Left Atrial Mechanics in Youth with Chronic Kidney Disease and Similarly Aged Healthy-Controls

doi:10.21203/rs.3.rs-4001372/v1

Introduction: In adults with chronic kidney disease (CKD), abnormal left atrial reservoir strain (LASr) is an early, yet clinically significant, indicator of myocardial dysfunction. However, left atrial mechanics are understudied in youth with CKD. The objective of this study was to assess left atrial strain function in youth with CKD and similarly aged, healthy controls.

Methods: We performed a single-center, retrospective, observational study of persons aged 12-21 years with stage 3-4 CKD and healthy controls. Exclusion criteria included a history of a kidney or other solid organ transplant, congenital heart disease, and/or dialysis requirement <3 months prior. We measured LAS (LASr, conduit, contractile), E/e’, E/A, left ventricular mass index (LVMI), and ejection fraction. Pearson correlations were performed between echocardiographic measures.

Results: This study included 37 patients with CKD and 19 controls. Mean age was similar between groups and male sex was over-represented in both groups (CKD: 62%, Healthy: 63%). Mean ± standard deviation (SD) eGFR in the CKD group was 32 ±14mL/min/1.73m2. Mean absolute LASr was significantly lower in those with CKD (43.0 ±8.5%) compared to healthy controls (47.4 ±6.1%). Patients with CKD had significantly higher LVMI, and lower E/A and E’ compared to controls. There was poor correlation between LASr with E/A, E/e’, and LVMI.

Conclusions: As observed in adults with CKD, LASr was significantly lower in youth with CKD compared to healthy controls. Moreover, LASr poorly correlated with traditional measures of diastolic dysfunction such as E/e’ and E/A.

Cardiovascular disease is an important complication of chronic kidney disease (CKD) across the lifespan¹. As such, echocardiography is commonly performed in youth with CKD to monitor for subclinical myocardial disease. There are no specific guidelines for routine echocardiographic surveillance in youth with CKD, however clinical and research studies commonly evaluate for left ventricular hypertrophy (LVH), systolic dysfunction and aortic dilation². Ventricular diastolic dysfunction is not universally included in monitoring of youth with CKD.

Subclinical left ventricular diastolic dysfunction (LVDD) is highly prevalent in adults with CKD, and closely associated with risk for incident heart failure and cardiovascular (CV) mortality^{3, 4}. However, there are significant limitations to the current approach for echocardiographic assessment of diastolic dysfunction in children⁵. Accordingly, monitoring for LVDD in pediatric CKD is not routinely performed. Assessment of left atrial structure and function could provide a new approach to overcome the challenges characterizing LVDD in youth with CKD.

The left atrium plays an important role in cardiovascular function, and is sensitive to changes in ventricular filling pressures⁶. Several echocardiographic parameters are used to measure left atrial structure and function⁷. Left atrial volume index is a body surface area (BSA)-normalized measurement of atrial volume and is elevated in adults and children with heart failure and elevated left atrial pressure^{8, 9}. Assessment of left atrial function using strain imaging has recently gained interest as a reproducible measure that is strongly associated with abnormal diastolic function and elevated ventricular filling pressures¹⁰. Left atrial function can be divided into 3 parts- reservoir function, conduit function and atrial contractile function, each of which can be measured using strain analysis (Figure 1)¹⁰. Of the three strain measures, left atrial reservoir strain (LASr) is most validated in studies of adults. LASr, has been found to change at the earliest stages of subclinical myocardial disease and is strongly associated with heart failure and cardiovascular mortality^{4, 11}.

Studies indicate that adults with CKD have decreased left atrial function, and this is associated with adverse cardiovascular outcomes⁴. Similar studies in pediatric CKD populations are limited. A recent study by Sharma et. al. showed that left atrial mechanics, including LASr, were significantly different in youth with end stage kidney disease (ESKD) on dialysis compared to healthy controls¹². However, it remains unknown whether left atrial function is affected at earlier stages of CKD in youth. Without this data, youth with mild to moderate CKD may be at risk for having overlooked evidence of clinically-relevant myocardial dysfunction. This study aimed to describe measures of left atrial mechanics in youth with CKD and healthy, age-matched controls.

