Mixed gangliocytoma-pituitary adenoma containing GH and GHRH co-secreting adenoma cells

in Endocrinology, Diabetes & Metabolism Case Reports

Summary

A 67-year-old woman with a past history of type 2 diabetes mellitus presented with worsening glycemic control. She had some acromegaly symptoms and magnetic resonance imaging demonstrated a pituitary tumor. Endocrinological examination found the resting growth hormone (GH) level within the normal range, but elevated insulin-like growth factor 1 level. A 75 g oral glucose tolerance test showed inadequate suppression of nadir GH levels. Acromegaly due to GH-secreting pituitary tumor was diagnosed. The patient underwent endoscopic transsphenoidal surgery resulting in gross total removal of the tumor and recovered well postoperatively. Histological examination of the tumor showed coexistence of relatively large gangliocytoma cells and pituitary adenoma cells, suggesting mixed gangliocytoma-pituitary adenoma. In addition, colocalization of GH and GH-releasing hormone (GHRH) in pituitary adenoma cells was revealed, so the adenomatous components were more likely to produce GHRH in our mixed gangliocytoma-pituitary adenoma case. Mixed gangliocytoma-pituitary adenoma is very rare, and the present unique case demonstrated only the adenomatous components associated with GHRH production.

Learning points:

  • Sellar gangliocytoma coexisting with pituitary adenoma is recognized as a mixed gangliocytoma-pituitary adenoma and is very rare.

  • A proposed developmental mechanism of growth hormone (GH)-secreting mixed gangliocytoma-pituitary adenoma involves GH-releasing hormone (GHRH) produced by the gangliocytic components promoting the growth of tumor including GH-secreting adenomatous components.

  • Since our present case indicated that the adenomatous components of mixed gangliocytoma-pituitary adenoma could secrete both GH and GHRH simultaneously, progression of GH-secreting mixed gangliocytoma and pituitary adenoma may involve exposure to spontaneously produced GHRH due to the adenomatous components.

Abstract

Summary

A 67-year-old woman with a past history of type 2 diabetes mellitus presented with worsening glycemic control. She had some acromegaly symptoms and magnetic resonance imaging demonstrated a pituitary tumor. Endocrinological examination found the resting growth hormone (GH) level within the normal range, but elevated insulin-like growth factor 1 level. A 75 g oral glucose tolerance test showed inadequate suppression of nadir GH levels. Acromegaly due to GH-secreting pituitary tumor was diagnosed. The patient underwent endoscopic transsphenoidal surgery resulting in gross total removal of the tumor and recovered well postoperatively. Histological examination of the tumor showed coexistence of relatively large gangliocytoma cells and pituitary adenoma cells, suggesting mixed gangliocytoma-pituitary adenoma. In addition, colocalization of GH and GH-releasing hormone (GHRH) in pituitary adenoma cells was revealed, so the adenomatous components were more likely to produce GHRH in our mixed gangliocytoma-pituitary adenoma case. Mixed gangliocytoma-pituitary adenoma is very rare, and the present unique case demonstrated only the adenomatous components associated with GHRH production.

Learning points:

  • Sellar gangliocytoma coexisting with pituitary adenoma is recognized as a mixed gangliocytoma-pituitary adenoma and is very rare.

  • A proposed developmental mechanism of growth hormone (GH)-secreting mixed gangliocytoma-pituitary adenoma involves GH-releasing hormone (GHRH) produced by the gangliocytic components promoting the growth of tumor including GH-secreting adenomatous components.

  • Since our present case indicated that the adenomatous components of mixed gangliocytoma-pituitary adenoma could secrete both GH and GHRH simultaneously, progression of GH-secreting mixed gangliocytoma and pituitary adenoma may involve exposure to spontaneously produced GHRH due to the adenomatous components.

