Prediction of short-term poor prognosis in patients with lacunar infarction based on superoxide dismutase combined with serum amyloid A_West China Medical Journal

Authors：

YE Sheng ¹ , QIN Yu ² , LI Weijia ³ , TANG Xiaolei ⁴ , XING Jingjing ¹ , PAN Huiqing ¹ ,  XU Li ⁵

1. Emergency Department, the Second Affiliated Hospital of Wannan Medical College, Wuhu, Anhui 241000, P. R. China;
2. Graduate School, Wannan Medical College, Wuhu, Anhui 241000, P. R. China;
3. School of Clinical Medicine, Wannan Medical College, Wuhu, Anhui 241000, P. R. China;
4. Translational Medicine Centre, the Second Affiliated Hospital of Wannan Medical College, Wuhu, Anhui 241000, P. R. China;
5. Neurology Department, the Second Affiliated Hospital of Wannan Medical College, Wuhu, Anhui 241000, P. R. China;

Corresponding author：

XU Li, Email: xuli19822002@163.com

Keywords：

Lacunar infarction; superoxide dismutase; serum amyloid A; neurological function; predictive power

DOI：

10.7507/1002-0179.202210152

Video：

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Objective To explore the predictive value of superoxide dismutase (SOD) and serum amyloid A (SAA) in short-term poor prognosis in patients with lacunar infarction. Methods The clinical data of 185 patients who were diagnosed with lacunar infarction in the Second Affiliated Hospital of Wannan Medical College between January 1st and December 31st, 2021 were analyzed retrospectively. According to the modified Rankin Scale (mRS) score 3 months after discharge, the patients were divided into the good prognostic group (mRS≤2) and the poor prognostic group (mRS>2). Multiple logistic regression was used to analyze the independent risk factors of the short-term adverse prognosis of patients with lacunar infarction, and a risk prediction model (nomograph) was constructed. The predictive efficacy of SOD, SAA and nomograph for poor prognosis was analyzed by using the receiver operating characteristic curve. Calibration curve and decision curve analysis were used to evaluate the differentiation and clinical application value of the model. Results A total of 185 lacunar cerebral infarction patients with a mean age of (68.26±10.77) years were enrolled in this study, among whom 80 (43.2%) were males and 39 (21.1%) had adverse prognosis. Multiple logistic regression analysis showed that systolic blood pressure [odds ratio (OR)=1.028, 95% confidence interval (CI) (1.004, 1.052), P=0.021], diabetes [OR=4.939, 95%CI (1.703, 14.320), P=0.003], SAA [OR=1.089, 95%CI (1.052, 1.128), P<0.001], apolipoprotein B [OR=7.647, 95%CI (2.186, 26.753), P=0.001] were independent risk factors for poor prognosis in lacunar infarction patients, while the level of SOD [OR=0.979, 95%CI (0.965, 0.994), P=0.006] was a protective factor. The area under the curve of the nomograph for predicting the short term poor prognosis was 0.874 [95%CI (0.812, 0.936), P<0.001]. The goodness-of-fit test with the calibration curve indicated that the prediction probability was consistent with the actual occurrence probability (Hosmer-Lemeshow test P=0.295), and the decision curve indicated that the nomograph had good clinical application value. Conclusion SAA and SOD have good predictive value for short-term adverse prognosis of lacunar cerebral infarction patients, and the nomograph constructed based on them has a good differentiation and consistency, which can provide a basis for clinicians to evaluate the prognosis of lacunar cerebral infarction patients.

