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Published in: Acta Neurochirurgica 11/2017

01-11-2017 | Original Article - Brain Tumors

Implications of the World Health Organization definition of atypia on surgically treated functional and non-functional pituitary adenomas

Authors: Sauradeep Sarkar, Vinu Joe Philip, Sai Kiran Cherukuri, Ari George Chacko, Geeta Chacko

Published in: Acta Neurochirurgica | Issue 11/2017

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Abstract

Background

The World Health Organization (WHO) defines atypical pituitary adenomas as tumours with a MIB-1 labelling index ≥3%, p53 positivity and increased mitotic activity. Although a few reports have described the clinical and radiological correlates of atypia in pituitary adenomas, its impact on postoperative outcomes is not clearly defined.

Method

We reviewed preoperative and postoperative records of patients undergoing surgery for pituitary adenomas. Postoperative outcomes for functional adenomas (FPAs) were assessed according to contemporary definitions of remission and recurrence. For non-functional pituitary adenomas (NFPAs), extent of resection and disease progression were defined on the basis of postoperative magnetic resonance imaging.

Results

Of 394 patients included for analysis, 29 cases (7.4%) fulfilled criteria for atypia. Patients with atypical tumours were significantly younger than those with typical adenomas. Remission was possible in 47.4% of FPAs, and was unrelated to the presence of atypia. In NFPAs, local invasiveness was negatively associated with extent of resection (OR, 0.255; 95% CI, 0.086–0.753; p < 0.001). In 93 NFPAs followed postoperatively with serial imaging over a mean duration of 37.5 months, disease progression/recurrence was significantly associated with the presence of atypia (OR, 5.058; 95% CI, 1.273–20.098; p = 0.021) on multivariate analysis.

