Clinical Efficacy Analysis of Different Surgical Methods for Giant Adrenal Tumors (≥10 cm): A Single-Center Study of 44 Cases

Abstract

Objective:

The objective of this study was to compare the efficacy and safety of open adrenalectomy (OA) and laparoscopic adrenalectomy (LA) by summarizing the clinical features and treatment experience of giant adrenal tumors.

Methods:

The clinical data of 44 patients with adrenal tumors ≥10 cm admitted to the Second Hospital of Lanzhou University from January 2006 to August 2022 were retrospectively analyzed. The mean tumor diameter was 11.6 ± 1.8 cm. Regular follow-up was performed to observe the outcome of symptoms and the recurrence after operation.

Results:

All the 44 patients successfully completed the operation and were divided into the OA group (21 cases) and the LA group (11 cases of transabdominal laparoscopic adrenalectomy [TLA] and 12 cases of retroperitoneal laparoscopic adrenalectomy [RLA]) according to different operation methods. The analysis results showed that the proportion of estimated blood loss (EBL) >100 mL and the postoperative length of stay (PLOS) in the LA group were superior to those in the OA group, and there were no significant differences in other surgical indicators (P > .05); subgroup analysis was conducted for patients in the LA group according to different surgical pathways, and the results showed that there were no significant differences in each surgical indicator between TLA and RLA (P > .05). Among the 44 patients, 15 (34.1%) had intraoperative complications, 19 (43.2%) had postoperative complications, and 5 (21.7%) were converted from LA to OA. The median follow-up time was 68 (5–162) months.

Conclusions:

For adrenal tumors with diameter ≥10 cm, both LA and OA have relatively large damage to the patients, and the incidence of conversion to open surgery is also high. However, LA is superior to OA in EBL and PLOS. Given the fact that giant adrenal tumors are mainly pheochromocytoma and paraganglioma and have an increased possibility of malignancy, we suggest that the relationship between tumors and peripheral important blood vessels and organs should be carefully evaluated before operation, and the operative methods should be selected according to the experience of the surgeon.

Introduction

With the development of minimally invasive techniques, laparoscopic adrenalectomy (LA) has gradually replaced open adrenalectomy (OA) as the standard operation for adrenal tumors, and transabdominal laparoscopic adrenalectomy (TLA) and retroperitoneal laparoscopic adrenalectomy (RLA) have also been widely used. At present, there is no unified standard for indications and contraindications of LA, and the controversy mainly focus on giant tumors and malignant tumors, with concerns concentrate on perioperative safety and whether the treatment of tumors with metastatic potential is safe and effective. This article retrospectively analyzed the clinical data of patients with adrenal tumors ≥10 cm in diameter who underwent surgery in our hospital, explored the efficacy and safety of different surgical methods in the treatment of giant tumors, and summarized the general characteristics of giant adrenal tumors to provide help for clinical diagnosis and treatment.

Methods

From January 2006 to August 2022, 1327 patients with adrenal tumors were treated by surgery in the Second Hospital of Lanzhou University, 44 of whom had tumors ≥10 cm in diameter, and clinical data were collected retrospectively. All patients completed preoperative examinations and were prepared according to pheochromocytoma and paraganglioma (PPGL). All operations were performed by experienced and senior urologists. The study was approved by the Clinical Research Ethics Committee. Regular follow-up was performed after the operation to observe the outcome of symptoms and recurrence.

The evaluation indicators of surgical effect were recorded including operating time (OT), estimated blood loss (EBL), blood transfusion, intraoperative complications (IC), intraoperative hemodynamic instability (IHD, defined as intraoperative systolic blood pressure >180 mmHg or mean arterial pressure <60 mmHg), postoperative intensive care unit stay (ICU stay), fasting time (FT, defined as from the day of completion of surgery until oral intake is acceptable), drainage time (DT, defined as the drainage tube was removed from the day of completion of surgery until the drainage volume of the drainage tube was <10 mL for two consecutive days), indwelling catheter time (ICT, defined as the catheter was removed from the day of completion of the surgery until the patient was assessed to no longer meet the indications for indwelling catheterization), postoperative complications (PC), and postoperative length of stay (PLOS).

