Abstract
Spinal fusion surgery is performed all over the world to help patients with cervical and thoracolumbar pathology. As outcomes continue to improve in patients with spine-related pathology, it is important to understand how we got to modern day spinal fusion surgery. Scientific innovations have ranged from the first spinal fusions performed with basic instrumentation in the late nineteenth century to contemporary tools such as pedicle screws, bone grafts, and interbody devices. This article tracks this technological growth so that surgeons may better serve their patients in treating spine-related pain and disability.
Electronic supplementary material
The online version of this article (10.1007/s11420-020-09747-7) contains supplementary material, which is available to authorized users.
Keywords: history of spinal surgery, spinal fusion, bone graft, spine technology
Introduction
The severity of spinal disease physicians faced in the late nineteenth century can hardly be overstated: traumatic injuries, congenital defects, and tuberculosis or Pott’s disease often resulted in severe neurologic impairment and global disability [47, 88]. With the advancements in antiseptic surgery by Joseph Lister and others and innovations in anesthesia by William T.G. Morton, bold surgeons dared to help patients suffering from spinal deformity [57, 79, 98].
In the 1890s, W.T. Wilkins described treating a newborn with spina bifida. Upon dissection, he found that “the last dorsal and the first lumbar vertebra were . . . separated by a half-inch and a hernia protruded through the fissure . . . . The hernia was reduced and the two vertebrae were held together by a figure-of-8 carbolized silk ligature” [11, 38]. An American surgeon, Berthold Earnest Hadra, attempted to treat a patient with progressive neurologic decline from a fracture dislocation of the cervical spine. In 1891, he described using a wire to bring together the sixth and seventh cervical vertebrae for stability [38, 47]. In the early twentieth century, two giants in spine surgery, Russell Hibbs and Fred Albee, pushed the boundaries of science to treat patients suffering from Pott’s disease. Hibbs’s original technique involved treating a 9-year-old boy with a kyphotic deformity by removing the spinous processes and laying them down over the interspinous space to promote fusion and repairing the periosteum over the fusion mass [85]. In this period, Albee, citing his experimental works on dogs, proposed using bone grafting to enhance spinal fusion in patients suffering from Pott’s disease [53].
In modern times, pedicle screws, interbody devices, and osteoinductive and osteoconductive bone grafts all work to assist in forming a solid fusion mass. Techniques in spinal fusion have advanced exponentially over the past 25 to 50 years, as has understanding of the biology and biomechanics surrounding spinal fusion. As we reflect on this history, we must also look forward to how spinal fusion will change over the next 50 years. In this article, we delve into the history of specific aspects of spinal fusion, such as instrumentation and bone grafts, and how scientific innovations are improving the outcomes of spinal surgery.
Fusion Without Instrumentation
The Hibbs technique of laying down bone graft over a fusion bed can be considered an early example of fusion without instrumentation. This technique was modified and further popularized by Melvin Watkins in a classic 1953 article outlining a posterolateral incision to lay down bone graft between transverse processes [96]. Thompson et al. described a similar technique to create a trough between transverse processes to lay down “match stick” bone grafts [87]. This method of spinal fusion is still a viable option for surgeons attempting minimally invasive lumbar fusion [37].
Spondylolisthesis at the lumbosacral junction was first described by Hermann Friedrich Kilian in 1854 and drove advances in anterior spinal fusion [15]. In 1932, Capener described treating patients with a bone dowel between L5 and the sacrum to help correct the forward slippage of the L5 vertebra [15]. Around this time, B.H. Burns performed an anterior lumbar interbody fusion in a 14-year-old boy with a traumatic spondylolisthesis, using a bone dowel from the patient’s tibia to achieve fusion between L5 and the sacrum [13, 25]. Rather than accessing the intervertebral disc space anteriorly, in 1944, Milligan and Briggs described using a posterolateral approach to access the intervertebral disc space [9, 25]. A bone peg was placed in the intervertebral disc space to augment a developing fusion mass in what can be described as a precursor to modern posterolateral interbody fusion (PLIF). Modifications in PLIF techniques have since been adopted for this technically demanding procedure [21, 56].
Instrumentation for Enhancing Fusion
The development of instrumentation to supplement fusion began with the steel wires used by Hadra in 1891 to supplement his posterior cervical surgery. Wire constructs were used in a similar pattern by Fritz Lange of Munich, Germany, to help treat patients with scoliosis [53]. The area of spinal instrumentation, however, has seen tremendous innovation for the purpose of supplementing biomechanical strength while the spine fuses. This includes screws, plates, cages, and interbody devices designed to enhance stability.
Harrington Rods
Between the 1940s and 1960s, there were innovations in facet screws and the use of vitallium in spinal surgery, but the most impactful instrumentation developed during this period was the Harrington rod, in 1962 [25, 49, 91]. Paul Harrington was able to correct scoliosis by first using a concave-distraction technique with a rod and hooks [32, 40, 41]. This rigid support augmented the creation of a spinal fusion but also led to a flattened spine in the sagittal and coronal planes [1, 41]. Nevertheless, Harrington rods were associated with excellent post-operative satisfaction scores after 20 years’ follow-up [62].
Pedicle Screws
Surgeons treating lumbosacral spondylolisthesis, scoliosis, and other conditions of the spine realized early on that post-operative immobilization led to high rates of pseudarthrosis. Developments such as facet screws seemed to improve fusion rates, but early innovators of spinal instrumentation, such as H.H. Boucher, recognized the potential strength of interpedicular fixation [7, 45, 86]. Raymond Roy-Camille was the first, in the early 1970s, to describe using screws oriented sagittally through the facet/pedicle [25, 45, 75, 76]. This three-column fixation strategy is still widely used today [54]. Further innovations to pedicle screw instrumentation have included the polyaxial screw, fenestration, and variations in screw pitch in order to provide more robust fixation in spinal fusion [31, 34, 61].
