Radiographic evaluation of perching-joint angles in cockatiels (Nymphicus hollandicus), Hispaniolan Amazon parrots (Amazona ventralis), and barred owls (Strix varia).
Article Type: Report
Subject: Birds (Physiological aspects)
Birds (Research)
Radiography (Usage)
Joints (Physiological aspects)
Joints (Research)
Authors: Bonin, Glen
Lauer, Susanne K.
Guzman, David Sanchez-Migallon
Nevarez, Javier
Tully, Thomas N., Jr.
Hosgood, Giselle
Gaschen, Lorrie
Pub Date: 06/01/2009
Publication: Name: Journal of Avian Medicine and Surgery Publisher: Association of Avian Veterinarians Audience: Academic Format: Magazine/Journal Subject: Health Copyright: COPYRIGHT 2009 Association of Avian Veterinarians ISSN: 1082-6742
Issue: Date: June, 2009 Source Volume: 23 Source Issue: 2
Topic: Event Code: 310 Science & research
Geographic: Geographic Scope: United States Geographic Code: 1USA United States
Accession Number: 252006948
Full Text: Abstract: Information on perching-joint angles in birds is limited. Joint immobilization in a physiologic perching angle has the potential to result more often in complete restoration of limb function. We evaluated perching-joint angles in 10 healthy cockatiels (Nymphicus hollandicus), 10 Hispaniolan Amazons (Amazona ventralis), and 9 barred owls (Strix varia) and determined intra- and interobserver variability for goniometric measurements in 2 different radiographic projections. Intra- and interobserver variation was less than 7% for all stifle and intertarsal joint measurements but frequently exceeded 10% for the hip-joint measurements. Hip, stifle, and intertarsal perching angles differed significantly among cockatiels, Hispaniolan Amazon parrots, and barred owls. The accuracy of measurements performed on straight lateral radiographic projections with superimposed limbs was not consistently superior to measurements on oblique projections with a slightly rotated pelvis. Stifle and intertarsal joint angles can be measured on radiographs by different observers with acceptable variability, but intra- and interobserver variability for hip-joint-angle measurements is higher.

Key words: joint angle, radiography, avian, cockatiels (Nymphicus hollandicus), Hispaniolan Amazon parrots (Amazona ventralis), barred owls (Strix varia)

Introduction

Over the last 2 decades, avian orthopedics has advanced to the point that, in avian practice today, osteosynthesis and joint surgery are frequently performed with state-of-the-art instrumentation and implants. Despite differences in cortical bone thickness, soft-tissue coverage, behavior, and biomechanics, (1,2) the basic principles of fracture stabilization and joint repair are often extrapolated from canine, feline, and human medicine to birds. (3-8) External coaptation, arthrodesis, and transarticular external skeletal fixation result in temporary or permanent immobilization of joints. In quadrupedal small mammals, joints are immobilized in a neutral standing angle to optimize limb function and to minimize adverse effects on ipsilateral and contralateral joints. (9-14) A joint immobilized in an overextended angle will force the animal to circumduct the limb during gait and result in disuse or abnormal locomotion. (9) A joint immobilized in an excessively flexed angle will cause functional shortening of the limb. Thus, weight bearing might be prohibited, and the mechanical load and propulsive and breaking forces on the other limbs are altered. (9,15) In bipedal species such as birds, the detrimental effect of joint immobilization at inappropriate angles might be more pronounced than in quadrupedal mammals, because only one other limb exists to compensate. In birds, uneven weight bearing is a predisposing factor for pododermatitis, which can be serious enough to warrant euthanasia. (2,16-18)

In canine orthopedics, flexion and extension angles of the fore- and hindlimb joints were determined in standing dogs based on radiographic, electrogoniometric, and manual goniometric measurements. (9,10,19-23) However, joint angles can vary in dogs with similar conformation. (9) Standing joint angles can be affected by breed, body-condition score, performance, and husbandry conditions. In dogs and cats undergoing arthrodesis, manual goniometric or radiographic measurement of joint angles in the unaffected limb has been recommended to sustain fusion angles when the animal is nonweight-bearing on the affected leg. (9) Metacarpophalangeal and metatarsophalangeal joint angles of dogs are influenced by the degree of weight bearing on the limb, while the proximal joint angles of the same leg are not altered. (9) Information on perching-joint angles in birds is limited. (24) Measurements of joint angles in quadrupedal species cannot be directly extrapolated to avian species because of class-specific anatomy, biomechanics, and gait. Scientifically derived information regarding perching angles of the avian leg is needed to immobilize joints at the appropriate angle.

