Diabetes Care
HOME HELP FEEDBACK SUBSCRIPTIONS ARCHIVE SEARCH TABLE OF CONTENTS
QUICK SEARCH:   [advanced]


     

Diabetes Care 29:792-797, 2006
DOI: 10.2337/diacare.29.04.06.dc05-1818
© 2006 by the American Diabetes Association
This Article
Right arrow Abstract Freely available
Right arrow Full Text (PDF)
Right arrow Erratum (v29,p1723)
Right arrow Purchase Article
Right arrow View Shopping Cart
Right arrow Alert me when this article is cited
Right arrow Alert me if a correction is posted
Services
Right arrow Email this article to a friend
Right arrow Similar articles in this journal
Right arrow Similar articles in PubMed
Right arrow Alert me to new issues of the journal
Right arrow Download to citation manager
Right arrow patientINFORMation
Right arrow Request Permissions
Citing Articles
Right arrow Citing Articles via HighWire
Right arrow Citing Articles via Google Scholar
Google Scholar
Right arrow Articles by Matz, K.
Right arrow Articles by Tuomilehto, J.
Right arrow Search for Related Content
PubMed
Right arrow PubMed Citation
Right arrow Articles by Matz, K.
Right arrow Articles by Tuomilehto, J.
Social Bookmarking
Add to CiteULike   Add to Del.icio.us   Add to Digg   Add to Reddit   Add to Technorati  
What's this?

Epidemiology/Health Services/Psychosocial Research
Original Article

Disorders of Glucose Metabolism in Acute Stroke Patients

An underrecognized problem

Karl Matz, MD1, Katharina Keresztes, MD1, Claudia Tatschl, MD1, Monika Nowotny, MD1, Alexandra Dachenhausen, MSC1, Michael Brainin, MD1 and Jaakko Tuomilehto, MD, MPOLSC, PHD2

1 Department of Neurology, Donauklinikum and Neurosciences Centre, Donau-Universität, Maria Gugging, Austria
2 Department of Public Health, University of Helsinki, Helsinki, Finland

Address correspondence and reprint requests to Karl Matz, Department of Neurology, Donauklinikum and Neurosciences Centre, Donau-Universität, Hauptstrasse 2, A-3400 Maria Gugging, Austria. E-mail: karl.matz{at}donauklinikum.at


   ABSTRACT
TOP
 ABSTRACT
INTRODUCTION
 RESEARCH DESIGN AND METHODS
 RESULTS
 CONCLUSIONS
 References
 
OBJECTIVE—To determine the prevalence of disturbances in glucose metabolism in patients with acute stroke.

RESEARCH DESIGN AND METHODS—Consecutively admitted acute stroke patients (n = 286) were screened for glucose tolerance according to the standardized World Health Organization protocol in the 1st and 2nd week after the stroke event. In addition, we repeatedly measured fasting capillary blood glucose during the first 10 days.

RESULTS—Measurements were not performed or cancelled if patients were not fully conscious or had severe dysphagia or early complications that made transfers to other hospitals necessary (n = 48). Of the remaining 238 patients, 20.2% had previously known diabetes; 16.4% were classified as having newly diagnosed diabetes, 23.1% as having impaired glucose tolerance (IGT), and 0.8% as having impaired fasting glucose; and only 19.7% showed normal glucose levels. Another 47 patients (19.7%) had hyperglycemic values only in the 1st week (transient hyperglycemia) or could not be fully classified due to missing data in the oral glucose tolerance test. Patients with diabetes compared with nondiabetic subjects had more severe strokes (National Institutes of Health Stroke Scale [NIHSS] on admission: 7.2 ± 6.6 vs. 4.6 ± 3.1, 4.2 ± 4.4, and 3.7 ± 3.6 for IGT, transient hyperglycemia, and normoglycemia, respectively; P < 0.001), a worse outcome (modified Rankin scale 0–1 at discharge: 40.2 vs. 54.4, 63.8, and 72.3% for IGT, transient hyperglycemia, and normoglycemia, respectively; P < 0.001), and a higher rate of infectious complications (35.6 vs. 12.3, 21.2, and 4.2% for IGT, transient hyperglycemia, and normoglycemia, respectively; P < 0.001). In the multivariate analysis, NIHSS on admission, female sex, and the occurrence of urinary tract infection were independently associated with newly diagnosed diabetes.

CONCLUSIONS—The majority of acute stroke patients have disorders of glucose metabolism, and in most cases this fact has been unrecognized. Diabetes worsens the outcome of acute stroke. Therefore, in the post–acute phase, an oral glucose tolerance test should be recommended in all stroke patients with no prior history of diabetes.

