TICK TAXONOMY

Two special publications have appeared on tick taxonomy: Camicas, Harvy, Adam & Morel compiled a comprehensive list of the ticks of the world (Camicas et al. 1998) and Horak, Camicas & Keirans (2002) continued this endeavour by presenting a revised world list of valid tick names. According to this latter list of valid tick names, approximately 80% of the world's tick fauna are ixodid ticks (hard ticks) (683 species) and, with the exception of one species in the family Nuttalliellidae, the remainder are argasid ticks (soft ticks) (183 species). This list has formed the basis for an interactive database in access 2000, designated Tickbase¹

IMPORTANT TICKS OF THE WORLD

Most ticks have a preference for feeding on certain groups of wild animals, with some even being quite host specific. Consequently, the number of species pertinent to domestic animals and/or humans is limited. As a matter of fact relatively few species of ticks have successfully adapted to livestock or feed on a human subject, and these have developed into efficient vectors of a range of pathogenic micro-organisms, while virtually all human tick-borne diseases are zoonoses (Table 1).

The following ecological criteria were used to underpin the tick–host–pathogen relationships listed in Table 1. A tick species is considered a vector for a particular pathogen only if it (1) will feed on an infectious vertebrate host, (2) is able to acquire the pathogen during the blood meal, (3) can maintain the pathogen through one or more life stages, and (4) can pass it on to other hosts when feeding again (Kahl et al. 2002). In addition to information on well-established vector competence, Table 1 also includes ticks that can induce paralysis, toxicosis, severe local reactions such as forms of pruritus, secondary bacterial abscesses and a variety of reactions caused by immune-mediated responses. A detailed account of the biology of ticks is available in two classic monographs by Sonenshine (1991, 1993).

ARGASID TICKS

Argasid ticks of medical and veterinary importance belong to the genera Argas, Ornithodoros and Otobius. The Argasidae live near their favourite host (in its nest, pen, stable, hut, etc.) and the parasitic stages (nymphs are always parasitic, larvae and adults usually so) feed for a short period only on the host (a matter of minutes to, say, an hour) and then go back to their hiding place. Exceptions are the larvae of certain Argas spp. that attach and feed for some days on domestic poultry, and the immature stages of Otobius which are parasitic for long periods in the external ear canals of their hosts. Soft ticks often have several nymphal stages. Adult Argasidae mate off the host; the female (again with the exception of Otobius whose adults are non-parasitic) feeds several times and produces a small batch of eggs after each meal. Argas miniatus is widely distributed in the Neotropical region and both A. persicus and A. reflexus are found in southern Europe and central Asia; they usually feed on birds. Argas monolakensis is an important argasid tick of birds that can feed on humans in the Western USA (Schwan, Corwin & Brown, 1992). Other ticks such as A. brumpti and Argas (now Carios) vespertilionis cause extensive local lesions resembling bruising after feeding on humans. Larvae and nymphs of the spinose ear tick, Otobius megnini, can be found deep in the external ear canals of livestock, companion animals and, occasionally, man and may cause otitis. This tick occurs in the western parts of the USA and parts of South America. It is also found in the Afrotropical and Oriental regions. The widely distributed argasid genus Ornithodoros contains 38 species, with O. moubata and O. porcinus as important species in the relatively arid parts of Africa, where they find shelter in caves, rodent burrows, bird nests and also in cracks and crevices of huts and shelters of indigenous peoples and their domestic animals. Another species, O. savignyi, lives in sandy soil at the shaded resting sites of livestock in semi-desert areas and feeds on the legs of cattle, sheep, goats and camels, building up massive infestations (Hoogstraal, 1956).

IXODID TICKS

Ixodidae may be one-, two- or three-host species depending on the number of host animals they attach to during their life cycle. Larvae and nymphs feed once to engorgement and then moult. One-host ticks moult twice on the same host animal, from larva to nymph and from nymph to adult. Two-host ticks moult once on the host, from the larval to the nymph stage; the engorged nymph drops off, moults off the host and the resulting adult has to find a second host animal (which may or may not be of the same species as the first). Three-host ticks do not moult on the host; the engorged larva drops off, moults to a nymph, which then has to find a second host animal on which it engorges and drops off again to moult to the adult stage, which attaches to a third host animal. Adult Ixodidae usually mate on the host, the female then feeds to engorgement, drops off, lays a large batch of eggs and dies (while the male may remain on the host for several months). Logically, the egg batches of one-host ticks contain on average far fewer eggs than those of three-host ticks, as the latter have to run the gauntlet of finding a new host three times in their life cycle, and the former only once. Two-host ticks run less risk than three-host species but more than one-host ticks, and their egg batches are intermediate in size.

