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Original Studies |
Departments of Clinical and Experimental Medicine and Medical Sciences, Diagnostics and Special Therapeutics (M.C.-C., G.P.F.), University of Padova, 35126 Padova, Italy
Address all correspondence and requests for reprints to: G. P. Rossi, M.D., F.A.C.C., Clinica Medica 4, Hypertension Unit, University Hospital, via Giustiniani 2, 35126 Padova, Italy. E-mail: gprossi{at}ux1.unipd.it
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Abstract |
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 Top Abstract IntroductionSubjects and MethodsResultsDiscussionReferences |
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An aldosterone-producing adenoma (average diameter, 12.2 ± 0.08
mm) was eventually diagnosed in 41 patients (39.4%) and was excluded
in the rest. Adrenal vein rupture leading to partial adrenal loss
occurred in 1 patient (0.9% complication rate). By assuming a cut-off
value of Cside/CIVC 
1.1, AVS was
selective in 85.7% and 94.1% of cases on the right and left sides,
respectively, and bilaterally in 80.6% of cases. Of all AVS-derived
indexes, the A/C of one over the A/C contralateral side
[(A/C)side/(A/C)contralateral side] furnished
the best diagnostic accuracy. With a bilaterally selective AVS, a value
of (A/C)side/(A/C)contralateral side
2 provided a conclusive etiological diagnosis of PA in 79.7% of
cases. At variance, no accurate diagnosis could be made from
unilaterally selective AVS.
AVS was feasible and safe in most PA patients with inconclusive
computed tomography and magnetic resonance scans. When bilaterally
selective (i.e. Cside/CIVC
1.1) a ratio of (A/C)side/(A/C)control
2 provided the best compromise of sensitivity and false positive
rate for lateralization of the etiology of PA.
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Introduction |
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TopAbstractIntroductionSubjects and MethodsResultsDiscussionReferences |
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Adrenal vein catheterization was introduced 4 decades ago for identification of the etiology of PA to the ends of identifying the underlying adrenal pathology through retrograde phlebography (7, 8) and demonstrating unilateral overproduction of aldosterone (9, 10). Although widely used thereafter (1, 11, 12, 13, 14, 15, 16), the usefulness of adrenal vein catheterization has been challenged in recent years by the advent of tests with unprecedented accuracy for imaging adrenocortical diseases, such as computed tomography (CT) and magnetic resonance (MR) (12, 17). This led to the abandonment of adrenal phlebography, because of its low sensitivity coupled to a substantial risk of adrenal vein rupture (18), whereas adrenal vein blood sampling (AVS) was confined to cases with inconclusive CT and/or MR results to demonstrate a unilateral source of aldosterone excess (16).
A widespread use of CT and MR in patients with the biochemical features of PA, however, has highlighted that the majority of APA are smaller than 10–15 mm in diameter and therefore may escape identification at both imaging techniques (14, 17). In addition, primary aldosteronism entails a pathological continuum between a true solitary adenoma, on the one extreme, and pure bilateral micronodular hyperplasia, on the other, with intermediate degrees of unilateral or bilateral macronodular and micronodular hyperplasia (11). Accordingly, the differential diagnosis between a microscopic or small APA or unilateral autonomous adrenal hyperplasia, which can be cured with adrenalectomy, and bilateral nodular adrenal hyperplasia, which does not benefit from surgery, remains extremely challenging. This difficulty is clearly illustrated by the high proportion (16%) of unilateral adrenalectomy of hyperplastic (nonadenomatous) glands, which is performed even at referral centers (5). Dexamethasone-suppressed adrenocortical scintigraphy (19) with [75Se]Met or [125I]cholesterol analogs (20) can occasionally solve this clinical dilemma; however, this test is intrinsically insensitive for diagnosing small APA because tracer uptake is poor in APA less than 1.5 cm in diameter. Furthermore, it is expensive and not widely available (2, 21).
It is conceivable that AVS performed solely to demonstrate a unilateral overproduction of aldosterone, although being devoid of the adrenal phlebography-associated risk of vein rupture, might be valuable and safe in patients with equivocal CT and/or MR findings. However, its feasibility, accuracy, and safety have been investigated to date only in a limited series of patients (16). Furthermore, no information is available on several key issues concerning utilization of the data that AVS can furnish.
