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The long posterior sacroiliac ligament: A histological study of morphological relations in the posterior sacroiliac region
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www.sciencedirect.com Joint Bone Spine 76 (2009) 57e62
Original article
The long posterior sacroiliac ligament: A histological study of morphological relations in the posterior sacroiliac region Christopher McGrath*, Helen Nicholson, Peter Hurst Otago University Department of Anatomy and Structural Biology, Dunedin, New Zealand Accepted 25 February 2008 Available online 25 September 2008
Abstract Objectives: To investigate the morphology of the long posterior sacroiliac ligament (LPSL) and its potential relationship to adjacent structures in the posterior sacroiliac region, and to consider any possible functional anatomical implications that may arise. Methods: Four large cadaveric tissue blocks of the posterior sacroiliac region were utilised in this qualitative histological study. The blocks underwent demineralisation in ethyl-diamine-tetra-acetic acid (EDTA). The end-point was determined radiographically. The demineralised tissue blocks were subsequently processed and a base sledge microtome used to section the blocks. Sequential sections were stained with Harris haematoxylin and alcoholic eosin (H&E) and mounted on glass slides prior to viewing under a light microscope. Results: The LPSL was observed to have proximal and distal regions of osseous attachment. Between these regions of attachment the middle LPSL was observed as a confluence of three layers: the erectores spinae aponeurosis, the ‘deep fascial layer’ and the gluteal aponeurosis. Deep to the ‘deep fascial layer’ a layer of adipose and loose connective tissue was observed. Lateral branches of the dorsal sacral rami were identified within this layer. Conclusions: The middle long posterior ligament appears to provide a pathway for the lateral branches of the dorsal sacral rami between the posterior sacral region and the gluteal region. This histological study provides a morphological basis for the proposal that putative sacroiliac joint pain may be due to an entrapment neuropathy of the lateral branches of the dorsal sacral rami at the long posterior sacroiliac ligament. Ó 2008 Elsevier Masson SAS. All rights reserved. Keywords: Long posterior sacroiliac ligament; Dorsal sacral rami; Sacroiliac joint pain; Sacroiliac joint; Radiofrequency neurotomy; Middle cluneal nerves; Sacroiliac joint syndrome; Sacroiliac pain; Sacroiliac tests; Peripartum pelvic pain; Nonspecific low back pain
1. Introduction Anatomical and clinical studies of the long posterior sacroiliac ligament (LPSL) suggest that it may have a role as a potential pain generating structure in the posterior sacroiliac region, in non-specific low back pain and peripartum pelvic pain [1e4]. However, there is a paucity of detailed morphological or histological information concerning the LPSL and its relationship to surrounding structures. The LPSL is described to attach to the posterior superior iliac spine (PSIS) and to the largest transverse tubercle of the
* Corresponding author. E-mail address: [email protected] (MC. McGrath).
sacrum between the third and the fourth dorsal sacral foramina [1,2,5] (Fig. 1). Traditional anatomical texts vary somewhat in both their morphological depiction and their description of the ligament [6]. The innervation of the posterior sacroiliac ligaments is reported to arise from the dorsal sacral rami [7,8]. Primary afferent Av and C nerve fibres, consistent with pain generation are identified in the posterior sacroiliac ligaments [7e9]. Radio-frequency neurotomy of the lateral branches of the dorsal sacral rami [10e14], is a promising therapeutic approach for sacroiliac joint pain and is the subject of recent study and commentary [15,16]. The lateral branches of the dorsal sacral rami (Fig. 1) also form the posterior sacrococcygeal plexus (PSP), a complex network of fine, interconnected neurovascular bundles located in the posterior
1297-319X/$ - see front matter Ó 2008 Elsevier Masson SAS. All rights reserved. doi:10.1016/j.jbspin.2008.02.015
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2. Methods
Fig. 1. Schematic representation of the location of the long posterior sacroiliac ligament. The posterior sacroiliac region is shown. The LPSL is attached superiorly to the posterior superior iliac spine (PSIS) and inferiorly to the third sacral transverse tubercle (TT). The four posterior sacral foramina (S1eS4) are shown from which the delicate neurovascular structures of lateral branches of the dorsal sacral rami (DSR) emerge, passing laterally deep to the LPSL. The ilium (I) is identified.
sacral region that penetrate the LPSL [1,4,8,17]. It is suggested that an entrapment neuropathy of the penetrating lateral branches of the dorsal sacral rami (middle cluneal nerves) may occur within the LPSL [1,4] leading to posterior sacroiliac pain. The concept of an entrapment neuropathy of the cluneal nerves is not new. Entrapment of the medial branch of the superior cluneal nerves has previously been described [18e 20]. Nevertheless, this appears to be the first time that the detailed morphology of the LPSL has been investigated histologically in an effort to understand the wider functional aspects of the region. The aim of this qualitative investigation is to explore the relationship between the LPSL and surrounding anatomical structures and in particular, to investigate whether a morphological relationship exists between the LPSL and the lateral branches of the dorsal sacral rami. This has the potential to provide a patho-anatomical basis for localised pain over the posterior sacroiliac region. To our knowledge, large tissue blocks that include the LPSL and related posterior sacroiliac region have not previously been utilised to elucidate regional morphology. This methodology was utilised as it offered the qualitative ability to view the region in a functionally integrated manner. Previous dissection studies have highlighted aspects of regional morphology but lack an integrated view [1,4,5,17,21,22].
