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Immunohistochemical evaluation of apelin and VEGF expression in cortisol-producing adrenal adenomas.

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Τίτλος: Immunohistochemical evaluation of apelin and VEGF expression in cortisol-producing adrenal adenomas.
Συγγραφείς: Çalişkan Burgucu H; Division of Endocrinology and Metabolism, Department of Internal Medicine, Konya City Hospital, Konya, Turkey. htcbrgc81@gmail.com., Günler T; Department of Pathology, Konya City Hospital, Konya, Turkey., Ömeroğlu E; Department of Pathology, University of Health Sciences, Konya City Hospital, Konya, Turkey., Ünlü Y; Department of Pathology, University of Health Sciences, Konya City Hospital, Konya, Turkey., Aksu O; Division of Endocrinology and Metabolism, Department of Internal Medicine, University of Health Sciences, Konya City Hospital, Konya, Turkey.
Πηγή: BMC endocrine disorders [BMC Endocr Disord] 2026 Sep 16; Vol. 26 (1). Date of Electronic Publication: 2026 Sep 16.
Τύπος έκδοσης: Journal Article
Γλώσσα: English
Στοιχεία περιοδικού: Publisher: BioMed Central Country of Publication: England NLM ID: 101088676 Publication Model: Electronic Cited Medium: Internet ISSN: 1472-6823 (Electronic) Linking ISSN: 14726823 NLM ISO Abbreviation: BMC Endocr Disord Subsets: MEDLINE
Imprint Name(s): Original Publication: London : BioMed Central, [2001-
Ιατρικοί όροι (MeSH): Apelin*/metabolism , Vascular Endothelial Growth Factor A*/metabolism , Adrenocortical Adenoma*/metabolism , Adrenocortical Adenoma*/pathology , Adrenocortical Adenoma*/complications , Hydrocortisone*/metabolism , Cushing Syndrome*/metabolism , Cushing Syndrome*/pathology , Cushing Syndrome*/etiology , Adrenal Cortex Neoplasms*/metabolism , Adrenal Cortex Neoplasms*/pathology , Adrenal Cortex Neoplasms*/complications , Adrenal Gland Neoplasms*/metabolism , Adrenal Gland Neoplasms*/pathology, Biomarkers, Tumor/metabolism ; Adrenal Cortex/metabolism ; Humans ; Female ; Male ; Retrospective Studies ; Immunohistochemistry ; Adult ; Middle Aged ; Case-Control Studies ; Prognosis ; Follow-Up Studies
Περίληψη: Purpose: In this study, we aimed to investigate the immunohistochemical expression of apelin in tissue samples obtained from patients with Cushing's syndrome (CS) due to cortisol-producing adrenal adenoma (CPA) and to compare these findings with normal adrenal cortex tissue. Additionally, we sought to evaluate the association of apelin expression with clinical, hormonal, and histopathological parameters. The expression profile of vascular endothelial growth factor (VEGF) was also assessed to explore potential angiogenic interactions.
Methods: This retrospective, single-center study included 11 patients diagnosed with CPA and 15 control subjects with histologically normal adrenal cortex tissue. Formalin-fixed, paraffin-embedded tissue sections were subjected to immunohistochemical staining for apelin and VEGF. Immunohistochemical evaluation was performed by assessing staining intensity and the percentage of positively stained cells. An immunoreactivity score (IRS) was calculated by combining these parameters to provide a semi-quantitative measure of protein expression.
Results: Apelin staining intensity was significantly higher in CPA tissues compared with controls (p = 0.026), whereas the percentage of apelin-positive cells and IRS values did not differ significantly between groups. In an exploratory ROC analysis, apelin staining intensity showed moderate discrimination between CPA and control adrenal cortex tissues (AUC = 0.776, 95% CI: 0.581-0.971, p = 0.018). In bias-reduced univariable logistic regression, apelin staining intensity was associated with CPA (OR = 2.96, 95% CI: 1.02-8.60, p = 0.046), although the wide confidence interval indicated considerable uncertainty. VEGF staining parameters did not differ significantly between CPA and control tissues. No statistically significant correlations could be demonstrated between apelin or VEGF IRS and the evaluated clinicopathological or hormonal parameters.
