Predictive Value of Fibrin Fibrinogen Degradation Products-to-Potassium Ratio for Poor Functional Outcome in Patients with Aneurysmal Subarachnoid Hemorrhage: A Retrospective Case-Control Study.

Aneurysmal subarachnoid hemorrhage Fibrin fibrinogen degradation products Hypokalemia Outcome Potassium Predict

Journal

Neurocritical care
ISSN: 1556-0961
Titre abrégé: Neurocrit Care
Pays: United States
ID NLM: 101156086

Informations de publication

Date de publication:
13 Oct 2023
Historique:
received: 09 03 2023
accepted: 19 09 2023
medline: 14 10 2023
pubmed: 14 10 2023
entrez: 13 10 2023
Statut: aheadofprint

Résumé

The relationship of fibrin(ogen) degradation products (FDPs) and potassium with the functional outcomes of patients with aneurysmal subarachnoid hemorrhage (aSAH) is still uncertain. This study aims to evaluate the predictive value of a novel combination biomarker, the FDP-to-potassium ratio (FPR), for poor functional outcomes in patients with aSAH. A total of 425 consecutive patients with aSAH at a single center were retrospectively enrolled in our study. An unfavorable outcome was defined as a modified Rankin Scale (mRS) score of 3-6 at 3 months after discharge. Univariate analysis and multivariable logistic regression were performed for baseline information and laboratory parameters recorded at admission. In addition, the receiver operating characteristic curve was plotted, and propensity score matching was performed based on the FPR. On the basis of mRS grade, 301 patients were classified as having favorable outcomes, and 124 patients were assessed as having unfavorable outcomes. FPR levels were significantly correlated with mRS grade (r[Spearman] = 0.410; P < 0.001). Multivariate logistic regression analysis showed that age (odds ratio [OR] 1.043, 95% confidence interval [CI] 1.016-1.071; P = 0.002), white blood cell count (OR 1.150, 95% CI 1.044-1.267; P = 0.005), potassium (OR 0.526, 95% CI 0.291-0.949; P = 0.033), World Federation of Neurosurgical Societies grade (OR 1.276, 95% CI 1.055-1.544; P = 0.012), and FPR (OR 1.219, 95% CI 1.102-1.349; P < 0.001) at admission were independently associated with poor functional outcomes. The DeLong test showed that the area under the receiver operating characteristic curve of FPR was higher than that of age, white blood cell count, potassium, World Federation of Neurosurgical Societies grade, or FDP alone, indicating that FPR had better predictive potential than these other variables. After 1:1 propensity score matching (FPR ≥ 1.45 vs. FPR < 1.45), the rate of poor prognosis was still significantly increased in the high-FPR group (48/121 [39.7%] vs. 16/121 [13.2%], P < 0.001). Fibrin(ogen) degradation product-to-potassium ratio is an independent predictor of poor outcomes for patients with aSAH and may be a promising tool for clinicians to evaluate patients' functional prognosis.

