Fluid administration strategies in traumatic brain injury

Abdulrahman Alharthy; Waleed Tharwat Aletreby; Ibrahim Soliman; Fahad AlFaqihi; Waseem Alzayer; Nassir Nasim Mahmoud; Lawrence Marshall Gillman; Dimitrios Karakitsos

doi:10.4103/2543-1854.259472

REVIEW ARTICLES

Year : 2019 | Volume : 3 | Issue : 1 | Page : 15-18

Fluid administration strategies in traumatic brain injury

Abdulrahman Alharthy¹, Waleed Tharwat Aletreby¹, Ibrahim Soliman¹, Fahad AlFaqihi¹, Waseem Alzayer¹, Nassir Nasim Mahmoud¹, Lawrence Marshall Gillman², Dimitrios Karakitsos³
¹ Department of Critical Care, Neurocritical Care Unit, King Saud Medical City, Riyadh, KSA
² Department of Surgery, Rady Faculty of Health Science, University of Manitoba, Winnipeg, MB, Canada
³ Department of Critical Care, Neurocritical Care Unit, King Saud Medical City, Riyadh, KSA; Department of Critical Care, Keck School of Medicine, USC, LA, CA, USA

Date of Web Publication

30-May-2019

Correspondence Address:
Abdulrahman Alharthy
Department of Critical Care, Neurocritical Care Unit, King Saud Medical City, Riyadh
KSA

Source of Support: None, Conflict of Interest: None

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DOI: 10.4103/2543-1854.259472

Abstract

Fluid restriction strategies may reduce morbidity and mortality in critical care patients and are currently trending as preliminary data showed encouraging results. A positive fluid balance was related to increase morbidity and mortality in a variety of disorders (i.e., sepsis, acute respiratory distress syndrome, and postsurgical cases) as well as resulted in an increased rate of complications observed in the intensive care unit setting. Traumatic brain injury (TBI) has been managed thus far in terms of fluid resuscitation under the concept of general trauma resuscitation recommendations that favored euvolemia above all fluid balance states. Notwithstanding, scarce data exist to clarify details about fluid management strategies in TBI such as the desirable fluid balance per se and/or its impact on patients' outcomes. We, therefore, reviewed previously published data and concluded in an observational manner (by creating a visual display model) that a highly positive and/or a negative fluid balance may have a detrimental impact on the prognosis of TBI patients. Accordingly, well-designed randomized controlled trials are clearly required to investigate further and in detail the most efficacious fluid administration strategies in TBI contributing thus in the rapidly expanding field of neurocritical care.

Keywords: Fluid balance, randomized controlled trials, traumatic brain injury

How to cite this article:
Alharthy A, Aletreby WT, Soliman I, AlFaqihi F, Alzayer W, Mahmoud NN, Gillman LM, Karakitsos D. Fluid administration strategies in traumatic brain injury. Saudi Crit Care J 2019;3:15-8

How to cite this URL:
Alharthy A, Aletreby WT, Soliman I, AlFaqihi F, Alzayer W, Mahmoud NN, Gillman LM, Karakitsos D. Fluid administration strategies in traumatic brain injury. Saudi Crit Care J [serial online] 2019 [cited 2023 Jun 4];3:15-8. Available from: https://www.sccj-sa.org/text.asp?2019/3/1/15/259472

Introduction

Traumatic brain injury (TBI) is one of the major causes of mortality and disability worldwide.^[1] In the United Kingdom, the incidence of TBI is 1.4 million cases per year with the majority being mild.^[2] The World Health Organization predicts increased rates of TBI by 2020.^[3] The burden of TBI on health-care systems in terms of the utilization of resources^[4] and on the community in terms of social functionality of TBI victims remains a major challenge.^[5] The sheer magnitude of the health-care issue imposed by TBI has led to the development of several management protocols such as the brain trauma foundation guidelines among others.^[6]

The aforementioned guidelines include versatile and detailed aspects of TBI management; however, when it comes to fluid balance data appear to be incomplete. Most TBI guidelines recommend euvolemia using isotonic fluids although no specific recommendations on the amount of fluids to be administered or total fluid balance to be achieved exist thus far.^[7] Notwithstanding, the positive fluid balance was related to detrimental effects on mortality, mechanical ventilation days, and lung function in critical care patients.^[8] Volume overloading was reported as an independent prognostic factor of mortality in critically ill sepsis patients.^[9] The former was associated with increased mortality risk even after adjustment for chronic medical conditions and different severity markers of illness at the time of intensive care unit (ICU) discharge.^[10] In contrast, the achievement of a negative fluid balance in surgical critically ill patients was associated with mortality reduction.^[11] Whether a comparable to the aforementioned fluid strategy trend might be the case in TBI management remains unclear. Hence, the aim of this review was to examine the available body of evidence regarding the impact of fluid balance on TBI outcomes.

