An arthropod is considered a vector when it is able to guarantee both the survival, within its own body, of one or more stages of the life cycle of a pathogenic unicellular or pluricellular organism and transmission of the organism. The vector is defined biological when the pathogen develops or multiplies within the arthropod before it is transmitted in an infective/infesting form to a susceptible host, whereas the vector is defined mechanical when the arthropod transmits an organism from an infected host to a healthy host without the pathogen undergoing any modification of development within the arthropod itself.
The capacity of many arthropods to transmit pathogenic agents to animals and humans is the result of a long process of evolution and adaptation which has gradually been established between the ectoparasite and its hosts from which the arthropod takes a blood meal. Indeed, blood is the main route through which arthropods, in most cases, transmit pathogenic organisms.
Females of arthropods such as ticks, mosquitoes, sand-flies and fleas require a blood meal in order to guarantee their gonotrophic cycle and deposition of eggs; the number of eggs produced and laid is directly proportional to the amount of blood taken from the host. Given these biological requirements, many arthropods have adapted to ectoparasitic life, managing to overcome the defence mechanisms of both animals and humans.
The ability to draw blood from a vertebrate host has led, over time, to the establishment of a complex interaction not only between the ectoparasite and the host but also between the ectoparasite and the pathogen. The pathogen’s survival, development and capacity to infect the vertebrate host are, therefore, strictly dependent on its arthropod vector. A multifactorial equilibrium in the interactions between vertebrate host/pathogen/invertebrate vector has been established: each component of the equilibrium has the aim of ensuring the survival of the others and, in fact, of promoting the widest spread of the pathogen within the populations of receptive hosts. The mechanisms put into play by the various protagonists of this delicate balance are usually very complex although ranging from the (relatively) simple capacity of some nematodes to develop in the vector in an infesting form, to the more sophisticated capacity of some protozoa to invade the ovaries of the arthropod in order to transmit their own progeny.
There are very “specialised” arthropods, in which the relationship with the pathogen that it transmits is ‘exclusive’ (e.g., Leishmania and sand-flies) and less specialised arthropods, such as ticks and mosquitoes, in which this relationship is less specific and the arthropods are vectors of various different types of pathogens.
The biological relationships that have evolved over time between pathogens and their own vectors are very close. A good example is the relationship between ticks and many of the micro-organisms that they transmit. The ability of a given species of tick to act as a vector depends on the pathogen’s capacity not only to survive and overcome the various barriers it encounters in its invertebrate host but also to exploit the host to continue its own life cycle. Babesia is able to survive in the salivary glands of the tick during the moults from larva to nymph and from nymph to adult, in this way increasing the possibility of being transferred to the vertebrate host during a blood meal. Another very close relationship is that between Leishmania and sand-flies: the morphological and functional alterations of the protozoon, which must change from an amastigote to a metacyclic promastigote (which infects the vertebrate at the next blood meal) in the insect, are aimed at ensuring both its own survival in the digestive tract of the insect and the survival of its vector, the phlebotomine sand-fly. The capacity of Leishmania to induce functional modifications in the host sand-fly is especially interesting; in particular, the metacyclic promastigotes accumulate at the stomodeal valve of the sand-fly and prevent the normal flow of blood in the insect’s digestive system. This functional modification changes the insect’s behaviour, inducing it to search frantically for a blood meal and feed for longer times, thus increasing the possibility that the vector transmits the protozoon.
Muscidae are among the mechanical vectors most widely involved in the transmission of pathogens; this is related to some morphological aspects of these insects. In fact, the morphology and the structure of flies make these insects particularly well adapted to carrying various pathogenic organisms: the proboscis is densely covered by hairs and the feet and foot-pads can carry viscous substances capable of attaching numerous micro-organisms. Furthermore, the habit of some species of feeding on decomposing matter (e.g. faeces, rubbish) indicates that these insects can potentially transmit a wide range of viruses, bacteria and protozoa. More than 100 different pathogenic organisms have been isolated from Musca domestica and, of these pathogens, more than half can be transmitted. Finally, vomiting, which is common in Muscidae, promotes mechanical transmission because pathogenic micro-organisms previously ingested from infected animals can, during the phase of feeding on another host, be easily transferred onto mucosa that has already been damaged by the action of the buccal apparatus of the insect. Furthermore, it should not be overlooked that some flies can act as intermediate hosts for some parasites that pass part of their life cycle within the Diptera, such as ocular nematodes of the genus Thelazia and equine nematodes of the genus Habronema (Fig. 1).