Thus, we investigated prospectively 1) the feasibility, sensitivity, specificity, and accuracy of AVS in a large series of consecutive PA patients who had inconclusive CT and MR scans; 2) the impact of different degrees of selectivity of AVS on its accuracy for identification of APA; and 3) the possibility of making an accurate diagnosis with indexes derived solely from unilaterally selective AVS.
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Subjects and Methods |
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TopAbstractIntroductionSubjects and MethodsResultsDiscussionReferences |
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A total of 104 Caucasians patients (45 women and 59 men, aged
49.6 ± 11.6 yr) referred to our institution from January 1990 to
December 1999 for evaluation of high blood pressure were investigated
as previously reported (22). In brief, they underwent
measurements of baseline and captopril-stimulated PRA and plasma
aldosterone. All individuals were receiving the normal diet of our
hospital that comprised 100–200 (range) mmol sodium and 50–75 mmol
potassium daily. Most were not taking any drug at the time of the
study; in 33 patients, in whom withdrawal of the antihypertensive
treatment was deemed to be unsafe, a calcium entry or an
1-adrenergic receptor blocker was allowed,
because this treatment did not significantly alter plasma aldosterone
or the cortisol secretion rate under the conditions of this study
(23, 24).
Adrenal CT was performed by administration of an iv bolus injection of 100 mL of a nonionic iodinated contrast agent (Iopamidolo, 37 g I/dL; Iopamiro 370, Bracco, Milan, Italy) followed by a continuous drip infusion as previously reported (17). Targeted analysis of the adrenal regions was performed with contiguous 3-mm-thick slices. For cases studied between 1990 and 1998 a third generation CT was used (Tomoscan LX III, Philips, Einthoven, The Netherlands). For the last 20 cases a spiral CT (Siemens Somatom Emotion, Erlangen, Germany) was used with collimation 3 mm thick, pitch of 1.2, and reconstruction interval of 2 mm. CT scans were examined blindly by two experienced radiologists (M.C.-C. and G.P.F.), and discordant interpretation was resolved by consensus. Measurements of urinary and plasma catecholamines and MR, or renal digital subtraction angiography and renal vein renin studies were carried out whenever required to rule out pheochromocytoma and renovascular hypertension, respectively. For the purposes of this study it was decided a priori in 1990 to consider as APA single nodes larger than 18 mm at CT in patients with the biochemical features of PA as assessed with the results of the captopril test and the saline infusion test. Accordingly, patients with smaller or undetectable nodes were enrolled and underwent AVS.
Diagnostic criteria
It was established beforehand that the etiological diagnosis of primary aldosteronism had to be based, for the purposes of this study, on results of the biochemical measurements, CT and/or MR, AVS, and, when clinically indicated, dexamethasone-suppressed adrenal scintigraphy, using previously reported criteria ( (20, 22). To minimize tautological biases in assessing the accuracy of AVS, the diagnosis of APA, however, had to be further confirmed at surgery, pathology, and by demonstration of normalization of serum potassium levels and a fall or normalization of blood pressure at follow-up after adrenalectomy.
Adrenal vein sampling
Catheterization of the right femoral vein with the Seldinger technique was performed in all patients between 0800 and 1130 h to avoid any bias due to the circadian rhythm of aldosterone (25). Furthermore, to avoid creating artificial gradients between sides to standing up stimulation, patients were kept supine from 3 h before throughout all the AVS procedure. We collected samples of adrenal venous and infrarenal inferior vena cava blood for measurement of plasma aldosterone (A) and cortisol (C). This was undertaken because CT scan (n = 104) and MR (n = 72) did not provide unequivocal identification of an APA. Informed written consent was obtained from each patient, and the protocol of the study was consistent with our institutional guidelines for human studies. All procedures were performed by the same interventional radiologists (M.C.-C. and G.P.F.) with an identical methodology. The position of the tip of the catheter before blood sampling was verified by manual injection of a small amount of contrast medium (Iopamidolo, 37 g I/dL; Iopamiro 370, Bracco). Given the well known difficulties of selective catheterization of the right adrenal vein, AVS was performed first on this side and then contralaterally. The time elapsing between selective catheterization of both adrenal veins of one side and the other was within 5 min in all cases. Blood was drained by gravity or by gentle negative pressure when necessary (10).
