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Epidomiology of Rhodococcus equi infection in horses
yeterinaryMicrobioiogy, 14 (1987) 211-214 Elsevier Science Publishers B.V., Amsterdam - - Printed in The Netherlands
211
Epidemiology of Rhodococcus equi Infection in Horses J.F.P R E S C O T T
Department o/Veterinary Microbiologyand Immunology, Ontario VeterinaryCollege, Universityof Guelph, Guelph, Ontario N IG 2WI (Canada)
ABSTRACT
Prescott, J.F., 1987. Epidemiology of Rhodococcus equi infection in horses. Vet. Microbiol., 14: 211-214. Current understanding of the epidemiology of Rhodococcus equi infection on horse farms is reviewed. Infection is widespread in herbivores and their environment, because herbivore manure supplies the simple organic acid substrates on which the organism thrives. There is a progressive development of infection in the soil on horse farms with prolonged use, because: (1) there is a continual supply of nutrients; (2) the organism multiplies progressively as temperatures rise; (3) the bacterium has a robust nature. While this aerobic organism fails to multiply in the largely anaerobic intestine of the adult horse, multiplication to very large numbers may occur in the intestine of a foal in its first 8-12 weeks of life. Farms used for foal breeding over many years may thus become particularly dangerous for foals. Areas for future study include the effectiveness of decontamination, manure-removal programs and dust reduction in reducing challenge to susceptible foals.
Rhodococcus equi p n e u m o n i a o f foals occurs c h a r a c t e r i s t i c a l l y in foals aged 2 - 3 m o n t h s . T h e c h r o n i c n a t u r e of t h e i n f e c t i o n suggests t h a t t h e y are i n f e c t e d for weeks b e f o r e t h e disease is recognized. A c h a r a c t e r i s t i c o f t h e i n f e c t i o n is t h a t it causes e n d e m i c disease o n some farms, sporadic disease o n o t h e r s a n d is n o t r e c o g n i z e d o n most. T h e p e a k i n c i d e n c e o f t h e disease coincides r e m a r k ably w i t h t h e t i m e at w h i c h m a t e r n a l l y d e r i v e d a n t i b o d i e s have v i r t u a l l y disappeared. T h e r e h a v e b e e n several r e c e n t r e p o r t s using sensitive i m m u n o l o g i c a l tests for c e l l - m e d i a t e d a n d h u m o r a l i m m u n i t y (e.g., P r e s c o t t et al., 1980; H i e t a l a et al., 1985 ) t h a t s h o w t h e w i d e s p r e a d n a t u r e of i n f e c t i o n with R. equi in horses. M o s t h o r s e s e x p e r i e n c e i n f e c t i o n e a r l y in life, m a i n l y t h r o u g h t h e i n t e s t i n a l tract. T h e s e i m m u n o l o g i c a l findings r e i n f o r c e c o n c e p t s of t h e epidemiology of R. equi i n f e c t i o n b a s e d o n isolation o f t h e organism. T h e selective isolation m e d i u m d e v e l o p e d b y W o o l c o c k et al. (1979) was followed b y t h e isolation of R. equi f r o m t h e faeces a n d m a n u r e o f h e r b i v o r o u s a n i m a l s a n d pigs, as well as f r o m soil w h i c h h a d b e e n c o n t a m i n a t e d b y herbi0378-1135/87/$03.50
© 1987 Elsevier Science Publishers B.V.
