Adrenocortical carcinomas (ACs) are uncommon malignancies that can have protean clinical manifestations. A majority of cases are metastatic at the time of diagnosis, with the most common sites of spread being the local periadrenal tissue, lymph nodes, lungs, liver, and bone. AC is relatively rare, however, accounting for just 0.02-0.2% of all cancer-related deaths. Detection of tumors at an early clinical stage is crucial for curative resection. See the image below.
View Image | A 68-year-old woman with a large right upper quadrant primary adrenocortical carcinoma with curvilinear calcification. Low-attenuation regions anterio.... |
Physical examination findings in patients with hormonally active AC include the following:
Patients with nonfunctional AC typically present with any of the following:
See Clinical Presentation for more detail.
Laboratory studies
These include the following:
Imaging studies
Adrenal computed tomography (CT) scanning and magnetic resonance imaging (MRI) are the imaging studies of choice in AC. The typical case is characterized by a large unilateral adrenal mass with irregular edges. The presence of contiguous adenopathy serves as corroborating evidence.
Histologic examination
Some of the macroscopic features of an AC that suggest malignancy include a weight of more than 500 g, the presence of areas of calcification or necrosis, and a grossly lobulated appearance. Histologic findings also include numerous mitoses, scant cytoplasm, and none of the rosettes observed in neuroblastoma.
See Workup for more detail.
When feasible, total resection remains the management modality of choice for the definitive treatment of AC. It also remains the only potentially curative therapeutic modality. While open laparotomy for adrenalectomy represents the standard of care, several reports suggest a role for laparoscopic resection if the adrenal tumor is small and there is no preoperative evidence of metastatic disease.
Medical care in patients with AC, which can be supportive or adjuvant to surgical resection, encompasses the following:
See Treatment and Medication for more detail.
Adrenocortical carcinomas (ACs) are uncommon malignancies that can have protean clinical manifestations. A majority of cases are metastatic at the time of diagnosis, with the most common sites of spread being the local periadrenal tissue, lymph nodes, lungs, liver, and bone. ACs are virtually always unilateral, although one report suggests that 2-10% of cases may be bilateral at initial diagnosis; however, this finding has not been replicated (see the image below). (See Etiology, Pathophysiology, and Workup.)
View Image | A 68-year-old woman with a large right upper quadrant primary adrenocortical carcinoma with curvilinear calcification. Low-attenuation regions anterio.... |
Adrenocortical masses are common; autopsy studies show that approximately 5-15% of the general adult population may have adrenal incidentalomas, biochemically and clinically asymptomatic adrenal masses found incidentally during unrelated imaging investigations, such as abdominal computed tomography (CT) scanning or magnetic resonance imaging (MRI). Findings from abdominal CT scans suggest that the prevalence is lower, just 1-5%. Ectopic adrenocortical tumors are exceedingly rare. (See Epidemiology and Workup.)
Only a small number of adrenal tumors are functional, and an even smaller number (approximately 1 per 1500) are malignant. The evaluation of adrenal incidentalomas, therefore, focuses on (1) identifying functional masses and treating them appropriately (including surgical removal); (2) identifying adrenal carcinomas early, with the intent of attempting complete surgical extirpation; and (3) reassuring patients whose masses are neither functional nor malignant and arranging for follow-up examinations. (See Presentation, Workup, Treatment, and Medication.)
Adrenocortical carcinomas
These include the following:
Metastatic adrenal tumors
The most common potential primaries include the following:
Adrenomedullary tumors
These include the following:
Stromal malignancies
These include the following:
Adrenal malignancies in the setting of familial predisposing syndromes
The associated syndromes include the following:
Other
These include primary adrenal lymphomas, which can be unilateral or bilateral. Adrenal malignancies can also be classified as composite tumors and mixed tumors.
Adrenal tumors are classified in several ways. One popular method, which has great clinical relevance, is to subclassify them as functional or nonfunctional, depending on the elaboration of adrenocortical hormones (glucocorticoids, mineralocorticoids, androgens, estrogens; rarely, a host of possible peptides).
Nonfunctional variants of AC were previously reported to be far less common than the functional types; older reports suggested that approximately 50-80% of ACs are functional (patients present mainly with Cushing syndrome). Subsequent reports, however, have suggested that nonfunctional ACs may be more common than previously thought.
Another classification method is to subdivide ACs into sporadic and syndromic variants. The syndromic variants occur with multiple cancer predisposition syndromes, including Gardner syndrome, Beckwith-Wiedemann syndrome (associated with hemihypertrophy), multiple endocrine neoplasia type 1, the SBLA syndrome (sarcoma, breast, lung, and adrenal carcinoma and other tumors within several kindreds, which have not been clearly associated with localization to a single gene), and Li-Fraumeni syndrome.
Adrenal tumors can also be classified based on their cellular origin. Included here are primary ACs, primary adrenal lymphomas, soft-tissue sarcomas of the adrenal, malignant pheochromocytomas, and secondary metastatic adrenal tumors (the common primaries of which are tumors of the breast, kidney, lung, and ovary, as well as melanoma, leukemia, and lymphoma). Only the ACs typically are included in discussions of adrenal cancers, and this monograph will be restricted to those. (See Pathophysiology and Etiology.)
Authorities also report rare composite adrenal tumors, which are different histologic variants of the same embryologic origin (eg, coexisting neuroblastoma and malignant pheochromocytoma), and mixed adrenal tumors (typically, mixtures of pheochromocytomas, spindle cell sarcomas, and adrenocortical carcinomas).
