Surgical and Radiologic Anatomy https://doi.org/10.1007/s00276-020-02456-0

ORIGINAL ARTICLE

The anatomical features of denticulate in human fetuses

Özlem Elvan1 · Gülden Kayan2 · Mustafa Aktekin2

Received: 19 December 2019 / Accepted: 6 March 2020 © Springer-Verlag France SAS, part of Springer Nature 2020

Abstract Purpose To determine the morphological features of the denticulate ligament in fetal period. Methods Twelve formalin-fxed fetuses (six females and six males) with a mean gestational age of 27.0 ± 2.04 weeks (range between 25 and 32 weeks) were dissected to reveal morphological properties of the denticulate . Results Denticulate ligament was observed as a continuous ligament extending throughout the length of in all fetuses. It separated the vertebral canal into two as anterior and posterior parts and was anchored to the on either side of the spinal cord with mostly triangular processes as well as thin band-like extensions. The frst denticulate ligament process was always a large and prominent fbrous band and was arising from the spinal cord surface, extending in an oblique direction upward to the anterolateral rim of foramen magnum, below and posterior to the hypoglossal canal. The last den- ticulate ligament process was observed either in the T11–12 (2 sides, 8%), T12–L1 (15 sides, 62%) or L1–2 (7 sides, 30%) and all were band-like processes. At certain spinal cord levels, denticulate ligament had no processes to attach duramater while in some other fetuses double denticulate ligament processes were detected within the same interval. The distance between the denticulate ligament process and the superior spinal nerve root and the distance between the denticulate liga- ment process and the inferior spinal nerve root were measured at each spinal level. This distance was found to be increased from upper to lower levels of the spine. Conclusion Detailed morphological data about fetal denticulate ligament presented in this study provide signifcant informa- tion which may be essential during several surgical interventions performed in early postnatal period and childhood focusing on the spinal cord, spinal nerve roots and meningeal structures.

Keywords Denticulate ligament · Dura mater · Fetus · Morphology · Spinal cord

Introduction of processes, the apices of which are fxed at intervals to the arachnoid lined dural sac. Usually, 20–22 processes are The denticulate (ligamentum denticulatum, dentate liga- observed on each side [1, 7, 17, 22, 24]. The frst process of ment) ligament (DL) is a fat, fbrous sheet of pia running DL is as a thick band and attaches dura mater over the upper on both sides of the spinal cord extending out to anchor into rim of foramen magnum and behind the hypoglossal nerve. arachnoid and dura. It is located between the ventral and The DL stabilizes the spinal cord within the vertebral dorsal spinal roots, thus divides the vertebral canal into ante- canal [20, 23, 24]. In its defciency, spinal cord may become rior and posterior compartments. It extends from the upper instable and vulnerable to trauma and herniation [5]. How- rim of foramen magnum till the level of conus medullaris. ever, during certain surgical interventions, resection of DL Its medial border is continuous with the subpial connec- processes allows the surgeon to mobilize the spinal cord as tive tissue of the cord while its lateral border has a series well as to decrease the tension on the cord [6, 9, 21, 24]. On the other hand, to determine the midline for a safe entry, DL is an essential landmark [5]. Again in anterior, anterolateral * Özlem Elvan or posterior approaches to spinal cord, DL sectioning per- [email protected] mits manupulations on spinal cord [2, 10, 13, 14, 16]. 1 School of Health, Mersin University, Çiftlikköy Campus, Although DL has been studied in detail on adult cadav- Yenişehir, 33343 Mersin, Turkey ers so far, to our knowledge there is no such study in the 2 Department of Anatomy, School of Medicine, Mersin antenatal period. In this study, we aimed to determine the University, Mersin, Turkey

