Implantation of surgical constructs (implants) to acquire rigid internal stabilization has been advocated for treatment of dogs with various cervical vertebrae diseases associated with vertebral unit instability.1–8 Conditions for which surgical stabilization is most commonly used to treat vertebral unit instability include vertebral fracture or luxation, caudal cervical stenotic myelopathy, or cervical vertebral malformation–malarticulation syndrome (ie, wobbler syndrome).1,3,9,10 Surgical procedures that internally stabilize portions of the cervical vertebrae may improve clinical outcomes; however, randomized controlled clinical trials in dogs to assess various treatment methods are lacking.8,10 Depending on the nature of the instability, various types of internal stabilization methods have been attempted. There is sparse biomechanical information regarding the stabilizing properties of various implants used to prevent motion of the cervical vertebrae.
One commonly accepted surgical method for stabilization of cervical vertebrae in dogs is application of an implant constructed from interbody smooth or threaded Steinmann pins placed in the vertebral bodies (traditional implant design) combined with overlying PMMA. This implant has been evaluated biomechanically in an uncontrolled clinical trial1 and in an in vitro biomechanical study.7 Although perceived to be biomechanically rigid, use of traditional pin-PMMA implants may be associated with decline in a patient's condition. A devastating complication is misplacement of pins in the vertebral bodies and inadvertent penetration of the vertebral canal or transverse foramen, which results in iatrogenic spinal cord or vertebral artery injury, respectively.7 In 1 in vitro study7 of the traditional pin-PMMA implant, the percentage of pins that were misplaced and penetrated these vital structural areas was as high as 57%. Therefore, an alternative implant design that decreases or eliminates motion of the vertebral unit but is technically easier to perform may be beneficial. One such method involves placing anchoring cortical bone screws in the transverse processes of the cervical vertebrae instead of in the vertebral body. Placing screws in the transverse processes (novel implant design) reduces the likelihood of penetrating the vertebral canal, compared with the likelihood from placing pins in the vertebral bodies, thereby mitigating the risk of iatrogenic injury to the spinal cord.
The objective of the biomechanical study reported here was to determine the change in stiffness of a cervical vertebral specimen after application of a novel screw-bar–PMMA internal fixation implant, compared with the change in stiffness after application of a traditional pin-PMMA internal fixation implant as evaluated by a dorsal bending moment. It was hypothesized that each implant would significantly increase the stiffness of the vertebral column specimens, compared with the stiffness prior to implant application, and there would be no significant difference in the overall change in the stiffness caused by each of these 2 implants. It was also anticipated that there would be a significant decrease in the incidence of transverse foramen or vertebral canal penetration in the novel screw-bar–PMMA implant group, compared with the incidence in the traditional pin-PMMA implant group.
Materials and Methods
Sample population—Twelve vertebral column specimens from C3 through C6 were harvested from cadavers of recently euthanatized dogs. For 11 dogs, results of physical and neurologic examinations performed prior to euthanasia were considered normal. The 12th dog was obtained after euthanasia, but it did not have a clinical history of neurologic disease. Dogs were euthanatized for purposes unrelated to this study. Each dog was mature (> 1 year old), and body weights ranged from 21 to 30 kg. Dual-energy x-ray absorptiometry scansa of each vertebral column were obtained to determine bone mineral density for each vertebra. Scans were performed immediately after euthanasia but before harvesting in all but 1 dog, whose vertebral column was scanned after harvesting.
Each vertebra from C2 through C7, including surrounding musculature, was collected immediately after completion of the dual-energy x-ray absorptiometry scans. Specimens were harvested by sharply removing the cervical region of the vertebral column en bloc from the rest of the cadaver. Digital survey radiography (lateral and dorsoventral views) of each specimen was performed to screen for skeletal abnormalities and to ensure physeal closure. Each specimen was wrapped in a heavy plastic bag and stored at −20°C until the time of the biomechanical study.11
Study design—Specimens were randomly allocated to 2 implant treatment groups. One group (n = 6; traditional pin-PMMA implant group) received implant fixation by use of a design in which positive-profile threaded cancellous pins were threaded through the vertebral bodies.7 A second group (n = 6; novel screwbar–PMMA implant group) received implant fixation by use of a design in which cortical bone screws were threaded into the transverse processes. Biomechanical assessment of each specimen was performed before (unaltered specimens) and after fixation of the intervertebral space between C4 and C5. Mechanical properties were compared within specimens (unaltered vs treated) and between treatments (traditional pin-PMMA implant group vs novel screw-bar–PMMA implant group).
