Relationship between age-adjusted Charlson comorbidity index and ischemic stroke in patients with ophthalmic artery occlusion or retinal artery occlusion_Chinese Journal of Ocular Fundus Diseases

Authors：

Yao Yufeng ^1,2 , Chen Zhenyu ^2,3 , Liang Huixian ^1,4 , Wang Jing ⁵ , Luo Tianyi ^1,4 , Song Qiyuan ^1,4 , Zhong Ying ¹ ,  Dou Xiaoyan ¹

1. Department of Ophthalmology, Shenzhen Second People's Hospital, Shenzhen 518035, China;
2. Shantou University Medical College, Shantou 515031, China;
3. Department of Cardiovascular Medicine, Shenzhen Second People's Hospital, Shenzhen 518035, China;
4. Department of Clinical Medicine, Division of Medicine, Shenzhen University, Shenzhen 518037, China;
5. Department of Cardiovascular Medicine, Shenzhen Second People's Hospital, Shenzhen 518035, China;

Corresponding author：

Dou Xiaoyan, Email: douxy08@163.com

Keywords：

Age-adjusted Charlson comorbidity index; Ophthalmic artery occlusion; Retinal artery occlusion; Ischemic stroke

DOI：

10.3760/cma.j.cn511434-20220623-00382

Video：

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Objective To investigate the relationship between age-adjusted Charlson comorbidity index (aCCI) and ischemic stroke in patients with ophthalmic artery occlusion (OAO) or retinal artery occlusion (RAO). Methods A single center retrospective cohort study. Seventy-four patients with OAO or RAO diagnosed by ophthalmology examination in Shenzhen Second People's Hospital from June 2004 to December 2020 were included in the study. The baseline information of patients were collected and aCCI was used to score the patients’ comorbidity. The outcome was ischemic stroke. The median duration of follow-up was 1 796.5 days. According to the maximum likelihood ratio of the two-piecewise COX regression model and the recursive algorithm, the aCCI inflection point value was determined to be 6, and the patients were divided into low aCCI group (＜6 points) and high aCCI group (≥6 points). A Cox regression model was used to quantify the association between baseline aCCI and ischemic stroke. Results Among the 74 patients, 53 were males and 21 were females, with the mean age of (55.22±14.18) (19-84) years. There were 9 patients of OAO and 65 patients of RAO. The aCCI value ranges from 1 to 10 points, with a median of 3 points. There were 63 patients (85.14%, 63/74) in the low aCCI group and 11 patients (14.86%, 11/74) in the high aCCI group. Since 2 patients could not determine the time from baseline to the occurrence of outcome events, 72 patients were included for Cox regression analysis. The results showed that 16 patients (22.22%, 16/72) had ischemic stroke in the future. The baseline aCCI in the low aCCI group was significantly associated with ischemic stroke [hazard ratio (HR)=1.76, 95% confidence interval (CI) 1.21-2.56, P=0.003], and for every 1 point increase in baseline aCCI, the risk of future ischemic stroke increased by 76% on average. The baseline aCCI in the high aCCI group had no significant correlation with the ischemic stroke (HR=0.66, 95%CI 0.33-1.33, P=0.247). Conclusions aCCI score is an important prognostic information for patients with OAO or RAO. A higher baseline aCCI score predicts a higher risk of ischemic stroke, and the association has a saturation effect.

Citation： Yao Yufeng, Chen Zhenyu, Liang Huixian, Wang Jing, Luo Tianyi, Song Qiyuan, Zhong Ying, Dou Xiaoyan. Relationship between age-adjusted Charlson comorbidity index and ischemic stroke in patients with ophthalmic artery occlusion or retinal artery occlusion. Chinese Journal of Ocular Fundus Diseases, 2023, 39(5): 387-393. doi: 10.3760/cma.j.cn511434-20220623-00382 Copy