The selectivity of AVS on both sides was assessed with the ratio between cortisol levels in the right (CRAV) and left (CLAV) adrenal veins and the inferior vena cava (CIVC) plasma.
AVS results were evaluated by comparing between patients with right and left APA and subjects without APA the following indexes: (A/C)RAV, (A/C)LAV, ARAV/ALAV, (A/C)RAV/(A/C)IVC, (A/C)LAV/ (A/C)IVC, (A/C)RAV/(A/C)LAV, (A/C)RAV/(A/C)LAV, and (A/C)unaffected or lower side/(A/C)IVC (26), where A and C indicate plasma aldosterone and cortisol, respectively. RAV, LAV, and IVC suffix denote right adrenal vein, left adrenal vein, and infrarenal interior vena cava, respectively. The suffix "unaffected" or "lower side" identifies the side without evidence of APA and that with lower A/C value in patients with and without APA, respectively.
Sample collection and RIAs
Venous blood for PRA, aldosterone, and cortisol measurements was collected into prechilled tubes containing 200 µL Na2 ethylenediamine tetraacetate after the subjects had been lying quietly in the supine position for at least 3 h. Utmost care was taken to avoid any stress to the patients and to avoid any possible mismatch of the tubes. Samples were kept on ice and centrifuged within 30 min at 3000 x g at 4 C for 15 min. The supernatant was collected and frozen at -20 C until assayed. Assay was performed within 15 days in all cases.
PRA (supine normal values with a daily sodium intake of 100–200 mmol, 0.39–2.04 nmol angiotensin I/L·h), was measured as previously reported (27).
Plasma aldosterone (supine n.v., with a daily sodium intake of 100–200 mmol, 33.3–332.9 pmol/L) was measured by RIA using a commercially available kit (Ares Serono, Milan, Italy). The intra- and interassay coefficients of variation was 5.9% and 9.3%, respectively.
Plasma cortisol (supine normal values in the morning, 138–688 nmol/L) was measured by RIA using a commercially available kit (Ares Serono).
Statistical analysis
Results are expressed as the mean ± SD or SE, when appropriate. As plasma aldosterone and cortisol values did not follow a normal distribution, their natural logarithm was used for statistical comparison. Patients with and without APA were compared by unpaired t test. AVS-derived indexes were compared between patients without and with right or left APA by computing an ANOVA table, followed by Dunnett’s test for multiple comparison. The variables with P < 0.05 were considered statistically significant. Analyses were carried out with the SPSS for Windows statistical package (version 9.0, SPSS, Inc., Chicago, IL).
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Results |
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TopAbstractIntroductionSubjects and MethodsResultsDiscussionReferences |
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APA was diagnosed in 41 patients and idiopathic hyperaldosteronism
(IHA) in the rest. Three of these latter patients, who had CT evidence
of an adrenal node, but no evidence of unilateral aldosterone excess,
were judged to harbor incidentaloma. The clinical features of all of
the patients are shown in Table 1
.
Patients with APA had significantly higher systolic blood pressure and
serum aldosterone and significantly lower serum
K+ than patients with IHA. APA was more common on
the left (26 cases, 65%) than on the right (15 cases, 35%). The mean
size of the longest dimension of the tumor was 12.2 ± 0.08 mm
(95% confidence interval, 10.0–14.0 mm); there was no difference in
size between right and left APAs (12.4 ± 1.8 vs.
12.1 ± 0.09).
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AVS was attempted 105 times in a total of 104 patients, as it was
repeated twice (with identical results) in 1 patient. In 3 patients
catheterization of the right adrenal vein was unfeasible; adrenal vein
cortisol levels were not assessed in 3 additional patients. These 6
patients were therefore excluded from the analysis of the usefulness of
AVS-derived indexes and used only for the feasibility/safety
assessment. Overall, AVS was feasible in 97.1% of the 105 times when
it was undertaken. In the remaining 98 patients where all hormonal data
were available, using a cut-off value of
Cside/CIVC 1.1 (see
later) AVS was selective in 85.7% and 94.1% on the right and left
sides, respectively; it was bilaterally selective in 80.6% of cases.
Adrenal vein rupture occurred in 1 patient with IHA 2 days after
discharge following an uneventful AVS procedure. This was treated
conservatively and led to the partial functional loss of the
adrenocortical gland, as shown by serial scintigraphies after 6 and 15
months, without cure of hypertension.
