A novel minimally invasive surgical technique (LONG procedure) for treating chylopericardium

Introduction

Chylopericardium, which was first reported by Hasebrock in 1888, is a rare disease characterized by the accumulation of chylous lymph in the pericardial cavity (1). In 1954, Groves and Effler proposed primary chylopericardium to be an independent disease (2). The lymphatic circulation of the pericardium has no specific trunk but drains into the mediastinum, paratracheal lymph nodes, and lymph nodes near the diaphragm through small lymphatic vessels. Various causes of chylopericardium have been suggested, including lymphatic malformation, abnormal lymphatic pathway, abnormal lymphatic valve function, infection, venous thrombosis, tumor, and trauma. When all definite causes are excluded, the condition is classified as primary chylopericardium (3-5).

Due to the low incidence of chylopericardium, the related research mostly consists of case reports or case series, while large-sample clinical trials, consensus, and guidelines are lacking. Currently, the treatment of chylopericardium includes conservative therapy and surgical therapy. Conservative treatments include fasting or a fat-free diet, intravenous injection of somatostatin or octreotide, parenteral nutrition, and pericardial catheter drainage. However, for chylopericardium, the recurrence rate is as high as 50–60% with conservative treatment. Patients have to eat a fat-free diet for a long time and are prone to malnutrition. And when the pericardial effusion accumulated a lot, the patients need to accept pericardial puncture and drainage repeatedly to relieve the cardiac tamponade. Chemically fixing the pericardial cavity, such as via chemical pleurodesis, with the heart in the pericardium involves considerable risk. Therefore, surgical therapy is considered as the last resort for treating chylopericardium. Commonly used surgical techniques include thoracic duct release, thoracic duct and abnormal lymph vessel ligation, and pericardial window (5-10).

However, the relevant literature suggests a high recurrence rate of chylopericardium even after thoracic duct release and ligation. Some patients were found their thoracic duct tapered again after few months of thoracic duct release surgery. While some criss-crossed fistulous lymph-vesseles were found in some patients that could not be ligated or embolized completely. These are the reasons lead to the recurrence. Pericardial window is now regarded as the most effective treatment for chylopericardium, with the recurrence rate less than 5% (10). But the anatomy of the pericardium is not thorough in the traditional pericardial fenestration, which may result in mediastinal effusion and hemothorax in some patients we met before. With this in mind, we reevaluated traditional pericardial fenestration based on our own treatment concept and the characteristics of the pericardial lymphatic structure, drawing from over 10 years of clinical experience in diagnosing and treating chylous diseases. We suspected that the traditional pericardial fenestration may not be completely effective for treating chylopericardium. Consequently, we designed a novel minimally invasive pericardial fenestration surgical technique, the LONG procedure, and successfully cured 7 chylopericardium patients. Its efficacy and technical characteristics would be discussed in this study, with the aim of providing valuable insights into the surgical treatment and management of chylopericardium. We present this article in accordance with the SUPER reporting checklist (available at https://jtd.amegroups.com/article/view/10.21037/jtd-2024-2111/rc).

Methods

Case series: general medical history of the patients

The clinical data of chylopericardium patients admitted to the lymphatic surgery department between January 2018 and June 2024 were retrospectively analyzed, included the patients’ medical history, imaging examination, pericardial effusion analysis, operative details, drainage output, length of hospital stay, and follow-up results. The indicators data were recorded and analyzed. A total of seven male patients, ranging in age from 7 to 35 years old, were included in this study. The time interval between the initial onset of symptoms and their first visit to our hospital varied from 3 months to 10 years. Common symptoms observed in all patients included chest tightness, palpitations, and shortness of breath. Pericardiocentesis and drainage had been performed on all patients at other hospitals before their admission to our hospital. Four patients experienced pulmonary infections, which were successfully treated with antibiotics. Two patients received empirical antituberculosis therapy but did not show any significant improvement. One patient opted for conservative therapy but experienced recurrent pericardial effusion for 10 years despite a normal diet. Five patients had been following a fat-free diet for at least 6 months. Additionally, three patients had undergone thoracic duct adhesiolysis, one patient had undergone bilateral bronchial and mediastinal lymphatic ligation, and another patient had accepted thoracic duct embolization. However, none of these surgical procedures resulted in the resolution of the chylopericardium.