Study Population:

This analysis is a retrospective, observational analysis of youth with CKD and age-matched healthy controls. To identify CKD patients, we performed a query of the electronic health record at our institution to generate a list of patients aged 12-21years of age with a diagnosis of CKD Stage 3a-4 who had received an echocardiogram as part of routine care. Exclusion criteria included: history of kidney transplant, current requirement for dialysis, congenital or acquired heart disease, and/or lack of suitable echocardiographic images for interpretation due to limited image acquisition or insufficient image. A total of 4 patients with CKD who met clinical criteria were excluded due to poor image quality. The date range (1/1/2022 to 6/1/2023) for data collection was set to ensure all echocardiograms were collected using the same equipment and software. Echocardiograms for healthy, similarly-age and sized persons were selected from a research repository of children with structurally normal hearts who underwent echocardiogram to evaluate murmur, family history of congenital heart disease, non-cardiac syncope, or chest pain that was determined to be non-cardiac in origin. Healthy controls were selected using the same age-range as CKD patients. This study was approved by the Institutional Review Board at the Ann & Robert H. Lurie Children’s Hospital of Chicago with a waiver of informed consent (IRB#2023-5809).

Covariables:

Basic demographics, clinical measurements, and laboratory results were extracted from the electronic health record. All individuals had their height, weight, blood pressure, and heart rate measured prior to the echocardiogram. The median absolute time between laboratory value measurement and echocardiography was 13.2 days. Laboratory values were not available for control patients. Blood pressure was measured in clinic as part of routine care using automated oscillometric device. We used the combined CKiD-U25 creatinine/cystatin-c equation to calculate the estimated glomerular filtration rate (eGFR) for all participants with CKD¹³. Data to calculate the urine protein to creatinine ratio (UPC) was only available in 23 participants with CKD.

Echocardiography:

Echocardiograms were performed on GE Vivid E95 or Philips EPIQ CVx ultrasound systems. Measurements from the clinical report were reviewed for accuracy and missing measurements were performed offline. Standard measures of left ventricular mass and diastolic function were collected including mitral valve inflow E and A wave velocities and early tissue Doppler velocities (E’) of the ventricular septum and left ventricular (LV) lateral wall were measured the mitral inflow E/A ratio and E/E’ ratios were calculated. Left atrial (LA) volume was measured using the modified biplane method from apical 4 chamber and apical 2 chamber views at end systole, excluding the pulmonary veins and atrial appendage according to American Society of Echocardiography guidelines¹⁴. LA volume was indexed to BSA (LAVi). Left Ventricular Mass Index (LVMI) was calculated by indexing left ventricular mass to body surface area (BSA, mass divided by height raised to a power of 2.7)¹⁵.

Strain Imaging

Left atrial strain measurements were post-processed using TomTec Imaging using the QRS complex as the reference point. Reservoir (LASr), conduit (LAScd) and contractile (LASct) portions of LA strain were measured using automated tracking and reviewed for accuracy. The cardiac cycle with best visualization of the LA throughout the cardiac cycle was used. Areas of poor tracking were manually adjusted.

Statistical Analysis:

Patient characteristics were reported as mean and standard deviation or median and interquartile range for normally and non-normally distributed data, respectively. Echocardiographic measurements were compared between those with and without CKD using student’s t-test. Pearson correlations were used to assess the correlation between LASr, LAVI, E/A, E/e’, and LVMI. In CKD participants only, Pearson correlations were also used to test the correlation between LASr with eGFR, parathyroid hormone (PTH), serum hemoglobin (Hgb), and clinic systolic blood pressure (SBP). A p-value of 0.05 was used to define statistical significance in all analyses. Inter- and intra-reader interclass correlation (ICC) was calculated using interclass correlation on a subset of 16 patients. All statistics were performed using R, version 3.6.2 (R Core Team, 2019).

