RESEARCH
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Clinical features and treatment options for pediatric adrenal incidentalomas: a retrospective single center study
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Xiaojiang Zhu1, Saisai Liu1, Yimin Yuan1, Nannan Gu1, Jintong Sha1, Yunfei Guo1 and Yongji Deng1*
Abstract
Background The aim of this study was to investigate the clinical features and treatment options for pediatric adrenal incidentalomas(AIs) to guide the diagnosis and treatment of these tumors.
Methods The clinical data of AI patients admitted to our hospital between December 2016 and December 2022 were collected and retrospectively analyzed. All patients were divided into neonatal and nonneonatal groups according to their age at the time of the initial consultation.
Results In the neonatal group, 13 patients were observed and followed up, and the masses completely disappeared in 8 patients and were significantly reduced in size in 5 patients compared with the previous findings. Four patients ultimately underwent surgery, and the postoperative pathological diagnosis was neuroblastoma in three patients and teratoma in one patient. In the nonneonatal group, there were 18 cases of benign tumors, including 9 cases of ganglioneuroma, 2 cases of adrenocortical adenoma, 2 cases of adrenal cyst, 2 cases of teratoma, 1 case of pheochromocytoma, 1 case of nerve sheath tumor, and 1 case of adrenal hemorrhage; and 20 cases of malignant tumors, including 10 cases of neuroblastoma, 9 cases of ganglioneuroblastoma, and 1 case of adrenocortical carcinoma.
Conclusions Neuroblastoma is the most common type of nonneonatal AI, and detailed laboratory investigations and imaging studies are recommended for aggressive evaluation and treatment in this population. The rate of spontaneous regression of AI is high in neonates, and close observation is feasible if the tumor is small, confined to the adrenal gland and has no distant metastasis.
Keywords Adrenal incidentaloma, Children, Retrospective, Clinical analysis
*Correspondence:
Yongji Deng sfsg000@126.com
1Department of Urology, Children’s Hospital of Nanjing Medical University, 72 Guangzhou Road, Nanjing 210008, Jiangsu, China
☒ BMC
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Background
The incidence of adrenal incidentaloma (AI) is increasing due to the increased frequency of imaging and improved imaging sensitivity [1]. AI is relatively common in adults, and several organizations, such as the American Associa- tion of Clinical Endocrinologists/American Association of Endocrine Surgeons and the European Society Endo- crinology, have proposed specific protocols to guide the evaluation, treatment, and follow-up management of AI in adults [2]. Although AI, a nonfunctioning adrenocorti- cal adenoma, is most common in adults, neuroblastoma is the most common incidental tumor of the adrenal gland in children. In addition, in the neonatal period, which is a more complex stage of childhood, the biology of adrenal masses found in this age group is also more specific, and the nature of these masses can range from spontaneous regression to rapid progression to aggressive disease with metastatic dissemination and even death. Given that AI is the most common malignant tumor, the management of AI in children cannot be simply based on the measurements used in adult AI. In this study, we retrospectively analyzed the clinical data of pediatric AI patients in a single center to investigate the clinical char- acteristics and management of AI in children.
Methods
A total of 66 children with adrenal tumors were diag- nosed and treated at the Department of Urology of the Children’s Hospital of Nanjing Medical University from December 2016 to December 2022. A total of 55 cases were detected during physical examination, or the patients were diagnosed and received treatment for dis- eases other than adrenal disease after excluding adrenal tumors detected due to typical clinical manifestations or signs such as centripetal obesity and precocious puberty. Research protocols involving human materials were
| Characteristic | n (%) | |
|---|---|---|
| Sex | Boy | 7(41.2) |
| Girl | 10(58.8) | |
| Site | Left | 5(29.4) |
| Right | 12(70.6) | |
| Discovery Time | Prenatal | 7(41.2) |
| Postnatal | 10(58.8) | |
| Size | $3.1 cm | 6(35.3) |
| ≥3.1 cm | 11(64.7) | |
| $5 cm | 17(100) | |
| ≥5 cm | 0(0) | |
| CT description | Cystic | 8(47.1) |
| Solid-cystic | 5(29.4) | |
| Solid | 4(23.5) | |
| Intervention | Observation | 13(76.5) |
| Surgical treatment | 4(23.5) |
approved by the Medical Ethics Committee of the Chil- dren’s Hospital of Nanjing Medical University. All clini- cal information, radiological diagnosis, laboratory test results, intervention results, and follow-up data were col- lected from the department’s database.