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5.	O'Donnell MJ, Xavier D, Liu L, et al. Risk factors for ischaemic and intracerebral haemorrhagic stroke in 22 countries (the INTERSTROKE study): a case-control study[J]. Lancet, 2010, 376(9735): 112-123. DOI: 10.1016/S0140-6736(10)60834-3.
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8.	Palnum KD, Petersen P, Sorensen HT, et al. Older patients with acute stroke in Denmark: quality of care and short-term mortality. A nationwide follow-up study[J]. Age Ageing, 2008, 37(1): 90-95. DOI: 10.1093/ageing/afm134.
9.	Koppie TM, Serio AM, Vickers AJ, et al. Age-adjusted Charlson comorbidity score is associated with treatment decisions and clinical outcomes for patients undergoing radical cystectomy for bladder cancer[J]. Cancer, 2008, 112(11): 2384-2392. DOI: 10.1002/cncr.23462.
10.	Sewell K, Tse T, Harris E, et al. Pre-existing comorbidity burden and patient perceived stroke impact[J]. Int J Stroke, 2021, 16(3): 273-279. DOI: 10.1177/1747493020920838.
11.	Ofori-Asenso R, Zomer E, Chin KL, et al. Effect of comorbidity assessed by the Charlson comorbidity index on the length of stay, costs and mortality among older adults hospitalised for acute stroke[J]. Int J Environ Res Public Health, 2018, 15(11): 2532. DOI: 10.3390/ijerph15112532.
12.	Kahl A, du Bois A, Harter P, et al. Prognostic value of the age-adjusted Charlson comorbidity index (aCCI) on short- and long-term outcome in patients with advanced primary epithelial ovarian cancer[J]. Ann Surg Oncol, 2017, 24(12): 3692-3699. DOI: 10.1245/s10434-017-6079-9.
13.	Shinkawa H, Tanaka S, Takemura S, et al. Predictive value of the age-adjusted Charlson comorbidity index for outcomes after hepatic resection of hepatocellular carcinoma[J]. World J Surg, 2020, 44(11): 3901-3914. DOI: 10.1007/s00268-020-05686-w.
14.	Maezawa Y, Aoyama T, Kano K, et al. Impact of the age-adjusted Charlson comorbidity index on the short- and long-term outcomes of patients undergoing curative gastrectomy for gastric cancer[J]. J Cancer, 2019, 10(22): 5527-5535. DOI: 10.7150/jca.35465.
15.	Flaxel CJ, Adelman RA, Bailey ST, et al. Retinal and ophthalmic artery occlusions preferred practice pattern(R)[J]. Ophthalmology, 2020, 127(2): 259-287. DOI: 10.1016/j.ophtha.2019.09.028.
16.	Grant EG, Benson CB, Moneta GL, et al. Carotid artery stenosis: gray-scale and Doppler US Diagnosis-Society of Radiologists in Ultrasound Consensus Conference[J]. Radiology, 2003, 229(2): 340-346. DOI: 10.1148/radiol.2292030516.
17.	Charlson M, Szatrowski TP, Peterson J, et al. Validation of a combined comorbidity index[J]. J Clin Epidemiol, 1994, 47(11): 1245-1251. DOI: 10.1016/0895-4356(94)90129-5.
18.	彭斌, 吴波. 中国急性缺血性脑卒中诊治指南2018[J]. 中华神经科杂志, 2018, 51(9): 666-682. DOI: 10.3760/cma.j.issn.1006-7876.2018.09.004.Peng B, Wu B. Chinese guidelines for diagnosis and treatment of acute ischemic stroke 2018[J]. Chin J Neurol, 2018, 51(9): 666-682. DOI: 10.3760/cma.j.issn.1006-7876.2018.09.004.