212 vore manure. Infection has been shown to be widespread in grazing animals and their environment. Barton and Hughes {1984/1985) produced evidence that the organism is a soil organism, with the ability to multiply in herbivore manure kept under optimum conditions of temperature and moisture. Optim u m temperature of growth is 30 ° C. The organism behaves similarly to Rhodococcus coprophilus, another soil organism whose growth is stimulated by herbivore manure (Rowbotham and Cross, 1977). Hughes and Sulaiman (1987) reported in this workshop that the simple organic acids found in herbivore manure were an important nutrient source for R. equi. Prescott et al. (1984) showed that the number of R. equi on horse farms increased with the time that the farms had been used for horse breeding. On a farm used for 30 years, there were several thousand R. equi per gram of pasture soil, although this farm did not experience problems with the disease. A farm with endemic R. equi pneumonia differed significantly from four other farms, where disease was not endemic, in the number of R. equi isolated in the stable area, where the foals were, but not elsewhere. Serotyping studies (e.g., Nakazawa et al., 1983) have shown that differences between serotypes found on farms appear to reflect geographic differences rather than virulence differences. Several serotypes may occur on a farm. Nevertheless we need to know more about virulence differences of isolates. In the workshop Bowles et al. {1987) report differences in mouse virulence between lung isolates and soil isolates of R. equi. We need simple markers for such differences. These studies and others have thus shown that because of the ecological behaviour of R. equi, there is a progressive build up of infection on horse farms with prolonged use. This may become of significance if the build up is in the immediate environment of the foals, particularly if the environment is dusty, since disease largely follows inhalation rather than ingestion of the organism. Takai et al. (1987), in this workshop, report how the number of R. equi which could be isolated from the air increased as environmental numbers increased with increasing environmental temperatures and with increasing dryness and windiness of the environment. The pattern of progressive development of soil infection on farms, because of the presence of growth factors in herbivore manure and of the horses as a passive carrier of infection acquired from the environment is, however, an oversimplified model of what is happening. Takai et al. (1986) have shown that the greatest time of colonization of the intestine of horses with R. equi is in the first 8 weeks of life, suggesting that multiplication occurs within the foal intestine. In this workshop Hughes and Sulaiman (1987) suggested that the specific ability of R. equi to multiply in the foal, but not adult intestine resulted from the lack of full development of the anaerobic bowel flora typical of the adult. Rhodococcus equi does not multiply anaerobically and does not grow in the large bowel of the adult horse. Manipulating the colonic flora of the foal, for example by feeding a foal manure from an adult, might be one way to prevent the specific growth of R. equi in the foal intestine.
213
W e have a soilorganism with simple growth requirements which are met perfectly in the intestine of the foal.This explains why farms which are used to breed foals over m a n y years m a y become particularly dangerous to new foal crops, especiallyiffoal-derivedisolatesare more virulent than soilisolates. The practical significanceof these findings is that removal of manure from the environment of foals should prevent build up of infection.Control of dust is also important, but m a y be difficulton farms with heavy concentrations of horses where grass near buildings is eaten or worn bare. Magnusson (1938) achieved control of the disease on an endemic farm in Sweden by moving the foaling date forward, into March from May, and foaling mares on an uninfected farm. The work of Takai et al. (1987) reported in this workshop supports the value of such an approach, but m a n y breeders will not find itfeasible. The former approach m a y be one option some breeders could use. W e need studies to show: (1) how long heavily contaminated areas on endemic farms need to be rested before they are safe for horses; (2) what disinfection procedures will decontaminate the environment on endemic farms; (3) what the effectivenessof manure-removal programs is in reducing the burden of environmental infection;(4) what the effectof concreting and grassing in the environment of the foals is in prevention of disease; (5) what measures will effectivelyreduce dust in the foal environment; (6) whether simple nose masks can be designed to prevent inhalation of the organism on heavily contaminated, endemic farms; (7) whether we can manipulate the foal intestinal flora to prevent the specificmultiplication of R. equi which occurs. Control of R. equi pneumonia on endemic farms using existingknowledge of the ecology of the organism m a y be the least expensive and most practical approach to control of the disease. W e need studies to confirm the value of these approaches.
