e-ISSN : 2149-8156
Turkish Journal of Thoracic and Cardiovascular Surgery     
Lymphatic evaluation with magnetic resonance lymphangiography in Fontan patients: Our single-center experience
Demet Kangel1, Serap Baş2, Ali Nazım Güzelbağ1, Halise Zeynep Genç1, Ezgi Direnç Yücel2, Ali Can Hatemi4, İbrahim Cansaran Tanıdır1, Erkut Öztürk1
1Division of Pediatric Cardiology, İstanbul Health Sciences University, Başakşehir Çam and Sakura City Hospital, İstanbul, Türkiye
2Department of Radiology, İstanbul Health Sciences University, Başakşehir Çam and Sakura City Hospital, İstanbul, Türkiye
3Department of Anesthesiology and Reanimation, İstanbul Health Sciences University, Başakşehir Çam and Sakura City Hospital, İstanbul, Türkiye
4Division of Pediatric Cardiovascular Surgery, İstanbul Sağlık Bilimleri University, Başakşehir Çam and Sakura City Hospital, İstanbul, Türkiye
DOI : 10.5606/tgkdc.dergisi.2025.28290

Abstract

Background: This study aims to evaluate our experience with magnetic resonance lymphangiography in single-ventricle congenital heart disease patients and to examine the association between imaging findings and clinical outcomes and postoperative outcomes.

Methods: Between November 2022 and May 2025, a total of 33 patients (22 males, 11 females; median age: 44 months; range, 37 to 57.5 months) with single-ventricle congenital heart disease who underwent T2-weighted magnetic resonance lymphangiography at our center were retrospectively analyzed. The T2-weighted sequences were chosen for their high-resolution depiction of lymphatic structures without the need for contrast agents. The imaging findings were analyzed for preoperative risk evaluation or suspected postoperative lymphatic complications.

Results: Lymphatic abnormalities were categorized into types 1 to 3 based on the extent and distribution of T2-hyperintense signals. No patients in this cohort exhibited type 4 abnormalities. Among 33 patients, 11 (33%) were classified as type 1, 18 (55%) as type 2, and four (12%) as type 3. Although not statistically significant, patients with type 3 patterns had the longest median pleural effusion duration (27.5 days) and length of hospital stay (61 days). One patient showed early postoperative progression from type 2 to type 3, which resolved clinically and radiologically after fenestration ballooning. In the late period, two patients developed protein-losing enteropathy, and one had Fontan failure.

Conclusion: Magnetic resonance lymphangiography provides critical information about structural lymphatic abnormalities. It also aids risk stratification prior to the Fontan procedure and guides individualized management of postoperative complications, ultimately guiding treatment and improving outcomes.

Single-ventricle congenital heart disease (SVCHD), affecting 2 to 3 per 10,000 live births and comprising 7 to 8% of congenital heart defects, requires staged palliation culminating in the Fontan procedure.[1] This surgery redirects systemic venous blood to the pulmonary arteries, bypassing a subpulmonary ventricle. Although it improves survival, the resulting chronic elevation in central venous pressure (CVP) and reduced cardiac output predispose patients to complications such as protein-losing enteropathy (PLE), chylothorax, plastic bronchitis (PB), and hepatic congestion.[2]

Recent evidence highlights the central role of the lymphatic system in these complications. Elevated CVP impairs lymphatic drainage and increases lymph production, particularly from hepatic sources, resulting in thoracic and abdominal congestion. More importantly, lymphatic abnormalities may exist even before Fontan surgery and are linked to adverse outcomes including Fontan failure, transplantation, and mortality.[2,3]

Magnetic resonance lymphangiography (MRL) has become essential for non-invasive evaluation of lymphatic abnormalities in Fontan patients. Also, T2-weighted techniques such as T2-SPACE (Sampling Perfection with Application-optimized Contrasts using different flip angle Evolution) and BLADE (a motion-corrected turbo spin-echo sequence) enable high-resolution imaging without contrast administration.[3,4] Biko et al.[2] proposed a thoracic lymphatic classification (types 1-4), with higher types correlating with poorer outcomes. More recently, Schroeder et al.[5] introduced grading systems for abdominal lymphatic territories, including para-aortic and portal-venous systems, underscoring the systemic nature of lymphatic dysfunction in this population.

