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Association between estimated pulse wave velocity and the risk of mortality in patients with subarachnoid hemorrhage: a retrospective cohort study based on the MIMIC database

BMC Neurology volume 24, Article number: 408 (2024) Cite this article

Abstract

Background

The estimated pulse wave velocity (ePWV) is a recently developed, simple and useful tool to measure arterial stiffness and to predict long-term cardiovascular mortality. However, the association of ePWV with mortality risk in patients with subarachnoid hemorrhage (SAH) is unclear. Herein, this study aims to assess the potential prediction value of ePWV on short- and long-term mortality of SAH patients.

Methods

Data of adult patients with no traumatic SAH were extracted from the Medical Information Mart for Intensive Care (MIMIC) III and IV database in this retrospective cohort study. Weighted univariate and multivariable Cox regression analyses were used to explore the associations of ePWV levels with 30-day mortality and 1-year mortality in SAH patients. The evaluation indexes were hazard ratios (HRs) and 95% confidence intervals (CIs). In addition, subgroup analyses of age, the sequential organ failure assessment (SOFA) score, surgery, atrial fibrillation (AF), renal failure (RF), hepatic diseases, chronic obstructive pulmonary disease (COPD), sepsis, hypertension, and diabetes mellitus (DM) were also performed.

Results

Among 1,481 eligible patients, 339 died within 30 days and 435 died within 1 year. After adjusting for covariates, ePWV ≥ 12.10 was associated with higher risk of both 30-day mortality (HR = 1.77, 95%CI: 1.17–2.67) and 1-year mortality (HR = 1.97, 95%CI: 1.36–2.85), compared to ePWV < 10.12. The receiver operator characteristic (ROC) curves showed that compared to single SOFA score, ePWV combined with SOFA score had a relative superior predictive performance on both 30-day mortality and 1-year mortality, with the area under the curves (AUCs) of 0.740 vs. 0.664 and 0.754 vs. 0.658. This positive relationship between ePWV and mortality risk was also found in age ≥ 65 years old, SOFA score < 2, non-surgery, non-hepatic diseases, non-COPD, non-hypertension, non-DM, and sepsis subgroups.

Conclusion

Baseline ePWV level may have potential prediction value on short- and long-term mortality in SAH patients. However, the application of ePWV in SAH prognosis needs further clarification.

Peer Review reports

Introduction

Subarachnoid hemorrhage (SAH) is a devastating subtype of stroke as well as an important cause of long-term cognitive dysfunction [1]. SAH can result in disability, with a mortality rate of up to 35% [2]. Exploring simple indexes for early identification of poor prognosis in patients with SAH is of great significance for improving survival and reducing the disease burdens.

Pulse wave velocity (PWV) provides the elastic characteristics of arteries and indicates the degree of arterial stiffness [3]. Multiple studies have showed that a higher PWV was associated with the development of delayed cerebral infarction in patients with SAH [4,5,6]. Also, a higher PWV level increased the risk of short-time poor prognosis and even mortality in patients with cerebral ischemic stroke [7, 8]. The potential mechanisms may be related to the changes of cerebral microcirculation and endothelial function resulted from the increase of pulsation pressure by low vascular resistance [4, 8]. However, no study have discussed the relationship between PWV and the risk of mortality in patients with SAH.

It is worth noting that although PWV is an emerging biomarker in the assessment of vascular health, the inconvenience of testing equipment limits its application. In recent years, the estimated pulse wave velocity (ePWV) method has been developed and used in predicting long-term risk of mortality in patients with stroke [9]. The ePWV is independently associated with all-cause mortality, and may be a useful tool for assessing mortality risk in diabetic populations [10]. ePWV is also recognized as a simple and useful index to measure arterial stiffness and to predict cardiovascular mortality outcome in patients with acute myocardial infarction without the necessity for equipment to measure PWV [11]. Nevertheless, the associations of ePWV levels with mortality risk in patients with SAH are still unclear.

