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Epidemiology of Uncinaria stenocephala infections in greyhound breeding kennels
Veterinary Parasitology, 10 (1982) 317--321 Elsevier Scientific Publishing Company, Amsterdam -- Printed in The Netherlands
EPIDEMIOLOGY OF UNCINARIA STENOCEPHALA GREYHOUND BREEDING KENNELS*
317
I N F E C T I O N S IN
M.J. WALKER and D.E. JACOBS
Department of Microbiology and Parasitology, The Royal Veterinary College, University of London, Hatfield (Gt. Britain) (Accepted for publication 2 February 1982)
ABSTRACT Walker, M.J. and Jacobs, D.E., 1982. Epidemiology of Uncinaria stenocephala infections in greyhound breeding kennels. Vet. Parasitol., 10: 317--321. Field observations at breeding kennels in eastern England support the view that perinatal transmission is of minor importance in the epidemiology of Uncinaria stenocephala infections in greyhounds. Patent infections became established soon after weaned pups were put onto grass paddocks. Egg-counts rose to high levels, tending to peak in dogs 25--35 weeks old and to decline thereafter. This pattern was related to the age of the host and was not seasonal. The consequent deposition of large numbers of eggs onto the paddocks at irregular intervals distorted the seasonal fluctuations in herbage larval counts previously found to be a consistent feature of grass paddocks used for exercising adult racing greyhounds.
INTRODUCTION M u c h i n f o r m a t i o n has a c c u m u l a t e d o n the prevalence o f Uncinaria s t e n o c e p h a l a in British racing g r e y h o u n d s over 15 m o n t h s o f age ( J a c o b s and Prole, 1 9 7 6 ; Jacobs, 1 9 7 8 ; Walker, 1980). In o n e survey, t h e p r o p o r t i o n o f animals s h e d d i n g eggs varied f r o m 41.7% o f t h e 1 5 - - 2 4 m o n t h ageg r o u p t o 12.5% in t h o s e over 4 years old (Jacobs, 1978). It was also s h o w n t h a t whereas 17.4% o f t h e y o u n g e s t animals had egg-counts in excess o f 500 e.p.g., n o n e o f t h e dogs in t h e o l d e s t g r o u p e x h i b i t e d such high c o u n t s . Earlier w o r k has also s h o w n t h a t t h e grass p a d d o c k s c o m m o n l y used for exercising racing g r e y h o u n d s c o n s t i t u t e a m a j o r reservoir o f i n f e c t i o n . The n u m b e r s o f larvae in these sites u n d e r g o regular seasonal f l u c t u a t i o n s (Jacobs, 1 9 7 6 ; 1 9 7 8 ) w h i c h were s h o w n t o be d e t e r m i n e d b y differing rates o f dev e l o p m e n t and l o n g e v i t y o f t h e larvae t h r o u g h o u t the y e a r (Walker a n d Jacobs, 1 9 8 1 ) . *Paper presented at the 9th International Conference of the W.A.A.V.P., 13--17 July 1981, Budapest.
0304-4017/82/0000--0000/$02.75 © 1982 Elsevier Scientific Publishing Company
318 Little i n f o r m a t i o n is available regarding the dynamics o f infection in g r e y h o u n d s u n d er 15 m o n t h s o f age, i.e., before t h e y enter the large training kennels. This paper describes observations made at a fairly typical greyhound breeding establishment in the east of England. MATERIALS AND METHODS At any one time the kennels housed a b o u t ten breeding bitches, their litters and around 30 racing or retired greyhounds. Pups were born in a small whelping kennel with a concrete floor. A ft er weaning each litter was m o v e d o n t o a grass paddock. T he whelping kennel was t h o r o u g h l y scrubbed b e fo re use, b u t it was o f course impossible to clean the paddocks. The normal kennel r o u tin e at the time these observations were made was to dose the pups with piperazine adipate (Coopane, Wellcome; 100 mg/kg) at 4 weeks old and at weaning {approximately 6 weeks o f age). Milk was obtained from three bitches during the third and f o u r t h weeks o f lactation. Ten ml was collected from each o f t w o animals, but only 1 ml was recovered from the third. After dilution in physiological saline the samples were examined microscopically for the presence o f n e m a t o d e larvae. Faecal samples were obtained from unweaned pups for qualitative examination by washing the rectum with warm water. This procedure was necessary as nursing bitches devour the excreta o f their offspring. In the case o f t h e older animals, freshly deposited faeces were collected from the ground. Herbage samples were taken at a p p r o x i m a t e l y three-weekly intervals and examined by the m e t h o d o f Lancaster (1970). Six litters o f pups were m o n i t o r e d between S e p t e m b e r 1977 and Sept e m b e r 1979. RESULTS AND DISCUSSION No larvae were recovered from the milk samples. During the suckling period evidence o f infection with U. stenocephala was found in only one of the six litters. No firm conclusions can be drawn from these results per se in view o f the inadequacy of the sampling procedures. Nevertheless these data s u p p o r t the view that perinatal transmission from dam to offspring plays only a min o r role in the epidemiology o f U. stenocephala infections {Miller, 1971). In contrast, t r a n s m a m m a r y transmission occurs regularly in the case o f Ancylostoma caninum (Stone and Girardeau, 1968). Enigk and S t o y e (1967) r ep o r t finding a single U. stenocephala larva in the milk of a naturally infected bitch. After weaning, however, all litters rapidly acquired infection from the p a d d o c k with egg-counts rising to high levels. The general pattern of eggo u t p u t is shown in Fig. 1. Although there was m uch variation from litter t o litter, egg-counts t ended to peak at around 25--35 weeks of age. No clear sign o f the d e v e l o p m e n t of a protective i m m une response becom e apparent until the pups were 7--8 m o n t h s o f age. A similar trend was seen in litters
319 10 4
e.p.g.
