Resection of a ganglioneuroma encasing major blood vessels using three-dimensional laparoscopy combined with organ suspension: A case report

Abstract

BACKGROUND

Ganglioneuroma is a rare, well-differentiated, slow-growing benign tumor of the peripheral nerves, with surgical resection being the only curative treatment. Surgical resection of ganglioneuromas encasing major blood vessels remains a substantial clinical challenge. Traditionally, these cases often require open abdominal surgery or combined organ resections, and in some instances, the tumors are considered unresectable. Currently, no reports have described the resection of such tumors via laparoscopy.

CASE SUMMARY

A 35-year-old woman was admitted to our hospital after the incidental discovery of a retroperitoneal space-occupying lesion. Imaging revealed a mass with the celiac axis and superior mesenteric artery passing through it. A neurogenic tumor was suspected, with ganglioneuroma being the most likely diagnosis. Following comprehensive preoperative preparation, the retroperitoneal tumor was resected using a three-dimensional laparoscopy combined with an organ suspension technique. The surgical approach involved incising the tumor along the vascular axis and conducting meticulous, vascular-preserving tumor excision. The operation lasted approximately 458 minutes, with an estimated blood loss of 50 mL. The patient was discharged on the 8th postoperative day. A transient liver injury occurred after surgery but improved rapidly. After 11 months of postoperative follow-up, no complications or tumor recurrence were observed.

CONCLUSION

This case illustrates the feasibility of minimally invasive laparoscopic resection for retroperitoneal ganglioneuromas encasing major blood vessels.

Key Words: Ganglioneuromas; Retroperitoneal; Three-dimensional laparoscopy; Organ suspension; Case report

Core Tip: Ganglioneuroma is a rare, well-differentiated, slow-growing benign tumor, with surgical resection being the only curative treatment. However, resecting ganglioneuromas that encase major blood vessels presents substantial technical challenges. Here, we present the first case of a retroperitoneal ganglioneuroma encasing the celiac axis and superior mesenteric artery, successfully resected with preservation of all vital vessels using three-dimensional laparoscopic surgery combined with organ suspension techniques. This case highlights the feasibility of minimally invasive laparoscopic approaches for managing complex retroperitoneal ganglioneuromas encasing major blood vessels.

INTRODUCTION

Ganglioneuroma is a rare benign tumor originating from primitive neural crest cells surrounding the paravertebral nerve plexus. It can occur in different body parts, most commonly in the retroperitoneum (32%-52%), posterior mediastinum (39%-43%), and then cervical region (8%-9%)[1,2]. Histologically, it primarily comprises mature Schwann and ganglion cells within a fibrous stroma[3].

This disease typically begins insidiously, and many patients exhibit no obvious clinical symptoms. It is often detected during routine physical examinations or while undergoing tests for unrelated conditions. Symptoms may appear in a few patients due to local tumor expansion and compression of surrounding structures, such as interruption of venous blood flow, lower abdominal pain, vomiting, weight loss, and neurological deficits. In some cases, hormone secretion by the tumor can also cause clinical manifestations of autonomic nervous system dysfunction. In extremely rare cases, it may progress to a malignant peripheral nerve sheath tumor[4,5].

Currently, no effective medical therapies exist for retroperitoneal ganglioneuromas, making surgical resection the primary treatment option[6]. Before the refinement of laparoscopic techniques, most cases were managed through open surgery. However, advancements in minimally invasive surgery have enabled the laparoscopic resection of many tumors. Laparoscopic resection is typically considered simple for ganglioneuromas within the adrenal gland, with numerous successful cases reported for tumors closely abutting major blood vessels[7,8]. However, ganglioneuromas encasing critical vascular structures pose substantial surgical challenges, even when accessed via open techniques[9,10]. To date, reports on the successful laparoscopic resection of such complex cases are lacking, highlighting the requirement for further technical innovation and advanced surgical expertise in managing these challenging tumors. Herein, we report a novel surgical approach involving the resection of retroperitoneal ganglioneuromas encasing major blood vessels using three-dimensional (3D) laparoscopy combined with an organ suspension technique.

CASE PRESENTATION

Chief complaints

A 35-year-old woman was admitted to the hospital on April 28, 2024, following the incidental discovery of a retroperitoneal space-occupying lesion the previous day.