Vol.:(0123456789)1 3 Surgical and Radiologic Anatomy morphological features of DL in fetal period to obtain data Fig. 1 Ventral view of the spi- which may be signifcant for related surgeries of spinal cord nal cord lower thoracic segment presenting double DL processes in early childhood. (asterisk) in T9–T10 level on the right side. DL process was absent in T8–T9 level on the Materials and methods same side. Arrows showing the distances between the attach- ment sites of DL process to Twelve formalin-fxed fetuses (six females and six males) the superior and inferior spinal without visible deformities of the and spi- nerve roots at its dural sac nal cord with a mean gestational age of 27.00 ± 2.04 weeks (range between 25 and 32 weeks), present in the collection of Anatomy Department, School of Medicine, Mersin Uni- versity were evaluated (Table 1). Clinical Research Ethics Committee of Mersin University approved the study. Fetuses were placed in a prone position, a midline skin incision was performed, and paraspinous muscles were retracted laterally. After laminectomy, facets and pedicles were removed. A longitudinal midline incision was made over the posterior dura mater to expose the spinal cord and dorsal rootlets. It is observed that some DL processes were whereas numbers and percentages were used to express cat- extending between two consecutive dorsal rootlets. How- egorical parameters. ever, some other DL processes were located at the same level with the dorsal rootlets. Therefore, we detected DL processes after retracting the dorsal rootlets medially to Results evaluate them properly. Microdissections were applied under surgical microscope (Zeiss Opmi-Pico, Germany) and digital The DL was observed between the frst cervical and frst caliper (0.01 mm precision) was used for measurements. lumbar spinal cord segments. It was more prominent in Dissection and measurements were conducted under the cervical and upper thoracic levels than in the lower levels. same environmental conditions by the same researcher (ÖE After retracting the dorsal rootlets medially, it was possible as an anatomist). to observe DL more clearly. Its lateral border had free mar- Presence, process type (triangular/band-like) and number gin except where it forms a series of processes, the apices of of DL processes at each spinal level were recorded. The which were fxed at intervals to the arachnoid lined dural sac. distance between the attachment site of DL process to the There were 5 double DL processes within the same inter- superior spinal nerve root within the dural sac was recorded. val, while in 14 other intervals no DL process was observed Then, the distance between the attachment site of DL pro- which we recorded them as absent (Fig. 1, Table 2). cess and inferior spinal nerve root was measured (Fig. 1). The DL processes were attaching externally to dura mater Shapiro–Wilk Test was used for normality checks. Mini- in diferent forms; the typical form which has been defned in mum, maximum, mean values and standard deviation were all classical textbooks as ‘triangular-shaped extensions with used as descriptive statistics in continuous parameters, an apex attaching the dura mater’ was the most common in the present study as well. We also observed that the apex of

Table 1 Demographic data of fetuses Table 2 Number of denticulate ligament processes Gestational age Foot length (mm) Gender (weeks) Number of fetus DL processes in pairs Unilateral DL processes Female Male at various levels (sides)

25 43.91 1 2 1 17 3 26 45.58 2 1 1 18 4 27 48.73 2 – 1 19 2 28 51.56 1 1 5 20 – 29 53.64 – 1 3 21 – 32 58.88 – 1 1 22 1 mm milimeter DL denticulate ligament