In total, this analysis included 37 patients with Stage 3-4 CKD and 19 healthy, age-matched controls. Baseline characteristics are presented in Table 1. Mean age was similar between those with CKD (15.6 ±2.2years) and without CKD (15.7 ±2.0years). Patients with CKD had higher mean SBP (125mmHg vs. 114mmHg) and slightly higher BMI (25.9kg/m² vs. 22.0kg/m²). There was a male-sex predominance in both groups. Laboratory data was only available for individuals with CKD. Within this group, the mean eGFR was 32mL/min/1.73m².

Left Atrial Parameters

Left atrial parameters are described in Table 2 and Figure 2. LASr was significantly lower in persons with CKD compared to healthy controls (43 ±8.5 vs. 47.4 ±6.1; p=0.050). While LAS conduit was diminished in CKD, this difference was not statistically significant (p=0.057). LAS contractile was similar between those with and without CKD (p=0.657). Intra- and inter-reader ICC for LASr was 0.89 and 0.83, respectively.

Left Atrial Function and Clinical measures in CKD

In youth with CKD, there was no correlation between eGFR and LASr (Figure 3, R=0.040, p=0.814). Similarly, there was no correlation between PTH (p=0.981), Hgb (p=0.440), or SBP (p=0.945). Additionally, SBP was not correlated with LASr in the complete cohort including healthy controls (R=-0.119, p=0.381).

Left Ventricular Parameters

LVMI was significantly higher in youth with CKD compared to controls (Figure 2 and Table 2, 37.2 ±10.0g/m^2.7vs 30.0 ±5.2g/m^2.7, p<0.005). Individuals with CKD also had a significantly lower E/A (1.75 ±0.5 vs. 2.4 ±0.6, p<0.001) and average E. E/e’ was slightly higher in youth with CKD compared to controls, but the difference was not statistically significant (p=0.056).

Correlation between atrial and ventricular parameters

Figure 4 contains the correlation matrices between echocardiographic parameters including all individuals. LASr was significantly correlated with LAS_conduit (R=-0.79, p<0.001) and LAS_contractile(R=-0.49, p<0.001). However, LASr was not significantly correlated with any other echocardiographic parameter, including E/A (p=0.239), E/e’ (p=0.335), or LVMI (p=0.234). Considering ventricular functional measures, E/A was significantly correlated with E/e’ (R=-0.48, p=0.002). Both E/e’ and E/A were significantly correlated with LVMI.

Our analysis found that left atrial strain, notably LASr, was significantly lower in youth with stage 3–4 CKD compared to similarly aged, healthy controls. This observation is consistent with findings in adults with CKD. LASr may provide unique insights into myocardial dysfunction as it poorly correlated with more traditionally measured parameters such as LVMI and E/e’. Secondary analyses in the subset of individuals with CKD did not identify any clinical determinants of lower LASr. In sum, these results support future studies into the determinants and clinical significance of LASr in youth with CKD.

Our findings are consistent with studies in adults with CKD that found left atrial strain, including LASr, are significantly lower in adults with CKD compared to similarly aged controls^{16, 17}. The prevalence of reduced left atrial strain begins to increase at the early stages of CKD in adults, and continues to rise at more advanced stages and ESKD¹⁸. In addition to the high prevalence of abnormal left atrial strain in adults with CKD, studies have revealed the clinical and prognostic utility of left atrial strain within CKD populations^{4, 19, 20}. LASr was found to be the most accurate echocardiographic predictor of exercise intolerance in a study of adults with CKD¹⁹. Furthermore, compared to left ventricular global longitudinal strain, E/e’ ratio, and LA volume, LASr was a stronger predictor of patients at risk for a composite cardiovascular outcome and death⁴. These results mirror the extensive body of literature in adult populations with heart failure, for whom LASr. Findings in adult CKD populations add to the extensive literature in adults with primary heart failure^{10, 11, 21}. In sum, left atrial strain is gaining traction as an important functional biomarker and being used to aid in diagnosis and treatment of adults with and without CKD. The prognostic significance of LASr in pediatric populations remains to be settled.

