R.A.I. Norval
International Laboratory for Research on Animal Diseases
P.O. Box 30709
Nairobi, Kenya
Tick control is one of the most important factors influencing the epidemiology of bovine theileriosis in eastern and southern Africa. It was largely through tick control by acaricides that East Coast fever (ECF), caused by Theileria parva parva, was eradicated from South Africa, Swaziland, Mozambique and Zimbabwe in the first half of this century. It was the only method of control of the disease in East and Central Africa until the 1970s, when the infection-and-treatment method of immunization was developed. Because of its effectiveness, acaricide control of ticks has been widely adopted for the control of tick-borne diseases and is still the most commonly used control method for the T. parva group of diseases. Its effect on the epidemiology of the diseases thus requires examination, particularly in the light of new information on the epidemiology and control of the major vector, Rhipicephalus appendiculatus. This paper considers production losses caused by R. appendiculatus, the seasonal occurrence of the tick, age-related resistance to T. parva group parasites, nymphal transmission of the parasites, resistance to the parasites and their vector in different breeds of cattle, tick control and the role of immunization. There is some bias towards southern Africa because a large amount of research has been carried out in this region in recent years and the situation in East Africa has already been widely reported and discussed.
PRODUCTION LOSSES CAUSED BY RHIPICEPHALUS APPENDICULATUS
The rapidly rising costs of tick control make it increasingly important to consider the economics of strategies for the control of ticks and tick-borne diseases. An important economic factor is the effect of ticks per se on cattle productivity, particularly where the diseases are controlled by immunization. In these situations the cost of tick control can be weighed against the benefit of increased productivity.
Norval et al. (1988) studied the effects of tick infestation on the growth of Sanga and Bos taurus cattle in Zimbabwe. Groups of young cattle were infested with high, moderate and low numbers of larvae, nymphs and adult R. appendiculatus. The numbers of each stage completing feeding and the liveweight gain (LWG) of the cattle were recorded. Larvae and nymphs had no significant effect on LWG, but each adult female that completed feeding caused a loss of approximately 4 gm. Bos taurus cattle had a low resistance to the tick and consequently suffered large losses from adult infestations. The losses in Sanga cattle, which were very resistant to the tick, were insignificant.
The effect of adult R. appendiculatus on milk production in Sanga cows was small but statistically significant (Norval et al., in preparation). In a more recent experiment by the same workers, it was found that cows of higher producing breeds were generally less resistant to the tick and the effect on milk production appeared to be greater, but statistical analysis of the data has not been completed.
SEASONAL OCCURRENCE OF RHIPICEPHALUS APPENDICULATUS
The pattern of seasonal occurrence of R. appendiculatus is determined by climate (Short and Norval, 1981; Rechav, 1982; Floyd et al., 1987a). The seasonal cycle is determined by the adults, which are only active under warm, wet conditions when the photophase (day length) exceeds approximately 11 hours. This means that in locations near the equator, such as Entebbe, Uganda, adults can be active throughout the year if there is no prolonged dry season. As a consequence, larvae and nymphs will also be continuously present and the tick will probably pass through two or more generations each year. If there are two wet seasons, as in the highlands of Kenya, there will be two periods of adult activity and probably two generations each year. Further south, where the seasons are more clearly defined and rain falls only in the summer, there is only one generation each year. Floyd et al. (1987a) have shown that the T3HOST population model, which is climate driven, can be used to predict patterns of seasonal occurrence.
AGE-RELATED RESISTANCE
It is well established that young cattle have an age-related resistance to most tick-borne protozoan and rickettsial diseases. In Zimbabwe, where the ages of cattle that died from T. p. bovis infection were recorded from 161 outbreaks in Mashonaland-West Province over an eight-year period, significantly less mortality occurred in calves than in adults or weaners (Koch et al., in preparation). However, in a laboratory experiment the same authors found that age-related resistance was only of short duration (approximately one month), which does not correspond with field observations. The calves used in the experiment were from non-immune dams and it was concluded that maternal factors are probably of importance in the protection of calves, as indicated by the work of Barnett and Bailey (1955) with T. p. parva in Kenya. In a more recent study, on Rusinga Island, in Lake Victoria, antibodies to sporozoites, schizonts and piroplasms have been recorded in the colostrum of immune cows and the serum of their calves (S.P. Morzaria, A.A. Latif and P.B. Capstick, personal communication). In this study, as in that of Barnett and Bailey (1955), it was shown that the majority of calves of indigenous breeds born to immune dams in an enzootic area recover from challenge with East Coast fever and become immune. Those from non-immune dams usually die.
