ORIGINAL ARTICLE
Research Landscape on Adrenocortical Carcinoma Over Four Decades
Tun-Pang Chu1,2,3 | Chi-Yu Kuo1,2 | Shih-Ping Cheng1,2,3,4 [D
1Department of Surgery, Mackay Memorial Hospital, Taipei, Taiwan | 2Department of Medicine, School of Medicine, MacKay Medical College, New Taipei City, Taiwan | 3Institute of Biomedical Sciences, Mackay Medical College, New Taipei City, Taiwan | 4Department of Pharmacology, School of Medicine, College of Medicine, Taipei Medical University, Taipei, Taiwan
Correspondence: Shih-Ping Cheng (surg.mmh@gmail.com)
Received: 20 February 2025 | Revised: 19 April 2025 | Accepted: 8 May 2025
Keywords: adrenocortical carcinoma | bibliometric analysis | Scopus | web of science
ABSTRACT
Objectives: Adrenocortical carcinoma is a rare but devastating endocrine malignancy. Our objective was to outline the aca- demic output and trends through bibliometric analysis.
Methods: We searched the Web of Science Core Collection, PubMed, and Scopus to retrieve publications related to adrenocor- tical carcinoma using the structured three-step PRISMA methodology. Co-authorship and co-occurrence analyses were con- ducted to visualize collaborative and thematic networks.
Results: This overview comprises 5507 documents. The number of publications on adrenocortical carcinoma has consistently increased over time. Most of these publications originate from North America and Europe. The co-occurrence map identified several major research clusters, with immunotherapy and targeted therapy emerging as new treatment modalities in recent years. The number of co-authoring institutions per publication was positively correlated with citation counts (Spearman’s rank coefficient =0.17, p<0.0001).
Conclusions: This literature analysis provides an overview of the current research landscape on adrenocortical carcinoma, highlighting geographical disparities. International and interdisciplinary collaboration may enhance productivity and foster scientific progress.
1 Introduction
Adrenocortical carcinoma is an extremely rare but aggres- sive endocrine malignancy that arises from the cortex of the adrenal gland. According to an analysis of the Surveillance, Epidemiology, and End Results database, patient outcomes have remained unchanged over 40years, with a 5-year cancer- specific survival rate of 38% [1]. In a single-center study, the median survival time was only 15.5 months [2]. These findings highlight the need for progress in the diagnosis and treatment of adrenocortical carcinoma. Alarmingly, some reports suggest that the incidence of this cancer is increasing. In Denmark, the
incidence rates for women rose from 2003 to 2019, with a ratio of 1.06 [3]. In Taiwan, we recently demonstrated that the average annual percent change in age-standardized incidence rates was 6.44% for women and 5.04% for men [4]. Therefore, it is essential to provide a synopsis of the current scientific landscape to guide relevant research and address the burden of this disease.
Bibliometrics is a quantitative method for content and citation analysis used to track academic output and impact [5]. Given the rarity of this neoplasm, literature on adrenocortical carcinoma is relatively scarce. To date, no bibliometric analysis has been con- ducted on this topic to identify strengths and gaps in research and
@ 2025 The Japanese Urological Association.
provide direction for future studies. In this study, our objective was to outline the research hotspots over the past 40years.
2 Methods
We searched the Web of Science Core Collection, PubMed, and Scopus using the term “adrenocortical carcinoma,” limiting the results to review and research articles. The publication timeframe was restricted to 1984-2024. Full records and cited references were retrieved without language restrictions. To avoid inconsis- tencies from database updates, literature searches and data col- lection were completed on April 6, 2025. Two investigators (Chu and Cheng) independently conducted the search and resolved any discrepancies through discussion to reach a consensus.
The Preferred Reporting Items for Systematic Reviews and Meta- Analyses (PRISMA) methodology was used for paper selection, following a structured three-step process (Figure 1). First, rel- evant data were identified and extracted from Web of Science, PubMed, and Scopus. After removing duplicate records, the second step involved excluding certain document types, such as conference papers, editorials, book chapters, letters, and notes. The extracted data were then saved in CSV format and analyzed using bibliometric methods.
The annual number of publications is depicted as a line chart with a polynomial regression smoothing curve [6]. The retrieved publications were analyzed for both quantity and citation fre- quency by contributing countries/regions, serving as a proxy for productivity. Keywords related to adrenocortical carcinoma treatment were categorized by treatment type, and their annual frequencies were normalized as previously reported [7]. Citation counts were obtained from the Web of Science. The relationship
Identification of studies via Web of Science, PubMed, and Scopus
Identification
Records identified from Web of Science (n = 6109)
Records identified from PubMed (n = 4262)
Records identified from Scopus (n = 5119)
Records screened (n = 6599)
Records excluded: Meeting Abstract (n = 492) Editorial Material (n = 217) Book / Chapters (n = 135) Letter (n = 122) Note (n = 85) Correction (n = 32) Retraction (n = 9)
Screening
Reports assessed for eligibility (Articles = 4629, Reviews = 878) (n = 5507)
Included
Reports included in review (n = 5507)
between citation counts and the number of co-authoring institu- tions was examined using Spearman’s rank correlation.
