Archives of Academic Emergency Medicine. 2020; 8(1): e73 OR I G I N A L RE S E A RC H Usefulness of Immature Granulocytes to Predict High Coronary SYNTAX Score in Acute Coronary Syndrome; a Cross-sectional Study Cihan Bedel1∗, Mustafa Korkut1, Fatih Aksoy2, Görkem Kuş3 1. Department of Emergency Medicine, Health Science University Antalya Training and Research Hospital, Antalya,Turkey. 2. Department of Cardiology, Suleyman Demirel University Faculty of Medicine, Isparta, Turkey. 3. Department of Cardiology, Health Science University Antalya Training and Research Hospital, Antalya,Turkey. Received: July 2020; Accepted: August 2020; Published online: 15 September 2020 Abstract: Introduction: Immature granulocytes (IG) in peripheral blood indicate increased bone marrow activation and inflammation, and SYNTAX score (SS) is an anatomical scoring system based on coronary angiogram. This study, aimed to evaluate the relationship between IG and SS, as a new inflammatory marker in patients with acute coronary syndrome (ACS). Methods: Patients aged >18 years who were diagnosed with ACS in the emergency department were included in this study, which was planned as a cross-sectional study. Patients were divided into two groups of patients with high and low SSs according to coronary angiography results. Demographic and laboratory parameters were compared between the groups. Results: Our study consisted of 78 patients diagnosed with ACS, who met the inclusion criteria. The average age of the study group was 59 years, and 67.9% of the patients were male. 21 patients (26.9%) had high SSs and 57 patients (73.1%) had low SSs. Mean IG% was significantly higher in high SS group compared to low SS group (0.71±0.25 vs 0.44±0.21 mg/dl, p<0.001). IG% can present a high SS with 76.2% sensitivity and 75.4% specificity at a cut-off value of 0.7. Conclusion: IG was significantly higher in ACS patients with high SSs. It seems that IG can be used as a parameter, which is quickly accessible and cheap, in order to predict high SS in ACS patients in daily clinical practice. Keywords: Inflammation; Acute coronary syndrome; Granulocytes; percutaneous coronary intervention; Emergency Medicine; Atherosclerosis Cite this article as: Bedel C, Korkut M, Aksoy F, Kuş G. Usefulness of Immature Granulocytes to Predict High Coronary SYNTAX Score in Acute Coronary Syndrome; a Cross-sectional Study. Arch Acad Emerg Med. 2020; 8(1): e73. 1. Introduction Acute coronary syndrome (ACS) is one of the main reasons for admission to the emergency department and hospitaliza- tion. ACS is usually characterized by atherosclerotic plaque rupture and complete or incomplete thrombosis of the coro- nary arteries, which is one of the most significant causes of mortality and morbidity [1, 2]. Many pathophysiological fac- tors influence this atherosclerotic process, and inflammation is one of these factors. Inflammation plays a significant role in initiating atherosclerosis and facilitating its progression ∗Corresponding Author: Cihan Bedel; Health Science University Antalya Training And Research Hospital, Kazim Karabekir Street postal zip code: 07100, Muratpaşa, Antalya, Turkey. Tel: +905075641254, Fax: +902422494487, Email: cihanbedel@hotmail.com. [3]. Inflammatory markers, such as white blood cell (WBC), C- reactive protein (CRP), Neutrophil-lymphocyte ratio (NLR), and platelet-lymphocyte ratio (PLR), have been researched in the demonstration of poor condition in cardiovascular events [4, 5]. Immature granulocyte (IG), a parameter that is not adequately known by many clinicians, reflects the frac- tion of immature granulocytes in the peripheral blood. This parameter can be easily and quickly measured in automated blood cell analyzers. It has been revealed to be useful in pre- dicting the severity of many disease processes, such