Conclusions

Patients with atypical non-functional pituitary adenomas are at risk for postoperative recurrence and disease progression, suggesting a need for adjuvant therapy. However, only a small fraction of pituitary tumours demonstrate atypia, as defined by the WHO, limiting its clinical utility.
Literature
1.
go back to reference Alahmadi H, Lee D, Wilson JR, Hayhurst C, Mete O, Gentili F, Asa SL, Zadeh G (2012) Clinical features of silent corticotroph adenomas. Acta Neurochir (Wein) 154:1493–1498CrossRef Alahmadi H, Lee D, Wilson JR, Hayhurst C, Mete O, Gentili F, Asa SL, Zadeh G (2012) Clinical features of silent corticotroph adenomas. Acta Neurochir (Wein) 154:1493–1498CrossRef
2.
go back to reference Batisse M, Raverot G, Maqdasy S, Durando X, Sturm N, Montoriol PF, Kemeny JL, Chazal J, Trouillas J, Tauveron I (2013) Aggressive silent GH pituitary tumor resistant to multiple treatments, including temozolomide. Cancer Investig 31:190–196CrossRef Batisse M, Raverot G, Maqdasy S, Durando X, Sturm N, Montoriol PF, Kemeny JL, Chazal J, Trouillas J, Tauveron I (2013) Aggressive silent GH pituitary tumor resistant to multiple treatments, including temozolomide. Cancer Investig 31:190–196CrossRef
3.
go back to reference Brochier S, Galland F, Kujas M, Parker F, Gaillard S, Raftopoulos C, Young J, Alexopoulou O, Maiter D, Chanson P (2010) Factors predicting relapse of nonfunctioning pituitary macroadenomas after neurosurgery: a study of 142 patients. Eur J Endocrinol 163:193–200CrossRefPubMed Brochier S, Galland F, Kujas M, Parker F, Gaillard S, Raftopoulos C, Young J, Alexopoulou O, Maiter D, Chanson P (2010) Factors predicting relapse of nonfunctioning pituitary macroadenomas after neurosurgery: a study of 142 patients. Eur J Endocrinol 163:193–200CrossRefPubMed
4.
go back to reference Chacko G, Chacko AG, Kovacs K, Scheithauer BW, Mani S, Muliyil J, Seshadri M (2010) The clinical significance of MIB-1 labeling index in pituitary adenomas. Pituitary 13:337–344CrossRefPubMed Chacko G, Chacko AG, Kovacs K, Scheithauer BW, Mani S, Muliyil J, Seshadri M (2010) The clinical significance of MIB-1 labeling index in pituitary adenomas. Pituitary 13:337–344CrossRefPubMed
5.
go back to reference Chang EF, Zada G, Kim S, Lamborn KR, Quinones-Hinojosa A, Tyrrell JB, Wilson CB, Kunwar S (2008) Long-term recurrence and mortality after surgery and adjuvant radiotherapy for nonfunctional pituitary adenomas. J Neurosurg 108:736–745CrossRefPubMed Chang EF, Zada G, Kim S, Lamborn KR, Quinones-Hinojosa A, Tyrrell JB, Wilson CB, Kunwar S (2008) Long-term recurrence and mortality after surgery and adjuvant radiotherapy for nonfunctional pituitary adenomas. J Neurosurg 108:736–745CrossRefPubMed
6.
go back to reference Chinezu L, Jouanneau E, Vasiljevic A, Trouillas J, Raverot G (2013) Silent GH pituitary tumor: diagnostic and therapeutic challenges. Ann Endocrinol (Paris) 74:491–495CrossRef Chinezu L, Jouanneau E, Vasiljevic A, Trouillas J, Raverot G (2013) Silent GH pituitary tumor: diagnostic and therapeutic challenges. Ann Endocrinol (Paris) 74:491–495CrossRef
7.
go back to reference Chinezu L, Vasiljevic A, Trouillas J, Lapoirie M, Jouanneau E, Raverot G (2017) Silent somatotroph tumour revisited from a study of 80 patients with and without acromegaly and a review of the literature. Eur J Endocrinol 176:195–201CrossRefPubMed Chinezu L, Vasiljevic A, Trouillas J, Lapoirie M, Jouanneau E, Raverot G (2017) Silent somatotroph tumour revisited from a study of 80 patients with and without acromegaly and a review of the literature. Eur J Endocrinol 176:195–201CrossRefPubMed
8.