The results of the aldosterone and cortisol data and the derived
indexes in the patients classified according to diagnosis are shown in
Table 2. Of the AVS-derived indexes, the
one providing the best discrimination between patients with and without
APA was the
(A/C)side/(A/C)contr., in
keeping with previous reports (16, 26) (Fig. 1). Instead, no satisfactory
discrimination of patients with and without APA was attained by
comparing the ratio of (A/C) of the unaffected side and of the inferior
vena cava (16).
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). With such
a cut-off value, overall 74.5% of the 98 patients who had all hormonal
data available were correctly identified; the proportion rose to 79.7%
if only bilaterally selective AVS (see below) were taken into
consideration.
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1.1, 1.25,
1.5, 1.75, and 2.0. This analysis showed that an accurate diagnosis
could be made starting from cut-off values of 1.1 or more, and that no
further improvement could be attained with higher cut-off values,
which, instead, resulted in the exclusion of an increasing proportion
of cases (Fig. 3).
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Discussion |
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TopAbstractIntroductionSubjects and MethodsResultsDiscussionReferences |
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This study is unique among available studies in several other aspects. First, it entails the largest series ever reported of consecutive primary aldosteronism patients prospectively studied with AVS. Second, AVS was performed solely to demonstrate unilateral aldosterone overproduction, given the low chance of success along with the high risk of adrenal vein rupture associated with forced retrograde flebography (18, 29, 30), in patients with inconclusive CT results. As such, our study provided an opportunity to address several key issues concerning AVS that are still unresolved, including the best way to assess its results as well as its feasibility and safety.
We found AVS to be feasible in approximately 97% of our patients. Of much interest, the complication rate was extremely low, with adrenal vein rupture occurring in one case (0.9%) and leading to partial adrenocortical loss. This rate is much lower than the 5% observed in earlier studies (10), possibly due to both avoidance of adrenal flebography and improved technique and catheter design.
Interpretation of AVS results has been difficult to date because of
hormonal values overlapping between patients with and without adenoma
(31). This might occasionally reflect the rare occurrence
of syndromes intermediate between unilateral adenoma and bilateral
hyperplasia (32) or other potential factors, including the
episodic secretion of aldosterone under ACTH control (33, 34), errors during the dilution of the samples before RIA and
variable venous anatomy (see for a review, see Ref. 35).
However, surprisingly, it remains unclear which AVS-derived
indexes provided the most accurate diagnosis and what cut-off value to
use. By using ROC curve analysis (28) we found that
(A/C)side/(A/C)contralateral
side provided the best discrimination between patients with
and without APA. At variance, we could not achieve a clear-cut
discrimination with other indexes, including the ratio of A/C in the
unaffected (or lower in IHA patients) side and the
(A/C)IVC, which was proposed by some researchers
(16, 26). Therefore, we next examined the effects of
different cut-off values of
(A/C)side/(A/C)contralateral
side on sensitivity and false positive rates and found that
a cut-off of 2.0 or greater provided the best compromise of sensitivity
and false positive rates. This cut-off allowed for a correct
classification of about 80% of all patients, provided that AVS was
bilaterally selective, i.e. with a
Cside/CIVC 1.1 (see
later). At variance with this finding most of the patients with APA and
primary unilateral adrenal hyperplasia reported by Young et
al. had a value greater than 4, whereas among patients with
surgically proven IHA the highest value was 3.5 (16).
Differences in patient selection, tumor size, biochemical assay, as
well as the fact that ACTH stimulation was routinely performed in that
study might account for these differences. Furthermore, as the majority
of the patients presumed to have IHA did not undergo surgery for
ethical reasons in most studies (16, 26), including ours,
it is obviously quite difficult to precisely assess the upper limit of
(A/C)side/(A/C)contralateral
side in IHA patients. Notwithstanding these limitations, it
has been commented that the use of more strict cut-off values would
deprive more patients with APA of curative surgery than would lead to
useless adrenalectomy in IHA patients (16, 26).
