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Japanese Journal of Clinical Oncology 30:68-74 (2000)
© 2000 Foundation for Promotion of Cancer Research

The Surgical Approach to the Adrenal Gland: a Comparison of the Retroperitoneal and the Transabdominal Routes in 326 Operations on 284 Patients

Suresh K. Nagesser1, Job Kievit1, Jo Hermans2, H. Michiel J. Krans3 and Cornelis J.H. van de Velde1,+

Departments of 1Surgery, 2Medical Statistics and 3Endocrinology and Metabolism, Leiden University Medical Center, Leiden, The Netherlands


    ABSTRACT
 TOP
 ABSTRACT
 INTRODUCTION
 PATIENTS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
Background: To compare the results of adrenalectomy using a retroperitoneal and a transabdominal approach, especially for adrenal carcinoma and pheochromocytoma.

Methods: A retrospective study was carried out at the Leiden University Medical Center. Charts of 284 patients who had undergone 326 adrenal operations between 1947 and 1995, including 44 patients with adrenal cancer and 60 patients with pheochromocytoma, were reviewed. The main outcome measures were operation time, blood loss, hospital stay and intra- and post-operative complications.

Results: In patients who underwent adrenalectomy (ADX) using a retroperitoneal (RP) approach, duration of operation, intra-operative blood loss, hospital stay and post-operative morbidity compared favourably with those undergoing a transabdominal approach (TA-ADX). However, most of these differences could be explained by the more frequently benign nature and smaller size of the lesions in patients undergoing RP-ADX. However, blood loss remained lower after correction for confounding in all patients undergoing RP-ADX. In patients with larger adrenal lesions, adrenal cancer and pheochromocytoma, that would nowadays be held unsuitable for laparoscopic adrenalectomy, RP-ADX was associated with shorter operation time, less blood loss and less intra-operative complications.

Conclusion: Although laparoscopic adrenalectomy is the treatment of choice for small and benign adrenal lesions, larger lesions and/or adrenal malignancy require open adrenalectomy. In these cases the retroperitoneal approach is the preferred route.


    INTRODUCTION
 TOP
 ABSTRACT
 INTRODUCTION
 PATIENTS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
In recent years, laparoscopic adrenalectomy (L-ADX) has been promoted as being superior to traditional adrenalectomy, using either a transabdominal (TA-ADX) or a retroperitoneal (RP-ADX) approach. Although the operation time is still longer, post-operative pain and hospital stay are less than with any open technique (1–3). However, L-ADX is a less suitable technique for large and/or malignant adrenal lesions and its morbidity and mortality have not been evaluated in large series.

Before the advent of L-ADX, earlier reports comparing the retroperitoneal with the transabdominal approach have stated that an important disadvantage of the retroperitoneal approach was the impossibility of exploring beyond the ipsilateral adrenal gland. This has been considered a major drawback for the use of RP-ADX in the treatment of adrenal cancer and pheochromocytoma. However, improved pre-operative localization techniques have practically eliminated this disadvantage as they allow for pre-operative assessment of local and distant disease in both malignancy and pheochromocytoma. Until the recent advent of L-ADX, the retroperitoneal approach had become the preferred approach for benign adreno­cortical lesions because of its shorter operation time, lower blood loss, less intra-operative complications and post-operative morbidity and shorter hospital stay (4–8). The transabdominal approach was reserved for pheochromocytoma or malignant adreno­cortical disease (5,9–11), as this approach permits wide exposure for ‘en bloc’ excision in the case of malignant tumours and allows exploration of the contralateral adrenal gland and extra-adrenal sites in the case of pheochromocytoma.