go back to reference Cho HY, Cho SW, Kim SW, Shin CS, Park KS, Kim SY (2010) Silent corticotroph adenomas have unique recurrence characteristics compared with other nonfunctioning pituitary adenomas. Clin Endocrinol 72:648–653CrossRef Cho HY, Cho SW, Kim SW, Shin CS, Park KS, Kim SY (2010) Silent corticotroph adenomas have unique recurrence characteristics compared with other nonfunctioning pituitary adenomas. Clin Endocrinol 72:648–653CrossRef
9.
go back to reference De Caro MDB, Solari D, Pagliuca F, Villa A, Guadagno E, Cavallo LM, Colao A, Pettinato G, Cappabianca P (2017) Atypical pituitary adenomas: clinical characteristics and role of Ki-67 and p53 in prognostic and therapeutic evaluation. A series of 50 patients. Neurosurg Rev 40:105–114CrossRef De Caro MDB, Solari D, Pagliuca F, Villa A, Guadagno E, Cavallo LM, Colao A, Pettinato G, Cappabianca P (2017) Atypical pituitary adenomas: clinical characteristics and role of Ki-67 and p53 in prognostic and therapeutic evaluation. A series of 50 patients. Neurosurg Rev 40:105–114CrossRef
10.
go back to reference De Paiva Neto MA, Vandergrift A, Fatemi N, Gorgulho AA, DeSalles AA, Cohan P, Wang C, Swerdloff R, Kelly DF (2010) Endonasal transsphenoidal surgery and multimodality treatment for giant pituitary adenomas. Clin Endocrinol 72:512–519CrossRef De Paiva Neto MA, Vandergrift A, Fatemi N, Gorgulho AA, DeSalles AA, Cohan P, Wang C, Swerdloff R, Kelly DF (2010) Endonasal transsphenoidal surgery and multimodality treatment for giant pituitary adenomas. Clin Endocrinol 72:512–519CrossRef
11.
go back to reference Dekkers O, Pereira A, Roelfsema F, Voormolen J, Neelis K, Schroijen M, Smit J, Romijn J (2006) Observation alone after transsphenoidal surgery for nonfunctioning pituitary macroadenoma. J Clin Endocrinol Metab 91:1796–1801CrossRefPubMed Dekkers O, Pereira A, Roelfsema F, Voormolen J, Neelis K, Schroijen M, Smit J, Romijn J (2006) Observation alone after transsphenoidal surgery for nonfunctioning pituitary macroadenoma. J Clin Endocrinol Metab 91:1796–1801CrossRefPubMed
12.
go back to reference DeLellis RA (2004) Pathology and genetics of tumours of endocrine organs. IARC Press, Lyon DeLellis RA (2004) Pathology and genetics of tumours of endocrine organs. IARC Press, Lyon
13.
go back to reference Figarella-Branger D, Trouillas J (2006) The new WHO classification of human pituitary tumors: comments. Acta Neuropathol 111:71–72CrossRefPubMed Figarella-Branger D, Trouillas J (2006) The new WHO classification of human pituitary tumors: comments. Acta Neuropathol 111:71–72CrossRefPubMed
14.
go back to reference Gejman R, Swearingen B, Hedley-Whyte ET (2008) Role of Ki-67 proliferation index and p53 expression in predicting progression of pituitary adenomas. Hum Pathol 39:758–766CrossRefPubMed Gejman R, Swearingen B, Hedley-Whyte ET (2008) Role of Ki-67 proliferation index and p53 expression in predicting progression of pituitary adenomas. Hum Pathol 39:758–766CrossRefPubMed
15.
go back to reference Grossman AB (2006) The 2004 World Health Organization classification of pituitary tumors: is it clinically helpful? Acta Neuropathol 111:76–77CrossRefPubMed Grossman AB (2006) The 2004 World Health Organization classification of pituitary tumors: is it clinically helpful? Acta Neuropathol 111:76–77CrossRefPubMed
16.
go back to reference Hadzhiyanev A, Ivanova R, Nachev E, Elenkova A, Yaneva M, Zaharieva S, Marinov M, Surchev J, Ivanova A (2014) Evaluation of prognostic utility of MIB-1 and p53 expression in pituitary adenomas: correlations with clinical behaviour and follow-up results. Biotechnol Biotechnol Equip 28:502–507CrossRefPubMedPubMedCentral Hadzhiyanev A, Ivanova R, Nachev E, Elenkova A, Yaneva M, Zaharieva S, Marinov M, Surchev J, Ivanova A (2014) Evaluation of prognostic utility of MIB-1 and p53 expression in pituitary adenomas: correlations with clinical behaviour and follow-up results. Biotechnol Biotechnol Equip 28:502–507CrossRefPubMedPubMedCentral
17.