Background

Gangliocytoma occurs in all regions of the central nervous system but rarely in the sellar region. Sellar gangliocytoma coexisting with pituitary adenoma is recognized as a mixed gangliocytoma-pituitary adenoma. Mixed gangliocytoma-pituitary adenoma is extremely rare, accounting for 0.14–0.52% of all sellar tumors, and mostly occurs in women (1, 2). Since mixed gangliocytoma-pituitary adenoma has no specific clinical symptoms, endocrine findings, or brain imaging appearance, it is usually only diagnosed by postoperative histopathology (3). The adenomatous components of mixed gangliocytoma-pituitary adenoma are known to frequently secrete excess growth hormone (GH) and are typically characterized as pituitary somatotroph adenoma (2, 4). The gangliocytic components of mixed gangliocytoma-pituitary adenoma showed immunoreactivity for hypothalamic releasing hormones other than the neuroendocrine markers (2, 5, 6). A proposed but controversial developmental mechanism of GH-secreting mixed gangliocytoma-pituitary adenoma involves GH-releasing hormone (GHRH) produced by the gangliocytic components promoting the growth of tumor including GH-secreting adenomatous components (2, 6).

We report a rare case of mixed gangliocytoma-pituitary adenoma in which the GH-secreting adenoma cells, but not the ganglion cells, produced GHRH.

Case presentation

A 67-year-old woman with a past history of type 2 diabetes mellitus presented with worsening glycemic control. She had some physical abnormalities such as face with enlarged forehead, nose, and chin, increased bone size of the extremities, and mild enlargement of the tongue.

Investigation

Magnetic resonance (MR) imaging revealed a pituitary tumor of 1.9 cm maximum length with Knosp grade 0 (7), appearing with less contrast enhancement than the normal pituitary gland on gadolinium-enhanced T1-weighted MR imaging and isointense on T2-weighted MR imaging. Endocrinological examination found resting GH level (3.321 ng/mL; normal: 0.010–3.607 ng/mL) within the normal range, but elevated insulin-like growth factor 1 (IGF-1) level (381 ng/mL; normal: 61–183 ng/mL). A 75 g oral glucose tolerance test (OGTT) achieved inadequate suppression of nadir GH level (3.190 ng/mL). Acromegaly due to GH-secreting pituitary tumor was diagnosed according to these findings.

Treatment

The patient underwent removal of the pituitary tumor via an endoscopic endonasal transsphenoidal approach without premedication, which was successful in accomplishing gross total removal.

Outcome and follow-up

The postoperative course was uneventful. Postoperative MR imaging demonstrated no obvious residual tumor. Resting GH level (2.467 ng/mL) remained within the normal range, and IGF-1 level (233 ng/mL) decreased but was slightly higher than normal at 1 week postoperatively. Postoperative 75 g OGTT found nadir GH level of 0.880 ng/mL, resulting in no suppression of less than 0.4 ng/mL (8). Since aggravation of diabetic hyperglycemia resolved promptly, the patient was discharged on foot without adjuvant therapy. Random GH level (0.587 ng/mL) remained below 1.0 ng/mL (9) and IGF-1 level (167 ng/mL) was normalized at 3 months postoperatively. Thereafter, the patient received outpatient follow-up with random GH levels <1.0 ng/mL and IGF-1 levels within the normal range.