Abbreviations: IGT, impaired glucose tolerance • mRS, modified Rankin scale • NIHSS, National Institutes of Health Stroke Scale • OGTT, oral glucose tolerance test


   INTRODUCTION
TOP
 ABSTRACT
 INTRODUCTION
RESEARCH DESIGN AND METHODS
 RESULTS
 CONCLUSIONS
 References
 
The prevalence of disturbances of glucose metabolism in acute stroke has hitherto not been properly investigated in a Western population. By a Chinese study (1), diabetes and impaired glucose tolerance (IGT) were diagnosed by performing an oral glucose tolerance test (OGTT) within 3–6 months after stroke in 33.5 and 21%, respectively, of patients. Of individuals with diabetes, 40% were previously undiagnosed. In the cohort of the Glucose Insulin in Ischemic Stroke Trial (GIST) (2) patients without previously known diabetes, 21% had diabetes, 37% had IGT, and 42% had normal glucose values 3 months after stroke. However, only 44% of randomized patients underwent the OGTT protocol in this study. In a study of patients with acute coronary syndromes (3), two-thirds had disturbances of glucose metabolism. In a recent study (4), more than half of the patients with previous stroke or transient ischemic attack had IGT or diabetes.

Diabetes is a proven risk factor for stroke (5–7), with a two- to threefold increased risk for diabetic patients compared with nondiabetic patients. The population attributable risk lies between 18 and 54% (8). According to a Finnish study, diabetes causes 16% of stroke mortality among men and 33% among women (9). Compared with the rates in the normoglycemic population, IGT carries a higher incidence of coronary heart disease (10), cardiovascular diseases (11,12), and total mortality (13). Its role as a risk factor for stroke is less well documented, but recently, a prospective cohort study showed an increased risk for ischemic stroke or transient ischemic attack in patients with the metabolic syndrome (14). In a recently published study (15), insulin resistance was found to be independently associated with the risk of stroke even if adjusted for glycemic control. Up to 50% of people with IGT develop manifest diabetes within 10 years (16), but lifestyle changes such as diet, weight control, and regular physical activity can substantially reduce this progression (17). Thus, screening the high–vascular risk group of stroke patients for disturbances of glucose metabolism may yield a significant potential for secondary prevention.

Furthermore, the early recognition of disorders of glucose metabolism in stroke patients is important because hyperglycemia during the acute phase worsens the outcome (18), probably by reducing the salvage of penumbral tissue mediated by high lactate levels in brain tissue (19).


   RESEARCH DESIGN AND METHODS
TOP
 ABSTRACT
 INTRODUCTION
 RESEARCH DESIGN AND METHODS
RESULTS
 CONCLUSIONS
 References
 
A total of 300 consecutive patients with a suspected acute (defined as symptom onset within 24 h preceding admission) ischemic or hemorrhagic stroke event were ascertained for the study, of whom 14 had to be excluded because their neurological deficit proved to be of nonischemic origin, leaving 286 patients for the screening program. Patients not fully conscious and patients with unstable severe dysphagia or with medical complications that made transfer to other hospitals necessary were excluded from analysis, as were patients on corticosteroid therapy or with high serum creatinine levels (>177 mmol/l) (n = 48), leaving 238 patients for the study protocol. The excluded patients were clinically heterogeneous, and it was not possible to obtain a history of diabetes or to perform standard fasting plasma glucose measurements in a comparable way. However, the mean HbA1c (A1C) value (5.8 ± 0.8%) of these patients did not significantly differ from that of the nondiabetic patients who underwent the protocol (Table 1). Patients with known diabetes or with admission blood glucose levels >11.1 mmol/l were excluded from oral glucose tolerance testing and considered diabetic. The OGTT was performed according to the World Health Organization protocol (20): after overnight fasting, patients drank 250 ml of a solution of 75 g glucose within 3 min. Immediately before administering the drink and after 60 and 120 min, venous blood samples were taken in sodium fluoride tubes. Blood samples were cooled and analyzed immediately (by Hitachi Laboratory Systems). The first OGTT was performed on day 4 after stroke onset and the second during the following week (days 7–10). During the first 10 days, we also repeatedly measured fasting capillary blood glucose. Results of plasma glucose levels were classified according to the World Health Organization (20) and American Diabetes Association guidelines (21). Diabetes was diagnosed if results of either the OGTT or fasting capillary blood glucose measurements exceeded the cutoff values for the diabetic metabolic state on at least two different occasions in the 1st and 2nd week. If patients had at least two raised values, but only in the measurements of the 1st week, they were classified as having transient hyperglycemia.


