The predictive value of neurally adjusted ventilatory assist indexes for the outcome of patients with severe hemorrhagic stroke

doi:10.21203/rs.3.rs-2096814/v1

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The predictive value of neurally adjusted ventilatory assist indexes for the outcome of patients with severe hemorrhagic stroke

https://doi.org/10.21203/rs.3.rs-2096814/v1

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Objective: This study assessed the predictive value of electrical activity of the diaphragm (EAdi) and the EAdi-derived monitoring index in the outcome of patients with severe hemorrhagic stroke. Methods: Ninety patients with severe hemorrhagic stroke were admitted to the neurosurgery intensive care unit of Yijishan Hospital from April 2019 to June 2021 and were divided into the good outcome group (Glasgow Outcome Scale [GOS] ≥4) and poor outcome group [GOS]≤3). The receiver operating characteristic (ROC) curve and area under the curve (AUC) were used to evaluate prediction accuracy. Results: EAdi, neuro-ventilatory efficiency (NVE), and neuro-muscular efficiency (NME) in patients with good outcome were significantly higher than those in patients with poor outcome (4.707 µV vs 2.80 µV, P < 0.001; 141.85 ml/µV vs 66.01 ml/µV, P = 0.000; 2.57 cm H₂O/µV vs 1.37 cm H₂O/µV, P = 0.000). The area under the ROC curve for the EAdi score was 0.719, with sensitivity of 69.70% and specificity of 68.42% when EAdi was 3.6 µV. The AUC for NVE score was 0.793, with sensitivity of 75.76% and specificity of 77.19% when the NVE value was 95.32 ml/µV. The AUC for NME score was 0.792, with sensitivity of 69.70% and specificity of 78.95% when the NME value was 2.06 H₂O/µV. The 6-month survival time of patients with higher EAdi, NVE, and NME was significantly longer than that of patients with lower EAdi, NVE, and NME. Conclusion: EAdi, NVE, and NME can be used as indices for predicting the outcome of patients with severe hemorrhagic stroke.

Trial registration: No.ChiCTR1900022861. Registered April 28, 2016, http:// www.chictr.org.cn

Hemorrhagic stroke

Electrical activity of the diaphragm

Neuro-ventilatory efficiency

Neuro-muscular efficiency

Outcome

Hemorrhagic stroke refers to the primary intracranial hemorrhagic disease caused by multiple etiologies, mainly including cerebral hemorrhage and subarachnoid hemorrhage (SAH), accounting for 15–20% of all strokes, the overall prognosis of hemorrhagic stroke is poor, and the acute mortality rate can reach 30–40% [1]. Patients with cerebral hemorrhage often have hypoxemia due to incomplete obstruction of the respiratory tract, hypoventilation, aspiration, and pulmonary infection [2]. Patients with severe cerebrovascular disease have a high incidence of impaired consciousness, severely impaired brainstem function, decreased airway motor function, and weakened or disappeared protective reflexes. These patients are more likely to have airway obstruction and aspiration symptoms, leading to respiratory failure. Mechanical ventilation is usually used to protect the airways from the risk of inhalation and prevent hypoxemia and hypercapnia [3, 4].

Neurally adjusted ventilatory assist (NAVA) is a new mode of mechanical ventilation that provides ventilation assistance in proportion to EAdi [5–7]. The NAVA is of little value if the patient's central respiratory system is completely disabled. NAVA can monitor and measure EAdi and is a relatively simple, minimally invasive tool for real-time monitoring of patient ventilator interactions [8]. The unique feature of NAVA is that it can recognize the beginning of nerve expiration, whereas auxiliary control ventilation or pressure support ventilation (PSV) cannot. NAVA has more clinical implications, such as better patient ventilator synchronization and more natural breathing patterns, which improve comfort and oxygenation. The EAdi allows quantification of the neural respiratory drive to the electrical activity of the diaphragm during pressure [9]. On the other hand, NAVA can be used as a monitoring tool to observe the functional changes to the respiratory center and its conduction pathway. However, this requires further research on a larger scale. EAdi is the sum of the action potentials of the diaphragmatic muscle fibers, which is related to the overall inspiratory effort of healthy subjects and patients with respiratory failure. When the respiratory central drive increases due to an increase in respiratory load, respiratory muscle weakness, or violent activity, the central nervous system will raise more muscle fibers by increasing the frequency of impulses and the number of nerve fibers transmitting impulses. In contrast, when the respiratory load decreases, the respiratory center has been shown to decrease the frequency of impulses and the number of nerve fibers transmitting impulses, and EAdi decreases. Therefore, it provides a reliable estimate of the central respiratory driving force [10, 11].

