Oxidation‑reduction potential parameters worsen following intraarterial therapy in patients with reduced collateral circulation and middle cerebral artery occlusions

Atchie,Benjamin; Jarvis,Stephanie; Bellon,Richard; Barton,Trevor; Disalvo,Lauren; Salottolo,Kristin; Bar-Or,Raphael; Bar-Or,David

doi:10.3892/etm.2023.11994

Oxidation‑reduction potential parameters worsen following intraarterial therapy in patients with reduced collateral circulation and middle cerebral artery occlusions

Authors:
- Benjamin Atchie
- Stephanie Jarvis
- Richard Bellon
- Trevor Barton
- Lauren Disalvo
- Kristin Salottolo
- Raphael Bar-Or
- David Bar-Or
View Affiliations

Affiliations: Department of Neuroradiology, Swedish Medical Center, Injury Outcomes Network (ION) Research, Englewood, CO 80113, USA, Department of Epidemiology, Injury Outcomes Network (ION) Research, Englewood, CO 80113, USA, Department of Neurology, Swedish Medical Center, Injury Outcomes Network (ION) Research, Englewood, CO 80113, USA, Department of Basic Science, Injury Outcomes Network (ION) Research, Englewood, CO 80113, USA, Department of Directors, Injury Outcomes Network (ION) Research, Englewood, CO 80113, USA
Published online on: May 5, 2023 https://doi.org/10.3892/etm.2023.11994
Article Number: 295
Copyright: © Atchie et al. This is an open access article distributed under the terms of Creative Commons Attribution License.

Metrics: Total Views: 0 (Spandidos Publications: | PMC Statistics: )

Metrics: Total PDF Downloads: 0 (Spandidos Publications: | PMC Statistics: )

Cited By (CrossRef): 0 citations Loading Articles...

Abstract

Collateral circulation is important for cerebral perfusion in acute ischemic strokes. Monitoring the oxidation‑reduction potential (ORP) may be useful to assess collateral status or treatment efficacy. The objectives of the present study were to determine if the ORP was associated with collateral circulation status in middle cerebral artery (MCA) occlusions and to identify patterns in the ORP and the collateral circulation status among patients treated with intraarterial therapy (IAT) over time. The present pilot study was nested within a prospective cohort study measuring the ORP of the peripheral venous plasma of stroke patients. The population included in the present study were patients with MCA (M1/M2) occlusions. Two ORP parameters were examined: Static ORP (sORP; mV), indicating oxidative stress, and capacity ORP (cORP; µC), indicating antioxidant reserves. Collateral status was retrospectively graded using Miteff's system as good (grade 1) or reduced (grade 2/3). Comparisons were made between collateral status groups (reduced vs. good collaterals) in all patients, within a subset including only patients who received IAT, and between thrombolysis in cerebral infraction scale score (TICI) groups (0‑2a vs. 2b/3). The Fisher's exact test, Student's t‑test and Wilcoxon tests were used (α<0.20). The 19 patients were categorized based on their collaterals: Good collaterals (53%) and reduced collaterals (47%). The baseline characteristics were similar with the exception that the patients with good collaterals had a lower international normalized ratio (P=0.12) and were more likely to have a stroke on the left side (P=0.18) or to have a mismatch (P=0.05). The admission sORP values were comparable (169.5 vs. 164.2 mV; P=0.65), as was admission cORP (P=0.73). When considering only the patients who received IAT (n=12), admission sORP (P=0.69) and cORP (P=0.90) were also statistically similar. On day 2, after IAT, both groups experienced a worsening in ORP measures; however, the patients with good collaterals had a significantly lower sORP (169.4 vs. 203.5 mV; P=0.02) and a higher cORP (0.2 vs. 0.1 µC; P=0.002) compared with the patients with reduced collaterals. Neither sORP nor cORP were significantly different between TICI score groups on admission or on day 2. Upon discharge, patients with a TICI of 2b‑3 had a significantly better sORP (P=0.03) and cORP (P=0.12) compared with those with a TICI of 0‑2a. In conclusion, upon patient admission, the ORP parameters were not significantly different between the collateral circulation status groups for MCA occlusions. The ORP parameters worsened after IAT regardless of the collateral circulation status; however, after IAT, on day 2, patients with good collaterals experienced less oxidative stress (sORP) and had higher antioxidant reserves (cORP) than patients with reduced collaterals.