We evaluated a group of 284 patients who had undergone a total of 326 adrenal operations in order to compare the merits of the transabdominal and retroperitoneal approaches with regard to operation time, blood loss, hospital stay and intra- and post-operative complications in patients with all kinds of adrenal disease, with emphasis on cases with large adrenal lesions, including pheochromocytoma and adrenal cancer. In addition, we analysed the accuracy of pre-operative localization techniques with respect to the presence of adrenal and associated pathology. Laparoscopic adrenalectomy, while rapidly becoming the standard of care for small- and inter­mediate-sized adrenal lesions, will have to be compared against the results of open adrenalectomy as reported in this and other series.


    PATIENTS AND METHODS
 TOP
 ABSTRACT
 INTRODUCTION
 PATIENTS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
Patients
The records of all patients who had undergone adrenal surgery between 1947 and 1995 at Leiden University Hospital were reviewed. Patients who had undergone exploration only and patients who had been reoperated on for local recurrence of malignant disease were excluded. Using these criteria, 284 patients who had undergone 326 operations (including 284 first, 38 second and four third operations) remained for evaluation. There were 82 (29%) males and 202 (71%) females, varying in age from 2 to 83 years (mean 38.6 years).

Diagnosis
Most patients presented with Cushing’s syndrome (167 patients; 59%), followed by symptoms due to pheochromo­cytoma (61 patients; 21%). Other patients presented with primary aldosteronism (15 patients; 5%) or with symptoms of virilization (15 patients; 5%) or feminization (three patients; 1%). In 19 asymptomatic patients (7%) an adrenal tumour was accidentally found by localization studies. These patients were operated on because the tumour was suspected of malignancy because of the aspect and size of the lesion. In four patients (1%) the presenting symptom was unknown.

Histological investigation of the adrenal lesions revealed adrenal hyperplasia in almost half of the cases (45%), while adrenal adenoma (13%), adrenal carcinoma (13%) and pheochromocytoma (18%) were found less frequently. In a minority of the cases (7%) the removed adrenal showed no abnormality. Other diagnoses, such as metastasis of other primary tumours, were found in a few cases only (2%).

Pre-operative Localization Studies
Pre-operative localization studies were performed using computed tomography (CT), magnetic resonance imaging (MRI) and m-iodobenzylguanidine (MIBG) scanning. CT scanning was performed using 10 mm slices, followed by more detailed studies using thinner slices in the case of negative or equivocal results. MRI studies in most patients were made using both T1 and T2 relaxation times. The choice of slice thickness and the plane resolution were adjusted to the size of the tumour expected. Oral contrast, if given, consisted of an initial dose of 500 ml of 1–2% iodinated contrast material, followed by 250 ml of the same contrast material immediately before scanning. IV contrast, if used, consisted of an intra­venous bolus injection of 50–100 ml of water-soluble iodinated contrast. Whole-body MIBG scanning was performed 48 h (and sometimes 24 and 72 h) following the slow intra­venous administration of 0.5 mCi of [131I]MIBG. Operative findings, in combination with post-operative clinical course, were used as the gold standard for pre-operative localization studies.

Other pre-operative localization studies such as ultrasono­graphy and retroperitoneal air insufflation, that was performed only in the earlier years of this study, were carried out less frequently and will not be discussed any further.

Operating Procedures
ADX was performed either unilaterally (right- or left-sided only) or using a one-stage bilateral procedure. Operations were performed using a transabdominal or retroperitoneal approach, the choice being made on clinical grounds (nature and extent of adrenal disease). TA-ADX consisted of adrenalectomy through a vertical or transverse epigastric incision or using a thoraco-abdominal incision with wide intentional opening of the peritoneal sac. RP-ADX included all operations with no or limited (accidental or intentional) opening of the peritoneum and abdominal cavity, using either a paravertebral, lumbar or thoraco-abdominal incision.

Adrenalectomies were in addition subdivided into unilateral and bilateral procedures and into simple adrenalectomies versus adrenalectomies that were combined with other procedures.

Outcome Measures
TA-ADX and RP-ADX were compared with respect to operation time, blood loss, intra-operative complications, post-operative morbidity and mortality and hospital stay.