The EAdi and EAdi-derived monitoring index can be used as a powerful monitoring tool for any other respiratory mode, providing a large amount of valuable clinical information such as the patient's respiratory drive, ventilation demand, and the impact of ventilator settings on the patient, as well as judging the depth of sedation and the possibility of weaning. Because research on NAVA mode is still in its infancy, future research should investigate the impact of EAdi signal intensity on the prognosis of patients with hemorrhagic stroke. The aim of this study was to analyze whether the EAdi and EAdi-derived monitoring index were related to the prognosis of patients with severe hemorrhagic stroke.

1.1 Selected patients

Patients with hemorrhagic stroke and invasive mechanical ventilation who were admitted to the neurosurgery intensive care unit (NSICU) of Yijishan Hospital of Wannan Medical College from April 2019 to June 2021 were selected. The experimental protocol was approved by the institutional review board of Yijishan Hospital (No.51 of 2019). The trial was registered before patient enrollment at www.chictr.org.cn (primary registries of the WHO Registry Network, Clinical Trial Registration No. ChiCTR1900022861, principal investigator: Tao Yu, date of registration: April 28, 2019). Patients were eligible for inclusion based on the following criteria: (1) patients with hemorrhagic stroke, including those with subarachnoid hemorrhage (SAH) who received surgery and invasive mechanical ventilation; (2) endogenous positive end-expiratory pressure (PEEP) ≥ 3 cmH₂O (1 cmH₂O = 0.098 kPa); (3) informed consent signed by the patient or family members; and (4) administration of only short-acting sedative agents (i.e., propofol and/or sufentanil). Exclusion criteria were: 1) pregnant or lactating women; 2) patients younger than 18 years old; 3) patients receiving mechanical ventilation for less than 72 hours; 4) hospice patients or patients with expected short-term death; 5) esophageal obstruction, esophageal perforation, severe esophageal varices, diaphragmatic hernia, and thoracic deformity; 6) patients with expected short-term death; 7) severe coagulation dysfunction (international normalized ratio > 1.5 and activated partial thromboplastin time > 44 s; 8) patients Severe respiratory central depression, high paraplegia, neuromuscular disease; 9) patients with severe hemodynamic instability (mean arterial pressure ≤ 65mmhg).

1.2 Implantation Of Eadi Catheter And Monitoring Of Eadi Signal

Each patient was consecutively ventilated for 72 hours using a Servo-i ventilator (Getinge Group, Gothenburg, Sweden). A suitable EAdi catheter was selected according to the patient's height and weight. After the catheter was selected, the distance between the nose tip, earlobe, and xiphoid process of the patient was measured, and the approximate depth of EAdi catheter insertion was calculated. The EAdi was obtained using a catheter through a nasogastric tube with electrodes placed at its distal end. The study patients were kept moderately sedated (Propofol 600mg and sufentanil 100ug + 48ml normal saline were pumped intravenously at 2ml / h).

1.3 Data Collection

(1) General information record

Participants: Sex, age, height, weight, blood pressure, location of cerebral hemorrhage, Glasgow Coma Scale (GCS) score, Acute Physiology and Chronic Health Evaluation (APACHE) II score, Sequential Organ Failure Assessment (SOFA) score at ICU admission, past history, complications, ICU stay time, and GOS score of patients 6 months after discharge.