In contrast to the findings with T. p. bovis, Barnett and Bailey (1955) and Irvin et al. (unpublished results) found that one-month-old calves from non-immune dams were more susceptible to T. p. parva infection than older calves. The reasons for this are not known.
An important factor to consider when interpreting the laboratory experiments on age-related resistance is that the calves were infected by injection of stabilate. This may have resulted in a higher dose of parasites than would normally be experienced in the field, where infection rates in ticks are usually very low (Morzaria and Young, 1987). Young calves also carry far fewer adult R. appendiculatus than older cattle (Barnett and Bailey, 1955, and Norval and Colborne, unpublished observations) and must therefore be exposed to lower numbers of Theileria parasites. This may be part of the reason for the milder reactions in this age group under field conditions.
In contrast to indigenous breeds, members of all age classes of Bos taurus cattle, including calves, usually die on initial exposure to T. p. parva infection.
NYMPHAL TRANSMISSION
Nymphs of R. appendiculatus transmit T. p. parva and play a role in the epidemiology of the disease (Barnett and Bailey, 1955; Neitz, 1956; Purnell et al., 1971). With T. p. bovis, however, Matson and Hill (1967) and Lawrence et al. (1983) reported that they had been unable to achieve transmission using nymphs. These findings are supported by the field data of Norval et al. (1985), who reported that of 190 recorded outbreaks of T. p. bovis in Zimbabwe in 1981 and 1982, 94.2% occurred from January to March, when adults of R. appendiculatus are active and few nymphs are present.
More recently Koch et al. (in preparation) have found that T. p. bovis can be transmitted to cattle by large numbers of nymphs of R. appendiculatus fed as larvae on reacting animals. The reactions caused were severe or fatal, but the authors were unable to induce mild or unapparent reactions using low numbers of infected nymphs. In field studies on commercial farms in Zimbabwe, however, the authors detected increases in serological titres to T. p. bovis schizont antigen late in the dry season, suggesting that nymphs were transmitting subclinical infection. The implication is that nymphs may play a role in the epidemiology of T. p. bovis by transmitting mild but immunizing infections before the onset of the more severe adult-transmitted challenge after the start of the rains.
RESISTANCE TO TICKS AND TICK-BORNE DISEASES
That indigenous Zebu and Sanga cattle are more resistant to ticks (Bonsma, 1944 and 1981; Barnett and Bailey, 1955; Rechav and Zeederberg, 1986; Norval et al., 1988; Spickett, in press), East Coast fever (Barrett and Bailey, 1955; Barnett, 1957; Guilbride and Opwata, 1963; Wilde, 1967; Dolan and McHardy, 1976; Moll et al., 1984, 1986) and other tick-borne diseases, such as babesiosis (anonymous, 1984) and heartwater (Van de Merwe, 1979), has been inadequately exploited in control programmes. In indigenous cattle little or no tick control is required to increase productivity, and mortality due to tick-borne diseases is usually low or insignificant because of enzootic stability. In overgrazed areas, where the suitability of the environment for tick survival is low, R. appendiculatus is frequently absent (Yeoman, 1967; Norval, 1977), and the numbers of ticks of other species on indigenous cattle are usually very low (Barnett and Bailey, 1955; Kaiser et al., 1982). In spite of this it is still common in several African countries to subject indigenous cattle to intensive tick control. The practice is uneconomic because increased productivity is minimal, and it is epidemiologically unsound because reduced tick challenge can adversely affect enzootic stability. Pegram and Chizyuka (1987) reported that in Zambia acaricide treatment of Sanga cattle was economically justified only to control occasional heavy infestations of adults of Amblyomma variegatum. They recommended the strategic use of acaricides. Floyd et al. (1987b) have shown how computer models can be used to identify the most cost-effective control strategies for different environments and breeds of cattle. Loss of enzootic stability can result in high mortality in adult indigenous cattle if control measures fail (Norval, 1979 and 1981).
As long as Bos taurus cattle are kept in areas in which R. appendiculatus and the T. parva group of diseases occur, the animals will have to be treated regularly with acaricide to control the tick to ensure high productivity. To guarantee their survival, the cattle will have to be immunized against tick-borne diseases.
TICK CONTROL
The aims of any tick control programme should be carefully defined. These are usually to control tick-borne diseases and to increase productivity or to prevent the formation of lesions that can become secondarily infested with screwworm fly (Chrysomya bezziana) larvae. Governments and farmers often fail to define the aims of control programmes and lack an adequate understanding of the epidemiology of the tick-borne diseases that occur in their areas. The result is that many programmes are uneconomic or destabilizing, as explained in the previous section.