Statistical Methods
The relation between characteristics of patient, lesion and procedure on the one hand and surgical approach on the other was analysed univariately using the chi-squared test for qualitative variables and the Mann–Whitney U-test for continuous variables (such as patient age and lesion weight). Likewise, the relation between surgical approach and outcomes variables was analysed using the chi-squared or Fisher’s exact test for discrete outcomes complications, morbidity or mortality and the Mann–Whitney U-test for the continuous outcomes of operation time, blood loss and hospital stay.

As univariate comparison of the outcomes of all cases of RP-ADX and TA-ADX may be confounded by the fact that patient age, lesion diagnosis and weight and year of operation may be non-randomly distributed over patients with different approaches, additional multivariate analyses were performed for relevant subgroups. For this purpose the confounders mentioned above were categorized into the following risk levels;

– patient age (age >=40 years and others);– lesion diagnosis (diagnosis carcinoma/pheochromocytoma and others);– lesion weight (weight categories <25 g, 25–200 g and >200 g);– year of operation (operations before and after 1980).

Logistic regression analysis was used for the discrete outcomes intra-operative complications and post-operative morbidity and mortality, and linear regression analysis for the continuous outcomes duration of operation, blood loss and hospital stay. The level of significance was set at p < 0.05 for all analyses.


    RESULTS
 TOP
 ABSTRACT
 INTRODUCTION
 PATIENTS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
Pre-operative Localization Studies
From 1978 onwards a total of 161 adrenals were studied by CT. Ninety-one of these were post-operatively demonstrated to be abnormal by histological criteria. The sensitivity of CT for adrenal pathology was 98% (89/91). The two lesions that were not detected by CT were cases of hyperplasia. The specificity was 99% (69/70); one lesion identified as a gland containing an adenoma was found to be a normal adrenal gland. From 1984 onwards 74 adrenals were investigated using MRI, with histologically verified pathology in 42 cases. In this series the overall sensitivity of MRI for detection of adrenal pathology was 100% (42/42), the specificity being 100% (32/32). From 1985 onwards MIBG scanning was used to localize pheochromocytoma, a total of 40 adrenals being investigated. The diagnostic accuracy of MIBG for pheochromocytoma was 95% (21/22), with a specificity of 100% (18/18). The one pheochromocytoma that was not found by MIBG was detected by both CT and MRI.

Operating Procedures
Some 326 adrenalectomies were performed in 284 patients, 299 unilaterally (92%) and 27 bilaterally (8%). The TA route was used in 59 (18%) operations, while an RP approach was utilized in 267 (82%) operations. Right-sided ADX was performed 154 times (47% of all operations) and left-sided ADX 145 times (44%).

Additional procedures were performed during 31 operations, most frequently in patients with adrenocortical carcinoma (19/31 operations; 61%) and in patients with pheochromocytoma (6/31 operations; 19%). The most frequent additional proced­ure was nephrectomy (16/31 operations; 52%) followed by splenectomy (6/31 operations; 19%), cholecystectomy (5/31; 16%) and resection of lung or liver metastases (4/31; 13%).

Overall Outcome of Adrenalectomy
The mean operation time for ADX was 114 min (range 30–270 min). The median blood loss during ADX was 300 ml (range 15–11,000 ml). Intra-operative complications occurred in 37 of 326 operations (11%). The majority of these complications involved injury of the adrenal vein or inferior caval vein (n = 25; 7.6%). Other complications (n = 12; 3.7%) included cardio­vascular problems (arrest, arrythmia, shock) (n = 5; 1.5%), splenic injury (n = 2; 0.6%) and coagulopathy (n = 2; 0.6%).

Post-operative morbidity occurred in 73 patients (22.4%), consisting mainly of wound healing problems (9%) and pulmonary problems (pleural effusion, pneumothorax and pneumonia) (8%). Less frequent were cardiovascular problems (hypertension, hypotension, arrhythmia), fever and adrenal insufficiency.

