Анатомическая оценка параселлярных треугольников средней черепной ямки

Введение: Разнообразие хирургических подходов к параселлярной области требует глубокого понимания микрохирургической анатомии. Целью данного исследования было определение границ параселлярных треугольников средней черепной ямки и морфометрическая оценка этих треугольников.

Материалы и методы: в ходе перекрестного наблюдательного исследования, проведенного на кафедре анатомии с мая 2021 по август 2022 г., на пятнадцати образцах черепной ямки были определены границы, морфометрические параметры и содержимое параселлярных треугольников средней черепной ямки.

Результаты: медиальная граница клиновидного треугольника, образованная зрительным нервом, была самой короткой, составляя в среднем 7,64 мм (± 0,59 мм) в длину, а латеральная граница, образованная глазодвигательным нервом, была самой длинной и достигала в среднем 14,5 мм (± 1,46 мм). Средняя длина медиальной границы глазодвигательного треугольника, образованной межклиновидной складкой твердой мозговой оболочки, составила 9,05 мм (±1,07 мм), а латеральной границы, образованной передней петроклиновидной складкой твердой мозговой оболочки, — 14,38 мм (±2,61 мм). Глазодвигательный нерв, формирующий медиальную границу супратрохлеарного треугольника, имел длину 10,81 мм (±1,25 мм), а латеральная граница по блоковому нерву — 14,94 мм (±1,08 мм).

Заключение: представлены морфометрические параметры параселлярных треугольников средней черепной ямки: клиновидного треугольника, глазодвигательного треугольника, надблокового и подблокового треугольников.

Ключевые слова: параселлярная область; клиновидный треугольник, глазодвигательный треугольник, надблоковый и подблоковый треугольники, морфометрия

Конфликт интересов. Авторы заявляют об отсутствии конфликта интересов.
Финансирование. Работа выполнена без спонсорской поддержки.

Introduction: various surgical approaches to parasellar region have been developed, necessitating a thorough understanding of the microsurgical anatomy. The objectives of this study were to delineate the borders of parasellar middle cranial fossa triangles and to morphometrically evaluate of these triangles.

Methodology: in a cross-sectional observational study design, conducted in Department of Anatomy from May 2021 to August 2022, borders, morphometry and contents of parasellar middle cranial fossa triangles were delineated in fifteen cranial fossa specimens.

Results: the medial border of clinoid triangle formed by optic nerve was the shortest with average length of 7.64 mm (± 0.59 mm) and lateral border formed by oculomotor nerve was the longest with average measurement of 14.5 mm (± 1.46 mm). The medial border of oculomotor triangle formed by interclinoid dural fold had average length of 9.05 mm (±1.07 mm) and lateral border formed by anterior petroclinoid dural fold had average measurement of 14.38 mm (±2.61 mm). The oculomotor nerve forming the medial limit of supratrochlear triangle measured 10.81 mm (±1.25 mm) and lateral trochlear nerve border measured 14.94 (±1.08 mm).

Conclusion: morphometric measurements of parasellar middle cranial fossa triangles, namely, clinoid triangle, oculomotor triangle, supratrochlear and infratrochlear triangle are presented.

Keywords: parasellar region; clinoid triangle, oculomotor triangle, supratrochlear and infratrochlear triangle, morphometry
Conflicts of interest. The authors have no conflicts of interest to declare.
Funding. There was no funding for this study 

