Association between lymphatic abnormalities in the neck and thorax in primary chylopericardium and surgical outcomes evaluated by non-enhanced magnetic resonance (MR) lymphangiography
Original Article

Association between lymphatic abnormalities in the neck and thorax in primary chylopericardium and surgical outcomes evaluated by non-enhanced magnetic resonance (MR) lymphangiography

Yimeng Zhang, Xiaoli Sun, Mengke Liu, Xingpeng Li, Mingxia Zhang, Yongli Duan, Rengui Wang

Department of Radiology, Beijing Shijitan Hospital Affiliated to Capital Medical University, Beijing, China

Contributions: (I) Conception and design: Y Zhang; (II) Administrative support: R Wang; (III) Provision of study materials or patients: Y Zhang, Y Duan; (IV) Collection and assembly of data: Y Zhang, M Zhang, M Liu; (V) Data analysis and interpretation: Y Zhang, X Sun, X Li; (VI) Manuscript writing: All authors; (VII) Final approval of manuscript: All authors.

Correspondence to: Rengui Wang, MD. Department of Radiology, Beijing Shijitan Hospital Affiliated to Capital Medical University, Yangfangdian Tieyi Road No. 10, Haidian District, Beijing 100038, China. Email: wangrg@bjsjth.cn.

Background: Chylopericardium refers to the accumulation of chylous fluid in the pericardial cavity. Non-enhanced magnetic resonance lymphangiography (MRL) can show neck and thoracic lymphatic abnormalities in the primary chylopericardium. It is not clear whether there is a relationship between neck and thoracic lymphatic abnormalities in primary chylopericardium and thoracic duct terminal release surgery. This study aimed to explore the correlation between the severity of neck and thoracic lymphatic abnormalities observed in non-enhanced MRL and the surgical outcomes in primary chylopericardium.

Methods: This is a retrospective cohort study. A retrospective analysis was conducted on fifty-six patients diagnosed with primary chylopericardium between January 2016 and December 2021, all of whom underwent thoracic duct terminal release surgery. Ultrasonography, chest computed tomography (CT) and non-enhanced MRL were performed prior to the surgical intervention. Patients were categorized into four types based on the severity of neck and thoracic lymphatic abnormalities observed in the non-enhanced MRL. Clinical and laboratory examinations and surgical outcomes were compared across different types using χ2-test or Fisher’s exact test, t-test, and Kruskal-Wallis H-test. Additionally, independent factors influencing surgical outcomes were analyzed.

Results: Among primary chylopericardium cases (n=56), 22 (39.2%) were classified as type I or II, 17 (30.4%) as type III, and 17 (30.4%) as type IV. Surgical outcomes were more favorable for type I or II patients than those with type III or IV, accompanied by a reduction in postoperative primary chylopericardium volume (P=0.002). Postoperative chest CT scans indicated that type I or II patients had fewer instances of large grid shadows, small grid shadows, and bronchovascular bundle thickening compared to preoperative scans (P=0.001, P=0.02, P=0.03). Age and bronchomediastinal trunk dilation emerged as independent factors influencing surgical outcomes [odds ratio (OR) 0.03, 95% confidence interval (CI): 0.003–0.220, P=0.001; OR 11.10, 95% CI: 1.70–72.39, P=0.01, respectively].

Conclusions: A more severe degree of neck and thoracic lymphatic abnormalities is associated with worse surgical outcomes. Moreover, age and bronchomediastinal trunk dilatation are independent predictors of surgical outcomes. Preoperative utilization of non-enhanced MRL for severity of lymphatic abnormalities classification in primary chylopericardium patients offers a noninvasive means of assessing surgical risk.