Given the stable fixation of these screws within the pedicle and vertebral body, there have been several innovations in connecting screws placed at varying levels within the spine. Roy-Camille first used specially designed cobalt–chromium alloy plates to connect pedicle screws for lumbosacral fusions in the 1970s [45]. In the 1980s, Friedrich Magerl used external spinal fixation with pedicle screws for unstable spinal injuries [60]. Arthur Steffee developed titanium plates with specially designed screw slots for implantation in the lumbosacral spine in the late 1980s [101]. These developments, along with the polyaxial screw, helped pave the way for the screw–rod constructs in use today.
Interbody Devices
Research on intervertebral cages for spinal fusion was based on attempts to achieve spinal fusion in horses with wobbler syndrome in the 1970s [25, 99] by decompressing the spinal cord and thereby creating a solid cervical spinal fusion [93]. In order to strengthen this fusion biomechanically, a specially designed cylindrical basket was placed between the vertebrae [4], a method that was subsequently modified by Stephen Kuslich for use in humans [51]. The Bagby and Kuslich or “BAK” cage was used for an ALIF and had a 91% fusion rate at 2 years post-surgery.
PLIF, lateral lumbar interbody fusion (LLIF), and transforaminal lumbar interbody fusion (TLIF), all widely used interbody surgeries, allow for three-column support of a lumbar fusion [65]. Ralph Cloward’s first description of PLIF involved placing autograft/allograft in the intervertebral disc space [21]. During the 1980s and 1990s, Harms et al. were able to pioneer a TLIF approach that used bone graft packed in a titanium cage [39]. By the late 1990s, polyetheretherketone (PEEK) cages offered an inert, rigid material that had a Young’s modulus similar to that of cortical bone and could be used in the intervertebral disc space [97]. Since then, there has been tremendous growth in PEEK device technology in ALIF, TLIF, and PLIF applications [67, 68, 77]. It is important to note, however, that unlike the titanium used for specially designed cages, PEEK is hydrophobic, which can inhibit bone growth [63]. Advances in surface technology continue to address this issue of osseous integration of cage material. LLIF has also gained in popularity in the past decade as a minimally invasive technique to place a large bone graft in the intervertebral space [52, 78]. With this technique, however, surgeons should be cognizant of the temporary but common occurrence of groin pain or numbness.
Cervical Spine Instrumentation
Fusion in the cervical spine using an anterior approach was first described by Robert Robinson and George Smith in the 1950s [27, 74]. By removing disc material and osteophytes and fusing a segment of the cervical spine, they treated cervical spondylosis through an anterior cervical discectomy and fusion (ACDF). Cloward modified this anterior spinal fusion technique using a bone dowel to supplement fusion [22]. A technique to treat multilevel disease pioneered by Boni et al. used a modification of the Cloward technique [6]. This involved decompressing the spinal cord anteriorly with a corpectomy and then inserting an autologous graft into a prepared trench.
Numerous plate–screw constructs have been designed to augment anterior cervical surgery [5, 17, 18, 66]. A recent meta-analysis showed that the use of an anterior plate with screws is associated with better fusion rates and decreased subsidence [69]. Recent innovations in anterior cervical plates include the use of locking screws and variable-angle screws to augment fixation strength [66, 71]. There has also been significant growth in the use of stand-alone cages for ACDF, on the theory that these lower-profile devices reduce the chances of implant-related complications such as dysphagia while providing an adequate fusion bed within the cervical spine [46, 55].
Significant research and iterative innovations in posterior cervical instrumentation, from wire constructs and plates to the lateral mass screw–rod constructs in use today, have resulted from the struggles to treat patients with severe rheumatologic deformities [20, 23, 70, 72].
Bone Grafts
Bone grafts have been used to treat dental and orthopedic injuries since ancient times. Mayans used jadeite, gold, and turquoise for dental inlays, and ancient Romans used gold for dental implants [28, 33, 84]. The first known use of an autograft was in Germany in 1821, whereas the first use of an allograft was for a humeral defect in a 4-year-old boy in 1879 by Sir William Macewen [48, 59]. During spinal surgery, bone grafting plays a vital role in promoting bone healing. Grafting materials can be categorized as osteoinductive, osteoconductive, osteogenic, or some combination of these properties. The history of bone grafting is complex, but it provides valuable insights into how new developments in bone graft technology can augment fusion.
Autografting is the gold standard in bone grafting because it can work as an osteoconductive, osteoinductive, and osteogenic material for bone healing. Hibbs’s early example of an autograft [42] involved the use of a material through which bone could grow (osteoconductive), providing factors encouraging bone growth (osteoinductive), and cells producing bone itself (osteogenic).
Iliac crest bone grafting was used as early as 1921, when it was employed for the treatment of a fractured mandible [19]. It has strong structural and biological properties and has been used extensively in spinal surgery to augment a fusion mass [58, 81]. Iliac crest bone graft harvesting, however, is associated with a high rate of complications, including infection and pain [2, 80].
Allografting provides an osteoconductive environment for bone growth in spinal fusion. One of the first uses of an allograft in spine surgery was in anterior cervical fusion in 1976 [10]. Advantages of allografting include the avoidance of morbidity associated with autograft harvesting from the iliac crest; plus, a large quantity can be used during spinal surgery, which is especially important during multilevel fusion [29]. Disadvantages of allografting include a lack of vascularization and limited osteoinductive or osteogenic properties [83].