Six patients died within 30 days following adrenal surgery, an overall 30-day mortality rate of 2.1%. Of these patients three had adrenocortical carcinoma, one pheochromocytoma, one adrenocortical adenoma and one adrenal hyperplasia. Two patients died after 2 months following surgery (one patient with adrenocortical hyperplasia and one with adrenocortical carcinoma). The last death following surgery for non-malignant disease occurred in 1966. Death following surgery for malignant disease in all cases occurred after extensive additional procedures such as resection of liver metastases or resection of intracaval and intracardiac tumour growth. The mean post-operative hospital stay was 13.2 days.

The median weight of the removed lesions was 13 g with a maximum of 2770 g.

Univariate Comparison Between Characteristics of Patient, Lesion and Procedure on the One Hand and Surgical Approach on the Other (Table 1)
Patients undergoing TA-ADX were older than those undergoing RP-ADX (p = 0.046). The type of adrenal lesions differed between the two groups: more patients suffering from adrenocortical carcinoma underwent TA-ADX, while most patients with benign adrenocortical disease underwent RP-ADX (p < 0.001). Bilateral ADX (p < 0.001) and additional surgical procedures (p < 0.001) were more frequently performed in TA-ADX than in RP-ADX.

The patients were divided into two groups: (a) 237 patients operated from 1947 to 1980 and (b) 89 patients operated from 1981 to 1995) [i.e. before (group a) and after (group b) adequate localization techniques were available].

Univariate Comparison Between Surgical Approach and Outcome of Adrenalectomy (Table 2)
In univariate analysis of all patients RP-ADX was associated with shorter operation time, lower blood loss and shorter hospital stay than TA-ADX. In addition, post-operative morbidity was lower. Intra-operative complications and post-operative mortality did not differ between RP-ADX and TA-ADX. In the subgroup of patiens operated from 1981 onwards mortality was also lower with RP-ADX than TA-ADX.

Multivariate Analysis in Patients Undergoing Unilateral Adrenalectomy Only
We first performed multivariate analysis of outcomes of RP-ADX and TA-ADX in cases of unilateral adrenalectomy only, eliminating all cases of bilateral exploration and/or additional surgical procedures or where no information about the approach was available. This left 268 cases for analysis, of which 242 were RP-ADX and 26 TA-ADX. Of these patients, 72 had a carcinoma or pheochromocytoma, while 196 had other diagnoses.

Operation time was influenced by lesion weight only (p < 0.001) and not by the surgical approach taken (p = 0.113). Blood loss was influenced by lesion weight (p < 0.001) and also by the approach taken (p = 0.003). Intra-operative complications and post-operative morbidity did not depend significantly on any of the above-mentioned parameters (all p > 0.15), while post-operative mortality correlated marginally with lesion weight only (p = 0.059).

Hospital stay had no significant relationship with any of the above-mentioned confounders or with the approach taken (p > 0.162 in all cases).

Univariate and Multivariate Analysis in Patients with Carcinoma or Pheochromocytoma Undergoing Unilateral Adrenalectomy Only
As the largest differences in confounders might be expected in cases of adrenal carcinoma and pheochromocytoma, we repeated the above analyses for patients with these diagnoses only. This left a total of 65 operations, 25 for carcinoma and 40 for pheochromocytoma (Table 3).


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Table 3. Outcomes in 65 cases of transabdominal or retroperitoneal unilateral adrenalectomy for carcinoma or pheochromocytoma only (with univariate comparisons)
 
Multivariate analyses in these patients demonstrated that operation time was now influenced by lesion weight only (p = 0.002) and did not depend on the approach taken (p = 0.119). In contrast, blood loss depended not only on lesion weight (p = 0.016), but also on the approach taken (p = 0.028). Neither intra-operative complications nor post-operative morbidity or mortality were found to depend on any of the above param­eters, neither was hospital stay influenced by them (p > 0.156 in all cases).

Analysis of the subgroup of patients operated from 1981 on showed no other findings.

