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Bovine laminitis: Clinical aspects,pathology and pathogenesiswith reference to acute equinelaminitisR. Boosman a , F. Németh a & E. Gruys ba Department of General and Large Animal Surgery,Faculty of Veterinary Medicine, University of Utrecht,Yalelaan 12, Utrecht, 3584 CM, The Netherlandsb Department of Veterinary Pathology, Faculty ofVeterinary Medicine, University of Utrecht, Yalelaan 1,Utrecht, 3584 CM, The NetherlandsPublished online: 01 Nov 2011.

To cite this article: R. Boosman , F. Nmeth & E. Gruys (1991) Bovine laminitis: Clinicalaspects, pathology and pathogenesis with reference to acute equine laminitis, VeterinaryQuarterly, 13:3, 163-171, DOI: 10.1080/01652176.1991.9694302

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REVIEW PAPERS

Bovine laminitis: clinical aspects, pathologyand pathogenesis with reference to acuteequine laminitis

R. Boosman', F. Németh' and E. Gruys2

SUMMARY. This review deals with the features of clinical and subclinical laminitis in cattle.Prominent clinical signs of acute laminitis are a tender gait and arched back. The sole hornreveals red and yellowish discolourations within five days. In subacute and chronic cases clinicalsigns are less severe. In chronic laminitis the shape of the claws is altered. Laminitis isfrequently followed by sole ulceration and white zone lesions.Blood tests showed no significant changes for laminitic animals. Arteriographic studies of clawsaffected by laminitis indicated that blood vessels had narrowed lumens. Gross pathologyrevealed congestion of the corium and rotation of the distal phalanx. Histopathologic studiesindicate that laminitis is associated with changes of the vasculature. Peripartum managementand nutrition are important factors in its aetiology. It is hypothesised that laminitis is evokedby disturbed digital circulation. In the pathogenesis of acute laminitis three factors areconsidered important: the occurrence of thrombosis, haemodynamic aspects of the corium,and endotoxins which trigger these pathologic events.

INTRODUCTION

Laminitis is defined as a diffnse aseptic inflammation of the corium of the clawof one or several digits, known to occur in hoofed animals (39). Its best-knownforms are acute laminitis, with its detrimental course in horses, and chroniclaminitis which is an important disease in dairy cattle.Laminitis as such may cause lameness in dairy cattle, but more important is itsrelation with the occurrence of sole ulceration and white zone lesions (28, 40).Digital disease, including sole ulceration and white zone lesions, is of greateconomic importance due to loss of milk production, decreased weight gain, andextra labour ( 1 1 ). The aetiology and pathogenesis of laminitis, sole ulceration,and white zone lesions are still not fully understood. Laminitis occurs as acomplication of severe diseases (e.g. metritis, mastitis, or carbohydrate overload)but is also found as a primary disease (39).Laminitis in cattle and horses is considered to have a comparable pathogenesis(41). In horses a laminitis model was developed in which horses or ponies wereoverloaded with a mixture of corn-starch (85%) and wood-cellulose flour (15%).A total of 17.6 g per kg body weight was administered as a gruel by stomach tube(17). The data for horses reported in this review have been compiled from studiesusing this laminitis model. In cattle such a model is not available.In the present paper, a review will be given of the various clinical signs, pathology,and aetiology of laminitis in dairy cattle. The pathogenesis of laminitis is discussedwith reference to acute laminitis in horses.

Department of General and Large Animal Surgery, Faculty of Veterinary Medicine, University ofUtrecht, Yalelaan 12, 3584 CM Utrecht, The Netherlands.

2 Department of Veterinary Pathology, Faculty of Veterinary Medicine, University of Utrecht,Yalelaan 1, 3584 CM Utrecht, The Netherlands.

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CLINICAL AND HAEMATOLOGIC CHANGES IN LAMINITIC ANIMALS

Acute laminitis

Cattle affected by acute laminitis generally have a stiff and tender gait, an archedback, and have the hind limbs, and some-times the front limbs also, placed wellunder the body. Hind lateral and front medial claws are more commonly affectedby laminitis than the other claws. In severe cases, cattle may therefore, stand cross-legged with their front limbs and with their hind limbs wide apart in order totake the pressure off of the most affected claws. Muscle fasciculations can benoticed occasionally. Animals may have difficulties in rising and prefer to remainlying. In the initial stages of the disease profuse sweating can occur. Appetite andmilk production are rarely reduced, except when systemic signs of other diseasesdominate. Distinct pulsation of the digital arteries and abnormal distension ofthe subcutaneous digital veins may be noticed (39).Cattle suffering from acutelaminitis regularly show increased pulse and respiratory rates proportional to theseverity of the disease. An elevated body temperature is not a common finding.Claws are warm to the touch. Examination of the claws, using percussor and hoof-tester, reveals an increased sensitivity (39). The mean arterial blood pressure ofanimals with acute laminitis was significantly lower than that of normal animals(39).None of the above-mentioned signs proved to be specific for laminitis. Measu-rements of haematocrit, haemoglobin concentrations, white blood cell counts anddifferential counts did not reveal any significant differences when compared withcontrol animals. Also, no changes in the serum concentrations of calcium,phosphorus, magnesium, sodium, and potassium were found (29, 39). Clinical andhaematologic findings in cattle affected by acute laminitis may often be outweighedby symptoms of other diseases.

