Veterinary Parasitology, 44 ( 1 9 9 2 ) 111-118 Elsevier Science Publishers B.V., A m s t e r d a m
Preventive treatment against toxocarosis in bovine calves J.A. Roberts Faculty of Veterinary Medicine and Animal Science, University of Peradeniya, Peradeniya, Sri Lanka (Accepted 27 January 1982)
ABSTRACT Roberts, J.A., 1992. Preventive treatment against toxocarosis in bovine calves. Vet. Parasitol., 44: 111-118. Treatment of bovine calves 10-16 days old with an anthelmintic which is effective against immature Toxocara vitulorum killed the parasites, there was no new infection and recontamination of the environment was precluded. When the management of the program was delegated to the livestock officers, approximately 3% of calves scheduled for treatment developed patent infections. The prevalences of toxocarosis on the different farms were correlated with annual rainfall, probably because the longer dry periods associated with lower rainfall killed infective eggs in the environment. The treatment schedules prevailing before the study commenced were ineffective. The prevalence of toxocarosis in the bovine calves on farms in the area with an annual rainfall of about 1000 m m was lower than that in buffalo calves studied previously in the same area.
Infections with Toxocara vitulorum in buffalo calves (Bubalus bubalis) were eliminated by treating calves 10-16 days old with an anthelmintic which is effective against immature parasites because infection from the maternal host did not occur beyond 10 days after parturition (Roberts, 1989a). Subsequently it was shown that the transmission of larvae through the milk of the mother ceased before the calf was 10 days old (Roberts et al., 1990 ). Larvae named as T. vitulorum by the authors have been collected from buffalo milk up to 24 days after parturition (Chauhan et al., 1974; Hossain et al., 1980; Baruah et al., 1981 ), but the descriptions do not correspond with that of larvae collected from milk, which had been radiolabelled when hatched in vitro from infective eggs, then used to infect the host (Roberts, 1990a). However larvae which do correspond to that description have been collected from the Correspondence to: J.A. Roberts, Yogyakarta A n i m a l Disease Investigation Centre, P O Box 79, Yogyakarta, Indonesia.
© 1992 Elsevier Science Publishers B.V. All rights reserved 0 3 0 4 - 4 0 1 7 / 9 2 / $ 0 5 . 0 0
milk of Bos taurus cows up to 18 days after parturition (Warren, 1971 ), so the duration of transmission from the cow to the calf may be longer for cattle than for buffalo. Thus, it is desirable to determine whether the treatment protocol for buffalo calves should be modified to protect calves of Bos spp. against toxocarosis. The present study describes the prevalence oftoxocarosis in Bos spp. herds in different environments and assesses, in bovine calves, the treatment schedule devised for buffalo calves. The prevalence of toxocarosis in some of the cattle herds is compared with that from the earlier study of buffalo herds in the same region (Roberts, 1989a). MATERIALS AND METHODS
Cattle herds Ten farms controlled by the National Livestock Development Board, Sri Lanka, were used in the study. All farms had Bos indicus milking cows which were either Gir, Sahiwal or crosses with local cattle. In addition, two farms had some infusion of Bos taurus through the use of Australian Milking Zebu bulls, and one had a herd of Killari cows which were not milked and which had exclusive use of a separate pasture (Table 1 ). All milking cows on each farm were run in one herd. The dry cows from milking herds were run separately, but used the same pastures as the milking cows. Cows with calves were brought to the milking sheds 5-8 days after calving and, thereafter, the calves were kept separate, except at milking time when they were used to stimulate milk let-down and suckled on at least one quarter of the udder. Calf births were recorded by the herdsman during his daily inspection of the dry herd and the calves were identified with an ear tattoo when brought to the milking shed.
