Skip to main content
Top
Published in: Neurocritical Care 2/2020

01-04-2020 | Cerebral Small Vessel Disease | Original Work

Stress-Induced Hyperglycemia and Remote Diffusion-Weighted Imaging Lesions in Primary Intracerebral Hemorrhage

Authors: Xiang-hua Ye, Xue-li Cai, Dong-liang Nie, Ye-jun Chen, Jia-wen Li, Xu-hua Xu, Jin-song Cai, Zhi-rong Liu, Xin-zhen Yin, Shui-jiang Song, Lu-sha Tong, Feng Gao

Published in: Neurocritical Care | Issue 2/2020

Login to get access

Abstract

Background and Purpose

Stress-induced hyperglycemia (SIH) is the relative transient increase in glucose during a critical illness such as intracerebral hemorrhage (ICH) and is likely to play an important role in the pathogenesis of remote diffusion-weighted imaging (DWI) lesion (R-DWIL) in primary ICH. We sought to determine the association between SIH and the occurrence of R-DWILs.

Methods

We prospectively enrolled primary ICH patients within 14 days after onset from November 2016 to May 2018. In these patients, cerebral magnetic resonance imaging was performed within 14 days after ICH onset. R-DWIL was defined as a hyperintensity signal in DWI with corresponding hypointensity in apparent diffusion coefficient, and at least 20 mm apart from the hematoma. SIH was measured by stress-induced hyperglycemia ratio (SHR). SHR was calculated by fasting blood glucose (FBG) divided by estimated average glucose derived from glycosylated hemoglobin. The included patients were dichotomized into two groups by the 50th percentile of SHR, and named as SHR (−P50) group and SHR (P50+) group, respectively. We evaluated the association between SHR and R-DWIL occurrence using multivariable logistic regression modeling adjusted for potential confounders.

Results

Among the 288 patients enrolled, forty-six (16.0%) of them had one or more R-DWILs. Compared with the patients in the lower 50% of SHR (SHR [−P50]), the odds ratio (OR) [95% confidence interval (CI)] for the higher 50% of SHR (SHR [P50+]) group for R-DWIL occurrence was 3.13 (1.39–7.07) in the total population and 6.33 (2.19–18.30) in population absent of background hyperglycemia after adjusting for potential covariates. Similar results were observed after further adjusted for FBG.