View this table:
[in this window]
[in a new window]
  		Table 1— Baseline characteristics and stroke subtypes in stroke patients with diabetes, IFG/IGT, transient hyperglycemia, and normoglycemia

 
We recorded data about the following known vascular risk factors: hypertension (repeatedly elevated blood pressure readings above 140/90 or concurrent drug treatment), coronary heart disease (history of angina, myocardial infarction, coronary artery bypass surgery, angioplasty, or stenting), previous stroke (either by clinical signs or by a documented history of a previous stroke), peripheral arterial disease (history of claudication, acute arterial occlusion, bypass surgery, angioplasty, or stenting of extremity arteries), dyslipidemia (any elevation of either total cholesterol or triglycerides or LDL cholesterol), smoking, and alcohol consumption. Documented parameters of stroke severity and outcome were the National Institutes of Health Stroke Scale (NIHSS) (22) and the modified Rankin scale (mRS) (23).

Additionally evaluated laboratory values were A1C and serum creatinine. All patients had fundoscopy to screen for diabetic retinopathy or maculopathy. If indicated, patients had an MRI scan (Siemens 1.0 T) of the brain including diffusion weighted imaging.

Statistical analysis
Dichotomous variables were tested with the {chi}2 test and continuous variables with variance analysis. To look for interdependency regarding the classification of newly diagnosed diabetes, the covariates age, sex, NIHSS on admission, hypertension, and occurrence of stroke-associated complications including infections were entered into a logistic regression model. Conversely, a similar logistic regression model was applied for the classification of normal versus disturbed glucose regulation.


   RESULTS
TOP
 ABSTRACT
 INTRODUCTION
 RESEARCH DESIGN AND METHODS
 RESULTS
CONCLUSIONS
 References
 
Of the 238 subjects analyzed, 48 (20.2%) had previously known diabetes; 39 (16.4%) were classified as having newly diagnosed diabetes, 55 (23.1%) as having IGT, 2 (0.8%) as having impaired fasting glucose; and only 47 (19.7%) were normoglycemic (Fig. 1). Another 47 (19.7%) subjects had hyperglycemic values only in the 1st week after stroke, suggesting transient stress hyperglycemia, or could not be classified into any category because of missing data in the OGTT (13 patients). One-quarter of the 1st week’s OGTT results were classified as diabetic values (17.5% of the results of the 2nd week). Overall, 68.5% of the OGTT results of the 1st week after the event implied disturbed glucose regulation, as did 62.5% of the results of the 2nd week (Fig. 2). In only 19 patients (8%), previously undiagnosed diabetes would have been diagnosed if considering fasting plasma or capillary glucose levels alone, whereas elevated 2-h values in the OGTT led to the diagnosis of diabetes in an additional 20 patients (8.4%). Furthermore, the best receiver-operator characteristic curve for diagnosing diabetes was obtained with the 2-h OGTT values of the 2nd week: area under the curve 0.925 (95% CI 0.869–0.982) for 2-h OGTT in the 2nd week, 0.829 (0.736–0.922) for 2-h OGTT in the 1st week, 0.801 (0.7–0.902) for the fasting value of the 2nd week, 0.803 (0.7–0.905) for the fasting value of the 1st week, and 0.565 (0.475–0.655) for A1C.


Figure 1
View larger version (17K):
[in this window]
[in a new window]
  		Figure 1— Flow chart displaying the mode of classification of different groups of disturbances in glucose metabolism according to the OGTT and fasting capillary blood glucose. OGTT I was performed at day 4; OGTT II was performed from days 7 to 10 after the stroke event. IFG, impaired fasting glucose.

 

Figure 2
View larger version (19K):
[in this window]
[in a new window]
  		Figure 2— Distribution of diagnostic groups according to the results of the OGTT performed in the 1st and 2nd week after stroke. {square}, Normoglycemic values; Figure 2, IGT; {blacksquare}, IFG; Figure 2, diabetic values.

 
Patients with normal glucose regulation were more often men (more women among diabetic patients) and significantly younger than patients classified as having abnormal glucose regulation (Table 1). Hypertension was the only vascular risk factor significantly more prevalent in the diabetic patients; reported family history of diabetes or cerebrovascular disease, BMI, and waist circumference did not differ between the glucose categories (Table 1).