Climate o f the farms The climate data are from the Land and Water Use Division of the Department of Agriculture, Sri Lanka. All of the farms were in the low country (below 100 m above mean sea level) with monthly average daily maximum temperatures ranging from 29 to 34°C and minima from 19 to 25 ° C. The rainfalls ranged from 730 to 1620 m m year- 1and are listed in Table 1. All of the farms received at least 500 m m of rain during the NE monsoon season from October to January. However, during the SW monsoon season from May to July, the farm with the highest rainfall received 570 mm, while that with the lowest rainfall received only 25 m m and the other farms received intermediate rainfalls. Consequently, low rainfall was associated with a prolonged dry period.
B. indicus B. indicus B. indicus
Rukkattana Martin Marandawila
~Number of calves examined. 2AMZ, Australian Milking Zebu.
AMZ 2 cross
Species/breed of cow
960 910 890
Annual rainfall (mm)
Once 208O Once 1217 None 12-40 Once 2849 Occasional None Occasional
Piperazine/ levamisole Piperazine/ levamisole
0 ( 16 )
16 (25) 80 (20) 9 (23)
50 (8) No data 24 (17)
60 ( 10 ) ~ No data No data No data 12 (8)
Schedule (days of age)
(29) (20) (34) (23) (74)
Not done Not done Not done
49 (23) 11 ( 18 ) 19 (36)
55 40 47 49 31
Only infected calves treated
(2o) 0 (16)
48 (31) 11 (18) 21 (53)
The situation on the farms before the treatment trials commenced. The treatment schedules, and the prevalences of infection under those schedules, are shown together with the prevalences of infection when only calves with patent infections were treated
Experimental procedure The prevalence of toxocarosis on each farm was determined on two occasions by counting the eggs in faecal samples from all calves 28-56 days old using the McMaster technique (Whitlock, 1948 ). Information on anthelmintic treatment schedules that were being followed by farm livestock officers was recorded at the same time. After the first assessment, three farms (Welikanda, Parasangahawewa and Oya Maduwa) were eliminated from the study because the prevalence of infection was low. The prevalence of toxocarosis was determined on the selected farms by treating only those calves confirmed as infected. While the prevalence was being determined, faecal samples were examined from all calves 17-42 days old each week until they became positive, in which case they were treated. Calves not becoming positive within 42 days were recorded as uninfected. Once the prevalence had been determined, three farms with a high prevalence and good management (Siringapatha, Koulwewa and Andigama) were selected to assess the pyrantel treatment schedule. These farms were visited on the same day of each week and on that day all calves 10-16 days old were treated with 250 mg ofpyrantel in the form of pyrantel tartrate and had an ear-tag applied. The efficacy of the treatment was assessed by examining faecal samples taken from the calves 35 and 49 days after treatment. When the appropriate treatment schedule was established, administration of the program was passed to the respective livestock officers. The instruction was to treat all calves aged 10-16 days old on a set day of every week. The efficacy of the schedule when managed by the livestock officers was then checked by examining faecal samples from all calves aged 3-8 weeks on a regular day each month.
Stat&tical analysis The correlation coefficient was calculated by the least squares method, without transforming the data. RESULTS
Prevalence of toxocarosis before the treatment trials The prevalences of toxocarosis with the treatment schedules operating before the trial commenced, and when treatment was only administered to individual animals in which infection had been confirmed, are listed in Table 1. The highest prevalence was in the Killari herd which was not milked. The prevalences of mature infections in the calves in the milking herds on the farms were positively correlated with annual rainfall (R = 0.73, P < 0.05 ). The
TOXOCAROSIS IN BOVINE CALVES
Killari herd was not included in the analysis because the high prevalence in that herd was attributed to the different husbandry procedure. Experimental treatment The treatment of 242 calves with 250 mg pyrantel at 10-16 days of age was supervised and no infections were detected on the three farms. On the basis of the prevalences before the pyrantel treatments commenced, 109 of the calves would have been infected before treatment. However, when treatment was delegated to the livestock officers, six calves of 203 treated developed patent infections. In three of those calves, the infection was detected less than the m i n i m u m pre-patent period of 18 days (Roberts, 1990b) after the anthelmintic was scheduled for administration. The other three failures were detected more than 22 days after the anthelmintic was scheduled for administration. The calves which developed infections were 12, 13, 14, 14, 15 and 16 days old on the scheduled treatment day. DISCUSSION
