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Extent of adrenalectomy for adrenal neoplasm: cortical sparing (subtotal) versus total adrenalectomy
Surg Clin N Am 84 (2004) 743–753
Extent of adrenalectomy for adrenal neoplasm: cortical sparing (subtotal) versus total adrenalectomy Martin K. Walz, MD, PhD Clinic of Surgery and Center of Minimally Invasive Surgery, Kliniken Essen-Mitte, Akademisches Lehrkrankenhaus der Universita¨t Duisburg-Essen, Henricistraße 92, D-45136, Essen, Germany
Since the first descriptions of adrenal surgery, the standard extent of adrenalectomy has been the total or complete extirpation of the gland. In recent years, an increasing interest in reduced radicality can be noticed in the surgical treatment of adrenal neoplasias. Triggered by the revolution of minimally invasive surgery, terms such as ‘‘subtotal adrenalectomy,’’ ‘‘partial adrenalectomy,’’ and ‘‘cortical-sparing’’ or ‘‘adrenal-sparing adrenalectomy’’ are more often found in the literature (Fig. 1). The concept based on these ‘‘noncomplete’’ adrenalectomies is the preservation of the adrenal cortical function, estimating the risks of recurrence or persistent disease versus adrenal insufficiency or Addison’s crisis. Up to now, the indications of noncomplete adrenalectomy, and the technical aspects concerning the essential extent of preserved tissue and the method of dissection have been controversial [1–6]. Although intended partial adrenalectomy has been used in adrenocorticotropic hormone (ACTH)-depending Cushing’s disease since the 1950s [7], this strategy is relatively new in the treatment of adrenal neoplasias. Noncomplete adrenalectomy has been performed, especially in bilateral pheochromocytomas, usually based on inherited diseases. Irvin and colleagues presented the first description in 1983 [8]. In three patients with familiar bilateral pheochromocytomas, they showed that preservation of the adrenal cortical function could be achieved by subtotal adrenalectomy. In 1984,
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90 80 70 60 50 40 30 20 10 0 -1953
1954-58 1959-63 1964-68 1969-73 1974-78 1979-83 1984-88 1989-93 1994-98 1999-03
Fig. 1. Number of publications concerning noncomplete (partial, subtotal, cortical-sparing, adrenal-sparing) adrenalectomy. Data from a search of PubMed Medline at: http:// www.ncbi.nlm.nih.gov. Accessed 2004.
van Heerden et al published two cases of multiple endocrine neoplasias (MEN) 2 syndrome with recurrent pheochromocytomas following subtotal adrenalectomy [9]. The time interval between primary and recurrent disease was more than 30 years in these two cases. In the era of endoscopic adrenalectomy, our group presented partial adrenalectomy for the first time. In a series of 27 patients, a resection of the gland was performed in 5 patients. Two of them suffered from bilateral pheochromocytomas; preservation of cortical function could be achieved completely in 1 patient [10]. Meanwhile, other groups also have adopted this concept, not only for pheochromocytomas, but also in Conn’s adenomas and Cushing’s adenomas [11–17].
Sequelae of unilateral or bilateral adrenalectomy Bilateral adrenalectomy requires a lifelong corticoid supplementation. This therapy has to be individually planned and adapted to actual circumstances. Patients should not have signs of over- or undertreatment, such as Cushing’s symptoms or fatigue. The main problem following bilateral adrenalectomy is hypocortisolism. Lairmore et al described 43 patients with bilateral pheochromocytomas and complete biadrenaletomy. Ten patients (23%) developed at least one episode of adrenal insufficiency, including 1 patient who died due to Addisonian crisis during an influenza [18]. Death related to adrenal insufficiency following bilateral adrenalectomy has also been mentioned by other authors [7]. In a group of 33 patients with bilateral adrenalectomy for Cushing’s disease, 3 patients (9%) had to
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be hospitalized because of acute steroid deficiency, and 20 patients (60%) suffered from chronic fatigue [19]. As reported by Telenius-Berg and coworkers, quality of life in biadrenalectomized patients is impaired by fatigue and worry [20]. This study also demonstrated relevant difficulties or noncompliance in taking the steroid medication, leading to extraordinary hospital admissions in one third of patients. Compared with the sequelae of bilateral adrenalectomy, functional complications after complete unilateral adrenalectomy are minor and rare. Normally the contralateral gland replaces the hormone secretion immediately, except in Cushing’s syndrome, which requires temporary corticoid supplementation for weeks to months. Reports about adrenal insufficiency after adrenalectomy for Conn’s adenomas are exceptional [21]. Potentially, patients needing unilateral adrenal surgery may lose the contralateral gland during their lives, due to trauma or because