Embalmed cadaveric material used in this study was bequeathed under the Human Tissue Act of 1964 and provided by the Department of Anatomy and Structural Biology of the University of Otago. Four cadavers with a mean age of 75.8 5.4 years (SD) provided four left sided tissue blocks. The group comprised three males with a mean age of 73.3 3.0 years (SD), and one female aged 83 years. Three cadavers had been previously embalmed in an ethanol, glycerin, water, phenoxyethanol and formalin mix, and one cadaver in a commercially available water based mix (Dodge Anatomical, Dodge Co., Boston). The large tissue blocks were harvested from previously prepared hemipelvises. The lumbosacral disc and the coccyx formed the supero-inferior boundaries and the median sagittal ridge, to a line 2 cm lateral to the PSIS, formed the medio-lateral boundary. The anteroposterior boundaries were defined by the skin posteriorly and by the sacral bone anteriorly. Radiographic analysis of each block confirmed the boundaries. The mean dimensions of the tissue blocks were: axial 12 0.05 cm, sagittal 7.2 0.05 cm and frontal 5.2 0.05 cm. Prior to de-calcification the skin and subcutaneous adipose tissue were removed from each block, as was the sacral promontory. De-calcification of the tissue blocks was undertaken in disodium EDTA 7.5% (Ajax Finechem) buffered to pH 7.0e7.1 with 5% sodium hydroxide. Individual tissue blocks were each immersed in a 2 l container of EDTA and agitated 9 h a day. The EDTA solution was changed every 5 days. Radiographic assessment of the rate of de-calcification was undertaken once per month until radiolucency was attained. The single tissue block of the female cadaver reached the de-calcification endpoint after a comparatively brief three months. The three tissue blocks from male cadavers reached the de-calcification endpoint in a mean time of 10.3 1.2 months (SD). At the conclusion of de-calcification, the tissue blocks were postfixed in 10% neutral buffered formalin. The initial dimensions of the tissue blocks exceeded the dimensions available under the sectioning knife, a 240 mm wedge, profile ‘C’, fixed horizontal blade, of the base sledge microtome (Leitz). However, with progressive de-calcification it became possible to transversely bisect each tissue block with a sharp blade to form two smaller tissue blocks having a mean supero-inferior (axial) dimension of 6.6 0.05 cm, which were then possible to accommodate on the base sledge microtome. Following de-calcification, the tissue blocks were dehydrated through 70% and 95% ethyl alcohol for 4 h. A final change was undertaken in 100% absolute ethyl alcohol for 4 h, microwaving to 64 C for 20 min during the last half hour. Dehydration and clearing was continued with four changes in iso-propyl alcohol, together with brief periods of microwaving. Iso-propyl alcohol was utilised to lessen the tissue hardening effects of prolonged exposure to ethyl alcohol. The tissue blocks were impregnated under low pressure in ‘beesoplast’ wax (10% bees wax, 90% Paraplast paraffin wax), undergoing four wax changes. Impregnated blocks were
MC. McGrath et al. / Joint Bone Spine 76 (2009) 57e62
embedded and mounted on the base sledge microtome. For sectioning, a knife clearance angle of 4 e6 was used with an angle of slope of 70 . Sequential sections of 35e40 mm thickness were cut. A section ‘capture’ bar was fitted to the top of the sectioning knife to prevent section curling. The cutting face of the block was pre-coated with 2% low viscosity nitrocellulose prior to sectioning. This coating physically stabilised the large sections, inhibiting fragmentation. Sections were floated on a 45 C water bath prior to being mounted on a ‘silanised’ (3-amino-propyl-triethoxy-silane, Sigma-Aldrich) coated glass slide (10 cm 5 cm). They were subsequently dried in an incubating oven at 37 C overnight. Sections were de-paraffinised in three changes of xylene for 3e5 min each and rehydrated through two changes of absolute ethyl alcohol at 95% and 70% before immersion in water for 1e2 min. Sections were stained with Harris haematoxylin. They were then hydrated through ethyl alcohol and stained in 0.1% eosin Y for 1e2 s. Rehydration was completed in three more changes of absolute ethyl alcohol before clearing in xylene. Cover-slips (90 mm 50 mm, Menzel Glaser) were used with a synthetic mounting medium, dibutyl phthalate in xylene (DPX). 3. Results Histological observations show that the LPSL was divided into three morphological distinct regions. Two regions of osseous attachment were observed, one to the PSIS superiorly and the other to the third sacral transverse tubercle inferiorly. A third region, corresponding to the middle LPSL, between the two sites of osseous ligamentous attachment, was observed at a confluence of layers of dense fibrous connective tissue. At the superior and inferior attachment sites of the LPSL, (Figs. 2 and 3, respectively) the LPSL was observed to attach to the underlying bone of the ilium superiorly, and sacrum inferiorly. In both these regions of osseous attachment, the LSPL was observed to merge medially with the erectores
Fig. 2. Proximal long posterior sacroiliac ligament (LPSL). This transverse H&E section shows the proximal LPSL attached to the posterior superior iliac spine (PSIS) of the ilium (I). The erectores spinae aponeurosis (ESA) blended with the proximal LPSL from the medial aspect. Fascicles of multifidus (M) were visible deep to the ESA. The proximal LPSL was viewed as continuous with the underlying iliac bone of the PSIS. No sub-ligamentous region of adipose and loose connective tissue was visible.
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Fig. 3. The distal long posterior sacroiliac ligament (LPSL). H&E stained transverse section of the posterior sacroiliac region at the level of the third sacral transverse tubercle. The erectores spinae aponeurosis (ESA) blended with the region of the distal LPSL. The sacrum (S), sacral multifidus (M) and gluteus maximus (GMx) were identified. The sub-ligamentous region of adipose and loose connective tissue seen at the mid LPSL was not evident.
spinae aponeurosis (ESA). Lateral branches of the dorsal sacral rami were not observed to penetrate the LPSL at either the proximal or distal sites of attachment. In contrast to the osseous sites of attachment, the middle LPSL, at the level of the second and third sacral vertebrae, was consistently observed at a confluence of three separate layers of dense fibrous connective tissue (Fig. 4). Passing continuously from the median sacral ridge, the thickest layer of dense fibrous connective tissue of the erectores spinae aponeurosis (ESA) was observed to blend with the medial aspect of the LPSL. Deep to the ESA, the fascicular mass of sacral multifidus was observed, enclosed between the ESA posteriorly and an additional thinner layer of dense fibrous connective tissue anteriorly, referred to as the deep fascial layer (DFL). The DFL was observed to pass laterally from the posterior sacral surface to blend with the middle LPSL and was observed to
Fig. 4. The middle long posterior sacroiliac ligament (LPSL): a confluence of layers. This H&E stained transverse section of the posterior sacroiliac region shows the LPSL at a confluence of layers: the erectores spinae aponeurosis (ESA), the deep fascial layer (DFL) from the posterior sacrum and laterally, the gluteal aponeurosis (GA). The ilium (I), sacrum (S), multifidus (M) and central sacral canal (C) were identified. Anterior (deep) to the LPSL a region of adipose and loose connective tissue was observed posterior to the sacroiliac joint (SIJ) that extended lateral, deep to the GA over the ilium and medially, deep to the DFL over the sacrum. Fibers of gluteus maximus were identified (GMx).