A1C was the only laboratory marker significantly higher in the group of diabetic patients. None of the newly diagnosed diabetic patients had diabetic retinopathy or maculopathy, indicating microvascular complications, whereas among the subjects with previously known diabetes, 12 had diabetic retinopathy.

Patients with diabetes (known and newly diagnosed) had more severe strokes (NIHSS on admission: 7.2 ± 6.6 vs. 4.6 ± 3.1, 4.2 ± 4.4, and 3.7 ± 3.6 for IGT, transient hyperglycemia, and normoglycemia, respectively; P < 0.001), a higher rate of pneumonia and urinary tract infections during the admission (35.6 vs. 12.3, 21.2, and 4.2% for IGT, transient hyperglycemia, and normoglycemia, respectively; P < 0.001), and a worse outcome at discharge (mRS 0–1 at discharge: 40.2 vs. 54.4, 63.8, and 72.3% for IGT, transient hyperglycemia, and normoglycemia, respectively; P < 0.001) than nondiabetic patients. Although the number of deaths in this patient material was quite small and the case fatality did not differ among the glucose categories, all seven deaths occurred in patients who had some kind of hyperglycemia and none occurred in normoglycemic patients. The occurrence of any other complication of acute stroke (recurrent stroke, symptomatic cerebral bleeding, cerebral edema, seizure, cardiac arrhythmia, heart failure, and extracerebral bleeding) did not differ between the groups.

In the multivariate logistic regression model, NIHSS on admission (P < 0.001, odds ratio [OR] 1.16, 95% CI 1.09–1.24), female sex (P = 0.01, 3.26, 1.33–8.0), and urinary tract infections (P = 0.002, 5.86, 1.93–17.8) were independently associated with the classification of newly diagnosed diabetes (Table 2). Age <70 years (P = 0.014, 2.34, 1.19–4.6) and normotension (P = 0.014, 2.38, 1.19–4.76) were factors associated with normal glucose values in OGTT.


View this table:
[in this window]
[in a new window]
  		Table 2— Logistic regression model for the classification of newly diagnosed diabetes

 

   CONCLUSIONS
TOP
 ABSTRACT
 INTRODUCTION
 RESEARCH DESIGN AND METHODS
 RESULTS
 CONCLUSIONS
References
 
In concordance with previous studies (1,2,4), we found a high proportion of disorders of glucose regulation, including newly discovered diabetes, in our study population. To what extent these hyperglycemic states were contributing to the risk of the stroke event remains unknown. There is a lack of data on the potential role of asymptomatic hyperglycemia for the stroke risk, whereas diabetes is an established risk factor (7,8). We found that the vast majority of patients suffering acute stroke had abnormal glucose regulation. In addition, diabetic patients had more severe strokes and a higher rate of infectious complications.

In a logistic regression analysis, stroke severity, urinary tract infection, and female sex were independently associated with previously unrecognized diabetes. This left the possibility that the test results of diabetic patients were influenced by inflammation or stroke-associated stress reaction (24). On the other hand, patients with diabetes tend to have more severe strokes and are generally prone to infections; therefore, the causal direction of this association cannot be decided. For lesser degrees of glucose intolerance (IGT and impaired fasting glucose), this may also be true, but the sample size of our study cohort was too small to detect these presumably small influences. The association with female sex was unexpected and cannot be interpreted by our data, leaving the possibility of a chance finding. It may also reflect the fact that women lose their relative advantage regarding cardiovascular risk compared with men when they have diabetes (25). Recently, a prospective cohort study found that women with metabolic syndrome have a 1.5 higher risk for ischemic stroke or transient ischemic attack than men (14).

One of the important results of this study was that the 2-h postchallenge glucose value during the OGTT was essential in identifying the majority of cases with newly diagnosed diabetes and, naturally, all cases with IGT. This is in keeping with the recent findings from the EuroHeart Survey among patients hospitalized with acute myocardial infarction or elective consultation for coronary heart disease (26). It is also known that the diagnostic value of 2-h glucose level is more predictive for vascular events and mortality in middle-aged and elderly subjects compared with the fasting glucose level (27,28,29,30).

There were limitations in our study. First, the OGTT could not be performed in all patients with acute stroke because of disease-associated complications such as dysphagia; therefore, we could not completely screen our hospital cohort for diabetes. Second, fasting capillary blood glucose and plasma glucose values during the OGTT were higher and more often hyperglycemic in the 1st week after stroke than in the 2nd week. This may indicate stress hyperglycemia during the acute phase of the illness, but part of it is due to the regression to the mean. Therefore, it is possible that patients with this transient hyperglycemia would be classified as normal if they are not tested during the acute phase of stroke.

