ISRAEL JOURNAL OF VETERINARY MEDICINE OUTBREAKS OF DIGITAL DERMATITIS, INTERDIGITAL DERMATITIS AND HEEL EROSION ASSOCIATED WITH A NUTRITIONAL ETIOLOGY Bargai U. Koret School of Veterinary Medicine, Hebrew University, Jerusalem Summary Digital dermatitis is a worldwide disease of dairy cattle. The lesions are very painful and cause clinical lameness resulting in reduction of milk production and other economic losses. There is no agreement in the literature about the etiology of the disease which is named differently in various publications. Three outbreaks of digital dermatitis in dairy cattle which were circumstantially attributed to a sudden elevation of protein in the ration are reported. The case histories and the clinical and laboratory findings are fully described. The current nomenclature of digital dermatitis, interdigital dermatitis and heel erosion are discussed in view of the clinical findings. The mechanistic causation of digital dermatitis by a sudden elevation of dietary protein is proposed. Introduction Digital dermatitis is a skin disorder prevalent in dairy cattle, that has been reported in western countries, Asia and the Far East. The disease was described first in 1974 in Italy (1), and was defined as digital dermatitis due to the inflammation of the skin around the digit. Since then the various forms of the inflammation that occur in this condition have been given different names assuming them to be different disease entities (2, 3, 4). The etiology of the disease is not agreed yet; among the etiological agents reported in the literature are hereditary predisposition, wet soil conditions, and synergism between environmental opportunistic bacteria (5). Several bacteriological findings in the lesions have been described and were claimed to be the etiological agent of the disease. For example, spirochetes of the genus Treponema were identified in tissue sections (6,7,8). We present here descriptions of three separate outbreaks of the disease with a similar etiologic background associated with nutrition, a factor never previously reported as a causative agent in the condition. Outbreak A A herd of dairy cattle of about 300 milking cows belonged to a kibbutz (cooperative communal agricultural settlement) in the upper Galilee in Israel. The herd suffered for many months from digital dermatitis at a quite constant rate during most of the winter and spring months. The attending veterinarian had first tried systemic antibiotic treatment for individual sick cows. This was effective, but owing to the cost of treatment and the associated wastage of milk, topical antibiotic treatment was tried, and was as effective as the systemic treatment. Moreover, new cases appeared quite frequently. After many months of new cases, the veterinarian consulted with the Koret School of Veterinary Medicine. A herd study disclosed that there were about 30 cows with the disease. On visiting the herd, clinical examination revealed edema and reddish discoloration of the skin on the dorsal aspect and above the coronary band, edema and swelling of the digital cushions on several or all the legs, ulcerative dermatitis in the interdigital space and proliferating keratosis of various forms over many of the digital cushions (Figures 1,2,3). The hooves of several of the affected cows were examined for evidence of subclinical laminitis but without visible evidence. An investigation revealed that all the affected cows belonged to one specific shed and that all were primiparous. There were 90 cows in the shed, but none of the multiparous cows in the shed was affected. In accordance with good management, the pregnant heifers were kept until calving in a separate shed. The ration of the heifers contained 10% digestible protein and 1.8 Kcal metabolic energy /Kg of feed. The nutritional investigation revealed that there was an overnight change in the diet of the heifers housed in a separate shed. After parturition, the heifers were moved into the shed with the high producing cows where the ration contained 18% digestible protein and the same energy level. The digital dermatitis lesions on the legs of most of the heifers moved in with the high lactating cows appeared within 2-3 weeks. Blood samples were taken at random for biochemical examination from six affected cows. It was then recommended to have a transitional period of 2-3 weeks in which the pre-parturition diet of the heifers would be gradually changed to the lactating cows diet. As a result new cases of digital dermatitis ceased to appear. eel Horn Erosion with matitis of the digital break 1 Fig. 2. Heel Horn ulcerative dermatitis. Outbreak 1. Fig. 3. Proliferating keratitis of the digital cushion. Outbreak 1. Outbreak 2 Outbreak B A consultation was requested by the attending veterinarian of a village on the Golan Heights in northern Israel. Preliminary information revealed that there were 13 dairy farms in the village, and the digital dermatitis had appeared in four of them. On clinical examination of the affected cows the following lesions were found. Edema and reddish discoloration of the skin around the coronary band, swelling of the digital cushions of several of the legs, primarily the hind legs, ulcerative dermatitis on the digital cushions, ulcerative dermatitis in the interdigital space and proliferative dermatitis over the digital cushions (Figures 4, 5, 6). Several of the affected cows were examined for sub-clinical laminitis, but none was detected. Epidemiologic investigation revealed that the four herds involved were the only ones where the cows were given the full recommended ration supplied by the fodder center of the village. The other 11 herds received only part of the recommended ration and were given a supplement from other sources and not from the fodder center. An inquiry into the recommended ration supplied by the center revealed that it contained 24% digestible protein. The reason for the high level of the protein in the diet was that the nutritionist-adviser to the center maintained that cows should receive a high level of digestible protein for the first 2 months post-parturition. Blood samples were examined from 5 cows affected with the disease and resulted in the findings shown in Table 2. After reducing the protein level of the diet of the affected four herds to the accepted level of 17%, new cases ceased to appear. Fig. 5. Hyperkeratosis of the Digital Cushion. Outbreak 2. Fig. 6. Heel Horn erosion with Proliferating dermatitis. Outbreak 2. Outbreak C In a village in the Jezreel Valley with dozens of dairy herds, digital dermatitis appeared in only one herd. During the farm visit, the affected cows had the following clinical findings; ulcerative lesions in the skin above the coronary band, interdigital ulcerative bleeding lesions, swelling and ulcerative lesions on the digital cushions of several legs (Figs. 7, 