All the children underwent ultrasonography and CT scanning, and 11 children underwent MRI. In addition to routine tests such as blood routine and biochemical indexes, the examination and evaluation of adrenal endo- crine hormones and tumor markers included (1) plasma cortisol and ACTH levels, (2) plasma catecholamine and metabolite determination, (3) plasma renin and plasma aldosterone, (4) urinary vanillylmandelic acid/homova- nillic acid(VMA/HVA), and (5) AFP, CEA, NSE, and CA19-9. Five patients underwent a low-dose dexametha- sone suppression test. Seventeen of the 55 patients were treated with watch-waiting therapy, 4 of the 17 ultimately underwent surgery, 4 of the 38 patients underwent tumor biopsy, and 34 underwent adrenalectomy.
The data were analyzed using Graph Pad Prism 8. The measurement data are expressed as x+sd. The maxi- mum diameter of the tumors, age of the patients with benign and malignant tumors, and maximum diameter of the tumors between the laparoscopic surgery group and the open surgery group were compared using paired t tests, and the percentages of the count data were com- pared using Fisher’s exact test.
Results
In this study, all patients were divided into two groups according to their age at the time of consultation: the neonate group and the nonneonate group.
Neonate group:
There were 7 male and 10 female patients, 7 of whom were diagnosed via prenatal examination and 10 of whom were diagnosed after birth. Five patients were diagnosed with lesions on the left side, 12 patients were diagnosed with lesions on the right side, and the maximal diameters of the masses ranged from 16 to 48 mm. The character- istics of the AIs in the neonate group are presented in Table 1.
Among the 17 patients, 8 had cystic masses with a max- imum diameter of 16_48 mm, 5 had cystic-solid masses with a maximum diameter of 33_ 39 mm, and 4 had solid masses with a maximum diameter of 18_45 mm. Two patients with solid adrenal gland masses suggested by CT scan had obvious elevations in serum NSE and maximum diameters of 44 and 45 mm, respectively. These patients underwent adrenal tumor resection, and the pathol- ogy diagnosed that they had neuroblastomas(NB). In one patient, the right adrenal gland was 26×24×27 mm in size with slightly elevated echogenicity at 38 weeks after delivery, and the mass increased to a size of 40×39×29 mm according to the 1-month postnatal
review. MRI suggested that the adrenal gland tumor was associated with liver metastasis, and the pathology of the tumor suggested that it was NB associated with liver metastasis after surgical resection (stage 4 S, FH). One child was found to have 25×24×14 mm cystic echoes in the left adrenal region during an obstetric examination, and ultrasound revealed 18×11 mm cystic solid echoes 5 days after birth. Ultrasound revealed 24×15 mm cys- tic solid echoes at 2 months. Serum NSE and urinary VMA were normal, and the tumor was excised due to the request of the parents. Pathology suggested a teratoma in the postoperative period. A total of 13 children did not receive surgical treatment or regular review via ultra- sound, serum NSE or urine VMA. The follow-up time ranged from 1 to 31 months, with a mean of 9.04±7.61 months. Eight patients had complete swelling, and 5 patients were significantly younger than the previous patients. Nonneonate group:
There were 24 male and 14 female patients in the non- neonate group; 24 patients had lesions on the left side, 14 patients had lesions on the right side, and the maxi- mal diameters of the masses ranged from 17 to 131 mm. Most of these tumors were found during routine physical examinations or incidentally during examinations per- formed for various complaints, such as gastrointestinal symptoms, respiratory symptoms, or other related condi- tions. As shown in Table 2, abdominal pain was the most common risk factor (44.7%) for clinical onset, followed by routine physical examination and examination for respiratory symptoms.