Statistical Methods

Data were processed using SPSS 26.0 statistical software. Enumeration data are expressed as percentages (%) and analyzed using the χ² test or Fisher's exact test; the Kolmogorov–Smirnov test was used to determine whether continuous variables were normally distributed and expressed as mean and standard deviation or median and interquartile range, and Student's t-test or the Mann–Whitney U test was used for analysis. P < .05 was considered statistically significant and two-tailed tests were used in hypothesis testing.

Results

General data

The mean age of the 44 patients was 49.3 ± 14.1 years, including 24 males (54.5%) and 20 females (45.5%). The tumor affected the left gland in 45.5% of cases, the right gland in 52.3%, and bilateral in 2.7%. The mean tumor diameter was 11.6 ± 1.8 cm. There were 11 cases (25.0%) of lumbago and back pain, 8 cases (18.2%) of abdominal pain, 7 cases (15.9%) of dizziness, palpitation, and elevated blood pressure, 1 case (2.3%) of abdominal mass, 1 case (2.3%) of bilateral lower limb edema, and 16 cases (36.4%) was found by physical examination. There were 13 patients (29.5%) with hypertension, 4 patients (9.1%) with diabetes, and 11 patients (25.0%) with previous abdominal surgery.

Comparison of general data of patients with different surgical methods

All 44 patients had no signs of distant metastasis and successfully completed the operation, including 21 patients in the OA group and 23 patients in the LA group (11 TLA and 12 RLA). The results showed that there were significant differences in the proportion of the left tumors (P = .01) and hypertension (P = .008) between the OA group and the LA group (Table 1). Considering the reason, the right central adrenal vein is short and drains horizontally into the inferior vena cava, and the liver may need to be separated during surgery and prone to collateral injury, so as to most surgeons prefer to choose OA for right giant adrenal tumors; hypertensive patients have a relatively high proportion of IHD due to anesthesia or touching the tumor during surgery, while the endoscopic anatomy is clear and the operation is fine, which is conducive to reducing direct extrusion of the tumor and early control of tumor-supplying blood vessels, so surgeons prefer to choose LA for patients with hypertension.

Table 1.

Comparison of General Data of Patients

Variable	OA group (n = 21)	LA group (n = 23)		Comparison between the LA group and the OA group		Comparison between the RLA group and the TLA group
Variable	OA group (n = 21)	RLA group (n = 11)	TLA group (n = 12)	t/χ² value	P	t/χ² value	P
Age, years	46.3 ± 13.0	57.6 ± 10.1	46.8 ± 16.9	1.345	.186	−1.827	.082
Gender				0.777	.545	0.068^a	1.000
Male	10 (41.7%)	7 (29.2%)	7 (29.2%)
Female	11 (55.0%)	4 (20.0%)	5 (25.0)
BMI	22.7 (3.9)	25.1 (5.8)	22.6 (3.9)	−0.600^b	.556	−0.770^b	.458
Combined with hypertension				7.736	.008	0.048	1.000
Yes	2 (15.4%)	5 (38.5%)	6 (46.2%)
No	19 (61.3%)	6 (19.4%)	6 (19.4%)
Combined with diabetes				0.009^a	1.000	0.004^a	1.000
Yes	2 (50.0%)	1 (25.5%)	1 (25.5%)
No	19 (47.5%)	10 (25.0%)	11 (27.5%)
Previous abdominal surgery				0.273	.732	0.158^a	1.000
Yes	6 (54.5%)	2 (18.2%)	3 (27.3%)
No	15 (45.5%)	9 (27.3%)	9 (27.3%)
Serum potassium	4.02 (0.70)	4.14 (0.55)	3.90 (1.00)	−0.506^b	.626	−0.719^b	.493
Tumor size, cm	12.0 ± 1.8	10.7 ± 1.3	11.7 ± 2.0	−1.357	.182	1.403	.175
Tumor side				11.624^a	.001	0.100^a	1.000
Left	4 (20.0%)	8 (40.0%)	8 (40.0%)
Right	16 (69.6%)	3 (13.0%)	4 (17.4%)
Bilateral	1 (100.0%)	0 (0.0%)	0 (0.0%)
Histological type				1.101^a	.837	1.550^a	.782
PPGL	9 (47.4%)	6 (31.6%)	4 (21.1%)
Malignancy	4 (40.0%)	2 (20.0%)	4 (40.0%)
AML	5 (62.5%)	1 (12.5%)	2 (25.0%)
Others	3 (42.9%)	2 (28.6%)	2 (28.6%)

The significance of bold values represents P < .05.

