Society for Endocrinology
European Society of Endocrinology
Incidence and risk factors of venous thromboembolism in an adrenocortical carcinoma patient cohort
Nienke Visser1, Isabelle Holscher02, C Willemien Menke-van der Houven van Oordt3, Anton F Engelsman2, Els J M Nieveen van Dijkum2, Alberto M Pereira1 and Koen M A Dreijerink ®1
1Department of Endocrinology and Metabolism, Amsterdam University Medical Centres, University of Amsterdam, Amsterdam, The Netherlands
2Department of Surgery, Amsterdam University Medical Centres, Cancer Centre Amsterdam, Amsterdam, The Netherlands
3Department of Medical Oncology, Amsterdam University Medical Centres, Cancer Centre Amsterdam, Amsterdam, The Netherlands
Correspondence should be addressed to K M A Dreijerink: k.dreijerink@amsterdamumc.nl
Abstract
Adrenocortical carcinoma (ACC) is a rare and aggressive endocrine malignancy. Venous thromboembolic events (VTE) have been reported in ACC patients. ACC is often associated with endogenous hypercortisolism, which is linked to increased VTE risk. The primary objective of this retrospective study in patients who received treatment for ACC at Amsterdam UMC between 2003 and 2024 was to determine the total incidence of VTE. Secondary objectives included determining the incidence of VTE after adrenalectomy and identifying risk factors for VTE. Patients were categorised into VTE and non-VTE groups. Mann-Whitney U tests, unpaired t-tests, and Chi-square or Fisher’s exact tests were used in order to assess differences. Seventy-four patients were included, of whom ten (13.5%) had experienced a VTE during the observation period, amounting to 29 VTEs (CI 13-58) per 1,000 patient-years. All VTEs were pulmonary embolisms. Sixty-four patients underwent adrenalectomy. Fifty (98%) patients, for whom data were available, used peri-operative thromboprophylaxis or anticoagulant therapy. The median duration of peri-operative thromboprophylaxis was 5 days (IQR 4-11, range 0-90). Two patients experienced a VTE within 6 months after surgery (3.3%). Four patients with a VTE (40%) had cortisol-producing ACC (P = 0.83). We conclude that the overall incidence of VTE in ACC patients is high. The incidence of post-operative VTE after adrenalectomy for ACC was lower in this cohort compared with that reported in the literature. No risk factors for VTE were identified; most notably, hypercortisolism was not associated with increased VTE incidence. Our findings expand the literature addressing this issue and reaffirm the importance of the use of peri-operative thromboprophylaxis in ACC patients undergoing adrenalectomy.
Keywords: venous thromboembolism; venous thromboembolic event; thromboprophylaxis; adrenocortical carcinoma; endogenous hypercortisolism
Introduction
Adrenocortical carcinoma (ACC) is a rare and often aggressive type of cancer originating from the adrenal cortex. ACC has an annual population incidence of about one per million. In 45-70% of cases, ACC is associated with hypersecretion of adrenocortical steroid hormones, including cortisol and sex hormones. Excess cortisol
production is considered a poor prognostic factor (1, 2). The mainstay of curative ACC therapy is surgical removal of the tumour. However, the prognosis of ACC is often poor due to high recurrence rates after adrenalectomy. In the adjuvant setting and in patients with metastatic disease, mitotane is the first treatment of choice.
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In addition, in patients with metastatic disease, mitotane can be combined with etoposide-doxorubicin-cisplatin (EDP) (3). ACC frequently presents at an advanced stage. The 5-year survival of patients with metastatic disease is poor (4). Still, debulking by adrenalectomy has been reported to be associated with longer life expectancy in patients with metastatic ACC and is therefore carried out regularly in this patient group (5, 6).
Venous thromboembolic events (VTE), such as deep venous thrombosis (DVT) and pulmonary embolism, have been reported in ACC patient cohorts (7, 8, 9). Malignancy-associated hypercoagulability is a known cause of VTE. In addition, VTE can result from treatment-related factors such as chemotherapy or surgery (10). In addition, in a subgroup of ACC patients, VTE risk may further be increased due to endogenous hypercortisolism or Cushing’s syndrome. Endogenous hypercortisolism causes a hypercoagulable state and has been associated with increased VTE risk, particularly in Cushing’s disease (11, 12, 13, 14). Cohort studies addressing VTE in ACC patients have thus far not identified hypercortisolism as a risk factor (8, 9). In this single-centre retrospective study, we aimed to determine the incidence of VTE in ACC patients and identify risk factors, in particular after adrenalectomy, in order to expand our understanding of this phenomenon and to further inform future thromboprophylaxis strategies.