Upon admission, electrocardiogram examinations revealed no obvious abnormalities in any of the seven patients. Chest computed tomography (CT) scans and echocardiography confirmed the presence of pericardial effusion in all patients (Figure 1). Four patients had massive pericardial effusion, while the remaining three had moderate pericardial effusion. Two patients had recently undergone pericardial drainage at other hospitals due to chest tightness. None of the patients reported any discomfort while at rest, but they did experience chest tightness and palpitations when walking quickly or exercising. There was no history of other surgery or trauma in any of the patients, and they had undergone various examinations at other hospitals to exclude common causes of chylopericardium, such as tumors, immune diseases, lymphohematopoietic diseases, and tuberculosis, among other conditions.

Figure 1 Pericardial effusion detected with computed tomography in two patients.

After ruling out these common causes, all patients were diagnosed with primary chylopericardium by meeting two or more of the following criteria (11,12): (I) effusion with a yellow or light-red color, (II) triglyceride levels higher than 1.25 mmol/L, (III) the effusion predominated by mononuclear cells and lymphocytes, with negative results for bacterial cultures, and (IV) a positive result from a chyle test. Table 1 presents the general information of the patients. Among them, cases 2–6 exhibited low chylous fluid triglyceride levels due to an extended fat-free diet, and their chylous fluid appeared light yellow or red (Figure 2A,2B); meanwhile, in case 1 and 7, the fluid was milk white in color (Figure 2C).

Figure 2 Appearance of chylous fluid in the patients.

Written informed consent was obtained from each patient and their legal guardians. The study was conducted in accordance with the Declaration of Helsinki (as revised in 2013) and was approved by the Ethics Committee of The Affiliated Guangdong Second Provincial General Hospital of Jinan University (ethics No. 2024-KY-KZ-307-01).

Preoperative preparations and requirements

Blood routine, liver and kidney function, electrolyte, coagulation function, infectious disease, routine urine and bowel, electrocardiography, chest X-ray, plain chest CT, and cardiac ultrasound examinations were performed for all patients after admission to rule out surgical contraindications. Pericardial effusion samples were obtained for examination from patients with drainage tubes or during the surgery. All patients began a fat-free diet after admission, which included fasting for 8 hours and abstaining from drinking for 4 hours before surgery. Skin was prepared in the thoracic operative field.

Surgical approach of the LONG procedure

General anesthesia was administered by a senior anesthesiologist, and the operation was performed by an experienced senior thoracic surgeon who was assisted by a junior thoracic surgeon and a scrub nurse in the operating room.

The specific steps of the LONG procedure are illustrated in Figure 3. (I) Following tracheal intubation under general anesthesia, the patient was placed in the right lateral position. A 2-cm fifth costal incision, between the anterior axillary line and the midaxillary line, was made in routine fashion to access the chest. The incision could be adjusted as necessary. Thoracoscopy was introduced into the thoracic cavity through the incision for observation purposes. (II) The thoracic cavity was carefully examined to identify and remove any pleural adhesions between the lung and the pericardial surface. The left lung was then gently pushed backward to expose and confirm the upper, lower, anterior, and posterior boundaries of the left parietal pericardium as well as the location of the phrenic nerve and accompanying vessels on the surface of the left pericardium (Figure 3A). (III) A small anterior incision was made on the parietal pericardium, about 3 cm anterior to the phrenic nerve, revealing the presence of chylous fluid pouring into the left thoracic cavity. It was necessary to ensure that the anesthesiologist was monitoring the patient’s heart rate and blood pressure during this step (Figure 3B,3C). (IV) All the chyle fluid in the thoracic and pericardial cavities was carefully aspirated, and the volume of the effusion was recorded. The incision was then extended further upward, near the pericardial reflection of the pulmonary artery root and downward to the diaphragmatic reflection of the pericardium, thereby creating an anterior pericardial window (Figure 3D-3F). (V) Following this, a small incision was made about 3 cm behind the phrenic nerve at the lateral wall of the parietal pericardium (Figure 3G,3H). (VI) Along the phrenic nerve, the incision on the lateral wall of the pericardium was extended upward to the left pulmonary vein and downward to the reflection of the diaphragmatic surface of the pericardium, forming a posterior pericardial window. It is crucial to protect the phrenic nerve and its accompanying vessels while performing the anterior and posterior pericardial incisions (Figure 3I,3J). (VII) Pathological biopsies were obtained as required, involving the excision of a small piece of the parietal pericardium (Figure 3K). (VIII) The free and incised parietal pericardium, both before and after the phrenic nerve, was folded and encircled around the phrenic nerve. The anterior and posterior incision margins were then aligned and fixed using Prolene sutures in consecutive stitching, ensuring complete fenestration of the anterior and posterior windows of the pericardium and preventing the failure of fenestration due to the rebound of the incised pericardium (Figure 3L,3M). (IX) Finally, the pericardial cavity was washed out with warm water, a 16-Fr chest tube was inserted in the lower part of the thoracic cavity, and the incision was sutured to complete the procedure (Figure 3N,3O). The key points of the LONG procedure are illustrated in Figure 4.