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enclose a deeper (anterior) region of adipose and loose connective tissue. At its greatest extent, this region was observed as continuous between the second and third dorsal sacral foramina medially and the gluteal aponeurosis, lateral to the LPSL, (Fig. 5). The middle LPSL was observed posterior to and separated from, the posterior sacroiliac joint by a region of adipose and loose connective tissue (Fig. 6) although variation was evident in the relative position of the layered confluence of the LPSL and the position, together with the angulation, of the posterior SIJ. The ‘sub-ligamentous’ space was observed as a relatively capacious region of adipose and loose connective tissue (Fig. 6) within which the lateral branches of the dorsal sacral rami are identified [4]. In summary, three morphologically distinct regions of the LPSL were observed: the proximal LSPL attaching to the PSIS; the middle LPSL, characterised by the confluence of dense fibrous connective tissue layers that enclosed an underlying region of adipose and loose connective tissue which contained the underlying lateral branches of the dorsal sacral rami; and the distal LPSL attaching at the third sacral transverse tubercle. 4. Discussion Previous anatomical studies have described morphological aspects of the posterior sacroiliac region [1,2,5,7,8,17,21,22] but lacked the integrated overview provided by this
investigation. The present study expands on an earlier finding [4] of layered morphology at the LPSL and introduces a new patho-anatomical hypothesis for the sacroiliac syndrome, for which the International Association of the Study of Pain [23] and others [13] offer no anatomical basis. The PSIS and the third sacral transverse tubercle are the key osseous anchor sites of the proximal and distal LPSL, respectively. The middle region of the LSPL demonstrates a more complex morphological arrangement, lying at a confluence of dense connective tissue layers: the erectores spinae aponeurosis, the gluteal aponeurosis and a deep fascial layer. We propose that this ‘tent-like’ fascial and ligamentous arrangement may serve as an isolating mechanism for the lateral branches of the dorsal sacral rami coursing within the underlying layer of adipose and loose connective tissue. Tensile forces in the erectores spinae aponeurosis, gluteus maximus and medius may be transmitted to the LPSL assisting the tensile stiffness of the ligament. This in turn may assist in maintaining the patency of the underlying layer of adipose and loose connective tissue that protects and surrounds the delicate neurovascular structures of the middle cluneal nerves. The thin deep fascial layer between the LPSL and the posterior sacral surface, medial to the dorsal sacral foramina, has previously been identified [5,22], but its potential significance and its continuity with the LPSL has, until now, remained open to functional interpretation. Previous clinical studies characterised putative sacroiliac joint pain as a well-localisable pain phenomenon; a range of
Fig. 5. The middle long posterior sacroiliac ligament (LPSL): continuity of adipose and loose connective tissue deep to the deep fascial layer (DFL). This H&E stained transverse section of the posterior sacroiliac region shows the continuity of the adipose and loose connective tissue region (Ad) from the gluteal aponeurosis (GA) lateral to the LPSL, to the cauda equina (CQ) medially. A deep fascial layer of dense fibrous connective tissue extended from the LPSL antero-medially to the medial aspect of the second and third dorsal sacral foramina at the sacral lamina (SL). Here, at the third dorsal sacral foramen (DSF), the deep fascial layer was fenestrated (black asterisks) and a vascular structure (V) was observed between the asterisks. The fenestration permitted the passage of the emerging medial branch of the dorsal sacral foramen. A larger vascular structure (V) was observed at the dorsal sacral foramina. The sacrum (S), ilium (I), sacroiliac joint (SIJ), sacral intervertebral canal (IVC) and a spinal nerve (SN) were identified. Gluteus maximus (GMx), multifidus (M) and the erectors spinae aponeurosis (ESA) were seen.
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Fig. 6. The sub-ligamentous region of the middle long posterior sacroiliac ligament (LPSL). This H&E stained transverse section shows a capacious region of adipose and loose connective tissue (Ad) deep to the LPSL, at a confluence of layers, the erectores spinae aponeurosis (ESA), the deep fascial layer (DFL) and the gluteal aponeurosis (GA). Gluteus maximus fibres (GMx) were observed to attach to the GA, LPSL and ESA. Deep to the ESA, but superficial to the DFL, fascicles of sacral multifidus (M) were observed. The posterior sacroiliac joint (SIJ) was observed between the ilium (I) laterally and the sacrum (S), medially. Small vascular structures (V) were observed within the region of adipose and loose connective tissue.