Specimen processing—On the day of mechanical testing, specimens were thawed to room temperature (21°C). The order of testing was chosen randomly and was independent of treatment group. The associated muscles were sharply removed from each specimen by use of scalpel dissection. However, the supporting ligaments were preserved (ligamenta flava, ligamenta interspinalia, synovial joint capsules, annuli fibrosus, and ligamentum longitudinale dorsale).12 The specimen ends, C2 and C7, were removed from the vertebral column via laceration of the ligaments, which left the supporting ligamentous structures intact from C3 through C6. The remaining segment of each original specimen was then used for further testing. During the testing period, all specimens were continuously kept moist with saline (0.9% NaCl) solution by soaking the specimens with mist from a spray bottle or wrapping the specimens with moist gauze.
A custom-made loading jig was used for mechanical testing in a servohydraulic materials-testing system.b The free ends of the cranial aspect of C3 and caudal aspect of C6 of each specimen were anchored in pots by use of PMMA.c This allowed proper placement of the specimen in the loading jig and left the VMUs of C3 and C4, C4 and C5, and C5 and C6 intact (Figure 1). Two 7/64-inch-diameter smooth Steinmann pins were placed through the vertebral body of C3 in orthogonal planes. This step was repeated for the C6 vertebral body. These pins anchored the specimen ends in the center of the pots that contained the PMMA. The PMMA was allowed to air-dry for 30 minutes prior to mechanical testing.
Mechanical testing protocol—Extension testing was performed via 4-point bending to approximate a pure bending moment throughout the length of the specimen. The loading jig applied an even load over the entire specimen length and prevented extraneous compressive or tensile forces on the specimens during testing (Figure 1). Specimens were placed in the jig in a neutral position. Each specimen was deformed at a displacement rate of 50 mm/min until a final actuator displacement of 20 mm was achieved. Prior to actual data collection, each specimen was preconditioned by undergoing 2 full extension cycles. Load-deformation curves were calculated from data recorded for extension during the third through fifth cycles. There was a period of 30 seconds between each cycle to allow elastic tissues to recoil. Displacement was measured by use of an internal linear variable differential transformer with a precision of 0.01 mm. Signals from a load celld recorded force data at a sampling rate of 20 Hz. Digital data were recorded with custom software.e
A preliminary study was performed on similar vertebral column specimens to determine the maximum actuator displacement that maintained the specimens within the physiologic (elastic) range of extension. Actuator displacement > 20 mm caused inelastic deformation of some of the specimens. This was characterized by an abrupt increase in angular deformation without a concomitant increase in bending moment. This was thought to reflect failure of 1 or more of the supporting ligamentous structures. Additionally, actuator displacements > 20 mm caused some of the anchoring pots to bind between the jig supports. This binding created a craniocaudal tensile force. On the basis of the preliminary study findings, it was decided to limit actuator displacement to 20 mm.
After testing of the unaltered specimens, the implants were applied by use of a standardized protocol. Specimens were secured in a vise for the procedures. Any remaining soft tissue was elevated from the ventral aspects of C4 and C5 by use of a periosteal elevator to expose the ventral vertebral bodies, ventral aspect of each transverse process, and associated disk space.
Pin-PMMA implant procedure—Specimens were secured in a neutral position. Two positive-profile threaded pins (1/8-inch-diameter) were placed in each of the vertebral bodies of C4 and C5 (4 pins total), with initial entry points on the ventral aspect of the vertebral bodies near midline. Pins were directed dorsolaterally at an angle of approximately 30° from the sagittal plane of the vertebrae so that they entered the vertebral pedicle. The ventral ends of the pins were cut to a length of 1.5 cm from the point of insertion in the vertebral bodies. A standard plastic mold was contoured in an oval shape to allow uniform application of PMMA that incorporated all of the ventral ends of the pins. Polymethylmethacrylatef was mixed as per manufacturer instructions, poured into the standard plastic mold to cover all pin ends, and allowed to cure for a minimum of 20 minutes.6 Weight of the PMMA was measured and recorded for each implant. Once the implant was completed, the implanted specimens were retested biomechanically as described for the unaltered specimens. Therefore, each specimen was its own control specimen for comparison of unaltered versus treated effects.
