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A nomogram including admission serum glycated albumin/albumin ratio to predict mortality in patients with severe fever with thrombocytopenia syndrome

BMC Infectious Diseases volume 24, Article number: 858 (2024) Cite this article

Abstract

Background

Severe fever with thrombocytopenia syndrome (SFTS) is a novel tick-borne infectious disease with a high fatality rate. Although several nomograms based on demographic and laboratory data have been reported to predict the prognosis of SFTS in recent studies, baseline serum glycated albumin (GA)/albumin (ALB) ratio included risk model has not been evaluated for the prediction of clinical outcome.

Methods

A total of 214 SFTS patients with integral data admitted to our hospital from May, 2020 to November, 2022 were included in this study. SFTS infection was confirmed by real time fluorescent quantitative PCR (qRT-PCR). The demographic characteristics, clinical and laboratory data were collected with in 24 h of admission and 1 to 2 days before discharge and were analysed retrospectively.

Results

Fiffty-seven patients (26.6%) died. Multivariate logistic regression analysis showed that age, aspartate aminotransferase (AST), blood glucose (GLU), GA/ALB ratio, neutrophil counts (NEU) and lymphocyte percentage (LYM%) were the independent risk factors for mortality. A nomogram by these factors was created using RMS package in the R program. Area under the receiver operating characteristic (ROC) curve (AUC) of this nomogram was 0.88 (95% CI: 0.83, 0.93). This model showed the excellent net benefit, as revealed by the decision curve analysis. GA/ALB ratios were also independent risk factors for poor out clinical come in subgroups of patients with hyperglycemia on admission and with diabetes history. Nomograms were constructed by the independent risk factors in the subgroups. AUCs of the nomograms in the subgroups showed high predictive values for adverse prognosis.

Conclusions

GA/ALB ratios were independent risk factors for mortality in all SFTS patients and subgroups of with hyperglycemia on admission and diabetes history. The nomograms including GA/ALB ratio had high predictive value for adverse clinical outcome.The nomograms provide a basis for clinical decision-making for the treatment of SFTS patients in different clinical settings.

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Introduction

Severe fever with thrombocytopenia syndrome (SFTS) is an emerging tick-borne disease caused by SFTS virus (SFTSV), a novel Bunyavirus, phlebovirus which may lead to multiple organ failure with an average fatality rate of approximately 20% [1]. The pathogenesis of SFTS is not fully elucidated which may involve several mechanisms: direct SFTSV invasion and replication of SFTSV in multi-organs induced inflammation responses [2, 3] and cell death, such as cell pyroptosis [4]; host immune responses against SFTSV [5] which result in the substantial production of inflammatory cytokines and chemokines, described as cytokine storm [6, 7]. The exacerbation of the inflammatory response causes oxidative stress and reactive oxygen species (ROS) production, alterations in mitochondrial energy dynamics, activates the sepsis cascade, and multiple organ failure [8]. No effective vaccines or no specific effective therapeutic methods are available for SFTS currently. It is crucial to identify risk factors of prognosis on admission for patients who need timely intensive treatment.

Human serum albumin (ALB) is the most abundant protein in human plasma or serum accounting for approximately 60% of the total protein content of serum. HSA participates in various physiological processes. For instance, it assists in the regulation of osmotic pressure and pH balance in blood [9]. HSA has multiple binding sites located in different subdomains which are responsible for binding of a variety of ligands [10]. Due to the free thiol group of the reduced cysteine at position 34 (Cys34), which represents the most abundant free thiol in the plasma, albumin can serve as a trap for ROS and reactive nitrogen species [11], thus participating in redox reactions [12]. Under long-term hyperglycemia, HSA frequently undergoes non-enzymatic glycation (NEG), which may affect its structure and impair HSA function as an antioxidant [12, 13]. Glycated albumin (GA) is one of the early precursor of advanced glycation end products (AGEs), which cause physiological alterations in various cellular proteins and organelles. GA contributed significantly to the pathogenesis of diabetes and other diseases and was regarded as a biomarker of some diseases [12, 14]. Thus, high GA levels may correlate with adverse clinical outcomes of patients with SFTS.

Previous studies [15,16,17] have demonstrated that hyperglycemia was associated with SFTS severity and SFTS-related death. In addition, low albumin level and related models had was positively correlated with inflammation and with poor prognosis in SFTS patients [18]. Whereas, serum GA/ALB ratio and risk models include this parameter for the prediction of the prognosis of SFTS have not been evaluated.

Due to the significant fluctuations of ALB and GLU levels in the clinical settings with different severity, we focus on the role of on admission GA/ALB ratio in the prediction of clinical outcome.

In this study, we sought to establish risk models (nomograms) containing admission GA/ALB ratio for the prediction of adverse clinical outcome of SFTS patients with different clinical settings during hospitalization which may help clinical therapeutic decision.

