4D automatic left atrial quantification technology—recommended for evaluating the impact of peritoneal dialysis on the left atrium of chronic kidney disease stage 5 patients

Introduction

Global age-standardized disability-adjusted life years (DALYs) rates show that overall global health has improved significantly between 1990 and 2019, but DALYs rates for chronic kidney disease (CKD) are still increasing (1). In end-stage kidney disease (ESKD), dialysis and kidney transplantation are the only available treatment options other than palliative care (2). A predominance of patients have received dialysis treatment for many years (2). Different from hemodialysis, which implies a large extracorporeal circuit, peritoneal dialysis (PD) has the advantages of low invasiveness and cost, and has become the preferred dialysis method (3,4). None of the current therapies used to treat CKD (including PD) can directly protect the heart of patients with CKD. Therefore, cardiovascular disease is a common complication in late stage of dialysis patients with uremia, and cardiogenic death occurs in 60% of dialysis patients (5-7). Left atrial (LA) remodeling is an independent risk factor for cardiovascular disease, and LA strain changes earlier than ejection fraction (8). Early detection of changes in LA structure and function in PD patients may be helpful for clinical evaluation of efficacy and early intervention treatment, and reduce patient mortality.

In the past, ultrasound techniques used to detect LA structure and function mainly included transthoracic echocardiography (TTE), two-dimensional speckle tracking echocardiography (2D-STE), three-dimensional speckle tracking echocardiography (3D-STE), transesophageal echocardiography (TEE), and tissue velocity echocardiography (TVE) were performed. However, these techniques have limitations. When TTE is combined with M-mode echocardiography to measure left ventricular (LV) size, only one dimension of LA is considered, and there is geometric asymmetry in the LA. When the LV is enlarged, M-mode echocardiography may underestimate the size of the LA (9,10). 2D-STE underestimated the volume of LA due to the planar pattern of cardiac motion and the difficulty in accurately evaluating the spot of shortened view space plane of myocardial deformation. 3D-STE is affected by the image quality of one or more segments and has limitations in time and spatial resolution. In addition, due to the need for a relatively constant R-R interval, the results of 3D echocardiography in patients with atrial fibrillation should not be overestimated (10-14). The disadvantage of TEE is that the probe is very close to the LA, and the position of the esophagus and posterior LA is variable, so it is difficult to measure LA size comprehensively with TEE (10). TVE can reflect atrial electrophysiological activities, but it cannot simultaneously record the electromechanical functions of all atrial walls in one heartbeat through TVE, which is a source of error (10,15).

The four-dimensional (4D) automatic LA quantitative technique is a new imaging technique, which breaks through the limitations of traditional imaging methods and can comprehensively and accurately evaluate the changes of LA (8). The purpose of this study was to evaluate the changes of LA volume and strain in CKD stage 5 (CKD-5) patients treated with PD by using 4D automatic left atrial quantitative technology (4D-LAQ), and to explore the independent related factors of LA function, so as to provide meaningful imaging data for clinical treatment of patients. We present this article in accordance with the STROBE reporting checklist (available at https://qims.amegroups.com/article/view/10.21037/qims-2025-392/rc).

Methods

Study design and population

This was a retrospective cohort study. A total of 109 patients with CKD-5 who visited our hospital consecutively from October 2021 to December 2024 were enrolled in the study. The inclusion criteria were as follows: (I) estimated glomerular filtration rate (eGFR) <15 mL/min/1.73 m² (16), and structural or functional renal dysfunction persisting for more than 3 months; (II) left ventricular ejection fraction (LVEF) >50%. The exclusion criteria were as follows: (I) poor image quality; (II) congenital heart diseases: atrial septal defect, ventricular septal defect, patent ductus arteriosus, tetralogy of Fallot, and so on; (III) severe valvular heart disease (17): moderate to severe valve stenosis or regurgitation caused by various reasons as described in the European Society of Cardiology/European Association for Cardio-Thoracic Surgery (ESC/EACTS) guidelines for the management of valvular heart disease; (IV) severe arrhythmias: atrial fibrillation, atrial flutter, ventricular fibrillation, ventricular flutter, third-degree atrioventricular block, and so on; (V) other heart diseases: dilated heart disease, hypertrophic heart disease, pulmonary heart disease, coronary heart disease, myocarditis, and so on; (VI) kidney transplantation; (VII) those who are unable to sign the informed consent voluntarily due to mental disorders; (VIII) initiation of hemodialysis during the course of the study. A total of 16 patients were excluded based on the above criteria. The primary reasons for exclusion included severe valvular disease (n=7), initiation of hemodialysis (n=4), atrial fibrillation (n=3), and kidney transplantation (n=2). Additionally, 38 healthy volunteers were recruited as the control group (N-group, n=38). Healthy control volunteers were recruited through advertisements posted on community and hospital bulletin boards. To ensure the health conditions of these volunteers, all volunteers completed a detailed health questionnaire to rule out a history of major chronic diseases. Eligible individuals then underwent a physical examination and a set of baseline laboratory tests, including assessment of blood pressure, electrocardiogram, renal function [creatinine (Cr), blood urea nitrogen (BUN), eGFR], cardiac biomarkers [N-terminal pro-B-type natriuretic peptide (NT-proBNP)], and lipid profile. Final inclusion was contingent upon the absence of clinically significant abnormalities at all screening stages. The specific research process is shown in Figure 1.

