A longitudinal investigation of an outbreak of toe tip necrosis syndrome in western Canadian feedlot cattle

Abstract

This investigation followed a cohort (n = 21) of single-sourced Angus cross yearling heifers diagnosed with toe tip necrosis syndrome (TTNS). The animals were intensively followed for ~7 months, over which time 5 animals were euthanized because of intractable lameness or life-threatening sequelae such as cellulitis and myositis. Treatment consisted of systemic antimicrobial and nonsteroidal anti-inflammatory therapy, removing the necrotic horn tissue to facilitate drainage, and relocating the cattle to an earthen-floor pen. Sixteen of the 21 heifers recovered uneventfully. Upon sectioning the feet after slaughter, all the foot lesions had healed, but in some instances, the 3rd phalangeal bone had undergone bone remodeling, indicative of an earlier pathological process. This study is unique in that it chronicled the clinical and pathological outcomes associated with TTNS over an extended period.

Introduction

Toe tip necrosis syndrome (TTNS) describes a lameness most commonly associated with feedlot cattle (1). While TTNS is a relatively new term, the disease was first reported in 1979 in a group of dairy heifers (2). These heifers developed a hind limb lameness within 3 wk of transit, and hence the disease was labeled as a “transit-related lameness.” Clinically, the affected feet were not swollen, but white line separation was evident and debriding the apical region of the affected claws revealed blackened (necrotic) horn tissue or a purulent solar abscess. Treatment consisted of debriding the lesion and relocating the cattle to pasture; most animals made a full recovery within 14 d. A similar outbreak was reported 3 y later in feedlot cattle (3); the epidemiology and clinical findings were consistent with those reported previously in the dairy heifers, but the lesions were described as “toe abscesses.” Some cattle also had postmortem findings consistent with bacteremia. It was noteworthy that the feedlot personnel frequently misdiagnosed the lameness as a hip injury or foot rot. Once properly diagnosed, treatment consisted of antimicrobial therapy, debridement of the abscesses, and moving the cattle to earthen-floored holding facilities. The next peer-reviewed report, in 1994, described outbreaks of toe abscesses in 5 mid-western American feedlots (4). Most lesions developed in the lateral hind claw but the medial claws and front feet were occasionally affected. Ascending tendonitis and/or cellulitis of the hind limb was reported. The disease was thought to be initiated by excessive wear of the soles on abrasive surfaces and it was postulated that wet weather conditions might have led to softer horn tissue, increasing the risk of abraded soles. More recently, outbreaks of TTNS have been reported in beef calves in the United Kingdom (5,6), and in one instance the calves were being handled in a new chute system having a solid galvanized steel floor outfitted with grip bars for traction (5).

In a case series study of 53 cattle with toe ulcers and/or apical pedal bone necrosis, 49 animals had necrosis of the 3rd phalangeal bone (P3 necrosis) (7). Fourteen of 49 animals had P3 necrosis involving 2 or 3 claws. Most (73%) affected claws had necrosis of the apical regions of the white line (zone 1) and sole (zone 5) as well as white line separation, thin soles, and under-run soles. In ~50% of cases, the lesions were attributed to excessive trimming with hoof grinders. More importantly, neither the degree of white line separation nor the size of the toe lesions correlated with the degree of osteolysis of P3. The uncomplicated toe ulcers were treated by debriding the horn tissue and affected corium. A bone curette or hammer and chisel were used to resect the infected P3 bone. Cases with minimal P3 involvement usually resolved within 30 d. While the toe lesions frequently fit the description of abscesses, “toe ulcer” was deemed to be a more appropriate term.

The International Committee for Animal Recording (ICAR) defines toe ulcer (Pododermatitis solearis circumscripta purulenta et neroticans chronica) as a “circumscribed chronic purulent and necrotizing inflammation of the corium of the claws at the toe” (8). Although the lesions found in feedlot cattle are frequently referred to as toe abscesses, the lesion is technically an ulcer because it is a full-thickness defect of the epidermis (horn tissue), which exposes the underlying fresh or necrotic dermis (corium) (9,10). The use of toe ulcer, however, may only serve to add further confusion. In the dairy industry, toe ulcers (TU) and thin sole toe ulcers (TSTU) are common causes of lameness; however, the etiology, pathogeneses, and clinical manifestations of these diseases are very different from TTNS of feedlot cattle (9,11,12). Therefore, it is important to appreciate that toe lesions of feedlot cattle differ from TU and TSTU of dairy animals.

