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SOCIÉTÉ INTERNATIONALE D’ONCOLOGIE PÉDIATRIQUE SKOP INTERNATIONAL SOCIETY OF PAEDIATRIC ONCOLOGY

aspho The American Society of Pediatric Hematology/Oncology

Erythrocytosis as the initial presentation of pediatric adrenocortical carcinoma: A case report and review of the literature

To the Editor:

Erythrocytosis refers to an increase in red blood cells (RBC) in circulation.1 Erythrocytosis caused by functional adrenocortical car- cinoma (ACC) with predominant androgen secretion in children is extremely rare in clinical practice. A previous case has been reported,2 and this case is the second report of pediatric ACC, with erythrocytosis as the initial presentation.

A 20-month-old female presented with erythrocytosis as an inci- dental finding. Physical examination revealed a ruddy complexion and an enlarged clitoris resembling a penis (Figure 1A). She had no past medical history or family history of genetic disorders. Laboratory tests showed RBC count 7.17 x 1012/L, hemoglobin 192 g/L, and hema- tocrit 58.5%. She was admitted to the hematology department, and abdominal ultrasound revealed a heterogeneous mass in the right adrenal region, measuring 5.6x5.1×5.8 cm. Positron emission tomog- raphy computed tomography (PET-CT) examination suggested a right adrenal mass, measuring 5.7x4.3x4.6 cm, with a maximum standard- ized uptake value (SUVmax) of 7.6 (Figure 1C) and breast development (Figure 1D). Further hormonal tests showed an elevated androgen level of 146.27 ng/dL and prolactin (PRL) level of 45.75 ng/ml. The initial diagnosis was secondary erythrocytosis with a right adrenal mass of unknown etiology. The patient was referred to our department for sur- gical treatment, and intraoperative exploration revealed an upward diaphragm invasion. Right adrenalectomy was performed without pre- serving the affected adrenal gland. Postoperative pathology reported ACC with a Weiss score of 5,3,4 ARAR0332 stage II5 (Figure 1F-H). Further, next-generation sequencing (NGS) on germline and tumor material revealed no TP53 gene mutations. The patient recovered well postoperatively, with normal hormone levels and a decrease in RBC count, hemoglobin, and hematocrit (Table S1). She was transferred to the department of medical oncology for further treatment. The key- words “adrenocortical carcinoma” and “erythrocytosis” were searched through PubMed, and three relevant papers were retrieved, all of which were case reports2,6,7 (Table 1).

ACC is a highly invasive and poor-prognosis malignant tumor.8 Chil- dren and adolescents represent the second peak incidence group, with an annual incidence rate of 0.5-2 cases per million.9,10 The clinical man- ifestations are mainly precocious puberty and Cushing’s syndrome, while secondary erythrocytosis is a rare clinical presentation. This case

is the second report of ACC in a young child with erythrocytosis as the initial presentation. In this, the youngest case, the first presenta- tion was erythrocytosis. ACC originates in the adrenal cortex and is often associated with elevated levels of sex hormones; the type of ele- vated hormones varying from patient to patient.11 The physiological functions of androgens include two main areas: reproduction, which includes promoting the formation of sexual organs, and the develop- ment of sexual characteristics. In terms of metabolism, these include inhibiting protein breakdown, promoting bone growth and develop- ment, and promoting bone marrow hematopoiesis and erythropoietin (EPO) production.12 PRL promotes breast development. In this case, androgen and PRL levels were predominantly elevated, and the effects of these hormones explain the physiopathology of erythrocytosis, vul- var masculinization, and breast development in this child. On the first postoperative day, the child’s sex hormone levels had returned to nor- mal, and the RBC count and hemoglobin gradually decreased to normal on regular postoperative reviews (Table S1), thus showing a correlation between the tumor, hormone levels, and clinical findings. Both cases 2 and 3 in the literature review had elevated androgen levels associ- ated with erythrocytosis. Case 1 reviewed in the literature had normal androgen levels and elevated EPO levels, leading the authors to con- sider local renal hypoxia due to massive tumor compression, resulting in impaired renal microcirculation or constriction of the renal arter- ies or veins, to be the cause of erythrocytosis due to increased EPO production.

