Abstract
To study the relationship between nocturnal blood pressure (BP) variation and spontaneous intracerebral hemorrhage (ICH) among Chinese hypertensive patients and its clinical significance, the authors retrospectively screened 371 patients with primary hypertension (189 patients with ICH, 182 patients without ICH) in Shanghai and analyzed their demographics, clinical information, nocturnal blood pressure variability and medication. Compared with the control group, the levels of blood glucose, triglycerides, and creatinine were significantly increased in the ICH group, along with a marked reduction in nocturnal BP drop (P<.05). Multivariate logistic regression indicated that blood glucose, creatinine, and nocturnal mean arterial pressure were risk factors for ICH, and the magnitude of nocturnal BP drop was negatively related to the risk for ICH. There was no significant difference in the prevalence of reverse dippers between the large hematoma volume group and the small hematoma volume group (χ2=2.529, P=.112), nor among the patients taking angiotensin‐converting enzyme inhibitors, angiotensin receptor blockers, or calcium channel blockers (χ2=1.981, P=.371). Reverse dipping is associated with the risk for ICH, suggesting that appropriate antihypertensive drug and chronotherapy might be effective to normalize the rhythm of abnormal circadian variation in hypertensive patients.
Spontaneous intracerebral hemorrhage (ICH) is defined as nontraumatic parenchymal hemorrhage characterized by acute onset, rapid progress, high incidence, and extremely high mortality rate. Prognosis of patients with primary ICH in the acute stage can be helpful to formulate the best therapeutic and rehabilitation strategies. Hypertension is one of the major risk factors for ICH.1 Although casual blood pressure (BP) has been widely employed in clinical practice, it has a number of limitations, including white‐coat hypertension, that prevent it from accurately reflecting real changes in BP, disease severity, or therapeutic efficacy in patients. Ambulatory BP monitoring (ABPM) can record BP periodically during 24 hours and thus accurately reflect circadian BP variability. It has been demonstrated that ABPM is very helpful to physicians to predict target organ damage (TOD) and decide protocol and treatment evaluation for hypertensive patients.2 Normotensive patients and hypertensive patients all have circadian BP variation. The normal circadian rhythm, namely “dipping,” is defined as a 10% to 20% decline in nocturnal BP compared with daytime as an important mechanism of protecting the cardiovascular system. In addition, “nondipping,” “reverse dipping,” and “extreme dipping” are defined as abnormal circadian BP rhythm.3, 4
Routledge and colleagues5 previously reported that a blunted nocturnal BP drop contributed to TOD, especially for cardiovascular and cerebrovascular diseases. Abnormal nocturnal BP variation has been shown to be associated with left ventricular hypertrophy,6, 7 cognitive impairment,8 silent cerebral infarct,9 microalbuminuria,10 and carotid artery intima‐media thickness.11 Furthermore, it has been reported that nocturnal BP is an independent predictor of cardiovascular events in hypertensive patients.12 Accordingly, magnitude of nocturnal BP drop can provide a more reliable and useful prognostic indication on cerebrovascular damage than casual BP, including spontaneous ICH. However, limited information is available on the association between abnormal circadian BP variation and ICH. In this work, we sought to investigate the relationship between circadian BP variation and spontaneous ICH among Chinese hypertensive patients.
Methods
Patients
This retrospective, case‐control study was approved by the ethics committee of Ruijin Hospital affiliated with Shanghai Jiao Tong University School of Medicine. We screened 371 patients with primary hypertension from databases of 4 hospitals in Shanghai (including Ruijin Hospital, Gongli Hospital, Shanghai City Second People's Hospital, and Shanghai Putuo District People's Hospital) from November 2010 to August 2012. Primary hypertension was diagnosed according to the diagnostic standard announced by the World Health Organization/International Society of Hypertension in 1999. All of the patients underwent ABPM and took long‐acting antihypertensive drugs.