Keywords: Chylopericardium; non-enhanced magnetic resonance lymphangiography (non-enhanced MRL); lymphatic abnormalities; thoracic duct; surgery


Submitted Jan 24, 2024. Accepted for publication Jun 07, 2024. Published online Jul 12, 2024.

doi: 10.21037/qims-24-144


Introduction

Chylopericardium is a very rare condition that involves the accumulation of chylous fluid within the pericardial cavity. It was initially described by Hasebrock et al. (1) in 1888 and is classified into primary and secondary chylopericardium based on its underlying causes. Primary chylopericardium is a rare condition arising from various conditions that lead to compression, obstruction, or rupture of the thoracic duct, lymphatic trunks (especially the bronchomediastinal trunks), and their accessory branches, causing chylous fluid to enter the pericardium (2). Secondary chylopericardium is commonly associated with factors such as trauma, surgical trauma, radiotherapy, mediastinal tumors, lymphangiomas, infections, filariasis, and subclavian vein embolism, among others (3). The exact etiology and pathogenesis of this condition remain unknown. Akamatsu et al. proposed potential factors, including (I) compromised lymphatic valves within branches connecting the thoracic duct and pericardial lymphatic vessels, (II) increased pressure in the thoracic duct due to lymphangiectasia, and (III) anomalous connections of lymphatic vessels to pericardial lymphatics resulting in chylous reflux (4). Additionally, primary chylopericardium attributed to lymphatic malformations is rare (5).

Diagnosing this condition is challenging and involves invasive procedures such as pericardiocentesis and chylous fluid characterization tests. Imaging techniques encompass direct lymphangiography (DLG), nuclear lymphoscintigraphy, computed tomography lymphangiography (CTL), and magnetic resonance lymphangiography (MRL) (6,7). DLG provides important insights into the interaction between the pericardial cavity and the lymphatic system, but its utility is limited because it is an invasive and complex procedure (8). Nuclear lymphoscintigraphy demonstrates radionuclide accumulation in the pericardial region but lacks high spatial resolution (9). CTL is useful to to detect secondary causes and lymphatic vessels larger than 1 mm, providing valuable information about abnormalities in the mediastinal region, thoracic duct, accessory branches, parietal pericardial lymphatics, as well as their relationships with adjacent organs. However, it carries the drawback of radiation exposure (8). MRL imaging has been sparingly employed in a few cases to elucidate the relationship between the thoracic duct and chylopericardium (10). Non-enhanced MRL obviates the need for contrast agents and employs a three-dimensional (3D) heavily T2-weighted fast spin-echo sequence water imaging approach. Axial images, coupled with coronal and sagittal maximum intensity projection (MIP) reconstructions, vividly depict the central lymphatic system, all while being non-invasive and devoid of radiation (11).

Surgical interventions remain the mainstay of treatment for this condition, with approaches primarily targeting the thoracic duct and pericardial lymphatics. These surgical procedures encompass thoracic duct terminal release surgery and ligation of the reflux branch (4). Notably, there is a lack of studies that examine the relationship between primary chylopericardium’s neck and thoracic lymphatic ducts abnormalities and surgical outcomes using non-enhanced MRL. Thus, this study aims to describe the relationship between different subtypes of neck and thoracic lymphatic abnormalities observed in non-enhanced MRL scans and surgical outcomes in 56 cases of primary chylopericardium. We present this article in accordance with the STROBE reporting checklist (available at https://qims.amegroups.com/article/view/10.21037/qims-24-144/rc).


Methods

General information

Clinical, laboratory examination, and imaging data of 104 patients diagnosed with chylopericardium between January 2016 and December 2021 were collected retrospectively and consecutively. The study was conducted in accordance with the Declaration of Helsinki (as revised in 2013). The study was approved by Institutional Ethics Board of Beijing Shijitan Hospital (No. IIT2024-059-001) and individual consent for this retrospective analysis was waived. Inclusion criteria comprised: (I) presence of pericardial effusion on ultrasound, (II) subjects that underwent pericardiocentesis and laboratory assessments: subjects that underwent pericardiocentesis and laboratory confirmation of the diagnosis of chylopericardium according to “Staats critera” (12), (III) all patients performed with non-enhanced MRL examination, (IV) all patients performed with thoracic duct end adhesion release. Exclusion criteria included: (I) secondary etiologies like trauma, radiotherapy, infection, tuberculosis, lymphoma, venous obstruction, and other malignant tumors, (II) incomplete clinical, laboratory, or imaging data. Out of the initial 104 patients, 16 were excluded due to secondary causes of chylopericardium [tuberculous pericarditis (n=8), idiopathic pericarditis (n=6), thymic malignant tumor (n=1), and mediastinal lymphoma (n=1)], and 32 were excluded due to incomplete data, leaving a total of 56 cases for analysis in this study.