Demineralized bone matrix (DBM) provides both osteoconductive and osteoinductive properties as a bone graft material [48]. The original work surrounding DBM was based on Marshall Urist’s original research on the “morphogenetic” properties of decalcified bone matrix [90]. Subsequent work showed promising results in bony defects in a rat femoral diaphyseal pre-clinical model [30]. DBM has been modified and is now frequently used in the augmentation of spinal fusions [43]. Although it offers an osteoinductive and osteoconductive bone graft substitute, disadvantages include batch-to-batch variations in DBM products [3].
The most widely used osteoinductive material is bone morphogenetic protein (BMP). Once again, it was the pioneering work of Urist that showed the potential for BMP to encourage and enhance bone growth [89]. Original pre-clinical research using recombinant human BMP-2 (RhBMP-2) and RhBMP-7 showed promising results in terms of augmenting spinal fusions [50, 100]. Although the rise in the use of RhBMP-2 in particular has sparked controversy regarding high rates of complications and off-label uses, there is evidence supporting its use in appropriate clinical situations [16, 82].
New Developments in Spinal Fusion: Where We May Be Heading
Innovation is in progress worldwide for the purpose of enhancing the strength of spinal fusions. Furthermore, the need for patient-specific treatment plans has pushed scientists to create new instrumentation, novel bone grafts, and translational medical research for spinal fusion. Surgeons continue to work toward creating a fusion mass using the most minimally invasive techniques possible.
As such innovations make it easier for surgeons to create a fusion mass in the spine, there has been significant interest and research in attenuating abrupt transitions between a mobile adjacent spinal level and a fused rigid spinal segment using tethers [12]. These tethering technologies likely will play an important role in the treatment of adult spinal deformity to prevent the complex problem of proximal junctional kyphosis, given the long segment fusions often used to correct sagittal plane deformity. We look forward to future research in this area to describe the optimal techniques in order reduce the risk of adjacent segment disease after a solid spinal arthrodesis.
The design of RhBMP-2 and RhBMP-7 products made use of basic science research in developing recombinant human proteins and the biology of osteocyte differentiation. Similarly, surgeons are using advancements in nanotechnology to design robust interbody devices with advanced surface technology to encourage bone growth [92]. Cao et al. have designed bioabsorbable cervical fusion cages that allow for bone growth while slowly being reabsorbed by the body [14]. Roughening the surface of titanium using nanotechnology within interbody cages has also shown encouraging results in enhancing osteocyte differentiation toward an osteogenic lineage [26, 36].
Carriers for osteoinductive proteins have been extensively studied to enhance safer and more powerful drug delivery at the site of spinal fusion. Specifically, the carrier for RhBMP-2 has typically been the absorbable collagen sponge. There is exciting new research on the delivery of RhBMP-2, in terms of timing and location, to best enhance spinal fusion. Hsu et al. have examined the use of a peptide amphiphile in order to improve BMP-2 delivery at the time of surgery and potentially reduce the dose of BMP-2 required for fusion [44]. Another study looked specifically at a polyelectrolyte complex for use as a BMP-2 carrier, noting improved and more controlled bone growth [94]. Scaffold material has also been highly engineered to induce local BMP-2 [8, 95]. Bouyer et al. were able to coat a poly(lactic-co-glycolic acid) tube to allow for tunable delivery of BMP-2 in rat femoral defect [8]. These innovations likely point to a future with varying methods to administer osteoinductive material at the fusion site.
Stem cells offer the potential to differentiate into bone-forming cell lineages that may have advantages for spinal fusions. In one rabbit study, a large dose of bone marrow stem cells mixed with hydroxyapatite performed better than a low dose of bone marrow stem cells mixed with hydroxyapatite, suggesting a role for stem cells to enhance fusion [64]. The use of stem cells in this manner needs further research, however, given mixed results regarding the vector for the study, the carrier for the stem cells, and the manner of delivery [24, 35]. Definitive pre-clinical and clinical studies showing benefit over traditional methods of providing osteoinductive material at the fusion site (i.e., autograft) are needed before the use of stem cells for spinal fusion is widely adopted [73].
In conclusion, there have been tremendous advances in spinal fusion since the first attempts at treating patients with Pott’s disease in the late 1800s. Scientists and surgeons have worked to make use of developments in biology and biomechanics to design instrumentation that provides more reliable fixation and bone grafts with greater potential to promote fusion. There is certainly more to be done as our knowledge of stem cells, nanotechnology, osteoinduction, and osteobiologics develops.
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Conflicts of Interest
Sohrab Virk, MD, MBA, declares no conflicts of interest. Sheeraz Qureshi, MD, MBA, reports consulting fees from Stryker, Globus Medical, Inc., and Paradigm Spine; royalties from RTI, Globus Medical, Inc., and Stryker; ownership interest in Avaz Surgical and Vital 5; medical/scientific advisory board membership at Spinal Simplicity and Lifelink.com; board membership at Healthgrades and the Minimally Invasive Spine Study Group; and honoraria from AMOpportunities, outside the submitted work. Harvinder Sandhu, MD, reports personal fees from Biorestorative Therapies and Prosidyan Medical and stock or stock options from Amedica, Biorestorative Therapies, Paradigm Spine, Prosydian Medical, and Spinewave, outside the submitted work.