Citation： YE Sheng, QIN Yu, LI Weijia, TANG Xiaolei, XING Jingjing, PAN Huiqing, XU Li. Prediction of short-term poor prognosis in patients with lacunar infarction based on superoxide dismutase combined with serum amyloid A. West China Medical Journal, 2022, 37(11): 1623-1629. doi: 10.7507/1002-0179.202210152 Copy

1.	Cannistraro RJ, Badi M, Eidelman BH, et al. CNS small vessel disease: a clinical review. Neurology, 2019, 92(24): 1146-1156.
2.	Jiménez-Balado J, Riba-Llena I, Abril O, et al. Cognitive impact of cerebral small vessel disease changes in patients with hypertension. Hypertension, 2019, 73(2): 342-349.
3.	Chojdak-Łukasiewicz J, Dziadkowiak E, Zimny A, et al. Cerebral small vessel disease: a review. Adv Clin Exp Med, 2021, 30(3): 349-356.
4.	Fan H, Yang S, Li Y, et al. Assessment of homocysteine as a diagnostic and early prognostic biomarker for patients with acute lacunar infarction. Eur Neurol, 2018, 79(1/2): 54-62.
5.	Mantero V, Scaccabarozzi C, Botto E, et al. Outcome in lacunar stroke: a cohort study. Acta Neurol Scand, 2018, 138(4): 320-326.
6.	Aldriweesh MA, Alluhidan WA, Al Bdah BA, et al. Prevalence and clinical characteristics of lacunar stroke: a hospital-based study. Brain Sci, 2021, 11(11): 1466.
7.	Cao X, Chen P. Changes in serum amyloid A (SAA) and 8-OHdG in patients with senile early cognitive impairment. Med Sci Monit, 2020, 26: e919586.
8.	Asmah RH, Sackey P, Adjei P, et al. Haematological indices and antioxidant enzyme activity in ghanaian stroke patients. Biomed Res Int, 2022, 2022: 1203120.
9.	Schweizer J, Bustamante A, Lapierre-Fétaud V, et al. SAA (serum amyloid A): a novel predictor of stroke-associated infections. Stroke, 2020, 51(12): 3523-3530.
10.	Tao L, ShiChuan W, DeTai Z, et al. Evaluation of lipoprotein-associated phospholipase A2, serum amyloid A, and fibrinogen as diagnostic biomarkers for patients with acute cerebral infarction. J Clin Lab Anal, 2020, 34(3): e23084.
11.	Zhang Y, Feng Y, Zuo J, et al. Elevated serum amyloid A is associated with cognitive impairment in ischemic stroke patients. Front Neurol, 2022, 12: 789204.
12.	Zhang MS, Liang JH, Yang MJ, et al. Low serum superoxide dismutase is associated with a high risk of cognitive impairment after mild acute ischemic stroke. Front Aging Neurosci, 2022, 14: 834114.
13.	Kwan A, Wei J, Dowling NM, et al. Cognitive impairment after lacunar stroke and the risk of recurrent stroke and death. Cerebrovasc Dis, 2021, 50(4): 383-389.
14.	Crosta F, Occhiuzzi U, Passalacqua G, et al. Association between the serum uric acid levels and lacunar infarcts in the elderly. J Mol Neurosci, 2018, 65(3): 385-390.
15.	Su JH, Meng LW, Dong D, et al. Noninvasive model for predicting future ischemic strokes in patients with silent lacunar infarction using radiomics. BMC Med Imaging, 2020, 20(1): 77.
16.	Wu B, Lin S, Hao Z, et al. Proportion, risk factors and outcome of lacunar infarction: a hospital-based study in a Chinese population. Cerebrovasc Dis, 2010, 29(2): 181-187.
17.	Fang XH, Wang WH, Zhang XQ, et al. Incidence and survival of symptomatic lacunar infarction in a Beijing population: a 6-year prospective study. Eur J Neurol, 2012, 19(8): 1114-1120.
18.	Makin SD, Turpin S, Dennis MS, et al. Cognitive impairment after lacunar stroke: systematic review and meta-analysis of incidence, prevalence and comparison with other stroke subtypes. J Neurol Neurosurg Psychiatry, 2013, 84(8): 893-900.