Non-enhanced MRL examination

All non-enhanced MRL images were acquired within two weeks prior to surgery. Axial images were obtained on a 1.5 T magnetic resonance imaging (MRI) system (Siemens MAGNETOM Avanto, Malvern, PA, USA), and coronal reconstructions were performed using the following parameters: 3D heavily T2-weighted fast spin-echo sequence hydrography (FRFSE) with a matrix of 256×256, field of view ranging from 300 to 450; repetition time of 2,500 ms; echo time of 650 ms, flip angle of 140; voxel size varying from 1.0×1.0×1.0 to 1.3×1.3×1.3 mm. Scans encompassed the neck and chest and, when applicable based on patient size, the abdomen, with an average imaging duration of around 5–6 minutes.

Imaging analysis

Non-enhanced MRL images were independently evaluated by two experienced lymphatic radiologists (Initials of the radiologists, Y.Z. and M.Z.) with over 5 years and 10 years of experience, blinded to clinical outcomes of patients with consensus reached in case of discrepancies. Axial and coronal images were utilized to assess non-enhanced MRL scans, categorizing them into types I to IV based on the degree of involvement of abnormal neck and thoracic lymphatics, ranging from mild to severe according to Biko’s et al. classification (13) (Figure 1). Non-enhanced MRL neck and thoracic lymphatic vessel abnormalities were defined as follows: type I images showed minimal abnormal lymphatic vessels in the supraclavicular region and mediastinum. Type II images depicted increased abnormal lymphatic vessels in the supraclavicular region without extension into the mediastinum. Type III images displayed increased abnormal lymphatic vessels in the supraclavicular region, extending into the mediastinum. Type IV images exhibited abnormal lymphatic vessels in the supraclavicular region, extending into the mediastinum, lung parenchyma, and interstitium (13).

Figure 1 Four types based on the severity of neck and thoracic lymphatic abnormalities observed in the non-enhanced MRL. (A) A 33-year-old female with primary chylopericardium with non-enhanced MRL (coronal) staging of type I and virtually no abnormal lymphatics in the supraclavicular region and mediastinum. (B) A 32-year-old male with primary chylopericardium with non-enhanced MRL (coronal) staging of type II and increased abnormal lymphatics in the supraclavicular region that do not extend into the mediastinum. (C) A 39-year-old female with primary chylopericardium with non-enhanced MRL (coronal) staging of type III and increased abnormal lymphatics in the supraclavicular region and extending into the mediastinum. (D) A 13-year-old male with primary chylopericardium with non-enhanced MRL (coronal) staging of type IV and abnormal supraclavicular lymphatics extending both into the mediastinum and into the lung parenchyma and interstitium. MRL, magnetic resonance lymphangiography.

Clinical data

Clinical data of included patients were recorded, including patient gender, age, course of disease, clinical symptoms (shortness of breath and chest tightness), and laboratory findings including the color of pericardial effusion, triglyceride levels, and cholesterol content. Furthermore, ultrasonography results were assessed, detailing the grading of pericardial effusion quantity and the identification of pericardial effusion in another serous membrane. The findings of the non-enhanced MRL imaging were documented, covering the bilateral supraclavicular region, mediastinum, pericardium, bilateral pulmonary hilar regions, and bilateral intrapulmonary regions with abnormalities. Similarly, the chest computed tomography (CT) findings were assessed, encompassing opacity of mediastinal fat spaces, ground-glass density shadows within the lungs, pulmonary consolidation, large-grid shadows within the lungs, small-grid shadows within the lungs, intrapulmonary nodules, coarsening of intrapulmonary bronchovascular bundles, and pleural effusions. Surgical outcomes were also documented, including the duration of hospitalization before and after the surgery, changes in the amount of pericardial effusion detected through ultrasonography, and changes in chest CT. Alterations in pericardial effusion were classified as decreased, unchanged, or increased based on the results of pre-and post-surgery ultrasound assessments. Similarly, pre-and post-surgery chest CT changes were categorized as decreased, unchanged, or increased, drawing from the findings of pre- and post-surgery chest CT scans.