Fisher's exact test.

The Mann–Whitney U test.

AML, adrenal myelolipoma; BMI, body mass index; LA, laparoscopic adrenalectomy; OA, open adrenalectomy; PPGL, pheochromocytoma and paraganglioma; RLA, retroperitoneal laparoscopic adrenalectomy; TLA, transabdominal laparoscopic adrenalectomy.

Comparison of intraoperative and postoperative outcomes of different surgical methods

Forty-four patients had a median OT of 180 (120) minutes and a median EBL of 250 (775) mL, of which 28 cases (63.6%) had EBL >100 mL. Thirteen patients (29.5%) had IHD. Twenty patients (45.5%) had more intraoperative bleeding and were given concentrated red blood cell or plasma infusion. Five patients (11.4%) were transferred to ICU after the operation. The median FT of 44 patients was 3 (2) days, median DT 5.5 (4) days, median ICT 4 (2) days, and median PLOS 9.5 (5) days.

The analysis results showed that the proportion of EBL >100 mL (47.8% versus 81.0%, P = .025) and the PLOS (8 days versus 11 days, P = .038) in the LA group were superior to those in the OA group; there were no significant differences in OT, EBL, blood transfusion rate, IC, IHD, ICU stay, FT, DT, ICT, and PC between the two groups (P > .05); subgroup analysis of TLA and RLA in the LA group showed that there was no significant difference in the above evaluation indicators for all (P > .05) (Table 2).

Table 2.

Comparison of Surgical Effects of Different Surgical Methods

Variable	OA group (n = 21)	LA group (n = 23)		Comparison between the LA group and the OA group		Comparison between the RLA group and the TLA group
Variable	OA group (n = 21)	RLA group (n = 11)	TLA group (n = 12)	t/χ² value	P	t/χ² value	P
OT (minutes)	180 (150)	180 (120)	180 (128)	−0.261	.800	−0.063	.968
EBL (mL)	300 (765)	300 (800)	100 (828)	−1.100	.277	−0.906	.381
EBL >100 mL	17 (60.7%)	7 (25.0%)	4 (14.3%)	5.391	.031	2.112	.220
Transfusion	9 (45.0%)	5 (25.0%)	6 (30.0%)	0.109	.771	0.048	1.000
IC	9 (60.0%)	3 (20.0%)	3 (20.0%)	1.374	.342	0.015^a	1.000
IHD	7 (53.8%)	3 (23.1%)	3 (23.1%)	0.277	.744	0.015^a	1.000
FT (days)	3 (2)	3 (2)	3 (2)	−0.409	.689	−0.195	.902
DT (days)	6 (5)	5 (4)	6.5 (4)	−0.119	.911	−0.407	.699
ICT (days)	4 (2)	4 (3)	5 (4)	−1.531	.129	−0.568	.587
PC	11 (57.9%)	5 (26.3%)	3 (15.8%)	1.386	.361	1.066^a	.400
ICU stay	3 (60.0%)	0 (0.0%)	2 (40.0%)	0.341^a	.658	2.777^a	.478
PLOS (days)	11 (7)	8 (4)	8 (8)	−2.073	.038	−0.562	.593

The significance of bold values represents P < .05.

Fisher's exact test.

DT, drainage time; EBL, estimated blood loss; FT, fasting time; IC, intraoperative complications; ICT, indwelling catheter time; ICU, intensive care unit; IHD, intraoperative hemodynamic instability; LA, laparoscopic adrenalectomy; OA, open adrenalectomy; OT, operating time; PC, postoperative complications; PLOS, postoperative length of stay; RLA, retroperitoneal laparoscopic adrenalectomy; TLA, transabdominal laparoscopic adrenalectomy.