History of present illness

The patient presented to our outpatient department with a complaint of a cough the previous day. A non-contrast computed tomography (CT) scan revealed a space-occupying lesion in the left retroperitoneum, prompting further evaluation with contrast-enhanced CT. Currently, the patient exhibits no symptoms, including abdominal pain, abdominal distension, nausea, vomiting, or dizziness. She was subsequently admitted to the hospital for further management.

History of past illness

The patient presents without history of abdominal surgery, smoking, alcohol use or hypertension.

Personal and family history

All other personal and family medical histories were noncontributory.

Physical examination

No skin or sclera jaundice was observed. The abdomen was soft without tenderness or rebound tenderness. No abdominal mass was palpable, and Murphy’s sign and shifting dullness were negative. The bilateral renal punch was negative.

Laboratory examinations

Blood routine, biochemistry, tumor markers, glucocorticoids, renin, angiotensin II, aldosterone, adrenocorticotropic hormone, and other tests were all within normal ranges.

Imaging examinations

Abdominal contrast-enhanced CT revealed a slightly hypodense left retroperitoneum mass with heterogeneous internal density. The largest cross-sectional diameter measured approximately 8.5 cm × 5 cm. Progressive mild enhancement was observed on contrast-enhanced imaging. The mass laterally displaced the left adrenal gland and encased the celiac axis and superior mesenteric artery without considerable vascular lumen stenosis. A neurogenic tumor was suspected, with ganglioneuroma considered the most likely diagnosis (Figure 1A and B).

Figure 1 Enhanced computed tomography scan depicting a tumor located posterior to the pancreas and adjacent to the hepatic portal vein with progressive enhancement. The maximum cross-sectional dimensions of the tumor are approximately 8.5 cm × 5 cm. A: The tumor completely encases the celiac axis, common hepatic artery, and splenic artery and is closely adjacent to the abdominal aorta; however, no notable luminal stenosis is observed in these vessels; B: The tumor completely encases the superior mesenteric artery and is closely associated with the superior mesenteric, splenic, and left renal veins. Arrow: Correspondingly mark the blood vessels or tumors; Red line: The boundary of the tumor.

Contrast-enhanced magnetic resonance imaging revealed a solid-cystic mass in the left retroperitoneum. On diffusion-weighted imaging, the lesion exhibited slightly hyperintense signals. The mass measured approximately 8.6 cm × 5.6 cm, with progressive enhancement observed on contrast-enhanced sequences. A ganglioneuroma was suspected.

FINAL DIAGNOSIS

Postoperative pathological examination confirmed ganglioneuroma. Immunohistochemical analysis revealed positive tumor cells for neurofilament, SRY-related HMG-box 10 protein, and S-100 protein (Figure 2A-D).

Figure 2 Hematoxylin-eosin staining and immunohistochemical results. A: Hematoxylin-eosin staining of the ganglioneuroma (magnification: × 200); B-D: Immunohistochemical staining demonstrates that the tumor cells are positive for neurofilament, SRY-related HMG-box 10 protein, and S-100 protein (magnification: × 200).

TREATMENT

Following meticulous preoperative preparation, a retroperitoneal tumor resection was performed on May 7, 2024, utilizing 3D laparoscopy combined with organ suspension (Figure 3A). The procedure involved carefully incising the tumor along the vascular axis (Figure 3B) and performing a vascular-preserving excision (Figure 4A and B). The surgery lasted approximately 458 minutes, with an estimated blood loss of 50 mL. Postoperative pathological examination revealed that the tumor measured approximately 6 cm × 9 cm × 14 cm, exhibiting a well-defined capsule and light yellow coloration (Figure 5).

Figure 3 Intraoperative images. A: A 10-Fr red rubber urinary catheter was passed beneath the pancreas and suspended from the abdominal wall, effectively exposing the retroperitoneal space; B: An ultrasonic scalpel was used to incise the tumor along the vascular axis, thereby exposing the celiac axis. The vascular wall remained intact without evidence of tumor cell infiltration or encroachment. Arrow: Correspondingly mark the blood vessels.