of other reasons, or may have even lost this gland before surgery. This mainly concerns patients with inherited pheochromocytomas, as their adrenal tumors often develop metachroneously, but it also may occur in sporadic diseases. In our group of about 400 patients with adrenalectomy performed during the last 10 years, 1 female patient suffered from a pheochromocytoma on the left side [11]. Her contralateral gland had been removed with her kidney due to renal cancer 12 years before. After left-partial adrenalectomy, she does not need corticoid treatment. This case demonstrates the potential benefit of a partial adrenalectomy, even in sporadic diseases. Noncomplete adrenalectomy in pheochromocytomas About 10% to 20% of pheochromocytomas are based on genetic disorders such as MEN type 2A or 2B, von Hippel-Lindau disease (VHL), neurofibromatosis, or new genes (succinate dehydrogenase subunit D and B [SDHD, SDHB]) [22,23]. These diseases show different genotype-phenotype relations affecting the adrenal glands and other chromaffine tissue in 1% to 50% of patients [24]. The nonsporadic pheochromocytomas are diagnosed between age 20 and age 40 [23], demonstrating the extended time needed for the development of a single tumor. Based on these data, the individual fate of affected patients cannot be accurately estimated. Therefore, the concept of preservation of cortical function has to be taken into consideration, especially in inherited diseases, and furthermore, is increasingly demanded by well-informed patients. Noncomplete adrenalectomy has been used in cases of pheochromocytoma with or without genetic disposition [1,6,8,9,13,16,25–40]. A subtotal adrenalectomy in sporadic disease mainly carries the risk of a persistent illness. In genetic disorders, a recurrent pheochromocytoma may additionally arise from the remnant tissue. The basic question concerns the rate of persistent and recurrent pheochromocytomas in total compared with subtotal adrenalectomy.
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In pheochromocytomas, complete adrenalectomy does not guarantee cure [41]. Locoregional recurrences are a well-known phenomenon, probably due to intraoperative spillage. In a recently published series, 8 of 260 patients developed local recurrences within a mean follow-up of 8 years [42]. Liu found 10 recurrent tumors in 210 patients after 1 to 21 years [43], and van Heerden et al saw a local relapse in 3 of 98 patients 5 to 13 years following the initial resection [44]. Persistent pheochromocytomas are rare after complete adrenalectomy. These cases occurred in the era before the availability of CT and MRI, when the tumor was missed intraoperatively. Most reports of noncomplete adrenalectomy concern pheochromocytomas. During the ‘‘open-approach’’ period, several groups initially published small series or case reports [8,9,25,27,29,34,45]. A more extended study was presented by Neumann and colleagues [33]. Between 1985 and 1998, they performed partial adrenalectomies in 38 of 39 consecutive patients with pheochromocytomas. Bilateral tumors occurred in 13 patients, and all but one was free of steroid supplementation. Similar data have been described by Lee et al [31], and recently by Brauckhoff and coworkers [6]. Since the initiation of the posterior retroperitoneoscopic approach in 1994, we have performed partial adrenalectomies in 27 patients with pheochromocytomas, including 14 patients with bilateral tumors. Only 1 patient needs corticoid treatment (Table 1). Data on recurrences after partial adrenalectomy in inherited pheochromocytomas are inconsistent. Whereas Inabnet at al [37] in 3 of 5 patients and van Heerden et al [9] in 2 patients saw a relapse following nontotal adrenalectomy, others found no cases or only one case of recurrence in larger series (Table 2). The controversial data may be explained by different lengths of follow-up. Probably, the recently published (mainly laparoscopic) studies underestimate the risk of recurrence. As the relapse of pheochromocytomas is usually diagnosed 10 years or longer after the initial resection [46,47], long-term follow-up is essential but not realized in most cases (see Table 1). Recurrent pheochromocytomas occur in MEN 2 syndrome as well as in VHL. Differences in biological behavior of these two entities are not evident. A minor problem of partial adrenalectomy in pheochromocytomas is a persistent disease. This may happen in a multinodular adrenal tumor when additional nodules are overlooked during the dissection. Therefore, intraoperative ultrasonography should be used in all cases of partial adrenalectomy, or at least in cases of doubt. In recent years, we saw a patient with MEN 2A syndrome and two 2-cm pheochromocytomas in a partially resected gland 1 year after the prior laparoscopic procedure [46]. To the best of our knowledge, this is the only published case of persistent disease following noncomplete adrenalectomy for pheochromocytomas. In case of a locally recurrent pheochromocytoma, surgical removal is the treatment of choice. In these cases the surgical approach depends on the surgeon’s preference and experience [46,48]. As most patients with