View Figures

View References

1	Liebeskind DS: Collateral Circulation. Stroke. 34:2279–2284. 2003.PubMed/NCBI View Article : Google Scholar
2	Menon BK, Qazi E, Nambiar V, Foster LD, Yeatts SD, Liebeskind D, Jovin TG, Goyal M, Hill MD, Tomsick TA, et al: Differential Effect of Baseline Computed Tomographic Angiography Collaterals on Clinical Outcome in Patients Enrolled in the Interventional Management of Stroke III trial. Stroke. 46:1239–1244. 2015.PubMed/NCBI View Article : Google Scholar
3	Bang OY, Saver JL, Buck BH, Alger JR, Starkman S, Ovbiagele B, Kim D, Jahan R, Duckwiler GR, Yoon SR, et al: Impact of collateral flow on tissue fate in acute ischaemic stroke. J Neurol Neurosurg Psychiatry. 79:625–629. 2008.PubMed/NCBI View Article : Google Scholar
4	Demirbag R, Gur M, Yilmaz R, Kunt AS, Erel O and Andac MH: Influence of oxidative stress on the development of collateral circulation in total coronary occlusions. Int J Cardiol. 116:14–19. 2007.PubMed/NCBI View Article : Google Scholar
5	Bjugstad KB, Rael LT, Levy S, Carrick M, Mains CW, Slone DS and Bar-Or D: Oxidation-Reduction Potential as a Biomarker for Severity and Acute Outcome in Traumatic Brain Injury. Oxid Med Cell Longev. 2016(6974257)2016.PubMed/NCBI View Article : Google Scholar
6	Chen Z and Zhong C: Oxidative stress in Alzheimer's disease. Neurosci Bull. 30:271–281. 2014.PubMed/NCBI View Article : Google Scholar
7	Rael LT, Bar-Or R, Kelly MT, Carrick MM and Bar-Or D: Assessment of oxidative stress in patients with an isolated traumatic brain injury using disposable electrochemical test strips. Electroanalysis. 27:2567–2573. 2015.
8	Spanidis Y, Mpesios A, Stagos D, Goutzourelas N, Bar-Or D, Karapetsa M, Zakynthinos E, Spandidos DA, Tsatsakis AM, Leon G and Kouretas D: Assessment of the redox status in patients with metabolic syndrome and type 2 diabetes reveals great variations. Exp Ther Med. 11:895–903. 2016.PubMed/NCBI View Article : Google Scholar
9	Sinha N and Dabla PK: Oxidative Stress and Antioxidants in Hypertension-A Current Review. Curr Hypertens Rev. 11:132–142. 2015.PubMed/NCBI View Article : Google Scholar
10	Bourg P, Salottolo K, Klein J and Bar-Or D: Can a biomarker for oxidative stress and antioxidant reserves identify frailty in geriatric trauma patients? Injury. 52:2908–2913. 2021.PubMed/NCBI View Article : Google Scholar
11	Kirkham PA and Barnes PJ: Oxidative stress in COPD. Chest. 144:266–273. 2013.PubMed/NCBI View Article : Google Scholar
12	Salottolo KM, Fanale CV, Leonard KA, Frei DF and Bar-Or D: Multimodal imaging does not delay intravenous thrombolytic therapy in acute stroke. AJNR Am J Neuroradiol. 32:864–868. 2011.PubMed/NCBI View Article : Google Scholar
13	Bjugstad KB, Fanale C, Wagner J, Jensen J, Salottolo K, Rael LT and Bar-Or D: A 24 h Delay in the Redox Response Distinguishes the most Severe Stroke Patients from Less Severe Stroke Patients. J Neurol Neurophysiol. 07(395)2016.
14	Rael LT, Leonard J, Salottolo K, Bar-Or R, Bartt RE, Wagner JC and Bar-Or D: Plasma oxidized albumin in acute ischemic stroke is associated with better outcomes. Front Neurol. 10(709)2019.PubMed/NCBI View Article : Google Scholar
15	Wagner JC, Salottolo K, Fanale CV, Whaley M, McCarthy KL and Bar-Or D: Abstract T P219: A Novel Method for Measuring Oxidative Stress in Patients with Stroke Symptoms. Stroke 46 Suppl. 1(ATP219)2015.
16	Miteff F, Levi CR, Bateman GA, Spratt N, McElduff P and Parsons MW: The independent predictive utility of computed tomography angiographic collateral status in acute ischaemic stroke. Brain. 132(Pt 8):2231–2238. 2009.PubMed/NCBI View Article : Google Scholar
