In western Canada, TTN is generally used to describe a clinical syndrome of cattle, typically beef feedlot cattle, characterized by lameness localized to the distal aspect of a hind limb (distal hind limb) in the absence of any obvious signs of swelling. Inspection of the feet of affected limbs usually reveals white line separation along the apex of the toe.1–4 Debridement of affected claws to the level of the corium with hoof nippers frequently reveals either a dark purulent exudate or a dry black area of necrosis.4 Aggressive debridement often confirms that the disease has progressed to involve P3. Accordingly, Gyan et al3 suggested that TTN be defned as infammation or necrosis of the corium, which may or may not extend to inflammation, necrosis, or lysis of P3. It could be argued that this is too broad of a definition because an animal, particularly a live animal, might be assumed to have TTN solely on the basis of lameness and the presence of apical white line separation in the affected claw or claws. However, postmortem examination of affected feet frequently reveals extensive necrosis of P3 and inflammation of the associated soft tissues. Although the antemortem and postmortem findings associated with TTN may vary, from a practical management standpoint, the severity of disease is somewhat irrelevant because feedlot veterinarians are primarily concerned about ensuring that feedlot personnel correctly identify the cause of lameness rather than the severity of pathological lesions so that affected cattle can be appropriately treated and managed. The standard treatment for cattle with TTN includes parenteral antimicrobial administration with or without removal of the affected portion of the apex of the toe to confirm the diagnosis and facilitate drainage.
Although assigning a diagnosis of TTN to lame cattle might represent a pragmatic approach for consolidating the many different manifestations of the disease, the rather simplistic definition for TTN has its detractors. Specifically, some argue that proper examination of the foot of a lame animal should provide sufficient information for a proper diagnosis, which in many instances may lead to the lesion being defined as toe necrosis. The International Committee for Animal Recording describes toe necrosis as necrosis of the tip of the toe with involvement of bone tissue.5 In western Canada, veterinarians frequently refer to confirmed toe necrosis as P3 necrosis, TTN, or, more recently, TTN syndrome.3,4,6–9 Complicating matters is the fact that there is another moniker used to describe what appears to be the same disease. In the early 1980s, Sick et al1 documented the first outbreak of TTN in North American feeder cattle, which was followed by a report by Miskimins2 in the early 1990s. In both instances, the authors described the presence of purulent discharge at the tips of the toes of affected cattle and ascribed the term toe abscesses to the disease. The epidemiology, clinical findings, and postmortem findings detailed in both of those reports1,2 are remarkably similar to what veterinarians currently refer to as TTN or TTN syndrome. Of particular interest are descriptions of the postmortem findings, which include rounding of the apex of the toe, white line separation, P3 necrosis, arthritis, cellulitis, tendonitis, tenosynovitis, myositis, and systemic pathological changes consistent with bacteremia.1,2,4,8,9 Consequently, TTN syndrome has entered the lexicon because that term denotes that, although the condition my initially begin with TTN, affected animals that die or are euthanized because of the disease invariably have P3 necrosis in conjunction with various other sequelae.
Perhaps 1 point that all researchers and feedlot veterinarians can agree on is that apical white line separation is associated with lameness. Specifically, lame cattle do not develop P3 necrosis in the absence of white line separation.3 Given the anatomic structure and importance of the white line to the bovine foot,10,11 the presence of white line separation as a prerequisite for TTN seems logical. The white line is an inherently weak junction of the hoof wall and sole and is composed primarily of laminar horn produced by the laminar corium. Laminar horn undergoes suboptimal keratinization, resulting in immature nontubular horn that is soft and flexible and predisposed to mechanical failure and foreign body penetration. Consequently, bacteria associated with TTN likely gain access to the deep tissues of the hoof through a breach in the white line.
