Imaging Findings and Treatment Outcomes of Pediatric Rectal Cancers: A Two-Decade Single-Center Retrospective Cohort Study from South India

Abstract

Introduction

Colorectal cancers are rare in the pediatric population.

Objective

The aim of the study was to describe the imaging findings and staging at presentation in pediatric rectal cancers and to assess the final treatment outcome.

Materials and Methods

Imaging findings, demographic data, histopathology type, and treatment outcomes of patients in the age group of 0 to 18 years who underwent imaging for rectal cancer in the past 20 years were obtained.

Results

A total of 18 patients (17 males and 1 female) with a mean (standard deviation [SD]) age of 16.5 (1.3) years and a range of 13 to 18 years were included. On histopathological analysis, 72% (13 cases) had poorly differentiated adenocarcinoma and 83% (15 cases) had either signet ring cells or mucin production. On imaging, 65% (11 cases) were low rectal cancers, 94% had involved circumferential resection margin (CRM), and 29% were positive for extramural vascular invasion (EMVI). Thirty-five percent (n = 6) cases had peritoneal disease. Of the eight patients who were offered neoadjuvant chemotherapy/radiation therapy, 62.5% (n = 5) had inoperable disease on follow-up. Among those who were started on palliative chemotherapy, 38% (n = 3) had disease progression and one patient succumbed to the illness.

Conclusion

Pediatric rectal cancers were found to be more prevalent in late childhood/adolescence, with most patients having poorly differentiated adenocarcinoma with signet and/or mucin production. Peritoneal metastasis and EMVI were common in pediatric rectal cancer at presentation, and treatment outcomes were poor.

 

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Keywords

colorectal cancers - adenocarcinoma - pediatric population - peritoneal metastasis - follow-up

Introduction

Colorectal cancer is the third most common cancer in the world, with age-standardized rates much higher in developed countries than in developing countries.[1] However, colorectal carcinoma is rare in children, accounting for less than 1% of all neoplasms in the pediatric population and is seen in 0.5 cases per 100,000 people younger than 20 years in the United States.[2] [3]

Among the colorectal cancers, rectal cancers are even rarer, resulting in a paucity of data and limitations in understanding the pathogenesis of this disease in children. Most of the literature available is on colorectal cancers, a collective entity, including cancers of the right- and left-sided colon and rectal cancers.

Most studies considering the age group of 0 to 25 years as representing pediatric and young adult populations, which are usually grouped together, have shown that colorectal malignancies in pediatric and young adult populations present with more advanced and aggressive diseases causing higher morbidity and mortality, and poorer outcomes compared with those in older adults.[4] [5] [6] Children with cancers involving the descending colon present with abdominal pain, bleeding per rectum, altered bowel habits, weight loss, and nausea and vomiting, while those with ascending colon cancers present with weight loss, abdominal mass, reduced appetite, blood in stools, and iron deficiency anemia.[7] [8] Compared with the adult population, there is increased incidence of mucinous adenocarcinoma and signet ring cell type in children and adolescents (aged 7–19 years).[9] Colorectal cancers in patients younger than 30 years are shown to be of higher grade with more prevalence of molecular markers like microsatellite stability (MSS)/BRAFV600E genotype, which is associated with poorer prognosis.[10] The differences in tumor biology and more advanced stage at presentation are thought to cause poor treatment outcomes in these patients.[9] [11] Most pediatric colorectal cancers are sporadic, while roughly 10% cases can have an underlying predisposing condition, most common of which are familial adenomatous polyposis, hereditary nonpolyposis colorectal cancer, Turcot's syndrome, Gardner's syndrome, Peutz–Jeghers syndrome, juvenile polyposis of the colon, and ulcerative colitis.[12]

Malignancies arising within 0 to 15 cm from the anal verge are categorized as rectal cancers.[13] Previous studies show that among patients with childhood colorectal cancers, ascending and descending colon cancers constitute approximately 30% cases, while rectal cancers occur in approximately 25% cases.[14] There is little literature describing the role of imaging in the diagnosis and management of pediatric rectal cancers. This study aims to bridge the gap in knowledge about the typical imaging morphology encountered in pediatric rectal cancers, their stage at presentation on imaging, and to assess the final treatment outcome. This would further help us understand the imaging findings of the tumor at presentation and its impact on decisions regarding managing these patients.