Some characteristics of seven important genera of ixodid ticks (Amblyomma, Boophilus, Dermacentor, Haemaphysalis, Hyalomma, lxodes and Rhipicephalus) are summarized below.

IMPACT ON LIVESTOCK

Without acting as vectors of disease, ticks can be harmful to livestock and of great economic importance simply because of their direct effects. Much depends on the circumstances, on the tick species involved, on the local climatic conditions (favourable or unfavourable to the ticks) and, to a large extent, on the susceptibility to tick infestation of the livestock in the region. Resistance to tick infestation, or at least the capability of developing an effective immunological response to infestation, is genetically determined. This is particularly important where one-host Boophilus spp. are implicated. Uncontrolled Boophilus infestations in climatically favourable conditions severely affect European cattle, but have little effect on zebu cattle. Such infestations per se, even when no diseases are transmitted by the ticks, can limit productivity of European Bos taurus cattle to the extent that a choice has to be made between simply renouncing the use of such cattle, or applying intensive and expensive chemical tick control, which usually leads rapidly to resistance against the acaricides used. For example, on the island of New Caledonia the tick Boophilus microplus has been introduced without the diseases it transmits elsewhere, namely babesioses and anaplasmosis. However, highly favourable climatic conditions throughout the year and a large population of susceptible European beef cattle breeds have made it necessary to develop intensive acaricidal treatment programmes, which have led to an enormous problem of widespread multi-acaricide resistance, with resistance having successively developed to the various groups of chemicals used (Bianchi, Barré & Messad, 2003). Hence, it may be far more economical to make more use of Bos indicus breeds, pure or cross-bred, as has been done in many instances in Australia, where zebu cattle have proved to be much more resistant to tick infestation than European cattle.

The damage caused by tick bites also diminishes the value of skins and hides for the manufacture of leather; even ticks with a short hypostome, such as Boophilus, may be important in this respect when present in large numbers on susceptible cattle. Ticks with long and massive hypostomes, such as Amblyomma and to some extent Hyalomma spp., may induce abscesses because of secondary bacterial infections. In this way Amblyomma spp. may cause loss of teats or lameness, depending on the site of attachment. In turn loss of teats will lead to increased calf mortality.

The saliva of certain tick species contains paralysing toxins; examples of this are D. andersoni in Canada and the USA that can cause death even in adult cattle, I. rubicundus that induces a severe form of paralysis in sheep in southern Africa, and I. holocyclus in Australia, that usually feeds on bandicoots, but can also feed on domestic animals, tropical bats (Pteropus spp.) or humans, and is considered a very important tick with respect to tick toxicosis (Gothe, 1999). Another form of tick toxicosis is ‘sweating sickness’, a generalised eczema-like condition of calves and other species of livestock in Africa, induced by the saliva of certain lines of Hyalomma truncatum. A detailed account of tick salivary toxins is given in the chapter by Mans, Gothe & Neitz in this Supplement.

There is also at least one example of a tick-associated disease which is not transmitted by ticks. This is severe bovine dermatophilosis induced by the presence of adult Amblyomma variegatum which, in certain regions of the tropics, may prevent upgrading of local cattle with highly susceptible imported breeds (Ambrose, Lloyd & Maillard, 1999).