Conclusion: Apelin staining intensity was higher in CPA than in normal adrenal cortex, whereas the proportion of apelin-positive cells and IRS did not differ significantly between groups. VEGF staining parameters also did not differ significantly between CPA and control tissues. These findings suggest altered apelin immunoreactivity in CPA; however, given the exploratory nature and small sample size of the study, larger studies are required to confirm these observations and clarify their biological significance.
Clinical Trial Number: Not applicable.
(© 2026. The Author(s).)
Competing Interests: Declarations. Ethics approval and consent to participate: This study was approved by the Non-Interventional Clinical Research Ethics Committee of Konya City Hospital (Approval No. 2025/116). The study was conducted in accordance with the ethical principles of the Declaration of Helsinki (as revised in 2013). Consent to participate: The requirement for individual informed consent was waived by the ethics committee due to the retrospective nature of the study and the use of fully anonymized data. Competing interests: The authors declare no competing interests.
References: Cell Metab. 2008 Nov;8(5):437-45. (PMID: 19046574)
Int J Mol Sci. 2025 Mar 25;26(7):. (PMID: 40243599)
Endocrine. 2023 Mar;79(3):554-558. (PMID: 36350461)
J Clin Endocrinol Metab. 2002 Nov;87(11):4961-5. (PMID: 12414859)
J Neurosci Res. 2021 Sep;99(9):2117-2133. (PMID: 34115895)
Pathol Oncol Res. 2018 Jul;24(3):689-693. (PMID: 28695321)
Circ Res. 2008 Aug 15;103(4):432-40. (PMID: 18617693)
Front Endocrinol (Lausanne). 2022 Apr 28;13:882906. (PMID: 35574028)
Endocr J. 2024 Aug 8;71(8):789-797. (PMID: 38945931)
JAMA. 2023 Jul 11;330(2):170-181. (PMID: 37432427)
Int J Mol Sci. 2022 May 17;23(10):. (PMID: 35628389)
J Pathol Clin Res. 2024 Sep;10(5):e12394. (PMID: 39177576)
Endocrinol Metab Clin North Am. 1988 Sep;17(3):445-72. (PMID: 3065076)
Cells. 2020 Mar 02;9(3):. (PMID: 32131466)
Cancers (Basel). 2021 Mar 01;13(5):. (PMID: 33804534)
J Biol Chem. 2000 Jul 14;275(28):21061-7. (PMID: 10777510)
Ann Transl Med. 2020 Mar;8(5):243. (PMID: 32309390)
J Clin Endocrinol Metab. 2022 Nov 23;107(11):3162-3174. (PMID: 36036941)
Am J Surg Pathol. 2002 Dec;26(12):1612-9. (PMID: 12459628)
J Clin Endocrinol Metab. 1999 Feb;84(2):440-8. (PMID: 10022398)
Pathologe. 1987 May;8(3):138-40. (PMID: 3303008)
Front Endocrinol (Lausanne). 2022 Mar 09;13:820002. (PMID: 35355561)
Dev Biol. 2007 May 15;305(2):599-614. (PMID: 17412318)
Endocrine. 2011 Aug;40(1):1-9. (PMID: 21725702)
Contributed Indexing: Keywords: Angiogenesis; Apelin; Cortisol-producing adrenal adenoma; Cushing’s syndrome; Immunohistochemistry; Vascular endothelial growth factor
Substance Nomenclature: 0 (Apelin)
0 (Vascular Endothelial Growth Factor A)
WI4X0X7BPJ (Hydrocortisone)
0 (VEGFA protein, human)
0 (Biomarkers, Tumor)
0 (APLN protein, human)
Entry Date(s): Date Created: 20260916 Date Completed: 20260917 Latest Revision: 20260918
Update Code: 20260918
PubMed Central ID: PMC13579810
DOI: 10.1186/s12902-026-02563-w
PMID: 42750037
Βάση Δεδομένων: MEDLINE
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  Data: Immunohistochemical evaluation of apelin and VEGF expression in cortisol-producing adrenal adenomas.