While toe ulcer may be the most appropriate terminology for describing the formative stages of the disease, feedlot veterinarians frequently encounter the more advanced stages of “toe necrosis.” The ICAR Claw Health Atlas describes toe necrosis as necrosis of the tip of the toe with involvement of bone tissue (10). This is synonymous with “P3 necrosis,” a term commonly used in western Canadian feedlots to describe toe necrosis. The term TTNS is an extension of toe necrosis, with toe tip necrosis describing the hallmark clinical findings of the disease, and syndrome encompassing all the sequelae. It has, however, been suggested that the term TTNS not be used. Rather, toe necrosis should be used to describe the primary foot lesion and any sequelae reported separately (13).

Confusion regarding the most appropriate terminology may be explained, in part, by the current understanding of the pathogenesis of TTNS. The “abrasion theory” posits that cattle abrade the apex of the toes during shipping and handling, resulting in a reduction in the integrity of the white line (14). During ambulation, loading forces placed on the hoof result in micro-fissures along the white line, which become colonized with bacteria such as Trueperella spp. (15). Pain, as evidenced by lameness, is manifested once the infection reaches the sensitive and highly vascularized corium (dermis). On close inspection, necrosis of the apical white line may appear as a dry black lesion, or it may have a dark brown, gray, or black exudate. This latter presentation is the classical toe abscess. The infection may underrun the sole or alternatively breach the corium and infect the pedal bone, resulting in toe necrosis. Finally, the infection may either ascend the hind limb or spread hematogenously to more distant organs.

Toe necrosis is a fitting term for describing a claw having necrosis of the horn and P3 osteolysis. However, in most feedlot situations a definitive diagnosis of toe necrosis is made at the time of postmortem examination. Unless euthanized, animals do not die of toe necrosis, rather they frequently die of the sequelae (14). Toe tip necrosis syndrome (TTNS) covers the range of clinical findings from uncomplicated necrosis of the tip of the toe (without P3 involvement) to a myriad of sequelae associated with toe necrosis. In outbreak situations, clinical signs range from early white line separation to extensive pedal bone necrosis and in some cases pathological findings consistent with bacterima (e.g., embolic pneumonia).

This report describes the clinical and pathological findings associated with an outbreak of TTNS involving a cohort of yearling beef heifers. The heifers were intensively followed for 216 d, from diagnosis to slaughter.

Materials and methods

History and clinical assessments

In the fall of 2014, 95 Angus cross yearling heifers were shipped ~90 km directly from a ranch to an auction market. The cattle were sold the following day and 45 of them were transported ~25 km to a commercial feedlot. Within 48 h of arrival, an unusually high number of animals developed lameness of the hind limbs. The auction market offered to take back the lame animals, which the feedlot obliged by returning 21 animals displaying varying degrees of lameness. It was undetermined whether the lame animals received antimicrobial therapy before being returned.

Day 1 of the investigation began at the auction market with an examination of the 21 heifers. Based on the clinical history and signalment, TTNS was considered the most probable cause of lameness and hence all hind claws, and when warranted the front feet as well, were examined for signs of apical white line separation and/or necrosis of the tips of the toes. The diagnosis was confirmed by paring the affected white line to the level of healthy horn tissue or to the corium. This procedure confirmed the diagnosis and facilitated drainage.

In addition to the clinical examinations, whole blood and ear notch skin samples were obtained for bovine viral diarrhea virus (BVDV) testing, and claws having a purulent discharge were swabbed for microbiological testing. Sample collection and laboratory testing procedures for BVDV and microbiological testing have been previously described (14).

A recumbent heifer (#1), having lost considerable body condition compared to her contemporaries, was euthanized. Of the remaining 20 heifers, 19 had ≥ 1 claw with white line separation and necrosis of the toe tip. The auction owner was advised of the clinical findings, at which point the animals were donated for research.