The most important diseases transmitted by ticks, particularly in domestic ruminants, are babesioses, theilerioses, anaplasmoses and cowdriosis (see chapters in this Supplement on babesiosis by Bock et al., theileriosis by Bishop et al. and anaplasmosis by Kocan et al.). Recovered animals retain the infection and remain immune for long periods, sometimes for life. In general, where such diseases are endemic, the local livestock has been exposed to a long process of natural selection and has, to various degrees, become tolerant, but not refractory to the infection. Furthermore, young animals are generally more tolerant than adults. The combination of natural tolerance and age-associated tolerance may result in an endemically stable situation which, at best, means that the prevalence of infection may be 100% but that the disease is not clinically apparent. In other cases, endemic stability may be less perfect and there may be some mortality following primo-infections in young animals, but older stock that have survived the infection are immune. Obviously tick numbers are important as endemic stability can only be attained where adequate numbers of infected ticks are present to infect all animals while they still possess their age-associated tolerance. For example, in regions where cowdriosis is endemic the situation may be endemically stable in local cattle, but not in local breeds of small ruminants, probably because fewer Amblyomma (at least adult ticks) feed on them. Climatic conditions are among the main factors influencing tick numbers and endemic stability is thus not attained in areas which are climatically marginal for the vector tick species.

Exotic livestock, introduced from disease-free regions in which they have not been exposed to natural selection, are far more susceptible to most tick-borne diseases and even though mortality in young stock of such breeds is less than in adults, endemic stability can often not be achieved. This is certainly true for cattle and theilerioses (at least tropical theileriosis, Theileria annulata, and East Coast fever caused by T. parva), babesiosis caused by Babesia bovis, and cowdriosis (Ehrlichia (Cowdria) ruminantium). However, there may be little difference in susceptibility to anaplasmosis (Anaplasma marginale) and babesiosis caused by B. bigemina between local and exotic cattle. Particularly theilerioses and cowdriosis may make it impossible, or at least uneconomical, to keep exotic ruminant breeds unless management and veterinary infrastructures are adequate. The same considerations apply to indigenous breeds of animals that have never been exposed to a particular pathogen. For instance, translocation of indigenous goats from the north of Mozambique to the south into Amblyomma hebraeum-infested areas were highly risky because of cowdriosis (Bekker et al. 2001).

Anyone involved with livestock in tropical and subtropical areas of the world recognises that ticks and tick-borne diseases are important, but there are few if any reliable global figures of the costs involved. Young, Groocock & Kariuki (1988) considered the control of ticks and tick-borne diseases as the most important health and management problem in Africa, presenting a problem of equal or greater magnitude than tsetse fly and trypanosomosis. Various estimates of effects are tentative, sometimes rather different, and moreover depend on variables, including annual climatic variations, fluctuating exchange rates and inflation. The global costs of tick and tick-borne disease control has been estimated at US$ 7 milliard (=7×10⁹) by McCosker (1979). This amount, still sometimes quoted, is certainly hugely underestimated because it was based on Australian figures taking only the tick B. microplus and its role as a vector into account, multiplied by the world cattle population exposed to ticks and tick-borne diseases. Some other economic estimates of the cost of ticks to the livestock industry only concern certain diseases and particular regions and, although we do quote a few of them, we are under no illusion as to their accuracy. Mukhebi et al. (1999) estimated that the national annual loss due to cowdriosis in Zimbabwe could attain 5·6 million US$, while a questionnaire study in 1991 by Meltzer, Perry & Donachie (1996) arrived at a figure of about 6·5 million US$ in cattle alone on large-scale commercial farms in Zimbabwe, most of this amount being the cost of dipping. Recently, Minjauw & McLeod (2003) have made a great effort at producing figures, tables and maps on the importance, the distribution, the numbers of animals at risk and the cost of the various diseases in eastern and southern Africa, also to some extent in sub-Saharan Africa as a whole, and of tropical theileriosis in India. They estimate the annual cost of tropical theileriosis in India at 384·3 million US$, of East Coast fever in the smallholder dairy system in Kenya and Tanzania at 54·4 million US$ and 4·41 million, respectively, in the traditional system in Kenya and Tanzania at 34·1 and 129·5 million, respectively. An older figure is 168 million US$ annually as the cost of Theileria parva in eastern, central and southern Africa (Mukhebi, Perry & Kruska, 1992).

