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The Journal of Clinical Endocrinology & Metabolism Vol. 86, No. 2 604-607
Copyright © 2001 by The Endocrine Society

Original Studies

The Patients with Incidentally Discovered Adrenal Adenoma (Incidentaloma) Are Not at Increased Risk of Osteoporosis

G. Osella, G. Reimondo, P. Peretti, A. Alì, P. Paccotti, A. Angeli and M. Terzolo

Dipartimento di Scienze Cliniche e Biologiche, Medicina Interna I, A. O. San Luigi, 10043 Orbassano, Torino, Italy

Address all correspondence and requests for reprints to: Giangia- como Osella, M.D., Dipartimento di Scienze Cliniche e Biologiche, Medicina Interna I, A. O. San Luigi, Regione Gonzole 10, 10043 Orbassano, Torino, Italy. E-mail: g.osella{at}tiscalinet.it


   Abstract
Top
 Abstract
Introduction
 Subjects and Methods
 Results
 Discussion
 References
 
The main problem in the management of the patients with incidentally discovered adrenal mass (incidentaloma) is whether and when the incidental mass puts the patient at increased risk for an adverse outcome. As osteoporosis is a well known complication of endogenous and exogenous glucocorticoid excess, it is likely that patients with incidentally discovered adrenocortical adenomas have impaired bone mass due to subclinical hypercortisolism. We measured spinal bone mineral density (BMD) by dual energy x-ray absorptiometry in 27 patients (9 men and 18 women) and 54 healthy subjects (18 men and 36 women) carefully matched for age, sex, body mass index, and menstrual status for a case-control analysis. BMD was also measured at the hip in the group of patients. A multiple regression analysis was performed to determine which biochemical variables might influence BMD values. Lumbar BMD values in patients with adrenal incidentaloma were not significantly different from those in control subjects (BMD, 0.926, 0.604–1.144 vs. 0.936, 0.645–1.268 g/cm2; P = NS). No significant difference in lumbar and femoral BMD was found between patients with or without subclinical Cushing’s syndrome. Among the variables processed, only PTH remained in the final model and was inversely correlated with lumbar spine and femoral neck BMD values (r = -0.5; r2 = 0.25; P = 0.015 and r = -0.42; r2 = 0.18; P = 0.03, respectively). In conclusion, our data do not suggest that the slight glucocorticoid excess associated with adrenal incidentaloma increases the risk of osteoporosis. The evaluation of BMD does not seem to be crucial in the management of incidentally discovered adrenal masses.


   Introduction
Top
 Abstract
 Introduction
Subjects and Methods
 Results
 Discussion
 References
 
THE DETECTION of an adrenal mass as an incidental finding is so increasingly frequent to be considered as an endocrine epidemic (1). The number of incidental adrenal masses (adrenal incidentalomas) is expected to increase further in the coming years because of advances in imaging techniques. Cost-effective guidelines for diagnosis and management are admittedly needed. At the heart of the problem is whether and when an incidental mass puts the patient at increased risk for an adverse outcome (2). By definition, patients with incidentally discovered adrenal masses do not present with overt physical stigmata of Cushing’s syndrome, but a subtle state of cortisol excess (subclinical Cushing’s syndrome) is often present in the cohort of patients bearing adrenocortical adenoma (3, 4, 5, 6, 7, 8). Adrenocortical adenomas are the most frequent type of incidentalomas, accounting for more than 50% of cases in a large series in Italy (9).

The natural history of patients with apparently silent adrenocortical adenoma is presently unknown, and controversy exists about the possibility that subclinical Cushing’s syndrome has any relevant clinical impact, even if recent evidence suggests a link with hypertension, diabetes, obesity, and dyslipidemia (3, 7, 10, 11, 12, 13).

As long ago as 1932, Harvey Cushing recognized osteoporosis as a serious consequence of endogenous hypercortisolism (14). The prevalence of osteoporosis in patients with Cushing’s disease has been reported to be around 50% (15). Glucocorticoid excess often results in a negative calcium balance that leads to secondary hyperparathyroidism (16). Serum osteocalcin (BGP) is reduced in patients with Cushing’s syndrome, reflecting impaired bone formation (17, 18, 19). A slight reduction of BGP has also been reported in subjects with adrenal incidentalomas, whereas data about markers of bone resorption are conflicting (20, 21).