In this study, we evaluated perching-joint angles in healthy cockatiels (Nymphicus hollandicus), Hispaniolan Amazon parrots (Amazona ventralis), and barred owls (Strix varia) and determined intra- and interobserver variability for goniometric measurements on 2 different radiographic views. We hypothesized 1) that perching-joint angles can be measured from straight lateral and oblique radiographic projections with intra- and interobserver variation of less than 10%, and 2) that perching-joint angles would differ between species.

Materials and Methods

Birds

Ten healthy adult cockatiels, 10 Hispaniolan Amazon parrots, and 9 barred owls were evaluated. The cockatiels and Hispaniolan Amazon parrots were selected from research colonies maintained at the institutional laboratory animal facilities. The cockatiels and Amazon parrots used in this investigation ranged in age from 8 to 10 years and from 2 to 3 years, respectively. Cockatiels and Amazon parrots were housed in separate areas. Groups of birds were maintained in stainless-steel primate cages that contained multiple plastic perches and washable cage toys. The owls were housed in stainless-steel cages (2 ft x 3 ft x 3 ft), with a newspaper substrate and a stump for perching. Three to four cockatiels were housed together, and Amazon parrots were housed in pairs. The owls were housed individually. The barred owls were selected from birds being treated for various nonorthopedic health reasons at the Wildlife Hospital of Louisiana. Only birds with no previous history of pelvic orthopedic injury and no musculoskeletal abnormalities evident on physical examination were included in the study. The body-condition score of each bird was determined. (25) All birds were housed and maintained according to an approved protocol by the Institutional Animal Care and Use Committee. The experimental protocol was approved by the Institutional Animal Care and Use Committee.

Radiographs

Each bird was positioned in a custom-built, wooden box (71.1 cm high x 45.7 cm wide x 40.6 cm deep) (Fig 1). The diameter of the perching stick was standardized for cockatiels at 1.6 cm, for Hispaniolan Amazon parrots at 2.2 cm, and for barred owls at 2.9 cm. After an acclimatization period of 10 minutes in darkness, lateral horizontal-beam radiographs of both pelvic extremities were performed with a digital radiographic imaging unit (model EDR5-MAF, Eklin Medical Systems Inc, Sunnyvale, CA, USA). The birds perched in either direction. The radiographic beam was centered at the level of the heart and included both pelvic limbs extending from the pelvis to the distal phalanx. If the bird switched the perching direction during the trial, the beam position was not adapted to avoid stress and subsequent alteration in perching. The source-to-image distance was 121.9 cm for all birds. Three views with the pelvic limbs in a left-to-right or right-to-left lateral projection, and 3 views with the pelvic limbs in a left-to-right or right-to-left oblique-projection position were used for radiographic measurements of the hip-, stifle-, and intertarsal-joint angles (Fig 2).

On left-to-right and right-to-left lateral views, the pelvic limbs were superimposed. On oblique views, the birds perched with the pelvic limbs in an asymmetric position, such that 1 limb was cranial to the opposite, and the pelvis was slightly tilted. Thus, the joint angles differed between both pelvic limbs. The x-ray beam was maintained in the same angle and position as for the lateral views, and an approximately 10[degrees] obliquity in the craniocaudal and ventrodorsal direction resulted from the bird's stance on the perching stick (Fig 2).