Table 1 Noncomplete bilateral adrenalectomy for adrenal neoplasias
Year
Patients (n)
Diagnosis
Surgical approach
Main veins divided (n)
Irvin [8] van Heerden [9] van Heerden [27] Hamberger [28] Birnbaum [29] Albanese [30] Lee [31] Janetscheck [32] Neumann [33] de Graff [34] Edstrom [35] Mugiya [36] Inabnet [37] Walther [16] Kaock [39] Porpiglia [38] Brauckhof [6] Brauckhof [40] Walz (unpublished)
1983 1984 1985 1987 1989 1993 1996 1998 1999 1999 1999 1999 2000 2000 2002 2002 2003 2003 2004
3 2 1 2 1 4 14 4 13 4 5 1 5 9 1 1 12 5 14
FP MEN MEN MEN SP FP MEN VHL MEN MEN MEN MEN MEN VHL SP MEN MEN MEN MEN
open open open open open open open laparoscopic open open open laparoscopic/retroperitoneoscopic open open and laparoscopic laparoscopic laparoscopic open laparoscopic retroperitoneoscopic
nd nd 0 2 nd nd nd 0 10 4 5 1 nd nd 0 1 10 5 13
3 1 1 2 1 4 13 4 12 4 3 1 2 9 1 1 11 5 13
2 2 2
2, VHL 2, VHL, NF 2 2 2 2, VHL, NF
2 2, VHL, SP, M 2, BNH 2, VHL, SDHD, SP
Recurrence (n)
Follow-up (months)
0 2 0 0 0 0 1 0 1 1 0 0 3 0 0 0 0 0 0
36–84 360–375 18 6–24 32 80–96 118–324 2–24 16–179 19–53 96–156 3 36–300 nd 3 12 3–76 6–36 1–92
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Author
Patients without steroid suppl. (n)
Abbreviations: BNH, adrenocortical nodular hyperplasia; FP, familial pheochromocytoma; M, adrenal metastases; MEN, multiple endocrine neoplasia; nd, no data; NF, neurofibromatosis; SDHD, succinate dehydrogenase subunit D; SP, sporadic pheochromocytoma; VHL, non-Hippel-Lindau disease. 747
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Table 2 ‘‘Noncomplete’’ unilateral adrenalectomy for adrenal neoplasias studies with more than 5 patient Author
Patients Year (n) Diagnosis
Surgical approach
Bao [25] Nakada [51] Walz [1]
1987 6 1995 26 1998 20
open 0 open 0 retroperitoneoscopic 0
nd 60 11
Imai [57] Pautler [26] Kok [54] Ikeda [58] Sasagawa [13]
1999 5 2002 11 2002 8 2003 9 2003 47
laparoscopic laparoscopic laparoscopic laparoscopic retroperitoneoscopic
0 0 0 0 0
3 0.45 nd 20–27 nd
Jeschke [4] Meria [50]
2003 13 2003 20
laproscopic laproscopic
0 0
39 nd
Pheo Conn Conn, Cushing, Pheo NF Conn, NF Pheo Conn Conn, Pheo Conn, Cushing, Pheo, NF Conn Conn
Recurrence Follow-up (n) (months)
Abbreviations: nd, no data; NF, non-functioning adrenal tumor; Pheo, pheochromocytoma.
a recurrent tumor diagnosed today have undergone an open approach transabdominally or posteriorly during their first operation, an endoscopic technique in the opposite route (laparoscopic or retroperitoneoscopic) should be taken into consideration; the adrenal gland can thereby be reached with few scars. Compared with open surgery, experiences with endoscopic reoperations in recurrent pheochromocytomas are still limited, but feasibility and safety have been demonstrated [46].
Noncomplete adrenalectomy in Conn’s adenomas and Cushing’s adenomas Conn’s adenomas seem to be an ideal indication for a partial adrenalectomy, due to different reasons. First, these tumors are almost always benign; second, they are small; and third, they often lie eccentrically. These conditions facilitate a partial adrenalectomy, but neoplastic and normal tissue has to be differentiated exactly (Fig. 2). Total adrenalectomy in Conn’s syndrome results in biochemical cure in almost all cases [49–53], as the data of partial adrenalectomy also demonstrate [1,4,17,50,51,54,55]. Surgeons using partial adrenalectomy in Conn’s syndrome argue that the removal of the tumor cures the patient if he or she has a single adenoma. In case of erroneous excision of a single nodule in multinodular hyperplasia, the patient is not cured, even by complete adrenalectomy, because the disease is always bilateral [1]. Persistent hyperaldosteronism following noncomplete adrenalectomy has been reported once [56]. In this case, two clearly visible tumors were located in one adrenal gland by computed tomography. In the initial operation, the nonfunctioning lesion was removed and the active nodule left in place. Intraoperatively, ultrasonography
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Fig. 2. Intraoperative ultrasonography. The adrenal tumor (Conn’s adenoma) can clearly be differentiated from the normal adrenal tissue.
was not used to localize the tumors. Cure has been achieved by a second open procedure. Compared with Conn’s syndrome, the experiences of partial adrenalectomy in patients with Cushing’s syndrome are very limited [1,5] Our earlier description of subtotal adrenalectomy in 22 patients with adrenal neoplasias included 4 patients with Cushing’s adenomas. These tumors had a size of 2 cm to 3 cm in diameter, and therefore no risk for malignancy [1]. Recurrent disease has not occurred after a mean follow up of 6.5 years.