VOSviewer version 1.6.20 (Leiden University, The Netherlands) was used for co-authorship and co-occurrence analyses, as well as to create network visualization maps. The co-authorship analysis assessed international and inter-institutional connec- tivity based on co-authored publications. A co-occurrence net- work visualization was created by counting publications that shared the same keywords, with keywords organized into the- matic clusters. Although some item labels were omitted to avoid overlap, the size of the labels and circles was based on the num- ber of publications per institution or the frequency of keyword occurrences [8]. The distance between items reflects their re- latedness, with shorter distances indicating higher frequencies of co-authorship or keyword co-occurrence. Strong links are represented by connecting lines, and each cluster is assigned a distinct color to enhance the recognition of visual relationships.
3 Results
I
After refining the selection of document types, a total of 878 re- views and 4629 articles were retrieved during the study period. The majority of publications were in English (n=5036, 91%), followed by Chinese (n=76), Japanese (n=74), French (n=68), German (n=59), Russian (n=58), and Spanish (n=43). Most non-English publications were found in the Scopus database.
The number of publications increased from 19 in 1984 to a peak of 366 in 2021 (Figure 2), indicating a growing global research interest in adrenocortical carcinoma. Most papers on this topic are published in endocrinology or surgery journals. The jour- nals with the highest number of publications on adrenocorti- cal carcinoma are the Journal of Clinical Endocrinology and Metabolism (n=230), the European Journal of Endocrinology (n=124), Endocrine-Related Cancer (n=98), Surgery (n=80), and Molecular and Cellular Endocrinology (n=77).
The United States accounted for nearly one-third of all papers on adrenocortical carcinoma, with European countries also rank- ing highly in productivity. Notably, publications from North
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America and Europe received more citations than those from Asian countries, such as China and Japan (Table 1). This may re- flect a bias, as publications from these Asian countries have in- creasingly emerged in recent years [9]. At the institutional level, the most productive institutions are primarily located in North America and Europe, with exceptions, such as the Universidade de São Paulo in Brazil, and Tohoku University in Japan. Examining the collaborative network map (Figure 3), most hub institutions are situated in North America and Europe, creating intricate and close-knit networks. Other institutions, whereas forming intercontinental connections, are generally limited to a single cluster, such as Japan (cluster 7), China (cluster 2), and Brazil (cluster 8). This finding suggests the existence of geo- graphical disparities in the study of adrenocortical carcinoma.
A co-occurrence map was created to illustrate the interrelation- ships among research topics. As shown in Figure 4, several major clusters can be identified. Cluster 1 includes general topics, such as diagnosis, and adrenal incidentaloma. Cluster 2 focuses on genetics, containing keywords like p53 and ß-catenin. Cluster
3 pertains to molecular biology, including gene expression, ste- roidogenesis, and apoptosis. Cluster 4 encompasses treatment modalities, such as mitotane, and chemotherapy. Cluster 5 is a minor biomarker group, consisting of keywords like immuno- histochemistry and classification. Overall, this co-occurrence analysis categorizes the publications into several major themes.
To gain an overview of the evolution of treatment modalities, we conducted a trend analysis using normalized frequencies of curated keywords. Surgery (including terms like adrenalec- tomy and resection), chemotherapy (including carboplatin and etoposide), and mitotane are the cornerstones of treatment, and their occurrence parallels the rising number of publications (Figure 5). Studies on steroidogenesis inhibitors (such as keto- conazole and osilodrostat) remained consistent throughout the study period. Notably, the number of publications on immuno- therapy (including nivolumab and ipilimumab) and targeted therapy (including cabozantinib and sorafenib) has increased in recent years. Published research accurately reflects advance- ments in the management of adrenocortical carcinoma.
