An incidence of acute diffuse aseptic inflammation of the corium of the hoof in dairy cows

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VETERINARSKI ARHIV 70 (3), 121-128, 2000 An incidence of acute diffuse aseptic inflammation of the Toma` Zadnik*, Ivan Jazbec, and Matja` Mesari~ Clinic for Ruminants, Veterinary Faculty, University of Ljubljana, Ljubljana, Slovenia ZADNIK, T., I. JAZBEC, M. MESARI^: An incidence of acute diffuse aseptic inflammation of the. Vet. arhiv 70, 121-128, 2000. ABSTRACT Herd health and production related problems were monitored on a high yield farm with 385 Holstein-Friesian cows near Ljubljana, Slovenia in 1993. At the end of August an outbreak of acute aseptic inflammation of the corium of the hoof (N=33) and retention of urine in vagina (N=37) was detected and treated in cows at pasture. The incidence of the disease in the summer months (pasture) was statistically significantly (P<0.01) higher than in the winter months. The analysis of intake revealed that it was markedly high in proteins and low in fibre in the summer months. A statistically significant (P<0.001) difference was revealed between fat, protein and urea bulk milk contents. Therefore, we may associate the occurrence of acute aseptic inflammation of the corium (sole haemorrhages) and retention of urine in vagina with protein overload (lush grass) and/or an increased urea content and some other toxic substances in the organism of dairy cows. Key words: cow, laminitis, bovine digit, hoof, welfare, Slovenia Introduction Laminitis (acute diffuse aseptic inflammation of the corium of the hoof) is a metabolic disorder of the corium and germinal layer. The condition is characterized by the occurrence of excess fluid in the corium of the hoof, which may be more accurately described as excessively high blood circulation (hyperaemia), accompanied by excretion of blood or fluid from blood vessels (NILSSON, 1963; TAKAHASHI and YOUNG, 1981; MORTENSEN et al., 1986; TIUSSAINT, 1989; BOOSMAN, 1990; BLOWEY, 1993, 1995). The disease is often considered to be a herd problem * Contact address: Prof. Dr. Toma` Zadnik, Clinic for Ruminants, Veterinary Faculta, University of Ljubljana, Cesta v Mestni log 47, SL-1000 Ljubljana, Slovenia, Phone: 386 61 1779 214; Fax: 386 61 332 243 ISSN 0372-5480 Printed in Croatia 121

associated with environmental, management and nutritional risk factors (GREENOUGH, 1985; DAVID, 1989). Three forms of clinical laminitis in cattle are recognized: acute, subacute, and chronic. In all three forms the animals exhibit lameness. The onset of laminitis is most frequently observed a month before and two months after parturition (NILSSON, 1963; MACLEAN, 1965; PETERSE, 1978, 1986; NILSSON, 1982; TIUSSAINT, 1989; BOOSMAN, 1990). Our knowledge of the origin of laminitis is still very incomplete. The acute form of laminitis has been frequently established to coincide with acute coliform mastitis, udder oedema, retention of the foetal membranes with postpartum septic metritis, rumen overload and acetonemia, indeed, the occurrence of laminitis is closely related to all locations where the production of bacterial endotoxins is increased. It has been established that nutrition, physiological state and specific digital blood circulation may lead to the development of a more or less pronounced form of laminitis (PETERSE, 1980; TAKAHASHI and YOUNG, 1981; NILSSON, 1982; LIVESEY and FLEMING, 1984; MORTENSEN et al., 1986; TIUSSAINT, 1989; BOOSMAN, 1990; VERMUNT and LEACH, 1992; BERGSTEN, 1994). Daily ration high in proteins and/or carbohydrates (rumen overload) plays an important role in the aetiology of laminitis (TAKAHASHI and YOUNG, 1981; NILSSON, 1982; LIVESEY and FLEMING, 1984). Three factors are recognized as being responsible for the development of the disease: endotoxin, lactic acid, and histamine, which triggers an allergic reaction. These pathogenetical products which are released mainly from the rumen, resp. intestines infiltrate the tissue of the corium of the hoof. In the pathogenesis of laminitis, capillary thrombosis in the hoof corium and haemodynamic disturbances of the digit evoked by oedema in the corium are particularly thought to be a cause of laminitis. These processes were investigated by NILSSON (1963) and BOOSMAN (1990), while the local effect of endotoxin E. coli O111B4 bacteria in the corium of the hoof was studied by TAKAHASHI and YOUNG (1981) and MORTENSEN et al. (1986). They have established that endotoxin triggers a severe local Schwartzman reaction causing haemorrhagic and necrotic lesions. Materials and methods The present paper reviews the incidence of laminitis and results of a 1-year observational study of some milk parameters data evaluation on a high yield dairy farm in Slovenia. 122 Vet. arhiv 70 (3), 121-128, 2000