Statistical analysis

SPSS 26.0 statistical software was used to analyze the data. Qualitative data were presented in terms of case counts and percentages, while quantitative data adhering to a normal distribution were expressed as mean ± standard deviation and median (quartile) was used for data with no-normal distribution. Shapiro-Wilk test was used to determine whether the data fit the normal distribution. Comparison of qualitative data across groups was executed using the χ2 test or Fisher’s exact test. For quantitative data that conformed to a normal distribution, the independent samples t-test was employed. In cases where quantitative data did not conform to a normal distribution, the Kruskal-Wallis H test was conducted. Statistical significance was established at a threshold of P<0.05. The χ2 test or Fisher’s exact test was employed to compare gender, pericardial effusion color, cholesterol, cholesterol/triglyceride ratio <1, clinical symptoms, pericardial effusion grade, non-isolated pericardial effusion, and surgical outcomes among patients categorized as type IV (including changes in pericardial effusion volume before and after surgery, the opacity of mediastinal fat spaces before and after surgery, intrapulmonary ground-glass density shadows, pulmonary solidity, intrapulmonary large-grid shadows, intrapulmonary small-grid shadows, intrapulmonary nodules, thickening of intrapulmonary bronchovascular bundles, and changes in pleural effusion). The t-test was employed to assess variations in cholesterol levels across the four patient types. The Kruskal-Wallis H test was used to examine differences in age, course of disease, triglyceride levels, and duration of hospitalization across the four patient types. The logistic regression test was also used to identify independent factors influencing surgical outcomes. P value tests were two-sided.


Results

Demographic and clinical data

Fifty-six patients met the inclusion and exclusion criteria and were included for evaluation (Figure 2). The age range was from 2 to 72 years, with a median age of 24.5 years (interquartile range: 13 to 34.5 years). Twenty-six patients were male (46%) and 30 patients were female (54%). The disease exhibited a slow progression, with a wide duration range between symptom onset and diagnosis, from 20 days to 19 years. Among the patients, clinical manifestations included cough and sputum in 9 cases, chest tightness and shortness of breath in 18 cases, and asymptomatic presentations in 26 cases, dyspnea in 3 cases. Chest tightness and shortness of breath were more frequent in type III patients than those with type I, type II, or type IV, and the most common initial symptoms were cough and dyspnea. Other rare symptoms encompassed heart palpitations, chest pain, gastrointestinal symptoms, fainting, fatigue, and edema, which correlated with those reported by Kwon et al. (3). The cases had additional conditions including chylothorax (n=18), chylous ascites (n=3), chyloptysis (n=2), chyluria (n=1), lymphoedema affecting the upper limbs and face (n=1), and lymphoedema affecting the lower limbs (n=1).

Figure 2 Flow chart of study population inclusion. 104 patients with chylopericardium were included between January 2016 and December 2021, 48 were excluded and finally 56 were included in the study. 3D, three-dimensional.

Non-enhancing MRL classification

Types I or II were combined due to their comparable clinical progression and outcomes. The included cases (n=56) consisted of types I or II (n=22, 39.2%), followed by type III (n=17, 30.4%) and type IV 17 cases (30.4%). The clinical and demographic details of the distinct non-enhanced MRL types are presented in Table 1. Patients with type III were significantly older than those with type IV. Notably, chest tightness and shortness of breath were more prevalent among type III cases than both type I or II and type IV (P=0.009). No significant differences were observed in terms of gender, disease duration, pericardial effusion color, triglycerides, cholesterol, graded effusion volume, or non-isolated pericardial effusion across different types.