| Country | Publications | Total citations | Without self-citations | Average citations | H-index |
|---|---|---|---|---|---|
| United States | 1662 | 40121 | 38712 | 46.07 | 125 |
| Germany | 584 | 14193 | 13 730 | 46.99 | 82 |
| Italy | 562 | 13 780 | 13 315 | 47.22 | 71 |
| France | 508 | 13 253 | 12822 | 54.66 | 88 |
| China | 486 | 5215 | 5029 | 12.52 | 37 |
| Japan | 377 | 8579 | 8396 | 26.82 | 42 |
| England | 284 | 10465 | 10 300 | 49.52 | 55 |
| Brazil | 258 | 4435 | 4231 | 32.34 | 47 |
| Netherlands | 212 | 7940 | 7788 | 61.38 | 56 |
| Canada | 208 | 7943 | 7832 | 47.73 | 51 |
tohoku univ tohoku univ hosp univ sao paulo mcgill univ nichd nichhd erasmus mc univ hosp freiburg g . univ wurzburg
hop trousseau
univ porto univ med & dent new jersey
univ sydney
hop cochin
cochin hosp
univ tokyo
univ michigan
us epa
univ bergen
univ texas md anderson canc ct
sichuan univ
univ padua
ohio state univ
univ helsinki
hungarian acad sci
univ ancona
washington univ
univ milan
univ genoa
univ calif san diego
univ verona
wake forest sch med
univ hosp padova
weill cornell med coll
univ montreal
univ vita salute san raffaele al ahliyya amman univ
| Cluster 1 | Cluster 5 |
| University of Michigan | University of Birmingham Erasmus Medical Center |
| National Cancer Institute | |
| MD Anderson Cancer Center | University of Helsinki |
| Cluster 2 | Cluster 6 |
| University of Texas | University of Turin |
| University of Sydney | University of Padua |
| Utrecht University | University of Milan |
| Cluster 3 | Cluster 7 |
| Cochin Hospital | Tohoku University |
| Paris Descartes University | University of Cambridge |
| University of Brescia | Keio University |
| Cluster 4 | Cluster 8 |
| University of Würzburg | University of São Paulo |
| University Hospital Würzburg | St. Jude Children's Hospital Federal University of Paraná |
| Karolinska Institute |
FIGURE 3 | Collaborative network map of institutions publishing research on adrenocortical carcinoma. The top three institutions in each cluster are presented.
FIGURE 4 | Keyword co-occurrence map for publications on adrenocortical carcinoma. The top three keywords in each cluster are highlighted.
doxorubicin
Cluster 1
cisplatin chemotherapy
immunotherapy
adrenocortical carcinoma management diagnosis cushings-syndrome laparoscopic adrenalectomy
radiotherapy
mitotane
prognosis
pan-cancer
series
acc
biomarker
Cluster 2
prognostic-factors
progression
carcinoma adrenocortical tumors gene children
resection
adrenal-cortical carcinoma
treatment
cancer
plasma
apoptosis
outcomes
features children
cells
p53
mutations
surgery
mortality
association
genes
metabolism
Cluster 3
adrenocortical tumor expression
bindinginduction
expression gene-expression cells
adrenocortical carcinoma
beta-catenin
cell-line inhibition
steroidogenesis proliferation
laparoscopic adrenalectomy
malignancy
tumor
gene
mice
jgf-ii-
in-vivo
h295r
Cluster 4
adrenalectomy
steroidogenesis
f-18-fdgpet/ct
diagnosis
adrenocortical tumors dna
cancer
testosterone
mitotane
adrenal
adrenal cortex
line
rat
survival features
prevalence
cortisol
secretion
surgery
masses
pheochromocytoma
carney complex
zona glomerulosa
Cluster 5
incidentaloma
primary aldosteronism
acth
tumors
prognosis
chemical-shift
gland
hypertension
immunohistochemistry classification metastasis
dogs
hyperadrenocorticism
Surgery
Chemotherapy
Mitotane
Steroidogenesis inhibitors
Immunotherapy
Keyword frequency
Targeted therapy
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The 5507 publications received 166065 citations from 70 904 articles (excluding self-citations, 66335 articles). The aver- age citation count per publication was 30.2. Journals that fre- quently cited papers on adrenocortical carcinoma also published many articles on the topic, including the Journal of Clinical Endocrinology and Metabolism, Cancers, and the International Journal of Molecular Sciences. As expected, review articles received more citations, averaging 37.9, compared to 29.6 for research articles. Interestingly, the number of co-authoring in- stitutions per publication was positively correlated with citation
counts (Figure 6), with a Spearman’s rank coefficient of 0.17 (95% confidence interval 0.14-0.20, p<0.0001).
I
4 Discussion
This is the first literature analysis to characterize the current research landscape on adrenocortical carcinoma. We observed geographical disparities in study productivity, with most pub- lications originating from North America and Europe. Unlike other primary cancers, race and ethnicity do not appear to be associated with any survival disadvantage in adrenocortical carcinoma [10, 11]. A plausible explanation for these dispari- ties is that international and inter-institutional collaboration is particularly important for rare diseases. Rigorous studies of disorders with low prevalence are only feasible within a multi- institutional consortium. It is noteworthy that in this study, the number of co-authoring institutions was positively correlated with citation counts, an indirect measure of research impact. Therefore, greater collaborative efforts should be encouraged to promote inter-institutional research.