Arsenical acaricides were used for at least 50 years in most areas before tick resistance became a problem. Subsequently, organochlorine, organophosphate, carbamate, amidine and synthetic pyrethroid acaricides have been introduced, in roughly that order, to most countries in the region. Tick resistance to organochlorines is now widespread and these compounds have largely been phased out. Organophosphates are currently the most widely used acaricides, but problems with tick resistance are increasing and so their use is likely to decline in the future. The amidines and synthetic pyrethroids are becoming more widely used and have a much longer residual effect than the other acaricide groups but are considerably more expensive. A potential problem with the pyrethroids is cross-resistance between them and the organochlorines; evidence of this has already been reported in Boophilus decoloratus in South Africa (Coetzee et al., 1987).
Acaricides are most commonly applied by dipping or spraying, dipping being considered the more effective means of application. In recent years several other methods of acaricide use have been tested, including the slow release of systemic acaricides from implants and boluses; the slow release of conventional acaricides from impregnated ear-tags; "pour-one", which are applied on the backs of livestock and spread rapidly over the entire body surface; and "spotons", which are similar to pour-one but have less capacity to spread. Neither systemic acaricides nor acaricide impregnated ear-tags have been marketed in Africa. The pour-on and spot-on formulations, which contain synthetic pyrethroids, are now available in some countries and their use is increasing. The advantages of these formulations are ease of application (no physical structures or capital investment are required) and long residual effect.
A recent advance of potentially great importance has been the production, using biotechnology, of an effective vaccine against B. microplus (Willadsen and Kemp, 1988). The immunizing agent is a "concealed" tick antigen, an antigen not normally encountered by the host. The immune mechanism it stimulates is different from that stimulated by exposure to feeding ticks. The antigen was derived from a crude extract of partially engorged adult female ticks. It stimulates the production of an antibody that damages tick gut cells and kills the ticks or drastically reduces their reproductive potential. It is likely that similar vaccines will be developed in the future against African tick species of major economic importance (R. appendiculatus, A. hebraeum, A. variegatum and B. decoloratus). These vaccines could render the other forms of tick control obsolete and completely alter our approaches to the control of ticks and tick-borne diseases.
EFFECT OF TEMPERATURE ON MATURATION OF SPOROZOITES IN TICK SALIVARY GLANDS
Young et al. (1979, 1984 and 1987) and Ochanda et al. (1988) have shown that exposure of adult R. appendiculatus to high temperatures (26 °C and 37 °C) prior to feeding stimulates the maturation of T. p. parva parasites in the salivary glands to mature sporozoites. The authors concluded that adult ticks exposed to high temperatures in the field would transmit infection to cattle more rapidly than would otherwise occur. This could reduce the efficiency of acaricide control of East Coast fever and should be considered in the design of control strategies and the selection of acaricides in the hotter areas in which the disease occurs.
DISCUSSION
Immunization offers the best means of protection of Bos taurus cattle against theileriosis and other tick-borne diseases. It can be used on indigenous breeds to create stability in enzootically unstable situations created by intensive dipping. Once cattle are immune, tick control can be relaxed and further use of vaccines may be unnecessary because the animals will be immunized against tick-borne diseases by exposure to infected ticks.
A factor contributing to the greater resistance to tick-borne diseases in indigenous breeds is their greater tick resistance. Barnett and Bailey (1955) reported that the recovery rate in calves from immune dams decreased significantly if the numbers of T. p. parva infected ticks fed on them were increased. Fivaz et al. (1984) and Leitch (1989) have shown that cattle with a high resistance to R. appendiculatus become less severely infected with T. p. bovis and T. p. parva than tick-naive cattle, which become heavily infested.
The modelling approach has indicated that the most effective control strategies for R. appendiculatus are those directed against the adult stage (Floyd et al., 1987b). These strategies would also reduce the severity of challenge with the T. parva group of diseases, because adults are the most important vectors.
Irvin et al. (unpublished observations) have shown that Boran calves can be safely immunized against T. p. parva by infection and treatment between 2 and 16 weeks old. There are several advantages to immunizing cattle when young. The animals carry low numbers of ticks and so the risk of acquiring a fatal infection from ticks is low. Calves born to immune dams appear to have some protection from severe reactions due to maternal antibodies and there is evidence of an age-related resistance. Calves are easier to handle than older cattle and the amount of drug required to treat the reaction is low, which minimizes the cost of immunization. Immunizing cattle when they are young also gives greater flexibility in tick control and, in the absence of vaccines for other tick-borne diseases, exposes calves to infection by ticks while they are still protected by age-related resistance.
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