Sections du résumé

BACKGROUND BACKGROUND
The relationship of fibrin(ogen) degradation products (FDPs) and potassium with the functional outcomes of patients with aneurysmal subarachnoid hemorrhage (aSAH) is still uncertain. This study aims to evaluate the predictive value of a novel combination biomarker, the FDP-to-potassium ratio (FPR), for poor functional outcomes in patients with aSAH.
METHODS METHODS
A total of 425 consecutive patients with aSAH at a single center were retrospectively enrolled in our study. An unfavorable outcome was defined as a modified Rankin Scale (mRS) score of 3-6 at 3 months after discharge. Univariate analysis and multivariable logistic regression were performed for baseline information and laboratory parameters recorded at admission. In addition, the receiver operating characteristic curve was plotted, and propensity score matching was performed based on the FPR.
RESULTS RESULTS
On the basis of mRS grade, 301 patients were classified as having favorable outcomes, and 124 patients were assessed as having unfavorable outcomes. FPR levels were significantly correlated with mRS grade (r[Spearman] = 0.410; P < 0.001). Multivariate logistic regression analysis showed that age (odds ratio [OR] 1.043, 95% confidence interval [CI] 1.016-1.071; P = 0.002), white blood cell count (OR 1.150, 95% CI 1.044-1.267; P = 0.005), potassium (OR 0.526, 95% CI 0.291-0.949; P = 0.033), World Federation of Neurosurgical Societies grade (OR 1.276, 95% CI 1.055-1.544; P = 0.012), and FPR (OR 1.219, 95% CI 1.102-1.349; P < 0.001) at admission were independently associated with poor functional outcomes. The DeLong test showed that the area under the receiver operating characteristic curve of FPR was higher than that of age, white blood cell count, potassium, World Federation of Neurosurgical Societies grade, or FDP alone, indicating that FPR had better predictive potential than these other variables. After 1:1 propensity score matching (FPR ≥ 1.45 vs. FPR < 1.45), the rate of poor prognosis was still significantly increased in the high-FPR group (48/121 [39.7%] vs. 16/121 [13.2%], P < 0.001).
CONCLUSIONS CONCLUSIONS
Fibrin(ogen) degradation product-to-potassium ratio is an independent predictor of poor outcomes for patients with aSAH and may be a promising tool for clinicians to evaluate patients' functional prognosis.

Identifiants

pubmed: 37833519
doi: 10.1007/s12028-023-01865-4
pii: 10.1007/s12028-023-01865-4
doi:

Types de publication

Journal Article

Langues

eng

Sous-ensembles de citation

IM

Subventions

Organisme : National College Students Innovation and Entrepreneurship Training Program
ID : 202210634045
Organisme : National College Students Innovation and Entrepreneurship Training Program
ID : 202210634026
Organisme : Cooperation Project of Nanchong City and North Sichuan Medical College
ID : 20SXKT0317
Organisme : Research development program of North Sichuan Medical College
ID : CBY-20-QA-Z02

Informations de copyright

© 2023. The Author(s).