Figure 1 Study design flowchart. 4D-LAQ, four-dimensional automatic left atrial quantitative technology; CKD, chronic kidney disease; N, normal; N-PD, without peritoneal dialysis; PD, peritoneal dialysis; ROC, receiver operating characteristic.

The study was conducted in accordance with the Declaration of Helsinki and its subsequent amendments and was approved by the Medical Ethics Committee of The Second Affiliated Hospital of Hainan Medical University (approval no. 2024-KCSN-16). All participants provided written informed consent.

Clinical features

We collected demographic and anthropometric data, including age, sex, body mass index (BMI), body surface area (BSA), systolic blood pressure (SBP), and diastolic blood pressure (DBP). Laboratory parameters—Cr, BUN, NT-proBNP, eGFR, total cholesterol, and triglycerides—were measured from blood samples drawn within two weeks before the ultrasound. We also documented relevant clinical history (e.g., anemia, hypertension, diabetes, primary hyperparathyroidism) and current use of medications such as beta-blockers, renin-angiotensin-aldosterone system (RAAS) inhibitors, alpha-receptor antagonists, and calcium channel blockers (CCBs).

Instruments and methods

Instruments

GE Vivid E95 color Doppler ultrasonography M5Sc (frequency 1.4–4.6 MHz) probe and 4Vc probe (frequency 1.5–4.0 MHz) (GE HealthCare, Chicago, IL, USA).

2D and Doppler assessments

Left atrial diameter (LAD), left ventricular systole (LVS), left ventricular end-diastolic dimension (LVEDD), and left ventricular posterior wall thickness (LVPWT) were obtained from the parasternal long axial section of the left ventricle after the participants had been instructed to rest for 5 minutes before examination and were measured by modified biplane Simpson method (LVEF). The peak blood flow velocity in early (E) and late (A) diastole was obtained at the mitral valve orifice by turning on the pulse Doppler function. Tissue Doppler was turned on to obtain the early diastolic velocity (e') at the mitral ring interval angle. Ultimately, by combining these measurement values, the E/A ratio and the E/e' ratio are calculated for use in assessing diastolic function.

4D auto LAQ assessments

Complete information about the left atrium was obtained in the apical four-chamber view, during which the patient was asked to hold their breath to collect dynamic images. The volume frame rate was adjusted to more than 40% of the participants’ heart rate.

In the EchoPAC PC 203 workstation (GE HealthCare), the stored dynamic image was imported, the system software was used to automatically wrap the inner membrane of LA, and it was adjusted manually if necessary to obtain satisfactory data of the region of interest. The result was clicked to obtain the 4D LA parameters—left atrial minimum volume (LAVmin), maximum left atrial volume (LAVmax), left atrial pre-atrial contraction volume (LAVpreA), left atrial maximum volume index (LAVImax), left atrial ejection volume (LAEV), left atrial ejection fraction (LAEF), left atrial reservoir longitudinal strain (LASr), left atrial conduit longitudinal strain (LAScd), left atrial contraction longitudinal strain (LASct), left atrial reservoir circumferential strain (LASr-c), left atrial conduit circumferential strain (LAScd-c), left atrial contraction circumferential strain (LASct-c), left atrial active ejection fraction (LAAEF), and left atrial passive ejection fraction (LAPEF). LAAEF and LAPEF are calculated as follows: LAAEF = (LAVpreA − LAVmin)/LAVpreA × 100%; LAPEF = (LAVmax − LAVpreA)/LAVmax × 100% (Figure 2).