Subacute laminitis

The term subacute laminitis is used for cattle only and refers to animals whichhave suffered from acute laminitis for more than 10 days. These animals exhibitmoderate to severe lameness (39). Toussaint Raven (59) used this term to describea mild laminitis with general stiffness and weight shifting. Subacute laminitis isto be considered as being intermediate between acute and chronic laminitis; it isusually less severe than acute laminitis and without changes in the claw form, asis seen in chronic laminitis.

Chronic laminitis

By definition, the type of laminitis which has persisted for more than 6 weeksis called chronic laminitis. Often the initial acute and subacute phases have notbeen observed, and the occurrence of laminitis is first noticed when claw changescharacteristic of chronic laminitis appear (39). Animals have a tender gait andmay be lame in one or more limbs, but mostly no lameness at all is seen. Theshape of the claw is invariably altered. Formations of ridges occur on the dorsalwall. These ridges diverge at the abaxial wall and heel area. The distance of theridges from the coronary margin gives an indication of the duration of laminitis.The shape of the dorsal margin is buckled and concave (59). The sole becomesflattened and broader than normal. Trimming the sole reveals haemorrhages and/or yellowish discolouration, especially in the white zone and the 'typical ulcerationsite'The horn of the sole may be softer than normal. Ablation/separation of the abaxialwall from the sole, in the white zone, is a frequent finding (39, 59). Due to hornovergrowth the lateral hind claws may be much higher and the sole more convexthan that of the medial hind claws.

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Subclinical laminitis

In dairy cattle not affected by clinical laminitis, paring of the sole 80-100 daysafter calving may reveal signs indicative of laminitis (increased incidence ofhaemorrhages, yellowish discolouration, and sole lesions). The term `subclinicallaminitis' has been introduced for this condition (45, 46). By definition, subclinicallaminitis does not manifest itself in perceptible lameness, but may be detected byclaw trimming. The distinction between subclinical and chronic laminitis is basedon ridges on the dorsal wall; when ridges on the dorsal wall are present, the termchronic laminitis is to be used (48, 49).Sole ulceration and white zone lesions have been related to laminitis. This hasbeen reported for acute laminitis (39), subacute laminitis (59), chronic laminitis(40, 30) and subclinical laminitis (45, 47). Sole ulcers and white zone lesions areoften preceded by haemorrhages (47). Ablation of the abaxial wall may progressand septic inflammation of the corium of the wall may occur, resulting in furtherseparation of the horn of the abaxial wall and/or the sole (59).

ARTERIOGRAPHY AND PATHOLOGY IN RELATION TO LAMINITIS

Arteriography

Maclean (28) studied (in vitro) arteriograms of laminitic and non-laminitic barleybeef animals (veal calves intensively fed with barley). The arteriograms of non-laminitic animals showed a regular, smooth, and evenly distended terminal archwith five clearly defined branches. The bulbar anastomoses were not clearlydefined. In animals affected by laminitis for two weeks or longer, both the terminalarch and its branches had a tortuous course. The most proximal branch was dilatedand the bulbar anastomoses were clearly defined. In dairy cattle, significantcorrelations were found between macroscopic signs of subclinical and chroniclaminitis and arteriographically defined narrowing of arteries in the claw (6). Indairy cattle affected by sole ulceration, a constriction in the terminal arch wasobserved where it emerged from the distal phalanx (study performed on amputatedclaws) (36).Furthermore, involvement of the vasculature in the pathogenesis oflaminitis has been described for horses affected by acute and chronic laminitis(I, 8).