EPIDEMIOLOGY OF ARTHROPOD-BORNE DISEASES
Many arthropod-transmitted diseases are considered (re)-emerging, especially because of the major changes that have influenced them and their epidemiology. In recent years important ecological, sociological and phenological alterations have influenced the presence and spread of both arthropod vectors and the pathogens transmitted by them and, for this reason, many vector-borne diseases are emerging, with a consequent increase in their importance to health both in already endemic areas and in previously unaffected areas.
Temperature, humidity and general environmental conditions are the main factors influencing the survival and development of both vectors and pathogens and, for this reason, one of the factors most strongly implicated in the current increase in the spread and distribution of arthropod-borne diseases is the global warming of the planet. Since the physiological processes of many invertebrates depend largely on the ambient temperature, the distribution of vector-borne diseases is strongly influenced by the increase in the temperature. Indeed, it seems that changes in climate have altered the geographical distribution of various diseases, challenging some previously firmly rooted “scientific paradigms”, such as the belief that heartworm is confined to the northern regions of Italy while leishmaniasis is limited to the southern regions. It has been seen in many Mediterranean regions, Italy included, that while some vectors (e.g., sand-flies) continue to show a typical seasonal activity, other arthropods, such as ticks, fleas and some species of mosquitoes, are now active throughout the whole year as a result of changes in environmental conditions. The areal of distribution of many arthropods is changing and, for this reason, host animals are now permanently at risk of arthropod-borne diseases in many geographical settings. Some species of tick have become adapted to living in urban environments, where the climate and domestic microhabitat promote the completion of their life-cycle and, consequently, the risk of transmission of pathogens not only to pets but also to humans has increased. Similar considerations apply to some species of fleas and the infections they transmit; in some geographical settings dogs can be infested throughout the year, in this way running the continuous risk of being infected by various micro-organisms transmitted by the ectoparasites (e.g., Bartonella). Another important example is that of mosquitoes and Dirofilaria; in recent years there has been a tendency for filariae to appear in geographical areas previously considered uninvolved and there has also been an increase in the number of infections in areas in which the parasite was already present. In fact, experimental models have confirmed that the increased temperature not only favours the life cycle of mosquitoes and the introduction of new species into previously uninvolved zones, but also the rate of development of the Dirofilaria within the mosquitoes themselves.
The reported autochthonous foci of canine leishmaniasis in numerous regions of northern Italy in recent years constitute a good example of how many arthropods, in this case sand-flies, are colonising new ecological niches. The distribution and prevalence of canine leishmaniasis in Italy are strongly related to the seasonal behaviour of the sand-flies and, in particular, of Phlebotomus perniciosus (Fig. 2), the most important vector of Leishmania in the Mediterranean area. This vector is normally present between June and October, but possible future changes in the seasonal behaviour of sand-flies should not be excluded. Such changes could cause an increase, also temporal, in the risk of infection by Leishmania.
It is, however, worth clarifying that although changes in the climate play an important role in increasing the areal of diffusion of many arthropod-borne pathogens, other variables are able to affect the distribution of the vectors and the diseases they transmit. Such factors include movement of animal (pets and livestock) and the now consolidated international trading. Indeed, the movement of animals can lead to the introduction of new species of pathogens into previously uninvolved geographical zones. As far as regards livestock and sporting animals (e.g., ruminants and horses), arthropod-borne diseases (such as babesiosis) for which the host animal’s immune system plays a particularly important role are the source of particular concern because infections introduced into previously uninvolved regions can have a major impact on the animals’ health.