The study demonstrates that treatment of bovine calves 10-16 days old with an anthelmintic which kills immature T. vitulorum precludes patent infections, as did the same schedule in buffalo calves (Roberts, 1989a). In the buffalo calves, the time for treatment corresponded with the duration of the presence of larvae in the milk (Roberts et al., 1990); however, larvae have been observed in bovine milk for up to 18 days, although 90% of the larvae in bovine milk had been detected by 11 days (Warren, 1971 ), so their presence beyond that time may not be significant. Toxocara vitulorum larvae first develop in the maternal host, where some have persisted for more than 2 years (Roberts, 1992 ). Late in pregnancy some of the larvae were reactivated, migrated to the m a m m a r y gland and infection of the calves occurred exclusively through the milk (Roberts, 1990a). The infection matures in the calf. Climate affected the development and survival of infective eggs in the environment (Roberts, 1989b) and so would be an important determinant of the number of infective eggs available to infect the cows. When the larvae infect the cow, they are sequestered in the liver and lungs (Roberts, 1990a), where they are presumably unaffected by the prevailing weather conditions. The prevalence of mature infections in calves, and the levels of infection in individual calves, would then be determined by the levels of infection acquired by the cows over a prolonged period before calving and so would be largely independent of the season of birth. All of the farms had substantial rainfall during the NE monsoon season and much of the difference in rainfalls between the farms was attributable to the amount of rain received during the SW monsoon season. Consequently, the farms with
lower rainfalls had longer dry seasons. A prolonged dry period killed T. vitulorum eggs in the environment (Roberts, 1989b), so that is probably the factor reducing the prevalences of infection in areas of lower rainfall. Husbandry procedures could also have affected the prevalence oftoxocarosis and the level of infection, particularly those procedures which determine the access of cows to areas contaminated by calves with patent infections and those which determine the proportion of the mother's milk consumed by the calf. In the dry climate zone, where the milking herds had low prevalences of infection, the Killari herd (in which the calves were never separated from their mothers) had the highest prevalence of toxocarosis of all the herds. It is likely that the high prevalence resulted from the higher probability that the cows became infected because the calves ran with them. Additionally, those calves received all of the milk produced by their respective dams and so had more opportunity to develop higher levels of mature infections. The treatment schedules being used when the study commenced did not affect the prevalences oftoxocarosis on the farms, as shown by comparing the prevalences when the study commenced with those which occurred when regular treatment was suspended (Table 1 ). This is not surprising since piperazine is not effective against immature T. vitulorum and febantel is unreliable (Roberts, 1989a). Moreover, treatments with levamisole, which is effective against immature parasites, will still allow further contamination of the environment if given after the infection becomes patent, when the calf is about 21 days old (Roberts, 1989a). Consequently, inefficient use of anthelmintics has little effect on the prevalence of toxocarosis, although it is possible that environmental contamination will build up to a higher level in the absence of any treatment. That would be less significant in the drier areas, where the annual prolonged period of moisture deficit would be restricting the build-up of environmental contamination. In spite of the relative failure of the treatment schedules prevailing at the c o m m e n c e m e n t of the study, the new simple schedule was implemented with a high level of efficacy by the same