19.	王陇德, 彭斌, 张鸿祺, 等. 《中国脑卒中防治报告2020》概要[J]. 中国脑血管病杂志, 2022, 19(2): 136-144. DOI: 10.3969/j.issn.1672-5921.2022.02.011.Wang LD, Peng B, Zhang HQ, et al. Brief report on stroke prevention and treatment in China, 2020[J]. Chin J Cerebrovasc Dis, 2022, 19(2): 136-144. DOI: 10.3969/j.issn.1672-5921.2022.02.011.
20.	Chodnicki KD, Pulido JS, Hodge DO, et al. Stroke risk before and after central retinal artery occlusion in a US cohort[J]. Mayo Clin Proc, 2019, 94(2): 236-241. DOI: 10.1016/j.mayocp.2018.10.018.
21.	Mir TA, Arham AZ, Fang W, et al. Acute vascular ischemic events in patients with central retinal artery occlusion in the United States: a nationwide study 2003-2014[J]. Am J Ophthalmol, 2019, 200: 179-186. DOI: 10.1016/j.ajo.2019.01.009.
22.	Avery MB, Magal I, Kherani A, et al. Risk of stroke in patients with ocular arterial occlusive disorders: a retrospective Canadian study[J/OL]. J Am Heart Assoc, 2019, 8(3): e010509[2019-02-05]. https://europepmc.org/article/MED/30712440. DOI: 10.1161/JAHA.118.010509.
23.	French DD, Margo CE, Greenberg PB. Ischemic stroke risk in medicare beneficiaries with central retinal artery occlusion: a retrospective cohort study[J]. Ophthalmol Ther, 2018, 7(1): 125-131. DOI: 10.1007/s40123-018-0126-x.
24.	李曼. 眼缺血综合征与缺血性脑卒中相关性研究进展[J]. 山东大学耳鼻喉眼学报, 2022, 36(5): 88-92, 99. DOI: 10.6040/j.issn.1673-3770.0.2021.185.Li M. Association between ocular ischemic syndrome and ischemic stroke[J]. Journal of Otolaryngology and Ophthalmology of Shandong University, 2022, 36(5): 88-92, 99. DOI: 10.6040/j.issn.1673-3770.0.2021.185.
25.	王敏, 王升, 陈小瑾, 等. 缺血性眼病与缺血性脑卒中发生的相关性研究[J]. 中华眼底病杂志, 2012, 28(2): 177-178. DOI: 10.3760/cma.j.issn.1005-1015.2012.02.021.Wang M, Wang S, Chen XJ, et al. Research on the relationship between ischemic ophthalmopathy and ischemic stroke[J]. Chin J Ocul Fundus Dis, 2012, 28(2): 177-178. DOI: 10.3760/cma.j.issn.1005-1015.2012.02.021.
26.	赵军, 胡莲娜, 魏世辉. 眼缺血性疾病对预测颈动脉狭窄发生的意义[J]. 国际眼科杂志, 2009, 9(2): 361-362. DOI: 10.3969/j.issn.1672-5123.2009.02.047.Zhao J, Hu LN, Wei SH. Clinical significance of ocular ischemia disease on predicted the happening of carotid stenosis[J]. Int J Ophthalmol, 2009, 9(2): 361-362. DOI: 10.3969/j.issn.1672-5123.2009.02.047.
27.	Zhang F, Bharadwaj A, Mohamed MO, et al. Impact of Charlson co-morbidity index score on management and outcomes after acute coronary syndrome[J]. Am J Cardiol, 2020, 130: 15-23. DOI: 10.1016/j.amjcard.2020.06.022.
28.	Chuang MH, Chuang TL, Huang KY, et al. Age-adjusted Charlson comorbidity index scores predict major adverse cardiovascular events and all-cause mortality among systemic lupus erythematosus patients[J]. Ci Ji Yi Xue Za Zhi, 2017, 29(3): 154-158. DOI: 10.4103/tcmj.tcmj_57_17.
29.	Schmidt M, Jacobsen J B, Johnsen SP, et al. Eighteen-year trends in stroke mortality and the prognostic influence of comorbidity[J]. Neurology, 2014, 82(4): 340-350. DOI: 10.1212/WNL.0000000000000062.
30.	Fischer U, Mono M L, Zwahlen M, et al. Impact of thrombolysis on stroke outcome at 12 months in a population: the Bern stroke project[J]. Stroke, 2012, 43(4): 1039-1045. DOI: 10.1161/STROKEAHA.111.630384.