as bac- terial infection, acute inflammatory diseases, tissue necrosis, and acute transplant rejection, in recent years [6, 7]. Synergy between percutaneous coronary intervention with taxus and cardiac surgery (SYNTAX) score (SS) is an anatom- ical scoring system based on coronary angiogram, which can help with evaluating the severity of coronary artery This open-access article distributed under the terms of the Creative Commons Attribution NonCommercial 3.0 License (CC BY-NC 3.0). Downloaded from: http://journals.sbmu.ac.ir/aaem C. Bedel et al. 2 disease and making revascularization decisions [8]. Previ- ously, many studies have examined the relationship between WBC, CRP, Neutrophil-lymphocyte ratio (NLR), and platelet- lymphocyte ratio (PLR) and SS; however, there are no studies evaluating the relationship between IG and SS in the litera- ture. Therefore, this study aimed to evaluate the relationship between IG and SS, as a new inflammatory marker in patients with ACS. 2. Methods Patients aged >18, who had presented to the emergency de- partment with pain in the chest and been admitted to the department of cardiology with a diagnosis of ACS (unstable angina pectoris/myocardial infarction without ST-segment elevation (NSTEMI)/myocardial infarction with ST-segment elevation (STEMI)), were included in this study, which was planned as a prospective cross-sectional study and per- formed during the period between December 01, 2019, and February 01, 2020. The diagnosis of ACS was defined as hav- ing electrocardiographic (ECG) change and/or increase of cardiac markers along with chest pain, which was assumed to be typical chest pain. In compliance with American College of Cardiology and European Society of Cardiology (ACC/ESC) criteria, STEMI was defined as ST-segment elevation in ECG and increase in all the derivations by âL’ě0.1mV in two con- secutive derivations. Necessary approval was received from the Clinical Research Ethics Committee for the study (No: IRB-2019-355). Written informed consent was obtained from all the patients, who agreed to participate in the study. 2.1. Participants Exclusion Criteria were determined as being <18 years old, being pregnant, having a myeloproliferative disease (it may change hematological parameters), malignancy, having trauma or surgery history within the past 1 week, arrhyth- mia causing hemodynamic instability, heart failure, inflam- matory bowel disease, granulocyte-colony stimulating factor, and using immunosuppressive agents or steroids. 2.2. Data gathering ACS patients’ age, gender, history of hyperlipidemia, his- tory of hypertension (HT), history of diabetes mellitus (DM), family history, drugs, systolic blood pressure (SBP), diastolic blood pressure (DBP), and heart rates (HR) (pulse/min) were recorded. The minimum sample size with a two-sided alpha value of 5%, a statistical power of 80% was estimated to be 50 patients. We planned to enrol a total of 80 patients, taking into account the 20% expected failure rate. 2.3. SYNTAX Score and Angiographic Analysis In the study, coronary angiography (CAG) was carried out for all the patients using the Judkins technique. In order to grade the stenosis of the coronary vessels, stenoses over 50% in vessels with a size of ≥1.5mm were taken into consider- ation. SS was prospectively calculated by two experienced cardiologists using an algorithm based on the diagnostic an- giogram. The final score was calculated using individual le- sion scores by analysts who were blind to operational data and clinical outcomes. Items such as whether the stenosis was total, the level and the size of the stenosis, presence of collateral flow, presence of bifurcation or trifurcation lesion, severe folds, and severe calcification were evaluated [9, 10]. 