clinical tests were used to confirm the finding [24e26]. Yet, the evidence and utility of diagnostic SIJ pain provocation tests remains limited [25,27,28]. Whilst this is debated [29,30], a measure of agreement exists that SIJ pain stricto sensu be better considered lato sensu [30]. The morphological evidence of this investigation highlights the potential vulnerability of the lateral branches of the middle cluneal nerves to entrapment and is timely in its provision of a potential pathoanatomical mechanism for localisable pain over the posterior SIJ corresponding to the middle LPSL. The LPSL has been previously proposed as a candidate for localised pain generation, either per se because of sustained tensile stress from counter-nutational loading [2], or as a possible pain generator in peripartum pelvic pain [3], or as a structure of potential entrapment [4]. This histological study presents morphological findings that not only provide a clearer functional basis for the long posterior sacroiliac ligament but also a site of potential entrapment neuropathy. Limitations arise in this study from the small number of large wax blocks taken from elderly cadaveric material. Nonetheless, the morphology of the LPSL and its relationship to the lateral branches of the dorsal sacral rami together with the observation of the deeper region of adipose and loose connective tissue appear consistent with a previous anatomical and histological study of the LPSL [4]. As expected, some morphological alteration was evident after large block processing because of differential tissue shrinkage within the tissue block. 5. Conclusion The long posterior sacroiliac ligament was found to be composed of layers of dense fibrous connective tissue and attaches between the posterior superior iliac spine and the
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third transverse sacral tubercle. At the middle ligamentous region, between the superior and inferior sites of attachment of the LPSL, a confluence of three layers of dense fibrous connective tissue layers, the erectores spinae aponeurosis, a deep fascial layer from the posterior sacral surface and the gluteal aponeurosis were observed. Deep to this morphological arrangement of dense fibrous connective tissue layers, a region of adipose and loose connective tissue was identified in which the lateral branches of the sacral dorsal rami (middle cluneal nerves) passed from the dorsal sacral foramen to the gluteal region. These morphological findings may provide a pathoanatomical basis for localised pain in the posterior sacroiliac region, possibly due to an entrapment neuropathy of the lateral branches of the middle cluneal nerves. Acknowledgments Thanks to the Department of Anatomy and Structural Biology, University of Otago School of Medical Sciences for the use of departmental facilities and resources; to Mr Kenneth Turner of the Histology Service Unit, Department of Pathology, University of Otago School of Medical Sciences; to Mr Andrew McNaughton of Otago Centre for Electron Microscopy, Otago Centre for Confocal Microscopy, Department of Anatomy and Structural Biology, University of Otago School of Medical Sciences; and to Dr Ming Zhang of the Department of Anatomy and Structural Biology, University of Otago School of Medical Sciences, for his advice. References [1] Willard FH, Carreiro JE, Manko W. The long posterior interosseous ligament and the sacrococcygeal plexus. In: Third Interdisciplinary World Congress on Low Back and Pelvic Pain; 1998. p. 207e209. Vienna. [2] Vleeming A, Pool-Goudzwaard AL, Hammudoghlu D, et al. The function of the long dorsal sacroiliac ligament e its implication for understanding low back pain. Spine 1996;21:556e562. [3] Vleeming A, De Vries HJ, Mens JM, et al. Possible role of the long dorsal sacroiliac ligament in women with peripartum pelvic pain. Acta Obstet Gynecol Scand 2002;8:430e436. [4] McGrath MC, Zhang M. Lateral branches of the dorsal sacral nerve plexus and the long posterior sacroiliac ligament. Surg Radiol Anat 2005; 27:327e330. [5] Weisl H. Ligaments of the sacroiliac joint examined with particular reference to their function. Acta Anat 1954;20:201e213. [6] Standring S, Ellis H, Berkowitz B, editors. Gray’s anatomy: the anatomical basis of clinical practice. 39th ed. Edinburgh: Elsevier; 2005. p. 792. Churchill Livingstone. [7] Ikeda R. Innervation of the sacroiliac joint: macroscopical and histological studies. Nippon Ika Daigaku Zasshi 1991;58:587e596. [8] Grob KR, Neuhuber WL, Kissling RO. Innervation of the human sacroiliac joint. Z Rheumatol 1995;54:117e122. [9] Vilensky JA, O’Connor BL, Fortin JD, et al. Histologic analysis of neural elements in the human sacroiliac joint. Spine 2002;27:1202e1207. [10] Yin W, Willard FH, Carreiro JE, et al. Sensory stimulation-guided sacroiliac joint radiofrequency neurotomy: technique based on neuroanatomy of the dorsal sacral plexus. Spine 2003;28:2419e2425. [11] Vallejo R, Benyamin RM, Kramer J, et al. Pulsed radiofrequency denervation for the treatment of sacroiliac joint syndrome. Pain Med 2006;7:429e434.
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[12] Gevargez A, Groenemeyer D, Schirp S, et al. CT-guided percutaneous radiofrequency denervation of the sacroiliac joint. Eur Radiol 2002;12: 1360e1365. [13] Ferrante FM, King LF, Roche EA, et al. Radiofrequency sacroiliac joint denervation for sacroiliac syndrome. Reg Anesth Pain Med 2001;26: 137e142. [14] Cohen SP, Salahadin A. Lateral branch blocks as a treatment for sacroiliac joint pain: a pilot study. Reg Anesth Pain Med 2003;28:113e119. [15] Burnham RS, Yasui Y. An alternate method of radiofrequency neurotomy of the sacroiliac joint: a pilot study of the effect on pain, function and satisfaction. Reg Anesth Pain Med 2007;32:12e19. [16] Cohen SP. Epidemics, evolution and sacroiliac joint pain. Reg Anaesth Pain Med 2007;32:3e6. [17] Zadeh J, Lazorthes G, Roux P, et al. Le plexus sacre posterieur. Bull Assoc Anat (Nancy) 1989;73:35e37. [18] Berthelot JM, Delecrin J, Maugars Y, et al. A potentially under recognised and treatable cause of chronic back pain: entrapment neuropathy of the cluneal nerves. J Rheumatol 1996;23:2179e2181. [19] Maigne JY, Doursounian L. Entrapment neuropathy of the medial superior cluneal nerve: nineteen cases surgically treated, with a minimum of two years’ follow-up. Spine 1997;22:1156e1159. [20] Lu J, Ebraheim NA, Huntoon M, et al. Anatomic considerations of superior cluneal nerve at posterior iliac crest region. Clin Orthop Rel Res 1998;347:224e228. [21] Horwitz TM. The Anatomy of (A) the Lumbosacral nerve plexus e its relation to variations of vertebral segmentation, and (B) the posterior sacral nerve plexus. Anat Rec 1939;74(Suppl 1):S91e107.
