The value of the proportion of perfused vessels change rate in the evaluation of early organ function deterioration in septic shock and ARDS

doi:10.21203/rs.3.rs-4654231/v1

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The value of the proportion of perfused vessels change rate in the evaluation of early organ function deterioration in septic shock and ARDS

https://doi.org/10.21203/rs.3.rs-4654231/v1

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This study explores the relationship between the proportion of perfused vessels change rate (ΔPPV), the shedding of the glycocalyx marker syndecan-1 (SDC-1), and the utility of ΔPPV in assessing early organ function deterioration in septic shock and acute respiratory distress syndrome (ARDS) patients.Patients were categorized into two groups based on the change in their Sequential Organ Failure Assessment (SOFA) score over 24 hours: the organ function deterioration group (SOFA_24h-0h score ≥ 1) and the non-deterioration group (SOFA_24h-0h score < 1). Sublingual microcirculation, lactic acid levels, and SDC-1 were evaluated at 0 and 6 hours. The primary endpoint was the area under the curve (AUC) for ΔPPV and its combination with lactate clearance rate (LCR). Secondary endpoints included the correlation between ΔPPV and SDC-1, hospital mortality, and survival analysis.The study included 67 patients. The AUC for ΔPPV was 0.813 (95% CI: 0.707-0.919), and when combined with LCR, it was 0.871 (95% CI: 0.785- 0.957). Additionally, a negative correlation between ΔPPV and SDC-1 was observed. Patients who met the criteria of ΔPPV≥7.6% and LCR≥14.6% demonstrated a higher survival rate compared to other groups (Log-rank test: χ²=6.489, P<0.011).Microcirculatory disorders are closely linked to glycocalyx shedding. ΔPPV, particularly when combined with LCR, can effectively predict early organ function deterioration and has significant prognostic value for hospital mortality.

Health sciences/Medical research

Health sciences/Medical research/Outcomes research

Septic shock

Acute respiratory distress syndrome

Microcirculation

Deterioration of organ function

Lactic acid clearance

Sepsis, a critical health condition, arises from a dysregulated host response to infection, leading to life-threatening organ dysfunction. Characterized by an imbalance in oxygen supply and demand, septic shock is a type of distributive shock that concurrently affects both macrocirculation and microcirculation^[¹^]. Following a severe infection, the body experiences acute circulatory disturbances that reduce effective circulating blood volume, leading to tissue hypoperfusion, cellular ischemia, and hypoxia. These conditions promote a systemic inflammatory response that compromises microcirculation and ultimately results in organ failure^[²^]. The lungs, often the initial target in the cascade of multiple organ dysfunction syndrome (MODS) triggered by sepsis, are particularly susceptible to acute respiratory distress syndrome (ARDS)^[³^]，making septic shock and ARDS significant contributors to mortality in critically ill patients.

The vascular endothelium's glycocalyx, which plays a crucial role in maintaining vascular homeostasis, can be severely damaged during sepsis, increasing vascular permeability and leading to tissue edema. This damage to the glycocalyx is a key pathological mechanism in sepsis-related ARDS^[⁴^,⁵^]. Studies indicate that the level of syndecan-1 (SDC-1), a component of the serum glycocalyx, correlates with the severity of sepsis^[⁶^]. Additionally, the severity of microcirculatory disorders and the extent of glycocalyx shedding are associated with increased risk of organ failure and poor prognosis^[⁷^].

Interestingly, few studies have explored the direct relationship between glycocalyx damage and microcirculatory disorders. Trzeciak et al.^[⁸^] found that improvements in sublingual microcirculation were associated with enhanced organ function during the early stages of septic shock resuscitation. Prompt improvement in microcirculation within the first 6 hours can significantly reduce the likelihood of early organ failure and mortality^[⁹^]. Clinical observations have shown that while some sepsis patients achieve macrocirculatory stability with treatment, their tissue hypoperfusion and cellular hypoxia often persist, leading to continued organ dysfunction and adverse outcomes. This suggests that reliance solely on macrocirculatory indices may result in suboptimal treatment, highlighting the necessity for integrated microcirculatory assessments.De Bacher et al^[¹⁰^] demonstrated that the degree of microcirculatory dysfunction independently predicts survival, with the proportion of perfused vessels (PPV) serving as a mortality indicator.