2.4. Blood Samples Venous blood samples of the patients were taken within the first hour of admission to the emergency department be- fore the primary CAG. In the samples taken during admis- sion, WBC, neutrophil count, lymphocyte count, and IG% IG count (IGC) were measured using an automated blood anal- ysis system (CoulterÂő LH 780 Hematologic Analyzer, Beck- man Coulter Inc. Brea, USA). Absolute cell numbers were used in the analyses. CRP, haemoglobin, glucose values, and cardiac Troponin T levels, which were measured dur- ing the admission, were recorded. The levels of total choles- terol, high-density lipoprotein (HDL), low-density lipopro- tein (LDL), and triglycerides were recorded during admission to the coronary intensive care. The left ventricular ejection fraction (LVEF) of the patients was measured using Vivid S5 (GE Healthcare, Inc. Chicago, IL, USA) device connected to 2-4 MHz transducer via Simpson’s method according to the recommendations of the American Society of Echocardiog- raphy [11]. According to CAG results, patients with high SSs (>22) and patients with low SSs (≤22) were separated into two groups, and all the parameters were compared. 2.5. Statistical Analysis Statistical analyses were conducted using SPSS 21.0 package program (SPSS Inc., Chicago, IL). Continuous variables were expressed as mean ± standard deviation, and categorical variables were given as number and percentage. An indepen- dent t-test was used for comparing the distribution of the pa- rameters with normal distribution, and the Mann-Whitney U test was applied for those that did not have a normal distribu- tion. In categorical data, the evaluation was made using the chi-square test. Logistic regression was conducted for factors associated with high SS. The optimum cut off value of IG in predicting high SS was assessed through Receiver operating characteristic (ROC) analysis. Statistical significance was de- fined as a p-value less than 0.05. This open-access article distributed under the terms of the Creative Commons Attribution NonCommercial 3.0 License (CC BY-NC 3.0). Downloaded from: http://journals.sbmu.ac.ir/aaem 3 Archives of Academic Emergency Medicine. 2020; 8(1): e73 Table 1: Comparing the baseline characteristics of patients with high (> 22) and low (≤ 22) SYNTAX score Variables SYNTAX Score P High (n=21) Low (n =57 ) Age (years) Mean ± SD 66.00 ± 16.67 57.57 ± 14.15 0.057 Gender n (%) Male 15 (68.2) 38 (66.6) 0.789 Female 6 (31.8) 19 (33.4) Underlying comorbidity Yes 25.55 34.19 13.62 No 8.71 11.49 5.84 Vital signs SBP, mm Hg 131.57 ± 14.92 144.14 ± 27.01 0.071 DBP, mm Hg 83.19 ± 8.04 91.47 ± 15.26 0.006 Heart rate, beats/min 83.07 ± 15.26 84.33 ± 15.26 0.283 Ejection fraction, % 45.95 ± 12.57 55.7 ± 12.93 0.002 SYNTAX score 27.78 ± 4.79 7.38 ± 6.24 <0.001 Previous history Current smoker 12 (57.1) 29 (50.9) 0.799 Hypertension 11 (52.4) 28 (49.1) 0.500 Diabetes mellitus 7 (33.3) 22 (38.6) 0.794 Dyslipidemia 9 (42.9) 21 (36.8) 0.409 History of CAD 8 (38.1) 6 (10.5) 0.009 Laboratory findings WBC count (×103 /mm3 ) 13.03 ± 3.05 10.68 ± 4.15 0.003 Neutrophil, (×103 /mm3 ) 8.77 ± 2.84 6.84 ± 3.4 0.005 Lymphocyte, (×103 /mm3 ) 3.67 ± 3.20 2.97 ± 2.41 0.318 NLR 4.09 ± 3.91 3.14 ± 2.71 0.367 PLR 112.14 ± 59.08 120.51 ± 57.22 0.499 Hemoglobin, mg/dL 13.89 ± 1.97 13.55 ± 1.97 0.355 Glucose (mg/dl) 163.33 ± 71.52 140.36 ± 69.22 0.017 IGC(×103 /mm3 ) 0.08 ± 0.06 0.07 ± 0.01 0.004 IG% 0.71 ± 0.25 0.44 ± 0.21 <0.001 CRP (mg/dL) 35.37 ± 17.12 3.92 ± 0.54 0.021 Troponin T (ng L) 502.00 ± 157.07 426.08 ± 157.74 0.012 Lipid profiles (mg/dl) Triglycerides 162.72 ± 92.30 212.33 ± 134.39 0.188 Total cholesterol 211.27 ± 65.80 220.64 ± 56.83 0.304 High-density lipoprotein 44.00 ± 9.01 46.28 ± 10.97 0.354 Low-density lipoprotein 135.50 ± 57.34 134.66 ± 45.95 0.650 Previous medication n (%) RAS blocker 2 (9.5) 5 (8.8) 0.611 ACE-I 2 (9.5) 14 (24.6) 0.210 Beta blocker 3 (14.3) 15 (26.3) 0.368 Diuretic 4 (19) 9 (15.8) 0.740 Calcium channel blocker 6 (28.6) 8 (14) 0.184 Statin 10 (47.6) 22 (38.6) 0.605 Antiaggregant 5 (23.8) 12 (21.1) 0.766 Oral antidiabetic drug 4 (19) 16 (28.1) 0.562 Mortality Number (%) 3 (14.3) 0 (0) 0.017 Data are presented as mean ± standard deviation or frequency (%). SYNTAX score: Synergy between percutaneous coronary intervention with taxus and cardiac surgery; SBP: Systolic Blood Pressure; DBP: Diastolic Blood Pressure; CAD: Coronary artery disease; WBC: white blood cell; NLR: neutrophil lymphocyte ratio; PLR: platelet lymphocyte ratio; IGC: Immature granulocyte count; IG%: Immature granulocyte percentage; CRP: C-reactive protein; RAS: Renin–angiotensin system; ACE-I: Angiotensin converting enzyme inhibitor. 3. Results Our study consisted of 78 patients diagnosed with ACS, who met the inclusion criteria. The average age of the study group was 59 ± 15.21 years, and 67.9% of the patients were male. 21 patients (26.9%) had high SSs (>22) and 57 pa- This open-access article distributed under the terms of the Creative Commons Attribution NonCommercial 3.0 License (CC BY-NC 3.0). Downloaded from: http://journals.sbmu.ac.ir/aaem C. Bedel et al. 4 Table 2: Comparing the baseline characteristics of patients with high (> 0.6) and low (≤ 0.6) immature granulocyte Variables Immature granulocyte P High (n=22) Low (n =56 ) Age (years) Mean ± SD 61.13 ± 20.28 59.33 ± 12.92 0.807 Gender n (%) Male 15 (68.2) 38 (66.6) 0.601 Female 6 (31.8) 19 (33.4) Vital signs SBP, mm Hg 129.45 ± 16.31 145.19 ± 26.37 0.07 DBP, mm Hg 83.54 ± 9.18 91.48 ± 15.15 0.024 Heart rate, beats/min 84.81 ± 18.21 82.85 ± 8.92 0.367 Ejection fraction, % 50.90 ± 11.51 54.01 ± 10.51 0.234 SYNTAX score 17.21 ± 14.80 10.97 ± 8.31 0.024 Previous history Current smoker 13 (59.1) 28 (50) 0.615 Hypertension 10 (45.5) 29 (51.8) 0.802 Diabetes mellitus 7 (31.8) 22 (39.3) 0.610 Dyslipidemia 5 (22.7) 25 (44.6) 0.120 History of CAD 5 (22.7) 9 (16.1) 0.522 Laboratory findings WBC count (×103 /mm3 ) 12.88 ± 3.92 10.70 ± 3.90 0.032 Neutrophil, (×103 /mm3 ) 9.26 ± 3.78 6.61 ± 2.87 0.003 Lymphocyte, (×103 /mm3 ) 3.70 ± 0.82 2.97 ± 0.96 0.526 NLR 4.22 ± 4.11 3.06 ± 2.73 0.111 PLR 112.78 ± 61.46 119.95 ± 56.66 0.560 Hemoglobin, mg/dL 12.95 ± 2.25 13.89 ± 1.78 0.131 Glucose (mg/dl) 114.38 ± 63.50 148.07 ± 73.39 0.556 CRP (mg/dL) 24.71 ± 14.98 7.35 ± 3.01 0.693 Troponin T (ng L) 519.66 ± 156.17 424.96 ± 160.55 0.011 Lipid profiles (mg/dl) Triglycerides 175.11 ± 107.80 208.35 ± 132.05 0.381 Total cholesterol 189.22 ± 41.98 227.73 ± 60.65 0.012 High-density lipoprotein 42.38 ± 8.90 46.80 ± 10.84 0.011 Low-density lipoprotein 118.77 ± 31.18 140.03 ± 52.11 0.08 Previous medication n (%) RAS blocker 2 (9.1) 5 (8.9) 0.561 ACE-I 3 (13.6) 13 (23.2) 0.535 Beta blocker 4 (18.2) 14 (25) 0.766 Diuretic 4 (18.2) 9 (16.1) 1.000 Calcium channel blocker 5 (22.7) 9 (16.1) 0.522 Statin 6 (27.3) 26 (46.4) 0.135 Antiaggregant 5 (22.7) 12 (21.4) 1.000 Oral antidiabetic drug 2 (9.1) 18 (32.1) 0.45 Mortality Number (%) 3 (13.6) 0 (0) 0.02 Data are presented as mean ± standard deviation (SD) or frequency (%). SBP: Systolic Blood Pressure; DBP: Diastolic Blood Pressure; SYNTAX score: Synergy between percutaneous coronary intervention with taxus and cardiac surgery; WBC: white blood cell; NLR: neutrophil lymphocyte ratio; PLR: platelet lymphocyte ratio; IGC: Immature granulocyte count; CAD: Coronary artery disease; WBC: white blood cell; NLR: neutrophil lymphocyte ratio; PLR: platelet lymphocyte ratio; IGC: Immature granulocyte count; IG%: Immature granulocyte percentage; CRP: C-reactive protein; RAS: Renin–angiotensin system; ACE-I: Angiotensin converting enzyme inhibitor. tients (73.1%) had low SSs (≤22). There was no statisti- cal difference between the groups