Gross pathology

On a longitudinal section of the acute laminitic claw, congestion can be seen inthe corium of the toe area, of the wall halfway up to the coronary margin, andin the corium at the plantar/palmar edge of the distal phalanx. Five days laterhaemorrhages in the sole horn may become visible. Also, a rotation of the distalPhalanx may be seen, although never as marked as is known in horses (26, 27,39).In chronic laminitis congestion of the corium is less obvious than in the acutephase or not present at all. Foci with a dark brown red discolouration are oftenobserved in the horn of the sole and the wall. Also, a frequent yellowishdiscolouration of the sole horn is noticed. Rotation of the distal phalanx isfrequently found (4, 26, 39). The newly formed space between the dorsal wall andthe tip of the distal phalanx is filled with pale, soft, slightly yellow horn (26).Radiographic examination reveals widened vascular channels (29).

Histopathology

The histopathologic characteristics of the corium of non-laminitic claws involvesmall blood vessels in the perioplic and coronary corium (30). Some hyperaemiamay occur in the corium of the toe and sole area, especially near the Tuberculum

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flexorium of the distal phalanx (30, 39). A slight perivascular lymphocyteinfiltration is noticed. Histiocytes and plasma cells are observed occasionally. Mastcells and eosinophilic leucocytes are rarely seen (4, 30, 39). The cells of the Stratumbasale have a palisade arrangement along the basement membrane. The tonofibrils(formerly referred to as onychogenic substance (39)) appear as fine, closely packedfibrils in the middle third of the epidermal layer (30). No changes in the connectivetissue of the corium are reported.In acute laminitis, hyperaemia, oedema, and haemorrhages were seen in thecorium. Severe haemorrhages occurred in the solar corium at the toe and oppositeto the plantar/palmar edge of the distal phalanx. Thrombi were found in bothsmall and large arteries and veins (4, 30, 39). Round cell infiltration was moresevere than in non-laminitic feet. Lymphocytes predominated (30), but focalinfiltration of neutrophils was also observed (4, 39). No mast cells (30) or veryfew mast cells were found (39). Some globular leucocytes (degranulated mast cells)were observed (30). Cells of the Stratum basale in the lamellar and solar areaswere enlarged and disorganised. The tonofibrils from the Stratum spinosum inthe lamellar and solar areas disappeared partially or totally. In most cases,'acidophilic bodies' (or keratin bodies) were seen in the deeper parts of theepidermal lamellae, giving them a 'pearl necklace-like' appearance (30, 39). Nerveswere often surrounded by an oedematous perineurium (30, 39).In subacute laminitis, oedema, hyperaemia, haemorrhages, and thrombosis wereobserved as in acute laminitis. Thrombi had a hyaline character. In the caudalpart of the solar corium, 'neo-capillary formation' may have started (neocapillaryformation refers to newly formed, glomus-like vascular complexes) (39). Infiltra-tion with lymphocytes and histiocytes was more severe than in acute cases. Mastcells were observed more often in the solar and coronary corium than in acutecases (39). Epidermal changes were similar to changes in the acute cases, but wereoften more prominent (39). A moderate degree of sclerosis and occasionallynecrosis of the connective tissue was found (39).In the chronic phase the pathologic processes in the lamellar and especially thesolar corium were dominated by vascular changes. Hyperaemia and congestionwere present (30, 39). Recanalisation of thrombi was common and many newlyformed capillaries and 'neo-capillary formations' were present. Arterial intimalproliferation of smooth muscle cells and collagen deposits together with fragmen-tation and reduplication of the internal elastic membrane were common.Sometimes these changes resulted in total occlusion of the arterial lumen (4). Inarteries, hypertrophy of the cells of the Tunica media occurred, and the Tunicaadventitia was fibrotic (30). These changes were described as arterio(lo)sclerosis(4). Round cell infiltration was observed consistently, particularly in the solarcorium. Few (4, 30) or large numbers (39) of mast cells were found. Cells of theStratum basale appeared normal and had resumed their original, characteristicpalisade arrangement. In the epidermis of the sole, the tonofibrils were normalat the base of the epidermal papillae, but less intensely stained areas occurredmore exteriorly (30, 39). Perineuria were thickened and granulation and imma-ture fibrous tissue were present throughout the corium (39).