Recent studies emphasize the dynamic changes in microvasculature following treatment, which are influenced by individual differences and potential confounding factors, making a single measurement of PPV less reliable. The rate of change in PPV (ΔPPV) provides insights into changes in vascular opening and flow heterogeneity over time and is closely associated with poor prognosis in patients with septic shock^[¹¹^]. However, clinical studies focusing on ΔPPV in the early deterioration of organ function in septic shock combined with ARDS are scarce. Microcirculatory disturbances in septic shock lead to dysregulation of cellular activity and suppression of aerobic glycolysis, resulting in lactic acid accumulation. Normalization of blood lactate levels is a critical goal in the resuscitation of septic shock patients, thus lactate clearance rate (LCR) is a valuable metric for evaluating the effectiveness of treatment^[¹²^], although it is subject to various influencing factors. Moreover, sublingual microcirculation monitoring may introduce data biases during image acquisition and processing.

In this study, we observed the proportion of perfused vessels change rate (ΔPPV) and LCR, analyzing their predictive value for early deterioration of organ function and 28-day survival outcomes in patients with septic shock and ARDS. Additionally, we examined the correlation between ΔPPV and the glycocalyx damage marker SDC-1, aiming to provide clinical insights for managing sepsis-induced organ failure.

Patient selection

A prospective study was conducted on patients diagnosed with septic shock and ARDS who were admitted to the intensive care unit (RICU) of Zhengzhou Central Hospital, affiliated with Zhengzhou University, from October 1, 2021, to May 31, 2023. Inclusion criteria included patients who met the diagnostic standards of Sepsis-3^[¹³^] and the ARDS Berlin Criteria^[¹⁴^]. Exclusion criteria were age under 18 years, pregnancy, presence of malignant neoplasms, use of immunosuppressive drugs, oral diseases or heavy bleeding that could affect sample quality, inability to perform invasive mechanical ventilation, and a hospital stay of less than 24 hours or death shortly after unsuccessful resuscitation. This study was performed in accordance with the guidelines of the Declaration of Helsinki and was approved from the Ethics Committee of Zhengzhou Central Hospital affiliated with Zhengzhou University (approval no. 202408), and informed consent was obtained from all patients or their legal representatives.

Clinical date collection

Data collected at admission and six hours later included the proportion of perfused vessels (PPV), syndecan-1 (SDC-1), lactate (Lac), oxygen to inspired oxygen fraction (PaO₂/FiO₂), central venous pressure (CVP), and mean arterial pressure (MAP). Serum creatinine (SCr), total bilirubin (Tbil), C-reactive protein (CRP), procalcitonin (PCT), and platelet count (PLT) were measured at admission. The change in perfused vessel proportion (ΔPPV) was calculated as ΔPPV = [(PPV_T - PPV_T0) / PPV_T0] × 100%; lactate clearance rate (LCR) was calculated as LCR = [(Lac_T0 - Lac_T) / Lac_T0] × 100%. Acute Physiology and Chronic Health Evaluation II (APACHE II) and Sequential Organ Failure Assessment (SOFA) scores were recorded at admission and 24 hours later. Patients were categorized based on the change in SOFA score over 24 hours (SOFA_24h-0h score), with groups defined as having organ function deterioration (SOFA_24h-0hscore ≥ 1) or non-deterioration (SOFA_24h-0h score < 1). Survival was defined as discharge from the RICU without the need for readmission.

Methods for measuring sublingual microcirculation

Sublingual microcirculation was assessed using the MicroSeeV100 handheld video microscope (Guangzhou Yiruan Intelligent Technology Co., Ltd., Guangzhou, China; Software version 2.84). A trained operator gently cleaned oral secretions, particularly under the tongue, with a normal saline swab maintained at 37°C. The microscopic video probe, after removing secretions with gauze, was utilized to avoid pressure effects on microcirculation, adjusting the focal length to acquire stable and clear video images. Five video images from different parts of the tongue-abdominal frenulum were captured, each lasting at least five seconds^[¹⁵^]. Small blood vessels were automatically traced by the software and manually adjusted as needed. The PPV percentage represents the ratio of perfused small vessel length to total small vessel length, serving as an indicator of microcirculatory perfusion quality.