The cattle were transported on day 8 from the auction to Agriculture and Agri-Food Canada’s Lethbridge Research Station (LRC), Lethbridge, Alberta. Here they were weighed, body temperatures taken, feet re-examined, and each administered tilmicosin (Micotil; Elanco, Guelph, Ontario), 10 mg/kg body weight (BW), IM, and a nonsteroidal anti-inflammatory drug (Metacam; Boehringer Ingelheim, Burlington, Ontario), 0.5 mg/kg BW, IM. The heifers were relocated to an earthen-floored feedlot pen and fed commercial feedlot rations for ~7 mo.

Body temperatures were within normal range 2 wk after arrival at the LRC. On day 36, 11 animals were febrile and had clinical signs consistent with bovine respiratory disease; each animal was administered tulathromycin (Draxxin; Zoetis, Kirkland, Quebec), 5 mg/kg BW, IM. One (#19) animal was re-treated with tulathromycin on day 50, along with 2 animals that had not received treatment on day 36. Animal #19 was re-treated on day 69 with tilmicosin (Micotil; Elanco), 10 mg/kg BW, IM.

Over the course of ~7 mo, the feet were examined bi-weekly for the first 3 mo and then monthly until slaughter: day 216. Double sole formation was a common finding, and the overlying sole was routinely debrided. More extensive debridement, removal of all necrotic tissue, was also undertaken when warranted. The feet and all carcass data were collected at slaughter.

Gross postmortem and histological examination procedures

Any animals deemed to be severely compromised, as determined by the systemic progression of the disease, were euthanized and a gross postmortem examination was performed. Hind feet and tissues having gross pathological changes were submitted to Prairie Diagnostic Services (PDS, Saskatoon, Saskatchewan) for histopathological examination and microbiological testing. In addition to standard hematoxylin and eosin (H&E) staining, a Warthin Faulkner silver stain was used to aid in the visualization of spirochetes. Sub-samples of each tissue were submitted for microbiological testing.

Results

Clinical and gross pathological findings

All 19 animals diagnosed with TTNS had separation of the white line in the apical region of the toe. Upon initial examination (day 1), most toe lesions appeared as dry black horn tissue; however, 5 heifers had a bloody, gray, or dark brown purulent exudate. Over the course of the study it was not unusual for lesions to develop in more than 1 claw; 1 heifer had TTNS in 3 of 4 hind claws. One animal developed draining abscesses above the coronary band. In total, 5 animals were euthanized over the course of the study, with animal #1 being euthanized on day 1.

Figures 1 to 4 are photographs of the clinical and gross pathological findings from 4 animals, 2 of which were euthanized. Figure 1 details the progression of the disease in animal #2. On day 1 (Figure 1A), the leading edge of the apex of the toe was worn and white line separation was evident. Removal of the apex (“nipping” or “tipping”) of the right lateral claw resulted in a purulent discharge. By day 50, granulation tissue was forming, and a double sole had developed (Figure 1B). The double sole formation was a finding in nearly all the cattle. At the time of slaughter, the right lateral (RL) claw had developed a much thicker sole compared to the medial claw of the same foot (Figure 1C). There was no evidence of an ongoing pathological process such as infection in either claw; however, P3 of the RL claw was noticeably blunt, indicative of past bone remodeling.

Figure 1.

A series of photographs taken from animal #2 on day 1, day 50, and after slaughter. A — Initial diagnosis on day 1 was confirmed by debriding the tip of the toe. B — Double sole has formed by day 50. C — At the time of slaughter, the 3rd phalangeal bone of the right lateral (RL) claw shows evidence of remodeling (arrow) and the sole is much thicker compared to that of the medial claw (arrows).

Figure 4.

A series of photographs from animal #5 taken on day 1 and day 8. A — There was minimal white line separation (arrow) of the right lateral (RL) claw on day 1. B — Tipping both right hind claws on day 8 shows an infected RL claw and a normal right medial claw. C — Both claws on the left hind foot were diseased, with the left lateral (LL) showing a typical “dry” lesion, while the medial claw appeared as a classical “toe abscess.”

