Clinical features and prognostic factors of Cardiorenal anemia syndrome in China: a retrospective single-center study

doi:10.21203/rs.3.rs-4274074/v1

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Clinical features and prognostic factors of Cardiorenal anemia syndrome in China: a retrospective single-center study

https://doi.org/10.21203/rs.3.rs-4274074/v1

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Background

There is little research on cardiorenal anemia syndrome (CRAS) in China. This study was to describe the characteristics of patients with CRAS and to explore predictive risk factors of all-cause mortality.

Methods

A total of 81795 patients were hospitalized from August 2012 to August 2021 in the nephrology department and cardiology department, of which 820 patients with CRAS met the inclusion criteria and were recruited into this study. The 820 patients with CRAS were divided into three groups based on New York Heart Association (NYHA) functional class: a NYHA Class II group (n = 124), a NYHA Class III group (n = 492), and a NYHA Class IV group (n = 204). Demographics and laboratory tests were collected and risk factors of death events were analyzed. The primary endpoint of the study was death.

Results

820 patients were included, with a median age of 65.00 (51.00–75.00) years and 61.2% were men. The median follow-up was 27.0 (13.0–51.0) months. 416 (50.7%) patients died during follow-up. Age, smoking history, cerebral infarction, NYHA functional class, albumin, serum creatinine (SCr), left ventricular end-diastolic diameter (LVEDD), and left ventricular ejection fraction (LVEF) remained independent predictors in patients with CRAS (P < 0.05) after adjusting to the potential confounders.

Conclusions

Heart failure and renal dysfunction are a fatal combination and are associated with poor prognosis in patients with CRAS.

CRAS

Heart failure

Chronic kidney disease

Anemia

Prognosis factors

Cardiorenal anemia syndrome (CRAS) is a term that refers to a complex group of disorders, including heart failure (HF), chronic kidney disease (CKD) combined with anemia [1–5], which has been widely used in recent years after understanding the importance and association between those mentioned above three. Cardiovascular disease (CVD), including HF, is one of the most common comorbidities in patients with CKD and the leading cause of death in patients with CKD [6]. Approximately 25–50% of patients with HF have CKD [1], and the risk of death is increased by 56% compared with those without CKD [7]. At the same time, the risk of anemia in patients with CKD and CVD significantly increased, and some studies have found that anemia is also an independent risk factor for the progression of CVD and CKD, considerably increasing the risk of hospitalization and death in patients with HF, promoting the progression of kidney disease, and increasing the risk of renal replacement therapy [8]. There is a triangular relationship between the three, a vicious circle in which any of the three can cause the other or be caused by the other. CRAS is attributed to numerous factors, but the exact pathophysiologic mechanisms remain uncertain. Almost all previous studies have been conducted to investigate CRAS in patients with HF, without analyzing the clinical features and prognosis of CRAS alone.

There is currently limited data on clinical features of the CRAS in China. Therefore, this study is aimed to investigate the characteristics and risk factors of survival in patients with CRAS at a single center in China.

Study cohort

81795 patients were admitted to the Department of Nephrology and Cardiovascular Medicine of the Northern Jiangsu People's Hospital between August 2012 and August 2021, of which 820 patients met our inclusion criteria for CRAS. CRAS was defined as a syndrome in which HF, CKD, and anemia coexist, referring to other literature [1–5]. The exclusion criteria were the following: 1) patients age < 18 years or age > 85 years; 2) patients diagnosed with congenital heart disease; 3) patients with malignant tumors, hematologic disease, severe hyperthyroidism, or severe infections; 4) history of blood transfusion in the past 4 months; 5) patients with acute heart failure and acute kidney injury; and 6) incomplete clinical data or lack of follow-up data (Figure. 1).

Data on demographics, comorbidities, vital signs, and laboratory tests were collected using electronic medical records at baseline and during the follow-up. The following echocardiography parameters were collected: left ventricular end-diastolic diameter (LVEDD) and left ventricular ejection fraction (LVEF). Two clinicians independently graded the patients’ NYHA functional class based on their HF symptoms.

