Case Series Prolonged Mitotane Administration in Metastatic Adrenocortical Carcinoma With Over a Decade of Survival: A Case Series

Lorenzo Tucci (D,1,2,3 Mengjie Xu (D,1,4 Miriam Asia,5 Kassiani Skordilis,6 Maninder S. Kalkat (D,7 Madava Djearaman,8 Robert P. Sutcliffe (D,9 Yasir S. Elhassan D,5 Alessandro Prete (D,1,5,10 and Cristina L. Ronchi iD1,5

1 Department of Metabolism and Systems Science, College of Medicine and Health, University of Birmingham, Birmingham, UK

2Department of Medical and Surgical Sciences Department, Alma Mater University of Bologna, Bologna, Italy

3Division of Endocrinology and Prevention and Care of Diabetes, IRCCS Azienda Ospedaliero-Universitaria di Bologna, Bologna, Italy

4Department of Endocrinology, Taihe Hospital, Hubei University of Medicine, Shiyan, China

5Department of Endocrinology, Queen Elizabeth Hospital Birmingham NHS Trust, Birmingham, UK

6Department of Cellular Pathology, Queen Elizabeth Hospital Birmingham NHS Trust, Birmingham, UK

7Department of Thoracic Surgery, Queen Elizabeth Hospital Birmingham NHS Trust, Birmingham, UK

8 Department of Imaging, Queen Elizabeth Hospital Birmingham NHS Trust, Birmingham, UK

9 Department of Hepatobiliary Surgery, Queen Elizabeth Hospital Birmingham NHS Trust, Birmingham, UK

10NIHR Birmingham Biomedical Research Centre, University of Birmingham and University Hospitals Birmingham NHS Trust, Birmingham, UK

Correspondence should be addressed to Cristina L. Ronchi; c.l.ronchi@bham.ac.uk

Received 16 May 2025; Revised 27 October 2025; Accepted 5 November 2025

Academic Editor: Osamu Isozaki

Copyright @ 2025 Lorenzo Tucci et al. Case Reports in Endocrinology published by John Wiley & Sons Ltd. This is an open access article under the terms of the Creative Commons Attribution License, which permits use, distribution and reproduction in any medium, provided the original work is properly cited.

Background: Reports of long-survival patients (>10 years) with metastatic adrenocortical carcinoma (ACC) and prolonged treatment with mitotane alone (>5 years) are rare. We present four patients treated for low tumour burden (LTB) metastatic ACC using multidisciplinary approaches, including long-term mitotane, who maintained a relatively good life quality for over 10- year survival.

Case Series Presentation: Four patients (one female) aged 34-52 years underwent adrenalectomy for ACC between 2004 and 2013. Two patients presented only with flank pain, while two presented with overt Cushing’s Syndrome. Ki-67 index ranged from <1% to 37%, and European Network for Study of Adrenal Tumour (ENSAT) tumour stage ranged from 2 to 3. Time to first recurrence ranged from 8 to 48 months. Overtime, all patients experienced recurrent metastatic disease, mostly in lungs or liver. From 2008 to 2024, we recorded a total of two stereotactic ablative radiotherapies, one microwave and eight radiofrequencies ablations, 10 liver and eight lung resections and three selective excisions for other abdominal metastases. Mitotane treatment lasted from 7.7 to 12.9 years, with mitotane average dose and plasma levels equal to 2.6±0.9 g/day (±standard deviation) and 20.4 ± 5.3 mg/L, respec- tively. Our patients developed different degrees of mitotane-induced hypothyroidism, hypogonadism, hypercholesterolaemia and mineralocorticoid insufficiency as well as episodes of neurologic and gastrointestinal side effects, which were countered with continuous dose adjustments, hormonal replacement therapies and specific treatments. Specialist nurses provided continuous support for mitotane dose titration and management of mitotane-induced adverse effects. All the patients were still taking mitotane at last available follow-up visit without radiological evidence of tumour manifestations, with a follow up duration ranging from 11.5 to 20 years from initial surgery.

Conclusion: Metastatic ACC should be managed by multidisciplinary tailored approaches, including close surveillance and local therapies (LT). In patients with LTB, prolonged mitotane therapy can represent a safe option to slow down disease progression and contribute to prolonging survival.