Measurement of hemodynamic indicators

Intracervical or subclavian venous catheters (7FR, Weihai Jiwei Intensive Care Medical Products Co., Ltd., China) were placed in all patients, and hemodynamic measurements were performed using IntelliVue MP60 monitors (Philips, Germany). Monitored parameters included heart rate (HR), central venous pressure (CVP), and mean arterial pressure (MAP).

SCD-1 detection method

Three milliliters of arterial blood were collected at 0 and 6 hours post-admission, allowed to clot naturally, and centrifuged at 3000 rpm for 10 minutes. The serum was then stored at -80 °C until analysis. The concentration of SDC-1 was determined using an enzyme-linked immunosorbent assay (ELISA) kit (Wuhan Cloud Clone, SEB966Hu, China).

Statistical analysis

Data were analyzed using SPSS 26.0 (IBM, Armonk, NY, USA). Continuous variables following a normal distribution were expressed as mean ± standard deviation, and comparisons between groups were made using the t-test. Variables not normally distributed were described using the median and interquartile range (IQR), with the Mann-Whitney u-test applied for intergroup comparisons. Categorical variables were summarized as counts and percentages, and analyzed using the Chi-square or Fisher's exact test as appropriate. Correlations were assessed using the Spearman rho statistic. The receiver operating characteristic (ROC) curve analysis was used to evaluate the discriminative ability of the clinical predictors. The optimal cutoff values were used to categorize influencing factors. In-hospital mortality rates were calculated, and survival curves were plotted using the Kaplan-Meier method, with the Log-rank test assessing differences among predefined groups. A P-value <0.05 was considered statistically significant.

General characteristics

Initially, we screened 106 patients diagnosed with septic shock and ARDS. Of these, seven patients either died or were discharged within 24 hours of admission to the RICU. Additionally, exclusions included nine patients with malignant neoplasms, six receiving immunosuppressive drugs, four affected by oral diseases or heavy bleeding, and thirteen unable to undergo invasive mechanical ventilation (see Fig.1). Ultimately, 67 patients were included in the study—43 males and 24 females—with an average age of 74.12 ± 14.01 years. Based on the 24-hour change in SOFA scores, patients were classified into two groups: the deterioration group (n=34) and the non-deterioration group (n=33). No significant statistical differences were observed in the baseline characteristics between these groups (P > 0.05) (see Table 1).

Table 1. Patient characteristics of the study population.Data are presented as means (standard deviation; ± SD), median (interquartile range; IQR), or counts (percentage). Differences were tested using the Kruskal-Wallis test or Fisher exact test unless indicated otherwise.APACHE-Ⅱ: Acute Physiology And Chronic Health Evaluation II, SCr, serum creatinine; Tbil, total bilirubin; CRP, c-reactive protein; PCT, procalcitonin; PLT, blood platelet; RICU, ICU, respiratory intensive care unit. *P＜0.05.

Characteristics	Deterioration	Non-deterioration	χ²/t/Z	P
Characteristics	(n=34)	(n=33)	χ²/t/Z	P
Age (years)	71.94±15.58	76.36±12.02	1.298	0.199
Males	22(64.7)	21(63.6)	0.008	0.927
Temperature (℃)	37.40±1.06	37.60±0.99	0.786	0.435
Respiratory rate (breaths/min)	21.86±4.59	21.00±3.35	0.871	0.387
Comorbidities
Hypertension	11(32.4)	15(45.5)	1.210	0.271
Diabetes	10(29.4)	9(27.3)	0.038	0.846
Cardiovascular	16(47.1)	15(45.5)	0.017	0.895
Respiratory	14(41.2)	10(30.3)	0.861	0.353
Site of infection			1.410	0.914
Respiratory tract	11(32.4)	14(42.4)
Intra-abdominal	5(14.7)	4(12.1)
Urinary tract	5(14.7)	4(12.1)
Skin/soft tissue	9(26.5)	6(18.2)
Others	4(11.8)	5(15.2)
APACHE Ⅱ score	24.23±5.86	22.82±5.24	1.042	0.301
SCr (μ mol/L)	127.50±84.25	104.97±71.24	1.180	0.242
Tbil (μ mol/L)	23.65(17.68，43.13)	19.60(9.70，27.10)	-2.596	0.009^*
CRP (mg/L)	119.45±82.40	94.63±72.82	1.305	0.196
PCT (ng/L)	28.17±42.50	8.19±13.36	2.611	0.013^*
PLT (×10⁹ /L)	113.41±80.10	133.24±81.55	1.004	0.319
RICU deaths	15(44.1)	6(18.2)	5.235	0.022^*