Uni- and Multivariate Analysis in Patients Unsuitable for Laparoscopic Adrenalectomy Because of Malignant and/or Large Lesions
Finally, we performed analyses in those patients who would nowadays be held less suitable for laparoscopic adrena­lectomy, i.e. those undergoing unilateral adrenalectomy for malignant or large lesions only (>100 g). This left 34 cases (25 carcinomas, seven pheochromocytomas and two large adenomas) out of our total of 326 (10.4%) (Table 4). Operations were performed by a retroperitoneal approach in 24 cases and a transabdominal approach in 10.


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Table 4. Outcomes in 34 cases of transabdominal or retroperitoneal unilateral adrenalectomy for carcinoma or large lesion only (with univariate comparisons)
 
Univariate comparison of the whole group of patients demonstrated that RP-ADX positively differed in blood loss and compared favourably but insignificantly so in operation time and hospital stay. Intra-operative complications occurred in one out of 24 RP-ADX and in four out of 10 TA-ADX (p = 0.019 by Fisher’s exact test). Post-operative morbidity and mortality did not differ significantly. The analysis in the subgroup of patients operated from 1981 onwards showed that operation time was also shorter in RP-ADX.

In multivariate analysis none of the above-described confounding variables significantly determined outcome.

Summary of Results
Although duration of operation, intra-operative blood loss, hospital stay and post-operative morbidity of RP-ADX compare favourably with TA-ADX, most of these differences are explained by the confounders lesion diagnosis and weight. However, in multivariate analysis some of the differences remained after correction for confounding.

RP-ADX compared favourably and significantly with TA-ADX with respect to (1) operation time and (2) blood loss both in all patients and in those with carcinoma or pheochromocytoma only and (3) intra-operative complications in those patients nowadays considered unsuitable for laparoscopic adrenalectomy because of malignant and/or large lesions.


    DISCUSSION
 TOP
 ABSTRACT
 INTRODUCTION
 PATIENTS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
It has been claimed that the use of the RP route for ADX is better tolerated by the patient because of the minimal wound pain and less post-operative paralytic ileus, leading to earlier post-operative ambulation (2,5) and shorter hospital stay (6–8). Furthermore, RP-ADX has been associated with shorter oper­ation time (5) because of the easy and direct access to the adrenal, especially in the adipose patient with Cushing’s syndrome, with lower blood loss (5,7) and with lower incidence of intra- and post-operative complications (4) and morbidity (6,7), such as splenic or pancreatic injury. Finally, RP-ADX will prevent the origination of intra-abdominal adhesions, thereby eliminating the risk of bowel obstruction. Still, in the case of adrenal cancer or pheochromocytoma the TA-ADX generally is considered the approach of choice, because of the wide exposure (5,9–11). This allows inspection and/or palpation of the contralateral gland and extra-adrenal sites and allows ‘en bloc’ excision in case of extended disease.

The results presented here are the results of a retrospective study with all its major drawbacks. Despite this, we consider that these results may bring about a change in the general idea that the surgical approach in cases of adrenal pathology or pheochromocytoma should always be a transabdominal one. Arguments for the use of RP-ADX are presented below.

In our series, CT, MRI and MIBG were used as pre-operative localization techniques for adrenal cancer and pheochromo­cytoma. The overall sensitivity of CT for non-hyperplastic adrenal disease is reported to be 94–100% (5,8,12,13), with a specificity of 100% (12). The overall sensitivity of MRI to detect adrenal and extra-adrenal masses is reported to be 100% (3,12), whereas for CT it was 91% (12,14,15). Therefore, MRI is considered to be superior to CT for the detection of both adrenal and extra-adrenal pheochromocytoma (12). MIBG is reported to have an overall sensitivity of 80–87.4% (8,16) and a specificity of 98.9% (16) for the detection of pheochromo­cytoma and is considered by many to be the initial localizing procedure of choice (16,17). CT, MRI and MIBG are complementary in localization of pheochromocytoma (17). The sensitivity and specificity of CT, MRI and MIBG reported in the present study corroborate with the above-mentioned studies. Therefore, for demonstrating contralateral or extra-adrenal pheochromocytoma or determining spread and metastasis of adrenal carcinoma, CT, MRI and MIBG scanning are at least as accurate as intra-operative visualization and palpation.