The pathogenesis of TTN has not been fully elucidated; however, the epidemiology and clinical findings support an abrasion theory. That theory posits that during transport and handling at auctions and processing shortly after feedlot arrival, cattle abrade the soles and apical region of the white line of their hooves on hard coarse surfaces, such as metal trailer and concrete flooring. This abrasion compromises the integrity of the white line, leading to its separation and the subsequent colonization of the foot tissues with bacteria that cause P3 necrosis and the myriad of associated sequelae. This theory seems plausible because the incidence of TTN is greatest for cattle within days to weeks after feedlot arrival,1,2,6 which coincides with exposure of the cattle to abrasive flooring surfaces. Moreover, the apical white line region of claws with TTN is significantly thinner than that of healthy claws,7 which strongly suggests an abrasive mechanism. There is also anecdotal evidence that a hyperexcitable temperament is a risk factor for TNN.1,4 Presumably, overcrowding or overly aggressive handling results in cattle forcing themselves against the animals ahead of them in alleyways and chute systems. As the force exerted by those cattle increases, they lose traction, especially in the hind limbs that are being used for propulsion, and this loss of traction results in rasping of the solar horn and white line on the handling system flooring. Paradoxically, to improve cattle footing and traction, the flooring of feedlot handling systems frequently consists of stamped or etched concrete or has metal cleats installed in it, which may be risk factors for white line abrasion. Once the white line is compromised, repetitive loading and unloading of the claws during ambulation presumably lead to apical white line separation. This last supposition is supported by the finding of macroscopic feed and bedding particles within the hoof capsule of affected claws, which suggests that white line separation can be sufficient to allow foreign material to become entrapped within the claw. This is important because white line separation is often difficult to appreciate in a non-weight-bearing foot,4,7 a fact that further suggests the separation must occur under physiologic loading.
The veterinary literature contains little information regarding the effects of physiologic loading on the hind feet of cattle, with only a few studies12–15 conducted related to materials testing and finite element analysis. Studies describing the extent of white line separation in diseased claws with and without loading are lacking. The purpose of the study reported here was to compare the extent of white line separation created during physiologic loading in bovine claws with and without evidence of TTN. The overall aim was to gather information about the possible role of mechanical loading on the pathogenesis of TTN in cattle.
Materials and Methods
Specimens
The distal hind limbs from yearling beef cattle of various breeds were acquired by feedlot veterinarians in Alberta, Canada, and sent to investigators for testing. Veterinarians were asked to submit distal hind limbs from cattle that met the definition of a putative diagnosis of TTN along with an equal number of clinically normal distal hind limbs (controls) from cattle of similar size and weight. All hind limbs were harvested during routine postmortem examination of feedlot cattle that were euthanized or found dead. All cattle from which hind limbs were harvested weighed approximately 250 to 300 kg at the time of death. Both hind limbs were harvested from cattle with gross evidence of TTN because it is not uncommon for affected cattle to have > 1 hind claw with TTN. For each animal with presumptive TTN, the submitting veterinarians sectioned 1 or both claws of the most severely affected hind limb to confirm the diagnosis. Confirmation of TTN required evidence of white line separation and P3 necrosis. After diagnosis of TTN was confirmed, the claws of the contralateral hind limb were examined for evidence of white line separation; if white line separation was present, the claws were considered affected with TTN for the purpose of the study and left intact for mechanical testing. Control hind limbs were obtained from cattle that died or were euthanized for diseases unrelated to lameness (eg, pneumonia), and the claws of the control hind limbs had no evidence of white line separation.
The distal hind limbs were removed from the carcass at the level just proximal to the metatarsophalangeal (fetlock) joint. Each specimen was placed in a clean plastic palpation sleeve, labeled, and stored frozen at −20°C until being shipped on ice to investigators at the Western College of Veterinary Medicine in Saskatchewan, Canada. After the harvested limbs arrived at the veterinary college, they were once more placed in a freezer and stored at −20°C until mechanical testing. Results of a previous study16 indicate that frozen storage does not affect the mechanical strength or stiffness of bovine horn material.
Specimen preparation
Distal hind limb specimens were thawed and processed prior to mechanical testing. Each thawed specimen was sectioned horizontally (ie, was cross-sectioned) at the middle of the first phalanx, and all soft tissues were removed. The specimens were then fixed (potted) in an anatomic position for mechanical testing. The bottom surface of the foot was angled at approximately 5° to the horizontal plane such that the apex of the claws made initial contact with the testing surface to simulate physiologic loading conditions. The potting system was comprised of an outer shell made of polyvinyl chloride with a support base made of bone cement (polymethyl methacrylatea) and a gypsum potting material.b The distal half of the first phalanx and part of the second phalanx were fixed in the potting system such that the distal 4 cm of hoof wall remained exposed on each claw (Figure 1).
Photographic images of the distal aspect of a bovine hind limb (distal hind limb) with TTN that was mounted in a customized apparatus integrated with a servohydraulic material testing system as obtained from the side (A) and looking upward to the solar surface of the mounted hoof during the application of a static load of 1 kN (B). The distal half of the first phalanx and part of the second phalanx were fixed (potted) in anatomic position in a customized apparatus that consisted of an outer shell of polyvinyl chloride with a support base of polymethyl methacrylate and a gypsum potting material such that the bottom and distal 4 cm of hoof wall remained exposed on each claw. The limb was fixed so that the bottom surface of the hoof was angled at approximately 5° to the horizontal plane such that the apex of the claws made initial contact with the testing surface to simulate physiologic loading conditions. A digital camera was mounted within a protective housing 30.5 cm underneath a 2.5-cm-thick clear acrylic plate (testing surface) and was used to obtain 2-D images of the bottom of the hoof during the application of each of 3 increasing static loads (1, 2, and 3 kN). The testing surface was lighted during image acquisition, and white line separation, which increased as the applied load increased, appeared as blackened areas along the white line.