IMPACT ON COMPANION ANIMALS

Companion (or pet) animals, in particular dogs, pay a heavy toll to tick-borne diseases. Again, we will only mention a few of the more important ones. In tropical and subtropical regions, but even in many of the temperate zones, there are several babesioses of which some are highly pathogenic to dogs. Ehrlichioses occur in many regions of the world and infection with Ehrlichia canis is often fatal. Dogs belonging to tourists travelling to warm regions are liable to contract (sub)tropical tick-borne diseases, which usually only become apparent after returning home. In Europe in particular ehrlichiosis and babesiosis are acquired by dogs travelling to the Mediterranean region. Moreover, Hepatozoon canis, with its peculiar life cycle wherein the vector has to be ingested by the dog, is found with increasing frequency in dogs returning to the northwest of Europe. From the viewpoint of the animal health industry, acaricides for companion animals are seen as an increasingly important part of their market portfolio and focus (see chapter by Leach-Bing et al. in this Supplement).

Since only 10% of the world's horse population resides in areas free from Babesia caballi and Theileria equi, piroplasmosis certainly has a great economic impact on the horse industry. Although these diseases are endemic throughout the (sub)tropics and even in some temperate regions, a disease-free status is required for any horse entering North America, Canada, Japan or Australia. Hence there have been many complications for horses harbouring either one of these parasites but fit to compete for instance at one of the Olympics Games (Atlanta, USA, 1996; Sydney, Australia, 2000) or at any other sporting event.

EMERGING ZOONOSES AND PUBLIC HEALTH IMPACT

Reviews of human tick-borne diseases have been published by Parola & Raoult (2001a,b), who reported that 15 novel bacterial pathogens have been described since the discovery of B. burgdorferi in 1982. Cunha (2000) edited a book encompassing the diagnosis and management of human tick-borne infectious diseases, while the literature pertaining to ticks feeding on humans has been reviewed by Estrada-Peña & Jongejan (1999). Recently, Gray et al. (2002) edited a volume dealing comprehensively with the complex biology and ecology of Lyme borreliosis in a worldwide context.

The mounting array of tick-borne zoonotic diseases emerging in the temperate parts of the world poses an ever increasing public health risk. There is a clear correlation between the increase in the USA and much of western Europe in abundance of deer (main host for adult I. scapularis and I. ricinus) with tick density. This is due to conversion of agricultural land into habitat suitable for the maintenance of large populations of deer, contributing to a sharp increase in tick numbers. Increased recreational activities in rural tick-infested areas have resulted in an increased number of humans who are bitten by ticks in the USA as well as in western Europe. To put another perspective on this, in some rural parts of Tanzania people prefer to sleep outdoors to avoid attack by the indoor-dwelling soft ticks and tick control is practised by spraying infested houses with pesticides to reduce the incidence of tick-borne relapsing fever (Talbert, Nyange & Molteni, 1998).

Human tick-borne diseases have gained enormously in notoriety since the discovery of Lyme borreliosis (LB) two decades ago (Burgdorfer et al. 1982), which stimulated a considerable quantity of research. Spirochaetes of the B. burgdorferi sensu lato complex consist of more than 10 different genospecies transmitted by ticks of the genus Ixodes (Gray et al. 2002). LB is now recognized as the most commonly reported arthropod-borne disease in North America and Europe, accounting for tens of thousands of new cases yearly in both regions. The complications of untreated LB in humans can be severe and disabling, but reports of LB as a cause of death are mostly unsubstantiated (Dennis & Hayes, 2002). The costs for medical care of LB patients, disease surveillance and laboratory diagnostics must of necessity be very high, but no accurate figures are available. A detailed account of Lyme borreliosis in Europe and the USA is given in the chapter by Piesman & Gern in this Supplement.

Some of the major human diseases transmitted by argasid ticks (mainly Ornithodoros) are caused by other Borrelia species, which induce relapsing fevers. In large areas of Africa and elsewhere, where soft ticks transmit such Borrelia spirochaetes to humans, the infections may be confused with malaria and consequently are much underestimated human tick-borne diseases in terms of morbidity and impact on public health.

Man-biting Ixodes spp. transmit viral infections causing European tick-borne encephalitis and the more severe Russian spring summer encephalitis. Other viral infections, such as Crimean-Congo haemorrhagic fever, transmitted by Hyalomma spp., occur sporadically throughout vast areas of Africa, Asia and Europe, and can cause mortality. Another potentially deadly flavivirus, which causes Kyasanur forest disease in India, is transmitted by Haemaphysalis spp., and claims many victims annually. A detailed account of tick-borne viruses is given in the accompanying chapter by Labuda & Nuttall in this Supplement.