Another disadvantage ascribed to the retroperitoneal approach has been the inability to perform more extensive operations for carcinoma or large pheochromocytoma. The ability to perform ‘radical’ operations for carcinoma with the use of the RP approach is entirely dependent on the type of incision used. With the use of a (retroperitoneal) thoraco-abdominal incision, ‘radical’ operations are highly feasible and generate little discomfort. If needed, such incisions can easily be extended to the peritoneal cavity.

In most reports comparing the TA and RP approaches to the adrenal gland, the comparability of the groups of patients operated on by either approach is questionable, since the patients in these groups differ in underlying pathology. As in our study, in most reports the patients undergoing ADX by the TA route were suffering from carcinoma or pheochromocytoma. Since these patients are prone to more extensive surgery, it is not surprising to find that operation time, blood loss, intra-operative complications, morbidity and hospital stay differ in a negative way from patients operated on using the RP approach (these are mostly patients with benign adrenal disease). After reviewing the literature, we found only two other comparative studies examining the relative merits of the TA and RP approaches in patients with similar disease. In patients with adrenocortical hyperplasia and adenoma weighing less than 25 g, the posterior, RP approach was associated with less need for blood transfusion (p < 0.01) and shorter hospital stay (p < 0.01), while mortality and complications (morbidity) seemed less (7). In patients with pheochromocytoma, the use of a lateral, RP operative approach was associated with shorter hospital stay (p = 0.002), while the need for blood transfusion and post-operative morbidity seemed less (6).

The most recent development in the field of adrenal surgery is laparoscopic adrenalectomy. This technique used for small benign adrenal disease has been reported to be better tolerated by the patient, owing to less post-operative pain and more rapid recovery and shorter hospital stay, than the conventionally used open techniques of adrenalectomy (1,6,18). Although the experience with this new technique is growing rapidly, its inherent limitations will most likely reserve open adrenalectomy as the surgical procedure of preference for large and/or malignant lesions. In patients with these lesions we found that open adrenalectomy through a retroperitoneal route was associated with shorter operation time, lower blood loss and less intra-operative complications than a transabdominal approach. Therefore, in our hospital we nowadays almost exclusively remove large or malignant adrenal lesions through a retroperitoneal approach.

In conclusion, for small or benign adrenal disease, laparoscopic adrenalectomy has become the preferred technique. In those lesions or patients that are unsuitable for L-ADX, open adrenalectomy will be performed. Using a retroperitoneal approach in these cases may be associated with shorter operation time, less blood loss and less intra-operative complications. The availability of proper pre-operative localization studies in these cases guarantees that no other lesions will be missed.


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Table 1. Group characteristics of all patients undergoing transabdominal or retroperitoneal adrenalectomy
 

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Table 2. Outcomes in all 326 cases of transabdominal or retroperitoneal adrenalectomy (with univariate comparisons)
 

    FOOTNOTES
 
+ For reprints and all correspondence: C. J. H. van de Velde, Department of Surgery, Leiden University Medical Center, P.O. Box 9600, 2300 RC Leiden, The NetherlandsAbbreviations: RP-ADX, adrenalectomy through a retroperitoneal approach; TA-ADX, adrenalectomy through a transabdominal approach; L-ADX, laparoscopic adrenalectomy Back


    REFERENCES
 TOP
 ABSTRACT
 INTRODUCTION
 PATIENTS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
1 Bonjer HJ, Lange JF, Kazemier G, de Herder WW, Steyerberg EW, Bruining HA. Comparison of three techniques for adrenalectomy. Br J Surg 1997;84:679–82.[Web of Science][Medline]

2 Linos DA, Stylopoulos N, Boukis M, Souvatzoglou A, Raptis S, Papadimitriou J. Anterior, posterior or laparoscopic approach for the management of adrenal diseases? Am J Surg 1997;173:120–5.[Web of Science][Medline]

3 Pagny J, Marichez M, Plouin P, et al. Nuclear magnetic resonance imaging of adrenal tumors in hypertensive subjects. J Hypertension 1986;4:s665–6.