Citation: American Journal of Veterinary Research 80, 8; 10.2460/ajvr.80.8.736
Mechanical testing and 2-D image acquisition
A customized testing apparatus was integrated with a servohydraulic material testing systemc (Figure 1). The customized apparatus was designed such that a load could be applied to the claws while a camera,d which was located within a protective housing 30.5 cm underneath a 2.5-cm-thick clear acrylic plate (testing surface), obtained 2-D images. Given that setup, each pixel was equivalent to 50 μm. Each potted specimen was centered above the camera when it was mounted in the testing system; therefore, image distortion (eg, fisheye) was minimized as verified by results of calibration studies.
Increasing static compressive loads were applied to the foot in a stepwise manner, and images of the bottom of the foot were obtained at each load to assess the presence and extent of white line separation. The initial load applied was 1 kN, which was consistent with a 250-kg feedlot animal placing 40% of its body weight on a single hind limb during ambulation (the remaining 60% of the animal's body weight would be supported by the contralateral forelimb).17 The second compressive load applied was 2 kN, which was consistent with sudden impact loading (twice body weight is a common impact load18). The final load applied was 3 kN, which was considered an extreme load that would be expected when an animal was aggressively pushing others in a chute or alley. The application of each load caused the bottom of the foot to rest flat (ie, at a 0° angle to the horizontal plane) on the testing surface. After completion of mechanical testing, white line separation within each claw was verified with a dental probe.
Image processing
All 2-D images were analyzed with commercial image-processing softwaree to characterize the presence and extent of white line separation. The white line space was segmented by use of a region-growing technique to quantify separation area, with manual correction performed with a tablet and stylusf (Figure 2). The half-maximum height method19 was used to identify the threshold for the region-growing technique. Measurement precision errors were assessed by segmentation of each image 3 times and calculation of the root mean square coefficients of variation. The root mean square coefficients of variation precision error was calculated to be 7.8% for measures of white line separation area.
Photographic images of the bottom of a bovine hind limb claw with TTN obtained during application of a static load of 1 (A), 2 (B), and 3 (C) kN following image processing to characterize the presence and extent of white line separation. A region-growing technique with manual correction via a stylus and tablet was used to identify regions of white line separation (yellow highlighted areas) and calculate the white line separation area. Notice that the white line separation area increased as the applied load increased.
Citation: American Journal of Veterinary Research 80, 8; 10.2460/ajvr.80.8.736
Statistical analysis
White line separation area was the outcome of interest. The white line separation area was calculated for each claw at each applied load and summed for the 2 claws of each hind limb. The data distribution for white line separation area was assessed for normality by visual inspection of Q-Q plots. A repeated-measures ANOVA was used to assess the interaction of group (TTN vs control) and tested load (1, 2, or 3 kN) on white line separation area. The model included fixed effects for group and the interaction between group and load. When necessary, post hoc pairwise comparisons were performed with Student t tests with the Bonferroni correction used to control for type I error. Cohen d, which provides an estimate of the effect size between 2 means in relation to the pooled SD,20 was calculated for each load. For this study, the Cohen d provided an estimate of the magnitude of effect that a given load had on the mean white line separation area between claws with and without TTN. A Cohen d > 0.80 is considered a large effect size.21 All analyses were performed with commercially available statistical software,g and values of P < 0.05 were considered significant.
Results
Descriptive statistics for white line separation area for claws with TTN (diseased claws) and control claws at each applied load were summarized (Table 1). There was a significant (P < 0.001) interaction between group (TTN vs control) and load on white line separation area. The white line separation area for diseased claws was significantly greater than that for the control claws at all 3 applied loads (Figure 3). The Cohen d indicated that each of the 3 applied loads had a large effect on the magnitude of the mean difference in white line separation area between diseased and control claws.
Plot of mean white line separation area versus applied static load for bovine hind limb claws with (dashed line with circles; n = 10) and without (controls; solid line with squares; 10) TTN. Brackets represent the SD and are not visible for the control group because the SDs were so small (< 0.22 mm2).