Conclusions

Our study demonstrated that SIH was associated with the occurrence of R-DWILs in patients with primary ICH within 14 days of symptom onset.
Literature
1.
go back to reference Qureshi AI, Tuhrim S, Broderick JP, et al. Spontaneous intracerebral hemorrhage. N Engl J Med. 2001;344(19):1450–60.PubMed Qureshi AI, Tuhrim S, Broderick JP, et al. Spontaneous intracerebral hemorrhage. N Engl J Med. 2001;344(19):1450–60.PubMed
2.
go back to reference Hemphill JC, Bonovich DC, Besmertis L, Manley GT, Johnston SC. The ICH score: a simple, reliable grading scale for intracerebral hemorrhage. Stroke. 2001;32(4):891–7.PubMed Hemphill JC, Bonovich DC, Besmertis L, Manley GT, Johnston SC. The ICH score: a simple, reliable grading scale for intracerebral hemorrhage. Stroke. 2001;32(4):891–7.PubMed
3.
go back to reference Menon RS, Burgess RE, Wing JJ, et al. Predictors of highly prevalent brain ischemia in intracerebral hemorrhage. Ann Neurol. 2012;71(2):199–205.PubMedPubMedCentral Menon RS, Burgess RE, Wing JJ, et al. Predictors of highly prevalent brain ischemia in intracerebral hemorrhage. Ann Neurol. 2012;71(2):199–205.PubMedPubMedCentral
4.
go back to reference Prabhakaran S, Gupta R, Ouyang B, et al. Acute brain infarcts after spontaneous intracerebral hemorrhage: a diffusion-weighted imaging study. Stroke. 2010;41(1):89–94.PubMed Prabhakaran S, Gupta R, Ouyang B, et al. Acute brain infarcts after spontaneous intracerebral hemorrhage: a diffusion-weighted imaging study. Stroke. 2010;41(1):89–94.PubMed
5.
go back to reference Tsai YH, Lee MH, Weng HH, et al. Fate of diffusion restricted lesions in acute intracerebral hemorrhage. PLoS ONE. 2014;9(8):e105970.PubMedPubMedCentral Tsai YH, Lee MH, Weng HH, et al. Fate of diffusion restricted lesions in acute intracerebral hemorrhage. PLoS ONE. 2014;9(8):e105970.PubMedPubMedCentral
6.
go back to reference Gregoire SM, Charidimou A, Gadapa N, et al. Acute ischemic brain lesions in intracerebral haemorrhage: multicentre cross-sectional magnetic resonance imaging study. Brain. 2011;134(Pt 8):2376–86.PubMed Gregoire SM, Charidimou A, Gadapa N, et al. Acute ischemic brain lesions in intracerebral haemorrhage: multicentre cross-sectional magnetic resonance imaging study. Brain. 2011;134(Pt 8):2376–86.PubMed
7.
go back to reference Kang DW, Han MK, Kim HJ, et al. New ischemic lesions coexisting with acute intracerebral hemorrhage. Neurology. 2012;79(9):848–55.PubMed Kang DW, Han MK, Kim HJ, et al. New ischemic lesions coexisting with acute intracerebral hemorrhage. Neurology. 2012;79(9):848–55.PubMed
8.
go back to reference Kimberly WT, Gilson A, Rost NS, et al. Silent ischemic infarcts are associated with hemorrhage burden in cerebral amyloid angiopathy. Neurology. 2009;72(14):1230–5.PubMedPubMedCentral Kimberly WT, Gilson A, Rost NS, et al. Silent ischemic infarcts are associated with hemorrhage burden in cerebral amyloid angiopathy. Neurology. 2009;72(14):1230–5.PubMedPubMedCentral
9.
go back to reference Gioia LC, Kate M, Choi V, et al. Ischemia in intracerebral hemorrhage is associated with leukoaraiosis and hematoma volume, not blood pressure reduction. Stroke. 2015;46(6):1541–7.PubMed Gioia LC, Kate M, Choi V, et al. Ischemia in intracerebral hemorrhage is associated with leukoaraiosis and hematoma volume, not blood pressure reduction. Stroke. 2015;46(6):1541–7.PubMed
10.