Measurements

The limbs were determined to be cranially or caudally positioned on the radiographs, based on the position of the cranial cnemial crest of the tibial tuberosity. The limb with the most cranially positioned cranial cnemial crest of the tibial tuberosity was defined as the cranial limb, and the limb with the more caudally positioned cranial cnemial crest of the tibial tuberosity was defined as the caudal limb. The joint angles were measured independently by 3 different observers (D.G., G.B., S.L.) for the cranial limb on the lateral and oblique projections and for the caudal limb on the oblique projections. The angles were determined based on specific anatomic landmarks (Figs 3 and 4) by using the line-and-angle tool of digital imaging software (VetPACS, Version 3.5.10, Sound Technologies, Inc, Carlsbad, CA, USA).

[FIGURE 1 OMITTED]

* The hip-joint angle was measured as the angle formed by the line extending through the ventral margin of the synsacrum ventral to the acetabulum and the long axis of the femur (the line through the center of femoral diaphysis at the subtrochanteric level and the center of the lateral femoral condyle).

* The stifle-joint angle was measured as the angle formed by the long axis of the femur (the line through the center of femoral diaphysis at the subtrochanteric level and the center of the lateral femoral condyle) and the long axis of the tibiotarsal shaft (the line through the center of the tibial plateau and the tibiotarsal condyle).

* The intertarsal-joint angle was measured as the angle formed by the long axis of the tibiotarsal shaft (the line through the center of the tibial plateau and the tibiotarsal condyle) and the long axis of the most cranial tarsometatarsus (for cockatiels and Hispaniolan Amazon parrots, the line through the center of the tarsometatarsal base and the center of the tarsometatarsal condyle; for barred owls, the line through the center of the tarsometatarsal base and the center of the tarsometatarsal diaphysis at the middiaphyseal level).

[FIGURE 2 OMITTED]

Each observer measured each joint angle once on each of the 3 lateral projections and the 3 oblique projections. Then, each observer repeated the measurements 3 times on 1 lateral and 1 oblique view to determine intra-observer variability. At least 54 different radiographic views were evaluated by each observer before the joint measurements were repeated.

Statistical evaluation

All response data were considered continuous and found to follow a normal distribution by failure to reject the null hypothesis of normality by using the Shapiro-Wilk statistic at P [less than or equal to] .05. All joint-angle data were summarized as mean (SD) and coefficient of variation (CV), where CV = (SD/mean)%. A mean CV was calculated by using the individual CVs for each joint measured for each specific leg on the views. A 2-way analysis of variance was performed to evaluate the effect of species for each joint angle. Significant effects were determined at P < .05. Ad hoc comparisons were performed by using the Scheffe procedure to maintain a type I error at .05 (Proc ANOVA, Proc Univariate, SAS version 9.1 SAS Institute, Cary, NC, USA).

Results

Animals

All birds had a body-condition score of 3 to 3.5. Although some birds were initially agitated when placed in the box, all birds calmed within the acclimatization period.

Mean intra-observer variability

The mean intra-observer variability is shown in Table 1. In all species, intra-observer variability was highest for joint angle measurements of the hip joint. Intra-observer CV ranged from 3.5% to 9.2% for hip joint, from 1.2% to 4.0% for stifle joint, and from 2.2% to 4.1% for intertarsal-joint measurements. Intra-observer variance was inconsistent across species, joints, and radiographic views.

Mean interobserver variability

The mean interobserver variability is shown in Table 2. In all species, interobserver variability was highest for joint-angle measurements of the hip joint. Interobserver CV ranged from 6.5% to 16% for hip-joint, from 2.7% to 6.5% for stifle-joint, and from 3.9% to 8.1% for intertarsal-joint measurements. Interobserver variance was inconsistent across species, joints, and radiographic views.

[FIGURE 3 OMITTED]

Joint angles

Joint angles are shown in Table 3.

Hip joint: The mean hip-joint angle ranged from 28.2[degrees] to 39.7[degrees] over all views. On the lateral projection (cranial leg), the hip-joint angle of Hispaniolan Amazon parrots was significantly smaller than that of barred owls or cockatiels. On the oblique projection (cranial leg), the hip-joint angle of Hispaniolan Amazon parrots was significantly smaller than that of barred owls. On the oblique projection (caudal leg), there was no significant difference between the hip-joint angles of the different species.