in terms of age and gen- der (p>0.05). Patients with high SSs had significantly lower DBP and LVEF (p=0.006, p=0.002, respectively). Patients with high SSs had significantly higher CAD history comorbidity (p=0.009). Mean WBC, neutrophil, glucose, IGC, and CRP and troponin T levels were significantly higher in patients with high SSs. The mean IG% was significantly higher in the high SYNTAX score group compared to the low SYNTAX score group (0.71±0.25 vs 0.44±0.21mg/dl, p<0.001) (Figure 1). Be- This open-access article distributed under the terms of the Creative Commons Attribution NonCommercial 3.0 License (CC BY-NC 3.0). Downloaded from: http://journals.sbmu.ac.ir/aaem 5 Archives of Academic Emergency Medicine. 2020; 8(1): e73 Table 3: Screening performance characteristics of immature granulocyte percentage in predicting the SYNTAX (synergy between percuta- neous coronary intervention with taxus and cardiac surgery) score in 0.7 cut off point Characters Value (95% CI) Characters Value (95% CI) Sensitivity 76.2 (67.21-84.67) NPV 76.5 (69.15 – 82.59 Specificity 75.4 (66.11-83.81) PLR 3.17 ( 2.2 - 4.57) PPV 76 (68.74 - 82.02) NLR 0.31 (0.21 –0.45) Data are presented as mean ± standard deviation (SD) or frequency (%). SBP: Systolic Blood Pressure; DBP: Diastolic Blood Pressure; Confidence interval (CI). PPV: Positive predictive value; NPV: Negative predictive value; PLR: Positive likelihood ratio; NLR: Negative likelihood ratio. Figure 1: Comparison of immature granulocyte levels between low and high syntax score groups. Figure 2: Receiver operating characteristic (ROC) curve of imma- ture granulocyte percentage for predicting high syntax (synergy be- tween percutaneous coronary intervention with taxus and cardiac surgery) score (p < 0.001). sides, the percentage of mortality was significantly higher in those with high SSs (p=0.017). The demographic data and laboratory results of the groups are compared in Table 1. 22 (28.2%) patients had high IG% values (>0.6), and 56 (71.8%) patients had low IG% values (≤0.6). As seen in Table 2, the prevalence of oral antidiabetic drug use was higher at high IG% values, and mean DBP, HDL, and LDL values of pa- tients were found to be significantly lower. In the group with high IG% levels, higher SSs were detected compared to the patients with low IG% values (17.21±14.80 vs. 10.97±8.31, p=0.024). Additionally, in the analysis of the ROC curve, IG% was shown to predict high SSs with 76.2% (95% Cl: 67.21 – 84.67) sensitivity, 75.4% (95% Cl: 66.11 – 83.81) specificity, and area under the ROC curve of 0.803 (95% CI: 0.699 - 0.908) at a cut-off value of 0.7 (Table 3, Figure 2). 4. Discussion To the best of our knowledge, this is the first study in the lit- erature evaluating the relationship between IG and SS in ACS patients. The main findings of this study suggested that SS was independently correlated with IG%. SS is a scoring system used to evaluate the complexity and prevalence of coronary artery disease based on CAG. It is commonly used by many physicians to specify the opti- mal cardiovascular treatment strategy [12, 13]. Studies have shown that patients with high SSs may have poorer cardio- vascular outcomes, and the score may be an independent predictor for percutaneous interventions. Moreover, high- risk patients can be identified using this scoring system, and appropriate treatment methods can be selected [14, 15]. Inflammation is critically important for the initiation and progression of coronary atherosclerosis. Inflammation af- fects many conditions, such as endothelial dysfunction, leukocyte recruitment, and platelet activation during the atherosclerosis process [16]. Recently, it has been re- vealed that many inflammatory markers, such as CRP, platelet/lymphocyte ratio (PLR) and neutrophil/lymphocyte ratio (NLR), WBC, TNF-α, and cytokines can be independent risk factors for atherosclerosis. The increase in these inflam- matory markers has been shown to correlate with the degree This open-access article distributed under the terms of the Creative Commons Attribution NonCommercial 3.0 License (CC BY-NC 3.0). Downloaded from: http://journals.sbmu.ac.ir/aaem C. Bedel et al. 6 and severity of CAD [14, 17]. These inflammatory markers have been evaluated as prognostic markers for many car- diovascular diseases, such as coronary artery ectasia, stable CAD, and myocardial infarction [18, 19]. 