Figure 4 Postoperative images. A: The left gastric artery was excised. After tumor removal, the celiac axis, common hepatic artery, splenic artery, abdominal aorta, and inferior vena cava were clearly visible in the images; B: Following tumor excision, the superior mesenteric artery, abdominal aorta, left renal vein, left renal artery, and left ovarian vein were distinctly depicted. All vital abdominal blood vessels were successfully preserved. Arrow: Correspondingly mark the blood vessels.

Figure 5 Surgical specimen following resection. The tumor had a capsule on its surface and exhibited a light yellow color. As measured by postoperative pathology, the tumor size was approximately 6 cm × 9 cm × 14 cm.

OUTCOME AND FOLLOW-UP

The patient was discharged on the 8^th postoperative day. Although transient liver injury occurred after surgery, it improved rapidly (Figure 6). No pancreatic fistula, chylous fistula, or other complications were observed. After 11 months of postoperative follow-up, no complications or tumor recurrence were observed. The patient fully regained the ability to perform daily activities and work, expressing high satisfaction with the treatment outcomes. To monitor tumor status, we recommended enhanced abdominal CT scans every six months. Additionally, we will continue to monitor the patient's condition closely.

Figure 6 Changes in transaminase levels during hospitalization. The black line represents aspartate aminotransferase, whereas the blue line denotes alanine aminotransferase. Surgery was performed on day nine of hospitalization. On the day of operation, the levels of both transaminases dramatically increased, peaking on the second postoperative day. Afterward, the levels gradually declined, approaching the normal range by the time of discharge. ALT: Alanine aminotransferase; AST: Aspartate aminotransferase.

DISCUSSION

Ganglioneuroma is a rare, well-differentiated, slow-growing benign tumor of the peripheral nervous system. It typically grows along periorgan spaces, encasing adjacent blood vessels without causing vascular occlusion or stenosis. Ganglioneuromas can develop anywhere along the peripheral autonomic ganglia[11]. Given the nonspecific clinical presentation and limited diagnostic utility of laboratory tests, imaging modalities are currently the primary method of diagnosis. However, a definitive diagnosis requires pathological confirmation, and surgical resection remains the only curative approach, with complete excision offering the potential for cure and minimizing the risk of local recurrence. The prognosis is generally excellent[12,13].

Ganglioneuromas are typically soft in texture due to the abundant mucinous matrix within the tumor. On CT, they often appear as low-density masses, with attenuation lower than that of adjacent muscle tissue at the same level[14]. Generally, ganglioneuromas possess a well-defined capsule and exhibit clear margins but tend to grow in a pseudopod-like or infiltrative manner along the spaces between surrounding organs and may compress and encase adjacent blood vessels. Ganglioneuromas are hypovascular tumors that typically exhibit no enhancement or only mild to moderate enhancement during the delayed phase of contrast-enhanced imaging. Approximately 10%–25% of ganglioneuromas may exhibit calcifications, usually in the form of pinpoint, punctate, or thin linear deposits along the[15]. This aligns with the CT features observed in the present case, although no calcifications were identified on imaging in this patient. Due to the characteristic of encircling blood vessels, ganglioneuromas are often misdiagnosed as malignant tumors before surgery, which may result in the tumor being deemed unresectable or unnecessary expansion of the resection scope. When needed, a puncture biopsy can be employed for a definitive diagnosis. However, in this case, given the tumor’s characteristic imaging features, both CT and magnetic resonance imaging provided a relatively definitive diagnosis suggestive of ganglioneuroma; therefore, a preoperative biopsy was not performed. Instead, an intraoperative biopsy was conducted, and a frozen-section pathological examination was promptly carried out prior to tumor resection. Surgical removal of the tumor was initiated only after its benign nature was conclusively confirmed by the histopathological findings.

Vascular invasion is a hallmark of malignant tumors. Malignant tumors encase blood vessels and infiltrate vessel walls, resulting in luminal stenosis. No clear boundary typically exists between the tumor and the vessel wall. Radical resection of malignant tumors requires simultaneous removal of the involved blood vessels. However, the celiac axis and superior mesenteric artery are among the most critical arteries in the abdominal cavity, supplying blood to essential organs, such as the liver, stomach, pancreas, small intestine, and right half of the large intestine. Consequently, malignant tumors that invade the celiac axis or superior mesenteric artery are typically considered unresectable by radical surgery, with nonsurgical treatments often preferred.