[22] Hakim M, Lazaro C. Le plan ligamenteux superficiel ilio-articulaire de l’articulation sacro-iliaque. Annales d’anatomie, pathologique me´decine et chirurgie 1937;14:458e466. [23] Meskey H, Bogduk N. Classifications of chronic pain: descriptions of chronic pain syndrome and definitions of pain terms. 2nd ed. Seattle, WA: IASP Press; 1993. [24] Fortin JD, Falco FJE. The Fortin finger test: an indicator of sacroiliac pain. Am J Orthop 1997;26:477e480. [25] Laslett L, Aprill CN, McDonald B, et al. Diagnosis of sacroiliac joint pain: validity of individual provocation tests and composites of tests. Man Ther 2005;10:207e218. [26] Van der Wurff P, Buijs EJ, Groen GJ. A multitest regimen of pain provocation tests as an aid to reduce unnecessary minimally invasive sacroiliac joint procedures. Arch Phys Med Rehabil 2006;87:10e14. [27] Berthelot JM, Labat JJ, Le Goff B, et al. Provocative sacroiliac joint maneuvers and sacroiliac joint block are unreliable for diagnosing sacroiliac joint pain. Joint Bone Spine 2004;73:17e23. [28] Hansen HC, McKenzie-Brown AM, Cohen SP, et al. Sacroiliac joint interventions: a systematic review. Pain Physician 2007;10:165e184. [29] Laslett M, Comments on Berthelot, et al. review: ‘‘Provocative sacroiliac joint maneuvers and sacroiliac joint block are unreliable for diagnosing sacroiliac joint pain.’’ Joint Bone Spine 2007;74: 306e307. [30] Berthelot J-M. Reply to the letter by Mark Laslett on the review entitled: ‘‘Provocative sacroiliac joint maneuvers and sacroiliac joint block are unreliable for diagnosing sacroiliac joint pain.’’ Joint Bone Spine 2007; 74:307e308.
www.sciencedirect.com Joint Bone Spine 76 (2009) 57e62
Original article
The long posterior sacroiliac ligament: A histological study of morphological relations in the posterior sacroiliac region Christopher McGrath*, Helen Nicholson, Peter Hurst Otago University Department of Anatomy and Structural Biology, Dunedin, New Zealand Accepted 25 February 2008 Available online 25 September 2008
Abstract Objectives: To investigate the morphology of the long posterior sacroiliac ligament (LPSL) and its potential relationship to adjacent structures in the posterior sacroiliac region, and to consider any possible functional anatomical implications that may arise. Methods: Four large cadaveric tissue blocks of the posterior sacroiliac region were utilised in this qualitative histological study. The blocks underwent demineralisation in ethyl-diamine-tetra-acetic acid (EDTA). The end-point was determined radiographically. The demineralised tissue blocks were subsequently processed and a base sledge microtome used to section the blocks. Sequential sections were stained with Harris haematoxylin and alcoholic eosin (H&E) and mounted on glass slides prior to viewing under a light microscope. Results: The LPSL was observed to have proximal and distal regions of osseous attachment. Between these regions of attachment the middle LPSL was observed as a confluence of three layers: the erectores spinae aponeurosis, the ‘deep fascial layer’ and the gluteal aponeurosis. Deep to the ‘deep fascial layer’ a layer of adipose and loose connective tissue was observed. Lateral branches of the dorsal sacral rami were identified within this layer. Conclusions: The middle long posterior ligament appears to provide a pathway for the lateral branches of the dorsal sacral rami between the posterior sacral region and the gluteal region. This histological study provides a morphological basis for the proposal that putative sacroiliac joint pain may be due to an entrapment neuropathy of the lateral branches of the dorsal sacral rami at the long posterior sacroiliac ligament. Ó 2008 Elsevier Masson SAS. All rights reserved. Keywords: Long posterior sacroiliac ligament; Dorsal sacral rami; Sacroiliac joint pain; Sacroiliac joint; Radiofrequency neurotomy; Middle cluneal nerves; Sacroiliac joint syndrome; Sacroiliac pain; Sacroiliac tests; Peripartum pelvic pain; Nonspecific low back pain
1. Introduction Anatomical and clinical studies of the long posterior sacroiliac ligament (LPSL) suggest that it may have a role as a potential pain generating structure in the posterior sacroiliac region, in non-specific low back pain and peripartum pelvic pain [1e4]. However, there is a paucity of detailed morphological or histological information concerning the LPSL and its relationship to surrounding structures. The LPSL is described to attach to the posterior superior iliac spine (PSIS) and to the largest transverse tubercle of the
* Corresponding author. E-mail address: [email protected] (MC. McGrath).
sacrum between the third and the fourth dorsal sacral foramina [1,2,5] (Fig. 1). Traditional anatomical texts vary somewhat in both their morphological depiction and their description of the ligament [6]. The innervation of the posterior sacroiliac ligaments is reported to arise from the dorsal sacral rami [7,8]. Primary afferent Av and C nerve fibres, consistent with pain generation are identified in the posterior sacroiliac ligaments [7e9]. Radio-frequency neurotomy of the lateral branches of the dorsal sacral rami [10e14], is a promising therapeutic approach for sacroiliac joint pain and is the subject of recent study and commentary [15,16]. The lateral branches of the dorsal sacral rami (Fig. 1) also form the posterior sacrococcygeal plexus (PSP), a complex network of fine, interconnected neurovascular bundles located in the posterior
1297-319X/$ - see front matter Ó 2008 Elsevier Masson SAS. All rights reserved. doi:10.1016/j.jbspin.2008.02.015
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MC. McGrath et al. / Joint Bone Spine 76 (2009) 57e62
2. Methods
Fig. 1. Schematic representation of the location of the long posterior sacroiliac ligament. The posterior sacroiliac region is shown. The LPSL is attached superiorly to the posterior superior iliac spine (PSIS) and inferiorly to the third sacral transverse tubercle (TT). The four posterior sacral foramina (S1eS4) are shown from which the delicate neurovascular structures of lateral branches of the dorsal sacral rami (DSR) emerge, passing laterally deep to the LPSL. The ilium (I) is identified.
sacral region that penetrate the LPSL [1,4,8,17]. It is suggested that an entrapment neuropathy of the penetrating lateral branches of the dorsal sacral rami (middle cluneal nerves) may occur within the LPSL [1,4] leading to posterior sacroiliac pain. The concept of an entrapment neuropathy of the cluneal nerves is not new. Entrapment of the medial branch of the superior cluneal nerves has previously been described [18e 20]. Nevertheless, this appears to be the first time that the detailed morphology of the LPSL has been investigated histologically in an effort to understand the wider functional aspects of the region. The aim of this qualitative investigation is to explore the relationship between the LPSL and surrounding anatomical structures and in particular, to investigate whether a morphological relationship exists between the LPSL and the lateral branches of the dorsal sacral rami. This has the potential to provide a patho-anatomical basis for localised pain over the posterior sacroiliac region. To our knowledge, large tissue blocks that include the LPSL and related posterior sacroiliac region have not previously been utilised to elucidate regional morphology. This methodology was utilised as it offered the qualitative ability to view the region in a functionally integrated manner. Previous dissection studies have highlighted aspects of regional morphology but lack an integrated view [1,4,5,17,21,22].