Références

Suwatcharangkoon S, Meyers E, Falo C, et al. Loss of consciousness at onset of subarachnoid hemorrhage as an important marker of early brain injury. JAMA Neurol. 2016;73(1):28–35. https://doi.org/10.1001/jamaneurol.2015.3188 .
doi: 10.1001/jamaneurol.2015.3188 pubmed: 26552033
Suarez JI, Tarr RW, Selman WR. Aneurysmal subarachnoid hemorrhage. N Engl J Med. 2006;354(4):387–96. https://doi.org/10.1056/NEJMra052732 .
doi: 10.1056/NEJMra052732 pubmed: 16436770
van Lieshout JH, Dibué-Adjei M, Cornelius JF, et al. An introduction to the pathophysiology of aneurysmal subarachnoid hemorrhage. Neurosurg Rev. 2018;41(4):917–30. https://doi.org/10.1007/s10143-017-0827-y .
doi: 10.1007/s10143-017-0827-y pubmed: 28215029
Teasdale GM, Drake CG, Hunt W, et al. A universal subarachnoid hemorrhage scale: report of a committee of the World Federation of Neurosurgical Societies. J Neurol Neuros Psychiatry. 1988;51(11):1457. https://doi.org/10.1136/jnnp.51.11.1457 .
doi: 10.1136/jnnp.51.11.1457
Teasdale G, Jennett B. Assessment of coma and impaired consciousness. A practical scale. Lancet (Lond Engl). 1974;2(7872):81–4. https://doi.org/10.1016/s0140-6736(74)91639-0 .
doi: 10.1016/s0140-6736(74)91639-0
Frontera JA, Claassen J, Schmidt JM, et al. Prediction of symptomatic vasospasm after subarachnoid hemorrhage: the modified fisher scale. Neurosurgery 2006;59(1):21–7; discussion 21–7. https://doi.org/10.1227/01.Neu.0000218821.34014.1b .
Fujiki Y, Matano F, Mizunari T, et al. Serum glucose/potassium ratio as a clinical risk factor for aneurysmal subarachnoid hemorrhage. J Neurosurg. 2018;129(4):870–5. https://doi.org/10.3171/2017.5.Jns162799 .
doi: 10.3171/2017.5.Jns162799 pubmed: 29148905
Fung C, Inglin F, Murek M, et al. Reconsidering the logic of World Federation of Neurosurgical Societies grading in patients with severe subarachnoid hemorrhage. J Neurosurg. 2016;124(2):299–304. https://doi.org/10.3171/2015.2.Jns14614 .
doi: 10.3171/2015.2.Jns14614 pubmed: 26381248
Zhang D, Zhuang Z, Wei Y, et al. Association of admission serum glucose-phosphate ratio with severity and prognosis of aneurysmal subarachnoid hemorrhage. World Neurosurg. 2019;127:e1145–51. https://doi.org/10.1016/j.wneu.2019.04.071 .
doi: 10.1016/j.wneu.2019.04.071 pubmed: 30995552
Qiu SZ, Zheng GR, Chen B, Huang JJ, Shen J, Mao W. Prognostic value of admission serum glucose-phosphate ratio in predicting the 6-month outcome of patients with severe traumatic brain injury: a retrospective study. Clin Chim Acta. 2020;510:659–64. https://doi.org/10.1016/j.cca.2020.08.038 .
doi: 10.1016/j.cca.2020.08.038 pubmed: 32882225
Fountas KN, Tasiou A, Kapsalaki EZ, et al. Serum and cerebrospinal fluid C-reactive protein levels as predictors of vasospasm in aneurysmal subarachnoid hemorrhage. Clin Artic Neurosurg Focus. 2009;26(5):E22. https://doi.org/10.3171/2009.2.Focus08311 .
doi: 10.3171/2009.2.Focus08311
Wang XT, Xu YH. Platelets-to-serum Ca2+ ratio as a risk factor for postoperative cerebral vasospasm in surgically treated aneurysmal subarachnoid hemorrhage patients. Eur Rev Med Pharmacol Sci. 2022;26(5):1439–49. https://doi.org/10.26355/eurrev_202203_28207 .
doi: 10.26355/eurrev_202203_28207 pubmed: 35302188
Zhang X, Zhang S, Wang C, Liu R, Li A. High neutrophil-to-albumin ratio predicts postoperative pneumonia in aneurysmal subarachnoid hemorrhage. Front Neurol. 2022;13:840858. https://doi.org/10.3389/fneur.2022.840858 .
doi: 10.3389/fneur.2022.840858 pubmed: 35463142 pmcid: 9021997
Jung HM, Paik JH, Kim SY, Hong DY. Association of plasma glucose to potassium ratio and mortality after aneurysmal subarachnoid hemorrhage. Front Neurol. 2021;12:661689. https://doi.org/10.3389/fneur.2021.661689 .
doi: 10.3389/fneur.2021.661689 pubmed: 34017305 pmcid: 8129165