Although lymphatic pathology is increasingly recognized in Fontan patients, data on the clinical utility of MRL still remain limited. Most of the studies are single-center and largely from North America or Europe, limiting generalizability due to regional differences in patient demographics, surgical strategies, and care protocols.[2,4,6] Moreover, longitudinal studies have shown that lymphatic abnormalities may persist despite clinical changes or hemodynamic interventions.[6]

High-resolution MRL has been integrated into the routine clinical evaluation of patients with congenital heart disease (CHD), particularly those undergoing Fontan or Glenn procedures, at our center. In the present study, we, therefore, aimed to evaluate the role of T2-weighted MRL in both preoperative risk stratification and the characterization of postoperative lymphatic complications in patients with SVCHD who were candidates for or underwent Fontan surgery.

Methods

This single-center, retrospective study was conducted at Başakşehir Çam and Sakura City Hospital, Division of Pediatric Cardiology and Division of Pediatric Cardiovascular Surgery between November 2022 and May 2025. A total of 33 patients (22 males, 11 females; median age: 44 months; range, 37 to 57.5 months) with SVCHD who underwent T2-weighted MRL were included. Thirty were imaged pre-Fontan for surgical planning and risk stratification. At the time of data analysis, 17 had completed Fontan surgery and 13 were awaiting the procedure. Five patients underwent post-Fontan imaging due to suspected complications such as prolonged effusion, PLE, or PB. Two had both pre- and post-Fontan scans, totaling 35 studies. Three patients with incomplete data were excluded from the analysis. Patients were eligible for inclusion, if they had a confirmed diagnosis of CHD and underwent MRL for clinical evaluation. Exclusion criteria included inadequate or incomplete imaging data, acquired heart conditions, and patients with primary lymphatic malignancies. Written informed consent was obtained from the parents and/or legal guardians of the patients. The study protocol was approved by the Başakşehir Çam Sakura City Hospital Scientific Research Ethics Committee (Date: 25.06.2025, No: 2025/150). The study was conducted in accordance with the principles of the Declaration of Helsinki.

Imaging protocol
All MRL examinations were performed on a 1.5 Tesla MRI system using high-resolution, non-contrast T2-weighted sequences multiplanar images were acquired to assess cervical, thoracic, abdominal, and pelvic lymphatic structures. All scans were interpreted by radiologists experienced in cardiovascular imaging.

Lymphatic classification
Lymphatic abnormalities were classified into types 1 to 4 based on T2-hyperintense signal patterns, as described by Biko et al.[2] Type 1 indicates little or no T2-hyperintense signal in the thoracic lymphatic system. Type 2 is characterized by T2-hyperintense signal confined to the mediastinum. Type 3 shows supraclavicular and axillary extension of abnormal signal, while type 4 involves diffuse T2-hyperintense signal extending into the abdominal and/or retroperitoneal lymphatics.

Clinical data collection
Demographic and clinical data, including age, sex, diagnosis, and stage of palliation, were obtained from patient records. Preoperative evaluations included transthoracic echocardiography and, when available, cardiac catheterization to assess CVP, pulmonary vascular resistance index (PVRi), and pulmonary-to-systemic blood flow ratio (Qp/Qs).

Operative details such as cardiopulmonary bypass (CPB) and cross-clamp times were also recorded. Postoperative outcomes, such as duration of pleural effusion, length of hospital stay, PLE, PB, and Fontan failure were collected to evaluate potential associations with lymphatic imaging findings.

Surgical and postoperative management details
Fontan type (extracardiac conduit or lateral tunnel) and fenestration decisions were individualized based on anatomy and hemodynamics, including ventricular function, atrioventricular valve status, and PVRi, with surgical team input. Postoperative care included fluid restriction (0.75× m aintenance), s odium-limited d iet, a nd diuretics (furosemide ± spironolactone), titrated by weight and chest tube output. Tubes were removed when drainage was <2 mL/kg/day for 24 h. Prolonged effusion was defined as drainage >2 mL/kg/day beyond seven days and managed with intensified diuretics, medium-chain triglyceride-based diet, and, when needed, steroids or octreotide. Protein-losing enteropathy was defined as hypoalbuminemia (<3.0 g/dL) with elevated fecal α1-antitrypsin or clinical signs (edema/ascites) without liver disease. Fontan failure was defined as refractory PLE, persistent chylothorax, or need for Fontan takedown/fenestration in the absence of anatomic causes. No major concomitant procedures were performed at the time of Fontan.

Outcome measures
The primary outcome measure was the extent and type of thoracic lymphatic abnormalities detected by T2-weighted MRL in single-ventricle patients, both pre- and post-Fontan.