There were 15 cases (34.1%) of IC: 10 cases of vascular injury, including 5 cases of OA, 3 cases of TLA, and 2 cases of RLA, all of which occurred in the tumor surrounding blood vessels or close adhesions; 1 case of spleen injury and 1 case of kidney injury, all of which occurred in OA; 3 cases of IHD, including 2 cases of OA and 1 case of RLA, all of which occurred when touching tumor and after resection of the tumor; and all 3 cases of postoperative pathological examination were PPGL.

Five cases (21.7%) were converted from LA to open surgery, including 3 cases of TLA and 2 cases of RLA, which were conversion due to severe intraoperative adhesion and a large amount of blood loss. Postoperative pathological examination results showed PPGL and adrenal cortical carcinoma (ACC) in 2 cases each, and adrenal myelolipoma (AML) in 1 case.

There were 19 cases (43.2%) of PC: OA in 11 patients, including incision infection in 3 patients, postoperative hypokalemia and hypotension in 2 patients each, adrenal crisis, ventricular premature beats, anemia, and lower limb thrombosis in 1 patient each; LA in 8 patients, including anemia and hypoxemia in 2 patients each, pleural effusion, fever, postoperative infection, and atrial fibrillation with incision infection in 1 patient each. The patients were treated with anti-infection, fluid and blood transfusion, correction of electrolyte imbalance, lower limb thrombi prevention filter, ventricular fibrillation correction, strengthening wound dressing change, or transfer to ICU after the operation. All patients were improved and discharged.

Postoperative pathological results showed that there were 34 cases of benign and 10 cases of malignant tumors: OA included PPGL in 9 cases, AML in 5 cases, liposarcoma in 2 cases, leiomyosarcoma, malignant schwannoma, ganglioneuroma, cortical adenoma (tumor giant cell atypia), and cyst in 1 case each; TLA included PPGL in 6 cases, metastatic malignant melanoma, ACC, AML, ganglioneuroma, and cyst in 1 case each; RLA included PPGL and ACC in 4 cases, AML in 2 cases, cyst and mature teratoma in 1 case each.

Of the 44 cases, 4 patients (9.1%) were lost to follow-up, and the remaining 40 cases were followed up until September 2022, with a median follow-up of 68 (5–162) months. Twelve patients were recurrent, progression, and/or death (Table 3). One case of liposarcoma received chemotherapy and 1 case of ACC recurrence received radiofrequency ablation. Patients with dizziness, hypertension, or lumbago and back pain before the operation were improved to varying degrees after the operation.

Table 3.

Status of 12 Patients with Recurrent, Progression, or Death

Number	Gender	Age (years)	Surgical methods	Pathological type	TR	Death (reason)	Follow-up time
A	M	74	RLA	ACC	Yes	Yes (TR)	33
B	F	45	OA	Leiomyosarcoma	Yes	Yes (TR)	57
C	M	61	RLA	ACC	No	Yes (MI)	12
D	F	66	COA	ACC	No	Yes (MI)	54
E	F	31	COA	ACC	Yes	No	47
F	M	55	COA	ACC	Yes	Yes (TR)	21
G	F	48	OA	Liposarcoma	Yes	No	33
H	M	63	OA	Liposarcoma	Yes	No	42
I	F	25	OA	Malignant schwannoma	Yes	Yes (TR)	37
G	M	56	TLA	PPGL	No	Yes (ACI)	69
K	M	41	OA	Cortical adenoma	No	Yes (LC)	156
L	M	45	OA	PPGL	No	Yes (MI)	82

ACC, adrenal cortical carcinoma; ACI, acute cerebral infarction; COA, conversion to open adrenalectomy; F, female; LC, lung cancer; M, male; MI, myocardial infarction; PPGL, pheochromocytoma and paraganglioma; RLA, retroperitoneal laparoscopic adrenalectomy; TLA, transabdominal laparoscopic adrenalectomy; TR, tumor recurrence.

Discussion

In recent years, with the development of surgical methods and the maturity of endoscopic technology, “safe, effective and minimally invasive” has gradually become the surgical concept pursued by urologists, which has also brought a revolution to adrenal surgery. Since Gagner et al.¹ first reported LA in 1992, LA has become the “gold standard” for adrenal surgery, which has the advantages of less tissue structure destruction, fewer surgical complications, and rapid postoperative recovery. The upper limit of the diameter of resectable tumors of LA is still not unified, and the surgeons often select the operation carefully based on their proficiency and screening cases. Because tumor growth can lead to changes in the normal anatomical relationship of adjacent tissues, rich collateral circulation of tumors and abnormal vascularization of surrounding tissues, increased difficulty of central vein ligation, and insufficient surgical space, it may be increased the incidence of IC and the conversion rate of LA.

