Acquisition of Autologous Cancellous Bone Graft using the Manubrium in Dogs undergoing Atlantoaxial Surgical Stabilization

Abstract

Objective

The aim of this study was to describe the feasibility of obtaining autologous cancellous bone graft from the manubrium in toy breed dogs undergoing ventral stabilization for naturally occurring atlantoaxial subluxation

Study Design

A retrospective descriptive study involved four dogs with naturally occurring atlantoaxial subluxation, which underwent ventral stabilization. In all dogs, the manubrium was surgically exposed and cancellous bone graft was harvested.

Results

In all dogs, the surgical approach to the manubrium subjectively was judged to be easy. Additional instrumentation other than that used for ventral stabilization of the atlantoaxial joint was not needed. In all dogs, the manubrium provided sufficient cancellous bone graft to fill the ventral region of the atlantoaxial joint cavity. No intraoperative or short-term complications were observed.

Clinical Significance

The manubrium provided for an acceptable donor site for autologous cancellous bone graft in dogs undergoing atlantoaxial stabilization. The manubrium may serve as an easily accessible alternative graft donor site in lieu of the proximal humerus. Future investigation into the robustness of the bone forming potential of cancellous bone from the manubrium may be warranted.

Keywords

atlantoaxial subluxation - cancellous bone graft - manubrium

Introduction

Atlantoaxial subluxation (AAS) is most commonly observed as a congenital or developmental disorder affecting young, toy breed dogs such as the Yorkshire terrier, Chihuahua, and toy poodle.[1] [2] As a consequence of structural anomalies involving the dens (aplasia, hypoplasia, or incomplete ossification), ligaments of the atlantoaxial (AA) joint, or a combination of both, AAS may occur.[1] [2] Clinical signs range from cervical pain alone to tetraplegia, hypoventilation and death as a consequence of spinal cord compression.[1] [2] Treatment options include conservative therapy and surgical stabilization. Conservative therapy involves external coaptation and exercise restriction.[3] Surgical stabilization techniques are broadly categorized as dorsal or ventral stabilization procedures.[4] Ventral stabilization techniques confer several advantages over dorsal techniques principally in enabling more proper AA joint alignment and exposure to the relatively robust bone stock of the vertebral bodies compared with the laminae for implant placement.[5] Ventral stabilization also may provide more rigid fixation.[6] Of additional benefit, ventral stabilization techniques provide a means for arthrodesis achieved with debridement of the articular cartilage of the AA joint and application of autologous cancellous bone graft (ACBG).[1] [2] [7] While almost any bone can serve as a donor site, graft material is commonly harvested from the proximal humerus.[8] While donor site complications rarely occur, obtaining ACBG from the proximal humerus can be challenging. The small size of the humerus in toy breed dogs, the accessibility, and the immobility of the limb as patients undergoing AA stabilization are typically secured on the surgical table using limb restraints create a need to identify an alternative donor site for obtaining ACBG. The aim of the present study is to describe the use of the manubrium as a donor site for ACBG in four dogs undergoing ventral stabilization of the AA joint.

Case Report

Dogs included a miniature poodle, Maltese terrier, Yorkshire terrier, and Chihuahua. Dogs ranged in age from 8 to 23 months. There were two spayed females, one neutered male, and one intact male dog. Body weights ranged from 1.2 to 2.5 kg. All dogs displayed signs consistent with a C1–C5 myelopathy. Three dogs presented less than 7 days from onset of signs, whereas one dog had a 21-day course of progressive signs. In two dogs, signs were precipitated by running into an object. Two dogs were ambulatory with subjectively mild and moderate general proprioceptive ataxia/upper motor neuron tetraparesis. Two dogs were tetraplegic. In all dogs, the diagnosis was established with radiographs and magnetic resonance imaging. All dogs underwent a modified ventral fixation technique using 1.5 mm diameter by 6 mm length, self-drilling, titanium cortical screws, 0.9-mm diameter Kirschner wires, and polymethylmethacrylate as previously described.[9] Prior to application of polymethylmethacrylate, ACBG was harvested from the manubrium.