go back to reference Hentschel SJ, McCutcheon IE, Moore W, Durity FA (2003) P53 and MIB-1 immunohistochemistry as predictors of the clinical behavior of nonfunctioning pituitary adenomas. Can J Neurol Sci 30:215–219CrossRefPubMed Hentschel SJ, McCutcheon IE, Moore W, Durity FA (2003) P53 and MIB-1 immunohistochemistry as predictors of the clinical behavior of nonfunctioning pituitary adenomas. Can J Neurol Sci 30:215–219CrossRefPubMed
18.
go back to reference Hofstetter CP, Nanaszko MJ, Mubita LL, Tsiouris J, Anand VK, Schwartz TH (2012) Volumetric classification of pituitary macroadenomas predicts outcome and morbidity following endoscopic endonasal transsphenoidal surgery. Pituitary 15:450–463CrossRefPubMed Hofstetter CP, Nanaszko MJ, Mubita LL, Tsiouris J, Anand VK, Schwartz TH (2012) Volumetric classification of pituitary macroadenomas predicts outcome and morbidity following endoscopic endonasal transsphenoidal surgery. Pituitary 15:450–463CrossRefPubMed
19.
go back to reference Hofstetter CP, Shin BJ, Mubita L, Huang C, Anand VK, Boockvar JA, Schwartz TH (2011) Endoscopic endonasal transsphenoidal surgery for functional pituitary adenomas. Neurosurg Focus 30:E10CrossRefPubMed Hofstetter CP, Shin BJ, Mubita L, Huang C, Anand VK, Boockvar JA, Schwartz TH (2011) Endoscopic endonasal transsphenoidal surgery for functional pituitary adenomas. Neurosurg Focus 30:E10CrossRefPubMed
20.
go back to reference Honegger J, Prettin C, Feuerhake F, Petrick M, Schulte-Mönting J, Reincke M (2003) Expression of Ki-67 antigen in nonfunctioning pituitary adenomas: correlation with growth velocity and invasiveness. J Neurosurg 99:674–679CrossRefPubMed Honegger J, Prettin C, Feuerhake F, Petrick M, Schulte-Mönting J, Reincke M (2003) Expression of Ki-67 antigen in nonfunctioning pituitary adenomas: correlation with growth velocity and invasiveness. J Neurosurg 99:674–679CrossRefPubMed
21.
go back to reference Ioachimescu AG, Eiland L, Chhabra VS, Mastrogianakis GM, Schniederjan MJ, Brat D, Pileggi AV, Oyesiku NM (2012) Silent corticotroph adenomas: Emory University cohort and comparison with ACTH-negative nonfunctioning pituitary adenomas. Neurosurgery 71:296–304CrossRefPubMed Ioachimescu AG, Eiland L, Chhabra VS, Mastrogianakis GM, Schniederjan MJ, Brat D, Pileggi AV, Oyesiku NM (2012) Silent corticotroph adenomas: Emory University cohort and comparison with ACTH-negative nonfunctioning pituitary adenomas. Neurosurgery 71:296–304CrossRefPubMed
22.
go back to reference Jane JA Jr, Starke RM, Elzoghby MA, Reames DL, Payne SC, Thorner MO, Marshall JC, Laws ER Jr, Vance ML (2011) Endoscopic transsphenoidal surgery for acromegaly: remission using modern criteria, complications, and predictors of outcome. J Clin Endocrinol Metab 96:2732–2740CrossRefPubMed Jane JA Jr, Starke RM, Elzoghby MA, Reames DL, Payne SC, Thorner MO, Marshall JC, Laws ER Jr, Vance ML (2011) Endoscopic transsphenoidal surgery for acromegaly: remission using modern criteria, complications, and predictors of outcome. J Clin Endocrinol Metab 96:2732–2740CrossRefPubMed
23.
go back to reference Kakade HR, Kasaliwal R, Khadilkar KS, Jadhav S, Bukan A, Khare S, Budyal SR, Goel A, Lila AR, Bandgar T (2014) Clinical, biochemical and imaging characteristics of Cushing’s macroadenomas and their long-term treatment outcome. Clin Endocrinol 81:336–342CrossRef Kakade HR, Kasaliwal R, Khadilkar KS, Jadhav S, Bukan A, Khare S, Budyal SR, Goel A, Lila AR, Bandgar T (2014) Clinical, biochemical and imaging characteristics of Cushing’s macroadenomas and their long-term treatment outcome. Clin Endocrinol 81:336–342CrossRef
24.
go back to reference Kleinschmidt-DeMasters B (2006) Subtyping does matter in pituitary adenomas. Acta Neuropathol 111:84–85CrossRefPubMed Kleinschmidt-DeMasters B (2006) Subtyping does matter in pituitary adenomas. Acta Neuropathol 111:84–85CrossRefPubMed