The outcome assessment at discharge is not completely standardized because the time of assessment from the onset of stroke varies considerably and is influenced by various factors, such as concurring complications, the necessity of further investigations, and patient compliance. Nevertheless, we consider the lower proportion of independency at discharge (mRS 0–1 40.2 vs. 62.9%) in diabetic patients versus nondiabetic patients to be a good indicator for a more severe disease course in diabetic patients. This finding contrasts with previous studies that did not find an influence of diabetes on stroke outcome (31,32). However, in these studies, diabetes was defined as history of clinically diagnosed diabetes, and therefore among nondiabetic patients, many subjects had asymptomatic hyperglycemia as shown by the present study. The negative influence of hyperglycemia in nondiabetic stroke patients is quite well documented (18,23,33). Moreover, there is evidence that hyperglycemia is associated with reduced penumbral salvage and worse functional outcome in diabetic and nondiabetic patients (19).

As several studies have demonstrated (34,35), it is important to detect diabetes early and to control blood glucose levels and other risk factor parameters carefully. Effective antidiabetic drug treatment may improve the prognosis of diabetic patients with stroke, but thus far, there are no data from randomized controlled trials that would indicate that newly diagnosed diabetic patients would benefit from such treatment, either in the acute phase of stroke or later on. There is solid evidence that the progression of hyperglycemia from IGT to diabetes can be drastically reduced by lifestyle intervention, i.e., by diet and physical activity (17,36). It would be important to find out whether this could also be achieved in stroke survivors with IGT. Because the lifestyle intervention also reduces the levels of other risk factors of stroke, such as blood pressure, central obesity, and dyslipidemia, it may not only lead to lower rates of diabetes but also to an overall improvement of prognosis of stroke patients. Again, randomized controlled trials to test this hypothesis are needed.

In summary, the majority of acute stroke patients have disturbances of glucose metabolism, and in most cases these have been hitherto undiscovered. Many of these disturbances were only revealed by performing an OGTT and interpreting the 2-h post–glucose challenge values. Therefore, an OGTT screening in the post–acute phase has to be recommended in all stroke patients with no prior history of diabetes. Patients with pre-diabetic stages, i.e., IGT and impaired fasting glucose, are important targets for primary and secondary prevention strategies, including lifestyle modification, pharmacological anti-obesity treatment, and statin therapy. Long-term outcome after myocardial infarction has recently been shown to be worse in patients with newly detected abnormal glucose tolerance (26); therefore, further studies are warranted to assess the long-term prognosis of stroke patients with diabetes, IGT, or impaired fasting glucose and the effect of preventive measures.


   Acknowledgments
 
We thank all colleagues, nurses, and laboratory technicians involved in obtaining and analyzing blood samples.

K.M., M.B., J.T., and K.K. conceived and designed the study. K.M., K.K., C.T., M.N., and A.D. obtained and analyzed the data. K.M. wrote the report, which was then revised by M.B. and J.T.


   Footnotes
 
A table elsewhere in this issue shows conventional and Système International (SI) units and conversion factors for many substances.

The costs of publication of this article were defrayed in part by the payment of page charges. This article must therefore be hereby marked "advertisement" in accordance with 18 U.S.C. Section 1734 solely to indicate this fact.

Received for publication September 27, 2005. Accepted for publication January 15, 2006.


   References
TOP
 ABSTRACT
 INTRODUCTION
 RESEARCH DESIGN AND METHODS
 RESULTS
 CONCLUSIONS
 References
 