Endocrine syndromes associated with AC include the following:
The exact etiopathogenesis of sporadic AC is unclear, but analysis of syndromic variants of the condition gives some insight. The role of tumor suppressor gene mutations is suggested by their association with Li-Fraumeni syndrome, which is characterized by inactivating germline mutations of the TP53 gene (a vital tumor suppressor gene, or antioncogene) on chromosome 17. This syndrome also is associated with a predisposition to other malignancies, including breast carcinoma, leukemias, osteosarcomas, and soft-tissue sarcomas.
A few reports describe an association between AC and familial adenomatous polyposis, which also is due to an inactivating germline mutation of a tumor suppressor gene (in this case, the adenomatous polyposis coli gene, APC). However, such mutations have not been found in sporadic APC cases.
Suggestions have been made that adrenal hyperplasia predisposes patients to develop AC. A few cases of congenital adrenal hyperplasia are associated with functional adrenocortical adenomas but not carcinoma. A few cases of AC are also associated with primary hyperaldosteronism, in which the adrenal tissue has portions showing adrenocortical hyperplasia. However, definitive proof of a sequence in which hyperplasia leads to adenoma, which then leads to carcinoma—similar to a sequence that produces colonic neoplasms—is lacking.
The association of AC with the Carney triad (GI stromal tumor, pulmonary chondromas, extra-adrenal paraganglioma) is far less defined. Since the Carney triad is so rare, there are very few reported cases.
Potential mechanisms for adrenocortical tumorigenesis include the following:
Among the putative pathogenetic mechanisms that may function in concert with each other are alterations in intercellular communication, paracrine and autocrine effects of various growth factors, cytokines elaborated by the tumor cells, and promiscuous expression of various ligand receptors on cell membranes (causing the cells to be in a state of perpetual hyperstimulation). This is presumed to lead to clonal adrenal cellular hyperplasia, autonomous proliferation, tumor formation, and hormone elaboration.
Some molecular studies of adrenocortical tumor cells show in situ mutations of the TP53 and TP57 genes (both antioncogenes) and increased production of insulinlike growth factor 2 (IGF-2). TP53 gene mutations are the most common mutant genes in human cancer. A potential role for this gene in sporadic AC is suggested by the frequent finding of loss of heterozygosity at the 17p13 locus in cases of sporadic AC. Definite germ cell mutations of the TP53 gene have also been demonstrated in more than 90% of children with AC from southern Brazil, which has the highest prevalence of sporadic AC in the world. Amplification of steroidogenic factor-1 expression has also been described in this population.
Another genetic locus of interest is the 11p chromosomal region that may also harbor a tumor suppressor gene and has been implicated in linkage studies in subjects with the Beckwith-Wiedemann syndrome. Loss of heterozygosity at band 11p15 and overexpression of IGF-2, whose gene is carried on this genetic locus, have been described in cases of sporadic AC.
Other studies demonstrate that some of AC cells express menin (the aberrant gene product in patients with multiple endocrine neoplasia type I [MEN1]); in other cases, the hybrid gene is associated with glucocorticoid-responsive aldosteronism (GRA).
Several reports suggest that, while benign adrenal tumors retain expression of the type 2 MHC antigens, these are lost in adrenocortical carcinoma cells. Furthermore, while adrenal adenomas can be monoclonal (43%), polyclonal (28%), or mixed (28%), virtually all ACs are monoclonal.
The fact that the normal adrenal cortex has multiple areas of adrenomedullary cells (often forming large cell nests) and that adrenocortical cells also are scattered in the adrenal medulla suggests a close interaction between the two groups of cells, despite their distinct phylogenetic and embryonic origins. The relevance of the paracrine interactions of these cells in the etiopathogenesis of AC and adrenal tumors as a whole is still being actively investigated.
AC tumors are uncommon, having an incidence of approximately 0.6-1.67 cases per million persons per year. In southern Brazil, however, the incidence of adrenal tumors is 10-15 times that of the general population, a difference that has been associated with a mutation in the P53 gene.
The female-to-male ratio for ACs is approximately 2.5-3:1. The accumulation of data, especially in international registries, revealed the incidence of adrenal tumors to be higher in female individuals than had previously been thought, particularly in those aged 0-3 years and those over 13 years. Nonfunctional ACs are distributed equally between the sexes.
AC occurs in 2 major peaks: in the first decade of life and again in the fourth to fifth decades. While, functional tumors are more common in children, however, nonfunctional tumors are more common in adults.
Based on data from the International Pediatric Adrenocortical Tumor Registry, the median age at which children develop adrenal carcinomas is 3.2 years; 60% are younger than four years, and 14% are older than 13 years.[1]
AC is relatively rare, accounting for just 0.02-0.2% of all cancer-related deaths. The most important predictive clinical parameters of prognosis are as follows:
Follow-up data from large centers, such as the MD Anderson Cancer Center and the Memorial Sloan-Kettering Cancer Center, suggest a temporal improvement in clinical survival of patients with AC since the late 1980s and early 1990s.