Methods

Patients’ enrollment and data collection

A total of 214 laboratory-confirmed SFTS patients with integral data who were admitted to our hospital from May, 2020 to November, 2022 were included in this study. Data of GA and GA/ALB ratio were absent in some patients in mild state, patients included were in more severe state. GA/ALB ratio was calculated as the ratio of serum GA level to serum ALB level. The diagnosis of SFTS was based on SFTSV positive results using real time fluorescent quantitative PCR (qRT-PCR) method. The baseline clinical and laboratory data were chosen at the time of with in 24 h of admission and 1–2 days before discharge, and were analyzed retrospectively. Serum biochemical parameters were assayed by Beckman AU5800 automatic biochemical analyzer.

Ethics, consent and permissions

The study was approved by the ethics committee of Qishan Hospital of Yantai, Shandong (Ethics number 202201), China, and was performed according to the Helsinki II Declaration.

Statistic analysis

Continuous variables were expressed as the mean ± standard deviation (SD) with normal distribution or median (interquartile range, IQR) for skew distribution, and categorical variables were described as a frequency. The independent or paired samples t-test or Mann–Whitney U test was used for comparing value difference between two the groups. The categorical variables were represented as percentages (n/N, %) and tested with the χ2 test or Fisher’s exact test. Paired t-test or paired nonparametric test were used for admission data and discharge data. Spearman’s correlation analysis was used for correlation analysis. Univariate and multivariate logistic regression analysis were applied to identify independent risk factors for mortality using the Stepwise method. Risk nomogram models were constructed based on independent risk factors. Area under receiver operating curve (ROC) (AUC), decision curve, decision curve analysis (DCA) curve were used to evaluate the accuracy of prediction for mortality. SPSS software (version 26.0, IBM, Armonk, NY, USA), MedCalc software and R software were used for statistical analysis. A two-sided p values < 0.05 were considered as statistical significance.

Results

Demographics, clinical characteristics and biochemical data of SFTS patients on admission

Of patients, 57 patients (26.6%) died. 68 cases (31.8%) admitted to intensive care unit (ICU). Thirty-nine patients (18.22%) had a diabetic history, and 119 cases (55.9%) manifested hyperglycemia of fasting blood glucose (GLU) (≥ 7 mmol/L) on admission. Hyperglycemia prevalence rate is higher in death group (73.6%) than in survival group (49%) (p = 0.002). Proportions with diabetes history had no significant difference between the two groups. The mean age, parameters of liver injury and kidney injury, serum levels of GLU (p < 0.0001) and GA/ALB ratio were higher (p = 0.001), ALB (p < 0.0001) concentrations were lower and hospital stay was shorter (p < 0.001) in mortality patients than in survivors on admission. Neutrophil percentage (NEU%) was higher, and lymphocyte percentage (LYM%) and platelet counts (PLT) were lower in non-survivors than in survivors. The comparison results in non-ICU and ICU patients were similar as in survivors and non-survivors (Table 1).

Table 1 Baseline demographic characteristics, clinical and biochemical parameters [Mean ± SD or M (Q₁, Q₃)]
Full size table

In patients with hyperglycemia (> 7 mmol/L), results of biochemical parameter of liver and renal function were similar compared with those in all patients. Levels of GLU were higher in non-survivors and in ICU patients than in survivors and non-ICU patients. While, GA/ALB were comparable in the groups (Table 2).

Table 2 Baseline demographic characteristics, clinical and biochemical parameters in patients with hyperglycemia[Mean ± SD or M (Q₁, Q₃)]
Full size table

Independent risk factors and nomograms for prediction of mortality in all patients and different subgroups during hospitalization

Results showed that age [odd ratio (OR): 1.12 ; 95% confidence interval [CI]: 1.06 ~ 1.17, p < 0.001], AST (OR: 1.01; 95% CI: 1.01 ~ 1.01, p < 0.001), GLU(OR: 1.12; 95% CI: 1.03 ~ 1.22, p = 0.011), GA/ALB ratio (OR: 1.1; 95% CI: 1.03 ~ 1.17, p = 0.005), neutrophil counts (NEU) (OR: 0.74; 95% CI: 0.55 ~ 0.98, p < 0.001) and LYM% (OR: 0.95; 95% CI: 0.92 ~ 0.99, p = 0.01) were the independent risk factors for mortality (Table 3). Age, AST, GLU, GA/ALB ratio and LYM% were the independent risk factors in patients with hyperglycemia (> 7 mmol/L), Age, AST and NEU% were the independent risk factors in patients with glycemia ≤ 7 mmol/L, and GA/ALB and serum cystatin (CysC) were the independent risk factors in patients with diabetes history for adverse clinical outcome (Table 3).