Embalmed cadaveric material used in this study was bequeathed under the Human Tissue Act of 1964 and provided by the Department of Anatomy and Structural Biology of the University of Otago. Four cadavers with a mean age of 75.8 5.4 years (SD) provided four left sided tissue blocks. The group comprised three males with a mean age of 73.3 3.0 years (SD), and one female aged 83 years. Three cadavers had been previously embalmed in an ethanol, glycerin, water, phenoxyethanol and formalin mix, and one cadaver in a commercially available water based mix (Dodge Anatomical, Dodge Co., Boston). The large tissue blocks were harvested from previously prepared hemipelvises. The lumbosacral disc and the coccyx formed the supero-inferior boundaries and the median sagittal ridge, to a line 2 cm lateral to the PSIS, formed the medio-lateral boundary. The anteroposterior boundaries were defined by the skin posteriorly and by the sacral bone anteriorly. Radiographic analysis of each block confirmed the boundaries. The mean dimensions of the tissue blocks were: axial 12 0.05 cm, sagittal 7.2 0.05 cm and frontal 5.2 0.05 cm. Prior to de-calcification the skin and subcutaneous adipose tissue were removed from each block, as was the sacral promontory. De-calcification of the tissue blocks was undertaken in disodium EDTA 7.5% (Ajax Finechem) buffered to pH 7.0e7.1 with 5% sodium hydroxide. Individual tissue blocks were each immersed in a 2 l container of EDTA and agitated 9 h a day. The EDTA solution was changed every 5 days. Radiographic assessment of the rate of de-calcification was undertaken once per month until radiolucency was attained. The single tissue block of the female cadaver reached the de-calcification endpoint after a comparatively brief three months. The three tissue blocks from male cadavers reached the de-calcification endpoint in a mean time of 10.3 1.2 months (SD). At the conclusion of de-calcification, the tissue blocks were postfixed in 10% neutral buffered formalin. The initial dimensions of the tissue blocks exceeded the dimensions available under the sectioning knife, a 240 mm wedge, profile ‘C’, fixed horizontal blade, of the base sledge microtome (Leitz). However, with progressive de-calcification it became possible to transversely bisect each tissue block with a sharp blade to form two smaller tissue blocks having a mean supero-inferior (axial) dimension of 6.6 0.05 cm, which were then possible to accommodate on the base sledge microtome. Following de-calcification, the tissue blocks were dehydrated through 70% and 95% ethyl alcohol for 4 h. A final change was undertaken in 100% absolute ethyl alcohol for 4 h, microwaving to 64 C for 20 min during the last half hour. Dehydration and clearing was continued with four changes in iso-propyl alcohol, together with brief periods of microwaving. Iso-propyl alcohol was utilised to lessen the tissue hardening effects of prolonged exposure to ethyl alcohol. The tissue blocks were impregnated under low pressure in ‘beesoplast’ wax (10% bees wax, 90% Paraplast paraffin wax), undergoing four wax changes. Impregnated blocks were
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embedded and mounted on the base sledge microtome. For sectioning, a knife clearance angle of 4 e6 was used with an angle of slope of 70 . Sequential sections of 35e40 mm thickness were cut. A section ‘capture’ bar was fitted to the top of the sectioning knife to prevent section curling. The cutting face of the block was pre-coated with 2% low viscosity nitrocellulose prior to sectioning. This coating physically stabilised the large sections, inhibiting fragmentation. Sections were floated on a 45 C water bath prior to being mounted on a ‘silanised’ (3-amino-propyl-triethoxy-silane, Sigma-Aldrich) coated glass slide (10 cm 5 cm). They were subsequently dried in an incubating oven at 37 C overnight. Sections were de-paraffinised in three changes of xylene for 3e5 min each and rehydrated through two changes of absolute ethyl alcohol at 95% and 70% before immersion in water for 1e2 min. Sections were stained with Harris haematoxylin. They were then hydrated through ethyl alcohol and stained in 0.1% eosin Y for 1e2 s. Rehydration was completed in three more changes of absolute ethyl alcohol before clearing in xylene. Cover-slips (90 mm 50 mm, Menzel Glaser) were used with a synthetic mounting medium, dibutyl phthalate in xylene (DPX). 3. Results Histological observations show that the LPSL was divided into three morphological distinct regions. Two regions of osseous attachment were observed, one to the PSIS superiorly and the other to the third sacral transverse tubercle inferiorly. A third region, corresponding to the middle LPSL, between the two sites of osseous ligamentous attachment, was observed at a confluence of layers of dense fibrous connective tissue. At the superior and inferior attachment sites of the LPSL, (Figs. 2 and 3, respectively) the LPSL was observed to attach to the underlying bone of the ilium superiorly, and sacrum inferiorly. In both these regions of osseous attachment, the LSPL was observed to merge medially with the erectores
Fig. 2. Proximal long posterior sacroiliac ligament (LPSL). This transverse H&E section shows the proximal LPSL attached to the posterior superior iliac spine (PSIS) of the ilium (I). The erectores spinae aponeurosis (ESA) blended with the proximal LPSL from the medial aspect. Fascicles of multifidus (M) were visible deep to the ESA. The proximal LPSL was viewed as continuous with the underlying iliac bone of the PSIS. No sub-ligamentous region of adipose and loose connective tissue was visible.