In contrast to malignant tumors, ganglioneuromas encase blood vessels but have a distinct boundary between the tumor and vessel walls, with no vascular infiltration. In this case, the tumor was incised along the vascular axis and meticulously dissected from the vessel walls, allowing complete removal while preserving vital abdominal blood vessels. Although this surgical technique carries a risk of tumor residue or dissemination, the benign nature of ganglioneuromas substantially reduces the likelihood of this concern. During the 11-month postoperative follow-up, enhanced CT scans were performed, with no evidence of tumor recurrence observed. The current follow-up period is still relatively short; therefore, continued monitoring of the patient is planned. It is recommended that contrast-enhanced abdominal CT scans be performed every six months. Although the tumor was completely resected, the possibility of postoperative recurrence cannot be ruled out.

Surgical resection of ganglioneuromas encasing major blood vessels remains technically challenging, with only a few cases reported. Early open surgical approaches often necessitated combined organ resection or vascular reconstruction with artificial grafts, causing substantial surgical trauma[16,17]. Subsequently, Wan et al[18] proposed a “staged resection” technique for tumors encasing major blood vessels. They applied this method to treat a 7.2 cm × 7.5 cm retroperitoneal ganglioneuroma, which, similar to our case, completely encased the celiac axis, splenic artery, common hepatic artery, and superior mesenteric artery. The tumor was dissected into four segments along the vascular courses and resected individually. Due to the close anatomical relationship between the tumor and the pancreas, a pancreatoduodenectomy was performed concurrently. However, all major retroperitoneal vessels were preserved throughout the procedure. The surgery was performed using an open abdominal approach. At one-year postoperative follow-up, no tumor recurrence was observed. These findings suggest that tumor segmentation and resection with vascular preservation in ganglioneuromas do not necessarily lead to residual disease or tumor dissemination. However, this conclusion requires validation through larger case series and longer-term follow-up. An important question for further investigation is whether this surgical strategy can be applied to other benign tumors encasing major blood vessels.

In 2016, Abe et al[19] described 24 cases of laparoscopic resection of paraspinal neurogenic tumors located adjacent to the abdominal aorta or inferior vena cava (IVC), noting that none of the tumors encased these vessels. The relatively large diameter and thick walls of the abdominal aorta and IVC reduced the risk of vascular injury, allowing for safe tumor removal through meticulous dissection along the tumor margins without the need for tumor incision or direct vascular exposure. Similarly, in 2012, Alimoglu et al[20] reported a case of ganglioneuroma located at the hepatic hilum, superior and posterior to the pancreas, measuring approximately 4.4 cm. Although the tumor was adjacent to the celiac trunk and its branches - including the left gastric artery, hepatic artery, and splenic artery - no vascular invasion was observed. In 2023, Felföldi et al[21] reported a ganglioneuroma in the hepatoduodenal ligament, closely abutting the IVC, portal vein, and hepatic artery. The tumor was safely resected along its margins without the need for tumor incision, as the vessels were not encased. In 2021, Nagano et al[22] presented a case of laparoscopic resection of a large (approximately 9 cm) extra-adrenal ganglioneuroma adherent to the abdominal aorta and inferior mesenteric artery. Only fibrous adhesions were observed intraoperatively, which were easily separated using an ultrasonic scalpel. Compared with the present case, the surgical complexity in these previously reported cases was significantly lower due to the absence of vascular encasement or deep anatomical involvement.

Compared with two-dimensional laparoscopy, 3D laparoscopy offers higher magnification and 3D stereoscopic imaging. These features facilitate more precise intraoperative localization and optimal hand-eye coordination, considerably enhancing surgical efficiency and safety. The improved spatial perception provided by 3D laparoscopy is advantageous for delicate procedures such as suturing, particularly in managing vascular bleeding[23,24]. To our knowledge, this report represents the first case of using 3D laparoscopy to resect ganglioneuromas encasing major blood vessels. Notably, no combined organ resection or vascular graft replacement was required. Our surgical team routinely employs 3D laparoscopy for pancreatic, hepatic, and other complex abdominal procedures. We are highly proficient in advanced laparoscopic surgeries, including laparoscopic pancreaticoduodenectomy, radical gastrectomy, and anatomical hepatectomy. Each year, we perform approximately 3000 hepatobiliary and pancreatic surgeries, allowing us to accumulate extensive clinical experience. This depth of surgical expertise provided a solid foundation for the successful execution of the present procedure. Accordingly, we recommend that such complex operations be performed in high-volume tertiary medical centers by experienced surgical teams. Inadequate surgical experience may compromise the ability to effectively manage intraoperative challenges and unforeseen complications.

