Zbl. Vet. Med. B, 22, 842-849 (1975) @ 1975 Verlag Paul Parey, Berlin und Hamburg ISSN 0044-4294/ASTM-Coden: ZVRBAZ

From the Veterinary Research Laboratory, Kabete, Kenya

Susceptibility of Boran Cattle to Experimental Infections with Anaplasma marginale and Babesia bigemina BY K.-F. LOHR,P. S. OTIENO and W. GACANGA With 2 tables (Received for publication March 19, 1971)

“Anaplasmosis is essentially a clinical disease of bovines (Bos taurus.) Allied species like zebu (Bos indicus), buffalo and antelope are considered susceptible to natural infection” (4.),and - beside bovines - zebu, buffalo and dromedary can be suffering from clinical anaplasmosis” (10). These quotations do not reveal clearly whether Bos indicus is less or equally susceptible as Bos taurus to anaplasma infection, but tend to give the impression that Bos indicus is less susceptible. This would agree with the claim of breeders in Africa that zebu and to some lesser extent their crosses with Bos taurus possess a high degree of resistance to anaplasmosis, but would disagree with observations and experimental findings in Peru claiming that Bos indicus is by no means more resistant against anaplasmosis than Bos taurus (14). Redwater (Babesia bigemina infection) is essentially a disease of cattle, Bos s p p (4). With regard to the susceptibility to this disease, HENNING does not differentiate between Bos indicus and Bos taurus but differentiates between cattle raised on infected veld and cattle imported from parts of the world where redwater does not exist. Other authors, however, found that some breeds of Bos indicus have a high degree of resistance against redwater (1,2,3,5,8). Boran cattle are a Bos indicus breed found in great numbers in the drier Northern Provinces of Kenya, in Somalia and Southern Ethiopia, and they are considered to possess a high degree of resistance to tick-borne diseases such as anaplasmosis and redwater. This breed has been crossed with Bos taurus breeds for many years in order to produce high yielding cattle of ostensibly European type with enhanced resistance to African environmental conditions including anaplasmosis and redwater. Yet death in pure bred Boran cattle is reported frequently by farmers due to anaplasmosis and occasionally due to redwater. There remains the uncertainty of opinion as to the degree of susceptibility of Boran cattle to infections with Anaplasma marginale and B. bigemina and the following experimental work was carried out to clarify this question.

Susceptibility of Boran Cattle to Experimental Infections

843

Material and Methods Fourteen Boran dams from the Mandera district in the arid North East of Kenya had been moved southwards to a holding ground near Isiolo where they gave birth to the 14 experimental calves. When these calves were 5 to 6 months old, they were weaned and brought to the Veterinary Farm at Kabete. Sera taken at this time from calves and their dams were negative and positive respectively to anaplasma and babesia antigens when tested by the indirect fluorescent antibody (IFA) and capillary tube agglutination (CA) tests (7, 9, 12). The 14 calves had been subjected to strict tick control by once or twice weekly dipping since birth and their sera had remained free from anaplasma and babesia antibodies during the entire period of observation until the time or' infection. The control group in the anaplasma challenge trial was 20 and in the babesia challenge trial 11 pure bred Ayrshire cattle, 18 to 24 months old and obtained from the Veterinary Farms at Ngong and Machakos. Nine out of the group of 20 animals had been used in a B. bigemina challenge trial 2 months before the anaplasma challenge trial. The sera of the 20 and 11 animals were free from anaplasma and babesia antibodies respectively. The 14 Boran animals were infected subcutaneously with 10 ml. of blood containing approximately 25 x 1O6 A . marginale parasitised erythrocytes. Two months later 12 of these animals received inoculates of 5 ml. of blood containing approximately 35 X lo5 B. bigemina parasites. The Ayrshire control groups were infected simultaneously with the Boran cattle and received the same infective inoculates. Thin blood smears were examined, temperatures recorded and packed cell volumes (PCV) determined thrice weekly during the first 2 weeks and daily during the ensuing critical period after A . marginale infection, and daily for the first 8 days and twice the following week after B. bigemina infection. Temperatures were taken between 8 and 9 a.m. before a physiological rise of body temperature could be expected. PVC's of blood from the jugular vein were determined with the aid of a haematocrit centrifuge. The prepatent period was assessed as the number of days between infection and the development of an anaplasma parasitaemia of 1 O / o or between infection and detection of the first B. bigemina parasite in a thin blood smear. I n the latter case an abortive examination was abandoned after 3 minutes. The parameters for treatment or otherwise were as follows: infections in the Boran cattle were allowed to develop fully without interference from treatment. In the Ayrshire cattle, anaplasma infections were treated when PCV's had dropped to approx. 15 O / o or when parasitaemias had risen to 55 O/o. Babesia infections were treated at the onset of haematuria or when P C V had dropped to approx. 15 O / o . In both types of infection treatment was not undertaken despite these parameters if punctate basophilia was apparent in thin blood smears (9). Treatment against anaplasmosis and redwater was carried out with 1000 mg. oxytetracycline on 3 or 4 consecutive days each and a single dose of 1.05 g. Berenil respectively. Infective blood inoculates were obtained from 2 splenectomised calves which had been infected with deep frozen stabilates of the following 2 strains: the A . mayginale strain was passaged for many years a t this laboratory and originated from the Veterinary Research Laboratory Onderstepoort, South Africa. The B. bigemina strain, referred to as H 184, was obtained from Dr. D. Brown, East African Veterinary Research Organization, Muguga. Finally, sera from 105 adult cattle of the Mandera district were screened in the CA-Test for anaplasma and babesia antibodies. This was done in order