Table 3 Independent risk factor for mortality obtained in univariate and multivariate regression in all patients and in patients with hyperglycemia, glycemia ≤ 7 mmol/ml and diabetes
Full size table

Nomograms were created by these independent risk factors in all patients and different subgroups (Fig. 1). Predictive values of these nomograms were evaluated by AUCs (Table 4; Fig. 2). In all patients, AUC of the nomogram was 0.88 (95% CI: 0.83, 0.93) with sensitivity and specificity were 0.79 (0.73, 0.86) and 0.85 (0.76, 0.95), respectively. The accuracy was 0.81 (0.75, 0.86). AUCs of the nomograms in the subgroups had high predictive values for adverse clinical outcome. And these models showed the excellent net benefit, as revealed by the decision curve analysis (Fig. 3).

Fig. 1
figure 1

Nomograms for the prediction of mortality in all patients (a), patients with hyperglycemia (> 7 mmol/L) (b), patients with glycemia (≤ 7 mmol/L) (c), and patients with diabetes history (d)

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Table 4 Predictive values of nomogarms constructed in all patients and in different subgroups for adverse clinical outcome
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Fig. 2
figure 2

AUCs of nomograms for the prediction of mortality in all patients (a), patients with hyperglycemia (> 7 mmol/L) (b), patients with glycemia (≤ 7 mmol/L) (c), and patients with diabetes history (d)

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Fig. 3
figure 3

DCA of nomograms for the prediction of mortality in all patients (a), patients with hyperglycemia (> 7 mmol/L) (b), patients with glycemia (≤ 7 mmol/L) (c), and patients with diabetes history (d)

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Paired comparison of GA/ALB ratio and related biochemical results at admission and before discharge in SFTS patients

A total of 107 patients had paired results of admission and before discharge. Serum GLU and ALB levels (p < 0.001), and GA/ALB ratio (p = 0.049) still had significant difference between survivors and nonsurvivors before discharge (Table 5). Levels of GLU (p < 0.001) and GA/ALB ratio (p = 0.044) elevated significantly in ICU than in non-ICU patients at discharge, while ALB level was comparable (Table 6). Paired nonparametric test showed levels of GA and GA/ALB ratio (p < 0.001) were higher before discharge than at admission in all patients. Whereas, only GA/ALB ratio level in survivors, and GLU level in non-survivors elevated significantly at discharge (p = 0.001) (Table 5).

Table 5 Paired comparison of biochemical parameters on admission and before discharge in survivor and non-survivor patients of SFTS
Full size table
Table 6 Paired comparison of biochemical parameters on admission and before discharge in non-ICU and ICU admission patients of SFTS
Full size table

Serum GLU and GA/ALB ratio levels were elevated significantly in ICU patients than in non-ICU patients before discharge. In non-ICU patients, serum ALB level decreased and in ICU patients, GLU increased significantly before discharge compared with baseline data (Table 6).

Discussion

In this study, we demonstrated that on admission GA/ALB ratios were independent risk factors for poor clinical outcome in all patients and in subgroups of patients with hyperglycemia on admission and with diabetes history. It is not an independent risk factor in patients with GLU ≤ 7mmol/L. These results suggest that GA/ALB may be a susceptible factor for SFTSV infection before admission and contribute disease progression during hospitalization. In addition, age, AST, GLU, NEU, and LYM% were other independent risk factors for in-hospital mortality.

Nomograms constructed by the independent risk factors including GA/ALB ratio in all patients and in the subgroups showed high predictive values for adverse prognosis.

The epidemic of SFTS is becoming a public health problem globally, especially prevalent in Central and Eastern China, Japan, and South Korea. Resident of age ≥ 60 years old in the epidemic area was regarded as a risk factor for SFTS [19] who usually had several preexisting chronic conditions. Diabetes mellitus (DM) (6.8%) is one of the common comorbidities in SFTS, and high serum glucose contributed to deterioration of diseases severity and higher death risk [20]. This is inline with our results. It has been demonstrated that elevated level of serum glucose was correlated with hypercoagulability, inflammation state, and lower platelet counts in SFTS patients [17]. Persistent hyperglycemia frequently lead to serum protein NEG resulting in the formation of advanced glycation end-products (AGEs).

Albumin can bind various endogenous and exogenous ligands and almost all known drugs and toxic substances. Albumin glycation affects the ligand binding properties, therefore not only influence redox state [10] but also the efficacy of anticoagulant [13], glycemic control [21] and other various physiological processes [22]. Being the most abundant serum protein, HSA has a higher chance to be modified by NEG [14]. GA could bind to the receptor for AGE (RAGE), known to be expressed in various kinds of cells. The engagement of AGEs with RAGE activates a myriad of signaling pathways such as MAPK/ERK, TGF-β, JNK, and NF-κB, leading to enhanced oxidative stress and inflammation. [23]. GA promotes the expression of various cytokines, such as IL-1β, IL-6, TNF-α and CCL-2 at both of mRNA and protein levels through the RAGE. The higher glucose concentration, the effect was predominant [24].