A few scoring schemes and algorithms have traditionally been used to differentiate between adrenocortical adenomas and carcinomas. Currently, ancillary biomarkers and molecular di- agnostics play important roles for endocrine pathologists [12]. Furthermore, molecular studies have revealed several hall- marks of adrenocortical carcinoma, including the overexpres- sion of IGF2, increased TERT expression, and, most critically, TP53 mutations [13]. The implications of chromosome copy number changes, including whole-genome doubling, in tum- origenesis are being clarified [14]. Moreover, research on the
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interactions between Wnt/ß-catenin and p53/Rb signaling has gained momentum in the last decade [15]. Advances in cancer genetics are accompanied by studies addressing familial syn- dromes associated with adrenocortical carcinoma, such as Li- Fraumeni syndrome, Lynch syndrome, and multiple endocrine neoplasia type 1. Overall, we have witnessed substantial growth in genetic and molecular studies, particularly in co-occurrence clusters 2 and 3, in recent years.
Given the aggressiveness of adrenocortical carcinoma, many patients present with locally advanced, unresectable tumors or metastatic disease. Even after complete resection, adjuvant ther- apy is often recommended due to high recurrence rates [16]. In this study, we identified co-occurrence cluster 4, which includes publications on adjuvant and systemic therapies. Among the various treatment modalities, mitotane remains pivotal in man- aging adrenocortical carcinoma since its introduction into clini- cal practice [17]. Regarding surgical interventions, laparoscopic approaches are not recommended for adrenal masses with local invasion or suspected metastasis [18]. Although laparoscopic adrenalectomy may be safe in selected patients, open surgery is associated with a lower rate of positive resection margins and better overall and recurrence-free survival compared to laparo- scopic surgery [19]. In the present study, we observed a grow- ing interest in immunotherapy and targeted therapy research. It remains unclear whether these novel treatment modalities will lead to a paradigm shift in the near future.
The impact of hormonal hypersecretion on the prognosis of ad- renocortical carcinoma is controversial [20, 21]. Approximately 60% of adrenocortical cancers are functional, with many se- creting multiple hormones. Morbidity from adrenocortical car- cinoma can arise from either the disease burden or hormonal excess. The stable trend of publications investigating hormonal control suggests a continued enthusiasm for reducing both hormonal overproduction and disease burden. We noted that a small co-occurrence cluster 5 contains several publications on outcome predictors based on clinicopathological features. A study on the National Cancer Database found that patients’ age and the presence of comorbidities were the only factors
associated with worse survival among those undergoing sur- gery [22]. Given the bimodal age distribution of adrenocortical carcinoma, this issue is particularly relevant for geriatric pa- tients. Elderly patients may experience higher treatment com- plications and hospitalizations, even though their treatment responses are similar to those of younger patients [23]. More refined classification systems and prognostic models, espe- cially in countries with aging populations, represent an unmet research need.
This bibliometric analysis reveals several underexplored areas and potential future directions. Research outside of North America and Europe is underrepresented; in particular, data from Africa and the Middle East are lacking. This shortfall necessitates inter- national efforts to address geographical disparities. Additionally, there is limited research on prognostication and efficacy predic- tion, such as identifying patients who are less likely to benefit from mitotane therapy. Multi-institutional collaboration will be neces- sary to increase the sample size and statistical power to overcome the rarity of this disease. Furthermore, revolutionary advances in the management of this deadly cancer depend on ongoing molec- ular and translational studies. Compared to other neoplasms, the number of such studies is relatively small and restricted to a few experimental models, such as NCI-H295R cells. Significant sci- entific breakthroughs may meaningfully transform clinical par- adigms, as evidenced by the growing number of clinical trials on immunotherapy and targeted therapy.
We acknowledge that the number of publications does not neces- sarily reflect the significance or validity of the information pro- vided. For instance, whereas there appear to be no novel surgical strategies, surgery remains the only potentially curative treat- ment for adrenocortical carcinoma. When confronting such an uncommon and challenging neoplasm, multidisciplinary team- work inevitably relies on limited evidence, clinical judgment, and biological rationale [24]. Thus, our study represents a small but meaningful step toward examining the trends and gaps in current research efforts.
In conclusion, this literature analysis provides an overview of the current research landscape on adrenocortical carcinoma that could guide future studies. Several clusters of trending topics have been identified, and geographical disparities are notable. International and interdisciplinary collaboration may not only enhance productivity but also promote scientific advances.
Author Contributions
Tun-Pang Chu: conceptualization, data curation, formal analysis, writing - original draft. Chi-Yu Kuo: methodology, formal analysis, writing - review and editing. Shih-Ping Cheng: conceptualization, investigation, formal analysis, writing - original draft.
Acknowledgments
We thank Leo Liang from Mackay Junior College of Medicine, Nursing, and Management for his assistance in accessing the database.
Consent
The authors have nothing to report.
Conflicts of Interest
The authors declare no conflicts of interest.
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