Figure 2 is a series of photographs obtained from animal #3. The slight wear along the apex of the toe and the mild degree of white line separation were difficult to visualize. However, nipping the toe resulted in a bloody brown discharge (Figure 2A). By day 78, the animal had formed a double sole (Figure 2B). Sectioning of the claws after slaughter revealed evidence of P3 remodeling (Figure 2C).

Figure 2.

A series of photographs obtained from animal #3 on day 1, day 78, and after slaughter. A — There was little evidence of white line separation on day 1; however, removing (nipping) the end of the toe resulted in a dark bloody discharge. B — The animal developed a double sole. C — At slaughter there was evidence of remodeling of 3rd phalangeal bone (arrow).

Animal #4 had no evidence of an active ongoing infection in any of the hind claws on day 1 (Figure 3A). By day 8, a bloody purulent exudate was expressed with hoof testers from the lateral claw of the right hind foot (Figure 3B). This animal was euthanized the same day, and the infection was found to have migrated from the foot to the level of the stifle, resulting in a necrotizing myositis and cellulitis (Figure 3C).

Figure 3.

A — The lateral left hind (LH) claw shows a normal hoof after nipping. B — By day 8, both claws of the contralateral limb had evidence of toe tip necrosis. C — The animal was euthanized on day 8 and postmortem examination revealed a necrotizing myositis and cellulitis that extended past the stifle joint.

Animal #5 had minimal white line separation of the lateral claw of the right hind foot (RL) (Figure 4A) on day 1. Nipping the toes revealed an underlying septic process in the lateral claw of the right hind foot (Figure 4B) and both claws of the left hind foot (Figure 4C). The animal was euthanized on day 8 and found to have an extensive necrosuppurative cellulitis of the hind limb.

Histopathological and laboratory findings

Five animals were euthanized between October 2 and 28, 2014, all of which underwent a gross postmortem examination. Animal #1, euthanized on day 1 at the auction, had toe necrosis (P3 necrosis) of both lateral hind claws and embolic pneumonia; a heavy growth of Trueperella pyogenes was isolated from both the lungs (4+) and P3 lesions (3+). The lungs and P3 lesions also had moderate growth of Escherichia coli (2+). Of the remaining 4 euthanized animals, all had toe necrosis involving more than 1 hind claw. Animal #4 had a necrotizing myositis and cellulitis, and animal #5 had a necrosuppurative cellulitis. Together these latter 2 animals had a mixed population of T. pyogenes, Pseudomonas spp., E. coli, and Fusobacterium spp. The main pathological finding associated with the remaining 2 submissions (animals # 2 and #3) was toe necrosis of the hind claws. No spirochetes were associated with any of the toe lesions.

Bovine viral diarrhea virus (BVDV) was not detected in any of the blood samples nor in any of the ear skin notches.

Slaughter data

The mean hot carcass weight of the 16 heifers was 348 kg ± 25.6 [standard deviation (± SD)]. Three heifers had a yield grade 1 (Y1), 11 were Y2, and 4 were Y3. The breakdown of the carcasses by quality grade was as follows: AAA (n = 7), AA (n = 8), and A (n = 1).

Discussion

The sporadic nature of toe tip necrosis syndrome (TTNS) complicates conducting well-designed clinical field studies dedicated to determining best practices for the treatment of this disease (TTNS). Therefore, this outbreak provided a unique research opportunity because the source of the cattle was known, the attack rate was very high, the cattle could be intensively studied over a period of several months, and pathological changes to the claws were correlated to the antemortem clinical findings. It was also fortuitous that the auction donated the animals and that the Lethbridge Research Centre’s facilities and personnel were available to house and study the animals over a 7-month period. Unfortunately, the health status of the remaining heifers that originated from the same ranch, but were sold to other feedlots, remains unknown. If all the heifers were similarly affected with TTNS, then this would suggest a common source of risk factors such as nutritional status while on pasture, genetics, temperament (hyperexcitability), and the shipping and handling from the pasture to the auction.