1. Hayreh SS. Ocular vascular occlusive disorders: natural history of visual outcome[J]. Prog Retin Eye Res, 2014, 41: 1-25. DOI: 10.1016/j.preteyeres.2014.04.001.
2. Park SJ, Choi NK, Yang BR, et al. Risk and risk periods for stroke and acute myocardial infarction in patients with central retinal artery occlusion[J]. Ophthalmology, 2015, 122(11): 2336-2343. DOI: 10.1016/j.ophtha.2015.07.018.
3. Helenius J, Arsava EM, Goldstein JN, et al. Concurrent acute brain infarcts in patients with monocular visual loss[J]. Ann Neurol, 2012, 72(2): 286-293. DOI: 10.1002/ana.23597.
4. Callizo J, Feltgen N, Pantenburg S, et al. Cardiovascular risk factors in central retinal artery occlusion: results of a prospective and standardized medical examination[J]. Ophthalmology, 2015, 122(9): 1881-1888. DOI: 10.1016/j.ophtha.2015.05.044.
5. O'Donnell MJ, Xavier D, Liu L, et al. Risk factors for ischaemic and intracerebral haemorrhagic stroke in 22 countries (the INTERSTROKE study): a case-control study[J]. Lancet, 2010, 376(9735): 112-123. DOI: 10.1016/S0140-6736(10)60834-3.
6. Kisialiou A, Grella R, Carrizzo A, et al. Risk factors and acute ischemic stroke subtypes[J]. J Neurol Sci, 2014, 339(1-2): 41-46. DOI: 10.1016/j.jns.2014.01.014.
7. Vogeli C, Shields AE, Lee TA, et al. Multiple chronic conditions: prevalence, health consequences, and implications for quality, care management, and costs[J]. J Gen Intern Med, 2007, 22 Suppl 3: S391-395. DOI: 10.1007/s11606-007-0322-1.
8. Palnum KD, Petersen P, Sorensen HT, et al. Older patients with acute stroke in Denmark: quality of care and short-term mortality. A nationwide follow-up study[J]. Age Ageing, 2008, 37(1): 90-95. DOI: 10.1093/ageing/afm134.
9. Koppie TM, Serio AM, Vickers AJ, et al. Age-adjusted Charlson comorbidity score is associated with treatment decisions and clinical outcomes for patients undergoing radical cystectomy for bladder cancer[J]. Cancer, 2008, 112(11): 2384-2392. DOI: 10.1002/cncr.23462.
10. Sewell K, Tse T, Harris E, et al. Pre-existing comorbidity burden and patient perceived stroke impact[J]. Int J Stroke, 2021, 16(3): 273-279. DOI: 10.1177/1747493020920838.
11. Ofori-Asenso R, Zomer E, Chin KL, et al. Effect of comorbidity assessed by the Charlson comorbidity index on the length of stay, costs and mortality among older adults hospitalised for acute stroke[J]. Int J Environ Res Public Health, 2018, 15(11): 2532. DOI: 10.3390/ijerph15112532.
12. Kahl A, du Bois A, Harter P, et al. Prognostic value of the age-adjusted Charlson comorbidity index (aCCI) on short- and long-term outcome in patients with advanced primary epithelial ovarian cancer[J]. Ann Surg Oncol, 2017, 24(12): 3692-3699. DOI: 10.1245/s10434-017-6079-9.
13. Shinkawa H, Tanaka S, Takemura S, et al. Predictive value of the age-adjusted Charlson comorbidity index for outcomes after hepatic resection of hepatocellular carcinoma[J]. World J Surg, 2020, 44(11): 3901-3914. DOI: 10.1007/s00268-020-05686-w.
14. Maezawa Y, Aoyama T, Kano K, et al. Impact of the age-adjusted Charlson comorbidity index on the short- and long-term outcomes of patients undergoing curative gastrectomy for gastric cancer[J]. J Cancer, 2019, 10(22): 5527-5535. DOI: 10.7150/jca.35465.
15. Flaxel CJ, Adelman RA, Bailey ST, et al. Retinal and ophthalmic artery occlusions preferred practice pattern(R)[J]. Ophthalmology, 2020, 127(2): 259-287. DOI: 10.1016/j.ophtha.2019.09.028.
16. Grant EG, Benson CB, Moneta GL, et al. Carotid artery stenosis: gray-scale and Doppler US Diagnosis-Society of Radiologists in Ultrasound Consensus Conference[J]. Radiology, 2003, 229(2): 340-346. DOI: 10.1148/radiol.2292030516.
17. Charlson M, Szatrowski TP, Peterson J, et al. Validation of a combined comorbidity index[J]. J Clin Epidemiol, 1994, 47(11): 1245-1251. DOI: 10.1016/0895-4356(94)90129-5.