To ensure that the surgical risk of large adrenal tumors is relatively controllable, domestic and foreign scholars have conducted corresponding studies. However, due to the development of imaging technology and people's attention to the health examination, the detection rate of nonfunctional adenoma or incidentaloma has increased, and the tumor has been treated before it increased to a certain extent. At present, it has not been found that large adrenal tumors have regional clustering, and it is not easy to collect and summarize the general characteristics of scattered cases, so it is difficult to evaluate the surgery safety of large adrenal tumors. As reported in the literature, the maximum diameter of the adrenal tumor removed by LA was 22.5 cm.²

The definition of a giant adrenal tumor is still inconclusive, and it is generally considered to be >6 cm. Prakobpon et al.³ analyzed 456 patients who underwent LA, and the results showed that OT, EBL, conversion rate, transfusion rate, and the incidence of IC and PC in patients with tumors <6 cm were significantly better than those in tumors >6 cm (P < .001 for all). Wang et al.⁴ performed propensity matching in patients with tumors >6 cm, and the results showed that the LA group was significantly better than the OA group in EBL, blood transfusion rate, and PLOS (P < .05 for all). Bozkurt et al.⁵ analyzed patients who underwent LA with 8 cm as the cutoff value, and the results showed that there were no statistical significances in OT, EBL, IC, and PC. Other studies also obtained similar results.^6,7 In this study, the tumor diameter was ≥10 cm, and the results showed that the LA group was superior to the OA group in the proportion of EBL >100 mL (P = .025) and PLOS (P = .038); TLA and RLA subgroup analysis showed no significant differences in each indicator.

Therefore, we believe that the clinical results of the three different surgical approaches were similar and all safe and effective with the tumor diameter increasing. We should not regard tumor size as the only factor to determine the surgical method but should determine it based on a combination of preoperative imaging data to assess the degree of adhesion between the tumor and the surrounding tissue and the surgeon's proficiency in the surgical procedure. In addition, we suggest that TLA is the best choice for large tumor or tumor closely related to abdominal tissue such as the inferior vena cava, pancreas, and gastrointestinal tract, which can not only provide a large surgical space and facilitate exposure of the relationship between the tumor and the surrounding organ, to perform subtle separation, but also be easily changed to open surgery when necessary.

Most adrenal tumors are benign. Nine hundred eleven cases of adrenal tumors with mean diameter of 3.3 cm in our hospital were studied in the early stage, and the overall benign and malignant rates were 98.1% and 1.9%, respectively.⁸ At present, it is generally accepted that as the diameter of adrenal tumors increases, their pathological distribution and malignant rate also change, and studies have proposed that the diagnostic specificity of malignant tumors with a diameter over 4 cm is 31%–61%.⁹ Minguez et al.¹⁰ showed that PPGL and ACC, respectively, accounted for 38.3% and 14.9% when the tumor diameter was ≥5 cm; PPGL and ACC, respectively, accounted for 42.9% and 17.9% when the tumor diameter was ≥6 cm. In this series of tumors ≥10 cm, PPGL and malignant tumors, respectively, accounted for 43.2% (19/44) and 22.7% (10/44), which supported the statement that PPGL and malignant tumors accounted for an increasing proportion with tumor diameter.

PPGL is rich in blood supply, tumor rupture or feeding vessel injury often causes massive hemorrhage, and intraoperative stimulation of the tumor can induce catecholamine secretion leading to IHD. Zhang et al.¹¹ performed a propensity-matched study of PPGL >6 cm and showed that the incidence of IHD in the LA group was lower than that in the OA group (P = .020). In this study, PPGL accounted for 23.1% (3/13) of IHD and occurred before and after anesthesia, tumor isolation, and tumor resection. Our experience is that preoperative preparation of large adrenal tumors is uniformly treated as PPGL; intraoperative extrusion and traction of the tumor should be avoided as far as possible to prevent catecholamines from entering the blood, thereby reducing the occurrence of IHD.