This investigation underscores several important points for consideration when investigating a TTNS outbreak. The disease frequently clusters and may involve a large percentage of the animals at risk. While nipping or debriding the lesions is an excellent diagnostic procedure, it is a poor prognostic tool. Administering systemic antibiotics, nipping the toes to facilitate drainage, and relocating the animals to earthen floor pens appear to have assisted healing in most animals. However, there were no nontreated controls and ~25% of the affected animals were euthanized because of intractable lameness or the development of life-threatening sequelae. Finally, temperament or hyperexcitability may have been a risk factor for developing TTNS.

The serial photographs underscore some important points concerning the clinical examination of animals with suspected TTNS. Close attention must be given to examining the apex of the toe for evidence of white line separation. If the feet are heavily soiled or if there are poor lighting conditions, then running a probe or thumbnail along the white line is a useful procedure for diagnosing white line separation. However, finding white line separation does not confirm toe tip necrosis (osteolysis of P3). Rather, the toe must be debrided or radiographed. Debridement, however, is usually sufficient to confirm the diagnosis. Furthermore, based on first principles for managing an abscess, debriding the claw assists with drainage. Feedlot veterinarians often refer to removing the toe tips as “tipping the toes,” which involves using a set of hoof nippers to remove the apex of the toe to determine the extent of the infection. In this study, nipping or tipping the toes was performed at the time of the initial examination, while debridement was performed at the LRC when there was more time and under working conditions. It is important to distinguish nipping from debridement. In the former, the horn is removed to confirm a diagnosis, while debridement is a therapeutic procedure that involves the removal of all the necrotic tissue.

Currently, there is no standard protocol for treating TTNS. Sick et al (3) outlined a 3-pronged approach: remove 0.5 to 1.0 cm of horn from the apex of the toe to facilitate drainage; administer systemic antimicrobials; and move the animals from abrasive flooring surfaces such as concrete. These 3 principles were followed in the current study. Also, the feet were debrided on routine follow-up examinations, and all cattle received a non-steroidal anti-inflammatory drug (NSAID) on day 8. However, the amount of time and effort expended on making a diagnosis and administering treatment was not typical of what occurs in most feedlots. In large commercial feedlots a putative diagnosis of TTNS is based on observing a lower limb lameness involving a hind leg, no obvious swelling of the foot, and the onset of lameness occurring within weeks of arrival at the feedlot. These animals typically receive antimicrobial therapy and are then returned to their home pen. In some feedlots, the protocol would involve “tipping the toes” to facilitate drainage or may involve administering an NSAID.

Antimicrobial therapy may be effective in the early course of the disease before P3 involvement. However, if the treatment fails, then these animals are at risk of developing deep digital sepsis (DDS), which includes conditions such as osteomyelitis, arthritis, and tenosynovitis (16–19). Chronic septic arthritis of the distal interphalangeal joint as well as a septic tenosynovitis are largely non-responsive to systemic antibiotics alone because of local ischemia. Similarly, P3 necrosis usually requires either curettage of the necrotic bone or complete amputation of the digit. In the current study, bone curettage was not performed on any of the heifers; however, 2 animals had evidence of P3 remodeling, indicative of P3 osteolysis. Regional intravenous perfusion (RIVP) antimicrobial therapy may be considered for treating toe necrosis and DDS conditions (20–22); however, it is important to appreciate that RIVP alone is unlikely to result in a satisfactory outcome. Rather, the lesion must be debrided or the digit amputated. A randomized clinical study dedicated to treatment options and outcomes is needed to determine the most appropriate treatments for the various stages of TTNS.

While the recovery rate in the current investigation was relatively good, intensive individual animal care is logistically challenging in large commercial feedlots that lack proper handling systems for restraining animals for foot examination. Furthermore, most cases occur during the autumn months when North American feedlots are processing large numbers of incoming cattle (23). Complicating matters is that the degree of lameness associated with the early stages of the disease is often mild. Hence, these subtle cases may be overlooked, particularly if the animals are fractious. Confinement in chutes and pens during on-arrival processing also makes it more difficult to observe normal ambulatory behavior. The lack of obvious clinical signs early in the disease may result in feedlot personnel attributing the lameness to trauma or misclassifying the disease as early stage foot rot (3). For those animals misclassified as having foot rot, administering antimicrobial therapy may result in full recovery. As a result, TTNS may be underreported, which is salient because antimicrobial therapy may mask substandard facility design and management practices. If feedlots correctly identify TTNS cases, then they may be more likely to change the flooring or take additional care when handling fractious animals.