Keywords: adrenocortical cancer; local therapy; long-term survival; low tumour burden; metastases; minimally invasive treatment; mitotane; recurrences

1. Background

Adrenocortical carcinoma (ACC) is a rare malignancy (0.5-2 cases/million/year) with an overall 5-year survival rate equal to 65%-82%, 56%-68%, 41%-55% and 10%-20% for tumour stages according to the European Network for Study of Adrenal Tumour (ENSAT) 1, 2, 3 and 4, respectively, and a median life expectancy of 15 months at Stage 4, with metastases frequently localised in the liver, lungs and bones [1-6]. The only drug approved for ACC by the European Medical Agency and by the Food and Drug Administration is mitotane, an adrenolytic agent with a long half-life, a narrow therapeutic window and numerous and potentially severe side effects. Therefore, it is recommended that patients taking mitotane undergo close clin- ical and laboratory monitoring [7]. International guidelines rec- ommend using mitotane either in an adjuvant setting for patients who underwent complete surgical resection but are considered at high risk for recurrence or in patients with advanced ACC aiming to increase overall and progression- free survival (PFS) [2, 3, 8, 9]. However, due to lack of evidence, current guidelines do not provide clear recommendations about the benefits and safety of mitotane treatment for periods longer than 5 years [2, 3, 8, 9]. In case of disease progression, guidelines suggest to associate mitotane with a systemic chemotherapy based on a combination of etoposide, cisplatin and doxorubicin (EDP), but side effects are common and the response rate remains unsatisfactory, that is, 15%-35% of treated cases [3, 8]. Guidelines also recommend to use local therapies (LT), especially in patients with low tumour burden (LTB, lesions smaller than 5 cm in size associated with a disease-free interval greater than 9 months), as additional options for the manage- ment of metastatic ACC, independently from systemic therapy [2]. LTs may include radiofrequency ablation (RFA), transcath- eter arterial chemoembolization and microwave ablation, all of which have been proved to have a positive impact in controlling localised metastatic lesions, mostly in patients with LTB in the liver and lungs [9-11]. Recent studies also investigated stereo- tactic ablative radiotherapy (SABR) for metastatic ACC with promising results, albeit heterogeneous [11, 12]. Potential ben- efits of LTs and resurgeries in metastatic ACC can be found even in articles from the early ’90s, especially in those about long- term survivors (> 10 years) with metastatic ACC [13-23]. How- ever, in these articles, patients had been treated with different approaches, and no or scarce descriptions of systemic therapies are provided [13-23]. Moreover, even if some patients surpassed 20 years of survival, there is no exhaustive description of pro- longed use (> 5 years) of mitotane in monotherapy [13-23].

Hence, nowadays it is not clear whether long-term treat- ment with mitotane could be useful and safe for patients with recurrent LTB metastatic ACC not suitable for or not willing to

undergo EDP. In the attempt to help filling this void, we checked our records looking for patients treated with pro- longed mitotane administration without EDP or other chemo- therapy schemes (Figure 1). Therefore, we present four cases of long-term metastatic ACC survivors, which had recurrent LTB and were managed by our multidisciplinary Team (MDT) through a combination of multiple surgical resections and LTs, as well as long-term mitotane therapy for over 10 years. All cases are reported following the CARE guidelines [24].

2. Case 1

2.1. Case Presentation. In September 2009, a 49-year-old man with unremarkable past medical history, underwent a thor- ax-abdomen-pelvis (TAP) contrast-enhanced computerised tomography (CT) scan for abdominal pain, which revealed a left upper quadrant mass measuring 21 cm × 19 cm × 16 cm with diffuse calcifications and central necrosis with no evidence of metastatic disease (Figure 2a). Details of case presentation at diagnosis are in Table 1. The patient underwent excision of the 3.8 kg left retroperitoneal mass in October 2009. The histologi- cal examination showed a diagnosis of conventional ACC with Weiss score 5/9, ENSAT Stage 3 (invasion of surrounding tissue), Resection status unknown (Rx), and Ki-67 index <1%. We retrospectively calculated the S-GRAS score as 3. S- GRAS score is based on five clinical/histopathological variables (i.e., age, symptoms at diagnosis, ENSAT tumour stage, resection status and Ki-67 index) as previously published [25].