Male patients tend to be older and have a worse overall prognosis than do female patients. Female patients are more likely than male patients to have an associated endocrine syndrome. Although still somewhat controversial, some suggest that children with AC have a better prognosis than do adults; favorable clinical outcome has been reported in 70% or more of pediatric cases.[2]
Detection of tumors at an early clinical stage is crucial for curative resection; total resection offers the only prospect for cure. The estimated overall five-year survival rate for patients with AC is approximately 20-35%. For cases in which total surgical resection is achieved, this rate is estimated to be approximately 32-47%, while in cases in which total surgical extirpation has not been possible, the five-year survival rate is estimated to be 10-30%.[3]
Even after apparently complete surgical resection, however, local or distant relapse occurs in nearly 80% of cases. Documented cases exist of AC recurrence more than 10 years after presumed curative surgery. Recurrent or relapsing AC is usually a bad omen. Although symptoms of hormonal excess can often be medically managed in this setting, cure is virtually unknown.
The presence of distant metastasis generally is another sign of an especially poor outcome. Estimates suggest that as many as 50% of such patients are dead within 12 months of detecting metastatic deposits, regardless of treatment. Indeed, patients with functional AC may have a better prognosis because they present earlier, unlike patients with nonfunctional variants, who invariably present when the tumors are very large or are associated with distant metastasis.
Estrogen receptor (ER)–negative status also confers a worse prognosis in AC. In a study of 17 patients, Shen et al found that one- and five-year survival rates were 86% and 60%, respectively, for patients with ER-positive tumors, versus 38% and 0% for those with ER-negative tumors.[4]
The prognosis for cases of AC occurring in pregnancy is also grim; however, the fetal prognosis in these cases remains excellent.
Patients who show no response to mitotane or who relapse are probably best served by referral to a major cancer center, where they can be enrolled in one of several ongoing combination chemotherapeutic/radiation and/or surgical resection protocols. AC is too uncommon for most tertiary hospitals to have enough expertise to manage these patients adequately.
In 2016, Kim and colleagues published nomograms to predict recurrence-free survival (RFS) and overall survival (OS) after curative resection of adrenocortical carcinoma (ACC). The nomograms were created using a multi-institutional cohort of 148 patients who underwent curative-intent surgery for ACC at 13 major US institutions.[5]
The prediction model for RFS is based on the following 5 independent prognostic factors[5] :
The nomogram to predict OS is based on the following 3 independent prognostic factors[5] :
Higher total points based on the sum of the assigned number of points for each factor in the nomograms were associated with a worse prognosis.[5]
Potential complications associated with AC can be subclassified as follows:
While AC accounts for only approximately 5-10% of cases of Cushing syndrome, approximately 40% of patients with both Cushing syndrome and an adrenal mass also have a malignant tumor. Virtually all feminizing adrenal tumors in men are malignant.
Unfortunately, most patients with adrenocortical carcinoma (AC) present with advanced disease that is characterized by multiple abdominal or extra-abdominal metastatic masses (stage IV disease); therefore, distinguishing potential AC from adrenal incidentalomas is crucial (and controversial).
These hormonally silent tumors account for approximately 40% of patients with AC. Nonfunctional variants of AC tend to be more common in older patients and appear to progress more rapidly than functional tumors do. Although in some cases, they are found incidentally, during either examination or radiologic imaging, nonfunctional ACs typically present with any of the following:
The hormonally active variants of AC constitute approximately 60% of cases. Approximately 30-40% of adult patients with these present with the typical features of Cushing syndrome, while 20-30% present with virilization syndromes.
More than 80% present of pediatric patients, however, present with virilization syndromes. Isolated Cushing syndrome is much less common, occurring in approximately 6% of pediatric cases. Virilization (in girls) or precocious puberty (in boys) is the most common endocrine presentation of a functional AC.
Hirsutism, facial acne, oligo/amenorrhea, and increased libido all are possible presenting symptoms. Feminization as a presentation of AC is quite rare. Other modes of presentation include profound weakness, hypertension, and/or ileus from hypokalemia related to hyperaldosteronism and hypoglycemia.
Physical findings almost always include a palpable mass in the abdomen; the mass is hard and nonmovable.[6]
Findings in males include premature puberty with enlargement of the penis and scrotum, pubic hair, acne, and deepening voice.
Findings in females include premature appearance of pubic and axillary hair, clitoral hypertrophy, acne, deepening voice, premature increase in growth velocity, lack of appropriate breast development, and lack of menarche.
Signs of Cushing syndrome include a round face, a double chin, buffalo-hump fat distribution, generalized obesity, failure of growth velocity, and hypertension.[7]
In rare cases, feminization may occur. Findings in male patients include gynecomastia and hypertension; findings in female patients include precocious sexual development and hypertension.
A full evaluation is advised in all patients with a distinct adrenal nodule or tumor larger than 1 cm in order to determine whether the tumor is functional. The general agreement is that all functional masses should be removed.
Laboratory results may also help in distinguishing between a neoplasm of the adrenal cortex and a neuroblastoma. Adrenocortical tumors should not be confused with adrenal medullary tumors, also known as pheochromocytomas, which, similar to neuroblastomas, secrete catecholamines.
In a comparison of imaging findings in pediatric patients with adrenocortical carcinoma (AC), carcinoma was highly suspected when adrenal lesions had a thin tumoral capsule, a stellate zone of central necrosis, and evidence of the production of adrenocortical hormone.
The following are the major imaging features that serve as red flags for a possible AC on adrenal imaging:
While some reports suggest an increased predilection for the left adrenal in AC, most studies indicate no side preference.
Laboratory studies for AC include determinations of the following:
Include screening tests that can exclude excess hormone production when evaluating all primary adrenal masses.