(2) Ventilator-related indices

Mean airway pressure (Pmean), peak airway pressure (Ppeak), positive end-expiratory pressure (PEEP), tidal volume (VT), and minute ventilation (MV). NME was calculated as the ratio of one airway pressure value and one EAdi value during 2 to 3s of end-expiratory occlusion (one inspiratory effort). NVE was measured by monitoring five unassisted breaths, and was calculated as the ratio of VT to EAdi during inspiration. The EAdi, EAdi-derived monitoring index, NVE, and NME were measured in the NAVA real-time PSV ventilation, in which each patient measured five groups of data once, took the average value, and measured for three consecutive days. All patients were under the same degree of analgesia and sedation. (Fig. 1)

1.4 Statistical Methods

SPSS version 21 (SPSS Inc., Chicago, IL, USA) was used for statistical analysis. Normally distributed data are expressed as the mean ± standard deviation or median (interquartile range). If data were normally distributed, they were analyzed using the paired Student’s t-test; otherwise, the Wilcoxon test was used. The difference was considered statistically significant at a P-value < 0.05.

MedCalc (version 20, Ostend, Belgium) software was used to draw the receiver operating characteristic (ROC) curve and Kaplan–Meier curve. The ROC curve was drawn and the area under the ROC curve (AUC) was calculated. Kaplan-Meier survival curves were used to analyze the effects of EAdi, NVE, and NME on the 6-month survival. The Z test was used for comparison, and statistical significance was set at p < 0.05.

1. Baseline Characteristics

A total of 178 patients were screened from April 2019 to June 2021. Finally, 90 patients were included in the study, of whom 33 were in the good outcome group (GOS ≥ 4) and 57 were in the poor outcome group (GOS ≤ 3) (Fig. 2). Patients with poor outcome were older than those with good outcome. The APACHE II and SOFA score of patients with poor prognosis was significantly higher than that of patients with good outcome (Table 1).

Table 1

Patients’ characteristics.
Characteristics	GOS ≥ 4 (n = 33)	GOS ≦ 3(n = 57)	p
Clinical parameters
Age, years (mean ± SD)	53.03 ± 14.29	60.54 ± 12.89	0.012
Sex, male/female, n	17/16	33/24	0.557
GCS score	7(5,10)	6(5,9)	0.691
APACHE Ⅱ	14.33 ± 2.62	16.14 ± 2.68	0.003
SOFA	5.73 ± 1.07	8.05 ± 1.46	0.000
BMI (kg/m²)	25.20 ± 3.21	24.64 ± 2.48	0.356
MAP, mmHg	88.42 ± 9.12	90.93 ± 9.16	0.214
Past history, n (%)
Cardiovascular disease	16	31	0.589
Cerebrovascular diseases	3	7	0.740
Endocrine diseases	3	3	0.662
Kidney diseases	1	4	0.648
Respiratory diseases	1	2	1.000
Comorbidities
pulmonary infection	23	30	0.113
Central system infection	5	19	0.060
Heart failure	1	6	0.255
Ventilatory Parameters
VT(ml)	558.309 ± 137.59	501.48 ± 118.60	0.042
MV(L)	9.43 ± 1.84	9.02 ± 2.06	0.349
Pmean, cmH₂O	7.49 ± 1.11	7.25 ± 1.23	0.348
Peep, cmH₂O	5.28 ± 0.88	5.16 ± 0.95	0.112
Ppeak, cmH₂O	14.53 ± 3.15	13.43 ± 3.11	0.20
FiO₂	0.36 ± 0.41	0.37 ± 0.44	0.439
EAdi(µV)	4.7(3,7.7)	2.80(1.95,4.15)	0.001
NVE(ml/µV)	141.85(90.52,212.06)	66.01(44.49,94.79)	0.000
NME(cm H₂O/µV)	2.57(1.71,4.75)	1.37(1.05,2.02)	0.000
Bleeding site, n
CPH	18	36	0.422
SAH	14	17	0.225
IVH	1	4	0.648
GOS, Glasgow Outcome Scale; GCS, Glasgow Coma Scale; APACHE Ⅱ, Acute Physiology and Chronic Health Evaluation Ⅱ; SOFA, Sequential Organ Failure Assessment; BMI, Body Mass Index; MAP, Mean Arterial Pressure; VT, Tidal Volume; MV, Minute Ventilation; Pmean, Mean Airway Pressure; PEEP, Positive End-Expiratory Pressure (PEEP); Ppeak, peak airway pressure; FiO₂; Fraction of inspiration O₂; EAdi, electrical activity of the diaphragm; NVE, neuro-ventilatory efficiency; NME, neuro-muscular efficiency; CPH, Cerebral parenchymal hemorrhage; SAH, Subarachnoid hemorrhage; IVH, Intraventricular hemorrhage