1 3 Surgical and Radiologic Anatomy

Fig. 2 The DL processes were attaching to dura mater in two forms; triangular and band-like. Both triangular (arrows) and band-like DL processes (dotted arrow) were shown (a). Band-like DL processes were observed to be directed both downward (arrows) and upward Fig. 3 Dorsal view of the upper spinal cord segments. The frst DL (dotted arrow) and they were more frequently observed in lower tho- process was like a large and prominent fbrous band (asterisk) and racic levels (b) was arising from the spinal cord surface, extending in an oblique direction upward to the anterolateral rim of foramen magnum, below and posterior to the hypoglossal canal (HC). Ventral rootlets of frst cervical nerve and (VA) were anterior to frst DL pro- triangle was not always reaching the dura mater, instead a cess while the spinal accessory nerve (arrow) was located posteriorly. thin, band-like process was arising from the apex and attach- A atlas, FM section of occipital bone at foramen magnum, JF jugular ing to dura mater. Moreover, this thin, band-like process was foramen directed downward to reach the dura mater in some fetuses, while it was in upward direction in some others (Fig. 2). In roots were measured bilaterally at each level (Table 3). cervical region between C1 and T1 spinal nerve roots, the Distance to upper nerve root was found to be 1.62 mm in DL processes were directly attaching dura mater forming cervical levels, while it was 2.05 mm in upper thoracic the triangular-shaped form in 60% of fetuses while in other and 2.32 mm in lower thoracic. At L1 level it was found 40% it was forming thin, band-like DL processes. However, 1.68 mm. Distances to lower nerve roots were similar to thin, band-like DL processes were more frequent in thoracic those of upper nerve roots in cervical and upper thoracic region (58%) than triangular-shaped ones (42%). levels. However, the distances to lower nerve roots were Twenty pairs of DL processes were observed in 5 out longer in lower thoracic and the frst lumbar levels. of 12 fetuses, while 21 pairs of DL processes were found in 3 fetuses. In other four fetuses, at least 17 pairs of DL processes were detected. However, in these four fetuses at Discussion certain spinal cord levels, DL processes were observed uni- laterally (Table 2, Fig. 1). Other sides in these four fetuses Our aim in this study was to provide anatomical data about were recorded as absent (Table 2). In fve fetuses, double DL the DL which has been well defned in adults but not in fetal processes were detected unilaterally. Four of these double period. DL processes were in thoracic levels, while only one of them Denticulate ligament extends continuously through- was observed in the cervical level (Fig. 1). out the entire length of the spinal cord beginning from the The frst DL process was observed typically diferent upper rim of foramen magnum till the upper level of conus from all others; it was like a large and prominent fbrous medullaris. Its medial border is continuous as the subpial band and was arising from the spinal cord surface, extend- connective tissue over the cord while its lateral border has ing in an oblique direction upward to the anterolateral rim free margin except where it forms a series of processes, the of foramen magnum, below and posterior to the hypoglos- apices of which are fxed at intervals to the arachnoid lined sal canal. Ventral rootlets of C1 and vertebral artery were dural sac. The numbers of these processes have been usually anterior to frst DL process, while the spinal accessory nerve given as 20–22 pairs [1, 7, 17, 22, 24]. However, unilateral was located posteriorly (Fig. 3). absence and asymmetry in the number of the DL have also The last DL processes were observed between T11 and 12 been reported [5, 9, 23]. In the present study, we detected dorsal rootlets in two sides (8%), between T12 and L1 in 15 20 pairs of DL processes in 5 out of 12 (42%) fetuses and 21 sides (%62) and at L1–2 in 7 sides (%30), and interestingly pairs in 3 other fetuses (25%). In other 4 fetuses (33%), we all were thin, band-like processes (Fig. 4). observed at least 17 pairs of DL processes, but each had sev- The mean distances between the dural attachment site of eral unilateral processes at various levels as well (Table 2). the DL processes and the superior and inferior spinal nerve Thus, the classical knowledge as having 20–22 pairs of DL

1 3 Surgical and Radiologic Anatomy

Table 3 Distances between the Distance to superior root (mm) Distance to inferior root (mm) denticulate ligament processes and the superior and inferior Mean ± SD (range) Mean ± SD (range) nerve roots at diferent spinal Cervical (C1–T1) 1.62 ± 0.48 (0–2.99) 1.65 ± 0.49 (0.66–3.23) levels Upper thoracic (T1–T7) 2.05 ± 0.66 (0–4.28) 1.98 ± 0.72 (0–5.60) Lower thoracic (T7–L1) 2.31 ± 0.69 (0.67–4.32) 2.80 ± 1.05 (0.92–5.71) Lumbar (L1–L2) 1.68 ± 0.41 (1.07–2.53) 4.21 ± 0.49 (3.55–4.99)