Hematoxylin and eosin staining of the tumor revealed that relatively large cells were adjacent to small round cells corresponding to the pituitary adenoma and were mixed within the boundary area (Fig. 1A). Immunohistochemical staining found the large cells were positive for microtubule-associated protein 2 (MAP-2) (anti-MAP-2 antibody; MAB364, Millipore) as the mature neuron marker, indicating the presence of gangliocytoma (Fig. 1B). Pituitary adenoma cells showed weak immunoreactivity for GH (anti-GH antibody; ab7905, Abcam) (Fig. 1C) and a strong dot-like immunopositive pattern representing the fibrous body for CAM 5.2 (anti-CAM 5.2 antibody; No. 349205, Beckton, Dickinson and Company) as the cytokeratin marker (Fig. 1D), indicating a sparsely granulated subtype of pituitary somatotroph adenoma. The histopathological findings of the gangliocytic and adenomatous components determined the diagnosis as mixed gangliocytoma-pituitary adenoma. Immunohistochemical demonstration of GHRH expression was performed using a pair of mirror section images. No correspondence of MAP-2- and GHRH (anti-GHRH antibody; ab80009, Abcam)-positive cells was found (Fig. 2A and B), but correspondence of GH- and GHRH-positive cells was demonstrated (Fig. 2C and D). Furthermore, double immunofluorescence staining for GH and GHRH revealed cells with colocalization (Fig. 2E, F and G).

Figure 1
Figure 1

Histopathological examination of the pituitary tumor. (A) Hematoxylin and eosin staining showing relatively large cells and pituitary adenoma cells adjacent and mixed within the boundary area. (B) Immunostaining for microtubule-associated protein 2 demonstrating positivity in large cells, indicating the presence of gangliocytoma. Immunostaining for growth hormone showing positivity but weak reactivity in pituitary adenoma cells (C) and CAM 5.2 immunostaining showing strong dot-like positive pattern (D), indicating the sparsely granulated subtype of pituitary somatotroph adenoma. Scale bar = 50 μm.

Citation: Endocrinology, Diabetes & Metabolism Case Reports 2019, 1; 10.1530/EDM-19-0099

Figure 2
Figure 2

Immunohistochemical demonstration of growth hormone-releasing hormone (GHRH). Immunohistochemical staining using a pair of mirror section images showing no correspondence of microtubule-associated protein 2-positive (A) and GHRH-positive (B) cells, but demonstrating correspondence of growth hormone (GH)-positive (C) and GHRH-positive (D) cells. Double immunofluorescence staining for GH (E) and GHRH (F) revealing cells with colocalization (G). Arrowheads, colocalized cells. Scale bar = 50 μm in A–D; 20 μm in E–G.

Citation: Endocrinology, Diabetes & Metabolism Case Reports 2019, 1; 10.1530/EDM-19-0099

Discussion

The gangliocytic components of mixed gangliocytoma-pituitary adenoma are presumed to secrete the hypothalamic releasing hormones including GHRH, gonadotropin-releasing hormone, thyrotropin-releasing hormone, and corticotropin-releasing hormone, and promote the proliferation of the correlated adenomatous components (6, 10, 11). On the other hand, both components of mixed gangliocytoma-pituitary adenoma were demonstrated to produce the hypothalamic releasing hormones (3). All previous reports of mixed gangliocytoma-pituitary adenoma investigating GHRH immunoreactivity have implied GHRH production in the gangliocytic components (Table 1) (1, 5, 6, 10, 11, 12, 13, 14, 15, 16, 17, 18, 19). However, our present case demonstrated that only the adenomatous components may produce GHRH in GH-secreting mixed gangliocytoma-pituitary adenoma. Recently transdifferentiation of neuroendocrine cells to a neuronal phenotype (20) and expression of pituitary transcription factors in gangliocytic components (21) were indicated in mixed gangliocytoma-pituitary adenoma. This indication that the origin of two components in mixed gangliocytoma-pituitary adenoma relates to pituitary lineage supports the possibility that either or both of these components produce GHRH in GH-secreting mixed gangliocytoma-pituitary adenoma.

Table 1

Summary of literature review reporting mixed gangliocytoma-pituitary adenoma associated with growth hormone-releasing hormone immunoreactivity.