103 .
500-
L3/kg
102 -
50
10
20 Age
30 40 (weeks).
50
6o
s
D
1977
H
1
1978
S
D
M
!
S
1979
Fig. 1. Mean faecal egg-counts for six litters of greyhound pups related to their age (U. stenocephala eggs per gram faeces +- SE). Fig. 2. Herbage larval counts from three exercising paddocks at greyhound breeding kennels (no. U. stenocephala infective larvae per kg wet weight). A, Paddock 1 ; . , Paddock 2 ; . , Paddock 3.
weaned in February, April, May, June and September, confirming that the pattern was related to age and was not seasonal. Egg-counts for t w o of these litters are shown in Fig. 3. Herbage larval counts on three paddocks are illustrated in Fig. 2, while Fig. 3 shows the relationship between the counts for one of these and the mean o f the faecal egg-counts of the dogs that it housed. The seasonal fluctuations described in racing greyhound training kennels, i.e., overwintered larvae disappearing in spring to be replaced by a new generation of larvae in the summer (Jacobs, 1976, 1978), are discernible, b u t the pattern is much less regular and varies in detail from paddock to paddock. In comparison with breeding kennels, the racing greyhound training kennels studied previously (loc. cir.) represented a very stable epidemiological situation. Each paddock was used by a wide variety of individual dogs, all of which were adult. Thirty per cent of these were shedding U. stenocephala eggs with e.p.g, values mostly in the low hundreds. Thus, the mean daily egg-output onto the herbage was a fairly constant factor throughout the year and the only variables governing larval numbers were climatic. In breeding kennels the epidemiological situation is more labile with large numbers o f eggs being deposited at irregular intervals. This produces distortions in the otherwise consistent pattern of herbage larval counts. In the case illustrated in Fig. 3, infective larvae on the herbage set up patent infections in the newly-weaned litter put onto the paddock in September 1977. Large numbers of eggs were excreted from December through to the following
320 I0000-
e.p.g
5000
I
II
i000
500
100 50-
0 500
S
D
M
f
J
S
D
M
L3/Kg
I0050-
,
~
..,..,/ ~
,.
D 1977
M
J S 1970
D
.... .,' ........
M J 1979
S
Fig. 3. Above: Mean faecal egg-counts (U. stenocephala eggs per gram faeces) for two litters of greyhound pups using Paddock 2. Below: Herbage larval count (no. U. stenocephala infective larvae per kg wet weight) for Paddock 2. Arrows indicate dates litters entered and left paddocks.
May when the pups were removed. These eggs, however, produced only a small rise in herbage larval numbers in June and July. Nevertheless, this was sufficient to ensure the establishment o f infection in the second newly-weaned litter which was turned onto the paddock in June 1978. Uncinaria stenocephala larvae are capable of rapid development even in early winter in the south of England and a new generation of larvae can appear in May or June (Walker and Jacobs, 1981). It seems likely, therefore, that the considerable numbers of eggs excreted by these pups from August onwards were responsible for the subsequent autumn, winter and spring peaks which were of a much greater magnitude than the " n o r m a l " summer peak of 1978. It is difficult to assess the clinical significance of the U. stenocephala infections in these dogs as t h e y also harboured large numbers of Toxocara canis during the first weeks of life and subsequently Toxascaris leonina and Trichuris vulpis. Uncinaria stenocephala is a non-haematophagous h o o k w o r m that produces a protein-losing enteropathy (Walker, 1980). The clinical impact in this case must, however, have been slight as, despite intermittent diarrhoea in all groups, most dogs appeared to grow satisfactorily and m a n y developed into successful racing animals.