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References
- 1.Aaro S, Dahlborn M. The effect of Harrington instrumentation on the longitudinal axis rotation of the apical vertebra and on the spinal and rib-cage deformity in idiopathic scoliosis studied by computer tomography. Spine (Phila Pa 1976) 1982;7:456–462. doi: 10.1097/00007632-198209000-00009. [DOI] [PubMed] [Google Scholar]
- 2.Arrington ED, Smith WJ, Chambers HG, Bucknell AL, Davino NA. Complications of iliac crest bone graft harvesting. Clin Orthop Relat Res. 1996;329:300–309. doi: 10.1097/00003086-199608000-00037. [DOI] [PubMed] [Google Scholar]
- 3.Bae HW, Zhao L, Kanim LE, Wong P, Delamarter RB, Dawson EG. Intervariability and intravariability of bone morphogenetic proteins in commercially available demineralized bone matrix products. Spine (Phila Pa 1976) 2006;31:1299–1306. doi: 10.1097/01.brs.0000218581.92992.b7. [DOI] [PubMed] [Google Scholar]
- 4.Bagby GW, inventor. Process for fusing bone joints. US Patent 4,501,269 A; February 26, 1985.
- 5.Barbier DD, Caspar W, Klara PM. Anterior cervical fusion and caspar plate stabilization for cervical trauma. Neurosurgery. 1989;25:491–502. doi: 10.1097/00006123-198910000-00001. [DOI] [PubMed] [Google Scholar]
- 6.Boni M, Cherubino P, Denaro V, Benazzo F. Multiple subtotal somatectomy. Technique and evaluation of a series of 39 cases. Spine (Phila Pa 1976) 1984;9:358–362. [PubMed] [Google Scholar]
- 7.Boucher HH. A method of spinal fusion. J Bone Joint Surg Br. 1959;41-b:248–259. doi: 10.1302/0301-620X.41B2.248. [DOI] [PubMed] [Google Scholar]
- 8.Bouyer M, Guillot R, Lavaud J, et al. Surface delivery of tunable doses of BMP-2 from an adaptable polymeric scaffold induces volumetric bone regeneration. Biomaterials. 2016;104:168–181. doi: 10.1016/j.biomaterials.2016.06.001. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 9.Briggs H, Milligan P. Chip fusion of the low back following exploration of the spinal canal. J Bone Joint Surg Am. 1944;26:125–130. [Google Scholar]
- 10.Brown MD, Malinin TI, Davis PB. A roentgenographic evaluation of frozen allografts versus autografts in anterior cervical spine fusions. Clin Orthop Relat Res. 1976:231–236. [PubMed]
- 11.Buck AH, editor. A Reference Handbook to the Medical Sciences, Embracing the Entire Range of Scientific and Practical Medicine and Allied Science. New York: William Wood & Co.; 1894. [Google Scholar]
- 12.Buell Thomas J., Bess Shay, Xu Ming, Schwab Frank J., Lafage Virginie, Ames Christopher P., Shaffrey Christopher I., Smith Justin S. Optimal tether configurations and preload tensioning to prevent proximal junctional kyphosis: a finite element analysis. Journal of Neurosurgery: Spine. 2019;30(5):574–584. doi: 10.3171/2018.10.SPINE18429. [DOI] [PubMed] [Google Scholar]
- 13.Burns B.H. AN OPERATION FOR SPONDYLOLISTHESIS. The Lancet. 1933;221(5728):1233. [Google Scholar]
- 14.Cao L, Duan P-G, Li X-L, et al. Biomechanical stability of a bioabsorbable self-retaining polylactic acid/nano-sized β-tricalcium phosphate cervical spine interbody fusion device in single-level anterior cervical discectomy and fusion sheep models. Int J Nanomedicine. 2012;7:5875–5880. doi: 10.2147/IJN.S38288. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 15.Capener N. Spondylolisthesis. Br J Surg. 1932;19:374–386. [Google Scholar]
- 16.Carragee EJ, Baker RM, Benzel EC, et al. A biologic without guidelines: the YODA project and the future of bone morphogenetic protein-2 research. Spine J. 2012;12:877–880. doi: 10.1016/j.spinee.2012.11.002. [DOI] [PubMed] [Google Scholar]
- 17.Castro FP, Jr, Holt RT, Majd M, Whitecloud TS., 3rd A cost analysis of two anterior cervical fusion procedures. J Spine Disord. 2000;13:511–514. doi: 10.1097/00002517-200012000-00008. [DOI] [PubMed] [Google Scholar]
- 18.Chen Y, Lu G, Wang B, Li L, Kuang L. A comparison of anterior cervical discectomy and fusion (ACDF) using self-locking stand-alone polyetheretherketone (PEEK) cage with ACDF using cage and plate in the treatment of three-level cervical degenerative spondylopathy: a retrospective study with 2-year follow-up. Euro Spine J. 2016;25:2255–2262. doi: 10.1007/s00586-016-4391-x. [DOI] [PubMed] [Google Scholar]
- 19.Chubb G. Demonstration of cases and radiographs illustrating the technique employed and results obtained in the repair of fractured mandible by means of the free autogenous bone-graft. Proc R Soc Med. 1921;14(Surg Sect):81–83. [PMC free article] [PubMed] [Google Scholar]
- 20.Clark CR, Goetz DD, Menezes AH. Arthrodesis of the cervical spine in rheumatoid arthritis. J Bone Joint Surg Am. 1989;71:381–392. [PubMed] [Google Scholar]