go back to reference Wu B, Yao X, Lei C, Liu M, Selim MH. Enlarged perivascular spaces and small diffusion-weighted lesions in intracerebral hemorrhage. Neurology. 2015;85(23):2045–52.PubMedPubMedCentral Wu B, Yao X, Lei C, Liu M, Selim MH. Enlarged perivascular spaces and small diffusion-weighted lesions in intracerebral hemorrhage. Neurology. 2015;85(23):2045–52.PubMedPubMedCentral
11.
go back to reference Auriel E, Gurol ME, Ayres A, et al. Characteristic distributions of intracerebral hemorrhage-associated diffusion-weighted lesions. Neurology. 2012;79(24):2335–41.PubMedPubMedCentral Auriel E, Gurol ME, Ayres A, et al. Characteristic distributions of intracerebral hemorrhage-associated diffusion-weighted lesions. Neurology. 2012;79(24):2335–41.PubMedPubMedCentral
12.
go back to reference Garg RK, Liebling SM, Maas MB, et al. Blood pressure reduction, decreased diffusion on MRI, and outcomes after intracerebral hemorrhage. Stroke. 2012;43(1):67–71.PubMed Garg RK, Liebling SM, Maas MB, et al. Blood pressure reduction, decreased diffusion on MRI, and outcomes after intracerebral hemorrhage. Stroke. 2012;43(1):67–71.PubMed
13.
go back to reference Ye XH, Gao T, Xu XH, et al. Factors associated with remote diffusion-weighted imaging lesions in spontaneous intracerebral hemorrhage. Front Neurol. 2018;9:209.PubMedPubMedCentral Ye XH, Gao T, Xu XH, et al. Factors associated with remote diffusion-weighted imaging lesions in spontaneous intracerebral hemorrhage. Front Neurol. 2018;9:209.PubMedPubMedCentral
14.
go back to reference Xu XH, Ye XH, Cai JS, et al. Association of renal dysfunction with remote diffusion-weighted imaging lesions and total burden of cerebral small vessel disease in patients with primary intracerebral hemorrhage. Front Aging Neurosci. 2018;10:171.PubMedPubMedCentral Xu XH, Ye XH, Cai JS, et al. Association of renal dysfunction with remote diffusion-weighted imaging lesions and total burden of cerebral small vessel disease in patients with primary intracerebral hemorrhage. Front Aging Neurosci. 2018;10:171.PubMedPubMedCentral
15.
go back to reference Xu XH, Ye XH, Li JW, et al. Association between remote diffusion-weighted imaging lesions and cerebral small vessel disease in primary intracerebral hemorrhage. Eur J Neurol. 2019;26(7):961–8.PubMed Xu XH, Ye XH, Li JW, et al. Association between remote diffusion-weighted imaging lesions and cerebral small vessel disease in primary intracerebral hemorrhage. Eur J Neurol. 2019;26(7):961–8.PubMed
16.
go back to reference 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. 2001;32(10):2426–32.PubMed 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. 2001;32(10):2426–32.PubMed
17.
go back to reference Yoon JA, Kim DY, Sohn MK, et al. Effect of stress hyperglycemia and intensive rehabilitation therapy in non-diabetic hemorrhagic stroke: Korean Stroke Cohort for Functioning and Rehabilitation. Eur J Neurol. 2016;23(11):1658–65.PubMed Yoon JA, Kim DY, Sohn MK, et al. Effect of stress hyperglycemia and intensive rehabilitation therapy in non-diabetic hemorrhagic stroke: Korean Stroke Cohort for Functioning and Rehabilitation. Eur J Neurol. 2016;23(11):1658–65.PubMed
18.
go back to reference Bejot Y, Aboa-Eboule C, Hervieu M, et al. The deleterious effect of admission hyperglycemia on survival and functional outcome in patients with intracerebral hemorrhage. Stroke. 2012;43(1):243–5.PubMed Bejot Y, Aboa-Eboule C, Hervieu M, et al. The deleterious effect of admission hyperglycemia on survival and functional outcome in patients with intracerebral hemorrhage. Stroke. 2012;43(1):243–5.PubMed
19.