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  Data: <searchLink fieldCode="AU" term="%22Çalişkan+Burgucu+H%22">Çalişkan Burgucu H</searchLink>; Division of Endocrinology and Metabolism, Department of Internal Medicine, Konya City Hospital, Konya, Turkey. htcbrgc81@gmail.com.<br /><searchLink fieldCode="AU" term="%22Günler+T%22">Günler T</searchLink>; Department of Pathology, Konya City Hospital, Konya, Turkey.<br /><searchLink fieldCode="AU" term="%22Ömeroğlu+E%22">Ömeroğlu E</searchLink>; Department of Pathology, University of Health Sciences, Konya City Hospital, Konya, Turkey.<br /><searchLink fieldCode="AU" term="%22Ünlü+Y%22">Ünlü Y</searchLink>; Department of Pathology, University of Health Sciences, Konya City Hospital, Konya, Turkey.<br /><searchLink fieldCode="AU" term="%22Aksu+O%22">Aksu O</searchLink>; Division of Endocrinology and Metabolism, Department of Internal Medicine, University of Health Sciences, Konya City Hospital, Konya, Turkey.
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  Data: <searchLink fieldCode="MM" term="%22Apelin%22">Apelin*</searchLink>/<searchLink fieldCode="MM" term="%22Apelin+metabolism%22">metabolism</searchLink> <br /><searchLink fieldCode="MM" term="%22Vascular+Endothelial+Growth+Factor+A%22">Vascular Endothelial Growth Factor A*</searchLink>/<searchLink fieldCode="MM" term="%22Vascular+Endothelial+Growth+Factor+A+metabolism%22">metabolism</searchLink> <br /><searchLink fieldCode="MM" term="%22Adrenocortical+Adenoma%22">Adrenocortical Adenoma*</searchLink>/<searchLink fieldCode="MM" term="%22Adrenocortical+Adenoma+metabolism%22">metabolism</searchLink> <br /><searchLink fieldCode="MM" term="%22Adrenocortical+Adenoma%22">Adrenocortical Adenoma*</searchLink>/<searchLink fieldCode="MM" term="%22Adrenocortical+Adenoma+pathology%22">pathology</searchLink> <br /><searchLink fieldCode="MM" term="%22Adrenocortical+Adenoma%22">Adrenocortical Adenoma*</searchLink>/<searchLink fieldCode="MM" term="%22Adrenocortical+Adenoma+complications%22">complications</searchLink> <br /><searchLink fieldCode="MM" term="%22Hydrocortisone%22">Hydrocortisone*</searchLink>/<searchLink fieldCode="MM" term="%22Hydrocortisone+metabolism%22">metabolism</searchLink> <br /><searchLink fieldCode="MM" term="%22Cushing+Syndrome%22">Cushing Syndrome*</searchLink>/<searchLink fieldCode="MM" term="%22Cushing+Syndrome+metabolism%22">metabolism</searchLink> <br /><searchLink fieldCode="MM" term="%22Cushing+Syndrome%22">Cushing Syndrome*</searchLink>/<searchLink fieldCode="MM" term="%22Cushing+Syndrome+pathology%22">pathology</searchLink> <br /><searchLink fieldCode="MM" term="%22Cushing+Syndrome%22">Cushing Syndrome*</searchLink>/<searchLink fieldCode="MM" term="%22Cushing+Syndrome+etiology%22">etiology</searchLink> <br /><searchLink fieldCode="MM" term="%22Adrenal+Cortex+Neoplasms%22">Adrenal Cortex Neoplasms*</searchLink>/<searchLink fieldCode="MM" term="%22Adrenal+Cortex+Neoplasms+metabolism%22">metabolism</searchLink> <br /><searchLink fieldCode="MM" term="%22Adrenal+Cortex+Neoplasms%22">Adrenal Cortex Neoplasms*</searchLink>/<searchLink fieldCode="MM" term="%22Adrenal+Cortex+Neoplasms+pathology%22">pathology</searchLink> <br /><searchLink fieldCode="MM" term="%22Adrenal+Cortex+Neoplasms%22">Adrenal Cortex Neoplasms*</searchLink>/<searchLink fieldCode="MM" term="%22Adrenal+Cortex+Neoplasms+complications%22">complications</searchLink> <br /><searchLink fieldCode="MM" term="%22Adrenal+Gland+Neoplasms%22">Adrenal