Table 1

Clinical and demographic data of primary chylopericardium with non-enhanced MRL staging

Variable Type I or II (n=22) Type III (n=17) Type IV (n=17) P value
Sex
   Male 9 (40.9) 8 (47.1) 9 (52.9) 0.76
   Female 13 (59.1) 9 (52.9) 8 (47.1) 0.76
Age (years) 26 [18] 35 [29]b 13 [18]b 0.046
Course of disease (years) 4 [18] 5 [7] 2 [25] 0.70
Color of chylous fluid accumulation
   Milk white 14 (63.6) 9 (52.9) 7 (41.2) 0.38
   Pink 3 (13.6) 4 (23.5) 5 (29.4) 0.52
   Bloodthirsty 1 (4.5) 1 (5.9) 3 (17.6) 0.5
   Yellow 2 (9.1) 3 (17.6) 3 (17.6) 0.7
Triglycerides (mmol/L) 2.95 [10] 2.38 [8] 2.81 [9] 0.84
Cholesterol (mmol/L) 3.09±1.109 3.12±1.354 3.19±1.118 0.97
Cholesterol/triglycerides <1 12 (54.5) 10 (58.8) 10 (58.8) 0.95
Clinical symptom
   Cough, sputum 3 (13.6) 2 (11.8) 4 (23.5) 0.73
   Chest tightness, shortness of breath 2a (9.1) 9ab (52.9) 7b (41.2) 0.009
   Asymptomatic 12 (54.5) 6 (35.3) 8 (47.1) 0.49
   Dyspnea 3 (0)
Graded effusion volume
   Mild 3 (13.6) 5 (29.4) 4 (23.5) 0.52
   Moderate 5 (22.7) 4 (23.5) 4 (23.5) >0.99
   Severe 15 (68.2) 8 (47.1) 9 (52.9) 0.49
   Non-isolated pericardial effusion 10 (45.5) 6 (35.3) 3 (17.6) 0.19

Data are expressed as n (%), median [IQR] or mean ± standard deviation. a, statistically significant difference between type I/II and type III; b, statistically significant difference between type III and type IV. MRL, magnetic resonance lymphangiography; IQR, interquartile range.

Surgical outcomes

Terminal obstruction of thoracic duct was present in all patients. All 56 patients underwent thoracic duct terminal release surgery. Thoracic duct terminal release surgery is used to treat thoracic duct end obstruction. And the outcomes of this procedure in treating primary chylopericardium across different MRL types exhibited statistically significant differences (Tables 2,3). The surgical outcomes in patients with type I or II was superior to types III and IV, the volume of postoperative chylous effusion was significantly lower in type I and II (Figure 3A,3B) (P=0.001, P=0.008, respectively). Conversely, no changes were observed in the amount of pericardial chylous fluid for type III or IV patients (Figure 3C,3D) (P=0.003, P=0.02, respectively). Hospitalization duration was similar among groups. When comparing type I or II with type IV, postoperative chest CT scans indicated fewer instances of large grid shadows (Figure 4A,4B), small grid shadows (Figure 4C,4D), and intrapulmonary bronchovascular bundles thickening (Figure 4E,4F) compared to the previous images (P=0.001, P=0.02, P=0.03, respectively). Preoperative and postoperative turbidity of mediastinal fat spaces, intrapulmonary ground-glass density shadow, pulmonary solidity, and intrapulmonary nodule changes showed no statistically significant differences among the different groups.

Table 2

Evaluation of the surgical outcomes of thoracic duct terminal adhesion release for the treatment of primary chylopericardium with different non-enhancing MRL type

Variable Type I or II (n=22) Type III
(n=17)
Type IV
(n=17)
P value
All Type
I or II vs. III
Type
I or II vs. IV
Type
III vs. IV
Volume of pericardial fluid pericardial fluid
   Decreased 17 (77.3) 4 (23.5) 6 (35.3) 0.002 0.001 0.008 0.452
   No change 4 (18.2) 11 (64.7) 9 (52.9) 0.009 0.003 0.02 0.486
   Increased 1 (4.5) 2 (11.8) 2 (11.8) 0.72 0.57 0.57 >0.99
Duration of hospitalization (d) 10 [3] 10 [6] 11 [10] 0.7

Data are expressed as n (%) or median [IQR]. MRL, magnetic resonance lymphangiography; IQR, interquartile range.