A consistent clinical finding encountered over the course of the study was the appearance of paint brush hemorrhages of the sole as well as double sole formation. In dairy heifers, under-run or double soles are invariably preceded by solar hemorrhage (24). In a recent study of Danish bull calves fed to slaughter, ~75% of animals had sole hemorrhages, with the odds increasing if the cattle were housed on slatted concrete versus deep litter straw, and in animals with a higher average daily weight gain (25). While the pathogenesis of double sole formation is not fully understood, fluid formation between dermal-epidermal interface is thought to result in separation of the sole from the underlying dermis. The fluid accumulation associated with the sole hemorrhage (bruising), as well as the inflammatory exudate from toe necrosis, likely led to the separation of the sole (epidermis) from the underlying dermis (corium), resulting in the growth of a new sole.

From a practical point of view, debriding the toes is a simple and relatively rapid diagnostic procedure for confirming toe tip necrosis. For example, heifer #5 had a minimal degree of white line separation; however, debriding revealed that 3 of 4 hind claws were affected. This animal was euthanized 7 d later because of an ascending necrosuppurative cellulitis, underscoring that TTNS is more than just localized toe necrosis. This case also confirms a previous report that the degree of white line separation and necrosis of the toe tip are not correlated to P3 osteolysis (7). The use of ultrasound and radiology to determine the extent of P3 involvement has been reviewed elsewhere (13).

None of the 20 heifers examined on day 1 tested positive for BVDV, which is interesting since Paetsch et al (15) found feedlot cattle with TTNS to be 4.4 times more likely to be transiently infected with BVDV compared to animals dying of all non-TTNS causes. Furthermore, few spirochetes were associated with the lesions, suggesting that they are not associated with TTNS development.

Sick et al (3) were the first to associate this disease with hyper-excitable cattle, which was likely a factor in the current investigation. No personnel ever walked amongst the cattle for fear of being physically injured. Even after 7 mo of confinement the animals became extremely agitated when handled. Conceivably, the pain associated with TTNS may have led to the cattle becoming irritable versus the hyper-excitability being a factor in TTNS formation. This, however, seems unlikely since most feet appeared normal at the time of slaughter. Based on the current understanding of the pathogenesis of the disease, it is logical that high-strung animals may be more likely to abrade the solar surfaces of their feet on coarse flooring. Hence, TTNS may be mitigated by modifying flooring, facility design, and handling practices. Change, however, is unlikely to occur until feedlot personnel and veterinarians gain a better appreciation of the incidence of the disease, which is contingent upon conducting a careful examination of the hind feet of lame feedlot cattle, particularly cattle that are < 30 d on feed.

Without a negative control group, it cannot be stated unequivocally that debridement and parenteral antimicrobial therapy influenced the successful outcome in 16 of the 21 animals. However, administration of antimicrobials, debridement or resection of P3, and moving the animals to earthen-floored pens seem logical. If claw amputation is required, then it is critical that all the claws, including the front feet, be inspected before amputation since multiple claws are commonly affected. Finding more than 1 claw affected also has implications with respect to animal welfare and the timing of euthanasia. Lameness is an animal welfare concern and it needs to be managed as such. Lame animals that are nonresponsive to treatment after 7 to 10 d need to be reassessed. Even in feedlot conditions, restraint of the animal and lifting the foot with a rope is a simple, albeit somewhat time-consuming technique for examining the hoof. Debriding all the necrotic sole allows for visualization and assessment of P3 involvement. A decision must then be made to debride the necrotic horn tissue, resect the necrotic bone, or opt for euthanasia. The use of pain control (NSAIDs) should always be considered. CVJ