2.2. Long-Term Pharmacological Treatment With Mitotane. The patient was referred to our department in March 2011, after the first disease recurrence (see paragraph below), when the case was reviewed by our adrenal MDT. Mitotane was started according to a high-dose saturation regimen along- side hydrocortisone replacement therapy [26]. The patient has been on continuous mitotane treatment from March 2011 to June 2024 (time of last record) but was briefly dis- continued in 2013 due to adrenal crisis, with a Time in Target Range (TTR) of 41.7% (Table 1) [27]. The patient experienced one severe episode of neurotoxic side effects (slurred speech in April 2012) and developed mitotane- induced hypogonadism (June 2012), mineralocorticoid insufficiency (January 2013) and hypothyroidism (December 2015). Mitotane dose was temporary reduced to face neuro- toxicity, while hypogonadism was treated with intramuscular nandrolone in the first place, then dihydrotestosterone skin gel, and fludrocortisone and levothyroxine were used for mineralocorticoid insufficiency and hypothyroidism, respec- tively. The patient was well compliant to all medications throughout the follow-up period and reported both a good

FIGURE 1: Identification of patients with adrenocortical cancer that received only prolonged mitotane administration (no etoposide-doxor- ubicin-cisplatin or other chemotherapy schemes). ACC, adrenocortical cancer; EDP, etoposide-doxorubicin-cisplatin.

Identification of patients with ACC that received only prolonged mitotane administration (no EDP or other chemotherapy schemes)

167 (from 2004 to 2024)

69 did not receive EDP or other chemotherapy schemes

98 received EDP or other chemotherapy schemes

25 did not receive mitotane or have no data about mitotane administration

44 received only mitotane

40 had mitotane less than 5 years

4 had prolonged mitotane administration

FIGURE 2: Computerised tomography at diagnosis of Case 1 (a) and Case 3 (b). (a) Computerised tomography of adrenocortical cancer at diagnosis time for Case 1; (b) computerised tomography of adrenocortical cancer at diagnosis time for Case 3.

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tolerability of mitotane after treatment of related side effects and a relatively good quality of life.

2.3. Long-Term Radiological Surveillance and Additional Treatments. Starting from June 2010, the patient underwent a TAP contrast-enhanced CT scan every 3-6 months. The patient had his first recurrence in December 2010, which presented with millimetric bilateral lung nodules, also confirmed through 18-fluorodeoxyglucose positron emission tomography-CT (FDG-PET-CT). In ~15 years of follow up, the patient had nine lung recurrences (min-max size: 6-14 mm) treated with two bilateral VAT lung excisions (2010 and 2011), six RFAs (2016, 2017, 2018, two in 2020, 2023) and one microwave abla- tion (2021, too close to the heart to perform RFA), a 5 cm recurrence in the 8th right rib treated with SABR (2017) and a 3 cm colon metastasis removed with polyp excision through colonoscopy (2017). The patient remained disease-free at the last surveillance CT scan in September 2024.

3. Case 2

3.1. Case Presentation. In November 2011, a 52-year-old female was diagnosed adrenocorticotropic hormone indepen- dent Cushing’s Syndrome with androgen excess and associated

with a 22 cm left adrenal mass (Table 1). Her past medical history included hysterectomy with bilateral oophorectomy for metrorrhagia (2006) and asthma. Her medical therapy included oestrogen replacement therapy (stopped in October 2011), ciclesonide and salbutamol inhalers. The patient under- went open left adrenalectomy and nephrectomy in January 2012, and the histology report was consistent with conventional ACC, Weiss score 9/9, ENSAT Stage 2, R0, Ki-67 index 37% and S-GRAS score 5. At discharge, glucocorticoid replacement therapy was prescribed, and the patient was referred to our department. Physical examination findings were available only from postoperative assessment and revealed overweight (body mass index 27.87 kg/m2) and no signs of androgen excess.

3.2. Long-Term Pharmacological Treatment With Mitotane. After MDT evaluation, adjuvant mitotane was started in June 2012 according to the high-dose saturation regimen along- side hydrocortisone replacement therapy [26]. The patient has been on continuous mitotane treatment from June 2012 to July 2024 (time of last record) but was discontinued for 4 weeks between February and March 2023 for surgical removal of liver metastases and for 2 weeks in July 2024 for markedly high mitotane plasma levels (41.4 mg/L). Over- all, TTR was 65.4% (Table 1) [27]. Overtime, the patient