In all dogs, a <2- to 3-cm ventral midline skin incision was made over the manubrium. In two dogs, the midline attachments of the pectoral muscles were elevated using a freer elevator to expose an approximately 1.0 to 1.5 cm² area of the ventral aspect of the manubrium ([Fig. 1]). In two dogs, a number 15 scalpel blade was used to remove cartilage covering the manubrium. In two dogs, a 1.0-mm burr and high-speed pneumatic drill was used to create a defect in the manubrium, whereas in the other two dogs, this was not necessary. A 5/0 Spratt bone curette was used to harvest grossly normal-appearing cancellous bone. A Brown Adson forceps was used to stabilize the manubrium during curettage. Curettage resulted in creating a small cavity within the manubrium; in one dog the bone of the dorsal and lateral sides of the manubrium was visible within the cavity. Cancellous bone was harvested and stored in the barrel of a 5-mL syringe. Once enough graft was harvested to fill the exposed ventral AA joint cavity, the graft was immediately placed in the AA joint cavity and the stabilization procedure was completed. Except for the far lateral aspects of the AA joint, enough ACBG was obtained in all dogs to fill the AA joint level to the ventral margin of the articular cartilage of the axis. A two-layer routine closure was done over the manubrium. Immediate postoperative radiographs and computed tomography of the cervical vertebral column revealed a reduction of the AAS, anatomical alignment of the AA joint, and appropriate implant placement in all dogs. Postoperative hospitalization ranged from 3 to 8 days. During hospitalization, all dogs demonstrated neurological improvement. No complications involving the incision over the manubrium or manubrium itself were seen. No dogs appeared painful at the donor site.

At the time of discharge, the two dogs that were ambulatory preoperatively remained ambulatory. One dog had improved to a normal neurological exam at discharge and remained normal on examination at 3 and 10 months, postoperatively. The other dog had a normal neurological exam at 33 days postoperatively. At the time of discharge, the two dogs that were tetraplegic preoperatively had improved to nonambulatory tetraparesis. One dog regained the ability to walk unassisted by approximately 40 days postoperatively based on telephone follow-up and a video provided by the owner. Three dogs maintained the ability to walk unassisted based on telephone conversation approximately 1 year postoperatively. One dog (tetraplegic preoperatively) was lost to follow-up.

Discussion

In veterinary medicine, ACBG is frequently used as a means to enhance bone formation. Such grafts are ideal insofar as promoting bone healing via osteogenic, osteoinductive, osteoconductive, and even osteopromotion functions.[8] They are relatively easy to obtain, and as an autograft, they lack histocompatibility issues.[8] For long-term success of AA stabilization procedures, decompression and permanent arthrodesis of the AA joint are considered important.[7] [10] The use of ACBG promotes arthrodesis.[11] As with other synovial joints, the application of ACBG within the AA joint cavity likely aides arthrodesis consequent to ingrowth of fibrous tissue, cartilage, and bone.[7] [12] Typically, ACBG is obtained from the proximal humerus during the ventral AA stabilization procedures. Acquisition of graft at the time of surgical stabilization avoids delay in grafting, which likely supports graft viability. Although complications are rare, fracture and premature closure of the proximal humeral physis can occur.[13] [14] Moreover, it can be challenging to obtain graft from a relatively small humerus of small and toy breed dogs with AAS, given the need to immobilize the thoracic limbs for positioning for ventral stabilization procedures. With the thoracic limbs immobilized, it can be difficult to manually stabilize the humerus during curettage; in some instances, bone grasping forceps or clamps may be needed. Consequently, it may be advantageous to identify an alternative donor site. In dorsal recumbency, the manubrium is easily accessed and contains cancellous bone. Although the manubrium in small and toy breed dogs also is small, the use of the manubrium as a donor site for ACBG may provide advantages over the humerus. As a nonweight-bearing bone, postoperative pain or complications from iatrogenic fracture of the manubrium are likely inconsequential. Moreover, optimal positioning for a ventral stabilization procedure for AAS provides ready access to the manubrium, thereby minimizing surgical time and likely reducing the time between harvesting and grafting. Finally, with the exception of a bone curette, additional instrumentation beyond that used for surgical stabilization of AAS was not needed. The manubrium was readily held stable using a Brown Addison during curettage negating the need for bone forceps or clamps.