Citation: American Journal of Veterinary Research 80, 8; 10.2460/ajvr.80.8.736
Descriptive statistics for white line separation area (mm2) following the application of each of 3 increasing static loads to bovine hind limb claws with (diseased claws; n = 10) and without (control claws; 10) gross evidence of TTN.
| Diseased claws | Control claws | |||||
|---|---|---|---|---|---|---|
| Load (kN) | Mean (SD) | Range | Mean (SD) | Range | P value* | Cohen d† |
| 1.0 | 28.5 (12.6) | 18.1–61.1 | 0.020 (0.045) | 0–0.129 | 0.016 | 1.41 |
| 2.0 | 51.9 (16.9) | 37.2–96.0 | 0.065 (0.086) | 0–0.198 | 0.014 | 1.41 |
| 3.0 | 101 (24.7) | 67.2–144 | 0.103 (0.105) | 0–0.294 | < 0.001 | 1.41 |
For a post hoc Student t test used to compare the mean white line separation area between diseased and control claws at the given applied load, values of P < 0.05 were considered significant.
Estimate of the magnitude of effect (effect size) that a given load had on the mean white line separation area between claws with and without TTN in relation to the pooled SD; a Cohen d > 0.80 was considered a large effect size.
Discussion
Results of the present study indicated that the mean white line separation area for bovine hind limb claws with TTN (diseased claws) was significantly greater than that for healthy bovine hind limb claws (controls) at each of 3 applied mechanical loads (1, 2, and 3 kN). Moreover, the mean white line separation area increased significantly as the applied load increased for diseased claws but did not change significantly as the applied load increased for control claws. In fact, the control claws had virtually no evidence of white line separation at any of the 3 applied loads. This finding was important because it provided an explanation for the pathogenesis of TTN and insight into how fairly large particles of organic material become lodged within the hoof capsule of diseased claws.
In the present study, the application of a static load with increasing force to diseased claws resulted in a significant increase in the extent of white line separation in those claws. This supported our supposition that repetitive loading and unloading associated with ambulation contribute to the physical breakdown of the white line in diseased bovine claws. Once the white line laminae become compromised and begin to separate, it seems logical that continuous loading and unloading of the affected claw will lead to additional separation of the white line.
As the extent of apical white line separation increases, so does the opportunity for organic material, laden with microorganisms, to become impacted within the white line and hoof capsule (Figure 4). In a previous study,7 a mixed population of anaerobic (Fusobacterium necrophorum and Bacteriodes spp) and facultative anaerobic (Escherichia coli, Corynebacterium spp, Trueperella pyogenes, Streptococcus spp, Staphylococcus spp, and Pseudomonas spp) bacteria was isolated from TTN lesions. We suspect that bacterial enzymes and enzymes associated with the inflammatory process likely contribute to further degradation of the white line and suspensory apparatus of TTN-affected limbs.
Photographic image of a sagittal cross section of a distal hind limb of a beef feedlot animal that depicts white line separation and P3 necrosis, which are characteristic of TTN. Notice that there is a considerable amount of plant material impacted between P3 and the sole of the hoof, which likely facilitated the entry of pathogenic organisms into the foot and contributed to the necrosis of P3.
Citation: American Journal of Veterinary Research 80, 8; 10.2460/ajvr.80.8.736
Breaches within the white line may help explain the rapid onset of TTN. In a large epidemiological study6 of 702 feedlot cattle with TTN, the mean interval between feedlot arrival and the first treatment for TTN-related lameness was only 18.9 days (median, 12.0 days), and some cattle were lame at feedlot arrival. Twenty-four of the 37 (65%) animals treated for lameness within the first 5 days after feedlot arrival were eventually euthanized and had lesions consistent with TTN identified during necropsy.6 The finding that apical white line separation increased with the applied load in the present study provided circumstantial evidence that physiologic loading may be an important factor in the pathogenesis of the TTN. Physiologic loading can contribute to the physical breakdown of a compromised white line and facilitate entry of bacterial pathogens into the white line and hoof capsule. Additionally, 3 kN was the highest static load applied to the feet of the present study. It is likely that the hind feet of heavily muscled beef cattle will be subjected to even greater loads. Also, in a typical feedlot situation, cattle are exposed to various types of flooring surfaces, many of which may be uneven, which could lead to the concentration of greater forces and subsequent focal degeneration of the white line.
The lack of white line separation in the control claws indicated that static compressive loading and isolated excess loading may not directly lead to TTN. Rather, loading likely exacerbates and accelerates the disease process once the white line becomes compromised. It is important to note that, for the diseased claws, marked white line separation was observed only under loading; white line separation was minimal when the diseased claws were not under load.