Technical aspects of noncomplete adrenalectomy As shown by clinical experience and endocrinological tests, preservation of the cortical function can be achieved by one third of one adrenal gland [6]. In reverse, if this amount of adrenal tissue cannot be preserved, complete adrenalectomy has to be recommended, especially in inherited pheochromocytomas, to minimize the risk of recurrence. It is not known whether smaller bilateral remnants allow a preservation of the cortical function. Dissection of the adrenal tissue can be performed safely with electrocauter, harmonic scalpel, and clip application or vascular stapler [1,5,40,57,58]. The disadvantages of stapling are a reduction of the remaining tissue and higher costs. We usually use a monopolar electrocauter without seeing bleeding, even when congestion has to be assumed following dissection of the vein [11]. Partial adrenalectomy is technically feasible and safe and does increase blood loss or operating time. Adrenal cortical function does not depend on patency of the main adrenal vein [6,11]. This seems to be essential, as pheochromocytomas are typically growing close to this vein, and the dissection of this vessel cannot be avoided in most of these cases (see Table 1). At that point, an exact knowledge of the anatomical variations of the main
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adrenal vein is of great importance. Whereas adrenal veins on the left side uniquely join the renal vein close to the upper pole of the kidney, adrenal veins on the right side have variations in about 10% of patients. Double veins and conjunctions with posterior hepatic veins have to be taken into account [12]. If a noncomplete adrenalectomy is planed, intraoperative (laparoscopic) ultrasound is useful and sometimes essential [26,59]. A clear identification of the border of normal and neoplastic tissue is possible, as the probe is directly positioned on the region of interest (see Fig. 2). Additionally, it allows verification or exclusion of further tumors in the same gland [58]. This is essential in multinodular cases and inherited pheochromocytomas.
Summary The standard operation on adrenal neoplasias is a complete adrenalectomy. Accepted exceptions are bilateral inherited pheochromocytomas. In these cases, clinical and biochemical cure, as well as preservation of cortical function, can be achieved by a noncomplete adrenalectomy. In that procedure, at least one third of one gland has to be preserved. In unilateral adrenal tumors, partial resection has been used, especially in Conn’s adenomas, with early results comparable to those of total adrenalectomy. Because long-term results are still limited in hyperaldosteronism, final conclusions are not possible today.
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[31] Lee JE, Curley SA, Gagel RF, Evans DB, Hickey RC. Cortical-sparing adrenalectomy for patients with bilateral pheochromocytoma. Surgery 1996;120(6):1064–70. [32] Janetschek G, Finkenstedt G, Gasser R, Waibel UG, Peschel R, Bartsch G, et al. Laparoscopic surgery for pheochromocytoma: adrenalectomy, partial resection, excision of paragangliomas. J Urol 1998;160(2):330–4. [33] Neumann HP, Bender BU, Reincke M, Eggstein S, Laubenberger J, Kirste G. Adrenalsparing surgery for phaeochromocytoma. Br J Surg 1999;86(1):94–7. [34] de Graaf JS, Lips CJ, Rutter JE, van Vroonhoven TJ. Subtotal adrenalectomy for phaeochromocytoma in multiple endocrine neoplasia type 2A. Eur J Surg 1999;165(6):535–8. [35] Edstrom E, Grondal S, Norstrom F, Palmer M, Svensson KA, Widell H, et al. Long term experience after subtotal adrenalectomy for multiple endocrine neoplasia type IIA. Eur J Surg 1999;165(5):431–5. [36] Mugiya S, Suzuki K, Saisu K, Fujita K. Unilateral laparoscopic adrenalectomy followed by contralateral retroperitoneoscopic partial adrenalectomy in a patient with multiple endocrine neoplasia type 2a syndrome. J Endourol 1999;13(2):99–104 [discussion: 6]. [37] Inabnet WB, Caragliano P, Pertsemlidis D. Pheochromocytoma: inherited associations, bilaterality, and cortex preservation. Surgery 2000;128(6):1007–11. [38] Porpiglia F, Destefanis P, Bovio S, Allasino B, Orlandi F, Fontana D, et al. Corticalsparing laparoscopic adrenalectomy in a patient with multiple endocrine neoplasia Type IIA. Horm Res 2002;57(5–6):197–9. [39] Kaouk JH, Matin S, Bravo EL, Gill IS. Laparoscopic bilateral partial adrenalectomy for pheochromocytoma. Urology 2002;60(6):1100–3. [40] Brauckhoff M, Kaczirek K, Thanh PN, Gimm O, Brauckhoff K, Ba¨r A, et al. Technical aspects of subtotal endoscopic adrenalectomy. European Surgeon 2003;35:84–8. [41] Brennan MF, Keiser HR. Persistent and recurrent pheochromocytoma: the role of surgery. World J Surg 1982;6(4):397–402. [42] Bel’tsevich DG, Kuznetsov NS. Causes of recurrence of patients with chromaffin