No.AuthorYearNumber of casesHormone producedImmunoreactivity of GHRH
Gangliocytic componentAdenomatous component
1Asa et al. (10)19842GH+
GH+
2Bevan et al. (13)19891GH, PRL+
3Li et al. (15)19891GH+
4Asada et al. (12)19901GH, PRL+
5Slowik et al. (19)19901GH, PRL+
6Horvath et al. (5)1994A few casesGH (all cases)+
7Saeger et al. (11)19941GH, PRL+
8Iwase et al. (14)19951GH+
9Morikawa et al. (17)19971GH+
10Saeger et al. (18)19975GH+
GH+
GH+
GH+
ACTH+
11Luna et al. (16)20011GH+
12Kurosaki et al. (6)20025GH, PRL+
GH+
GH+
GH+
GH+
13Kontogeorgos et al. (1)20063GH+
GH+
GH+

ACTH, adrenocorticotropic hormone; GH, growth hormone; GHRH, growth hormone-releasing hormone; PRL, prolactin.

We present a unique case of mixed gangliocytoma-pituitary adenoma with the adenomatous components which could secrete both GH and GHRH simultaneously. This finding suggested that progression of GH-secreting mixed gangliocytoma-pituitary adenoma may involve exposure to spontaneously produced GHRH due to the adenomatous components.

Declaration of interest

The authors declare that there is no conflict of interest that could be perceived as prejudicing the impartiality of this case report.

Funding

This research did not receive any specific grant from any funding agency in the public, commercial or not-for-profit sector.

Patient consent

Written informed consent was obtained from the patient/patient’s mother for publication of this case report.

Author contribution statement

ST, YT, HG and HA contributed to the conception and design of the study. HI and YT treated the patient and collected the data. IO performed immunohistochemical staining and prepared the pathological images.

References

  • 1

    KontogeorgosGMouroutiGKyrodimouELiapi-AvgeriGParasiE. Ganglion cell containing pituitary adenomas: signs of neuronal differentiation in adenoma cells. Acta Neuropathology 2006 2128. (https://doi.org/10.1007/s00401-006-0055-y)

    • Search Google Scholar
    • Export Citation
  • 2

    PuchnerMJLudeckeDKSaegerWRiedelMAsaSL. Gangliocytomas of the sellar region–a review. Experimental and Clinical Endocrinology & Diabetes 1995 129149. (https://doi.org/10.1055/s-0029-1211342)

    • Search Google Scholar
    • Export Citation
  • 3

    YangBYangCSunYDuJLiuPJiaGJiaWZhangYWangJXuY Mixed gangliocytoma-pituitary adenoma in the sellar region: a large-scale single-center experience. Acta Neurochirurgica 2018 19891999. (https://doi.org/10.1007/s00701-018-3632-7)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 4

    TowfighiJSalamMMMcLendonREPowersSPageRB. Ganglion cell-containing tumors of the pituitary gland. Archives of Pathology & Laboratory Medicine 1996 369377.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 5

    HorvathEKovacsKScheithauerBWLloydRVSmythHS. Pituitary adenoma with neuronal choristoma (PANCH): composite lesion or lineage infidelity? Ultrastructural Pathology 1994 565574. (https://doi.org/10.3109/01913129409021900)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 6

    KurosakiMSaegerWLudeckeDK. Intrasellar gangliocytomas associated with acromegaly. Brain Tumor Pathology 2002 6367. (https://doi.org/10.1007/BF02478929)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 7

    KnospESteinerEKitzKMatulaC. Pituitary adenomas with invasion of the cavernous sinus space: a magnetic resonance imaging classification compared with surgical findings. Neurosurgery 1993 610617; discussion 617618. (https://doi.org/10.1227/00006123-199310000-00008)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 8

    GiustinaAChansonPBronsteinMDKlibanskiALambertsSCasanuevaFFTrainerPGhigoEHoKMelmedS A consensus on criteria for cure of acromegaly. Journal of Clinical Endocrinology & Metabolism 2010 31413148. (https://doi.org/10.1210/jc.2009-2670)