Stifle joint: The mean stifle-joint angle ranged from 32.9[degrees] to 69.5[degrees] over all projections. On the lateral projection (cranial leg), the stifle-joint angle of barred owls was significantly smaller than that of Hispaniolan Amazon parrots or cockatiels. On the oblique view (cranial and caudal leg), the stifle-joint angle of barred owls was significantly smaller than the stifle-joint angle of Hispaniolan Amazon parrots and cockatiels and the stifle-joint angle of cockatiels was significantly smaller than the stifle angle of Hispaniolan Amazon parrots.

Intertarsal joint: The mean intertarsal-joint angle ranged from 52.4[degrees] to 101.8[degrees] over all projections. On each projection or leg, the intertarsaljoint angle of cockatiels was significantly smaller than that of Hispaniolan Amazon parrots or barred owls. The intertarsal-joint angle of Hispaniolan Amazon parrots was significantly smaller than the intertarsal-joint angle of barred owls.

Discussion

As expected, perching-joint angles differed significantly among the 3 species. Intra- and interobserver variation was less than 7% for all stifle- and intertarsal-joint measurements but frequently exceeded 10% for the hip-joint measurements. Consistency of measurements performed on straight lateral radiographic projections with superimposed limbs was not consistently superior to measurements on oblique projections with a slightly tilted pelvis. Therefore, our hypothesis that perching-joint angles would differ between species was supported. However, our results only partially supported the hypothesis that perching-joint angles can be measured from lateral radiographs with intra- and interobserver variations of less than 10%.

[FIGURE 4 OMITTED]

We measured perching-joint angles by using radiography, because manual goniometric measurements cannot be performed in small birds. Although joint measurements with a standard goniometer can be performed with adequate accuracy in dogs positioned in lateral recumbency, (26) this technique is not applicable in smaller birds because of the size of the instrument. Moreover, this technique requires handling that would stress the bird and consequently alter perching position of the leg when being measured.

In our study, the inter- and intra-observer CV for the stifle and intertarsal joints was higher than 5%. The precision of a technique is inversely related to the CV between measurements, and a CV of less than 5% is generally considered satisfactory for consistency. Inter- and intraobserver variability for the stifle and intertarsal joints in our study is within the range of studies that evaluated consistency of radiographic measurements of tibial-plateau angles used for preoperative planning of osteotomies in dogs. (27-29) In these studies, intra-observer variability was 3.4[degrees]

for angles that ranged from 17[degrees] to 30[degrees], (27) whereas interobserver variability ranged from 1.5[degrees] to 4.8[degrees] for angles that ranged from 17[degrees] to 320. (27-29) An ideal goniometric measurement technique for perching birds would allow precise measurement of joint angles that are reproducible by different observers at any point in time. As expected, interobserver variability was higher than intraobserver variability, reflecting that perching-joint angles measured by different observers are more variable than measurements performed by the same observer.

In our study, intra- and interobserver variation was higher for the hip-joint measurements, when compared with stifle- and intertarsal-joint measurements. Variability was lowest for hip-joint measurements in cockatiels when using the cranial leg. The ventral margin of the synsacrum was the only anatomic landmark that could be consistently identified on the radiographs of all 3 species. Nevertheless, all 3 observers perceived the synsacrum as difficult to identify for the hip-joint measurements. Visualization of the ventral margin of the synsacrum was more difficult in Amazon parrots and barred owls and was particularly challenging on oblique projections when the pelvis was rotated. This might explain the high variability observed for hip-joint-angle measurements in all 3 species.

In our study, intra- and interobserver variability was not consistently lower for measurements on straight lateral radiographic projections compared with oblique projections. Lateral projections were often more difficult to obtain than oblique projections. However, because deviation from true lateral radiographic projections can result in erroneous measurement of limb alignment in people and dogs, lateral projections were judged best for assessing joint angles. (29-31) The effect of obliquity of radiographic views on measurement of flexion- and extension-joint angles has not been reported. Nevertheless, we suspect that goniometric measurements performed on straight lateral views have a higher potential to reflect true anatomic extension and flexion angles than oblique views. Furthermore, although joint angles on lateral views with superimposed limbs provide information on mean perching-joint angles that allow even weight distribution, oblique views reflect more extreme joint angles observed during perching.