Table 3

Evaluation of the surgical outcomes of thoracic duct terminal adhesion release in the treatment of primary chylopericardium with different non-enhancing MRL staging

Variable Type I or II (n=22) Type III
(n=17)
Type IV
(n=17)
P value
All Type
I or II vs. III
Type
I or II vs. IV
Type
III vs. IV
Turbidity of the mediastinal fat space 2 (9.09) 5 (29.4) 2 (11.8)
   Decreased 2 (100) 1 (20) 0 (0) 0.17 0.14 0.33 0.71
   No change 0 (0) 3 (60) 2 (100) 0.37 0.43 0.33 >0.99
   Increased 0 (0) 1 (20) 0 (0) >0.99 >0.99 >0.99
Ground glass opacities 5 (22.7) 7 (41.2) 9 (52.9)
   Decreased 5 (100) 5 (71.4) 6 (66.7) 0.45 0.47 0.26 0.64
   No change 0 (0) 0 (0) 0 (0)
   Increased 0 (0) 2 (28.6) 3 (33.3) 0.45 0.47 0.26 0.64
Large grid shadow 7 (31.8) 4 (23.5) 13 (76.5)
   Decreased 6 (85.7) 1 (25) 1 (7.7) 0.001 0.09 0.001 0.43
   No change 1 (14.3) 1 (25) 8 (61.5) 0.11 0.62 0.07 0.29
   Increased 0 (0) 2 (50) 4 (30.8) 0.14 0.11 0.25 0.58
Small grid shadow 2 (9.1) 0 (0) 9 (52.9)
   Decreased 2 (100) 0 (0) 0 (0) 0.02 0.02
   No change 0 (0) 0 (0) 3 (33.3) >0.99 >0.99
   Increased 0 (0) 0 (0) 6 (66.7) 0.182 0.18
Thickening of bronchial vascular bundles 4 (18.2) 4 (23.5) 11 (64.7)
   Decreased 3 (75) 1 (25) 1 (9.09) 0.04 0.49 0.03 0.48
   No change 1 (25) 1 (25) 6 (54.5) 0.55 0.79 0.57 0.57
   Increased 0 (0) 2 (50) 4 (36.4) 0.51 0.43 0.52 0.54
Pleural effusion 6 (27.3) 5 (29.4) 3 (17.6)
   Decreased 4 (66.7) 0 (0) 0 (0) 0.03 0.06 0.17
   No change 0 (0) 1 (20) 1 (33.3) 0.47 0.46 0.33 0.46
   Increased 2 (33.3) 4 (80) 2 (66.7) 0.40 0.24 0.52 0.64

Values are presented as n (%). MRL, magnetic resonance lymphangiography; T2WI-MRI, T2 weighted imaging-magnetic resonance imaging.

Figure 3 CT changes of lung before and after thoracic duct terminal release surgery. (A,B) Female, a 39-year-old patient with primary chylopericardium who underwent thoracic duct terminal release surgery and type II severity in non-enhanced MRL. (A) Preoperative chest CT demonstrated a pericardial effusion (white triangle) and pleural effusion (asterisk). (B) Postoperative chest CT showed a decrease in pericardial effusion (white triangle) and right pleural effusion (asterisk) compared with the previous one. (C,D) Female, a 29-year-old patient with primary chylopericardium who underwent thoracic duct terminal release surgery and type III severity in non-enhanced MRL. (C) Preoperative chest CT demonstrated pericardial effusion (white thin arrow). (D) Postoperative chest CT showed no change in pericardial effusion compared with the previous one (thin white arrow). CT, computed tomography; MRL, magnetic resonance lymphangiography.
Figure 4 CT changes of lung before and after thoracic duct terminal release surgery. (A,B) Male, a 23-year-old patient with primary chylopericardium who underwent thoracic duct terminal release surgery and type I severity in non-enhanced MRL. (A) Preoperative chest CT showed large grid shadows (thin black arrow). (B) Postoperative chest CT indicated fewer instances of large grid shadows compared with the previous one (thin black arrow). (C,D) Female, a 72-year-old patient with primary chylopericardium who underwent thoracic duct terminal release surgery and type I severity in non-enhanced MRL. (C) Preoperative chest CT showed small grid shadows in the lower lobe of the right lung (thick black arrow). (D) Postoperative chest CT showed a decrease in small grid shadows in the lower lobe of the right lung compared with the previous one (thick black arrow). (E,F) Male, a 13-year-old patient with primary chylopericardium who underwent thoracic duct terminal release surgery and type I severity in non-enhanced MRL. (E) Preoperative chest CT showed thickening of bronchovascular bundles (black triangle). (F) Postoperative chest CT showed thickening of the bronchial vascular bundle that was better than before (black triangle). CT, computed tomography; MRL, magnetic resonance lymphangiography.