The best screening tests for Cushing syndrome are the standard 1-mg dexamethasone suppression test and the 24-hour urinary cortisol excretion test. The recognition of the relatively high prevalence of subclinical Cushing syndrome in adrenal incidentalomas (some reports suggest a prevalence as high as 5-8%) that may otherwise appear hormonally silent informs the policy of some experts to perform more in-depth testing of the hypothalamic-pituitary-adrenal axis in patients with identified adrenal masses. Such testing would include the screening tests mentioned, as well as diurnal rhythm evaluation with 8 am and midnight serum or salivary cortisol estimations, corticotropin-releasing hormone (CRH) stimulation test, serum adrenocorticotropic hormone (ACTH) estimations (generally found to be low), and serum dehydroepiandrosterone (DHEAS) levels (also generally found to be suppressed). Alternatively, 24-hour urinary cortisol and its metabolites can be measured.
The evaluation of adrenal masses must also include screening for possible pheochromocytoma, including, at a minimum, a 24-hour urinary estimation of catecholamines (epinephrine, norepinephrine, dopamine) and metabolites (particularly metanephrines and normetanephrines). In addition, plasma metanephrines and catecholamines can be assayed.
Evaluation of adrenal masses also includes screens for the following:
Adrenal CT scanning and MRI are the imaging studies of choice in AC. The typical case is characterized by a large unilateral adrenal mass with irregular edges. The presence of contiguous adenopathy serves as corroborating evidence. (See the image below.)
View Image | A 68-year-old woman with a large right upper quadrant primary adrenocortical carcinoma with curvilinear calcification. Low-attenuation regions anterio.... |
The National Italian Study Group review of adrenal incidentalomas demonstrated that 90% of AC cases had diameters of 4 cm or larger on radiologic imaging. This study, based on a cohort of 887 patients, showed that using the 4 cm cutoff resulted in 90% sensitivity but poor specificity.[8]
Targeted CT scans of the adrenal using 3- to 5-mm sections offer the best resolution and are particularly useful in detecting tumors that are 1 cm or smaller.
Intravenous contrast generally is not necessary for localization of adrenal masses but is useful for demonstrating vascularity and clarifying sites of metastases. Some reports have also shown that in comparison with ACs, adrenal adenomas have a much earlier washout of contrast enhancement and that this may be of diagnostic utility. The contrast washout at 5 minutes postinjection is approximately 50% in adenomas, versus 8% in nonadenomas; at 15 minutes, the contrast washout is approximately 70% versus 20%, respectively.
Accumulating evidence suggests that low attenuation values on unenhanced CT scans can distinguish benign adrenal adenomas from AC or metastatic adrenal deposits that have attenuation values generally greater than 20 Hounsfield units (HU). Authorities suggest that adenomas have HU values of 10 or less. (However, many caveats significantly limit the clinical utility of this.)
Authorities also suggest using norms for HU values in intravenous contrast studies to assist in distinguishing adrenal adenomas from AC. A study by Hamrahian et al found that the sensitivity and specificity for the 10- and 20-HU cutoffs in distinguishing adenomas from nonadenomas, including AC and pheochromocytoma, were 40.5% and 100% for adenomas and 58.2% and 96.9% for nonadenomas.[9] These numbers suggest that, while limited as a screening instrument, the HU score has considerable utility in making definitive diagnoses when the scores are either less than 10 HU or greater than 20 HU.
MRI, in particular, shows significant utility in distinguishing AC from nonfunctional adenomas and pheochromocytomas. The malignant lesions tend to be of intermediate to high density on T2 imaging, while the nonfunctional adenomas are low intensity, and pheochromocytomas have a very high signal intensity. On gadolinium–diethylenetriamine penta-acetic acid (DTPA) contrast-enhanced MRI scans, adenomas generally demonstrate mild enhancement with rapid contrast washout, while ACs show rapid and intense enhancement with sluggish washout. The relatively higher fat content of adrenal adenomas compared with ACs has been used in the new chemical shift imaging (CSI) MRI protocols to further enhance the distinguishing capacity of these studies.
Chest CT scanning should be performed when metastatic disease is present. Affected lung parenchyma strongly suggests an AC over a neuroblastoma.
Ultrasonography has less sensitivity in detecting adrenal tumors and is highly user-dependent with regard to the interpretation and quality of results. It has particular utility, however, in the follow-up of previously detected incidentalomas. Abdominal and retroperitoneal ultrasonography is usually followed with abdominal CT scanning and MRI.
Bone scanning should be performed to detect metastatic disease. However, the presence of bone disease does not allow for the differential diagnosis of malignancies.
Iodocholesterol scans rarely are indicated in suspected cases of AC; the findings generally are negative in this setting, unlike in steroid-secreting adrenal adenomas.
Arteriography and venography currently have very little, if any, place in the diagnostic evaluation of adrenal masses suspected to be AC.
Because the histologic analysis of these masses may be unreliable, and owing to the potential for tumor seeding into the retroperitoneum, fine-needle aspiration and core tissue biopsies (percutaneous route) generally are not recommended.[10] Presently, the only setting where these biopsies are justified is in the evaluation of patients with a known malignancy, in order to exclude adrenal metastases.[11] The biopsies may be CT- or ultrasonographically guided.
Fine-needle aspirations should not be performed on any adrenal mass until pheochromocytoma has been definitively excluded; otherwise, the procedure may precipitate a potentially fatal crisis.