TABLE 1: Summary of case presentation, mitotane and recurrences management.
FeaturesCase 1Case 2Case 3Case 4
Presentation at diagnosis
SexMaleFemaleMaleMale
Age49523439
Previous smoke habitYesNoNoNo
Previous alcohol habitYesNoNoNo
SymptomsYes (mass effect)Yes (weight gain and virilization)Yes (mass effect)Yes (mass effect)
Hormonal secretionUnknown (likely inactive)Glucocorticoid and androgen excessGlucocorticoid and androgen excessInactive
Clinical examinationNegativeCushing syndromeCushing syndromeNegative
Weiss score598Unknown
Ki 67 index (%)<1374.48-10
ENSAT Stage3232
Resection statusRxR0R0RX
S-GRAS score3523
Mitotane management
Average mitotane plasma level (mg/L±SD)21.10 ±5.4621.88 ±4.4720.06 ±7.1118.42 ± 3.98
Average mitotane dosage (g/day ± SD)2.8±1.12.0±9.82.2 ±8.53.6± 8.1
Years of mitotane12.911.810.67.7
Time below target range (<14 mg/L) (%)9.72.615.012.1
Time in target range (14-20 mg/L) (%)41.765.441.727.3
Time above target range (> 20 mg/L) (%)48.632.043.360.6
Induced hypothyroidismYesYesYesYes
Induced hypogonadismYesNoYesYes
Induced mineralocorticoid insufficiencyYesNoNoYes
Induced hypercholesterolaemiaNoNoNoYes
Neurologic side effects requiring dose adjustmentYesYesNoNo
Gastrointestinal side effects requiring dose adjustmentNoYesYesNo
Recurrences management
Time to first recurrence (months)84420~48
SABR treatments1100
MWA treatments1000
RFA treatments6110
Liver resection (NAR or HH)0451
Lung resection (VAT or wedge)2420
Otherª1011
Disease status at last follow-upFreeFreeFreeFree
Years of follow up15121120

Note: Rx: resection status unknown; R0: tumour fully excised.

Abbreviations: ENSAT, European Network for the Study on Adrenal Tumours; HH, hemi-hepatectomy; MWA, microwave ablation; NAR, non-anatomical resection; RFA, radiofrequency ablation; S-GRAS, Stage, Grade, Resection status, Age, Symptoms; SABR, stereotactic ablative radiotherapy; SD, standard deviation; VAT, video-assisted thoracoscopy.

ªCase 1: Surgical removal of transverse colon metastasis through colonoscopy; Case 2: None; Case 3: Selective excision of retroperitoneal abdominal lymph nodes; Case 4: Surgical excision of local recurrence.

experienced two severe episodes of neurotoxic and gastroin- testinal side effects (diarrhoea, indigestion and slurred speech in August 2012, brain fog in October 2012) and devel- oped mitotane-induced hypothyroidism (January 2017). Mitotane dose was temporary reduced for both toxicity events, with also temporary use of ondansetron for gastroin- testinal (nausea and vomiting) adverse effects. The patient had outstanding compliance with all her medications, including mitotane, which was overall well tolerated after side effect treatments.

3.3. Long-Term Radiological Surveillance and Additional Treatments. Starting from April 2012, the patient underwent a TAP contrast-enhanced CT scan every 3-6 months, along- side with a liver-specific abdomen magnetic resonance imag- ing (LS-AMRI) from September 2015, when she presented her first disease recurrence in the liver, which also was dem- onstrated to be FDG avid at PET-CT. In 12 years of follow- up, the patient had 14 liver recurrences (min-max size: 5-35 mm), for which she had three non-anatomical resec- tions (NAR) of the liver (2015, 2019, 2022), one hemi- hepatectomy (2017) and one SABR (2022), and four lung metastases (min-max size: 5-9 mm) for which she had one RFA (2021), two VATs (both in 2016) and two wedge lung excisions (2018, 2024). The patient remained disease-free at the last surveillance CT scan in January 2025.

4. Case 3

4.1. Case Presentation. In May 2013, a 34-year-old male was diagnosed with adrenocorticotropic hormone-independent Cushing’s Syndrome with androgen excess and associated with a 15 cm left adrenal mass (Figure 2b), which was causing abdom- inal pain (Table 1). The patient had an unremarkable personal and familiar medical history. The patient underwent an open left adrenalectomy in September 2013, and hydrocortisone replace- ment therapy was started. The histology report was consistent with 21 cm× 16 cm × 10 cm conventional ACC, 2.2 kg, Weiss score 8/9, Ki-67 index 4.4%, R0, ENSAT Stage 3 (invasion of surrounding tissue) and S-GRAS score 2.

