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Molecular Alterations of Human Lumbar Yellow Ligament Related to the Process of Intervertebral Disk Degeneration and Stenosis

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Molecular Alterations of Human Lumbar Yellow Ligament Related to the Process of Intervertebral Disk Degeneration and Stenosis European Spine Journal (2019) 28:1413–1422 https://doi.org/10.1007/s00586-019-05994-3 ORIGINAL ARTICLE Molecular alterations of human lumbar yellow ligament related to the process of intervertebral disk degeneration and stenosis Delio E. Martins1,2,4 · Marcelo Wajchenberg2 · Juliana M. Veridiano3 · Thérèse R. Theodoro3 · Olga M. S. Toledo3 · Maria A. S. Pinhal1,3 Received: 2 March 2019 / Accepted: 30 April 2019 / Published online: 8 May 2019 © Springer-Verlag GmbH Germany, part of Springer Nature 2019 Abstract Purpose The objective of this study was to analyze the layers of yellow ligament in lumbar canal stenosis and disk herniation. Methods Eighteen ligaments were harvested from patients with lumbar spinal canal stenosis. Twenty-nine normal samples from lumbar spine disk herniation patients served as control. All surgical procedures were the same. Ligaments were stained in hematoxylin and eosin; picrosirius–hematoxylin for collagen; Weigert’s resorcin-fuchsin for elaunin, oxytalan and elastic fbers; and transmission electron microscopy. Immunohistochemistry was performed for Il-6; Il-10; and CD-31, PGP9.5. Results are described in means and standard error (mean ± SE), and all analyses adopted the signifcance level of P < 0.05. Results Spinal stenosis ligaments were 2.5 × thicker. Control superfcial ligaments presented a large number of thick, compact collagen fbers and a signifcant amount of oxytalan and mature elastic fbers. The deep layer presented a large number of mature elastic fbers. In the stenosis group, collagen was thinner and compacted in both layers. There was no diference in the interleukin profle among groups. The deep portion of the stenosis group presented a higher number of vessels and nerves. Conclusion Two layers compose the elastic system of the normal ligamentum favum, where the deep portion is mainly responsible for its elasticity (elaunin fbers), while its resistance depends on the concentration of oxytalan fbers, which are more present in the superfcial layer. Ligamentum favum in the stenosis samples presents more mononuclear infltrate and more degraded elastic fbers with a higher number of vessels in its deep portion. Graphical abstract These slides can be retrieved under Electronic Supplementary Material. Key points Take Home Messages Transmission Electron Microscopy images of elastic [Keywords: ligamentum flavum; spinal stenosis; elastic fibers; elaunin and collagen fibers of the ligamentum flavum of fibers; oxytalan fibers ] patients with disc herniation (A and B) and patients 1. The two layers of normal yellow ligament are different in with stenosis (C and D) stained with tanic acid. In A and B, elastic fibers of a disc herniation patient composition. 1. Anatomic and biological differentiation between layers of yellow presenting normal morphological appearance. In C and D, elastic fibers of a patient with stenosis, presenting ligament. changes in the elastin core. Electron dense elastic fibers 2. The deep portion of ligamentum flavum is mainly responsible for (arrow); collagen fibers (C) Magnification: 20,000x (a / its elasticity while superficial portion is manly responsible for its c); 60,000x (b); 50,000x (d) 2. Deep portion of yellow ligament is the mainly responsible for resistance. elasticity. 3. Ligamentum flavum in the stenosis samples presents more 3. Deep portion of the ligament in stenosis patients has a higher mononuclear infiltrate and more degraded elastic fibers with a amount of vessels. higher number of vessels in its deep portion. Martins DE, Wajchenberg M, Veridiano JM, Theodoro TR, de Toledo OMS, Pinhal MAS Martins DE, WajchenbergM, VeridianoJM, Theodoro TR, de Toledo OMS, Pinhal MAS Martins DE, WajchenbergM, Veridiano JM, Theodoro TR, de Toledo OMS, Pinhal MAS (2019) Molecular alterations of human lumbar yellow ligament related to the process of (2019) Molecular alterations of human lumbar yellow ligament related to the process of (2019) Molecular alterations of human lumbar yellow ligament related to the process of intervertebral disc degeneration and stenosis. EurSpine J; intervertebral disc degeneration and stenosis. EurSpine J; intervertebral disc degeneration and stenosis. EurSpine J; Keywords Ligamentum favum · Spinal stenosis · Elastic fbers · Elaunin fbers · Oxytalan fbers Electronic supplementary material The online version of this Introduction article (https ://doi.org/10.1007/s0058 6-019-05994 -3) contains supplementary material, which is available to authorized users. The thickening of the ligamentum favum (LF) and its bio- * Delio E. Martins chemical and morphological changes are considered one of [email protected] the most important causes of spinal stenosis [1]. The LF is Extended author information available on the last page of the article important for providing spinal stability in many postures Vol.:(0123456789)1 3 1414 European Spine Journal (2019) 28:1413–1422 and maintaining a smooth surface on the posterior