According to the presence of ICH, patients were categorized into two groups: ICH group and control group. The inclusion criteria of the ICH group included the following: (1) history of hypertension; (2) the sudden onset of acute focal neurological deficit; (3) the presence of accompanying symptoms of increased intracranial pressure, such as headache, nausea, vomiting; (4) first cranial computed tomographic (CT) or magnetic resonance imaging (MRI) scan obtained within 24 hours after ICH, and the diagnoses confirmed by neurologist and neuroradiologist; and (5) ABPM performed 15 to 28 days after the acute onset of ICH. Patients with other causes of ICH were excluded, including those with trauma, aneurysm, arteriovenous malformation, brain tumors, atrial fibrillation, and coagulation disorder (eg, anticoagulant or antiplatelet aggregation drug). The inclusion criteria of the control group included: (1) history of hypertension; (2) exclusion of acute cerebrovascular diseases symptoms; (3) ABPM during treatment; (4) normal results from brain MRI and all diffusion‐weighted imaging of MRI; and (5) age‐matched control group.
Clinical information was recorded including fasting blood glucose, serum triglycerides (TGs), total cholesterol (TC), high‐density lipoprotein cholesterol (HDL‐C), low‐density lipoprotein cholesterol (LDL‐C), blood urea nitrogen, serum creatinine, and medical histories (hypertension duration, family history, and medication use). Furthermore, electrocardiography (ECG), cranial CT or MRI scans, and ABPM were documented.
Ambulatory BP Monitoring
Systolic pressure, diastolic pressure, and heart rate were recorded automatically at an interval of 30 minutes during the day (6 am to 10 pm) or 60 minutes at night (10 pm to 6 am) with a Spacelabs 90217 ABPM device (Spacelabs Healthcare, Snoqualmie, WA) for 24 hours. The mean values of daytime and nighttime BP and the magnitude of nocturnal BP drop were calculated automatically. Mean arterial pressure (MAP) was calculated as one third systolic pressure plus two thirds diastolic pressure. The percentage of nocturnal BP drop was defined as ([daytime MAP – nighttime MAP]/daytime MAP) × 100.13 According to the percentage of nocturnal BP drop, circadian BP variation could be subdivided into 4 groups: (1) extreme dipping “percent decline ≥20%,” (2) dipping “≥10% but <20%,” (3) nondipping “≥0 but <10%,” (4) reverse dipping “<0 or nocturnal BP elevation.”3, 4
Volume of Hematoma
Cranial CT scans (64‐slice) were reviewed independently by two experienced neurologists with slice thickness of 5 mm or 10 mm. The maximal longitudinal and transverse diameter in the largest slice of hematoma, and the number and thickness of slices were outlined and recorded, respectively. Hematoma volume was calculated using the formula 1/2 ABC, with A as the largest hematoma diameter, B as the maximum diameter perpendicular to A, while C as the number of slices with hemorrhage multiplied by the slice thickness.14 Finally, the average value was calculated to avoid the bias. Surgery was recommended if the supratentorial hemorrhage was >30 mL or the infratentorial hemorrhage was >15 mL.15, 16 Therefore, according to the ICH volume, patients were subdivided into large‐volume and small‐volume groups.
Statistical Analysis
Statistical analysis was performed using SPSS 18.0 software (SPSS Inc, Chicago, IL). Values were expressed as mean±standard deviation, and Student t test was used for intergroup comparison. Chi‐square test was performed for enumeration data. The multiple logistic regression analysis was made to analyze the independent risk factors for ICH. P<.05 was considered statistically significant.
Results
Clinical Characteristics of Study Population
In this study we collected data from 371 primary hypertensive patients (hypertension duration, 0.1–40 years; 115 cases with family history of hypertension). All patients took one of following long‐acting antihypertensive drugs: angiotensin‐converting enzyme inhibitor (ACE inhibitor; 37 cases), angiotensin receptor blocker (ARB; 102 cases), and calcium channel blocker (CCB; 232 cases). Our results revealed that there was no statistically significant difference in age, TC, LDL‐C, and urea nitrogen between the ICH and control groups (P>.05). Values of blood glucose, TGs, HDL‐C, and creatinine increased significantly in the ICH group compared with the control group, whereas the degree of nocturnal BP drop was significantly decreased. In addition, there were more men in the ICH group than in the control group (χ2=51.965, P=.000). The percentage of nocturnal BP drop in the ICH group (−3.48%±13.91%) was significantly less than that in the control group (11.48%±7.24%; Table 1).
Table 1.
