Advanced multimodal neuromonitoring: applicability for the pathophysiological study of intracranial pressure plateau waves

Abstract

INTRODUCTION Multimodal neuromonitoring increases the knowledge of the physiopathology underlying the pathological slow vasogenic waves known as ‘plateau waves’ of intracranial pressure (ICP). The transcranial Doppler (TCD) pulsatility index (PI) describes changes in the morphology of the blood flow velocity (FV) waveform and is classically consider a descriptor of the distal cerebrovascular resistance (CVR). Critical closing pressure (CCP) or zero-flow pressure denotes a threshold of arterial blood pressure (ABP) at which small cerebral vessels collapse and cerebral blood flow (CBF) ceases increasing the ischemic risk. The difference between CCP and ICP is explained by the tone of the small cerebral vessels, so-called wall tension (WT). Although it has inspired theoretical interest, its clinical applicability is limited for methodological reasons.

HYPOTHESIS 1) PI is a complex function determined by the interaction of multiple haemodynamic variables, and is not solely determined by distal CVR; 2) CCP and WT estimated with a cerebrovascular impedance model, could accurately define the pathophysiological changes during plateau waves.

AIMS 1) to clarify the relationship between PI and CVR; to define which factors truly influence PI; 2) to calculate CCP and arterial WT with a novel multiparametric mathematical model in order to examine the proposed vasodilatory pathophysiology of plateau waves; to evaluate its possible clinical appliance.

SUBJECTS AND METHODS Recordings from patients with severe head-injury undergoing monitoring of ABP, ICP, cerebral perfusion pressure (CPP), and TCD assessed CBF velocities (FV) were analysed. The Gosling PI was compared between baseline and ICP plateau waves (n = 20 patients) or short-term (30–60 min) hypocapnia (n = 31). In addition, a modeling study was conducted with the ‘‘spectral’’ PI (calculated using fundamental harmonic of FV) resulting in a theoretical formula expressing the dependence of PI on balance of cerebrovascular impedances.

Multimodality neuromonitoring integrated with bio-informatics analysis (ICM+™ Software, www.neurosurg.cam.ac.uk/icmplus). Both studies are based in a multiparametric method new model of cerebrovascular impedance; first a retrospective study of 2 opposing physiological conditions comparing basal PI to: a) plateau waves (n= 20 patients, 38 plateau waves); and b) moderate hyperventilation (n=31); next CCP was calculated in the plateau waves group (n= 20). According to Burton’s model, wall tension was estimated as: WT = CCP-ICP.

RESULTS 1) PI increased significantly (p< 0.001) while CVR decreased (p< 0.001) during plateau waves. During hypocapnia both PI and CVR increased (p< 0.001). The modeling formula explained more than 65 % of the variability of Gosling PI and 90% of the variability of the ‘spectral’ PI (R=0.81 and R=0.95, respectively); 2) During the vasodilatory loop of the plateau waves, there is a rise in CCP and reduction in WT (both significant, p < 0.001). Change in CCP was correlated to ICP changes (R=0.80, p<0.001). Cerebral arterial WT decrement (a 34.3%) confirms its vasodilatatory origin. However, the effect of rising ICP is more pronounced than the corresponding vasodilatatory response decreasing WT. All results were significant with both traditional and multi-parameter methods of calculation.

The “safety collapsing margin” (ABP-CCP) decreased significantly (p < 0.001) from baseline ICP to plateau levels, indicating that the probability for brain vessels to collapse.

CONCLUSIONS 1) TCD- PI is usually misinterpreted as a descriptor of distal CVR. The presented mathematical model describes PI as a product of the interplay between CPP, the fundamental harmonic of ABP, CVR, compliance of the cerebral arterial bed and the heart rate; 2) During plateau waves, CCP increases significantly while active vasomotor tone, represented by WT, decreases due to vasodilation. A new mathematical model to estimate CCP based on the impedance methodology disallows non-physiologic negative values and provides a more physiological interpretation.

ANTECEDENTES: la neuromonitorización multimodal aumenta el conocimiento de la fisiopatología subyacente a las ondas plateau de hipertensión intracraneal. El índice de pulsatilidad (IP) del Doppler transcraneal (DTC) se considera un descriptor de las resistencias cerebrovasculares (RCV) distales. La presión crítica de cierre (critical closing pressure, CCP) es un umbral de presión arterial por debajo del cual los vasos cerebrales pequeños se colapsan interrumpiendo el flujo sanguíneo cerebral (FSC) y aumentando la lesión secundaria. Teóricamente útil, su aplicabilidad clínica está limitada por razones metodológicas.

HIPÓTESIS: 1) el IP está determinado por la interacción de múltiples variables hemodinámicas y no solo por las RCV; 2) la CCP (estimada mediante un modelo de impedancia cerebrovascular) aumenta durante las ondas plateau.

OBJETIVOS: 1) definir qué factores determinan el IP de la velocidad del FSC; 2) medir la CCP y verificar un nuevo método para su cálculo durante las ondas plateau.

METODOLOGÍA: pacientes con traumatismo craneoencefálico (TCE) monitorizados con presión arterial continua, presión intracraneal (PIC) y DTC. Análisis con un software específico (ICM+®) validado. Ambos trabajos se basan en un método multiparamétrico basado en un modelo de impedancia cerebrovascular: 1) estudio retrospectivo de 2 situaciones fisiológicas contrapuestas comparando el IP basal con: a) ondas plateau (n= 20 pacientes, 38 ondas) y b) hiperventilación moderada (n=31); 2) cálculo de la CCP en el grupo de ondas plateau (n= 20). Según el modelo de Burton la tensión de la pared arterial (wall tension, WT) se estimó como: WT = CCP-PIC.

RESULTADOS: 1) durante las ondas plateau el IP aumenta de forma significativa pero las RCV disminuyen. Durante la hipocapnia aumentan el IP y las RCV; 2) La CCP aumenta significativamente en el plateau de la onda y la WT disminuye un 34.3%. El nuevo método matemático es más fisiológico.

CONCLUSIONES: 1) El IP no es solo un descriptor de la RCV distales, existiendo una compleja relación matemática con múltiples variables hemodinámicas; 2) La CCP aumenta durante las ondas plateau, pero la WT disminuye. Se aplica un nuevo modelo matemático para calcular la CCP que permite una interpretación más fisiológica de sus valores.