Herein, this study aims to explore the association of ePWV with 30-day mortality and 1-year mortality in SAH patients, and assess the predictive performance of ePWV on the risk of mortality. We hope our findings could provide some reference for further exploration on a convenient tool to early identify SAH patients with poor prognosis, and reduced the mortality risk.

Methods

Study design and participants

Data of participants in this retrospective cohort study were extracted from the Medical Information Mart for Intensive Care (MIMIC) III (2001–2012) and IV database (2008–2019). The MIMIC database is jointly published by the computational physiology laboratory of Massachu-setts Institute of Technology (MIT, Cambridge, MA, USA), the Beth Israel Deaconess Medical Center (BIDMC, Boston, MA, USA), and the Philips Medical. Information on clinical diagnosis and treatment of more than 40,000 real patients, who are predominantly White people, living in the intensive care unit (ICU) of the BIDMC were collected and sorted out by the MIMIC since 2001. More details of this public database were shown elsewhere: https://mimic.mit.edu/.

A total of 1,645 adult patients with no traumatic SAH in the database were initially included. The exclusion criteria were (1) hospitalized in the ICU for less than 24 h, and (2) missing information on the measurement of systolic blood pressure (SBP) or diastolic blood pressure (DBP) measured at the ICU admission. Finally, 1,481 were eligible. The MIMIC database has been approved by the Institutional Review Boards (IRBs) of both the BIDMC and the MIT. Since the database is publicly available, no ethical approval from our institution’s IRB was required.

Measurement and calculation of ePWV

The calculation of ePWV was based on the mean blood pressure (MBP), which is calculated as DBP + 0.4 × SBP - DBP. Then, the following formula was utilized for ePWV calculation: ePWV = 9.587 - (0.402 × age) + (4.5610 × 0.001 × age2) - (2.621 × 0.00001 × age2 × MBP) + (3.176 × 0.001 × age × MBP) - (1.832 × 0.01 × MBP) [9, 12]. In our study, we classified the continuous ePWV value into three levels through X-Tile method, including ePWV < 10.12, 10.12 ≤ ePWV < 12.10, and ePWV ≥ 12.10 [13].

Diagnosis of SAH

The SAH diagnosis was according to the international classification of diseases (ICD) 9th revision (ICD-9) and 10th revision (ICD-10), with the codes of 430 (ICD-9), and I60-I609 (ICD-10) [14]. According to the Modified World Federation of Neurosurgical Societies (WFNS) SAH grading system [15], we categorized SAH into 5 grades: grade I (GCS 15), grade II (GCS 14), grade III (GCS 13), grade IV (GCS 7–12), and grade V (GCS 3–6). In addition, grade I to III and grade IV to V were combined respectively on the basis of distribution of study participants.

Variables selection

We also extracted variables as potential covariates from the database (measured in 24 h after the ICU admission), including age, gender, race, ICU types, heart failure (HF), atrial fibrillation (AF), renal failure (RF), hepatic diseases, chronic obstructive pulmonary disease (COPD), sepsis, hypertension, diabetes mellitus (DM), malignancy, heart rate (HR), respiratory rate (RR), temperature, the sequential organ failure assessment (SOFA) score, white blood cell (WBC), red cell distribution width (RDW), platelet, hematocrit, creatinine (Cr), bicarbonate, sodium (Na), potassium (K), chloride, calcium (Ca), SpO2, urine output, mechanical ventilation use, vasopressors use, renal replacement therapy (RRT), clipping of aneurysm, and endovascular coil occlusion. The diagnoses of these diseases were all according to the ICD codes, including ICD-9 and ICD-10 codes.

Study outcomes and follow-up duration

The study outcomes were 30-day mortality and 1-year mortality. The MIMIC followed up by information in the electronic medical charts and hospital department records, or making contact with the patients, their family members, their attending health care workers, or family physicians on the phone. The follow-up started at the first ICU admission, and ended when patients died or 30 days/1-year after the admission.