- 21.Cloward RB. The treatment of ruptured lumbar intervertebral discs by vertebral body fusion. I. Indications, operative technique, after care. J Neurosurg. 1953;10:154–168. doi: 10.3171/jns.1953.10.2.0154. [DOI] [PubMed] [Google Scholar]
- 22.Cloward RB. The anterior approach for removal of ruptured cervical disks. J Neurosurg. 1958;15(6):602–617. doi: 10.3171/jns.1958.15.6.0602. [DOI] [PubMed] [Google Scholar]
- 23.Cregan JC. Internal fixation of the unstable rheumatoid cervical spine. Ann Rheum Dis. 1966;25:242–252. doi: 10.1136/ard.25.3.242. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 24.Cuenca-Lopez MD, Andrades JA, Gomez S, et al. Evaluation of posterolateral lumbar fusion in sheep using mineral scaffolds seeded with cultured bone marrow cells. Int J Mol Sci. 2014;15:23359–23376. doi: 10.3390/ijms151223359. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 25.de Kunder Suzanne L., Rijkers Kim, Caelers Inge J.M.H., de Bie Rob A., Koehler Peter J., van Santbrink Henk. Lumbar Interbody Fusion. SPINE. 2018;43(16):1161–1168. doi: 10.1097/BRS.0000000000002534. [DOI] [PubMed] [Google Scholar]
- 26.De Leonardis D, Garg AK, Pecora GE. Osseointegration of rough acid-etched titanium implants: 5-year follow-up of 100 minimatic implants. Int J Oral Maxillofac Implants. 1999;14(3):384–391. [PubMed] [Google Scholar]
- 27.Denaro V, Di Martino A. Cervical spine surgery: an historical perspective. Clin Orthop Relat Res. 2011;469:639–648. doi: 10.1007/s11999-010-1752-3. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 28.Donaldson JA. The use of gold in dentistry. Gold Bulletin. 1980;13:117–124. doi: 10.1007/BF03216551. [DOI] [PubMed] [Google Scholar]
- 29.Ehrler Douglas M., Vaccaro Alexander R. The Use of Allograft Bone in Lumbar Spine Surgery. Clinical Orthopaedics and Related Research. 2000;371:38–45. doi: 10.1097/00003086-200002000-00005. [DOI] [PubMed] [Google Scholar]
- 30.Einhorn TA, Lane JM, Burstein AH, Kopman CR, Vigorita VJ. The healing of segmental bone defects induced by demineralized bone matrix. A radiographic and biomechanical study. J Bone Joint Surg Am. 1984;66:274–279. [PubMed] [Google Scholar]
- 31.Elder BD, Lo SF, Holmes C, et al. The biomechanics of pedicle screw augmentation with cement. Spine J. 2015;15:1432–1445. doi: 10.1016/j.spinee.2015.03.016. [DOI] [PubMed] [Google Scholar]
- 32.Erwin WD, Dickson JH, Harrington PR. Clinical review of patients with broken Harrington rods. J Bone Joint Surg Am. 1980;62:1302–1307. [PubMed] [Google Scholar]
- 33.Fastlicht S. Tooth mutilations and dentistry in pre-Columbian Mexico. Berlin: Quintessenz Verlags-GmbH; 1976. [Google Scholar]
- 34.Fogel GR, Reitman CA, Liu W, Esses SI. Physical characteristics of polyaxial-headed pedicle screws and biomechanical comparison of load with their failure. Spine (Phila Pa 1976) 2003;28:470–473. doi: 10.1097/01.BRS.0000048652.45964.2E. [DOI] [PubMed] [Google Scholar]
- 35.Fu TS, Chang YH, Wong CB, et al. Mesenchymal stem cells expressing baculovirus-engineered BMP-2 and VEGF enhance posterolateral spine fusion in a rabbit model. Spine J. 2015;15:2036–2044. doi: 10.1016/j.spinee.2014.11.002. [DOI] [PubMed] [Google Scholar]
- 36.Gittens RA, Olivares-Navarrete R, McLachlan T, et al. Differential responses of osteoblast lineage cells to nanotopographically-modified, microroughened titanium–aluminum–vanadium alloy surfaces. Biomaterials. 2012;33:8986–8994. doi: 10.1016/j.biomaterials.2012.08.059. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 37.Guiroy A, Sícoli A, Masanés NG, Ciancio AM, Gagliardi M, Falavigna A. How to perform the Wiltse posterolateral spinal approach: technical note. Surg Neurol Int. 2018;9:38. doi: 10.4103/sni.sni_344_17. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 38.Hadra BE. Wiring of the vertebrae as a means of immobilization in fracture and Potts’ disease. 1891. Clin Orthop Relat Res. 2007;460:11–13. doi: 10.1097/BLO.0b013e318068692a. [DOI] [PubMed] [Google Scholar]
- 39.Harms JG. The unilateral, transforaminal approach for posterior lumbar interbody fusion. Oper Orthop Traumatol. 1998;10:90–102. doi: 10.1007/s00064-006-0112-7. [DOI] [PubMed] [Google Scholar]
- 40.Harrington PR, Dickson JH. Spinal instrumentation in the treatment of severe progressive spondylolisthesis. Clin Orthop Relat Res. 1976:157–163. [PubMed]
- 41.Hasler CC. A brief overview of 100 years of history of surgical treatment for adolescent idiopathic scoliosis. J Child Orthop. 2013;7(1):57–62. doi: 10.1007/s11832-012-0466-3. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 42.Hibbs RA. An operation for progressive spinal deformities: a preliminary report of three cases from the service of the orthopaedic hospital. 1911. Clin Orthop Relat Res. 2007;460:17–20. doi: 10.1097/BLO.0b013e3180686b30. [DOI] [PubMed] [Google Scholar]