Introduction. Various surgical approaches to middle cranial fossa especially in parasellar region have been developed in the recent past, necessitating a thorough understanding of the microsurgical anatomy [1]. In addition, endoscopic endonasal surgical techniques are frequently used to explore the medial cavernous sinus region [2]. As the endoscopic view and transcranial view of the parasellar region differ significantly, it is prudent to be well-versed with the identified dissecting corridors and to know the safe area of manoeuvring in this region [3]. Especially so in the skull base, as the operating space is often too minimal and any deviations from the operating protocol proves catastrophic. However, normative values of the measurements of the structures and spaces related the parasellar region are missing. The identified parasellar middle cranial fossa triangles are clinoidal (anteromedial or Dolenc) triangle, oculomotor (medial or Hakuba’s) triangle, supratrochlear triangle and infratrochelear (Parkinson’s) triangle [2]. Clinoidal (anteromedial or Dolenc) triangle is bordered by the optic nerve, oculomotor nerve and tentorial edge (and the dura extending between the dural entry point of the third cranial nerve and the optic nerve) [4]. Clinoidal segment of internal carotid artery (ICA) and the anterior clinoid process (ACP) are located here. Anterior clinoid process has three roots: anterior root (attached to the planum medial to falciform ligament), posterior root (optic strut) and third root (attachment of anterior clinoid process to the lesser wing of sphenoid) [5]. Oculomotor (medial or Hakuba’s) triangle is located in relation to middle cranial fossa bounded by anteriorly by anterior petroclinoid dural fold, posteriorly by posterior petroclinoid dural fold, and medially by the interclinoid dural fold [6]. Its contents are the oculomotor nerve and horizontal segment of ICA. Also, in this space the origin of meningohypophyseal trunk, the initial intracavernous course of the abducens nerve, and the interclinoid ligament can be visualized. This triangle is important during oculomotor nerve exposure [7]. Oculomotor nerve courses just below the dura of the anterior clinoid process (lower margin) [8]. Oculomotor nerve has its own cistern (oculomotor cistern) up to the tip of the anterior clinoid process [8]. To expose the clinoid segment of ICA, anterior clinoid process needs to be removed. Upper dural ring defines the superior limit of clinoid segment of ICA. Upper dural ring extends medially from upper surface of anterior clinoid process. Lower dural ring, also called Perneczky’s ring, defines the inferior limit of the clinoid segment of ICA [9]. Lower dural ring extends from the lower surface of anterior clinoid process. It separates the clinoid process from the upper surface of the oculomotor nerve. This dural sheath continues medially as the carotid-oculomotor membrane (COM) [10]. COM covers the carotid artery. Ophthalmic artery arises just above the clinoid segment. Opening the clinoid and oculomotor triangles with removal of anterior clinoid process up to the optic strut exposes COM [10]. Supratrochlear triangle (or paramedian triangle) is located between the lower aspect of oculomotor nerve (medial border) and upper aspect of trochlear nerve (lateral border). The dura between these two nerves (3rd and 4th) forms the third boundary [11]. It has meningohypophyseal trunk. Frequently inferolateral trunk and medial loop of ICA are located within this triangle. In the posterior part of the cavernous sinus, trochlear nerve is inferior to oculomotor nerve. In the anterior part, it turns upwards and at the level of optic strut, it becomes the most superior part of the cavernous sinus [12]. Trochlear nerve is always superior to the maxillary nerve. As the presence of inferolateral trunk and medial loop of ICA are not constant, evaluating the contents of the supratrochlear triangle provides anatomical details about the cavernous segment of the trochlear nerve [13]. Infratrochlear triangle (Parkinson’s triangle) is bounded by inferior margin of trochlear nerve (medial border), superior margin of ophthalmic nerve (lateral border) and tentorial edge (base). It has cavernous part of ICA and abducent nerve [14]. Dissection in this triangle exposes the abducent nerve [15]. Parkinson described this triangle for direct entry to the cavernous sinus [16, 17]. Few authors have called inferior trochlear triangle as lateral triangle [4, 18]. Dissecting this triangle is important in exposing the trochlear nerve. With this background, the study was designed with the objectives delineate the borders of parasellar middle cranial fossa triangles and to morphometrically evaluate of these triangles.