Among the 38 patients, 10 had NBs with maximum diameters ranging from 20 to 131 mm, 9 had ganglion cell neuroblastomas with maximum diameters ranging from 33.6 to 92 mm, 9 had ganglion cell neuromas with maxi- mum diameters ranging from 33 to 62 mm, 2 had adre- nal adenomas with maximum diameters ranging from 17 to 70 mm, 1 had a cortical carcinoma with a maximum diameter of 72 mm, 2 had adrenal cysts with maximum diameters ranging from 26 to 29 mm, 2 had mature tera- tomas with maximum diameters of 34 and 40 mm, 1 had a pheochromocytoma with a diameter of 29 mm, 1 had a nerve sheath tumor with a diameter of 29 mm, and 1 patient with postoperative pathological confirmation of partial hemorrhagic necrosis of the adrenal gland had focal calcification with a maximum diameter of 25 mm (Table 3).
The mean age of children with malignant tumors was significantly lower than that of children with benign tumors (57.95±37.20 months vs. 105.0±23.85 months; t=4.582, P<0.0001). The maximum diameter of malig- nant tumors ranged from 20 to 131 mm, while that of benign tumors ranged from 17 to 72 mm, and the maxi- mum diameter of malignant tumors was significantly greater than that of benign tumors (65.15±27.61 mm v
| Clinical presentation | n (%) |
|---|---|
| Abdominal pain | 17(44.7) |
| Medical checkup | 7(18.4) |
| Fever | 4(10.5) |
| Pneumonia | 3(7.9) |
| Cough | 1(2.6) |
| Diarrhea | 1(2.6) |
| Vomiting | 1(2.6) |
| Urinary tract infection | 1(2.6) |
| Low back pain | 1(2.6) |
| Hodgkin's lymphoma | 1(2.6) |
| Vaginal bleeding | 1(2.6) |
| Clinical diagnosis | No. | Size <40 mm | Size 40~60mm | Size >60 mm |
|---|---|---|---|---|
| Neuroblastoma | 10 | 1 | 4 | 5 |
| Ganglioneuroblastoma | 9 | 3 | 3 | 3 |
| Ganglioneuromas | 9 | 0 | 8 | 1 |
| Adrenocortical | 2 | 1 | 0 | 1 |
| adenoma | ||||
| Adrenocortical | 1 | 0 | 0 | 1 |
| carcinoma | ||||
| Cyst | 2 | 2 | 0 | 0 |
| Mature teratoma | 2 | 0 | 2 | 0 |
| Pheochromocytoma | 1 | 1 | 0 | 0 |
| Nerve sheath tumor | 1 | 1 | 0 | 0 |
| Hematoma | 1 | 1 | 0 | 0 |
37.59±12.98 mm; t=3.863, P=0.0004). Four biopsies, 5 laparoscopic adrenal tumor resections and 11 open adrenal tumor resections were performed for malig- nant tumors, and 16 laparoscopic adrenal tumor resec- tions and 2 open procedures were performed for benign tumors. The maximum diameter of the tumors ranged from 17 to 62 mm in 21 children who underwent laparo- scopic surgery and from 34 to 99 mm in 13 children who underwent open resection; there was a statistically signif- icant difference in the maximum diameter of the tumors between the laparoscopic surgery group and the open surgery group (35.63±10.36 mm v 66.42±20.60 mm; t=5.798, P<0.0001).
Of the 42 children with definitive pathologic diag- noses at surgery, 23 had malignant tumors, and 19 had benign tumors. There were 15 malignant tumors with calcification on imaging and 5 benign tumors. The per- centage of malignant tumors with calcifications in was significantly greater than that of benign tumors (65.22% v 26.32%; P=0.0157). In the present study, all the chil- dren underwent CT, and 31 patients had postoperative pathological confirmation of NB. A total of 26 patients were considered to have neurogenic tumors according
to preoperative CT, for a diagnostic compliance rate of 83.97%. Three children were considered to have cortical adenomas by preoperative CT, and 1 was ultimately diag- nosed by postoperative pathology, for a diagnostic com- pliance rate of 33.33%. For 4 patients with teratomas and adrenal cysts, the CT findings were consistent with the postoperative pathology. According to our research, NB 9-110HU, GNB 15-39HU, GB 19-38HU, ACA 8HU, adre- nal cyst 8HU, and cellular achwannoma 17HU.