- 43.Hsu WK, Wang JC. Demineralized bone matrix for spinal arthrodesis. Semin Spine Surg. 2006;18:22–25. [Google Scholar]
- 44.Hsu W, Weiner J, Chun D, et al. Peptide amphiphile nanogel as an improved BMP-2 carrier for spinal arthrodesis. Global Spine J. 2016;6(1_suppl):s-0036. [Google Scholar]
- 45.Kabins MB, Weinstein JN. The history of vertebral screw and pedicle screw fixation. Iowa Orthop J. 1991;11:127–136. [Google Scholar]
- 46.Kapetanakis S, Thomaidis T, Charitoudis G, Pavlidis P, Theodosiadis P, Gkasdaris G. Single anterior cervical discectomy and fusion (ACDF) using self-locking stand-alone polyetheretherketone (PEEK) cage: evaluation of pain and health-related quality of life. J Spine Surg. 2017;3:312–322. doi: 10.21037/jss.2017.06.21. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 47.Keller T, Holland MC. Some notable American spine surgeons of the 19th century. Spine (Phila Pa 1976) 1997;22:1413–1417. doi: 10.1097/00007632-199706150-00022. [DOI] [PubMed] [Google Scholar]
- 48.Khan SN, Cammisa FP, Jr, Sandhu HS, Diwan AD, Girardi FP, Lane JM. The biology of bone grafting. J Am Acad Orthop Surg. 2005;13:77–86. [PubMed] [Google Scholar]
- 49.King D. Internal fixation for lumbosacral fusion. J Bone Joint Surg Am. 1948;30:560–578. [PubMed] [Google Scholar]
- 50.Krebsbach PH, Gu K, Franceschi RT, Rutherford RB. Gene therapy–directed osteogenesis: BMP-7-transduced human fibroblasts form bone in vivo. Hum Gene Ther. 2000;11(8):1201–1210. doi: 10.1089/10430340050015248. [DOI] [PubMed] [Google Scholar]
- 51.Kuslich SD, Ulstrom CL, Griffith SL, Ahern JW, Dowdle JD. The Bagby and Kuslich method of lumbar interbody fusion. History, techniques, and 2-year follow-up results of a United States prospective, multicenter trial. Spine (Phila Pa 1976) 1998;23:1267–1278. doi: 10.1097/00007632-199806010-00019. [DOI] [PubMed] [Google Scholar]
- 52.Kwon B, Kim DH. Lateral lumbar interbody fusion: indications, outcomes, and complications. J Am Acad Orthop Surg. 2016;24:96–105. doi: 10.5435/JAAOS-D-14-00208. [DOI] [PubMed] [Google Scholar]
- 53.Lange F, Peltier LF. The classic. Support for the spondylitic spine by means of buried steel bars, attached to the vertebrae. By Fritz Lange. 1910. Clin Orthop Relat Res. 1986;203:3–6. [PubMed] [Google Scholar]
- 54.Larson AN, Polly DW, Ackerman SJ, et al. What would be the annual cost savings if fewer screws were used in adolescent idiopathic scoliosis treatment in the US? J Neurosurg Spine. 2016;24(1):116–123. doi: 10.3171/2015.4.SPINE131119. [DOI] [PubMed] [Google Scholar]
- 55.Li Z, Zhao Y, Tang J, Ren D, Guo J, Wang H, Li L, Hou S. A comparison of a new zero-profile, stand-alone Fidji cervical cage and anterior cervical plate for single and multilevel ACDF: a minimum 2-year follow-up study. Euro Spine J. 2017;26:1129–1139. doi: 10.1007/s00586-016-4739-2. [DOI] [PubMed] [Google Scholar]
- 56.Lin PM. A technical modification of Cloward’s posterior lumbar interbody fusion. Neurosurgery. 1977;1(2):118–124. doi: 10.1227/00006123-197709000-00006. [DOI] [PubMed] [Google Scholar]
- 57.Lister J. On the antiseptic principle in the practice of surgery. Brit Med J. 1867;2:246–248. doi: 10.1136/bmj.2.351.246. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 58.Lopez GD, Hijji FY, Narain AS, Yom KH, Singh K. Iliac crest bone graft: a minimally invasive harvesting technique. Clin Spine Surg. 2017;30(10):439–441. doi: 10.1097/BSD.0000000000000556. [DOI] [PubMed] [Google Scholar]
- 59.Macewen W. Observations concerning transplantation of bone. Illustrated by a case of inter-human osseous transplantation, whereby over two-thirds of the shaft of a humerus was restored. Proc Royal Soc London. 1881;32:232–247. [Google Scholar]
- 60.Magerl FP. Stabilization of the lower thoracic and lumbar spine with external skeletal fixation. Clin Orthop Relat Res. 1984:125–141. [PubMed]
- 61.Malhotra D, Kalb S, Rodriguez-Martinez N, et al. Instrumentation of the posterior thoracolumbar spine: from wires to pedicle screws. Neurosurgery. 2014;10(Suppl 4):497–504. doi: 10.1227/NEU.0000000000000489. [DOI] [PubMed] [Google Scholar]
- 62.Mariconda M, Galasso O, Barca P, Milano C. Minimum 20-year follow-up results of Harrington rod fusion for idiopathic scoliosis. Euro Spine J. 2005;14:854–861. doi: 10.1007/s00586-004-0853-7. [DOI] [PubMed] [Google Scholar]