Clinical use of perching-joint angles

We measured hip-joint angles because they might alter subsequent to orthopedic treatment or husbandry conditions and, therefore, are important to investigate. For goniometric studies on hip-joint angles in birds, measurements should be performed by the same observer when considering the high variability observed in our study. From an orthopedic point of view, hip-joint perching angles are rarely measured because hip joints are rarely immobilized.

Because birds commonly sustain musculoskeletal injuries to the lower pelvic limb, stifle and intertarsal perching-joint angles as evaluated in our study are important for clinicians. Thus, stifle and intertarsal joints are commonly immobilized when injuries are treated with external coaptation, temporary transarticular external skeletal fixation, or arthrodesis. (32-37) Joint immobilization in a physiologic perching angle may result more often in complete restoration of limb function, might allow an earlier return to normal function, and may decrease morbidity. Perching-joint angles on straight lateral views can be used as a guideline for external coaptation or for presurgical planning. If postoperative radiographs reflect immobilization with a suboptimal joint angle, then minimal and maximal joint angles measured from oblique views can be used to guide a decision as to whether or not the fixation should be revised.

Perching-joint angles varied between birds of the same species. Thus, the radiographic perching-joint angles observed in our study can only be used as guidelines to approximate joint angles before surgery. However, radiographic evaluation of perching-joint angles in an injured bird itself is often impossible because of the inability to perch and the excessive stress. Furthermore, similar to standing-joint angles in dogs, (9) perching angles in injured birds might be altered when they are monopedal and painful.

Our study had several limitations. The cockatiels and Hispaniolan Amazon parrots used for the measurements in our study originated from research colonies, whereas the barred owls were rescued birds from a wildlife rehabilitation hospital. Although the results of our study can be extrapolated to individual birds of the same species, differences in husbandry, exercise regimen, and degree of stress during the radiographic procedure must be taken into account. In our study, joint-angle measurements were performed by using predetermined anatomic landmarks on

digital radiographs. Similar measurements on printed radiographs might be less accurate, when considering a recent study that compared tibial-plateau slope measurements on digital radiographs with measurements on printed radiographs in dogs. (28)

We standardized x-ray beam position, because the beam position in relation to the limb has been shown to affect tibial-plateau angle measurements in some instances. (28,29) Nevertheless, during our study, few birds switched perching direction on the perching stick. Thus, craniocaudal beam position in relation to the heart changed between views. We did not correct an altered beam position in these birds to avoid stress and a subsequent change in perching. However, we evaluated the effect of an altered beam position in a pilot study on joint angle measurements in a chicken skeleton. Alteration of the x-ray beam by a 5-cm distance in cranial, caudal, dorsal, and ventral directions did not affect our measurements.

Our results indicate that hip-, stifle-, and intertarsal-joint angles differ between cockatiels, Hispaniolan Amazon parrots, and barred owls. Stifle- and intertarsal-joint angles can be measured on radiographs by different observers with acceptable variability, but intra- and interobserver variability for hip-joint angle measurements is high. The radiographic perching-joint angles observed in this study can be used as a guideline to approximate joint angles in these species.

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Glen Bonin, DVM, Susanne K. Lauer, Dr med vet, Dipl ACVS, Dipl ECVS, David Sanchez-Migallon Guzman, Lic en Vet, MS, Javier Nevarez, DVM, PhD, Thomas N. Tully, Jr, DVM, MS, Dipl ABVP (Avian), Dipl ECAMS, Giselle Hosgood, BVSc, PhD, Dipl ACVS, and Lorrie Gaschen, DVM, Dr med vet, PhD, Dipl ECVDI

From the Department of Veterinary Clinical Sciences, School of Veterinary Medicine, Louisiana State University, Baton Rouge, LA 70803, USA.
Table 1. Intra-observer variation: the mean coefficient
of variation (%) for 3 observers who performed
goniometric measurements of the hip, stifle, and
intertarsal joints in cockatiels, Hispaniolan Amazon
parrots, and barred owls.