Materials and methods
In this single-centre retrospective cohort study, patients who underwent treatment for ACC between 2003 and 2024 at Amsterdam UMC were included. The primary aim of this study was to assess the incidence of VTE in patients with ACC. Secondary objectives were to identify potential risk factors for the development of VTE. Patients were included if they were 18 years or older, were diagnosed with histologically confirmed ACC, and had received treatment at Amsterdam UMC during the study period.
The study was found to be exempt from consideration by the medical ethical committee of Amsterdam UMC (2025- 0397). Data were collected from medical records. In addition to baseline demographic characteristics, tumour characteristics collected included primary tumour size, laterality, and ENSAT stage at diagnosis and at the time of the VTE or the end of follow-up. The hormonal work-up, including assessment for endogenous hypercortisolism, was in line with guideline recommendations (3). Peri- operative data from patients who underwent surgery, such as the type of procedure (laparotomy or laparoscopy), peri-operative complications, and total hospital stay, were recorded, as were known risk factors for VTE: BMI, smoking, and oral contraceptive use.
A diagnosis of VTE had to be confirmed by imaging. Tumour thrombi were not considered VTEs. The start and stop dates of thromboprophylaxis, duration after
| surgery, | and | complications | while | on | |
|---|---|---|---|---|---|
| thromboprophylaxis patient files. | were | extracted | from | the | |
Person-time in years was calculated by subtracting the date of the VTE within the study period, death, or the end of follow-up, whichever occurred first, from the date of diagnosis. Incidence rates were presented per 1,000 person-years with accompanying 95% confidence intervals (CI). Patients were categorised into two groups: those who experienced a VTE and those who did not. The normality of distribution for continuous variables was initially assessed using visual inspection of histograms. When the visual inspection was inconclusive, the Shapiro-Wilk test was conducted to evaluate the normality of the data distribution. Normally distributed continuous variables were presented as mean values with standard deviations (SD), while non-normally distributed continuous variables were presented as medians with interquartile ranges (IQRs). Categorical variables were presented as absolute numbers and percentages. As a result, descriptive statistics were employed to assess potential differences between groups. Comparisons between continuous variables were conducted using the Mann-Whitney U test for non-normally distributed data and the unpaired t-test for normally distributed data. Categorical variables were compared using the Chi-square or Fisher’s exact test. The Fisher’s exact test was used when counts <5 were present in the 2 × 2 table. A two-tailed P-value of <0.05 was considered statistically significant. Patients with missing data were excluded from the analysis only for those variables that were missing. We used Statistical Package for the Social Sciences (SPSS, version 28.0, IBM Corp., USA) software.
Results
Between 2003 and 2024, 78 patients were listed as having an ACC diagnosis. Four patients were not treated for ACC at Amsterdam UMC, resulting in 74 patients fulfilling the inclusion criteria (Fig. 1). Table 1 provides an overview of
78 patients with ACC diagnosis in Amsterdam UMC between 2003 and August 2024
4 patients not treated in Amsterdam UMC
74 Total inclusions 64 (of 74) patients underwent adrenalectomy
| Total (n = 74) | No VTE (n = 64) | VTE (n = 10) | P-value | |
|---|---|---|---|---|
| Female | 44 (59.5%) | 38 | 6 | 1 |
| Age (at diagnosis) | 53.4 (15.4) | 54.1 (15.8) | 48.6 (2.9) | 0.203 |
| BMI (kg/m2)* | 26.5 (5) | 26.6 (5.1) | 25.7 (5) | 0.730 |
| Hormonal activity tumour | 0.834 | |||
| · Cortisol | 33 (44.6%) | 29 (45.3%) | 4 (40%) | |
| · None | 38 (51.4%) | 32 (50%) | 6 (60%) | |
| · Other | 3 (4.1%) | 3 (4.7%) | 0 (0%) | |
| ENSAT stage at ACC diagnosis+ | 0.331 | |||
| · 1 | 4 (5.6%) | 4 (6.5%) | 0 (0%) | |
| · 2 | 18 (25%) | 14 (22.6%) | 4 (40%) | |
| · 3 | 21 (29.2%) | 20 (32.3%) | 1 (10%) | |
| · 4 | 29 (40.3%) | 24 (38.7%) | 5 (50%) | |
| ENSAT stage 4 at VTE or end of follow-up | 49 (66%) | 40 (63%) | 9 (90%) | 0.149 |
| Mitotane and/or chemotherapy | 60 (81%) | 50 (78%) | 10 (100%) | 0.192 |
| Smoking* | 0.516 | |||
| · Yes | 15 (21.4%) | 12 (19.7%) | 3 (33.3%) | |
| · No | 26 (37.1%) | 24 (39.3%) | 2 (22.2%) | |
| · Former | 29 (41.4%) | 25 (41%) | 4 (44.4%) | |
| Laterality | 0.622 | |||
| · Left | 35 (47.3%) | 31 (48.4%) | 4 (40%) | |
| · Right | 39 (52.7%) | 33 (51.6%) | 6 (60%) | |
| Tumour size (mm)* | 129.1 (74.8) | 129.8 (79.2) | 125 (41.8) | 0.331 |
VTE, venous thromboembolic event; BMI, body mass index; ACC, adrenocortical carcinoma.