A specific histologic diagnosis of AC may be difficult in a case that is lacking clinical evidence of metastasis. Some of the macroscopic features of an AC that suggest malignancy include a weight of more than 500 g, the presence of areas of calcification or necrosis, and a grossly lobulated appearance. Histologic findings also include numerous mitoses, scant cytoplasm, and none of the rosettes observed in neuroblastoma.
In the Weiss system, which is considered the standard for determining malignancy in adrenocortical tumors, tumors are scored from zero to nine, with a higher score indicating increased malignancy.[12] As an adjunct to the Weiss score, Soon et al studied the use of microarray gene expression profiling to discriminate between adrenocortical adenomas and carcinomas; they found that the combination of insulinlike growth factor–2 (IGF-2) and Ki-67 overexpression identified ACs with 96% sensitivity and 100% specificity.[13]
These typically have a yellowish brown appearance on the cut surface. Pathologic features suggestive of malignancy are the large size of the primary tumor (tumor weights >100 g suggest malignancy), high mitotic rate, atypical mitoses, high nuclear grade, large areas of necrosis, low percentage of clear cells, diffuse cellular architecture, and evidence of capsular, lymphatic, or vascular invasion.[14]
Tumors may have broad fibrous bands separating them into nodules, and they often have a variegated appearance, a zona glomerulosa–like appearance, or a fascicular and reticulated appearance. Still, other areas may show near-total dedifferentiation.
Most of the cells are lipid-poor compared with typical adrenocortical cells, and they have an eosinophilic cytoplasm. Bizarre-looking, pleomorphic cells and multinucleate giant cells also may be evident. Predicting the hormonal products of a particular tumor based on histologic appearance is impossible.
These two types of tumors have distinctive histologic appearances and immunohistochemical staining patterns. While adrenomedullary tumors stain positive for neuroendocrine markers (eg, synaptophysin, neuron-specific enolase, chromogranin A), adrenocortical cells stain positive for D11, with very little overlap.
The various AC staging criteria, as delineated by the Union for International Cancer Control (UICC),[15] are outlined below.
These are as follows:
These are as follows:
These are as follows:
Staging for AC, below, follows the stage I-IV pattern for most solid tumors:
Fassnacht et al have argued that the UICC’s staging criteria have limited prognostic value. After reviewing 492 patients in the German AC registry who were diagnosed between 1986 and 2007, these researchers proposed that the prognostic value would be improved if stage 3 disease were defined by the presence of positive lymph nodes, infiltration of surrounding tissue, or venous tumor thrombus, and if stage 4 were restricted to patients with distant metastasis.[16]
Because adrenocortical carcinomas (ACs) are so rare, clinical series are small and there has been only limited prospective evaluation of treatment strategies. Therefore, significant controversy over therapy exists, and very few, if any, universally accepted treatment standards have been determined. Current practices are strongly influenced by expert consensus opinion from a few medical centers that specialize in ACs.
When feasible, total resection remains the management modality of choice for the definitive treatment of AC. It also remains the only potentially curative therapeutic modality.
Medical care in patients with AC, which can be supportive or adjuvant to surgical resection, encompasses the following:
Virtually all authorities agree that because of the significant potential cancer risk, all nonfunctional adrenal tumors of 6 cm or greater should be removed. Authorities also generally agree that nonfunctional adrenal tumors of 3 cm or less have a very low probability of being adrenal cancer; therefore, they can be observed safely.
The management strategy for adrenal masses larger than 3 cm and less than 6 cm is disputed. Some authorities suggest lowering the threshold for surgical removal of nonfunctional masses from 6 cm to 4-5 cm. Others individualize the follow-up of these patients depending on their clinical status, CT scan characteristics, and age. Particularly important is the fact that these criteria do not apply to children, who generally have smaller ACs.
A review of the available data suggests that the incidence rate of malignancy is small (< 0.03%) in all adrenal incidentalomas that are 1.5-6 cm. However, this rate increases considerably with tumors larger than 6 cm (up to 15%). The smallest identified AC associated with metastasis reported in the literature was 3 cm in diameter.
This drug remains the major chemotherapeutic option for the management of AC because it is a relatively specific adrenocortical cytotoxin. It is used as primary therapy, as adjuvant therapy, and as therapy in recurrent or relapsing disease.[17]
Mitotane apparently causes adrenal inhibition without cellular destruction. The exact mechanism of action is unknown. It inhibits cholesterol side-chain cleavage and 11-beta-oxyhydrase reactions. It also appears to reduce the peripheral metabolism of steroids. Alteration of extra-adrenal metabolism of cortisol reduces measurable 17-hydroxy corticosteroid while stimulating the formation of 6-beta-hydroxy cortisol. Plasma levels of corticosteroids do not fall.
This drug may be considered in the treatment of inoperable adrenal cortical carcinoma (functional, nonfunctional). It controls endocrine hypersecretion in 70-75% of patients. While objective tumor responses often are cited in as many as 20-25% of patients, a study has yet to be conducted with modern imaging techniques and response criteria accepted by clinical oncologists. Tumor response has been reported to correlate with serum levels and often requires several months of continuous therapy. Assaying mitotane levels during therapy is valuable because therapeutic efficacy depends on achieving serum levels of at least 15 mcg/mL.
Approximately 40% of the drug is absorbed, and approximately 10% of the dose is recovered in the urine as a water-soluble metabolite. Active metabolite excreted in the bile varies from 1-17%. The balance apparently is stored in tissues. Autopsy data indicate that fat tissue is the primary storage site, but the active metabolite is found in most tissues. After therapy, plasma terminal half-life varies from 18-159 days.