REFERENCES Barton, M.D. and Hughes, K.L., 1984/1985. Ecology of Rhodococcus equi. Vet. Microbiol., 9: 65-76. Bowles, P.M., Woolcock, J.B. and Mutimer, M.D., 1987. Experimental infection of mice with Rhodococcus equi: Differences in virulence between strains. Vet. Microbiol., 14: 259-268. Hietala, S.K., Ardans, A.A. and Sansome, A., 1985. Detection of Corynebacterium equi-specific antibody in horses by enzyme-linked immunosorbent assay. Am. J. Vet. Res., 46: 13-15. Hughes, K.L. and Sulaiman, I., 1987. The ecologyofRhodococcus equi and physicochemical influences on growth. Vet. Microbiol., 14: 241-250. Magnusson, H., 1938. Pyaemia in foals caused by Corynebacterium equi. Vet. Rec., 44: 1459-1468. Nakazawa, M., Kubo, M., Sugimoto, C. and Isayama, Y., 1983. Serogrouping ofRhodococcus equi. Microbiol. Jmmunol., 27: 837-846. Prescott, J.F., Ogilvie, T.H. and Markham. R.J.F., 1980. Lymphocyte immunostimulation in the diagnosis of Corynebacterium equi pneumonia of foals. Am. J. Vet. Res., 41: 2073-2075.
214 Pzeecott, J.F., Travem, M. and Yager-Johnson, J.A., 1984. Epidemiological suzvey of Corynebacterium equi infections on five Ontario horse farms. Can. J. Comp. Med., 48: 10-13. Rowbotham, T~I. and Cross, T., 1977. Ecology of Rhodococcus coprophilus and associated actinomycetes in fresh waters and agricultural habitats. J. Gen. Microbiol., 100: 231-240. Takai, S.,Ohkura, H., Watanabe, Y. and Tsuhaki, S., 1986. Quantitative~pects of Rhodococcu.s (Corynebacterium) equi in foals.J. Clin. Microbiol.,23: 794-796. Takai, S., Fujimori, T., Katsuzaki, K. and Tsubaki, S., 1987. Ecology of Rhodococcus equi in horses and theireavironment on horse-bzeedingfarms. Vet. Microbiol.,14: 233-239. Woolcock, J.B.,Farmer, A.-M.T. and Mutimer, M.D., 1979. Selectivemedium for Corynebacterium equi isolation.J. CIin.Microbiol.,9: 640-642.
211
Epidemiology of Rhodococcus equi Infection in Horses J.F.P R E S C O T T
Department o/Veterinary Microbiologyand Immunology, Ontario VeterinaryCollege, Universityof Guelph, Guelph, Ontario N IG 2WI (Canada)
ABSTRACT
Prescott, J.F., 1987. Epidemiology of Rhodococcus equi infection in horses. Vet. Microbiol., 14: 211-214. Current understanding of the epidemiology of Rhodococcus equi infection on horse farms is reviewed. Infection is widespread in herbivores and their environment, because herbivore manure supplies the simple organic acid substrates on which the organism thrives. There is a progressive development of infection in the soil on horse farms with prolonged use, because: (1) there is a continual supply of nutrients; (2) the organism multiplies progressively as temperatures rise; (3) the bacterium has a robust nature. While this aerobic organism fails to multiply in the largely anaerobic intestine of the adult horse, multiplication to very large numbers may occur in the intestine of a foal in its first 8-12 weeks of life. Farms used for foal breeding over many years may thus become particularly dangerous for foals. Areas for future study include the effectiveness of decontamination, manure-removal programs and dust reduction in reducing challenge to susceptible foals.