19.	Arboix A, Martí-Vilalta JL. Lacunar stroke. Expert Rev Neurother, 2009, 9(2): 179-196.
20.	Lau LH, Lew J, Borschmann K, et al. Prevalence of diabetes and its effects on stroke outcomes: a meta-analysis and literature review. J Diabetes Investig, 2019, 10(3): 780-792.
21.	Piernik-Yoder B, Ketchum N. Rehabilitation outcomes of stroke patients with and without diabetes. Arch Phys Med Rehabil, 2013, 94(8): 1508-1512.
22.	Liu J, Rutten-Jacobs L, Liu M, et al. Causal impact of type 2 diabetes mellitus on cerebral small vessel disease: a mendelian randomization analysis. Stroke, 2018, 49(6): 1325-1331.
23.	Cukierman-Yaffe T, McClure LA, Risoli T, et al. The relationship between glucose control and cognitive function in people with diabetes after a lacunar stroke. J Clin Endocrinol Metab, 2021, 106(4): e1521-e1528.
24.	van Sloten TT, Sedaghat S, Carnethon MR, et al. Cerebral microvascular complications of type 2 diabetes: stroke, cognitive dysfunction, and depression. Lancet Diabetes Endocrinol, 2020, 8(4): 325-336.
25.	Megherbi SE, Milan C, Minier D, et al. Association between diabetes and stroke subtype on survival and functional outcome 3 months after stroke: data from the European BIOMED Stroke Project. Stroke, 2003, 34(3): 688-694.
26.	Blanco M, Castellanos M, Rodríguez-Yáñez M, et al. High blood pressure and inflammation are associated with poor prognosis in lacunar infarctions. Cerebrovasc Dis, 2006, 22(2/3): 123-129.
27.	Yang S, Yuan J, Qin W, et al. Twenty-four-hour ambulatory blood pressure variability is associated with total magnetic resonance imaging burden of cerebral small-vessel disease. Clin Interv Aging, 2018, 13: 1419-1427.
28.	White CL, Pergola PE, Szychowski JM, et al. Blood pressure after recent stroke: baseline findings from the secondary prevention of small subcortical strokes trial. Am J Hypertens, 2013, 26(9): 1114-1122.
29.	Kalani R, Krishnamoorthy S, Deepa D, et al. Apolipoproteins B and A1 in ischemic stroke subtypes. J Stroke Cerebrovasc Dis, 2020, 29(4): 104670.
30.	Yuan S, Tang B, Zheng J, et al. Circulating lipoprotein lipids, apolipoproteins and ischemic stroke. Ann Neurol, 2020, 88(6): 1229-1236.
31.	Rallidis LS, Vikelis M, Panagiotakos DB, et al. Inflammatory markers and in-hospital mortality in acute ischaemic stroke. Atherosclerosis, 2006, 189(1): 193-197.
32.	Tölle M, Huang T, Schuchardt M, et al. High-density lipoprotein loses its anti-inflammatory capacity by accumulation of pro-inflammatory-serum amyloid A. Cardiovasc Res, 2012, 94(1): 154-162.
33.	Song C, Hsu K, Yamen E, et al. Serum amyloid A induction of cytokines in monocytes/macrophages and lymphocytes. Atherosclerosis, 2009, 207(2): 374-383.
34.	Huang HF, Guo F, Cao YZ, et al. Neuroprotection by manganese superoxide dismutase (MnSOD) mimics: antioxidant effect and oxidative stress regulation in acute experimental stroke. CNS Neurosci Ther, 2012, 18(10): 811-818.
35.	Broughton BR, Reutens DC, Sobey CG. Apoptotic mechanisms after cerebral ischemia. Stroke, 2009, 40(5): e331-e339.
36.	Ciancarelli I, Di Massimo C, De Amicis D, et al. Uric acid and Cu/Zn superoxide dismutase: potential strategies and biomarkers in functional recovery of post-acute ischemic stroke patients after intensive neurorehabilitation. Curr Neurovasc Res, 2015, 12(2): 120-127.

