Syndactyly is a congenital anomaly that may compromise the hoof, skin, fibrous tissue, or bone, depending on the affected species.1–6 The defect has been described in humans3 and cattle4,6 and, less frequently, in sheep,1 dogs,2 cats,2,5 and pigs.7 In cloven-hoofed animals, the condition is also known as mulefoot because affected animals have fused or uncloven hooves that resemble the feet of a mule.4,7 The condition may occur as a sporadic malformation with no previous family history of the disorder, or it may occur as a genetic disorder.1,2,4
In swine, the Mulefoot breed is characterized by an uncloven hoof, although this breed is in a critical state according to the World Watch List for Domestic Animal Diversity.8,9 Few reports of the condition in other swine breeds exist,10,11 although the condition may persist in an entire population or breeding group.7 A single dominant gene has been linked to this condition in pigs,12 and researchers have induced congenital malformations of nutritional origin, including syndactylia, paralysis agitans, and talipes,13 which suggests that the condition may have diverse manifestations.7
Partial or complete fusion of the digits may occur in 1 or more limbs.6 However, dissection records, which indicate that the forelimbs are the most affected region, as well as results of radiography suggest that such fusion in pigs may have great diversity.7,10,14 Furthermore, there is controversy about the influence of syndactyly on locomotion. Some investigators have reported that affected animals tend to have fewer locomotion-associated problems, whereas other investigators have reported a restricted gait.7
Use of a pressure-sensing walkway as an objective method for gait analysis has facilitated studies15–18 of animal locomotion. The advantages of this method include evaluation of consecutive and simultaneous footfalls to reduce the labor and time required to complete data collection.17,19 These advantages are especially important for animals that may be problematic to handle, such as pigs.17,18,20
Syndactyly apparently is an uncommon problem in pigs that may induce health problems, presumably as a result of impaired gait; it may also pose a welfare issue. Therefore, the purpose of the study reported here was to characterize a population of pigs with naturally occurring syndactyly by use of plain radiographs and CT images and to evaluate kinetic and temporospatial variables by use of a pressure-sensing walkway. The main hypothesis was that syndactyly would not cause kinetic alterations or affect temporospatial variables.
Materials and Methods
Animals
Ten sexually intact Brazilian minipigs between 6 and 8 months of age were obtained from the Centre for Wildlife Medicine and Research. The pigs were littermates, but additional information about the parents or genetic lineage was not available. Group 1 consisted of 5 healthy animals (2 males and 3 females; body weight, 10.5 to 18.5 kg); these pigs were considered healthy on the basis of results of a complete physical and orthopedic evaluation. Group 2 consisted of 5 animals with syndactyly (3 males and 2 females; body weight, 7.5 to 18.0 kg). All pigs of a group were housed together in 1 pen. The reason young growing pigs were chosen for use in the study was the ease of handling and availability of a sufficient number of animals of this age. The study was approved by the Ethics Committee of the Universidade Estadual Paulista School of Veterinary Medicine and Animal Science.
Experimental procedures
Radiographic and CT images of the forelimbs and hind limbs were obtained for all pigs. Additionally, visual gait analysis21 as well as gait analysis by use of a pressure-sensing walkway were performed for both groups. For each animal, both gait analyses were conducted on the same day by 2 of the authors (PLTJ and FSA).
Radiographic and CT imaging
Pigs were anesthetized by IM administration of acepromazine maleate (0.3 mg/kg), midazolam (0.3 mg/kg), and ketamine hydrochloride (15 mg/kg). When necessary, additional anesthetic was administered at one-fourth of the initial dose. An electric blanket was used to keep anesthetized pigs warm. Pigs received oxygen through a mask during the procedures. Heart and respiratory rates and rectal temperature were constantly monitored.
Lateromedial and dorsopalmar (or dorsoplantar) radiographic images were obtained of all limbs at locations immediately distal to the radius and tibia. Images were obtained by use of a digital radiographic system.3 Specifically, a focal film distance of 100 cm was used with settings of 60 to 90 kV, 200 mA, and 8 mAs. Images were evaluated qualitatively by an experienced veterinary radiologist to determine size, shape, number, and position of the bones; congruence; and appearance of joints and articular surfaces. Relationships between bone structures affected by syndactyly as well as other radiographic features were also assessed.