He J, Zhang Y, Li T, et al. Glucose-albumin ratio as new biomarker for predicting mortality after intracerebral hemorrhage. Neurosurg Rev. 2023;46(1):94. https://doi.org/10.1007/s10143-023-02002-7.16 .
doi: 10.1007/s10143-023-02002-7.16 pubmed: 37074539
Navarro J, Kang I, Hwang HK, Yoon DS, Lee WJ, Kang CM. Glucose to lymphocyte ratio as a prognostic marker in patients with resected pT2 gallbladder cancer. J Surg Res. 2019;240:17–29. https://doi.org/10.1016/j.jss.2019.02.043 .
doi: 10.1016/j.jss.2019.02.043 pubmed: 30909062
Geraghty JR, Testai FD. Delayed cerebral ischemia after subarachnoid hemorrhage: beyond vasospasm and towards a multifactorial pathophysiology. Curr Atheroscler Rep. 2017;19(12):50. https://doi.org/10.1007/s11883-017-0690-x .
doi: 10.1007/s11883-017-0690-x pubmed: 29063300
Fang F, Wang P, Yao W, et al. Association between D-dimer levels and long-term mortality in patients with aneurysmal subarachnoid hemorrhage. Neurosurg Focus. 2022;52(3):E8. https://doi.org/10.3171/2021.12.Focus21512 .
doi: 10.3171/2021.12.Focus21512 pubmed: 35231898
Fukuda H, Lo B, Yamamoto Y, et al. Plasma D-dimer may predict poor functional outcomes through systemic complications after aneurysmal subarachnoid hemorrhage. J Neurosurg. 2017;127(2):284–90. https://doi.org/10.3171/2016.5.Jns16767 .
doi: 10.3171/2016.5.Jns16767 pubmed: 27518526
Hurth H, Birkenhauer U, Steiner J, Schlak D, Hennersdorf F, Ebner FH. Delayed cerebral ischemia in patients with aneurysmal subarachnoid hemorrhage—serum D-dimer and C-reactive protein as early markers. J Stroke Cerebrovasc Dis. 2020;29(3):104558. https://doi.org/10.1016/j.jstrokecerebrovasdis.2019.104558 .
doi: 10.1016/j.jstrokecerebrovasdis.2019.104558 pubmed: 31889655
Juvela S, Siironen J. D-dimer as an independent predictor for poor outcome after aneurysmal subarachnoid hemorrhage. Stroke. 2006;37(6):1451–6. https://doi.org/10.1161/01.Str.0000221710.55467.33 .
doi: 10.1161/01.Str.0000221710.55467.33 pubmed: 16690901
Liu JH, Li XK, Chen ZB, et al. D-dimer may predict poor outcomes in patients with aneurysmal subarachnoid hemorrhage: a retrospective study. Neural Regener Res. 2017;12(12):2014–20. https://doi.org/10.4103/1673-5374.221158 .
doi: 10.4103/1673-5374.221158
Chen I, Mitchell P. Serum potassium and sodium levels after subarachnoid haemorrhage. Br J Neurosurg. 2016;30(5):554–9. https://doi.org/10.1080/02688697.2016.1181151 .
doi: 10.1080/02688697.2016.1181151 pubmed: 27248003
Wang J, Feng Q, Zhang Y, Qiu W, Gao H. Elevated glucose-potassium ratio predicts preoperative rebleeding in patients with aneurysmal subarachnoid hemorrhage. Front Neurol. 2021;12:795376. https://doi.org/10.3389/fneur.2021.795376 .
doi: 10.3389/fneur.2021.795376 pubmed: 35095738
Collins GS, Reitsma JB, Altman DG, Moons KG. Transparent reporting of a multivariable prediction model for individual prognosis or diagnosis (TRIPOD): the TRIPOD statement. BMJ (Clin Res Ed). 2015;350:g7594. https://doi.org/10.1136/bmj.g7594 .
doi: 10.1136/bmj.g7594
Vergouwen MD, Vermeulen M, van Gijn J, et al. Definition of delayed cerebral ischemia after aneurysmal subarachnoid hemorrhage as an outcome event in clinical trials and observational studies: proposal of a multidisciplinary research group. Stroke. 2010;41(10):2391–5. https://doi.org/10.1161/strokeaha.110.589275 .
doi: 10.1161/strokeaha.110.589275 pubmed: 20798370
Vilar R, Fish RJ, Casini A, Neerman-Arbez M. Fibrin(ogen) in human disease: both friend and foe. Haematologica. 2020;105(2):284–96. https://doi.org/10.3324/haematol.2019.236901 .
doi: 10.3324/haematol.2019.236901 pubmed: 31949010 pmcid: 7012490
Davalos D, Akassoglou K. Fibrinogen as a key regulator of inflammation in disease. Semin Immunopathol. 2012;34(1):43–62. https://doi.org/10.1007/s00281-011-0290-8 .
doi: 10.1007/s00281-011-0290-8 pubmed: 22037947
Petersen MA, Ryu JK, Akassoglou K. Fibrinogen in neurological diseases: mechanisms, imaging and therapeutics. Nat Rev Neurosci. 2018;19(5):283–301. https://doi.org/10.1038/nrn.2018.13 .
