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Reference: Biol. Bull. 197: I 1-13. (August 1999) Regeneration of Amputated Avian Bone by a Coral Skeletal Implant B. RINKEVICH1 S. BEN-YAKIR2 AND R. BEN-YAKIR2 , , ' National Institute ofOceanography, Tel Shikmona, P.O.B. 8030, Haifa 31080, Israel: and 2 Hod-Hasharon Veterinan< Clinic, 17 Gordon Street, Hod Hasttaron, Israel Bone fractures are common in both wild and captive avian bones (3-5) results in problems that are not encoun- birds (I, 2). Avian bones are thin and brittle and tend to tered in mammals. break intofragments or shatter upon a variety ofnatural We recently investigated the use of coral skeleton as a events (midair collisions, fights with other animals; ref. 2) natural intramedullary fixation device for fractures of bird or anthropogenic experiences (wounding by gunfire, colli- bone and found that fractured avian bones can be rehabili- sions with cars orfences, encounters with traps, attacks by tated following the internal implantation of coral skeletal dogs or cats, etc.; ref. 1). The prospect offull recovery pins (unpubl. data). This investigation was based on studies following repair ofavion bonefracture is often poor, and with mammals (including humans) documenting that coral the complication rate is high (3). For wild birds, anything skeletons may be employed as osseous substitutes, as scaf- less than complete normal function cannot be regarded as folds for direct osteoblastic application, or as an artificial successful, and slight malunion or a change in a few de- bone filler forrepairing bone defects (6, 7). The coral tested greesofrotation canproducea severe lossofflightfunction here was ofthe branching species Stylophorapistillata, one (4). Furthermore, in nomadic species, time is critical be- of the most abundant coral species in the Gulf of Eilat (8). cause long periods ofrehabilitation may prevent the birds Mature domestic pigeons (Colmnba Hvia domestica) from reunitingwith theirflocks. In experiments with implan- were randomly assigned to a variety oftreatment groups (in tation offragments ofskeleton from the coral Stylophora preparation). For all radiographic and surgical procedures, pistillata, wefound the implants to be avion osteo-conduc- the birds were given Halothane as a general anesthetic. The tive biomaterial, acting as a scaffoldfora directosteoblas- skin was prepared for aseptic surgery using a septal scrub tic deposition. In the case study presented here, the bird followed by a povidone-iodine wash. Whenever possible, regained completeflight activity within 2 weeks after sur- flight feathers were not removed or clipped; others were gery, withfull regeneration ofthe amputated ulna. pluckedoverthe intended incision. Reflexesandcardiac and The general principles for treating fractures in birds are respiratory activities were monitored. Birds were placed on similar to those established for mammals and include rigid their backs and a limited ventral approach to the ulna was stabilization (primary bone healingdoes notoccurifthere is performed. Two of the same bones from the wings of two a gap or motion at the fracture site; ref. 4). However, birds were used as experimental and control bones (ban- treatment such as external coaptation (slings, bandages, daged in the traditional manner; ref. 5). Small processed casts, splints, etc.), intramedullary pins or rods, bone plate coral pins were obtained from SagivCoral, P.O. Box 3337, fixation, or modifications ofany ofthe traditional means of Ramot Hashavim 45930, Israel. Postoperative radiographs external skeleton fixation (3-5) not only fails for rehabili- were taken to evaluate fracture repair and to document the tating wild birds, but also involves prolonged hospitaliza- status of the coral implant. Pigeons were housed in the tion of avian patients. Internal fixation is one of the best flypen system and fed with a commercial pigeon food procedures forfracture management,butthebrittle natureof supplemented with vitamin D and oyster shell as a calcium source. Received 26 January 1999; accepted 23 April 1999. In one of the experiments, which is detailed in this E-mail: [email protected] communication, the proximal half of the ulna (which pro- 11 B. RINKEVICH ET AL Figure 1. Progressive repairofulna fracture treated hy implantation ofan intramedullary coral pin (a-e), comparedtocontrol,anuntreatedamputatedulna(fl.Weeksafteroperation: a = 2. h = 4,c = 6,d = 8,e,f= 12. vides primary support for the wing) was accidentally com- in layers and the first sign of coral resorption was evident. minuted during surgery. Full