4 Blichert-Toft M, Bagerskov A, Lockwood K, Hasner E. Operative treatment, surgical approach and related complications in 195 operations upon the adrenal glands. Surg Gynecol Obstet 1971;135:261–6.[Web of Science]

5 Bruining HA, Lamberts SWJ, Ong EGL, van Seyen AJ. Results of adrenalectomy with various surgical approaches in the treatment of different diseases of the adrenal glands. Surg Gynecol Obstet 1984;158:367–9.[Web of Science][Medline]

6 Irvin III GL, Fishman LM, Sher JA, Yeung LK, Irani H. Pheochromocytoma: lateral versus anterior operative approach. Ann Surg 1989;209:774–8.[Web of Science][Medline]

7 Russell CF, Hamberger B, van Heerden JA, Edis AJ, Ilstrup DA. Adrenalectomy: anterior or posterior approach? Am J Surg 1982;144:322–4.[Web of Science][Medline]

8 Schwarz RJ, Schmidt N. Efficient management of adrenal tumors. Am J Surg 1991;161:576–9.[Web of Science][Medline]

9 Javadpour N. Surgical management. In: Javadpour N, editor. Principles and Management of Adrenal Cancer, 1st ed. Berlin: Springer 1987;165–73.

10 Scott HW Jr. The panic syndrome: pheochromocytoma. In: Friesen SR, Thompson: NW, editors. Surgical Endocrinology: Clinical Syndromes, 2nd ed. Philadelphia: JB Lippincott 1990;163–80.

11 Thompson NW: Cushing’s syndrome: hypercortisolism. In: Friesen SR, Thompson NW, editors. Surgical Endocrinology: Clinical Syndromes, 2nd ed. Philadelphia: JB Lippincott 1990: 405–20.

12 Falke THM. Localization and identification of adrenocortical and sympathomedullary disorders with CT and MRI. Thesis, State University, Leiden. The Hague: Pasmans 1989.

13 Malmaeus J, Markaes A, Öberg K, Abdalla El-Sherief M, Johansson H, Rastad J, et al. Adrenal gland surgery: pre-operative location of lesions, histological findings and outcome of surgery. Acta Chir Scand 1986;152:577–81.[Web of Science][Medline]

14 Chatal T, Charbonnel B. Comparison of iodobenzylguanidine imaging with computed tomography in locating pheochromocytoma. J Clin Endocrinol Metab 1985;61:769–72.[Abstract/Free Full Text]

15 Welch TJ, Sheedy PF II, van Heerden JA, Sheps SG, Hattery RR, Stephens DH. Pheochromocytoma: value of computed tomography. Radiology 1983;148:501–3.[Abstract/Free Full Text]

16 Shapiro B, Copp JE, Sisson JC, Eyre PL, Wallis J, Beierwaltes WH. Iodine-131 metaiodobenzylguanidine for the locating of suspected pheochromocytoma: experience in 400 cases. J Nucl Med 1985;26:576–85.[Abstract/Free Full Text]

17 Velchik MG, Alavi A, Kressel HY, Engelman K. Localization of pheochromocytoma: MIBG, CT and MRI correlation. J Nucl Med 1989;30:328–36.[Abstract/Free Full Text]

18 Prinz RA. A comparison of laparoscopic and open adrenalectomies. Arch Surg 1995;130:489–94.[Abstract/Free Full Text]

Received August 9, 1999; accepted November 12, 1999.


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