go back to reference Saxena A, Anderson CS, Wang X, et al. Prognostic significance of hyperglycemia in acute intracerebral hemorrhage: the INTERACT2 Study. Stroke. 2016;47(3):682–8.PubMed Saxena A, Anderson CS, Wang X, et al. Prognostic significance of hyperglycemia in acute intracerebral hemorrhage: the INTERACT2 Study. Stroke. 2016;47(3):682–8.PubMed
20.
go back to reference Zheng J, Yu Z, Ma L, et al. Association between blood glucose and functional outcome in intracerebral hemorrhage: a systematic review and meta-analysis. World Neurosurg. 2018;114:S1878875018305552. Zheng J, Yu Z, Ma L, et al. Association between blood glucose and functional outcome in intracerebral hemorrhage: a systematic review and meta-analysis. World Neurosurg. 2018;114:S1878875018305552.
21.
go back to reference Guo X, Li H, Zhang Z, et al. Hyperglycemia and mortality risk in patients with primary intracerebral hemorrhage: a meta-analysis. Mol Neurobiol. 2016;53(4):2269–75.PubMed Guo X, Li H, Zhang Z, et al. Hyperglycemia and mortality risk in patients with primary intracerebral hemorrhage: a meta-analysis. Mol Neurobiol. 2016;53(4):2269–75.PubMed
22.
go back to reference Selvin E, Rawlings AM, Grams M, et al. Prognostic utility of fructosamine and glycated albumin for incident diabetes and microvascular complications. Lancet Diabetes Endocrinol. 2014;2(4):279.PubMedPubMedCentral Selvin E, Rawlings AM, Grams M, et al. Prognostic utility of fructosamine and glycated albumin for incident diabetes and microvascular complications. Lancet Diabetes Endocrinol. 2014;2(4):279.PubMedPubMedCentral
23.
go back to reference Roberts GW, Quinn SJ, Valentine N, et al. Relative hyperglycemia, a marker of critical illness: introducing the stress hyperglycemia ratio. J Clin Endocrinol Metab. 2015;100(12):4490–7.PubMed Roberts GW, Quinn SJ, Valentine N, et al. Relative hyperglycemia, a marker of critical illness: introducing the stress hyperglycemia ratio. J Clin Endocrinol Metab. 2015;100(12):4490–7.PubMed
24.
go back to reference Yang Y, Kim TH, Yoon KH, et al. The stress hyperglycemia ratio, an index of relative hyperglycemia, as a predictor of clinical outcomes after percutaneous coronary intervention. Int J Cardiol. 2017;241:57–63.PubMed Yang Y, Kim TH, Yoon KH, et al. The stress hyperglycemia ratio, an index of relative hyperglycemia, as a predictor of clinical outcomes after percutaneous coronary intervention. Int J Cardiol. 2017;241:57–63.PubMed
25.
go back to reference Greenberg SM, Charidimou A. Diagnosis of cerebral amyloid angiopathy: evolution of the Boston criteria. Stroke. 2018;49(2):491–7.PubMedPubMedCentral Greenberg SM, Charidimou A. Diagnosis of cerebral amyloid angiopathy: evolution of the Boston criteria. Stroke. 2018;49(2):491–7.PubMedPubMedCentral
26.
go back to reference Teo BW, Xu H, Wang D, et al. GFR estimating equations in a multiethnic Asian population. Am J Kidney Dis. 2011;58(1):56–63.PubMed Teo BW, Xu H, Wang D, et al. GFR estimating equations in a multiethnic Asian population. Am J Kidney Dis. 2011;58(1):56–63.PubMed
27.
go back to reference Coburn HJ, Carroll JJ. Improved manual and automated colorimetric determination of serum glucose, with use of hexokinase and glucose-6-phosphate dehydrogenase. Clin Chem. 1973;19(1):127–30.PubMed Coburn HJ, Carroll JJ. Improved manual and automated colorimetric determination of serum glucose, with use of hexokinase and glucose-6-phosphate dehydrogenase. Clin Chem. 1973;19(1):127–30.PubMed
28.
go back to reference Nathan DM, Kuenen J, Borg R, et al. Translating the A1C assay into estimated average glucose values. Diabetes Care. 2008;31(8):1473–8.PubMedPubMedCentral Nathan DM, Kuenen J, Borg R, et al. Translating the A1C assay into estimated average glucose values. Diabetes Care. 2008;31(8):1473–8.PubMedPubMedCentral