The tick-borne rickettsiosis, Rocky Mountain spotted fever, caused by Rickettsia rickettsii, a life-threatening but treatable rickettsial disease, is widespread in most of the United States and beyond, and is transmitted by Dermacentor spp. Another rickettsial infection, fìèvre boutonneuse, caused by Rickettsia conorii and transmitted by Rhipicephalus sanguineus and other tick species, occurs mainly in Europe. In Africa, Amblyomma spp. transmit Rickettsia africae, whereas Dermacentor reticulatus transmits R. sibirica, the causative organism of Siberian tick typhus, in the former Soviet Union. Two other tick-borne rickettsioses of humans, monocytic and granulocytic ehrlichiosis, caused by Ehrlichia chaffeensis and E. phagocytophila (or Anaplasma phagocytophila according to Dumler et al. (2001), rectified to A. phagocytophilum (Anonymous, 2002)), have recently emerged. E. chaffeensis is transmitted by Amblyomma americanum and E. phagocytophila by Ixodes scapularis in the USA and by Ixodes ricinus in Europe.

Protozoan diseases also play a role in human public health. Babesiosis is transmitted by Ixodes spp. in the USA and Europe. Traditionally thought to be caused by Babesia microti in the USA and by B. divergens in Europe, this view of human babesiosis may be oversimplified since it appears that not all of the approximately 300 cases reported in the USA thus far are due to B. microti. Other parasites, distinct from B. microti, have now been identified and some of them are B. divergens-like (Kjemtrup & Conrad, 2000; Beattie, Michelson & Holman, 2002). Although the role of B. microti needs to be established, clinical cases in Europe have mostly been attributed to B. divergens, but perhaps wrongly so (Herwaldt et al. 2003). Human babesiosis appears to be on the increase, with more than half of the cases in the literature reported since 1985. A further dimension is added if one considers the incidence of human babesiosis transmitted by blood transfusions which also appears to be on the increase. Since 1980 over 20 cases have been reported including recent cases from Japan (Saito-Ito et al. 2000) and Canada (Bu Jassoum et al. 2000). It is currently the second most common parasitic infection (after Plasmodium) acquired by blood transfusion and the risk of becoming infected by blood transfusion has been estimated at six per 1 million units of blood collected (McQuistion et al. 2000). The chapter by Telford & Goethert in this Supplement describes new and re-emerging human tick-borne diseases.

Finally, human international travel, one of the largest and most rapidly evolving industries worldwide, has a significant impact on health care. Travel-associated tick-borne diseases have emerged as common subjects of international travel medicine. For instance, African tick-bite fever, a spotted fever group rickettsiosis caused by Rickettsia africae, transmitted by Amblyomma spp., is present in many countries in sub-Saharan Africa, as well as in the Caribbean region. Although the clinical course of African tick-bite fever is usually mild, complications may occur. In addition, the infection may easily be overlooked or confused with other tropical diseases such as malaria (Jensenius et al. 2003).

TICK CONTROL ON LIVESTOCK

Within the limits of this review, it is possible to outline only briefly the various aspects of tick control and discuss various new developments. Except on islands, where successful campaigns have sometimes been implemented, eradication of ticks is generally not feasible. Although the eradication of Boophilus spp. from the USA remains a notable exception, eradication of ticks on large islands and on continents is in most cases not a realistic goal. In the case of the USA, eradication was possible through the stringent application of legislative measures and particularly because Boophilus spp. are one-host ticks with a distinct preference for cattle. Luck may also have played a role in that acaricide resistance was not a complicating factor during the campaign. It is, however, now becoming increasingly difficult to prevent the ticks from becoming re-established from neighbouring Mexico, partly because of acaricide resistance and the presence of large numbers of deer. Acaricide resistance was probably also one of the main reasons for the failure to eradicate B. microplus in New South Wales, Australia. Because wild animals act as reservoirs or preferred hosts for economically important ticks, it is generally unrealistic to consider eradicating ticks, including those such as I. ricinus, which parasitize many animals in addition to domestic livestock in temperate regions.