Methodology. In a cross-sectional observational study design, conducted in Department of Anatomy from May 2021 to August 2022, borders, morphometry and contents of parasellar middle cranial fossa triangles were delineated in fifteen cranial fossa specimens. Institutional ethics committee and scientific review board approved the protocol before starting the study (letter number YEC-1/2021/049). Cadaveric evaluation After removal of calvaria, the occipital bone and squamma of temporal bones were cut up to the transverse sinus and attachment of tentorium cerebelli. The falx cerebri attachment to the crista galli was severed, and carefully reflected outwards cutting any bridging veins connecting the superficial cortical veins and superior sagittal sinus. Cranial nerves in their order were cut under vision away from the skull base, towards the brain to retain the part of the nerves entering the skull base foramen. The pituitary stalk was also cut similarly. The internal carotid artery was cut after ophthalmic artery branching (in the intracerebral segment). The temporal lobe was carefully delivered out of the temporal fossa and a linear incision was taken along the attached margin of the tentorium cerebelli. Tentorium is slid backwards cutting any bridging veins from inferior anastomotic vein of Labbe. The brainstem is blunt cut with the finger as far down as possible in relation to the clivus. The brain was removed intact. The cranial fossa thus exposed was inspected. Inclusion criteria: all fresh cadavers used for routine undergraduate dissection during the study duration where brain removal was undertaken were included in the study. The skull base specimens available in the Department of Anatomy with no damages to the cavernous sinus and related structures, with intact dura over the anterior, middle and posterior cranial fossa were included in the study. Exclusion criteria: specimen with cavernous sinus structures previously dissected, with no dural covering over the anterior, middle and posterior cranial fossa were excluded. Specimens with no identifiable intracranial segments of oculomotor, trochlear, trigeminal and abducens nerves were also excluded. The specimen thus prepared were examined under 3X to 20X magnification using a surgical microscope. The triangles considered in the study were evaluated. A square shaped incision was made in the dura from lesser wing of sphenoid to the planum sphenoidale. This exposes the anterior clinoid process, optic canal and sphenoid edge. Bony canal of the optic canal was removed and anterior clinoid process was drilled. This exposes the clinoidal triangle. The borders of this triangles were noted. Dura over the middle cranial fossa was meticulously removed leaving all the cranial nerves in situ. Structures related to the lateral wall of cavernous sinus was noted. Every effort will be made to avoid any changes in the anatomical relationships of the related structures at this step. All the structures were photographed. At this stage, limits and contents of supratrochlear and infratrochlear were noted. The measurements were taken with digital scale. Right and left sides were compared. Area was calculated as √p(p-a)(p-b)(p-c) where p is half of the perimeter, or p = (a+b+c)/2 and a,b and c were length of boundaries [19]. If the area of the triangle cannot be calculated with this formula as the case when the sum of two side lengths does not exceed the length of the third side, those area calculations are excluded from measure of central tendency. The consistency in shape and size were noted between the specimens. Measurements and statistical analysis Clinoid triangle: medial border is measured as length of the optic nerve within the optic canal. Initially, the intra-canalicular part of the optic nerve is marked, bony covering of the optic canal removed and measurements of intracanalicular part of the optic nerves were taken. The lateral border was measured from oculomotor nerve from dural entry point up to the entry point of superior orbital fissure. Base is the tentorial edge extending between the dural entry point of oculomotor nerve and optic nerve. Oculomotor triangle: anterior clinoid process, posterior clinoid process and petrous apex is identified as most prominent palpable bony projections under the dural folds. Lateral border of oculomotor triangle is measured from the anterior clinoid process tip to the petrous apex and correspond to anterior petroclinoid ligament. Medial border of this triangle measured from posterior clinoid process to the petrous apex and correspond to posterior petroclinoid ligament. Base of the triangle representing the interclinoid dural fold was measured from anterior clinoid process to posterior clinoid process. Supratrochlear triangle: medial border and lateral borders are measured as distances from dural entry points of oculomotor nerve and trochlear nerve up to the superior orbital fissure. Base was measured between the dural entry points of oculomotor and trochlear nerves. Infratrochlear triangle: medial border and lateral borders are measured as distances from dural entry points of trochlear nerve and ophthalmic nerve up to the superior orbital fissure. Base was measured between the dural entry points of trochlear and ophthalmic nerves. To take the measurements, surgical microscope, Almicrosterio zoom microscope (Micro Measures & Instruments, Haryana, India) was used. This three-dimensional zoom trinocular microscope has a high point wide field eye pieces 10x and 15x, parafocal zoom objectives of 1x to 5x provides continuous variable magnification from 10x to 150x depending upon the eye pieces and supplementary lens used, having well designed pole stand, extension pillar, 360 revolving zoom trinocular head, 6 volts 21 watts incident spot light illuminator with light control transformer. Each specimen was placed at 5 cm from the objective of the microscope and images are obtained. Along with every measurement, a measuring scale of length 10mm was also be kept for standardization. Each measurement was taken twice and by two observers to avoid inter and intra-observational bias. Average values of these recordings were considered for analysis. All measurements were expressed in millimetres.