The study was conducted in 1993 on one herd of 385 Holstein- Friesian cows. In the winter months the cows were housed in stalls with deep straw bedding, and pastured 24 h in the summer months. Clinical signs of lameness and changes in the pododerm of the hoof were established by clinical examination of the digit. The incidence occurred at the end of August, mostly in cows 150±10 days after parturition. Bulk milk samples were analysed weekly for fat, protein and urea concentrations. The urea content in raw milk was measured photometrically with the Cobas Mira spectrophotometer. Proteins in milk were measured by Milkoscan. The obtained data and the disease incidence were statistically evaluated by the SPSS program (NIE et al., 1975). Fat, protein, and urea weekly concentrations were correlated with some reproduction indexes and retention of urine in vagina and laminitis incidence. Results and discussion There was a marked difference between the average winter ration and diet during the disease incidence in the summer with regard to milk parameters concentration. Table 1 shows that summer ration was high in proteins and energy and low in crude fibre content. Table 1. Evaluation of nutritional substances in ration for examined dairy cows Ration Kg DS (kg) CF (g) Energy (SU/kg) DP (g) Na (g) K (g) Winter * 41.9 17.13 3.413 10.546 1.644 35.3 256 During the incidence ** 50.2 17.70 2.760 11.840 2.760 56.9 205 * = maize and grass silage, hay, concentrates ** = summer/pasture, alfalfa hay, concentrates DS = dry substance; CF = crude fibre; SU = starch unit; DP = degradable proteins Vet. arhiv 70 (3), 121-128, 2000 123

We found a significant difference between fat, protein and urea content in weekly bulk milk samples with regard to winter, resp. nonwinter feeding regimen. Table 2. Average values of fat, protein and urea in bulk cow milk samples Perameter in bulk milk Winter (N=27) Summer (N=25) Fat (g/100 ml) 3.806±0.16 3.230±0.22* Protein (g/100 ml) 3.231±0.14 3.078±0.09* Urea (mmol/l) 3.801±0.19 7.373±0.43* * P<0.05 During the summer a higher incidence of retention urine in vagina, acute laminitis and reproduction disorders was established. The results are presented in Table 3. Table 3. Mean fat, protein and urea values in weekly bulk cow milk samples and reproduction indexes, and retention of urine in vagina and sole haemorrhages incidence Parameter Winter (N=27) Summer (N=25) P Fat in bulk milk (g/100 ml) 3.806 3.230 *** Protein in bulk milk (g/100 ml) 3.231 3.078 *** Urea in bulk milk (mmol/l) 3.801 7.373 *** Calving -firs AI (days) 64.42 65.34 0.7360 Calving - last AI (days) 94.22 97.05 0.6683 Number of AI 1.58 1.73 0.1762 Number of retention of urine in vagina 16 37 2 ** Number of acute laminitis (sole hemorrhages) 7 33 2 ** ** P<0.01; *** P<0.001 Despite a statistically insignificant difference between reproduction indexes, we are of the opinion that the data obtained during the summer demonstrated an association with higher urea content in the organism, respectively milk. Our assessment of the statistically significant higher incidence of laminitis and retention of urine in vagina is associated with protein overload (lush grass) and walking on hard roads, respectively higher urea content and coincidence of other toxins in the cows' organism. At the end of August 1993, an outbreak of laminitis was observed among cows at grass that was particularly lush. Thirty-three severe cases of lameness and a reduced milk production (2.5 l per cow daily) were recorded. Also detected were 37 cases of retention of urine in vagina, 124 Vet. arhiv 70 (3), 121-128, 2000

while urea concentration in bulk milk was above normal, between 7.21 and 9.33 mmol/l. According to our experience it should not exceed 5.5 mmol/l (^ADONI^-ŠPELI^ et al., 1994; ZADNIK, 1995). During this period fat and protein concentrations were, in comparison to other weeks of the year, the lowest (fats 3.12% - 3.43%; proteins 1.97% - 3.09%). In our opinion, the established diseases are closely related to nutritional regime; that is to say, the animals were at pasture during that period. In this period cows were supplemented with 4.0 kg alfalfa hay and concentrates with 18% crude proteins. We believe that laminitis, lower reproduction indexes and higher incidence of retention of urine in vagina resulted from a largely pasture diet (protein overload), respectively urea content increase in the system. Table 4. Frequency distribution of affected hoofs in examined dairy cows Haemorrhages of the sole Summer (N=33) Front foot (N=5) outer hoofs 1 inner hoofs 5 Hind foot (N=29) outer hoofs 44 inner hoofs 4 Total hoofs 54 N = number of cows Scandinavian researchers have also reported on distinct seasonal variations of protein levels in bulk milk samples (REFSDAL, 1984; ROPSTAD and REFSDAL, 1987). A relationship between increased urea content in blood and milk and the reproduction disorders was established by several authors (JORDAN and SWANSON, 1979a, 1979b; JORDAN et al., 1983; CARROL et al., 1987a; CARROL et al., 1987b; ^ADONI^-ŠPELI^ et al., 1994). Lush growing grass, and particularly young rye with its high protein and metabolizable energy content, has been considered important in the pathogenesis of laminitis (BOOSMAN, 1990; BLOWEY, 1993, 1995; BERGSTEN, 1994). NILSSON (1963) and MACLEAN (1971) have found that lush grass intake is high in protein and energy content, which may contribute to the occurrence of laminitis in cattle. In our case the affected animals were lame during walking. Because of high incidence, the outbreak was initially associated with some sort of infection (e.g. digital dermatitis, interdigital necrobacillosis) or injuries. Animals were lame, particularly in hind feet. Their gait was stiff and Vet. arhiv 70 (3), 121-128, 2000 125