4.2. Long-Term Pharmacological Treatment With Mitotane. After MDT discussion, adjuvant mitotane was started in November 2013 according to the high-dose saturation regi- men, but due to gastrointestinal side effects, the patient did not exceed 4500 mg daily [26]. The patient has been on continuous mitotane treatment from November 2013 to July 2024 (time of last record) but was discontinued for 2 weeks in September 2015 and June 2016 due to high mito- tane plasma levels. In total, TTR was 41.7% (Table 1) [27]. In 11 years, the patient experienced fatigue with brain fog in December 2013, nausea with episodes of vomiting in January 2014 and developed mitotane-induced hypogonadism in August 2014 and hypothyroidism in August 2019. Mitotane dose was temporary reduced to face neurotoxicity and gas- trointestinal (nausea and vomiting) side effects with tempo- rary administration of ondansetron to treat the latter. Hypogonadism was treated with intramuscular nandrolone in the first place, then testosterone skin gel and levothyroxine

was administrated to correct hypothyroidism. The patient had good compliance to all medications and reported a rela- tively good life quality after side effect treatments.

4.3. Long-Term Radiological Surveillance and Additional Treatments. Starting from November 2013, the patient underwent a TAP contrast-enhanced CT scan every 3-6 months, alongside with a LS-AMRI from August 2015, when the first liver recurrence was detected. From October 2015 to August 2024, the patient experienced 14 liver metas- tases (min-max size: 5-31 mm), treated with one hemi- hepatectomy (2017) and four NARs (2015, 2017 with hemi-hepatectomy, two in 2018), one RFA (2017), two retro- peritoneal lymph node recurrences (24 and 21 mm) which were surgically removed (2022), and two lung metastases (7 and 9 mm) treated by VAT and lung wedge excision (2021 and 2024, respectively). The patient remained disease-free at the last surveillance CT scan in March 2025.

5. Case 4

Unfortunately, we were not able to retrieve Case 4 original documentation reporting exact dates of surgeries and sizes of primary ACC and metastases. Nevertheless, we consider this case to be useful for the purpose of the article.

5.1. Case Presentation. In 2004, a 39-year-old man with an unremarkable medical history was admitted due to right flank pain and underwent a TAP CT scan, which revealed a right adrenal mass. No clinical or biochemical evidence of hormonal excess was documented. He underwent a right adrenalectomy a few weeks after, and histology was consistent with conventional ACC (Weiss score unavailable), ENSAT Stage II, Rx, Ki-67 index 8%-10%, S-GRAS 3. The patient was referred to our department only in January 2017 for suspected second liver metastases, which were ruled out with LS-AMRI.

5.2. Long-Term Pharmacological Treatment With Mitotane. According to the ESE-ENSAT Clinical Practice Guidelines, adjuvant mitotane therapy is recommended in patients with a high-risk of recurrences or incomplete resection [2, 3]. As patients with previous disease recurrences are at higher risk of developing further relapses, mitotane was started in Janu- ary 2017, for example, with a high-dose saturation regimen alongside hydrocortisone replacement therapy [6, 26]. The patient has been on continuous mitotane treatment from January 2017 to July 2024 (time of last record) without inter- ruptions, with a TTR of 27.3% (Table 1) [27]. The patient developed drug-induced hypothyroidism in March 2017, as well as hypercholesterolaemia and hypogonadism in October 2018, and experienced adrenal crisis following mineralocor- ticoid insufficiency in July 2022, treated with levothyroxine, atorvastatin, testosterone gel and fludrocortisone, respec- tively. The patient adhered well to all prescribed medications and reported a satisfactory quality of life following the man- agement of side effects.

5.3. Long-Term Radiological Surveillance and Additional Treatments. Starting from 2004, the patient underwent a CT scan every 3-6 months alongside with an LS-AMRI

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Mitotane started123
RFA① ②① ③① ×2
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Other treatments④ ∗① †③ ‡

FIGURE 3: Longitudinal treatments for Case 1, Case 2, Case 3 and Case 4. 1: Case 1; 2: Case 2; 3: Case 3; @: Case 4. * Surgical excision of local recurrence, *Surgical removal of transverse colon metastasis through colonoscopy, *Selective excision of retroperitoneal abdominal lymph nodes; ACC, adrenocortical carcinoma; RFA, radiofrequency ablation; MWA, microwave ablation; SABR, stereotactic ablative radiotherapy; VAT, video-assisted thoracoscopy.

from December 2016. The patient had a first liver recurrence in 2008, treated with partial hepatectomy, and a local recur- rence surgically treated, followed by radiotherapy to the adre- nal bed (60 Gy in 30 fractions) in 2013. The patient remained disease-free at the last follow-up imaging in September 2024.