Figure 2 LA parameters of 4D-LAQ. (A) Left atrial circumferential strain of the N group. (B) Left atrial circumferential strain of the N-PD group. (C) Left atrial circumferential strain of the PD group. The green circles, the regions of interest outlined by the system or manually. 2ch, two-chamber view; 4ch, four-chamber view; 4D-LAQ, four-dimensional automatic left atrial quantitative technology; ED, end-diastolic; ES, end-systolic; LAEF, left atrial ejection fraction; LAEV, left atrial ejection volume; LAScd, left atrial conduit longitudinal strain; LAScd_c, left atrial conduit circumferential strain; LASct, left atrial contraction longitudinal strain; LASct_c, left atrial contraction circumferential strain; LASr, left atrial reservoir longitudinal strain; LASr_c, left atrial reservoir circumferential strain; LAVmax, left atrial maximum volume; LAVmin, left atrial minimum volume; LAVImax, left atrial maximum volume index; LAVpreA, left atrial pre-atrial contraction volume; N, normal; N-PD, without peritoneal dialysis; PD, peritoneal dialysis; PreA, pre-atrial contraction; SAX, short-axis view.

All of the above images were taken by the same ultrasonographer with more than five years of experience in diagnosis. The data was repeated three times by two other experienced doctors, with the average taken as the final result.

Statistical analysis

The statistical software SPSS 27.0 (IBM Corp., Armonk, NY, USA) was employed for data analysis. Normally distributed continuous variables were presented as means and standard deviations, whereas non-normally distributed variables are expressed as medians with interquartile ranges. For normally distributed continuous data with homogeneity of variance, comparisons among three groups were conducted using one-way analysis of variance (ANOVA); pairwise comparisons between two groups utilized independent samples t-test. In cases where the assumption of homogeneity of variance was violated or normality was not met, the Kruskal-Wallis test was applied for comparisons among three groups, and the Wilcoxon rank-sum test was used for two-group comparisons. For categorical variables, differences between two groups were assessed using Chi-squared (χ²) tests or Fishe’s exact test, with results reported as frequencies. A binary logistic regression model was established to identify relevant risk factors. The diagnostic efficacy of the 4D-LA parameter in identifying myocardial injury was evaluated using receiver operating characteristic (ROC) curve analysis. To comprehensively evaluate the reliability of the 4D-LAQ parameters, 15 participants were randomly selected. Each participant underwent two independent 4D-LAQ scans during a single visit to assess scan-rescan reproducibility. All images from both scans were independently analyzed by two observers to determine inter-observer variability. Subsequently, one observer repeated the analysis of all images after an interval of several days to assess intra-observer variability. This protocol allowed for the simultaneous evaluation of scan-rescan reproducibility, intra-observer consistency, and inter-observer consistency. The intraclass correlation coefficient (ICC) served to assess both inter-observer and intra-observer reliability. An ICC value equal to or greater than 0.75 indicated “good” reliability; values ranging from 0.41 to 0.75 indicated “moderate” reliability; and values below 0.40 suggested “poor” reliability. A p value less than 0.05 denoted statistical significance.

Results

Clinical and laboratory characteristics

This study included a total of 109 patients in the CK5 stage (N-PD group: 48 patients, aged 30–70 years; PD group: 61 patients, aged 20–76 years) and 38 healthy volunteers. Compared to healthy volunteers, CK5 patients exhibited significantly elevated levels of SBP, DBP, Cr, BUN, and NT-proBNP, along with a marked decrease in eGFR. These differences were statistically significant (P<0.05). Furthermore, when comparing the N-PD group to the PD group, there was a notable increase in Cr and eGFR in the PD group alongside a significant reduction in BUN; these differences also reached statistical significance (P<0.05). The N-PD group had a higher average age compared to the other two groups, which was statistically significant (P<0.05). No statistically significant differences were observed among the three groups regarding gender, BSA, BMI, total cholesterol, triglyceride, anemia status, hypertension prevalence, diabetes incidence, primary hyperparathyroidism presence, β-Rb levels, α-RA levels, RAAS activity, or CCB usage, as shown in Table 1.

