A New Endoscopic Surgical Classification and Invasion Criteria for Pituitary Adenomas Involving the Cavernous Sinus

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    Or g nal I nvest gat ons

    Turkish Neurosurgery 2011, Vol: 21, No: 3, 330-339330

    ABSTRACT

    AIM:There are two major problems for the pituitary adenomas invading the Cavernous Sinus (CS); differentiation of extension and invasionand inability to demonstrate the medial wall via preoperative imaging methods. Two important corridors are defined in endoscopic cavernoussinus approaches; the lateral and medial corridor.

    MATERIAL and METHODS: A retrospective analysis was performed in 400 endoscopic transphenoidal approaches and 360 pituitary adenomasunderwent endoscopic transphenoidal surgery in our department between September 1997 and December 2010. 48 patients affected by thetumours involving the cavernous sinus were included in this study.

    RESULTS: We performed an intraoperative evaluation of cavernous sinus invasion considering visualization of the medial wall defect,intracavernous ICA segments, minor tumour extensions through small focal pit holes of the medial wall of CS or confirming carotid segmentsof CS by micro-doppler. Cavernous sinus involvement was classified into three types according to the medial and lateral corridor extension ofthe tumor as 25 isolated medial corridor involvement (Type I), 5 isolated lateral corridor involvement (Type II) and 18 total involvement (TypeIII).

    CONCLUSION:Our classification depends on fully surgical endoscopic approach supported by neuroimaging techniques and anatomical

    studies and shows a good predictive value for all cavernous sinus involvement.KEYWORDS:Endoscope, Pituitary adenoma, Cavernous sinus, Transphenoidal approach

    Z

    AMA: Kavernz sins invaze eden hipofiz adenomlar iin iki nemli sorun vardr; ekstansiyonla invazyonun ayrlmas ve preoperatifgrntleme yntemleriyle medial duvarn gsterilememesi. Endoskopik kavernz sinus yaklamlarnda iki nemli koridor tanmlanmtr;lateral ve medial koridorlar.

    YNTEM ve GERE: Kliniimizde Eyll 1997 ile Aralk 2010 tarihleri arasnda 400 endoskopik transsfenoidal yaklam iinde ameliyat edilen360 hipofiz adenomu retrospektif olarak deerlendirilmitir. almaya kavernz sins de tutan tmrl 48 olgu dahil edilmitir.

    BULGULAR: Kavernz sinus invazyonunu intraoperatif olarak medial duvar defektini, intrakavernz carotid arter segmentlerini, kavernzsinus medial duvarndaki kk defektleri grntleyerek ya da mikrodopler ile kavernz sinsn karotid segmentlerini konfirme edereksaladk. nvazyonu tanmladktan sonra kavernz sinse yaylm eklini tmrn medial ve lateral koridorlardan ilerlemesine gre gruptasnflandrdk.25 hastada izole medial koridor tutulumu (Tip I), 5 hastada lateral koridor tutulumu (Tip II) ve18 hastada da her iki koridortutulumu saptadk (Tip III).

    SONU: Yapm olduumuz snflandrma anatomik almalarla ve grntleme yntemleriyle desteklenmi bir endoskopik cerrahisnflandrmadr ve sadece yksek dereceli deil, tm kavernz sinus tutulumlar iin prediktif deer tamaktadr.

    ANAHTAR SZCKLER:Endoskop, Hipofiz adenomu, Kavernz sins, Transfenoidal yaklam

    Correspondence address:Savas CEYLAN / E-mal: [email protected]

    Savas CEYLAN, Ihsan ANIK, Kenan KOC

    Kocael Unversty, Faculty of Medcne, Department of Neurosurgery and Ptutary Research Centre, Kocael, Turkey

    A New Endoscopc Surgcal Classfcaton andInvason Crtera for Ptutary Adenomas Involvng

    the Cavernous SnusKavernz Sns Tutan Hpofz Adenomlarnda Yen Br EndoskopkCerrah Snflandrma ve nvazyon Krterler

    Receved:14.01.2011 /Accepted: 08.02.2011

    DOI: 10.5137/1019-5149.JTN.4149-11.0

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    INTRODUCTION

    Pituitary adenomas usually compress surrounding structures,commonly resulting in sella enlargement and suprasellarextension. Extended microscopic and endoscopic approachesfor the cavernous sinus (CS) invasion have been reported in

    the literature (4,5,6,11,12,17,21,22).