tender, back arched and they tried to unload the most affected hoofs. While stationary, they shifted weight frequently. Walking caused a lot of pain. Examination of the hoofs revealed haemorrhages in the horn of the sole. In some cases the haemorrhages were very extensive, often undermining the complete sole. By trimming (removal of the surplus horn) red and partly congested tissue, fluid was excreted. Beneath those haemorrhages a growth of new horn came to the surface. After cleaning, the lesion was dressed with disinfectant (povidon iodine), packed with gauze, cotton wool, and a waterproof pressure bandage was applied. The animals received 5 ml Ahistin (difenhidramin-klorid) i/m injection for three days (twice daily). Cows were housed in straw yards and fed 4 kg of hay in addition to their daily ration. The dressing was checked after 5 days, and 14 to 21 days afterwards lameness was no longer evident. Our observations and the obtained results led us to conclusion that the outbreak of acute laminitis was closely associated with nutrition and with the transfer of cows from milking parlour to pasture. The cows walked to the milking parlour twice a day, covering 3 km on rough roads. Low concentrations of fats and proteins and high urea content in bulk milk samples also confirmed the incidence of acute laminitis. Acknowledgements We greatly appreciate the time and effort that has been contributed by all the people involved in this study, both in the laboratory and in the field. Special thanks are due to our colleague, Mag. Darko Veternik. The observation was made possible by the support of Mr. Bo`o Pirc at the Computer Center, Veterinary Faculty in Ljubljana. References BERGSTEN, C. (1994): Haemorrhages of the sole horn of dairy cows as a retrospective indicator of laminitis: an epidemiological study. Acta Vet. Scand. 35, 55-66. BLOWEY, R. W. (1993): Cattle Lamenees & Hoofcare. Farming Press Books. Ipswich. BLOWEY, R. W. (1995): Diseases of the bovine digit. Magyar Allatorvosok Lapja 10, 706-709. BOOSMAN, R. (1990): Bovine laminitis. Histopatological and arteiriographic aspects, and its relation to endotoxaemia. Dissertation. Faculty of Veterinary Medicine. University of Utrecht, The Netherlands. CAROLL, D. J., B. A. BARTON, G. W. ANDERSON, B. P. GRINDLE (1987a): Influence of dietary crude protein on urea-nitrogen and ammonia concentration of plasma, ruminal, and vaginal fluids of dairy cows. J. Dairy Sci. 70, Suppl. 1, 117. CARROLL, D. J., B. A. BARTON, G. W. ANDERSON (1987b): The influence of level of crude protein on the reproductive performance of the early lactation dairy cow. J Dairy Sci. 70, Suppl. 1, 264. ^ADONI^-ŠPELI^ V., D. VETERNIK, T. ZADNIK (1994): Protein and urea coefficients, effect on dairy cows, reproduction indexes in weekly bulk tank samples. Proceedings. XVIII World Buiatrics Congress. Bologna. pp. 1075-1079. 126 Vet. arhiv 70 (3), 121-128, 2000