wall of sagittal T2-weighted (2890/58, 2; 256 × 192; 4 mm; 40 cm), the spinal canal and foramina [2]. LF is constituted of two coronal T2-weighted fat suppressed (2756/58, 2; 256 × 192; portions frmly adherent to each other. The superfcial layer 4 mm; 40 cm) and axial T2-weighted (2756/58, 2; 256 × 192; is a light-yellow structure, adjacent to the multifdus muscles 4 mm; 25 cm). and bigger than the deep component, while the deep layer is The thickness of the LF was measured at its midpoint a thin dark-yellow layer on the ventral side, adjacent to the using magnetic resonance imaging on T1-weighted axial spinal canal [3]. images, which was clearly seen as a low-signal intensity The elastic fber system consists of three diferent kinds mass just ventral to the vertebral lamina. All measures were of fbers. The oxytalan fber composed of parallel bundles done by a single investigator and performed at worksta- of microfbrils that serve as a guide for the deposition of a tions through the Carestream Vue Motion (PACS), version small amount of elastin, forming the elaunin fbers, and as 12.1.5.6529 Inc. 2009 system (Carestream Health, USA). more elastin adheres to those fbers, it becomes thicker and The average age of the disk herniation group was forms the mature elastic fber [4–6]. 40 ± 11.54 (range 19–57) with 18 males (62%); and in the The elasticity of the tissue depends on the concentration stenosis group, the average age was 67 ± 9.59 (range 56–83) of mature elastic fber and elaunin fbers, while its com- with 9 males (50%). pression resistance is related to oxytalan fbers [7]. A large The LF was cut sagittally and fxed with 4% paraformal- amount of oxytalan fbers has been reported as a marker of dehyde in 0.1 M PBS, pH 7.4, for 24 h. Samples were dehy- strong local mechanical stress in muscles [8]. Loss of LF drated in graded concentrations of ethanol and embedded elasticity could be responsible for allowing it to fold into the in parafn. Serial 5 μm coronal sections were made using spinal canal, thus promoting stenosis [1]. a manual microtome LEICA RM-2145-2245 (Leica, Nuss- This adherence between the layers has led the LF to be loch, Germany) and subjected to hematoxylin and eosin; treated as a single structure. However, the goal of this study picrosirius–hematoxylin for collagen analysis; Weigert’s was to determine whether there are diferences in thickness resorcin-fuchsin with previous oxidation for the detection between the layers and whether they difer in histomorphol- and analysis of elastic fbers; and transmission electron ogy, thus implying diferent function. An anatomical inves- microscopy (TEM). For histology and immunohistochem- tigation was therefore performed on LF layers obtained from istry, three slides from each sample were used for analysis. both spinal canal stenosis patients and lumbar disk hernia- All analyses were performed by the same investigator and tion patients. were blinded to groups. The histological sections were analyzed under a light microscope, the stained slides were analyzed, and images Methods were acquired using the Nikon Eclipse E800 ® photomi- croscope (Nikon, Tokyo, Japan) and Nis-Elements® image After Institutional Review Board approval (897.222), 29 capture software (Nikon, Tokyo, Japan). This analysis was consecutive patients with lumbar disk herniation and 18 used for hematoxylin and eosin; picrosirius–hematoxylin and patients with lumbar spinal canal stenosis had their LF har- Weigert’s resorcin-fuchsin. vested during either a microdiscectomy procedure or decom- pression surgery after failure of conservative treatment. All Picrosirius–hematoxylin microdiscectomy procedures were performed by posterior approach using tubular retractors, and the LF was released Sections were deparafnized and hydrated in distilled water, from lamina using a curette. The two layers of the ligament stained with Sirius Red, dissolved in a 0.1% saturated pic- were removed. The frst dorsal layer was called superfcial, ric acid solution for 1 h at room temperature, rinsed with and the second ventral layer, which lies closer to the verte- distilled water and counterstained with hematoxylin for two bral canal, was called the deep portion. The decompression minutes. Sections were then dehydrated with increasing surgery was performed under direct vision. ethanol concentrations, diaphanized in xylene and mounted Spine MRI examinations were conducted as clinical rou- with Entellan (Merck, Darmstadt, Germany) [9]. tine on a 1.5-T magnet HDX (GE Healthcare, Milwaukee, USA) according to the departmental protocol: Subjects were Weigert’s resorcin-fuchsin scanned in a supine position, and their leg extended using a multichannel spine dedicated coil. Examinations used the All elastic system fbers were stained after the tissue was following sequences: sagittal T2-weighted fat suppressed oxidized and prior to staining by Weigert’s resorcin-fuchsin. (TR/TE, 2756/58; number of excitations [NEX], 2; matrix, Sections were deparafnized and treated with a 10% potas- 256 × 192; thickness, 4 mm; feld of view [FOV], 40 cm), sium peroxymonosulfuric acid solution for 40 min [6] and sagittal T1-weighted (357/15; 2; 320 × 256; 4 mm; 40 cm), stained by Weigert’s resorcin-fuchsin method.
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