K.-F. LOHR,P. S. OTIENO and W. GACANGA

844

Table 1 Reactions of Boran and Ayrshire cattle to Anaplasma marginale inefction

Breed

no. of

parasitaemia in '10

drop of PCV in 'I. maxi- mini-

maxi- mini-

prep, period in days

mum

mum

mum

mum

Boran

1L*

7

25

1

56

74

30

39.4

40.6

37.7

11.2

Ayrshire

20**

41

75

1

65

74

35

40.1

40.8

36.4

13.1

;:''i

average

average

average

't

cattle aver- maxi- miniage mum mum

temperature in OC

one animal died on day 17 p i . with a parasitaemia of 9 O/o, PCV of 1 4 o/o and temperature of 40.6 O C . 18 animals had to be treated for anaplasmosis.

to obtain some information on the prevalence of anaplasmosis and babesiasis in the district from which the experimental Boran cattle were obtained.

Results Reactions to A . marginale infection: Only one animal in the Boran group died from anaplasmosis in contrast to 18 animals in the Ayrshire group which if left untreated would most likely have died from anaplasmosis. The average minimum parasitaemia in the Boran group was sixfold lower than in the Ayrshire group. The average minimum fall of P C V and the average maximum temperature were 56 O/o and 39.4 OC respectively in the Boran group and 65 O / o and 40.1 O C respectively in the Ayrshire group (Table 1). The average prepatent period was 2 days shorter in the Boran group. The values for maximum parasitaemia and drop of PCV in the Ayrshire group would have been much higher if treatment had not been undertaken. I n spite of their very severe reactions to the anaplasma challenge none of the 9 Ayrshire animals which had undergone a B. bigemina challenge 2 months previously showed B. bigemina parasites on daily examination of their blood smears. Reactions to B. bigemina infection: None of the Boran animals died and only two of the Ayrshire cattle had to be treated for redwater. The average maximum parasitaemia in the Boran group was again approximately sixfold lower than in the Ayrshire group. The average values for drop of PCV, temperature and prepatent period was 19 "/o, 39.5 O C and 4.2 days respectively in the Boran group and 42 O / o , 40.9 OC and 3.3 days respectively in the Ayrshire group (Table 2). 59 O / o and 68 O / o of the sera from 105 adult cattle of the Mandera district showed positive reactions in the A . marginale and B. bigemina CA tests respectively. Table 2 Reactions of Boran and Avrshire cattle to Babesia binemina infection

Breed

'i

no. of

parasitaemia in %

cattle aver- maxi- miniage mum mum

drop of PCV in %

temperature in O C

aver- maxi- miniage mum mum

average

mum

maxi- mini-

mum

average prep. period in days

Boran

12

0.35

2

0.02

19

35

3

39.5

39.9

39.2

4.2

Ayrshire

11 +

2.3

7

0.5

42

71

27

40.9

41.7

40.1

3.3

two animals had to be treated for redwater.