Secondary outcome measures included associations between lymphatic patterns and clinical factors such as Fontan completion status, hospital stay, pleural drainage duration, and lymphatic complications (e.g., PB, PLE, mortality). These findings were used to conduct preoperative risk assessment and postoperative management.

Statistical analysis
Statistical analysis was performed using the IBM SPSS version 23.0 software (IBM Corp., Armonk, NY, USA). Data distribution was assessed using the Kolmogorov-Smirnov test. Continuous variables were expressed in mean ± standard deviation (SD) or median and interquartile range (IQR), while continuous variables were expressed in number and frequency. Group comparisons were conducted using one-way analysis of variance (ANOVA) or the Kruskal-Wallis test for continuous variables and the chi-square test for categorical variables. The Bonferroni method was applied to adjust for multiple comparisons. Boxplots were generated for visual comparison of clinical outcomes among lymphatic types. A p value of <0.05 was considered statistically significant.

Results

Of 33 patients, 30 underwent MRL in the pre- Fontan period for risk stratification and surgical planning, and five in the post-Fontan period due to suspected lymphatic complications (e.g., prolonged effusion, PB, or PLE). Two patients were imaged at both time points, yielding 35 MRL studies in total. All analyses were conducted on a per-patient basis for 33 patients to ensure data independence. Due to the small number of post-Fontan cases, subgroup analysis was not performed, and results were reported collectively.

Baseline demographic and operative characteristics are summarized in Table 1. There were no statistically significant differences among lymphatic groups in terms of age at SCPC, age at imaging, ventricular dominance, atrioventricular valve regurgitation, or operative parameters including CPB and cross-clamp times. Both study groups were comparable with respect to baseline features.

Table 1. Comparison of demographic, clinical, surgical, and hemodynamic parameters among patients with different lymphatic pattern types

According to the classification of Biko et al.,[2] 11 patients (36.6%) had type 1, 18 (60%) had type 2, and four (13.3%) had type 3 lymphatic abnormalities. Patients with type 3 morphology showed a trend toward worse outcomes. Specifically, these patients had the longest median pleural effusion duration (27.5 days) and hospital stay (61 days), compared to 11.5 and 17.5 days in type 1 and 5.5 and 17 days in type 2, respectively. Although these differences did not reach statistical significance, they indicated a clinically relevant tendency (Table 1, Figure 1).

Figure 1. (a) Boxplot comparison of pleural effusion duration among patients with different lymphatic pattern types. Data are presented as median and interquartile range. Patients with type 3 patterns showed a trend toward longer effusion duration, although the difference was not statistically significant (Kruskal-Wallis test, p=0.145). (b) Boxplot comparison of hospital stay duration across lymphatic pattern groups. Patients with type 3 lymphatic patterns exhibited the longest hospitalizations. Although differences did not reach statistical significance, a clinically relevant trend was observed (Kruskal-Wallis test, p=0.131).

Five (14%) patients underwent post-Fontan MRL due to suspected lymphatic complications, four with late and one with early onset. The early case involved prolonged chylothorax. Initial preoperative MRL showed a type 2 pattern, which progressed to type 3 postoperatively with persistent effusion and abdominal hyperintensity. Medical treatment failed, but balloon dilation of the fenestration reduced Fontan pressure and resolved the effusion. The patient improved clinically and was discharged. Follow-up MRL showed regression to type 2 (Figure 2).

Figure 2. (a) Preoperative T2-weighted magnetic resonance lymphangiography demonstrating type 2 thoracic lymphatic abnormalities, limited to the supraclavicular region (white arrows). (b) Postoperative image demonstrating progression to a type 3 pattern with extensive supraclavicular and mediastinal lymphatic congestion (white arrows). (c) Abdominal T2-weighted image showing dilated mesenteric and periportal lymphatics (white arrows) consistent with lymphatic congestion. (d) Follow-up image after fenestration balloon dilatation revealing regression to a type 2 thoracic pattern, with markedly reduced cervical and mediastinal lymphatic signal (white arrows).
LA: Left anterior; RP: Right posterior.

Four patients underwent MRL for late Fontan complications. The first, a 3.5-year-old male, developed PLE 20 months postoperatively. Preoperative MRL showed type 1, but follow-up revealed progression to type 3 and mesenteric lymphatic abnormalities (Figure 3). Imaging and catheterization identified restrictive ventricular septal defect (VSD), and surgical enlargement led to marked improvement in PLE.

