Long-Term Surgical Outcomes of Patients With Isomeric Right and Left Atrial Appendages

Abstract

Objectives: To compare the long-term outcomes of biventricular, univentricular, and so-called one-and-one-half ventricular repairs in patients with left and right isomerism. Methods: Surgical correction was undertaken, between 2000 and 2021, in 198 patients with right, and 233 with left isomerism. Results: The median age at operation was 24 days (interquartile range [IQR]: 18-45) and 60 days (IQR: 29-360) for those with right and left isomerism, respectively. Multidetector computed-tomographic angiocardiography demonstrated more than half of those with right isomerism had superior caval venous abnormalities, and one-third had a functionally univentricular heart. Almost four-fifths of those with left isomerism had an interrupted inferior caval vein, and one-third had complete atrioventricular septal defect. Biventricular repair was achieved in two-thirds of those with left isomerism, but under one-quarter with right isomerism (P < .001). Hazard regression for mortality revealed odds for prematurity at 5.5, pulmonary atresia at 2.81, atrioventricular septal defect with a common valvar orifice at 2.28, parachute mitral valve at 3.73, interrupted inferior caval vein at 0.53, and functionally univentricular heart with a totally anomalous pulmonary venous connection at 3.77. At a median follow-up of 124 months, the probability of survival was 87% for those with left, and 77% for those with right isomerism (P = .006). Conclusions: Multimodality imaging characterizes and delineates the relevant anatomical details, facilitating surgical management of individuals with isomeric atrial appendages. Continuing higher mortality despite surgical intervention in those with right isomerism points to the need for the reassessment of strategies for management.

Keywords

anomalous systemic venous drainage heterotaxy left isomerism right isomerism totally anomalous pulmonary venous connection univentricular heart

Introduction

It is now accepted that the extent of the pectinate muscles relative to the vestibules of the atrioventricular junctions permits the distinction of right versus left isomerism.^1–5 Individuals with these morphologies are characterized by complex intracardiac anatomies, particularly regarding the systemic and pulmonary venous connections, for which surgical corrections are commonly performed.^1–9^,E1-E5 To date, however, little emphasis has been placed on whether surgical approaches should be tailored specifically to one or other of the subsets. Studies on long-term outcomes, furthermore, are limited. With this in mind, we have assessed our own extensive experience, aiming to determine the morphological characteristics favoring functionally biventricular as opposed to univentricular repair, the need for reoperations, and the risk factors associated with mortality and morbidity.

Patients and Methods

Our retrospective study conforms to the principles outlined in the Declaration of Helsinki and was approved by the Institutional Ethics Committee. All patients were enrolled after we obtained written informed consent from themselves or their guardians.

Criterions for Selection

We included all patients identified with isomerism of the right or left atrial appendages between 2000 and 2021 undergoing surgical intervention by the corresponding author at the All India Institute of Medical Sciences, New Delhi. There were 198 patients with isomeric right atrial appendages, of whom 102 were females, and 233 with isomeric left appendages, 154 being females. The records were reviewed to establish demographic, operative, and perioperative features. Suspicion of the presence of isomeric appendages was raised when abdominal heterotaxy, or isomeric bronchial patterns, had been seen on plain x-ray films of the chest and abdomen. E6,E7 The final diagnosis, however, was made intraoperatively according to the extent of the pectinate muscles with the atrial appendages relative to the atrial vestibules.^3,4^,E8-E10 Cardiac catheterization and angiocardiography had been performed in 297 patients. Since 2007, we have used computed tomographic angiography routinely to delineate the anatomic details. To identify risk factors for mortality, we assessed birth weight and length of gestation, cyanosis and prostaglandin dependence at presentation, specific intracardiac lesions, presence of extracardiac lesions, age at first surgical intervention, and types of interventions performed. The demographic and clinical profiles are summarized in Tables E1-E3. All preoperative studies had been performed within 15 days before surgery.