6. Continouos Monitoring by Adrenal Specialist Nurse

At our centre, we offer a nurse-led service for continuous clinical and biochemical assessment as well as treatment mon- itoring for patients with ACC. Hereby, patients’ compliance and tolerance to mitotane were assessed monthly for the first 12 months, then quarterly, by an adrenal specialist nurse that kept track of subjective symptoms, physical exam findings, lab test results and plasma mitotane concentrations. In parallel, the nurse provided continuous support to encourage self- management of mitotane-related adrenal insufficiency, such as reinforcing sick-day rules and the use of emergency injection kits. All patients were initiated on hydrocortisone 50 mg/day (20-20-10 mg) concomitantly with mitotane, with subsequent dose adjustments made by the specialist nurse and/or the patients themselves, after appropriate training, according to intercurrent illness or stress-dosing requirements.

7. Discussion

We present four cases of patients with 20-, 15-, 12- and 11- year histories of metastatic ACC, treated with repeated sur- geries, long-term mitotane therapy and multiple locally

mini-invasive tumoral ablations, without EDP or other che- motherapy schemes (Table 1, Figure 3). Within our records, which included 167 patients with ACC from 2004 to 2024 diagnosed at different stages, these four patients are the only that received prolonged mitotane administration with- out EDP (Figure 1), reflecting how unique they are. Our four cases well illustrate that no single clinical or biological marker reliably predicts aggressiveness: for example, Case 2 had a high Ki-67 (37%, adverse) but favourable ENSAT Stage II and R0 resection, whereas Cases 1, 3 and 4 showed low Ki-67 yet had either ENSAT Stage III disease or unknown resection status (both adverse) [25]. To our knowledge, this is the first case series with exhaustive doc- umentation of mitotane plasma levels maintained above 14 mg/L for most of the time, not provided by other reports about metastatic ACC long-term survivors. These cases illustrate the complexity of managing patients with meta- static ACC, emphasising the need for a multidisciplinary approach to assure the best possible care and simulta- neously optimise disease control and quality of life. This case series also highlights the importance of continuous clinical, biochemical and radiological surveillance to allow a timely and comprehensive intervention. In fact, the regu- lar close monitoring allowed early detection of disease recurrences and enabled prompt MDT review and discus- sion, which is known to positively affect overall and PFS in patients with metastatic ACC [28]. Within the MDT, a systemic chemotherapy approach with EDP + mitotane was discussed several times for Case 1, Case 2 and Case 3, although it was never administered in consideration of the

TABLE 2: Patients with metastatic ACC and survival longer than 10 years.
Author (publication year)Age (years)Sex OS (years)SideSize (cm)HormonesSymptomsENSAT stage
Aalderen et al. [20] (1992)NANA 22NANANANANA
Sakamoto et al. [19] (1995)40F 18LNAInactiveNA3
Ilias et al. [15] (2001)39F 14L9CortisolCushing2
24F 16L19CortisolHypertension, amenorrhoea2
Orlando et al. [14] (2003)58M 15NANAInactiveNANA
Meyer et al. [13] (2007)34F 32L17InactiveMass related2
Hamanaka et al. [22] (2008)40F 16L14Inactive, AFPªNANA
Hermsen et al. [16] (2008)53F 12L10CortisolCushing2
38F 17L14InactiveMass related4
34F 18R12CortisolCushing2
49F 18L7InactiveMass related2
31F 25R9AldosteroneHypertension2
22F 28L8CortisolCushing2
Tran et al. [17] (2016)33F 10NA20NANA3
32F 11NANAAndrogensVirilizationNA
49F 12NA13InactiveNA2
42F 12NA9InactiveNA2
55M 12NA10.5InactiveNA4
73F 14NA4.5InactiveNA1
57M 11L4.5NAMass related1
Kostiainen et al. [23] (2019)bNANA >10NANANANANA
Mauda-Havakuk et al. [21] (2021)"NANA 24NANANANANA
Current study34M 11L21CortisolCushing3
52F 12L22CortisolCushing2
49M 15L21Likely inactiveMass related3
39M 20RNAInactiveMass related2

Note: ENSAT stage, where not specified, was calculated according to reported mass diameter and tumour stage.

Abbreviations: AFP, alpha-fetoprotein; ENSAT, European Network for the Study on Adrenal Tumours; F, female; L, left; M, male; NA, not available; OS, overall survival; R, right. aMetastasis secreting AFP.

bOne single patient undergone multiple treatment for metastatic ACC with survival >10 years from a cohort of 43 adult patients with ACC.

