Clinical significance of neutrophil extracellular traps biomarkers in thrombosis

Xu, Xiangbo; Wu, Yuting; Xu, Shixue; Yin, Yue; Ageno, Walter; De Stefano, Valerio; Zhao, Qingchun; Qi, Xingshun

doi:10.1186/s12959-022-00421-y

Thrombosis Journal

Table 1 Studies evaluating NETs biomarkers in VTE

From: Clinical significance of neutrophil extracellular traps biomarkers in thrombosis

First author/year	Study design	Included patients	Groups (No. patients)	Samples processing	NETs biomarkers	Analytical methods for NETs biomarkers	Detailed values
Arnalich et al (2013) [47]	Case–control and cohort	Patients with acute massive or sub-massive PE, confirmed with computed tomographic pulmonary angiography	Massive PE (n = 37) vs. Sub-massive PE (n = 37) vs. HC (n = 37)	Plasma, 4 ºC, 1800 × g,10 min	Mitochondrial DNA	qPCR	2970 vs. 870 vs. 185 GE/mL
Arnalich et al (2013) [47]	Case–control and cohort			Plasma, 4 ºC, 1800 × g,10 min	Nuclear DNA	qPCR	3325 vs. 1245 vs. 520 GE/mL
Diaz et al (2013) [48]	Case–control	Patients performed duplex ultrasound to confirm the presence of DVT	DVT (n = 47) vs. Negative DVT (n = 28) vs. HC (n = 19)	Plasma, 4 °C, 2000 × g, 10 min	MPO	ELISA	31.7 vs. 15.5 vs. 5.7 AU
Diaz et al (2013) [48]	Case–control		DVT (n = 47) vs. Negative DVT (n = 28) vs. HC (n = 19)	Plasma, 4 °C, 2000 × g, 10 min	DNA	SytoxGreen fluorimetry	57.7 vs. 17.9 vs. 23.9 ng/mL
van Montfoort et al (2013) [49]	Case–control	Adult patients with and without acute symptomatic DVT of the leg	DVT (n = 150) vs. No DVT (n = 195)	Plasma, RT, 1500 × g, 15 min	NE-α1-antitrypsin	ELISA	53 vs. 45 ng/mL
van Montfoort et al (2013) [49]	Case–control		DVT (n = 150) vs. No DVT (n = 195)	Plasma, RT, 1500 × g, 15 min	Nucleosomes	ELISA	17 vs. 9 U/mL
Jiménez-Alcázar et al (2018) [50]	Case–control and cohort	Patients aged > 65 years with acute, symptomatic VTE	Distal DVT (n = 51) vs. Proximal DVT (n = 133) vs. PE (n = 427)	Plasma	DNA-histone-MPO	ELISA	NA
					Nucleosomes	ELISA	NA
					DNA	SytoxGreen fluorimetry	NA
Lee et al (2018) [51]	Case–control	Patients with sepsis and thrombosis	DVT (n = 25) vs. HC (n = 23)	Serum, 4 °C, 1500 × g, 15 min	MPO	ELISA	250.5 vs. 120.4 ng/mL
					MPO-DNA	ELISA	0.07 vs. 0.05 OD
					Nucleosomes	ELISA	0.3 vs. 0.1 U/L
					NE	ELISA	370.8 vs. 162.4 ng/mL
					DNA	SytoxGreen fluorimetry	22.3 vs.8.1 ng/mL
Martos et al (2020) [52]	Case–control	Patients with VTE	DVT (n = 192) vs. SVT (n = 61) vs. HC (n = 249)	Plasma, 4 ℃, 1811 × g, 30 min	MPO	ELISA	1728.5 vs. 1882.5 vs. 1250.0 ng/mL
					DNA	PicoGreen fluorimetry	1657.6 vs. 1586.4 vs. 1320.9 ng/mL
					Calprotectin	ELISA	NA
Medeiros et al (2020) [53]	Case–control	Patients with VTE and anticoagulation therapy	VTE off warfarin (n = 263) vs. VTE on warfarin (n = 245) vs. HC (n = 50)	Plasma, 20 °C, 1700 × g, 15 + 5 min	DNA	QIAamp	5.53 vs. 3.11 vs. 2.77 µg/mL
Ząbczyk et al (2020) [54]	Case–control and cohort	Patients with acute PE	Acute PE (n = 126) vs. HC (n = 25)	Plasma, 2500 × g, 10 min	H3Cit	ELISA	2.77 vs. 0.59 ng/mL
Liu et al (2021) [55]	Case–control	Patients with traumatic fracture	Trauma non-DVT (n = 37) vs. Trauma DVT (n = 39) vs. DVT (n = 34) vs. HC (n = 24)	Plasma, 2500 × g, 15 min	H3Cit	ELISA	0.38 vs. 0.87 vs. 1.88 vs. 1.79 ng/mL
					Nucleosomes	ELISA	1.20 vs. 1.03 vs. 1.29 vs.—ratio
					DNA	PicoGreen fluorimetry	185.56 vs. 165.70 vs. 216.15 vs. 135.08 ng/mL
Sharma et al (2021) [44]	Case–control	Patients with stable CTEPH	CTEPH (n = 141) vs. Controls (n = 60)	Plasma, 2000 × g, 10 min	MPO	ELISA	NA
					H3Cit	ELISA	NA
					DNA	SytoxGreen fluorimetry	NA
Turon et al (2021) [56]	Cohort	Patients with cirrhosis	PVT (n = 23) vs. No PVT (n = 287)	Plasma	MPO-DNA	ELISA	0.21 vs. 0.29 AU
Turon et al (2021) [56]	Cohort	Patients with cirrhosis	PVT (n = 23) vs. No PVT (n = 287)	Plasma	DNA	PicoGreen fluorimetry	0.89 vs. 0.89 µg/mL
Xing et al (2022) [57]	Case–control	Patients with cirrhosis	PVT (n = 28) vs. No PVT (n = 44)	Plasma, 1000 × g, 15 min	MPO	ELISA	NA
					NE	ELISA	NA
					H3Cit	ELISA	NA
Smith et al (2022) [58]	Case–control	Patients with VTE	VEBIOS ER Cohort: VTE (n = 51) vs. No VTE (n = 96) vs. HC (n = 30) DFW-VTE Cohort: VTE (n = 61) vs. No VTE (n = 86) vs. HC (n = 30)	Plasma, 3000 × g, 15 min	H3Cit-DNA	ELISA	VEBIOS ER Cohort: 110 vs. 73 vs. 38 ng/mL DFW-VTE Cohort: 102 vs. 54 vs. 38 ng/mL
					NE	ELISA	VEBIOS ER Cohort: 31 vs. 24 vs.21 ng/mL DFW-VTE Cohort: 49 vs. 38 vs. 21 ng/mL
					DNA	PicoGreen fluorimetry	VEBIOS ER Cohort: 423 vs. 405 vs. 421 ng/mL DFW-VTE Cohort: 396 vs. 392 vs. 421 ng/mL

Abbreviations: AU Absorbance unit, CTEPH Chronic thromboembolic pulmonary hypertension, DVT Deep vein thrombosis, HC Healthy control, H3Cit Citrullinated histone H3, ELISA Enzyme-linked immunosorbent assay, Min Minute, MPO Myeloperoxidase, NA Not available, NE Neutrophil elastase, NETs Neutrophil extracellular traps, OD Optical density, PE Pulmonary embolism, PVT Portal vein thrombosis, qPCR Quantitative polymerase chain reaction, RT Room temperature, SVT Splanchnic vein thrombosis, VTE Venous thromboembolism

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