    Surgical approaches to the cavernous sinus, whethertranscranial or inferomedial are still challenges. In recentstudies, increases in the rate of pituitary adenomas invadingthe CS (15-20%) are reported (18,20).

    Contrary to detailed anatomic studies of the cavernoussinus shown by endoscopic approaches, endoscopic clinicalstudies demonstrating cavernous sinus invasion are limited(1,2,3,4,7,13,19,20,21,22,23).

    Numerous studies have dealt with the predictive value ofpreoperative neuroimaging of cavernous sinus invasion (10,24,31). However, all these studies are based on the relationamong pituitary adenoma with CS, ICA and venous sinusesdemonstrated by preoperative MRI studies.

    Recent neuroimaging techniques cannot demonstrate themedial wall of the CS and these classifications also cannotdefine inferomedial cavernous sinus invasion. Among thesewidely used classifications due to confirmation of surgicalfindings with a conventional microscope, invasion is notseen in especially grade 2 lesions and some grade 3 lesionsby the endoscopic technique. The most efficient techniquefor visualization of the cavernous sinus medial wall is theendoscopic technique.

    The endoscopic approach also has an important role in

    surgically defining and differentiating displacement orinvasion of the cavernous sinus by pituitary adenoma. Theendoscopic technique is a more favourable method than themicroscopic technique in defining cavernous sinus invasion.

    The aim of this study was to define cavernous sinus invasioncriteria and endoscopic classification of cavernous sinusinvasion pathways of the adenomas.

    This classification was based on two important corridors,the medial and lateral corridors that have been defined inanatomic and clinic studies (3).

    MATERIAL and METHODS

    A retrospective analysis was performed on 400 endoscopictransphenoidal approaches and 360 pituitary adenomasthat underwent endoscopic transphenoidal surgery in ourdepartment between September 1997 and December 2010.

    48 patients, 23 female (48 %) and 25 male (52%), affected bythe tumours involving the cavernous sinus and treated for thelast 9 years were included in this study. Ages ranged from 11to 70 (mean 42.48) years. Follow-up was between 1 monthand 78 months (mean 34.37 months) (Table I).

    Pituitary adenomas were histologically andimmunohistochemically investigated. They were classified as

    functioning (GH (n: 22), PRL (n: 7) and ACTH (n: 6) secretingadenomas) or non-functioning adenomas (n: 13) in relationto the clinical activity.

    Preoperative MRI findings were assessed according to Knospclassification.

    The extent of resection was evaluated based on MR Imagesobtained in the immediate postoperative period and again 3months afterwards. The extent of resection was determinedas the radical, subtotal (the clear presence of residual tumourbut with resection of > 80% of the tumour), or partial (theclear presence of residual tumour but with resection of < 80%of the tumour). Tumour pathologic type was confirmed by theDepartment of Pathology.

    Surgcal Approach

    We performed previously defined cavernous sinus approachesin our first 14 cases including the paraseptal approach,middle turbinectomy and contralateral middle turbinectomy

    (3,21,22).

    Recently defined extended approaches were performedin 2 patients and combined approaches for 32 patients. Incombined approaches, the surgeries were performed via abinostril approach with enlarged anterior sphenoidotomyallowing wide exposure and easier surgical maneuver.After medial pterygoid process resection, wide sellar flooropening expanding more laterally to the cavernous sinus wasperformed. In this part of the approach, a Kerrison rongeurwas used to widen the sellar floor through the cavernoussinus and following the dissection of this part of the dura,surgical micro-scissors were used rather than a surgical blade

    to enlarge the dura. This avoids redundant carotid arteryinjury (Figure 1A,B). After removal of the sellar componentof the tumor, the invasive part of the lesion was resectedaccording to whether the medial or lateral corridor or bothcorridors were involved.

    Intraoperatve Cavernous Snus InvolvementClassfcaton

    We performed an intraoperative evaluation of cavernoussinus invasion considering;

    1. Visualization of the medial wall defect (Figure 2A-C).

    2. Visualization of at least one of the intracavernous ICAsegments (anterior vertical, horizontal, posterior bend,paraclival carotid artery) (Figure 3A-C).

    3. Visualization of minor tumoral extensions through smallfocal pit holes of the medial wall of CS (Figure 4A-C).

    4. Carotid artery segments were confirmed by micro dopplerand CS invasion was evaluated during the tumor removalin cases of inability to view the carotid segments of CSendoscopically due to CS hemorrhage (Figure 5A-C).