25.
go back to reference Knosp E, Steiner E, Kitz K, Matula C (1993) Pituitary adenomas with invasion of the cavernous sinus space: a magnetic resonance imaging classification compared with surgical findings. Neurosurgery 33:610–618CrossRefPubMed Knosp E, Steiner E, Kitz K, Matula C (1993) Pituitary adenomas with invasion of the cavernous sinus space: a magnetic resonance imaging classification compared with surgical findings. Neurosurgery 33:610–618CrossRefPubMed
26.
go back to reference Kontogeorgos G (2006) Innovations and controversies in the WHO classification of pituitary adenomas. Acta Neuropathol 111:73–75CrossRefPubMed Kontogeorgos G (2006) Innovations and controversies in the WHO classification of pituitary adenomas. Acta Neuropathol 111:73–75CrossRefPubMed
27.
go back to reference Kovacs K (2006) The 2004 WHO classification of pituitary tumors: comments. Acta Neuropathol 111:62–63CrossRefPubMed Kovacs K (2006) The 2004 WHO classification of pituitary tumors: comments. Acta Neuropathol 111:62–63CrossRefPubMed
28.
go back to reference Laws ER, Lopes MBS (2006) The new WHO classification of pituitary tumors: highlights and areas of controversy. Acta Neuropathol 111:80–81CrossRefPubMed Laws ER, Lopes MBS (2006) The new WHO classification of pituitary tumors: highlights and areas of controversy. Acta Neuropathol 111:80–81CrossRefPubMed
29.
go back to reference Losa M, Franzin A, Mangili F, Terreni MR, Barzaghi R, Veglia F, Mortini P, Giovanelli M (2000) Proliferation index of nonfunctioning pituitary adenomas: correlations with clinical characteristics and long-term follow-up results. Neurosurgery 47:1313–1319CrossRefPubMed Losa M, Franzin A, Mangili F, Terreni MR, Barzaghi R, Veglia F, Mortini P, Giovanelli M (2000) Proliferation index of nonfunctioning pituitary adenomas: correlations with clinical characteristics and long-term follow-up results. Neurosurgery 47:1313–1319CrossRefPubMed
30.
go back to reference Losa M, Mortini P, Barzaghi R, Ribotto P, Terreni MR, Marzoli SB, Pieralli S, Giovanelli M (2008) Early results of surgery in patients with nonfunctioning pituitary adenoma and analysis of the risk of tumor recurrence. J Neurosurg 108:525–532CrossRefPubMed Losa M, Mortini P, Barzaghi R, Ribotto P, Terreni MR, Marzoli SB, Pieralli S, Giovanelli M (2008) Early results of surgery in patients with nonfunctioning pituitary adenoma and analysis of the risk of tumor recurrence. J Neurosurg 108:525–532CrossRefPubMed
31.
go back to reference Mindermann T, Kovacs K, Wilson CB (1994) Changes in the immunophenotype of recurrent pituitary adenomas. Neurosurgery 35:39–44CrossRefPubMed Mindermann T, Kovacs K, Wilson CB (1994) Changes in the immunophenotype of recurrent pituitary adenomas. Neurosurgery 35:39–44CrossRefPubMed
32.
go back to reference Ozer E, Canda MS, Ulukus C, Guray M, Erbayraktar S (2003) Expression of Bcl-2, Bax and p53 proteins in pituitary adenomas: an immunohistochemical study. Tumori 89:54–59PubMed Ozer E, Canda MS, Ulukus C, Guray M, Erbayraktar S (2003) Expression of Bcl-2, Bax and p53 proteins in pituitary adenomas: an immunohistochemical study. Tumori 89:54–59PubMed
33.
go back to reference Park P, Chandler WF, Barkan AL, Orrego JJ, Cowan JA, Griffith KA, Tsien C (2004) The role of radiation therapy after surgical resection of nonfunctional pituitary macroadenomas. Neurosurgery 55:100–107CrossRefPubMed Park P, Chandler WF, Barkan AL, Orrego JJ, Cowan JA, Griffith KA, Tsien C (2004) The role of radiation therapy after surgical resection of nonfunctional pituitary macroadenomas. Neurosurgery 55:100–107CrossRefPubMed
34.
go back to reference Perry A, Scheithauer BW (2006) Commentary: classification and grading of pituitary tumors. Observations of two working neuropathologists. Acta Neuropathol 111:68–70CrossRefPubMed Perry A, Scheithauer BW (2006) Commentary: classification and grading of pituitary tumors. Observations of two working neuropathologists. Acta Neuropathol 111:68–70CrossRefPubMed