livestock officers. Three of the six breakdowns occurred within the m i n i m u m pre-patent period of 18 days for T. vitulorum (Roberts, 1990b), so it is likely that they were due to failure to administer the anthelmintic. It is not possible to determine the reason for the other failures because the efficacy of the treatment schedule was only checked once per month. However, it is unlikely that any failures were due to transmission of larvae in the milk of the cows beyond 10 days after parturition because there were no failures in calves treated when l0 or 11 days old, either under supervision or by the livestock officers. The occurrence of failures once supervision of the treatment schedule ceased emphasises the need for careful record keeping, and for keeping to a regular treatment day each week (Roberts, 1990c). The prevalences of infection in buffalo herds in the greater than 950 m m rainfall zone was above 90% (Roberts, 1989a), compared with up to 51% for
TOXOCAROSIS IN BOVINE CALVES
bovine milking herds in the present study. The husbandry procedures used for the two species were comparable, except that the buffalo wallowed each day. The predilection of buffalo for water, and the survival of T. vitulorum eggs in water (Roberts, 1989b), may have led to higher levels of infection of the buffalo cows, which would then have caused higher levels and prevalences of infection with mature parasites in their calves by milk transmission. It has been suggested that buffalo are more susceptible to toxocarosis than cattle (Das and Singh, 1955; Patnaik and Pande, 1963; Chaudhry, 1978 ) and if that is correct it could explain the observed difference between prevalences. However, there are no data to support the contention and it is difficult to assess the relative susceptibilities of the two species because of their different behaviour traits. ACKNOWLEDGEMENTS
The hospitality and support of the Dean of the Faculty, Professor S.T. Fernando, is greatly appreciated. Mr. S.G. Wijeratna Banda provided careful technical assistance. The project is funded by the Australian Centre for International Agricultural Research. REFERENCES Baruah, P.K., Singh, R.P. and Bali, M.K., 1981. Relationship between presence of 3rd stage larvae of Neoascaris vitulorum and Strongyloides papillosus in colostrum/milk of buffaloes and appearance of eggs in the faecal samples of their calves. Indian. J. Dairy Sci., 34: 76-78. Chaudhry, N.I., 1978. Common disease problems in buffalo calves. Pak. J. Sci., 30: 120-126. Chauhan, P.P.S., Agrawal, R.D. and Ahluwalia, S.S., 1974. A note on the presence of Strongyloides papillosus and Neoascaris vitulorum larvae in the milk of buffaloes. Curt., Sci., 43: 486-487. Das, K.M. and Singh, G.B., 1955. Calf ascariasis in India. A nine years' survey with special reference to "Hetrazan". Br. Vet. J., 11 l: 342-347. Hossain, M.I., Dewan, M.L. and Baki, M.A., 1980. Preliminary studies on the efficacy of tetramisole hydrochloride (ICI) against transmammary migration of Toxocara (Neoascaris) vitulorum larvae in buffalo cows. Bangladesh J. Agric. Sci., 7: 25-28. Patnaik, M.M. and Pande, B.P., 1963., Notes on the helminthic infestations encountered in one month old buffalo calves. Indian Vet. J., 40:128-133. Roberts, J.A., 1989a. Toxocara vitulorum: treatment based on the duration of the infectivity of buffalo cows (Bubalus bubalis) for their calves. J. Vet. Pharmacol. Ther., 12: 5-13. Roberts, J.A., 1989b. The extraparasitic life cycle of Toxocara vitulorum in the village environment ofSri Lanka. Vet. Res. Commun., 13: 377-388. Roberts, J.A., 1990a. The life cycle of Toxocara vitulorum in Asian buffalo (Bubalus bubalis). Int. J. Parasitol., 20: 833-840. Roberts, J.A., 1990b. The egg production of Toxocara vitulorum in Asian buffalo (Bubalus bubalis). Vet. Parasitol., 37:113-120. Roberts, J.A., 1990c. Field trials of a single treatment for Toxocara vitulorum in Asian buffalo (Bubalus bubalis). Buffalo J., 6:113-123. Roberts, J.A., 1992. The persistence of larvae Toxocara vitulorum in Asian buffalo calves. Buffalo J., submitted.
Roberts, J.A., Fernando, S.T. and Sivanathan, S., 1990. Toxocara vitulorum in the milk of buffalo (Bubalus bubalis) cows. Res. Vet. Sci., 49: 289-291. Warren, E.G., 1971. Observations on the migration and development of Toxocara vitulorum in natural and experimental hosts. Int. J. Parasitol., 1: 85-99. Whitlock, H.V., 1948. Some modifications of the McMaster helminth egg-counting technique and apparatus. J. Counc. Sci. Ind. Res., 21: 177-180.