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Fig. 3. The distal long posterior sacroiliac ligament (LPSL). H&E stained transverse section of the posterior sacroiliac region at the level of the third sacral transverse tubercle. The erectores spinae aponeurosis (ESA) blended with the region of the distal LPSL. The sacrum (S), sacral multifidus (M) and gluteus maximus (GMx) were identified. The sub-ligamentous region of adipose and loose connective tissue seen at the mid LPSL was not evident.
spinae aponeurosis (ESA). Lateral branches of the dorsal sacral rami were not observed to penetrate the LPSL at either the proximal or distal sites of attachment. In contrast to the osseous sites of attachment, the middle LPSL, at the level of the second and third sacral vertebrae, was consistently observed at a confluence of three separate layers of dense fibrous connective tissue (Fig. 4). Passing continuously from the median sacral ridge, the thickest layer of dense fibrous connective tissue of the erectores spinae aponeurosis (ESA) was observed to blend with the medial aspect of the LPSL. Deep to the ESA, the fascicular mass of sacral multifidus was observed, enclosed between the ESA posteriorly and an additional thinner layer of dense fibrous connective tissue anteriorly, referred to as the deep fascial layer (DFL). The DFL was observed to pass laterally from the posterior sacral surface to blend with the middle LPSL and was observed to
Fig. 4. The middle long posterior sacroiliac ligament (LPSL): a confluence of layers. This H&E stained transverse section of the posterior sacroiliac region shows the LPSL at a confluence of layers: the erectores spinae aponeurosis (ESA), the deep fascial layer (DFL) from the posterior sacrum and laterally, the gluteal aponeurosis (GA). The ilium (I), sacrum (S), multifidus (M) and central sacral canal (C) were identified. Anterior (deep) to the LPSL a region of adipose and loose connective tissue was observed posterior to the sacroiliac joint (SIJ) that extended lateral, deep to the GA over the ilium and medially, deep to the DFL over the sacrum. Fibers of gluteus maximus were identified (GMx).
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enclose a deeper (anterior) region of adipose and loose connective tissue. At its greatest extent, this region was observed as continuous between the second and third dorsal sacral foramina medially and the gluteal aponeurosis, lateral to the LPSL, (Fig. 5). The middle LPSL was observed posterior to and separated from, the posterior sacroiliac joint by a region of adipose and loose connective tissue (Fig. 6) although variation was evident in the relative position of the layered confluence of the LPSL and the position, together with the angulation, of the posterior SIJ. The ‘sub-ligamentous’ space was observed as a relatively capacious region of adipose and loose connective tissue (Fig. 6) within which the lateral branches of the dorsal sacral rami are identified [4]. In summary, three morphologically distinct regions of the LPSL were observed: the proximal LSPL attaching to the PSIS; the middle LPSL, characterised by the confluence of dense fibrous connective tissue layers that enclosed an underlying region of adipose and loose connective tissue which contained the underlying lateral branches of the dorsal sacral rami; and the distal LPSL attaching at the third sacral transverse tubercle. 4. Discussion Previous anatomical studies have described morphological aspects of the posterior sacroiliac region [1,2,5,7,8,17,21,22] but lacked the integrated overview provided by this
investigation. The present study expands on an earlier finding [4] of layered morphology at the LPSL and introduces a new patho-anatomical hypothesis for the sacroiliac syndrome, for which the International Association of the Study of Pain [23] and others [13] offer no anatomical basis. The PSIS and the third sacral transverse tubercle are the key osseous anchor sites of the proximal and distal LPSL, respectively. The middle region of the LSPL demonstrates a more complex morphological arrangement, lying at a confluence of dense connective tissue layers: the erectores spinae aponeurosis, the gluteal aponeurosis and a deep fascial layer. We propose that this ‘tent-like’ fascial and ligamentous arrangement may serve as an isolating mechanism for the lateral branches of the dorsal sacral rami coursing within the underlying layer of adipose and loose connective tissue. Tensile forces in the erectores spinae aponeurosis, gluteus maximus and medius may be transmitted to the LPSL assisting the tensile stiffness of the ligament. This in turn may assist in maintaining the patency of the underlying layer of adipose and loose connective tissue that protects and surrounds the delicate neurovascular structures of the middle cluneal nerves. The thin deep fascial layer between the LPSL and the posterior sacral surface, medial to the dorsal sacral foramina, has previously been identified [5,22], but its potential significance and its continuity with the LPSL has, until now, remained open to functional interpretation. Previous clinical studies characterised putative sacroiliac joint pain as a well-localisable pain phenomenon; a range of
Fig. 5. The middle long posterior sacroiliac ligament (LPSL): continuity of adipose and loose connective tissue deep to the deep fascial layer (DFL). This H&E stained transverse section of the posterior sacroiliac region shows the continuity of the adipose and loose connective tissue region (Ad) from the gluteal aponeurosis (GA) lateral to the LPSL, to the cauda equina (CQ) medially. A deep fascial layer of dense fibrous connective tissue extended from the LPSL antero-medially to the medial aspect of the second and third dorsal sacral foramina at the sacral lamina (SL). Here, at the third dorsal sacral foramen (DSF), the deep fascial layer was fenestrated (black asterisks) and a vascular structure (V) was observed between the asterisks. The fenestration permitted the passage of the emerging medial branch of the dorsal sacral foramen. A larger vascular structure (V) was observed at the dorsal sacral foramina. The sacrum (S), ilium (I), sacroiliac joint (SIJ), sacral intervertebral canal (IVC) and a spinal nerve (SN) were identified. Gluteus maximus (GMx), multifidus (M) and the erectors spinae aponeurosis (ESA) were seen.
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Fig. 6. The sub-ligamentous region of the middle long posterior sacroiliac ligament (LPSL). This H&E stained transverse section shows a capacious region of adipose and loose connective tissue (Ad) deep to the LPSL, at a confluence of layers, the erectores spinae aponeurosis (ESA), the deep fascial layer (DFL) and the gluteal aponeurosis (GA). Gluteus maximus fibres (GMx) were observed to attach to the GA, LPSL and ESA. Deep to the ESA, but superficial to the DFL, fascicles of sacral multifidus (M) were observed. The posterior sacroiliac joint (SIJ) was observed between the ilium (I) laterally and the sacrum (S), medially. Small vascular structures (V) were observed within the region of adipose and loose connective tissue.