29.
go back to reference Greenberg SM, Vernooij MW, Cordonnier C, et al. Cerebral microbleeds: a guide to detection and interpretation. Lancet Neurol. 2009;8(2):165–74.PubMedPubMedCentral Greenberg SM, Vernooij MW, Cordonnier C, et al. Cerebral microbleeds: a guide to detection and interpretation. Lancet Neurol. 2009;8(2):165–74.PubMedPubMedCentral
30.
go back to reference Fazekas F, Barkhof F, Wahlund LO, et al. CT and MRI rating of white matter lesions. Cerebrovasc Dis. 2002;13(Suppl 2):31–6.PubMed Fazekas F, Barkhof F, Wahlund LO, et al. CT and MRI rating of white matter lesions. Cerebrovasc Dis. 2002;13(Suppl 2):31–6.PubMed
31.
go back to reference Maclullich AM, Wardlaw JM, Ferguson KJ, et al. Enlarged perivascular spaces are associated with cognitive function in healthy elderly men. J Neurol Neurosurg Psychiatry. 2004;75(11):1519–23.PubMedPubMedCentral Maclullich AM, Wardlaw JM, Ferguson KJ, et al. Enlarged perivascular spaces are associated with cognitive function in healthy elderly men. J Neurol Neurosurg Psychiatry. 2004;75(11):1519–23.PubMedPubMedCentral
32.
go back to reference Hansen TP, Cain J, Thomas O, Jackson A. Dilated perivascular spaces in the Basal Ganglia are a biomarker of small-vessel disease in a very elderly population with dementia. AJNR Am J Neuroradiol. 2015;36(5):893–8.PubMed Hansen TP, Cain J, Thomas O, Jackson A. Dilated perivascular spaces in the Basal Ganglia are a biomarker of small-vessel disease in a very elderly population with dementia. AJNR Am J Neuroradiol. 2015;36(5):893–8.PubMed
33.
go back to reference Lau KK, Li L, Schulz U, et al. Total small vessel disease score and risk of recurrent stroke: validation in 2 large cohorts. Neurology. 2017;88(24):2260–7.PubMedPubMedCentral Lau KK, Li L, Schulz U, et al. Total small vessel disease score and risk of recurrent stroke: validation in 2 large cohorts. Neurology. 2017;88(24):2260–7.PubMedPubMedCentral
34.
go back to reference Fan Z, Hao L, Juan Q, et al. Hyperglycemia is associated with island sign in patients with intracerebral hemorrhage. World Neurosurg. 2018;119:e703–9. Fan Z, Hao L, Juan Q, et al. Hyperglycemia is associated with island sign in patients with intracerebral hemorrhage. World Neurosurg. 2018;119:e703–9.
35.
go back to reference Zhang F, Li H, Qian J, et al. Hyperglycemia predicts blend sign in patients with intracerebral hemorrhage. Med Sci Monit. 2018;24:6237–44.PubMedPubMedCentral Zhang F, Li H, Qian J, et al. Hyperglycemia predicts blend sign in patients with intracerebral hemorrhage. Med Sci Monit. 2018;24:6237–44.PubMedPubMedCentral
36.
go back to reference Wu TY, Putaala J, Sharma G, et al. Persistent hyperglycemia is associated with increased mortality after intracerebral hemorrhage. J Am Heart Assoc. 2017;6(8):e005760.PubMedPubMedCentral Wu TY, Putaala J, Sharma G, et al. Persistent hyperglycemia is associated with increased mortality after intracerebral hemorrhage. J Am Heart Assoc. 2017;6(8):e005760.PubMedPubMedCentral
37.
go back to reference Wada S, Yoshimura S, Inoue M, et al. Outcome prediction in acute stroke patients by continuous glucose monitoring. J Am Heart Assoc. 2018;7(8):e008744.PubMedPubMedCentral Wada S, Yoshimura S, Inoue M, et al. Outcome prediction in acute stroke patients by continuous glucose monitoring. J Am Heart Assoc. 2018;7(8):e008744.PubMedPubMedCentral
38.