The manubrium is used as a donor site for ACBG in horses. Cancellous bone from the manubrium in horses is microscopically similar to other donor sites.[15] Based on gross visual inspection of cancellous bone from the manubrium in the present cases, the manubrium in dogs may be an equally suitable donor site for cancellous bone graft, as it is in the horse. In the dogs described here, exposure of the manubrium did not necessitate altered patient positioning. Access to the manubrium was easily gained through a <2- to 3-cm incision, minimal dissection of subcutaneous fat, and elevation of the pectoral muscle attachments. In two dogs, it was necessary to use a high-speed pneumatic drill to gain access to the cancellous bone of the manubrium. In two dogs, once the surface cartilage was removed using a scalpel blade, thereafter a Spratt bone curette enabled access to the cancellous bone. In all dogs, the manubrium provided a sufficient amount of cancellous bone to fill the AA joint level to the ventral aspect of the articular cartilage of the axis. Except for the most lateral aspects of the AA joint, the majority of the joint space was filled with ACBG. While the exact volume of ACBG needed to promote arthrodesis of the AA joint is unknown, subjectively the AA joint was not considered underfilled. Likewise, overfilling may not enhance more rapid osteogenesis.[16] Finally, no intraoperative or postoperative complications were observed in any dog.

Our study has several limitations. Only four dogs are described that hinders broad conclusions. However, the dogs reported here reflect the typical signalment and body size of dogs with AAS. Moreover, one dog was 1.2 kg, suggesting small size may not be a limitation. Second, the volume of ACBG harvested and grafted was not quantified or standardized. While 0.3 g may promote bone production in ulnar defects, the volume needed for AA arthrodesis remains unknown.[16] In practice, the volume of ACBG used likely varies between cases. In some studies of surgical stabilization of the AA joint, cases may not be grafted without affecting overall success rates.[4] [5] [10] The same is likely true in the present cases, despite the positive outcome of most of the dogs described here. This stands to reason as the use of ACBG does not affect AA joint alignment or degree of spinal cord decompression.

In the present report, the manubrium subjectively provided a sufficient amount of ACBG to fill the exposed AA joint, which likely replicates common practice. Most important, the viability and biologic efficacy of ACBG from the manubrium were not assessed. To date, studies comparing the efficacy of grafting using ACBG material harvested from different anatomical locations are lacking. In using the manubrium, the graft was harvested and immediately grafted, the viability likely remained high. However, osteogenic potential varies according to donor site.[17] The manubrium in dogs may not have robust osteogenic potential.[17] Ascertainment of the biologic activity with the endpoint of arthrodesis would necessitate a larger study involving a comparison group. Radiographic evidence of bony arthrodesis may be seen by 6 weeks and importantly diagnostic imaging may fail to identify fibrous tissues sufficient to provide immobility of the joint.[7] [18] In the present study, ACBG material was not visible on postoperative computed tomography (CT) imaging. This likely reflects the amount of ACBG used and the bone density of the cancellous bone of the manubrium. It is possible that the cancellous bone of the manubrium has lower bone density than cancellous bone from other sites. Moreover, the attenuation of the normally hyperattenuating cancellous graft material at the recipient site may have been lowered by the admixture of lower attenuating surgical site hemorrhage and irrigation fluids. Such factors likely combined to make the cancellous graft material inconspicuous on CT.

Although the present study may have limited impact on the success of ventral stabilization procedures for AAS, arthrodesis may factor into long-term success. Arthrodesis may be slowed or not achieved without ACBG. Therefore, if the reason for not using ACBG results from difficulty obtaining graft material from the humerus, then it would be paramount to identify more easily accessible donor sites capable of supplying ample cancellous bone. Based on our observations, the manubrium is an acceptable donor site. Furthermore, should the manubrium not provide ample ACBG, the second and perhaps even third sternebrae may be utilized. In the end, studies evaluating the robustness of ACBG from the manubrium and other sternebrae along with the volume of graft needed to enhance arthrodesis of the AA joint in dogs may be warranted.

Conclusion

The manubrium provides for a safe and easily accessible donor site for obtaining ACBG in young, toy breed dogs. Subjectively, an adequate amount of grossly normal-appearing ACBG can be harvested to fill the AA joint in dogs undergoing ventral stabilization procedures for AAS. While technically feasible as evidenced herein, further investigations into the viability and biologic activity of ACBG are needed to ensure cancellous bone harvested from the manubrium will promote arthrodesis.

Fig. 1 (A) A three-dimensional model of the manubrium (M) and second sternebra (S2) was created using a computed tomography study of the thorax of a 5-year-old, 12-kg, mixed breed dog to illustrate the ventral surface of the cranial sternum. The red dotted circle defines an area on the cranial, ventral aspect of the manubrium where cancellous bone can be harvested for grafting. (B) An intraoperative image of an 8-month, spayed female, Yorkshire terrier obtained during surgical atlantoaxial stabilization shows the donor site on the cranial, ventral surface of the manubrium. The overlying skin and subcutaneous tissues are retracted using a 3.5-inch Gelpi retractor (asterisk). The manubrium is outlined (black). The red dotted circle defines the site where cancellous bone was harvested. The dog is positioned in dorsal recumbency and cranial is to the top of the image. (C) Same image as in panel B without annotations.