rehabilitation of this amputa- During resorption. which was significantly advanced at 8 tion hone by the use of coral skeleton implant is described and 12 weeks (Fig. Id, e), radiography showed that the area here. between the two ends of the broken ulna was being filled In thecaseofthe accidentallycomminuted ulna, all brittle with accumulated new bone, replacing the degradable pin. fragments were immediately removed and a small coral pin Sft'liiplwni pistillntti skeleton (although its mechanical and mm mm (24 length.4 diameter) was first passeddistally and biological properties were notyetevaluated) was thus found then retrogradely until resistance was met at the proximal to be avian osteo-conductive biomaterial, acting as a scaf- side of the ulna. The coral pin was then firmly wedged in fold fordirect osteoblastic deposition. The birdregained full place, forming an inert calcium carbonate milieu between flight activities 2 weeks after surgery, and the coral pin the two separated parts, replacing the amputated portion of activated skeletal regeneration (compare with the control; the ulna. This pigeon used the treated wing freely 14 days Fig. If). This process ended in complete regeneration ofthe after the operation, alleviating ankylosis resulting fromjoint amputated area. immobilization. In the control bird, the entire segment of This case of regeneration of an amputated bone and our proximal ulnar bone (cortex and medulla) was removed study (in prep.) demonstrate the value of coral skeletal using Gilgi wire. implants for avian bone repair. Coral material (calcium Two weeks after the operation, the coral pin was encap- carbonate) is well tolerated by bird tissue. The pin matrix is sulated firmly at both ends by overgrown calcium deposits porous enough to be colonized by the birds' bony cells, is and callus formation along the pin shall, providing rota- biodegradable, and is easily adjustable in size and shape to tional stability (Fig. la). After 4 weeks (Fig. Ib). the coral the osseous site of grafting. Previous studies employing implant was already overgrown by deposited material. By 6 coral implants for bone repair in mammals have shown that weeks (Fig. Ic), deposited material surrounded the implant coral resorption rates varied with porosity of the coral CORAL IMPLANTS IN AVIAN FRACTURES 13 species used and with host reaction (9). We used natural 2. Houston,D.C. 1993. Theincidenceofhealedfracturestowingbones fragments of 5. pistillata skeletons, the first pocilloporid ofWhite-backedand Ruppell'sGriffonVulturesGypsafricaiiusandG. coral used in vertebrate skeleton rehabilitation. Each year, 3. Mntatt'phpet'wtsln,aKn.dGo.t,heLr.biJr.dsW.alIlbiasce1,35P:.4T6.8-R4e7d5ig., J. E. Bechtold, R. R. around the globe, veterinarians tend an ever-increasing Pool, and V. L. King. 1994. Avian fracture healing following stabi- number of wild and domestic birds with broken bones; lization with mtramedullary polyglycolic acid rods and cyanoacrylate unfortunately, at present the prognosis for many of these adhesive vs. polypropylene rods and polymethylmethacrylate. Vel. birds is poor. The approach described here may provide a Comp. Orthop. Trauma 7: 15X-169. fast and dependable method for rehabilitation ofavian frac- 4 Bennett, R. A., and A. B. Kuzma. 1992. Fracture management in tures, increasing the survival rate of birds treated for bone 5. bMiardcsC.oJy.,ZoDo..MW.ild1l99M2e.il.T2r3e:at5m-e3n8t.of fractures in avian species. Vet. injuries. dm. North Am. Small Aiiini. Pract. 22: 225-238. 6. Kehr, P. H., A. G. Graftiaux, F. Gosset, I. Bogorin, and K. Ben- Acknowledgments cheikh. 1993. Coral as a graft in cervical spine surgery. Ortlmp. Traumarol. 3: 287-293. This study was supported by the Minerva Center for 7 Guillemin, G., J-L. Patat, and A. Meunier. 1995. Natural corals Marine Invertebrate Immunology and Developmental Biol- used as bone graft substitutes. Bull. lust. Oceanogr. (Monaco) 14: ogy. Animal surgeries and treatments were conducted in 67-77. conformance with the guidelines of the Canadian Council 8. Loya, V. 1976. The Red Sea coral Stylophora pistillata is an r on Animal Care. strategist. Nature (Land.) 259: 478-480. 9. Roudier, M., C. Bouchon.J. I.. Rouvillain,J. Amedee, R. Bareille, F. Rouais, J. Ch. Fricain, B. Dupay, P. Kien, R. Jeandot, and B. Literature Cited Basse-Cathalinat. 1995. The resorption of bone-implanted corals 1. Fix, A. S., and S. Z. Barrows. 1990. Raptors rehabilitated in Iowa varies with porosity but also with the host reaction. J. Biomed. Mater. during 1986 and 1987: aretrospective study.J. Wildl. Dis. 26: 18-21. Res. 29: 909-915.