�CJKHOJQJaJnH	@tH	@"h<B,CJKHOJQJaJnH	@tH	@"h�1CJKHOJQJaJnH	@tH	@(h<B,hj,�CJKHOJQJaJnH	@tH	@(h<B,h}ICJKHOJQJaJnH	@tH	@"h�YCJKHOJQJaJnH	@tH	@ small population study ,second ABMP is ideally conducted at home in a routine daily environment ,third because DM patients enrolled in the study were treated with various drugs, including antihypertensive drugs and statins, the effect of those treatments on MBPS could not be totally neglected.
Conclusion:
The current study demonstrated that poor glycemic control and insulin resistance have predictive value for the occurrence of MBPS in Type 2 DM patients, which might be significantly associated with endothelial dysfunction.








 









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