Demographic Characteristics and Risk Factors of ICH and Control Groups
| Characteristic | Control (n=182) | ICH (n=189) | χ2 | P Value |
|---|---|---|---|---|
| Age, y | 60.0±8.3 | 60.7±9.9 | .441 | |
| Male/female sex | 61/121 | 134/55 | 51.965 | .000 |
| Glucose, mmol/L | 5.44±1.15 | 6.00±1.93 | .001 | |
| TGs, mmol/L | 1.62±1.16 | 2.00±1.53 | .008 | |
| TC, mmol/L | 4.63±1.14 | 4.44±1.13 | .105 | |
| HDL‐C, mmol/L | 1.44±1.04 | 1.27±0.51 | .048 | |
| LDL‐C, mmol/L | 3.01±0.91 | 2.91±0.81 | .301 | |
| Urea nitrogen, mmol/L | 5.17±2.22 | 5.22±2.34 | .824 | |
| Creatinine, μmol/L | 66.30±18.14 | 79.65±42.93 | .000 | |
| Nocturnal BP drop, % | 11.48±7.24 | −3.48±13.91 | .000 | |
| ECG, normal/abnormal | 65/117 | 75/114 | 0.621 | .431 |
Abbreviations: BP, blood pressure; ECG, electrocardiography; HDL‐C, high‐density lipoprotein; ICH, intracerebral hemorrhage; LDL‐C, low‐density lipoprotein; TC, total cholesterol; TGs, triglycerides.
There was no statistical significance in abnormal ECG between the ICH and control groups (χ2=0.621, P=.431). Abnormal ECG results were found in 231 patients, such as supervoltage of ventriculus sinister, T or ST‐T changes, atrial or ventricular premature contractions, atrial fibrillation, sinus bradycardia, first‐degree or type 1 second‐degree atrioventricular block, right bundle branch block, left anterior fascicular block, and abnormal Q wave. Ten patients (5.3%) in the ICH group had acute multifocal cerebral hemorrhage. The occurrence of lesions in various brain regions are as follows: basal ganglia (99 of 189), lobes of brain (40 of 189), thalamus (30 of 189), external capsule (8 of 189), cerebellum (8 of 189), internal capsule (4 of 189), corona radiate (4 of 189), pons (4 of 189), and perilateral ventricles (2 of 189).
Multivariate Logistic Regression Analyses of Potential ICH Risk Factors
The multivariate logistic regression indicated that blood glucose, creatinine, and nighttime MAP were risk factors for ICH, and the magnitude of nocturnal BP drop was negatively associated with the risk for ICH (Table 2).
Table 2.
The Multivariate Logistic Regression Analyses of Potential ICH Risk Factors
| Parameters | Partial Regression Coefficient | Standard Error | Wald | P Value | OR | 95% CI |
|---|---|---|---|---|---|---|
| Glucose | 0.213 | 0.103 | 4.241 | .039 | 1.237 | 1.010–1.515 |
| Creatinine | 0.027 | 0.008 | 12.081 | .001 | 1.027 | 1.012–1.043 |
| Nighttime MAP | 0.067 | 0.015 | 20.539 | .000 | 1.070 | 1.039–1.101 |
| Magnitude of nocturnal BP drop | −9.736 | 1.895 | 26.406 | .000 | 0.000 | 0.000–0.002 |
Abbreviations: BP, blood pressure; CI, confidence interval; ICH, intracerebral hemorrhage; MAP, mean arterial pressure; OR, odds ratio.
Comparison of ICH Among Patterns of Circadian BP Rhythm
The occurrence of 4 patterns of the circadian BP rhythm (dipping, nondipping, reverse dipping, and extreme dipping) in the ICH group was compared with those in the control group. There was a significantly greater prevalence of reverse dippers in the ICH group (96 [50.8%]) than in the control group (7 [3.8%]). This result indicated that the tendency of ICH was increased in reverse dippers (χ2=121.047, P=.000; Figure 1, Table 3). For further verification, dipping, nondipping, and extreme dipping patients were combined as a group, and found that the tendency of ICH remained significantly higher in reverse dippers. Reverse dipping status was associated with ICH (χ2=101.897, P=.000; Table 4).
Figure 1.
Comparison of intracerebral hemorrhage (ICH) among 4 patterns of circadian blood pressure (BP) rhythm (dipping, nondipping, reverse dipping, and extreme dipping). There was a significantly greater prevalence of reverse dipping in the ICH group (96 [50.8%]) than the control group (7 [3.8%]; χ2=121.047; P=.000).
Table 3.