The study complied with the Declaration of Helsinki and was approved by the institutional Ethics Research Committee of Northern Jiangsu People's Hospital (No. 2022ky310).

Definitions

The primary endpoint of the study was death. Heart failure was defined by reference to the European Society of Cardiology (ESC) criteria as judged by patients’ symptoms, signs, and ancillary tests [9]. Chronic kidney disease was defined as estimated glomerular filtrate (eGFR) < 60 ml/min/1.73m² or serum creatinine levels > 177 mmol/L for at least 3 months. The eGFR was determined using the CKD-EPI equation [10]. According to the World Health Organization, anemia is defined as a concentration of hemoglobin < 130 g/L in men and < 120 g/L in women [11]. Anemia is classified as mild, moderate, severe, and very severe anemia based on the expert consensus on anemia in China. Mild anemia is a hemoglobin lower than normal and greater than or equal to 90 g/L. Moderate anemia is a hemoglobin greater than or equal to 60 and less than 90 g/L. The amount of hemoglobin in severe anemia is greater than or equal to 30 and less than 60 g/L. The amount of hemoglobin in very severe anemia is less than 30 g/L. Systolic blood pressure (SP) refers to systolic blood pressure at admission.

Statistical analyses

Quantitative data were expressed as mean ± standard deviation or median with interquartile range, depending on whether the data were normally distributed, and differences were compared by t-test or Kruskal-Wallis rank sum test. Categorical data were expressed as numbers (%), and differences were assessed by χ² test or Fisher’s exact test. Patient survival was analyzed by the Kaplan-Meier curve and log-rank test. Univariable and multivariable Cox regression analyses were performed to identify predictors of death. Multivariable Cox regression analyses were adjusted for potential confounders. Variables were selected based on clinical relevance. Results are expressed as hazard ratio (HR) with 95% confidence interval (95% CI). Receiver operating characteristic curve (ROC) and area under the curve (AUC) were used to compare the values of different parameters in the prognosis of CRAS patients. A 2-sided P-value < 0.05 was used to determine statistical significance. Empower (www.empowerstats.com; X&Y Solutions Inc, Boston, MA) and R (http://www.R-project.org) were used for all statistical analyses.

Patient characteristics

A total of 820 patients diagnosed with CRAS were included in the study. Patients were categorized according to the NYHA functional class on admission into three groups: one with NYHA Class II, one with NYHA Class III, and one with NYHA Class IV. There were 124, 492, and 204 patients with NYHA Class II, NYHA Class III, and NYHA Class IV, respectively. We found that there were significant differences in gender, age, diabetes mellitus, atrial fibrillation, edema, dialysis, SCr, N-terminal pro-brain natriuretic peptide (NT-proBNP), patient survival months, and mortality between the three groups (P < 0.05).

Baseline characteristics of patients with CRAS are shown in Table 1. There were 41 patients with CKD stage 3, 109 with CKD stage 4, and 670 with CKD stage 5. There were 366 patients with mild anemia, 429 with moderate anemia, and 25 with severe anemia. The median age of the patients was 65.00 (51.00–75.00) years, and 61.2% were men. In the whole sample, the median SCr was 601.6 (378.0-818.0) umol/L, the median hemoglobin was 88.0 (75.0-101.0) g/L, and the median NT-proBNP was 31200.0 (11800.0-83000.0) pg/mL. The rates of statin use, renal replacement therapy, and correction of anemia were 29.3%, 47.1%, and 69.4%, respectively. Median follow-up was 27.0 (13.0–51.0) months, 86.5% of patients had at least six months of follow-up, and 416 (50.7%) patients died. The mortality rate was observed to increase with worsening of heart failure, with mortality rates of 44.4%, 47.4%, and 62.8% in NYHA functional class II, III, and IV, respectively.