8).There was an additional unique lesion on several of the affected cows with many focal discolored lesions and hemorrhages on the metatarsal and metacarpal skin (Fig. 9). An investigation of the nutrition of the herd revealed that the farmer had an agreement with a nearby biscuits and wafers factory to take away every few days its broken and reject products. The high energy, protein rich factory-waste product was fed to the cows as part of the whole ration and put into the trough. Normally, the quantity was small and regular, and there were no noticeable effects on the cows.About two weeks before the dermatitis lesions appeared, the amount taken from the factory amounted to a whole platform, weighing a few hundred kilos. The farmer was not aware of the risk in feeding large quantities of biscuits, and had given the cows large amounts on three successive days. At about two weeks, lesions on the skin of the lower legs had started to appear. The interdigital lesions and the hyperkeratosis on the digital cushions followed shortly after. The farmer was advised to reduce the amount of biscuits in the ration and feed them evenly. New cases did not appear. l ulcerative dermatitis 3. Fig. 8. Edema and Heel Horn Erosion . Outbreak 3. Fig. 9. Defuse Hemorrhages over the skin between the Tarsi and the fetlock Outbreak 3. Discussion On circumstantial evidence, the three outbreaks of digital dermatitis have one factor in common, the association of a sudden elevation of dietary protein with the appearance of digital dermatitis in the herds. In outbreak A, a sudden increase of protein from 10% to 18% without any transitional period in the heifer herd was introduced before parturition. The fact that the cases appeared mostly in winter and spring is related to this period when most of the parturitions occur. The parturient calvers were mixed with the group of high producing cows and were given a sudden change in the protein concentration. In outbreak B, the very high level of dietary protein of the high-producing cows was apparent. In outbreak C also, a sudden increase in protein was important since biscuits and chocolate biscuits contain high protein levels (vanilla and milk products). In outbreaks A and B, blood samples were taken to support the clinical diagnosis. In both most of the samples were either outside or at the upper normal range. The laboratory findings indicated also high levels of blood albumin (Tables 1,2) In the third outbreak, no blood samples were collected since the nutritional event had occurred several weeks previously and there was no chance of finding biochemical evidence. The circumstantial evidence between the sudden increased protein level in the ration in outbreak A, the extremely high protein level in the diet in outbreak B, and the digital dermatitis which occurred in most of the cows, lead the author to suggest that the sudden increase in protein should be added to the list of etiological agents of digital dermatitis. It is well known in medicine that the skin is very reactive to nutritional changes. Every dermatology textbook defines urticaria as one of the first clinical sign of nutritional allergy to a new food, and protein products are among the major causes of urticaria. In cattle it was reported that the incidence of sole ulcer, which is a skin lesion in the foot, is increased when cows are given high levels of protein ( 10). The mechanism for formation of digital dermatitis by the sudden elevation of dietary protein has yet to be investigated, but the following hypothesis is suggested. The very high levels of protein in the diet result in abnormal levels of blood albumin. This results in elevated osmotic pressure of the blood which in turn increases serum transfer into the circulation, and is resolved in the body by tissue edema in the lowest tissues in the body. In cattle it occurs with two other well known clinical signs.The first is the acute udder edema following parturition in heifers when they start receiving high dietary protein levels, and the second is brisket edema which also appears post- parturition in many cows. The digits, and especially the heels may become edematous due to plasma escaping into the tissues. Severe tissue edema in the digital skin increases its susceptibility to injury, followed by the entrance of bacteria such as spirochetes from the manure,. This hypothetical mechanism can explain the reported findings of spirochetes in the tissues of the digital cushion. This hypothesis is well substantiated by the report that digital dermatitis could not be reproduced by merely spreading spirochetes over the skin of the lower digit (11). It was postulated in this experiment that tissue injury must take place before the spirochetes can gain entrance to the tissues. Digital dermatitis is a multi-factorial disease, and the description of these outbreaks suggests that extreme sudden elevated protein in the diet should be included in the etiological agents of digital dermatitis. Other interesting observations among the clinical findings of the three outbreaks, are the presence of all three forms of digital dermatitis, heel erosion, interdigital ulceration and digital cushion hyperkeratinization and papillomatosis, which appeared in each of the outbreaks, in the same herd and sometimes in the same cow. The question whether these are separate diseases or should be considered as one disease entity under the name digital dermatitis was a subject discussed at the 10th international symposium of diseases of the ruminants digit in Lucerne in 1998 ( 9 ). The findings reported here support strongly that all these features should be grouped under the original name digital dermatitis. It is therefore suggested that one alternative is to name all these clinical features as the digital skin disorders syndrome (D.S.D.S) as is done in many other multifactorial diseases. References 1. Cheli R., Mortellaro CM. 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Proceedings 10th International Symposium on Lameness in Ruminants. Lucern, Switzerland, 266-268 , 1998. 7. Reed DH. An invasive spirochete associated with interdigital papillomatosis of dairy cattle. Vet.Rec. 130: 59-60, 1992. 8. Blowey RW. Studies on the pathogenesis and control of digital dermatitis of the ruminant digit. Proceedings, 8th International Symposium on disorders of the Ruminant Digit, Banff, Canada, 168-173, 1994. 9) Bargai U. Digital dermatitis, interdigital dermatitis and heel erosion - are these separate diseases? Proceedings 10th International Symposium on Lameness in Ruminants, Lucern, Switzerland, p 265, 1998. 10. Manson FJ, Leaver JD. The influence of concentrate amount on the locomotion and clinical lameness in dairy cattle. Animal Prod 47, 185-190, 1988. 11. Zemljic N. Etiopathogenesis of dermatitis digitalis in cattle. Proc.23rd WBC Congress, Quebec City, Canada, p.10, 2004.