GA has recently gained more attention as a good alternative reliable indicator of glycemic control in diabetic patients due to its shorter lifespan compared to glycated hemoglobin (HbA1c), the currently “gold standard” for diabetes monitoring in clinics [25]. Therefore, albumin glycation in SFTS patients may affect multiple physiological functions and ultimately results in disease aggravation.

Recent studies showed that native albumin binds the spike protein S1 subunit of SARS-CoV-2 virus, suggesting that native albumin may act as a scavenger of the virus. This binding ability of native albumin was decreased in the presence of an increasing concentration of GA. The preference of SARS-CoV-2 for GA may in part explain the severity and pathology of acute respiratory distress and the bias towards the elderly and those with (pre) diabetic and metabolic disease [26]. Age and diabetes were also risk factors for SFTSV infection and disease progression which suggest that the influence of GA on SFTSV infection shared common mechanisms with that of GA on SARS-CoV-2.

Serum ALB concentrations were decreased in non-survivors and ICU patients than in survivors and non-ICU patients, respectively both at admission and discharge. In paired comparison, ALB levels were reduced in survivors and non-ICU patients at discharge compared to admission results, respectively. While they were comparable at admission and discharge in the death and ICU patients. This may be that albumin synthesis and supplementation can not compensate for loss and metabolism in mild patients. And in patients with severe condition, they were given albumin infusion more frequently due to the hypoalbuminemia than in patients with mild condition during hospitalization as supportive therapy. Due to the dramatic change of ALB level because of metabolic alterations in SFTS, this supportive therapy could not relieve severe condition, it should combined with other therapeutic measures including controlling hyperglycaemia, improving liver and kidney injury and other measures.

Admission multi-organ injury represented by AST elevation [27], and decreased NEU, and LYM% which may lead to combined with bacterial and fungal infections contributed together with other independent risk factors to poor clinical outcome.

Conclusions

GA/ALB ratios were independent risk factor for mortality in SFTS patients and patients with high GLU level and diabetes history, and the nomograms including this ratio had superior efficacy for the prediction of adverse clinical outcome.The nomograms provide basis for clinical decision-making for the treatment of SFTS patients. Deep insight into the role of GA/ALB ratio in SFTS etiopathogenesis and clinical course of disease may provide additional information for clinical therapeutic decision. The precision mechanism of GA on SFTSV susceptibility, effects on drug treatment needs further investigation in the future.

Data availability

The datasets generated and/or analysed during the current study are not publicly available due to secrecy but are available from the corresponding author on reasonable request.

Abbreviations

ALB:

Albumin

AGEs:

Advanced glycation end-products

AST:

Aspartate aminotransferase

AUC:

Area under ROC curve

BUN:

Blood urea nitrogen

CI:

Confidence interval

CysC:

Cystatin

DCA:

Decision curve analysis

GA:

Glycated albumin

GLU:

Blood glucose

ICU:

Intensive care unit

IQR:

Interquartile range

NEG:

Non-enzymatic glycation

NEU:

Neutrophil counts

NEU:

Neutrophil counts

OR:

Odd ratio

ROC:

Receiver operating characteristic curve

RAGE:

Receptor for AGE

SFTS:

Severe fever with thrombocytopenia syndrome

SFTSV:

SFTS virus

sCr:

Serum creatinine

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Acknowledgements

The authors thank those who contributed to SFTS diagnosis and treatment.

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Authors and Affiliations

  1. Department of Clinical Laboratory, Qishan Hospital of Yantai, 62 Huanshan Road, Zhifu District, Yantai, 264001, Shandong, The People’s Republic of China

    Li Wang

  2. Department of Infectious disease, Qishan Hospital of Yantai, 62 Huanshan Road, Zhifu District, Yantai, 264001, Shandong, The People’s Republic of China

    Hui Xie, Youde Liu & Zhiqiang Zou

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Contributions

Li Wang wrote tha main manuscript text, Hui Xie and Youde Liu prepared the Figures, Zhiqiang Zou collected some of the data. All authors reviewed the manuscript.

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Correspondence to Li Wang.

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This study was performed according to the Helsinki II Declaration and was approved by the ethics committee of Qishan Hospital of Yantai, Shandong, China (Ethics number 202201). The requirement for informed consent by individual patients was waived by the Ethical Committee of Qishan Hospital of Yantai due to the retrospective nature of the study.

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Wang, L., Xie, H., Liu, Y. et al. A nomogram including admission serum glycated albumin/albumin ratio to predict mortality in patients with severe fever with thrombocytopenia syndrome. BMC Infect Dis 24, 858 (2024). https://doi.org/10.1186/s12879-024-09752-9

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BMC Infectious Diseases

ISSN: 1471-2334

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