Two groups of hemodynamic and microcirculatory perfusion indicators

At the outset and six hours post-admission, there were no significant differences in heart rate (HR), central venous pressure (CVP), mean arterial pressure (MAP), or PaO₂/FiO₂ ratios between the two groups (P>0.05). Similarly, no significant differences were noted in initial SDC-1 and PPV values. However, after six hours of treatment, SDC-1 levels in the deterioration group were significantly higher, and PPV significantly lower, compared to the non-deterioration group (P<0.05) (see Table 2). Additionally, both ΔPPV and LCR were lower in the deterioration group compared to the non-deterioration group (P<0.05) (see Fig.1).

Table 2. Comparison of patient indicators between the two groups. HR, heart rate; CVP, central venous pressure; MAP, mean arterial pressure; PaO₂/FiO₂-ratio, pressure of oxygen/fraction of inspired oxygen-ratio PPV, the proportion of perfused vessels. *P＜0.05.

Characteristics		Deterioration	Non-deterioration	t	P
		(n=34)	(n=33)	t	P
HR (min-1)	0 h	100.59±8.00	97.24±7.75	0.805	0.087
	6 h	97.50±12.98	93.88±6.13	1.467	1.149
CVP (cmH₂O)	0 h	9.32±2.77	9．12±1.43	0.195	0.710
	6 h	9.38±2.28	9.27±1.35	0.240	0.811
MAP (mmHg)	0 h	73.36±13.97	73.44±11.79	0.023	0.981
	6 h	79.61±14.98	81.09±10.58	0.468	0.641
SDC-1(ng/mL)	0 h	54.60±15.08	52.72±16.93	0.482	0.631
	6 h	65.32(57.71,69.89)	51.89(46.31,64.53)	-3.411	0.001
PaO₂/FiO₂	0 h	186.32±70.08	187.24±62.16	0.057	0.955
	6 h	218.78±89.58	231.86±65.62	0.683	0.499
Lac (mmol/L)	0 h	7.3(5.28,9.65)	5.1(3.90,6.75)	-2.735	0.006*
	6 h	6.25(4.52,8.75)	4.00(3.15,5.45)	-3.375	0.001*
PPV %	0 h	70.61±11.94	72.28±12.25	0.404	0.574
	6 h	74.54±11.58	81.18±12.54	0.297	0.028*
LCR	-	13.41(4.06,20.71)	17.65(9.71，29.75)	-2.602	0.009*
ΔPPV	-	6.41(3.08,8.78)	11.66(8.75,14.07)	-4.402	＜0.001*

Correlation between PPV and serum SDC-1 levels

Spearman correlation analysis demonstrated a negative correlation between ΔPPV and SDC-1 (r_s = -0.310, p = 0.011) (see Fig. 2).

Multivariate regression analysis on early organ function deterioration

Multivariate logistic regression analysis revealed that factors including ΔPPV and LCR were independently associated with the onset of early organ function deterioration (see Table 3).

Table 3. Multivariate logistic regression analysis of factors influencing early organ deterioration SE, Standard error; CI, Confidence interval; OR, Odds ratio.

Variable	B	SE	Wals	P	OR	95%CI
Tbil	0.024	0.014	2.699	0.100	1.024	0.995~1.053
PCT	0.038	0.022	2.923	0.087	1.038	0.995~1.084
ΔPPV	-0.201	0.068	8.747	0.003	0.818	0.716~0.935
LCR	-0.077	0.031	6.223	0.013	0.926	0.871~0.984

Predictive test and subgroup survival analysis of early organ function deterioration

ROC analysis indicated that ΔPPV possesses predictive value for early organ function deterioration in patients with septic shock and ARDS. The combined area under the curve (AUC) for ΔPPV and LCR was 0.871, with a sensitivity of 61.80% and a specificity of 97.00% (see Fig. 3,Table 4).