doi: 10.1038/nrn.2018.13 pubmed: 29618808 pmcid: 6743980
Göbel K, Eichler S, Wiendl H, Chavakis T, Kleinschnitz C, Meuth SG. The coagulation factors fibrinogen, thrombin, and factor XII in inflammatory disorders—a systematic review. Front Immunol. 2018;9:1731. https://doi.org/10.3389/fimmu.2018.01731 .
doi: 10.3389/fimmu.2018.01731 pubmed: 30105021 pmcid: 6077258
Ono Y, Hayakawa M, Maekawa K, et al. Fibrin/fibrinogen degradation products (FDP) at hospital admission predict neurological outcomes in out-of-hospital cardiac arrest patients. Resuscitation. 2017;111:62–7. https://doi.org/10.1016/j.resuscitation.2016.11.017 .
doi: 10.1016/j.resuscitation.2016.11.017 pubmed: 27940211
Hori YS, Ebisudani Y, Aoi M, Fukuhara T. Elevated serum fibrinogen degradation products on admission is a novel predictive factor for recurrence of chronic subdural hematoma. World Neurosurg. 2018;118:e753–7. https://doi.org/10.1016/j.wneu.2018.07.039 .
doi: 10.1016/j.wneu.2018.07.039 pubmed: 30026157
Yakovlev S, Strickland DK, Medved L. Current view on the molecular mechanisms underlying fibrin(ogen)-dependent inflammation. Thromb Haemost. 2022;122(11):1858–68. https://doi.org/10.1055/a-1910-4538 .
doi: 10.1055/a-1910-4538 pubmed: 35896433
Luyendyk JP, Schoenecker JG, Flick MJ. The multifaceted role of fibrinogen in tissue injury and inflammation. Blood. 2019;133(6):511–20. https://doi.org/10.1182/blood-2018-07-818211 .
doi: 10.1182/blood-2018-07-818211 pubmed: 30523120 pmcid: 6367649
Norris EH, Strickland S. Fibrinogen in the nervous system: glia beware. Neuron. 2017;96(5):951–3. https://doi.org/10.1016/j.neuron.2017.11.021 .
doi: 10.1016/j.neuron.2017.11.021 pubmed: 29216454 pmcid: 6782050
Ryu JK, Davalos D, Akassoglou K. Fibrinogen signal transduction in the nervous system. J Thromb Haemost JTH. 2009;7(Suppl 1):151–4. https://doi.org/10.1111/j.1538-7836.2009.03438.x .
doi: 10.1111/j.1538-7836.2009.03438.x pubmed: 19630789
Tsantes AG, Parastatidou S, Tsantes EA, et al. Sepsis-induced coagulopathy: an update on pathophysiology, biomarkers, and current guidelines. Life (Basel, Switzerland). 2023. https://doi.org/10.3390/life13020350 .
doi: 10.3390/life13020350 pubmed: 36836706
Chen S, Li Q, Wu H, Krafft PR, Wang Z, Zhang JH. The harmful effects of subarachnoid hemorrhage on extracerebral organs. BioMed Res Int. 2014;2014:858496. https://doi.org/10.1155/2014/858496 .
doi: 10.1155/2014/858496 pubmed: 25110700 pmcid: 4109109
Massara F, Tripodina A, Rotunno M. Propranolol block of epinephrine-induced hypokaliaemia in man. Eur J Pharmacol. 1970;10(3):404–7. https://doi.org/10.1016/0014-2999(70)90214-1 .
doi: 10.1016/0014-2999(70)90214-1 pubmed: 5422467
Beseoglu K, Etminan N, Steiger HJ, Hänggi D. The relation of early hypernatremia with clinical outcome in patients suffering from aneurysmal subarachnoid hemorrhage. Clin Neurol Neurosurg. 2014;123:164–8. https://doi.org/10.1016/j.clineuro.2014.05.022 .
doi: 10.1016/j.clineuro.2014.05.022 pubmed: 24956546
Koide M, Bonev AD, Nelson MT, Wellman GC. Inversion of neurovascular coupling by subarachnoid blood depends on large-conductance Ca2+-activated K+ (BK) channels. Proc Natl Acad Sci USA. 2012;109(21):E1387–95. https://doi.org/10.1073/pnas.1121359109 .
doi: 10.1073/pnas.1121359109 pubmed: 22547803 pmcid: 3361424
Antunes AP, Schiefecker AJ, Beer R, et al. Higher brain extracellular potassium is associated with brain metabolic distress and poor outcome after aneurysmal subarachnoid hemorrhage. Crit Care (Lond Engl). 2014;18(3):R119. https://doi.org/10.1186/cc13916 .
doi: 10.1186/cc13916
Ybanez N, Agrawal V, Tranmer BI, Gennari FJ. Severe hypokalemia in a patient with subarachnoid hemorrhage. Am J Kidney Dis. 2014;63(3):530–5. https://doi.org/10.1053/j.ajkd.2013.07.005 .
doi: 10.1053/j.ajkd.2013.07.005 pubmed: 23972266