Independent factors

Age and bronchomediastinal trunk dilation emerged as independent factors influencing surgical outcomes (Table 4). The likelihood of surgical success was lower in the older group (>30 years) in comparison to the younger group (age ≤30 years), with an odds ratio (OR) of 0.918. Conversely, bronchomediastinal trunk dilation cases exhibited a higher probability of surgical success than those with undilated bronchial mediastinum (OR of 11.1). The receiver operating characteristic (ROC) curve indicated a predictive probability of age at 0.918 [95% confidence interval (CI): 0.861–0.978, P=0.001] (Figure 5). The sensitivity was 0.815. The specificity was 0.448.

Table 4

Analysis of logistic regression results affecting the surgical outcomes of thoracic duct terminal adhesion release in the treatment of primary chylopericardium

Variable OR (95% CI) P value
General information
   Age 0.918 (0.861–0.978) 0.001
   Sex 0.73 (0.15–3.64) 0.70
   Course of disease 0.99 (0.97–1.01) 0.52
Lymphatic dilatation on non-enhancing MRL
   Thoracic duct trunk 5.13 (0.47–56.06) 0.18
   End of thoracic duct 1.47 (0.26–8.47) 0.67
   Right lymphatic duct 3.12 (0.50–19.43) 0.22
   Bronchial mediastinum trunk 11.10 (1.70–72.39) 0.01
   Subclavian trunk 0.16 (0.021–1.16) 0.07
   Glacial trunk 9.67 (0.82–114.54) 0.07

OR, odds ratio; CI, confidence interval; MRL, magnetic resonance lymphangiography.

Figure 5 ROC curve shows age in predicting surgical efficacy. ROC, receiver operating characteristic.

Discussion

The present study revealed that primary chylopericardium predominantly affected young adults. Notably, the median age of type III was greater than that of type I, type II, and type IV. Gender differences were not observed, consistent with findings reported by Yu et al. (14). Savla et al. and Dori et al. (15,16) utilized dynamic contrast-enhanced MR lymphangiography, indicating associations between abnormal signals in the supraclavicular region, mediastinum, peribronchial areas, and interstitial lungs with lymphatic perfusion abnormalities and lymphatic dilation. In this study, we employed non-enhanced MRL to demonstrate abnormal signals in neck and thoracic lymphatic vessels. Abnormal lymphatic signals were detected in the supraclavicular region, mediastinum, peribronchial areas, and interstitium, indicative of lymphatic dilation in corresponding regions. The dilation typically occurred in the thoracic duct and its accessory branches, leading us to hypothesize that terminal thoracic duct obstruction underlay primary chylopericardium. Reflux into the thoracic duct and its accessory branches might contribute to the etiology of primary chylopericardium.

Biko et al. employed non-enhanced MRL to categorize primary chylopericardium patients into types I–IV based on neck and thoracic lymphangiectasia and investigated the correlation between the degree of lymphangiectasia and surgical outcomes after Fontan’s operation for congenital neonatal diseases (13). Results indicated a worse prognosis in patients with neck and thoracic lymphatic vessel anomalies extending to the lung interstitium (type IV) after Fontan surgery (13). In our study, we evaluated the correlation between the degree of neck and thoracic lymphatic vessel abnormalities and surgical outcomes in primary chylopericardium patients, utilizing the same as Biko’s classification system. Our results highlighted that neck and thoracic lymphatic vessel abnormalities assessed through non-enhanced MRL correlated with surgical outcomes. Statistically significant differences were observed in surgical outcomes among different types. Better surgical outcomes were observed for type I or II compared to type III or IV, resulting in reduced postoperative chylous fluid amounts compared to preoperative levels (P=0.001, P=0.008, respectively). Conversely, type III or IV patients experienced no change in postoperative chylous fluid amounts relative to preoperative levels (P=0.009). The length of hospitalization was comparable among different MRL staging groups. Primary chylopericardium chest CT scans illustrated mediastinal fat space turbidity, intrapulmonary ground-glass density shadows, pulmonary solidity, intrapulmonary nodules, intrapulmonary large-mesh shadows, intrapulmonary small-mesh shadows, intrapulmonary bronchovascular bundle thickening, and pleural effusion. Comparing type I or II with type IV, fewer postoperative intrapulmonary large-mesh shadows, small-mesh shadows, and bronchovascular bundle thickening were observed. Patients with type I or II exhibited abnormalities solely in the supraclavicular region, with less severe lymphatic abnormalities, leading to positive postoperative outcomes and diminished lung interstitial changes compared to the images before surgery. Conversely, patients classified as type III or IV, displayed mediastinal and pulmonary lymphatic involvement, characterized by more severe lymphatic duct dilation. We hypothesized that the worse prognosis might stem from increased resistance in returning lymph within the thoracic ducts in type III or IV. Moreover, our findings suggest that preoperative non-enhanced MRL assessment of neck and thoracic lymphatic vessel abnormality in primary chylopericardium patients may contribute to predict surgical outcomes.