Discussion
According to the clinical practice guidelines developed by the European Society of Endocrinology and European Network for the Study of Adrenal Tumors, AI is an adre- nal mass incidentally detected on imaging not performed for a suspected adrenal disease [3]. The prevalence of AI is approximately 4%, and the incidence increases with age [4]. Most adult AIs are nonfunctioning benign adrenal adenomas (up to 75%), while others include functioning adrenal adenomas, pheochromocytomas, and adrenocor- tical carcinomas [5]. In contrast to the disease spectrum of adult AI cases, NB is the most common tumor type among children with AI, and benign cortical adenomas, which account for the vast majority of adult AI, account- ing for less than 0.5% of cases in children [6]. According to several guidelines, urgent assessment of an AI is rec- ommended in children because of a greater likelihood of malignancy [3, 7].
When an adult patient is initially diagnosed with AI, it should be clear whether the lesion is malignant and functional. In several studies, the use of noncontrast CT has been recommended as the initial imaging method for adrenal incidentaloma; a CT attenuation value≤10 HU is used as the diagnostic criterion for benign ade- nomas; and these methods have a specificity of 71-79% and a sensitivity of 96-98% [8, 9]. A CT scan of tumors with diameters greater than 4 to 6 cm, irregular margins or heterogeneity, a CT attenuation value greater than 10 HU, or a relative contrast enhancement washout of less than 40% 10 or 15 min after administration of contrast media on enhanced CT is considered to indicate poten- tial malignancy [7]. As the most common AI in children, NB often appears as a soft tissue mass with uneven den- sity on CT, often accompanied by high-density calcified shadows, low-density cystic lesions or necrotic areas. CT scans can easily identify more typical NBs, and for those AIs that do not show typical calcified shadows on CT, it is sometimes difficult to differentiate neurogenic tumors from adenomas. In these patients, except for the 1 patient with adrenal cysts who had a CT value of 8 HU, very few of the remaining AI patients had a CT value less than 10 HU. Therefore, the CT value cannot be used simply as a criterion for determining the benign or malignant nature of AI, and additional imaging examinations, such as CT
enhancement, MRI, and FDG-PET if necessary, should be performed immediately for AI in children.
Initial hormonal testing is also needed for functional assessment, and aldosterone secretion should also be assessed when the patient is hypertensive or hypokale- mic [7]. Patients with AI who are not suitable for surgery should be observed during the follow-up period, and if abnormal adrenal secretion is detected or suggestive of malignancy during this period, prompt adrenal tumor resection is needed. For adult patients with AI, laparo- scopic adrenal tumor resection is one of the most effec- tive treatments that has comparative advantages in terms of hospitalization time and postoperative recovery speed; however, there is still some controversy over whether to perform laparoscopic surgery for some malignant tumors with large diameters, especially adrenocortical carci- nomas, and some studies have shown that patients who undergo laparoscopic surgery are more prone to perito- neal seeding of tumors [10].
The maximum diameter of an adult AI is a predictor of malignancy, and a study by the National Italian Study Group on Adrenal Tumors, which included 887 AIs, showed that adrenocortical carcinoma was significantly correlated with the size of the mass, and the sensitivity of detecting adrenocortical carcinoma with a threshold of 4 cm was 93% [11]. According to the National Insti- tutes of Health, patients with tumors larger than 6 cm should undergo surgical treatment, while patients with tumors smaller than 4 cm should closely monitored; for patients with tumors between 4 and 6 cm, the choice of whether to be monitored or surgically treated can be based on other indicators, such as imaging [12]. A diam- eter of 4 cm is not the initial threshold for determining the benign or malignant nature of a mass in children.
In a study of 26 children with AI, Masiakos et al. reported that 9 of 18 benign lesions had a maximal diam- eter less than 5 cm, 4 of 8 malignant lesions had a maxi- mal diameters less than 5 cm, and 2 had a diameter less than 3 cm. The mean maximal diameter of benign lesions was 4.2+1.7 cm, whereas the mean maximum diameter of malignant lesions was 5.1+2.3 cm. There was no sta- tistically significant difference between the two compari- sons; therefore, this study concluded that children with AI diameters less than 5 cm cannot be treated expec- tantly [6]. Additionally, this study revealed that malig- nant lesions occurred significantly more frequently than benign lesions in younger children (mean age 1.7±1.8 years v 7.8±5.9 years; P=0.02).