SD standard deviation, mm milimeter

process is important for recognition of contributions to the spinal accessory nerve during denervation procedures for spasmodic torticollis [8, 23]. In all these clinical cases, sec- tioning the frst DL process may allow better lateral and anterior approaches to spinal cord as well as being a part of the therapy. Although it has been reported as absent in only 1 side out of 30 in an adult cadaver study, we detected the frst DL processes bilaterally in all fetuses [23]. It was aris- ing medially from the spinomedullary junction of the spinal cord and was attaching to duramater over the anterolateral rim of foramen magnum. Vertebral artery and frst ventral nerve root were anterior to the frst DL process, while spinal accessory and hypoglossal nerves were posterior to it. Simi- lar to Tubbs et al.’s [24] fndings in adult cadavers, larger and thinner medial end of frst DL process was getting thicker laterally and was forming a fbrous band in our series as well. This thicker form of lateral end has been described as cord-like previously [24], (Fig. 3). Fig. 4 The last DL processes were always as band-like processes (arrows) The form of the DL processes was defned as “triangular- shaped extensions with an apex attaching the dura mater” in the literature [5, 7, 15, 19, 22, 24]. Moore et al. characterized processes was not observed in all fetuses unless adding the the DL as a long ribbon-like ligament on each side of the unilateral processes. Neither unilateral absence nor double spine that suspends the spinal cord in the dural sac through a DL processes within the same interval has been mentioned series of bilateral saw toothed ligamentous attachments [17]. in classical textbooks so far [17, 22]. The signifcant fnd- We also observed that the apex of triangular process was not ing detected in this study was that these processes can be always reaching the dura mater, instead a thin, band-like pro- observed unilaterally or double processes can be observed cess was arising from the apex and attaching to dura mater. within the same interval in fetal period. Moreover, this thin, band-like process was directed down- The frst (intracranial or highest) DL process has been ward to reach the dura mater in some fetuses, while it was in considered to be important in neurosurgery of the craniocer- upward direction in some others (Fig. 2). This second type vical region. Classifcation of meningioma location has been process was similar to those previously presented by Gürer decided regarding its relationship with the frst DL process et al. as “Y” shaped processes. They stated that this type of attachment as anterior, lateral and posterolateral [4, 11, 12, processes was particularly observed in thoracic segments. 21]. Also, the frst DL processes have been linked to the Our results show that in cervical region between C1 and T1 formation of the kinking of the spinomedullary junction spinal nerve roots, the DL processes were directly attaching in Chiari malformation Type 2 in which the caudal por- dura mater forming the triangular-shaped form in 60% of tion of medulla is thought to be held in relative immobility fetuses while in other 40% it was forming thin, band-like DL by DL process [6]. Hypertrophic DL processes have been processes. However, thin, band-like DL processes were more reported to cause spinal cord damage and compression of frequent in thoracic segments (58%) than triangular-shaped the C2 root of the spinal accessory nerve [3]. Similarly, tor- ones (42%) which are relevant with those of Gürer et al. [9]. ticollis may be observed due to compression of the spinal The last DL processes were observed as thin, band-like accessory nerve between the frst DL process and the dural between T11 and 12 dorsal rootlets as 8%, between T12 and perforation of vertebral artery [18, 23]. Thus, the frst DL L1 as 62% and at L1–2 as 30% in the present study. The