The diagnostic accuracy attained in this study (79.7%) might appear disappointing compared with that (95–100%) alleged in previous studies (12, 13, 14, 36). However, it must be appreciated that our patients were consecutive cases selected because of negative or inconclusive CT and MR scans and therefore entail the most challenging cohort from the diagnostic standpoint. Furthermore, in previous studies, which were of much smaller series of selected patients with larger tumors, no formal analysis was available. Thus, although not being readily comparable to available studies (16, 26), our results show that the diagnostic accuracy achieved in this study is much higher than that attainable with scintigraphy in patients with such small tumors (2).
Different criteria have been used to assess the selectivity of AVS. Although early studies did not pay much attention to this issue (9, 14, 29, 37), it became evident that because of the low blood flow to the adrenal cortex and the short length of the adrenal veins, artificial differences between sides could be created by a different degree of proximity of the catheter’s tip to the adrenals. Therefore, measurements of cortisol (9, 36) or epinephrine (38) levels were introduced to correct for different degrees of selectivity. Nonetheless, there is uncertainty what cut-off level of Cside/CIVC should be used, and even more recent studies did not take this issue into consideration (39). According to Blumenfeld et al. AVS was successful if Cside/CIVC > 2 (5), whereas Young et al. set a cut-off value of 5 (16), and Gordon et al. reported a minimum value of 2.7 in their series (40). However, to our knowledge, no systematic assessment of different cut-off values was available. By examining the impact of different degrees of selectivity, as assessed from the Cside/CIVC, on diagnostic accuracy, we found that the lower cut-off value of Cside/CIVC still providing an accurate diagnosis was 1.1. With such a cut-off value, AVS was bilaterally selective in 80.6% of all cases; 14.3% and 5.9% of failures occurred on the right and left sides, respectively. According to an early report (34), the failure rate for right adrenal catheterization was 10%, but the figure given in later reports was as high as 25–38% (2, 15, 41). It is unclear, however, how selectivity was assessed. By showing that a cut-off value lower than those previously suggested (5, 16, 40) can still provide an accurate diagnosis, our results can considerably increase the number of AVS results that are suitable for diagnostic calculations.
Catheterization of the adrenal vein fails more commonly on the right than on the left side for both anatomical and technical reasons, as confirmed by our present findings. It has therefore been proposed to perform the localization of APA with catheterization of only the left adrenal vein (10, 39). However, this contention was neither prospectively investigated nor convincingly validated. By analyzing AVS indexes derived solely from catheterization of either the left or the right adrenal vein and the infrarenal inferior vena cava, we obtained ROC curves that did not differ significantly from the identity lines, thereby indicating that the overall diagnostic accuracy attained with this approach is low. The fact that compared with previous reports (10, 39) we investigated a much larger series of patients with smaller tumors might account for these discrepancies. More importantly, our results do not support the feasibility of localizing adrenal tumors in CT-negative patients with hormonal data derived exclusively from left adrenal vein catheterization.
As the prevalence of nonfunctioning adrenal adenoma can be as high as 10% (42), the simple CT or MR detection of an adrenal mass in a patient with the biochemical features of primary aldosteronism does not necessarily imply an aldosterone-producing tumor. Furthermore, a larger nonfunctioning adenoma can concur with a smaller CT-negative contralateral APA (43). Thus, even in cases with unequivocal CT or MR demonstration of an adrenal mass, the indication to perform adrenalectomy in a patient with primary aldosteronism should rely upon demonstration of a lateralized aldosterone production. Accordingly, the present results showing the feasibility and safety of AVS can be relevant not only for patients with small tumors and inconclusive CT or MR findings.
Limitations
This study has some limitations, as do most previous studies on this issue (44). First, as the results of AVS were part of the work-up used to make the final diagnosis, there might be some tautology in our evaluation of AVS for diagnostic purposes (10, 26, 45). In other words, it could be that a few small APA were missed in the group of patients considered to have idiopathic hyperaldosteronism. However, this seems unlikely, as none of these patients developed APA at long-term follow-up. Second, we used cortisol and not epinephrine to assess the selectivity of AVS, whereas less overlap between adrenal vein and infrarenal inferior vena would be attained with the latter (38). Finally, it has been shown that both aldosterone and cortisol are secreted in a burst-like mode in both normal subjects and patients with APA (33, 46). Accordingly, it was proposed to perform AVS during ACTH stimulation to minimize potential problems due to episodic aldosterone secretion from APA (47). This stimulation was not performed in this study, because to provide accurate results it requires simultaneous bilateral AVS (34). There are, however, several reasons to believe that ACTH stimulation might not have given better results. First, both increased interbursts (basal) aldosterone release and significant cross-correlations between aldosterone and cortisol plasma levels throughout a 24-h observation period were shown to occur in APA patients (33, 46). Second, we used a normalization of aldosterone for cortisol levels. Third, all of our patients were studied in the morning, when ACTH, cortisol, and aldosterone secretion is high (48). All of these factors should have minimized potential problems due to burst-like aldosterone secretion. Nonetheless, we cannot conclusively rule out the possibility that a different diagnostic accuracy might be accomplished by performing bilateral catheterization of both adrenal veins during ACTH stimulation.