Experience suggests that the best approach is continuous treatment with the maximum possible dosage. If the dose is tolerated and an improved clinical response appears possible, increase the dose until adverse reactions interfere. The aim is to achieve doses as high as 10-20 g/day.
Efficacy
Mitotane’s major beneficial effect is on symptoms; treatment benefits are generally short-lived, and long-term survivors on this therapy are rare.
El Ghorayeb et al.reported a rapid and complete remission of metastatic ACC with mitotane monotherapy 2 years after a right adrenalectomy for stage III nonsecreting ACC. The patient remained disease-free with good quality of life on low maintenance dose of mitotane during the following 10 years.[18]
The potential benefit of postoperative adjuvant therapy with mitotane is still controversial. A retrospective study by Terzolo et al examining adjuvant mitotane therapy in patients who underwent radical surgery for AC, found evidence that mitotane can significantly increase recurrence-free survival. The study included 47 Italian patients who received mitotane postoperatively and control groups of 55 Italian patients and 75 German patients.
In the Italian patients, baseline features were similar in the treatment and control groups; the German patients were significantly older and had more stage I or II disease than did patients in the mitotane group. Median recurrence-free survival was 42 months in the mitotane group, as compared with 10 months in the Italian control group and 25 months in the German control group. Multivariate analysis indicated that mitotane treatment had a significant advantage for recurrence-free survival.[19]
However, a retrospective study by Grubbs et al contradicted these results. In this study, which involved 28 patients with AC who underwent primary resection, the investigators found that, although the overwhelming majority of these patients did not receive adjuvant treatment with mitotane, the patients’ recurrence rate was 50%—indistinguishable from the 49% recurrence rate reported by Terzolo et al for patients who received adjuvant mitotane.[20]
A 13-institution study by the US Adrenocortical Carcinoma Group of 207 patients who underwent resection of adrenocortical carcinoma compared the outcomes of 88 patients who received adjuvant treatment with mitotane to 119 patients who did not receive mitotane. There was no improvement noted in recurrence-free survival (RFS) or overall survival (OS) in those receiving mitotane.[21]
Some reports exist of the potential utility of streptozotocin in combination with mitotane (at a dose of 1 g qd for first 5 d, followed by 2 g q3-4wk thereafter). This regimen has been reported to be associated with a significantly better disease-free interval and with a greater number of long-term survivors.
Mitotane plus etoposide
The First International Randomized Trial in Locally Advanced and Metastatic Adrenocortical Carcinoma Treatment (FIRM-ACT) study group reported that first-line therapy patients who received mitotane and etoposide had higher response rates and longer median progression-free survival than patients treated with streptozocin plus mitotane (5 mo vs 2.1 mo, respectively). Toxicity rates for both of the combinations were similar. Overall survival in the entire group was not significantly better; however, the study revealed that for those patients who did not receive alternative second-line therapy, overall survival was better with mitotane plus etoposide.[22]
Although a few reports suggest the potential utility of suramin as an additional chemotherapeutic agent in the treatment of AC, this drug is not recommended for the disease.
Gossypol also has been tried for metastatic adrenal cancer, but experience and success have been limited. Derived from cottonseed oil, it was originally developed as a spermatotoxin. It has been used widely in China as a male contraceptive with few adverse effects. While the exact mechanism for its action is unclear, gossypol is known to cause selective mitochondrial destruction by the uncoupling of oxidative phosphorylation.
In cases where mitotane fails, chemotherapeutic regimens containing cisplatin alone or in combination often are used. (Cyclophosphamide, doxorubicin [Adriamycin], and cisplatin [CAP]; 5-fluorouracil, Adriamycin, and cisplatin [FAP]; and cisplatin with etoposide-16 have been tried.) Cisplatin also is often used in combination with ongoing mitotane administration.
Ronchi et al found that, as with other types of cancer, expression of excision repair cross-complementing group 1 (ERCC1) by ACs predicts resistance to platinum-based chemotherapy. Median overall survival after platinum treatment was 8 months in patients with high ERCC1 expression, versus 24 months in those with low ERCC1 expression.[23]
In the future, the treatment of adrenal carcinoma may utilize novel chemotherapeutic agents, vascular growth inhibitors, and small-molecule therapy based on a better understanding of the molecular pathways involved in tumorigenesis.
In functional tumors, management of the endocrine syndromes is often important because the associated systemic effects may significantly impact patient well-being.
Therapeutic options for Cushing syndrome include mitotane, ketoconazole, metyrapone, aminoglutethimide, RU 486 (mifepristone), and intravenous etomidate, alone or in various combinations.
For hyperaldosteronism, the major therapeutic options are spironolactone, eplerenone, amiloride, triamterene, and various antihypertensives, especially long-acting dihydropyridine calcium channel blockers.
For hyperandrogenism or hyperestrogenism, several options are available if adverse effects from androgen or estrogen significantly affect patient well-being. Antiestrogens may include the following:
Potential antiandrogens include the following:
Ketoconazole, spironolactone, and cimetidine also have a significant antiandrogen effect. The various aromatase inhibitors (eg, testolactone, anastrozole, letrozole, fadrozole) have some antiandrogen effect as well; therefore, they may be used. Controlled studies have not yet been performed to assess which of these agents, either alone or in combination, achieves the best metabolic control. The choice of medication often is guided by cost, availability, patient preference, adverse effects, and tolerance.
