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Original Article
Thoracoabdominal approach to large adrenal tumors – when laparoscopic adrenalectomy is not enough: a retrospective four-year study
expand article infoKonstantinos Tsalis, Orestis Ioannidis, Natalia Antigoni Savvala, Grigorios Gkasdaris, Panagiotis Christidis, Elissavet Anestiadou, Ioannis Mantzoros, Manousos Pramateftakis, Efstathios Kotidis, Nikolaos Ouzounidis, Vasilis Foutsitzis, Savvas Symeonidis, Stefanos Bitsianis, Angeliki Cheva, Stamatios Angelopoulos
‡ Aristotle University of Thessaloniki, Thessaloniki, Greece
Open Access

Abstract

Introduction: Laparoscopic adrenalectomy is considered to be the gold standard approach in the field of adrenal surgery. This technique offers advantages of great importance compared to variant laparotomy techniques. Notwithstanding, a technique that needs to be mentioned is the thoracoabdominal approach which facilitates the anatomic exposure of the retroperitoneum, adrenal gland, and great vessels and is strongly recommended for the surgery of large, malignant adrenal tumors.

Aim: The objective of this study is to evaluate the effectiveness and outcomes of the thoracoabdominal approach in adrenal surgery for large adrenal tumors. By presenting our results and experiences, we aim to highlight the advantages of this technique in providing optimal anatomic exposure of the retroperitoneum, adrenal gland, and great vessels, and to establish its role as a viable alternative to laparoscopic adrenalectomy in complex cases.

Materials and methods: We reviewed retrospectively the data of our patients admitted to our Surgical Department and treated surgically with the thoracoabdominal incision, performed by a single surgeon at our tertiary care center, over the period 01/01/20-31/12/23.

Results: All patients had large retroperitoneal masses of varying complexity, requiring maximal surgical exposure. Seventeen patients in total underwent operation with the indication of unilateral adrenal tumor. Five of those patients underwent a laparoscopic tumor resection, while 12 patients were treated by thoracoabdominal approach. Our study group included 7 women (58%) and 5 men (42%), with average age 57 years. The mean maximum tumor diameter was 10.8 cm.

Conclusion: The advantages of the thoracoabdominal approach regarding the exposure of the operative field in challenging cases, together with the low incidence of complications noted in our experience, render this technique an excellent alternative if indicated.

Keywords

adrenal gland, adrenalectomy, large, laparoscopic approach, tumor, thoracoabdominal

Introduction

The first open adrenalectomy was performed in 1914 by Sargent and the first laparoscopic adrenalectomy was described by Gagner in 1992.[1, 2] Over the last decades, various posterior and anterior approaches have been developed including anterior, posterior, and thoracoabdominal approaches. More specifically, adrenal surgery by open technique includes transperitoneal (anterior or thoracoabdominal), retroperitoneal or lateral posterior approach, while laparoscopic adrenalectomy may be performed via the transperitoneal, lateral anterior, retroperitoneal or lateral posterior approach. In addition, single-port laparoscopic adrenalectomy can be performed via the lateral transperitoneal or the posterior transperitoneal approach.[3]

In the era of minimally invasive surgery, laparoscopic adrenalectomy is considered to be the gold standard in the field of adrenal surgery. This technique offers advantages of great importance compared to variant laparotomy techniques such as reduced levels of postoperative pain, decreased morbidity, lower or equivalent operative blood loss, shorter hospital stay and quicker return of bowel function and recovery.[4, 5] Nevertheless, this approach has specific limits that have to be underlined to guarantee its safety. Laparotomy techniques are recommended for the spectrum of cases that laparoscopic approach is not safe, such as large and invasive adrenal tumors.[6–8] Additionally, open adrenalectomy is the treatment of choice for patients in whom laparoscopic surgery is contraindicated such as patient’s inability to undergo pneumoperitoneum and multiple previous abdominal operations. Amongst open techniques, a technique that needs to be mentioned is the thoracoabdominal approach. This uncommon technique is unique because it facilitates the anatomic exposure of the retroperitoneum, adrenal gland, and great vessels and is strongly recommended for the surgery of large, malignant adrenal tumors, usually with diaphragmatic involvement or tumor extension into the chest.[9]

Aim

This study presents the outcomes, the postoperative course and our experience with the thoracoabdominal approach. A step-by-step analysis of the approach is also described. In addition, we provide a comprehensive literature review and outline the indications, advantages, and disadvantages of this approach.