Echocardiographic parameters

Compared to the normal group, patients in the CK5 phase exhibited significantly increased values for LAD, interventricular septum (IVS), LVEDD, LVPWT, and E/e'. Conversely, e' and E/A were found to be decreased, with all differences reaching statistical significance (P<0.05). No statistically significant differences were observed between the N-PD group and PD group regarding LAD, LVS, LVEDD, LVPWT, e', E/A, or E/e'. When comparing the three groups, no statistically significant differences were noted for LVEF or peak E (Table 2).

4D-LAQ parameters

Compared with the normal group, LAVmax, LAVpreA, LAVImax, and LAEV were significantly increased in two groups of CKD-5 patients, and the differences were statistically significant (P<0.05). Compared with N-PD group, the absolute value of LASr-c% in PD group was significantly increased, whereas LAVmin, LAVmax, LAVpreA, LAVImax, and LAEV were significantly decreased, with statistical significance (P<0.05). In addition, compared with the normal group, LAVmin in the N-PD group was significantly increased, and the absolute values of LASr-c% and LASct-c% in the PD group were significantly increased, with statistical significance (P<0.05). There was no significant difference in other variables between groups (P<0.05) (Table 3).

Establishment of multivariate analysis and risk prediction model

According to whether the patients had adverse cardiovascular events (defined as coronary atherosclerosis, hypertensive heart disease, new atrial fibrillation, progressive heart failure, etc.), the PD group was divided into the Event group and the N-Event group. Chi-squared test, independent sample t-test, and Wilcoxon rank sum test (Table S1) were used to screen the general clinical data of patients including gender, edema, cerebral infarction, hypertension, diabetes, carotid plaque, anemia, hyperparathyroidism, New York Heart Association (NYHA) heart function classification ≥ II, E/e' ≥14), and 4D-LAQ individual indicators (including LAVmin, LAVmax, LAVpreA, LAVImax, LAEV, LAEF, LASr%, LAScd%, LASct%, LASr-c%, LAScd-c%, LASct-c%). After the screening, edema, hypertension, NYHA heart function classification ≥ II, E/e' ≥14, LAVmin, LAVmax, LAVpreA, LAVImax, LAEV, LASct-c% were statistically different between the two groups. Therefore, these factors could be included in the binary logistic regression model. It is suggested that LAVImax, NYHA heart function classification ≥ II, and E/e' ≥14 are independent risk factors for adverse cardiovascular events in PD patients, as shown in Table 4. According to the above table, the regression formula of risk score for PD patients according to whether adverse cardiovascular events occur is as follows:

Logit (P) = −9.751 + 0.5 × LAVImax + 5.575 × n (if NYHA heart function classification ≥ II, n=1; otherwise n=0) + 4.854 × n (if E/e' ≥14, n=1; otherwise n=0).

ROC curve analysis

An analysis of the ROC curve was performed for the above PD patients. There were statistically significant differences in LAVImax, NYHA heart function classification ≥ II, and E/e' ≥14 between the Event group and the N-Event group, and the areas under the curve (AUC) were 0.830, 0.779, and 0.717, respectively. LAVImax, NYHA heart function classification ≥ II, and E/e' ≥14 were combined, and the AUC was Pre 1 =0.968, which was statistically significant. ROC analysis of LAVImax showed that the optimal cut-off value was ≥27.5 (mL/m²), the specificity was 82.1%, and the sensitivity was 78.1%. ROC analysis of NYHA heart function classification ≥ II showed that the specificity was 96.4% and the sensitivity was 59.4%. ROC analysis of E/e' ≥14 showed that the specificity was 96.4% and the sensitivity was 46.9%. ROC analysis of Pre 1 showed that the optimal cut-off value was ≥0.37, the specificity was 89.3%, and the sensitivity was 88%. Pre 1 had the highest efficiency in identifying adverse cardiovascular events, as shown in Figure 3.

Figure 3 Receiver operating characteristic curve analysis for the accuracy of LAVImax, NYHA heart function classification ≥ II, and E/e' ≥14 in identifying peritoneal dialysis patients with adverse cardiovascular events (N=61). E, the peak transmitral flow velocity in early diastole; e', peak early diastolic of myocardial; LAVImax, left atrial maximum volume index; NYHA, New York Heart Association.