Gland Neoplasms*</searchLink>/<searchLink fieldCode="MM" term="%22Adrenal+Gland+Neoplasms+metabolism%22">metabolism</searchLink> <br /><searchLink fieldCode="MM" term="%22Adrenal+Gland+Neoplasms%22">Adrenal Gland Neoplasms*</searchLink>/<searchLink fieldCode="MM" term="%22Adrenal+Gland+Neoplasms+pathology%22">pathology</searchLink><br /><searchLink fieldCode="MH" term="%22Biomarkers%2C+Tumor%22">Biomarkers, Tumor</searchLink>/<searchLink fieldCode="MH" term="%22Biomarkers%2C+Tumor+metabolism%22">metabolism</searchLink> ; <searchLink fieldCode="MH" term="%22Adrenal+Cortex%22">Adrenal Cortex</searchLink>/<searchLink fieldCode="MH" term="%22Adrenal+Cortex+metabolism%22">metabolism</searchLink> ; <searchLink fieldCode="MH" term="%22Humans%22">Humans</searchLink> ; <searchLink fieldCode="MH" term="%22Female%22">Female</searchLink> ; <searchLink fieldCode="MH" term="%22Male%22">Male</searchLink> ; <searchLink fieldCode="MH" term="%22Retrospective+Studies%22">Retrospective Studies</searchLink> ; <searchLink fieldCode="MH" term="%22Immunohistochemistry%22">Immunohistochemistry</searchLink> ; <searchLink fieldCode="MH" term="%22Adult%22">Adult</searchLink> ; <searchLink fieldCode="MH" term="%22Middle+Aged%22">Middle Aged</searchLink> ; <searchLink fieldCode="MH" term="%22Case-Control+Studies%22">Case-Control Studies</searchLink> ; <searchLink fieldCode="MH" term="%22Prognosis%22">Prognosis</searchLink> ; <searchLink fieldCode="MH" term="%22Follow-Up+Studies%22">Follow-Up Studies</searchLink>
– Name: Abstract
  Label: Abstract
  Group: Ab
  Data: Purpose: In this study, we aimed to investigate the immunohistochemical expression of apelin in tissue samples obtained from patients with Cushing's syndrome (CS) due to cortisol-producing adrenal adenoma (CPA) and to compare these findings with normal adrenal cortex tissue. Additionally, we sought to evaluate the association of apelin expression with clinical, hormonal, and histopathological parameters. The expression profile of vascular endothelial growth factor (VEGF) was also assessed to explore potential angiogenic interactions.<br />Methods: This retrospective, single-center study included 11 patients diagnosed with CPA and 15 control subjects with histologically normal adrenal cortex tissue. Formalin-fixed, paraffin-embedded tissue sections were subjected to immunohistochemical staining for apelin and VEGF. Immunohistochemical evaluation was performed by assessing staining intensity and the percentage of positively stained cells. An immunoreactivity score (IRS) was calculated by combining these parameters to provide a semi-quantitative measure of protein expression.<br />Results: Apelin staining intensity was significantly higher in CPA tissues compared with controls (p = 0.026), whereas the percentage of apelin-positive cells and IRS values did not differ significantly between groups. In an exploratory ROC analysis, apelin staining intensity showed moderate discrimination between CPA and control adrenal cortex tissues (AUC = 0.776, 95% CI: 0.581-0.971, p = 0.018). In bias-reduced univariable logistic regression, apelin staining intensity was associated with CPA (OR = 2.96, 95% CI: 1.02-8.60, p = 0.046), although the wide confidence interval indicated considerable uncertainty. VEGF staining parameters did not differ significantly between CPA and control tissues. No statistically significant correlations could be demonstrated between apelin or VEGF IRS and the evaluated clinicopathological or hormonal parameters.