Results. Out of fifteen cadavers 14 were male and one was female. Clinoid triangle: The measurements of clinoid triangle are tabulated in table 1. The medial border formed by optic nerve was the shortest with average length of 7.64 mm (± 0.59 mm) and lateral border formed by oculomotor nerve was the longest with average measurement of 14.5 mm (± 1.46 mm) (Figure 1). There was no statistically significant difference between right and left side of clinoid triangle. Clinoid segment of ICA was noted clearly after severing the anterior clinoid process (Figure 2 and Figure 3). The morphometric measurements of anterior clinoid process are presented in Table 2. The measurements had np statistical difference between right and left side. The average length of clinoid part of internal carotid artery was 4.2 mm (±0.41 mm), with maximum and minimum lengths being 4.75 mm and 3.33 mm. There was no statistical difference between right side measurements and left side measurements. Oculomotor triangle: The measurements of oculomotor triangle are tabulated in table 2. The medial border formed by interclinoid dural fold was the shortest with average length of 9.05 mm (±1.07 mm) and lateral border formed by anterior petroclinoid dural fold was the longest with average measurement of 14.38 mm (±2.61 mm) (Figure 4). There was no statistically significant difference between right and left side of oculomotor triangle. The average length of the cavernous part of ICA within the triangle was 13.02 mm (±1.53 mm) with maximum and minimum values being 15.88 mm and 10.91 mm respectively. The average distance of oculomotor nerve from apex of the triangle to dural entry point was 3.44 mm (±0.86 mm) and from base to dural entry point was 6.23 mm (±1.0 mm). The average thickness of the oculomotor nerve within the triangle was 1.6 mm (± 0.5 mm). Maximum thickness of 2.71 mm oculomotor nerve was observed on the left side in one of the specimens. There was no statistical difference between right and left side measurements. Supratrochlear triangle: The measurements of supratrochlear triangle are tabulated in table 3. The oculomotor nerve forming the medial limit of the triangle measured 10.81 mm (±1.25 mm) and lateral trochlear nerve border measured 14.94 (±1.08 mm). There was no statistically significant difference between measurements of right and left side. In all the specimens, trochlear nerve was superior to maxillary nerve. Infratrochlear triangle: The measurements of infratrochlear triangle are tabulated in table 4. The trochlear nerve forming the medial limit of the triangle measured 14.53 mm (±1.18 mm) and ophthalmic division of trigeminal nerve forming the lateral border measured 12.83 (±1.57 mm) (Figure 5). There was no statistically significant difference between measurements of right and left side.

Discussion. Paraclival, cavernous and paraclinoid segments of carotid artery and its relations are crucial for any skull base surgeries involving sellar region [20]. Though the endoscopic and transcranial view of the parasellar region differ significantly due to cavernous and clinoid segment of internal carotid artery hinders visualization of supratrochlear and infratrochlear triangles [12, 21] in this study, the morphometric analysis of these triangles (in addition to clinoid and oculomotor triangles) is considered through transcranial views in order to generate the normative values and to understand the variations in the contents of these triangles. Exposure of clinoid segment of internal carotid artery and optic nerve delineates the clinoid triangle. This gives access to superior cavernous sinus pathology extending to middle cranial fossa [22]. Clinoid triangle: Watanabe et al., reported measurements of 9.5, 13.3, 7.2 mm and 32.3 mm2 (medial border, lateral border, base, and area) [4]. Isolan et al., reported measurements of 7.34, 13.89, 8.53 mm and 26.25 mm2 (medial border, lateral border, base, and area) [23]. Day and Fukushima reported measurements of 6.30, 6.88 and 8.72 mm (medial border, lateral border and base) [24]. The findings of our study (7.64, 14.5, 8.69 mm and 26.02 mm2 medial border, lateral border, base and area respectively) are in line with the Watanabe and Isolan studies. Oculomotor triangle: This triangle is important during oculomotor nerve exposure and in cases of aneurysm of ICA at the crossing of posterior communicating artery with ICA. The average measurements are 10.4, 16.1, 12.2 mm (anterior, posterior and medial respectively). There is a discrepancy in describing the extent of the triangle. Day et al have defined triangle with subclinoidal carotid segment, posterior clinoid process and porus oculomotorius. They have specifically named it as medial triangle [24]. This resulted in differences in dimensions as well. Umansky reported a measurements of 9.6, 16.6, 13.8 mm (anterior, posterior and medial respectively) [25]. Our results are in line with Umanksy study outcomes. Supratrochlear triangle: Wantabee reports dimensions of 10.9, 14.0, and 7.0 mm for medial, lateral and base measurements of this triangle [4]. Whereas, Doniel et al. reports measurement of 13.18, 14.27, and 5.51 mm respectively [12]. Results of this study (10.81, 14.94, 5.51 mm for medial, lateral and base) are similar to both these studies. During transcavernous approach, supratrochlear triangle is exposed to find the carotid-oculomotor membrane, distal dural ring (Figure 2), and meningohypophyseal trunk. Infratrochlear triangle: Harris et al in their cadaveric study, reported an average length of 13 mm (medial border), 14 mm (lateral border) and 6 mm (base) respectively [26]. They report that this space can be enlarged by displacing the ophthalmic nerve and trochlear nerve. Few authors have called inferior trochlear triangle as lateral triangle [4, 18]. There is discrepancy in naming the triangle, a uniform definition of the triangle avoids confusion. Defining the borders and contents of the triangle provides better understanding of the superior quadrangular area. Conclusion Morphometric measurements of parasellar middle cranial fossa triangles, namely, clinoid triangle, oculomotor triangle, supratrochlear and infratrochlear triangle are presented.