Figure 3 Step-by-step illustration of the LONG procedure.

Figure 4 Key points of the anatomical procedure for the parietal pericardium. Left: intraoperative view. Right: corresponding parietal pericardium area. (A) Left parietal pericardial operation field and phrenic nerve. The red dashed line indicates the pericardial incision. (B) The position of the anterior pericardial window. (C) The position of the posterior pericardial window. (D) Suture site of the parietal pericardium on both windows.

Postoperative management and follow-up

All patients accepted a fat-free diet after surgery, ate high-protein foods (egg white, chicken breast, lean meat, fat-free milk), and could eat rice, vegetables, and fruits as they would normally to meet their caloric needs. The draining of the chylous fluid was maintained, and all patients were treated with oxygen inhalation and analgesic drugs for two days after surgery. When the drainage volume was larger than 500 mL/d, a transfusion of electrolyte supplementation, intravenous nutrition (intravenous fat emulsion, amino acids), and human serum albumin were deemed necessary. When the drainage flow of the effusion decreased significantly (<50 mL/d) and became clear, the drainage tube was clamped for about 5–7 days, and chest radiography or chest CT was reviewed. If there was no significant accumulation of fluid in the chest cavity, the drainage tube could be removed. After discharge, diet control was continued, and small doses of diuretics (furosemide, spironolactone) were administered for 2 weeks. The patients returned to hospital every 1 month for reexamination.

Statistical analysis

SPSS 20.0 (IBM Corp., Armonk, NY, USA) was used for statistical analyses. Measurement data, including operation time, intraoperative blood loss, and duration of postoperative stay are expressed as the minimum – maximum value. The change in the chyle effusion volumes after surgery was recorded in a line chart.

Results

All patients underwent a successful LONG procedure, with an operation time of 54 to 95 minutes and minimal intraoperative blood loss (1–5 mL). The pathological results of pericardial biopsy all indicated chronic pericardial inflammation and lymphocyte infiltration, and no pathogens or tumors were found (Figure 5). All patients accepted thoracic drainage after surgery and were administered intravenous nutrition support as appropriate. The volume of the chyle effusion was reduced in 7 patients after 5–30 days of drainage (Figure 6). After the drainage tube was clamped and observed for 5–7 days, no recurrence of fluid accumulation was found in chest radiographs or ultrasound, and the drainage tube was removed. After discharge, all patients continued their fat-free diet and took diuretics regularly for 2 weeks. Chest radiography and ultrasound were reviewed every other month in the first 3 months after discharge, and chest CT was reviewed if necessary. Follow-up was conducted every 3 months, and then annually after 1 year. When there was no recurrence of fluid accumulation after 3 to 6 months, patients were advised to eat a small amount of fatty food—such as egg yolks, whole milk, or cooking oil—and to gradually increase consumption until retuning to a normal diet. The patients were followed up for 3 months to 5 years, and no recurrence of pericardial and pleural effusion or other complications were observed. Among the patients, cases 1–6 gradually returned to a normal diet 1 year after surgery, while case 7 had no pleural or pericardial effusion and ate a small amount of fatty food 3 months after surgery. At the time of writing, long-term follow-up is ongoing.

Figure 5 Pathological analysis of the pericardial biopsy samples. The parietal pericardium specimen stained with hematoxylin and eosin at a magnification of ×20.

Figure 6 The trend of thoracic drainage volume after surgery in the 7 patients.

Discussion

Chylopericardium and chylothorax are predominantly treated via thoracic surgery. However, these conditions have a low incidence, an unknown etiology, and a tendency to recur, and thus treatment is challenging. Moreover, the circumstances of the medical system in China often mean the length of hospital stays for these patients is limited. As a result, most cases are managed conservatively at home, leading to a scarcity of specialists focused on the treatment of these diseases. Furthermore, the therapeutic approaches examined in previous studies over the past decade are not particularly diverse (5,7,8,10,11,13).