Susceptibility of Boran Cattle to Experimental Infections

845

Discussion Three easily measurable effects on the cattle of A . murginule/B. bigeminu interactions were used for assaying the degree of susceptibility of the host to the parasite. These were the degree of parasitaemia, the drop of PCV and the rise of body temperature. During this study it emerged that these 3 parameters were not necessarily correlated to each other and that only the drop of PCV was consistantly correlated to the degree of illness of the animals, e.g. Boran cattle responded particularly badly to a rise of parasitaemia or a drop of PCV with a corresponding rise of body temperature; also low anaplasma parasitaemias could cause a steeper drop of PCV than higher anaplasma parasitaemias. Among the 20 Ayrshire cattle a better but by no means consistent correlation between the 3 parameters was found. Since death following anaplasma or babesia infection is caused by anaemia and anoxia, in animals which do not succumb to these diseases, the drop of PCV can be considered safely the best parameter for assaying the clinical syndrome e.g. the degree of the host's susceptibility to the parasite, whereas the other 2 parameters can be considered of assistance but as not being very reliable. It was of paramount importance that the Boran cattle and also the control animals had no contact with anaplasma and babesia parasites before the challenge. The regular dipping of the Boran cattle together with the negative serological results obtained with 2 different tests indicate that these animals were very likely free from infection. The Ayrshire cattle were chosen only by negative serological results. Their severe reactions to the A . murginule challenge again would indicate absence of infection prior to challenge. Their mild reactions to the B. bigeminu challenge were more severe than experienced following heterologous B. bigeminu challenge infection of premune animals (6) and thus indicated a low virulence of the challenge strain rather than yrechallenge experience by B. bigeminu infection. The experimental results showed that the Boran cattle in general were much less affected by anaplasmosis than the Ayrshire cattle. Individual Boran animals, however, could react very severely and even die from anaplasmosis, showing that Boran are not resistant per se to clinical anaplasmosis but merely possess a higher degree of resistance compared to that of Ayrshire cattle. These results were obtained from cattle living under very favourable environmental conditions. In cattle subjected to severe stress from drought, movement, transport, concurrent diseases etc., there would probably have been more severe reactions and higher mortality. Under such conditions and without observations on Bos tuurus control animals observers might easily be misled to assume that Boran cattle are highly susceptible to anaplasmosis. A higher virulence of the B. bigeminu strain than experienced in the challenge experiment would have been desirable. Nevertheless the virulence of the strain was sufficient to show that Boran cattle react much less severely to the same challenge of B. bigeminu than Ayrshire cattle. In fact, none of the Boran cattle showed any signs of illness, with maximum temperatures just exceeding the physiological range in only 4 animals whereas 5 of the Ayrshire cattle were clinically very sick and all of them were running temperatures between 40.1 and 41.7 O C . It can be argued that infection with a more virulent strain would have provoked clinical reactions in individual Boran animals. The wide variety of reactions obtained below the clinical threshhold would support this argument. Most likely it would be erroneous to assume that the results obtained from Boran cattle and Ayrshire cattle are representative for the degree of resistance of Bos indicus and Bos taurus. Generally Bos indicus has lived inZbl. Vet. Med., Reihe B, Bd. 22, Heft 10