2. Comparison of ventilator-related index (Table 1)

(1) There was no significant difference between the MV, Pmean, PEEP, Ppeak, and FiO₂ in patients with good and poor outcome.

(2) The VT of patients with poor outcome was lower than that of patients with good outcome.

(3) The EAdi, NVE, and NME in patients with good outcome were significantly higher than those in patients with poor outcome (4.70 µV vs 2.80 µV, P < 0.001; 141.85 ml/µV vs 66.01 ml/µV, P = 0.000; 2.57 cm H₂O/µV vs 1.37 cm H₂O/µV, P = 0.000).

3. EAdi, NVE, and NME predictive value of patients’ survival prognosis (Table 2, Fig. 3)

Table 2

ROC data analysis in this study
	AUC	Cut-off value	Sensitivity	Specificity	Youden index	95% Confidence interval
EAdi(µV)	0.719	3.6	69.70%	68.42%	0.3812	0.614 to 0.808
NVE(ml/µV)	0.793	95.32	75.76%	77.19%	0.5295	0.694 to 0.871
NME(cmH₂O/µV)	0.792	2.06	69.70%	78.95%	0.4864	0.694 to 0.871
ROC, receiver operating characteristic curve; AUC, area under the curve; EAdi: electrical activity of the diaphragm; NVE, neuro-ventilatory efficiency; NME, neuro-muscular efficiency

(1) The AUC for the EAdi score was 0.719; when the EAdi was 3.6 µV, the sensitivity was 69.70%, and the specificity was 68.42%.

(2) The AUC for the NVE score was 0.793; when the NVE value was 95.32 ml/µV, the sensitivity was 75.76%, and the specificity was 77.19%.

(3) The AUC for the NME score was 0.792; when the NVE value was 2.06 H₂O/µV, the sensitivity was 69.70%, and the specificity was 78.15%.

(4) The AUC for the multi-variate (EAdi + NVE + NME) score was 0.911.

4. Comparison of patient survival

The 6-month survival rate of patients with higher EAdi, NVE, and NME was significantly higher than that of patients with lower EAdi, NVE, and NME (Fig. 4).

Critical illness in patients is usually accompanied by direct or indirect respiratory or neuro-transduct damage, which is directly manifested as a lack or loss of the central drive. Studies have shown that many patients with severe disease have diaphragm dysfunction in the early stage of mechanical ventilation, and the long-term mortality and readmission rate of patients with diaphragm dysfunction at discharge are significantly higher than those of patients without diaphragm dysfunction [12, 13].