17	Seker F, Potreck A, Möhlenbruch M, Bendszus M and Pham M: Comparison of four different collateral scores in acute ischemic stroke by CT angiography. J Neurointerv Surg. 8:1116–1118. 2016.PubMed/NCBI View Article : Google Scholar
18	Bar-Or D, Bar-Or R, Rael LT and Brody EN: Oxidative stress in severe acute illness. Redox Biol. 4:340–345. 2015.PubMed/NCBI View Article : Google Scholar
19	National Institutes of Health and National Institutes of Neurological Disorders and Stroke. NIH Stroke Scale. 1-5. https://www.stroke.nih.gov/resources/scale.htm. Accessed 3/28/2023.
20	Joint Commission National Quality Measures: Modified Rankin Score (mRS) Specifications Manual. 1-3. 2023. https://manual.jointcommission.org/releases/TJC2023B/DataElem0773.html. Accessed 3/28/2023.
21	Higashida RT, Furlan AJ, Roberts H, Tomsick T, Connors B, Barr J, Dillon W, Warach S, Broderick J, Tilley B, et al: Trial design and reporting standards for intra-arterial cerebral thrombolysis for acute ischemic stroke. Stroke. 34:e109–e137. 2003.PubMed/NCBI View Article : Google Scholar
22	Lewis M, Bromley K, Sutton CJ, McCray G, Myers HL and Lancaster GA: Determining sample size for progression criteria for pragmatic pilot RCTs: The hypothesis test strikes back! Pilot Feasibility. Stud. 7(40)2021.PubMed/NCBI View Article : Google Scholar
23	Schoenfeld D: Statistical considerations for pilot studies. Int J Radiat Oncol Biol Phys. 6:371–374. 1980.PubMed/NCBI View Article : Google Scholar
24	Kianifard F and Islam MZ: A guide to the design and analysis of small clinical studies. Pharm Stat. 10:363–368. 2011.PubMed/NCBI View Article : Google Scholar
25	Stallard N: Optimal sample sizes for phase II clinical trials and pilot studies. Stat Med. 31:1031–1042. 2012.PubMed/NCBI View Article : Google Scholar
26	Gómez-de-Mariscal E, Guerrero V, Sneider A, Jayatilaka H, Phillip JM, Wirtz D and Muñoz-Barrutia A: Use of the p-values as a size-dependent function to address practical differences when analyzing large datasets. Sci Rep. 11(20942)2021.PubMed/NCBI View Article : Google Scholar
27	Boers AM, Jansen IG, Berkhemer OA, Yoo AJ, Lingsma HF, Slump CH, Roos YB, van Oostenbrugge RJ, Dippel DW, van der Lugt A, et al: Collateral status and tissue outcome after intra-arterial therapy for patients with acute ischemic stroke. J Cereb Blood Flow Metab. 37:3589–3598. 2017.PubMed/NCBI View Article : Google Scholar
28	Sarraj A, Goyal N, Chen M, Grotta JC, Blackburn S, Requena M, Kamal H, Abraham MG, Elijovich L, Dannenbaum M, et al: Direct to angiography vs repeated imaging approachs in transferred patients undergoing endovascular thrombectomy. JAMA Neurol. 78:916–926. 2021.PubMed/NCBI View Article : Google Scholar
29	Yazici S, Demirtas S, Guclu O, Karahan O, Yavuz C, Caliskan A and Mavitas B: Using oxidant and antioxidant levels to predict the duration of both acute peripheral and mesenteric ischemia. Perfusion. 29:450–455. 2014.PubMed/NCBI View Article : Google Scholar
30	Semerano A, Laredo C, Zhao Y, Rudilosso S, Renú A, Llull L, Amaro S, Obach V, Planas AM, Urra X and Chamorro Á: Leukocytes, collateral circulation, and reperfusion in ischemic stroke patients treated with mechanical thrombectomy. Stroke. 50:3456–3464. 2019.PubMed/NCBI View Article : Google Scholar
31	Tang Z, Zhu Y, Lu X, Wu D, Fan X, Shen J and Xiao L: Deep learning-based prediction of hematoma expansion using a single brain computed tomographic slice in patients with spontaneous intracerebral hemorrhages. World Neurosurg. 165:e128–e136. 2022.PubMed/NCBI View Article : Google Scholar
32	Tang ZR, Chen Y, Hu R and Wang H: Predicting hematoma expansion in intracerebral hemorrhage from brain CT scans via K-nearest neighbors matting and deep residual network. Biomed Signal Process Control. 76(103656)2022.