Over the past 10 years, our team has been dedicated to refining the treatment of chylopericardium and chylothorax. We have experimented with various treatment approaches, such as classic fasting combined with the intravenous use of somatostatin or octreotide, chemical pleurodesis for refractory chylothorax (14,15), and traditional pericardial fenestration. In recent years, we have encountered several patients with chylopericardium and chylothorax who did not respond to thoracic duct adhesiolysis and/or ligation. However, by modifying our treatment methods and stimulating pleural resorption, we have been able to alleviate or even cure the conditions in most of these patients. This observation has greatly inspired us, as it supports the potential for collateral circulation reconstruction and recanalization within the lymphatic system.

Anatomy and molecular biology serve as the foundation of modern medicine, enabling us to understand pathological processes and devise evidence-based approaches for treating diseases at the organ, tissue, and molecular levels. This guiding principle has led to the adoption of techniques such as vessel ligation for hemostasis, lymphatic decompression for lymphatic stenosis, and ligation for lymphatic leakage. Although the exact efficacy of thoracic duct ligation remains uncertain, there are few alternatives to this nearly decade-old mainstream approach. In an attempt to acquire anatomical evidence, some researchers even have used lipiodol to perform lymphography (16), with the aim of identifying lymphatic fistulas or stenoses that can be directly treated by ligation or embolization. When these patients were admitted to our department for evaluation, it was discovered that some had experienced limb edema due to lipiodol blocking lymphatic vessels or aggravation of chylous leakage due to lipiodol obstruction of the thoracic duct.

Extensive and detailed investigations of the anatomical structure of pericardial lymphatic circulation have been conducted. However, due to the low number of chylopericardium cases, this subject has not attracted significant research attention. As early as 1992, Li et al. observed the presence of numerous lymphatic pores in the human pericardial mesothelium that connected with the surrounding lymphatic capillaries and ultimately merged into the vascular system. Animal experiments demonstrated that these lymphatic pores actively absorbed macromolecular substances, with the number of open pores increasing significantly with the increase in pericardial effusion (17). Eliskova et al. reported the distribution and drainage patterns of human pericardial lymphatic vessels through staining in 1995 (18). Their study revealed that there is no main trunk for pericardial lymphatic circulation but rather a distribution of lymphatic vessels in the upper and lower regions, extending from the front to the back. These vessels drain lymphatic fluid from the pericardial cavity to the mediastinal, paratracheal, or diaphragmatic lymphatic vessels and lymph nodes. They further reported numerous communication branches present between the lymphatic vessels in the parietal pericardium and the pleural lymphatic vessels. The findings from these two studies directly verified the strong circulatory compensatory ability of the pericardial lymphatic system. This serves as the core principle of the LONG procedure in the treatment of chylopericardium and is evidence against recommending thoracic duct ligation. Rochefort believed that the probability of postoperative chylous recurrence is lower when right pericardial fenestration is performed concurrently with thoracic catheter ligation, but this view was based only on a few case reports (10). Instances of patients recovering well with no thoracic catheter ligation after pericardiectomy have also been reported (5), and some researchers have even proposed performing left pericardial fenestration to prevent pericardial effusion after cardiac surgery (19).

It was believed that chylopericardium is caused by abnormal communication between the thoracic duct and the pericardial cavity leading to the regurgitation of chylous fluid into the pericardial cavity (3,20,21). Based on this understanding, to cure chylopericardium, clinicians have relied on fasting, the use of somatostatin to reduce the absorption and production of lymph fluid, and the ligation of abnormal lymphatic vessels. However, recurrence of chylopericardium occurs in many patients who have undergone these treatments. Unlike blood vessels, lymphatic vessels have weaker walls and valve structures with numerous small branches. An approach that involves opening the chest in an attempt to identify and repair these so-called diseased lymphatic vessels under a microscope is inherently unreasonable and unrealistic. Consequently, we believe that blocking lymph leakage should not be solely relied upon in the treatment if chylopericardium, but with the current level of medical technology, this is not practicable.

The optimal treatment approach for chylopericardium should aim to establish alternative, more efficient pathways through which lymphatic fluid can return, which would ultimately achieve long-term stability and cure. Traditional pericardial fenestration, designed by researchers for the treatment of chylopericardium, considers this to an extent; however, it involves certain shortcomings (22-24). The area of the pleura is substantially larger than that of the pericardium, and the lymphatic circuit within the pleura is considerably more extensive than that of the pericardium. In cases of isolated chylous pericardium, the pleural cavity presents itself as the optimal route for lymph reflux due to its robust resorption capacity.