    • Search Google Scholar
    • Export Citation
  • 9

    KatznelsonLLawsER JrMelmedSMolitchMEMuradMHUtzAWassJA & Endocrine Society. Acromegaly: an endocrine society clinical practice guideline. Journal of Clinical Endocrinology & Metabolism 2014 39333951. (https://doi.org/10.1210/jc.2014-2700)

    • Search Google Scholar
    • Export Citation
  • 10

    AsaSLScheithauerBWBilbaoJMHorvathERyanNKovacsKRandallRVLawsER JrSingerWLinfootJA. A case for hypothalamic acromegaly: a clinicopathological study of six patients with hypothalamic gangliocytomas producing growth hormone-releasing factor. Journal of Clinical Endocrinology & Metabolism 1984 796803. (https://doi.org/10.1210/jcem-58-5-796)

    • Search Google Scholar
    • Export Citation
  • 11

    SaegerWPuchnerMJLudeckeDK. Combined sellar gangliocytoma and pituitary adenoma in acromegaly or Cushing's disease. A report of 3 cases. Virchows Archiv 1994 9399.

    • Search Google Scholar
    • Export Citation
  • 12

    AsadaHOtaniMFuruhataSInoueHToyaSOgawaY. Mixed pituitary adenoma and gangliocytoma associated with acromegaly–case report. Neurologia Medico-Chirurgica 1990 628632. (https://doi.org/10.2176/nmc.30.628)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 13

    BevanJSAsaSLRossiMLEsiriMMAdamsCBBurkeCW. Intrasellar gangliocytoma containing gastrin and growth hormone-releasing hormone associated with a growth hormone-secreting pituitary adenoma. Clinical Endocrinology 1989 213224. (https://doi.org/10.1111/j.1365-2265.1989.tb02229.x)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 14

    IwaseTNishizawaSBabaSHinokumaKSugimuraHNakamuraSUemuraKShirasawaHKinoI. Intrasellar neuronal choristoma associated with growth hormone-producing pituitary adenoma containing amyloid deposits. Human Pathology 1995 925928. (https://doi.org/10.1016/0046-8177(95)90018-7)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 15

    LiJYRacadotOKujasMKouadriMPeillonFRacadotJ. Immunocytochemistry of four mixed pituitary adenomas and intrasellar gangliocytomas associated with different clinical syndromes: acromegaly, amenorrhea-galactorrhea, Cushing's disease and isolated tumoral syndrome. Acta Neuropathologica 1989 320328. (https://doi.org/10.1007/bf00687585)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 16

    LunaVMoralesFLuengoLMSanzADiazJ. Pituitary gangliocytoma-adenoma presenting with acromegaly: response to treatment. Archives of Internal Medicine 2001 10101011. (https://doi.org/10.1001/archinte.161.7.1010)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 17

    MorikawaMTamakiNKokunaiTImaiY. Intrasellar pituitary gangliocyto-adenoma presenting with acromegaly: case report. Neurosurgery 1997 611614; discussion 614615. (https://doi.org/10.1097/00006123-199703000-00036)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 18

    SaegerWLüdeckeDKLosaM. Combined neuronal and endocrine tumors of the sellar region. Der Pathologe 1997 419424. (https://doi.org/10.1007/s002920050236)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 19

    SlowikFFazekasIBálintKGazsóLPásztorECzirjákSLapisK. Intrasellar hamartoma associated with pituitary adenoma. Acta Neuropathologica 1990 328333. (https://doi.org/10.1007/bf00294652)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 20

    LopesMBSloanEPolderJ. Mixed gangliocytoma-pituitary adenoma: insights on the pathogenesis of a rare sellar tumor. American Journal of Surgical Pathology 2017 586595. (https://doi.org/10.1097/PAS.0000000000000806)

    • Search Google Scholar
    • Export Citation
  • 21

    SergeantCJublancCLeclercqDBochALBielleFRaverotGDalyAFTrouillasJVillaC. Transdifferentiation of neuroendocrine cells: gangliocytoma associated with two pituitary adenomas of different lineage in MEN1. American Journal of Surgical Pathology 2017 849853. (https://doi.org/10.1097/PAS.0000000000000803)