tumors. Khirurgiia (Mosk) 2002;(8):19–23. [43] Liu DY. Diagnosis and treatment of recurrent pheochromocytoma. Zhonghua Wai Ke Za Zhi 1993;31(10):622–4. [44] van Heerden JA, Roland CF, Carney JA, Sheps SG, Grant CS. Long-term evaluation following resection of apparently benign pheochromocytoma(s)/paraganglioma(s). World J Surg 1990;14(3):325–9. [45] Klempa I, Menzel J, Baca I. Subtotale Adrenalektomie versus Autotransplantation der Nebennierenrinde—Alternativverfahren bei der bilateralen Adrenalektomie bei MEN II? (Subtotal adrenalectomy versus autotransplantation of adrenal cortex- an alternative procedure is bilateral adrenalectomy in MEN II) Chirurg 1989;60(4):266–71. [46] Walz MK, Neumann HPH, Peitgen K, Petersenn S, Janssen OE, Mann K. Endoscopic treatment of recurrent and extraadrenal pheochromocytomas. European Surgeon 2003;35: 93–6. [47] Sparagana M. Late recurrence of benign pheochromocytomas: the necessity for long-term follow-up. J Surg Oncol 1988;37(2):140–6. [48] Al-Sobhi S, Peschel R, Zihak C, Bartsch G, Neumann H, Janetschek G. Laparoscopic partial adrenalectomy for recurrent pheochromocytoma after open partial adrenalectomy in von Hippel-Lindau disease. J Endourol 2002;16(3):171–4. [49] Rutherford JC, Stowasser M, Tunny TJ, Klemm SA, Gordon RD. Laparoscopic adrenalectomy. World J Surg 1996;20(7):758–60. [50] Meria P, Kempf BF, Hermieu JF, Plouin PF, Duclos JM. Laparoscopic management of primary hyperaldosteronism: clinical experience with 212 cases. J Urol 2003;169(1):32–5. [51] Nakada T, Kubota Y, Sasagawa I, Yagisawa T, Watanabe M, Ishigooka M. Therapeutic outcome of primary aldosteronism: adrenalectomy versus enucleation of aldosteroneproducing adenoma. J Urol 1995;153(6):1775–80.
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Extent of adrenalectomy for adrenal neoplasm: cortical sparing (subtotal) versus total adrenalectomy Martin K. Walz, MD, PhD Clinic of Surgery and Center of Minimally Invasive Surgery, Kliniken Essen-Mitte, Akademisches Lehrkrankenhaus der Universita¨t Duisburg-Essen, Henricistraße 92, D-45136, Essen, Germany
Since the first descriptions of adrenal surgery, the standard extent of adrenalectomy has been the total or complete extirpation of the gland. In recent years, an increasing interest in reduced radicality can be noticed in the surgical treatment of adrenal neoplasias. Triggered by the revolution of minimally invasive surgery, terms such as ‘‘subtotal adrenalectomy,’’ ‘‘partial adrenalectomy,’’ and ‘‘cortical-sparing’’ or ‘‘adrenal-sparing adrenalectomy’’ are more often found in the literature (Fig. 1). The concept based on these ‘‘noncomplete’’ adrenalectomies is the preservation of the adrenal cortical function, estimating the risks of recurrence or persistent disease versus adrenal insufficiency or Addison’s crisis. Up to now, the indications of noncomplete adrenalectomy, and the technical aspects concerning the essential extent of preserved tissue and the method of dissection have been controversial [1–6]. Although intended partial adrenalectomy has been used in adrenocorticotropic hormone (ACTH)-depending Cushing’s disease since the 1950s [7], this strategy is relatively new in the treatment of adrenal neoplasias. Noncomplete adrenalectomy has been performed, especially in bilateral pheochromocytomas, usually based on inherited diseases. Irvin and colleagues presented the first description in 1983 [8]. In three patients with familiar bilateral pheochromocytomas, they showed that preservation of the adrenal cortical function could be achieved by subtotal adrenalectomy. In 1984,
E-mail address: [email protected] 0039-6109/04/$ - see front matter Ó 2004 Elsevier Inc. All rights reserved. doi:10.1016/j.suc.2004.01.003
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90 80 70 60 50 40 30 20 10 0 -1953
1954-58 1959-63 1964-68 1969-73 1974-78 1979-83 1984-88 1989-93 1994-98 1999-03
Fig. 1. Number of publications concerning noncomplete (partial, subtotal, cortical-sparing, adrenal-sparing) adrenalectomy. Data from a search of PubMed Medline at: http:// www.ncbi.nlm.nih.gov. Accessed 2004.
van Heerden et al published two cases of multiple endocrine neoplasias (MEN) 2 syndrome with recurrent pheochromocytomas following subtotal adrenalectomy [9]. The time interval between primary and recurrent disease was more than 30 years in these two cases. In the era of endoscopic adrenalectomy, our group presented partial adrenalectomy for the first time. In a series of 27 patients, a resection of the gland was performed in 5 patients. Two of them suffered from bilateral pheochromocytomas; preservation of cortical function could be achieved completely in 1 patient [10]. Meanwhile, other groups also have adopted this concept, not only for pheochromocytomas, but also in Conn’s adenomas and Cushing’s adenomas [11–17].