In patients with Cushing’s syndrome, bone mineral content and bone mineral density (BMD) are clearly reduced and improve significantly after successful treatment (22, 23, 24). To our knowledge, only two reports have presented data on BMD in subjects with adrenal incidentaloma (25, 26). Torlontano et al. found that spinal and femoral BMD were similar between 32 female patients with incidentaloma and 64 matched controls. BMD at each site was lower in the 8 patients with subclinical hypercortisolism (25). Conversely, Rossi et al. studying 18 patients with bone absorptiometry did not find any significant difference in BMD z-scores in patients with and without subclinical hypercortisolism (26).

The aim of the present study was to measure lumbar and femoral BMD in subjects with incidentally discovered adrenocortical adenomas and to correlate these data with the function of the hypothalamic-pituitary-adrenal (HPA) axis.


   Subjects and Methods
Top
 Abstract
 Introduction
 Subjects and Methods
Results
 Discussion
 References
 
We studied 27 consecutive patients (9 men and 18 women; mean and median age, 56.6 and 57 yr, respectively; range, 42–73 yr) bearing adrenal incidentaloma discovered during a diagnostic work-up performed for extraadrenal complaints. According to the definition of incidentaloma, none of the subjects had any sign or symptom of overt endocrine disease. Only the patients with presumed cortical adenoma were selected for the study. The diagnosis of cortical adenoma rested on the following computed tomography (CT) features: size no greater than 4.0 cm, regular shape with well defined margins and homogenous, hypodense content. Concerning this last feature, an attenuation value of 10, or fewer Hounsfield units on unenhanced CT scan and 30 or fewer Hounsfield units on enhanced CT scan were considered suggestive of adrenal adenoma (27, 28). The size of the mass did not change after at least 1 yr follow-up.

All of the patients were hospitalized and underwent biochemical screening to exclude silent pheochromocytoma or aldosterone-producing adenoma. Standard blood analytes were determined using routine clinical laboratory methods and were in the normal ranges. None of the patients had a clinical history of bone disease or was taking any medication known to affect bone turnover, including calcium and hormonal replacement therapy.

All of the patients underwent the following endocrine evaluation: 1) measurement of serum cortisol at 0800 and 2400 h; 2) measurement of the 24-h excretion of urinary free cortisol (UFC); 3) measurement of plasma ACTH, serum dehydroepiandrosterone sulfate (DHEA-S), testosterone, PTH, BGP at 0800 h; and 4) overnight dexamethasone suppression test (1 mg, orally, at 2300 h and measurement of serum cortisol at 0800 h the following morning). Premenopausal women were tested in the follicular phase of the menstrual cycle.

Serum and urinary cortisol and serum testosterone were measured by RIA (Sorin Biomedica, Saluggia, Italy), serum DHEA-S was determined by RIA (Diagnostics Systems Laboratories, Inc., Webster, TX), plasma ACTH and serum PTH were measured by immunoradiometric assay (Nichols Institute Diagnostics, San Juan Capistrano, CA), and serum BGP was determined by RIA (CIS Diagnostici, Santhià, Italy). Sera were immediately separated and stored at -20 C until assayed. All hormonal assays of a single subject were performed in duplicate in the same assay section. Intra- and interassay coefficients of variation for all of the above-mentioned variables were below 8% and 12%, respectively.

The reference ranges of the tests used to study the HPA axis were determined in healthy subjects as previously reported (4). Briefly, normal ACTH levels ranged between 1–13 pmol/L (5–59 pg/mL); normal average cortisol levels and 2400 h/0800 h cortisol percent ratio ranged between 165–414 nmol/L (6–15 µg/dL) and 12–47%, respectively. The upper limit of normality for UFC levels was 596 nmol/24 h (216 µg/24 h). Normal dexamethasone suppression was demonstrated when morning cortisol levels fell below 138 nmol/L (5 µg/dL) (29). The ranges of normality for DHEA-S levels (calculated in a group of 180 healthy subjects) were 402-1751 nmol/L (116–505 µg/dL) and 243-1491 nmol/L (70–430 µg/dL), respectively, for men and women under 40 yr of age; 277-1456 nmol/L (80–420 µg/dL) and 208–957 nmol/L (60–276 µg/dL), respectively, for men and women between 41 and 60 yr, and 73–1345 nmol/L (21–388 µg/dL) and 243-1491 nmol/L (70–430 µg/dL), respectively, for men and women over 60 yr of age. Normal ranges of testosterone are less than 2.8 nmol/L (0.8 ng/mL) for women and between 14–35 nmol/L (4.0 and 10.0 ng/mL) for men; the normal range of serum PTH is 10–65 pg/mL; the normal range of serum BGP is 2.5–7 ng/mL for men and premenopausal women and 3.5–11 ng/mL for postmenopausal women. The presence of subclinical Cushing’s syndrome was established as previously reported (4). Briefly, the association of at least two abnormal results in the tests used to evaluate the HPA axis (elevated UFC, failure of cortisol to suppress after dexamethasone, suppressed ACTH, high cortisol average, and elevated night/day ratio) was required to qualify a patient for subclinical Cushing’s syndrome.