Table 4. Predictive value of single and combined indicators in the early organ function deterioration ROC, Receiver operating characteristic; AUC, Area under the curve.

Variable	AUC（95%CI）	Sensitivity（%）	Specificity（%）	Cutoff	P
ΔPPV	0.813(0.707,0.919)	90.90	64.70	7.642	<0.0001
LCR	0.685(0.559,0.811)	69.70	38.20	14.557	0.009
ΔPPV+ LCR	0.884(0.803,0.965)	61.80	97.00	-	<0.0001

Based on the established cutoff values for ΔPPV and LCR, patients were categorized into four groups: (1) ΔPPV ≥ 7.6% and LCR ≥ 14.6%, (2) ΔPPV ≥ 7.6% and LCR < 14.6%, (3) ΔPPV < 7.6% and LCR ≥ 14.6%, and (4) ΔPPV < 7.6% and LCR < 14.6%. The cumulative survival rate of patients in the first group was significantly higher than that of the other three groups (Log-rank test: χ² = 38.39, P < 0.001) (see Fig. 4).

Organ failure is a critical event in the pathogenesis of sepsis, marking a hallmark of the disease and a pivotal determinant of prognosis. The damage induced by sepsis stems from the persistence of a mismatch between perfusion and tissue metabolic demands^[¹⁶^]. Inflammatory responses leading to cardiac dysfunction and systemic volume redistribution are central to this mismatch, but the situation is exacerbated by impaired tissue oxygen utilization^[¹⁷^]. Early indicators of organ function deterioration are vital for prognosis, as they represent the most significant changes in the disease's course. Thus, the prompt, accurate assessment of macrocirculation-microcirculation coupling, and clarification of patient conditions are essential for developing personalized blood flow management strategies to reduce organ failure rates and improve outcomes^[¹⁸^].

Recent advances in visual imaging technology have enabled the direct observation of capillary changes at the bedside. Studies confirm that alterations in sublingual microcirculation mirror changes in other vital organs, such as the intestines and kidneys^[¹⁹^,²⁰^]. Therefore, microcirculation imaging systems used to analyze sublingual microcirculation parameters effectively evaluate the early and ongoing deterioration of critically ill patients and guide precise, individualized treatment strategies. Research by Sakr et al.^[²¹^] found that microcirculatory perfusion, continuously impaired in non-survivors of multiple organ failure, improved rapidly in survivors. Our study corroborates these findings, showing uncoupling of microcirculation from macrocirculation after early resuscitation, with sustained hypoperfusion despite normal macrocirculation indices. Patients whose organ function did not deteriorate exhibited significantly higher ΔPPV and PPV during early resuscitation, suggesting that disturbances in microcirculation induced by sepsis are a likely mechanism behind multiorgan dysfunction. Even when initial microcirculatory abnormalities are corrected, improved responses can gradually reduce the likelihood of organ function deterioration^[²²^].Stephen et al.^[²³^] also demonstrated experimentally that microcirculatory disturbances occur independently of macrocirculatory changes, with early fluid resuscitation enhancing microcirculatory flow and reducing organ failure within 24 hours.

