Sinus activation originates from the sinus node and spreads anteriorly to the right atrium (RA) and subsequently to the left atrium (LA) [1]. LA activation is mediated by the Bachmann bundle, a group of muscular fibers crucial for efficient interatrial conduction [2]. This efficient conduction is essential for the proper electromechanical activation of the LA, which ensures optimal filling of the left ventricle (LV) [3, 4]. Efficient conduction through the Bachmann bundle also contributes to the correct “valvular” function of the pulmonary vein (PV) outlets. Consequently, the circular fibers around the venous openings reduce their diameter, preventing blood from flowing back and protecting the lungs against blood retention [5]. Inter-atrial and atrioventricular (AV) conduction disturbances impair mechanical AV synchrony, which is more harmful in the left heart due to higher filling pressure [6]. Interestingly, the lengthening of both P-wave duration and AV conduction often occurs sequentially as a compensatory mechanism. Uncompensated pathologies resulting in abnormal AV synchrony and suboptimal LV filling may lead to heart failure (HF), particularly in the form of HF with preserved ejection fraction (HFpEF) [7]. A specific pathology is the complete block of the Bachmann bundle (advanced interatrial block (IAB)), which results in activation through alternative pathways [8]. In the classic form of advanced IAB, the duration of the P-wave is extended, accompanied by a typical change in morphology. Abnormal electrical activation is followed by abnormal mechanical LA contraction, which is logical. The wave moves from the base towards the openings of the superior PV, which significantly impairs LV filling and may contribute to the development of HF [9].

This study aimed to evaluate the mechanical function of the LA using LA strain in patients with normal and impaired interatrial conduction, specifically focusing on contractility and retrograde flow in the upper and lower pulmonary veins. It also aimed to prove that the precise interpretation of electrocardiography (ECG) using vector graphics is complementary to LA strain assessment in terms of impaired function in IABs.

The study included 51 unselected patients (25 women, 26 men) with a mean age of 69.5 $\pm$ 13.1 years. The patients were admitted to the University Hospital in Zielona Góra with a positive SARS-CoV-2 test and related symptoms. Inclusion criteria included sinus rhythm at the time of examination. IABs were more frequently observed in COVID-19 patients; hence, these patients were included despite SARS-CoV-2 potentially being a study limitation. Exclusion criteria included heart rhythm other than stable sinus rhythm at the time of examination, moderate and severe valvular heart disease, hemoglobin 11 mg/dL, estimated glomerular filtration rate 30 mL/min/1.73 m², presence of malignancy, autoimmune disease, or thyroid illness. Six patients with persistent AF were excluded from the study -45 patients (23 males, 22 females; mean age 69.0 $\pm$ 12.9 years) eventually qualified for the study.

All participants underwent clinical evaluation, ECG, echocardiography, and blood sampling for laboratory analysis. Two independent researchers performed the examinations, unaware of each other’s results and blinded to clinical data. All study subjects were informed of the purpose and provided written informed consent. The study adhered to the Declaration of Helsinki and was approved by the local Bioethical Committee at Collegium Medicum University of Zielona Góra, Poland.

The ECG was interpreted using vector graphics at a recording speed of 200 mm/s with $\times$256 enhancement (Biomedical Instruments Co. Ltd, TeleECG-12C, Shenzen, China) (Fig. 1). Interatrial conduction disorders were defined based on the original definition published by Bayes de Luna in 1979 and further developed in 2017 [10, 11]. Advanced IAB diagnosis was performed by analyzing the 12-lead ECG. As presented in Fig. 1, patients were categorized based on P-wave morphology (especially in leads II, III, and aVF) and duration:

Group 1: Positive P-wave shape with a duration of up to 120 ms and amplitude above 0.1 mV in lead I [12].

Group 2: Partial interatrial block (P-IAB) with “long and flat” P-wave morphology characteristic of a structurally damaged atrium, with a duration exceeding 120 ms and an amplitude below 0.1 mV in lead I.

Group 3: Advanced interatrial block (A-IAB) with P-wave morphology described by Bayes de Luna as a positive and negative deflection of the P-wave (two phases) - “plus/minus” morphology and duration exceeding 120 ms [8].

Fig. 1.

An exemplary image of ECG recordings, presenting normal (A), long and flat – low voltage (B), full Bachmann bundle block (C) P-wave morphologies. The ECG recording parameters were: speed 200 mm/s, gain 80 mm/mv. The ECG leads are II, III, aVF. The P-wave durations are as follows: (A) 110 ms, (B) 130 ms, (C) 166 ms. ECG, electrocardiography.