Pathophysiological Considerations

Fluid balance management in TBI aims on restoring intravascular volume and stabilizing hemodynamics to ensure adequate cerebral perfusion pressures (CPPs).^[12] The former may be particularly important in TBI as various complex factors play a joining role in determining the effect of fluid volume on cerebral blood flow and cerebral tissue oxygenation such as the disruption of blood–brain barrier (BBB), inflammatory mediators, and cerebral autoregulatory mechanisms. Moreover, TBI patients are prone to intravascular, osmotic, and electrolyte disturbances due to central neuroendocrine disturbances.^[7]

Under normal circumstances, fluid shifts across an intact BBB are compensated by the neurons through active solute depletion to the extracellular compartment and the endothelial cells of BBB to expel water to the intravascular compartment.^[13] The aforementioned mechanisms are impaired in TBI thus fluid shifts become more dependent on pressure differences between intravascular and extravascular compartments.

Fluid balance could affect CPP in two ways: driving-in and driving-out. The obvious driving-in force is that of the arterial pressure. The driving-out mechanism is attributed mainly to the venous pressure. When the latter is high and/or the arterial pressure is low, CPP could be significantly reduced depending surely on impaired cerebral autoregulation.^[14] Normally, high central venous pressure (CVP) should not be reflected on the intracranial venous circuits when the intracranial venous structures are collapsed due to a higher intracranial pressure (ICP).^[15] However, this might be the case when CVP exceeds ICP in mechanically ventilated patients baring an extremely high positive end-expiratory pressure.^[16],[17]

Methods

This was a nonsystematic electronic literature search integrating articles reporting the impact of fluid balance on TBI outcomes. There were no restrictions imposed on language, age of patients, year of publication, or methodology of the study; however, we excluded studies analyzing solely other causes of brain injury. We searched for relevant articles in PubMed and EMBASE databases. We did not attempt to evaluate the quality or risk of bias of individual studies.

Results

Our search revealed seven major studies that were included in this review. Notably, only two studies were randomized controlled trials (RCT). None of the aforementioned studies was originally designed to investigate the impact of fluid balance on TBI. Five studies were retrospectively analyzing data of patients' medical records or commenting on data of other studies. [Table 1] summarizes the results of included trials.

Table 1: Literature data summary

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The study by Roquilly et al., 2013,^[18] recruited both TBI and subarachnoid hemorrhage mechanically ventilated patients, who were randomized to either isotonic balanced solution or isotonic sodium chloride for 48 hrs reported neither differences in fluid status between the two groups nor difference in ICU mortality and length of ICU stay.

Ichai et al., 2013,^[19] conducted an RCT on 60 TBI patients integrating ICP monitoring which were randomized to receive half molar lactated ringer versus saline at a rate of 0.5 ml/kg/h for 48 h. The saline group had significantly higher 48 h fluid balance in ml/kg (27 [11–43] vs. 5 [−5–19], P < 0.01). The former group exhibited more episodes of high ICP; however, poor neurological outcome (death, vegetative state, or severe disability) was not different at 6 months even though more survivors in the saline group had poorer outcome (P = 0.16).

Clifton et al., 2002,^[20] studied the impact of fluid balance on ICP and CPP in a retrospective manner. When the patients were stratified in quartiles of 4 days' fluid balance, poor outcome (death, severe disability, or vegetative state) occurred more frequently in the group with balance <−594 ml followed by the group with balance >4859, while the euvolemic group exhibited better outcomes. None of the aforementioned differences were statistically significant; however, stepwise logistic regression analysis revealed that fluid balance <−594 was significantly associated with poor outcomes (P = 0.005).

Another study by Fletcher et al., 2010,^[21] revealed that fluid balance was not a predictor of refractory intracranial hypertension, whereas it was a predictor for the development of pulmonary edema (Hazard Ratio 1.69 [95% confidence interval [CI] 1.4–2.04], P < 0.0001).

The impact of fluid balance on ICP was reported to be significant by Moore et al., 2015,^[22] in a retrospective analysis of 100 adult TBI patients. Those with a positive fluid balance between days 3 and 7 had a higher mean ICP (13.9 vs. 12.6 mmHg, P = 0.05), and when adjusted for confounders, a more positive fluid balance in days 3–7 was significantly associated with an increase of mean ICP (P = 0.04).