AETIOLOGY AND PATHOGENESIS OF LAMINITIS

Currently, there are two hypotheses on the aetiology and pathogenesis of laminitis,applying to both cattle and horses.Several authors stated that changes in the haemodynamics of the corium areprimary. The changes observed in the epidermal layers are considered secondaryto the disturbed microcirculation in the corium. This hypothesis is supported byclinical, pathologic, and histopathologic findings which indicate the involvement

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of the vascular system in the pathogenesis of acute laminitis, e.g. digital pulse,warm hooves, oedema, haemorrhages, congestion, perivascular white cell infil-tration, ischaemia, and thrombosis in the corium (2, 4, 8, 9, 30, 39).Obel (42) stated that changes in the epidermis are primary and the inflammatoryreaction and attendant oedema in the corium are secondary. Histologic studiesconfirmed irregular organisation of tonofibrils in hooves affected by acutelaminitis (42). Supportive evidence for this hypothesis was found in an in vitrostudy with tissue fragments of acute laminitic and non-laminitic hooves; animpaired incorporation of sulphur-amino acids was found in acute laminitichooves (25). Furthermore, in vitro studies of the incorporation of radioactive-labelled cystine in (13, 14), and specific binding of epidermal growth factor to,membranes of the matrix of hoof and claw have been conducted (15). These invitro studies on keratogenesis were propagated as an important tool in the studyof the aetiology of laminitis.

Aetiology

Epidemiologic studies revealed that numerous factors are involved in the aetiologyof bovine laminitis. The most important factors for acute laminitis are peripartumdiseases and malnutrition. Acute laminitis was seen in connection with mastitis(both Gram-negative and Gram-positive bacteria), acetonaemia, and (endo)me-tritis (27, 39). In addition, Toussaint Raven (59) associated udder oedema andretained foetal membranes with (sub)acute laminitis. Nutrition-related laminitisoccurs in cases of overeating of protein-rich or carbohydrate-rich rations, mostoften in association with severe systemic illness (7, 38, 39, 41, 56). Also, theconsumption of mouldy hay has been associated with laminitis (39).The following three factors were suggested as being important in triggering thechanges in the digits: (1) endotoxin released from inflammatory foci andendotoxaemia, (2) lactic acid in relation to ruminal acidosis, and (3) histamine,released in allergic reactions or absorbed from the gut.Besides the above-mentioned factors, the age of the animal, genetic predisposition,and housing are considered to influence the manifestation of laminitis. Chroniclaminitis is seen more often in older dairy cows (47, 59). The breed seems to beimportant; susceptibility to laminitis is found to be higher in Friesian-Holsteincows than in Holstein and Meusse-Rhein-IJssel cattle (47). For Jersey cattle aninherited form of laminitis has been reported; animals become laminitic at an ageof 3-6 months (34). Furthermore, the housing of cattle was considered to beimportant; unyielding concrete floors may predispose the animals to acutelaminitis (5, 40). The weight load on the claw is also of importance. Cattle exposedto long-lasting transit may show signs of acute laminitis (10). Overgrowth of thehind lateral claw attributable to laminitis may lead to overloading of this claw(43, 58, 61). Overloading is considered to play an important role in thepathogenesis of sole ulceration.

Pathogenesis

Thrombosis and disturbance of the haemodynamics in the digital circulation areconsidered to be the most important factors in the pathogenesis of acute bovineand equine laminitis. Vasoactive agents such as endotoxin are regarded as triggersof these pathologic events.

ThrombosisThrombosis is a prominent feature of the histology of bovine and equine laminitis(16, 32, 39). Whether thrombosis is caused by local or general coagulative activityis not clear.No data are available for cattle on the function of the haemostaticsystem during the development and acute clinical phases of laminitis.

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In the equine laminitis model the prothrombin time was not significantly changedduring the development phase of laminitis. The activated, partial thromboplastintime, platelet counts, and fibrin-degradation-product titre fluctuated, indicatingepisodes of clotting dysfunction. These episodes preceded lameness by one hour(21). Evidence of consumptive coagulopathy was found 6-12 hours after the onsetof lameness (33). Recent investigations revealed less dramatic changes of thehaemostatic system (50, 60). The concentration of protein C, a serum protein withanticoagulant and profibrinolytic properties, was increased (50).

Disturbance of the haemodynamicsDisturbance of the haemodynamics in the digits is considered to be importantin the pathogenesis of laminitis (8, 9, 20, 22). No data are available from in vivostudies in cattle on the haemo-dynamics in the digit during the development andacute phases of laminitis. In laminitic ponies (experimental) an increased digitalblood flow, increased arterial and venous pressure, and a decreased vascularresistance were found. Vascular responses to several mediators did not differ fromthose in healthy ponies (51, 52). Therefore, increased digital blood flow could notbe attributed to altered vascular responsiveness. No evidence for increasedcapillary permeability was found (52).During the development and acute phases of experimentally induced laminitis,using scintigraphy with radioactive albumin-technetium particles, a markeddecrease in regional blood volume and capillary perfusion occurred. A significantpositive correlation exists between arteriovenous shunting and the severity oflameness (20). Trout (60) measured an increased total blood flow toward thelamellar region in laminitic horses. Within the constraint of his study, he wasunable to distinguish between effective capillary flow and arteriovenous shuntflow.Arteriovenous shunts occur in large numbers in the corium of the equinehoof, especially in the coronary and lamellar region (53, 57).

