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A Comparison of Mesenchymal Precursor Cells and Amnion Epithelial Cells for Enhancing Cervical Interbody Fusion in an Ovine Model

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A Comparison of Mesenchymal Precursor Cells and Amnion Epithelial Cells for Enhancing Cervical Interbody Fusion in an Ovine Model RESEARCH—ANIMAL TOPIC Research—Animal A Comparison of Mesenchymal Precursor Cells and Amnion Epithelial Cells for Enhancing Cervical Interbody Fusion in an Ovine Model Tony Goldschlager, MBBS, BACKGROUND: Rapid, reliable fusion is the goal in anterior cervical diskectomy and PhD*‡{‡‡ fusion. Iliac crest autograft has a high rate of donor-site morbidity. Alternatives such as Peter Ghosh, DSc, PhD§** bone graft substitutes lack osteoinductivity, and recombinant bone morphogenetic Andrew Zannettino, PhD# proteins risk life-threatening complications. Both allogeneic mesenchymal precursor cells (MPCs) and amnion derived epithelial cells (AECs) have osteogenic potential. Mark Williamson, DVM, PhD‡‡ Jeffrey Victor Rosenfeld, MD, OBJECTIVE: To compare for the first time the capacity of MPCs and AECs to promote FRACS‡k osteogenesis in an ovine model. Silviu Itescu, MD, PhD§ METHODS: Five groups of 2-year-old ewes were subjected to C3-4 anterior cervical diskectomy and fusion with a Fidji interbody cage packed with iliac crest autograft alone Graham Jenkin, PhD§§ (group A; n = 6), hydroxyapatite-tricalcium phosphate Mastergraft granules (HA/TCP) *Monash Immunology and Stem Cell alone (group B; n = 6), HA/TCP containing 5 million MPCs (group C; n = 6), or HA/TCP Laboratories, Melbourne, Victoria, Australia; containing 5 million AECs (group D; n = 5); group E was made up of age-matched ‡Department of Surgery, Monash Uni- versity, Melbourne, Victoria, Australia; nonoperative controls (n = 6). At 3 months, animals were euthanized and quantitative §Mesoblast Ltd, Melbourne, Victoria, multislice computed tomography, functional radiography, biomechanics, histology, and Australia; {Department of Neurosurgery, histomorphometry were performed. Monash Medical Centre, Clayton, Victoria Australia; kDepartment of Neurosurgery, RESULTS: No procedure- or cell-related adverse events were observed. There was sig- The Alfred Hospital, Prahran, Victoria, nificantly more fusion in the MPC group (C) than in group A, B, or D. Computed Australia; #Centre for Cancer Biology, tomography scan at 3 months revealed that 5 of 6 MPC-treated animals (83%) had Institute of Medical and Veterinary Sci- ence/SA Pathology and Robinson Insti- continuous bony bridging compared with 0 of 5 AEC-treated and only 1 of 6 autograft- tute, University of Adelaide, South and 2 of 6 HA/TCP-treated animals (P = .01). Australia, Australia; **Institute of Bone and Joint Research, Royal North Shore CONCLUSION: Implantation of allogeneic MPCs in combination with HA/TCP within an Hospital, St Leonards, New South Wales, interbody spacer facilitates interbody fusion after diskectomy. The earlier, more robust Australia; ‡‡Gribbles Pathology Pty Ltd, fusion observed with MPCs relative to autograft and HA/TCP bone substitute indicates Clayton, Victoria, Australia; §§Ritchie Centre, Monash Institute of Medical that this approach may offer a therapeutic benefit. Research, Monash University, Clayton, KEY WORDS: Amnion epithelial cell, Anterior cervical diskectomy and fusion, Biologics, Mesenchymal stem Victoria, Australia cell, Sheep, Spine fusion, Stem cells Correspondence: Neurosurgery 68:1025–1035, 2011 DOI: 10.1227/NEU.0b013e31820d5375 www.neurosurgery-online.com Dr Tony Goldschlager, MBBS, PhD, Department of Neurosurgery, Monash Medical Centre, 246 Clayton Rd, Clayton, ultiple strategies for interbody grafting fusion because it fulfills these criteria in that it Victoria 3168, Australia. are used in anterior cervical diskectomy contains live cells and growth factors within the E-mail: 1 2 [email protected] Mand fusion surgery. The ideal graft extracellular matrix. However, autograft may should be osteogenic, osteoconductive, and os- result in short- or long-term problems such as Received, February 20, 2010. teoinductive, as well as mechanically stable and prolonged operation time, increased blood loss, Accepted, June 10, 2010. disease free.2,3 Autograft has traditionally been and donor-site morbidity.2,4,5 To alleviate these the gold standard source material for cervical difficulties, alternatives such as allograft cadav- Copyright ª 2011 by the Congress of Neurological Surgeons eric bone and synthetic bone substitutes are used. However, these alternatives are inferior to ABBREVIATIONS: AEC, amnion epithelial cell; autograft because they have limited osteoin- HA/TCP, hydroxyapatite/tricalcium phosphate; ductive properties and depend on the local IVA, intervertebral angle; LA, lordosis angle; 2,4 MPC, mesenchymal precursor stem cell in-growth of osteogenic precursor cells. More- over, the levels and bioactivity of