<br />Conclusion: Apelin staining intensity was higher in CPA than in normal adrenal cortex, whereas the proportion of apelin-positive cells and IRS did not differ significantly between groups. VEGF staining parameters also did not differ significantly between CPA and control tissues. These findings suggest altered apelin immunoreactivity in CPA; however, given the exploratory nature and small sample size of the study, larger studies are required to confirm these observations and clarify their biological significance.<br />Clinical Trial Number: Not applicable.<br /> (© 2026. The Author(s).)
– Name: Abstract
  Label: Competing Interests
  Group: Ab
  Data: Declarations. Ethics approval and consent to participate: This study was approved by the Non-Interventional Clinical Research Ethics Committee of Konya City Hospital (Approval No. 2025/116). The study was conducted in accordance with the ethical principles of the Declaration of Helsinki (as revised in 2013). Consent to participate: The requirement for individual informed consent was waived by the ethics committee due to the retrospective nature of the study and the use of fully anonymized data. Competing interests: The authors declare no competing interests.
– Name: Ref
  Label: References
  Group: RefInfo
  Data: Cell Metab. 2008 Nov;8(5):437-45. (PMID: <searchLink fieldCode="PM" term="%2219046574%22">19046574)</searchLink><br />Int J Mol Sci. 2025 Mar 25;26(7):. (PMID: <searchLink fieldCode="PM" term="%2240243599%22">40243599)</searchLink><br />Endocrine. 2023 Mar;79(3):554-558. (PMID: <searchLink fieldCode="PM" term="%2236350461%22">36350461)</searchLink><br />J Clin Endocrinol Metab. 2002 Nov;87(11):4961-5. (PMID: <searchLink fieldCode="PM" term="%2212414859%22">12414859)</searchLink><br />J Neurosci Res. 2021 Sep;99(9):2117-2133. (PMID: <searchLink fieldCode="PM" term="%2234115895%22">34115895)</searchLink><br />Pathol Oncol Res. 2018 Jul;24(3):689-693. (PMID: <searchLink fieldCode="PM" term="%2228695321%22">28695321)</searchLink><br />Circ Res. 2008 Aug 15;103(4):432-40. (PMID: <searchLink fieldCode="PM" term="%2218617693%22">18617693)</searchLink><br />Front Endocrinol (Lausanne). 2022 Apr 28;13:882906. (PMID: <searchLink fieldCode="PM" term="%2235574028%22">35574028)</searchLink><br />Endocr J. 2024 Aug 8;71(8):789-797. (PMID: <searchLink fieldCode="PM" term="%2238945931%22">38945931)</searchLink><br />JAMA. 2023 Jul 11;330(2):170-181. (PMID: <searchLink fieldCode="PM" term="%2237432427%22">37432427)</searchLink><br />Int J Mol Sci. 2022 May 17;23(10):. (PMID: <searchLink fieldCode="PM" term="%2235628389%22">35628389)</searchLink><br />J Pathol Clin Res. 2024 Sep;10(5):e12394. (PMID: <searchLink fieldCode="PM" term="%2239177576%22">39177576)</searchLink><br />Endocrinol Metab Clin North Am. 1988 Sep;17(3):445-72. (PMID: <searchLink fieldCode="PM" term="%223065076%22">3065076)</searchLink><br />Cells. 2020 Mar 02;9(3):. (PMID: <searchLink fieldCode="PM" term="%2232131466%22">32131466)</searchLink><br />Cancers (Basel). 2021 Mar 01;13(5):. (PMID: <searchLink fieldCode="PM" term="%2233804534%22">33804534)</searchLink><br />J Biol Chem. 2000 Jul 14;275(28):21061-7. (PMID: <searchLink fieldCode="PM" term="%2210777510%22">10777510)</searchLink><br />Ann Transl Med. 2020 Mar;8(5):243. (PMID: <searchLink fieldCode="PM" term="%2232309390%22">32309390)</searchLink><br />J Clin Endocrinol Metab. 