58

846

K.-F. LOHR,P. S . OTIENO and W. GACANGA

finitely longer under selection pressure from babesia and anaplasma infections than Bos taurus. The selection pressure, however, was certainly not equally high wherever Bos indicus lived, and different Bos indicus breeds, or even populations of the same breed, may have built up a different degree of resistance depending on the prevalence of the parasitic challenge. In the arid areas where the Boran cattle live, many animals seem to grow up and reproduce without having come into contact with the parasites, as shown by the serological results. The selection pressure in this breed, therefore, can be considered moderate in contrast to that experienced by the Small East African Shorthorn Zebu of the Masai. In the latter clinical anaplasmosis or babesiasis is virtually unknown and inherent resistance alone might be responsible. However, this is difficult to prove because of the masking effect by the state of premunity these animals acquire during early calfhood when still under the protection of maternally derived antibodies (1 3). In conclusion, the results indicate that the claim of farmers that Boran cattle die from anaplasmosis and redwater is correct a t least for anaplasmosis and may be correct for redwater, too, and farmers are well advised to take precautions against both diseases not only when farming Bos taurus breeds but also when farming Boran cattle. One further result ermerged from this challenge experiment: It is well lcnown from field observations that cattle regarded premunised against redwater may suffer from attacks of redwater, generally a t widely spaced intervals. Sometimes these attacks coincide with an intercurrent disease or some other severe stress condition. It has not been decided whether these attacks are the result of a relapse or a re-infection (4). The fact, that none of the 9 B. bigemina infected Ayrshire cattle suffered from an attack of redwater although most of them only marginally survived a very severe attack of anaplasmosis, would indicate that redwater attacks in cattle considered premunised are rather the result of a re-infection than of a relapse. Homologous or heterologous re-infections of truly premunised cattle, however, do not result in clinical disease (6). Apparently there are B. bigemina strains of different virulence in Kenya but so far no indication exists for them not premunising against each other, an epizootiological condition found analogously in South Africa (4). Therefore, cattle regarded premunised but which showed attacks irom redwater must have lost their state of premunity before re-infection, which is very likely in view of the fact that cattle can lose their state of preinunity 5 months after infection (1 1).

Summary 14 and 12 Boran and 20 and 11 Ayrshire cattle were challenged with A. marginale and B. bigemina, respectively. Following A. marginale infection, one Boran animal died, the average maximum parasitaemia and average drop of PCV were 7O/o and 56O/o respectively compared with 18 out of 20 Ayrshire cattle which would have died if not treated, and with an average maxim u m parasitaemia and average drop of PCV of 41 O / o and 65 O / o . Following 0 . bigemina infection, average maximum parasitaemia and drop of PCV in the Boran and Ayrshire group were 0.35 O / o and 19 O / O and 2.3 O / o and 42 O / o respectively. The results showed that Boran cattle possess a considerably higher degree of resistance to A. marginale and B. bigemina infections than Ayrshire cattle, although they can be affected very severely and even die from anaplasmosis. The 9 Ayrshire cattle previously infected with B. bigemina did not develop babesia parasitaemia when very severely stressed by anaplasmosis, thus

Susceptibility of Boran Cattle to Experimental Infections

847

indicating that redwater attacks in cattle considered premunised are rather the result of a reinfection than of a relapse coinciding with an intercurrent disease.