  1. Lam KS, Ma JT, Woo E, Lam C, Yu YL: High prevalence of undiagnosed diabetes among Chinese patients with ischemic stroke. Diabetes Res Clin Pract 14:133–137, 1991[Medline]
  2. Gray CS, Scott JF, French JM, Alberti KG, O’Connell JE: Prevalence and prediction of unrecognised diabetes mellitus and impaired glucose tolerance following acute stroke. Age Ageing 33:71–77, 2004[Abstract/Free Full Text]
  3. Norhammar A, Tenerz A, Nilsson G, Hamsten A, Efendic S, Ryden L, Malmberg K: Glucose metabolism in patients with acute myocardial infarction and no previous diagnosis of diabetes mellitus: a prospective study. Lancet 359:2140–2144, 2002[Medline]
  4. Kernan WN, Viscoli CM, Inzucchi SE, Brass LM, Bravata DM, Shulman GI, McVeety JC: Prevalence of abnormal glucose tolerance following a transient ischemic attack or ischemic stroke. Arch Intern Med 24:227–233, 2005
  5. Barrett-Connor E, Khaw KT: Diabetes mellitus: an independent risk factor for stroke? Am J Epidemiol 128:116–123, 1988[Abstract/Free Full Text]
  6. Burchfiel CM, Curb JD, Rodriguez BL, Abbott RD, Chiu D, Yano K: Glucose intolerance and 22-year stroke incidence: The Honolulu Heart Program. Stroke 25:951–957, 1994[Abstract]
  7. Folsom AR, Rasmussen ML, Chambless LE, Howard G, Cooper LS, Schmidt MI, Heiss G: Prospective associations of fasting insulin, body fat distribution, and diabetes with risk of ischemic stroke: The Atherosclerosis Risk in Communities (ARIC) Study Investigators. Diabetes Care 22:1077–1083, 1999[Abstract/Free Full Text]
  8. Goldstein LB, Adams R, Becker K, Furberg CD, Gorelick PB, Hademenos G, Hill M, Howard G, Howard VJ, Jacobs B, Levine SR, Mosca L, Sacco RL, Sherman DG, Wolf PA, del Zoppo GJ: Primary prevention of ischemic stroke: a statement for healthcare professionals from the Stroke Council of the American Heart Association. Circulation 103:163–182, 2001[Free Full Text]
  9. Tuomilehto J, Rastenyte D, Jousilahti P, Sarti C, Vartiainen E: Diabetes mellitus as a risk factor for death from stroke: prospective study of the middle-aged Finnish population. Stroke 27:210–215, 1996[Abstract/Free Full Text]
  10. Blake DR, Meigs JB, Muller DC, Najjar SS, Andres R, Nathan DM: Impaired glucose tolerance, but not impaired fasting glucose, is associated with increased levels of coronary heart disease risk factors: results from the Baltimore Longitudinal Study on Aging. Diabetes 53:2095–2100, 2004[Abstract/Free Full Text]
  11. Coutinho M, Gerstein HC, Wang Y, Yusuf S: The relationship between glucose and incident cardiovascular events: a metaregression analysis of published data from 20 studies of 95,783 individuals followed for 12.4 years. Diabetes Care 22:233–240, 1999[Abstract/Free Full Text]
  12. Lowe LP, Liu K, Greenland P, Metzger BE, Dyer AR, Stamler J: Diabetes, asymptomatic hyperglycemia, and 22-year mortality in black and white men: the Chicago Heart Association Detection Project in Industry Study. Diabetes Care 20:163–169, 1997[Abstract]
  13. Saydah SH, Loria CM, Eberhardt MS, Brancati FL: Subclinical states of glucose intolerance and risk of death in the U.S. Diabetes Care 24:447–455, 2001[Abstract/Free Full Text]
  14. Koren-Morag N, Goldbourt U, Tanne D: Relationship between the metabolic syndrome and ischemic stroke or transient ischemic attack. Stroke 36:1366–1371, 2005[Abstract/Free Full Text]
  15. Bravata DM, Wells CK, Kernan WN, Concato J, Brass LM, Gulanski BI: Association between impaired insulin sensitivity and stroke. Neuroepidemiology 25:69–74, 2005[Medline]
  16. Alberti KG: Impaired glucose tolerance: fact or fiction. Diabet Med 13(Suppl. 2):S6–S8, 1996
  17. Tuomilehto J, Lindstrom J, Eriksson JG, Valle TT, Hamalainen H, Ilanne-Parikka P, Keinanen-Kiukaanniemi S, Laakso M, Louheranta A, Rastas M, Salminen V, Uusitupa M: Finnish Diabetes Prevention Study Group: Prevention of type 2 diabetes by changes in lifestyle among subjects with impaired glucose tolerance. N Engl J Med 344:1343–1350, 2001[Abstract/Free Full Text]
  18. Williams LS, Rotich J, Qi R, Fineberg N, Espay A, Bruno A, Fineberg SE, Tierney WR: Effects of admission hyperglycemia on mortality and costs in acute ischemic stroke. Neurology 59:67–71, 2002[Abstract/Free Full Text]