Materials and methods

Case series

Methods

The files of the patients admitted to our surgical department over the period 01/01/20-31/12/23 were retrospectively reviewed. Seventeen patients were operated with the indication of a unilateral adrenal tumor and twelve of them underwent an operation according to the thoracoabdominal approach. The large size of the tumor and the suspicion of malignancy were strong criteria for the use of the thoracoabdominal technique. All tumors were estimated to be over 5 cm in the preoperative imaging evaluation. Below we present the thoracoabdominal approach performed by a single surgeon at our tertiary surgical center (Fig. 1). Written informed consent was obtained from all patients for publication of this case series and accompanying images. Copies of the written consent are available for review by the editor-in-chief of this journal on request.

Figure 1.

Right adrenal tumor as depicted in a CT scan.

Surgical technique

After induction of general anesthesia, the patient is placed in the lateral decubitus position. A pillow is placed longitudinally along the hemithorax and flank to support the body position. The ipsilateral arm is placed across the chest on a padded arm rest and the other arm is secured to an armboard. The patient’s legs are bent at the knee and the top leg straightened with a pillow between the legs. The table is flexed at the patient’s waist. An incision is made across the eighth intercostal space from a point 2 cm below the tip of the scapula to a point in the midline of the abdomen equidistant from the xiphoid process and the umbilicus (Fig. 2). The incision is deepened, preserving the latissimus dorsi and incising the serratus anterior muscle and then deviated towards the costal margin, dividing the rectus muscle along with the anterior and posterior laminae of the rectus sheath and the peritoneum (Fig. 3). The superior epigastric artery is encountered and ligated. The intercostal space is entered along the superior margin of the rib to avoid injury of the neurovascular bundle. The pulmonary ligament is divided and the lung is mobilized and retracted cephalad and medially out of the field, allowing for exposure of the intrathoracic aorta. The abdominal cavity is entered by dividing the diaphragm with electrocautery, 1 to 2 cm from its lateral and anterior attachments to the ribs, circumferentially, so as to avoid injury of the phrenic nerve. Stitches of silk 2.0 are attached on the diaphragm in order to facilitate reconstruction. Once the diaphragm is divided, a self-retaining retractor is placed. Subsequently, the approach to the adrenal gland is developed as usual. Specifically, in the case of left adrenocortical carcinomas, the line of Toldt is incised and the descending colon is mobilized medially. Three laparotomy packs are placed above the spleen in order to downward mobilize and protect the organ. The splenic flexure is taken down by dividing the splenocolic ligament, and the tail of the pancreas is mobilized exposing the splenic vein, the inferior mesenteric vein and furthermore the base of the superior mesenteric vessels (Fig. 4). The lienorenal ligament is divided, the spleen and pancreas are retracted superiorly and dissection is continued along the inferior border of the tumor and the superior pole of the kidney with exposure of the left renal vein. The adrenal vein is identified at its confluence with the renal vein, ligated and divided. The medial attachments to the aorta are taken down with harmonic scalpel while applying gentle lateral traction on the gland. The lateral and inferior attachments to the kidney are taken down by blunt and sharp dissection. Alternatively, in the case of right adrenocortical carcinomas, the hepatic flexure, duodenum and head of the pancreas are taken down. The right triangular ligament is divided and the right lobe of the liver is mobilized exposing the inferior vena cava (Fig. 5). Dissection around the vena cava exposed the right adrenal vein. Consequently, dissection posteriorly and laterally, assisted in the medial rotation of the tumor. Then, the adrenal vein is double ligated and incised. Finally, the dissection is continued inferiorly along the superior pole of the right kidney.

Figure 2.

Patient in the lateral decubitus position.

Figure 3.

Incision of the rectus sheath and peritoneum.

Figure 4.

Left adrenal tumor exposed by left thoracoabdominal incision.

Figure 5.

Right adrenal tumor exposed by right thoracoabdominal incision. The IVC is depicted.

Closure starts with reconstruction of the diaphragm with interrupted non-absorbable sutures. Pericostal figure of eight sutures of Vicryl No 1 are placed around the ribs but are left untied until a chest tube is inserted (Fig. 6). The abdomen is closed using a running No 1 PDS loop. The serratus anterior is also approximated with running Prolene.

Figure 6.

Closure of the diaphragm and the peritoneum.

Fig. 7 shows the adrenocortical tumors after resection.

Figure 7.

Cases of adrenocortical tumors after resection.