                            Radiographic projection (leg)

                              Lateral     Oblique    Oblique
Joint angle   Species        (cranial)   (cranial)   (caudal)

Hip           Amazons           8.9         5.8        6.4
              Barred owls       6.0         9.2        9.1
              Cockatiels        3.5         4.2        7.4
Stifle        Amazons           3.0         1.2        1.4
              Barred owls       4.0         3.5        2.1
              Cockatiels        1.8         1.5        2.0
Intertarsal   Amazons           3.8         2.5        2.2
              Barred owls       2.2         2.9        4.1
              Cockatiels        2.9         4.1        2.8

Table 2. Interobserver variation: the mean coefficient of
variation (%) for 3 observers who performed
goniometric measurements of the hip, stifle, and
intertarsal joints in cockatiels, Hispaniolan Amazon
parrots, and barred owls.
                            Radiographic projection (leg)

                            Lateral     Oblique    Oblique
Joint angle   Species       cranial)   (cranial)   (caudal)

Hip           Amazons        11.0        11.7       12.1
              Barred owls     7.8        13.8       16.0
              Cockatiels      6.9         6.5       11.4
Stifle        Amazons         5.7         3.5        3.5
              Barred owls     6.5         5.4        3.9
              Cockatiels      3.1         2.7        4.6
Intertarsal   Amazons         5.4         5.2        4.8
              Barred owls     6.5         5.5        8.1
              Cockatiels      3.9         5.5        4.2

Table 3. Mean (SD) hip-, stifle-, and intertarsal-joint angles
([degrees]) in cockatiels, Hispaniolan Amazon parrots, and
barred owls.

                            Radiographic projection
                            (leg) (mean [+ or -] SD)

Joint angle   Species         Lateral (cranial)

Hip           Amazons       28.2 [+ or -] 8.9 (a)
              Barred owls   33.7 [+ or -] 8.8 (b)
              Cockatiels    34.8 [+ or -] 7.6 (b)
Stifle        Amazons       56.8 [+ or -] 8.4 (c)
              Barred owls   34.3 [+ or -] 8.9 (d)
              Cockatiels    56.8 [+ or -] 7.9 (e)
Intertarsal   Amazons       68.8 [+ or -] 14.6 (f)
              Barred owls   90.0 [+ or -] 18.1 (g)
              Cockatiels    55.9 [+ or -] 14.l (h)

                            Radiographic projection
                            (leg) (mean [+ or -] SD)

Joint angle   Species          Oblique (cranial)

Hip           Amazons       35.7 [+ or -] 11.6 (a)
              Barred owls   39.7 [+ or -] 9.0 (b)
              Cockatiels    37.4 [+ or -] 6.7 (a,b)
Stifle        Amazons       54.8 [+ or -] 8.8 (c)
              Barred owls   32.9 [+ or -] 7.3 (d)
              Cockatiels    52.5 [+ or -] 5.5 (e)
Intertarsal   Amazons       65.8 [+ or -] 13.0 (f)
              Barred owls   93.6 [+ or -] 14.3 (g)
              Cockatiels    52.4 [+ or -] 8.l (h)

                            Radiographic projection
                            (leg) (mean [+ or -] SD)

Joint angle   Species           Oblique (caudal)

Hip           Amazons        33.8 [+ or -] 11.4 (a)
              Barred owls    36.1 [+ or -] 16.3 (a)
              Cockatiels     33.3 [+ or -] 9.0 (a)
Stifle        Amazons        69.5 [+ or -] 12.2 (c)
              Barred owls    41.5 [+ or -] 8.7 (d)
              Cockatiels     60.5 [+ or -] 8.5 (e)
Intertarsal   Amazons        80.4 [+ or -] 14.0 (f)
              Barred owls   101.8 [+ or -] 22.5 (g)
              Cockatiels     64.2 [+ or -] 8.0 (h)

(a,b) Mean hip joint angles with different superscripts
were significantly different within column (P < .05).

(c-c) Mean stifle joint angles with different superscripts
were significantly different within column (P < .05).

(f-h) Mean intertarsal joint angles with different
superscripts were significantly different within column
(P < .05).
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