Conflict of Interest

None declared.

Acknowledgments

None.

Authors Contributions

All authors substantially contributed to the conception and drafting of the manuscript. All authors have approved the manuscript for submission.

• References

• 1 Stalin C, Gutierrez-Quintana R, Faller K, Guevar J, Yeamans C, Penderis J. A review of canine atlantoaxial joint subluxation. Vet Comp Orthop Traumatol 2015; 28 (01) 1-8
• 2 Slanina MC. Atlantoaxial instability. Vet Clin North Am Small Anim Pract 2016; 46 (02) 265-275
• 3 Havig ME, Cornell KK, Hawthorne JC, McDonnell JJ, Selcer BA. Evaluation of nonsurgical treatment of atlantoaxial subluxation in dogs: 19 cases (1992-2001). J Am Vet Med Assoc 2005; 227 (02) 257-262
• 4 Beaver DP, Ellison GW, Lewis DD, Goring RL, Kubilis PS, Barchard C. Risk factors affecting the outcome of surgery for atlantoaxial subluxation in dogs: 46 cases (1978-1998). J Am Vet Med Assoc 2000; 216 (07) 1104-1109
• 5 Stout Steele MW, Hodshon AW, Hopkins AL. et al. Multi-center retrospective evaluation of screw and polymethylmethacrylate constructs for atlantoaxial fixation in dogs. Vet Surg 2016; 45 (07) 909-915
• 6 Riedinger B, Bürki A, Stahl C, Howard J, Forterre F. Biomechanical evaluation of the stabilizing function of three atlantoaxial implants under shear loading: a canine cadaveric study. Vet Surg 2015; 44 (08) 957-963
• 7 Sorjonen DC, Shires PK. Atlantoaxial instability: a ventral surgical technique for decompression, fixation, and fusion. Vet Surg 1981; 10: 22-29
• 8 Martinez SA, Walker T. Bone grafts. Vet Clin North Am Small Anim Pract 1999; 29 (05) 1207-1219
• 9 Platt SR, Chambers JN, Cross A. A modified ventral fixation for surgical management of atlantoaxial subluxation in 19 dogs. Vet Surg 2004; 33 (04) 349-354
• 10 Aikawa T, Shibata M, Fujita H. Modified ventral stabilization using positively threaded profile pins and polymethylmethacrylate for atlantoaxial instability in 49 dogs. Vet Surg 2013; 42 (06) 683-692
• 11 Johnson KA, Bellenger CR. The effects of autologous bone grafting on bone healing after carpal arthrodesis in the dog. Vet Rec 1980; 107 (06) 126-132
• 12 Takahashi F, Hakozaki T, Kanno N. et al. Influence of ventral fixation techniques on atlantoaxial joint fusion in canine models with dens partial resection. J Vet Med Sci 2022; 84 (05) 694-699
• 13 Ferguson JF. Fracture of the humerus after cancellous bone graft harvesting in a dog. J Small Anim Pract 1996; 37 (05) 232-234
• 14 Palmisano MP, Schrader SC. Premature closure of the proximal physis of the humerus in a dog as a result of harvesting a cancellous bone graft. J Am Vet Med Assoc 1999; 215 (10) 1460-1462 , 1447
• 15 Richardson GL, Pool RR, Pascoe JR. et al. Autogenous cancellous bone grafts from the sternum in horses comparison with other donor sites and results of use in orthopedic surgery. Vet Surg 1986; 15: 9-15
• 16 DeVries WJ, Runyon CL, Martinez SA, Ireland WP. Effect of volume variations on osteogenic capabilities of autogenous cancellous bone graft in dogs. Am J Vet Res 1996; 57 (10) 1501-1505
• 17 McDuffee LA, Anderson GI. In vitro comparison of equine cancellous bone graft donor sites and tibial periosteum as sources of viable osteoprogenitors. Vet Surg 2003; 32 (05) 455-463
• 18 Takahashi F, Hakozaki T, Kanno N, Harada Y, Yamaguchi S, Hara Y. Biomechanical evaluation of three ventral fixation methods for canine atlantoaxial instability: a cadaveric study. J Vet Med Sci 2017; 78 (12) 1897-1902

Publication History

Received: 04 December 2023

Accepted: 17 December 2024

Article published online:
25 March 2025