Dual energy x-ray absorptiometry of the lumbar spine (L1–L4) was performed in the patients and also in 54 healthy subjects (18 men and 36 women) to perform a 1:2 case-control analysis. Control subjects were recruited among the medical staff of our institute and their relatives. They had no previous personal or family history of osteoporosis or metabolic bone disease, were not taking medication, and were carefully matched for sex, age (patients: median, 57; range, 42–73 yr; controls: median, 56.5; range, 41–74 yr), body mass index (patients: median, 24.6; range, 19.3–32.2 kg/m2; controls: median, 24.1; range, 19.9–33.9 kg/m2), and menstrual status. As glucocorticoids affect predominantly trabecular bone (30, 31), we focused the case-control analysis on the lumbar spine. In the patient group we also measured BMD at the hip, but because of budgetary restrictions we did not have dual energy x-ray absorptiometry data on this site in the controls.

Bone density was determined using the Hologic QDR 4500 W instrument (Hologic, Inc., Waltham, MA; software version 9.03). According to the manufacturer, in vivo precision is less than 1%. Data were analyzed using absolute BMD values (grams/cm2), t-score (or young adult z-score), and z-score referred to the manufacturer’s normative data of L1–L4, total hip, and femoral neck. The classical WHO criteria (32) were used to define the conditions of normality, osteopenia, and osteoporosis (t-score, above -1, between -1 and -2.5, or below -2.5, respectively).

Because criteria for normal distribution were not satisfied at the Wilk-Shapiro test, statistical analysis was performed using nonparametric methods (Mann-Whitney U test for continuous variables and 2 x 2 table with Yates correction for categorical variables). Spearman rank correlation analysis was performed as appropriate. A multiple regression analysis was performed to determine which variables might influence BMD values. The candidate predictive variables were chosen after performing a matrix of simple correlations. They were age, PTH, BGP, and UFC. Levels of statistical significance were set at P < 0.05. Data are expressed as the median and range.

All of the patients and controls gave their informed consent to the study, and the design of the study was approved by the local ethical committee.


   Results
Top
 Abstract
 Introduction
 Subjects and Methods
 Results
Discussion
 References
 
Pertinent clinical data for the patients are given in Table 1Go. Lumbar BMD values in patients with adrenal incidentaloma were not significantly different from those in control subjects [BMD (median and range), 0.926 and 0.604–1.144 g/cm2 vs. 0.936 and 0.645–1.268 g/cm2 (P = NS); t-score, -1.10 and -4.17 to 0.88 vs. -1.10 and -3.65 to 2.01 (P = NS); z-score, -0.33 and -3.86 to 1.79 vs. -0.34 and -2.96 to 2.67 (P = NS); Fig. 1Go]. According to WHO criteria (32), t-scores were in the normal range in 14 of 27 (52%) patients while they were in the osteopenic range in 7 of 27 (26%) patients, and they were in the osteoporotic range in 6 of 27 (22%) patients. Seventy percent of the patients had z-scores greater than -1, 23% had scores between -1 and -2.5, and 7% had scores below -2.5. In female patients the proportion of abnormal t-scores (osteopenia plus osteoporosis) was greater than that in males (11 of 18, 61% vs. 3 of 9, 33%), but the difference was not statistically significant.


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  		Table 1.

 


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  		Figure 1. The scatterplot shows the individual z-score of BMD of the lumbar spine in the group of 27 subjects with adrenal incidentaloma ({blacksquare}) and 54 matched controls ({blacktriangleup}).

 
BMD of the total hip was 0.890 g/cm2 (range, 0.551–1.140); the t-score was -0.77 (range, -3.53 to 1.17); the z-score was -0.04 (range, -2.59 to 1.26). The figures for the femoral neck were: BMD, 0.736 g/cm2 (range, 0.502–0.971), t-score, -1.59 (range, -4.02 to 0.76), and z-score, -0.45 (range, -2.92 to 1.03). The t-scores of the total hip were in the normal range in 70%, in the osteopenic range in 26%, and in the osteoporotic range in 4% of patients. Eighty-five percent of the patients had z-scores above -1, 11% had scores between -1 and -2.5, and 4% had scores below -2.5.

The t-scores of the femoral neck were in the normal range in 41%, in the osteopenic range in 37%, and in the osteoporotic range in 22% of patients. Seventy percent of the patients had z-scores greater than -1, 26% had scores between -1 and -2.5, and 4% had scores less than -2.5.