Sequelae of unilateral or bilateral adrenalectomy Bilateral adrenalectomy requires a lifelong corticoid supplementation. This therapy has to be individually planned and adapted to actual circumstances. Patients should not have signs of over- or undertreatment, such as Cushing’s symptoms or fatigue. The main problem following bilateral adrenalectomy is hypocortisolism. Lairmore et al described 43 patients with bilateral pheochromocytomas and complete biadrenaletomy. Ten patients (23%) developed at least one episode of adrenal insufficiency, including 1 patient who died due to Addisonian crisis during an influenza [18]. Death related to adrenal insufficiency following bilateral adrenalectomy has also been mentioned by other authors [7]. In a group of 33 patients with bilateral adrenalectomy for Cushing’s disease, 3 patients (9%) had to
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be hospitalized because of acute steroid deficiency, and 20 patients (60%) suffered from chronic fatigue [19]. As reported by Telenius-Berg and coworkers, quality of life in biadrenalectomized patients is impaired by fatigue and worry [20]. This study also demonstrated relevant difficulties or noncompliance in taking the steroid medication, leading to extraordinary hospital admissions in one third of patients. Compared with the sequelae of bilateral adrenalectomy, functional complications after complete unilateral adrenalectomy are minor and rare. Normally the contralateral gland replaces the hormone secretion immediately, except in Cushing’s syndrome, which requires temporary corticoid supplementation for weeks to months. Reports about adrenal insufficiency after adrenalectomy for Conn’s adenomas are exceptional [21]. Potentially, patients needing unilateral adrenal surgery may lose the contralateral gland during their lives, due to trauma or because of other reasons, or may have even lost this gland before surgery. This mainly concerns patients with inherited pheochromocytomas, as their adrenal tumors often develop metachroneously, but it also may occur in sporadic diseases. In our group of about 400 patients with adrenalectomy performed during the last 10 years, 1 female patient suffered from a pheochromocytoma on the left side [11]. Her contralateral gland had been removed with her kidney due to renal cancer 12 years before. After left-partial adrenalectomy, she does not need corticoid treatment. This case demonstrates the potential benefit of a partial adrenalectomy, even in sporadic diseases. Noncomplete adrenalectomy in pheochromocytomas About 10% to 20% of pheochromocytomas are based on genetic disorders such as MEN type 2A or 2B, von Hippel-Lindau disease (VHL), neurofibromatosis, or new genes (succinate dehydrogenase subunit D and B [SDHD, SDHB]) [22,23]. These diseases show different genotype-phenotype relations affecting the adrenal glands and other chromaffine tissue in 1% to 50% of patients [24]. The nonsporadic pheochromocytomas are diagnosed between age 20 and age 40 [23], demonstrating the extended time needed for the development of a single tumor. Based on these data, the individual fate of affected patients cannot be accurately estimated. Therefore, the concept of preservation of cortical function has to be taken into consideration, especially in inherited diseases, and furthermore, is increasingly demanded by well-informed patients. Noncomplete adrenalectomy has been used in cases of pheochromocytoma with or without genetic disposition [1,6,8,9,13,16,25–40]. A subtotal adrenalectomy in sporadic disease mainly carries the risk of a persistent illness. In genetic disorders, a recurrent pheochromocytoma may additionally arise from the remnant tissue. The basic question concerns the rate of persistent and recurrent pheochromocytomas in total compared with subtotal adrenalectomy.