    • Search Google Scholar
    • Export Citation

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    Histopathological examination of the pituitary tumor. (A) Hematoxylin and eosin staining showing relatively large cells and pituitary adenoma cells adjacent and mixed within the boundary area. (B) Immunostaining for microtubule-associated protein 2 demonstrating positivity in large cells, indicating the presence of gangliocytoma. Immunostaining for growth hormone showing positivity but weak reactivity in pituitary adenoma cells (C) and CAM 5.2 immunostaining showing strong dot-like positive pattern (D), indicating the sparsely granulated subtype of pituitary somatotroph adenoma. Scale bar = 50 μm.

  • View in gallery

    Immunohistochemical demonstration of growth hormone-releasing hormone (GHRH). Immunohistochemical staining using a pair of mirror section images showing no correspondence of microtubule-associated protein 2-positive (A) and GHRH-positive (B) cells, but demonstrating correspondence of growth hormone (GH)-positive (C) and GHRH-positive (D) cells. Double immunofluorescence staining for GH (E) and GHRH (F) revealing cells with colocalization (G). Arrowheads, colocalized cells. Scale bar = 50 μm in A–D; 20 μm in E–G.

References

  • 1

    KontogeorgosGMouroutiGKyrodimouELiapi-AvgeriGParasiE. Ganglion cell containing pituitary adenomas: signs of neuronal differentiation in adenoma cells. Acta Neuropathology 2006 2128. (https://doi.org/10.1007/s00401-006-0055-y)

    • Search Google Scholar
    • Export Citation
  • 2

    PuchnerMJLudeckeDKSaegerWRiedelMAsaSL. Gangliocytomas of the sellar region–a review. Experimental and Clinical Endocrinology & Diabetes 1995 129149. (https://doi.org/10.1055/s-0029-1211342)

    • Search Google Scholar
    • Export Citation
  • 3

    YangBYangCSunYDuJLiuPJiaGJiaWZhangYWangJXuY Mixed gangliocytoma-pituitary adenoma in the sellar region: a large-scale single-center experience. Acta Neurochirurgica 2018 19891999. (https://doi.org/10.1007/s00701-018-3632-7)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 4

    TowfighiJSalamMMMcLendonREPowersSPageRB. Ganglion cell-containing tumors of the pituitary gland. Archives of Pathology & Laboratory Medicine 1996 369377.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 5

    HorvathEKovacsKScheithauerBWLloydRVSmythHS. Pituitary adenoma with neuronal choristoma (PANCH): composite lesion or lineage infidelity? Ultrastructural Pathology 1994 565574. (https://doi.org/10.3109/01913129409021900)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 6

    KurosakiMSaegerWLudeckeDK. Intrasellar gangliocytomas associated with acromegaly. Brain Tumor Pathology 2002 6367. (https://doi.org/10.1007/BF02478929)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 7

    KnospESteinerEKitzKMatulaC. Pituitary adenomas with invasion of the cavernous sinus space: a magnetic resonance imaging classification compared with surgical findings. Neurosurgery 1993 610617; discussion 617618. (https://doi.org/10.1227/00006123-199310000-00008)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 8

    GiustinaAChansonPBronsteinMDKlibanskiALambertsSCasanuevaFFTrainerPGhigoEHoKMelmedS A consensus on criteria for cure of acromegaly. Journal of Clinical Endocrinology & Metabolism 2010 31413148. (https://doi.org/10.1210/jc.2009-2670)

    • Search Google Scholar
    • Export Citation
  • 9

    KatznelsonLLawsER JrMelmedSMolitchMEMuradMHUtzAWassJA & Endocrine Society. Acromegaly: an endocrine society clinical practice guideline. Journal of Clinical Endocrinology & Metabolism 2014 39333951. (https://doi.org/10.1210/jc.2014-2700)