“Patient with longest survival among 10 patients reported with metastatic ACC and survival >10 years.

FIGURE 4: Continued.

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FIGURE 4: Mitotane plasma level, mitotane dose and side effect events for Case 1 (a), Case 2 (b), Case 3 (c) and Case 4 (d). ☒ neurological side effects; ☐ gastroin- ☒ Drug-induced hypogonadism; O drug-induced hypothyroidism; A drug-induced mineralocorticoid insufficiency; ☐ testinal side effects; ☒ drug induce hypercholesterolaemia (a) Case 1; (b) Case 2; (c) Case 3; (d) Case 4.

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Therapeutic window (14-20 mg/L)

☒ Neurological side effects

·- Mitotane dose (mg/day) ☒

× ·· Mitotane plasma level (mg/L) ☒

☒ Drug-induced hypercholesterolaemia

☒ Drug-induced hypogonadism

☒ Drug-induced mineralocorticoid insufficiency

☐ Drug-induced hypothyroidism

☐ Gastrointestinal side effects

(d)

slow disease progression and location of tumour manifesta- tions (approachable by surgery or other LT), as well as the patient’s preference. Hence, our MDT opted for a long-term mitotane therapy associated with LTs and resurgeries. Although surgical excisions, RFA, SABR and microwave ablation have indeed contributed to prolong the survival

of the patients (a summary of treatments is in Figure 3 and Table 1), we can speculate that mitotane played an additional role in slowing the progression of the disease, allowing a tailored and local approach at each recurrence. One further possible explanation, though limited to Case 2, could be the lower Ki-67 index observed in three liver

metastases (16%, 25% and 30%) compared with the primi- tive tumour Ki-67 (37%). However, this difference alone is unlikely to fully account for the overall clinical picture.

In the literature, there are few reports of patients (~30 worldwide) with metastatic ACC and 10 or more years of survival [13-23]. Female sex, age > 40 years and left side of primary tumour are overall the most represented features in this cohort of patients (Table 2). However, these features are described as common characteristics of ACC; hence, it is not possible to indicate them as predictors of long-term survival in patients with metastatic ACC [29]. Even therapies and treatments administered to this cohort are strongly hetero- geneous, including mitotane, EDP and other chemotherapy schemes, repeated surgeries and LTs [13-23]. The heteroge- neity in terms of treatment approaches might be due to the more recent development of new mini-invasive treatments [2, 3, 13-23, 30]. Interestingly, among these patients, only few were reported receiving mitotane for more than 5 or 10 years, while the mean mitotane treatment duration of our patients is 10.8 ± 2.2 years (±standard deviation) (Table 1). Two patients reported by Ilias et al. [15] in 2001 received mitotane for 14 and 16 years, although no description of mitotane concentrations was provided. More cases of long- term mitotane administration were reported by Terzolo et al. [7] in 2007. Hereby, within the mitotane treatment group (median duration 29 months, range: 6-164 months), 21 patients received mitotane for 4 years or more, but no further details were given [7]. Differently from the patients reported by Ilias and Terzolo, we used the high-saturation dose regi- men first described in 2013, leading to a quick increase in mitotane plasma levels even above 20 mg/L within the first 3 months, which has been proved to positively impact the PFS [31]. In the following years, we provided continuous support and management of side effects, while making continuous adjustments to mitotane daily dose according to the mito- tane plasma levels, that frequently fluctuated above the tox- icity limit for most of the time (especially for Cases 1-3, Figure 4 and Table 1). This was possible thanks to a patient-centred plan led by a specialist nurse that enabled regular clinical assessments and supported self-management of mitotane-induced adrenal insufficiency through ongoing education and monitoring [32, 33]. This model is supported by successful outcomes in the management of other cancers, where specialist nurses have contributed not only to service coordination and psychological support but also to improved overall survival [34, 35].

Our findings may support the hypothesis that prolonged mitotane therapy may be safely and effectively maintained in selected patients with LTB metastatic ACC, even at plasma concentrations exceeding 20 mg/L and for durations longer than 5 years. It should also be considered that our patients spent most of the treatment period within the mitotane ther- apeutic range, a pattern that may also have contributed to prolonged disease control, as suggested by Puglisi et al. [27]. Although, it is worth to mention that whenever applicable, we arbitrarily reduced mitotane dose when its plasma levels surpassed 35 mg/L. Future research is needed to confirm our findings, which could support the long-term use of the

mitotane and LT in similar cases for which current guide- lines do not provide clear indications [2, 3].