840 patients, who underwent coronary angiography for CAD evaluation, were included in a recent study by Sahin et al. In this study, NLR was shown to be significantly associated with CAD severity in patients with STEMI, and they also reported that NLR is an independent marker for SS [2]. In a recent study by Al- tun et al., Troponin T and NLR were significantly associated with the angiographic severity of ACS evaluated with SS [16]. In a study conducted by Kundi et al., it was reported that the ratio of the Monocyte count to HDL could be used as a pa- rameter that would be quickly accessible and cheap in or- der to predict high SS and it may be used in daily practice as well [13]. In a study conducted by Sivri et al. on 175 pa- tients, the WBC/mean platelet volume ratio was shown to be correlated with increased SS, and thus, short- and long- term mortality [1]. IG in peripheral blood indicates increased bone marrow activation, and it can be easily measured in au- tomated blood analyzers. It has been shown in studies that the presence of immature granulocytes in peripheral blood, which is not normally observed in healthy people, can indi- cate bone marrow activation and serious infection [20, 21]. Recent studies suggest that IG is correlated with prevalent in- travascular coagulation and mortality in critical patients with suspected sepsis [22]. Park et al. reported that high IG values are a good diagnostic sign for severe sepsis and septic shock within the first 24 hours after admission to the intensive care unit [23]. Mathews et al. discovered that the increase in IG% was significant in appendicitis complications in the pediatric age group and only compared it with an increased CRP level and left shift [24]. In this study, we showed that patients with high IG levels had higher SSs. Besides, mortality was higher at high IG levels. 5. Limitations The first limitation was that our study, although it was de- signed prospectively, was conducted with a small number of patients due to the COVID-19 pandemic. Furthermore, the mono-center design of our study increases bias. As another limitation, the fact that the decision on CAG was not made by the same physicians may have influenced the results. Ad- ditionally, the period from the emergence of the symptoms until hospital admission could not be assessed, which may affect the values of inflammatory markers. Finally, since pa- tients with a history of CABG were not included in the study, SS could not be confirmed in this population. 6. Conclusion IG was significantly higher in ACS patients with high Syntax scores. It seems that IG can be used as a parameter, which is quickly accessible and cheap, in order to predict the high SYNTAX score in ACS patients in daily clinical practice. 7. Declarations 7.1. Acknowledgements The authors would like to thank MD. Asli BEDEL for helping in preparation of this paper. 7.2. Author contribution All the authors have a substantial contribution in the study design, data interpretation and writing and reviewing the manuscript. Authors ORCIDs Cihan Bedel: 0000-0002-3823-2929 Mustafa Korkut: 0000-0003-1665-1601 Fatih Aksoy: 0000-0002-6480-4935 Görkem kuş: 0000-0002-6058-5501 7.3. 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