DAVID, G. B. (1989): Epidemiological factors associated with a high incidence of sole ulcer and white line disease in dairy cattle. Prc. Soc. Vet. Epid. Prev. Med. Exeter, England, 149-158. GREENOUGH, P. R. (1985): The subclinical laminitis syndrome. Bov. Pract. 20, 144-149. JORDAN, E. R., T. E. CHAPMAN, D. W. HOLTAN, L. V. SWANSON (1983): Relationship of dietary crude protein to composition of uterine secretions and blood in high-productive postpartum dairy cows. J. Dairy Sci. 66, 1854-1862. JORDAN, E. R., L. V. SWANSON (1979a): Effect of crude protein on reproductive efficiency, serum total protein, and albumin in the high-producting dairy cow. J. Dairy Sci. 62, 58-63. JORDAN, E. R., L. V. SWANSON (1979b): Serum progesterone and luteinizing hormone in dairy cows fed varying levels of crude protein. J. Anim. Sci. 48, 1154-1158. LIVESEY, C. T., F. L. FLEMING (1984): Nutritional influence on laminitis, sole ulcer and bruised sole in Friesian cows. Vet. Rec. 114, 510-512. MACLEAN, C. W. (1965): Observations on acute laminitis of cattle in south Hampshire. Vet. Rec. 77, 662-672. MACLEAN, C. W. (1971): The long-term effects of laminitis in dairy cattle. Vet. Rec. 89, 34-37. MORTENSEN, K., M. HESSELHOLT, A. BASSE (1986): Pathogenesis of bovine laminitis (diffuse aseptic pododermatitis). Experimental models. Proc. of the 14 th World Congress on Diseases of Cattle. Dublin. pp. 1025-1030. NILSSON, S. A. (1963): Clinical morphological and experimental studies of laminitis in cattle. Acta Vet. Scand. (Suppl.) 4, 9-304. NILSSON, S. A. (1982): Laminitis in cattle. Etiology and metabolic problems. Rep. on the 4 th Symp. on Disorders of Ruminant Digit. Paris. NIE, N. H., C. H. HULL, G. J. JENKINS, K. STEINBRENNER, H. B. DALE (1975): Statistical package for the social sciences. 2. ed. McGrow-Hill. New York. PETERSE, D. J. (1978): Subclinical laminitis in the Netherlands. Rep. on the 24 th Symp. on Bovine Digital Disease. Skara. PETERSE, D. J. (1980): De beoordeling van de runderklauw op basis van optreden van zoollaesies. PhD Thesis. Rijks Universiteit. Utrecht. PETERSE, D. J. (1986): Lameness in cattle. Proc. of the 14 th World Congress on Diseases of Cattle. Dublin. pp. 1015-1024. REFSDAL, A. O. (1984): Urea in bulk milk as compared to the herd mean of urea blood. Acta Vet. Scand. 24, 518-520. ROPSTAD, E., A. O. REFSDAL (1987): Herd reproductive performance related to urea concentration in bulk milk. Acta Vet. Scand. 28, 55-63. TAKAHASHI, K., B. A. YOUNG (1981): Effects of grain overfeeding and histamine injection on physiological responses related to acute laminitis. Jpn. J. Vet. Sci. 43, 375-385. TIUSSAINT, R. E. (1989): Cattle footcare and claw trimming. Farming Press Book. London. VERMUNT, J. J., D. H. LEACH (1992): A macroscopic study of the vascular system of the bovine hind limb claw. New Zel. Vet. J. 5, 139-145. ZADNIK, T. (1995): Komparativno prou~evanje metaboli~nega in mle~no profilnega testa pri pre`vekovalcih v Sloveniji (A coparative investigation of metabolic and milk profile test from ruminants in Slovenia). Zaklju~no poro~ilo L4-5473-0406. Veterinarska Fakulteta. Ljubljana. pp. 1-94. Received: 22 September 1999 Accepted: 24 February 2000 Vet. arhiv 70 (3), 121-128, 2000 127

ZADNIK, T., I. JAZBEC, M. MESARI^: Pojavljivanje akutne difuzne asepti~ne upale korijuma papaka mlije~nih krava. Vet. arhiv 70, 121-128, 2000. SA@ETAK Zdravlje stada i proizvodnja mlijeka je promatrana na visoko produktivnoj farmi s 385 hol{tain-frizijskih krava pokraj Ljubljane u Sloveniji tijekom 1993. godine. Krajem kolovoza je izbila akutna asepti~na upala korijuma papaka (N=33) i zaostajanje mokra}e u rodnici (N=37) mlje~nih krava {to je lije~eno na pa{njaku. U~estalost pojave oboljenja u ljetnim mjesecima na pa{i je bila statisti~ki zna~ajno (P<0,01) vi{a nego u zimskim mjesecima. Analizom kori{tene hrane u ljetnim mjesecima je utvr eno da je sadr`avala uo~ljivo vi{e bjelan~evina i manje vlaknatih sastojaka nego u zimskim mjesecima. Statisti~ki zna~ajna (P<0,001) razlika izme u ljetnih i zimskih mjeseci, bila je utvr ena u koli~ini masti, bjelan~evina i mokra}evine u mlijeku istra`ivanih krava. Na osnovi navedenog, mo`emo povezati pojavu akutne asepti~ne upale korijuma (krvarenja u pap~anom potplatu) i zaostajanja mokra}e u rodnici s prevelikom koli~inom bjelan~evina u hrani (bujnom i so~nom travom) krava i/ili povi{enjem sadr`aja mokra}evine ili nekih drugih otrovnih tvari u organizmu mlje~nih krava. Klju~ne rije~i: krava, laminitis, gove i prst, papak, dobrobit, Slovenija 128 Vet. arhiv 70 (3), 121-128, 2000