Screw-bar–PMMA implant procedure—Specimens were secured in a neutral position. Cortical bone screws (3.5 × 22 mm) were placed bilaterally in the transverse processes of C4 and C5 (1 screw/transverse process). Each screw was implanted in the center of the transverse process perpendicular to the plane of the medial side of the transverse process. Screws penetrated the transcortices (dorsal cortices) by at least 2 threads. Each screw and associated head extended ventromedially approximately 1 cm from the point of insertion in the ventral aspect of the transverse process to the end of the screw head. Holes for screw placement were drilled by use of a 2.5-mm drill bit, and the ciscortex (ventral cortex) was tapped by use of a 3.5-mm thread tap. A nonthreaded Steinmann pin (5/64-inch diameter) was manually contoured around a standard round template to form a U-shape. This contoured pin was wired to the screw heads by use of 20-gauge orthopedic wire to subsequently lie parallel to the ventral aspect of the vertebral column (Figure 2). Polymethylmethacrylate was poured into a standard plastic mold (as used for the pin-PMMA implant) to incorporate the screws, wires, and contoured pin. The PMMA was allowed to cure for a minimum of 20 minutes. Weight of the PMMA was measured and recorded for each implant. Specimens were retested biomechanically as described for the unaltered specimens. Therefore, each specimen was its own control specimen for comparison of unaltered versus treated effects.
Mechanical data analysis—Data were collected from the third through fifth loading cycles, and the mean values at each data point were determined for use in analysis. Bending moment was calculated by use of the following equation: M = ([P × W]/2)/1,000, where M is the bending moment, P is the axial load measured by the machine, and W is the distance between the inner and outer supports of the jig. Angular deformation was calculated by use of the following equation: Θ = atan(([D × {−1/W}]/180)/π), where Θ is the angular deformation, atan is the arc tangent, and D is the displacement of the servohydraulic machine actuator. From these data, load-deformation curves (bending moment vs angular displacement) were generated (Figure 3).
From the load-deformation curves, 8 angular (2°) intervals that were evenly distributed across the entire curve were selected. Stiffness was calculated by use of the equation M/Θ for each data point within each 2° interval. The overall mean stiffness from each interval was used for further analysis.
Pin placement assessment—After completion of the mechanical testing, all soft tissues were removed from the specimens by use of dermestid beetlesg; beetles were allowed to debride the specimens for a duration of 14 days. Each vertebra was inspected visually to assess screw or pin placement and for gross fractures or gross implant failure. A method described in another study7 was used to determine a semiquantitative score to evaluate placement of the screws or pins. Scoring criteria were based on the location of the screw or pin relative to the vertebral canal or transverse foramen. Scores were defined as 0 = no penetration, 1 = penetration into the vertebral canal or transverse foramen that was > 0 to ≤ 0.5 times the diameter of the pin or screw, 2 = penetration that was > 0.5 and < 1 times the diameter of the pin or screw, and 3 = penetration that was ≥ 1 times the diameter of the pin or screw. The distributions of the scores between the groups were assessed to determine differences in pin versus screw placements.
Statistical analysis—For comparison between treatment groups, the stiffness data were fitted to a mixed linear model.h A Fisher least significant difference test was used to determine angular (2°) intervals at which there were significant differences in the measurements between treatment groups. A paired t test was used to compare unaltered with treated specimens. Pin placement accuracy was compared between treatment groups by use of a Fisher exact test. To determine whether bone mineral density, weight of PMMA used in each implant, sex, or neuter status influenced stiffness, the data were fitted to a mixed linear model.h Results for stiffness are reported as EMD, which represents the difference in the calculated stiffness between the groups being compared. Differences were considered to be significant at values of P < 0.05.