clinical tests were used to confirm the finding [24e26]. Yet, the evidence and utility of diagnostic SIJ pain provocation tests remains limited [25,27,28]. Whilst this is debated [29,30], a measure of agreement exists that SIJ pain stricto sensu be better considered lato sensu [30]. The morphological evidence of this investigation highlights the potential vulnerability of the lateral branches of the middle cluneal nerves to entrapment and is timely in its provision of a potential pathoanatomical mechanism for localisable pain over the posterior SIJ corresponding to the middle LPSL. The LPSL has been previously proposed as a candidate for localised pain generation, either per se because of sustained tensile stress from counter-nutational loading [2], or as a possible pain generator in peripartum pelvic pain [3], or as a structure of potential entrapment [4]. This histological study presents morphological findings that not only provide a clearer functional basis for the long posterior sacroiliac ligament but also a site of potential entrapment neuropathy. Limitations arise in this study from the small number of large wax blocks taken from elderly cadaveric material. Nonetheless, the morphology of the LPSL and its relationship to the lateral branches of the dorsal sacral rami together with the observation of the deeper region of adipose and loose connective tissue appear consistent with a previous anatomical and histological study of the LPSL [4]. As expected, some morphological alteration was evident after large block processing because of differential tissue shrinkage within the tissue block. 5. Conclusion The long posterior sacroiliac ligament was found to be composed of layers of dense fibrous connective tissue and attaches between the posterior superior iliac spine and the
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third transverse sacral tubercle. At the middle ligamentous region, between the superior and inferior sites of attachment of the LPSL, a confluence of three layers of dense fibrous connective tissue layers, the erectores spinae aponeurosis, a deep fascial layer from the posterior sacral surface and the gluteal aponeurosis were observed. Deep to this morphological arrangement of dense fibrous connective tissue layers, a region of adipose and loose connective tissue was identified in which the lateral branches of the sacral dorsal rami (middle cluneal nerves) passed from the dorsal sacral foramen to the gluteal region. These morphological findings may provide a pathoanatomical basis for localised pain in the posterior sacroiliac region, possibly due to an entrapment neuropathy of the lateral branches of the middle cluneal nerves. Acknowledgments Thanks to the Department of Anatomy and Structural Biology, University of Otago School of Medical Sciences for the use of departmental facilities and resources; to Mr Kenneth Turner of the Histology Service Unit, Department of Pathology, University of Otago School of Medical Sciences; to Mr Andrew McNaughton of Otago Centre for Electron Microscopy, Otago Centre for Confocal Microscopy, Department of Anatomy and Structural Biology, University of Otago School of Medical Sciences; and to Dr Ming Zhang of the Department of Anatomy and Structural Biology, University of Otago School of Medical Sciences, for his advice. References [1] Willard FH, Carreiro JE, Manko W. The long posterior interosseous ligament and the sacrococcygeal plexus. In: Third Interdisciplinary World Congress on Low Back and Pelvic Pain; 1998. p. 207e209. Vienna. [2] Vleeming A, Pool-Goudzwaard AL, Hammudoghlu D, et al. The function of the long dorsal sacroiliac ligament e its implication for understanding low back pain. Spine 1996;21:556e562. [3] Vleeming A, De Vries HJ, Mens JM, et al. Possible role of the long dorsal sacroiliac ligament in women with peripartum pelvic pain. Acta Obstet Gynecol Scand 2002;8:430e436. [4] McGrath MC, Zhang M. Lateral branches of the dorsal sacral nerve plexus and the long posterior sacroiliac ligament. Surg Radiol Anat 2005; 27:327e330. [5] Weisl H. Ligaments of the sacroiliac joint examined with particular reference to their function. Acta Anat 1954;20:201e213. [6] Standring S, Ellis H, Berkowitz B, editors. Gray’s anatomy: the anatomical basis of clinical practice. 39th ed. Edinburgh: Elsevier; 2005. p. 792. Churchill Livingstone. [7] Ikeda R. Innervation of the sacroiliac joint: macroscopical and histological studies. Nippon Ika Daigaku Zasshi 1991;58:587e596. [8] Grob KR, Neuhuber WL, Kissling RO. Innervation of the human sacroiliac joint. Z Rheumatol 1995;54:117e122. [9] Vilensky JA, O’Connor BL, Fortin JD, et al. Histologic analysis of neural elements in the human sacroiliac joint. Spine 2002;27:1202e1207. [10] Yin W, Willard FH, Carreiro JE, et al. Sensory stimulation-guided sacroiliac joint radiofrequency neurotomy: technique based on neuroanatomy of the dorsal sacral plexus. Spine 2003;28:2419e2425. [11] Vallejo R, Benyamin RM, Kramer J, et al. Pulsed radiofrequency denervation for the treatment of sacroiliac joint syndrome. Pain Med 2006;7:429e434.
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[22] Hakim M, Lazaro C. Le plan ligamenteux superficiel ilio-articulaire de l’articulation sacro-iliaque. Annales d’anatomie, pathologique me´decine et chirurgie 1937;14:458e466. [23] Meskey H, Bogduk N. Classifications of chronic pain: descriptions of chronic pain syndrome and definitions of pain terms. 2nd ed. Seattle, WA: IASP Press; 1993. [24] Fortin JD, Falco FJE. The Fortin finger test: an indicator of sacroiliac pain. Am J Orthop 1997;26:477e480. [25] Laslett L, Aprill CN, McDonald B, et al. Diagnosis of sacroiliac joint pain: validity of individual provocation tests and composites of tests. Man Ther 2005;10:207e218. [26] Van der Wurff P, Buijs EJ, Groen GJ. A multitest regimen of pain provocation tests as an aid to reduce unnecessary minimally invasive sacroiliac joint procedures. Arch Phys Med Rehabil 2006;87:10e14. [27] Berthelot JM, Labat JJ, Le Goff B, et al. Provocative sacroiliac joint maneuvers and sacroiliac joint block are unreliable for diagnosing sacroiliac joint pain. Joint Bone Spine 2004;73:17e23. [28] Hansen HC, McKenzie-Brown AM, Cohen SP, et al. Sacroiliac joint interventions: a systematic review. Pain Physician 2007;10:165e184. [29] Laslett M, Comments on Berthelot, et al. review: ‘‘Provocative sacroiliac joint maneuvers and sacroiliac joint block are unreliable for diagnosing sacroiliac joint pain.’’ Joint Bone Spine 2007;74: 306e307. [30] Berthelot J-M. Reply to the letter by Mark Laslett on the review entitled: ‘‘Provocative sacroiliac joint maneuvers and sacroiliac joint block are unreliable for diagnosing sacroiliac joint pain.’’ Joint Bone Spine 2007; 74:307e308.