EAdi is the best indicator of the central driving force [14, 15]. In this study, two patients had no EAdi and could not convert to NAVA, which was caused by inhibition of the respiratory center or damage to the nerve conduction pathway. In addition, the respiratory rate of two patients with brainstem hemorrhage in NAVA mode was accelerated, which was also due to the inhibition of the respiratory center and the decrease in EAdi, resulting in insufficient tidal volume and compensatory respiratory acceleration. This study also found that EAdi in patients with good outcome tended to change at any time and gradually increased to the normal range, which was directly related to the gradual recovery of brain function, especially life center function. The EAdi signal is the intensity of the central nervous system impulse of the phrenic nerve, which plays an important role in the pathogenesis of acute respiratory failure. Research has shown that there is a significant negative correlation between EAdi and the degree of stress support. With an increase in the degree of stress support, EAdi is positively correlated with the degree of stress support. Therefore, the strength of EAdi is an index of respiratory load, and it can be considered as an early warning index for reintubation or noninvasive ventilation [16].

The EAdi signal is a new and unique ventilator monitoring parameter that provides clues for clinical diagnosis. The EAdi signal can be used as a decisive index to guide the ventilator support level [10, 17]. When the patient's condition is improved, the decrease in EAdi signal intensity leads to a decrease in ventilator support level, which is an important indicator when considering weaning and extubation. Mechanical ventilation depends on the interaction of three key factors: central respiratory drive, respiratory muscle strength, and the load exerted on the respiratory muscle [18]. EAdi is the sum of action potentials of diaphragmatic muscle fibers and is therefore the best index to reflect the central drive [19]. EAdi reflects the neural respiratory drive, is the closest indicator that reflects the driving strength of the respiratory center, and is approximately 10 uV when normal healthy people are at rest. The EAdi signal is burdened by inter-individual variability and is also affected by sedatives. In our study, the EAdi in patients with good outcome was significantly higher than that in patients with poor outcome. However, the EAdi signal of most patients with hemorrhagic stroke is lower than that of healthy people, possibly due to damage to the respiratory center or diaphragm function.

ROC curve analysis in this study showed that EAdi had a good predictive value for the outcome of patients with hemorrhagic stroke (AUC = 0.719). When EAdi = 3.60 uV was the best cut-off value, the sensitivity and specificity for predicting the patient outcome level were 69.70% and 68.42%, respectively, which showed that EAdi was a good predictive index. However, there are inter-individual and intra-individual variabilities in EAdi values since it depends on underlying disease conditions, such as the presence of COPD, location (e.g., lobar, deep, or brainstem) and amount of ICH, Hunt and Hess grade for SAH, etc, so comparing EAdi values between individuals may be meaningless. Therefore, we further studied the effect of NVE and NME on the outcome of patients with hemorrhagic stroke, which reflects the ability of the diaphragm to convert the respiratory drive into ventilation.

NVE describes the ability of the respiratory muscles to convert EAdi to tidal volume (VT/EAdi, ml/µV). NVE is used to describe the ability of respiratory muscles to convert EAdi into ventilation volume, assess the proportion of respiratory muscle unloading, and predict the readiness for extubation [20, 21]. Studies have shown that NVE is a potential tool for predicting extubation readiness [22]. The clinical relevance of the NVE index is that an increase in the index over time indicates that a patient can generate more VT for a given respiratory drive. ROC curve analysis of our study showed that NVE had a better predictive value for the outcome of patients with hemorrhagic stroke (AUC = 0.793). When NVE = 95.32 ml/µV was the best cutoff value, the sensitivity and specificity for predicting the patient outcome level were 75.76% and 77.19%, respectively, which proved that NVE was a good predictive index. The low NVE value and patient's heavier condition can indicate that the patient's ventilation load is greater, and higher support may be needed at this time.

NME is defined as delta airway pressure divided by EAdi measured during an end-expiratory occlusion and has been used to estimate inspiratory effort breath by breath [23–25]. This ratio describes how much pressure can be generated for each microvolt of the EAdi signal and the efficiency of the diaphragm in generating pressure for a certain amount of electrical activity. NME outlines the ability to convert EAdi to inspiratory pressure. NME helps to titrate ventilatory support to minimize diaphragm dysfunction resulting from ventilator over-assist and under-assist [26]. In the present study, we found that NME was significantly lower in patients with poor outcome, indicating a weaker diaphragm. When NME = 2.06 cmH₂O/µV was the best cut-off value, the sensitivity and specificity for predicting the patient outcome level were 69.70% and 78.95%, respectively, which proved that NME was a good predictive index (AUC = 0.792).