    After identifying cavernous sinus invasion, cavernous sinusinvolvement is classified into three types according to themedial and lateral corridor extension of the tumor.

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    Fgure 1:Case 31:18 year-old female with GH secreting adenoma. A, B)Sellar floor was expanded through the cavernous sinus byKerrison rongeur and after dissection of this part of dura, surgical micro-scissor was used rather than the surgical blade to enlarge aftercontrolling by aspirator or micro-hook. This avoids redundant carotid artery injury.*:Carotid Artery underlying the dura, H:Horizontal Segment of the Cavernous Carotid Artery, Pb:Posterior Bend of the CavernousCarotid Artery.

    Fgure 2: Case 24:39 year-old male with GH secreting adenoma. A)Intraoperative visualization of the medial wall defect. PreoperativeB)and Postoperative C)Gd-enhanced, T1-weighted MR images of the patient.*:Cavernous Sinus Medial Wall.

    Fgure 3: Case 31:18 year-old female with GH secreting adenoma. A)Visualization of intracavernous ICA segments. Preoperative B)and Postoperative C)Gd-enhanced, T1-weighted MR images of the patient.LW:Lateral Wall, H:Horizontal Segment of the Cavernous Carotid Artery, Pb:Posterior Bend of the Cavernous carotid Artery, Pcl:Pa-raclival Carotid Artery.

    A B

    A B C

    A B C

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    Fgure 4: Case 29:40 year-old female with GH secreting adenoma. A)Visualization of minor tumoral extensions through small focalpit-holes of the medial wall of CS. Preoperative B)and Postoperative C)Gd-enhanced, T1-weighted MR images of the patient.*: Focal pit-hole.

    Fgure 5: Case 14:28 year-old female with GH secreting adenomaA)In case of inability to view the CS endoscopically due to hemorrhage,carotid artery segments were confirmed by microdoppler and CS invasion was evaluated. Preoperative B)and Postoperative C)Gd-enhanced, T1-weighted MR images of the patient.Blue Arrows: Segment of carotid Artery.

    Type 1; isolated medial corridor involvement (Figure 6A).

    Type 2; isolated lateral corridor involvement (Figure 6B)

    Type 3; total involvement (both medial and lateral corridorinvolvement) (Figure 6C).

    RESULTS

    Considering this classification, there were 25 isolated medialcorridor involvement (Type I), 5 isolated lateral corridorinvolvement (Type II) and 18 total involvement (Type III) cases.

    Among 48 patients with CS invasion, 43 patients were grade3-4 according to the Knosp classification. Minor tumourextension was observed in 2 patients with grade 3. Gr 2 wasnot defined in any patient. 5 patients, who could not beevaluated according to Knosp classification, were defined asisolated lateral corridor.

    During the intraoperative assessment, group 2 ,which isdefined as visualization of at least one of the ICA segments,was the most commonly seen criteria with 29 patients, andgroup 3, which is defined as visualization of minor tumourextension through small focal pit holes of the medial wall,was the least common with 3 patients according to cavernoussinus invasion criteria.

    25 patients with type 1, isolated medial corridor, 5 patientswith type 2, isolated lateral corridor and 18 patients with type3, total lesions were evaluated according to the involvementof the corridors.

    DISCUSSION

    There are two major problems with pituitary adenomasinvading CS. The first is to define extension and invasion. Inthis study, cavernous sinus invasion criteria were definedendoscopically. Invasion is identified and extension isdistinguished according to these criteria. Invasion of thecavernous sinus on one side and extension to the cavernous

    sinus on the other side were clearly demonstrated by theendoscopic approach in the same case in one of our patients(Figure 7A-C).

    The second problem is the difficulty in demonstratingmedial wall via preoperative imaging modalities. There isno neuroimaging method that can show the medial wallprecisely. In the literature, different results of the anatomicstudies have been published about the structure of theCS medial wall. Studies on the structure of the medial wallwere reported as one layer by some authors, as two layers inanother or thin, loose and histological defects by the other

    A B C

    A B C

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    Fgure 7: Case 32:44 year-old male with nonsecretory adenomaA)Invasion on one side and displacement B)on the other sidewere seen in the same case and was excellently viewed bythe endoscopic technique. C) Preoperative Gd-enhanced, T1-weighted MR images of the patient.LC (long arrow): Lateral Corridor, Pcl:Paraclival Carotid Artery,T: Fibrotic Tumor, Short blue arrow: SupradiaphragmaticOphthalmic Segment, Short arrow:ICA

    authors (8,9,14,15,26,28,30). Thus, some authors reportedthat tumour histology is responsible for CS invasion whilesome authors insist on histological defects of the medial wall(15,16,25,27,29).