321 ACKNOWLEDGEMENTS
This work was made possible by a grant from the Wellcome Trust. Mr. C. Donald provided technical assistance.
REFERENCES Enigk, K. and Stoye, M., 1967. Untersuchungen fiber den Infectionsweg yon Ancylostoma caninum Ercolani, 1859 (Ancylostomidae) beim Hund. Kongressbericht fiber die III Tagung der deutschen tropenmedizinischen Gesellschaft e.V., Hamburg, 20--27 April, 1967. Jacobs, D.E., 1976. Studies on the epidemiology of Uncinaria stenocephala infections in British greyhounds: seasonal availability of larvae on grass runs. Res. Vet. Sci., 21: 238--239. Jacobs, D.E., 1978. The epidemiology of hookworm infections of dogs in the UK. In: C.S.G. Grunsell and F.W.G. Hill (Editors), The Veterinary Annual Eighteenth Issue. Scientechnica, Bristol, pp. 220--224. Jacobs, D.E. and Prole, J.H.B., 1976. Helminth infections of British dogs: prevalence in racing greyhounds. Vet. Parasitol., 1: 377--387. Lancaster, M.B., 1970. The recovery of infective nematode larvae from herbage samples. J. Helminthol., 44: 219--230. Miller, T.A., 1971. Vaccination against the canine hookworm diseases. Adv. Parasitol., 9: 153--180. Stone, W.M. and Girardeau, M., 1968. Transmammary passage of Ancylostoma caninum larvae in dogs. J. Parasitol., 54: 426--429. Walker, M.J., 1980. Studies on the epidemiology and pathogenicity of Uncinaria stenocephala infections in British dogs. Ph.D. Thesis, University of London, 231 pp. Walker, M.J. and Jacobs, D.E., 1981. Studies on the epidemiology of Uncinaria stenocephala in British greyhounds: development and persistence of larvae on herbage. Res. Vet. Sci., 31: 264--265.
EPIDEMIOLOGY OF UNCINARIA STENOCEPHALA GREYHOUND BREEDING KENNELS*
317
I N F E C T I O N S IN
M.J. WALKER and D.E. JACOBS
Department of Microbiology and Parasitology, The Royal Veterinary College, University of London, Hatfield (Gt. Britain) (Accepted for publication 2 February 1982)
ABSTRACT Walker, M.J. and Jacobs, D.E., 1982. Epidemiology of Uncinaria stenocephala infections in greyhound breeding kennels. Vet. Parasitol., 10: 317--321. Field observations at breeding kennels in eastern England support the view that perinatal transmission is of minor importance in the epidemiology of Uncinaria stenocephala infections in greyhounds. Patent infections became established soon after weaned pups were put onto grass paddocks. Egg-counts rose to high levels, tending to peak in dogs 25--35 weeks old and to decline thereafter. This pattern was related to the age of the host and was not seasonal. The consequent deposition of large numbers of eggs onto the paddocks at irregular intervals distorted the seasonal fluctuations in herbage larval counts previously found to be a consistent feature of grass paddocks used for exercising adult racing greyhounds.
INTRODUCTION M u c h i n f o r m a t i o n has a c c u m u l a t e d o n the prevalence o f Uncinaria s t e n o c e p h a l a in British racing g r e y h o u n d s over 15 m o n t h s o f age ( J a c o b s and Prole, 1 9 7 6 ; Jacobs, 1 9 7 8 ; Walker, 1980). In o n e survey, t h e p r o p o r t i o n o f animals s h e d d i n g eggs varied f r o m 41.7% o f t h e 1 5 - - 2 4 m o n t h ageg r o u p t o 12.5% in t h o s e over 4 years old (Jacobs, 1978). It was also s h o w n t h a t whereas 17.4% o f t h e y o u n g e s t animals had egg-counts in excess o f 500 e.p.g., n o n e o f t h e dogs in t h e o l d e s t g r o u p e x h i b i t e d such high c o u n t s . Earlier w o r k has also s h o w n t h a t t h e grass p a d d o c k s c o m m o n l y used for exercising racing g r e y h o u n d s c o n s t i t u t e a m a j o r reservoir o f i n f e c t i o n . The n u m b e r s o f larvae in these sites u n d e r g o regular seasonal f l u c t u a t i o n s (Jacobs, 1 9 7 6 ; 1 9 7 8 ) w h i c h were s h o w n t o be d e t e r m i n e d b y differing rates o f dev e l o p m e n t and l o n g e v i t y o f t h e larvae t h r o u g h o u t the y e a r (Walker a n d Jacobs, 1 9 8 1 ) . *Paper presented at the 9th International Conference of the W.A.A.V.P., 13--17 July 1981, Budapest.