Among the variables processed in the multiple regression analysis, only PTH remained in the final model and was inversely correlated with either lumbar or femoral neck BMD values (r = -0.5; r2 = 0.25; P = 0.015 and r = -0.42; r2 = 0.18; P = 0.03, respectively).

Using the above-mentioned criteria, 8 of 27 (30%) patients qualified for subclinical Cushing’s syndrome. No significant difference in lumbar BMD was found between patients with and without subclinical Cushing’s syndrome [BMD (median and range), 0.929 and 0.707–1.144 g/cm2 vs. 0.926 and 0.604–1.113 g/cm2 (P = NS); z-score, -0.55 and -1.82 to 1.79 vs. -0.33 and -3.86 to 1.62 (P = NS)]. The same was true when considering BMD measured at the total hip and the femoral neck (data not shown). In postmenopausal women, a significant inverse correlation was found between the number of years after the menopause and BMD values (lumbar BMD: r = -0.60; P = 0.02; femoral neck: r = -0.59; P = 0.02).


   Discussion
Top
 Abstract
 Introduction
 Subjects and Methods
 Results
 Discussion
References
 
Glucocorticoids are well known inhibitors of bone formation and intestinal calcium absorption. Therefore, as many as 50% of patients with Cushing’s syndrome or subjects chronically treated with synthetic corticoid derivatives suffer from osteoporotic fractures (15). Recently, Torlontano et al. found that bone mass was also reduced in women with adrenal incidentaloma exposed to a slight degree of cortisol excess (subclinical Cushing’s syndrome) (25). Even if the researchers emphasized the issue of osteoporosis, bone mass did not differ between the whole group of their patients and controls. In a further study, Rossi et al. did not find significant bone loss in patients with adrenal incidentaloma, even when associated with subclinical Cushing’s syndrome (26).

The outcome of the present study does not support the view that osteoporosis is a relevant clinical problem of patients with incidentally discovered adrenocortical adenoma, because bone mass was not significantly lower in patients than in carefully matched controls. Moreover, we did not find any difference in either lumbar or femoral BMD between patients with or without subclinical Cushing’s syndrome, arguing that a slight degree of cortisol excess is not so detrimental for bone.

The present conclusions are at variance with those of Torlontano et al. (25), but it is not easy to account for the reason(s) for the discrepancy. The outcome of our study does not change when restricting the analysis to women, as done by Torlontano et al. (25). As glucocorticoid-induced osteoporosis predominantly affects the axial skeleton (30, 31), we limited the case-control analysis to the spine. Torlontano et al. also analyzed the hip, and their results were otherwise comparable at either site. A major difference was in the criteria used to define subclinical Cushing’s syndrome, because the association of at least two hormone alterations was required in our study, whereas the elevation of UFC was the only criterion chosen by Torlontano et al. (25). Different endocrine protocols were used to explore the function of the HPA axis in the literature, but most researchers suggest that two or more abnormalities should be present to define a truly relevant hypercortisolemic state (7, 9, 26, 33). The pitfalls in using only UFC to qualify a patient for subclinical Cushing’s syndrome also come from the observation that fast bone-loosing oophorectomized women display high normal values of UFC excretion (34). Torlontano et al. may have selected patients at higher risk of osteoporosis for reasons not related to the adrenal adenoma but to their condition of fast bone loss, and indeed, differences in BMD were confirmed only in their subgroup of postmenopausal women (25).

We confirmed the inverse correlation between BMD values and serum PTH levels in the whole group of patients with adrenal incidentaloma. Secondary hyperparathyroidism has been described in patients with Cushing’s syndrome (35), but it is also common in the general population of osteoporotic patients, possibly due to an underestimated occurrence of vitamin D deficiency (36). There are presently no data available in the literature on vitamin D metabolites in patients with adrenal incidentaloma.

To conclude, the present data do not suggest that an incidental adrenal adenoma puts the patient at increased risk of osteoporosis, notwithstanding the slight degree of cortisol excess (subclinical Cushing’s syndrome) that may be observed in this circumstance. At the present time the evaluation of BMD does not seem to have a role in the management strategies of patients with adrenal incidentaloma. However, a prolonged longitudinal study is needed to assess the risk for fracture of patients with subclinical Cushing’s syndrome.


   Acknowledgments
 
We thank Angela Termine for the skillful technical assistance.

Received June 29, 2000.

Revised August 29, 2000.

Revised October 6, 2000.

Accepted October 16, 2000.


   References
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 Abstract
 Introduction
 Subjects and Methods
 Results
 Discussion
 References
 

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