    In our previously reported study, we encountered invasion

    through fragile points of the medial wall only in one case withnon-functional adenoma (7).

    We observed that medial wall kept its integrity in caseswithout cavernous sinus involvement. Furthermore in onecase the cavernous components of pituitary adenomawere removed from the thick fibrous membrane and fibrintrabeculation of the medial wall in CS as Songtao et al (26)defined (Figure 8A-C).

    Two important corridors are defined in endoscopic cavernoussinus approaches (3). The ICA medial corridor is formed by theC-shaped segment of the intracavernous sinus carotid arteryand is bordered posteriorly by the dorsum sella and posterior

    petroclinoid fold. The lateral corridor to the ICA (triangulararea) is delineated by the intracavernous track of the internalcarotid posteriorly, by the vidian nerve inferiorly and by themedial pterygoid process anteriorly (3).

    We have demonstrated these corridors via the endoscopicapproach in our previously published clinical series (7).Pituitary adenomas create an entry through these corridors,and we have used the same pathway as surgical corridors(Figure 9A-D).

    Cavernous sinus invasion of pituitary adenomas most oftenprogresses through the medial corridor as reported in clinicalseries (7,19,20,23).

    In recently published anatomic studies, it is reported that thesuperior part of the medial wall was thinner while the inferiorpart thicker (25,26). This confirms why pituitary adenomas areusually located at the medial corridor and demonstrate CSinvasion through the superior part. Thus, this part is namedthe natural gate in CS surgery (26).

    In our series, although isolated medial corridor involvementwas seen in 25 cases, isolated lateral corridor involvementwas encountered in 5 cases. Total involvement was presentin 18 cases. Less frequently seen isolated lateral corridorinvolvement is not defined fully in the Knosp classification.

    Cottier et al (10) defined the carotid sulcus venouscompartment and inferolateral venous compartment, whichform only a part of the isolated lateral corridor emphasized inour classification. Alfieri et al (1) demonstrated the cavernoussinus subdividing into two portions through the endoscopicapproach as paraclival ICA and parasellar ICA in their anatomicstudy. They exposed the paraclival ICA into two parts; thelacerum segment and trigeminal segment.The lateral corridordefined in our classification is formed by the carotid sulcusvenous and inferolateral venous compartments described byCottier et al (10), and the trigeminal segment demonstratedby Alfier et al (1) in their anatomic study.

    A

    B

    C

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    nostril, which was the one with the larger cavity in FEPS andhomolateral to the involved cavernous sinus in EPSea (19, 20).

    We performed a binostril approach for the last 34 cases inthis series, without the need of a far lateral approach andproviding more maneuverability.

    In this study, the most significant hemorrhage was encoun-

    tered in cases with an isolated lateral corridor. In three of fivecases, profuse hemorrhage was seen during the inferolateralextension of the sellar opening. CS hemorrhage was mostlyseen in this group of series. Venous sinuses are compressedand obliterated by the lesion in total involvement cases. Avenous bleed can start after lesion removal when the sinusesare decompressed. In isolated lateral corridor involvement,the sinuses are not totally compressed. Therefore, profusebleeding can be encountered in the beginning.

    Table I:Summary of Clinical and Surgical Information in 48 Patients with Adenomas

    Cont MT: Contralateral Mddle Turbnectomy, MT:Mddle Turbnectomy, PRL:Prolactnoma, Knosp Parasellar Extenson Grade, IOE:Intraoperatve Evaluaton, ESC:Endoscopc

    Surgcal Confrmaton.

    We analyzed our cases according to the Knosp classificationusing the endoscopic technique. Cavernous sinus invasionwas not seen especially in grade 2 cases (Figure 10A-C) and inthree cases with grade 3 lesions; invasion developed throughthe pit holes (Figure 4A-C).

    Frank et al published the only classification study on CSinvasion via the endoscope (19, 20). This classification contains5 grades. Grade 2 and over are accepted as CS invasion asfollows: Grade 2 is focal extension through one or more littlepit holes. Grade 3 is multifocal invasion without encasementof ICA. Grade 4 is total encasement of the ICA.