33	Wufuer A, Wubuli A, Mijiti P, Zhou J, Tuerxun S, Cai J, Ma J and Zhang X: Impact of collateral circulation status on favorable outcomes in thrombolysis treatment: A systematic review and meta-analysis. Exp Ther Med. 15:707–718. 2018.PubMed/NCBI View Article : Google Scholar
34	Marks MP, Lansberg MG, Mlynash M, Olivot JM, Straka M, Kemp S, McTaggart R, Inoue M, Zaharchuk G, Bammer R, et al: Effect of collateral blood flow on patients undergoing endovascular therapy for acute ischemic stroke. Stroke. 45:1035–1039. 2014.PubMed/NCBI View Article : Google Scholar
35	Liebeskind DS, Jahan R, Rogueira RG, Zaidat OO and Saver JL: SWIFT Investigators. Impact of collaterals on successful revascularization in solitaire FR with the intention for thrombectomy. Stroke. 45:2036–2040. 2014.PubMed/NCBI View Article : Google Scholar
36	Tan BL, Norhaizan ME and Liew WP: Nutrients and oxidative stress: Friend or foe? Oxid Med Cell Longev. 2018(9719584)2018.PubMed/NCBI View Article : Google Scholar
37	Loh KP, Qi J, Tan BK, Liu XH, Wei BG and Zhu YZ: Leonurine protects middle cerebral artery occluded rats through antioxidant effect and regulation of mitochondrial function. Stroke. 41:2661–2668. 2010.PubMed/NCBI View Article : Google Scholar
38	Liu ZJ, Ran YY, Qie SY, Gong WJ, Gao FH, Ding ZT and Xi JN: Melatonin protects against ischemic stroke by modulating microglia/macrophage polarization toward anti-inflammatory phenotype through STAT3 pathway. CNS Neurosci Ther. 25:1353–1362. 2019.PubMed/NCBI View Article : Google Scholar
39	Chang CY, Chen JY, Wu MH and Hu ML: Therapeutic treatment with vitamin C reduces focal cerebral ischemia-induced brain infarction in rats by attenuating disruptions of blood brain barrier and cerebral neuronal apoptosis. Free Radic Biol Med. 155:29–36. 2020.PubMed/NCBI View Article : Google Scholar
40	Mota M, Porrini V, Parrella E, Benarese M, Bellucci A, Rhein S, Schwaninger M and Pizzi M: Neuroprotective epi-drugs quench the inflammatory response and microglial/macrophage activation in a mouse model of permanent brain ischemia. J Neuroinflammation. 17(361)2020.PubMed/NCBI View Article : Google Scholar
41	Liu Q, Jin Z, Xu Z, Yang H, Li L, Li G, Li F, Gu S, Zong S, Zhou J, et al: Antioxidant effects of ginkgolides and bilobalide against cerebral ischemia injury by activating the Akt/Nrf2 pathway in vitro and in vivo. Cell Stress Chaperones. 24:441–452. 2019.PubMed/NCBI View Article : Google Scholar
42	Cao G, Jiang N, Hu Y, Zhang Y, Wang G, Yin M, Ma X, Zhou K, Qi J, Yu B and Kou J: Ruscogenin attenuates cerebral ischemia-induced blood-brain barrier dysfunction by suppressing TXNIP/NLRP3 inflammasome activation and the MAPK pathway. Int J Mol Sci. 17(1418)2016.PubMed/NCBI View Article : Google Scholar
43	Bahonar A, Saadatnia M, Khorvash F, Maracy M and Khosravi A: Carotenoids as potential antioxidant agents in stroke prevention: A systematic review. Int J Prev Med. 8(70)2017.PubMed/NCBI View Article : Google Scholar
44	Törnwall ME, Virtamo J, Korhonen PA, Virtanen MJ, Albanes D and Huttunen JK: Postintervention effect of alpha tocopherol and beta carotene on different strokes: A 6-year follow-up of the alpha tocopherol, beta carotene cancer prevention study. Stroke. 35:1908–1913. 2004.PubMed/NCBI View Article : Google Scholar
45	Rabadi MH and Kristal BS: Effect of vitamin C supplementation on stroke recovery: A case-control study. Clin Interv Aging. 2:147–151. 2007.PubMed/NCBI View Article : Google Scholar
46	Suter PM: Effect of Vitamin E, Vitamin C, and beta-carotene on stroke risk. Nutr Rev. 58:184–187. 2000.PubMed/NCBI View Article : Google Scholar