Results
Biomechanical data—All treated specimens were significantly (P < 0.001) stiffer than unaltered specimens (EMD, 0.098 N·m/°; 95% CI, 0.074 to 0.122 N·m/°). Analysis between the unaltered and treated specimens was also conducted separately for the lowload, high-deformation region of the load-deformation curve (0° to 10° of angular deformation) and the high-load, low-deformation region of the curve (> 12° of angular deformation). Similar to the findings for the entire load-deformation curve, treated specimens were significantly (P < 0.001) stiffer than unaltered specimens in the low-load, high-deformation region (EMD, 0.0239 N·m/°; 95% CI, 0.0167 to 0.0311 N·m/°) and the high-load, low-deformation region (EMD, 0.1721 N·m/°; 95% CI, 0.1357 to 0.2085 N·m/°; Table 1). There was no significant difference in stiffness between the 2 treatment groups at any interval evaluated.
Mean ± SD stiffness before (unaltered; n = 12 specimens) and after treatment with a traditional pin-PMMA (6) or novel screw-bar–PMMA (6) implant at the intervertebral disk space between C4 and C5 in vertebral column specimens obtained from canine cadavers.
Segment of load-deformation curve (°)* | Unaltered (N·m/°) | Pin-PMMA implant (N·m/°) | Screw-bar–PMMA implant (N·m/°) |
---|---|---|---|
1–3 | 0.0119 ± 0.0129a | 0.0194 ± 0.0091b | 0.0174 ± 0.0115b |
4–6 | 0.0052 ± 0.0044a | 0.0215 ± 0.0137b | 0.0174 ± 0.0154b |
8–10 | 0.0084 ± 0.0161a | 0.0329 ± 0.0192b | 0.0335 ± 0.0365b |
12–14 | 0.0134 ± 0.0229a | 0.0642 ± 0.0304b | 0.0627 ± 0.0432b |
16–18 | 0.0164 ± 0.0089a | 0.1167 ± 0.0315b | 0.0969 ± 0.0475b |
20–22 | 0.0462 ± 0.0474a | 0.1922 ± 0.0499b | 0.1254 ± 0.0876b |
24–26 | 0.0596 ± 0.0244a | 0.3144 ± 0.1286b | 0.2243 ± 0.1078b |
26–28 | 0.0772 ± 0.0306a | 0.3983 ± 0.1805b | 0.3075 ± 0.1554b |
Within a row, values with different superscript letters differ significantly (P < 0.001).
Stiffness within 8 angular (2°) intervals distributed across the load-deformation curves was analyzed.
Pin position—None of the screws in the novel screw-bar–PMMA implant group penetrated the transverse foramen or vertebral canal (score, 0; Table 2). Overall, 22 of the 24 (92%) threaded pins in the traditional pin-PMMA implant group had a score ≥ 1 (ie, some penetration of the vertebral canal or transverse foramen). Two threaded pins did not penetrate the vertebral canal or the transverse foramen and were graded 0 in each category. Vertebral canal penetration (15/24 [62.5%]) was more common than transverse foramen penetration (7/24 [29%]). There was a significant (P < 0.001) difference in the distribution of the placement scores between the treatment groups.
Placement grade distributions of pins or screws from the 2 implants used in surgical stabilization of cervical vertebral specimens obtained from canine cadavers.
Grade* | Vertebral canal | Transverse foramen | ||
---|---|---|---|---|
Pin-PMMA implant (No.) | Screw-bar–PMMA implant (No.) | Pin-PMMA implant (No.) | Screw-bar–PMMA implant (No.) | |
0 | 2 | 24 | 2 | 24 |
1 | 1 | 0 | 1 | 0 |
2 | 6 | 0 | 3 | 0 |
3 | 8 | 0 | 3 | 0 |
There were 24 pins or screws inserted/treatment group. The same pins or screws graded 0 for the vertebral canal were also graded 0 for the transverse foramen. When analyzed together, grade distributions for the vertebral canal and transverse foramen were significantly (P < 0.001) different between the treatment groups.
Grade criteria: 0 = no penetration; 1 = > 0 to ≤ 0.5 times the diameter of the pin or screw penetrated the vertebral canal or transverse foramen; 2 = > 0.5 and < 1 times the diameter of the pin or screw penetrated the vertebral canal or transverse foramen; 3 = ≥ 1 times the diameter of the pin or screw penetrated the vertebral canal or transverse foramen.