osteogenic NEUROSURGERY VOLUME 68 | NUMBER 4 | APRIL 2011 | 1025 Copyright © Congress of Neurological Surgeons. Unauthorized reproduction of this article is prohibited. Copyright © Congress of Neurological Surgeons. Unauthorized reproduction of this article is prohibited. GOLDSCHLAGER ET AL precursor cells within autographs decline with age, an issue that with monoclonal antibodies23 to STRO-3+ and manufactured by Lonza may reduce bone fusion in the elderly.3 Other factors that may Inc (Walkersville, Maryland) under good manufacturing practice independently decrease fusion rates include multilevel surgery, guidelines. The MPCs were derived from a single batch and culture 6 7,8 expanded to passage 4. The MPC surface marker characteristics have rheumatoid arthritis, smoking, and the concomitant use of 24 antiinflammatory medications.9 If fusion does not occur, a pseu- previously been reported. The optimal dose and matrix combination were determined previously by our group. doarthrosis results, commonly causing recurrent radiculopathy and 10 The cells were frozen and maintained in the vapor phase of a liquid neck pain that may require surgical revision. nitrogen tank until thawed and used within 30 minutes. Cellular via- Recombinant human bone morphogenetic proteins have been bility was determined before implantation using Trypan Blue exclusion tried as osteoinductive agents in the cervical interbody space and and was . 85%. have demonstrated increased fusion rates.11,12 Significantly, this advantage comes with an increase in complication rates of up to Amnion Epithelial Cells 1 24%, including life-threatening complications such as airway After institutional ethics approval (Monash Medical Centre, Clayton, 13 and neurological compression. Australia) and patient informed consent were obtained, discarded term Allogeneic mesenchymal precursor stem cells (MPCs) are placentas were collected from elective caesarean section deliveries. The derived from donor bone marrow and were recently shown to cells were harvested by the method previously described,19 culture ex- increase bone fusion rates in other indications.14-16 Allogeneic panded, and then frozen and maintained in the vapor phase of a liquid amnion epithelial cells (AECs) are readily available from discarded nitrogen tank until thawed and used within 30 minutes. Cellular via- afterbirth tissue; therefore, an invasive procedure such as bone bility was . 80% using Trypan Blue exclusion. The cells were char- marrow aspiration is not required to harvest them. AECs are acterized with monoclonal antibodies and flow cytometry as previously described (Figure 1). derived from epiblast cells before gastrulation that migrate along 17 the walls of the amniotic cavity to form the amnion epithelium. Interbody Cage and Carrier It has been hypothesized, therefore, that they retain pluri- 3 3 potency18 and are able to be differentiated down all 3 germ cell The interbody cage (7.7 12 15 mm) was made from poly- etheretherketone and was packed with iliac crest autograft cancellous lineages.18,19 In relation to the present study, AECs are reported 17,19,20 bone in the autograft control group. The HA/TCP carrier was mixed to show significant osteogenic differentiation potential. with autologous blood and then packed into the cage in the HA/TCP Both AECs and MPCs exhibit low immunogenicity and an- alone group. In the cell-treated groups, the MPCs or AECs were added to 18,21 tiinflammatory properties, which diminish their potential to the carrier within the cage and allowed to soak into the granules, avoiding elicit an immune response when transplanted to an allogeneic spillage (Figure 2). host. Human AECs fail to induce a xenogeneic mixed lym- phocyte reaction in animal models and exhibit minimal major Surgical Technique and Postoperative Care histocompatibility complex class I and II expression, supporting The surgical procedure has been previously described25 and was 18 the use of AECs xenogeneically. In the present study, we carried out with institutional ethics approval (School of Biomedical compared the capacity of allogeneic ovine MPCs with human Sciences, Monash University). Animals were fasted 12 to 24 hours before AECs to promote cervical interbody fusion in an ovine model of surgery and were allowed water ad libitum. Sheep were anaesthetized by cervical diskectomy. intravenous injection of thiopentone 20 mg/kg and anesthesia main- tained by isoflurane (1%-3%) inhalation and were positioned supine on the operating table. Local anesthetic (0.5% Bupivicaine with 1:200 000 METHODS adrenaline) was injected before a right anterolateral approach through a longitudinal neck incision. The longus colli muscle was elevated bi- Study Design laterally with diathermy, and the position of the C3-4 level was con- firmed with fluoroscopy. Distraction was achieved with 16-mm Caspar Twenty-nine 2-year-old Boarder-Leicester/Merino ewes were divided
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