Acknowledgement The authors thank Dr. I. E. MURIITHI,Director of Veterinary Services, Kenia, for permission to publish this paper. Zusammenfassung Die Empfanglichkeit von Boran-Rindern gegenuber experimentellen Infektionen rnit Anaplasma marginale und Babesia bigemina 14 Boran- und 20 Ayrshire-Rinder wurden rnit Anaplasma marginale und 12 Boran- und 11 Ayrshire-Rinder wurden Belastungsinfektionen mit Babesia bigemina ausgesetzt. Nach der Infektion rnit A. marginale starb ein Tier der Boran-Gruppe an Anaplasmose. Die durchschnittliche maximale Parasitamie sowie der durchschnittliche maximale Abfall des Erythrozytenvolumens betrugen bei dieser Gruppe 7 bzw. 56 " / o . Im Vergleich hierzu waren in der Ayrshire-Gruppe ohne Behandlung wahrscheinlich 18 Tiere gestorben. Die durchschnittliche maximale Parasitamie und der durchschnittliche maximale Abfall des Erythrozytenvolumens waren mit 41 bzw. 65 O / o bei den Ayrshires wesentlich hoher als bei der Boran-Gruppe. Nach der Babesia-Infektion waren die Durchschnittsmaximumparasitaemien und der Durchschnittsmaximumabfall des Erythrozytenvolumens 0.35 O/o und 19 O/o bei den Boran-Tieren und 2. 3O/n und 42 O / o bei den Ayrshire-Tieren. Die Ergebnisse wiesen somit auf eine betrachtlich hohere Resistenz der BoranTiere gegen A . marginale und B. bigemina-Infektionen im Vergleich zu Ayrshire-Tieren hin. Sie zeigten aber auch, dai3 Boran-Tiere schwer an Anaplasmose erkranken und sogar sterben konnen. In 9 Ayrshire-Rindern, die zuvor mit B. bigemina infiziert worden waren, konnten wahrend ihrer sehr schweren Anaplasmosereaktionen keinerlei B. bigemina-Parasiten festgestellt werden. Dies wird als Hinweis dafur angesehen, dai3 Erkrankungsfalle an Babesiose bei Tieren, die als premunisiert gelten, eher die Folge von Keinfektionen als von Ruckfallsparasitaemien im Verlauf anderer Erkankungen sind. Resume RCceptivitC de bovins de race Boran 21 des infections exPCrimentales avec Anaplasma marginale et Babesia bigemina O n a infect6 14 bovins de race Boran et 20 de race Ayrshire avec Anaplasma marginale ainsi que 12 animaux de race Boran et 11 de race Ayrshire avec Babesia bigemina. Un animal du groupe Boran a pkri aprhs l'infection avec A. marginale. La parasitkmie moyenne maximale e t la chute moyenne maximale du volume des globules rouge fut respectivement dans ce groupe de 7 et 56 O/o. En compraison, il y aurait eu 18 animeaux pkris dans le groupe Ayrshire si aucun traitement n'avait ktk entrepris. La parasitkmie et la chute moyenne maximale du volume des krythrocytes furent avec respectivement 41 et 65 O / o nettement plus klevkes dans le groupe Ayrkhire que dans le groupe Boran. Les moyennes maximales de parasitkmie et de chute du volume des krythrocytes furent de 0,35 et 19 O/o chez les animaux Boran, de 2,3 et 42 O/o chez les animaux

K.-F. LOHR,P. S. OTIENO and W. GACANGA

848

Ayrshire a p r h l'infection A Babesia. Les rksultats ont montrk unleplus grande rksistance contre A . marginale et B. bigemina chez les animaux Boran que chez les animaux Ayrshire et ont indiquk que les animaux Boran pouvaient &re gravement atteints d'anaplasmose et m&meen mourir. Aucun parasite B. bigemina ne fut mis en kvidence durant la trks grave anaplasmose chez 9 bovins Ayrshire prkckdemment infectis avec B. bigemina. Ceci tente A montrer que les cas de babesiose chez des animaux prkimmunisks sont davantage la conskquence de rkinfections que de rechutes de parasitkmies au cours d'autres maladies.