Results

Over 30 years, more than 70 cases of adrenal tumors have been treated surgically in our Surgical Department. During the last 4 years, 17 patients of them underwent operation. Five of those patients underwent a laparoscopic resection of the tumor. The rest 12 were treated with the thoracoabdominal approach. The study group consisted of 7 women (58%) and 5 men (42%). The average age was 57 years old. Average maximum tumor diameter was 10.8 cm. The average length of hospitalization was estimated to be approximately 8 days in the department and one day in the ICU. Almost, one out of five patients of the group presented at least one complication including postoperative bleeding and pneumonia. The majority of tumors (70%) were malignant. No difference between left and right position of the tumor was observed.

Discussion

It is true that the increasing use of computed tomography (CT) and magnetic resonance imaging (MRI) for diagnosis of other conditions has led to increased diagnosis of adrenal masses. The incidence of these incidental adrenal masses has been estimated to be around 5%.[10–12]

Regarding the indications for surgery, masses larger than 6 cm present a rate of adrenocortical carcinoma of 25% and should be managed surgically.[13, 14] Furthermore, surgical resection is also indicated for hormonally active lesions such as cases of Conn syndrome, Cushing syndrome or pheochromocytoma, despite the higher perioperative risk due to hormone-related comorbidities and intraoperative hemodynamic effects of hormone excess.[15]

Nowadays, despite the fact that laparoscopic surgery has become the treatment of choice for the majority of adrenal masses, open adrenalectomy still has a crucial role in the treatment of specific cases.[16, 17]

The choice of approach depends on the size and location of the mass, the possibility of malignancy, and the surgeon’s experience with the different techniques. The open approach to adrenalectomy is considered the gold standard for masses suspected of being adrenal carcinoma.[18] Size of tumor over 5 cm is considered the only significant predictor of conversion from laparoscopic to open.[11] Additionally, Broome et Gauger state that except in the case of pheochromocytoma, large adrenal tumors >6 cm should not be removed laparoscopically due to the risk of adrenocortical carcinoma.[19]

Regarding the open techniques, we should keep in mind that posterior approaches, also known as lumbodorsal approaches, offer the least efficient access to great abdominal vessels, while anterior approaches present the greatest morbidity.[20] Thoracoabdominal approach offers excellent exposure to the retroperitoneum and the great vessels. However, it carries the risks of prolonged ileus, pulmonary complications, and the need for chest tube placement.[21]

Over the last decades a great evolution has been achieved in the surgery of adrenal glands, favoring the minimally invasive techniques of laparoscopy.[22] The scientific society frantically accepted these techniques and surgeons with cumulative experience tried to expand its indications to the most challenging cases.[4,7,8] Nevertheless, ethics and respect to the patient each time dictate the selection of the most appropriate technique balancing the advantages and the disadvantages. Trials performed during the past years shed light on many debates, particularly those concerning the limits of laparoscopy and the extension of the resection needed when confronting an adrenocortical carcinoma. Herein, most of them are retrospective studies with significant heterogeneity among them and increased risk of bias limiting the value of their conclusions.[4, 7]

Appropriate planning of the surgical approach of adrenals implies an excellent preoperative visualization (CT, MRI angiography) and staging of the tumor by means of TNM or European Network for Study of Adrenal Tumors (ENSAT) classification.[23] More specifically, four parameters have to be considered, in order to accurately organize the surgical approach: the size of the adrenal and possible invasion of adjacent tissues, adjacent veins, and invasion of lymph nodes. In addition, metastasis in distant organs is indicative of tumor aggressiveness that needs aggressive resection.[24]

Large adrenal tumors have a high possibility of being malignant. Specifically, 2% of lesions less than 4 cm and 6% of adrenal lesions between 4 and 6 cm are malignant while adrenocortical carcinoma accounts for 25% of adrenal lesions larger than 6 cm.[7] In addition, one should always bear in mind that a CT scan may underestimate the actual size of adrenal tumors larger than 3 cm by 18%.[25] The distinction between a metastatic lesion and a primary adrenocortical carcinoma can be challenging, although radiographic features and medical history can be helpful.‌[26] According to literature, an upper cutoff size of 12 cm is considered to be the limit of laparoscopic approach while invasive adrenal carcinoma and adrenal vein or vena cava involvement is an absolute contra-indication.[27] In addition, conversion from a laparoscopic to an open approach is recommended in cases with intraoperative signs of carcinoma such as tumor adhesions or local invasion, enlarged lymph nodes, or a difficult dissection. In addition, patients suffering from cardiac or pulmonary insufficiency are not candidates for laparoscopy.[28]