Computed tomographic images were obtained by use of a spiral scanner.b Pigs were placed in dorsal recumbency in a padded v-shaped trough; cranial traction was placed on the forelimbs, and caudal traction was placed on the hind limbs. Transverse images were obtained immediately distal to the radius and tibia. Settings for the images were 120 kVp, 160 mA, 2.0-mm-thick slices, pitch of 2.0, and rotation of 2 seconds. Images were reconstructed by use of 3-D medical imaging software.c
Gait analysis
Data for kinetic and temporospatial variables were obtained by use of a pressure-sensing walkwayd (1.951 × 0.447 m), which was equilibrated and calibrated in accordance with the manufacturer's specifications. Data were analyzed by use of walkway software.e
Pigs were allowed to acclimatize to the room and stimulated to move across the walkway for approximately 20 minutes prior to data collection. Immediately before data collection, each pig was weighed on an electronic scale. During each trial, boards were placed on each side of the walkway, and feed was used to encourage pigs to move across the pressure-sensing walkway at a comfortable speed without a handler. Approximately 20 trials were obtained for each pig, and the first 5 valid trials were selected for data analysis. A trial was considered valid when a pig moved in a straight line across the pressure-sensing walkway with acceleration between −0.20 and 0.20 m/s2. Acceleration was determined automatically by the pressure-sensing walkway.
Temporospatial variables analyzed for each limb were gait cycle time, stance time, swing time, and stride length. Approximately 3 footfalls/limb were collected for each trial, and the walkway software automatically calculated mean values for each limb. Stance time percentage was determined by use of the following equation: (stance time/gait cycle time) × 100. Swing time percentage was determined by use of the following equation: (swing time/gait cycle time) × 100. Stride length corresponded to the distance between 2 consecutive walkway contacts of the same limb. Kinetic variables evaluated were PVF and VI; these variables were normalized on the basis of each pig's body weight. Percentage of body distribution among the 4 limbs was calculated by use of the following equation: (PVF of a limb/total PVF of the 4 limbs) × 100.
SI
The SI between the right and left sides for both forelimbs and hind limbs was calculated for all kinetic and temporospatial variables by use of the following equation: SI (%) = ([X1 – X2]/[0.5 × {X1 + X2}]) × 100, where X1 and X2 correspond to the right and left sides, respectively. An SI value of 0 indicated total symmetry between the 2 sides, and values > 0 represented the percentage of asymmetry.
Statistical analysis
All variables were evaluated for normality by use of the Shapiro-Wilk test. Values were expressed as mean ± SD. Comparisons between groups were performed by use of the F test followed by the Student t test. Differences were considered significant at P < 0.05.
Results
Animals
Pigs with syndactyly did not have signs of lameness. Also, pigs with syndactyly did not have a high-stepping gait.
Radiographic and CT evaluation
Evaluation of radiographs of the healthy pigs (group 1) revealed congruent joints, preservation of articular spaces, and unaltered articular surfaces. There was no radiographic evidence of bone proliferation, cortical irregularity, or changes of the cortical bone or medullary canal. Most of the growth plates were still not closed. Radiographic features were consistent with reconstructed 3-D CT images of the bones. All pigs had 8 carpal bones (proximal row: radial, intermediate, ulnar, and accessory carpal bones; distal row: first, second, third, and fourth carpal bones), 4 metacarpal bones, 4 digits (II, III, IV, and V), and 3 phalanges for each digit (Figure 1). Digits III and IV had 2 proximal sesamoid bones and 1 distal sesamoid bone, whereas digits II and V had only 2 proximal sesamoid bones. The tarsus was composed of 7 bones (proximal row: talus and calcaneus; middle row: central tarsal bone; and distal row: first, second, third, and fourth tarsal bones). There were 4 metatarsal bones, 4 digits (II, III, IV, and V), and 3 phalanges for each digit (Figure 2).