Resumen Receptividad de vacunos Boran frente a infestaciones experimentales con Anaplasma marginale y Babesia bigemina 14 vacunos Boran y 20 Ayrshire se expusieron a infestaciones de recargo con Anaplasma marginale y 12 vacunos Boran y 11 Ayrshire con Babesia bigemina. Tras la infestaci6n con A . marginale murib un animal del grupo Boran de anaplasmosis. La parasitemia maxima media y el descenso mlximo medio del volumen de eritrocitos era en este grupo del orden de 7 resp. 56 O/o. En comparaci6n con esto, habrian muerto con toda probabilidad 18 animales del grupo Ayrshire si no hubieran sido sometidos a tratamiento. La parasitemia mixima media y el descenso miximo medio del volumen d e eritrocitos eran bastante mayores con 41 resp. 65 O/ o en 10s Ayrshires que en el grupo Boran. Tras la infestaci6n con babesias alcanzaban las parasitemias miximas medias y el descenso mkximo medio del volumen de eritrocitos 0.35 O/o y 19 O/o en animales Boran y 2.3 O/o y 42 O/o en 10s animales Ayrshire. Por lo tanto, 10s resultados seiialan hacia una resistencia bastante mayor de 10s animales Boran frente a infestaciones A . marginale y B. bigemina en comparaci6n con 10s vacunos Ayrshire. Pero mostraron tambikn que 10s Boran enferman de anaplasmosis en forma grave, pudiendo morir incluso. En 9 vacunos Ayrshire, 10s cuales se habian infestado antes con B. bigemina, no se pudo verificar n i n d n pardsito B. bigemina durante sus reacciones anaplismicas graves. Esto se interpreta como indicaci6n de que 10s casos nosol6gicos de babesiosis en animales que se consideran premunizados son mis bien consecuencia de reinfestaciones que parasitemias recidivantes durante el curso de otras enfermedades. References 1. DALY,G. D., and W. T. K. HALL, 1955: A note on the susceptibility of British and some zebu type-cattle to tick fever (babesiosis). Aust. Vet. J., 31, 152. 2. FRANCIS, J., and D. A. LITTLE,1964: Resistance of Droughtmaster cattle to ti& infestation and babesiosis. Aust. J., 40,247. 3. FRANCIS,J., 1966: Resistance of zebu and other cattle to tick infestation and babesiosis with special reference to Australia: a historical review. Brit. Vet. J., 122, 301. 4. HENNING, M. W., 1956: Animal Diseases of South Africa. Central News Agency Ltd.,

South Africa. 5. KELLEY,R. B., 1943: Zebu-cross cattle in Northern Australia. An ecological experiment. Bull. Counc. sci. and Res. (Melbourne), 172, 96. 6. Kenya, Ann. Report Dept. Vet. Services, 1974. 7. LOHR,K.-F., und J. P. J. Ross, 1969: Ein Kapillarrohrchen-Agglutinationstestzum Nachweis von Babesia bigernina-Antikorpern. 2. Tropenmed., 20, 287. 8. LOHR,K.-F., 1973 : Susceptibility of non-splenectomised and splenectomised Sahiwal cattle to experimental Babesia bigemina infection. Zbl. Vet. Med. B, 20, 52. 9. LOHR, K.-F., J. P. J. Ross and MEYER,1973: Studies on homologous and heterologous antibody responses to infections with Anaplasma marginale and A. centrale using the

indirect fluorescent antibody and capillary tube agglutination tests. 2. Tropenmed. Parasit., 24, 86.

Susceptibility of Boran Cattle to Experimental Infections

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10. MITSCHERLICH, E., un K. WAGENER, 1970: Tropische Tierseuchen und ihre Bekampfung. Verlag Paul Parey, Berlin und Hamburg. 11. ROSENBUSCH. F.. und R. GONZALES.1925: Beitrag zum Studium der Tristeza. Arch. Protistenk.; 50; 443. 12. Ross, J. P.J., and K.-F. LOHR, 1968: Serological diagnosis of Babesia bigemina infections in cattle by the direct fluorescent antibody test. Vet. Sci., 9 , 557. 13. Ross, J. P. J., un K.-F. LOHR, 1970: Ubertragung und Verweildauer von kolostral erworbenen Babesia bigemina- und Anaplasma marginale Antikorpern. Z . Tropenmed. Parasit., 21, 401. 14. SEIFERT,H. S. F., 1971 : Die Anaplasmose, Atiologie, Epidemiologie, Behandlung und Verhutung. Verlag M. H. Schaper, Hannover. I

Address of Authors: Dr. K.-F. LOHR, P. S. OTIENO and W. GACANGA,Veterinary Research Laboratory, Kabete, Kenya.

Susceptibility of Boran cattle to experimental infections with Anaplasma marginale and Babesia bigemina.

Zbl. Vet. Med. B, 22, 842-849 (1975) @ 1975 Verlag Paul Parey, Berlin und Hamburg ISSN 0044-4294/ASTM-Coden: ZVRBAZ From the Veterinary Research Labo...
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