Intra- and inter-observer variability

The intra-observer intra-group correlation coefficients (ICCs) of LAVmin, LAVmax, LAVpreA, LAVImax, LAEV, LAEF, LASr, LAScd, LASct, LASR-c, LAScd-c, and LASct-c were, respectively, 0.949, 0.935, 0.972, 0.973, 0878, 0.911, 0954, 0.861, 0.752, 0.885, 0.890, and 0.786, The inter-observer ICC values of 0.934, 0.930, 0.985, 0.972, 0.780, 0.815, 0.915, 0.799, 0.767, 0.915, 0.886, and 0.811, respectively, indicate that LA strain measurement has good intra- and inter-observer consistency (Table 5).

Discussion

In this study, the 4D-LAQ technique was used to evaluate the effect of abdominal dialysis on LA volume and function in patients with CKD-5. The main findings are as follows: (I) routine echocardiography showed no significant difference in the difference of cardiac volume and strain between N-PD group and PD group. (II) Compared with the N-PD group, PD-group LAVmin, LAVmax, LAVpreA, LAVImax, and LAEV all decreased, whereas LASr-c value increased. In addition, compared with the N group, LAVmax, LAVpreA, LAVImax, and LAEV of the N-PD and PD groups were increased, and the absolute values of LASr-c% and LASct-c% of PD-group were increased. (III) LAVImax, NYHA heart function classification ≥ II, and E/e' ≥14 were independent risk factors for adverse cardiovascular events in the PD-group, and LAVImax was more effective in diagnosing individual factors. These conclusions show that the 4D-LAQ technique is more sensitive to detect LA function in patients with uremia treated with PD, and can be used to predict the occurrence of adverse cardiovascular events.

In this study, compared with the normal group, Cr and BUN levels were significantly elevated, whereas eGFR was markedly reduced in both groups of CKD5 patients. Notably, BUN and Cr levels were lower, and eGFR was higher in the PD group compared to the N-PD group. This is attributed to the prolonged biological activity of water-soluble small molecules such as BUN during the pre-dialysis phase before reaching ESKD, which are traditionally used as markers for adequate uremic toxin removal during dialysis (18). Consequently, BUN levels decrease post-PD in ESKD patients, consistent with our findings. Additionally, Cr levels increased in PD patients, possibly due to dietary restrictions being lifted post-dialysis, leading to increased Cr production. Cardiac hypertrophy, a hallmark of uremic cardiomyopathy in CKD patients, can increase by up to 70–80% in ESKD patients (19). This condition arises from water and sodium retention, activation of the RAAS, sympathetic nervous system activation, or endothelial dysfunction due to impaired kidney function, resulting in hypertension and cardiac hypertrophy. Numerous studies have demonstrated the impact of kidney failure on the heart, with certain uremic toxins such as fibroblast growth factor 23 exhibiting direct harmful effects. For instance, indoxyl sulfate can activate RAAS and induce cardiac hypertrophy, whereas asymmetric dimethylarginine accumulation may lead to increased afterload, impaired myocardial blood flow, LV hypertrophy, and cardiac insufficiency (18-20). Echocardiographic findings revealed significant increases in LAD, IVS, LVEDD, and LVPWT in CKD-5 patients compared to the normal group, indicating LA enlargement and LV hypertrophy. Additionally, decreased E/A ratio and e' velocity, along with increased E/e' ratio, indicated impaired LV diastolic function in CKD-5 patients. Notably, no significant differences were observed between the N-PD and PD groups in these parameters, suggesting that conventional echocardiography struggles to differentiate cardiac conditions in CKD-5 patients treated with or without PD. However, 4D-LAQ technology may address this limitation.