In the rare setting of mixed carcinoma associated with pheochromocytoma components, high-dose, radiolabeled metaiodobenzylguanidine (MIBG) has a potential role.
The management of blood pressure elevation in endocrine syndrome from adrenal cancer is similar to that in pheochromocytoma, with use of long-acting alpha blockers (usually phenoxybenzamine), followed by long-acting beta blockers (eg, propranolol) and, finally, metyrosine. There is no evidence suggesting that a combination of radiotherapy with mitotane (or any other chemotherapeutic regimen for that matter) confers any survival benefit.
Patients treated with mitotane may present with features of both glucocorticoid and aldosterone insufficiency requiring replacement therapy.
Some experts recommend that the use of radiation therapy be restricted to palliation of local disease, such as symptomatic metastases to the bone and local luminal obstructive disease.[24]
A meta-analysis by Polat et al suggested that radiotherapy to the tumor bed may be considered in patients at high risk for local recurrence. These researchers recommended administering a total dose of more than 40 gray (Gy), with single fractions of 1.8-2 Gy (including a boost volume to reach from 50-60 Gy in individual patients).[24]
Removal of all nonmetastatic adrenal masses larger than 6 cm is advisable (although several authorities have said 4 or 5 cm), regardless of the patient's hormonal profile. Include a full evaluation to determine the extent of disease and staging, which has implications for the ultimate prognosis.
The most common sites for metastases are the lungs, liver, bone, and lymph nodes. Contiguous spread to the kidney and liver (if the primary is on the right side) and tumor extension into the venous drainage system of the adrenals and the inferior vena cava are common.
Preoperative diagnostic accuracy should increase in the future with improved MRI technology, percutaneous core needle biopsy technology, and advances in molecular, genetic, and immunotyping interpretation.
When feasible, total resection remains the treatment of choice for the definitive management of AC. It also is still the only potentially curative therapeutic modality.
Open versus laparoscopic surgery
While open laparotomy for adrenalectomy represents the standard of care, several reports suggest a role for laparoscopic resection if the adrenal tumor is small and there is no evidence of metastatic disease preoperatively.[25, 26, 27]
A study by Agha et al suggested that laparoscopic adrenalectomy can be effectively performed even on larger tumors (>6 cm). Data from 279 patients who underwent the minimally invasive procedure (227 with tumors of 6 cm or smaller and 52 with tumors >6 cm) showed that although the mean duration of surgery, estimated blood loss, intraoperative bleeding rate, conversion rate, and postoperative complication rate were greater in the patients with larger tumors, the two tumor groups each had only one major complication.[28]
Recurrent and metastatic tumor management
Recurrent local and metastatic tumors are common in AC, even among patients who undergo a successful complete resection. In such settings, the only effective treatment is attempted reoperation.[29, 30] Case reports indicate that repeated thoracotomy can allow for more than 10 years of high-quality survival despite recurring crops of metastatic disease. Moreover, a large, retrospective series showed that pulmonary metastasectomy may be beneficial in carefully selected patients.[31] In the study, by Kemp et al, median overall survival was 40 months and five-year actuarial survival was 41%, following resection of pulmonary metastasis.
In a study at Memorial Sloan-Kettering Cancer center, investigators found that in patients with AC, aggressive primary surgical removal and aggressive surgical treatment of local or distant relapse led to long-term survival rates far superior to those reported in previous studies, regardless of the patients' ages. One important feature of this study was that patients who underwent a complete second resection had a median survival of 74 months (5-y survival rate, 57%).[32]
If lesions seem particularly sensitive to chemotherapy, with dramatic diminishment of tumoral masses in the chest or elsewhere, autologous stem-cell transplantation may be a consideration. However, only anecdotal data suggest that transplantation is helpful in managing AC. One study reported the use of a combination of adrenalectomy, chemotherapy, surgical debulking of lung metastases, and autologous transplantation; two years of continuous complete remission were reported.[33]
Percutaneous radiofrequency ablation may have a place in the control of local symptoms related to local compression by an invasive tumor.
Ambulatory follow-up should occur every month for the first two years after treatment because repeat resection of locally recurring disease and resection of metastatic lung disease can substantially affect long-term survival.
Scanning of the local area in the abdomen or pelvis and of sites of metastatic disease should continue every three months for the first two years, every four months for the next two years, and every six months during the fifth year.
Patients should be monitored for the reappearance of adrenocortical hormone hyperactivity, along with scanning, unless their history suggests that Cushing syndrome or autonomous adrenocortical hormonal production is present. If this is the case, the physician should immediately search for recurrence.
No definitive guidelines exist for all nonfunctional adrenal masses being followed serially. A suggested follow-up regimen is to perform repeat adrenal CT or MRI scans 3-6 months after the initial evaluation, then yearly (some suggest every 6 mo for the first few years) in order to detect any change in tumor size. Accompany these with periodic checks of hormonal profiles (after 1 y, then every 1-2 y thereafter).
Clinical practice guidelines for the management of adrenocortical carcinoma (ACC) in adults were released in October 2018 by the European Society of Endocrinology.[34]
Diagnosis
Perform a detailed hormonal workup of all patients with suspected ACC to identify potential autonomous excess of glucocorticoids, sex hormones, mineralocorticoids, and adrenocortical steroid hormone precursors.
Perform a chest CT in addition to an abdominal-pelvic cross-sectional imaging (CT or MRI) in any case where there is high suspicion for ACC.