1. Cannistraro RJ, Badi M, Eidelman BH, et al. CNS small vessel disease: a clinical review. Neurology, 2019, 92(24): 1146-1156.
2. Jiménez-Balado J, Riba-Llena I, Abril O, et al. Cognitive impact of cerebral small vessel disease changes in patients with hypertension. Hypertension, 2019, 73(2): 342-349.
3. Chojdak-Łukasiewicz J, Dziadkowiak E, Zimny A, et al. Cerebral small vessel disease: a review. Adv Clin Exp Med, 2021, 30(3): 349-356.
4. Fan H, Yang S, Li Y, et al. Assessment of homocysteine as a diagnostic and early prognostic biomarker for patients with acute lacunar infarction. Eur Neurol, 2018, 79(1/2): 54-62.
5. Mantero V, Scaccabarozzi C, Botto E, et al. Outcome in lacunar stroke: a cohort study. Acta Neurol Scand, 2018, 138(4): 320-326.
6. Aldriweesh MA, Alluhidan WA, Al Bdah BA, et al. Prevalence and clinical characteristics of lacunar stroke: a hospital-based study. Brain Sci, 2021, 11(11): 1466.
7. Cao X, Chen P. Changes in serum amyloid A (SAA) and 8-OHdG in patients with senile early cognitive impairment. Med Sci Monit, 2020, 26: e919586.
8. Asmah RH, Sackey P, Adjei P, et al. Haematological indices and antioxidant enzyme activity in ghanaian stroke patients. Biomed Res Int, 2022, 2022: 1203120.
9. Schweizer J, Bustamante A, Lapierre-Fétaud V, et al. SAA (serum amyloid A): a novel predictor of stroke-associated infections. Stroke, 2020, 51(12): 3523-3530.
10. Tao L, ShiChuan W, DeTai Z, et al. Evaluation of lipoprotein-associated phospholipase A2, serum amyloid A, and fibrinogen as diagnostic biomarkers for patients with acute cerebral infarction. J Clin Lab Anal, 2020, 34(3): e23084.
11. Zhang Y, Feng Y, Zuo J, et al. Elevated serum amyloid A is associated with cognitive impairment in ischemic stroke patients. Front Neurol, 2022, 12: 789204.
12. Zhang MS, Liang JH, Yang MJ, et al. Low serum superoxide dismutase is associated with a high risk of cognitive impairment after mild acute ischemic stroke. Front Aging Neurosci, 2022, 14: 834114.
13. Kwan A, Wei J, Dowling NM, et al. Cognitive impairment after lacunar stroke and the risk of recurrent stroke and death. Cerebrovasc Dis, 2021, 50(4): 383-389.
14. Crosta F, Occhiuzzi U, Passalacqua G, et al. Association between the serum uric acid levels and lacunar infarcts in the elderly. J Mol Neurosci, 2018, 65(3): 385-390.
15. Su JH, Meng LW, Dong D, et al. Noninvasive model for predicting future ischemic strokes in patients with silent lacunar infarction using radiomics. BMC Med Imaging, 2020, 20(1): 77.
16. Wu B, Lin S, Hao Z, et al. Proportion, risk factors and outcome of lacunar infarction: a hospital-based study in a Chinese population. Cerebrovasc Dis, 2010, 29(2): 181-187.
17. Fang XH, Wang WH, Zhang XQ, et al. Incidence and survival of symptomatic lacunar infarction in a Beijing population: a 6-year prospective study. Eur J Neurol, 2012, 19(8): 1114-1120.
18. Makin SD, Turpin S, Dennis MS, et al. Cognitive impairment after lacunar stroke: systematic review and meta-analysis of incidence, prevalence and comparison with other stroke subtypes. J Neurol Neurosurg Psychiatry, 2013, 84(8): 893-900.
19. Arboix A, Martí-Vilalta JL. Lacunar stroke. Expert Rev Neurother, 2009, 9(2): 179-196.
20. Lau LH, Lew J, Borschmann K, et al. Prevalence of diabetes and its effects on stroke outcomes: a meta-analysis and literature review. J Diabetes Investig, 2019, 10(3): 780-792.