Auteurs

Weida Li (W)

Department of Neurosurgery, Affiliated Hospital of North Sichuan Medical College, Nanchong, 637000, China.
School of Clinical Medicine, North Sichuan Medical College, Nanchong, 637000, China.
Neurosurgical Research Center, Affiliated Hospital of North Sichuan Medical College, Nanchong, 637000, China.

Shuangquan Zhao (S)

Neurosurgical Research Center, Affiliated Hospital of North Sichuan Medical College, Nanchong, 637000, China.
Department of Emergency, Affiliated Hospital of North Sichuan Medical College, Nanchong, 637000, China.

Xinlong Chen (X)

Department of Neurosurgery, Affiliated Hospital of North Sichuan Medical College, Nanchong, 637000, China.
School of Clinical Medicine, North Sichuan Medical College, Nanchong, 637000, China.

Yi Zhang (Y)

Department of Neurosurgery, Affiliated Hospital of North Sichuan Medical College, Nanchong, 637000, China.
School of Clinical Medicine, North Sichuan Medical College, Nanchong, 637000, China.

Ping Lin (P)

Department of Neurosurgery, Affiliated Hospital of North Sichuan Medical College, Nanchong, 637000, China.
School of Clinical Medicine, North Sichuan Medical College, Nanchong, 637000, China.

Xingyuan Huang (X)

School of Psychiatry, North Sichuan Medical College, Nanchong, 637000, China.

Simeng Yi (S)

Department of Neurosurgery, Affiliated Hospital of North Sichuan Medical College, Nanchong, 637000, China.
School of Clinical Medicine, North Sichuan Medical College, Nanchong, 637000, China.

Xuehai Deng (X)

Department of Neurosurgery, Affiliated Hospital of North Sichuan Medical College, Nanchong, 637000, China.
School of Clinical Medicine, North Sichuan Medical College, Nanchong, 637000, China.

Jianlin Ding (J)

Department of Neurosurgery, Affiliated Hospital of North Sichuan Medical College, Nanchong, 637000, China.
School of Clinical Medicine, North Sichuan Medical College, Nanchong, 637000, China.

Mingkai Xia (M)

School of Medical Imaging, North Sichuan Medical College, Nanchong, 637000, China.

Peijun Tang (P)

School of Medical Imaging, North Sichuan Medical College, Nanchong, 637000, China.

Xiaoping Tang (X)

Department of Neurosurgery, Affiliated Hospital of North Sichuan Medical College, Nanchong, 637000, China.
School of Clinical Medicine, North Sichuan Medical College, Nanchong, 637000, China.
Neurosurgical Research Center, Affiliated Hospital of North Sichuan Medical College, Nanchong, 637000, China.

Long Zhao (L)

Department of Neurosurgery, Affiliated Hospital of North Sichuan Medical College, Nanchong, 637000, China. cbyzhaolong@163.com.
School of Clinical Medicine, North Sichuan Medical College, Nanchong, 637000, China. cbyzhaolong@163.com.
Neurosurgical Research Center, Affiliated Hospital of North Sichuan Medical College, Nanchong, 637000, China. cbyzhaolong@163.com.

Classifications MeSH