Statistical analysis

Normally distributed data were described by mean ± standard deviation (mean ± SD), and analysis of variance (ANOVA) was used for comparation among three ePWV level groups. Non-normally distributed data were described by median and quartiles [M (Q1, Q3)], and rank sum test was used for comparation. Frequency and composition ratio [N (%)] was used to describe the categorical data, and chi-square test (χ2) was used for comparation.

Weighted univariable Cox regression analysis was used to screen the covariates associated with the 30-day mortality and 1-year mortality respectively. Weighted univariable and multivariable Cox regression analyses were established to explore the associations of ePWV levels with 30-day mortality and 1-year mortality in patients with SAH. Model 1 was unadjusted model. Model 2 for 30-day mortality adjusted for age, ICU types, HF, AF, RF, hepatic diseases, sepsis, DM, malignancy, HR, RR, temperature, SOFA, WBC, Cr, Ca, mechanical ventilation use, vasopressor use, and RRT. Model 2 for 1-year mortality adjusted for age, ICU types, HF, AF, RF, hepatic diseases, COPD, sepsis, hypertension, DM, malignancy, HR, RR, temperature, SOFA, WBC, Cr, Ca, mechanical ventilation use, vasopressor use, and RRT. Kaplan-Meier (KM) curves were drawn to reflect the survival probability of 30-day and 1-year in SAH patients with different ePWV levels. To assess the predictive performance of ePWV on 30-day mortality and 1-year mortality in SAH patients, we compared the receiver operator characteristic (ROC) curve with area under the curve (AUC) between single SOFA score and SOFA score combined ePWV. In addition, these associations were assessed in subgroups of age, SOFA, surgery, AF, RF, hepatic diseases, COPD, sepsis, hypertension, and DM.

The evaluation index was hazard ratios (HRs) and 95% confidence intervals (CIs). Two-sided P < 0.05 is considered as a significant association. We used the Structured Query Language (SQL) and PostgreSQL software (version 9.6.22) to extract data from the MIMIC. Statistical analyses were conducted by Python 3.9.12 (Python Software Foundation, Delaware, USA) and SAS 9.4 (SAS Institute., Cary, NC, USA). Variables including missing values were deleted if the missing proportion over 10%, otherwise were interpolated by multiple interpolation. Sensitivity analysis of the participants’ characteristics before and after interpolation of missing data was shown in the Table S1.

Results

Characteristics of participants

Figure 1 showed the flowchart of study process. There were 1,645 adult patients with no traumatic SAH in the MIMIC database. We excluded those who without information on SBP or DBP measured at the ICU admission (n = 16) or stayed in the ICU for less than 24 h (n = 148). Finally, 1,481 of them were eligible.

Fig. 1
figure 1

Flowchart of patients screening

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Participants’ characteristics were showed in the Table 1. A total of 339 (22.89%) patients died within 30 days, and that 435 (29.37%) died within 1 year. The average age of total population was 60.16 years old, and more than a half of them were female (55.64%). Among the three ePWV level groups, age, ICU types, HF, AF, hepatic diseases, COPD, hypertension, DM, malignancy, SBP, DBP, temperature, SOFA, hematocrit, Cr, urine output, and RRT were significantly different (all P < 0.05).

Table 1 Characteristics of patients with SAH
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Association between ePWV and mortality in SAH

We firstly screened the covariates associated with 30-day mortality and 1-year mortality respectively (Table S2). Then, we explored the associations between ePWV and 30-day/1-year mortality in patients with SAH (Table 2). After adjusting for all covariates, ePWV level ≥ 12.10 was associated with higher risk of both 30-day mortality (HR = 1.77, 95%CI: 1.17–2.67) and 1-year mortality (HR = 1.97, 95%CI: 1.36–2.85) compared with ePWV level < 10.12. Similarly, these positive associations was also found in SAH patients with grade I-III (30-day mortality: HR = 2.04, 95%CI: 1.11–3.75; 1-year mortality: HR = 2.13, 95%CI: 1.24–3.67) (Table 3).