*3 missing. 12 missing. +4 missing.
the patients’ main demographic, disease, and treatment characteristics: 44 (59.5%) were female, and the mean age at diagnosis was 53.4 years (SD: 15.4, range 18-84 years). The mean duration of follow-up after the diagnosis of ACC was 3 years (range 0-14 years), and the total follow-up time included 237 person-years. Hormonally active tumours were present in 36 (48.7%) of the patients; 33 (44.6%) produced cortisol. Two tumours (co-) secreted testosterone, two aldosterone, and one oestradiol. Of all patients, 29 (39%) had stage 4 disease at diagnosis. Four patients had stage 1, 18 stage 2, and 21 stage 3 disease at diagnosis. The mean tumour size was 129 mm (SD 74.8), and 39 (52.7%) of the ACCs were located in the right adrenal gland. Of the 74 patients, 64 underwent adrenalectomy. Of the 33 patients with hypercortisolism, 16 (48%) received cortisol-lowering medication, which included ketoconazole, metyrapone, and osilodrostat. Table 2 summarises the main demographic, disease, and treatment characteristics of the patients who underwent adrenalectomy. The majority of the patients had a laparotomy (n = 49, 80.3%) rather than laparoscopic surgery. The median hospital stay duration was 7 days (IQR: 4-9, range 1-37). All patients underwent regular abdominal and thoracic CT imaging.
Ten of the 74 patients (13.5%) were diagnosed with a VTE during the observed period. The incidence rate of VTE was 29 (CI 13-58) cases per 1,000 person-years after ACC diagnosis. The median interval between the ACC diagnosis and VTE was +5 months (IQR: 0-16, range: - 1 to 32 months). All VTEs in this patient population were pulmonary embolisms, and there were no diagnoses of
DVT. Of the total patient population, three (30%) of the VTEs occurred within 1 month before the diagnosis of ACC, and seven VTEs occurred after the ACC diagnosis. Four VTEs (5.6%) occurred within 1 year after the ACC diagnosis. Nine (90%) patients had stage 4 disease at the time of the VTE, and all eventually received mitotane and/or chemotherapy. Three patients presented with symptomatic pulmonary embolisms, while the remaining seven cases were discovered incidentally during routine CT imaging.