Dorsopalmar radiographic view (A) and dorsal (B) and palmar (C) views of a multiplanar 3-D CT reconstruction of the foot of the left forelimb of a healthy pig. 1 = Distal phalanx of digit III. 2 = Distal phalanx of digit IV. 3 = Middle phalanx of digit IV. 4 = Middle phalanx of digit III. 5 = Proximal phalanx of digit IV. 6 = Proximal phalanx of digit III. 7 = Phalanges of digit II. 8 = Phalanges of digit V. 9 = Metacarpal III. 10 = Metacarpal IV. 11 = Metacarpal V. 12 = Metacarpal II. 13 = Fourth carpal bone. 14 = Third carpal bone. 15 = Ulnar carpal bone. 16 = Second carpal bone. 17 = Radial carpal bone. 18 = Intermediate carpal bone. 19 = Radius. 20 = Head of the ulna.
Citation: American Journal of Veterinary Research 77, 9; 10.2460/ajvr.77.9.976
Dorsoplantar radiographic view (A) and dorsal (B) and plantar (C) views of a multiplanar 3-D CT reconstruction of the foot of the left hind limb of a healthy pig. 9 = Metatarsal III. 10 = Metatarsal IV. 11 = Metatarsal V. 12 = Metatarsal II. 13 = Fourth tarsal bone. 14 = Third tarsal bone 15 = Central tarsal bone. 16 = Calcaneus. 17 = Talus. 18 = Tibia. See Figure 1 for remainder of key.
Citation: American Journal of Veterinary Research 77, 9; 10.2460/ajvr.77.9.976
Radiographic and CT findings for the pigs with syndactyly (group 2) were used to classify the lesions by use of a classification system developed by the authors. Simple syndactyly was defined as the hoof being fused but without fusion of the bones (Figure 3). Complex-1 syndactyly was defined as the hoof being fused along with complete bony fusion of the distal phalanges of digits III and IV (Figure 4). Complex-2 syndactyly was defined as the hoof being fused along with complete bony fusion of both the middle and distal phalanges of digits III and IV (Figure 5).
Dorsoplantar radiographic view (A) and dorsal (B) and plantar (C) views of a multiplanar 3-D CT reconstruction of the foot of the left hind limb of a pig with simple syndactyly. In panel A, notice the radiopaque structures (arrows) located between the middle and distal phalanges of digits III and IV. See Figure 1 for remainder of key.
Citation: American Journal of Veterinary Research 77, 9; 10.2460/ajvr.77.9.976
Dorsopalmar radiographic view (A) and dorsal (B) and palmar (C) views of a multiplanar 3-D CT reconstruction of the foot of the left forelimb of a pig with complex-1 syndactyly. Notice the total fusion of the distal phalanges of digits III and IV. 1–2 = Fused distal phalanges. See Figure 1 for remainder of key.
Citation: American Journal of Veterinary Research 77, 9; 10.2460/ajvr.77.9.976
Dorsopalmar radiographic view (A) and dorsal view (B) of a multiplanar 3-D CT reconstruction of the foot of the left forelimb of a pig with complex-2 syndactyly and palmar view of a multiplanar 3-D CT reconstruction of the foot of the right forelimb of a pig with complex-2 syndactyly (C). Notice the total fusion of the middle and distal phalanges of digits III and IV. In panel C, notice the fusion of the distal sesamoid (arrow). 3–4 = Fused middle phalanges. See Figures 1 and 4 for remainder of key.
Citation: American Journal of Veterinary Research 77, 9; 10.2460/ajvr.77.9.976
By use of the aforementioned classification system, the type of syndactyly for each pig in group 2 was determined. One female pig had complex-2 syndactyly of both forelimbs and simple syndactyly of both hind limbs, whereas the other female pig had complex-2 syndactyly of all 4 limbs. One of the male pigs had complex-2 syndactyly of the right forelimb and hind limb and complex-1 syndactyly of the left forelimb and hind limb. Another of the male pigs had complex-2 syndactyly in all 4 limbs. The third male pig had complex-2 syndactyly of the right forelimb, complex-1 syndactyly of the left forelimb, and simple syndactyly in both of the hind limbs.