35.
go back to reference Ragel BT, Couldwell WT (2004) Pituitary carcinoma: a review of the literature. Neurosurg Focus 16:E7CrossRefPubMed Ragel BT, Couldwell WT (2004) Pituitary carcinoma: a review of the literature. Neurosurg Focus 16:E7CrossRefPubMed
36.
go back to reference Salehi F, Agur A, Scheithauer BW, Kovacs K, Lloyd RV, Cusimano M (2009) Ki-67 in pituitary neoplasms: a review—part I. Neurosurgery 65:429–437CrossRefPubMed Salehi F, Agur A, Scheithauer BW, Kovacs K, Lloyd RV, Cusimano M (2009) Ki-67 in pituitary neoplasms: a review—part I. Neurosurgery 65:429–437CrossRefPubMed
37.
go back to reference Sarkar S, Rajaratnam S, Chacko G, Chacko AG (2014) Endocrinological outcomes following endoscopic and microscopic transsphenoidal surgery in 113 patients with acromegaly. Clin Neurol Neurosurg 126:190–195CrossRefPubMed Sarkar S, Rajaratnam S, Chacko G, Chacko AG (2014) Endocrinological outcomes following endoscopic and microscopic transsphenoidal surgery in 113 patients with acromegaly. Clin Neurol Neurosurg 126:190–195CrossRefPubMed
38.
go back to reference Scheithauer BW, Gaffey TA, Lloyd RV, Sebo TJ, Kovacs KT, Horvath E, Yapcer Ö, Young WF Jr, Meyer FB, Kuroki T (2006) Pathobiology of pituitary adenomas and carcinomas. Neurosurgery 59:341–353CrossRefPubMed Scheithauer BW, Gaffey TA, Lloyd RV, Sebo TJ, Kovacs KT, Horvath E, Yapcer Ö, Young WF Jr, Meyer FB, Kuroki T (2006) Pathobiology of pituitary adenomas and carcinomas. Neurosurgery 59:341–353CrossRefPubMed
39.
go back to reference Scheithauer BW, Kurtkaya-Yapcer Ö, Kovacs KT, Young WF Jr, Lloyd RV (2005) Pituitary carcinoma: a clinicopathological review. Neurosurgery 56:1066–1074PubMed Scheithauer BW, Kurtkaya-Yapcer Ö, Kovacs KT, Young WF Jr, Lloyd RV (2005) Pituitary carcinoma: a clinicopathological review. Neurosurgery 56:1066–1074PubMed
40.
go back to reference Schwyzer L, Starke RM, Jane JA Jr, Oldfield EH (2015) Percent reduction of growth hormone levels correlates closely with percent resected tumor volume in acromegaly. J Neurosurg 122:798–802CrossRefPubMed Schwyzer L, Starke RM, Jane JA Jr, Oldfield EH (2015) Percent reduction of growth hormone levels correlates closely with percent resected tumor volume in acromegaly. J Neurosurg 122:798–802CrossRefPubMed
41.
go back to reference Tanaka Y, Hongo K, Tada T, Sakai K, Kakizawa Y, Kobayashi S (2003) Growth pattern and rate in residual nonfunctioning pituitary adenomas: correlations among tumor volume doubling time, patient age, and MIB-1 index. J Neurosurg 98:359–365CrossRefPubMed Tanaka Y, Hongo K, Tada T, Sakai K, Kakizawa Y, Kobayashi S (2003) Growth pattern and rate in residual nonfunctioning pituitary adenomas: correlations among tumor volume doubling time, patient age, and MIB-1 index. J Neurosurg 98:359–365CrossRefPubMed
42.
go back to reference Thapar K, Kovacs K, Scheithauer BW, Stefaneanu L, Horvath E, Pernicone PJ, Murray D, Laws ER Jr (1996) Proliferative activity and invasiveness among pituitary adenomas and carcinomas: an analysis using the MIB-1 antibody. Neurosurgery 38:99–107CrossRefPubMed Thapar K, Kovacs K, Scheithauer BW, Stefaneanu L, Horvath E, Pernicone PJ, Murray D, Laws ER Jr (1996) Proliferative activity and invasiveness among pituitary adenomas and carcinomas: an analysis using the MIB-1 antibody. Neurosurgery 38:99–107CrossRefPubMed
43.
go back to reference Thapar K, Scheithauer BW, Kovacs K, Pernicone PJ, Laws ER Jr (1996) p53 expression in pituitary adenomas and carcinomas: correlation with invasiveness and tumor growth fractions. Neurosurgery 38:765–771CrossRefPubMed Thapar K, Scheithauer BW, Kovacs K, Pernicone PJ, Laws ER Jr (1996) p53 expression in pituitary adenomas and carcinomas: correlation with invasiveness and tumor growth fractions. Neurosurgery 38:765–771CrossRefPubMed