Bone mineral density, PMMA, sex, and neuter status—Bone mineral density for all vertebrae ranged from 0.4102 to 0.8204 g/cm2 (mean, 0.6394 g/cm2; median, 0.6497 g/cm2; Table 3). The mean bone mineral density (0.7284 g/cm2) in specimens from female dogs was significantly (P = 0.002; mean ± SE difference, 0.1187 ± 0.0361) increased, compared with the mean bone mineral density (0.6097 g/cm2) in specimens from male dogs. Bone mineral density, weight of PMMA used in each implant, sex, and neuter status were not significantly different between treatment groups.
Mean bone mineral density of cervical vertebrae from 12 cadavers of skeletally mature dogs of various sex and neuter status used in a biomechanical study to assess 2 stabilization implants.
Overall mean (g/cm2)* | Sex | C3 (g/cm2) | C4 (g/cm2) | C5 (g/cm2) | C6 (g/cm2) |
---|---|---|---|---|---|
M | 0.6973 | 0.5969 | 0.5781 | 0.5935 | 0.6165 |
MC | 0.6626 | 0.6092 | 0.5694 | 0.5842 | 0.6063 |
FS | 0.7903 | 0.7471 | 0.7241 | 0.6522 | 0.7284 |
Values for this variable differed significantly (P = 0.002) between male and female dogs.
M = Male, sexually intact (n = 3). MC = Male, castrated (n = 6). FS = Female, spayed (n = 3).
Implant failure—One implant in the traditional pin-PMMA implant group failed, whereas none in the novel screw-bar–PMMA implant group failed. Implant failure was attributed to breakage of the PMMA in the transverse plane midway between the vertebral body pins.
Discussion
The objectives of this in vitro biomechanical study were to determine whether there was a significant difference in stiffness between unaltered and surgically stabilized vertebral column specimens from C3 through C6 of dogs. The specimens were stabilized by use of 1 of 2 implants designed to stabilize the VMU of C4 and C5 and analyzed to determine significant differences in stiffness between the 2 treatment groups.
Surgical stabilization of the cervical region of the vertebral column is performed in dogs that have gross mechanical instabilities (fracture, luxation, or subluxation), vertebral malformation, or disk-associated cervical vertebral malformation–malarticulation syndrome.1,10,13 In vitro biomechanical evaluation of cervical instrumentations is 1 method to compare implants, identify potential design weaknesses, and assist in initial implant development.14 The implants chosen for the present study were a traditional pin-PMMA implant design and a novel screw-bar–PMMA implant design. The novel screw-bar–PMMA implant design was developed to reduce the risk of penetrating the transverse foramen or vertebral canal and to provide rigid internal fixation of VMUs.
Four-point bending was used to approximate a pure bending moment across the length of the vertebral column motion segments (from C3 through C6).2,5 Changes in stiffness after treatment were primarily attributed to the effect of the implant. Bone mineral density has been used as a method of grouping orthopedic specimens and can influence results of biomechanical studies that use vertebral column specimens from humans.15–17 The bone mineral density was comparable among the specimens of the present study, thus reducing the influence of this variable on the results.
The load-deformation curves were similar in shape for unaltered and treated specimens and had 2 distinct regions. The slope was smaller in the first region (< 10° of angular deformation), which indicated that incremental increases in bending moment caused relatively large increases in angular deformation (ie, low-load, high-deformation change). The second region of the load-deformation curve (> 12° of angular deformation) had an exponential association between bending moment and angular deformation: as angular deformation increased, there were progressively larger changes in bending moment. This phenomenon has been reported in other studies5,7,13 of the vertebral column of canids. The most likely explanation for this in the unaltered specimens was that the supportive ligamentous structures (ligamenta flava, ligamenta interspinalia, synovial joint capsules, annuli fibrosus, and ligamentum longitudinale dorsale) were lax when the specimen was in a neutral position. However, when the angular deformation increased, the ligaments became taut, which increased the resistance to a bending moment. In the treated specimens, bending moment was likely transferred to the implant at the intervertebral disk space between C4 and C5 instead of to the ligamentous structures. Implant rigidity diminished angular deformation of the VMU of C4 and C5 but likely increased it at adjacent sites. Values of angular deformation for each individual VMU would be required to quantify the changes in angular deformation for any given VMU within the specimen. The load-deformation curves of the treated specimens, compared with curves for the unaltered specimens, indicated that a larger bending moment was needed for each degree of angular deformation. This was more apparent when angular deformation was > 12°.