Table 2 Association between ePWV and mortality risk in SAH
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Table 3 Association between ePWV and mortality risk in patients with different SAH grades
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Figure 2 was the KM curves of the survival probability of 30-day and 1-year respectively in SAH patients with different ePWV levels. It was easy to observed that patients in the highest ePWV level group had the lowest survival probability whatever within 30 days (Fig. 2A) or 1 year (Fig. 2B), indicating that the risk of short- and long- term mortality in patients with SAH seemed to increase along with the elevated ePWV levels. Moreover, we considered a cluster analysis through partitioning around medoids (PAM). The silhouette coefficient is used to determine the final category (final K = 2). The associations between ePWV and outcomes were re-examined in each category (Table S3), and the distribution of variables in each category after clustering has been shown in the Table S4. The results similarly suggested positive associations between ePWV level and mortality risk.

Fig. 2
figure 2

KM curves of survival probability of 30-day and (A) 1-year (B) in SAH patients with different ePWV levels

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In addition, we assessed the predictive performance of ePWV on 30-day mortality and 1-year mortality in SAH patients (Fig. 3). The ROC curves showed that SOFA score combined with ePWV had a relatively superior predictive performance to single SOFA score on 30-day mortality (AUC: 0.740 vs. 0.664) and 1-year mortality (AUC: 0.754 vs. 0.658).

Fig. 3
figure 3

The predictive performance of ePWV on 30-day (A) and 1-year (B) mortality in patients with SAH

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Relationships between ePWV levels and SAH mortality in different subgroups

Associations of ePWV levels with 30-day mortality (Table 4) and 1-year mortality (Table 5) were further explored in SAH patients with different age and healthy conditions. After adjusting covariates, ePWV ≥ 12.10 was associated with higher risk of 30-day mortality in age ≥ 65 years old, SOFA score < 2, non-surgery, non-RF, non-hepatic diseases, non-COPD, sepsis, non-hypertension, and non-DM subgroups (all P < 0.05).

Table 4 Relationship between ePWV and 30-day mortality in different subgroups
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Table 5 Relationship between ePWV and 1-year mortality in different subgroups
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Besides, the positive association between ePWV and 1-year mortality was found in subgroups of age < 65 years old, age ≥ 65 years old, SOFA score < 2, non-surgery, non-AF, non-hepatic diseases, hepatic diseases, non-COPD, sepsis, non-hypertension, and non-DM (all P < 0.05). Attention should be focused on SAH patients who at an older age, with lower SOFA scores, did not received surgery, without hepatic diseases, COPD, hypertension or DM, and with sepsis. But specially, the relationship between ePWV and short-term/long-term mortality of SAH was not similar when patients aged < 65 years old, non-RF, and had sepsis.

Discussion

The present study explored associations of ePWV levels with 30-day mortality and 1-year mortality in patients with SAH. The study results showed that ePWV ≥ 12.10 was associated with both higher risk of 30-day mortality and 1-year mortality. Also, the ePWV level has a potential to improve predictive performance of SOFA score on mortality risk in SAH patients. In addition, these positive relationships were also significant in age ≥ 65 years old, SOFA score < 2, non-surgery, non-hepatic diseases, non-COPD, sepsis, non-hypertension, and non-DM subgroups.

In recent years, the ePWV calculated from age and MBP using an equation generated from the reference values for arterial stiffness collaboration had similar predictive value as carotid-femoral-PWV for a combined cardiovascular end point in healthy individuals [16, 17]. To the best of our knowledge, no study has discussed the role of ePWV level in prognosis prediction in patients with SAH. In fact, the predictive value of ePWV in all-cause and cardiovascular mortality in other populations has been reported in previous researches. In a prospective cohort, Vishram-Nielsen et al. [18] showed that elevated ePWV was associated with subsequent mortality and cardiovascular morbidity in the apparently healthy persons independently of systematic coronary risk evaluation and Framingham Risk Score, but not independently of traditional cardiovascular risk factors. Wu et al. [19] indicated that ePWV had positive linear associations with both all-cause mortality and cardiovascular mortality in patients with DM during an average 10 years follow-up duration. Similarly, we conducted a retrospective cohort study based on the MIMIC database, which includes large sample of real cases in the United States, and found that higher ePWV level was associated with increased risk of both 30-day mortality and 1-year mortality. The study results indicated that clinicians need to focus on ePWV level at the ICU admission in patients with SAH and timely take measures to control it at appropriate levels that may help reduce both short- and long-term mortality risk, and these findings relatively supplemented the literature blank in relevant field.