2022 Nov 23;107(11):3162-3174. (PMID: <searchLink fieldCode="PM" term="%2236036941%22">36036941)</searchLink><br />Am J Surg Pathol. 2002 Dec;26(12):1612-9. (PMID: <searchLink fieldCode="PM" term="%2212459628%22">12459628)</searchLink><br />J Clin Endocrinol Metab. 1999 Feb;84(2):440-8. (PMID: <searchLink fieldCode="PM" term="%2210022398%22">10022398)</searchLink><br />Pathologe. 1987 May;8(3):138-40. (PMID: <searchLink fieldCode="PM" term="%223303008%22">3303008)</searchLink><br />Front Endocrinol (Lausanne). 2022 Mar 09;13:820002. (PMID: <searchLink fieldCode="PM" term="%2235355561%22">35355561)</searchLink><br />Dev Biol. 2007 May 15;305(2):599-614. (PMID: <searchLink fieldCode="PM" term="%2217412318%22">17412318)</searchLink><br />Endocrine. 2011 Aug;40(1):1-9. (PMID: <searchLink fieldCode="PM" term="%2221725702%22">21725702)</searchLink>
– Name: SubjectMinor
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  Data: <i>Keywords: </i>Angiogenesis; Apelin; Cortisol-producing adrenal adenoma; Cushing’s syndrome; Immunohistochemistry; Vascular endothelial growth factor
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        Text: English
    Subjects:
      – SubjectFull: Biomarkers, Tumor metabolism
        Type: general
      – SubjectFull: Adrenal Cortex metabolism
        Type: general
      – SubjectFull: Humans
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      – SubjectFull: Female
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      – SubjectFull: Case-Control Studies
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      – SubjectFull: Apelin metabolism
        Type: general
      – SubjectFull: Vascular Endothelial Growth Factor A metabolism
        Type: general
      – SubjectFull: Adrenocortical Adenoma metabolism
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      – SubjectFull: Adrenocortical Adenoma pathology
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      – SubjectFull: Adrenocortical Adenoma complications
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      – SubjectFull: Hydrocortisone metabolism
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      – SubjectFull: Cushing Syndrome metabolism
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      – SubjectFull: Cushing Syndrome pathology
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      – SubjectFull: Cushing Syndrome etiology
        Type: general
      – SubjectFull: Adrenal Cortex Neoplasms metabolism
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      – SubjectFull: Adrenal Cortex Neoplasms pathology
        Type: general
      – SubjectFull: Adrenal Cortex Neoplasms complications
        Type: general
      – SubjectFull: Adrenal Gland Neoplasms metabolism
        Type: general
      – SubjectFull: Adrenal Gland Neoplasms pathology
        Type: general
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      – TitleFull: Immunohistochemical evaluation of apelin and VEGF expression in cortisol-producing adrenal adenomas.
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              Text: 2026 Sep 16
              Type: published
              Y: 2026
          Identifiers:
            – Type: issn-electronic
              Value: 1472-6823
          Numbering:
            – Type: volume
              Value: 26
            – Type: issue
              Value: 1
          Titles:
            – TitleFull: BMC endocrine disorders
              Type: main
ResultId 1