The laparoscopic suspension technique is analogous to the use of retractors in open abdominal surgeries. It allows the primary surgeon and assistant to keep their hands free from other surgical maneuvers. Suspension does not prolong the overall operative time; adequate suspension provides an excellent field of view and optimal exposure during the procedure[25,26]. Suspension of the liver and stomach is a widely used technique in hepatobiliary and pancreatic surgery. By employing sutures or specialized instruments to retract and stabilize these organs, the technique enables optimal exposure of complex anatomical regions, including the hepatic hilum, retrohepatic IVC, posterior segments of the right hepatic lobe, gastroesophageal junction, lesser curvature of the stomach, and pancreas. In contrast, pancreatic suspension is relatively rare. Adequate exposure of these critical areas facilitates the safe and effective execution of complex surgical procedures, thereby enhancing both surgical safety and oncological radicality.

In the case presented, a multilayer suspension of the stomach, liver, and pancreas was implemented. The gastrocolic and hepatogastric ligaments were first dissected using an ultrasonic scalpel, followed by a laparoscopic gauze strip to encircle the gastric body. The gauze was then sutured and fixed to the falciform ligament of the liver. To elevate the left lateral lobe of the liver, a purse-string suture was placed, with both ends passed through the abdominal wall on either side of the round ligament. A 10-Fr red rubber catheter was passed through the suture, secured at the root of the hepatogastric ligament with a Hem-o-lok clip, and tightened to establish the necessary suspension. A second catheter was introduced through the pancreatic base and suspended from the abdominal wall after the pancreatic base was separated. This comprehensive suspension method provided the necessary space for successful tumor resection. This technique, reported for the first time in retroperitoneal ganglioneuroma resection, was integral to the success of the procedure.

Postoperatively, the patient's transaminase levels rose sharply but improved rapidly thereafter. An early postoperative contrast-enhanced CT scan revealed ischemic changes in the liver's left lateral segment that resolved over time. Upon analysis, two potential causes were identified: (1) During the operation, bleeding from the left gastric artery required resection. However, the accessory left hepatic artery originated from the left gastric artery, impairing the blood supply to the left lateral segment of the liver; and (2) If the intraoperative suspension of the pancreas was too tight, it may have compromised the blood flow to the splenic, superior mesenteric, and portal veins, potentially leading to ischemia-reperfusion injury. Therefore, future surgeries should avoid unnecessary vascular resections and ensure the pancreatic suspension is not overly tight.

The operative time was 458 minutes, primarily due to the complexity of the procedure. Even when performed via an open approach, such surgeries typically require a relatively long duration. We anticipate that, with increased experience and greater proficiency in the surgical workflow, the operative time will gradually decrease. Similarly, after years of refinement, laparoscopic procedures such as pancreaticoduodenectomy and hepatectomy can now be performed within a timeframe comparable to that of open surgery. Moreover, laparoscopic surgery offers several well-established advantages, including reduced invasiveness, less intraoperative blood loss, faster postoperative recovery, and shorter hospital stays[27,28].

CONCLUSION

Ganglioneuroma is a rare, well-differentiated, and slow-growing benign tumor arising from the peripheral nervous system, with surgical resection being the sole curative treatment. However, resecting ganglioneuromas that encase major blood vessels presents considerable technical challenges. These tumors have traditionally often required open abdominal surgery or combined organ resections and, in some cases, are deemed unresectable. This report presents the first case of a retroperitoneal ganglioneuroma encasing major vessels successfully resected using 3D laparoscopic surgery combined with organ suspension. At 11 months of postoperative follow-up, the patient exhibited neither complications nor evidence of tumor recurrence. This case highlights the feasibility of minimally invasive laparoscopic approaches for managing complex retroperitoneal ganglioneuromas encasing major blood vessels. However, further studies with larger cohorts and extended follow-up are needed to confirm these findings.