Although traditional pericardial fenestration drains chyle into the thoracic cavity, creating a window by removing a portion of the parietal pericardium is not entirely rational. The studies of the anatomical structure of the pericardium suggest that the parietal pericardium itself contains numerous lymphatic capillaries, which interconnect with the lymphatic vessels of the mediastinum and pleura and can be utilized (16,17). However, the direct resection of the parietal pericardium disrupts the integrity of the pericardial lymphatic vessels, reduces the surface area available for lymph resorption, and diminishes efficiency. Additionally, if only one incision is made in the parietal pericardium to create the window, there is a risk of the surgical field becoming adhered to prepericardial fat, mediastinal pleura, or even lung tissue, potentially leading to long-term closure of the window.

To address the limitations of traditional pericardial fenestration, we developed the LONG procedure, taking into account the anatomical structure of pericardial lymphatic tissue. Our aim is to promote effective drainage of effusion while preserving the integrity of the pericardial structure. The key features of the LONG procedure are as follows: (I) the lymphatic vessels of the pericardium predominantly run vertically, concentrating primarily at the upper and lower poles of the pericardium. The pericardium also contains numerous lymphatic capillaries that communicate with mediastinal pleural lymphatic vessels. Therefore, the incision on the pericardium is a longitudinal incision parallel to the phrenic nerve, as this can avoid the severing of the original lymphatic vessels. (II) The original lymphatic structure and function of the pericardium can be preserved without the need for resection. Even after the incision, the pericardium maintains its role in protecting the heart. (III) The pericardial incision is secured by reverse folding on both sides, ensuring a sufficiently large drainage area for the pericardial windows. The thick reverse-folding site of the pericardium minimizes the likelihood of the windows being blocked by surrounding tissues. Moreover, the large pericardial reflex facilitates full contact and adhesion with the pleura, thereby establishing a new route of lymphatic circulation between the pericardium and the pleura. These modifications in the LONG procedure offer potential advantages over traditional pericardial fenestration, enabling more effective drainage, promoting better resorption of chylous effusion, and preserving pericardial structure and function.

Thus far, we have successfully conducted the LONG procedure in 7 patients with chylopericardium. This procedure is typically performed using minimally invasive single-incision thoracoscopic surgery, resulting in reduced pain and faster recovery. The high absorptive capacity of the pleura allows for a fat-free or low-fat diet postsurgery without causing pericardial effusion. In this study, the effusion in some patients was initially drained through chest tubes, allowing the pleura to absorb it over time. In most patients, the chylous fluid decreased to less than 50 mL/day after 2–4 weeks, and in some cases, it completely disappeared. Patients were advised to control their water intake or use diuretics in the short-term after discharge, and the longest follow-up period was 5 years. Fortunately, no significant recurrence of pericardial or left pleural chylous effusion was observed in any patient; however, the long-term effects of the LONG procedure remain need to be observed.

Limitations

Despite the encouraging findings, it is important to acknowledge certain limitations. First, the number of cases in our study was relatively small, and individual differences among patients might have influenced the results. Furthermore, we have not yet directly confirmed through experiments that pericardial chylous fluid is absorbed through the pleura and enters the recirculating process, and thus should be confirmed in further research.

Conclusions

Our study demonstrated promising initial results for the surgical treatment of chylopericardium with the LONG procedure, particularly in patients for whom previous conservative treatments and lymphatic surgeries had failed. Our findings constitute valuable clinical insights into the treatment of chylopericardium and can hopefully contribute to the advancement of medical research in this field. Additional studies and clinical trials should be conducted to confirm the potential of the LONG procedure in the management of chylopericardium and to determine if its broader application is warranted.

Acknowledgments

Funding: This work was supported by a grant from the Medical Science and Technology Research Fund Project of Guangdong Province (No. C2023009).

Footnote

Reporting Checklist: The authors have completed the SUPER reporting checklist. Available at https://jtd.amegroups.com/article/view/10.21037/jtd-2024-2111/rc

Data Sharing Statement: Available at https://jtd.amegroups.com/article/view/10.21037/jtd-2024-2111/dss

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Conflicts of Interest: All authors have completed the ICMJE uniform disclosure form (available at https://jtd.amegroups.com/article/view/10.21037/jtd-2024-2111/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.Written informed consent was obtained from each patient and their legal guardians. The study was conducted in accordance with the Declaration of Helsinki (as revised in 2013) and was approved by the Clinical Ethics Committee of The Affiliated Guangdong Second Provincial General Hospital of Jinan University (ethics No. 2024-KY-KZ-307-01).

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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