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      Pituitary Adenomas and Invasiveness from Anatomo-Surgical, Radiological, and Histological Perspectives: A Systematic Literature Review

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          Abstract

          Invasiveness in pituitary adenomas has been defined and investigated from multiple perspectives, with varying results when its predictive value is considered. A systematic literature review, following PRISMA guidelines, was performed, searching PubMed and Scopus databases with terms that included molecular markers, histological, radiological, anatomical and surgical data on invasiveness of pituitary adenomas. The results showed that differing views are still present for anatomical aspects of the sellar region that are relevant to the concept of invasiveness; radiological and histological diagnoses are still limited, but might improve in the future, especially if they are related to surgical findings, which have become more accurate thanks to the introduction of the endoscope. The aim is to achieve a correct distinction between truly invasive pituitary adenomas from those that, in contrast, present with extension in the parasellar area through natural pathways. At present, diagnosis of invasiveness should be based on a comprehensive analysis of radiological, intra-operative and histological findings.

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          Pituitary adenomas with invasion of the cavernous sinus space: a magnetic resonance imaging classification compared with surgical findings.

          E Knosp, E Steiner, K Kitz … (1993)
          We present 25 pituitary adenomas that were confirmed surgically to have invaded the cavernous sinus space. The surgical results are compared with the preoperative magnetic resonance imaging findings. For comparable radiological criteria, we classified parasellar growth into five grades. This proposed classification is based on coronal sections of unenhanced and gadolinium diethylene-triamine-pentaacetic acid enhanced magnetic resonance imaging scans, with the readily detectable internal carotid artery serving as the radiological landmark. The anatomical, radiological, and surgical conditions of each grade are considered. Grades 0, 1, 2, and 3 are distinguished from each other by a medial tangent, the intercarotid line--through the cross-sectional centers--and a lateral tangent on the intra- and supracavernous internal carotid arteries. Grade 0 represents the normal condition, and Grade 4 corresponds to the total encasement of the intracavernous carotid artery. According to this classification, surgically proven invasion of the cavernous sinus space was present in all Grade 4 and Grade 3 cases and in all but one of the Grade 2 cases; no invasion was present in Grade 0 and Grade 1 cases. Therefore, the critical area where invasion of the cavernous sinus space becomes very likely and can be proven surgically is located between the intercarotid line and the lateral tangent, which is represented by our Grade 2. We also measured tumor growth rates, using the monoclonal antibody KI-67, which shows a statistically higher proliferation rate (P < 0.001) in adenomas with surgically observed invasion into the cavernous sinus space, as compared with noninvasive adenomas.
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            Invasion of the cavernous sinus space in pituitary adenomas: endoscopic verification and its correlation with an MRI-based classification.

            Alexander Micko, Adelheid Wöhrer, Stefan Wolfsberger … (2015)
            OBJECT An important prognostic factor for the surgical outcome and recurrence of a pituitary adenoma is its invasiveness into parasellar tissue, particularly into the space of the cavernous sinus (CS). The aims of this study were to reevaluate the existing parasellar classifications using an endoscopic technique and to evaluate the clinical and radiological outcomes associated with each grade. METHODS The authors investigated 137 pituitary macroadenomas classified radiologically at least on one side as Grade 1 or higher (parasellar extension) and correlated the surgical findings using an endoscopic technique, with special reference to the invasiveness of the tumor into the CS. In each case, postoperative MRI was performed to evaluate the gross-total resection (GTR) rate and the rate of endocrinological remission (ER) in functioning adenomas. RESULTS The authors found a 16% rate of CS invasion during surgery for these macroadenomas. Adenomas radiologically classified as Grade 1 were found to be invasive in 1.5%, and the GTR/ER rate was 83%/88%. For Grade 2 adenomas, the rate of invasion was 9.9%, and the GTR/ER rate was 71%/60%. For Grade 3 adenomas, the rate of invasion was 37.9%, and the GTR/ER rate was 75%/33%. When the superior compartment of the CS (Grade 3A) was involved, the authors found a rate of invasion that was lower (p < 0.001) than that when the inferior compartment was involved (Grade 3B). The rate of invasion in Grade 3A adenomas was 26.5% with a GTR/ER rate of 85%/67%, whereas for Grade 3B adenomas, the rate of surgically observed invasion was 70.6% with a GTR/ER rate of 64%/0%. All of the Grade 4 adenomas were invasive, and the GTR/ER rate was 0%. A comparison of microscopic and endoscopic techniques revealed no difference in adenomas with Grade 1 or 4 parasellar extension. In Grade 2 adenomas, however, the CS was found by the endoscopic technique to be invaded in 9.9% and by microscopic evaluation to be invaded in 88% (p < 0.001); in Grade 3 adenomas, the difference was 37.9% versus 86%, respectively (p = 0.002). Grade 4 adenomas had a statistically significant lower rate of GTR than those of all the other grades. In case of ER only, Grade 1 adenomas had a statistically significant higher rate of remission than did Grade 3B and Grade 4 adenomas. CONCLUSIONS The proposed classification proved that with increasing grades, the likelihood of surgically observed invasion rises and the chance of GTR and ER decreases. The direct endoscopic view confirmed the low rate of invasion of Grade 1 adenomas but showed significantly lower rates of invasion in Grade 2 and 3 adenomas than those previously found using the microscopic technique. In cases in which the intracavernous internal carotid artery was encased (Grade 4), all the adenomas were invasive and the GTR/ER rate was 0%/0%. The authors suggest the addition of Grades 3A and 3B to distinguish the strikingly different outcomes of adenomas invading the superior CS compartments and those invading the inferior CS compartments.
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              A new prognostic clinicopathological classification of pituitary adenomas: a multicentric case-control study of 410 patients with 8 years post-operative follow-up.