Do not use adrenal biopsy in the diagnostic workup of patients with suspected ACC unless there is evidence of metastatic disease that precludes surgery.
Surgery
Complete en bloc resection of all adrenal tumors suspected to be ACC is recommended. Enucleation and partial adrenal resection is not recommended.
Open surgery for all tumors with radiological findings suspicious of malignancy and evidence for local invasion is recommended.
Routine loco-regional lymphadenectomy should be performed with adrenalectomy for highly suspected or proven ACC. At a minimum, it should include the periadrenal and renal hilum nodes. All suspicious or enlarged lymph nodes identified on preoperative imaging or intraoperatively should be removed.
Perioperative hydrocortisone replacement in all patients with hypercortisolism that undergo surgery for ACC is recommended.
Pathological work-up
Use immunohistochemistry for steroidogenic factor-1 (SF1) for the distinction of primary adrenocortical tumors and non-adrenocortical tumors.
Use the Weiss system for the distinction of benign and malignant adrenocortical tumors.
Use Ki67 immunohistochemistry for every resection specimen of an adrenocortical tumor.
Adjuvant therapy
Adjuvant therapy is not recommended for adrenal tumors with uncertain malignant potential.
Adjuvant mitotane treatment is recommended for those patients without macroscopic residual tumor after surgery who have a high risk of recurrence.
Administer adjuvant mitotane for at least 2 years, but not longer than 5 years, in patients without recurrence.
Treatment of Recurrent and/or Advanced ACC
For advanced ACC not amenable to complete surgical resection, local therapeutic measures (eg, radiation therapy, radiofrequency ablation, chemoembolization) are of particular value.
Routine use of adrenal surgery in case of widespread metastatic disease at the time of first diagnosis is not recommended.
In patients with advanced ACC at the time of diagnosis not qualifying for local treatment, either mitotane monotherapy or mitotane + EDP is recommended.
Surgery is recommended for patients with recurrent disease and a disease-free interval of at least 12 months.
Pregnancy and ACC
Prompt surgical resection is recommended when an adrenal mass suspected to be an ACC is diagnosed in a pregnant patient.
Patients should avoid pregnancy while on mitotane treatment.
Adjuvant or palliative treatment for adrenocortical carcinoma (AC) has been studied by using mitotane, cisplatin, etoposide, and doxorubicin. Mitotane leads to autodestruction of the adrenal cortex. Therefore, it is used in almost all protocols in the hope that it will decrease any autonomous hormone production and suppress tumor growth. Chemotherapy has focused on 3 antineoplastics—cisplatin, etoposide, and doxorubicin—given alone or in combination; studies have focused on the regimen etoposide and cisplatin and on etoposide, doxorubicin, and cisplatin.
Clinical Context: Mitotane is an option for the management of AC because it is a relatively specific adrenocortical cytotoxin. It decreases the production of cortisol by causing adrenal atrophy and affecting mitochondria in adrenocortical cells. No pediatric standards or dosages have been established; doses in children must be individualized.
Clinical Context: Cisplatin inhibits DNA synthesis and, therefore, cell proliferation, by causing DNA cross-linking and denaturation of the double helix.
Clinical Context: Doxorubicin, a cytotoxic anthracycline antibiotic isolated from cultures of Streptomyces peucetius var. caesius, is mutagenic and carcinogenic. It blocks DNA and RNA synthesis by inserting between adjacent base pairs and binding to the sugar-phosphate backbone of DNA, inhibiting DNA polymerase. The drug binds to nucleic acids presumably by specific intercalation of the anthracycline nucleus with the DNA double helix. It can also cause DNA strand breakage, because of its effects on topoisomerase II.
Doxorubicin is a powerful iron chelator; the iron-doxorubicin complex induces the production of free radicals that can destroy DNA and cancer cells.
Doxorubicin's maximum toxicity occurs during the S phase of cell cycle. The drug has a multiphasic disappearance curve, with half-lives of up to 30 hours. This agent does not cross blood-brain barrier but is taken up rapidly by the heart, lungs, liver, kidney, and spleen. The dosage is related to body surface area.
Antiproliferative drugs may be useful for palliating symptoms in patients with diffuse metastases. Liposomes in different drug products can vary in chemical and physical properties, which can substantially affect functional properties.
Clinical Context: Etoposide is a glycosidic derivative of podophyllotoxin that exerts a cytotoxic effect by stabilizing the normally transient covalent intermediates formed between the DNA substrate and topoisomerase II. The drug leads to single-stranded and double-stranded DNA breaks that arrest cellular proliferation in the late S or early G2 phase of cell cycle.
These agents inhibit cell growth and proliferation. Cancer chemotherapy is based on an understanding of tumor cell growth and how drugs affect it. After cells divide, they enter a period of growth (phase G1), followed by DNA synthesis (phase S). The next phase is a premitotic phase (phase G2). Finally, a period of mitotic cell division (phase M) occurs.
Rates of cell division vary for different tumors. Most common cancers grow slowly compared with normal tissues, and the rate may decrease if tumors are large. This difference allows healthy cells to recover from chemotherapy more quickly than do malignant cells, and this is the rationale for current cyclic dosage schedules.
In interfering with cell reproduction, some antineoplastic agents are specific to certain phases of the cell cycle, whereas others (eg, alkylating agents, anthracyclines, cisplatin) are not phase specific. Cellular apoptosis (ie, programmed cell death) is another potential mechanism of many antineoplastic agents.