Like traditional OA, minimally invasive adrenalectomy (MIA) should also follow the “tumor-free principle”, including intact tumor capsule, adequate resection margin, and no risk of tumor metastasis and luminal metastasis. Calcatera et al.¹² analyzed 588 ACC patients and showed no significant difference in overall survival (OS) between the LA group and the OA group (4.4 versus 4.6 years, P = .85). The results of Zhang et al.¹¹ showed no significant difference in metastasis rate between the LA group and the OA group for PPGL >6 cm (4.0% versus 3.3%, P = 1.000).

Ginsburg et al.¹³ studied the positive rate of surgical margins and OS in 698 non-metastatic ACC patients with different tumor size and surgical methods by the propensity score matching and stratified analysis, and the results showed that: for adrenal tumors of different sizes, MIA (≤6 cm: 21%; 6.1–10 cm: 17%; 10.1–20 cm: 27%) and OA (≤6 cm: 16%; 6.1–10 cm: 19%; 10.1–20 cm: 18%) were similar in positive rate of surgical margins (P < .05); when controlling for one factor, tumor size or surgical method, the other factor had no significant correlation with positive surgical margin (P < .05); regardless of tumor size or surgical margin, there was no correlation between the surgical method and OS (P < .05). The results of these several studies to a certain extent indicated that LA is not an absolute contraindication for malignant tumors. Because malignant adrenal tumors are rare in clinical practice, this study cannot provide strong evidence for their clinical effect analysis in different surgical procedures.

For the surgical skills of large adrenal tumors, we have the following experiences: giant tumors often overlap or adhere to renal veins and inferior vena cava, and the use of ultrasonic knife can minimize the wound bleeding, so as to maintain the operative field clear and prevent surrounding organ injury; there are many nourishing vessels on the tumor surface, and the central vein is pulled and displaced, so it is difficult to control them directly. Therefore, anatomical separation should be performed from outside the tumor capsule first, and finally, the vascular anatomical plane is established, so as to avoid blind separation causing peripheral tissue injury and nourishing vessel bleeding; if the lesion is on the left, damage to the pancreas and spleen should be avoided, if the lesion is on the right, the protection of inferior vena cava and liver should be strengthened.

Therefore, clear identification of the anatomical structure around the tumor is helpful to safely and completely remove the large tumor; abdominal implantation should be prevented during tumor removal, mainly to avoid capsular tear; due to the compression of the large tumor, after removing the tumor or will be bleeding with the release of intra-abdominal pressure, pneumoperitoneum pressure should be reduced before closing the abdomen, and a careful examination should be performed to ensure no missed bleeding; finally, if the poor vision of the operative field or anatomical difficulties, to avoid vessel injury caused by the blind operation, conversion from LA to open surgery should be performed in time when necessary.

There were some limitations: this study was a retrospective analysis, with potential inherent selection and bias due to failure to better minimize the interaction between variables in the design that could affect the results; in addition, the small and uneven number of cases in each group is an important limitation of this article, which leads to the limitation of patient survival outcome research.

In conclusion, both OA and LA have relatively large damage and high incidence of conversion to open surgery, but LA is superior to OA in EBL and PLOS. In view of the fact that giant adrenal tumors are mainly PPGL and the possibility of malignancy increases, it has a certain difficulty in different surgical methods, and which surgical method should be selected according to the patient's personal conditions such as the nature of the lesion, tumor size, location, and the surgeon's own experience. Surgical skill is to early expose the tumor and control the major blood vessels, thereby reducing dissection and stimulating the tumor. In addition, the incidence of conversion from LA to OA in the giant adrenal tumor is high. Controllable factors should be evaluated and treated before surgery and accurately grasp the timing of conversion. Early and active conversion can reduce the adverse effects on patients and improve the postoperative situation.

Footnotes

Authors' Contributions

Conceptualization and design: P.S. and Q.H. Data curation: Q.H., J.L., and Y.L. Formal analysis and methodology: Q.H. Writing—original draft: Q.H. Writing, review and editing: P.S., Q.H., and B.Z. Funding acquisition: P.S.

Disclosure Statement

No competing financial interests exist.

Funding Information

No funding was received for this article.

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