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In pheochromocytomas, complete adrenalectomy does not guarantee cure [41]. Locoregional recurrences are a well-known phenomenon, probably due to intraoperative spillage. In a recently published series, 8 of 260 patients developed local recurrences within a mean follow-up of 8 years [42]. Liu found 10 recurrent tumors in 210 patients after 1 to 21 years [43], and van Heerden et al saw a local relapse in 3 of 98 patients 5 to 13 years following the initial resection [44]. Persistent pheochromocytomas are rare after complete adrenalectomy. These cases occurred in the era before the availability of CT and MRI, when the tumor was missed intraoperatively. Most reports of noncomplete adrenalectomy concern pheochromocytomas. During the ‘‘open-approach’’ period, several groups initially published small series or case reports [8,9,25,27,29,34,45]. A more extended study was presented by Neumann and colleagues [33]. Between 1985 and 1998, they performed partial adrenalectomies in 38 of 39 consecutive patients with pheochromocytomas. Bilateral tumors occurred in 13 patients, and all but one was free of steroid supplementation. Similar data have been described by Lee et al [31], and recently by Brauckhoff and coworkers [6]. Since the initiation of the posterior retroperitoneoscopic approach in 1994, we have performed partial adrenalectomies in 27 patients with pheochromocytomas, including 14 patients with bilateral tumors. Only 1 patient needs corticoid treatment (Table 1). Data on recurrences after partial adrenalectomy in inherited pheochromocytomas are inconsistent. Whereas Inabnet at al [37] in 3 of 5 patients and van Heerden et al [9] in 2 patients saw a relapse following nontotal adrenalectomy, others found no cases or only one case of recurrence in larger series (Table 2). The controversial data may be explained by different lengths of follow-up. Probably, the recently published (mainly laparoscopic) studies underestimate the risk of recurrence. As the relapse of pheochromocytomas is usually diagnosed 10 years or longer after the initial resection [46,47], long-term follow-up is essential but not realized in most cases (see Table 1). Recurrent pheochromocytomas occur in MEN 2 syndrome as well as in VHL. Differences in biological behavior of these two entities are not evident. A minor problem of partial adrenalectomy in pheochromocytomas is a persistent disease. This may happen in a multinodular adrenal tumor when additional nodules are overlooked during the dissection. Therefore, intraoperative ultrasonography should be used in all cases of partial adrenalectomy, or at least in cases of doubt. In recent years, we saw a patient with MEN 2A syndrome and two 2-cm pheochromocytomas in a partially resected gland 1 year after the prior laparoscopic procedure [46]. To the best of our knowledge, this is the only published case of persistent disease following noncomplete adrenalectomy for pheochromocytomas. In case of a locally recurrent pheochromocytoma, surgical removal is the treatment of choice. In these cases the surgical approach depends on the surgeon’s preference and experience [46,48]. As most patients with
Table 1 Noncomplete bilateral adrenalectomy for adrenal neoplasias
Year
Patients (n)
Diagnosis
Surgical approach
Main veins divided (n)
Irvin [8] van Heerden [9] van Heerden [27] Hamberger [28] Birnbaum [29] Albanese [30] Lee [31] Janetscheck [32] Neumann [33] de Graff [34] Edstrom [35] Mugiya [36] Inabnet [37] Walther [16] Kaock [39] Porpiglia [38] Brauckhof [6] Brauckhof [40] Walz (unpublished)
1983 1984 1985 1987 1989 1993 1996 1998 1999 1999 1999 1999 2000 2000 2002 2002 2003 2003 2004
3 2 1 2 1 4 14 4 13 4 5 1 5 9 1 1 12 5 14
FP MEN MEN MEN SP FP MEN VHL MEN MEN MEN MEN MEN VHL SP MEN MEN MEN MEN
open open open open open open open laparoscopic open open open laparoscopic/retroperitoneoscopic open open and laparoscopic laparoscopic laparoscopic open laparoscopic retroperitoneoscopic
nd nd 0 2 nd nd nd 0 10 4 5 1 nd nd 0 1 10 5 13
3 1 1 2 1 4 13 4 12 4 3 1 2 9 1 1 11 5 13
2 2 2
2, VHL 2, VHL, NF 2 2 2 2, VHL, NF
2 2, VHL, SP, M 2, BNH 2, VHL, SDHD, SP
Recurrence (n)
Follow-up (months)
0 2 0 0 0 0 1 0 1 1 0 0 3 0 0 0 0 0 0
36–84 360–375 18 6–24 32 80–96 118–324 2–24 16–179 19–53 96–156 3 36–300 nd 3 12 3–76 6–36 1–92
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Author
Patients without steroid suppl. (n)
Abbreviations: BNH, adrenocortical nodular hyperplasia; FP, familial pheochromocytoma; M, adrenal metastases; MEN, multiple endocrine neoplasia; nd, no data; NF, neurofibromatosis; SDHD, succinate dehydrogenase subunit D; SP, sporadic pheochromocytoma; VHL, non-Hippel-Lindau disease. 747
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Table 2 ‘‘Noncomplete’’ unilateral adrenalectomy for adrenal neoplasias studies with more than 5 patient Author
Patients Year (n) Diagnosis
Surgical approach
Bao [25] Nakada [51] Walz [1]
1987 6 1995 26 1998 20
open 0 open 0 retroperitoneoscopic 0
nd 60 11
Imai [57] Pautler [26] Kok [54] Ikeda [58] Sasagawa [13]
1999 5 2002 11 2002 8 2003 9 2003 47
laparoscopic laparoscopic laparoscopic laparoscopic retroperitoneoscopic
0 0 0 0 0
3 0.45 nd 20–27 nd
Jeschke [4] Meria [50]
2003 13 2003 20
laproscopic laproscopic
0 0
39 nd
Pheo Conn Conn, Cushing, Pheo NF Conn, NF Pheo Conn Conn, Pheo Conn, Cushing, Pheo, NF Conn Conn
Recurrence Follow-up (n) (months)
Abbreviations: nd, no data; NF, non-functioning adrenal tumor; Pheo, pheochromocytoma.