As far as concerns pets, changes in the dynamics of human-animal interrelations, closer contact and the consequent increase in the movement of animals (e.g., for shows, tourism, holidays, hunting) have facilitated the spread not only of the vectors but also of the pathogens in different vertebrate and invertebrate host populations. The increase in the number of dogs and the social role of these animals raise new problems for public health in that many vectors feed on blood from animals and humans and can, therefore, act as a potential reservoir for the transmission of various zoonotic micro-organisms.
Another change that contributes to the spread of vector-borne diseases is the habit of considering as pets (to be kept in the house or garden) so-called “non-conventional animals” such as ferrets, which are potential hosts of Dirofilaria, or hedgehogs, which host some species of ticks (Ixodes), the vectors of Borrelia, which is a zoonotic pathogen.
Commercial trade can be a cause of the spread of vectors able to transmit infections/infestations into new geographical areas, a phenomenon well demonstrated by Aedes albopictus. This species of mosquito, known as the tiger mosquito, originated from Asia, but was introduced into Italy with a cargo of used tyres (from the USA). A. albopictus, a proven vector of canine and feline filariae, has adapted very well to the Italian climate, spreading throughout the country and, probably, contributing to the increase in the areal of distribution of Dirofilaria in Italy. This situation is very important because A. albopictus has a marked predilection for humans and, therefore, considering the zoonotic potential of filariae, also represents a problem for public health.
Other changes in the habits of society, for example, urbanisation of suburban areas, a return to nature with the creation of housing units far from cities, with many green areas, can underlie a further risk of vector-borne diseases. In fact, walks in woods or forest areas, as well as tourism centred around the countryside or stables, increase the possibility of humans being a source of food for arthropods, such as ticks, able to transmit zoonotic pathogens (e.g., Rickettsiales) and also increase the possibility of there being important reservoirs in wild animals. Likewise, residential green areas and peri-urban zones can enable vectors such as mosquitoes, sand-flies and ticks, to survive and reproduce, thanks to ecological conditions created by the very inhabitants of the area (ponds, artificial ravines, etc.) and to the presence of wild or semi-domestic hosts (voles, mice, rats), which can be a supply of blood meals for the arthropods and, at the same time, can host one or more zoonotic pathogens (e.g., Leishmania).
Another important and indeed dramatic phenomenon that favours the presence of ectoparasites and the pathogens that they transmit is that of stray animals. The risk that stray dogs and/or cats, whether living freely in the environment or kept in shelters, can harbour vector-borne pathogens is very high both because such animals rarely receive systematic antiparasite treatment and because the general conditions of these animals (e.g. malnutrition or concomitant diseases) can contribute to making them susceptible to many diseases, including those transmitted by arthropods. When carrying parasites, these animals act as mobile reservoirs for the populations of ectoparasites in the territory which can, in their turn, contribute to the propagation of various infectious agents and parasites among domestic animals and also among the human population.
The conservation of wildlife and the increase in the number of wild animals are other variables that could have contributed in recent years to the emergence of arthropod-borne diseases. In fact, many wild species (e.g., ungulates) are able not only to support heavy tick infestations, but also supply the ectoparasites “protection” and generous blood meals since they do not receive any antiparasite treatment. In this way they favour the life cycle of the vectors and enable their increase in the territory. This situation is further aggravated by the fact that many wild ungulates, although hosting tick-borne pathogens, do not show any clinical signs of infection. For example, the immature stages of Ixodes ricinus feed on small rodents whereas the adults (Fig. 3) feed on deer or other large mammals and, in the absence of clinical signs, play an important role in the spread of Borrelia.
Another biological feature that has contributed to the growing importance of arthropod-transmitted diseases is the increased frequency of co-infections. In fact, many arthropods can act as vectors for several pathogens, thus being able to transmit single or multiple infections, particularly in vertebrate hosts that live in endemic zones and/or in areas in which the density of the vectors is high. The vectors may ingest several pathogens after a single blood meal on a host with multiple infections or contract infections after feeding, at different stages of development, on several infected hosts enabling trans-stadial transmission of pathogens. In both cases the role of the different hosts that can act as reservoirs (e.g., rodents, dogs, deer), possibly infected by several pathogens, is of fundamental importance in maintaining the enzootic cycle.