- 63.McGilvray KC, Waldorff EI, Easley J, et al. Evaluation of a polyetheretherketone (PEEK) titanium composite interbody spacer in an ovine lumbar interbody fusion model: biomechanical, microcomputed tomographic, and histologic analyses. Spine J. 2017;17:1907–1916. doi: 10.1016/j.spinee.2017.06.034. [DOI] [PubMed] [Google Scholar]
- 64.Minamide A, Yoshida M, Kawakami M, et al. The use of cultured bone marrow cells in type I collagen gel and porous hydroxyapatite for posterolateral lumbar spine fusion. Spine (Phila Pa 1976) 2005;30:1134–1138. doi: 10.1097/01.brs.0000162394.75425.04. [DOI] [PubMed] [Google Scholar]
- 65.Mobbs RJ, Phan K, Malham G, Seex K, Rao PJ. Lumbar interbody fusion: techniques, indications and comparison of interbody fusion options including PLIF, TLIF, MI-TLIF, OLIF/ATP, LLIF and ALIF. J Spine Surg. 2015;1(1):2–18. doi: 10.3978/j.issn.2414-469X.2015.10.05. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 66.Moftakhar R, Trost GR. Anterior cervical plates: a historical perspective. Neurosurg Focus. 2004;16:E8. doi: 10.3171/foc.2004.16.1.9. [DOI] [PubMed] [Google Scholar]
- 67.Nemoto O, Asazuma T, Yato Y, Imabayashi H, Yasuoka H, Fujikawa A. Comparison of fusion rates following transforaminal lumbar interbody fusion using polyetheretherketone cages or titanium cages with transpedicular instrumentation. Euro Spine J. 2014;23:2150–2155. doi: 10.1007/s00586-014-3466-9. [DOI] [PubMed] [Google Scholar]
- 68.Ni J, Zheng Y, Liu N, Wang X, Fang X, Phukan R, Wood KB. Radiological evaluation of anterior lumbar fusion using PEEK cages with adjacent vertebral autograft in spinal deformity long fusion surgeries. Euro Spine J. 2015;24:791–799. doi: 10.1007/s00586-014-3745-5. [DOI] [PubMed] [Google Scholar]
- 69.Oliver JD, Goncalves S, Kerezoudis P, et al. Comparison of outcomes for anterior cervical discectomy and fusion with and without anterior plate fixation: a systematic review and meta-analysis. Spine (Phila Pa 1976) 2018;43:E413–E422. doi: 10.1097/BRS.0000000000002441. [DOI] [PubMed] [Google Scholar]
- 70.Omeis I, DeMattia JA, Hillard VH, Murali R, Das K. History of instrumentation for stabilization of the subaxial cervical spine. Neurosurg Focus. 2004;16:E10. doi: 10.3171/foc.2004.16.1.11. [DOI] [PubMed] [Google Scholar]
- 71.Paxinos O, Ghanayem AJ, Zindrick MR, et al. Anterior cervical discectomy and fusion with a locked plate and wedged graft effectively stabilizes flexion-distraction stage-3 injury in the lower cervical spine: a biomechanical study. Spine (Phila Pa 1976). 2009;34(1):E9–E15. doi: 10.1097/BRS.0b013e318188386a. [DOI] [PubMed] [Google Scholar]
- 72.Ranawat CS, O’Leary P, Pellicci P, Tsairis P, Marchisello P, Dorr L. Cervical spine fusion in rheumatoid arthritis. J Bone Joint Surg Am. 1979;61:1003–1010. [PubMed] [Google Scholar]
- 73.Robbins MA, Haudenschild DR, Wegner AM, Klineberg EO. Stem cells in spinal fusion. Global Spine J. 2017;7:801–810. doi: 10.1177/2192568217701102. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 74.Robinson RA, Smith GW. Anterolateral cervical disc removal and interbody fusion for cervical disc syndrome. Bull John Hopkins Hosp. 1955;96:223–224. [Google Scholar]
- 75.Roy-Camille R, Demeulenaere C. Ostéosynthèse du rachis dorsal, lombaire et lombo-sacré par plaques métalliques vissées dans les pédicules vertébraux et les apophyses articulaires. Presse Méd. 1970;78:1447–1448. [PubMed]
- 76.Roy-Camille R, Saillant G, Mazel C. Internal fixation of the lumbar spine with pedicle screw plating. Clin Orthop Relat Res. 1986:7–17. [PubMed]
- 77.Sakaura H, Ohnishi A, Yamagishi A, Ohwada T. Early fusion status after posterior lumbar interbody fusion with cortical bone trajectory screw fixation: a comparison of titanium-coated polyetheretherketone cages and carbon polyetheretherketone cages. Asian Spine J. 2019;13(2):248–253. doi: 10.31616/asj.2018.0169. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 78.Salzmann Stephan N., Shue Jennifer, Hughes Alexander P. Lateral Lumbar Interbody Fusion—Outcomes and Complications. Current Reviews in Musculoskeletal Medicine. 2017;10(4):539–546. doi: 10.1007/s12178-017-9444-1. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 79.Schwartz M. The life and works of Louis Pasteur. J Appl Microbiol. 2001;91:597–601. doi: 10.1046/j.1365-2672.2001.01495.x. [DOI] [PubMed] [Google Scholar]
- 80.Shaw KA, Griffith MS, Shaw VM, Devine JG, Gloystein DM. Harvesting autogenous cancellous bone graft from the anterior iliac crest. JBJS Essent Surg Tech. 2018;8:e20–e20. doi: 10.2106/JBJS.ST.17.00068. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 81.Sheha ED, Meredith DS, Shifflett GD, et al. Postoperative pain following posterior iliac crest bone graft harvesting in spine surgery: a prospective, randomized trial. Spine J. 2018;18(6):986–992. doi: 10.1016/j.spinee.2017.10.011. [DOI] [PubMed] [Google Scholar]