Comparison of ICH Among 4 Patterns of Circadian BP Rhythm
| Parameters, No. (%) | Control | ICH | χ2 | P Value |
|---|---|---|---|---|
| Extreme dippers | 20 (11.0) | 0 (0.0) | ||
| Dippers | 86 (47.3) | 33 (17.5) | ||
| Nondippers | 69 (37.9) | 60 (31.7) | ||
| Reverse dippers | 7 (3.8) | 96 (50.8) | 121.047 | .000 |
Abbreviations: BP, blood pressure; ICH, intracerebral hemorrhage.
Table 4.
Comparison of ICH Between Reverse Dippers and Other Patterns of Circadian BP Rhythm
| Parameters, No. (%) | Control | ICH | χ2 | P Value |
|---|---|---|---|---|
| Others | 175 (96.2) | 93 (49.2) | ||
| Reverse dippers | 7 (3.8%=) | 96 (50.8) | 101.897 | .000 |
Abbreviations: BP, blood pressure; ICH, intracerebral hemorrhage.
Comparison of Hematoma Volume and Antihypertensive Drugs Between Reverse Dippers and Other Patterns of Circadian BP Rhythm
There was no significant difference in the prevalence of reverse dippers between the large hematoma volume group and the small hematoma volume group (χ2=2.529, P=.112). Reverse dipping status was not related to the volume of hematoma (Table 5). In addition, there was no significant difference in the prevalence of reverse dippers among patients treated with ACE inhibitors, ARBs, or CCBs (χ2=1.981, P=.371; Figure 2). The patterns of circadian BP rhythm were not correlated with the use of long‐acting antihypertensive drug.
Table 5.
Comparison of Hematoma Volume Between Reverse Dippers and Other Patterns of Circadian Blood Pressure Rhythm
| Parameters | Small Hematoma Volume | Large Hematoma Volume | χ2 | P Value |
|---|---|---|---|---|
| Others, No. (%) | 85 (91.4) | 8 (8.6) | ||
| Reverse dippers, No. (%) | 92 (96.8) | 3 (3.2) | 2.529 | .112 |
Figure 2.
Comparison of 3 antihypertensive drugs between reverse dipping and other patterns of circadian blood pressure (BP) rhythm (dipping, nondipping, and extreme dipping). There was no significant difference in prevalence of reverse dipping among patients treated with angiotensin‐converting enzyme inhibitors (7 [18.9%]), angiotensin receptor blockers (27 [26.5%]), or calcium channel blockers (69 [29.7%]; χ2=1.981, P=.371).
Discussion
This retrospective work was made based on records of 371 primary hypertensive patients, which showed that reverse dipping status was associated with the tendency of ICH but not with the volume of hematoma or the use of 3 long‐acting antihypertensive drugs (ACE inhibitors, ARBs, and CCBs).
Tsivgoulis and colleagues13 previously demonstrated that the blunted nocturnal BP drop was related to the risk for ICH (odds ratio, 1.143) with ABPM performed at 21 to 28 days after ictus but not related to the site of the intracerebral hemorrhage. However, Yamamoto and associates17 validated that the blunted nocturnal BP drop was associated with the site of the intracerebral hemorrhage. Compared with that in the control group, the percentage of nocturnal BP drop was decreased for thalamic and pontine hemorrhages except for the putaminal hemorrhage. Furthermore, Lip and colleagues18 demonstrated that the abnormal nocturnal BP variation (nondipping) was found in most stroke patients (cerebral infarction and ICH), and there was also a tendency to reverse dipping status in ICH patients. Kario and coworkers19 made a follow‐up study in 575 older Japanese patients with sustained hypertension for an average of 41 months and found that extreme dippers and reverse dippers may have a worse prognosis. They reported that extreme dipping status was associated with silent and clinical cerebral ischemia caused by hypoperfusion during sleep and an exaggerated rise of BP in the morning, whereas reverse dipping status was shown to increase the tendency of ICH.19 Our results were consistent with the above studies, which showed that the magnitude of nocturnal BP drop was negatively related to ICH and reverse dipping status increased the risk for ICH.