a recurrent tumor diagnosed today have undergone an open approach transabdominally or posteriorly during their first operation, an endoscopic technique in the opposite route (laparoscopic or retroperitoneoscopic) should be taken into consideration; the adrenal gland can thereby be reached with few scars. Compared with open surgery, experiences with endoscopic reoperations in recurrent pheochromocytomas are still limited, but feasibility and safety have been demonstrated [46].
Noncomplete adrenalectomy in Conn’s adenomas and Cushing’s adenomas Conn’s adenomas seem to be an ideal indication for a partial adrenalectomy, due to different reasons. First, these tumors are almost always benign; second, they are small; and third, they often lie eccentrically. These conditions facilitate a partial adrenalectomy, but neoplastic and normal tissue has to be differentiated exactly (Fig. 2). Total adrenalectomy in Conn’s syndrome results in biochemical cure in almost all cases [49–53], as the data of partial adrenalectomy also demonstrate [1,4,17,50,51,54,55]. Surgeons using partial adrenalectomy in Conn’s syndrome argue that the removal of the tumor cures the patient if he or she has a single adenoma. In case of erroneous excision of a single nodule in multinodular hyperplasia, the patient is not cured, even by complete adrenalectomy, because the disease is always bilateral [1]. Persistent hyperaldosteronism following noncomplete adrenalectomy has been reported once [56]. In this case, two clearly visible tumors were located in one adrenal gland by computed tomography. In the initial operation, the nonfunctioning lesion was removed and the active nodule left in place. Intraoperatively, ultrasonography
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Fig. 2. Intraoperative ultrasonography. The adrenal tumor (Conn’s adenoma) can clearly be differentiated from the normal adrenal tissue.
was not used to localize the tumors. Cure has been achieved by a second open procedure. Compared with Conn’s syndrome, the experiences of partial adrenalectomy in patients with Cushing’s syndrome are very limited [1,5] Our earlier description of subtotal adrenalectomy in 22 patients with adrenal neoplasias included 4 patients with Cushing’s adenomas. These tumors had a size of 2 cm to 3 cm in diameter, and therefore no risk for malignancy [1]. Recurrent disease has not occurred after a mean follow up of 6.5 years.
Technical aspects of noncomplete adrenalectomy As shown by clinical experience and endocrinological tests, preservation of the cortical function can be achieved by one third of one adrenal gland [6]. In reverse, if this amount of adrenal tissue cannot be preserved, complete adrenalectomy has to be recommended, especially in inherited pheochromocytomas, to minimize the risk of recurrence. It is not known whether smaller bilateral remnants allow a preservation of the cortical function. Dissection of the adrenal tissue can be performed safely with electrocauter, harmonic scalpel, and clip application or vascular stapler [1,5,40,57,58]. The disadvantages of stapling are a reduction of the remaining tissue and higher costs. We usually use a monopolar electrocauter without seeing bleeding, even when congestion has to be assumed following dissection of the vein [11]. Partial adrenalectomy is technically feasible and safe and does increase blood loss or operating time. Adrenal cortical function does not depend on patency of the main adrenal vein [6,11]. This seems to be essential, as pheochromocytomas are typically growing close to this vein, and the dissection of this vessel cannot be avoided in most of these cases (see Table 1). At that point, an exact knowledge of the anatomical variations of the main
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adrenal vein is of great importance. Whereas adrenal veins on the left side uniquely join the renal vein close to the upper pole of the kidney, adrenal veins on the right side have variations in about 10% of patients. Double veins and conjunctions with posterior hepatic veins have to be taken into account [12]. If a noncomplete adrenalectomy is planed, intraoperative (laparoscopic) ultrasound is useful and sometimes essential [26,59]. A clear identification of the border of normal and neoplastic tissue is possible, as the probe is directly positioned on the region of interest (see Fig. 2). Additionally, it allows verification or exclusion of further tumors in the same gland [58]. This is essential in multinodular cases and inherited pheochromocytomas.
Summary The standard operation on adrenal neoplasias is a complete adrenalectomy. Accepted exceptions are bilateral inherited pheochromocytomas. In these cases, clinical and biochemical cure, as well as preservation of cortical function, can be achieved by a noncomplete adrenalectomy. In that procedure, at least one third of one gland has to be preserved. In unilateral adrenal tumors, partial resection has been used, especially in Conn’s adenomas, with early results comparable to those of total adrenalectomy. Because long-term results are still limited in hyperaldosteronism, final conclusions are not possible today.
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