Table 1

Baseline characteristics of patients with CRAS
Characteristic	Total (N = 820)	NYHA Class II (N = 124)	NYHA Class III (N = 492)	NYHA Class IV (N = 204)	P-value
Male, n(%)	502 (61.2)	85 (68.6)	307 (62.4)	110 (53.9)	0.022
Age, years	65.0 (51.0–75.0)	61.0 (45.0–72.0)	64.0 (51.0–74.0)	69.0 (51.0–76.0)	0.001
Hypertension, n(%)	725 (88.4)	103 (83.1)	437 (88.8)	185 (90.7)	0.102
SP, mmHg	150.0 (135.0-170.0)	150.0 (136.0-171.3)	150.0 (134.0-169.0)	152.0 (138.0-175.3)	0.305
Smoking, n(%)	157 (19.2)	18 (14.5)	98 (19.9)	41 (20.1)	0.363
Diabetes mellitus, n(%)	386 (47.1)	44 (35.5)	207 (42.1)	104 (51)	0.016
Myocardial infarction, n(%)	38 (4.6)	5 (4.0)	23 (4.7)	10 (4.9)	0.934
Cerebral infarction, n(%)	140 (17.1)	21 (17.0)	80 (16.3)	39 (19.1)	0.659
Atrial fibrillation, n(%)	108 (13.2)	6 (4.8)	66 (13.4)	36 (17.7)	0.004
Edema, n(%)	501 (61.1)	63 (50.8)	291 (59.2)	147 (72.1)	< 0.001
Dialysis	386 (47.1)	60 (48.4)	248 (50.4)	78 (38.2)	0.013
White blood cells, *10^9/L	6.4 (4.5–8.4)	6.0 (4.9-8.0)	6.4 (5.0-8.5)	6.7 (5.0-8.6)	0.076
Hemoglobin, g/L	88.0 (75.0-101.0)	87.5 (75.0-103.0)	88.0 (76.0-102.0)	89.0 (74.8–100.0)	0.929
Albumin ,g/L	35.9 (31.7–39.9)	36.1 (31.6–40.7)	36.6 (32.2–40.0)	34.7 (31.4–40.0)	0.155
SCr, umol/L	601.6 (378.0-818.0)	634.0 (396.3-889.3)	614.5 (402.9-821.3)	529.0 (328.0-763.2)	0.003
eGFR, ml/min/1.73m2	7.1 (5.0-12.2)	6.7 (4.8–11.1)	7.0 (5.0-11.5)	7.9 (5.1–13.8)	0.075
NT-proBNP	31200.0 (11800.0-83000.0)	38100.0 (15000.0-96977.0)	28950.0 (9862.5-78025.0)	33016.8 (13475.0-84207.5)	0.012
cTnT, ng/mL	0.1 (0.0-0.3)	0.1 (0.0-0.3)	0.1 (0.0-0.2)	0.1 (0.0-0.4)	0.413
LVEF, %	55.0 (45.0–60.0)	54.5 (46.0–60.0)	55.0 (46.0–60.0)	53.0 (42.8–60.0)	0.055
LVEDD, mm	54.0 (50.0–58.0)	55.0 (50.0–59.0)	53.0 (49.8–58.0)	54.0 (49.0–59.0)	0.458
Survival, months	27.0 (13.0–51.0)	39.5 (17.0-77.3)	27.50 (14.0–49.0)	18.00 (9.00–44.0)	< 0.001
Death, n(%)	416 (50.7)	55 (44.4)	233 (47.4)	128 (62.8)	< 0.001
Values are median (interquartile range) or n (%).
CRAS, cardiorenal anemia syndrome; NYHA, New York Heart Association functional class; SP, systolic blood pressure; SCr, serum creatinine; eGFR, estimated glomerular filtration rate; NT-proBNP, N-terminal pro-brain natriuretic peptide; cTnT, serum cardiac troponin T; LVEF, left ventricular ejection fraction; LVEDD, left ventricular end-diastolic diameter.