Figure 3. (a) Pre-Fontan T2-weighted magnetic resonance lymphangiography showing a normal type 1 thoracic lymphatic pattern. No dilated thoracic lymphatic structures are observed. (b) Postoperative image after restrictive ventricular septal defect physiology demonstrating progression to a type 3 thoracic pattern with diffuse supraclavicular, mediastinal, and mesenteric lymphatic enhancement (white arrows) consistent with lymphatic congestion.

The second patient presented with PLE two years after Fontan. The MRL showed Increased mesenteric T2 signals, duodenal and jejunal wall edema, and ascites, with thoracic findings consistent with type 2. Medical treatment for PLE was initiated.

Another patient, a 27-year-old woman with a history of Fontan at age five years, presented with dyspnea, fatigue, and abdominal distension. Thoracic MRL showed type 1 findings, but abdominal imaging revealed hepatic fibrosis and mesenteric lymphatic abnormalities. Due to recurrent chylothorax, PLE, and osteoporosis, she was diagnosed with Fontan failure and referred for the Hraska procedure.

Our final patient, a 16-year-old male who underwent Fontan at age 4.5, presented with hemoptysis. The MRL showed type 1 thoracic findings without additional abnormalities. Bronchoscopy revealed no active bleeding. Bronchoalveolar lavage cultures grew Pseudomonas and Staphylococcus aureus; targeted antibiotics were initiated. The patient was followed by the Pediatric Pulmonology and Immunology Team.

Discussion

In the present study, we assessed the prognostic relevance of thoracic lymphatic abnormalities identified via T2-weighted MRL in patients with SVCHD, including both those undergoing pre-Fontan evaluation and those presenting with post-Fontan complications. Our findings suggest that lymphatic pattern classification using T2-weighted MRL may serve as a non-invasive method for preoperative risk stratification in single-ventricle patients. Although statistical significance was not reached, patients with type 3 lymphatic patterns exhibited numerically longer durations of pleural effusion and hospital stay, suggesting a possible trend toward more complex postoperative courses, consistent with the previous literature.[2,3,7] However, these findings should be interpreted with caution due to the exploratory nature of the study and small subgroup sizes. Among post-Fontan patients, prolonged effusions occurred in four of 10 with type 2, two of five with type 1, and both patients with type 3 lymphatic abnormalities.

In the current study, in one patient, progression from type 2 to type 3 lymphatic morphology was documented in the early postoperative period, coinciding with persistent chylothorax and abdominal lymphatic congestion. Intervention based on these findings, balloon dilation of the fenestration, led to both clinical and radiological improvement. This case highlights the diagnostic and therapeutic value of serial MRL in dynamic postoperative monitoring.[8]

In a study, Dori et al.[6] previously demonstrated that MRL could identify lymphatic abnormalities after early palliative surgeries, such as the bidirectional Glenn procedure, underscoring the need for early lymphatic assessment. Furthermore, Ghosh et al.[9] and Dittrich et al.[10] showed that unrecognized lymphatic abnormalities might contribute to early Fontan complications such as prolonged drainage or chylothorax, particularly in the absence of overt hemodynamic causes. These studies emphasize the importance of incorporating MRL into routine evaluations even before Fontan completion. These observations are consistent with our findings, where pre-Fontan and post-Glenn MRL revealed lymphatic abnormalities in patients who later developed early postoperative complications, supporting the relevance of early lymphatic imaging in clinical decision-making.

Our study also included patients" data evaluated in the late postoperative period. One case presented with Fontan failure characterized by recurrent chylothorax, ascites, and PLE; two others exhibited abdominal PLE findings, and another showed no MRL abnormalities despite clinical symptoms. These findings underline both the systemic extent and diagnostic complexity of lymphatic involvement in Fontan physiology. Previous studies have similarly emphasized the role of lymphatic dysfunction in early post-Fontan complications, such as chylothorax and prolonged effusions,[3,7,11] and have described lymphatic abnormalities not only in the thorax, but also in hepatic and mesenteric territories.[2,4,12,13] Furthermore, recent imaging reviews and technical reports have supported the use of MRL for comprehensive lymphatic evaluation across diverse CHD populations.[8,14,15]

While definitive conclusions are limited by sample size and heterogeneity, the observed correlation between higher-grade lymphatic patterns and adverse clinical trajectories supports the hypothesis that lymphatic morphology may be predictive of Fontan-related complications.[2,7] No patients exhibited type 4 lymphatic patterns in our cohort, which may reflect the characteristics of the patient population or imaging timing. Larger prospective studies are needed to confirm the prognostic utility of MRL-based grading systems.