go back to reference Claude H, Greenberg SM, Anderson CS, et al. Guidelines for the management of spontaneous intracerebral hemorrhage: a guideline for healthcare professionals from the American Heart Association/American Stroke Association. Stroke J Cereb Circ. 2015;46(7):2032. Claude H, Greenberg SM, Anderson CS, et al. Guidelines for the management of spontaneous intracerebral hemorrhage: a guideline for healthcare professionals from the American Heart Association/American Stroke Association. Stroke J Cereb Circ. 2015;46(7):2032.
39.
go back to reference Prabhakaran S, Naidech AM. Ischemic brain injury after intracerebral hemorrhage: a critical review. Stroke. 2012;43(8):2258–63.PubMed Prabhakaran S, Naidech AM. Ischemic brain injury after intracerebral hemorrhage: a critical review. Stroke. 2012;43(8):2258–63.PubMed
40.
go back to reference Bosarge PL, Kerby JD. Stress-induced hyperglycemia: is it harmful following trauma? Adv Surg. 2013;47:287–97.PubMed Bosarge PL, Kerby JD. Stress-induced hyperglycemia: is it harmful following trauma? Adv Surg. 2013;47:287–97.PubMed
41.
go back to reference McCowen KC, Malhotra A, Bistrian BR. Stress-induced hyperglycemia. Crit Care Clin. 2001;17(1):107–24.PubMed McCowen KC, Malhotra A, Bistrian BR. Stress-induced hyperglycemia. Crit Care Clin. 2001;17(1):107–24.PubMed
42.
go back to reference Feibel JH, Hardy PM, Campbell RG, Goldstein MN, Joynt RJ. Prognostic value of the stress response following stroke. JAMA. 1977;238(13):1374–6.PubMed Feibel JH, Hardy PM, Campbell RG, Goldstein MN, Joynt RJ. Prognostic value of the stress response following stroke. JAMA. 1977;238(13):1374–6.PubMed
43.
go back to reference Huang YH, Chung CL, Tsai HP, et al. Hyperglycemia aggravates cerebral vasospasm after subarachnoid hemorrhage in a rat model. Neurosurgery. 2017;80(5):809–15.PubMed Huang YH, Chung CL, Tsai HP, et al. Hyperglycemia aggravates cerebral vasospasm after subarachnoid hemorrhage in a rat model. Neurosurgery. 2017;80(5):809–15.PubMed
44.
go back to reference Ago T, Matsuo R, Hata J, et al. Insulin resistance and clinical outcomes after acute ischemic stroke. Neurology. 2018;90(17):e1470–7.PubMed Ago T, Matsuo R, Hata J, et al. Insulin resistance and clinical outcomes after acute ischemic stroke. Neurology. 2018;90(17):e1470–7.PubMed
46.
go back to reference Kosiborod M. Blood glucose and its prognostic implications in patients hospitalised with acute myocardial infarction. Diab Vasc Dis Res. 2008;5(4):269–75.PubMed Kosiborod M. Blood glucose and its prognostic implications in patients hospitalised with acute myocardial infarction. Diab Vasc Dis Res. 2008;5(4):269–75.PubMed
47.
go back to reference Wu TY, Putaala J, Sharma G, et al. Persistent hyperglycemia is associated with increased mortality after intracerebral hemorrhage. J Am Heart Assoc. 2017;6(8):e005760.PubMedPubMedCentral Wu TY, Putaala J, Sharma G, et al. Persistent hyperglycemia is associated with increased mortality after intracerebral hemorrhage. J Am Heart Assoc. 2017;6(8):e005760.PubMedPubMedCentral
Metadata
Title
Stress-Induced Hyperglycemia and Remote Diffusion-Weighted Imaging Lesions in Primary Intracerebral Hemorrhage
Authors
Xiang-hua Ye
Xue-li Cai
Dong-liang Nie
Ye-jun Chen
Jia-wen Li
Xu-hua Xu
Jin-song Cai
Zhi-rong Liu
Xin-zhen Yin
Shui-jiang Song
Lu-sha Tong
Feng Gao
Publication date
01-04-2020
Publisher
Springer US
Published in
Neurocritical Care / Issue 2/2020
Print ISSN: 1541-6933
Electronic ISSN: 1556-0961
DOI
https://doi.org/10.1007/s12028-019-00747-y

Other articles of this Issue 2/2020

Neurocritical Care 2/2020 Go to the issue