    Frank et al (19) used two different surgical approaches forpituitary adenomas involving the cavernous sinus includingthe classic functional endoscopic pituitary surgery (FEPS)or the ethmoid-pterygoidsphenoidal endoscopic approach(EPSea). The operations were usually performed through one

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    Fgure 8: Case 27: 42 year-old male with GH secretingadenoma.A)Cavernous componentof pituitary adenomawas removed from thethick fibrous membraneand fibrous trabeculationof medial wall in CS.

    PreoperativeB)and postoperativeC)Gd-enhanced, T1-weighted MR images of thepatient.MW:Medial wall of theCavernous Sinus,FT:Fibrous Trabeculation*:Horizantal Segment ofCavernous Carotid Artery,Blue Arrow:Posterior bendof the Cavernous CarotidArtery.

    Fgure 9:The relationbetween the hypophysis,medial wall, corridors andcarotid artery segments.A)A cadaveric specimen,B)CT Angiography,C,D)Intraoperative viewduring the surgical removalof the adenoma.PS: Pituitary Stalk,Nh:Neurohypophysis,Ah:Adenohypophysis,MW:Medial Wall,Pb:Posterior Bend ofCavernous Carotid Artery,Hs:Horizantal Segment ofCavernous Carotid Artery,Vs:Vertical Segment ofCavernous Carotid Artery,Star:Medial Corridor,LC:Lateral Corridor (bluearrow)

    A

    B C

    A B

    C D

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    7. Ceylan S, Koc K, Anik I: Endoscopic endonasal transsphenoidalapproach for pituitary adenomas invading the cavernous

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    10. Cottier JP, Destrieux C, Brunereau L, Bertrand P, Moreau L,Jan M, Herbreteau D: Cavernous sinus invasion by pituitaryadenoma: MR imaging. Radiology 215:463469, 2000

    11. Couldwell WT, Sabit I, Weiss MH, Giannotta SL, Rice D:Transmaxillary approach to the anterior cavernous sinus:A microanatomic study. Neurosurgery 40:13071311,1997

    12. Das K, Spencer W, Nwagwu CI, Schaeffer S, Wenk E, Weiss

    MH, Couldwell WT: Approaches to the sellar and parasellarregion: Anatomic comparison of endonasal-transsphenoidal,sublabialtranssphenoidal,and transethmoidal approaches.Neurol Res 23:5154, 2001

    13. Doglietto F, Lauretti L, Frank G, Pasquini E, Fernandez E,Tschabitscher M, Maira G: Microscopic and endoscopicextracranial approaches to the cavernous sinus: Anatomicstudy. Neurosurgery 64: (5 Suppl 2):413-421; discussion421-422, 2009

    14. Dolenc VV: Relation of the cavernous sinus to the sella, inDolenc VV (ed): Anatomy and Surgery of the Cavernous Sinus.Vienna: Springer- Verlag, 1989:118130

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    Berlin, Springer, 1989

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    17. Fahlbusch R, Buchfelder M: Transsphenoidal surgery ofparasellar pituitary adenomas. Acta Neurochir (Wien) 92:9399, 1988

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    CONCLUSION

    Cavernous sinus invasion criteria were defined and pituitaryadenomas classified according to their corridor involvementin this study. This classification was confirmed with theendoscopic surgical technique. Isolated lateral corridorinvolvement, which was not evaluated by neuroimagingtechniques previously, was defined. Invasion extension andcavernous sinus medial wall involvement is best demonstratedby the endoscopic technique. However, further anatomicalstudies are required for the confirmation of endoscopicclinical observations.

    ACKNOWLEDGMENT

    We thank Assoc. Prof. Volkan ETUS of our Department ofNeurosurgery, Kocaeli University, School of Medicine, Kocaeli-Turkey, for preparing the illustrated drawings.

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    Fgure 10:45 year-old male with GH secreting adenoma. A)Intraoperative view of the case demonstrating cavernous sinus medialwall. Preoperative B)and Postoperative C)Gd-enhanced, T1-weighted MR images of the patient with Knosp grade 2. Absence ofCavernous Sinus invasion was demonstrated by the endoscopic technique.MW:Medial wall of the Cavernous Sinus, Cst: Suprasellar Cistern.

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