During adrenalectomy, iatrogenic injuries of the great vessels or the adjacent viscera can be jeopardous. Safety measures dictate that when such an event is expected, the surgeon must have the most adequate field to confront with the possible complications. There is a plethora of incision techniques in the armamentarium of a surgeon when approaching the adrenal glands with laparotomy.[28, 29] Transperitoneally, a midline, subcostal or thoracoabdominal incision can be performed offering the advantages of excellent surgical exposure and better access to the hilum and great vessels.[30] Higher risk of intra-abdominal organ injury and ileus are the disadvantages; thus, anterior transabdominal approach is indicated in cases of large or potentially malignant tumors for which adequate exposure for extensive dissection is needed. It is also mandatory in cases of vena cava or extensive nodal involvement.[31, 32] Thoracoabdominal approach is generally preferred for selected cases with large and invasive tumors with extensive involvement of surrounding structures or vena cava that require maximal surgical exposure and they cannot be safely removed via the anterior trans-abdominal approach.[29, 33] This approach is also particularly useful in right-sided tumors since the liver and inferior vena cava can limit the exposure.[34] Retroperitoneally, a flank or a posterior lumbodorsal approach is an alternative which overcomes the disadvantages of the previous approach as they are associated with less ileus and shorter hospitalization at the expense of a smaller operative field. Thus, retroperitoneal approaches should not be used for large tumors or adrenal cortical carcinomas. On the contrary, these approaches are ideal for the obese patient.[35]

Adrenocortical carcinoma has a poor prognosis when a locally advanced or a metastatic disease is present. Extirpation of the tumor along with the involved adjacent tissues so as to achieve negative margins and complete lymph node resection is considered the cornerstone of treatment with curative intent.[36] It is of paramount importance not to fragmentize the tumor and prevent spillage. Even though these patients have a high recurrence rate, complete resection of all gross disease is sine qua non. In addition, tumor thrombectomy (infrarenal VC or adrenal vein), or even vascular resection may be needed in order to achieve a R0 resection.[37] Thoracoabdominal incision provides an optimal vascular control as it allows the surgeon to have a frontal view of the paracaval portion which becomes crucial when the dissection is deeper and closer to the major vascular structures or when a thrombectomy is intended.[34]

There is a debate concerning the extent of the lymphadenectomy that has to be performed, given the lack of knowledge of the exact lymphatic drainage pathway of the adrenal glands, the lack of guidelines and the relative morbidity of the technique. Taking into consideration that insufficient lymphadenectomy may be a cause of recurrence, an extended resection of the locoregional and involved lymph nodes should be preferred. Lymph nodes that have to be harvested include celiac, renal hilum and lateroaortic lymph nodes of the suprarenal aorta ipsilateral to the tumor.[38, 39] Thoracoabdominal approach facilitates lymph node dissection, not only of the interaortocaval region but especially the retrocaval and retroaortic regions on the right and left, respectively.[29, 34]

The idea of a thoracoabdominal incision was described by Carter, while Mikulicz was the first to perform such an incision on a human. Other surgeons, including Henle, Wendel, Kirschner, and Janeway, performed variations of the technique (a two-stage procedure).[32] The left thoracoabdominal approach provides the best visualization of the lower esophagus, the gastroesophageal junction, the gastric cardia and stomach, the left hemidiaphragm, the distal pancreas and spleen the left kidney and adrenal gland and aorta.[34] The right thoracoabdominal approach provides the best exposure of the upper esophagus, the liver, the hepatic triad and inferior cava, the proximal pancreas, the right hemidiaphragm, the right kidney and the adrenal gland. Thus, retroperitoneum, adrenal gland and great vessels, the necessary elements to be recognized for the performance of a safe adrenalectomy, are maximally exposed.[32, 34]

What is the cost of this approach and does it fairly balance its disadvantages? The thoracoabdominal approach is an arduous technique that has almost been abandoned due to the implying complications: postoperative pain, pulmonary morbidities, chylous fistula, splenic injury, phrenic nerve injury and ureteric injury.[32, 34] A meticulous and experienced surgeon can avoid most of these complications. Insertion of a thoracic drain before closing the thoracic cavity, individual ligation of dilated lymphatic connections when the dissection arrives at the left crus near the thoracic duct and its branches and lastly division of the diaphragm peripherally away from the phrenic nerve are simple ways to avoid complications.[40] As it is presented in our case series, the percentage of complications was low, no irreversible complications occurred and the stay in hospital was relatively short with satisfying recovery to the normal activities.

Conclusion

According to our experience, the thoracoabdominal approach offers maximal surgical exposure and it is a great alternative in the hands of an experienced surgeon when facing a large, malignant adrenal gland tumor.

Acknowledgments

The authors have no one to acknowledge.

Declaration of interests

The authors declare no competing financial interests or conflicts of interest.

Funding

No funding was received for the present study.

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