 

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Materials and Methods

This was an institutional review board approved (IRB Min No. 16065) retrospective cohort study conducted by the departments of radiology, pediatric surgery, pediatric hemato-oncology, and colorectal surgery unit of a tertiary care referral center.

Patients

Patients were identified using the picture archiving and communication system (PACS; GE Health system, Barrington, IL, United States) database using word search in computed tomography (CT) and magnetic resonance imaging (MRI) modality within the patient age group of 0 to 18 years from January 2000 to December 2023. Consecutive patients who underwent imaging for suspected rectal cancer were included. The final histopathology report of the patients were analyzed, and those with alternate histopathological diagnosis or no histopathological analysis were excluded ([Fig. 1]).

Fig. 1 Flowchart of patients included and excluded from the study. CT, computed tomography; MRI, magnetic resonance imaging; PACS, picture archiving and communication system.

 

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Imaging Protocol

Staging pelvic MRI was performed in most patients using a 1.5- or 3-T MRI scanner. No bowel preparation was given. No spasmolytic medications were used. T2 high-resolution MRI of the pelvis was performed in all patients in sagittal, oblique axial, and oblique coronal planes. Axial diffusion-weighted imaging (DWI) was obtained in 11 patients. Postcontrast imaging was not performed in any of the patients who underwent MRI.

Among the 15 patients who underwent pretreatment MRI, for the T2-weighted imaging, the repetition time (TR) ranged from 3,500 to 7,700 milliseconds, the echo time (TE) ranged from 81 to 108 milliseconds, slice thickness was 3 to 4 mm, and matrix size ranged from 320 × 240 to 800 × 800.

A contrast-enhanced CT of the abdomen and pelvis was done in two patients, using arterial phase imaging of the upper abdomen and venous phase imaging of the abdomen and pelvis. None of the patients had both MRI and CT of the abdomen at the initial evaluation.

 

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Image Interpretation

MRI was reviewed for signal intensity, morphology, location, the longest dimension of the tumor, and pattern of diffusion restriction. Additional assessments included the following: distance of the distal margin of cancer from the anal verge and the anorectal junction; extramural spread; circumferential resection margins (CRMs); extramural vascular invasion (EMVI); extent of infiltration of the anal sphincter complex in terms of involvement of the internal anal sphincter, inter-sphincteric space, external anal sphincter, and ischio-rectal fossa; infiltration of the puborectalis, levator ani, and other skeletal muscles of the pelvis; and infiltration of adjacent structures like the urethra, bladder, prostate, seminal vesicles in males and vagina, uterus, and cervix in females. CRM was defined as the least distance between one of the following: leading margin of tumor, significant node, tumor deposit, EMVI, and adjacent structures such as mesorectal fascia, puborectalis, levator ani muscle, and prostate or seminal vesicles in males and vagina in females.[15] A distance of less than 1 mm was considered as an involved CRM.[15] Lymph nodes were assessed for their location, size, and number. Clinical TNM stages were derived as per the 8th edition of the American Joint Committee on Cancer (AJCC) staging system for all included patients.[16] Lymph node metastases were assessed based on size and morphology criteria. Other relevant images available on PACS were reviewed to document metastases on imaging at staging.

Both patients who underwent CT as initial imaging had T4b disease with involvement of adjacent structures (prostate/seminal vesicle/vagina). Lymph nodal involvement and metastatic disease seen on CT were also documented. Staging was documented based on imaging at presentation. All images were interpreted by radiologists with experience in abdominal imaging ranging from 5 to 15 years.

 

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Data Collection and Statistical Analysis

Demographic data, histopathology type of rectal cancer, treatment decisions made at multidisciplinary team (MDT) meetings, and final treatment outcomes were obtained from the electronic medical records. Technical parameters in MR image acquisition, such as TR, TE, matrix size, slice thickness, and slice gap, were also documented. Imaging findings were reviewed using the PACS. Descriptive statistics were reported as mean and range for continuous variables and frequency with percentage for categorical variables. Telephonic conversation with the family of all the patients who opted to continue treatment elsewhere was attempted to obtain data on final outcome of treatment.