Several mechanisms may be involved in the relationship of arterial stiffness with mortality in patients with SAH, and however, no studies have concluded a certain one. The speculation of possible underlying mechanisms could reference from previous researches. The arterial stiffness is not only influenced by blood pressure, related to oxidative stress and inflammation, and it plays a significant role in the pathophysiology of diseases with high-risk of mortality, such as inflammatory diseases as well as cancers [17, 20, 21]. Also, arterial function and mortality have genetic predispositions because there are strongly associations between vascular biomarkers and genetic indicators of biological aging and life expectancy [22, 23]. Increased arterial stiffness can result in high pulse pressure and hypertension, reduce coronary perfusion pressure, increase the afterload of left ventricle, and further promote remodeling and dysfunction [24]. The increased pulse pressures may enhance the penetration of pulsatile flow to microvasculature in organs, such as kidney, heart, and brain [25]. Besides, pulsatile pressure, hemodynamic stress, and blood pressure variability damage brain and heart [26]. In the present study, both the average SBP and DBP among three ePWV level groups were significantly different, where patients in the highest ePWV level group had the highest blood pressure, followed by those in the middle ePWV level group. Moreover, after adjusting for the potential influencing factors of mortality, ePWV was significantly associated with 30-day mortality and 1-year mortality in SAH patients. Arterial stiffness is an important contributor to hypertension, and hypertension can in turn promote arterial stiffness, resulting in a vicious cycle. Although the association between ePWV and mortality risk in SAH population suggests possible links to cerebral microcirculation and endothelial function, further research is needed to elucidate these pathways.

We further explored the association between ePWV and mortality risk in SAH patients with different age, SOFA score, surgery, AF, RF, hepatic diseases, COPD, sepsis, hypertension, and DM conditions. Among patients aged ≥ 65 years old, higher ePWV level was significantly associated with higher risk of both 30-day mortality and 1-year mortality. In Laugesen’s study, in contrast to continuous ePWV, the association between dichotomized ePWV and mortality in patients with stable angina pectoris became nonsignificant with adjustment for age and SBP [27]. Laugesen considered that increases in ePWV were associated with increased risk across both low and high levels of ePWV, and that dichotomizing the nonlinear age and blood pressure effects captured by the ePWV is too crude a measure to capture the added prognostic information beyond the linear effects of age and SBP [27]. When SAH patients with SOFA score < 2 had higher ePWV level, they seemed to have higher risk of mortality. SOFA is associated with severity of SAH, and the score < 2 represents a mild condition of the patient. The ePWV level could be applicated in predicting mortality in SAH patients with mild conditions because those who had severe SAH may access to earlier and more targeted treatment to reduce mortality. Similarly, we also categorized patients into different grade of SAH according to the WFNS SAH grading system, and found among those with grade I-III, the positive association between ePWV level and mortality risk was significant. Besides, the predictive performance of single SOFA score and ePWV combined with SOFA score were compared on mortality risk in SAH patients, indicating that ePWV may have a potential to improve the prediction value of SOFA. In addition, this positive relationship was also found in non-surgery, non-hepatic diseases, non-hypertension, and non-DM subgroups. The SAH population may be complicated by hypertension as arterial stiffness increases and that most of the population has been already on antihypertensive therapy at this time. Due to ePWV is calculated using age and blood pressure, it may be affected by antihypertensive therapy in predicting the risk of mortality. Clinical studies have showed that patients with DM are more likely to develop arterial stiffness and had a higher cf-PWV than those who without DM [28,29,30]. DM can lead to elevated blood pressure and arterial stiffness through activating MMP2, MMP9, TGFβ1/Smad2/3, and Runx2 pathways, and aggravating aortic fibrosis though promoting oxidative stress [31, 32]. Although controlling arterial stiffness is very important especially for patients with DM, our results indicated that monitoring the ePWV level in patients without DM is also necessary. In a retrospective cohort study conducted by Zhang et al. [33], they found that chronic liver disease (CLD) was associated with an increased risk of mortality in patients with aneurysmal SAH, and Among the patients with CLD, an increased severity of CLD was associated with a significant increase in the risk of mortality. However, we did not obvious the relationship between ePWV and 30-day mortality risk in SAH patients who had hepatic diseases, which may possibly due to the influencing of complex factors associated with liver disease, such as virus infection and liver cirrhosis [33]. Additionally, the roles of ePWV levels in short- and long-term mortality may be different in patients with different disease conditions, but the specific mechanisms needed further clarification.