Echocardiographic examination assessed ejection fraction (EF), mitral regurgitation (MR), LA peak global longitudinal strain in phases (reservoir [peak atrial longitudinal strain (PALS)], conduit, contraction [peak atrial contraction strain (PACS)]) using two-dimensional tissue tracking (2DTT) technology, LA regional strain (qualitative assessment focusing on the order of regional contractions), LA volume, and the pressure and speed of PV retrograde wave using FujiFilm Corporation Arietta 65. The volumes of the LV and LA were evaluated using the biplane Simpson and area-length methods, respectively. LV end-diastolic and end-systolic volumes in the apical 4- and 2-chamber views were used to calculate EF. The retrograde flow pressure in superior and inferior PV was measured with pulse wave Doppler, placing the marker approximately 1 cm inside the PV inlet. LA strains were assessed by semi-automated 2DTT speckle tracking technology by FujiFilm Corporation, analyzing all segments of LA in the apical 4- and 2-chamber views with a temporal resolution of 60 to 90 frames/s, using the onset of the QRS complex as the reference point. PALS was calculated as the peak value of longitudinal strain during LV systole. PACS was measured as the strain value at the onset of the P-wave in the ECG, and LA conduit strain was determined as the difference between PALS and PACS. The peaks of regional strain curves were set on a timeline, which helped define the LA regional contraction order. No separate quantification of regional strain values was used. The LV inflow parameters, including peak early (E) and late diastolic flow velocity (A), and deceleration time of the early diastolic flow wave (DT), were assessed from the apical 4-chamber view by pulsed-wave Doppler (Hitachi Ltd., Tokyo, Japan) with the sample volume.

The collected data were registered, processed, and analyzed using Statistica 13.3 (TIBCO Software Inc., Palo Alto, CA, USA). Statistical analyses included qualitative variables measured on nominal and ordinal scales, which were cross-tabulated. The correlation strength between pairs of variables was assessed using the Chi-square test. Fisher’s exact test was used when the expected count in at least one cell of a four-field table was below 5. In cases of quantitative variables, means (M), standard deviations (SD), medians (Me), lower quartiles (Q1), upper quartiles (Q3), and ranges (minimum and maximum) were calculated. The Shapiro-Wilk test was used to assess the normality of distribution, while homogeneity of variance was assessed using Bartlett’s and Levene’s tests. Student’s t-test was used for the significance of differences between the mean values of variables with normal distribution and homogeneous variances in two independent groups. The non-parametric Mann-Whitney U test was used to verify the significance of differences between mean values of variables with non-normal distribution or heterogeneous variances in two groups. For multiple comparisons, analysis of variance (ANOVA) or its non-parametric equivalents were used.

Regression analysis, based on the Pearson r linear correlation coefficient, was applied to determine the direction and the strength of linear correlations between two continuous variables. The least square method was used to estimate regression coefficient values. Multiple regression analysis was conducted to assess the influence of different factors on the dependent variable. In multiple regression models, regression coefficients ($\beta$) were standardized to make their values independent of the value range of the associated random variable (standardized regression coefficients $\beta$ range between –1 and +1, allowing comparison for different random variables; the higher the absolute value of the standardized regression coefficient, the stronger the variable’s impact on the dependent variable). A significance level of p = 0.05 was used for all statistical analyses. The results of the statistical analyses are included in graphs or tables.

Our primary achievement was demonstrating that the presence of IABs impair the synchrony of LA contraction, as evidenced by LA regional strain analysis. This method complements precise ECG assessment. Moreover, we identified factors directly influencing PALS and PACS.

6.3 Major Correlations in Our Study

We identified key factors influencing global LA strain, finding that PALS independently correlates with P-wave duration and HF. PALS indicates LA early diastole, suggesting that longer P-wave duration implies more impaired conduction and diastole of both LV and LA, making PALS a potential HF diagnostic variable. Parameters of IABs, P-wave measurements, LA strain, and HF correlate, providing a foundation for further research on HFpEF pathomechanisms.

Discussing HF and impaired atrial conduction, we must mention “Bayes’ Syndrome” [31, 32]. Bayes de Luna concluded that in HF patients, A-IAB predicts new-onset atrial fibrillation (AF) and ischemic stroke. Our study found strong correlations between:

(1) The presence of IABs and episodes of PAF (Table 3, p 0.001).

(2) A-IAB and decreased PALS and PACS (Table 2, p 0.001; Fig. 5, 1 vs. 2 p 0.004, 1 vs. 3 p 0.001).

(3) Decreased PALS, PACS, and HF (reduced LVEF). (Fig. 2, p 0.003).

Table 3. Number (percentage) of patients in groups differing in the P-wave morphology and the results of tests of independence.

Comorbidities	P-wave morphology			p-value
	Normal	Long and flat	Bachmann’s block
	N = 18	N = 12	N = 15
Arterial hypertension, n (%)	10 (55.6)	8 (66.7)	15 (100.0)	0.023
CKD, n (%)	1 (5.6)	0 (0.0)	1 (6.7)	0.762
HF, n (%)	2 (11.1)	3 (25.0)	4 (26.7)	0.264
IHD, n (%)	3 (16.7)	3 (25.0)	5 (33.3)	0.695
Asthma, n (%)	0 (0.0)	1 (8.3)	1 (6.7)	0.469
COPD, n (%)	3 (16.7)	1 (8.3)	2 (13.3)	0.925
Obesity, n (%)	0 (0.0)	0 (0.0)	4 (26.7)	0.038
DM2, n (%)	7 (38.9)	2 (16.7)	8 (53.3)	0.136
AFP, n (%)	0 (0.0)	2 (16.7)	4 (26.7)	0.001

CKD, chronic kidney disease; IHD, ischemic heart disease; COPD, chronic obstructive pulmonary disease; DM2, diabetes mellitus type 2; AFP, paroxysmal atrial fibrillation; HF, heart failure.