Statistical Analysis

Statistical analysis was performed using STATA 16.0 software (Stata Corp). Independent variables were expressed as mean plus or minus standard deviations, or median values with the interquartile range. Categorical variables were expressed as absolute number and percentages and analyzed using the χ² test or Fisher exact test. Quantitative variables were analyzed using Student t test or the Wilcoxon-rank sum test. Mortality rates were calculated depending on the total number of years of follow-up. The survival probability with 95% confidence intervals was determined with Kaplan-Meier techniques, using log-rank testing to determine differences in survival between the cohorts. Baseline predictors of hospital mortality were identified by univariable Cox proportional hazards regression. E11 Stratified survival for biventricular and univentricular repairs for both groups was also performed using log-rank test.

The diagnostic assumptions of the Cox regression model, proportional hazards assumption, examination of influential observations (or outliers), and detecting nonlinearity in the relationship between the log hazard and the covariates were examined using the Residuals method. The common residuals for the Cox model include:

Schoenfeld residuals to check the proportional hazards assumption,

Martingale residual to assess nonlinearity, and

Deviance residual (symmetric transformation of the Martingale residuals), to examine influential observations.E11

A stepwise selection procedure, using an entry probability of 0.15 and exit probability of 0.05 based on univariable analysis, along with age and sex as a covariate, was used in subsequent multivariable analysis. A P value of less than .05 was considered statistically significant.

Results

Study Population

The age at operation for those with right isomerism varied from 1 day to 2.24 years, with a median of 24 days, and interquartile ranges of 18 to 45 days. For those with left isomerism, ages varied from 1 day to 14.79 years, with a median of 60 days, and interquartile ranges of 29 to 360 days. Just over three-quarters of patients with right isomerism were younger than 45 days, whereas just over half of those with left isomerism were younger than one year. Prostaglandin E1 had been administered in 35 (15%) patients with left isomerism, and 45 (22.7%) with right isomerism. Preoperative ventilatory support had been required in 41 (17.6%) patients with left isomerism, and 81 (41%) with right isomerism (Tables E1-E3).

Cardiac Lesions

More than half of the patients with right isomerism had either bilateral superior caval veins or a solitary left superior caval vein (Tables E1-E3). Totally anomalous hepatic venous drainage was present in one-tenth. All patients had a totally anomalous pulmonary venous connection, which was obstructive in one-third. A functionally univentricular heart was present in one-third, with one-fifth having pulmonary atresia (Figures 1 and 2).

Almost four-fifths of those with left isomerism had an interruption of the inferior caval vein, while one-sixth had common atriums. An atrioventricular septal defect with a common valve was found in one-third, and one-tenth had a functionally univentricular heart (Figures 3 and 4).

Surgical Techniques

Most procedures were undertaken using moderately hypothermic cardiopulmonary bypass at 32 °C, using cold blood St. Thomas cardioplegia. Direct venous cannulation was preferred. Problems of venous cannulation, however, were ubiquitous because of the abnormal systemic venoatrial connections. Deep hypothermic circulatory arrest, with selective cerebral perfusion, was used in 21 patients when separate venous cannulation proved impractical. In those individuals with interrupted inferior caval veins, the hepatic veins, if confluent, were separately cannulated, or else managed using a sump sucker (Tables E4 and E5).

Banding of the pulmonary trunk had been performed on 23 (11.6%) individuals with right isomerism, and 16 (6.9%) with left isomerism. Palliative systemic-to-pulmonary arterial shunts had been constructed in 39 (19.7%) patients with right isomerism, and 6 (2.6%) with left. Complex baffling procedures were required in 55 patients with essentially common atrial chambers, 18 with right and 38 with left isomerism.

Kawashima's procedure, with concomitant biventricular repair, was undertaken in 115 (26.7%) patients with interruption of the inferior caval vein. Of these, 92 had isomeric left appendages, but 23 had right isomerism. Completion of the Fontan circulation was achieved in 65 patients deteriorating after a previous superior cavopulmonary connection, and in 21 patients after Kawashima repair with the development of pulmonary arteriovenous malformations. The hepatic venous return in the latter patients was redirected using either an extracardiac polytetrafluoroethylene conduit or a partial intracardiac fenestrated conduit.