Sixty-four patients underwent adrenalectomy. Nine VTEs occurred in this group of patients, of which six VTEs occurred post-operatively (listed in Table 3). Two patients (of the 61 patients who had not experienced a VTE before surgery, 3.3%) had a VTE within 6 months after surgery. One of these two VTEs occurred during the hospital stay, while the other occurred 2 months after surgery. The patient experiencing a VTE during the hospital stay was using postoperative thromboprophylaxis at the time of the VTE and did not have hypercortisolism. The patient who had a VTE 2 months after surgery had active hypercortisolism and was using a coumarin derivative for atrial fibrillation at the time of the VTE. One patient experienced a VTE between 6 and 12 months after surgery while not on thromboprophylaxis. One patient developed a VTE between 1 and 2 years after surgery. He was not on thromboprophylaxis and had previously been diagnosed with endogenous hypercortisolism, but there was no active Cushing’s syndrome at the time of the VTE. Two patients experienced a VTE between 2 and 3 years
| Total (n = 64) | No VTE (n = 55) | VTE (n = 9) | P-value | |
|---|---|---|---|---|
| Female | 41 (64.0%) | 35 | 6 | 1 |
| Age (at diagnosis) | 52.1 (15.1) | 52.6 (15.4) | 49 (13.6) | 0.388 |
| Age (at surgery) | 52.1 (15) | 52.6 (15.3) | 49.1 (13.5) | 0.424 |
| BMI (kg/m2)* | 26.8 (5.2) | 27 (5.3) | 25.8 (5.3) | 0.726 |
| Hormonal activity tumour | 0.831 | |||
| · Cortisol | 31 (48.4%) | 27 (49.9%) | 4 (44.4%) | |
| · None | 30 (46.9%) | 25 (45.5%) | 5 (55.6%) | |
| · Other | 3 (4.7%) | 3 (5.5%) | 0 (0%) | |
| ENSAT stage at ACC diagnosis* | 0.311 | |||
| · 1 | 4 (6.3%) | 4 (7.4%) | 0 (0%) | |
| · 2 | 18 (28.1%) | 14 (25.9%) | 4 (44.4%) | |
| · 3 | 21 (32.8%) | 20 (37%) | 1 (11.1%) | |
| · 4 | 20 (31.3%) | 16 (29.6%) | 4 (44.4%) | |
| Smoking+ | 0.239 | |||
| · Yes | 13 (21.3%) | 10 (18.9%) | 3 (37.5%) | |
| · No | 23 (37.7%) | 22 (41.5%) | 1 (12.5%) | |
| · Former | 25 (41%) | 21 (39.6%) | 4 (50%) | |
| Laterality | 0.494 | |||
| · Left | 29 (45.3%) | 26 (47.3%) | 3 (33.3%) | |
| · Right | 35 (54.7%) | 29 (52.7%) | 6 (66.7%) | |
| Tumour size (mm)* | 120.5 (54) | 119.6 (55.8) | 125.6 (44.3) | 0.631 |
| Surgical procedure+ | 0.337 | |||
| · Laparoscopy | 12 (19.7%) | 12 (22.6%) | 0 (0%) | |
| · Laparotomy | 49 (80.3%) | 41 (77.4%) | 8 (100%) | |
| Total hospital stay (days)§ | 7 (IQR: 4-9) | 7 (IQR: 4-9) | 6.5 (IQR: 6-8.5) | 0.156 |
| Already on thromboprophylaxis before surgery !! | 18 (28.1%) | 13 (26%) | 5 (55.6%) | 0.115 |
VTE, venous thromboembolic event; BMI, body mass index; ACC, adrenocortical carcinoma.
*1 missing. 13 missing. * 2 missing. $10 missing. 5 missing.
after surgery, both while not using thromboprophylaxis and in the absence of active hypercortisolism.
No statistically significant outcomes were found with regard to risk factors (Tables 1 and 2): although nine of the ten patients who experienced a VTE had ENSAT stage 4 disease at the time of the event, the stage at VTE was not found to be different from the disease stages in the no-VTE group at the end of follow-up. We found that six of the patients (60%) who experienced a VTE were older than 40 years at the time of the VTE diagnosis, with a mean age of 48.6 years (range 29-69 years). Two patients (20%) were undergoing chemotherapy at the time of the VTE. Three patients (33.3%) were smokers, and four (44.4%) were former smokers. Additional comorbidities observed in the patients with VTE included obesity (BMI ≥30 kg/m2) in four patients (40%), and four patients (40%) had cortisol-producing tumours; the other six patients (60%)
had non-functioning tumours. Six (60%) of the patients with VTE were female. None of the women was using oral contraceptives at the time of the VTE.
Thromboprophylaxis or anticoagulants were provided at any time in 62 patients (84%). Data regarding the use of postoperative thromboprophylaxis were available for 51 operated patients (80%). The median duration of thromboprophylaxis with low-molecular-weight heparin in this group following surgery was 6 days (IQR: 4-11). One patient did not receive any documented thromboprophylaxis peri-operatively, whereas the longest duration was 90 days. Ten patients (19.6%) received thromboprophylaxis >14 days; the other patients had varying durations of thromboprophylaxis between 0 and 14 days often related to their hospital stay duration and ending thromboprophylaxis on the day of discharge. Eighteen (28.1%) patients were already using
| Patient | 1 | 2 | 3 | 4 | 5 | 6 |
|---|---|---|---|---|---|---|
| VTE time post-op | 1 day | 2 months | 7 months | 1 year | 2 years | 2 years |
| ENSAT stage at VTE | 4 | 4 | 4 | 4 | 4 | 4 |
| CS at ACC diagnosis | No | Yes | No | Yes | No | Yes |
| Active CS at VTE | No | Yes | No | No | No | No |
| Thromboprophylaxis at time of VTE | LMWH | Coumarin | None | None | None | None |
VTE, venous thromboembolic event; Cushing’s syndrome/endogenous hypercortisolism; LMWH, low-molecular-weight heparin.