1 3 Surgical and Radiologic Anatomy most caudal DL has been reported in the L1–2 level (31.2%) 5. Ceylan D, Tatarlı N, Abdullaev T, Seker A, Yıldız SD, Keles E, or in the T12–L1 level (68.8%) in the study of Gürer et al. Konya D, Bayrı Y, Kılıç T, Çavdar S (2012) The denticulate liga- ment: anatomical properties, functional and clinical signifcance. [9]. On the other hand, Ceylan et al. [5] suggested no DL at Acta Neurochir (Wien) 154(7):1229–1234 the lumbar segments. However, Tubbs et al. [24] stated that 6. Emery JL (1967) Kinking of the medulla in children with acute more cephalad termination of the cord did not change the cerebral oedema and hydrocephalus and its relationship to the anatomy and number of the DL. dentate ligaments. J Neurol Neurosurg Psychiatry 30:267–275 7. Epstein BS (1967) Cinemyelographic examination of the cervical The distances from the dural attachment of the DL pro- spinal canal and the craniovertebral junction: the dentate liga- cesses to the superior and inferior spinal nerve root axilla ments. Br J Radiol 40:195–200 were varying among the cervical, upper thoracic and lower 8. Fabinyi G, Dutton J (1980) The surgical treatment of spasmodic thoracic segments. Both distances were increasing from cer- torticollis. Aust N Z J Surg 50(2):155–157 9. Gürer B, Canbay S, Bozkurt M, Cikla U, Hananya T, Okut H, vical to lower thoracic segments. This has been thought to be Başkaya MK (2014) Microsurgical anatomy of the denticulate caused by the enlargement of the vertebral bodies from cer- ligaments and their relationship with the axilla of the spinal nerve vical to lumbar segments [5, 9]. Our results were in accord- roots. Clin Anat 27:733–737 ance with previous studies. Moreover, in cervical and upper 10. Joaquim AF, Almeida JP, Dos Santos MJ, Ghizoni E, de Oliveira E, Tedeschi H (2012) Surgical management of intradural thoracic levels, dural attachment site of DL processes was extramedullary tumors located anteriorly to the spinal cord. J Clin in similar distance to both upper and lower nerve root, while Neurosci 19:1150–1153 in lower thoracic levels, the distances to lower nerve roots 11. Jung TY, Jung S, Kim IY, Kang SS (2009) Foramen magnum were longer than those to upper. meningioma originating from the dentate ligament. Acta Neuro- chir (Wien) 151(4):385–388 12. Jurinovic P, Bulicic AR, Marcic M, Mise NI, Titlic M, Suljic E (2016) Foramen magnum meningioma: a case report and review Conclusion of literature. Acta Inform Med 24(1):74–77 13. Krol G, Arbit E (1993) Percutaneous lateral cervical cordotomy: target localization with water soluble contrast medium. J Neuro- This study presented unique morphological data about the surg 79:390–392 DL in fetal period for the frst time regarding its presence, 14. Lu DC, Lawton MT (2010) Clinical presentation and surgical form and relationships with neighboring structures. The management of intramedullary spinal cord cavernous malforma- morphological features of DL were observed to present its tions. Neurosurg Focus 29:E12 15. McCormick PC, Stein BM (1990) Functional anatomy of the spi- adults form in third trimester. Descriptive fndings of this nal cord and related structures. Neurosurg Clin N Am 1:469–489 study may be helpful in several surgical procedures, particu- 16. Moon SJ, Lee JK, Jang JW, Hur H, Lee JH, Kim SH (2010) The larly in the craniocervical region, which will be performed in transdural approach for thoracic disc herniations: a technical note. the postnatal period and early childhood targeting the spinal Eur Spine J 19:1206–1211 17. Moore KL, Dalley AF, Agur AMR (2014) Clinically oriented cord, , and nerve roots. anatomy, 7th edn. Lippincott Williams & Wilkins, Baltimore 18. Nagata K, Matsui T, Joshita H, Shigeno T, Asano T (1989) Surgi- cal treatment of spasmodic torticollis: efectiveness of microvas- Author contributions ÖE, MA: Project development, data collection cular decompression. Brain Nerve 41:97–102 and analysis, manuscript writing, editing. GK: Data collection and 19. Nicholas DS, Weller RO (1988) The fne anatomy of the human analysis. spinal meninges. A light and scanning electron microscopy study. J Neurosurg 69(2):276–282 Compliance with ethical standards 20. Polak-Kraśna K, Robak-Nawrocka S, Szotek S, Czyż M, Gheek D, Pezowicz C (2019) The denticulate ligament-tensile charac- terization and fnite element micro-scale model of the structure Conflict of interest Authors declared no confict of interest. stabilizing spinal cord. J Mech Behav Biomed Mater 91:10–17 21. Sawada M, Nakae T, Munemitsu T, Hojo M (2018) Spinal men- ingioma arising from the denticulate ligament. World Neurosurg References 115:329–333 22. Standring S, Borley NR, Collins P, Crossman AR, Gatzoulis MA, Healy JC (2008) Gray’s anatomy: the anatomical basis of clinical 1. Adeeb N, Mortazavi MM, Deep A, Griessenauer CJ, Watanabe K, practice, 40th edn. Elsevier, London Shoja MM, Loukas M, Tubbs RS (2013) The : a compre- 23. Tubbs RS, Mortazavi MM, Loukas M, Shoja MM, Cohen-Gadol hensive review of literature. Childs Nerv Syst 29(10):1803–1810 AA (2011) The intracranial denticulate ligament: anatomical study 2. Angevine PD, Kellner C, Haque RM, McCormick PC (2011) Sur- with neurosurgical signifcance. J Neurosurg 114(2):454–457 gical management of ventral intradural spinal lesions. J Neurosurg 24. Tubbs RS, Salter G, Grabb PA, Oakes WJ (2001) The denticulate Spine 15:28–37 ligament: anatomy and functional signifcance. J Neurosurg 94(2 3. Bedford PD, Bosanquet FD, Russell WR (1952) Degeneration of Suppl):271–275 the spinal cord associated with cervical spondylosis. The Lancet 260(6724):55–59 Publisher’s Note Springer Nature remains neutral with regard to 4. Bruneau M, George B (2010) Classifcation system of foramen jurisdictional claims in published maps and institutional afliations. magnum meningiomas. J Craniovertebr Junction Spine 1(1):10–17

1 3