              Jacqueline Trouillas, Pascal Roy, Nathalie Sturm … (2013)
              Pituitary adenomas are currently classified by histological, immunocytochemical and numerous ultrastructural characteristics lacking unequivocal prognostic correlations. We investigated the prognostic value of a new clinicopathological classification with grades based on invasion and proliferation. This retrospective multicentric case-control study comprised 410 patients who had surgery for a pituitary tumour with long-term follow-up. Using pituitary magnetic resonance imaging for diagnosis of cavernous or sphenoid sinus invasion, immunocytochemistry, markers of the cell cycle (Ki-67, mitoses) and p53, tumours were classified according to size (micro, macro and giant), type (PRL, GH, FSH/LH, ACTH and TSH) and grade (grade 1a: non-invasive, 1b: non-invasive and proliferative, 2a: invasive, 2b: invasive and proliferative, and 3: metastatic). The association between patient status at 8-year follow-up and age, sex, and classification was evaluated by two multivariate analyses assessing disease- or recurrence/progression-free status. At 8 years after surgery, 195 patients were disease-free (controls) and 215 patients were not (cases). In 125 of the cases the tumours had recurred or progressed. Analyses of disease-free and recurrence/progression-free status revealed the significant prognostic value (p < 0.001; p < 0.05) of age, tumour type, and grade across all tumour types and for each tumour type. Invasive and proliferative tumours (grade 2b) had a poor prognosis with an increased probability of tumour persistence or progression of 25- or 12-fold, respectively, as compared to non-invasive tumours (grade 1a). This new, easy to use clinicopathological classification of pituitary endocrine tumours has demonstrated its prognostic worth by strongly predicting the probability of post-operative complete remission or tumour progression and so could help clinicians choose the best post-operative therapy.
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                Author and article information

                Journal
                Journal ID (nlm-ta): Cancers (Basel)
                Journal ID (iso-abbrev): Cancers (Basel)
                Journal ID (publisher-id): cancers
                Title: Cancers
                Publisher: MDPI
                ISSN (Electronic): 2072-6694
                Publication date (Electronic): 04 December 2019
                Publication date Collection: December 2019
                Volume: 11
                Issue: 12
                Electronic Location Identifier: 1936
                Affiliations
                [1 ]Neurosurgery, Department of Surgical Specialties, Radiological Sciences and Public Health, University of Brescia, 25123 Brescia, Italy; s.serioli002@ 123456studenti.unibs.it (S.S.); alessandro.fiorindi@ 123456gmail.com (A.F.); antoniobiroli@ 123456yahoo.com (A.B.); claudio.cornali@ 123456unibs.it (C.C.); marco.fontanella@ 123456unibs.it (M.M.F.)
                [2 ]Neurosurgery, Spedali Civili Hospital, 25123 Brescia, Italy
                [3 ]Otorhinolaryngology–Head and Neck Surgery, Department of Surgical Specialties, Radiological Sciences and Public Health, University of Brescia, 25123 Brescia, Italy; davide.mattavelli@ 123456unibs.it (D.M.); 1990marcoferrari@ 123456gmail.com (M.F.); piero.nicolai@ 123456unibs.it (P.N.)
                [4 ]Section of Anatomy and Physiopathology, Department of Clinical and Experimental Sciences, University of Brescia, 25123 Brescia, Italy; barbara.buffoli@ 123456unibs.it (B.B.); luigi.rodella@ 123456unibs.it (L.R.)
                [5 ]Radiology, Department of Surgical Specialties, Radiological Sciences and Public Health, University of Brescia, 25123 Brescia, Italy; roberto.maroldi@ 123456unibs.it
                [6 ]Neuroradiology, Department of Surgical Specialties, Radiological Sciences and Public Health, University of Brescia, 25123 Brescia, Italy; roberto.gasparotti@ 123456unibs.it
                [7 ]Section of Pathology, Department of Molecular and Translational Medicine, University of Brescia, 25123 Brescia, Italy
                Author notes
                [* ]Correspondence: francesco.doglietto@ 123456unibs.it (F.D.); luigi.poliani@ 123456unibs.it (P.L.P.); Tel.: +39-0303995587 (F.D.); +39-0303998497 (P.L.P.)
                [†]

                These authors equally contributed to the study.

                Author information
                https://orcid.org/0000-0002-7438-0734
                https://orcid.org/0000-0001-7023-6746
                https://orcid.org/0000-0002-8531-7730
                https://orcid.org/0000-0002-4023-0121
                https://orcid.org/0000-0002-5662-8978
                Article
                Publisher ID: cancers-11-01936
                DOI: 10.3390/cancers11121936
                PMC ID: 6966643
                PubMed ID: 31817110
                SO-VID: 82f6f215-e9c1-4916-8c37-8d1cdcac389c
                Copyright © © 2019 by the authors.
                License:

                Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license ( http://creativecommons.org/licenses/by/4.0/).

                History
                Date received : 15 October 2019
                Date accepted : 28 November 2019
                Categories
                Subject: Review

                Keywords: anatomy,cavernous sinus,classification,diagnosis,histology,invasiveness,pituitary adenoma,pitnet,radiology,surgery
                Data availability:
                Keywords: anatomy, cavernous sinus, classification, diagnosis, histology, invasiveness, pituitary adenoma, pitnet, radiology, surgery

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