0304-4017/82/0000--0000/$02.75 © 1982 Elsevier Scientific Publishing Company
318 Little i n f o r m a t i o n is available regarding the dynamics o f infection in g r e y h o u n d s u n d er 15 m o n t h s o f age, i.e., before t h e y enter the large training kennels. This paper describes observations made at a fairly typical greyhound breeding establishment in the east of England. MATERIALS AND METHODS At any one time the kennels housed a b o u t ten breeding bitches, their litters and around 30 racing or retired greyhounds. Pups were born in a small whelping kennel with a concrete floor. A ft er weaning each litter was m o v e d o n t o a grass paddock. T he whelping kennel was t h o r o u g h l y scrubbed b e fo re use, b u t it was o f course impossible to clean the paddocks. The normal kennel r o u tin e at the time these observations were made was to dose the pups with piperazine adipate (Coopane, Wellcome; 100 mg/kg) at 4 weeks old and at weaning {approximately 6 weeks o f age). Milk was obtained from three bitches during the third and f o u r t h weeks o f lactation. Ten ml was collected from each o f t w o animals, but only 1 ml was recovered from the third. After dilution in physiological saline the samples were examined microscopically for the presence o f n e m a t o d e larvae. Faecal samples were obtained from unweaned pups for qualitative examination by washing the rectum with warm water. This procedure was necessary as nursing bitches devour the excreta o f their offspring. In the case o f t h e older animals, freshly deposited faeces were collected from the ground. Herbage samples were taken at a p p r o x i m a t e l y three-weekly intervals and examined by the m e t h o d o f Lancaster (1970). Six litters o f pups were m o n i t o r e d between S e p t e m b e r 1977 and Sept e m b e r 1979. RESULTS AND DISCUSSION No larvae were recovered from the milk samples. During the suckling period evidence o f infection with U. stenocephala was found in only one of the six litters. No firm conclusions can be drawn from these results per se in view o f the inadequacy of the sampling procedures. Nevertheless these data s u p p o r t the view that perinatal transmission from dam to offspring plays only a min o r role in the epidemiology o f U. stenocephala infections {Miller, 1971). In contrast, t r a n s m a m m a r y transmission occurs regularly in the case o f Ancylostoma caninum (Stone and Girardeau, 1968). Enigk and S t o y e (1967) r ep o r t finding a single U. stenocephala larva in the milk of a naturally infected bitch. After weaning, however, all litters rapidly acquired infection from the p a d d o c k with egg-counts rising to high levels. The general pattern of eggo u t p u t is shown in Fig. 1. Although there was m uch variation from litter t o litter, egg-counts t ended to peak at around 25--35 weeks of age. No clear sign o f the d e v e l o p m e n t of a protective i m m une response becom e apparent until the pups were 7--8 m o n t h s o f age. A similar trend was seen in litters
319 10 4
e.p.g.
103 .
500-
L3/kg
102 -
50
10
20 Age
30 40 (weeks).
50
6o
s
D
1977
H
1
1978
S
D
M
!
S
1979
Fig. 1. Mean faecal egg-counts for six litters of greyhound pups related to their age (U. stenocephala eggs per gram faeces +- SE). Fig. 2. Herbage larval counts from three exercising paddocks at greyhound breeding kennels (no. U. stenocephala infective larvae per kg wet weight). A, Paddock 1 ; . , Paddock 2 ; . , Paddock 3.