Compared with the normal group, LAVmax, LAVpreA, LAVImax, and LAEV of CKD-5 stage two groups were significantly increased, and these values were significantly lower in the PD group than in the N-PD group. This reflects the advantage of 4D-LAQ technology, that is, it can distinguish differences that cannot be identified by conventional echocardiography. It also shows that the symptoms of LA enlargement have been significantly improved after abdominal dialysis treatment. In addition, CKD-5 patients showed an increase in LAEV. As it is well known (21), the LA is directly influenced by LV filling pressure, which is described according to the different stages: (I) during the LV contraction, blood from the pulmonary vein moves into the LA (reservoir); (II) in the early diastole, the LA as a catheter for blood to be transported from the pulmonary veins to the LV (tube); (III) in late LV diastole, LA actively contracts, further promoting LV filling (enhancement stage). Due to the decreased diastolic function of the left ventricle in CKD-5 patients, the suction to the LA during diastole is impaired, and more blood stasis is in the LA (22). This explains the LA enlargement in these patients. Similarly, the above parameters (LAVmax, LAVpreA, LAVImax, LAEV) also showed significant differences between the N-PD and PD groups, suggesting that the degree of LA enlargement was significantly reduced after PD. In previous studies (8,23,24), representation of the LA function of accumulator, catheter function, and pump function of the longitudinal index LASr, LAScd, and LASct have consistently appeared when in the thickening of the LV compliance declined. In this study, these longitudinal response variables also showed a downward trend, but did not show statistical significance, which may be related to individual differences and the small sample size. Meanwhile, the absolute values of the toroidal strain variables LASr-c (reservoir function) and LASct-c (pump function) increased in the PD group compared with the normal group and the N-PD group. In similarity with previous studies (25), there is indeed a dissociation between longitudinal and circumferential strain. Early LV system dysfunction is characterized by impaired longitudinal strain and enhanced circumferential strain (26). A similar event occurs in the atria, where the LA wall is composed of a mixed set of muscles, including circumferential and longitudinal muscle bundles. When PD causes endocardial damage, subendocardial dysfunction may promote the dominance of the epicardial helical muscle fibers, leading to greater annular pressure (25,27,28). This explains the improvement in circumferential strain in patients with PD, but the separation of circumferential and longitudinal strain is also thought to indicate subclinical atrial dysfunction (25).

The 4D-LAQ technique can also predict adverse events in patients with PD. Binary logistic regression equation showed that LAVImax, NYHA heart function classification ≥ II, and E/e' ≥14 were independent risk factors for adverse cardiovascular events in PD patients. A single factor to LAVImax has the highest AUC. Combined with LAVImax, NYHA heart function classification ≥ II, and E/e' ≥14, the AUC reached the maximum value. Therefore, 4D-LAQ technology can be used as a non-innovative indicator to evaluate adverse events in patients with ESKD after abdominal dialysis.

This study has the following limitations. (I) The study was conducted in a single center, so selection bias could not be completely avoided. (II) The sample size is small. If prospective studies with multiple centers could be included and the sample size increased, the risk prediction model may be further strengthened and improved. (iii) There are few independent risk factors included in the regression model, and other adverse cardiovascular events of the participants should be further collected to improve the model.

Conclusions

The 4D-LAQ technique can be used to evaluate the effect of PD on LA structure and function in CKD-5 patients. In CKD-5 patients after PD, the LA circumferential strain was separated from the longitudinal strain, suggesting subclinical dysfunction. The 4D-LAQ technique can be used to predict the probability of adverse cardiovascular events in CKD-5 patients after PD.

Acknowledgments

None.

Footnote

Reporting Checklist: The authors have completed the STROBE reporting checklist. Available at https://qims.amegroups.com/article/view/10.21037/qims-2025-392/rc

Data Sharing Statement: Available at https://qims.amegroups.com/article/view/10.21037/qims-2025-392/dss

Funding: This work was supported by Joint Program on Health Science & Technology Innovation of Hainan Province (No. WSJK2024MS218), and Hainan Provincial Natural Science Foundation of China (No. 822RC841).

Conflicts of Interest: All authors have completed the ICMJE uniform disclosure form (available at https://qims.amegroups.com/article/view/10.21037/qims-2025-392/coif). All authors report that this work was supported by Joint Program on Health Science & Technology Innovation of Hainan Province (No. WSJK2024MS218), and Hainan Provincial Natural Science Foundation of China (No. 822RC841). The authors have no other conflicts of interest to declare.

Ethical Statement: The authors are accountable for all aspects of the work in ensuring that questions related to the accuracy or integrity of any part of the work are appropriately investigated and resolved. The study was conducted in accordance with the Declaration of Helsinki and its subsequent amendments and was approved by the Medical Ethics Committee of The Second Affiliated Hospital of Hainan Medical University (approval No. 2024-KCSN-16). Written informed consent was obtained from each participant.

Open Access Statement: This is an Open Access article distributed in accordance with the Creative Commons Attribution-NonCommercial-NoDerivs 4.0 International License (CC BY-NC-ND 4.0), which permits the non-commercial replication and distribution of the article with the strict proviso that no changes or edits are made and the original work is properly cited (including links to both the formal publication through the relevant DOI and the license). See: https://creativecommons.org/licenses/by-nc-nd/4.0/.

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