The double-barreled technique was used in two patients with left isomerism and superior sinus venosus defects. Patch closure of a ventricular septal defect was performed in 18 (7.7%) patients with left isomerism, while the repair of divided left-sided atrium was needed in three further patients. Unilateral or bilateral superior cavopulmonary connections were constructed in four patients. Such superior cavopulmonary connections, with concomitant rechanneling of pulmonary veins as single-stage procedures, were made in 65 individuals with right isomerism, and 18 with left isomerism. Total cavopulmonary connections, with redirection of pulmonary veins, were accomplished in nine patients (4.5%) with right isomerism.

In 62 patients with balanced atrioventricular septal defects, 52 having left isomerism, repair proved possible using a “two patch” technique. We used the one-and-a-half ventricular repair in 10 individuals with right, and eight with left isomerism. Redirection of pulmonary veins was required in 228 patients, with 30 of these having isomeric left appendages. In 21 patients with left isomerism and 11 with right isomerism, the transected left superior caval vein was implanted in the left pulmonary artery.

Overall, we achieved biventricular repair in 68.7% of patients with left isomerism, but only 22.7% with right isomerism (P < .001, Table E3). Postoperatively, computed tomographic angiocardiography was used in 68 patients to assess the systemic superior cavoatrial junction, the newly reconstructed systemic and pulmonary venous pathways, the adequacy of reparative procedures, and the suitability for second-stage procedures.

Operative Results

The mean hospital stay was 29.7 ± 17.6 days, with the mean stay in the intensive care unit lasting 15.8 ± 12.6 days. The mean ventilatory time was 10.9 ± 14.6 days. Of 198 patients with right isomerism, 42 died (21.2%). For those with isomeric left appendages, 28 of 233 (12%) patients did not survive. Of the deaths in hospital, 13 patients suffered intractable pulmonary hypertensive crises, 10 suffered massive pulmonary hemorrhage, and 13 had persistent low cardiac output despite the use of extracorporeal membrane oxygenation. Complications related to prematurity and respiratory distress syndrome contributed to death in seven patients. Of the remainder, septicemia occurred in five, coagulopathy and bleeding in two, secondary peritonitis from the perforated small intestine in two patients with left isomerism and malrotation of the gut, hepatic failure in two patients with biliary atresia, and hepatic portal venous anomalies, and meningitis in two patients. Twenty-one patients had pulmonary hemorrhage subsequent to the repair of totally anomalous pulmonary venous connection, with or without additional shunting procedures; of which 10 patients died. Of 10 patients with leakage of chyle, seven recovered with conservative management, while the rest required thoracic duct ligation.

Arrhythmias and Morbidity

We encountered supraventricular arrhythmias postoperatively in 52 (26.2%) patients with right isomerism, and in 55 (23.6%) patients with left isomerism. Implantation of permanent pacemakers was required in eight patients with right isomerism, and 14 with left isomerism (Table E3).

Late Outcomes

Subsequent to discharge from hospital, we lost an additional 8 (4.8%) patients with right isomerism, and 6 (2.8%) patients with left isomerism. The median age of patients dying late postoperatively was 6.6 months (range 1-24 months, interquartile range [IQR] 15.26) at a median follow-up of 2 months (range 2-165 months, IQR 17 months).