Previous literature has reported that mutations in the TP53 gene are more common in pediatric ACC, accounting for approximately 50% of cases, and are associated with poor clinical prognosis.13,14 Fortu- nately, postoperative NGS testing in this child did not detect TP53 mutations. Results from the Children’s Oncology Group ARAR0332 protocol show a 94.7% 5-year survival rate for children with stage III ACC.5 Other reports have found that children with androgen-secreting predominant functional ACC have a better prognosis, mainly due to the androgen-promoting role in metabolic regulation.15-17 Our patient had a predominantly androgenic hormonal abnormality, was operated on to achieve complete resection, had ARAR0332 stage II, had no evidence of lymph node or distant metastases, had a negative NGS test for TP53, and received regular chemotherapy, and thus has a good long-term prognosis.

Yu Lin and Wei Yang contributed equally to this work.

FIGURE 1 Clinical and pathological picture data of the child in this case. The female has abnormal vulvar development with an enlarged clitoris resembling a penis (A). Enhanced computed tomography (CT) showed a right adrenal gland occupancy with mixed density and uneven enhancement, with CT values of 33-122 HU. The tumor was closely adjacent to the posterior border of the right lobe of liver (B). Positron emission tomography (PET)-CT revealed a soft tissue mass measuring 5.7 x 4.3 x 4.6 cm in the right adrenal region, which was inadequately defined by the diaphragm, the right posterior lobe of the liver, and the upper pole of the right kidney, with unevenly increased FDG uptake, maximum standardized uptake value (SUVmax) 7.6 (C). PET-CT shows mild breast development (D). The gross postoperative appearance of the tumor (E). HE-stained images at 100x magnification (F), 200x magnification (G), and 400x magnification (H). The Weiss score of 5 includes the following: nuclear anisotropy, nuclear division index ≥5/50 HPF, clear cells <25% of all cells, tumor necrosis, and venous invasion.

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TABLE 1 Clinical information on three patients with ACC with erythrocytosis reported in the previous literature.
CasesAuthorsYear reportedAge (years)Maximum tumor diameter (cm)Types of hormones abnormally elevatedEPO levelRBC levelHGB levelTreatmentSurvival periodPrognosis
1Oka et al619966219Renin AldosteroneElevatedElevatedElevatedSurgery3.5Death, liver and lung metastases
2Radi et al720195810.4Cortisol AndrogenElevatedSurgery Chemotherapy
3Cannavò et al220191414Androgens ProgesteroneElevatedElevatedSurgery18Alive

Abbreviations: ACC, adrenocortical carcinoma; EPO, erythropoietin; RBC, red blood cells.

In conclusion, when erythrocytosis is found on incidental exami- nation in children, the possibility of ACC should be considered after excluding hematological-related diseases. Although adrenal cancer is rare in clinical practice, it is a malignant tumor that is highly inva- sive and has a poor prognosis in children with advanced disease. Early detection may improve its long-term prognosis.

DATA AVAILABILITY STATEMENT

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.

ACKNOWLEDGMENTSYu Lin1
Wei Yang1
The patient's parents gave written consent to the release of the medi-Hong Qin1
cal history and images. We are grateful to the patient and the familiesHaiyan Cheng1
of the patients who have made this research possible. We also thankShen Yang1 (D
Genetron Health Inc. that supported genomic studies.Qinghua Ren1
Shuangtao Xiao2
CONFLICT OF INTEREST STATEMENTLianyuan Yu3
The authors declare no conflicts of interest.Huanmin Wang İD

1 Department of Oncology Surgery, Beijing Children’s Hospital, Capital Medical University, National Center for Children’s Health, Beijing, China 2 Department of Thoracic Surgery, Beijing Children’s Hospital, Capital Medical University, National Center for Children’s Health, Beijing, China 3 Department of Pathology, Beijing Children’s Hospital, Capital Medical University, National Center for Children’s Health, Beijing, China

Correspondence

Huanmin Wang, Department of Oncology Surgery, Beijing Children’s Hospital, Capital Medical University, National Center for Children’s Health, Beijing 100045, China.

Email: wanghuanmin@bch.com.cn

ORCID

Shen Yang (D https://orcid.org/0000-0002-2029-3977

Huanmin Wang D https://orcid.org/0000-0001-6769-9643

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