44.
go back to reference Trouillas J, Roy P, Sturm N, Dantony E, Cortet-Rudelli C, Viennet G, Bonneville J-F, Assaker R, Auger C, Brue T (2013) A new prognostic clinicopathological classification of pituitary adenomas: a multicentric case–control study of 410 patients with 8 years post-operative follow-up. Acta Neuropathol 126:123–135CrossRefPubMed Trouillas J, Roy P, Sturm N, Dantony E, Cortet-Rudelli C, Viennet G, Bonneville J-F, Assaker R, Auger C, Brue T (2013) A new prognostic clinicopathological classification of pituitary adenomas: a multicentric case–control study of 410 patients with 8 years post-operative follow-up. Acta Neuropathol 126:123–135CrossRefPubMed
45.
go back to reference van Bunderen CC, van Varsseveld NC, Baayen JC, van Furth WR, Aliaga ES, Hazewinkel MJ, Majoie CB, Freling NJ, Lips P, Fliers E (2013) Predictors of endoscopic transsphenoidal surgery outcome in acromegaly: patient and tumor characteristics evaluated by magnetic resonance imaging. Pituitary 16:158–167CrossRefPubMed van Bunderen CC, van Varsseveld NC, Baayen JC, van Furth WR, Aliaga ES, Hazewinkel MJ, Majoie CB, Freling NJ, Lips P, Fliers E (2013) Predictors of endoscopic transsphenoidal surgery outcome in acromegaly: patient and tumor characteristics evaluated by magnetic resonance imaging. Pituitary 16:158–167CrossRefPubMed
46.
go back to reference Widhalm G, Wolfsberger S, Preusser M, Fischer I, Woehrer A, Wunderer J, Hainfellner JA, Knosp E (2009) Residual nonfunctioning pituitary adenomas: prognostic value of MIB-1 labeling index for tumor progression. J Neurosurg 111:563–571CrossRefPubMed Widhalm G, Wolfsberger S, Preusser M, Fischer I, Woehrer A, Wunderer J, Hainfellner JA, Knosp E (2009) Residual nonfunctioning pituitary adenomas: prognostic value of MIB-1 labeling index for tumor progression. J Neurosurg 111:563–571CrossRefPubMed
47.
go back to reference Wolfsberger S, Knosp E (2006) Comments on the WHO 2004 classification of pituitary tumors. Acta Neuropathol 111:66–67CrossRefPubMed Wolfsberger S, Knosp E (2006) Comments on the WHO 2004 classification of pituitary tumors. Acta Neuropathol 111:66–67CrossRefPubMed
48.
go back to reference Wolfsberger S, Wunderer J, Zachenhofer I, Czech T, Böcher-Schwarz H-G, Hainfellner J, Knosp E (2004) Expression of cell proliferation markers in pituitary adenomas–correlation and clinical relevance of MIB-1 and anti-topoisomerase-IIα. Acta Neurochir (Wein) 146:831–839 Wolfsberger S, Wunderer J, Zachenhofer I, Czech T, Böcher-Schwarz H-G, Hainfellner J, Knosp E (2004) Expression of cell proliferation markers in pituitary adenomas–correlation and clinical relevance of MIB-1 and anti-topoisomerase-IIα. Acta Neurochir (Wein) 146:831–839
49.
go back to reference Zada G, Woodmansee WW, Ramkissoon S, Amadio J, Nose V, Laws ER Jr (2011) Atypical pituitary adenomas: incidence, clinical characteristics, and implications: clinical article. J Neurosurg 114:336–344CrossRefPubMed Zada G, Woodmansee WW, Ramkissoon S, Amadio J, Nose V, Laws ER Jr (2011) Atypical pituitary adenomas: incidence, clinical characteristics, and implications: clinical article. J Neurosurg 114:336–344CrossRefPubMed
Metadata
Title
Implications of the World Health Organization definition of atypia on surgically treated functional and non-functional pituitary adenomas
Authors
Sauradeep Sarkar
Vinu Joe Philip
Sai Kiran Cherukuri
Ari George Chacko
Geeta Chacko
Publication date
01-11-2017
Publisher
Springer Vienna
Published in
Acta Neurochirurgica / Issue 11/2017
Print ISSN: 0001-6268
Electronic ISSN: 0942-0940
DOI
https://doi.org/10.1007/s00701-017-3223-z

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