In pigs with simple syndactyly, 2 structures of the same bone radiopacity were also visible (one with a circular shape located between the middle phalanges of digits III and IV and the other with a triangular shape located between the distal phalanges of digits III and IV). Of the 3 limbs with complex-1 syndactyly, 2 had total fusion of the distal phalanges and 1 had partial fusion of the distal phalanges. Of the 13 limbs with complex-2 syndactyly, 6 had total fusion of the middle and distal phalanges and 7 had partial fusion of the middle phalanges and total fusion of the distal phalanges. In addition, fusion of the distal sesamoids of the forelimbs was detected in 1 pig.
Gait analysis
Mean ± SD velocity was 0.80 ± 0.14 m/s for the healthy pigs and 0.64 ± 0.08 m/s for the pigs with syndactyly. Mean velocity did not differ significantly (P = 0.069) between groups. On the basis that the duty factors (fraction of cycle duration when the limb maintains contact with the ground) of the hind limbs were > 0.5, pigs in both groups were deemed to be walking. Forelimbs and hind limbs of healthy pigs and pigs with syndactyly did not differ significantly with regard to any kinetic or temporospatial variable (Table 1). Similarly, the SI did not differ significantly between groups (Table 2).
Comparison of the temporospatial and kinetic variables for the forelimbs and hind limbs of 5 healthy pigs (group 1) and 5 pigs with syndactyly (group 2).
| Forelimbs | Hind limbs | |||||
|---|---|---|---|---|---|---|
| Variable | Group 1 | Group 2 | P value* | Group 1 | Group 2 | P value* |
| Stance time (s) | 0.35 ± 0.02 | 0.39 ± 0.05 | 0.06 | 0.34 ± 0.03 | 0.35 ± 0.02 | 0.51 |
| Swing time (s) | 0.25 ± 0.01 | 0.25 ± 0.02 | 0.29 | 0.28 ± 0.02 | 0.30 ± 0.03 | 0.23 |
| Gait cycle time (s) | 0.60 ± 0.04 | 0.64 ± 0.07 | 0.16 | 0.62 ± 0.03 | 0.65 ± 0.05 | 0.05 |
| Stride length (m) | 0.48 ± 0.03 | 0.46 ± 0.05 | 0.19 | 0.48 ± 0.03 | 0.45 ± 0.05 | 0.16 |
| Stance (%) | 58.33 ± 2.33 | 60.93 ± 4.01 | 0.14 | 54.83 ± 2.86 | 53.84 ± 3.07 | 0.13 |
| Swing (%) | 41.66 ± 2.49 | 39.07 ± 3.33 | 0.48 | 45.17 ± 3.95 | 46.16 ± 2.62 | 0.65 |
| PVF (%BW) | 46.07 ± 1.66 | 48.49 ± 4.57 | 0.13 | 35.64 ± 2.36 | 34.45 ± 4.69 | 0.48 |
| VI (%BW•s) | 11.98 ± 1.07 | 13.32 ± 2.45 | 0.14 | 8.00 ± 0.86 | 8.17 ± 0.87 | 0.67 |
| Body distribution (%) | 28.19 ± 0.94 | 29.26 ± 1.43 | 0.06 | 21.81 ± 1.43 | 20.74 ± 1.67 | 0.14 |
Values reported are mean ± SD.
Values were considered significant at P < 0.05.
%BW = Percentage of body weight.
Comparison of the SI of the temporospatial and kinetic variables for the forelimbs and hind limbs of 5 healthy pigs (group 1) and 5 pigs with syndactyly (group 2).