Predictors of death

In univariable Cox regression analyses, age, SP, smoking history, myocardial infarction, cerebral infarction, atrial fibrillation, dialysis, NYHA functional class, SCr, and LVEDD were observed to show a significant association with the risk of death. After adjusting the gender, age, smoking history, SP, myocardial infarction, cerebral infarction, atrial fibrillation, NYHA functional class, dialysis, SCr, LVEDD, and LVEF, multivariable Cox regression analyses showed that age, smoking history, cerebral infarction, NYHA functional class, albumin, SCr, LVEDD, and LVEF were close-dependent related to the risk of death (P < 0.05) (Table 2). The Kaplan-Meier survival curves of patients with CRAS in three groups were shown in Fig. 2, which showed that the higher NYHA functional class, the worse the prognosis of patients with CRAS (P < 0.001).

Table 2

Predictors of death (univariable and multivariable analyses)
Variable	Unadjusted HR (95%CI)	P-value	Adjusted HR (95%CI)	P-value
Gender	1.25 (1.03, 1.52)	0.024	1.23 (0.99, 1.52)	0.063
Age, years	1.04 (1.03, 1.05)	< 0.001	1.04 (1.03, 1.05)	< 0.001
Hypertension	1.07 (0.79, 1.45)	0.658	1.02 (0.75, 1.40)	0.887
SP, per 10 mmHg	0.95 (0.91, 0.98)	0.004	0.98 (0.94, 1.02)	0.330
Smoking	1.37 (1.08, 1.76)	0.011	1.38 (1.06, 1.80)	0.018
Diabetes mellitus	1.21 (0.99, 1.46)	0.058	1.01 (0.83, 1.24)	0.904
Myocardial infarction	1.80 (1.19, 2.72)	0.005	1.17 (0.76, 1.78)	0.479
Cerebral infarction	1.79 (1.41, 2.26)	< 0.001	1.36 (1.07, 1.74)	0.012
Atrial fibrillation	1.46 (1.12, 1.90)	0.005	0.86 (0.65, 1.15)	0.303
Dialysis	0.62 (0.51, 0.76)	< 0.001	0.83 (0.66, 1.04)	0.105
NYHA, per I class	1.46 (1.25, 1.70)	< 0.001	1.28 (1.10, 1.51)	0.002
Hemoglobin, per 10 g/L	1.02 (0.96, 1.07)	0.586	0.97 (0.91, 1.03)	0.266
Albumin, g/L	0.99 (0.97, 1.00)	0.146	0.98 (0.96, 0.99)	0.005
SCr, per 88.4 umol/L	0.93 (0.91, 0.96)	< 0.001	1.04 (1.01, 1.07)	0.007
NT-proBNP, per 100 pg/ml	1.00 (1.00, 1.00)	0.708	1.00 (1.00, 1.00)	0.073
cTnT, per 0.1 ng/mL	1.01 (0.99, 1.03)	0.421	1.00 (0.98, 1.02)	0.719
LVEDD, per 10 mm	0.78 (0.67, 0.90)	< 0.001	0.82 (0.68, 0.97)	0.023
LVEF, per 10%	0.92 (0.84, 1.01)	0.087	0.81 (0.72, 0.91)	< 0.001
HR, hazard ratio; CI, confidence interval; SP, systolic blood pressure; NYHA, New York Heart Association functional class; SCr, serum creatinine; NT-proBNP, N-terminal pro-brain natriuretic peptide; cTnT, serum cardiac troponin T; LVEDD, left ventricular end-diastolic diameter; LVEF, left ventricular ejection fraction.
Multivariable analyses adjusted gender, age, smoking history, SP, myocardial infarction, cerebral infarction, atrial fibrillation, NYHA functional class, dialysis, SCr, LVEDD, and LVEF.

Comparison of clinical characteristics and laboratory parameters in predicting prognosis in CRAS patients

Receiver operating characteristic curve (ROC) analysis was used to compare the values of different parameters in the prognosis of CRAS patients (Figure. 3). The age (P < 0.001), SCr (P < 0.001), LVEDD (P < 0.001), and NYHA functional class (P = 0.001) all had diagnostic values with statistical significance for prognosis of patients with CRAS. Among these values, the area under the curve (AUC) value of age was the largest (AUC = 0.709) (Table 3).