21. Piernik-Yoder B, Ketchum N. Rehabilitation outcomes of stroke patients with and without diabetes. Arch Phys Med Rehabil, 2013, 94(8): 1508-1512.
22. Liu J, Rutten-Jacobs L, Liu M, et al. Causal impact of type 2 diabetes mellitus on cerebral small vessel disease: a mendelian randomization analysis. Stroke, 2018, 49(6): 1325-1331.
23. Cukierman-Yaffe T, McClure LA, Risoli T, et al. The relationship between glucose control and cognitive function in people with diabetes after a lacunar stroke. J Clin Endocrinol Metab, 2021, 106(4): e1521-e1528.
24. van Sloten TT, Sedaghat S, Carnethon MR, et al. Cerebral microvascular complications of type 2 diabetes: stroke, cognitive dysfunction, and depression. Lancet Diabetes Endocrinol, 2020, 8(4): 325-336.
25. Megherbi SE, Milan C, Minier D, et al. Association between diabetes and stroke subtype on survival and functional outcome 3 months after stroke: data from the European BIOMED Stroke Project. Stroke, 2003, 34(3): 688-694.
26. Blanco M, Castellanos M, Rodríguez-Yáñez M, et al. High blood pressure and inflammation are associated with poor prognosis in lacunar infarctions. Cerebrovasc Dis, 2006, 22(2/3): 123-129.
27. Yang S, Yuan J, Qin W, et al. Twenty-four-hour ambulatory blood pressure variability is associated with total magnetic resonance imaging burden of cerebral small-vessel disease. Clin Interv Aging, 2018, 13: 1419-1427.
28. White CL, Pergola PE, Szychowski JM, et al. Blood pressure after recent stroke: baseline findings from the secondary prevention of small subcortical strokes trial. Am J Hypertens, 2013, 26(9): 1114-1122.
29. Kalani R, Krishnamoorthy S, Deepa D, et al. Apolipoproteins B and A1 in ischemic stroke subtypes. J Stroke Cerebrovasc Dis, 2020, 29(4): 104670.
30. Yuan S, Tang B, Zheng J, et al. Circulating lipoprotein lipids, apolipoproteins and ischemic stroke. Ann Neurol, 2020, 88(6): 1229-1236.
31. Rallidis LS, Vikelis M, Panagiotakos DB, et al. Inflammatory markers and in-hospital mortality in acute ischaemic stroke. Atherosclerosis, 2006, 189(1): 193-197.
32. Tölle M, Huang T, Schuchardt M, et al. High-density lipoprotein loses its anti-inflammatory capacity by accumulation of pro-inflammatory-serum amyloid A. Cardiovasc Res, 2012, 94(1): 154-162.
33. Song C, Hsu K, Yamen E, et al. Serum amyloid A induction of cytokines in monocytes/macrophages and lymphocytes. Atherosclerosis, 2009, 207(2): 374-383.
34. Huang HF, Guo F, Cao YZ, et al. Neuroprotection by manganese superoxide dismutase (MnSOD) mimics: antioxidant effect and oxidative stress regulation in acute experimental stroke. CNS Neurosci Ther, 2012, 18(10): 811-818.
35. Broughton BR, Reutens DC, Sobey CG. Apoptotic mechanisms after cerebral ischemia. Stroke, 2009, 40(5): e331-e339.
36. Ciancarelli I, Di Massimo C, De Amicis D, et al. Uric acid and Cu/Zn superoxide dismutase: potential strategies and biomarkers in functional recovery of post-acute ischemic stroke patients after intensive neurorehabilitation. Curr Neurovasc Res, 2015, 12(2): 120-127.

West China Medical Journal

Prediction of short-term poor prognosis in patients with lacunar infarction based on superoxide dismutase combined with serum amyloid A

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