Between January and December of 2021, we followed up all but 2 of 347 patients (99.4%) patients, capturing 3585.66 patient-years of data, with a mean follow-up time of 119.52 months. Median follow-up was 124 months, with interquartile ranges from 36 to 177 months. Follow-up of greater than 12 months was achieved in 345 patients (99.4%). The probability of 15-year survival for those with left isomerism was 86.60% ± 0.0249%, with 95% confidence intervals from 0.808 to 0.907). The comparable figures for those with right isomerism were 77.05% ± 0.0326% survival, and 95% confidence intervals from 0.698 to 0.827. The differences between the groups were statistically significant (P = .006, Figure 5). The probability of stratified survival at 15 years for both right and left isomeric individuals undergoing biventricular and univentricular repairs was 85.0% ± 0.025% and 83.0% ± 0.318%, respectively. The differences between the groups were marginally statistically significant (P = .05, Figure 6). At their last follow-up, 300 (87%) of the patients were in the first class of the New York Heart Association, with the other 45 (13%) in the second class. In 12 survivors, we now anticipate the need to relieve pulmonary venous obstruction, and in 10 to undertake repair of an atrioventricular valve. Additional solitary patients will require relief of right ventricular outflow tract obstruction and closure of a previously unrecognized ventricular septal defect.

As part of the staging procedure, we took down the systemic-to-pulmonary artery shunts and performed 14 superior cavopulmonary connections, 25 total cavopulmonary connections, and 6 biventricular repairs. Debanding of the pulmonary trunk was required along with takedown in four patients with superior cavopulmonary connections, 18 with total cavopulmonary connections, and 19 during the biventricular repair.

Of 87 patients undergoing completion of the Fontan circulation, we used either an extracardiac or intra-extraatrial fenestrated pathway in 65 (74.7%). The remaining patients are awaiting completion.

Cox proportional hazards analysis revealed the risk of death to be significantly high in the presence of prematurity, pulmonary atresia, atrioventricular septal defect guarded by a common valve, parachute mitral valve, interrupted inferior caval vein; functionally univentricular heart with totally anomalous pulmonary venous connection, obstructed pulmonary veins, and postoperative requirement of extracorporeal membrane oxygenation (Tables E6-E11).

Additional risk factors for death in right isomerism were prematurity, weight less than 2.5 kg, pulmonary atresia, cyanosis, atrioventricular septal defect guarded by a common valve, functionally univentricular hearts with anomalous pulmonanary veins, and obstructed pulmonary veins (Table E10). The comparable risk factors for those with left isomerism were prematurity, requirement for infusion of prostaglandins, complete heart block, preoperative requirement for inotropes, obstructed pulmonary veins, functionally univentricular heart with pulmonary venous problems, and postoperative requirement for extracorporeal membrane oxygenation (Table E11).

Comment

Studies assessing the surgical outcomes for individuals with isomeric atrial appendages are limited.^4–9^{,E3-E5,E9,E10} To our knowledge, our cohort of 431 patients undergoing surgery consecutively by a single surgeon is one of the largest studies currently available in the English literature. It is now beginning to be accepted that individuals with the so-called “heterotaxy” are best segregated according to the morphology of the atrial appendages.^4–9^{,E3-E5,E8,E9,E38,E39} Our study now shows that computed tomographic imaging is capable of determining appendage morphology, thus facilitating surgical planning (Figures 1-4).^3,5^,E7,E9 It also proved possible to confirm the distinguishing features during the surgical procedures. Cyanosis as a presenting symptom was present in both groups, and about half of the patients in each group also had congestive cardiac failure (Table E3). We found a highly significant statistical difference for age at initial diagnosis, being much earlier for right isomerism. A significantly increased risk of death emerged for cyanosed patients with left isomerism requiring prostaglandins (Table E11).

The presence of isomeric appendages alerts the surgeon to several significant findings,^3–5^,E6-E9 such as duplication of the sinus node in right isomerism, E20,E21 as opposed to an abnormal location of the atrial pacemaker in left isomerism. These features are important when performing the superior cavopulmonary shunt, or completing the Fontan circulation. E22,E23 With right isomerism, the coronary sinus is universally absent, and the pulmonary veins are anomalously connected even if returning to the heart. In left isomerism, the pulmonary venous drainage will always be anatomically normal, even if bilaterally symmetrical. The most usual finding, however, is interruption of the inferior caval vein, found in four-fifths of our cohort, but also, surprisingly, in almost one-quarter of those with right isomerism. When performing a bidirectional superior cavopulmonary connection, therefore, it is important to confirm, prior to ligating an azygos vein, whether it is a continuation of an interrupted inferior caval vein (Figures 3 and 4).^6–8^,E3,E9 The inferior caval vein may connect to either the left-sided or right-sided atrium. In left isomerism, this should be distinguished from bilateral connection of hepatic veins.