The current research was the first to explore the associations of ePWV levels with 30-day mortality and 1-year mortality in patients with SAH, which indicated there may be a potential prediction value of ePWV in short- and long-term SAH prognosis. Also, since both the SBP and DBP are simple and easy to measure, ePWV had the potential to be used as a convenient tool to identify SAH patients at high-risk of poor prognosis in clinical practice. However, there are still some limitations. This was a retrospective cohort study, so that it was difficult to avoid the effects of recalling bias and information bias. Although we have adjusted for several covariates, there might still be unmeasured confounders that could affect the association between ePWV and mortality, such as lifestyle factors, genetic predispositions, or unrecorded comorbidities. While the calculation formula of ePWV has been validated, it is an estimated measure rather than directly measured PWV, which may introduce errors or variability compared to direct measurements, potentially impacting the conclusions. Additionally, data extracted from the MIMIC database predominantly includes a population of White patients from a single geographical region, which limited the generalizability of the findings to other populations and healthcare settings. Therefore, these associations in different populations need to be further validated.

Conclusion

The ePWV level at ICU admission may be a potential predictor for mortality in patients with SAH. This study may provide some references for further exploration on an easy and convenient tool for early identification of SAH patients with poor prognosis.

Data availability

No datasets were generated or analysed during the current study.

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Authors and Affiliations

  1. Second Affiliated Hospital of Soochow University, Suzhou, 215000, Jiangsu Province, People’s Republic of China

    Min Chen & Yingzhu Chen

  2. Yancheng Third People’s Hospital, Yancheng, 224000, Jiangsu Province, People’s Republic of China

    Min Chen, Lili Xie & Li Zhou

  3. Northern Jiangsu People’s Hospital, Yangzhou, 225009, Jiangsu Province, People’s Republic of China

    Yingzhu Chen

  4. Yangzhou University, 225009, Yangzhou, Jiangsu Province, People’s Republic of China

    Hongyang Fan

Authors
  1. Min Chen
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  2. Hongyang Fan
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  3. Lili Xie
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  4. Li Zhou
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  5. Yingzhu Chen
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Contributions

Min Chen. wrote the main manuscript text and Min Chen&Hongyang Fan. prepared Figs. 1, 2 and 3 and Lili Xie&Li Zhou. prepared tables.Yingzhu Chen and all authors reviewed the manuscript.

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Correspondence to Yingzhu Chen.

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Chen, M., Fan, H., Xie, L. et al. Association between estimated pulse wave velocity and the risk of mortality in patients with subarachnoid hemorrhage: a retrospective cohort study based on the MIMIC database. BMC Neurol 24, 408 (2024). https://doiorg.publicaciones.saludcastillayleon.es/10.1186/s12883-024-03897-5

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  • DOI: https://doiorg.publicaciones.saludcastillayleon.es/10.1186/s12883-024-03897-5

Keywords

BMC Neurology

ISSN: 1471-2377

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