EndotoxaemiaIt has been stated that toxins resorbed from the gut or inflammatory processescould play a pivotal role in the aetiology of laminitis. Endotoxin of Gram-negativebacteria has received particular attention because of its potency and toxicity. Acutelaminitis has been reported to occur in diseases accompanied by endotoxaemia,such as mastitis caused by Gram-negative bacteria (19), endometritis (44), andcarbohydrate overload (12). In cases of carbohydrate overload the large amountof starch causes an overgrowth of Gram-positive, lactate-producing bacteria inthe rumen of cattle or caecum of horses, resulting in a decrease in the ruminaland caecal pH (12, 31, 35). Subsequently, endotoxin is released from the cell wallsof dying and disintegrating Gram-negative bacteria. The acidity of the ruminaland caecal contents also causes damage to the epithelium of the rumen and mucosaof the caecum, allowing endotoxin to be absorbed more easily (23, 24).In cattle affected by acetonaemia the clearance of endotoxin from the circulationis decreased (3). Acetonaemia has been associated with the occurrence of acutelaminitis (39).

Local effects of endotoxinsMortensen et al. (37) tried to induce laminitic changes in the claw corium of calvesby injecting high doses of E.coli endotoxin into the digital artery of ligated digits,resulting in severe inflammatory changes. Repetition of this experiment, usingdoses of between 10 and 75 jig endotoxin given as a bolus injection into the digitalartery of the ligated lower limbs of dairy cattle, resulted neither in lameness norin histologic changes indicative of laminitis (Boosman, 1990 unpublished data).

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Plasma endotoxin concentrationsNo direct relationship between laminitis and endotoxaemia has been establishedin cattle. Sprouse et al. (55) demonstrated endotoxaemia in horses affected bylaminitis, induced by carbohydrate overload, using the quantitative chromogeniclimulus amoebocyte lysate (LAL) test. In an experiment with 20 horses, 13 animalsdeveloped Obel grade 3 laminitis (the horse moves most reluctantly and resistsattempts to lift a foot). Increases in plasma endotoxin from control levels of lessthan 0.1 pg/ml to values ranging from 2.4 to 81.53 pg/ml were measured in 11of the 13 horses during the onset of lameness (55).

Local Shwartzman reactionThe local Shwartzman reaction (LSR) is a haemorrhagic, necrotic lesion. Twenty-four hours after local sensitisation, a challenge is given by means of an intravenousinjection of endotoxin. Four to eight hours after the challenge an LSR develops,characterised by a recurrence of inflammation at the intradermal injection sitewith deposition of fibrin in or around blood vessels (18). Sprouse et al. (54)described the LSR in horses. Sensitisation was acquired by an intradermalendotoxin injection. A subsequent carbohydrate overload then functioned as achallenge for the LSR. Similarities between the histopathology of the skin regionsaffected by this LSR and of the corium of the hoof affected by acute laminitissuggest an LSR in the pathogenesis of laminitis (54).

DISCUSSION

Laminitis in cattle is manifested in various ways and to various extents. The timeof onset of each particular case is often hard to detect. Therefore, the aetiologyand pathogenesis of laminitis are difficult to study. Studies on claws affected bychronic laminitis revealed dyskeratosis and involvement of the vasculature in thepathogenesis of laminitis. The role of vascular lesions is not clear. For an exactanswer to this question, the influence of the age of the animal, the time of onset,exact localisation and the relation to the severity of laminitis must be investigatedin more detail.The equine laminitis model has provided valuable information on several clinicaland haematologic parameters in the development phase of acute laminitis. Studiesthat made use of this model have yielded three important clues to the laminitisresearch, namely: thrombosis, disturbed haemodynamics, and bacterial endotoxinas a trigger for these pathologic events. Intra-arterial administration of endotoxinin the bovine digit resulted in severe inflammation of the claw corium. However,neither clinical nor pathologic changes characteristic of laminitis were found.Therefore, if endotoxin is to play a role in the aetiology and/or pathogenesis oflaminitis, it is more likely to be an indirect effect of endotoxin on the claw corium.Disturbance of haemodynamics may be achieved by endotoxin, which in itselfhas vasoactive properties, but endotoxin also has the capacity to liberatevasoactive agents such as prostaglandins and vasoactive amines. Research onendotoxaemia in cattle may provide useful information on its role in thepathogenesis of laminitis. Furthermore, it may yield a laminitis model in dairycattle, which would greatly enhance the progress in cattle laminitis research.

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