The finding that high blood glucose level and creatinine were also risk factors for intracranial hemorrhage was derived from a multiple step‐wise logistic regression based on a relatively small sample of patients. It conformed to the clinical regularity in which high blood glucose had been generally proved in the literature to be a risk factor for intracranial hemorrhage. It is known that the risk of intracranial hemorrhage for diabetic patients is 3 to 4 times higher for nondiabetics. On the other hand, the increase in creatinine level is a sensitive indication for chronic renal diseases. A recent article argued that chronic kidney disease was independently associated with cerebral microbleeds in patients without diabetes20 and in ICH patients.21 As the relationship between microbleeds and ICH did exist,22 chronic renal disease could also pose a risk for ICH, probably resulting from the decrease in some coagulation factors.
Our results indicate that there is no significant difference in the prevalence of reverse dipping among patients treated with ACE inhibitors, ARBs, or CCBs. The patterns of circadian BP rhythm were not correlated with the use of long‐acting antihypertensive drugs. Some researches pointed out that nondipping status might be relevant in the absence of 24‐hour therapeutic coverage.23 Therefore, chronotherapy should be employed according to the patterns of circadian BP variation to avoid TOD, especially for nondippers and reverse dippers. Patients with elevated nocturnal BP could take a long‐acting antihypertensive drug at bedtime to recover the rhythm.
It has been revealed that reverse dipping was also implicated in prognosis in patients with nondialysis chronic kidney disease,24 impairment of cardiac function and structure,25 neurologic deficit in early acute ischemic stroke,26 and higher incidences of cardiovascular events and mortality.27 These findings strongly support the hypothesis that long‐term elevated BP (especially for nocturnal BP) may result in endothelium dysfunction and remodeling of large and small arteries as a result of TOD and affect the prognosis of hypertensive patients. Due to the impairment of autonomic nervous system, sustained excitement of sympathetic nervous system or decreased parasympathetic nervous system activity during sleep may lead to elevated nocturnal BP and abnormal rhythm.28, 29 Other possible mechanisms include orthostatic hypotension,30, 31 thyroid hormones,32 sleep quality,33 and apnea.34
Study Limitations
There are some limitations in our work. Firstly, we could not investigate sleep quality in every hypertensive patients. Studies have shown that patients with poor sleep quality present a higher prevalence of nondipping status.33 There is also evidence that sleep apnea syndrome has been shown to increase the activity of sympathetic nervous system, contributing to the elevated nocturnal BP.34 Further research is needed to determine the relationship between sleep and BP in the future. Secondly, Ohwaki and colleagues35 pointed out that elevated nocturnal BP significantly increased the risk of hematoma enlargement. Nevertheless, reverse dipping status (nocturnal elevation) was not related to the volume of hematoma in our result. There were only 11 ICH patients with supratentorial hemorrhage >30 mL or infratentorial hemorrhage >15 mL in the present study, which might be the reason we could not find a relationship between reverse dipping and hematoma volume. Thirdly, we screened 371 patients with primary hypertension from 4 hospitals in Shanghai from November 2010 to August 2012. There were more men in the ICH group as compared with the control group. It is well known that sex is one of the risk factors for ICH. Due to the small number of patients, we did not match the sex between ICH and control groups after adjustment for age. Finally, it may be interesting to investigate the relationship between hypertensive duration and the prevalence or volume of hematoma. Therefore, in the future, large‐scale prospective study should be carried out.
Conclusions
Compared with other patterns of the circadian BP rhythm, reverse dipping is related to the risk of ICH, implying that appropriate antihypertensive drug therapy and chronotherapy may be effective to normalize the rhythm for hypertensive patients with abnormal circadian rhythm. There are many risk factors for ICH such as sex, aging, smoking, hypertension, and diabetes mellitus, while hypertension is known to be one of the most important risk factors for ICH. However, the purpose of our research is to find out new relationships concerning ICH rather than repeating the results that have already been proven. It is important to measure nocturnal BP variation in hypertensive patients to evaluate the risk of ICH.
Acknowledgments
This work was sponsored by the Science and Technology Commission of Shanghai Municipality (12ZR1418600), the Key Discipline Construction Project of Pudong Health Bureau of Shanghai (PWZx2014‐08), the Training Program of the National Major Research Plan (91339108), the National Natural Science Foundation of China (81370362 & 81170246), and the National Basic Research Program of China (2014CB542300).
Disclosure
None.
J Clin Hypertens (Greenwich). 2014;16:652–657. © 2014 Wiley Periodicals, Inc.25056509
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