weaned in February, April, May, June and September, confirming that the pattern was related to age and was not seasonal. Egg-counts for t w o of these litters are shown in Fig. 3. Herbage larval counts on three paddocks are illustrated in Fig. 2, while Fig. 3 shows the relationship between the counts for one of these and the mean o f the faecal egg-counts of the dogs that it housed. The seasonal fluctuations described in racing greyhound training kennels, i.e., overwintered larvae disappearing in spring to be replaced by a new generation of larvae in the summer (Jacobs, 1976, 1978), are discernible, b u t the pattern is much less regular and varies in detail from paddock to paddock. In comparison with breeding kennels, the racing greyhound training kennels studied previously (loc. cir.) represented a very stable epidemiological situation. Each paddock was used by a wide variety of individual dogs, all of which were adult. Thirty per cent of these were shedding U. stenocephala eggs with e.p.g, values mostly in the low hundreds. Thus, the mean daily egg-output onto the herbage was a fairly constant factor throughout the year and the only variables governing larval numbers were climatic. In breeding kennels the epidemiological situation is more labile with large numbers o f eggs being deposited at irregular intervals. This produces distortions in the otherwise consistent pattern of herbage larval counts. In the case illustrated in Fig. 3, infective larvae on the herbage set up patent infections in the newly-weaned litter put onto the paddock in September 1977. Large numbers of eggs were excreted from December through to the following
320 I0000-
e.p.g
5000
I
II
i000
500
100 50-
0 500
S
D
M
f
J
S
D
M
L3/Kg
I0050-
,
~
..,..,/ ~
,.
D 1977
M
J S 1970
D
.... .,' ........
M J 1979
S
Fig. 3. Above: Mean faecal egg-counts (U. stenocephala eggs per gram faeces) for two litters of greyhound pups using Paddock 2. Below: Herbage larval count (no. U. stenocephala infective larvae per kg wet weight) for Paddock 2. Arrows indicate dates litters entered and left paddocks.
May when the pups were removed. These eggs, however, produced only a small rise in herbage larval numbers in June and July. Nevertheless, this was sufficient to ensure the establishment o f infection in the second newly-weaned litter which was turned onto the paddock in June 1978. Uncinaria stenocephala larvae are capable of rapid development even in early winter in the south of England and a new generation of larvae can appear in May or June (Walker and Jacobs, 1981). It seems likely, therefore, that the considerable numbers of eggs excreted by these pups from August onwards were responsible for the subsequent autumn, winter and spring peaks which were of a much greater magnitude than the " n o r m a l " summer peak of 1978. It is difficult to assess the clinical significance of the U. stenocephala infections in these dogs as t h e y also harboured large numbers of Toxocara canis during the first weeks of life and subsequently Toxascaris leonina and Trichuris vulpis. Uncinaria stenocephala is a non-haematophagous h o o k w o r m that produces a protein-losing enteropathy (Walker, 1980). The clinical impact in this case must, however, have been slight as, despite intermittent diarrhoea in all groups, most dogs appeared to grow satisfactorily and m a n y developed into successful racing animals.
321 ACKNOWLEDGEMENTS
This work was made possible by a grant from the Wellcome Trust. Mr. C. Donald provided technical assistance.
REFERENCES Enigk, K. and Stoye, M., 1967. Untersuchungen fiber den Infectionsweg yon Ancylostoma caninum Ercolani, 1859 (Ancylostomidae) beim Hund. Kongressbericht fiber die III Tagung der deutschen tropenmedizinischen Gesellschaft e.V., Hamburg, 20--27 April, 1967. Jacobs, D.E., 1976. Studies on the epidemiology of Uncinaria stenocephala infections in British greyhounds: seasonal availability of larvae on grass runs. Res. Vet. Sci., 21: 238--239. Jacobs, D.E., 1978. The epidemiology of hookworm infections of dogs in the UK. In: C.S.G. Grunsell and F.W.G. Hill (Editors), The Veterinary Annual Eighteenth Issue. Scientechnica, Bristol, pp. 220--224. Jacobs, D.E. and Prole, J.H.B., 1976. Helminth infections of British dogs: prevalence in racing greyhounds. Vet. Parasitol., 1: 377--387. Lancaster, M.B., 1970. The recovery of infective nematode larvae from herbage samples. J. Helminthol., 44: 219--230. Miller, T.A., 1971. Vaccination against the canine hookworm diseases. Adv. Parasitol., 9: 153--180. Stone, W.M. and Girardeau, M., 1968. Transmammary passage of Ancylostoma caninum larvae in dogs. J. Parasitol., 54: 426--429. Walker, M.J., 1980. Studies on the epidemiology and pathogenicity of Uncinaria stenocephala infections in British dogs. Ph.D. Thesis, University of London, 231 pp. Walker, M.J. and Jacobs, D.E., 1981. Studies on the epidemiology of Uncinaria stenocephala in British greyhounds: development and persistence of larvae on herbage. Res. Vet. Sci., 31: 264--265.