Although the arrangement of the inferior caval vein tends to distinguish those with left from right isomerism, this is not the case for the superior caval veins. There is a fundamental difference in the cavoatrial connections, nonetheless, between the subsets. In those with right isomerism, each vein connects to the top corner of its atrium, adjacent to a terminal crest and a sinus node. This can produce difficulties in diverting a left-sided vein to the right-sided atrium (Figures 1 and 2). There are several strategies available for redirection in these settings. E25-E29 We succeeded in re-routing the vein in 21 of our patients with left isomerism, and 11 with right isomerism. Although the venoatrial connections are uniformly abnormal, it is still possible in some individuals to find quasi-usual or quasi-mirror-imaged venous drainage. In these circumstances, it is possible to achieve atrial septation without creating an obstruction. This is rarely the case when the venoatrial connections are eccentric.^5,8^{,E3-E5,E14,E15,E17}

It is particularly important to take note of the hepatic venous connections. Direct drainage was present in just under one-quarter of our patients with right isomerism, and almost half of those with left isomerism. Preoperative demonstration of such venous arrangements can facilitate the construction of an intra-extraatrial Fontan pathway for redirection of the systemic venous return. In just under one-third of our patients with interruption of the inferior caval vein, we opted to perform Kawashima's procedure (Figure 3). Development of pulmonary arteriovenous malformations is reported in up to three-fifths of these patients. Redirection of the hepatic venous return to the systemic venous circuit, as achieved in several of our patients, can produce a resolution of the malformations (Figure 3).^5,7^,E31-E37 Furthermore, the systemic venous abnormalities of the hepatic circulation, and heptic portal venous abnormalities may also contribute to a higher incidence of hepatic dysfunction after surgery.

Many of the patients, irrespective of the type of isomerism, have common atrioventricular valves. In this setting, the successful creation of new and competent left and right atrioventricular valves is the cornerstone of repair. Such repair was attempted in one-sixth of our patients with right isomerism, and three-tenths of those with left isomerism (P < .001).

Previous reports have described the achievement of biventricular repairs in up to half of those with left isomerism, but in fewer individuals with right isomerism.^5–9^{,E3-E5,E40-E55,E68,E69} We achieved biventricular repair in just over two-thirds of those with left isomerism, and just over one-quarter of those with right isomerism. Among patients undergoing biventricular repair, surgery was straightforward in approximately two-thirds and complex in the remainder. When attempting biventricular repair, the surgeon is usually faced with creating complex intra-atrial baffles or intraventricular tunnels. This obviously always carries the risk of inducing surgical heart block, as occurred in 22 (5.1%) of our patients. Other problems are an obstruction to the left ventricular outflow tract, atrioventricular valvar regurgitation, and the need for a ventricle to pulmonary conduit. The risks of these procedures must be balanced against the known late complications of the Fontan circulation.^4–8^{,E3,E5,E40-E43} The intermediate option is the one-and-a-half ventricular repair, achieved in 18 of our patients (4.1%). We limited its use to those with Z-scores for the morphologically tricuspid valve between −1.5 and −4.8, or diameters of the valve between 45% and 70% of normal, along with bipartite right ventricular cavity morphology. E56-E58

The option always remains, nonetheless, to create the Fontan circulation, although this remains challenging in the light of features such as abnormal pulmonary venous connections, atrioventricular valvar dysfunction, and pulmonary atresia. E4,E17,E30,E41 Additional extracardiac anomalies also adversely affect morbidity and late postoperative outcome. E14,E23,E41 Outcomes with regard to atrioventricular valvar repair are reported to be improving.^5–7^,E52,E53 Repair or replacement of the valve is advocated prior to completing the Fontan circuit. In our experience, this approach did not result in early mortality. Early mortality overall has significantly decreased subsequent to the turn of the millennium but still remains high. E4,E40-E47 Further to improve the postoperative outcome, several investigators have proposed that all patients should have a fenestration. Our current approach is to fenestrate an intra-extracardiac or extracardiac polytetrafluoroethylene conduit. Using such techniques, some investigators have recently demonstrated late outcomes comparable to those achieved in the setting of usual atrial arrangement. E42-E47