 

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Results

Patient Demographics

A total of 18 patients (17 males, 1 female) with a mean (standard deviation [SD]) age of 16.5 (1.3) years and a range of 13 to 18 years were included for the final analysis. Out of them, 72% (13/18 cases) had poorly differentiated adenocarcinoma, 11% (2/18 cases) had moderately differentiated adenocarcinoma, and 11% (2/18 cases) had well-differentiated adenocarcinoma. In one patient, the grading of histopathology was not available. Further, on histopathological analysis, 83% (15 cases) had either signet ring cells or mucin production, 56% (10 cases) had signet ring cells, 22% (4 cases) had mucinous adenocarcinoma, and 6% (1 case) had both signet ring cells and mucin production. One patient had constitutional mismatch repair disease on genetic analysis; the rest did not have any documented significant molecular/genetic markers. Microsatellite stability testing was available in only one patient in whom the lesion was found to be microsatellite stable.

The initial clinical presentation included bleeding per rectum in 61% (11 cases), altered bowel habits in 50% (9 cases), features of large bowel obstruction in 17% (3 cases), and abdominal pain in 22% (4 cases; [Table 1]). None of the patients had a family history of malignancies. Only one patient had multiple colonic polyps.

Table 1 Summary of symptoms at presentation

Symptom	No. of patients having the symptom at presentation
Bleeding per rectum	11
Altered bowel habits	9
Intestinal obstruction	4
Abdominal pain	4
Mass per rectum	1

 

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Imaging Findings

Pretreatment imaging findings were available in 17 patients, two of whom underwent CT; the rest had MRI for staging. Sixty-five percent (11 cases) patients had low rectal cancer, 24% (4 cases) had mid-rectal cancer, and 6% (1 case) had high rectal cancer. Among the patients who underwent MRI (n = 15), the signal intensity of the tumor on T2-weighted images was intermediate in 73% (11 cases; [Fig. 2A, B]), hyperintense in 20% (3 cases; [Fig. 3]), and mixed-signal intensity in 7% (1 case). DWI was available in 11 patients, and 55% (6 cases of 11) had restricted diffusion within the tumor ([Fig. 3]), while 45% (5 of 11 cases) had no diffusion restriction. CRM was involved in 94% (17/18) and 29% (5/17) were positive for EMVI.

Fig. 2 Magnetic resonance imaging (MRI) of a 15-year-old male patient with moderately differentiated rectal cancer. (A, B) T2-weighted sagittal and axial high-resolution images showing a long segment circumferential wall thickening of the rectum with T2 intermediate signal intensity. (C) T2-weighted axial high-resolution image shows right external iliac lymphadenopathy.

Fig. 3 Magnetic resonance imaging (MRI) of a 17-year-old male patient with poorly differentiated rectal cancer. (A) T2-weighted axial high-resolution image show a long segment hyperintense circumferential wall thickening of the rectum. (B) T2-weighted sagittal image showing longitudinal extent of the tumor. (C, D) High b-value (b-800) diffusion-weighted images and apparent diffusion coefficient (ADC) map predominantly shows facilitated diffusion and diffusion restriction along the mucosa.

Stage on cross-sectional imaging was as follows: 6% (n = 1) had the T2 stage, 24% (n = 4) had the T3c stage, 24% (n = 4) had the T4a stage, and 47% (n = 8) had the T4b stage at presentation. The average tumor length was 7.7 cm, ranging from 2.2 to 15.5 cm. Among the 15 patients with lymph nodal involvement, 12% (2 cases) had N0, 29% (5 cases) had N1, and 59% (10 cases) had N2 nodal stage at presentation; 87% (13 cases) had mesorectal nodes ([Fig. 4B]), 40% (6 cases) had internal iliac nodes, 33% (5 cases) had para-aortic nodes ([Fig. 4D, E]), 20% (3 cases) had common iliac nodes, 13% (2 cases) had presacral nodes, 13% (2 cases) had inferior mesenteric nodes, 13% (2 cases) had external iliac nodes ([Fig. 2C]), and 7% (1 case) had inguinal node involvement. Fifty-three percent (9 cases) had metastatic disease, of which 33% (3 cases of 9) had M1a disease with spread to nonregional nodes ([Table 2]), and 67% (6 cases of 9) had M1b disease with peritoneal spread ([Fig. 5]). A structured report was followed in 53% of the cohort (9 cases) and all had MRI. The standard reporting format was implemented in our center in 2011; thus, those diagnosed prior to this do not have a structured report.