Table 3

Comparsion of eight influencing factors in patients with CRAS
Test	AUC	95%CI	P-value
Smoking (Yes/NO)	0.503	0.464–0.543	0.870
LVEF, %	0.522	0.482–0.561	0.279
Albumin, g/L	0.526	0.487–0.566	0.193
Cerebral infarction (Yes/NO)	0.546	0.507–0.586	0.022
NYHA, class	0.565	0.526–0.604	0.001
LVEDD, mm	0.568	0.529–0.607	< 0.001
SCr, umol/L	0.590	0.551–0.629	< 0.001
Age, years	0.709	0.674–0.744	< 0.001
AUC, area under the curve; CI, confidence interval; LVEF, left ventricular ejection fraction; NYHA, New York Heart Association functional class; LVEDD, left ventricular end-diastolic diameter; SCr, serum creatinine; LVEDD, left ventricular end-diastolic diameter.

There is a strong link between heart disease and kidney disease, and the two influence each other, which has long been a concern by the medical community [12, 13]. The first mention of cardiorenal syndrome (CRS) was in 1913, when Thomas Lewis proposed the presence of a close relationship between the heart and the kidney [14]. Since then, much progress has been made in the pathogenesis, classification, and treatment of cardiorenal syndrome. In 2008, under the initiative of Ronco et al. [15], the Acute Disease Quality Initiative (ADQI) working group proposed the first consensus on the definition and classification of CRS. CRS often coexists with anemia, which leads to reciprocal and progressive cardiac and renal deterioration. The triad of heart failure, chronic kidney disease, and anemia is termed cardiorenal anemia syndrome (CRAS).

CRAS is considerably prevalent, and the management of patients with CRAS remains a challenging undertaking worldwide because of the complexity and heterogeneity of this syndrome and the lack of evidence-based clinical guidelines. At present, CRAS is common in patients with HF and is an independent predictor of all-cause mortality [3], but few studies have reported the clinical features of CRAS and its prognostic factors. Therefore, this study focused on describing the baseline characteristics of patients with CRAS and the influencing factors of their prognosis. We compared the baseline characteristics of the patients with CRAS according to their NYHA functional class and found that there were significant differences in gender, age, diabetes mellitus, atrial fibrillation, edema, dialysis, SCr, NT-proBNP, patient survival months, and mortality between the three groups (P < 0.05). Although there was no relationship between gender and prognosis after multivariate adjustment, there was a significant difference in gender between the three groups, which is an interesting phenomenon. Marta et al. found sex-related differences in patients with cardiorenal syndrome. More advanced kidney disease, anemia, and an increased prevalence of preserved ejection fraction are more common in women with CRS, whereas heart failure with reduced ejection fraction was more frequently observed in men [16]. It has been found that CRAS is associated with increasing age and diabetes mellitus [3], which is similar to our research, and we found that with the increase of NYHA functional class, the proportion of CRAS patients with diabetes mellitus and age increased. Diabetes mellitus is also a major risk factor for the development of coronary artery disease and HF [17, 18], and diabetes mellitus is the most common cause of CKD in Western countries and China [19]. Moreover, as the NYHA functional class increased, the proportion of edema, atrial fibrillation, and NT-proBNP values were higher, while the LVEF values were lower, indicating that CRAS patients had more severe HF or other cardiovascular diseases. NT-proBNP is associated with HF NYHA functional class, LVEF, and ventricular pressure, thereby contributing to prognosis and risk classification in patients with HF [20]. Moreover, NT-proBNP is associated with renal insufficiency and is more sensitive in predicting cardiovascular and all-cause mortality in patients with CKD [21].

The development of CRAS is multifactorial, and some risk factors have been recognized. Advanced age, diabetes mellitus, ischaemic etiology, NYHA functional class, and LVEF are independently associated with CRAS in patients with HF [2, 5]. Most studies have explored the effect of the presence or absence of CRAS on prognosis in patients with HF, and few studies have described the prognostic factors of CRAS itself, whether it is HF, renal insufficiency, anemia, or others. Therefore, this article found that age, smoking history, cerebral infarction, NYHA functional class, albumin, SCr, LVEDD, and LVEF were closely related to the risk of death in patients with CRAS (P < 0.05). In addition, We further compared survival of patients with CRAS in three groups by the Kaplan-Meier curve, which showed that the higher NYHA functional class, the worse the prognosis of patients with CRAS. All these indicated that HF plays an important role in the prognosis factors of CRAS.