thromboprophylaxis or anticoagulant therapy at the time of surgery. Reasons included hospital stay before surgery (n = 5), endogenous hypercortisolism (n = 3), a clinical history of vascular disease (n = 3), and pre-operative VTE (3). Two patients had a bleeding-related complication during the use of postoperative thromboprophylaxis.
Discussion
The aim of this study was to determine the incidence and identify risk factors for VTE in 74 patients with ACC who underwent treatment at our centre. We found an overall incidence of ten VTEs (13.5%) and an incidence rate of 29 (CI 13-58) cases per 1,000 person-years after ACC diagnosis. Two events (3.3%) were observed in 61 patients who underwent surgery and had not experienced a VTE before, within 3 and 6 months after surgery, of which one event occurred within 30 days (1.6%). This cohort is the fourth ACC cohort in which VTE incidence has been reported in the literature. The incidence found in this study is considerable but lower compared with previous studies addressing this topic: a registry-based study carried out in the American College of Surgeons National Surgical Quality Improvement Program found a 30-day postoperative VTE occurrence of 2.6% in 576 ACC patients (7). In a single-centre study from the Netherlands, a 6-month postoperative VTE incidence of eight VTEs (24%) in 34 patients was observed (8). A similar study from the United States found an overall incidence of 54 VTEs in 289 ACC patients (18.7%), and a 6-month postoperative incidence of 18 VTEs in 216 operated patients (8.3%) (9). Peri-operative thromboprophylaxis use was reported to be in line with current guidelines in the patients included both in the Dutch and in the American studies (8, 9).
Nine of the ten patients who experienced a VTE in this study had ENSAT stage 4 disease at the time of the event; however, this was not significantly different from the no-VTE group (Table 1). We did not find an association between the presence of endogenous hypercortisolism and VTE in this cohort, which is in line with previous reports (8, 9). Higher incidences of VTE compared with the healthy population have been reported in studies on patients with endogenous hypercortisolism (11, 12, 13, 14). Use of thromboprophylaxis has been associated with a lower incidence of VTE in patients with endogenous hypercortisolism (15). These observations have recently resulted in guidelines for extended thromboprophylaxis in endogenous Cushing’s syndrome (16). A key recommendation from this consensus paper is that thromboprophylaxis should be considered at the time of hypercortisolism diagnosis and continued for 3 months after biochemical remission, provided there are no obvious contraindications. It should be noted that in benign adrenal ACTH-independent endogenous hypercortisolism, VTE incidence appears to be lower
than in Cushing’s disease, in particular in the postoperative phase (7, 11, 13, 14). Therefore, given the fact that there was no association between the presence of endogenous hypercortisolism and VTE in this study, the high VTE incidence in ACC patients may be predominantly attributed to malignancy-associated risk factors, as is the case in many types of cancer (10, 17). The postoperative incidence of VTE in this cohort is comparable to the cumulative VTE incidence 6 months after orthopaedic surgery in patients using postoperative thromboprophylaxis (2.7%) (18). A limitation of this study is that due to the low number of VTEs in the cohort, we were not able to perform more extensive analyses to identify specific predictors of VTE, nor did the study have the statistical power to exclude associations between risk factors and VTEs. Additional and more comprehensive studies, preferably set up prospectively, are needed to provide more detailed information about the risk factors associated with VTE to further guide thromboprophylaxis strategies tailored for ACC patients.
In conclusion, the incidence of VTE in ACC patients is high. VTE in ACC appears not to be related to endogenous hypercortisolism. Our findings expand the literature addressing this issue and reaffirm the importance of the use of thromboprophylaxis after adrenalectomy and possibly extended thromboprophylaxis in case of additional potential risk factors.
Declaration of interest
The authors declare that there is no conflict of interest that could be perceived as prejudicing the impartiality of the work reported.
Funding
This work did not receive any specific grant from any funding agency in the public, commercial, or not-for-profit sector.
Ethical approval
The study was found to be exempt from consideration by the medical ethical committee of Amsterdam UMC (2025-0397).
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