- 82.Simmonds MC, Brown JV, Heirs MK, Higgins JP, Mannion RJ, Rodgers MA, Stewart LA. Safety and effectiveness of recombinant human bone morphogenetic protein-2 for spinal fusion: a meta-analysis of individual-participant data. Ann Intern Med. 2013;158(12):877–889. doi: 10.7326/0003-4819-158-12-201306180-00005. [DOI] [PubMed] [Google Scholar]
- 83.Smith KA, Russo GS, Vaccaro AR, Arnold PM. Scientific, clinical, regulatory, and economic aspects of choosing bone graft/biological options in spine surgery. Neurosurgery. 2019;84(4):827–835. doi: 10.1093/neuros/nyy322. [DOI] [PubMed] [Google Scholar]
- 84.Tapia JL, Suresh L, Plata M, Aguirre A. Ancient esthetic dentistry in Mesoamerica. Alpha Omegan. 2002;95(4):21–24. [PubMed] [Google Scholar]
- 85.Tarpada SP, Morris MT, Burton DA. Spinal fusion surgery: a historical perspective. J Orthop. 2016;14:134–136. doi: 10.1016/j.jor.2016.10.029. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 86.Thompson Walter A. L., Ralson Edgar L. PSEUDARTHROSIS FOLLOWING SPINE FUSION. The Journal of Bone & Joint Surgery. 1949;31(2):400–405. [PubMed] [Google Scholar]
- 87.Thompson WA, Gristina AG, Healy WA., Jr Lumbosacral spine fusion: a method of bilateral posterolateral fusion combined with a Hibbs fusion. J Bone Joint Surg Am. 1974;56:1643–1647. [PubMed] [Google Scholar]
- 88.Tuli SM. Historical aspects of Pott’s disease (spinal tuberculosis) management. European Spine J. 2013;22(Suppl 4):529–538. doi: 10.1007/s00586-012-2388-7. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 89.Urist MR. Bone: formation by autoinduction. Science. 1965;150:893–899. doi: 10.1126/science.150.3698.893. [DOI] [PubMed] [Google Scholar]
- 90.Urist MR. The classic: a morphogenetic matrix for differentiation of bone tissue. Clin Orthop Relat Res. 2009;467(12):3068–3070. doi: 10.1007/s11999-009-1070-9. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 91.Venable CS, Stuck WG. Three years’ experience with vitallium in bone surgery. Ann Surg. 1941;114:309–315. doi: 10.1097/00000658-194108000-00014. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 92.Viswanathan VK, Rajaram Manoharan SR, Subramanian S, Moon A. Nanotechnology in spine surgery: a current update and critical review of the literature. World Neurosurg. 2019;123:142–155. doi: 10.1016/j.wneu.2018.11.035. [DOI] [PubMed] [Google Scholar]
- 93.Wagner PC, Grant BD, Bagby GW, Gallina AM, Sande RD, Ratzlaff MJ. Evaluation of cervical spinal fusion as a treatment in the equine “wobbler” syndrome. Vet Surg. 1979;8(3):84–88. [Google Scholar]
- 94.Wang M, Lam RW, Abbah SA, et al. Heparin-based polyelectrolyte complex enhances the therapeutic efficacy of bone morphogenetic protein-2 for posterolateral fusion in a large animal model. Spine (Phila Pa 1976) 2016;41:1199–1207. doi: 10.1097/BRS.0000000000001543. [DOI] [PubMed] [Google Scholar]
- 95.Wang W, Miao Y, Zhou X, et al. Local delivery of BMP-2 from poly(lactic-co-glycolic acid) microspheres incorporated into porous nanofibrous scaffold for bone tissue regeneration. J Biomed Nanotech. 2017;13:1446–1456. doi: 10.1166/jbn.2017.2445. [DOI] [PubMed] [Google Scholar]
- 96.Watkins MB. Posterolateral fusion of the lumbar and lumbosacral spine. J Bone Joint Surg Am. 1953;35-a:1014–1018. [PubMed] [Google Scholar]
- 97.Weiner BK. Lumbar interbody cages. Spine (Phila Pa 1976) 1998;23:634–640. doi: 10.1097/00007632-199803010-00020. [DOI] [PubMed] [Google Scholar]
- 98.Weiner BK. Historical perspective: the development and use of spinal disease categories. Spine (Phila Pa 1976). 2008;33(8):925–930. doi: 10.1097/BRS.0b013e31816b4738. [DOI] [PubMed] [Google Scholar]
- 99.Weiner BK, Fraser RD. Spine update lumbar interbody cages. Spine (Phila Pa 1976) 1998;23:634–640. doi: 10.1097/00007632-199803010-00020. [DOI] [PubMed] [Google Scholar]
- 100.Yasko AW, Lane J, Fellinger E, Rosen V, Wozney J, Wang EA. The healing of segmental bone defects, induced by recombinant human bone morphogenetic protein (rhBMP-2). A radiographic, histological, and biomechanical study in rats. J Bone Joint Surg Am. 1992;74:659–670. [PubMed] [Google Scholar]
- 101.Zucherman J, Hsu K, White A, Wynne G. Early results of spinal fusion using variable spine plating system. Spine (Phila Pa 1976) 1988;13:570–579. doi: 10.1097/00007632-198805000-00024. [DOI] [PubMed] [Google Scholar]
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