Control of tropical tick-borne diseases, especially in more susceptible and productive exotic or upgraded breeds of livestock, still depends mainly on intensive tick control using acaricides (see chapter in this Supplement by George et al.). However, these chemicals are toxic, leave residues in meat and milk and cause environmental pollution. Moreover, acaricides are costly and require expenditure in foreign currencies, thus constituting a major economic strain on the development of the livestock industry, particularly in developing countries. Finally, the resistance of ticks to acaricides poses an increasing threat to livestock production. Consequently intensive (and thus expensive) dipping or spraying programmes have been largely unsuccessful in eradicating ticks and tick-borne diseases.

Integrated tick control strategies are therefore advocated. Such strategies have been preferred for quite some time (e.g. Young et al. 1988) and are based on host resistance to ticks and to the diseases they transmit, strategic tick control (taking into account the seasonal dynamics of tick infestation), the availability of vaccines against tick-borne diseases and cost/benefit analyses of acaricidal application. Accurate data on tick ecology (e.g. geographical distribution, seasonal occurrence and host preference) are required, together with data on the prevalence of tick-borne diseases within both traditional and commercial livestock production systems. Epidemiological data, combined with tick ecological data, form a basis for a sustainable tick control programme. Detailed accounts of tick ecology by Randolph and the application of GIS tools for tick-borne disease surveys by Daniel, Kovar & Zeman are given in separate chapters in this Supplement.

Sometimes solutions to specific tick-related problems are available but not implemented. For instance, it is feasible to keep susceptible highly productive cattle breeds in areas infested with Hyalomma spp. that are infected with Theileria annulata through vaccination using attenuated cell cultures derived from the Theileria parasites. This approach, successfully implemented in a number of countries, should be further examined and developed, in particular in northern Africa and in the Sudan.

New opportunities have been created with the development of anti-tick vaccines (Willadsen & Jongejan, 1999). Although this subject is discussed in detail by Willadsen elsewhere in this Supplement, the very high efficacy of available anti-Boophilus microplus vaccines (TickGARD and GAVAC) against Boophilus annulatus in two independent trials with two different vaccines is interesting to note (Fragoso et al. 1998; Pipano et al. 2003). This result indicates that it may actually be possible to eradicate B. annulatus from particular areas.

Progress in the Caribbean Amblyomma Programme to eradicate A. variegatum with the aim of increasing food security in the Caribbean and prevent tick introduction onto the American mainland is showing encouraging results with several islands declared provisionally free of the tick (Pegram & Eddy, 2002). However the programme will only truly be successful if the tick is eradicated from all the infested islands.

Acaricidal control of soft ticks on poultry is very difficult because of the particular hiding behaviour of the ticks in the housing. The poultry industry nowadays has become a large professional agribusiness using improved housing facilities; this is also the case in the tropics and certainly in most Latin American countries. These modifications have diminished the possibility of ticks being able to hide inside. On the other hand, free-range egg production is an emerging trend in response to concerns about the welfare of poultry kept in strict confinement in large farm complexes and Argas may yet strike again.

Tick control on dogs in particular is advocated by the use of acaricide-impregnated collars, whereas individual treatment for horses usually consists of synthetic pyrethroid pour-on compounds.

CONCLUDING REMARKS

The impact of tick feeding and tick-transmitted diseases and their control should be much better defined in economic terms. Tick control on livestock remains to a large extent based on acaricides but their use in possible combination with anti-tick vaccines and utilization of host resistance to ticks should reduce dependency on chemical tick control. Research into novel, ecologically sound, practical tick control methods should be intensified and implementation of existing methods to vaccinate against tick-borne diseases is recommended, as well as intensified research towards developing novel vaccines and delivery systems.

Much progress is expected in the next few years by the use of tools available in the post-genomic era. It can also be expected that new tick-borne pathogens will continue to be discovered. Furthermore, in the future we may be able to exploit for medical purposes some of the considerable number of bio-active molecules of the fascinating largely undisclosed tick pharmacy (see chapter by Valenzuela in this Supplement).