In the nonneonatal group of this study, 20 patients with malignant tumors had maximum diameters rang- ing from 20 to 131 mm, 10 had malignant tumors larger than 60 mm, and 3 had tumors smaller than 40 cm; 18 patients with benign tumors had maximum diameters ranging from 17 to 70 mm, 5 had diameters ranging from
40 to 60 mm, and 5 had diameters larger than 60 mm. Therefore, it is not recommended to use the size of the largest diameter of the tumor to decide whether to wait and observe or intervene surgically for children with AI. Instead, it is necessary to consider the age of the child; laboratory test results, such as whether the tumor indices are elevated or not; whether the tumor has an endocrine function; etc .; and imaging test results to make compre- hensive judgments and decisions. Preoperative aggressive evaluation and prompt surgical treatment are recom- mended for nonneonatal pediatric AI patients.
Adrenal hematoma and NBs are the most common types of adrenal area masses in children, while pheochro- mocytoma, adrenal cyst, and teratoma are rarer masses [13]. In clinical practice, adrenal hematoma and NB are sometimes difficult to differentiate, especially when adre- nal masses are found during the prenatal examination and neonatal period, and such children need to be man- aged with caution. The Children’s Oncology Group (COG ANBL00B1) implemented the watchful waiting treatment for children under 6 months of age with a solid adrenal mass<3.1 cm in diameter (or a cystic mass<5 cm) with- out evidence of distant metastasis, and if there is a>50% increase in the adrenal mass volume, there is no return to the baseline VMA or HVA levels, or if there is a>50% increase in the urinary VMA/HVA ratio or an inversion, surgical resection should be performed [14]. Eighty-three children in this study underwent expectant observation, 16 of whom ultimately underwent surgical resection (8 with INSS stage 1 NB, 1 with INSS stage 2B, 1 with INSS stage 4 S, 2 with low-grade adrenocortical neo- plasm, 2 with adrenal hemorrhage, and 2 with extralo- bar pulmonary sequestration). Most of the children who were observed had a reduced adrenal mass volume. Of the 56 patients who completed the final 90 weeks of expectant observation, 27 (48%) had no residual mass, 13 (23%) had a residual mass volume of 0-1 ml, 8 (14%) had a mass volume of 1-2 ml, and 8 (14%) had a volume of >2 ml; ultimately, 71% of the residual masses had a vol- ume≤1 ml and 86% had a residual volume≤2 ml. In this study, a total of 16 patients were included in the watchful waiting treatment group; 3 patients underwent surgical treatment during the follow-up period, and 13 patients ultimately completed watchful waiting treatment. After 1-31 months of follow-up, 8 patients’ swelling com- pletely disappeared, and 5 patients’ swelling significantly decreased. After strict screening for indications and thor- ough follow-up review, AIs in the neonatal period can be subjected to watchful waiting treatment, and satisfactory results can be achieved.
For benign adrenal tumors, laparoscopic surgery is superior to open surgery in terms of successful resec- tion, whereas the feasibility of minimally invasive sur- gery for AI with preoperative suspicion of malignancy is
controversial. The European Cooperative Study Group for Pediatric Rare Tumors recommends that minimally invasive surgery be considered only for early childhood tumors and should be limited to small, localized tumors; additionally, imaging should suggest no invasion of sur- rounding tissue structures or lymph nodes; and this strategy requires surgeons with extensive experience in oncologic and adrenal surgery [15]. NB is the most com- mon pediatric AI, and open tumor resection remains the mainstay of treatment. For small, early tumors without evidence of invasion on preoperative examination, lapa- roscopic resection may be considered if the principles of oncologic surgery can be adhered to. If the patient responds to chemotherapy, the decision to perform lapa- roscopic tumor resection can also be re-evaluated after chemotherapy. According to the current study, the recur- rence and mortality rates of laparoscopic surgery are comparable to those of open surgery [16, 17]. The relative contraindications for laparoscopic NB resection include a tumor diameter greater than 6 cm, venous dilatation, and the involvement of adjacent organs or blood vessels [18]. Patients who undergo open adrenalectomy have higher overall survival and recurrence-free survival rates than patients who undergo laparoscopic adrenalectomy [19]. Open adrenalectomy remains the gold standard for surgi- cal resection of adrenocortical carcinoma, whereas lapa- roscopic adrenalectomy should be reserved for highly selected patients and performed by surgeons with appro- priate expertise [20].