Despite two-fifths of those with right isomerism, and one-fifth with left isomerism undergoing univentricular repair, a minority needed first-stage palliation, and none needed a Norwood procedure. Just over three-fourths of right isomeric patients were younger than 45 days, and over half of left isomeric patients were younger than one year. Because the late presentation of congenital heart diseases is not unusual in the developing world, many who needed neonatal palliation might have died and could not be included in this series. Although our institution is a tertiary-level center, the socioeconomic profile of the patients and the lack of health insurance benefits led to delayed referral and surgery.

A totally anomalous pulmonary venous connection is an anatomical necessity in the setting of hearts in which both atrial chambers have morphologically right appendages. In the setting of cardiac connection, the venous return is often obstructed.^1–6^{,E3,E5,E9,E15,E17,E54} Pectinate muscles all around the muscular vestibules are part of the problem and should be noted by the surgeon.^1–6^{,E3,E5,E9,E15,E17,E54} In the majority of the patients, nonetheless, all of the pulmonary veins connect to an extracardiac systemic site, but still often with obstruction to the drainage.

When we recognize this finding and encounter suprasystemic pulmonary artery hypertension subsequent to weaning from bypass, we perform adjustable ligation of the vertical vein, routine augmentation of the left-sided atrium, and interatrial septal fenestration. The operative technique and results have been reported earlier. E50,E51

The pulmonary venous connections will always be anatomically normal in left isomerism, but are often bilaterally symmetrical, creating in essence partially anomalous drainage.^1–6^{,E3,E5,E9,E15,E17,E54} The significant distance between the right- and left-sided vein then mandates elongated and complex suture lines for any potential intra-atrial baffle.^1–6^{,E3,E5,E9,E15,E17,E54} On occasion, the veins can produce quasi-mirror-imaged drainage should all the systemic venous return to the left-sided atrium.

Pulmonary venous obstruction is more frequent when the pulmonary arteries are hypoplastic, atretic, or discontinuous, as is often the case in right isomerism.^1–8^{,E10,E15-E17,E30,E54} The overall risk of death for our patients was almost three times higher when they had pulmonary atresia (Table E9). Any severe obstruction to pulmonary venous flow may also mask clinically important pulmonary venous anomalies (Figures 1-4).^1–8^{,E10,E15-E17,E30,E54} In this setting, volume overload imposed by a systemic-to-pulmonary artery shunt, or by a superior cavopulmonary connection, has previously been associated with death. E5,E18,E30,E36,E46,E50-E60 Further complications are the intrinsic anatomic and histopathologic differences found in the pulmonary veins of individuals with right isomerism.⁶^{,E15,E17,E49-E51,E61-E63} It is hardly surprising, therefore, that up to half of those with functionally univentricular hearts and anomalous pulmonary venous connections still die during initial palliation, with ongoing mortality of up to one-third when creating the Fontan circulation.⁶^{,E15,E17,E49-E51,E61-E63}

Although still less than satisfactory, and in keeping with previous experiences, our outcomes were better for those with left as opposed to right isomerism.^5–9^{,E1,E4,E27,E43,E46,E48,E68,E69} Taken overall, almost four-fifths of our patients with right isomerism were alive at last follow-up and almost nine-tenths of those with left isomerism. Our findings are similar to those reported in a recent study from the Society of Thoracic Surgeons, which demonstrated greater postsurgical mortality, more postsurgical respiratory complications, and a more complicated postsurgical course in patients with isomeric appendages. E30,E65

We recognize that our study has its limitations. Any analysis from a single center may not be generalizable to all centers. We still remain uncertain as to whether the one-and-a-half ventricle repair is ever the right thing to do in the setting of isomerism. Properly assessing whether this approach may produce superior outcomes in those with isomeric appendages will require a multi-institutional prospective study.