Both single infections and co-infections also depend on the complex interactions of the pathogens in vertebrate and invertebrate hosts. It seems that Leishmania plays a primary role as a factor predisposing to infection by other pathogens. In fact, ehrlichiosis and leishmaniasis are among the most frequent canine co-infections found in endemic regions. In dogs with leishmaniasis, the altered cellular and humoral immune responses seem to contribute to an exacerbation of subclinical forms of ehrlichiosis. Another variable to consider is the possibility that an interaction between several pathogens can cause more profound immunosuppression which is, therefore, more clinically relevant than that caused by a single pathogen.
PREVENTION AND CONTROL
In conclusion, the infectious and parasitic diseases transmitted by arthropods are a daily danger to both livestock and pets and, therefore, the application of appropriate and effective methods of control is the most efficient way to counter risks related to these diseases in the context of public health and veterinary medicine.
The control of these infections and infestations requires a holistic approach based on the knowledge of both the distribution and ecology of the vectors and pathogens that they can transmit, as well as the pathogenic action exerted by the vectors and the organisms transmitted. Compounds with insecticidal/acaricidal activity are useful, particularly considering the large number of formulations available on the market. The main characteristics that these compounds must have are low toxicity to humans, animals and the environment, manageability, knockdown activity, residual activity and, possibly, repellent activity. Repellent activity is a characteristic of some compounds (e.g., deltamethrin, permethrin) and consists in the capacity of the product to provoke the detachment of the parasite before it feeds on the host, although it does not completely exclude contact between the invertebrate and its vertebrate host. The use of repellent substances is very important because these substances protect the animal for a long period preventing the parasitic activity of the arthropod, any inoculation of pathogens and, ultimately, the circulation of the pathogens among the vertebrate and invertebrate hosts.
The numerous antiparasitic compounds with insecticidal and/or acaricidal activity are available in various different formulations, for example, forpour-on, baths and sponging, as sprays, powders, and collars and in spot-on pipettes. There are also formulations containing combinations of different compounds which guarantee synergic activities and/or knockdown plus residual effects or, in other cases, even the possibility of a broader spectrum of action, extended to endoparasites.
Since the spread and risk of infections/infestations vary depending on the geographical and seasonal distribution of the respective vectors, the veterinarian must have full knowledge of the epidemiological aspects in the area in which he or she works before suggesting prophylactic or control interventions. In fact, the success of treatment and prophylaxis of ectoparasites and the diseases they transmit depends not only on the appropriate use of commercially available products, but also on an understanding of the biology and epidemiology of the vector(s) in a given geographical area or region.
Suggested readings
- Genchi C., Marinculic A., 2007. Zecche e malattie trasmesse. Supplemento de La Settimana Veterinaria n. 566 del 30 maggio 2007, pp 7-22.
- Genchi C., Venco L., Genchi M., 2007. Pulci e zecche: controllare e prevenire le infestazioni. Supplemento de La Settimana Veterinaria n. 566 del 30 maggio 2007, pp 25-30.
- Giangaspero A., Otranto D. 2010. Ectoparassiti ed artropodi vettori. In: Parassitologia e Malattie Parassitarie degli Animali. A cura di Garippa G., Manfredi M.T., Otranto d. Edizioni Mediche Scientifiche Internazionali, Roma, pp. 679-708.
- Otranto D., 2008. Aspetti critici nel controllo delle CVBD. Supplemento de La Settimana Veterinaria n. 611 del 4 giugno 2008, pp 25-30.
- Otranto D., Dantas-Torres F. 2010. Canine and feline vector-borne diseases in Italy: current situation and perspectives. Parasites and Vectors, 3: 2.
- Otranto D., Dantas-Torres F., Breitschwerdt E.B. 2009. Managing canine vector-borne diseases of zoonotic concern: part one. Trends in Parasitology 25 (4): 157-163.
- Otranto D., Dantas-Torres F., Breitschwerdt E.B. 2009. Managing canine vector-borne diseases of zoonotic concern: part two. Trends in Parasitology 25 (5): 228-235.