Our study presents some major limitations, such as the lack of quality-of-life systematic evaluation. The latter has been addressed by few articles on and highlighted the com- plexity of assessing quality of life in patients with ACC, as it involves psychological distress caused by both oncological disease burden and hormonal insufficiency or excess [36-38]. Nevertheless, continuous support was offered to our patients and their primary care physicians by means of phone and email contacts to cope with mitotane-related side effects and assure compliance with replacement medications and other treatments. This established pathway allowed patients and their families to engage with our clinical care, in which endocrine nurses played a pivotal role in addressing patients’ concerns, not only by supporting the management of physical symptoms but also by attending to emotional, mental and psychological wellbeing through coaching and signposting to patient associations and support groups.

8. Conclusion

Metastatic ACC is a challenging malignancy that requires continuous monitoring and timely treatment that only a multidisciplinary approach can provide. Few similar cases of metastatic ACC long survivors have been reported world- wide, with no shared characteristic that can be isolated for outcome prediction, while fewer reported mitotane use lon- ger than 5 years. With this case series, we highlight the suc- cessful integration of multiple surgical resections, localised treatments and long-lasting mitotane therapy with highly specialised nurse support to achieve long-term disease con- trol in LTB metastatic ACC. Moreover, we provided real- world evidence supporting the safety of mitotane adminis- tration for more than 5 or even 10 years. Long-term treat- ment with mitotane was associated with relatively good quality of life and manageable drug-related side effects.

Nomenclature

ACC:Adrenocortical carcinoma
CT:Computerised tomography
EDP:Etoposide, cisplatin, doxorubicin
ENSAT:European Network for Study of Adrenal Tumour
FDG-PET-18-fluorodeoxyglucose positron emission
CT:tomography-CT
LS-AMRI:Liver-specific abdomen magnetic reso- nance imaging
LT:Local therapy
LTB:Low tumour burden
MDT:Multidisciplinary team
NAR:Non-anatomical resection
PFS:Progression Free Survival
RFA:Radiofrequency ablation
Rx:Resection status unknown
SABR:Stereotactic ablative radiotherapy
S-GRAS:Stage, Grade, Resection status, Age, Symptoms
TAP:Thorax-abdomen-pelvis
TTR:Time in target range
VAT:Video-assisted thoracoscopy.

Data Availability Statement

The data obtained for this article were collected from the electronic archives of Queen Elizabeth Hospital Birmingham. The longitudinal trends for mitotane plasma levels and daily dose displayed in Figure 3a,b,c,d were retrospectively retrieved from Lysosafe Service (https://lysosafe.clinfile. com). The data that support the findings of this study are available on request from the corresponding author. The data are not publicly available due to privacy or ethical restrictions.

Ethics Statement

Clinical management and monitoring were part of standard clinical care, and hence ethical approval was not required.

Informed written consent for publication of clinical details and/or clinical images was obtained from the patients.

Disclosure

All authors revised and accepted the final version of the manuscript.

Conflicts of Interest

The authors declare no conflicts of interest.

Author Contributions

Lorenzo Tucci and Mengjie Xu share first author position. Alessandro Prete and Cristina L. Ronchi share last author position. All authors contributed to the conception and edit- ing of the manuscript. Mengjie Xu, Lorenzo Tucci and Cris- tina L. Ronchi wrote the initial draft of the article, coordinated with the other authors and prepared the final manuscript. Miriam Asia, Yasir S. Elhassan, Alessandro Prete, Maninder S. Kalkat, Madava Djearaman, Robert P. Sutcliffe and Cristina L. Ronchi contributed to the clinical care of the patient. Kassiani Skordilis provided critical path- ological insights for the interpretation of the results. Alessandro Prete provided expert opinion on the results.

Funding

This work did not receive any specific funding from agency in the public, commercial, or not-for-profit sector. Alessandro Prete receives support from the NIHR Birmingham Biomedi- cal Research Centre at the University Hospitals Birmingham NHS Foundation Trust and the University of Birmingham (Grant NIHR203326).

Acknowledgments

The authors thank the patients for their permission to publish the article and the entire adrenal multidisciplinary team in our hospital for the support in the management of complex cases, including endocrinologists, radiologists, surgeons, interven- tional radiologists, nurses and pathologists. We thank the COST Action CA20122 Harmonisation for supportive networking.

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