Fig. 5.

P-wave duration, age, PALS, PACS and LA volume in groups of patients with regard to P-wave morphology, and the results of tests of independence and multiple comparisons (post-hoc tests). We noted a significant difference in P-wave duration between normal conditions and P-IAB and A-IAB. No significant difference was observed between P-IAB and A-IAB. Differences in PALS and PACS were also statistically significant only between normal and abnormal P-wave morphologies. No statistical differences were present between P-IAB and A-IAB. PALS, peak atrial longitudinal strain; PACS, peak atrial contraction strain; LVEF, left ventricular ejection fraction; PV, pulmonary veins; LA volume, left atrial volume; SE, standard error; ANOVA, analysis of variance; P-IAB, partial interatrial block; A-IAB, advanced interatrial block.

Interestingly, we found no clear correlation between retrograde PV flow and IAB type. The topic seems to be scarcely explored in the literature. Reversed PV flow during atrial contraction, often discussed with regards to MR, did not correlate in our research [33, 34]. The complexity of IABs, as well as the potential subtypes warrant further study.

The primary limitation of our study was the small sample size, which restricted our ability to make precise comparisons among groups based on interatrial conduction. Another limitation is the lack of extensive clinical research on this topic, making it challenging to discuss our findings without sufficient comparative studies. However, what is worth noticing is that in 2022, Bucciarelli-Ducci et al. [40] published a review of the most relevant literature on the role of cardiovascular imaging in cardiovascular medicine about COVID-19. It emphasized that despite the limited access to hospital-based cardiovascular care, the developing imaging technology and artificial intelligence facilitated the understanding of myocardial damage caused by coronavirus. The authors presented examples connected with valvular diseases, coronary diseases, and hypertension. However, there needs to be sufficient information about the effects of COVID-19 on the cardiac conduction system, which stays within the scope of our interest.

We agree that acute COVID-19 is a significant limitation, which could have influenced the results. On the other hand, the specific group of patients provides unique data that can be compared with other groups in future studies. In his letter to the Editor, Russo Vincenzo referred to Yenercağ’s work, emphasizing that IABs may be revealed or amplified by COVID-19, which can potentially worsen the patient’s condition [41, 42]. We selected COVID-19-positive patients with this consideration in mind.

COVID-19 infection often acts as both a catalyst and a cause for IAB development. We highlight the need for further studies to establish average reference values for LA strain in normal P-waves. Pathan’s meta-analysis (2017) showed that average LA strain values in healthy P-waves differ slightly from those in our COVID-19 patients [43]. The reservoir phase values were 39% compared to our 29.97%, with no significant differences in the contraction phase (17% vs. 17.63%).

On the other hand, Nyberg et al. [44] 2023 published original research that included 1329 healthy patients. The research aimed to “establish echocardiographic reference ranges, including lower normal limits of global strains for all four cardiac chambers”. The LA reservoir strain (4ch) was, on average, 32% compared to our 29.97%. The LA contractile strain (4ch) was 15.4% vs. 17.63% respectively. However, we should pay attention to the age of the groups included in the research regarding LA strain. The mean age in our research was 69 years, and for that age, Nyberg assessed the LA reservoir strain (4ch) of 30.1% (females) and 30.6% (males), nearly equaling the 29.97% found in our study. Furthermore, the LA contraction strain was 15.8% (females) and 17.9% (males) vs. 17.63%, respectively, presenting no significant difference in our study. These comparisons attract our attention and make us ask further questions about the influence of COVID-19 on cardiac health.

The impaired function of the LA muscle associated with IABs presents a pathophysiological target for treating patients with HFpEF. Precise P-wave assessment is crucial in determining the condition of the LA.

(1) IABs negatively impact the mechanical profile of LA contraction.

(2) PALS (%) is correlated with P-wave duration (ms), LVEF (%), LA volume (ml), and the presence of MR.

(3) PACS (%) is correlated with LVEF (%), LA volume (ml), and P-wave morphology.

(4) Examining LA mechanics using regional strain complements precise electrocardiographic assessment.

(5) The influence of IABs on retrograde flow in PV is unclear, possibly due to insufficient patients with specific conduction disorders.

The datasets used and/or analyzed during the current study are available from the corresponding author on reasonable request.

JZ and JG designed the research study. JZ and BK performed the research. JZ, GZ and AS substantially participated in analysis and interpretation of data. GZ and AS provided the technical help and advice on the research. All authors have been involved in drafting the manuscript and have approved the final manuscript. All authors have participated sufficiently in the work and agreed to be accountable for all aspects of the work.

All study subjects were informed of the purpose and provided written informed consent. The study adhered to the Declaration of Helsinki and was approved by the local Bioethical Committee at Collegium Medicum University of Zielona Góra, Poland (17/153/2021).

We would like to express our deep gratitude to MIRO Company for their support in providing equipment and sharing advanced technological knowledge during this research.

This research received no external funding.

The authors declare no conflict of interest.