This study also revealed that age and bronchomediastinal trunk dilation were independent factors influencing surgical outcomes. For the group older than 30 years old, the surgical efficacy was lower, with an OR of 0.03 and a 95% CI ranging from 0.003 to 0.220, which could be linked to the predominance of type III cases within this age group. Conversely, patients with bronchomediastinal trunk dilation exhibited significant postoperative efficacy after thoracic duct terminal release surgery, with an OR of 11.10 and a 95% CI ranging from 1.70 to 72.39. It is now understood that lymphatic fluid draining from the pericardial cavity navigates through the epicardial lymphatic plexus, subepicardial lymphatic plexus, left lymphatic trunk of the heart, and mediastinal lymph nodes into the left bronchomediastinal trunk, and partially through the right lymphatic trunk to the mediastinal lymph nodes (17). When thoracic duct outlet pressure rises due to thoracic duct obstruction or dilation, chylous fluid may reflux into the cervical trunk, subclavian trunk, and bronchomediastinal trunk, where pressure is comparatively lower. We hypothesize that transbronchomediastinal trunk reflux constitutes one of the primary pathways leading to chylopericardium. Bronchomediastinal trunk dilation group had good surgical outcomes.

This study’s primary limitations encompass four aspects. It was a retrospective study with selection bias. Secondly, the sample size is relatively small, and further studies with larger cohorts are warranted. Thirdly, this study exclusively focuses on primary chylopericardium, leaving room for exploration into whether neck and thoracic lymphatic vessel abnormalities in secondary chylopericardium correlate with surgical outcomes. Lastly, the next step is to investigate using dynamic contrast enhanced MRI imaging.

Overall, this study demonstrated an association between non-enhanced MRL neck and thoracic lymphatic vessel abnormalities and surgical outcomes in primary chylopericardium patients. More severe neck and thoracic lymphatic abnormalities were associated with a worse surgical outcomes. Age and bronchomediastinal trunk dilation emerged as independent factors on surgical outcomes. Thus, preoperative utilization of non-enhanced MRL for severity of lymphatic abnormalities classification in primary chylopericardium patients offers a noninvasive means of assessing surgical risk.


Acknowledgments

Funding: This work was supported by the National Natural Science Foundation of China (61876216).


Footnote

Reporting Checklist: The authors have completed the STROBE reporting checklist. Available at https://qims.amegroups.com/article/view/10.21037/qims-24-144/rc

Conflicts of Interest: All authors have completed the ICMJE uniform disclosure form (available at https://qims.amegroups.com/article/view/10.21037/qims-24-144/coif). The authors have no 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 (as revised in 2013). The study was approved by Institutional Ethics Board of Beijing Shijitan Hospital (No. IIT2024-059-001) and individual consent for this retrospective analysis was waived.

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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Cite this article as: Zhang Y, Sun X, Liu M, Li X, Zhang M, Duan Y, Wang R. Association between lymphatic abnormalities in the neck and thorax in primary chylopericardium and surgical outcomes evaluated by non-enhanced magnetic resonance (MR) lymphangiography. Quant Imaging Med Surg 2024;14(8):5961-5972. doi: 10.21037/qims-24-144

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