    • Search Google Scholar
    • Export Citation
  • 10

    AsaSLScheithauerBWBilbaoJMHorvathERyanNKovacsKRandallRVLawsER JrSingerWLinfootJA. A case for hypothalamic acromegaly: a clinicopathological study of six patients with hypothalamic gangliocytomas producing growth hormone-releasing factor. Journal of Clinical Endocrinology & Metabolism 1984 796803. (https://doi.org/10.1210/jcem-58-5-796)

    • Search Google Scholar
    • Export Citation
  • 11

    SaegerWPuchnerMJLudeckeDK. Combined sellar gangliocytoma and pituitary adenoma in acromegaly or Cushing's disease. A report of 3 cases. Virchows Archiv 1994 9399.

    • Search Google Scholar
    • Export Citation
  • 12

    AsadaHOtaniMFuruhataSInoueHToyaSOgawaY. Mixed pituitary adenoma and gangliocytoma associated with acromegaly–case report. Neurologia Medico-Chirurgica 1990 628632. (https://doi.org/10.2176/nmc.30.628)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 13

    BevanJSAsaSLRossiMLEsiriMMAdamsCBBurkeCW. Intrasellar gangliocytoma containing gastrin and growth hormone-releasing hormone associated with a growth hormone-secreting pituitary adenoma. Clinical Endocrinology 1989 213224. (https://doi.org/10.1111/j.1365-2265.1989.tb02229.x)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 14

    IwaseTNishizawaSBabaSHinokumaKSugimuraHNakamuraSUemuraKShirasawaHKinoI. Intrasellar neuronal choristoma associated with growth hormone-producing pituitary adenoma containing amyloid deposits. Human Pathology 1995 925928. (https://doi.org/10.1016/0046-8177(95)90018-7)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 15

    LiJYRacadotOKujasMKouadriMPeillonFRacadotJ. Immunocytochemistry of four mixed pituitary adenomas and intrasellar gangliocytomas associated with different clinical syndromes: acromegaly, amenorrhea-galactorrhea, Cushing's disease and isolated tumoral syndrome. Acta Neuropathologica 1989 320328. (https://doi.org/10.1007/bf00687585)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 16

    LunaVMoralesFLuengoLMSanzADiazJ. Pituitary gangliocytoma-adenoma presenting with acromegaly: response to treatment. Archives of Internal Medicine 2001 10101011. (https://doi.org/10.1001/archinte.161.7.1010)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 17

    MorikawaMTamakiNKokunaiTImaiY. Intrasellar pituitary gangliocyto-adenoma presenting with acromegaly: case report. Neurosurgery 1997 611614; discussion 614615. (https://doi.org/10.1097/00006123-199703000-00036)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 18

    SaegerWLüdeckeDKLosaM. Combined neuronal and endocrine tumors of the sellar region. Der Pathologe 1997 419424. (https://doi.org/10.1007/s002920050236)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 19

    SlowikFFazekasIBálintKGazsóLPásztorECzirjákSLapisK. Intrasellar hamartoma associated with pituitary adenoma. Acta Neuropathologica 1990 328333. (https://doi.org/10.1007/bf00294652)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 20

    LopesMBSloanEPolderJ. Mixed gangliocytoma-pituitary adenoma: insights on the pathogenesis of a rare sellar tumor. American Journal of Surgical Pathology 2017 586595. (https://doi.org/10.1097/PAS.0000000000000806)

    • Search Google Scholar
    • Export Citation
  • 21

    SergeantCJublancCLeclercqDBochALBielleFRaverotGDalyAFTrouillasJVillaC. Transdifferentiation of neuroendocrine cells: gangliocytoma associated with two pituitary adenomas of different lineage in MEN1. American Journal of Surgical Pathology 2017 849853. (https://doi.org/10.1097/PAS.0000000000000803)

    • Search Google Scholar
    • Export Citation

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