Rhodococcus equi p n e u m o n i a o f foals occurs c h a r a c t e r i s t i c a l l y in foals aged 2 - 3 m o n t h s . T h e c h r o n i c n a t u r e of t h e i n f e c t i o n suggests t h a t t h e y are i n f e c t e d for weeks b e f o r e t h e disease is recognized. A c h a r a c t e r i s t i c o f t h e i n f e c t i o n is t h a t it causes e n d e m i c disease o n some farms, sporadic disease o n o t h e r s a n d is n o t r e c o g n i z e d o n most. T h e p e a k i n c i d e n c e o f t h e disease coincides r e m a r k ably w i t h t h e t i m e at w h i c h m a t e r n a l l y d e r i v e d a n t i b o d i e s have v i r t u a l l y disappeared. T h e r e h a v e b e e n several r e c e n t r e p o r t s using sensitive i m m u n o l o g i c a l tests for c e l l - m e d i a t e d a n d h u m o r a l i m m u n i t y (e.g., P r e s c o t t et al., 1980; H i e t a l a et al., 1985 ) t h a t s h o w t h e w i d e s p r e a d n a t u r e of i n f e c t i o n with R. equi in horses. M o s t h o r s e s e x p e r i e n c e i n f e c t i o n e a r l y in life, m a i n l y t h r o u g h t h e i n t e s t i n a l tract. T h e s e i m m u n o l o g i c a l findings r e i n f o r c e c o n c e p t s of t h e epidemiology of R. equi i n f e c t i o n b a s e d o n isolation o f t h e organism. T h e selective isolation m e d i u m d e v e l o p e d b y W o o l c o c k et al. (1979) was followed b y t h e isolation of R. equi f r o m t h e faeces a n d m a n u r e o f h e r b i v o r o u s a n i m a l s a n d pigs, as well as f r o m soil w h i c h h a d b e e n c o n t a m i n a t e d b y herbi0378-1135/87/$03.50
© 1987 Elsevier Science Publishers B.V.
212 vore manure. Infection has been shown to be widespread in grazing animals and their environment. Barton and Hughes {1984/1985) produced evidence that the organism is a soil organism, with the ability to multiply in herbivore manure kept under optimum conditions of temperature and moisture. Optim u m temperature of growth is 30 ° C. The organism behaves similarly to Rhodococcus coprophilus, another soil organism whose growth is stimulated by herbivore manure (Rowbotham and Cross, 1977). Hughes and Sulaiman (1987) reported in this workshop that the simple organic acids found in herbivore manure were an important nutrient source for R. equi. Prescott et al. (1984) showed that the number of R. equi on horse farms increased with the time that the farms had been used for horse breeding. On a farm used for 30 years, there were several thousand R. equi per gram of pasture soil, although this farm did not experience problems with the disease. A farm with endemic R. equi pneumonia differed significantly from four other farms, where disease was not endemic, in the number of R. equi isolated in the stable area, where the foals were, but not elsewhere. Serotyping studies (e.g., Nakazawa et al., 1983) have shown that differences between serotypes found on farms appear to reflect geographic differences rather than virulence differences. Several serotypes may occur on a farm. Nevertheless we need to know more about virulence differences of isolates. In the workshop Bowles et al. {1987) report differences in mouse virulence between lung isolates and soil isolates of R. equi. We need simple markers for such differences. These studies and others have thus shown that because of the ecological behaviour of R. equi, there is a progressive build up of infection on horse farms with prolonged use. This may become of significance if the build up is in the immediate environment of the foals, particularly if the environment is dusty, since disease largely follows inhalation rather than ingestion of the organism. Takai et al. (1987), in this workshop, report how the number of R. equi which could be isolated from the air increased as environmental numbers increased with increasing environmental temperatures and with increasing dryness and windiness of the environment. The pattern of progressive development of soil infection on farms, because of the presence of growth factors in herbivore manure and of the horses as a passive carrier of infection acquired from the environment is, however, an oversimplified model of what is happening. Takai et al. (1986) have shown that the greatest time of colonization of the intestine of horses with R. equi is in the first 8 weeks of life, suggesting that multiplication occurs within the foal intestine. In this workshop Hughes and Sulaiman (1987) suggested that the specific ability of R. equi to multiply in the foal, but not adult intestine resulted from the lack of full development of the anaerobic bowel flora typical of the adult. Rhodococcus equi does not multiply anaerobically and does not grow in the large bowel of the adult horse. Manipulating the colonic flora of the foal, for example by feeding a foal manure from an adult, might be one way to prevent the specific growth of R. equi in the foal intestine.