The veterinary literature regarding mechanical testing of bovine claws is sparse. Most of the previous studies10–13,22 focused on determining the material properties of claws, not investigating white line separation. The present study was novel in that it investigated the premise that mechanical loading would increase white line separation in claws with TTN. Furthermore, mechanical loading did not result in white line separation in control claws, which suggested that loading forces alone are insufficient to initiate white line separation. It is most likely that the inciting cause of TTN is physical abrasion of the apex of the toe leading to a thinning of the white line. Supporting evidence for that supposition is the fact that the apical white line of hind limb claws is thinner in feedlot cattle that died or were euthanized because of TTN than in cattle that died of all other causes.3
The present study had multiple strengths and weaknesses. One strength was that we developed a useful tool for characterization of the white line area. This tool could be beneficial for future research into TTN. Another strength was that, to our knowledge, the present study was the first to mechanically test bovine claws in a manner similar to in vivo loading conditions. This method could become the standard for assessment of bovine claws and be applied in clinical settings (eg, integration of cameras in the flooring of cattle handling facilities). It could also be applied to other ruminant species for which the observation of the solar surface of the feet under physiologic loading is warranted or desired.
The limitations of the present study included the small sample size, nonrandomization and potential selection bias of samples, potential for the presence of concurrent laminitis in the diseased claws, and issues associated with the loading magnitude and configuration. Although only 10 diseased and 10 control claws were evaluated, on the basis of the large effect sizes observed, we do not believe evaluation of a larger number of claws would have substantially changed our overall findings. Toe-tip necrosis occurs only sporadically; thus, it was not possible to select study feet on the basis of specific variables such as breed, body weight, and claw length. It would be prudent to repeat this study with a larger and more varied cohort of study specimens to investigate the role of those specific variables on white line separation. The diseased claws were not assessed for laminitis prior to testing. That was a notable limitation because laminitis can cause dyskeratosis and alter the chemical structure of the white line. Thus, white line separation during loading may be exacerbated in laminitic claws. However, we believe that it was unlikely the diseased feet used in the present study were concurrently affected with laminitis because TTN typically occurs soon after feedlot arrival, whereas laminitis generally occurs later in the feeding period following the implementation of an aggressive, high-energy nutritional program.23 Finally, only compressive loading was assessed in this study. The application of a combination of vertical and horizontal forces would have better approximated the physiologic forces that bovine claws undergo during normal ambulation and is a direction for future research.
The findings of the present study added to the understanding of the pathogenesis and clinical presentation of TTN in beef feedlot cattle. Veterinarians and feedlot operators should be cognizant that the white line of TTN-affected claws will have minimal evidence of separation during a routine hoof examination when the limb is not bearing weight. Once the white line becomes compromised, mechanical loading contributes to white line separation, which facilitates bacterial contamination and subsequent infection of the subcapsular structures of the hoof. We recommend that TTN lesions be treated in a manner similar to that for toe abscesses with aggressive debridement of damaged tissues. The application of a block to the unaffected claw will minimize the force applied to the affected claw, thereby preventing further damage to the white line.
In conclusion, the extent of white line separation during mechanical loading was significantly greater in bovine claws with TTN than unaffected control claws. That finding supported our hypothesis that mechanical loading is involved in exacerbation of TTN. Moreover, the fact that virtually no white line separation was observed in the control claws during mechanical loading seemed to suggest that compressive loading alone, even at excessive levels, does not initiate TTN.
Acknowledgments
Supported by the Government of Saskatchewan Agriculture Development Fund.
The authors declare that there were no conflicts of interest.
The authors thank Dr. Mike Jelinski, Dr. Elizabeth Homerosky, Dr. Fritz Shumann, and Merle Friesen for donation of the diseased and control specimens used in this study and Rob Peace for assistance with the experimental setup.
ABBREVIATIONS
| P3 | Third phalanx |
| TTN | Toe-tip necrosis |
Footnotes
Fastray, Bosworth, Chicago, Ill.
Denstone, Modern Materials Inc, South Bend, Ind.
MTS Bionix, Model 370.02 Axial/Torsional, MTS Systems Corp, Eden Prairie, Minn.
Point Grey Chameleon3 5MP monochrome camera with 16-mm focal length, FLIR, Richmond, BC, Canada.
Analyze 10, Analyze Direct Inc, Overland Park, Kan.
WACOM Cintiq 21UX, Portland, Ore.
SPSS, version 22 for Windows, SPSS Inc, Chicago, Ill.
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