Conclusions

We submit that multimodality imaging is now capable of characterizing and delineating all the anatomical details required for optimal presurgical planning in the setting of isomerism. Despite innovative methods of treatment, surgical mortality and morbidity remain substantial in those with right isomerism. In this light, it seems prudent to reassess the conventional strategies for management.

Supplemental Material

sj-docx-1-pch-10.1177_21501351221151049 - Supplemental material for Long-Term Surgical Outcomes of Patients With Isomeric Right and Left Atrial Appendages

Supplemental material, sj-docx-1-pch-10.1177_21501351221151049 for Long-Term Surgical Outcomes of Patients With Isomeric Right and Left Atrial Appendages by Ujjwal Kumar Chowdhury and Robert H Anderson, Niraj Nirmal Pandey, Niwin George, Lakshmi Kumari Sankhyan, Maroof A Khan, Shikha Goja, Sivasubramanian Ramakrishnan, Saurabh Kumar Gupta in World Journal for Pediatric and Congenital Heart Surgery

Footnotes

Authors’ Note

The authors assert that all procedures contributing to this study comply with the ethical standards of the relevant national guidelines on human experimentation and with the Helsinki declaration of 1975, as revised in 2008.

Declaration of Conflicting Interests

The author(s) declared no potential conflicts of interest with respect to the research, authorship, and/or publication of this article.

Funding

The author(s) received no financial support for the research, authorship, and/or publication of this article.

ORCID iDs

Ujjwal Kumar Chowdhury

Robert H Anderson

Niwin George

Shikha Goja

Saurabh Kumar Gupta

Supplemental Material

Supplemental material for this article is available online.

References

Anderson

Spicer

Loomba

. Is an appreciation of isomerism the key to unlocking the mysteries of the cardiac findings in heterotaxy? J Cardiovasc Dev Dis. 2018;5(1):11.

Anderson

. Atrial structure in the presence of visceral heterotaxy. Cardiol Young. 2000;10(4):299-302.

Uemura

Devine

Kilpatrick

Anderson

. Atrial appendages and venoatrial connections in hearts from patients with visceral heterotaxy. Ann Thorac Surg. 1995;60(3):561-569.

Spicer

Chowdhury

Anderson

, et al. The surgical anatomy of heart with isomeric atrial appendages—implications for surgical management. Eur J Cardiothorac Surg. 2022;62(1):ezac139. doi:10.1093/ejcts/ezac139

Chowdhury

Anderson

Spicer

, et al. Surgical management of hearts with isomeric atrial appendages. J Card Surg. 2022;37(5):1-13.

Hashmi

Abu-Sulaiman

McCrindle

, et al. Management and outcomes of right atrial isomerism: a 26-year experience. J Am Coll Cardiol. 1998;31(5):1120-1126.

Gilljam

McCrindle

Smallhorn

Williams

Freedom

. Outcomes of left atrial isomerism over a 28-year period at a single institution. J Am Coll Cardiol. 2000;36(3):908-911.

Anagnostopoulos

Pearl

Octave

, et al. Improved current era outcomes in patients with heterotaxy syndromes. Eur J Cardiothorac Surg. 2009;35(5):871-877.

Makhija

Marwah

Mishra

, et al. Biventricular repair in heterotaxy patients. World J Pediatr Congenit Heart Surg. 2015;6(2):195-202.

Supplementary Material

Please find the following supplemental material available below.

For Open Access articles published under a Creative Commons License, all supplemental material carries the same license as the article it is associated with.

For non-Open Access articles published, all supplemental material carries a non-exclusive license, and permission requests for re-use of supplemental material or any part of supplemental material shall be sent directly to the copyright owner as specified in the copyright notice associated with the article.

0.00 MB

0.06 MB