EAdi is the best indicator of the central driving force, and the diaphragm is the most important respiratory muscle in the human body, and its contraction is completed under the control of the respiratory center. If the patient's central nervous system or respiratory center is damaged, their diaphragm function may be affected, the EAdi is directly related to the respiratory center, so monitoring EAdi, NVE, and NME can evaluate the respiratory drive of the respiratory center to the diaphragm. Phrenic nerve stimulation may achieve lung and diaphragm protection at the same time. Ahn studied unilateral phrenic nerve stimulation during cardiac surgery and found that stimulation every 30 minutes can increase diaphragm contractility by 30% compared with the healthy side [27]. For patients with hemorrhagic stroke, early phrenic nerve stimulation may improve the prognosis of patients. By monitoring patients' EAdi, NVE and NME, we can intuitively evaluate the diaphragm function of patients.

In future studies, it is often necessary to further expand the sample size and adopt a multicenter randomized controlled study to compensate for study deficiencies. In addition, because this was a single-center retrospective study, the sample size was small, dynamics were lacking, and the applicable population was limited, we cannot completely eliminate the interference of other factors, and it is difficult to characterize the target study population because of the broad inclusion criteria (ICH, SAH, and IVH, etc) and not meticulously collecting variables regarding patients’ condition (for example, location (e.g., lobar, deep, or brainstem) and amount of ICH, Hunt and Hess grade for SAH, etc). It should be pointed out that the patients in this study were all severe hemorrhagic stroke and could not represent all patients with hemorrhagic stroke. In the future, we will expand the sample size and adopt a multicenter and prospective research approach to further analyze the relationship between EAdi, NVE, and NME, in postoperative patients with hemorrhagic stroke.

Patients with a good outcome have increased EAdi, reflecting a higher neural respiratory drive, and increased NME and NVE indicating more pronounced respiratory muscle strength. The EAdi curve and EAdi-derived monitoring index have predictive value for patient outcome.

Ethics approval and consent to participate

The experimental protocol was approved by the institutional review board of Yijishan Hospital (No.51 of 2019). The trial was registered before patient enrollment at www.chictr.org.cn (primary registries of the WHO Registry Network, Clinical Trial Registration No. ChiCTR1900022861, principal investigator: Tao Yu, date of registration: April 28, 2019). This study is consistent with the Helsinki Declaration.

Consent to publish

All authors confirms that the work described has not been published before.

Availability of data and materials

Our date will be freely available to any scientist wishing to use them for non-commercial purposes.

Competing interests

All authors declare that there is no conflict of interest. All authors have read and approved the manuscript.

Funding

This work was supported by the Key Research and Development Program of Anhui Province (201904a07020034) and the “Peak” Training Program for Scientific Research of Yijishan Hospital, Wannan Medical College (GF2019G05).

Author Contributions

All authors have read and approved the manuscript

Writing: LY

Data curation: SN, TY

Formal analysis: KW, ZF

Telephone follow-up: NLW, GLW

Review and editing: YT

Acknowledgements

We are thankful to our colleagues in the Department of NSICU at Wannan Medical College First Affiliated Hospital, Yijishan Hospital, for their help in sample collection.

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The predictive value of neurally adjusted ventilatory assist indexes for the outcome of patients with severe hemorrhagic stroke

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Abstract

Figures

Introduction

Methods

1.1 Selected patients

1.2 Implantation Of Eadi Catheter And Monitoring Of Eadi Signal

1.3 Data Collection

1.4 Statistical Methods

Results

Discussion

Conclusion

Declarations

References

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