Similar results were reported by Zhao et al. 2016^[23] in a retrospective analysis of 351 adult patients with moderate-to-severe TBI. Patients at the low (<637 mL) and upper (>3673 mL) tertiles of fluid balance were associated with poor outcomes. More patients in the upper tertile had ICP higher than 20 mmHg (P = 0.009). A fluid balance in the upper tertile was an independent predictor of poor 30 days' clinical outcomes after the adjustment for confounding variables in a multivariable logistic regression model (odds ratio: 1.373 [95% CI 1.003–1.880) P = 0.047].

Finally, in a post hoc analysis^[24] derived from the data of TBI and cerebrovascular accident patients who participated in an observational study about the occurrence of sepsis, survivors had a significantly lower mean fluid balance compared to nonsurvivors (−0.2 ± 11.1 vs. 0.1 ± 1.5 l, P < 0.05).

Discussion

A positive fluid balance observed at different stages of ICU hospitalization was found to be harmful in critically ill patients with sepsis, influenza, cancer as well as in postsurgical cases.^{[8],[9],[10],[11],[25]} In TBI patients, scarce data exist to support that fluid resuscitation should be directed toward euvolemia by the administration of isotonic fluids. Previously published data suggested that both volume overloading and depletion should be avoided.^[25] However, there is still limited evidence that loading brain-injured patients with fluids may exacerbate brain edema formation when the BBB is disrupted; and that hypervolemia may be detrimental as appears to be the case in nonbrain injured patients. Furthermore, evaluating different types of traumatic injuries which may coexist in a TBI patient such as other blunt or penetrating torso and/or extremity trauma is vital especially in acute clinical settings. Therefore, adopting a suitable fluid resuscitation strategy to achieve desirable hemodynamic targets should be individualized for each patient as it remains largely a multifactorial clinical decision.

Studies evaluating the impact of fluid balance on TBI outcomes are scarce. Most published studies are retrospective and/or observational and thus not designed to evaluate the aforementioned endpoint per se the latter seems to be the case for RCTs that are originally designed and powered for a different outcome. Hence, no safe conclusions can be drawn regarding the impact of fluid balance on TBI outcomes that are free of confounders and/or attributed solely to that factor. Notwithstanding, the studies that were analyzed in this review suggested that poor outcomes in TBI patients, namely death, severe disability, or vegetative state, were mainly observed when positive and/or negative fluid balance occurred while euvolemia was associated with better prognosis. This observation when visually displayed could be tailored as a curve baring one end (positive fluid balance) higher than the other one (negative fluid balance) while the area in the middle of the curve (low incidence of poor TBI outcomes) represents euvolemic states. Moreover, published data revealed that as the fluid balance increased so did the rate of various complications such as high ICP, pulmonary edema, and acute respiratory distress syndrome in a linear manner which can be further superimposed on the aforementioned curve as an inclined straight line creating thus a “gondola-like” visual display model. Analyzing further the latter is beyond the scopes of the current review.

Our study has several limitations which are mainly attributed to its inherent nature. There was no statistical analysis or estimation of the overall effect of the pooled data from included studies as the latter were scarce. However, we managed to tailor a visual display model that underpins the effect of fluid balance on TBI based on previously published data. The aforementioned model illustrates that volume overloading is associated with a poor prognosis and increased rate of complications in TBI. Adequately powered RCTs specifically designed to study the impact of fluid balance on TBI outcomes while controlling for other factors are required. Further research studies could shed more light to previous observations and hopefully establish “cut-off” values for the administration of fluids in the management of TBI.

Financial support and sponsorship

Nil.

Conflicts of interest

There are no conflicts of interest.