Fig. 4 Magnetic resonance imaging (MRI) of an 18-year-old male patient with poorly differentiated rectal cancer. (A) T2-weighted axial high-resolution image showing intermediate intensity circumferential wall thickening of the rectum. (B) T2-weighted axial high-resolution image showing mesorectal nodes. (C) T2-weighted sagittal image showing longitudinal extent of the tumor with shouldering. (D, E) Spectral attenuated inversion recovery (SPAIR) and T2 axial images of the upper abdomen showing significant para-aortic lymphadenopathy

Fig. 5 (A, B) Follow-up CT of the same patient as in [Fig. 4], showing the development of peritoneal disease with small bowel obstruction.

Table 2 Summary table highlighting the clinico-radiological findings of 17 patients with pediatric rectal cancer

Sl. no.	Age	Gender	Year of diagnosis	Pathology type	Signet cell or mucin production	T	N	M	M site	Imaging modality
1	13	Male	2021	Well-differentiated adenocarcinoma in adenoma	Nil	T2	N1	M0	–	MRI
2	15	Male	2023	Moderately differentiated adenocarcinoma	Nil	T4a	N2	M1a	Nonregional node (external iliac node)	MRI
3	15	Male	2014	Poorly differentiated adenocarcinoma	Signet ring cells	T4a	N2	M1b	Peritoneal	MRI
4	15	Male	2009	Moderately differentiated adenocarcinoma	Mucin production	T4a	N2	M1b	Peritoneal	CT
5	15	Male	2008	Poorly differentiated adenocarcinoma	Signet ring cells	T4b	N0	M0	–	MRI
6	16	Male	2011	Poorly differentiated adenocarcinoma	Signet ring cells	T3c	N2	M1b	Peritoneal	MRI
7	17	Male	2015	Mucinous adenocarcinoma	Mucin production	T4a	N2	M1b	Peritoneal	MRI
8	17	Female	2019	Poorly differentiated adenocarcinoma	Mucin production	T4b	N1	M0	–	MRI
9	17	Male	2014	Poorly differentiated adenocarcinoma	Signet ring cells	T3c	N2	M0	–	MRI
10	17	Male	2011	Poorly differentiated adenocarcinoma	Mucin production	T3c	N0	M0	–	MRI
11	17	Male	2011	Well-differentiated adenocarcinoma	Nil	T4b	N1	M0	–	MRI
12	17	Male	2011	Poorly differentiated adenocarcinoma	Signet ring cells	T4b	N1	M0	–	MRI
13	17	Male	2023	Poorly differentiated adenocarcinoma	Signet ring cells	T4a	N2	M1a	Nonregional node (para-aortic node)	MRI
14	18	Male	2014	Poorly differentiated adenocarcinoma	Signet ring cells	T4b	N2	M1b	Peritoneal	MRI
15	18	Male	2017	Poorly differentiated adenocarcinoma	Both signet ring cells and mucin production	T4b	N2	M1b	Peritoneal	CT
16	18	Male	2016	Poorly differentiated adenocarcinoma	Signet ring cells	T3c	N1	M0	–	MRI
17	18	Male	2021	Poorly differentiated adenocarcinoma	Signet ring cells	T4b	N2	M1a	Nonregional node (para-aortic node)	MRI

Abbreviations: CT, computed tomography; MRI, magnetic resonance imaging.

 

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Multidisciplinary Team Decision-Making

Among the 17 patients included in the study, the pretreatment MDT decision was to offer surgery in 1 case (6%), neoadjuvant chemotherapy/radiation therapy (NACRT) in 8 cases (47%), and palliative chemotherapy in 8 cases (47%; [Table 2]). Surgery was offered to one patient with a staging of T2, N, M0. The patient opted to take treatment elsewhere and is doing well. Most of the patients (12 out of 17) underwent diversion colostomy.

Of the eight patients who were offered NACRT, 62.5% (5 cases) had inoperable disease on follow-up. In one patient, emergent trial dissection was attempted after neoadjuvant chemotherapy due to uncontrolled bleeding from the stoma site; however, the patient succumbed in the post-op period. In two patients, the status after NACRT is unavailable.

Of the eight patients who were started on palliative chemotherapy, 38% (3 cases) had disease progression ([Fig. 5F, G]), one patient succumbed to the illness, and four cases were lost to follow-up.