Conclusions
The most important finding of this study is that AVS is feasible and safe in the vast majority of patients, including the cohort with negative or equivocal CT and MR scan, i.e. those who are most challenging to the physician. An accurate diagnosis can be made, provided that the adrenal vein blood/infrarenal inferior vena cava cortisol is 1.1 or more. With a bilaterally selective AVS, a value of aldosterone/cortisol of one side over the contralateral side of 2.0 or greater identifies a unilateral source of excess aldosterone in approximately 80% of the patients. In contrast, no accurate diagnosis could be accomplished using data derived from unilaterally selective AVS. Given the high prevalence of incidentalomas (42) that can occur in patients with primary aldosteronism (43), the information that can be safely achieved with AVS is essential, in our view, for appropriate surgical management (49).
Received July 14, 2000.
Revised October 9, 2000.
Accepted November 26, 2000.
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P. Milliez, X. Girerd, P.-F. Plouin, J. Blacher, M. E. Safar, and J.-J. Mourad Evidence for an increased rate of cardiovascular events in patients with primary aldosteronism J. Am. Coll. Cardiol., April 19, 2005; 45(8): 1243 - 1248. [Abstract] [Full Text] [PDF]
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Y. Takeuchi, H. Suzuki, S. Ogura, R. Imai, Y. Yamazaki, T. Yamashita, Y. Miyamoto, H. Okazaki, K. Nakamura, K. Nakahara, et al. Venous Sampling for Fibroblast Growth Factor-23 Confirms Preoperative Diagnosis of Tumor-Induced Osteomalacia J. Clin. Endocrinol. Metab., August 1, 2004; 89(8): 3979 - 3982. [Abstract] [Full Text] [PDF]
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P.-F. Plouin, L. Amar, and G. Chatellier Trends in the prevalence of primary aldosteronism, aldosterone-producing adenomas, and surgically correctable aldosterone-dependent hypertension Nephrol. Dial. Transplant., April 1, 2004; 19(4): 774 - 777. [Full Text] [PDF]
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R. Coutant, H. Maurey, S. Rouleau, E. Mathieu, P. Mercier, J. M. Limal, and A. Le Bouil Defect in Epinephrine Production in Children with Craniopharyngioma: Functional or Organic Origin? J. Clin. Endocrinol. Metab., December 1, 2003; 88(12): 5969 - 5975. [Abstract] [Full Text] [PDF]
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E. A. Espiner, D. G. Ross, T. G. Yandle, A. M. Richards, and P. J. Hunt Predicting Surgically Remedial Primary Aldosteronism: Role of Adrenal Scanning, Posture Testing, and Adrenal Vein Sampling J. Clin. Endocrinol. Metab., August 1, 2003; 88(8): 3637 - 3644. [Abstract] [Full Text] [PDF]
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G. P. Rossi, V. Di Bello, C. Ganzaroli, A. Sacchetto, M. Cesari, A. Bertini, D. Giorgi, R. Scognamiglio, M. Mariani, and A. C. Pessina Excess ldosterone Is Associated With Alterations of Myocardial Texture in Primary Aldosteronism Hypertension, July 1, 2002; 40(1): 23 - 27. [Abstract] [Full Text] [PDF]
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) vs. cut-off values of the
(A/C)RAV/(A/C)LAV for the identification of
right APA. The best compromise between sensitivity and false
positive rate could be achieved with a cut-off value of 2.0
(vertical line). Similar results were
obtained for the (A/C)LAV/(A/C)RAV in the
identification of left APA.