Next, we used ROC analysis to compare the values of different parameters in the prognosis of CRAS patients, and we found that the AUC value of age was the largest (AUC = 0.709). Undoubtedly, advanced age is a prognostic risk factor for heart failure and chronic kidney disease, and Domenico et al. also found that age was independently related to CRAS (P < 0.001) [5]. Likewise, cigarette smoking has been identified as an independent risk factor for cardiovascular events and incident CKD [22, 23], which is similar to our conclusions, and we found that smoking history is an independent risk factor for the prognosis of CRAS patients. We also found cerebral infarction, albumin, and SCr were closely related to the risk of death in patients with CRAS. Cerebrovascular disease and cardiovascular disease not only have similarities in the occurrence and development of diseases, such as cerebral infarction and myocardial infarction, but also have a high overlap rate in the affected population. Albumin has anti-inflammatory, antioxidant, and antithrombotic properties [24]. Hypoalbuminemia is a strong predictor of increased all-cause and cardiovascular mortality based on several cohort studies and meta-analyses [16, 25–27]. Pedro et al. explored the survival rates of HF patients with CRAS in Tanzania and found that renal dysfunction was a predictor of mortality [4], which is consistent with our conclusions.

Patients with CKD and HF have an increased risk of anemia. The presence of anemia increases in parallel with the severity of HF, the CKD stage, and the patients' age, while the treatment of anemia leads to an improvement in cardiac and renal function as well as fewer hospitalizations for HF [28]. Here, we found that anemia in CRAS patients was not related to prognosis, either because these patients were treated aggressively or because of sample size.

CRAS is a comprehensive term encompassing the intricate relationship between simultaneous cardiac, renal impairments and anemia, wherein the deterioration of one organ initiates, perpetuates, or accelerates the decline of the other. The pathologic triangle formed by HF, CKD, and anemia carries high morbidity and mortality rates and decreases quality of life. Our study showed that 50.7% of patients with CRAS died during follow-up. Moreover, the mortality rate of patients is closely related to age, smoking history, cerebral infarction, NYHA functional class, albumin, SCr, LVEDD, and LVEF.

Although the pathophysiologic mechanisms underlying CRAS remain uncertain, we can identify and treat the potentially reversible causes early based on prognostic influencing factors, which may improve outcomes in these CRAS patients.

Our study still had some limitations. The retrospective study reflected patient data and findings only from a single center in China. Moreover, Hb concentrations on admission were measured, which may not accurately reflect Hb levels after discharge or changes in Hb levels over time. We also did not attempt to identify the cause or assess the treatment or maintenance of anemia during follow-up.

Acknowledgments

Not applicable

Funding

This work was supported by the Scientific Research Project of Jiangsu Provincial Healthcare Commission (Grant number Z2022068) and Hospital Research Projects (Grant number SBQN22006 and FCJS202340).

Availability of data and materials

Availability of data and material datasets collected and analyzed in the current study are available from the corresponding author on reasonable request.

Ethical approval and Informed consent

This study was approved by the ethics committee of Northern Jiangsu People's Hospital (No. 2022ky310) and was carried out following the principle of the Helsinki Declaration. This is a retrospective study using de-identified data, and our institutional review board did not require consent from the patient.

Competing Interest

All the authors declared no competing interests.

Author Contribution

RW, DH and CL contributed to the conception of the study. ML, JL and XX screened the data, and MZ analyzed and interpreted the data. MZ,YC, CZ, JX and GZ contributed to the follow-up. MZ finished the manuscript. HM, GB, and CL supervised and edited the manuscript. All authors contributed to the work and approved the submitted version for publication.

Data Availability

Data is provided within the manuscript or supplementary information files

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Reviewers agreed at journal
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Clinical features and prognostic factors of Cardiorenal anemia syndrome in China: a retrospective single-center study

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