Stiffness is measured by calculating the slope of the load-deformation curve and is used to evaluate a structure's resistance to bending.18 Stiffness has been used to evaluate cervical vertebrae implants.7 Stiffness relative to dorsal bending was used to determine the effect of treatment within specimens and between treatment groups.7,15 There were significant differences in stiffness between unaltered and subsequently implanted specimens at all intervals evaluated. Therefore, both implants altered biomechanics of the cervical specimen by causing the specimens to be more resistant to dorsal bending. Restricting motion at the intervertebral disk space between C4 and C5 did not change the overall shape of the load-deformation curve, but it did shift the curve in an upward direction.
Evaluation of screw or pin placement revealed significantly less penetration of the transverse foramen or vertebral canal in the novel screw-bar–PMMA implant group, compared with penetration in the traditional pin-PMMA implant group (Figure 4). In a clinical setting, penetration of the transverse foramen or vertebral canal could lead to iatrogenic vertebral artery or spinal cord damage, respectively, with a subsequent increase in morbidity or death. However, because the present study involved the use of cadavers, the actual clinical effects of pin or screw placement could not be assessed.
Evidence of bone fracture was not detected at any of the interfaces between the implanted pins or screws and the bone. Undoubtedly, skeletal maturity and vertebrae size may influence whether the transverse process would fail in certain conditions in which the novel screw-bar–PMMA implant would be used. Further biomechanical evaluation should be conducted in which specimens from dogs of a variety of ages and weights are used.
The only catastrophic implant failure detected was in the traditional pin-PMMA implant group. Failure occurred during bending and was characterized by complete breakage of the PMMA midway between the pins in a transverse plane. Inadequate mixing, air entrapment, or insufficient curing of the PMMA has been reported19 to decrease PMMA strength. The PMMA used in the study was mixed and applied by use of a standard protocol; however, vacuum mixing was not used. It is possible that a defect in the PMMA caused the premature failure during testing. The horizontal bar wired to the screw heads in the novel screw-bar–PMMA implant likely increased PMMA stiffness, which allowed the PMMA to resist higher bending moments prior to failure. To quantify the effect of the reinforcing bar, the stiffness of PMMA aliquots with dimensions similar to those used in the present study with and without a horizontal reinforcing bar would need to be evaluated.
Extrapolation of this biomechanical information to an in vivo setting should be done with caution because the active stabilizing components of the vertebral column (muscle and muscle-tendon units) were not evaluated. Additionally, formation of postoperative fibrous tissue and osseous remodeling contributes to the overall biomechanical properties of cervical vertebrae, but these processes cannot be evaluated in an in vitro study.20 Currently, there is not an established target value for postoperative VMU stiffness in dogs. Procedures that allow too much or too little motion may be detrimental to the desired outcome. Likely, there is an optimal stiffness at which motion is reduced without being totally eliminated, which would thereby promote osseous remodeling and fusion. Furthermore, optimal vertebral biomechanics may be different for various cervical problems. Therefore, although each of the tested implants in the study reported here had similar alterations in vertebral biomechanics, this does not necessarily suggest that this effect would be advantageous clinically.
The novel screw-bar–PMMA implant design described here has been used clinically by one of the authors (RSB) to stabilize various VMUs of dogs affected with a variety of instabilities of the cervical region of the vertebral column. On the basis of in vitro biomechanical data, a controlled clinical trial to assess other variables that cannot be evaluated in an in vitro experiment would be important to determine the overall use of such an implant for treating dogs with clinical signs attributable to cervical vertebral instability.
ABBREVIATIONS
CI | Confidence interval |
EMD | Estimated mean difference |
PMMA | Polymethylmethacrylate |
VMU | Vertebral motion unit |
QDR 4500 acclaim series Elite, Hologic Inc, Bedford, Mass.
Instron, model 1350, Instron Industrial Products, Grove City, Pa.
Ortho-Jet, Lang Dental Manufacturing Co Inc, Wheeling, Ill.
Instron load cell, Instron Industrial Products, Grove City, Pa.
LabView Software, National Instruments Corp, Austin, Tex.
Surgical Simplex P, Styker Haowmedica Osteonics, Mahwah, NJ.
Dermestid Beetles (Dermestes frishii), Carolina Biological Supply, Burlington, NC.
PROC MIXED, SAS, version 9.1, SAS Institute Inc, Cary, NC.
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