[Table 2] is a summary of the clinico-radiological features of the17 pediatric rectal cancer patients in our cohort.

 

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Discussion

This study demonstrated a male predominance, with the majority of cases having poorly differentiated adenocarcinoma with signet cells or mucin production. The most common presenting symptoms were bleeding per rectum and altered bowel habits. None of the patients had family history of malignancy. Low rectal cancers accounted to 65% cases and 73% cases showed intermediate signal intensity on T2-weighted imaging. Most patients had advanced disease on imaging at presentation warranting neoadjuvant or palliative therapy.

Pediatric rectal cancers were found to be more prevalent in late childhood/adolescence, as seen in previous studies, with a male preponderance.[2] Most patients were found to have poorly differentiated adenocarcinoma with signet ring cells or mucin production, as observed in previous studies on colorectal malignancies in the pediatric and young adult population.[5] Within the age group of 13 to 18 years included in this study, older patients were noted to have more advanced T-stage disease.

Lymph node involvement was seen in 88% (15 cases) of the patients, and 53% had metastatic disease, in concordance with previous studies showing presentation with advanced disease in patients with colon cancer younger than 25 years. Among the patients who had metastatic disease, 67% had peritoneal metastasis ([Fig. 6]). Previous studies have also noted a higher incidence of peritoneal disease and carcinomatosis in the pediatric population as compared with adult patients with colon cancer.[6]

Fig. 6 Contrast-enhanced computed tomography (CT) of the abdomen of an 18-year-old male patient with poorly differentiated adenocarcinoma. (A) Coronal reconstructed image showing a heterogeneously enhancing mass arising from the rectum with multiple adjacent enlarged mesorectal nodes. (B) Axial image through the pelvis demonstrating circumferential heterogeneously enhancing wall thickening in the rectum. (C) Axial image through the abdomen showing peritoneal disease in the form of nodular thickening along the greater omentum.

On pretreatment imaging evaluation, 63% of cases were found to be low rectal cancers, which are known to be associated with an increased risk of local recurrence and poorer prognosis in adult patients.[8] EMVI positivity, which is a known poor prognostic indicator in rectal cancer patients, was seen in 29% of cases.[15] The structured reporting format was followed in only 53% of the cases. This could be because the cases were distributed over 20 years.

Of the 17 patients who underwent preoperative imaging, only 1 was offered surgery as the primary treatment modality. The remaining 16 cases (94%) had locally advanced or metastatic disease requiring neoadjuvant chemotherapy or palliative chemotherapy. Of these cases, 63% (10 cases) had documented disease progression or succumbed to the illness. This finding is consistent with previous studies demonstrating poorer 5-year overall survival rates and increased mortality due to colorectal cancer in the pediatric population (<21 years of age) in comparison with young adults (22–50 years of age).[5] Details of the treatment provided for these patients are presented in [Table 3].

Table 3 Treatment details of 17 patients with pediatric rectal cancer

Sl. no.	Stage at diagnosis	Surgery	Chemotherapy	RT	Status post NACRT	Palliation	Follow-up
1	T4aN2M1b	Diversion colostomy	FOLFOX (6 cycles)	Nil	Inoperable	Yes	Not available
2	T3N2M1b	Diversion colostomy	FOLFOX(6 cycles)	Nil	NA	Yes	Recurrence in 3 mo; succumbed to illness
3	T4aN2M0	Nil	Nil	Nil	NA	Yes	Not available
4	T2N1M0	Polypectomy	Nil	Nil	NA	Nil	Doing well
5	T4bN1M0	Diversion colostomy	Nil	Nil	Not available	Yes	Not available
6	T4aN2M1b	Diversion colostomy	CAPOX (8 cycles)	Nil	NA	Yes	Not available
7	T3cN2M0	Nil	FOLFIRINOX (4 cycles)	Nil	Inoperable	Yes	Not available
8	T3cN0M0	Diversion colostomy	FOLFOX (3 cycles)	50.4 Gy in 28 fractions with adjuvant capecitabine	Inoperable	Yes	Not available
9	T4bN1M0	Diversion colostomy	FOLFOX (6 cycles)	Nil	Trial dissection due to bleeding from stoma site	Nil	Death during post-op period
10	T4bN2M1b	Ultralow anterior resection done elsewhere	FOLFOX (6 cycles)	Nil	NA	Yes	Not available
11	T4bN1M0	Nil	Nil	Nil	NA	Yes	Not available
12	T4aN2M1a	Diversion colostomy	Nil	30 Gy in 12 fractions with capecitabine	Not available	Yes	Not available
13	T4bN0M0	Diversion colostomy	FOLFOX (6 cycles)	50.4 Gy in 28 fractions	Inoperable	Nil	Death
14	T4bN2M1b	Diversion colostomy	Nil	Nil	NA	Yes	Not available
15	T4bN2M1b	Diversion colostomy	FOLFOX (6 cycles)	Nil	NA	Yes	Death
16	T3cN1M0	Diversion colostomy	FOLFIRINOX (3 cycles)	50.4 Gy in 28 fractions	Inoperable	Yes	Not available
17	T4bN2M1a	Diversion colostomy	CAPOX (4 cycles)	Nil	NA	Yes	Not available