References

1.	Sharma D, Vavilala MS. Perioperative management of adult traumatic brain injury. Anesthesiol Clin 2012;30:333-46.
2.	Yates PJ, Williams WH, Harris A, Round A, Jenkins R. An epidemiological study of head injuries in a UK population attending an emergency department. J Neurol Neurosurg Psychiatry 2006;77:699-701.
3.	Maas AI, Stocchetti N, Bullock R. Moderate and severe traumatic brain injury in adults. Lancet Neurol 2008;7:728-41.
4.	Ponsford JL, Spitz G, Cromarty F, Gifford D, Attwood D. Costs of care after traumatic brain injury. J Neurotrauma 2013;30:1498-505.
5.	Temkin NR, Corrigan JD, Dikmen SS, Machamer J. Social functioning after traumatic brain injury. J Head Trauma Rehabil 2009;24:460-7.
6.	Carney N, Totten AM, O'Reilly C, Ullman JS, Hawryluk GW, Bell MJ, et al. Guidelines for the management of severe traumatic brain injury, fourth edition. Neurosurgery 2017;80:6-15.
7.	van der Jagt M. Fluid management of the neurological patient: A concise review. Crit Care 2016;20:126.
8.	McDermid RC, Raghunathan K, Romanovsky A, Shaw AD, Bagshaw SM. Controversies in fluid therapy: Type, dose and toxicity. World J Crit Care Med 2014;3:24-33.
9.	Acheampong A, Vincent JL. A positive fluid balance is an independent prognostic factor in patients with sepsis. Crit Care 2015;19:251.
10.	Lee J, de Louw E, Niemi M, Nelson R, Mark RG, Celi LA, et al. Association between fluid balance and survival in critically ill patients. J Intern Med 2015;277:468-77.
11.	Barmparas G, Liou D, Lee D, Fierro N, Bloom M, Ley E, et al. Impact of positive fluid balance on critically ill surgical patients: A prospective observational study. J Crit Care 2014;29:936-41.
12.	Monteiro JN, Goraksha SU. 'ROSE concept' of fluid management: Relevance in neuroanaesthesia and neurocritical care. J Neuroanaesthesiol Crit Care 2017;4:10-6. [Full text]
13.	Ertmer C, Van Aken H. Fluid therapy in patients with brain injury: What does physiology tell us? Crit Care 2014;18:119.
14.	Leone M, Asfar P, Radermacher P, Vincent JL, Martin C. Optimizing mean arterial pressure in septic shock: A critical reappraisal of the literature. Crit Care 2015;19:101.
15.	Luce JM, Huseby JS, Kirk W, Butler J. A starling resistor regulates cerebral venous outflow in dogs. J Appl Physiol Respir Environ Exerc Physiol 1982;53:1496-503.
16.	Kurishima C, Tsuda M, Shiima Y, Kasai M, Abe S, Ohata J, et al. Coupling of central venous pressure and intracranial pressure in a 6-year-old patient with fontan circulation and intracranial hemorrhage. Ann Thorac Surg 2011;91:1611-3.
17.	Mascia L, Grasso S, Fiore T, Bruno F, Berardino M, Ducati A. Cerebro-pulmonary interactions during the application of low levels of positive end-expiratory pressure. Intensive Care Med 2005;31:373-9.
18.	Roquilly A, Loutrel O, Cinotti R, Rosenczweig E, Flet L, Mahe PJ, et al. Balanced versus chloride-rich solutions for fluid resuscitation in brain-injured patients: A randomised double-blind pilot study. Crit Care 2013;17:R77.
19.	Ichai C, Payen JF, Orban JC, Quintard H, Roth H, Legrand R, et al. Half-molar sodium lactate infusion to prevent intracranial hypertensive episodes in severe traumatic brain injured patients: A randomized controlled trial. Intensive Care Med 2013;39:1413-22.
20.	Clifton GL, Miller ER, Choi SC, Levin HS. Fluid thresholds and outcome from severe brain injury. Crit Care Med 2002;30:739-45.
21.	Fletcher JJ, Bergman K, Blostein PA, Kramer AH. Fluid balance, complications, and brain tissue oxygen tension monitoring following severe traumatic brain injury. Neurocrit Care 2010;13:47-56.
22.	Moore E, Saxby ER, Wang J, Pilcher M, Bailey D, Heritier S, et al. The impact of fluid balance on intracranial pressure in patients with traumatic brain injury. Intensive Care Med Exp 2015;3 Suppl 1:A439.
23.	Zhao Z, Wang D, Jia Y, Tian Y, Wang Y, Wei Y, et al. Analysis of the association of fluid balance and short-term outcome in traumatic brain injury. J Neurol Sci 2016;364:12-8.
24.	Mascia L, Sakr Y, Pasero D, Payen D, Reinhart K, Vincent JL, et al. Extracranial complications in patients with acute brain injury: A post hoc analysis of the SOAP study. Intensive Care Med 2008;34:720-7.
25.	Chao WC, Tseng CH, Chien YC, Sheu CC, Tsai MJ, Fang WF, et al. Association of day 4 cumulative fluid balance with mortality in critically ill patients with influenza: A multicenter retrospective cohort study in Taiwan. PLoS One 2018;13:e0190952.