  19. Parsons MW, Barber PA, Desmond PM, Baird TA, Darby DG, Byrnes G, Tress BM, Davis SM: Acute hyperglycemia adversely affects stroke outcome: a magnetic resonance imaging and spectroscopy study. Ann Neurol 52:20–28, 2002[Medline]
  20. World Health Organization: Definition, Diagnosis and Classification of Diabetes Mellitus and Its Complications: Report of a WHO Consultation. Geneva, World Health Org., 1999
  21. Expert Committee on the Diagnosis and Classification of Diabetes Mellitus: Report of the Expert Committee on the Diagnosis and Classification of Diabetes Mellitus. Diabetes Care 25(Suppl. 1):S5–S20, 2002
  22. Brott T, Adams HP Jr, Olinger CP, Marler JR, Barsan WG, Biller J, Spilker J, Holleran R, Eberle R, Hertzberg V: Measurements of acute cerebral infarction: a clinical examination scale. Stroke 20:864–870, 1989[Abstract/Free Full Text]
  23. Bonita R, Beaglehole R: Recovery of motor function after stroke. Stroke 19:1497–1500, 1988[Abstract/Free Full Text]
  24. Capes SE, Hunt D, Malmberg K, Pathak P, Gerstein HC: Stress hyperglycemia and prognosis of stroke in nondiabetic and diabetic patients: a systematic overview. Stroke 32:2426–2432, 2001[Abstract/Free Full Text]
  25. DECODE Study Group: Gender difference in all-cause and cardiovascular mortality related to hyperglycaemia and newly-diagnosed diabetes. Diabetologia 46:608–617, 2003[Medline]
  26. Bartnik M, Malmberg K, Norhammar A, Tenerz A, Ohrvik J, Ryden L: Newly detected abnormal glucose tolerance: an important predictor of long-term outcome after myocardial infarction. Eur Heart J 25:1990–1997, 2004[Abstract/Free Full Text]
  27. DECODE Study Group: Glucose tolerance and cardiovascular mortality: comparison of fasting and 2-hour diagnostic criteria. Arch Intern Med 161:397–405, 2001[Abstract/Free Full Text]
  28. Smith NL, Barzilay JI, Shaffer D, Savage PJ, Heckbert SR, Kuller LH, Kronmal RA, Resnick HE, Psaty BM: Fasting and 2-hour postchallenge serum glucose measures and risk of incident cardiovascular events in the elderly: the Cardiovascular Health Study. Arch Intern Med 162:209–216, 2002[Abstract/Free Full Text]
  29. DECODE Study Group: Consequences of the new diagnostic criteria for diabetes in older men and women. Diabetes Care 22:1667–1671, 1999[Abstract/Free Full Text]
  30. Qiao Q, Tuomilehto J, Borch-Johnsen K: Post-challenge hyperglycaemia is associated with premature death and macrovascular complications. Diabetologia 46:M17–M21, 2003
  31. Woo J, Lam CW, Kay R, Wong AH, Teoh R, Nicholls MG: The influence of hyperglycemia and diabetes mellitus on immediate and 3-month morbidity and mortality after acute stroke. Arch Neurol Nov47:1174–1177, 1990[Abstract]
  32. Karapanayiotides T, Piechowski-Jozwiak B, van Melle G, Bogousslavsky J, Devuyst G: Stroke patterns, etiology and prognosis in patients with diabetes mellitus. Neurology 62:1558–1562, 2004[Abstract/Free Full Text]
  33. Bruno A, Levine SR, Frankel MR, Brott TG, Lin Y, Tilley BC, Lyden PD, Broderick JP, Kwiatkowski TG, Fineberg SE, NINDS rt-PA Stroke Study Group: Admission glucose levels and clinical outcomes in the NINDS rt-PA Stroke Trial. Neurology 59:669–674, 2002[Abstract/Free Full Text]
  34. UK Prospective Diabetes Study (UKPDS): Group intensive blood-glucose control with sulphonylureas or insulin compared with conventional treatment and risk of complications in patients with type 2 diabetes (UKPDS 33). Lancet 352:837–853, 1998[Medline]
  35. Tuomilehto J, Rastenyte D, Birkenhager WH, Thijs L, Antikainen R, Bulpitt CJ, Fletcher AE, Forette F, Goldhaber A, Palatini P, Sarti C, Fagard R: Effects of calcium-channel blockade in older patients with diabetes and systolic hypertension: Systolic Hypertension in Europe Trial Investigators. N Engl J Med 340:677–684, 1999[Abstract/Free Full Text]
  36. Diabetes Prevention Program Research Group: Reduction in the incidence of type 2 diabetes with lifestyle modification or metformin. N Engl J Med 346:393–403, 2002[Abstract/Free Full Text]