| Forelimbs | Hind limbs | |||||
|---|---|---|---|---|---|---|
| Variable | Group 1 | Group 2 | P value* | Group 1 | Group 2 | P value* |
| Stance time | 4.16 ± 2.10 | 5.49 ± 4.80 | 0.59 | 3.93 ± 2.47 | 5.61 ± 2.46 | 0.31 |
| Swing time | 6.16 ± 3.87 | 9.74 ± 8.79 | 0.43 | 7.61 ± 3.96 | 5.03 ± 5.58 | 0.42 |
| Gait cycle time | 4.00 ± 3.80 | 4.35 ± 3.66 | 0.89 | 3.29 ± 2.63 | 3.72 ± 5.63 | 0.88 |
| Stride length | 2.01 ± 0.99 | 0.95 ± 0.61 | 0.07 | 1.86 ± 1.69 | 3.49 ± 4.77 | 0.49 |
| Stance percentage | 4.46 ± 1.52 | 4.04 ± 4.27 | 0.84 | 2.47 ± 0.93 | 6.39 ± 4.02 | 0.09 |
| Swing percentage | 6.40 ± 5.75 | 7.05 ± 6.04 | 0.87 | 8.85 ± 4.10 | 8.05 ± 4.67 | 0.78 |
| PVF | 5.04 ± 3.11 | 1.89 ± 0.76 | 0.09 | 10.34 ± 6.92 | 5.26 ± 6.97 | 0.28 |
| VI | 4.67 ± 3.47 | 6.04 ± 3.26 | 0.54 | 7.43 ± 1.85 | 9.05 ± 8.04 | 0.67 |
| Body distribution | 5.04 ± 3.11 | 1.89 ± 0.76 | 0.09 | 10.34 ± 6.92 | 5.26 ± 6.97 | 0.28 |
Values reported are mean ± SD percentages.
See Table 1 for remainder of key.
The palmar surface and plantar surface of healthy pigs had 2 areas of maximum pressure. In contrast, pigs with syndactyly had only 1 area of maximum pressure (Figure 6).
Images of pressure plots obtained for the feet of the right (top row) and left (bottom row) limbs of a pig with syndactyly and a healthy pig without syndactyly. Notice that there is 1 area of maximum pressure on the palmar and plantar surfaces of the feet of the pig with syndactyly and 2 areas of maximum pressure on the palmar and plantar surfaces of the feet of the healthy pig. The color scale for pressure distribution ranged from dark blue (low pressure) to red (high pressure).
Citation: American Journal of Veterinary Research 77, 9; 10.2460/ajvr.77.9.976
Discussion
In dogs and cats, genetic forms of syndactyly are generally bilateral, whereas unilateral forms are sporadic.2 Because all limbs of pigs with syndactyly in the present study were compromised, it is strongly suggestive of a genetic condition; however, studies are needed to confirm this hypothesis. Because there was no history for these pigs, the genetic background was not known.
Syndactyly in humans may be described by 3 classification schemes: simple anatomic systems, descriptive and embryological approaches, and clinical and genetic approaches.22 In Angus cattle, syndactyly has been subdivided into 4 groups on the basis of the type of lesions: hooves without external signs of fusion, hooves incompletely fused, fused hooves with the presence of a groove, and hooves totally fused.4 In the present study, classification was based on results for clinical and radiographic examinations in which pigs with syndactyly were characterized by completely fused hooves.
Use of radiographs and CT images in the study reported here enabled further classification of syndactyly as simple syndactyly, complex-1 syndactyly, or complex-2 syndactyly. This classification method resembles classification schemes used in human patients (ie, simple or complex and complete or incomplete).3,23–25 In particular, simple syndactyly refers to connection between adjacent digits by only skin or fibrous tissue, whereas complex syndactyly refers to bony fusion of the adjacent digits and deformities of the fibrous tissue and skin.3,23 For complete syndactyly, adjacent fingers are joined throughout the entire length with soft tissue or bone (or both), and for incomplete syndactyly, interconnection of the digits may be discontinuous.3,24,25 In the present study, 13 of 20 limbs were characterized as complex-2 syndactyly, which suggested a more severe malformation because 2 bones were compromised.