Beyond providing insight into cardiovascular risk, LASr may serve as a useful indicator of subclinical myocardial dysfunction. This is especially true in regard to LVDD- which is common in patients with CKD and is closely linked to incident heart failure²². In studies of adults undergoing catheterization for intracardiac hemodynamics, LASr was the most accurate echocardiographic predictor of elevated end diastolic pressure and diastolic dysfunction^{23, 24}. In addition to being an accurate indicator of diastolic dysfunction, LASr may also be the earliest functional change identifiable on echocardiogram in patients with subclinical LVDD^{11, 25}. Identifying patients with subclinical diastolic dysfunction is important for several reasons. These patients are at elevated risk for progression to symptomatic heart failure^{23, 26}. Additionally, subclinical diastolic dysfunction may indicate a still reversible stage of myocardial disease^{27, 28}.

Identifying diastolic dysfunction in youth with CKD presents an even greater challenge. Many of the commonly used markers of diastolic dysfunction, such as the mitral inflow velocities (E/e’, E/A), are poorly correlated with invasive measures of diastolic dysfunction^{5, 29}. More research is needed to see if LASr could perform equally well in children with CKD as in adults for indicating the presence of diastolic dysfunction. While our findings are inadequate to comment on the association between LASr and diastolic dysfunction, we did observe that similar to adults, LASr was poorly correlated with E/e’ and E/A³⁰. Taken as a whole, LASr may provide a unique insight into myocardial function in youth with CKD, and this should be explored in future studies.

Our findings add to the growing volume of research into left atrial function in pediatric populations. Reduced left atrial strain has been observed in a wide range of pediatric disease populations, including those with diabetes, hypertension, and cardiomyopathy^31–33. A recent study of 29 children receiving hemodialysis and 13 healthy controls demonstrated a similar pattern of reduced left atrial strain in dialysis patients and found that FGF-23 was associated with reduced left atrial strain¹². FGF-23 is associated with myocardial remodeling and stiffening³⁴. Therefore, it is plausible that patients with higher FGF-23 would be more likely to have diastolic dysfunction and associated reduced left atrial strain. While we did not have data on FGF-23, we did not observe an association between serum PTH and phosphorus with LASr. This may be due to fact that many of our subjects only had mild hyperphosphatemia and/or hyperparathyroidism. Another possible explanation is that mineral bone disease is not the primary driver of abnormal left atrial dysfunction in CKD. Overall, more research is needed into the mechanisms underlying reduced atrial function in youth with CKD. Identification of targetable mechanisms may inform medical therapies most likely to slow or reverse myocardial disease at the earliest stages.

One practical takeaway from our study was that atrial function was measurable in the majority of echocardiograms collected as part of routine CKD care. Moreover, the intra- and inter-observer correlation was strong. These findings suggest that left atrial mechanics are feasible to incorporate in future studies, and potentially clinical care, of pediatric CKD. Establishing strong collaborations between pediatric cardiologists and nephrologists will be essential to future efforts to study left atrial structure and function in pediatric kidney disease.

This study comes with inherent strengths and weaknesses. Several factors contributed strengths to our findings. We reduced variability by only including echocardiograms collected and analyzed using the same clinical software and read by a single, experienced pediatric cardiologist. We also benefited from the repository of healthy-control echocardiograms to allow for comparisons between CKD and non-CKD populations. However, there were several notable limitations to our results. We did not have laboratory data in the healthy control patients. Additionally, there was a male predominance in our study cohort. The reasons underlying this are unknown and future prospective studies should ensure to recruit both sexes equally. Due to the small sample size, we had limited power to detect significant clinical determinants of LASr in CKD, and this analysis must be followed up with larger studies. Lastly, there are no widely established normative values for left atrial strain, or other measures of diastolic dysfunction, in pediatric populations.