Cortical tumors are particularly rare among children with AIs and are sometimes not clearly distinguishable from neurogenic tumors on preoperative imaging; in such patients, the presence of subclinical Cushing’s syn- drome needs to be carefully evaluated preoperatively; otherwise, a perioperative adrenal crisis may occur [21]. In patients in whom the possibility of an adrenocortical tumor was considered preoperatively, the assessment for subclinical Cushing’s syndrome mainly involved assess- ing the serum dehydroepiandrosterone sulfate level and performing an overnight dexamethasone suppression test.
A procedure for evaluating pediatric AI is shown in Fig. 1. Imaging is the first step in the evaluation of AI in children. CT can be used to clarify the nature of most tumors. MRI can be used to evaluate imaging risk fac- tors (IDRFs) for NB. Bone marrow cytomorphology is recommended for all children with AI, along with micro- scopic residual neuroblastoma testing and further bone scanning if the bone marrow examination is positive. In addition, serum tumor marker levels and other relevant tests should be performed, and hormone levels should be evaluated. If adrenal adenomas cannot be completely excluded during the preoperative examination, a 1 mg overnight dexamethasone suppression test should be
Pediatric adrenal incidentaloma
CT scan (abdomen, chest, head) MRI, Bone marrow cell morphology (Isotope bone scan when necessary)
Tumor markers: NSE, AFP, CEA, CA19-9 Hormonal evaluation: cortisol, ACTH, plasma-free metanephrines and normetanephrines, PAC/PRA, DST overnight*
a solid adrenal mass <3.1 cm in diameter (or a cystic mass <5 cm) without evidence of distant metastasis in neonate
YES
NO
NO
Observation
Tumor progression
Surgery
Biopsy/Chemotherapy
performed to exclude subclinical Cushing’s syndrome. In patients with hypertensive hypokalemia, the presence of aldosteronism should be evaluated by testing plasma aldosterone concentrations and plasma renin activ- ity. Adrenal masses found in the neonatal period can be observed if the tumor is small, confined to the adre- nal gland and shows no evidence of distant metastasis, while tumors that increase significantly in size during the follow-up period or that are associated with persis- tently elevated tumor markers require aggressive surgical treatment.
Abbreviations
| CT | computed tomographic |
| MRI | magnetic resonance imaging |
| ACTH | adrenocorticotropic hormone |
| VMA | vanillylmandelic acid |
| HVA | homovanillic Acid |
| AFP | alpha-fetoprotein |
| CEA | carcinoembryonic antigen |
| NSE | neuron-specific enolase |
| CA19-9 | cancerantigen 19-9 |
| FH | favorable histology |
| HU | Hounsfiled Unit |
| COG | Children's Oncology Group |
| INSS | International Neuroblastoma Staging System |
Acknowledgements
We would like to express our deepest gratitude to all the patients and their parents who participated in this study. Their patience and cooperation were instrumental to the success of this research. We thank our colleagues in the Department of Radiology for their invaluable contributions in diagnosing and monitoring the progression of adrenal incidentalomas. We sincerely appreciate the hard work of the pathologists in diagnosing and classifying tumors, which laid the foundation for our study. Finally, we would like to thank our institution for providing the necessary resources and an enabling environment to conduct this research.
Author contributions
X.J.Z. and Y.J.D designed the study; S.S.L., Y.M.Y., N.N.G., and J.T.S. carried out the study and collected important data; XJ.Z. analysed data and wrote the manuscript; Y.F.G. and Y.J.D.gave us a lot of very good advices and technical support; All authors read and approved the final manuscript.
Funding
Not applicable.
Data availability
The datasets analyzed during the current study are not public, but are available from the corresponding author on reasonable request.
Declarations
Competing interests
The authors declare no competing interests.
Ethics approval and consent to participate
Ethics approval for this study was granted by the Ethics Committee of Children’s Hospital of Nanjing Medical University. Informed written consent was obtained from all the guardians of the children and we co-signed the informed consent form with their parents before the study. We confirmed
(2024) 24:186
that all methods were performed in accordance with relevant guidelines and regulations.
Conflict of interest There are no conflicts of interest.
Received: 16 January 2024 / Accepted: 26 February 2024 Published online: 16 March 2024
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