Abbreviations: CAPOX, capecitabine and oxaliplatin; FOLFIRINOX, folinic acid, fluorouracil, irinotecan, and oxaliplatin; FOLFOX, folinic acid, fluorouracil, and oxaliplatin; NA, not applicable; NACRT, neoadjuvant chemotherapy/radiation therapy; RT, radiation therapy.

Although the study includes patients imaged over two decades, most of the patients (15 out of 17) underwent MRI for initial staging of the disease, which is the standard of care followed even at present. CT of the abdomen was performed in patients who had features of bowel obstruction at presentation. The implementation of structured reporting formats in the later decade made it easier to present data at the MDT meets. It also provides meticulous documentation of prognostic factors on imaging, like stations of lymph node involvement and EMVI, making retrospective review of archived data easier.

There is transparent reporting of missing data in the study. The maximum proportion of missing data is observed for the final outcome (70.5%). However, since the final intent of treatment was palliation in all of these patients whose final outcome was not available, it is reasonable to infer that the prognosis of pediatric rectal cancers is dismal.

Through this series, we share our experience of pediatric rectal cancer and highlight the clinico-radiological findings and management practices.

Strengths: The topic is novel and presents a collection of pediatric rectal cancers. It highlights the need for including rectal cancer in the differential diagnosis of patients presenting with the described clinical signs and symptoms in the pediatric population. A major strength of the study is the inclusion of the large number of patients despite the rarity of this pediatric disease.

Generalizability: As this is a rare disease, data from this cohort may be generalized until further research is available.

Future perspectives: A larger cohort will help analyze differences in imaging findings in rectal cancer between the adult and pediatric populations. Further research correlating imaging findings and intraoperative findings can help redefine the criteria for imaging diagnosis of key prognostication factors, like EMVI, nodal involvement, sphincter involvement, and categorization of high, mid-, and low tumors, in the pediatric population and to determine whether they should differ from those being currently used for the adult population.

 

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Limitations

Ours is a tertiary care referral center, and patients travel long distances for evaluation and treatment. Often, those patients with advanced stages of cancer opt for palliative treatment closer to home. This could partly be attributed to the missing data in our series. Quantitative data on survival of most of these patients were hence not available.

 

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Conclusion

Pediatric rectal cancers were found to be more prevalent in late childhood/adolescence, with most patients having poorly differentiated adenocarcinoma with signet and/or mucin production on histology and other poor prognostic features like metastatic disease at presentation with the presence of peritoneal metastasis and EMVI. The majority of the cases underwent neoadjuvant or palliative chemotherapy as the first line of management.

 

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Conflict of Interest

None declared.

Ethics

This study protocol follows the ethical guidelines as per the Declaration of Helinski and was approved by the institutional review board (Silver, Research and Ethics Committee) of the Christian Medical College, Vellore (IRB Min. No. 16065 [RETRO], dated: January 24, 2024). Consent was waived as it is a retrospective study.

Authors' Contributions

R.A.S. contributed to concept design, literature search, data acquisition, data analysis, manuscript preparation.

A.C. contributed to concept design, literature search, data acquisition, data analysis, manuscript editing review.

B.S., A.E., S.G. contributed to data acquisition, data analysis, manuscript editing review.

S.S.R.K.B., R.M., L.G.M. contributed to concept design, literature search, data analysis, manuscript editing review.

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Publication History

Article published online:
11 July 2025