Add to CiteULike CiteULike   Add to Del.icio.us Del.icio.us   Add to Digg Digg   Add to Reddit Reddit   Add to Technorati Technorati    What's this?

Find additional patient-related information at:

Most Stroke Patients Have Problems With Glucose Metabolism


This article has been cited by other articles:


Home page
 StrokeHome page
A. Rautio, M. Eliasson, and B. Stegmayr
Favorable Trends in the Incidence and Outcome in Stroke in Nondiabetic and Diabetic Subjects: Findings From the Northern Sweden MONICA Stroke Registry in 1985 to 2003
Stroke, December 1, 2008; 39(12): 3137 - 3144.
[Abstract] [Full Text] [PDF]

Home page
 Diabetes CareHome page
Z. T. Bloomgarden
American College of Endocrinology Pre-Diabetes Consensus Conference: Part One
Diabetes Care, October 1, 2008; 31(10): 2062 - 2069.
[Full Text] [PDF]

Home page
 HeartHome page
R Peter, A Cox, and M Evans
Management of diabetes in cardiovascular patients
Heart, March 1, 2008; 94(3): 369 - 375.
[Full Text] [PDF]

Home page
 StrokeHome page
A. Bruno, T. A. Kent, B. M. Coull, R. R. Shankar, C. Saha, K. J. Becker, B. M. Kissela, and L. S. Williams
Treatment of Hyperglycemia In Ischemic Stroke (THIS): A Randomized Pilot Trial
Stroke, February 1, 2008; 39(2): 384 - 389.
[Abstract] [Full Text] [PDF]

Home page
 Eur Heart J SupplHome page
Authors/Task Force Members, L. Ryden, E. Standl, M. Bartnik, G. V. d. Berghe, J. Betteridge, M.-J. de Boer, F. Cosentino, B. Jonsson, M. Laakso, et al.
Guidelines on diabetes, pre-diabetes, and cardiovascular diseases: full text: The Task Force on Diabetes and Cardiovascular Diseases of the European Society of Cardiology (ESC) and of the European Association for the Study of Diabetes (EASD)
Eur. Heart J. Suppl., June 1, 2007; 9(suppl_C): C3 - C74.
[Full Text] [PDF]

Home page
 British Journal of Diabetes & Vascular DiseaseHome page
C. Day
Cardio-diabetes: new ESC-EASD joint guidelines
The British Journal of Diabetes & Vascular Disease, March 1, 2007; 7(2): 47 - 48.
[PDF]

Home page
 Eur Heart JHome page
Authors/Task Force Members, L. Ryden, E. Standl, M. Bartnik, G. Van den Berghe, J. Betteridge, M.-J. de Boer, F. Cosentino, B. Jonsson, M. Laakso, et al.
Guidelines on diabetes, pre-diabetes, and cardiovascular diseases: executive summary: The Task Force on Diabetes and Cardiovascular Diseases of the European Society of Cardiology (ESC) and of the European Association for the Study of Diabetes (EASD)
Eur. Heart J., January 1, 2007; 28(1): 88 - 136.
[Full Text] [PDF]

Home page
 NeurologyHome page
H.-F. Li, X.-D. Pan, N. Sanossian, and B. Ovbiagele
Premorbid antiplatelet use and ischemic stroke outcomes.
Neurology, November 14, 2006; 67(9): 1723 - 1723.
[Full Text] [PDF]

This Article
Right arrow Abstract Freely available
Right arrow Full Text (PDF)
Right arrow Erratum (v29,p1723)
Right arrow Purchase Article
Right arrow View Shopping Cart
Right arrow Alert me when this article is cited
Right arrow Alert me if a correction is posted
Services
Right arrow Email this article to a friend
Right arrow Similar articles in this journal
Right arrow Similar articles in PubMed
Right arrow Alert me to new issues of the journal
Right arrow Download to citation manager
Right arrow patientINFORMation
Right arrow Request Permissions
Citing Articles
Right arrow Citing Articles via HighWire
Right arrow Citing Articles via Google Scholar
Google Scholar
Right arrow Articles by Matz, K.
Right arrow Articles by Tuomilehto, J.
Right arrow Search for Related Content
PubMed
Right arrow PubMed Citation
Right arrow Articles by Matz, K.
Right arrow Articles by Tuomilehto, J.
Social Bookmarking
Add to CiteULike   Add to Del.icio.us   Add to Digg   Add to Reddit   Add to Technorati  
What's this?

HOME HELP FEEDBACK SUBSCRIPTIONS ARCHIVE SEARCH TABLE OF CONTENTS
Diabetes Diabetes Care Clinical Diabetes Diabetes Spectrum