18. 彭斌, 吴波. 中国急性缺血性脑卒中诊治指南2018[J]. 中华神经科杂志, 2018, 51(9): 666-682. DOI: 10.3760/cma.j.issn.1006-7876.2018.09.004.Peng B, Wu B. Chinese guidelines for diagnosis and treatment of acute ischemic stroke 2018[J]. Chin J Neurol, 2018, 51(9): 666-682. DOI: 10.3760/cma.j.issn.1006-7876.2018.09.004.
19. 王陇德, 彭斌, 张鸿祺, 等. 《中国脑卒中防治报告2020》概要[J]. 中国脑血管病杂志, 2022, 19(2): 136-144. DOI: 10.3969/j.issn.1672-5921.2022.02.011.Wang LD, Peng B, Zhang HQ, et al. Brief report on stroke prevention and treatment in China, 2020[J]. Chin J Cerebrovasc Dis, 2022, 19(2): 136-144. DOI: 10.3969/j.issn.1672-5921.2022.02.011.
20. Chodnicki KD, Pulido JS, Hodge DO, et al. Stroke risk before and after central retinal artery occlusion in a US cohort[J]. Mayo Clin Proc, 2019, 94(2): 236-241. DOI: 10.1016/j.mayocp.2018.10.018.
21. Mir TA, Arham AZ, Fang W, et al. Acute vascular ischemic events in patients with central retinal artery occlusion in the United States: a nationwide study 2003-2014[J]. Am J Ophthalmol, 2019, 200: 179-186. DOI: 10.1016/j.ajo.2019.01.009.
22. Avery MB, Magal I, Kherani A, et al. Risk of stroke in patients with ocular arterial occlusive disorders: a retrospective Canadian study[J/OL]. J Am Heart Assoc, 2019, 8(3): e010509[2019-02-05]. https://europepmc.org/article/MED/30712440. DOI: 10.1161/JAHA.118.010509.
23. French DD, Margo CE, Greenberg PB. Ischemic stroke risk in medicare beneficiaries with central retinal artery occlusion: a retrospective cohort study[J]. Ophthalmol Ther, 2018, 7(1): 125-131. DOI: 10.1007/s40123-018-0126-x.
24. 李曼. 眼缺血综合征与缺血性脑卒中相关性研究进展[J]. 山东大学耳鼻喉眼学报, 2022, 36(5): 88-92, 99. DOI: 10.6040/j.issn.1673-3770.0.2021.185.Li M. Association between ocular ischemic syndrome and ischemic stroke[J]. Journal of Otolaryngology and Ophthalmology of Shandong University, 2022, 36(5): 88-92, 99. DOI: 10.6040/j.issn.1673-3770.0.2021.185.
25. 王敏, 王升, 陈小瑾, 等. 缺血性眼病与缺血性脑卒中发生的相关性研究[J]. 中华眼底病杂志, 2012, 28(2): 177-178. DOI: 10.3760/cma.j.issn.1005-1015.2012.02.021.Wang M, Wang S, Chen XJ, et al. Research on the relationship between ischemic ophthalmopathy and ischemic stroke[J]. Chin J Ocul Fundus Dis, 2012, 28(2): 177-178. DOI: 10.3760/cma.j.issn.1005-1015.2012.02.021.
26. 赵军, 胡莲娜, 魏世辉. 眼缺血性疾病对预测颈动脉狭窄发生的意义[J]. 国际眼科杂志, 2009, 9(2): 361-362. DOI: 10.3969/j.issn.1672-5123.2009.02.047.Zhao J, Hu LN, Wei SH. Clinical significance of ocular ischemia disease on predicted the happening of carotid stenosis[J]. Int J Ophthalmol, 2009, 9(2): 361-362. DOI: 10.3969/j.issn.1672-5123.2009.02.047.
27. Zhang F, Bharadwaj A, Mohamed MO, et al. Impact of Charlson co-morbidity index score on management and outcomes after acute coronary syndrome[J]. Am J Cardiol, 2020, 130: 15-23. DOI: 10.1016/j.amjcard.2020.06.022.
28. Chuang MH, Chuang TL, Huang KY, et al. Age-adjusted Charlson comorbidity index scores predict major adverse cardiovascular events and all-cause mortality among systemic lupus erythematosus patients[J]. Ci Ji Yi Xue Za Zhi, 2017, 29(3): 154-158. DOI: 10.4103/tcmj.tcmj_57_17.
29. Schmidt M, Jacobsen J B, Johnsen SP, et al. Eighteen-year trends in stroke mortality and the prognostic influence of comorbidity[J]. Neurology, 2014, 82(4): 340-350. DOI: 10.1212/WNL.0000000000000062.
30. Fischer U, Mono M L, Zwahlen M, et al. Impact of thrombolysis on stroke outcome at 12 months in a population: the Bern stroke project[J]. Stroke, 2012, 43(4): 1039-1045. DOI: 10.1161/STROKEAHA.111.630384.

Chinese Journal of Ocular Fundus Diseases

Relationship between age-adjusted Charlson comorbidity index and ischemic stroke in patients with ophthalmic artery occlusion or retinal artery occlusion

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