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Anemia Is a Risk Factor for the Development of Ischemic Stroke and Post-Stroke Mortality

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Anemia Is a Risk Factor for the Development of Ischemic Stroke and Post-Stroke Mortality Journal of Clinical Medicine Article Anemia Is a Risk Factor for the Development of Ischemic Stroke and Post-Stroke Mortality Jayoon Heo 1, Tae-Mi Youk 2,3 and Kwon-Duk Seo 4,* 1 Department of Hematology-Oncology, National Health Insurance Service Ilsan Hospital, 100 Ilsan-ro, Ilsan-donggu, Goyang 10444, Korea; [email protected] 2 Research Institute, National Health Insurance Service Ilsan Hospital, 100 Ilsan-ro, Ilsan-donggu, Goyang 10444, Korea; [email protected] 3 Department of Statistics, Korea University, 145 Anam-ro, Seongbuk-gu, Seoul 02841, Korea 4 Department of Neurology, National Health Insurance Service Ilsan Hospital, 100 Ilsan-ro, Ilsan-donggu, Goyang 10444, Korea * Correspondence: [email protected] Abstract: Background: anemia is known to be a risk factor for developing ischemic stroke in long- term follow-up studies, and it is also known to increase the risk of death in ischemic stroke patients. We aimed to determine the association of anemia with the risk of ischemic stroke and the risk of death after ischemic stroke. Methods: The study included patients from National Health Insurance Service cohort, from January 2005 to December 2015. Anemia patients were defined as those with confirmed diagnostic codes and related medications in the sample cohort, and patients under the age of 18 were excluded. To perform a comparative analysis with the control group, twice as many patients were extracted by propensity score matching. The effects of anemia on the development of ischemic stroke were analyzed. Results: A total of 58,699 patients were newly diagnosed with anemia during the study period. In anemia group, the rate of ischemic stroke occurring within 1 year was Citation: Heo, J.; Youk, T.-M.; Seo, 0.550%, and the rate was 0.272% in the control group. The odds ratio of anemia related to ischemic K.-D. Anemia Is a Risk Factor for the stroke was 1.602 (95% confidence intervals (CI) 1.363–1.883). During the follow-up period, 175 out Development of Ischemic Stroke and of 309 (56.6%) died in anemia group, and 130 out of 314 (41.4%) died in control group. The anemia Post-Stroke Mortality. J. Clin. Med. 2021, 10, 2556. https://doi.org/ group showed a higher risk of death than the control group (Hazard ratio 1.509, 95% CI 1.197–1.902). 10.3390/jcm10122556 Conclusion: Analysis of the nationwide health insurance data revealed that anemia is one of the risk factors for the development of ischemic stroke, and also an independent prognostic factor affecting Academic Editors: Hansjörg Bäzner post-stroke mortality. and Hans Henkes Keywords: anemia; ischemic stroke; mortality Received: 6 May 2021 Accepted: 7 June 2021 Published: 9 June 2021 1. Introduction Publisher’s Note: MDPI stays neutral Anemia is a decrease in red blood cells (RBCs) or hemoglobin in the blood. The most with regard to jurisdictional claims in common cause of anemia is a blood loss, and insufficient RBC production or increased published maps and institutional affil- breakdown of RBCs can be causes as well. Anemia is a common disease in about 10% iations. of people aged ≥65 years and its prevalence increase with age [1]. Ischemic stroke is fre- quently accompanied by anemia; previous studies have confirmed an average prevalence rate of 15–20% [2–6], and a maximum prevalence of 30% [7]. These prevalence rates of anemia are not significantly different from the 33% for diabetes or atrial fibrillation, which Copyright: © 2021 by the authors. are known major risk factors for developing ischemic stroke [8,9]. In a previous long-term Licensee MDPI, Basel, Switzerland. observational study, anemia in women increased the risk of ischemic stroke [10]. In subse- This article is an open access article quent observational studies, high or low hemoglobin levels increased the developmental distributed under the terms and risk of ischemic stroke for both men and women [11]. In patients with chronic kidney conditions of the Creative Commons disease accompanied by anemia, the reported risk for stroke is high [12]. In patients with Attribution (CC BY) license (https:// creativecommons.org/licenses/by/ ischemic stroke, a history of iron-deficiency anemia was more prevalent than in those 4.0/). without [13]. J. Clin. Med. 2021, 10, 2556. https://doi.org/10.3390/jcm10122556 https://www.mdpi.com/journal/jcm J. Clin. Med. 2021, 10, 2556 2 of 12 Anemia alone is known to increase mortality risks in older adults [1], and when accompanied by cardiac diseases [14,15]. An observational study has shown that anemia at the time of hospitalization in patients with ischemic stroke increases the risk of death upon long-term follow-up [16]. In a meta-analysis of observational studies lasting >1 year, mor- tality risk for both ischemic stroke and hemorrhagic stroke increased when accompanied by anemia [4,17]. Additionally, a recent study confirmed that patients who were anemic at the time of an ischemic stroke had a high risk for recurrence and development of cardiovas- cular disease and cardiovascular death within a year [2]. Furthermore, it was reported that delayed treatment of anemia during hospitalization with ischemic stroke was associated with poor outcome at 3 months [6]. Therefore, anemia is a risk factor for developing ischemic stroke and increases the chance of recurrence and mortality risk. While there have been many cohort studies, no study has investigated data representing one nation’s entire population. We analyzed health insurance claims data to confirm the development risk of ischemic stroke due to anemia; we followed up with patients who developed ischemic stroke to analyze whether anemia influenced the post-stroke mortality risk. 2. Materials and Methods 2.1. Study Population The National Health Insurance Service (NHIS) in South Korea is medical insurance to which 97% of all South Koreans have registered. The NHIS manages the claims data of all medical practices covered by insurance. This study used the national sample cohort data from the NHIS, created with about a million samples representing about 2% of the entire population, extracted out of all NHI claims data using a stratified random method with sex, age, address and insurance cost as references. This sample cohort is a validated dataset that represents the population in terms of the prevalence of major diseases [18]. Our study was conducted for the standard cohort in 1 January 2005–31 December 2015. Data from 1 January 2005 to 31 December 2005, and 1 January 2015 to 31 December 2015 were excluded to take washout and follow-up periods into account; thus, study subjects were extracted from the nine years of data for 2006–2014. Subjects <18 years old were excluded because our focus was on adult patients. Diagnoses in the sample cohort data were categorized based on the International Classification of Diseases, 10th Revision codes (ICD-10). Patients were selected for our study if they had claims that occurred for primary diagnoses of: D50. Iron deficiency anemia; D51. Vitamin B12-deficiency anemia; D52. Folate deficiency anemia; D53. Other nutritional anemia; D55. Anemia due to enzyme disorders; D59. Acquired hemolytic anemia; D61. Other aplastic anemia; D63. Anemia in chronic diseases classified elsewhere; D64. Other anemias. The hemoglobin level was unavailable in the cohort data, so the following method was used to improve the analysis accuracy regarding patients diagnosed with anemia. For those hospitalized, the hemoglobin level was identified from tests performed on admission, so any of the above diagnoses in admission claims data were selected as subjects. In out-patient treatment claims data, the above diagnostic codes can be claimed to not contain hemoglobin levels, so subjects had treatment medication prescribed. We extracted data if patients diagnosed with D50, D53, D63 and D64 had medications prescribed for treating iron-deficiency anemia; if those diagnosed with D51, D52, D53, D61, D63 and D64 had medications prescribed for treating aplastic anemia (cobalamin, folic acid); if those diagnosed with D63 were prescribed erythropoietin. Out of the billing statements satisfying the above conditions, the start date of medical treatment was defined as the time of confirmation of anemia; with this time point as a reference, the development of ischemic stroke or related death was searched. If the diagnosis code appears multiple times within a person, only the first claim was confirmed as newly diagnosed with anemia. Patients who received a claim with an anemia diagnosis but did not receive a relevant prescription, and patients who only claimed an anemia treatment drug without a diagnosis were not included as study subjects. In total, 59,905 patients received their first diagnosis in 2006–2014. The diagnosed anemic J. Clin. Med. 2021, 10, 2556 3 of 12 patients were compared with those not in terms of developing ischemic stroke and death; a control group was created based on 1:2 propensity score matching (PSM) with sex and age (years) as references. The remaining 58,699 patients were used for analysis in pairs. The developmental risk of ischemic stroke is high when accompanied by diseases such as hypertension, diabetes, dyslipidemia, atrial fibrillation and chronic kidney disease. To evaluate the influence of accompanying anemia on the development of ischemic stroke, we confirmed the presence or absence of accompanying disease in previous claims data from the time of anemia diagnosis. In the control group, it was confirmed using the paired anemia patient’s diagnosis date as the index date. It was not possible to extract the propensity score matching, since the matching with the control group should be based on the same time with the newly diagnosed anemia. Therefore, it was not possible to extract so that the proportions of comorbid diseases were the same in the anemia group and the control group.
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