In a morphological study11 that involved use of local Mexican pigs, it was observed that the native Mulefoot pigs had a first phalanx similar to that of pigs without syndactyly. However, the second phalanx was shorter and a third phalanx positioned between the principal digits was longer, compared with results for pigs without syndactyly. In the present study, 4 of the limbs of pigs in group 2 had 2 radiopaque structures located between the middle and distal phalanges, but the structure between the distal phalanges appeared similar to a third phalanx. For human patients, some cases are classified as complicated syndactyly if there is interposition of accessory phalanges or abnormal bone between the digits.25
In the present study, most of the bony fusions involved the middle and distal phalanges (13/16) or distal phalanges (3/16) of digits III and IV. Nevertheless, the fusion of paired phalanges in cattle with syndactyly reportedly includes from 1 paired phalanx to all 3 paired phalanges.26–28 In a case report,10 syndactyly in a pig was described as medial fusion of half of the second pair of phalanges. In addition to fusion of the phalanges, fusion of 1 or more carpal or tarsal bones and sesamoid bones has been identified in Angus cattle.28 Except for the phalanges, no signs of alterations in carpal or metacarpal bones or signs of secondary degenerative disease were identified in the pigs of the present study. However, 1 pig with complex-2 syndactyly had fusion of the distal sesamoids of the forelimbs.
Feet of the forelimbs are affected more frequently in cattle, but 1 or all feet may be compromised.4,6 In the present study, all feet were affected, but radiographic and CT imaging revealed complex-2 syndactyly in 8 feet of the forelimbs and 5 feet of the hind limbs. Cattle with syndactyly walk more slowly, often have a high-stepping gait, and may develop hyperthermia.6,28 In dogs, lameness or even inability for locomotion because of syndactyly has been reported,29–32 whereas in domestic cats, there are cases without signs of lameness.30 In the present study, signs of lameness were not observed in the affected pigs, which had locomotion similar to that of the healthy pigs, as suggested by visual analysis. Moreover, gait analysis by use of a pressure-sensing walkway did not reveal significant differences in kinetic and temporospatial variables as well as the SI.
Although the pigs were not trained to walk on the walkway, velocity did not differ significantly between groups. Thus, velocity did not affect group comparisons of kinetic and temporospatial variables or the SI. Gait analysis of weaned pigs deemed healthy during growth revealed that greater velocity was related to higher values for kinetic data collected with a pressure mat and normalized on the basis of body weight, but velocity did not influence asymmetry indices.17
In a study33 of 170-kg pigs walking on a pressure mat, differences in pressure distribution between the outer and inner claw were reported. Although quantification of pressure areas was not possible in the present study, 1 area of maximum pressure on both the plantar and palmar surfaces of pigs with syndactyly may eventually induce lesions in the feet of the forelimbs and hind limbs, especially in overweight or obese animals. Moreover, the study sample was composed of young pigs, and long-term effects of syndactyly must be investigated. In Angus cattle with syndactyly, hooves become increasingly curled and bent as the cattle mature, and gait becomes more altered as the animals grow older.28 In addition, the body weight distribution in both groups of pigs in the study reported here was greater toward the forelimbs than the hind limbs, which is similar to results in another study33 of healthy pigs. This fact needs to be considered in pigs with more severe syndactyly of the forelimbs because of a greater susceptibility to injury.
Limitations of the present study included the relatively small sample size and the fact that the malformations were analyzed only by use of radiographic and CT imaging. Evaluation of the gross anatomy could have provided more information about the malformation but was precluded by the fact that these pigs were not destined for slaughter.
In the population of pigs in the present study, the most common type of syndactyly was complex-2. Despite the lesions, most of the data obtained for pigs with syndactyly by use of a pressure-sensing walkway were similar to those of healthy pigs.
Acknowledgments
This manuscript represents a portion of a dissertation submitted by Dr. Justolin to the Universidade Estadual Paulista (UNESP) School of Veterinary Medicine and Animal Science as partial fulfillment of the requirements for a Master of Science degree.
Supported in part by FAPESP (The State of São Paulo Research Foundation, No. 2009/18299-7) and CNPq (National Council for Scientific and Technological Development [No. 300710/2013-5]).
ABBREVIATIONS
| PVF | Peak vertical force |
| SI | Symmetry index |
| VI | Vertical impulse |
Footnotes
Digital X-ray system, GE Health DR-F, Rio de Janeiro, Brazil.
Spiral scanner, Shimadzu SCT-7800CT, Kyoto, Japan.
Voxer 3D 6.3, Barco, Kortrijk, Belgium.
Walkway high resolution HRV4, Tekscan Inc, South Boston, Mass.
Walkway software, version 7.0, Tekscan Inc, South Boston, Mass.
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