Review of the literature have emphasized that lymphatic abnormalities in patients with single-ventricle physiology may persist over time, regardless of interventions aimed at modifying hemodynamics. Moosmann et al.[8] reported that, while a subset of patients demonstrated imaging regression following catheter-based procedures, the majority maintained stable lymphatic classifications on serial T2-weighted MRL, highlighting the limited impact of isolated hemodynamic interventions on lymphatic remodeling. Additionally, Kristensen et al.[16] found that lymphatic a bnormalities were present even before the Glenn operation in children with single-ventricle physiology, and higher-grade abnormalities were associated with increased risk of chylothorax and mortality. Furthermore, Mills et al.[12] and Negm et al.[14] highlighted the diagnostic utility of abdominal MRL in detecting mesenteric and portal lymphatic involvement, features commonly associated with PLE and ascites in Fontan patients. This expands the scope of lymphatic evaluation beyond the thorax, where most standard assessments are typically focused.

Recent advances in contrast-enhanced lymphatic imaging, including intrahepatic and intramesenteric dynamic MRL (IH-DCMRL and IM-DCMRL), have enabled real-time visualization of lymphatic flow and identification of hepatoduodenal or mesenteric leaks, particularly in patients with PLE and refractory ascites.[16-19] These techniques can reveal pathologies that may not be detectable with T2-weighted imaging alone. Although such contrast-based methods were not applied in our study, they offer valuable complementary information in selected cases, particularly when detailed flow mapping or targeted interventions are required.[5,12,14]

In comparison to contrast-enhanced MRL (CE-MRL), T2-weighted MRL offers a non-invasive, contrast-free alternative suitable for fragile pediatric populations.[8,17,20] While CE-MRL techniques provide real-time flow assessment and detailed leak localization,[16,19] T2-weighted MRL remains valuable for screening and longitudinal monitoring. The two approaches should be viewed as complementary rather than competing techniques.[16,19]

In a recent study, Kelly et al.[21] showed that lymphatic abnormalities might progress over time, with higher-grade patterns after Fontan completion being associated with longer postoperative drainage and higher incidence of PLE and chylothorax. This highlights the importance of longitudinal lymphatic imaging in identifying high-risk individuals and tailoring follow-up strategies.[21,22] Additionally, Dori and Smith[23] emphasized that lymphatic dysfunction was not merely a consequence of Fontan hemodynamics, but also involved congenital and possibly genetic predispositions, making early imaging essential in the management of single ventricle physiology.

On the other hand, as a single-center, retrospective study with a relatively small sample size, the generalizability of our findings is inherently limited. In addition, longitudinal follow-up was available only for one patient, which precludes our ability to assess dynamic changes in lymphatic morphology across time. Additionally, although multivariate analysis or logistic regression could have provided deeper insights into the association between lymphatic patterns and clinical outcomes, such analyses were not feasible due to the small sample size and limited number of outcome events. Therefore, this limitation may reduce the ability to control for potential confounding variables and should be considered while interpreting the findings.

In conclusion, T2-weighted magnetic resonance lymphangiography holds promise as a tool for individualized risk assessment and targeted postoperative management in Fontan patients. With the advancement of novel contrast and sequence-based protocols, magnetic resonance lymphangiography is poised to become an essential component of congenital heart disease care. Further research is essential to standardize lymphatic grading criteria and define its role in guiding long-term therapeutic strategies.

Data Sharing Statement: The data that support the findings of this study are available from the corresponding author upon reasonable request.

Author Contributions: Concept, analysis and/or interpretation, writing: S.B., E.Ö., D.K.; Design: S.B., İ.C.T.; Supervision: S.B., A.C.H., E.Ö.; Resource: S.B., E.Ö.; Materials: S.B., E.D.Y.; Data collection and/or processing: S.B., D.K., H.Z.G.; Literature search: S.B.,D.K.; Critical reviews: S.B., İ.C.T., E.Ö.

Conflict of Interest: The authors declared no conflicts of interest with respect to the authorship and/or publication of this article.

Funding: The authors received no financial support for the research and/or authorship of this article.

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Keywords : Congenital heart defects, Fontan procedure, lymphatic abnormalities, magnetic resonance imaging, risk assessment
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