213
W e have a soilorganism with simple growth requirements which are met perfectly in the intestine of the foal.This explains why farms which are used to breed foals over m a n y years m a y become particularly dangerous to new foal crops, especiallyiffoal-derivedisolatesare more virulent than soilisolates. The practical significanceof these findings is that removal of manure from the environment of foals should prevent build up of infection.Control of dust is also important, but m a y be difficulton farms with heavy concentrations of horses where grass near buildings is eaten or worn bare. Magnusson (1938) achieved control of the disease on an endemic farm in Sweden by moving the foaling date forward, into March from May, and foaling mares on an uninfected farm. The work of Takai et al. (1987) reported in this workshop supports the value of such an approach, but m a n y breeders will not find itfeasible. The former approach m a y be one option some breeders could use. W e need studies to show: (1) how long heavily contaminated areas on endemic farms need to be rested before they are safe for horses; (2) what disinfection procedures will decontaminate the environment on endemic farms; (3) what the effectivenessof manure-removal programs is in reducing the burden of environmental infection;(4) what the effectof concreting and grassing in the environment of the foals is in prevention of disease; (5) what measures will effectivelyreduce dust in the foal environment; (6) whether simple nose masks can be designed to prevent inhalation of the organism on heavily contaminated, endemic farms; (7) whether we can manipulate the foal intestinal flora to prevent the specificmultiplication of R. equi which occurs. Control of R. equi pneumonia on endemic farms using existingknowledge of the ecology of the organism m a y be the least expensive and most practical approach to control of the disease. W e need studies to confirm the value of these approaches.
REFERENCES Barton, M.D. and Hughes, K.L., 1984/1985. Ecology of Rhodococcus equi. Vet. Microbiol., 9: 65-76. Bowles, P.M., Woolcock, J.B. and Mutimer, M.D., 1987. Experimental infection of mice with Rhodococcus equi: Differences in virulence between strains. Vet. Microbiol., 14: 259-268. Hietala, S.K., Ardans, A.A. and Sansome, A., 1985. Detection of Corynebacterium equi-specific antibody in horses by enzyme-linked immunosorbent assay. Am. J. Vet. Res., 46: 13-15. Hughes, K.L. and Sulaiman, I., 1987. The ecologyofRhodococcus equi and physicochemical influences on growth. Vet. Microbiol., 14: 241-250. Magnusson, H., 1938. Pyaemia in foals caused by Corynebacterium equi. Vet. Rec., 44: 1459-1468. Nakazawa, M., Kubo, M., Sugimoto, C. and Isayama, Y., 1983. Serogrouping ofRhodococcus equi. Microbiol. Jmmunol., 27: 837-846. Prescott, J.F., Ogilvie, T.H. and Markham. R.J.F., 1980. Lymphocyte immunostimulation in the diagnosis of Corynebacterium equi pneumonia of foals. Am. J. Vet. Res., 41: 2073-2075.
214 Pzeecott, J.F., Travem, M. and Yager-Johnson, J.A., 1984. Epidemiological suzvey of Corynebacterium equi infections on five Ontario horse farms. Can. J. Comp. Med., 48: 10-13. Rowbotham, T~I. and Cross, T., 1977. Ecology of Rhodococcus coprophilus and associated actinomycetes in fresh waters and agricultural habitats. J. Gen. Microbiol., 100: 231-240. Takai, S.,Ohkura, H., Watanabe, Y. and Tsuhaki, S., 1986. Quantitative~pects of Rhodococcu.s (Corynebacterium) equi in foals.J. Clin. Microbiol.,23: 794-796. Takai, S., Fujimori, T., Katsuzaki, K. and Tsubaki, S., 1987. Ecology of Rhodococcus equi in horses and theireavironment on horse-bzeedingfarms. Vet. Microbiol.,14: 233-239. Woolcock, J.B.,Farmer, A.-M.T. and Mutimer, M.D., 1979. Selectivemedium for Corynebacterium equi isolation.J. CIin.Microbiol.,9: 640-642.