In conclusion, this analysis demonstrates that mean LASr in a population of youth with stage 3–4 CKD is significantly lower than in healthy controls. This finding is consistent with the adult CKD literature, and with a recent study of pediatric patients with ESKD. Left atrial mechanics were readily measurable in the majority of echocardiograms obtained as part of routine CKD care. Our results support future studies into the clinical significance and determinants of abnormal left atrial function, especially since decreased LASr may be one of the earliest identifiable echocardiographic changes on the disease spectrum ending with symptomatic heart failure.

Conflicts of Interest: All authors have nothing to disclose

Acknowledgements

This study was funded in part by NIH/NIDDK K23DK138313. All authors have nothing to disclose.

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Table 1: Participant Characteristics

	Healthy Controls	CKD Patients
	N=19	N=37	p-value
Demographics
Age, years	15.7 (2.0)	15.6 (2.2)	0.917
Male Sex, n (%)	12 (63)	23 (62)	1.000
Body Measures
Height, cm	170 (10.0)	158 (12.4)	0.001
Weight, Kg	63.8 (12.0)	66.4 (26.9)	0.685
BSA, m²	1.73 (0.21)	1.69 (0.39)	0.639
BMI, kg/m²	22.0 (3.2)	25.9 (8.5)	0.058
SBP, mmHg	114 (7.6)	125 (12.6)	0.001
DBP, mmHg	69 (7.1)	78 (10.7)	0.002
Laboratory
Creatinine, mg/dl		3.3 (2.7)
eGFR, mL/min/1.73m²		31.5 (13.8)
Bicarbonate, mEq/L		21.4 (2.8)
Phosphorus, mg/dl		4.6 (1.2)
PTH, pg/mL		114 [68, 202]
Hemoglobin, g/dl		12.1 (1.6)
UPC, g/g		1.3 [0.5, 2.3]

All values represent mean (standard deviation) or median [interquartile range]. BSA: body surface area, BMI: body mass index, SBP: systolic blood pressure, DBP: diastolic blood pressure, eGFR: estimated glomerular filtration rate, PTH: parathyroid hormone, UPC: urine protein to creatinine ratio, Ace-I: angiotensin converting enzyme inhibitors, ARB: angiotensin receptor blockers, CCB: calcium channel blockers

Table 2: Echocardiographic Parameters

	Healthy Controls	CKD Patients
	N=19	N=37	p-value
LASr, (%)	47.44 (6.06)	43.04 (8.51)	0.050
LAS_conduit, (%)	-36.19 (6.38)	-32.41 (7.14)	0.057
LAS_contractile, (%)	-11.23 (3.66)	-10.62 (5.70)	0.671
LAVI, mL/m²	21.89 (5.25)	22.92 (9.39)	0.730
E/A ratio	2.40 (0.58)	1.75 (0.50)	<0.001
E/e’ ratio	5.86 (1.07)	6.50 (1.18)	0.056
Average E’	0.16 (0.02)	0.14 (0.03)	0.008
LVMI, g/height^2.7	29.99 (5.17)	37.21 (9.98)	0.005

All values represent Mean (Standard Deviation). LASr: left atrial reservoir strain, LAS_conduit: left atrial conduit strain, LAS_contractile: left atrial contractile strain, LAVi: left atrial volume index, LVMI: left ventricular mass index (Khoury)

Left Atrial Mechanics in Youth with Chronic Kidney Disease and Similarly Aged Healthy-Controls

Status:

Version 1

Abstract

Figures

Introduction

Methods

Results

Discussion

Declarations

References

Tables

Status:

Version 1