Abnormal microcirculatory perfusion often coincides with impaired cellular metabolic energy. Although cell metabolism indices reflect tissue cellular metabolism, they also indirectly indicate microcirculatory function. Occasionally, despite optimal resuscitation and life support, elevated lactate levels persist, possibly due to mitochondrial dysfunction triggered by sepsis^[²⁴^]. Effective lactate clearance requires not only sufficient macrocirculatory blood flow to provide oxygen and reduce anaerobic fermentation but also robust microcirculatory function for effective lactate metabolism. Our findings reveal that the lactate clearance rate (LCR) is higher in patients without early organ function deterioration, suggesting that mitochondrial dysfunction is another critical factor contributing to organ dysfunction during sepsis. Previous studies^[²⁵^]have shown that both human and animal models exhibit improved organ function and survival rates when mitochondrial function is enhanced^[²⁶^,²⁷^]. ROC analysis indicates that ΔPPV, SDC-1, and LCR can predict the risk of septic shock and worsening organ function in ARDS patients, but the predictive accuracy of a single index is limited. Combining ΔPPV with LCR enhances predictive efficacy. The highest survival rates were observed in patients with high ΔPPV and LCR, underscoring the clinical importance of these indicators. PanPan et al.^[¹¹^] noted that 28-day mortality rates are elevated in septic shock patients with ΔPPV below 12.1% six hours post-admission. In our study, a ΔPPV cutoff below 7.6% is also significant for identifying patients at increased risk of early organ function deterioration and mortality.

Moreover, correlation analyses suggest that microcirculation changes are linked to endothelial injury markers, indicating that microcirculatory disorders are intrinsic to the microvascular system rather than merely additive effects of systemic hemodynamics, with glycocalyx damage playing a contributory role in sepsis-induced microcirculatory disorders. The endothelial glycocalyx, crucial for regulating microcirculatory function and maintaining vascular integrity, is significantly impacted during sepsis. Recent clinical studies have frequently detected high concentrations of glycocalyx shedding biomarkers in patients with sepsis-induced ARDS, pointing to early disruption of the endothelial glycocalyx associated with poor prognosis. Preliminary research by Yuka Kajita et al.^[²⁸^]also highlights the close association between persistently elevated SDC-1 levels and sepsis-induced ARDS. Our findings indicate more severe and prolonged glycocalyx damage in patients with early-stage organ dysfunction, suggesting that prompt repair of the endothelial glycocalyx could enhance patient outcomes. The negative correlation between ΔPPV and SDC-1 further underscores the relationship between endothelial glycocalyx injury and microcirculatory disturbances, emphasizing the need for clinicians to focus on endothelial health during resuscitation and actively work to restore endothelial glycocalyx integrity. Data from experimental models indicate a window for intervention to stimulate early repair, with ample evidence supporting the role of timely and adequate fluid resuscitation in protecting and restoring the glycocalyx.

Our study has several limitations. It is an observational, single-center study with a limited duration and lacks the support of large-scale multicenter trials. Additionally, while the relationship between ΔPPV and SDC-1 has been clarified, these findings do not definitively establish a causal link. Lastly, routine clinical use of serum SDC-1 levels has yet to be implemented.

This study demonstrates that the change rate in the proportion of perfused vessels (ΔPPV) holds significant predictive value for early organ function deterioration in patients with septic shock and acute respiratory distress syndrome (ARDS). When combined with the lactate clearance rate (LCR), ΔPPV enhances predictive efficiency, establishing these metrics as effective indicators for evaluating disease progression and treatment outcomes. Additionally, this research corroborates the presence of a correlation between microcirculatory disorders and vascular endothelial glycocalyx damage. Monitoring sublingual microcirculation and its alterations emerges as a crucial focus for future clinical research aimed at enhancing treatment strategies. Continued research is essential to guide the recovery processes in septic shock patients, minimize early organ deterioration, and expand our understanding of the interactions with glycocalyx damage markers.

Credit authorship contribution statement

Shu-Ya Huang: Conceptualization, Data curation, Formal analysis, Project administration, Writing – original draft. Rui Dong: Conceptualization, Data curation, Formal analysis, Project administration. Xiao-Yan Li: Conceptualization, Data curation, Formal analysis, Project administration. Gen-Sheng Zhan: Conceptualization, Data curation, Formal analysis, Project administration, Supervision, Writing – review & editing. Yan-Qiu Gao: Conceptualization, Project administration, Resources, Supervision, Writing – review & editing.

Declaration of Competing Interest

The authors declare no conflict of interest.

Data availability

The datasets used and/or analyzed in the current study are available from the corresponding author upon reasonable request. E-mail address: [email protected] (Yan-Qiu Gao).

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No competing interests reported.

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The value of the proportion of perfused vessels change rate in the evaluation of early organ function deterioration in septic shock and ARDS

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